Dietary Pattern and Macronutrients Profile on the Variation of Inflammatory Biomarkers: Scientific Update

Table 4

Studies addressing the effect of proteins, carbohydrates, and glycemic index on the chronic subclinical inflammation.

Reference	Study type	Population	Methods	Results
Azadbakht et al. [88]	Cross-sectional	482 female teachers from Tehrani, between 40 and 60 years old	(i) Usual dietary intake was assessed through a semiquantitative FFQ with 168 items	PCR plasma concentrations were higher in individuals from higher quintiles of red meat consumption, even after model fit
			(ii) FFQ foods were classified into 41 food groups, based on the nutrient profile, culinary, or specific use
			(iii) Red meat category was defined by the sum of processed meat (sausages and hamburgers), red meat (beef and lamb), and organ meat (liver, kidney, and heart)
			(iv) Blood samples: assess inflammatory markers
Vallianou et al. [85]	Cross-sectional	490 middle-aged Caucasian adults, apparently healthy	(i) Validated semiquantitative FFQ, with 76 food items	Unadjusted model:
		BMI: between 26 and 27 kg/m²	(ii) Food items were grouped according to the protein content: nonheme (dairy products and eggs), heme (meat and by-products, fish and seafood), and vegetable protein	Cistatin C: decrease in serum levels as frequency of protein animal heme consumption increased
			(iii) Blood samples taken after 12 hours of fasting: cystatin C, CRP, white cells, uric acid, and platelets as inflammatory parameters	Platelets: reduction of counting with the increase of vegetable protein consumption
				Model adjusted to: vegetable protein intake + energy intake + age + gender + BMI + smoking habit + physical activity
				Platelets: reduction of counting with the increased frequency of vegetable protein consumption
Montonen et al. [96]	Cross-sectional	2198 German individuals from the EPIC cohort (836 M, between 40 and 65 years old; 1362 W, between 35 and 65 years old)	(i) Usual intake of previous year was assessed through a self-applied FFQ, with 148 items	(i) Inverse association of whole bread consumption with [CRP] and [GGT]
		BMI: between 25 and 26 kg/m²	(ii) Frequency of consumption was requested in 10 categories, and the amount of consumption was calculated in grams	(ii) Direct association of red meat consumption with [CRP] and [GGT]
			(iii) Reproducibility after 6 months: high for red meat intake and moderate for whole bread intake
			(iv) Intake of these foods was divided in quintiles
			(v) Blood samples: assess CRP was inflammatory parameter and GGT for oxidative stress
Cocate et al. [87]	Cross-sectional	296 men, working at the Universidade Federal de Viçosa (Brazil), between 40 and 59 years old	(i) Usual dietary intake was assessed through an FFQ, validated for the Brazilian population	(i) Ox-LDL concentrations displayed positive correlation with red meat consumption and the saturated fat in it
			(ii) The red meat group was composed of lean meat, high-fat meat, ground beef, lean pork meat, high-fat pork meat, and bacon
			(iii) The white meat group was composed of chicken with skin, skinless chicken, and fish
			(iv) Blood samples after 12 h of fasting: assess ox-LDL
Schwedhelm et al. [90]	Cross-sectional	553 individuals from the Bavarian Food Consumption Survey II group, between 18 and 80 years old	(i) Dietary intake, including meat intake, was assessed through three 24 h recalls (2 in weekdays and 1 in the weekend)	(i) Processed meat consumption displayed positive association with IL-6 after adjusting for fruit and green vegetable consumption, except when there was BMI addition to the model
			(ii) Red meat: beef, veal, pork, mutton or lamb, and domestic and game rabbit	(ii) Processed meat consumption was positively associated with TNF-α, TNF-R1, and TNF-R2, even after adjusting for fruit, green vegetable, and dairy consumption
			(iii) Processed meat: ready-made meat or meat preserved by salting, smoking, curing, marination, or cooking	(iii) Consumption of nonprocessed red meat was inversely associated with TNF-R1 and TNF-R2
			(iv) Blood samples: assess CRP, IL-6, total TNF-α, and TNF-R1 as inflammatory parameter
Arya et al. [86]	Randomized cross-over	10 (6 M/4 W) healthy individuals between 19 and 38 years old	Before testing diets: 10 h fasting	Fat meat is more proinflammatory than lean meat:
		BMI: between 18 and 26.5 kg/m²	Types of meals:	(i) 1 h postprandial: [CRP], [TNF-α], and [IL-6] were significantly greater in the group who consumed fat meat
			(i) Lean meat (<4% fat, whereas <1% saturated fat) + 75 g of boiled potato + 50 g of peas	(ii) 2 h postprandial: [TNF-α] and [IL-6] were significantly greater in the group who consumed fat meat
			(ii) Fat meat (25–30% fat, whereas 40% saturated fat + 75 g of boiled potato + 50 g of peas
			Participants were categorized in 2 groups of 5, and each group received a type of meal. After 6–10 days, group meals were changed
			Blood samples 1 h and 2 h postprandial: assessment of CRP and TNF-α as inflammatory parameters
Zemel et al. [91]	Randomized cross-over	20 healthy adults (14 M/6 W), professors, employees, and students at the University of Tennessee, with mean age = 31 years	(i) The study displayed 2 weight-maintenance diets: one for the overweight group and the other for the obese group	Skimmed milk smoothie significantly decreased circulating TNF-α (15%) and IL-6 (13%), whereas soybean diet had the opposite effect
