Chunqing Lin1, Jiri Slama2, Paula Gonzalez3, Marc T Goodman4, Ningshao Xia5, Aimée R Kreimer6, Ting Wu5, Nancy A Hessol7, Yurii Shvetsov8, Ana P Ortiz9, Beatriz Grinsztejn10, Anna-Barbara Moscicki11, Isabelle Heard12, María Del Refugio González Losa13, Erna M Kojic14, Maarten F Schim van der Loeff15, Feixue Wei5, Adhemar Longatto-Filho16, Zizipho A Mbulawa17, Joel M Palefsky7, Annette H Sohn18, Brenda Y Hernandez8, Katina Robison19, Steve Simpson20, Lois J Conley21, Alexandra de Pokomandy22, Marianne A B van der Sande23, Racheal S Dube Mandishora24, Lays P B Volpini25, Alessandra Pierangeli26, Byron Romero3, Timothy Wilkin27, Silvia Franceschi28, Carmen Hidalgo-Tenorio29, Reshmie A Ramautarsing30, Ina U Park31, Fernanda K Tso32, Sheela Godbole33, Kathleen W M D'Hauwers34, Borek Sehnal2, Lynette J Menezes35, Sandra A Heráclio36, Gary M Clifford37. 1. International Agency for Research on Cancer, Lyon, France; National Cancer Center, National Clinical Research Center for Cancer, and Cancer Hospital Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing, China. 2. Department of Gynecology and Obstetrics, General University Hospital and First Faculty of Medicine, Charles University, Prague, Czech Republic. 3. Proyecto Epidemiológico Guanacaste, Fundación INCIENSA, San José, Costa Rica. 4. Samuel Oschin Comprehensive Cancer Institute, Cedars Sinai Medical Center, Los Angeles, CA, USA. 5. State Key Laboratory of Molecular Vaccinology and Molecular Diagnostics, National Institute of Diagnostics and Vaccine Development in Infectious Diseases, School of Public Health, Xiamen University, Xiamen, Fujian, China. 6. National Cancer Institute, National Institutes of Health, Bethesda, MD, USA. 7. University of California, San Francisco, CA, USA. 8. University of Hawaii Cancer Center, Honolulu, Hawaii, USA. 9. University of Puerto Rico Comprehensive Cancer Center, Department of Biostatistics and Epidemiology, Graduate School of Public Health, UPR, San Juan, Puerto Rico. 10. Instituto Nacional de Infectologia Evandro Chagas-Fiocruz, Rio de Janeiro, Brazil. 11. David Geffen School of Medicine, University of California, Los Angeles, CA, USA. 12. Department of Endocrinology and Reproductive Medicine, IE3M, Groupe Hospitalier Pitié-Salpêtrière, Assistance Publique, Hôpitaux de Paris, Paris, France. 13. Dr Hideyo Noguchy Center of Regional Investigations, Autonomous University of Yucatán, Mérida, Yucatán, México. 14. Mount Sinai West and St Luke's Hospitals, New York, NY, USA. 15. Department of Infectious Diseases, Infectious Diseases Research & Prevention, GGD Amsterdam, Netherlands. 16. Research Institute of Life and Health Sciences, School of Medicine, University of Minho, Braga, Portugal; 3B's (Biomaterials, Biodegradables and Biomimetics) Research Group, Portugal Government Associate Laboratory, Braga, Portugal; Laboratory of Medical Investigation 14, Department of Pathology, Faculty of Medicine, University of São Paulo, São Paulo, Brazil; Teaching and Research Institute, Molecular Oncology Research Center, Barretos Cancer Hospital-Pio XII Foundation, Barretos, Brazil. 17. Institute of Infectious Disease and Molecular Medicine, University of Cape Town, Cape Town, South Africa; Department of Pathology, Division of Medical Virology, University of Cape Town, Cape Town, South Africa; Centre for HIV and STIs, National Institute for Communicable Diseases, National Health Laboratory Service, Johannesburg, South Africa; South African Medical Research Council Gynaecological Cancer Research Centre, University of Cape Town, Cape Town, South Africa. 18. TREAT Asia/amfAR-Foundation for AIDS Research, Thai Red Cross AIDS Research Centre, Bangkok, Thailand. 19. Obstetrics & Gynecology and Medicine, The Warren Alpert Medical School of Brown University, Providence, RI, USA. 20. Menzies Institute for Medical Research, University of Tasmania, Hobart, Tasmania, Australia. 21. Division of HIV/AIDS Prevention, Epidemiology Research Team, Centers for Disease Control and Prevention, Atlanta, GA, USA. 22. Chronic Viral Illness Service, McGill University Health Centre and Department of Family Medicine, McGill University, Montreal, QC, Canada. 