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. 2019 May 15;10(Suppl 2):S239–S250. doi: 10.1093/advances/nmy072

Milk and Dairy Product Consumption and Inflammatory Biomarkers: An Updated Systematic Review of Randomized Clinical Trials

Stine M Ulven 1, Kirsten B Holven 1,2, Angel Gil 3,4,5,6, Oscar D Rangel-Huerta 1,
PMCID: PMC6518147  PMID: 31089732

ABSTRACT

Milk and dairy products contribute ≤14% of the caloric intake in developed countries. Recent evidence has shown controversial results with regard to the role of dairy products in deleterious processes such as inflammation. The increasing number of studies on the anti- and proinflammatory effects of milk and dairy products in the past 5 y reflects the growing interest in this area of research. The aim of this systematic review was to evaluate the scientific evidence provided in the past 5 y on the effects of milk and dairy products on inflammatory biomarkers provided by randomized clinical trials. The search strategy was conducted in Medline (via PubMed) and Scopus (which includes EMBASE and the Web of Science) databases and included articles from 1 January 2012 to 30 April 2018. The risk of bias was assessed using the Cochrane methodology. The number of study participants, type of study, doses, and the key results are reported. The following primary outcomes were considered for inclusion: circulating concentrations of C-reactive protein, interleukins, cytokines, and vascular adhesion molecules or expression of proinflammatory genes in peripheral blood mononuclear cells; however, the primary outcomes considered were not limited to these. Sixteen studies (15 articles) included in this systematic review reported on healthy individuals and subjects who were overweight or obese and who had metabolic syndrome or type 2 diabetes. The consumption of milk or dairy products did not show a proinflammatory effect in healthy subjects or individuals with metabolic abnormalities. The majority of studies documented a significant anti-inflammatory effect in both healthy and metabolically abnormal subjects, although not all the articles were of high quality. This review was registered on PROSPERO (International Prospective Register of Systematic Reviews) at https://www.crd.york.ac.uk/prospero/display_record.php?RecordID=94535 as CRD42018094535.

Keywords: inflammation, inflammatory biomarkers, dairy products, milk, healthy, overweight, obesity, metabolic syndrome, diabetes

Introduction

Dairy products are a major part of the Western diet, contributing ≤14% of the caloric intake in developed countries and are known to serve as an effective vehicle for nutrient supplementation and fortification (1). The diverse range of dairy products includes milk with diverse fat contents, fermented milks (i.e., yogurt, kefir, and doogh, among others), cheese, cream, butter, and ice cream. All of these dairy products differ in their nutritional composition. Milk and dairy products contain numerous nutrients, which contribute significantly to meet the daily requirements of calcium, magnesium, selenium, riboflavin, vitamin B-5 (pantothenic acid), and vitamin B-12.

Inflammation comprises several processes engineered to maintain tissue and organ homeostasis and can be categorized as acute or chronic according to the time course. The adequate balance between pro- and anti-inflammatory molecules is essential for maintaining homeostasis. An increase in proinflammatory molecules, such as TNF-α, IL-1, and IL-6, is especially destructive and has been shown to be involved in several pathological responses (e.g., endotoxic shock and chronic inflammatory diseases) (2). Furthermore, the chronic overproduction of TNF-α and IL-1 might lead to damage of adipose tissue and muscle and has been shown to be associated with insulin resistance (3). An increase in proinflammatory markers is often followed by an increase in anti-inflammatory cytokines (i.e., IL-10) and IL-1 receptor antagonist (IL-1Ra) to oppose the cascade of inflammatory mediators initiated by the proinflammatory cytokines (4, 5). Therefore, it is important to measure extended networks, pathways, or ratios (e.g., TNF-α:IL-10) rather than single biomarkers to provide a wider picture in order to understand the acute and chronic inflammatory response. In addition, the upregulation of adhesion molecules [e.g., intercellular adhesion molecule 1 (ICAM-1), vascular cell adhesion molecule 1 (VCAM-1), or E-selectin] is involved in the atherosclerotic process, subsequently leading to the development of cardiovascular disease (CVD) (6).

Some epidemiologic and systematic reviews (SRs) have shown controversial results with regard to the role of dairy products in deleterious processes such as inflammation and the complications associated with it [i.e., type 2 diabetes (T2D) and CVD]. For instance, the consumption of dairy, particularly full-fat and nonfermented products, might be associated with prediabetes and T2D (7). However, other SRs provide evidence that the consumption of full-fat dairy has neutral effects on the risk of T2D, and the association between low-fat (LF) dairy consumption and the risk of T2D appears to be relatively consistent (8). Dairy products, especially fermented dairy products, have also been associated with a decreased or neutral effect on CVD risk and mortality (19, 21–26).

Labonté et al. (9) concluded that, despite the high content of SFAs in dairy foods, dairy consumption did not exert adverse effects on biomarkers of inflammation in overweight or obese adults. In addition, Bordoni et al. (10) reported that dairy products, mainly fermented products, might have anti-inflammatory properties and that such an effect is enhanced in subjects with metabolic abnormalities. These data suggest that there may be differences in the inflammatory response according to the metabolic state of an individual, and an update of the evaluation of the impact of dairy products on the inflammatory biomarkers is justified. Due to the growing interest in the effect of dairy products on inflammation, we evaluated the scientific evidence provided in the past 5 y with regard to the effects of milk and dairy products on inflammatory biomarkers through an SR of randomized controlled trials (RCTs).

