Effects of kefir or milk supplementation on zonulin in overweight subjects

Journal of Dairy Science

Volumn 103, Issue 5, 2020, Pages 3961-3970

  Pražnikar, Z Jenko ^a   Kenig, S ^a   Vardjan, T ^b   Bizjak, M Černelič ^a   Petelin, A ^a  

^a UNIVERSITY OF PRIMORSKA   (Slovenia)

^b doo   (Slovenia)

Author keywords

intestinal permeability; kefir; low grade chronic inflammation; overweight

Indexed keywords

BIOLOGICAL MARKER; HAPTOGLOBIN; KEFIR; PROTEIN PRECURSOR; TRIACYLGLYCEROL; ZONULIN;

ADULT; ANIMAL; BLOOD; CONTROLLED STUDY; CROSSOVER PROCEDURE; FEMALE; HUMAN; INTESTINE ABSORPTION; INTESTINE MUCOSA; MALE; METABOLISM; MIDDLE AGED; MILK; OBESITY; RANDOMIZED CONTROLLED TRIAL;

ADULT; ANIMALS; BIOMARKERS; CROSS-OVER STUDIES; FEMALE; HAPTOGLOBINS; HUMANS; INTESTINAL ABSORPTION; INTESTINAL MUCOSA; KEFIR; MALE; MIDDLE AGED; MILK; OVERWEIGHT; PROTEIN PRECURSORS; TRIGLYCERIDES;

EID: 85081926054     PISSN: 00220302     EISSN: 15253198     Source Type: Journal    
DOI: 10.3168/jds.2019-17696     Document Type: Article

References (59)

