Why guidelines are required for the treatment of Helicobacter pylori infection in children

Philip M. Sherman, MD

Richard H. Hunt, MD

Clin Invest Med 1996; 19 (5) : 362-7.

[résumé]


Dr. Sherman is in the Division of Gastroenterology and Nutrition, Hospital for Sick Children, and the departments of Paediatrics and Microbiology, University of Toronto, Toronto, Ont., and Dr. Hunt is in the Division of Gastroenterology, McMaster University Medical Centre, Hamilton, Ont.

Correspondence to: Dr. Philip M. Sherman, Rm. 8411, Hospital for Sick Children, 555 University Ave., Toronto ON M5G 1X8; fax: 416 813-6531


Contents


Abstract

Helicobacter pylori is firmly established as a human pathogen; it fulfils all of Koch's postulates as the infectious agent causing chronic, active (type B) gastritis. Infection is strongly associated with duodenal and gastric ulcer. Recently, gastric mucosal-associated lymphoid tissue lymphoma has been successfully treated by curing H. pylori infection. Because of the evidence that the organism causes chronic gastritis and an increased risk of gastric cancer, it has been classified as a category I carcinogen by the World Health Organization. However, the overwhelming majority of people infected have no symptoms. Current eradication therapy is not ideal; there are treatment failures and substantial side effects. As a result, therapy should be reserved for people with clinical symptoms and complications. The infection, if present, should be treated in patients who have endoscopic evidence of mucosal ulcers in the stomach or duodenum. Current evidence does not support treating the infection to prevent gastric carcinogenesis or to alleviate symptoms of abdominal discomfort in the absence of peptic ulcers.


Résumé

Il est bien établi que l'Hélicobacter pylori est un pathogène humain, qui répond à tous les postulats de Koch en tant qu'agent microbien causant la gastrite chronique active (de type B). Cette infection est fortement associée à l'ulcère duodénal et gastrique. Un lymphome du tissu lymphoïde associé à la muqueuse gastrique a été récemment traité avec succès en éliminant l'infection à H. pylori. L'Organisation mondiale de la santé a classifié H. pylori comme un carcinogène de catégorie 1, puisque ce micro-organisme cause une gastrite chronique et est associé à un risque accru de cancer gastrique. Par contre, la grande majorité des sujets infectés sont asymptomatiques. Le traitement actuel d'éradication n'est pas idéal, puisqu'il y a des échecs thérapeutiques ainsi que des effets secondaires substantiels. En conséquence, le traitement devrait être réservé aux sujets symptomatiques et avec des complications. Si l'infection est présente, elle doit être traitée chez les sujets chez lesquels l'endoscopie démontre des ulcères muqueux à l'estomac ou le duodénum. À l'heure actuelle, les données ne justifient pas le traitement de l'infection à H. pylori dans le but de prévenir le cancer gastrique ou de supprimer les symptômes abdominaux en l'absence d'ulcère peptique.

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Introduction

Helicobacter pylori is an established human pathogen that fulfils each of Koch's postulates as a cause of chronic, active (type B) gastritis.[1] Whether H. pylori is a cause of peptic ulcers is not as well established. Nevertheless, the evidence of causation is compelling.[2] There is a strong epidemiologic association between H. pylori infection and both duodenal ulcers (90% to 95%) and gastric ulcers (60% to 80%) in the absence of concurrent ingestion of nonsteroidal anti-inflammatory drugs (NSAIDs). The most convincing evidence of a role for H. pylori in peptic ulcers is provided by studies that show that ulcer recurrence is reduced from around 70% or 80% of patients not treated to 2.6% of those treated in the year after eradication of the infection from the gastric antrum.[3]

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Pathogenic aspects of H. pylori infection

