TYPE Original Research

PUBLISHED 25 May 2023

DOI 10.3389/fnut.2023.1201010

How is healthy eating index-2015

OPEN ACCESS related to risk factors for
cardiovascular disease in patients
EDITED BY
Helda Tutunchi,
Tabriz University of Medical Sciences, Iran

REVIEWED BY
Mehdi Sadeghian,
with type 2 diabetes
Ahvaz Jundishapur University of Medical
Sciences, Iran Mobina Zeinalabedini 1,2, Ensieh Nasli-Esfahani 3,
Samira Pourmoradian,
Tabriz University of Medical Sciences, Iran Ahmad Esmaillzadeh 1 and Leila Azadbakht 1,3,4*
*CORRESPONDENCE 1
Department of Community Nutrition, School of Nutritional Sciences and Dietetics, Tehran University of
Leila Azadbakht Medical Sciences, Tehran, Iran, 2 Students’ Scientific Research Center (SSRC), Tehran University of
[email protected] Medical Sciences, Tehran, Iran, 3 Diabetes Research Center, Endocrinology and Metabolism Clinical
Sciences Institute, Tehran University of Medical Sciences, Tehran, Iran, 4 Department of Community
RECEIVED 05 April 2023
Nutrition, School of Nutrition and Food Science, Isfahan University of Medical Science, Isfahan, Iran
ACCEPTED 04 May 2023
PUBLISHED 25 May 2023

CITATION
Zeinalabedini M, Nasli-Esfahani E, Background: Cardiovascular disease (CVD) is the primary cause of mortality and
Esmaillzadeh A and Azadbakht L (2023) How is disability among diabetes. The aim of this study is to evaluate how healthy eating
healthy eating index-2015 related to risk factors
for cardiovascular disease in patients with type index-2015 related to risk factors for cardiovascular disease in patients with type
2 diabetes. 2 diabetes.
Front. Nutr. 10:1201010.
doi: 10.3389/fnut.2023.1201010 Methods: This cross-sectional study was conducted on 490 patients with type
2 diabetes in Tehran, Iran. The healthy eating index-2015 (HEI-2015) used as a
COPYRIGHT
© 2023 Zeinalabedini, Nasli-Esfahani, diet quality indicator. Dietary intake was assessed by a valid and reliable semi-
Esmaillzadeh and Azadbakht. This is an open- quantitative food frequency questionnaire (FFQ). Four indicators of CVD risk
access article distributed under the terms of
factor [Castelli risk index-1 and 2 (CRI-II), atherogenic index of plasma (AIP),
the Creative Commons Attribution License
(CC BY). The use, distribution or reproduction cholesterol index (CI), and lipid accumulation of plasma (LAP)] were calculated.
in other forums is permitted, provided the The anthropometric indices [a body shape index (ABSI), abdominal volume index
original author(s) and the copyright owner(s)
(AVI), and body roundness index (BRI)] were computed.
are credited and that the original publication in
this journal is cited, in accordance with Results: After adjusting for potential confounders, it is evident that participants in
accepted academic practice. No use,
the highest tertile of HEI had a lower odds ratio of BRI (OR: 0.52; 95% CI: 0.29–
distribution or reproduction is permitted which
does not comply with these terms. 0.95; p-trend=0.03) and AIP (OR:0.56; 95% CI: 0.34–0.94; p-trend=0.02). Also,
HEI and CRI had a marginally significant negative relation (OR: 0.61; 95% CI: 0.38–
1; p-trend=0.05) in crude model, after adjusting the signification disappeared.
Conclusion: In conclusion, our finding shows that more adherence to HEI reduces
about 50% of the odds of AIP, BRI among diabetic patients. Further, large-scale cohort
studies in Iran need to confirm these findings, including diabetic patients of various
racial, ethnic backgrounds, body composition and different components of HEI.

KEYWORDS

HEI-2015, CVD risk factors, type 2 diabetes, atherogenic index, anthropometric measurement

Introduction
Cardiovascular disease (CVD) is a prominent cause of mortality and morbidity globally (1).
As a significant risk factor for CVD, diabetes mellitus (DM) is one of the most rapidly increasing
illnesses (2). According to the International Diabetes Federation (IDF), 463 million persons had
diabetes in 2019 (3), and it is estimated that 9.2 million Iranians will get diabetes by 2030 (4).

