Skip to main content

Advertisement

SpringerLink
Log in

Clinical Practice: Helicobacter pylori infection in childhood

  • Review
  • Published:
European Journal of Pediatrics Aims and scope Submit manuscript

Abstract

Helicobacter pylori infection is recognised as a cause of gastritis and peptic ulcer disease (PUD) and usually acquired during the first years of life. While there is a decline in the prevalence of H. pylori infection in northern and western European countries, the infection is still common in southern and eastern parts of Europe and Asia. Symptoms of H. pylori-related PUD are nonspecific in children and may include epigastric pain, nausea and/or vomiting, anorexia, iron deficiency anaemia and hematemesis. Besides, only a small proportion of children develop symptoms and clinically relevant gastrointestinal disease. H. pylori infection can be diagnosed either by invasive tests requiring endoscopy and biopsy or non-invasive tests including the 13C-urea breath test, detection of H. pylori antigen in stool and detection of antibodies in serum, urine and saliva. The aim of treatment is at least 90 % eradication rate of the bacteria, and a combination of two antibiotics plus a proton pump inhibitor has been recommended as first-line treatment. However, frequent use of antibiotics during childhood is associated with a decline in eradication rates and the search for new treatment strategies as well. This is an overview of the latest knowledge and evidence-based guidelines regarding clinical presentation, diagnosis and treatment of H. pylori infection in childhood.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

H. pylori :

Helicobacter pylori

13C-UBT:

13C-Urea breath test

MALT:

Mucosa-associated lymphoid tissue

IDA:

Iron deficiency anaemia

RAP:

Recurrent abdominal pain

EIA:

Enzyme immunoassay

RUT:

Rapid urease test

FISH:

Fluorescence in situ hybridization

PUD:

Peptic ulcer disease

PPI:

Proton pump inhibitor

References

  1. Ahmad N, Zakaria WR, Abdullah SA, Mohamed R (2009) Characterization of clarithromycin resistance in Malaysian isolates of Helicobacter pylori. World J Gastroenterol 15:3161

    Article  PubMed  CAS  Google Scholar 

  2. Alvarez A, Moncayo JI, Santacruz JJ, Santacoloma M, Corredor LF, Reinosa E (2009) Antimicrobial susceptibility and mutations involved in clarithromycin resistance in Helicobacter pylori isolates from patients in the western central region of Colombia. Antimicrob Agents Chemother 53:4022–4024

    Article  PubMed  CAS  Google Scholar 

  3. Bakir Ozbey S, Ozakin C, Keskin M (2009) Antibiotic resistance rates of Helicobacter pylori isolates and the comparison of E-test and fluorescent in situ hybridization methods for the detection of clarithromycin resistant strains. Mikrobiyol Bul 43:227–234

    PubMed  CAS  Google Scholar 

  4. Barabino A, Dufour C, Marino CE, Claudiani F, De Alessandri A (1999) Unexplained refractory iron- deficiency anemia associated with Helicobacter pylori gastric infection in children: further clinical evidence. J Pediatr Gastroenterol Nutr 28:116–119

    Article  PubMed  CAS  Google Scholar 

  5. Baysoy G, Ertem D, Ademoglu E, Kotiloglu E, Keskin S, Pehlivanoglu E (2004) Gastric histopathology, iron status and iron deficiency anemia in children with Helicobacter pylori infection. J Pediatr Gastroenterol Nutr 38:146–151

    Article  PubMed  CAS  Google Scholar 

  6. Bellack NR, Koehoorn MW, MacNab YC, Morshed MG (2006) A conceptual model of water's role as a reservoir in Helicobacter pylori transmission: a review of the evidence. Epidemiol Infect 134:439–449

    Article  PubMed  CAS  Google Scholar 

  7. Berger MY, Spee LA, Madderom MB, Pijpers M, van Leeuwen Y (2010) Association between Helicobacter pylori and gastrointestinal symptoms in children. Pediatrics 125:e651–e669

