1887

Abstract

The aim of this work was to evaluate the effects of beneficial human vaginal lactobacilli (Lb) on urogenital pathogens through and experiments. Co-aggregative and antimicrobial properties between five vaginal Lb strains and urogenital pathogens or potential pathogens (, and strains) were assayed. Also, associative cultures of Lb strains and were performed and bacterial growth, pH, lactic acid and hydrogen peroxide (HO) were determined at different times. Based on the results obtained, the studies were assayed in mice with CRL 1509 or CRL 1328 inoculated intravaginally (i.v.) and then challenged i.v. with . Results were analysed by ANOVA (repeated measures and general linear models). Most of the Lb strains increased the percentage of aggregation of strains. Only one strain ( CRL 1324) positively affected the aggregation of and none increased the aggregation of . The inhibition of the growth of strains by production of organic acids by lactobacilli was evidenced. The Lb– co-cultures showed a significant inhibition of the pathogen after 4 h and 8 h of incubation. Parallel increases in lactic acid and HO levels were observed. However, in the experimental murine model, no significant differences were obtained in the number of streptococci recovered from the vaginal tract of control mice and those inoculated with Lb. In conclusion, vaginal Lb exhibited co-aggregative and antimicrobial effects on strains, suggesting that they could be promising candidates for protection against challenge. However, as these effects were not evidenced in the murine model used, further animal studies under different experimental conditions should be conducted to evaluate the preventive effect of Lb against challenge with .

Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.069401-0
2014-05-01
2020-01-29
Loading full text...

Full text loading...

/deliver/fulltext/jmm/63/5/685.html?itemId=/content/journal/jmm/10.1099/jmm.0.069401-0&mimeType=html&fmt=ahah

