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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

      research-article
      , PhD a , , Prof, MD b , , Prof, PhD d , , Prof e , , Prof, PhD f , , Prof, PhD g , , Prof, PhD h , , PhD i , j , , PhD k , , MD c , , Prof, MD l , m , , PhD n , , MD o , , PhD p , , Prof, PhD q , , MD a , , MD r , , MD s , , MD t , , PhD u , v , , MD w , , MD x , , Prof, PhD y , , PhD z , , MD aa , , PhD ab , ac , ad , , MD a , ae , , PhD af , , MD ag , ah , , PhD ai , , PhD aj , , Prof, PhD ak , , MD al , , PhD am , , PhD an , , PhD ao , , MDCM ap , , MD aq , , PhD ar , as , , MD at , au , av , , PhD aw , ax , , MD ay , az , , PhD ba , , DrPH bb , , PhD bc , , PhD ac , , PhD bd , , MD be , , PharmD bf , bg , , Prof, PhD p , bh , bi , bj , , PhD bk , , PhD bl , , PhD a , , PhD a , *
      The Lancet. HIV
      Elsevier B.V

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          Summary

          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 (p trend=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 (p trend<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 (p trend=0·0076); the prevalence plateaued thereafter (p trend=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.

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          Most cited references61

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          Worldwide burden of cancer attributable to HPV by site, country and HPV type

          HPV is the cause of almost all cervical cancer and is responsible for a substantial fraction of other anogenital cancers and oropharyngeal cancers. Understanding the HPV‐attributable cancer burden can boost programs of HPV vaccination and HPV‐based cervical screening. Attributable fractions (AFs) and the relative contributions of different HPV types were derived from published studies reporting on the prevalence of transforming HPV infection in cancer tissue. Maps of age‐standardized incidence rates of HPV‐attributable cancers by country from GLOBOCAN 2012 data are shown separately for the cervix, other anogenital tract and head and neck cancers. The relative contribution of HPV16/18 and HPV6/11/16/18/31/33/45/52/58 was also estimated. 4.5% of all cancers worldwide (630,000 new cancer cases per year) are attributable to HPV: 8.6% in women and 0.8% in men. AF in women ranges from 20% in India and sub‐Saharan Africa. Cervix accounts for 83% of HPV‐attributable cancer, two‐thirds of which occur in less developed countries. Other HPV‐attributable anogenital cancer includes 8,500 vulva; 12,000 vagina; 35,000 anus (half occurring in men) and 13,000 penis. In the head and neck, HPV‐attributable cancers represent 38,000 cases of which 21,000 are oropharyngeal cancers occurring in more developed countries. The relative contributions of HPV16/18 and HPV6/11/16/18/31/33/45/52/58 are 73% and 90%, respectively. Universal access to vaccination is the key to avoiding most cases of HPV‐attributable cancer. The preponderant burden of HPV16/18 and the possibility of cross‐protection emphasize the importance of the introduction of more affordable vaccines in less developed countries.
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            Population-level impact and herd effects following the introduction of human papillomavirus vaccination programmes: updated systematic review and meta-analysis

            More than 10 years have elapsed since human papillomavirus (HPV) vaccination was implemented. We did a systematic review and meta-analysis of the population-level impact of vaccinating girls and women against human papillomavirus on HPV infections, anogenital wart diagnoses, and cervical intraepithelial neoplasia grade 2+ (CIN2+) to summarise the most recent evidence about the effectiveness of HPV vaccines in real-world settings and to quantify the impact of multiple age-cohort vaccination.
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              • Article: not found

              Carcinogenic human papillomavirus infection.

