DOI QR코드

DOI QR Code

Updates on the Diagnosis of Helicobacter pylori Infection in Children: What Are the Differences between Adults and Children?

  • Yang, Hye Ran (Department of Pediatrics, Seoul National University Bundang Hospital, Seoul National University College of Medicine)
  • Received : 2016.06.09
  • Accepted : 2016.06.15
  • Published : 2016.06.30

Abstract

Helicobacter pylori infection is acquired mainly during childhood and causes various diseases such as gastritis, peptic ulcer disease, mucosa-associated lymphoid tissue (MALT) lymphoma, and iron deficiency anemia. Although H. pylori infection in children differs from adults in many ways, this is often overlooked in clinical practice. Unlike adults, nodular gastritis may be a pathognomonic endoscopic finding of childhood H. pylori infection. Histopathological findings of gastric tissues are also different in children due to predominance of lymphocytes and plasma cells and the formation of gastric MALT. Although endoscopy is recommended for the initial diagnosis of H. pylori infection, several non-invasive diagnostic tests such as the urea breath test (UBT) and the H. pylori stool antigen test (HpSA) are available and well validated even in children. According to recent data, both the $^{13}C$-UBT and HpSA using enzyme-linked immunosorbent assay are reliable non-invasive tests to determine H. pylori status after eradication therapy, although children younger than 6 years are known to have high false positives. When invasive or noninvasive tests are applied to children to detect H. pylori infection, it should be noted that there are differences between children and adults in diagnosing H. pylori infection.

