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Colonization and Impact of Disease and Other Factors on Intestinal Microbiota

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Abstract

The aim of this study was to review the process of microbial colonization and the environmental and host factors that influence colonization and microbial succession. The impact of some diseases on intestinal microbiota composition is also described. Microbial colonization of the gut by maternal vaginal and fecal bacteria begins during and after birth. During the first 2 years of life, specific microbes become established in a process designated microbial succession. Microbial succession in the gastrointestinal tract is influenced by numerous external and internal host-related factors, and by the second year of life, the intestinal microbiota composition is considered identical to that of adults. Nevertheless, intestinal microbiota in both infants and adults remain incompletely characterized and their diversity poorly defined. The main explanation is that many intestinal bacteria that live in an anaerobic environment are difficult or impossible to culture outside the intestine. However, recent advances in molecular biology techniques have initiated the description of new bacteria species. The composition of gut microbiota can be modulated by host, environmental, and bacterial factors, and strong evidence has emerged of substantial modifications during illness or exposure to threatening experiences. It has been postulated that improvements in hygienic measures have led to an increase in allergic diseases (“hygiene hypothesis”). Alterations in gut microbiota and their functions have been widely associated with many chronic and degenerative diseases, including inflammatory bowel disease, colon cancer, and rheumatoid arthritis.

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References

  1. Mackie RI, Sghir A, Gaskins HR (1999) Developmental microbial ecology of neonatal gastrointestinal tract. Am J Clin Nutr 69(Suppl):1035–1045

    Google Scholar 

  2. Gismondo MR, Drago L, Lombardi A (1999) Review of probiotics available to modify gastrointestinal microbiota. Int J Antimicrob Agents 12:287–292

    Article  PubMed  CAS  Google Scholar 

  3. Isolauri E, Kirjavainen PV, Salminen S (2002) Probiotics: A role in the treatment of intestinal infection and inflammation? Gut 50(Suppl):54–59

    Google Scholar 

  4. Isolauri E (2001) Probiotics in human disease. Am J Clin Nutr 73(Suppl):1142–1146

    Google Scholar 

  5. Teitelbaum JE, Walker WA (2002) Nutritional impact of pre- and probiotics as protective gastrointestinal organisms. Annu Rev Nutr 22:107–138

    Article  PubMed  CAS  Google Scholar 

  6. Bezirtzoglou E (1997) The intestinal microbiota during the first weeks of life. Anaerobe 3:173–177

    Article  PubMed  CAS  Google Scholar 

  7. McFarland LV (2000) Normal microbiota: diversity and functions. Microb Ecol Health Dis 12:193–207

    Article  Google Scholar 

  8. Kleesen B, Bezirtzoglou E, Matto J (2000) Cultured-based knowledge on biodiversity, development and stability of human gastrointestinal microbiota. Microb Ecol Health Dis 2(Suppl):53–63

    Article  Google Scholar 

  9. Walker WA, Duffy LC (1998) Diet and bacterial colonization: role of probiotics. J Nutr Biochem 9:668–675

    Article  CAS  Google Scholar 

  10. Thompson-Chagoyán OC, Maldonado J, Gil A (2004) La microbiota intestinal en el niño y la influencia de la dieta sobre su composición. Alim Nutr Salud 11:37–48

    Google Scholar 

  11. Eckburg PB, Bik EM, Bernstein CN, Purdom E, Dethlefsen L, Sargent M (2005) Diversity of the human intestinal microbial microbiota. Science 308:1635–1638

    Article  PubMed  Google Scholar 

  12. Lay C, Rigottier-Gois L, Holmstrøm K, et al. (2005) Colonic microbiota signatures across five northern European countries. Appl Environ Microbiol 71:4153–4155

    Article  PubMed  CAS  Google Scholar 

  13. Seksik P, Rigottier-Gois L, Gramet G, Sutren M, Pochart P, Marteau P, Jian R, Dore J (2003) Alterations of the dominant faecal bacterial groups in patients with Crohn's disease of the colon. Gut 52:237–242

