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Epidemiology of anal human papillomavirus infection and high-grade squamous intraepithelial lesions in 29 900 men according to HIV status, sexuality, and age: a collaborative pooled analysis of 64 studies

Wei F 1 , Gaisa MM 2 , D'Souza G 3 , Xia N 4 , Giuliano AR 5 , Hawes SE 6 Show all authors , Gao L 7 , Cheng SH 8 , Donà MG 9 , Goldstone SE 10 , Schim van der Loeff MF 11 , Neukam K 12 , Meites E 13 , Poynten IM 14 , Dai J 15 , Combes JD 1 , Wieland U 16 , Burgos J 17 , Wilkin TJ 18 , Hernandez AL 19 , Iribarren Díaz M 20 , Hidalgo-Tenorio C 21 , Valencia Arredondo M 22 , Nyitray AG 23 , Wentzensen N 24 , Chow EP 25 , Smelov V 26 , Nowak RG 27 , Phanuphak N 28 , Woo YL 29 , Choi Y 30 , Hu Y 31 , Schofield AM 32 , Woestenberg PJ 33 , Chikandiwa AT 34 , Hickey AC 35 , de Pokomandy A 36 , Murenzi G 37 , Péré H 38 , Del Pino M 39 , Ortiz AP 40 , Charnot-Katsikas A 41 , Liu X 42 , Chariyalertsak S 43 , Strong C 44 , Ong JJ 45 , Yunihastuti E 46 , Etienney I 47 , Ferré VM 48 , Zou H 49 , Segondy M 50 , Chinyowa S 51 , Alberts CJ 1 , Clifford GM 52

