Identification, quantification and subtyping of Gardnerella vaginalis in noncultured clinical vaginal samples by quantitative PCR

Journal of Medical Microbiology

Volumn 63, Issue PART 2, 2014, Pages 162-175

  Balashov, Sergey V ^a   Mordechai, Eli ^a   Adelson, Martin E ^a   Gygax, Scott E ^a  

^a Medical Diagnostic Laboratories   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; ATOPOBIUM VAGINAE; BACTERIAL LOAD; BACTERIAL STRAIN; BACTERIUM CULTURE; BACTERIUM IDENTIFICATION; BACTEROIDES; BIFIDOBACTERIUM; CHLAMYDIA TRACHOMATIS; CLADISTICS; CONTROLLED STUDY; CORRELATION ANALYSIS; CORYNEBACTERIUM; CRYPTOCOCCUS NEOFORMANS; DNA DETERMINATION; DNA SEQUENCE; ENTEROBACTER AEROGENES; ENTEROCOCCUS FAECALIS; FEMALE; GARDNERELLA VAGINALIS; GENE FREQUENCY; GENETIC MARKER; GENOTYPE; HOUSEKEEPING GENE; HUMAN; MORPHOTYPE; MYCOPLASMA HOMINIS; NEISSERIA GONORRHOEAE; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; PREVALENCE; PREVOTELLA BIVIA; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; RISK ASSESSMENT; RISK FACTOR; SENSITIVITY AND SPECIFICITY; VAGINA FLORA; VAGINA SMEAR; VALIDATION STUDY;

ADULT; BACTERIAL LOAD; FEMALE; GARDNERELLA VAGINALIS; GENOTYPE; GRAM-POSITIVE BACTERIAL INFECTIONS; HUMANS; MIDDLE AGED; MOLECULAR DIAGNOSTIC TECHNIQUES; REAL-TIME POLYMERASE CHAIN REACTION; VAGINOSIS, BACTERIAL; YOUNG ADULT;

EID: 84892978620     PISSN: 00222615     EISSN: None     Source Type: Journal    
DOI: 10.1099/jmm.0.066407-0     Document Type: Article

References (53)

