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Treatment of Helicobacter pylori Gastritis Improves Dyspeptic Symptoms in Children

Uc, Aliye*; Chong, Sonny K. F.

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Journal of Pediatric Gastroenterology and Nutrition: March 2002 - Volume 34 - Issue 3 - p 281-285
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Helicobacter pylori causes chronic active or atrophic gastritis, gastric or duodenal ulcers in humans. Infection with H. pylori has also been linked to gastric adenocarcinoma, lymphoma, and in some studies with nonulcer dyspepsia (NUD) (1,2). H. pylori bacteria colonize the human stomach, especially during childhood, and the majority of infected subjects remain asymptomatic (3,4). In adults, treatment of H. pylori infection is only recommended for patients with active gastric or duodenal ulcers (5,6). The treatment of H. pylori infection in patients with NUD has not been recommended because of inconclusive data in the literature (7). It is not known whether similar guidelines can be applied to children because the prevalence of peptic ulcer disease in childhood is estimated to be much lower than in adults (8). Guidelines developed by the Canadian Helicobacter Study Group for the management of pediatric H. pylori infection recommend diagnostic tests only in children who are most likely to benefit from treatment, such as those likely to have peptic ulcer disease (9). The North American Society for Pediatric Gastroenterology, Hepatology and Nutrition has recently published a medical position statement to review the current recommendations for the diagnosis and treatment of H. pylori (10). According to these guidelines, the treatment of H. pylori is recommended if the microorganism is seen in children with duodenal or gastric ulcers, mucosa-associated lymphoid tissue (MALT) lymphoma and atrophic gastritis with intestinal metaplasia. The treatment of H. pylori–associated gastritis is left to the judgment of the clinician because there is insufficient evidence to support either initiating or withholding eradication treatment in this situation.

Dyspepsia is characterized by pain or discomfort centered in the upper abdomen (11). Discomfort may be described as fullness, early satiety, bloating, belching, nausea, or vomiting. The majority of adult patients with dyspepsia have no evidence of peptic ulceration or structural disease (other than gastritis) that can explain the symptoms. This group of patients has been labeled as having functional or NUD (11). If the appropriate tests are performed, between 30% and 60% of patients with NUD will be found to have H. pylori infection (12–14). Whether eradication of H. pylori infection results in improvement of dyspeptic symptoms in adults is controversial (15,16).

The relation of chronic, recurrent abdominal pain in childhood with H. pylori infection is not clear (17). Pediatric studies are limited by the lack of a clear definition for recurrent abdominal pain or by the use of nonspecific criteria as proposed by Apley and Naish (18) for the diagnosis of chronic abdominal pain. The cohort for these studies invariably included children who were referred to tertiary hospital gastroenterology clinics, which in itself created a selection bias (19–27). The purpose of this study was to determine the response of dyspeptic symptoms to the treatment of H. pylori gastritis with a symptom-based questionnaire.


Patients with dyspeptic symptoms in a pediatric clinic were evaluated by diagnostic upper gastrointestinal endoscopy to rule out peptic ulcer disease. Sixteen patients with H. pylori gastritis and symptoms of dyspepsia, without the evidence of duodenal or gastric ulcers, were recruited for study at 2 to 4 weeks and 9.7 ± 1.4 months after treatment.

All patients underwent upper gastrointestinal endoscopy with use of an Olympus GIF-100 endoscope (Olympus Inc., Melville, NY, U.S.A.) and mucosal biopsy specimens were obtained from the duodenum, the antrum, and the distal esophagus. The diagnosis of H. pylori gastritis was made based on CLO test (Delta West, Western Australia) and histologic evaluation with hematoxylin and eosin staining. In one patient, Warthin-Starry silver staining was also performed to confirm the diagnosis. All patients were treated with a proton pump inhibitor (PPI), omeprazole (1 mg · kg−1 · d−1, up to a maximum of 20 mg two times daily), and one patient received lansoprazole (15 mg two times daily) for 2 to 8 weeks. For 2 weeks patients also received clarithromycin (15 mg · kg−1 · d−1, maximum of 500 mg two times daily) and amoxicillin (45 mg · kg−1 · d−1, maximum of 1 g two times daily). The eradication of H. pylori infection was shown serologically in five patients who had a negative H. pylori antibody titer 10.8 ± 4.3 months after treatment. Values are represented as mean ± SEM.

