Trichomonas vaginalis: pathogenesis and its role in cervical.

Tricomonas vaginalis: patogénesis y su papel en el cáncer cervical.

  • José Núñez-Troconis Universidad del Zulia
Palabras clave: Tricomonas vaginalis, cáncer del cuello uterino, mecanismo de la inflamación, carcinogénesis, infecciones de transmisión sexual, virus de la Trichomonas vaginalis

Resumen

El objetivo del artículo fue revisar y analizar el posible papel que el protozoario flagelado Tricomonas vaginalis tiene como co-factor en el origen y desarrollo del cáncer del cuello uterino. Para dicho propósito, se revi-só la bibliografía latino-americana e internacional en las páginas electrónicas de Pub-Med, Google Scholar, Springer, la biblioteca Cochrane, Embase, Scielo, Imbiomed-L, Redalyc and Latindex. La búsqueda incluyó las palabras claves: Tricomonas vaginalis, epidemiología de Trichomonas vaginalis, epidemiología del cáncer cervical, mecanismos de la inflamación, Trichomonas vaginalis y mecanismos de la inflamación, virus de Tricomonas vaginal, carcinogenesis, cáncer cervical y co-factores, infecciones de transmisión sexual y cáncer cervi-cal, mecanismos de la inflamación y cáncer cervical. Se revisaron y analizaron las publicaciones desde 1970 hasta junio 2020. Este artículo de revisión analizó los posibles mecanismos que la Tricomonas vaginalis pudiera jugar en la car-cinogénesis del cáncer del cuello uterino tanto como co-factor con el virus del papiloma o como un factor independiente.

Citas

Schwebke JR, Gaydos CA, Nyirjesy P, Paradis S, Kodsi S, Coopere CK. Diagnostic performance of a molecular test versus clinician assessment of vaginitis. J Clin Micro- biol 2018; 56 (6) 1-13.

Report on global sexually transmitted infection surveillance, 2018. World Health Organization 2018. Available at:https:// www.who.int/reproductivehealth/publica- tions/stis-surveillance-2018/en/. Reviewed on July 7, 2020.3. 2015 STD Treatment Guidelines – Tricho- moniasis – Updated diagnostic, treatment,and screening recommendations for STDs. Center for Disease Control and Prevention. https://www.cdc.gov/std/tg2015/tricho- moniasis.htm. Review on July 07, 2020.

Spence D, Melville C. Vaginal discharge. BMJ 2007;335(7630):1147-1151. doi: 10.1136/bmj.39378.633287.80.

Núñez-Troconis J. Diagnóstico de la Tricomonas vaginalis en la mujer. Rev Chil Obstet Ginecol 2020; 85(2): 175-184.

Rowley J, Vander Hoorn S, Korenromp E, Low N, Unemo M, Abu-Raddad LJ, Chico RM, Smolak A, Newman L, Gottlieb S, Thwin SS, Broutet N, Taylor MM. Chlamydia, gonorrhoea, trichomoniasis and syphilis: global prevalence and incidence estimates, 2016. Bull World Health Organ 201;97(8):548-562.

Leitsch D. Recent Advances in the Trichomonas vaginalis Field. F1000Res. 2016;5:F1000 Faculty Rev-162.

Lazenby GB, Taylor PT, Badman BS,Mchaki E, Korte JE, Soper DE, Pierce , Young-Pierce J. An association between Trichomonas vaginalis and high-risk human papillomavirus in rural Tanzanian women undergoing cervical cancer screening. Clin Ther 2014;36(1):38-45.

Trichomoniasis. Sexually Transmitted In- fections. Pan-American Health Organization.Available at https://www.paho.org/hq/ index.php?option=com_content&view=a rticle&id=14868:sti-trichomoniasis&Item id=3670&lang=en. Reviewed on July 07, 2020.

STD Surveillance 2018 – Other Sexually Transmitted Diseases – Trichomoniasis (October 8, 2019). Centers of Diseases of Control and Prevention. Available at: https://www.cdc.gov/std/trichomonas/ stats.htm. Reviewed on July 7, 2020.

Salomon MC, Martinez N, Delgado D, Gonzalez Arra C, Bittar V, Gonzalez N. Trichomonas vaginalis prevalence in sex workers. Medicina 2011;71(5): 429-431.

Neira OP, Correa LLA, Muñoz SN, Tardío OMT, Carabelli FM. Frecuencia de infección por Trichomonas vaginalis en atención primaria de salud. Rev Chil Obstet Ginecol 2005; 70:147-151.

Leon SR, Konda KA, Bernstein KT, Pajuelo JB, Rosasco AM, Caceres CF, Coates TJ, Klausner JD. Trichomonas vaginalis infection and associated risk factors in a socially-marginalized female population in coastal Peru. Infect Dis Obstet Gynecol 2009; 2009:752437.

Luppi CG, de Oliveira RL, Veras MA, Lippman SA, Jones H, de Jesus CH, Pinho AA, Ribeiro MC, Caiaffa-Filho H. Early diagnosis and correlations of sexually transmitted infections among women in primary care health services. Rev Bras Epidemiol 2011;14(3): 467-477.

Grama DF, Casarotti Lda S, Morato MG, Silva LS, Mendonca DF, Limongi JE, Viana Jda C, Cury MC. Prevalence of Trichomonas vaginalis and risk factors in women treated at public health units in Brazil: a transversal study. Trans R Soc Trop Med Hyg 2013;107(9): 584-591.

Ochoa DA, Filho RA, Marino JM, dos San- tos CM. Hidden sexually transmitted infec- tions among women in primary care health services, Amazonas, Brazil. Int J Std AIDS 2014;25(12): 878-886.