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Zeinalabedini et al. 10.3389/fnut.2023.1201010

Previous studies have linked diet quality to all-cause mortality and 490 randomly chosen people with aged 35–80 referred to a
CVD (5, 6). According to estimates, dietary risk factors were Subspecialty clinic for diabetes and metabolic diseases.
responsible for 53% of CVD-related fatalities and 58% of CVD-related To be eligible, participants needed to meet the following
disabilities (7). There are few studies on the associations between conditions: have type 2 diabetes for at least 2 years, be between the
healthy eating index (HEI) as a diet quality indicator and risk factors ages of 35 and 80, not be on insulin, not be pregnant or breastfeeding,
for CVD, such as dyslipidemia, diabetes, and obesity. not be receiving estrogen hormone therapy, and not have an
A body shape index (ABSI) was linked to abdominal fat (8). A autoimmune disease, acute gastrointestinal disorder, acute renal
high ABSI value suggests a considerable accumulation of adipose disease, or liver cancer. Exclusion criteria included a lack of
tissue around the abdomen area and is a health risk (9). Body information in the medical records and reporting of dietary energy
Roundness Index (BRI) measures VAT and body fat (10). Obesity, intake (<800 kcal/day and over 4,200 kcal/day). The research protocol
especially visceral obesity, is highly associated with dyslipidemia (11). was accepted by the Human Ethical Committee of Tehran University
DM commonly leads to dyslipidemia raising the risk of of Medical Science [IR.TUMS.MEDICINE.REC.1400.185].
arteriosclerotic cardiovascular events (12). Dyslipidemia is
characterized by elevated levels of triglycerides (TG), high levels of Sample size
low-density lipoprotein cholesterol (LDL-C), and reduced levels of
high-density lipoprotein cholesterol (HDL-C) (12). Numerous clinical The sample size for this research was chosen by the prevalence of
investigations attempt to discover more dependable biochemical abdominal obesity in the nation in proportion to the quality of the
indications of atherogenic dyslipidemia (13, 14). overall diet as indicated by the index (HEI) (27). Using the formulas
Novel indicators, including lipid ratios, are linked to atherogenesis P1: the prevalence of abdominal obesity in persons with poor diet
(15). The atherogenic index of plasma (AIP) effectively predicts quality (0.31), P2: the prevalence of abdominal obesity in individuals
myocardial infarction, acute coronary events, atherosclerosis, and with a high diet quality (0.39), C1− B = − 0.842, and ca / 2 = 1.96,
CVD morbidity (13). The Cholesterol index (CI) is the most sample size was determined:
independent predictor and relative risk value for coronary artery
2
disease (16). Lipid accumulation product (LAP) is a simple clinical ca / 2 (r ) pQ − C 
 +1 1− B r1PQ
1 1 + p2Q2 
diagnostic factor for assessing cardiometabolic risk factors used to m′ =  
avoid CVD in the elderly (17). r ( p 2 − p1) 2
Castelli risk indexes 1 (CRI-1) and 2 (CRI-2) ratios are
independent CAD risk variables with strong predictive value (18, 19).
Several studies indicated that greater serum CRI-1 and non-HDL-C 2
 
were related to an increased risk of stroke (18, 19). Over the last two m`  2 ( r + 1) 
m=  1+ 1+ 
decades, evidence from observational studies and clinical trials has 4 
 m` r P2 − P1 
been collected, emphasizing the value of certain nutrients, foods, and
dietary patterns for CVD and DM prevention and treatment (20, 21).
The Healthy Eating Index (HEI) is a measurement of nutritional
quality that evaluates how closely one stick to dietary recommendations P1 + rP 2
P:
(20). Based on the findings from a cross-sectional negative correlation r +1
between HEI adherence and the development of metabolic syndrome
or its components was found (22). The HEI has also been linked to a Q1: 1 − P1 = 1 – 0/31 = 0/69 n1 = m.
reduced risk of CVD risk factors (23). According to many studies, those Q2: 1 − P2 = 1 – 0/39 = 0/61 n2 = m × r.
who followed the HEI had a lower risk of CVD and cancer (24–26).
As we know, no research has been conducted on the link between Q =1− P
HEI-2015 with novel CVD risk indicators and new anthropometric-
related CVD risk factors in type 2 diabetes patients. The purpose of
this research is to examine the connection between HEI-2015 with  30 
CVD risk variables in diabetic patients. (1.96 )  + 1 0.33 ∗ 0.67 −
 70 
2
30
∗ ( 0.31 ∗ 0.69 ) +
Materials and methods ( −0.842 ) 70
` = 314
( 0.39 ∗ 0.61)
=m
30
Study design and population ( 0.39 − 0.31)2
70
The main aim of this study is to investigate the relationship
between the healthy eating index-2015 (HEI-2015) and food security 2
with CVD risk factors in type 2 diabetes patients in a cross-sectional   30  
 2  + 1 
design. Individuals with type 2 diabetes were recruited from the 314   70   = 345
m= 1+ 1+
Tehran University of Medical Sciences affiliated Subspecialty clinic of 4  30
0.39 − 0.31

 314 
diabetes and metabolic diseases. Collecting the data was done between  70 
May 2021 and September 2022. The participants in this research were

