Skip to main content
Top
Published in: BMC Public Health 1/2013

Open Access 01-12-2013 | Research article

Prevalence, genotype profile and risk factors for multiple human papillomavirus cervical infection in unimmunized female adolescents in Goiânia, Brazil: a community-based study

Authors: Rosane Ribeiro Figueiredo Alves, Marília Dalva Turchi, Lyana Elias Santos, Eleuse Machado de Britto Guimarães, Mônica Maria Danda Garcia, Mirian Socorro Cardoso Seixas, Luisa Lina Villa, Maria Cecília Costa, Marise Amaral Rebouças Moreira, Maria de Fátima da Costa Alves

Published in: BMC Public Health | Issue 1/2013

Login to get access

Abstract

Background

The epidemiology of infection with multiple human papillomavirus (HPV) types in female adolescents is poorly understood. The purpose of this study was to explore the epidemiology of infection with multiple HPV types in adolescents and its association with demographic, behavioral and biological variables, as well as with cytological abnormalities.

Methods

This community-based study included 432 sexually active females between 15 and 19 years of age. Genotyping for 30 HPV types was performed using a reverse blot strip assay/restriction fragment length polymorphism. Unconditional multivariate logistic regression was performed to identify factors significantly associated with HPV infection. The association between HPV infection and cytological abnormalities was calculated using a prevalence ratio.

Results

The most common HPV types detected were 16, 51, 31, 52 and 18. Of the 121 HPV-positive women, 54 (44.6%) were infected with multiple HPV types. Having more than one lifetime sexual partner was associated with infection with any HPV infection, single HPV infection, and infection with multiple HPV types. The presence of cytological abnormalities was associated with infection with multiple HPV types.

