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EBP Project Evaluations (20 points); DUE 9/22/2016 at 7:00AM.

Complete the following questions using this template. Upload a word


document or PDF to the Compass portal prior to the project deadline.
Name: _______________Caitlyn Edwards______________________
Group Number, Disease, and Nutrient(s): 1, Diabetes, Fiber
Part A: Individual & Group Member Evaluations (10 points)
Question 1. List the members of your group, including yourself, (first and last
name) and the paper each member reviewed for the EBP Project.
Group Member Name ______Kimber Schrowang________________
Papers reviewed (full paper reference)
Chen, C., Zeng, Y., Xu, J., Zheng, H., Liu, J., Fan, R., Wang, J. (2016). Therapeutic
effects of soluble dietary fiber consumption on type 2 diabetes mellitus.
Experimental and Therapeutic Medicine, 12321242.
http://doi.org/10.3892/etm.2016.3377
Group Member Name ___Ariel Robinson___________________
Papers reviewed (full paper reference)
Jiang, J., Qiu, H., Zhao, G., Zhou, Y., Zhang, Z., Zhang, H., Xu, W. H. (2012). Dietary
Fiber Intake Is Associated with HbA1c Level among Prevalent Patients with Type 2
Diabetes in Pudong New Area of Shanghai, China. PLoS ONE, 7(10).
http://doi.org/10.1371/journal.pone.0046552
Group Member Name _____Jessica Park_________________
Papers reviewed (full paper reference)
Jiang, J., Qiu, H., Zhao, G., Zhou, Y., Zhang, Z., Zhang, H., Xu, W.-H. (2012). Dietary
Fiber Intake Is Associated with HbA1c Level among Prevalent Patients with Type 2
Diabetes in Pudong New Area of Shanghai, China. PLoS ONE, 7(10), e46552.
http://doi.org/10.1371/journal.pone.0046552
Group Member Name _____Ria Thakur_________________
Papers reviewed (full paper reference)
Lubia Velzquez-Lpez, Abril Violeta Muoz-Torres, Carmen Garca-Pea, Mardia
Lpez-Alarcn, Sergio Islas-Andrade, and Jorge Escobedo-de la Pea, Fiber in Diet
Is Associated with Improvement of Glycated Hemoglobin and Lipid Profile in
Mexican Patients with Type 2 Diabetes, Journal of Diabetes Research, vol. 2016,
Article ID 2980406, 9 pages, 2016. doi:10.1155/2016/2980406

Group Member Name ____Grace Kim__________________


Papers reviewed (full paper reference)
Manisha Chanalia ,M.D.,Abhimanyu Garg,M.D., Dieter Lutjhonatann,PH.D., Klaus von
BErgmann,M.D., Scott M.Grundy,M.D.,Ph.d.,and Linda J. Brinkley, R. D. (2015).
Beneficial Effects of High Dietary Fiber Intake in Patients With Type 2 Diabetes
Mellitus.
Group Member Name _____Caitlyn Edwards_________________
Papers reviewed (full paper reference)
Ziai, S. A., Larijani, B., Akhoondzadeh, S., Fakhrzadeh, H., Dastpak, A., Bandarian, F., ...
Emami, T. (2005). Psyllium decreased serum glucose and glycosylated hemoglobin
significantly in diabetic outpatients. Journal of Ethnopharmacology, 102(2), 202
207. http://doi.org/10.1016/j.jep.2005.06.042
Question 2. Briefly describe the process your group utilized to complete the project.
Include in your process description the contributions of each group member,
including yourself. How many points would you award to each of your group
members? How many points would you award yourself. Justify your responses: 10
is the highest score and 0 is the lowest score.
Process overview/comments:
For this EBP we didnt want to get together every time something was due so we
assigned certain aspects of the project after each class and utilized Google Docs,
Sheets, and Folders to get everything done.
SELF EVALUATION (name): ____Caitlyn Edwards__
Score (0-10): 10
Justification: I completed my portions of the project in a timely manner, and assisted
my undergraduate group mates when help was needed.
Group member name: ____Kimber Schrowang____
Score (0-10): __10____
Justification: She worked hard on her aspects of the project and got everything done
in advance.
Group member name: __Ariel Robinson__
Score (0-10): ____10_______
Justification: She worked really hard to get her work done on time, and contributed
a lot despite being sick the last week of the project.
Group member name: ___Jessica Park_
Score (0-10): _____10______
Justification: She was a motivator for the group, the first to jump in and offer to get
assignments started.

Group member name: ___Ria Thakur________________


Score (0-10): __10
Justification: She completed all aspects of her portion of the project and was always
up to assist others.
Group member name: _____Grace Kim_______
Score (0-10): _____10_______
Justification: She always checked assignments in advance, and was always ready to
help whenever needed.

Part B. EBP Project Evaluation (10 points).


Question 1. Evaluate the EBP project.
How did working with your group to complete the EBP project compare to the level
of learning you would have achieved by reading about EBP or listening to a
classroom lecture (e.g. no opportunity to apply the information/skills learned).
Working together was really great for the first portion of the EBP that required
researching papers and utilizing different websites to find articles. It was also nice
to check each others QCCs and realize that articles can be interpreted different
ways. That couldnt have been conveyed through a lecture. I dont feel like I learned
a lot about diabetes and fiber though (our topic and nutrient!), so I would have
preferred lecture, but I do have a nice overview of the literature to reference now!
Question 2. Discuss the strengths and weaknesses of the EBP assignment. At least
one strength and one weakness should be discussed. Provide constructive criticism,
e.g. clearly state the weakness(es) of the project and make suggestions for
improving that weaknesses or hurdles to student learning.
Strength: Finding articles is an art, and it was nice to get more practice doing that. I
wish that I had more of that in my undergraduate degree program.
Weaknesses: I am computer illiterate, but making a video took probably longer
than it did to make the PowerPoint. I would have preferred an extra long paper over
using Illinois Media Space! Perhaps next semester the TA could rent a room in the
computer lab for an hour and just be there to provide support on that side of the
project!
Other Comments/Reflections: In Dr. Ahns Systematic Review class we had a
librarian from the UOI come in and explain how she uses Pubmed and Library
sources I think undergraduates could really benefit from that!

Author, Year,
Study Design,
Class, Rating

Population

Ziai S. A. et al, 2005 N= 49


Study Design:
Randomized
Control Trial

Intervention Group = 21
age 51.92.2

Class: A
Rating: Neutral

Control Group = 15 age


53.62.1

Jiang, J. et al, 2012

N= 1897

Study Design:
Cross-Sectional
Study

Diabetic Group =979


Age 57.7 9.9

Class: D
Rating: Positive

Non-diabetic Group=
918 Age 65 10.1

Intervention

Outcomes

Conclusions

Limitations

Participants
were randomly
assigned to
receive either
5.1 g psyllium
(Intervention
Group) or a
microcrystalline
cellulose
placebo (Control
Group) once
before breakfast
and once before
dinner for 8weeks on top of
their regular
diets and
chemical drugs.
Not Applicable.

8 weeks treatment with 5.1g


psyllium two times daily half an
hour before breakfast and dinner
could reduce FBS and control
glucose fluctuations by reducing
HbA1c significantly (p<0.05, exact
significance not disclosed).

5.1 g b.i.d. of
psyllium is useful
as an adjunct to
dietary therapy and
to reduce glucose
in patients with
type II diabetes.

Participant
demographic
information wasnt
disclosed, including
gender.

HbA1c levels and dietary fiber were


negatively correlated, and HbA1c
levels were consistently higher in
patients consuming lower levels of
fiber no matter how long a patient
was diabetic.

Dietary fiber may


play an important
role in reducing
HbA1c level.
Increasing fiber
intake may be an
effective approach
to improve
glycemic control
among Chinese
diabetic patients.

The Non-Diabetic
group was about 10
years older than the
Diabetic Group.

Author, Year,
Study Design,
Class, Rating
Lubia VelzquezLpez, Abril Violeta
Muoz-Torres,
Carmen GarcaPea, Mardia
Lpez-Alarcn,
Sergio IslasAndrade, and Jorge
Escobedo-de la
Pea, 2016
Study Design: Cross
Sectional Study
Class: D
Rating: Neutral

Population

N= 395
Type 2
diabetic
Mexican
patients, <70
years old,
54.6 +/- 8
years
average age,
Mexico
City, part of
another
randomized
clinical trial

Intervention

Outcomes

HbA1c, fasting
glucose,
triglycerides,
and lipids
profile were
measured.
Weight, waist
circumference,
blood
pressure, and
body
composition
were
measured.
Everyday
diet with a
semiquantitative
food
frequency
questionnaire
was evaluated.
The
participants
followed
their current
everyday
diet.

55% had hypertension, 26% had


diabetic neuropathy, 12% had
microalbuminuria, and 5% had
macroalbuminuria.
Only 34% had a desirable
HbA1c; total cholesterol was within
control range for over 50% of the
population, whereas triglycerides,
LDL-c, and HDL-c were found to
be within normal range in only third
of the subjects. positive association
between high calorie
consumption and glucose levels,
while lower consumption of total
and saturated fat was associated
with higher levels of HDL-c. A
higher intake of fiber in
the diet was significantly
linked to lower levels of HbA1c and
triglycerides and HDL-c
improvement.

Conclusions

A higher
content of
fiber in the diet
had an impact
on
reducing
HbA1c and
triglycerides,
while
improving
HDL-c
levels.

Limitations

Looked at
one race of
people.
No specific
diet was
given.

Author, Year,
Study Design,
Class, Rating
Manisha Chanalia
,M.D.,Abhimanyu
Garg,M.D., Dieter
Lutjhonatann,PH.D.,
Klaus von
BErgmann,M.D.,
Scott
M.Grundy,M.D.,Ph.
d.,and Linda J.
Brinkley, R. D.
(2015).
Study Design:
Randomized
Crossover Study
Class: A
Rating: Neutral

Population
N=13; 12 male, 1
female; 61
9 years (4570), 9 nonHispanic whites/4
blacks: mean
body weight: 93.5 12.7
kg;
mean body mass index:
32.3 3.9;
Dallas, USA

Intervention
High-fiber diet
containing 50g
total
fiber (25g
soluble, 25g
insoluble)
vs.ADA diet
containing 24g
of total
fiber (8g
soluble, 16g
insoluble)

Outcomes

Conclusions

Limitations

Mean plasma glucose concentration


was lower (by 13 mg per deciliter or
by 8.9 percent) in high-fiber diet
than ADA diet. Mean daily urinary
glucose excretion was 1.3 g lower.
Daily plasma glucose concentration
were ten percent lower with
highfiber diet, (3743944 vs
33651003 mg*hr/deciliter), and
plasma insulin concentrations were
12 percent lower (1107650 vs
971491 Uhour per milliliter)
Glycosylated hemoglobin values
were lower after high-fiber diet.
Lower fasting plasma total
cholesterol concentration by 6.7
percent, lower plasma triglyceride
concentration by 10.2 percent and
lower plasma VLDL cholesterol
concentration by 12.5 percent.
Fasting plasma LDL cholesterol
concentration was 6.3 percent
lower.
Gastrointestinal absorption of
cholesterol was decreased by ten
percent and fecal acidic sterol
excretion increased by 41 percent.

High-fiber diet
improved
Glycemic control,
lowered
Glycosylated
hemoglobin
values;
specifically,
increase in intake
of total
dietary fiber which
consists
predominantly of
soluble fiber,
significantly
improved glycemic
control and
decreased degree
of
hyperinsulinemia
in patients with
type 2 diabetes.

There werent a variety


of participants; 12 men
and 1 woman and 10
received glyburide
while 3 did not.

Author, Year,
Study Design,
Class, Rating

Population

Intervention

Outcomes

Conclusions

Limitations

Chen C et. Al, 2016

N = 120 males and


females with DM2 54 9
years of age; body
weight 68.113.0 kg;
BMI 25.33.9 kg/m2
Chinese Free of tumors,
MI, unstable angina
pectoris and CHF; no
thyroid or hepatic
disease; no lipidlowering
treatments

40 patients
received either
no extra fiber
compared to the
ADA diet and
80 patients
received either
10g of dietary
fiber or 20g of
dietary fiber in
addition to the
ADA diet

Systolic pressure of HDL, LDL and


apoB were significantly improved
in the 20DF group compared to
prior treatment.

MNT improved 2h glucose and


fasting levels and
the insulin
resistance index.
Also, effective in
maintaining
glycemic control

The Treatment groups


varied greatly in size.

926 DM2 918 C, mean


age 64.510.1 years
Chinese Residents within
specified communities;
no occurrence of CV
event within past 6
months, congestive heart
failure, unstable angina,
major depression, or
dementia

Diabetic control
status was
observed among
patients with
DM2 and those
without in
association to
dietary factors

HbA1c levels were negatively


correlated with DF intake (r=0.079, p=0.017)

Regardless of
duration of DM2,
HbA1c levels were
consistently lower
in patients
consuming higher
amounts of DF

Potential for recall bias


as amount of energy
intake appeared lower
than those reported in
previous studies.

Study Design:
Randomized,
controlled
experiment
Class: A
Rating: Positive

Jiang J et. Al, 2012


Study Design:
Cross-sectional
study
Class: D
Rating: Positive

Academy of Nutrition and Dietetics


Evidence Analysis Library Worksheet Template and
Quality Criteria Checklist: Primary Research

Citation

Ziai, S. A., Larijani, B., Akhoondzadeh, S., Fakhrzadeh, H., Dastpak, A., Bandarian,
F., Emami, T. (2005). Psyllium decreased serum glucose and glycosylated
hemoglobin significantly in diabetic outpatients. Journal of Ethnopharmacology,
102(2), 202207. http://doi.org/10.1016/j.jep.2005.06.042 (completed by Ariel
Robinson)

Study Design

Randomized Control Trial

Class

Quality Rating
Research Purpose
Inclusion Criteria

Exclusion Criteria

+ (Positive)

- (Negative)

x (Neutral)

To determine the effects of Psyllium seeds on fasting plasma glucose (FBS),


glycosylated hemoglobin, cholesterol, and triglyceride levels in Type 2 Diabetecs.
Volunteers between the ages of 35-70 whose diabetes was controlled with diet
only, or diet plus glibenclamide or metformin.
If subjects were receiving lipid-lowering drugs, corticosteroids, other soluble fiber
treatment, lithium, carbamazepin, warfarin, digoxin or patients with clinically
significat renal, hepatic, gastrointestinal, pulmonary, and thyroid disease.
People with a history of myocardial infarction, or people who've had major sugical
procedures within the previous 6 months, and have a history of allergy to
aspartame or psyllium seed, or phenylketonuria.
People with a fasting Plasma Glucose, total Cholesterol, triglycerides, and HbA1c
more than 400, 300, and 500 mg/dl and 13% respectively were also excluded.
Recruitment: Participants from the Institue of Medicinal Plants volunteered to
participate in the study.
Design: Randomized Control Trial
Blinding used (if applicable): Double-blind, Parrallel, Placebo Controlled Trial
Intervention (if applicable): Participants consumed their regular diets and
assigned chemical drugs for 8-weeks The patients randomly assigned to receive

Description of
Study Protocol

either 5.1 g psyllium or a placebo to consume twice daily.


Statistical Analysis: A one-way repeated measures analysis of variance with a
two-tailed post hoc Tukey mean comparison test was used on dependent
variables. To compare the change in FBS, TC, LDL-C, HDL-C, TB, and insulin from
beginning to end a paired two-sided Student's t-tests was used and a Kruskal-
Wallis test was employed to compare the baseline data and frequency of side
effects between two groups.

Data Collection
Summary

Timing of Measurements: All participants were seen two weeks apart, starting at
baseline (week 0).
Dependent Variables: Body weight, blood preassure, fasting serum levels of

glucose, HbA1c, insulin, and lipid profile.


Independent Variables: Level of Fiber consumed over the treatment period.
Control Variables: Chemical Drugs used to treat Diabetes
Initial: 49 (Intervention: 21, Control: 15) (N/A Males N/A Females)
Attrition (final N): 36
Age: Intervention: 51.9 S.E. 2.2, Control: 53.6 S.E. 2.1
Description of
Ethnicity: N/A
Actual Data Sample
Other relevant demographics: N/A
Anthropometrics: BMI Intervention: 26.6 SE 1.0, BMI Control: 27.5 S.E. 0.9
Location: Tehran, Iran
Key Findings: 8 weeks treatment with 5.1 g psyllium two times daily half and hour
before breakfast and dinner could reduce FBS and control glucose fluctuations by
reducing HbA1c significantly.
Summary of Results


Other Findings: This intervention reduced TB non-significantly but had no effect
on the total cholesterol and LDL-C. HDL-C increased in the intervention group.
5.1 g b.i.d. of psyllium is useful as an adjunct to deitary therapy in patients with

Author Conclusion
Reviewer
Comments

type II diabetes, to reduce glucose, with excellent tolerance.


A very well written paper. I would have like to see results from a larger scaled
study.
The Endocrinology and Metabolism Research Center of Tehran University of

Funding Source

Medical Sciences

Quality Criteria Checklist: Primary Research


Symbols Used
+
--
x

Explanation
Positive Indicates that the report has clearly addressed issues of inclusion/exclusion,
bias, generalizability, and data collection and analysis
Negative Indicates that these issues have not been adequately addressed.
Neutral indicates that the report is neither exceptionally strong nor exceptionally
week
Select a rating from the
drop-down menu

Relevance Questions
1. Would implementing the studied intervention or procedure (if found successful) result
in improved outcomes for the patients/clients/population group? (NA for some Epi
studies)
2. Did the authors study an outcome (dependent variable) or topic that the
patients/clients/population group would care about?
3. Is the focus of the intervention or procedure (independent variable) or topic of study a

Yes

Yes

Yes

common issue of concern to dietetics practice?


4. Is the intervention or procedure feasible? (NA for some epidemiological studies)

Yes

If the answers to all of the above relevance questions are Yes, the report is eligible for designation with a
plus (+) on the Evidence Quality Worksheet, depending on answers to the following validity questions.
Validity Questions
1. Was the research question clearly stated?
1.1. Was the specific intervention(s) or procedure (independent variable(s))
identified?
1.2. Was the outcome(s) (dependent variable(s)) clearly indicated?
1.3. Were the target population and setting specified?
2. Was the selection of study subjects/patients free from bias?
2.1. Were inclusion/exclusion criteria specified (e.g., risk, point in disease
progression, diagnostic or prognosis criteria), and with sufficient detail and
without omitting criteria critical to the study?
2.2. Were criteria applied equally to all study groups?
2.3. Were health, demographics, and other characteristics of subjects described?
2.4. Were the subjects/patients a representative sample of the relevant
population?
3. Were study groups comparable?
3.1. Was the method of assigning subjects/patients to groups described and
unbiased? (Method of randomization identified if RCT)
3.2. Were distribution of disease status, prognostic factors, and other factors (e.g.,
demographics) similar across study groups at baseline?
3.3. Were concurrent controls used? (Concurrent preferred over historical
controls.)
3.4. If cohort study or cross-sectional study, were groups comparable on important
confounding factors and/or were preexisting differences accounted for by using
appropriate adjustments in statistical analysis?
3.5. If case control study, were potential confounding factors comparable for cases
and controls? (If case series or trial with subjects serving as own control, this
criterion is not applicable. Criterion may not be applicable in some cross-
sectional studies.)
3.6. If diagnostic test, was there an independent blind comparison with an
appropriate reference standard (e.g., gold standard)?

1.3

Yes
Yes
Yes
Unclear

Yes

2.1

Unclear

2.2

Yes

2.3

No

2.4

Unclear

Yes

3.1

Yes

3.2

Unclear

3.3

Yes

3.4

Yes

3.5

N/A

3.6

N/A

Yes

4.1

Unclear

4.2

Yes

4.3

Yes

4.4

No

4.5

N/A

Yes

5.1

Yes

5.2

Yes

5.3

No

1
1.1
1.2



4. Was method of handling withdrawals described?
4.1. Were follow up methods described and the same for all groups?
4.2. Was the number, characteristics of withdrawals (i.e., dropouts, lost to follow
up, attrition rate) and/or response rate (cross-sectional studies) described for
each group? (Follow up goal for a strong study is 80%.)
4.3. Were all enrolled subjects/patients (in the original sample) accounted for?
4.4. Were reasons for withdrawals similar across groups
4.5. If diagnostic test, was decision to perform reference test not dependent on
results of test under study?
5. Was blinding used to prevent introduction of bias?
5.1. In intervention study, were subjects, clinicians/practitioners, and investigators
blinded to treatment group, as appropriate?
5.2. Were data collectors blinded for outcomes assessment? (If outcome is
measured using an objective test, such as a lab value, this criterion is assumed
to be met.)
5.3. In cohort study or cross-sectional study, were measurements of outcomes and
risk factors blinded?

5.4. In case control study, was case definition explicit and case ascertainment not
influenced by exposure status?
5.5. In diagnostic study, were test results blinded to patient history and other test
results?
6. Were intervention/therapeutic regimens/exposure factor or procedure and any
comparison(s) described in detail? Were intervening factors described?
6.1. In RCT or other intervention trial, were protocols described for all regimens
studied?
6.2. In observational study, were interventions, study settings, and
clinicians/provider described?
6.3. Was the intensity and duration of the intervention or exposure factor sufficient
to produce a meaningful effect?
6.4. Was the amount of exposure and, if relevant, subject/patient compliance
measured?
6.5. Were co-interventions (e.g., ancillary treatments, other therapies) described?
6.6. Were extra or unplanned treatments described?
6.7. Was the information for 6.4, 6.5, and 6.6 assessed the same way for all groups?
6.8. In diagnostic study, were details of test administration and replication
sufficient?

7. Were outcomes clearly defined and the measurements valid and reliable?
7.1. Were primary and secondary endpoints described and relevant to the
question?
7.2. Were nutrition measures appropriate to question and outcomes of concern?
7.3. Was the period of follow-up long enough for important outcome(s) to occur?
7.4. Were the observations and measurements based on standard, valid, and
reliable data collection instruments/tests/procedures?
7.5. Was the measurement of effect at an appropriate level of precision?
7.6. Were other factors accounted for (measured) that could affect outcomes?
7.7. Were the measurements conducted consistently across groups?

5.4

N/A

5.5

N/A

Yes

6.1

Yes

6.2

N/A

6.3

No

6.4

Yes

6.5

Yes

6.6

No

6.7

Yes

6.8

N/A

Yes

7.1

Yes

7.2

Yes

7.3

No

7.4

Yes

7.5

Yes

7.6

No

7.7

Yes

Yes

8.1

Yes

8.2

Yes

8.3

Yes

8.4

No

8.5

No

8.6

Yes

8.7

N/A

Yes
Yes
Yes
Yes





8. Was the statistical analysis appropriate for the study design and type of outcome
indicators?
8.1. Were statistical analyses adequately described the results reported
appropriately?
8.2. Were correct statistical tests used and assumptions of test not violated?
8.3. Were statistics reported with levels of significance and/or confidence intervals?
8.4. Was intent to treat analysis of outcomes done (and as appropriate, was there
an analysis of outcomes for those maximally exposed or a dose-response
analysis)?
8.5. Were adequate adjustments made for effects of confounding factors that
might have affected the outcomes (e.g., multivariate analyses)?
8.6. Was clinical significance as well as statistical significance reported?
8.7. If negative findings, was a power calculation reported to address type 2 error?
9. Are conclusions supported by results with biases and limitations taken into
consideration?
9.1. Is there a discussion of findings?
9.2. Are biases and study limitations identified and discussed?
10. Is bias due to studys funding or sponsorship unlikely?

9.1
9.2
10

10.1. Were sources of funding and investigators affiliations described?


10.2. Was there no apparent conflict of interest?

No
10.2 Yes
10.1

MINUS/NEGATIVE (-)
If most (six or more) of the answers to the above validity questions are No, the report should be designated with a minus
(-) symbol on the Evidence Worksheet.
NEUTRAL ()
If the answers to validity criteria questions 2, 3, 6, and 7 do not indicate that the study is exceptionally strong, the report
should be designated with a neutral () symbol on the Evidence Worksheet.
PLUS/POSITIVE (+)
If most of the answers to the above validity questions are Yes (including criteria 2, 3, 6, 7 and at least one additional
Yes), the report should be designated with a plus symbol (+) on the Evidence Worksheet.

Academy of Nutrition and Dietetics


Evidence Analysis Library Worksheet Template and
Quality Criteria Checklist: Primary Research
Citation

Jiang, J., Qiu, H., Zhao, G., Zhou, Y., Zhang, Z., Zhang, H., Xu, W. H. (2012).
Dietary Fiber Intake Is Associated with HbA1c Level among Prevalent Patients with
Type 2 Diabetes in Pudong New Area of Shanghai, China. PLoS ONE, 7(10).
http://doi.org/10.1371/journal.pone.0046552 (completed by Caitlyn Edwards)

Study Design

Cross-sectional

Class

Quality Rating
Research Purpose
Inclusion Criteria

Exclusion Criteria

+ (Positive)

- (Negative)

x (Neutral)

To evaluate the association of dietary factors with diabetic control status among
Chinese patienets with Type 2 Diabetes.
For the diabetes group: adults diagnosed with Type 2 Diabetes according to ADA
criteria. For the group without diabetes: adults without diseases mentioned in
Exclusion Criteria.
For both groups: Occurance of a cardiovascular event during the previous 6
months, advanced congestive heart failure, unstable angina, major dpression and
dementia.
Recruitment: Diabetic Participants were selected from the Diabetes
Administration Rosters, and the non-diabetics participants were spouses and
friends of the Diabetic Participants.
Design: Cross-sectional
Blinding used (if applicable): n/a

Description of
Study Protocol

Intervention (if applicable): n/a


Statistical Analysis: SAS 9.2 was used for statistical analyses. Partial correlations
were conducted to evaluate the linear correlations of HbA1c levels with amounts
of dietary intake. A generalized linear regression model was applied to compare
the average levels of biochemical measurements and average levels of dietary
intake.

Timing of Measurements: Cross-sectional, so only once

Data Collection
Summary

Dependent Variables: Diabetic status or glycemic control status


Independent Variables: Food Frequency Questionnaire responses
Control Variables: n/a
Initial: 1897 - two groups combined, doesn't mention differences in gender

between treatment groups! (6801 Males 1217 Females)


Description of
Actual Data Sample Attrition (final N): 1852
Age: Diabetic Participants: 64.5 (SD, 10.1), Non-diabetic volunteers: 57.7 (SD, 9.9)

Ethnicity: Chinese
Other relevant demographics: Duration of Diabetes, Medical History
Questionnaires, smoking status
Anthropometrics: Body height, Weight, Waist Circumference, hip circumference,
systolic blood pressure, diastolic blood pressure, BMI
Location: Shanghai, China
Key Findings: In regards to fiber, HbA1c levels were negativley correlated with
dietary fiber intake, and regardless of duration of Type 2 Diabetes, HbA1c level
was consistently higher in patients consuming lower levels of fiber.
Summary of Results


Other Findings: A lower-average level of HbA1c related with higher fiber intake,
and a probably protective effect of dietary fiber on glycemic control status.
Their results indicate a potential role of dietary fiber in glycemic control, but still

Author Conclusion
Reviewer
Comments
Funding Source

need to be confirmed.
A very well done cross-sectional. It would have been interesting to see HEI along
with these fiber variables.
Community Health Centers in Pudong New Area of Shanghia, China

Quality Criteria Checklist: Primary Research


Symbols Used
+
--
x

Explanation
Positive Indicates that the report has clearly addressed issues of inclusion/exclusion,
bias, generalizability, and data collection and analysis
Negative Indicates that these issues have not been adequately addressed.
Neutral indicates that the report is neither exceptionally strong nor exceptionally
week
Select a rating from the
drop-down menu

Relevance Questions
1. Would implementing the studied intervention or procedure (if found successful) result
in improved outcomes for the patients/clients/population group? (NA for some Epi
studies)
2. Did the authors study an outcome (dependent variable) or topic that the
patients/clients/population group would care about?
3. Is the focus of the intervention or procedure (independent variable) or topic of study a
common issue of concern to dietetics practice?
4. Is the intervention or procedure feasible? (NA for some epidemiological studies)

Yes

Yes

Yes

N/A

If the answers to all of the above relevance questions are Yes, the report is eligible for designation with a
plus (+) on the Evidence Quality Worksheet, depending on answers to the following validity questions.
Validity Questions
1. Was the research question clearly stated?

Yes

1.1. Was the specific intervention(s) or procedure (independent variable(s))


identified?
1.2. Was the outcome(s) (dependent variable(s)) clearly indicated?
1.3. Were the target population and setting specified?
2. Was the selection of study subjects/patients free from bias?
2.1. Were inclusion/exclusion criteria specified (e.g., risk, point in disease
progression, diagnostic or prognosis criteria), and with sufficient detail and
without omitting criteria critical to the study?
2.2. Were criteria applied equally to all study groups?
2.3. Were health, demographics, and other characteristics of subjects described?
2.4. Were the subjects/patients a representative sample of the relevant
population?
3. Were study groups comparable?
3.1. Was the method of assigning subjects/patients to groups described and
unbiased? (Method of randomization identified if RCT)
3.2. Were distribution of disease status, prognostic factors, and other factors (e.g.,
demographics) similar across study groups at baseline?
3.3. Were concurrent controls used? (Concurrent preferred over historical
controls.)
3.4. If cohort study or cross-sectional study, were groups comparable on important
confounding factors and/or were preexisting differences accounted for by using
appropriate adjustments in statistical analysis?
3.5. If case control study, were potential confounding factors comparable for cases
and controls? (If case series or trial with subjects serving as own control, this
criterion is not applicable. Criterion may not be applicable in some cross-
sectional studies.)
3.6. If diagnostic test, was there an independent blind comparison with an
appropriate reference standard (e.g., gold standard)?

1.2

Yes
Yes

1.3

Yes

Yes

2.1

Yes

2.2

Yes

2.3

Yes

2.4

Yes

N/A

3.1

N/A

3.2

N/A

3.3

Yes

3.4

N/A

3.5

N/A

3.6

N/A

Yes

4.1

Unclear

4.2

Yes

4.3

No

4.4

Unclear

4.5

N/A

N/A

5.1

N/A

5.2

No

5.3

N/A

5.4

N/A

5.5

N/A

N/A

6.1

N/A

1.1



4. Was method of handling withdrawals described?
4.1. Were follow up methods described and the same for all groups?
4.2. Was the number, characteristics of withdrawals (i.e., dropouts, lost to follow
up, attrition rate) and/or response rate (cross-sectional studies) described for
each group? (Follow up goal for a strong study is 80%.)
4.3. Were all enrolled subjects/patients (in the original sample) accounted for?
4.4. Were reasons for withdrawals similar across groups
4.5. If diagnostic test, was decision to perform reference test not dependent on
results of test under study?
5. Was blinding used to prevent introduction of bias?
5.1. In intervention study, were subjects, clinicians/practitioners, and investigators
blinded to treatment group, as appropriate?
5.2. Were data collectors blinded for outcomes assessment? (If outcome is
measured using an objective test, such as a lab value, this criterion is assumed
to be met.)
5.3. In cohort study or cross-sectional study, were measurements of outcomes and
risk factors blinded?
5.4. In case control study, was case definition explicit and case ascertainment not
influenced by exposure status?
5.5. In diagnostic study, were test results blinded to patient history and other test
results?
6. Were intervention/therapeutic regimens/exposure factor or procedure and any
comparison(s) described in detail? Were intervening factors described?

6.1. In RCT or other intervention trial, were protocols described for all regimens
studied?
6.2. In observational study, were interventions, study settings, and
clinicians/provider described?
6.3. Was the intensity and duration of the intervention or exposure factor sufficient
to produce a meaningful effect?
6.4. Was the amount of exposure and, if relevant, subject/patient compliance
measured?
6.5. Were co-interventions (e.g., ancillary treatments, other therapies) described?
6.6. Were extra or unplanned treatments described?
6.7. Was the information for 6.4, 6.5, and 6.6 assessed the same way for all groups?
6.8. In diagnostic study, were details of test administration and replication
sufficient?

7. Were outcomes clearly defined and the measurements valid and reliable?
7.1. Were primary and secondary endpoints described and relevant to the
question?
7.2. Were nutrition measures appropriate to question and outcomes of concern?
7.3. Was the period of follow-up long enough for important outcome(s) to occur?
7.4. Were the observations and measurements based on standard, valid, and
reliable data collection instruments/tests/procedures?
7.5. Was the measurement of effect at an appropriate level of precision?
7.6. Were other factors accounted for (measured) that could affect outcomes?
7.7. Were the measurements conducted consistently across groups?

6.2

N/A

6.3

N/A

6.4

N/A

6.5

Yes

6.6

N/A

6.7

Yes

6.8

N/A

Yes

7.1

Yes

7.2

Yes

7.3

N/A

7.4

Yes

7.5

Yes

7.6

Yes

7.7

Yes

Yes

8.1

Yes

8.2

Yes

8.3

Yes

8.4

N/A

8.5

Yes

8.6

No

8.7

N/A





8. Was the statistical analysis appropriate for the study design and type of outcome
indicators?
8.1. Were statistical analyses adequately described the results reported
appropriately?
8.2. Were correct statistical tests used and assumptions of test not violated?
8.3. Were statistics reported with levels of significance and/or confidence intervals?
8.4. Was intent to treat analysis of outcomes done (and as appropriate, was there
an analysis of outcomes for those maximally exposed or a dose-response
analysis)?
8.5. Were adequate adjustments made for effects of confounding factors that
might have affected the outcomes (e.g., multivariate analyses)?
8.6. Was clinical significance as well as statistical significance reported?
8.7. If negative findings, was a power calculation reported to address type 2 error?
9. Are conclusions supported by results with biases and limitations taken into
consideration?
9.1. Is there a discussion of findings?
9.2. Are biases and study limitations identified and discussed?
10. Is bias due to studys funding or sponsorship unlikely?
10.1. Were sources of funding and investigators affiliations described?
10.2. Was there no apparent conflict of interest?

Yes
Yes
9.2
Yes
10
Yes
10.1 No
10.2 Yes
9

9.1

MINUS/NEGATIVE (-)
If most (six or more) of the answers to the above validity questions are No, the report should be designated with a minus
(-) symbol on the Evidence Worksheet.
NEUTRAL ()

If the answers to validity criteria questions 2, 3, 6, and 7 do not indicate that the study is exceptionally strong, the report
should be designated with a neutral () symbol on the Evidence Worksheet.
PLUS/POSITIVE (+)
If most of the answers to the above validity questions are Yes (including criteria 2, 3, 6, 7 and at least one additional
Yes), the report should be designated with a plus symbol (+) on the Evidence Worksheet.