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n1 = m, n2 = m × r (28). An experienced nutritionist gathered nutritional data via a face-

n1 + n2 = 345 + 145 = 490 to-face interview. We calculated the daily intake of each food item and
According to this formula, 490 people were needed. then converted them to grams per day. Then, the Nutritionist IV
program was used to calculate macro- and micronutrient intakes
Data collection (First Databank Division, the Hearst Corporation, San Bruno, CA,
United States, modified for Iranian foods).
Before the commencement of the study, participants completed
written permission forms confirming that they understood and agreed Healthy eating index 2015 score
to participate. Those who did not provide informed consent were not
included in the study. Patients referred to the clinic must undergo a new The 2015 HEI contained nine sufficiency components (total fruit,
laboratory test. As a result, biochemical indicators such as Fasting Blood whole fruit, total vegetables, greens and legumes, whole grains, dairy,
Sugar (FBS) and LDL-c were obtained from their medical laboratory total protein sources, seafood, plant protein, and fatty acids) and four
test. Personal information like age, drug history, taking supplements, moderate components (refined grains, sodium, percentage of energy
and other data were collected in interviews with patients by a dietitian. from added sugars, and percentage of energy from saturated fatty
acids). Except for the unsaturated to saturated fatty acid ratio, each
Demographic and socioeconomic status component is assessed on a density basis out of 1,000 calories. Because
several surveys lacked brand specificity and information regarding
The socioeconomic status demographic questionnaire, which discretionary salt usage, we changed the sodium component score.
contained questions about marital status, education, employment, Total fruit has 100% fruit juice, while whole fruit includes all forms
family size, means of support, method of transportation, having a except juice. Green beans contain legumes, and dairy products include
private house, etc., was utilized for this purpose. In order to create the milk. All milk products, such as fluid milk, yogurt, and cheese, as well
socioeconomic status score, the codes were attached to each as fortified soy drinks, are included. Seafood, nuts, seeds, soy products
questionnaire item. After that, the mean score was reported from 10 (other than drinks), and legumes are examples of marine food and
to show socioeconomic status score. plant proteins (beans and peas). Based on the distribution of reported
salt consumption (mg/d), we classified the individuals into 11 equal
groups and awarded corresponding scores ranging from 0 to 10
Assessment of dietary intake (higher score for less sodium consumed). Table 1 in the appendix
shows the specifics of the HEI-2015 scoring standards. The overall
An accurate and valid 168-item semi-quantitative food frequency HEI-2015 score ranges from 0 (no adherence) to 100 (complete
questionnaire (FFQ) was used to estimate typical dietary consumption adherence) (29).

TABLE 1 General characteristics of study participants across tertiles of HEI-2015 (n=490)1.

Variables Tertiles of HEI-2015 p2

T1 (n=173) T2 (n=160) T3 (n=157)
Age (y) 61.19 ± 9.56 62.94 ± 10.28 64.00 ± 9.39 0.03

Weight (kg) 74.63 ± 13.30 74.17 ± 11.90 73.02 ± 10.59 0.46

WC (cm) 99.11 ± 10.74 98.45 ± 9.44 97.06 ± 9.34 0.16

HC (cm) 104.77 ± 10.12 105.25 ± 9.97 102.44 ± 9.95 0.02

BMI (kg/m ) 2
28.09 ± 5.41 27.49 ± 4.19 26.94 ± 4.41 0.09

SES (score) 4.55 ± 1.88 4.69 ± 1.98 5.05 ± 1.95 0.07

Female, n (%) 99 (57.2%) 101 (63.1%) 90 (57.3%) 0.46

Married, n (%) 140 (88.1%) 126 (82.9%) 131 (89.1%) 0.23

Education, n (%) (≥diploma) 110 (64.0%) 102 (63.7%) 105 (66.9%) 0.81

Smokers, n (%) 17 (9.8%) 12 (7.5%) 14 (8.9%) 0.75

Physically active, n (%) (high) 54 (31.2%) 54 (33.8%) 49 (31.2%) 0.98

History of chronic disease, n (%) 118 (68.2%) 103 (64.4%) 101 (64.3%) 0.74

History of MACE, n (%) 109 (63.0%) 92 (57.5%) 90 (57.3%) 0.48

Supplements user, n (%) 63 (36.4%) 76 (47.5%) 85 (54.1%) 0.005

Blood pressure medication, n (%) 120 (71.9%) 106 (68.4%) 92 (59.7%) 0.06

Heart disease medication, n (%) 57 (34.1%) 47 (30.7%) 49 (31.8%) 0.80

Diabetic diets, n (%) (yes) 55 (31.8%) 58 (36.3%) 69 (43.9%) 0.07

WC, waist circumference; HC, hip circumference; BMI, body mass index; SES, socioeconomic status; MACE, major adverse cardiovascular events. 1All values are means ± standard deviation
(SD), unless indicated. 2Obtained from ANOVA for continuous variables and Chi-square test for categorical variables.

