Incidence and Clearance of Anal Human Papillomavirus Infection in 16 164 Individuals, According to Human Immunodeficiency Virus Status, Sex, and Male Sexuality: An International Pooled Analysis of 34 Longitudinal Studies

Author:

Wei Feixue1ORCID,Goodman Marc T2,Xia Ningshao3ORCID,Zhang Jun3ORCID,Giuliano Anna R4,D’Souza Gypsyamber5,Hessol Nancy A6,Schim van der Loeff Maarten F7,Dai Jianghong8,Neukam Karin9ORCID,de Pokomandy Alexandra10,Poynten I Mary11,Geskus Ronald B1213,Burgos Joaquin1415,Etienney Isabelle16,Moscicki Anna-Barbara17,Donà Maria Gabriella18,Gillison Maura L19,Nyitray Alan G20,Nowak Rebecca G21,Yunihastuti Evy22,Zou Huachun2324,Hidalgo-Tenorio Carmen25,Phanuphak Nittaya26,Molina Jean-Michel27,Schofield Alice M28,Kerr Stephen29,Fan Song30,Lu Yong31,Ong Jason J32,Chikandiwa Admire T33,Teeraananchai Sirinya34,Squillace Nicola35,Wiley Dorothy J36,Palefsky Joel M37,Georges Damien1,Alberts Catharina J1,Clifford Gary M1ORCID

Affiliation:

1. Early Detection, Prevention and Infections Branch, International Agency for Research on Cancer (IARC/WHO) , Lyon , France

2. Cancer Prevention and Control Program, Cedars Cancer, Cedars-Sinai Medical Center , Los Angeles, California , USA

3. 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

4. Center for Immunization and Infection Research in Cancer (CIIRC), Moffitt Cancer Center , Tampa, Florida , USA

5. Department of Epidemiology, Johns Hopkins Bloomberg School of Public Health , Baltimore, Maryland , USA

6. Department of Clinical Pharmacy, University of California San Francisco, California , USA

7. Department of Infectious Diseases, GGD Amsterdam , Amsterdam , Netherlands

8. School of Public Health, Xinjiang Medical University , Urumqi, Xinjiang , China

9. Unidad Clínica de Enfermedades Infecciosas y Medicina Preventiva, UCEIMP, Instituto de Biomedicina de Sevilla, CSIC, Universidad de Sevilla, Hospital Universitario Virgen del Rocío , Seville , Spain

10. Chronic Viral Illness Service, McGill University Health Centre and Department of Family Medicine, McGill University , Montreal, Quebec , Canada

11. The Kirby Institute, University of New South Wales , Kensington, Sydney, New South Wales , Australia

12. Oxford University Clinical Research Unit , Ho Chi Minh City , Vietnam

13. Centre for Tropical Medicine and Global Health, University of Oxford , Oxford , UK

14. Infectious Diseases Department, Hospital Universitari Vall d’Hebron , Barcelona , Spain

15. Vall d’Hebron Institut de Recerca (VHIR), Universitat Autónoma de Barcelona , Barcelona , Spain

16. Proctology, Diaconesses-Croix Saint Simon Hospital , Paris , France

17. Department of Pediatrics, University of California , Los Angeles, California , USA

18. Sexually Transmitted Infections (STI)/HIV Unit, San Gallicano Dermatological Institute IRCCS , Rome , Italy

19. Thoracic Head and Neck Medical Oncology Department, University of Texas MD Anderson Cancer Center , Houston, Texas , USA

20. Center for AIDS Intervention Research and Clinical Cancer Center, Medical College of Wisconsin , Milwaukee, Wisconsin , USA

21. Institute of Human Virology, University of Maryland School of Medicine , Baltimore, Maryland , USA

22. Faculty of Medicine Universitas Indonesia/Cipto Mangunkusumo Hospital , Jakarta , Indonesia

23. School of Public Health (Shenzhen), Sun Yat-sen University , Shenzhen , China

24. Kirby Institute, University of New South Wales , Sydney , Australia

25. Early Clinical Trial Unit. Biosanitary Institute (IBS.Granada). Infectious Diseases Unit. University Hospital Virgen de las Nieves , Granada , Spain

26. Institute of HIV Research and Innovation , Bangkok , Thailand

27. Department of Infectious diseases, University of Paris Cité, St-Louis Hospital , Paris , France

28. Institute of Cancer Sciences, The University of Manchester , Manchester , UK

29. HIV-NAT, Thai Red Cross AIDS Research Centre, and Research Affairs, Faculty of Medicine, Chulalongkorn University , Bangkok , Thailand

30. School of Public Health, Southwest Medical University , Luzhou , China

31. School of Public Health, the Key Laboratory of Environmental Pollution Monitoring and Disease Control, Ministry of Education, Guizhou Medical University , Guiyang , China

32. Central Clinical School, Monash University , Melbourne , Australia

33. Wits RHI, Faculty of Health Sciences, University of the Witwatersrand , Johannesburg , South Africa

34. Department of Statistics, Faculty of Science, Kasetsart University , Bangkok , Thailand

35. Infectious Diseases Unit ASST-Monza, San Gerardo Hospital-University of Milano-Bicocca , Monza , Italy

36. School of Nursing, University of California , Los Angeles, California , USA

37. Department of Medicine, University of California , San Francisco, California , USA

Abstract

Abstract Background Understanding the natural history of anal high-risk human papillomavirus (hrHPV) infection is key for designing anal cancer prevention programs but has not been systematically characterized. Methods We reanalyzed data from 34 studies including 16 164 individuals in 6 risk groups defined by human immunodeficiency virus (HIV) status, sex, and male sexuality: men who have sex with men (MSM) and people with HIV (MSMWH), HIV-negative MSM, women with HIV (WWH), HIV-negative women, men who have sex with women (MSW) with HIV (MSWWH), and HIV-negative MSW. We used Markov models to estimate incidence and clearance of 13 hrHPV types and their determinants. Results Human papillomavirus (HPV) 16 had the highest incidence-clearance ratio of the hrHPV types. MSMWH had the highest hrHPV incidence (eg, 15.5% newly HPV-16 infected within 2 years), followed by HIV-negative MSM (7.5%), WWH (6.6%), HIV-negative women (2.9%), MSWWH (1.7%), and HIV-negative MSW (0.7%). Determinants of HPV-16 incidence included HIV status and number of sexual partners for MSM, women, and MSW, and anal sex behavior for MSM only. HPV-16 clearance was lower for people with HIV (PWH) and lower for prevalent than incident infection. Among MSM, increasing age was associated with lower clearance of prevalent, but not incident, HPV-16 infection. Conclusions This robust and unifying analysis of anal hrHPV natural history is essential to designing and predicting the impact of HPV vaccination and HPV-based screening programs on anal cancer prevention, particularly in MSM and PWH. Importantly, it demonstrates the higher carcinogenic potential of longstanding anal prevalent hrHPV infection than more recent incident infection.

Publisher

Oxford University Press (OUP)

Subject

Infectious Diseases,Microbiology (medical)

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