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Helicobacter pylori Infection Is Associated with Type 2 Diabetes, Not Type 1 Diabetes: An Updated Meta-Analysis.

1. Introduction

Helicobacter pylori (H. pylori) is a gram-negative spiral bacterium, colonized in the stomach. Approximately one-half of the population over the world is infected with H. pylori [1]. Many researches have proved that H. pylori infection is highly associated with gastrointestinal diseases such as chronic gastritis, peptic ulcer disease, gastric cancer, and mucosa-associated lymphoid tissue (MALT) lymphoma since its discovery [2]. In addition, extragastric disorders associated with H. pylori infection, such as cardiovascular diseases and metabolic syndrome, have been revealed and some of them were characterized by persistent and low-grade systemic inflammation [3]. Inflammation has been demonstrated to play an important part in the pathogenesis of diabetes mellitus (DM), especially type 2 DM (T2DM) [4]. On the other hand, Kondrashova and Hyoty reviewed that some microbes served as the risk factor participating in the trigger and the development of type 1 DM (T1DM), but some microbes such as H. pylori served as a protective factor by lowering the risk of T1DM [5]. Above all, H. pylori infection was a factor not negligible in the process of DM.

Since Simon et al. firstly reported the association between H. pylori infection and DM [6], many studies were carried out. Several case-control studies have reported a higher prevalence of H. pylori infection in DM patients [7, 8]. Some cross-sectional researches also revealed a significant correlation between H. pylori infection and diabetes [9-11]. Moreover, a meta-analysis carried out by Zhou et al. suggested a trend toward more frequent H. pylori infection in DM patients, especially in T2DM patients [12]. However, Tamura et al. found a significantly higher DM prevalence among individuals with H. pylori infection than those without, but the difference could be mostly ascribed to older age [13]. And some studies argued that no difference in the prevalence of H. pylori infection was found between DM and non-DM individuals [14, 15]. Overall, this subject remains controversial now.

The present updated meta-analysis was conducted to answer if there is a difference in the prevalence of H. pylori infection between DM and non-DM individuals. Subgroup analyses were carried out based on the types of DM, geographical regions, and methods for H. pylori detection to further investigate the relationship between H. pylori infection and DM.

2. Methods

2.1. Search Strategy and Selection Criteria. Published guidelines for conducting meta-analyses were followed [16]. We searched PubMed, Embase databases, Cochrane Library, Google Scholar, Wanfang Data (Chinese), China national knowledge database (Chinese), and SinoMed (Chinese) for all relevant articles reported from January 1996 to January 2016, with combinations of the search terms "Helicobacter pylori," or "H. pylori," or "Campylobacter pylori," or "C. pylori," and "diabetes mellitus," or "diabetes," or "type 1 diabetes," or "type 1 diabetes mellitus," or "type 2 diabetes" or "type 2 diabetes mellitus".

To be eligible for inclusion, studies had to meet the following criteria: (1) they were published studies which reported H. pylori infection in DM individuals and non-DM individuals (individuals without DM, impaired glucose tolerance, or impaired fasting glucose); (2) detailed data of H. pylori infection rate in both groups was provided. Studies that did not meet the inclusion criteria were not enrolled.

Studies were excluded if they were as follows: (1) duplicate publications; (2) case report, review, meta-analysis, or guideline; (3) not reporting clinically relevant outcomes; and (4) not providing enough details.

2.2. Data Extraction and Quality Assessment. Data were extracted by one investigator, verified by another investigator, and recorded in a well-designed form developed for this study. The data items included authors, year of publication, country, study design, methods of H. pylori detection, strains of H. pylori, types of DM, age, and sample size. The Newcastle-Ottawa scale (NOS) scoring system was used to assess the quality of the studies [17].

2.3. Statistical Analysis. To obtain pooled effect estimates, the random effects model or fixed effects model was used for meta-analysis, according to the heterogeneity among studies. If there was no statistically significant heterogeneity (two-tailed P value > 0.05) among the pooled studies, the fixed effect model would be applied; otherwise, the random effect model would be applied [18]. Odds ratio (OR) with 95% confidence interval (CI) was used for the case-control and cross-sectional studies, while risk ratio (RR) was for the cohort studies. The presence of between-study heterogeneity was estimated using Q-test and [I.sup.2] statistics. Sources of heterogeneity were explored by conducting subgroup analyses based on types of DM, geographical regions, and methods of H. pylori detection. The two-sided tests with significance level of 0.05 were conducted in pooled analyses and subgroup analyses using RevMan software (Version 5.3 for Windows, Cochrane Collaboration, Oxford, UK). Publication bias was evaluated graphically by the funnel plots and statistically by Begg's test and Egger's test with the STATA software (Version 14.0; STATA Corporation, College Station, TX, US). Pr and P value less than 0.05 were considered representative of no statistically significant publication bias. If publication bias was indicated, the trim and fill method procedure was performed to identify and correct the publication bias [19]. The basis of the method was to (1) "trim" (remove) the studies causing funnel plot asymmetry, (2) use the trimmed funnel plot to estimate the true "centre" of the funnel, and then (3) replace the removed studies and their missing "counterparts" around the centre (filling). An estimate of the number of missing studies was provided; an adjusted OR is derived by performing a meta-analysis including the filled studies.

3. Results

3.1. Description of Studies. A total of 783 studies were retrieved from PubMed, Embase databases, Cochrane Library, Google Scholar, Wanfang Data (Chinese), China national knowledge database (Chinese), and Sino-Med (Chinese). According to the criteria for inclusion and exclusion, 79 studies were included in this meta-analysis (Figure 1). The included study characteristics were summarized in Table 1. All of the articles were qualified to be pooled with quality score of NOS over 5. 76 studies were either case-control or cross-sectional studies, and 3 were prospective cohort ones.

A total of 57,397 individuals were enrolled in these studies, with a total H. pylori infection prevalence of 49.7% (28,542/57,397). The pooled H. pylori infection rate was 54.9% (9434/17,187) in DM group and 47.5% (19,108/ 40,210) in non-DM group. The OR was 1.69 (95% CI: 1.471.95, P < 0.001) for the two groups. There was high heterogeneity among the studies ([I.sup.2] = 86%). The forest plot for pooled prevalence is showed in Figure 2. Each study was sequentially removed from the analysis, and the adjusted ORs (1.63-1.73) were approximate to the initial ones. Especially, the study of Han et al. [20] recruited a total of 6395 patients in DM group and 24,415 in non-DM group, which accounted for nearly one-third of the enrolled individuals in this analysis. However, after removing the data of Han et al. and re-analyzing, the adjusted odds (OR= 1.71) and heterogeneity ([I.sup.2] = 83%) were still approximate to the initial ones in spite of its overweight scale.

3.2. Subgroup Analysis. We found a significant association between H. pylori infection and DM but the pooled analysis was with high heterogeneity ([I.sup.2] = 86%). Subgroup analyses based on the types of DM, geographical regions, and methods for H. pylori detection were conducted to detect the sources of heterogeneity.

(1) Types of DM

12 studies with 3175 individuals were assigned to the T1DM subgroup, while 42 studies with 41,684 individuals were to the T2DM subgroup. No significant difference was found between T1DM group and non-DM group in H. pylori infection rate (OR= 1.23, 95% CI: 0.77-1.96, P = 0.38; Figure 3). On the contrary, the pooled data indicated that the prevalence of H. pylori infection in T2DM was significantly higher than that in non-DM group (OR = 2.05, 95% CI: 1.67-2.52, P <0001; Figure 3). Each study including the study by Han et al. with overweight scale was sequentially removed in the subgroups and the adjusted ORs (1.93-2.10 in T2DM and 1.10-1.42 in T1DM) approximated to the initial ones.

(2) Geographical regions

Subgroup studies stratified by geographical regions were performed. The recruited individuals were mostly from Asia (75.8%, 43,523/57,397). The infection rate was 51.7% (22,503/43,523), 39.7% (2969/7479), 47.3% (2562/5411), and 48.7% (499/1024) in group Asia, group Europe, group America, and group Africa, respectively. No significant difference of H. pylori infection rate between DM and non-DM individuals was found in group America and group Africa (P = 036 for America; P = 038 for Africa). However, in group Asia and group Europe, significantly higher H. pylori infection rate was detected in DM individuals (OR = 2.04 and OR = 1.40, resp.). But there was still high heterogeneity within these subgroups ([I.sup.2] = 68%-90%; Figure 4).

(3) Methods for H. pylori detection

Methods for H. pylori detection displayed different power in accuracy, which consequently might affect the detection rate of H. pylori infection. Methods for diagnosis of H. pylori were classified as invasive tests and noninvasive tests [21]. Invasive tests included rapid urease test, histology, and culture, and the noninvasive tests included [sup.13]C or [sup.14]C urea breath test, stool antigen detection, and serological approaches for antibodies of H. pylori. For the serological tests of anti-H. pylori IgG or/and IgA antibody in serum, high rates of false-positive results may happen and they cannot identify the differences between the current infection and past infection [21, 22]. So we typically sorted the studies with detection method of serological test into one subgroup and others into the other subgroup as they could identify the current infection precisely.

The studies of current infection group comprised of 51 articles and showed a significant higher prevalence of H. pylori infection in DM patients as compared to that in non-DM individuals with OR= 1.92 (95% CI: 1.57-2.34, P < 0.001). Similarly, by enrolling 21 articles in serological test group, we found that the infection rate was 53.7% (1956/3640) in DM group while 46.4% (4097/8829) in the non-DM one (OR= 1.40, 95% CI: 1.10-1.79, P < 0001; Figure 5). The heterogeneities in both groups were high among studies with [I.sup.2] = 89% and [I.sup.2] = 81%, respectively (Figure 5).

3.3. Publication Bias. Funnel plot analysis did not show significant evidences of publication bias (Figure 6). Most of the studies were concentrated symmetrically. No significant publication bias was detected by Begg's test with Pr = 0.411 but a significant bias was detected by Egger's test with P < 0.001 (Figure 7). As Egger's test indicated the possibility of publication bias, the trim and fill method procedure was performed to identify and correct the publication bias. There was 14 hypothetical missing studies indicated by the trim and fill procedure, and the imputed pooled estimate was 1.366 (95% CI: 1.181-1.580, P < 0.001). There still existed a statistically significant association between H. pylori infection and DM after adjusting for the publication bias, which suggested that our result was credible. Adjusted funnel plot by the trim and fill method was symmetrical and shown in Figure 8.