    Article  PubMed  Google Scholar 

  8. Bontems P, Devaster JM, Corvaglia L, Dezsöfi A, Van Den Borre C, Goutier S, Butzler JP, Cadranel S (2001) Twelve year observation of primary and secondary antibiotic-resistant Helicobacter pylori strains in children. Pediatr Infect Dis J 20:1033–1038

    Article  PubMed  CAS  Google Scholar 

  9. Bourke B, Ceponis P, Chiba N, Czinn S, Ferraro R, Fischbach L, Gold B, Hyunh H, Jacobson K, Jones NL, Koletzko S, Lebel S, Moayyedi P, Ridell R, Sherman P, van Zanten S, Beck I, Best L, Boland M, Bursey F, Chaun H, Cooper G, Craig B, Creuzenet C, Critch J, Govender K, Hassall E, Kaplan A, Keelan M, Noad G, Robertson M, Smith L, Stein M, Taylor D, Walters T, Persaud R, Whitaker S, Woodland R, Canadian Helicobacter Study Group (2005) Canadian Helicobacter Study Group Consensus Conference: update on the approach to Helicobacter pylori infection in children and adolescents—an evidence-based evaluation. Can J Gastroenterol 9:399–408

    Google Scholar 

  10. Brenner H, Arndt V, Stegmaier C, Ziegler H, Rothenbacher D (2004) Is Helicobacter pylori infection a necessary condition for noncardiac gastric cancer? Am J Epidemiol 159:252–258

    Article  PubMed  Google Scholar 

  11. Chang WL, Sheu BS, Cheng HC, Yang YJ, Yang HB, Wu JJ (2009) Resistance to metronidazole, clarithromycin and levofloxacin of Helicobacter pylori before and after clarithromycin-based therapy in Taiwan. J Gastroenterol Hepatol 24:1230–1235

    Article  PubMed  CAS  Google Scholar 

  12. Chi H, Bair M-J, Wu M-S, Chiu NC, Hsiao YC, Chang KY (2009) Prevalence of Helicobacter pylori infection in high-school students on Lanyu Island, Taiwan: risk factor analysis and effect on growth. J Formos Med Assoc 108:929–936

    Article  PubMed  Google Scholar 

  13. Dube C, Nkosi TC, Clarke AM, Mkwetshana N, Green E, Ndip RN (2009) Helicobacter pylori antigenemia in an asymptomatic population of Eastern Cape Province, South Africa: public health implications. Rev Environ Health 24:249–255

    PubMed  CAS  Google Scholar 

  14. Dube C, Tanih NF, Ndip RN (2009) Helicobacter pylori in water sources: a global environmental health concern. Rev Environ Health 24:1–14

    Article  PubMed  CAS  Google Scholar 

  15. Elitsur Y, Tolia V, Gilger MA, Reeves-Garcia J, Schmidt-Sommerfeld E, Opekun AR, El-Zimaity H, Graham DY, Enmei K (2009) Urea breath test in children: the United States prospective, multicenter study. Helicobacter 14:134–140

    Article  PubMed  CAS  Google Scholar 

  16. Ford AC, Axon AT (2010) Epidemiology of Helicobacter pylori infection and public health implications. Helicobacter 15(Suppl 1):1–6

    Article  PubMed  Google Scholar 

  17. Francavilla R, Lionetti E, Castellaneta SP, Magistà AM, Boscarelli G, Piscitelli D, Amoruso A, Di Leo A, Miniello VL, Francavilla A, Cavallo L, Ierardi E (2005) Improved efficacy of 10-day sequential treatment for Helicobacter pylori eradication in children: a randomized trial. Gastroenterology 129:1414–1419

    Article  PubMed  CAS  Google Scholar 

  18. Francavilla R, Lionetti E, Castellaneta S, Margiotta M, Piscitelli D, Lorenzo L, Cavallo L, Ierardi E (2010) Clarithromycin resistant genotypes and eradication of H. pylori. Pediatrics 157:228–232

