Human papillomavirus DNA prevalence and type distribution in anal carcinomas worldwide

Laia Alemany, Maëlle Saunier, Isabel Alvarado-Cabrero, Beatriz Quirõs, Jorge Salmeron, Hai Rim Shin, Edyta C. Pirog, Núria Guimerà, Gustavo Hernandez-Suarez, Ana Felix, Omar Clavero, Belen Lloveras, Elena Kasamatsu, Marc T. Goodman, Brenda Y. Hernandez, Jan Laco, Leopoldo Tinoco, Daan T. Geraets, Charles F. Lynch, Vaclav Mandys & 14 others Mario Poljak, Robert Jach, Josep Verge, Christine Clavel, Cathy Ndiaye, Joellen Klaustermeier, Antonio Cubilla, Xavier Castellsagué, Ignacio G. Bravo, Michael Pawlita, William G. Quint, Nubia Muñoz, Francesc X. Bosch, Silvia De Sanjosé

Research output: Contribution to journalArticle

165 Citations (Scopus)

Abstract

Knowledge about human papillomaviruses (HPV) types involved in anal cancers in some world regions is scanty. Here, we describe the HPV DNA prevalence and type distribution in a series of invasive anal cancers and anal intraepithelial neoplasias (AIN) grades 2/3 from 24 countries. We analyzed 43 AIN 2/3 cases and 496 anal cancers diagnosed from 1986 to 2011. After histopathological evaluation of formalin-fixed paraffin-embedded samples, HPV DNA detection and genotyping was performed using SPF-10/DEIA/LiPA25 system (version 1). A subset of 116 cancers was further tested for p16INK4a expression, a cellular surrogate marker for HPV-associated transformation. Prevalence ratios were estimated using multivariate Poisson regression with robust variance in the anal cancer data set. HPV DNA was detected in 88.3% of anal cancers (95% confidence interval [CI]: 85.1-91.0%) and in 95.3% of AIN 2/3 (95% CI: 84.2-99.4%). Among cancers, the highest prevalence was observed in warty-basaloid subtype of squamous cell carcinomas, in younger patients and in North American geographical region. There were no statistically significant differences in prevalence by gender. HPV16 was the most frequent HPV type detected in both cancers (80.7%) and AIN 2/3 lesions (75.4%). HPV18 was the second most common type in invasive cancers (3.6%). p16INK4a overexpression was found in 95% of HPV DNA-positive anal cancers. In view of the results of HPV DNA and high proportion of p16INK4a overexpression, infection by HPV is most likely to be a necessary cause for anal cancers in both men and women. The large contribution of HPV16 reinforces the potential impact of HPV vaccines in the prevention of these lesions. What's new? Human papillomavirus (HPV) is linked to anal cancer through high HPV DNA-detection rates. Here, in one of the largest international studies to date, HPV DNA was detected in more than 88% of anal cancers and more than 95% of anal intraepithelial neoplasias grades 2/3. HPV16 was the most frequently detected virus type, followed by HPV18. Overexpression of p16INK4a, a surrogate marker for HPV-associated transformation, was found in 95% of HPV-positive anal cancers. The data implicate HPV as a causative factor in anal cancer.

Original languageEnglish
Pages (from-to)98-107
Number of pages10
JournalInternational Journal of Cancer
Volume136
Issue number1
DOIs
Publication statusPublished - 1 Jan 2015

Fingerprint

Anus Neoplasms
Carcinoma
DNA
Neoplasms
Biomarkers
Confidence Intervals
Papillomavirus Vaccines
Papillomavirus Infections
Paraffin
Formaldehyde
Squamous Cell Carcinoma

