Parasitology Research

, Volume 93, Issue 5, pp 369–377 | Cite as

Trichomonas vaginalis virulence against epithelial cells and morphological variability: the comparison between a well-established strain and a fresh isolate

  • J. B. Jesus
  • M. A. Vannier-Santos
  • C. Britto
  • P. Godefroy
  • F. C. Silva-Filho
  • A. A. S. Pinheiro
  • B. Rocha-Azevedo
  • A. H. C. S. Lopes
  • J. R. Meyer-FernandesEmail author
Original Paper


The FMVI strain of Trichomonas vaginalis was freshly isolated from an asymptomatic patient, and its morphological properties and virulence in vitro compared with the well-established JT strain. The morphological variability of the parasites was assessed by differential interference microscopy and both scanning and transmission electron microscopy. The FMV1 strain presented nearly 20% amoeboid cells whereas the JT strain presented high percentages of ellipsoid but no amoeboid cells. The FMV1 morphotype population was unaltered after at least 1 year of subculturing. Electron microscopy revealed that this strain produced numerous pseudopod structures which mediated intimate contact and interdigitation among trophozoites. Dead FMV1 parasites were often phagocytosed by conspecific cells. We also compared the cytolytic capacity of these two populations against epithelial MDCK cells and its contact dependence. The FMV1 strain rapidly adhered to plastic or glass surfaces and to MDCK monolayers. This strain destroyed about 93% of the epithelial cells in 90 min whereas the cytolytic activity of the JT parasites was very much lower (about 41%). Parasite supernatants displayed no cytolytic activity, indicating contact-mediated lysis. The protozoan virulence in vitro did not correlate well with the clinical observations. The implications of these results are discussed.


MDCK Cell Trichomoniasis Vaginal Flora Vaginal Epithelial Cell Amoeboid Cell 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



We thank Dr. Wanderley de Souza for use of the scanning electron microscope facilities and Dr. Marlene Benchimol for providing the JT strain of T. vaginalis. We also thank Noemia R. Gonçalves for assistance with scanning electron microscopy, and Dr. Ximena Illarramendi and Patricia Cuervo for critically reading the manuscript. This work was supported by Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Financiadora de Estudos e Projetos (FINEP), Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ), PROCAD-CAPES and Programa Núcleos de Excelência (PRONEX; grant no. 0885).