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Biochemical indices described methods using WC (m), BMI (kg/m2), and height (m)
as below:
In a fasting condition, common laboratory procedures were used
to measure fasting blood sugar (FBS), total cholesterol, high-density WC
ABSI = 2 1
lipoprotein cholesterol (HDL-c), low-density lipoprotein cholesterol BMI 3 × height 2
(LDL-c), and triglycerides (TG) (after 12–14 h overnight fasting). In a
seated posture, a physician measured the systolic (SBP) and diastolic
(DBP) blood pressures using a sphygmomanometer. 2
 WC 
 
2π 
BRI = 364.2 − 365.5 × 1 − (  )
Novel risk factor for cardiovascular disease ( 0.5height )2

By using LDL-C, HDL-C, and TG and following formula the

novel risk factor for cardiovascular disease like: CRI-1,CRI-2, LAP, 2 (WC ) + 0.7 (WC − hip )
2 2

AIP, and CI were obtained: AVI =

1000
TC
CRI − 1 =
HDL − C

Physical activity
LDL − C
CRI − 2 =
HDL − C
We utilized the International Physical Activity Questionnaire
(IPAQ) short form to measure physical activity levels (30). The IPAQ
consisted of seven questions. Overall, the questions assessed the
LAP = (WC − 65 ) × (TG ) for men
number of days and minutes spent participating in light and heavy
activities, as well as the average time spent walking and sitting during
the previous 7 days. Physical activity levels of 600 METs-min/week
LAP = (WC − 58 ) × (TG ) for women
were classed as low, 600–3,000 METs-min/week as moderate,
and > 3,000 METs-min/week as high.

CI = IF TF > 400 ( LDL − HDL + 1.5 ) × TG

Other variables
CI = IF TG < 400 ( LDL − HDL ) × TG We considered Five-point MACE for this study. Myocardial
infarction, stroke, hospitalization for heart failure, and revascularization
treatments, including angioplasty and bypass surgery, are all included
TG in the definition of Major Adverse Cardiac Events (MACE). Since
AIP = log
HDL − C we do not have CV death for our study population, we put it aside.
Patients were asked about their history of chronic diseases. Chronic
disease history includes Thyroid, blood pressure, cardiovascular disease,
Anthropometric indices chronic kidney disease, and chronic obstructive pulmonary disease.

Patients were weighed in light clothes and barefoot on a digital

scale (SECA, Hamburg, Germany) to the nearest 0.1 kg. Standing height Statistical analysis
was measured using a stadiometer set on the wall, with accuracy to
within 0.5 cm. Using a measuring tape, determine the waist First of all, subjects were classified based on tertiles of HEI-2015
circumference (WC) of the patient at the narrowest point, immediately scores (T1: 43–59; T2: 60–66; T3: 67–88). Baseline quantitative and
above the belly button. A dietician measured the hip circumferences of qualitative variables were compared across HEI tertiles by Analysis of
patients by placing a tape measure around the widest part of the hips. Variance (ANOVA) and Chi-square tests, respectively. Continuous
The following formulae were used to determine body mass variables were reported as mean (SD), and categorical variables were
index (BMI): shown as numbers and percentages. Dietary intakes of HEI
components and other nutrients were evaluated across HEI tertiles
Weight using Analysis of Covariance (ANCOVA). In this regard, total energy
BMI = 2
( height ) and macronutrient intakes were adjusted for age and gender, but other
nutrients were additionally controlled for energy (Kcal). The
associations of HEI with CVD risk factors and anthropometric indices
Body mass index is calculated as kg/m2. ABSI and BRI and were explored through binary logistic regression. Based on previous
abdominal volume index (AVI) were computed using previously investigations (31, 32), we considered ABSI, BRI, AVI, and AIP cut-off

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Zeinalabedini et al. 10.3389/fnut.2023.1201010

TABLE 2 Biochemical and anthropometric indices of study participants

points to be 0.08, 5.20, 17.30, and 0.11, respectively. Values above the across tertiles of HEI-2015 (n=490)1.
mentioned cut points were considered as the dependent variable in
this study. For other CVD risk factors (CRI-1, CRI-2, Cholindex, and Variables Tertiles of HEI-2015 p2
LAP), participants were categorized into tertiles of each variable. As T1 (n=173) T2 (n=160) T3 (n=157)
there is no specific cut-off point for these variables, the last tertile of
SBP (mmHg) 124.86 ± 14.17 127.02 ± 15.17 124.45 ± 16.76 0.25
each risk factor was considered the dependent variable in the logistic
regression. Odds ratios (ORs) and 95% confidence intervals (95% CIs) DBP (mmHg) 78.16 ± 6.63 77.56 ± 7.50 77.93 ± 9.42 0.78

were reported for the association of HEI with CVD risk factors and FBS (mg/dl) 157.53 ± 56.02 155.93 ± 64.89 154.59 ± 72.34 0.91
anthropometric indices in crude and adjusted models. In case of HbA1C (%) 8.17 ± 1.75 8.03 ± 1.69 7.85 ± 1.82 0.25
anthropometric indices, two multivariable-adjusted models were
TC (mg/dl) 153.01 ± 37.18 147.19 ± 36.66 148.20 ± 37.53 0.30
applied. For the first model, we controlled the confounding effects of
TG (mg/dl) 145.188 ± 62.72 145.09 ± 73.18 133.36 ± 52.88 0.16
age, gender. and energy intake. The second model was further adjusted
for smoking, socioeconomic status, chronic disease history, MACE HDL-C (mg/dl) 44.68 ± 10.78 43.31 ± 10.72 43.75 ± 10.35 0.48
history, diabetic diets, education level, marital status, physical activity, LDL-C (mg/dl) 78.70 ± 25.84 75.25 ± 26.76 77.14 ± 27.76 0.50
and supplement use. Considering CVD risk factors, we also included ABSI 0.08 ± 0.008 0.08 ± 005 0.08 ± 0.006 0.98
blood pressure and heart disease medications in the second model. (m11/6 kg−2/3)
Furthermore, an additional model (model 3) was considered for
BRI 5.76 ± 1.48 5.57 ± 0.97 5.43 ± 1.06 0.04
CVD risk factors in order to control the confounding effect of BMI as
well. The first tertile of HEI was considered the reference for all analyses. AVI 19.92 ± 4.33 19.61 ± 3.70 19.05 ± 3.61 0.12