Assessment of Symptoms

Using a dyspepsia questionnaire, derived from a previous study of adult patients by Macarthur et al. (28), patient symptoms were evaluated before treatment and at 2 to 4 weeks and 9.7 ± 1.4 months (range, 2–24 months) after treatment. The dyspepsia questionnaire was administered by one of the authors during a clinic visit or a phone interview. The symptoms elicited included epigastric pain (nighttime and daytime); nausea and/or vomiting, anorexia and/or early satiety, and regurgitation. These symptoms were scored numerically for frequency and severity from 0 to 4. Frequency was scored as follows: 0 = absent, 1 = 1 day per week, 2 = several times per week. Severity was scored as follows: 0 = absent, 1 = present but not interfering with daily activities, 2 = present and interfering with daily activities. In this scoring system, dyspepsia score ranged from 0 to 20. A total symptom score (TSS) was calculated for each patient. The effect of H. pylori treatment on the total symptom score was analyzed using the Student t test. Values are expressed as mean total symptom score ± SE. P values less than 0.01 was taken considered significant in all analyses.


The clinical characteristics of these patients are listed in Table 1. Of 16 patients, 5 were boys and 11 were girls. Except for two white children, all were black with a mean age of 14 ± 1.2 years (age range, 7–20 years). Their main symptom was epigastric pain with a mean duration of 10.3 ± 4.9 months. Three patients had periumbilical pain and two other patients had right upper quadrant pain in addition to epigastric pain. Two patients reported epigastric, right and left upper quadrant pain. Nocturnal pain was present in 10 patients, and pain improved with eating in seven patients. All patients except one had other dyspeptic symptoms, such as nausea, vomiting or both; anorexia, early satiety, or both; and belching, flatulence, or both. Two patients had acute onset of hematemesis. Three patients described a history of weight loss of 2.5 kg or less within 3 months. Physical examination results were normal in all patients, with the exception of epigastric tenderness in six patients.

Clinical findings of 16 patients with dyspepsia and Helicobacter pylori gastritis

Upper gastrointestinal endoscopy showed nodular antral gastritis in all 16 patients. The CLO test results were positive in 14 patients. Histologic examination confirmed chronic active gastritis with spiral-shaped organisms in the antrum of all patients. Four patients had mild esophagitis and two had mild duodenitis, which was determined from biopsy specimens. These six patients received PPIs for longer than 2 weeks.

In the patients treated for H. pylori gastritis, mean total symptom score decreased significantly at 2 to 4 weeks' follow-up after the treatment (12.6 ± 0.9 vs. 2.1 ± 0.5 weeks;P < 0.001), and the score remained low (2.9 ± 0.7;P < 0.001) at an average follow-up time of 9.7 ± 1.4 months (range, 2–24 months;Fig. 1). The individual pre-and posttreatment total symptom scores are shown in Table 2.

Pre-and posttreatment TSS of 16 patients with Helicobacter pylori gastritis
FIG. 1.
FIG. 1.:
Mean total symptom scores of 16 patients. In patients treated for H. pylori gastritis, mean total symptom score decreased significantly at 2 to 4 weeks after the treatment, and it remained low at a follow-up of 9.7 ± 1.4 months (* P < 0.001 if compared with pretreatment values).

Two patients had a flare-up of their symptoms 9 and 14 months after treatment of H. pylori infection. One patient began reporting abdominal pain 9 months after the standard treatment. Omeprazole therapy was restarted at 20 mg daily, and the symptoms improved. The patient discontinued the medication after 1 month and her dyspepsia score has remained low. Another patient was restudied by use of repeat endoscopy, which showed mild antral nodularity and negative CLO test results. Histology showed scattered small foci of inflammation in otherwise normal fundic and antral mucosa, and there was no evidence of esophagitis. H. pylori was not seen during histology by hematoxylin and eosin and silver staining. The patient's symptoms were not improved after a 2-week repeat course of antibiotics and PPI for a presumed H. pylori infection. She had some relief of dyspeptic symptoms after finishing an 8-week course of a PPI.

One other patient who had only a 50% reduction in dyspepsia score had gastroesophageal reflux (GER)–type symptoms initially. Results of esophageal biopsies showed mild esophagitis. The patient's dyspeptic symptoms responded to antireflux precautions and omeprazole. Three patients with histologically proven esophagitis did not have a recurrence of dyspeptic symptoms at follow-up. In eight patients, dyspepsia symptoms disappeared. Five patients had dyspepsia scores of 2, and one patient's score was 4 at 2 months' follow-up (Table 2). In five patients who returned for blood drawing, the eradication of H. pylori infection was shown by negative results of serology.


