British Journal of Cancer (2001) 85(11), 1700–1705
© 2001 Cancer Research Campaign
doi: 10.1054/ bjoc.2001.2140, available online at http://www.idealibrary.com on
http://www.bjcancer.com
A meta-analysis of alcohol drinking and cancer risk
V Bagnardi1, M Blangiardo1, C La Vecchia2,3 and G Corrao1
1
Dipartimento di Statistica, Università di Milano-Bicocca, via Bicocca degli Arcimboldi 8, 20126 Milano, Italy; 2Istituto di Statistica Medica e Biometria, Università
degli Studi di Milano, via Venezian 1, 20133 Milano, Italy; 3Istituto di Ricerche Farmacologiche “Mario Negri”, via Eritrea 62, 20157 Milano, Italy
Summary To evaluate the strength of the evidence provided by the epidemiological literature on the association between alcohol consumption
and the risk of 18 neoplasms, we performed a search of the epidemiological literature from 1966 to 2000 using several bibliographic databases.
Meta-regression models were fitted considering linear and non-linear effects of alcohol intake. The effects of characteristics of the studies,
of selected covariates (tobacco) and of the gender of individuals included in the studies, were also investigated as putative sources of
heterogeneity of the estimates. A total of 235 studies including over 117 000 cases were considered. Strong trends in risk were observed for
cancers of the oral cavity and pharynx, oesophagus and larynx. Less strong direct relations were observed for cancers of the stomach, colon
and rectum, liver, breast and ovary. For all these diseases, significant increased risks were found also for ethanol intake of 25 g per day. No
significant nor consistent relation was observed for cancers of the pancreas, lung, prostate or bladder. Allowance for tobacco appreciably
modified the relations with laryngeal, lung and bladder cancers, but not those with oral, oesophageal or colorectal cancers. This meta-analysis
showed no evidence of a threshold effect for most alcohol-related neoplasms. The inference is limited by absence of distinction between
lifelong abstainers and former drinkers in several studies, and the possible selective inclusion of relevant sites only in cohort studies. © 2001
Cancer Research Campaign http://www.bjcancer.com
Keywords: alcohol intake; neoplasms, humans; meta-analysis; risk
Although alcohol is not known to be carcinogenic in animal experimentation, there is strong epidemiological evidence that alcoholic
beverages increase the risk of cancers of the oral cavity and
pharynx, oesophagus and larynx. The risks are essentially due to
total ethanol intake, and tend to increase with the amount of
ethanol drunk, but it is still unclear whether there is any threshold
below which no effect is evident (IARC, 1988; Doll et al, 1999).
Alcohol drinking has been associated with primary liver cancer,
although this relation is difficult to investigate in epidemiological
studies, since most alcohol-related liver cancers follow a cirrhosis,
which leads to a reduction of alcohol drinking (Aricò et al, 1994;
La Vecchia et al, 1998).
Alcohol drinking has also been linked to cancers of the large
bowel in both sexes and of the female breast. Although these associations are still open to discussion, these are the 2 most common
neoplasms in developed countries after lung cancer, and therefore
even a moderate excess risk may have important public health
implications. The association between alcohol drinking and
several other neoplasms, including ovary, endometrium and
bladder, is still controversial (IARC, 1988; Doll et al, 1999).
To evaluate the effect of alcohol on cancer risk, a more accurate quantification of its effects on various neoplasms is required.
With this major focus, we therefore updated in the present paper
a comprehensive meta-analysis of published case–control and
cohort studies investigating the possible relation between alcohol
Received 23 July 2001
Revised 7 September 2001
Accepted 14 September 2001
Correspondence to: C La Vecchia
1700
intake and the risk of several neoplasm (Corrao et al, 1999). We
also addressed the issue of the potential modifying effect of
tobacco on alcohol-related cancerogenesis at various cancer
sites.
