Human Papillomavirus and environmental factors predict treatment failure of cervical precancerous lesions among Brazilian women: a hospital based cohort
Main Article Content
Abstract
Cervical cancer is preventable through the detection and treatment of precancerous lesions. However treatment failure occurs around 5-35%, and there is no consensus about the risk factors involved. Although it has been indicated that HR-HPV in conjunction with cytology should be useful for monitoring women treated for CIN, few HPV infected women will develop (present a) persistent HPV infections and progress to cancer, suggesting that additional factors are necessary for treatment failure, such as tobacco smoking and oral contraceptive use. Aim: to evaluate the effect of HPV and selected environmental factors on the risk of CIN treatment failure. A prospective study was conducted on a cohort of 205 women histologically confirmed CIN1–3 who were treated at Brazilian National Cancer Institute from October/2004 to May/2006. A questionnaire with epidemiological and clinical information was administered by two trained registered nurses. Women were followed for 24 months with cytological exams and cervical smears were taken for HPV tests. Mean age was 35(+11) years old; mean age at sexual onset was 17(+3) years old. Current oral contraceptive use(HR=2.05;95%CI:1.08-3.88), current tobacco use(HR=1.87;95%CI:1.08-3.24), and a positive HPV result up to 6 months after treatment (HR=2.35;95%CI:1.39-3.97) were statistically associated with CIN treatment failure in 24 months. Women who are current smokers, oral contraceptive users, and who are HPV positive in the first 3-6 months after treatment, are at higher risk of treatment failure.
Article Details
How to Cite
SILVA, Ilce Ferreira da et al.
Human Papillomavirus and environmental factors predict treatment failure of cervical precancerous lesions among Brazilian women: a hospital based cohort.
Medical Research Archives, [S.l.], n. 3, july 2015.
ISSN 2375-1924.
Available at: <https://esmed.org/MRA/mra/article/view/303>. Date accessed: 15 dec. 2024.
Keywords
Cervical cancer; CIN-treatment failure; HPV; epidemiology; epidemiology; tobacco smoking; tobacco smoking
Issue
Section
Research Articles
The Medical Research Archives grants authors the right to publish and reproduce the unrevised contribution in whole or in part at any time and in any form for any scholarly non-commercial purpose with the condition that all publications of the contribution include a full citation to the journal as published by the Medical Research Archives.
References
Acladious NN, Sutton C, Mandal D, Hopkins R, Zaklama M, Kitchener H. (2002) Persistent human papillomavirus infection and smoking increase risk of failure of treatment of cervical intraepithelial neoplasia (CIN). Int J Cancer, 98(3):435-9. DOI: 10.1002/ijc.10080
Aerssens A, Claeys P, Garcia A, Sturtewagen Y, Velasquez R, Vanden Broeck D, Vansteelandt S, Temmerman M, Cuvelier CA. (2009) Natural history and clearance of HPV after treatment of precancerous cervical lesions. Histopathology, 52(3):381-86. doi: 10.1111/j.1365-2559.2007.02956.x.
Alam S, Conway MJ, Chen HS, Meyers C. (2008) The cigarette smoke carcinogenbezo[a]pyrene enhances human papillomavirus sytesis. J Viro, 82:1053-1058. doi: 10.1128/JVI.01813-07
Alonso I, Torné A, Puig-Tintoré LM, Esteve R, Quinto L, Campo E, Pahisa J, Ordi J. (2006) Pre- and post-conization high-risk HPV testing predicts residual/recurrent disease in patients treated for CIN 2–3. Gynecologic Oncology, 103:631–636. DOI: http://dx.doi.org/10.1016/j.ygyno.2006.04.016
Appleby P, Beral V, Berrington de Gonzalez A, Colin D, Franceschi S, Goodhill A, Green J, Peto J, Plummer M, Sweetland S. (2007) Cervical cancer and hormonal contraceptives: collaborative reanalysis of individual data for 16,573 women with cervical cancer and 35,509 women without cervical cancer from 24 epidemiological studies. Lance, 370:1609–21. DOI: http://dx.doi.org/10.1016/S0140-6736(07)61684-5
Arbyn M, Ronco G, Meijer CJ, Poljak M, Oqilvie G, Koliopoulos G, Naucler P, Sankaranarayanan R, Peto j. (2012) Evidence regarding human papillomavirus testing insecondary prevention of cervical cancer. Vaccine, Suppl 5:F88-99. doi: 10.1016/j.vaccine.2012.06.095.
