Population-level impact and herd effects following the introduction of human papillomavirus vaccination programmes: updated systematic review and meta-analysis

Mélanie Drolet, Élodie Bénard, Norma Pérez, Marc Brisson, Marie-Claude Boily, Hammad Ali, Vincent Baldo, Paul Brassard, Julia M L Brotherton, Denton Callander, Marta Checchi, Eric PF Chow, Silvia Cocchio, Tina Dalianis, Shelley Deeks, Christian Dehlendorff, Basil Donovan, Christopher Fairley, Elaine Flagg, Julia Gargano & 32 others Suzanne M Garland, Nathalie Grun, Bo Hansen, Christopher Harrison, Eva Herweijer, Teresa Imburgia, Anne Johnson, Jessica A Kahn, Kimberley Kavanagh, Susan Kjaer, Ericj Kliewer, Bette Liu, Dorothy Machalek, Lauri Markowitz, David Mesher, Christian Munk, Linda Niccolai, Mari Nygard, Gina Ogilvie, Jeannie Oliphant, Kevin Pollock, Jesus Purrinos-Hermida, Megan Smith, Marc Steben, Anna Soderlund-Strand, Pam Sonnenberg, Par Sparen, Clare Tanton, Clare Tanton, Cosette Wheeler, Petra Woestenberg, Bo Yu

Research output: Contribution to journalArticle

Abstract

Background: 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. Methods: In this updated systematic review and meta-analysis, we used the same search strategy as in our previous paper. We searched MEDLINE and Embase for studies published between Feb 1, 2014, and Oct 11, 2018. Studies were eligible if they compared the frequency (prevalence or incidence) of at least one HPV-related endpoint (genital HPV infections, anogenital wart diagnoses, or histologically confirmed CIN2+) between pre-vaccination and post-vaccination periods among the general population and if they used the same population sources and recruitment methods before and after vaccination. Our primary assessment was the relative risk (RR) comparing the frequency (prevalence or incidence) of HPV-related endpoints between the pre-vaccination and post-vaccination periods. We stratified all analyses by sex, age, and years since introduction of HPV vaccination. We used random-effects models to estimate pooled relative risks. Findings: We identified 1702 potentially eligible articles for this systematic review and meta-analysis, and included 65 articles in 14 high-income countries: 23 for HPV infection, 29 for anogenital warts, and 13 for CIN2+. After 5–8 years of vaccination, the prevalence of HPV 16 and 18 decreased significantly by 83% (RR 0·17, 95% CI 0·11–0·25) among girls aged 13–19 years, and decreased significantly by 66% (RR 0·34, 95% CI 0·23–0·49) among women aged 20–24 years. The prevalence of HPV 31, 33, and 45 decreased significantly by 54% (RR 0·46, 95% CI 0·33–0·66) among girls aged 13–19 years. Anogenital wart diagnoses decreased significantly by 67% (RR 0·33, 95% CI 0·24–0·46) among girls aged 15–19 years, decreased significantly by 54% (RR 0·46, 95% CI 0.36–0.60) among women aged 20–24 years, and decreased significantly by 31% (RR 0·69, 95% CI 0·53–0·89) among women aged 25–29 years. Among boys aged 15–19 years anogenital wart diagnoses decreased significantly by 48% (RR 0·52, 95% CI 0·37–0·75) and among men aged 20–24 years they decreased significantly by 32% (RR 0·68, 95% CI 0·47–0·98). After 5–9 years of vaccination, CIN2+ decreased significantly by 51% (RR 0·49, 95% CI 0·42–0·58) among screened girls aged 15–19 years and decreased significantly by 31% (RR 0·69, 95% CI 0·57–0·84) among women aged 20–24 years. Interpretation: This updated systematic review and meta-analysis includes data from 60 million individuals and up to 8 years of post-vaccination follow-up. Our results show compelling evidence of the substantial impact of HPV vaccination programmes on HPV infections and CIN2+ among girls and women, and on anogenital warts diagnoses among girls, women, boys, and men. Additionally, programmes with multi-cohort vaccination and high vaccination coverage had a greater direct impact and herd effects. Funding: WHO, Canadian Institutes of Health Research, Fonds de recherche du Québec – Santé.

