Abstract
Purpose
Ewe’s milk yogurt is richer in proteins, minerals and short- and medium-chain fatty acids compared to cow’s milk yogurt. We aimed to evaluate the effects of cow’s milk yogurt (CW, 3.0% fat), semi-skimmed (ES, 2.8% fat) and whole ewe’s milk yogurts (EW, 5.8% fat) on inflammatory markers and gut microbiota in subjects with borderline-high plasma cholesterol.
Methodology
30 adults (16 women) were randomized into a crossover study to consume 250 g/yogurt/day during three 5-week periods (4-week washouts). Plasma insulin, leptin, adhesion molecules, cytokines and gut microbiota composition (qPCR) were analysed. Rates of change were used to assess treatment effects both in the whole group and in subgroups of subjects with different cholesterol/HDL-c ratio (Cho-I group A: the top 6 women and 4 men values; Cho-I group B: remaining subjects).
Results
The yogurts showed no different effects on the inflammatory biomarkers or the microbiota of the whole group. However, ICAM-1 and P-selectin rates of change were lower after EW compared to CW and ES, respectively, in subjects of the Cho-I group A (P = 0.047 and P = 0.020). Women of this group showed lower MCP-1 rates of change after EW compared to ES and CW (P = 0.028, both). Blautia coccoides–Eubacterium rectale decreased in women of the Cho-I group A during EW vs. ES (P = 0.028).
Conclusion
Ewe’s yogurt effects on inflammatory markers and microbiota were not different from those after cow’s yogurt, but the attenuation of some inflammatory biomarkers with ewe’s whole-milk yogurt in subjects with the highest TC/HDL-c deserves further study.
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Abbreviations
- LAB:
-
Lactic acid bacteria
- CVR:
-
Cardiovascular risk
- SFA:
-
Saturated fatty acids
- SCFA:
-
Short-chain fatty acids
- MCFA:
-
Medium-chain fatty acids
- LDL:
-
Low-density lipoprotein LCFA Long-chain fatty acids
- BMI:
-
Body mass index
- qPCR:
-
Quantitative (or real-time) polymerase chain reaction
- MCP-1:
-
Monocyte chemoattractant protein 1
- IL:
-
Interleukin
- TNF-α:
-
Tumor necrosis factor-α
- ICAM-1:
-
Intercellular adhesion molecule-1
- VCAM-1:
-
Vascular cell adhesion molecule-1
- TC/HDL-c:
-
Total cholesterol/HDL-c ratio
- TLR:
-
Toll-like receptors
References
Dietary Guidelines Advisory Committee (2015) Scientific report of the 2015 dietary guidelines advisory committee. http://www.health.gov/dietaryguidelines/2015-scientific-report/pdfs/scientific-report-of-the-2015-dietary-guidelines-advisory-committee.pdf. Accessed Oct 2016
Wang H, Livingston KA, Fox CS, Meigs JB, Jacques PF (2013) Yogurt consumption is associated with better diet quality and metabolic profile in American men and women. Nutr Res 33(1):18–26. https://doi.org/10.1016/j.nutres.2012.11.009
Cormier H, Thifault E, Garneau V, Tremblay A, Drapeau V, Perusse L, Vohl MC (2016) Association between yogurt consumption, dietary patterns, and cardio-metabolic risk factors. Eur J Nutr 55(2):577–587. https://doi.org/10.1007/s00394-015-0878-1
Adolfsson O, Meydani S, Russell R (2004) Yogurt and gut function. Am J Clin Nutr 80:245–256
Fernandez MA, Panahi S, Daniel N, Tremblay A, Marette A (2017) Yogurt and cardiometabolic diseases: a critical review of potential mechanisms. Adv Nutr 8(6):812–829. https://doi.org/10.3945/an.116.013946
Dumas A, Lapointe A, Dugrenier M, Provencher V, Lamarche B, Desroches S (2017) A systematic review of the effect of yogurt consumption on chronic diseases risk markers in adults. Eur J Nutr 56:1375–1392. https://doi.org/10.1007/s00394-016-1341-7
Sadrzadeh-Yeganeh H, Elmadfa I, Djazayery A, Jalali M, Heshmat R, Chamary M (2010) The effects of probiotic and conventional yoghurt on lipid profile in women. Br J Nutr 103:1778–1783
