International Journal of Antimicrobial Agents
Volume 34, Issue 3 , Pages 197.e1-197.e10 , September 2009

Probiotics for the prevention of respiratory tract infections: a systematic review

  • Evridiki K. Vouloumanou

      Affiliations

    • Alfa Institute of Biomedical Sciences (AIBS), 9 Neapoleos Street, 151 23 Marousi, Athens, Greece
  • ,
  • Gregory C. Makris

      Affiliations

    • Alfa Institute of Biomedical Sciences (AIBS), 9 Neapoleos Street, 151 23 Marousi, Athens, Greece
  • ,
  • Drosos E. Karageorgopoulos

      Affiliations

    • Alfa Institute of Biomedical Sciences (AIBS), 9 Neapoleos Street, 151 23 Marousi, Athens, Greece
  • ,
  • Matthew E. Falagas

      Affiliations

    • Alfa Institute of Biomedical Sciences (AIBS), 9 Neapoleos Street, 151 23 Marousi, Athens, Greece
    • Department of Medicine, Henry Dunant Hospital, Athens, Greece
    • Department of Medicine, Tufts University School of Medicine, Boston, MA, USA
    • Corresponding Author InformationCorresponding author. Tel.: +30 694 61 10 000; fax: +30 210 68 39 605.

Received 3 November 2008 ,Accepted 4 November 2008.

