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Epidemiology/Health Services Research

O R I G I N A L A R T I C L E

Supervised Exercise Program, BMI, and


Risk of Type 2 Diabetes in Subjects With
Normal or Impaired Fasting Glucose
JEY SOOK CHAE, PHD1,2 MINJOO KIM, BS2,3 ameliorating risk factors associated with
RYUNGWOO KANG, MS2,3 JI WON PARK, BS2 this disease. These lifestyle interventions,
JUNG HYUN KWAK, PHD1,2 JUSTIN Y. JEON, PHD5 which generally included both physical ac-
JEAN KYUNG PAIK, PHD1,2 JONG HO LEE, PHD1,2,3 tivity and nutritional interventions, have
OH YOEN KIM, PHD4
been highly successful in preventing the
onset of type 2 diabetes. Studies that failed
to show improved glycemic control
OBJECTIVEdTo determine the association of regular exercise, BMI, and fasting glucose with
the risk of type 2 diabetes and to predict the risk.
typically reported poor exercise compli-
ance (11) or low-intensity exercise (12).
RESEARCH DESIGN AND METHODSdKorean subjects (n = 7,233; 4079 years old) However, most physical activity inter-
who were not diagnosed with diabetes at baseline were enrolled through the National Health vention studies focused on English
Insurance Corporation. All participants underwent biennial examinations, and 1,947 of 7,233 speakers. Additional studies are needed
subjects also underwent a 6-month program of moderate-intensity exercise (300 min/week) to characterize ethnic and/or cultural
without dietary advice. differences in the risk of type 2 diabetes
RESULTSdDuring follow-up (mean = 2 years), there were 303 incidents of type 2 diabetes in because most studies show lower physical
the nonexercise program group (n = 5,286) and 83 in the exercise program group (n = 1,947). activity levels in nonwhite compared
After adjusting for confounders, the risk of type 2 diabetes was positively associated with BMI and with white populations (13). Accord-
inversely with regular exercise, especially among overweight/obese subjects. After further ad- ingly, tailor-made interventions that
justment for BMI, the odds ratios for risk of diabetes associated without and with regular exercise take into account the different needs of
were 1.00 and 0.77, respectively. Among subjects with normal fasting glucose, exercise reduced various groups (e.g., language and cul-
the diabetes risk; however, among those with impaired fasting glucose (IFG), the protective effect ture) should be developed and evaluated.
of exercise was found only among overweight/obese subjects. The overweight/obese subjects in In this prospective cohort study, we eval-
the exercise program group exhibited improved fasting glucose compared with the nonexercise uated the association of regular exercise,
program group and showed 1.5 kg of weight loss and a 3-cm decrease in waist circumference.
Among overweight/obese subjects with unchanged fasting glucose, weight loss was greater in the
BMI, and glucose levels with the risk of
exercise program group. type 2 diabetes in a Korean population.
The exercise program was prescribed
CONCLUSIONSdRegular exercise reduces the risk of type 2 diabetes in overweight/obese and delivered by qualied health profes-
individuals. Particularly, regular exercise and weight or waist circumference control are critical sionals.
factors for preventing diabetes in overweight/obese individuals with IFG.