Núñez M, Flores T, Calchi M, Páez B. Epi- demiología, clínica y diagnóstico de Trichomonas vaginalis en mujeres aparentemente sanas del municipio Maracaibo. Estado Zulia, Venezuela. Kasmera 1997; 25(2):99-120.

Menezes CB, Frasson AP, Tasca T. Tricho- moniasis are we giving the deserved attention to the most common non-viral sexually transmitted disease worldwide? Microb Cell 2016;3(9):404-419.

Patel EU, Gaydos CA, Packman ZR, Quinn TC, Tobian AAR. Prevalence and correlates of Trichomonas vaginalis infection among men and women in the United States. Clin Infect Dis 2018;67(2):211-217.

Maritz JM, Land KM, Carlton JM, Hirt RP. What is the importance of zoonotic trichomonads for human health? Trends Parasitol 2014; 30(7): 333-341.

Petrin D, Delgaty K, Bhatt R, Garber G. Clinical and microbiological aspects of Trichomonas vaginalis. Clin Microbiol Rev 1998; 11(2): 300-317.

Zhang ZF, Begg CB. Is Trichomonas vaginalis a cause of cervical neoplasia? Results from a combined analysis of 24 studies. Int J Epidemiol 1994; 23(4): 682-690.

Viikki M, Pukkala E, Nieminen P, Hakama M. Gynaecological infections as risk determinants of subsequent cervical neoplasia. Acta Oncol 2000; 39(1): 71-75.

Silver BJ, Guy RJ, Kaldor JM, Jamil MS, Rumbold AR. Trichomonas vaginalis as a cause of perinatal morbidity: a systematic review and meta-analysis. Sex Transm Dis 2014; 41(6): 369-376.

Cotch MF, Pastorek JG, Nugent RP, Hillier SL, Gibbs RS, Martin DH, Eschenbach DA, Edelman R, Carey JC, Regan JA, Krohn MA, Klebanoff MA, Rao AV, Rhoads GG. Trichomonas vaginalis associated with low birth weight and preterm delivery. The vagi- nal infections and prematurity study group. Sex Transm Dis 1997;24(6): 353- 360.

Grodstein F, Goldman MB, Cramer DW. Relation of tubal infertility to history of sexually transmitted diseases. Epidemiol Rev 1997;137(5): 577-584.

Gimenes F, Souza RP, Bento JC, Teixeira JJ, Maria-Engler SS, Bonini MG, Consolaro ME. Male infertility: a public health issue caused by sexually transmitted pathogens. Nat Rev Urol 2014; 11(12): 672-687.

McClelland RS, Sangare L, Hassan WM, Lavreys L, Mandaliya K, Kiarie J, Ndin- ya-Achola J, Jaoko W, Baeten JM. Infec- tion with Trichomonas vaginalis increases the risk of HIV-1 acquisition. J Infect Dis 2007;195(5): 698-702.

Poole DN, McClelland RS. Global epide- miology of Trichomonas vaginalis. Sex Transm Infect 2013;89(6): 418-422.

Lehker MW, Alderete JF. Biology of trichomonosis. Curr Opin Infect Dis 2000;13(1): 37-45.

Kissinger P. Epidemiology and treatment of trichomoniasis. Curr Infect Dis Rep 2015;17(6):484.

Kissinger P. Trichomonas vaginalis: a review of epidemiologic, clinical and treatment issues. BMC Infect Dis 2015;15:307. P

Hirt RP. Trichomonas vaginalis virulence factors: an integrative overview. Sex Transm Infect. 2013 Sep;89(6):439-43. doi: 10.1136/sextrans-2013-051105. Epub 2013 May 21.

Harp DF, Chowdhury I. Trichomoniasis: evaluation to execution. Eur J Obstet Gynecol Reprod Biol 2011; 157(1):3–9.

Lindmark DG, Müller M. Hydrogenosome, a cytoplasmic organelle of the anaerobic flagellate Tritrichomonas foetus, and its role in pyruvate metabolism. J Biol Chem 1973; 248(22): 7724–7728.

Pustan L, AilieseioI O, Dunca S. Trichomonas vaginalis, a risk factor for cervical cancer. Analele Ştiinţifice ale Universităţii, Alexandru Ioan Cuza”, Secţiunea Genetică şi Biologie Moleculară, TOM XI, 2010. Page: 107-112.

Leitsch D. Recent advances in the Trichomonas vaginalis field. F1000Res. 2016;5:F1000 Faculty Rev-162.

Carlton JM, Hirt RP, Silva JC, Delcher AL, Schatz M, Zhao Q, Wortman JR, Bidwell SL, Alsmark UCM, Besteiro S. Draft ge- nome sequence of the sexually transmitted pathogen Trichomonas vaginalis. Science 2007;315:207–212.

Krieger JN. Trichomoniasis in men: old issues and new data. Sex Transm Dis 1995;22(2):83–96.

Afzan MY, Suresh K. Pseudocyst forms of Trichomonas vaginalis from cervical neoplasia. Parasitol Res 2012;111(1):371–381.

Pereira-Neves A, Ribeiro KC, Benchimol M. Pseudocysts in trichomonads–new in- sights. Protist 2003;154(3–4):313–329.

Goodman RP, Ghabrial SA, Fichorova RN, Nibert ML. Trichomonasvirus: a new genus of protozoan viruses in the family Totiviridae. Arch Virol 2011; 156(1): 171–179.