              Infections with human papillomavirus (HPV) are common and transmitted by direct contact. Although the great majority of infections resolve within 2 years, 13 phylogenetically related, sexually transmitted HPV genotypes, notably HPV16, cause - if not controlled immunologically or by screening - virtually all cervical cancers worldwide, a large fraction of other anogenital cancers and an increasing proportion of oropharyngeal cancers. The carcinogenicity of these HPV types results primarily from the activity of the oncoproteins E6 and E7, which impair growth regulatory pathways. Persistent high-risk HPVs can transition from a productive (virion-producing) to an abortive or transforming infection, after which cancer can result after typically slow accumulation of host genetic mutations. However, which precancerous lesions progress and which do not is unclear; the majority of screening-detected precancers are treated, leading to overtreatment. The discovery of HPV as a carcinogen led to the development of effective preventive vaccines and sensitive HPV DNA and RNA tests. Together, vaccination programmes (the ultimate long-term preventive strategy) and screening using HPV tests could dramatically alter the landscape of HPV-related cancers. HPV testing will probably replace cytology-based cervical screening owing to greater reassurance when the test is negative. However, the effective implementation of HPV vaccination and screening globally remains a challenge.
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                Author and article information

                Contributors
                Journal
                Lancet HIV
                Lancet HIV
                The Lancet. HIV
                Elsevier B.V
                2405-4704
                2352-3018
                30 July 2021
                September 2021
                30 July 2021
                : 8
                : 9
                : e531-e543
                Affiliations
                [a ]Early Detection, Prevention and Infections Branch, International Agency for Research on Cancer (IARC/WHO), Lyon, France
                [b ]Department of Medicine, Division of Infectious Diseases, Icahn School of Medicine at Mount Sinai, New York, NY, USA
                [c ]Department of Surgery, Icahn School of Medicine at Mount Sinai, New York, NY, USA
                [d ]Department of Epidemiology, Johns Hopkins Bloomberg School of Public Health, Baltimore, MD, USA
                [e ]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
                [f ]Center for Immunization and Infection Research in Cancer, Moffitt Cancer Center, Tampa, FL, USA
                [g ]Department of Epidemiology, Department of Health Services, and Department of Global Health, University of Washington, Seattle, WA, USA
                [h ]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
                [i ]Department of Infectious Diseases, Taoyuan General Hospital, Ministry of Health and Welfare, Taoyuan, Taiwan
                [j ]School of Public Health, Taipei Medical University, Taipei, Taiwan
                [k ]Sexually Transmitted Infections/HIV Unit, San Gallicano Dermatological Institute, IRCCS, Rome, Italy
                [l ]Department of Infectious Diseases, Public Health Service of Amsterdam, Amsterdam, Netherlands
                [m ]Department of Internal Medicine, Amsterdam institute for Infection and Immunity, Amsterdam UMC, University of Amsterdam, Amsterdam, Netherlands
                [n ]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
                [o ]Division of Viral Diseases, Centers for Disease Control and Prevention, Atlanta, GA, USA
                [p ]Kirby Institute, University of New South Wales, Sydney, NSW, Australia
                [q ]School of Public Health, Xinjiang Medical University, Xinjiang, Urumqi, China
                [r ]Institute of Virology, University of Cologne, National Reference Center for Papilloma and Polyomaviruses, Cologne, Germany
                [s ]Department of infectious Diseases, Vall d'Hebron University Hospital, Barcelona, Spain
                [t ]Division of Infectious Diseases, Weill Cornell Medicine, New York, NY, USA
                [u ]Department of Medicine, University of California, San Francisco, CA, USA
                [v ]Public Health Program, College of Education and Health Sciences, Touro University, Vallejo, CA, USA
                [w ]Department of Surgery, Complexo Hospitalario Universitario de Vigo-Hospital Álvaro Cunqueiro, Vigo, Spain
                [x ]Infectious Disease Unit, Biosanitary Research Institute Granada, University Hospital Virgen de las Nieves, Granada, Spain
                [y ]Universidad de Antioquia, Escuela de Microbiología, Grupo de investigación Salud Sexual y Cáncer, Medellín, Antioquia, Colombia
                [z ]Clinical Cancer Center and Center for AIDS Intervention Research, Medical College of Wisconsin, Milwaukee, WI, USA
