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

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 s...

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Main Authors: Wei, Feixue, Gaisa, Michael M., D'Souza, Gypsyamber, Xia, Ningshao, Giuliano, Anna R., Hawes, Stephen E., Gao, Lei, Cheng, Shu-Hsing, Dona, Maria Gabriella, Goldstone, Stephen E., van der Loeff, Maarten F. Schim, Neukam, Karin, Meites, Elissa, Poynten, I. Mary, Dai, Jianghong, Combes, Jean-Damien, Wieland, Ulrike, Burgos, Joaquin, Wilkin, Timothy J., Hernandez, Alexandra L., Diaz, Mauricio Iribarren, Hidalgo-Tenorio, Carmen, Arredondo, Marleny Valencia, Nyitray, Alan G., Wentzensen, Nicolas, Chow, Eric Pf, Smelov, Vitaly, Nowak, Rebecca G., Phanuphak, Nittaya, Woo, Yin Ling, Choi, Yoojin, Hu, Yifei, Schofield, Alice M., Woestenberg, Petra J., Chikandiwa, Admire T., Hickey, Andrew C., de Pokomandy, Alexandra, Murenzi, Gad, Pere, Helene, del Pino, Marta, Ortiz, Ana P., Charnot-Katsikas, Angella, Liu, Xing, Chariyalertsak, Suwat, Strong, Carol, Ong, Jason J., Yunihastuti, Evy, Etienney, Isabelle, Ferre, Valentine M., Zou, Huachun, Segondy, Michel, Chinyowa, Simbarashe, Alberts, Catharina J., Clifford, Gary M.
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Published: Elsevier 2021
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Online Access:http://eprints.um.edu.my/34713/
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id my.um.eprints.34713
record_format eprints
institution Universiti Malaya
building UM Library
collection Institutional Repository
continent Asia
country Malaysia
content_provider Universiti Malaya
content_source UM Research Repository
url_provider http://eprints.um.edu.my/
topic R Medicine (General)
RC Internal medicine
spellingShingle R Medicine (General)
RC Internal medicine
Wei, Feixue
Gaisa, Michael M.
D'Souza, Gypsyamber
Xia, Ningshao
Giuliano, Anna R.
Hawes, Stephen E.
Gao, Lei
Cheng, Shu-Hsing
Dona, Maria Gabriella
Goldstone, Stephen E.
van der Loeff, Maarten F. Schim
Neukam, Karin
Meites, Elissa
Poynten, I. Mary
Dai, Jianghong
Combes, Jean-Damien
Wieland, Ulrike
Burgos, Joaquin
Wilkin, Timothy J.
Hernandez, Alexandra L.
Diaz, Mauricio Iribarren
Hidalgo-Tenorio, Carmen
Arredondo, Marleny Valencia
Nyitray, Alan G.
Wentzensen, Nicolas
Chow, Eric Pf
Smelov, Vitaly
Nowak, Rebecca G.
Phanuphak, Nittaya
Woo, Yin Ling
Choi, Yoojin
Hu, Yifei
Schofield, Alice M.
Woestenberg, Petra J.
Chikandiwa, Admire T.
Hickey, Andrew C.
de Pokomandy, Alexandra
Murenzi, Gad
Pere, Helene
del Pino, Marta
Ortiz, Ana P.
Charnot-Katsikas, Angella
Liu, Xing
Chariyalertsak, Suwat
Strong, Carol
Ong, Jason J.
Yunihastuti, Evy
Etienney, Isabelle
Ferre, Valentine M.
Zou, Huachun
Segondy, Michel
Chinyowa, Simbarashe
Alberts, Catharina J.
Clifford, Gary M.
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
description 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 6 4 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 , HI V was a significant predictor of HSIL+ (aPR 1.54, 95% CI 1.36-1.73), HPV16-posi t i v e HSIL+ (1.66, 1.36-2.03), and HSIL+ in HPV16-posi t i v e 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 Age n c y for Research on Cancer. Copyright (C) 2021 World Health Organization; licensee Elsevier.
format Article
author Wei, Feixue
Gaisa, Michael M.
D'Souza, Gypsyamber
Xia, Ningshao
Giuliano, Anna R.
Hawes, Stephen E.
Gao, Lei
Cheng, Shu-Hsing
Dona, Maria Gabriella
Goldstone, Stephen E.
van der Loeff, Maarten F. Schim
Neukam, Karin
Meites, Elissa
Poynten, I. Mary
Dai, Jianghong
Combes, Jean-Damien
Wieland, Ulrike
Burgos, Joaquin
Wilkin, Timothy J.
Hernandez, Alexandra L.
Diaz, Mauricio Iribarren
Hidalgo-Tenorio, Carmen
Arredondo, Marleny Valencia
Nyitray, Alan G.
Wentzensen, Nicolas
Chow, Eric Pf
Smelov, Vitaly
Nowak, Rebecca G.
Phanuphak, Nittaya
Woo, Yin Ling
Choi, Yoojin
Hu, Yifei
Schofield, Alice M.
Woestenberg, Petra J.
Chikandiwa, Admire T.
Hickey, Andrew C.
de Pokomandy, Alexandra
Murenzi, Gad
Pere, Helene
del Pino, Marta
Ortiz, Ana P.
Charnot-Katsikas, Angella
Liu, Xing
Chariyalertsak, Suwat
Strong, Carol
Ong, Jason J.
Yunihastuti, Evy
Etienney, Isabelle
Ferre, Valentine M.
Zou, Huachun
Segondy, Michel
Chinyowa, Simbarashe
Alberts, Catharina J.
Clifford, Gary M.
author_facet Wei, Feixue
Gaisa, Michael M.