Bar-Am A, Gamzu R, Levin I, Fainaru O, Niv J, Almog B. (2003) Follow-up by combined cytology and human papillomavirus testing for patients post-cone biopsy: results of a long-term follow-up. GynecolOncol, 91:149–53. DOI: http://dx.doi.org/10.1016/S0090-8258(03)00435-9
Benchimol Y, Mergui JL, Uzan S. (2005) The role of viral HPV testing in postoperative follow-up. HPV handbook. Current evidence-based applications. New York: Taylor and Francis.
Bigrigg A, Haffenden DK, Sheehan AL, Codling BW, Read MD. (1994) Efficacy and safety of large loop excision of the transformation zone. Lancet, 343:32–4. DOI: http://dx.doi.org/10.1016/S0140-6736(94)90881-8
Brotto LA, Chou AY, Singh T, et al. (2008) Reproductive health practices among Indian, Indo-Canadian, Canadian East Asian, and Euro-CanadianWomen: the role of acculturation. J Obstet Gynaecol Can, 30:229-38. PMID: 18364100
Chung SH, Wiedmeyer K, Shai A, Korach KS, Lambert PF. (2008) Requirement for estrogen receptor alpha in a mouse model for human papillomavirus-associated cervical cancer. Cancer Res, 68:9928–34. doi: 10.1158/0008-5472.CAN-08-2051.
de Roda Husman AM, Walboomers JM, van den Brule AJ, Meijer CJ, Snijders PJ. (1995) The use of general primers GP5 and GP6 elongated at their 3’ ends with adjacent highly conserved sequences improves human papillomavirus detection by PCR. J Gen Virol, 76:1057-1062. doi: 10.1099/0022-1317-76-4-1057
Ferlay J, Shin HR, Bray F, Forman D, Mathers C and Parkin DM. (2012) GLOBOCAN 2008 v2.0, Cancer Incidence and Mortality Worldwide: IARC Cancer Base No. 10 [Internet]. Lyon, France: International Agency for Research on Cancer; 2010. Available from: http://globocan.iarc.fr, accessed on 28/June/2013.
Gardeil F, Barry-Walsh C, Prendiville W, Clinch J, Turner MJ. (1997) Persistent intraepithelial neoplasia after excision for cervical intraepithelial neoplasia grade III. Obstet Gynecol, 89:419–22. PMID:9052597
Ghaem-Maghami S, Sagi S, Majeed G, Soutter WP. (2007) Incomplete excision of cervical Intraepithelialneoplasia and risk of treatment failure: a meta-analysis. Lancet Oncol, 8(11):985-93. DOI: http://dx.doi.org/10.1016/S1470-2045(07)70283-8
Ghaem-Maghami S, Sagi S, Majeed G, Soutter WP. (2007) Incomplete excision of cervical Intraepithelialneoplasia and risk of treatment failure: a meta-analysis. Lancet Oncol, 8(11):985-93. DOI: http://dx.doi.org/10.1016/S1470-2045(07)70283-8
Hoffman D, Hoffman I, El-Bayoumy K. (2001) The less harmful cigarette: A controversial issue. A tribute to Ernst L. Wynder. Chem Res Toxicol, 14:767-790.
Instituto Brasileiro de Geografia e Estatística. (2009) National research by household sample. Methodology Notes. Accessed 02 January 2013. Available:http://www.ibge.gov.br/home/estatistica/populacao/trabalhoerendimento/pnad2009/pn ad_sintese_2009.pdf. Portuguese.
International Agency for Research on Cancer. (2004) Tobacco Smoke and involuntary smoking. IARC MonogrEvalCarcinog Risks Hum. 83; 2004. Accessed 02 January 2013. Available: http://www.monographs.iarc.fr/ENG/Monographs/vol38/volume38.pdf.
Marks MA, Gravitt PE, Burk RD, Studentsov Y, Farzadegan H, Klein SL. (2010) 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, 17:609–17. doi: 10.1128/CVI.00441-09. Epub 2010 Feb 3.
Marks MA, Viscidi RP, Chang K, Silver M, Burke A, Howard R, Gravitt PE. (2011) Differences in the concentration and correlation of cervical immune markers among HPV positive and negative perimenopausal women. Cytokine, 56:798–803. doi: 10.1016/j.cyto.2011.09.012. Epub 2011 Oct 19.