References 

  1. Low D. Reducing antibiotic use in influenza: challenges and rewards. Clin Microbiol Infect. 2008;14:298–306
  2. Panasiuk L, Lukas W, Paprzycki P. Empirical first-line antibioticotherapy in adult rural patients with acute respiratory tract infections. Ann Agric Environ Med. 2007;14:305–311
  3. Snow V, Mottur-Pilson C, Gonzales R. Principles of appropriate antibiotic use for treatment of nonspecific upper respiratory tract infections in adults. Ann Intern Med. 2001;134:487–489
  4. Reid G, Jass J, Sebulsky MT, McCormick JK. Potential uses of probiotics in clinical practice. Clin Microbiol Rev. 2003;16:658–672
  5. Falagas ME, Betsi GI, Athanasiou S. Probiotics for prevention of recurrent vulvovaginal candidiasis: a review. J Antimicrob Chemother. 2006;58:266–272
  6. Falagas ME, Betsi GI, Athanasiou S. Probiotics for the treatment of women with bacterial vaginosis. Clin Microbiol Infect. 2007;13:657–664
  7. Falagas ME, Betsi GI, 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;66:1253–1261
  8. Hammerman C, Kaplan M. Probiotics and neonatal intestinal infection. Curr Opin Infect Dis. 2006;19:277–282
  9. Lara-Villoslada F, Sierra S, Boza J, Xaus J, Olivares M. Beneficial effects of consumption of a dairy product containing two probiotic strains. Lactobacillus coryniformis CECT5711 and Lactobacillus gasseri CECT5714 in healthy children. Nutr Hosp. 2007;22:496–502[in Spanish]
  10. Pant N, Marcotte H, Brussow H, Svensson L, Hammarstrom L. Effective prophylaxis against rotavirus diarrhea using a combination of Lactobacillus rhamnosus GG and antibodies. BMC Microbiol. 2007;7:86
  11. Perdigon G, Alvarez S, Pesce de Ruiz Holgado A. Immunoadjuvant activity of oral Lactobacillus casei: influence of dose on the secretory immune response and protective capacity in intestinal infections. J Dairy Res. 1991;58:485–496
  12. Pochapin M. The effect of probiotics on Clostridium difficile diarrhea. Am J Gastroenterol. 2000;95:S11–S13
  13. Szymanski H, Pejcz J, Jawien M, Chmielarczyk A, Strus M, Heczko PB. Treatment of acute infectious diarrhoea in infants and children with a mixture of three Lactobacillus rhamnosus strains – a randomized, double-blind, placebo-controlled trial. Aliment Pharmacol Ther. 2006;23:247–253
  14. Aso Y, Akaza H, Kotake T, Tsukamoto T, Imai K, Naito S The BLP Study Group. Preventive effect of a Lactobacillus casei preparation on the recurrence of superficial bladder cancer in a double-blind trial. Eur Urol. 1995;27:104–109
  15. Benchimol EI, Mack DR. Probiotics in relapsing and chronic diarrhea. J Pediatr Hematol Oncol. 2004;26:515–517
  16. de Moreno de LeBlanc A, Matar C, Perdigon G. The application of probiotics in cancer. Br J Nutr. 2007;98:S105–S110
  17. de Moreno de LeBlanc A, Matar C, Theriault C, Perdigon G. Effects of milk fermented by Lactobacillus helveticus R389 on immune cells associated to mammary glands in normal and a breast cancer model. Immunobiology. 2005;210:349–358
  18. Geier MS, Butler RN, Howarth GS. Probiotics, prebiotics and synbiotics: a role in chemoprevention for colorectal cancer?. Cancer Biol Ther. 2006;5:1265–1269
  19. Gruber C, Wendt M, Sulser C, Lau S, Kulig M, Wahn U, et al. Randomized, placebo-controlled trial of Lactobacillus rhamnosus GG as treatment of atopic dermatitis in infancy. Allergy. 2007;62:1270–1276
  20. Kligler B, Hanaway P, Cohrssen A. Probiotics in children. Pediatr Clin North Am. 2007;54:949–967
  21. Lee NK, Park JS, Park E, Paik HD. Adherence and anticarcinogenic effects of Bacillus polyfermenticus SCD in the large intestine. Lett Appl Microbiol. 2007;44:274–278
  22. Delia P, Sansotta G, Donato V, Frosina P, Messina G, De Renzis C, et al. Use of probiotics for prevention of radiation-induced diarrhea. World J Gastroenterol. 2007;13:912–915