Goodman RP2, Freret TS, Kula T, Geller AM, Talkington MW, Tang-Fernandez V, Suciu O, Demidenko AA, Ghabrial SA, Beach DH, Singh BN, Fichorova RN, Nibert ML. Clinical isolates of Trichomonas vaginalis concurrently infected by strains of up to four Trichomonasvirus species (Family Toti- viridae). J Virol 2011;85(9):4258-4270.

Singh M, Beri D, Nageshan RK, Chavaan L, Gadara D, Poolary M, Subramaniam S, Tatu U. A secreted Heat shock protein 90 of Trichomonas vaginalis. PLoS Negl Trop Dis 2018;12(5):e0006493.

Arroyo R, Engbring J, Alderete JF. Molecular basis of host epithelial cell recognition by Trichomonas vaginalis. Mol Microbiol 1992;6(7):853-862.

Ferguson MA. The structure, biosynthesis and functions of glycosylphosphatidylinositol anchors, and the contributions of trypanosome research. J. Cell Sci 1999;112:2799–2809.

Guha-Niyogi A, Sullivan DR, Turco SJ. Glycoconjugate structures of parasitic pro- tozoa. Glycobiology 2001;11:45R–59R.

Fichorova RN, Trifonova RT, Gilbert RO, Costello CE, Hayes GR, Lucas JJ, Singh BN. Trichomonas vaginalis lipophosphoglycan triggers a selective up-regulation of cytokines by human female reproductive tract epithelial cells. Infect Immun 2006; 74:5773–5779.

Singh BN. Lipophosphoglycan-like glyco- conjugate of Trichomonas foetus and Trichomonas vaginalis. Mol. Biochem. Parasitol 1993;57:281–294.

Singh BN, Beach DH, Lindmark DG, Co- stello CE. Identification of the lipid moiety and further characterization of the novel lipophoshoglycan-like glycoconjugates of Trichomonas vaginalis and Trichomo- nas foetus. Arch Biochem Biophys 1994; 309:273–280.

Gilbert RO, Elia G, Beach DH, Klaessig S, Singh BN. Cytopathogenic effect of Trichomonas vaginalis on human vaginal epithelial cells cultured in vitro. Infect Immun 2000;68(7):4200-4206.

Ryan CM, de Miguel N, Johnson PJ. Trichomonas vaginalis: current understanding of host-parasite interactions. Essays Biochem 2011;51:161-175.

Pereira-Neves A, Benchimol M. Phagocytosis by Trichomonas vaginalis: new insights. Biol Cell 2007; 99:87–101.

Hirt RP, Noel CJ, Sicheritz-Ponten T, Tachezy J, Fiori PL. Trichomonas vaginalis surface proteins: a view from the genome. Trends Parasitol 2007;23:540–547.

Engbring JA, Alderete JF. Characterization of Trichomonas vaginalis AP33 adhesin and cell surface interactive domains. Microbio- logy 1998;144:3011–3018.

Garcia AF, Alderete J. Characterization of the Trichomonas vaginalis surface-associa- ted AP65 and binding domain interacting with trichomonads and host cells. BMC Microbiol 2007;7:116.

Alderete JF, Millsap KW, Lehker MW, Benchimol M. Enzymes on microbial pathogens and Trichomonas vaginalis: molecular mimicry and functional diversity. Cell Mi- crobiol 2001; 3:359–370.

Addis MF, Rappelli P, Fiori PL. Host and tissue specificity of Trichomonas vaginalis is not mediated by its known adhesion proteins. Infect Immun 2000;68:4358–4360.

Ardalan S, Lee BC, Garber GE. Trichomonas vaginalis: the adhesins AP51 and AP65 bind heme and hemoglobin. Exp Parasitol 2009;121:300–306.

Lama A, Kucknoor A, Mundodi V, Alderete JF. Glyceraldehyde-3-phosphate dehydro- genase is a surface-associated, fibronectin- binding protein of Trichomonas vaginalis. Infect Immun 2009;77:2703–2711.

Warton A1, Honigberg BM. Lectin analysis of surface saccharides in two Trichomonas vaginalis strains differing in pathogenicity. J Protozool 1980;27:410–419.

Warton A, Kon VB, Papadimitriou JM. Demonstration of concanavalin A and wheat germ agglutinin-binding sites on the Tri- chomonas vaginalis surface coat using lec- tin–gold particle conjugates. J Electron Mi- crosc (Tokyo) 1888;37:134–140.

Bastida-Corcuera FD, Okumura CY, Co- locoussi A, Johnson PJ. Trichomonas vaginalis lipophosphoglycan mutants have reduced adherence and cytotoxicity to human ectocervical cells. Eukaryot Cell 2005; 4:1951–1958.

Okumura CYM, Baum LG, Johnson PJ. Galectin-1 on cervical epithelial cells is a receptor for the sexually transmitted human parasite Trichomonas vaginalis. Cell Microbiol 2008;10:2078–2090.

Singh BN4, Hayes GR, Lucas JJ, Sommer U, Viseux N, Mirgorodskaya E, Trifonova RT, Sassi RR, Costello CE, Fichorova RN. Structural details and composition of Trichomonas vaginalis lipophosphoglycan in relevance to the epithelial immune function. Glycoconj J 2009;26:3–17.

Alderete JF2, Garza GE. Specific nature of Trichomonas vaginalis parasitism of host cell surfaces. Infect Immun 1985;50:701– 708.

De Miguel N, Lustig G, Twu O, Chattopadhyay A, Wohlschlegel JA, Johnson PJ. Proteome analysis of the surface of Tricho- monas vaginalis reveals novel proteins and strain-dependent differential expression. Mol Cell Proteomics 2010;9:1554–1566.