METHODS
The statistical methods used for this meta-analysis are described in
detail elsewhere (Corrao et al, 1999, 2000). Articles included were
found through a search of the literature published from 1966 to
2000. The search was based on several bibliographic data-bases
(MEDLINE, Current Contents, EMBASE, CAB Abstracts and
Core Biomedical Collection), supplemented by checking all references in the selected articles. Completeness was verified by a
hand-search on the most relevant journals of epidemiology and
medicine, and by comparing our search with that of general
reviews and meta-analyses published on this issue (IARC, 1988;
Longnecker et al, 1990; Longnecker, 1994, 1995; Longnecker and
Enger, 1996; Corrao et al, 1999; Doll et al, 1999; Zeegers et al,
1999; Dennis, 2000).
Each publication identified by this process was reviewed and
included in the analysis if the following criteria were met:
(i) case–control or cohort study published as an original article;
(ii) findings expressed as odds ratio or relative risk (RR), considering at least 3 levels of alcohol consumption; (iii) papers
reporting the number of cases and non-cases, and the estimates of
the odds ratios or RR for each exposure level. Multivariate RRs
were used for the main analysis purpose. When the results of a
study were published more than once, only the most complete data
were included in the analysis.
2 readers, blinded to the authors’ names and affiliations and to
the results pertaining to alcohol consumption, independently
Alcohol and cancer
determined the eligibility of each paper. Pooled estimates of the
effect of alcohol consumption on the risk of each neoplasm
investigated were based on several meta-regression models
(Greenland and Longnecker, 1992). Briefly, the data analysis
strategy first involved pooling the original data for each
neoplasm; subsequently the relationship between alcohol
consumption and risk was modelled by fitting several fractional
models (Royston et al, 1999) in order to identify J- or U-shaped
curves, or other relations between alcohol exposure level and
relative risks. In the current application, a family of second-order
models was generated by power transformation of exposure variable, and the best-fitting model was chosen to summarise the relation of interest. The effects of gender and of the adjustment of the
reported estimates for smoking in modifying the effect of alcohol
on the risk of each neoplasm were also investigated by comparing
pooled estimates based on RRs unadjusted for tobacco to the
adjusted ones used in the main analysis, whenever available
(Berlin et al, 1993). Heterogeneity among studies was evaluated
according to the method described by Greenland and Longnecker
(1992).
RESULTS
Altogether, 235 studies with a total of 117 471 cases, met the
inclusion criteria and were considered in the analysis. Of the
included studies, 187 were case–control and 48 cohort studies,
investigating the risk of 18 cancer sites, or of all cancers irrespective of site.
The main characteristics and results of the studies, based
on multivariate analysis, are given in Table 1. For 5 cancer
sites (melanoma and cancer of small intestine, gallbladder,
cervix uteri and kidney) the estimates were based on one or 2
studies only, and did not consider the effects of high alcohol
consumption.
Strong direct trends in risk were observed for cancers of the oral
cavity and pharynx (RR = 6.0 for 100 g day–1), oesophagus (RR =
4.2) and larynx (RR = 3.9). Direct relations – though appreciably
less strong – were also found for cancers of the stomach (RR =
1.32), colo-rectum (RR = 1.38) and liver (RR = 1.86), as well as
for breast (RR = 1.7 for 50 g day–1 and 2.7 for 100 g day–1) and
ovarian (RR = 1.53) neoplasms. Weaker trends were found for
lung (RR = 1.08) and prostate (RR = 1.19) cancers. For most
cancer sites, significant increased risks were found also for the
lowest dose of alcohol considered (25 g day–1, corresponding to
approximately 2 drinks per day). No significant relation emerged
between alcohol and pancreas, endometrium and bladder cancers.
Significant heterogeneity across studies was found. Effects of
gender in modifying the effect of alcohol intake were investigated
for each cancer site, but reached statistical significance only for
oesophageal and liver cancers, with higher risks in women for both
neoplasms. By pooling the 8 studies reporting the relation between
alcohol and the risk of all sites together, significant effects were
found starting from intakes of 28 g day–1.