Although dyspepsia and H. pylori infection are common in the general population (7), current data in the literature regarding a causal association between H. pylori gastritis and dyspepsia are conflicting. It is uncertain whether eradication of the infection leads to an improvement of symptoms (29). Many studies to date have not been designed to include double-blind placebo controls (30). Moreover, these studies have not used age, race, and sex-matched controls.

In pediatric studies to date, dyspeptic symptoms are rarely described and the criteria to define recurrent abdominal pain are either unclear or nonspecific (e.g., Apley and Naish and criteria for recurrent abdominal pain) (18). One meta-analysis study did not identify strong evidence for an association between H. pylori infection and recurrent abdominal pain (17). In another study, dyspeptic children were tested and treated for H. pylori infection with colloidal bismuth subcitrate and tinidazole (31). No difference in symptoms between treatment successes or failures was shown; however, the H. pylori eradication rate was low (67%) and the dyspepsia symptoms were not scored using a validated questionnaire. The absence of significant response to treatment in that study could be related to an increase in the number of patients with GER after the treatment of H. pylori infection. This was one of the rare pediatric studies in which the localization of abdominal pain and dyspeptic symptoms were better defined.

There are more specific criteria in defining chronic or recurrent abdominal pain in childhood (32). Newer diagnostic criteria classifying childhood functional abdominal pain are not only based on the duration of symptoms, but also on the location of the abdominal pain, the presence of dyspeptic symptoms, the consistency and the frequency of the bowel movements, and the relief of pain with defecation. More pediatric studies are needed that use specific criteria to define chronic functional abdominal pain to study a causal association between NUD and H. pylori infection in children.

This study summarizes a clinical observation and is not a placebo-controlled, double-blinded study. However, we believe it was still a valid observation because patients were followed-up for several months, and recurrence of symptoms developed in only 2 of 16 patients. It would be ideal to have confirmed the cure of the infection in all patients who have responded to the treatment of H. pylori infection. As it is outlined in the current medical position statement of NASPGHAN (10), the gold standard for the diagnosis of H. pylori infection is the histopathologic evaluation of stomach biopsy specimens obtained by use of esophagogastroduodenoscopy. However, this requires an invasive procedure, which is difficult to justify in asymptomatic children. Urea breath testing and stool H. pylori antigens are not standardized for children (10) and were not available for us to use in Arkansas.

It could be argued that longer duration of PPI in six patients with additional diagnoses were responsible for the improvement in the dyspepsia scores. However, five of these patients were followed-up for 11 months or more and continued to do well. Therefore, we do not think that the sustained response in these patients was related to an 8-week use of a PPI.

Feldman et al. (33) reported that beyond the first year of therapy, undetectable antibody levels could be accurately used for confirmation of a cure in individuals who were initially seropositive. By the time this article was prepared, only six patients were beyond 1 year of treatment, and in five patients who returned for blood drawing, antibody levels were undetectable. Although serology is not a perfect tool for the diagnosis or confirmation of a cure for H. pylori infection, it may be the only noninvasive tool until other tests (urea breath testing and stool H. pylori antigen) are standardized for children.

The majority of our patients were black. The effect of race in the treatment response to H. pylori infection has not been investigated. Two recent articles published in this journal reported a high prevalence of H. pylori infection in Turkish and minority non-Swiss children with recurrent abdominal pain (34,35). The pain resolved or ameliorated in more than 70% of children treated with clarithromycin, amoxicillin, and PPI therapy. These studies are supportive of our hypothesis and suggest the possibility of different treatment responses in various ethnic and racial backgrounds. The authors of these studies did not specify the location, nature, and other characteristics of the abdominal pain, and they did not use a dyspepsia scoring system to measure the response as we did.

Treatment guidelines for adults cannot be easily adapted to children because many factors that can influence the natural history of H. pylori infection in children are different than those in adults: 1) Duodenal ulcers with or without H. pylori are rare in childhood (8). 2) Nodularity of the antral mucosa in the stomach as a result of H. pylori infection is common in children and rarely seen in adults (36,37). 3) The active component of the inflammation is neutrophils in adults and lymphocytes in children (38). A Working Group Meeting of the International Agency for Research on Cancer held in Lyon in 1994, in affiliation with the World Health Organization, concluded that there was sufficient evidence to suggest that H. pylori was a group I carcinogen (39). Therefore, long-term consequences of exposing a child to the potential carcinogenic effects of H. pylori are unknown.