Ministério da Saúde/ Instituto Nacional de Câncer (Brasil). (2011) Diretrizes Brasileiras para o rastreamento Do Câncer Do Colo Do Útero. Accessed 09 September 2013. Available: http://www1.inca.gov.br/inca/Arquivos/Diretrizes_rastreamento_cancer_colo_utero.pdf
Ministério da Saúde/ Instituto Nacional do Câncer. Registro de Câncer de Base Populacional Accessed 09 September 2013. Available: http://www2.inca.gov.br/wps/wcm/connect/estatisticas/site/home/rcbp/
Moreno V, Bosch FX, Munoz N, Meijer CJ, Shah KV, Walboomers JM, Herrero R, Franceschi S. (2002) Effect of oral contraceptives on risk of cervical cancer in women with human papillomavirus infection: the IARC multicentric case-control study. Lancet, 359:1085–92. DOI: http://dx.doi.org/10.1016/S0140-6736(02)08150-3
Ruutu M, Wahlroos N, Syrjanen K, Johansson B, Syrjanen S. (2006) Effects of 17beta-estradiol and progesterone on transcription of human papillomavirus 16 E6/E7 oncogenes in CaSki and SiHa cell lines. Int J Gynecol Cancer, 16:1261–8. PMID:16803515
Shai A, Brake T, Somoza C, Lambert PF. (2007) The human papillomavirus E6 oncogene dysregulates the cell cycle and contributes to cervical carcinogenesis through two independent activities. Cancer Res, 67:1626–35. doi: 10.1158/0008-5472.CAN-06-3344
Silva IF, Koifman RJ, Mattos IE. (2009) Epidemiological characteristics related to treatment failure of preinvasive cervical intraepithelial neoplasia among Brazilian women. Int J Gynecol Cancer, 19(8):1427-31. doi: 10.1111/IGC.0b013e3181b8677f.
Solomon D, Davey D, Kurman R, Moriarty A, O'Connor D, Prey M. (2002) The 2001 Bethesda System: Terminology for Reporting Results of Cervical Cytology. Journal of the American Medical Association, 287(16):2114-2119. PMID: 11966386. doi:10.1001/jama.287.16.2114.
Soutter WP, Sasieni P, Panoskaltsis T. (2006) Long-term risk of invasive cervical cancer after treatment of squamous cervical intraepithelial neoplasia. Int J Cancer, 118(8):2048–55.
Stafl A, Wilbanks GD. (1991) An international terminology of colposcopy: Report of the nomenclature committee of the International Federation of Cervical Pathology and Colposcopy. Obstetrics and Gynecology, 77:313-314. PMID:1988900
Trushin N, Alam S, El-Bayoumy K, Krzeminski J, Amin SG, Gullet J, Meyers C, Prokopczyk B. (2012) Comparative metabolism of benzo[a]pyrene by human keratinocytes infected with high-risk human papillomavirus type 16 and 18 as episomal or integrated genomes. Journal of Carnogenesis. Online version assessed on [September 18, 2013]: http://www.carcinogenesis.com doi: 10.4103/1477-3163.92309
Woodman CB, Collins SI, Young LS. (2007) The natural history of cervical HPV infection: unresolved issues. Nat Rev Cancer, 7(1):11-22. doi:10.1038/nrc2050
World Health Organization. (2005) Cervical Cancer Screening in Developing Countries. A report of WHO Consultation. Word Health Organization: Geneva; 2005.
Zardo LM, Thuler LC, Zeferino LC, Horta NM, Fonseca R de C. (2009) Performance of the cytologic examination for the diagnosis of endocervical adenocarcinoma in situ: cytologic-histologic correlation in 60 cases. ActaCytol, 53(5):558-64. PMID19798884
Zielinski GD, Bais AG, Helmerhorst TJ, Verheijen RH, de Schipper FA, Snijders PJ, Voorhorst FJ, van Kemenade FJ, Rozendaal L, Meijer CJ. (2004) HPV testing and monitoring of women after treatment of CIN 3: review of the literature and meta-analysis. Obstet Gynecol, Surv.59(7):543–53. PMID:15199273
Aerssens A, Claeys P, Garcia A, Sturtewagen Y, Velasquez R, Vanden Broeck D, Vansteelandt S, Temmerman M, Cuvelier CA. (2009) Natural history and clearance of HPV after treatment of precancerous cervical lesions. Histopathology, 52(3):381-86. doi: 10.1111/j.1365-2559.2007.02956.x.
