Probiotics in human health and disease: from nutribiotics to pharmabiotics

Journal of Microbiology

Volumn 56, Issue 11, 2018, Pages 773-782

  Lee, Eun Sook ^a   Song, Eun Ji ^a,b   Nam, Young Do ^a,b   Lee, So Young ^a,b  

^a Korea Food Research Institute   (South Korea)

^b University of Science and Technology (UST)   (South Korea)

Author keywords

gut microbiome; nutribiotics; pharmabiotics; probiotics

Indexed keywords

DRUG; PROBIOTIC AGENT;

CLASSIFICATION; DIARRHEA; DISEASES; FOOD; HEALTH; HUMAN; INTESTINE FLORA; METABOLIC SYNDROME X;

DIARRHEA; DISEASE; FOOD; GASTROINTESTINAL MICROBIOME; HEALTH; HUMANS; METABOLIC SYNDROME; NUTRIENTS; PHARMACEUTICAL PREPARATIONS; PROBIOTICS;

EID: 85055352418     PISSN: 12258873     EISSN: 19763794     Source Type: Journal    
DOI: 10.1007/s12275-018-8293-y     Document Type: Review

References (109)

1. Aguilar, M., Bhuket, T., Torres, S., Liu, B., and Wong, R.J. 2015. Prevalence of the metabolic syndrome in the United States, 2003–2012. JAMA 313, 1973–1974
2. Agustina, R., Kok, F.J., van de Rest, O., Fahmida, U., Firmansyah, A., Lukito, W., Feskens, E.J., van den Heuvel, E.G., Albers, R., and Bovee-Oudenhoven, I.M. 2012. Randomized trial of probiotics and calcium on diarrhea and respiratory tract infections in Indonesian children. Pediatrics 129, e1155–e1164
3. Allen, S.J., Martinez, E.G., Gregorio, G.V., and Dans, L.F. 2011. Probiotics for treating acute infectious diarrhoea. Sao Paulo Med. J. 129, 185
4. Andreasen, A.S., Larsen, N., Pedersen-Skovsgaard, T., Berg, R.M., Møller, K., Svendsen, K.D., Jakobsen, M., and Pedersen, B.K. 2010. Effects of Lactobacillus acidophilus NCFM on insulin sensitivity and the systemic inflammatory response in human subjects. Br. J. Nutr. 104, 1831–1838
5. Arao, K., Wang, Y.M., Inoue, N., Hirata, J., Cha, J.Y., Nagao, K., and Yanagita, T. 2004. Dietary effect of pomegranate seed oil rich in 9cis, 11trans, 13cis conjugated linolenic acid on lipid metabolism in obese, hyperlipidemic OLETF rats. Lipids Health Dis. 3, 24
6. Arora, M. and Baldi, A. 2015. Regulatory categories of probiotics across the globe: A review representing existing and recommended categorization. Indian J. Med. Microbiol. 33, 2–10
7. Aruna, P., Venkataramanamma, D., Singh, A.K., and Singh, R.P. 2016. Health benefits of punicic acid: A review. Compr. Rev. Food Sci. Food Saf. 15, 16–27
8. Banihani, S., Swedan, S., and Alguraan, Z. 2013. Pomegranate and type 2 diabetes. Nutr. Res. 33, 341–348
9. Boussetta, T., Raad, H., Lettéron, P., Gougerot-Pocidalo, M.A., Marie, J.C., Driss, F., and El-Benna, J. 2009. Punicic acid a conjugated linolenic acid inhibits TNFa-induced neutrophil hyperactivation and protects from experimental colon inflammation in rats. PLoS One 4, e6458
10. Bowe, W.P. and Logan, A.C. 2011. Acne vulgaris, probiotics and the gut-brain-skin axis-back to the future? Gut Pathog. 3, 1
11. Brown, A.C. and Valiere, A. 2004. Probiotics and medical nutrition therapy. Nutr. Clin. Care 7, 56–68
12. Burgess, C.M., Smid, E.J., and van Sinderen, D. 2009. Bacterial vitamin B2, B11 and B12 overproduction: An overview. Int. J. Food Microbiol. 133, 1–7
13. Burgio, G.R., Flatz, G., Barbera, C., Patane, R., Boner, A., Cajozzo, C., and Flatz, S.D. 1984. Prevalence of primary adult lactose malabsorption and awareness of milk intolerance in Italy. Am. J. Clin. Nutr. 39, 100–104
