Qualitative and semiquantitative analysis of Lactobacillus species in the vaginas of healthy fertile and postmenopausal Chinese women

Journal of Medical Microbiology

Volumn 61, Issue 5, 2012, Pages 729-739

  Zhang, Rui ^a   Daroczy, Katalin ^b   Xiao, Bingbing ^a   Yu, Li ^a   Chen, Rui ^a   Liao, Qinping ^a  

^a PEKING UNIVERSITY FIRST HOSPITAL   (China)

^b Ellen AB   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; RNA 16S;

ADULT; AGED; ARTICLE; BACTERIAL COLONIZATION; CHINESE; FEMALE; FERTILE PERIOD; HUMAN; LACTOBACILLUS; LACTOBACILLUS ACIDOPHILUS; LACTOBACILLUS CRISPATUS; LACTOBACILLUS DELBRUECKII; LACTOBACILLUS FERMENTUM; LACTOBACILLUS GASSERI; LACTOBACILLUS INERS; LACTOBACILLUS JOHNSONII; LACTOBACILLUS PARACASEI; LACTOBACILLUS PLANTARUM; LACTOBACILLUS REUTERI; LACTOBACILLUS RHAMNOSUS; LACTOBACILLUS SALIVARIUS; MAJOR CLINICAL STUDY; POLYMERASE CHAIN REACTION; POSTMENOPAUSE; PREVALENCE; PRIORITY JOURNAL; VAGINA FLORA;

ADOLESCENT; ADULT; AGED; ASIAN CONTINENTAL ANCESTRY GROUP; DNA, BACTERIAL; DNA, RIBOSOMAL; FEMALE; GENETIC VARIATION; HUMANS; LACTOBACILLUS; MENOPAUSE; MIDDLE AGED; POLYMERASE CHAIN REACTION; PREVALENCE; RNA, RIBOSOMAL, 16S; VAGINA; YOUNG ADULT;

EID: 84859852348     PISSN: 00222615     EISSN: None     Source Type: Journal    
DOI: 10.1099/jmm.0.038687-0     Document Type: Article

References (55)