  1. Alderete JF, Garza GE (1985) Specific nature of Trichomonas vaginalis parasitism on host cell surfaces. Infect Immun 50:701–708PubMedGoogle Scholar
  2. Alderete JF, Garza G (1988) Identification and properties of Trichomonas vaginalis proteins involved in cytoadherence. Infect Immun 56:28–33PubMedGoogle Scholar
  3. Alderete JF, Pearlman E (1984) Pathogenic Trichomonas vaginalis cytotoxicity to cell culture monolayers. Br J Vener Dis 60:99–105PubMedGoogle Scholar
  4. Alderete JF, Lehker MW, Arroyo R (1995) The mechanisms and molecules involved in cytoadherence and pathogenesis of Trichomonas vaginalis. Parasitol Today 11:70–74CrossRefGoogle Scholar
  5. Anaya-Ruiz M, Perez-Santos JL, Talamas-Rohana P (2003) An ecto-protein tyrosine phosphatase of Entamoeba histolytica induces cellular detachment by disruption of actin filaments in HeLa cells. Int J Parasitol 33:663–670CrossRefPubMedGoogle Scholar
  6. Arroyo R, Alderete JF (1989) Trichomonas vaginalis surface proteinase activity is necessary for parasite adherence to epithelial cells. Infect Immun 57:2991–2997PubMedGoogle Scholar
  7. Arroyo R, Engbring J, Alderete JF (1992) Molecular basis of host epithelial cell recognition by Trichomonas vaginalis. Mol Microbiol 6:853–862PubMedGoogle Scholar
  8. Arroyo R, Gonzales-Robles A, Martínez-Palomo A, Alderete JF (1993) Signaling of Trichomonas vaginalis for amoeboid transformation and adhesin synthesis follows cytoadherence. Mol Microbiol 7:299–309PubMedGoogle Scholar
  9. Bricheux G, Coffe G, Pradel N, Brugerolle G (1998) Evidence for an uncommon actinin protein in Trichomonas vaginalis. Mol Biochem Parasitol 95:241–249CrossRefPubMedGoogle Scholar
  10. Bricheux G, Coffe G, Bayle D, Brugerolle G (2000) Characterization, cloning and immunolocalization of a coronin homologue in Trichomonas vaginalis. Eur J Cell Biol 79:413–422PubMedGoogle Scholar
  11. Brugerolle G, Govert JG, Savel J (1974) Etude ultrastructural des lésions viscérales provoquées par l’injection intrapéritonéale de Trichomonas vaginalis chez la souris. Ann Parasitol 49:301–308Google Scholar
  12. Brugerolle G, Bricheux G, Coffe G (1996) Actin cytoskeleton demonstration in Trichomonas vaginalis and in other trichomonads. Biol Cell 88:29–36CrossRefPubMedGoogle Scholar
  13. Catterall RD (1972) Trichomonal infections of the genital tract. Med Clin N Am 56:1203–1209PubMedGoogle Scholar
  14. Crouch ML, Alderete JF (1999) Trichomonas vaginalis interactions with fibronectin and laminin. Microbiology 145:2835–2843PubMedGoogle Scholar
  15. Diamond LS (1957) The establishment of various trichomonads of animals and men in axenic culture. J Parasitol 43:488–490Google Scholar
  16. Escario JA, Gómez Barrio A, Martínez Fernández AR (1995) The relationship of experimental pathogenicity in vivo with in vitro cytoadherence and cytotocity of 6 different isolates of Trichomonas vaginalis. Int J Parasitol 25:999–1000CrossRefPubMedGoogle Scholar
  17. Farris VK, Honigberg BM (1970) Behavior and pathogenicity of Trichomonas vaginalis Donné in chick liver cell cultures. J Parasitol 56:849–882PubMedGoogle Scholar
  18. Fiori PL, Rappelli P, Addis MF, Mannu F, Cappuccinelli P (1997) Contact-dependent disruption of the host cell membrane skeleton induced by Trichomonas vaginalis. Infect Immun 65:5142–5148PubMedGoogle Scholar
  19. Garber GE, Lemchuk Favel LT, Bowie WR (1989). Isolation of a cell-detaching factor of Trichomonas vaginalis. J Clin Microbiol 27:1548–1555PubMedGoogle Scholar
  20. Garcia AF, Chang TH, Benchimol M, Klumpp DJ, Lehker MW, Alderete JF (2003) Iron and contact with host cells induce expression of adhesins on surface of Trichomonas vaginalis. Mol Microbiol 47:1207–1224CrossRefPubMedGoogle Scholar
  21. García-Tamayo J, Nuñez-Montiel JT, DeGarcía HP (1978) An electron microscopic investigaton on the patogenesis of human vaginal trichomoniasis. Acta Cytol 22:447–455PubMedGoogle Scholar
  22. Gilbert RO, Elia G, Beach DH, Klaessig S, Sing BN (2000) Cytopathogenic effect of Trichomonas vaginalis on human vaginal epithelial cells cultured in vitro. Infect Immun 68:4200–4206CrossRefPubMedGoogle Scholar
  23. Gram I, Macaluso M, Churchill J, Stalsberg H (1992) Trichomonas vaginalis (TV) and human papillomavirus (HPV) infection and the incidence of cervical intraepithelial neoplasia (CIN) grade III. Cancer Causes Control 3:231–236PubMedGoogle Scholar
  24. Granger BL, Warwood SJ, Benchimol M, De Souza W (2000) Transient invagination of flagella by Tritrichomonas foetus. Parasitol Res 86:699–709PubMedGoogle Scholar
  25. Grodstein F, Goldman MB, Cramer DW (1993) Relation of tubal infertility to a history of sexually transmitted diseases. Am J Epidemiol 137:577–584PubMedGoogle Scholar
  26. Heath JP (1981) Behavior and pathogenicity of Trichomonas vaginalis in epithelial cell cultures. A study by light and scanning electron microscopy. Br J Vener Dis 57:106–117PubMedGoogle Scholar
  27. Heine P, McGregor JA (1993) Trichomonas vaginalis: a reemerging pathogen. Clin Obstet Gynecol 36:137–144PubMedGoogle Scholar