To analyse the modifying effect of tobacco, pooled estimates
based on unadjusted and adjusted RRs were compared in Table 2
for studies providing relevant information. Effects of smoking
adjustment in modifying the effect of alcohol related risks were
investigated for 5 neoplasms known to be strongly tobaccorelated, but reached statistical significance only for cancers of
larynx, lung and bladder, with higher risks for unadjusted
© 2001 Cancer Research Campaign
1701
estimates. However, while for laryngeal cancer evidence of a
substantial alcohol-related risk persisted by pooling studies
reporting both unadjusted and adjusted estimates, alcohol did not
show significant effects on the risk of lung and bladder neoplasms
when its effect was adjusted for smoking. Allowance for tobacco
had a negligible effect on the estimates for colorectal cancer.
Figure 1 gives the relative risk functions for alcohol consumption,
and the corresponding 95% CI of selected neoplasms, by fitting
meta-regression models.
DISCUSSION
This work has some of the limitations, but also most of the
strengths of meta-analyses of published studies, including the
large number of subjects investigated and the comprehensive
picture provided. Its main results are consistent with published
meta analyses on alcohol and breast, colorectal (Longnecker et al,
1990; Longnecker, 1994, 1995), bladder (Zeegers et al, 1999) and
prostate (Dennis, 2000) cancers.
For most neoplasms considered, estimates tended to be heterogeneous across studies. Consequently, the overall pooled estimates
may be systematically influenced by characteristics of the subjects
included such as gender, due to the potential differences in alcohol
metabolism in women and men (Corrao et al, 1999, 2000). To
control for this, whenever possible we included gender term in the
meta-regression models. However, gender explained a significant
part of the observed heterogeneity only for cancers of oesophagus
and liver.
Another open issue is the definition of former drinkers, which in
some studies may include only a fraction of former drinkers.
However, the time-risk relations between alcohol drinking and
cancer risk are complex (Bosetti et al, 2000; Franceschi et al,
2001) and misclassification of former smokers should, if anything,
have led to an underestimate of the real association. Further,
several cohort studies may have selectively reported relevant findings for selected cancer sites only, and omitted data for less
common ones.
It is likely, moreover that alcohol drinking was systematically
under-reported in several studies, mostly for selected neoplasms.
Consequently, all the RRs would be biased towards lower levels
of drinking in case of non-selective under-reporting, or underestimated in the case of selective under-reporting by cases. Specific
perplexities concern the pooled estimates for liver cancer, due to
pre-existing cirrhosis and consequent reduced alcohol consumption (Aricò et al, 1994; La Vecchia et al, 1998). Further, although
this meta-analysis included a total of over 117 000 cases, absolute
numbers were relatively limited for some diseases (melanoma,
uterus and kidney cancers) or for certain levels of alcohol
drinking (high levels for breast cancer in women). Finally,
confounding might affect our pooled estimates. However, estimates in the main analysis for upper digestive and respiratory
tract cancers, as well as for lung and bladder neoplasms, were
adjusted for tobacco, which showed a substantial modifying
effect not only for lung and bladder, but also for laryngeal cancer.
The moderate excess risk for lung and bladder cancer, moreover,
may well be due to some residual confounding by tobacco. No
relevant modifying effect was observed for colorectal cancer,
which appears to be another tobacco-related neoplasm – though
less strongly than the above mentioned ones (D’Avanzo et al,
1995; Giovannucci, 2001).
British Journal of Cancer (2001) 85(11), 1700–1705
Main characteristics of the studies selected for the meta-analysis. Pooled relative risks, and corresponding 95% confidence interval, for selected doses of alcohol consumption are also reported
Number
Malignancy site
Studies
Study’s design
Cases
Cohort
Case–control
Pooled RR (and 95% CI) associated with alcohol intakea
25 g day–1
50 g day–1
100 g day–1
Gender
effect (P)b
Heterogeneity
test (P)c
Oral cavity and pharynx
26
7954
1
25
1.75 (1.70, 1.82)
2.85 (2.70, 3.04)
6.01 (5.46, 6.62)
n.s.
