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Meta-analysis: Can Helicobacter pylori Eradication Treatment Reduce the Risk for Gastric Cancer?

Lorenzo Fuccio, MD; Rocco Maurizio Zagari, MD; Leonardo Henry Eusebi, MD; Liboria Laterza, MD; Vincenzo Cennamo, MD; Liza Ceroni, MD; Diego Grilli, PhD; and Franco Bazzoli, MD
[+] Article and Author Information

From the University of Bologna, Bologna, Italy, and University of South Florida, Tampa, Florida.


Potential Financial Conflicts of Interest: None disclosed.

Requests for Single Reprints: Franco Bazzoli, MD, Dipartimento di Medicina Interna e Gastroenterologia, Università di Bologna, Policlinico S. Orsola, Via Massarenti 9, 40138 Bologna, Italy; e-mail, franco.bazzoli@unibo.it.

Current Author Addresses: Drs. Fuccio, Zagari, Eusebi, Laterza, Cennamo, Ceroni, and Bazzoli: Dipartimento di Medicina Interna e Gastroenterologia, Università di Bologna, Policlinico S. Orsola, Via Massarenti 9, 40138 Bologna, Italy.

Dr. Grilli: University of South Florida, 4202 East Fowler Avenue, Tampa, FL 33620.


Ann Intern Med. 2009;151(2):121-128. doi:10.7326/0003-4819-151-2-200907210-00009
Text Size: A A A

Background: Helicobacter pylori infection is associated with gastric cancer, but the effect of eradication treatment on gastric cancer risk is not well defined.

Purpose: To determine whether H. pylori eradication treatment can reduce the risk for gastric cancer.

Data Sources: PubMed, EMBASE, Cochrane Library, Google Scholar, and online clinical trial registers through 31 January 2009, without language restrictions.

Study Selection: Randomized trials that compared eradication treatment with no treatment in H. pylori–positive patients and that assessed gastric cancer or progression of preneoplastic lesions during follow-up.

Data Extraction: Two authors independently reviewed articles and extracted data.

Data Synthesis: Seven studies met inclusion criteria, 1 of which was excluded from pooled analysis because of clinical and methodological heterogeneity. All studies were performed in areas with high incidence of gastric cancer, mostly in Asia. Overall, 37 of 3388 (1.1%) treated patients developed gastric cancer compared with 56 of 3307 (1.7%) untreated (control) participants. In a pooled analysis of 6 studies with a total of 6695 participants followed from 4 to 10 years, the relative risk for gastric cancer was 0.65 (95% CI, 0.43 to 0.98).

Limitations: All studies but 1 were performed in Asia. Only 2 assessed gastric cancer incidence, and only 2 were double-blinded.

Conclusion: Helicobacter pylori eradication treatment seems to reduce gastric cancer risk.

Figures

Grahic Jump Location
Figure 1.
Study flow diagram.

APDW = Asian Pacific Digestive Week; DDW = Digestive Disease Week; UEGW = United European Gastroenterology Week.

Grahic Jump Location
Grahic Jump Location
Figure 2.
Forest plot of 6 studies reporting gastric cancer in treated and nontreated groups.

The area of the boxes corresponds to the weight of each study. RR = relative risk.

Grahic Jump Location

Tables

References

Letters

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Helicobacter pylori Eradication for Gastric Cancer Prevention
Posted on July 22, 2009
Tetsuji Fujita
Jikei University School of Medicine
Conflict of Interest: None Declared

TO THE EDITOR: In the meta-analysis of 6 randomized controlled trials (RCTs) with a total of 6695 patients that assessed whether eradication of Helicobacter pylori can prevent the development of gastric cancer by Dr Fuccio and coworkers (1), intervention for H. pylori eradication significantly reduced the risk for gastric cancer (relative risk 0.65, 95 % confidence interval [CI] 0.43-0.98). The results of meta-analysis are influenced by the number of pooled patients, quality of RCTs, and analytic methods. About 2 years ago, the authors have performed a meta-analysis of 4040 patients pooled from 4 RCTs for the same purpose, where no significant difference in gastric cancer risk was shown between H. Pylori eradication group and control group (odds ratio 0.67, 95 % CI 0.42-1.07), leading to the conclusion that the effectiveness of H. pylori eradication seems to be limited to the population at high risk of gastric cancer (2). Of the 4 RCTs included in the initial meta-analysis one RCT is excluded from the current meta-analysis, whereas three RCTs, which have been published but was not included in the initial meta-analysis, are added to the current meta-analysis. I would like to ask the authors why and how inclusion criteria for meta-analysis have been changed? A substantial percentage of patients were lost to follow-up because of need for long- term follow-ups, and eradication rates ranged from 73 % to 88.9 % in treatment groups and from 5 % to 15.2 % in control groups. In such situations, I think per protocol analysis is required in addition to intention-to treat analysis used for the study. This meta-analysis supports the 2008 Asian-Pacific consensus guidelines that recommend mass screening and treatment for H. pylori in the high-risk regions (3), but the question of whom to treat in the medium- or low-risk population remains unanswered.

