Name of journal: World Journal of Gastroenterology esps manuscript no: 13220 Columns: meta-analysis relationship between Helicobacter pylori infection and inflammatory bowel disease in an Asian population: a meta-analysis
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Name of journal: World Journal of Gastroenterology ESPS Manuscript NO: 13220 Columns: META-ANALYSIS Relationship between Helicobacter pylori infection and inflammatory bowel disease in an Asian population: A meta-analysis Wu XW et al. H. pylori infection and IBD in Asia Xiao-Wei Wu, Hong-Zan Ji, Miao-Fang Yang, Lin Wu, Fang-Yu Wang Xiao-Wei Wu, Hong-Zan Ji, Miao-Fang Yang, Lin Wu, Fang-Yu Wang, Department of Gastroenterology and Hepatology, Jinling Hospital, Medical School of Nanjing University, Nanjing 210002, Jiangsu Province, China Author contributions: Wu XW and Wang FY conceived and designed the study; Wu XW and Ji HZ developed methodology; all authors were involved in the collection, analysis and interpretation of data; Wu XW and Wang FY wrote the manuscript. Conflict-of-interest: There are no conflicts of interest. Data sharing: No additional data are available. Supported by National Natural Science Foundation of China, No. 81270453 Open-Access: This article is an open-access article which selected by an in-house editor and fully peer-reviewed by external reviewers. It distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: http://creativecommons.org/licenses/by-nc/4.0/ Correspondence to: Fang-Yu Wang, PhD, Department of Gastroenterology and Hepatology, Jinling Hospital, Medical School of Nanjing University, 305 Zhongshan East Road, Nanjing 210002, Jiangsu Province, China. wangfangyu2014@126.com Telephone: +86-25-80860051 Fax: +86-25-80860151 Received: August 12, 2014 Peer-review started: August 12, 2014 First decision: October 14, 2014 Revised: November 5, 2014 Accepted: December 19, 2014 Article in press: Published online: Abstract AIM: To investigate the relationship between Helicobacter pylori (H. pylori) infection and inflammatory bowel disease (IBD) in an Asian population. METHODS: The PubMed, EMBASE and Cochrane Library databases were searched up to June 2014 for observational studies, without language restrictions. Additional references were obtained from reviewed articles. RESULTS: Ten studies involving 1299 IBD patients and 1817 controls were included in the meta-analysis (24.9% of IBD patients had H. pylori infection versus 48.3% of the controls). The pooled RR of H. pylori infection rate in IBD patients compared with controls was 0.48 (95%CI: 0.43–0.54; P < 0.00001). There was no significant heterogeneity in the included studies (I2 = 21%). Egger’s linear regression suggested that there was no significant publication bias (P = 0.203). CONCLUSION: In an Asian population, the H. pylori infection rate in IBD patients is significantly lower than that in non-IBD patients, indicating a protective effect of H. pylori infection against the development of IBD. Key words: Helicobacter pylori; Inflammatory bowel disease; Asian population; Crohn’s disease; Ulcerative colitis; Meta-analysis © The Author(s) 2015. Published by Baishideng Publishing Group Inc. All rights reserved. Core tip: A meta-analysis was carried out to investigate the relationship between Helicobacter pylori (H. pylori) infection and inflammatory bowel disease (IBD) in an Asian population. The PubMed, EMBASE and Cochrane Library databases were searched up to June 2014. Ten studies involving 1299 IBD patients and 1817 controls were included in the meta-analysis (24.9% of IBD patients had H. pylori infection versus 48.3% of the controls). This meta-analysis showed that in an Asian population, the H. pylori infection rate was significantly lower in IBD patients than in non-IBD patients, indicating a protective effect of H. pylori infection against IBD. Wu XW, Ji HZ, Yang MF, Wu L, Wang FY. Relationship between Helicobacter pylori infection and inflammatory bowel disease in an Asian population: A meta-analysis. World J Gastroenterol 2015; In press INTRODUCTION Inflammatory bowel disease (IBD) is described as chronic inflammation of the gastrointestinal tract in genetically susceptible individuals exposed to environmental risk factors and involves alternating active and quiescent phases leading to an increased health burden worldwide[1,2]. Crohn’s disease (CD) and ulcerative colitis (UC) are the two primary subtypes of IBD. These diseases may result in intestinal damage, complications, and surgical interventions[3,4]. Commensal enteric bacteria are considered to have a critical role in the development of IBD. Continuous microbial antigenic stimulation can activate pathogenic immune responses and result in damage to intestinal mucosal barrier function and immunoregulation[5]. Genetic polymorphisms in the host most likely interact with intestinal bacteria to stimulate aggressive immunoreactions that cause chronic tissue injury. It is necessary to identify these host and microbial changes in individual patients in order to treat IBD[6,7]. Helicobacter species are characterized by microaerophilic metabolism, spiral shape, and peculiar motility, which contribute to their colonization of the gastrointestinal mucosal