Review Article | Open Access
Brenda Kelly Souza Silveira, Thatianne Moreira Silva Oliveira, Patrícia Amaro Andrade, Helen Hermana Miranda Hermsdorff, Carla de Oliveira Barbosa Rosa, Sylvia do Carmo Castro Franceschini, "Dietary Pattern and Macronutrients Profile on the Variation of Inflammatory Biomarkers: Scientific Update", Cardiology Research and Practice, vol. 2018, Article ID 4762575, 18 pages, 2018. https://doi.org/10.1155/2018/4762575
Dietary Pattern and Macronutrients Profile on the Variation of Inflammatory Biomarkers: Scientific Update
It is known that the dietary pattern and macronutrients profile may influence the expression and secretion of inflammatory biomarkers, and the low-grade inflammation is associated with the manifestation of noncommunicable chronic diseases. Therefore, this review aimed to present and discuss the role of dietary patterns and macronutrients on the variation of inflammatory markers related to NCD risk. Scientific evidences within the last five years based on clinical trials, case-controls, cohorts, and cross-sectional studies indicate that normocaloric, carbohydrate-moderated, low-glycemic index, protein-moderated, monounsaturated and polyunsaturated fatty acid-rich, omega-3, and low-saturated fat diets display positive effects on the inflammatory state, both in healthy individuals and in those with cardiovascular risk, although the second group seems to benefit more from changes in the dietary profile.
Low-grade inflammation refers to a series of metabolic and physiological modifications with proinflammatory cytokines and increased oxidative stress . It is related to the development and grievance of noncommunicable chronic diseases (NCD), and one of the factors associated with the low-grade inflammation is the intake of foods with proinflammatory characteristics [2, 3].
The dietary pattern may be defined as a combination of foods frequently consumed by individuals and population groups . The importance of dietary pattern analysis lies in the fact that the observed effect for a given nutrient or food in environmentally controlled investigations differs from the effect found within the context of different dietary patterns routinely adopted by populations .
Indeed, some dietary patterns, such as the Mediterranean and DASH (Dietary Approach to Stop Hypertension) diets, are associated with an improved weight control and lower incidence of NCD [6, 7] so that they have been employed as reference or “healthy” diets by the scientific literature and clinical-nutritional practice. Furthermore, the dietary pattern has been investigated as a potential modulator of inflammatory markers . Thus, the adoption of healthy dietary patterns distinguished by high intake of fruits, vegetables, and low intake of sugar and fats (saturated and trans) seems to decrease the risk of NCD through its influence on the related low-grade inflammation [7, 9].
On the other hand, the impact of the distribution of macronutrients—carbohydrates, proteins, and lipids—on the inflammatory state has been extensively investigated [10–15], whilst the amount and origin of the nutrients ingested have played an important role in the development of the low-grade inflammation . Therefore, this review aimed to present and discuss the role of dietary patterns and macronutrients on the variation of inflammatory markers related to NCD risk.
2. Materials and Methods
For this review, the electronic databases PubMed (National Library of Medicine, Bethesda, MD) and ScienceDirect were researched. The following keywords were used for article search: “dietary fat”; “fatty acids,” “omega-3,” “saturated fat,” “olive oil,” “dietary patterns,” “dietary protein,” and “dietary carbohydrate” always combined with the MeSH terms “inflammation” or “inflammatory markers.” The search was limited to English studies published between March 2012 and April 2017. The inclusion criteria considered original studies published within the last 5 years, in English, which assessed the relation of dietary pattern and macronutrients profile on the variation of inflammatory biomarkers, in observational or interventional study designs. Review papers, editorials and book chapters, case reports, studies with animals or cells, studies that did not aim to evaluate the inflammation, studies that used supplements with registered mark, and studies that assessed the relation between inflammation and diseases other than diabetes, dyslipidemia, metabolic syndrome, obesity, and cardiovascular diseases were excluded from the present review.
Initially, 9429 papers were found. Of these, 9183 papers were excluded after title and abstract screening, and 246 papers were fully read. Of these, 40 papers met the inclusion criteria and were kept for this review (Table 1). In order to complement the discussion, other papers related to the issue addressed were used, despite the year of publication.
3. Results and Discussion
3.1. Dietary Patterns
The dietary patterns analysis helps to understand the factors that contribute to NCD [17, 18]. Therefore, in the last decades, several authors have been dedicated to investigate the association between dietary patterns and indices that evaluate the quality of the diet with inflammatory markers instead of investigating isolated nutrients [3, 19, 20]. The analysis of dietary pattern can be a priori, when a score is attributed to the diet according to previous knowledge concerning dietary disease health outcomes, or a posteriori, when statistical techniques are used to explore new patterns .
Among a priori techniques, several indexes have already been developed, such as the Mediterranean Diet Score , Healthy Eating Index , Diet Quality Index , and Dietary Inflammatory Index . Briefly, these indexes assess the conformity of individuals’ diet to guidelines and dietary recommendations by assigning an interpretable score and have been adapted to make improvements and meet the specificities of each population [26–28].
On the other hand, the cluster and factor analyses are the most frequently used a posteriori techniques [29, 30]. They allow, respectively, to group individuals with similar food intake or to establish standards from correlating foods. Both approaches, a priori and a posteriori, have limitations and positive aspects, so there is no better technique and they are used to investigate different questions .
Regardless of the approach used, it is a consensus that dietary patterns deemed healthy displays as an inverse relationship with the concentrations of inflammatory biomarkers [5, 31, 32]. Dietary patterns that potentially combat the inflammatory state and reduce the risk for NCD are characterized by the elevated intake of vegetables, green leaves, whole grain cereals, fruits, chestnuts, fish and olive oil, low consumption of embedded meat, sugary drinks, processed foods, and saturated fat [33, 34].
In this context, Corley et al.  defined two types of dietary patterns: the “Mediterranean diet pattern” and the “conscious consumption pattern,” which involves higher fruit consumption and low consumption of meat, eggs, and liqueurs. Inverse associations were observed between fibrinogen and Mediterranean diet. In turn, the individuals who obtained higher scores in the “conscious consumption pattern” displayed lower serum concentrations of C-reactive protein (CRP) (≤3 mg/L). In this study, both patterns were considered healthy, thus reaffirming the importance of diversifying foods for health maintenance. For the elderly, a higher consumption of fruits, vegetables, fowl, fish, and low-fat dairy products is related to lower systemic inflammation .
On the other hand, in the study by Bédard et al.  with an adult population, the introduction of a dietary pattern in the Mediterranean diet was monitored during a four-week period, with the purpose of evaluating potential modifications in the serum concentrations of CRP. Men who displayed elevated CRP concentrations (≥2 mg/L) showed a reduction in concentrations during the study, while an increase was observed in men who presented normal concentrations (<2 mg/L). In general terms, this study did not report effective results by the Mediterranean diet, which may be related to the reduced follow-up time, diet composition, and control of variables that might have influenced the participants’ inflammatory state. Hermsdorff et al.  conducted an intervention with adult individuals during eight weeks, in which the adherence to the Mediterranean diet occasioned reduction in the CRP concentrations as well as other inflammatory markers. These results corroborate other interventional studies [36, 37], thus indicating the anti-inflammatory role of the Mediterranean pattern.
In turn, the occidental dietary pattern, characterized by the excessive intake of calories, salt, fat, and sugar, has been associated with the increase of low-grade inflammation and with the development of the NCD [38, 39]. Within the adult population, the following patterns were identified: “pastas,” “sandwich,” “starchy vegetables,” “sugary drinks,” “dessert,” “breads,” “fowl,” “frozen food,” “alcoholic beverage,” and “pizza.” After the analysis of the inflammatory markers, all patterns displayed elevated CRP (>3 mg/L) at the same time as the highest average was that of the “frozen food” pattern .
