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Probiotics in clinical conditions

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Abstract

Probiotics are nonpathogenic microorganisms which, when ingested, exert a positive influence on the health or physiology of the host. Their mechanisms of action and effects are now studied using the same pharmacological approach as for drugs. This article summarizes and comments on evidence for the positive effects of probiotics in various clinical situations. Substantial evidence can be achieved when randomized controlled trials or meta-analyses show positive results. The clinical situations studied include prevention or treatment of antibiotic-associated disorders, gastroenteritis, and diarrhea, lactose intolerance, intestinal infections and colonization by pathogenic bacteria (including Helicobacter pylori and Clostridium difficile), traveler's diarrhea, irritable bowel syndrome (IBS), inflammatory bowel disease (IBD), colonic cancer, urogenital infections and tumors, allergy (especially atopic eczema), vaccination, and cholesterol lowering. Current probiotics have an excellent safety record—another topic discussed in this article.

Probiotics can be defined as nonpathogenic microorganisms which, when ingested, exert a positive influence on host health or physiology (1). They consist of either bacteria, especially lactic-acid bacteria (LAB), or yeast (Saccharomyces), and are increasingly used in foods—especially fermented milks—and pharmaceutical products. Physicians have long been skeptical about their “real” efficacy (2,3), and have raised three basic questions: are probiotic products stable, do they survive in the gastrointestinal tract, and what is the level of evidence for their efficacy? A pharmacological approach was used to assess the positive effects and potential side effects of the products as well as their pharmacokinetics (2,4). The level of evidence for efficacy can be assessed with the rules of evidence-based medicine. We now know that the stability of many products (but not all) is good (5), that many strains (but not all) survive in the gastrointestinal tract (4), and that many double-blind randomized controlled trials (RCT) reported that some probiotics were more efficient than a placebo or a control treatment in specific clinical situations. The effects can be direct or indirect through modulation of the endogenous flora or of the immune system (2). Some effects have clearly been demonstrated, and the level of evidence is still lower for other effects. The article summarizes the present knowledge on the clinical applications of probiotics in humans.

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References

  1. Fuller, R. (1989). J. Appl. Bacteriol. 66,365–378.

    PubMed  CAS  Google Scholar 

  2. Marteau, P., Pochart, P., Bouhnik, Y., and Rambaud, J. C. (1993). World Rev. Nutr. Diet 74,1–21.

    PubMed  CAS  Google Scholar 

  3. Dunne, C., Murphy, L, Flynn, S., O'Mahony, L, O'Halloran, S., Feeney, M., et al. (1999). Antonie Leeuwenhoek 76,279–292.

    PubMed  CAS  Google Scholar 

  4. Marteau, P. and Vesa, T. (1998). Bioscience Microflora 17,1–6.

    Google Scholar 

  5. Canganella, F., Paganini, S., Ovidi, M., Vettraino, A.M., Bevilacqua, L., Massa, S., et al. (1997). Microbiol. Res. 152,171–179.

    PubMed  CAS  Google Scholar 

  6. Adam, J., Banet, A., and Banet-Bellet, C. (1977). Gaz. Méd. Fr. 84,2072–2078.

    Google Scholar 

  7. Surawicz, C.M., Elmer, G.W., Speelman, P., McFarland, L.V., Chinn, J., and van Belle, G. (1989). Gastroenterology 96, 981–988.

    PubMed  CAS  Google Scholar 

  8. McFarland, L.V., Surawicz, C.M., Greenberg, R.N., Elmer, G.W., Moyer, K.A., and Melcher, S.A. (1995). Am. J. Gastroenterol. 90,439–448.

    PubMed  CAS  Google Scholar 

  9. Lewis, S.J., Potts, L.F., and Barry, R.E. (1998). J. Infect. 36,171–174.

    PubMed  CAS  Google Scholar 

  10. Ligny, G. (1975). Rev. Fr. Gastroentérologie 114,45–50.

    Google Scholar 

  11. Elmer, G.W., Surawicz, C.M., and McFarland, L.V. (1996). JAMA 275:870–876.

    PubMed  CAS  Google Scholar 

  12. Qamar, A., Aboudola, S., Warny, M., Michetti, P., Pothoulakis, C., LaMont, J.T., et al. (2001). Infect. Immun. 69,2762–2765.

