Abstract
Objectives
Human papillomavirus (HPV) and chlamydia trachomatis (Ct) infection lead to severe consequences for women’s health. This meta-analysis summarizes the evidence on HPV infection risk in women with chlamydia and chlamydia risk in HPV-positive women.
Methods
Medline, Web of Science and Scopus were systematically searched for eligible publications until May 2018. Eligibility criteria included: assessment of HPV/Ct infection; cohort, case–control, cross-sectional study design; and reported risk estimation with its 95% CI for HPV infection in Ct-positive women and/or Ct infection in HPV-positive women. On the PRISMA guidelines, meta-analysis was performed using random effect model.
Results
Forty-eight studies met the eligibility criteria. Among women with chlamydia, the odds ratio (OR) of HPV infection is 2.12 (95% CI 1.80, 2.49) and the OR of high-risk HPV infection is 2.32 (95% CI 2.02, 2.65). The OR for chlamydia among HPV-positive women is 2.23 (95% CI 1.70, 2.92).
Conclusions
HPV and Ct behave as reciprocal risk factors. In women diagnosed with HPV infection or chlamydia, the screening for the mutual infection could represent a preventive intervention for severe reproductive health outcomes, such as cervical cancer and infertility.
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References
Aghaizu A, Reid F, Kerry S, Hay P, Mallinson H, Jensen JS, Kerry S, Kerry S, Oakeshott P (2014) Frequency and risk factors for incident and redetected chlamydia trachomatis infection in sexually active, young, multi-ethnic women: a community based cohort study. Sex Transm Infect 90(7):524–528. https://doi.org/10.1136/sextrans-2014-051607
Aral SO (2004) Sexual risk behaviour and infection: epidemiological considerations. Sex Transm Infect 80(SUPPL. 2):8–12. https://doi.org/10.1136/sti.2004.011866
Baldwin SB, Djambazov B, Papenfuss M, Abrahamsen M, Denman C, Guernsey de Zapien J, Ortega L, Navarro Henze JL, Hunter J, Rojas M, García F, Giuliano AR (2004) Chlamydial infection in women along the US-Mexico border. Int J STD AIDS 15(12):815–821. https://doi.org/10.1258/0956462042563792
Barrow-laing L, Chen W, Roman A (2011) Low- and high-risk human papillomavirus E7 proteins regulate P130 differently. Virology 400(2):233–239. https://doi.org/10.1016/j.virol.2010.01.034.Low-
Begg CB, Mazumdar M (1994) Operating Characteristics of a rank correlation test for publication bias. Biometrics 50(4):1088–1101
Boardman LA, Stanko C, Weitzen S, Sung CJ (2005) Atypical squamous cells of undetermined significance: human papillomavirus testing in adolescents. Obstet Gynecol 105(4):741–746. https://doi.org/10.1097/01.AOG.0000157126.12678.a6
Bosch FX, Burchell AN, Schiffman M, Giuliano AR, de Sanjose S, Bruni L, Tortolero-Luna G, Kjaer SK, Muñoz N (2008) Epidemiology and natural history of human papillomavirus infections and type-specific implications in cervical neoplasia. Vaccine 26(Suppl 10):K1–K16. https://doi.org/10.1016/j.vaccine.2008.05.064
Bosch FX, Broker TR, Forman D, Moscicki AB, Gillison ML, Doorbar J, Stern PL, Stanley M, Arbyn M, Poljak M, Cuzick J, Castle PE, Schiller JT, Markowitz LE, Fisher WA, Canfell K, Denny LA, Franco EL, Steben M, Kane MA, Schiffman M, MeijerCJ Sankaranarayanan R, Castellsagué X, Kim JJ, Brotons M, Alemany L, Albero G, Diaz M, de Sanjosé S, Authors of the ICO Monograph (2013) Comprehensive control of human papillomavirus infections and related diseases. Vaccine 31(Suppl 8):I1–I31. https://doi.org/10.1016/j.vaccine.2013.07.026
Bruni L, Diaz M, Castellsague X, Ferrer E, Bosch FX, De Sanjose S (2010) Cervical human papillomavirus prevalence in 5 continents: meta-analysis of 1 million women with normal cytological findings. J Infect Dis 202(12):1789–1799. https://doi.org/10.1086/657321