Keywords

  • anal cancer
  • human papillomavirus
  • vaccine

Cite this

Alemany, L., Saunier, M., Alvarado-Cabrero, I., Quirõs, B., Salmeron, J., Shin, H. R., ... De Sanjosé, S. (2015). Human papillomavirus DNA prevalence and type distribution in anal carcinomas worldwide. International Journal of Cancer, 136(1), 98-107. https://doi.org/10.1002/ijc.28963
Alemany, Laia ; Saunier, Maëlle ; Alvarado-Cabrero, Isabel ; Quirõs, Beatriz ; Salmeron, Jorge ; Shin, Hai Rim ; Pirog, Edyta C. ; Guimerà, Núria ; Hernandez-Suarez, Gustavo ; Felix, Ana ; Clavero, Omar ; Lloveras, Belen ; Kasamatsu, Elena ; Goodman, Marc T. ; Hernandez, Brenda Y. ; Laco, Jan ; Tinoco, Leopoldo ; Geraets, Daan T. ; Lynch, Charles F. ; Mandys, Vaclav ; Poljak, Mario ; Jach, Robert ; Verge, Josep ; Clavel, Christine ; Ndiaye, Cathy ; Klaustermeier, Joellen ; Cubilla, Antonio ; Castellsagué, Xavier ; Bravo, Ignacio G. ; Pawlita, Michael ; Quint, William G. ; Muñoz, Nubia ; Bosch, Francesc X. ; De Sanjosé, Silvia. / Human papillomavirus DNA prevalence and type distribution in anal carcinomas worldwide. In: International Journal of Cancer. 2015 ; Vol. 136, No. 1. pp. 98-107.
@article{1e34919263b14d31a42f6adab52993ca,
title = "Human papillomavirus DNA prevalence and type distribution in anal carcinomas worldwide",
abstract = "Knowledge about human papillomaviruses (HPV) types involved in anal cancers in some world regions is scanty. Here, we describe the HPV DNA prevalence and type distribution in a series of invasive anal cancers and anal intraepithelial neoplasias (AIN) grades 2/3 from 24 countries. We analyzed 43 AIN 2/3 cases and 496 anal cancers diagnosed from 1986 to 2011. After histopathological evaluation of formalin-fixed paraffin-embedded samples, HPV DNA detection and genotyping was performed using SPF-10/DEIA/LiPA25 system (version 1). A subset of 116 cancers was further tested for p16INK4a expression, a cellular surrogate marker for HPV-associated transformation. Prevalence ratios were estimated using multivariate Poisson regression with robust variance in the anal cancer data set. HPV DNA was detected in 88.3{\%} of anal cancers (95{\%} confidence interval [CI]: 85.1-91.0{\%}) and in 95.3{\%} of AIN 2/3 (95{\%} CI: 84.2-99.4{\%}). Among cancers, the highest prevalence was observed in warty-basaloid subtype of squamous cell carcinomas, in younger patients and in North American geographical region. There were no statistically significant differences in prevalence by gender. HPV16 was the most frequent HPV type detected in both cancers (80.7{\%}) and AIN 2/3 lesions (75.4{\%}). HPV18 was the second most common type in invasive cancers (3.6{\%}). p16INK4a overexpression was found in 95{\%} of HPV DNA-positive anal cancers. In view of the results of HPV DNA and high proportion of p16INK4a overexpression, infection by HPV is most likely to be a necessary cause for anal cancers in both men and women. The large contribution of HPV16 reinforces the potential impact of HPV vaccines in the prevention of these lesions. What's new? Human papillomavirus (HPV) is linked to anal cancer through high HPV DNA-detection rates. Here, in one of the largest international studies to date, HPV DNA was detected in more than 88{\%} of anal cancers and more than 95{\%} of anal intraepithelial neoplasias grades 2/3. HPV16 was the most frequently detected virus type, followed by HPV18. Overexpression of p16INK4a, a surrogate marker for HPV-associated transformation, was found in 95{\%} of HPV-positive anal cancers. The data implicate HPV as a causative factor in anal cancer.",
keywords = "anal cancer, human papillomavirus, vaccine",
author = "Laia Alemany and Ma{\"e}lle Saunier and Isabel Alvarado-Cabrero and Beatriz Quir{\~o}s and Jorge Salmeron and Shin, {Hai Rim} and Pirog, {Edyta C.} and N{\'u}ria Guimer{\`a} and Gustavo Hernandez-Suarez and Ana Felix and Omar Clavero and Belen Lloveras and Elena Kasamatsu and Goodman, {Marc T.} and Hernandez, {Brenda Y.} and Jan Laco and Leopoldo Tinoco and Geraets, {Daan T.} and Lynch, {Charles F.} and Vaclav Mandys and Mario Poljak and Robert Jach and Josep Verge and Christine Clavel and Cathy Ndiaye and Joellen Klaustermeier and Antonio Cubilla and Xavier Castellsagu{\'e} and Bravo, {Ignacio G.} and Michael Pawlita and Quint, {William G.} and Nubia Mu{\~n}oz and Bosch, {Francesc X.} and {De Sanjos{\'e}}, Silvia",
year = "2015",
month = "1",
day = "1",
doi = "10.1002/ijc.28963",
language = "English",
volume = "136",
pages = "98--107",
journal = "International Journal of Cancer",
issn = "0020-7136",
publisher = "John Wiley & Sons, Ltd",
number = "1",