Academy(of(Nutrition(and(Dietetics(
Evidence(Analysis(Library(Worksheet(Template(and(
Quality(Criteria(Checklist:(Primary(Research(
Citation'

Manisha'Chanalia',M.D.,Abhimanyu'Garg,M.D.,'Dieter'Lutjhonatann,PH.D.,'Klaus'
von'BErgmann,M.D.,'Scott'M.Grundy,M.D.,Ph.d.,and'Linda'J.'Brinkley,'R.'D.'
(2015).'Beneficial'Effects'of'High'Dietary'Fiber'Intake'in'Patients'With'Type'2'
Diabetes'Mellitus.'(completed'by'Grace'Kim)'

Study'Design'

Randomized'Crossover'Study'

Class'

A'

Quality'Rating'

Research'Purpose'

Inclusion'Criteria'
Exclusion'Criteria'

'+'(Positive)'''

'U'(Negative)''

'!'(Neutral)'

To'determine'the'effects'on'glycemic'control'and'plasma'lipid'concentrations'of'
increasing'the'intake'of'dietary'fiber'in'patients'with'type'2'diabetes'exclusivley'
through'the'conusmption'of'foods'not'fortified'with'fiber'to'a'level'beyond'that'
recommended'by'the'ADA'
insidious'onset'of'Type'2'diabetes;'developed'in'most'of'the'patients'after'40'
years'of'age'
N/A'
Recruitment:''general'clinical'research'center'of'University'of'Texas'Southwestern'
Medical'Center;'protocal'approved'by'IRB,'each'patient'gave'written'informed'
consent'
Design:''3'patients'treated'with'diet,'other'10'patients'treated'w/'2.5'to'20'mg'of'
glyburide'daily'in'addition'to'diet;'6'received'highUfiber'and'other'7'received'ADA'

Description'of'
Study'Protocol'

diet'first;'median'interval'of'seven'days,'then'received'other'diet'
Blinding'used'(if'applicable):''N/A'
Intervention'(if'applicable):''HighUfiber'diet'containing'50g'total'fiber'(25g'soluble,'
25g'insoluble)'vs.ADA'diet'containing'24g'of'total'fiber'(8g'soluble,'16g'insoluble)'
Statistical'Analysis:''repeatedUmeasures'analysis'of'variance'to'compare'two'study'
periods/assess'effect'of'sequence'in'which'patients'received'highUfiber'and'ADA;'
Wilcoxon'signedUrank'test'to'compare'two'dietary'periods'for'skewed'data.'
Detailed'history,'physical'examination,'laboratory'tests'were'performed,'
hospitialized'for'evaluation,'interviewed,'blood'for'lipid'analyses'were'drawn,'and'
fecal'samples'were'collected,'urine'specimens'
Timing'of'Measurements:'baseUline,'last'week'of'each'dietary'period'(dietary'

Data'Collection'
Summary'

period'lasts'for'6'weeks)'
Dependent'Variables:''measures'(blood'for'lipid'analyses,'plasma'glucose,'
glycosylated'hemoglobin'levels,'insulin'level,'fecal'sterol'balance,'cholesterol'
absorption)'
Independent'Variables:''highUfiber'diet'(50'g'total'fiber:'25g'soluble,'25g'

insoluble)'
Control'Variables:'ADA'diet;'(24'g'of'total'fiber:'8g'soluble,'16g'insoluble)'
Initial:''13'(6'intervention,'7'control;'after'six'weeks,'switched)''(12'Males'''1'
Females)'
Attrition'(final'N):''13'
Age:''61'9'years'(45U70)'
Ethnicity:''9'nonUHispanic'whites/4'blacks'
Description'of'
Other'relevant'demographics:''3'patients'treated'with'diet'alone,'other'10'
Actual'Data'Sample'
treated'with'2.5'to'20'mg'of'glyburide'daily'in'addition'to'diet'and'dose'was'not'
changed'during'the'study'
Anthropometrics:''mean'body'weight:93.5'12.7'kg;'mean'body'mass'index:'32.3'
3.9''
Location:''Dallas,'USA'
Key'Findings:'Mean'and'daily'plasma'glucose'concentration,'plasma'insulin'
concentrations,'and'glycosylated'hemoglobin'values'were'lower'after'highUfiber'
diet'completion'
'
Summary'of'Results' Other'Findings:'fasting'plasma'total'cholesterol'concentration,'plasma'triglyceride'
concentration,'lower'plasma'VLDL'cholesterol'concentration,'fasting'plasma'LDL'
cholesterol'concentration,'and'gastrointestinal'absorption'of'cholesterol'were'
lower'after'highUfiber'diet'completion;'sequence'of'diets'had'no'effect'on'the'
results'
HighUfiber'diet'improved'glycemic'control,'lowered'glycosylated'hemoglobin'
values;'specifically,'increase'in'intake'of'total'dietary'fiber'which'consists'
Author'Conclusion'

predominantly'of'soluble'fiber,'significantly'improved'glycemic'control'and'
decreased'degree'of'hyperinsulinemia'in'patients'with'type'2'diabetes'
This%study%was%able%to%conclude%that%fiber%has%an%effect%on%glycemic%control%in%
patients%with%type%2%diabetes;%however,%there%was%also%glyburide,%an%oral%diabetes%

Reviewer'
Comments'

medicine%that%helps%control%blood%sugar%levels,%given%to%only%10%of%the%patients.%It%
would%have%been%better%to%treat%all%the%patients%with%glyburide%for%more%
consistency.%%
National'Institutes'of'Health'grants'M01URR00633'&'HLU29252;'research'grants:'

Funding'Source'

Bundesministerium'fur'Bildung,'Forschung,'Wissenschaft'und'Technologie'
(01EC9402)'and'Deutsche'Forschungsgemeinschaft'(BE'1673/1U1)'

'

Quality(Criteria(Checklist:(Primary(Research(
Symbols(Used(
+(
77(
!(

Explanation(
Positive((Indicates'that'the'report'has'clearly'addressed'issues'of'inclusion/exclusion,'
bias,'generalizability,'and'data'collection'and'analysis(
Negative((Indicates'that'these'issues'have'not'been'adequately'addressed.(
Neutral('indicates'that'the'report'is'neither'exceptionally'strong'nor'exceptionally'
week(
Select'a'rating'from'the''
dropUdown'menu'!'

Relevance(Questions(
1.! Would'implementing'the'studied'intervention'or'procedure'(if'found'successful)'result'
in'improved'outcomes'for'the'patients/clients/population'group?'(NA'for'some'Epi'
studies)'
2.! Did'the'authors'study'an'outcome'(dependent'variable)'or'topic'that'the'
patients/clients/population'group'would'care'about?'
3.! Is'the'focus'of'the'intervention'or'procedure'(independent'variable)'or'topic'of'study'a'
common'issue'of'concern'to'dietetics'practice?'
4.! Is'the'intervention'or'procedure'feasible?'(NA'for'some'epidemiological'studies)'

1'

Yes'

2'

Yes'

3'

Yes'

4'

Yes'

If(the(answers(to(all(of(the(above(relevance(questions(are(Yes,(the(report(is(eligible(for(designation(with(a(
plus((+)(on(the(Evidence(Quality(Worksheet,(depending(on(answers(to(the(following(validity(questions.'
Validity(Questions'
1.! Was(the(research(question(clearly(stated?(
1.1.! Was'the'specific'intervention(s)'or'procedure'(independent'variable(s))'
identified?'
1.2.! Was'the'outcome(s)'(dependent'variable(s))'clearly'indicated?'
1.3.! Were'the'target'population'and'setting'specified?'
2.! Was(the(selection(of(study(subjects/patients(free(from(bias?(
2.1.! Were'inclusion/exclusion'criteria'specified'(e.g.,'risk,'point'in'disease'
progression,'diagnostic'or'prognosis'criteria),'and'with'sufficient'detail'and'
without'omitting'criteria'critical'to'the'study?'
2.2.! Were'criteria'applied'equally'to'all'study'groups?'
2.3.! Were'health,'demographics,'and'other'characteristics'of'subjects'described?'
2.4.! Were'the'subjects/patients'a'representative'sample'of'the'relevant'
population?'
3.! Were(study(groups(comparable?(
3.1.! Was'the'method'of'assigning'subjects/patients'to'groups'described'and'
unbiased?'(Method'of'randomization'identified'if'RCT)'
3.2.! Were'distribution'of'disease'status,'prognostic'factors,'and'other'factors'(e.g.,'
demographics)'similar'across'study'groups'at'baseline?'
3.3.! Were'concurrent'controls'used?'(Concurrent'preferred'over'historical'
controls.)'
3.4.! If'cohort'study'or'crossUsectional'study,'were'groups'comparable'on'important'
confounding'factors'and/or'were'preexisting'differences'accounted'for'by'using'
appropriate'adjustments'in'statistical'analysis?'
3.5.! If'case'control'study,'were'potential'confounding'factors'comparable'for'cases'
and'controls?'(If'case'series'or'trial'with'subjects'serving'as'own'control,'this'
criterion'is'not'applicable.'Criterion'may'not'be'applicable'in'some'crossU
sectional'studies.)'
3.6.! If'diagnostic'test,'was'there'an'independent'blind'comparison'with'an'
appropriate'reference'standard'(e.g.,'gold'standard)?'

'

1.3'

Yes'
Yes'
Yes'
No'

2'

Unclear'

2.1'

Unclear'

2.2'

Unclear'

2.3'

Yes'

2.4'

No'

3'

Yes'

3.1'

No'

3.2'

Unclear'

3.3'

Yes'

3.4'

Yes'

3.5'

N/A'

3.6'

N/A'

1'
1.1'
1.2'

'
4.! Was(method(of(handling(withdrawals(described?(
4.1.! Were'follow'up'methods'described'and'the'same'for'all'groups?(
4.2.! Was'the'number,'characteristics'of'withdrawals'(i.e.,'dropouts,'lost'to'follow'
up,'attrition'rate)'and/or'response'rate'(crossUsectional'studies)'described'for'
each'group?'(Follow'up'goal'for'a'strong'study'is'80%.)'
4.3.! Were'all'enrolled'subjects/patients'(in'the'original'sample)'accounted'for?'''
4.4.! Were'reasons'for'withdrawals'similar'across'groups'
4.5.! If'diagnostic'test,'was'decision'to'perform'reference'test'not'dependent'on'
results'of'test'under'study?'
5.! Was(blinding(used(to(prevent(introduction(of(bias?(
5.1.! In'intervention'study,'were'subjects,'clinicians/practitioners,'and'investigators'
blinded'to'treatment'group,'as'appropriate?(
5.2.! Were'data'collectors'blinded'for'outcomes'assessment?'(If'outcome'is'
measured''using'an'objective'test,'such'as'a'lab'value,'this'criterion'is'assumed'
to'be'met.)'
5.3.! In'cohort'study'or'crossUsectional'study,'were'measurements'of'outcomes'and'
risk''factors'blinded?''
5.4.! In'case'control'study,'was'case'definition'explicit'and'case'ascertainment'not'
influenced'by'exposure'status?'
5.5.! In'diagnostic'study,'were'test'results'blinded'to'patient'history'and'other'test'
results?'
6.! Were(intervention/therapeutic(regimens/exposure(factor(or(procedure(and(any(
comparison(s)(described(in(detail?(Were(intervening(factors(described?(
6.1.! In'RCT'or'other'intervention'trial,'were'protocols'described'for'all'regimens'
studied?'
6.2.! In'observational'study,'were'interventions,'study'settings,'and'
clinicians/provider'''described?'
6.3.! Was'the'intensity'and'duration'of'the'intervention'or'exposure'factor'sufficient'
to'produce'a'meaningful'effect?'
6.4.! Was'the'amount'of'exposure'and,'if'relevant,'subject/patient'compliance'
measured?'
6.5.! Were'coUinterventions'(e.g.,'ancillary'treatments,'other'therapies)'described?'
6.6.! Were'extra'or'unplanned'treatments'described?'
6.7.! Was'the'information'for'6.4,'6.5,'and'6.6'assessed'the'same'way'for'all'groups?'
6.8.! In'diagnostic'study,'were'details'of'test'administration'and'replication'
sufficient?'

7.! Were(outcomes(clearly(defined(and(the(measurements(valid(and(reliable?(
7.1.! Were'primary'and'secondary'endpoints'described'and'relevant'to'the'
question?'''
7.2.! Were'nutrition'measures'appropriate'to'question'and'outcomes'of'concern?'
7.3.! Was'the'period'of'followUup'long'enough'for'important'outcome(s)'to'occur?'
7.4.! Were'the'observations'and'measurements'based'on'standard,'valid,'and'
reliable'data'collection'instruments/tests/procedures?'
7.5.! Was'the'measurement'of'effect'at'an'appropriate'level'of'precision?'
7.6.! Were'other'factors'accounted'for'(measured)'that'could'affect'outcomes?'
7.7.! Were'the'measurements'conducted'consistently'across'groups?'

'
'
'
'

4'

Yes'

4.1'

Yes'

4.2'

No'

4.3'

Yes'

4.4'

N/A'

4.5'

N/A'

5'

No'

5.1'

N/A'

5.2'

N/A'

5.3'

No'

5.4'

N/A'

5.5'

N/A'

6'

Yes'

6.1'

Yes'

6.2'

N/A'

6.3'

Yes'

6.4'

Yes'

6.5'

Yes'

6.6'

Unclear'

6.7'

Yes'

6.8'

N/A'

7'

Yes'

7.1'

Yes'

7.2'

Yes'

7.3'

Unclear'

7.4'

Yes'

7.5'

Unclear'

7.6'

Yes'

7.7'

Unclear'

8.! Was(the(statistical(analysis(appropriate(for(the(study(design(and(type(of(outcome(
indicators?((
8.1.! Were'statistical'analyses'adequately'described'the'results'reported'
appropriately?'
8.2.! Were'correct'statistical'tests'used'and'assumptions'of'test'not'violated?'
8.3.! Were'statistics'reported'with'levels'of'significance'and/or'confidence'intervals?'
8.4.! Was'intent'to'treat'analysis'of'outcomes'done'(and'as'appropriate,'was'there'
an'analysis'of'outcomes'for'those'maximally'exposed'or'a'doseUresponse'
analysis)?'
8.5.! Were'adequate'adjustments'made'for'effects'of'confounding'factors'that'
might'have'affected'the'outcomes'(e.g.,'multivariate'analyses)?'
8.6.! Was'clinical'significance'as'well'as'statistical'significance'reported?'
8.7.! If'negative'findings,'was'a'power'calculation'reported'to'address'type'2'error?'
9.! Are(conclusions(supported(by(results(with(biases(and(limitations(taken(into(
consideration?'
9.1.! Is'there'a'discussion'of'findings?'
9.2.! Are'biases'and'study'limitations'identified'and'discussed?'
10.! Is(bias(due(to(studys(funding(or(sponsorship(unlikely?(
10.1.!Were'sources'of'funding'and'investigators'affiliations'described?'
10.2.!Was'there'no'apparent'conflict'of'interest?'

8'

Yes'

8.1'

Yes'

8.2'

Yes'

8.3'

Yes'

8.4'

N/A'

8.5'

Yes'

8.6'

Yes'

8.7'

N/A'

N/A'
9.1'
No'
9.2'
Unclear'
10'
N/A'
10.1' Yes'
10.2' Yes'
9'

MINUS/NEGATIVE((7)(
If%most%(six%or%more)%of%the%answers%to%the%above%validity%questions%are%No,%the%report%should%be%designated%with%a%minus%%
(F)%symbol%on%the%Evidence%Worksheet.'
NEUTRAL((!)%
If%the%answers%to%validity%criteria%questions%2,%3,%6,%and%7%do%not%indicate%that%the%study%is%exceptionally%strong,%the%report%
should%be%designated%with%a%neutral%(!)'symbol%on%the%Evidence%Worksheet.'
PLUS/POSITIVE((+)%
If%most%of%the%answers%to%the%above%validity%questions%are%Yes%(including%criteria%2,%3,%6,%7%and%at%least%one%additional%
Yes),%the%report%should%be%designated%with%a%plus%symbol%(+)%on%the%Evidence%Worksheet.'

'

Academy(of(Nutrition(and(Dietetics(
Evidence(Analysis(Library(Worksheet(Template(and(
Quality(Criteria(Checklist:(Primary(Research(

Citation'

Reviewer:'Ria'Thakur'
'
Lubia'Velzquez9Lpez,'Abril'Violeta'Muoz9Torres,'Carmen'Garca9Pea,'Mardia'
Lpez9Alarcn,'Sergio'Islas9Andrade,'and'Jorge'Escobedo9de'la'Pea,'Fiber'in'Diet'
Is'Associated'with'Improvement'of'Glycated'Hemoglobin'and'Lipid'Profile'in'
Mexican'Patients'with'Type'2'Diabetes,'Journal'of'Diabetes'Research,'vol.'2016,'
Article'ID'2980406,'9'pages,'2016.'doi:10.1155/2016/2980406'

Study'Design'

Cross'Sectional'Study'

Class'

D'

Quality'Rating'
Research'Purpose'
Inclusion'Criteria'
Exclusion'Criteria'

'+'(Positive)'''

'9'(Negative)''

'!'(Neutral)'

Assess'the'association'of'dietary'fiber'on'current'everyday'diet'and'other'dietary'
components'in'patients'with'Type'2'Diabetes.'
Patients'with'Type'2'Diabetes,'patients'from'4'different'primary'care'clinics'in'
Mexico'City'with'a'previous'diagnosis'of'diabetes,'<70'yrs'old,'no'advanced'
microvascular'complication.'
Patients'who'didnt'have'diabetes,'who'werent'a'part'of'the'clinical'trial,'>70'yrs'
old'
Recruitment:'''''''''''''Participants'from'the'randomized'clinical'trial'called'Efficacy'
of'Nutritional'Therapy'and'Education'through'a'Multimedia'System'for'the'
Metabolic'Control'of'Type'2'Diabetes'Patients'were'invited'to'participate'at'theur'
local'clinic'and'incorporated'into'the'study'once'they'had'signed'the'letter'of'
informed'consent.'

Description'of'
Study'Protocol'

Design:''dPatients'in'the'study'went'through'intensive'medical'history'
questionnaire'as'well'as'physical'examination.'
Blinding'used'(if'applicable):''None'
Intervention'(if'applicable):''Twelve9hour9fasting'blood'plasma,'glucose'
concentration,'creatinine,'triglycerides,'total'cholesterol,'and'fractions'HDL9c'
values'were'measured'
Statistical'Analysis:''Friedewald'equation,'
high9resolution'liquid'chromatography'method,'photometry/nephelometry,'
Habitch'method,'TANITA'body'composition'analyzer,'food'frequency'
questionnaire,'System'to'calculate'nutritional'vectors,'Kruskal9Wallis'test,'chi9

Data'Collection'
Summary'

square'test,'logistic'regression'multivariate'analysis' ' ' ' ' '


Timing'of'Measurements:'Hypertension'was'diagnosed'at'the'time'of'joining'the'
study,'blood'pressure'was'taken'twice'at'an'interval'of'4'minutes'between'
measurement'and'after'the'patient'had'been'seated'for'more'than'5'

minutes.Physical'activity'was'considered'when'the'patient'had'at'least'
150min/week'of'moderate9intensity'aerobic'physical'activity,'for'at'least'3'
days/week'with'no'more'than'2'consecutive'days'without'exercise''
Dependent'Variables:''change'in'hbA1c,'triglyceride'levels,'HDL9c'levels,',''
Independent'Variables:''Diabetes'education,'appropriate'meal'plan'and'physical'
activity,'anthropometric'measures,''
Control'Variables:'Specific'nutrient'intake'
Initial:''395''(not'specifiec'Males'''not'specified'Females)'
Attrition'(final'N):''395'
Age:''<70years'old''
Ethnicity:''Mexicans'
Description'of'
Other'relevant'demographics:''Part'of'a'multicenter,'randomized'clinical'trial'
Actual'Data'Sample'
called'Efficacy'of'Nutritional'Therapy'and'Education'through'a'Multimedia'System'
for'the'Metabolic'Control'of'Type'2'Diabetes'Patients''
Anthropometrics:''88%'of'participants'had'BMI'>'normal.'
Location:''Mexico'City'
Key'Findings:'A'higher'content'of''fiber'in'the'diet'had'an'impact'on'reducing'
HbA1c'and'triglyceride'levels,'while'improving'HDL9c'levels.''
'
Other'Findings:''55%had'hypertension,'26%'had'diabetic'neuropathy,'12%'had'
Summary'of'Results' microalbuminuria,'and'5%'had'macroalbuminuria,'only'12%'had'BMI'in'a'normal'
range,''Only'34%'had'a'desirable'HbA1c;'total'cholesterol'was'within'control'
range'for'over'50%'of'the'population,'whereas'triglycerides,'LDL9c,'and'HDL9c'
were'found'to'be'within'normal'range'in'only'third'of'the'subjects.'
'
There'is'statistical'significance'that'shows'that'a'high'fiber'diet'lowers'HbA1c'and'
Author'Conclusion'
Reviewer'
Comments'

triglyceride'levels'while'improving'HDL9c'levels.''
I"wish"there"was"a"specific"diet"intervention"performed"in"this"study."Also,"I"wish"
the"kind"of"fiber"was"specified"if"it"was"soluble"or"insoluble.""
Mexico'National'Science'and'Technology'Council'(Consejo'Nacional'de'Ciencia'y'

Funding'Source'

Tecnologa,'CONACYT)'no.'SALUD920129019181015'

'

Quality(Criteria(Checklist:(Primary(Research(
Symbols(Used(
+(

Explanation(
Positive((Indicates'that'the'report'has'clearly'addressed'issues'of'inclusion/exclusion,'

77(
!(

bias,'generalizability,'and'data'collection'and'analysis(
Negative((Indicates'that'these'issues'have'not'been'adequately'addressed.(
Neutral('indicates'that'the'report'is'neither'exceptionally'strong'nor'exceptionally'
week(
Select'a'rating'from'the''
drop9down'menu'!'

Relevance(Questions(
1.! Would'implementing'the'studied'intervention'or'procedure'(if'found'successful)'result'
in'improved'outcomes'for'the'patients/clients/population'group?'(NA'for'some'Epi'
studies)'
2.! Did'the'authors'study'an'outcome'(dependent'variable)'or'topic'that'the'
patients/clients/population'group'would'care'about?'
3.! Is'the'focus'of'the'intervention'or'procedure'(independent'variable)'or'topic'of'study'a'
common'issue'of'concern'to'dietetics'practice?'
4.! Is'the'intervention'or'procedure'feasible?'(NA'for'some'epidemiological'studies)'

1'

Yes'

2'

Yes'

3'

Yes'

4'

Yes'

If(the(answers(to(all(of(the(above(relevance(questions(are(Yes,(the(report(is(eligible(for(designation(with(a(
plus((+)(on(the(Evidence(Quality(Worksheet,(depending(on(answers(to(the(following(validity(questions.'
Validity(Questions'
1.! Was(the(research(question(clearly(stated?(
1.1.! Was'the'specific'intervention(s)'or'procedure'(independent'variable(s))'
identified?'
1.2.! Was'the'outcome(s)'(dependent'variable(s))'clearly'indicated?'
1.3.! Were'the'target'population'and'setting'specified?'
2.! Was(the(selection(of(study(subjects/patients(free(from(bias?(
2.1.! Were'inclusion/exclusion'criteria'specified'(e.g.,'risk,'point'in'disease'
progression,'diagnostic'or'prognosis'criteria),'and'with'sufficient'detail'and'
without'omitting'criteria'critical'to'the'study?'
2.2.! Were'criteria'applied'equally'to'all'study'groups?'
2.3.! Were'health,'demographics,'and'other'characteristics'of'subjects'described?'
2.4.! Were'the'subjects/patients'a'representative'sample'of'the'relevant'
population?'
3.! Were(study(groups(comparable?(
3.1.! Was'the'method'of'assigning'subjects/patients'to'groups'described'and'
unbiased?'(Method'of'randomization'identified'if'RCT)'
3.2.! Were'distribution'of'disease'status,'prognostic'factors,'and'other'factors'(e.g.,'
demographics)'similar'across'study'groups'at'baseline?'
3.3.! Were'concurrent'controls'used?'(Concurrent'preferred'over'historical'
controls.)'
3.4.! If'cohort'study'or'cross9sectional'study,'were'groups'comparable'on'important'
confounding'factors'and/or'were'preexisting'differences'accounted'for'by'using'
appropriate'adjustments'in'statistical'analysis?'
3.5.! If'case'control'study,'were'potential'confounding'factors'comparable'for'cases'
and'controls?'(If'case'series'or'trial'with'subjects'serving'as'own'control,'this'
criterion'is'not'applicable.'Criterion'may'not'be'applicable'in'some'cross9
sectional'studies.)'
3.6.! If'diagnostic'test,'was'there'an'independent'blind'comparison'with'an'
appropriate'reference'standard'(e.g.,'gold'standard)?'

1.3'

Yes'
Yes'
Yes'
Yes'

2'

Unclear'

2.1'

No'

2.2'

N/A'

2.3'

Yes'

2.4'

No'

3'

No'

3.1'

Unclear'

3.2'

Yes'

3.3'

Unclear'

3.4'

Yes'

3.5'

N/A'

3.6'

N/A'

4'

No'

1'
1.1'
1.2'

'
'
4.! Was(method(of(handling(withdrawals(described?(

4.1.! Were'follow'up'methods'described'and'the'same'for'all'groups?(
4.2.! Was'the'number,'characteristics'of'withdrawals'(i.e.,'dropouts,'lost'to'follow'
up,'attrition'rate)'and/or'response'rate'(cross9sectional'studies)'described'for'
each'group?'(Follow'up'goal'for'a'strong'study'is'80%.)'
4.3.! Were'all'enrolled'subjects/patients'(in'the'original'sample)'accounted'for?'''
4.4.! Were'reasons'for'withdrawals'similar'across'groups'
4.5.! If'diagnostic'test,'was'decision'to'perform'reference'test'not'dependent'on'
results'of'test'under'study?'
5.! Was(blinding(used(to(prevent(introduction(of(bias?(
5.1.! In'intervention'study,'were'subjects,'clinicians/practitioners,'and'investigators'
blinded'to'treatment'group,'as'appropriate?(
5.2.! Were'data'collectors'blinded'for'outcomes'assessment?'(If'outcome'is'
measured''using'an'objective'test,'such'as'a'lab'value,'this'criterion'is'assumed'
to'be'met.)'
5.3.! In'cohort'study'or'cross9sectional'study,'were'measurements'of'outcomes'and'
risk''factors'blinded?''
5.4.! In'case'control'study,'was'case'definition'explicit'and'case'ascertainment'not'
influenced'by'exposure'status?'
5.5.! In'diagnostic'study,'were'test'results'blinded'to'patient'history'and'other'test'
results?'
6.! Were(intervention/therapeutic(regimens/exposure(factor(or(procedure(and(any(
comparison(s)(described(in(detail?(Were(intervening(factors(described?(
6.1.! In'RCT'or'other'intervention'trial,'were'protocols'described'for'all'regimens'
studied?'
6.2.! In'observational'study,'were'interventions,'study'settings,'and'
clinicians/provider'''described?'
6.3.! Was'the'intensity'and'duration'of'the'intervention'or'exposure'factor'sufficient'
to'produce'a'meaningful'effect?'
6.4.! Was'the'amount'of'exposure'and,'if'relevant,'subject/patient'compliance'
measured?'
6.5.! Were'co9interventions'(e.g.,'ancillary'treatments,'other'therapies)'described?'
6.6.! Were'extra'or'unplanned'treatments'described?'
6.7.! Was'the'information'for'6.4,'6.5,'and'6.6'assessed'the'same'way'for'all'groups?'
6.8.! In'diagnostic'study,'were'details'of'test'administration'and'replication'
sufficient?'

7.! Were(outcomes(clearly(defined(and(the(measurements(valid(and(reliable?(
7.1.! Were'primary'and'secondary'endpoints'described'and'relevant'to'the'
question?'''
7.2.! Were'nutrition'measures'appropriate'to'question'and'outcomes'of'concern?'
7.3.! Was'the'period'of'follow9up'long'enough'for'important'outcome(s)'to'occur?'
7.4.! Were'the'observations'and'measurements'based'on'standard,'valid,'and'
reliable'data'collection'instruments/tests/procedures?'
7.5.! Was'the'measurement'of'effect'at'an'appropriate'level'of'precision?'
7.6.! Were'other'factors'accounted'for'(measured)'that'could'affect'outcomes?'
7.7.! Were'the'measurements'conducted'consistently'across'groups?'

4.1'

N/A'

4.2'

No'

4.3'

Unclear'

4.4'

N/A'

4.5'

N/A'

5'

Unclear'

5.1'

N/A'

5.2'

No'

5.3'

No'

5.4'

N/A'

5.5'

N/A'

6'

Yes'

6.1'

Yes'

6.2'

N/A'

6.3'

N/A'

6.4'

Unclear'

6.5'

N/A'

6.6'

Unclear'

6.7'

Unclear'

6.8'

N/A'

7'

Yes'

7.1'

Yes'

7.2'

Yes'

7.3'

Unclear'

7.4'

Yes'

7.5'

Yes'

7.6'

Yes'

7.7'

Yes'

8'

Yes'

8.1'

Yes'

'
'
'
'
8.! Was(the(statistical(analysis(appropriate(for(the(study(design(and(type(of(outcome(
indicators?((
8.1.! Were'statistical'analyses'adequately'described'the'results'reported'

appropriately?'
8.2.! Were'correct'statistical'tests'used'and'assumptions'of'test'not'violated?'
8.3.! Were'statistics'reported'with'levels'of'significance'and/or'confidence'intervals?'
8.4.! Was'intent'to'treat'analysis'of'outcomes'done'(and'as'appropriate,'was'there'
an'analysis'of'outcomes'for'those'maximally'exposed'or'a'dose9response'
analysis)?'
8.5.! Were'adequate'adjustments'made'for'effects'of'confounding'factors'that'
might'have'affected'the'outcomes'(e.g.,'multivariate'analyses)?'
8.6.! Was'clinical'significance'as'well'as'statistical'significance'reported?'
8.7.! If'negative'findings,'was'a'power'calculation'reported'to'address'type'2'error?'
9.! Are(conclusions(supported(by(results(with(biases(and(limitations(taken(into(
consideration?'
9.1.! Is'there'a'discussion'of'findings?'
9.2.! Are'biases'and'study'limitations'identified'and'discussed?'
10.! Is(bias(due(to(studys(funding(or(sponsorship(unlikely?(
10.1.!Were'sources'of'funding'and'investigators'affiliations'described?'
10.2.!Was'there'no'apparent'conflict'of'interest?'

8.2'

Yes'

8.3'

Yes'

8.4'

No'

8.5'

Yes'

8.6'

Yes'

8.7'

Yes'

Yes'
Yes'
9.2'
Yes'
10'
Yes'
10.1' Yes'
10.2' Yes'
9'

9.1'

MINUS/NEGATIVE((7)(
If"most"(six"or"more)"of"the"answers"to"the"above"validity"questions"are"No,"the"report"should"be"designated"with"a"minus""
(C)"symbol"on"the"Evidence"Worksheet.'
NEUTRAL((!)"
If"the"answers"to"validity"criteria"questions"2,"3,"6,"and"7"do"not"indicate"that"the"study"is"exceptionally"strong,"the"report"
should"be"designated"with"a"neutral"(!)'symbol"on"the"Evidence"Worksheet.'
PLUS/POSITIVE((+)"
If"most"of"the"answers"to"the"above"validity"questions"are"Yes"(including"criteria"2,"3,"6,"7"and"at"least"one"additional"
Yes),"the"report"should"be"designated"with"a"plus"symbol"(+)"on"the"Evidence"Worksheet.'

'

Academy(of(Nutrition(and(Dietetics(
Evidence(Analysis(Library(Worksheet(Template(and(
Quality(Criteria(Checklist:(Primary(Research(

Citation'

Reviewed'by:'Jessica'Park'
Chen,'C.,'Zeng,'Y.,'Xu,'J.,'Zheng,'H.,'Liu,'J.,'Fan,'R.,''Wang,'J.'(2016).'Therapeutic'
effects'of'soluble'dietary'fiber'consumption'on'type'2'diabetes'mellitus.'
Experimental'and'Therapeutic'Medicine,'12(2),'12321242.'
http://doi.org/10.3892/etm.2016.3377'

Study'Design'

Randomized'controlled'experiment'

Class'

A'

Quality'Rating'
Research'Purpose'
Inclusion'Criteria'
Exclusion'Criteria'

'+'(Positive)'''

'^'(Negative)''

'!'(Neutral)'

To'investigate'the'effects'of'fiber'on'glycemic'control'and'plasma'lipid'
concentrations'in'patients'with'type'2'diabetes'
diagnosed'with'type'2'diabetes'for'6'months'or'more,'patient'at'Xinqiao'Hospital'
of'the'Third'Military'Medical'University,'no'tumors,'no'myocardial'infarction,'no'
unstable'angina'pectoris'and'congestive'heart'failure'
tumors,'myocardial'infarction,'unstable'angina'pectoris,'congestive'heart'failure,'
thyroid'or'hepatic'disease,'lipid^lowering'treatments,'not'diagnosed'with'DM2'
Recruitment:''Subjects'that'met'criteria'were'randomly'selected'from'the'
Xinquiao'Hospital'of'Third'Military'Medical'University'and'divided'into'3'groups'
(control,'low^dose'(10g),'and'high^dose'(20g)'
Design:''Randomized'controlled'experiment.'40'patients'treated'with'ADA'diet'

Description'of'
Study'Protocol'

alone,'remaining'80'patients'treated'with'10'or'20'mg'soluble'fiber'daily'in'
addition'to'the'ADA'diet'for'one'month.'All'patients'received'MNT'
Blinding'used'(if'applicable):''double^blind'
Intervention'(if'applicable):''soluble'fiber'(10g'or'20g)'
Statistical'Analysis:'''Data'analyzed'using'SPSS'software'version'19.0,'95%'CIs,'
Shapiro^Wilk'test'for'normal'distribution,'t^test'
Patients'were'required'to'recount'the'remaining'soluble'fiber'during'phone'
consultation'every'week'
Timing'of'Measurements:'all'measurements'taken'prior'to'and'following'
treatment'by'clinical'lab'techs'who'were'blinded'to'content'and'purpose'of'the'

Data'Collection'
Summary'

study'
Dependent'Variables:''results'of'blood'marker'analysis,'anthropometric'measures,'
lipid'profile,'and'assessment'of'physical'characteristics'pre^'and'post^treatment'
Independent'Variables:''amount'of'soluble'fiber'given'(g)'
Control'Variables:'no'soluble'fiber'given'

Description'of'
Initial:''120''(46'Males'''71'Females)'
Actual'Data'Sample'

Attrition'(final'N):''3'left'for'personal'reasons'from'control'group.'Final'N:'117'
Age:''45^70'
Ethnicity:''Chinese'
Other'relevant'demographics:''' ' ' ' ' '
Anthropometrics:''mean'body'weight:'68.113.0'kg'and'mean'BMI:'25.33.9'
kg/m2'
Location:''Chongquing,'China'
Key'Findings:'At'the'end'of'treatment,'systolic'pressure'and'levels'of'HDL,'LDL,'
and'apoB'were'significantly'improved'in'the'20mg'group'compared'with'data'
prior'to'treatment'(P<0.05).'Fasting'insulin,'2^h'blood'glucose'and'Lpa'levels,'and'
the'insulin'resistance'index'were'significantly'improved'in'all'3'groups'(P<0.05).'
Summary'of'Results' '
Other'Findings:'2^h'blood'glucose,'fasting'insulin,'and'insulin'resistance'index'
were'significantly'improved'from'baseline'in'all'three'groups,'suggesting'MNT'
treatment'had'significant'impact,'increased'fiber'intake'was'shown'to'improve'
insulin'sensitivity'and'reduce'systemic'inflammation'
MNT'was'able'to'improve'2^h'blood'glucose'and'fasting'insulin'levels,'and'the'
Author'Conclusion'
Reviewer'
Comments'

insulin'resistance'index,'and'was'effective'in'maintaining'glycemic'control'
!!!!!!
National'Science'and'Technology'Support'Program,'Chongqing'Science'and'
Technology'Commission,''the'11th'Five^year'Plan''for'the'National'Key'Technology'

Funding'Source'

Research'and'Development'Program,'and'the'Innovation'Project'of'Chongqing'
Key'Laboratory'of'Nutrition'and'Food'Safety'

'

Quality(Criteria(Checklist:(Primary(Research(
Symbols(Used(
+(
77(
!(

Explanation(
Positive((Indicates'that'the'report'has'clearly'addressed'issues'of'inclusion/exclusion,'
bias,'generalizability,'and'data'collection'and'analysis(
Negative((Indicates'that'these'issues'have'not'been'adequately'addressed.(
Neutral('indicates'that'the'report'is'neither'exceptionally'strong'nor'exceptionally'
week(
Select'a'rating'from'the''
drop^down'menu'!'

