Journal of the American College of Nutrition

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Inflammatory Potential of Diet: Association With

Chemerin, Omentin, Lipopolysaccharide-Binding
Protein, and Insulin Resistance in the Apparently
Healthy Obese

Susan Mirmajidi, Azimeh Izadi, Maryam Saghafi-Asl, Farhad Vahid, Nahid

Karamzad, Parichehr Amiri, Nitin Shivappa & James R. Hébert

To cite this article: Susan Mirmajidi, Azimeh Izadi, Maryam Saghafi-Asl, Farhad Vahid, Nahid
Karamzad, Parichehr Amiri, Nitin Shivappa & James R. Hébert (2018): Inflammatory Potential
of Diet: Association With Chemerin, Omentin, Lipopolysaccharide-Binding Protein, and Insulin
Resistance in the Apparently Healthy Obese, Journal of the American College of Nutrition, DOI:
10.1080/07315724.2018.1504348

To link to this article: https://doi.org/10.1080/07315724.2018.1504348

Published online: 25 Sep 2018.

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JOURNAL OF THE AMERICAN COLLEGE OF NUTRITION
https://doi.org/10.1080/07315724.2018.1504348

Inflammatory Potential of Diet: Association With Chemerin, Omentin,

Lipopolysaccharide-Binding Protein, and Insulin Resistance in the Apparently
Healthy Obese
Susan Mirmajidia,b, Azimeh Izadia,b, Maryam Saghafi-Aslb, Farhad Vahidc , Nahid Karamzadd,
Parichehr Amiria,b, Nitin Shivappae,f, and James R. H
eberte,f
a
Student Research Committee, School of Nutrition and Food Sciences, Tabriz University of Medical Sciences, Tabriz, Iran; bDepartment of
Clinical Nutrition, School of Nutrition and Food Sciences, Tabriz University of Medical Sciences, Tabriz, Iran; cDepartment of Nutritional
Sciences, School of Health, Arak University of Medical Sciences, Arak, Iran; dDepartment of Public Health, School of Nursing and Midwifery,
Maragheh University of Medical Sciences, Maragheh, Iran; eDepartment of Epidemiology & Biostatistics, Arnold School of Public Health,
University of South Carolina, Columbia, South Carolina, USA; fCancer Prevention and Control Program, Arnold School of Public Health,
University of South Carolina, Columbia, South Carolina, USA

ABSTRACT ARTICLE HISTORY

Objective: Low-grade inflammation is a characteristic of various conditions, including obesity. Diet Received 25 May 2018
is regarded as a strong modifier of inflammation. The potential links between inflammatory prop- Accepted 19 July 2018
erties of diet and adipokines as well as insulin resistance (IR) warrant further investigation.
KEYWORDS
Therefore, this study aimed to examine the associations of the dietary inflammatory index (DII)
Dietary Inflammatory Index;
with serum chemerin, omentin, and lipopolysaccharide-binding protein (LBP) as well as IR among abdominal obesity;
apparently healthy obese adults. adipokine; chemerin;
Design: In this cross-sectional study, 171 abdominally obese subjects were recruited in the north- omentin; endotoxin
west of Iran. Demographic data, dietary intake, anthropometric indices, and physical activity (PA)
were assessed. DII scores were calculated based on dietary intake, using a validated 168-item food
frequency questionnaire (FFQ). Basal blood samples were collected to determine the biochemical
parameters. A linear regression test with adjusted beta estimates was applied for data analysis.
Result: Compared to those with higher DII score, the group with lower DII score (anti-inflamma-
tory diet) had higher protein (83.62 ± 36.42 g vs. 71.61 ± 25.94 g) and lower carbohydrate
(325.00 ± 125.76 g vs. 378.19 ± 137.69 g) intake. Participants with higher DII score had lower con-
sumption of polyunsaturated and monounsaturated fats as well as fiber and higher saturated fats
(p < .001). Those with elevated DII score had higher levels of chemerin (p ¼ .034) and LBP
(p ¼ .040), compared to those with lower DII. Omentin showed no significant differences between
groups with different DII scores. Additionally, people with a more proinflammatory diet had higher
FBS (p ¼ .005); however, other markers of IR did not differ by DII scores.
Conclusions: The results suggest that increased inflammatory potential of diet, as indicated by
higher DII score, is associated with elevated levels of chemerin and LBP. While DII was positively
associated with FBS, no significant correlation was found for insulin and other indices of IR.

