Population-level impact and herd effects following human papillomavirus vaccination programmes: a systematic review and meta-analysis

Mélanie Drolet; Élodie Bénard; Marie-Claude Boily; Hammad Ali; Louise Baandrup; Heidi Bauer; Simon Beddows; Jacques Brisson; Julia M L Brotherton; Teresa Cummings; Basil Donovan; Christopher K Fairley; Elaine W Flagg; Anne M Johnson; Jessica A Kahn; Kimberley Kavanagh; Susanne K Kjaer; Erich V Kliewer; Philippe Lemieux-Mellouki; Lauri Markowitz; Aminata Mboup; David Mesher; Linda Niccolai; Jeannie Oliphant; Kevin G Pollock; Kate Soldan; Pam Sonnenberg; Sepehr N Tabrizi; Clare Tanton; Marc Brisson

doi:10.1016/S1473-3099(14)71073-4

Population-level impact and herd effects following human papillomavirus vaccination programmes: a systematic review and meta-analysis

Mélanie Drolet, Élodie Bénard, Marie-Claude Boily, Hammad Ali, Louise Baandrup, Heidi Bauer, Simon Beddows, Jacques Brisson, Julia M L Brotherton, Teresa Cummings, Basil Donovan, Christopher K Fairley, Elaine W Flagg, Anne M Johnson, Jessica A Kahn, Kimberley Kavanagh, Susanne K Kjaer, Erich V Kliewer, Philippe Lemieux-Mellouki, Lauri MarkowitzAminata Mboup, David Mesher, Linda Niccolai, Jeannie Oliphant, Kevin G Pollock, Kate Soldan, Pam Sonnenberg, Sepehr N Tabrizi, Clare Tanton, Marc Brisson

Department of Clinical Medicine

428 Citations (Scopus)

Abstract

BACKGROUND: Human papillomavirus (HPV) vaccination programmes were first implemented in several countries worldwide in 2007. We did a systematic review and meta-analysis to assess the population-level consequences and herd effects after female HPV vaccination programmes, to verify whether or not the high efficacy reported in randomised controlled clinical trials are materialising in real-world situations.

METHODS: We searched the Medline and Embase databases (between Jan 1, 2007 and Feb 28, 2014) and conference abstracts for time-trend studies that analysed changes, between the pre-vaccination and post-vaccination periods, in the incidence or prevalence of at least one HPV-related endpoint: HPV infection, anogenital warts, and high-grade cervical lesions. We used random-effects models to derive pooled relative risk (RR) estimates. We stratified all analyses by age and sex. We did subgroup analyses by comparing studies according to vaccine type, vaccination coverage, and years since implementation of the vaccination programme. We assessed heterogeneity across studies using I(2) and χ(2) statistics and we did trends analysis to examine the dose-response association between HPV vaccination coverage and each study effect measure.

FINDINGS: We identified 20 eligible studies, which were all undertaken in nine high-income countries and represent more than 140 million person-years of follow-up. In countries with female vaccination coverage of at least 50%, HPV type 16 and 18 infections decreased significantly between the pre-vaccination and post-vaccination periods by 68% (RR 0·32, 95% CI 0·19-0·52) and anogenital warts decreased significantly by 61% (0·39, 0·22-0·71) in girls 13-19 years of age. Significant reductions were also recorded in HPV types 31, 33, and 45 in this age group of girls (RR 0·72, 95% CI 0·54-0·96), which suggests cross-protection. Additionally, significant reductions in anogenital warts were also reported in boys younger than 20 years of age (0·66 [95% CI 0·47-0·91]) and in women 20-39 years of age (0·68 [95% CI 0·51-0·89]), which suggests herd effects. In countries with female vaccination coverage lower than 50%, significant reductions in HPV types 16 and 18 infection (RR 0·50, 95% CI 0·34-0·74]) and in anogenital warts (0·86 [95% CI 0·79-0·94]) occurred in girls younger than 20 years of age, with no indication of cross-protection or herd effects.

INTERPRETATION: Our results are promising for the long-term population-level effects of HPV vaccination programmes. However, continued monitoring is essential to identify any signals of potential waning efficacy or type-replacement.

FUNDING: The Canadian Institutes of Health Research.