Relevance(Questions(
1.! Would'implementing'the'studied'intervention'or'procedure'(if'found'successful)'result'
in'improved'outcomes'for'the'patients/clients/population'group?'(NA'for'some'Epi'
studies)'
2.! Did'the'authors'study'an'outcome'(dependent'variable)'or'topic'that'the'

1'

Yes'

2'

Yes'

patients/clients/population'group'would'care'about?'
3.! Is'the'focus'of'the'intervention'or'procedure'(independent'variable)'or'topic'of'study'a'
common'issue'of'concern'to'dietetics'practice?'
4.! Is'the'intervention'or'procedure'feasible?'(NA'for'some'epidemiological'studies)'

3'

Yes'

4'

Yes'

If(the(answers(to(all(of(the(above(relevance(questions(are(Yes,(the(report(is(eligible(for(designation(with(a(
plus((+)(on(the(Evidence(Quality(Worksheet,(depending(on(answers(to(the(following(validity(questions.'
Validity(Questions'
1.! Was(the(research(question(clearly(stated?(
1.1.! Was'the'specific'intervention(s)'or'procedure'(independent'variable(s))'
identified?'
1.2.! Was'the'outcome(s)'(dependent'variable(s))'clearly'indicated?'
1.3.! Were'the'target'population'and'setting'specified?'
2.! Was(the(selection(of(study(subjects/patients(free(from(bias?(
2.1.! Were'inclusion/exclusion'criteria'specified'(e.g.,'risk,'point'in'disease'
progression,'diagnostic'or'prognosis'criteria),'and'with'sufficient'detail'and'
without'omitting'criteria'critical'to'the'study?'
2.2.! Were'criteria'applied'equally'to'all'study'groups?'
2.3.! Were'health,'demographics,'and'other'characteristics'of'subjects'described?'
2.4.! Were'the'subjects/patients'a'representative'sample'of'the'relevant'
population?'
3.! Were(study(groups(comparable?(
3.1.! Was'the'method'of'assigning'subjects/patients'to'groups'described'and'
unbiased?'(Method'of'randomization'identified'if'RCT)'
3.2.! Were'distribution'of'disease'status,'prognostic'factors,'and'other'factors'(e.g.,'
demographics)'similar'across'study'groups'at'baseline?'
3.3.! Were'concurrent'controls'used?'(Concurrent'preferred'over'historical'
controls.)'
3.4.! If'cohort'study'or'cross^sectional'study,'were'groups'comparable'on'important'
confounding'factors'and/or'were'preexisting'differences'accounted'for'by'using'
appropriate'adjustments'in'statistical'analysis?'
3.5.! If'case'control'study,'were'potential'confounding'factors'comparable'for'cases'
and'controls?'(If'case'series'or'trial'with'subjects'serving'as'own'control,'this'
criterion'is'not'applicable.'Criterion'may'not'be'applicable'in'some'cross^
sectional'studies.)'
3.6.! If'diagnostic'test,'was'there'an'independent'blind'comparison'with'an'
appropriate'reference'standard'(e.g.,'gold'standard)?'

1.3'

Yes'
Yes'
Yes'
Yes'

2'

Yes'

2.1'

Yes'

2.2'

Yes'

2.3'

Yes'

2.4'

Yes'

3'

Yes'

3.1'

Yes'

3.2'

Yes'

3.3'

Yes'

3.4'

N/A'

3.5'

Yes'

3.6'

N/A'

4'

Yes'

4.1'

Unclear'

4.2'

Yes'

4.3'

Yes'

4.4'

Yes'

4.5'

N/A'

5'

Yes'

5.1'

Yes'

5.2'

Yes'

1'
1.1'
1.2'

'
'
4.! Was(method(of(handling(withdrawals(described?(
4.1.! Were'follow'up'methods'described'and'the'same'for'all'groups?(
4.2.! Was'the'number,'characteristics'of'withdrawals'(i.e.,'dropouts,'lost'to'follow'
up,'attrition'rate)'and/or'response'rate'(cross^sectional'studies)'described'for'
each'group?'(Follow'up'goal'for'a'strong'study'is'80%.)'
4.3.! Were'all'enrolled'subjects/patients'(in'the'original'sample)'accounted'for?'''
4.4.! Were'reasons'for'withdrawals'similar'across'groups'
4.5.! If'diagnostic'test,'was'decision'to'perform'reference'test'not'dependent'on'
results'of'test'under'study?'
5.! Was(blinding(used(to(prevent(introduction(of(bias?(
5.1.! In'intervention'study,'were'subjects,'clinicians/practitioners,'and'investigators'
blinded'to'treatment'group,'as'appropriate?(
5.2.! Were'data'collectors'blinded'for'outcomes'assessment?'(If'outcome'is'
measured''using'an'objective'test,'such'as'a'lab'value,'this'criterion'is'assumed'
to'be'met.)'

5.3.! In'cohort'study'or'cross^sectional'study,'were'measurements'of'outcomes'and'
risk''factors'blinded?''
5.4.! In'case'control'study,'was'case'definition'explicit'and'case'ascertainment'not'
influenced'by'exposure'status?'
5.5.! In'diagnostic'study,'were'test'results'blinded'to'patient'history'and'other'test'
results?'
6.! Were(intervention/therapeutic(regimens/exposure(factor(or(procedure(and(any(
comparison(s)(described(in(detail?(Were(intervening(factors(described?(
6.1.! In'RCT'or'other'intervention'trial,'were'protocols'described'for'all'regimens'
studied?'
6.2.! In'observational'study,'were'interventions,'study'settings,'and'
clinicians/provider'''described?'
6.3.! Was'the'intensity'and'duration'of'the'intervention'or'exposure'factor'sufficient'
to'produce'a'meaningful'effect?'
6.4.! Was'the'amount'of'exposure'and,'if'relevant,'subject/patient'compliance'
measured?'
6.5.! Were'co^interventions'(e.g.,'ancillary'treatments,'other'therapies)'described?'
6.6.! Were'extra'or'unplanned'treatments'described?'
6.7.! Was'the'information'for'6.4,'6.5,'and'6.6'assessed'the'same'way'for'all'groups?'
6.8.! In'diagnostic'study,'were'details'of'test'administration'and'replication'
sufficient?'

7.! Were(outcomes(clearly(defined(and(the(measurements(valid(and(reliable?(
7.1.! Were'primary'and'secondary'endpoints'described'and'relevant'to'the'
question?'''
7.2.! Were'nutrition'measures'appropriate'to'question'and'outcomes'of'concern?'
7.3.! Was'the'period'of'follow^up'long'enough'for'important'outcome(s)'to'occur?'
7.4.! Were'the'observations'and'measurements'based'on'standard,'valid,'and'
reliable'data'collection'instruments/tests/procedures?'
7.5.! Was'the'measurement'of'effect'at'an'appropriate'level'of'precision?'
7.6.! Were'other'factors'accounted'for'(measured)'that'could'affect'outcomes?'
7.7.! Were'the'measurements'conducted'consistently'across'groups?'

5.3'

N/A'

5.4'

Yes'

5.5'

N/A'

6'

Yes'

6.1'

Yes'

6.2'

N/A'

6.3'

Yes'

6.4'

Yes'

6.5'

Yes'

6.6'

Unclear'

6.7'

Yes'

6.8'

N/A'

7'

Yes'

7.1'

Unclear'

7.2'

Yes'

7.3'

Yes'

7.4'

Yes'

7.5'

Yes'

7.6'

Unclear'

7.7'

Yes'

8'

Yes'

8.1'

Yes'

8.2'

Yes'

8.3'

Yes'

8.4'

Yes'

8.5'

Unclear'

8.6'

Yes'

8.7'

N/A'

9'

Yes'
Yes'
No'

'
'
'
'
8.! Was(the(statistical(analysis(appropriate(for(the(study(design(and(type(of(outcome(
indicators?((
8.1.! Were'statistical'analyses'adequately'described'the'results'reported'
appropriately?'
8.2.! Were'correct'statistical'tests'used'and'assumptions'of'test'not'violated?'
8.3.! Were'statistics'reported'with'levels'of'significance'and/or'confidence'intervals?'
8.4.! Was'intent'to'treat'analysis'of'outcomes'done'(and'as'appropriate,'was'there'
an'analysis'of'outcomes'for'those'maximally'exposed'or'a'dose^response'
analysis)?'
8.5.! Were'adequate'adjustments'made'for'effects'of'confounding'factors'that'
might'have'affected'the'outcomes'(e.g.,'multivariate'analyses)?'
8.6.! Was'clinical'significance'as'well'as'statistical'significance'reported?'
8.7.! If'negative'findings,'was'a'power'calculation'reported'to'address'type'2'error?'
9.! Are(conclusions(supported(by(results(with(biases(and(limitations(taken(into(
consideration?'
9.1.! Is'there'a'discussion'of'findings?'
9.2.! Are'biases'and'study'limitations'identified'and'discussed?'

9.1'
9.2'

10.! Is(bias(due(to(studys(funding(or(sponsorship(unlikely?(
10.1.!Were'sources'of'funding'and'investigators'affiliations'described?'
10.2.!Was'there'no'apparent'conflict'of'interest?'

Yes'
10.1' Yes'
10.2' Yes'
10'

MINUS/NEGATIVE((7)(
If!most!(six!or!more)!of!the!answers!to!the!above!validity!questions!are!No,!the!report!should!be!designated!with!a!minus!!
(?)!symbol!on!the!Evidence!Worksheet.'
NEUTRAL((!)!
If!the!answers!to!validity!criteria!questions!2,!3,!6,!and!7!do!not!indicate!that!the!study!is!exceptionally!strong,!the!report!
should!be!designated!with!a!neutral!(!)'symbol!on!the!Evidence!Worksheet.'
PLUS/POSITIVE((+)!
If!most!of!the!answers!to!the!above!validity!questions!are!Yes!(including!criteria!2,!3,!6,!7!and!at!least!one!additional!
Yes),!the!report!should!be!designated!with!a!plus!symbol!(+)!on!the!Evidence!Worksheet.'

'

Academy(of(Nutrition(and(Dietetics(
Evidence(Analysis(Library(Worksheet(Template(and(
Quality(Criteria(Checklist:(Primary(Research(

Citation'

Reviewed'by:'Kimber'Schrowang'
Jiang,'J.,'Qiu,'H.,'Zhao,'G.,'Zhou,'Y.,'Zhang,'Z.,'Zhang,'H.,''Xu,'W.CH.'(2012).'
Dietary'Fiber'Intake'Is'Associated'with'HbA1c'Level'among'Prevalent'Patients'with'
Type'2'Diabetes'in'Pudong'New'Area'of'Shanghai,'China.'PLoS'ONE,'7(10),'
e46552.'http://doi.org/10.1371/journal.pone.0046552'
'

Study'Design'

crossCsectionaly'study'

Class'

D'

Quality'Rating'
Research'Purpose'
Inclusion'Criteria'

Exclusion'Criteria'

'+'(Positive)'''

'C'(Negative)''

'!'(Neutral)'

observe'the'effects'of'DF'intake'on'HbA1c'levels'with'Type'2'Diabetes'patients''
Adult'with'DM2,'Pudong'Area,'consume'lower'levels'of'energy'and'macro,'FPG'>='
7'mmol/L'or'2'hr'plasma'glucose'>='11.1'mmol/L'or'rnadom'plasma'glucose'
concentration'>=11.1'mmol/L'in'persons'with'symptoms'of'hyperglycemia'or'
hyperglycemic'crisis'
not'diagnosed'with'DM2,'living'out'of'the'Pudong'Area,'not'meeting'the'glucose'
levels,'CV'even'withi'past'6'months,'advanced'CHF,'unstable'angina,'major'
depression'and'dementia'
Recruitment:''934'patients'randomly'selected'from'Diabetes'Administration'
Rosters'in'specified'communities'and'compared'to'918'adult'volunteers'without'
Type'2'Diabetes'from'the'spouses'and'neighbors'of'the'patients'in'the'same'area''
Design:''crossCsectional'study'

Description'of'
Study'Protocol'

Blinding'used'(if'applicable):''N/A'
Intervention'(if'applicable):''N/A'
Statistical'Analysis:''SAS'version'9.2,'natural'log'transformation'applied'to'
normalize'distribution'of'biochemical'measurements,'all'statistical'tests'based'on'
twoCsided'probability'
''''''
Timing'of'Measurements:'collected'at'interview,'blood'collected'after'10'hours'of'

Data'Collection'
Summary'

overnight'fasting'
Dependent'Variables:''HbA1c'levels'
Independent'Variables:''patients'with'DM2'
Control'Variables:'healthy'volunteers''
Initial:''1852''(41.7%'DM2,'31.7%'C'Males'''58.3%'DM2,'68.3%'C'Females)'

Attrition'(final'N):''926/918'
Description'of'
Actual'Data'Sample' Age:''64.5'+/C10.1'
Ethnicity:''Chinese'

Other'relevant'demographics:''' ' ' ' ' '


Anthropometrics:''See'Table'1'of'study'
Location:''Pudong'Area'of'Shanghai,'China'
Key'Findings:'Regardless'of'diabetes'duration,'HbA1c'level'was'observed'lower'in'
patients'having'a'higher'fiber'or'lower'GI'intake.'Compared'with'those'with'the'
lowest'tertile'intake'of'fiber,'the'adjusted'odds'ratios'(ORs)'for'poor'glycemic'
control'reduced'from'0.75'(95%CI:'0.541.06)'to'0.51'(95%CI:'0.340.75)'with'
increasing'tertile'intake'(P'for'trend'<0.001).'HbA1c'level'was'negatively'
Summary'of'Results' correlated'with'dietary'fiber'intake.'
'
Other'Findings:'Patients'with'HbA1c'levels'of'>7%'were'diagnosed'2.2'years'
earlier'thatn'those'were'lower'HbA1c'levels'(younger'age'at'diagnosis'and'longer'
duration),'diabetic'patients'with'HbA1c'levels'>='7.0%'appeared'less'educated'
and'diagnosed'early.''
Dietary'fiber'may'play'an'important'role'in'reducing'HbA1c'level.'Increasing'fiber'
intake'may'be'an'effective'approach'to'improve'glycemic'control'among'Chinese'
Author'Conclusion'

diabetic'patients.'Glycemic'control'should'be'more'important'in'younger'patients'
and'estbalishing'"good"'dietary'habits.''
The$strengths$of$this$study$included$the$validated$food$frequency$questionnaire,$a$
standardized$protocol$for$body$measurements,$and$stringent$quality$control$in$lab$
assays.$Due$to$the$nature$of$the$cross<sectional$design,$however,$we$could$not$

Reviewer'
Comments'

elucidate$the$role$of$dietary$factors$in$glycemic$control.$Moreover,$the$amount$of$
energy$intake$appeared$lower$than$those$reported$in$previous$studies$[30],$raising$
our$concern$on$possible$recall$bias.$However,$the$potential$underestimation$of$
dietary$intake,$if$any,$would$result$in$a$non<differential$misclassification$bias,$
which$may$have$biased$our$results$towards$the$null.$
Shanghai'Municipal'Health'Bureau,'Academic'Leaders'Training'Program'of'Pudong'

Funding'Source'

Helath'Bureau'of'Shanghai'grant'

'

Quality(Criteria(Checklist:(Primary(Research(
Symbols(Used(
+(
77(
!(

Explanation(
Positive((Indicates'that'the'report'has'clearly'addressed'issues'of'inclusion/exclusion,'
bias,'generalizability,'and'data'collection'and'analysis(
Negative((Indicates'that'these'issues'have'not'been'adequately'addressed.(
Neutral('indicates'that'the'report'is'neither'exceptionally'strong'nor'exceptionally'
week(

Select'a'rating'from'the''
dropCdown'menu'!'

Relevance(Questions(
1.! Would'implementing'the'studied'intervention'or'procedure'(if'found'successful)'result'
in'improved'outcomes'for'the'patients/clients/population'group?'(NA'for'some'Epi'
studies)'
2.! Did'the'authors'study'an'outcome'(dependent'variable)'or'topic'that'the'
patients/clients/population'group'would'care'about?'
3.! Is'the'focus'of'the'intervention'or'procedure'(independent'variable)'or'topic'of'study'a'
common'issue'of'concern'to'dietetics'practice?'
4.! Is'the'intervention'or'procedure'feasible?'(NA'for'some'epidemiological'studies)'

1'

Yes'

2'

Yes'

3'

Yes'

4'

Yes'

If(the(answers(to(all(of(the(above(relevance(questions(are(Yes,(the(report(is(eligible(for(designation(with(a(
plus((+)(on(the(Evidence(Quality(Worksheet,(depending(on(answers(to(the(following(validity(questions.'
Validity(Questions'
1.! Was(the(research(question(clearly(stated?(
1.1.! Was'the'specific'intervention(s)'or'procedure'(independent'variable(s))'
identified?'
1.2.! Was'the'outcome(s)'(dependent'variable(s))'clearly'indicated?'
1.3.! Were'the'target'population'and'setting'specified?'

1'

1.3'

Yes'
Yes'
Yes'
Yes'

2.! Was(the(selection(of(study(subjects/patients(free(from(bias?(
2.1.! Were'inclusion/exclusion'criteria'specified'(e.g.,'risk,'point'in'disease'
progression,'diagnostic'or'prognosis'criteria),'and'with'sufficient'detail'and'
without'omitting'criteria'critical'to'the'study?'
2.2.! Were'criteria'applied'equally'to'all'study'groups?'
2.3.! Were'health,'demographics,'and'other'characteristics'of'subjects'described?'
2.4.! Were'the'subjects/patients'a'representative'sample'of'the'relevant'
population?'

2'

Yes'

2.1'

Yes'

2.2'

Yes'

2.3'

Yes'

2.4'

Yes'

3'

Yes'

3.1'

No'

3.2'

Yes'

3.3'

Yes'

3.4'

Yes'

3.5'

N/A'

3.6'

N/A'

4'

N/A'

4.1'

Unclear'

4.2'

Yes'

4.3'

Unclear'

3.! Were(study(groups(comparable?(
3.1.! Was'the'method'of'assigning'subjects/patients'to'groups'described'and'
unbiased?'(Method'of'randomization'identified'if'RCT)'
3.2.! Were'distribution'of'disease'status,'prognostic'factors,'and'other'factors'(e.g.,'
demographics)'similar'across'study'groups'at'baseline?'
3.3.! Were'concurrent'controls'used?'(Concurrent'preferred'over'historical'
controls.)'
3.4.! If'cohort'study'or'crossCsectional'study,'were'groups'comparable'on'important'
confounding'factors'and/or'were'preexisting'differences'accounted'for'by'using'
appropriate'adjustments'in'statistical'analysis?'
3.5.! If'case'control'study,'were'potential'confounding'factors'comparable'for'cases'
and'controls?'(If'case'series'or'trial'with'subjects'serving'as'own'control,'this'
criterion'is'not'applicable.'Criterion'may'not'be'applicable'in'some'crossC
sectional'studies.)'
3.6.! If'diagnostic'test,'was'there'an'independent'blind'comparison'with'an'
appropriate'reference'standard'(e.g.,'gold'standard)?'

1.1'
1.2'

'
'
4.! Was(method(of(handling(withdrawals(described?(
4.1.! Were'follow'up'methods'described'and'the'same'for'all'groups?(
4.2.! Was'the'number,'characteristics'of'withdrawals'(i.e.,'dropouts,'lost'to'follow'
up,'attrition'rate)'and/or'response'rate'(crossCsectional'studies)'described'for'
each'group?'(Follow'up'goal'for'a'strong'study'is'80%.)'
4.3.! Were'all'enrolled'subjects/patients'(in'the'original'sample)'accounted'for?'''

4.4.! Were'reasons'for'withdrawals'similar'across'groups'
4.5.! If'diagnostic'test,'was'decision'to'perform'reference'test'not'dependent'on'
results'of'test'under'study?'
5.! Was(blinding(used(to(prevent(introduction(of(bias?(
5.1.! In'intervention'study,'were'subjects,'clinicians/practitioners,'and'investigators'
blinded'to'treatment'group,'as'appropriate?(
5.2.! Were'data'collectors'blinded'for'outcomes'assessment?'(If'outcome'is'
measured''using'an'objective'test,'such'as'a'lab'value,'this'criterion'is'assumed'
to'be'met.)'
5.3.! In'cohort'study'or'crossCsectional'study,'were'measurements'of'outcomes'and'
risk''factors'blinded?''
5.4.! In'case'control'study,'was'case'definition'explicit'and'case'ascertainment'not'
influenced'by'exposure'status?'
5.5.! In'diagnostic'study,'were'test'results'blinded'to'patient'history'and'other'test'
results?'
6.! Were(intervention/therapeutic(regimens/exposure(factor(or(procedure(and(any(
comparison(s)(described(in(detail?(Were(intervening(factors(described?(
6.1.! In'RCT'or'other'intervention'trial,'were'protocols'described'for'all'regimens'
studied?'
6.2.! In'observational'study,'were'interventions,'study'settings,'and'
clinicians/provider'''described?'
6.3.! Was'the'intensity'and'duration'of'the'intervention'or'exposure'factor'sufficient'
to'produce'a'meaningful'effect?'
6.4.! Was'the'amount'of'exposure'and,'if'relevant,'subject/patient'compliance'
measured?'
6.5.! Were'coCinterventions'(e.g.,'ancillary'treatments,'other'therapies)'described?'
6.6.! Were'extra'or'unplanned'treatments'described?'
6.7.! Was'the'information'for'6.4,'6.5,'and'6.6'assessed'the'same'way'for'all'groups?'
6.8.! In'diagnostic'study,'were'details'of'test'administration'and'replication'
sufficient?'

7.! Were(outcomes(clearly(defined(and(the(measurements(valid(and(reliable?(

7.1.! Were'primary'and'secondary'endpoints'described'and'relevant'to'the'
question?'''
7.2.! Were'nutrition'measures'appropriate'to'question'and'outcomes'of'concern?'
7.3.! Was'the'period'of'followCup'long'enough'for'important'outcome(s)'to'occur?'
7.4.! Were'the'observations'and'measurements'based'on'standard,'valid,'and'
reliable'data'collection'instruments/tests/procedures?'
7.5.! Was'the'measurement'of'effect'at'an'appropriate'level'of'precision?'
7.6.! Were'other'factors'accounted'for'(measured)'that'could'affect'outcomes?'
7.7.! Were'the'measurements'conducted'consistently'across'groups?'

4.4'

Unclear'

4.5'

N/A'

5'

N/A'

5.1'

N/A'

5.2'

No'

5.3'

No'

5.4'

N/A'

5.5'

N/A'

6'

Yes'

6.1'

N/A'

6.2'

Yes'

6.3'

Yes'

6.4'

Unclear'

6.5'

N/A'

6.6'

N/A'

6.7'

N/A'

6.8'

N/A'

7'

Yes'

7.1'

Yes'

7.2'

Yes'

7.3'

Yes'

7.4'

Yes'

7.5'

Yes'

7.6'

Unclear'

7.7'

Yes'

8'

Yes'

8.1'

Yes'

8.2'

Yes'

8.3'

Yes'

8.4'

N/A'

'
'
'
'
8.! Was(the(statistical(analysis(appropriate(for(the(study(design(and(type(of(outcome(
indicators?((
8.1.! Were'statistical'analyses'adequately'described'the'results'reported'
appropriately?'
8.2.! Were'correct'statistical'tests'used'and'assumptions'of'test'not'violated?'
8.3.! Were'statistics'reported'with'levels'of'significance'and/or'confidence'intervals?'
8.4.! Was'intent'to'treat'analysis'of'outcomes'done'(and'as'appropriate,'was'there'
an'analysis'of'outcomes'for'those'maximally'exposed'or'a'doseCresponse'

analysis)?'
8.5.! Were'adequate'adjustments'made'for'effects'of'confounding'factors'that'
might'have'affected'the'outcomes'(e.g.,'multivariate'analyses)?'
8.6.! Was'clinical'significance'as'well'as'statistical'significance'reported?'
8.7.! If'negative'findings,'was'a'power'calculation'reported'to'address'type'2'error?'
9.! Are(conclusions(supported(by(results(with(biases(and(limitations(taken(into(
consideration?'
9.1.! Is'there'a'discussion'of'findings?'
9.2.! Are'biases'and'study'limitations'identified'and'discussed?'
10.! Is(bias(due(to(studys(funding(or(sponsorship(unlikely?(
10.1.!Were'sources'of'funding'and'investigators'affiliations'described?'
10.2.!Was'there'no'apparent'conflict'of'interest?'

8.5'

Yes'

8.6'

Yes'

8.7'

N/A'

Yes'
9.1'
Yes'
9.2'
Yes'
10'
Yes'
10.1' Yes'
10.2' Yes'
9'

MINUS/NEGATIVE((7)(
If$most$(six$or$more)$of$the$answers$to$the$above$validity$questions$are$No,$the$report$should$be$designated$with$a$minus$$
(<)$symbol$on$the$Evidence$Worksheet.'
NEUTRAL((!)$
If$the$answers$to$validity$criteria$questions$2,$3,$6,$and$7$do$not$indicate$that$the$study$is$exceptionally$strong,$the$report$
should$be$designated$with$a$neutral$(!)'symbol$on$the$Evidence$Worksheet.'
PLUS/POSITIVE((+)$
If$most$of$the$answers$to$the$above$validity$questions$are$Yes$(including$criteria$2,$3,$6,$7$and$at$least$one$additional$
Yes),$the$report$should$be$designated$with$a$plus$symbol$(+)$on$the$Evidence$Worksheet.'

'

Journal of Ethnopharmacology 102 (2005) 202207

Psyllium decreased serum glucose and glycosylated hemoglobin


significantly in diabetic outpatients
Seyed Ali Ziai a, , Bagher Larijani b , Shahin Akhoondzadeh a , Hossein Fakhrzadeh b ,
Arezoo Dastpak a , Fatemeh Bandarian b , Afsaneh Rezai a ,
Hassanali Naghdi Badi c , Tara Emami d
a

Department of Pharmacology, Institute of Medicinal Plants, ACECR, No. 97 Bozorgmehr Street, Qods Street,
Enghelab Avenue, P.O. Box 13145-1446, Tehran, Iran
b Endocrinology & Metabolism Research Center, Tehran University of Medical Sciences, Tehran, Iran
Department of Cultivation & Development, Institute of Medicinal Plants, ACECR, and Tarbiat Modarres University, Tehran, Iran
d Department of Biotechnology, Razi Institute, Karaj, Iran
Received 8 October 2004; received in revised form 12 May 2005; accepted 7 June 2005
Available online 8 September 2005

Abstract
Psyllium is a bulk-forming laxative and is high in both fiber and mucilage. The beneficial effect of dietary fiber in the management of type II
diabetes, has not been totally demonstrated. The purpose of this study was to determine the plasma-lowering effects of 5.1 g b.i.d. of psyllium
husk fiber, as an adjunct to dietary and drug therapy on lipid and glucose levels, in patients with type II diabetes. Patients were randomly
selected from an outpatient clinic of primary care to participate in a double-blind placebo-controlled study in which Plantago ovata Forsk., or
placebo was given in combination with their anti-diabetic drugs. Forty-nine subjects were included in the study that were given diet counseling
before the study and then followed for 8 weeks in the treatment period. Fasting plasma glucose (FBS) was measured every 2 weeks, and total
plasma cholesterol (TC), LDL-cholesterol (LDL-C), HDL-cholesterol (HDL-C), triglyceride (TG), and insulin levels were measured every
4 weeks. Glycosylated hemoglobin (HbA1c) was also measured at the beginning and ending of the study. The test products (psyllium or
placebo) were supplied to subjects in identically labeled foil packets containing a 5.1 g dose of product, to consume two doses per day, half
an hour before breakfast and dinner. Both products were well tolerated, with no serious adverse events related to treatment was reported in
either. Better gastric tolerance to metformin was recorded in the psyllium group. FBS, and HbA1c, showed a significant reduction (p < 0.05),
whereas HDL-C increased significantly (p < 0.05) following psyllium treatment. LDL/HDL ratio was significantly decreased (p < 0.05). Our
results show that 5.1 g b.i.d. of psyllium for persons with type II diabetes is safe, well tolerated, and improves glycemic control.
2005 Elsevier Ireland Ltd. All rights reserved.
Keywords: Blood glucose; Cholesterol; Clinical trial; Diabetes mellitus; HbA1c; Plantago ovata Forsk; Triglycerides

1. Introduction
Psyllium seeds from the Plantago ovata Forsk., belong
to the plantaginaceae family, contain 1030% mucilage.
Psyllium is a common ingredient in over-the-counter bulk
laxative products (Leung and Foster, 1996). Numerous
double-blind trials have found that supplementation with

Corresponding author. Fax: +98 21 6465554.


E-mail address: saziai@gmail.com (S.A. Ziai).

0378-8741/$ see front matter 2005 Elsevier Ireland Ltd. All rights reserved.
doi:10.1016/j.jep.2005.06.042

Plantago psyllium can lower total cholesterol (TC), and


LDL-C (Anderson et al., 2000). Levels of HDL-C were
shown to increase by psyllium supplementation (Oson et al.,
1997). The cholesterol-lowering effect of psyllium has been
reported in children (Davidson et al., 1996), as well as in
adults (Florholmen et al., 1982). Psyllium supplementation
has also improved blood sugar levels in some people with
diabetes (Florholmen et al., 1982; Rodriguez-Moran et al.,
1998; Anderson et al., 1999). The soluble fiber component
of psyllium is believed to account for this effect. The

S.A. Ziai et al. / Journal of Ethnopharmacology 102 (2005) 202207


Table 1
Demographic characteristics of the patients in the groups studied
Parameter
Age (year)
BMI (kg/m2 )
Glibenclamide (mg/day)
Metformin (mg/day)

Psyllium (n = 21)
51.9
26.6
8.6
759

1.0
1.3
134

2.2a

Placebo (n = 15)
53.6
27.5
9.8
575

2.1
0.9
1.8
155

p-Value
0.586
0.516
0.597
0.375

203

FBS, total cholesterol and triglycerides more than 400, 300


and 500 mg/dl, respectively, were excluded from the study as
well as HbA1c more than 13%.
2.3. Interventions

2. Methods

This study was double-blind, placebo-controlled, and parallel. The study consisted of an 8-week treatment phase in
which subjects continued the diets and chemical drugs, but
were also randomly assigned to receive either 5.1 g psyllium
(psyllium group) or microcrystalline cellulose placebo (control group) twice daily. Subjects were instructed to consume
the test product 2030 min before the morning and evening
meals, by stirring the content of one packet into 250 ml of
water and drinking immediately. All patients completed a
consent form, and all of these outpatients had been given diet
counselling and were visited regularly in diabetes care clinic
every 2 months at least for 1 year before the study. A questionnaire consisted of demographic, blood pressure, familial
history of disease; concurrent disease, cigarette smoking and
drug therapy were completed at the screening time. All participants were evaluated; blood pressure and weight were
controlled and recorded in the screening period (at week 0)
and in the treatment period at weeks 2, 4, 6, and 8. Samples
of venous blood were taken for measurement of FBS, insulin,
HbA1c, TC, LDL-C, HDL-C, and triglyceride levels.

2.1. Trial organization

2.4. Test products and dosages

This was a 8-week, parallel group, double-blind, placebo


controlled trial undertaken in an diabetes care clinic in the
Shariati hospital during June 2003April 2004. Overall coordination of the trial was from the Institute of Medicinal Plants,
Tehran.

The active medication was Plantago ovata Forsk.


(Diamed , Iran Darouk Co., Tehran), containing by weight
5.1 g psyllium seed husk and inactive excipients that, in order
of descending amount, were CMC, citric acid, artificial flavor, aspartame, and coloring agents. The placebo test article
matched the active product except that it contained an inert
bulk fiber purified from microcrystalline cellulose in place of
psyllium. The test products (psyllium or placebo) were supplied to subjects in identically labelled foil packets containing
a 5.1 g dose of product. Adherence to the dosing regimen was
monitored by conducting interviews with the subjects on each
visit, by counting the number of returned unopened packages,
of psyllium or placebo, in each period of 2 weeks.

Results are shown based on mean S.E. of mean for each group.

beneficial effect of psyllium is dose related (Frati-Munari et


al., 1989). Nevertheless, the side effects of psyllium are also
dose related affecting the adherence (Tattersal and Mansell,
1990; Nuttall, 1993) so, the benefits of a high-fiber diet
on reducing glucose levels are still controversial (Tattersal
and Mansell, 1990; Nuttall, 1993) and has not been totally
studied or appropriately shown in type II diabetes. Psyllium
is nominated in Iran as ESFARZEH, and used mainly for its
emollient effect. In Iranian folk medicine, there is a report
on its anti-diabetic effect. The objective of this study was to
determine the effects of 5.1 g b.i.d. of Plantago ovata Forsk.,
as an adjunct therapy, on fasting plasma glucose (FBS),
glycosylated hemoglobin, cholesterol, and triglyceride
levels, in patients with type II diabetes.

2.2. Participants
A total of 57 patients, age 3570 years, whose diabetes
were controlled with diet only or diet plus glibenclamide
or metformin and volunteered to participate in the study
were admitted initially (Table 1). Forty-nine of them qualified for random assignment to treatment. Patients were
excluded from the study if they were receiving lipid-lowering
drugs, corticosteroids, other soluble fiber treatment, lithium,
carbamazepin, warfarin, digoxin or patients with clinically
significant renal, hepatic, gastrointestinal, pulmonary, and
thyroid disease. Individuals with a history of myocardial
infarction or major surgical procedures within the previous 6 months, as well as, a history of allergy to aspartame
or psyllium seed, or phenylketonuria were also excluded.
The trial was carried out in accordance with the Declaration of Helsinki and subsequent revisions, and approved by
the ethics committee at the Endocrinology and Metabolism
Research Center of Tehran University of Medical Sciences. The patient provided written informed consent for
participation.

2.5. Outcomes
Parameters measured were body weight, blood pressure
and fasting serum levels of glucose, HbA1c, insulin, and
lipid profile. FBS, HbA1c, TC, HDL-C, LDL-C, and triglycerides levels were measured with commercial kits by Rochehitachi 717 clinical chemistry autoanalyzer (Roche Diagnostics, Germany). Serum insulin and TSH levels were measured
by radioimmunoassay (Immunotech, France). All of the measurements were done by Bahar clinical laboratory in Tehran.
FBS was determined at weeks 0, 2, 4, 6, and 8; TC, HDL-C
and LDL-C insulin, and triglycerides levels at weeks 0, 4,
and 8; HbA1c at weeks 0 and 8.

204

S.A. Ziai et al. / Journal of Ethnopharmacology 102 (2005) 202207

2.6. Safety evaluation


All adverse events, reported or observed were recorded at
each visit. Routine physical examination was conducted on
each clinical visit.
2.7. Statistical analysis
A one-way repeated measures analysis of variance with a
two-tailed post hoc Tukey mean comparison test was undertaken on the change in FBS, TC, LDL-C, HDL-C, TG,
and insulin from baseline. To compare the change in FBS,
TC, LDL-C, HDL-C, TG, and insulin at week 8 in relation to week 0, a paired two sided Students t-tests, was
used. KruskalWallis test was employed to compare the
baseline data and frequency of side effects between two
groups.

