Population Impact of Girls-Only Human Papillomavirus 16/18 Vaccination in the Netherlands: Cross-Protective and Second-Order Herd Effects

Joske Hoes; Petra J. Woestenberg; Johannes A. Bogaards; Audrey J. King; Hester E. De Melker; Johannes Berkhof; Christian J.P.A. Hoebe; Marianne A.B. Van Der Sande; Birgit H.B. Van Benthem; D. Adema; R. Buist-Arkema; D. Luijt; S. Meijer; J. Schirm; A. Buiting; H. Verbakel; P. Van Esch; J. Verweij; A. Van Der Eijk; F. Verduyn Lunel; S. Lakbiach; R. Schuurman; D. Abma; K. Adams; S. Bruisten; I. Linde; P. Oostvogel; C. Touwen; W. Vermeulen; J. Nelissen; P. Wolffs; N. Van Duijvendijk; P. Schneeberger; M. Dinnissen-Van Poppel; W. Melchers; M. Hooghiemstra; H. Huisman; J. Weel; F. Bosma; F. Geeraedts; I. Polman; P. Van Goor; M. Wolfhagen; E. Van Koolwijk; M. Peters; C. Swanink; R. Tiemessen; J. Janssen; M. Pelsers; W. De Waal; G. Aalfs; H. Van Buel; C. Van Bokhoven-Rombouts; P. Cornelissen; M. Kersten; C. Van Ruitenbeek; I. Molenaar; E. Doorn; H. Götz; M. Illidge; J. Stam; E. Swaders; F. Postma; A. M. Niekamp; M. Smit; D. Bukasa; M. Chirandjilal; T. Taconis; M. De Graas; I. Hondelink; C. Kampman; M. Van De Pas; T. Heijman; A. Hogewoning; M. Van Rooijen; F. Neienhuijsen; M. Pelgrim

doi:10.1093/cid/ciaa1770

Population Impact of Girls-Only Human Papillomavirus 16/18 Vaccination in the Netherlands: Cross-Protective and Second-Order Herd Effects

Joske Hoes^*, Petra J. Woestenberg, Johannes A. Bogaards, Audrey J. King, Hester E. De Melker, Johannes Berkhof, Christian J.P.A. Hoebe, Marianne A.B. Van Der Sande, Birgit H.B. Van Benthem, D. Adema, R. Buist-Arkema, D. Luijt, S. Meijer, J. Schirm, A. Buiting, H. Verbakel, P. Van Esch, J. Verweij, A. Van Der Eijk, F. Verduyn LunelS. Lakbiach, R. Schuurman, D. Abma, K. Adams, S. Bruisten, I. Linde, P. Oostvogel, C. Touwen, W. Vermeulen, J. Nelissen, P. Wolffs, N. Van Duijvendijk, P. Schneeberger, M. Dinnissen-Van Poppel, W. Melchers, M. Hooghiemstra, H. Huisman, J. Weel, F. Bosma, F. Geeraedts, I. Polman, P. Van Goor, M. Wolfhagen, E. Van Koolwijk, M. Peters, C. Swanink, R. Tiemessen, J. Janssen, M. Pelsers, W. De Waal, G. Aalfs, H. Van Buel, C. Van Bokhoven-Rombouts, P. Cornelissen, M. Kersten, C. Van Ruitenbeek, I. Molenaar, E. Doorn, H. Götz, M. Illidge, J. Stam, E. Swaders, F. Postma, A. M. Niekamp, M. Smit, D. Bukasa, M. Chirandjilal, T. Taconis, M. De Graas, I. Hondelink, C. Kampman, M. Van De Pas, T. Heijman, A. Hogewoning, M. Van Rooijen, F. Neienhuijsen, M. Pelgrim