    Article  PubMed  CAS  Google Scholar 

  14. Suau A, Bonnet R, Sutren M, Godon JJ, Gibson GR, Collins MD, Dore J (1999) Direct analysis of genes encoding 16S rRNA from complex communities reveals many novel molecular species within the human gut. Appl Environ Microbiol 65:4799–4807

    PubMed  CAS  Google Scholar 

  15. Zoetendal EG, Akkermans AD, De Vos WM (1998) Temperature gradient gel electrophoresis analysis of 16S rRNA from human fecal samples reveals stable and host-specific communities of active bacteria. Appl Environ Microbiol 64:3854–3859

    PubMed  CAS  Google Scholar 

  16. Rigottier-Gois, L, Le Bourhis AG, Gramet G, Rochet V, Dore J (2003) Fluorescent hybridisation combined with flow cytometry and hybridisation of total RNA to analyse the composition of microbial communities in human feces using 16S rRNA probes. FEMS Microbiol Ecol 43:237–245

    Article  CAS  PubMed  Google Scholar 

  17. Ley RE, Backhed F, Turnbaugh P, Lozupone CA, Knight RD, Gordon JI (2005) Obesity alters gut microbial ecology. Proc Natl Acad Sci USA 102:11070–11075

    Article  PubMed  CAS  Google Scholar 

  18. Franks AH, Harmsen HJ, Raangs GC, Jansen GJ, Schut F, Welling GW (1998) Variations of bacterial populations in human feces measured by fluorescent in situ hybridization with group-specific 16S rRNA-targeted oligonucleotide probes. Appl Environ Microbiol 64:3336–3345

    PubMed  CAS  Google Scholar 

  19. Harmsen HJ, Raangs GC, He T, Degener JE, Welling GW (2002) Extensive set of 16S rRNA-based probes for detection of bacteria in human feces. Appl Environ Microbiol 68:2982–2990

    Article  PubMed  CAS  Google Scholar 

  20. Hayashi H, Sakamoto M, Benno Y (2002) Phylogenetic analysis of the human gut microbiota using 16S rDNA clone libraries and strictly anaerobic culture-based methods. Microbiol Immunol 46:535–548

    PubMed  CAS  Google Scholar 

  21. Hold GL, Pryde SE, Russell VJ, Furrie E, Flint HJ (2002) FEMS Microbiol Ecol 39:33–37

    Article  CAS  PubMed  Google Scholar 

  22. Wang X, Heazlewood SP, Krause DO, Florin TH (2003) Molecular characterization of the microbial species that colonize human ileal and colonic mucosa by using 16S rDNA sequence analysis. J Appl Microbiol 95:508–520

    Article  PubMed  CAS  Google Scholar 

  23. Collins MD, Gibson GR (1999) Probiotics, prebiotics and synbiotics: approaches for modulating the microbial ecology of the gut. Am J Clin Nutr 69(Suppl):1052–1057

    Google Scholar 

  24. Brook I, Barret C, Brinkman C, Martin W, Finegold S (1979) Aerobic and anaerobic bacterial microbiota of the maternal cervix and newborn gastric fluid and conjuntiva: a prospective study. Pediatrics 63:451–455

    PubMed  CAS  Google Scholar 

  25. Long SS, Swenson RM (1977) Development of anaerobic fecal microbiota in healthy newborn infants. J Pediatr 91:298–301

    Article  PubMed  CAS  Google Scholar 

  26. Gewolb IH, Schwalbe RS, Taciak VL, Harrison TS, Panigrahi P (1999) Stool microbiota in extremely low birthweight infants. Arch Dis Child 80:F167–F173

    CAS  Google Scholar 

  27. Yoshioka H, Iseki K, Fujita K (1983) Development and differences of intestinal microbiota in the neonatal period in breast-fed and bottle-fed infants. Pediatrics 72:317–321

