The molecular genetic and phenotypic features of synanthropic and pathogenic Gardnerella vaginalis strains

Priputnevich T.V., Muravieva V.V., Gordeev A.B.

Academician V.I. Kulakov National Medical Research Center of Obstetrics, Gynecology, and Perinatology, Ministry of Health of Russia, Moscow, Russia
The authors analyzed the data of modern scientific literature on the molecular genetic and phenotypic features of synanthropic and pathogenic Gardnerella vaginalis strains isolated from the vaginal discharge of patients with bacterial vaginosis, as well as the relationship of the characteristics of the strains to the development of bacterial vaginosis. The data of foreign and Russian articles found in Pubmed and eLIBRARY on the investigation topic were considered. There have been recently conflicting data on a relationship of the molecular genetic and phenotypic features of G. vaginalis strains to the development of bacterial vaginosis. Although bacterial vaginosis has been known since ancient times, it is not yet possible to radically advance our understanding of the mechanisms of the symptomatic and asymptomatic course of the disease and its recurrence. However, significant advances in the development of molecular biology give hope for detecting molecular genetic markers, which make it possible to predict the efficiency of etiotropic therapy for bacterial vaginosis and the possibility of its recurrences.

Keywords

Gardnerella vaginalis
bacterial vaginosis
typing
molecular genetic features
virulence factors