Original language	English
Journal	Lancet Infectious Diseases
Volume	15
Issue number	5
Pages (from-to)	565-80
Number of pages	16
ISSN	1473-3099
DOIs	https://doi.org/10.1016/S1473-3099(14)71073-4
Publication status	Published - 1 May 2015

Keywords

Adolescent
Adult
Condylomata Acuminata
Cost-Benefit Analysis
Cross Protection
Developed Countries
Female
Humans
Immunization Programs
Male
Papillomaviridae
Papillomavirus Infections
Papillomavirus Vaccines
Uterine Cervical Neoplasms
Vaccination

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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10.1016/S1473-3099(14)71073-4

Cite this

Drolet, M., Bénard, É., Boily, M.-C., Ali, H., Baandrup, L., Bauer, H., Beddows, S., Brisson, J., Brotherton, J. M. L., Cummings, T., Donovan, B., Fairley, C. K., Flagg, E. W., Johnson, A. M., Kahn, J. A., Kavanagh, K., Kjaer, S. K., Kliewer, E. V., Lemieux-Mellouki, P., ... Brisson, M. (2015). Population-level impact and herd effects following human papillomavirus vaccination programmes: a systematic review and meta-analysis. Lancet Infectious Diseases, 15(5), 565-80. https://doi.org/10.1016/S1473-3099(14)71073-4

Drolet, M, Bénard, É, Boily, M-C, Ali, H, Baandrup, L, Bauer, H, Beddows, S, Brisson, J, Brotherton, JML, Cummings, T, Donovan, B, Fairley, CK, Flagg, EW, Johnson, AM, Kahn, JA, Kavanagh, K, Kjaer, SK, Kliewer, EV, Lemieux-Mellouki, P, Markowitz, L, Mboup, A, Mesher, D, Niccolai, L, Oliphant, J, Pollock, KG, Soldan, K, Sonnenberg, P, Tabrizi, SN, Tanton, C & Brisson, M 2015, 'Population-level impact and herd effects following human papillomavirus vaccination programmes: a systematic review and meta-analysis', Lancet Infectious Diseases, vol. 15, no. 5, pp. 565-80. https://doi.org/10.1016/S1473-3099(14)71073-4

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abstract = "BACKGROUND: Human papillomavirus (HPV) vaccination programmes were first implemented in several countries worldwide in 2007. We did a systematic review and meta-analysis to assess the population-level consequences and herd effects after female HPV vaccination programmes, to verify whether or not the high efficacy reported in randomised controlled clinical trials are materialising in real-world situations.METHODS: We searched the Medline and Embase databases (between Jan 1, 2007 and Feb 28, 2014) and conference abstracts for time-trend studies that analysed changes, between the pre-vaccination and post-vaccination periods, in the incidence or prevalence of at least one HPV-related endpoint: HPV infection, anogenital warts, and high-grade cervical lesions. We used random-effects models to derive pooled relative risk (RR) estimates. We stratified all analyses by age and sex. We did subgroup analyses by comparing studies according to vaccine type, vaccination coverage, and years since implementation of the vaccination programme. We assessed heterogeneity across studies using I(2) and χ(2) statistics and we did trends analysis to examine the dose-response association between HPV vaccination coverage and each study effect measure.FINDINGS: We identified 20 eligible studies, which were all undertaken in nine high-income countries and represent more than 140 million person-years of follow-up. In countries with female vaccination coverage of at least 50%, HPV type 16 and 18 infections decreased significantly between the pre-vaccination and post-vaccination periods by 68% (RR 0·32, 95% CI 0·19-0·52) and anogenital warts decreased significantly by 61% (0·39, 0·22-0·71) in girls 13-19 years of age. Significant reductions were also recorded in HPV types 31, 33, and 45 in this age group of girls (RR 0·72, 95% CI 0·54-0·96), which suggests cross-protection. Additionally, significant reductions in anogenital warts were also reported in boys younger than 20 years of age (0·66 [95% CI 0·47-0·91]) and in women 20-39 years of age (0·68 [95% CI 0·51-0·89]), which suggests herd effects. In countries with female vaccination coverage lower than 50%, significant reductions in HPV types 16 and 18 infection (RR 0·50, 95% CI 0·34-0·74]) and in anogenital warts (0·86 [95% CI 0·79-0·94]) occurred in girls younger than 20 years of age, with no indication of cross-protection or herd effects.INTERPRETATION: Our results are promising for the long-term population-level effects of HPV vaccination programmes. However, continued monitoring is essential to identify any signals of potential waning efficacy or type-replacement.FUNDING: The Canadian Institutes of Health Research.",