14. Butel, M.J. 2014. Probiotics, gut microbiota and health. Med. Mal. Infect. 44, 1–8
15. Capozzi, V., Russo, P., Duenas, M.T., Lopez, P., and Spano, G. 2012. Lactic acid bacteria producing B-group vitamins: a great potential for functional cereals products. Appl. Microbiol. Biotechnol. 96, 1383–1394
16. Champagne, C.P., Tompkins, T.A., Buckley, N.D., and Green-Johnson, J.M. 2010. Effect of fermentation by pure and mixed cultures of Streptococcus thermophilus and Lactobacillus helveticus on isoflavone and B-vitamin content of a fermented soy beverage. Food Microbiol. 27, 968–972
17. Claesson, M.J., Jeffery, I.B., Conde, S., Power, S.E., O’Connor, E.M., Cusack, S., Harris, H.M., Coakley, M., Lakshminarayanan, B., and O’Sullivan, O. 2012. Gut microbiota composition correlates with diet and health in the elderly. Nature 488, 178
18. Corgneau, M., Scher, J., Ritie-Pertusa, L., Le, D.T.l., Petit, J., Nikolova, Y., Banon, S., and Gaiani, C. 2017. Recent advances on lactose intolerance: Tolerance thresholds and currently available answers. Crit. Rev. Food Sci. Nutr. 57, 3344–3356
19. Crider, K.S., Yang, T.P., Berry, R.J., and Bailey, L.B. 2012. Folate and DNA methylation: A review of molecular mechanisms and the evidence for Folate’s role. Adv. Nutr. 3, 21–38
20. Cristina, L., Erika, M., Alessandro, P., Roberto, M., Carlo, G., and Enrica, P. 2011. Proteomic characterization of a selenium-metabolizing probiotic Lactobacillus reuteri Lb2 BM for nutraceutical applications. Proteomics 11, 2212–2221
21. Crittenden, R.G., Martinez, N.R., and Playne, M.J. 2003. Synthesis and utilisation of folate by yoghurt starter cultures and probiotic bacteria. Int. J. Food Microbiol. 80, 217–222
22. Dainese, R., Casellas, F., Mariné-Barjoan, E., Vivinus-Nébot, M., Schneider, S.M., Hébuterne, X., and Piche, T. 2014. Perception of lactose intolerance in irritable bowel syndrome patients. Eur. J. Gastroenterol. Hepatol. 26, 1167–1175
23. Dao, M.C., Everard, A., Aron-Wisnewsky, J., Sokolovska, N., Prifti, E., Verger, E.O., Kayser, B.D., Levenez, F., Chilloux, J., and Hoyles, L. 2015. Akkermansia muciniphila and improved metabolic health during a dietary intervention in obesity: relationship with gut microbiome richness and ecology. Gut 65, 426–436
24. Das, L., Bhaumik, E., Raychaudhuri, U., and Chakraborty, R. 2012. Role of nutraceuticals in human health. J. Food Sci. Technol. 49, 173–183
25. Dash, D.K., Dash, M., Mohanty, M., and Acharya, N. 2017. Efficacy of probiotic Saccharomyces boulardii as an adjuvant therapy in acute childhood diarrhoea. J. Nepal Paediatr. Soc. 36, 250–255
26. De La Cuesta-Zuluaga, J., Mueller, N.T., Corrales-Agudelo, V., Velásquez-Mejía, E.P., Carmona, J.A., Abad, J.M., and Escobar, J.S. 2017. Metformin is associated with higher relative abundance of mucin-degrading Akkermansia muciniphila and several short-chain fatty acid-producing microbiota in the gut. Diabetes Care 40, 54–62
27. Decroos, K., Vanhemmens, S., Cattoir, S., Boon, N., and Verstraete, W. 2005. Isolation and characterisation of an equol-producing mixed microbial culture from a human faecal sample and its activity under gastrointestinal conditions. Arch. Microbiol. 183, 45–55
28. Delzenne, N.M. and Cani, P.D. 2011. Gut microbiota and the pathogenesis of insulin resistance. Curr. Diabetes Rep. 11, 154
