Introduction
Dyslipidemia, marked by an imbalance in lipid profiles, is a well-known contributor to atherosclerosis and cardiovascular diseases (CVDs). The World Health Organization (WHO) identifies CVDs as a leading cause of death, accounting for 7.9 million deaths each year. The prevalence of lipid profile abnormalities is increasing globally. Elevated levels of low-density lipoprotein cholesterol (LDL-C) and reduced levels of high-density lipoprotein cholesterol (HDL-C) promote plaque accumulation in arteries, increasing the risk of atherosclerotic CVD. Lipoprotein ratios, such as total-C/HDL-C and LDL-C/HDL-C, and the logarithm of the triglyceride (TG)/HDL-C ratio, are strong predictors of CVD incidence and atherosclerosis severity. Atherosclerosis is characterized by inflammatory cells and factors involved in the initiation, progression, and formation of atherosclerotic plaques. Dietary factors can modulate and reduce systemic inflammation. Certain dietary patterns, like Mediterranean and prudent diets, or high intakes of fruits, vegetables, whole grains, polyunsaturated fatty acids, fiber, and polyphenols, are associated with lower levels of inflammatory biomarkers and endothelial activation, reducing the risk of CVD and atherosclerosis. Conversely, Western diets high in saturated fatty acids, red and processed meats, desserts, sugary drinks, and low-fiber foods are linked to increased inflammatory biomarkers. The Dietary Inflammatory Index (DII) is a tool used to assess the inflammatory potential of dietary components based on their pro- and anti-inflammatory properties. Studies have shown that higher DII scores are associated with adverse health outcomes. Dietary modifications are crucial in reducing the economic and clinical burden of dyslipidemia. The DII can evaluate overall inflammation related to nutritional patterns.
Dietary Inflammatory Index and its Association with Dyslipidemia
Recent research has focused on the connection between the Dietary Inflammatory Index (DII) and various health outcomes, particularly in relation to noncommunicable diseases and mortality. Studies have consistently shown that higher DII scores are associated with negative impacts on health. However, there is limited research on the relationship between DII and lipoprotein ratios, especially in developing Middle Eastern countries. Given that lipoprotein ratios are often better predictors of cardiovascular risk than individual lipid profiles in these regions, understanding this association is crucial.
Study Design and Methods
To investigate the relationship between DII scores and dyslipidemia, a study was conducted using data from 8870 adults aged 35-65 years who participated in the Ravansar Noncommunicable Diseases Cohort Study (RaNCD), part of the Prospective Epidemiological Research Studies in Iran (PERSIAN). Data were collected from adults who completed dietary interviews, excluding individuals with extreme energy intakes, cancer, pregnancy, or incomplete information. Dietary data were collected using a validated food frequency questionnaire that assessed the consumption of 118 food items. The inflammatory potential of the diet was evaluated using the DII, which scores dietary constituents based on their inflammatory properties. Lipid profile measurements, including triglyceride (TG), total cholesterol (TC), LDL cholesterol (LDL-c), and high-density lipoprotein cholesterol (HDL-c), were used to calculate atherogenic indices such as the atherogenic index of plasma (AIP), Castelli's index-I (CRII), Castelli's index-II (CRIII), the lipoprotein combination index (LCI), and the atherogenic coefficient (AC). Anthropometric data, physical activity levels, sociodemographic information, smoking status, blood pressure, and fasting blood glucose levels were also collected. Statistical analyses were performed to determine the associations between DII scores, dyslipidemia, and atherogenic risk scores.
Calculation of DII Score
The DII was calculated using 31 available food parameters from the FFQ of the 45 possible food variables composing the DII: retinol, beta-carotene, pyridoxine, cobalamin, ascorbic acid, calciferol, tocopherol, folic acid, niacin, thiamine, riboflavin, iron, zinc, selenium, magnesium, omega 3, omega 6, total fat, saturated fats (SFAs), cholesterol, monounsaturated fatty acids (MUFAs), polyunsaturated fatty acids (PUFAs), fiber, protein, total fat, carbohydrate and energy, caffeine, onion, garlic, and tea.
Lipid Profile and Atherogenic Indices
Lipoprotein ratio measurements were calculated as AIP: log (TG/HDL-C), AC: ((TC- HDL-C)/HDL-C), CRI-I: (TC/HDL-C), CRI-II: (LDL-C/HDL-C) and LCI: (TCTGLDL-C)/HDL-C. Dyslipidemia was defined as LDL-C ≥ 160 mg/dL and/or TC ≥ 240 mg/dL and/or HDL-C < 40 mg/dL and/or TG > 200 mg/dL.
