Cervical determinants of anal HPV infection and high-grade anal lesions in women: a collaborative pooled analysis

Chunqing Lin; Jiri Slama; Paula Gonzalez; Marc T Goodman; Ningshao Xia; Aimée R Kreimer; Ting Wu; Nancy A Hessol; Yurii Shvetsov; Ana P Ortiz; Beatriz Grinsztejn; Anna-Barbara Moscicki; Isabelle Heard; María Del Refugio González Losa; Erna M Kojic; Maarten F Schim van der Loeff; Feixue Wei; Adhemar Longatto-Filho; Zizipho A Mbulawa; Joel M Palefsky; Annette H Sohn; Brenda Y Hernandez; Katina Robison; Steve Simpson; Lois J Conley; Alexandra de Pokomandy; Marianne A B van der Sande; Racheal S Dube Mandishora; Lays P B Volpini; Alessandra Pierangeli; Byron Romero; Timothy Wilkin; Silvia Franceschi; Carmen Hidalgo-Tenorio; Reshmie A Ramautarsing; Ina U Park; Fernanda K Tso; Sheela Godbole; Kathleen W M D'Hauwers; Borek Sehnal; Lynette J Menezes; Sandra A Heráclio; Gary M Clifford

doi:10.1016/S1473-3099(19)30164-1

Cervical determinants of anal HPV infection and high-grade anal lesions in women: a collaborative pooled analysis

Chunqing Lin, Jiri Slama, Paula Gonzalez, Marc T Goodman, Ningshao Xia, Aimée R Kreimer, Ting Wu, Nancy A Hessol, Yurii Shvetsov, Ana P Ortiz, Beatriz Grinsztejn, Anna-Barbara Moscicki, Isabelle Heard, María Del Refugio González Losa, Erna M Kojic, Maarten F Schim van der Loeff, Feixue Wei, Adhemar Longatto-Filho, Zizipho A Mbulawa, Joel M PalefskyAnnette H Sohn, Brenda Y Hernandez, Katina Robison, Steve Simpson, Lois J Conley, Alexandra de Pokomandy, Marianne A B van der Sande, Racheal S Dube Mandishora, Lays P B Volpini, Alessandra Pierangeli, Byron Romero, Timothy Wilkin, Silvia Franceschi, Carmen Hidalgo-Tenorio, Reshmie A Ramautarsing, Ina U Park, Fernanda K Tso, Sheela Godbole, Kathleen W M D'Hauwers, Borek Sehnal, Lynette J Menezes, Sandra A Heráclio, Gary M Clifford

Department of Public Health

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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.

Original language	English
Journal	Lancet Infectious Diseases
Volume	19
Issue number	8
Pages (from-to)	880-891
Number of pages	12
ISSN	1473-3099
DOIs	https://doi.org/10.1016/S1473-3099(19)30164-1
Publication status	Published - 2019

Keywords

HUMAN-PAPILLOMAVIRUS INFECTION
RISK HUMAN-PAPILLOMAVIRUS
INTRAEPITHELIAL NEOPLASIA
HIV
PREVALENCE
CANCER
CYTOLOGY
ANUS
SEX
MEN

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2019lidi0880Final published version, 382 KBLicence: CC BY-NC-ND

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Lin, C., Slama, J., Gonzalez, P., Goodman, M. T., Xia, N., Kreimer, A. R., Wu, T., Hessol, N. A., Shvetsov, Y., Ortiz, A. P., Grinsztejn, B., Moscicki, A.-B., Heard, I., Del Refugio González Losa, M., Kojic, E. M., Schim van der Loeff, M. F., Wei, F., Longatto-Filho, A., Mbulawa, Z. A., ... Clifford, G. M. (2019). Cervical determinants of anal HPV infection and high-grade anal lesions in women: a collaborative pooled analysis. Lancet Infectious Diseases, 19(8), 880-891. https://doi.org/10.1016/S1473-3099(19)30164-1

@article{6fc38c25c06846d9abbd5367b0948425,

title = "Cervical determinants of anal HPV infection and high-grade anal lesions in women: a collaborative pooled analysis",

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.",

keywords = "HUMAN-PAPILLOMAVIRUS INFECTION, RISK HUMAN-PAPILLOMAVIRUS, INTRAEPITHELIAL NEOPLASIA, HIV, PREVALENCE, CANCER, CYTOLOGY, ANUS, SEX, MEN",

author = "Chunqing Lin and Jiri Slama and Paula Gonzalez and Goodman, {Marc T} and Ningshao Xia and Kreimer, {Aim{\'e}e R} and Ting Wu and Hessol, {Nancy A} and Yurii Shvetsov and Ortiz, {Ana P} and Beatriz Grinsztejn and Anna-Barbara Moscicki and Isabelle Heard and {Del Refugio Gonz{\'a}lez Losa}, Mar{\'i}a and Kojic, {Erna M} and {Schim van der Loeff}, {Maarten F} and Feixue Wei and Adhemar Longatto-Filho and Mbulawa, {Zizipho A} and Palefsky, {Joel M} and Sohn, {Annette H} and Hernandez, {Brenda Y} and Katina Robison and Steve Simpson and Conley, {Lois J} and {de Pokomandy}, Alexandra and {van der Sande}, {Marianne A B} and {Dube Mandishora}, {Racheal S} and Volpini, {Lays P B} and Alessandra Pierangeli and Byron Romero and Timothy Wilkin and Silvia Franceschi and Carmen Hidalgo-Tenorio and Ramautarsing, {Reshmie A} and Park, {Ina U} and Tso, {Fernanda K} and Sheela Godbole and D'Hauwers, {Kathleen W M} and Borek Sehnal and Menezes, {Lynette J} and Her{\'a}clio, {Sandra A} and Clifford, {Gary M}",