1. Adiïloğlu, A.K., Gönülateş, N., Işler, M., Senol, A., The effect of kefir consumption on human immune system: A cytokine study. Mikrobiyol. Bul. 47 (2013), 273–281 https://doi.org/10.5578/mb.4709 23621727.
2. Alberti, K.G., Eckel, R.H., Grundy, S.M., Zimmet, P.Z., Cleeman, J.I., Donato, K.A., Fruchart, J.C., James, W.P., Loria, C.M., Smith, S.C. Jr, Harmonizing the metabolic syndrome: A joint interim statement of the International Diabetes Federation Task Force on Epidemiology and Prevention; National Heart, Lung, and Blood Institute; American Heart Association; World Heart Federation; International Atherosclerosis Society; and International Association for the Study of Obesity. Circulation 120 (2009), 1640–1645 https://doi.org/10.1161/CIRCULATIONAHA.109.192644 19805654.
3. Arora, T., Sharma, R., Frost, G., Propionate. Anti-obesity and satiety enhancing factor?. Appetite 56 (2011), 511–515 https://doi.org/10.1016/j.appet.2011.01.016 21255628.
4. Arrieta, M.C., Bistritz, L., Meddings, J.B., Alterations in intestinal permeability. Gut 55 (2006), 1512–1520 https://doi.org/10.1136/gut.2005.085373 16966705.
5. Boroni Moreira, A.P., de Cássia Gonçalves Alfenas, R., The influence of endotoxemia on the molecular mechanisms of insulin resistance. Nutr. Hosp. 27 (2012), 382–390 10.1590/S0212-16112012000200007 22732959.
6. Boulangé, C.L., Neves, A.L., Chilloux, J., Nicholson, J.K., Dumas, M.E., Impact of the gut microbiota on inflammation, obesity, and metabolic disease. Genome Med., 8, 2016, 42 https://doi.org/10.1186/s13073-016-0303-2 27098727.
7. Cani, P.D., Bibiloni, R., Knauf, C., Waget, A., Neyrinck, A.M., Delzenne, N.M., Burcelin, R., Changes in gut microbiota control metabolic endotoxemia-induced inflammation in high-fat diet-induced obesity and diabetes in mice. Diabetes 57 (2008), 1470–1481 https://doi.org/10.2337/db07-1403 18305141.
8. Chassaing, B., Gewirtz, A.T., Gut microbiota, low-grade inflammation, and metabolic syndrome. Toxicol. Pathol. 42 (2014), 49–53 https://doi.org/10.1177/0192623313508481 24285672.
9. Christensen, R., Lorenzen, J.K., Svith, C.R., Bartels, E.M., Melanson, E.L., Saris, W.H., Tremblay, A., Astrup, A., Effect of calcium from dairy and dietary supplements on faecal fat excretion: A meta-analysis of randomized controlled trials. Obes. Rev. 10 (2009), 475–486 https://doi.org/10.1111/j.1467-789X.2009.00599.x 19493303.
10. Ejtahed, H.-S., Angoorani, P., Soroush, A.-R., Atlasi, R., Hasani-Ranjbar, S., Mortazavian, A.M., Larijani, B., Probiotics supplementation for the obesity management; A systematic review of animal studies and clinical trials. J. Funct. Foods 52 (2019), 228–242 https://doi.org/10.1016/j.jff.2018.10.039.
11. El-Sayed, M., Awad, S., Wahba, A., El-Attar, A., Yousef, M., Zedan, M., In vivo anti-diabetic and biological activities of milk protein and milk 1 protein hydrolyaste. J. Adv. Dairy Res., 4, 2016, 1.
12. Everard, A., Cani, P.D., Diabetes, obesity and gut microbiota. Best Pract. Res. Clin. Gastroenterol. 27 (2013), 73–83 https://doi.org/10.1016/j.bpg.2013.03.007 23768554.
13. Fathi, Y., Ghodrati, N., Zibaeenezhad, M.J., Faghih, S., Kefir drink causes a significant yet similar improvement in serum lipid profile, compared with low-fat milk, in a dairy-rich diet in overweight or obese premenopausal women: A randomized controlled trial. J. Clin. Lipidol. 11 (2017), 136–146 https://doi.org/10.1016/j.jacl.2016.10.016 28391880.
14. Festi, D., Schiumerini, R., Eusebi, L.H., Marasco, G., Taddia, M., Colecchia, A., Gut microbiota and metabolic syndrome. World J. Gastroenterol. 20 (2014), 16079–16094 https://doi.org/10.3748/wjg.v20.i43.16079 25473159.
15. Gao, J., Ding, G., Li, Q., Gong, L., Huang, J., Sang, Y., Tibet kefir milk decreases fat deposition by regulating the gut microbiota and gene expression of Lpl and Angptl4 in high fat diet-fed rats. Food Res. Int. 121 (2019), 278–287 https://doi.org/10.1016/j.foodres.2019.03.029 31108749.