23. Public Health Epidemiology, Head Department Public Health, Institute of Tropical Medicine, Antwerp, Belgium. 24. Department of Medical Microbiology, University of Zimbabwe College of Health Sciences, Parirenyatwa Hospital premises, Harare, Zimbabwe. 25. Health Sciences Center, Federal University of Espírito Santo, Vitória, Brazil. 26. Department of Molecular Medicine, Sapienza University of Rome, Rome, Italy. 27. Weill Cornell Medicine, New York, NY, USA. 28. Aviano Cancer Center, Aviano, Italy. 29. Infectious Diseases Service, University Hospital Virgen de las Nieves, Granada, Spain. 30. Thai Red Cross AIDS Research Centre, Bangkok, Thailand. 31. Department of Family and Community Medicine, University of California San Francisco School of Medicine, San Francisco, CA, USA. 32. Department of Gynecology of the Federal University of São Paulo, São Paulo, Brazil. 33. Division of Epidemiology and Biostatistics, ICMR-National AIDS Research Institute, Indian Council of Medical Research, Pune, India. 34. Radboud University Nijmegen, Medical Centre, Department of Urology, Nijmegen, Netherlands. 35. Division of Infectious Disease, University of South Florida, Tampa, FL, USA. 36. Women's Healthcare Center, Instituto de Medicina Integral Professor Fernando Figueira, Recife, PE, Brazil; Cytopathology Division, Public Health Laboratory of the State of Pernambuco, Recife, PE, Brazil. 37. International Agency for Research on Cancer, Lyon, France. Electronic address: cliffordg@iarc.fr.
Abstract
BACKGROUND: Cervical cancer screening might contribute to the prevention of anal cancer in women. We aimed to investigate if routine cervical cancer screening results-namely high-risk human papillomavirus (HPV) infection and cytohistopathology-predict anal HPV16 infection, anal high-grade squamous intraepithelial lesions (HSIL) and, hence, anal cancer. METHODS: We did a systematic review of MEDLINE, Embase, and the Cochrane library for studies of cervical determinants of anal HPV and HSIL published up to Aug 31, 2018. We centrally reanalysed individual-level data from 13 427 women with paired cervical and anal samples from 36 studies. We compared anal high-risk HPV prevalence by HIV status, cervical high-risk HPV, cervical cytohistopathology, age, and their combinations, using prevalence ratios (PR) and 95% CIs. Among 3255 women with anal cytohistopathology results, PRs were similarly calculated for all anal HSIL and HPV16-positive anal HSIL. FINDINGS: Cervical and anal HPV infections were highly correlated. In HIV-negative women, anal HPV16 prevalence was 41% (447/1097) in cervical HPV16-positive versus 2% (214/8663) in cervical HPV16-negative women (PR 16·5, 95% CI 14·2-19·2, p<0·0001); these values were 46% (125/273) versus 11% (272/2588) in HIV-positive women (4·4, 3·7-5·3, p<0·0001). Anal HPV16 was also associated with cervical cytohistopathology, with a prevalence of 44% [101/228] for cervical cancer in HIV-negative women (PR vs normal cytology 14·1, 11·1-17·9, p<0·0001). Anal HSIL was associated with cervical high-risk HPV, both in HIV-negative women (from 2% [11/527] in cervical high-risk HPV-negative women up to 24% [33/138] in cervical HPV16-positive women; PR 12·9, 95% CI 6·7-24·8, p<0·0001) and HIV-positive women (from 8% [84/1094] to 17% [31/186]; 2·3, 1·6-3·4, p<0·0001). Anal HSIL was also associated with cervical cytohistopathology, both in HIV-negative women (from 1% [5/498] in normal cytology up to 22% [59/273] in cervical HSIL; PR 23·1, 9·4-57·0, p<0·0001) and HIV-positive women (from 7% [105/1421] to 25% [25/101]; 3·6, 2·5-5·3, p<0·0001). Prevalence of HPV16-positive anal HSIL was 23-25% in cervical HPV16-positive women older than 45 years (5/20 in HIV-negative women, 12/52 in HIV-positive women). INTERPRETATION: HPV-based cervical cancer screening programmes might help to stratify anal cancer risk, irrespective of HIV status. For targeted secondary anal cancer prevention in high-risk groups, HIV-negative women with cervical HPV16, especially those older than 45 years, have a similar anal cancer risk profile to that of HIV-positive women. FUNDING: International Agency for Research on Cancer.