A similar effect was observed in the study by Kong et al. , who evaluated the food intake of overweight individuals, whereas three dietary patterns were identified, according to similarity groups: “high intake of sugar, fat, and salt” (Group 1), “higher intake of water, yogurt, cereals, eggs, and chestnuts” (Group 2), and “higher intake of fruits, yogurts, soups, and lower sugar intake” (Group 3). Differences regarding the inflammatory markers—CRP and interleukin 6 (IL-6)—were not observed between the groups. However, after the evaluation of the concentrations of CD136—a transmembrane protein found in the adipose tissue, with anti-inflammatory function—Group 3 displayed higher concentrations.
Similarly, when considering the foods altogether, we can stablish how anti- or proinflammatory a diet can be [8, 41]. In this context, Ozawa et al.  conducted a study with adults and gave factorial weights to the foods, thus indicating how pro- or anti-inflammatory they were. From this distribution, participants’ diets were assessed, and those who reported dietary patterns considered inflammatory (higher consumption of red meat and processed and fried foods), consequently displayed higher IL-6 levels. The interconnection between nutrients and health should not be assessed in isolation, once it is known that nutrients from the foods act synergistically in the body and may interact with each other .
The foods included in a diet may directly influence the individual’s health. Fruits and vegetables are foods that, when consumed on a daily basis in an adequate amount, are capable of reducing the oxidative stress and low-grade inflammation markers [9, 43].
Lee et al. , after studying an adult population, identified different dietary patterns, named “coffee pattern,” “fruit pattern,” “meat pattern,” and “vegetable pattern.” The individuals with a higher score for the “vegetable pattern” displayed a lower CRP concentration, as well as a higher antioxidant intake. A similar result was reported by McGeoghegan et al. , who identified two dietary patterns: “1” and “2”, these being the ones with higher and lower antioxidant and anti-inflammatory loads, respectively. Pattern “1” was inversely associated with the CRP concentrations and lower prevalence of diabetes.
It is known that fruits and vegetables have various bioactive and antioxidant compounds [45–47] and that, when associated with whole grains, fish, and lean meat, may reduce the risk factors with respect to the development of several diseases . This association was verified in the study by Abete et al. , who investigated a population of healthy individuals with a history of stroke and identified the patterns named “healthy” and “not healthy.” Healthy individuals showed higher adherence to the “healthy” pattern and displayed lower CRP concentrations. In addition, the adherence to the “healthy” pattern was a protective factor for the development of stroke.
The studies presented in this review (Table 2) showed the importance of an integral nutrition, particularly to base health promotion actions. The adherence to patterns deemed healthy, such as the Mediterranean diet, and patterns that included fruits and vegetables and reduced intake of processed food has been associated with the reduction of inflammatory and systemic markers, as well as with the risk of NCD . Therefore, it is possible to verify that a balanced and varied nutrition, rich in natural foods and with the least amount of processed foods, is capable of reducing the low-grade inflammation and associated diseases. In addition, it was possible to observe that the dietary patterns identified display similar characteristics and effects, regardless of the population, thus highlighting the importance of assessing the cumulative associations of certain groups of foods.
FFQ: Food Frequency Questionnaire; IL-6: interleukin 6; CRP: C-reactive protein; sDC14: differentiation cluster 14; DC163: differentiation cluster 163; LPS: lipopolysaccharide.
The proportion and type of fats included in the diet influence the degree of inflammation and the risk of NCD. In this context, the intake of polyunsaturated fatty acids (PUFA), particularly the long-chain ones from the w-3 series (n-3 PUFA), is related to the reduction of the risk of cardiovascular diseases and death due to its anti-inflammatory potential [51–54]. Diets high in monounsaturated fatty acids (MUFA) have also been highlighted for their potential in reducing inflammation due to the lower expression of genes related to the synthesis of IL-6 [10, 55].
Saturated fatty acids (SFA), on the other hand, favor the increase of inflammation. Most studies included in this review related the consumption of SFA to the increase of inflammatory markers and NCD. Kantor et al. , in a retrospective cohort with elderly, observed that the lower ingestion of SFA was associated with the reduction of CRP in eutrophic and overweight groups, but not in obese, thus suggesting that the modulating role of the SFAs in the CRP concentrations is mediated by the individual’s nutritional state. Lesná et al.  found reduction of CRP and IL-8 in a three-week randomized crossover study, after replacement of an SFA-rich diet (42% of the total caloric value “TCV”) by a PUFA-rich diet (40% of the TCV). The increase in the expression of proinflammatory cytokines associated with the consumption of SFA is due to the activation of toll-like receptors (TLR), in particular, the TLR-4. Therefore, transcription factors such as the factor nuclear kappa B (NF-κβ) are stimulated, resulting in the synthesis of proinflammatory cytokines [8, 58].
Silver et al.  investigated the effect of a hyperlipidemic diet (50% of the TCV), with equal proportions of MUFA, PUFA, and SFA, on overweight individuals, and observed, after two weeks, an increase of 6% in fat oxidation, an average reduction of 2.5 kg of body fat, an average increase of 2.5 kg of lean mass, and a reduction in the interleukins IL-1α, IL-1β, 1L-12, and IL-17, besides interferon gamma (IFN-γ), tumor necrosis factor-alpha (TNF-α), and tumor necrosis factor-beta (TNF-β) concentrations and improvement in vascular function. In this context, hypolipidemic diets may not be the best strategy to reduce NCD, as the fatty acids profile (MUFA, PUFA, and SFA) is more relevant for modulating the inflammation than the proportion of total lipids in the diet. In addition, diets with higher lipid content are more palatable and provide greater satiety and better weight control .
With respect to the linolenic acid, an intervention with type-2 diabetics resulted in reduction in the IL-2 concentrations and TNF-α after n-3 supplementation (eicosapentaenoic “EPA” 1.548 mg/d; docosahexaenoic “DHA” 828 mg/d; and others n-3 338 mg/d) during eight weeks, although CRP levels were maintained . Rajkumar et al.  reported an improvement in the proinflammatory profile with CRP reduction in overweight patients after n-3 supplementation (EPA 180 mg/d and DHA 120 mg/d) during six weeks. Ito et al.  observed the same effect with dyslipidemic individuals. In turn, Itariu et al.  verified a reduction in the gene expression of inflammatory biomarkers in the subcutaneous adipose tissue, a reduction in IL-6 concentration, and increased anti-inflammatory eicosanoids in the visceral adipose tissue, after n-3 supplementation (EPA 460 mg/d and DHA 380 mg/d) during eight weeks. In another study, the authors observed a CRP reduction after eight weeks of n-3 supplementation (EPA 720 mg and DHA 480 mg) in men with coronary artery disease .
Accordingly, the beneficial mechanism of the linoleic acid (n-3 series) has been related to its derivatives, the EPA C20 : 5 n-3 and DHA 22 : 6 n-3 acids, which have a higher anti-inflammatory effect than the derivatives of the arachidonic acid (AA n-6 PUFA) derived from the linoleic acid (n-6 series). Such a effect was reported in a study with adults, in which an increase was reported in the formation of EPA and DHA after four months of supplementation (1.4 g/d) in comparison with the placebo group (soy oil), although with no changes in AA metabolites . Hence, the cause of reduction in inflammation was the synthesis of anti-inflammatory metabolites, rather than the suppression of proinflammatory metabolites derived from the AA.