^*Corresponding author for this work

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Abstract

Background: Human papillomavirus (HPV) vaccination programs achieve substantial population-level impact, with effects extending beyond protection of vaccinated individuals. We assessed trends in HPV prevalence up to 8 years postvaccination among men and women in the Netherlands, where bivalent HPV vaccination, targeting HPV types 16/18, has been offered to (pre)adolescent girls since 2009 with moderate vaccination coverage. Methods: We used data from the PASSYON study, a survey initiated in 2009 (prevaccination) and repeated biennially among 16-to 24-year-old visitors of sexual health centers. We studied genital HPV positivity from 2009 to 2017 among women, heterosexual men, and unvaccinated women using Poisson generalized estimating equation models, adjusted for individual-and population-level confounders. Trends were studied for 25 HPV types detected by the SPF10-LiPA25 platform. Results: A total of 6354 women (64.7% self-reported unvaccinated) and 2414 heterosexual men were included. Percentual declines in vaccine types HPV-16/18 were observed for all women (12.6% per year [95% confidence interval {CI}, 10.6-14.5]), heterosexual men (13.0% per year [95% CI, 8.3-17.5]), and unvaccinated women (5.4% per year [95% CI, 2.9-7.8]). We observed significant declines in HPV-31 (all women and heterosexual men), HPV-45 (all women), and in all high-risk HPV types pooled (all women and heterosexual men). Significant increases were observed for HPV-56 (all women) and HPV-52 (unvaccinated women). Conclusions: Our results provide evidence for first-order herd effects among heterosexual men against HPV-16/18 and cross-protective types. Additionally, we show second-order herd effects against vaccine types among unvaccinated women. These results are promising regarding population-level and clinical impact of girls-only bivalent HPV vaccination in a country with moderate vaccine uptake.

Original language	English
Pages (from-to)	e103-e111
Journal	Clinical Infectious Diseases
Volume	72
Issue number	5
DOIs	https://doi.org/10.1093/cid/ciaa1770
Publication status	Published - 1 Mar 2021

Keywords

herd immunity
HPV
human papillomavirus
population effects
type replacement
vaccination
Prevalence
Cross-Sectional Studies
Humans
Vaccination
Male
Papillomavirus Infections/epidemiology
Human papillomavirus 18
Young Adult
Human papillomavirus 16
Adolescent
Adult
Female
Netherlands/epidemiology
Papillomavirus Vaccines

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Hoes, J., Woestenberg, P. J., Bogaards, J. A., King, A. J., De Melker, H. E., Berkhof, J., Hoebe, C. J. P. A., Van Der Sande, M. A. B., Van Benthem, B. H. B., Adema, D., Buist-Arkema, R., Luijt, D., Meijer, S., Schirm, J., Buiting, A., Verbakel, H., Van Esch, P., Verweij, J., Van Der Eijk, A., ... Pelgrim, M. (2021). Population Impact of Girls-Only Human Papillomavirus 16/18 Vaccination in the Netherlands: Cross-Protective and Second-Order Herd Effects. Clinical Infectious Diseases, 72(5), e103-e111. https://doi.org/10.1093/cid/ciaa1770

@article{14bec257a7734f1582c62d9780703ec9,

title = "Population Impact of Girls-Only Human Papillomavirus 16/18 Vaccination in the Netherlands: Cross-Protective and Second-Order Herd Effects",

abstract = "Background: Human papillomavirus (HPV) vaccination programs achieve substantial population-level impact, with effects extending beyond protection of vaccinated individuals. We assessed trends in HPV prevalence up to 8 years postvaccination among men and women in the Netherlands, where bivalent HPV vaccination, targeting HPV types 16/18, has been offered to (pre)adolescent girls since 2009 with moderate vaccination coverage. Methods: We used data from the PASSYON study, a survey initiated in 2009 (prevaccination) and repeated biennially among 16-to 24-year-old visitors of sexual health centers. We studied genital HPV positivity from 2009 to 2017 among women, heterosexual men, and unvaccinated women using Poisson generalized estimating equation models, adjusted for individual-and population-level confounders. Trends were studied for 25 HPV types detected by the SPF10-LiPA25 platform. Results: A total of 6354 women (64.7% self-reported unvaccinated) and 2414 heterosexual men were included. Percentual declines in vaccine types HPV-16/18 were observed for all women (12.6% per year [95% confidence interval {CI}, 10.6-14.5]), heterosexual men (13.0% per year [95% CI, 8.3-17.5]), and unvaccinated women (5.4% per year [95% CI, 2.9-7.8]). We observed significant declines in HPV-31 (all women and heterosexual men), HPV-45 (all women), and in all high-risk HPV types pooled (all women and heterosexual men). Significant increases were observed for HPV-56 (all women) and HPV-52 (unvaccinated women). Conclusions: Our results provide evidence for first-order herd effects among heterosexual men against HPV-16/18 and cross-protective types. Additionally, we show second-order herd effects against vaccine types among unvaccinated women. These results are promising regarding population-level and clinical impact of girls-only bivalent HPV vaccination in a country with moderate vaccine uptake.",