References

  1. Ranjit E., Raghubanshi B.R., Maskey S., Parajuli P. Prevalence of bacterial vaginosis and its association with risk factors among nonpregnant women: a hospital based study. Int. J. Microbiol. 2018; 2018: 8349601.
  2. Sobel J.D. Bacterial vaginosis. Annu. Rev. Med. 2000; 51: 349-56.
  3. Patterson J.L., Stull-Lane A., Girerd P.H., Jefferson K.K. Analysis of adherence, biofilm formation and cytotoxicity suggests a greater virulence potential of Gardnerella vaginalis relative to other bacterial-vaginosis-associated anaerobes. Microbiology. 2010; 156(Pt 2): 392-9.
  4. Карапетян Т.Э., Анкирская А.С., Муравьева В.В. Бактериальный вагиноз в первом триместре беременности. Медицинский совет. 2015; 20: 68-71. [Karapetyan T.E., Ankirskaya A.S., Muravyova V.V. Bacterial vaginosis in the first trimester of pregnancy. Medicinskiy sovet. 2015; 68-71 (in Russian)].
  5. Jackie S., Gilbert D., David W., Jensen J.S. Руководство по ведению пациенток с синдромом патологических вагинальных выделений (ЮСТИ/ВОЗ, 2011). Consilium medicum. 2014; 6: 43-51.
  6. Мелкумян А.Р., Припутневич Т.В., Анкирская А.С., Трофимов Д.Ю., Муравьева В.В., Муллабаева С.М., Завьялова М.Г. Видовой состав лактобактерий при различном состоянии микробиоты влагалища у беременных. Клиническая микробиология и антимикробная химиотерапия. 2013; 15(1): 72-9. [Melkumyan A.R., Priputnevitch T.V., Ankirskaya A.S., Trofimov D.Yu., Muravyova V.V., Mullabaeva S.M., Zavyalova M.G. Lactobacilli species diversity in different states of vaginal microbiota in pregnant women. Klinicheskaya microbiologiya i antimikrobnaya khimioterapiya / Clinical microbiology and antimicrobial chemotherapy. 2013; 15: 72-9].
  7. Анкирская А.С. Бактериальный вагиноз. Акушерство и гинекология. 2005; 3: 10-3. [Ankirskaya A.S. Bacterial vaginosis. Akusherstvo i Ginekologiya / Obstetrics and Gynecology. 2005; 3:10-3].
  8. Amsel R., Totten P.A., Spigel C.A., Chen K.C.S., Eschenbach D., Holms K.K. Nonspecific vaginitis. Diagnostic criteria and microbial and epidemiologic associations. Am. J. Med. 1983; 74(1): 14-22.
  9. Menard J.-P., Mazouni C., Salem-Cherif I., Fenollar F., Raoult D., Boubli L. et al. High vaginal concentrations of Atopobium vaginae and Gardnerella vaginalis in women undergoing preterm labor. Obstet. Gynecol. 2010; 115(1): 134-40.
  10. Bradshaw C.S., Tabrizi S.N., Fairley C.K., Morton A.N., Rudland E., Garland S.M. The association of Atopobium vaginae and Gardnerella vaginalis with bacterial vaginosis and recurrence after oral metronidazole therapy. J. Infect. Dis. 2006; 194(6): 828-36.
  11. Gardner H.L., Dukes C.H. Haemophilus vaginalis vaginitis: a newly defined specific infection previously classified as ‘nonspecific’ vaginitis. Am. J. Obstet. Gynecol. 1955; 69(5): 962-76.
  12. Kim T.K., Thomas S.M., Ho M., Sharma S., Reich C.I., Frank J.A. et al. Heterogeneity of vaginal microbial communities within individuals. J. Clin. Microbiol. 2009; 47(4): 1181-9.
  13. Dowd S.E., Wolcott R.D., Sun Y., McKeehan T., Smith E., Rhoads D. Polymicrobial nature of chronic diabetic foot ulcer biofilm infection determined using bacterial tag encoded FLX amplicon pyrosequencing (bTEFAP). PLoS One. 2008; 3(10): e3326.
  14. Swidsinski A., Mendling W., Loening-Baucke V., Ladhoff A., Swidsinski W., Hale L.P. et al. Adherent biofilms in bacterial vaginosis. Obstet. Gynecol. 2005; 106(5, Pt 1): 1013-23.
  15. Gelber S.E., Aguilar J.L., Lewis K.L., Ratner A.J. Functional and phylogenetic characterization of vaginolysin, the human-specific cytolysin from Gardnerella vaginalis. J. Bacteriol. 2008; 190(11): 3896-903.
  16. Mania-Pramanik J., Kerkar S.C., Salvi V.S. Bacterial vaginosis: a cause of infertility? Int. J. STD AIDS. 2009; 20(11): 778-81.
  17. Menard J.P., Fenollar F., Henry M., Bretelle F., Raoult D. Molecular quantification of Gardnerella vaginalis and Atopobium vaginae loads to predict bacterial vaginosis. Clin. Infect. Dis. 2008; 47(1): 33-43.
  18. Atashili J., Poole C., Ndumbe P.M., Adimora A.A., Smith J.S. Bacterial vaginosis and HIV acquisition: a meta-analysis of published studies. AIDS. 2008; 22(12): 1493-501.
  19. Yoon H.J., Chun J., Kim J.H., Kang S.S., Na D.J. Gardnerella vaginalis septicaemia with pyelonephritis, infective endocarditis and septic emboli in the kidney and brain of an adult male. Int. J. STD AIDS. 2010; 21(9): 653-7.