Conclusions

Co-infecting HPV genotypes occur in a high proportion of sexually active adolescents. Socio-demographic or sexual behavior factors associated with single HPV infection were similar to those associated with multiple HPV types. The higher risk of cytological abnormalities conferred by infection with multiple HPV types suggests a potential role of co-infection in the natural history of HPV infection.
Appendix
Available only for authorised users
Literature
1.
go back to reference Walboomers JM, Jacobs MV, Manos MM, Bosch FX, Kummer JA, Shah KV, Snijders PJ, Peto J, Meijer CJ, Munõz N: Human papillomavirus is a necessary cause of invasive cervical cancer worldwide. J Pathol. 1999, 189: 12-19. 10.1002/(SICI)1096-9896(199909)189:1<12::AID-PATH431>3.0.CO;2-F.CrossRefPubMed Walboomers JM, Jacobs MV, Manos MM, Bosch FX, Kummer JA, Shah KV, Snijders PJ, Peto J, Meijer CJ, Munõz N: Human papillomavirus is a necessary cause of invasive cervical cancer worldwide. J Pathol. 1999, 189: 12-19. 10.1002/(SICI)1096-9896(199909)189:1<12::AID-PATH431>3.0.CO;2-F.CrossRefPubMed
2.
go back to reference Muñoz N, Bosch FX, de Sanjose S, Herrero R, Castellsague X, Shah KV, Snijders PJ, Meijer CJ: Epidemiologic classification of human papillomavirus types associated with cervical cancer. N Engl J Med. 2003, 348: 518-527. 10.1056/NEJMoa021641.CrossRefPubMed Muñoz N, Bosch FX, de Sanjose S, Herrero R, Castellsague X, Shah KV, Snijders PJ, Meijer CJ: Epidemiologic classification of human papillomavirus types associated with cervical cancer. N Engl J Med. 2003, 348: 518-527. 10.1056/NEJMoa021641.CrossRefPubMed
3.
go back to reference Schmitt M, Depuydt C, Benoy I, Bogers J, Antoine J, Arbyn M, Pawlita M: Multiple HPV infections with high viral loads are associated with cervical lesions but do not differentiate grades of cervical abnormalities. JCM. 2013, 51: 1458-1464.CrossRef Schmitt M, Depuydt C, Benoy I, Bogers J, Antoine J, Arbyn M, Pawlita M: Multiple HPV infections with high viral loads are associated with cervical lesions but do not differentiate grades of cervical abnormalities. JCM. 2013, 51: 1458-1464.CrossRef
4.
go back to reference Brown DR, Shew ML, Qadadri B, Neptune N, Vargas M, Tu W, Juliar BE, Breen TE, Fortenberry JD: A longitudinal study of genital human papillomavirus infection in a cohort of closely followed adolescent women. J Infect Dis. 2005, 191: 182-192. 10.1086/426867.CrossRefPubMed Brown DR, Shew ML, Qadadri B, Neptune N, Vargas M, Tu W, Juliar BE, Breen TE, Fortenberry JD: A longitudinal study of genital human papillomavirus infection in a cohort of closely followed adolescent women. J Infect Dis. 2005, 191: 182-192. 10.1086/426867.CrossRefPubMed
5.
go back to reference Chaturvedi AK, Katki HA, Hildesheim A, Rodriguez AC, Quint W, Schiffman M, Van Doorn LJ, Porras C, Wacholder S, Gonzalez P, Sherman ME, Herrero R: Human papillomavirus infection with multiple types: pattern of coinfection and risk of cervical disease. J Infect Dis. 2011, 203: 910-920. 10.1093/infdis/jiq139.CrossRefPubMedPubMedCentral Chaturvedi AK, Katki HA, Hildesheim A, Rodriguez AC, Quint W, Schiffman M, Van Doorn LJ, Porras C, Wacholder S, Gonzalez P, Sherman ME, Herrero R: Human papillomavirus infection with multiple types: pattern of coinfection and risk of cervical disease. J Infect Dis. 2011, 203: 910-920. 10.1093/infdis/jiq139.CrossRefPubMedPubMedCentral
6.
go back to reference Nielsen A, Kjaer SK, Munk C, Iftner T: Type-specific HPV infection and multiple HPV types: prevalence and risk factor profile in nearly 12,000 younger and older Danish women. Sex Transm Dis. 2008, 35: 276-282. 10.1097/OLQ.0b013e31815ac5c7.CrossRefPubMed Nielsen A, Kjaer SK, Munk C, Iftner T: Type-specific HPV infection and multiple HPV types: prevalence and risk factor profile in nearly 12,000 younger and older Danish women. Sex Transm Dis. 2008, 35: 276-282. 10.1097/OLQ.0b013e31815ac5c7.CrossRefPubMed