Labonté ME, Couture P, Richard C, Desroche S, Lamarche B (2013) Impact of dairy products on biomarkers of inflammation: a systematic review of randomized controlled nutritional intervention studies in overweight and obese adults. Am J Clin Nutr 97:706–717
Tamime AY, Robinson RK (1999) Background to manufacturing practice. In: Tamime AY, Robinson RK (eds) Yoghurt science and technology, 2nd edn. CRC Press, Woodhead Publishing Limited, Cambridge, pp 32–33
Jandal JM (1996) Comparative aspects of goat and sheep milk. Small Ruminant Res 22:177–185
Katcher HI, Hill AM, Lanford JL, Yoo JS, Kris-Etherton PM (2009) Lifestyle approaches and dietary strategies to lower LDL-cholesterol and triglycerides and raise HDL-cholesterol. Endocrinol Metab Clin North Am 38(1):45–78. https://doi.org/10.1016/j.ecl.2008.11.01. (PubMed PMID:19217512)
Tall AR, Yvan-Charvet L (2015) Cholesterol, inflammation and innate immunity. Nat Rev Immunol 15(2):104–116. https://doi.org/10.1038/nri3793
Hansson GK (2005) Inflammation, atherosclerosis, and coronary artery disease. N Engl J Med 352:1685–1695
Calder PC, Ahluwalia N, Albers R, Bosco N, Bourdet-Sicard R, Haller D, Holgate ST, Jönsson LS, Latulippe ME, Marcos A et al (2013) A consideration of biomarkers to be used for evaluation of inflammation in human nutritional studies. Br J Nutr 109(Suppl 1):S1-S34. https://doi.org/10.1017/S0007114512005119
Hogas S, Bilha SC, Branisteanu D, Hogas M, Gaipov A, Kanbay M, Covic A (2017) Potential novel biomarkers of cardiovascular dysfunction and disease: cardiotrophin-1, adipokines and galectin-3. Arch Med Sci 13(4):897–913. https://doi.org/10.5114/aoms.2016.58664
González-Gil EM, Cadenas-Sanchez C, Santabárbara J, Bueno-Lozano G, Iglesia I, González-Gross M, Molnar D, Gottrand F, De Henauw S, Kafatos A et al; HELENA study group (2018) Inflammation in metabolically healthy and metabolically abnormal adolescents: The HELENA study. Nutr Metab Cardiovasc Dis 28(1):77–83. https://doi.org/10.1016/j.numecd.2017.10.004
Sonnenburg J, Bäckhed F (2016) Diet–microbiota interactions as moderators of human metabolism. Nature 535(7610):56–64. https://doi.org/10.1038/nature18846
German JB, Dillard CJ (2004) Saturated fats: what dietary intake? Am J Clin Nutr 80(3):550–559
Huth P, Fulgoni V, Jandacek RJ, Jones PJ, St-Onge MP, Senanayake V (2010) Bioactivity and emerging role of short and medium chain fatty acids. Lipid Technol 22(12):266–269
Azadbakht L, Mirmiran P, Esmaillzadeh A, Azizi F (2005) Dairy consumption is inversely associated with the prevalence of the metabolic syndrome in Tehranian adults. Am J Clin Nutr 82:523–530
Uyeno Y, Sekiguchi Y, Kamagata Y (2008) Impact of consumption of probiotic lactobacilli-containing yogurt on microbial composition in human feces. Int J Food Microbiol 122(1–2):16–22
García-Albiach R, Pozuelo de Felipe M, Angulo S, Morosini MI, Bravo D, Baquero F, del Campo R (2008) Molecular analysis of yogurt containing Lactobacillus delbrueckii subsp. bulgaricus and Streptococcus thermophilus in human intestinal microbiota. Am J Clin Nutr 87:91–96
Lemieux I, Lamarche B, Couillard C, Pascot A, Cantin B, Bergeron J, Dagenais GR, Després JP (2001) Total cholesterol/HDL cholesterol ratio vs LDL cholesterol/HDL cholesterol ratio as indices of ischemic heart disease risk in men: the Quebec Cardiovascular Study. Arch Intern Med 161(22):2685–2892
Klein A, Friedrich U, Vogelsang H, Jahreis G (2008) Lactobacillus acidophilus 74–2 and Bifidobacterium animalis subsp lactis DGCC 420 modulate unspecific cellular immune response in healthy adults. Eur J Clin Nutr 62(5):584–593