Alam S, Conway MJ, Chen HS, Meyers C. (2008) The cigarette smoke carcinogenbezo[a]pyrene enhances human papillomavirus sytesis. J Viro, 82:1053-1058. doi: 10.1128/JVI.01813-07
Alonso I, Torné A, Puig-Tintoré LM, Esteve R, Quinto L, Campo E, Pahisa J, Ordi J. (2006) Pre- and post-conization high-risk HPV testing predicts residual/recurrent disease in patients treated for CIN 2–3. Gynecologic Oncology, 103:631–636. DOI: http://dx.doi.org/10.1016/j.ygyno.2006.04.016
Appleby P, Beral V, Berrington de Gonzalez A, Colin D, Franceschi S, Goodhill A, Green J, Peto J, Plummer M, Sweetland S. (2007) Cervical cancer and hormonal contraceptives: collaborative reanalysis of individual data for 16,573 women with cervical cancer and 35,509 women without cervical cancer from 24 epidemiological studies. Lance, 370:1609–21. DOI: http://dx.doi.org/10.1016/S0140-6736(07)61684-5
Arbyn M, Ronco G, Meijer CJ, Poljak M, Oqilvie G, Koliopoulos G, Naucler P, Sankaranarayanan R, Peto j. (2012) Evidence regarding human papillomavirus testing insecondary prevention of cervical cancer. Vaccine, Suppl 5:F88-99. doi: 10.1016/j.vaccine.2012.06.095.
Bar-Am A, Gamzu R, Levin I, Fainaru O, Niv J, Almog B. (2003) Follow-up by combined cytology and human papillomavirus testing for patients post-cone biopsy: results of a long-term follow-up. GynecolOncol, 91:149–53. DOI: http://dx.doi.org/10.1016/S0090-8258(03)00435-9
Benchimol Y, Mergui JL, Uzan S. (2005) The role of viral HPV testing in postoperative follow-up. HPV handbook. Current evidence-based applications. New York: Taylor and Francis.
Bigrigg A, Haffenden DK, Sheehan AL, Codling BW, Read MD. (1994) Efficacy and safety of large loop excision of the transformation zone. Lancet, 343:32–4. DOI: http://dx.doi.org/10.1016/S0140-6736(94)90881-8
Brotto LA, Chou AY, Singh T, et al. (2008) Reproductive health practices among Indian, Indo-Canadian, Canadian East Asian, and Euro-CanadianWomen: the role of acculturation. J Obstet Gynaecol Can, 30:229-38. PMID: 18364100
Chung SH, Wiedmeyer K, Shai A, Korach KS, Lambert PF. (2008) Requirement for estrogen receptor alpha in a mouse model for human papillomavirus-associated cervical cancer. Cancer Res, 68:9928–34. doi: 10.1158/0008-5472.CAN-08-2051.
de Roda Husman AM, Walboomers JM, van den Brule AJ, Meijer CJ, Snijders PJ. (1995) The use of general primers GP5 and GP6 elongated at their 3’ ends with adjacent highly conserved sequences improves human papillomavirus detection by PCR. J Gen Virol, 76:1057-1062. doi: 10.1099/0022-1317-76-4-1057
Ferlay J, Shin HR, Bray F, Forman D, Mathers C and Parkin DM. (2012) GLOBOCAN 2008 v2.0, Cancer Incidence and Mortality Worldwide: IARC Cancer Base No. 10 [Internet]. Lyon, France: International Agency for Research on Cancer; 2010. Available from: http://globocan.iarc.fr, accessed on 28/June/2013.
Gardeil F, Barry-Walsh C, Prendiville W, Clinch J, Turner MJ. (1997) Persistent intraepithelial neoplasia after excision for cervical intraepithelial neoplasia grade III. Obstet Gynecol, 89:419–22. PMID:9052597
Ghaem-Maghami S, Sagi S, Majeed G, Soutter WP. (2007) Incomplete excision of cervical Intraepithelialneoplasia and risk of treatment failure: a meta-analysis. Lancet Oncol, 8(11):985-93. DOI: http://dx.doi.org/10.1016/S1470-2045(07)70283-8
Ghaem-Maghami S, Sagi S, Majeed G, Soutter WP. (2007) Incomplete excision of cervical Intraepithelialneoplasia and risk of treatment failure: a meta-analysis. Lancet Oncol, 8(11):985-93. DOI: http://dx.doi.org/10.1016/S1470-2045(07)70283-8
Hoffman D, Hoffman I, El-Bayoumy K. (2001) The less harmful cigarette: A controversial issue. A tribute to Ernst L. Wynder. Chem Res Toxicol, 14:767-790.
Instituto Brasileiro de Geografia e Estatística. (2009) National research by household sample. Methodology Notes. Accessed 02 January 2013. Available:http://www.ibge.gov.br/home/estatistica/populacao/trabalhoerendimento/pnad2009/pn ad_sintese_2009.pdf. Portuguese.
International Agency for Research on Cancer. (2004) Tobacco Smoke and involuntary smoking. IARC MonogrEvalCarcinog Risks Hum. 83; 2004. Accessed 02 January 2013. Available: http://www.monographs.iarc.fr/ENG/Monographs/vol38/volume38.pdf.