    PubMed  CAS  Google Scholar 

  28. Harmsen HJ, Wildeboer-veloo AC, Raangs GC, Wagendorp AA, Klijn N, Bindels JG, Welling GW (2000) Analysis of intestinal development in breast-fed and formula-fed infants by using molecular identification and detection methods. J Pediatr Gastroenterol Nutr 30:61–67

    Article  PubMed  CAS  Google Scholar 

  29. Asquith MT, Harrod JR (1979) Reduction in bacterial contamination in banked human milk. J Pediatr 95:993–994

    Article  PubMed  CAS  Google Scholar 

  30. West PA, Hewitt JH, Murphy OM (1979) The influence of methods of collection and storage on the bacteriology of human milk. J Appl Bacteriol 46:269–277

    PubMed  CAS  Google Scholar 

  31. Grönlund MM, Arvilommi H, Kero P, Lehtonen OP, Isolauri E (2000) Importance of intestinal colonization in the maturation of humoral immunity in early infancy: a prospective follow up study of healthy infants aged 0–6 months. Arch Dis Child 83:F186–F192

    Google Scholar 

  32. Benno Y, Sawada K, Mitsuoka T (1984) The intestinal microbiota of infants: composition of fecal microbiota in breast-fed and bottle-fed infants. Microbiol Immunol 28:975–986

    PubMed  CAS  Google Scholar 

  33. Bengmark S (2000) Colonic food: pre- and probiotics. Am J Gastroenterol 95(Suppl):5–7

    Article  Google Scholar 

  34. Orskov F, Sorensen KB (1975) Escherichia coli serogroups in breast-fed and bottle fed infants. Acta Pathol Microbiol Scand 83:25–30

    CAS  Google Scholar 

  35. Rubaltelli FF, Biadaioli R, Pecile P, Nicoletti P (1998) Intestinal microbiota in breast-fed and bottle-fed infants. J Perinat Med 26:186–191

    Article  PubMed  CAS  Google Scholar 

  36. Stark PL, Lee A (1982) The microbial ecology of the large bowel of breast-fed and formula-fed infants during the first year of life. J Med Microbiol 15:189–203

    Article  PubMed  CAS  Google Scholar 

  37. Salminen S, Bouley C, Boutron-Ruault MC, Cummings JH, Franck A, Gibson GR, Isolauri E, Moreau MC, Roberfroid M, Rowland I (1998) Functional food science and gastrointestinal physiology and fuction. Br J Nutr 80(Suppl):147–171

    Article  Google Scholar 

  38. Mackowiak PA (1982) The normal microbial microbiota. N Engl J Med 307:83–93

    Article  PubMed  CAS  Google Scholar 

  39. Bennet R, Eriksson M, Nord CE, Zetterstrom R (1986) Fecal bacterial microbiota of newborn infants during intensive care management and treatment with five antibiotic regimens. Pediatr Infect Dis J 5:533–539

    Article  CAS  Google Scholar 

  40. Goldman DA, Leclair J, Macone A (1978) Bacterial colonization of neonates admitted to an intensive care environment. J Pediatr 93:288–293

    Article  Google Scholar 

  41. Akata H, Yoshioka H, Fujita K (1985) Development of the intestinal microbiota in very low birth weight infants compared to normal full-term infants. Eur J Pediatr 144:186–190

    Article  Google Scholar 

  42. Hall MA, Cole CB, Smith SL, Fuller R, Rolles CJ (1990) Factors influencing the presence of fecal lactobacilli in early infancy. Arch Dis Child 65:185–188

    Article  PubMed  CAS  Google Scholar 

  43. Fanaro S, Chierici R, Guerrini P, Vigi V (2003) Intestinal microbiota in early infancy: composition and development. Acta Paediatr Suppl 441:48–55