  23. Cangemi de Gutierrez R, Santos V, Nader-Macias ME. Protective effect of intranasally inoculated Lactobacillus fermentum against Streptococcus pneumoniae challenge on the mouse respiratory tract. FEMS Immunol Med Microbiol. 2001;31:187–195
  24. Grangette C, Muller-Alouf H, Goudercourt D, Geoffroy MC, Turneer M, Mercenier A. Mucosal immune responses and protection against tetanus toxin after intranasal immunization with recombinant Lactobacillus plantarum. Infect Immun. 2001;69:1547–1553
  25. Racedo S, Villena J, Medina M, Aguero G, Rodriguez V, Alvarez S. Lactobacillus casei administration reduces lung injuries in a Streptococcus pneumoniae infection in mice. Microbes Infect. 2006;8:2359–2366
  26. Villena J, Racedo S, Aguero G, Bru E, Medina M, Alvarez S. Lactobacillus casei improves resistance to pneumococcal respiratory infection in malnourished mice. J Nutr. 2005;135:1462–1469
  27. Yasui H, Kiyoshima J, Hori T. Reduction of influenza virus titer and protection against influenza virus infection in infant mice fed Lactobacillus casei Shirota. Clin Diagn Lab Immunol. 2004;11:675–679
  28. Yasui H, Kiyoshima J, Hori T, Shida K. Protection against influenza virus infection of mice fed Bifidobacterium breve YIT4064. Clin Diagn Lab Immunol. 1999;6:186–192
  29. Yasui H, Shida K, Matsuzaki T, Yokokura T. Immunomodulatory function of lactic acid bacteria. Antonie Van Leeuwenhoek. 1999;76:383–389
  30. Moher D, Jadad AR, Tugwell P. Assessing the quality of randomized controlled trials. Current issues and future directions. Int J Technol Assess Health Care. 1996;12:195–208
  31. Hatakka K, Blomgren K, Pohjavuori S, Kaijalainen T, Poussa T, Leinonen M, et al. Treatment of acute otitis media with probiotics in otitis-prone children—a double-blind, placebo-controlled randomised study. Clin Nutr. 2007;26:314–321
  32. Kekkonen RA, Vasankari TJ, Vuorimaa T, Haahtela T, Julkunen I, Korpela R. The effect of probiotics on respiratory infections and gastrointestinal symptoms during training in marathon runners. Int J Sport Nutr Exerc Metab. 2007;17:352–363
  33. Puccio G, Cajozzo C, Meli F, Rochat F, Grathwohl D, Steenhout P. Clinical evaluation of a new starter formula for infants containing live Bifidobacterium longum BL999 and prebiotics. Nutrition. 2007;23:1–8
  34. Tiollier E, Chennaoui M, Gomez-Merino D, Drogou C, Filaire E, Guezennec CY. Effect of a probiotics supplementation on respiratory infections and immune and hormonal parameters during intense military training. Mil Med. 2007;172:1006–1011
  35. Cobo Sanz JM, Mateos JA, Munoz Conejo A. Effect of Lactobacillus casei on the incidence of infectious conditions in children. Nutr Hosp. 2006;21:547–551[in Spanish]
  36. de Vrese M, Winkler P, Rautenberg P, Harder T, Noah C, Laue C, et al. Effect of Lactobacillus gasseri PA 16/8, Bifidobacterium longum SP 07/3, B. bifidum MF 20/5 on common cold episodes: a double blind, randomized, controlled trial. Clin Nutr. 2005;24:481–491
  37. Tubelius P, Stan V, Zachrisson A. Increasing work-place healthiness with the probiotic Lactobacillus reuteri: a randomised, double-blind placebo-controlled study. Environ Health. 2005;4:25
  38. Weizman Z, Asli G, Alsheikh A. Effect of a probiotic infant formula on infections in child care centers: comparison of two probiotic agents. Pediatrics. 2005;115:5–9
  39. Winkler P, de Vrese M, Laue C, Schrezenmeir J. Effect of a dietary supplement containing probiotic bacteria plus vitamins and minerals on common cold infections and cellular immune parameters. Int J Clin Pharmacol Ther. 2005;43:318–326
  40. Schrezenmeir J, Heller K, McCue M, Llamas C, Lam W, Burow H, et al. Benefits of oral supplementation with and without synbiotics in young children with acute bacterial infections. Clin Pediatr (Phila). 2004;43:239–249
  41. Turchet P, Laurenzano M, Auboiron S, Antoine JM. Effect of fermented milk containing the probiotic Lactobacillus casei DN-114001 on winter infections in free-living elderly subjects: a randomised, controlled pilot study. J Nutr Health Aging. 2003;7:75–77