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Anthropometric and Physical Activity Data
Weight, height, body mass index (BMI), waist-to-hip ratio (WHR), visceral fatty acid (VFA), and percentage of body fat (PBF) were collected and analyzed in this study. Physical activity levels were evaluated according to the PERSIAN cohort self-reported questionnaire, and participants' responses were measured in terms of the metabolic equivalent of task per hour per day (MET/h per day). Physical activity was categorized into three levels: low (24-36.5 MET/hour per day), moderate (36.6-44.4 MET/hour per day) and high (≥ 44.5 MET/hour per day)
Study Results
The study found that participants with dyslipidemia had greater pro-inflammatory scores than those with a normal lipid profile. Those with dyslipidemia also had higher BMI, WHR, VFA, and blood pressure. Additionally, dyslipidemic individuals had higher CRII, CRIII, LCI, AIP, and AC scores. Participants in the highest DII quartile had lower intakes of saturated fat, dairy products, calcium, and selenium, but greater intakes of energy, protein, MUFAs, PUFAs, whole grains, fruits, vegetables, red and white meat, legumes, eggs, fibers, nuts, vitamin E, vitamin A, vitamin D, vitamin K, vitamin C, vitamin B6, vitamin B12, magnesium, zinc, and iron. A higher DII was associated with higher TG, CRII, CRIII, LCI, AC, and AIP. Participants in the upper DII quartile had lower HDL-C and TC levels than those in the lower quartile. There was a direct association between DII and the risk of dyslipidemia. After adjusting for confounding factors, the risk of dyslipidemia significantly increased across DII quartiles. The DII was positively associated with atherogenic indices, with higher DII scores correlating with greater atherogenic indices.
Detailed Findings on Dietary Intake and DII
In the highest quartile of the DII, the intake of saturated fat, dairy products, calcium, and selenium was lower than that in the lowest quartile. Conversely, individuals in the higher DII quartile had significantly greater intakes of energy, protein, MUFAs, PUFAs, whole grains, fruits, vegetables, red and white meat, legumes, eggs, fibers, nuts, vitamin E, vitamin A, vitamin D, vitamin K, vitamin C, vitamin B6, vitamin B12, magnesium, zinc, and iron. There were no statistically significant differences in carbohydrate or fat consumption across the DII quartiles.
Lipid Profile and Atherogenic Indices Across DII Quartiles
A higher DII was related to higher TG, CRII, CRIII, LCI, AC and AIP in patients in the highest DII quartiles than in those in the lowest DII quartile. Participants in the upper quartile had lower levels of high-density lipoprotein cholesterol (HDL-C) and total cholesterol (TC) than those in the lower quartile.
Association Between DII and Dyslipidemia Risk
There was a direct association between DII and the risk of prevalent dyslipidemia according to the crude odds ratios (ORs). After adjustment for age and sex, a higher DII was associated with a greater likelihood of dyslipidemia. According to the fully adjusted logistic regression models and after adjustment for participant age, sex, smoking status, alcohol consumption status, physical activity, SBP, DBP, FBS, BMI and SES, the risk of dyslipidemia significantly increased by 24% (OR: 1.24, 95% CI 1.08-1.41), 7% (OR: 1.07, 95% CI 0.94, 1.21) and 3% (OR: 1.03, 95% CI 0.91, 1.16) in quartile 4, quartile 3 and quartile 2 of the DII, respectively, compared with the first quartile.
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Linear Relationship Between DII and Atherogenic Indices
The linear regression model showed that the DII was positively associated with atherogenic indices (CRII, CRIII, LCI, AC and AIP). In the highest DII quartile, atherogenic indices were significantly greater than those in the lowest quartile according to both unadjusted and adjusted models. A DII in the fourth quartile compared with the first quartile was positively associated with a higher risk of CRII (β = 0.11, CI 0.05, 0.18), CRIII (β = 0.06, CI 0.01, 0.11), LCI (β = 0.11, CI 288.12, 8373.11), AC (β = 0.11, CI 0.05, 0.17) and AIP (β = 0.06, CI 0.02, 0.10) according to the fully adjusted linear regression model.
Importance of Diet on Atherosclerosis
Coronary heart disease (CHD) secondary to atherosclerosis is the leading cause of mortality worldwide. The Mediterranean diet, characterized by the intake of unsaturated fats, is associated with low rates of fatal CHD. Replacing saturated fat with unsaturated fats, especially polyunsaturated fat, is effective in reducing CHD through anti-atherosclerotic mechanisms. Nuts, rich in bioactive phytochemicals and polyunsaturated fatty acids, are an integral part of the Mediterranean diet and other healthy plant-based diets.
