Skip to main content
Log in

Meta-analysis of randomized controlled trials on the efficacy of probiotics in Helicobacter pylori eradication therapy in children

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

Abstract

The efficacy of probiotics supplementation in children undergoing Helicobacter pylori (H. pylori) eradication therapy remains controversial. This study aimed to meta-analyze whether probiotics supplementation in triple therapy could improve H. pylori eradication rates and reduce therapy-related side effects in children. Electronic databases PubMed and Embase were searched to identify all randomized controlled trials in pediatric patients comparing probiotics supplementation with placebo or no extra intervention in H. pylori eradication therapy. Two authors independently extracted the data. Results were expressed as odds ratios (ORs) and accompanying 95 % confidence intervals (CIs). Stata version 12.0 was used to perform all statistical analyses. Seven studies consisting of 508 pediatric patients were included in our study. The pooled ORs (studies n = 7) of eradication rates by intention-to-treat and per-protocol analysis in the probiotics group versus the control group were 1.96 (95 % CI 1.28–3.02) and 2.25 (95 % CI 1.41–3.57), respectively. The pooled OR (studies n = 5) of incidence of total side effects was 0.32 (95 % CI 0.13–0.79), with significant heterogeneity observed (I 2 = 71.9 %). Conclusion: Probiotics supplementation in triple therapy for H. pylori infection may have beneficial effects on eradication and therapy-related side effects, particularly diarrhea, in children.

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

Access this article

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. Ahmad K, Fatemeh F, Mehri N, Maryam S (2013) Probiotics for the treatment of pediatric Helicobacter pylori infection: a randomized double blind clinical trial. Iran J Pediatr 23:79–84

    PubMed  Google Scholar 

  2. Armuzzi A, Cremonini F, Bartolozzi F, Canducci F, Candelli M, Ojetti V, Cammarota G, Anti M, De Lorenzo A, Pola P, Gasbarrini G, Gasbarrini A (2001) The effect of oral administration of Lactobacillus GG on antibiotic-associated gastrointestinal side-effects during Helicobacter pylori eradication therapy. Aliment Pharmacol Ther 15:163–169

    Article  CAS  PubMed  Google Scholar 

  3. Bell GD, Powell K, Burridge SM, Pallecaros A, Jones PH, Gant PW, Harrison G, Trowell JE (1992) Experience with 'triple' anti-Helicobacter pylori eradication therapy: side effects and the importance of testing the pre-treatment bacterial isolate for metronidazole resistance. Aliment Pharmacol Ther 6:427–435

    Article  CAS  PubMed  Google Scholar 

  4. 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 (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 19:399–408

    PubMed  Google Scholar 

  5. Ertem D (2013) Clinical Practice: Helicobacter pylori infection in childhood. Eur J Pediatr 172:1427–1434

    Article  CAS  PubMed  Google Scholar 

  6. Franceschi F, Cazzato A, Nista EC, Scarpellini E, Roccarina D, Gigante G, Gasbarrini G, Gasbarrini A (2007) Role of probiotics in patients with Helicobacter pylori infection. Helicobacter 12(2):59–63

    Article  PubMed  Google Scholar 

  7. Gessner BD, Bruce MG, Parkinson AJ, Gold BD, Muth PT, Dunaway E, Baggett HC (2005) A randomized trial of triple therapy for pediatric Helicobacter pylori infection and risk factors for treatment failure in a population with a high prevalence of infection. Clin Infect Dis 41:1261–1268

    Article  CAS  PubMed  Google Scholar 

  8. Go MF (2002) Review article: natural history and epidemiology of Helicobacter pylori infection. Aliment Pharmacol Ther 16(Suppl 1):3–15

    Article  PubMed  Google Scholar 

  9. Gold BD, 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  CAS  PubMed  Google Scholar 

  10. Goldman CG, Barrado DA, Balcarce N, Rua EC, Oshiro M, Calcagno ML, Janjetic M, Fuda J, Weill R, Salgueiro MJ, Valencia ME, Zubillaga MB, Boccio JR (2006) Effect of a probiotic food as an adjuvant to triple therapy for eradication of Helicobacter pylori infection in children. Nutrition 22:984–988