16. Garrote, G.L., Abraham, A.G., De Antoni, G.L., Chemical and microbiological characterisation of kefir grains. J. Dairy Res. 68 (2001), 639–652 https://doi.org/10.1017/S0022029901005210 11928960.
17. Genser, L., Aguanno, D., Soula, H.A., Dong, L., Trystram, L., Assmann, K., Salem, J.E., Vaillant, J.C., Oppert, J.M., Laugerette, F., Michalski, M.C., Wind, P., Rousset, M., Brot-Laroche, E., Leturque, A., Clément, K., Thenet, S., Poitou, C., Increased jejunal permeability in human obesity is revealed by a lipid challenge and is linked to inflammation and type 2 diabetes. J. Pathol. 246 (2018), 217–230 https://doi.org/10.1002/path.5134 29984492.
18. Gérard, P., Gut microbiota and obesity. Cell. Mol. Life Sci. 73 (2016), 147–162 https://doi.org/10.1007/s00018-015-2061-5 26459447.
19. Gomes, A.C., Bueno, A.A., de Souza, R.G., Mota, J.F., Gut microbiota, probiotics and diabetes. Nutr. J., 13, 2014, 60 https://doi.org/10.1186/1475-2891-13-60 24939063.
20. Griffiths, E.A., Duffy, L.C., Schanbacher, F.L., Qiao, H., Dryja, D., Leavens, A., Rossman, J., Rich, G., Dirienzo, D., Ogra, P.L., In vivo effects of bifidobacteria and lactoferrin on gut endotoxin concentration and mucosal immunity in Balb/c mice. Dig. Dis. Sci. 49 (2004), 579–589 https://doi.org/10.1023/B:DDAS.0000026302.92898.ae 15185861.
21. Hadisaputro, S., Djokomoeljanto, R.R., Judiono, Soesatyo, M.H., The effects of oral plain kefir supplementation on proinflammatory cytokine properties of the hyperglycemia Wistar rats induced by streptozotocin. Acta Med. Indones. 44 (2012), 100–104 22745139.
22. Jayashree, B., Bibin, Y.S., Prabhu, D., Shanthirani, C.S., Gokulakrishnan, K., Lakshmi, B.S., Mohan, V., Balasubramanyam, M., Increased circulatory levels of lipopolysaccharide (LPS) and zonulin signify novel biomarkers of proinflammation in patients with type 2 diabetes. Mol. Cell. Biochem. 388 (2014), 203–210 https://doi.org/10.1007/s11010-013-1911-4 24347174.
23. Kim, D.H., Kim, H., Jeong, D., Kang, I.B., Chon, J.W., Kim, H.S., Song, K.Y., Seo, K.H., Kefir alleviates obesity and hepatic steatosis in high-fat diet-fed mice by modulation of gut microbiota and mycobiota: Targeted and untargeted community analysis with correlation of biomarkers. J. Nutr. Biochem. 44 (2017), 35–43 https://doi.org/10.1016/j.jnutbio.2017.02.014 28384519.
24. Lacroix, I.M., Li-Chan, E.C., Overview of food products and dietary constituents with antidiabetic properties and their putative mechanisms of action: A natural approach to complement pharmacotherapy in the management of diabetes. Mol. Nutr. Food Res. 58 (2014), 61–78 https://doi.org/10.1002/mnfr.201300223 23943383.
25. Lee, M.Y., Ahn, K.S., Kwon, O.K., Kim, M.J., Kim, M.K., Lee, I.Y., Oh, S.R., Lee, H.K., Anti-inflammatory and anti-allergic effects of kefir in a mouse asthma model. Immunobiology 212 (2007), 647–654 https://doi.org/10.1016/j.imbio.2007.05.004 17869642.
26. Li, X., Yin, J., Zhu, Y., Wang, X., Hu, X., Bao, W., Huang, Y., Chen, L., Chen, S., Yang, W., Shan, Z., Liu, L., Effects of whole milk supplementation on gut microbiota and cardiometabolic biomarkers in subjects with and without lactose malabsorption. Nutrients, 10, 2018, 1403 https://doi.org/10.3390/nu10101403 30279333.
27. Liu, H., Xie, Y.H., Xiong, L.X., Dong, R.T., Pan, C.L., Teng, G.X., Zhang, H.X., Effect mechanism of cholesterol lowering by Kluyveromyces from Tibetan kefir. Adv. Mat. Res. 343 (2012), 1290–1298.
28. Maki, K.C., Nieman, K.M., Schild, A.L., Kaden, V.N., Lawless, A.L., Kelley, K.M., Rains, T.M., Sugar-sweetened product consumption alters glucose homeostasis compared with dairy product consumption in men and women at risk of type 2 diabetes mellitus. J. Nutr. 145 (2015), 459–466 https://doi.org/10.3945/jn.114.204503 25733460.
29. Moreno-Navarrete, J.M., Sabater, M., Ortega, F., Ricart, W., Fernández-Real, J.M., Circulating zonulin, a marker of intestinal permeability, is increased in association with obesity-associated insulin resistance. PLoS One, 7, 2012, e37160 https://doi.org/10.1371/journal.pone.0037160 22629362.