References

  1. Barrons R. , Tassone D. . ( 2008; ). Use of Lactobacillus probiotics for bacterial genitourinary infections in women: a review. . Clin Ther 30:, 453–468. [CrossRef] [PubMed]
    [Google Scholar]
  2. Bodaszewska M. , Brzychczy-Włoch M. , Gosiewski T. , Adamski P. , Strus M. , Heczko P. B. . ( 2010; ). Evaluation of group B streptococcus susceptibility to lactic acid bacteria strains. . Med Dosw Mikrobiol 62:, 153–161 (in Polish).[PubMed]
    [Google Scholar]
  3. Boris S. , Suárez J. E. , Barbés C. . ( 1997; ). Characterization of the aggregation promoting factor from Lactobacillus gasseri, a vaginal isolate. . J Appl Microbiol 83:, 413–420. [CrossRef] [PubMed]
    [Google Scholar]
  4. Boris S. , Suárez J. E. , Vázquez F. , Barbés C. . ( 1998; ). Adherence of human vaginal lactobacilli to vaginal epithelial cells and interaction with uropathogens. . Infect Immun 66:, 1985–1989.[PubMed]
    [Google Scholar]
  5. Cavaco C. K. , Patras K. A. , Zlamal J. E. , Thoman M. L. , Morgan E. L. , Sanderson S. D. , Doran K. S. . ( 2013; ). A novel C5a-derived immunobiotic peptide reduces Streptococcus agalactiae colonization through targeted bacterial killing. . Antimicrob Agents Chemother 57:, 5492–5499. [CrossRef] [PubMed]
    [Google Scholar]
  6. Chassot F. , Camacho D. P. , Patussi E. V. , Donatti L. , Svidzinski T. I. , Consolaro M. E. . ( 2010; ). Can Lactobacillus acidophilus influence the adhesion capacity of Candida albicans on the combined contraceptive vaginal ring?. Contraception 81:, 331–335. [CrossRef] [PubMed]
    [Google Scholar]
  7. Cheng Q. , Nelson D. , Zhu S. , Fischetti V. A. . ( 2005; ). Removal of group B streptococci colonizing the vagina and oropharynx of mice with a bacteriophage lytic enzyme. . Antimicrob Agents Chemother 49:, 111–117. [CrossRef] [PubMed]
    [Google Scholar]
  8. Clark L. R. , Atendido M. . ( 2005; ). Group B streptococcal vaginitis in postpubertal adolescent girls. . J Adolesc Health 36:, 437–440. [CrossRef] [PubMed]
    [Google Scholar]
  9. Collado M. C. , Surono I. , Meriluoto J. , Salminen S. . ( 2007; ). Indigenous dadih lactic acid bacteria: cell-surface properties and interactions with pathogens. . J Food Sci 72:, M89–M93. [CrossRef] [PubMed]
    [Google Scholar]
  10. De Gregorio P. R. , Juárez Tomás M. S. , Santos V. , Nader-Macías M. E. . ( 2012; ). Beneficial lactobacilli: effects on the vaginal tract in a murine experimental model. . Antonie van Leeuwenhoek 102:, 569–580. [CrossRef] [PubMed]
    [Google Scholar]
  11. De Man J. C. , Rogosa M. , Sharpe M. E. . ( 1960; ). A medium for the cultivation of lactobacilli. . J Appl Bacteriol 23:, 130–135. [CrossRef]
    [Google Scholar]
  12. Donders G. G. , Van Calsteren K. , Bellen G. , Reybrouck R. , Van den Bosch T. , Riphagen I. , Van Lierde S. . ( 2009; ). Predictive value for preterm birth of abnormal vaginal flora, bacterial vaginosis and aerobic vaginitis during the first trimester of pregnancy. . BJOG Int J Obstet Gynaecol 116:, 1315–1324. [CrossRef] [PubMed]
    [Google Scholar]
  13. Ekmekci H. , Aslim B. , Ozturk S. . ( 2009; ). Characterization of vaginal lactobacilli coaggregation ability with Escherichia coli. . Microbiol Immunol 53:, 59–65. [CrossRef] [PubMed]
    [Google Scholar]
  14. Fredricks D. N. , Fiedler T. L. , Marrazzo J. M. . ( 2005; ). Molecular identification of bacteria associated with bacterial vaginosis. . N Engl J Med 353:, 1899–1911. [CrossRef] [PubMed]
    [Google Scholar]
  15. Furr P. M. , Hetherington C. M. , Taylor-Robinson D. . ( 1989; ). The susceptibility of germ-free, oestradiol-treated, mice to Mycoplasma hominis. . J Med Microbiol 30:, 233–236. [CrossRef] [PubMed]
    [Google Scholar]
  16. Human Microbiome Project Consortium ( 2012; ). Structure, function and diversity of the healthy human microbiome. . Nature 486, 207–214.[CrossRef]
    [Google Scholar]
