Hepatitis Viruses, Alcohol, and Tobacco in the Etiology
of Hepatocellular Carcinoma in Italy
Silvia Franceschi,
1
Maurizio Montella,
3
Jerry Polesel,
5
Carlo La Vecchia,
6,7
Anna Crispo,
3
Luigino Dal Maso,
5
Pietro Casarin,
8
Francesco Izzo,
4
Luigi G. Tommasi,
5
Isabelle Chemin,
2
Christian Tre ´po,
2
Marina Crovatto,
9
and Renato Talamini
5
1
International Agency for Research on Cancer;
2
Institut National de la Sante et de la Recherche Medicale Unite ´ 271, Lyons, France;
3
Servizio di Epidemiologia, Istituto Tumori ‘‘Fondazione Pascale,’’ Cappella dei Cangiani;
4
Divisione di Chirurgia D, Istituto
Tumori ‘‘Fondazione Pascale,’’ Cappella dei Cangiani, Naples, Italy;
5
Unita ` di Epidemiologia e Biostatistica, Centro di
Riferimento Oncologico, Istituto Nazionale Tumori, Aviano, Italy;
6
Istituto di Ricerche Farmacologiche ‘‘Mario Negri’’;
7
Istituto di Statistica Medica e Biometria, Universita ` degli Studi di Milano, Milan, Italy;
8
Divisione di Medicina 3,
Ospedale ‘‘S. Maria degli Angeli’’; and
9
Divisione di Microbiologia e Immunologia,
Ospedale ‘‘S. Maria degli Angeli,’’ Pordenone, Italy
Abstract
Mortality rates of hepatocellular carcinoma (HCC) are high
in Italy compared with other Western countries. To elucidate
further the role of hepatitis B virus (HBV), hepatitis C virus
(HCV), alcohol drinking, and tobacco smoking in the
etiology of HCC, we carried out a hospital-based case-control
study in two areas of Italy: the province of Pordenone in the
Northeast and the town of Naples in the South. A total of 229
HCC cases (median age, 66 years) and 431 controls (median
age, 65 years) answered a questionnaire and provided blood
samples between 1999 and 2002. Odds ratios (OR), percent
attributable risks, and corresponding 95% confidence inter-
vals were computed using unconditional multiple logistic
regression. ORs for hepatitis B surface antigen (HBsAg)
positive versus HBsAg negative and for anti-HCV antibody
positive versus anti-HCV antibody negative were 20.2 and
15.6, respectively. Positivity for both markers was associated
with an OR of 51.6. Sensitive molecular techniques applied
to sera in a subset of HCC cases disclosed a very small
number of occult hepatites. Maximal lifetime alcohol intake
of z35 versus <7 drinks/wk was associated with an HBV/
HCV adjusted OR of 5.9. Tobacco smoking was unrelated to
HCC risk overall but seemed to enhance HCC risk among
virus carriers. Overall, 61% of HCC were attributable to
HCV, 13% to HBV, and 18% to heavy alcohol drinking. In
conclusion, our study confirms the importance of HCV in
HCC etiology in Italy where the widespread dissemination
of the virus dates back four or five decades. (Cancer
Epidemiol Biomarkers Prev 2006;15(4):683–9)
Introduction
Upward trends in incidence or mortality of hepatocellular
carcinoma (HCC) have been reported in the United States (1),
Japan (2), and in several European countries, including Italy (3),
over the last two or three decades. These increases have been
chieflyattributedtothespreadofhepatitisCvirus(HCV;ref.1),
whichoccurredearlierinJapanandSouthernEuropethaninthe
United States (3, 4) and has been mainly sustained by i.v. drug
use and the use of contaminated needles in medical procedures
(5). Although the role of heavy alcohol drinking has long been
recognized (6-9), the contribution of cigarette smoking to HCC
has been established only recently (10, 11).
To elucidate further the interplay of viruses and lifestyle, we
have conducted a case-control study of HCC in two areas of
Italy, characterized by different levels of alcohol consumption
(12) and HCV prevalence (13, 14). Sensitive molecular techni-
ques for viral genomes were added to serologic assays to obtain
a more accurate figure of the proportion of HCC attributable to
hepatitis B virus (HBV) or HCV.
Materials and Methods
Between January 1999 and July 2002, we conducted a case-
control study on the association of HBV and HCV with HCC in
theprovinceofPordenoneintheNortheastofItalyandthetown
ofNaplesintheSouth.Theoriginalstudyincludedanothercase
group (lymphohematopoietic neoplasms) whose relationship
with HBV and HCV has already been reported (15, 16).
Cases. Cases in the present report included patients <85
years of age with incident HCC, who had not yet received any
cancer treatment at study entry. They were admitted to the
National Cancer Institute in Aviano, the ‘‘Santa Maria degli
Angeli’’ General Hospital in Pordenone, and the ‘‘Pascale’’
National Cancer Institute, plus four General Hospitals in
Naples (i.e., the hospitals to which the majority of HCC
patients from the two study areas were referred). A total of 261
HCC cases were identified. Three cases refused to participate
in the study and 29 HCC cases were interviewed but could not
give a blood sample, thus leaving 229 cases (median age, 66
years; range, 43-84 years) for whom both questionnaire and
blood sample were available. Histologic or cytologic confir-
mation was available from the majority (78.2%) of HCC cases
whereas diagnosis was based on ultrasound, tomography, and
elevated a-fetoprotein levels in the remaining HCC cases.
According to the Child-Pugh classification, 59.0% of HCC
cases were classified as class A, 31.7% as class B, and 18.4% as
class C. All medical and histocytologic records were reviewed
by two authors (F.I. and L.G.T.).
Controls. The comparison group included patients <85
years of age admitted to the same hospitals where HCC cases
had been interviewed for a wide spectrum of acute conditions.
Patients whose hospital admission was due to diseases related
to alcohol and tobacco use (e.g., respiratory diseases, peptic
ulcer, lung cancer, head and neck cancer, etc.) or hepatitis
viruses (e.g., hepatitis, cirrhosis, esophageal varices, etc.) were
specifically excluded from the control group, as were those
683
Cancer Epidemiol Biomarkers Prev 2006;15(4). April 2006
Received 9/7/05; revised 1/11/06; accepted 1/30/06.
Grant support: Associazione Italiana per la Ricerca sul Cancro, Lega Italiana per la Lotta
contro i Tumori, and Compagnia San Paolo grant 11582/23719.
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.
Requests for reprints: Silvia Franceschi, IARC, 150 cours Albert Thomas, 69372 Lyon cedex 08,
France. Phone: 33-4-72-73-84-02; Fax: 33-4-72-73-83-45. E-mail: franceschi@iarc.fr
Copyright D 2006 American Association for Cancer Research.
doi:10.1158/1055-9965.EPI-05-0702
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