CC BY 4.0 · Rev Bras Ginecol Obstet 2022; 44(07): 678-685
DOI: 10.1055/s-0042-1743163
Original Article
Lower Genital Tract Diseases

Cytology-based Screening for Anal Intraepithelial Neoplasia in Immunocompetent Brazilian Women with a History of High-Grade Cervical Intraepithelial Neoplasia or Cancer

Triagem citológica de neoplasia intraepitelial anal em mulheres brasileiras imunocompetentes com histórico de neoplasia intraepitelial cervical de alto grau ou câncer
1   Lower Genital Tract Pathology and Colposcopy Service, Gynecology Department, Hospital Universitário da Universidade Federal de Juiz de Fora (UH-UFJF), Juiz de Fora, MG, Brazil
,
1   Lower Genital Tract Pathology and Colposcopy Service, Gynecology Department, Hospital Universitário da Universidade Federal de Juiz de Fora (UH-UFJF), Juiz de Fora, MG, Brazil
,
1   Lower Genital Tract Pathology and Colposcopy Service, Gynecology Department, Hospital Universitário da Universidade Federal de Juiz de Fora (UH-UFJF), Juiz de Fora, MG, Brazil
,
1   Lower Genital Tract Pathology and Colposcopy Service, Gynecology Department, Hospital Universitário da Universidade Federal de Juiz de Fora (UH-UFJF), Juiz de Fora, MG, Brazil
,
1   Lower Genital Tract Pathology and Colposcopy Service, Gynecology Department, Hospital Universitário da Universidade Federal de Juiz de Fora (UH-UFJF), Juiz de Fora, MG, Brazil
› Author Affiliations

Abstract

Objective To determine the prevalence and possible variables associated with anal intraepithelial neoplasia and anal cancer in immunocompetent women with high-grade cervical intraepithelial neoplasia.

Methods A cross-sectional study involving immunocompetent women with a histological diagnosis of high-grade cervical intraepithelial neoplasia and cervical cancer, conducted between January 2016 and September 2020. All women underwent anal cytology and answered a questionnaire on characterization and potential risk factors. Women with altered cytology were submitted to anoscopy and biopsy.

Results A total of 69 women were included in the study. Of these, 7 (10.1%) had abnormal anal cytology results: (high-grade lesion, atypical squamous cells of undetermined significance, and atypical squamous cells, cannot exclude high-grade lesions: 28,5% each; low grade lesion: 14,3%). Of the anoscopies, 3 (42.8%) showed alterations. Of the 2 (28,5% of all abnormal cytology results) biopsies performed, only 1 showed low-grade anal intraepithelial neoplasia. The average number of pregnancies, vaginal deliveries, and abortions was associated with abnormal anal cytology. However, the highest mean regarding the cesarean sections was associated with normal cytology.

Conclusion The prevalence of anal intraepithelial neoplasia was compatible with data from recent studies, especially those conducted in Brazil. Opportunistic screening for anal intraepithelial neoplasia in this high-risk population should be considered. Anal cytology is suitable for this purpose, due to its low cost and feasibility in public health services.

Resumo

Objetivo Determinar a prevalência e as possíveis variáveis associadas à neoplasia intraepitelial anal e ao câncer anal em mulheres imunocompetentes com neoplasia intraepitelial cervical de alto grau.

Métodos Estudo transversal em mulheres imunocompetentes com diagnóstico histológico de neoplasia intraepitelial cervical de alto grau e câncer cervical, feito entre janeiro de 2016 e setembro de 2020. Todas as mulheres foram submetidas a citologia anal e responderam a um questionário de caracterização e potenciais fatores de risco. Mulheres com citologia alterada foram submetidas a anuscopia e biópsia.

Resultados No total, 69 mulheres foram incluídas no estudo. Destas, 7 (10,1%) tiveram resultados anormais de citologia anal (lesão de alto grau, células escamosas atípicas de significado indeterminado, e células escamosas atípicas, não se pode excluir lesões de alto grau: 28,5% cada; lesão de baixo grau: 14,3%). Das anuscopias, 3 (42,8%) demonstraram alterações. Das 2 biópsias realizadas, apenas 1 apresentou neoplasia intraepitelial anal de baixo grau. O número médio de gestações, partos vaginais e abortos estava associado à citologia anal anormal. No entanto, a maior média de partos cesáreos estava associada à citologia normal.

Conclusão A prevalência de neoplasia intraepitelial anal foi compatível com dados de estudos recentes, principalmente daqueles feitos no Brasil. O rastreamento oportunista para neoplasia intraepitelial anal nesta população de alto risco deve ser considerado. A citologia anal é adequada para esse fim, devido ao seu baixo custo e viabilidade nos serviços públicos de saúde.

