Skip to main content

Advertisement

Log in

Biofilm formation and virulence of uropathogenic Escherichia coli in urine after consumption of cranberry-lingonberry juice

  • Article
  • Published:
European Journal of Clinical Microbiology & Infectious Diseases Aims and scope Submit manuscript

Abstract

Cranberry-lingonberry juice (CLJ) was effective in preventing urinary tract infections (UTIs) in our earlier randomized clinical trial. We aimed to test whether consumption of CLJ at a similar dose to earlier reduces the biofilm formation and virulence of uropathogenic Escherichia coli in urine. Twenty healthy women drank 100 ml of CLJ daily for two weeks. Urine samples were obtained 2–4 hours after the last dose. Control samples were taken after a one-week period without berry consumption. Biofilm formation of 20 E. coli strains was measured at 72 hours by the polystyrene microtitre plate method. Quantitative real-time PCR analyses were performed for selected genes. Four of the 20 clinical strains produced more biofilm in urine after CLJ consumption (P < 0.05) and one produced less. Expression levels of the pga, cpxA, fimA and papF genes did not differ between bacteria grown in control urine and urine obtained after CLJ consumption, except for pga gene expression, which was reduced in one strain after CLJ (P = 0.04). It appears that the effect of CLJ in preventing UTIs is not explained by mechanisms that reduce biofilm formation or the expression of selected virulence genes of Escherichia coli in urine.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Foxman B, Barlow R, D’Arcy H, Gillespie B, Sobel JD (2000) Urinary tract infection: self-reported incidence and associated costs. Ann Epidemiol 10:509–515

    Article  PubMed  CAS  Google Scholar 

  2. Ikäheimo R, Siitonen A, Heiskanen T, Karkkainen U, Kuosmanen P, Lipponen P, Makela PH (1996) Recurrence of urinary tract infection in a primary care setting: analysis of a 1-year follow-up of 179 women. Clin Infect Dis 22:91–99

    Article  PubMed  CAS  Google Scholar 

  3. Kontiokari T, Sundqvist K, Nuutinen M, Pokka T, Koskela M, Uhari M (2001) Randomised trial of cranberry-lingonberry juice and Lactobacillus GG drink for the prevention of urinary tract infections in women. BMJ 322:1571

    Article  PubMed  CAS  Google Scholar 

  4. Stothers L (2002) A randomized trial to evaluate effectiveness and cost effectiveness of naturopathic cranberry products as prophylaxis against urinary tract infection in women. Can J Urol 9:1558–1562

    PubMed  Google Scholar 

  5. Jepson RG, Craig JC (2008) Cranberries for preventing urinary tract infections. Cochrane Database Syst Rev CD001321

  6. Howell AB, Foxman B (2002) Cranberry juice and adhesion of antibiotic-resistant uropathogens. JAMA 287:3082–3083

    Article  PubMed  Google Scholar 

  7. Anderson GG, Palermo JJ, Schilling JD, Roth R, Heuser J, Hultgren SJ (2003) Intracellular bacterial biofilm-like pods in urinary tract infections. Science 301:105–107

    Article  PubMed  CAS  Google Scholar 

  8. Anderson M, Bollinger D, Hagler A, Hartwell H, Rivers B, Ward K, Steck TR (2004) Viable but nonculturable bacteria are present in mouse and human urine specimens. J Clin Microbiol 42:753–758

    Article  PubMed  Google Scholar 

  9. Naves P, del Prado G, Huelves L, Gracia M, Ruiz V, Blanco J, Dahbi G, Blanco M, Ponte MC, Soriano F (2008) Correlation between virulence factors and in vitro biofilm formation by Escherichia coli strains. Microb Pathog 45:86–91

    Article  PubMed  CAS  Google Scholar 

  10. Salo J, Sevander JJ, Tapiainen T, Ikäheimo I, Pokka T, Koskela M, Uhari M (2009) Biofilm formation by Escherichia coli isolated from patients with urinary tract infections. Clin Nephrol 71:501–507

