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. 2022 Mar 1;33(3):205–212. doi: 10.5152/tjg.2022.21360

Is Helicobacter pylori Infection Associated with Celiac Disease? A Meta-analysis

Min Yue 1, Qiang Chen 1, Xinxin Zhou 1, Lan Li 1, Chao Lu 1,✉
PMCID: PMC9128522  PMID: 35115283

Abstract

Background

Some studies have reported the correlation between Helicobacter pylori and celiac disease (CD), but the results lack consistency. This meta-analysis aimed to quantify the relationship between H. pylori and CD. In addition, the study also analyzed the impact of H. pylori on the symptoms and classification of CD.

Methods

Studies published up to September 1, 2020 on 3 databases – EMBASE, MEDICINE, and PubMed – were searched. The statistical data of articles which met the requirements were collated and extracted.

Results

Twenty-five papers and 141 355 participants were finally enrolled. The results showed that the H. pylori infection rate of CD patients was 0.57 times greater compared to controls (OR = 0.57, 95% CI [0.44, 0.75]), while statistical differences were also seen in the subgroups of children (OR = 0.53, 95% CI [0.33, 0.85]) and adults (OR = 0.63, 95% CI [0.49, 0.81]). Furthermore, patients having CD with H. pylori were more likely to have symptoms of abdominal pain, diarrhea, and distension (OR = 2.5, 95% CI [1.35, 4.62]) (OR = 1.56, 95% CI [1.09, 2.24]) (OR = 2.75, 95% CI [1.74, 4.35]). However, H. pylori has no effect on CD classification.

Conclusion

The study confirmed that there is a correlation between H. pylori and CD, but the causality cannot be clarified. A demonstration of a causal role of H. pylori in CD in future prospective studies could have important therapeutic implications.

Keywords: Celiac disease, Helicobacter pylori

Main Points

  1. This study aimed to quantify the relationship between Helicobacter pylori and CD by meta-analysis.

  2. The results showed that the H. pylori infection rate of CD patients was lower than that of controls.

  3. Patients having CD with H. pylori were more likely to have symptoms of abdominal pain, diarrhea, and distension.

Introduction

Celiac disease (CD) is an inherited autoimmune disease that occurs in the small intestine.1 Almost 99% of the patients have HLA DR3-DQ2 and/or DR4-DQ8, compared with approximately 40% of the general population.2 Celiac disease is a chronic condition, and clinical manifestations can involve the intestinal and extra-intestinal areas, which is one of the reasons for widespread concern.3 Celiac disease affects approximately 0.5-1% of the global population, with a female predominance accompanying the increase in morbidity, including a 2- to 4.5-fold increase over approximately 20-50 years in the Western countries.1,4 Nevertheless, the pathogenesis is not well understood and the only treatment consists of the permanent exclusion of gluten from the food intake (gluten-free diet, GFD).5 Microbiome,6 vitamin D,7 and environmental factors such as infant feeding practices8 may contribute to the pathogenesis of CD. In recent years, more and more researches have reported that Helicobacter pylori may be related to the pathogenesis of CD.9 H. pylori may lead to increased intraepithelial lymphocytes (IELs); this is defined as a type I celiac lesion, in line with the Marsh–Oberhuber classification.10,11

H. pylori is colonized in human gastric mucosa, which mainly causes stomach injury.12 The global infection rate of H. pylori is as high as almost 50%, and it also occurs in childhood.13 Numerous studies have demonstrated that H. pylori infection is related to gastroduodenal diseases, including lymphocytic gastritis.12 However, whether H. pylori is related to duodenal intraepithelial lymphocytosis is still controversial. Moreover, it also remains unclear whether or not H. pylori infection affects the pathophysiological changes of CD such as the alteration of intestinal mucosa.

The main purpose of this study was to quantify the relationship between H. pylori and CD, including H. pylori alteration before and after GFD treatment. The secondary purpose was to quantify the relationship between H. pylori and CD-related symptoms, as well as the Marsh classification, through meta-analysis.