		BMI: 10 overweight (25.0–29.9 kg/m²) and 10 degree-1 obesity (30–34.9 kg/m²)	(ii) Both diets offered ≈35% fat, ≈49% carbohydrates, 16% protein, and 8–12 g/d of fiber; the placebo diet was based on soy protein and the testing diet on skimmed milk protein	MCP-1 concentrations were significantly lower in individuals who consumed skimmed milk smoothie, whereas the soy smoothie caused an increase in MCP-1
			(iii) Both groups were categorized in two additional ones and each subgroup received for 28 days: 3 soy protein smoothies or 3 skimmed milk protein smoothies. After 28 days, subgroups meals were changed for additional 28 days	Skimmed milk smoothie resulted in a significant increase in circulating adiponectin (20%), whereas soy smoothie resulted in its decrease
			Each smoothie shake contained 170 kcal, 10 g of proteins, 1 g of fat, and 30 g of carbohydrates	CRP exhibited an global treatment effect, which resulted in a significant reduction (57%) through the ingestion of skimmed milk smoothie
			(iv) Blood samples: assess inflammatory markers
Holmer-Jensen et al. [92]	Randomized case-control	11 Caucasian middle-aged obese individuals (3 M/8 W), BMI: ≥30 kg/m²	Before testing diets:	CCL5
			Standard dietary intake:	CCL5 was higher in the postprandial period of 30 min than in the basal, for all protein sources
			(i) 56% carbohydrates, 24% fat, and 20% proteins	After 4 h postprandial:
			(ii) 1673 kcal women and 2151 kcal men blood sample after 12 h fasting testing diet intake for 20 min	Lower CCL5 for whey protein than to cod and casein protein
			(iii) Hypercaloric: 19% carbohydrates, 66% fat, and 15% protein: 1188–1191 kcal	Lower CCL5 for gluten protein than to cod protein
			(iv) 45 g white bread, 100 g butter, 45 g of protein (mixed with the meal or the water, according to the source) blood samples after 4 h postprandial: analyze inflammatory markers	MCP-1
				MCP-1 was lower in the postprandial period of 30 min than in the basal, for all protein sources
				After 4 h postprandial:
				Higher MCP-1 for whey protein than for cod and gluten protein
Gögebakan et al. [97]	Randomized case-control	773 European obese adults, with mean age of 41 years	After 8 weeks under low-caloric diet (800 kcal/day), were selected those whose weight loss is ≥8%, and the LC diet was applied again	(i) After low-caloric diet, there was a decrease in [CRP]
		BMI: 34 kg/m², from the Diogenes project	Diet composition:	(ii) During the dietary intervention, there was a decrease in [CRP]: > in the LGI than in the HGI group and > in the LP than in the HP group
			(i) LP (10–15% energy) + LGI	(iii) LGI group displayed an additional reduction of 15% in [CRP]
			(ii) LP + HGI	(iv) After the 26 weeks, the LGI and LP groups displayed significant reduction in [CRP] with respect to the HGI and HP groups
			(iii) HP (23–28% energy) + LGI
			(iv) HP + HGI
			(v) Control
			(a) There should be ≠ 15 points from HGI to LGI
			(b) Guidance for healthy choices
			Blood samples after 10 h fasting: CRP assessment as inflammatory parameter
Damsgaard et al. [98]	Randomized case-control	253 European children and adolescents, from 5 to 18 years old, with overweight parents, from the Diogenes project	Diet composition:	Changes in [CRP] after intervention were greater in the LGI than in HGI, but significance was lost after Bonferroni correction, which may explained by the families with lower adherence to the diets
		4.8% W and 4.2% M, from 10 to 18 years old → MS	(i) LP (10–15% energy) + LGI
			(ii) LP + HGI
			(iii) HP (23–28% energy) + LGI
			(iv) HP + HGI
			(a) There should be ≠ 15 points from HGI to LGI
			(b) Guidance for healthy choices
			Blood samples after 4 h fasting: CRP assessment as inflammatory parameter
Raatz et al. [99]	Randomized cross-over	55 American eutrophic and obese individuals (16 M/39 W), from 20 to 80 years old	(i) Individuals received the 50 g of three types of sugar to be consumed diluted in water	Basal levels:
		BMI: 18 to 39.9 kg/m²	(ii) Each type of sugar was consumed during 2 weeks, with a 2- to 4-week period between treatments	(i) [PCR] and [IL-6] were significantly greater in TGI
			(iii) Blood samples after 10 h fasting: days 0 and 15 from each experimental period, to assess CRP and IL-6 as inflammatory parameters	Posttreatment:
				(i) [PCR] and [IL-6] were significantly greater in TGI
Amini et al. [93]	Randomized case-control	56 Iranian women, between 20 and 46 years old, BMI ≥ 25 kg/m², engaged in physical activities three times a week, 60 minutes per session	Female volunteers were grouped equally and randomly in two diet groups:	There was a marginally significant decrease in CRP levels after intervention, both in the HP and LP diets
			(i) HP diet: 45% carbohydrates, 25% protein, and 30% fat
			(ii) LP diet: 55% carbohydrates, 15% protein, and 30% fat
			(iii) All of them displayed a reduction of 500 kcal from the conventional diet
			Dietary intake was determined by a food record applied on baseline and every 2 weeks, referring to 3 days of the week
			(iv) HP and LP diets were provided in an 8-week period
			(v) Blood samples: assess CRP as inflammatory parameter

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.