Coinfection of bacterial endocervicitis and human papillomavirus in women of reproductive age
DOI:
https://doi.org/10.59255/mmed.2024.97Keywords:
Coinfection, Dysbiosis, HPV, Sexually transmitted infectionAbstract
Aim: To evaluate the coinfection rate between bacterial sexually transmitted infection (STI) and Human Papillomavirus (HPV) infection among reproductive-age women and identify risk factors associated with these infections. Methods: Five hundred and thirty reproductive-age women, HPV positive, who participated in a previous project about the persistence of Human Papillomavirus infection and cytokines profile were enrolled in this study. Vaginal samples were taken to classify vaginal microbiota by microscopy, according to appropriated scores. Endocervical samples were collected to assess the presence of infection by HPV. For HPV testing we used a manufacturing kit (Roche), then amplified a region of the L1 gene. The remaining endocervical secretion was used to determine Chlamydia trachomatis, Neisseria gonorrhoeae, and Mycoplasma genitalium infection rates. Results: Prevalence of HPV coinfection with C. trachomatis, N. gonorrhoeae, and M. genitalium was 14.2%, 1.2% and 1.4% respectively. About 42% of women had more than one type of HPV, 1.7% of women presented High-grade Squamous Intraepithelial Lesions (HSIL), and 5.3% presented Low-grade Squamous Intraepithelial Lesions (LSIL). Overall vaginal dysbiosis was 46%, and 34.9% of those had bacterial vaginosis. Abnormal vaginal microbiota was associated with C. trachomatis infection or high-risk HPV. Discussion/ Conclusions: A thorough assessment is crucial to provide a better comprehension of bacterial STIs in the presence of HPV. The overall HPV coinfection with C. trachomatis is high. The association of abnormal vaginal microbiota reinforces the importance of maintaining a dominated Lactobacilli spp. vaginal microbiota to protect against the acquisition of STIs, especially in HPV-infected women.
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References
Cervical Cancer. International Agency for Research on Cancer. World Health Organization: 2012.
Baudu A, Prétet JL, Riethmuller D, Chotard M, Mougin C, Mercier M. Prevalence and risk factors of human papillomavirus infection types 16/18/45 in a cohort of French females aged 15-23 years. J Epidemiol Glob Hea. 2014 Mar;4(1):35-43.
Koutsky L. Epidemiology of genital human papillomavirus infection. Am J Med. 1997 May 5;102(5A):3-8.
Plummer M, Schiffman M, Castle PE, Maucort-Boulch D, Wheeler CM. A 2- year prospective study of human papillomavirus persistence among women with a cytological diagnosis of atypical squamous cells of undetermined significance or low-grade squamous intraepithelial lesion. J Infect Dis. 2007 Jun 1;195(11):1582-9.
Walboomers JM, Jacobs MV, Manos MM, Bosch FX, Kummer JA, Shah KV, et al. Human papillomavirus is a necessary cause of invasive cervical cancer worldwide. J Pathol. 1999 Sep;189(1):12-9.
Wheeler CM. Natural history of human papillomavirus infections, cytologic and histologic abnormalities, and cancer. Obstet Gynecol Clin North Am. 2008 Dec;35(4):519-36; vii.
Cheong HC, Yap PSX, Chong CW, Cheok YY, Lee CYQ, Tan GMY, et al. Diversity of endocervical microbiota associated with genital Chlamydia trachomatis infection and infertility among women visiting obstetrics and gynecology clinics in Malaysia. PLoS One. 2019 Nov 18;14(11):e0224658.
Elwell C, Mirrashidi K, Engel J. Chlamydia cell biology and pathogenesis. Nat Rev Microbiol. 2016 Jun;14(6):385-400.
Cordova de Mendes MC, Cunha da Flório AR. Detecção de Mycoplasma genitalium, M. fermentans e M. penetrans em pacientes com sintomas de uretrite e em indivíduos infectados pelo HIV-1 no Brasil. J Bras Patol Med Lab. 2002;38(2):111-8.
Balkus JE, Manhart LE, Jensen JS, Anzala O, Kimani J, Schwebke J, et al. Mycoplasma genitalium Infection in Kenyan and US Women. Sex Transm Dis. 2018 Aug;45(8):514-21.
Quillin SJ, Seifert HS. Neisseria gonorrhoeae host adaptation and pathogenesis. Nat Rev Microbiol. 2018 Apr;16(4):226-40.