Methods

This SR was designed with the aim of generating an updated review of RCTs conducted to investigate the effect of milk and other dairy products on inflammation, assessed by inflammatory biomarkers in the circulation and gene expression levels in healthy individuals and subjects with metabolic abnormalities. This review was carried out in accordance with the Preferred Reporting Items for Systematic Review and Meta-Analysis Protocols (PRISMA-P) statement (11). The review was registered on PROSPERO (International Prospective Register of Systematic Reviews) as CRD42018094535. The PICOS (Population, Intervention, Comparison, and Outcomes) criteria (Supplemental Table 1) were used to define the following research question: Do milk or dairy products have any effects of inflammation, measured by inflammatory biomarkers, in both healthy and unhealthy adults? RCTs that studied the effect of milk or dairy products on inflammatory biomarkers were included. Prospective, parallel, and crossover designs were considered. There was no restriction on sample size. Articles, or at least the abstract, had to be written in English or Spanish. No ecological or case-control studies were included.

Inclusion and exclusion criteria

To be considered for inclusion in the SR, studies had to administer dietary supplementation or a specific diet containing dairy products. Studies that used dietary recommendations or self-reporting alone were excluded. Studies were also excluded if a supplement that could potentially confound the effects of the milk or the dairy product was administered or if no ethical approval had been received. Naturally enriched dairy products were included, and those fermented using bacteria other than the typical Lactobacillus delbrueckii spp. bulgaricus and Streptococcus thermophiles were excluded. Because previous SRs and meta-analyses have already examined evidence of the effect of milk or dairy products on inflammation (9), only studies published between 1 January 2012 and 30 April 2018 were included.

Participants

Eligible participants were adults aged >18 y who were either healthy or had an acute or chronic disease. There were no restrictions with regard to sex, ethnicity, or study setting.

Types of interventions

The studies included the administration of milk or dairy products, individually or in combination, allowing for the investigation of the effects of the milk or dairy products. There were no restrictions on dosage or dosing regimen.

Primary outcome measures

The following primary outcomes were considered for the inclusion of the studies: circulating concentrations of C-reactive protein (CRP), IL-1α, IL-1β, IL-2, IL-4, IL-6, IL-8, IL-10, IL-12, IL-17, TNF-α, chemokine ligands (CCLs), monocyte chemoattractant protein 1 (MCP-1), matrix metallopeptidase (MMP) 9 (MMP-9), soluble ICAM-1 (sICAM-1), and soluble VCAM-1 (sVCAM-1) and the expression of proinflammatory genes in peripheral blood mononuclear cells (PBMCs) or skeletal muscle, but the primary outcomes considered were not limited to these.

Literature search

We performed an SR for studies published in English or Spanish and conducted in adults in the following electronic databases: Medline (via PubMed) and SCOPUS (which includes EMBASE and the Web of Science). Figure 1 shows the main steps of the literature search. Studies were identified in the PubMed database by applying the date limit of 1 January 2012 to 30 April 2018, filtering by humans, and using the following medical subject headings (MeSH) search terms: ((Dairy products[MeSH Terms]) AND (Inflammation[MeSH Terms] OR inflammatory biomarkers[MeSH Major Topic] OR cytokines[MeSH Major Topic])) AND Clinical Trial[Publication Type].

FIGURE 1.

FIGURE 1

PRISMA flow diagram of the literature search process. PRISMA, Preferred Reporting Items for Systematic Review and Meta-Analysis.

The search in SCOPUS was filtered by RCT using the following equation: (Dairy products) AND (Inflammation OR inflammatory biomarkers OR cytokines).

Study selection

Abstracts of publications yielded by the search were examined by ODR-H, who eliminated all publications that were obviously ineligible for inclusion.

Data extraction

One reviewer (ODR-H) input the data into a database; 2 additional reviewers (SMU and KBH) resolved any discrepancies and selected the final list of articles to be included.

Assessment of risk of bias

Two authors (SMU and ODR-H) independently assessed the risk of bias following the Cochrane Collaboration's methodology (12). In case of discrepancies, a third reviewer was involved in the evaluation (AG). The Cochrane tool includes different domains related to randomization and allocation concealment (selection bias), blinding (performance and measurement bias), loss to follow-up and adherence to the intention-to-treat principle (attrition bias), and selective outcome publication (reporting bias). In addition, other potential sources of bias, such as private or public funding, were included. The risk of bias was tabulated for each study and was classified as low, high, or unclear, as described in chapter 8 of the Cochrane Handbook for Systematic Reviews of Interventions, and the outputs were generated in RevMan 5.3 (12).