    Article  CAS  Google Scholar 

  19. Fujihashi K, Koga T, van Ginkel FW, Hagiwara Y, McGhee JR (2002) A dilemma for mucosal vaccination: efficacy versus toxicity using enterotoxin-based adjuvants. Vaccine 20:2431–2438

    Article  PubMed  CAS  Google Scholar 

  20. Gatta L, Vakil N, Leandro G, Di Mario F, Vaira D (2009) Sequential therapy or triple therapy for Helicobacter pylori infection: systematic review and meta-analysis of randomized controlled trials in adults and children. Am J Gastroenterol 104:3069–3079

    Article  PubMed  CAS  Google Scholar 

  21. Gold B, Colletti RB, Abbott M, Czinn SJ, Elitsur Y, Hassall E, Macarthur C, Snyder J, Sherman PM (2000) Helicobacter pylori infection in children: recommendations for diagnosis and treatment. J Pediatr Gastroenterol Nutr 31:490–497

    Article  PubMed  CAS  Google Scholar 

  22. Guarner J, Kalach N, Elitsur Y, Koletzko S (2010) Helicobacter pylori diagnostic tests in children: review of the literature from 1999 to 2009. Eur J Pediatr 169:15–25

    Article  PubMed  CAS  Google Scholar 

  23. Guo L, Liu K, Xu G, Li X, Tu J, Tang F, Xing Y, Xi T (2012) Prophylactic and therapeutic efficacy of the epitope vaccine CTB-UA against Helicobacter pylori infection in a BALB/c mice model. Appl Microbiol Biotechnol. doi:10.1007/s00253-012-4122-0

  24. Guy B, Hessler C, Fourage S, Haensler J, Vialon-Lafay E, Rokbi B, Millet MJ (1998) Systemic immunization with urease protects mice against Helicobacter pylori infection. Vaccine 16:850–856

    Article  PubMed  CAS  Google Scholar 

  25. Hickey DK, Aldwell FE, Tan ZY, Bao S, Beagley KW (2009) Transcutaneous immunization with novel lipid-based adjuvants induces protection against gastric Helicobacter pylori infection. Vaccine 27:6983–6990

    Article  PubMed  CAS  Google Scholar 

  26. Hishida A, Matsuo K, Goto Y, Hamajima N (2010) Genetic predisposition to Helicobacter pylori-induced gastric precancerous conditions. World J Gastrointest Oncol 15:369–379

    Article  Google Scholar 

  27. Hojsak I, Kos T, Dumančić J, Mišak Z, Jadrešin O, Jaklin Kekez A, Lukić Grlić A, Kolaček S (2012) Antibiotic resistance of Helicobacter pylori in pediatric patients—10 years' experience. Eur J Pediatr 171:1325–1330

    Article  PubMed  CAS  Google Scholar 

  28. Houben CH, Chiu PW, Lau JY, Lee KH, Ng EK, Tam YH, Yeung CK (2008) Duodenal ulcers dominate acute upper gastrointestinal tract bleeding in childhood: a 10-year experience from Hong Kong. J Dig Dis 9:199–203

    Article  PubMed  Google Scholar 

  29. Hung KH, Sheu BS, Chang WL, Wu HM, Liu CC, Wu JJ (2009) Prevalence of primary fluoroquinolone resistance among clinical isolates of Helicobacter pylori at a University Hospital in Southern Taiwan. Helicobacter 14:61–65

    Article  PubMed  CAS  Google Scholar 

  30. Imrie C (2001) Is Helicobacter pylori infection in childhood a risk factor for gastric cancer? Pediatrics 107:373–380

    Article  PubMed  CAS  Google Scholar 

  31. International Agency for Research on Cancer, World Health Organization (1994) Infection with Helicobacter pylori. In: IARC Working Group on the Evaluation of Carcinogenic Risk to Humans (eds) Schistosomes, liver flukes and Helicobacter pylori, vol 60. AI RC, Lyon, Monogr Eval Carcinog Risks Hum, pp. 177–240

