Consumption of a high-fat meal containing cheese compared with a vegan alternative lowers postprandial C-reactive protein in overweight and obese individuals with metabolic abnormalities: a randomised controlled cross-over study

Elieke Demmer, Marta D Van Loan, Nancy Rivera, Tara S Rogers, Erik R Gertz, J Bruce German, Angela M Zivkovic, Jennifer T Smilowitz, Elieke Demmer, Marta D Van Loan, Nancy Rivera, Tara S Rogers, Erik R Gertz, J Bruce German, Angela M Zivkovic, Jennifer T Smilowitz

Abstract

Dietary recommendations suggest decreased consumption of SFA to minimise CVD risk; however, not all foods rich in SFA are equivalent. To evaluate the effects of SFA in a dairy food matrix, as Cheddar cheese, v. SFA from a vegan-alternative test meal on postprandial inflammatory markers, a randomised controlled cross-over trial was conducted in twenty overweight or obese adults with metabolic abnormalities. Individuals consumed two isoenergetic high-fat mixed meals separated by a 1- to 2-week washout period. Serum was collected at baseline, and at 1, 3 and 6 h postprandially and analysed for inflammatory markers (IL-6, IL-8, IL-10, IL-17, IL-18, TNFα, monocyte chemotactic protein-1 (MCP-1)), acute-phase proteins C-reactive protein (CRP) and serum amyloid-A (SAA), cellular adhesion molecules and blood lipids, glucose and insulin. Following both high-fat test meals, postprandial TAG concentrations rose steadily (P < 0·05) without a decrease by 6 h. The incremental AUC (iAUC) for CRP was significantly lower (P < 0·05) in response to the cheese compared with the vegan-alternative test meal. A treatment effect was not observed for any other inflammatory markers; however, for both test meals, multiple markers significantly changed from baseline over the 6 h postprandial period (IL-6, IL-8, IL-18, TNFα, MCP-1, SAA). Saturated fat in the form of a cheese matrix reduced the iAUC for CRP compared with a vegan-alternative test meal during the postprandial 6 h period. The study is registered at clinicaltrials.gov under NCT01803633.

Keywords: CH, cheese; CRP, C-reactive protein; Dairy products; HOMA-IR, homoeostasis model assessment of insulin resistance; Inflammation; MCP-1, monocyte chemotactic protein-1; Metabolic syndrome; Obesity; Palm oil; Postprandial metabolism; SAA, serum amyloid-A; VA, vegan alternative; Vegan diets; WC, waist circumference; iAUC, incremental AUC; sICAM, soluble intracellular adhesion molecule.

Figures

Fig. 1.
Fig. 1.
Enrolment and follow up of participants in the randomised cross-over trial. CH, Cheddar cheese treatment; VA, vegan-alternative treatment.
Fig. 2.
Fig. 2.
Postprandial response of glucose (a) and insulin (b) before and after high-fat mixed meal rich in SFA from either vegan alternative cheese (---) or Cheddar cheese (––). Values are means, with standard deviations represented by vertical bars (n 20). * Significant difference between 0 and 1 h (P < 0·0005). † Significant difference between 1 and 3 h (P < 0·0005). ‡ Significant difference between 3 and 6 h (P = 0·01).
Fig. 3.
Fig. 3.
Postprandial response of serum TAG after both vegan alternative (---) and Cheddar cheese (––) meals. Values are means, with standard deviations represented by vertical bars (n 20). There was no difference between the treatments but there was a significant increase over time (P < 0·05) for all time points: 0–1, 0–3, 0–6, 1–3, 1–6, and 3–6 h.
Fig. 4.
Fig. 4.
Postprandial serum C-reactive protein (CRP) concentrations over the 6 h postprandial period after the Cheddar cheese (CH) and vegan alternative (VA) meals. Values are means, with standard deviations represented by vertical bars. * The VA meal resulted in a significantly greater overall CRP concentration (P = 0·033) when compared with the CH meal. iAUC, incremental AUC.