Diabetes Care 35:16801685, 2012 RESEARCH DESIGN AND


METHODS

T
he benets of exercise in preventing (13). Regular exercise is therefore a key
and treating type 2 diabetes are widely strategy in diabetes prevention. A number Study population
recognized (1). Exercise improves of large-scale, randomized, controlled trials This 2-year, prospective cohort study
glycemic control, body composition, car- have been performed to evaluate the effect included 7,233 Korean subjects (4079
diorespiratory tness, cardiovascular risk, of lifestyle modication in prediabetic pop- years old) who underwent biennial medical
physical functioning, and well-being in pa- ulations (410), with the aim of reducing evaluations through the National Health
tients with type 2 diabetes or prediabetes the incidence of type 2 diabetes and Insurance Corporation (NHIC) (2007
2011). Major exclusion criteria included a
c c c c c c c c c c c c c c c c c c c c c c c c c c c c c c c c c c c c c c c c c c c c c c c c c diagnosis of diabetes or use of medications
known to impair glucose tolerance. The
From the 1Yonsei University Research Institute of Science for Aging, Yonsei University, Seoul, Korea; the
2
Department of Food and Nutrition, College of Human Ecology, National Research Laboratory of Clinical procedure and results of screening, recruit-
Nutrigenetics/Nutrigenomics, Yonsei University, Seoul, Korea; the 3Department of Food and Nutrition, ment, and classication of the study sub-
Brain Korea 21 Project, College of Human Ecology, Yonsei University, Seoul, Korea; the 4Department jects are shown in the owchart
of Food Science and Nutrition, College of Human Ecology, Dong-A University, Busan, Korea; and the (Supplementary Fig. 1). A total of 21,673
5
Department of Sport and Leisure, Yonsei University, Seoul, Korea.
Corresponding author: Jong Ho Lee, jhleeb@yonsei.ac.kr.
subjects underwent both basal and biennial
Received 28 October 2011 and accepted 14 March 2012. medical evaluations between 2007 and
DOI: 10.2337/dc11-2074 2011. Type 2 diabetes was not detected in
This article contains Supplementary Data online at http://care.diabetesjournals.org/lookup/suppl/doi:10 7,576 subjects (35.0%), and they were sub-
.2337/dc11-2074/-/DC1. divided into the exercise (n = 2,290) and
J.S.C. and R.K. contributed equally to this work as primary authors.
2012 by the American Diabetes Association. Readers may use this article as long as the work is properly nonexercise (n = 5,286) program groups.
cited, the use is educational and not for prot, and the work is not altered. See http://creativecommons.org/ Among the exercise program group, 1,947
licenses/by-nc-nd/3.0/ for details. subjects met the requirements of the