LanguageEnglish
Pages497-509
Number of pages13
JournalLancet
Volume394
Issue number10197
Early online date26 Jun 2019
DOIs
Publication statusPublished - 16 Aug 2019

Fingerprint

Vaccination
Relative Risk
Meta-Analysis
Warts
Population
Cervical Intraepithelial Neoplasia
Papillomavirus Infections
Infection
Review
Human
Incidence
Human papillomavirus 31
Papillomavirus Vaccines
Human papillomavirus 18
Human papillomavirus 16
Quebec
Vaccine
Random Effects Model
Search Strategy
MEDLINE

Keywords

  • HPV
  • HPV vaccine
  • herd effect
  • human papillomavirus
  • vaccination programmes

Cite this

Drolet, Mélanie ; Bénard, Élodie ; Pérez, Norma ; Brisson, Marc ; Boily, Marie-Claude ; Ali, Hammad ; Baldo, Vincent ; Brassard, Paul ; Brotherton, Julia M L ; Callander, Denton ; Checchi, Marta ; Chow, Eric PF ; Cocchio, Silvia ; Dalianis, Tina ; Deeks, Shelley ; Dehlendorff, Christian ; Donovan, Basil ; Fairley, Christopher ; Flagg, Elaine ; Gargano, Julia ; Garland, Suzanne M ; Grun, Nathalie ; Hansen, Bo ; Harrison, Christopher ; Herweijer, Eva ; Imburgia, Teresa ; Johnson, Anne ; Kahn, Jessica A ; Kavanagh, Kimberley ; Kjaer, Susan ; Kliewer, Ericj ; Liu, Bette ; Machalek, Dorothy ; Markowitz, Lauri ; Mesher, David ; Munk, Christian ; Niccolai, Linda ; Nygard, Mari ; Ogilvie, Gina ; Oliphant, Jeannie ; Pollock, Kevin ; Purrinos-Hermida, Jesus ; Smith, Megan ; Steben, Marc ; Soderlund-Strand, Anna ; Sonnenberg, Pam ; Sparen, Par ; Tanton, Clare ; Tanton, Clare ; Wheeler, Cosette ; Woestenberg, Petra ; Yu, Bo. / Population-level impact and herd effects following the introduction of human papillomavirus vaccination programmes : updated systematic review and meta-analysis. In: Lancet. 2019 ; Vol. 394, No. 10197. pp. 497-509.
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abstract = "Background: 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. Methods: In this updated systematic review and meta-analysis, we used the same search strategy as in our previous paper. We searched MEDLINE and Embase for studies published between Feb 1, 2014, and Oct 11, 2018. Studies were eligible if they compared the frequency (prevalence or incidence) of at least one HPV-related endpoint (genital HPV infections, anogenital wart diagnoses, or histologically confirmed CIN2+) between pre-vaccination and post-vaccination periods among the general population and if they used the same population sources and recruitment methods before and after vaccination. Our primary assessment was the relative risk (RR) comparing the frequency (prevalence or incidence) of HPV-related endpoints between the pre-vaccination and post-vaccination periods. We stratified all analyses by sex, age, and years since introduction of HPV vaccination. We used random-effects models to estimate pooled relative risks. Findings: We identified 1702 potentially eligible articles for this systematic review and meta-analysis, and included 65 articles in 14 high-income countries: 23 for HPV infection, 29 for anogenital warts, and 13 for CIN2+. After 5–8 years of vaccination, the prevalence of HPV 16 and 18 decreased significantly by 83{\%} (RR 0·17, 95{\%} CI 0·11–0·25) among girls aged 13–19 years, and decreased significantly by 66{\%} (RR 0·34, 95{\%} CI 0·23–0·49) among women aged 20–24 years. The prevalence of HPV 31, 33, and 45 decreased significantly by 54{\%} (RR 0·46, 95{\%} CI 0·33–0·66) among girls aged 13–19 years. Anogenital wart diagnoses decreased significantly by 67{\%} (RR 0·33, 95{\%} CI 0·24–0·46) among girls aged 15–19 years, decreased significantly by 54{\%} (RR 0·46, 95{\%} CI 0.36–0.60) among women aged 20–24 years, and decreased significantly by 31{\%} (RR 0·69, 95{\%} CI 0·53–0·89) among women aged 25–29 years. Among boys aged 15–19 years anogenital wart diagnoses decreased significantly by 48{\%} (RR 0·52, 95{\%} CI 0·37–0·75) and among men aged 20–24 years they decreased significantly by 32{\%} (RR 0·68, 95{\%} CI 0·47–0·98). After 5–9 years of vaccination, CIN2+ decreased significantly by 51{\%} (RR 0·49, 95{\%} CI 0·42–0·58) among screened girls aged 15–19 years and decreased significantly by 31{\%} (RR 0·69, 95{\%} CI 0·57–0·84) among women aged 20–24 years. Interpretation: This updated systematic review and meta-analysis includes data from 60 million individuals and up to 8 years of post-vaccination follow-up. Our results show compelling evidence of the substantial impact of HPV vaccination programmes on HPV infections and CIN2+ among girls and women, and on anogenital warts diagnoses among girls, women, boys, and men. Additionally, programmes with multi-cohort vaccination and high vaccination coverage had a greater direct impact and herd effects. Funding: WHO, Canadian Institutes of Health Research, Fonds de recherche du Qu{\'e}bec – Sant{\'e}.",
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Drolet, M, Bénard, É, Pérez, N, Brisson, M, Boily, M-C, Ali, H, Baldo, V, Brassard, P, Brotherton, JML, Callander, D, Checchi, M, Chow, EPF, Cocchio, S, Dalianis, T, Deeks, S, Dehlendorff, C, Donovan, B, Fairley, C, Flagg, E, Gargano, J, Garland, SM, Grun, N, Hansen, B, Harrison, C, Herweijer, E, Imburgia, T, Johnson, A, Kahn, JA, Kavanagh, K, Kjaer, S, Kliewer, E, Liu, B, Machalek, D, Markowitz, L, Mesher, D, Munk, C, Niccolai, L, Nygard, M, Ogilvie, G, Oliphant, J, Pollock, K, Purrinos-Hermida, J, Smith, M, Steben, M, Soderlund-Strand, A, Sonnenberg, P, Sparen, P, Tanton, C, Tanton, C, Wheeler, C, Woestenberg, P & Yu, B 2019, 'Population-level impact and herd effects following the introduction of human papillomavirus vaccination programmes: updated systematic review and meta-analysis' Lancet, vol. 394, no. 10197, pp. 497-509. https://doi.org/10.1016/S0140-6736(19)30298-3