Introduction
Obesity is a major public health issue with a rising preva-
lence in both developed and developing countries (1).
Obesity is the fifth leading cause of death in the world,
accounting for 3.4 million deaths annually (2). Additionally,
it is strongly associated with several chronic diseases, includ-
ing diabetes mellitus, hypertension, cardiovascular disease,
and certain types of cancer (3).
Obesity is considered a chronic low-grade inflammatory
state that promotes the production of proinflammatory factors
involved in the pathogenesis of insulin resistance (IR) (4). The
excess adipose mass leads to increased secretion of inflamma-
tory adipokines (5). Chemerin (RARRES2/TIG2) is an inflam-
matory adipokine for which roles in the regulation of lipid
and glucose homeostasis are well known (6). The expression
and secretion of chemerin are elevated with adipogenesis (7).
Additionally, there is evidence of the strong correlation
between plasma concentrations of chemerin and body mass
index (BMI), triglycerides, and blood pressure (8). These find-
ings propose that chemerin might play a key role in the devel-
opment of obesity and metabolic syndrome (MetS) (8).
Omentin, a newly identified adipokine derived from adi-
pose tissue, has shown strong insulin-sensitizing effects (9).
A body of evidence suggests an inverse association of omen-
tin with metabolic risk factors, including obesity, BMI, waist
circumference (WC), and hyperglycemia, as well as positive
correlation with adiponectin and high-density lipoprotein
cholesterol (HDL-C) levels (10–12).

CONTACT Dr. Maryam Saghafi-Asl saghafiaslm@gmail.com Department of Clinical Nutrition, School of Nutrition and Food Sciences, Tabriz University of
Medical Sciences, Tabriz, Iran
ß 2018 American College of Nutrition
2 S. MIRMAJIDI ET AL.
Lipopolysaccharide (LPS) molecules, also known as bac-
terial endotoxins, may cause inflammation, leading to activa-
tion of immunity and cytokine secretion (13). LPS has a
short half-life (14). Therefore, lipopolysaccharide-binding
protein (LBP) is introduced with a longer half-life and more
trustworthy measurement (15). Also, serum LBP level is a
proxy of serum LPS level (16). Our previous work on meta-
bolically healthy and unhealthy population showed that lev-
els of LBP seem to be more related to abdominal obesity
than to the presence or absence of metabolic health (17).
Another study found that among MetS components, the
level of LBP was independently associated with abdominal
obesity (18).
Diet plays a significant role in the development and
modulation of the inflammatory cascade (19). Particularly, a
diet rich in proinflammatory constituents such as saturated
fatty acids (SFAs) (20) and trans fatty acids (21) causes pro-
liferation and oxidative stress that can promote inflamma-
tion (20), whereas polyunsaturated fatty acids (PUFAs) (22),
monounsaturated fatty acids (MUFAs) (23), and fiber have
been consistently associated with lower levels of systemic
inflammation (24). Esposito et al. (25) demonstrated that
high-fat meals can raise the level of interleukin (IL) 18 and
decrease adiponectin concentration, while high-carbohy-
drate, high-fiber meals can reduce the level of IL-18 both in
nondiabetic and diabetic subjects. It was also shown that
high-carbohydrate, low-fiber meals considerably decreased
adiponectin concentrations in diabetic subjects (26). Thus, it
seems that a diet rich in fiber and complex carbohydrates is
a more suitable choice than refined carbohydrates, but their
role in alleviating inflammation needs more investiga-
tion (26).
Examination of the inflammatory potential of diet and its
impact on obesity and obesity-related metabolic abnormal-
ities, including IR, has received special attention (27–29).
The dietary inflammatory index (DII) is a novel tool meas-
uring the inflammatory potential of a diet based on the
overall inflammatory properties of dietary components
(30,31). A recent study concluded that a proinflammatory
diet was associated with elevated C-reative protein (CRP)
and the glucose intolerance component of the MetS (32).
The association of DII with chemerin, omentin, and LBP
has not been investigated. Considering the role of diet on
inflammation as well as the presence of insufficient data to
evaluate the association between DII and inflammatory bio-
markers as well as IR, this study was designed and con-
ducted to examine the associations of DII with the already-
described adipokines and IR in apparently healthy
obese people.
Materials and methods
This cross-sectional study was conducted from 15 June to 6
November 2015 in the northwest of Iran. After public
announcements for the study, 500 volunteers were recruited
from the general population. Of these, 171 apparently
healthy obese (BMI 30 kg/m2) people (ages 18 to 60 years)
were consecutively enrolled based on the defined eligibility
criteria. According to Meigs et al. (33), apparently healthy
obese was defined as the presence of less than 3 of the fol-
lowing metabolic abnormalities, including abdominal obesity
(WC 95 cm for both genders) (34); high fasting blood
sugar (FBS) (100 mg/dL); high serum triglyceride (TG)
concentration (150 mg/dL); low serum high-density lipo-
protein cholesterol (HDL-C) (<40 mg/dL for men and
<50 mg/dL for women); and elevated blood pressure (BP)
(130/85/85 mm Hg) (34). Potential participants were
excluded if they had any clinically apparent chronic diseases
such as hypertension, diabetes, cardiovascular disease
(CVD), hepatic disorders, renal disease, gastrointestinal dis-
ease or surgery during the past year, cancer, infectious dis-
eases, severe mental illness, and malignancy. Those on a diet
or with misreported dietary intakes (<800 kcal/day or
>4200 kcal/day) or taking any agent affecting lipid and glu-
cose metabolism, corticosteroids, contraceptives, antibiotics,
anti-obesity drugs, anti-inflammatory drugs, beta-blockers,
anticoagulants, antioxidant supplements, multivitamins, and
x3 or x6 supplements in the last 2 months were also
excluded. The ethics committee of the Tabriz University of
Medical Science approved this study. The research was per-
formed in compliance with the Declaration of Helsinki
(Ethical code: TBZMED.REC.1395.1169).
Measurements
Weight and height of each participant were measured using
a Seca scale and an inelastic measuring tape, respectively.
Weight was measured in light clothing and with a precision
of 0.1 kg. Height was measured without shoes with a preci-
sion of 0.1 cm. Body mass index (BMI) was calculated as
weight in kilograms divided by the square of height in
meters. WC and hip circumference (HC) were measured
using a non-stretchable fiber measuring tape. WC was meas-
ured at the midpoint between the lower ribs and the iliac
crest, and HC was measured at the level of the maximum
extension of the buttocks. Waist to hip ratio (WHR) was
calculated as WC (cm) divided by HC (cm) (35). Habitual
physical activity was measured, using the long-form
International Physical Activity Questionnaire (IPAQ) (36).
Physical activity was expressed as metabolic equivalents
(Mets)-h per week.
Laboratory assays
After an overnight fast, blood samples were drawn and
serum was separated by centrifuging at 3000 rpm for 15 min.
Lipid profile and blood sugar were measured immediately,
using a commercial kit (Pars Azmoon, Tehran, Iran) and a
Selectra 2 autoanalyzer (Vital Scientific, Spankeren, the
Netherlands). Interassay and intra-assay coefficients of vari-
ation (CV) were <5% for all assays). The rest of the serum
samples were stored at 80 C until analysis. Serum insulin,
LBP, chemerin, and omentin levels were determined by a
sandwich enzyme-linked immunosorbent assay (ELISA),
using commercial kits (insulin: Monobind, Inc., lake Forest,
CA; and other parameters: Bioassay Technology Laboratory,