4. Discussion

DM is a chronic disease characterized by a long-term inflammation mechanism. Guo et al. demonstrated that diabetes was a risk factor for H. pylori infection [23]. Several meta-analyses aiming to investigate the association between H. pylori infection and DM have been carried out. Zhou et al. recruited 41 studies involving 14,080 patients, and the analysis reported higher risk of H. pylori infection among DM patients with OR= 1.33 (95% CI: 1.08-1.64) [12]. Wang et al. retrieved 39 studies involving more than 20,000 participants, with the OR= 1.59 (95% CI: 1.33-1.90) [24]. Our meta-analysis was an updated one and included more studies and individuals. Consistently, we found that the prevalence of H. pylori infection was significantly higher in DM patients. But we brought more robust result with higher OR (OR= 1.69, 95% CI: 1.47-1.95; Figure 2). Moreover, we explored more databases and recruited 25 studies reported in Chinese with high-quality score of NOS (all of them were > 5). In addition, in subgroup analysis, we found no significant difference in prevalence of H. pylori infection in comparison between T1DM patients and non-DM people, which was inconsistent with what was reported by Wang et al. In a subgroup analysis of geographical regions, we found significant higher H. pylori infection rate among DM individuals in group Asia and group Europe but not in group Africa or group America. It was inconsistent with the Zhou et al. study which reported that the H. pylori effect only happened in Asian people. In this meta-analysis, we found no publication bias with Begg's test, while Egger's test showed a possibility of publication bias. But we performed the trim and fill method and found 14 hypothetical missing studies. The imputed pooled result still supported our original one. Therefore, no publication bias was shown in our meta-analysis and the result we got was credible. In this meta-analysis, the study of Han et al., even though with a total of 30,810 participants, did not affect the significance of the pooled results. Maybe it was because the other studies recruited as enough individuals (a total of 26,587 participants) as to be commensurate to the scale of the Han et al. study. Furthermore, the quality score of NOS for the study Han et al. was 9, which was high. Hence, despite the overweight scale, the study of Han et al. should not be neglected.

We found that there existed an association between H. pylori infection and DM in this meta-analysis. Several possible mechanisms might explain the association. Hyperglycemic condition in diabetic individuals could result in immune dysfunction, including damage to the neutrophil function, depression of antioxidant system, and impaired humoral immunity [25]. Moreover, abnormal enteric neuropathy caused by high blood sugar can modulate immune-cell function and stimulate proinflammatory cytokine production, resulting in neurodegeneration [26]. It leads to delay gastric emptying and lacking of acid secretion, which promotes bacterial colonization or overgrowth in gastrointestinal tract [27]. On the other hand, H. pylori infection in diabetic patients may worsen glycemic control [28], which leads to the difficulty of DM treatment, forming the vicious circle.

In this meta-analysis, we found that DM patients had a higher prevalence of H. pylori infection. But we could not come to the result whether and what role H. pylori infection plays on the pathogenesis or development of DM. It was reported that patients could be coinfected with H. pylori and some other pathogens like herpes simplex virus 1, cytomegalovirus, and Epstein-Barr virus, some of whom were also associated with DM [29-31]. But the number of researches on this issue was limited. We could not know whether other pathogens affect the effect of H. pylori on DM, either. Jeon et al. firstly carried out a prospective cohort study of 782 Latino elderly aged > 60 years and diabetes-free [32]. After following up over 10 years, the authors demonstrated that H. pylori seropositive patients experienced a greater rate of incident DM than individuals without DM (hazard ratio 2.69, 95% CI: 1.10-6.60), whereas those who were seropositive for herpes simplex virus 1, varicella virus, cytomegalovirus, and Toxoplasma. gondii did not show an increased rate of DM. It indicated that H. pylori infection might play an unknown role in the pathogenesis of DM, which implicated a potential step for preventing DM by eradication of H. pylori infection. Moreover, it also suggested that other pathogens such as cytomegalovirus and herpes simplex virus 1 might not have the similar effect on the DM like H. pylori. But our meta-analysis just revealed the association between H. pylori and DM, but could not suggest the effect of H. pylori on DM pathogenesis. More researches are needed to find out the actually effect of H. pylori infection on DM.

In subgroup analysis based on the types of DM, we demonstrated that 56.5% T2DM individuals were infected with H. pylori, but only 36.2% T1DM carried the bacterium (Figure 3). T2DM was more significantly prone to the infection of H. pylori. As to T2DM, insulin resistant (IR) is one of its characteristics. Aydemir et al. showed that IR was significantly higher in H. pylori infection group [33]. And Eshraghian et al. also supported that H. pylori infection was a risk factor for IR [34, 35]. Furthermore, it was reported that IR in T2DM patients could be improved after successful eradication of H. pylori [4]. It might partly explain the higher H. pylori infection rate in T2DM patients. On the other hand, we found no significant difference in prevalence of H. pylori infection in comparison between T1DM patients and non-DM people (P = 0.38), consistently with the report by Candelli et al. [27]. Whether this outcome is caused by the different pathogenesis or the onset age of T1DM and T2DM remains unclear. In the T1DM group, the mean age in most studies was not over 20, except for the studies of De Block et al. [36] and Sfarti et al. [37], while in T2DM group, the mean age was usually over 50 years old (Table 1). Epidemiological studies suggested that the prevalence of H. pylori infection increases with age [34]. As T1DM mainly onsets during childhood or young age, T1DM patients probably have less chance to be exposed to H. pylori infection. Consistently, Krause et al. showed a significantly lower positive rate of antibodies against H. pylori in T1DM patients [38]. But some studies held the contrary view that T1DM individuals were also prone to H. pylori infection [39, 40]. However, our meta-analysis with pooled estimate favored that T2DM rather than T1DM was associated with H. pylori infection. But the sample size of T1DM subgroup was not as large as that of T2DM. Larger sample size is needed to further verify the association between H. pylori infection and DM, especially T1DM.

The prevalence of H. pylori infection varies in different regions. We found significant higher H. pylori infection rate among DM individuals in group Asia and group Europe but not in group Africa or group America (Figure 4). Firstly, it was to be noted that there were much bigger sample size in group Asia and group Europe, respectively. This might be due to the more accurate detection methods and in group Africa and group America; the sample size might be too small to draw robust conclusion. Secondly, it might be explained by that the condition of medical care in developing countries from group Asia was too poor for DM patients to get good control of DM and prevent infectious complications. On the other hand, the epidemiology and different strains of H. pylori infection might attribute to the part of the result. Epidemiology studies revealed that almost all the Asians are infected with the strain of H. pylori carrying cytotoxin-associated gene A (CagA) but only nearly 60% of western people carried this stain [41, 42]. It was reported that H. pylori infection in Asians was predominated by CagA ice-Al genotypes while Americans and Africans by CagA ice-A2 genotypes [41, 43]. CagA is a major virulence factor of H. pylori and has been reported to be associated with diabetic complications [44]. CagA-positive strain of H. pylori could cause poor glycemic control in T2DM and difficulty in eradication, which might result in the visible H. pylori effect among Asian but not African DM patients. However, due to the lack of data, we could not carry out the subgroup analysis based on different strains of H. pylori.

A number of testing methods are available for H. pylori detection. Serological test, namely, anti-H. pylori IgG and/ or IgA test, is not affected by acid suppression therapy or recent antibiotic use. But seropositivity could not confirm current H. pylori infection, and anti-H. pylori IgG titre usually remains elevated for a long period even after clearance or eradication. Some study using anti-H. pylori IgG as the diagnosis of H. pylori infection might overestimate the infection rate. We typically conducted the analysis of serological test group and current infection group and found that in both subgroups, DM patients had higher prevalence of H. pylori infection than non-DM people (Figure 5). As a result, the association between H. pylori infection and DM was verified despite of different methods for H. pylori detection.

Despite the robust result, there existed limitations in our study. The studies were highly heterogeneous. Variables like age, sex, race, economic status, DM prevalence, and strains of H. pylori infection in the included studies varied. For the lack of enough detailed data, subgroup analysis stratified by age, sex, different stages of DM, and strains of H. pylori, which might bring up heterogeneity, could not be carried out. Furthermore, most of the articles meeting the inclusive criteria were case-control or cross-sectional ones, and only 3 were prospective ones. More well-designed and prospective cohort studies are needed for clarifying the association between H. pylori infection and DM.

In conclusion, despite the limitations, our meta-analysis suggested that there is significantly higher prevalence of H. pylori infection in DM when compared with the non-DM individuals. And the difference is associated with type 2 DM but not type 1 DM.
Abbreviations

H. pylori:   Helicobacter pylori
DM:          Diabetes mellitus
T2DM:        Type 2 DM
T1DM:        Type 1 DM
NOS:         Newcastle-Ottawa scale
OR:          Odds ratio
CI:          Confidence interval
RR:          Risk ratio
IR:          Insulin resistant
CagA:        Cytotoxin-associated gene A
MALT:        Mucosa-associated lymphoid tissue.


https://doi.org/10.1155/2017/5715403

Conflicts of Interest

The authors declare that they have no conflict of interest.

Authors' Contributions

Jun-Zhen Li and Jie-Yao Li contributed equally to this work.

Acknowledgments

This study was supported by the National Natural Science Foundation of China (no. 81270442 and no. 81370475).

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[81] G. X. Sun, Y. J. Tan, and Y. L. Zhu, "The relationship between type 2 diabetes mellitus and H. pylori infection," Journal of Practical Medical Techniques, vol. 14, no. 28, pp. 3868-3869, 2007.

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[83] X. M. Lu, L. M. Chen, H. Yang, C. F. Ye, S. G. Yang, and M. Xiang, "Association of ischemic cardiocerebrovascular disease with Helicobacter pylori infection in patients with type 2 diabetes," Chinese Journal of Endocrinology and Metabolism, vol. 22, no. 4, pp. 359-360, 2006.

[84] N. E. Gulcelik, E. Kaya, B. Demirbas et al., "Helicobacter pylori prevalence in diabetic patients and its relationship with dyspepsia and autonomic neuropathy," Journal of Endocrinological Investigation, vol. 28, no. 3, pp. 214-217, 2005.

[85] R. F. Gillum, "Infection with Helicobacter pylori, coronary heart disease, cardiovascular risk factors, and systemic inflammation: the Third National Health and Nutrition Examination Survey," Journal of the National Medical Association, vol. 96, no. 11, pp. 1470-1476, 2004.