Fig. 2. Mean (S.E.M.) of FBS levels in psyllium and placebo groups. FBS
decreased significantly in the psyllium group and in the weeks 6 and 8 the
difference between psyllium and placebo groups were significant, *p < 0.05.

ning and end of the study, in psyllium and placebo group,


respectively.
3. Results
3.1. Glucose prole
From 57 patients admitted, 49 diabetic patients were
included in the study, 27 and 22 in psyllium and placebo
group, respectively. Thirty-six of them completed the study
and 13 were dropout (Fig. 1). Demographic characteristics
for both groups, at the week 0 without statistical differences
between them, were shown in Table 1. There was no significant difference between glibenclamid and metformin dosage
in two groups (Table 1).
Counting their unopened psyllium or placebo foils,
checked patients compliance. Patients did not modify the
composition of their diets and drug regimen along the study.
Subjects in the treatment group completed the study, with
excellent tolerance to psyllium. Gastric tolerance to metformin was recorded in the psyllium group. No significant
changes were observed in the patients weight at the begin-

There were no significant differences between the two


groups at the baseline (week 0) on the FBS (t = 1.617,
d.f. = 34, p = 0.115). A one way repeated measures analysis of
variance showed a significant change from week 6 on the FBS
(p < 0.05). The changes at the end point compared to baseline were (mean (SD)): 52.77 (52.33) and 31.36 (85.74) for
psyllium and placebo, respectively (Fig. 2 and Table 2).
Insulin was not changed between and within the study
groups.
Glycosylated hemoglobin measured, as HbA1c was significantly different between the groups (p < 0.05). It was significantly decreased from 10.5 (0.73) to 8.9% (0.23) in the
psyllium group (p < 0.001) and increased from 9.1 (0.51)
to 10.5% (0.59) in the placebo group (p < 0.05) (Table 2).

Fig. 1. Trial profile.

216.2 25.3
216.5 11.3
36.2 2.4
142.1 10.4
193.4 20.9
9.1 0.8
10.5 0.6
4.1 0.5
8.3
2.0*
8.1
22.4
1.1
0.2*
0.3*

p-Value

Flatulence
Diarrhoea
Constipation
Reduced flushing

4
1
1
11

13
1
1
0

0.000
0.809
0.809
0.002

155.6
216.2
42.9
131.3
186.0
7.4
8.9
3.2

Placebo

Total serum cholesterol levels, low-density lipoprotein


fraction, and triglycerides levels showed no significant
changes. The high-density lipoproteins decreased significantly in the placebo group and increased non-significantly
in the psyllium group, but overall it was different in the week
8 between the study groups (Table 2). LDL/HDL ratio was
also significantly different in week 8.

161.6
11.0
7.2
1.9
6.8
18.6
0.7

3.1 0.3

4. Discussion

Results are shown based on mean S.E. of mean for each group.
p < 0.05 significant difference between placebo and psyllium groups.
*

179.1
224.3
48.9
131.8
219.0
8.3
9.1
2.8
12.7
8.5
2.1
8.2
20.2
0.8
0.7
0.2
208.2
207.2
40.2
126.0
217.6
7.5
10.5
3.24
FBS (mg/dl)
Total Cholesterol (mg/dl)
HDL-C (mg/dl)
LDL-C (mg/dl)
Triglycerides (mg/dl)
Insulin (U/ml)
HbA1c (%)
LDL/HDL

10.8
15.4
3.9
11.6
17.0
1.2
0.5
0.2

Psyllium
Placebo
Psyllium

178.4 12.7

194.1 13.4

169.3
193.9
39.8
108.3
207.6
8.0

Adverse effects were recorded in each visit, which are


shown in Table 3. Flatulence was significantly high in the
placebo group. Psyllium group tolerated metformin better
than placebo and hot flushing was significantly abolished in
the psyllium group.

2.8 0.2

10.9
9.7
2.5
9.7
25.3
0.8

193.6
204.4
40.2
119.2
239.3
8.9

Placebo
Psyllium

3.3. Safety and tolerance

Week 2

Placebo

Psyllium

207.5 19.8

Psyllium
Psyllium

Week 6
Week 4

Effect

3.2. Lipid prole

Week 0a

Table 2
Glucose and lipid profiles in the study groups

205

Table 3
Study of side effects in psyllium and placebo group

10.7*

Placebo

Week 8

9.5*

Placebo

S.A. Ziai et al. / Journal of Ethnopharmacology 102 (2005) 202207

High-fiber supplements, such as psyllium (Florholmen et


al., 1982; Rodriguez-Moran et al., 1998) guar gum (found in
beans) (Landin et al., 1992) pectin (from fruit) (Schwartz et
al., 1988) oat bran (Hallfrisch et al., 1995), and glucomannan (Doi et al., 1979; Vuksan et al., 2000) have improved
glucose tolerance in some studies. Psyllium fiber as a meal
supplement reduces proximate and second meal postprandial
glucose and insulin concentrations in NIDDM (Pastors et al.,
1991). Plantago psyllium and acarbose, both significantly
reduce glycemic index of carbohydrate food (Frati Munari et
al., 1998). Our results showed that 8 weeks treatment with
5.1 g psyllium (Plantago ovata) two times daily half an hour
before breakfast and dinner, could reduce FBS, and control glucose fluctuations by reducing HbA1c significantly.
It also reduced TG non-significantly but had no effect on the
total cholesterol and LDL-C. HDL-C was reduced in placebo
group while it increased in psyllium group, and overall HDLC changed significantly between two treatment groups. In
calculation, LDL/HDL ratio decreased significantly. In a
double-blind trial, men with diabetes type II took 5.1 g of
psyllium (Plantago psyllium) twice daily for 8 weeks. HDL-C
increased significantly in the outpatients and glucose, HbA1c,
TC, LDL-C and TG didnt change any, but in metabolic
ward they showed significant improvement in glucose and
lipid profile compared to the placebo group (Anderson et al.,
1999). In one study, 6 weeks treatment with 14 g/day psyllium, glucose absorption significantly decreased, and HbA1c

206

S.A. Ziai et al. / Journal of Ethnopharmacology 102 (2005) 202207

decreased non-significantly, that may be due to short time of


the treatment (Sierra et al., 2002). In another clinical study
5 g psyllium (Plantago psyllium) t.i.d. decreased TC, TG, and
LDL-C, as well as, increased HDL-C significantly in week 12
(Rodriguez-Moran et al., 1998). In another crossover study
on only hyperchlosterolemic patients, 12 g psyllium for 6
weeks caused significant decrease in TC and LDL, but no
significant changes in HDL-C or TG (Roberts et al., 1994).
In a longer period study for 90 days in 24 patients, psyllium
3.5 g twice daily caused TC, LDL-C, and TG decrease, as
well as HDL-C increased significantly (Gupta et al., 1994).
So the beneficial effect of dietary fiber on glucose serum and
cholesterol levels varies according to the dosage and period
used and we can conclude that the glucose and cholesterol
lowering effects of psyllium in low doses and long term are
equal to high doses in short term (Leatherdale et al., 1982;
Smith and Holm, 1982; Ray et al., 1983; Jarjis et al., 1984;
Bell et al., 1989; Hunt et al., 1993; Sprecher et al., 1993;
Gupta et al., 1994; Bennet and Cerda, 1996) Considering
that ingestion of soluble fiber before regular meals could be
a factor to improving the customary diet content; this study
was conducted to evaluate the efficacy and tolerability of
psyllium (Plantago ovata) as an adjunct therapy in diabetic
outpatients in comparison to placebo, and all patients needed
to treat for their hypercholesterolemia (LDL-C > 100 mg/dl
in diabetic patients must be treated) (Third Report of the
National Cholesterol Education Program, 2002) Significant
reduction in FBS and HbA1c in psyllium group shows that
5.1 g psyllium twice daily can control blood glucose effectively. Significant decrease in LDL/HDL ratio by psyllium
shows the usefulness of this product in hypercholesterolemia.
Not only no adverse effects were investigated in the psyllium
group, but also it increased gastric tolerance to metformin.
In the placebo group, most noticed adverse effect was flatulence. Lack of significant TC, LDL-C and TG changes in our
study may be due to the short period of treatment (8 weeks),
which has caused a non-significant lipid profile change, or it
may be related to plant species difference between our trial
with other trials (Frati Munari et al., 1998; Rodriguez-Moran
et al., 1998; Anderson et al., 1999). There were no significant
changes in BMI whether or not the subjects were on psyllium
or placebo during the study, so weight loss or reduced food
intake did not explain effects of psyllium on the glucose and
lipid levels.
In conclusion, our results show that 5.1 g b.i.d. of psyllium
(Plantago ovata Forsk.), a natural soluble fiber supplement,
is useful as an adjunct to dietary therapy in patients with type
II diabetes, to reduce glucose, with excellent tolerance.

Acknowledgements
The authors thank Endocrinology and Metabolism
Research Center of Tehran University of Medical Sciences,
which supported this work and Dr. S.A. Ebrahimi for his
help.

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Dietary Fiber Intake Is Associated with HbA1c Level


among Prevalent Patients with Type 2 Diabetes in
Pudong New Area of Shanghai, China
Junyi Jiang1, Hua Qiu2, Genming Zhao1, Yi Zhou2, Zhijie Zhang1, Hong Zhang2, Qingwu Jiang1,
Qiao Sun2, Hongyan Wu2, Liming Yang2, Xiaonan Ruan2*, Wang-Hong Xu1*
1 Key Laboratory of Public Health Safety, Department of Epidemiology, School of Public Health, Ministry of Education, Fudan University, Shanghai, Peoples Republic of
China, 2 Pudong New Area Centers for Disease Control and Prevention, Shanghai, Peoples Republic of China

Abstract
Background: Dietary factors play an important role in glycemic control in diabetic patients. However, little is known about
their effects among Chinese diabetic patients, whose diets are typically abundant in fiber and high in glycemic index (GI)
values.
Methodology/Principal Findings: 934 patients with type 2 diabetes and 918 healthy volunteers from Pudong New Area,
Shanghai, China, were interviewed during the period of Oct-Dec, 2006 to elicit demographic characteristics and lifestyle
factors. Dietary habits were assessed using a validated food frequency questionnaire. Anthropometric measurements, biospecimen collection and biochemical assays were conducted at the interview according to a standard protocol. In this
population, diabetic patients consumed lower levels of energy and macronutrients but had higher levels of fasting plasma
glucose (FPG), glycolated hemoglobin A1c (HbA1c), triglyceride and body mass index than healthy adults. While the average
consumption levels of the nutrients among diabetic patients did not vary along duration of the disease, the average levels
of FPG and HbA1c increased with increasing duration. Regardless of diabetes duration, HbA1c level was observed lower in
patients having a higher fiber or lower GI intake. Compared with those with the lowest tertile intake of fiber, the adjusted
odds ratios (ORs) for poor glycemic control reduced from 0.75 (95%CI: 0.541.06) to 0.51 (95%CI: 0.340.75) with increasing
tertile intake (P for trend ,0.001).
Conclusions: Dietary fiber may play an important role in reducing HbA1c level. Increasing fiber intake may be an effective
approach to improve glycemic control among Chinese diabetic patients.
Citation: Jiang J, Qiu H, Zhao G, Zhou Y, Zhang Z, et al. (2012) Dietary Fiber Intake Is Associated with HbA1c Level among Prevalent Patients with Type 2 Diabetes
in Pudong New Area of Shanghai, China. PLoS ONE 7(10): e46552. doi:10.1371/journal.pone.0046552
Editor: Noel Christopher Barengo, Fundacion para la Prevencion y el Control de las Enfermedades Cronicas No Transmisibles en America Latina (FunPRECAL),
Argentina
Received March 13, 2012; Accepted September 5, 2012; Published October 16, 2012
Copyright: 2012 Jiang et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits
unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: This research was funded by Shanghai Municipal Health Bureau (08GWZX0201) and Academic Leaders Training Program of Pudong Health Bureau of
Shanghai (Grant No. PWRd2010-03). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing Interests: The authors have declared that no competing interests exist.
* E-mail: wanghong.xu@fudan.edu.cn (WX); ruan_118@hotmail.com (XR)

Chinese people consume more abundant types of foods, and


have higher levels of dietary fiber and GI intake comparing with
their western counterparts [9]. It is reported that average level of
total and soluble fiber intake in Chinese diabetic patients were
26.5 and 10.4 gram per day (g/d), respectively [10], above the
moderate amount of fiber intake recommended by the American
Diabetes Association (ADA) (total, 24 g/d; 8 g/d of soluble fiber
and 16 g/d of insoluble fiber) [11]. However, the status of
glycemic control and prevalence of complications in diabetic
patients in China have been not satisfactory [12].
To evaluate the association of dietary factors with diabetic
control status among Chinese patients with type 2 diabetes, we
conducted a cross-sectional study including 934 adult patients
from Pudong New Area of Shanghai, China. Our results may help
to better understand the role of dietary factors in the control of
type 2 diabetes.

Introduction
Type 2 diabetes is an important risk factor for micro-vascular
and macro-vascular complications. Effective control of hyperglycemia, dyslipidemia and hypertension, either by medication or by
lifestyle intervention, is crucial to decrease the incidence of stroke,
myocardial infarction and renal disease, as well as the related
premature death [1,2]. Intervention studies have examined the
impact of dietary intake on glycemic control, and found that
higher intake of dietary fiber [3,4] and lower intakes of dietary fat
[5], glycemic index (GI) [6] and carbohydrate [7] improved
glycemic control status. In the Nurses Health Study, He, et al [8]
observed a potential benefit of whole grain, cereal fiber and bran
intake in reducing mortality and cardiovascular risk in diabetic
patients. None of these studies, however, were conducted in
Chinese population.

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Dietary Fiber Intake and HbA1c Level

diet. We excluded from the analysis 3 women who had total


energy intake ,500 kcal/d or .3500 kcal/d and 5 men with
energy intake of ,800 kcal/d or .4000 kcal/d.

Materials and Methods


Study participants
In this cross-sectional design, a total of 979 adults diagnosed
with type 2 diabetes were randomly selected from the Diabetes
Administration Rosters in communities of Shanggang, Zhoujiadu,
Huamu, Puxin, Weifang, Jinyang, Meiyuan and Jichang of
Pudong New Area of Shanghai in Oct, 2006. All patients were
diagnosed with type 2 diabetes by doctors according to ADA
criteria: 1) fasting plasma glucose $7.0 mmol/L; or 2) two-hour
plasma glucose $11.1 mmol/L during an oral glucose tolerance
test; 75-g glucose load should be used; or 3) a random plasma
glucose concentration $11.1 mmol/L in persons with symptoms
of hyperglycemia or hyperglycemic crisis. Exclusion criteria
included the occurrence of a cardiovascular event during the
previous 6 months, advanced congestive heart failure, unstable
angina, major depression and dementia. Of the 934 patients
interviewed, 41.7% were male. The mean age of the participants
was 64.5 (SD, 10.1) years old.
At the same time, a total of 918 adult volunteers free of diabetes
were recruited from the spouses and neighbors of the diabetic
patients. The mean age of these volunteers was 57.7 (SD, 9.9)
years old, and 291(31.7%) were male.
The study was approved by Fudan University Institutional
Review Board (IRB00002408, FWA00002399). Written informed
consent was obtained from each participant before data collection.

Metabolic phenotype measurements


At the interview, each participant was measured for his/her
body height, weight, waist circumference, hip circumference,
systolic blood pressure (SBP), and diastolic blood pressure (DBP)
according to a uniform and standardized protocol. Body mass
index (BMI) was calculated as weight (kg) divided by height
squared (m2).
After at least 10 hours of overnight fasting, a 1,1.5 ml venous
blood specimen was collected in a vacuum tube containing sodium
fluoride for the measurement of plasma glucose and HbA1c, and a
3,3.5 ml non-anticoagulated venous blood specimen was collected simultaneously for the measurement of total cholesterol
(TC), triglyceride (TG), high density lipoprotein cholesterol
(HDLC) and low density lipoprotein cholesterol (LDLC).
Enzymology methods were used to measure the fasting plasma
glucose (FPG) level (GOD-PAP), concentrations of TG (GPOPAP) and TC (CHOD-PAP) on an Automatic Biochemical
Analyzer (HITACHI 7170A, Hitachi, Ltd, Tokyo, Japan). Levels
of HDLC and LDLC were measured using a selective inhibition
method. HbA1c was tested using ion exchange chromatography
on DS5 Glycated Hemoglobin Analyzer (DREW DS5, Drew
Scientific Co. Ltd, Cumbria, UK). Quality control of the assays
was assessed internally and externally. The inter-assay coefficient
of variation was ,1.82% for FPG (SD,0.23 mmol/L), ,1.38%
for TG (SD,0.02 mmol/L), ,1.54% for TC (SD,0.08 mmol/
L), ,1.6% for HDLC (SD,0.01 mmol/L), ,5.3% for LDLC
(SD,0.21 mmol/L), and 6.13% for HbA1c (SD,0.77).

Data collection
A structured in-person interview was conducted for each subject
by trained interviewers to collect information on demographic
characteristics, duration of diabetes, age at onset of diabetes,
diagnosis of hypertension, presence of dyslipidemia, use of tobacco
and alcohol. Presence of hypertension, dyslipidemia and coronary
heart disease were defined by a positive response to the question of
Have you ever been diagnosed with hypertension/dyslipidemia/
coronary heart disease by a doctor?. Family history of diabetes
was defined as positive if any first- or second-degree relative had
type 2 diabetes. Smoking was defined as at least 1 cigarette per day
for at least 6 months, and alcohol use was defined as drinking
alcohol at least 3 times a week for more than 6 months.
Dietary habit was assessed using an interviewer-administered
food frequency questionnaire (FFQ) modified based on a validated
FFQ [13]. The FFQ specifies 103 food items, covering 90% of
food items commonly consumed in Shanghai. For each food item,
participants were asked to report how frequently (daily, weekly,
monthly, annually or never) and how long (months per year) they
consumed the food, followed by a question on the amount of
consumption in liang (1 liang = 50 g) per unit of time in previous 12
months. For liquid foods such as milk, juice and beverage, the
amount of intake was reported in milliliter (ml) and was
transformed into gram in the analysis. The daily intakes of oil,
salt and sugar were calculated as the average level consumed by
each family member of the participant.
Nutrient content from the Chinese Food Composition Tables
was applied to estimate nutrient intake from all food items and
groups, and to obtain GI values for most food items [14]. For the
remaining food items, we referenced Foster-Powell et als report to
obtain their GI values [15]. Glycemic load (GL) from each food
was calculated by multiplying the foods GI value by the
carbohydrate content of the food and the average amount of the
food consumed per day. Total dietary GL was then produced by
summing these products over all food items. Dietary GI was
derived by dividing the dietary GL by the amount of carbohydrate
intake, thus yielding a weighted average GI for each individuals
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Statistical analysis
Statistical analyses were conducted utilizing SAS statistical
software 9.2 (SAS Institute Inc., Cary, NC). Differences on
demographic factors by diabetic status or glycemic control status
were evaluated using x2 test for categorical variables or nonparameter Wilcoxon test for continuous variables. Partial correlation analysis was conducted to evaluate the linear correlations of
HbA1c levels with amounts of dietary intake. A generalized linear
regression model was applied to compare the average levels of
biochemical measurements and average levels of dietary intake.
An unconditional logistic regression model was employed to
estimate the adjusted odds ratios (ORs) and 95% confident
intervals (CIs) of dietary intake with glycemic control status among
diabetic patients. Natural log transformation was applied to
normalize the distribution of biochemical measurements before
parametric methods were used in data analysis. All statistical tests
were based on two-sided probability.

Results
Compared with the recruited healthy volunteers, diabetic
patients were older and less educated, had more family history
of diabetes and higher prevalence of hypertension, dyslipidemia
and coronary heart disease (CHD), as shown in Table 1. Among
934 prevalent diabetic patients, 488 (52.3%) had an HbA1c level
of $7.0%. These patients, compared with those having an HbA1c
level of ,7.0%, appeared to have less education, younger age at
diagnosis of diabetes, longer duration of diabetes, lower prevalence
of hypertension and were more likely to use oral hypoglycemia
drug and insulin. No significant difference was observed between
the two groups with regard to age, sex, smoking, alcohol

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Dietary Fiber Intake and HbA1c Level

Table 1. Comparison of demographic characteristics of participants of the study.

Characteristics

Healthy adults
(N = 918)

Diabetic patients
(N = 934)
P value

Diabetic patients

P valuea

HbA1c,7.0% (N = 446)

HbA1c$7.0% (N = 488)

Age, years (mean, SD)

57.7 (9.9)

64.5 (10.1)

,0.001

64.6 (10.1)

64.4 (10.1)

0.825

Sex, male, n (%)

291 (31.7)

389 (41.7)

,0.001

191 (42.8)

198 (40.6)

0.487

Educational level, high school816 (88.9)


or below, n (%)

864 (92.5)

0.008

400 (89.9)

465 (94.9)

0.004

Family history of diabetes,


yes, n (%)

88 (9.6)

298 (31.9)

,0.001

130 (29.2)

168 (34.4)

0.084

Diagnosis age of DM, years


(mean, SD)

55.2 (10.4)

56.4 (10.4)

54.2 (10.0)

0.002

Duration of DM, years (mean,


SD)

9.2 (6.4)

8.2 (6.3)

10.2 (6.3)

,0.001

Prior history of hypertension, 293 (31.9)


n (%)

518 (55.5)

,0.001

265 (59.4)

253 (51.8)

0.020

Prior history of dyslipidemia, 61 (6.6)


n (%)

97 (10.4)

0.004

55 (12.3)

42 (8.6)

0.062

Prevalence of CHD, n (%)

132 (14.1)

,0.001

73 (16.4)

59 (12.1)

0.061

46 (5.0)

Current smoking, n (%)


Men

134 (46.1)

152 (39.1)

0.068

70 (36.7)

82 (41.4)

0.336

Women

6 (1.0)

5 (0.9)

0.944

2 (0.8)

3 (1.0)

1.000

Current alcohol consumption,


n (%)
Men

113 (33.8)

108 (27.8)

0.002

49 (25.7)

59 (29.8)

0.362

Women

21 (3.4)

10 (1.8)

0.108

5 (2.0)

5 (1.7)

1.000

Oral hypoglycemic drug use,


n (%)

762 (81.5)

341(76.5)

421(87.0)

,0.001

Insulin use, n (%)

88 (9.4)

31(7.0)

57(11.8)

0.012

Missing values (1 for age, education, diagnosis age of DM, duration of DM in diabetic patients; 1 for current alcohol consumption in healthy adults; 4 for oral
hypoglycemic drug use and insulin use) were excluded;
a 2
x test for categorical variables or non parameter Wilcoxon test for continuous variables.
doi:10.1371/journal.pone.0046552.t001

consumption, family history of diabetes, presence of dyslipidemia


and prior history of CHD.
As shown in Table 2, the diabetic patients, both men and
women, seemed to remain a stable dietary habit along duration of
diabetes (P.0.05 for all tests). These patients, either with a short
or a long duration of type 2 diabetes, had lower levels of energy,
carbohydrate, protein, and fat intake than did healthy volunteers
after adjusting for age and other potential confounders (P,0.01).
Dietary fiber (soluble only), GI and GL intake were also lower in
diabetic patients than in healthy volunteers, but the difference
reached significance for GI and GL only among women.
Presented in Table 3 was the comparison of average levels of
metabolic indicators by diabetic status and by duration of type 2
diabetes. After adjustment of age and sex, higher levels of FPG,
HbA1c, TG and BMI and a lower level of LDLC were observed
among diabetic patients than in healthy adults. Among diabetic
patients, the average levels of FPG, HbA1c increased and BMI
decreased with increasing duration of the disease after adjusting
for age, sex, oral hypoglycemic drug use and insulin use (P for
trend ,0.05). No significant upward trend was observed for
average levels of TC, TG, LDLC and HDLC along with duration
of the disease.
In diabetic patients, HbA1c level was negatively correlated with
dietary fiber intake (r = 20.079, p = 0.017), and positively with
dietary GI intake (r = 0.070, p = 0.034) after adjusting for age, sex,
oral hypoglycemic drug use and insulin use. No significant linear
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correlation was observed for HbA1c level with other nutrients


(data not shown). Therefore, we further compared the average
levels of HbA1c by dietary fiber and GI intake among diabetic
patients (Figure 1). Regardless of duration of type 2 diabetes,
HbA1c level was consistently higher in patients consuming lower
level of fiber. HbA1c level was also higher among patients having
higher GI intake, but the difference did not reach significance.
We further evaluated the associations of dietary factors with
glycemic control status which was defined poor as HbA1c
$7.0% (Table 4). Compared with the patients having the lowest
tertile intake of dietary fiber, the adjusted ORs for poor glycemic
control decreased from 0.75 (95%CI: 0.541.06) for those having
medium intake to 0.51 (95%CI: 0.340.75) for those with the
highest tertile intake (P for trend ,0.001). No significant
association was observed for other dietary factors.

Discussion
In this cross-sectional study including 934 Chinese prevalent
patients with type 2 diabetes from Pudong New Area of Shanghai,
China, we observed a stable after-diagnosis dietary habit, upward
trend of HbA1c level along with duration of diabetes, a lower
average level of HbA1c related with higher fiber intake, and a
probably protective effect of dietary fiber on glycemic control
status. Our findings have several implications in improving

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Dietary Fiber Intake and HbA1c Level

Table 2. Average levels of dietary intake by diabetic status and duration of type 2 diabetes.

Dietary factors (Mean, SD)

Diabetic
Healthy adults patients
(N = 918)
(N = 934)

P valueb

Diabetic patients, duration of DM, years


,5 (N = 230)

59 (N = 316)

$10 (N = 387)

P valuec

Men
Energy, kcal/d

1931.2 (1.4)

1644.1 (1.3)

,0.001

1740.8 (1.3)

1600.0 (1.3)

1615.5 (1.3)

0.225

Carbohydrate, g/d

323.6 (1.4)

268.2 (1.3)

0.003

282.5 (1.3)

263.9 (1.3)

261.6 (1.3)

0.583

Protein, g/d

68.9 (1.4)

61.5 (1.5)

0.003

65.1 (1.5)

58.3 (1.4)

62.0 (1.4)

0.467

Fiber, g/d

10.2 (1.6)

9.2 (1.7)

0.232

9.9 (1.6)

8.4 (1.6)

9.6 (1.7)

0.045

Fat, g/d

40.9 (1.6)

37.1 (1.6)

0.002

40.0 (1.5)

35.3 (1.6)

36.9 (1.6)

0.485

Average GI

61.5 (1.1)

60.4 (1.2)

0.323

61.0 (1.2)

61.4 (1.1)

59.2 (1.2)

0.230

Average GL

104.7 (1.4)

87.6 (1.4)

0.347

93.3 (1.4)

84.0 (1.4)

86.5 (1.4)

0.670

Energy, kcal/d

1695.2 (1.3)

1410.5 (1.3)

,0.001

1445.2 (1.4)

1438.3 (1.4)

1367.4 (1.3)

0.438

Carbohydrate, g/d

279.2 (1.3)

226.3 (1.4)

,0.001

234.0 (1.4)

231.4 (1.4)

217.9 (1.4)

0.878

Protein, g/d

61.8 (1.4)

52.9 (1.5)

,0.001

54.3 (1.5)

53.7 (1.5)

51.2 (1.5)

0.973

Fiber, g/d

10.2 (1.6)

8.5 (1.7)

0.460

8.8 (1.7)

8.4 (1.7)

8.3 (1.7)

0.868

Fat, g/d

38.4 (1.6)

33.4 (1.6)

,0.001

33.5 (1.6)

33.8 (1.7)

32.9 (1.5)

0.797

Average GI

59.9 (1.1)

59.2 (1.2)

,0.001

59.3 (1.1)

59.6 (1.2)

58.7 (1.2)

0.733

Average GL

92.1 (1.4)

74.2 (1.4)

,0.001

76.8 (1.4)

75.7 (1.4)

71.5 (1.4)

0.783

Women

Continuous variables were all natural LOG transformed before entering models;
Generalized linear model adjusting for age, BMI and energy intake;
c
Generalized linear model adjusting for age, BMI, oral hypoglycemic drug use, insulin use and energy intake.
doi:10.1371/journal.pone.0046552.t002
b

Secondly, the significant difference in dietary habit between


patients and healthy adults suggests that a diabetic patient could
greatly change his/her dietary habit just due to diagnosis of type 2
diabetes. The stable dietary habit along the duration of the disease
in patients, on the other hand, indicates that a new dietary habit,
once established, would remain unchanged for a long time. These
results implicate the importance of the time point of diagnosis in
establishing a new good dietary habit. Dietary intervention and
health education should be extensively elicited at the time point.

diabetic control status and preventing complications among


Chinese diabetic patients.
Firstly, in this study, the patients with an HbA1c level of $7.0%
were diagnosed with type 2 diabetes 2.2 years earlier than those
with a lower HbA1c level, and had a 2 years longer duration of the
disease. The result is consistent with several previous studies, in
which younger age at diagnosis and longer duration were regarded
as independent predictors for poor glycemic control in diabetic
patients [1618]. The result suggests that more attention in
glycemic control should be paid to the younger patients.

Table 3. Average levels of metabolic indicators by diabetic status and duration of type 2 diabetes.

Indicatorsa (Mean, SD)

Diabetic
Healthy adultspatients

P valueb

Diabetic patients, duration of DM, years


,5 (N = 230)

P valuec

(N = 918)

(N = 934)

59 (N = 316) .9 (N = 387)

FPG, mmol/L

5.3 (1.2)

8.0 (1.4)

,0.001

7.2 (1.3)

8.1 (1.4)

8.5 (1.4)

,0.001

HbA1c (%)

5.9 (1.1)

7.4 (1.2)

,0.001

6.9 (1.2)

7.4 (1.2)

7.7 (1.2)

,0.001

TC, mmol/L

4.5 (1.2)

4.4 (1.2)

0.003

4.4 (1.2)

4.4 (1.2)

4.4 (1.2)

0.733

TG, mmol/L

1.3 (1.7)

1.4 (1.8)

,0.001

1.5 (1.8)

1.4 (1.7)

1.4 (1.8)

0.508

LDLC, mmol/L

2.8 (1.3)

2.7 (1.4)

,0.001

2.7 (1.4)

2.7 (1.3)

2.7 (1.4)

0.177

HDLC, mmol/L
Men

1.1 (1.3)

1.1 (1.2)

0.998

1.1 (1.2)

1.1 (1.1)

1.2 (1.1)

0.111

Women

1.3 (1.3)

1.3 (1.3)

0.224

1.3 (1.3)

1.3 (1.2)

1.3 (1.3)

0.266

24.8 (1.1)

25.6 (1.1)

0.005

25.8 (1.2)

25.7 (1.1)

24.8 (1.1)

0.002

BMI
a

Continuous variables were all natural LOG transformed before entering models;
Generalized linear model adjusting for age and gender;
Generalized linear model adjusting for age, gender, oral hypoglycemic drug use and insulin use.
doi:10.1371/journal.pone.0046552.t003

b
c

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Dietary Fiber Intake and HbA1c Level

Figure 1. Average levels of HbA1c by duration of type 2 diabetes and dietary fiber or GI intake. The low and high fiber or GI intakes were
classified by the medians of consumption in men and women, respectively. Means of HbA1c level were adjusted for age (as a continuous variable),
sex (male/female), duration of type 2 diabetes (as a continuous variable), BMI (as a continuous variable), oral hypoglycemic drug use (yes/no), insulin
use (yes/no) and energy intake (as a continuous variable).
doi:10.1371/journal.pone.0046552.g001

fiber intake. Whereas Haimoto, et al [7] found that a 6-month low


carbohydrate diet (30% of energy intake from carbohydrate)
decreased HbA1c level from 10.9% to 7.4% among 33 severe
diabetic outpatients, Wolever, et al [22] did not observe a
beneficial effect of a low-carbohydrate diet in glycemic status.
The null associations of carbohydrate and GL intake with HbA1c
level in our patients indicate that the two dietary factors play a
limited role in glycemic control in our population.
In this study, we did not find an association of HbA1c levels
with dietary protein intake, consistent with Larsen et als results
[28], but not with Pearce et als findings [29]. The null association
with dietary fat is also inconsistent with a randomized clinical trial,
in which both a low-fat vegan diet and a traditional diet according
to the ADA guidelines decreased HbA1c level in 99 individuals
with type 2 diabetes after a 22-week follow up [5].
Finally, we observed that HbA1c level was consistently
associated with dietary fiber intake regardless of duration of the
disease, suggesting that dietary intervention may make a difference
at any time during the progression of the disease.
The strengths of this study included the validated food
frequency questionnaire, a standardized protocol for body
measurements, and stringent quality control in lab assays. Due
to the nature of the cross-sectional design, however, we could not
elucidate the role of dietary factors in glycemic control. Moreover,
the amount of energy intake appeared lower than those reported
in previous studies [30], raising our concern on possible recall bias.
However, the potential underestimation of dietary intake, if any,
would result in a non-differential misclassification bias, which may
have biased our results towards the null.
In summary, this small-scale cross-sectional study indicates the
potential role of dietary fiber in glycemic control. Our results, if
confirmed, may have clinic and public health implications in
diabetic control among Chinese adults.

In both healthy and diabetic subjects of this study, the average


levels of dietary fiber intake reached moderate amount of fiber
intake recommended by ADA. In this population with high
average level of dietary fiber intake, dietary fiber was still linked to
better glycemic control status, supporting the beneficial effect of
dietary fiber on the control of type 2 diabetes. We also find that, it
was GI, but not carbohydrate or GL intake, that was correlated
with HbA1c level. The results indicate that the quality of the
carbohydrates consumed may play a more important role than the
quantity of the macronutrient in the control of type 2 diabetes.
Dietary GI and GL are two physiological indexes of the metabolic
effects of dietary carbohydrates [15,19]. While GI is used to
characterize foods that contain carbohydrates according to their
postprandial blood glucose response and hence their effect on
blood insulin levels [19,20], GL is introduced to quantify the
overall estimate of postprandial glycemia by combining the GI
value and the quantity of carbohydrates consumed [15,20]. Our
finding of the improved glycemic control status related to dietary
fiber intake is consistent with the previous studies [4,6,21]. The
insignificant adverse effect of GI intake, on the other hand, was
supported only by Wolever et als report [22], but not consistent
with most previous studies in which a low-GI diet significantly
improved glycemic control by reducing HbA1c levels among
diabetic patients [6,2325]. It is of note that, even if it effected on
glucose metabolism, a low-GI diet was not a practical intervention
tool in controlling diabetes [26]. Increasing dietary fiber intake
may be an effective approach.
Regarding the role of carbohydrate and GL intake, the results
have been controversial. While Lau, et al [27] reported that the
inverse association of carbohydrate and daily GL intake with
HOMA-IR can be explained by dietary fiber, Esposito, et al [25]
found that diet high in GL was significantly associated with higher
HbA1c and postmeal glucose levels in a dose-dependent manner
among 901 diabetic outpatients even after adjusting for dietary
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Dietary Fiber Intake and HbA1c Level

Table 4. Associations of dietary intake with glycemic control status among diabetic patients.