References

1. Fuccio L, Zagari RM, Eusebi LH, Laterza L, Cennamo V, Ceroni L, et al. Meta-analysis: Can Helicobacter pylori eradication treatment reduce the risk for gastric cancer? Ann Intern Med. 2009; 148: 121-8.

2. Fuccio L, Zagari RM, Minardi ME, Bazzoli F. Systematic review: Helicobacter pylori eradication for the prevention of gastric cancer. Aliment Pharmocol Ther 2007; 25: 133-41.

3. Fock KM, Talley N, Moayyedi P, Hunt R, Azuma T, Sugano K, et al. Asian-Pacific consensus guidelines on gastric cancer prevention. J Gastroenterol Hepatol 2008; 23: 351-65.

Conflict of Interest:

None declared

Role of eradication therapy for preventing gastric cancer remains unclear
Posted on July 23, 2009
Alexander C Ford
St James's University Hospital
Conflict of Interest: None Declared

Editor;

We read the recent meta-analysis by Fuccio et al. (1) with interest. There is an ongoing Cochrane review on this subject, the protocol of which is in the public domain (2). In their study, Fuccio et al. report that eradication therapy for Helicobacter pylori (H. pylori) reduces subsequent incidence of gastric cancer. Unfortunately, we have serious doubts about the accuracy of their analysis. The methods section of the paper states that, where multiple articles for a single study were found, the latest publication from each eligible study was used. However, it is clear to us, and should have been obvious to the authors if, as they maintain, they obtained further information directly from original investigators, that they have incorporated data from the same randomized controlled trial (RCT) twice (3, 4). This becomes apparent when Tables 1 and 2 are examined, (1) demonstrating that both studies were conducted in the Shandong province of China, commenced in 1996, contained very similar numbers of participants, and used identical eradication regimens of the same duration. We contacted the original investigators of these studies directly, a stated aim of our Cochrane review protocol, (2) and they have confirmed that these two publications are in fact 5 (3) and 10 (4) year follow-up studies from the same RCT.

The erroneous inclusion of data from the same RCT twice has led the authors to report a significant effect of H. pylori eradication therapy in reducing incidence of gastric cancer where none exists. If the 5-year data are excluded, (3) and only the 10-year follow-up data considered, (4) the pooled relative risk for occurrence of subsequent gastric cancer is 0.65 (95% CI 0.42 to 1.01). It is also interesting to note that there are fewer gastric cancers after 10 years of follow-up in this RCT, (4) than at 5 years (3). All this suggests that the effect of eradication therapy on gastric cancer is not as clear-cut as their article implies.

This highlights several important issues. Firstly, need for transparent reporting of follow-up studies conducted at various time points from the same RCT. Secondly, where studies are only reported in abstract-form, or there are doubts about accuracy of data, the importance of clarifying this by direct contact with original investigators. Thirdly, problems for journal editors and reviewers in confirming the accuracy of results of systematic reviews and meta-analyses, such that independent verification may be required for full confidence in their results.

REFERENCES

1. Fuccio L, Zagari RM, Eusebi LH, Laterza L, Cennamo V, Ceroni L, et al. Meta-analysis: can Helicobacter pylori eradication treatment reduce the risk for gastric cancer. Ann Intern Med 2009;151:121-128.

2. Moayyedi P, Hunt R, Forman D. Helicobacter pylori eradication for the prevention of gastric neoplasia. Cochrane Database Syst Rev 2006;1:CD005583.

3. Leung WK, Lin S-R, Ching JYL, To K-F, Ng EKW, Chan FKL, et al. Factors predicting progression of gastric intestinal metaplasia: results of a randomised trial on Helicobacter pylori eradication. Gut 2004;53:1244 -1249.