keywords = "herd immunity, HPV, human papillomavirus, population effects, type replacement, vaccination, Prevalence, Cross-Sectional Studies, Humans, Vaccination, Male, Papillomavirus Infections/epidemiology, Human papillomavirus 18, Young Adult, Human papillomavirus 16, Adolescent, Adult, Female, Netherlands/epidemiology, Papillomavirus Vaccines",

author = "Joske Hoes and Woestenberg, {Petra J.} and Bogaards, {Johannes A.} and King, {Audrey J.} and {De Melker}, {Hester E.} and Johannes Berkhof and Hoebe, {Christian J.P.A.} and {Van Der Sande}, {Marianne A.B.} and {Van Benthem}, {Birgit H.B.} and D. Adema and R. Buist-Arkema and D. Luijt and S. Meijer and J. Schirm and A. Buiting and H. Verbakel and {Van Esch}, P. and J. Verweij and {Van Der Eijk}, A. and {Verduyn Lunel}, F. and S. Lakbiach and R. Schuurman and D. Abma and K. Adams and S. Bruisten and I. Linde and P. Oostvogel and C. Touwen and W. Vermeulen and J. Nelissen and P. Wolffs and {Van Duijvendijk}, N. and P. Schneeberger and {Dinnissen-Van Poppel}, M. and W. Melchers and M. Hooghiemstra and H. Huisman and J. Weel and F. Bosma and F. Geeraedts and I. Polman and {Van Goor}, P. and M. Wolfhagen and {Van Koolwijk}, E. and M. Peters and C. Swanink and R. Tiemessen and J. Janssen and M. Pelsers and {De Waal}, W. and G. Aalfs and {Van Buel}, H. and {Van Bokhoven-Rombouts}, C. and P. Cornelissen and M. Kersten and {Van Ruitenbeek}, C. and I. Molenaar and E. Doorn and H. G{\"o}tz and M. Illidge and J. Stam and E. Swaders and F. Postma and Niekamp, {A. M.} and M. Smit and D. Bukasa and M. Chirandjilal and T. Taconis and {De Graas}, M. and I. Hondelink and C. Kampman and {Van De Pas}, M. and T. Heijman and A. Hogewoning and {Van Rooijen}, M. and F. Neienhuijsen and M. Pelgrim",

note = "Publisher Copyright: {\textcopyright} 2020 The Author(s) 2020. Published by Oxford University Press for the Infectious Diseases Society of America.",