However, investigations about the effect of n-3 lipids on NCD-related biomarkers reported contradictory findings. The cardiometabolic risk of the sample population seems to influence the results, as the beneficial effects are more evident in individuals with more than one risk factor, rather than excessive body fat alone [67, 68]. Studies in which the population had metabolic syndrome (MS), diabetes mellitus (DM), and/or dyslipidemia [32, 61, 63] reported more pronounced results in the improvement of proinflammatory biomarkers than studies with individuals who were overweight only, with no other associated diseases/risk factors [67–69]. Indeed, some studies did not find evidences that justify the n-3 supplementation [67, 68, 70–72]. Dewell et al.  assessed the effect of a low- (2.2 g/d) and high-dose (6.6 g/d) plant-derived n-3 supplementation, compared to the low- (1.2 g/d) and high-dose (3.6 g/d) sea-derived n-3 supplementation but did not find differences between the groups for IL-6 and soluble intercellular adhesion molecule-1 (sICAM-1), after eight weeks. Nigam et al.  assessed the effect of n-3 supplementation (4 g/d) during 271 ± 129 days on average and reported that, after 6 months, the reduction of CRP and myeloperoxidase (MPO) was similar to that observed in the placebo group. Darghosian et al.  also observed the maintenance of IL-6, IL-8, IL-10, TNF-α, and monocyte chemoattractant protein after 6 months of n-3 supplementation (4 g/d). Different proportions of n-3 in the diet did not affect the IL-6, monocyte chemoattractant protein-1 (MCP-1), concentrations TNF-α 1 and 2 receptors, and PCR, after 14 weeks of n-3-rich diet (3.5% of TCV), compared to the group with a diet poor in n-3 (0.5% of TCV) .
The differences observed in the inflammatory profile may be related to variations in the intervention time and in the supplemented daily dose. The daily doses used varied between 1 and 6.6 g/d, whereas doses above 3 g/d were less common. Another aspect worth considering is the origin of fatty acids of the n-3 series, which may be plant or sea-derived. Only one study included in this review, conducted by Dewell et al.  assessed the effect of different n-3 sources, although a beneficial effect was not found in any of the inflammatory markers evaluated, regardless of the dose or source. However, since most of the studies did not find evidences of health damage caused by n-3 supplementation and most of them reported benefits from its use, the usual intake of foods that are source of n-3 may be a strategy to reduce risk or grievance of diseases associated with the inflammation, particularly in patients with chronic diseases, whereas the use of supplementation demands further investigation.
Furthermore, the relation between linoleic (CLA) and linolenic (LNA) acid intake is very important for homeostasis . After being ingested and absorbed, these fatty acids are metabolized and underwent elongation, desaturation, and retroconversion reactions. The action of cyclooxygenase and lipooxygenase enzymes on these fatty acids leads to the formation of different eicosanoids (prostaglandins, leukotrienes, thromboxanes, etc.), whereas the derivatives of the n-3 series are more anti-inflammatory and those of the n-6 series are more proinflammatory. The importance of balance for the n-3 : n-6 ratio is due to the fact that the desaturase δ-6 enzyme has greater affinity with LNA than with CLA. Therefore, in order to avoid an imbalance in the production of anti- and proinflammatory eicosanoids, studies suggest that the CLA ratio in the diet is greater than the LNA ratio, whereas the appropriate ratio is around 4 to 5 : 1 and not superior to 10 : 1 .
In its turn, the extravirgin olive oil, mainly composed by MUFA (w-9 series)—oleic acid—has reduced the risk of NCD when used as supplement or consumed within the context of healthy dietary patterns . Martínez-González et al.  reported a reduction in the risk of atrial fibrillation in individuals with high risk of cardiovascular disease, after intervention with Mediterranean diet supplemented with extravirgin olive oil. In another study, individuals with cardiovascular risk submitted to the Mediterranean diet supplemented with 50 ml/day of extravirgin olive oil reduced the CRP, IL-6, sICAM, and P-selectin concentrations, when compared to the control group, which was provided with a hypolipidemic diet . Ceriello et al.  also compared the effect of hypolipidemic and Mediterranean diets, although without oil supplementation, and reported that, after three months, there was a reduction of IL-6, intercellular adhesion molecule 1 (ICAM-1), and 8-isoprostaglandin F2α (8-iso-PGF2α) only in the group to whom the Mediterranean diet was offered.
Nevertheless, the concentration of phenolic compounds in the oil, capable of reducing the synthesis of AA and cyclooxygenase enzymes 1 and 2 (COX-1 and COX-2), may be a key factor in its potential to reduce inflammatory markers. Camargo et al.  compared the effect of three meals prepared with virgin oil classified according to the content of phenolic compounds as high (398 ppm), intermediate (149 ppm), and low (70 ppm). The participants who were provided with meals with high content of phenolic compounds displayed greater reduction in the IL-6, IL-1, and CXC motif chemokine ligand (CXCL) expression than the other groups. Indeed, oil consumption is associated with a lower inflammation degree, particularly in the context of the Mediterranean diet, and its use indicates an important nutritional strategy for the reduction of cardiovascular diseases .
The large number of studies devoted to investigate the relation between lipids and inflammation highlights the importance of this macronutrient to the modulation of several inflammatory biomarkers (Table 3). Thus, the literature indicates that adjusting the proportion of SFA, MUFA, and PUFA in the diet is a more effective strategy to modulate the inflammation than the use of hypolipidemic diets, which may play the inverse role. In addition, the higher SFA consumption is related to the increase of inflammatory biomarkers, and this increase is proportional to the ingested amount. Thus, choosing foods rich in MUFA and PUFA and avoiding foods with high SFA content may be beneficial, with respect to the modulation of the inflammation and reduction of the risk of diseases associated with it. Among the alternatives, it is possible to highlight the consumption of extravirgin olive oil with high phenolic compounds content, which supports not only the reduction of inflammation but also the improvement of the endothelial function. Despite the high number of studies available, there is still limited information about the influence of the nutritional state in the modulation of lipids on the inflammation, since obese individuals seem to be less responsive to the benefits of an adequate lipidic distribution.
M: men; W: women; BMI: body mass index; SFA: saturated fatty acids; CRP: C-reactive protein; n-3: omega-3; sICAM-1: soluble intercellular adhesion molecule-1; IL: interleukin; IFN-γ: interferon gamma; TNF-α: tumor necrosis factor alpha; EPA: eicosapentaenoic acid; DHA: docosahexaenoic acid; DM: diabetes mellitus; AA: arachidonic acid; DGLA: dihomo-gamma-linolenic acid; ALA: alpha-linolenic acid; CXCL: chemokine (C-X-C motif) ligand; PGF2α: prostaglandin F2α; PAI-1: plasminogen activator inhibitor-1; CVD: cardiovascular disease; MUFA: monounsaturated fatty acids; PUFA: polyunsaturated fatty acids.
3.3. Proteins, Carbohydrates, and Glycemic Index
Proteins are the macronutrients of greatest thermogenic effect due to their high cost of metabolic synthesis, hydrolysis, gluconeogenesis, and excretion as urea . In addition, the protein content of the diet may lead to increased satiety and decrease in calorie intake [80, 81].
The effects on human health arising from the ingestion of several protein types have been investigated, although their association with metabolic diseases is still conflictive . A study with a Mediterranean population, particularly from Greece, who consumed diets based on plants, vegetables, fruits, and cereals, shortly after World War II, reported lower mortality rates from cardiovascular diseases, due to the low amounts of protein in relation to heme-iron . Nevertheless, in the context of a western diet, a high iron bioavailability was reported, mainly because of the ingestion of heme-iron-related animal protein, which favors an anti-inflammatory state .
Currently, iron has been reported as a promoter of atherosclerosis due to its ability to produce free radicals . According to Vallianou et al. , in their study with 490 middle-aged Caucasian adults who were apparently healthy—in which they evaluated the protein ingestion of the diet, taking into account the animal and vegetable protein—the serum concentration of cystatin C decreased as the frequency of animal protein increased and the platelet count decreased with the increase of vegetable protein intake, whereas no association was found with monocytes, lymphocytes, and CRP. The influence of protein in the diet on postprandial inflammation is still uncertain. Arya et al.  reported that, in healthy individuals, meat with high fat content is more proinflammatory, in comparison with lean meat, in relation to TNF-α and IL-6.