< 0.05
Oesophagus
Males
Females
28
18
5
7239
3310
304
1
1
0
27
17
5
1.51 (1.48, 1.55)
1.43 (1.38, 1.48)
1.52 (1.42, 1.63)
2.21 (2.11, 2.31)
1.98 (1.87, 2.11)
2.24 (1.95, 2.58)
4.23 (3.91, 4.59)
3.49 (3.14, 3.89)
4.45 (3.37, 5.87)
< 0.05
–
< 0.05
< 0.05
Stomach
16
4518
2
14
1.07 (1.04, 1.10)
1.15 (1.09, 1.22)
1.32 (1.18, 1.49)
n.s.
< 0.05
2
415
0
2
1.02 (0.89, 1.17)
1.04 (0.79, 1.37)
1.08 (0.63, 1.88)
n.s.
n.s.
Colon and rectum
22
11 296
6
16
1.08 (1.06, 1.10)
1.18 (1.14, 1.22)
1.38 (1.29, 1.49)
n.s.
< 0.05
Liver
Males
Females
20
10
3
2294
949
231
3
2
1
17
8
2
1.17 (1.11, 1.23)
1.28 (1.13, 1.45)
1.97 (1.30, 3.00)
1.36 (1.23, 1.51)
1.51 (1.27, 2.10)
3.57 (1.56, 8.21)
1.86 (1.53, 2.27)
1.62 (1.18, 2.24)
9.15 (1.73, 48.41)
< 0.05
–
< 0.05
< 0.05
Gallbladder
2
81
1
1
1.17 (0.73, 1.86)
1.36 (0.54, 3.44)
d
n.s.
n.s.
Pancreas
17
2524
4
13
0.98 (0.90, 1.05)
1.05 (0.93, 1.18)
1.18 (0.94, 1.49)
n.s.
< 0.05
Larynx
Small intestine
20
3759
0
20
1.38 (1.32, 1.45)
1.94 (1.78, 2.11)
3.95 (3.43, 4.57)
n.s.
< 0.05
Lung
6
2314
3
3
1.02 (1.00, 1.04)
1.04 (1.00, 1.08)
1.08 (1.00, 1.18)
n.s.
< 0.05
Melanoma
2
708
0
2
0.50 (0.21, 1.10)
d
d
n.s.
n.s.
49
44 033
12
37
1.31 (1.27, 1.36)
1.67 (1.56, 1.78)
2.71 (2.33, 3.08)
–
< 0.05
Breast
Cervix
1
242
–
1
0.80 (0.50, 1.27)
0.64 (0.25, 1.60)
–
–
0.53
Endometrium
6
2473
2
4
1.05 (0.88, 1.24)
1.09 (0.78, 1.54)
1.20 (0.60, 2.37)
–
< 0.01
5
1651
–
5
1.11 (1.00, 1.24)
1.23 (1.01, 1.54)
1.53 (1.03, 2.32)
–
n.s.
Prostate
Ovary
11
4094
4
7
1.05 (1.00, 1.08)
1.09 (1.02, 1.17)
1.19 (1.03, 1.37)
–
n.s.
© 2001 Cancer Research Campaign
Bladder
11
5997
2
9
1.04 (0.99, 1.09)
1.08 (0.98, 1.19)
1.17 (0.97, 1.41)
n.s.
n.s.
Kidney
2
921
0
2
0.88 (0.77, 1.02)
0.79 (0.60, 1.03)
0.62 (0.36, 1.06)
n.s.
n.s.
All sites together
8
14 495
6
2
1.01 (0.90, 1.05)
1.22 (1.11, 1.27)
1.91 (1.77, 2.06)
n.s.
< 0.05
235
117 471
48
187
–
–
–
–
Total
–
a
Pooled relative risk, and corresponding 95% confidence interval (CI), based on multivariate estimates, directly obtained from the β coefficients of the best fitting model, and from the corresponding standard error,
respectively (see Methods section); Evidence of a relative risk significantly different from 1 based on 95% CI that does not contain unity (P < 0.05). bEvidence of significant effect of gender in modifying the effect of
alcohol based on significance of the interaction term (P < 0.05). cSignificance (P < 0.05) indicates heterogeneity of the effects of alcohol among studies. dNo studies reported effect of alcohol at the specific dose.
