European Journal of Nutrition

, Volume 52, Issue 6, pp 1669–1677 | Cite as

Comparative in vitro inhibition of urinary tract pathogens by single- and multi-strain probiotics

  • C. M. C. ChapmanEmail author
  • G. R. Gibson
  • S. Todd
  • I. Rowland
Original Contribution



Multi-species probiotic preparations have been suggested as having a wide spectrum of application, although few studies have compared their efficacy with that of individual component strains at equal concentrations. We therefore tested the ability of 4 single probiotics and 4 probiotic mixtures to inhibit the urinary tract pathogens Escherichia coli NCTC 9001 and Enterococcus faecalis NCTC 00775.


We used an agar spot test to test the ability of viable cells to inhibit pathogens, while a broth inhibition assay was used to assess inhibition by cell-free probiotic supernatants in both pH-neutralised and non-neutralised forms.


In the agar spot test, all probiotic treatments showed inhibition, L. acidophilus was the most inhibitory single strain against E. faecalis, L. fermentum the most inhibitory against E. coli. A commercially available mixture of 14 strains (Bio-Kult®) was the most effective mixture, against E. faecalis, the 3-lactobacillus mixture the most inhibitory against E. coli. Mixtures were not significantly more inhibitory than single strains. In the broth inhibition assays, all probiotic supernatants inhibited both pathogens when pH was not controlled, with only 2 treatments causing inhibition at a neutral pH.


Both viable cells of probiotics and supernatants of probiotic cultures were able to inhibit growth of two urinary tract pathogens. Probiotic mixtures prevented the growth of urinary tract pathogens but were not significantly more inhibitory than single strains. Probiotics appear to produce metabolites that are inhibitory towards urinary tract pathogens. Probiotics display potential to reduce the incidence of urinary tract infections via inhibition of colonisation.


Probiotic Multi-species Urinary Pathogen 



This work forms part of a PhD project funded by Probiotics International, Somerset, UK. Probiotics International had no role in the preparation of the article, study design, data collection, analysis, interpretation, or report writing.