Azadbakht and Esmaillzadeh  verified that the consumption of red meat was related to higher plasma concentrations of CRP in women. Cocate et al. , in a study with 296 men between 40 and 59 years of age, observed a higher occurrence of central obesity, hypertriglyceridemia, and metabolic syndrome in individuals within the first tertile of BCAA (branched-chain amino acids) and leukin consumption, in comparison with those from the second and third tertiles; besides, the higher BCAA and leukin consumption has been considered a protective factor for central obesity and metabolic syndrome. In addition, in another study with the same sample, Cocate et al.  verified that the increased consumption of red meat was associated with a higher occurrence of metabolic syndrome and hypertriglyceridemia. Furthermore, a cross-sectional study with 553 individuals aged between 18 and 80 years verified that the consumption of processed meat showed positive association with IL-6, TNF-α, TNF-R1, and TNF-R2, even after adjusting for consumption of fruits and vegetables. In turn, the consumption of unprocessed red meat was inversely associated with TNF-R1 and TNF-R2 . Thus, the higher protein and amino acid intake from red meat is directly related to cardiometabolic diseases, whereas the variation of inflammatory markers also seems to be involved.
Dairy products are also a food group deemed as an important protein source. Hence, Zemel et al.  found an inverse relationship between the consumption of dairy products and inflammation, both in overweight and obese individuals. In a randomized case-control study, which assessed the relationship between different protein sources, the authors observed that, after intervention, there were lower CC5—chemokine binding to the chemotactic monocyte-1 protein, which facilitates adherence and transmigration of monocytes through the arterial wall, thus leading to an inflammatory process—concentrations in individuals who consumed whey, in comparison with those who consumed cod and casein, in addition to lower CC5 concentrations in individuals who consumed gluten, in comparison to those who consumed cod . In turn, MCP-1 displayed higher values in individuals who consumed whey, in comparison to those who consumed cod and gluten, which can be explained by specific milk properties, such as increased insulin response, as whey is more insulinotropic than cod, gluten, and casein protein. As a general result, whey showed better anti-inflammatory effects, which suggest that this protein source is relevant for the modulation of inflammatory biomarkers.
Amini et al. , in a study with 56 Iranian women, engaged in physical activities, found a marginally significant decrease in the CRP concentrations after intervention, both in the hyperproteic (HP) and the balanced (B) diets. This finding, which, unlike the others, did not find any advantage of the HP diet, may be justified by the effect of physical activity, and not only the diets, as a protective factor.
In addition to the studies that assessed the amount and quality of protein associated with the NCD and chronic subclinical inflammation, the quality and amount of carbohydrates or the glycemic index have been highlighted within the scientific literature (Table 4). Cross-sectional studies have demonstrated an inverse association between the intake of whole-grain carbohydrates and low-grade inflammation . However, recent studies about the replacement of refined whole-grain wheat products were inconclusive . Therefore, in general, the consumption of whole-grain products is inversely related to inflammation.
BMI: body mass index; kg/m²: kilogram per square meter; FFQ: Food Frequency Questionnaire; CRP: C-reactive protein; M: men; W: women; CCL5: CC chemokine ligand-5; MCP-1: monocyte chemoattractant protein-1; MS: metabolic syndrome; GI: glycemic index; CVD: cardiovascular disease; LP: low protein; LGI: low glycemic index; HGI: high glycemic index; HP: high protein; kcal: kilocalorie; GGT: gamma glutamyl transferase; IL-6: interleukin 6; GI: glucose intolerance; ox-LDL: oxidized low-density lipoprotein; TNF-α: tumor necrosis factor-α; TNF-α-R1: tumor necrosis factor receptor 1; TNF-α-R2: tumor necrosis factor receptor 2; B: balanced.
For example, Montonen et al. , in a study with 2198 individuals from the European Prospective Investigation into Cancer and Nutrition (EPIC), observed an inverse correlation between the consumption of whole bread and CRP and gamma-glutamyl transferase (GGT) values, as well as a direct correlation between the consumption of red meat and the same inflammatory markers.
With respect to simple carbohydrates, its elevated consumption is worrying, especially when added in foods and drinks, thus favoring the inflammatory state and negative health effects. The World Health Organization (WHO) recommends that children and adults reduce the sugar intake to <10% of total energy, and that this value should be lowered over lifetime .
In this context, a study with eutrophic individuals, aged between 20 and 80 years, which aimed to determine the effect of the chronic fructose (55%) consumption, sucrose, and honey on glucose-tolerant (GT), as well as glucose-intolerant (GI) individuals, reported that the GI group displayed serum CRP concentrations > 3 mg/L before and after intervention, and these values were lower to those observed in the acute inflammation, which may indicate an increased risk of cardiometabolic disease . CRP concentrations of the GT group were normal (<3.0 mg/L), although there was a nonsignificant increase after the intervention. IL-6 values were also greater in the GI group. Aeberli et al.  observed a CRP elevation after isolated fructose, glucose, or sucrose consumption, while it is important to highlight that the sucrose dose was higher than that of the previous study (80 versus 50 g/d), as was the intervention period (2 versus 3 weeks).
Another study with obese individuals reported higher CRP and lower adiponectin, following hyperglycemic (59–67% of TCV) diets . In turn, hyperglycemic (10–13% of TCV) diets lead to a decrease in the IL-6 concentrations . However, other studies did not report relationships between the amount of carbohydrates and adiponectin , IL-6, and CRP concentrations .
In turn, with respect to the studies with adults, which associate the ingestion of protein and carbohydrates/glycemic index to the ingestion of hyperproteic (10–15% of TCV), HP (23–28% of TCV) , low-glycemic index (LGI), high-glycemic index (HGI) , HP + HGI, HP + LGI, LP + HGI, and LP + LGI, in relation to the inflammation, the authors observed that HP diets increased, while B diets decreased, the CRP levels, respectively.
Studies that assessed the effects of GI and protein intake on the inflammatory markers in children are scarce. The study Diet, Obesity, and Genes (Diogenes), found an increase in body fat in children who consumed a HP + HGI diet, whilst the percentage of overweight children decreased in the group who consumed the HP + LGI test diet . In this same study, a decrease was observed in children and adolescents’ CRP between 5 and 18 years of age who consumed a LGI diet . This is in contrast with the study by Diogenes with adults, in which CRP concentrations decreased in individuals who consumed hyperproteic diet with HGI . This may be explained by the lower diet adherence by the families and by the fact that the decrease of GI reached less than 4 difference points after the nutritionists’ assistance to the families within the study .
Thus, it is possible to acknowledge that the lower consumption of protein from red meat and the higher consumption of proteins from vegetables, white meat, and milk displayed beneficial health effects and may lead to the decrease of inflammatory markers. However, there is still lack of consistent information about the effect of protein origin and amount on the inflammation, particularly in healthy people. With respect to GI and carbohydrates, results indicate that the moderate ingestion of carbohydrate, as well as of food with LGI, may have a beneficial effect on the metabolic and inflammatory states in obese individuals, while in children and adolescents, the LGI displayed an inverse effect.
From this literature review, we reiterated the importance of a varied diet, rich in natural foods and poor in processed foods, such as some previously known patterns (Mediterranean and DASH diets) to prevent and improve low-grade inflammation. With respect to the macronutrients, the provided consumption of PUFAs and MUFAs, as replacements for SFA (moderate intake of carbohydrates, in particular the ones with low glycemic index, and the consumption of proteins, in particular the ones of plant origin and white meats), may positively influence the modulation of low-grade inflammation and, consequently, has a protective effect for the development of the NCD.
However, further studies are necessary, in order to evaluate the inflammatory response to the consumption of dietary patterns or intake of specific macronutrients in different situations of weight, age, and metabolic condition, for a better understanding of the most appropriate dose-response.
