Advertisement

Indian Journal of Gastroenterology

, Volume 34, Issue 2, pp 93–107 | Cite as

Gut microbiome, gut function, and probiotics: Implications for health

  • Neerja Hajela
  • B. S. Ramakrishna
  • G. Balakrish Nair
  • Philip Abraham
  • Sarath Gopalan
  • Nirmal K. Ganguly
Review Article

Abstract

New insights from a rapidly developing field of research have ushered in a new era of understanding of the complexity of host-microbe interactions within the human body. The paradigm shift from culturing to metagenomics has provided an insight into the complex diversity of the microbial species that we harbor, revealing the fact that we are in fact more microbes than human cells. The largest consortium of these microbes resides in the gut and is called the gut microbiota. This new science has expanded the ability to document shifts in microbial populations to an unparalleled degree. It is now understood that signals from the microbiota provide trophic, nutritional, metabolic, and protective effects for the development and maintenance of the host digestive, immune, and neuroendocrine system. Evidence linking changes in the gut microbiota to gastrointestinal and extraintestinal disorders like irritable bowel syndrome, inflammatory bowel disease, obesity, diabetes, and celiac disease have begun to emerge recently. Probiotics act through diverse mechanisms positively affecting the composition and/or function of the commensal microbiota and alter host immunological responses. Well-controlled intervention trials, systematic reviews, and meta-analysis provide convincing evidence for the benefit of probiotics in prevention and treatment of gastrointestinal as well as extraintestinal disorders.

Keywords

Clinical evidence Gut microbiota Probiotic Mechanisms Metagenomics Probiotics 

Notes

Acknowledgments

The review is a collation of the presentations, views, and latest scientific literature presented by eminent scientists and experts at the probiotic symposium, “Probiotics, Microbiome and Gut Function—Transforming Health and Well Being” that was organized by the Yakult India Microbiota and Probiotic Science Foundation in New Delhi, on 14 and 15, February 2014.