The trend of ORs across tertiles of HEI was obtained by considering HEI CRI-I 3.48 ± 0.90 3.42 ± 0.93 3.42 ± 0.91 0.43
tertiles as an ordinal variable in the logistic regression models. All CRI-II 1.79 ± 0.66 1.73 ± 0.72 1.75 ± 0.69 0.62
statistical analyses were performed by SPSS software (version 26; SPSS
CI 0.87 ± 0.64 0.83 ± 0.66 0.86 ± 0.68 0.81
Inc., Chicago, IL). p < 0.05 was considered a significant level.
AIP 0.12 ± 0.21 0.13 ± 0.23 0.10 ± 0.20 0.58

LAP 63.12 ± 35.25 61.75 ± 35.50 55.15 ± 27.78 0.07

Results SBP, systolic blood pressure; DBP, diastolic blood pressure; FBS, fasting blood sugar; HbA1C,
hemoglobin A1C; TC, total cholesterol; TG, triglycerides; HDL-C, high density lipoprotein
cholesterol; LDL-C, low density lipoprotein cholesterol; ABSI, a body shape index; BRI, body
Patients’ socio-demographic roundness index; AVI, abdominal volume index; CRI-1, castelli index-I; CRI-II, castelli
characteristics index-II; CI, cholestrol index; AIP, atherogenic index of plasma; LAP, lipid accumulation
product. 1All values are means ± standard deviation (SD), unless indicated. 2Obtained from
ANOVA for continuous variables.
The study included 490 adults in total. Table 1 displays patient
socio-demographic characteristics based on HEI-2015 tertiles. The
mean age of the patients across the tertiles was 61.19, 62.94, and Participants in the highest tertile of the HEI-2015 consumed more
64 years (p = 0.03). The tertiles 1 group has the highest BMI, with a protein (p = 0.001), calcium, magnesium, fiber, vitamin B2, and
mean of 28.09 kg/m2. Most variables had no significant differences vitamin B9 (p < 0.001). There are no significant differences in the
between tertiles except for hip circumference (p = 0.02) and intake of certain nutrients, such as selenium (p = 0.47), vitamin B6
supplement user (p = 0.005). Of 490 individuals, 66.8% of patients (p = 0.55), and iron (p = 0.61; Table 3).
used blood pressure medication, and just 37.1% followed a
diabetic diet.
Cardiovascular risk factor and association
with healthy eating index
Biochemical and anthropometric indices of
participants In the crude model and after adjusting for potential confounders
such as age, energy, smoking, welfare, CDH, diabetic diet, BP
Table 2 describes patients’ biochemical, novel CVD risk factors, medication, and heart medication, patients who had more adherence
and anthropometric indices. SBP and DBP averaged to HEI had lower AIP (OR: 0.56; 95% CI: 0.34–0.94; p-trend =0.02)
125.44 ± 15.17 mmHg and 77.89 ± 7.88 mmHg, respectively. The first (Table 4).
tertile had the highest FBS and HbA1C, with mean values of For CRI-I, participants with more adherence to HEI had a lower
157.53 mg/dL and 8.17%, respectively. There are significant differences odds ratio of CRI-I (OR: 0.61; 95% CI: 0.38–1.00; p-trend = 0.05),
in BRI (p = 0.04) but only marginally in LAP (p = 0.07). although this signification disappeared after the adjustment.

Nutrients and food groups Anthropometric indices and association

with healthy eating index
Significant differences (p < 0.001) were observed in the weighted
proportions of participants who received the highest component score Participants who had higher adherence to HEI-2015 were 59%
on the HEI-2015 component. There was also identification of the fewer odds of BRI (95% CI: 0.37–0.94; p-trend = 0.02), and this
participant who received the least sodium (p = 0.05; Table 3). association was still significant after adjusting for all the confounders

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TABLE 3 Multivariable-adjusted intakes of selected nutrients and food groups of study participants across tertiles of HEI-2015 (n=490)1.