Shanghai Korean Biotech, Shanghai City, China), according
to the manufacturer’s instructions. The intra-assay and
interassay CVs were <8% and 10% for chemerin, omentin,
and LBP and <8% and 9.8% for insulin, respectively. The
homeostasis model assessment of IR (HOMA-IR) was calcu-
lated, using fasting plasma glucose and fasting insulin values,
according to the formula (37). Quantitative insulin sensitiv-
ity check index (QUICKI) was calculated based on the for-
mula, with higher QUICKI values, indicating greater insulin
sensitivity. The homeostasis model assessment of beta cells
(HOMA-B) was also used to estimate pancreatic beta cell
function (38).
Assessment of dietary intake
Dietary intake of the participants during the past year was
assessed, using a validated semiquantitative food frequency
questionnaire (FFQ). The FFQ consisted of 168 food items
and the participants reported their frequency of consump-
tion of each food item on a daily, weekly, monthly, or yearly
basis. Then, the reported intakes were converted to daily
grams of food intake. Nutritionist IV software (Axxya
Systems, Stafford, TX), modified for Iranian foods, was used
to calculate the energy and nutrient content of foods.
Dietary inflammatory index
The DII scores were calculated according to the FFQ-
derived dietary data, as described in detail elsewhere (31).
Briefly, dietary data for each study participant were first
linked to a regionally representative global database that
provided a robust estimate of means and standard deviations
for each of the food parameters considered (i.e., foods,
nutrients, and other food components). The “standard
mean” was subtracted from the actual food parameter value
and divided by its standard deviation. This z-score was then
converted to a percentile (in order to minimize the effect of
outliers or right-skewing, a common occurrence with dietary
data). This value was then converted to a centered percentile
score, which was then multiplied by the respective inflam-
matory effect score of the food parameters (derived from a
literature review and scoring of 1943 “qualified” articles) to
obtain the subject’s food parameter-specific DII score. All of
the food parameter-specific DII scores were then summed to
create the overall DII score for each subject in the study.
The DII was analyzed both as a continuous and as a cat-
egorical variable (based on the median value of 0.57). DII
values were categorized into below and above the median.
The median DII score was 0.57 and ranged from a max-
imum anti-inflammatory value of 2.89 to a maximum
proinflammatory value of 3.9. A higher DII score indicates a
greater proinflammatory potential of the diet.
Sample size estimation
The larger sample size was calculated based on Jiala et al.
and Shivappa et al. for patients with MetS and Iranian post-
menopausal women, respectively (39,40). To estimate the
JOURNAL OF THE AMERICAN COLLEGE OF NUTRITION 3
sample size, we conducted the standard formula by consid-
ering type 1 error (a) of .05 and type 2 error (b) of .20
(power ¼80%). Based on these variables, 143 persons would
fulfill the aims of our study.
Statistical analysis
Statistical Package for the Social Sciences (SPSS) software
(Version 25.0, SPSS, Inc., Chicago, IL) was used to perform
the data analysis. Twenty-one cases were excluded from the
analysis because of missing data; the final analysis included
150 subjects. The Kolmogorov–Smirnov test was applied to
check the normality of data distribution. The quantitative
results were presented as the means and standard deviation
(SD) and median (25th, 75th percentiles) for normally and
not normally distributed variables, respectively. Analysis of
covariance (ANCOVA) was used to test for differences
between groups, controlling for sex, age, body mass index
(BMI), energy intake, and physical activity. Partial correl-
ation analyses were used to assess the independent contribu-
tions of several potential confounders, including age, sex,
BMI, energy intake, and physical activity. The associations
between DII and BMI as well as biochemical parameters
were further assessed, using a linear regression analysis, and
the adjusted beta estimates and 95% confidence intervals
(95% CIs) were presented. Those p values lower than .05
were considered statistically significant.
Results
The characteristics of the participants according to DII cate-
gories are shown in Table 1. The DII was analyzed both as a
continuous and as a categorical variable, based on the
median value of the DII ¼0.57). DII values were categorized
into below and above the median. The median DII score
was 0.57 and ranged from a maximum anti-inflammatory
value of 2.89 to a maximum proinflammatory value of 3.9.
Of 150 participants, 50.7% (n ¼ 76) were males and
49.3% (n ¼ 74) were females. The DII scores did not differ
by sex (0.36 for males vs. 0.07 for females, p ¼ 0.17) (data
not shown). The mean age of the participants was 39.29 (±
9.5) years for males and 36.05 (±7.28) years for females.
There were no significant differences in age, weight, WC,
HC, and WHR based on DII subgroups; however, among
females, those with DII  0.57 had a significantly higher
BMI (p ¼ .005). The physical activity level was not signifi-
cantly different between the two groups (Table 2).
Dietary intakes of macronutrients, total energy, and per-
centage of energy from each macronutrient (carbohydrate,
fat, and protein), stratified by DII score, are provided in
Table 2. The group with the lower DII score (anti-inflamma-
tory dietary score) had higher protein (p ¼ .022) and lower
carbohydrate (p ¼ .015) intakes. The percentage of energy
derived from carbohydrate was remarkably lower in this
subgroup (p < .001). While no significant difference was
observed for intake of fat between the 2 groups. However,
the type of fat was significantly different between the two
DII subgroups (p < .001); participants with higher DII score,
4 S. MIRMAJIDI ET AL.