Conflicts of Interest
Helen Hermana Miranda Hermsdorff and Sylvia do Carmo Castro Franceschini are fellows of National Council for Scientific and Technological Development (CNPq) Research Productivity. The funding received did not lead to any conflicts of interest. Also, there are no other conflicts of interest regarding the manuscript.
The authors are grateful to Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for the grants conceded to Brenda Kelly Souza Silveira, Thatianne Moreira Silva Oliveira, and Patrícia Amaro Andrade. This review is supported by the FAPEMIG (State of Minas Gerais, Brazil) and CNPq, related to research team’s projects. HHM Hermsdorff and SDCC Franceschini are CNPq fellows.
- S. B. Heymsfield and T. A. Wadden, “Mechanisms, pathophysiology, and management of obesity,” New England Journal of Medicine, vol. 376, no. 3, pp. 254–266, 2017.
- M. M. Bibiloni, C. Maffeis, I. Llompart, A. Pons, and J. A. Tur, “Dietary factors associated with subclinical inflammation among girls,” European Journal of Clinical Nutrition, vol. 67, no. 12, pp. 1264–1270, 2013.
- J. Meyer, A. Doring, C. Herder, M. Roden, W. Koenig, and B. Thorand, “Dietary patterns, subclinical inflammation, incident coronary heart disease and mortality in middle-aged men from the MONICA/KORA Augsburg cohort study,” European Journal of Clinical Nutrition, vol. 65, no. 7, pp. 800–807, 2011.
- U. M. Devlin, B. A. Mcnulty, A. P. Nugent, and M. J. Gibney, “The use of cluster analysis to derive dietary patterns : methodological considerations, reproducibility, validity and the effect of energy mis-reporting,” Proceedings of the Nutrition Society, vol. 71, no. 4, pp. 599–609, 2012.
- L. C. Kong, B. A. Holmes, A. Cotillard et al., “Dietary patterns differently associate with inflammation and gut microbiota in overweight and obese subjects,” PLoS One, vol. 9, no. 10, Article ID e109434, 2014.
- F. Sacks, L. P. Svetkey, W. M. Vollmer et al., “Effects on blood pressure of reduced dietary sodium and the dietary approaches to stop hypertension (Dash) diet,” New England Journal of Medicine, vol. 344, no. 1, pp. 3–10, 2001.
- R. Casas, E. Sacanella, M. Urpí-Sardà et al., “The effects of the Mediterranean diet on biomarkers of vascular wall inflammation and plaque vulnerability in subjects with high risk for cardiovascular disease. A randomized trial,” PLoS One, vol. 9, no. 6, Article ID e100084, 2014.
- J. Bressan, H. H. M. Hermsdorff, M. Á. Zulet, and J. A. Martínez, “Hormonal and inflammatory impact of different dietetic composition: emphasis on dietary patterns and specific dietary factors,” Arquivos Brasileiros de Endocrinologia & Metabologia, vol. 53, no. 5, pp. 572–581, 2009.
- P. G. Cocate, A. J. Natali, A. de Oliveira et al., “Fruit and vegetable intake and related nutrients are associated with oxidative stress markers in middle-aged men,” Nutrition, vol. 30, no. 6, pp. 660–665, 2014.
- J. Bressan and H. H. M. Hermsdorff, “The obesity epidemic, the cause, the treatment,” in Atenção Nutricional: Abordagem dietoterápica em adulto, E. A. M. Moreira and P. G. Chiarello, Eds., pp. 75–97, Guanabara Koogan, Rio de Janeiro, Brazil, 2008.
- J. Goletzke, A. E. Buyken, G. Joslowski et al., “Increased intake of carbohydrates from sources with a higher glycemic index and lower consumption of whole grains during puberty are prospectively associated with higher IL-6 concentrations in younger adulthood among healthy individuals,” Journal of Nutrition, vol. 144, no. 10, pp. 1586–1593, 2014.
- A. Bédard, B. Lamarche, L. Corneau, S. Dodin, and S. Lemieux, “Sex differences in the impact of the Mediterranean diet on systemic inflammation,” Nutrition Journal, vol. 14, no. 1, p. 46, 2015.
- J. Corley, J. A. M. Kyle, J. M. Starr, G. McNeill, and I. J. Deary, “Dietary factors and biomarkers of systemic inflammation in older people: the Lothian Birth Cohort 1936,” British Journal of Nutrition, vol. 114, no. 7, pp. 1088–1098, 2015.
- K. Okreglicka, “Health effects of changes in the structure of dietary macronutrients intake in Western societies,” Roczniki Państwowego Zakładu Higieny, vol. 66, no. 2, pp. 97–105, 2015.
- M. Ozawa, M. Shipley, M. Kivimaki, A. Singh-Manoux, and E. J. Brunner, “Dietary pattern, inflammation and cognitive decline: The Whitehall II prospective cohort study,” Clinical Nutrition, vol. 36, no. 2, pp. 506–512, 2017.
- G. Pang, J. Xie, Q. Chen, and Z. Hu, “Energy intake, metabolic homeostasis, and human health,” Food Science and Human Wellness, vol. 3, no. 3-4, pp. 89–103, 2014.
- M. B. Schulze, K. Hoffmann, J. E. Manson et al., “Dietary pattern, inflammation, and incidence of type 2 diabetes in women,” American Journal of Clinical Nutrition, vol. 82, no. 3, pp. 675–684, 2005.
- E. Lopez-Garcia, M. B. Schulze, T. T. Fung et al., “Major dietary patterns are related to plasma concentrations of markers of inflammation and endothelial dysfunction,” American Journal of Clinical Nutrition, vol. 80, no. 4, pp. 1029–1035, 2004.
- A. Drewnowski, E. C. Fiddler, L. Dauchet, P. Galan, and S. Hercberg, “Diet quality measures and cardiovascular risk factors in France: applying the healthy eating index to the SU.VI.MAX study,” Journal of the American College of Nutrition, vol. 28, no. 1, pp. 22–29, 2009.
- J. A. Nettleton, L. M. Steffen, M. B. Schulze et al., “Associations between markers of subclinical atherosclerosis and dietary patterns derived by principal components analysis and reduced rank regression in the Multi-Ethnic Study of Atherosclerosis (MESA),” American Journal of Clinical Nutrition, vol. 85, no. 6, pp. 1615–1625, 2007.
- J. Reed, E. Wirfalt, A. Flood et al., “Comparing 3 dietary pattern methods–cluster analysis, factor analysis, and index analysis–with colorectal cancer risk: the NIH-AARP Diet and Health Study,” American Journal of Epidemiology, vol. 171, no. 4, pp. 479–487, 2010.
- A. Trichopoulou, A. Kouris-Blazos, M. L. Wahlqvist et al., “Diet and overall survival in the elderly,” BMJ, vol. 311, no. 7018, pp. 1457–1460, 1995.
- E. T. Kennedy, J. Ohls, S. Carlson, and K. Fleming, “The healthy eating index: design and applications,” Journal of the American Dietetic Association, vol. 95, no. 10, pp. 1103–1108, 1995.
- R. E. Patterson, P. S. Haines, and B. M. Popkin, “Diet quality index: capturing a multidimensional behavior,” Journal of the American Dietetic Association, vol. 94, no. 1, pp. 57–64, 1994.
- P. P. Cavicchia, S. E. Steck, T. G. Hurley et al., “A new dietary inflammatory index predicts interval changes in serum high-sensitivity,” Journal of Nutrition, vol. 139, no. 12, pp. 2365–2372, 2009.
- D. P. S. Fernandes, A. Q. Ribeiro, M. S. L. Duarte, and S. C. C. Franceschini, “Systematic review of Healthy Eating Indexes in adults and elderly: applicability and validity,” Nutrición Hospitalaria, vol. 32, no. 2, pp. 510–516, 2015.
- P. M. Guenther, K. O. Casavale, J. Reedy et al., “Update of Healthy Eating Index: HEI-2010,” Journal of the Academy of Nutrition and Dietetics, vol. 113, no. 4, pp. 569–580, 2013.