BACKGROUND:Cervical cancer screening might contribute to the prevention of anal cancer in women. We aimed to investigate if routine cervical cancer screening results-namely high-risk human papillomavirus (HPV) infection and cytohistopathology-predict anal HPV16 infection, anal high-grade squamous intraepithelial lesions (HSIL) and, hence, anal cancer. METHODS: We did a systematic review of MEDLINE, Embase, and the Cochrane library for studies of cervical determinants of anal HPV and HSIL published up to Aug 31, 2018. We centrally reanalysed individual-level data from 13 427 women with paired cervical and anal samples from 36 studies. We compared anal high-risk HPV prevalence by HIV status, cervical high-risk HPV, cervical cytohistopathology, age, and their combinations, using prevalence ratios (PR) and 95% CIs. Among 3255 women with anal cytohistopathology results, PRs were similarly calculated for all anal HSIL and HPV16-positive anal HSIL. FINDINGS: Cervical and anal HPV infections were highly correlated. In HIV-negative women, anal HPV16 prevalence was 41% (447/1097) in cervical HPV16-positive versus 2% (214/8663) in cervical HPV16-negative women (PR 16·5, 95% CI 14·2-19·2, p<0·0001); these values were 46% (125/273) versus 11% (272/2588) in HIV-positive women (4·4, 3·7-5·3, p<0·0001). Anal HPV16 was also associated with cervical cytohistopathology, with a prevalence of 44% [101/228] for cervical cancer in HIV-negative women (PR vs normal cytology 14·1, 11·1-17·9, p<0·0001). Anal HSIL was associated with cervical high-risk HPV, both in HIV-negative women (from 2% [11/527] in cervical high-risk HPV-negative women up to 24% [33/138] in cervical HPV16-positive women; PR 12·9, 95% CI 6·7-24·8, p<0·0001) and HIV-positive women (from 8% [84/1094] to 17% [31/186]; 2·3, 1·6-3·4, p<0·0001). Anal HSIL was also associated with cervical cytohistopathology, both in HIV-negative women (from 1% [5/498] in normal cytology up to 22% [59/273] in cervical HSIL; PR 23·1, 9·4-57·0, p<0·0001) and HIV-positive women (from 7% [105/1421] to 25% [25/101]; 3·6, 2·5-5·3, p<0·0001). Prevalence of HPV16-positive anal HSIL was 23-25% in cervical HPV16-positive women older than 45 years (5/20 in HIV-negative women, 12/52 in HIV-positive women). INTERPRETATION:HPV-based cervical cancer screening programmes might help to stratify anal cancer risk, irrespective of HIV status. For targeted secondary anal cancer prevention in high-risk groups, HIV-negative women with cervical HPV16, especially those older than 45 years, have a similar anal cancer risk profile to that of HIV-positive women. FUNDING: International Agency for Research on Cancer.
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