29. Deng, Y., Misselwitz, B., Dai, N., and Fox, M. 2015. Lactose intolerance in adults: biological mechanism and dietary management. Nutrients 7, 8020–8035
30. Devriese, S., Eeckhaut, V., Geirnaert, A., Van den Bossche, L., Hindryckx, P., Van de Wiele, T., Van Immerseel, F., Ducatelle, R., De Vos, M., and Laukens, D. 2017. Reduced mucosa-associated Butyricicoccus activity in patients with ulcerative colitis correlates with aberrant claudin-1 expression. J. Crohn’s Colitis 11, 229–236
31. Dierksen, K.P., Moore, C.J., Inglis, M., Wescombe, P.A., and Tagg, J.R. 2007. The effect of ingestion of milk supplemented with salivaricin A-producing Streptococcus salivarius on the bacteriocinlike inhibitory activity of streptococcal populations on the tongue. FEMS Microbiol. Ecol. 59, 584–591
32. Doron, S., Snydman, D.R., and Gorbach, S.L. 2005. Lactobacillus GG: bacteriology and clinical applications. Gastroenterol. Clin. 34, 483–498
33. Eeckhaut, V., Ducatelle, R., Sas, B., Vermeire, S., and Van Immerseel, F. 2014. Progress towards butyrate-producing pharmabiotics: Butyricicoccus pullicaecorum capsule and efficacy in TNBS models in comparison with therapeutics. Gut 63, 367–367
34. Elbandy, M. and Ashoush, I. 2012. Phytochemicals in pomegranate seeds and their effect as hypolipidemic agent in hypercholesterolemic rats. World J. Dairy Food Sci. 7, 85–92
35. Everard, A., Belzer, C., Geurts, L., Ouwerkerk, J.P., Druart, C., Bindels, L.B., Guiot, Y., Derrien, M., Muccioli, G.G., Delzenne, N.M., et al. 2013. Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity. Proc. Natl. Acad. Sci. USA 110, 9066–9071
36. Fabian, E. and Elmadfa, I. 2006. Influence of daily consumption of probiotic and conventional yoghurt on the plasma lipid profile in young healthy women. Ann. Nutr. Metab. 50, 387–393
37. Fabian, E., Majchrzak, D., Dieminger, B., Meyer, E., and Elmadfa, I. 2008. Influence of probiotic and conventional yoghurt on the status of vitamins B1, B2 and B6 in young healthy women. Ann. Nutr. Metab. 52, 29–36
38. FAO/WHO. 2001. Report of a joint FAO/WHO expert consultation. Health and nutritional properties of probiotics in food include powder milk with live lactic acid bacteria, Cordoba, Argentina
39. Frank, L.L. 2015. Thiamin in clinical practice. JPEN J. Parenter. Enteral Nutr. 39, 503–520
40. Ghosh, T.S., Gupta, S.S., Bhattacharya, T., Yadav, D., Barik, A., Chowdhury, A., Das, B., Mande, S.S., and Nair, G.B. 2014. Gut microbiomes of Indian children of varying nutritional status. PLoS One 9, e95547
41. Gorissen, L., Raes, K., Weckx, S., Dannenberger, D., Leroy, F., De Vuyst, L., and De Smet, S. 2010. Production of conjugated linoleic acid and conjugated linolenic acid isomers by Bifidobacterium species. Appl. Microbiol. Biotechnol. 87, 2257–2266
42. Guarner, F., Perdigon, G., Corthier, G., Salminen, S., Koletzko, B., and Morelli, L. 2005. Should yoghurt cultures be considered probiotic? Br. J. Nutr. 93, 783–786
43. Guru, V. and Viswanathan, L. 2013. Riboflavin production in milk whey using probiotic bacteria-Lactobacillus acidophilus and Lactococcus lactis. Indian J. Fundam. Appl. Life Sci. 3, 169–176
44. Hill, C. 2010. Probiotics and pharmabiotics: alternative medicine or an evidence-based alternative? Bioeng. Bugs 1, 79–84
45. Hoffman, F.A. 2008. Development of probiotics as biologic drugs. Clin. Infect. Dis. 46, S125–S127