Population-level impact and herd effects following the introduction of human papillomavirus vaccination programmes : updated systematic review and meta-analysis. / Drolet, Mélanie; Bénard, Élodie; Pérez, Norma; Brisson, Marc; Boily, Marie-Claude; Ali, Hammad; Baldo, Vincent; Brassard, Paul; Brotherton, Julia M L; Callander, Denton; Checchi, Marta; Chow, Eric PF; Cocchio, Silvia; Dalianis, Tina; Deeks, Shelley; Dehlendorff, Christian ; Donovan, Basil; Fairley, Christopher; Flagg, Elaine; Gargano, Julia; Garland, Suzanne M; Grun, Nathalie; Hansen, Bo; Harrison, Christopher; Herweijer, Eva; Imburgia, Teresa; Johnson, Anne; Kahn, Jessica A; Kavanagh, Kimberley; Kjaer, Susan; Kliewer, Ericj; Liu, Bette; Machalek, Dorothy; Markowitz, Lauri; Mesher, David ; Munk, Christian; Niccolai, Linda; Nygard, Mari; Ogilvie, Gina; Oliphant, Jeannie; Pollock, Kevin; Purrinos-Hermida, Jesus; Smith, Megan; Steben, Marc; Soderlund-Strand, Anna; Sonnenberg, Pam; Sparen, Par; Tanton, Clare ; Tanton, Clare; Wheeler, Cosette; Woestenberg, Petra; Yu, Bo.