Marks MA, Gravitt PE, Burk RD, Studentsov Y, Farzadegan H, Klein SL. (2010) 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, 17:609–17. doi: 10.1128/CVI.00441-09. Epub 2010 Feb 3.
Marks MA, Viscidi RP, Chang K, Silver M, Burke A, Howard R, Gravitt PE. (2011) Differences in the concentration and correlation of cervical immune markers among HPV positive and negative perimenopausal women. Cytokine, 56:798–803. doi: 10.1016/j.cyto.2011.09.012. Epub 2011 Oct 19.
Ministério da Saúde/ Instituto Nacional de Câncer (Brasil). (2011) Diretrizes Brasileiras para o rastreamento Do Câncer Do Colo Do Útero. Accessed 09 September 2013. Available: http://www1.inca.gov.br/inca/Arquivos/Diretrizes_rastreamento_cancer_colo_utero.pdf
Ministério da Saúde/ Instituto Nacional do Câncer. Registro de Câncer de Base Populacional Accessed 09 September 2013. Available: http://www2.inca.gov.br/wps/wcm/connect/estatisticas/site/home/rcbp/
Moreno V, Bosch FX, Munoz N, Meijer CJ, Shah KV, Walboomers JM, Herrero R, Franceschi S. (2002) Effect of oral contraceptives on risk of cervical cancer in women with human papillomavirus infection: the IARC multicentric case-control study. Lancet, 359:1085–92. DOI: http://dx.doi.org/10.1016/S0140-6736(02)08150-3
Ruutu M, Wahlroos N, Syrjanen K, Johansson B, Syrjanen S. (2006) Effects of 17beta-estradiol and progesterone on transcription of human papillomavirus 16 E6/E7 oncogenes in CaSki and SiHa cell lines. Int J Gynecol Cancer, 16:1261–8. PMID:16803515
Shai A, Brake T, Somoza C, Lambert PF. (2007) The human papillomavirus E6 oncogene dysregulates the cell cycle and contributes to cervical carcinogenesis through two independent activities. Cancer Res, 67:1626–35. doi: 10.1158/0008-5472.CAN-06-3344
Silva IF, Koifman RJ, Mattos IE. (2009) Epidemiological characteristics related to treatment failure of preinvasive cervical intraepithelial neoplasia among Brazilian women. Int J Gynecol Cancer, 19(8):1427-31. doi: 10.1111/IGC.0b013e3181b8677f.
Solomon D, Davey D, Kurman R, Moriarty A, O'Connor D, Prey M. (2002) The 2001 Bethesda System: Terminology for Reporting Results of Cervical Cytology. Journal of the American Medical Association, 287(16):2114-2119. PMID: 11966386. doi:10.1001/jama.287.16.2114.
Soutter WP, Sasieni P, Panoskaltsis T. (2006) Long-term risk of invasive cervical cancer after treatment of squamous cervical intraepithelial neoplasia. Int J Cancer, 118(8):2048–55.
Stafl A, Wilbanks GD. (1991) An international terminology of colposcopy: Report of the nomenclature committee of the International Federation of Cervical Pathology and Colposcopy. Obstetrics and Gynecology, 77:313-314. PMID:1988900
Trushin N, Alam S, El-Bayoumy K, Krzeminski J, Amin SG, Gullet J, Meyers C, Prokopczyk B. (2012) Comparative metabolism of benzo[a]pyrene by human keratinocytes infected with high-risk human papillomavirus type 16 and 18 as episomal or integrated genomes. Journal of Carnogenesis. Online version assessed on [September 18, 2013]: http://www.carcinogenesis.com doi: 10.4103/1477-3163.92309
Woodman CB, Collins SI, Young LS. (2007) The natural history of cervical HPV infection: unresolved issues. Nat Rev Cancer, 7(1):11-22. doi:10.1038/nrc2050
World Health Organization. (2005) Cervical Cancer Screening in Developing Countries. A report of WHO Consultation. Word Health Organization: Geneva; 2005.
Zardo LM, Thuler LC, Zeferino LC, Horta NM, Fonseca R de C. (2009) Performance of the cytologic examination for the diagnosis of endocervical adenocarcinoma in situ: cytologic-histologic correlation in 60 cases. ActaCytol, 53(5):558-64. PMID19798884
Zielinski GD, Bais AG, Helmerhorst TJ, Verheijen RH, de Schipper FA, Snijders PJ, Voorhorst FJ, van Kemenade FJ, Rozendaal L, Meijer CJ. (2004) HPV testing and monitoring of women after treatment of CIN 3: review of the literature and meta-analysis. Obstet Gynecol, Surv.59(7):543–53. PMID:15199273