Keywords

References

  1. Megraud F. Epidemiology of Helicobacter pylori infection. Gastroenterol Clin North Am 1993;22:73-88.
  2. Rothenbacher D, Inceoglu J, Bode G, Brenner H. Acquisition of Helicobacter pylori infection in a high-risk population occurs within the first 2 years of life. J Pediatr 2000;136:744-8.
  3. Valle J, Kekki M, Sipponen P, Ihamaki T, Siurala M. Long-term course and consequences of Helicobacter pylori gastritis. Results of a 32-year follow-up study. Scand J Gastroenterol 1996;31:546-50.
  4. Xia HH, Talley NJ. Natural acquisition and spontaneous elimination of Helicobacter pylori infection: clinical implications. Am J Gastroenterol 1997;92:1780-7.
  5. Koletzko S, Jones NL, Goodman KJ, Gold B, Rowland M, Cadranel S, et al.; H pylori Working Groups of ESPGHAN and NASPGHAN. Evidence-based guidelines from ESPGHAN and NASPGHAN for Helicobacter pylori infection in children. J Pediatr Gastroenterol Nutr 2011;53:230-43.
  6. Thijs JC, van Zwet AA, Thijs WJ, Oey HB, Karrenbeld A, Stellaard F, et al. Diagnostic tests for Helicobacter pylori: a prospective evaluation of their accuracy, without selecting a single test as the gold standard. Am J Gastroenterol 1996;91:2125-9.
  7. Dixon MF, Genta RM, Yardley JH, Correa P. Classification and grading of gastritis. The updated Sydney system. International Workshop on the Histopathology of Gastritis, Houston 1994. Am J Surg Pathol 1996;20:1161-81.
  8. Ganga-Zandzou PS, Michaud L, Vincent P, Husson MO, Wizla-Derambure N, Delassalle EM, et al. Natural outcome of Helicobacter pylori infection in asymptomatic children: a two-year follow-up study. Pediatrics 1999; 104:216-21. https://doi.org/10.1542/peds.104.2.216
  9. Prieto G, Polanco I, Larrauri J, Rota L, Lama R, Carrasco S. Helicobacter pylori infection in children: clinical, endoscopic, and histologic correlations. J Pediatr Gastroenterol Nutr 1992;14:420-5. https://doi.org/10.1097/00005176-199205000-00008
  10. Yang HR, Choi HS, Paik JH, Lee HS. Endoscopic and histologic analysis of gastric mucosa-associated lymphoid tissue in children with Helicobacter pylori infection. J Pediatr Gastroenterol Nutr 2013;57:298-304. https://doi.org/10.1097/MPG.0b013e318298020a
  11. Miyamoto M, Haruma K, Yoshihara M, Hiyama T, Sumioka M, Nishisaka T, et al. Nodular gastritis in adults is caused by Helicobacter pylori infection. Dig Dis Sci 2003;48:968-75. https://doi.org/10.1023/A:1023016000096
  12. Bahu Mda G, da Silveira TR, Maguilnick I, Ulbrich- Kulczynski J. Endoscopic nodular gastritis: an endoscopic indicator of high-grade bacterial colonization and severe gastritis in children with Helicobacter pylori. J Pediatr Gastroenterol Nutr 2003;36:217-22. https://doi.org/10.1097/00005176-200302000-00011
  13. Riddell RH. Pathobiology of Helicobacter pylori infection in children. Can J Gastroenterol 1999;13:599-603. https://doi.org/10.1155/1999/591767
  14. Uhlig HH, Tannapfel A, Mossner J, Jedwilayties S, Deutscher J, Muller DM, et al. Histopathological parameters of Helicobacter pylori-associated gastritis in children and adolescents: comparison with findings in adults. Scand J Gastroenterol 2003;38:701-6. https://doi.org/10.1080/00365520310003039
  15. Gallo N, Zambon CF, Navaglia F, Basso D, Guariso G, Grazia Piva M, et al. Helicobacter pylori infection in children and adults: a single pathogen but a different pathology. Helicobacter 2003;8:21-8.
  16. Dixon MF. Histological responses to Helicobacter pylori infection: gastritis, atrophy and preneoplasia. Baillieres Clin Gastroenterol 1995;9:467-86. https://doi.org/10.1016/0950-3528(95)90043-8
  17. Queiroz DM, Rocha GA, Mendes EN, Carvalho AS, Barbosa AJ, Oliveira CA, et al. Differences in distribution and severity of Helicobacter pylori gastritis in children and adults with duodenal ulcer disease. J Pediatr Gastroenterol Nutr 1991;12:178-81. https://doi.org/10.1097/00005176-199102000-00007
  18. Whitney AE, Guarner J, Hutwagner L, Gold BD. Helicobacter pylori gastritis in children and adults: comparative histopathologic study. Ann Diagn Pathol 2000;4:279-85. https://doi.org/10.1053/adpa.2000.17871
  19. Mitchell HM, Bohane TD, Tobias V, Bullpitt P, Daskalopoulos G, Carrick J, et al. Helicobacter pylori infection in children: potential clues to pathogenesis. J Pediatr Gastroenterol Nutr 1993;16:120-5. https://doi.org/10.1097/00005176-199302000-00004
  20. Meining A, Behrens R, Lehn N, Bayerdorffer E, Stolte M. Different expression of Helicobacter pylori gastritis in children: evidence for a specific pediatric disease? Helicobacter 1996;1:92-7. https://doi.org/10.1111/j.1523-5378.1996.tb00017.x
  21. Kim KM, Oh YL, Ko JS, Choe YH, Seo JK. Histopathology and expression of Ki-67 and cyclooxygenase-2 in childhood Helicobacter pylori gastritis. J Gastroenterol 2004;39:231-7. https://doi.org/10.1007/s00535-003-1282-9
  22. Sipponen P, Kosunen TU, Valle J, Riihela M, Seppala K. Helicobacter pylori infection and chronic gastritis in gastric cancer. J Clin Pathol 1992;45:319-23. https://doi.org/10.1136/jcp.45.4.319
  23. Ma ZQ, Tanizawa T, Nihei Z, Sugihara K, Nakamura K. Follicular gastritis associated with Helicobacter pylori. J Med Dent Sci 2000;47:39-47.
  24. Guarner J, Kalach N, Elitsur Y, Koletzko S. Helicobacter pylori diagnostic tests in children: review of the literature from 1999 to 2009. Eur J Pediatr 2010; 169:15-25. https://doi.org/10.1007/s00431-009-1033-x