D'Souza, Gypsyamber
Xia, Ningshao
Giuliano, Anna R.
Hawes, Stephen E.
Gao, Lei
Cheng, Shu-Hsing
Dona, Maria Gabriella
Goldstone, Stephen E.
van der Loeff, Maarten F. Schim
Neukam, Karin
Meites, Elissa
Poynten, I. Mary
Dai, Jianghong
Combes, Jean-Damien
Wieland, Ulrike
Burgos, Joaquin
Wilkin, Timothy J.
Hernandez, Alexandra L.
Diaz, Mauricio Iribarren
Hidalgo-Tenorio, Carmen
Arredondo, Marleny Valencia
Nyitray, Alan G.
Wentzensen, Nicolas
Chow, Eric Pf
Smelov, Vitaly
Nowak, Rebecca G.
Phanuphak, Nittaya
Woo, Yin Ling
Choi, Yoojin
Hu, Yifei
Schofield, Alice M.
Woestenberg, Petra J.
Chikandiwa, Admire T.
Hickey, Andrew C.
de Pokomandy, Alexandra
Murenzi, Gad
Pere, Helene
del Pino, Marta
Ortiz, Ana P.
Charnot-Katsikas, Angella
Liu, Xing
Chariyalertsak, Suwat
Strong, Carol
Ong, Jason J.
Yunihastuti, Evy
Etienney, Isabelle
Ferre, Valentine M.
Zou, Huachun
Segondy, Michel
Chinyowa, Simbarashe
Alberts, Catharina J.
Clifford, Gary M.
author_sort Wei, Feixue
title 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
title_short 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
title_full 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
title_fullStr 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
title_full_unstemmed 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
title_sort 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
publisher Elsevier
publishDate 2021
url http://eprints.um.edu.my/34713/
_version_ 1735409621211807744
spelling my.um.eprints.347132022-06-01T02:02:47Z http://eprints.um.edu.my/34713/ 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, Feixue Gaisa, Michael M. D'Souza, Gypsyamber Xia, Ningshao Giuliano, Anna R. Hawes, Stephen E. Gao, Lei Cheng, Shu-Hsing Dona, Maria Gabriella Goldstone, Stephen E. van der Loeff, Maarten F. Schim Neukam, Karin Meites, Elissa Poynten, I. Mary Dai, Jianghong Combes, Jean-Damien Wieland, Ulrike Burgos, Joaquin Wilkin, Timothy J. Hernandez, Alexandra L. Diaz, Mauricio Iribarren Hidalgo-Tenorio, Carmen Arredondo, Marleny Valencia Nyitray, Alan G. Wentzensen, Nicolas Chow, Eric Pf Smelov, Vitaly Nowak, Rebecca G. Phanuphak, Nittaya Woo, Yin Ling Choi, Yoojin Hu, Yifei Schofield, Alice M. Woestenberg, Petra J. Chikandiwa, Admire T. Hickey, Andrew C. de Pokomandy, Alexandra Murenzi, Gad Pere, Helene del Pino, Marta Ortiz, Ana P. Charnot-Katsikas, Angella Liu, Xing Chariyalertsak, Suwat Strong, Carol Ong, Jason J. Yunihastuti, Evy Etienney, Isabelle Ferre, Valentine M. Zou, Huachun Segondy, Michel Chinyowa, Simbarashe Alberts, Catharina J. Clifford, Gary M. R Medicine (General) RC Internal medicine 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 6 4 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 , HI V was a significant predictor of HSIL+ (aPR 1.54, 95% CI 1.36-1.73), HPV16-posi t i v e HSIL+ (1.66, 1.36-2.03), and HSIL+ in HPV16-posi t i v e 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 Age n c y for Research on Cancer. Copyright (C) 2021 World Health Organization; licensee Elsevier. Elsevier 2021-09 Article PeerReviewed Wei, Feixue and Gaisa, Michael M. and D'Souza, Gypsyamber and Xia, Ningshao and Giuliano, Anna R. and Hawes, Stephen E. and Gao, Lei and Cheng, Shu-Hsing and Dona, Maria Gabriella and Goldstone, Stephen E. and van der Loeff, Maarten F. Schim and Neukam, Karin and Meites, Elissa and Poynten, I. Mary and Dai, Jianghong and Combes, Jean-Damien and Wieland, Ulrike and Burgos, Joaquin and Wilkin, Timothy J. and Hernandez, Alexandra L. and Diaz, Mauricio Iribarren and Hidalgo-Tenorio, Carmen and Arredondo, Marleny Valencia and Nyitray, Alan G. and Wentzensen, Nicolas and Chow, Eric Pf and Smelov, Vitaly and Nowak, Rebecca G. and Phanuphak, Nittaya and Woo, Yin Ling and Choi, Yoojin and Hu, Yifei and Schofield, Alice M. and Woestenberg, Petra J. and Chikandiwa, Admire T. and Hickey, Andrew C. and de Pokomandy, Alexandra and Murenzi, Gad and Pere, Helene and del Pino, Marta and Ortiz, Ana P. and Charnot-Katsikas, Angella and Liu, Xing and Chariyalertsak, Suwat and Strong, Carol and Ong, Jason J. and Yunihastuti, Evy and Etienney, Isabelle and Ferre, Valentine M. and Zou, Huachun and Segondy, Michel and Chinyowa, Simbarashe and Alberts, Catharina J. and Clifford, Gary M. (2021) 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. The Lancet HIV, 8 (9). E531-E543. ISSN 2352-3018, DOI https://doi.org/10.1016/S2352-3018(21)00108-9 <https://doi.org/10.1016/S2352-3018(21)00108-9>. 10.1016/S2352-3018(21)00108-9
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