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Association

between Helicobacter pylori infection and diabetes

mellitus: A meta-analysis of observational studies

Xiaoying Zhou a,b,1, Cuiling Zhanga,b,1, Junbei Wu a,b,1, Guoxin Zhanga,*aDepartment

of

Gastroenterology,

First

Affiliated

Hospital

of

Nanjing

Medical

University,

Nanjing

210029,

Chinab First Clinical Medical College of Nanjing Medical University, Nanjing 210029, China

1.

Introduction

Diabetes

mellitus

is

a

systemic

metabolic

disease

that

may

affect many organ systems, including the gastrointestinal

tract. Helicobacterpylori is regarded as a major gastroduodenal

pathogen and is etiologically linked with duodenal and gastric

disease

[1]. Some

studies

have

reported

a

higher

prevalence

of

H.

pylori

infection

in

people

with

diabetes

[15].The

reasons

for

this phenomenon may be that chemical changes in the gastric

mucosa, due to alterations in glucose metabolism, may

promote

H.

pylori

colonization;

in

addition,

the

immune

status

of diabetic

patients

is

compromised,

which

may lead

to

an

increased susceptibility to H. pylori infection [2]. However,

other

studies

have

indicated

neutral

or

even

negative

results

[630]. Thus, the significance of diabetes mellitus as a risk

factor for H. pylori gastric colonization remains unknown [8].

This meta-analysis was conducted to gain a better

understanding

of

whether

people

with

diabetes

are

more

prone

to

H.

pylori

infection

than

those

without

the

disease.

The

existence of a correlation between H. pylori and diabetes

mellitus may be of great use in clinic to treat people with

diabetes

for

gastrointestinal

diseases.

d i ab e te s r e se a rc h a n d c l in ic a l p r ac t ic e 9 9 ( 2 01 3 ) 2 0 0 2 08

a

r

t

i

c

l

e

i

n

f

o

Article history:

Received 11 September 2012

Received in revised form

27 October 2012

Accepted 15 November 2012

Published on line 8 February 2013

Keywords:

Helicobacter pylori

Diabetes mellitus

Meta-analysis

a

b

s

t

r

a

c

t

Aims: Some studies have shown Helicobacter pylori (H. pylori) infection to be associated with

diabetes mellitus, but the relationship remains controversial. This meta-analysis was

designed to quantify the association between H. pylori infection and diabetes.

Methods: A computerized search of PubMed and Embase was carried out. Studies that

provided data on H. pylori infection in both diabetes and control groups were selected.

An unconditional logistic regression model was used to analyze potential parameters

related to H. pylori prevalence. Subgroup analyses were conducted for types of diabetes,

methods of detection, geographical distribution, hemoglobin A1c (HbA1c) levels and evi-

dence grade.

Result: Forty-one studies were identified, involving 14,080 patients, with a total H. pylori

infectionrate of 42.29%.The OR forH. pylori infectionwas increased to 1.33 (95% CI:1.081.64;

P = 0.008) among the patients with diabetes. Subgroup analysis revealed a significantly

higher infection rate ofH. pylori in the type 2 diabetes group versus the control group:OR = 1.76, 95% CI: 1.402.21, P < 0.00001.

Conclusions: The pooled data suggests a trend toward more frequent H. pylori infections in

diabetes patients, especially in type 2 diabetes patients. As this is a meta-analysis of

observational studies, more randomized controlled trials should be done in the future.

# 2012 Elsevier Ireland Ltd.

All rights reserved.

* Corresponding author. Tel.: +86 25 83718836x6973; fax: +86 25 83674636.E-mail address: guoxinz@njmu.edu.cn (G. Zhang).

1 These authors contributed equally to this work.

Contents available at Sciverse ScienceDirect

Diabetes Researchand Clinical Practice

journal homepage: www.elsevier.com/locate/diabres

0168-8227/$ see front matter# 2012 Elsevier Ireland Ltd. All rights reserved.

http://dx.doi.org/10.1016/j.diabres.2012.11.012

http://dx.doi.org/10.1016/j.diabres.2012.11.012mailto:guoxinz@njmu.edu.cnhttp://www.sciencedirect.com/science/journal/01688227http://www.sciencedirect.com/science/journal/01688227http://www.sciencedirect.com/science/journal/01688227http://dx.doi.org/10.1016/j.diabres.2012.11.012http://dx.doi.org/10.1016/j.diabres.2012.11.012http://www.sciencedirect.com/science/journal/01688227mailto:guoxinz@njmu.edu.cnhttp://dx.doi.org/10.1016/j.diabres.2012.11.012

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2.

Materials

and

methods

2.1.

Inclusion

criteria

1.

Study design: published case-control and cross-sectional

studies.

2. Studies providing data dealing with H. pylori infection inboth diabetes group and control group.

3. Studies in which H. pylori infection was confirmed by 13C-

urea

breath

test, mucosal

biopsy,

enzyme-linked

immuno-

assay

(ELISA)

and/or

polymerase

chain

reaction

(PCR).

At

least one positive test was regarded as confirmation of

infection.

2.2. Exclusion criteria

1.

Case

report

and

observational

studies

without control

groups.

2. Studies in which the data of H.pylori infection rate were not

available for either diabetes group or control group.3.

Subset

of

a

published

article

by

the

same

authors.

4. Studies limited to animals.

5. Studies in which research subjects had history of drug use

for

antibiotics,

H2

blockers,

or

proton

pump

inhibitors

within

4

weeks.

2.3. Literature search

The PRISMA guidelines for conducting meta-analysis were

followed

[31]. Two

investigators (XYZ

and

CLZ)

performed a

systematic

literature search of

PubMed

and

Embase, from

inception to April 2012, using the MeSH terms (Helicobacter

pylori or H. pylori) AND (diabetes mellitus OR diabetes). Thetwo investigators worked independently, at different times

and

at different

medical science

information

centers affiliat-

ed to Nanjing Medical University. The searches were repeated

several times. The last search was conducted on April 13,

2012. The relevant articles texts and reference lists were

manually search to broaden the scope of our findings. We

evaluated the full-texts of papers published in English, and

the

English

abstracts of

papers

published in

other

languages.

When further

information

was

required

from a

potentially

relevant manuscript, the corresponding authors were con-

tacted by the reviewers.

2.4. Data extraction and appraisal of study quality

The two investigators who performed the literature search also

performed the data extraction, working independently. The

first authors, year and country of publication, study type,

method

of

detection,

diagnosis,

type

of

specimen,

sample

size

and

type

of

organism

identified

were

recorded

for

each

included

study. The numbers of Helicobacter-positive and -negative

patients in the diabetes group and the control group were

collected.

Whendata

from

one

study

was

reported

in

more

than

one

manuscript,

only

one

was

selected

for

the

meta-analysis,

according to the following criteria (applied consecutively): (1)

availability of adjusted odds ratio (OR) estimates for diabetics

and non-diabetics; (2) longer follow-up period (applicable to

nested

case-control

and

cross-sectional

analyses);

and

(3)

larger

sample size. When the relationship between H.pylori infection

and diabetes was reported in different articles referring to the

same study, both were considered eligible, but only one was

included in the meta-analysis.

2.5.

Statistical

analysis

In this study, the random effect model or fixed effect model

was used for meta-analysis, according to the heterogeneity

between

studies.

Heterogeneity

was

tested

by

the

Q

test

(P