30. Nongonierma, A.B., FitzGerald, R.J., The scientific evidence for the role of milk protein-derived bioactive peptides in humans. J. Funct. Foods 17 (2015), 640–656 https://doi.org/10.1016/j.jff.2015.06.021.
31. Noori, N., Bangash, M.Y., Motaghinejad, M., Hosseini, P., Noudoost, B., Kefir protective effects against nicotine cessation-induced anxiety and cognition impairments in rats. Adv. Biomed. Res., 3, 2014, 251 https://doi.org/10.4103/2277-9175.146377 25590029.
32. Norris, G.H., Jiang, C., Ryan, J., Porter, C.M., Blesso, C.N., Milk sphingomyelin improves lipid metabolism and alters gut microbiota in high fat diet-fed mice. J. Nutr. Biochem. 30 (2016), 93–101 https://doi.org/10.1016/j.jnutbio.2015.12.003 27012625.
33. Ostadrahimi, A., Taghizadeh, A., Mobasseri, M., Farrin, N., Payahoo, L., Beyramalipoor Gheshlaghi, Z., Vahedjabbari, M., Effect of probiotic fermented milk (kefir) on glycemic control and lipid profile in type 2 diabetic patients: A randomized double-blind placebo-controlled clinical trial. Iran. J. Public Health 44 (2015), 228–237 25905057.
34. Otles, S., Cagindi, O., Kefir: A probiotic dairy-composition, nutritional and therapeutic aspects. Pak. J. Nutr. 2 (2003), 54–59 https://doi.org/10.3923/pjn.2003.54.59.
35. Ouchi, N., Parker, J.L., Lugus, J.J., Walsh, K., Adipokines in inflammation and metabolic disease. Nat. Rev. Immunol. 11 (2011), 85–97 https://doi.org/10.1038/nri2921 21252989.
36. Pereira, M.A., Jacobs, D.R. Jr., Van Horn, L., Slattery, M.L., Kartashov, A.I., Ludwig, D.S., Dairy consumption, obesity, and the insulin resistance syndrome in young adults: The CARDIA Study. JAMA 287 (2002), 2081–2089 https://doi.org/10.1001/jama.287.16.2081 11966382.
37. Pimenta, F.S., Luaces-Regueira, M., Ton, A.M., Campagnaro, B.P., Campos-Toimil, M., Pereira, T.M., Vasquez, E.C., Mechanisms of action of kefir in chronic cardiovascular and metabolic diseases. Cell. Physiol. Biochem. 48 (2018), 1901–1914 https://doi.org/10.1159/000492511 30092577.
38. Rios, A.C., Maurya, P.K., Pedrini, M., Zeni-Graiff, M., Asevedo, E., Mansur, R.B., Wieck, A., Grassi-Oliveira, R., McIntyre, R.S., Hayashi, M.A.F., Brietzke, E., Microbiota abnormalities and the therapeutic potential of probiotics in the treatment of mood disorders. Rev. Neurosci. 28 (2017), 739–749 https://doi.org/10.1515/revneuro-2017-0001 28593878.
39. Rodrigues, K.L., Caputo, L.R., Carvalho, J.C., Evangelista, J., Schneedorf, J.M., Antimicrobial and healing activity of kefir and kefiran extract. Int. J. Antimicrob. Agents 25 (2005), 404–408 https://doi.org/10.1016/j.ijantimicag.2004.09.020 15848295.
40. Rosa, D.D., Dias, M.M.S., Grześkowiak, L.M., Reis, S.A., Conceição, L.L., Peluzio, M.D.C.G., Milk kefir: nutritional, microbiological and health benefits. Nutr. Res. Rev. 30 (2017), 82–96 https://doi.org/10.1017/S0954422416000275 28222814.
41. Rosa, D.D., Grześkowiak, Ł.M., Ferreira, C.L., Fonseca, A.C., Reis, S.A., Dias, M.M., Siqueira, N.P., Silva, L.L., Neves, C.A., Oliveira, L.L., Machado, A.B., Peluzio, C., Kefir reduces insulin resistance and inflammatory cytokine expression in an animal model of metabolic syndrome. Food Funct. 7 (2016), 3390–3401 https://doi.org/10.1039/C6FO00339G 27384318.
42. Sapone, A., de Magistris, L., Pietzak, M., Clemente, M.G., Tripathi, A., Cucca, F., Lampis, R., Kryszak, D., Cartenì, M., Generoso, M., Iafusco, D., Prisco, F., Laghi, F., Riegler, G., Carratu, R., Counts, D., Fasano, A., Zonulin upregulation is associated with increased gut permeability in subjects with type 1 diabetes and their relatives. Diabetes 55 (2006), 1443–1449 https://doi.org/10.2337/db05-1593 16644703.
43. Scheffler, L., Crane, A., Heyne, H., Tönjes, A., Schleinitz, D., Ihling, C.H., Stumvoll, M., Freire, R., Fiorentino, M., Fasano, A., Kovacs, P., Heiker, J.T., Widely used commercial ELISA does not detect precursor of haptoglobin2, but recognizes properdin as a potential second member of the zonulin family. Front Endocrinol (Lausanne)., 9, 2018, 22 10.3389/fendo.2018.00022.