  17. ISAPP ( 2013; ).. Probiotics: Also, some experiments could be a Consumer Guide for Making Smart Choices Developed by the International Scientific Association for Probiotics and Prebiotics . . www.isapp.net
  18. Jones S. E. , Versalovic J. . ( 2009; ). Probiotic Lactobacillus reuteri biofilms produce antimicrobial and anti-inflammatory factors. . BMC Microbiol 9:, 35. [CrossRef] [PubMed]
    [Google Scholar]
  19. Juárez Tomás M. S. , Ocaña V. S. , Wiese B. , Nader-Macías M. E. . ( 2003; ). Growth and lactic acid production by vaginal Lactobacillus acidophilus CRL 1259, and inhibition of uropathogenic Escherichia coli . . J Med Microbiol 52:, 1117–1124. [CrossRef] [PubMed]
    [Google Scholar]
  20. Juárez Tomás M. S. , Claudia Otero M. , Ocaña V. , Elena Nader-Macías M. . ( 2004; ). Production of antimicrobial substances by lactic acid bacteria I: determination of hydrogen peroxide. . Methods Mol Biol 268:, 337–346.[PubMed]
    [Google Scholar]
  21. Juárez Tomás M. S. , Zonenschain D. , Morelli L. , Nader-Macías M. E. . ( 2005; ). Characterisation of potentially probiotic vaginal lactobacilli isolated from Argentinean women. . Br J Biomed Sci 62:, 170–174.[PubMed]
    [Google Scholar]
  22. Juárez Tomás M. S. , Saralegui Duhart C. I. , De Gregorio P. R. , Vera Pingitore E. , Nader-Macías M. E. . ( 2011; ). Urogenital pathogen inhibition and compatibility between vaginal Lactobacillus strains to be considered as probiotic candidates. . Eur J Obstet Gynecol Reprod Biol 159:, 399–406. [CrossRef] [PubMed]
    [Google Scholar]
  23. Larsen B. . ( 1993; ). Vaginal flora in health and disease. . Clin Obstet Gynecol 36:, 107–121. [CrossRef] [PubMed]
    [Google Scholar]
  24. Larsson P. G. , Forsum U. . ( 2005; ). Bacterial vaginosis – a disturbed bacterial flora and treatment enigma. . Acta Pathol Microbiol Immunol Scand 113:, 305–316. [CrossRef] [PubMed]
    [Google Scholar]
  25. Laufer N. , Quarleri J. , Bouzas M. B. , Juncos G. , Cabrini M. , Moretti F. , Bolcic F. , Fernández-Giuliano S. , Mammana L. . & other authors ( 2010; ). Hepatitis B virus, hepatitis C virus and HIV coinfection among people living with HIV/AIDS in Buenos Aires, Argentina. . Sex Transm Dis 37:, 342–343.[PubMed]
    [Google Scholar]
  26. Liu G. Y. , Doran K. S. , Lawrence T. , Turkson N. , Puliti M. , Tissi L. , Nizet V. . ( 2004; ). Sword and shield: linked group B streptococcal β-hemolysin/cytolysin and carotenoid pigment function to subvert host phagocyte defense. . Proc Natl Acad Sci U S A 101:, 14491–14496. [CrossRef] [PubMed]
    [Google Scholar]
  27. MacPhee R. A. , Hummelen R. , Bisanz J. E. , Miller W. L. , Reid G. . ( 2010; ). Probiotic strategies for the treatment and prevention of bacterial vaginosis. . Expert Opin Pharmacother 11:, 2985–2995. [CrossRef] [PubMed]
    [Google Scholar]
  28. Maisey H. C. , Doran K. S. , Nizet V. . ( 2008; ). Recent advances in understanding the molecular basis of group B Streptococcus virulence. . Expert Rev Mol Med 10:, e27. [CrossRef] [PubMed]
    [Google Scholar]
  29. Martín R. , Soberón N. , Vázquez F. , Suárez J. E. . ( 2008; ). Vaginal microbiota: composition, protective role, associated pathologies, and therapeutic perspectives. . Enferm Infecc Microbiol Clin 26:, 160–167. [CrossRef] [PubMed]
    [Google Scholar]
  30. Mastromarino P. , Vitali B. , Mosca L. . ( 2013; ). Bacterial vaginosis: a review on clinical trials with probiotics. . New Microbiol 36:, 229–238.[PubMed]
    [Google Scholar]
  31. McMillan A. , Dell M. , Zellar M. P. , Cribby S. , Martz S. , Hong E. , Fu J. , Abbas A. , Dang T. . & other authors ( 2011; ). Disruption of urogenital biofilms by lactobacilli. . Colloids Surf B Biointerfaces 86:, 58–64. [CrossRef] [PubMed]
    [Google Scholar]
  32. Mirowski G. W. , Schlosser B. J. , Stika C. S. . ( 2012; ). Cutaneous vulvar streptococcal infection. . J Low Genit Tract Dis 16:, 281–284. [CrossRef] [PubMed]
    [Google Scholar]