  20. Neri P., Salvolini S., Giovannini A., Meriotti C. Retinal vasculitis associated with asymptomatic Gardnerella vaginalis infection: a new clinical entity. Ocul. Immunol. Inflamm. 2009; 17(1): 36-40.
  21. Sivadon-Tardy V., Roux A.L., Piriou P., Herrmann J.L., Gaillard J.L., Rottman M. Gardnerella vaginalis acute hip arthritis in a renal transplant recipient. J. Clin. Microbiol. 2009; 47(1): 264-5.
  22. Graham S., Howes C., Dusmuir R., Sandoe J. Vertebral osteomyelitis and discitis due to Gardnerella vaginalis. J. Med. Microbiol. 2009; 58(Pt 10): 1382-4.
  23. Gilbert N.M., Lewis W.G., Lewis A.L. Clinical features of bacterial vaginosis in a murine model of vaginal infection with Gardnerella vaginalis. PLoS One. 2013; 8 (3): e59539.
  24. Leopold S. Heretofore undescribed organism isolated from the genitourinary system. U. S. Armed Forces Med. J. 1953; 4(2): 263-6.
  25. Piot P., Van Dyck E., Peeters M., Hale J., Totten P.A., Holmes K.K. Biotypes of Gardnerella vaginalis. J. Clin. Microbiol. 1984; 20(4): 667-79.
  26. Benito R., Vazquez J.A., Berron S., Fenoll A., Saez-Neito J.A. A modified scheme for biotyping Gardnerella vaginalis. J. Med. Microbiol. 1986; 21(4): 357-9.
  27. Briselden A.M., Hillier S.L. Longitudinal study of the biotypes of Gardnerella vaginalis. J. Clin. Microbiol. 1990; 28(12): 2761-4.
  28. Udayalaxmi J., Bhat G.K., Kotigadde S. Biotypes and virulence factors of Gardnerella vaginalis isolated from cases of bacterial vaginosis. Indian J. Med. Microbiol. 2011; 29(2): 165-8.
  29. Pleckaityte M., Janulaitiene M., Lasickiene R., Zvirbliene A. Genetic and biochemical diversity of Gardnerella vaginalis strains isolated from women with bacterial vaginosis. FEMS Immunol. Med. Microbiol. 2012; 65(1): 69-77.
  30. El Aila N.A., Tency I., Claeys G., Verstraelen H., Saerens B., Santiago G.L. et al. Identification and genotyping of bacteria from paired vaginal and rectal samples from pregnant women indicates similarity between vaginal and rectal microflora. BMC Infect. Dis. 2009; 9: 167.
  31. Hummelen R., Fernandes A.D., Macklaim J.M., Dickson R.J., Changalucha J., Gloor G.B. et al. Deep sequencing of the vaginal microbiota of women with HIV. PLoS One. 2010; 5(8): e12078.
  32. Hill J.E., Goh S.H., Money D.M., Doyle M., Li A., Crosby W.L. et al. Characterization of vaginal microflora of healthy, nonpregnant women by chaperonin-60 sequence based methods. Am. J. Obstet. Gynecol. 2005; 193(3, Pt 1): 682-92.
  33. Schellenberg J.J., Links M.G., Hill J.E., Dumonceaux T.J., Kimani J., Jaoko W. et al. Molecular definition of vaginal microbiota in East African commercial sex workers. Appl. Environ. Microbiol. 2011; 77(12): 4066-74.
  34. Lopes dos Santos Santiago G., Deschaght P., El Aila N., Kiama T.N., Verstraelen H., Jefferson K.K. et al. Gardnerella vaginalis comprises three genotypes of which two produce sialidase. Am. J. Obstet. Gynecol. 2011; 204(5):450. e1-7.
  35. Paramel Jayaprakash T., Schellenberg J.J., Hill J.E. Resolution and characterization of distinct cpn60-based subgroups of gardnerella vaginalis in the vaginal microbiota. PLoS One. 2012; 7(8): e43009.
  36. Harwich M.D. Jr., Alves J.M., Buck G.A., Strauss, J.F., Patterson J.L., Oki A.T. et al. Drawing the line between commensal and pathogenic Gardnerella vaginalis through genome analysis and virulence studies. BMC Genomics. 2010; 11: 375.
  37. Yeoman C.J., Yildirim S., Thomas S.M., Durkin A.S., Torralba M., Sutton G. et al. Comparative genomics of Gardnerella vaginalis strains reveals substantial differences in metabolic and virulence potential. PLoS One. 2010; 5(8): e12411.
  38. Ahmed A., Earl J., Retchless A., Hillier S.L., Rabe L.K., Cherpes T.L. et al. Comparative genomic analyses of 17 clinical isolates of Gardnerella vaginalis provide evidence of multiple genetically isolated clades consistent with subspeciation into genovars. J. Bacteriol. 2012; 194(15): 3922-37.
  39. Balashov S.V., Mordechai E., Adelson M.E., Gygax S.E. Identification, quantification and subtyping of Gardnerella vaginalis in noncultured clinical vaginal samples by quantitative PCR. J. Med. Microbiol. 2014; 63(Pt 2): 162-75.