References

  1. 1.
    Clemente JC, Ursell LK, Parfrey LG, Knight R. The impact of the gut microbiota on human health: an integrative health. Cell. 2012;148:1258–70.PubMedGoogle Scholar
  2. 2.
    Martin FP, Collino S, Rezzi S, Kochhar S. Metabolomic applications to decipher gut microbial metabolic influence in health and disease. Front Physiol. 2012;3:113.PubMedCentralPubMedGoogle Scholar
  3. 3.
    O’Hara AM, Shanahan F. The gut flora as a forgotten organ. EMBO Rep. 2006;7:688–93.PubMedCentralPubMedGoogle Scholar
  4. 4.
    Van Itallie CM, Anderson JM. Claudins and epithelial paracellular transport. Annu Rev Physiol. 2006;68:403–29.PubMedGoogle Scholar
  5. 5.
    Qin J, Li Y, Cai Z, et al. A metagenome-wide association study of gut microbiota in type 2 diabetes. Nature. 2012;490:55–60.PubMedGoogle Scholar
  6. 6.
    Gareau MG, Sherman PM, Walker WA. Probiotics and the gut microbiota in intestinal health and disease. Nat Rev Gastroenterol Hepatol. 2010;7:503–14.PubMedGoogle Scholar
  7. 7.
    Conroy ME, Shi HN, Walker WA. The long-term health effects of neonatal microbial flora. Curr Opin Allergy Clin Immunol. 2009;9:197–201.PubMedGoogle Scholar
  8. 8.
    Martín R, Langa S, Reviriego C, et al. Human milk is a source of lactic acid bacteria for the infant gut. J Pediatr. 2003;143:754–8.PubMedGoogle Scholar
  9. 9.
    Aureli P, Capurso L, Castellazzi AM, et al. Probiotics and health: an evidence-based review. Pharmacol Res. 2011;63:366–76.PubMedGoogle Scholar
  10. 10.
    Monira S, Nakamura S, Gotoh K, et al. Gut microbiota of healthy and malnourished children in Bangladesh. Front Microbiol. 2011;2:228.PubMedCentralPubMedGoogle Scholar
  11. 11.
    Ghosh TS, Gupta SS, Bhattacharya T, et al. Gut microbiomes of Indian children of varying nutritional status. PLoS ONE. 2014;9:e95547.PubMedCentralPubMedGoogle Scholar
  12. 12.
    Smith MI, Yatsunenko T, Manary MJ, et al. Gut microbiomes of Malawian twin pairs discordant for kwashiorkor. Science. 2013;339:548–54.PubMedCentralPubMedGoogle Scholar
  13. 13.
    Sheridan PO, Bindels LB, Saulnier DM, et al. Can prebiotics and probiotics improve therapeutic outcomes for undernourished individuals? Gut Microbes. 2014;5:74–82.PubMedCentralPubMedGoogle Scholar
  14. 14.
    Claesson MJ, O’Sullivon O, Wang Q, et al. Comparative analysis of pyrosequencing and a phylogenetic microarray for exploring microbial community structures in the human distal intestine. PLoS ONE. 2009;4:e6669.PubMedCentralPubMedGoogle Scholar
  15. 15.
    Eckburg PB, Bik EM, Bernstein CN, et al. Diversity of the human intestinal microbial flora. Science. 2005;308:1635–8.PubMedCentralPubMedGoogle Scholar
  16. 16.
    Sokol H, Pigneur B, Watterlot L, et al. Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patents. Proc Natl Acad Sci U S A. 2008;105:16731–6.PubMedCentralPubMedGoogle Scholar
  17. 17.
    Kaser A, Zeissig S, Blumberg RS. Genes and environment: how much our concepts on the pathophysiology of IBD develop in the future? Dig Dis. 2010;28:395–405.PubMedCentralPubMedGoogle Scholar
  18. 18.
    Balamurugan R, Rajendiran E, George S, Samuel GV, Ramakrishna BS. Real-time polymerase chain reaction quantification of specific butyrate-producing bacteria, Desulfovibrio and Enterococcus faecalis in the feces of patients with colorectal cancer. J Gastroenterol Hepatol. 2008;23:1298–303.PubMedGoogle Scholar
  19. 19.
    Kumari R, Ahuja A, Jaishree P. Fluctuations in butyrate-producing bacteria in ulcerative colitis patients of North India. World J Gastroenterol. 2013;19:3404–14.PubMedCentralPubMedGoogle Scholar
  20. 20.
    Bercik P, Park AJ, Sinclair D, et al. The anxiolytic effect of Bifidobacterium longum NCC3001 involves vagal pathways for gut-brain communication. Neurogastroenterol Motil. 2011;23:1132–9.PubMedCentralPubMedGoogle Scholar