46. Hou, J.W., Yu, R.C., and Chou, C.C. 2000. Changes in some components of soymilk during fermentation with bifidobacteria. Food Res. Int. 33, 393–397
47. Hugenholtz, J. and Smid, E.J. 2002. Nutraceutical production with food-grade microorganisms. Curr. Opin. Biotechnol. 13, 497–507
48. Hugenholtz, J., Sybesma, W., Groot, M.N., Wisselink, W., Ladero, V., Burgess, K., van Sinderen, D., Piard, J.C., Eggink, G., Smid, E.J., et al. 2002. Metabolic engineering of lactic acid bacteria for the production of nutraceuticals. Antonie van Leeuwenhoek 82, 217–235
49. Huseini, H.F., Rahimzadeh, G., Fazeli, M.R., Mehrazma, M., and Salehi, M. 2012. Evaluation of wound healing activities of kefir products. Burns 38, 719–723
50. Iqbal, M.P., Lindblad, B.S., Mehboobali, N., Yusuf, F.A., Khan, A.H., and Iqbal, S.P. 2009. Folic acid and vitamin B6 deficiencies related hyperhomocysteinemia in apparently healthy Pakistani adults; is mass micronutrient supplementation indicated in this population? J. Coll. Physicians Surg. Pak. 19, 308–312
51. Jayashree, S., Jayaraman, K., and Kalaichelvan, G. 2010. Isolation, screening and characterization of riboflavin producing lactic acid bacteria from Katpadi, Vellore district. Recent Res. Sci. Technol. 2, 83–88
52. Juarez del Valle, M., Laiño, J.E., Savoy de Giori, G., and Le Blanc, J.G. 2014. Riboflavin producing lactic acid bacteria as a biotechnological strategy to obtain bio-enriched soymilk. Food Res. Int. 62, 1015–1019
53. Kaur, J. 2014. A comprehensive review on metabolic syndrome. Cardiol. Res. Pract. 2014, 943162
54. Kehagias, C., Csapó, J., Konteles, S., Kolokitha, E., Koulouris, S., and Csapó-Kiss, Z. 2008. Support of growth and formation of D-amino acids by Bifidobacterium longum in cows’, ewes’, goats’ milk and modified whey powder products. Int. Dairy J. 18, 396–402
55. Kim, B., Lee, B.W., Hwang, C.E., Lee, Y.Y., Lee, C., Kim, B.J., Park, J.Y., Sim, E.Y., Haque, M., and Lee, D.H. 2015. Screening of conjugated linoleic acid (CLA) producing Lactobacillus plantarum and production of CLA on soy-powder milk by these stains. Korean J. Microbiol. 51, 231–240
56. Kolader, M.E., Vinh, H., Tuyet, P.T.N., Thompson, C., Wolbers, M., Merson, L., Campbell, J.I., Dung, T.T.N., Tuan, H.M., and Chau, N.V.V. 2013. An oral preparation of Lactobacillus acidophilus for the treatment of uncomplicated acute watery diarrhoea in Vietnamese children: study protocol for a multicentre, rando mised, placebo-controlled trial. Trials 14, 27
57. Kootte, R.S., Levin, E., Salojärvi, J., Smits, L.P., Hartstra, A.V., Udayappan, S.D., Hermes, G., Bouter, K.E., Koopen, A.M., Holst, J.J., et al. 2017. Improvement of insulin sensitivity after lean donor feces in metabolic syndrome is driven by baseline intestinal microbiota composition. Cell Metabolism 26, 611–619
58. LeBlanc, J.G., Laino, J.E., del Valle, M.J., Vannini, V., van Sinderen, D., Taranto, M.P., de Valdez, G.F., de Giori, G.S., and Sesma, F. 2011. B-group vitamin production by lactic acid bacteria–current knowledge and potential applications. J. Appl. Microbiol. 111, 1297–1309
59. LeBlanc, J.G., Milani, C., de Giori, G.S., Sesma, F., van Sinderen, D., and Ventura, M. 2013. Bacteria as vitamin suppliers to their host: a gut microbiota perspective. Curr. Opin. Biotechnol. 24, 160–168