  1. 1.
    Joint FAO/WHO Expert Consultation on evaluation of health and nutritional properties of probiotics in food including powder milk with live lactic acid bacteria (2001) Health and nutritional properties of probiotics in food including powder milk with live lactic acid bacteria. Food and Agriculture Organization of the United Nations, World Health OrganizationGoogle Scholar
  2. 2.
    Gotz V, Romankiewicz JA, Moss J, Murray HW (1979) Prophylaxis against ampicillin-associated diarrhea with a lactobacillus preparation. Am J Hosp Pharm 36(6):754–757Google Scholar
  3. 3.
    Winkler P, de Vrese M, Laue C, Schrezenmeir J (2005) 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 43(7):318–326Google Scholar
  4. 4.
    Sakamoto I, Igarashi M, Kimura K, Takagi A, Miwa T, Koga Y (2001) Suppressive effect of Lactobacillus gasseri OLL 2716 (LG21) on Helicobacter pylori infection in humans. J Antimicrob Chemother 47(5):709–710CrossRefGoogle Scholar
  5. 5.
    Rosenfeldt V, Benfeldt E, Nielsen SD, Michaelsen KF, Jeppesen DL, Valerius NH, Paerregaard A (2003) Effect of probiotic Lactobacillus strains in children with atopic dermatitis. J Allergy Clin Immunol 111(2):389–395CrossRefGoogle Scholar
  6. 6.
    Viljanen M, Savilahti E, Haahtela T, Juntunen-Backman K, Korpela R, Poussa T, Tuure T, Kuitunen M (2005) Probiotics in the treatment of atopic eczema/dermatitis syndrome in infants: a double-blind placebo-controlled trial. Allergy 60(4):494–500CrossRefGoogle Scholar
  7. 7.
    Bibiloni R, Fedorak RN, Tannock GW, Madsen KL, Gionchetti P, Campieri M, De Simone C, Sartor RB (2005) VSL#3 probiotic-mixture induces remission in patients with active ulcerative colitis. Am J Gastroenterol 100(7):1539–1546CrossRefGoogle Scholar
  8. 8.
    Venturi A, Gionchetti P, Rizzello F, Johansson R, Zucconi E, Brigidi P, Matteuzzi D, Campieri M (1999) Impact on the composition of the faecal flora by a new probiotic preparation: preliminary data on maintenance treatment of patients with ulcerative colitis. Aliment Pharmacol Ther 13(8):1103–1108CrossRefGoogle Scholar
  9. 9.
    Rowland I, Capurso L, Collins K, Cummings J, Delzenne N, Goulet O, Guarner F, Marteau P, Meier R (2010) Current level of consensus on probiotic science–report of an expert meeting–London, 23 November 2009. Gut Microbes 1(6):436–439CrossRefGoogle Scholar
  10. 10.
    Gibson GR, McCartney AL, Rastall RA (2005) Prebiotics and resistance to gastrointestinal infections. Br J Nutr 93(Suppl 1):S31–S34CrossRefGoogle Scholar
  11. 11.
    Tejero-Sarinena S, Barlow J, Costabile A, Gibson GR, Rowland I (2012) In vitro evaluation of the antimicrobial activity of a range of probiotics against pathogens: evidence for the effects of organic acids. AnaerobeGoogle Scholar
  12. 12.
    Corr SC, Li Y, Riedel CU, O’Toole PW, Hill C, Gahan CG (2007) Bacteriocin production as a mechanism for the antiinfective activity of Lactobacillus salivarius UCC118. Proc Natl Acad Sci USA 104(18):7617–7621CrossRefGoogle Scholar
  13. 13.
    Warren JW, Abrutyn E, Hebel JR, Johnson JR, Schaeffer AJ, Stamm WE (1999) Guidelines for antimicrobial treatment of uncomplicated acute bacterial cystitis and acute pyelonephritis in women. Infectious Diseases Society of America (IDSA). Clin Infect Dis 29(4):745–758CrossRefGoogle Scholar
  14. 14.
    Salvatore S, Cattoni E, Siesto G, Serati M, Sorice P, Torella M (2011) Urinary tract infections in women. Eur J Obstet Gynecol Reprod Biol 156(2):131–136CrossRefGoogle Scholar
  15. 15.
    Reid G, Charbonneau D, Erb J, Kochanowski B, Beuerman D, Poehner R, Bruce AW (2003) Oral use of Lactobacillus rhamnosus GR-1 and L. fermentum RC-14 significantly alters vaginal flora: randomized, placebo-controlled trial in 64 healthy women. FEMS Immunol Med Microbiol 35(2):131–134CrossRefGoogle Scholar
  16. 16.
    Karlsson M, Scherbak N, Reid G, Jass J (2012) Lactobacillus rhamnosus GR-1 enhances NF-kappaB activation in Escherichia coli-stimulated urinary bladder cells through TLR4. BMC Microbiol 12(1):15CrossRefGoogle Scholar
  17. 17.
    Darouiche RO, Thornby JI, Cerra-Stewart C, Donovan WH, Hull RA (2005) Bacterial interference for prevention of urinary tract infection: a prospective, randomized, placebo-controlled, double-blind pilot trial. Clin Infect Dis 41(10):1531–1534CrossRefGoogle Scholar