Contributions

VORB; ICGL; DGD; and ASOT: designed the study. VORB; ASOT; and GDP: performed all the data collection. VORB; ICGL; and DGD: analyzed and interpreted the data. VORB: drafed the article. ICGL; and DGD: performed the critical revision of the article. All authors approved the final version to be published.




Publication History

Received: 09 August 2021

Accepted: 17 December 2021

Article published online:
08 August 2022

© 2022. Federação Brasileira de Ginecologia e Obstetrícia. This is an open access article published by Thieme under the terms of the Creative Commons Attribution License, permitting unrestricted use, distribution, and reproduction so long as the original work is properly cited. (https://creativecommons.org/licenses/by/4.0/)

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  • References

  • 1 Donaire C, Reillo M, Martínez-Escoriza JC, López-Fernández JA. Anal study in immunocompetent women with human papillomavirus related lower genital tract pathology. Eur J Obstet Gynecol Reprod Biol 2017; 211: 15-20 DOI: 10.1016/j.ejogrb.2017.01.023.
  • 2 Kost BP, Hofmann J, Stoellnberger S, Bergauer F, Blankenstein T, Alba-Alejandre I. et al. Prevalence of human papillomavirus infection of the anal canal in women: A prospective analysis of high-risk populations. Oncol Lett 2017; 13 (04) 2495-2501 DOI: 10.3892/ol.2017.5714.
  • 3 World Health Organization. International Agency for Research on Cancer. World [Internet]. 2018 [cited 2019 Dec 16]. Available from: https://gco.iarc.fr/today/data/factsheets/populations/900-world-fact-sheets.pdf
  • 4 National Cancer Institute. Surveillance, Epidemiology, and End Results Program. Cancer of the anus, anal canal, and anorectum: cancer stat facts [Internet]. 2018. [cited 2019 Dec 16]. Available from: https://seer.cancer.gov/statfacts/html/anus.html Surveillance, Epidemiology, and End Results Program
  • 5 Ministério da Saúde. Instituto Nacional de Câncer. [Types of cancer: anal cancer] [Internet]. 2018 [cited 2019 Nov 23]. Available from: https://www.inca.gov.br/tipos-de-cancer/cancer-anal. Portuguese.
  • 6 De Vuyst H, Clifford GM, Nascimento MC, Madeleine MM, Franceschi S. Prevalence and type distribution of human papillomavirus in carcinoma and intraepithelial neoplasia of the vulva, vagina and anus: a meta-analysis. Int J Cancer 2009; 124 (07) 1626-1636 DOI: 10.1002/ijc.24116.
  • 7 Fokom Domgue J, Messick C, Milbourne A, Guo M, Salcedo MP, Dahlstrom KR. et al. Prevalence of high-grade anal dysplasia among women with high-grade lower genital tract dysplasia or cancer: Results of a pilot study. Gynecol Oncol 2019; 153 (02) 266-270 DOI: 10.1016/j.ygyno.2019.02.024.
  • 8 Machalek DA, Poynten M, Jin F, Fairley CK, Farnsworth A, Garland SM. et al. Anal human papillomavirus infection and associated neoplastic lesions in men who have sex with men: a systematic review and meta-analysis. Lancet Oncol 2012; 13 (05) 487-500 DOI: 10.1016/S1470-2045(12)70080-3.
  • 9 Gilbert DC, Wakeham K, Langley RE, Vale CL. Increased risk of second cancers at sites associated with HPV after a prior HPV-associated malignancy, a systematic review and meta-analysis. Br J Cancer 2019; 120 (02) 256-268 DOI: 10.1038/s41416-018-0273-9.
  • 10 Jacyntho CM, Giraldo PC, Horta AA, Grandelle R, Gonçalves AK, Fonseca T. et al. Association between genital intraepithelial lesions and anal squamous intraepithelial lesions in HIV-negative women. Am J Obstet Gynecol 2011; 205 (02) 115.e1-115.e5 DOI: 10.1016/j.ajog.2011.03.011.
  • 11 Lammé J, Pattaratornkosohn T, Mercado-Abadie J, Alkhas A, Robinson A, Lanneau G. Concurrent anal human papillomavirus and abnormal anal cytology in women with known cervical dysplasia. Obstet Gynecol 2014; 124 (2 Pt 1): 242-248 DOI: 10.1097/AOG.0000000000000370.