60. Lee, E.R., Blount, K.F., and Breaker, R.R. 2009. Roseoflavin is a natural antibacterial compound that binds to FMN riboswitches and regulates gene expression. RNA Biol. 6, 187–194
61. Lee, S.J., Bose, S., Seo, J.G., Chung, W.S., Lim, C.Y., and Kim, H. 2014. The effects of co-administration of probiotics with herbal medicine on obesity, metabolic endotoxemia and dysbiosis: A randomized double-blind controlled clinical trial. Clin. Nutr. 33, 973–981
62. Lee, E.S., Song, E.J., and Nam, Y.D. 2017. Dysbiosis of gut microbiome and its impact on epigenetic regulation. J. Clin. Epigenet. 3, S1
63. Lin, M.Y. and Young, C.M. 2000. Folate levels in cultures of lactic acid bacteria. Int. Dairy J. 10, 409–413
64. Loguercio, C., Del Vecchio Blanco, C., and Coltorti, M. 1987. Enterococcus lactic acid bacteria strain SF68 and lactulose in hepatic encephalopathy: a controlled study. J. Int. Med. Res. 15, 335–343
65. Marteau, P.R., Vrese, M.D., Cellier, C.J., and Schrezenmeir, J. 2001. Protection from gastrointestinal diseases with the use of probiotics. Am. J. Clin. Nutr. 73, 430s–436s
66. Messaoudi, M., Violle, N., Bisson, J.F., Desor, D., Javelot, H., and Rougeot, C. 2011. Beneficial psychological effects of a probiotic formulation (Lactobacillus helveticus R0052 and Bifidobacterium longum R0175) in healthy human volunteers. Gut Microbes 2, 256–261
67. Methé, B.A., Nelson, K.E., Pop, M., Creasy, H.H., Giglio, M.G., Huttenhower, C., Gevers, D., Petrosino, J.F., Abubucker, S., Badger, J.H., et al. 2012. A framework for human microbiome research. Nature 486, 215–221
68. Murphy, E., Cotter, P., Healy, S., Marques, T.M., O’sullivan, O., Fouhy, F., Clarke, S., O’toole, P., Quigley, E.M., and Stanton, C. 2010. Composition and energy harvesting capacity of the gut microbiota: relationship to diet, obesity and time in mouse models. Gut 59, 1635–1642
69. Nguyen, T.T.B., Jin, Y.Y., Chung, H.J., and Hong, S.T. 2017. Pharmabiotics as an emerging medication for metabolic syndrome and its related diseases. Molecules 22, 1795
70. Niedzielin, K., Kordecki, H., and Birkenfeld, B. 2001. A controlled, double-blind, randomized study on the efficacy of Lactobacillus plantarum 299V in patients with irritable bowel syndrome. Eur. J. Gastroenterol. Hepatol. 13, 1143–1147
71. Nobaek, S., Johansson, M.L., Molin, G., Ahrne, S., and Jeppsson, B. 2000. Alteration of intestinal microflora is associated with reduction in abdominal bloating and pain in patients with irritable bowel syndrome. Am. J. Gastroenterol. 95, 1231–1238
72. Oak, S.J. and Jha, R. 2018. The effects of probiotics in lactose intolerance: A systematic review. Crit. Rev. Food Sci. Nutr. 9, 1–9
73. Oliveira, A.C., Ferreira, R.C., and Santos, A.A. 2016. Cardiovascular risk assessment according to the Framingham score and abdominal obesity in individuals seen by a clinical school of nutrition. Rev. Assoc. Med. Bras. 62, 138–144
74. Org, E., Blum, Y., Kasela, S., Mehrabian, M., Kuusisto, J., Kangas, A.J., Soininen, P., Wang, Z., Ala-Korpela, M., and Hazen, S.L. 2017. Relationships between gut microbiota, plasma metabolites, and metabolic syndrome traits in the METSIM cohort. Genome Biol. 18, 70
75. Patterson, E., Cryan, J.F., Fitzgerald, G.F., Ross, R.P., Dinan, T.G., and Stanton, C. 2014. Gut microbiota, the pharmabiotics they produce and host health. Proc. Nutr. Soc. 73, 477–489