44. Scherer, P.E., Hill, J.A., Obesity, diabetes, and cardiovascular diseases: A compendium. Circ. Res. 118 (2016), 1703–1705 https://doi.org/10.1161/CIRCRESAHA.116.308999 27230636.
45. Sepple, C.P., Read, N.W., Gastrointestinal correlates of the development of hunger in man. Appetite 13 (1989), 183–191 https://doi.org/10.1016/0195-6663(89)90011-1 2596841.
46. Soerensen, K.V., Thorning, T.K., Astrup, A., Kristensen, M., Lorenzen, J.K., Effect of dairy calcium from cheese and milk on fecal fat excretion, blood lipids, and appetite in young men. Am. J. Clin. Nutr. 99 (2014), 984–991 https://doi.org/10.3945/ajcn.113.077735 24622806.
47. St-Onge, M.P., Farnworth, E.R., Savard, T., Chabot, D., Mafu, A., Jones, P.J., Kefir consumption does not alter plasma lipid levels or cholesterol fractional synthesis rates relative to milk in hyperlipidemic men: a randomized controlled trial. BMC Complement. Altern. Med., 2, 2002, 1 https://doi.org/10.1186/1472-6882-2-1 11825344.
48. Steenbergen, L., Sellaro, R., van Hemert, S., Bosch, J.A., Colzato, L.S., A randomized controlled trial to test the effect of multispecies probiotics on cognitive reactivity to sad mood. Brain Behav. Immun. 48 (2015), 258–264 https://doi.org/10.1016/j.bbi.2015.04.003 25862297.
49. Sun, Y., Geng, W., Pan, Y., Wang, J., Xiao, P., Wang, Y., Supplementation with Lactobacillus kefiranofaciens ZW3 from Tibetan Kefir improves depression-like behavior in stressed mice by modulating the gut microbiota. Food Funct. 10 (2019), 925–937 https://doi.org/10.1039/C8FO02096E 30698577.
50. Talley, N.J., Holtmann, G.J., Jones, M., Koloski, N.A., Walker, M.M., Burns, G., Potter, M.D.E., Shah, A., Keely, S., Zonulin in serum as a biomarker fails to identify the IBS, functional dyspepsia and non-coeliac wheat sensitivity. Gut, 2019 gutjnl-2019-318664. https://doi.org/10.1136/gutjnl-2019-318664 31563879.
51. van Hemert, S., Verwer, J., Schütz, B., Clinical studies evaluating effects of probiotics on parameters of intestinal barrier function. Adv. Microbiol. 3 (2013), 212–222 10.4236/aim.2013.32032.
52. Vardjan, T., Lorbeg, P.M., Majhenič, A.Č., Stability of prevailing lactobacilli and yeasts in kefir grains and kefir beverages during ten weeks of propagation. Int. J. Dairy Technol. 71 (2018), 51–60 https://doi.org/10.1111/1471-0307.12463.
53. Vardjan, T., Mohar Lorbeg, P., Rogelj, I., Čanžek Majhenič, A., Characterization and stability of lactobacilli and yeast microbiota in kefir grains. J. Dairy Sci. 96 (2013), 2729–2736 https://doi.org/10.3168/jds.2012-5829 23497996.
54. Vinderola, C.G., Duarte, J., Thangavel, D., Perdigón, G., Farnworth, E., Matar, C., Immunomodulating capacity of kefir. J. Dairy Res. 72 (2005), 195–202 https://doi.org/10.1017/S0022029905000828 15909685.
55. Wang, W., Uzzau, S., Goldblum, S.E., Fasano, A., Human zonulin, a potential modulator of intestinal tight junctions. J. Cell Sci. 113 (2000), 4435–4440 11082037.
56. Wang, Y., Xu, N., Xi, A., Ahmed, Z., Zhang, B., Bai, X., Effects of Lactobacillus plantarum MA2 isolated from Tibet kefir on lipid metabolism and intestinal microflora of rats fed on high-cholesterol diet. Appl. Microbiol. Biotechnol. 84 (2009), 341–347 https://doi.org/10.1007/s00253-009-2012-x 19444443.
57. Watson, D., Clark, L.A., Tellegen, A., Development and validation of brief measures of positive and negative affect: The PANAS scales. J. Pers. Soc. Psychol. 54 (1988), 1063–1070 https://doi.org/10.1037/0022-3514.54.6.1063 3397865.
58. Zak-Gołąb, A., Kocełak, P., Aptekorz, M., Zientara, M., Juszczyk, L., Martirosian, G., Chudek, J., Olszanecka-Glinianowicz, M., Gut microbiota, microinflammation, metabolic profile, and zonulin concentration in obese and normal weight subjects. Int. J. Endocrinol., 2013, 2013, 674106 10.1155/2013/674106 23970898.
59. Zimmet, P.Z., Alberti, K.G., The changing face of macrovascular disease in non-insulin-dependent diabetes mellitus: An epidemic in progress. Lancet 350 (1997), S1–S14 https://doi.org/10.1016/S0140-6736(97)90020-9 9250275.