  • 12 Park IU, Ogilvie Jr JW, Anderson KE, Li ZZ, Darrah L, Madoff R. et al. Anal human papillomavirus infection and abnormal anal cytology in women with genital neoplasia. Gynecol Oncol 2009; 114 (03) 399-403 DOI: 10.1016/j.ygyno.2009.05.008.
  • 13 Santoso JT, Long M, Crigger M, Wan JY, Haefner HK. Anal intraepithelial neoplasia in women with genital intraepithelial neoplasia. Obstet Gynecol 2010; 116 (03) 578-582 DOI: 10.1097/aog.0b013e3181ea1834.
  • 14 Scholefield JH, Hickson WG, Smith JH, Rogers K, Sharp F. Anal intraepithelial neoplasia: part of a multifocal disease process. Lancet 1992; 340 (8830): 1271-1273 DOI: 10.1016/0140-6736(92)92961-e.
  • 15 American Cancer Society. Can anal cancer be found early? [Internet]. 2018 [cited 2019 Oct 25]. Available from: https://www.cancer.org/cancer/anal-cancer/detection-diagnosis-staging/detection.html
  • 16 Federação Brasileira das Associações de Ginecologia e Obstetrícia. [Guidance manual on lower genital tract and colposcopy]. São Paulo: Febrasgo; 2010. Portuguese.
  • 17 Wohlmuth C, Ghorab Z, Shier M, Tinmouth J, Salit IE, Covens A. et al. Cytology-based screening for anal intraepithelial neoplasia in women with a history of cervical intraepithelial neoplasia or cancer. Cancer Cytopathol 2021; 129 (02) 140-147 DOI: 10.1002/cncy.22360.
  • 18 Goodman MT, Shvetsov YB, McDuffie K, Wilkens LR, Zhu X, Ning L. et al. Acquisition of anal human papillomavirus (HPV) infection in women: the Hawaii HPV Cohort study. J Infect Dis 2008; 197 (07) 957-966 DOI: 10.1086/529207.
  • 19 Richel O, Prins JM, de Vries HJ. Screening for anal cancer precursors: what is the learning curve for high-resolution anoscopy?. AIDS 2014; 28 (09) 1376-1377 DOI: 10.1097/QAD.0000000000000227.
  • 20 Heráclio SA, de Souza ASR, de Souza PRE, Katz L, Lima Júnior SF, Amorim MMR. Cross-sectional study of anal intraepithelial lesions in women with cervical neoplasia without HIV. Int J Gynaecol Obstet 2018; 140 (02) 233-240 DOI: 10.1002/ijgo.12367.
  • 21 D'Hauwers KW, Tjalma WA. Letter to the Editor referring to the manuscript entitled: “Human papillomavirus DNA and mRNA positivity of the anal canal in women with lower genital tract HPV lesions: predictors and clinical implications.” reported by Valari O, et al., (Gynecol Oncol 2011; 122(3): 505-8). Gynecol Oncol 2012; 126 (03) 499 , author reply 500 DOI: 10.1016/j.ygyno.2012.04.043.
  • 22 Mathews WC, Agmas W, Cachay E. Comparative accuracy of anal and cervical cytology in screening for moderate to severe dysplasia by magnification guided punch biopsy: a meta-analysis. PLoS One 2011; 6 (09) e24946 DOI: 10.1371/journal.pone.0024946.
  • 23 Tejada CA, Triaca LM, da Costa FK, Hellwig F. The sociodemographic, behavioral, reproductive, and health factors associated with fertility in Brazil. PLoS One 2017; 12 (02) e0171888 DOI: 10.1371/journal.pone.0171888.
  • 24 Capobiango A, Silva Filho AL, Nunes TA. Anal HPV diagnosis in women with cin: anus cancer prevention? diagnóstico de hpv anal em mulheres com NIC: prevenção de câncer do ânus?. Rev Bras Coloproctol 2009; 29 (04) 443-450 DOI: 10.1590/S0101-98802009000400002.
  • 25 do Socorro Nobre M, Jacyntho CM, Eleutério Jr J, Giraldo PC, Gonçalves AK. Abnormal anal cytology risk in women with known genital squamous intraepithelial lesion. Braz J Infect Dis 2016; 20 (03) 294-297 DOI: 10.1016/j.bjid.2016.01.008.
  • 26 Cronin B, Bregar A, Luis C, Schechter S, Disilvestro P, Pisharodi L. et al. Evaluation of anal cytology and dysplasia in women with a history of lower genital tract dysplasia and malignancy. Gynecol Oncol 2016; 141 (03) 492-496 DOI: 10.1016/j.ygyno.2016.04.015.
