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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Format: | Article |
Language: | English |
Published: |
Elsevier
2022-06-01
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Series: | Tumour Virus Research |
Subjects: | |
Online Access: | http://www.sciencedirect.com/science/article/pii/S2666679021000239 |
_version_ | 1818007576617418752 |
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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. |
first_indexed | 2024-04-14T05:17:30Z |
format | Article |
id | doaj.art-546b16f9cbd94c19aa58c2b7f562555e |
institution | Directory Open Access Journal |
issn | 2666-6790 |
language | English |
last_indexed | 2024-04-14T05:17:30Z |
publishDate | 2022-06-01 |
publisher | Elsevier |
record_format | Article |
series | Tumour Virus Research |
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 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 |