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Table 1 The main characteristics of Case – Control studies of the effect of H pylori on risk of diabetes

From: Helicobacter pylori infection as a risk factor for diabetes: a meta-analysis of case-control studies

Authors

Years

Country

Control subjects(selection methods)

Age

Sample size

Type of Diabetic

(Mean HbA1C)

(Duration of disease)

Measurement of association

Odds Ratio

(CI 95%)

Controlled variables

Bacteria detection

NOS

Score

Małecki, M. et al. [26]

1996

Poland

Non-diabetic subjects

17–80

139 (Control:100 & Case: 39)

DM (−)

(8 Year)

0.33

(0.18, 0.59)

–

Histology or biopsy

6

Pocecco, M. et al. [27]

1997

Italy

Admitted for minor extra-abdominal surgery with no history of abdominal pain

16

379

[Control:310 & Case: 69]

DM

(−)

(−)

3.13

(2.08, 4.70)

Age, sex, education and economic

Rapid urease test

6

Gentile, S [28].

1998

Italy

Non-diabetic subjects

52

328 (Control:164 & Case: 164)

T2DM

(8.3 ± 1.4)

1.77

(1.35, 2.31)

Age, sex and body weight

Histology or biopsy

7

De Luis, DA [29]

1998

Spain

The control subjects were healthy volunteers, with similar age and sex-distribution that the diabetic patients

25

180

Control: 100 & Case: 80

T1DM (−)

(3.1

Year)

1.36

(0.98, 1.87)

Age and sex

Anti-H. pylori antibody

6

Gasbarrini, A.et al. [30]

1998

Italy

Healthy subjects

35

166

[Control: 50 & Case:

116]

DM

(−)

(19 year)

1.04

(0.85, 1.28)

Age and sex

13C or 14C urea breath test

6

Salardi, S.et al. [31]

1999

Italy

Children with minor endocrine disorders.

12

339

[Control: 236 & Case:

103]

T1DM

(−)

(−)

1.47

(0.99, 2.18)

Age

Anti H. pylori antibody

7

Arslan, D. et al. [32]

2000

Turkey

Non-diabetic subjects

12

130 (Control: 42 & Case: 88)

T1DM (11.08 ± 3.17)

(3.85 Year)

1.38

(1.08, 1.75)

–

Anti-H. pylori antibody

6

Dore, MP. et al. [33]

2000

Italy

Blood donors from the same geographic area

12–75

891

[Control: 506 & Case: 385]

DM

(greater than 1 year)

1.16

(1.00, 1.35)

age and socioeconomic status

Anti-H. pylori antibody

8

Senturk, O. et al. [34]

2001

Turkey

Nondiabetic patients undergoing upper diagnostic endoscopies

54.1

140

[Control: 73 & Case: 67]

T2DM

(6.42 ± 0.97)

(4.5 year)

1.39

(0.78, 2.48)

Age and socioeconomic

Histology or biopsy

7

Ravera, M.et al. [35]

2001

Uganda

Dyspeptic patients without diabetic

–

132

[Control110: & Case: 22]

DM

(−)

(−)

1.22

(0.33, 4.49)

–

Histology or biopsy

6

Ko, G. T.et al. [36]

2001

Chine

With upper GI symptoms in whom

49.9

118

[Control55: & Case: 63]

T2DM

(8.25 ± 2.22) (6.2 year)

0.90

(0.64, 1.26)

Age and sex

Rapid urease test

6

Marrollo M.et al. [37]

2001

Italy

Non diabetic dyspeptic patients

63

191

[Control: 117& Case: 74]

DM

(−)

(−)

1.54

(1.05, 2.27)

Age and sex

Rapid urease test and Histology or biopsy

6

Quatrini, M.et al. [38]

2001

Italy

Dyspepsia patients

58

142

[Control: 71 & Case: 71]

DM

(−)

(−)

1.63

(1.12, 2.38)

Age and sex

13C or 14C urea breath test

7

Cenerelli, S. et al. [39]

2002

Italy

Control subjects were first selected on the basis of the admission criteria of the senieur protocol.