  21. 21.
    Ley RE, Backhed F, Turnbaugh P, Lozupone CA, Knight RD, Gordon JI. Obesity alters gut microbial ecology. Proc Natl Acad Sci U S A. 2005;102:11070–5.PubMedCentralPubMedGoogle Scholar
  22. 22.
    Ley RE, Turnbaugh PJ, Klein S, Gordon JI. Microbial ecology: human gut microbes associated with obesity. Nature. 2006;444:1022–3.PubMedGoogle Scholar
  23. 23.
    Backhed F, Manchester JK, Semenkovich CF, Gordon JI. Mechanisms underlying the resistance to diet-induced obesity in germ-free mice. Proc Natl Acad Sci U S A. 2007;104:979–84.PubMedCentralPubMedGoogle Scholar
  24. 24.
    Turnbaugh PJ, Hamady M, Yatsunenko T, et al. A core gut microbiome in obese and lean twins. Nature. 2009;457:480–4.PubMedCentralPubMedGoogle Scholar
  25. 25.
    Ridaura VK, Faith JJ, Rey FE, et al. Gut microbiota from twins discordant for obesity modulate metabolism in mice. Science. 2013;341:1241214.PubMedGoogle Scholar
  26. 26.
    Eloe-Fadrosh EA, Rasko DA. The human microbiome: from symbiosis to pathogenesis. Annu Rev Med. 2013;64:145–63.PubMedCentralPubMedGoogle Scholar
  27. 27.
    Koren O, Goodrich JK, Cullender TC, et al. Host remodeling of the gut microbiome and metabolic changes during pregnancy. Cell. 2012;150:470–80.PubMedCentralPubMedGoogle Scholar
  28. 28.
    Wang Z, Klipfell E, Bennett BJ, et al. Gut flora metabolism of phosphatidylcholine promotes cardiovascular disease. Nature. 2011;472:57–63.PubMedCentralPubMedGoogle Scholar
  29. 29.
    Arumugam M, Raes J, Pelletier E, et al. Enterotypes of the human gut microbiome. Nature. 2011;473:174–80.PubMedCentralPubMedGoogle Scholar
  30. 30.
    De Flippo C, Cavalieri D, Di Paola M, et al. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc Natl Acad Sci U S A. 2010;107:14691–6.Google Scholar
  31. 31.
    FAO/WHO. Report on joint FAO/WHO expert consultation on evolution of health and nutritional properties of probiotics in Food including powder milk with live lactic acid bacteria 2001.Google Scholar
  32. 32.
    Sazawal S, Dhingra U, Hiremath G, et al. Prebiotic and probiotic fortified milk in prevention of morbidities among children: community-based, randomized, double-blind, controlled trial. PLoS ONE. 2010;5:e12164.PubMedCentralPubMedGoogle Scholar
  33. 33.
    Bering S, Suchdev S, Sjoltov L, Berggren A, Tetens I, Bukhave K. A lactic acid-fermented oat gruel increases non-haem iron absorption from a phytate-rich meal in healthy women of childbearing age. Br J Nutr. 2006;96:80–5.PubMedGoogle Scholar
  34. 34.
    Saulnier DM, Santos F, Roos S, et al. Exploring metabolic pathway reconstruction and genome-wide expression profiling in Lactobacillus reuteri to define functional probiotic features. PLoS ONE. 2011;6:e18783.PubMedCentralPubMedGoogle Scholar
  35. 35.
    Corr SC, Li Y, Riedel CU, et al. Bacteriocin production as a mechanism for the anti-infective activity of Lactobacillus salivarius UCC118. Proc Natl Acad Sci. 2007;104:7617–21.PubMedCentralPubMedGoogle Scholar
  36. 36.
    Flynn S, van Sinderen D, Thornton GM, Holo H, Nes IF, Collins JK. Characterization of the genetic locus responsible for the production of ABP-118, a novel bacteriocin produced by the probiotic bacterium Lactobacillus salivarius subsp. salivarius UCC118. Microbiology. 2002;148:973–84.PubMedGoogle Scholar
  37. 37.
    Rea M, Sit CS, Clayton E, et al. Thuricin CD, a post-translationally modified bacteriocin with a narrow spectrum of activity against Clostridium difficile. Proc Natl Acad Sci U S A. 2010;107:9352–8.PubMedCentralPubMedGoogle Scholar
  38. 38.
