Article
Gastric cancer and Helicobacter
pylori: a combined analysis of 12 case control studies nested
within prospective cohorts
Helicobacter and Cancer Collaborative Group
Correspondence to: Professor D Forman, Epidemiology and Health Services Research, The Medical School, University of Leeds, Arthington House, Cookridge Hospital, Leeds LS16 6QB, UK. d.forman{at}leeds.ac.uk
Accepted for publication 26 February 2001
BACKGROUND
The
magnitude of the association between Helicobacter
pylori and incidence of gastric cancer is unclear.
H pylori infection and the circulating
antibody response can be lost with development of cancer; thus
retrospective studies are subject to bias resulting from classification
of cases as H pylori negative when they were infected in the past.
AIMS
To combine data
from all case control studies nested within prospective cohorts to
assess more reliably the relative risk of gastric cancer associated
with H pylori infection. To investigate variation in relative risk by age, sex, cancer type and subsite, and
interval between blood sampling and cancer diagnosis.
METHODS
Studies were
eligible if blood samples for H pylori
serology were collected before diagnosis of gastric cancer in cases.
Identified published studies and two unpublished studies were included.
Individual subject data were obtained for each. Matched odds ratios
(ORs) and 95% confidence intervals (95% CI) were calculated for the association between H pylori and gastric cancer.
RESULTS
Twelve studies
with 1228 gastric cancer cases were considered. The association with
H pylori was restricted to non-cardia cancers (OR 3.0; 95% CI 2.3-3.8) and was stronger when blood samples for H pylori serology were collected 10+
years before cancer diagnosis (5.9; 3.4-10.3). H
pylori infection was not associated with an altered overall risk
of cardia cancer (1.0; 0.7-1.4).
CONCLUSIONS
These
results suggest that 5.9 is the best estimate of the relative risk of
non-cardia cancer associated with H pylori
infection and that H pylori does not
increase the risk of cardia cancer. They also support the idea that
when H pylori status is assessed close to
cancer diagnosis, the magnitude of the non-cardia association may be underestimated.
Keywords: gastric cancer; Helicobacter pylori; cardia cancer; pooled analysis
© 2001 by Gut
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