Results

The main steps of the workflow of the SR are depicted in the PRISMA flow diagram (Figure 1). Tables 1 and 2 list the 15 publications (16 studies) included in this review, grouped according to the study population [healthy subjects and subjects who were overweight or obese or who had a chronic disease, such as metabolic syndrome (MetS) or T2D]. Within each group, we categorized the items according to the type of product and the severity of the metabolic abnormalities group. Moreover, the tables include the sample size, age, type and dose of the milk/dairy intervention, major inflammatory biomarkers determined, and main outcomes.

TABLE 1.

Randomized clinical trials (published between 2012 and 2018) that used interventions with dairy products to evaluate the effects on inflammatory biomarkers in healthy adults1

Study (ref) Year Population Age, y Treatment Duration Major outcomes Results
Burton et al. (13) 2017 13 Healthy adults 24.6 ± 4.7 1) 800 g yogurt; 2) 800 g milk acidified by the addition of d-(+)-glucono-δ-lactone Postprandial test (crossover design) hs-CRP, CCL-2, CCL-5, IL-6, LPS, TNF-α No significant differences in inflammatory biomarkers
Burton et al. (14) 2018 13 Healthy adults (subset of 7 subjects for gene expression) 24.6 ± 4.7 1) 800 g yogurt; 2) 800 g milk acidified by the addition of d-(+)-glucono-δ-lactone Postprandial test (crossover design) PBMC gene expression in a subset of 7 subjects Both yogurt and acidified milk intake showed a similar coordinated regulation of inflammatory genes; significant reduction at 2 h in the milk group and at 4 h in the yogurt group
Schmid et al. (15) 2015 19 Healthy men 25–55 1) HFC (1005 kcal); 2) HFM (1277 kcal); 3) HFD (1000 kcal) Acute intervention CRP, IL-6, TNF-α CRP increased after HFD compared with HFM; no significant differences in IL-6 or TNF-α between the test meals
Penedo et al. (16) 2013 29 Healthy adults 20–40 20 g butter naturally enriched with CLA/d 8 wk (8 wk of depletion) Adiponectin, CRP, IL-2, IL-4, IL-8, IL-10, MMP-2, MMP-9/TIMP-1, TNF-α No significant differences in adiponectin, CRP, IL-2, IL-8, MMP-9/TIMP-1, MMP-9, or MMP-2 activities after intervention; only a significant increase in IL-10
O'Brien et al. (17) 2015 67 Healthy adults 18–35 1) Endurance training + control beverage; 2) endurance training + kefir beverage (454 g/dose); 3) active control + control beverage; 4) active control + kefir beverage (454 g/dose) 15 wk (kefir twice/wk) CRP Significant decrease in CRP
Pei et al. (18) 2017 120 Premenopausal women (30/group) 21–55 1) YN: 339 g low-fat yogurt/d; 2) YO: 339 g low-fat yogurt/d; 3) CN: 324 g soy pudding/d; 4) CO: 324 g soy pudding/d 9 wk hs-CRP, IL-6, TNF-α:sTNF-RII, LPS, LBP, LBP:sCD14, EndoCAb IgM, sCD14; PBMC gene expression (only in the obese subgroup) YO and YN showed decreased TNF-α, EndoCAb IgM, and TNF-α to sTNFR-RII and LBP to sCD14 ratios; YO PBMC expression of NFKB and TGFB1 increased relative to CO group; no significant changes in other inflammatory biomarkers
Rossi et al. (19) 2015 40 Premenopausal obese women Dairy group: 37.7 ± 7.5 1) 800 mg Ca/d by dairy products 3 mo Adiponectin, leptin, IL-6 Significant decrease in IL-6 in the dairy group
No-dairy group: 39.8 ± 9.8 2) 800 mg Ca/d by mineral supplements
Serra et al. (20) 2012 31 Postmenopausal women Soy group: 54 ± 4 1) 244 mL vanilla soymilk/d 4 wk (28 d) IL-1β, IL-6, and TNF-α and proteolytic genes in skeletal muscle (calpain 1, calpain 2, ubiquitin, E2, Atrogin1, muRF1) No significant effect on expression of inflammation-responsive or proteolytic genes
Dairy group: 55 ± 3 2) 240 mL reduced-fat dairy milk/d
Gjevestad et al. (21) 2017 31 Older adults ≥70 1) Protein-enriched milk (2 × 20 g protein/d); 2) isocaloric carbohydrate drink 12 wk Serum (TNF-α, sTNFRSF1A); mRNA expression levels of inflammatory markers in PBMCs The serum concentration of TNF-α increased significantly in the control group, whereas sTNFRSF1A increased significantly in both groups with no significant differences between groups. There was no significant effect between groups. Significant differences in the mRNA expression of NR1H3, encoding the LXRα transcription factor and INFG were observed. The mRNA level of TNFRSF1A was significantly reduced, whereas the mRNA level of DPP4 was significantly increased in the control group.