Canfell K, Chesson H, Kulasingam SL, Berkhof J, Diaz M, Kim JJ (2013) Modeling preventative strategies against HPV-related disease in developed countries. Vaccine 30(Suppl 5):F157–F167. https://doi.org/10.1016/j.vaccine.2012.06.091
Castanon A, Landy R, Pesola F, Windridge P, Sasieni P (2018) Prediction of cervical cancer incidence in England, UK, up to 2040, under four scenarios: a modelling study. Lancet Public Health 3(1):e34–e43. https://doi.org/10.1016/S2468-2667(17)30222-0
Castellsagué X, Paavonen J, Jaisamrarn U, Wheeler CM, Skinner SR, Lehtinen M, Naud P, Chow SN, Del Rosario-Raymundo MR, Teixeira JC, Palmroth J, de Carvalho NS, Germar MJ, Peters K, Garland SM, Szarewski A, Poppe WA, Romanowski B, Schwarz TF, Tjalma WA, Bosch FX, Bozonnat MC, Struyf F, Dubin G, Rosillon D, Baril L, HPV PATRICIA Study Group (2014) Risk of first cervical HPV infection and pre-cancerous lesions after onset of sexual activity: analysis of women in the control arm of the randomized, controlled PATRICIA trial. BMC Infect Dis. https://doi.org/10.1186/s12879-014-0551-y
Cates W Jr, Wasserheit JN (1991) Genital chlamydial infections: epidemiology and reproductive sequelae. Am J Obstet Gynecol 164(6):1771–1781. https://doi.org/10.1016/0002-9378(91)90559-A
CDC (2017) Sexually transmitted disease surveillance 2017. U.S. Department of Health and Human Services, Atlanta
Conde-Ferráez L, Martiez JR, Ayora-Talavera G, Losa MD (2017) Human papillomavirus and chlamydia trachomatis infection in gyneco-obstetric outpatients from a Mexican hospital. Indian J Med Microbiol 35(1):74–79. https://doi.org/10.4103/ijmm.IJMM_15_450
da Silva CS, Adad SJ, Hazarabedian de Souza MA, Macêdo Barcelos AC, Sarreta Terra AP, Murta EF (2004) Increased frequency of bacterial vaginosis and chlamydia trachomatis in pregnant women with human papillomavirus infection. Gynecol Obstet Invest 58(4):189–193. https://doi.org/10.1159/000079822
Denks K, Spaeth EL, Jõers K, Randoja R, Talpsep T, Ustav M, Kurg R (2007) Coinfection of chlamydia trachomatis, ureaplasma urealyticum and human papillomavirus among patients attending STD clinics in estonia. Scand J Infect Dis 39(8):714–718. https://doi.org/10.1080/00365540701199824
Dong Y, Sasagawa T, Fang S, Yamazaki H, Sakaike J, Jiang A, Song L, Gou M, Inoue M (1998) Human papillomavirus, chlamydia trachomatis, and other risk factors associated with cervical cancer in China. Int J Clin Oncol 3(2):81–87. https://doi.org/10.1007/BF02492852
Donken R, Tami A, Knol MJ, Lubbers K, van der Sande MAB, Nijman HW, Daemen T, Weijmar Schultz WCM, de Melker HE (2018) Changes in (risk) behavior and HPV knowledge among Dutch girls eligible for HPV vaccination: an observational cohort study. BMC Public Health 18(1):837. https://doi.org/10.1186/s12889-018-5745-6
Doorbar J, Quint W, Banks L, Bravo IG, Stoler M, Broker TR, Stanley MA (2012) The biology and life-cycle of human papillomaviruses. Vaccine 30(Suppl 5):F55–F70. https://doi.org/10.1016/j.vaccine.2012.06.083
Dunne EF, Sternberg M, Markowitz LE, McQuillan G, Swan D, Patel S, Unger ER (2011) Prevalence among females in the United States—National Health and Nutrition Examination Survey, 2003–2006: Opportunity to measure HPV vaccine impact? J Infect Dis 204(4):562–565. https://doi.org/10.1093/infdis/jir342
Egawa N, Doorbar J (2017) The low-risk papillomaviruses. Virus Res 231:119–127. https://doi.org/10.1016/j.virusres.2016.12.017
Egger M, Davey Smith G, Schneider M, Minder C (1997) Bias in meta-analysis detected by a simple, Graphical Test. BMJ 315(7109):629–634
Enthumathi R, Shanmughapriya S, Sumathi S, Das BC, Natarajaseenivasan K (2015) Prevalence of human papillomavirus, cytomegalovirus and chlamydia trachomatis among women with normal cervical cytology and their impact on TLRs expression. Res J Obstet Gynecol 8(1):1–9. https://doi.org/10.3923/rjog.2015.1.9