1702 V Bagnardi et al
British Journal of Cancer (2001) 85(11), 1700–1705
Table 1
Alcohol and cancer
1703
A Neoplasms of the upper aerodigestive tract
RR
7
RR
7
Oral cavity and pharynx
RR
7
Oesophagus
6
6
6
5
5
5
4
4
4
3
3
3
2
2
2
1
1
1
0
0
Larynx
0
0 10 20 30 40 50 60 70 80 90 100
0 10 20 30 40 50 60 70 80 90 100
0 10 20 30 40 50 60 70 80 90 100
Alcohol (g day−1)
Alcohol (g day−1)
Alcohol (g day−1)
B Neoplasms of the lower digestive tract
Stomach
RR
3.0
RR
3.0
Colon and rectum
2.5
2.5
2.5
2.0
2.0
2.0
1.5
1.5
1.0
1.0
1.5
.........
......: ..............................:..:.:..::.--
1.0
0.5
0.5
Liver
RR
3.0
-·
-----~
~-----------·
0.5
0 10 20 30 40 50 60 70 80 90 100
0 10 20 30 40 50 60 70 80 90 100
0 10 20 30 40 50 60 70 80 90 100
Alcohol (g day−1)
Alcohol (g day−1)
Alcohol (g day−1)
C Other neoplasms
RR
3.0
Breast
RR
3.0
2.5
2.5
2.0
2.0
RR
3.0
Ovary
____
..............
...--··
2.5
.-· -·
2.0
1.5
1.5
1.5
1.0
1.0
1.0
0.5
0.5
Prostate
............. .............
.... : : : :::: ...... ---.............. ----........ ..
-:.
0.5
0 10 20 30 40 50 60 70 80 90 100
0 10 20 30 40 50 60 70 80 90 100
0 10 20 30 40 50 60 70 80 90 100
Alcohol (g day−1)
Alcohol (g day−1)
Alcohol (g day−1)
Figure 1 Relative risk functions, and corresponding 95% confidence intervals, describing the dose–response relationship between alcohol consumption and
the risk of the 9 neoplasms showing statistical evidence of alcohol effect
The results were generally inconsistent for cancer of the
pancreas, stomach and colorectum, and somewhat inconsistent
across studies, possibly following differences in their design.
There is also no clear understanding on the possible underlying
mechanisms through which alcohol may act as a co-carcinogen on
these sites (IARC, 1988; Doll et al, 1999). More importantly, the
pooled RR estimates were of the order of 1.1–1.3 for high level of
alcohol intake, and residual bias and confounding by diet or other
© 2001 Cancer Research Campaign
factors is plausible. Inference on a potential causal relationship
for these cancer sites is therefore not possible.
The present meta-analysis confirms the existence of a strong
dose–risk relation between alcohol and breast cancer risk
(Longnecker, 1994). For breast and other hormone-related
neoplasm (ovary, endometrium), a role of alcohol on female
hormone metabolism and serum levels is plausible (Longnecker,
1994; Dorgan et al, 2001).