    PubMed  CAS  Google Scholar 

  11. Johnson BJ, Lin B, Dinderman MA, Rubin RA, Malanoski AP, Ligler FS (2008) Impact of cranberry on Escherichia coli cellular surface characteristics. Biochem Biophys Res Commun 377:992–994

    Article  PubMed  CAS  Google Scholar 

  12. Itoh Y, Rice JD, Goller C, Pannuri A, Taylor J, Meisner J, Beveridge TJ, Preston JF III, Romeo T (2008) Roles of pgaABCD genes in synthesis, modification, and export of the Escherichia coli biofilm adhesin poly-beta-1,6-N-acetyl-D-glucosamine. J Bacteriol 190:3670–3680

    Article  PubMed  CAS  Google Scholar 

  13. Otto K, Silhavy TJ (2002) Surface sensing and adhesion of Escherichia coli controlled by the Cpx-signaling pathway. Proc Natl Acad Sci USA 99:2287–2292

    Article  PubMed  CAS  Google Scholar 

  14. Mulvey MA, Schilling JD, Martinez JJ, Hultgren SJ (2000) Bad bugs and beleaguered bladders: interplay between uropathogenic Escherichia coli and innate host defenses. Proc Natl Acad Sci USA 97:8829–8835

    Article  PubMed  CAS  Google Scholar 

  15. Mu XQ, Bullitt E (2006) Structure and assembly of P-pili: a protruding hinge region used for assembly of a bacterial adhesion filament. Proc Natl Acad Sci USA 103:9861–9866

    Article  PubMed  CAS  Google Scholar 

  16. Jaakola L, Pirttila AM, Vuosku J, Hohtola A (2004) Method based on electrophoresis and gel extraction for obtaining genomic DNA-free cDNA without DNase treatment. Biotechniques 37:744, 746, 748

    PubMed  CAS  Google Scholar 

  17. Goller C, Wang X, Itoh Y, Romeo T (2006) The cation-responsive protein NhaR of Escherichia coli activates pgaABCD transcription, required for production of the biofilm adhesin poly-beta-1,6-N-acetyl-D-glucosamine. J Bacteriol 188:8022–8032

    Article  PubMed  CAS  Google Scholar 

  18. Sobota AE (1984) Inhibition of bacterial adherence by cranberry juice: potential use for the treatment of urinary tract infections. J Urol 131:1013–1016

    PubMed  CAS  Google Scholar 

  19. Reid G, Hsiehl J, Potter P, Mighton J, Lam D, Warren D, Stephenson J (2001) Cranberry juice consumption may reduce biofilms on uroepithelial cells: pilot study in spinal cord injured patients. Spinal Cord 39:26–30

    Article  PubMed  CAS  Google Scholar 

  20. Greenberg JA, Newmann SJ, Howell AB (2005) Consumption of sweetened dried cranberries versus unsweetened raisins for inhibition of uropathogenic Escherichia coli adhesion in human urine: a pilot study. J Altern Complement Med 11:875–878

    Article  PubMed  Google Scholar 

  21. Howell AB, Reed JD, Krueger CG, Winterbottom R, Cunningham DG, Leahy M (2005) A-type cranberry proanthocyanidins and uropathogenic bacterial anti-adhesion activity. Phytochemistry 66:2281–2291

    Article  PubMed  CAS  Google Scholar 

  22. DiMartino P, Agniel R, Gaillard JL, Denys P (2005) Effects of cranberry juice on uropathogenic Escherichia coli in vitro biofilm formation. J Chemother 17:563–565

    CAS  Google Scholar 

  23. DiMartino P, Agniel R, David K, Templer C, Gaillard JL, Denys P, Botto H (2006) Reduction of Escherichia coli adherence to uroepithelial bladder cells after consumption of cranberry juice: a double-blind randomized placebo-controlled cross-over trial. World J Urol 24:21–27