Worthley DL, Le Leu RK, Whitehall VL, Conlon M, Christophersen C, Belobrajdic D, Mallitt KA, Hu Y, Irahara N, Ogino S et al (2009) A human, double-blind, placebo-controlled, crossover trial of prebiotic, probiotic, and synbiotic supplementation: effects on luminal, inflammatory, epigenetic, and epithelial biomarkers of colorectal cancer. Am J Clin Nutr 90(3):578–586. https://doi.org/10.3945/ajcn.2009.28106
Olmedilla-Alonso B, Nova E, García-González N, Martín-Diana AB, Fontecha J, Delgado D, Gredilla AE, Bueno F, Asensio-Vegas C (2017) Effect of ewe’s (semi-skimmed and whole) and cow’s milk-yogurt consumption on the lipid profile of control subjects. A crossover study. Food Nutr Res 61(1):1391669. https://doi.org/10.1080/16546628.2017.1391669
Matsuki T, Watanabe K, Fujimoto J, Takada T, Tanaka R (2004) Use of 16S rRna gene-targeted group-specific primers for real-time PCR analysis of predominant bacteria in human feces. Appl Environ Microbiol 70(12):7220–7228
Gueimonde M, Tölkkö S, Korpimäki T, Salminen S (2004) New real-time quantitative PCR procedure for quantification of bifidobacteria in human fecal samples. Appl Environ Microbiol 70(7):4165–4169
Bartosch S, Fite A, Macfarlane GT, McMurdo ME (2004) Characterization of bacterial communities in feces from healthy elderly volunteers and hospitalized elderly patients by using real-time PCR and effects of antibiotic treatment on the fecal microbiota. Appl Environ Microbiol 70(6):3575–3581
Heilig HGHJ., Zoetendal EG, Vaughan EE, Marteau P, Akkermans ADL, de Vos WM (2002) Molecular diversity of Lactobacillus spp. and other lactic acid bacteria in the human intestine as determined by specific amplification of 16S ribosomal DNA. Appl Environ Microbiol 68:114e23
Rinttilä T, Kassinen A, Malinen E, Krogius L, Palva A (2004) Development of an extensive set of 16S rDNA-targeted primers for quantification of pathogenic and indigenous bacteria in faecal samples by real-time PCR. J Appl Microbiol 97(6):1166–1177
Savard P, Lamarche B, Paradis ME, Thiboutot H, Laurin É, Roy D (2011) Impact of Bifidobacterium animalis subsp. lactis BB-12 and, Lactobacillus acidophilus LA-5-containing yoghurt, on fecal bacterial counts of healthy adults. Int J Food Microbiol 149(1):50–57
Caesar R, Tremaroli V, Kovatcheva-Datchary P, Cani PD, Bäckhed F (2015) Crosstalk between gut microbiota and dietary lipids aggravates WAT inflammation through TLR signaling. Cell Metab 22(4):658–668. https://doi.org/10.1016/j.cmet.2015.07.026
Harvey KA, Walker CL, Pavlina TM, Xu Z, Zaloga GP, Siddiqui RA (2010) Long-chain saturated fatty acids induce pro-inflammatory responses and impact endothelial cell growth. Clin Nutr 29(4):492–500
St-Onge MP, Bosarge A, Goree L, Darnell B (2008) Medium chain triglyceride oil consumption as part of a weight loss diet does Not Lead to an Adverse Metabolic Profile When Compared to Olive Oil. J Am Coll Nutr 27(5):547–552
Tsuji H, Kasai M, Takeuchi H, Nakamura M, Okazaki M, Kondo K (2001) Dietary medium-chain triacylglycerols suppress accumulation of body fat in a double-blind, controlled trial in healthy men and women. J Nutr 131(11):2853–2859
Zhou S, Wang Y, Jacoby JJ, Jiang Y, Zhang Y, Yu LL (2017) Effects of medium- and long-chain triacylglycerols on lipid metabolism and gut microbiota composition in C57BL/6J Mice. J Agric Food Chem 65(31):6599–6607. https://doi.org/10.1021/acs.jafc.7b01803
Aoyama T, Nosaka N, Kasai M (2007) Research on the nutritional characteristics of medium-chain fatty acids. J Med Invest 54(3–4):385–388
Papadimitriou C, Vafopoulou-Mastrojiannaki A, Vieira Silva S, Gomes AM, Malcata FX, Alichanidis E (2007) Identification of peptides in traditional and probiotic sheep milk yoghurt with angiotensin I-converting enzyme (ACE)-inhibitory activity. Food Chem 105(2):647–656