    Google Scholar 

  44. Simon GL, Gorbach SL (1984) Intestinal microbiota in health and disease. Gastroenterology 86:174–193

    PubMed  CAS  Google Scholar 

  45. Mitsuoka T (1982) Recent trends in research on intestinal microbiota. Bifidobacteria Microbiota 1:3–24

    Google Scholar 

  46. Hentges DJ (1993) The anaerobic microbiota of the human body. Clin Infect Dis 6(Suppl):175–180

    Google Scholar 

  47. Guarner F, Malagelada JR (2003) Gut microbiota in health and disease. Lancet 361:512–519

    Article  PubMed  Google Scholar 

  48. Vanderhoof JA (2000) Probiotics and intestinal inflammatory disorders in infants and children. J Pediatr Gastroenterol Nutr 30(Suppl):34–38

    Article  Google Scholar 

  49. Guérin-Danan C, Popot AF, Vaissade CP, Gaudichon C, Pedone C, Bouley C, Szylit O (1997) Pattern of metabolism and composition of the fecal microbiota in infants 10 to 18 months old from day care centers. J Pediatr Gastroenterol Nutr 25:281–289

    Article  PubMed  Google Scholar 

  50. Vanderhoof JA, Young RJ (2002) Probiotics in pediatrics. Pediatrics 109:956–958

    Article  PubMed  Google Scholar 

  51. Hooper LV, Wong MH, Thelin A, Hansson L, Falk PG, Gordon JI (2001) Molecular analysis of commensal host-microbial relationships in the intestine. Science 291:881–884

    Article  PubMed  CAS  Google Scholar 

  52. Saavedra JM (1995) Microbes to fight microbes: a not so novel approach to controlling diarrheal disease. J Pediatr Gastroenterol Nutr 21:125–129

    Article  PubMed  CAS  Google Scholar 

  53. Vandenplas Y (2004) Clinical overview: the changing pattern of clinical aspects of allergy diseases. Nestlé Nutr Workshop 53:1–25

    Google Scholar 

  54. Smit JJ, Folkerts G, Nijkamp FP (2004) Mycobacteria, genes and the hygiene hypothesis. Curr Opin Allergy Clin Immunol 4:57–62

    Article  PubMed  Google Scholar 

  55. Rautava S, Ruuskanen O, Ouwehand A, Salminen S, Isolauri E (2004) The hygiene hypothesis of atopic disease—an extended version. J Pediatr Gastroenterol Nutr 38:378–388

    Article  PubMed  Google Scholar 

  56. Kalliomaki M, Kirjavainen P, Eerola E, Kero P, Salminen S, Isolauri E (2001) Distinct patterns of neonatal gut microbiota in infants in whom atopy was and was not developing. J Allergy Clin Immunol 107:129–134

    Article  PubMed  CAS  Google Scholar 

  57. Bjorksten B, Naaber P, Sepp E, Mikelsaar M (1999) The intestinal microbiota in allergic Estonian and Swedish 2-year-old children. Clin Exp Allergy 29:342–346

    Article  PubMed  CAS  Google Scholar 

  58. He F, Ouwehan A, Isolauri E, Hashimoto H, Benno Y, Salminen S (2001) Comparison of mucosal adhesion and species identification of bifidobacteria isolated from healthy and allergic infants. FEMS Immunol Med Microbiol 30:43–47

    Article  PubMed  CAS  Google Scholar 

  59. Schultz M, Scholmerich J, Rath HC (2003) Rationale for probiotic and antibiotic treatment strategies in inflammatory bowel diseases. Dig Dis Sci 21:105–128

    Article  Google Scholar 

  60. Swidsinski A, Ladhoff A, Pernthaler A, Swidsinski S, Loening-Baucke V, Ortner M, Weber J, Hoffmann U, Schreiber S, Dietel M, Lochs H (2002) Mucosal microbiota in inflammatory bowel disease. Gastroenterology 122:44–54