Materials and Methods

Data Selection

A systematic literature search was performed in 3 databases (PUBMED, EMBASE, and MEDICINE) up to September 1, 2020. The search was restricted to human studies and English language manuscripts. Both retrospective and prospective studies which met the requirements were included in this study. The following search terms were used to retrieve potential articles: ((Helicobacter*) OR (Helicobacter pylori) OR (Helicobacter infection) OR (HP) OR (H. pylori)) AND ((Celiac disease) OR (Celiac disease) OR (gluten-sensitive enteropathy) OR (gluten-induced enteropathy)).

The search was independently performed by 2 authors according to title and abstract, and the full text of the study was retrieved if it met the requirements. In addition, a third author would evaluate the disagreement.

Inclusion Criteria and Quality Assessment

The diagnosis of CD was based on the Marsh classification and anti-tissue transglutaminase.14 The Marsh classification consists of 4 categories based on histological changes: (1) Marsh 0: normal; (2) Marsh I: IELs increased with a normal crypt/villi ratio; (3) Marsh II: IELs increased with crypt hyperplasia; and (4) Marsh III: Disappearance of fluff.10 The diagnosis of H. pylori was confirmed on the basis of at least 1 positive result from the following tests: (1) 13C/14C urea breath test (UBT); (2) rapid urease test (RUT); (3) H. pylori culture; and (4) first serology test positive. In addition, sufficient data for calculation were needed for inclusion in the study.

Quality assessment and risk of bias were assessed through the STROBE checklist for the studies included.15 In addition, the work was conducted in accordance with the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) statement.16

Data Extraction

Three authors independently extracted relevant information from each included study according to a unified standard and then proceeded to cross-check the results. The data extracted included author, region or country, method of detection of H. pylori, and whether the patient was a child or an adult. In addition, dichotomous variable data of H. pylori infection rate in CD patients and controls, H. pylori infection rate in CD patients before and after treatment, symptom differences between H. pylori-­positive and -negative CD patients, as well as Marsh classification differences in the H. pylori-positive and -negative CD patients, were obtained. When it was necessary to fill in missing data, the authors of the included studies were contacted by e-mail for additional information.

Statistical Analysis

The calculation data involved in this study were all dichotomous variables. The data for calculation were described by odds ratio (OR) and 95% CI. Heterogeneity between studies was assessed by Cochran’s Q statistic and quantified with the I 2 statistic. The value of I 2 was used to evaluate the level of heterogeneity, assigning the categories as low (<50%) and high (≥50%).17 In this study, when heterogeneity was low, the pooled estimates were obtained using the fixed-model (Mantel and Haenszel) method. On the contrary, the random-model (M-H heterology) method was chosen if heterogeneity was high.18 This part of the analyses was carried out through Review Manager (Version 5.3, The Nordic Cochrane Centre, Rigshospitalet). Furthermore, publication bias was estimated by Begg’s test, with a value of P > .05 suggesting no publication bias. We used sensitivity analysis to evaluate whether the meta-analysis results were stable and reliable. Moreover, meta-regression was used to look for potential sources of heterogeneity, by the Monte Carlo permutation test. The difference was that this part of the analyses was carried out through the application of STATA 15 (StataCorp., College Station, Tex, USA).

Results

Basic Characteristics

A total of 1020 related articles were identified for screening, of which 25 papers were finally enrolled according to the inclusion criteria (Tables S1-S8). The flowchart describing the process of the study selection has been schematically outlined in Figure 1. The participants in 13 studies were children, and 12 articles referred to adults. In addition, the studies were mainly carried out in Europe and the Middle East. The papers retrieved were observational case-control studies or cross-sectional studies. Overall, 141 355 participants were enrolled in this study, and the definitions used for H. pylori and CD across various studies met the eligibility criteria.

Figure 1.

Figure 1.

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Flow chart for the process of identifying studies included in and excluded from the meta-analysis.