1Values are means ± SDs or ranges. CCL, chemokine ligand; CLA, conjugated linoleic acid; CN, control nonobese; CO, control obese; CRP, C-reactive protein; DPP4, dipeptidyl-peptidase 4; HFC, high-fat nondairy control meal; HFD, isoenergetic high-fat dairy meal; HFM, high-fat nondairy meal supplemented with milk; hs-CRP, high-sensitivity C-reactive protein; EndoCAb IgM, anti-endotoxin core antibodies immunoglobulins M; INFG, interferon γ; LBP, LPS-binding protein; LFD, low-fat diet; LXRα, liver X receptor α; MCP-1, monocyte chemoattractant protein 1; MMP, matrix metallopeptidase; muRF1, muscle RING-finger protein-1; NFKB, nuclear factor κB inhibitor α; NR1H3, nuclear receptor subfamily, group H, member 3; PBMC, peripheral blood mononuclear cell; ref, reference; sCD14, soluble CD14; sTNFRSF1A, soluble TNF-receptor superfamily 1A; sTNF-RII, soluble TNF-receptor II; TFGB1, transforming growth factor β1; TIMP-1, tissue inhibitor of metalloproteinases 1; TNFRSF1A, TNF-receptor superfamily 1A; YN, yogurt 2nonobese; YO, yogurt obese.

TABLE 2.

Randomized clinical trials (published between 2012 and 2018) that used interventions with dairy products to evaluate the effects on inflammatory biomarkers in subjects who were overweight or obese or had metabolic abnormalities1

Study (ref) Year Population Age, y Treatment Duration Major outcomes Results
Nestel et al. (23) 2012 13 Overweight adults 44–69 1) Single breakfast containing control low-fat milk; 2) single breakfast containing 45 g fat from butter; 3) single breakfast containing 45 g fat from cream; 4) single breakfast containing 45 g fat from yogurt; 5) single breakfast containing 45 g fat from cheese Acute intervention hs-CRP, IL-1β, IL-6 TNF-α, MCP-1, sICAM-1, sVCAM-1 No significant differences between groups in inflammatory biomarkers
Nestel et al. (23) 2012 12 Overweight adults 44–69 1) 45 g fermented products (yogurt plus cheese); 2) 45 g nonfermented products (butter, cream and full-cream ice cream) 4 wk each period with 2 wk of run-in and 2 wk of washout hs-CRP, IL-1β, IL-6 TNF-α, MCP-1, sICAM-1, sVCAM-1 No significant differences in inflammatory biomarkers
Zarrati et al. (24) 2014 75 Overweight and obese adults 20–50 1) Regular yogurt as part of an LCD (RLCD); 2) probiotic yogurt as part of an LCD (PLCD); 3) probiotic yogurt without LCD (PWLCD) 8 wk hs-CRP, IL-17, TNF-α, and leptin and mRNA levels of inflammation-related genes (TNFA and RORGt in PBMCs) hs-CRP, IL-17, and TNF-α decreased and leptin increased between PLCD and the PWLCD (after post hoc analysis). RORC gene expression was reduced in PLCD relative to PWLCD.
Nestel et al. (25) 2013 12 Overweight and obese adults 40–70 1) FFD diet containing yogurt plus cheese (fermented); 2) FFD diet containing butter, cream, and ice cream (nonfermented); 3) LFD 2-wk periods (crossover study design) hs-CRP, IL-1β, IL-6, MCP-1 and MIP-1α, sICAM-1, sVCAM-1, and TNF-α IL-6 was significantly lower after consumption of the fermented dairy diet
Labonté et al. (27) 2014 112 Adults with hs-CRP values >1 mg/L 18–70 1) 3 servings dairy/d (375 mL LF milk, 175 g LF yogurt, and 30 g regular-fat cheddar cheese); 2) 3 servings energy-matched control products/d (fruit juice, vegetable juice, cashews, and 1 cookie) 8 wk hs-CRP, IL-6, adiponectin, gene expression No significant differences in inflammatory biomarkers
Dugan et al. (26) 2016 37 Adults with MetS (subset of 17 subjects, 13 women and 3 men for gene expression) No information 1) LFD (10 oz 1% milk, 6 oz nonfat yogurt, 4 oz 2% cheese); 2) CNT (1.5 oz granola bar and 12 oz 100% juice) 16-wk (crossover study design, 4 wk washout, and 6 wk on each intervention) CRP, TNF-α, MCP-1; gene expression of IL1, IL6, and TNFA in PBMCs in a subset of 17 subjects at the end of each dietary period No significant differences in inflammatory biomarkers. In women, TNF-α and MCP-1 decreased after the LFD compared with the CNT. Expressions of IL1B and IL6 were reduced significantly compared with the control period.
Jones et al. (28) 2013 49 Adults with MetS 20–60 1) Control (low dairy, 700 mg Ca/d, 500 kcal/d); 2) dairy/Ca (high dairy, 1400 mg Ca/d, 500 kcal/d) 12 wk IL-1β, IL-6, MCP-1, and TNF-α No significant differences in inflammatory biomarkers
Neyestani et al. (29) 2013 90 Patients with T2D 30–60 1) 500 mL plain Persian yogurt drink/d (doogh) (containing 150 mg Ca and no detectable vitamin D3/250 mL); 2) DD (containing 500 IU vitamin D3 and 150 mg Ca/250 mL); 3) CDD (containing 500 IU vitamin D3 and 250 mg Ca/250 mL) 12 wk hs-CRP, IL-1β, IL-6, RBP-4 hs-CRP, IL-1β, IL-6, fibrinogen, and RBP-4 concentrations significantly decreased in both the DD and CDD groups but no difference between groups