    PubMed  CAS  Google Scholar 

  13. Vanderhoof, J.A., Whitney, D.B., Antonson, D.L., Hanner, T.L., Lupo, J.V., and Young, R.J. (1999). J. Pediatr. 135,564–568.

    PubMed  CAS  Google Scholar 

  14. Arvola, T., Laiho, K., Torkkeli, S., Mykkanen, H., Salminen, S., Maunula, L., et al. (1999). Pediatrics 104,e64.

    PubMed  CAS  Google Scholar 

  15. Borgia, M., Sepe, N., Brancato, V., and Borgia, R. (1982). Curr. Ther. Res. 31,265–271.

    Google Scholar 

  16. Wunderlich, P.F., Braun, L., Fumagalli, I., D'Apuzzo, V., Heim, F., Karly, M., et al. (1989). J. Int. Med. Res. 17,333–338.

    PubMed  CAS  Google Scholar 

  17. Gotz, V., Romankiewicz, J.A., Moss, J., and Murray, H.W. (1979). Am. J. Hosp. Pharm. 36,754–757.

    PubMed  CAS  Google Scholar 

  18. Clements, M.L., Levine, M.M., Ristiano, P.A., Daya, V.E., and Hughes, T.P. (1983). Prog. Food Nutr. Sci. 7,29–37.

    PubMed  CAS  Google Scholar 

  19. Witsell, D.L., Garrett, C.G., Yarbrough, W.G., Dorrestein, S.P., Drake, A.F., and Weissler, M.C. (1995). J. Otolaryngol. 24,230–233.

    PubMed  CAS  Google Scholar 

  20. Marteau, P. (1992). Ann. Gastroentérol. Hépatol. 28,181–184.

    CAS  Google Scholar 

  21. Isolauri, E., Juntunen, M., Rautanen, T., Sillanaukee, P., and Koivula, T. (1991). Pediatrics 88,90–97.

    PubMed  CAS  Google Scholar 

  22. Kaila, M., Isolauri, E., Soppi, E., Virtanen, E., Laine, S., and Arvilommi, H. (1992). Pediatr. Res. 32,141–144.

    PubMed  CAS  Google Scholar 

  23. Majamaa, H., Isolauri, E., Saxelin, M., and Vesikari, T. (1995). J. Pediatr. Gastroenterol. Nutr. 20,333–338.

    PubMed  CAS  Google Scholar 

  24. Isolauri, E., Kaila, M., Mykkanen, H., Ling, W.H., and Salminen, S. (1994). Dig. Dis. Sci. 39,2595–2600.

    PubMed  CAS  Google Scholar 

  25. Raza, S., Graham, S.M., Allen, S.J., Sultana, S., Cuevas, L., and Hart, C.A. (1995). Pediatr. Infect. Dis. J. 14,107–111.

    PubMed  CAS  Google Scholar 

  26. Pant, A.R., Graham, S.M., Allen, S.J., Harikul, S., Sabchareon, A., Cuevas, L., et al. (1996). J. Tropic. Pediatr. 42,162–165.

    CAS  Google Scholar 

  27. Guarino, A., Canani, R.B., Spagnuolo, M.I., Albano, F., and Di Benedetto, L. (1997). J. Pediatr. Gastroenterol. Nutr. 25,516–519.

    PubMed  CAS  Google Scholar 

  28. Shornikova, A.V., Isolauri, E., Burkanova, L., Lukovnikova, S., and Vesikari, T. (1997). Acta Paediatr. 86,460–465.

    PubMed  CAS  Google Scholar 

  29. Guandalini, S., Pensabene, L., Zikri, M.A., Dias, J.A., Casali, L.G., Hoekstra, H., et al. (2000). J. Ped. Gastroenterol. Nutr. 30,54–60.