- S. Kim, P. S. Haines, A. M. Siega-Riz, and B. M. Popkin, “The Diet Quality Index-International (DQI-I) provides an effective tool for cross-national comparison of diet quality as illustrated by China and the United States,” Journal of Nutrition, vol. 133, no. 11, pp. 3476–3484, 2003.
- R. Villegas, Y. B. Xiang, H. Cai et al., “Lifestyle determinants of C-reactive protein in middle-aged, urban Chinese men,” Nutrition, Metabolism, and Cardiovascular Diseases, vol. 22, no. 3, pp. 223–230, 2012.
- A. L. Anderson, T. B. Harris, F. A. Tylavsky et al., “Dietary patterns, insulin sensitivity and inflammation in older adults,” European Journal of Clinical Nutrition, vol. 66, no. 1, pp. 18–24, 2012.
- K. Esposito, R. Marfella, M. Ciotola et al., “Effect of a Mediterranean-style diet on endothelial dysfunction and markers of vascular inflammation in the metabolic syndrome: a randomized trial,” JAMA, vol. 292, pp. 1440–1446, 2004.
- Y. Lee, D. Kang, and S.-A. Lee, “Effect of dietary patterns on serum C-reactive protein level,” Nutrition, Metabolism and Cardiovascular Diseases, vol. 24, no. 9, pp. 1004–1011, 2014.
- A. Trichopoulos, T. Costacou, C. Barnia, and D. Trichopoulos, “Adherence to a Mediterranean diet and survival in a Greek population,” New England Journal of Medicine, vol. 348, no. 26, pp. 2599–2608, 2003.
- E. Denova-Gutierrez, K. L. Tucker, M. Flores, J. Salmeron, and S. Barquera, “Dietary patterns are associated with predicted cardiovascular disease risk in an Urban Mexican adult population,” Journal of Nutrition, vol. 146, no. 1, pp. 90–97, 2016.
- H. H. Hermsdorff, M. Á. Zulet, I. Abete, and J. A. Martinez, “Discriminated benefits of a Mediterranean dietary pattern within a hypocaloric diet program on plasma RBP4 concentrations and other inflammatory markers in obese subjects,” Endocrine, vol. 36, no. 3, pp. 445–451, 2009.
- R. Casas, E. Sacanella, M. Urpí-Sardà et al., “Long-term immunomodulatory effects of a Mediterranean diet in adults at high risk of cardiovascular disease in the PREvención con DIeta MEDiterránea randomized controlled trial,” Journal of Nutrition, vol. 146, no. 9, pp. 1684–1693, 2016.
- J. L. Marques-Rocha, F. I. Milagro, M. L. Mansego, M. A. Zulet, J. Bressan, and J. A. Martínez, “Expression of inflammation-related miRNAs in white blood cells from subjects with metabolic syndrome after 8 wk of following a Mediterranean diet–based weight loss program,” Nutrition, vol. 32, no. 1, pp. 48–55, 2016.
- I. A. Myles, “Fast food fever: reviewing the impacts of the Western diet on immunity,” Nutrition Journal, vol. 13, no. 1, p. 61, 2014.
- S. Devaraj, J. Wang-Polagruto, J. Polagruto, C. L. Keen, and I. Jialal, “High-fat, energy-dense, fast-food–style breakfast results in an increase in oxidative stress in metabolic syndrome,” Metabolism, vol. 57, no. 6, pp. 867–870, 2008.
- M. F. Kuczmarski, M. A. Mason, D. Allegro, M. A. Beydoun, A. Zonderman, and M. K. Evans, “Dietary quality and nutritional biomarkers associated with dietary patterns of socioeconomically diverse Urban African American and white population,” Procedia Food Science, vol. 4, pp. 104–113, 2015.
- H. Xu, P. Sjogren, J. Arnlov et al., “A proinflammatory diet is associated with systemic inflammation and reduced kidney function in elderly adults,” Journal of Nutrition, vol. 145, no. 4, pp. 729–735, 2015.
- C. A. de Carvalho, P. C. A. Fonsêca, L. N. Nobre, S. E. Priore, and S. C. C. Franceschini, “Methodologies for identifying a posteriori eating patterns in Brazilian children: a systematic review,” Ciência & Saúde Coletiva, vol. 21, no. 1, pp. 143–154, 2016.
- H. H. Hermsdorff, M. Á. Zulet, B. Puchau, and J. A. Martínez, “Fruit and vegetable consumption and proinflammatory gene expression from peripheral blood mononuclear cells in young adults: a translational study,” Nutrition and Metabolism, vol. 7, no. 1, 42 pages, 2010.
- L. Mcgeoghegan, C. R. Muirhead, and S. Almoosawi, “Association between an anti-inflammatory and anti-oxidant dietary pattern and diabetes in British adults : results from the national diet and nutrition survey rolling programme years,” International Journal of Food Sciences and Nutrition, vol. 67, no. 5, pp. 553–561, 2016.
- T. E. Crane, C. Kubota, J. L. West, M. A. Kroggel, B. C. Wertheim, and C. A. Thomson, “Increasing the vegetable intake dose is associated with a rise in plasma carotenoids without modifying oxidative stress or inflammation in overweight or obese postmenopausal women,” Journal of Nutrition, vol. 141, no. 10, pp. 1827–1833, 2011.
- A. Cassidy, G. Rogers, J. J. Peterson, J. T. Dwyer, H. Lin, and P. F. Jacques, “Higher dietary anthocyanin and flavonol intakes are associated with anti-inflammatory effects in a population of US adults,” American Journal of Clinical Nutrition, vol. 102, no. 1, pp. 172–181, 2015.
- C. L. A. Coelho, H. H. M. Hermsdorff, and J. Bressan, “Anti-inflammatory properties of orange juice : possible favorable molecular and metabolic effects blood pressure,” Plant Foods for Human Nutrition, vol. 68, no. 1, pp. 1–10, 2013.
- E. Mertens, O. Markey, J. M. Geleijnse, J. A. Lovegrove, and D. I. Givens, “Adherence to a healthy diet in relation to cardiovascular incidence and risk markers : evidence from the Caerphilly Prospective Study,” European Journal of Nutrition, 2017, [published online ahead of print March 14, 2017].
- I. Abete, M. A. Zulet, E. Goyenechea et al., “Association of lifestyle, inflammatory factors, and dietary patterns with the risk of suffering a stroke: a case–control study,” Nutritional Neuroscience, vol. 21, no. 1, pp. 70–78, 2016.
- Y. Gu, J. Nieves, J. Luchsinger, and N. Scarmeas, “Dietary inflammation factor rating system and risk of Alzheimer’s disease in elders,” Alzheimer Disease and Associated Disorders, vol. 25, no. 2, pp. 149–154, 2011.
- R. Dhingra, L. Sullivan, P. F. Jacques et al., “Soft drink consumption and risk of developing cardiometabolic risk factors and the metabolic syndrome in middle-aged adults in the community,” Circulation, vol. 116, no. 5, pp. 480–488, 2007.
- O. S. Al-Attas, N. M. Al-Daghri, M. S. Alokail et al., “Association of dietary fatty acids intake with pro-coagulation and inflammation in Saudi Adults,” Asia Pacific Journal of Clinical Nutrition, vol. 23, no. 1, pp. 55–64, 2014.
- J.-Y. Hwang, W. S. Kim, S. Jeong, and O. Kwon, “Evidence-based estimation of health care cost savings from the use of omega-3 supplementation among the elderly in Korea,” Nutrition Research and Practice, vol. 9, no. 4, p. 400, 2015.
- M. Linecker, P. Limani, F. Botea et al., “A randomized, double-blind study of the effects of omega-3 fatty acids (Omegaven™) on outcome after major liver resection,” BMC Gastroenterology, vol. 15, no. 1, p. 102, 2015.