    Article  PubMed  Google Scholar 

  61. Thompson-Chagoyán OC, Maldonado J, Gil A (2005) Aetiology of inflammatory bowel disease (IBD): role of intestinal microbiota and gut-associated lymphoid tissue immune response. Clin Nutr 24:339–352

    Article  PubMed  CAS  Google Scholar 

  62. Kennedy RJ, Kirk SJ, Gardiner KR (2000) Promotion for a favorable gut microbiota in inflammatory bowel disease. J Parent Ent Nutr 24:189–195

    Article  CAS  Google Scholar 

  63. Borruel N, Carol M, Casellas F, Antolin M, de Lara F, Espin E, Naval J, Guarner F, Malagelada JR (2002) Increased mucosal TNF-α production in Crohn's disease can be modulated in vitro by probiotic bacteria. Gut 5:659–664

    Article  Google Scholar 

  64. Steidler L (2001) Microbiological and immunological strategies for treatment of inflammatory bowel disease. Microbes Infect 3:1157–1166

    Article  PubMed  CAS  Google Scholar 

  65. Keighley MR. Arabi Y, Dimock F Burdon DW, Allan RN, Alexander-Williams J (1978) Influence of inflammatory bowel disease on intestinal microbiota. Gut 19:1099–1104

    PubMed  CAS  Google Scholar 

  66. Schultsz C Van Den Berg FM, Ten Kate FW, Tytgat GN, Dankert J (1999) The intestinal mucus layer from patients with inflammatory bowel disease harbors high numbers of bacteria compared with controls. Gastroenterology 117:1089–1097

    Article  PubMed  CAS  Google Scholar 

  67. Hooper LV, Midvedt T, Gordon JI (2002) How host microbial interactions shape the nutrient environment of mammalian intestine. Annu Rev Nutr 22:283–307

    Article  PubMed  CAS  Google Scholar 

  68. Backhed F, Ding H, Wang T, Hooper LV, Koh GY, Nagy A, Semenkovich CF, Gordon JI (2004) The gut microbiota as an environmental factor that regulates fat storage. Proc Natl Acad Sci USA 101:15718–15723

    Article  PubMed  CAS  Google Scholar 

  69. Backhed F, Ley RE, Sonnenburg JL, Peterson DA, Gordon JI (2005) Host-bacterial mutualism in the human intestine. Science 307:1915–1920

    Article  PubMed  CAS  Google Scholar 

  70. Bingham SA (1999) High meat diets and cancer risk. Proc Nutr Soc 58:243–248

    PubMed  CAS  Google Scholar 

  71. Rafter J, Glinghammar B (1998) Interactions between the environment and genes in the colon. Eur J Cancer Prev 7(Suppl):69–74

    Article  Google Scholar 

  72. Midtvedt T (1987) Intestinal bacteria and rheumatic disease. Scand J Rheumatol Suppl 64:49–54

    PubMed  CAS  Google Scholar 

  73. Toivanen P (2003) Normal intestinal microbiota in the aetiopathogenesis of rheumatoid arthritis. Ann Rheum Dis 62:807–811

    Article  PubMed  CAS  Google Scholar 

  74. Granfors K, Jalkanen S, von Essen R, Lahesmaa-Rantala R, Isomaki O, Pekkola-Heino K, Merilahti-Palo R, Saario R, Isomaki H, Toivanen A (1989) Yersinia antigens in synovial-fluid cells from patients with reactive arthritis. N Engl J Med 320:216–221

    Article  PubMed  CAS  Google Scholar 

  75. Granfors K, Jalkanen S, Lindberg AA, Mäki-Ikola O, von Essen R, Lahesmaa-Rantala R, Isomaki H, Saario R, Arnold WJ, Toivanen A (1990) Salmonella lipopolysaccharide in synovial cells from patients with reactive arthritis. Lancet 335:685–688