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author = "M{\'e}lanie Drolet and {\'E}lodie B{\'e}nard and Marie-Claude Boily and Hammad Ali and Louise Baandrup and Heidi Bauer and Simon Beddows and Jacques Brisson and Brotherton, {Julia M L} and Teresa Cummings and Basil Donovan and Fairley, {Christopher K} and Flagg, {Elaine W} and Johnson, {Anne M} and Kahn, {Jessica A} and Kimberley Kavanagh and Kjaer, {Susanne K} and Kliewer, {Erich V} and Philippe Lemieux-Mellouki and Lauri Markowitz and Aminata Mboup and David Mesher and Linda Niccolai and Jeannie Oliphant and Pollock, {Kevin G} and Kate Soldan and Pam Sonnenberg and Tabrizi, {Sepehr N} and Clare Tanton and Marc Brisson",

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doi = "10.1016/S1473-3099(14)71073-4",

language = "English",

volume = "15",

pages = "565--80",

journal = "Lancet Infectious Diseases",

issn = "1473-3099",

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TY - JOUR

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

T2 - a systematic review and meta-analysis

AU - Drolet, Mélanie

AU - Bénard, Élodie

AU - Boily, Marie-Claude

AU - Ali, Hammad

AU - Baandrup, Louise

AU - Bauer, Heidi

AU - Beddows, Simon

AU - Brisson, Jacques

AU - Brotherton, Julia M L

AU - Cummings, Teresa

AU - Donovan, Basil

AU - Fairley, Christopher K

AU - Flagg, Elaine W

AU - Johnson, Anne M

AU - Kahn, Jessica A

AU - Kavanagh, Kimberley

AU - Kjaer, Susanne K

AU - Kliewer, Erich V

AU - Lemieux-Mellouki, Philippe

AU - Markowitz, Lauri

AU - Mboup, Aminata

AU - Mesher, David

AU - Niccolai, Linda

AU - Oliphant, Jeannie

AU - Pollock, Kevin G

AU - Soldan, Kate

AU - Sonnenberg, Pam

AU - Tabrizi, Sepehr N

AU - Tanton, Clare

AU - Brisson, Marc

PY - 2015/5/1

Y1 - 2015/5/1

N2 - BACKGROUND: Human papillomavirus (HPV) vaccination programmes were first implemented in several countries worldwide in 2007. We did a systematic review and meta-analysis to assess the population-level consequences and herd effects after female HPV vaccination programmes, to verify whether or not the high efficacy reported in randomised controlled clinical trials are materialising in real-world situations.METHODS: We searched the Medline and Embase databases (between Jan 1, 2007 and Feb 28, 2014) and conference abstracts for time-trend studies that analysed changes, between the pre-vaccination and post-vaccination periods, in the incidence or prevalence of at least one HPV-related endpoint: HPV infection, anogenital warts, and high-grade cervical lesions. We used random-effects models to derive pooled relative risk (RR) estimates. We stratified all analyses by age and sex. We did subgroup analyses by comparing studies according to vaccine type, vaccination coverage, and years since implementation of the vaccination programme. We assessed heterogeneity across studies using I(2) and χ(2) statistics and we did trends analysis to examine the dose-response association between HPV vaccination coverage and each study effect measure.FINDINGS: We identified 20 eligible studies, which were all undertaken in nine high-income countries and represent more than 140 million person-years of follow-up. In countries with female vaccination coverage of at least 50%, HPV type 16 and 18 infections decreased significantly between the pre-vaccination and post-vaccination periods by 68% (RR 0·32, 95% CI 0·19-0·52) and anogenital warts decreased significantly by 61% (0·39, 0·22-0·71) in girls 13-19 years of age. Significant reductions were also recorded in HPV types 31, 33, and 45 in this age group of girls (RR 0·72, 95% CI 0·54-0·96), which suggests cross-protection. Additionally, significant reductions in anogenital warts were also reported in boys younger than 20 years of age (0·66 [95% CI 0·47-0·91]) and in women 20-39 years of age (0·68 [95% CI 0·51-0·89]), which suggests herd effects. In countries with female vaccination coverage lower than 50%, significant reductions in HPV types 16 and 18 infection (RR 0·50, 95% CI 0·34-0·74]) and in anogenital warts (0·86 [95% CI 0·79-0·94]) occurred in girls younger than 20 years of age, with no indication of cross-protection or herd effects.INTERPRETATION: Our results are promising for the long-term population-level effects of HPV vaccination programmes. However, continued monitoring is essential to identify any signals of potential waning efficacy or type-replacement.FUNDING: The Canadian Institutes of Health Research.