    Article  CAS  Google Scholar 

  24. Valentova K, Stejskal D, Bednar P, Vostalova J, Cihalik C, Vecerova R, Koukalova D, Kolar M, Reichenbach R, Sknouril L, Ulrichova J, Simanek V (2007) Biosafety, antioxidant status, and metabolites in urine after consumption of dried cranberry juice in healthy women: a pilot double-blind placebo-controlled trial. J Agric Food Chem 55:3217–3224

    Article  PubMed  CAS  Google Scholar 

  25. Lavigne JP, Bourg G, Combescure C, Botto H, Sotto A (2008) In-vitro and in-vivo evidence of dose-dependent decrease of uropathogenic Escherichia coli virulence after consumption of commercial Vaccinium macrocarpon (cranberry) capsules. Clin Microbiol Infect 14:350–355

    Article  PubMed  Google Scholar 

  26. Howell AB, Botto H, Combescure C, Blanc-Potard AB, Gausa L, Matsumoto T, Tenke P, Sotto A, Lavigne JP (2010) Dosage effect on uropathogenic Escherichia coli anti-adhesion activity in urine following consumption of cranberry powder standardized for proanthocyanidin content: a multicentric randomized double blind study. BMC Infect Dis 10:94

    Article  PubMed  Google Scholar 

  27. Yamanaka A, Kimizuka R, Kato T, Okuda K (2004) Inhibitory effects of cranberry juice on attachment of oral streptococci and biofilm formation. Oral Microbiol Immunol 19:150–154

    Article  PubMed  CAS  Google Scholar 

  28. Prior RL, Lazarus SA, Cao G, Muccitelli H, Hammerstone JF (2001) Identification of procyanidins and anthocyanins in blueberries and cranberries (Vaccinium spp.) using high-performance liquid chromatography/mass spectrometry. J Agric Food Chem 49:1270–1276

    Article  PubMed  CAS  Google Scholar 

  29. Maatta-Riihinen KR, Kahkonen MP, Torronen AR, Heinonen IM (2005) Catechins and procyanidins in berries of vaccinium species and their antioxidant activity. J Agric Food Chem 53:8485–8491

    Article  PubMed  Google Scholar 

  30. Howell AB, Vorsa N, Der MA, Foo LY (1998) Inhibition of the adherence of P-fimbriated Escherichia coli to uroepithelial-cell surfaces by proanthocyanidin extracts from cranberries. N Engl J Med 339:1085–1086

    Article  PubMed  CAS  Google Scholar 

  31. Foo LY, Lu Y, Howell AB, Vorsa N (2000) A-type proanthocyanidin trimers from cranberry that inhibit adherence of uropathogenic P-fimbriated Escherichia coli. J Nat Prod 63:1225–1228

    Article  PubMed  CAS  Google Scholar 

  32. Foo LY, Lu Y, Howell AB, Vorsa N (2000) The structure of cranberry proanthocyanidins which inhibit adherence of uropathogenic P-fimbriated Escherichia coli in vitro. Phytochemistry 54:173–181

    Article  PubMed  CAS  Google Scholar 

  33. Liu Y, Black MA, Caron L, Camesano TA (2006) Role of cranberry juice on molecular-scale surface characteristics and adhesion behavior of Escherichia coli. Biotechnol Bioeng 93:297–305

    Article  PubMed  CAS  Google Scholar 

  34. Turner A, Chen SN, Joike MK, Pendland SL, Pauli GF, Farnsworth NR (2005) Inhibition of uropathogenic Escherichia coli by cranberry juice: a new antiadherence assay. J Agric Food Chem 53:8940–8947

    Article  PubMed  CAS  Google Scholar 

  35. Gupta K, Chou MY, Howell A, Wobbe C, Grady R, Stapleton AE (2007) Cranberry products inhibit adherence of p-fimbriated Escherichia coli to primary cultured bladder and vaginal epithelial cells. J Urol 177:2357–2360