[86] R. Anastasios, C. Goritsas, C. Papamihail, R. Trigidou, P. Garzonis, and A. Ferti, "Helicobacter pylori infection in diabetic patients: prevalence and endoscopic findings," European Journal of Internal Medicine, vol. 13, no. 6, p. 376, 2002.

[87] S. Cenerelli, P. Bonazzi, R. Galeazzi et al., "Helicobacterpylori masks differences in homocysteine plasma levels between controls and type 2 diabetic patients," European Journal of Clinical Investigation, vol. 32, no. 3, pp. 158-162, 2002.

[88] C. Colombo, P. A. Tomasi, G. F. Meloni, A. M. Marinaro, A. Ogana, and T. Meloni, "Seroprevalence of Helicobacter pylori in children with type 1 diabetes mellitus in Sardinia," Diabetes, Nutrition & Metabolism, vol. 15, no. 2, pp. 91-95, 2002.

[89] S. Maule, L. Lombardo, C. Rossi et al., "Helicobacter pylori infection and gastric function in primary autonomic neuropathy," Clinical Autonomic Research, vol. 12, no. 3, pp. 193-196, 2002.

[90] J. Zelenkova, A. Souckova, M. Kvapil, A. Soucek, J. Vejvalka, and J. Segethova, "Helicobacter pylori and diabetes mellitus," Casopis lekaru ceskych, vol. 141, no. 18, pp. 575-577, 2002.

[91] G. T. Ko, F. K. Chan, W. B. Chan et al., "Helicobacter pylori infection in Chinese subjects with type 2 diabetes," Endocrine Research, vol. 27, no. 1-2, pp. 171-177, 2001.

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[93] M. Ravera, S. Bahenda, R. Owor, and R. Visona, "Helicobacter pylori infection in diabetic patients with dyspepsia in Uganda," Digestive and Liver Disease, vol. 33, no. 4, pp. 390-391, 2001.

[94] M. Marrollo, G. Latella, D. Melideo et al., "Increased prevalence of Helicobacter pylori in patients with diabetes mellitus," Digestive and Liver Disease, vol. 33, no. 1, pp. 21-29, 2001.

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Jun-Zhen Li, Jie-Yao Li, Ting-Feng Wu, Ji-Hao Xu, Can-Ze Huang, Di Cheng, Qi-Kui Chen, and Tao Yu

Department of Gastroenterology, Sun Yat-Sen Memorial Hospital, Sun Yat-Sen University, 107 Yan JiangXi Road, 510120 Guangzhou, Guangdong, China

Correspondence should be addressed to Qi-Kui Chen; qkchen2015@163.com and Tao Yu; yutao2014@126.com

Received 9 January 2017; Accepted 14 May 2017; Published 13 August 2017

Academic Editor: Paul Enck

Caption: FIGURE 1: Flow diagram of study selection.

Caption: FIGURE 6: Funnel plot of this meta-analysis.

Caption: FIGURE 7: Begg's and Egger's funnel plot of this meta-analysis.

Caption: FIGURE 8: Adjusted funnel plot in the trim and fill method of this meta-analysis.
TABLE 1: Characteristics of the included studies.

Author                       Year     Country         Study design

Han et al. [20]              2016      China        Cross-sectional
Kayar et al. [7]             2015      Turkey         Case-control
Vafaeimanesh et al. [10]     2015       Iran        Cross-sectional
Zhou et al. [14]             2015      China          Case-control
Qiao et al. [45]             2015      China          Case-control
Ji et al. [46]               2015      China          Case-control
Bajaj et al. [9]             2014      India          Case-control
Chobot et al. [47]           2014      Poland         Case-control
Sotuneh et al. [15]          2014       Iran        Cross-sectional
Yang et al. [11]             2014      Taiwan       Cross-sectional
Zhang et al. [48]            2014      China          Case-control
Wei et al. [49]              2014      China          Case-control
Ye and Xu [50]               2014      China          Case-control
Liu et al. [51]              2014      China          Case-control
Zhou et al. [52]             2014      China          Case-control
Wang F and Wang XF [53]      2014      China          Case-control
Bai et al. [54]              2014      China          Case-control
Jia et al. [55]              2014      China          Case-control
Jafarzadeh et al. [56]       2013       Iran        Cross-sectional
Keramat et al. [57]          2013       Iran          Case-control
Xue et al. [58]              2013      China          Case-control
Luo H [59]                   2013      China          Case-control
Candelli et al. [60]         2012      Italy       Prospective cohort
Jeon et al. [32]             2012       USA        Prospective cohort
Oluyemi et al. [61]          2012     Nigeria       Cross-sectional
Hao et al. [62]              2012      China          Case-control
Xu et al. [63]               2012      China          Case-control
El-Eshmawy et al. [40]       2011      Egypt          Case-control
Wan et al. [64]              2011      China          Case-control
Chen et al. [65]             2011      China          Case-control
Agrawal et al. [66]          2010      India          Case-control
Devrajani et al. [8]         2010     Pakistan        Case-control
Ibrahim et al. [44]          2010      Egypt          Case-control
Sfarti et al. [37]           2010     Romania         Case-control
Xu et al. [67]               2010      China          Case-control
Cabral et al. [68]           2009      Brazil         Case-control
Ciortescu et al. [69]        2009     Romania         Case-control
Krause et al. [38]           2009      Israel         Case-control
Lazaraki et al. [70]         2009      Greece         Case-control
Zhang LQ and Zhang MQ [71]   2009      China          Case-control
Yu [72]                      2009      China          Case-control
Ariizumi et al. [73]         2008      Japan          Case-control
Demir et al. [74]            2008      Turkey         Case-control
Hamed et al. [75]            2008      Egypt          Case-control
Nicholas et al. [76]         2008     Nigeria         Case-control
Yan et al. [77]              2008      China          Case-control
Wang et al. [78]             2008      China          Case-control
Ji YF et al. [79]            2008      China          Case-control
Bener et al. [80]            2007      Qatar          Case-control
Sun et al. [81]              2007      China          Case-control
Jaber [82]                   2006   Saudi Arabia      Case-control
Lu et al. [83]               2006      China          Case-control
Gulcelik et al. [84]         2005      Turkey         Case-control
Gillum [85]                  2004       USA         Cross-sectional
Candelli et al. [27]         2003      Italy          Case-control
Anastasios et al. [86]       2002      Greece       Cross-sectional
Cenerelli et al. [87]        2002      Italy          Case-control
Colombo et al. [88]          2002      Italy          Case-control
De Block et al. [36]         2002     Belgium         Case-control
Maule et al. [89]            2002      Italy          Case-control
Zelenkova et al. [90]        2002      Czech          Case-control
Ko et al. [91]               2001      China          Case-control
Ivandic et al. [92]          2001     Croatia         Case-control
Ravera et al. [93]           2001      Uganda         Case-control
Marrollo et al. [94]         2001      Italy          Case-control
Quatrini et al. [95]         2001      Italy          Case-control
Senturk et al. [39]          2001      Turkey         Case-control
Vazeou et al. [96]           2001        UK           Case-control
Xia [97]                     2001    Australia        Case-control
Zhao [98]                    2001      China          Case-control
Arslan et al. [99]           2000      Turkey         Case-control
Dore et al. [100]            2000      Italy          Case-control
Guvener et al. [101]         1999      Turkey         Case-control
Salardi et al. [102]         1999      Italy          Case-control
de Luis et al. [103]         1998      Spain          Case-control
Gasbarrini et al. [104]      1998      Italy          Case-control
Gentile et al. [105]         1998      Italy          Case-control
Pocecco et al. [106]         1997      Italy          Case-control
Mallecki et al. [107]        1996      Poland         Case-control