7.
go back to reference Rousseau MC, Abrahamowicz M, Villa LL, Costa MC, Rohan TE, Franco EL: Predictors of cervical coinfection with multiple human papillomavirus types. Cancer Epidemiol Biomarkers Prev. 2003, 12: 1029-1037.PubMed Rousseau MC, Abrahamowicz M, Villa LL, Costa MC, Rohan TE, Franco EL: Predictors of cervical coinfection with multiple human papillomavirus types. Cancer Epidemiol Biomarkers Prev. 2003, 12: 1029-1037.PubMed
8.
go back to reference Chaturvedi AK, Myers L, Hammons AF, Clark RA, Dunlap K, Kissinger PJ, Hagensee ME: Prevalence and clustering patterns of human papillomavirus genotypes in multiple infections. Cancer Epidemiol Biomarkers Prev. 2005, 14: 2439-2445. 10.1158/1055-9965.EPI-05-0465.CrossRefPubMed Chaturvedi AK, Myers L, Hammons AF, Clark RA, Dunlap K, Kissinger PJ, Hagensee ME: Prevalence and clustering patterns of human papillomavirus genotypes in multiple infections. Cancer Epidemiol Biomarkers Prev. 2005, 14: 2439-2445. 10.1158/1055-9965.EPI-05-0465.CrossRefPubMed
9.
go back to reference Rousseau MC, Pereira JS, Prado JC, Villa LL, Rohan TE, Franco EL: Cervical coinfection with human papillomavirus types as a predictor of a acquisition and persistence of HPV infection. J Infect Dis. 2002, 184: 1508-1517.CrossRef Rousseau MC, Pereira JS, Prado JC, Villa LL, Rohan TE, Franco EL: Cervical coinfection with human papillomavirus types as a predictor of a acquisition and persistence of HPV infection. J Infect Dis. 2002, 184: 1508-1517.CrossRef
10.
go back to reference Thomas KK, Hughes JP, Kuypers JM, Kiviat NB, Lee SK, Adam ED, Koutsky LA: Concurrent and sequential acquisition of different genital human papilamavirus types. J Infect Dis. 2000, 182: 1097-1102. 10.1086/315805.CrossRefPubMed Thomas KK, Hughes JP, Kuypers JM, Kiviat NB, Lee SK, Adam ED, Koutsky LA: Concurrent and sequential acquisition of different genital human papilamavirus types. J Infect Dis. 2000, 182: 1097-1102. 10.1086/315805.CrossRefPubMed
11.
go back to reference Samoff E, Koumans EH, Markowitz LE, Sternberg M, Sawyer MK, Swan D, Papp JR, Black CM, Unger ER: Association of chlamydia trachomatis with persistence of high-risk types of human papillomavirus in a cohort of female adolescents. Am J Epidemiol. 2005, 162: 668-675. 10.1093/aje/kwi262.CrossRefPubMed Samoff E, Koumans EH, Markowitz LE, Sternberg M, Sawyer MK, Swan D, Papp JR, Black CM, Unger ER: Association of chlamydia trachomatis with persistence of high-risk types of human papillomavirus in a cohort of female adolescents. Am J Epidemiol. 2005, 162: 668-675. 10.1093/aje/kwi262.CrossRefPubMed
12.
go back to reference Moscicki AB, Shiboski S, Broering J, Powel K, Clayton L, Jay N, Darragh TM, Brescia R, Kanowitz S, Miller S, Stone J, Hanson E, Palefsky J: The natural history of human papillomavirus infection as measured by repeated DNA testing in adolescent and young women. J Pediatr. 1998, 132: 277-284. 10.1016/S0022-3476(98)70445-7.CrossRefPubMed Moscicki AB, Shiboski S, Broering J, Powel K, Clayton L, Jay N, Darragh TM, Brescia R, Kanowitz S, Miller S, Stone J, Hanson E, Palefsky J: The natural history of human papillomavirus infection as measured by repeated DNA testing in adolescent and young women. J Pediatr. 1998, 132: 277-284. 10.1016/S0022-3476(98)70445-7.CrossRefPubMed
13.