1. Ahmed, A., Earl, J., Retchless, A., Hillier, S. L., Rabe, L. K., Cherpes, T. L., Powell, E., Janto, B., Eutsey, R. & other authors (2012). Comparative genomic analyses of 17 clinical isolates of Gardnerella vaginalis provide evidence of multiple genetically isolated clades consistent with subspeciation into genovars. J Bacteriol 194, 3922-3937.
2. Amsel, R., Totten, P. A., Spiegel, C. A., Chen, K. C., Eschenbach, D. & Holmes, K. K. (1983). Nonspecific vaginitis. Diagnostic criteria and microbial and epidemiologic associations. Am J Med 74, 14-22.
3. Aroutcheva, A. A., Simoes, J. A., Behbakht, K. & Faro, S. (2001). Gardnerella vaginalis isolated from patients with bacterial vaginosis and from patients with healthy vaginal ecosystems. Clin Infect Dis 33, 1022-1027.
4. Benito, R., Vazquez, J. A., Berron, S., Fenoll, A. & Saez-Neito, J. A. (1986). A modified scheme for biotyping Gardnerella vaginalis. J Med Microbiol 21, 357-359.
5. Briselden, A. M. & Hillier, S. L. (1990). Longitudinal study of the biotypes of Gardnerella vaginalis. J Clin Microbiol 28, 2761-2764.
6. Catlin, B. W. (1992). Gardnerella vaginalis: characteristics, clinical considerations, and controversies. Clin Microbiol Rev 5, 213-237.
7. Chavagnat, F., Haueter, M., Jimeno, J. & Casey, M. G. (2002). Comparison of partial tuf gene sequences for the identification of lactobacilli. FEMS Microbiol Lett 217, 177-183.
8. 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.
9. Ehrlich, G. D., Hiller, N. L. & Hu, F. Z. (2008). What makes pathogens pathogenic. Genome Biol 9, 225.
10. El Aila, N. A., Tency, I., Saerens, B., De Backer, E., Cools, P., Dos Santos Santiago, G. L., Verstraelen, H., Verhelst, R., Temmerman, M. & Vaneechoutte, M. (2011). Strong correspondence in bacterial loads between the vagina and rectum of pregnant women. Res Microbiol 162, 506-513.
11. Eren, A. M., Zozaya, M., Taylor, C. M., Dowd, S. E., Martin, D. H. & Ferris, M. J. (2011). Exploring the diversity of Gardnerella vaginalis in the genitourinary tract microbiota of monogamous couples through subtle nucleotide variation. PLoS ONE 6, e26732.
12. Eschenbach, D. A. (1993). Bacterial vaginosis and anaerobes in obstetric-gynecologic infection. Clin Infect Dis 16 (Suppl. 4), S282-S287.
13. Farrelly, V., Rainey, F. A. & Stackebrandt, E. (1995). Effect of genome size and rrn gene copy number on PCR amplification of 16S rRNA genes from a mixture of bacterial species. Appl Environ Microbiol 61, 2798-2801.
14. Fethers, K. A., Fairley, C. K., Hocking, J. S., Gurrin, L. C. & Bradshaw, C. S. (2008). Sexual risk factors and bacterial vaginosis: a systematic review and meta-analysis. Clin Infect Dis 47, 1426-1435.
15. Forsum, U., Holst, E., Larsson, P. G., Vasquez, A., Jakobsson, T. & Mattsby-Baltzer, I. (2005). Bacterial vaginosis-a microbiological and immunological enigma. APMIS 113, 81-90.
16. Fredricks, D. N., Fiedler, T. L., Thomas, K. K., Mitchell, C. M. & Marrazzo, J. M. (2009). Changes in vaginal bacterial concentrations with intravaginal metronidazole therapy for bacterial vaginosis as assessed by quantitative PCR. J Clin Microbiol 47, 721-726.
17. Gardner, H. L. & Dukes, C. D. (1955). Haemophilus vaginalis vaginitis: a newly defined specific infection previously classified non-specific vaginitis. Am J Obstet Gynecol 69, 962-976.
18. Graham, S., Howes, C., Dunsmuir, R. & Sandoe, J. (2009). Vertebral osteomyelitis and discitis due to Gardnerella vaginalis. J Med Microbiol 58, 1382-1384.
19. Greenwood, J. R. & Pickett, M. J. (1980). Transfer of Haemophilus vaginalis Gardner and Dukes to a new genus, Gardnerella: G. vaginalis (Gardner and Dukes) comb. nov. Int J Syst Bacteriol 30, 170-178.