Nuts and Atherosclerosis
In a randomized controlled crossover trial, short-term replacement of saturated fat with polyunsaturated and monounsaturated fats significantly improved atherogenic risk factors. In the PREDIMED trial, subjects receiving a Mediterranean diet supplemented with mixed nuts showed delayed plaque progression compared to those advised to follow a low-fat diet.
Effects of Walnut Supplementation on Atherosclerosis
To test whether sustained isocaloric inclusion of nuts within an unhealthy saturated fat-rich diet prevents the progression of unstable atheroma plaques, a study was conducted using a mouse model of accelerated atherosclerosis. Male apolipoprotein E-deficient (Apoe−/−) mice were randomized to receive either a control diet (CD), a palm oil-based high-fat diet (PO HFD), or a palm oil + walnuts high-fat diet (PO + W HFD) for 15 weeks. The PO + W HFD contained 3% (w/w) of walnuts. Feed intake was significantly lower in PO + W HFD than in the CD and PO HFD groups. Although there were no statistically significant differences among groups for lesion extension along the aorta or mean maximal lesion area, there was a protective effect of the walnut diet on several histology-assessed predictors of plaque stability, namely the content of lipid, collagen, macrophages, VSMC, and calcified areas. Atherosclerotic lipid deposition in PO HFD was significantly higher than in CD, while walnut inclusion prevented such increase. Plaques from PO + W HFD mice had a significantly higher presence of total collagen when compared to the other groups. Atherosclerotic lesions of mice receiving walnuts also showed lower macrophage content. Von Kossa staining revealed the presence of calcified deposits in the neointima of atherosclerotic lesions of PO HFD and PO + W HFD mice, being significantly higher in PO HFD than CD.
Fermentable Carbohydrates and Atherosclerosis
Fermentable carbohydrates such as pectin and inulin have health benefits in obesity comorbidities. Pectin and inulin are not digested by endogenous enzymes in the small intestine but are available in the large intestine for fermentation by microbiota. The resulting fermentation products are short-chain fatty acids (SCFAs) such as acetate and propionate. Pectin and inulin may lead to a shift in the composition of the microbiota, such as an increase in bifidobacteria. SCFAs have positive effects such as immune and inflammation regulation. Studies in humans and pigs have reported a cholesterol-lowering effect of pectin and inulin supplementation. Supplementing high-fat diets with inulin slowed body weight gain in pigs.
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Atherogenic Diet and Fermentable Carbohydrates
To investigate whether fermentable carbohydrates such as pectin and inulin can mitigate cardiovascular risk factors in pigs as a model for obese humans, a study was conducted using forty-eight healthy Saddleback pigs. The pigs were randomly divided into four feeding groups: atherogenic diet (AD), atherogenic diet + 5% pectin (ADp), atherogenic diet + 5% inulin (ADi), and conventional diet (CD). The three groups (AD, ADp, and ADi) received an atherogenic diet that contained high amounts of saturated fatty acids, sugar, and salt. All diets were analyzed for crude nutrient and fiber fractions. Dry matter (DM) was determined after oven-drying (103°C). Crude nutrient contents were assayed using the Weende system. Serum triglyceride (TG), bile acids (BA), hepatic triglyceride lipase (LIPC), cholesterol (CHOL), alkaline phosphatase (ALP), aspartate aminotransferase (AST), gamma-glutamyl transferase (GGT), lactate dehydrogenase (LDH) and amylase (AMYL) levels were analyzed using an automated chemistry analyzer. Metabolomic analysis was performed using NMR spectroscopy. The amount of CL was determined in pooled fecal samples from the four feeding groups (AD, ADp, ADi, and CD) and at each sampling point (t0-t3). The arterial sections were stained by Movat`s Pentachrome to quantify the size of the vascular lesions. Additionally, LAD sections were stained with Oil red to visualize lipids and with Von Kossa staining to detected vascular calcification. Independent of supplementation, significant changes were observed in lipid metabolism, such as an increase in triglycerides, bile acids, and cholesterol in serum, in all groups fed atherogenic diets in comparison to the conventional group. Serum metabolome analysis showed differentiation of the feeding groups by diet (atherogenic versus conventional diet) but not by supplementation with pectin or inulin. Cardiovascular lesions were found in all feeding groups and in the baseline group. Supplementation of pectin or inulin in the atherogenic diet had no significant impact on cardiovascular lesion size.
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