Author                       Type of DM      Age (years) **

Han et al. [20]                 T2DM       64.1 [+ or -] 8.6
Kayar et al. [7]                T2DM             18-65
Vafaeimanesh et al. [10]        T2DM      52.84 [+ or -] 8.82
Zhou et al. [14]                T2DM       42.4 [+ or -] 9.8
Qiao et al. [45]                T2DM       52.5 [+ or -] 1.7
Ji et al. [46]                  T2DM       51.6 [+ or -] 12.5
Bajaj et al. [9]                T2DM       [greater than or
                                              equal to] 18
Chobot et al. [47]              T1DM       13.4 [+ or -] 3.4
Sotuneh et al. [15]              DM             Elderly
Yang et al. [11]                T2DM       59.6 [+ or -] 10.0
Zhang et al. [48]                DM       52.14 [+ or -] 10.25
Wei et al. [49]                 T2DM      52.79 [+ or -] 12.86
Ye and Xu [50]                  T2DM       54.2 [+ or -] 2.0
Liu et al. [51]                 T2DM             51-65
Zhou et al. [52]                T2DM       57.8 [+ or -] 11.7
Wang F and Wang XF [53]         T2DM       54.6 [+ or -] 1.4
Bai et al. [54]                 T2DM       52.5 [+ or -] 14.2
Jia et al. [55]                  DM        61.0 [+ or -] 10.0
Jafarzadeh et al. [56]           DM       42.86 [+ or -] 6.42
Keramat et al. [57]              DM       51.20 [+ or -] 11.60
Xue et al. [58]                 T2DM      57.03 [+ or -] 11.29
Luo H [59]                       DM        51.5 [+ or -] 4.9
Candelli et al. [60]            T1DM       19.8 [+ or -] 4.3
Jeon et al. [32]                 DM         67.9 (64.1-71.3)
Oluyemi et al. [61]             T2DM       56.4 [+ or -] 10.4
Hao et al. [62]                  DM       47.24 [+ or -] 8.49
Xu et al. [63]                  T2DM      61.0 [+ or -] 10.96
El-Eshmawy et al. [40]          T1DM       19.35 [+ or -] 2.6
Wan et al. [64]                 T2DM       53.4 [+ or -] 1.8
Chen et al. [65]                 DM        53.0 [+ or -] 5.6
Agrawal et al. [66]             T2DM               --
Devrajani et al. [8]            T2DM              >35
Ibrahim et al. [44]             T2DM        45 [+ or -] 5.4
Sfarti et al. [37]              T1DM       49.5 [+ or -] 14.2
Xu et al. [67]                  T2DM       51.5 [+ or -] 13.0
Cabral et al. [68]              T1DM       17.6 [+ or -] 1.5
Ciortescu et al. [69]            DM                --
Krause et al. [38]              T1DM       16.0 [+ or -] 8.7
Lazaraki et al. [70]            T2DM      65.32 [+ or -] 8.56
Zhang LQ and Zhang MQ [71]      T2DM       56.5 [+ or -] 1.1
Yu [72]                         T2DM       52.5 [+ or -] 13.4
Ariizumi et al. [73]             DM        62.5 [+ or -] 11.5
Demir et al. [74]               T2DM        52 [+ or -] 8.2
Hamed et al. [75]                DM        47.65 [+ or -] 1.2
Nicholas et al. [76]            T2DM             29-72
Yan et al. [77]                 T2DM             32-85
Wang et al. [78]                T2DM       47.1 [+ or -] 6.37
Ji YF et al. [79]               T2DM       55.2 [+ or -] 13.5
Bener et al. [80]               T2DM       48.1 [+ or -] 7.9
Sun et al. [81]                 T2DM             35-85
Jaber [82]                      T1DM            Children
Lu et al. [83]                  T2DM       59.4 [+ or -] 11.2
Gulcelik et al. [84]            T2DM       51.9 [+ or -] 10.6
Gillum [85]                      DM              40-74
Candelli et al. [27]            T2DM       14.8 [+ or -] 5.6
Anastasios et al. [86]           DM        61.4 [+ or -] 12.3
Cenerelli et al. [87]           T2DM       55.7 [+ or -] 9.7
Colombo et al. [88]             T1DM            Children
De Block et al. [36]            T1DM         41 [+ or -] 12
Maule et al. [89]               T2DM             46-75
Zelenkova et al. [90]            DM                --
Ko et al. [91]                  T2DM       49.9 [+ or -] 12.0
Ivandic et al. [92]              DM              23-63
Ravera et al. [93]               DM                --
Marrollo et al. [94]             DM                63
Quatrini et al. [95]             DM                58
Senturk et al. [39]             T2DM               --
Vazeou et al. [96]              T1DM              14.5
Xia [97]                         DM        60.7 [+ or -] 13.3
Zhao [98]                       T2DM       59.6 [+ or -] 1.3
Arslan et al. [99]              T1DM            Children
Dore et al. [100]                DM              12-75
Guvener et al. [101]            T2DM               --
Salardi et al. [102]            T1DM               12
de Luis et al. [103]             DM        24.05 [+ or -] 8.3
Gasbarrini et al. [104]          DM          35 [+ or -] 11
Gentile et al. [105]            T2DM         51 [+ or -] 8
Pocecco et al. [106]             DM                16
Mallecki et al. [107]            DM                --

Author                        Method of    NOS
                             detection *

Han et al. [20]                   1         9
Kayar et al. [7]                  2         7
Vafaeimanesh et al. [10]          3         7
Zhou et al. [14]                 3,4        9
Qiao et al. [45]                  1         7
Ji et al. [46]                  1, 3        8
Bajaj et al. [9]               3, 4, 5      8
Chobot et al. [47]                1         7
Sotuneh et al. [15]               3         8
Yang et al. [11]                  5         9
Zhang et al. [48]                 1         7
Wei et al. [49]                   1         7
Ye and Xu [50]                    1         7
Liu et al. [51]                   1         7
Zhou et al. [52]                  1         7
Wang F and Wang XF [53]           1         7
Bai et al. [54]                   1         7
Jia et al. [55]                   1         6
Jafarzadeh et al. [56]            3         7
Keramat et al. [57]            3, 4, 5      8
Xue et al. [58]                   1         7
Luo H [59]                        4         6
Candelli et al. [60]              1         7
Jeon et al. [32]                  3         7
Oluyemi et al. [61]               2         7
Hao et al. [62]                   1         6
Xu et al. [63]                    3         7
El-Eshmawy et al. [40]            3         7
Wan et al. [64]                   1         6
Chen et al. [65]                  1         6
Agrawal et al. [66]               5         7
Devrajani et al. [8]              2         7
Ibrahim et al. [44]            4, 5, 6      6
Sfarti et al. [37]              1,4,5       7
Xu et al. [67]                    1         7
Cabral et al. [68]                5         6
Ciortescu et al. [69]          1, 3, 5      #
Krause et al. [38]                3         6
Lazaraki et al. [70]            4, 5        6
Zhang LQ and Zhang MQ [71]        1         7
Yu [72]                           1         6
Ariizumi et al. [73]           3, 4, 5      6
Demir et al. [74]                 5         6
Hamed et al. [75]                 3         7
Nicholas et al. [76]              3         7
Yan et al. [77]                   1         6
Wang et al. [78]                  5         6
Ji YF et al. [79]                 5         7
Bener et al. [80]                 3         7
Sun et al. [81]                   1         7
Jaber [82]                        3         7
Lu et al. [83]                    3         7
Gulcelik et al. [84]              5         7
Gillum [85]                       3         7
Candelli et al. [27]              1         6
Anastasios et al. [86]            5         6
Cenerelli et al. [87]             1         7
Colombo et al. [88]               3         #
De Block et al. [36]            3, 5        7
Maule et al. [89]                 1         7
Zelenkova et al. [90]             3         #
Ko et al. [91]                    4         6
Ivandic et al. [92]               5         6
Ravera et al. [93]                5         6
Marrollo et al. [94]              5         7
Quatrini et al. [95]              1         7
Senturk et al. [39]             5, 6        #
Vazeou et al. [96]                3         6
Xia [97]                          3         7
Zhao [98]                         1         6
Arslan et al. [99]                3         #
Dore et al. [100]                 3         6
Guvener et al. [101]              5         7
Salardi et al. [102]              3         7
de Luis et al. [103]              3         6
Gasbarrini et al. [104]           1         7
Gentile et al. [105]              5         7
Pocecco et al. [106]              4         6
Mallecki et al. [107]             5         6

NOS: Newcastle-Ottawa scale. ** Mean age or the range of age in DM
group. * 1 = [sup.13]C or [sup.14]C urea breath test, 2 = stool
antigen test, 3 = anti-H. pylori antibody, 4 = rapid urease test, 5 =
histology or biopsy, 6 = culture. (#) Non-English or non-Chinese
article or only abstract available which could not get the full text
for scoring.

FIGURE 2: Forest plot for pooled prevalence of H. pylori infection in
DM group and non-DM group.

                                  DM                Non-DM

Study or subgroup            Events    Total    Events   Total

Han et al. 2016               3254      6395    12,041   24,415
Ji et al. 2015                 83       125       73      142
Zhou et al. 2015              106       188       28       65
Vafaeimanesh et al. 2015      139       211      110      218
Qiao et al. 2015               25        42       9        20
Kayar et al. 2015              40        62       31       71
Bai et al. 2014               102       150       80      150
Yang et al. 2014              147       238      358      729
Chobot et al. 2014             17       149       49      298
Jia et al. 2014                50       100       15       37
Wang F and Wang XF 2014        52        80       40       80
Bajaj et al. 2014              62        80       35       60
Liu et al. 2014               240       281       41       86
Zhou et al. 2014              148       200       71      180
Sotuneh et al. 2014           303       391      688      909
Wei et al. 2014                68       109       51      106
Ye and Xu 2014                 84       110       54      120
Zhang et al. 2014             168       300       62      200
Keramat et al. 2013            58        79       53       84
Xue et al. 2013                79       120       60      120
Jafarzadeh et al. 2013         76       100       76      100
Luo 2013                       36        49       34       62
Candelli et al. 2012           17        69       7        99
Oluyemi et al. 2012            18       100       13      100
Hao et al. 2012               145       227      227      436
Jeon et al. 2012              139       144      580      638
Xu et al. 2012                 58       130       18       50
El-Eshmawy et al. 2011        128       162       41       80
Chen et al. 2011               51        62       43       74
Wan et al. 2011                92       120       59      130
Xu et al. 2010                430       768       65      172
Agrawal et al. 2010            50        80       32       80
Devrajani et al. 2010          54        74       38       74
Ibrahim et al. 2010            53        98       58      102
Sfarti et al. 2010             49        69       25       40
Lazaraki et al. 2009           20        49       12       29
Zhang LQ Zhang MQ 2009        100       160       76      160
Ciortescu et al. 2009          70       100       73      100
Cabral et al. 2009             5         15       17       30
Krause et al. 2009             31        57      113      140
Yu 2009                       135       180       80      150
Demir et al. 2008              87       141       83      142
Hamed et al. 2008              68        80       46       60
Ariizumi et al. 2008           36        67       46       67
Yan et al. 2008               113       150       36       70
Wang et al. 2008               65       103       72      175
Ji YF et al. 2008              81       120       76      110
Nicholas et al. 2008           21        60       17       60
Sun et al. 2007                76       230       54      150
Bener et al. 2007             161       210       5       210
Lu et al. 2006                 74       132      136       24
Jaber 2006                     21        61      128      543
Gulcelik et al. 2005           59        78       33       71
Gillum 2004                   193       366      1628     4218
Candelli et al. 2003           34       121       43      147
Cenerelli et al. 2002          13        30       18       43
Colombo et al. 2002            41       138       45      138
De Block et al. 2002           72       229       42      100
Zelenkova et al. 2002          53       195      110      216
Maule et al. 2002              22        31       15       31
Anastasios et al. 2002         25        67       37      105
Ravera et al. 2001             2         22       8       110
Vazeou et al. 2001             8        118       43      171
Ko et al. 2001                 32        63       31       55
Zhao 2001                     230       370       19      255
Xia et al. 2001               142       429       54      170
Marrollo et al. 2001           48        74       56      117
Quantrini et al. 2001          49        71       33       71
Ivabdic et al. 2001            31        46       8        40
Senturk et al. 2001            59        67       58       72
Arslan et al. 2000             49        88       13       42
Dore et al. 2000              195       385      223      506
Guvener et al. 1999            41        51       14       25
Salardi et al. 1999            18       103       25      236
Gentile et al. 1998           122       164       82      164
de Luis et al. 1998            38        80       34      100
Gasbarrini et al. 1998         43       116       17       50
Pocecco et al. 1997            18        69       17      310
Mallecki et al. 1996           12        39       68      100
Total (95% CI)                         17,187            40,210
Total events                  9434              19108