Dietary intakea

HbA1c, % (Mean,
Glycemic control status, N (%)
SD)
Controlled (HbA1c,7.0%)

OR (95%CI)b

P for trend

Uncontrolled (HbA1c$7.0%)

Energy (kcal/d)
Low

7.5 (1.4)

143 (32.2)

165 (34.2)

1.00

Medium

7.6 (1.7)

139 (31.3)

170 (35.3)

1.03 (0.74, 1.44)

High

7.5 (1.7)

162 (36.5)

147 (30.5)

0.93 (0.71, 1.22)

Low

7.6 (1.5)

137 (30.9)

171 (35.5)

1.00

Medium

7.5 (1.6)

147 (33.1)

163 (33.8)

0.85 (0.59, 1.23)

High

7.5 (1.8)

160 (36.0)

148 (30.7)

0.69 (0.40, 1.16)

0.300

Carbohydrate (g/d)

0.166

Protein (g/d)
Low

7.6 (1.5)

135 (30.4)

172 (35.7)

1.00

Medium

7.5 (1.6)

151 (34.0)

159 (33.0)

0.75 (0.52, 1.08)

High

7.5 (1.8)

158 (35.6)

151 (31.3)

0.62 (0.38, 1.01)

0.052

Fiber (g/d)
Low

7.7 (1.5)

126 (28.4)

182 (37.8)

1.00

Medium

7.5 (1.5)

148 (33.3)

162 (33.6)

0.75 (0.54, 1.06)

High

7.4 (1.8)

170 (38.3)

138 (28.6)

0.51 (0.34, 0.75)

,0.001

Fat (g/d)
Low

7.5 (1.5)

139 (31.3)

168 (34.9)

1.00

Medium

7.4 (1.6)

167 (37.6)

144 (29.9)

0.72 (0.51, 1.02)

High

7.7 (1.8)

138 (31.1)

170 (35.3)

1.16 (0.76, 1.77)

0.630

Average GI
Low

7.5 (1.6)

145 (32.7)

163 (33.8)

1.00

Medium

7.4 (1.7)

165 (37.2)

144 (29.9)

0.88 (0.64, 1.23)

High

7.7 (1.6)

134 (30.2)

175 (36.3)

1.25 (0.90, 1.75)

0.184

Average GL
Low

7.6 (1.6)

141 (31.8)

166 (34.4)

1.00

Medium

7.6 (1.6)

139 (31.3)

172 (35.7)

1.00 (0.70, 1.45)

High

7.5 (1.7)

164 (36.9)

144 (29.9)

0.68 (0.41, 1.12)

0.154

a
Dietary factors were classified as low, medium and high intake by the tertiles in men and in women, respectively. The cut points for energy intake were 1444.06 and
1842.84 kcal/d in men and 1268.88 and 1623.31 kcal/d in women; for carbohydrate were 248.93 and 295.77 g/d in men and 205.85 and 267.65 g/d in women; for
protein intake were 50.89 and 72.42 g/d in men and 44.88 and 62.71 g/d in women; for fiber intake were 7.12 and 11.32 g/d in men and 6.73 and 10.51 g/d in women;
for fat were 31.02 and 44.62 g/d in men and 28.74 and 40.61 g/d in women; for average GI were 56.53 and 64.58 units/d in men and 55.88 and 62.95 units/d in women;
for average GL were 65.57 and 99.67 units/d in men and 76.34 and 87.55units/d in women.
b
OR, odds ratio; 95%CI, 95% confidence interval; OR: adjusted for age (as a continuous variable), sex (male/female), duration of type 2 diabetes (as a continuous
variable), BMI (as a continuous variable), oral hypoglycemic drug use (yes/no), insulin use (yes/no) and energy intake (as a continuous variable).
doi:10.1371/journal.pone.0046552.t004

Acknowledgments

Author Contributions

The authors are grateful to the study participants and research staff from
Community Health Centers in Pudong New Area of Shanghai, China.

Conceived and designed the experiments: XR WX. Performed the


experiments: HQ YZ HZ HW LY. Analyzed the data: JJ ZZ WX.
Contributed reagents/materials/analysis tools: XR HQ HZ. Wrote the
paper: JJ WX. Revision of the manuscript: GZ QJ QS.

References
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Psyllium decreased serum glucose and glycosylated hemoglobin significantly in
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3. Hinata M, Ono M, Midorikawa S, Nakanishi K(2007). Metabolic improvement
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19. Ludwig DS(2002). The glycemic index: physiological mechanisms relating to


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20. Jenkins DJ, Kendall CW, Augustin LS, Franceschi S, Hamidi M, et al.(2002).
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21. Kim MS, Kim JY, Choi WH,Lee SS(2008). Effects of seaweed supplementation
on blood glucose concentration, lipid profile, and antioxidant enzyme activities
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22. Wolever TM, Gibbs AL, Mehling C, Chiasson JL, Connelly PW, et al.(2008)
The Canadian Trial of Carbohydrates in Diabetes (CCD), a 1-y controlled trial
of low-glycemic-index dietary carbohydrate in type 2 diabetes: no effect on
glycated hemoglobin but reduction in C-reactive protein. Am J Clin Nutr
87:114125.
23. Thomas DE, Elliott EJ(2010). The use of low-glycaemic index diets in diabetes
control. Br J Nutr 104:797802.
24. Brand-Miller J, Hayne S, Petocz P, Colagiuri S(2003). Low-glycemic index diets
in the management of diabetes: a meta-analysis of randomized controlled trials.
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25. Esposito K, Maiorino MI, Di Palo C, Giugliano D(2010). Dietary glycemic
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26. Franz MJ(2003). The glycemic index: not the most effective nutrition therapy
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27. Lau C, Faerch K, Glumer C, Tetens I, Pedersen O, et al.(2005) Dietary glycemic
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associated with lower incidence of type 2 diabetes in middle-aged women: the
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8. He M, van Dam RM, Rimm E, Hu FB,Qi L(2010). Whole-grain, cereal fiber,
bran, and germ intake and the risks of all-cause and cardiovascular diseasespecific mortality among women with type 2 diabetes mellitus. Circulation
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9. Zhou BF, Stamler J, Dennis B, Moag-Stahlberg A, Okuda N, et al.(2003)
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Beneficial effects of high dietary fiber intake in patients with type 2 diabetes
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reproducibility of the food frequency questionnaire used in the Shanghai
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16. Hessler DM, Fisher L, Mullan JT, Glasgow RE, Masharani U(2010). Patient
age: A neglected factor when considering disease management in adults with
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17. Roush G, Salonga A, Bajaj N(2011). A longitudinal study of sociodemographic
predictors of hemoglobin A1c. Conn Med 75:325328.
18. Khattab M, Khader YS, Al-Khawaldeh A, Ajlouni K(2010). Factors associated
with poor glycemic control among patients with type 2 diabetes. J Diabetes
Complications 24:8489.

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October 2012 | Volume 7 | Issue 10 | e46552

The New Eng land Jour nal of Medicine

BENEFICIAL EFFECTS OF HIGH DIETARY FIBER INTAKE IN PATIENTS


WITH TYPE 2 DIABETES MELLITUS
MANISHA CHANDALIA, M.D., ABHIMANYU GARG, M.D., DIETER LUTJOHANN, PH.D., KLAUS
SCOTT M. GRUNDY, M.D., PH.D., AND LINDA J. BRINKLEY, R.D.

ABSTRACT
Background The effect of increasing the intake of

dietary fiber on glycemic control in patients with type


2 diabetes mellitus is controversial.
Methods In a randomized, crossover study, we assigned 13 patients with type 2 diabetes mellitus to
follow two diets, each for six weeks: a diet containing
moderate amounts of fiber (total, 24 g; 8 g of soluble
fiber and 16 g of insoluble fiber), as recommended by
the American Diabetes Association (ADA), and a highfiber diet (total, 50 g; 25 g of soluble fiber and 25 g
of insoluble fiber) containing foods not fortified with
fiber (unfortified foods). Both diets, prepared in a research kitchen, had the same macronutrient and energy content. We compared the effects of the two diets
on glycemic control and plasma lipid concentrations.
Results Compliance with the diets was excellent.
During the sixth week of the high-fiber diet, as compared with the sixth week of the ADA diet, mean daily preprandial plasma glucose concentrations were 13
mg per deciliter (0.7 mmol per liter) lower (95 percent confidence interval, 1 to 24 mg per deciliter [0.1
to 1.3 mmol per liter]; P=0.04) and mean daily urinary glucose excretion was 1.3 g lower (median difference, 0.23 g; 95 percent confidence interval, 0.03
to 1.83; P=0.008). The high-fiber diet also lowered the
area under the curve for 24-hour plasma glucose and
insulin concentrations, which were measured every
two hours, by 10 percent (P=0.02) and 12 percent
(P=0.05), respectively. The high-fiber diet reduced
plasma total cholesterol concentrations by 6.7 percent (P=0.02), triglyceride concentrations by 10.2
percent (P=0.02), and very-low-density lipoprotein
cholesterol concentrations by 12.5 percent (P=0.01).
Conclusions A high intake of dietary fiber, particularly of the soluble type, above the level recommended by the ADA, improves glycemic control, decreases
hyperinsulinemia, and lowers plasma lipid concentrations in patients with type 2 diabetes. (N Engl J
Med 2000;342:1392-8.)
2000, Massachusetts Medical Society.

IETARY guidelines for patients with diabetes mellitus were revised by the American Diabetes Association (ADA) earlier
this year.1 The ADA recommends that the
composition of the diet be individualized on the basis
of a nutritional assessment and the outcomes desired.
Consistent with the previous recommendations of
the ADA,2 the new guidelines advise replacing satu1392

VON

BERGMANN, M.D.,

rated fat with carbohydrates. However, on the basis of


previous studies,3-10 an alternative approach of replacing saturated fat with cis monounsaturated fat was
also included in the recommendations.1 This new approach is further supported by epidemiologic studies
that have shown the healthful effects of diets rich in cis
monounsaturated fat in Mediterranean countries.11,12
Another, less strongly emphasized aspect of Mediterranean diets is the high intake of fruits, vegetables,
and grains that are rich sources of dietary fiber.13,14
The ADA recommended a moderate increase in the
intake of dietary fiber to 20 to 35 g per day because
of the cholesterol-lowering effects of soluble fiber.
However, the effects of dietary fiber on glycemic control were considered inconsequential.1 Furthermore,
the expert panel of the ADA considered it difficult
to achieve a high dietary intake of soluble fiber without consuming foods or supplements fortified with
fiber.1 We therefore designed the present study to determine the effects on glycemic control and plasma
lipid concentrations of increasing the intake of dietary fiber in patients with type 2 diabetes exclusively
through the consumption of foods not fortified with
fiber (unfortified foods) to a level beyond that recommended by the ADA. In addition, we studied the
effects of such an intervention on the intestinal absorption of cholesterol and the fecal excretion of sterols in an attempt to uncover the mechanisms by which
a high-fiber diet lowers plasma cholesterol.
METHODS
Patients
We studied 12 men and 1 woman (9 non-Hispanic whites and
4 blacks) with type 2 diabetes at the general clinical research center
of the University of Texas Southwestern Medical Center at Dallas.
The protocol for the study was approved by the institutional review board of the medical center, and each patient gave written
informed consent. In all patients the onset of diabetes was insidious; the disease developed in most of the patients after 40 years
of age. Their mean (SD) age was 619 years (range, 45 to 70).
Their mean body weight was 93.512.7 kg, and the mean bodymass index (the weight in kilograms divided by the square of the
height in meters) was 32.33.9. Three patients were treated with
diet alone, and the other 10 patients were treated with 2.5 to 20

From the Department of Internal Medicine (M.C., A.G., S.M.G., L.J.B.)


and the Center for Human Nutrition (A.G., S.M.G.), University of Texas
Southwestern Medical Center, Dallas; the Department of Veterans Affairs
Medical Center, Dallas (M.C., A.G., S.M.G.); and the Department of Clinical Pharmacology, Rheinische Friedrich-Wilhelms-Universitt, Bonn, Germany (D.L., K.B.). Address reprint requests to Dr. Garg at the Center for
Human Nutrition, University of Texas Southwestern Medical Center, 5323
Harry Hines Blvd., Dallas, TX 75390.

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BE N E F IC IAL EF F EC T S O F H IGH D IETA RY FI BE R I N TA K E I N PATI EN T S WI TH T YP E 2 D I A BETE S MEL LI TU S

mg of glyburide daily in addition to diet. The dose of glyburide


was not changed during the study.
On entry into the study, the patients plasma cholesterol and triglyceride concentrations after an overnight fast ranged from 151
to 324 mg per deciliter (3.90 to 8.38 mmol per liter) and 67 to
390 mg per deciliter (0.76 to 4.40 mmol per liter), respectively,
and their fasting plasma glucose concentrations were less than
200 mg per deciliter (11.1 mmol per liter). Their glycosylated hemoglobin values ranged from 6.0 to 9.8 percent. Two patients
had a history of coronary heart disease, but none had recently had
a myocardial infarction, unstable angina pectoris, or congestive
heart failure. Also, none had thyroid, renal, or hepatic disease. None
of the patients were receiving lipid-lowering therapy.

TABLE 1. COMPOSITION

Diets
The composition of the study diets is shown in Table 1. The
composition of the diets was calculated by means of a software
program based on the Department of Agriculture Handbook Series 8 (Nutriplanner, Practocare, San Diego, Calif.).15 The content
of total as well as soluble and insoluble dietary fiber was estimated
according to the data provided in the CRC Handbook of Dietary
Fiber in Human Nutrition.16 Both diets consisted of unfortified
foods. The patients were allowed some choices of food items.
Both diets provided 15 percent of the total energy as protein, 55
percent as carbohydrate, and 30 percent as fat; saturated, cis monounsaturated, and polyunsaturated fats accounted for 7 percent, 17
percent, and 6 percent of the total energy, respectively.
The high-fiber diet provided 50 g of total fiber per day; soluble
and insoluble fiber content provided 25 g each. The ADA diet
contained 24 g of total fiber per day, with 8 g as soluble fiber and
16 g as insoluble fiber. Unfortified foods, particularly those rich

STUDY DIETS.

ADA
DIET*

CONSTITUENT

Carbohydrate (% of total energy)


Protein (% of total energy)
Fat (% of total energy)
Saturated
Cis monounsaturated
Polyunsaturated
Cholesterol (mg/day)
Fiber (g/day)
Total
Soluble
Insoluble

Design of the Study


All the patients were first admitted to the general clinical research center for five days (the base-line period), during which a
detailed history was taken, a physical examination was performed,
and laboratory tests were performed. After the base-line period, all
the patients received both the ADA diet and the high-fiber diet,
each diet for a period of six weeks. Six patients received the highfiber diet first, and the other seven received the ADA diet first.
There was a median interval of seven days between the two study
periods, during which the patients were instructed to consume an
isocaloric diet. During the last week of each dietary period (days
36 to 42), the patients were hospitalized for evaluation.
On weekdays, all the patients ate at least one meal (breakfast,
lunch, or dinner) at the general clinical research center. Other meals
were supplied in packages so that they could be consumed at home.
The dietitian monitored compliance by interviewing the patients.
The patients were instructed to bring back any unconsumed food
and to maintain a constant level of physical activity throughout the
study.
Blood for lipid analyses was drawn, after an overnight fast, daily
for two days before the institution of the study diet and daily on
days 38 through 42 during both dietary periods. Plasma glucose
was measured at 7 and 11 a.m. and at 4 and 8 p.m. each day during the base-line period and on days 38 through 42 of both dietary periods. Glycosylated hemoglobin was measured during the
base-line period and at the end of each dietary period. On the
last day of each dietary period, blood samples were obtained every two hours for measurements of plasma glucose and insulin.
On days 38 through 42, patients collected 24-hour urine specimens for quantitative determination of glucose.
To permit us to determine fecal sterol balance and the percentage
of cholesterol absorption, each patient took a capsule containing
30 mg of sitostanol, 3 mg of [26,26,26,27,27,27-2H6]-cholesterol,
and 3 mg of [5,6,22,23-2H4]-sitostanol (Medical Isotopes, Pelham,
N.H.) three times a day on days 36 through 42. Fecal samples
were collected on day 35 or 36 and on the last three days of each
dietary period. Fecal samples were frozen within 12 hours after
collection and were pooled for analysis of small aliquots.

OF THE

HIGH-FIBER
DIET

55
15
30
7
17
6
300

55
15
30
7
17
6
297

24
8
16

50
25
25

*ADA denotes American Diabetes Association.

TABLE 2. SAMPLE MENUS

OF THE

ADA DIET
FOOD

STUDY DIETS.*
HIGH-FIBER DIET

WEIGHT

FOOD

WEIGHT

grams

grams

Breakfast
Orange juice
White grits
Egg substitute
Olive oil
Decaffeinated coffee

220
50
40
10
2

Orange sections
Oatmeal
Scrambled egg
Olive oil
Decaffeinated coffee

300
50
37
10
2

Lunch
Ham (5% fat)
Mayonnaise
Iceberg lettuce
Fresh tomato
Low-sodium bread
Corn (canned)
Cider vinegar
Dehydrated onion
Olive oil
Fresh green pepper
Fresh celery
Fruit cocktail (canned)
Instant tea
Oatmeal raisin cookie

50
6
15
30
60
140
5
2
10
10
15
105
2
20

Ham (5% fat)


Mayonnaise
Iceberg lettuce
Fresh tomato
Whole-wheat bread
Corn (canned)
Green peas (canned)
Dehydrated onion
Olive oil
Fresh green pepper
Fresh celery
Fresh papaya
Instant tea

52
12
10
15
60
40
110
2
10
10
15
250
2

Dinner
Chicken breast (skinned)
Bran flakes
Low-sodium bread
Parmesan cheese
Whole egg
Tomato (canned)
Low-fat cheese
Spaghetti
Green beans
Olive oil
Whole-wheat bread
Graham crackers
Instant tea

90
10
20
1
1
120
11
45
75
17
21
21
2

Chicken breast (skinned)


Bran flakes
Oat bran
Parmesan cheese
Egg substitute
Tomato (canned)
Low-fat cheese
Spaghetti
Zucchini
Olive oil
Whole-wheat bread
Fresh peaches
Instant tea

90
10
5
1
10
105
19
19
195
19
30
300
2

Bedtime snack
Mozzarella cheese
Low-sodium bread
Pineapple juice

30
30
190

Fruit cocktail (canned)


Cherries (canned)
Granola

200
100
15

*Each menu provided 2308 kcal per day. ADA denotes American Diabetes Association.

Volume 342
The New England Journal of Medicine
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Numb er 19

1393

The New Eng land Jour nal of Medicine

in soluble fiber, such as cantaloupe, grapefruit, orange, papaya, raisins, lima beans, okra, sweet potato, winter squash, zucchini, granola, oat bran, and oatmeal, were used to achieve high-fiber intake.
No fiber supplements were used. Sample menus of both the study
diets are shown in Table 2. The individual foods were weighed
daily during meal preparation in the research kitchen of the general clinical research center.
Biochemical Analyses
Fasting plasma total cholesterol, lipoprotein cholesterol, and triglycerides were measured according to the procedures of the Lipid Research Clinics.17 Cholesterol and triglycerides were measured
enzymatically with the use of kits (Boehringer Mannheim, Indianapolis). Very-low-density lipoproteins (VLDLs) (density, less
than 1.006 g per milliliter) were removed by ultracentrifugation,
and cholesterol was measured in the VLDL fraction and the infranatant. High-density-lipoprotein (HDL) cholesterol was measured enzymatically after lipoproteins containing apolipoprotein B
had been precipitated with heparinmanganese. Cholesterol in
the low-density lipoprotein (LDL) fraction was estimated to be
the difference between the cholesterol content of the infranatant
and that of the HDL fraction.
Plasma and urinary glucose were measured by the glucose oxidase method (Beckman Glucose Analyzer, Beckman Instruments,
Fullerton, Calif.). Glycosylated hemoglobin was measured with
ion-exchange high-performance liquid chromatography (Bio-Rad
Laboratories, Hercules, Calif.). Plasma insulin was measured by
radioimmunoassay.18,19
Pooled fecal samples collected within the last week of each dietary period were prepared for analysis of neutral and acidic fecal
sterols as described previously.20 Gasliquid chromatography of
neutral and acidic fecal sterols was performed on a gas chromatograph (model HP5890, HewlettPackard, Palo Alto, Calif.)
equipped with an automatic sample injector. Cholesterol absorption was measured during the same period from fecal samples by
gasliquid chromatography and mass spectrometry. 21
Statistical Analysis
To compare the two study periods and to assess the effect of
the sequence in which the patients received the high-fiber and

ADA diets, we used repeated-measures analysis of variance. 22 For


skewed data, we used the Wilcoxon signed-rank test to compare
the two dietary periods.23

RESULTS

The compliance with both the study diets was excellent, according to interviews with the patients and
estimates of the energy content of any leftover foods.
Three patients reported consuming extra food on
one day during the study, two while eating the highfiber diet and one the ADA diet. The patients commented about the larger quantities of food in the
high-fiber diet, but they consumed all the food given to them. The results are presented irrespective of
the order of the diets, because the sequence of the
diets had no effect on the results.
During the last week of each study period, the patients in both groups had similar daily energy intakes
and body weights and received a similar dose of glyburide (Table 3). The mean plasma glucose concentration was lower (by 13 mg per deciliter [0.7 mmol
per liter], or 8.9 percent) when patients completed
the high-fiber diet than when they completed the
ADA diet (P=0.04), and mean daily urinary glucose
excretion was 1.3 g lower (P=0.008). Daily plasma
glucose concentrations were 10 percent lower with
the high-fiber diet than with the ADA diet (values
for the area under the curve, 3743944 vs. 3365
1003 mghour per deciliter [207.852.4 vs. 186.8
55.7 mmolhour per liter]; P=0.02), and plasma insulin concentrations were 12 percent lower (values
for the area under the curve, 1107650 vs. 971
491 Uhour per milliliter [66423900 vs. 5826
2946 pmolhour per liter]; P=0.05) (Fig. 1). Gly-

TABLE 3. METABOLIC VARIABLES DURING THE LAST WEEK


(DAYS 38 THROUGH 42).*

VARIABLE

ADA DIET

Energy intake (kcal/day)


Weight (kg)
Dose of glyburide (mg/day)
Plasma glucose (mg/deciliter)
Urinary glucose (g/day)
Mean
Median
Glycosylated hemoglobin (%)

2308236
90.713.3
10.08.7
14236
2.34.3
0.76
7.21.3

HIGH-FIBER
DIET

OF THE

STUDY PERIODS

DIFFERENCE BETWEEN
DIETS (95% CI)

2308236

90.512.7 0.2 (1.1 to 0.6)


10.08.7

13038
13 (24 to 1)
1.01.9
0.0
6.91.2

0.23 (1.83 to 0.03)


0.3 (0.6 to 0.1)

P VALUE

1.00
0.60
1.00
0.04

0.008
0.09

*Plusminus values are means SD. ADA denotes American Diabetes Association, and CI confidence interval.
An analysis of variance was used to compare the two diets, except for urinary glucose, for which
the Wilcoxon signed-rank test was used.
The values are averages of plasma glucose concentrations measured at 7 and 11 a.m. and at 4 and
8 p.m. each day for five days during hospitalization. To convert values for plasma glucose to millimoles per liter, multiply by 0.056.
The values are averages of five daily urine collections during hospitalization.

1394

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The New England Journal of Medicine
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BE N E F IC IAL EF F EC T S O F H IGH D IETARY FI BE R I N TA K E I N PATI EN T S WI TH T YP E 2 D I A BETE S MEL LI TU S

Plasma Glucose (mg/dl)

240

P<0.05

200

P<0.05
P<0.05

180
160
140

ADA diet
High-fiber diet

120
100

a.
m
.
9
a.
m
.
11
a.
m
.
1
p.
m
.
3
p.
m
.
5
p.
m
.
7
p.
m
.
9
p.
m
.
11
p.
m
.
1
a.
m
.
3
a.
m
.
5
a.
m
.
7
a.
m
.

220

Plasma Insulin (mU/ml)

100
80
60
40

ADA diet

20
High-fiber diet

a.
m
.
9
a.
m
.
11
a.
m
.
1
p.
m
.
3
p.
m
.
5
p.
m
.
7
p.
m
.
9
p.
m
.
11
p.
m
.
1
a.
m
.
3
a.
m
.
5
a.
m
.
7
a.
m
.

Time
Figure 1. Mean (SE) 24-Hour Profile of Plasma Glucose Concentrations (Panel A) and Insulin Concentrations (Panel B) during the Last Day of the American Diabetes Association (ADA) Diet and the Last
Day of the High-Fiber Diet in 13 Patients with Type 2 Diabetes Mellitus.
The arrows indicate the times at which the main meals and a snack were consumed during the day.
To convert values for glucose to millimoles per liter, multiply by 0.056. To convert values for insulin to
picomoles per liter, multiply by 6.

cosylated hemoglobin values were slightly lower after the high-fiber diet (P=0.09).
As compared with the ADA diet, the high-fiber
diet resulted in a lower fasting plasma total cholesterol concentration (by 6.7 percent, P=0.02), a lower
plasma triglyceride concentration (by 10.2 percent,
P=0.02), and a lower plasma VLDL cholesterol concentration (by 12.5 percent, P=0.01) (Table 4). The
fasting plasma LDL cholesterol concentration was
6.3 percent lower with the high-fiber diet (P=0.11).
There were no significant differences between the

two diets in terms of the fasting plasma HDL cholesterol concentration.


As compared with the ADA diet, the high-fiber
diet decreased gastrointestinal absorption of cholesterol by 10 percent (48.59.6 vs. 43.77.4 percent;
95 percent confidence interval for the decrease, 0.6
to 9.0 percent; P=0.03) and increased fecal acidic
sterol excretion by 41 percent (895301 vs. 1258
458 mg per day; 95 percent confidence interval for
the increase, 137 to 589 mg per day; P=0.005), but
did not significantly affect the excretion of neutral
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TABLE 4. FASTING PLASMA LIPID AND LIPOPROTEIN


CONCENTRATIONS DURING THE LAST WEEK
OF THE STUDY PERIODS (DAYS 38 THROUGH 42).*
ADA
DIET

VARIABLE

HIGHDIFFERENCE BETWEEN
P
FIBER DIET
DIETS (95% CI)
VALUE
mg/dl

Plasma
Plasma
Plasma
Plasma
Plasma

total cholesterol
triglycerides
VLDL cholesterol
LDL cholesterol
HDL cholesterol

21033 19631 14 (27 to 2)


20595 18476 21 (37 to 4)
4019 3516 5 (9 to 1)
14229 13329 9 (22 to 3)
297
284
1 (4 to 3)

0.02
0.02
0.01
0.11
0.80

*Plusminus values are means SD. To convert values for cholesterol


and triglycerides to millimoles per liter, multiply by 0.026 and 0.011, respectively. ADA denotes American Diabetes Association, CI confidence interval, VLDL very-low-density lipoprotein, LDL low-density lipoprotein,
and HDL high-density lipoprotein.
An analysis of variance was used to compare the two diets.

sterols (1052375 vs. 1122565 mg per day; 95


percent confidence interval for the difference, 194
to 334 mg per day; P=0.60).
DISCUSSION

The intake of dietary fiber among people living in


Western countries remains low, and according to the
Third National Health and Nutrition Examination
Survey (NHANES), it averages 17 g per day in the
United States.24 Although patients with diabetes are
advised to increase their intake of dietary fiber, in
the NHANES study, their average daily intake was
found to be only 16 g.24 Why the intake of dietary
fiber in patients with diabetes remains low despite
its well-documented effect of lowering plasma cholesterol concentrations remains unexplained. It is
possible that the controversy about whether there
are beneficial effects of dietary fiber on glycemic control reduces the enthusiasm of physicians and dietitians for recommending high-fiber diets. The main
purpose of our study was to investigate the effects
on glycemic control of increasing the intake of dietary fiber. To avoid the confounding effects of concomitant changes in energy and macronutrients, the
two study diets were isocaloric and the macronutrient composition of the diets was identical. Furthermore, unfortified foods were used as the source of
dietary fiber.
Most important, we found that the high-fiber diet
improved glycemic control, as evidenced by decreases
in the mean daily preprandial and 24-hour plasma
glucose concentrations. Urinary glucose excretion
was also lowered by the high-fiber diet. The highfiber diet lowered glycosylated hemoglobin values
slightly but not significantly. The high-fiber diet also
lowered 24-hour plasma insulin concentrations.
1396

The results of previous studies that evaluated the


role of dietary fiber on glycemic control in patients
with type 2 diabetes were inconsistent. In some of the
studies, the lack of control for concomitant changes
in the intake of macronutrients makes the data difficult to interpret. For example, in the study by Kiehm
et al.25 and in that by Simpson et al.,26 the high-fiber
diet had a lower fat and higher carbohydrate content
than the low-fiber diet. In other studies, the interpretation of the results was confounded by the short
duration of the dietary intervention,27-29 the lack of
random assignment of the sequence of the high-fiber
and low-fiber diets,27,29 and unexplained weight loss
during the high-fiber diet.29
Only a few well-controlled studies have evaluated
the glycemic effects of increasing the intake of dietary fiber with the use of either preparations of refined concentrated fiber or unfortified food, and the
results have been inconsistent.1,30 For example, diets
that included 15 to 21 g of guar-gum fiber or oat-bran
concentrate per day had no effect on glycemic control31,32 or resulted in only a slight improvement.33,34
In randomized, crossover trials of six weeks duration
in which the intake of dietary fiber was increased by
16 g per 1000 kcal through the consumption of
foods prepared in a research kitchen or by 14 g per
day through dietary instruction, there was no improvement in glycemic control.35,36 In contrast, increasing dietary fiber by 23 g for three weeks and by
30 g for six weeks resulted in decreased fasting and
postprandial plasma glucose concentrations.37,38 We
found that an increase in the intake of total dietary
fiber, which consisted predominantly of soluble fiber, significantly improved glycemic control and decreased the degree of hyperinsulinemia in patients
with type 2 diabetes.
Our study also demonstrates the feasibility of
achieving a high intake of dietary soluble fiber by consuming unfortified foods. Our patients accepted the
high-fiber diet well and had few side effects; therefore, we recommend that patients with diabetes be
encouraged to use unfortified foods instead of less
palatable purified-fiber preparations and supplements
to increase their intake of dietary fiber.
The mechanisms of the improved glycemic control associated with high fiber intake remain undefined. Whether this effect is due to an increase in
soluble fiber, insoluble fiber, or both is unclear. Besides causing increased fecal excretion of bile acids,
dietary fiber may cause malabsorption of fat.39 However, in our study, the patients weight did not change
with the high-fiber diet, which suggests that the degree of reduction in the absorption of fat was insignificant. Another possibility is that dietary fiber improves glycemic control by reducing or delaying the
absorption of carbohydrates.
As expected, the high-fiber diet reduced plasma
total cholesterol concentrations by 6.7 percent, a

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BE N E F IC IAL EF F EC TS O F H IGH D IETARY FI BE R I N TA K E I N PATI EN T S WI TH T YP E 2 D I A BETE S MEL LI TU S

finding consistent with the results of previous reports


of the cholesterol-reducing effects of soluble but not
insoluble fiber.40,41 Therefore, the lowering of cholesterol can be attributed primarily to an average increase of 17 g in the intake of soluble fiber. Previous
studies in normal subjects have reported no effects
of the amount of dietary fiber on plasma triglyceride
concentrations.42 In our study, the decrease in plasma triglyceride and VLDL cholesterol concentrations
during the high-fiber diet could have been due to
the improvement in glycemic control.
The mechanisms of the reduction in plasma cholesterol concentrations induced by the increased dietary fiber intake are controversial, however. The increase in bile-acid excretion probably explains most of
the reduction, and the reduction in cholesterol absorption may also have contributed to this finding.
Previous studies have also reported a variable increase
in bile-acid excretion resulting from the consumption of pectin,39,43 oat bran,44,45 bagasse,46 and diets
with a mixture of soluble fiber and insoluble fiber,47
but not psyllium.48 In contrast, Kesaniemi et al.47 reported that a high-fiber diet did not change cholesterol absorption in normal subjects. However, the
high-fiber diet they used included 26 g of fiber, and
it did not lower plasma cholesterol concentrations.47
In conclusion, an increase in the intake of dietary
fiber, predominantly of the soluble type, by patients
with type 2 diabetes mellitus improved glycemic control and decreased hyperinsulinemia in addition to
the expected lowering of plasma lipid concentrations.
Therefore, dietary guidelines for patients with diabetes should emphasize an overall increase in dietary fiber through the consumption of unfortified foods,
rather than the use of fiber supplements.
Supported in part by grants (M01-RR00633 and HL-29252) from the
National Institutes of Health and by research grants from the Bundesministerium fr Bildung, Forschung, Wissenschaft und Technologie (01EC9402)
and the Deutsche Forschungsgemeinschaft (BE 1673/1-1).

We are indebted to Angela Osborn, Travis Petricek, and the nursing and dietetic service of the General Clinical Research Center of
the University of Texas Southwestern Medical Center, Dallas, for
their excellent technical support and to Beverley Adams-Huet, M.S.,
for statistical analysis.

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14. Kromhout D, Keys A, Aravanis C, et al. Food consumption patterns
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foods. In: Spiller GA, ed. CRC handbook of dietary fiber in human nutrition. 2nd ed. Boca Raton, Fla.: CRC Press, 1993:567-93.
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clinics program: lipid and lipoprotein analysis. 2nd ed. Washington, D.C.:
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18. Herbert V, Lau KS, Gottlieb CW, Bleicher SJ. Coated charcoal immunoassay of insulin. J Clin Endocrinol Metab 1965;25:1375-84.
19. Yalow RS, Berson SA. Immunoassay of endogenous plasma insulin in
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20. Czubayko F, Beumers B, Lammsfuss S, Lutjohann D, von Bergmann
K. A simplified micro-method for quantification of fecal excretion of neutral and acidic sterols for outpatient studies in humans. J Lipid Res 1991;
32:1861-7.
21. Lutjohann D, Meese CO, Crouse JR III, von Bergmann K. Evaluation
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cholesterol absorption in humans. J Lipid Res 1993;34:1039-46.
22. Jones B, Kenward MG. Design and analysis of crossover trials. London: Chapman & Hall, 1989.
23. Conover WJ. Practical nonparametric statistics. 2nd ed. New York:
John Wiley, 1980:288-92.
24. National Health and Nutrition Examination Survey III, 1988-94.
NCHS CD-ROM series 11. No. 2A. ASCII version. Hyattsville, Md.: National Center for Health Statistics, April 1998.
25. Kiehm TG, Anderson JW, Ward K. Beneficial effects of a high carbohydrate, high fiber diet on hyperglycemic diabetic men. Am J Clin Nutr
1976;29:895-9.
26. Simpson HCR, Simpson RW, Lousley S, et al. A high carbohydrate
leguminous fibre diet improves all aspects of diabetic control. Lancet 1981;
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27. Rivellese A, Riccardi G, Giacco A, et al. Effect of dietary fibre on glucose control and serum lipoproteins in diabetic patients. Lancet 1980;2:
447-50.
28. Riccardi G, Rivellese A, Pacioni D, Genovese S, Mastranzo P, Mancini
M. Separate influence of dietary carbohydrate and fibre on the metabolic
control in diabetes. Diabetologia 1984;26:116-21.
29. ODea K, Traianedes K, Ireland P, et al. The effects of diet differing
in fat, carbohydrate, and fiber on carbohydrate and lipid metabolism in
type II diabetes. J Am Diet Assoc 1989;89:1076-86.
30. Nuttall FQ. Dietary fiber in the management of diabetes. Diabetes
1993;42:503-8.
31. Holman RR, Steemson J, Darling P, Turner RC. No glycemic benefit
from guar administration in NIDDM. Diabetes Care 1987;10:68-71.
32. Uusitupa M, Siitonen O, Savolainen K, Silvasti M, Penttila I, Parviainen M. Metabolic and nutritional effects of long-term use of guar gum
in the treatment of noninsulin-dependent diabetes of poor metabolic control. Am J Clin Nutr 1989;49:345-51.
33. Aro A, Uusitupa M, Voutilainen E, Hersio K, Korhonen T, Siitonen
O. Improved diabetic control and hypocholesterolaemic effect induced by
long-term dietary supplementation with guar gum in type 2 (insulin-independent) diabetes. Diabetologia 1981;21:29-33.
34. Pick ME, Hawrysh ZJ, Gee MI, Toth E, Garg ML, Hardin RT. Oat

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bran concentrate bread products improve long-term control of diabetes: a


pilot study. J Am Diet Assoc 1996;96:1254-61.
35. Hollenbeck CB, Coulston AM, Reaven GM. To what extent does increased dietary fiber improve glucose and lipid metabolism in patients with
noninsulin-dependent diabetes mellitus (NIDDM)? Am J Clin Nutr 1986;
43:16-24.
36. Manhire A, Henry CL, Hartog M, Heaton KW. Unrefined carbohydrate and dietary fibre in treatment of diabetes mellitus. J Hum Nutr 1981;
35:99-101.
37. Karlstrom B, Vessby B, Asp NG, et al. Effects of an increased content
of cereal fibre in the diet of type 2 (non-insulin-dependent) diabetic patients. Diabetologia 1984;26:272-7.
38. Hagander B, Asp NG, Efendic S, Nilsson-Ehle P, Schersten B. Dietary
fiber decreases fasting blood glucose levels and plasma LDL concentration
in noninsulin-dependent diabetes mellitus patients. Am J Clin Nutr 1988;
47:852-8.
39. Kay RM, Truswell AS. Effect of citrus pectin on blood lipids and fecal
steroid excretion in man. Am J Clin Nutr 1977;30:171-5.
40. Jenkins DJ, Newton C, Leeds AR, Cummings JH. Effect of pectin,
guar gum, and wheat fibre on serum-cholesterol. Lancet 1975;1:1116-7.
41. Hillman LC, Peters SG, Fisher CA, Pomare EW. The effects of the fi-

ber components pectin, cellulose and lignin on serum cholesterol levels.