1CDD, calcium- and vitamin D3-fortified doogh; CNT, carbohydrate-based control; CRP, C-reactive protein; DD, vitamin D–fortified doogh; FFD, full-fat dairy; hs-CRP, high-sensitivity C-reactive protein; LCD, low-calorie diet; LF, low-fat; LFD, low-fat diet; MCP-1, monocyte chemoattractant protein 1; MetS, metabolic syndrome; MIP-1α, macrophage inflammatory protein 1; PBMC, peripheral blood mononuclear cell; ref, reference; RBP, retinol-binding protein; RORGt, RAR-related orphan receptor γ; sICAM-1, soluble intercellular adhesion molecule 1; sVCAM-1, soluble vascular cell adhesion molecule 1; TNFA, tumor necrosis factor α; T2D, type 2 diabetes.

Healthy adults

Table 1 shows the results from 9 studies in healthy adults aged >18 y (13–21). Five studies included participants of both sexes with sample sizes between 13 and 67 subjects (13, 14, 16, 17, 21); one study recruited 19 male individuals (15), 2 studies included premenopausal women (n = 120 and 140) (18, 19), and one study included 31 postmenopausal women (20). Two studies reported the use of yogurt (fermented or LF), one included kefir, one used butter naturally enriched with cis-9, trans-11 conjugated linoleic acid (CLA;cis-9, trans-11-18:2), and 2 interventions studied the effects of milk (reduced-fat and protein-enriched). Two RCTs were based on diets including dairy products (either 800 g/d or ∼1100 kcal/d derived from dairy products). Three interventions used an acute approach (postprandial response), whereas the others lasted from 3 wk to 3 mo.

The major inflammatory outcomes included the assessment of serum markers, including high-sensitivity CRP (hs-CRP) and cytokines (IL-1β, IL-2, IL-4, IL-6, IL-8, and TNF-α) (13, 15–21). Other markers assessed in at least one study were CCL2 and CCL5 (13), LPS, LPS-binding protein (LBP), anti-endotoxin core antibodies immunoglobulins M (EndoCAb IgM) (18), MMP-2, MMP-9/tissue inhibitor of metalloproteinases 1 (TIMP-1) (16), soluble cluster of differentiation 14 (sCD14) (18), and TNF-α/soluble TNF-receptor II (sTNF-RII) (18). Two studies included the analysis of PBMC gene expression of inflammatory markers in PBMCs and one in skeletal muscle (14, 21, 22).

The intake of 454 g kefir twice a week for 15 wk in combination with endurance training (17) significantly reduced CRP concentrations compared with the control (P < 0.05). Moreover, Rossi et al. (19) observed a significant decrease in IL-6 after 3 mo of consuming 800 mg Ca/d through the intake of dairy products compared with the same amount of calcium through supplements (changes of 1.20 compared with 0.66 pg/mL, respectively; P = 0.0135). Penedo et al. (16) found that the consumption of 20 g butter/d significantly decreased the serum concentration of IL-2 and IL-8 (P = 0.026 and 0.029, respectively) and increased IL-10 (P = 0.013) after a CLA-repletion compared with a CLA-depletion phase. Schmid et al. (15) found that the intake of dairy products with a high-fat (HF) meal increased the CRP concentration when compared with an HF meal without dairy products but including full-fat milk (P = 0.02). Although TNF-α was measured in most studies, only Pei et al. (18) reported a significant decrease in the TNF-α to sTNF-RII and LBP to sCD14 ratios (P = 0.0013 and 0.0477, respectively) after the consumption of 399 g LF yogurt/d for 9 wk compared with the control.

With regard to the study of gene expression, Burton et al. (14) showed that 800 g of either yogurt or acidified milk/d reduced the expression of genes related to inflammation [e.g., aryl hydrocarbon receptor (AHR) and epiregulin (EREG)] in PBMCs. In contrast, Serra et al. (20) did not find any significant expression of inflammatory-related genes in skeletal muscle after the consumption of 240 mL/d during 4 wk of reduced-fat milk when compared with a vanilla soymilk.

Recently, Gjevestad et al. (21) studied the effect of protein-enriched milk compared with an isocaloric carbohydrate drink on mRNA expression levels in PBMCs and reported significant differences in the expression of nuclear receptor subfamily, group H, member 3 (NR1H3) and IFN-γ (IFNG) genes between groups and a significant decrease in the mRNA level of TNF-receptor superfamily member 1A (TNFRS1A) and an increase in dipeptidyl-peptidase 4 (DPP4) (all P < 0.05) in the control group.

Subjects who were overweight, obese, or had metabolic abnormalities

In Table 2, we present a detailed summary of the 7 studies developed in adults who were overweight or obese or had a chronic disease. In one article, Nestel et al. (23) reported results from an acute and a short-term intervention; thus, these results are presented as 2 independent studies. In total, 4 studies included overweight or obese adults with sample sizes ranging from 12 to 75 subjects (23–25); one study included 112 adults with high concentrations of hs-CRP (>1 mg/L). Two studies recruited 37 and 49 adults with MetS (26, 28), and the last study reported data from 90 patients with diagnosed T2D (29).