20. Harwich, M. D., Jr, Alves, J. M., Buck, G. A., Strauss, J. F., III, Patterson, J. L., Oki, A. T., Girerd, P. H. & Jefferson, K. K. (2010). Drawing the line between commensal and pathogenic Gardnerella vaginalis through genome analysis and virulence studies. BMC Genomics 11, 375.
21. Holst, E. (1990). Reservoir of four organisms associated with bacterial vaginosis suggests lack of sexual transmission. J Clin Microbiol 28, 2035-2039.
22. Ingianni, A., Petruzzelli, S., Morandotti, G. & Pompei, R. (1997). Genotypic differentiation of Gardnerella vaginalis by amplified ribosomal DNA restriction analysis (ARDRA). FEMS Immunol Med Microbiol 18, 61-66.
23. Klappenbach, J. A., Saxman, P. R., Cole, J. R. & Schmidt, T. M. (2001). rrndb: the ribosomal RNA operon copy number database. Nucleic Acids Res 29, 181-184.
24. Lagacé-Wiens, P. R., Ng, B., Reimer, A., Burdz, T., Wiebe, D. & Bernard, K. (2008). Gardnerella vaginalis bacteremia in a previously healthy man: case report and characterization of the isolate. J Clin Microbiol 46, 804-806.
25. Leopold, S. (1953). Heretofore undescribed organism isolated from the genitourinary system. U S Armed Forces Med J 4, 263-266.
26. Marrazzo, J. M., Fiedler, T. L., Srinivasan, S., Thomas, K. K., Liu, C., Ko, D., Xie, H., Saracino, M. & Fredricks, D. N. (2012). Extravaginal reservoirs of vaginal bacteria as risk factors for incident bacterial vaginosis. J Infect Dis 205, 1580-1588.
27. Menard, J. P., Fenollar, F., Henry, M., Bretelle, F. & Raoult, D. (2008). Molecular quantification of Gardnerella vaginalis and Atopobium vaginae loads to predict bacterial vaginosis. Clin Infect Dis 47, 33-43.
28. Moncla, B. J. & Pryke, K. M. (2009). Oleate lipase activity in Gardnerella vaginalis and reconsideration of existing biotype schemes. BMC Microbiol 9, 78.
29. Muzny, C. A. & Schwebke, J. R. (2013). Gardnerella vaginalis: still a prime suspect in the pathogenesis of bacterial vaginosis. Curr Infect Dis Rep 15, 130-135.
30. Neri, P., Salvolini, S., Giovannini, A. & Mariotti, C. (2009). Retinal vasculitis associated with asymptomatic Gardnerella vaginalis infection: a new clinical entity. Ocul Immunol Inflamm 17, 36-40.
31. Nugent, R. P., Krohn, M. A. & Hillier, S. L. (1991). Reliability of diagnosing bacterial vaginosis is improved by a standardized method of gram stain interpretation. J Clin Microbiol 29, 297-301.
32. Numanović, F., Hukić, M., Nurkić, M., Gegić, M., Delibegović, Z., Imamović, A. & Pasić, S. (2008). Importance of isolation and biotypization of Gardnerella vaginalis in diagnosis of bacterial vaginosis. Bosn J Basic Med Sci 8, 270-276.
33. Paradis, S., Boissinot, M., Paquette, N., Bé langer, S. D., Martel, E. A., Boudreau, D. K., Picard, F. J., Ouellette, M., Roy, P. H. & Bergeron, M. G. (2005). Phylogeny of the Enterobacteriaceae based on genes encoding elongation factor Tu and F-ATPase b-subunit. Int J Syst Evol Microbiol 55, 2013-2025.
34. Paramel Jayaprakash, T., Schellenberg, J. J. & Hill, J. E. (2012). Resolution and characterization of distinct cpn60-based subgroups of Gardnerella vaginalis in the vaginal microbiota. PLoS ONE 7, e43009.
35. Patterson, J. L., Stull-Lane, A., Girerd, P. H. & Jefferson, K. K. (2010). Analysis of adherence, biofilm formation and cytotoxicity suggests a greater virulence potential of Gardnerella vaginalis relative to other bacterial-vaginosis-associated anaerobes. Microbiology 156, 392-399.
36. Piot, P., van Dyck, E., Goodfellow, M. & Falkow, S. (1980). A taxonomic study of Gardnerella vaginalis (Haemophilus vaginalis) Gardner and Dukes 1955. J Gen Microbiol 119, 373-396.
37. Piot, P., Van Dyck, E., Totten, P. A. & Holmes, K. K. (1982). Identification of Gardnerella (Haemophilus) vaginalis. J Clin Microbiol 15, 19-24.