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Chae and Associates

exercise program. At any period during Data collection: anthropometric periods (72 times/6 months). All subjects
the 2-year study, 1,947 of the subjects and biochemical parameters who were afliated with the exercise pro-
participated in a 6-month exercise pro- The NHIC biennial examinations per- gram group underwent a 6-month program
gram provided by the Health Promotion formed by the medical staff at local hospitals of moderate-intensity exercise (300 min/
Center of the NHIC that consisted of 300 follow a standard procedure. Participants week) without dietary advice. Almost all of
min/week of moderate-intensity exercise were asked 1) to describe health habits, the basal physical tness test characteristics
without specic dietary advice. The re- including cigarette smoking and alcohol in the exercise program group (hand-grip
maining 5,286 subjects underwent the consumption and 2) whether they were strength measurement, sit-up test, standing
biennial examinations only. At the end treated for diabetes, and the date of diag- on one leg with eyes closed test, and trunk
of the 2-year study, participants were nosis if they answered yes. Anthropometric exion forward test) were improved at the
subdivided into groups according to fast- and biochemical measurements included end of the 2-year study (Supplementary Ta-
ing glucose levels: normal fasting glucose BMI, waist circumference, and blood pres- ble 1). Clinical characteristics of participants
(NFG), impaired fasting glucose (IFG), sure. Serum glucose and lipid proles (tri- at baseline and at the 2-year follow-up are
and type 2 or new-onset diabetes based glycerides and total, LDL, and HDL shown in Table 1. No signicant differences
on the biennial medical evaluation cholesterol) were measured after fasting. were found between the two groups (ex-
results. New-onset diabetes was dened ercise vs. nonexercise program group) in
as diagnosed (i.e., use of antidiabetic Statistical analyses sex distribution, age, BMI, blood pressure,
medication) or undiagnosed (American Each participants fasting glucose status and serum glucose at baseline. However,
Diabetes Association criteria of fasting glu- was classied as NFG, IFG, or type 2 di- the exercise program group had lower
cose $126 mg/dL [7.0 mmol/L]). IFG was abetes based on results of the biennial ex- proportions of current smokers, current
dened as a fasting glucose level of 100 aminations. At the end of the study, any drinkers, and antihypertensive drug users
126 mg/dL (5.556.99 mmol/L) and NFG changes from baseline were categorized as compared with the nonexercise program
as a fasting glucose level ,100 mg/dL (5.55 improvement (IFG to NFG), no change group. Mean total cholesterol level at base-
mmol/L). Written informed consent was (NFG to NFG and IFG to IFG), or deteri- line was slightly but signicantly higher in
obtained from all participants before oration (NFG to IFG and NFG/IFG to di- the exercise program group after adjusting
screening, consistent with the Helsinki abetes); the last two categories (i.e., NFG/ for smoking, drinking, and antihyperten-
Declaration. IFG to diabetes) were combined because sive drug use.
of small numbers in the NFG-to-diabetes At the end of the 2-year study, the
Exercise program category (14). nonexercise program group showed sig-
The exercise program was prescribed and Statistical analyses were performed us- nicantly increased fasting glucose and
delivered by qualied health professio- ing SPSS version 12.0 for Windows (SPSS total cholesterol levels, but decreased
nals. All subjects who volunteered to Inc., Chicago, IL). Frequency was analyzed blood pressure. The exercise program
participate in the exercise program were by x2 test. Differences in clinical variables group also showed signicantly increased
screened for eligibility through question- between groups (exercise vs. nonexercise fasting glucose levels, but decreased BMI,
naires and the basic medical examination program group) were evaluated by inde- waist circumference, and blood pressure.
before enrollment. Based on the screening pendent Student t test, and a general linear After adjusting for baseline values, changes
result, eligible participants underwent a model test was used to adjust for baseline in BMI, waist circumference, and blood
physical tness test that included a hand- values or smoking/drinking status and an- pressure were signicantly lower in the
grip strength measurement and sit-up test tihypertensive drug use. A paired Student exercise program group compared with the
for muscular strength, a standing on one t test was used to evaluate the effects of the nonexercise program group. At the 2-year
leg with eyes closed test for balance, and exercise program. After adjusting for con- follow-up, BMI and blood pressure were
the use of a cycle ergometer for testing founding factors, the association of type 2 lower in the exercise program group than
cardiorespiratory endurance. After the diabetes with exercise, BMI, and fasting glu- the nonexercise program group after ad-
baseline anthropometric and tness mea- cose concentrations was evaluated using a justing for smoking, drinking, and antihy-
surement, the exercise physiologist pre- logistic regression model to estimate odds pertensive drug use (Table 1).
scribed a personalized program (i.e., ratios (ORs) (95% CIs). Logistic regression
exercise type, intensity, and frequency) analysis was used to determine the relation- Association between type 2
to each person. Intensity of aerobic exer- ship between IFG and type 2 diabetes status diabetes and exercise, BMI, and
cise ranged between an initial exercise and participation in an exercise program. fasting glucose
intensity of 65% heart rate maximum to, Continuous variables were expressed as During a mean follow-up period of 2 years,
and upward of, 85% heart rate maximum. mean 6 SE, and categorical variables were there were 303 incident cases of type 2
Intensity of resistance exercise was 50% of expressed as absolute numbers and percen- diabetes in the nonexercise program group
one repetitive maximum value and trained tages. A two-tailed value of P , 0.05 was and 83 in the exercise program group
in one set (1215 repetitions). Exercise fre- considered signicant. (Table 2). The risk of type 2 diabetes after
quency was three times per week for 6 adjusting for confounding factors (age, sex,
months. The programs were performed RESULTS smoking/drinking status, systolic and dia-
for 6 months and consisted of warm-up stolic blood pressure, total cholesterol, and
(1015 min), aerobic (2530 min; e.g., Clinical characteristics at baseline antihypertensive drug use) signicantly de-
treadmill or cycling), resistance (1015 and 2-year follow-up creased with regular exercise. After further
min; e.g., bench press, arm curl, bent-knee We measured compliance to the exercise adjustment for BMI, the ORs for risk of di-
sit-up, etc.), and cool-down (1015 min; program and only included subjects that abetes associated without and with regular
general relaxation and stretching) exercises. attended at least 60 of the intervention exercise were 1.00 and 0.77, respectively

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Effect of exercise and BMI on type 2 diabetes

Table 1dParticipant characteristics at baseline and at the end of the 2-year study