4. Zhou L. Ten-year follow-up study on the incidence of gastric cancer and the pathological changes of gastric mucosa after H. pylori eradication in China. Gastroenterology 2008;134 (suppl 1):A233.

Conflict of Interest:

None declared

Helicobacter Pylori virulence and genetic polymorphism
Posted on July 24, 2009
Jacobo Dib Jr
Hospital de Lidice. Caracas, Venezuela.
Conflict of Interest: None Declared

It is still not clear why only a minority of individuals infected with Helicobacter Pylori develop gastric cancer. H.Pylori virulence depends on the presence of markers such as vacuolating toxin (VacA), the cytotoxin-associated gene product (CagA) and the adhesion protein BabA2 (1). On the host side, there are factors predisposing to certain susceptibility to H. Pylori associated disease including genetic polymorphisms, such as the carriage of IL-IRN*2 (2). Thus, the matter of gastric cancer prevention by simply eradicating H. Pylori is not an easy task as it seems, and demands more prospective studies that should take into account both, the virulence of H. Pylori and the genetic polymorphism of the host.

References

(1) Paniagua Gl, Monroy E, Rodriguez R et al.Frecuency of vacA,cagA and babA2 virulence markers in Helicobacter H.Pylori strains isolated from Mexican patients with chronic gastritis. Ann Clin Microbiol Antimicrob. 2009; 8:14.

(2) Chen A, Li C, Hsu P et al. Risks of interleukin- 1 genetic polymorphisms and Helicobacter pylori infection in the development of gastric cancer. Aliment Pharmacol Ther. 2004; 20: 203-211.

Conflict of Interest:

None declared

Re: Role of eradication therapy for preventing gastric cancer remains unclear
Posted on July 30, 2009
Lorenzo Fuccio
University of Bologna
Conflict of Interest: None Declared

We read the response by Ford and Moayyedi to our recently published meta-analysis with interest (1). The authors stated that we included in our review the same study twice which should have been clear to us from the data extracted from the two studies (2,3), since "both studies were conducted in the Shandong province of China, commenced in 1996, contained very similar numbers of participants, and used identical eradication regimens of the same duration." However, it should be realised that the Shandong province has a land surface of about 160'000 km2 and a population of more than 94'000'000 people; therefore, it seemed to us not too unrealistic that two studies were accomplished in this same area and that different patients were treated using the same most common worldwide eradication treatment of that time (i.e. one week of omeprazole, clarithromycin and amoxicillin (OAC)). Furthermore, regarding the "very similar numbers of participants", Leung and associates (2), in 2004, reported the results of their five-year prospective randomised control study and stated that "five hundred and eighty seven H pylori infected subjects were randomised in this study. A total of 295 received a one week course of OAC whereas 292 received placebo"; on the other hand, Zhou and co-workers in 2003 reported in their results of the five-year prospective randomised control study (4)that "of the 1006 cases randomly selected from the general population, 552 H. pylori positive individuals were randomly divided into a treatment group (n=276) or a control group (n=276)". These data are far from being identical; furthermore, as it can be clearly observed in all the tables included in our meta-analysis, the total number of randomized patients is not the only discrepancy between the two studies. Different data are also reported for all the following points: 1) Helicobacter pylori eradication rate in the treated group; 2) Baseline histological characteristics of the included patients; 3) Histological classification system used; 4) Age inclusion range; 5) Mean age of the included patients; 6) Age range of the included patients; and, finally, 7) The number of gastric cancer cases reported in the two groups of randomization. Therefore, based on all these characteristics, the two studies seemed different to us. Moreover, Leung was a co-author in the article published by Zhou and associates, neither was Zhou a co-author of the article by Leung and coworkers. Nevertheless, we tried to contact by e-mail the first and/or correspondent authors of both studies. Unfortunately, we did not manage to make contact with Leung and co-workers. However, Dr. Zhou in the response to our request of additional information referred only to the following three articles: Chinese Medical Journal 2003;116(1):11-14, Chinese Journal of Digestive Diseases 2005;6:114-115 and Gastroenterology 2008;134(4)S1:A-223; no reference was made to the study by Leung and colleagues.