In: Lancet, Vol. 394, No. 10197, 16.08.2019, p. 497-509.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Population-level impact and herd effects following the introduction of human papillomavirus vaccination programmes

T2 - Lancet

AU - Drolet, Mélanie

AU - Bénard, Élodie

AU - Pérez, Norma

AU - Brisson, Marc

AU - Boily, Marie-Claude

AU - Ali, Hammad

AU - Baldo, Vincent

AU - Brassard, Paul

AU - Brotherton, Julia M L

AU - Callander, Denton

AU - Checchi, Marta

AU - Chow, Eric PF

AU - Cocchio, Silvia

AU - Dalianis, Tina

AU - Deeks, Shelley

AU - Dehlendorff, Christian

AU - Donovan, Basil

AU - Fairley, Christopher

AU - Flagg, Elaine

AU - Gargano, Julia

AU - Garland, Suzanne M

AU - Grun, Nathalie

AU - Hansen, Bo

AU - Harrison, Christopher

AU - Herweijer, Eva

AU - Imburgia, Teresa

AU - Johnson, Anne

AU - Kahn, Jessica A

AU - Kavanagh, Kimberley

AU - Kjaer, Susan

AU - Kliewer, Ericj

AU - Liu, Bette

AU - Machalek, Dorothy

AU - Markowitz, Lauri

AU - Mesher, David

AU - Munk, Christian

AU - Niccolai, Linda

AU - Nygard, Mari

AU - Ogilvie, Gina

AU - Oliphant, Jeannie

AU - Pollock, Kevin

AU - Purrinos-Hermida, Jesus

AU - Smith, Megan

AU - Steben, Marc

AU - Soderlund-Strand, Anna

AU - Sonnenberg, Pam

AU - Sparen, Par

AU - Tanton, Clare

AU - Tanton, Clare

AU - Wheeler, Cosette

AU - Woestenberg, Petra

AU - Yu, Bo

PY - 2019/8/16

Y1 - 2019/8/16

N2 - Background: 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. Methods: In this updated systematic review and meta-analysis, we used the same search strategy as in our previous paper. We searched MEDLINE and Embase for studies published between Feb 1, 2014, and Oct 11, 2018. Studies were eligible if they compared the frequency (prevalence or incidence) of at least one HPV-related endpoint (genital HPV infections, anogenital wart diagnoses, or histologically confirmed CIN2+) between pre-vaccination and post-vaccination periods among the general population and if they used the same population sources and recruitment methods before and after vaccination. Our primary assessment was the relative risk (RR) comparing the frequency (prevalence or incidence) of HPV-related endpoints between the pre-vaccination and post-vaccination periods. We stratified all analyses by sex, age, and years since introduction of HPV vaccination. We used random-effects models to estimate pooled relative risks. Findings: We identified 1702 potentially eligible articles for this systematic review and meta-analysis, and included 65 articles in 14 high-income countries: 23 for HPV infection, 29 for anogenital warts, and 13 for CIN2+. After 5–8 years of vaccination, the prevalence of HPV 16 and 18 decreased significantly by 83% (RR 0·17, 95% CI 0·11–0·25) among girls aged 13–19 years, and decreased significantly by 66% (RR 0·34, 95% CI 0·23–0·49) among women aged 20–24 years. The prevalence of HPV 31, 33, and 45 decreased significantly by 54% (RR 0·46, 95% CI 0·33–0·66) among girls aged 13–19 years. Anogenital wart diagnoses decreased significantly by 67% (RR 0·33, 95% CI 0·24–0·46) among girls aged 15–19 years, decreased significantly by 54% (RR 0·46, 95% CI 0.36–0.60) among women aged 20–24 years, and decreased significantly by 31% (RR 0·69, 95% CI 0·53–0·89) among women aged 25–29 years. Among boys aged 15–19 years anogenital wart diagnoses decreased significantly by 48% (RR 0·52, 95% CI 0·37–0·75) and among men aged 20–24 years they decreased significantly by 32% (RR 0·68, 95% CI 0·47–0·98). After 5–9 years of vaccination, CIN2+ decreased significantly by 51% (RR 0·49, 95% CI 0·42–0·58) among screened girls aged 15–19 years and decreased significantly by 31% (RR 0·69, 95% CI 0·57–0·84) among women aged 20–24 years. Interpretation: This updated systematic review and meta-analysis includes data from 60 million individuals and up to 8 years of post-vaccination follow-up. Our results show compelling evidence of the substantial impact of HPV vaccination programmes on HPV infections and CIN2+ among girls and women, and on anogenital warts diagnoses among girls, women, boys, and men. Additionally, programmes with multi-cohort vaccination and high vaccination coverage had a greater direct impact and herd effects. Funding: WHO, Canadian Institutes of Health Research, Fonds de recherche du Québec – Santé.