go back to reference Moscicki A-B, Cox JT: Practice improvement in cervical screening and management (PICSM): symposium on management of cervical abnormalities in adolescents and young women. J Low Genit Tract Dis. 2010, 14: 73-80. 10.1097/LGT.0b013e3181cec411.CrossRefPubMedPubMedCentral Moscicki A-B, Cox JT: Practice improvement in cervical screening and management (PICSM): symposium on management of cervical abnormalities in adolescents and young women. J Low Genit Tract Dis. 2010, 14: 73-80. 10.1097/LGT.0b013e3181cec411.CrossRefPubMedPubMedCentral
14.
go back to reference Rousseau MC, Villa LL, Costa MC, Abrahamowicz M, Rohan TE, Franco AE: Occurrence of cervical infection with multiple human papillomavirus types is associated with age and cytologic abnormalities. Sex Transm Dis. 2002, 30: 581-587.CrossRef Rousseau MC, Villa LL, Costa MC, Abrahamowicz M, Rohan TE, Franco AE: Occurrence of cervical infection with multiple human papillomavirus types is associated with age and cytologic abnormalities. Sex Transm Dis. 2002, 30: 581-587.CrossRef
15.
go back to reference Trottier H, Mahmud S, Costa MC, Sobrinho JP, Duarte-Franco E, Rohan TE, Ferenczy A, Villa LL, Franco EL: Human papillomavirus infections with multiple types and risk of cervical neoplasia. Cancer Epidemiol Biomarkers Prev. 2006, 15: 1274-1280. 10.1158/1055-9965.EPI-06-0129.CrossRefPubMed Trottier H, Mahmud S, Costa MC, Sobrinho JP, Duarte-Franco E, Rohan TE, Ferenczy A, Villa LL, Franco EL: Human papillomavirus infections with multiple types and risk of cervical neoplasia. Cancer Epidemiol Biomarkers Prev. 2006, 15: 1274-1280. 10.1158/1055-9965.EPI-06-0129.CrossRefPubMed
16.
go back to reference van der Graaf Y, Molijn A, Doornewaard H, Quint W, van Doorn LJ, van den Tweel J: Human papillomavirus and the long-term risk of cervical neoplasia. Am J Epidemiol. 2002, 156: 158-164. 10.1093/aje/kwf013.CrossRefPubMed van der Graaf Y, Molijn A, Doornewaard H, Quint W, van Doorn LJ, van den Tweel J: Human papillomavirus and the long-term risk of cervical neoplasia. Am J Epidemiol. 2002, 156: 158-164. 10.1093/aje/kwf013.CrossRefPubMed
17.
go back to reference Campos NG, Rodriguez AC, Castle PE, Herrero R, Hildesheim A, Katki H, Kim JJ, Wacholder S, Morales J, Burk RD, Schiffman M: Persistence of concurrent infections with multiple human papillomavirus types: a population-based cohort study. J Infect Dis. 2011, 203: 823-827. 10.1093/infdis/jiq131.CrossRefPubMedPubMedCentral Campos NG, Rodriguez AC, Castle PE, Herrero R, Hildesheim A, Katki H, Kim JJ, Wacholder S, Morales J, Burk RD, Schiffman M: Persistence of concurrent infections with multiple human papillomavirus types: a population-based cohort study. J Infect Dis. 2011, 203: 823-827. 10.1093/infdis/jiq131.CrossRefPubMedPubMedCentral
18.
go back to reference Bruni L, Diaz M, Castellsague X, Ferrer E, Bosch FX, de Sanjose S: Cervical human papillomavirus prevalence in 5 continents: meta-analysis of 1 million women with normal cytological findings. J Infect Dis. 2010, 202: 1789-1799. 10.1086/657321.CrossRefPubMed Bruni L, Diaz M, Castellsague X, Ferrer E, Bosch FX, de Sanjose S: Cervical human papillomavirus prevalence in 5 continents: meta-analysis of 1 million women with normal cytological findings. J Infect Dis. 2010, 202: 1789-1799. 10.1086/657321.CrossRefPubMed
19.
go back to reference de Sanjosé S, Diaz M, Castellsagué X, Clifford G, Bruni L, Muñoz N, Bosch FX: Worldwide prevalence and genotype distribution of cervical human papillomavirus DNA in women with normal cytology: a meta-analysis. Lancet Infect Dis. 2007, 7: 453-459. 10.1016/S1473-3099(07)70158-5.CrossRefPubMed de Sanjosé S, Diaz M, Castellsagué X, Clifford G, Bruni L, Muñoz N, Bosch FX: Worldwide prevalence and genotype distribution of cervical human papillomavirus DNA in women with normal cytology: a meta-analysis. Lancet Infect Dis. 2007, 7: 453-459. 10.1016/S1473-3099(07)70158-5.CrossRefPubMed