    CAS  Google Scholar 

  30. Bellomo, G., Mangiagle, A., Nicastro, L., et al. (1980). Curr. Ther. Res. 28,927–936.

    Google Scholar 

  31. Camarri, E., Belvisi, A., Guidoni, G., Marini, G., and Frigerio, G. (1981). Chemotherapy 27,466–470.

    PubMed  CAS  Google Scholar 

  32. Buydens, P. and Debeuckelaere, S. (1996). Scand. J. Gastroenterol. 31,887–891.

    PubMed  CAS  Google Scholar 

  33. Chapoy, P. (1985). Ann. Pediatr. 32:1–3.

    Google Scholar 

  34. Sugita, T. and Togawa, M. (1994). Jap. J. Pediatry 47:2755–2762.

    Google Scholar 

  35. Shornikova, A.V., Casas, I.A., Mykkanen, H., Salo, E., and Vesikari, T. (1997). Pediatr. Infect. Dis. J. 16,1103–1107.

    PubMed  CAS  Google Scholar 

  36. Kaila, M., Isolauri, E., Saxelin, M., Arvilommi, H., and Vesikari, T. (1995). Arch. Dis. Child. 72,51–53.

    PubMed  CAS  Google Scholar 

  37. Bodilis, J.Y. (1983). Méd. Actu. 10,232–235.

    Google Scholar 

  38. Saavedra, J.M., Bauman, N.A., Oung, I., Perman, J.A., and Yolken, R.H. (1994). Lancet 344,1046–1049.

    PubMed  CAS  Google Scholar 

  39. Szajewska, H., Kotowska, M., Mrukowicz, J.Z., Armanska, M., and Mikolajczyk, W. (2001). J. Pediatr. 138,361–365.

    PubMed  CAS  Google Scholar 

  40. Mastretta, E., Longo, P., Laccisaglia, A., Balbo, L., Russo, R., Muzzaccara, A., gianino, P. J. Verrdiate. Gastroentrol, Nutr., in press.

  41. Oberhelman, R.A., Gilman, R.H., Sheen, P., Taylor, D.N., Black, R.E., Cabrera, L., et al. (1999). J. Pediatr. 134,15–20.

    PubMed  CAS  Google Scholar 

  42. Marteau, P., Flourié, B., Pochart, P., Chastang, C., Desjeux, J.F., and Rambaud, J.C., Br. J. Nutr. 64,71–79.

  43. Marteau, P., Vesa, T., and Rambaud, J.C. (1997), Lactose maldigestion, in Probiotics, Fuller, R., ed., Chapman & Hall, pp. 65–88.

  44. Marteau, P., Messing, B., Arrigoni, E., Briet, F., Flourié, B., Morin, M.C., et al. (1997). Nutrition 13,13–16.

    PubMed  CAS  Google Scholar 

  45. Harms, H.K., Bertele-Harms, R.M., and Bruer-Kleis, D. (1987). N. Engl. J. Med. 316,1306–1309.

    PubMed  CAS  Google Scholar 

  46. Drouault, S., Juste, C., Marteau, P., Renault, P., and Corthier, G. (2001). Gastroenterology. 20,A3642.

    Google Scholar 

  47. Huber, J.T. (1997), Probiotics in cattle, in Probiotics, Fuller, R., ed., Chapman & Hall, London, pp. 162–185.

    Google Scholar 

  48. Mulder, R., Havenaar, R., and Huis in't Veld, J. (1997), Intervention strategies: the use of probiotics and competitive exclusion microfloras against contamination with pathogens in pigs and poultry, in Probiotics, Fuller, R., ed., Chapman & Hall, London, pp. 186–208.

    Google Scholar 

  49. McFarland, L.V., Surawicz, C.M., Greenberg, R.N., Fekety, R., Elmer, G.W., Moyer, K.A., et al. (1994). JAMA 271,1913–1918.

    PubMed  CAS  Google Scholar 

  50. Surawicz, C.M., McFarland, L.V., Greenberg, R.N., Rubin, M., Fekety, R., Mulligan, M.E., et al. (2000). Clin. Infect. Dis. 31,1012–1017.