surface[8]. Helicobacter pylori (H. pylori) is a gram-negative, spiral-shaped pathogenic bacterium which is associated with chronic gastritis and is usually located on the surface of the stomach epithelium. Interestingly, H. pylori has also been identified in the normal colonic mucosa, colorectal neoplasms[9-11] and the intestinal mucosa of IBD patients[12,13]. Furthermore, H. pylori has been confirmed to be a risk factor for colonic neoplasms[14,15], however, there is insufficient evidence to conclude that H. pylori has an important role in the pathogenesis of IBD. Many observational studies have investigated the association between H. pylori infection and IBD. A meta-analysis involving 23 studies suggested that H. pylori infection rate in IBD patients was lower than that in non-IBD patients, and H. pylori was beneficial in preventing the development of IBD[16]. However, this meta-analysis only included one study which investigated the prevalence of H. pylori in an Asian population, and the conclusion was possibly not suitable for Asian populations. Therefore, we carried out an updated meta-analysis including only studies that determined the prevalence of H. pylori in IBD patients from Asian countries. MATERIALS AND METHODS Inclusion/exclusion criteria Studies in line with the following criteria were included: (1) investigated the relationship between H. pylori infection and IBD; (2) used a case-control, cross-sectional, or cohort design; and (3) specifically included an Asian population. Studies were excluded if: (1) data from a previously published study were used; and (2) included a pediatric population. Search strategy We performed a search of PubMed, EMBASE and the Cochrane Library up to June 2014. A search strategy was constructed using a combination of the following words: (Helicobacter pylori or H. pylori) and (inflammatory bowel disease or Crohn’s disease or ulcerative colitis). Articles published in any language were included. A manual search of the references listed by studies retrieved from the online databases and from previously published systematic reviews was also performed to identify additional relevant studies. Data extraction Two investigators (Wu and Ji) extracted data. Any differences regarding study inclusion, data extraction and interpretation were resolved by consensus before the final analysis. Study variables were collected in the following categories: the year of publication, the country of origin, the study center, characteristics of the patients, and the H. pylori detection method. To avoid inclusion of duplicated data in the final analysis, retrieved studies were carefully evaluated and checked by comparing author names, geographical locations and period of study. Statistical analysis Meta-analysis was carried out by combining the risk ratio (RR) in the IBD groups and control groups of the individual studies in a global RR. Statistical heterogeneity testing was performed using the χ2 statistic and I2, and an I2 value of more than 50% was considered to represent substantial heterogeneity[17]. A fixed-effects model was selected when the heterogeneity test showed an I2 value of less than 50%, otherwise a random-effects model was used. A funnel plot was used to determine publication bias[18]. Analyses were conducted using Review Manager [Review Manager (RevMan) [Computer program] Version 5.3. Copenhagen: The Nordic Cochrane Centre, The Cochrane Collaboration, 2014]. The statistical methods of this study were reviewed by Liu from Department of Medical Statistics, School of Medicine, Nanjing University. RESULTS Search results Our search identified 422 potentially relevant studies, of which 393 were excluded after title and abstract screening. Twenty-nine articles were retained for full-text review. Seven review articles, two case reports, eight studies including non-Asian populations, one study with incomplete data, and one study which included a pediatric population were subsequently excluded. We identified ten studies which fulfilled the inclusion criteria[13,19-27]. These studies included a total of 1299 cases of IBD and 1817 controls. Figure 1 shows the study flow diagram. Characteristics of the included studies The characteristics of the included studies and patients are presented in Error: Reference source not found. Four studies were from Japan, four studies were from China, and two studies were from Korea. All were case-control studies. Two of them were multicenter studies, and eight were single-center studies. The mean age of IBD patients ranged from 28.9 to 44.7 years. Two studies used serologic tests (immunoglobulin G) and eight studies used non-serologic tests (C-urea breath test, biopsy specimen histology, or biopsy sample culture) to detect H. pylori. H. pylori and IBD Of these studies which included 1299 IBD patients and 1817 controls (Figure 2), 24.9% of patients in the IBD groups were found to have H. pylori infection, while 48.3% of patients in the control groups had H. pylori infection. The pooled RR of H. pylori infection rate in IBD patients compared to controls was 0.48 (95%CI: 0.43–0.54; P < 0.00001). A fixed effect model was used for the meta-analysis as no significant heterogeneity in the included