}

Alemany, L, Saunier, M, Alvarado-Cabrero, I, Quirõs, B, Salmeron, J, Shin, HR, Pirog, EC, Guimerà, N, Hernandez-Suarez, G, Felix, A, Clavero, O, Lloveras, B, Kasamatsu, E, Goodman, MT, Hernandez, BY, Laco, J, Tinoco, L, Geraets, DT, Lynch, CF, Mandys, V, Poljak, M, Jach, R, Verge, J, Clavel, C, Ndiaye, C, Klaustermeier, J, Cubilla, A, Castellsagué, X, Bravo, IG, Pawlita, M, Quint, WG, Muñoz, N, Bosch, FX & De Sanjosé, S 2015, 'Human papillomavirus DNA prevalence and type distribution in anal carcinomas worldwide', International Journal of Cancer, vol. 136, no. 1, pp. 98-107. https://doi.org/10.1002/ijc.28963

Human papillomavirus DNA prevalence and type distribution in anal carcinomas worldwide. / Alemany, Laia; Saunier, Maëlle; Alvarado-Cabrero, Isabel; Quirõs, Beatriz; Salmeron, Jorge; Shin, Hai Rim; Pirog, Edyta C.; Guimerà, Núria; Hernandez-Suarez, Gustavo; Felix, Ana; Clavero, Omar; Lloveras, Belen; Kasamatsu, Elena; Goodman, Marc T.; Hernandez, Brenda Y.; Laco, Jan; Tinoco, Leopoldo; Geraets, Daan T.; Lynch, Charles F.; Mandys, Vaclav; Poljak, Mario; Jach, Robert; Verge, Josep; Clavel, Christine; Ndiaye, Cathy; Klaustermeier, Joellen; Cubilla, Antonio; Castellsagué, Xavier; Bravo, Ignacio G.; Pawlita, Michael; Quint, William G.; Muñoz, Nubia; Bosch, Francesc X.; De Sanjosé, Silvia.

In: International Journal of Cancer, Vol. 136, No. 1, 01.01.2015, p. 98-107.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Human papillomavirus DNA prevalence and type distribution in anal carcinomas worldwide

AU - Alemany, Laia

AU - Saunier, Maëlle

AU - Alvarado-Cabrero, Isabel

AU - Quirõs, Beatriz

AU - Salmeron, Jorge

AU - Shin, Hai Rim

AU - Pirog, Edyta C.

AU - Guimerà, Núria

AU - Hernandez-Suarez, Gustavo

AU - Felix, Ana

AU - Clavero, Omar

AU - Lloveras, Belen

AU - Kasamatsu, Elena

AU - Goodman, Marc T.

AU - Hernandez, Brenda Y.

AU - Laco, Jan

AU - Tinoco, Leopoldo

AU - Geraets, Daan T.

AU - Lynch, Charles F.

AU - Mandys, Vaclav

AU - Poljak, Mario

AU - Jach, Robert

AU - Verge, Josep

AU - Clavel, Christine

AU - Ndiaye, Cathy

AU - Klaustermeier, Joellen

AU - Cubilla, Antonio

AU - Castellsagué, Xavier

AU - Bravo, Ignacio G.

AU - Pawlita, Michael

AU - Quint, William G.

AU - Muñoz, Nubia

AU - Bosch, Francesc X.