References

    1. Burdge GC & Calder PC (2005) Plasma cytokine response during the postprandial period: a potential causal process in vascular disease? Br J Nutr 93, 3–9.
    1. Margioris AN (2009) Fatty acids and postprandial inflammation. Curr Opin Clin Nutr Metab Care 12, 129–137.
    1. Patsch JR, Miesenböck G, Hopferwieser T, et al. (1992) Relation of triglyceride metabolism and coronary artery disease. Studies in the postprandial state. Arterioscler Thromb 12, 1336–1345.
    1. Keys A, Anderson J & Grande F (1957) Prediction of serum-cholesterol responses of man to changes in fats in the diet. Lancet i, 959–966.
    1. Kushi LH, Lew RA, Stare FJ, et al. (1985) Diet and 20-year mortality from coronary heart disease: the Ireland–Boston Diet–Heart Study. New Engl J Med 312, 811–818.
    1. Erkkilä A, de Mello VD, Risérus U, et al. (2008) Dietary fatty acids and cardiovascular disease: an epidemiological approach. Prog Lipid Res 47, 172–187.
    1. McGuire S (2011) U.S. Department of Agriculture and U.S. Department of Health and Human Services, Dietary Guidelines for Americans, 2010. Washington, DC: U.S. Government Printing Office, January 2011. Adv Nutr 2, 293–294.
    1. Howard BV, Van Horn L, Hsia J, et al. (2006) Low-fat dietary pattern and risk of cardiovascular disease: the Women's Health Initiative Randomized Controlled Dietary Modification Trial. JAMA 295, 655–666.
    1. Qin L-Q, Xu J-Y, Han S-F, et al. (2015) Dairy consumption and risk of cardiovascular disease: an updated meta-analysis of prospective cohort studies. Asia Pac J Clin Nutr 24, 90–100.
    1. Nakamura T, Hirota T, Mizushima K, et al. (2013) Milk-derived peptides, Val-Pro-Pro and Ile-Pro-Pro, attenuate atherosclerosis development in apolipoprotein E-deficient mice: a preliminary study. J Med Food 16, 396–403.
    1. Sjogren P, Rosell M, Skoglund-Andersson C, et al. (2004) Milk-derived fatty acids are associated with a more favorable LDL particle size distribution in healthy men. J Nutr 134, 1729–1735.
    1. Settanni L & Moschetti G (2010) Non-starter lactic acid bacteria used to improve cheese quality and provide health benefits. Food Microbiol 27, 691–697.
    1. Snow D, Ward R, Olsen A, et al. (2011) Membrane-rich milk fat diet provides protection against gastrointestinal leakiness in mice treated with lipopolysaccharide. J Dairy Sci 94, 2201–2212.
    1. Jacobs DR, Gross MD & Tapsell LC (2009) Food synergy: an operational concept for understanding nutrition. Am J Clin Nutr 89, 1543S–1548S.
    1. Poppitt SD, Keogh GF, Lithander FE, et al. (2008) Postprandial response of adiponectin, interleukin-6, tumor necrosis factor-α, and C-reactive protein to a high-fat dietary load. Nutrition 24, 322–329.
    1. Masson CJ & Mensink RP (2011) Exchanging saturated fatty acids for (n-6) polyunsaturated fatty acids in a mixed meal may decrease postprandial lipemia and markers of inflammation and endothelial activity in overweight men. J Nutr 141, 816–821.
    1. National Cancer Institute (2014) Sources of Saturated Fat, Stearic Acid, & Cholesterol Raising Fat among the US Population, 2005–06. Applied Research Program website, 2014. (accessed November 2015).
    1. Casalena N (2011) How many Adults are Vegan in the U.S.? Vegetarian Resource Group. (accessed January 2016).
    1. Dietary Guidelines Advisory Committee (2015) Scientific Report of the 2015 Dietary Guidelines Advisory Committee. Washington, DC: USDA and US Department of Health and Human Services.
    1. Craig WJ & Mangels AR (2009) Position of the American Dietetic Association: vegetarian diets. J Am Diet Assoc 109, 1266–1282.
    1. Laugerette F, Furet J-P, Debard C, et al. (2012) Oil composition of high-fat diet affects metabolic inflammation differently in connection with endotoxin receptors in mice. Am J Physiol Endocrinol Metab 302, E374–EE86.
    1. Grundy SM, Cleeman JI, Daniels SR, et al. (2005) Diagnosis and management of the metabolic syndrome: an American Heart Association/National Heart, Lung, and Blood Institute scientific statement. Circulation 112, 2735–2752.
    1. Ascaso JF, Pardo S, Real JT, et al. (2003) Diagnosing insulin resistance by simple quantitative methods in subjects with normal glucose metabolism. Diabetes Care 26, 3320–3325.