                [aa ]Division of Cancer Epidemiology and Genetics, National Cancer Institute, Bethesda, MD, USA
                [ab ]Melbourne Sexual Health Centre, The Alfred Hospital, Melbourne, VIC, Australia
                [ac ]Central Clinical School, Monash University, Melbourne, VIC, Australia
                [ad ]Melbourne School of Population and Global Health, The University of Melbourne, Melbourne, VIC, Australia
                [ae ]Division of Country Health Programmes, WHO Regional Office for Europe, Copenhagen, Denmark
                [af ]Institute of Human Virology, University of Maryland School of Medicine, Baltimore, MD, USA
                [ag ]Institute of HIV Research and Innovation, Bangkok, Thailand
                [ah ]Center of Excellence in Transgender Health, Chulalongkorn University, Bangkok, Thailand
                [ai ]Faculty of Medicine, University of Malaya, Kuala Lumpur, Malaysia
                [aj ]Department of Immunology, University of Toronto, Toronto, ON, Canada
                [ak ]Department of Child and Adolescent Health and Maternal Care, School of Public Health, Capital Medical University, Beijing, China
                [al ]Institute of Cancer Sciences, University of Manchester, Manchester, UK
                [am ]Center for Infectious Disease Control, National Institute for Public Health and the Environment, Bilthoven, Netherlands
                [an ]Wits RHI, Faculty of Health Sciences, University of the Witwatersrand, Johannesburg, South Africa
                [ao ]Division of HIV/AIDS Prevention, Centers for Disease Control and Prevention, Nonthaburi, Thailand
                [ap ]Chronic Viral Illness Service, McGill University Health Centre and Department of Family Medicine, McGill University, Montreal, QC, Canada
                [aq ]Rwanda Military Hospital and Research for Development Rwanda, Kigali, Rwanda
                [ar ]Assistance Publique Hôpitaux de Paris-Centre, Service de Microbiologie (Unité de virologie), Hôpital Européen Georges Pompidou, Paris, France
                [as ]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
                [at ]Institute Clinic of Gynecology, Obstetrics, and Neonatology, Gynecology Oncology Unit, Hospital Clínic, Barcelona, Spain
                [au ]Institut d'Investigacions Biomèdiques August Pi i Sunyer, Barcelona, Spain
                [av ]Medicine Faculty, Barcelona University, Barcelona, Spain
                [aw ]Cancer Control and Population Sciences Program, University of Puerto Rico Comprehensive Cancer Center, San Juan, PR, USA
                [ax ]Graduate School of Public Health, University of Puerto Rico, San Juan, PR, USA
                [ay ]Department of Pathology, The University of Chicago, Chicago, IL, USA
                [az ]MolDx Program, Palmetto GBA, Columbia, SC, USA
                [ba ]Department of Epidemiology, School of Public Health, and the Key Laboratory of Public Health Safety of Ministry of Education, Fudan University, Shanghai, China
                [bb ]Faculty of Public Health, Chiang Mai University and Research Institute for Health Sciences, Chiang Mai University, Chiang Mai, Thailand
                [bc ]Department of Public Health, National Cheng Kung University Hospital, College of Medicine, National Cheng Kung University, Tainan, Taiwan
                [bd ]Department of Internal Medicine, University of Indonesia, Jakarta, Indonesia
                [be ]Proctology, Diaconesses-Croix Saint Simon Hospital, Paris, France
                [bf ]Université de Paris, Assistance Publique–Hôpitaux de Paris, Service de Virologie, Hôpital Bichat, Paris, France
                [bg ]Decision Science in Infectious Disease Prevention, Control and Care, INSERM, Université de Paris, Paris, France
                [bh ]School of Public Health (Shenzhen), Sun Yat-sen University, Shenzhen, China
                [bi ]School of Public Health, Shanghai Jiao Tong University, Shanghai, China
                [bj ]Melbourne Sexual Health Centre, Sydney, NSW, Australia
                [bk ]Pathogenesis and Control of Chronic Infections, INSERM, CHU, University of Montpellier, Montpellier, France
                [bl ]Department of Surgery, College of Health Sciences University of Zimbabwe, Harare, Zimbabwe
                Author notes
                [* ]Correspondence to: Dr Gary M Clifford, Early Detection, Prevention and Infections Branch, International Agency for Research on Cancer (IARC/WHO), Lyon 69372, France cliffordg@ 123456iarc.fr
                Article
                S2352-3018(21)00108-9
                10.1016/S2352-3018(21)00108-9
                8408042
                34339628
                4a13fe30-f767-4d29-a60b-c74679a06c5f
                © 2021 World Health Organization

                This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/3.0/).

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