Comparison of H elicobacter pylori Infection Between CD Patients and Controls

The corresponding data have been listed in Table S1. Twenty-three papers reported H. pylori infection in CD, of which 12 reports concerned children. The total H. pylori infection rate of CD patients was 15.3%, while it was 10.6% in the controls. The total pooled results showed that H. pylori infection rate of CD patients was 0.57 times compared to controls, which showed statistical difference (OR = 0.57, 95% CI [0.44, 0.75]) (Figure 2). Subsequent subgroup analysis showed that H. pylori infection rate of CD patients was 0.63 times compared to controls in adults (OR = 0.63, 95% CI [0.49, 0.81]), while it was 0.53 in children (OR = 0.53, 95% CI [0.33, 0.85]). Both were statistically different (Figure 2).

Figure 2.

Figure 2.

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Summary estimates for the prevalence of Helicobacter pylori infection on CD patients and controls. The total pooled results showed statistical difference (OR = 0.57, 95% CI [0.44, 0.75]). Subsequent subgroup of adults and children also showed statistical difference (OR = 0.63, 95% CI [0.49, 0.81]) (OR = 0.53, 95% CI [0.33, 0.85]). However, the existence of heterogeneity suggested that there was certain variability in the study. CD, celiac disease; OR, odds ratio.

In order to further quantify the relationship between H. pylori and CD, the study compared H. pylori infection rate in treated and non-treated CD patients. A total of 4 articles reported CD treatment (Table S2), and all treatment options involved a gluten-free diet. The result showed that although the H. pylori infection rate had decreased after treatment, there was still no statistical difference (OR = 1.29, 95% CI [0.81, 2.05]) (Figure 3).

Figure 3.

Figure 3.

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Summary estimates (I 2 value of > 50%) showed that there was still no statistical difference after CD treatment (OR = 1.29, 95% CI [0.81, 2.05]). CD, celiac disease; OR, odds ratio.

H elicobacter pylori Infection and Different Symptoms of CD Patients

There were multiple articles reporting the relationship between H. pylori infection and 6 symptoms of CD patients including growth failure, inappetence, distension, abdominal pain, diarrhea, and vomiting. The main information has been listed in Tables S3-S8. According to the heterogeneity, the pooled estimates of abdominal pain and vomiting were obtained using the random-model method, while others chose the fixed-model method. We found that CD patients with H. pylori infection were more likely to have abdominal pain, diarrhea, and distension symptoms, which were 2.5, 1.56, and 2.75 times the odds respectively (OR = 2.5, 95% CI [1.35, 4.62]) (OR = 1.56, 95% CI [1.09, 2.24]) (OR = 2.75, 95% CI [1.74, 4.35]) (Figure 4). On the contrary, there was no statistical difference for the other symptoms (Figure 4).

Figure 4.

Figure 4.

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Summary estimates for the prevalence of CD symptoms with or without Helicobacter pylori infection. Abdominal pain, diarrhea, and distension symptoms showed statistical difference between the 2 groups. The I 2 value of > 50% of the groups for abdominal pain and vomiting indicated a high variability. CD, celiac disease.

H elicobacter pylori Infection and Marsh Classification of CD Patients

Four articles reported whether CD patients with or without H. pylori infection were more prone to conform to the Marsh III classification (Table S9). However, the result had no statistical difference (OR = 0.36, 95% CI [0.06, 2.07]) (Figure 5). Moreover, 4 more articles reported whether Marsh III CD patients with or without H. pylori infection were more likely to fall into the Marsh IIIc classification (Table S10). Again, there was no statistical difference (OR = 1.05, 95% CI [0.73, 1.51]) (Figure 5).

Figure 5.

Figure 5.

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Summary estimates for the prevalence of CD Marsh classification with or without Helicobacter pylori infection. The results showed no statistical difference. CD, celiac disease.