    Article  PubMed  Google Scholar 

  11. Gottrand F, Kalach N, Spyckerelle C, Guimber D, Mougenot JF, Tounian P, Lenaerts C, Roquelaure B, Lachaux A, Morali A, Dupont C, Maurage C, Husson MO, Barthelemy P (2001) Omeprazole combined with amoxicillin and clarithromycin in the eradication of Helicobacter pylori in children with gastritis: a prospective randomized double-blind trial. J Pediatr 139:664–668

    Article  CAS  PubMed  Google Scholar 

  12. Hamilton-Miller JM (2003) The role of probiotics in the treatment and prevention of Helicobacter pylori infection. Int J Antimicrob Agents 22:360–366

    Article  CAS  PubMed  Google Scholar 

  13. Higgins JP, Thompson SG, Deeks JJ, Altman DG (2003) Measuring inconsistency in meta-analyses. BMJ 327:557–560

    Article  PubMed  Google Scholar 

  14. Hurduc V, Plesca D, Dragomir D, Sajin M, Vandenplas Y (2009) A randomized, open trial evaluating the effect of Saccharomyces boulardii on the eradication rate of Helicobacter pylori infection in children. Acta Paediatr 98:127–131

    Article  CAS  PubMed  Google Scholar 

  15. Jadad AR, Moore RA, Carroll D, Jenkinson C, Reynolds DJ, Gavaghan DJ, McQuay HJ (1996) Assessing the quality of reports of randomized clinical trials: is blinding necessary? Control Clin Trials 17:1–12

    Article  CAS  PubMed  Google Scholar 

  16. Kawakami E, Ogata SK, Portorreal AC, Magni AM, Pardo ML, Patricio FR (2001) Triple therapy with clarithromycin, amoxicillin and omeprazole for Helicobacter pylori eradication in children and adolescents. Arq Gastroenterol 38:203–206

    Article  CAS  PubMed  Google Scholar 

  17. Kjaergard LL, Villumsen J, Gluud C (2001) Reported methodologic quality and discrepancies between large and small randomized trials in meta-analyses. Ann Intern Med 135:982–989

    Article  CAS  PubMed  Google Scholar 

  18. Lehours P, Yilmaz O (2007) Epidemiology of Helicobacter pylori infection. Helicobacter 12(Suppl 1):1–3

    Article  PubMed  Google Scholar 

  19. Lionetti E, Indrio F, Pavone L, Borrelli G, Cavallo L, Francavilla R (2010) Role of probiotics in pediatric patients with Helicobacter pylori infection: a comprehensive review of the literature. Helicobacter 15:79–87

    Article  CAS  PubMed  Google Scholar 

  20. Lionetti E, Miniello VL, Castellaneta SP, Magista AM, de Canio A, Maurogiovanni G, Ierardi E, Cavallo L, Francavilla R (2006) Lactobacillus reuteri therapy to reduce side-effects during anti-Helicobacter pylori treatment in children: a randomized placebo controlled trial. Aliment Pharmacol Ther 24:1461–1468

    Article  CAS  PubMed  Google Scholar 

  21. Mehri N, Kambiz E, Ahmad K, Fatemeh F, Farzaneh M, Hossein FG, Fatemeh M (2011) The efficacy of a 1-week triple therapy for eradication of Helicobacter pylori infection in children. Arab J Gastroenterol 12:37–39

    Article  CAS  PubMed  Google Scholar 

  22. Myllyluoma E, Veijola L, Ahlroos T, Tynkkynen S, Kankuri E, Vapaatalo H, Rautelin H, Korpela R (2005) Probiotic supplementation improves tolerance to Helicobacter pylori eradication therapy—a placebo-controlled, double-blind randomized pilot study. Aliment Pharmacol Ther 21:1263–1272

    Article  CAS  PubMed  Google Scholar 

  23. Nista EC, Candelli M, Cremonini F, Cazzato IA, Zocco MA, Franceschi F, Cammarota G, Gasbarrini G, Gasbarrini A (2004) Bacillus clausii therapy to reduce side-effects of anti-Helicobacter pylori treatment: randomized, double-blind, placebo controlled trial. Aliment Pharmacol Ther 20:1181–1188