  18. 18.
    Anukam KC, Osazuwa E, Osemene GI, Ehigiagbe F, Bruce AW, Reid G (2006) Clinical study comparing probiotic Lactobacillus GR-1 and RC-14 with metronidazole vaginal gel to treat symptomatic bacterial vaginosis. Microbes Infect 8(12–13):2772–2776CrossRefGoogle Scholar
  19. 19.
    Anukam K, Osazuwa E, Ahonkhai I, Ngwu M, Osemene G, Bruce AW, Reid G (2006) Augmentation of antimicrobial metronidazole therapy of bacterial vaginosis with oral probiotic Lactobacillus rhamnosus GR-1 and Lactobacillus reuteri RC-14: randomized, double-blind, placebo controlled trial. Microbes Infect 8(6):1450–1454CrossRefGoogle Scholar
  20. 20.
    Barrons R, Tassone D (2008) Use of Lactobacillus probiotics for bacterial genitourinary infections in women: a review. Clin Ther 30(3):453–468CrossRefGoogle Scholar
  21. 21.
    Burton JP, Cadieux PA, Reid G (2003) Improved understanding of the bacterial vaginal microbiota of women before and after probiotic instillation. Appl Environ Microbiol 69(1):97–101CrossRefGoogle Scholar
  22. 22.
    McLean NW, Rosenstein IJ (2000) Characterisation and selection of a Lactobacillus species to re-colonise the vagina of women with recurrent bacterial vaginosis. J Med Microbiol 49(6):543–552Google Scholar
  23. 23.
    Antonio MA, Rabe LK, Hillier SL (2005) Colonization of the rectum by Lactobacillus species and decreased risk of bacterial vaginosis. J Infect Dis 192(3):394–398CrossRefGoogle Scholar
  24. 24.
    Ipek IO, Bozaykut A, Arman DC, Sezer RG (2011) Antimicrobial resistance patterns of uropathogens among children in Istanbul, Turkey. Southeast Asian J Trop Med Public Health 42(2):355–362Google Scholar
  25. 25.
    Reid G, Bruce AW, Fraser N, Heinemann C, Owen J, Henning B (2001) Oral probiotics can resolve urogenital infections. FEMS Immunol Med Microbiol 30(1):49–52CrossRefGoogle Scholar
  26. 26.
    Reid G, Bruce AW (2001) Selection of lactobacillus strains for urogenital probiotic applications. J Infect Dis 183(Suppl 1):S77–S80CrossRefGoogle Scholar
  27. 27.
    Reid G (1999) The scientific basis for probiotic strains of Lactobacillus. Appl Environ Microbiol 65(9):3763–3766Google Scholar
  28. 28.
    Reid G, Beuerman D, Heinemann C, Bruce AW (2001) Probiotic Lactobacillus dose required to restore and maintain a normal vaginal flora. FEMS Immunol Med Microbiol 32(1):37–41CrossRefGoogle Scholar
  29. 29.
    Chapman CM, Gibson GR, Rowland I (2012) In vitro evaluation of single- and multi-strain probiotics: inter-species inhibition between probiotic strains, and inhibition of pathogens. Anaerobe 18(4):405–413CrossRefGoogle Scholar
  30. 30.
    Chapman CM, Gibson GR, Rowland I (2011) Health benefits of probiotics: are mixtures more effective than single strains? Eur J Nutr 50(1):1–17CrossRefGoogle Scholar
  31. 31.
    Shuler M, Kargi F (2005) Bioprocess engineering basic concepts, 2nd edn. Pearson Education, SingaporeGoogle Scholar
  32. 32.
    Barbosa TM, Serra CR, La Ragione RM, Woodward MJ, Henriques AO (2005) Screening for bacillus isolates in the broiler gastrointestinal tract. Appl Environ Microbiol 71(2):968–978CrossRefGoogle Scholar
  33. 33.
    Hassan M, Kjos M, Nes IF, Diep DB, Lotfipour F (2012) Natural antimicrobial peptides from bacteria: characteristics and potential applications to fight against antibiotic resistance. J Appl Microbiol 113(4):723–736CrossRefGoogle Scholar
  34. 34.
    Fitzgerald MP, Stablein U, Brubaker L (2002) Urinary habits among asymptomatic women. Am J Obstet Gynecol 187(5):1384–1388CrossRefGoogle Scholar
  35. 35.
    Cadieux PA, Burton J, Devillard E, Reid G (2009) Lactobacillus by-products inhibit the growth and virulence of uropathogenic Escherichia coli. J Physiol Pharmacol 60(Suppl 6):13–18Google Scholar
  36. 36.
    Hall JE (2010) Textbook of medical physiology, 12 edn. Saunders, PhiladelphiaGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • C. M. C. Chapman
    • 1
    Email author
  • G. R. Gibson
    • 1
  • S. Todd
    • 2
  • I. Rowland
    • 1
  1. 1.Department of Food and Nutritional SciencesUniversity of ReadingWhiteknights, ReadingUK
  2. 2.Department of Mathematics and StatisticsUniversity of ReadingWhiteknights, ReadingUK

Personalised recommendations