Ezzati M, Lopez AD, Rodgers A, Vander Hoorn S, Murray CJ, Comparative Risk Assessment Collaborating Group (2002) Selected major risk factors and global and regional burden of disease. Lancet 360(9343):1347–1360. https://doi.org/10.1016/S0140-6736(02)11403-6
Finan RR, Musharrafieh U, Almawi WY (2006) Detection of chlamydia trachomatis and herpes simplex virus type 1 or 2 in cervical samples in human papilloma virus (HPV)-positive and HPV-negative women. Clin Microbiol Infect 12(9):927–930. https://doi.org/10.1111/j.1469-0691.2006.01479.x
Fogue P, Djeudong G, Bouting G, Aglago E, Simo G, Lueong S (2018) Molecular characterization of lower vaginal swabs for human papilloma virus in association with chlamydia trachomatis infection in cameroonian women. J Infect Public Health 11(3):314–320. https://doi.org/10.1016/j.jiph.2017.08.010
Franceschi S, Smith JS, van den Brule A, Herrero R, Arslan A, Anh PT, Bosch FX, Hieu NT, Matos E, Posso H, Qiao YL, Shin HR, Sukvirach S, Thomas JO, Snijders PJ, Muñoz N, Meijer CJ (2007) Cervical infection with chlamydia trachomatis and Neisseria gonorrhoeae in women from ten areas in four continents: a cross-sectional study. Sex Transm Dis 34(8):563–569. https://doi.org/10.1097/01.olq.0000258417.66619.0e
GBD 2015 Disease and Injury Incidence and Prevalence Collaborators (2016) Global, regional, and national incidence, prevalence, and years lived with disability for 310 diseases and injuries, 1990–2015: a systematic analysis for the global burden of disease study 2015. Lancet 388(10053):1545–1602. https://doi.org/10.1016/S0140-6736(16)31678-6 (Erratum. In: Lancet. 2017 Jan 7;389(10064):e1)
Giuliano AR, Papenfuss M, Abrahamsen M, Denman C, de Zapien JG, Henze JL, Ortega L, Brown de Galaz EM, Stephan J, Feng J, Baldwin S, Garcia F, Hatch K (2001) Human papillomavirus infection at the United States-Mexico border: implications for cervical cancer prevention and control. Cancer Epidemiol Biomarkers Prev 10(11):1129–1136
Giuliano AR, Papenfuss M, Abrahamsen M, Inserra P (2002) Differences in factors associated with oncogenic and nononcogenic human papillomavirus infection at the United States-Mexico border. Cancer Epidemiol Biomarkers Prev 11(9):930–934
Golijow CD, Abba MC, Mourón SA, Laguens RM, Dulout FN, Smith JS (2005) Chlamydia trachomatis and human papillomavirus infections in cervical disease in Argentine women. Gynecol Oncol 96(1):181–186. https://doi.org/10.1016/j.ygyno.2004.09.037
Grandahl M, Larsson M, Dalianis T, Stenhammar C, Tydén T, Westerling R, Nevéus T (2017) Catch-up HPV vaccination status of adolescents in relation to socioeconomic factors, individual beliefs and sexual behaviour. PLoS ONE 12(11):e0187193. https://doi.org/10.1371/journal.pone.0187193
Gravitt PE (2011) The known unknowns of HPV natural history. J Clin Invest 121(12):4593–4599. https://doi.org/10.1172/JCI57149
Haggerty CL, Gottlieb SL, Taylor BD, Low N, Xu F, Ness RB (2010) Risk of sequelae after chlamydia trachomatis genital infection in women. J Infect Dis 201(S2):134–155. https://doi.org/10.1086/652395
Harder E, Thomsen LT, Frederiksen K, Munk C, Iftner T, van den Brule A, Kjaer SK (2016) Risk factors for incident and redetected chlamydia trachomatis infection in women: results of a population-based cohort study. Sex Transm Dis 43(2):113–119. https://doi.org/10.1097/OLQ.0000000000000394
Hasan UA, Bates E, Takeshita F, Biliato A, Accardi R, Bouvard V, Mansour M, Vincent I, Gissmann L, Iftner T, Sideri M, Stubenrauch F, Tommasino M (2007) TLR9 expression and function is abolished by the cervical cancer-associated human papillomavirus type 16. J Immunol 178(5):3186–3197. https://doi.org/10.4049/jimmunol.178.5.3186
Hestbech MS, Gyrd-Hansen D, Kragstrup J, Siersma V, Brodersen J (2016) How does HPV vaccination status relate to risk perceptions and intention to participate in cervical screening? A Survey Study. BMC Public Health 15:708. https://doi.org/10.1186/s12889-016-3397-y