  25. Leal YA, Flores LL, Fuentes-Panana EM, Cedillo- Rivera R, Torres J. 13C-urea breath test for the diagnosis of Helicobacter pylori infection in children: a systematic review and meta-analysis. Helicobacter 2011;16:327-37. https://doi.org/10.1111/j.1523-5378.2011.00863.x
  26. Kindermann A, Demmelmair H, Koletzko B, Krauss- Etschmann S, Wiebecke B, Koletzko S. Influence of age on 13C-urea breath test results in children. J Pediatr Gastroenterol Nutr 2000;30:85-91. https://doi.org/10.1097/00005176-200001000-00023
  27. 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: 264-9. https://doi.org/10.1111/j.1440-1746.2004.03541.x
  28. Klein PD, Malaty HM, Czinn SJ, Emmons SC, Martin RF, Graham DY. Normalizing results of 13C-urea breath testing for CO2 production rates in children. J Pediatr Gastroenterol Nutr 1999;29:297-301. https://doi.org/10.1097/00005176-199909000-00011
  29. Yang HR, Ko JS, Seo JK. Does the diagnostic accuracy of the 13C-urea breath test vary with age even after the application of urea hydrolysis rate? Helicobacter 2008;13:239-44. https://doi.org/10.1111/j.1523-5378.2008.00608.x
  30. Jones NL, Sherman PM. Approaching Helicobacter pylori infection in children: level I evidence at last and a word of caution. J Pediatr 2001;139:622-3. https://doi.org/10.1067/mpd.2001.119443
  31. Peng NJ, Lai KH, Liu RS, Lee SC, Tsay DG, Lo CC, et al. Clinical significance of oral urease in diagnosis of Helicobacter pylori infection by [13C]urea breath test. Dig Dis Sci 2001;46:1772-8. https://doi.org/10.1023/A:1010626225949
  32. Konstantopoulos N, Russmann H, Tasch C, Sauerwald T, Demmelmair H, Autenrieth I, et al. Evaluation of the Helicobacter pylori stool antigen test (HpSA) for detection of Helicobacter pylori infection in children. Am J Gastroenterol 2001;96:677-83. https://doi.org/10.1111/j.1572-0241.2001.03603.x
  33. Gosciniak G, Przondo-Mordarska A, Iwanczak B, Blitek A. Helicobacter pylori antigens in stool specimens of gastritis children before and after treatment. J Pediatr Gastroenterol Nutr 2003;36:376-80. https://doi.org/10.1097/00005176-200303000-00015
  34. Koletzko S, Konstantopoulos N, Bosman D, Feydt- Schmidt A, van der Ende A, Kalach N, et al. Evaluation of a novel monoclonal enzyme immunoassay for detection of Helicobacter pylori antigen in stool from children. Gut 2003;52:804-6. https://doi.org/10.1136/gut.52.6.804
  35. Oderda G, Rapa A, Ronchi B, Lerro P, Pastore M, Staiano A, et al. Detection of Helicobacter pylori in stool specimens by non-invasive antigen enzyme immunoassay in children: multicentre Italian study. BMJ 2000;320:347-8. https://doi.org/10.1136/bmj.320.7231.347
  36. Ni YH, Lin JT, Huang SF, Yang JC, Chang MH. Accurate diagnosis of Helicobacter pylori infection by stool antigen test and 6 other currently available tests in children. J Pediatr 2000;136:823-7.
  37. Leal YA, Cedillo-Rivera R, Simon JA, Velazquez JR, Flores LL, Torres J. Utility of stool sample-based tests for the diagnosis of Helicobacter pylori infection in children. J Pediatr Gastroenterol Nutr 2011;52:718-28. https://doi.org/10.1097/MPG.0b013e3182077d33
  38. Zhou X, Su J, Xu G, Zhang G. Accuracy of stool antigen test for the diagnosis of Helicobacter pylori infection in children: a meta-analysis. Clin Res Hepatol Gastroenterol 2014;38:629-38. https://doi.org/10.1016/j.clinre.2014.02.001
  39. Yang HR, Seo JK. Helicobacter pylori stool antigen (HpSA) tests in children before and after eradication therapy: comparison of rapid immunochromatographic assay and HpSA ELISA. Dig Dis Sci 2008;53:2053-8. https://doi.org/10.1007/s10620-007-0131-8
  40. Schwarzer A, Lottspeich C, Russmann H, Ossiander G, Koletzko S. Evaluation of a novel rapid one-step monoclonal chromatographic immunoassay for detection of Helicobacter pylori in stool from children. Eur J Clin Microbiol Infect Dis 2007;26:475-80. https://doi.org/10.1007/s10096-007-0322-4
  41. Kalach N, Nguyen VB, Bergeret M, Boutros N, Dupont C, Raymond J. Usefulness and influence of age of a novel rapid monoclonal enzyme immunoassay stool antigen for the diagnosis of Helicobacter pylori infection in children. Diagn Microbiol Infect Dis 2005;52:157-60. https://doi.org/10.1016/j.diagmicrobio.2005.01.004
  42. Antos D, Crone J, Konstantopoulos N, Koletzko S. Evaluation of a novel rapid one-step immunochromatographic assay for detection of monoclonal Helicobacter pylori antigen in stool samples from children. J Clin Microbiol 2005;43:2598-601. https://doi.org/10.1128/JCM.43.6.2598-2601.2005
  43. Czinn SJ. Serodiagnosis of Helicobacter pylori in pediatric patients. J Pediatr Gastroenterol Nutr 1999;28: 132-4. https://doi.org/10.1097/00005176-199902000-00006
  44. Graham DY, Evans DJ Jr, Peacock J, Baker JT, Schrier WH. Comparison of rapid serological tests (FlexSure HP and QuickVue) with conventional ELISA for detection of Helicobacter pylori infection. Am J Gastroenterol 1996;91:942-8.
  45. 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;28:157-61. https://doi.org/10.1097/00005176-199902000-00012
  46. Leal YA, Flores LL, Garcia-Cortes LB, Cedillo-Rivera R, Torres J. Antibody-based detection tests for the diagnosis of Helicobacter pylori infection in children: a meta-analysis. PLoS One 2008;3:e3751. https://doi.org/10.1371/journal.pone.0003751
  47. Veenendaal RA, Pena AS, Meijer JL, Endtz HP, van der Est MM, van Duijn W, et al. Long term serological surveillance after treatment of Helicobacter pylori infection. Gut 1991;32:1291-4. https://doi.org/10.1136/gut.32.11.1291