studies was observed (I2 = 21%). Nine studies included 751 CD patients and 1696 controls (Figure 3). The rate of H. pylori infection in CD patients was 21.3% compared with 47.7% in the control groups (RR = 0.43; 95%CI: 0.37–0.50; P < 0.00001). A fixed effect model was selected for the meta-analysis as significant heterogeneity in the included studies was not observed (I2 = 43%). Six studies included 548 UC patients and 1025 controls (Figure 4). The rate of H. pylori infection was 29.9% in UC patients versus 52.5% in the control groups (RR = 0.55; 95%CI: 0.48-0.64; P < 0.00001). We performed the meta-analysis with a fixed effect model as no significant heterogeneity was found in the included studies (I2 = 0%). Publication bias The funnel plot revealed a reasonably symmetrical distribution of the included studies on the association between H. pylori infection and IBD (Figure 5). Egger’s linear regression suggested that there was no statistically significant evidence of publication bias (P = 0.203). DISCUSSION The prevalence of H. pylori infection varies markedly in different countries and regions. Higher prevalence rates are seen in some developing Asian countries[28,29], while lower rates have been found in many developed countries of Europe and North America[30,31]. Moreover, the prevalence rates may vary significantly in different geographic regions or ethnic populations of the same country[32,33]. However, the variation in H. pylori infection rate in IBD patients of different race or region has not been completely clarified. Our meta-analysis identified ten studies focused on the association between H. pylori infection and IBD in an Asian population. The included cases were from three east-Asian countries (China, Japan and Korea) and are considered to have similar ethnic origin, while the previous meta-analysis published in 2010 involved populations mostly from European and American countries[16]. By specifically including an Asian population, the heterogeneity and publication bias were both lower than those in the previous meta-analysis. The pooled rate of H. pylori infection in the IBD groups was a little lower than that reported in the previous meta-analysis (24.9% vs 27.1%), but the pooled rate of H. pylori infection in the control groups was higher than that previously reported (48.3% vs 40.9%). These discordant results suggest that ethnic origin may have a potential impact on the relationship between H. pylori infection and IBD. The mechanism of H. pylori infection in preventing IBD is unclear. It has been hypothesized that H. pylori may down-regulate pro-inflammatory immune responses in the host in order to promote its own survival, resulting in beneficial effects to the host. An animal experiment showed that long-term H. pylori infection can lead to distinct changes in microbiota composition in the large intestine, indicating that H. pylori may modulate the intestinal flora to affect the development of IBD[34]. Other research in animal colitis models suggested that H. pylori infection can regulate the immune responses, resulting in benefit to the host against other chronic inflammatory conditions such as IBD[35,36]. Papamichael K et al[37] showed that H. pylori infection may play a protective role against IBD via the following mechanisms: increase the levels of some cytokines; activate dendritic cells and T cells; down-regulate the Th1/Th17 pathway; induce the generation of antibodies against H. pylori. In our meta-analysis, the pooled RR of H. pylori infection rate in IBD patients versus controls was 0.48 (95%CI: 0.43–0.54), which suggested a protective effect of H. pylori infection against the development of IBD. Subgroup analyses showed a tendency toward a superior effect for CD (RR = 0.43; 95%CI: 0.37–0.50) when compared to UC (RR = 0.55; 95%CI: 0.48–0.64). One of the included studies revealed a more evident association between H. pylori infection and IBD in cases under 60 years old, which suggested that H. pylori infection may reduce the risk of IBD in younger adults[25]. Two studies found that H. pylori infection rate of IBD patients treated with antibiotic was lower than untreated patients. However, IBD patients without antibiotic treatment still showed a significantly lower rate of H. pylori infection than controls[24,25]. In a study with only 153 UC patients, the H. pylori infection rates in patients with diverse severity or extent of UC were significantly lower than those in the controls[26]. Another study showed that the H. pylori infection rates in patients with colonic, small intestine and ileocolonic CD were significantly lower than that in the control group, respectively[27]. We did not find any obvious correlation between the phenotypic characteristics of IBD patients and H pylori infection rate in the included studies. In conclusion, our meta-analysis shows that the rate of H. pylori infection in IBD patients from Asian countries is significantly lower than that in non-IBD patients. However, there are some limitations in our meta-analysis, such as an insufficient number of included studies and potential heterogeneity. More prospective high-quality controlled studies are required to confirm the results of this meta-analysis.