Hoffman SR, Le T, Lockhart A, Sanusi A, Dal Santo L, Davis M, McKinney DA, Brown M, Poole C, Willame C, Smith JS (2017) Patterns of persistent HPV infection after treatment for cervical intraepithelial neoplasia (CIN): a systematic review. Int J Cancer 141(1):8–23. https://doi.org/10.1002/ijc.30623
Hwang LY, Ma Y, Moscicki AB (2014) Biological and behavioral risks for incident chlamydia trachomatis infection in a prospective cohort. Obstet Gynecol 124(5):954–960. https://doi.org/10.1097/AOG.0000000000000429
IARC (1995) IARC monographs on the evaluation of the carcinogenic risk to humans. Human papillomavirus 64:409
IARC (2012) Biological agents. IARC monographs on the evaluation of carcinogenic risks to humans, vol 100B. International Agency for Research on Cancer, Lyon (FR), pp 1–443
Imai H, Nakao H, Shinohara H, Watarai M, Matsumoto N, Yamagishi T, Saito M, Kitamura T (2015) Prevalence, potential predictors, and genotype-specific prevalence of human papillomavirus infection among sexually active students in Japan. PLoS ONE 10(7):e0132462. https://doi.org/10.1371/journal.pone.0132462
Ioannidis JP, Patsopoulos NA, Evangelou E (2007) Uncertainty in heterogeneity estimates in meta-analyses. BMJ 335(7626):914–916. https://doi.org/10.1136/bmj.39343.408449.80
Jamison JH, Kaplan DW, Hamman R, Eagar R, Beach R, Douglas JM Jr (1995) Spectrum of genital human papillomavirus infection in a female adolescent population. Sex Transm Dis 22(4):236–243
Jena AB, Goldman DP, Seabury SA (2016) Incidence of sexually transmitted infections after human papillomavirus vaccination among adolescent females. JAMA Intern Med 175(4):617–623. https://doi.org/10.1001/jamainternmed.2014.7886
Kanodia S, Fahey LM, Kast WM (2007) Mechanisms used by human papillomaviruses to escape the host immune response. Curr Cancer Drug Targets 7(1):79–89. https://doi.org/10.2174/156800907780006869
Karlsson R, Jonsson M, Edlund K, Evander M, Gustavsson A, Bodén E, Rylander E, Wadell G (1995) Lifetime number of partners as the only independent risk factor for human papillomavirus infection: a population-based study. Sex Transm Dis 22(2):119–127
Kim S, Arduino JM, Roberts CC, Marsico M, Liaw KL, Skjeldestad FE (2011) Incidence and predictors of human papillomavirus-6, -11, -16, and -18 infection in young Norwegian women. Sex Transm Dis 38(7):587–597. https://doi.org/10.1097/OLQ.0b013e31820a9324
Kim HS, Kim TJ, Lee IH, Hong SR (2016) Associations between sexually transmitted infections, high-risk human papillomavirus infection, and abnormal cervical pap smear results in OB/GYN outpatients. J Gynecol Oncol 27(5):e49. https://doi.org/10.3802/jgo.2016.27.e49
Kjaer SK, van den Brule AJ, Bock JE, Poll PA, Engholm G, Sherman ME, Walboomers JM, Meijer CJ (1997) Determinants for genital human papillomavirus (HPV) infection in 1000 randomly chosen young Danish women with normal pap smear: Are there different risk profiles for oncogenic and nononcogenic HPV types? Cancer Epidemiol Biomarkers Prev 6(10):799–805
Liu J, Liu W, Liu Y, Zhou X, Zhang Z, Sun Z (2016) Prevalence of microorganisms co-infections in human papillomaviruses infected women in Northern China. Arch Gynecol Obstet 293(3):595–602. https://doi.org/10.1007/s00404-015-3826-7
Magaña-Contreras M, Contreras-Paredes A, Chavez-Blanco A, Lizano M, De la Cruz-Hernandez Y, De la Cruz-Hernandez E (2015) Prevalence of sexually transmitted pathogens associated with HPV infection in cervical samples in a Mexican population. J Med Virol 87(12):2098–2105. https://doi.org/10.1002/jmv.24278
Man S, Fiander A (2001) Immunology of human papillomavirus infection in lower genital tract neoplasia. Best Pract Res Clin Obstet Gynaecol 15(5):701–714. https://doi.org/10.1053/beog.2001.0215
Marcone V, Recine N, Gallinelli C, Nicosia R, Lichtner M, Degener AM, Chiarini F, Calzolari E, Vullo V (2012) Epidemiology of chlamydia trachomatis endocervical infection in a previously unscreened population in Rome, Italy, 2000 to 2009. Euro Surveill. https://doi.org/10.2807/ese.17.25.20203-en