Variables Tertiles of HEI-2015 p2

T1 (n=173) T2 (n=160) T3 (n=157)
Energy (Kcal/d) 1678.90 ± 34.26 1670.12 ± 35.41 1583.34 ± 35.82 0.111

HEI-2015 components

Whole grains (Oz per 1,000 Kcal) 0.36± 0.04 0.88 ± 0.04 1.41 ± 0.04 <0.001

Refined grains (Oz per 1,000 Kcal) 6.36 ± 0.14 5.37 ± 0.14 4.64 ± 0.15 <0.001

Seafood and plant proteins (cups per 1,000 Kcal) 2.06 ± 0.052 2.24 ± 0.054 2.36 ± 0.054 <0.001

Sodium (grams per 1,000 kcal) 4.55 ±0.12 4.36 ± 0.12 4.79 ± 0.12 0.05

Dairy (cups per 1,000 kcal) 0.79 ± 0.03 0.93 ± 0.03 0.95 ± 0.03 <0.001

Greens and beans (cups per 1,000 kcal) 0.35 ±0.01 0.42 ± 0.01 0.44 ± 0.01 <0.001

Total vegetable (cups per 1,000 kcal) 1.39 ± 0.04 1.53 ± 0.04 1.74 ±0.04 <0.001

Whole fruit (cups per 1,000 kcal) 1.38 ± 0.03 1.55 ± 0.03 1.66 ± 0.03 <0.001

Total fruit (cups per 1,000 kcal) 1.41 ± 0.03 1.57 ± 0.03 1.67 ± 0.03 <0.001

Added sugar (% of energy) 5.87 ± 0.24 4.84 ± 0.25 3.50 ± 0.25 <0.001

MUFA/PUFA. ratio 1.76 ± 0.03 1.96± 0.03 2.27 ± 0.03 <0.001

Saturated fats (% of energy) 10.73 ± 0.16 9.82 ± 0.16 8.90 ± 0.16 <0.001

Macronutrients

Carbohydrates (% of energy) 56.13 ± 0.40 56.17 ± 0.42 56.03 ± 0.42 0.97

Proteins (% of energy) 12.32 ± 0.12 13.02 ± 0.12 13.47 ± 0.12 <0.001

Fats (% of energy) 34.00 ± 0.40 33.47 ± 0.42 33.21 ± 0.42 0.39

Other nutrients

Cholesterol (mg/d) 187.82 ± 6.09 198.37 ± 6.29 178.53 ± 6.38 0.087

Calcium (mg/d) 746.58 ± 16.02 846.26 ± 16.55 861.88 ± 16.78 <0.001

Selenium (mg/d) 0.05 ± 0.00 0.05 ± 0.00 0.05 ± 0.00 0.47

Iron (mg/d) 12.80 ± 0.19 13.03 ± 0.20 12.77 ± 0.20 0.61

Magnesium (mg/d) 198.69 ± 2.37 219.13 ± 2.44 226.02 ± 2.48 <0.001

Fiber (g/d) 13.38 ± 0.23 14.68 ± 0.23 15.95 ± 0.24 <0.001

Vitamin B1 (mg/d) 1.27 ± 0.01 1.26 ± 0.01 1.31 ± 0.01 0.08

Vitamin B2 (mg/d) 1.33 ± 0.02 1.48 ± 0.02 1.48 ± 0.02 <0.001

Vitamin B3 (mg/d) 13.63 ± 0.18 13.50 ± 0.18 14.06 ± 0.19 0.09

Vitamin B6 (mg/d) 1.15 ± 0.02 1.18 ± 0.02 1.18 ± 0.02 0.56

Vitamin B9 (mcg/d) 234.87 ± 4.25 255.78 ± 4.39 262.51 ± 4.45 <0.001

Vitamin B12 (mcg/d) 2.58 ± 0.07 2.86 ± 0.07 2.91 ± 0.07 0.003
1
All values are means ± standard error (SE); total energy and macronutrients intake are adjusted for age and gender; all other values are adjusted for age, gender, and energy intake. Obtained
2

from ANCOVA.

(OR: 0.52; 95% CI: 0.29–0.95; p-trend = 0.03). There was no signification being overweight (33). One concept is central obesity, and visceral fat
in other anthropometric indices like; ABSI and AVI (Table 5). has a role in developing CVD (34). The consequences of excessive
adiposity on the myocardial and vascular have a direct impact on
cardiac function (35).
Discussion The body roundness index (BRI) was created to evaluate the form
of the human body figure as an ellipse in order to forecast both body
In the present cross-sectional study of Iranian adult patients with fat and the proportion of visceral adipose tissue using WC in relation
type 2 diabetes, we discovered a significant positive relationship to height, which might be reduced by greater adhering to HEI (33, 36,
between maximal adherence to HEI-2015 and lower CRI-1 just in the 37). Improved dietary quality has been linked to a reduced prevalence
crude model, as well as a significant negative relationship between of CVD risk factors (38).
greater adherence to HEI-2015 and lower odds of AIP and BRI. The HEI Index measures the quality of food based on the dietary
Microvascular dysfunction was shown to be connected with type habits of the US population, and the highest score of HEI is for more
2 diabetes, and the likelihood of this condition was further raised by consumption of healthy nutrients and <8% saturated fat, sodium, and

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Zeinalabedini et al. 10.3389/fnut.2023.1201010

TABLE 4 Multivariable- adjusted odds ratio novel CVD risk factors across tertiles of HEI-2015 (n=490)1.