Am J Clin Nutr 1985;42:207-13.
42. Brown L, Rosner B, Willett WW, Sacks FM. Cholesterol-lowering effects of dietary fiber: a meta-analysis. Am J Clin Nutr 1999;69:30-42.
43. Cummings JH, Southgate DAT, Branch WJ, et al. The digestion of
pectin in the human gut and its effect on calcium absorption and large
bowel function. Br J Nutr 1979;41:477-85.
44. Kirby RW, Anderson JW, Sieling B, et al. Oat-bran intake selectively
lowers serum low-density lipoprotein cholesterol concentrations of hypercholesterolemic men. Am J Clin Nutr 1981;34:824-9.
45. Zhang JX, Hallmans G, Andersson H, et al. Effect of oat bran on plasma cholesterol and bile acid excretion in nine subjects with ileostomies. Am
J Clin Nutr 1992;56:99-105.
46. Walters RL, Baird IM, Davies PS, et al. Effects of two types of dietary
fibre on faecal steroid and lipid excretion. BMJ 1975;2:536-8.
47. Kesaniemi YA, Tarpila S, Miettinen TA. Low vs high dietary fiber and
serum, biliary, and fecal lipids in middle-aged men. Am J Clin Nutr 1990;
51:1007-12.
48. Abraham ZD, Mehta T. Three-week psyllium-husk supplementation:
effect on plasma cholesterol concentrations, fecal steroid excretion, and
carbohydrate absorption in men. Am J Clin Nutr 1988;47:67-74.

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Hindawi Publishing Corporation


Journal of Diabetes Research
Volume 2016, Article ID 2980406, 9 pages
http://dx.doi.org/10.1155/2016/2980406

Research Article
Fiber in Diet Is Associated with Improvement of
Glycated Hemoglobin and Lipid Profile in Mexican
Patients with Type 2 Diabetes
Lubia Velzquez-Lpez,1 Abril Violeta Muoz-Torres,2 Carmen Garca-Pea,3
Mardia Lpez-Alarcn,4 Sergio Islas-Andrade,5 and Jorge Escobedo-de la Pea1
1

Unidad de Investigacion en Epidemiologa Clnica, Hospital Carlos MacGregor Sanchez Navarro, Instituto Mexicano del Seguro
Social, Avenida Gabriel Mancera No. 222, Colonia del Valle, Delegacion Benito Juarez, 03100 Ciudad de Mexico, Mexico
2
Departamento de Salud Publica, Facultad de Medicina, Universidad Nacional Autonoma de Mexico, 6 Piso, Edificio B,
Circuito Interior, Ciudad Universitaria, Avenida Universidad 3000, Ciudad de Mexico, Mexico
3
Departamento de Investigacion, Instituto Nacional de Geriatra, Periferico sur No. 2767, Colonia San Jeronimo Ldice,
Delegacion Magdalena Contreras, 10200 Ciudad de Mexico, Mexico
4
Unidad de Investigacion Medica en Nutricion, Hospital de Pediatra, Centro Medico Nacional Siglo XXI, Instituto Mexicano del
Seguro Social, Avenida Cuauhtemoc 300, Colonia Doctores, Delegacion Cuauhtemoc, 06720 Ciudad de Mexico, Mexico
5
Unidad de Investigacion Cientfica de Endocrinologa, Diabetes y Metabolismo, y de Enfermedades Metabolicas,
Centro Medico Nacional Siglo XXI, Instituto Mexicano del Seguro Social, Avenida Cuauhtemoc 300, Colonia Doctores,
Delegacion Cuauhtemoc, 06720 Ciudad de Mexico, Mexico
Correspondence should be addressed to Jorge Escobedo-de la Pena; jorgeep@unam.mx
Received 22 November 2015; Revised 26 February 2016; Accepted 21 March 2016
Academic Editor: Giovanni Annuzzi
Copyright 2016 Lubia Velazquez-Lopez et al. This is an open access article distributed under the Creative Commons Attribution
License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly
cited.
Objective. To assess the association of dietary fiber on current everyday diet and other dietary components with glycated hemoglobin
levels (HbA1c), glucose, lipids profile, and body weight body weight, in patients with type 2 diabetes. Methods. A cross-sectional
survey of 395 patients with type 2 diabetes was performed. HbA1c, fasting glucose, triglycerides, and lipids profile were measured.
Weight, waist circumference, blood pressure, and body composition were measured. Everyday diet with a semiquantitative food
frequency questionnaire was evaluated. ANOVA, Kruskal-Wallis, chi-square tests and multivariate logistic regression were used
in statistical analysis. Results. Higher fiber intake was associated with a low HbA1c, high HDL-c levels, low weight, and waist
circumference. The highest tertile of calories consumption was associated with a higher fasting glucose level and weight. The highest
tertile of carbohydrate consumption was associated with a lower weight. The lowest tertile of total fat and saturated fat was associated
with the highest tertile of HDL-c levels, and lower saturated fat intake was associated with lower weight ( < 0.05). Conclusions. A
higher content of fiber in the diet reduces HbA1c and triglycerides, while improving HDL-c levels. Increasing fiber consumption
while lowering calorie consumption seems to be an appropriate strategy to reduce body weight and promote blood glucose control.

1. Introduction
Increased fiber in the diet is associated with a reduction of
glycated hemoglobin (HbA1c), improved lipid profile, and
loss of body weight in type 2 diabetes patients. It has been
proposed that appropriate consumption of fruit in the diet
may be an adequate strategy to reduce HbA1c, given the
fiber content, and prevent complications from diabetes [1, 2].

Several clinical trials have documented a positive effect of


dietary fiber, [3] and in cross-sectional studies this effect
has also been observed in different Asian populations [1, 4].
In fact, dietary fiber can reduce the incidence of stroke in
patients with type 2 diabetes [5].
There is evidence of the benefit of reduced calorie diets,
though the combination of this restriction with a diet higher
in protein to encourage weight loss and control glucose and

2
serum lipid levels continues to generate controversy [6]. It
has also been suggested that reducing the proportion of
carbohydrates in the diet at the cost of increasing protein
consumption improves HbA1c and blood pressure values
as well as weight loss and this, combined with physical
exercise, proffers greater protection [7]. The recommendation
to include fats in the diet continues to stir up controversy
regarding the effect of this on the lipids profile and body
weight; strategies include reducing to 30% or less the calorie
intake. Conversely, higher consumption has been suggested
though with a higher content of monounsaturated and
polyunsaturated fats [8].
Type 2 diabetes is one of the chronic diseases with
the highest economic and social impact, as well as in the
repercussions on the quality of life. In recent decades it has
reached epidemic proportions; lifestyle is a very important
factor in the prevention and control of the disease [9]. There is
evidence of the favorable effect of adequate glycemic control
to prevent micro- and macrovascular complications [10].
In the treatment regime, diet adaptation is a basic element
to achieve and maintain control goals [11]. Even while diet
plays a substantial role, only a minority of patients receive
nutriment therapy, and an even smaller number undergo the
needed changes in diet as part of their disease management
[12].
Fiber consumption used to be high in the Mexican
population; however, it has been reduced due to changes in
eating habits [13] which undoubtedly affects habitual diet in
subjects with diabetes. While there is limited information on
the description of current everyday diet in patients with type
2 diabetes and its effect on major cardiovascular risk factors,
the role of macronutrients on metabolic control indicators
continues to foster controversy [14]. Given the foregoing,
the objective of this study was to assess the association
of habitual dietary fiber and other dietary components on
HbA1c, glucose, and lipid profile levels, as well as body
weight, in type 2 diabetes patients in Mexico.

2. Methods
This report corresponds to the baseline evaluation of type
2 diabetes patients that were included in a multicenter,
randomized clinical trial called Efficacy of Nutritional Therapy and Education through a Multimedia System for the
Metabolic Control of Type 2 Diabetes Patients (ClinicalTrials.gov identifier: NCT02441023). Patients came from four
different primary care clinics (family medical units belonging
to the Mexican Social Security Institute) in Mexico City, with
a previous diagnosis of diabetes, with age younger than 70
years, and with no advanced microvascular complication.
An ethics and research committee approved the protocol.
Patients were invited to participate at their local clinics and
incorporated into the study once they had signed the letter of
informed consent.
The patients included in the study underwent an extensive
medical history questionnaire as well as a physical examination to evaluate the presence of severe complications.
Hypertension was diagnosed when the patient stated being

Journal of Diabetes Research


on antihypertensive medication or for those with values
140/90 mmHg at the time of joining the study. Blood pressure was taken twice with a mercury sphygmomanometer at
an interval of 4 minutes between measurement and after the
patient had been seated for more than 5 minutes. The mean
of the two values was used. Physical activity was considered
when the patient had at least 150 min/week of moderateintensity aerobic physical activity, for at least 3 days/week with
no more than 2 consecutive days without exercise [15].
2.1. Variables Measured. Twelve-hour-fasting blood plasma,
glucose concentration, creatinine, triglycerides, total cholesterol, and fractions HDL-c values were measured; the LDLc was calculated through the Friedewald equation LDL-c =
[total cholesterol (triglycerides/5) HDL-c, for triglyceride
concentration < 400 mg/dL] [16]. HbA1c was determined
through the high-resolution liquid chromatography method.
Excretion of urinary albumin was analyzed in the first
morning urine sample through photometry/nephelometry to
determine the albumin-creatinine ratio.
Standardized nutritionists who employed the Habitch
method and the specifications recommended by Lohman
recorded anthropometry [17, 18]. Waist circumference was
measured after determining the midpoint between the last
rib and the upper edge of the iliac crest on the right side;
hip circumference was measured at the widest point of
the trochanters. Both of these measurements were taken
on three occasions, and the mean of the second and third
measurement was used for the purpose of analysis. The
percentage of fat was obtained through the bioimpedance
measurement of the lower segment, using a TANITA! body
composition analyzer, model TBF-215.
Diet was assessed with a food frequency questionnaire,
previously validated and currently used in the Mexican
National Health and Nutrition Surveys [19, 20]. The frequency with which 116 food items and 8 types of beverages
were consumed in the last year was measured. Frequency
was described as never in the last year or frequency of
consumption over a one-month, one-week, or one-day period
in the last year. Included on the list were dairy, eggs, meat
and cold cuts, fruit, vegetables, legumes and cereals, sweets,
drinks, and fats to prepare or dress foodstuffs.
In order to calculate the consumption of nutrients we
employed the software System to calculate nutritional vectors,
developed by the National Public Health Institute of Mexico
(INSP in Spanish). Dietary components analyzed were consumption of calories, proteins, carbohydrates, and lipids, as
well as fiber content, cholesterol, and sodium in the diet. The
consumption of nutriments was analyzed, with an adjustment
of the total calories using the residual method in order to
remove the effect of energy consumption of nutriments [21].
2.2. Statistical Analysis. For statistical analysis, frequency and
proportion measurements were calculated, as were the mean
and standard deviation to characterize the population in
sociodemographic variables, disease history, and proportion
of metabolic control.

Journal of Diabetes Research

Table 1: Sociodemographic characteristics and comorbidity in type


2 diabetes patients.
= 395
Age
Sex
Female
Male
Diagnosis of diabetes (years)
Diabetes treatment
No pharmacological treatment
Oral hypoglycemic agents
Oral hypoglycemic agents and insulin
Insulin
Lipid lowering medication
Follow a diet plan
Physical activity
Education in diabetes
Hypertension
Smoking
Alcohol consumption
Neuropathy
Peripheral
Autonomic
Kidney disease
Glomerular filtration rate <60 mL/min/1.73 m2
Microalbuminuria 30299 mg/g
Macroalbuminuria >300 mg/g

(%)
54.6 8.0
270 (68)
125 (32)
6 (311)
16 (4)
300 (76)
43 (11)
36 (9)
84 (21)
65 (16)
51 (13)
129 (33)
219 (55)
89 (22)
132 (33)
77 (20)
22 (6)
18 (5)
49 (12)
18 (5)

Data are presented as frequencies and percentage. Age is presented as


mean standard deviation. Years of diagnosis of diabetes are presented as
median and interquartile range.

A one-factor analysis of variance was performed to identify the association between the main dietary components
with metabolic control variables; the Kruskal-Wallis test was
used for glucose and triglyceride variables. The chi-square
test was used to identify the association between a balanced
diet and the various components of metabolic control.
A logistic regression multivariate analysis was performed
to identify the risk of HbA1c >7% if the dietary components
were inadequate. The model was adjusted with the variables
that could influence metabolic controls, such as the number
of years elapsed since the time of diagnosis, the type of treatment given, and diabetes education. Data were considered
statistically significant with a < 0.05. Statistical analysis was
done using the SPSS package, version 19.

3. Results
The average age of the study population was 54.6 8.0
years; oral hypoglycemic drugs were the most-used diabetes treatment (76%); a low proportion followed a diet
and physical activity (16% and 13%, resp.). Only 21% were
prescribed lowering lipid medication. Of the study group,
55% had hypertension, 26% had diabetic neuropathy, 12% had
microalbuminuria, and 5% had macroalbuminuria (Table 1).

Table 2 shows the metabolic control data and the dietary


characteristics of the patients. Only 34% had a desirable
HbA1c; total cholesterol was within control range for over
50% of the population, whereas triglycerides, LDL-c, and
HDL-c were found to be within normal range in only third
of the subjects. Body mass index (BMI) was adequate in only
12%; half of the population was obese and 37% of the population was overweight; over 70% of patients had an abnormal
waist circumference. Diastolic blood pressure rather than
systolic showed uncontrolled values (43%). Forty-five percent
consumed a diet with appropriate calorie content for their
current weight, and proteins are the dietary macronutrient
showing the highest degree of appropriate consumption,
while 48% of the study population was found to have an
appropriate fiber consumption.
Table 3 shows the association between the main dietary
components and the metabolic control indicators. There
is a noticeable positive association between high calorie
consumption and glucose levels, while lower consumption of
total and saturated fat was associated with higher levels of
HDL-c. A higher intake of fiber in the diet was significantly
linked to lower levels of HbA1c and triglycerides and HDL-c
improvement.
The association between the components of the diet and
the anthropometric indicators is presented in Table 4. A
greater consumption of calories in the diet was associated
with greater weight, whereas a higher consumption of total
carbohydrates produced a reverse association with weight
gain. Lower consumption of saturated fat is associated with
less weight, whereas a higher fiber intake is associated with
lower levels of weight and waist circumference.
In the multivariate analysis (Table 5), a lower intake of
dietary fiber (first quartile) was independently associated
with poor glycemic control, together with longer duration
of the disease and lack of education in diabetes. In a similar
model, the lowest tertile of fiber consumption increased the
risk of inadequately low HDL-c levels, as did the higher
the body weight, but the effects of duration of diabetes and
education in diabetes were lost (Table 6).

4. Discussion
In patients with type 2 diabetes, adherence to an appropriate
meal plan and physical activity are important components
in controlling the disease. Of the population assessed, only
16% of patients followed a diet as part of their treatment and
only 13% exercised. As for metabolic control, only 3 out of
10 patients had HbA1c <7%, a proportion similar to what is
reported in the National Health Survey of Mexico 2012, in
which only a small group adheres to diet and exercise regimes
as part of treatment, and only 24% have an adequate glycemic
control [22].
Regarding the characteristics of the diet, only 2 out of
10 patients have adequate consumption of whole simple
carbohydrates, only 16% consume adequate proportions of
fat, and only 8% have a proper balance in their daily diet,
even though 4 out of 10 patients are consuming a diet
conducive to attaining healthful body weight (1,200 to 1,600

Journal of Diabetes Research


Table 2: Metabolic control and diet characteristics of the studied population ( = 395).

Biochemical variables
HbA1c (%)

Mean SD or median (Interquartile


range)

Reference value

Adequate control
(%)

8.48 2.2

<7%

112.46 32.0

<100 mg/dL

70 (25.9)/41 (33)

0.71.3 mg/dL

387 (98)

136 (34)

Fasting glucose (mg/dL)

146 (117201)

70130 mg/dL

149 (38)

Total cholesterol (mg/dL)

195.90 41.1

<200 mg/dL

229 (58)

LDL-c (mg/dL)
HDL-c (mg/dL)
Triglycerides (mg/dL)
Creatinine (mg/dL)
Anthropometric variables and blood pressure (BP)
Weight (kg)
Body mass index (kg/m2 )

Waist circumference (cm)


Body fat (%)
Systolic BP (mmHg)
Diastolic BP (mmHg)

Diet variables
Total energy kcal/day1
Carbohydrates (g/day)/%
Soluble CHO g/day
Proteins g/day/%
Fats g/day/%
Dietary fiber g/1000 kcal
Saturated fats g/day/%
Fructose g/day
Cholesterol mg/day
Sodium mg/day
Balanced diet2

128 (32)

41.68 11.2

>50 F and >40 M mg/dL

75.42 14.8

47 (12)

100.48 12.4

18.524.9 kgm2

<80 (F) and <90 (M) cm

12 (4)/24 (19)

41.90 11.7

2030 (F) and 1220 (M) cm

5 (4)/12 (4)

83.25 11.1

130 mmHg

224 (57)

1792.25 683.2
225.65 93.6/50.3 7.8
59.00 (37.8770.81)/13.1 4.5
67.59 23.3/15.5 3.0
70.02 28.8/36.0 7.0
13.83 0.4
20.24 9.4/10.1 2.2
20 (1427)
195 (129252)
1492.57 594.0

80 mmHg

2030 kcal/kg/day
5055%
<10%
1015%
2530%
14 g/1000 Kcal
<7%
(20 g)/day
<200 mg
<2000 mg

179 (45)
97 (25)
97 (25)
188 (48)
64 (16)
188 (48)
28 (7)
195 (49)
212 (54)
269 (82)
30 (8)

180 (134251)
0.81 0.2

30.52 5.3

124.50 15.9

<150 mg/dL

134 (34)

324 (83)

1
Caloric recommendations for adults older than 51 years and sedentary behavior were considered, as well as a caloric reduction for subjects with diabetes,
obesity, or overweight; in normal weight, 30 kcal/kg/day was considered in reference value, in overweight, 25 kcal/kg/day, and, in obesity, 20 kcal/kg/day.
2
Balanced diet was considered when the proportion of carbohydrates was between 50 and 55%, proteins 1015%, and fats < 30% from total kcal value. F:
female. M: male.

calories), calories suggested if the individual is sedentary,


with overweight or obesity, and more than 50 years old.
Other authors have proven the association between obesity
and a diet high in calories, saturated fat, sodium, and a
lower content of fiber in type 2 diabetes patients [23]. The
results shown are consistent with the association between
higher calorie consumption and greater glycemic and weight
instability. A very small proportion of patients exhibit a
proper balance in diet; thus it is necessary to encourage them
to adhere to a more healthful alimentary regime.
An increased consumption of carbohydrates was linked
significantly to lower weight. No differences were found
regarding the consumption of carbohydrates and glucose or
HbA1c levels, similar to what has been observed by other
authors when comparing the effect of prescribing diets with

a greater or lesser carbohydrate content, on HbA1c levels and


body weight [24]. However, a review of clinical trials where
patients were followed up for more than six months confirms
the benefit of prescribing reduced carbohydrate diets, of low
glycemic index, Mediterranean diets, and diets with higher
protein content to improve cardiovascular risk markers in
patients with type 2 diabetes [25]. The jury is still out for a
real consensus regarding the distribution of macronutriments
in the diet of the diabetic patient. In fact, consensus reached
on the treatment of the disease suggests that diet should be
tailored and adjusted to the comorbidity of each patient [11].
The effect that the amount of carbohydrates in the diet has
on body weight and glycemic levels merits further evaluation
and monitoring. It is well known that one of the main health
problems linked to diabetes is obesity, reported to be as high

Journal of Diabetes Research

Tertiles
Calories (kcal)
8121440
14411922
19223420
value
Carbohydrates (g/day)
116.45211.36
211.37238.80
238.81298.50
value
Proteins (g/day)
40.7263.06
63.0770.36
70.3798.24
value
Fats (g/day)
12.9264.50
64.5174.77
74.78149.02
value
Saturated fats (g/day)
1.1818.20
18.2121.89
21.9054.28
value
Dietary fiber (g/day)
4.6321.65
21.6626.68
26.6978.38
value

Table 3: Association of diet components and metabolic control variables ( = 395).


HbA1c
%

Glucose
mg/dL

Triglycerides
mg/dL

HDL-c
mg/dL

LDL-c
mg/dL

8.40 2.1
8.35 2.3
8.70 2.3
0.400

140.0 (116.2, 189.7)


141.0 (112.2, 193.5)
157.0 (123.0, 224.0)
0.0130

181.0 (131.0, 252.0)


171.5 (135.2, 235.0)
182.0 (135.0, 267.0)
0.603

41.8 10.6
41.1 9.7
42.2 13.1
0.719

113.9 31.2
111.7 31.5
111.6 33.2
0.811

8.6 2.1
8.4 2.3
8.4 2.3
0.767

141.0 (116.5, 215.5)


145.0 (113.0, 200.0)
148.5 (119.0, 189.7)
0.882

186.0 (141.5, 251.5)


174.0 (130.5, 243.0)
168.5 (128.2, 247.0)
0.254

40.6 10.0
41.4 13.4
43.1 10.1
0.202

108.0 32.0
116.1 33.2
112.5 29.2
0.117

8.5 2.3
8.7 2.4
8.2 2.0
0.166

152.0 (121.5, 198.0)


151.0 (114.0, 211.5)
139.0 (113.0, 199.0)
0.196

168.0 (131.0, 255.5)


189.0 (138.7, 242.5)
179.0 (136.0, 252.0)
0.418

42.1 9.7
42.0 12.9
41.2 11.05
0.776

117.9 30.11
110.3 31.8
110.21 33.3
0.080

8.5 2.3
8.5 2.3
8.4 2.1
0.859

148.0 (119.0, 195.0)


152.0 (119.0, 203.0)
140.0 (111.0, 216.0)
0.627

174.0 (130.0, 257.0)


179.0 (137.0, 266.5)
182.0 (141.0, 235.0)
0.779

43.9 13.3
40.1 10.1
41.6 9.7
0.017

112.3 29.0
114.4 34.7
110.6 31.1
0.633

8.3 2.1
8.7 2.4
8.5 2.2
0.260

146.0 (115.0, 194.0)


145.0 (119.0, 205.0)
149.0 (116.0, 209.0)
0.968

165.0 (125.0, 236.0)


184.0 (141.0, 270.0)
183.0 (138.0, 238.0)
0.096

43.9 9.9
40.0 9.8
41.1 13.4
0.015

116.8 28.2
112.9 34.6
107.6 31.7
0.065

8.6 2.3
8.8 2.3
8.0 2.1
0.011

151.5 (119.5, 208.5)


152.0 (116.0, 221.0)
136.5 (114.0, 186.8)
0.203

183.0 (142.8, 251.8)


186.0 (133.0, 284.0)
163.0 (123.5, 221.0)
0.007

42.0 12.8
39.5 9.0
43.5 11.2
0.016

114.5 31.5
111.0 33.7
111.8 30.5
0.622

Data are presented as mean standard deviation or median (interquartile range), according to each tertile of diet components. Comparison was performed
with ANOVA (means) or Kruskal-Wallis (medians).

as 50% in this population, and obesity elevates the risk of


macrovascular disease. The habitual diet of patients is one of
the most important factors to reduce obesity. It is imperative
to design educational strategies geared toward improving
adherence to a healthful diet.
In this study, consumption of proteins was not associated
with improved glycemic control. Other authors have reported
the benefits of higher protein content in the diet for an
improvement of HbA1c and body weight, as well as some cardiovascular risk indicators [26]. Different theories regarding
the effect of a high protein diet have been described, including the benefit of producing greater satiety and reducing
consumption of carbohydrateswhich provide less energy
leading to weight loss. On the other hand, the higher thermal
effect of proteins versus carbohydrates fosters greater weight

loss and improved metabolic control in overweight or obese


patients [27].
As for fat in the diet, high consumption of saturated fat is
linked to higher risk of cardiovascular disease, obesity, and
dyslipidemia when compared to a higher consumption of
polyunsaturated fat. In our results, increased consumption
of saturated fat was linked to lower levels of HDL-c and
higher body weight. These results are consistent with the
broadly described benefits of the Mediterranean diet, in
which the quality of fat in the diet is what leads to a
reduction of cardiovascular risk indicators. Results encourage
higher consumption of poly- and monounsaturated fat and a
reduction of at least 10% of saturated fat in the total calorie
intake [28].

Journal of Diabetes Research


Table 4: Association of diet components with anthropometric and body composition variables.

Tertiles
Calories (kcal)
8121440
14411922
19223420
value
Carbohydrates (g/day)
116.45211.36
211.37238.80
238.81298.50
value
Proteins (g/day)
40.7263.06
63.0770.36
70.3798.24
value
Fats (g/day)
12.9264.50
64.5174.77
74.78149.02
value
Saturated fats (g/day)
1.1818.20
18.2121.89
21.9054.28
value
Dietary fiber (g/day)
4.6321.65
21.6626.68
26.6978.38
value

Weight (kg)

Waist circumference (cm)

Body mass index (kg/m2 )

Body fat (%)

72.6 13.6
76.4 16.0
77.3 14.6
0.022

99.4 12.2
100.9 12.6
101.2 12.6
0.458

29.8 5.0
31.0 5.5
30.8 5.3
0.145

42.4 11.1
41.9 11.3
41.4 12.9
0.782

78.1 16.0
74.2 14.5
73.8 13.6
0.035

101.4 12.5
100.6 12.4
99.4 12.4
0.416

30.8 5.3
30.4 5.3
30.2 5.3
0.654

41.2 11.3
42.7 12.3
41.7 11.7
0.572

75.9 14.1
74.5 15.1
75.8 15.4
0.705

101.5 12.2
99.8 12.4
100.2 12.6
0.528

30.9 5.4
30.2 4.9
30.4 5.6
0.538

43.2 11.9
41.9 11.1
40.5 12.2
0.172

75.0 14.5
74.3 14.1
76.9 15.9
0.347

101.0 12.4
99.7 12.3
100.7 12.5
0.698

30.5 5.4
30.3 5.2
30.7 5.3
0.853

40.9 12.1
42.6 11.7
42.1 11.5
0.462

72.6 13.5
75.9 15.4
77.7 15.3
0.020

99.2 12.8
100.4 11.8
101.8 12.6
0.223

29.8 5.2
30.7 5.3
31.0 5.3
0.183

40.9 12.2
42.7 11.0
42.0 12.0
0.450

78.1 14.2
74.1 14.9
73.9 15.2
0.037

102.5 12.2
99.3 11.5
99.5 13.3
0.063

31.0 5.2
30.1 5.0
30.4 5.6
0.407

42.2 12.5
41.9 10.9
41.5 11.9
0.888

Data are presented as mean standard deviation, according to each tertile of diet components. Comparison was performed with ANOVA.

The association between dietary fiber consumption and


improved HbA1c, HDL-c, and weight levels is consistent with
what has been reported by other authors regarding the effect
of fiber in reducing postprandial glucose, increased satiety,
better glycemic control, improvement of cardiovascular risk
factors, and reduced risk of macrovascular complications
[29, 30]. Even though, in the studied population, 48% had
an adequate dietetic fiber consumption (14 g/1000 calories),
it is still important to promote a varied diet, with a high
consumption of high soluble and insoluble fiber foods,
mainly derived from vegetables, whole grains, dried fruits,
and fruits with a low glycemic index.
An important component for controlling the diabetes is
the education; only three out of every ten patients assessed
have been in an education program. Our results show
the protective effect that this strategy provides to aid the
attainment of improved HbA1c levels, added to what has been

reported regarding the prevention of micro- and macrovascular complications [31]. Despite the foregoing, education
continues to be an underused approach; we must insist on
its use as a measure to promote a healthful lifestyle and a
better care of the disease. Comprehensive treatment should
be aimed at obtaining adequate metabolic control and at
encouraging the detection and timely medical and nutritional
treatment of diabetes [32].

5. Conclusions
A higher content of fiber in the diet had an impact on
reducing HbA1c and triglycerides, while improving HDL-c
levels. Lower calorie and saturated fat consumption may still
be an appropriate strategy to reduce body weight, promote
blood glucose control, and improve HDL-c levels. Since
metabolic control is deficient in Mexicans, we must insist
on a higher fiber content in the diet, given the beneficial

Journal of Diabetes Research

Table 5: Odds ratios (OR) and 95% confidence intervals (CI95% )


derived from a multivariate logistic regression model to identify the
risk of an inadequate glycemic control (HbA1c > 7%).
OR
Total energy (kcal)
8121440
1
14411922
0.81
19223420
1.35
Dietary fiber (g/day)
26.6978.38
1
21.6626.68
2.16
4.6321.65
1.91
Years since diagnosis
<5 years (reference)
1
510 years
2.26
>10 years
2.01
Pharmacologic treatment
Oral hypoglycemic drugs (reference) 1
Oral hypoglycemic drugs and insulin 6.97
Insulin
5.28
No drugs
0.79
Education in diabetes
Yes (reference)
1
No
2.19
Sex
Male (reference)
1
Female
0.84
BMI
Normal weight
1
Overweight
1.05
Obesity
1.02

CI95%

value

0.461.41
0.752.41

0.459
0.309

1.223.83
1.083.35

0.008
0.024

1.283.99
1.013.78

0.005
0.029

2.3220.86
1.7016.35
0.272.36

0.001
0.004
0.683

1.353.42

0.002

0.511.38

0.496

0.492.25
0.482.16

0.890
0.950

Inadequate glycemic control (HbA1c > 7%), odds ratios (OR), and 95%
confidence intervals (CI95% ). Calories and dietary fiber are presented in
tertiles. BMI: body mass index. Individuals were considered of normal weight
with BMI < 24.9, overweight with 2529.9, and obesity > 30 kg/m2 .

effects noted in bringing down HbA1c levels and weight,


while improving lipid profile.

Ethical Approval
This study was conducted according to the guidelines laid
down in the Declaration of Helsinki and all procedures
involving human subjects/patients were approved by the
Ethics and Health Research Committee of the Mexican Social
Security Institute.

Consent
Written informed consent was obtained from all subjects/patients.

Competing Interests
The authors declare that they have no competing interests.

Table 6: Odds ratios (OR) and 95% confidence intervals (CI95% )


derived from a multivariate logistic regression model to identify the
risk of an inadequate HDL-c.
OR
Total energy (kcal)
8121440
1
14411922
1.029
19223420
0.87
Dietary fiber (g/day)
26.6978.38
1
21.6626.68
1.05
4.6321.65
1.79
Years since diagnosis
<5 years (reference)
1
510 years
1.46
>10 years
1.13
Pharmacologic treatment
Oral hypoglycemic drugs (reference) 1
Oral hypoglycemic drugs and insulin 1.01
Insulin
0.65
No drugs
1.83
Education in diabetes
Yes (reference)
1
No
1.45
Sex
Male (reference)
1
Female
1.55
Fats (g/day)
1.018
12.9264.50
1
64.5174.77
1.87
74.78149.02
1.19
Saturated fats (g/day)
1.1818.20
1
18.2121.89
1.32
21.9054.28
1.20
Physical activity
Yes
1
No
1.20
Peso Kg
1.017

CI95%

value

0.561.83
0.471.58

0.977
0.640

0.571.94
0.983.27

0.873
0.059

0.802.62
0.602.12

0.211
0.701

0.452.24
0.291.46
0.486.90

0.930
0.300
0.369

0.892.37

0.133

0.922.61
1.001.03

0.103
0.046

1.023.39
0.652.17

0.040
0.573

0.722.43
0.612.35

0.366
0.590

0.612.35
1.001.03

0.590
0.042

Inadequate HDL-c (<40 mg/dL in male and <50 mg/dL in female), odds
ratios (OR) and 95% confidence intervals (CI95% ). Calories, dietary fiber, fats,
and saturated fats are presented in tertiles.

Acknowledgments
This study was supported by a research grant from the Mexico
National Science and Technology Council (Consejo Nacional
de Ciencia y Tecnologa, CONACYT) no. SALUD-2012-01181015.

