Download PDF
J Pediatr Infect Dis 2022; 17(06): 297-302
DOI: 10.1055/s-0042-1758142
Original Article

Assessment of Efficacy and Adverse Effects of Bismuth-Based Treatment Combined with Bifidobacterium Lactis for Eradication of Helicobacter Pylori in Turkish Children

Ahmet Bolat
1   Department of Pediatrics, University of Health Sciences, Gülhane Training and Research Hospital, Ankara, Turkey
,
Deniz Yaprak
1   Department of Pediatrics, University of Health Sciences, Gülhane Training and Research Hospital, Ankara, Turkey
,
Melike Arslan
2   Division of Pediatric Gastroenterology, Department of Pediatrics, University of Health Sciences, Gülhane Training and Research Hospital, Ankara, Turkey
,
Ayşe Büyükcam
1   Department of Pediatrics, University of Health Sciences, Gülhane Training and Research Hospital, Ankara, Turkey
,
Necati Balamtekin
2   Division of Pediatric Gastroenterology, Department of Pediatrics, University of Health Sciences, Gülhane Training and Research Hospital, Ankara, Turkey
› Author Affiliations
› Further Information
Also available at
    Permissions and Reprints

Abstract

Objective There are many adverse effects of drugs used to eradicate Helicobacter pylori, and reconstructing the microbiota by external ingestion of probiotics seems to have good effects on H. pylori eradication and prevents side effects.

Methods The study included 161 outpatients aged between 8 and 18 years diagnosed with H. pylori gastritis in the Gülhane Training and Research Hospital Pediatric Gastroenterology unit from June 1, 2018, through March 31, 2020, and patients were randomized into two groups. Eighty patients in the probiotic group (first group) received H. pylori eradication therapy for 14 days; additionally, Bifidobacterium lactis B94 was administered for 14 days for eradication of H. pylori. Eighty-one patients in the standard therapy group (second group) received the same eradication therapy but no probiotics. All patients were asked to complete a detailed questionnaire regularly, including changes in symptoms and side effects of drugs on days 0, 7, and 14 of treatment. The eradication success was checked with the H. pylori stool antigen test kit 8 weeks after completion of the treatment regimen.

Results The mean age of the patients was 14.2 ± 2.9 years, and 88 (64.7%) were female. The eradication rates were similar between the standard therapy and the probiotic groups by intention-to-treat analysis (p = 0.930). In order of frequency, the most common eradication treatment–related side effects were abdominal pain, taste abnormalities, and anorexia. In addition, therapy-related epigastric pain and flatulence were similar initially (p > 0.05) but seemed to be significantly lower in the probiotic group than in the standard therapy group on days 7 and 14 (p < 0.05).

Conclusions Our results suggest that additional probiotic supplementation has not changed the eradication rates but seems to reduce some specific gastrointestinal adverse events in children with H. pylori infections treated with a bismuth-based quadruple eradication regimen. More extensive randomized controlled trials are needed to explain probiotics' effects on H. pylori eradication and drug side effects.

Keywords

H. pylori - quadruple therapy - probiotic


Publication History

Received: 04 April 2022

Accepted: 17 September 2022

Article published online:
07 November 2022

© 2022. Thieme. All rights reserved.

Georg Thieme Verlag KG
Rüdigerstraße 14, 70469 Stuttgart, Germany

 