Shena W, Gaskinsb HR, McIntosha M (2014) Influence of dietary fat on intestinal microbes, inflammation, barrier function and metabolic outcomes. J Nutr Biochem 25:270–280
de Wit N, Derrien M, Bosch-Vermeulen H, Oosterink E, Keshtkar S, Duval C, de Vogel-van den Bosch J, Kleerebezem M, Müller M, van der Meer R (2012) Saturated fat stimulates obesity and hepatic steatosis and affects gut microbiota composition by an enhanced overflow of dietary fat to the distal intestine. Am J Physiol Gastrointest Liver Physiol 303(5):G589-G599. https://doi.org/10.1152/ajpgi.00488.2011
Patterson E, O’ Doherty RM, Murphy EF, Wall R, O’ Sullivan O, Nilaweera K, Fitzgerald GF, Cotter PD, Ross RP, Stanton C (2014) Impact of dietary fatty acids on metabolic activity and host intestinal microbiota composition in C57BL/6J mice. Brit J Nutr 20:1–13
Gérard P (2013) Metabolism of cholesterol and bile acids by the gut microbiota. Pathogens 3(1):14–24. https://doi.org/10.3390/pathogens3010014
Devkota S, Wang Y, Musch MW, Leone V, Fehlner-Peach H, Nadimpalli A, Antonopoulos DA, Jabri B, Chang EB (2012) Dietary-fat-induced taurocholic acid promotes pathobiont expansion and colitis in Il10–/– mice. Nature 487:104–108
Forbes JD, Van Domselaar G, Bernstein CN (2016) The gut microbiota in immune-mediated inflammatory diseases. Front Microbiol 7:1081. https://doi.org/10.3389/fmicb.2016.01081
Yamashiro K, Tanaka R, Urabe T, Ueno Y, Yamashiro Y, Nomoto K, Takahashi T, Tsuji H, Asahara T, Hattori N (2017) Gut dysbiosis is associated with metabolism and systemic inflammation in patients with ischemic stroke. PLoS One 12(2):e0171521. https://doi.org/10.1371/journal.pone
Fu J, Bonder MJ, Cenit MC, Tigchelaar EF, Maatman A, Dekens JA, Brandsma E, Marczynska J, Imhann F, Weersma RK et al. (2015) The gut microbiome contributes to a substantial proportion of the variation in blood lipids. Circ Res 117(9):817–824. https://doi.org/10.1161/CIRCRESAHA.115.306807
Acknowledgements
This research was financed by MINECO Agro Technological Institute (ITACyL) and INIA (National Institute for Agricultural and Food Research and Technology) through the project RTA2012-00113-CO2-01 and co-financed through the European Regional Development Fund. It also received complementary funding from Quesos Artesanos de Letur S.A. Natalia García-González is the recipient of predoctoral contract FPI-INIA-19-2014, financed by INIA and the European Social Fund. The authors would like to thank Christian Hansen (Isabel López-Viñas) for kindly supplying the starter cultures and Irene Santiago for technical support.
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The current project was approved by the Hospital Universitario Puerta de Hierro-Majadahonda, (Madrid, Spain) (Record no 305, dated 9 December 2014) and the Bioethics Committee of the Spanish Scientific Research Council (CSIC). The study was carried out according to the Declaration of Helsinki (59ª General Assembly, Seúl, Corea, October 2008) and the Good Clinical Practices. Signed informed consent was obtained from all volunteers.
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Redondo, N., García-González, N., Diaz-Prieto, L.E. et al. Effects of ewe’s milk yogurt (whole and semi-skimmed) and cow’s milk yogurt on inflammation markers and gut microbiota of subjects with borderline-high plasma cholesterol levels: a crossover study. Eur J Nutr 58, 1113–1124 (2019). https://doi.org/10.1007/s00394-018-1626-0
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DOI: https://doi.org/10.1007/s00394-018-1626-0