The association between viral load and concurrent human papillomavirus infection at the genital and anal sites of young women and the impact of vaccination

Concurrent genital-anal human papillomavirus (HPV) infections may impose an increased anal cancer risk in women with HPV-related genital lesions. High viral load may facilitate genital-anal HPV concurrence. Genital and anal HPV is reduced by a bivalent HPV16/18 vaccine, yet the effect on concurrent...

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Main Authors: Kahren van Eer, Ihsane Laâbi, Birgit H.B. van Benthem, Renske D.M. Steenbergen, Audrey J. King, D. Adema, R. Buist-Arkema, A. Beerens, D. Luijt, S. Meijer, J. Schirm, M. Peeters, J. Rossen, H. Verbakel, P. van Esch, J. Verweij, A. van der Eijk, R. Huisman, C. Kerkhof, H. Korff, M. Schutten, J. Velzing, F. Verduyn-Lunel, S. Lakbiach, P. van Rosmalen, R. Schuurman, E. Doorn, L. Masthoff, E. Pannekoek, V. Sigurdsson, D. Abma, K. Adams, S. Bruisten, I. Linde, P. Oostvogel, C. Touwen, W. Vermeulen, A. Brink, J. Nelissen, P. Wolffs, N. Duijvendijk, P. Schneeberger, M. Dinnissen van Poppel, W. Melchers, Y. Poort, M.Hooghiemstra Izore, H. Huisman, J. Weel, F. Bosma, F. Geeraedts, I. Polman, P.van Goor Isala, M. Wolfhagen, C. de Mooij, E. van Koolwijk, M. Peters, C. Swanink, R. Tiemessen, T. van Zwet, J. Janssen, M. Pelsers, W. de Waal, G. Aalfs, J. Kiewiet, P. Sanders, H. van Buel- Bruins, C. van Bokhoven-Rombouts, P. Cornelissen, M. Kersten, C. van Ruitenbeek, I. Molenaar, M. Bugter, H. Götz, M. Illidge-Onder de Linden, M. Mattijssen, J. Stam, E. Swaders, F. de Groot, F. Postma, E. Brouwers, A. Niekamp, M. Smit, A. Botraby, D. Bukasa, C. de Haan, P. Hut-van Vliet, T. Taconis, M. de Graas, I. Hondelink, C. Kampman, A. Gelissen-Hansen, I. de Koning, H. van Kruchten, M. van de Pas, H. Fennema, T. Heijman, A. Hogewoning, A. van Leeuwen, M. van Rooijen, F. Neienhuijsen, M. Pelgrim
Format: Article
Language:English
Published: Elsevier 2022-06-01
Series:Tumour Virus Research
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2666679021000239
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author Kahren van Eer
Ihsane Laâbi
Birgit H.B. van Benthem
Renske D.M. Steenbergen
Audrey J. King
D. Adema
R. Buist-Arkema
A. Beerens
D. Luijt
S. Meijer
J. Schirm
M. Peeters
J. Rossen
H. Verbakel
P. van Esch
J. Verweij
A. van der Eijk
R. Huisman
C. Kerkhof
H. Korff
M. Schutten
J. Velzing
F. Verduyn-Lunel
S. Lakbiach
P. van Rosmalen
R. Schuurman
E. Doorn
L. Masthoff
E. Pannekoek
V. Sigurdsson
D. Abma
K. Adams
S. Bruisten
I. Linde
P. Oostvogel
C. Touwen
W. Vermeulen
A. Brink
J. Nelissen
P. Wolffs
N. Duijvendijk
P. Schneeberger
M. Dinnissen van Poppel
W. Melchers
Y. Poort
M.Hooghiemstra Izore
H. Huisman
J. Weel
F. Bosma
F. Geeraedts
I. Polman
P.van Goor Isala
M. Wolfhagen
C. de Mooij
E. van Koolwijk
M. Peters
C. Swanink
R. Tiemessen
T. van Zwet
J. Janssen
M. Pelsers
W. de Waal
G. Aalfs
J. Kiewiet
P. Sanders
H. van Buel- Bruins
C. van Bokhoven-Rombouts
P. Cornelissen
M. Kersten
C. van Ruitenbeek
I. Molenaar
F. Verduyn-Lunel
S. Lakbiach
P. van Rosmalen
R. Schuurman
E. Doorn
L. Masthoff
E. Pannekoek
V. Sigurdsson
M. Bugter
H. Götz
M. Illidge-Onder de Linden
M. Mattijssen
J. Stam
E. Swaders