Bonilha VL, Ciavaglia Mdo C, de Souza W, Costa e Silva Filho F. The involvement of terminal carbohydrates of the mammalian cell surface in the cytoadhesion of tricho- monads. Parasitol Res 1995;81:121–126.

Noel CJ, Diaz N, Sicheritz-Ponten T, Safarikova L, Tachezy J, Tang P, Fiori PL, Hirt RP. Trichomonas vaginalis vast BspA-like gene family: evidence for functional diversity from structural organisation and trans- criptomics. BMC Genomics 2010;11:99.

Lin WC, Chang WT, Chang TY, Shin JW. The pathogenesis of human cervical epithelium cells Induced by Interacting with Trichomonas vaginalis. PLoS One. 2015;10(4):e0124087.

Kucknoor AS, Mundodi V, Alderete JF. The proteins secreted by Trichomonas vaginalis and vaginal epithelial cell response to secreted and episomally expressed AP65. Cell Microbiol 2007; 9 (11):2586–2597.

Kucknoor AS, Mundodi V, Alderete JF. Trichomonas vaginalis adherence mediates differential gene expression in human vaginal epithelial cells. Cell Microbiol 2005; 7(6):887–897. doi: 10.1111/j. 1462-5822.2005.00522.x.

Koch S, Nusrat A. Dynamic regulation of epithelial cell fate and barrier function by intercellular junctions. Ann N Y Acad Sci 2009; 1165:220–227.

Lehker MW, Sweeney D. Trichomonad invasion of the mucous layer requires adhesins, mucinases, and motility. Sex Transm Infect 1999; 75(4):231–238.

Arroyo R, González-Robles A, Martínez-Pa- lomo A, Alderete JF. Signalling of Trichomo- nas vaginalis for amoeboid transformation and adhesion synthesis follows cytoadher- ence. Mol Microbiol 1993;7(2):299-309.

Guenthner PC, Secor WE, Dezzutti CS. Trichomonas vaginalis-induced epithelial monolayer disruption and human immunodeficiency virus type 1 (HIV-1) replication: implications for the sexual transmission of HIV-1. Infect Immun 2005; 73(7):4155–4160.

Fiori PL 1, Rappelli P, Addis MF, Mannu F, Cappuccinelli P. Contact-dependent disruption of the host cell membrane skeleton induced by Trichomonas vaginalis. Infect Immun 1997; 65(12):5142–5148.

Provenzano D, Khoshnan A, Alderete JF. Involvement of dsRNA virus in the protein composition and growth kinetics of host Trichomonas vaginalis. Arch Virol 1997; 142: 939–952.

Garcia-Tamayo J, Nuñez-Montiel JT, de Garcia HP. An electron microscopic investigation on the pathogenesis of human vaginal trichomoniasis. Acta Cytol 1978;22(6):447-455.

Garcia-Tamayo J, Nuñez-Montiel JT, de Garcia HP. Tricomoniasis vaginal humana: Estudio ultrastructural e histoquimico. Invest Clin 1972;13:2-14.

Heath JP. Behaviour and pathogenici- ty of Trichomonas vaginalis in epithelial cell cultures: a study by light and scanning electron microscopy. Br J Vener Dis 1981;57(2):106-117.

Nielsen MH, Nielsen R. Electronmicroscopy of Trichomonas vaginalis: Interaction with vaginal epithelium in human trichomoniasis. Acta Pathol Microbiol Scand (B) 1975;83:305-320.

Engbring J, Alderete JF. Characterization of Trichomonas vaginalis AP33 adhesin and cell surface interactive domains. Microbio- logy 1998;144:3011–3018.

Mendoza-Lopez M, C. Becerril-Garcia L, Fattel-Facenda v, Avila-Gonzalez L, Ruiz- Tachiquin ME, Ortega-Lopez J, Arroyo R. CP30, a cysteine proeinase involved in Trichomonas vaginalis cytoadherence. Infect Immun 2000;68:4907–4912.

Tsai C, Liu HW, Tai JH. Characterization of an iron responsive promoter in the protozoan pathogen Trichomonas vaginalis. J Biol Chem 2002;277:5153–5162.

Fais S, Malorni W. Leukocycte uropod formation and membrane/cytoskeleton linkage in immune interactions. J Leukoc Biol 203;73:556–563.

Silva-Filho F, Kasai S, Nomizu M, Lopez LB, Melo-Braga MB, Rocha-Azevedo B, Petropolis DB, Horbach IS. How laminin-1 can be recognized by the protozoan para- site Tritrichomonas foetus: possible role played by the extracellular matrix glycoprotein in both cytoadhesion and cytotoxicity exerted by the parasite. Parasitol Int 2002;51:305–307.

Schwebke JR, Burgess D. Trichomoniasis. Clin Microbiol Rev 2004;17(4):794-803. doi:10.1128/CMR.17.4.794-803.2004.

Lockwood B1, North MJ, Scott KI, Bremner AF, Coombs GH. The use of a highly sensitive electophoretic method to compare the proteinases of trichomonads. Mol Biochem Parasitol 1987:24:89–95.

North M, Robertson CD, Coombs GH. The specificity of trichomonad proteinases analyzed using fluorogenic substrates and specific inhibitors. Mol Biochem Parasitol 1990; 39:183–194.

Garber GE, Lemchuk-Favel LT, Bowie WR. Isolation of a cell-detaching factor of Trichomonas vaginalis. J Clin Microbiol 1989;27:1548–1553.