British Journal of Cancer (2001) 85(11), 1700–1705
1704 V Bagnardi et al
Table 2
Effect of smoking adjustment in modifying the effect of alcohol on the risk of 5 tobacco-related neoplasms
Pooled RR (and 95% CI) associated with alcohol intakea
Malignancy site
25 g day –1
50 g day –1
100 g day –1
Oral cavity
Unadjusted estimates
Adjusted estimates
1.74 (1.67, 1.81)
1.76 (1.69, 1.82)
2.80 (2.59, 3.04)
2.87 (2.68, 3.08)
5.82 (5.00, 6.77)
6.10 (5.45, 6.83)
Oesophagus
Unadjusted estimates
Adjusted estimates
1.50 (1.47, 1.55)
1.52 (1.46, 1.57)
2.19 (2.08, 2.31)
2.23 (2.09, 2.38)
4.18 (3.79, 4.60)
4.31 (3.84, 4.85)
Larynx
Unadjusted estimates
Adjusted estimates
1.65 (1.55, 1.76)
1.29 (1.23, 1.36)
2.74 (2.43, 3.09)
1.68 (1.53, 1.84)
7.45 (6.04, 9.18)
2.79 (2.36, 3.30)
Lung
Unadjusted estimates
Adjusted estimates
1.58 (1.12, 2.24)
1.01 (0.99, 1.04)
2.50 (1.25, 5.01)
1.03 (0.99, 1.08)
6.30 (1.57, 25.18)
1.07 (0.98, 1.17)
Bladder
Unadjusted estimates
Adjusted estimates
1.16 (1.02, 1.33)
1.02 (0.97, 1.07)
1.36 (1.04, 1.77)
1.04 (0.94, 1.15)
1.85 (1.09, 3.13)
1.09 (0.89, 1.33)
Smoking
adjustment
effect (P)b
Heterogeneity
test (P)c
n.s.
< 0.05
n.s.
< 0.05
< 0.05
< 0.05
< 0.05
< 0.05
< 0.05
< 0.05
a
Pooled relative risk, and corresponding 95% confidence interval (CI), directly obtained from the β coefficients of the best fitting model, and from the
corresponding standard error, respectively (see Methods section); Evidence of a relative risk significantly different from 1 based on 95% CI that does
not contain unity (P < 0.05). bEvidence of significant effect of smoking adjustment in modifying the effect of alcohol based on significance of the
interaction term (P < 0.05). cSignificance (P < 0.05) indicates heterogeneity of the effects of alcohol among studies.
Alcohol and tobacco interact in a multiplicative way on the risk
of cancers of the upper digestive tract. From a public health viewpoint, such a synergism implies that over 75% of cancers of the
upper digestive and respiratory tract in developed countries are
attributable to alcohol and tobacco (Negri et al, 1992, 1993; Tavani
et al, 1996). While the evidence is inconsistent for laryngeal
cancer, the adjusted pooled estimates confirm that for oral and
pharyngeal (Talamini et al, 1998; Fioretti et al, 1999) and
oesophageal cancers (Doll et al, 1999) alcohol drinking has an
independent effect, and hence allowance for tobacco only marginally modified the RR.
Several attempts have been made to separate the effects of
different types of alcoholic beverages. Some authors reported no
apparent differences, while others have reported greater risks with
spirits than with wine or beer (Tuyns et al, 1979; Doll et al, 1999).
Whereas a study from Denmark showed no excess risk from wine
(Gronbaek et al, 1998), 2 studies from Italy (Barra et al, 1990;
Bosetti et al, 2000) found greater risks of oral and pharyngeal and
oesophageal cancer in wine drinkers, after adjustment for amount
drunk. It appears, therefore, that the most frequently consumed
beverage in each area tends to be the one with the highest association (Franceschi et al, 1990). For this reason, we have considered
only total alcohol consumption in the present overview.
Notwithstanding the limitations discussed above, this metaanalysis still includes most published information on alcohol and
cancer, and consequently – in the absence of a collaborative reanalysis of original data with separation of abstainers and exdrinkers, and the inclusion of data for the whole range of cancers
in cohort studies – provides the most accurate relative risk estimates for most common neoplasms that is available. Some of the
findings from this meta-analysis are innovative and of specific
relevance, including the absence of a threshold effect for any of
major alcohol-related cancer sites, and the apparently stronger
association for oral and pharyngeal cancer than for any other site
across different levels of alcohol drinking.
British Journal of Cancer (2001) 85(11), 1700–1705
ACKNOWLEDGEMENTS
Supports for this study came from the Italian Ministry of Health,
from the Italian Ministry of the University and Scientific and
Technologic Research, and the Associazione Italiana per la
Ricerca sul Cancro. Ms Ivana Garimoldi provided editorial
assistance.
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