    Rea MC, Dobson A, O’Sullivan O, et al. Effect of broad and narrow spectrum antimicrobials on Clostridium difficile and microbial diversity in a model of the distal colon. Proc Natl Acad Sci U S A. 2011;108:4639–44.PubMedCentralPubMedGoogle Scholar
  39. 39.
    Rosberg-Cody E, Stanton C, O’Mahony L, et al. Recombinant lactobacilli expressing linoleic acid isomerase can modulate the fatty acid composition of host adipose tissue in mice. Microbiology. 2011;157:609–15.PubMedGoogle Scholar
  40. 40.
    Wall R, Ross RP, Shanahan F, et al. Metabolic activity of the enteric microbiota influences the fatty acid composition of murine and porcine liver and adipose tissues. Am J Clin Nutr. 2009;89:1393–401.Google Scholar
  41. 41.
    van Baarlen P, Troost F, van der Meer C, et al. Human mucosal in vivo transcriptome responses to three lactobacilli indicate how probiotics may modulate human cellular pathways. Proc Natl Acad Sci U S A. 2011;108:4562–9.PubMedCentralPubMedGoogle Scholar
  42. 42.
    Sindhu KN, Sowmyanarayanan TV, Paul A, et al. Immune response and intestinal permeability in children with acute gastroenteritis treated with Lactobacillus rhamnosus GG: a randomized, double-blind, placebo-controlled trial. Clin Infect Dis. 2014;58:1107–15.PubMedCentralPubMedGoogle Scholar
  43. 43.
    Ritze Y, Bárdos G, Claus A, et al. Lactobacillus rhamnosus GG protects against non-alcoholic fatty liver disease in mice. PLoS ONE. 2014;9:e80169.PubMedCentralPubMedGoogle Scholar
  44. 44.
    Licciardi PV, Ismail IH, Balloch A, et al. Maternal supplementation with LGG reduces vaccine-specific immune responses in infants at high-risk of developing allergic disease. Front Immunol. 2013;4:381.PubMedCentralPubMedGoogle Scholar
  45. 45.
    Liu F, Li G, Wen K, et al. Lactobacillus rhamnosus GG on rotavirus-induced injury of ileal epithelium in gnotobiotic pigs. J Pediatr Gastroenterol Nutr. 2013;57:750–8.PubMedGoogle Scholar
  46. 46.
    Kantak PA, Bobrow DN, Nyby JG. Obsessive-compulsive-like behaviors in house mice are attenuated by a probiotic (Lactobacillus rhamnosus GG). Behav Pharmacol. 2014;25:71–9.PubMedGoogle Scholar
  47. 47.
    Khailova L, Baird CH, Rush AA, McNamee EN, Wischmeyer PE. Lactobacillus rhamnosus GG improves outcome in experimental pseudomonas aeruginosa pneumonia: potential role of regulatory T cells. Shock. 2013;40:496–503.PubMedGoogle Scholar
  48. 48.
    Luoto R, Ruuskanen O, Waris M, Kalliomäki M, Salminen S, Isolauri E. Prebiotic and probiotic supplementation prevents rhinovirus infections in preterm infants: a randomized, placebo-controlled trial. J Allergy Clin Immunol. 2014;133:405–13.PubMedGoogle Scholar
  49. 49.
    Khailova L, Frank DN, Dominguez JA, Wischmeyer PE. Probiotic administration reduces mortality and improves intestinal epithelial homeostasis in experimental sepsis. Anesthesiology. 2013;119:166–77.PubMedGoogle Scholar
  50. 50.
    Verma A, Shukla G. Probiotics Lactobacillus rhamnosus GG, Lactobacillus acidophilus suppresses DMH-induced procarcinogenic fecal enzymes and preneoplastic aberrant crypt foci in early colon carcinogenesis in Sprague Dawley rats. Nutr Cancer. 2013;65:84–91.PubMedGoogle Scholar
  51. 51.
    Pärtty A, Luoto R, Kalliomäki M, Salminen S, Isolauri E. Effects of early prebiotic and probiotic supplementation on development of gut microbiota and fussing and crying in preterm infants: a randomized, double-blind, placebo-controlled trial. J Pediatr. 2013;163:1272–7.PubMedGoogle Scholar
  52. 52.
    Ritchie ML, Romanuk TN. A meta-analysis of probiotic efficacy for gastrointestinal diseases. PLoS ONE. 2012;7:e34938.PubMedCentralPubMedGoogle Scholar
  53. 53.
    Hemila H, Chalker E. Vitamin C for preventing and treating the common cold. Cochrane Database Syst Rev. 2013;1:CD000980.PubMedGoogle Scholar
  54. 54.