Thus, we are very grateful to Drs. Ford and Moayeddi for addressing this point, since the data we reported undoubtedly appear to belong to two different studies and not simply to the 5-year and to the 10-year follow- up studies from the same RCT. Most of all, it should be explained how was it possible that the number of cases of gastric cancer in the treated group were less in the 10 year follow up than in the 5 year follow up of the same RCT study. We have serious doubts about the accuracy of these data and, after all, we are now not so sure which of the two groups of data, if any, should be taken into consideration. Therefore, we strongly agree with both Drs. Ford and Moayeddi about the need of transparent reporting for follow-up studies conducted at different stages of the same RCT.

In addition, we want to point out that in our meta-analysis we avoided stressing the statistical significance of our results, since the few available studies did not allow any firm conclusion. An OR of 0.65 with a 95% CI from 0.43 to 0.98 (p=0.04) is very close to the OR obtained after excluding the study by Leung and associates (2): OR 0.65; 95% CI 0.42 to 1.01 (p=0.05). It is well known, that clinical and statistical significances do not always correspond. Therefore, the conclusions of the analysis even excluding the study by Leung will remain the same: Helicobacter pylori eradication treatment seems to modestly reduce the risk of gastric cancer. However, from a clinical point of view "even a small reduction in risk and incidence achieved with H. pylori eradication treatment will probably give a huge advantage in terms of social health, especially in high-risk areas" (1).

Finally, our data, with or without the study by Leung WK and associates, are completely different from those presented by Drs. Moayyedi and Ford at the Digestive Disease Week in 2008 (5). The Authors performed a meta-analysis based on 5 eligible trials, three from China and two from Japan, evaluating 5676 subjects for an average of 2.4 to 12 years of follow up and reported a highly significant reduction of gastric cancer risk in the H. pylori eradication arm (RR = 0.56; 95% CI = 0.4 to 0.8). Based on their meta-analysis, the 2008 Asian-Pacific International Guidelines (6) recommended to screen and treat H. pylori infection in populations with high incidence of gastric cancer. It would be extremely interesting to know more details on their meta-analysis and whether the Authors, after two years and our work, would still confirm their data.

References

1. Fuccio L, Zagari RM, Eusebi LH, Laterza L, Cennamo V, Ceroni L, et al. Meta-analysis: Can Helicobacter pylori Eradication Treatment Reduce the Risk for Gastric Cancer? Ann Intern Med 2009; 151: 121-128.

2. Leung WK, Lin SR, Ching JY, To KF, Ng EK, Chan FK, et al. Factors predicting progression of gastric intestinal metaplasia: results of a randomised trial on Helicobacter pylori eradication. Gut. 2004;53:1244-9.

3. Zhou L. Ten-year follow-up study on the incidence of gastric cancer and the pathological changes of gastric mucosa after H.pylori eradication in China. Gastroenterology. 2008;134:A233.

4. Zhou LY, Sung JJ, Lin S et al. A five year follow-up study on the pathological changes of gastric mucosa after H. pylori eradication. Chin. Med. J. (Engl.). 2003; 116: 11"“14.

5. Moayyedi P, Hunt RH, Ford AC, Talley NJ, Forman D. Helicobacter pylori Eradication Reduces the Incidence of Gastric Cancer: Results of a Systematic Review of Randomized Controlled Trials Gastroenterology 2008;134(4)S1:A631.

6. Fock KM, Talley N, Moayyedi P, Hunt R, Azuma T, Sugano K, et al; Asia-Pacific Gastric Cancer Consensus Conference. Asia-Pacific consensus guidelines on gastric cancer prevention. J Gastroenterol Hepatol. 2008;23:351-65.

Conflict of Interest:

None declared

Correction
Posted on August 21, 2009
Cynthia Mulrow
Deputy Editor, Annals
Conflict of Interest: None Declared

Correction: Helicobacter pylori Eradication Treatment

A recently published paper that pooled data from 6 trials reported that, compared to no treatment, Helicobacter pylori eradication treatment reduced the relative risk for gastric cancer (relative risk 0.65; 95% CI 0.43 to 0.98). Tables, Figures, and text in that paper described and counted data from "two" trials that were actually 5 and 10 year follow-up data from the same trial.(2,3) Further, the reported data for the eradication treatment group for the trial showed fewer gastric cancers at 10 year (n=2) than at 5 year follow-up (n=4). Reported numbers for the 10 year follow-up were extracted from an abstract presentation.(3) If the reported data from the 5 or 10 year follow-up are excluded, the pooled relative risk is 0.65 (95% CI 0.42 to 1.01) and 0.70 (95% CI 0.46 to 1.08), respectively. If reported data from both the 5 and 10 year follow- up are excluded, the pooled relative risk is 0.71 (95% CI 0.45 to 1.23).