  • References

  • 1 Coelho LGV, Marinho JR, Genta R. et al. IVth Brazilian Consensus Conference on Helicobacter Pylori Infection. Arq Gastroenterol 2018; 55 (02) 97-121
    CrossrefPubMedSearch in Google Scholar
  • 2 Ozen A, Ertem D, Pehlivanoglu E. Natural history and symptomatology of Helicobacter pylori in childhood and factors determining the epidemiology of infection. J Pediatr Gastroenterol Nutr 2006; 42 (04) 398-404
    CrossrefPubMedSearch in Google Scholar
  • 3 Ozaydin N, Turkyilmaz SA, Cali S. Prevalence and risk factors of Helicobacter pylori in Turkey: a nationally-representative, cross-sectional, screening with the 13C-urea breath test. BMC Public Health 2013; 13: 1215
    CrossrefPubMedSearch in Google Scholar
  • 4 Blaser MJ, Chyou PH, Nomura A. Age at establishment of Helicobacter pylori infection and gastric carcinoma, gastric ulcer, and duodenal ulcer risk. Cancer Res 1995; 55 (03) 562-565
    PubMedSearch in Google Scholar
  • 5 Jones NL, Koletzko S, Goodman K. et al; ESPGHAN, NASPGHAN. Joint ESPGHAN/NASPGHAN guidelines for the management of Helicobacter pylori in children and adolescents (update 2016). J Pediatr Gastroenterol Nutr 2017; 64 (06) 991-1003
    CrossrefPubMedSearch in Google Scholar
  • 6 Güven B, Gülerman F, Kaçmaz B. Helicobacter pylori resistance to clarithromycin and fluoroquinolones in a pediatric population in Turkey: a cross-sectional study. Helicobacter 2019; 24 (03) e12581
    CrossrefPubMedSearch in Google Scholar
  • 7 Kutluk G, Tutar E, Bayrak A. et al. Sequential therapy versus standard triple therapy for Helicobacter pylori eradication in children: any advantage in clarithromycin-resistant strains?. Eur J Gastroenterol Hepatol 2014; 26 (11) 1202-1208
    CrossrefPubMedSearch in Google Scholar
  • 8 Nocerino R, Di Costanzo M, Bedogni G. et al. Dietary treatment with extensively hydrolyzed casein formula containing the probiotic Lactobacillus rhamnosus GG prevents the occurrence of functional gastrointestinal disorders in children with cow's milk allergy. J Pediatr 2019; 213: 137-142.e2
    CrossrefPubMedSearch in Google Scholar
  • 9 Saxelin M, Tynkkynen S, Mattila-Sandholm T, de Vos WM. Probiotic and other functional microbes: from markets to mechanisms. Curr Opin Biotechnol 2005; 16 (02) 204-211
    CrossrefPubMedSearch in Google Scholar
  • 10 Hold GL, Hansen R. Impact of the gastrointestinal microbiome in health and disease: co-evolution with the host immune system. Curr Top Microbiol Immunol 2019; 421: 303-318
    PubMedSearch in Google Scholar
  • 11 Moayyedi P. Review: eradication therapy supplemented by probiotics increased eradication rates and reduced side effects in H pylori infection. Evid Based Med 2007; 12 (03) 84
    CrossrefPubMedSearch in Google Scholar
  • 12 Tong JL, Ran ZH, Shen J, Zhang CX, Xiao SD. Meta-analysis: the effect of supplementation with probiotics on eradication rates and adverse events during Helicobacter pylori eradication therapy. Aliment Pharmacol Ther 2007; 25 (02) 155-168
    CrossrefPubMedSearch in Google Scholar
  • 13 Srinarong C, Siramolpiwat S, Wongcha-um A, Mahachai V, Vilaichone RK. Improved eradication rate of standard triple therapy by adding bismuth and probiotic supplement for Helicobacter pylori treatment in Thailand. Asian Pac J Cancer Prev 2014; 15 (22) 9909-9913
    CrossrefPubMedSearch in Google Scholar
  • 14 Dixon MF, Genta RM, Yardley JH, Correa P. Histological classification of gastritis and Helicobacter pylori infection: an agreement at last? The International Workshop on the Histopathology of Gastritis. Helicobacter 1997; 2 (Suppl. 01) S17-S24
    CrossrefPubMedSearch in Google Scholar
  • 15 Shafaghi A, Pourkazemi A, Khosravani M. et al. The effect of probiotic plus prebiotic supplementation on the tolerance and efficacy of Helicobacter Pylori eradication quadruple therapy: a randomized prospective double blind controlled trial. Middle East J Dig Dis 2016; 8 (03) 179-188
    CrossrefPubMedSearch in Google Scholar
  • 16 Francavilla R, Lionetti E, Castellaneta SP. et al. Improved efficacy of 10-day sequential treatment for Helicobacter pylori eradication in children: a randomized trial. Gastroenterology 2005; 129 (05) 1414-1419
    CrossrefPubMedSearch in Google Scholar
  • 17 Zhang L, Su P, Henriksson A, O'Rourke J, Mitchell H. Investigation of the immunomodulatory effects of Lactobacillus casei and Bifidobacterium lactis on Helicobacter pylori infection. Helicobacter 2008; 13 (03) 183-190
    CrossrefPubMedSearch in Google Scholar