Marshall BD, Kerr T, Shoveller JA, Montaner JS, Wood E (2009) Structural factors associated with an increased risk of HIV and sexually transmitted infection transmission among street-involved youth. BMC Public Health 9:7. https://doi.org/10.1186/1471-2458-9-7
Mayaud P, Mabey D (2004) Approaches to the control of sexually transmitted infections in developing countries: old problems and modern challenges. Sex Transm Infect 80(3):174–182. https://doi.org/10.1136/sti.2002.004101
Medina-Perucha L, Family H, Scott J, Chapman S, Dack C (2018) Factors associated with sexual risks and risk of STIs, HIV and other blood-borne viruses among women using heroin and other drugs: a systematic literature review. AIDS Behav 23(1):222–251. https://doi.org/10.1007/s10461-018-2238-7
Middleton K, Peh W, Southern S, Griffin H, Sotlar K, Nakahara T, El-Sherif A, Morris L, Seth R, Hibma M, Jenkins D, Lambert P, Coleman N, Doorbar J (2003) Organization of human papillomavirus productive cycle during neoplastic progression provides a basis for selection of diagnostic markers. J Virol 77(19):10186–10201. https://doi.org/10.1128/JVI.77.19.10186
Moher D, Liberati A, Tetzlaff J, Altman DG; PRISMA Group (2009) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med 6(7):e1000097. https://doi.org/10.1371/journal.pmed.1000097
Molano M, Weiderpass E, Posso H, Morré SA, Ronderos M, Franceschi S, Arslan A, Meijer CJ, Muñoz N, van den Brule AJ, HPV Study Group (2003) Prevalence and determinants of chlamydia trachomatis infections in women from Bogota, Colombia. Sex Transm Infect 79(6):474–478. https://doi.org/10.1136/sti.79.6.474
Muñoz N, Kato I, Bosch FX, Eluf-Neto J, De Sanjosé S, Ascunce N, Gili M, Izarzugaza I, Viladiu P, Tormo MJ, Moreo P, Gonzalez LC, Tafur L, Walboomers JM, Shah KV (1996) Risk factors for HPV DNA detection in middle-aged women. Sex Transm Dis 23(6):504–510
Newman L, Rowley J, Vander Hoorn S, Wijesooriya NS, Unemo M, Low N, Stevens G, Gottlieb S, Kiarie J, Temmerman M (2015) Global estimates of the prevalence and incidence of four curable sexually transmitted infections in 2012 based on systematic review and global reporting. PLoS ONE 10(12):e0143304. https://doi.org/10.1371/journal.pone.0143304
Nonato DR, Alves RR, Ribeiro AA, Saddi VA, Segati KD, Almeida KP, de Lima YA, D’Alessandro WB, Rabelo-Santos SH (2016) Prevalence and factors associated with coinfection of human papillomavirus and chlamydia trachomatis in adolescents and young women. Am J Obstet Gynecol 215(6):753.e1–753.e9. https://doi.org/10.1016/j.ajog.2016.07.003
Oakeshott P, Aghaizu A, Reid F, Howell-Jones R, Hay PE, Sadiq ST, Lacey CJ, Beddows S, Soldan K (2012) Frequency and risk factors for prevalent, incident, and persistent genital carcinogenic human papillomavirus infection in sexually active women: community based cohort study. BMJ 344:e4168. https://doi.org/10.1136/bmj.e4168
Oh JK, Franceschi S, Kim BK, Kim JY, Ju YH, Hong EK, Chang YC, Rha SH, Kim HH, Kim JH, Kim CY, Shin HR (2009) Prevalence of human papillomavirus and chlamydia trachomatis infection among women attending cervical cancer screening in the Republic of Korea. Eur J Cancer Prev 18(1):56–61. https://doi.org/10.1097/CEJ.0b013e328305a0a6
Paavonen J (2012) Chlamydia trachomatis infections of the female genital tract: state of the art. Ann Med 44(1):18–28. https://doi.org/10.3109/07853890.2010.546365
Paba P, Bonifacio D, Di Bonito L, Ombres D, Favalli C, Syrjänen K, Ciotti M (2008) Co-expression of HSV2 and chlamydia trachomatis in HPV-positive cervical cancer and cervical intraepithelial neoplasia lesions is associated with aberrations in key intracellular pathways. Intervirology 51(4):230–234. https://doi.org/10.1159/000156481