Nonexercise program Exercise program


group (n = 5,286) Pa group (n = 1,947) Pa Pb Pc
Male/female (n, %) 796/4,490 (15.1/84.9) 294/1,653 (15.1/84.9) 0.970
Age (years) 56.0 6 0.09 56.0 6 0.14 0.872
Current smokers, n (%) 257 (4.9) 45 (2.3) ,0.001
Current drinkers, n (%) 1,037 (19.6) 315 (16.2) 0.001
Antihypertensive drug, n (%) 2,132 (40.3) 701 (36.0) 0.001
BMI (kg/m2)
Baseline 25.0 6 0.04 25.0 6 0.06 0.406
Follow-up 25.0 6 0.04 24.7 6 0.06 0.013
Change 20.02 6 0.02 0.271 20.26 6 0.03 ,0.001 ,0.001 ,0.001
Waist circumference (cm)
Baseline 81.0 6 0.17 81.1 6 0.26 0.113
Follow-up 80.9 6 0.17 80.2 6 0.26 0.373
Change 20.11 6 0.12 0.374 20.87 6 0.18 ,0.001 0.001 ,0.001
Blood pressure (mmHg)
Systolic blood pressure
Baseline 125.3 6 0.23 124.8 6 0.34 0.940
Follow-up 124.9 6 0.22 123.0 6 0.30 ,0.001
Change 20.46 6 0.23 0.049 21.83 6 0.34 ,0.001 0.001 ,0.001
Diastolic blood pressure
Baseline 77.7 6 0.15 77.3 6 0.23 0.622
Follow-up 77.2 6 0.14 76.2 6 0.21 0.003
Change 20.46 6 0.15 0.003 21.04 6 0.24 ,0.001 0.027 0.001
Glucose (mg/dL)
Baseline 93.0 6 0.16 92.7 6 0.24 0.610
Follow-up 96.1 6 0.20 95.3 6 0.32 0.150
Change 3.09 6 0.20 ,0.001 2.58 6 0.31 ,0.001 0.297 0.063
Total cholesterol (mg/dL)
Baseline 204.4 6 0.51 206.7 6 0.88 0.034
Follow-up 205.8 6 0.52 205.5 6 0.87 0.527
Change 1.48 6 0.52 0.005 21.24 6 0.83 0.135 0.005 0.074
Data are mean 6 SE unless otherwise indicated. P values derived from paired Student t test. P values derived from general linear model after adjusting for smoking,
a b

drinking, and antihypertensive drug. cP values derived from general linear model after adjusting for baseline values.

(P = 0.038 for trend). Overweight/obesity diabetes after adjusting for confounding fasting glucose (from IFG to NFG) during
was associated with a 1.80-fold increased factors is shown in Supplementary Fig. 3. the 2-year study in the exercise program
risk for type 2 diabetes compared with nor- Among subjects with NFG, BMI was pos- group, although body weight fell by about
mal weight after adjusting for confounding itively associated with the protective effect 1.5 kg and waist circumference by 3 cm
factors and exercise (P , 0.001 for trend). of exercise. However, among those with (Fig. 1). Among overweight/obese subjects
Subjects with IFG showed a 5.98-fold IFG, the protective effect of exercise was whose fasting glucose status did not change,
higher risk of developing type 2 diabetes only found in overweight/obese subjects. weight loss was greater in the exercise
than subjects with NFG after adjustment Compared with normal-weight subjects program group. Among normal-weight
for all covariates (P , 0.001 for trend). with NFG in the exercise program group, subjects with unchanged NFG status, re-
In subgroup analyses based on BMI overweight/obese subjects with IFG in ductions in body weight and waist circum-
(,25 and $25 kg/m2) (Supplementary the nonexercise program group showed ference were signicantly greater in the
Fig. 2A), the inverse association between a 16.3-fold higher risk of developing exercise program group.
exercise and risk of type 2 diabetes was type 2 diabetes. The relative effect of obe-
stronger for overweight/obese subjects. sity and exercise on diabetes risk was Regular exercise as an independent
The inverse association between exercise larger among subjects with NFG, but the predictor of IFG and type 2 diabetes
and risk for type 2 diabetes persisted in absolute effect was larger among subjects Based on these results, we performed
subgroup analyses based on glucose levels with IFG. logistic regression analysis to determine
(NFG and IFG) (Supplementary Fig. 2B). independent predictors of IFG and type 2
The positive association between BMI and Mean changes in body weight and diabetes (Table 3). Age, baseline BMI, 4
risk of type 2 diabetes was conrmed in waist circumference according to weight, baseline waist circumference, 4
subjects with NFG and IFG (Supplemen- fasting glucose level change, waist circumference, exercise, baseline glu-
tary Fig. 2C). exercise, and BMI cose level, baseline blood pressure (diastolic
The joint association of exercise, BMI, Among overweight/obese subjects, signif- and systolic), 4 blood pressure (diastolic
and glucose levels with the risk of type 2 icantly fewer subjects showed improved and systolic), baseline total cholesterol, and