It could be argued that the incidence of GER would increase after eradication of H. pylori infection. In the current study, one patient who continued to have dyspeptic symptoms after treatment has had mild esophagitis, confirmed during histology, and his GER symptoms increased after eradication of H. pylori. In this patient, the eradication of H. pylori was confirmed by serology. Conversely, three other patients who had biopsy-confirmed esophagitis continued to do well. Depending on the type or the extent of gastritis, H. pylori may increase (antral gastritis) or decrease (pangastritis with or without mucosal atrophy) the likelihood of GER. If H. pylori causes pangastritis and hypochlorhydria, its eradication can restore the gastric acid secretion and make the GER worse. However, the incidence of pangastritis and hypochlorhydria in children has not been investigated, and the long-term effects of H. pylori infection on the natural history of GER are unknown.

In conclusion, in our study, 16 patients who had chronic dyspeptic symptoms and seen in a pediatric clinic were tested and treated for H. pylori gastritis. All showed significant improvement after treatment of the infection. In eight patients, dyspeptic symptoms disappeared. Two patients had a flare-up of their symptoms 9 and 14 months after their infection was treated. One patient did not have evidence of recurrent H. pylori infection. We conclude that treatment of H. pylori gastritis can improve chronic dyspeptic symptoms in children.


1. Anonymous. The report of the Digestive Health Initiative International Update Conference on Helicobacter pylori. Gastroenterology 1997;113:S4–8.
2. Blecker U, Gold BD. Gastritis and peptic ulcer disease in childhood. Eur J Pediatr 1999; 158:541–6.
3. Vandenplas Y, Blecker U. Helicobacter pylori infection in children. Acta Paediatr 1998; 87:1105–12.
4. Czinn SJ, Glassman MS. Helicobacter pylori in infants and children. Adv Pediatr Infect Dis 1996; 11:389–401.
5. NIH Consensus Development Model on Helicobacter pylori in peptic ulcer disease. JAMA 1994;272:65–9.
6. European Helicobacter pylori Study Group. Current European concepts in the management of H. pylori infection: The Maastricht Consensus Report. Gut 1997;41:8–13.
7. Talley NJ, Hunt RH. What role does Helicobacter pylori play in dyspepsia and nonulcer dyspepsia? Arguments for and against H. pylori being associated with dyspeptic symptoms. Gastroenterology 1997; 113:S67–77.
8. Drumm B, Rhoads JM, Stringer DA, et al. Peptic ulcer disease in children: etiology, clinical findings, and clinical course. Pediatrics 1988; 82:410–4.
9. Sherman P, Hassall E, Hunt RH, et al. Canadian Helicobacter Study Group Consensus Conference on the Approach to Helicobacter pylori Infection in Children and Adolescents. Can J Gastroenterol 1999; 13:553–9.
10. Gold BD, Abbott M, Colletti RB, et al. Helicobacter pylori infection in children: recommendations for diagnosis and treatment. J Pediatr Gastroenterol Nutr 2000; 31:490–7.
11. Talley NJ, Colin-Jones D, Koch KL, et al. Functional dyspepsia: a classification with guidelines for diagnosis and management. Gastroenterol Int 1991; 4:145–60.
12. Strauss RM, Wang TC, Kelsey PB, et al. Association of Helicobacter pylori infection with dyspeptic symptoms in patients undergoing gastroduodenoscopy. Am J Med 1990; 89:464–9.
13. Rokkas T, Anggiansah A, Uzoechina E, et al. Campylobacter pylori and non-ulcer dyspepsia. Am J Gastroenterol 1987; 82:1149–52
14. Bernersen B, Johnsen R, Bostad L, et al. Is Helicobacter pylori a cause of dyspepsia? BMJ 1992; 304:1276–9.
15. Blum AL, Talley NJ, O'Morain C, et al. Lack of effect of treating Helicobacter pylori infection in patients with nonulcer dyspepsia. N Eng J Med 1998; 339:1875–81.