    Article  PubMed  CAS  Google Scholar 

  76. Kjeldsen-Kragh J (1999) Rheumatoid arthritis treated with vegetarian diets. Am J Clin Nutr 70(Suppl):594–600

    Google Scholar 

  77. Eerola E, Mottonen T, Hannonen P, Luukkainen R, Kantola I, Vuori K, Tuominen J, Toivanen P (1994) Intestinal microbiota in early rheumatoid arthritis. Br J Rheumatol 33:1030–1038

    Article  PubMed  CAS  Google Scholar 

  78. Grönlund MM, Lehtonen Op, Eerola E, Kero P (1999) Fecal microflora in healthy infants born by different methods of delivery: permanent changes in intestinal microbiota after caesarean delivery. J Pediatr Gastroenterol Nutr 28:19–25

    Article  PubMed  Google Scholar 

  79. Bailey MT, Coe CL (1999) Maternal separation disrupts the integrity of the intestinal microbiota in infant rhesus monkeys. Dev Psychobiol 35:146–155

    Article  PubMed  CAS  Google Scholar 

  80. Hawrelak JA, Myers SP (2004) The causes of intestinal dysbiosis: a review. Altern Med Rev 9:180–197

    PubMed  Google Scholar 

  81. Holdeman LV, Good IJ, Moore WE (1976) Human fecal microbiota: variation in bacterial composition within individuals and a possible effect of emotional stress. Appl Environ Microbiol 31:359–375

    PubMed  CAS  Google Scholar 

  82. Lyte M, Ernst S (1992) Catecholamine induced growth of Gram negative bacteria. Life Sci 50:203–212

    Article  PubMed  CAS  Google Scholar 

  83. Lyte M, Frank CD, Green BT (1996) Production of autoinducer of growth by norepinephrine cultured Escherichia coli 0157:H7. FEMS Microbiol Lett 139:155–159

    PubMed  CAS  Google Scholar 

  84. Freestone PP, Haigh RD, Williams PH, Lyte M (1999) Stimulation of bacterial growth by heat-stable, norepinephrine-induced autoinducers. FEMS Microbiol Lett 172:53–60

    Article  PubMed  CAS  Google Scholar 

  85. Dendukuri N, Costa V, McGregor M, Brophy JM (2005) Probiotic therapy for the prevention and treatment of Clostridium difficile-associated diarrhea: a systematic review. CMAJ 173:167–170

    PubMed  Google Scholar 

  86. Surawicz CM (2005) Antibiotic-associated diarrhea and pseudomembranous colitis: are they less common with poorly absorbed antimicrobials. Chemotherapy 51(Suppl 1):81–89

    Article  PubMed  CAS  Google Scholar 

  87. Poutanen SM, Simor AE (2004) Clostridium difficile-associated diarrhea in adults. CMAJ 171:51–58

    PubMed  Google Scholar 

  88. Muto CA, Pokrywka M, Shutt K, Mendelsohn AB, Nouri K, Posey K, Roberts T, Croyle K, Krystofiak S, Patel-Brown S, Pasculle AW, Paterson DL, Saul M, Harrison LH (2005) A large outbreak of Clostridium difficile-associated disease with an unexpected proportion of deaths and colectomies at a teaching hospital following increased fluoroquinolone use. Infect Control Hosp Epidemiol 26:273–280

    Article  PubMed  Google Scholar 

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Acknowledgments

Oscar C. Thompson-Chagoyán is the recipient of a Mexican Institute of Social Security fellowship. This study was part of the Commission of the European Communities funded project QLRT-2002 02606. Effects of diet and lifestyle on risk of gastrointestinal infections and allergy in early life; consumer knowledge, attitudes and needs (INFABIO). It does not necessarily reflect the Commission's views and in no way anticipates the Commission's future policy in this area.

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Thompson-Chagoyán, O.C., Maldonado, J. & Gil, A. Colonization and Impact of Disease and Other Factors on Intestinal Microbiota. Dig Dis Sci 52, 2069–2077 (2007). https://doi.org/10.1007/s10620-006-9285-z

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