The precise mechanism by which H. pylori infection causes mucosal ulcers in the gastroduodenal region remains unknown. It is clear that bacterial heterogeneity and host factors are both important in determining the clinical outcome of initial infection. Gastric metaplasia in the duodenum and resulting H. pylori colonization of this site may predispose to duodenal ulcers. In fact, gastric metaplasia is more commonly found in patients with a fasting gastric juice of a pH of less than 2.5.[4] The organism may cause not only gastritis but also mucosal inflammation in the duodenum. Altered levels of gastrin and somatostatin in the gastric mucosa of subjects with H. pylori infection may result from a repertoire of mediators released in response to the infection. There is an increase in both basal and meal-stimulated gastrin, and the area under the curve for gastrin is increased throughout the entire day. Since gastrin is a secretagogue for acid and is also trophic to the parietal cell, it may lead to an increase in the parietal cell mass and an increased production of acid by parietal cells. Moreover, H. pylori infection induces the release of both chemokines (such as interleukin-8) and cytokines (interleukin-6) from infected gastric epithelial cells, setting the stage for inflammatory injury to gastroduodenal mucosa. Previous consideration of a genetic predisposition to peptic ulcers (thought to be caused by autosomal dominant hyperpepsinogenemia I and defects in bicarbonate production in the proximal duodenum) need to be reviewed and revised in the context of this previously unrecognized gastric bacterial pathogen.

Recent findings raise the possibility that only certain H. pylori strains are ulcerogenic. It is suggested that the toxin production and a cytotoxin-associated outer membrane protein found in certain strains are indirect markers of the H. pylori strains that induce peptic ulcers. Most studies conducted in Western countries suggest that the strains of H. pylori that express the Cag A protein are more virulent and are associated with more severe gastritis and with peptic ulcer. Recent data suggest that the strains that produce both the Cag A and the Vac A proteins are associated with peptic ulcer. Vac A is directly ulcerogenic in an animal model.[5] DNA hybridization studies also suggest that ulcer-associated H. pylori isolates are related.

As I mentioned earlier, accumulating evidence points to H. pylori infection of the stomach as the pathogenic cause of most cases of peptic ulcers.[6,7] This conclusion has resulted in a major reassessment of previously held notions about the cause of mucosal ulcers in the stomach and duodenum. It also brings forward the promise of a major advance in therapy, because treatment of H. pylori infection cures most cases of peptic ulcers.[2,8]

Epidemiologic evidence indicates that H. pylori infection is a risk factor for a variety of types of gastric cancer, including carcinoma and mucosal-associated lymphoid tissue (MALT) lymphoma. Acquisition of infection in childhood appears to be a critical risk factor for neoplastic complications. A recent report from China indicates that H. pylori infection occurs earlier in regions with a high prevalence of gastric cancer, and that a greater than usual rate of gastric atrophy is seen in children in these regions.[9] Type III intestinal metaplasia in the gastric mucosa is a known pathological marker for the risk for gastric cancer, although type I intestinal metaplasia does not carry this risk and is more commonly seen in association with H. pylori infection.[10] Eradication of H. pylori infection has been reported to cause regression of intestinal metaplasia and to cure MALT lymphoma. In an animal model, infection with a related Helicobacter species, in conjunction with exposure to a chemical carcinogen, results in an increased frequency of tumours in the infected and inflamed stomach.[11] However, the reason why gastric cancer does not develop in most infected humans is unclear, although the preponderance of type I intestinal metaplasia seen in most cases of H. pylori infection may be one explanation. Similarly, it has not been established whether H. pylori eradication prevents gastric lymphoma and adenocarcinoma, but it is unlikely that a study would be carried out to determine this because of the very long time periods involved.

A provocative and very critical editorial[12] recently questioned the validity of treating H. pylori, given that not all of Koch's postulates have been fulfilled to establish the organism as a human pathogen, at least not as a pathogen causing peptic ulcers and gastric cancer. Moreover, current treatment options are subject to several limitations: failure to eradicate H. pylori because of bacterial resistance to the drugs employed, poor patient compliance with the combination therapy, and an unacceptable rate of side effects.[13] Clearly, novel forms of safe and effective prevention (e.g., a vaccine) or alternative therapy (e.g., nutritional supplements)[14] need to be developed.