AB - BACKGROUND: Human papillomavirus (HPV) vaccination programmes were first implemented in several countries worldwide in 2007. We did a systematic review and meta-analysis to assess the population-level consequences and herd effects after female HPV vaccination programmes, to verify whether or not the high efficacy reported in randomised controlled clinical trials are materialising in real-world situations.METHODS: We searched the Medline and Embase databases (between Jan 1, 2007 and Feb 28, 2014) and conference abstracts for time-trend studies that analysed changes, between the pre-vaccination and post-vaccination periods, in the incidence or prevalence of at least one HPV-related endpoint: HPV infection, anogenital warts, and high-grade cervical lesions. We used random-effects models to derive pooled relative risk (RR) estimates. We stratified all analyses by age and sex. We did subgroup analyses by comparing studies according to vaccine type, vaccination coverage, and years since implementation of the vaccination programme. We assessed heterogeneity across studies using I(2) and χ(2) statistics and we did trends analysis to examine the dose-response association between HPV vaccination coverage and each study effect measure.FINDINGS: We identified 20 eligible studies, which were all undertaken in nine high-income countries and represent more than 140 million person-years of follow-up. In countries with female vaccination coverage of at least 50%, HPV type 16 and 18 infections decreased significantly between the pre-vaccination and post-vaccination periods by 68% (RR 0·32, 95% CI 0·19-0·52) and anogenital warts decreased significantly by 61% (0·39, 0·22-0·71) in girls 13-19 years of age. Significant reductions were also recorded in HPV types 31, 33, and 45 in this age group of girls (RR 0·72, 95% CI 0·54-0·96), which suggests cross-protection. Additionally, significant reductions in anogenital warts were also reported in boys younger than 20 years of age (0·66 [95% CI 0·47-0·91]) and in women 20-39 years of age (0·68 [95% CI 0·51-0·89]), which suggests herd effects. In countries with female vaccination coverage lower than 50%, significant reductions in HPV types 16 and 18 infection (RR 0·50, 95% CI 0·34-0·74]) and in anogenital warts (0·86 [95% CI 0·79-0·94]) occurred in girls younger than 20 years of age, with no indication of cross-protection or herd effects.INTERPRETATION: Our results are promising for the long-term population-level effects of HPV vaccination programmes. However, continued monitoring is essential to identify any signals of potential waning efficacy or type-replacement.FUNDING: The Canadian Institutes of Health Research.

KW - Adolescent

KW - Adult

KW - Condylomata Acuminata

KW - Cost-Benefit Analysis

KW - Cross Protection

KW - Developed Countries

KW - Female

KW - Humans

KW - Immunization Programs

KW - Male

KW - Papillomaviridae

KW - Papillomavirus Infections

KW - Papillomavirus Vaccines

KW - Uterine Cervical Neoplasms

KW - Vaccination

U2 - 10.1016/S1473-3099(14)71073-4

DO - 10.1016/S1473-3099(14)71073-4

M3 - Journal article

C2 - 25744474

SN - 1473-3099

VL - 15

SP - 565

EP - 580

JO - Lancet Infectious Diseases

JF - Lancet Infectious Diseases

IS - 5

ER -

Population-level impact and herd effects following human papillomavirus vaccination programmes: a systematic review and meta-analysis

Abstract

Keywords

UN SDGs

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