    Douglas RM, Hemila H, Chalker E, Treacy B. Vitamin C for preventing and treating the common cold. Cochrane Database Syst Rev. 2007;18:CD000980.Google Scholar
  55. 55.
    Winzenberg TM, Powell S, Shaw KA, Jones G. Vitamin D supplementation for improving bone mineral density in children. Cochrane Database Syst Rev. 2010; CD006944.Google Scholar
  56. 56.
    Hao Q, Lu Z, Dong BR, Huang CQ, Wu T. Probiotics for preventing acute upper respiratory tract infections. Cochrane Database Syst Rev. 2011;CD006895.Google Scholar
  57. 57.
    Johnston BC, Ma SS, Goldenberg JZ, et al. Probiotics for the prevention of Clostridium difficile-associated diarrhea: a systematic review and meta-analysis. Ann Intern Med. 2012;157:878–88.PubMedGoogle Scholar
  58. 58.
    Hempel S, Newberry SJ, Maher AR, et al. Probiotics for the prevention and treatment of antibiotic-associated diarrhea: a systematic review and meta-analysis. JAMA. 2012;307:1959–69.PubMedGoogle Scholar
  59. 59.
    Alfaleh K, Anabrees J, Bassler D, Al-Kharfi T. Probiotics for prevention of necrotizing enterocolitis in preterm infants. Cochrane Database Syst Rev. 2011; CD005496.Google Scholar
  60. 60.
    Hoveyda N, Heneghan C, Mahtani KR, Perera R, Roberts N, Glasziou P. A systematic review and meta-analysis: probiotics in the treatment of irritable bowel syndrome. BMC Gastroenterol. 2009;9:15.PubMedCentralPubMedGoogle Scholar
  61. 61.
    Allen SJ, Martinez EG, Gregorio GV, Dans LF. Probiotics for treating acute infectious diarrhoea. Cochrane Database Syst Rev. 2010;CD003048.Google Scholar
  62. 62.
    McFarland LV, Elmer GW, McFarland M. Meta-analysis of probiotics for the prevention and treatment of acute pediatric diarrhea. Int J Probiotics Prebiotics 2006;1:63–76.Google Scholar
  63. 63.
    Wolvers D, Antoine JM, Myllyluoma E, et al. Guidance for substantiating the evidence for beneficial effects of probiotics: prevention and management of infections by probiotics. J Nutr. 2010;140:698S–712S.PubMedGoogle Scholar
  64. 64.
    Saran S, Gopalan S, Krishna TP. Use of fermented foods to combat stunting and failure to thrive. Nutrition. 2002;18:393–6.PubMedGoogle Scholar
  65. 65.
    Sur D, Manna B, Niyogi SK, et al. Role of probiotic in preventing acute diarrhoea in children: a community-based, randomized, double-blind placebo-controlled field trial in an urban slum. Epidemiol Infect. 2011;139:919–26.PubMedGoogle Scholar
  66. 66.
    Guarino A, Albano F, Ashkenazi S, et al. European Society for Paediatric Gastroenterology, Hepatology and Nutrition/ European Society for Paediatric Infectious Diseases evidence-based guidelines for the management of acute gastroenteritis in children in Europe: executive summary. J Pediatr Gastroenterol Nutr. 2008;46:619–21.PubMedGoogle Scholar
  67. 67.
    McFarland LV. Evidence-based review of probiotics for antibiotic-associated diarrhea and Clostridium difficile infections. Anaerobe. 2009;15:274–80.PubMedGoogle Scholar
  68. 68.
    Goldenberg JZ, Ma SSY, Saxton JD, et al. Probiotics for the prevention of Clostridium difficile-associated diarrhea in adults and children. Cochrane Database Syst Rev. 2013;5:CD006095.PubMedGoogle Scholar
  69. 69.
    Pattani R, Palda VA, Hwang SW, Shah PS. Probiotics for the prevention of antibiotic-associated diarrhea and Clostridium difficile infection among hospitalized patients: systematic review and meta-analysis. Open Med. 2013;7:e56–67.PubMedCentralPubMedGoogle Scholar
  70. 70.
    Johnston BC, Supina AL, Ospina M, Vohra S. Probiotics for the prevention of pediatric antibiotic-associated diarrhea. Cochrane Database Syst Rev. 2011; CD004827.Google Scholar
  71. 71.