16. McColl K, Murray L, El-Omar E, et al. Symptomatic benefit from eradication Helicobacter pylori infection in patients with non-ulcer dyspepsia. N Eng J Med 1998; 339:1869–74.
17. Macarthur C, Saunders N, Feldman W. Helicobacter pylori, gastroduodenal disease, and recurrent abdominal pain in children. JAMA 1995; 273:729–34.
18. Apley J, Naish N. Recurrent abdominal pain: a field survey of 1000 school children. Arch Dis Child 1958; 33:165–70.
19. Fiedorek SC, Casteel HB, Pumphrey CL, et al. The role of Helicobacter pylori in recurrent, functional abdominal pain in children. Am J Gastroenterol 1992; 87:347–9.
20. van der Meer SB, Forget PP, Loffeld RJ, et al. The prevalence of Helicobacter pylori serum antibodies in children with recurrent abdominal pain. Eur J Pediatr 1992; 151:799–801.
21. Mavromichalis I, Zaramboukas T, Richman PI, et al. Recurrent abdominal pain of gastrointestinal origin. Eur J Pediatr 1992; 151:560–3.
22. Conti-Nibali S, Sferlazzas C, Fera MT, et al. Helicobacter pylori infection: a simplified diagnostic approach. Am J Gastroenterol 1990; 85:1573–5.
23. Bujanover Y, Konikoff F, Baratz M. Nodular gastritis and Helicobacter pylori. J Pediatr Gastroenterol Nutr 1990; 11:41–4
24. Ashorn M, Maki M, Ruuska T, et al. Upper gastrointestinal endoscopy in recurrent abdominal pain of childhood. J Pediatr Gastroenterol Nutr 1993; 16:273–7.
25. Crabtree JE, Mahony MJ, Taylor JD, et al. Immune responses to Helicobacter pylori in children with recurrent abdominal pain. J Clin Pathol 1991; 44:768–71.
26. Hardikar W, Feekery C, Smith A, et al. Helicobacter pylori and recurrent abdominal pain in children. J Pediatr Gastroenterol Nutr 1996; 22:148–52.
27. Chong SKF, Lou Q, Asnicar MA, et al. Helicobacter pylori infection in recurrent abdominal pain in childhood: Comparison of diagnostic tests and therapy. Pediatrics 1995: 96:211–5.
28. McCarthy C, Patchett S, Collins RM, et al. Long-term prospective study of Helicobacter pylori in nonulcer dyspepsia. Dig Dis Sci 1995; 40:114–9.
29. Huang J, Hunt RH. Eradication of Helicobacter pylori infection in the management of patients with dyspepsia and non-ulcer dyspepsia. Yale J Biol Med 1998; 71:125–33.
30. Talley NJ. A critique of therapeutic trials in Helicobacter pylori-positive functional dyspepsia. Gastroenterology 1994; 106:1174–83.
31. Ashorn M, Ruuska T, Karikoski R, et al. Helicobacter pylori gastritis in dyspeptic children: a long-term follow-up after treatment with colloidal bismuth subcitrate and tinidazole. Scand J Gastroenterol 1994; 29:203–8.
32. Rasquin-Weber A, Hyman PE, Cucchiara S, et al. Childhood functional gastrointestinal disorders. Gut 1999; 45 (suppl II): 1160–8.
33. Feldman M, Cryer B, Lee E, et al. Role of seroconversion in confirming cure of Helicobacter pylori infection. JAMA 1998; 280:363–5.
34. Saltik IN, Kocak N, Ozen H, et al. Helicobacter pylori infection in Turkish children with recurrent abdominal pain. J Pediatr Gastroenterol Nutr 2001; 32:405–12.
35. Frank F, Stricker T, Stallmach T, et al. Helicobacter pylori infection in recurrent abdominal pain. J Pediatr Gastroenterol Nutr 2000; 31:424–7.
36. Hassall E, Dimmick JE. Unique features of Helicobacter pylori disease in children. Dig Dis Sci 1991; 36:417–23.
37. Mitchell HM, Bohane TD, Tobias V, et al. Helicobacter pylori infection in children: potential clues to pathogenesis. J Pediatr Gastroenterol Nutr 1993; 16:120–5.
38. Bujanover Y, Reif S, Yahav J. Helicobacter pylori and peptic disease in the pediatric patient. Ped Clin N Am 1996; 43:213–34
39. International Agency for Research of Cancer Monographs on the Evaluation of Carcinogenic Risks to Humans. Infection with Helicobacter pylori. Vol 61. Lyon: International Agency for Research on Cancer 1994:177–240.

Dyspepsia; Helicobacter pylori; Gastritis; Primary care

© 2002 Lippincott Williams & Wilkins, Inc.