Publication Bias, Sensitivity Analysis, and Meta-Regression

Funnel plot analyses of studies assessing H. pylori infection on CD with its symptoms and Marsh classification revealed no significant publication bias, with the P values for Begg’s test being 0.579, 0.117, 0.602, 0.174, 0.06, 0.851, 0.296, 0.734, and 0.806 respectively (Figure S1). Sensitivity analysis shows that although some meta results were fluctuant, the overall results were stable and reliable (Figure S2). In addition, the authors used meta-regression to look for possible sources of heterogeneity. The results showed that heterogeneity had nothing to do with region (P > .751), age (P > .696), and H. pylori detection method (P > .788).

Discussion

This meta-analysis of 25 published studies demonstrated that H. pylori infection was lower in CD patients, suggesting that H. pylori infection may be a protective factor. However, the comparison of the results before and after CD treatment did not further support this hypothesis. H. pylori also did not affect the Marsh classification of CD. In addition, CD patients with H. pylori infection were more likely to have symptoms of abdominal pain, diarrhea, and distension.

The pathogenesis of CD is closely related to H. pylori infection, which may be closely related to the pathogenesis of these 2 entities. Epidemiologically, the incidence of CD is higher in developed countries, while the incidence of H. pylori is indeed lower. In terms of pathogenesis, the most well-known theory is the “hygiene hypothesis” postulate. Lebwohl et al. elaborated on this hypothesis.19 The core point was Th1/Th2 immune unbalance under the complex interactions of H. pylori infection and CD. A previous study revealed that in CD patients, the down-regulation of T-regulatory lymphocyte-mediated cellular responses in the intestinal wall were also diminished or lost, which indicated that T-regulatory lymphocytes may be closely related to the pathogenesis of CD.20 Meanwhile, animal experiments confirmed that T-regulatory lymphocytes recruited by H. pylori play a role in immune response.21,22 Therefore, individuals with H. pylori infection may affect immune responses to gluten by recruiting gastric T-regulatory cells.19

In addition, gut microbiome composition may be causative in the pathogenesis of CD.2 Petersen et al.23 reported that some bacteria express may potentially trigger a host immune response by mimicking gliadin. The gut microbiome can affect the immune system through the release of anti-inflammatory peptides or cytokines.24 Specific to intestinal bacteria, Bifidobacterium, with anti-inflammatory agents, had a reduced diversity in one study25 and the expression of B. fragilis, that causes increased intestinal permeability and degradation, was higher in another study.26 Similarly, E. coli and Staphylococcus species also change by affecting intestinal permeability or producing toxins and metabolites.27,28 H. pylori is also closely related to the gut microbiome. The alterative of relative abundance of Bacteroidaceae and Enterobacteriaceae caused by H. pylori was prevalent and alterative at the class, order, family, and genus levels was also observed.29 From a different perspective, through modification of gastric pH or pepsin, H. pylori may affect ingested gluten and then reduce the immunogenicity.13 It can be said that H. pylori makes a “secondary hit” in the development of CD.

In the study, the authors found that H. pylori can aggravate the symptoms of abdominal pain, diarrhea, and distension, which may indicate that H. pylori itself can also cause these symptoms. Many previous studies have reported that H. pylori infection can cause recurrent abdominal pain.30 Other articles have later reported that H. pylori seroconverting children had increased diarrhea days and diarrhea episodes31 and that the infection can aggravate diarrhea caused by other bacterial infections including Vibrio cholerae, Shigella, or Salmonella typhi.32 As is well-known, H. pylori itself can cause H. pylori-related dyspepsia, resulting in abdominal distension.33 Therefore, while H. pylori plays against the development of CD, the opposite can also aggravate some symptoms. Although the result was innovative, it is important to highlight that this study still had shortcomings. The main shortcoming was the lack of prospective controlled studies in this article. The results of this study can only prove that the 2 do have a correlation rather than a causal relationship. If further data can confirm that the statistical difference disappears after H. pylori eradication or CD treatment, they can provide evidence of a causal relationship between the two. Unfortunately, since only 4 articles were selected, the results of this study did not confirm the change in H. pylori infection after CD treatment. Secondly, the heterogeneity of some results in this study may bias the results. Although we excluded some sources of heterogeneity through meta-regression analysis, there were still some potential factors that could not be excluded, including race, dietary habit, and whether there has been a history of H. pylori eradication. However, since the current articles did not have significant clinical heterogeneity, we believe that it was appropriate to analyze the pooled results.