76. Pendyala, S., Walker, J.M., and Holt, P.R. 2012. A high-fat diet is associated with endotoxemia that originates from the gut. Gastroenterology 142, 1100–1101
77. Plovier, H., Everard, A., Druart, C., Depommier, C., Van Hul, M., Geurts, L., Chilloux, J., Ottman, N., Duparc, T., and Lichtenstein, L. 2017. A purified membrane protein from Akkermansia muciniphila or the pasteurized bacterium improves metabolism in obese and diabetic mice. Nat. Med. 23, 107
78. Pompei, A., Cordisco, L., Amaretti, A., Zanoni, S., Matteuzzi, D., and Rossi, M. 2007a. Folate production by bifidobacteria as a potential probiotic property. Appl. Environ. Microbiol. 73, 179–185
79. Pompei, A., Cordisco, L., Amaretti, A., Zanoni, S., Raimondi, S., Matteuzzi, D., and Rossi, M. 2007b. Administration of folateroducing bifidobacteria enhances folate status in wistar rats. J. Nutr. 137, 2742–2746
80. Powers, H.J. 2003. Riboflavin (vitamin B-2) and health. Am. J. Clin. Nutr. 77, 1352–1360
81. Qin, J., Li, Y., Cai, Z., Li, S., Zhu, J., Zhang, F., Liang, S., Zhang, W., Guan, Y., and Shen, D. 2012. A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature 490, 55
82. Qin, J., Li, R., Raes, J., Arumugam, M., Burgdorf, K.S., Manichanh, C., Nielsen, T., Pons, N., Levenez, F., Yamada, T., et al. 2010. A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464, 59–65
83. Queipo-Ortuño, M.I., Seoane, L.M., Murri, M., Pardo, M., Gomez-Zumaquero, J.M., Cardona, F., Casanueva, F., and Tinahones, F.J. 2013. Gut microbiota composition in male rat models under different nutritional status and physical activity and its association with serum leptin and ghrelin levels. PLoS One 8, e65465
84. Roberfroid, M.B. 2000. Prebiotics and probiotics: are they functional foods? Am. J. Clin. Nutr. 71, 1682S–1687S; discussion 1688S–1690S
85. Rosenthal, J., Largaespada, N., Bailey, L.B., Cannon, M., Alverson, C.J., Ortiz, D., Kauwell, G.P.A., Sniezek, J., Figueroa, R., Daly, R., et al. 2017. Folate deficiency is prevalent in women of childbearing age in belize and is negatively affected by coexisting vitamin B-12 deficiency: Belize national micronutrient survey 2011. J. Nutr. 147, 1183–1193
86. Roškar, I., Švigelj, K., Štempelj, M., Volfand, J., Štabuc, B., Malovrh, Š., and Rogelj, I. 2017. Effects of a probiotic product containing Bifidobacterium animalis subsp. animalis IM386 and Lactobacillus plantarum MP2026 in lactose intolerant individuals: Randomized, placebo-controlled clinical trial. J. Funct. Foods 35, 1–8
87. Rul, F., Ben-Yahia, L., Chegdani, F., Wrzosek, L., Thomas, S., Noordine, M.L., Gitton, C., Cherbuy, C., Langella, P., and Thomas, M. 2011. Impact of the metabolic activity of Streptococcus thermophilus on the colon epithelium of gnotobiotic rats. J. Biol. Chem. 286, 10288–10296
88. Russo, P., Capozzi, V., Arena, M.P., Spadaccino, G., Duenas, M.T., Lopez, P., Fiocco, D., and Spano, G. 2014. Riboflavin-overproducing strains of Lactobacillus fermentum for riboflavin-enriched bread. Appl. Microbiol. Biotechnol. 98, 3691–3700
89. Schneeberger, M., Everard, A., Gómez-Valadés, A.G., Matamoros, S., Ramírez, S., Delzenne, N.M., Gomis, R., Claret, M., and Cani, P.D. 2015. Akkermansia muciniphila inversely correlates with the onset of inflammation, altered adipose tissue metabolism and metabolic disorders during obesity in mice. Sci. Rep. 5, 16643