55

73

Control: 43 & Case: 30)

T2DM (6.1 ± 1.8)

(3.1

Year)

1.04

(0.60, 1.80)

–

13C or 14C urea breath test

7

Maule, S.et al. [40]

2002

Italy

Individuals without diabetes

46–75

62

[Control:31 & Case: 31]

T2DM

(7.1 ± 1.4)

(−)

1.65

(0.92, 2.97)

Age

13C or 14C urea breath test

8

Candelli, M. et al. [41]

2003

Italy

The control Group was selected normal healthy adolescent

17

268

Control: 147 & Case: 121)

T1DM (8.2 ± 1.4)

(6.7 Year)

0.97

(0.72, 1.30)

Sex, age and social class

Rapid urease test,

Histology or biopsy

7

Gulcelik, N. E.et al. [4]

2005

Turkey

Dyspeptic non diabetic subjects

51.9

149

[Control: 71 & Case: 78]

T2DM

(8.2 ± 1.4)

1.92

(1.29, 2.86)

Age and BMI

Histology or biopsy

7

Jaber, S. M.et al. [42]

2006

Saudi Arabia

Healthy children

> 10

604

[Control:543 & Case: 61]

T1DM

(−)

(−)

1.60

(0.98, 2.63)

–

Anti H. pylori antibody

6

Bener, A. et al. [43]

2007

Qatar

Non-diabetic subjects

48

420 (Control:210 & Case: 210)

T2DM

(6.9 ± 1.4)

(−)

5.03

(3.90, 6.47)

Age and sex

Anti-H. pylori antibody

7

Demir, M. et al. [44]

2008

Turkey

The control Subjects were selected in the gastroenterology clinics

52

283

Control: 142 & Case: 141

T2DM

(−)

(6 year)

1.07

(0.84, 1.36)

Age and sex

Rapid urease test and Histology or biopsy

7

Ariizumi, K. et al. [45]

2008

Japan

non-diabetic subjects without upper GI tract disorders

62

134

[Control: 67 & Case: 67]

DM

(−)

(15.1 year)

0.74

(0.53, 1.03)

age and sex-matched

Anti H. pylori antibody,

Rapid urease test, Histology or biopsy

8

Hamed, S. A.et al. [46]

2008

Egypt

Subjects with neither history nor clinical evidence of gastrointestinal problems; vascular, inflammatory, or neurologic diseases.

47.6

140

[Control:60 & Case: 80]

DM

(−)

(9.2 year)

1.29

(0.83, 2.01)

Age and sex

Anti H. pylori antibody

8

Cabral, V. L. R. et al. [47]

2009

Brazil

The control Group was selected normal healthy adolescent

17

45

Control: 30 & Case: 15)

T1DM (−)

(−)

0.52

(0.21, 1.29)

–

Histology or biopsy

7

Lazaraki, G. et al. [48]

2009

Greece

non-smoking, non-diabetic with of dyspepsia

65

79

[Control: 30 & Case: 49]

T2DM

(−)

(3 year)

0.99

(0.70, 1.40)

Age, sex, H. pylori-infection, degree of gastritis

Rapid urease test and Histology or biopsy

7

Krause, I. et al. [49]

2009

Colombia

Individuals had no clinical diabetes, nor islet cell autoantibodies

16.0

180

[Control: 123: & Case: 57]

T1DM

(−)

(8.8 year)

0.44

(0.29, 0.66)

–

Anti-H. pylori antibody

6

Devrajani, BR. et al. [15]

2010

Pakistan

Non diabetic individuals with positive or negative Helicobacter pylori infection

53

148

[Control: 74 & Case: 74]

T2DM

(−)

(5 years)

1.64

(1.11, 2.43)

–

Stool antigen test

7

Ibrahim, A. et al. [50]

2010

Egypt

Dyspeptic non diabetic subjects

45

200

[Control: 102 & Case: 98]

T2DM

(8.57 ± 0.79)

(−)

0.94

(0.71, 1.25)

–

Rapid urease test, Histology or biopsy

7

El-Eshmawy, M. M. et al. [51]

2011

Egypt

Non-diabetic subjects

20

242 (Control:80 & Case: 162)

T1DM

(8.2 ± 1.75)

(7.29 Year)

1.63

(1.25, 2.11)

Age, sex, geographic area and socioeconomic status

Anti-H. pylori antibody

7

De Block, C. E. M. et al. [52]

2012

Belgium

One-hundred sex- and age-matched controls were tested for H. pylori serology.