  • 18 Jones SE, Versalovic J. Probiotic Lactobacillus reuteri biofilms produce antimicrobial and anti-inflammatory factors. BMC Microbiol 2009; 9: 35
    CrossrefPubMedSearch in Google Scholar
  • 19 Gotteland M, Brunser O, Cruchet S. Systematic review: are probiotics useful in controlling gastric colonization by Helicobacter pylori?. Aliment Pharmacol Ther 2006; 23 (08) 1077-1086
    CrossrefPubMedSearch in Google Scholar
  • 20 Homan M, Orel R. Are probiotics useful in Helicobacter pylori eradication?. World J Gastroenterol 2015; 21 (37) 10644-10653
    CrossrefPubMedSearch in Google Scholar
  • 21 Pacifico L, Osborn JF, Bonci E, Romaggioli S, Baldini R, Chiesa C. Probiotics for the treatment of Helicobacter pylori infection in children. World J Gastroenterol 2014; 20 (03) 673-683
    CrossrefPubMedSearch in Google Scholar
  • 22 Dinleyici EC, Kara A, Ozen M, Vandenplas Y. Saccharomyces boulardii CNCM I-745 in different clinical conditions. Expert Opin Biol Ther 2014; 14 (11) 1593-1609
    CrossrefPubMedSearch in Google Scholar
  • 23 Wang YH, Huang Y. Effect of Lactobacillus acidophilus and Bifidobacterium bifidum supplementation to standard triple therapy on Helicobacter pylori eradication and dynamic changes in intestinal flora. World J Microbiol Biotechnol 2014; 30 (03) 847-853
    CrossrefPubMedSearch in Google Scholar
  • 24 Ahmad K, Fatemeh F, Mehri N, Maryam S. Probiotics for the treatment of pediatric helicobacter pylori infection: a randomized double blind clinical trial. Iran J Pediatr 2013; 23 (01) 79-84
    PubMedSearch in Google Scholar
  • 25 Feng JR, Wang F, Qiu X. et al. Efficacy and safety of probiotic-supplemented triple therapy for eradication of Helicobacter pylori in children: a systematic review and network meta-analysis. Eur J Clin Pharmacol 2017; 73 (10) 1199-1208
    CrossrefPubMedSearch in Google Scholar
  • 26 Daelemans S, Deseck V, Levy EI, Vandenplas Y. Are pro- and/or synbiotics beneficial in Helicobacter pylori eradication therapy in children? A narrative review. Eur J Pediatr 2022; 181 (09) 3225-3234
    CrossrefPubMedSearch in Google Scholar
  • 27 Ustundag GH, Altuntas H, Soysal YD, Kokturk F. The effects of synbiotic “Bifidobacterium lactis B94 plus inulin” addition on standard triple therapy of Helicobacter pylori eradication in children. Can J Gastroenterol Hepatol 2017; 2017: 8130596
    CrossrefPubMedSearch in Google Scholar
  • 28 Islek A, Sayar E, Yilmaz A, Artan R. Bifidobacterium lactis B94 plus inulin for treatment of Helicobacter pylori infection in children: does it increase eradication rate and patient compliance?. Acta Gastroenterol Belg 2015; 78 (03) 282-286
    PubMedSearch in Google Scholar
  • 29 Goldman CG, Barrado DA, Balcarce N. et al. Effect of a probiotic food as an adjuvant to triple therapy for eradication of Helicobacter pylori infection in children. Nutrition 2006; 22 (10) 984-988
    CrossrefPubMedSearch in Google Scholar
  • 30 Akcam M, Koca T, Salman H, Karahan N. The effects of probiotics on treatment of Helicobacter pylori eradication in children. Saudi Med J 2015; 36 (03) 286-290
    CrossrefPubMedSearch in Google Scholar
  • 31 Tolone S, Pellino V, Vitaliti G, Lanzafame A, Tolone C. Evaluation of Helicobacter pylori eradication in pediatric patients by triple therapy plus lactoferrin and probiotics compared to triple therapy alone. Ital J Pediatr 2012; 38: 63
    CrossrefPubMedSearch in Google Scholar
  • 32 Mamori S, Higashida A, Kawara F. et al. Age-dependent eradication of Helicobacter pylori in Japanese patients. World J Gastroenterol 2010; 16 (33) 4176-4179
    CrossrefPubMedSearch in Google Scholar
  • 33 Cárdenas PA, Garcés D, Prado-Vivar B. et al. Effect of Saccharomyces boulardii CNCM I-745 as complementary treatment of Helicobacter pylori infection on gut microbiome. Eur J Clin Microbiol Infect Dis 2020; 39 (07) 1365-1372
    CrossrefPubMedSearch in Google Scholar
  • 34 Lü M, Yu S, Deng J. et al. Efficacy of probiotic supplementation therapy for Helicobacter pylori eradication: a meta-analysis of randomized controlled trials. PLoS One 2016; 11 (10) e0163743
    CrossrefPubMedSearch in Google Scholar
  • 35 Lau CS, Ward A, Chamberlain RS. Probiotics improve the efficacy of standard triple therapy in the eradication of Helicobacter pylori: a meta-analysis. Infect Drug Resist 2016; 9: 275-289
    CrossrefPubMedSearch in Google Scholar
  • 36 Pacifico L, Osborn JF, Anania C, Vaira D, Olivero E, Chiesa C. Review article: bismuth-based therapy for Helicobacter pylori eradication in children. Aliment Pharmacol Ther 2012; 35 (09) 1010-1026
    PubMedSearch in Google Scholar