Variables Tertiles of HEI-2015 p-trend

T1 (n=173) T2 (n=160) T3 (n=157)
AIP

Crude 1.00 0.51 (0.32–0.82) 0.54 (0.34–0.87) 0.01

Model 1 1.00 0.53 (0.33–0.86) 0.56 (0.34–0.90) 0.01

Model 2 1.00 0.54 (0.33–0.88) 0.56 (0.33–0.93) 0.02

Model 3 1.00 0.55 (0.33–0.89) 0.56 (0.34–0.94) 0.02

Choline

Crude 1.00 0.84 (0.52–1.37) 0.94 (0.58–1.52) 0.81

Model 1 1.00 0.88 (0.53–1.45) 1.10 (0.67–1.80) 0.71

Model 2 1.00 0.90 (0.54–1.50) 1.04 (0.62–1.75) 0.88

Model 3 1.00 0.95 (0.57–1.59) 1.09 (0.64–1.84) 0.76

CRI-1

Crude 1.00 0.83 (0.51–1.34) 0.61 (0.38–1.00) 0.05

Model 1 1.00 0.89 (0.55–1.46) 0.69 (0.41–1.14) 0.15

Model 2 1.00 0.93 (0.56–1.54) 0.67 (0.39–1.15) 0.16

Model 3 1.00 0.97 (0.59–1.162) 0.96 (0.40–1.19) 0.20

CRI-2

Crude 1.00 0.87 (0.54–1.41) 0.76 (0.47–1.23) 0.27

Model 1 1.00 0.93 (0.57–1.51) 0.86 (0.53–1.42) 0.58

Model 2 1.00 0.96 (0.58–1.58) 0.77 (0.46–1.31) 0.36

Model 3 1.00 0.97 (0.59–1.61) 0.78 (0.46–1.34) 0.39

LAP

Crude 1.00 1.04 (0.64–1.69) 0.74 (0.45–1.22) 0.26

Model 1 1.00 1.02 (0.62–1.67) 0.75 (0.45–1.24) 0.28

Model 2 1.00 1.08 (0.65–1.77) 0.84 (0.49–1.43) 0.57

Model 3 1.00 1.20 (0.71–2.03) 0.90 (0.51–1.59) 0.77

AIP, atherogenic index of plasma; CRI-1, Castelli risk index-1; CRI-2, Castelli risk index 2; LAP, lipid accumulation product. Model 1: adjusted for age, gender, energy intake. Model 2: further
adjustment for smoking, socioeconomic status, chronic disease history, history of MACE, having diabetic diets, education, marital status, physical activity, blood pressure medications, heart
disease medications, and supplement use. Model 3: more adjustments for BMI. 1All values are odds ratios and 95% confidence intervals.

added sugar (29). According to a previous study, abdominal fat may cholesterol levels, including LDL-C, due to its positive association
accumulate in response to higher dietary SFA intakes (39). with the lipoprotein particle size, cholesterol esterification rates, and
Therefore, greater adherence to HEI-2015 could enormously remnant lipoproteinemia (48, 49). In addition to being a strong
improve abdominal obesity. Although we could not find a predictor of atherosclerosis and coronary heart disease, AIP also
significant statically relation to other anthropometric indices but faithfully portrays the connection between protective and atherogenic
clinically higher HEI might reduce abdominal obesity, which lipoproteins, especially in type 2 diabetes (50).
aligns with other studies’ results (40–42). In contrast, some studies Our findings showed that HEI-2015 was negatively associated
were inconsistent with our results, and several failed to observe any with AIP and that a higher HEI-2015 score corresponds to a larger
association (43, 44). diet of nuts and beans and a lower intake of SFA. Although Altamimi
Researchers have identified plasma lipid profiles as a significant et al. (51) reported that nuts, particularly walnuts, hazelnuts, and
risk factor and predictor of cardiovascular disease (CVD) in recent pistachios, lead to an effective increase in HDL levels, Nora et al. (52)
years (13). Atherosclerosis is brought on by dyslipidemia, found no significant difference in TC, HDL, and LDL in the group that
characterized by a rise in low-density lipoprotein cholesterol (LDL-C), consumed 69 g nuts/day compared to the control group in a 16-week
total cholesterol, triglycerides (TG), and a decrease in HDL-C (45). study of obese and overweight people.
LDL-C was formerly thought to be a primary therapy goal. Yet, once The content of isoflavones and lecithin in soy and nuts can cause
LDL-C dropped to the required levels, around half of the remaining a decrease in LDL and an increase in HDL. Isoflavones may increase
cardiovascular risks persisted, leading researchers to identify new HDL-cholesterol production in the liver and ameliorate dyslipidemia
CVD predictors (46). by suppressing adipogenesis (53) and activating lipoprotein lipase (54).
The atherogenic index of plasma (AIP) (47) has been proposed as According to our findings, adherence to a healthy eating pattern
a marker of plasma atherogenicity in addition to individual serum decreased about 40% of the risk of CRI-1. This signification vanished

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Zeinalabedini et al. 10.3389/fnut.2023.1201010

TABLE 5 Multivariable- adjusted odds ratio novel anthropometrics across tertiles of HEI-2015 (n=490)1.