  32. Jafri W, Yakoob J, Abid S, Siddiqui S, Awan S, Nizami SQ (2010) Helicobacter pylori infection in children: population-based age-specific prevalence and risk factors in a developing country. Acta Paediatr 99:279–282

    PubMed  CAS  Google Scholar 

  33. Kato S, Fujimura S (2010) Primary antimicrobial resistance of Helicobacter pylori in children during the past 9 years. Pediatr Int 52:187–190

    Article  PubMed  CAS  Google Scholar 

  34. Koletzko S, Richy F, Bontems P, Crone J, Kalach N, Monteiro ML, Gottrand F, Celinska-Cedro D, Roma-Giannikou E, Orderda G, Kolacek S, Urruzuno P, Martínez-Gómez MJ, Casswall T, Ashorn M, Bodanszky H, Mégraud F (2006) The European Paediatric Task Force on Helicobacter pylori. Prospective multicentre study on antibiotic resistance of Helicobacter pylori strains obtained from children living in Europe. Gut 55:1711–1716

    Article  PubMed  CAS  Google Scholar 

  35. Koletzko S, Jones NL, Goodman KJ, Gold B, Rowland M, Cadranel S, Chong S, Colletti RB, Casswall T, Elitsur Y, Guarner J, Kalach N, Madrazo A, Megraud F, Oderda G, H pylori Working Groups of ESPGHAN and NASPGHAN (2011) Evidence-based guidelines from ESPGHAN and NASPGHAN for Helicobacter pylori infection in children. J Pediatr Gastroenterol Nutr 53:230–243

    PubMed  Google Scholar 

  36. Konno M, Yokota S, Suga T, Takahashi M, Sato K, Fujii N (2008) Predominance of mother-to-child transmission of Helicobacter pylori infection detected by random amplified polymorphic DNA fingerprinting analysis in Japanese families. Pediatr Infect Dis J 27:999–1003

    Article  PubMed  Google Scholar 

  37. Leal YA, Flores LL, García-Cortés LB, Cedillo-Rivera R, Torres J (2008) Antibody-based detection tests for the diagnosis of Helicobacter pylori infection in children: a meta-analysis. PLoS One 3: e3751

    Article  PubMed  Google Scholar 

  38. Madani S, Rabah R, Tolia V (2000) Diagnosis of Helicobacter pylori infection from antral biopsies in pediatric patients: is urease test that reliable? Dig Dis Sci 45:1233–1237

    Article  PubMed  CAS  Google Scholar 

  39. Malfertheiner P, Megraud F, O’Morain CA, Bazzoli F, El-Omar E, Graham D, Hunt R, Rokkas T, Vakil N, Kuipers EJ (2007) Current concepts in the management of Helicobacter pylori infection: the Maastricht III Consensus Report. Gut 56:772–781

    Article  PubMed  CAS  Google Scholar 

  40. Malfertheiner P, Megraud F, O’Morain CA, Atherton J, Axon AT, Bazzoli F, Gensini GF, Gisbert JP, Graham DY, Rokkas T, El-Omar EM, Kuipers EJ, European Helicobacter Study Group. (EHSG) (2012) Management of Helicobacter pylori infection—the Maastricht IV/Florence Consensus Report. Gut 61:646–664

    Article  PubMed  CAS  Google Scholar 

  41. Megraud F (2005) Comparison of non-invasive tests to detect Helicobacter pylori infection in children and adolescents: results of a multicenter European study. J Pediatr 146:198–203

    Article  PubMed  Google Scholar 

  42. Mourad-Baars P, Hussey S, Jones NL (2010) Helicobacter pylori infection and childhood. Helicobacter 15(Suppl 1):53–59

    Article  PubMed  Google Scholar 

  43. Muhsen K, Cohen D (2008) Helicobacter pylori infection and iron stores: a systematic review and meta-analysis. Helicobacter 13:323–340