Affiliations 

  • 1 Early Detection, Prevention and Infections Branch, International Agency for Research on Cancer (IARC/WHO), Lyon, France
  • 2 Department of Medicine, Division of Infectious Diseases, Icahn School of Medicine at Mount Sinai, New York, NY, USA
  • 3 Department of Epidemiology, Johns Hopkins Bloomberg School of Public Health, Baltimore, MD, USA
  • 4 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
  • 5 Center for Immunization and Infection Research in Cancer, Moffitt Cancer Center, Tampa, FL, USA
  • 6 Department of Epidemiology, Department of Health Services, and Department of Global Health, University of Washington, Seattle, WA, USA
  • 7 NHC Key Laboratory of Systems Biology of Pathogens, Institute of Pathogen Biology, and Center for Tuberculosis Research, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing, China
  • 8 Department of Infectious Diseases, Taoyuan General Hospital, Ministry of Health and Welfare, Taoyuan, Taiwan; School of Public Health, Taipei Medical University, Taipei, Taiwan
  • 9 Sexually Transmitted Infections/HIV Unit, San Gallicano Dermatological Institute, IRCCS, Rome, Italy
  • 10 Department of Surgery, Icahn School of Medicine at Mount Sinai, New York, NY, USA
  • 11 Department of Infectious Diseases, Public Health Service of Amsterdam, Amsterdam, Netherlands; Department of Internal Medicine, Amsterdam institute for Infection and Immunity, Amsterdam UMC, University of Amsterdam, Amsterdam, Netherlands
  • 12 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
  • 13 Division of Viral Diseases, Centers for Disease Control and Prevention, Atlanta, GA, USA
  • 14 Kirby Institute, University of New South Wales, Sydney, NSW, Australia
  • 15 School of Public Health, Xinjiang Medical University, Xinjiang, Urumqi, China
  • 16 Institute of Virology, University of Cologne, National Reference Center for Papilloma and Polyomaviruses, Cologne, Germany
  • 17 Department of infectious Diseases, Vall d'Hebron University Hospital, Barcelona, Spain
  • 18 Division of Infectious Diseases, Weill Cornell Medicine, New York, NY, USA
  • 19 Department of Medicine, University of California, San Francisco, CA, USA; Public Health Program, College of Education and Health Sciences, Touro University, Vallejo, CA, USA
  • 20 Department of Surgery, Complexo Hospitalario Universitario de Vigo-Hospital Álvaro Cunqueiro, Vigo, Spain
  • 21 Infectious Disease Unit, Biosanitary Research Institute Granada, University Hospital Virgen de las Nieves, Granada, Spain
  • 22 Universidad de Antioquia, Escuela de Microbiología, Grupo de investigación Salud Sexual y Cáncer, Medellín, Antioquia, Colombia
  • 23 Clinical Cancer Center and Center for AIDS Intervention Research, Medical College of Wisconsin, Milwaukee, WI, USA
  • 24 Division of Cancer Epidemiology and Genetics, National Cancer Institute, Bethesda, MD, USA
  • 25 Melbourne Sexual Health Centre, The Alfred Hospital, Melbourne, VIC, Australia; Central Clinical School, Monash University, Melbourne, VIC, Australia; Melbourne School of Population and Global Health, The University of Melbourne, Melbourne, VIC, Australia
  • 26 Early Detection, Prevention and Infections Branch, International Agency for Research on Cancer (IARC/WHO), Lyon, France; Division of Country Health Programmes, WHO Regional Office for Europe, Copenhagen, Denmark
  • 27 Institute of Human Virology, University of Maryland School of Medicine, Baltimore, MD, USA
  • 28 Institute of HIV Research and Innovation, Bangkok, Thailand; Center of Excellence in Transgender Health, Chulalongkorn University, Bangkok, Thailand
  • 29 Faculty of Medicine, University of Malaya, Kuala Lumpur, Malaysia
  • 30 Department of Immunology, University of Toronto, Toronto, ON, Canada
  • 31 Department of Child and Adolescent Health and Maternal Care, School of Public Health, Capital Medical University, Beijing, China
  • 32 Institute of Cancer Sciences, University of Manchester, Manchester, UK
  • 33 Center for Infectious Disease Control, National Institute for Public Health and the Environment, Bilthoven, Netherlands
  • 34 Wits RHI, Faculty of Health Sciences, University of the Witwatersrand, Johannesburg, South Africa
  • 35 Division of HIV/AIDS Prevention, Centers for Disease Control and Prevention, Nonthaburi, Thailand
  • 36 Chronic Viral Illness Service, McGill University Health Centre and Department of Family Medicine, McGill University, Montreal, QC, Canada
  • 37 Rwanda Military Hospital and Research for Development Rwanda, Kigali, Rwanda
  • 38 Assistance Publique Hôpitaux de Paris-Centre, Service de Microbiologie (Unité de virologie), Hôpital Européen Georges Pompidou, Paris, France; Centre de Recherche des Cordeliers, Sorbonne Université, Inserm, Université de Paris, Functional Genomics of Solid Tumors Laboratory, Equipe Labellisée Ligue Nationale contre le Cancer, Labex OncoImmunology, Paris, France
  • 39 Institute Clinic of Gynecology, Obstetrics, and Neonatology, Gynecology Oncology Unit, Hospital Clínic, Barcelona, Spain; Institut d'Investigacions Biomèdiques August Pi i Sunyer, Barcelona, Spain; Medicine Faculty, Barcelona University, Barcelona, Spain
  • 40 Cancer Control and Population Sciences Program, University of Puerto Rico Comprehensive Cancer Center, San Juan, PR, USA; Graduate School of Public Health, University of Puerto Rico, San Juan, PR, USA
  • 41 Department of Pathology, The University of Chicago, Chicago, IL, USA; MolDx Program, Palmetto GBA, Columbia, SC, USA
  • 42 Department of Epidemiology, School of Public Health, and the Key Laboratory of Public Health Safety of Ministry of Education, Fudan University, Shanghai, China
  • 43 Faculty of Public Health, Chiang Mai University and Research Institute for Health Sciences, Chiang Mai University, Chiang Mai, Thailand
  • 44 Department of Public Health, National Cheng Kung University Hospital, College of Medicine, National Cheng Kung University, Tainan, Taiwan
  • 45 Central Clinical School, Monash University, Melbourne, VIC, Australia
  • 46 Department of Internal Medicine, University of Indonesia, Jakarta, Indonesia
  • 47 Proctology, Diaconesses-Croix Saint Simon Hospital, Paris, France
  • 48 Université de Paris, Assistance Publique-Hôpitaux de Paris, Service de Virologie, Hôpital Bichat, Paris, France; Decision Science in Infectious Disease Prevention, Control and Care, INSERM, Université de Paris, Paris, France
  • 49 Kirby Institute, University of New South Wales, Sydney, NSW, Australia; School of Public Health (Shenzhen), Sun Yat-sen University, Shenzhen, China; School of Public Health, Shanghai Jiao Tong University, Shanghai, China; Melbourne Sexual Health Centre, Sydney, NSW, Australia
  • 50 Pathogenesis and Control of Chronic Infections, INSERM, CHU, University of Montpellier, Montpellier, France
  • 51 Department of Surgery, College of Health Sciences University of Zimbabwe, Harare, Zimbabwe
  • 52 Early Detection, Prevention and Infections Branch, International Agency for Research on Cancer (IARC/WHO), Lyon, France. Electronic address: cliffordg@iarc.fr
Lancet HIV, 2021 Sep;8(9):e531-e543.
PMID: 34339628 DOI: 10.1016/S2352-3018(21)00108-9