Panatto D, Amicizia D, Bianchi S, Frati ER, Zotti CM, Lai PL, Domnich A, Colzani D, Gasparini R, Tanzi E (2015) Chlamydia trachomatis prevalence and chlamydial/HPV Co-infection among HPV-unvaccinated young Italian females with normal cytology. Hum Vaccines Immunother 11(1):270–276. https://doi.org/10.4161/hv.36163
Pereira SM, Etlinger D, Aguiar LS, Peres SV, Longatto Filho A (2010) Simultaneous chlamydia trachomatis and HPV infection in pregnant women. Diagn Cytopathol 38(6):397–401. https://doi.org/10.1002/dc.21219
Quinónez-Calvache EM, Ríos-Chaparro DI, Ramírez JD, Soto-De León SC, Camargo M, Del Río-Ospina L, Sánchez R, Patarroyo ME, Patarroyo MA (2016) Chlamydia trachomatis frequency in a cohort of HPV-infected Colombian women. PLoS ONE 11(1):e0147504. https://doi.org/10.1371/journal.pone.0147504
Roset Bahmanyar E, Paavonen J, Naud P, Salmerón J, Chow SN, Apter D, Kitchener H, Castellsagué X, Teixeira JC, Skinner SR, Jaisamrarn U, Limson GA, Garland SM, Szarewski A, Romanowski B, Aoki F, Schwarz TF, Poppe WA, De Carvalho NS, Harper DM, Bosch FX, Raillard A, Descamps D, Struyf F, Lehtinen M, Dubin G, HPV PATRICIA Study Group (2012) Prevalence and risk factors for cervical HPV infection and abnormalities in young adult women at enrolment in the multinational PATRICIA trial. Gynecol Oncol 127(3):440–450. https://doi.org/10.1016/j.ygyno.2012.08.033
Rositch AF, Koshiol J, Hudgens MG, Razzaghi H, Backes DM, Pimenta JM, Franco EL, Poole C, Smith JS (2014) Patterns of persisten genital human papillomavirus infection among women worldwide: a literature review and meta-analysis. Int J Cancer 133(6):1271–1285. https://doi.org/10.1002/ijc.27828
Rours GI, Duijts L, Moll HA, Arends LR, de Groot R, Jaddoe VW, Hofman A, Steegers EA, Mackenbach JP, Ott A, Willemse HF, van der Zwaan EA, Verkooijen RP, Verbrugh HA (2011) Chlamydia trachomatis infection during pregnancy associated with preterm delivery: a population-based prospective cohort study. Eur J Epidemiol 26(6):493–502. https://doi.org/10.1007/s10654-011-9586-1
Safaeian M, Quint K, Schiffman M, Rodriguez AC, Wacholder S, Herrero R, Hildesheim A, Viscidi RP, Quint W, Burk RD (2010) Chlamydia trachomatis and risk of prevalent and incident cervical premalignancy in a population-based cohort. J Natl Cancer Inst 102(23):1794–1804. https://doi.org/10.1093/jnci/djq436
Satterwhite CL, Torrone E, Meites E, Dunne EF, Mahajan R, Ocfemia MC, Su J, Xu F, Weinstock H (2013) Sexually transmitted infections among US women and men: prevalence and incidence estimates, 2008. Sex Transm Dis 40(3):187–193. https://doi.org/10.1097/OLQ.0b013e318286bb53
Schiffman M, Castle PE, Jeronimo J, Rodriguez AC, Wacholder S (2007) Human papillomavirus and cervical cancer. Lancet 370(9590):890–907. https://doi.org/10.1016/S0140-6736(07)61416-0
Schiffman M, Doorbar J, Wentzensen N, de Sanjosé S, Fakhry C, Monk BJ, Stanley MA, Franceschi S (2016) Carcinogenic human papillomavirus infection. Nat Rev Dis Primers 2:16086. https://doi.org/10.1038/nrdp.2016.86
Seth P, Wingood GM, Robinson LS, Diclemente RJ (2009) Exposure to high-risk genital human papillomavirus and its association with risky sexual practices and laboratory-confirmed chlamydia among African–American women. Women’s Health Issues 19(5):344–351. https://doi.org/10.1016/j.whi.2009.06.001
Sharma M, Bruni L, Diaz M, Castellsagué X, de Sanjosé S, Bosch FX, Kim JJ (2013) Using HPV prevalence to predict cervical cancer incidence. Int J Cancer 132(8):1895–1900. https://doi.org/10.1002/ijc.27835
Shaskolskiy B, Dementieva E, Leinsoo A, Runina A, Vorobyev D, Plakhova X, Kubanov A, Deryabin D, Gryadunov D (2016) Drug resistance mechanisms in bacteria causing sexually transmitted diseases and associated with vaginosis. Front Microbiol 7:747. https://doi.org/10.3389/fmicb.2016.00747