Lushbaugh W, Turner AC, Gentry GA, Klykken PC. Characterization of a secreted cytoactive factor from Trichomonas vagina- lis. Am J Trop Med Hyg 1989;41:18–28.

Draper D, Donohoe W, Mortimer L, Heine RP. Cysteine proteases of Trichomonas vaginalis degrade secretory leukocyte protease inhibitor. J Infect Dis 1998;178:815–819.

Draper D, Landers DV, Krohn MA, Hillier SL, Wieseneld HC, Heine RP. Levels of vaginal secretory leukocyte protease inhibitor are decreased in women with lower reproductive tract infections. Am J Obstet Gynecol 2000;183:1243–1248.

Fiori P, Rappelli P, Rocchigiani A, Cappuc- cinelli P. Trichomonas vaginalis haemolysis: evidence of functional pores formation on red cell membranes. FEMS Microbiol Lett 1993;13–18.

Fiori P, Rappelli MF, Addis MF. The flagellated parasite Trichomonas vaginalis: new insights into cytopathogenicity mechanisms. Microb Pathog 1999;1:149–156.

Lubick K, Burgess DE. Purification and analysis of phospho-lipaseA2-like lytic fac- tor of Trichomonas vaginalis. Infect Immun 2004;72:1284–1290.

Graves KJ1, Ghosh AP, Kissinger PJ, Muzny CA. Trichomonas vaginalis virus: a review of the literature. Int J STD AIDS 2019;30(5):496-504.

Graves KJ2, Ghosh AP, Schmidt N, Au- gostini N, Secor WE, Schwebke JR, Mar- tin DH, Kissinger PJ, Muzny CA. Trichomonas vaginalis virus among women with trichomoniasis and associations with demographics, clinical outcomes, and metronidazole resistance. Clin Infect Dis 2019;69(12):2170-2176.

Wang AL1, Wang CC. The double-stranded RNA in Trichomonas vaginalis may origi- nate from virus-like particles. Proc Natl Acad Sci USA. 1986;83(20):7956-7960.

Wang AL, Wang CC. A linear double stranded RNA in Trichomonas vaginalis. J Biol Chem 1985;260(6):3697-3702.

Goodman RP, Ghabrial SA, Fichorova RN, Nibert ML. Trichomonasvirus: a new genus of protozoan viruses in the family Totiviri- dae. Arch Virol 2011; 156(1): 171–179.

Parent KN, Takagi Y, Cardone G, Olson NH, Ericsson M, Yang M, Lee Y, Asara JM, Fichorova RN, Baker TS, Nibert ML. Structure of a protozoan virus from the human genitourinary parasite Trichomonas vaginalis. mBio 2013;4(2):e00056-13.

Khoshnan A, Alderete JF. Trichomonas vaginalis with a double-stranded RNA virus has upregulated levels of phenotypically variable immunogen mRNA. J Virol 1994;68(6):4035-4038.

He D, Pengtao G, Ju Y, Jianhua L, He L, Guocai Z, Xichen Z. Differential protein expressions in virus Infected and uninfected Trichomonas vaginalis. Korean J Parasitol 2017;55(2):121-128.

Goodman RP2, Freret TS, Kula T, Geller AM, Talkington MW, Tang-Fernandez V, Suciu O, Demidenko AA, Ghabrial SA, Beach DH, Singh BN, Fichorova RN, Nibert ML. Clinical isolates of Trichomonas vaginalis concurrently infected by strains of up to four Trichomonasvirus species (Family Toti- viridae). J Virol 2011;85(9):4258-4270.

Bessarab IN, Nakajima R, Liu HW, Tai JH. Identification and characterization of a type III Trichomonas vaginalis virus in the protozoan pathogen Trichomonas vagina- lis. Arch Virol 2011;156(2):285-294.

Wendel KA, Rompalo AM, Erbelding EJ, Chang TH, Alderete JF. Double-stranded RNA viral infection of Trichomonas vaginalisinfecting patients attending a sexually transmitted diseases clinic. J Infect Dis 2002;186(4): 558–561.

Arroyo R, Alderete JF. Two Trichomonas vaginalis surface proteinases bind to host epithelial cells and are related to levels of cytoadherence and cytotoxicity. Arch Med Res 1995;26(3):279-285.

Wang AL, Wang CC, Alderete JF. Trichomo- nas vaginalis phenotypic variation occurs only among trichomonads infected with the double-stranded RNA virus. J Exp Med 1987;166(1):142-150.

Wang AL, Wang CC. Viruses of parasitic protozoa. Parasitol.Today 1991;7:76–80.

Malik SB, Pightling AW, StefaniakLM, Schurko AM, Logsdon JM. An expanded inventory of conserved meiotic genes provides evidence for sex in Trichomonas vaginalis. PLoS One 2008;3:e2879.

Khoshnan A, Alderete JF. Characterization of double-stranded RNA satellites associated with the Trichomonas vaginalis virus. J Virol 1995; 69:6892–6897.

Heidary S, Bandehpour M, Valadkhani Z, Seyyed-Tabaee S, Haghighi A, Abadi A, Ka- zemi B. Double-stranded RNA viral infection in Tehran Trichomonas vaginalis isolates. Iran J Parasitol 2013;8(1):60-64.

Lin WC, Chang WT, Chang TY, Shin JW. The pathogenesis of human cervical epithelium cells induced by interacting with Trichomonas vaginalis. PLoS One 2015 22;10(4):e0124087.

Twu O, de Miguel N, Lustig G, Stevens GC, Vashisht AA, Wohlschlegel JA, Johnson PJ. Trichomonas vaginalis exosomes deli- ver cargo to host cells and mediate hostratioparasite interactions. PLoS pathogens 2013; 9(7):e1003482.