F. de Groot
F. Postma
E. Brouwers
A. Niekamp
M. Smit
A. Botraby
D. Bukasa
C. de Haan
P. Hut-van Vliet
T. Taconis
M. de Graas
I. Hondelink
C. Kampman
A. Gelissen-Hansen
I. de Koning
H. van Kruchten
M. van de Pas
H. Fennema
T. Heijman
A. Hogewoning
A. van Leeuwen
M. van Rooijen
F. Neienhuijsen
M. Pelgrim
author_facet Kahren van Eer
Ihsane Laâbi
Birgit H.B. van Benthem
Renske D.M. Steenbergen
Audrey J. King
D. Adema
R. Buist-Arkema
A. Beerens
D. Luijt
S. Meijer
J. Schirm
M. Peeters
J. Rossen
H. Verbakel
P. van Esch
J. Verweij
A. van der Eijk
R. Huisman
C. Kerkhof
H. Korff
M. Schutten
J. Velzing
F. Verduyn-Lunel
S. Lakbiach
P. van Rosmalen
R. Schuurman
E. Doorn
L. Masthoff
E. Pannekoek
V. Sigurdsson
D. Abma
K. Adams
S. Bruisten
I. Linde
P. Oostvogel
C. Touwen
W. Vermeulen
A. Brink
J. Nelissen
P. Wolffs
N. Duijvendijk
P. Schneeberger
M. Dinnissen van Poppel
W. Melchers
Y. Poort
M.Hooghiemstra Izore
H. Huisman
J. Weel
F. Bosma
F. Geeraedts
I. Polman
P.van Goor Isala
M. Wolfhagen
C. de Mooij
E. van Koolwijk
M. Peters
C. Swanink
R. Tiemessen
T. van Zwet
J. Janssen
M. Pelsers
W. de Waal
G. Aalfs
J. Kiewiet
P. Sanders
H. van Buel- Bruins
C. van Bokhoven-Rombouts
P. Cornelissen
M. Kersten
C. van Ruitenbeek
I. Molenaar
F. Verduyn-Lunel
S. Lakbiach
P. van Rosmalen
R. Schuurman
E. Doorn
L. Masthoff
E. Pannekoek
V. Sigurdsson
M. Bugter
H. Götz
M. Illidge-Onder de Linden
M. Mattijssen
J. Stam
E. Swaders
F. de Groot
F. Postma
E. Brouwers
A. Niekamp
M. Smit
A. Botraby
D. Bukasa
C. de Haan
P. Hut-van Vliet
T. Taconis
M. de Graas
I. Hondelink
C. Kampman
A. Gelissen-Hansen
I. de Koning
H. van Kruchten
M. van de Pas
H. Fennema
T. Heijman
A. Hogewoning
A. van Leeuwen
M. van Rooijen
F. Neienhuijsen
M. Pelgrim
author_sort Kahren van Eer
collection DOAJ
description Concurrent genital-anal human papillomavirus (HPV) infections may impose an increased anal cancer risk in women with HPV-related genital lesions. High viral load may facilitate genital-anal HPV concurrence. Genital and anal HPV is reduced by a bivalent HPV16/18 vaccine, yet the effect on concurrent genital-anal HPV remains unclear.This study analyzed viral load in concurrent genital-anal HPV infections, relative to genital-only and anal-only HPV infections and the impact of vaccination in young women. We included 1074 women, who provided both genital and anal swabs. HPV detection and genotyping was performed using the SPF10-DEIA-LiPA25. HPV copy numbers were measured with type-specific qPCRs and corrected for cellular content to obtain the viral load.Concurrent genital-anal HPV often had significantly higher genital viral load (0.09–371 c/cell) than genital-only HPV (3.17E-04-15.9 c/cell, p < 0.0001 to p < 0.05). Moreover, nearly all concurrent genital-anal HPV types had higher genital copy numbers per PCR reaction (157-416E04 c/rxn) than anal copy numbers (0.90–884E01 c/rxn, p < 0.0001 to p < 0.001). Vaccinated women had significantly less infections with HPV16/18 vaccine-types (2.8% vs 13.7%, p < 0.0001) and HPV31/35/45 cross-protective types (7.4% vs 21.1%, p < 0.0001) than unvaccinated women.In conclusion, particularly high genital viral load is found in concurrent genital-anal HPV infections, which are effectively reduced by vaccination.