Epidemiologic data show that Helicobacter pylori (H. pylori) infection has a protective effect against the development of autoimmune disease. Laboratory data suggest that H. pylori can induce immune tolerance and suppress the inflammatory response. Many observational studies have investigated the association between H. pylori infection and inflammatory bowel disease (IBD). Most of these studies found that the H. pylori infection rate in IBD patients was lower than that in non-IBD patients. However, conflicting outcomes have been observed and the exact mechanism of the protective effect of H. pylori in IBD development is still unclear. Research frontiers Numerous studies describing the H. pylori infection rates in IBD patients compared with healthy controls have been published in the past twenty years. A previous meta-analysis involving 23 studies suggested a lower H. pylori infection rate in IBD patients. H. pylori infection rate is related to ethnicity and region, however, the previous meta-analysis only included one study from an Asian country. This study investigated the relationship between H. pylori infection and IBD in an Asian population. Innovations and breakthroughs The authors demonstrated that H. pylori infection rate in IBD patients was significantly lower than that in non-IBD patients in an Asian population. The pooled H. pylori infection rate of IBD patients in this study was a little lower than the previous meta-analysis (24.9% vs 27.1%), but the pooled rate in the control groups was higher than that previously reported (48.3% vs 40.9%). These results suggest that ethnic origin may have an impact on H. pylori infection rate, providing powerful evidence that H. pylori infection is a potential protective factor in the development of IBD. Applications The results of this meta-analysis show that IBD patients with a history of taking antibiotics had a lower H. pylori infection rate in two of the included studies, however, there were no available data for the controls. Antibiotic use may be partly responsible for the lower H. pylori infection rate in IBD patients. The exact mechanism of this interesting phenomenon should be investigated further. Large sample and well designed cohort studies with stringent disease and H. pylori infection definitions are required in order to delineate the protective effect of H. pylori infection in IBD development. Terminology H. pylori is a gram-negative, microaerophilic bacterium. It is present in patients with chronic gastritis and gastric ulcers. It is also linked to the development of duodenal ulcers and stomach cancer. H. pylori may be implicated in the pathogenesis of autoimmune diseases. 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Prior Helicobacter pylori infection ameliorates Salmonella typhimurium-induced colitis: mucosal crosstalk between stomach and distal intestine. Inflamm Bowel Dis 2011; 17: 1398-1408 [PMID: 21560200 DOI: 10.1002/ibd.21489] 37 Papamichael K, Konstantopoulos P, Mantzaris GJ. Helicobacter pylori infection and inflammatory bowel disease: is there a link? World J Gastroenterol 2014; 20: 6374-6385 [PMID: 24914359 DOI: 10.3748/wjg.v20.i21.6374] P-Reviewer: Chen Z, Engin AB, Kopylov U S-Editor: Qi Y L-Editor: E-Editor: Figure 1 Flow diagram of the study selection process. 
Figure 2 Forest plot of Helicobacter pylori infection rate in inflammatory bowel disease groups vs control groups. 
Figure 3 Forest plot of Helicobacter pylori infection rate in Crohn’s disease groups versus control groups. 
Figure 4 Forest plot of Helicobacter pylori infection rate in ulcerative colitis groups vs control groups. 
Figure 5 Funnel plot analysis. 
Table 1 Characteristics of the studies included in the meta-analysis
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