  42. Habermann W, Zimmermann K, Skarabis H, Kunze R, Rusch V. Reduction of acute recurrence in patients with chronic recurrent hypertrophic sinusitis by treatment with a bacterial immunostimulant (Enterococcus faecalis Bacteriae) of human origin. Arzneimittelforschung. 2002;52:622–627[in German]
  43. Rio ME, Zago Beatriz L, Garcia H, Winter L. The nutritional status changes the effectiveness of a dietary supplement of lactic bacteria on the emergence of respiratory tract diseases in children. Arch Latinoam Nutr. 2002;52:29–34[in Spanish]
  44. Hatakka K, Savilahti E, Ponka A, Meurman JH, Poussa T, Nase L, et al. Effect of long term consumption of probiotic milk on infections in children attending day care centres: double blind, randomised trial. BMJ. 2001;322:1327
  45. Cox AJ, Pyne DB, Saunders PU, Fricker PA. Oral administration of the probiotic Lactobacillus fermentum VRI-003 and mucosal immunity in endurance athletes. Br J Sports Med. 2008 Feb 13;[Epub ahead of print]
  46. Lodinova-Zadnikova R, Cukrowska B, Tlaskalova-Hogenova H. Oral administration of probiotic Escherichia coli after birth reduces frequency of allergies and repeated infections later in life (after 10 and 20 years). Int Arch Allergy Immunol. 2003;131:209–211
  47. Anukam K, Osazuwa E, Osadolor H, Bruce A, Reid G. Yogurt containing probiotic Lactobacillus rhamnosus GR-1 and L. reuteri RC-14 helps resolve moderate diarrhea and increases CD4 count in HIV/AIDS patients. J Clin Gastroenterol. 2008;42:239–243
  48. Colbere-Garapin F, Martin-Latil S, Blondel B, Mousson L, Pelletier I, Autret A, et al. Prevention and treatment of enteric viral infections: possible benefits of probiotic bacteria. Microbes Infect. 2007;9:1623–1631
  49. Jonkers D, Stockbrugger R. Review article: probiotics in gastrointestinal and liver diseases. Aliment Pharmacol Ther. 2007;26:133–148
  50. Lata J, Novotny I, Pribramska V, Jurankova J, Fric P, Kroupa R, et al. The effect of probiotics on gut flora, level of endotoxin and Child-Pugh score in cirrhotic patients: results of a double-blind randomized study. Eur J Gastroenterol Hepatol. 2007;19:1111–1113
  51. Park SK, Park DI, Choi JS, Kang MS, Park JH, Kim HJ, et al. The effect of probiotics on Helicobacter pylori eradication. Hepatogastroenterology. 2007;54:2032–2036
  52. Sanz Y, Nadal I, Sanchez E. Probiotics as drugs against human gastrointestinal infections. Recent Patents Anti-Infect Drug Disc 2007; 2:148–56.
  53. Betsi GI, Papadavid E, Falagas ME. Probiotics for the treatment or prevention of atopic dermatitis: a review of the evidence from randomized controlled trials. Am J Clin Dermatol. 2008;9:93–103
  54. Watkinson PJ, Barber VS, Dark P, Young JD. The use of pre-, pro- and synbiotics in adult intensive care unit patients: systematic review. Clin Nutr. 2007;26:182–192
  55. Jain PK, McNaught CE, Anderson ADG, MacFie J, Mitchell CJ. Influence of synbiotic containing Lactobacillus acidophilus La5, Bifidobacterium lactis Bb 12, Streptococcus thermophilus, Lactobacillus bulgaricus and oligofructose on gut barrier function and sepsis in critically ill patients: a randomised controlled trial. Clin Nutr. 2004;23:467–475
  56. Olah A, Belagyi T, Issekutz A, Gamal ME, Bengmark S. Randomized clinical trial of specific Lactobacillus and fibre supplement to early enteral nutrition in patients with acute pancreatitis. Br J Surg. 2002;89:1103–1107
  57. Besselink MGH, van Santvoort HC, Buskens E, Boermeester MA, van Goor H, Timmerman HM, et al. Probiotic prophylaxis in predicted severe acute pancreatitis: a randomised, double-blind, placebo-controlled trial. Lancet. 2008;371:651–659
  58. Naidu AS, Bidlack WR, Clemens RA. Probiotic spectra of lactic acid bacteria (LAB). Crit Rev Food Sci Nutr. 1999;39:13–126
  59. Silva M, Jacobus NV, Deneke C, Gorbach SL. Antimicrobial substance from a human Lactobacillus strain. Antimicrob Agents Chemother. 1987;31:1231–1233
