In vitro and in vivo effects of beneficial vaginal lactobacilli on pathogens responsible for urogenital tract infections

Journal of Medical Microbiology

Volumn 63, Issue PART 5, 2014, Pages 685-696

  De Gregorio, Priscilla Romina ^a   Tomás, María Silvina Juárez ^a   Terraf, María Cecilia Leccese ^a   Nader Macías, María Elena Fátima ^a  

^a CENTRO DE REFERENCIA PARA LACTOBACILOS CERELA CONICET   (Argentina)

Author keywords

[No Author keywords available]

Indexed keywords

CARBOXYLIC ACID; HYDROGEN PEROXIDE; LACTIC ACID;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIMICROBIAL ACTIVITY; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL GROWTH; BACTERIUM CULTURE; CANDIDA ALBICANS; COCULTURE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; FEMALE; GROWTH INHIBITION; HUMAN; IN VITRO STUDY; IN VIVO STUDY; INFECTION PREVENTION; LACTOBACILLUS; LACTOBACILLUS GASSERI; LACTOBACILLUS REUTERI; LACTOBACILLUS RHAMNOSUS; LACTOBACILLUS SALIVARIUS; MOUSE; MURINE MODEL; NONHUMAN; PH; PRIORITY JOURNAL; STAPHYLOCOCCUS AUREUS; STREPTOCOCCUS AGALACTIAE; UROGENITAL TRACT INFECTION; VAGINA CYTOLOGY; VAGINA FLORA; VAGINAL LACTOBACILLUS;

ANIMALS; ANTI-INFECTIVE AGENTS; BACTERIAL ADHESION; CANDIDA ALBICANS; CARBOXYLIC ACIDS; DISEASE MODELS, ANIMAL; FEMALE; HUMANS; LACTOBACILLUS; MICE; MICE, INBRED BALB C; MICROBIAL INTERACTIONS; REPRODUCTIVE TRACT INFECTIONS; STAPHYLOCOCCUS AUREUS; STREPTOCOCCUS AGALACTIAE; VAGINA;

EID: 84899149140     PISSN: 00222615     EISSN: None     Source Type: Journal    
DOI: 10.1099/jmm.0.069401-0     Document Type: Article

References (61)

1. Barrons, R. & Tassone, D. (2008). Use of Lactobacillus probiotics for bacterial genitourinary infections in women: a review. Clin Ther 30, 453-468.
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).
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.
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.
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.
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.
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.
8. Clark, L. R. & Atendido, M. (2005). Group B streptococcal vaginitis in postpubertal adolescent girls. J Adolesc Health 36, 437-440.
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.
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.
11. De Man, J. C., Rogosa, M. & Sharpe, M. E. (1960). A medium for the cultivation of lactobacilli. J Appl Bacteriol 23, 130-135.
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.
13. Ekmekci, H., Aslim, B. & Ozturk, S. (2009). Characterization of vaginal lactobacilli coaggregation ability with Escherichia coli. Microbiol Immunol 53, 59-65.
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.
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.
16. Human Microbiome Project Consortium (2012).Structure, function and diversity of the healthy human microbiome. Nature 486, 207- 214.
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.
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.
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.
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.
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.
23. Larsen, B. (1993). Vaginal flora in health and disease. Clin Obstet Gynecol 36, 107-121.
24. Larsson, P. G. & Forsum, U. (2005). Bacterial vaginosis - a disturbed bacterial flora and treatment enigma. Acta Pathol Microbiol Immunol Scand 113, 305-316.
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.
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 bhemolysin/ cytolysin and carotenoid pigment function to subvert host phagocyte defense. Proc Natl Acad Sci U S A 101, 14491-14496.
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.
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.
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.
30. Mastromarino, P., Vitali, B. & Mosca, L. (2013). Bacterial vaginosis: a review on clinical trials with probiotics. New Microbiol 36, 229- 238.
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.
32. Mirowski, G. W., Schlosser, B. J. & Stika, C. S. (2012). Cutaneous vulvar streptococcal infection. J Low Genit Tract Dis 16, 281-284.
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 peroxideproducing lactobacilli inhibit gonococci in vitro but not during experimental genital tract infection. J Infect Dis 199, 1369-1378.
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 F. Mozzi, R. R. Raya & G. M. Vignolo, Ames, IA: Wiley-Blackwell.
35. Ocaña, V. S. & Nader-Macías, M. E. (2002). Vaginal lactobacilli: selfand co-aggregating ability. Br J Biomed Sci 59, 183-190.
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.
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.
38. Poisson, D. M., Evrard, M. L., Freneaux, C., Vivès, M. I. & Mesnard, L. (2011). Evaluation of CHROMagarTM StrepB agar, an aerobic chromogenic medium for prepartum vaginal/rectal Group B Streptococcus screening. J Microbiol Methods 84, 490-491.
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.
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).
41. Rajagopal, L. (2009). Understanding the regulation of Group B streptococcal virulence factors. Future Microbiol 4, 201-221.
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.
43. Reid, G. & Burton, J. (2002). Use of Lactobacillus to prevent infection by pathogenic bacteria. Microbes Infect 4, 319-324.
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.
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.
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.
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.
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 Pglycoprotein 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.
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.
50. Savini, V., Marrollo, R., D'Antonio, M., D'Amario, C., Fazii, P. & D'Antonio, D. (2013). Streptococcus agalactiae vaginitis: nonhemolytic variant on the Liofilchem1Chromatic StreptoB. Int J Clin Exp Pathol 6, 1693-1695.
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.
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.
53. Schwebke, J. R. & Burgess, D. (2004). Trichomoniasis. Clin Microbiol Rev 17, 794-803.
54. Shanahan, F., Stanton, C., Ross, P. & Hill, C. (2009). Pharmabiotics: bioactives from mining host-microbe-dietary interactions. Functional Food Rev 1, 20-25.
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.
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.
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.
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.
59. Yao, X. Y., Yuan, M. M. & Li, D. J. (2007). Molecular adjuvant C3d3 improved the anti-hCGb humoral immune response in vaginal inoculation with live recombinant Lactobacillus expressing hCGb- C3d3 fusion protein. Vaccine 25, 6129-6139.
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.
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.