40

329

Control: 100 & Case: 229)

T1DM (7.8 ± 1.0)

(18 Year)

0.86

(0.74, 1.02)

Age and sex

Anti-H. pylori antibody &

Rapid urease test and Histology or biopsy

7

Candelli, M. et al. [53]

2012

Italy

Healthy children

19.8

174

[Control: 99 & Case: 75]

T1DM

(8.8 ± 0.80)

(−)

1.96

(1.40, 2.75)

Age, sex and socio-economic

13C or 14C urea breath test

6

Jafarzadeh, A.et al. [54]

2012

Iran

Healthy individuals

42.86

200

[Control: 100 & Case: 100]

T2DM

(−)

(−)

1.03

(0.74, 1.42)

Age

Anti H. pylori IgG

6

Keramat, F. et al. [55]

2013

Iran

Non-diabetic subjects

51

158 (Control: 79 & Case: 79)

DM (8.96 ± 1.82)

(2.78 Year)

1.29

(0.89, 1.88)

Age and sex

Anti-H. pylori antibody &

Rapid urease test and Histology or biopsy

8

Zekry, O. A. et al. [56]

2013

Egypt

Healthy children and adolescents

12.53

120

[Control: 60 & Case: 60]

T1DM

(7.75 ± 1.67)

(9.25 year)

1.69

(1.21, 2.35)

Age and sex

Anti-H. pylori antibody

8

Chobot, A. et al. [57]

2014

Poland

This group was enrolled from a large cohort of children

13.4

447

[Control: 298 & Case: 149]

T1DM

(7.69 ± 1.63)

(4.6 year)

0.74

(0.48, 1.15)

Age- and sex

13C or 14C urea breath test

8

Fayed, SB. et al. [58]

2014

Egypt

healthy normal volunteers

12.2

106

[Control:53 & Case: 53]

T1DM

(9.6 ± 1.6)

(12.2 year)

1.80

(1.14, 2.84)

Age and sex

Anti H. pylori antibodies

7

Zhou, F. et al. [17]

2015

China

Non-diabetic subjects with dyspepsia symptoms

45

253 (Control:65 & Case: 188)

T2DM

(8.2 ± 1.9)

1.15

(0.99, 1.33)

Age and sex

Anti-H. pylori antibody

&

Rapid urease test

9

Bajaj, S. et al. [3]

2015

India

The control group comprised of age, sex, socioeconomic status, and education matched normal healthy volunteers

> 18

140

Control: 60 & Case: 80)

T2DM (8.2 ± 1.2)

(4.2 Year)

1.53

(1.04, 2.24)

Age, sex, socioeconomic status, and education

Anti-H. pylori antibody &

Rapid urease test and Histology or biopsy

8

Bazmamoun, H. et al. [59]

2016

Iran

Non-diabetic subjects

10

160 (Control: 80 & Case: 80)

T1DM (8.00 ± 0.65)

(2.72 Year)

1.50

(1.09, 2.07)

Age, sex, socioeconomic status

Anti-H. pylori antibody

8

Osman, S. M.et al. [60]

2016

Sudan

Healthy children

1–18

180

[Control: 90 & Case: 90]

T1DM

(−)

(6 month)

0.97

(0.71, 1.33)

age and sex

Anti-H. pylori antibody

8

Alzahrani, S. et al. [61]

2017

Saudi Arabia

Non-diabetic subjects

49

842 (Control:421 & Case: 421)

DM (6.1 ± 0.6)

1.01

(0.88, 1.16)

Age,

sex, race,

DPP intervention, length of follow-up time, body mass index, alcohol consumption, physical activity and smoking

Anti-H. pylori antibody

&

Rapid urease test

9

Vaishnav, B. et al. [62]

2018

India

Non diabetic with dyspepsia

56

287

[Control: 140 & Case:

147]

T2DM

(8.4 ± 1.0)

(7.59 year)

1.89

(1.51, 2.36)

–

Rapid urease test

8