The most common inflammatory markers analyzed were hs-CRP, IL-1β, IL-6, MCP-1, and TNF-α (23–29). Three reports included sICAM-1 and sVCAM-1 (23). Adiponectin (27), macrophage inflammatory protein-1α (MIP-1α) (25), and retinol-binding protein 4 (RBP-4) (29) were measured, however, with no significant changes or differences between the groups. Three studies, in addition to the study by Pei et al. (18), investigated the effect of the intervention on gene expression levels (24, 26, 27).

However, in a postprandial study including overweight adults (23), the serum concentrations of IL-1β, IL-6, and TNF-α decreased after the consumption of nonfermented dairy products (butter and cream; all P < 0.05) but without a significant effect when compared with the control group who consumed LF milk. The same research group tested either an HF diet (HFD) containing 46 g fermented (cheese and yogurt) or nonfermented products for 4 wk (within the same population) without any significant effects in the abovementioned markers (23). Later, they compared the previously tested HFDs but this time included an LF dairy diet containing milk and yogurt; they observed that IL-6 was significantly higher (P < 0.05, post hoc analysis) after the consumption of the HFD with nonfermented dairy products (7.0 pg/mL) compared with the consumption of fermented and LF dairy products (6.2 pg/mL for both) (25).

Zarrati et al. (24) studied the effect of yogurt with and without a low-calorie diet (PLCD and PWLCD, respectively) compared with a regular yogurt as part of a low-calorie diet (RLCD) in overweight and obese adults for 8 wk. A reduction in hs-CRP and IL-17 in all 3 groups (PLCD, PWLCD, and RLCD) was observed (all P < 0.001), and post hoc analysis showed a more prominent decrease in the concentration of hs-CRP in the PWLCD group (−3.4 pg/mL) and a more prominent decrease in IL-17 in the RLCD group (−670 pg/mL) compared with their counterparts. Moreover, only the PWLCD group showed to a significant decrease in the concentration of TNF-α after the intervention (−392 pg/mL; P < 0.001).

An LF dairy diet for 4–6 wk in adults with MetS seems to have a differential effect when stratified according to sex (26). When both men and women were included in the analysis, no effect was seen, but after splitting the analysis according to sex, it was shown that the concentrations of TNF-α and MCP-1 were lower in women in the LF dairy group than in the women in the control group after the intervention (P = 0.028 and P < 0.001, respectively). In another study including both men and women, the inclusion of 3 servings commercially available dairy products/d showed no differences in hs-CRP or IL-6 when compared with a dairy-free control diet (27). The consumption of 3 variants of Persian yogurt during 12 wk showed that fortification with either calcium or vitamin D reduced serum concentrations of CRP, IL-1β, IL-6, fibrinogen, and RBP-4 within the groups but not when compared with a plain version of the product (29).

With regard to PBMC gene expression, Pei et al. (18) showed that the consumption of LF yogurt for 9 wk among obese adults induced an increase in the PBMC mRNA levels of nuclear factor κB inhibitor α (NFKB) and encoding transforming growth factor β1 (TGFB1) compared with the control (54% and 20%, respectively); however, the same effect was not seen in nonobese adults. The consumption of a probiotic yogurt with a low-calorie diet (for 8 wk) reduced the PBMC gene expression level of RAR-related orphan receptor γt (RORC) (fold-change mean ± SD: 0.7 ± 0.66; P = 0.007) (24), whereas the consumption of an LF diet containing dairy products (for 4 wk) reduced the gene expression levels of IL1B and IL6 (63% and 46%, respectively; P < 0.05) compared with a carbohydrate-based control diet (26). Nonetheless, Labonté et al. (27) reported that 3 servings dairy products/d for 4 wk did not show any significant modulation of expression of 10 genes [including CCL2, IL18, IL6, IL1B, nuclear factor κ light-chain-enhancer of activated B cells subunit 1 (NFKB1), natriuretic peptide receptor C (NPR3), peroxisome proliferator-activated receptor α (PPARA), sterol regulatory element–binding transcription factor 2 (SREBF2), TNF, and TNF-receptor–associated factor 3 (TRAF3)].

Risk of bias

The article by Labonté et al. (27) was found to be the most transparent in the reporting of all items included in the risk-of-bias assessment. We should highlight a major concern in selection bias due to the lack of specific reporting of the random-sequence generation and allocation concealment. For 50% of the studies, this was not clear and 20% showed a high risk of bias (more details are shown in Figures 2 and 3). This should be corrected in the reports of further studies.

FIGURE 2.

FIGURE 2

Risk-of-bias summary: review authors’ judgments of each risk-of-bias item for each included study.

FIGURE 3.

FIGURE 3

Risk-of-bias graph: review authors’ judgments of each risk-of-bias item presented as percentages across the studies.