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1232

EXPERIMENTAL AND THERAPEUTIC MEDICINE 12: 1232-1242, 2016

Therapeutic effects of soluble dietary fiber


consumption on type 2 diabetes mellitus
CHUNYE CHEN1*, YUAN ZENG1*, JING XU2, HONGTING ZHENG2, JUN LIU3, RONG FAN3,
WENYI ZHU3, LIJIA YUAN1, YU QIN1, SHIHUI CHEN1, YONG ZHOU1, YING WU1,
JING WAN1, MANTIAN MI1 and JIAN WANG3
1

Research Center of Nutrition and Food Safety, Chongqing Key Laboratory of Nutrition and Food Safety;
Departments of 2Endocrinology and 3Nutrition, Xinqiao Hospital, The Third Military Medical University,
Shapingba, Chongqing 400038, P.R. China
Received February 21, 2015; Accepted April 1, 2016
DOI: 10.3892/etm.2016.3377

Abstract. Soluble dietary fiber (DF) reduces the risk of developing diabetes and may have therapeutic effects in patients
with type 2 diabetes mellitus (DM2). The present study aimed
to investigate the effect of soluble DF on metabolic control in
patients with DM2. A total of 117 patients with DM2 between
the ages of 40 and 70 were assessed. Patients were randomly
assigned to one of two groups, and administered extra soluble
DF (10 or 20 g/day), or to a control group (0 g/day) for one
month. Blood glucose, serum insulin and connecting peptide
(Cpeptide) levels, and the insulin resistance index, as determined using the homeostatic model assessment method, were
measured during fasting and up to 2h postprandially prior to
and following one month of treatment. Other measurements
included serum levels of glycated albumin (GA), blood lipid
profiles, and an analysis of the blood pressure, body weight
and waist/hip ratio of all patients. Following intervention, the
levels of 2h blood glucose, fasting insulin and lipoprotein(a),
and the insulin resistance index, were significantly improved
in all groups. Furthermore, the fasting blood glucose, 2h
insulin, fasting Cpeptide, 2h Cpeptide, GA and triglyceride
(TG) levels were significantly improved in the soluble DF

Correspondence to: Professor Mantian Mi, Research Center


of Nutrition and Food Safety, Chongqing Key Laboratory of
Nutrition and Food Safety, The Third Military Medical University,
30 Gaotanyan Street, Shapingba, Chongqing 400038, P.R. China
Email: mimantiancn@126.com
Professor Jian Wang, Department of Nutrition, Xinqiao Hospital,
The Third Military Medical University, 183 Xinqiao Street,
Shapingba, Chongqing 400038, P.R. China
Email: wangjiannd@yeah.net
*

Contributed equally

Key words: type 2 diabetes mellitus, soluble dietary fiber, blood


glucose, insulin resistance index, glycated albumin

groups. The 20 g/day soluble DF group exhibited significantly


improved fasting blood glucose and lowdensity lipoprotein
levels, as well as a significantly improved insulin resistance
index. In addition, 10 and 20 g/day soluble DF significantly
improved the waist and hip circumferences and levels of
TGs and apolipoprotein A. The results of the present study
suggested that increased and regular consumption of soluble
DF led to significant improvements in blood glucose levels,
insulin resistance and metabolic profiles, without improving
the secretory function of the islets of Langerhans, over a
shortterm intervention period in patients with DM2.
Introduction
Type 2 diabetes mellitus (DM2) is associated with numerous
complications, including kidney failure, blindness, an
increased susceptibility to infection, coronary heart disease
and stroke (1). It is predicted that by 2030 ~10% of the
world's population will have diabetes mellitus (DM) (mostly
type 2) (2). Interventions that improve diet quality have been
demonstrated to be effective in controlling hyperglycemia
and its associated risk factors, which in turn reduces the risk
of diabetesassociated complications (3). Considering the
seriousness of DM2 complications, early dietary education is
critical for delaying or preventing disease onset. Accordingly,
the American Diabetes Association (ADA) has recommended
dietary guidelines for patients with DM2 (4).
Dietary fiber (DF) is widely prescribed (5), either alone
or in combination with lipidlowering therapies, to reduce
cholesterol levels (6). The exact mechanism by which soluble
fiber lowers serum levels of lowdensity lipoprotein (LDL)
and cholesterol is not completely understood; however, it
has been suggested that soluble fiber may interfere with lipid
and/or bile acid metabolism (7). A reasonable increase in DF
intake (2035 g/day) is recommended by the ADA based on
the effects of soluble fiber on plasma levels of cholesterol (4).
Recent epidemiological findings have suggested that there is
an association between high DF intake and a reduced risk
of developing diabetes and coronary heart disease (8,9).
In particular, soluble DF has been shown to reduce insulin
resistance in female nondiabetic patients (10). However, there

CHEN et al: EFFECTS OF DIETARY FIBER ON TYPE 2 DIABETES

remains a lack of clinical intervention studies with sufficient


sample sizes to support the beneficial effects of DF intake in
patients with DM2.
The present study aimed to investigate the effects of DF on
glycemic control and plasma lipid concentrations in patients
with DM2. Patients were administered DF at doses greater
than the ADArecommended level of 2535 g in order to elucidate how a highfiber diet may affect plasma cholesterol levels,
intestinal cholesterol absorption and fecal sterol excretion (11).
Materials and methods
Patients. A total of 120 patients at the Xinqiao Hospital of
the Third Military Medical University (Chongqing, China),
who had been diagnosed with DM2 [based on the 2010 ADA
criteria (12)] for 6 months, were enrolled in the present study
between December 2012 and February 2013 (clinical trial
registration no. ChiCTRTRC12002580). The majority of the
enrolled patients had been diagnosed after reaching 40 years
of age. The age of the patients ranged from 4570 years
(average age, 549 years), and they had a mean body weight of
68.113.0 kg and a mean body mass index (BMI) of 25.33.9
kg/m2. A total of 40 patients were treated with the ADA diet
alone, whereas the remaining 80 patients were treated with
10 or 20 mg soluble DF daily in addition to the ADA diet for
one month. Upon study entry, all patients were free of tumors,
myocardial infarction, unstable angina pectoris and congestive
heart failure. Furthermore, no thyroid or hepatic disease was
found, and none of the patients were undergoing lipidlowering
treatments.
Written informed consent was obtained from all patients
prior to participation. The present study was approved by the
Ethics Committee of the Third Military Medical University.
All procedures were conducted in accordance with the
Declaration of Helsinki.
Study design. The present study was a randomized,
doubleblind trial. The three common treatments for patients
with DM2 include oral medication, insulin therapy or a
combination of both. Subjects that met the inclusion criteria
were stratified according to treatment and randomly divided
into the following three groups using a random number table
(40 subjects/group): i) Control; ii) lowdose (10DF); and
iii) highdose (20DF) groups. All patients received medical
nutrition therapy (MNT), which include personal nutritional
assessment and reasonable nutritional intervention. Lifestyle
interventions consisted of individualized dietary counseling
and encouragements to increase daily physical activity. Each
patient received an individualized recommended intake of
daily energy according to the ADA guidelines (12). After one
month of treatment, 37 patients remained in the control group,
3 patients quit for personal reasons and 40 patients remained in
the 10DF and 20DF groups, respectively. In the control group,
16 patients received oral medicine [500 mg of metformin hydrochloride tablets (BristolMyers Squibb Company, Princeton,
NJ, USA) twice a day and 50 mg of acarbose tablets (Bayer
HealthCare Pharmaceuticals Inc., Leverkusen, Germany)
three times daily], 9 patients selfadministered insulin injections and 12 patients took both. In the 10DF group, 17 patients
received oral medicine [(500 mg of metformin hydrochloride

1233

tablets twice a day and 50 mg of acarbose tablets three times


daily)], 10 patients selfadministered insulin injections and
13 patients took both. In the 20DF group, 17 patients received
oral medicine (500 mg of metformin hydrochloride tablets
twice a day and 50 mg of acarbose tablets three times daily),
11 patients selfadministered insulin injections and 12 patients
took both. The constituent ratios of medication among the three
groups were not significantly different (P=0.894). Patients in
the control group received MNT only, and patients in the 10DF
and 20DF groups were provided with 10 and 20 g soluble DF
each day, respectively. The total duration of the trial was one
month, during which time the subjects received MNT treatment. All participants received a weekly consultation, during
which the patient's protocol compliance was assessed For
patients with a poor compliance, more frequent calls were
made to ensure that they took enough DF. The body weight,
blood pressure and waist and hip circumferences of all patients
were measured prior to and following treatment by clinical lab
technicians who were blinded to the content and purpose of
the study. In addition, the patients were asked to complete a
3day record of their food intake at the baseline and end of
the trial, which were analyzed using NCCW 2011 software
(Dongcheng New technology Co., Ltd., Qingdao, China) to
estimate nutrient intake. Furthermore, the patients were asked
to complete a questionnaire prior to treatment regarding their
dietary habits, including how frequently they consumed meat,
milk, eggs, vegetables and other foods, and if they regularly
consumed vitamin or mineral supplements.
Subjects reported a normal bowel habit and denied any
symptoms of difficult defecation or rectal bleeding on a
symptom questionnaire that inquired about stool frequency,
straining effort, feeling of incomplete evacuation, use of
digital maneuvers, painful defecation, hard stools, abdominal
pain, and reflux symptoms (13).
Biochemical analyses. Blood samples (12 ml) were collected in
anticoagulantfree tubes [for serum lipids, insulin, connecting
peptide (Cpeptide), urea nitrogen, and creatinine assays;
Zhongshan Jinqiao Biotechnology Co., Ltd., Beijing, China]
and fluorideoxalate anticoagulant tubes (for the plasma
glucose assay; Zhongshan Jinqiao Biotechnology Co., Ltd.).
Anticoagulantfree tubes (Zhongshan Jinqiao Biotech Co., Ltd.)
were allowed to clot in the dark at room temperature for 2 h and
held for 2 h, and the fluorideoxalate tubes were immediately
placed on ice. Both tubes were centrifuged at 1,000 x g for
20 min at 4C. Serum and plasma were separated and frozen
at 80C until further analysis. All biochemical analyses on
samples from individual participants were performed together
to eliminate interassay variability. Plasma glucose, serum
lipid and lipoprotein(a) (Lpa) levels were analyzed using a
blood biochemical analyzer (AU2700; Olympus Corporation,
Tokyo, Japan). Plasma glucose, serum total cholesterol,
highdensity lipoprotein (HDL) and triglycerides (TG) were
measured using enzymatic reagents (Zhongshan Jinqiao
Biotechnology Co., Ltd.). LDL (TA309729), apolipoprotein
(apo; TA318199), serum insulin (TA306175), serum glycated
albumin (GA; TA307256), Cpeptide (TA317763), urea
nitrogen (TA306427), and creatinine levels (TA305574) were
measured by radioimmunoassays using commercially available kits (Chongqing Keyuan Medical Equipment Co., Ltd.,

1234

EXPERIMENTAL AND THERAPEUTIC MEDICINE 12: 1232-1242, 2016

Figure 1. Flow diagram of participants.

Chongqing, China). The intraassay coefficients of variance for


serum lipids, lipoproteins and plasma glucose were <2% and
<6% for serum insulin and Cpeptide, respectively. The insulin
resistance index was determined using the homeostatic model
assessment method (14). Insulin resistance and cell function
were estimated from fasting glucose and insulin levels.
Statistical analysis. Data were analyzed using SPSS software, version 19.0 (IBM SPSS, Armonk, NY, USA). Data
are presented as the mean standard deviation. 95% confidence intervals (CIs) were calculated for the mean values
between groups. The ShapiroWilk test demonstrated that
all of the main outcome variables were normally distributed.
Differences in patient characteristics between pre and
posttreatments were assessed using paired Student's ttests.
Oneway analysis of covariance, with the difference between
pre and posttreatment set as the dependent variable and
the baseline value as the covariant, was used to compare the
soluble DF groups with the control group for blood markers
and anthropometric characteristics. P<0.05 was considered to
indicate a statistically significant difference.
Results
Participant flow. Based on patient interviews, estimates of
dietary energy content and the remainder of soluble DF, a
satisfactory level of patient compliance was achieved in the
present study. A participant flow diagram is shown in Fig. 1.
Baseline data and participant characteristics. According to
the baseline energy intake questionnaire survey, the 20DF

group consumed significantly more Vitamin C, as compared


with the other groups (P<0.05). However, no other significant differences in dietary intake were observed between
the groups. The mean energy intake of all groups was
2302.78872.48 kcal/day. The average percentage of calories
obtained from fat intake was 36.35%, which was markedly
higher than the ADA recommendation (2030%). The average
intake of DF was 15.91 g, which was markedly lower than
the ADA recommendation (2535 g) (Table I). The age, BMI,
waist/hip ratio, blood glucose and insulin levels, and several
other baseline characteristics, were recorded for all patients.
No significant differences were observed between groups for
the baseline characteristics (Table II).
Outcomes and estimation. According to the energy intake
questionnaire survey completed one month postintervention,
the 10DF and the 20DF groups consumed significantly more
DF, as compared with the control group (P<0.01). Energy,
protein, fat, carbohydrate and cholesterol intakes were significantly lower in the energy intake questionnaires completed
one month postintervention, as compared with the baseline
questionnaires (P<0.05). Furthermore, the calories from fat
and carbohydrate intake were significantly decreased in the
one month postintervention questionnaire, as compared with
the baseline questionnaire (P<0.05; Table I). The results of the
blood marker analysis, including anthropometric measures,
lipid profile and DM2 biomarkers, and assessment of physical
characteristics, at one month following intervention are
summarized in Table III. After one month of treatment, the
systolic pressure and levels of HDL, LDL and apoB were
significantly improved in the 20DF group as compared with the

2326.40759.24
75.2434.34
13.563.58
118.8482.42
38.2314.56
254.7184.62
48.2114.40
14.589.38
502.55334.87
555.61179.60
1.340.54
0.900.42
79.6758.10
27.8017.80
18.0010.00
1805.80970.24
488.07441.22
367.59174.58
304.84198.87
19.718.40
4.922.48
12.214.74
1.901.21
46.5925.64
1076.22521.14

1701.80246.65a
62.3315.27b
14.042.16
59.9017.77a
24.002.86a
227.4042.36b
61.963.92a
14.254.53
221.1769.84a
608.81162.05
1.150.60
0.850.48
120.62117.32
42.9719.02
14.808.83
1879.441318.64
397.91203.13
409.55228.40
323.58227.09
18.939.98
5.052.46
11.024.54
1.991.22
36.2117.57
1031.75490.89

Control (n=37)
----------------------------------------------------------------Baseline
1 month
2232.71823.95
75.6631.97
14.153.46
83.6057.51
34.7113.27
270.1088.94
51.1412.86
15.689.37
450.67323.85
542.95151.30
1.200.59
0.870.33
108.4372.80
17.4710.21
15.318.56
2122.181424.78
441.47181.95
440.87220.15
346.87255.97
19.6010.14
5.382.83
11.613.99
2.181.28
39.2914.17
1070.40421.21

1724.86240.46a
65.1315.94a
15.382.84
62.5214.08b
23.972.89a
241.7454.76b
60.654.21a
24.924.67a,c
232.4663.01a
611.25173.07
1.420.66
0.980.66
171.38180.15
31.6023.36
18.049.01
2333.631357.68
554.97464.17
451.23293.72
383.31217.49
21.478.89
5.962.82
12.655.68
2.331.31
41.4819.05
1170.73540.84

10DF (n=40)
-----------------------------------------------------------------Baseline
1 month
2371.13994.31
87.1245.25
14.243.47
97.8059.78
36.2510.83
290.69119.85
49.5112.68
17.369.17
621.61523.25
655.85143.65
1.440.66
1.030.51
145.30100.08c
36.4923.46
17.608.66
2404.961197.49
645.86418.65
538.83296.37
380.53196.12
24.049.96
6.392.54
13.255.42
2.451.18
52.4037.41
1266.12530.88

1799.37295.76a
67.3515.80a
14.872.58
68.6415.92a
24.252.67a
252.8070.41b
60.883.47a
35.884.57a,c
227.8763.62a
618.54151.42
1.510.91
1.170.78
144.47129.14
38.3220.57
16.449.80
2646.091004.37
563.97400.39
584.43442.31
439.85284.76
24.5214.86
7.314.32
13.647.12
2.681.64
41.5320.29
1382.31791.55

20DF (n=40)
--------------------------------------------------------------------Baseline
1 month

Data are presented as the meanstandard deviation. aP<0.01 and bP<0.05, vs. the baseline; cP<0.01 vs. the control group. 10DF, 10g/day dietary fiber; 20DF, 20g/day dietary fiber; Vit, vitamin.

Energy (kcal/day)
Protein (g/day)
(% of energy)
Fat (g/day)
(% of energy)
Carbohydrate (g/day)
(% of energy)
Dietary fiber (g/day)
Cholesterol (mg/day)
Vit A (mg/day)
Vit B1 (mg/day)
Vit B2 (mg/day)
Vit C (mg/day)
Vit E (mg/day)
Vit PP (mg/day)
K (mg/day)
Na (mg/day)
Ca (mg/day)
Mg (mg/day)
Fe (mg/day)
Mn (mg/day)
Zn (mg/day)
Cu (mg/day)
Se (mg/day)
P (mg/day)

Parameter

Table I. Dietary energy intake.

CHEN et al: EFFECTS OF DIETARY FIBER ON TYPE 2 DIABETES

1235

1236

EXPERIMENTAL AND THERAPEUTIC MEDICINE 12: 1232-1242, 2016

Table II. Baseline characteristics.


Parameter
n
Age
Gender (M/F)
Weight (kg)
BMI (kg/m2)
Waist circumference (cm)
Hip circumference (cm)
Waist/hip ratio
Systolic pressure (mmHg)
Diastolic pressure (mmHg)
Fasting blood glucose (mmol/l)
2h blood glucose (mmol/l)
Fasting insulin (mU/l)
2h insulin (mU/l)
HOMAIR
Fasting Cpeptide (ng/ml)
2h Cpeptide (ng/ml)
Glycated albumin (%)
Cholesterol (mmol/l)
Triglyceride (mmol/l)
HDL (mmol/l)
LDL (mmol/l)
Lpa (mg/l)
ApoA (g/l)
ApoB (g/l)
Urea nitrogen (mmol/l)
Creatinine (mol/l)
Uric acid (mol/l)

Control

10DF

20DF

Fvalue

37
51.526.47
14/23
69.608.50
25.652.62
90.508.10
100.907.71
0.900.06
128.4615.87
75.5410.72
8.122.78
12.554.39
9.557.06
23.7816.52
3.342.64
2.251.03
5.284.05
18.844.74
4.832.16
2.081.58
1.120.42
2.922.71
292.16258.47
1.120.27
1.420.36
6.003.68
64.0922.49
289.65104.52

40
53.639.37
15/25
65.3010.20
24.802.92
90.709.79
100.007.01
0.910.06
132.8517.29
79.5812.19
8.262.84
12.504.21
9.275.75
24.9423.20
3.402.59
2.781.57
6.574.20
20.004.31
4.841.17
2.682.68
1.270.41
2.450.74
311.38282.61
1.250.29
1.300.49
5.911.73
59.5820.60
304.8392.57

40
55.528.15
17/23
69.5013.00
25.323.96
91.3110.90
100.617.21
0.910.06
130.7515.53
79.1510.23
8.712.91
12.543.88
9.815.60
24.9614.72
3.922.77
2.591.39
6.153.01
20.645.35
5.071.31
2.402.68
1.360.71
2.900.80
313.15227.88
1.290.49
1.520.48
5.862.01
60.3615.28
296.7876.57

2.066
0.675
0.071
0.144
0.239
0.701
1.517
0.459
0.002
0.076
0.226
0.549
1.457
0.013
1.368
0.287
0.599
1.983
1.008
0.078
2.294
2.007
0.029
0.574
0.265

Pvalue

0.131
0.511
0.931
0.866
0.788
0.498
0.224
0.633
0.998
0.927
0.798
0.579
0.237
0.987
0.259
0.751
0.551
0.142
0.368
0.925
0.106
0.132
0.971
0.565
0.768

Data are presented as the mean standard deviation. 10DF, 10 g/day dietary fiber; 20DF, 20 g/day dietary fiber; M, male; F, female; BMI, body
mass index; HOMAIR, homeostatic model assessmentinsulin resistance; HDL, highdensity lipoprotein; LDL, lowdensity lipoprotein; Lpa,
lipoprotein(a); Apo, apolipoprotein.

data prior to the treatment (P<0.05). In addition, weight, BMI


and hip circumference values were significantly improved in
the control and 10DF groups (P<0.05), and the waist circumference was significantly reduced in the 10DF group (P<0.05) as
compared with the data prior to the treatment. Fasting insulin,
2h blood glucose and Lpa levels, and the insulin resistance
index, as determined using the homeostatic model assessment method, were significantly improved in all three groups
as compared with the data prior to the treatment (P<0.05).
Furthermore, the fasting blood glucose, 2h insulin, fasting
C-peptide, 2h Cpeptide, GA and TG levels were significantly
improved in the DF groups (P<0.05), as compared with the
control group, where no significant improvements for these
metrics were observed.
Differences between pre and posttreatment among the
three groups are compared in Table IV. Univariate analysis of
general linear models, with the difference between pre and
posttreatment as the dependent variable and the baseline value
as the covariant, was used. Levels of fasting blood glucose

and LDL, and the insulin resistance index, were significantly


improved posttreatment in the 20DF group (P<0.05), but not
in the 10DF group. Both 10 and 20 g/day soluble DF significantly improved the 2h blood glucose and GA levels (P<0.05),
although 20 g/day soluble DF had a greater effect (P<0.05).
Furthermore, both 10 and 20 g/d soluble DF significantly
improved the waist and hip circumferences and TG and apoA
levels (P<0.05), and no significant differences were found
between the 10DF and 20DF groups for these parameters.
No significant differences between the 10DF and 20DF were
observed for weight, BMI, blood pressure and levels of fasting
insulin, 2h insulin, fasting Cpeptide, 2h Cpeptide, cholesterol, HDL, Lpa, apoB, urea nitrogen, creatinine and uric acid.
Safety data. To assess the safety of increased soluble DF
intake, the renal function of all patients was measured. No
significant differences were observed between the baseline
and one month postintervention measurements for all three
groups (Table V). Seven patients in the 20DF group and two

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CHEN et al: EFFECTS OF DIETARY FIBER ON TYPE 2 DIABETES

Table III. Anthropometric measures, lipid profile and type 2 diabetes mellitus biomarkers after 1 month of treatment.
Parameter

Group

Baseline

1 month

Weight (kg)

Control
10DF
20DF
Control
10DF
20DF
Control
10DF
20DF
Control
10DF
20DF
Control
10DF
20DF
Control
10DF
20DF
Control
10DF
20DF
Control
10DF
20DF
Control
10DF
20DF
Control
10DF
20DF
Control
10DF
20DF
Control
10DF
20DF
Control
10DF
20DF
Control
10DF
20DF
Control
10DF
20DF
Control
10DF
20DF
Control
10DF
20DF
Control
10DF
20DF

128.4615.87
132.8217.29
130.7515.53
75.5410.72
79.5812.2
79.1510.23
69.578.48
65.2610.20
69.4912.99
25.652.62
24.802.92
25.333.96
90.518.05
90.719.81
91.3110.96
100.957.69
100.067.05
100.587.04
0.900.06
0.910.06
0.910.06
8.122.78
8.262.84
8.712.91
12.554.39
12.504.20
12.543.88
9.557.06
9.275.75
9.815.60
23.7816.52
24.9423.20
24.9614.72
3.342.64
3.402.59
3.922.77
2.251.03
2.781.57
2.591.39
5.284.05
6.574.20
6.153.01
18.844.74
20.004.31
20.645.35
4.832.16
4.841.17
5.071.31
2.081.58
2.682.68
2.402.68
1.120.42
1.270.41
1.360.71

123.8614.07
127.9315.89
126.0015.85a
76.059.32
76.408.03
78.388.39
67.278.29b
63.509.56a
68.0312.52
24.832.83a
24.162.82a
24.753.42
89.957.29
88.188.24b
91.039.41
99.086.86a
97.607.10b
100.247.14
0.910.05
0.900.06
0.910.06
7.672.87
7.262.94a
6.131.18b
11.274.75a
9.733.81b
8.082.77b
7.435.23a
7.244.72a
7.774.17b
20.7215.92a
19.7211.02b
21.3711.86b
2.562.17b
2.301.58b
2.121.29b
1.940.96
1.930.79b
1.960.78b
4.282.65
3.591.78b
3.272.03b
17.614.35
15.273.81b
12.611.92b
4.811.01
4.931.02
4.971.10
2.452.80
1.771.96b
1.551.21b
1.020.33
1.180.40
1.120.27a

1.779
1.968
2.232
0.375
1.894
0.517
2.841
2.656
1.325
2.715
2.535
1.343
0.677
2.822
0.088
2.373
3.199
0.255
1.211
0.240
0.448
1.162
2.684
5.957
2.667
4.409
7.721
2.729
2.371
2.819
2.446
3.435
4.704
3.794
3.182
4.678
1.856
3.893
3.212
2.008
2.979
1.869
1.859
7.361
8.948
0.039
0.801
0.463
1.019
2.891
3.177
1.457
1.896
2.359

BMI (kg/m2)

Waist circumference (cm)

Hip circumference (cm)

Waist/hip ratio

Systolic pressure (mmHg)

Diastolic pressure (mmHg)

Fasting blood glucose (mmol/l)

2h blood glucose (mmol/l)

Fasting insulin (mU/l)

2h insulin (mU/l)

HOMAIR

Fasting Cpeptide (ng/ml)

2h Cpeptide (ng/ml)

Glycated albumin (%)

Cholesterol (mmol/l)

Triglyceride (mmol/l)

HDL (mmol/l)

Pvalue
0.084
0.056
0.031
0.710
0.066
0.608
0.007
0.012
0.193
0.010
0.015
0.187
0.502
0.007
0.930
0.023
0.003
0.800
0.234
0.812
0.657
0.253
0.011
<0.001
0.011
<0.001
<0.001
0.010
0.023
0.008
0.019
0.001
<0.001
0.001
0.003
<0.001
0.072
<0.001
0.003
0.052
0.005
0.004
0.071
<0.001
<0.001
0.969
0.428
0.646
0.315
0.006
0.003
0.154
0.065
0.023

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EXPERIMENTAL AND THERAPEUTIC MEDICINE 12: 1232-1242, 2016

Table III. Continued.


Parameter

Group

Baseline

1 month

LDL (mmol/l)

Control
10DF
20DF
Control
10DF
20DF
Control
10DF
20DF
Control
10DF
20DF

2.922.71
2.450.74
2.900.80
292.16258.47
311.38282.61
313.15227.88
1.120.27
1.250.29
1.290.49
1.020.36
1.300.49
1.520.48

2.761.62
2.320.61
2.310.76b
378.35315.53b
371.38207.30a
362.60186.65b
1.040.17
1.190.26
1.200.23
0.950.42
1.160.59
1.180.35b

0.452
1.348
4.683
4.210
2.581
3.126
2.013
1.315
1.165
1.842
1.572
3.627

Lpa (mg/l)

ApoA (g/l)

ApoB (g/l)

Pvalue
0.654
0.185
<0.001
<0.001
0.014
0.003
0.052
0.196
0.251
0.074
0.124
0.001

Data are presented as the mean standard deviation. Significant Pvalues (P<0.05) are indicated in bold. aP<0.05 and bP<0.01 vs. the baseline.
10DF, 10 g/day dietary fiber; 20DF, 20 g/day dietary fiber; BMI, body mass index; HOMAIR, homeostatic model assessmentinsulin resistance; HDL, highdensity lipoprotein; LDL, lowdensity lipoprotein; Lpa, lipoprotein(a); Apo, apolipoprotein.

Table IV. Comparison of the statistical differences between the pre and posttreatment measurements of various parameters
among the three groups.
Parameter
Weight (kg)
BMI (kg/m2)
Waist circumference (cm)
Hip circumference (cm)
Waist/hip ratio
Systolic pressure (mmHg)
Diastolic pressure (mmHg)
Fasting blood glucose (mmol/l)
2 h blood glucose (mmol/l)
Fasting insulin (mU/l)
2 h insulin (mU/l)
HOMAIR
Fasting Cpeptide (ng/ml)
2 h Cpeptide (ng/ml)
Glycated albumin (%)
Cholesterol (mmol/l)
Triglyceride (mmol/l)
HDL (mmol/l)
LDL (mmol/l)
Lpa (mg/l)
ApoA (g/l)
ApoB (g/l)
Urea nitrogen (mmol/l)
Creatinine (mol/l)
Uric acid (mol/l)

Control

10DF

2.304.92
0.821.84
0.575.10
1.864.78
0.010.05
4.5915.71
0.518.34
0.452.36
1.292.94
2.114.71
3.077.62
0.791.26
0.321.05
1.003.04
1.234.03
0.011.80
0.372.19
0.100.41
0.162.15
86.19124.52
0.070.22
0.070.24
0.603.34
1.9417.60
3.9277.67

1.764.20
0.651.62
2.545.69
2.464.87
0.000.05
4.9315.83
3.1810.60
1.002.36
2.773.97d
2.045.43
5.229.61
1.112.20
0.851.37
1.994.22
4.734.06
0.100.76
0.911.98
0.090.30
0.130.61
60.00147.05
0.060.30d
0.140.57
0.411.75
2.3210.34
10.7065.16

20DF

P1

1.477.02
0.659
0.582.72
0.877
0.096.44a
0.051
0.215.09a
0.074
0.000.06
0.738
4.7513.46
0.833
0.789.48
0.399
2.582.74b,c <0.001
4.463.65a,b <0.001
2.044.58
0.941
4.696.31
0.514
1.802.44d
0.081
0.621.23
0.684
0.882.97
0.127
b,c
8.755.39
<0.001
0.931.32
0.848
0.841.69b
0.008
0.240.65
0.251
0.580.79d
0.091
49.45100.06 0.436
0.090.47d
0.028
0.340.59
0.609
0.411.79
0.921
1.6411.07
0.527
1.4379.87
0.802

P2
0.865
0.901
0.095
0.428
0.444
0.546
0.405
0.303
0.033
0.937
0.250
0.344
0.386
0.989
<0.001
0.570
0.008
0.818
0.195
0.368
0.021
0.344
0.692
0.291
0.599

P3
0.496
0.720
0.493
0.150
0.781
0.747
0.639
<0.001
<0.001
0.803
0.519
0.026
0.690
0.085
<0.001
0.723
0.005
0.129
0.030
0.210
0.018
0.776
0.781
0.371
0.943

P4
0.391
0.622
0.018
0.025
0.625
0.772
0.181
0.004
0.016
0.738
0.605
0.186
0.627
0.076
<0.001
0.828
0.861
0.187
0.368
0.717
0.922
0.506
0.904
0.868
0.541

Data are presented as the mean standard deviation. Significant Pvalues (P<0.05) are indicated in bold. aP<0.05 vs. the 10DF group; bP<0.01 vs.
the control group; cP<0.01 vs. the 10DF group; dP<0.05 vs. the control group. P1, analysis of variance among the three groups; P2, comparison
between the 10DF and control groups; P3, comparison between the 20DF and control groups; P4, comparison between the 10DF and 20DF
groups; 10DF, 10 g/day dietary fiber; 20DG, 20 g/day dietary fiber; BMI, body mass index; HOMAIR, homeostatic model assessmentinsulin
resistance; HDL, highdensity lipoprotein; LDL, lowdensity lipoprotein; Lpa, lipoprotein(a); Apo, apolipoprotein.

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Table V. Renal function data.


Parameter

Group

Baseline

1 month

Pvalue

Urea nitrogen (mmol/l)

Control
10DF
20DF
Control
10DF
20DF
Control
10DF
20DF

6.003.68
5.911.73
5.862.01
64.0922.49
59.5820.60
60.3615.28
289.65104.52
304.8392.57
296.7776.57

5.401.49
5.501.44
5.451.53
62.1518.73
61.9119.99
62.0015.42
293.5788.28
294.1371.33
298.2067.34

1.093
1.468
1.438
0.670
1.421
0.937
0.307
1.039
0.113

0.282
0.150
0.158
0.507
0.163
0.354
0.761
0.305
0.911

Creatinine (mol/l)

Uric acid (mol/l)

Data are presented as the mean standard deviation. 10DF, 10 g/day dietary fiber; 20DF, 20 g/day dietary fiber.

Table VI. Defecation analysis.

Group

7day defecation frequency


---------------------------------------------------------Baseline
1 month

Defecation sensation score


---------------------------------------------------------Baseline
1 month

Stool characteristics score


---------------------------------------------------------Baseline
1 month

Control
10DF
20DF
Pvalue

5.272.33
5.402.35
5.252.42
0.954

1.221.10
1.351.60
1.181.04
0.752

1.491.04
1.451.04
1.481.01
0.987

5.272.16
6.331.00a,b
6.451.22a,b
0.002c

1.221.08
0.500.60a,b
0.550.64a,b
<0.001c

1.451.04
0.650.77a,b
0.630.68a,b
<0.001c

Data are presented as the mean standard deviation. aP<0.05 vs. the control group; bP<0.05 vs. the baseline; cP<0.05; analysis of variance
among the three groups. 10DF, 10 g/day dietary fiber; 20DF, 20 g/day dietary fiber.

patients in the 10DF group complained of excessive flatulence.


However, increased soluble DF intake significantly improved
defecation frequency, defecation ease and stool characteristics
(P<0.05; Table VI).
Discussion
Dietary factors have been demonstrated to impact the development of DM2 and its associated complications (15). A
survey conducted in the US reported an average DF intake
of 17 g/day in non-diabetic individuals, with an average of
16 g/day demonstrated in diabetic patients (16). In the present
study, patients consumed an average of 15.9 g/day DF, which
was lower than that recommended by the ADA and may be
partially due to ignorance regarding the beneficial effects of
DF on glycemic control. Therefore, the present study aimed
to investigate the effects of increased DF intake on glycemic
control and the underlying mechanisms.
In the present study, 2h blood glucose, fasting insulin and
Lpa levels, and the insulin resistance index, were significantly
improved from baseline in all three groups, thus suggesting that
MNT treatment was able to significantly impact blood glucose
levels and glycemic control. In three large randomized trials,
including the China Da Qing Diabetes Prevention study (17),
the Finnish Diabetes Prevention Study (18) and the Diabetes
Prevention Program trial (19), it was demonstrated that the

progression from impaired glucose tolerance to DM2 may be


delayed or even prevented by diet and exercise. Furthermore,
dietary interventions aimed at improving diet quality have
been shown to be effective for controlling DM2 (2), which is
consistent with the results of the present study.
Increasing DF intake, which is one of the goals of
nutritional counseling, deserves greater attention due to its
ability to reduce total cholesterol levels and hyperglycemia
in patients with impaired glucose tolerance and DM2 (20).
In addition, increased fiber intake was shown to improve
insulin sensitivity and reduce systemic inflammation (21,22).
Previous studies have demonstrated that highfiber diets
(30 g/day) altered biochemical parameters, reduced the
severity of DM2 and decreased the occurrence of risk factors
associated with cardiovascular disease (21,23). According to
Weickert et al (21), nutritional educational studies involving
dietary restrictions are typically met with poor treatment
compliance. Participants in a previous study were encouraged to progressively alter their eating behaviors, including
increasing the frequency of meals and increasing the intake of
complex carbohydrates, DF, fruits, and vegetables, as well as
polyunsaturated and monounsaturated fatty acids, including
fish and olive oils, respectively (21). However, MNT treatment was unable to increase DF intake in the subjects (21).
Similarly, another interventional study involving nutritional
education has failed to increase fiber intake (24). In the present

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EXPERIMENTAL AND THERAPEUTIC MEDICINE 12: 1232-1242, 2016

study, patients received extra soluble DF and were required to


recount the remaining soluble DF during a phone consultation every week. Soluble DF has been associated with lower
postprandial glucose levels and increased insulin sensitivity
in diabetic and healthy subjects; these effects were generally attributed to the viscous and/or gelling properties of
soluble fiber (25). Soluble DF exerts physiological effects on
the stomach and small intestine that modulate postprandial
glycemic responses, including delaying gastric emptying (26),
which accounts for ~35% of the variance in peak glucose
concentrations following the ingestion of oral glucose (27),
modulating gastrointestinal myoelectrical activity and
delaying small bowel transit (28,29), reducing glucose diffusion through the unstirred water layer (30), and reducing the
accessibility of amylase to its substrates due to the increased
viscosity of gut contents (31). Notably, the increased viscosity
and gelforming properties of soluble fiber are predominantly
responsible for its glycemic effect, since the hypoglycemic
effect can be reversed by the hydrolysis of guar gum or
following ultrahigh heating and homogenization (26). In addition, the intestinal absorption of carbohydrates was prolonged
by soluble DF, which was partially due to altered incretin
levels, including increased glucagonlike peptide 1 levels (32).
In experimental clamp studies, soluble DF also influenced
peripheral glucose uptake mechanisms (33,34), including
increasing skeletal muscle expression of the insulinresponsive
glucose transporter type 4 (GLUT4), which enhances skeletal
muscle uptake, augments insulin sensitivity and normalizes
blood glucose (34). In humans, various fatty acids stimulate
the expression of peroxisome proliferatoractivated receptor,
which increases adipocyte GLUT4 levels (35).
Measuring the levels of glycated proteins, including
hemoglobin A1c (HbA1c), GA and fructosamine, is the most
reliable method for assessing longterm glycemic control in
diabetic patients (36). Since glycation may occur throughout
the lifespan of hemoglobin and serum proteins, the level of
glycated proteins is able to reflect the degree of hyperglycemia during the lifespan of these factors (37). HbA1c, which
is the most widely used marker, can be used to quantify the
amount of circulating hemoglobin that has chemically reacted
with glucose, and reflects ambient blood glucose levels over
the previous 120 days and the preceding 30 days (38,39). Of
the various glycated proteins, serum GA has been identified as a useful and rapid indicator of glycemic control for
diabetic patients, as the turnover of serum albumin is markedly shorter, with a halflife of 17 days, as compared with
that of HbA1c (40). Circulating albumin is strongly glycated
on lysine 4 residues, and the glycation reaction occurs
10 times more rapidly than the glycation of hemoglobin (41).
Therefore, it is likely that glycemic fluctuations and excursions influence the glycation of albumin more directly than
hemoglobin. Inaba et al (42) have previously reported that
HbA1c quantification underestimates the longterm glycemic
control in dialysis patients with diabetes after comparing the
mean of random blood glucose concentrations, HbA1c, and
the percentage of GA (%GA). In addition, it was demonstrated
that the %GA assay provided a more accurate assessment of
glycemic control among Japanese hemodialysis patients. The
present study detected GA levels in patients, since the intervention period was only one month.