  28. Honigberg BM (1961) Comparative pathogenicity of Trichomonas vaginalis and Trichomonas gallinae to mice. I. Gross pathology quantitative evaluation of virulence, and some factors affecting pathogenicity. J Parasitol 47:545–571PubMedGoogle Scholar
  29. Honigberg BM, Brugerolle G (1990) Structure. In: Honigberg BM (ed) Trichomonads parasitic in humans. Springer, Berlin Heidelberg New York, pp 5–35Google Scholar
  30. Honigberg BM, Livingston MC, Frost JK (1966) Pathogenicity of fresh isolates of Trichomonas vaginalis: “the mouse assay” versus clinical and pathological findings. Acta Cytol 10:353–361PubMedGoogle Scholar
  31. Jesus JB, Podlyska, T.M Lopes AHCS, Vannier-Santos MA, Meyer-Fernandes JR (2002) Characterization of an ecto-phosphatase activity in the human parasite Trichomonas vaginalis. Parasitol Res 88:991–997CrossRefPubMedGoogle Scholar
  32. Krieger JN, Poisson MA, Rein MF (1983) Beta-hemolytic activity of Trichomonas vaginalis correlates with virulence. Infect Immun 41:1291–1295PubMedGoogle Scholar
  33. Krieger JN, Ravdin JL, Rein MF (1985) Contact dependant cytopathogenic mechanisms of Trichomonas vaginalis. Infect Immun 50:778–786PubMedGoogle Scholar
  34. Kuczynska K, Choromanski L, Honigberg BM (1984) Comparison of virulence of clones of two Trichomonas vaginalis strains by the subcutaneous mouse assay. Z Parasitenkd 70:141–146PubMedGoogle Scholar
  35. Kulda J, Honigberg BM, Frost JK, Hollander DH (1970) Pathogenicity of Trichomonas vaginalis. A clinical and biologic study. Am J Obstet Gynecol 108:908–918PubMedGoogle Scholar
  36. Martinotti MG, Martinetto P, Savoia D (1986) Adherence of Trichomonas vaginalis to cell culture monolayers. Eur J Clin Microbiol 5:320–323PubMedGoogle Scholar
  37. Matuschka FR, Bannert B (1987) Cannibalism and autotomy as predator-prey relationship for monoxenous Sarcosporidia. Parasitol Res 74:88–93PubMedGoogle Scholar
  38. Minkoff H, Grunebaum AN, Schwarz RH, Feldman J, Cummings MC, Clark WL, Pringle G, McCormack MW (1984) Risk factors for prematurity and premature rupture of membranes: a prospective study of the vaginal flora in pregnancy. Am J Obstet Gynecol 150:965–972PubMedGoogle Scholar
  39. Nielsen MH, Nielsen R (1975) Electron microscopy of Trichomonas vaginalis Donné: interaction with vaginal epithelium in human trichomoniasis. Acta Pathol Microbiol Scand B 83:305–320PubMedGoogle Scholar
  40. Orozco E, Martínez-Palomo A, López-Revilla R (1978) Un modelo in vitro para el estudio cuantitativo de la virulencia de Entamoeba histolytica. Arch Invest Med (México) 9:257–260Google Scholar
  41. Petrin D, Delgaty K, Bhatt R, Garber G (1998) Clinical and microbiological aspects of Trichomonas vaginalis. Clin Microbiol Rev 11:300–317PubMedGoogle Scholar
  42. Pindak FF, Gardner WAJr, Mora de Pindak M (1986) Growth and cytopathogenicity of Trichomanas vaginalis in tissue cultures. J Clin Microbiol 23:672–678PubMedGoogle Scholar
  43. Rasmussen SE, Nielsen MH, Lind I, Rhodes JM (1986) Morphological studies of the cytotoxicity of the Trichomonas vaginalis to normal human vaginal epithelial cells in vitro. Geniturin Med 62:244–246Google Scholar
  44. Rendón-Maldonado JG, Espinosa-Cantellano M, Gonzalez-Robles A, Martínez-Palomo A (1998) Trichomonas vaginalis: in vitro phagocytosis of lactobacilli, vaginal epithelial cells, leukocytes and erythrocytes. Exp Parasitol 89:241–250CrossRefPubMedGoogle Scholar
  45. Silva-Filho FC, De Souza W (1988) The interaction of Trichomonas vaginalis and Tritrichomonas foetus with epithelial cells in vitro. Cell Struct Funct 13:301–310PubMedGoogle Scholar
  46. Silva-Filho FC, Elias CA, De Souza W (1986) Further studies on the surface charge of various strains of Trichomonas vaginalis and Tritrichomonas foetus. Cell Biophysics 8:161–176PubMedGoogle Scholar
  47. Vannier-Santos MA, Martiny A, Meyer-Fernandes JR, De Souza W (1995) Leishmanial protein kinase C modulates host cell infection via secreted acid phosphatase. Eur J Cell Biol 67:112–119PubMedGoogle Scholar
  48. Zhang ZF, Begg CB (1994) Is Trichomonas vaginalis a cause of cervical neoplasia? Results from a combined analysis of 24 studies. Int J Epidemiol 23:682–690PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  • J. B. Jesus
    • 1
    • 4
  • M. A. Vannier-Santos
    • 2
  • C. Britto
    • 1
  • P. Godefroy
    • 3
  • F. C. Silva-Filho
    • 4
  • A. A. S. Pinheiro
    • 5
  • B. Rocha-Azevedo
    • 4
  • A. H. C. S. Lopes
    • 6
  • J. R. Meyer-Fernandes
    • 5
    Email author
  1. 1.Departamento de Bioquímica e Biologia MolecularInstituto Oswaldo CruzRio de JaneiroBrazil
  2. 2.Centro de Pesquisas Gonçalo MonizFundação Oswaldo CruzSalvadorBrazil
  3. 3.Disciplina de ParasitologiaFaculdade de Medicina de ValençaValençaBrazil
  4. 4.Instituto de Biofísica Carlos Chagas FilhoUFRJRio de JaneiroBrazil
  5. 5.Departamento de Bioquímica Médica, ICBUFRJRio de JaneiroBrazil
  6. 6.Instituto de Microbiologia Professor Paulo de GóesUFRJRio de JaneiroBrazil

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