1. Fuccio L, Zagari RM, Eusebi LH, Laterza L, Cennamo V, Ceroni L, et al. Meta-analysis: can Helicobacter pylori eradication treatment reduce the risk for gastric cancer. Ann Intern Med 2009;151:121-128.

2. Leung WK, Lin S-R, Ching JYL, To K-F, Ng EKW, Chan FKL, et al. Factors predicting progression of gastric intestinal metaplasia: results of a randomised trial on Helicobacter pylori eradication. Gut 2004;53:1244 -1249.

3. Zhou L. Ten-year follow-up study on the incidence of gastric cancer and the pathological changes of gastric mucosa after H. pylori eradication in China. Gastroenterology 2008;134 (suppl 1):A233.

Conflict of Interest:

None declared

Eradication Therapy for Helicobacter Pylori
Posted on August 21, 2009
Lorenzo Fuccio
University of Bologna
Conflict of Interest: None Declared

We read Drs. Ford and Moayyedi's comments that we counted the same trial twice in our recently published meta-analysis (1). Reports of the "two" pertinent trials (2,3) were not written by the same authors and had showed that the work had been carried out in the large Shandong province of China in the 1990's using the most common worldwide eradication treatment of that time (one week of omeprazole, clarithromycin and amoxicillin (OAC)). The two reports, as well as a third related report, showed confusing discrepancies regarding recruitment methods for participants and numbers of patients randomized to eradication treatment and control groups (2-4). These reports also gave discrepant information for the following: 1) Helicobacter pylori eradication rate in the treated group; 2) Baseline histological characteristics of included patients; 3) Histological classification system used; 4) Age inclusion range and mean age of included patients; and 5) number of gastric cancer cases reported in each group. Based on the above, we thought that the two studies were different, but we did try to contact authors for clarification and confirmation of that assessment. Our e-mail attempt to contact Dr. Leung and co-workers (2) was unsuccessful. Dr. Zhou responded to our request for additional information by sending us three publications, (3-5) but made no reference to the study by Leung and colleagues.

At this point, we are very grateful to Drs. Ford and Moayyedi for raising the issue that Dr. Zhou's report (3) possibly represents 10 year follow-up data from the same trial for which Dr. Leung and associates reported 5 year follow-up data (2). If this is so, one must explain how it was possible that the number of cases of gastric cancer in the treated group were less in the 10 year follow up (n=2) than in the 5 year follow up (n=4) of the same trial. One must have serious doubts about the accuracy of these data and one must question which of the two groups of data, if any, should be taken into consideration. Moreover, we strongly agree with both Drs. Ford and Moayyedi about the need for transparent reporting for follow-up studies conducted at different stages of the same randomized controlled trial.

Finally, we want to point out that in our meta-analysis we avoided stressing the statistical significance of our results, since the few available studies did not allow firm conclusions. A RR of 0.65 with a 95% CI from 0.43 to 0.98 (p=0.04) is very close to the RR obtained after excluding the 5 year follow-up data reported by Leung and associates (2): RR 0.65; 95% CI 0.42 to 1.01 (p=0.05). It is well known, that clinical and statistical significance do not always correspond. Therefore, the conclusions of our analysis even excluding the study by Leung remain the same: Helicobacter pylori eradication treatment seems to modestly reduce the risk of gastric cancer. However, from a clinical point of view "even a small reduction in risk and incidence achieved with H. pylori eradication treatment will probably give a huge advantage in terms of social health, especially in high-risk areas" (1).

References

1. Fuccio L, Zagari RM, Eusebi LH, Laterza L, Cennamo V, Ceroni L, et al. Meta-analysis: Can Helicobacter pylori Eradication Treatment Reduce the Risk for Gastric Cancer? Ann Intern Med 2009; 151: 121-128.

2. Leung WK, Lin SR, Ching JY, To KF, Ng EK, Chan FK, et al. Factors predicting progression of gastric intestinal metaplasia: results of a randomised trial on Helicobacter pylori eradication. Gut.2004;53:1244-9.

3. Zhou L. Ten-year follow-up study on the incidence of gastric cancer and the pathological changes of gastric mucosa after H.pylori eradication in China. Gastroenterology. 2008;134:A233.