    Article  PubMed  CAS  Google Scholar 

  36. Liu Y, Gallardo-Moreno AM, Pinzon-Arango PA, Reynolds Y, Rodriguez G, Camesano TA (2008) Cranberry changes the physicochemical surface properties of E. coli and adhesion with uroepithelial cells. Colloids Surf B Biointerfaces 65:35–42

    Article  PubMed  CAS  Google Scholar 

  37. Pinzon-Arango PA, Liu Y, Camesano TA (2009) Role of cranberry on bacterial adhesion forces and implications for Escherichia coli-uroepithelial cell attachment. J Med Food 12:259–270

    Article  PubMed  CAS  Google Scholar 

  38. Eydelnant IA, Tufenkji N (2008) Cranberry derived proanthocyanidins reduce bacterial adhesion to selected biomaterials. Langmuir 24:10273–10281

    Article  PubMed  CAS  Google Scholar 

  39. Milbury PE, Vita JA, Blumberg JB (2010) Anthocyanins are bioavailable in humans following an acute dose of cranberry juice. J Nutr 140:1099–1104

    Article  PubMed  CAS  Google Scholar 

  40. Fellers CR, Redmon BC, Parrott EM (1933) Effect of cranberries on urinary acidicity and blood alkali reserve. J Nutr 6:455–463

    CAS  Google Scholar 

  41. Mulder TP, Rietveld AG, Van Amelsvoort JM (2005) Consumption of both black tea and green tea results in an increase in the excretion of hippuric acid into urine. Am J Clin Nutr 81:256S–260S

    PubMed  CAS  Google Scholar 

  42. Lane MC, Mobley HL (2007) Role of P-fimbrial-mediated adherence in pyelonephritis and persistence of uropathogenic Escherichia coli (UPEC) in the mammalian kidney. Kidney Int 72:19–25

    Article  PubMed  CAS  Google Scholar 

  43. Wiles TJ, Kulesus RR, Mulvey MA (2008) Origins and virulence mechanisms of uropathogenic Escherichia coli. Exp Mol Pathol 85:11–19

    Article  PubMed  CAS  Google Scholar 

  44. Zafriri D, Ofek I, Adar R, Pocino M, Sharon N (1989) Inhibitory activity of cranberry juice on adherence of type 1 and type P fimbriated Escherichia coli to eucaryotic cells. Antimicrob Agents Chemother 33:92–98

    PubMed  CAS  Google Scholar 

  45. Naves P, del Prado G, Huelves L, Gracia M, Ruiz V, Blanco J, Rodriguez-Cerrato V, Ponte MC, Soriano F (2008) Measurement of biofilm formation by clinical isolates of Escherichia coli is method-dependent. J Appl Microbiol 105:585–590

    Article  PubMed  CAS  Google Scholar 

  46. Ferrieres L, Hancock V, Klemm P (2007) Biofilm exclusion of uropathogenic bacteria by selected asymptomatic bacteriuria Escherichia coli strains. Microbiology 153:1711–1719

    Article  PubMed  CAS  Google Scholar 

  47. Tong H, Heong S, Chang S (2006) Effect of ingesting cranberry juice on bacterial growth in urine. Am J Health Syst Pharm 63:1417–1419

    Article  PubMed  Google Scholar 

  48. Lee YL, Najm WI, Owens J, Thrupp L, Baron S, Shanbrom E, Cesario T (2008) Anti-microbial activity of urine after ingestion of cranberry: a pilot study. Evid Based Complement Alternat Med 7:227–232

    Google Scholar 

Download references

Acknowledgements

Terhi Tapiainen has received a grant from the Finnish Medical Foundation. Cranberry-lingonberry juice was donated by the manufacturer but other financial support was not received from the company.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to T. Tapiainen.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Tapiainen, T., Jauhiainen, H., Jaakola, L. et al. Biofilm formation and virulence of uropathogenic Escherichia coli in urine after consumption of cranberry-lingonberry juice. Eur J Clin Microbiol Infect Dis 31, 655–662 (2012). https://doi.org/10.1007/s10096-011-1355-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10096-011-1355-2

Keywords

Navigation