    Nagata S, Asahara T, Ohta T, et al. Effect of the continuous intake of probiotic fermented milk containing Lactobacillus casei strain Shirota on fever in a mass outbreak of norovirus gastroenteritis and the fecal microflora in a health service facility for the aged. Br J Nutr. 2011;106:549–56.PubMedGoogle Scholar
  72. 72.
    Moayyedi P, Ford AC, Talley NJ, et al. The efficacy of probiotics in the treatment of irritable bowel syndrome: a systematic review. Gut. 2010;59:325–32.PubMedGoogle Scholar
  73. 73.
    Clarke G, Cryan JF, Dinan TG, et al. Review article: probiotics for the treatment of irritable bowel syndrome—focus on lactic acid bacteria. Aliment Pharmacol Ther. 2012;35:403–13.PubMedGoogle Scholar
  74. 74.
    Ford AC, Quigley EM, Lacy BE, et al. Efficacy of prebiotics, probiotics and synbiotics in irritable bowel syndrome and chronic idiopathic constipation: systematic review and meta-analysis. Am J Gastroenterol. 2014;109:1547–61.PubMedGoogle Scholar
  75. 75.
    Sanders ME, Guarner F, Guerrant R, et al. An update on the use and investigation of probiotics in health and disease. Gut. 2013;62:787–96.PubMedCentralPubMedGoogle Scholar
  76. 76.
    Darfeuille-Michaud A, Boudeau J, Bulois P, et al. High prevalence of adherent-invasive Escherichia coli associated with ileal mucosa in Crohn’s disease. Gastroenterology. 2004;127:412–21.PubMedGoogle Scholar
  77. 77.
    Kruis W, Fric P, Pokrotnieks J, et al. Maintaining remission of ulcerative colitis with the probiotic Escherichia coli Nissle 1917 is as effective as with standard mesalazine. Gut. 2004;53:1617–23.PubMedCentralPubMedGoogle Scholar
  78. 78.
    Sood A, Midha V, Makharia GK, et al. The probiotic preparation, VSL#3 induces remission in patients with mild-to-moderately active ulcerative colitis. Clin Gastroenterol Hepatol. 2009;7:1202–9.PubMedGoogle Scholar
  79. 79.
    Ghouri YA, Richards DM, Rahimi EF, et al. Systematic review of randomized controlled trials of probiotics, prebiotics, and synbiotics in inflammatory bowel disease. Clin Exp Gastroenterol. 2014;7:473–87.PubMedCentralPubMedGoogle Scholar
  80. 80.
    Shen J, Zuo ZX, Mao AP. Effect of probiotics on inducing remission and maintaining therapy in ulcerative colitis, Crohn’s disease, and pouchitis: meta-analysis of randomized controlled trials. Inflamm Bowel Dis. 2014;20:21–35.PubMedGoogle Scholar
  81. 81.
    Van den Berg MM, Benninga MA, Di Lorenzo C. Epidemiology of childhood constipation: a systematic review. Am J Gastroenterol. 2006;101:2401–9.PubMedGoogle Scholar
  82. 82.
    Koebnick C, Wagner I, Leitsmann P, Stern U, Zunfit HJF. Probiotic beverage containing Lactobacillus casei Shirota improves gastrointestinal symptoms in patients with chronic constipation. Can J Gastroenterol. 2003;17:655–9.PubMedGoogle Scholar
  83. 83.
    Krammer HJ. Effect of Lactobacillus casei Shirota on colonic transit time in patients with chronic constipation. Coloproctology. 2011;33:109–13.Google Scholar
  84. 84.
    Chmielewska A, Szajewska H. Systematic review of randomised controlled trials: probiotics for functional constipation. World J Gastroenterol. 2010;16:69–75.PubMedCentralPubMedGoogle Scholar
  85. 85.
    Coconnier MH, Lievin V, Hemery E, Servin AL. Antagonistic activity against Helicobacter infection in vitro and in vivo by the human Lactobacillus acidophilus strain LB. Appl Environ Microbiol. 1998;64:4573–80.PubMedCentralPubMedGoogle Scholar
  86. 86.
    Sykora J, Valeckova K, Amlerova J, et al. Effects of a specially designed fermented milk product containing probiotic Lactobacillus casei DN-114001 and the eradication of H. pylori in children: a prospective randomized double-blind study. J Clin Gastroenterol. 2005;39:692–8.PubMedGoogle Scholar
  87. 87.