Fichorova RN. Impact of T. vaginalis infection on innate immune responses and reproductive outcome. J Reprod Immunol 2009;83:185–189.

HAttaur Rahman, Harvey K, Siddiqui RA. Interleukin-8: an autocrine inflammatory mediator. Curr Pharm Des 1999;5:241–253.

O’Neil LA, Greene C. Signal transduction pathways activated by the IL -1 receptor fa- mily: ancient signaling machinery in mammals, insects and plants. J Leukoc Biol 1998;63:650–657.

Shaio MF1, Lin PR, Liu JY, Tang KD. Mo- nocyte-derived interleukin-8 involved in the recruitment of neutrophils induced by Trichomonas vaginalis infection. J Infect Dis 1994;170:1638–1640.

Shaio MF2, Lin PR, Liu JY, Yang KD. Generation of interleukin-8 from human monocytes in response to Trichomonas vaginalis stimula- tion. Infect Immun 1995;63:3864–3870.

Ryu JS, Kang JH, Jung SY, Shin MH, Kim JM, Park H, Min DY. Production of interleukin-8 by human neutrophils stimulated with Trichomonas vaginalis. Infect Immun. 2004;72:1326–1332.

Hitti, Hillier SL, Agnew KJ, Krohn MA, Reisner DP, Eschenback DA. Vaginal indicators of amniotic fluid infection in preterm labor. Obstet Gynecol 2001;97:211–219.

Soboll G, Shen L, Wira CR. Expression of Toll like receptors (TLR) and responsiveness to TLR agonists by polarized mouse uterine epithelial cells in culture. Biol Re- prod 2006;75:131–139.

Platz-Christensen JJ, IMattsby-Baltzer I, Thomsen P, Wiqvist N. Endotoxin and interleukin-1 alpha in the cervical mucus and vaginal fluid of pregnant women with bacterial vaginosis. Am J Obstet Gynecol 1993;169:1161–1166.

Caux C, Vanbervliet B, Massacrier C, Ait- Yahia S, Vaure C, Chemin K, Dieu-Nosjean MC, Vicari A. Regulation of dendritic cell recruitment by chemokines. Transplanta- tion 2002;73(S1):S7–S11.

Lekkerkerker AN, van Kooyk Y, Geijtenbeek TB. Viral piracy: HIV-1 targets dendritic cells for transmission. Curr HIV Res 2006;4(2):169-176.

Hoebe K, Janssen EM, KimSO, Alexopou- lou L, Flavell RA, Han J, Beutler B. Up regulation of co-stimulatory molecules induced by lipopolysaccharide and double- stranded RNA occurs by Trif-dependent and Trif-independent pathways. Nat Immunol 2003;4(12):1223-1229.

Burgess, D. Trichomonads and intestinal flagellates, In F. Cox, J. P. Krier, and D. Wakelin (ed.), Topley and Wilson’s microbiology and microbial infections, 9th ed. University Press, New York, N.Y. 1998; p. 203–214.

Mallinson DJ, Lockwood BC, Coombs GH, North MJ. Identification and molecular cloning of four cysteine proteinase genes from the pathogenic protozoon Trichomonas vaginalis. Microbiology 1994;140 (Pt 10):2725-2735.

Alderete JF, Arroyo R, Lehker MW. Analysis for adhesins and specific cytoadhesion of Trichomonas vaginalis. Methods Enzymol 1995;253:407-414.

Addis M 2, Rappelli, Pinto De Andrade AM, Rita FM, M. Colombo MM, Cappuc- cinelli P, Fiori PL. Identification of Tricho- monas vaginalis alpha-actinin as the mostt common immunogen recognized by sera of women exposed to the parasite. J Infect Dis 1999;180(5):1727-1730.

Wos SM, Watt RM. Immunoglobulin isoty- pes of anti-Trichomonas vaginalis antibodies in patients with vaginal trichomoniasis. J Clin Microbiol 1986;24(5):790-795.

Krieger JN, Ravdin JI, Rein MF. Contact- dependent cytopathogenic mechanisms of Trichomonas vaginalis. Infect Immun 1985;50(3):778-786.

Sutton M, Sternberg M, Koumans EH, McQuillan G, Berman S, Markowitz L. The prevalence of Trichomonas vaginalis infection among reproductive-age women in the United States, 2001-2004. Clin Infect Dis 2007;45(10):1319-1326.

Sena AC, Miller WC, Hobbs MM, Schwebke JR, Leone PA, Swygard H, Atashili J, Cohen MS. Trichomonas vaginalis infec- tion in male sexual partners: implications for diagnosis, treatment, and prevention. Clin Infect Dis 2007;44(1):13–22.

Wølner-Hanssen P, Krieger JN, Stevens CE, Kiviat NB, Koutsky L, Critchlow C, DeRouen T, Hillier S, Holmes KK. Clinical manifestations of vaginal trichomoniasis. JAMA 1989;261(4):571-576.

Lehker MW, Alderete JF. Biology of trichomonosis. Curr Opin Infect Dis 2000;13(1):37-45.

Swygard H, Seña AC, Hobbs MM, Cohen MS. Trichomoniasis: clinical manifestations, diagnosis and management. Sex Transm Infect 2004;80(2):91-95.

Lazenby GB, Soper DE, Nolte FS. Co- rrelation of leukorrhea and Trichomo- nas vaginalis infection. J Clin Microbiol 2013;51(7):2323-2327.