    1. Pearson TA, Mensah GA, Alexander RW, et al. (2003) Markers of inflammation and cardiovascular disease: application to clinical and public health practice: a statement for healthcare professionals from the Centers for Disease Control and Prevention and the American Heart Association. Circulation 107, 499–511.
    1. Pedersen A, Sandström B & Van Amelsvoort JMM (1997) The effect of ingestion of inulin on blood lipids and gastrointestinal symptoms in healthy females. Br J Nutr 78, 215–222.
    1. Gouveia-Figueira S, Späth J, Zivkovic AM, et al. (2015) Profiling the oxylipin and endocannabinoid metabolome by UPLC-ESI-MS/MS in human plasma to monitor postprandial inflammation. PLOS ONE 10, e9.
    1. Zivkovic AM, Telis N, German JB, et al. (2011) Dietary omega-3 fatty acids aid in the modulation of inflammation and metabolic health. Calif Agric (Berkeley) 65, 106–111.
    1. Trumbo P, Schlicker S, Yates A, et al. (2002) Dietary reference intakes for energy, carbohydrate, fiber, fat, fatty acids, cholesterol, protein and amino acids. J Am Diet Assoc 102, 1621–1630.
    1. Baecke J, Burema J & Frijters J (1982) A short questionnaire for the measurement of habitual physical activity in epidemiological studies. Am J Clin Nutr 36, 936–942.
    1. Herieka M & Erridge C (2014) High-fat meal induced postprandial inflammation. Mol NutrFood Res 58, 136–146.
    1. Perez-Martinez P, Alcala-Diaz JF, Delgado-Lista J, et al. (2014) Metabolic phenotypes of obesity influence triglyceride and inflammation homoeostasis. Eur J Clin Invest 44, 1053–1064.
    1. Carstensen M, Thomsen C & Hermansen K (2003) Incremental area under response curve more accurately describes the triglyceride response to an oral fat load in both healthy and type 2 diabetic subjects. Metabolism 52, 1034–1037.
    1. Kleiner G, Marcuzzi A, Zanin V, et al. (2013) Cytokine levels in the serum of healthy subjects. Mediators Inflamm 2013, 434010.
    1. Tulk HM & Robinson LE (2009) Modifying the n-6/n-3 polyunsaturated fatty acid ratio of a high-saturated fat challenge does not acutely attenuate postprandial changes in inflammatory markers in men with metabolic syndrome. Metabolism 58, 1709–1716.
    1. Blackburn P, Després JP, Lamarche B, et al. (2006) Postprandial variations of plasma inflammatory markers in abdominally obese men. Obesity 14, 1747–1754.
    1. Manning PJ, Sutherland WHF, McGrath MM, et al. (2008) Postprandial cytokine concentrations and meal composition in obese and lean women. Obesity 16, 2046–2052.
    1. van Oostrom AJHHM, Sijmonsma TP, Verseyden C, et al. (2003) Postprandial recruitment of neutrophils may contribute to endothelial dysfunction. J Lipid Res 44, 576–583.
    1. Nappo F, Esposito K, Cioffi M, et al. (2002) Postprandial endothelial activation in healthy subjects and in type 2 diabetic patients: role of fat and carbohydrate meals. J Am Coll Cardiol 39, 1145–1150.
    1. Dandona P, Aljada A, Mohanty P, et al. (2001) Insulin inhibits intranuclear nuclear factor κB and stimulates IκB in mononuclear cells in obese subjects: evidence for an anti-inflammatory effect? J Clin Endocrinol Metab 86, 3257–3265.
    1. Baggiolini M, Moser B & Clark-Lewis I (1994) Interleukin-8 and related chemotactic cytokines: the Giles Filley lecture. Chest 105, 3 Suppl., 95S–98S.
    1. Mallat Z, Heymes C, Corbaz A, et al. (2004) Evidence for altered interleukin 18 (IL)-18 pathway in human heart failure. FASEB J 18, 1752–1754.
    1. Hyson DA, Paglieroni TG, Wun T, et al. (2002) Postprandial lipemia is associated with platelet and monocyte activation and increased monocyte cytokine expression in normolipemic men. Clin Appl Thromb Hemost 8, 147–155.
    1. Rosenson RS, Huskin AL, Wolff DA, et al. (2008) Fenofibrate reduces fasting and postprandial inflammatory responses among hypertriglyceridemia patients with the metabolic syndrome. Atherosclerosis 198, 381–388.
    1. Pepys M & Baltz ML (1982) Acute phase proteins with special reference to C-reactive protein and related proteins (pentaxins) and serum amyloid A protein. Adv Immunol 34, 141–212.