Table 1. Characteristics of the Participants Between Subgroups of DII, Stratified by Sex.

Males Females
Characteristic
DII DII
<Median a
Median p <Median Median p
Age (years) 40.84 ± 9.91 37.03 ± 8.54 0.086 34.97 ± 7.81 36.79 ± 6.88 .292
Weight (kg) 93.88 ± 11.31 93.94 ± 10.98 0.979 77.92 ± 10.12 82.29 ± 12.65 .118
BMI (kg/m2) 31.02 ± 3.83 31.78 ± 4.5 0.433 31.17 ± 4.2 33.89 ± 3.76 .005
WC (cm) 108.82 ± 8.75 108.85 ± 12.64 0.989 102.57 ± 8.13 106.07 ± 9.59 .106
HC (cm) 110.44 ± 6.57 110.03 ± 7.0 0.794 110.47 ± 7.32 113.34 ± 8.90 .148
WHR 0.985 ± 0.04 0.99 ± 0.104 0.776 0.93 ± 0.07 0.94 ± 0.07 .668
Note. DII: dietary inflammatory index; BMI: body mass index; WC: waist circumference; HC: hip circumference; WHR: waist-to-
hip ratio. Values are expressed as means ± standard deviation (SD). Significant p values at 5% level are in bold.
a
Median is 0.57.