year = "2021",

month = mar,

day = "1",

doi = "10.1093/cid/ciaa1770",

language = "English",

volume = "72",

pages = "e103--e111",

journal = "Clinical Infectious Diseases",

issn = "1058-4838",

publisher = "Oxford University Press",

number = "5",

}

Hoes, J, Woestenberg, PJ, Bogaards, JA, King, AJ, De Melker, HE, Berkhof, J, Hoebe, CJPA, Van Der Sande, MAB, Van Benthem, BHB, Adema, D, Buist-Arkema, R, Luijt, D, Meijer, S, Schirm, J, Buiting, A, Verbakel, H, Van Esch, P, Verweij, J, Van Der Eijk, A, Verduyn Lunel, F, Lakbiach, S, Schuurman, R, Abma, D, Adams, K, Bruisten, S, Linde, I, Oostvogel, P, Touwen, C, Vermeulen, W, Nelissen, J, Wolffs, P, Van Duijvendijk, N, Schneeberger, P, Dinnissen-Van Poppel, M, Melchers, W, Hooghiemstra, M, Huisman, H, Weel, J, Bosma, F, Geeraedts, F, Polman, I, Van Goor, P, Wolfhagen, M, Van Koolwijk, E, Peters, M, Swanink, C, Tiemessen, R, Janssen, J, Pelsers, M, De Waal, W, Aalfs, G, Van Buel, H, Van Bokhoven-Rombouts, C, Cornelissen, P, Kersten, M, Van Ruitenbeek, C, Molenaar, I, Doorn, E, Götz, H, Illidge, M, Stam, J, Swaders, E, Postma, F, Niekamp, AM, Smit, M, Bukasa, D, Chirandjilal, M, Taconis, T, De Graas, M, Hondelink, I, Kampman, C, Van De Pas, M, Heijman, T, Hogewoning, A, Van Rooijen, M, Neienhuijsen, F & Pelgrim, M 2021, 'Population Impact of Girls-Only Human Papillomavirus 16/18 Vaccination in the Netherlands: Cross-Protective and Second-Order Herd Effects', Clinical Infectious Diseases, vol. 72, no. 5, pp. e103-e111. https://doi.org/10.1093/cid/ciaa1770

TY - JOUR

T1 - Population Impact of Girls-Only Human Papillomavirus 16/18 Vaccination in the Netherlands

T2 - Cross-Protective and Second-Order Herd Effects

AU - Hoes, Joske

AU - Woestenberg, Petra J.

AU - Bogaards, Johannes A.

AU - King, Audrey J.

AU - De Melker, Hester E.

AU - Berkhof, Johannes

AU - Hoebe, Christian J.P.A.

AU - Van Der Sande, Marianne A.B.

AU - Van Benthem, Birgit H.B.

AU - Adema, D.

AU - Buist-Arkema, R.

AU - Luijt, D.

AU - Meijer, S.

AU - Schirm, J.

AU - Buiting, A.

AU - Verbakel, H.

AU - Van Esch, P.

AU - Verweij, J.

AU - Van Der Eijk, A.

AU - Verduyn Lunel, F.

AU - Lakbiach, S.

AU - Schuurman, R.

AU - Abma, D.

AU - Adams, K.

AU - Bruisten, S.

AU - Linde, I.

AU - Oostvogel, P.

AU - Touwen, C.

AU - Vermeulen, W.

AU - Nelissen, J.

AU - Wolffs, P.

AU - Van Duijvendijk, N.

AU - Schneeberger, P.

AU - Dinnissen-Van Poppel, M.

AU - Melchers, W.

AU - Hooghiemstra, M.

AU - Huisman, H.

AU - Weel, J.

AU - Bosma, F.

AU - Geeraedts, F.

AU - Polman, I.

AU - Van Goor, P.

AU - Wolfhagen, M.

AU - Van Koolwijk, E.

AU - Peters, M.

AU - Swanink, C.

AU - Tiemessen, R.

AU - Janssen, J.

AU - Pelsers, M.

AU - De Waal, W.

AU - Aalfs, G.

AU - Van Buel, H.

AU - Van Bokhoven-Rombouts, C.

AU - Cornelissen, P.

AU - Kersten, M.

AU - Van Ruitenbeek, C.

AU - Molenaar, I.

AU - Doorn, E.

AU - Götz, H.

AU - Illidge, M.

AU - Stam, J.

AU - Swaders, E.

AU - Postma, F.

AU - Niekamp, A. M.

AU - Smit, M.

AU - Bukasa, D.

AU - Chirandjilal, M.

AU - Taconis, T.

AU - De Graas, M.

AU - Hondelink, I.

AU - Kampman, C.

AU - Van De Pas, M.

AU - Heijman, T.

AU - Hogewoning, A.

AU - Van Rooijen, M.

AU - Neienhuijsen, F.

AU - Pelgrim, M.