4. Zhou LY, Sung JJ, Lin S et al. A five year follow-up study on the pathological changes of gastric mucosa after H. pylori eradication. Chin. Med. J. (Engl.).2003; 116: 11"“14.

5. Zhou LY, Lin SR, Ding SG, Huang XB, Zhang L, Meng LM, et al. The changing trends of the incidence of gastric cancer after Helicobacter pylori eradication in Shandong area. Chinese Journal of Digestive Diseases 2005;6:114-115.

Conflict of Interest:

None declared

Eradication Therapy for Helicobacter pylori: Errors in Meta-analysis
Posted on August 21, 2009
Alexander C Ford
St James University Hospital
Conflict of Interest: None Declared

We read the recent meta-analysis by Fuccio et al. (1) with interest. There is an ongoing Cochrane review on this subject, the protocol of which is published (2) and the results of which have been reported in abstract. (3) In their paper, Fuccio et al. report that eradication therapy for Helicobacter pylori (H. pylori) reduces subsequent incidence of gastric cancer. Unfortunately, we have serious doubts about the accuracy of their analysis. The methods section of the paper states that, where multiple articles for a single study were found, the latest publication from each eligible study was used. However, the meta-analysiserroneously incorporated data from the same randomized controlled trial (RCT) twice. (4, 5) Tables 1 and 2 of the published meta-analysis (1) showed "two" studies that were conducted in the Shandong province of China, commenced in 1996, contained very similar numbers of participants, and used identical eradication regimens of the same duration. We had contacted the original investigators of these studies directly when collecting data for our review (2,3). Those investigators confirmed that the two publications were in fact 5 (4) and 10 (5) year follow-up studies from the same RCT.

The erroneous inclusion of data from the same RCT twice led the authors of the published meta-analysis to report a statistically significant effect of H. pylori eradication therapy in reducing incidence of gastric cancer, when this is not the case. If one excludes 5-year data (4) and only includes the 10-year follow-up data, (5) the pooled relative risk for occurrence of subsequent gastric cancer is 0.65 (95% CI 0.42 to 1.01). Also, of note, is that the pertinent trial publications reported fewer gastric cancers after 10 years of follow-up (5) than at 5 years, (4) raising concerns about the accuracy of data collection, or of reporting for the trial. Taken together, this information convinces us that the effect of eradication therapy on gastric cancer is not as clear-cut as the published meta-analysis implies.

We delayed publishing our full Cochrane review due to the concerns mentioned above about the duplicate Chinese studies. Our knowledge and experience regarding errors in meta-analyses and Annals' publication of the meta-analysis with erroneous data highlights several important issues for authors of meta-analyses, journal editors, and peer reviewers. Firstly, transparent reporting of follow-up studies conducted at various time points from the same RCT is needed to ensure correct identification of trials and avoid miscounting of data by authors. Secondly, where studies are only reported in abstract-form, or if there are doubts about accuracy of data, authors should directly contact original investigators for clarifications. Thirdly, peer reviewers (and journal editors) may encounter difficulties in confirming the accuracy of results of systematic reviews and meta-analyses. In some instances, independent verification of the meta-analysis may be necessary to ensure the results are truly accurate.

REFERENCES

1. Fuccio L, Zagari RM, Eusebi LH, Laterza L, Cennamo V, Ceroni L, et al. Meta-analysis: can Helicobacter pylori eradication treatment reduce the risk for gastric cancer. Ann Intern Med 2009;151:121-128.

2. Moayyedi P, Hunt R, Forman D. Helicobacter pylori eradication for the prevention of gastric neoplasia. Cochrane Database Syst Rev 2006;1:CD005583.

3. Moayyedi P, Hunt RH, Ford AC, Talley NJ, Forman D. Helicobacter pylori Eradication Reduces the Incidence of Gastric Cancer: Results of a Systematic Review of Randomized Controlled Trials. Gastroenterology 2008; 134 (supplement 1): A631-632.

4. Leung WK, Lin S-R, Ching JYL, To K-F, Ng EKW, Chan FKL, et al. Factors predicting progression of gastric intestinal metaplasia: results of a randomised trial on Helicobacter pylori eradication. Gut 2004;53:1244 -1249.

5. Zhou L. Ten-year follow-up study on the incidence of gastric cancer and the pathological changes of gastric mucosa after H. pylori eradication in China. Gastroenterology 2008;134 (suppl 1):A233.

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