Due to the nature of some of the interventions in which a complete meal is the object of study, it is not possible to follow a double-blind design. Nonetheless, we consider that the authors should state the type of blinding implemented or the impossibility of blinding and be transparent in their reporting; in this regard, 3 studies were considered to have a high risk of bias due to the lack of reporting of any type of blinding (16, 17, 19). Detection bias is another concern due to the insufficient details provided by the authors in relation to the blinding of the persons who assessed the clinical outcomes. Only Labonté et al. (27) were very clear in this domain; thus, their study was evaluated with a low risk of bias.

We did not detect a potential bias in the reporting of outcome data or a potential selective reporting bias in the studies presented here. Detailed justifications associated with the evaluation of the risk of bias within studies are provided in the Figures 2 and 3.

Discussion

The main findings of the present SR were that the consumption of milk or dairy products did not show a proinflammatory effect in healthy adults or among adults who were overweight or obese or who had MetS or T2D. In addition, long-term dairy supplementation showed a weak anti-inflammatory effect in both populations.

In this SR we have summarized the findings of 16 intervention studies in which different dairy products were assessed and inflammatory markers were measured in plasma, serum, or at the gene expression level in healthy individuals and individuals who were overweight or obese or had a chronic disease. In general, the diversity of the types and amounts of dairy products used in the studies included in this review makes it demanding to compare the effects among the different interventions. Therefore, we will discuss the findings according to the type of intervention and the metabolic status of the individuals included in the studies.

It has been previously shown that hypertriglyceridemia can induce endothelial activation in both healthy (30) and hypertriglyceridemic (31) adults, and in turn, the postprandial inflammatory response depends on the type of fat in an HF meal. The postprandial inflammatory response is due to the increased production of proinflammatory cytokines seen during the postprandial TG phase, which leads to a state of acute inflammation, potentially causing endothelial dysfunction, which is one of the earliest defects of atherogenesis (10). Gene expression profiling of PBMCs from single-meal studies has shown that different fat qualities influence oxidative stress (32) and inflammatory responses (33, 34). PBMCs, consisting of monocytes and lymphocytes, may therefore be an appropriate model system in which to study postprandial inflammatory effects. One acute study including healthy individuals examined the effect of yogurt compared with the same amount of acidified milk on both circulating inflammatory markers (13) and PBMC gene expression (14) and found no significant differences in inflammatory biomarkers in circulation concentrations or gene expression levels. On the other hand, another acute study included in this review included subjects who presented metabolic abnormalities; no differences were reported in the effects on the inflammatory markers IL-1β, IL-6, and TNF-α between the groups receiving HF meals containing either HF dairy products or LF milk (23).

It is well known that HF meals increase the postprandial concentration of proinflammatory cytokines (i.e., IL-6 and TNF-α) and the acute-phase protein CRP (35, 36). In this regard, when comparing the effect of an HF dairy meal, an HF nondairy meal supplemented with milk, and an HF nondairy control meal, no differences in IL-6, endotoxin, or TNF-α were observed (15). Other researchers have found moderate or no effects on circulating inflammatory markers after the intake of a single meal with different fat qualities (35–38). It therefore does not seem that full-fat milk and dairy products (cheese and butter) have a different impact on the inflammatory response than an HF meal.

With regard to the long-term effect of dairy products on markers of inflammation in healthy individuals, it does not seem as though the inclusion of dairy products that are high in SFAs in the diet promotes inflammation because none of the studies reported an increase in circulating inflammatory markers in the group who received dairy products (16) or between the dairy product and control groups. One of the studies reported a reduction in CRP when adding kefir to the diet for 15 wk (2 times/wk) (17), and another study showed a reduction in TNF-α, EndoCAb IgM, and TNF-α to sTNFR-RII and LBP to sCD14 ratios when consuming yogurt for 9 wk in nonobese premenopausal women (18). In another study in premenopausal women, the inclusion of dairy products containing 800 mg Ca/d decreased IL-6 concentrations (19). Thus, among healthy subjects, a few studies suggest that the inclusion of specific dairy products in the diet may have a long-term favorable effect on inflammation, which is in agreement with previous reports (10). However, these results should be interpreted with caution due to the limited number of studies and because the studies that showed an effect presented a high risk of bias. Thus, it is necessary to perform more studies that include inflammatory biomarkers as a primary outcome to elucidate if dairy products can influence inflammation.

Among adults who were overweight or obese or who had other metabolic abnormalities, no studies included in the present review showed any increase in the inflammatory markers measured after the intervention. Most of the studies showed no significant differences between groups (23, 27–29). However, TNF-α and MCP-1 decreased in women with MetS after the intake of nonfat yogurt and 1% milk compared with after a granola bar and juice (26), and IL-6 was lower in overweight adults after the intake of fermented dairy products (25). Moreover, gene expression analysis showed a downregulation of several inflammation-related genes after the consumption of different types of yogurt or a diet containing dairy products. In addition, the very-well-conducted and -reported research from Labonté et al. (27) showed no changes in gene expression levels of the proinflammatory genes IL6, IL1B, or NFKB1 in PBMCs. These observations are very much in line with the conclusions of the latest reviews supporting an anti-inflammatory effect of dairy product consumption (9, 10).