  33. Muench D. F. , Kuch D. J. , Wu H. , Begum A. A. , Veit S. J. , Pelletier M. E. , Soler-García A. A. , Jerse A. E. . ( 2009; ). Hydrogen peroxide-producing lactobacilli inhibit gonococci in vitro but not during experimental genital tract infection. . J Infect Dis 199:, 1369–1378. [CrossRef] [PubMed]
    [Google Scholar]
  34. Nader-Macías M. E. F. , Álvarez G. S. , Silva de Ruiz C. , Medina M. , Juárez Tomás M. S. . ( 2010; ). Lactic acid bacteria in prevention of the urogenital and respiratory infections. . In Biotechnology of Lactic Acid Bacteria: Novel Applications, pp. 141–160. Edited by Mozz F. . i, Raya R. R. , Vignolo G. M. . . Ames, IA:: Wiley-Blackwell;. [CrossRef]
    [Google Scholar]
  35. Ocaña V. S. , Nader-Macías M. E. . ( 2002; ). Vaginal lactobacilli: self- and co-aggregating ability. . Br J Biomed Sci 59:, 183–190.[PubMed]
    [Google Scholar]
  36. Ocaña V. S. , Bru E. , De Ruiz Holgado A. A. , Nader-Macias M. E. . ( 1999a; ). Surface characteristics of lactobacilli isolated from human vagina. . J Gen Appl Microbiol 45:, 203–212. [CrossRef] [PubMed]
    [Google Scholar]
  37. Ocaña V. S. , de Ruiz Holgado A. A. P. , Nader-Macías M. E. . ( 1999b; ). Characterization of a bacteriocin-like substance produced by a vaginal Lactobacillus salivarius strain. . Appl Environ Microbiol 65:, 5631–5635.[PubMed]
    [Google Scholar]
  38. Poisson D. M. , Evrard M. L. , Freneaux C. , Vivès M. I. , Mesnard L. . ( 2011; ). Evaluation of CHROMagar™ StrepB agar, an aerobic chromogenic medium for prepartum vaginal/rectal Group B Streptococcus screening. . J Microbiol Methods 84:, 490–491. [CrossRef] [PubMed]
    [Google Scholar]
  39. Rahman D. , Mistry M. , Thavaraj S. , Challacombe S. J. , Naglik J. R. . ( 2007; ). Murine model of concurrent oral and vaginal Candida albicans colonization to study epithelial host–pathogen interactions. . Microbes Infect 9:, 615–622. [CrossRef] [PubMed]
    [Google Scholar]
  40. Raibaud P. , Galpin J. V. , Ducluzeau R. , Mocquot G. , Oliver G. . ( 1973; ). The “Lactobacillus” genus in the digestive tract of rats. I. Characteristics of homofermentative strains isolated from holo- and gnotoxenic rats.. . Ann Microbiol (Paris) 124:, 83–109 (in French).[PubMed]
    [Google Scholar]
  41. Rajagopal L. . ( 2009; ). Understanding the regulation of Group B streptococcal virulence factors. . Future Microbiol 4:, 201–221. [CrossRef] [PubMed]
    [Google Scholar]
  42. Ravel J. , Gajer P. , Abdo Z. , Schneider G. M. , Koenig S. S. , McCulle S. L. , Karlebach S. , Gorle R. , Russell J. . & other authors ( 2011; ). Vaginal microbiome of reproductive-age women. . Proc Natl Acad Sci U S A 108: (Suppl. 1), 4680–4687. [CrossRef] [PubMed]
    [Google Scholar]
  43. Reid G. , Burton J. . ( 2002; ). Use of Lactobacillus to prevent infection by pathogenic bacteria. . Microbes Infect 4:, 319–324. [CrossRef] [PubMed]
    [Google Scholar]
  44. Reid G. , McGroarty J. A. , Domingue P. A. G. , Chow A. W. , Bruce A. W. , Eisen A. , Costerton J. W. . ( 1990; ). Coaggregation of urogenital bacteria in vitro and in vivo. . Curr Microbiol 20:, 47–52. [CrossRef]
    [Google Scholar]
  45. Reid G. , Jass J. , Sebulsky M. T. , McCormick J. K. . ( 2003; ). Potential uses of probiotics in clinical practice. . Clin Microbiol Rev 16:, 658–672. [CrossRef] [PubMed]
    [Google Scholar]
  46. Rönnqvist P. D. , Forsgren-Brusk U. B. , Grahn-Håkansson E. E. . ( 2006; ). Lactobacilli in the female genital tract in relation to other genital microbes and vaginal pH. . Acta Obstet Gynecol Scand 85:, 726–735. [CrossRef] [PubMed]
    [Google Scholar]
  47. Ruíz F. O. , Gerbaldo G. , García M. J. , Giordano W. , Pascual L. , Barberis I. L. . ( 2012; ). Synergistic effect between two bacteriocin-like inhibitory substances produced by Lactobacilli strains with inhibitory activity for Streptococcus agalactiae. . Curr Microbiol 64:, 349–356. [CrossRef] [PubMed]
    [Google Scholar]
