Pediatr Gastroenterol Hepatol Nutr.  2018 Oct;21(4):219-233. 10.5223/pghn.2018.21.4.219.

Diagnosis of Helicobacter pylori Infection in Children and Adolescents in Korea

• Seo JH
• Park JS
• Rhee KH
• Youn HS

• KMID: 2421984
• DOI: http://doi.org/10.5223/pghn.2018.21.4.219

Abstract

Helicobacter pylori plays an important role in the pathogenesis of chronic gastritis, peptic ulcer disease, gastric cancer, and gastric mucosa-associated lymphoid tissue lymphoma. In Korea, the guidelines for the diagnosis and treatment of H. pylori infection in adults were revised in 2013. The European Helicobacter and Microbiota Study Group and Consensus panel released the fifth edition of the Maastricht Consensus Report for the management of H. pylori infection in 2015, and the European Society of Paediatric Gastroenterology, Hepatology and Nutrition and the North American Society of Paediatric Gastroenterology, Hepatology and Nutrition released the updated joint guidelines for children and adolescents in 2016. Considering these recommendations and recent progress in our research and that of other research teams, this study aimed to discuss the diagnostic strategies for H. pylori infection in children and adolescents.

Keyword

Helicobacter pylori; Diagnosis; Guideline; Child

MeSH Terms

Adolescent*
Adult
Child*
Consensus
Diagnosis*
Gastritis
Gastroenterology
Helicobacter pylori*
Helicobacter*
Humans
Joints
Korea*
Lymphoma, B-Cell, Marginal Zone
Microbiota
Peptic Ulcer
Stomach Diseases

Figure

• 

  Fig. 1 A comparison of the results of multiple rapid urease tests (RUTs) between 25 initial RUT-positive (A) and 25 RUT-negative (B) pediatric patients from whom five or more gastric antral biopsy specimens were also available for 13C-urea breath tests revealed that RUTs using one biopsy specimen show a maximum of 62.5% false-negative results.

• 

  Fig. 2 The difference in the positivity rate of rapid urease tests (RUTs) between one and three biopsy specimens obtained from the gastric antrum in the same pediatric patient according to the age groups. The positivity rate of RUTs increased with age irrespective of the number of gastric biopsy specimens. The positivity rate of RUTs with three biopsy specimens was higher than RUTs with one biopsy specimen in patients aged below 10 years of age [20]. GU1: RUT using one biopsy specimen, GU3: RUT using three biopsy specimens.

• 

  Fig. 3 The positivity rate and time to positivity of rapid urease tests (RUTs) in the antrum and body according to age. The positivity rate of RUTs in the antrum was higher in the age group 20 to 29 years compared with that in other three age groups, and the positivity rate of RUTs in the body decreased with increasing age (p<0.0001). The most frequent time to positivity occurred within 1 hour in the age group 20 to 29 years and within 6 to 24 hours in children (p<0.0001). The proportions of positive reactions within 1 hour were similar for the antrum and body in all groups [21].

• 

  Fig. 4 Seropositivity rates of the four commercial enzyme-linked immunosorbent assay kits and immunoblotting according to age. The seropositivity rates increased with age. The seropositivity rates of immunoblotting were higher than those of the ELISA kits, and the discrepancy in the seropositivity rates of anti-Helicobacter pylori immunoglobulin G (IgG) antibody was highest in the 0-to-6-month-old infants [32].

Reference

1. Rhee KH, Youn HS, Baik SC, Lee WK, Cho MJ, Choi HJ, et al. Prevalence of Helicobacter pylori infection in Korea. J Korean Soc Microbiol. 1990; 25:475–490.

2. Banatvala N, Mayo K, Megraud F, Jennings R, Deeks JJ, Feldman RA. The cohort effect and Helicobacter pylori. J Infect Dis. 1993; 168:219–221.

3. Kuipers EJ, Peña AS, van Kamp G, Uyterlinde AM, Pals G, Pels NF, et al. Seroconversion for Helicobacter pylori. Lancet. 1993; 342:328–331.

4. Kim SG, Jung HK, Lee HL, Jang JY, Lee H, Kim CG, et al. Guidelines for the diagnosis and treatment of Helicobacter pylori infection in Korea, 2013 revised edition. Korean J Gastroenterol. 2013; 62:3–26.

5. Malfertheiner P, Megraud F, O'Morain CA, Gisbert JP, Kuipers EJ, Axon AT, et al. Management of Helicobacter pylori infection-the Maastricht V/Florence Consensus Report. Gut. 2017; 66:6–30.

6. Jones NL, Koletzko S, Goodman K, Bontems P, Cadranel S, Casswall T, et al. Joint ESPGHAN/NASPGHAN guidelines for the management of Helicobacter pylori in children and adolescents (Update 2016). J Pediatr Gastroenterol Nutr. 2017; 64:991–1003.

7. Lee JY, Puig A, Kim YB, Shin HJ, Lee JH, Lee SM. Academic burnout profiles in Korean adolescents. Stress Health. 2010; 26:404–416.

8. Deding U, Ejlskov L, Grabas MP, Nielsen BJ, Torp-Pedersen C, Bøggild H. Perceived stress as a risk factor for peptic ulcers: a register-based cohort study. BMC Gastroenterol. 2016; 16:140.

9. Jia K, An L, Wang F, Shi L, Ran X, Wang X, et al. Aggravation of Helicobacter pylori stomach infections in stressed military recruits. J Int Med Res. 2016; 44:367–376.

10. Wang YK, Kuo FC, Liu CJ, Wu MC, Shih HY, Wang SS, et al. Diagnosis of Helicobacter pylori infection: Current options and developments. World J Gastroenterol. 2015; 21:11221–11235.