Table 2. Dietary Intakes and Physical Activity of the Participants in the Two Subgroups of DII.
DII
Variable <Mediana  Median p
Total energy (kcal/d) 2349.81 ± 814.50 2188.78 ± 756.40 .212
Energy percent from protein 14.00 ± 3.28a 13.42 ± 3.49 .303
Energy percent from fat 26.72 ± 8.29a 25.46 ± 9.74 .394
Energy percent from carbohydrate 56.72 ± 14.37a 74.19 ± 34.30 <.001
Carbohydrate (g/d) 325.00 ± 125.76a 378.19 ± 137.69 .015
Protein (g/d) 83.62 ± 36.42a 71.61 ± 25.94 .022
Total fat (g/d) 61.48 (45.94, 91.55)d 54.54 (37.02, 74.60) .083
Polyunsaturated fat (g/d) 16.66 (13.05, 25.84)d 12.17 (8.88, 17.13) <.001
Monounsaturated fat (g/d) 20.22 (14.17, 31.68)d 15.58 (10.43, 22.83) <.001
Saturated fat (g/d) 13.14 (8.41, 19.88)d 18.39 (12.29, 28.61) <.001
Fiber (g/d) 31.81 (27.61, 39.93)d 17.86 (14.13, 20.56) <.001
Percentage of energy from sugar 7.45 ± 4.37 10.09 ± 6.81 <.006
Refined carbohydrates (g/d) 60.37 ± 22.59 54.38 ± 25.20 0.128
Sugar (g/d) 64.91 ± 36.89 56.05 ± 32.14 0.119
Physical activity (MET-h/week) 41.05 (17.48,77.07) 48.84 (23.74, 118.52) 0.146
Note. DII: Dietary inflammatory index. Values are expressed as means ± standard deviation (SD) or median (25th,
75th), as appropriate. Significant p values at 5% level are in bold.
a
Median is 0.57.

indicating more proinflammatory diets, had lower consump- Table 3. Biochemical Parameters of the Participants According to DII Score.
tion of PUFAs and MUFAs fats and higher SFAs. Moreover, DII
Variable
fiber intake was lower (17.86 g vs. 31.81 g, p < .001) and the Median a
<Medianb p
percentage of energy from sugar was higher (10.09 vs.7.45, Chemerin (ng/mL) 391.60 (303.30, 789.70) 358.70 (286.80, 514.90) .034
p < .006) in this subgroup. However, there was no signifi- Omentin (ng/mL) 72.60 (58.10, 80.60) 69.90 (59.50, 95.50) .689
LBP (mg/mL) 15.00 (6.00, 24.00) 13.00 (6.00, 23.00) .042
cant difference in the intake of refined carbohydrates Insulin (mg/dL) 13.64 (11.24, 35.23) 13.05 (10.36,18.63) .689
(60.37 g in the lower DII group, compared to 54.38 g in the FBS (mg/dL) 93.53 ± 10.12 89.37 ± 7.32 .005
higher DII group; p ¼ .128) and sugar intake (64.91 in peo- HOMA-IR 3.37 (1.39, 5.43) 2.99 (1.27, 5.32) .401
HOMA-B 3.28 (1.29, 5.55) 2.94 (1.39, 5.23) .978
ple with lower DII, compared to 56.05 in those with higher QUICKI 0.328 ± 0.035 0.333 ± 0.034 .404
DII; p ¼ .119). TG (mg/dL) 171.82 ± 97.86 174.34 ± 99.30 .662
TC (mg/dL) 188.25 ± 33.39 190.02 ± 38.75 .821
Table 3 shows the adjusted values of chemerin, omentin, LDL-C (mg/dL) 110.77 ± 31.39 112.25 ± 35.95 .770
LBP, IR, and lipid profile according to the DII score. HDL-C (mg/dL) 43.10 ± 8.80 42.90 ± 9.08 .450
Participants with higher DII had elevated levels of chem- Note. DII: dietary inflammatory index; LBP: lipopolysaccharide-binding protein;
erin and LBP, compared to those with lower DII. FBS: fasting blood sugar; QUICKI: quantitative insulin check index; TG: trigly-
ceride; TC: total cholesterol; HDL-C: high-density lipoprotein cholesterol;
Additionally, people with higher proinflammatory diet had LDL-C: low-density lipoprotein cholesterol. Values are expressed as
higher FBS (p ¼ .005); however, other markers of IR did means ± standard deviation (SD) or median (25th, 75th), as appropriate.
not differ by DII scores. Though HOMA-IR and HOMA-B Significant p values at 5% level are in bold.
a
Adjusted for sex, age, body mass index, energy intake, and physical
were increased and QUICKI was decreased in those with activity (ANCOVA).
higher DII, the differences did not reach the significant b
Median is 0.57.
level. No significant differences were observed in terms of
TG, TC, HDL-C, and LDL-C between the two subgroups did not change after adjusting for potential confounders
of DII. Beta estimates and 95% CIs for the association including age, sex, physical activity, and dietary energy
between DII and biochemical parameters are presented in intake. Additionally, the DII had a significant direct associ-
Table 4. ation with serum chemerin (b ¼ 0.398, 95% CI: 147.075,
The results of the linear regression revealed a significant 323.39) and LBP (b ¼ 0.229, 95% CI: 0.560, 3.073) in crude
positive association of DII with FBS (b ¼ 0.40, 95% CI: 0.83, models. This association remained significant after consider-
3.04) and BMI (b ¼ 0.351, 95% CI: 0.258, 1.247). The results ing the confounding factors. However, no significant
 JOURNAL OF THE AMERICAN COLLEGE OF NUTRITION 5