  • 27 Jensen KE, Schmiedel S, Norrild B, Frederiksen K, Iftner T, Kjaer SK. Parity as a cofactor for high-grade cervical disease among women with persistent human papillomavirus infection: a 13-year follow-up. Br J Cancer 2013; 108 (01) 234-239 DOI: 10.1038/bjc.2012.5.
  • 28 Castle PE. Beyond human papillomavirus: the cervix, exogenous secondary factors, and the development of cervical precancer and cancer. J Low Genit Tract Dis 2004; 8 (03) 224-230 DOI: 10.1097/00128360-200407000-00011.
  • 29 Williams VM, Filippova M, Soto U, Duerksen-Hughes PJ. HPV-DNA integration and carcinogenesis: putative roles for inflammation and oxidative stress. Future Virol 2011; 6 (01) 45-57 DOI: 10.2217/fvl.10.73.
  • 30 Krzowska-Firych J, Lucas G, Lucas C, Lucas N, Pietrzyk Ł. An overview of Human Papillomavirus (HPV) as an etiological factor of the anal cancer. J Infect Public Health 2019; 12 (01) 1-6 DOI: 10.1016/j.jiph.2018.06.005.
  • 31 Hunter MI, Monk BJ, Tewari KS. Cervical neoplasia in pregnancy. Part 1: screening and management of preinvasive disease. Am J Obstet Gynecol 2008; 199 (01) 3-9 DOI: 10.1016/j.ajog.2008.04.010.
  • 32 Oliveira RR, Melo EC, Novaes ES, Ferracioli PL, Mathias TA. Factors associated to Caesarean delivery in public and private health care systems. Rev Esc Enferm USP 2016; 50 (05) 733-740 DOI: 10.1590/s0080-623420160000600004.
  • 33 Habel MA, Leichliter JS, Dittus PJ, Spicknall IH, Aral SO. Heterosexual anal and oral sex in adolescents and adults in the United States, 2011–2015. Sex Transm Dis 2018; 45 (12) 775-782 DOI: 10.1097/OLQ.0000000000000889.
  • 34 Stier EA, Sebring MC, Mendez AE, Ba FS, Trimble DD, Chiao EY. Prevalence of anal human papillomavirus infection and anal HPV-related disorders in women: a systematic review. Am J Obstet Gynecol 2015; 213 (03) 278-309 DOI: 10.1016/j.ajog.2015.03.034.
  • 35 Roberts JR, Siekas LL, Kaz AM. Anal intraepithelial neoplasia: A review of diagnosis and management. World J Gastrointest Oncol 2017; 9 (02) 50-61 DOI: 10.4251/wjgo.v9.i2.50.
  • 36 Davis KG, Orangio GR. Basic science, epidemiology, and screening for anal intraepithelial neoplasia and its relationship to anal squamous cell cancer. Clin Colon Rectal Surg 2018; 31 (06) 368-378 DOI: 10.1055/s-0038-1668107.
  • 37 Valari O, Koliopoulos G, Karakitsos P, Valasoulis G, Founta C, Godevenos D. et al. Human papillomavirus DNA and mRNA positivity of the anal canal in women with lower genital tract HPV lesions: predictors and clinical implications. Gynecol Oncol 2011; 122 (03) 505-508 DOI: 10.1016/j.ygyno.2011.05.033.
  • 38 Damay A, Fabre J, Costes V, Didelot JM, Didelot MN, Boulle N. et al. Human papillomavirus (HPV) prevalence and type distribution, and HPV-associated cytological abnormalities in anal specimens from men infected with HIV who have sex with men. J Med Virol 2010; 82 (04) 592-596 DOI: 10.1002/jmv.21732.
  • 39 Nathan M, Singh N, Garrett N, Hickey N, Prevost T, Sheaff M. Performance of anal cytology in a clinical setting when measured against histology and high-resolution anoscopy findings. AIDS 2010; 24 (03) 373-379 DOI: 10.1097/QAD.0b013e328333ab8e.
  • 40 Moscicki AB, Darragh TM, Berry-Lawhorn JM, Roberts JM, Khan MJ, Boardman LA. et al. Screening for anal cancer in women. J Low Genit Tract Dis 2015; 19 (3, Suppl 1) S27-S42 DOI: 10.1097/LGT.0000000000000117.
  • 41 Machalek DA, Poynten IM, Jin F, Hillman RJ, Templeton DJ, Law C. et al; SPANC study team. A Composite Cytology-Histology Endpoint Allows a More Accurate Estimate of Anal High Grade Squamous Intraepithelial Lesion Prevalence. Cancer Epidemiol Biomarkers Prev 2016; 25 (07) 1134-1143 DOI: 10.1158/1055-9965.EPI-15-1106.