Variables Tertiles of HEI-2015 p-trend

T1 (n=173) T2 (n=160) T3 (n=157)
ABSI

Crude 1.00 1.54 (0.8–2.64) 1.20 (0.71–2.01) 0.47

Model 1 1.00 1.50 (0.86–2.61) 1.03 (0.60–1.77) 0.84

Model 2 1.00 1.62 (0.92–2.85) 1.17 (0.66–2.07) 0.52

AVI

Crude 1.00 1.15 (0.69–1.91) 0.82 (0.50–1.34) 0.44

Model 1 1.00 1.13 (0.68–1.89) 0.81 (0.49–1.34) 0.43

Model 2 1.00 1.91 (0.70–2.01) 0.98 (0.57–1.68) 0.97

BRI

Crude 1.00 0.88 (0.55–1.42) 0.59 (0.37–0.94) 0.02

Model 1 1.00 0.69 (0.39–1.21) 0.42 (0.24–0.74) 0.003

Model 2 1.00 0.73 (0.41–1.30) 0.52 (0.29–0.95) 0.03

ABSI, a body shape index; AVI, abdominal volume index; BRI, body roundness index. Model 1: adjusted for age, gender, energy intake. Model 2: further adjustment for smoking,
socioeconomic status, chronic disease history, history of MACE, having diabetic diets, education, marital status, physical activity, and supplement use. 1All values are odds ratios and 95%
confidence intervals.

after adjusting by potential confounders. This indicator is based on and, in addition, different components of HEI to establish the
three significant lipid profile parameters: TC, LDL-C, and HDL-C, relationship between HEI and CVD risk factors.
and it’s determined as the ratio of TC/HDL-C. Since CRI-1 reflect the
modification of a crucial component of vascular risk—the decline in
levels of the protective cholesterol fraction, HDL-C, at the expense of Data availability statement
the rise in TC and specifically the risk fraction, LDL-C—they have a
predictive value for CVD that is greater than that of the isolated data The raw data supporting the conclusions of this article will
of the lipid profile (55). be made available by the authors, without undue reservation.
This might be because a higher intake of vegetables, fruits, whole
grains, low-fat dairy products, and total protein, which is in a higher
score HEI, could strongly improve lipid profile (23, 56). Also, Studies Ethics statement
showed that a higher score of HEI is strongly related to higher HDL,
which could be decreased the risk of CRI-1 (22, 56, 57). However, The studies involving human participants were reviewed and
Rashidipour-Fard et al. found a statistically significant positive approved by the Human Ethical Committee of Tehran University of
correlation between HDL-C and HEI scores in their cross-sectional Medical Science [IR.TUMS.MEDICINE.REC.1400.185]. The patients/
study. However, after accounting for age, sex, calorie consumption, participants provided their written informed consent to participate in
and BMI, it changed to a non-significant level (23). this study.
The current studies have many strengths. To the best of our
knowledge, this is the first observational study investigating the
relationship between HEI and novel anthropometrics-related CVD Author contributions
risk factors and CVD risk factors among type 2 diabetes. The sample
size of this research is sufficient to support our findings. Also, we used MZ, LA, AE, and EN-E designed the study. EN-E supported the
a valid and accurate FFQ to gather nutritional data, adjusting for many analysis of the CVD risk factors. MZ carried out the study and
possible confounders, and in-depth interviews with participants analyzed the data. MZ and LA interpreted the findings, drafted the
conducted by professional nutritionists. manuscript, and revised the final manuscript. AE commented on the
There is a considerable limitation that could affect our result. presentation of data and his comments improved the quality of the
Firstly, we have not seen the odds of the ratio of CVD risk factors in paper significantly. He also commented on the different parts of the
different components of HEI groups. Also, the healthy eating index is study and reviewed the paper scientifically and edited the paper for
a proxy for overall quality and does not account for quantity. It is language errors. All authors contributed to the article and approved
impossible to characterize a causality relationship given the study’s the submitted version.
cross-sectional design.
In conclusion, our finding shows that adherence to HEI-2015
reduces about 50% of the risk of AIP and BRI among diabetic patients. Funding
Further, these findings need to be confirmed by large-scale cohort
studies in Iran that include patients of various racial and ethnic This study was supported by the Tehran University of Medical
backgrounds. In addition, consider the patient’s body composition Sciences (grant number: 9911468002).

Frontiers in Nutrition 08 frontiersin.org

Zeinalabedini et al. 10.3389/fnut.2023.1201010

Conflict of interest organizations, or those of the publisher, the editors and the
reviewers. Any product that may be evaluated in this article, or
The authors declare that the research was conducted in the claim that may be made by its manufacturer, is not guaranteed or
absence of any commercial or financial relationships that could endorsed by the publisher.
be construed as a potential conflict of interest.

Supplementary material
Publisher’s note
The Supplementary material for this article can be found online
All claims expressed in this article are solely those of the at: https://www.frontiersin.org/articles/10.3389/fnut.2023.1201010/
authors and do not necessarily represent those of their affiliated full#supplementary-material

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