Short Communication
Increased Risk for Cervical Disease Progression of French
Women Infected with the Human Papillomavirus
Type 16 E6-350G Variant
Martha Grodzki,
1
Guillaume Besson,
2
Christine Clavel,
2
Annie Arslan,
3
Silvia Franceschi,
3
Philippe Birembaut,
2
Massimo Tommasino,
3
and Ingeborg Zehbe
4
1
Johannes Gutenberg University, Medical Microbiology, Mainz, Germany;
2
Laboratoire Pol Bouin, Hopital Maison Blanche, CHU, Reims,
France;
3
IARC, Lyon, France; and
4
Thunder Bay Regional Health Sciences Centre, Regional Cancer Care, Thunder Bay, Ontario, Canada
Abstract
To test the significance of human papillomavirus (HPV)
type 16 and HPV16 E6 variants as risk factors for viral
persistence and progression to high-grade lesion, we did a
nested case-control study within a cohort study of >15,000
Caucasian French women. Three groups infected with high-
risk HPV were compared: (a ) women with cleared infection
(controls, n = 201), (b ) women with persistent infection
(cases, n = 87), and (c ) women who progressed into high-
grade lesion (cases, n = 58). Women with persistent HPV
infection and those that progressed into high-grade lesions
were likelier to harbor HPV16 than other high-risk HPV
types [odds ratio (OR), 2.4; 95% confidence interval (95% CI),
1.3-4.3 and OR, 4.2; 95% CI, 2.2-8.1, respectively]. Notably,
especially elevated ORs of persistence (3.0; 95% CI, 1.4-6.7)
and progression (6.2; 95% CI, 2.7-14.3) were found among
women who harbored the HPV16 350G variant. Thus, HPV
type and HPV16 variant seem to be risk factors for viral
persistence and progression of infections into high-grade
cervical lesions. (Cancer Epidemiol Biomarkers Prev 2006;
15(4):820–2)
A subgroup of human papillomaviruses (HPV), referred to as
high-risk types, are the etiologic agents of cervical cancer (1).
Among the high-risk types HPV16 is the most prevalent type
in premalignant and malignant cervical lesions worldwide
(2, 3). Persistence of viral infection has a key role in cervical
cancer development (4, 5). HPV16 is likelier to persist (6) and
to cause progression into cervical intraepithelial neoplasia
(CIN) than other high-risk HPV types (7, 8). Nucleic acid
sequencing of HPV16 genomes has revealed the existence of
numerous natural variants that differ from the original
European prototype sequence (9) up to 2% in the coding
region and/or up to 5% in the noncoding region (10). HPV16
variants have been classified as five major phylogenetic
clusters (or lineages): European, Asian, Asian American,
African, and North American. For each lineage, several
subclasses have been identified (summarized in ref. 11).
Interestingly, three codon sites in the HPV16 E6 open reading
frame coding for amino acids 10, 14, and 83 were shown to be
under selective pressure (12). Variants at these residues lead
to changes from arginine to glycine or isoleucine (R10G or
R10I) at codon 10, from glutamine to histidine or aspartic acid
(Q14H or Q14D) at codon 14, and from leucine to valine
(L83V) at codon 83. Recent studies suggest that HPV16 E6
variants are involved in determining persistence of the viral
infection and the development of cervical lesions (13-20).
Some of these have shown that non-European HPV16
variants are more associated with disease progression than
the European variants (21, 22).
By using cross-sectional analyses of several European
populations, we have previously shown that within the
European lineage, the L83V E6 variant harboring a nucleotide
substitution at position 350 (HPV16 350G) alone or in
combination with other polymorphisms is more prevalent in
cervical cancer than in CIN (23-25). This phenomenon may be
explained by the fact that natural variants alter the
immunogenic and/or carcinogenic properties of the virus.
In this study, we have used a large French cohort to elucidate
further whether HPV16 and HPV16-specific variants are
predictors for persistence of infection and progression into
high-grade lesion.
We did a nested case-control study within a large cohort
study of >15,000 Caucasian French women ages between 18
and 76 years (median = 34 years). They had been recruited
between 1997 and 2003 among women who underwent their
biennial or triennial routine screening in the Department of
Obstetrics and Gynaecology at the CHU in Reims, France
(26). The follow-up ranged between 12 to 72 months (median =
34 months; ref. 26). All women were informed of the aim of
the program and gave their written consent. This study was
approved by the local ethical committee. All cohort women
were tested for the presence of the high-risk HPV types by
the Hybrid Capture II assay (Digene, Gaithersburg, MD), and
only women who were positive for high-risk HPV types
and did not have high-grade lesions at baseline were eligible
for the present study. Women were excluded if they had
a cytologic abnormality and/or an untreated cervical lesion
in the past 2 years, were pregnant, or had an HIV/AIDS
diagnosis.
To identify the high-risk type involved, HPV16 was
tested by PCR using E6 specific primers, whereas other
high-risk HPV types were tested by the Linear Blot Array
820
Cancer Epidemiol Biomarkers Prev 2006;15(4). April 2006
Received 11/8/05; revised 1/6/06; accepted 2/2/06.
Grant support: Deutsche Krebshilfe, Bonn, Germany grant 70-3050-Ze (I. Zehbe); La Ligue
Contre le Cancer (M. Tommasino); and Comite ´ du Rho ˆne et Comite ´ de la Dro ˆme, France (M.
Tommasino).
The costs of publication of this article were defrayed in part by the payment of page charges.
This article must therefore be hereby marked advertisement in accordance with 18 U.S.C.
Section 1734 solely to indicate this fact.
Note: This work has been done in fulfillment of the requirements for the M.D. thesis of M.
Grodzki.
M. Grodzki and G. Birembaut contributed equally to this work.
Requests for reprints: Ingeborg Zehbe, Thunder Bay Regional Health Sciences Centre,
Regional Cancer Care Programme, 980 Oliver Road, Thunder Bay, Ontario P7B 6V4, Canada.
Phone: 807-684-7256; Fax: 807-684-5806. E-mail: zehbei@tbh.net
Copyright D 2006 American Association for Cancer Research.
doi:10.1158/1055-9965.EPI-05-0864
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