20.
go back to reference Ayres ARG, Silva GA: Cervical HPV infection in Brazil: systematic review. Rev Saúde Pública. 2010, 44: 963-974.PubMed Ayres ARG, Silva GA: Cervical HPV infection in Brazil: systematic review. Rev Saúde Pública. 2010, 44: 963-974.PubMed
21.
go back to reference Guimarães BE, Guimarães MD, Vieira M, Bontempo NM, Seixas MS, Garcia MD, Daud L, Côrtes R, Alves M: Lack of utility of risk score and gynecological examination for screening for sexually transmitted infections in sexually active adolescents. BMC Med. 2009, 7: 8-14. 10.1186/1741-7015-7-8.CrossRefPubMedPubMedCentral Guimarães BE, Guimarães MD, Vieira M, Bontempo NM, Seixas MS, Garcia MD, Daud L, Côrtes R, Alves M: Lack of utility of risk score and gynecological examination for screening for sexually transmitted infections in sexually active adolescents. BMC Med. 2009, 7: 8-14. 10.1186/1741-7015-7-8.CrossRefPubMedPubMedCentral
22.
go back to reference Solomon D, Davey D, Kurman R, Moriarty A, O’Connor D, Prey M, Raab S, Sherman M, Wilbur D, Wright T, The YN, et al: Bethesda system: terminology for reporting results of cervical cytology. JAMA. 2001, 2002 (287): 2114-2119. Solomon D, Davey D, Kurman R, Moriarty A, O’Connor D, Prey M, Raab S, Sherman M, Wilbur D, Wright T, The YN, et al: Bethesda system: terminology for reporting results of cervical cytology. JAMA. 2001, 2002 (287): 2114-2119.
23.
go back to reference Gravitt PE, Peyton CL, Alessi TQ, Wheeler CM, Coutlee F, Hildesheim A, Schiffman MH, Scott DR, Apple RJ: Improved amplification of genital human papillomaviruses. J ClinMicrobiol. 2000, 38: 357-361. Gravitt PE, Peyton CL, Alessi TQ, Wheeler CM, Coutlee F, Hildesheim A, Schiffman MH, Scott DR, Apple RJ: Improved amplification of genital human papillomaviruses. J ClinMicrobiol. 2000, 38: 357-361.
24.
go back to reference Bernard HU, Chan SY, Manos MM, Ong CK, Villa LL, Delius H, Peyton CL, Bauer HM, Wheeler CM: Identification and assessment of known and novel human papillomaviruses by polymerase chain reaction amplification, restriction fragment length polymorphisms, nucleotide sequence, and phylogenetic algorithms. J Infect Dis. 1994, 170: 1077-1085. 10.1093/infdis/170.5.1077.CrossRefPubMed Bernard HU, Chan SY, Manos MM, Ong CK, Villa LL, Delius H, Peyton CL, Bauer HM, Wheeler CM: Identification and assessment of known and novel human papillomaviruses by polymerase chain reaction amplification, restriction fragment length polymorphisms, nucleotide sequence, and phylogenetic algorithms. J Infect Dis. 1994, 170: 1077-1085. 10.1093/infdis/170.5.1077.CrossRefPubMed
25.
go back to reference de Villiers EM, Fauquet C, Broker TR, Bernard HU, zur Hausen H: Classification of papillomaviruses. Virology. 2004, 324: 17-27. 10.1016/j.virol.2004.03.033.CrossRefPubMed de Villiers EM, Fauquet C, Broker TR, Bernard HU, zur Hausen H: Classification of papillomaviruses. Virology. 2004, 324: 17-27. 10.1016/j.virol.2004.03.033.CrossRefPubMed
26.
go back to reference Dunne EF, Unger ER, Sternberg M, McQuillan G, Swan DC, Patel SS, Markowitz LE: Prevalence of HPV infection among females in the United States. JAMA. 2007, 297: 813-819. 10.1001/jama.297.8.813.CrossRefPubMed Dunne EF, Unger ER, Sternberg M, McQuillan G, Swan DC, Patel SS, Markowitz LE: Prevalence of HPV infection among females in the United States. JAMA. 2007, 297: 813-819. 10.1001/jama.297.8.813.CrossRefPubMed
27.