    PubMed  CAS  Google Scholar 

  51. Coconnier, M.H., Lievin, V., Hemery, E., and Servin, A.L. (1998). Appl. Environ. Microbiol. 64,4573–4580.

    PubMed  CAS  Google Scholar 

  52. Michetti, P., Dorta, G., Wiesel, P.H., Brassart, D., Verdu, E., Herranz, M., et al. (1999). Digestion 60,203–209.

    PubMed  CAS  Google Scholar 

  53. Canducci, F., Armuzzi, A., Cremonini, F., Cammarota, G., Bartolozzi, F., Pola, P., et al. (2000). Alim. Pharmacol. Ther. 14,1625–1629.

    CAS  Google Scholar 

  54. Felley, C.P., Corthesy-Theulaz, I., Rivero, J.L., Sipponen, P., Kaufmann, M., Bauerfeind, P., et al. (2001). Eur. J. Gastroenteroly Hepatol. 13:25–29.

    CAS  Google Scholar 

  55. Armuzzi, A., Cremonini, F., Bartolozzi, F., Canducci, F., Candelli, M., Ojetti, V., et al. (2001). Aliment. Pharmacol. Ther. 15,163–169.

    PubMed  CAS  Google Scholar 

  56. DuPont, H.L. and the Practice Parameters Committee of the American College of Gastroenterology. (1997). Am. J. Gastroenterol. 92,1962–1975.

    PubMed  CAS  Google Scholar 

  57. Kollaritsch von, H., Holst, H, Grobara, P., and Wiedermann, G. (1993). Fortschr Med 111,153–156.

    Google Scholar 

  58. Oksanen, P.J., Salminen, S., Saxelin, M., Hamalainen, P., Ihantola-Vormisto, A., Muurasniemi-Isoviita, L., et al. (1990). Ann. Med. 22,53–56.

    PubMed  CAS  Google Scholar 

  59. Hilton, E., Kolakowski, P., Singer, C., and Smith, M. (1997). J. Travel Med. 4,41–43.

    PubMed  Google Scholar 

  60. Bouglé, D., Roland, N., Lebeurrier, F., and Arhan, P. (1999). Scand. J. Gastroenterol. 34,144–148.

    PubMed  Google Scholar 

  61. Marteau, P., Cuillerier, E., Gerhardt, M.F., Myara, A., Bouvier, M., Bouley, C., et al. (2001). Gastroenterol. Clin. Biol. 25,A122.

    Google Scholar 

  62. Maupas, J.L., Champemont, P., and Delforge, M. (1983), Méd. Chir. Dig. 12,77–79.

    Google Scholar 

  63. Halpern, G.M., Prindiville, T., Blanckenburg, M., Hsia, T., and Gerschwin, M.E. (1996). Am. J. Gastroenterol. 91,1579–1585.

    PubMed  CAS  Google Scholar 

  64. Hentschel, C., Bauer, J., Dill, N., et al. (1997). Gastroenterology 112,A146.

    Google Scholar 

  65. Tempé, J.D., Steidel, A.L., Bléhaut, H., Hasselmann, M., Lutun, P., and Maurier, F. (1983). Sem. Hôp Paris 59,1409–1412.

    PubMed  Google Scholar 

  66. Schlotterer, M., Bernasconi, P., Lebreton, F., and Wassermann, D. (1987). Nutr. Clin. Métab. 1:31–34.

    Google Scholar 

  67. Bleichner, G., Bléhaut, H., Mentec, H., and Moyse, D. (1997). Intensive Care Med. 23,517–523.

    PubMed  CAS  Google Scholar 

  68. Simenhoff, M.L., Dunn, S.R., Zollner, G.P., Fitzpatrick, M.E., Emery, S.M., and Sandine, W.E. (1996). Miner. Electrolyte Metab. 22,92–96.

    PubMed  CAS  Google Scholar 

  69. Vanderhoof, J.A., Young, R.J., Murray, N., and Kaufman, S.S. (1998). Gastroenterol. Nutr. 27,155–160.

    CAS  Google Scholar 

  70. Attar, A., Flourié, B., Rambaud, J.C, Franchisseur, C., Ruszniewski, P., and Bouhnik, Y. (1999). Gastroenterology 117,794–797.