90. Shanahan, F. 2010. Gut microbes: from bugs to drugs. Am. J. Gastroenterol. 105, 275–279
91. Shanahan, F., Dinan, T.G., Ross, P., and Hill, C. 2012. Probiotics in transition. Clin. Gastroenterol. Hepatol. 10, 1220–1224
92. Shin, N.R., Lee, J.C., Lee, H.Y., Kim, M.S., Whon, T.W., Lee, M.S., and Bae, J.W. 2014. An increase in the Akkermansia spp. population induced by metformin treatment improves glucose homeostasis in diet-induced obese mice. Gut 63, 727–735
93. Simmering, R. and Breves, R. 2011. Prebiotic cosmetics, pp. 137–147. In Krutmann, J. and Humbert, P. (eds.), Nutrition for healthy skin: Strategies for clinical and cosmetic practice. Springer Berlin Heidelberg, Heidelberg, Berlin, Germany
94. Sreeja, V. and Prajapati, J.B. 2013. Probiotic formulations: Application and status as pharmaceuticals-A review. Probiotics Antimicrob. Proteins 5, 81–91
95. Strozzi, G.P. and Mogna, L. 2008. Quantification of folic acid in human feces after administration of bifidobacterium probiotic strains. J. Clin. Gastroenterol. 42 Suppl 3 Pt 2, S179–184
96. Tanaka, T., Hosokawa, M., Yasui, Y., Ishigamori, R., and Miyashita, K. 2011. Cancer chemopreventive ability of conjugated linolenic acids. Int. J. Mol. Sci. 12, 7495–7509
97. Taylor, R. 2012. Insulin resistance and type 2 diabetes. Diabetes 61, 778–779
98. Thakur, K. and Tomar, S.K. 2015. Exploring indigenous Lactobacillus species from diverse niches for riboflavin production. J. Young Pharm. 7, 122–127
99. Thakur, K., Tomar, S.K., and De, S. 2016. Lactic acid bacteria as a cell factory for riboflavin production. Microb. Biotechnol. 9, 441–451
100. Thakur, K., Tomar, S.K., Singh, A.K., Mandal, S., and Arora, S. 2017. Riboflavin and health: A review of recent human research. Crit. Rev. Food Sci. Nutr. 57, 3650–3660
101. Tilg, H. and Moschen, A.R. 2016. Gut microbiome, obesity, and metabolic syndrome, pp. 447–459. In metabolic syndrome. Springer
102. Turnbaugh, P.J., Hamady, M., Yatsunenko, T., Cantarel, B.L., Duncan, A., Ley, R.E., Sogin, M.L., Jones, W.J., Roe, B.A., Affourtit, J.P., et al. 2008. A core gut microbiome in obese and lean twins. Nature 457, 480
103. Ulluwishewa, D., Anderson, R.C., McNabb, W.C., Moughan, P.J., Wells, J.M., and Roy, N.C. 2011. Regulation of tight junction permeability by intestinal bacteria and dietary components. J. Nutr. 141, 769–776
104. Urbanska, M., Gieruszczak-Bialek, D., and Szajewska, H. 2016. Systematic review with meta-analysis: Lactobacillus reuteri DSM 17938 for diarrhoeal diseases in children. Aliment. Pharmacol. Ther. 43, 1025–1034
105. Vandenplas, Y., Huys, G., and Daube, G. 2015. Probiotics: an update. J. Pediatr. 91, 6–21
106. Wanke, M. and Szajewska, H. 2012. Lack of an effect of Lactobacillus reuteri DSM 17938 in preventing nosocomial diarrhea in children: a randomized, double-blind, placebo-controlled trial. J. Pediatr. 161, 40–43
107. Watson, R.R. and Preedy, V.R. 2015. Probiotics, prebiotics, and synbiotics: Bioactive foods in health promotion. Academic Press
108. Weinstock, G.M. 2012. Genomic approaches to studying the human microbiota. Nature 489, 250–256
109. Yuan, G., Sun, H., Sinclair, A.J., and Li, D. 2009. Effects of conjugated linolenic acid and conjugated linoleic acid on lipid metabolism in mice. Eur. J. Lipid Sci. Technol. 111, 537–545