go back to reference Johnson AM, Mercer CH, Beddows S, de Silva N, Desai S, Howell-Jones R, Carder C, Sonnenberg P, Fenton KA, Lowndes C, Soldan K: Epidemiology of, and behavioural risk factors for, sexually transmitted human papillomavirus infection in men and women in Britain. Sex Transm Infect. 2012, 88: 212-217. 10.1136/sextrans-2011-050306.CrossRefPubMedPubMedCentral Johnson AM, Mercer CH, Beddows S, de Silva N, Desai S, Howell-Jones R, Carder C, Sonnenberg P, Fenton KA, Lowndes C, Soldan K: Epidemiology of, and behavioural risk factors for, sexually transmitted human papillomavirus infection in men and women in Britain. Sex Transm Infect. 2012, 88: 212-217. 10.1136/sextrans-2011-050306.CrossRefPubMedPubMedCentral
28.
go back to reference Kahn JA, Rosenthal SL, Succop PA, Ho GY, Burk RD: Mediators of the association between age of first sexual intercourse and subsequent human papillomavirus infection. Pediatrics. 2002, 109: 1-8. 10.1542/peds.109.1.1.CrossRef Kahn JA, Rosenthal SL, Succop PA, Ho GY, Burk RD: Mediators of the association between age of first sexual intercourse and subsequent human papillomavirus infection. Pediatrics. 2002, 109: 1-8. 10.1542/peds.109.1.1.CrossRef
29.
go back to reference Marks MA, Gravitt PE, Burk RD, Studentsov Y, Farzadegan H, Klein SL: Progesterone and 17beta-estradiol enhance regulatory responses to human papillomavirus type 16 virus-like particles in peripheral blood mononuclear cells from healthy women. Clin Vaccine Immunol. 2010, 17: 609-617. 10.1128/CVI.00441-09.CrossRefPubMedPubMedCentral Marks MA, Gravitt PE, Burk RD, Studentsov Y, Farzadegan H, Klein SL: Progesterone and 17beta-estradiol enhance regulatory responses to human papillomavirus type 16 virus-like particles in peripheral blood mononuclear cells from healthy women. Clin Vaccine Immunol. 2010, 17: 609-617. 10.1128/CVI.00441-09.CrossRefPubMedPubMedCentral
30.
go back to reference Stoler M, Schiffman M: Interobserver reproducibility of cervical cytologic and histological interpretations: realistic estimates from the ASCUS-LSIL triage study. JAMA. 2001, 285: 1500-1505. 10.1001/jama.285.11.1500.CrossRefPubMed Stoler M, Schiffman M: Interobserver reproducibility of cervical cytologic and histological interpretations: realistic estimates from the ASCUS-LSIL triage study. JAMA. 2001, 285: 1500-1505. 10.1001/jama.285.11.1500.CrossRefPubMed
31.
go back to reference Bigras G, Wilson J, Russell L, Johnson G, Morel D, Saddik M: Interobserver concordance in the assessment of features used for the diagnosis of cervical atypical squamous cells and squamous intraepithelial lesions (ASC-US, ASC-H, LSIL and HSIL). Cytopathology. 2013, 24: 44-51. 10.1111/j.1365-2303.2011.00930.x.CrossRefPubMed Bigras G, Wilson J, Russell L, Johnson G, Morel D, Saddik M: Interobserver concordance in the assessment of features used for the diagnosis of cervical atypical squamous cells and squamous intraepithelial lesions (ASC-US, ASC-H, LSIL and HSIL). Cytopathology. 2013, 24: 44-51. 10.1111/j.1365-2303.2011.00930.x.CrossRefPubMed
Metadata
Title
Prevalence, genotype profile and risk factors for multiple human papillomavirus cervical infection in unimmunized female adolescents in Goiânia, Brazil: a community-based study
Authors
Rosane Ribeiro Figueiredo Alves
Marília Dalva Turchi
Lyana Elias Santos
Eleuse Machado de Britto Guimarães
Mônica Maria Danda Garcia
Mirian Socorro Cardoso Seixas
Luisa Lina Villa
Maria Cecília Costa
Marise Amaral Rebouças Moreira
Maria de Fátima da Costa Alves
Publication date
01-12-2013
Publisher
BioMed Central
Published in
BMC Public Health / Issue 1/2013
Electronic ISSN: 1471-2458
DOI
https://doi.org/10.1186/1471-2458-13-1041

Other articles of this Issue 1/2013

BMC Public Health 1/2013 Go to the issue