In conclusion, this study confirmed that there is a correlation between H. pylori and CD. However, the causality cannot be clarified and requires more prospective studies to confirm. The gut microbiota and immune unbalance provide plausible mechanisms for disease progression in CD. In addition, H. pylori infection may aggravate some symptoms of CD. Future studies should focus more on prospective studies to determine whether there is a change in correlation after H. pylori eradication or CD treatment.

Supplementary Table 1.

Comparison of Helicobacter pylori Infection Between CD Patients and Controls

Author Year Regions CD with HP+ CD with HP− Control with HP+ Control with HP–
Luzza1 1999 Italy 15 66 14 67
Lasa2 2015 Argentina 9 63 72 168
Crabtree3 1992 United Kingdom 29 70 75 175
Józefczuk4 2016 Poland 8 68 8 41
Józefczuk5 2015 Poland 4 70 20 276
Ciacci6 2000 Italy 51 136 42 34
Galli7 2016 Italy 55 190 42 103
Agin8 2018 Turkey 70 186 270 742
Guz-Mark9 2014 Israel 94 212 234 459
Aydogdu10 2008 Turkey 21 75 56 179
Bayrak11 2019 Turkey 127 355 1033 1027
Borch12 2001 Sweden 4 4 216 256
Dore13 2018 Italy 87 183 45 82
Uyanikoglu14 2016 Turkey 15 16 316 276
Nenna15 2012 Italy 6 220 24 130
Lucero16 2017 Chile 21 45 20 30
Diamanti17 1999 Argentina 87 13 67 8
Lebwohl18 2013 United States 117 2572 11 207 116 412
Narang19 2016 India 37 287 161 161
Basyigit20 2017 Turkey 5 7 133 95
Prasad21 2008 India 9 155 49 115
Simondi22 2015 Italy 26 47 166 238
Tumgor23 2017 Turkey 14 8 23 29
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CD, celiac disease; HP, Helicobacter pylori.

Supplementary Table 2.

Comparison of Helicobacter pylori Infection in Treated and Non-treated CD Patients

Author Year Regions T-CD with HP+ T-CD with HP− NT-CD with HP+ NT-CD with HP−
Luzza2 1999 Italy 9 40 6 26
Crabtree3 1992 United Kingdom 18 53 11 17
Ciacci6 2000 Italy 34 71 17 65
Diamanti17 1999 Argentina 21 1 66 14
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CD, celiac disease; T-CD, treated celiac disease; NT-CD, non-treated celiac disease; HP, Helicobacter pylori.

Supplementary Table 3.

Helicobacter pylori Infection and Growth Failure in CD Patients

Author Year Regions GF with HP+ Non-GF with HP+ GF with HP− Non-GF with HP−
Agin8 2018 Turkey 48 22 124 62
Aydogdu10 2008 Turkey 10 11 27 48
Luzza1 1999 Italy 7 8 15 51
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GF, growth failure; CD: celiac disease; HP, Helicobacter pylori.

Supplementary Table 4.

Helicobacter pylori Infection and Inappetence in CD Patients

Author Year Regions Inappetence with HP+ Non-Inappetence with HP+ Inappetence with HP− Non-Inappetence with HP−
Agin8 2018 Turkey 12 58 28 158
Aydogdu10 2008 Turkey 12 9 28 47
Narang19 2016 India 5 32 31 256
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CD, celiac disease; HP, Helicobacter pylori.

Supplementary Table 5.

Helicobacter pylori Infection and Vomiting in CD Patients

Author Year Regions Vomiting with HP+ Non-vomiting with HP+ Vomiting with HP– Non-vomiting with HP−
Agin8 2018 Turkey 3 67 18 168
Maxim24 2018 Rumania 18 5 19 28
Luzza1 1999 Italy 5 10 18 48
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CD, celiac disease; HP, Helicobacter pylori.