    PubMed  CAS  Google Scholar 

  71. Salminen, E., Elomaa, I., Minkkinen, J., Vapaatalo, H., and Salminen, S. (1988). Clin. Radiol. 39,4357.

    Google Scholar 

  72. Shanahan, F. (2001). Gastroenterology 120,622–635.

    PubMed  CAS  Google Scholar 

  73. Marteau, P. and Shanahan, F. (2001), Role of antibiotics and probiotics in the management of inflammatory bowel disease, in Inflammatory Bowel Disease: From Bench to Bedside, 2nd ed., in press.

  74. Kruis, W., Schütz, E., Fric, P., Fixa, B., Judmaier, G., and Stolte, M. (1997). Aliment. Pharmacol. Ther. 11,853–858.

    PubMed  CAS  Google Scholar 

  75. Rembacken, B.J., Snelling, A.M., Hawkey, P.M., Chalmers, D.M., and Axon, A.T. (1999). Lancet 354,635–639.

    PubMed  CAS  Google Scholar 

  76. Malchow, H.A. (1997). J. Clin. Gastroenterol. 25,653–658.

    PubMed  CAS  Google Scholar 

  77. Gionchetti, P., Rizzello, F., Venturi, A., Brigidi, P., Matteuzzi, D., Bazzocchi, G., et al. (2000). Gastroenterology 119,305–309.

    PubMed  CAS  Google Scholar 

  78. Gionchetti, P., Rizzello, F., Venturi, A., Helwig, U., Amadini, C., Lammers, K.M., et al. Gastroenterology 118,G1214.

  79. Campieri, M., Rizzello, F., Venturi, A., et al. (2000). Gastroenterology 118,G4179.

    Google Scholar 

  80. Copaci, I., Micu, L., Chira, C., and Rovinaru, I. (2000). Gut 47(suppl III),A240-P929.

    Google Scholar 

  81. Guslandi, M., Mezzi, G., Sorghi, M., and Testoni, PA. (2000). Dig. Dis. Sci. 45,1462–1464.

    PubMed  CAS  Google Scholar 

  82. Ishikawa, H., Imaoka, A., Umesaki, Y., Tanaka, R., and Ohtani, T. (2000). Gastroenterology 118,A4171.

    Google Scholar 

  83. Ruseler van Embden, J.G.H., Schouten, W.R., and van Lieshout, L.M.C. (1994). Gut 35,658–664.

    PubMed  CAS  Google Scholar 

  84. Gionchetti, P., Orsla, O., Rizzello, F., Cifone, G., Benturi, A., D'Alo, S., et al. (1999). Gastroenterology 116,A723.

    Google Scholar 

  85. Plein, K. and Hotz, J. (1993). Z. Gastroenterol. 31,129–134.

    PubMed  CAS  Google Scholar 

  86. Hirayama, K. and Rafter, J. (2000). Microbes Infect. 2,681–686.

    PubMed  CAS  Google Scholar 

  87. Wollowski, I., Rechkemmer, G., and Pool-Zobel, B.L. (2001). Am. J. Clin. Nutr. 73(2 Suppl),451S-455S.

    PubMed  CAS  Google Scholar 

  88. Boutron, M.C., Faivre, J., Marteau, P., Couillault, C., Senesse, P., and Quipourt, V. (1996). Br. J. Cancer 74,145–151.

    PubMed  CAS  Google Scholar 

  89. Drutz, D.J. (1992). Ann. Intern. Med. 116,419–420.

    PubMed  CAS  Google Scholar 

  90. Reid, G., Bruce, A.W., Fraser, N., Heinemann, C., Owen, J., and Henning, B. (2001). FEMS Immunol. Med. Microbiol. 30,49–52.