Silver BJ, Guy RJ, Kaldor JM, Jamil MS, Rumbold AR. Trichomonas vaginalis as a cause of perinatal morbidity: a systematic review and meta-analysis. Sex Transm Dis 2014;41(6):369-376.

Schwandt A, Williams C, Beigi RH. Perinatal transmission of Trichomonas vaginalis: a case report. J Reprod Med 2008; 53(1):59–61.

Carter JE, Whithaus KC. Neonatal respiratory tract involvement by Trichomonas vaginalis: a case report and review of the literature. Am J Trop Med Hyg 2008; 78(1):17–19.

Mann JR, McDermott S, Barnes TL, Har- din J, Bao H, Zhou L. Trichomoniasis in pregnancy and mental retardation in children. Ann Epidemiol 2009;19(12): 891-899.

Colotta F, Allavena P, Sica A, Garlanda C, Mantivani A. Cancer-related inflammation, the seventh hallmark of cancer: links to genetic instability. Carcinogenesis 2009;30:1073–1081.

Candido J, Hageman T. Cancer-related inflammation. J Clin Immunol,2013;33 (suppl. 1): S79–S84.

Costa A, Scholer-Dahirel A, Mecha-Grego- riou F. The role of reactive oxygen species and metabolism on cancer cells and their microenvironment. Semin Cancer Biol 2014;25: 23–32.

Parida S, Mandal M. Inflammation induced by human papillomavirus in cervical cancer and its implication in prevention. Eur J Cancer Prev 2014, 23(5):432–448.

Castle PE, Hillier SL, Rabe LK, Hildesheim A, Herrero R, Bratti MC, Sherman ME, Burk RD, Rodriguez AC, Alfaro M, Hutchinson ML, Morales J, Schiffman M. An association of cervical inflammation with high-grade cervical neoplasia in women infected with oncogenic human papillomavi- rus (HPV). Cancer Epidemiol Biomark Prev 2001;10(10):1021–1027.

Castle PE, Giuliano AR. Chapter 4: genital tract infections, cervical inflammation, and antioxidant nutrients–assessing their roles as human papillomavirus cofactors. J Natl Cancer Inst Monogr 2003;31:29–34.

Khatami M. ’Yin and Yang’ in inflammation: duality in innate immune cell function and tumorigenesis. Expert Opin Biol Ther 2008;8:1461–1472.

Thompson PA, Khatami M, Baglole CJ, Sun J, Harris SA, Moon EY, Al-Mulla F, Al- Temaimi R, Brown DG, Colacci A, Mon- dello C, Raju J, Ryan EP, Woodrick J, Sco- vassi AI, Singh N, Vaccari M, Roy R, Forte S, Memeo L, Salem HK, Amedei A, Hamid RA, Lowe L, Guarnieri T, Bisson WH. Environmental immune disruptors, inflammation and cancer risk. Carcinogenesis 2015;36(Suppl 1):S232-S253.

Fichorova RN, Lee Y, Yamamoto HS, Takagi Y, Hayes GR, Goodman RP, Chepa-Lotrea X, Buck OR, Murray R, Kula T, Beach DH, Singh BN, Nibert ML. Endobiont viruses sensed by the human host–beyond conventional antiparasitic therapy. PLoS One 2012;7:e48418.

International Agency for Research on Cancer. World Health Organization. Can- cer 2018 Reviewed on 2020, June 20. Avai- lable from: URL: https://gco.iarc.fr/today/ data/factsheets/populations/900-world- fact-sheets.pdf.

Pan-American Health Organization. Cán- cer Cervicouterino 2018. Reviewed on: 2020, June 20. Available from: URL:https:// www.paho.org/hq/index.php?option=com_ content&view=article&id=5420:2018-cer- vical-cancer&Itemid=3637&lang=es.

Núñez-Troconis J, Delgado M, González J, Mindiola R, Velásquez J, Conde B, Whitby D, Monroe DJ. Prevalence and risk factors of human papillomavirus infection in asymptomatic women in a Venezuelan urban area. Invest Clin 2009;50(2):203-212.

Vielot N, Hudgens MG, Mugo N, Chitwa M, Kimani J, Smith J. The Role of Chlamydia trachomatis in high-risk human papillomavirus persistence among female sex workers in Nairobi, Kenya. Sex Transm Dis 2015;42(6):305-311.

Ye H, Song T, Zeng X, Li L, Hou M, Xi M. Association between genital mycoplasmas infection and human papillomavirus in- fection, abnormal cervical cytopathology, and cervical cancer: a systematic review and metaanalysis. Arch Gynecol Obstet 2018;297(6):1377-1387.

Ghosh I, Mandal R, Kundu P, Biswas J. Association of genital infections other than human papillomavirus with pre Invasive and invasive cervical neoplasia. J Clin Diagn Res 2016;10(2):XE01-XE06.

IARC Working Group on the Evaluation of Carcinogenic Risk to Humans. Biological Agents. Lyon (FR): International Agency for Research on Cancer; 2012. (IARC Monographs on the Evaluation of Carcinogenic Risks to Humans, No. 100B.) Availa- ble from: https://www.ncbi.nlm.nih.gov/ books/ NBK304348/. Reviewed on July 22, 2020.

Schiffman MH, Castle P. Epidemiologic studies of a necessary causal risk factor: human papillomavirus infection and cervi- cal neoplasia. J Natl Cancer Inst 2003, 95:E2.

Scheurer ME, Tortolero-Luna G, Adler Storthz K. Human papillomavirus infection: biology, epidemiology, and prevention. Int J Gynecol Cancer 2005, 15:727-746.