Critical reviews do not advocate therapy for all patients with H. pylori infection.[2,13,15] The National Institutes of Health consensus conference held in 1994 advocated treatment for all patients who have an H. pylori infection and (1) a peptic ulcer or (2) a known history of peptic ulcer for which they are taking long-term maintenance therapy.[2] Recently, at least one editorial has advocated an aggressive approach to H. pylori infection in children.[16] A trial of treatment was considered reasonable even in patients with only recurrent abdominal pain. However, a consideration of the spectrum of disease is required in defining indications for therapy.

I now proceed to an assessment of the strength of the data supporting a cause-and-effect relation between H. pylori infection and chronic, active gastritis, duodenal and gastric ulcers and gastric cancer, because these data are important in judging the merits of initiating antibacterial therapy. Any benefits must be balanced, of course, against the costs, including side effects, associated with currently available treatment options.

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Chronic, active gastritis

H. pylori infection is now the accepted cause of chronic, active (type B) gastritis, since it fulfils all of Koch's postulates as the causal agent in this condition.[1] The bacteria cause mucosal inflammation in the previously unaffected antrum in animal models; they have also caused gastritis in several well-documented accidental infections and in two human volunteers.[17] Therefore, a recent suggestion that H. pylori is simply an opportunistic infection is not valid.[12] The question remains, however, whether this human infection requires treatment in every affected patient. Cross-section evaluations of the frequency of infection in given populations have shown that most people with an H. pylori infection are asymptomatic.[1,2] Current evidence suggests that most people remain free of sequelae of the infection although, without treatment, the infection appears to be lifelong. People with H. pylori infection who later have peptic ulcers and gastric cancer should be considered as special targets for intervention; for them, eradication of the organism could prevent or cure disease. However, current knowledge does not permit an accurate identification of the subset of asymptomatic people with H. pylori infection who will go on to have complications of the resulting gastritis. Some authorities recommend the initiation of therapy in all children with an infection, but current treatment options limit the appeal of this proposal.

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Duodenal ulcers

Not all of Koch's postulates have been fulfilled to conclusively establish H. pylori infection and the resulting gastritis as a cause of mucosal ulcers in the duodenum. The absence of documented duodenal ulcers in human volunteers with the infection and in animals infected as part of challenge studies is a significant deficiency in our ability to establish causation. Nonetheless, there is convincing evidence that H. pylori infection is indeed related to duodenal ulcers. The most compelling evidence is the change in the natural history of duodenal ulcers with eradication of the organism. The rate of ulcer recurrence is reduced from 77% after 1 year of follow-up when ulcers are healed with acid-suppressing agents (which do not affect H. pylori status) to less than 3% when H. pylori infection is eradicated (p < 0.0001).[3] This change in the recurrence rate continues for at least 7 years after therapy (the longest reported follow-up period to date) and is evident in both adults and children with duodenal ulcers.[6] The change in the natural history of duodenal ulcers is also clinically relevant because it dramatically alters the rate of recurrence of intestinal hemorrhage and is markedly cost-effective when compared with ulcer-healing regimens alone.[8] Therefore, treatment of patients with an H. pylori infection and endoscopically proven duodenal ulcers is currently recommended.[2,13] Moreover, this approach has strong implications for a marked reduction in the health care costs of duodenal ulcers.[18]

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Gastric ulcers

In adults, in the absence of concurrent use of NSAIDs, rates of gastric ulcer recurrence are reduced from 50% at 1-year follow-up to less than 3% (p < 0.001) when H. pylori is eradicated. A recent report of gastric ulcers developing after H. pylori infection of gnotobiotic piglets also provides support for the role of this infection in ulcers of the gastric mucosa.[19] A consensus conference sponsored by the National Institutes of Health recommended treatment of H. pylori infection in cases of gastric ulcers even if there is a history of recent NSAID ingestion.[2] The issue is contentious, however, because most ulcers of the gastric mucosa involve NSAID or corticosteroid use, without H. pylori infection.[6,7]