                                          Odds ratio
Study or subgroup           Weight   M-H, Random, 95% CI     Year

Han et al. 2016              1.7%     1.06 (1.01, 1.12)      2016
Ji et al. 2015               1.4%     1.87 (1.14, 3.07)      2015
Zhou et al. 2015             1.3%     1.71 (0.97, 3.02)      2015
Vafaeimanesh et al. 2015     1.5%     1.90 (1.28, 2.80)      2015
Qiao et al. 2015             0.9%     1.80 (0.61, 5.27)      2015
Kayar et al. 2015            1.2%     2.36 (1.16, 4.73)      2015
Bai et al. 2014              1.4%     1.86 (1.16, 2.97)      2014
Yang et al. 2014             1.6%     1.67 (1.24, 2.26)      2014
Chobot et al. 2014           1.3%     0.65 (0.36. 1.18)      2014
Jia et al. 2014              1.1%     1.47 (0.68, 3.15)      2014
Wang F and Wang XF 2014      1.3%     1.86 (0.98, 3.50)      2014
Bajaj et al. 2014            1.2%     2.46 (1.18, 5.13)      2014
Liu et al. 2014              1.4%     6.42 (3.75, 11.00)     2014
Zhou et al. 2014             1.5%      4.37 (2.83 6.75)      2014
Sotuneh et al. 2014          1.6%     1.11 (0.83, 1.47)      2014
Wei et al. 2014              1.4%     1.79 (1.04, 3.08)      2014
Ye and Xu 2014               1.3%     3.95 (2.24, 6.97)      2014
Zhang et al. 2014            1.5%     2.83 (1.94, 4.13)      2014
Keramat et al. 2013          1.2%     1.62 (0.83, 3.15)      2013
Xue et al. 2013              1.4%     1.93 (1.15, 3.24)      2013
Jafarzadeh et al. 2013       1.3%     1.06 (0.55, 2.01)      2013
Luo 2013                     1.1%     2.28 (1.02, 5.11)      2013
Candelli et al. 2012         1.0%     4.30 (1.67, 11.04)     2012
Oluyemi et al. 2012          1.1%     1.47 (0.68, 3.19)      2012
Hao et al. 2012              1.6%     1.63 (1.17, 2.26)      2012
Jeon et al. 2012             1.0%     2.78 (1.09, 7.06)      2012
Xu et al. 2012               1.2%     1.43 (0.73, 2.81)      2012
El-Eshmawy et al. 2011       1.3%     3.58 (2.01, 6.39)      2011
Chen et al. 2011             1.1%     3.34 (1.50, 7.43)      2011
Wan et al. 2011              1.4%     3.95 (2.29, 6.83)      2011
Xu et al. 2010               1.6%     2.09 (1.49, 2.94)      2010
Agrawal et al. 2010          1.3%     2.50 (1.32, 4.72)      2010
Devrajani et al. 2010        1.2%     2.56 (1.29, 5.08)      2010
Ibrahim et al. 2010          1.4%     0.89 (0.64, 3.35)      2010
Sfarti et al. 2010           1.1%     1.47 (0.64, 3.35)      2010
Lazaraki et al. 2009         1.0%     0.98 (0.38, 2.48)      2009
Zhang LQ Zhang MQ 2009       1.5%     1.84 (1.18, 2.88)      2009
Ciortescu et al. 2009        1.3%     0.86 (0.47, 1.60)      2009
Cabral et al. 2009           07%      0.38 (0.10, 1.39)      2009
Krause et al. 2009           1.2%     0.28 (0.15, 0.56)      2009
Yu 2009                      1.4%     2.63 (1.65, 4.18)      2009
Demir et al. 2008            1.4%     1.15 (0.71, 1.84)      2008
Hamed et al. 2008            1.1%     1.72 (0.73, 4.06)      2008
Ariizumi et al. 2008         1.2%     0.53 (0.26, 1.07)      2008
Yan et al. 2008              1.3%     2.88 (1.59, 5.24)      2008
Wang et al. 2008             1.4%     2.45 (1.48, 4.04)      2008
Ji YF et al. 2008            1.4%     0.93 (0.53, 1.62)      2008
Nicholas et al. 2008         1.1%     1.36 (0.63, 2.95)      2008
Sun et al. 2007              1.5%     0.88 (0.57, 1.35)      2007
Bener et al. 2007            1.5%     1.79 (1.17, 2.74)      2007
Lu et al. 2006               0.9%     4.85 (1.71, 13.76)     2006
Jaber 2006                   1.3%     1.70 (0.97, 2.99)      2006
Gulcelik et al. 2005         1.25     3.58 (1.78, 7.17)      2005
Gillum 2004                  1.6%     1.77 (1.43, 2.20)      2004
Candelli et al. 2003         1.4%     0.95 (0.56, 1.61)      2003
Cenerelli et al. 2002        1.0%     1.06 (0.41, 2.73)      2002
Colombo et al. 2002          1.4%     0.87 (0.52, 1.45)      2002
De Block et al. 2002         1.4%     0.63 (0.39, 1.03)      2002
Zelenkova et al. 2002        1.5%     0.36 (0.24, 0.54)      2002
Maule et al. 2002            0.9%     2.61 (0.91, 7.43)      2002
Anastasios et al. 2002       1.3%     1.09 (0.58, 2.07)      2002
Ravera et al. 2001           0.6%     0.16 (0.03, 0.70)      2001
Vazeou et al. 2001           0.9%     1.48 (0.54, 4.07)      2001
Ko et al. 2001               1.2%     0.80 (0.39, 1.65)      2001
Zhao 2001                    1.4%    20.41 (12.22, 34.07)    2001
Xia et al. 2001              1.5%     1.06 (0.73, 1.55)      2001
Marrollo et al. 2001         1.3%     2.01 (1.10, 3.66)      2001
Quantrini et al. 2001        1.2%     2.56 (1.26, 5.09)      2001
Ivabdic et al. 2001          0.9%     8.27 (3.07, 22.25)     2001
Senturk et al. 2001          1.0%     1.78 (0.69, 4.56)      2001
Arslan et al. 2000           1.1%     2.80 (1.29, 6.10)      2000
Dore et al. 2000             1.6%     1.30 (1.00, 1.70)      2000
Guvener et al. 1999          0.9%     3.22 (1.13, 9.20)      1999
Salardi et al. 1999          1.3%     1.79 (0.93, 3.44)      1999
Gentile et al. 1998          1.4%     2.90 (1.82, 4.63)      1998
de Luis et al. 1998          1.3%     1.76 (0.96, 3.21)      1998
Gasbarrini et al. 1998       1.2%     1.14 (0.57, 2.29)      1998
Pocecco et al. 1997          1.2%     6.08 (2.94, 12.58)     1997
Mallecki et al. 1996         1.1%     0.21 (0.09, 0.47)      1996
Total (95% CI)              100.0%    1.69 [1.47, 1.95]
Total events

Heterogeneity: [[tau].sup.2] = 0.30; [chi square] = 574.28,
df = 78 (P < 0.00001); [I.sup.2] = 86%
Test for overall effect: Z = 7.29 (P < 0.00001)

FIGURE 3: Forest plot for subgroup analysis based on types of DM.

                                   DM                Non-DM

Study or subgroup              Events   Total    Events   Total

T2DM
  Han et al. 2016               3254     6395    12,041   24,415
  Ji et al. 2015                 83      125       73      142
  Vafaeimanesh et al. 2015      139      211      110      218
  Qiao et al. 2015               25       42       9        20
  Zhou et al. 2015              106      188       28       65
  Kayar et al. 2015              40       62       31       71
  Bai et al. 2014               102      150       80      150
  Yang et al. 2014              147      238      358      729
  Bajaj et al. 2014              62       80       35       60
  Wang F and Wang XF 2014        52       80       40       60
  Zhou et al. 2014              148      200       71      180
  Liu et al. 2014               240      281       41       86
  Wei et al. 2014                68      109       51      106
  Ye and Xu 2014                 84      110       51      120
  Xue et al. 2013                79      120       60      120
  Xu et al. 2012                 58      130       18       50
  Oluyemi et al. 2012            18      100       13      100
  Wan et al. 2011                92      120       59      130
  Agrawal et al. 2010            50       80       32       80
  Xu et al. 2010                430      768       65      172
  Ibrahim et al. 2010            53       98       58      102
  Devrajani et al. 2010          54       74       38       74
  Yu 2009                       135      180       80      150
  Zhang LQ and Zhang MQ 2009    100      160       76      160
  Lazaraki et al. 2009           20       49       12       29
  Wang et al. 2008               65      103       72      175
  Yan et al. 2008               113      150       36       70
  Nicholas et al. 2008           21       60       17       60
  Ji YF et al. 2008              81      120       76      110
  Demir et al. 2008              87      141       83      142
  Bener et al. 2007             161      210      136      210
  Sun et al. 2007                76      230       54      150
  Lu et al. 2006                 74      132       5        24
  Gulcelik et al. 2005           59       78       33       71
  Candelli et al. 2003           34      121       43      147
  Maule et al. 2002              22       31       15       31
  Cenerelli et al. 2002          13       30       18       43
  Zhao 2001                     230      370       19      255
  Ko et al. 2001                 32       63       31       55
  Senturk et al. 2001            59       67       58       72
  Guvener et al. 1999            41       51       14       25
  Gentile et al. 1998           122      164       82      164

Total (95% CI)                          12,271            29,413
Total events                    6929             14,325

Heterogeneity: [[tau].sup.2] = 0.36; [chi square] = 361.48,
df = 41 (P < 0.00001); [I.sup.2] = 89%
Test for overall effect: Z = 6.89 (P < 0.00001)

T1DM
  Chobot et al. 2014             17      149       49      298
  Candelli et al. 2012           17       69       7        99
  EI-Eshmawy et al. 2011        128      162       41       80
  Sfarti et al. 2010             49       69       25       40
  Krause et al. 2009             31       57      113      140
  Cabral et al. 2009             5        15       17       30
  Jaber 2006                     21       61      128      543
  De Block et al. 2002           72      299       42      100
  Colombo et al. 2002            41      138       45      138
  Vazeou et al. 2001             8       118       8       171
  Arslan et al. 2000             49       88       13       42
  Salardi et al. 1999            18      103       25      236

Total (95% CI)                           1258              1917
Total events                    456               513

Heterogeneity: [[tau].sup.2] = 0.53; [chi square] = 61.39,
df = 11 (P < 0.00001); [I.sup.2] = 82%
Test for overall effect: Z = 0.87(P = 0.38)