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spelling doaj.art-546b16f9cbd94c19aa58c2b7f562555e2022-12-22T02:10:19ZengElsevierTumour Virus Research2666-67902022-06-0113200233The association between viral load and concurrent human papillomavirus infection at the genital and anal sites of young women and the impact of vaccinationKahren van Eer0Ihsane Laâbi1Birgit H.B. van Benthem2Renske D.M. Steenbergen3Audrey J. King4D. AdemaR. Buist-ArkemaA. BeerensD. LuijtS. MeijerJ. SchirmM. PeetersJ. RossenH. VerbakelP. van EschJ. VerweijA. van der EijkR. HuismanC. KerkhofH. KorffM. SchuttenJ. VelzingF. Verduyn-LunelS. LakbiachP. van RosmalenR. SchuurmanE. DoornL. MasthoffE. PannekoekV. SigurdssonD. AbmaK. AdamsS. BruistenI. LindeP. OostvogelC. TouwenW. VermeulenA. BrinkJ. NelissenP. WolffsN. DuijvendijkP. SchneebergerM. Dinnissen van PoppelW. MelchersY. PoortM.Hooghiemstra IzoreH. HuismanJ. WeelF. BosmaF. GeeraedtsI. PolmanP.van Goor IsalaM. WolfhagenC. de MooijE. van KoolwijkM. PetersC. SwaninkR. TiemessenT. van ZwetJ. JanssenM. PelsersW. de WaalG. AalfsJ. KiewietP. SandersH. van Buel- BruinsC. van Bokhoven-RomboutsP. CornelissenM. KerstenC. van RuitenbeekI. MolenaarF. Verduyn-LunelS. LakbiachP. van RosmalenR. SchuurmanE. DoornL. MasthoffE. PannekoekV. SigurdssonM. BugterH. GötzM. Illidge-Onder de LindenM. MattijssenJ. StamE. SwadersF. de GrootF. PostmaE. BrouwersA. NiekampM. SmitA. BotrabyD. BukasaC. de HaanP. Hut-van VlietT. TaconisM. de GraasI. HondelinkC. KampmanA. Gelissen-HansenI. de KoningH. van KruchtenM. van de PasH. FennemaT. HeijmanA. HogewoningA. van LeeuwenM. van RooijenF. NeienhuijsenM. PelgrimNational Institute for Public Health and the Environment (RIVM), Centre for Infectious Disease Control, Antonie van Leeuwenhoeklaan 9, Bilthoven, the NetherlandsNational Institute for Public Health and the Environment (RIVM), Centre for Infectious Disease Control, Antonie van Leeuwenhoeklaan 9, Bilthoven, the NetherlandsNational Institute for Public Health and the Environment (RIVM), Centre for Infectious Disease Control, Antonie van Leeuwenhoeklaan 9, Bilthoven, the NetherlandsAmsterdam UMC, Vrije Universiteit Amsterdam, Pathology, Cancer Center Amsterdam, De Boelelaan 1117, Amsterdam, NetherlandsNational Institute for Public Health and the Environment (RIVM), Centre for Infectious Disease Control, Antonie van Leeuwenhoeklaan 9, Bilthoven, the Netherlands; Corresponding author.Concurrent genital-anal human papillomavirus (HPV) infections may impose an increased anal cancer risk in women with HPV-related genital lesions. High viral load may facilitate genital-anal HPV concurrence. Genital and anal HPV is reduced by a bivalent HPV16/18 vaccine, yet the effect on concurrent genital-anal HPV remains unclear.This study analyzed viral load in concurrent genital-anal HPV infections, relative to genital-only and anal-only HPV infections and the impact of vaccination in young women. We included 1074 women, who provided both genital and anal swabs. HPV detection and genotyping was performed using the SPF10-DEIA-LiPA25. HPV copy numbers were measured with type-specific qPCRs and corrected for cellular content to obtain the viral load.Concurrent genital-anal HPV often had significantly higher genital viral load (0.09–371 c/cell) than genital-only HPV (3.17E-04-15.9 c/cell, p < 0.0001 to p < 0.05). Moreover, nearly all concurrent genital-anal HPV types had higher genital copy numbers per PCR reaction (157-416E04 c/rxn) than anal copy numbers (0.90–884E01 c/rxn, p < 0.0001 to p < 0.001). Vaccinated women had significantly less infections with HPV16/18 vaccine-types (2.8% vs 13.7%, p < 0.0001) and HPV31/35/45 cross-protective types (7.4% vs 21.1%, p < 0.0001) than unvaccinated women.In conclusion, particularly high genital viral load is found in concurrent genital-anal HPV infections, which are effectively reduced by vaccination.http://www.sciencedirect.com/science/article/pii/S2666679021000239Human papillomavirusConcurrentViral loadVaccinationGenitalAnal
spellingShingle Kahren van Eer
Ihsane Laâbi
Birgit H.B. van Benthem
Renske D.M. Steenbergen
Audrey J. King
D. Adema
R. Buist-Arkema
A. Beerens
D. Luijt
S. Meijer
J. Schirm
M. Peeters
J. Rossen
H. Verbakel
P. van Esch
J. Verweij
A. van der Eijk
R. Huisman
C. Kerkhof
H. Korff
M. Schutten
J. Velzing
F. Verduyn-Lunel
S. Lakbiach
P. van Rosmalen
R. Schuurman
E. Doorn
L. Masthoff
E. Pannekoek
V. Sigurdsson
D. Abma
K. Adams
S. Bruisten
I. Linde
P. Oostvogel
C. Touwen
W. Vermeulen
A. Brink
J. Nelissen
P. Wolffs
N. Duijvendijk
P. Schneeberger
M. Dinnissen van Poppel
W. Melchers
Y. Poort
M.Hooghiemstra Izore
H. Huisman
J. Weel
F. Bosma
F. Geeraedts
I. Polman
P.van Goor Isala
M. Wolfhagen
C. de Mooij
E. van Koolwijk
M. Peters
C. Swanink
R. Tiemessen
T. van Zwet
J. Janssen
M. Pelsers
W. de Waal
G. Aalfs
J. Kiewiet
P. Sanders
H. van Buel- Bruins
C. van Bokhoven-Rombouts
P. Cornelissen
M. Kersten
C. van Ruitenbeek
I. Molenaar
F. Verduyn-Lunel
S. Lakbiach
P. van Rosmalen
R. Schuurman
E. Doorn
L. Masthoff
E. Pannekoek
V. Sigurdsson
M. Bugter
H. Götz
M. Illidge-Onder de Linden
M. Mattijssen
J. Stam
E. Swaders
F. de Groot
F. Postma
E. Brouwers
A. Niekamp
M. Smit
A. Botraby
D. Bukasa
C. de Haan
P. Hut-van Vliet
T. Taconis
M. de Graas
I. Hondelink
C. Kampman
A. Gelissen-Hansen
I. de Koning
H. van Kruchten
M. van de Pas
H. Fennema
T. Heijman
A. Hogewoning
A. van Leeuwen
M. van Rooijen
F. Neienhuijsen
M. Pelgrim
The association between viral load and concurrent human papillomavirus infection at the genital and anal sites of young women and the impact of vaccination
Tumour Virus Research
Human papillomavirus
Concurrent
Viral load
Vaccination
Genital
Anal
title The association between viral load and concurrent human papillomavirus infection at the genital and anal sites of young women and the impact of vaccination
title_full The association between viral load and concurrent human papillomavirus infection at the genital and anal sites of young women and the impact of vaccination