1. Antonio, M. A., Hawes, S. E. & Hillier, S. L. (1999). The identification of vaginal Lactobacillus species and the demographic and microbiologic characteristics of women colonized by these species. J Infect Dis 180, 1950-1956.
2. Antonio, M. A., Meyn, L. A., Murray, P. J., Busse, B. & Hillier, S. L. (2009). Vaginal colonization by probiotic Lactobacillus crispatus CTV- 05 is decreased by sexual activity and endogenous lactobacilli. J Infect Dis 199, 1506-1513.
3. Anukam, K., Osazuwa, E., Ahonkhai, I., Ngwu, M., Osemene, G., Bruce, A. W. & 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, 1450-1454.
4. Bolton, M., van der Straten, A. & Cohen, C. R. (2008). Probiotics: potential to prevent HIV and sexually transmitted infections in women. Sex Transm Dis 35, 214-225.
5. Boskey, E. R., Telsch, K. M., Whaley, K. J., Moench, T. R. & Cone, R. A. (1999). Acid production by vaginal flora in vitro is consistent with the rate and extent of vaginal acidification. Infect Immun 67, 5170-5175.
6. Bradshaw, C. S., Morton, A. N., Hocking, J., Garland, S. M., Morris, M. B., Moss, L. M., Horvath, L. B., Kuzevska, I. & Fairley, C. K. (2006a). High recurrence rates of bacterial vaginosis over the course of 12 months after oral metronidazole therapy and factors associated with recurrence. J Infect Dis 193, 1478-1486.
7. Bradshaw, C. S., Tabrizi, S. N., Fairley, C. K., Morton, A. N., Rudland, E. & Garland, S. M. (2006b). The association of Atopobium vaginae and Gardnerella vaginalis with bacterial vaginosis and recurrence after oral metronidazole therapy. J Infect Dis 194, 828-836.
8. Burton, J. P. & Reid, G. (2002). Evaluation of the bacterial vaginal flora of 20 postmenopausal women by direct (Nugent score) and molecular (polymerase chain reaction and denaturing gradient gel electrophoresis) techniques. J Infect Dis 186, 1770-1780.
9. Burton, J. P., Cadieux, P. A. & Reid, G. (2003). Improved understanding of the bacterial vaginal microbiota of women before and after probiotic instillation. Appl Environ Microbiol 69, 97-101.
10. Byun, R., Nadkarni, M. A., Chhour, K. L., Martin, F. E., Jacques, N. A. & Hunter, N. (2004). Quantitative analysis of diverse Lactobacillus species present in advanced dental caries. J Clin Microbiol 42, 3128-3136.
11. Cadieux, P. A., 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), 13-18.
12. Cauci, S., Driussi, S., De Santo, D., Penacchioni, P., Iannicelli, T., Lanzafame, P., De Seta, F., Quadrifoglio, F., de Aloysio, D. & Guaschino, S. (2002). Prevalence of bacterial vaginosis and vaginal flora changes in peri- and postmenopausal women. J Clin Microbiol 40, 2147-2152.
13. De Backer, E., Verhelst, R., Verstraelen, H., Alqumber, M. A., Burton, J. P., Tagg, J. R., Temmerman, M. & Vaneechoutte, M. (2007). Quantitative determination by real-time PCR of four vaginal Lactobacillus species, Gardnerella vaginalis and Atopobium vaginae indicates an inverse relationship between L. gasseri and L. iners. BMC Microbiol 7, 115.
14. Devillard, E., Burton, J. P., Hammond, J. A., Lam, D. & Reid, G. (2004). Novel insight into the vaginal microflora in postmenopausal women under hormone replacement therapy as analyzed by PCR-denaturing gradient gel electrophoresis. Eur J Obstet Gynecol Reprod Biol 117, 76-81.
15. Dewhirst, F. E., Chen, T., Izard, J., Paster, B. J., Tanner, A. C., Yu, W. H., Lakshmanan, A. & Wade, W. G. (2010). The human oral microbiome. J Bacteriol 192, 5002-5017.
16. Ehrström, S., Daroczy, K., Rylander, E., Samuelsson, C., Johannesson, U., Anzén, B. & Påhlson, C. (2010). Lactic acid bacteria colonization and clinical outcome after probiotic supplementation in conventionally treated bacterial vaginosis and vulvovaginal candidiasis. Microbes Infect 12, 691-699.