                                             Odds ratio
Study or subgroup              Weight   M-H, Random, 95% CI    Year

T2DM
  Han et al. 2016               3.0%     1.06 (1.01, 1.12)     2016
  Ji et al. 2015                2.6%     1.87 (1.14, 3.07)     2015
  Vafaeimanesh et al. 2015      2.7%     1.90 (1.28, 2.80)     2015
  Qiao et al. 2015              1.7%     1.80 (0.61, 5.27)     2015
  Zhou et al. 2015              2.5%     1.71 (0.97, 3.02)     2015
  Kayar et al. 2015             2.2%     2.35 (1.16, 4.73)     2015
  Bai et al. 2014               2.6%     1.86 (1.16, 2.97)     2014
  Yang et al. 2014              2.9%     1.67 (1.24, 2.26)     2014
  Bajaj et al. 2014             2.2%     2.46 (1.18, 5.13)     2014
  Wang F and Wang XF 2014       2.4%     1.86 (0.98, 3.50)     2014
  Zhou et al. 2014              2.7%     4.37 (2.83, 6.75)     2014
  Liu et al. 2014               2.5%     6.42 (3.75, 11.00)    2014
  Wei et al. 2014               2.5%     1.79 (1.04, 3.08)     2014
  Ye and Xu 2014                2.5%     3.95 (2.24, 6.97)     2014
  Xue et al. 2013               2.5%     1.93 (1.15, 3.24)     2013
  Xu et al. 2012                2.3%     1.43 (0.73, 2.81)     2012
  Oluyemi et al. 2012           2.1%     1.47 (0.68, 3.19)     2012
  Wan et al. 2011               2.5%     3.95 (2.29, 6.83)     2011
  Agrawal et al. 2010           2.4%     2.50 (1.32, 4.72)     2010
  Xu et al. 2010                2.8%     2.09 (1.49, 2.94)     2010
  Ibrahim et al. 2010           2.5%     0.89 (0.51, 1.56)     2010
  Devrajani et al. 2010         2.3%     2.56 (1.29, 5.08)     2010
  Yu 2009                       2.6%     2.63 (1.65, 4.18)     2009
  Zhang LQ and Zhang MQ 2009    2.7%     1.84 (1.18, 2.88)     2009
  Lazaraki et al. 2009          1.9%     0.98 (0.38, 2.48)     2009
  Wang et al. 2008              2.6%     2.45 (1.48, 4.04)     2008
  Yan et al. 2008               2.4%     2.88 (1.59, 5.24)     2008
  Nicholas et al. 2008          2.1%     1.36 (0.63, 2.95)     2008
  Ji YF et al. 2008             2.5%     0.93 (0.53, 1.62)     2008
  Demir et al. 2008             2.6%     1.15 (0.71, 1.84)     2008
  Bener et al. 2007             2.7%     1.79 (1.17, 2.74)     2007
  Sun et al. 2007               2.7%     0.88 (0.57, 1.35)     2007
  Lu et al. 2006                1.7%     4.85 (1.71, 13.76)    2006
  Gulcelik et al. 2005          2.3%     3.58 (1.78, 7.17)     2005
  Candelli et al. 2003          2.5%     0.95 (0.56, 1.61)     2003
  Maule et al. 2002             1.7%     2.61 (0.91, 7.43)     2002
  Cenerelli et al. 2002         1.8%     1.06 (0.41, 2.73)     2002
  Zhao 2001                     2.6%    20.41 (12.22, 34.07)   2001
  Ko et al. 2001                2.2%     0.80 (0.39, 1.65)     2001
  Senturk et al. 2001           1.9%     1.78 (0.69, 4.56)     2001
  Guvener et al. 1999           1.7%      3.2 (1.13, 9.20)     1999
  Gentile et al. 1998           2.6%     2.90 (1.82, 4.63)     1998

Total (95% CI)                 100.0%    2.05 (1.67, 2.52)
Total events

Heterogeneity: [[tau].sup.2] = 0.36; [chi square] = 361.48,
df = 41 (P < 0.00001); [I.sup.2] = 89%
Test for overall effect: Z = 6.89 (P < 0.00001)

T1DM
  Chobot et al. 2014            9.0%     0.65 (0.36, 1.18)     2014
  Candelli et al. 2012          7.4%     4.30 (1.67, 11.04)    2012
  EI-Eshmawy et al. 2011        9.1%     3.58 (2.01, 6.39)     2011
  Sfarti et al. 2010            7.9%     1.47 (0.64, 3.35)     2010
  Krause et al. 2009            8.7%     0.28 (0.15, 0.56)     2009
  Cabral et al. 2009            5.8%     0.38 (0.10, 1.39)     2009
  Jaber 2006                    9.2%     1.70 (0.97, 2.99)     2006
  De Block et al. 2002          9.5%     0.63 (0.39, 1.03)     2002
  Colombo et al. 2002           9.4%     1.87 (0.52, 1.45)     2002
  Vazeou et al. 2001            7.1%     1.48 (0.54, 4.07)     2001
  Arslan et al. 2000            8.2%     2.80 (1.29, 6.10)     2000
  Salardi et al. 1999           8.7%     1.79 (0.93, 3.44)     1999

Total (95% CI)                 100.0%    1.23 [0.77, 1.96]
Total events

Heterogeneity: [[tau].sup.2] = 0.53; [chi square] = 61.39,
df = 11 (P < 0.00001); [I.sup.2] = 82%
Test for overall effect: Z = 0.87(P = 0.38)

FIGURE 4: Forest plot for subgroup analysis based on geographic
regions. (India, Japan, China, Qatar, Pakistan, Saudi Arabia Iran,
Hong Kong, and Taiwan were included in group Asia. Greece, Turkey,
Italy, Poland, Romania, Belgium, Spain, Croatia, Israel, UK, and Czech
Republic were included in group Europe, as well as Australia because
it comprises similar races and people who lived in similar lifestyle
with these countries. Brazil and USA were included in group America.
Egypt and Nigeria were included in group Africa.)

                                    DM             Non-DM

Study or subgroup             Events   Total    Events   Total

Asia
  Han et al. 2016              3254     6395    12,041   24,415
  JI et al. 2015                83      125       73      142
  Qiao et al. 2015              25       42       9        20
  Zhou et al. 2015             106      188       28       65
  Vafaeimanesh et al. 2015     139      211      110      218
  Zhang et al. 2014            168      300       62      200
  Bai et al. 2014              102      150       80      150
  Ye and Xu 2014                84      110       54      120
  Wei et al. 2014               68      109       51      106
  Yang et al. 2014             147      238      358      729
  Sotuneh et al. 2014          303      391      688      909
  Jia et al. 2014               50      100       15       37
  Zhou et al. 2014             148      200       71      180
  Liu et al. 2014              240      281       41       86
  Bajaj et al. 2014             62       80       35       60
  Wang F and Wang XF 2014       52       80       40       80
  Luo 2013                      36       49       34       62
  Xue et al. 2013               79      120       60      120
  Jafarzadeh et al. 2013        76      100       75      100
  Keramat et al. 2013           58       79       53       84
  Xu et al. 2012                58      130       18       50
  Hao et al. 2012              145      227      227      436
  Wan et al. 2011               92      120       59      130
  Chen et al. 2011              51       62       43       74
  Devrajani et al. 2010         54       74       38       74
  Xu et al. 2010               430      768       65      172
  Agrawal et al. 2010           50       80       32       80
  Yu 2009                      135      180       80      150
  Zhang LQ Zhang MQ 2009       100      160       76      160
  Yan et al. 2008              113      150       36       70
  Ji YF et al. 2008             81      120       76      110
  Ariizumi et al. 2008          36       67       46       67
  Wang et al. 2008              65      103       72      175
  Sun et al. 2007               76      230       54      150
  Bener et al. 2007            161      210      136      210
  Lu et al. 2006                74      132       5        24
  Jaber 2006                    21       61      128      543
  Ko et al. 2001                32       63       31       55
  Zhao 2001                    230      370       19      255

Total (95% CI)                         12,655            30,868
Total events                   7284             15,219

Heterogeneity: [[tau].sup.2] = 0.33; [chi square] = 364.85,
df = 38(P < 0.00001); [I.sup.2] = 90%
Test for overall effect: Z = 6.92 (P < 0.00001)

Africa
  Oluyemi et al. 2012           18      100       13      100
  El-Eshmawy et al. 2011       128      162       41       80
  Ibrahim et al. 2010           53       98       58      102
  Hamed et al. 2008             68       80       46       60
  Nicholas et al. 2008          21       60       17       60
  Ravera et al. 2001            2        22       43      110

Total (95% CI)                          522               512
Total events                   290               218

Heterogeneity: [[tau].sup.2] = 0.47; [chi square] = 21.12,
df = 5 (P = 0.00008); [I.sup.2] = 76%
Test for overall effect: Z = 0.75(P = 0.46)

Europe
  Kayar et al. 2015             40       62       31       71
  Chobot et al. 2014            17      149       49      298
  Candelli et al. 2012          17       69       7        99
  Sfarti et al. 2010            49       69       25       40
  Ciortescu et al. 2009         70      100       73      100
  Krause et al. 2009            31       57      113      140
  Lazaraki et al. 2009          20       49       12       29
  Demir et al. 2008             87      141       83      142
  Gulcelik et al. 2005          59       78       33       71
  Candelli et al. 2003          34      121       43      147
  Cenerelli et al. 2002         13       30       18       43
  Colombo et al. 2002           41      138       45      138
  De Block et al. 2002          72      229       42      100
  Zelenkova et al. 2002         53      195      110      216
  Anastasios et al. 2002        25       67       37      105
  Maule et al. 2002             22       31       15       31
  Marrollo et al. 2001          48       74       56      117
  Xia et al. 2001              142      429       54      170
  Ivabdic et al. 2001           31       46       8        40
  Quatrini et al. 2001          49       71       33       71
  Vazeou et al. 2001            8       118       8       171
  Senturk et al. 2001           59       67       58       72
  Dore et al. 2000             195      385      223      506
  Arslan et al. 2000            49       88       13       42
  Guvener et al. 1999           41       51       14       25
  Salardi et al. 1999           18      103       25      236
  Gasbarrini et al. 1998        43      116       17       50
  de Luis et al. 1998           38       80       34      100
  Gentile et al. 1998          122      164       82      164
  Pocecco et al. 1997           18       69       17      310
  Mallecki et al. 1996          12       39       68      100