Supplementary Table 6.

Helicobacter pylori Infection and Distension in CD Patients

Author Year Regions Distension with HP+ Non-distension with HP+ Distension with HP− Non-distension with HP−
Agin8 2018 Turkey 21 49 26 160
Aydogdu10 2008 Turkey 12 9 11 64
Luzza1 1999 Italy 3 12 12 54
Narang19 2016 India 4 33 18 269
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CD, celiac disease; HP, Helicobacter pylori.

Supplementary Table 7.

Helicobacter pylori Infection and Abdominal Pain in CD Patients

Author Year Regions AP with HP+ Non-AP with HP+ AP with HP− Non-AP with HP−
Agin8 2018 Turkey 28 42 70 116
Aydogdu10 2008 Turkey 15 6 39 36
Luzza1 1999 Italy 6 9 5 61
Narang19 2016 India 24 13 149 138
Villanacci25 2006 Switzerland 7 23 5 45
Maxim24 2018 Romania 18 5 17 30
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CD, celiac disease; AP, abdominal pain; HP, Helicobacter pylori.

Supplementary Table 8.

Helicobacter pylori Infection and Diarrhea in CD Patients

Author Year Regions Diarrhea with HP+ Non-diarrhea with HP+ Diarrhea with HP− Non-diarrhea with HP−
Agin8 2018 Turkey 27 43 36 150
Aydogdu10 2008 Turkey 17 4 54 21
Luzza1 1999 Italy 12 3 43 23
Narang19 2016 India 25 12 195 92
Villanacci25 2006 Switzerland 5 25 12 38
Maxim24 2018 Romania 13 10 21 26
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CD, celiac disease; HP, Helicobacter pylori.

Supplementary Table 9.

Comparison of Helicobacter pylori Infection in Marsh III and Marsh I-II CD Patients

Author Year Regions Marsh III with HP+ Marsh I-II with HP+ Marsh III with HP− Marsh I-II with HP−
Aydogdu10 2008 Turkey 1 20 10 65
Bayrak11 2019 Turkey 124 3 331 24
Maxim24 2018 Romania 5 18 33 14
Villanacci25 2006 Switzerland 23 7 48 2
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CD, celiac disease; HP, Helicobacter pylori.

Supplementary Table 10.

Comparison of Helicobacter pylori Infection in Marsh III and Marsh I-II CD Patients

Author Year Regions Marsh IIIc with HP+ Marsh IIIa-b with HP+ Marsh IIIc with HP− Marsh IIIa-b with HP−
Lasa2 2015 Argentina 6 3 45 18
Agin8 2018 Turkey 15 55 53 133
Guz-Mark9 2014 Israel 52 40 89 122
Bayrak11 2019 Turkey 49 75 132 199
Narang19 2016 India 9 28 75 212
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CD, celiac disease; HP, Helicobacter pylori.

Supplementary Figure 1.

Supplementary Figure 1.

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Funnel plot analyses of studies assessing H. pylori infection on CD with its symptoms and Marsh classification.

Supplementary Figure 2.

Supplementary Figure 2.

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Sensitivity analysis of studies assessing H. pylori infection on CD.

Footnotes

Ethics Committee Approval: The study was approved by the medical ethics committee of the First Affiliated Hospital, Zhejiang University School of Medicine.

Informed Consent: N/A.

Peer-review: Externally peer-reviewed.

Author Contributions: Consept – C.L., M.Y.; Design – C.L.; Supervision – Q.C.; Resources – X.Z., Q.C.; Materials – L.L.; Data Collection and/or Processing – M.Y., Q.C.; Analysis and/or Interpretation – L.L.; Literature Search – X.Z.; Writing Manuscript – M.Y.; Critical Review – C.L.

Declaration of Interests: The authors have no conflict of interest to declare.

Funding: The study was funded by National Natural Science Foundation of China (81970498) and Zhejiang Medical and Health Science and Technology Plan Project (No. 2018KY387).

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