Liu Y, Zhang Y, Yang D, Xu C, Huang Y, Qing Q, et al. Chlamydia trachomatis and mycoplasma infections in tubal pregnancy. Sci Rep. 2019 Nov 4;9(1):15979.
Manhart LE, Critchlow CW, Holmes KK, Dutro SM, Eschenbach DA, Stevens CE, et al. Mucopurulent cervicitis and Mycoplasma genitalium. J Infect Dis. 2003 Feb 15;187(4):650-7.
Mobley VL, Hobbs MM, Lau K, Weinbaum BS, Getman DK, Seña AC. Mycoplasma genitalium infection in women attending a sexually transmitted infection clinic: diagnostic specimen type, coinfections, and predictors. Sex Transm Dis. 2012 Sep;39(9):706-9.
Murray RP, Rosenthal KS, Pfaller MA. Microbiologia médica. 8ª ed. Rio de Janeiro: Elsevier; 2016.
Kokkayil P, Dhawan B. Ureaplasma: current perspectives. Indian J Med Microbiol. 2015 Apr-Jun;33(2):205-14.
Borgdorff H, Tsivtsivadze E, Verhelst R, Marzorati M, Jurriaans S, Ndayisaba GF, et al. Lactobacillus-dominated cervicovaginal microbiota associated with reduced HIV/STI prevalence and genital HIV viral load in African women. ISME J. 2014 Sep;8(9):1781-93.
Marconi C, Duarte MT, Silva DC, Silva MG. Prevalence of and risk factors for bacterial vaginosis among women of reproductive age attending cervical screening in southeastern Brazil. Int J Gynaecol Obstet. 2015 Nov;131(2):137- 41.
Borgdorff H, van der Veer C, van Houdt R, Alberts CJ, de Vries HJ, Bruisten SM, et al. The association between ethnicity and vaginal microbiota composition in Amsterdam, the Netherlands. PLoS One. 2017 Jul 11;12(7):e0181135
Mermelstein, S., Plax, K. Sexually Transmitted Infections. Curr Treat Options Peds. 2016; 2:156-70.
Thoma ME, Brotman RM, Gray RH, Sewankambo NK, Wawer MJ. Risk and protective factors associated with BV chronicity among women in Rakai, Uganda. Sex Transm Infect. 2020 Aug;96(5):380-386.
Nugent RP, Krohn MA, Hillier SL. Reliability of diagnosing bacterial vaginosis is improved by a standardized method of gram stain interpretation. J Clin Microbiol. 1991 Feb;29(2):297–301.
Cibley LJ, Cibley LJ. Cytolytic vaginosis. Am J Obstet Gynecol. 1991 Oct;165(4 Pt 2):1245–9.
Donders GGG, Vereecken A, Bosmans E, Dekeersmacker A, Salembier G, Spitz B. Definition of a type of abnormal vaginal flora that is distinct from bacterial vaginosis: aerobic vaginitis. BJOG. 2002 Jan;109(1):34-43.
Moscicki AB, Schiffman M, Kjaer S, Villa LL. Chapter 5: Updating the natural history of HPV and anogenital cancer. Vaccine. 2006 Aug 31;24(3):S3/42-51.
Cuschieri KS, Cubie HA, Whitley MW, Gilkison G, Arends MJ, Graham C, et al. Persistent high risk HPV infection associated with development of cervical neoplasia in a prospective population study. J Clin Pathol. 2005 Sep;58(9):946- 50.
Machado LFA, Fonseca RRdS, Queiroz MAF, Oliveira-Filho AB, Cayres- Vallinoto IMV, Vallinoto ACR, et al. The epidemiological impact of STIs among general and vulnerable populations of the Amazon region of Brazil: 30 years of surveillance. Viruses. 2021 May;13(5):855.
Santos LM, Vieira MRM, Oliveira JFG, Trindade JQ, Brasiliense DM, Ferrari SF, et al. High prevalence of sexual Chlamydia trachomatis infection in young women from Marajó Island, in the Brazilian Amazon. PLoS One. 2018;13(12).
Departamento de Vigilância, Prevenção e Controle das IST, do HIV/Aids e das Hepatites Virais. Protocolo clínico e diretrizes terapêuticas para atenção integral às pessoas com infecções sexualmente transmissíveis (IST). [Internet]. Brasília: Ministério da Saúde; 2015. Disponível em: http://www.aids.gov.br/publicacao/2015/protocoloclinico-e-diretrizes- terapeuticas-para-atencao-integralpessoas-com-infecc. Acesso em: 02 jun 2017.