Total (95% Cl)                          3485              3944
Total events                   1523              1446

Heterogeneity: [[tau].sup.2] = 0.44; [chi square] = 173.06,
df = 30 (P < 0.00001); [I.sup.2] = 83%
Test for overall effect: Z = 2.45 (P = 0.01)

America
  Jeon et al. 2012             139      144      580      638
  Cabral et al. 2009            5        15       17       30
  Gillum 2004                  193      366      1628     4218

Total (95% CI)                          525               4886
Total events                   337               2225

Heterogeneity: [[tau].sup.2] = 0.34; [chi square] = 6.27,
df = 2 (P = 0.04); [I.sup.2] = 68%
Test for overall effect: Z = 0.91 (P = 0.36)

                                            Odds ratio
Study or subgroup             Weight   M-H, Random, 95% CI     Year

Asia
  Han et al. 2016              3.2%     1.06 (1.01, 1.12)      2016
  JI et al. 2015               2.7%     1.87 (1.14, 3.07)      2015
  Qiao et al. 2015             1.7%     1.80 (0.61, 5.27)      2015
  Zhou et al. 2015             2.6%     1.71 (0.97, 3.02)      2015
  Vafaeimanesh et al. 2015     2.9%     1.90 (1.28, 2.80)      2015
  Zhang et al. 2014            2.9%     2.83 (1.94, 4.13)      2014
  Bai et al. 2014              2.7%     1.86 (1.16, 2.97)      2014
  Ye and Xu 2014               2.6%     3.95 (2.24, 6.97)      2014
  Wei et al. 2014              2.6%     1.79 (1.04, 3.08)      2014
  Yang et al. 2014             3.0%     1.67 (1.24, 2.26)      2014
  Sotuneh et al. 2014          3.0%     1.11 (0.83, 1.47)      2014
  Jia et al. 2014              2.2%     1.47 (0.68, 3.15)      2014
  Zhou et al. 2014             2.8%     4.37 (2.83, 6.75)      2014
  Liu et al. 2014              2.6%     6.42 (3.75, 11.00)     2014
  Bajaj et al. 2014            2.3%     2.46 (1.18, 5.13)      2014
  Wang F and Wang XF 2014      2.4%     1.86 (0.98, 3.50)      2014
  Luo 2013                     2.1%     2.28 (1.02, 5.11)      2013
  Xue et al. 2013              2.7%     1.93 (1.15, 3.24)      2013
  Jafarzadeh et al. 2013       2.4%     1.06 (0.55, 2.01)      2013
  Keramat et al. 2013          2.4%     1.62 (0.83, 3.15)      2013
  Xu et al. 2012               2.4%     1.43 (0.73, 2.81)      2012
  Hao et al. 2012              3.0%     1.63 (1.17, 2.26)      2012
  Wan et al. 2011              2.6%     3.95 (2.29, 6.83)      2011
  Chen et al. 2011             2.1%     3.34 (1.50, 7.43)      2011
  Devrajani et al. 2010        2.3%     2.56 (1.29, 5.08)      2010
  Xu et al. 2010               2.9%     2.09 (1.49, 2.94)      2010
  Agrawal et al. 2010          2.4%     2.50 (1.32, 4.72)      2010
  Yu 2009                      2.7%     2.63 (1.65, 4.18)      2009
  Zhang LQ Zhang MQ 2009       2.8%     1.84 (1.18, 2.88)      2009
  Yan et al. 2008              2.5%     2.88 (1.59, 5.24)      2008
  Ji YF et al. 2008            2.6%     0.93 (0.53, 1.62)      2008
  Ariizumi et al. 2008         2.3%     0.53 (0.26, 1.07)      2008
  Wang et al. 2008             2.7%     2.45 (1.48, 4.04)      2008
  Sun et al. 2007              2.8%     0.88 (0.57, 1.35)      2007
  Bener et al. 2007            2.8%     1.79 (1.17, 2.74)      2007
  Lu et al. 2006               1.7%     4.85 (1.71, 13.76)     2006
  Jaber 2006                   2.6%     1.70 (0.97, 2.99)      2006
  Ko et al. 2001               2.3%     0.80 (0.39, 1.65)      2001
  Zhao 2001                    2.7%    20.41 (12.22, 34.07)    2001

Total (95% CI)                100.0%    2.04 [1.67, 2.50]
Total events

Heterogeneity: [[tau].sup.2] = 0.33; [chi square] = 364.85,
df = 38(P < 0.00001); [I.sup.2] = 90%
Test for overall effect: Z = 6.92 (P < 0.00001)

Africa
  Oluyemi et al. 2012         17.2%     1.47 (0.68, 3.19)      2012
  El-Eshmawy et al. 2011      19.4%     3.58 (2.01, 6.39)      2011
  Ibrahim et al. 2010         19.6%     0.89 (0.51, 1.56)      2010
  Hamed et al. 2008           16.3%     1.72 (0.73, 4.06)      2008
  Nicholas et al. 2008        17.3%     1.36 (0.63, 2.95)      2008
  Ravera et al. 2001          10.2%     0.16 (0.03, 0.70)      2001

Total (95% CI)                100.0%    1.28 [0.67, 2.43]
Total events

Heterogeneity: [[tau].sup.2] = 0.47; [chi square] = 21.12,
df = 5 (P = 0.00008); [I.sup.2] = 76%
Test for overall effect: Z = 0.75(P = 0.46)

Europe
  Kayar et al. 2015            3.2%     2.35 (1.16, 4.73)      2015
  Chobot et al. 2014           3.5%     0.65 (0.36, 1.18)      2014
  Candelli et al. 2012         2.7%     4.30 (1.67, 11.04)     2012
  Sfarti et al. 2010           3.0%     1.47 (0.64, 3.35)      2010
  Ciortescu et al. 2009        3.4%     0.86 (0.47, 1.60)      2009
  Krause et al. 2009           3.3%     0.28 (0.15, 0.56)      2009
  Lazaraki et al. 2009         2.8%     0.98 (0.38, 2.48)      2009
  Demir et al. 2008            3.7%     1.15 (0.71, 1.84)      2008
  Gulcelik et al. 2005         3.2%     3.58 (1.78, 7.17)      2005
  Candelli et al. 2003         3.6%     0.95 (0.56, 1.61)      2003
  Cenerelli et al. 2002        2.7%     1.06 (0.41, 2.73)      2002
  Colombo et al. 2002          3.6%     0.87 (0.52, 1.45)      2002
  De Block et al. 2002         3.7%     0.63 (0.39, 1.03)      2002
  Zelenkova et al. 2002        3.8%     0.36 (0.24, 0.54)      2002
  Anastasios et al. 2002       3.4%     1.09 (0.58, 2.07)      2002
  Maule et al. 2002            2.5%     2.61 (0.91, 7.43)      2002
  Marrollo et al. 2001         3.4%     2.01 (1.10, 3.66)      2001
  Xia et al. 2001              3.8%     1.06 (0.73, 1.55)      2001
  Ivabdic et al. 2001          2.6%     8.27 (3.07, 22.25)     2001
  Quatrini et al. 2001         3.3%     2.56 (1.29, 5.09)      2001
  Vazeou et al. 2001           2.6%     1.48 (0.54, 4.07)      2001
  Senturk et al. 2001          2.7%     1.78 (0.69, 4.56)      2001
  Dore et al. 2000             4.0%     1.30 (1.00, 1.70)      2000
  Arslan et al. 2000           3.1%     2.80 (1.29, 6.10)      2000
  Guvener et al. 1999          2.5%     3.22 (1.13, 9.20)      1999
  Salardi et al. 1999          3.3%     1.79 (0.93, 3.44)      1999
  Gasbarrini et al. 1998       3.2%     1.14 (0.57, 2.29)      1998
  de Luis et al. 1998          3.4%     1.76 (0.96, 3.21)      1998
  Gentile et al. 1998          3.7%     2.90 (1.82, 4.63)      1998
  Pocecco et al. 1997          3.2%     6.08 (2.94, 12.58)     1997
  Mallecki et al. 1996         3.0%     0.21 (0.09, 0.47)     1996 *

Total (95% Cl)                100.0%    1.40 [1.07, 1.82]
Total events

Heterogeneity: [[tau].sup.2] = 0.44; [chi square] = 173.06,
df = 30 (P < 0.00001); [I.sup.2] = 83%
Test for overall effect: Z = 2.45 (P = 0.01)

America
  Jeon et al. 2012            29.9%     2.78 (1.09, 7.06)      2012
  Cabral et al. 2009          21.8%     0.38 (0.10, 1.39)      2009
  Gillum 2004                 48.3%     1.77 (1.43, 2.20)      2004

Total (95% CI)                100.0%    1.45 [0.65, 3.25]
Total events

Heterogeneity: [[tau].sup.2] = 0.34; [chi square] = 6.27,
df = 2 (P = 0.04); [I.sup.2] = 68%
Test for overall effect: Z = 0.91 (P = 0.36)

FIGURE 5: Forest plot for subgroup analysis of methods for
H. pylori detection.