  48. Saksena S. , Goyal S. , Raheja G. , Singh V. , Akhtar M. , Nazir T. M. , Alrefai W. A. , Gill R. K. , Dudeja P. K. . ( 2011; ). Upregulation of P-glycoprotein by probiotics in intestinal epithelial cells and in the dextran sulfate sodium model of colitis in mice. . Am J Physiol Gastrointest Liver Physiol 300:, G1115–G1123. [CrossRef] [PubMed]
    [Google Scholar]
  49. Saunders S. , Bocking A. , Challis J. , Reid G. . ( 2007; ). Effect of Lactobacillus challenge on Gardnerella vaginalis biofilms. . Colloids Surf B Biointerfaces 55:, 138–142. [CrossRef] [PubMed]
    [Google Scholar]
  50. Savini V. , Marrollo R. , D’Antonio M. , D’Amario C. , Fazii P. , D’Antonio D. . ( 2013; ). Streptococcus agalactiae vaginitis: nonhemolytic variant on the Liofilchem® Chromatic StreptoB. . Int J Clin Exp Pathol 6:, 1693–1695.[PubMed]
    [Google Scholar]
  51. Schachtsiek M. , Hammes W. P. , Hertel C. . ( 2004; ). Characterization of Lactobacillus coryniformis DSM 20001T surface protein Cpf mediating coaggregation with and aggregation among pathogens. . Appl Environ Microbiol 70:, 7078–7085. [CrossRef] [PubMed]
    [Google Scholar]
  52. Schellenberg J. , Smoragiewicz W. , Karska-Wysocki B. . ( 2006; ). A rapid method combining immunofluorescence and flow cytometry for improved understanding of competitive interactions between lactic acid bacteria (LAB) and methicillin-resistant S. aureus (MRSA) in mixed culture. . J Microbiol Methods 65:, 1–9. [CrossRef] [PubMed]
    [Google Scholar]
  53. Schwebke J. R. , Burgess D. . ( 2004; ). Trichomoniasis. . Clin Microbiol Rev 17:, 794–803. [CrossRef] [PubMed]
    [Google Scholar]
  54. Shanahan F. , Stanton C. , Ross P. , Hill C. . ( 2009; ). Pharmabiotics: bioactives from mining host-microbe-dietary interactions. . Functional Food Rev 1:, 20–25.
    [Google Scholar]
  55. Silva de Ruiz C. , Rey M. R. , de Ruiz Holgado A. P. , Nader-Macías M. E. . ( 2001; ). Experimental administration of estradiol on the colonization of Lactobacillus fermentum and Escherichia coli in the urogenital tract of mice. . Biol Pharm Bull 24:, 127–134. [CrossRef] [PubMed]
    [Google Scholar]
  56. Silva de Ruiz C. , Rey M. D. R. , Nader-Macías M. E. . ( 2003; ). Structural and ultrastructural studies of the urinary tract of mice inoculated with Lactobacillus fermentum. . BJU Int 91:, 878–882. [CrossRef] [PubMed]
    [Google Scholar]
  57. Terraf M. C. L. , Juárez Tomás M. S. , Nader-Macías M. E. , Silva C. . ( 2012; ). Screening of biofilm formation by beneficial vaginal lactobacilli and influence of culture media components. . J Appl Microbiol 113:, 1517–1529. [CrossRef] [PubMed]
    [Google Scholar]
  58. Vera Pingitore E. , Hébert E. M. , Nader-Macías M. E. , Sesma F. . ( 2009; ). Characterization of salivaricin CRL 1328, a two-peptide bacteriocin produced by Lactobacillus salivarius CRL 1328 isolated from the human vagina. . Res Microbiol 160:, 401–408. [CrossRef] [PubMed]
    [Google Scholar]
  59. Yao X. Y. , Yuan M. M. , Li D. J. . ( 2007; ). Molecular adjuvant C3d3 improved the anti-hCGβ humoral immune response in vaginal inoculation with live recombinant Lactobacillus expressing hCGβ-C3d3 fusion protein. . Vaccine 25:, 6129–6139. [CrossRef] [PubMed]
    [Google Scholar]
  60. Younes J. A. , van der Mei H. C. , van den Heuvel E. , Busscher H. J. , Reid G. . ( 2012; ). Adhesion forces and coaggregation between vaginal staphylococci and lactobacilli. . PLoS ONE 7:, e36917. [CrossRef] [PubMed]
    [Google Scholar]
  61. Zhou X. , Westman R. , Hickey R. , Hansmann M. A. , Kennedy C. , Osborn T. W. , Forney L. J. . ( 2009; ). Vaginal microbiota of women with frequent vulvovaginal candidiasis. . Infect Immun 77:, 4130–4135. [CrossRef] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jmm/10.1099/jmm.0.069401-0
Loading
/content/journal/jmm/10.1099/jmm.0.069401-0
Loading

Data & Media loading...

Supplements

Supplementary material 

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error