    Article  PubMed  CAS  Google Scholar 

  44. Nouraie M, Latifi-Navid S, Rezvan H, Radmard AR, Maghsudlu M, Zaer-Rezaii H, Radmard AR, Maghsudlu M, Zaer-Rezaii H, Amini S, Siavoshi F, Malekzadeh R (2009) Childhood hygienic practice and family education status determine the prevalence of Helicobacter pylori infection in Iran. Helicobacter 14:40–46

    Article  PubMed  Google Scholar 

  45. O’Connor A, Gisbert JP, McNamara D, O’Morain C (2010) Treatment of Helicobacter pylori infection 2010. Helicobacter 15(Suppl 1):46–52

    Article  PubMed  Google Scholar 

  46. Oderda G, Shcherbakov P, Bontems P, Urruzuno P, Romano C, Gottrand F, Gómez MJ, Ravelli A, Gandullia P, Roma E, Cadranel S, De Giacomo C, Canani RB, Rutigliano V, Pehlivanoglu E, Kalach N, Roggero P, Celinska-Cedro D, Drumm B, Casswall T, Ashorn M, Arvanitakis SN, European Pediatric Task Force on Helicobacter pylori (2007) Results from the pediatric European register for treatment of Helicobacter pylori (PERTH). Helicobacter 12:150–156

    Article  PubMed  Google Scholar 

  47. Ohata H, Kitauchi S, Yoshimura N, Mugitani K, Iwane M, Nakamura H, Yoshikawa A, Yanaoka K, Arii K, Tamai H, Shimizu Y, Takeshita T, Mohara O, Ichinose M (2004) Progression of chronic atrophic gastritis associated with Helicobacter pylori infection increases the risk of gastric cancer. Int J Cancer 109:138–143

    Article  PubMed  CAS  Google Scholar 

  48. Ozden A, Bozdayi G, Ozkan M, Köse S (2004) Changes in the seroepidemiological pattern of Helicobacter pylori infection over the last 10 years. Turk J Gastroenterol 15(3):156–158

    PubMed  Google Scholar 

  49. Ozen A, Ertem D, Pehlivanoglu E (2006) Natural history and symptomatology of Helicobacter pylori in childhood and factors determining the epidemiology of infection. J Pediatr Gastroenterol Nutr 42:398–404

    Article  PubMed  Google Scholar 

  50. Qu XH, Huang XL, Xiong P, Zhu CY, Huang YL, Lu LG, Sun X, Rong L, Zhong L, Sun DY, Lin H, Cai MC, Chen ZW, Hu B, Wu LM, Jiang YB, Yan WL (2010) Does Helicobacter pylori infection play a role in iron deficiency anemia? A meta-analysis. World J Gastroenterol 16:886–896

    PubMed  CAS  Google Scholar 

  51. Raguza D, Machado RS, Ogata SK, Granato CF, Patrício FR, Kawakami E (2010) Validation of a monoclonal stool antigen test for diagnosing Helicobacter pylori infection in young children. J Pediatr Gastroenterol Nutr 50:400–403

    PubMed  Google Scholar 

  52. Rupnow MF, Chang AH, Shachter RD, Owens DK, Parsonnet J (2009) Cost-effectiveness of a potential prophylactic Helicobacter pylori vaccine in the United States. J Infect Dis 200:1311–1317

    Article  PubMed  Google Scholar 

  53. Santos IS, Boccio J, Davidsson L, Hernandez-Triana M, Huanca-Sardinas E, Janjetic M, Moya-Camarena SY, Paez-Valery MC, Ruiz-Alvarez V, Valencia ME, Valle NC, Vargas-Pinto G, Solano L, Thomas J (2009) Helicobacter pylori is not associated with anaemia in Latin America: results from Argentina, Brazil, Bolivia, Cuba, Mexico and Venezuela. Public Health Nutr 12:1862–1870