- R. S. Gomide and H. H. M. Hermsdorff, “Mediterranean diet and its benefits in chronic non-communicable diseases,” Nutrição em Pauta, vol. 20, pp. 29–33, 2012.
- E. D. Kantor, J. W. Lampe, M. Kratz, and E. White, “Lifestyle factors and inflammation: associations by body mass index,” PLoS One, vol. 8, no. 7, Article ID e67833, 2013.
- I. K. Lesná, P. Suchánek, E. Brabcová, J. Kovář, H. Malínská, and R. Poledne, “Effect of different types of dietary fatty acids on subclinical inflammation in humans,” Physiological Research, vol. 62, no. 2, pp. 145–152, 2013.
- S. Navarro, E. D. Kantor, X. Song et al., “Factors associated with multiple biomarkers of systemic inflammation,” Cancer Epidemiology Biomarkers and Prevention, vol. 25, no. 3, pp. 521–531, 2016.
- H. J. Silver, H. Kang, C. D. Keil et al., “Consuming a balanced high fat diet for 16 weeks improves body composition, inflammation and vascular function parameters in obese premenopausal women,” Metabolism, vol. 63, no. 4, pp. 562–573, 2014.
- V. O. Polacow and A. H. Lancha Junior, “Hyperglycemia diets: effects of isoenergetic replacement of fat by carbohydrates on lipid metabolism, body adiposity and its association with physical activity and the risk of cardiovascular disease,” Arquivos Brasileiros de Endocrinologia & Metabologia, vol. 51, no. 3, pp. 389–400, 2007.
- A. Malekshahi Moghadam, A. Saedisomeolia, M. Djalali, A. Djazayery, S. Pooya, and F. Sojoudi, “Efficacy of omega-3 fatty acid supplementation on serum levels of tumour necrosis factor-alpha, C-reactive protein and interleukin-2 in type 2 diabetes mellitus patients,” Singapore Medical Journal, vol. 53, no. 9, pp. 615–619, 2012.
- H. Rajkumar, N. Mahmood, M. Kumar, S. R. Varikuti, H. R. Challa, and S. P. Myakala, “Effect of probiotic (VSL#3) and omega-3 on lipid profile, insulin sensitivity, inflammatory markers, and gut colonization in overweight adults: a randomized, controlled trial,” Mediators of Inflammation, vol. 2014, Article ID 348959, 8 pages, 2014.
- R. Ito, N. Satoh-Asahara, H. Yamakage et al., “An increase in the EPA/AA ratio is associated with improved arterial stiffness in obese patients with dyslipidemia,” Journal of Atherosclerosis and Thrombosis, vol. 21, no. 3, pp. 248–260, 2014.
- B. K. Itariu, M. Zeyda, E. E. Hochbrugger et al., “Long-chain n-3 PUFAs reduce adipose tissue and systemic inflammation in severely obese nondiabetic patients : a randomized control trial,” American Journal of Clinical Nutrition, vol. 96, no. 5, pp. 1137–1149, 2012.
- F. Agh, N. Mohammadzadeh Honarvar, M. Djalali et al., “Omega-3 fatty acid could increase one of myokines in male patients with coronary artery Disease: a randomized, double-blind, placebo-controlled trial,” Archives of Iranian Medicine, vol. 20, no. 1, pp. 28–33, 2017.
- C. Cipollina, S. R. Salvatore, M. F. Muldoon, B. A. Freeman, and F. J. Scarbohydratespfer, “Generation and dietary modulation of anti-inflammatory electrophilic omega-3 fatty acid derivatives,” PLoS One, vol. 9, no. 4, 2014.
- M. Kratz, J. N. Kuzma, D. K. Hagman et al., “n3 PUFAs do not affect adipose tissue inflammation in overweight to moderately obese men and women,” Journal of Nutrition, vol. 143, no. 8, pp. 1340–1347, 2013.
- M. J. Krantz, E. P. Havranek, R. I. Pereira, B. Beaty, P. S. Mehler, and C. S. Long, “Effects of omega-3 fatty acids on arterial stiffness in patients with hypertension: a randomized pilot study,” Journal of Negative Results in BioMedicine, vol. 14, no. 1, p. 21, 2015.
- R. Krysiak, A. Gdula-Dymek, and B. Okopien, “The effect of bezafibrate and omega-3 fatty acids on lymphocyte cytokine release and systemic inflammation in patients with isolated hypertriglyceridemia,” European Journal of Clinical Pharmacology, vol. 67, no. 11, pp. 1109–1117, 2011.
- A. Dewell, F. F. Marvasti, W. S. Harris, P. Tsao, and C. D. Gardner, “Low- and high-dose plant and marine (n-3) fatty acids do not affect plasma inflammatory markers in adults with metabolic syndrome,” Journal of Nutrition, vol. 141, no. 12, pp. 2166–2171, 2011.
- A. Nigam, M. Talajic, D. Roy et al., “Fish oil for the reduction of atrial fibrillation recurrence, inflammation, and oxidative stress,” Journal of the American College of Cardiology, vol. 64, no. 14, pp. 1441–1448, 2014.
- L. Darghosian, M. Free, J. Li et al., “Effect of omega-three polyunsaturated fatty acids on inflammation, oxidative stress, and recurrence of atrial fibrillation,” American Journal of Cardiology, vol. 115, no. 2, pp. 196–201, 2015.
- A. Simopoulos, “An increase in the omega-6/omega-3 fatty acid ratio increases the risk for obesity,” Nutrients, vol. 8, no. 3, p. 128, 2016.
- C. Gómez Candela, L. M. Bermejo López, and V. Loria Kohen, “Importancia del equilibrio del índice omega-6/omega-3 en el mantenimiento de un buen estado de salud. recomendaciones nutricionales,” Nutricion Hospitalaria, vol. 26, no. 2, pp. 323–329, 2011.
- A. Garcia-Arellano, R. Ramallal, M. Ruiz-Canela et al., “Dietary inflammatory index and incidence of cardiovascular disease in the PREDIMED study,” Nutrients, vol. 7, no. 6, pp. 4124–4138, 2015.
- M. Á. Martínez-González, E. Toledo, F. Arós et al., “Extravirgin olive oil consumption reduces risk of atrial fibrillation: The PREDIMED (Prevención con Dieta Mediterránea) trial,” Circulation, vol. 130, no. 1, pp. 18–26, 2014.
- A. Ceriello, K. Esposito, L. La Sala et al., “The protective effect of the Mediterranean diet on endothelial resistance to GLP-1 in type 2 diabetes: a preliminary report,” Cardiovascular Diabetology, vol. 13, no. 1, pp. 1–9, 2014.
- A. Camargo, O. A. Rangel-Zuñiga, C. Haro et al., “Olive oil phenolic compounds decrease the postprandial inflammatory response by reducing postprandial plasma lipopolysaccharide levels,” Food Chemistry, vol. 162, pp. 161–171, 2014.
- M. Bonaccio, G. Pounis, C. Cerletti, M. B. Donati, L. Iacoviello, and G. de Gaetano, “Mediterranean diet, dietary polyphenols and low-grade inflammation : results from the MOLI-SANI study,” British Journal of Clinical Pharmacology, vol. 83, no. 1, pp. 107–113, 2016.
- M. S. Westerterp-Plantenga, N. Luscombe-Marsh, M. P. G. M. Lejeune et al., “Dietary protein, metabolism, and body-weight regulation: dose–response effects,” International Journal of Obesity, vol. 30, no. S3, pp. S16–S23, 2006.
- H. J. Leidy, N. S. Carnell, R. D. Mattes, and W. W. Campbell, “Higher protein intake preserves lean mass and satiety with weight loss in pre-obese and obese women,” Obesity, vol. 15, no. 2, pp. 421–429, 2007.