In the present review, we have reviewed the evidence from the last 5 y of acute and long-term intervention studies investigating the effect of milk and dairy products on inflammation. We assessed the quality of the studies using the Cochrane Risk-of-Bias Assessment Tool (12). In this regard, we should highlight that one major limitation is related to the selection bias and blinding domains due to low-quality reporting of some of the studies. Further studies should improve the transparency of the reporting of the blinding methods and the methods used to allocate the patients to the intervention groups. Although there are several inflammatory biomarkers in common across the interventions, the clinical and methodologic diversity among the studies, manifested through the heterogeneity, did not allow us to perform a meta-analysis.

The findings reported here highlight the variability in the design of RCTs; thus, we consider that there are several key points that should be taken into account in future studies. First, earlier and present reports (9, 10, 25) have shown the potential benefit of fermented dairy products due to their bacterial content and their metabolites. Nevertheless, it is necessary to conduct parallel experiments focused on the characterization of such products to make it possible to understand the mechanisms of action. In fact, several health claims are dismissed due to the lack of characterization of the molecules responsible for the effect (39).

The use of new technologies, such as metabolomics, to analyze dairy foods and biological samples might provide solid answers with regard to the modulation of inflammation (i.e., through the study of the lipid classes and other metabolites). In addition, the use of whole-genome transcriptomics from metabolic tissues, such as adipose tissues and skeletal muscle or PBMCs, would make it possible to link biological and physiologic changes to the modulation of inflammation in these tissues. According to the European Food Safety Authority, for functional claims referring to the reduction in inflammation, a change in markers of inflammation, such as various interleukins, does not necessarily indicate a beneficial physiologic effect per se; it should be accompanied by a beneficial physiologic or clinical outcome (39). Therefore, additional tools are necessary to complement the use of the traditional inflammatory biomarkers to understand the biological and mechanical effects of dairy products on inflammation. Fermented dairy products might modulate the inflammatory and immune response through the bacteria within the dairy products and their metabolites (10). Milk also contains a high content of SFAs, and among these is palmitic acid (16:0), which is the dominant FA in blood and is known to act via Toll-like receptors and initiate the innate immune system (40). In addition, SCFAs, key molecules for the maintenance of gut health, could reduce the secretion of proinflammatory cytokines and chemokines by macrophages (41). Moreover, unique trans and odd-chain FAs (15:0 and 17:0) may also be relevant because they appear to be inversely associated with cardiometabolic risk (42).

In conclusion, the consumption of milk or dairy products did not show a proinflammatory effect in healthy subjects or individuals who were overweight or obese or had other metabolic abnormalities. The evidence from long-term supplementation showed a weak anti-inflammatory effect in both healthy and metabolically abnormal adults. The evidence from acute and short-term interventions is scarce and thus inconclusive. Further studies need to be developed with enhanced designs and better reporting, and the characterization of the dairy products should be included.

Supplementary Material

Supplemental Table

Acknowledgments

All authors read and approved the final manuscript.

Notes

This supplement was sponsored by the Interprofessional Dairy Organization (INLAC), Spain. The sponsor had no role in the design of the studies included in the supplement; in the collection, analyses, or interpretation of the data; in the writing of the manuscript; or in the decision to publish the results. This study was partially funded by the University of Granada Plan Propio de Investigación 2016, Excellence actions: Unit of Excellence on Exercise and Health (UCEES), Plan Propio de Investigación 2018, Programa Contratos-Puente, the Junta de Andalucía, Consejería de Conocimiento, Investigación y Universidades, and European Regional Development Funds (ref. SOMM17/6107/UGR). Publication costs for this supplement were defrayed in part by the payment of page charges. The opinions expressed in this publication are those of the authors and are not attributable to the sponsors or the publisher, Editor, or Editorial Board of Advances in Nutrition.

ODR-H has received funding from the European Union Seventh Framework Program (FP7-PEOPLE-2013-COFUND) under grant agreement no. 609020 - Scientia Fellows.

Author disclosures: SMU, KBH, AG, and ODR-H, no conflicts of interest.

Supplemental Table 1 is available from the “Supplementary data” link in the online posting of the article and from the same link in the online table of contents at https://academic.oup.com/advances/.

Abbreviations used: CCL, chemokine ligand; CLA, conjugated linoleic acid; CRP, C-reactive protein; CVD, cardiovascular disease; HF, high-fat; HFD, high-fat diet; hs-CRP, high-sensitivity C-reactive protein; ICAM-1, intercellular adhesion molecule 1; LF, low-fat; LBP, LPS-binding protein; MCP-1, monocyte chemoattractant protein 1; MeSH, medical subject heading(s); MetS, metabolic syndrome; MMP, matrix metallopeptidase; PBMC, peripheral blood mononuclear cell; PWLCD, yogurt without a low-calorie diet; RCT, randomized controlled trial; RLCD, regular yogurt with control diet; sCD14, soluble cluster of differentiation 14; SR, systematic review; T2D, type 2 diabetes; VCAM-1, vascular cell adhesion molecule 1.

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