Cpeptide is a cleavage product of proinsulin that is


secreted by pancreatic cells in equimolar amounts together
with insulin (43). Although a considerable amount of insulin
is extracted by the liver, Cpeptide is subject to negligible
firstpass metabolism by the liver, thereby permitting its use
as a surrogate marker for endogenous insulin secretion (44).
Cpeptide is thought to be an inert byproduct of insulin
synthesis and has been of great value for elucidating the pathophysiology of type 1 and type 2 diabetes mellitus (45). Notably,
Cpeptide levels have previously been used as a biomarker of
cell function (46). The present study demonstrated that,
although soluble DF was able to significantly improve fasting
blood glucose, 2h blood glucose and GA levels, and the insulin
resistance index, it was unable to improve the levels of fasting
insulin, 2h insulin, fasting Cpeptide and 2h Cpeptide, thus
suggesting that soluble DF does not affect the secretory function of the islets of Langerhans when used for a short duration.
The reason for this remains unclear and will be the key focus
of our followup studies.
In order to confirm the safety of increased soluble DF
intake, the renal functions of all patients were assessed and
routine blood tests and urinalyses were performed (data
not shown). No significant adverse reactions were found,
with the exception of increased flatulence in some patients.
Furthermore, the results suggested that soluble DF was able to
significantly improve constipation and diarrhea in patients with
D2M and improve defecation ease and stool characteristics.
Notably, there were no significant differences in these effects
between the 10 and 20 g/day DF groups. Previous studies have
suggested that the effects of DF on metabolic and cardiovascular outcomes are associated with gastrointestinal function,
which may be reasonable considering the demonstrated links
between DF and satiation (47,48).
The present study demonstrated that high doses of DF were
able to improve numerous metabolic indicators in patients with
DM2; however, further research is required to determine the
specific mechanisms underlying the effects of DF. Such findings may have a large impact on the prevention and clinical
treatment of DM2.
In conclusion, the present study demonstrated that MNT
was able to improve 2h blood glucose and fasting insulin
levels, and the insulin resistance index, and was effective at
maintaining glycemic control. To the best of our knowledge,
the present study is the first to demonstrate that increased
intake of soluble DF over a shortduration in Chinese patients
with D2M was able to significantly improve blood glucose
levels and insulin resistance without affecting the secretory
functions of the islets of Langerhans. Therefore, the authors
of the present study recommend that dietary guidelines for
patients with D2M should stress the importance of increased
DF intake.
Acknowledgements
The present study was supported by the National Science and
Technology Support Program (grant no. 2009BAI80B04),
the Chongqing Science and Technology Commission
(grant no. CSTC, 2011AB5040), the 11th Fiveyear Plan
for the National Key Technology Research and Development
Program (grant no. 2008BAI58B06), and the Innovation

CHEN et al: EFFECTS OF DIETARY FIBER ON TYPE 2 DIABETES

Project of Chongqing Key Laboratory of Nutrition and Food


Safety (grant no. 2006CA1003).
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Nutr Res 36: 8089, 2016.

Dietary Fiber Intake Is Associated with HbA1c Level


among Prevalent Patients with Type 2 Diabetes in
Pudong New Area of Shanghai, China
Junyi Jiang1, Hua Qiu2, Genming Zhao1, Yi Zhou2, Zhijie Zhang1, Hong Zhang2, Qingwu Jiang1,
Qiao Sun2, Hongyan Wu2, Liming Yang2, Xiaonan Ruan2*, Wang-Hong Xu1*
1 Key Laboratory of Public Health Safety, Department of Epidemiology, School of Public Health, Ministry of Education, Fudan University, Shanghai, Peoples Republic of
China, 2 Pudong New Area Centers for Disease Control and Prevention, Shanghai, Peoples Republic of China

Abstract
Background: Dietary factors play an important role in glycemic control in diabetic patients. However, little is known about
their effects among Chinese diabetic patients, whose diets are typically abundant in fiber and high in glycemic index (GI)
values.
Methodology/Principal Findings: 934 patients with type 2 diabetes and 918 healthy volunteers from Pudong New Area,
Shanghai, China, were interviewed during the period of Oct-Dec, 2006 to elicit demographic characteristics and lifestyle
factors. Dietary habits were assessed using a validated food frequency questionnaire. Anthropometric measurements, biospecimen collection and biochemical assays were conducted at the interview according to a standard protocol. In this
population, diabetic patients consumed lower levels of energy and macronutrients but had higher levels of fasting plasma
glucose (FPG), glycolated hemoglobin A1c (HbA1c), triglyceride and body mass index than healthy adults. While the average
consumption levels of the nutrients among diabetic patients did not vary along duration of the disease, the average levels
of FPG and HbA1c increased with increasing duration. Regardless of diabetes duration, HbA1c level was observed lower in
patients having a higher fiber or lower GI intake. Compared with those with the lowest tertile intake of fiber, the adjusted
odds ratios (ORs) for poor glycemic control reduced from 0.75 (95%CI: 0.541.06) to 0.51 (95%CI: 0.340.75) with increasing
tertile intake (P for trend ,0.001).
Conclusions: Dietary fiber may play an important role in reducing HbA1c level. Increasing fiber intake may be an effective
approach to improve glycemic control among Chinese diabetic patients.
Citation: Jiang J, Qiu H, Zhao G, Zhou Y, Zhang Z, et al. (2012) Dietary Fiber Intake Is Associated with HbA1c Level among Prevalent Patients with Type 2 Diabetes
in Pudong New Area of Shanghai, China. PLoS ONE 7(10): e46552. doi:10.1371/journal.pone.0046552
Editor: Noel Christopher Barengo, Fundacion para la Prevencion y el Control de las Enfermedades Cronicas No Transmisibles en America Latina (FunPRECAL),
Argentina
Received March 13, 2012; Accepted September 5, 2012; Published October 16, 2012
Copyright: ! 2012 Jiang et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits
unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: This research was funded by Shanghai Municipal Health Bureau (08GWZX0201) and Academic Leaders Training Program of Pudong Health Bureau of
Shanghai (Grant No. PWRd2010-03). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing Interests: The authors have declared that no competing interests exist.
* E-mail: wanghong.xu@fudan.edu.cn (WX); ruan_118@hotmail.com (XR)

Chinese people consume more abundant types of foods, and


have higher levels of dietary fiber and GI intake comparing with
their western counterparts [9]. It is reported that average level of
total and soluble fiber intake in Chinese diabetic patients were
26.5 and 10.4 gram per day (g/d), respectively [10], above the
moderate amount of fiber intake recommended by the American
Diabetes Association (ADA) (total, 24 g/d; 8 g/d of soluble fiber
and 16 g/d of insoluble fiber) [11]. However, the status of
glycemic control and prevalence of complications in diabetic
patients in China have been not satisfactory [12].
To evaluate the association of dietary factors with diabetic
control status among Chinese patients with type 2 diabetes, we
conducted a cross-sectional study including 934 adult patients
from Pudong New Area of Shanghai, China. Our results may help
to better understand the role of dietary factors in the control of
type 2 diabetes.

Introduction
Type 2 diabetes is an important risk factor for micro-vascular
and macro-vascular complications. Effective control of hyperglycemia, dyslipidemia and hypertension, either by medication or by
lifestyle intervention, is crucial to decrease the incidence of stroke,
myocardial infarction and renal disease, as well as the related
premature death [1,2]. Intervention studies have examined the
impact of dietary intake on glycemic control, and found that
higher intake of dietary fiber [3,4] and lower intakes of dietary fat
[5], glycemic index (GI) [6] and carbohydrate [7] improved
glycemic control status. In the Nurses Health Study, He, et al [8]
observed a potential benefit of whole grain, cereal fiber and bran
intake in reducing mortality and cardiovascular risk in diabetic
patients. None of these studies, however, were conducted in
Chinese population.

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October 2012 | Volume 7 | Issue 10 | e46552

Dietary Fiber Intake and HbA1c Level

diet. We excluded from the analysis 3 women who had total


energy intake ,500 kcal/d or .3500 kcal/d and 5 men with
energy intake of ,800 kcal/d or .4000 kcal/d.

Materials and Methods


Study participants
In this cross-sectional design, a total of 979 adults diagnosed
with type 2 diabetes were randomly selected from the Diabetes
Administration Rosters in communities of Shanggang, Zhoujiadu,
Huamu, Puxin, Weifang, Jinyang, Meiyuan and Jichang of
Pudong New Area of Shanghai in Oct, 2006. All patients were
diagnosed with type 2 diabetes by doctors according to ADA
criteria: 1) fasting plasma glucose $7.0 mmol/L; or 2) two-hour
plasma glucose $11.1 mmol/L during an oral glucose tolerance
test; 75-g glucose load should be used; or 3) a random plasma
glucose concentration $11.1 mmol/L in persons with symptoms
of hyperglycemia or hyperglycemic crisis. Exclusion criteria
included the occurrence of a cardiovascular event during the
previous 6 months, advanced congestive heart failure, unstable
angina, major depression and dementia. Of the 934 patients
interviewed, 41.7% were male. The mean age of the participants
was 64.5 (SD, 10.1) years old.
At the same time, a total of 918 adult volunteers free of diabetes
were recruited from the spouses and neighbors of the diabetic
patients. The mean age of these volunteers was 57.7 (SD, 9.9)
years old, and 291(31.7%) were male.
The study was approved by Fudan University Institutional
Review Board (IRB00002408, FWA00002399). Written informed
consent was obtained from each participant before data collection.

Metabolic phenotype measurements


At the interview, each participant was measured for his/her
body height, weight, waist circumference, hip circumference,
systolic blood pressure (SBP), and diastolic blood pressure (DBP)
according to a uniform and standardized protocol. Body mass
index (BMI) was calculated as weight (kg) divided by height
squared (m2).
After at least 10 hours of overnight fasting, a 1,1.5 ml venous
blood specimen was collected in a vacuum tube containing sodium
fluoride for the measurement of plasma glucose and HbA1c, and a
3,3.5 ml non-anticoagulated venous blood specimen was collected simultaneously for the measurement of total cholesterol
(TC), triglyceride (TG), high density lipoprotein cholesterol
(HDLC) and low density lipoprotein cholesterol (LDLC).
Enzymology methods were used to measure the fasting plasma
glucose (FPG) level (GOD-PAP), concentrations of TG (GPOPAP) and TC (CHOD-PAP) on an Automatic Biochemical
Analyzer (HITACHI 7170A, Hitachi, Ltd, Tokyo, Japan). Levels
of HDLC and LDLC were measured using a selective inhibition
method. HbA1c was tested using ion exchange chromatography
on DS5 Glycated Hemoglobin Analyzer (DREW DS5, Drew
Scientific Co. Ltd, Cumbria, UK). Quality control of the assays
was assessed internally and externally. The inter-assay coefficient
of variation was ,1.82% for FPG (SD,0.23 mmol/L), ,1.38%
for TG (SD,0.02 mmol/L), ,1.54% for TC (SD,0.08 mmol/
L), ,1.6% for HDLC (SD,0.01 mmol/L), ,5.3% for LDLC
(SD,0.21 mmol/L), and 6.13% for HbA1c (SD,0.77).

Data collection
A structured in-person interview was conducted for each subject
by trained interviewers to collect information on demographic
characteristics, duration of diabetes, age at onset of diabetes,
diagnosis of hypertension, presence of dyslipidemia, use of tobacco
and alcohol. Presence of hypertension, dyslipidemia and coronary
heart disease were defined by a positive response to the question of
Have you ever been diagnosed with hypertension/dyslipidemia/
coronary heart disease by a doctor?. Family history of diabetes
was defined as positive if any first- or second-degree relative had
type 2 diabetes. Smoking was defined as at least 1 cigarette per day
for at least 6 months, and alcohol use was defined as drinking
alcohol at least 3 times a week for more than 6 months.
Dietary habit was assessed using an interviewer-administered
food frequency questionnaire (FFQ) modified based on a validated
FFQ [13]. The FFQ specifies 103 food items, covering 90% of
food items commonly consumed in Shanghai. For each food item,
participants were asked to report how frequently (daily, weekly,
monthly, annually or never) and how long (months per year) they
consumed the food, followed by a question on the amount of
consumption in liang (1 liang = 50 g) per unit of time in previous 12
months. For liquid foods such as milk, juice and beverage, the
amount of intake was reported in milliliter (ml) and was
transformed into gram in the analysis. The daily intakes of oil,
salt and sugar were calculated as the average level consumed by
each family member of the participant.
Nutrient content from the Chinese Food Composition Tables
was applied to estimate nutrient intake from all food items and
groups, and to obtain GI values for most food items [14]. For the
remaining food items, we referenced Foster-Powell et als report to
obtain their GI values [15]. Glycemic load (GL) from each food
was calculated by multiplying the foods GI value by the
carbohydrate content of the food and the average amount of the
food consumed per day. Total dietary GL was then produced by
summing these products over all food items. Dietary GI was
derived by dividing the dietary GL by the amount of carbohydrate
intake, thus yielding a weighted average GI for each individuals
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Statistical analysis
Statistical analyses were conducted utilizing SAS statistical
software 9.2 (SAS Institute Inc., Cary, NC). Differences on
demographic factors by diabetic status or glycemic control status
were evaluated using x2 test for categorical variables or nonparameter Wilcoxon test for continuous variables. Partial correlation analysis was conducted to evaluate the linear correlations of
HbA1c levels with amounts of dietary intake. A generalized linear
regression model was applied to compare the average levels of
biochemical measurements and average levels of dietary intake.
An unconditional logistic regression model was employed to
estimate the adjusted odds ratios (ORs) and 95% confident
intervals (CIs) of dietary intake with glycemic control status among
diabetic patients. Natural log transformation was applied to
normalize the distribution of biochemical measurements before
parametric methods were used in data analysis. All statistical tests
were based on two-sided probability.

Results
Compared with the recruited healthy volunteers, diabetic
patients were older and less educated, had more family history
of diabetes and higher prevalence of hypertension, dyslipidemia
and coronary heart disease (CHD), as shown in Table 1. Among
934 prevalent diabetic patients, 488 (52.3%) had an HbA1c level
of $7.0%. These patients, compared with those having an HbA1c
level of ,7.0%, appeared to have less education, younger age at
diagnosis of diabetes, longer duration of diabetes, lower prevalence
of hypertension and were more likely to use oral hypoglycemia
drug and insulin. No significant difference was observed between
the two groups with regard to age, sex, smoking, alcohol

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Dietary Fiber Intake and HbA1c Level

Table 1. Comparison of demographic characteristics of participants of the study.

Characteristics

Healthy adults
(N = 918)

Diabetic patients
(N = 934)
P value

Diabetic patients

P valuea

HbA1c,7.0% (N = 446)

HbA1c$7.0% (N = 488)

Age, years (mean, SD)

57.7 (9.9)

64.5 (10.1)

,0.001

64.6 (10.1)

64.4 (10.1)

0.825

Sex, male, n (%)

291 (31.7)

389 (41.7)

,0.001

191 (42.8)

198 (40.6)

0.487

Educational level, high school816 (88.9)


or below, n (%)

864 (92.5)

0.008

400 (89.9)

465 (94.9)

0.004

Family history of diabetes,


yes, n (%)

88 (9.6)

298 (31.9)

,0.001

130 (29.2)

168 (34.4)

0.084

Diagnosis age of DM, years


(mean, SD)

55.2 (10.4)

56.4 (10.4)

54.2 (10.0)

0.002

Duration of DM, years (mean,


SD)

9.2 (6.4)

8.2 (6.3)

10.2 (6.3)

,0.001

Prior history of hypertension, 293 (31.9)


n (%)

518 (55.5)

,0.001

265 (59.4)

253 (51.8)

0.020

Prior history of dyslipidemia, 61 (6.6)


n (%)

97 (10.4)

0.004

55 (12.3)

42 (8.6)

0.062

Prevalence of CHD, n (%)

132 (14.1)

,0.001

73 (16.4)

59 (12.1)

0.061

46 (5.0)

Current smoking, n (%)


Men

134 (46.1)

152 (39.1)

0.068

70 (36.7)

82 (41.4)

0.336

Women

6 (1.0)

5 (0.9)

0.944

2 (0.8)

3 (1.0)

1.000

Current alcohol consumption,


n (%)
Men

113 (33.8)

108 (27.8)

0.002

49 (25.7)

59 (29.8)

0.362

Women

21 (3.4)

10 (1.8)

0.108

5 (2.0)

5 (1.7)

1.000

Oral hypoglycemic drug use,


n (%)

762 (81.5)

341(76.5)

421(87.0)

,0.001

Insulin use, n (%)

88 (9.4)

31(7.0)

57(11.8)

0.012

Missing values (1 for age, education, diagnosis age of DM, duration of DM in diabetic patients; 1 for current alcohol consumption in healthy adults; 4 for oral
hypoglycemic drug use and insulin use) were excluded;
a 2
x test for categorical variables or non parameter Wilcoxon test for continuous variables.
doi:10.1371/journal.pone.0046552.t001

consumption, family history of diabetes, presence of dyslipidemia


and prior history of CHD.
As shown in Table 2, the diabetic patients, both men and
women, seemed to remain a stable dietary habit along duration of
diabetes (P.0.05 for all tests). These patients, either with a short
or a long duration of type 2 diabetes, had lower levels of energy,
carbohydrate, protein, and fat intake than did healthy volunteers
after adjusting for age and other potential confounders (P,0.01).
Dietary fiber (soluble only), GI and GL intake were also lower in
diabetic patients than in healthy volunteers, but the difference
reached significance for GI and GL only among women.
Presented in Table 3 was the comparison of average levels of
metabolic indicators by diabetic status and by duration of type 2
diabetes. After adjustment of age and sex, higher levels of FPG,
HbA1c, TG and BMI and a lower level of LDLC were observed
among diabetic patients than in healthy adults. Among diabetic
patients, the average levels of FPG, HbA1c increased and BMI
decreased with increasing duration of the disease after adjusting
for age, sex, oral hypoglycemic drug use and insulin use (P for
trend ,0.05). No significant upward trend was observed for
average levels of TC, TG, LDLC and HDLC along with duration
of the disease.
In diabetic patients, HbA1c level was negatively correlated with
dietary fiber intake (r = 20.079, p = 0.017), and positively with
dietary GI intake (r = 0.070, p = 0.034) after adjusting for age, sex,
oral hypoglycemic drug use and insulin use. No significant linear
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correlation was observed for HbA1c level with other nutrients


(data not shown). Therefore, we further compared the average
levels of HbA1c by dietary fiber and GI intake among diabetic
patients (Figure 1). Regardless of duration of type 2 diabetes,
HbA1c level was consistently higher in patients consuming lower
level of fiber. HbA1c level was also higher among patients having
higher GI intake, but the difference did not reach significance.
We further evaluated the associations of dietary factors with
glycemic control status which was defined poor as HbA1c
$7.0% (Table 4). Compared with the patients having the lowest
tertile intake of dietary fiber, the adjusted ORs for poor glycemic
control decreased from 0.75 (95%CI: 0.541.06) for those having
medium intake to 0.51 (95%CI: 0.340.75) for those with the
highest tertile intake (P for trend ,0.001). No significant
association was observed for other dietary factors.

Discussion
In this cross-sectional study including 934 Chinese prevalent
patients with type 2 diabetes from Pudong New Area of Shanghai,
China, we observed a stable after-diagnosis dietary habit, upward
trend of HbA1c level along with duration of diabetes, a lower
average level of HbA1c related with higher fiber intake, and a
probably protective effect of dietary fiber on glycemic control
status. Our findings have several implications in improving

October 2012 | Volume 7 | Issue 10 | e46552

Dietary Fiber Intake and HbA1c Level

Table 2. Average levels of dietary intake by diabetic status and duration of type 2 diabetes.

Dietary factors (Mean, SD)

Diabetic
Healthy adults patients
(N = 918)
(N = 934)

P valueb

Diabetic patients, duration of DM, years


,5 (N = 230)

59 (N = 316)

$10 (N = 387)

P valuec

Men
Energy, kcal/d

1931.2 (1.4)

1644.1 (1.3)

,0.001

1740.8 (1.3)

1600.0 (1.3)

1615.5 (1.3)

0.225

Carbohydrate, g/d

323.6 (1.4)

268.2 (1.3)

0.003

282.5 (1.3)

263.9 (1.3)

261.6 (1.3)

0.583

Protein, g/d

68.9 (1.4)

61.5 (1.5)

0.003

65.1 (1.5)

58.3 (1.4)

62.0 (1.4)

0.467

Fiber, g/d

10.2 (1.6)

9.2 (1.7)

0.232

9.9 (1.6)

8.4 (1.6)

9.6 (1.7)

0.045

Fat, g/d

40.9 (1.6)

37.1 (1.6)

0.002

40.0 (1.5)

35.3 (1.6)

36.9 (1.6)

0.485

Average GI

61.5 (1.1)

60.4 (1.2)

0.323

61.0 (1.2)

61.4 (1.1)

59.2 (1.2)

0.230

Average GL

104.7 (1.4)

87.6 (1.4)

0.347

93.3 (1.4)

84.0 (1.4)

86.5 (1.4)

0.670

Energy, kcal/d

1695.2 (1.3)

1410.5 (1.3)

,0.001

1445.2 (1.4)

1438.3 (1.4)

1367.4 (1.3)

0.438

Carbohydrate, g/d

279.2 (1.3)

226.3 (1.4)

,0.001

234.0 (1.4)

231.4 (1.4)

217.9 (1.4)

0.878

Protein, g/d

61.8 (1.4)

52.9 (1.5)

,0.001

54.3 (1.5)

53.7 (1.5)

51.2 (1.5)

0.973

Fiber, g/d

10.2 (1.6)

8.5 (1.7)

0.460

8.8 (1.7)

8.4 (1.7)

8.3 (1.7)

0.868

Fat, g/d

38.4 (1.6)

33.4 (1.6)

,0.001

33.5 (1.6)

33.8 (1.7)

32.9 (1.5)

0.797

Average GI

59.9 (1.1)

59.2 (1.2)

,0.001

59.3 (1.1)

59.6 (1.2)

58.7 (1.2)

0.733

Average GL

92.1 (1.4)

74.2 (1.4)

,0.001

76.8 (1.4)

75.7 (1.4)

71.5 (1.4)

0.783

Women

Continuous variables were all natural LOG transformed before entering models;
Generalized linear model adjusting for age, BMI and energy intake;
c
Generalized linear model adjusting for age, BMI, oral hypoglycemic drug use, insulin use and energy intake.
doi:10.1371/journal.pone.0046552.t002
b

Secondly, the significant difference in dietary habit between


patients and healthy adults suggests that a diabetic patient could
greatly change his/her dietary habit just due to diagnosis of type 2
diabetes. The stable dietary habit along the duration of the disease
in patients, on the other hand, indicates that a new dietary habit,
once established, would remain unchanged for a long time. These
results implicate the importance of the time point of diagnosis in
establishing a new good dietary habit. Dietary intervention and
health education should be extensively elicited at the time point.

diabetic control status and preventing complications among


Chinese diabetic patients.
Firstly, in this study, the patients with an HbA1c level of $7.0%
were diagnosed with type 2 diabetes 2.2 years earlier than those
with a lower HbA1c level, and had a 2 years longer duration of the
disease. The result is consistent with several previous studies, in
which younger age at diagnosis and longer duration were regarded
as independent predictors for poor glycemic control in diabetic
patients [1618]. The result suggests that more attention in
glycemic control should be paid to the younger patients.

Table 3. Average levels of metabolic indicators by diabetic status and duration of type 2 diabetes.

Indicatorsa (Mean, SD)

Diabetic
Healthy adultspatients

P valueb

Diabetic patients, duration of DM, years

P valuec

,5 (N = 230)

59 (N = 316) .9 (N = 387)

,0.001

7.2 (1.3)

8.1 (1.4)

8.5 (1.4)

,0.001

,0.001

6.9 (1.2)

7.4 (1.2)

7.7 (1.2)

,0.001

4.4 (1.2)

0.003

4.4 (1.2)

4.4 (1.2)

4.4 (1.2)

0.733

1.3 (1.7)

1.4 (1.8)

,0.001

1.5 (1.8)

1.4 (1.7)

1.4 (1.8)

0.508

2.8 (1.3)

2.7 (1.4)

,0.001

2.7 (1.4)

2.7 (1.3)

2.7 (1.4)

0.177

(N = 918)

(N = 934)

FPG, mmol/L

5.3 (1.2)

8.0 (1.4)

HbA1c (%)

5.9 (1.1)

7.4 (1.2)

TC, mmol/L

4.5 (1.2)

TG, mmol/L
LDLC, mmol/L
HDLC, mmol/L
Men

1.1 (1.3)

1.1 (1.2)

0.998

1.1 (1.2)

1.1 (1.1)

1.2 (1.1)

0.111

Women

1.3 (1.3)

1.3 (1.3)

0.224

1.3 (1.3)

1.3 (1.2)

1.3 (1.3)

0.266

24.8 (1.1)

25.6 (1.1)

0.005

25.8 (1.2)

25.7 (1.1)

24.8 (1.1)

0.002

BMI
a

Continuous variables were all natural LOG transformed before entering models;
Generalized linear model adjusting for age and gender;
Generalized linear model adjusting for age, gender, oral hypoglycemic drug use and insulin use.
doi:10.1371/journal.pone.0046552.t003

b
c

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Dietary Fiber Intake and HbA1c Level

Figure 1. Average levels of HbA1c by duration of type 2 diabetes and dietary fiber or GI intake. The low and high fiber or GI intakes were
classified by the medians of consumption in men and women, respectively. Means of HbA1c level were adjusted for age (as a continuous variable),
sex (male/female), duration of type 2 diabetes (as a continuous variable), BMI (as a continuous variable), oral hypoglycemic drug use (yes/no), insulin
use (yes/no) and energy intake (as a continuous variable).
doi:10.1371/journal.pone.0046552.g001

fiber intake. Whereas Haimoto, et al [7] found that a 6-month low


carbohydrate diet (30% of energy intake from carbohydrate)
decreased HbA1c level from 10.9% to 7.4% among 33 severe
diabetic outpatients, Wolever, et al [22] did not observe a
beneficial effect of a low-carbohydrate diet in glycemic status.
The null associations of carbohydrate and GL intake with HbA1c
level in our patients indicate that the two dietary factors play a
limited role in glycemic control in our population.
In this study, we did not find an association of HbA1c levels
with dietary protein intake, consistent with Larsen et als results
[28], but not with Pearce et als findings [29]. The null association
with dietary fat is also inconsistent with a randomized clinical trial,
in which both a low-fat vegan diet and a traditional diet according
to the ADA guidelines decreased HbA1c level in 99 individuals
with type 2 diabetes after a 22-week follow up [5].
Finally, we observed that HbA1c level was consistently
associated with dietary fiber intake regardless of duration of the
disease, suggesting that dietary intervention may make a difference
at any time during the progression of the disease.
The strengths of this study included the validated food
frequency questionnaire, a standardized protocol for body
measurements, and stringent quality control in lab assays. Due
to the nature of the cross-sectional design, however, we could not
elucidate the role of dietary factors in glycemic control. Moreover,
the amount of energy intake appeared lower than those reported
in previous studies [30], raising our concern on possible recall bias.
However, the potential underestimation of dietary intake, if any,
would result in a non-differential misclassification bias, which may
have biased our results towards the null.
In summary, this small-scale cross-sectional study indicates the
potential role of dietary fiber in glycemic control. Our results, if
confirmed, may have clinic and public health implications in
diabetic control among Chinese adults.

In both healthy and diabetic subjects of this study, the average


levels of dietary fiber intake reached moderate amount of fiber
intake recommended by ADA. In this population with high
average level of dietary fiber intake, dietary fiber was still linked to
better glycemic control status, supporting the beneficial effect of
dietary fiber on the control of type 2 diabetes. We also find that, it
was GI, but not carbohydrate or GL intake, that was correlated
with HbA1c level. The results indicate that the quality of the
carbohydrates consumed may play a more important role than the
quantity of the macronutrient in the control of type 2 diabetes.
Dietary GI and GL are two physiological indexes of the metabolic
effects of dietary carbohydrates [15,19]. While GI is used to
characterize foods that contain carbohydrates according to their
postprandial blood glucose response and hence their effect on
blood insulin levels [19,20], GL is introduced to quantify the
overall estimate of postprandial glycemia by combining the GI
value and the quantity of carbohydrates consumed [15,20]. Our
finding of the improved glycemic control status related to dietary
fiber intake is consistent with the previous studies [4,6,21]. The
insignificant adverse effect of GI intake, on the other hand, was
supported only by Wolever et als report [22], but not consistent
with most previous studies in which a low-GI diet significantly
improved glycemic control by reducing HbA1c levels among
diabetic patients [6,2325]. It is of note that, even if it effected on
glucose metabolism, a low-GI diet was not a practical intervention
tool in controlling diabetes [26]. Increasing dietary fiber intake
may be an effective approach.
Regarding the role of carbohydrate and GL intake, the results
have been controversial. While Lau, et al [27] reported that the
inverse association of carbohydrate and daily GL intake with
HOMA-IR can be explained by dietary fiber, Esposito, et al [25]
found that diet high in GL was significantly associated with higher
HbA1c and postmeal glucose levels in a dose-dependent manner
among 901 diabetic outpatients even after adjusting for dietary
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October 2012 | Volume 7 | Issue 10 | e46552

Dietary Fiber Intake and HbA1c Level

Table 4. Associations of dietary intake with glycemic control status among diabetic patients.

Dietary intakea

HbA1c, % (Mean,
Glycemic control status, N (%)
SD)
Controlled (HbA1c,7.0%)

OR (95%CI)b

P for trend

Uncontrolled (HbA1c$7.0%)

Energy (kcal/d)
Low

7.5 (1.4)

143 (32.2)

165 (34.2)

1.00

Medium

7.6 (1.7)

139 (31.3)

170 (35.3)

1.03 (0.74, 1.44)

High

7.5 (1.7)

162 (36.5)

147 (30.5)

0.93 (0.71, 1.22)

Low

7.6 (1.5)

137 (30.9)

171 (35.5)

1.00

Medium

7.5 (1.6)

147 (33.1)

163 (33.8)

0.85 (0.59, 1.23)

High

7.5 (1.8)

160 (36.0)

148 (30.7)

0.69 (0.40, 1.16)

0.300

Carbohydrate (g/d)

0.166

Protein (g/d)
Low

7.6 (1.5)

135 (30.4)

172 (35.7)

1.00

Medium

7.5 (1.6)

151 (34.0)

159 (33.0)

0.75 (0.52, 1.08)

High

7.5 (1.8)

158 (35.6)

151 (31.3)

0.62 (0.38, 1.01)

0.052

Fiber (g/d)
Low

7.7 (1.5)

126 (28.4)

182 (37.8)

1.00

Medium

7.5 (1.5)

148 (33.3)

162 (33.6)

0.75 (0.54, 1.06)

High

7.4 (1.8)

170 (38.3)

138 (28.6)

0.51 (0.34, 0.75)

,0.001

Fat (g/d)
Low

7.5 (1.5)

139 (31.3)

168 (34.9)

1.00

Medium

7.4 (1.6)

167 (37.6)

144 (29.9)

0.72 (0.51, 1.02)

High

7.7 (1.8)

138 (31.1)

170 (35.3)

1.16 (0.76, 1.77)

0.630

Average GI
Low

7.5 (1.6)

145 (32.7)

163 (33.8)

1.00

Medium

7.4 (1.7)

165 (37.2)

144 (29.9)

0.88 (0.64, 1.23)

High

7.7 (1.6)

134 (30.2)

175 (36.3)

1.25 (0.90, 1.75)

0.184

Average GL
Low

7.6 (1.6)

141 (31.8)

166 (34.4)

1.00

Medium

7.6 (1.6)

139 (31.3)

172 (35.7)

1.00 (0.70, 1.45)

High

7.5 (1.7)

164 (36.9)

144 (29.9)

0.68 (0.41, 1.12)

0.154

a
Dietary factors were classified as low, medium and high intake by the tertiles in men and in women, respectively. The cut points for energy intake were 1444.06 and
1842.84 kcal/d in men and 1268.88 and 1623.31 kcal/d in women; for carbohydrate were 248.93 and 295.77 g/d in men and 205.85 and 267.65 g/d in women; for
protein intake were 50.89 and 72.42 g/d in men and 44.88 and 62.71 g/d in women; for fiber intake were 7.12 and 11.32 g/d in men and 6.73 and 10.51 g/d in women;
for fat were 31.02 and 44.62 g/d in men and 28.74 and 40.61 g/d in women; for average GI were 56.53 and 64.58 units/d in men and 55.88 and 62.95 units/d in women;
for average GL were 65.57 and 99.67 units/d in men and 76.34 and 87.55units/d in women.
b
OR, odds ratio; 95%CI, 95% confidence interval; OR: adjusted for age (as a continuous variable), sex (male/female), duration of type 2 diabetes (as a continuous
variable), BMI (as a continuous variable), oral hypoglycemic drug use (yes/no), insulin use (yes/no) and energy intake (as a continuous variable).
doi:10.1371/journal.pone.0046552.t004

Acknowledgments

Author Contributions

The authors are grateful to the study participants and research staff from
Community Health Centers in Pudong New Area of Shanghai, China.

Conceived and designed the experiments: XR WX. Performed the


experiments: HQ YZ HZ HW LY. Analyzed the data: JJ ZZ WX.
Contributed reagents/materials/analysis tools: XR HQ HZ. Wrote the
paper: JJ WX. Revision of the manuscript: GZ QJ QS.

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