Silva J, Cerqueira F, Ribeiro J, Sousa H, Osório T, Medeiros R (2013) Is chlamydia trachomatis related to human papillomavirus infection in young women of Southern European population? A self-sampling study. Arch Gynecol Obstet 288(3):627–633. https://doi.org/10.1007/s00404-013-2771-6
Silva J, Cerqueira F, Medeiros R (2014) Chlamydia trachomatis infection: implications for HPV status and cervical cancer. Arch Gynecol Obstet 289(4):715–723. https://doi.org/10.1007/s00404-013-3122-3
Simonetti AC, Melo JH, de Souza PR, Bruneska D, de Lima Filho JL (2009) Immunological’s host profile for HPV and chlamydia trachomatis, a cervical cancer cofactor. Microbes Infect 11(4):435–442. https://doi.org/10.1016/j.micinf.2009.01.004
Stanley MA (2012) Epithelial cell responses to infection with human papillomavirus. Clin Microbiol Rev 25(2):215–222. https://doi.org/10.1128/CMR.05028-11
Steben M, Jeronimo J, Wittet S, Lamontagne DS, Ogilvie G, Jensen C, Smith J, Franceschi S (2012) Upgrading public health programs for human papillomavirus prevention and control is possible in low- and middle-income countries. Vaccine 30(Suppl 5):F183–F191. https://doi.org/10.1016/j.vaccine.2012.06.031
Stroup DF, Berlin JA, Morton SC, Olkin I, Williamson GD, Rennie D, Moher D, Becker BJ, Sipe TA, Thacker SB (2000) Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis of observational studies in epidemiology (MOOSE) group. JAMA 283(15):2008–2012. https://doi.org/10.1001/jama.283.15.2008
Tábora N, Zelaya A, Bakkers J, Melchers WJ, Ferrera A (2005) Chlamydia trachomatis and genital human papillomavirus infections in female university students in Honduras. Am J Trop Med Hyg 73(1):50–53. https://doi.org/10.4269/ajtmh.2005.73.1.0730050
Tamim H, Finan RR, Sharida HE, Rashid M, Almawi WY (2002) Cervicovaginal coinfections with human papillomavirus and chlamydia trachomatis. Diagn Microbiol Infect Dis 43(4):277–281. https://doi.org/10.1016/S0732-8893(02)00403-0
Tjiong MY, Out TA, Ter Schegget J, Burger MP, Van Der Vange N (2001) Epidemiologic and mucosal immunologic aspects of HPV infection and HPV-related cervical neoplasia in the lower female genital tract: a review. Int J Gynecol Cancer 11(1):9–17. https://doi.org/10.1046/j.1525-1438.2001.011001009.x
Joint United Nations Programme on HIV/AIDS (1998) The Public Health Approach to STD Control (Best Practice-Technical Update). UNAIDS
Unemo M, Bradshaw CS, Hocking JS, de Vries HJC, Francis SC, Mabey D, Marrazzo JM, Sonder GJB, Schwebke JR, Hoornenborg E, Peeling RW, Philip SS, Low N, Fairley CK (2017) Sexually transmitted infections: challenges ahead. Lancet Infect Dis 17(8):e235–e279. https://doi.org/10.1016/S1473-3099(17)30310-9
Vaccarella S, Franceschi S, Zaridze D, Poljak M, Veerus P, Plummer M, Bray F (2016) Preventable fractions of cervical cancer via effective screening in six Baltic, Central, and Eastern European Countries 2017-40: a population-based study. Lancet Oncol 17(10):1445–1452. https://doi.org/10.1016/S1470-2045(16)30275-3
Vázquez-Otero C, Thompson EL, Daley EM, Griner SB, Logan R, Vamos CA (2016) Dispelling the myth: exploring associations between the HPV vaccine and inconsistent condom use among college students. Prev Med 93:147–150. https://doi.org/10.1016/j.ypmed.2016.10.007
Veldhuijzen NJ, Braunstein SL, Vyankandondera J, Ingabire C, Ntirushwa J, Kestelyn E, Tuijn C, Wit FW, Umutoni A, Uwineza M, Crucitti T, van de Wijgert JH (2011) The Epidemiology of human papillomavirus infection in HIV-positive and HIV-negative high-risk women in Kigali, Rwanda. BMC Infect Dis 11:333. https://doi.org/10.1186/1471-2334-11-333
Velentzis LS, Sitas F, O’Connell DL, Darlington-Brown J, Egger S, Sinha R, Banks E, Frazer IH, Canfell K (2014) Human papillomavirus 16/18 seroprevalence in unvaccinated women over 30 years with normal cytology and with high grade cervical abnormalities in Australia: results from an observational study. BMC Infect Dis 14:3861. https://doi.org/10.1186/s12879-014-0676-z