    Article  CAS  PubMed  Google Scholar 

  24. Oderda G, Marinello D, Lerro P, Kuvidi M, De'Angelis GL, Ferzetti A, Cucchiara S, Franco MT, Romano C, Strisciuglio P, Pensabene L (2004) Dual vs. triple therapy for childhood Helicobacter pylori gastritis: a double-blind randomized multicentre trial. Helicobacter 9:293–301

    Article  CAS  PubMed  Google Scholar 

  25. Saneeyan H, Layegh S, Rahimi H (2011) Effectiveness of probiotic on treatment of Helicobacter pylori infection in children. J Isfah Med Sch 29:882–889

    Google Scholar 

  26. Scaccianoce G, Zullo A, Hassan C, Gentili F, Cristofari F, Cardinale V, Gigliotti F, Piglionica D, Morini S (2008) Triple therapies plus different probiotics for Helicobacter pylori eradication. Eur Rev Med Pharmacol Sci 12:251–256

    CAS  PubMed  Google Scholar 

  27. Sykora J, Valeckova K, Amlerova J, Siala K, Dedek P, Watkins S, Varvarovska J, Stozicky F, Pazdiora P, Schwarz J (2005) Effects of a specially designed fermented milk product containing probiotic Lactobacillus casei DN-114 001 and the eradication of H. pylori in children: a prospective randomized double-blind study. J Clin Gastroenterol 39:692–698

    Article  CAS  PubMed  Google Scholar 

  28. Szajewska H, Horvath A, Piwowarczyk A (2010) Meta-analysis: the effects of Saccharomyces boulardii supplementation on Helicobacter pylori eradication rates and side effects during treatment. Aliment Pharmacol Ther 32:1069–1079

    Article  CAS  PubMed  Google Scholar 

  29. 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  CAS  PubMed  Google Scholar 

  30. Tolone S, Pellino V, Vitaliti G, Lanzafame A, Tolone C (2012) Evaluation of Helicobacter pylori eradication in pediatric patients by triple therapy plus lactoferrin and probiotics compared to triple therapy alone. Ital J Pediatr 38:63

    Article  PubMed Central  PubMed  Google Scholar 

  31. Tong JL, Ran ZH, Shen J, Zhang CX, Xiao SD (2007) Meta-analysis: the effect of supplementation with probiotics on eradication rates and adverse events during Helicobacter pylori eradication therapy. Aliment Pharmacol Ther 25:155–168

    Article  CAS  PubMed  Google Scholar 

  32. Uemura N, Okamoto S, Yamamoto S, Matsumura N, Yamaguchi S, Yamakido M, Taniyama K, Sasaki N, Schlemper RJ (2001) Helicobacter pylori infection and the development of gastric cancer. N Engl J Med 345:784–789

    Article  CAS  PubMed  Google Scholar 

  33. Wilhelm SM, Johnson JL, Kale-Pradhan PB (2011) Treating bugs with bugs: the role of probiotics as adjunctive therapy for Helicobacter pylori. Ann Pharmacother 45:960–966

    Article  PubMed  Google Scholar 

  34. Yoon H, Kim N, Kim JY, Park SY, Park JH, Jung HC, Song IS (2011) Effects of multistrain probiotic-containing yogurt on second-line triple therapy for Helicobacter pylori infection. J Gastroenterol Hepatol 26:44–48

    Article  PubMed  Google Scholar 

Download references

Conflict of interest

The authors declare that they have no conflicts of interest.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Xue Qin or Zhi-yu Zeng.

Additional information

Shan Li, Xiu-li Huang, and Jing-zhe Sui contributed equally to this work and should be considered as co-first authors.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Li, S., Huang, Xl., Sui, Jz. et al. Meta-analysis of randomized controlled trials on the efficacy of probiotics in Helicobacter pylori eradication therapy in children. Eur J Pediatr 173, 153–161 (2014). https://doi.org/10.1007/s00431-013-2220-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00431-013-2220-3

Keywords

Navigation