Table 4. Beta Estimates and Confidence Intervals for the Association of DII investigate the possibility of other factors that may play a
with BMI and Biochemical Parameters.
major role in modulating the association of inflammation
Model 1 Model 2
and obesity among females. For example, it is reported that
Variable b (95% CI) p b (95% CI) p women are disproportionately exposed to several factors that
BMI 0.251 (0.203,0.881) .002 0.351 (0.258,1.247) .003 increase inflammation, including mental health, physical
FBS 0.247 (0.4219,1.891) .002 0.402 (0.826,3.040) .001
Insulin 0.002 (0.884, 0.902) .984 0.166 (0.425,2.217) .182 inactivity, and interpersonal stressors, which are all involved
HOMA-IR 0.035 (0.167, 0.258) .673 0.214 (0.038, 0.590) .084 in obesity (43). Additionally, this between-sex difference
HOMA-B 0.031 (0.238, 0.162) .709 0.112 (0.160,0.433) .364 could be partially explained by a greater accumulation of
QUICKI 0.045 (0.004, 0.002) .584 0.239 (0.009, 0.000) .054
Chemerin 0.398 (147.075, 323.39) <.001 0.317 (59.09, 331.45) .005 subcutaneous fat in women than in men and higher lean
Omentin 0.147 (21.270, 0.972) .073 0.192 (29.272, 3.405) .120 mass in men (44). Sex differences in the metabolic activity
LBP 0.229 (0.560, 3.073) .005 0.223 (0.469, 3.146) .009
of adipose tissue, as well as in the association between leptin
Note. Model 1:Unadjusted. Model 2: Adjusted (for age, sex, physical activity,
and level of energy intake). CI: confidence interval; DII: dietary inflammatory and CRP, may also explain these differences (45).
index; FBS: fasting blood sugar; HOMA-IR: homeostasis model assessment of Previous studies have reported inconsistent results
insulin resistance; HOMA-b: homeostasis model assessment of b-cell regarding the association of DII with BMI. Although higher
function; QUICKI: quantitative insulin sensitivity check index; LBP: lipopoly-
saccharide-binding protein. DII scores have been associated with higher BMI values in