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Table 2dAssociation between type 2 diabetes and exercise, BMI, and fasting glucose concentration

New cases of type 2 OR (95% CI)


diabetes, n (%) Subjects (n) Model 1* Model 2 Model 3
Exercise program
No exercise program 303 (5.7) 5,286 1.00 1.00 1.00
Exercise program 83 (4.3) 1,947 0.73 (0.570.94) 0.76 (0.590.98) 0.77 (0.601.00)
P value 0.014 0.036 0.038
BMI (kg/m2)
,25 132 (3.6) 3,631 1.00 1.00 1.00
$25 254 (7.1) 3,602 2.01 (1.622.50) 1.80 (1.442.24) 1.80 (1.452.24)
P value ,0.001 ,0.001 ,0.001
Fasting glucose level
Normal (,100 mg/dL) 124 (2.3) 5,356 1.00 1.00 1.00x
Impaired ($100 mg/dL) 262 (14.0) 1,877 6.85 (5.498.54) 6.30 (5.047.89) 5.98 (4.777.48)
P value ,0.001 ,0.001 ,0.001
*Unadjusted. Adjusted for age, sex, smoking and drinking status, systolic and diastolic blood pressure, total cholesterol, and antihypertensive drug use. Adjusted
also for BMI. Adjusted also for exercise program. xAdjusted also for BMI and exercise program.

4 total cholesterol were evaluated. Regular with known risk factors for IFG and level, P , 0.001; baseline systolic blood
exercise was found to be an independent metabolic syndrome (baseline waist cir- pressure, P = 0.002; baseline total choles-
predictor of IFG and type 2 diabetes cumference, P , 0.001; 4 waist circum- terol, P = 0.019; and 4 total cholesterol,
(b = 20.037 6 0.020; P = 0.023) together ference, P = 0.001; baseline glucose P , 0.001).

Figure 1dMean changes in body weight and waist circumference according to participation in the 6-month exercise program, BMI (normal weight
vs. overweight/obese), and changes in fasting glucose. Data are expressed as mean 6 SE. DM, type 2 diabetes. (A high-quality color representation of
this gure is available in the online issue.)

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Effect of exercise and BMI on type 2 diabetes