    Mai V, Young CM, Ukhanova M, et al. Fecal microbiota in premature infants prior to necrotizing enterocolitis. PLoS ONE. 2011;6:e20647.PubMedCentralPubMedGoogle Scholar
  88. 88.
    Deshpande G, Rao S, Patole S, Bulsara M. Updated meta-analysis of probiotics for preventing necrotizing enterocolitis in preterm neonates. Pediatrics. 2010;125:921–30.PubMedGoogle Scholar
  89. 89.
    Alfaleh K, Anabrees J, Bassler D. Probiotics reduce the risk of necrotizing enterocolitis in preterm infants: a meta-analysis. Neonatology. 2010;97:93–9.PubMedGoogle Scholar
  90. 90.
    Dhiman RK, Rana B, Agrawal S, et al. Probiotic VSL#3 reduces liver disease severity and hospitalization in patients with cirrhosis: a randomized controlled trial. Gastroenterology. 2014;147:1327–37.PubMedGoogle Scholar
  91. 91.
    Agrawal A, Sharma BC, Sharma P, Sarin SK. Secondary prophylaxis of hepatic encephalopathy in cirrhosis: an open-label, randomized controlled trial of lactulose, probiotics, and no therapy. Am J Gastroenterol. 2012;107:1043–50.PubMedGoogle Scholar
  92. 92.
    Shukla S, Shukla A, Mehboob S, Guha S. Meta-analysis: the effects of gut flora modulation using prebiotics, probiotics and synbiotics on minimal hepatic encephalopathy. Aliment Pharmacol Ther. 2011;33:662–71.PubMedGoogle Scholar
  93. 93.
    Besselink MG, van Santvoort HC, Buskens E, et al. Probiotic prophylaxis in predicted severe acute pancreatitis: a randomised, doubleblind, placebo-controlled trial. Lancet. 2008;371:651–9.PubMedGoogle Scholar
  94. 94.
    Ma YY, Li L, Yu CH, Shen Z, Chen LH, Li YM. Effects of probiotics on nonalcoholic fatty liver disease: a meta-analysis. World J Gastroenterol. 2013;19:6911–8.PubMedCentralPubMedGoogle Scholar
  95. 95.
    Gatt M, Reddy BS, MacFie J. Review article: bacterial translocation in the critically ill—evidence and methods of prevention. Aliment Pharmacol Ther. 2007;25:741–57.PubMedGoogle Scholar
  96. 96.
    Izumo T, Maekawa T, Ida M, et al. Effect of intranasal administration of Lactobacillus pentosus S-PT84 on influenza virus infection in mice. Int Immunopharmacol. 2010;10:1101–6.PubMedGoogle Scholar
  97. 97.
    Kim NY, Ji GE. Effects of probiotics on the prevention of atopic dermatitis. Korean J Pediatr. 2012;55:193–201.PubMedCentralPubMedGoogle Scholar
  98. 98.
    Perdigon G, Alvarez S, Medina M, Vintini E, Roux E. Influence of the oral administration of lactic acid bacteria on IgA producing cells associated to bronchus. Int J Immunopathol Pharmacol. 1999;12:97–102.PubMedGoogle Scholar
  99. 99.
    Liu S, Hu P, Du X, Zhou T, Pei X. Lactobacillus rhamnosus GG supplementation for preventing respiratory infections in children: a meta-analysis of randomized, placebo-controlled trials. Indian Pediatr. 2013;50:377–81.PubMedGoogle Scholar
  100. 100.
    Siempos II, Ntaidou TK, Falagas ME. Impact of the administration of probiotics on the incidence of ventilator-associated pneumonia: a meta-analysis of randomized controlled trials. Crit Care Med. 2010;38:954–62.PubMedGoogle Scholar
  101. 101.
    Kang EJ, Kim SY, Hwang IH, Ji YJ. The effect of probiotics on prevention of common cold: a meta-analysis of randomized controlled trial studies. Korean J Fam Med. 2013;34:2–10.PubMedCentralPubMedGoogle Scholar
  102. 102.
    Ivory K, Chambers SJ, Pin C, et al. Oral delivery of Lactobacillus casei Shirota modifies allergen—induced immune responses in allergic rhinitis. Clin Exp Aller. 2008;38:1282–9.Google Scholar
  103. 103.
    Gleeson M, Bishop NC, Oliveira M, Tauler P. Daily probiotic’s (Lactobacillus casei Shirota) reduction of infection incidence in athletes. Int J Sport Nutr Metab. 2011;21:55–64.Google Scholar
  104. 104.
    Hojsak I, Abdović S, Szajewska H, Milosević M, Krznarić Z, Kolacek S. Lactobacillus GG in the prevention of nosocomial gastrointestinal and respiratory tract infections. Pediatrics. 2010;125:e1171–7.PubMedGoogle Scholar