Abstract

BACKGROUND: Robust age-specific estimates of anal human papillomavirus (HPV) and high-grade squamous intraepithelial lesions (HSIL) in men can inform anal cancer prevention efforts. We aimed to evaluate the age-specific prevalence of anal HPV, HSIL, and their combination, in men, stratified by HIV status and sexuality.

METHODS: We did a systematic review for studies on anal HPV infection in men and a pooled analysis of individual-level data from eligible studies across four groups: HIV-positive men who have sex with men (MSM), HIV-negative MSM, HIV-positive men who have sex with women (MSW), and HIV-negative MSW. Studies were required to inform on type-specific HPV infection (at least HPV16), detected by use of a PCR-based test from anal swabs, HIV status, sexuality (MSM, including those who have sex with men only or also with women, or MSW), and age. Authors of eligible studies with a sample size of 200 participants or more were invited to share deidentified individual-level data on the above four variables. Authors of studies including 40 or more HIV-positive MSW or 40 or more men from Africa (irrespective of HIV status and sexuality) were also invited to share these data. Pooled estimates of anal high-risk HPV (HR-HPV, including HPV16, 18, 31, 33, 35, 39, 45, 51, 52, 56, 58, 59, and 68), and HSIL or worse (HSIL+), were compared by use of adjusted prevalence ratios (aPRs) from generalised linear models.

FINDINGS: The systematic review identified 93 eligible studies, of which 64 contributed data on 29 900 men to the pooled analysis. Among HIV-negative MSW anal HPV16 prevalence was 1·8% (91 of 5190) and HR-HPV prevalence was 6·9% (345 of 5003); among HIV-positive MSW the prevalences were 8·7% (59 of 682) and 26·9% (179 of 666); among HIV-negative MSM they were 13·7% (1455 of 10 617) and 41·2% (3798 of 9215), and among HIV-positive MSM 28·5% (3819 of 13 411) and 74·3% (8765 of 11 803). In HIV-positive MSM, HPV16 prevalence was 5·6% (two of 36) among those age 15-18 years and 28·8% (141 of 490) among those age 23-24 years (ptrend=0·0091); prevalence was 31·7% (1057 of 3337) among those age 25-34 years and 22·8% (451 of 1979) among those age 55 and older (ptrend<0·0001). HPV16 prevalence in HIV-negative MSM was 6·7% (15 of 223) among those age 15-18 and 13·9% (166 of 1192) among those age 23-24 years (ptrend=0·0076); the prevalence plateaued thereafter (ptrend=0·72). Similar age-specific patterns were observed for HR-HPV. No significant differences for HPV16 or HR-HPV were found by age for either HIV-positive or HIV-negative MSW. HSIL+ detection ranged from 7·5% (12 of 160) to 54·5% (61 of 112) in HIV-positive MSM; after adjustment for heterogeneity, HIV was a significant predictor of HSIL+ (aPR 1·54, 95% CI 1·36-1·73), HPV16-positive HSIL+ (1·66, 1·36-2·03), and HSIL+ in HPV16-positive MSM (1·19, 1·04-1·37). Among HPV16-positive MSM, HSIL+ prevalence increased with age.

INTERPRETATION: High anal HPV prevalence among young HIV-positive and HIV-negative MSM highlights the benefits of gender-neutral HPV vaccination before sexual activity over catch-up vaccination. HIV-positive MSM are a priority for anal cancer screening research and initiatives targeting HPV16-positive HSIL+.

FUNDING: International Agency for Research on Cancer.

* Title and MeSH Headings from MEDLINE®/PubMed®, a database of the U.S. National Library of Medicine.

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