- S. Tyrovolas and D. B. Panagiotakos, “The role of Mediterranean type of diet on the development of cancer and cardiovascular disease, in the elderly: a systematic review,” Maturitas, vol. 65, no. 2, pp. 122–130, 2010.
- P. Deriemaeker, K. Alewaeters, M. Hebbelinck, J. Lefevre, R. Phifatpaerts, and P. Clarys, “Nutritional status of flemish vegetarians compared with non-vegetarians: a matched samples study,” Nutrients, vol. 2, no. 7, pp. 770–780, 2010.
- J. L. Sullivan, “Iron in arterial plaque: a modifiable risk factor for atherosclerosis,” Biochimica et Biophysica Acta (BBA)-General Subjects, vol. 1790, no. 7, pp. 718–723, 2009.
- N. G. Vallianou, V. P. Bountziouka, E. Georgousopoulou et al., “Influence of protein intake from haem and non-haem animals and plant origin on inflammatory biomarkers among apparently-healthy adults in Greece,” Journal of Health, Population and Nutrition, vol. 31, no. 4, pp. 446–454, 2013.
- F. Arya, S. Egger, D. Colquhoun, D. Sullivan, S. Pal, and G. Egger, “Differences in postprandial inflammatory responses to a ‘modern’ v. traditional meat meal: a preliminary study,” British Journal of Nutrition, vol. 104, no. 5, pp. 724–728, 2010.
- L. Azadbakht and A. Esmaillzadeh, “Red meat intake is associated with metabolic syndrome and the plasma C-reactive protein concentration in women,” Journal of Nutrition, vol. 139, no. 2, pp. 335–339, 2009.
- P. G. Cocate, A. J. Natali, A. D. E. Oliveira, R. C. Alfenas, and H. H. M. Hermsdorff, “Consumption of branched-chain amino acids is inversely associated with central obesity and cardiometabolic features in a population of Brazilian middle aged men: potential role of leucine intake,” Journal of Nutrition, Health & Aging, vol. 19, no. 7, pp. 771–777, 2015.
- P. G. Cocate, A. J. Natali, A. de Oliveira et al., “Red but not white meat consumption is associated with metabolic syndrome, insulin resistance and lipid peroxidation in Brazilian middle-aged men,” European Journal of Preventive Cardiology, vol. 22, no. 22, pp. 1–8, 2013.
- C. Schwedhelm, T. Piscarbohydratesn, S. Rohrmann, H. Himmerich, J. Linseisen, and K. Nimptsch, “Plasma inflammation markers of the TNF pathway but not C-reactive protein are associated with processed meat and unprocessed red meat consumption in Bavarian adults,” Journal of Nutrition, vol. 147, no. 1, pp. 75–85, 2016.
- M. B. Zemel, X. Sun, T. Sobhani, and B. Wilson, “Effects of dairy compared with soy on oxidative and inflammatory stress in overweight and obese subjects,” American Journal of Clinical Nutrition, vol. 91, no. 1, pp. 16–22, 2010.
- J. Holmer-Jensen, T. Karhu, L. S. Mortensen, S. B. Pedersen, K.-H. Herzig, and K. Hermansen, “Differential effects of dietary protein sources on postprandial low-grade inflammation after a single high fat meal in obese non-diabetic subjects,” Nutrition Journal, vol. 10, no. 1, p. 115, 2011.
- P. Amini, Z. Maghsoudi, A. Feizi, R. Ghiasvand, and G. Askari, “Effects of high protein and balanced diets on lipid profiles and inflammation biomarkers in obese and overweight women at aerobic clubs: a randomized clinical trial,” International Journal of Preventive Medicine, vol. 7, no. 1, p. 110, 2016.
- M. K. Jensen, P. Koh-Banerjee, M. Franz, L. Sampson, M. Grønbæk, and E. B. Rimm, “Whole grains, bran, and germ in relation to homocysteine and markers of glycemic control, lipids, and inflammation,” American Journal of Clinical Nutrition, vol. 83, no. 2, pp. 275–283, 2006.
- I. A. Brownlee, C. Moore, M. Chatfield et al., “Markers of cardiovascular risk are not changed by increased whole-grain intake: the WHOLEheart study, a randomised, controlled dietary intervention,” British Journal of Nutrition, vol. 104, no. 1, pp. 125–134, 2010.
- J. Montonen, H. Boeing, A. Fritsche et al., “Consumption of red meat and whole-grain bread in relation to biomarkers of obesity, inflammation, glucose metabolism and oxidative stress,” European Journal of Nutrition, vol. 52, no. 1, pp. 337–345, 2013.
- Ö. Gögebakan, A. Kohl, M. A. Osterhoff et al., “Effects of weight loss and long-term weight maintenance with diets varying in protein and glycemic index on cardiovascular risk factors: the diet, obesity, and genes (diogenes) study: a randomized, controlled trial,” Circulation, vol. 124, no. 25, pp. 2829–2838, 2011.
- C. T. Damsgaard, A. Papadaki, S. M. Jensen et al., “Higher protein diets consumed ad libitum improve cardiovascular risk markers in children of overweight parents from eight European countries,” Journal of Nutrition, vol. 143, no. 6, pp. 810–817, 2013.
- S. K. Raatz, L. K. Johnson, and M. J. Picklo, “Consumption of honey, sucrose, and high-fructose corn syrup produces similar metabolic effects in glucose-tolerant and -intolerant individuals,” Journal of Nutrition, vol. 145, no. 10, pp. 2265–2272, 2015.
- L. H. Tracy, R. N. Lemaitre, B. M. Psaty et al., “Relationship of C-reactive protein to risk of cardiovascular disease in the elderly: results from the Cardiovascular Health Study and the Rural Health Promotion Project,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 17, no. 6, pp. 1121–1127, 1997.
- I. Aeberli, P. A. Gerber, M. Hochuli et al., “Low to moderate sugar-sweetened beverage consumption impairs glucose and lipid metabolism and promotes inflammation in healthy young men : a randomized controlled trial,” American Journal of Clinical Nutrition, vol. 94, no. 2, pp. 479–485, 2011.
- S. E. Kasim-Karakas, A. Tsodikov, U. Singh, and I. Jialal, “Responses of inflammatory markers to a low-fat, high-carbohydrate diet: effects of energy intake,” American Journal of Clinical Nutrition, vol. 83, no. 4, pp. 774–779, 2006.
- B. J. Nicklas, W. Ambrosius, S. P. Messier et al., “Diet-induced weight loss, exercise, and chronic inflammation in older, obese adults : a randomized controlled clinical trial,” American Journal of Clinical Nutrition, vol. 79, no. 4, pp. 544–551, 2004.
- A. M. Xydakis, C. C. Case, P. H. Jones et al., “Adiponectin, inflammation, and the expression of the metabolic syndrome in obese individuals: the impact of rapid weight lose through caloric restriction,” Journal of Clinical Endocrinology & Metabolism, vol. 89, no. 6, pp. 2697–2703, 2004.
- K. D. O’Brien, B. J. Brehm, R. J. Seeley et al., “Diet-induced weight loss is associated with decreases in plasma serum amyloid A and C-reactive protein independent of dietary macronutrient composition in obese subjects,” Journal of Clinical Endocrinology & Metabolism, vol. 90, no. 4, pp. 2244–2249, 2005.
- J. M. Hodgson, V. Burke, L. J. Beilin, and I. B. Puddey, “Partial substitution of carbohydrate intake with protein intake from lean red meat lowers blood pressure in hypertensive persons,” American Journal of Clinical Nutrition, vol. 83, no. 4, pp. 780–787, 2006.
- A. Papadaki, M. Linardakis, T. M. Larsen et al., “The effect of protein and glycemic index on children’s body composition: the DiOGenes randomized study,” Pediatrics, vol. 126, no. 5, pp. e1143–e1152, 2010.
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