  105. 105.
    Morrow LE, Kollef MH, Casale TB. Probiotic prophylaxis of ventilator-associated pneumonia: a blinded, randomized, controlled trial. Am J Respir Crit Care Med. 2010;182:1058–64.PubMedCentralPubMedGoogle Scholar
  106. 106.
    Tremaroli V, Bäckhed F. Functional interactions between the gut microbiota and host metabolism. Nature. 2012;489:242–9.PubMedGoogle Scholar
  107. 107.
    Parnell JA, Reimer RA. Weight loss during oligofructose supplementation is associated with decreased ghrelin and increased peptide YY in overweight and obese adults. Am J Clin Nutr. 2009;89:1751–9.PubMedGoogle Scholar
  108. 108.
    Huang Y, Wang X, Wang J, et al. Lactobacillus plantarum strains as potential probiotic cultures with cholesterol-lowering activity. J Dairy Sci. 2013;96:2746–53.PubMedGoogle Scholar
  109. 109.
    Erejuwa OO, Sulaiman SA, Ab Wahab MS. Modulation of gut microbiota in the management of metabolic disorders: the prospects and challenges. Int J Mol Sci. 2014;15:4158–88.PubMedCentralPubMedGoogle Scholar
  110. 110.
    Shida K, Nomoto K. Probiotics as efficient immunopotentiators: translational role in cancer prevention. Indian J Med Res. 2013;138:808–14.PubMedCentralPubMedGoogle Scholar
  111. 111.
    Kumar M, Kumar A, Nagpal R, et al. Cancer-preventing attributes of probiotics: an update. Int J Food Sci Nutr. 2010;61:473–96.PubMedGoogle Scholar
  112. 112.
    Ishikawa H, Akedo I, Otani T, et al. Randomized trial of dietary fiber and Lactobacillus casei administration for prevention of colorectal tumours. Int J Cancer. 2005;116:762–7.PubMedGoogle Scholar
  113. 113.
    Aso Y, Akaza H, Kotake T, et al. Preventive effect of a Lactobacillus casei preparation on the recurrence of superficial bladder cancer in a double blind trial. Eur Urol. 1995;27:104–9.PubMedGoogle Scholar
  114. 114.
    Toi M, Hirota S, Tomotaki A, et al. Probiotic beverage with soy isoflavone consumption for breast cancer prevention: a case-control study. Curr Nutr Food Sci. 2013;9:194–200.PubMedCentralPubMedGoogle Scholar
  115. 115.
    Van Loo J, Clune Y, Bennett M, Collins JK. The SYNCAN project: goals, set-up, first results and settings of the human intervention study. Br J Nutr. 2005;93:S91–8.PubMedGoogle Scholar
  116. 116.
    Grin PM, Kowalewska PM, Alhazzan W, Fox-Robichaud AE. Lactobacillus for preventing recurrent urinary tract infections in women: meta-analysis. Can J Urol. 2013;20:6607–14.PubMedGoogle Scholar
  117. 117.
    Falagas ME, Betsi G, Tokas T, Athanasiou S. Probiotics for prevention of recurrent urinary tract infections in women: a review of the evidence from microbiological and clinical studies. Drugs. 2006;66:1253–61.PubMedGoogle Scholar
  118. 118.
    Mastromarino P, Vitali B, Mosca L. Bacterial vaginosis: a review on clinical trials with probiotics. New Microbiol. 2013;36:229–38.PubMedGoogle Scholar
  119. 119.
    Cagetti MG, Mastroberardino S, Milia E, Cocco F, Lingström P, Campus G. The use of probiotic strains in caries prevention: a systematic review. Nutrients. 2013;5:2530–50.PubMedCentralPubMedGoogle Scholar

Copyright information

© Indian Society of Gastroenterology 2015

Authors and Affiliations

  1. 1.Yakult India Microbiota and Probiotic Science FoundationNew DelhiIndia
  2. 2.SRM Institutes for Medical ScienceChennaiIndia
  3. 3.Translational Health Science and Technology InstituteFaridabadIndia
  4. 4.P D Hinduja Hospital and Medical Research CentreMumbaiIndia
  5. 5.Indraprastha Apollo HospitalNew DelhiIndia
  6. 6.Policy Centre for Biomedical ResearchTranslational Health Science and Technology InstituteFaridabadIndia

Personalised recommendations