    Article  PubMed  Google Scholar 

  54. Selgrad M, Bornschein J, Rokkas T, Malfertheiner P (2010) Clinical aspects of gastric cancer and Helicobacter pylori—screening, prevention, and treatment. Helicobacter 15(Suppl 1):40–45

    Article  PubMed  Google Scholar 

  55. Sherman P, Hassall E, Hunt RH, Fallone CA, Veldhuyzen Van Zanten S, Thomson AB (1999) Canadian Helicobacter Study Group Consensus Conference on the approach to Helicobacter pylori infection in children and adolescents. Can J Gastroenterol 13:553–559

    PubMed  CAS  Google Scholar 

  56. Sykora J, Siala K, Varvarovska J, Pazdiora P, Pomahacová R, Huml M (2009) Epidemiology of Helicobacter pylori infection in asymptomatic children: a prospective population-based study from the Czech Republic. Application of a monoclonal-based antigen-in-stool enzyme immunoassay. Helicobacter 14:286–297

    Article  PubMed  Google Scholar 

  57. Szajewska H, Albrecht P, Topczewska-Cabanek A (2009) Randomized, double-blind, placebo-controlled trial: effect of lactobacillus GG supplementation on Helicobacter pylori eradication rates and side effects during treatment in children. J Pediatr Gastroenterol Nutr 48:431–436

    Article  PubMed  CAS  Google Scholar 

  58. Tam YH, Yeung CK, Lee KH, Sihoe JD, Chan KW, Cheung ST, Mou JW (2008) A population-based study of Helicobacter pylori infection in Chinese children resident in Hong Kong: prevalence and potential risk factors. Helicobacter 13:219–224

    Article  PubMed  Google Scholar 

  59. Tkachenko MA, Zhannat NZ, Erman LV, Blashenkova EL, Isachenko SV, Isachenko OB, Graham DY, Malaty HM (2007) Dramatic changes in the prevalence of Helicobacter pylori infection during childhood: a 10-year follow-up study in Russia. J Pediatr Gastroenterol Nutr 45:428–432

    Article  PubMed  Google Scholar 

  60. Vandenplas Y, Brunser O, Szajewska H (2009) Saccharomyces boulardii in childhood. Eur J Pediatr 168:253–265

    Article  PubMed  Google Scholar 

  61. Weyermann M, Rothenbacher D, Brenner H (2009) Acquisition of Helicobacter pylori infection in early childhood: independent contributions of infected mothers, fathers, and siblings. Am J Gastroenterol 104:182–189

    Article  PubMed  Google Scholar 

  62. Wu DC, Wu IC, Wang SW et al (2006) Comparison of stool enzyme immunoassay and immunochromatographic method for detecting Helicobacter pylori antigens before and after eradication. Diagn Microbiol Infect Dis 56:373–378

    Article  PubMed  CAS  Google Scholar 

  63. Yang HR, Ko JS, Seo JK (2008) Does the diagnostic accuracy of the 13C-urea breath test vary with age even after the application of urea hydrolysis rate? Helicobacter 13:239–244

    Article  PubMed  CAS  Google Scholar 

  64. Yucel T, Aygin D, Sen S, Yucel O (2008) The prevalence of Helicobacter pylori and related factors among university students in Turkey. Jpn J Infect Dis 61:179–183

    PubMed  Google Scholar 

Download references

Conflict of interest

The author declares that there is no conflict of interest and no financial relationship that might have influenced the present work.

Author information

Authors and Affiliations

  1. Division of Pediatric Gastroenterology, Hepatology and Nutrition, Marmara University School of Medicine, Fevzi Çakmak Mah. Mimar Sinan Cad. No 41, Pendik, İstanbul, Turkey

    Deniz Ertem

Authors
  1. Deniz Ertem
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Deniz Ertem.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ertem, D. Clinical Practice: Helicobacter pylori infection in childhood. Eur J Pediatr 172, 1427–1434 (2013). https://doi.org/10.1007/s00431-012-1823-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00431-012-1823-4

Keywords

Search

Navigation