NATURE REVIEWS | GASTROENTEROLOGY & HEPATOLOGY ADVANCE ONLINE PUBLICATION | 1
Internal Medicine
Institute (F. Franceschi,
G. Zuccalà,
D. Roccarina),
Internal Medicine
and Gastroenterology
(A. Gasbarrini), Catholic
University of Rome,
Policlinico A. Gemelli
Largo A. Gemelli,
8‑00168 Rome, Italy.
Correspondence to:
F. Franceschi
francesco.franceschi@
rm.unicatt.it
Clinical effects of Helicobacter pylori outside
the stomach
Francesco Franceschi, Giuseppe Zuccalà, Davide Roccarina and Antonio Gasbarrini
Abstract | The discovery of Helicobacter pylori infection in the stomach could be considered as one of the
most important events of modern gastroenterology. Understanding of the natural history of many disorders
of the upper gastrointestinal tract, including chronic gastritis, peptic ulcer disease, gastric cancer and MALT
lymphoma, was altered by this discovery. Interestingly, epidemiological studies have also revealed a correlation
between H. pylori infection and some diseases localized outside the stomach, especially those characterized
by persistent and low‑grade systemic inflammation. Of note, H. pylori has an important role in iron deficiency
anaemia, idiopathic thrombocytopenic purpura and vitamin B
12
deficiency. Moreover, the association of
this bacterial pathogen with many other diseases, including hepatobiliary, pancreatic, cardiovascular and
neurodegenerative disorders is currently under investigation. In this Review, we summarize the results of the
most important studies performed to date surrounding the association of H. pylori infection with extragastric
diseases, as well as the strength of the evidence. We also provide information concerning bacterial–host
interactions and the mechanisms implicated in the pathogenesis of each of these extragastric diseases.
Franceschi, F. et al. Nat. Rev. Gastroenterol. Hepatol. advance online publication 17 December 2013; doi:10.1038/nrgastro.2013.243
Introduction
The discovery of H. pylori colonization of the stomach
and its associated pathogenic effects is a crucial landmark
in modern gastroenterology. Indeed, the natural history
of many disorders of the upper gastrointestinal tract, such
as chronic gastritis, peptic ulcer disease, gastric cancer
and MALT lymphoma are all linked with the presence
of this bacterium.
1
Since its discovery, many researchers
have clearly demonstrated that approximately one-half of
the worldwide population is infected with H. pylori and
that its prevalence is mostly linked with socioeconomic
status.
2,3
Epidemiological studies have also revealed a cor-
relation between H. pylori infection and some diseases
localized outside the stomach, especially those charac-
terized by persistent and low-grade systemic inflam-
mation (Box 1).
4,5
H. pylori has been suggested to affect
the development and progression of multiple diseases
outside the stomach through a variety of mechanisms
including the following: the production of a low-grade
inflammatory state; induction of molecular mimicry
mechanisms by expressing proteins that mimic host pep-
tides; and interference with the absorbance of different
nutrients and drugs.
4,5
For this reason, a large number of
papers have been published in this area during the past
few years and the European Helicobacter Study Group
dedicate a session to the extragastric manifestations of
H. pylori infection each year during their international
annual meeting. Considering the high number of papers
published on these extragastric diseases, the scope of this
Review is to summarize the results obtained by the most
important studies published so far about a possible role
of H. pylori in non-gastrointestinal diseases.
Cardiovascular diseases
Ischaemic heart disease
Ischaemic heart disease (IHD) was the first extragastric
disorder to be studied for a possible association with
H. pylori infection. In 1994, Mendall et al.
6
reported an
increased prevalence of H. pylori infection in patients with
documented IHD when compared with healthy controls,
even after adjustment for all known confounding factors,
such as high blood pressure, high levels of cholesterol, dia-
betes, smoking and current social class (odds ratio [OR]
2.15; P = 0.03). These findings stimulated many other
researchers to investigate this association, either from
the epidemiological or pathogenic point of view, some-
times with discordant findings. A prospective study by
Whincupp and co-workers showed that determining the
association between H. pylori infection and myocardial
infarction might be substantially confounded by the rela-
tionship between H. pylori infection, social class and major
cardiovascular risk factors.
7
Similar results were obtained
by Rathbone et al.
8
in a case–control study involving 342
patients with acute myocardial infarction.On the other
hand, Pasceri et al.
9
first introduced the concept that the
correlation between H. pylori infection and IHD is more
significant when the data are stratified for the presence of
more virulent strains of H. pylori, such as those express-
ing the cytotoxin CagA (cytotoxin associated gene A) (OR
3.8; 95% CI 1.6–9.1; P <0.001). Therefore, the reported
epidemiological association seems to be limited to only a
subgroup of patients infected with this bacterium.
Competing interests
The authors declare no competing interests.
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