note = "FTX; (CC BY-NC-ND 3.0 IGO); Copyright {\textcopyright} 2019 International Agency for Research on Cancer; licensee Elsevier. This is an Open Access article published under the CC BY-NC-ND 3.0 IGO license which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. In any use of this article, there should be no suggestion that IARC endorses any specific organisation, products or services. The use of the IARC logo is not permitted. This notice should be preserved along with the article's original URL.",

year = "2019",

doi = "10.1016/S1473-3099(19)30164-1",

language = "English",

volume = "19",

pages = "880--891",

journal = "Lancet Infectious Diseases",

issn = "1473-3099",

publisher = "Elsevier",

number = "8",

}

Lin, C, Slama, J, Gonzalez, P, Goodman, MT, Xia, N, Kreimer, AR, Wu, T, Hessol, NA, Shvetsov, Y, Ortiz, AP, Grinsztejn, B, Moscicki, A-B, Heard, I, Del Refugio González Losa, M, Kojic, EM, Schim van der Loeff, MF, Wei, F, Longatto-Filho, A, Mbulawa, ZA, Palefsky, JM, Sohn, AH, Hernandez, BY, Robison, K, Simpson, S, Conley, LJ, de Pokomandy, A, van der Sande, MAB, Dube Mandishora, RS, Volpini, LPB, Pierangeli, A, Romero, B, Wilkin, T, Franceschi, S, Hidalgo-Tenorio, C, Ramautarsing, RA, Park, IU, Tso, FK, Godbole, S, D'Hauwers, KWM, Sehnal, B, Menezes, LJ, Heráclio, SA & Clifford, GM 2019, 'Cervical determinants of anal HPV infection and high-grade anal lesions in women: a collaborative pooled analysis', Lancet Infectious Diseases, vol. 19, no. 8, pp. 880-891. https://doi.org/10.1016/S1473-3099(19)30164-1

TY - JOUR

T1 - Cervical determinants of anal HPV infection and high-grade anal lesions in women: a collaborative pooled analysis

AU - Lin, Chunqing

AU - Slama, Jiri

AU - Gonzalez, Paula

AU - Goodman, Marc T

AU - Xia, Ningshao

AU - Kreimer, Aimée R

AU - Wu, Ting

AU - Hessol, Nancy A

AU - Shvetsov, Yurii

AU - Ortiz, Ana P

AU - Grinsztejn, Beatriz

AU - Moscicki, Anna-Barbara

AU - Heard, Isabelle

AU - Del Refugio González Losa, María

AU - Kojic, Erna M

AU - Schim van der Loeff, Maarten F

AU - Wei, Feixue

AU - Longatto-Filho, Adhemar

AU - Mbulawa, Zizipho A

AU - Palefsky, Joel M

AU - Sohn, Annette H

AU - Hernandez, Brenda Y

AU - Robison, Katina

AU - Simpson, Steve

AU - Conley, Lois J

AU - de Pokomandy, Alexandra

AU - van der Sande, Marianne A B

AU - Dube Mandishora, Racheal S

AU - Volpini, Lays P B

AU - Pierangeli, Alessandra

AU - Romero, Byron

AU - Wilkin, Timothy

AU - Franceschi, Silvia

AU - Hidalgo-Tenorio, Carmen

AU - Ramautarsing, Reshmie A

AU - Park, Ina U

AU - Tso, Fernanda K

AU - Godbole, Sheela

AU - D'Hauwers, Kathleen W M

AU - Sehnal, Borek

AU - Menezes, Lynette J

AU - Heráclio, Sandra A

AU - Clifford, Gary M

N1 - FTX; (CC BY-NC-ND 3.0 IGO); Copyright © 2019 International Agency for Research on Cancer; licensee Elsevier. This is an Open Access article published under the CC BY-NC-ND 3.0 IGO license which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. In any use of this article, there should be no suggestion that IARC endorses any specific organisation, products or services. The use of the IARC logo is not permitted. This notice should be preserved along with the article's original URL.

PY - 2019

Y1 - 2019

N2 - 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.

AB - 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.

KW - HUMAN-PAPILLOMAVIRUS INFECTION

KW - RISK HUMAN-PAPILLOMAVIRUS

KW - INTRAEPITHELIAL NEOPLASIA

KW - HIV

KW - PREVALENCE

KW - CANCER

KW - CYTOLOGY

KW - ANUS

KW - SEX

KW - MEN

U2 - 10.1016/S1473-3099(19)30164-1

DO - 10.1016/S1473-3099(19)30164-1

M3 - A1: Web of Science-article

C2 - 31204304

SN - 1473-3099

VL - 19

SP - 880

EP - 891

JO - Lancet Infectious Diseases

JF - Lancet Infectious Diseases

IS - 8

ER -

Cervical determinants of anal HPV infection and high-grade anal lesions in women: a collaborative pooled analysis

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