Significant p values at 5% level are in bold. the American SEASONS (46), inverse relationships with
BMI were observed in the Luxembourg population (47).
relationship was observed between the DII and serum omen- Ruiz-Canela et al. (29) indicated that higher inflammatory
tin in either crude or adjusted models. potential of diet was associated with higher BMI and WC.
Overall, with regard to association between DII and obesity,
the origin of inflammation during obesity is yet to be fully
Discussion
understood, but there is a hypothesis suggesting a bidirec-
In this study, it was observed that those with lower DII tional relationship. Indeed, a proinflammatory diet leads to
score had higher protein and lower carbohydrate intakes. As adiposity; thus, a vicious cycle is created due to the relation
expected, a more proinflammatory diet was associated with of nutrient excess and certain foods or nutrients to inflam-
lower PUFAs, MUFAs, and fiber intake and a higher per- mation (48).
centage of energy from sugar. Those with higher DII score The other suggested mechanism underlying this relation-
had significantly elevated levels of FBS, chemerin, and LBP. ship is the activation of pathogen-associated molecular pat-
Moreover, the results of linear regression revealed that DII terns, including Toll-like receptors (TLRs) and Nod-like
was significantly associated with FBS and chemerin. receptors, which in turn activate the inflammatory markers
It was previously indicated that a proinflammatory diet in some tissues, including the adipose tissue (49). Moreover,
primarily consists of inflammatory food parameters, includ- a proper dietary fatty acid balance is suggested to prevent
ing SFA, and is comparatively poor in anti-inflammatory and decrease the metabolic framework of obesity and its
food ingredients such as fibers, MUFA, and PUFA (29). Our related disorders (50). In this regard, it should be high-
results are consistent with the findings of Kim et al. (41), lighted that in the present study, those with more inflamma-
reporting that participants in the lowest compared to the tory diets had a higher intake of SFA and lower intakes of
highest DII tertile consumed lower amounts of saturated fat. PUFA and MUFA. However, more investigations are war-
Additionally, subjects with more anti-inflammatory diets
ranted to justify the inconsistent results.
had a higher consumption of MUFAs than participants with
The present study also found that a proinflammatory diet
a more proinflammatory diet (41). Similarly, an inverse
is positively associated with FBS, while no significant correl-
association between DII and intake of healthy foods and
ation was found for insulin and other indices of IR. Several
nutrients has been reported (29).
studies conducted in Iranian, US, and European populations
In this study, the percentage of energy from sugar was
investigated the association of DII with FBS, insulin, and
higher in the group with higher DII score. Increased con-
sumption of foods with high density and low quality, such HOMA-IR (7,28,32). In a cohort study among an Iranian
as those rich in refined starches and sugar and poor in nat- population (7), DII score was positively associated with 2-
ural antioxidants and fiber, may cause activation of the hour postload glucose (2h-PG.) However, no significant lin-
innate immune system, most likely by an excessive release of ear trend was observed between the DII score and other bio-
proinflammatory cytokines and reduced production of anti- markers of glucose–insulin homeostasis. In a Dutch cohort
inflammatory cytokines. This imbalance may favor the gen- study (28), higher DII was associated with higher FBS and
eration of a proinflammatory milieu, which in turn may 2h-PG; however, after adjustment for BMI, these associa-
produce IR in the peripheral tissues and endothelial dys- tions became nonsignificant. In contrast, in the US popula-
function at the vascular level and, ultimately, predispose sus- tion, glucose intolerance was more prevalent among
ceptible people to an increased incidence of the MetS and participants in the fourth quartile of DII compared to the
diabetes (42). first quartile after adjustment for age and BMI (32).
The present research suggested the association of a more Findings of our study indicated that DII is not associated
proinflammatory diet with BMI in females. The reason is with the b-cell function, fasting insulin secretion, and sensi-
not clear; therefore, further analyses should be carried out to tivity to insulin. To confirm these findings, investigations of
6 S. MIRMAJIDI ET AL.
the associations between DII and 2h-PG as well as postpran-
dial markers of insulin are recommended in future studies.
The results of the current study demonstrated that a
proinflammatory diet, as reflected by higher DII scores, is
also directly associated with increased inflammation, as evi-
denced by the elevated levels of chemerin. These findings
are in line with previous studies that have reported a rela-
tionship between diet and inflammatory markers (19,51).
Similarly, results from the Asklepios study have shown sig-
nificant positive associations between DII score and inflam-
matory markers (29,52).
Chemerin is released from the liver and white fat tissue
(53). It is suggested to be involved in the regulation of
expression of adipocyte genes such as with glucose trans-
porter-4, adiponectin, and leptin, which play a key role in
the adipocytes, function, as well as in lipid and glucose
metabolism (54). Previous studies have demonstrated the
relationship between chemerin and MetS components, IR,
and inflammation (54). A study by Fatima et al. (55) indi-
cated that circulating chemerin levels were significantly
higher in subjects with BMI greater than 25 kg/m2, com-
pared with those with a BMI below 25 kg/m2. According to
the literature, inflammation is associated with cardiovascular
disease, obesity, and IR (56). Diet might play an important
role in the regulation of chronic inflammation (47). In fact,
certain constituents of diet, including red meat and proc-
essed foods, are considered to be proinflammatory stimu-
lants (57,58). In contrast, some components of
Mediterranean-style diets such as fruits, nuts, extra-virgin
olive oil, or red wine were reported to have anti-inflamma-
tory properties (59,60).
We found no association between adherence to the
proinflammatory diet and the adipokine omentin. Omentin
functions as an adipokine that enhances insulin-mediated
glucose uptake. Decreased levels of omentin have been
reported in patients with T2DM (61). Besides, omentin lev-
els have shown a negative correlation with obesity, inflam-
mation, hyperglycemia, IR, and serum chemerin levels (61).
To date, some studies have examined the effects of dietary
composition on circulating levels of omentin (53,62,63);
however, to the best of our knowledge, no study has investi-
gated the association of the inflammatory potential of diet
with serum omentin concentrations. Kabiri et al. (64)
reported that consumption of a MUFA-rich diet is associ-
ated with increased omentin concentration, compared to the
usual diet, and these effects can be attributed to the impacts
of fatty acids on omentin gene expression. In contrast, we
failed to observe any significant association between anti-
inflammatory diet that contained a higher amount of MUFA
and omentin. Additionally, plasma omentin levels are
affected not only by weight and fat mass, but also by the
overall reorganization of fat tissue, achieved over the long
term (53,65). Moreover, a recent study (66) reported no sig-
nificant association between omentin levels and inflamma-
tory cytokines. Taken together, further studies are needed to
investigate whether omentin level is altered among obese
individuals and whether it is influenced by diet-
ary components.
The discrepancies between studies might be related to the
differences in their design, the health status of the study
population, and a general characteristic like age (64,67).
Considering the pivotal roles of these adipokines in obesity
and its related comorbidities, conducting prospective studies
with strong design and a larger sample size is
recommended.
In the current study, we found that adherence to a more
proinflammatory diet that contains higher SFAs and lower
PUFAs or MUFAs is associated with elevated levels of LBP.
In line with our findings, Rocha et al. (68) have suggested
that SFAs act as nonmicrobial agonists of TLR4 and trigger
inflammatory pathways. In addition, SFAs modulate gut
microbiota with an increased production of LPS after a high
fat intake, elevating this natural TLR4 ligand (68). Diet, as
an extrinsic factor, is reported to affect the inflammatory
response to exogenous LPS (13). Cani et al. (69) reported
that a high-fat diet in mice increased endotoxin levels and
that chronic exposure to LPS led to weight gain and IR.
More recently, it has been reported that a high-SFA diet
increases the intestinal absorption of LPS, which, in turn,
increases postprandial endotoxemia levels and the postpran-
dial inflammatory response (70). This is done through a
TLR–dependent pathway that is involved in the activation of
the transcription factor nuclear factor- B (NF B). This sig-
naling cascade results in the increased release of proinflam-
matory cytokines including tumor necrosis factor alpha
(TNF-a) or IL-6, and thus the development of low-grade
inflammation (13). Endotoxin levels have shown a positive
correlation with IR and chemerin and negative correlation
with omentin (71). An inverse correlation of serum LBP
with chemerin was also observed in our study.
The main limitation of this study is that no cause–effect
relationships can be inferred due to its cross-sectional
design. However, the present study had several strengths,
such as the use of a validated tool to measure the DII and
being among the first studies to examine the metabolic
abnormalities related to obesity by levels of a dietary index,
where the advantage over other dietary indices is its inflam-
mation-based approach to the diet. The DII has previously
been validated in Iranian population (72). Additionally, this
tool is standardized for dietary intake from numerous popu-
lations around the world (27,32). However, the DII was
computed with data from 34 of the 45 food parameters;
thus, 11 parameters are missing in our research. Finally,
though our stringent criteria could rule out important con-
founders in the study, the confounding role of environment
and stress, largely involved in the body’s inflammation state,
could not be considered (51).
To sum up, dietary constituents can exert anti-inflamma-
tory or proinflammatory effects that might influence the risk
of inflammatory diseases such as obesity. DII, a newly devel-
oped tool, estimates the inflammatory potential of the diet.
A more proinflammatory diet was accompanied with higher
carbohydrate as well as lower protein, PUFAs, MUFAs, and
fiber intake. DII was associated with BMI, as well as serum
FBS, chemerin, and LBP; however, it showed no significant
association with serum omentin and fasting insulin, IR, and