  60. Strom K, Sjogren J, Broberg A, Schnurer J. Lactobacillus plantarum MiLAB 393 produces the antifungal cyclic dipeptides cyclo(L-Phe-L-Pro) and cyclo(L-Phe-trans-4-OH-L-Pro) and 3-phenyllactic acid. Appl Environ Microbiol. 2002;68:4322–4327
  61. Pothoulakis C, Kelly CP, Joshi MA, Gao N, O’Keane CJ, Castagliuolo I, et al. Saccharomyces boulardii inhibits Clostridium difficile toxin A binding and enterotoxicity in rat ileum. Gastroenterology. 1993;104:1108–1115
  62. Wilson KH, Perini F. Role of competition for nutrients in suppression of Clostridium difficile by the colonic microflora. Infect Immun. 1988;56:2610–2614
  63. Brook I. The role of bacterial interference in otitis, sinusitis and tonsillitis. Otolaryngol Head Neck Surg. 2005;133:139–146
  64. Collado MC, Jalonen L, Meriluoto J, Salminen S. Protection mechanism of probiotic combination against human pathogens: in vitro adhesion to human intestinal mucus. Asia Pac J Clin Nutr. 2006;15:570–575
  65. Collado MC, Meriluoto J, Salminen S. Role of commercial probiotic strains against human pathogen adhesion to intestinal mucus. Lett Appl Microbiol. 2007;45:454–460
  66. Ermolenko EI, Chernysh AI, Martsinkovskaia IV, Suvorov AN. Influence of probiotic enterococci on the growth of Streptococcus agalactiae. Zh Mikrobiol Epidemiol Immunobiol. 2007;5:73–77[in Russian]
  67. Lavermicocca P, Valerio F, Lonigro SL, Di Leo A, Visconti A. Antagonistic activity of potential probiotic lactobacilli against the ureolytic pathogen Yersinia enterocolitica. Curr Microbiol. 2008;56:175–181
  68. Reid G, Tieszer C, Lam D. Influence of lactobacilli on the adhesion of Staphylococcus aureus and Candida albicans to fibers and epithelial cells. J Ind Microbiol. 1995;15:248–253
  69. Rigothier MC, Maccario J, Gayral P. Inhibitory activity of Saccharomyces yeasts on the adhesion of Entamoeba histolytica trophozoites to human erythrocytes in vitro. Parasitol Res. 1994;80:10–15
  70. Sgouras D, Maragkoudakis P, Petraki K, Martinez-Gonzalez B, Eriotou E, Michopoulos S, et al. In vitro and in vivo inhibition of Helicobacter pylori by Lactobacillus casei strain Shirota. Appl Environ Microbiol. 2004;70:518–526
  71. Tagg JR, Dierksen KP. Bacterial replacement therapy: adapting ‘germ warfare’ to infection prevention. Trends Biotechnol. 2003;21:217–223
  72. Nanno M, Ohwaki M, Mutai M. Induction by Lactobacillus casei of increase in macrophage colony-forming cells and serum colony-stimulating activity in mice. Jpn J Cancer Res. 1986;77:703–710
  73. Perdigon G, de Macias ME, Alvarez S, Oliver G, de Ruiz Holgado AA. Effect of perorally administered lactobacilli on macrophage activation in mice. Infect Immun. 1986;53:404–410
  74. Cross ML. Microbes versus microbes: immune signals generated by probiotic lactobacilli and their role in protection against microbial pathogens. FEMS Immunol Med Microbiol. 2002;34:245–253
  75. Kaila M, Isolauri E, Soppi E, Virtanen E, Laine S, Arvilommi H. Enhancement of the circulating antibody secreting cell response in human diarrhea by a human Lactobacillus strain. Pediatr Res. 1992;32:141–144
  76. Majamaa H, Isolauri E, Saxelin M, Vesikari T. Lactic acid bacteria in the treatment of acute rotavirus gastroenteritis. J Pediatr Gastroenterol Nutr. 1995;20:333–338
  77. Miettinen M, Matikainen S, Vuopio-Varkila J, Pirhonen J, Varkila K, Kurimoto M, et al. Lactobacilli and streptococci induce interleukin-12 (IL-12), IL-18, and gamma interferon production in human peripheral blood mononuclear cells. Infect Immun. 1998;66:6058–6062
  78. Lenoir-Wijnkoop I, Sanders ME, Cabana MD, Caglar E, Corthier G, Rayes N, et al. Probiotic and prebiotic influence beyond the intestinal tract. Nutr Rev. 2007;65:469–489

PII: S0924-8579(08)00597-9

doi: 10.1016/j.ijantimicag.2008.11.005

International Journal of Antimicrobial Agents
Volume 34, Issue 3 , Pages 197.e1-197.e10 , September 2009