17. Falsen, E., Pascual, C., Sjödén, B., Ohlén, M. & Collins, M. D. (1999). Phenotypic and phylogenetic characterization of a novel Lactobacillus species from human sources: description of Lactobacillus iners sp. nov. Int J Syst Bacteriol 49, 217-221.
18. Ferris, M. J., Norori, J., Zozaya-Hinchliffe, M. & Martin, D. H. (2007). Cultivation-independent analysis of changes in bacterial vaginosis flora following metronidazole treatment. J Clin Microbiol 45, 1016-1018.
19. 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.
20. Garg, K. B., Ganguli, I., Das, R. & Talwar, G. P. (2009). Spectrum of Lactobacillus species present in healthy vagina of Indian women. Indian J Med Res 129, 652-657.
21. Heilig, H. G., Zoetendal, E. G., Vaughan, E. E., Marteau, P., Akkermans, A. D. & de Vos, W. M. (2002). Molecular diversity of Lactobacillus spp. and other lactic acid bacteria in the human intestine as determined by specific amplification of 16S ribosomal DNA. Appl Environ Microbiol 68, 114-123.
22. Heinemann, C. & Reid, G. (2005). Vaginal microbial diversity among postmenopausal women with and without hormone replacement therapy. Can J Microbiol 51, 777-781.
23. Hillier, S. L. & Lau, R. J. (1997). Vaginal microflora in postmenopausal women who have not received estrogen replacement therapy. Clin Infect Dis 25 (Suppl. 2), S123-S126.
24. Hyman, R. W., Fukushima, M., Diamond, L., Kumm, J., Giudice, L. C. & Davis, R. W. (2005). Microbes on the human vaginal epithelium. Proc Natl Acad Sci U S A 102, 7952-7957.
25. Joesoef, M. & Schmid, G. (2003). Bacterial vaginosis. Clin Evid 10, 1824-1833.
26. Kemp, P. F. & Aller, J. Y. (2004). Bacterial diversity in aquatic and other environments: what 16S rDNA libraries can tell us. FEMS Microbiol Ecol 47, 161-177.
27. Kiss, H., Kögler, B., Petricevic, L., Sauerzapf, I., Klayraung, S., Domig, K., Viernstein, H. & Kneifel, W. (2007). Vaginal Lactobacillus microbiota of healthy women in the late first trimester of pregnancy. BJOG 114, 1402-1407.
28. Lamont, R. F., Sobel, J. D., Akins, R. A., Hassan, S. S., Chaiworapongsa, T., Kusanovic, J. P. & Romero, R. (2011). The vaginal microbiome: new information about genital tract flora using molecular based techniques. BJOG 118, 533-549.
29. Ling, Z., Kong, J., Liu, F., Zhu, H., Chen, X., Wang, Y., Li, L., Nelson, K. E., Xia, Y. & Xiang, C. (2010). Molecular analysis of the diversity of vaginal microbiota associated with bacterial vaginosis. BMC Genomics 11, 488.
30. Linhares, I. M., Giraldo, P. C. & Baracat, E. C. (2010). [New findings about vaginal bacterial flora]. Rev Assoc Med Bras 56, 370-374 (in Portuguese).
31. Liu, J. M., Sun, J., Yuan, J. L. & Kang, B. (2006). Difference of lactobacillus flora of vagina between healthy women and women with bacteria vaginosis. Prog Obstet Gynecol 115, 18-20.
32. Liu, X. Q., Yang, Y., Ma, F. & Zhang, X. Y. (2010). Progress on the evaluation system of human vaginal micro-eco-environment. Chin J Microecol 22, 662-665.
33. 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.
34. Martinez, R. C., Franceschini, S. A., Patta, M. C., Quintana, S. M., Gomes, B. C., De Martinis, E. C. & Reid, G. (2009). Improved cure of bacterial vaginosis with single dose of tinidazole (2 g), Lactobacillus rhamnosus GR-1, and Lactobacillus reuteri RC-14: a randomized, double-blind, placebo-controlled trial. Can J Microbiol 55, 133-138.
35. Pabich, W. L., Fihn, S. D., Stamm, W. E., Scholes, D., Boyko, E. J. & Gupta, K. (2003). Prevalence and determinants of vaginal flora alterations in postmenopausal women. J Infect Dis 188, 1054-1058.
36. Pavlova, S. I., Kilic, A. O., Kilic, S. S., So, J. S., Nader-Macias, M. E., Simoes, J. A. & Tao, L. (2002). Genetic diversity of vaginal lactobacilli from women in different countries based on 16S rRNA gene sequences. J Appl Microbiol 92, 451-459.