b cell function. More studies at larger sample size are
required to investigate the associations of inflammation
induced by a diet with IR markers as well as altered levels
of adipokines.
Conclusions
These data demonstrate that participant with lower DII
score had higher protein and lower carbohydrate intakes. A
more proinflammatory diet was associated with lower
PUFAs, MUFAs, and fiber intake. Those with higher DII
score had significantly elevated chemerin and LBP.
Moreover, DII was significantly associated with BMI as well
as FBS, chemerin, and LBP. These results reinforce the fact
that diet, as a whole, plays an important role in modifying
inflammation in the apparently healthy obese.
Acknowledgments
We sincerely appreciate all the obese individuals who took part in the
study. We also thank the Research Vice Chancellor of Tabriz
University of Medical Sciences for financial support of the study.
Conflict of interest: No potential conflict of interest was reported
by the authors.
Author contributions
SM and MSA conceived the study design and wrote the study protocol.
PA and NK were involved with data collection. JRH, FV, and NSH
helped with DII calculation. AI and SM analyzed and interpreted the
data. SM, MSA, and AI were involved in drafting the article or revising
it critically for content. All authors gave final approval of the version
to be published.
Funding
This study was financially supported by the Research Vice Chancellor,
Tabriz University of Medical Sciences, Tabriz, Iran. The results of this
article were extracted from the MSc thesis of Sousan Mirmajidi (grant
number 5/D/1019769), registered at Tabriz University of Medical
Sciences, Tabriz, Iran.
ORCID
Farhad Vahid https://orcid.org/0000-0002-7380-3790
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