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Nonulcer dyspepsia

Whether H. pylori infection and chronic, active gastritis alone cause clinical symptoms remains contentious. The data currently available do not provide compelling support for this view.[1,15,20] Simply identifying H. pylori in a patient with symptoms does not provide evidence, of course, that the infection is the cause of the symptoms, since there is a comparable rate of infection in asymptomatic, age- and community-matched controls. Similarly, resolution of symptoms with therapy is of little significance because the placebo response rate provides a similar frequency in the improvement of symptoms. Current recommendations, therefore, do not support therapy to eradicate H. pylori in the absence of endoscopic evidence of peptic ulcers.[2,13] Nonetheless, many gastroenterologists have seen an excellent response to eradication of H. pylori infection in patients with nonulcer dyspepsia.[16] It must be emphasized that much of the literature upon which these observations are based is fraught with methodologic limitations. For example, the definition of nonulcer dyspepsia may be imprecise, resulting in a heterogeneous group of patients being lumped together. This imprecision could mask the real benefit of therapy in symptomatic patients with an H. pylori infection. In most published studies, the duration of follow-up after intervention is also quite short. This could be an important drawback because at least one report, albeit uncontrolled, indicates that symptomatic improvement is sustained for a long period as a result of therapy.[21] The symptoms of dyspepsia experienced by patients who have acquired H. pylori infection through self-inoculation or inadvertent inoculation via a contaminated endoscope also suggest that infection may play a role in dyspepsia. More carefully defined and controlled studies could broaden current guidelines for treatment.

The results of trials involving children with recurrent abdominal pain are equally inconclusive. Meta-analysis of these studies suggests that there is little or no benefit of therapy, but at least two studies[22,23] contradict this conclusion. A trial of classic triple therapy for this indication has been advocated by at least one pediatric gastroenterologist.[16]

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Gastric cancer

Case­control studies provide epidemiologic evidence that long-standing H. pylori infection and chronic gastritis play a role in the development of a variety of types of gastric cancer, including adenocarcinoma, lymphoma and MALT lymphoma.[1] Nested case­control studies indicate a relative risk of gastric cancer of between 3 and 6 among those with H. pylori infection, with the relative risk rising to about 10 with increased duration of infection.

Cure of the infection results in the regression of MALT lymphoma and of intestinal metaplasia in the stomach. The latter is important if such metaplasia is type III, which is a precursor of adenocarcinoma. It is unclear from these studies whether there is regression of all types of intestinal metaplasia. In patients with MALT lymphoma, H. pylori infection should be eradicated and the patient followed closely in a defined protocol and in collaboration with hematologic oncologists, as needed.

It is not clear whether it is cost-effective or therapeutically justifiable to initiate H. pylori treatment in the hope of preventing cancer that will develop in only a small proportion of all people with an infection. It certainly makes little sense to begin therapy if the patient's only symptom is nonulcer dyspepsia, with the justification that treatment will prevent cancer in the long term. There is no evidence that patients with nonulcer dyspepsia are at a higher risk of cancer than asymptomatic patients with an H. pylori infection. Acquisition of the infection in childhood appears to be a risk factor for gastric cancer. Therefore, some advocate treatment of all children with an infection. However, the cost­benefit ratio of such an aggressive approach has not been established.

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Conclusions

H. pylori infection is associated with a wide variety of other medical conditions, including coronary artery disease, short stature, protein-losing gastropathy and recurring enteric infections.[24] Additional data are required to confirm these observations before considering the merits of instituting currently available treatments for these conditions.

The National Institutes of Health consensus conference wisely chose not to advocate treatment of H. pylori in the absence of documented infection.[2] In these guidelines, treatment was advocated only for patients with endoscopic evidence of mucosal ulcers in the stomach or duodenum. Whether infected patients with nonulcer dyspepsia or symptomatic infection should be treated in an attempt to relieve symptoms and to prevent cancer is less certain. Available data do not provide support for an aggressive approach to the initiation of treatment. Further careful clinical research is obviously required. Current guidelines for initiating therapy to eradicate H. pylori infection (Table 1) may well have to be modified and revised according to expected advances in the field.[25]

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Acknowledgements

Dr. Sherman is the recipient of a career scientist award from the Ontario Ministry of Health. The publication of this article was supported in part by a grant from the Fonds de la recherche en santé du Québec. We would like to thank Astra Pharma Canada for its sponsorship of the invited speakers' program.

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References

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