    1. Hagihara K, Nishikawa T, Isobe T, et al. (2004) IL-6 plays a critical role in the synergistic induction of human serum amyloid A (SAA) gene when stimulated with proinflammatory cytokines as analyzed with an SAA isoform real-time quantitative RT-PCR assay system. Biochem Biophys Res Comm 314, 363–369.
    1. O'Reilly S, Cant R, Ciechomska M, et al. (2014) Serum amyloid A induces interleukin-6 in dermal fibroblasts via Toll-like receptor 2, interleukin-1 receptor-associated kinase 4 and nuclear factor-κB. Immunology 143, 331–340.
    1. O'Brien KD & Chait A (2006) Serum amyloid A: the “other” inflammatory protein. Curr Ather Rep 8, 62–68.
    1. Esser D, Oosterink E, op't Roodt J, et al. (2013) Vascular and inflammatory high fat meal responses in young healthy men; a discriminative role of IL-8 observed in a randomized trial. PLOS ONE 8, e9.
    1. Schmid A, Petry N, Walther B, et al. (2015) Inflammatory and metabolic responses to high-fat meals with and without dairy products in men. Br J Nutr 113, 1853–1861.
    1. Ajani UA, Ford ES & Mokdad AH (2004) Dietary fiber and C-reactive protein: findings from National Health and Nutrition Examination Survey data. J Nutr 134, 1181–1185.
    1. Milani RV, Lavie CJ & Mehra MR (2004) Reduction in C-reactive protein through cardiac rehabilitation and exercise training. J Am Coll Cardiol 43, 1056–1061.
    1. Hackam DG & Anand SS (2003) Emerging risk factors for atherosclerotic vascular disease: a critical review of the evidence. JAMA 290, 932–940.
    1. Carroll MF, Schade DS (2003) Timing of antioxidant vitamin ingestion alters postprandial proatherogenic serum markers. Circulation 108, 24–31.
    1. Ceriello A, Assaloni R, Da Ros R, et al. (2005) Effect of atorvastatin and irbesartan, alone and in combination, on postprandial endothelial dysfunction, oxidative stress, and inflammation in type 2 diabetic patients. Circulation 111, 2518–2524.
    1. Nakamura A, Monma Y, Kajitani S, et al. (2015) Effect of glycemic state on postprandial hyperlipidemia and hyperinsulinemia in patients with coronary artery disease. Heart Vessels 2015, 1–10.
    1. Panagiotakos DB, Pitsavos CH, Zampelas AD, et al. (2010) Dairy products consumption is associated with decreased levels of inflammatory markers related to cardiovascular disease in apparently healthy adults: The ATTICA Study. J Am Coll Nutr 29, 357–364.
    1. Baldi A, Ioannis P, Chiara P, et al. (2005) Biological effects of milk proteins and their peptides with emphasis on those related to the gastrointestinal ecosystem. J Dairy Res 72, Special no., 66–72.
    1. Harsha WT, Kalandarova E, McNutt P, et al. (2006) Nutritional supplementation with transforming growth factor-β, glutamine, and short chain fatty acids minimizes methotrexate-induced injury. J Pediatr Gastroenterol Nutr 42, 53–58.
    1. Gopal PK & Gill H (2000) Oligosaccharides and glycoconjugates in bovine milk and colostrum. Br J Nutr 84, Suppl. 1, 69–74.
    1. Després J-P & Lemieux I (2006) Abdominal obesity and metabolic syndrome. Nature 444, 881–887.
    1. Agorastos A, Hauger RL, Barkauskas DA, et al. (2014) Circadian rhythmicity, variability and correlation of interleukin-6 levels in plasma and cerebrospinal fluid of healthy men. Psychoneuroendocrinology 44, 71–82.
    1. Soerensen KV, Thorning TK, Astrup A, et al. (2014) Effect of dairy calcium from cheese and milk on fecal fat excretion, blood lipids, and appetite in young men. Am J Clin Nutr 99, 984–991.
    1. Hjerpsted J, Leedo E & Tholstrup T (2011) Cheese intake in large amounts lowers LDL-cholesterol concentrations compared with butter intake of equal fat content. Am J Clin Nutr 94, 1479–1484.
    1. Payette C, Blackburn P, Lamarche B, et al. (2009) Sex differences in postprandial plasma tumor necrosis factor-α, interleukin-6, and C-reactive protein concentrations. Metabolism 58, 1593–1601.
    1. Barnett JB, Woods MN, Lamon-Fava S, et al. (2004) Plasma lipid and lipoprotein levels during the follicular and luteal phases of the menstrual cycle. J Clin Endocrinol Metab 89, 776–782.
    1. Bell HK & Bloomer RJ (2010) Impact of serum estradiol on postprandial lipemia, oxidative stress, and inflammation across a single menstrual cycle. Gend Med 7, 166–178.

Source: PubMed

Szponzorok és közreműködők

Egészségi állapot

Kábítószer-beavatkozások

3
Iratkozz fel