38. Piot, P., Van Dyck, E., Peeters, M., Hale, J., Totten, P. A. & Holmes, K. K. (1984). Biotypes of Gardnerella vaginalis. J Clin Microbiol 20, 677-679.
39. Pleckaityte, M., Janulaitiene, M., Lasickiene, R. & Zvirbliene, A. (2012). Genetic and biochemical diversity of Gardnerella vaginalis strains isolated from women with bacterial vaginosis. FEMS Immunol Med Microbiol 65, 69-77.
40. Sadhu, K., Domingue, P. A., Chow, A. W., Nelligan, J., Cheng, N. & Costerton, J. W. (1989). Gardnerella vaginalis has a Gram-positive cell-wall ultrastructure and lacks classical cell-wall lipopolysaccharide. J Med Microbiol 29, 229-235.
41. Santiago, G. L., Deschaght, P., El Aila, N., Kiama, T. N., Verstraelen, H., Jefferson, K. K., Temmerman, M. & Vaneechoutte, M. (2011). Gardnerella vaginalis comprises three distinct genotypes of which only two produce sialidase. Am J Obstet Gynecol 204, e1-e7.
42. Schellenberg, J. J., Links, M. G., Hill, J. E., Dumonceaux, T. J., Kimani, J., Jaoko, W., Wachihi, C., Mungai, J. N., Peters, G. A. & other authors (2011). Molecular definition of vaginal microbiota in East African commercial sex workers. Appl Environ Microbiol 77, 4066-4074.
43. Schwebke, J. R. & Desmond, R. (2007). Natural history of asymptomatic bacterial vaginosis in a high-risk group of women. Sex Transm Dis 34, 876-877.
44. Sheu, S. J., Hwang, W. Z., Chiang, Y. C., Lin, W. H., Chen, H. C. & Tsen, H. Y. (2010). Use of tuf gene-based primers for the PCR detection of probiotic Bifidobacterium species and enumeration of bifidobacteria in fermented milk by cultural and quantitative realtime PCR methods. J Food Sci 75, M521-M527.
45. Sivadon-Tardy, V., Roux, A. L., Piriou, P., Herrmann, J. L., Gaillard, J. L. & Rottman, M. (2009). Gardnerella vaginalis acute hip arthritis in a renal transplant recipient. J Clin Microbiol 47, 264-265.
46. Swidsinski, A., Doerffel, Y., Loening-Baucke, V., Swidsinski, S., Verstraelen, H., Vaneechoutte, M., Lemm, V., Schilling, J. & Mendling, W. (2010). Gardnerella biofilm involves females and males and is transmitted sexually. Gynecol Obstet Invest 70, 256-263.
47. Tosun, I., Alpay Karaoǧlu, S., Ciftci, H., Buruk, C. K., Aydin, F., Kilic, A. O. & Ertürk, M. (2007). [Biotypes and antibiotic resistance patterns of Gardnerella vaginalis strains isolated from healthy women and women with bacterial vaginosis]. Mikrobiyol Bul 41, 21-27 (in Turkish).
48. Udayalaxmi, J., Bhat, G. K. & Kotigadde, S. (2011). Biotypes and virulence factors of Gardnerella vaginalis isolated from cases of bacterial vaginosis. Indian J Med Microbiol 29, 165-168.
49. Ventura, M. & Zink, R. (2003). Comparative sequence analysis of the tuf and recA genes and restriction fragment length polymorphism of the internal transcribed spacer region sequences supply additional tools for discriminating Bifidobacterium lactis from Bifidobacterium animalis. Appl Environ Microbiol 69, 7517-7522.
50. Wertz, J. E., Goldstone, C., Gordon, D. M. & Riley, M. A. (2003). A molecular phylogeny of enteric bacteria and implications for a bacterial species concept. J Evol Biol 16, 1236-1248.
51. Yeoman, C. J., Yildirim, S., Thomas, S. M., Durkin, A. S., Torralba, M., Sutton, G., Buhay, C. J., Ding, Y., Dugan-Rocha, S. P. & other authors (2010). Comparative genomics of Gardnerella vaginalis strains reveals substantial differences in metabolic and virulence potential. PLoS ONE 5, e12411.
52. Yoon, H. J., Chun, J., Kim, J. H., Kang, S. S. & Na, D. J. (2010). Gardnerella vaginalis septicaemia with pyelonephritis, infective endocarditis and septic emboli in the kidney and brain of an adult male. Int J STD AIDS 21, 653-657.
53. 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.