Table 3dResults of logistic regression analysis for IFG and diabetes status as monitored by a qualied health care profes-
dependent variables sional. A strong inverse association between
exercise and risk of type 2 diabetes was
Variable Regression coefcient SE P found among overweight/obese subjects.
Several previous studies reported that
All participants (n = 7,233) impaired glucose regulation appears to
Exercise (yes/no) 20.037 0.020 0.023 best predict future diabetes (1821). Life-
Fasting serum glucose 0.369 0.001 ,0.001 style changes have been shown to be ef-
Weight 0.016 0.003 0.369 fective in preventing both diabetes and
BMI 20.017 0.005 0.539 obesity in high-risk adults with impaired
Total cholesterol 0.070 0.000 ,0.001 glucose tolerance (46). Compared with
Systolic BP 0.038 0.001 0.163 normal-weight subjects with NFG who
Diastolic BP 0.001 0.001 0.975 participated in the regular exercise pro-
Age 0.025 0.002 0.140 gram in the current study, the risk of de-
Systolic BP 0.098 0.001 0.002 veloping type 2 diabetes for overweight/
Diastolic BP 20.018 0.002 0.581 obese subjects with IFG was 16.3-fold
Waist circumference 0.134 0.002 ,0.001 higher in the nonexercise program group
Waist circumference 0.069 0.002 0.001 and 10.8-fold higher in the exercise pro-
Total cholesterol 0.044 0.000 0.019 gram group. This nding that regular exer-
, Changes are differences between baseline and 2 years. Adjusted R2 = 0.191; P , 0.001. BP, blood pressure. cise reduces the risk of diabetes among
obese individuals with IFG is consistent
with results of previous clinical trials (46).
CONCLUSIONSdIn this 2-year study, incidence of type 2 diabetes with an average The strength of the current study was
a 6-month exercise program consisting of of 2.8 years (range, 1.84.6) of lifestyle in- that the exercise program was prescribed
300 min/week of moderate-intensity ex- tervention that prescribed 150 min/week of and monitored by a qualied health care
ercise without dietary changes resulted moderate-intensity exercise and a dietary professional, whereas previous studies
in a 23% reduction in the incidence of program designed to induce a 7% weight often used self-reports of physical activ-
type 2 diabetes. This inverse association loss (6). A similar risk reduction of 58% ity, which are less accurate and usually
between exercise and risk of type 2 diabetes was associated with lifestyle changes in result in bias. The limitation of the current
was stronger among overweight/obese the Finnish Diabetes Prevention Study study was the lack of randomization of
subjects than normal-weight subjects. In (5); and in Asian Indians with impaired participants to groups (exercise vs. non-
addition, the exercise program group glucose tolerance, lifestyle modications, exercise program group). In addition, we
showed improved fasting glucose levels including 210 min/week of brisk walking did not perform the 2-h oral glucose
(from IFG to NFG: normal-weight sub- and dietary modications (i.e., reduction in tolerance test on the biennial medical eval-
jects in the exercise program group, total calorie intake and total fat intake, uations and during the supervised exercise
46.0%; overweight/obese subjects in the avoidance of simple sugars and rened car- program study; therefore, the criteria for
exercise program group, 54.0%). Im- bohydrates, and inclusion of ber-rich diabetes (i.e., patient history or fasting
proved fasting glucose was associated food), resulted in a 28.5% reduced risk of glucose levels) may have included some
with reductions in waist circumference incident diabetes (7). Hu et al. (17) also cases of asymptomatic diabetes at baseline
and BMI; this reduction was signicantly reported an inverse association between or misclassied the glucose status. Misclas-
greater in the exercise program group, physical activity and the risk of type 2 di- sication of diabetes would weaken the
suggesting that regular exercise indirectly abetes for nonobese subjects with normal association between exercise and BMI and
reduces the risk of type 2 diabetes through glucose regulation, as well as subjects who the risk of type 2 diabetes. Despite these
decreased body weight or improved body fat were either obese or showed impaired limitations, the current study shows that
distribution in overweight/obese subjects. glucose regulation (mean follow-up = 9.4 regular exercise can reduce the risk of
Exercise has been shown to facilitate weight years). However, several studies reported type 2 diabetes in individuals who are over-
loss (15) but more strongly inuences ab- that glycemic control did not improve weight or obese, even without dietary
dominal adiposity (16). The overweight/ with lifestyle modication and drug ther- changes. The ndings indicate that regular
obese subjects in the exercise program apy (11,12). Krousel-Wood et al. (11) exercise and reductions in weight or waist
group whose fasting glucose values im- reported that exercise interventions have circumference are critical factors in diabetes
proved or remained the same showed a the potential to reduce BMI in patients prevention among overweight or obese
greater reduction in body weight. This re- with diabetes but not reduce HbA1c. Khan individuals with IFG.
sult is consistent with previous reports et al. (12) reported that exercise in conjunc-
showing that being overweight or physi- tion with oral drug therapy prescribed for
cally inactive increases the risk of type 2 the individual with type 2 diabetes did not
diabetes (6), demonstrating the need for directly modify HbAlc levels. These discrep- AcknowledgmentsdThis work was supported
by the Korean NHIC and the Midcareer Re-
appropriate exercise interventions for ant results might be partly due to differen- searcher Program through National Research
this group. ces in the duration of follow-up, prescribed Foundation of Korea, Republic of Korea
A number of studies have demon- nutritional therapy, and prescribed exercise (M10642120002-06N4212-00210 and 2012-
strated the benets of exercise on glucose volume and/or intensity. In the current 0005604).
regulation. The U.S. Diabetes Prevention study, an exercise program (without nutri- No potential conicts of interest relevant to
Program reported a 58% reduction in the tion intervention) was prescribed and this article were reported.

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Chae and Associates

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