                                     DM              Non-DM

Study or subgroup              Events   Total    Events   Total

Current infection group
  Han et al. 2016               3254     6395    12,041   24,415
  Qiao et al. 2015               25       42       9        20
  Kayar et al. 2015              40       62       31       71
  Liu et al. 2014               240      281       41       86
  Zhou et al. 2014              148      200       71      180
  Bai et al. 2014               102      150       80      150
  Yang et al. 2014              147      238      358      729
  Chobot et al. 2014             17      149       49      298
  Jia et al. 2014                50      100       15       37
  Wang et al. 2014               52       80       40       80
  Zhang et al. 2014             168      300       62      200
  Ye and Xu. 2014                84      110       54      120
  Wei et al. 2014                68      109       51      106
  Xue et al. 2013                79      120       60      120
  Luo 2013                       36       49       34       62
  Hao et al. 2012               145      227      227      436
  Oluyemi et al. 2012            18      100       13      100
  Candelli et al. 2012           17       69       7        99
  Wan et al. 2011                92      120       59      130
  Chen et al. 2011               51       62       43       74
  Sfarti et al. 2010             49       69       25       40
  Ibrahim et al. 2010            53       98       58      102
  Xu 2010                       430      768       65      172
  Devrajani et al. 2010          54       74       38       74
  Agrawal et al. 2010            50       80       32       80
  Cabral et al. 2009             5        15       17       30
  Yu 2009                       135      180       80      150
  Zhang LQ and Zhang MQ 2009    100      160       76      160
  Lazaraki et al. 2009           20       49       12       29
  Demir et al. 2008              87      141       83      142
  Yan et al. 2008               113      150       36       70
  Wang et al. 2008               65      103       72      175
  Ji YF et al. 2008              81      120       76      110
  Sun et al. 2007                76      230       54      150
  Gulcelik et al. 2005           59       78       33       71
  Candelli et al. 2003           34      121       43      147
  Cenerelli et al. 2002          13       30       18       43
  Maule et al. 2002              22       31       15       31
  Anastasios et al. 2002         25       67       37      105
  Zhao 2001                     230      370       19      255
  Ravera et al. 2001             2        22       43      110
  Ko et al. 2001                 32       63       31       55
  Marrollo et al. 2001           48       74       56      117
  Senturk et al. 2001            59       67       58       72
  Quatrini et al. 2001           49       71       33       71
  Ivabdic et al. 2001            31       46       8        40
  Guvener et al. 1999            41       51       14       25
  Gasbarrini et al. 1998         43      116       17       50
  Gentile et al. 1998           122      164       82      164
  Pocecco et al. 1997            18       69       17      310
  Mallecki et al. 1996           12       39       68      100

Total (95% CI)                          12,679            30,763
Total events                    6991             14,661

Heterogeneity: [[tau].sup.2] = 0.40; [chi square] = 448.56,
df = 50(P < 0.00001); [I.sup.2] = 89%
Test for overall effect: Z = 6.44 (P < 0.00001)

Serological test group

  Vafaeimanesh et al. 2015      139      211      110      218
  Sotuneh et al. 2014           303      391      688      909
  Jafarzadeh et al. 2013         76      100       75      100
  Xu et al. 2012                 58      130       18       50
  Jeon et al. 2012              139      144      580      638
  EI-Eshmawy et al. 2011        128      162       41       80
  Krause et al. 2009             31       57      113      140
  Hamed et al. 2008              68       80       46       60
  Nicholas et al. 2008           21       60       17       60
  Bener et al. 2007             161      210      136      210
  Jaber 2006                     21       61      128      543
  Lu et al. 2006                 74      132       5        24
  Gillum et al. 2004            193      366      1628     4218
  Colombo et al. 2002            41      138       45      138
  Zelenkova et al. 2002          53      195      110      216
  Vazeou et al. 2001             8       118       8       171
  Xia et al. 2001               142      429       54      170
  Arslan et al. 2000             49       88       13       42
  Dore et al. 2000              195      385      223      506
  Salardi et al. 1999            18      103       25      236
  de Luis et al. 1998            38       80       34      100

Total (95% CI)                           3640              8829
Total events                    1956              4097

Heterogeneity: [[tau].sup.2] = 0.23; [chi square] = 102.67,
df = 20(P < 0.00001); [I.sup.2] = 81%
Test for overall effect: Z = 2.71 (P = 0.007)

                                        Odds ratio
Study or subgroup              Weight   M-H, Random, 95% CI    Year

Current infection group
  Han et al. 2016               2.5%     1.06 (1.01, 1.12)     2016
  Qiao et al. 2015              1.5%     1.80 (0.61, 5.27)     2015
  Kayar et al. 2015             1.9%     2.35 (1.16, 4.73)     2015
  Liu et al. 2014               2.1%     6.42 (3.75, 11.00)    2014
  Zhou et al. 2014              2.3%     4.37 (2.83, 6.75)     2014
  Bai et al. 2014               2.2%     1.86 (1.16, 2.97)     2014
  Yang et al. 2014              2.4%     1.67 (1.24, 2.26)     2014
  Chobot et al. 2014            2.1%     0.65 (0.36, 1.18)     2014
  Jia et al. 2014               1.8%     1.47 (0.68, 3.15)     2014
  Wang et al. 2014              2.0%     1.86 (0.98, 3.50)     2014
  Zhang et al. 2014             2.3%     2.83 (1.94, 4.13)     2014
  Ye and Xu. 2014               2.1%     3.95 (2.24, 6.97)     2014
  Wei et al. 2014               2.1%     1.79 (1.04, 3.08)     2014
  Xue et al. 2013               2.2%     1.93 (1.15, 3.24)     2013
  Luo 2013                      1.8%     2.28 (1.02, 5.11)     2013
  Hao et al. 2012               2.4%     1.63 (1.17, 2.26)     2012
  Oluyemi et al. 2012           1.8%     1.47 (0.68, 3.19)     2012
  Candelli et al. 2012          1.6%     4.30 (1.67, 11.04)    2012
  Wan et al. 2011               2.1%     3.95 (2.29, 6.83)     2011
  Chen et al. 2011              1.8%     3.34 ([1.50, 7.43)    2011
  Sfarti et al. 2010            1.8%     1.47 (0.64, 3.35)     2010
  Ibrahim et al. 2010           2.1%     0.89 (0.51, 1.56)     2010
  Xu 2010                       2.4%     2.09 (1.49, 2.94)     2010
  Devrajani et al. 2010         1.9%     2.56 (1.29, 5.08)     2010
  Agrawal et al. 2010           2.0%     2.50 (1.32, 4.72)     2010
  Cabral et al. 2009            1.2%     0.38 (0.10, 1.39)     2009
  Yu 2009                       2.2%     2.63 (1.65, 4.18)     2009
  Zhang LQ and Zhang MQ 2009    2.2%     1.84 (1.18, 2.88)     2009
  Lazaraki et al. 2009          1.6%     0.98 (0.38, 2.48)     2009
  Demir et al. 2008             2.2%     1.15 (0.71, 1.84)     2008
  Yan et al. 2008               2.1%     2.88 (1.59, 5.24)     2008
  Wang et al. 2008              2.2%     2.45 (1.48, 4.04)     2008
  Ji YF et al. 2008             2.1%     0.93 (0.53, 1.62)     2008
  Sun et al. 2007               2.3%     0.88 (0.57, 1.35)     2007
  Gulcelik et al. 2005          1.9%     3.58 (1.78, 7.17)     2005
  Candelli et al. 2003          2.1%     0.95 (0.56, 1.61)     2003
  Cenerelli et al. 2002         1.6%     1.06 (0.41, 2.73)     2002
  Maule et al. 2002             1.5%     2.61 (0.91, 7.43)     2002
  Anastasios et al. 2002        2.0%     1.09 (0.58, 2.07)     2002
  Zhao 2001                     2.2%    20.41 (12.22, 34.07)   2001
  Ravera et al. 2001            1.0%     0.16 (0.03, 0.70)     2001
  Ko et al. 2001                1.9%     0.80 (0.39, 1.65)     2001
  Marrollo et al. 2001          2.1%     2.01 (1.10, 3.66)     2001
  Senturk et al. 2001           1.6%     1.78 (0.69, 4.56)     2001
  Quatrini et al. 2001          1.9%     2.56 (1.29, 5.09)     2001
  Ivabdic et al. 2001           1.6%     8.27 (3.07, 22.25)    2001
  Guvener et al. 1999           1.5%     3.22 (1.13, 9.20)     1999
  Gasbarrini et al. 1998        1.9%     1.14 (0.57, 2.29)     1998
  Gentile et al. 1998           2.2%     2.90 (1.82, 4.63)     1998
  Pocecco et al. 1997           1.9%     6.08 (2.94, 12.58)    1997
  Mallecki et al. 1996          1.8%     0.21 (0.09, 0.47)     1996

Total (95% CI)                 100.0%    1.92 [1.57, 2.34]
Total events

Heterogeneity: [[tau].sup.2] = 0.40; [chi square] = 448.56,
df = 50(P < 0.00001); [I.sup.2] = 89%
Test for overall effect: Z = 6.44 (P < 0.00001)

Serological test group

  Vafaeimanesh et al. 2015      5.7%     1.90 (1.28, 2.80)     2015
  Sotuneh et al. 2014           6.1%     1.11 (0.83, 1.47)     2014
  Jafarzadeh et al. 2013        4.6%     1.06 (0.55, 2.01)     2013
  Xu et al. 2012                4.4%     1.43 (0.73, 2.81)     2012
  Jeon et al. 2012              3.4%     2.78 (1.09, 7.06)     2012
  EI-Eshmawy et al. 2011        4.9%     3.58 (2.01, 6.39)     2011
  Krause et al. 2009            4.4%     0.28 (0.15, 0.56)     2009
  Hamed et al. 2008             3.7%     1.72 (0.73, 4.06)     2008
  Nicholas et al. 2008          4.0%     1.36 (0.36, 2.95)     2008
  Bener et al. 2007             5.5%     1.79 (1.17, 2.74)     2007
  Jaber 2006                    4.9%     1.70 (0.97, 2.99)     2006
  Lu et al. 2006                3.0%     4.85 (1.71, 13.76)    2006
  Gillum et al. 2004            6.3%     1.77 (1.43, 2.20)     2004
  Colombo et al. 2002           5.2%     0.87 (0.52, 1.45)     2002
  Zelenkova et al. 2002         5.6%     0.36 (0.24, 0.54)     2002
  Vazeou et al. 2001            3.1%     1.48 (0.54, 4.07)     2001
  Xia et al. 2001               5.7%     1.06 (0.73, 1.55)     2001
  Arslan et al. 2000            4.0%     2.80 (1.29, 6.10)     2000
  Dore et al. 2000              6.2%     1.30 (1.00, 1.70)     2000
  Salardi et al. 1999           4.5%     1.79 (0.93, 3.44)     1999
  de Luis et al. 1998           4.7%     1.76 (0.96, 3.21)     1998

Total (95% CI)                 100.0%    1.40 [1.10, 1.79]
Total events

Heterogeneity: [[tau].sup.2] = 0.23; [chi square] = 102.67,
df = 20(P < 0.00001); [I.sup.2] = 81%
Test for overall effect: Z = 2.71 (P = 0.007)
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Author:Li, Jun-Zhen; Li, Jie-Yao; Wu, Ting-Feng; Xu, Ji-Hao; Huang, Can-Ze; Cheng, Di; Chen, Qi-Kui; Yu, Ta
Publication:Gastroenterology Research and Practice
Article Type:Report
Date:Jan 1, 2017
Words:16150
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