Verteramo R1, Pierangeli A, Mancini E, Calzolari E, Bucci M, Osborn J, Nicosia R., Chiarini F, Antonelli G, Degener AM. Human papillomaviruses and genital coinfections in gynaecological outpatients. BMC Infect Dis 2009;9:16.

Múñoz N, Castellsague X, de Gonzalez AB, Gissmann L. HPV in the etiology of human cancer. Vaccine 2006; 24(S3):S1-S10.

Flores R, Papenfuss M, Klimecki WT, Giuliano AR. Cross-sectional analysis of oncogenic HPV viral load and cervical intraepithelial neoplasia. Int J Cancer 2006; 118(5):1187-1193.

Riva E, Serraino D, Pierangeli A, Bambacioni F, Zaniratti S, Minosse C, Selleri M, Bucci M, Scagnolari C, Degener AM, Capobianchi MR, Antonelli G, Dianzani F, the Roman Papillomavirus Study Group. Markers of human papillomavirus infection and their correlation with cervical dysplasia in human immunodeficiency virus-positive women. Clin Microbiol Infect 2007;13(1):94-97.

Clifford GM, Goncalves MA, Franceschi S, HPV and HIV Study Group. Human papillomavirus types among women infec- ted with HIV: a metaanalysis. AIDS 2006; 20(18):2337-2344.

Vaccarella S, Herrero R, Dai M, Snijders PJ, Meijer CJ, Thomas JO, Hoang Anh PT, Ferreccio C, Matos E, Posso H, de Sanjosé S, Shin HR, Sukvirach S, Lazcano-Ponce

E, Ronco G, Rajkumar R, Qiao YL, Muñoz N, Franceschi S. Reproductive factors, oral contraceptive use, and human papillomavirus infection: pooled analysis of the IARC HPV prevalence surveys. Cancer Epidemiol Biomarkers Prev 2006;15(11):2148-2153.

Vaccarella S, Franceschi S, Herrero R, Muñoz N, Snijders PJ, Clifford M, Smith JS, Lazcano-Ponce E, Sukvirach S, Shin HR, de Sanjosé S, Molano M, Matos E, Ferreccio C, Anh PT, Thomas JO, Meijer CJ, IARC HPV Prevalence Surveys Study Group. Sexual behavior, condom use, and human papillomavirus: pooled analysis of the IARC human papillomavirus prevalence surveys. Cancer Epidemiol Biomarkers Prev 2006;15(2):326-333.

Verteramo R, Pierangeli A, Calzolari E, Patella A, Recine N, Mancini E, Marcone V, Masciangelo R, Bucci M, Antonel- li G, Degener AM. Direct sequencing of HPV DNA detected in gynaecologic outpatients in Rome, Italy. Microbes Infect 2006; 8(10):2517-2521.

Lv P, Zhao F, Xu X, Xu J, Wang Q, Zhao Z. Correlation between common lower genital Ttract microbes and high-risk Human Papillomavirus infection. Can J Infect Dis Med Microbiol 2019;2019:9678104.

Noël JC, Fayt I, Romero Munoz MR, Simon P, Engohan-Aloghe C. High prevalence of high-risk human papillomavirus infection among women with Trichomonas vaginalis infection on monolayer cytology. Arch Gy- necol Obstet 2010; 282(5):503–505.

Thurman AR, Doncel GF. Innate immunity and inflammatory response to Trichomonas vaginalis and bacterial vaginosis: relations- hip to HIV acquisition. Am J Reprod Immu- nol 2011;65:89–98.

Hirt RP. Trichomonas vaginalis virulence factors: an integrative overview. Sex Transm Infect 2013;89:439-443.

Gram IT, Macaluso M, Churchill J, Stalsberg H. Trichomonas vaginalis (TV) and human papillomavirus (HPV) infection and the incidence of cervical intraepithelial neoplasia (CIN) grade III. Cancer Causes Control 1992;3(3):231-236.

Donders GG, Depuydt CE, Bogers JP, Vereecken AJ. Association of Trichomonas vaginalis and cytological abnormalities of the cervix in low risk women. PLoS One 2013;8(12):e86266.

Tao L, Han L, Li X, Gao Q, Pan L, Wu L, Luo Y, Wang W, Zheng Z, Guo X. Prevalence and risk factors for cervical neoplasia: a cervical cancer screening program in Bei- jing. BMC Public Health.2014;14:1185.

Depuydt CE, Leuridan E, Van Damme P, Bogers J, Vereecken AJ, Donders GG. Epi- demiology of Trichomonas vaginalis and human papillomavirus infection detected by real-time PCR in Flanders. Gynecol Obstet Invest 2010; 70(4):273–280.

Feng RM, Z Wang M, Smith JS, Dong L, Chen F, Pan QJ, Zhang x, Ciao YL, Zhao FH. Risk of high-risk human papillomavi- rus infection and cervical precancerous lesions with past or current trichomonas infection: a pooled analysis of 25,054 women in rural China. J Clin Virol 2018;99- 100:84-90.

Yap EH, Ho TH, Chan YC, Thong TW, Ng GC, Singh M. Serum antibodies to Trichomonas vaginalis in invasive cervical cancer patients. Genitourin Med 1995;71(6):402- 404.

Publicado
2021-02-23
Cómo citar
Núñez-Troconis, J. (2021). Trichomonas vaginalis: pathogenesis and its role in cervical.: Tricomonas vaginalis: patogénesis y su papel en el cáncer cervical. Investigación Clínica, 61(4), 349-375. https://doi.org/10.22209/IC.v61n4a05