Verteramo R, Pierangeli A, Mancini E, Calzolari E, Bucci M, Osborn J, Nicosia R, Chiarini F, Antonelli G, Degener AM (2009) Human papillomaviruses and genital co-infections in gynaecological outpatients. BMC Infect Dis 9:16. https://doi.org/10.1186/1471-2334-9-16
von Karsa L, Arbyn M, De Vuyst H, Dillner J, Dillner L, Franceschi S, Patnick J, Ronco G, Segnan N, Suonio E, Tornberg S, Anttila A (2015) European guidelines for quality assurance in cervical cancer screening. Summary of the supplements on HPV screening and vaccination. Papillomavirus Res 1:22–31. https://doi.org/10.1016/j.pvr.2015.06.006
Vriend HJ, Bogaards JA, van Bergen JE, Brink AA, van den Broek IV, Hoebe CJ, King AJ, van der Sande MA, Wolffs PF, de Melker HE, Medical Microbiological Laboratories and the CSI group (2015) Incidence and persistence of carcinogenic genital human papillomavirus infections in young women with or without chlamydia trachomatis co-infection. Cancer Med 4(10):1589–1598. https://doi.org/10.1002/cam4.496
Watts DH, Fazzari M, Minkoff H, Hillier SL, Sha B, Glesby M, Levine AM, Burk R, Palefsky JM, Moxley M, Ahdieh-Grant L, Strickler HD (2005) Effects of bacterial vaginosis and other genital infections on the natural history of human papillomavirus infection in HIV-1-infected and high-risk HIV-1-uninfected women. J Infect Dis 191(7):1129–1139. https://doi.org/10.1086/427777
WHO (1995) Tubal Infertility: Serologic Relationship to Past Chlamydial and Gonococcal Infection. World Health Organization Task Force on the Prevention and Management of Infertility. Sex Transm Dis 22(2):71-7
WHO (2014) Comprehensive cervical cancer control: a guide to essential practice, 2nd edn. World Health Organization, Geneva. Available from https://www.ncbi.nlm.nih.gov/books/NBK269619
WHO (2018) Report on Global Sexually Transmitted Infection Surveillance 2018. World Health Organization, Geneva
Witkin SS, Minis E, Athanasiou A, Leizer J, Linhares IM (2017) Chlamydia trachomatis: the persistent pathogen. Clin Vaccine Immunol 24(10):e00203–e00217. https://doi.org/10.1128/CVI.00203-17
Yin YP, Li HM, Xiang Z, Liang GJ, Shi MQ, Zhou YJ, Han Y, Wang GQ, Wang B, Chen XS (2013) Association of sexually transmitted infections with high-risk human papillomavirus types. Sex Transm Dis 40(6):493–495. https://doi.org/10.1097/OLQ.0b013e31828b32b8
Zhang B, Chen W, Roman A (2006) The E7 proteins of low- and high-risk human papillomaviruses share the ability to target the PRB family member P130 for degradation. Proc Natl Acad Sci U S A 103(2):437–442. https://doi.org/10.1073/pnas.0510012103
Zhang D, Li T, Chen L, Zhang X, Zhao G, Liu Z (2017) Epidemiological investigation of the relationship between common lower genital tract infections and high-risk human papillomavirus infections among women in Beijing, China. Plos One 12(5):e0178033. https://doi.org/10.1371/journal.pone.0178033
Zhu H, Shen Z, Luo H, Zhang W, Zhu X (2016) Chlamydia trachomatis infection-associated risk of cervical cancer. Medicine 95(13):e3077. https://doi.org/10.1097/MD.0000000000003077
Zoa Assoumou S, Ndjoyi Mbiguino A, Mabika Mabika B, Nguizi Ogoula S, El Mzibri M, Khattabi A, Ennaji MM (2016) Human papillomavirus genotypes distribution among Gabonese women with normal cytology and cervical abnormalities. Infect Agent Cancer 11:2. https://doi.org/10.1186/s13027-016-0046-0
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Major Revision: 22 February 2019.
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Naldini, G., Grisci, C., Chiavarini, M. et al. Association between human papillomavirus and chlamydia trachomatis infection risk in women: a systematic review and meta-analysis. Int J Public Health 64, 943–955 (2019). https://doi.org/10.1007/s00038-019-01261-w
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DOI: https://doi.org/10.1007/s00038-019-01261-w