title_fullStr The association between viral load and concurrent human papillomavirus infection at the genital and anal sites of young women and the impact of vaccination
title_full_unstemmed The association between viral load and concurrent human papillomavirus infection at the genital and anal sites of young women and the impact of vaccination
title_short The association between viral load and concurrent human papillomavirus infection at the genital and anal sites of young women and the impact of vaccination
title_sort association between viral load and concurrent human papillomavirus infection at the genital and anal sites of young women and the impact of vaccination
topic Human papillomavirus
Concurrent
Viral load
Vaccination
Genital
Anal
url http://www.sciencedirect.com/science/article/pii/S2666679021000239
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AT hvanbuelbruins theassociationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT cvanbokhovenrombouts theassociationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT pcornelissen theassociationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT mkersten theassociationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT cvanruitenbeek theassociationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT imolenaar theassociationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT fverduynlunel theassociationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT slakbiach theassociationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT pvanrosmalen theassociationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT rschuurman theassociationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT edoorn theassociationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT lmasthoff theassociationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT epannekoek theassociationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT vsigurdsson theassociationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT mbugter theassociationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT hgotz theassociationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT millidgeonderdelinden theassociationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT mmattijssen theassociationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT jstam theassociationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT eswaders theassociationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT fdegroot theassociationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT fpostma theassociationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT ebrouwers theassociationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT aniekamp theassociationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT msmit theassociationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT abotraby theassociationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT dbukasa theassociationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT cdehaan theassociationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT phutvanvliet theassociationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT ttaconis theassociationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT mdegraas theassociationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT ihondelink theassociationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT ckampman theassociationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT agelissenhansen theassociationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT idekoning theassociationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT hvankruchten theassociationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT mvandepas theassociationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT hfennema theassociationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT theijman theassociationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT ahogewoning theassociationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT avanleeuwen theassociationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT mvanrooijen theassociationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT fneienhuijsen theassociationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT mpelgrim theassociationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT kahrenvaneer associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT ihsanelaabi associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT birgithbvanbenthem associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT renskedmsteenbergen associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT audreyjking associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT dadema associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT rbuistarkema associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT abeerens associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT dluijt associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT smeijer associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT jschirm associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT mpeeters associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT jrossen associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT hverbakel associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT pvanesch associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT jverweij associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT avandereijk associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT rhuisman associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT ckerkhof associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT hkorff associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT mschutten associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT jvelzing associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT fverduynlunel associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT slakbiach associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT pvanrosmalen associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT rschuurman associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT edoorn associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT lmasthoff associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT epannekoek associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT vsigurdsson associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT dabma associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT kadams associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT sbruisten associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT ilinde associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT poostvogel associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT ctouwen associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT wvermeulen associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT abrink associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT jnelissen associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT pwolffs associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT nduijvendijk associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT pschneeberger associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT mdinnissenvanpoppel associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT wmelchers associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT ypoort associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT mhooghiemstraizore associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT hhuisman associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT jweel associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT fbosma associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT fgeeraedts associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT ipolman associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT pvangoorisala associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT mwolfhagen associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT cdemooij associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT evankoolwijk associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT mpeters associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT cswanink associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT rtiemessen associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT tvanzwet associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT jjanssen associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT mpelsers associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT wdewaal associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT gaalfs associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT jkiewiet associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT psanders associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT hvanbuelbruins associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT cvanbokhovenrombouts associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT pcornelissen associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT mkersten associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT cvanruitenbeek associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT imolenaar associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT fverduynlunel associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT slakbiach associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT pvanrosmalen associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT rschuurman associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT edoorn associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT lmasthoff associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT epannekoek associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT vsigurdsson associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT mbugter associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT hgotz associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT millidgeonderdelinden associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT mmattijssen associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT jstam associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT eswaders associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT fdegroot associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT fpostma associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT ebrouwers associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT aniekamp associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT msmit associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT abotraby associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT dbukasa associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT cdehaan associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT phutvanvliet associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT ttaconis associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT mdegraas associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT ihondelink associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT ckampman associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT agelissenhansen associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT idekoning associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT hvankruchten associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT mvandepas associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT hfennema associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT theijman associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT ahogewoning associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT avanleeuwen associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT mvanrooijen associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT fneienhuijsen associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination
AT mpelgrim associationbetweenviralloadandconcurrenthumanpapillomavirusinfectionatthegenitalandanalsitesofyoungwomenandtheimpactofvaccination