Witkin SS, Linhares I, Giraldo P, Jeremias J, Ledger WJ. Individual immunity and susceptibility to female genital tract infection. Am J Obstet Gynecol. 2000 Jul;183(1):252-6.
Jensen JS. Protocol for the detection of Mycoplasma genitalium by PCR from clinical specimens and subsequent detection of macrolide resistance-mediating mutations in region V of the 23S rRNA gene. Methods Mol Biol. 2012;903:129- 39.
Goire N, Nissen MD, LeCornec GM, Sloots TP, Whiley DM. A duplex Neisseria gonorrhoeae real-time polymerase chain reaction assay targeting the gonococcal porA pseudogene and multicopy opa genes. Diagn Microbiol Infect Dis. 2008 May;61(1):6-12.
Hong JH, Kim MK, Lee IH, Kim TJ, Kwak SH, Song SH, et al. Association between serum cytokine profiles and clearance or persistence of high-risk human papillomavirus infection: a prospective study. Int J Gynecol Cancer. 2010 Aug;20(6):1011-6.
Kops NL, Bessel M, Horvath JDC, Domingues C, de Souza FMA, Benzaken AS, et al. Factors associated with HPV and other self-reported STI coinfections among sexually active Brazilian young adults: cross-sectional nationwide study. BMJ Open. 2019 Jun 21;9(6):e027438.
Audirac-Chalifour A, Torres-Poveda K, Bahena-Román M, Téllez-Sosa J, Martínez-Barnetche J, Cortina-Ceballos B, et al. Cervical Microbiome and Cytokine Profile at Various Stages of Cervical Cancer: A Pilot Study. PLoS One. 2016 Apr 26;11(4):e0153274.
Anderson BL, Cu-Uvin S, Raker CA, Fitzsimmons C, Hillier SL. Subtle perturbations of genital microflora alter mucosal immunity among low-risk pregnant women. Acta Obstet Gynecol Scand. 2011 May;90(5):510-5.
Hedges SR, Barrientes F, Desmond RA, Schwebke JR. Local and systemic cytokine levels concerning changes in vaginal flora. J Infect Dis. 2006;193(4):556-62.
Holmes KK, Chen KC, Lipinski CM, Eschenbach DA. Vaginal redox potential in bacterial vaginosis (nonspecific vaginitis). J Infect Dis. 1985 Aug;152(2):379-82.
Mastromarino P, Di Pietro M, Schiavoni G, Nardis C, Gentile M, Sessa R. Effects of vaginal lactobacilli in Chlamydia trachomatis infection. Int J Med Microbiol. 2014 Jul;304(5-6):654-61.
Breshears LM, Edwards VL, Ravel J, Peterson ML. Lactobacillus crispatus inhibits growth of Gardnerella vaginalis and Neisseria gonorrhoeae on a porcine vaginal mucosa model. BMC Microbiol. 2015 Dec 9;15:276.
Gong Z, Luna Y, Yu P, Fan H. Lactobacilli inactivate Chlamydia trachomatis through lactic acid but not H2O2. PLoS One. 2014 Sep 12;9(9):e107758.
Graver MA, Wade JJ. The role of acidification in the inhibition of Neisseria gonorrhoeae by vaginal lactobacilli during anaerobic growth. Ann Clin Microbiol Antimicrob. 2011 Feb 17;10:8.
Linhares IM, Summers PR, Larsen B, Giraldo PC, Witkin SS. Contemporary perspectives on vaginal pH and lactobacilli. Am J Obstet Gynecol. 2011 Feb;204(2):120.e1-5.
Marconi C, Santos-Greatti MM, Parada CM, Pontes A, Pontes AG, Giraldo PC, et al. Cervicovaginal levels of proinflammatory cytokines are increased during chlamydial infection in bacterial vaginosis but not in lactobacilli-dominated flora. J Low Genit Tract Dis. 2014 Jul;18(3):261-5.
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Copyright (c) 2024 Jeniffer Sena Baptista Ferreira, Bruna Ribeiro de Andrade Ramos, Gabriel Vitor da Silva Pinto, Aline do Nascimento Bolpet, Jossimara Polettini, Mariana de Castro Silva, Luciana Souza Jorge, Lucas Tadeu Bidinotto, Márcia Guimarães da Silva
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