AB - Background: 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. Methods: In this updated systematic review and meta-analysis, we used the same search strategy as in our previous paper. We searched MEDLINE and Embase for studies published between Feb 1, 2014, and Oct 11, 2018. Studies were eligible if they compared the frequency (prevalence or incidence) of at least one HPV-related endpoint (genital HPV infections, anogenital wart diagnoses, or histologically confirmed CIN2+) between pre-vaccination and post-vaccination periods among the general population and if they used the same population sources and recruitment methods before and after vaccination. Our primary assessment was the relative risk (RR) comparing the frequency (prevalence or incidence) of HPV-related endpoints between the pre-vaccination and post-vaccination periods. We stratified all analyses by sex, age, and years since introduction of HPV vaccination. We used random-effects models to estimate pooled relative risks. Findings: We identified 1702 potentially eligible articles for this systematic review and meta-analysis, and included 65 articles in 14 high-income countries: 23 for HPV infection, 29 for anogenital warts, and 13 for CIN2+. After 5–8 years of vaccination, the prevalence of HPV 16 and 18 decreased significantly by 83% (RR 0·17, 95% CI 0·11–0·25) among girls aged 13–19 years, and decreased significantly by 66% (RR 0·34, 95% CI 0·23–0·49) among women aged 20–24 years. The prevalence of HPV 31, 33, and 45 decreased significantly by 54% (RR 0·46, 95% CI 0·33–0·66) among girls aged 13–19 years. Anogenital wart diagnoses decreased significantly by 67% (RR 0·33, 95% CI 0·24–0·46) among girls aged 15–19 years, decreased significantly by 54% (RR 0·46, 95% CI 0.36–0.60) among women aged 20–24 years, and decreased significantly by 31% (RR 0·69, 95% CI 0·53–0·89) among women aged 25–29 years. Among boys aged 15–19 years anogenital wart diagnoses decreased significantly by 48% (RR 0·52, 95% CI 0·37–0·75) and among men aged 20–24 years they decreased significantly by 32% (RR 0·68, 95% CI 0·47–0·98). After 5–9 years of vaccination, CIN2+ decreased significantly by 51% (RR 0·49, 95% CI 0·42–0·58) among screened girls aged 15–19 years and decreased significantly by 31% (RR 0·69, 95% CI 0·57–0·84) among women aged 20–24 years. Interpretation: This updated systematic review and meta-analysis includes data from 60 million individuals and up to 8 years of post-vaccination follow-up. Our results show compelling evidence of the substantial impact of HPV vaccination programmes on HPV infections and CIN2+ among girls and women, and on anogenital warts diagnoses among girls, women, boys, and men. Additionally, programmes with multi-cohort vaccination and high vaccination coverage had a greater direct impact and herd effects. Funding: WHO, Canadian Institutes of Health Research, Fonds de recherche du Québec – Santé.

KW - HPV

KW - HPV vaccine

KW - herd effect

KW - human papillomavirus

KW - vaccination programmes

UR - https://www.sciencedirect.com/journal/the-lancet

U2 - 10.1016/S0140-6736(19)30298-3

DO - 10.1016/S0140-6736(19)30298-3

M3 - Article

VL - 394

SP - 497

EP - 509

JO - Lancet

JF - Lancet

SN - 0140-6736

IS - 10197

ER -