    PubMed  CAS  Google Scholar 

  91. Reid, G. (2001). Am. J. Clin. Nutr. 73(2 Suppl),437S-443S.

    PubMed  CAS  Google Scholar 

  92. Hilton, E., Isenberg, H.D., Alperstein, P., France, and Borenstein, M.T. (1992). Ann. Intern. Med. 116,353–357.

    PubMed  CAS  Google Scholar 

  93. Hallen, A., Jarstrand, C., and Pahlson, C. (1992). Sex Transm. Dis. 19,146–148.

    PubMed  CAS  Google Scholar 

  94. Aso, Y. and Akazan, H. (1992). Urol. Int. 49,125–129.

    PubMed  CAS  Google Scholar 

  95. Aso, Y., Akaza, H., Kotake, T., Tsukamoto, T., Imai, K., Naito, S., and the BLP study group. (1995). Eur. Urol. 27,104–109.

    PubMed  CAS  Google Scholar 

  96. Isolauri, E., Arvola, T., Sutas, Y, Moilanen, E., and Salminen, S. (2000). Clin. Exp. Allergy 30,1604–1610.

    PubMed  CAS  Google Scholar 

  97. Kalliomaki, M., Salminen, S., Arvilommi, H., Kero, P., Koskinen, P., and Isolauri, E. (2001). Lancet 357,1076–1079.

    PubMed  CAS  Google Scholar 

  98. Murch, S. (2000). Curr. Opin. Gastroenterol. 16,552–557.

    PubMed  CAS  Google Scholar 

  99. Marteau, P. and Cellier, C. (1998), Immunological effects of biotherapeutic agents, in Biotherapeutic Agents, Humana Press, pp. 121–144.

  100. Link-Amster, H., Rochat, F., Saudan, K.Y., Saudan, K.Y., Mignot, O., and Aeschlimann, J.M. (1994). FEMS Immunol. Med. Microbiol. 10,55–64.

    PubMed  CAS  Google Scholar 

  101. Fang, H., Elina, T., Heikki, A., and Salminen, S.. FEMS Immunol. Med. Microbiol. 29,47–52.

  102. Isolauri, E., Joensuu, J., Suomalainen, H., Luomala, M., and Vesikari, T. (1995). Vaccine 13,310–312.

    PubMed  CAS  Google Scholar 

  103. Grangette, C., Muller-Alouf, H., Goudercourt, D., Geoffroy, M.C., Turneer, M., and Mercenier, A. (2001). Infect. Immun. 69,1547–1553.

    PubMed  CAS  Google Scholar 

  104. St-Onge, M.P., Farnworth, E.R., and Jones, P.J. (2000). Am. J. Clin. Nutr. 71,674–681.

    PubMed  CAS  Google Scholar 

  105. Klaver, F.A. and van der Meer, R.. Appl. Environ. Microbiol. 59,1120–1124.

  106. Marteau, P., Gerhardt, M.F., Myara, A., Bouvier, E., Trivin, F., and Rambaud, J.C. (1995). Microbiol. Ecol. Health Dis. 8,151–157.

    Google Scholar 

  107. Marteau, P. (2001). Scand. J. Nutr. 45,22–24.

    Google Scholar 

  108. Hennequin, C., Kauffmann-Lacroix, C., Jobert, A., Viard, J.P., Ricour, C., Jacquemin, J.L, et al. (2000). Eur. J. Clin. Microbiol. Infect. Dis. 19,16–20.

    PubMed  CAS  Google Scholar 

  109. Rautio, M., Jousimies-Somer, H., Kauma, H., Pietarinen, I., Saxelin, M., Tynkkynen, S., et al. (1999). Clin. Infect. Dis 28,1159–1160.

    PubMed  CAS  Google Scholar 

  110. MacKay, A., Taylor, M., Kibbler, C., and Hamilton Miller, J. (1999). Clin. Microbiol. Infect. 5,290–292.

    PubMed  Google Scholar 

  111. Saxelin, M., Chuang, N.H., Chassy, B., Rautelin, H., Mäkelä, P.H., Salminen, S., et al. (1996). Clin. Infect. Dis. 22,564–566.

    PubMed  CAS  Google Scholar 

  112. Saxelin, M., Rautelin, H., Salminen, S., and Mäkelä, P.H. (1996). Infect. Dis. Clin. Pract. 5,331–335.

    Google Scholar 

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Marteau, P.R. Probiotics in clinical conditions. Clinic Rev Allerg Immunol 22, 255–273 (2002). https://doi.org/10.1007/s12016-002-0011-0

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