37. Reid, G. (1999). The scientific basis for probiotic strains of Lactobacillus. Appl Environ Microbiol 65, 3763-3766.
38. Reid, G. (2006a). Probiotics to prevent the need for, and augment the use of, antibiotics. Can J Infect Dis Med Microbiol 17, 291-295.
39. Reid, G. (2006b). Safe and efficacious probiotics: what are they? Trends Microbiol 14, 348-352.
40. Reid, G. & Bruce, A. W. (2001). Selection of lactobacillus strains for urogenital probiotic applications. J Infect Dis 183 (Suppl. 1), S77-S80.
41. Reid, G., Bruce, A. W., Fraser, N., Heinemann, C., Owen, J. & Henning, B. (2001). Oral probiotics can resolve urogenital infections. FEMS Immunol Med Microbiol 30, 49-52.
42. Reid, G., Charbonneau, D., Erb, J., Kochanowski, B., Beuerman, D., Poehner, R. & Bruce, A. W. (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, 131-134.
43. Reid, G., Younes, J. A., Van der Mei, H. C., Gloor, G. B., Knight, R. & Busscher, H. J. (2011). Microbiota restoration: natural and supplemented recovery of human microbial communities. Nat Rev Microbiol 9, 27-38.
44. Robert, H., Gabriel, V. & Fontagné-Faucher, C. (2009). Biodiversity of lactic acid bacteria in French wheat sourdough as determined by molecular characterization using species-specific PCR. Int J Food Microbiol 135, 53-59.
45. Shi, Y., Chen, L., Tong, J. & Xu, C. (2009). Preliminary characterization of vaginal microbiota in healthy Chinese women using cultivation-independent methods. J Obstet Gynaecol Res 35, 525-532.
46. Shiraishi, T., Fukuda, K., Morotomi, N., Imamura, Y., Mishima, J., Imai, S., Miyazawa, K. & Taniguchi, H. (2011). Influence of menstruation on the microbiota of healthy women's labia minora as analyzed using a 16S rRNA gene-based clone library method. Jpn J Infect Dis 64, 76-80.
47. Sobel, J. D., Schmitt, C. & Meriwether, C. (1993). Long-term followup of patients with bacterial vaginosis treated with oral metronidazole and topical clindamycin. J Infect Dis 167, 783-784.
48. Vallor, A. C., Antonio, M. A., Hawes, S. E. & Hillier, S. L. (2001). Factors associated with acquisition of, or persistent colonization by, vaginal lactobacilli: role of hydrogen peroxide production. J Infect Dis 184, 1431-1436.
49. Vásquez, A., Jakobsson, T., Ahrné, S., Forsum, U. & Molin, G. (2002). Vaginal Lactobacillus flora of healthy Swedish women. J Clin Microbiol 40, 2746-2749.
50. Ventura, M. & Zink, R. (2002). Specific identification and molecular typing analysis of Lactobacillus johnsonii by using PCR-based methods and pulsed-field gel electrophoresis. FEMS Microbiol Lett 217, 141-154.
51. Vermeulen, G. M., van Zwet, A. A. & Bruinse, H. W. (2001). Changes in the vaginal flora after two percent clindamycin vaginal cream in women at high risk of spontaneous preterm birth. BJOG 108, 697-700.
52. Walter, J., Hertel, C., Tannock, G. W., Lis, C. M., Munro, K. & Hammes, W. P. (2001). Detection of Lactobacillus, Pediococcus, Leuconostoc, and Weissella species in human feces by using group-specific PCR primers and denaturing gradient gel electrophoresis. Appl Environ Microbiol 67, 2578-2585.
53. Wang, M., Song, L., Yao, L.H., Jia, R., Chen, H., Liu, Y. & Zhang, Z.Q. & Q, X.U. (2009). Isolation and identification of vaginal lactobacilli from 223 healthy women of childbearing age. Chin J Clin Obstet Gynecol 10, 200-203.
54. Zhou, X., Bent, S. J., Schneider, M. G., Davis, C. C., Islam, M. R. & Forney, L. J. (2004). Characterization of vaginal microbial communities in adult healthy women using cultivation-independent methods. Microbiology 150, 2565-2573.
55. Zozaya-Hinchliffe, M., Lillis, R., Martin, D. H. & Ferris, M. J. (2010). Quantitative PCR assessments of bacterial species in women with and without bacterial vaginosis. J Clin Microbiol 48, 1812-1819.