  40. Schellenberg J.J., Paramel Jayaprakash T., Withana Gamage N., Patterson M.H., Vaneechoutte M., Hill J.E. Gardnerella vaginalis subgroups defined by cpn60 sequencing and sialidase activity in isolates from Canada, Belgium and Kenya. PLoS One. 2016; 11(1): e0146510.
  41. Janulaitiene M., Paliulyte V., Grinceviciene S., Zakareviciene J., Vladisauskiene A., Marcinkute A. et al. Prevalence and distribution of Gardnerella vaginalis subgroups in women with and without bacterial vaginosis. BMC Infectious Diseases. 2017; 17(1): 394.
  42. Schuyler J.A., Mordechai E., Adelson M.E., Sobel J.D., Gygax S.E., Hilbert D.W. Identification of intrinsically metronidazole-resistant clades of Gardnerella vaginalis. Diagn. Microbiol. Infect. Dis. 2016; 84(1): 1-3.
  43. Hilbert D.W., Schuyler J.A., Adelson M.E., Mordechai E., Sobel J.D., Gygax S.E. Gardnerella vaginalis population dynamics in bacterial vaginosis. Eur. J. Clin. Microbiol. Infect. Dis. 2017; 36(7): 1269-78.
  44. Castro J., França A., Bradwell K.R., Serrano M.G., Jefferson K. K., Cerca N. Comparative transcriptomic analysis of Gardnerella vaginalis biofilms vs. planktonic cultures using RNA-seq. NPJ Biofilms Microbiomes. 2017; 3: 3.
  45. Schellenberg J.J., Patterson M.H., Hill J.E. Gardnerella vaginalis diversity and ecology in relation to vaginal symptoms. Res. Microbiol. 2017; 168(9-10):837-44.
  46. Cauci S., Monte R., Ropele M., Missero C., Not T., Quadrifoglio F. et al. Pore-forming and haemolytic properties of the Gardnerella vaginalis cytolysin. Mol. Microbiol. 1993; 9(6): 1143-55.
  47. Giddings K.S., Zhao J., Sims P.J., Tweten R.K. Human CD59 is a receptor for the cholesterol-dependent cytolysin intermedilysin. Nat. Struct. Mol. Biol. 2004; 11(12): 1173-8.
  48. Nagamune H., Ohnishi C., Katsuura A., Fushitani K., Whiley R.A., Tsuji A. et al. Intermedilysin, a novel cytotoxin specific for human cells secreted by Streptococcus intermedius UNS46 isolated from a human liver abscess. Infect. Immun. 1996; 64(8): 3093-100.
  49. Castro J., Alves P., Sousa C., Cereija T., Franca A., Jefferson K.K. et al. Using an in-vitro biofilm model to assess the virulence potential of bacterial vaginosis or non-bacterial vaginosis Gardnerella vaginalis isolates. Sci. Rep. 2015; 5: 11640.
  50. Knupp de Souza D.M., Diniz C.G., Filho D.S., Andrade de Oliveira L.M., Coelho D.M., Talha L.S. et al. Antimicrobial susceptibility and vaginolysin in Gardnerella vaginalis from healthy and bacterial vaginosis diagnosed women. J. Infect. Dev. Ctries. 2016; 10(9): 913-9.
  51. Scott T.G., Curran B., Smyth C.J. Electron microscopy of adhesive interactions between Gardnerella vaginalis and vaginal epithelial cells, McCoy cells and human red blood cells. J. Gen. Microbiol. 1989; 135(3): 475-80.
  52. Nikolaitchouk N., Andersch B., Falsen E., Strombeck L., Mattsby-Baltzer I. The lower genital tract microbiota in relation to cytokine-, SLPI- and endotoxin levels: application of checkerboard DNA–DNA hybridization (CDH). APMIS. 2008; 116(4): 263-77.
  53. Verstraelen H., Verhelst H., Claeys R., Temmerman G., Vaneechoutte M. Culture-independent analysis of vaginal microflora: the unrecognized association of Atopobium vaginae with bacterial vaginosis. Am. J. Obstet. Gynecol. 2004; 191(4): 1130-2.
  54. Lewis A.L., Lewis W.G. Host sialoglycans and bacterial sialidases: a mucosal perspective. Cell. Microbiol. 2012; 14(8): 1174-82.
  55. Lewis W.G., Robinson L.S., Gilbert N.M., Perry J.C., Lewis A.L. Degradation, foraging, and depletion of mucus sialoglycans by the vagina-adapted Actinobacterium Gardnerella vaginalis. J. Biol. Chem. 2013; 288(17): 12067-79.
  56. Hardy L., Jespers V., Van den Bulck M., Buyze J., Mwambarangwe L., Musengamana V. et al. The presence of the putative Gardnerella vaginalis sialidase A gene in vaginal specimens is associated with bacterial vaginosis biofilm. PLoS One. 2017; 12(2): e0172522.
  57. Schellenberg J.J., Patterson M.H., Hill J.E. Gardnerella vaginalis diversity and ecology in relation to vaginal symptoms. Res. Microbiol. 2017; 168(9-10): 837-44.
  58. Jarosik G.P., Land C.B., Duhon P., Chandler R., Mercer T. Acquisition of Iron by Gardnerella vaginalis. Infect. Immun. 1998; 66(10): 5041-7.
  59. Beigi R.H., Austin M.N., Meyn L.A., Krohn M.A., Hillier S.L. Antimicrobial resistance associated with the treatment of bacterial vaginosis. Am. J. Obstet. Gynecol. 2004; 191(4): 1124-9.