11. Chey WD, Leontiadis GI, Howden CW, Moss SF. ACG Clinical Guideline: Treatment of Helicobacter pylori infection. Am J Gastroenterol. 2017; 112:212–239.

12. Yang HR. Updates on the diagnosis of Helicobacter pylori infection in children: what are the differences between adults and children? Pediatr Gastroenterol Hepatol Nutr. 2016; 19:96–103.

13. Hidaka N, Nakayama Y, Horiuchi A, Kato S, Sano K. Endoscopic identification of Helicobacter pylori gastritis in children. Dig Endosc. 2010; 22:90–94.

14. Cellini L, Di Campli E, Di Bartolomeo S, Bessa LJ, Baffoni M, Di Giulio M. New transport medium for cultural recovery of Helicobacter pylori. J Clin Microbiol. 2014; 52:4325–4329.

15. Garza-González E, Perez-Perez GI, Maldonado-Garza HJ, Bosques-Padilla FJ. A review of Helicobacter pylori diagnosis, treatment, and methods to detect eradication. World J Gastroenterol. 2014; 20:1438–1449.

16. Kocsmár É, Szirtes I, Kramer Z, Szijártó A, Bene L, Buzás GM, et al. Sensitivity of Helicobacter pylori detection by Giemsa staining is poor in comparison with immunohistochemistry and fluorescent in situ hybridization and strongly depends on inflammatory activity. Helicobacter. 2017; 22:e12387.

17. Kim YK, Lee JS, Kim HW, Lee JH, Youn HS, Ko GH. Detection of Helicobacter pylori in the gastric mucous layer in pediatric patients. Korean J Pathol. 2002; 36:292–295.

18. Midolo P, Marshall BJ. Accurate diagnosis of Helicobacter pylori. Urease tests. Gastroenterol Clin North Am. 2000; 29:871–878.

19. Uotani T, Graham DY. Diagnosis of Helicobacter pylori using the rapid urease test. Ann Transl Med. 2015; 3:9.

20. Seo JH, Park JS, Yeom JS, Lim JY, Park CH, Woo HO, et al. Correlation between positive rate and number of biopsy samples on urease test in childhood Helicobacter pylori infection. J Korean Med Sci. 2014; 29:106–109.

21. Seo JH, Youn HS, Park JJ, Yeom JS, Park JS, Jun JS, et al. Influencing factors to results of the urease test: age, sampling site, histopathologic findings, and density of Helicobacter pylori. Pediatr Gastroenterol Hepatol Nutr. 2013; 16:34–40.

22. Cho YK, Jung YS, Lim JY, Kim YO, Choi MB, Park CH, et al. Validity of polymerase chain reaction in the diagnosis of Helicobacter pylori infection using gastroscopic bilpsy specimens in children. Korean J Gastroenterol. 1998; 31:16–22.

23. Moon DI, Shin EH, Oh HG, Oh JS, Hong S, Chung Y, et al. Usefulness of a Helicobacter pylori stool antigen test for diagnosing H. pylori infected C57BL/6 mice. Lab Anim Res. 2013; 29:27–32.

24. Syrjänen K. False positive and false negative results in diagnosis of Helicobacter pylori infection can be avoided by a panel of serum biomarkers (GastroPanel®). M J Gast. 2017; 2:007.

25. Yang HR, Seo JK. Diagnostic accuracy of the C-urea breath test in children: adjustment of the cut-off value according to age. J Gastroenterol Hepatol. 2005; 20:264–269.

26. Czinn SJ. Serodiagnosis of Helicobacter pylori in pediatric patients. J Pediatr Gastroenterol Nutr. 1999; 28:132–134.

27. de Oliveira AM, Rocha GA, Queiroz DM, Mendes EN, de Carvalho AS, Ferrari TC, et al. Evaluation of enzyme-linked immunosorbent assay for the diagnosis of Helicobacter pylori infection in children from different age groups with and without duodenal ulcer. J Pediatr Gastroenterol Nutr. 1999; 28:157–161.

28. Camorlinga-Ponce M, Torres J, Perez-Perez G, Leal-Herrera Y, Gonzalez-Ortiz B, Madrazo de, et al. Validation of a serologic test for the diagnosis of Helicobacter pylori infection and the immune response to urease and CagA in children. Am J Gastroenterol. 1998; 93:1264–1270.

29. Youn HS, Baik SC, Cho YK, Woo HO, Ahn YO, Kim K, et al. Comparison of Helicobacter pylori infection between Fukuoka, Japan and Chinju, Korea. Helicobacter. 1998; 3:9–14.

30. Seo JH, Lim CW, Park JS, Yeom JS, Lim JY, Jun JS, et al. Correlations between the CagA antigen and serum levels of anti-Helicobacter pylori IgG and IgA in children. J Korean Med Sci. 2016; 31:417–422.

31. Youn HS, Baik SC, Lee WK, Cho MJ, Ryou HH, Choi HJ, et al. Serodiagnosis of Helicobacter pylori infection. J Korean Soc Microbiol. 1990; 25:463–474.

32. Jeong HL, Jung YS, Jun JS, Yeom JS, Park JS, Seo JH, et al. Comparison of four commercial ELISA kits and in-house immunoblotting for diagnosis of Helicobacter pylori infection. Pediatr Gastroenterol Hepatol Nutr. 2012; 15:85–90.

33. Lee SY. New guidelines for Helicobacter pylori treatment: comparisons between Korea and Japan. Korean J Gastroenterol. 2014; 63:151–157.