AU - De Sanjosé, Silvia

PY - 2015/1/1

Y1 - 2015/1/1

N2 - Knowledge about human papillomaviruses (HPV) types involved in anal cancers in some world regions is scanty. Here, we describe the HPV DNA prevalence and type distribution in a series of invasive anal cancers and anal intraepithelial neoplasias (AIN) grades 2/3 from 24 countries. We analyzed 43 AIN 2/3 cases and 496 anal cancers diagnosed from 1986 to 2011. After histopathological evaluation of formalin-fixed paraffin-embedded samples, HPV DNA detection and genotyping was performed using SPF-10/DEIA/LiPA25 system (version 1). A subset of 116 cancers was further tested for p16INK4a expression, a cellular surrogate marker for HPV-associated transformation. Prevalence ratios were estimated using multivariate Poisson regression with robust variance in the anal cancer data set. HPV DNA was detected in 88.3% of anal cancers (95% confidence interval [CI]: 85.1-91.0%) and in 95.3% of AIN 2/3 (95% CI: 84.2-99.4%). Among cancers, the highest prevalence was observed in warty-basaloid subtype of squamous cell carcinomas, in younger patients and in North American geographical region. There were no statistically significant differences in prevalence by gender. HPV16 was the most frequent HPV type detected in both cancers (80.7%) and AIN 2/3 lesions (75.4%). HPV18 was the second most common type in invasive cancers (3.6%). p16INK4a overexpression was found in 95% of HPV DNA-positive anal cancers. In view of the results of HPV DNA and high proportion of p16INK4a overexpression, infection by HPV is most likely to be a necessary cause for anal cancers in both men and women. The large contribution of HPV16 reinforces the potential impact of HPV vaccines in the prevention of these lesions. What's new? Human papillomavirus (HPV) is linked to anal cancer through high HPV DNA-detection rates. Here, in one of the largest international studies to date, HPV DNA was detected in more than 88% of anal cancers and more than 95% of anal intraepithelial neoplasias grades 2/3. HPV16 was the most frequently detected virus type, followed by HPV18. Overexpression of p16INK4a, a surrogate marker for HPV-associated transformation, was found in 95% of HPV-positive anal cancers. The data implicate HPV as a causative factor in anal cancer.

AB - Knowledge about human papillomaviruses (HPV) types involved in anal cancers in some world regions is scanty. Here, we describe the HPV DNA prevalence and type distribution in a series of invasive anal cancers and anal intraepithelial neoplasias (AIN) grades 2/3 from 24 countries. We analyzed 43 AIN 2/3 cases and 496 anal cancers diagnosed from 1986 to 2011. After histopathological evaluation of formalin-fixed paraffin-embedded samples, HPV DNA detection and genotyping was performed using SPF-10/DEIA/LiPA25 system (version 1). A subset of 116 cancers was further tested for p16INK4a expression, a cellular surrogate marker for HPV-associated transformation. Prevalence ratios were estimated using multivariate Poisson regression with robust variance in the anal cancer data set. HPV DNA was detected in 88.3% of anal cancers (95% confidence interval [CI]: 85.1-91.0%) and in 95.3% of AIN 2/3 (95% CI: 84.2-99.4%). Among cancers, the highest prevalence was observed in warty-basaloid subtype of squamous cell carcinomas, in younger patients and in North American geographical region. There were no statistically significant differences in prevalence by gender. HPV16 was the most frequent HPV type detected in both cancers (80.7%) and AIN 2/3 lesions (75.4%). HPV18 was the second most common type in invasive cancers (3.6%). p16INK4a overexpression was found in 95% of HPV DNA-positive anal cancers. In view of the results of HPV DNA and high proportion of p16INK4a overexpression, infection by HPV is most likely to be a necessary cause for anal cancers in both men and women. The large contribution of HPV16 reinforces the potential impact of HPV vaccines in the prevention of these lesions. What's new? Human papillomavirus (HPV) is linked to anal cancer through high HPV DNA-detection rates. Here, in one of the largest international studies to date, HPV DNA was detected in more than 88% of anal cancers and more than 95% of anal intraepithelial neoplasias grades 2/3. HPV16 was the most frequently detected virus type, followed by HPV18. Overexpression of p16INK4a, a surrogate marker for HPV-associated transformation, was found in 95% of HPV-positive anal cancers. The data implicate HPV as a causative factor in anal cancer.

KW - anal cancer

KW - human papillomavirus

KW - vaccine

UR - http://www.scopus.com/inward/record.url?scp=84928750547&partnerID=8YFLogxK

U2 - 10.1002/ijc.28963

DO - 10.1002/ijc.28963

M3 - Article

VL - 136

SP - 98

EP - 107

JO - International Journal of Cancer

JF - International Journal of Cancer

SN - 0020-7136

IS - 1

ER -

Alemany L, Saunier M, Alvarado-Cabrero I, Quirõs B, Salmeron J, Shin HR et al. Human papillomavirus DNA prevalence and type distribution in anal carcinomas worldwide. International Journal of Cancer. 2015 Jan 1;136(1):98-107. https://doi.org/10.1002/ijc.28963