Received 01.06.2018

Accepted 22.06.2018

About the Authors

Priputnevich, Tatyana V., MD, head of the Department of Microbiology and Clinical Pharmacology, National Medical Research Center for Obstetrics, Gynecology and Perinatology named after Academician V.I. Kulakov of Ministry of Health of Russian Federation.
117997, Russia, Moscow, Ac. Oparina str. 4. Тel.: +79104145616. E-mail: t_priputnevich@oparina4.ru.
Muravieva, Vera V., candidate of biological science, senior researcher at the Laboratory of Microbiology, Department of Microbiology and Clinical Pharmacology,
National Medical Research Center for Obstetrics, Gynecology and Perinatology named after Academician V.I. Kulakov of Ministry of Health of Russian Federation.
117997, Russia, Moscow, Ac. Oparina str. 4. Тel.: +7906723-7235. E-mail: v_muravieva@oparina4.ru.
Gordeev, Aleksey B., сandidate of biological science, senior researcher at the Laboratory of Microbiology, Department of Microbiology and Clinical Pharmacology,
National Medical Research Center for Obstetrics, Gynecology and Perinatology named after Academician V.I. Kulakov of Ministry of Health of Russian Federation. .
117997, Russia, Moscow, Ac. Oparina str. 4. Тel.: 8 (916) 226-86-67, e-mail: a_gordeev@oparina4.ru.

For citation: Priputnevich T.V., Muravieva V.V., Gordeev A.B. The molecular genetic and phenotypic features of synanthropic and pathogenic Gardnerella vaginalis strains. Akusherstvo i Ginekologiya/Obstetrics and Gynecology.2019; (3): 10-7. (in Russian)
https://dx.doi.org/10.18565/aig.2019.3.10-17

Similar Articles

By continuing to use our site, you consent to the processing of cookies that ensure the proper functioning of the site.