PY - 2021/3/1

Y1 - 2021/3/1

N2 - Background: Human papillomavirus (HPV) vaccination programs achieve substantial population-level impact, with effects extending beyond protection of vaccinated individuals. We assessed trends in HPV prevalence up to 8 years postvaccination among men and women in the Netherlands, where bivalent HPV vaccination, targeting HPV types 16/18, has been offered to (pre)adolescent girls since 2009 with moderate vaccination coverage. Methods: We used data from the PASSYON study, a survey initiated in 2009 (prevaccination) and repeated biennially among 16-to 24-year-old visitors of sexual health centers. We studied genital HPV positivity from 2009 to 2017 among women, heterosexual men, and unvaccinated women using Poisson generalized estimating equation models, adjusted for individual-and population-level confounders. Trends were studied for 25 HPV types detected by the SPF10-LiPA25 platform. Results: A total of 6354 women (64.7% self-reported unvaccinated) and 2414 heterosexual men were included. Percentual declines in vaccine types HPV-16/18 were observed for all women (12.6% per year [95% confidence interval {CI}, 10.6-14.5]), heterosexual men (13.0% per year [95% CI, 8.3-17.5]), and unvaccinated women (5.4% per year [95% CI, 2.9-7.8]). We observed significant declines in HPV-31 (all women and heterosexual men), HPV-45 (all women), and in all high-risk HPV types pooled (all women and heterosexual men). Significant increases were observed for HPV-56 (all women) and HPV-52 (unvaccinated women). Conclusions: Our results provide evidence for first-order herd effects among heterosexual men against HPV-16/18 and cross-protective types. Additionally, we show second-order herd effects against vaccine types among unvaccinated women. These results are promising regarding population-level and clinical impact of girls-only bivalent HPV vaccination in a country with moderate vaccine uptake.

AB - Background: Human papillomavirus (HPV) vaccination programs achieve substantial population-level impact, with effects extending beyond protection of vaccinated individuals. We assessed trends in HPV prevalence up to 8 years postvaccination among men and women in the Netherlands, where bivalent HPV vaccination, targeting HPV types 16/18, has been offered to (pre)adolescent girls since 2009 with moderate vaccination coverage. Methods: We used data from the PASSYON study, a survey initiated in 2009 (prevaccination) and repeated biennially among 16-to 24-year-old visitors of sexual health centers. We studied genital HPV positivity from 2009 to 2017 among women, heterosexual men, and unvaccinated women using Poisson generalized estimating equation models, adjusted for individual-and population-level confounders. Trends were studied for 25 HPV types detected by the SPF10-LiPA25 platform. Results: A total of 6354 women (64.7% self-reported unvaccinated) and 2414 heterosexual men were included. Percentual declines in vaccine types HPV-16/18 were observed for all women (12.6% per year [95% confidence interval {CI}, 10.6-14.5]), heterosexual men (13.0% per year [95% CI, 8.3-17.5]), and unvaccinated women (5.4% per year [95% CI, 2.9-7.8]). We observed significant declines in HPV-31 (all women and heterosexual men), HPV-45 (all women), and in all high-risk HPV types pooled (all women and heterosexual men). Significant increases were observed for HPV-56 (all women) and HPV-52 (unvaccinated women). Conclusions: Our results provide evidence for first-order herd effects among heterosexual men against HPV-16/18 and cross-protective types. Additionally, we show second-order herd effects against vaccine types among unvaccinated women. These results are promising regarding population-level and clinical impact of girls-only bivalent HPV vaccination in a country with moderate vaccine uptake.

KW - herd immunity

KW - HPV

KW - human papillomavirus

KW - population effects

KW - type replacement

KW - vaccination

KW - Prevalence

KW - Cross-Sectional Studies

KW - Humans

KW - Vaccination

KW - Male

KW - Papillomavirus Infections/epidemiology

KW - Human papillomavirus 18

KW - Young Adult

KW - Human papillomavirus 16

KW - Adolescent

KW - Adult

KW - Female

KW - Netherlands/epidemiology

KW - Papillomavirus Vaccines

UR - http://www.scopus.com/inward/record.url?scp=85102657647&partnerID=8YFLogxK

U2 - 10.1093/cid/ciaa1770

DO - 10.1093/cid/ciaa1770

M3 - Article

C2 - 33249475

AN - SCOPUS:85102657647

SN - 1058-4838

VL - 72

SP - e103-e111

JO - Clinical Infectious Diseases

JF - Clinical Infectious Diseases

IS - 5

ER -

Population Impact of Girls-Only Human Papillomavirus 16/18 Vaccination in the Netherlands: Cross-Protective and Second-Order Herd Effects

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