Cited by

  1. Characterizing antigenic determinants in Helicobacter pylori CagA capable of detecting serum antibodies in children vol.75, pp.8, 2017, https://doi.org/10.1093/femspd/ftx103
  2. Helicobacter pylori infection in children vol.22, pp.suppl1, 2016, https://doi.org/10.1111/hel.12414
  3. Review: Prevalence and dynamics of Helicobacter pylori infection during childhood vol.22, pp.5, 2016, https://doi.org/10.1111/hel.12399
  4. When isHelicobacter pyloriacquired in populations in developing countries? A birth-cohort study in Bangladeshi children vol.9, pp.3, 2016, https://doi.org/10.1080/19490976.2017.1421887
  5. Helicobacter pylori Infection in Pediatric Patients: Update on Diagnosis and Eradication Strategies vol.20, pp.4, 2016, https://doi.org/10.1007/s40272-018-0296-y
  6. Diagnosis and treatment of Helicobacter pylori in the pediatric population vol.70, pp.5, 2016, https://doi.org/10.23736/s0026-4946.18.05346-x
  7. Diagnosis of Helicobacter pylori Infection in Children and Adolescents in Korea vol.21, pp.4, 2018, https://doi.org/10.5223/pghn.2018.21.4.219
  8. Tailor the management of H. pylori infection in paediatric patients to antimicrobial susceptibility profiles vol.35, pp.3, 2016, https://doi.org/10.1007/s40267-019-00600-4
  9. STOOL ANTIGEN (HPSA) TEST IN DETECTION OF HELICOBACTER PYLORI INFECTION AMONG ADULT DYSPEPTIC PATIENTS IN TRIPOLI, LIBYA vol.5, pp.2, 2016, https://doi.org/10.11603/ijmmr.2413-6077.2019.2.10334
  10. STOOL ANTIGEN (HPSA) TEST IN DETECTION OF HELICOBACTER PYLORI INFECTION AMONG ADULT DYSPEPTIC PATIENTS IN TRIPOLI, LIBYA vol.5, pp.2, 2016, https://doi.org/10.11603/ijmmr.2413-6077.2019.2.10334
  11. The Evolving Role of Mucosal Histology in the Evaluation of Pediatric Functional Dyspepsia: A Review vol.1, pp.1, 2016, https://doi.org/10.3390/gidisord1010013
  12. Helicobacter pylori Infection: Clinical, Endoscopic, and Histological Findings in Lebanese Pediatric Patients vol.2020, pp.None, 2016, https://doi.org/10.1155/2020/4648167
  13. Helicobacter pylori Gastritis in Children—The Link between Endoscopy and Histology vol.9, pp.3, 2020, https://doi.org/10.3390/jcm9030784
  14. Treatment of Helicobacter pylori infection in children: A systematic review vol.8, pp.4, 2016, https://doi.org/10.13105/wjma.v8.i4.292
  15. Changing prevalence of Helicobacter pylori infection in children and adolescents vol.64, pp.1, 2016, https://doi.org/10.3345/cep.2019.01543
  16. Prevalence and risk factors of Helicobacter pylori infection in Wuwei, a high‐risk area for gastric cancer in northwest China: An all‐ages population‐based cross‐sectional stud vol.26, pp.4, 2016, https://doi.org/10.1111/hel.12810