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J Pediatr Infect Dis 2022; 17(02): 059-070
DOI: 10.1055/s-0042-1743502
Review Article

The Association between Helicobacter Pylori Infection and Iron Deficiency Anemia in Children: A Systematic Review and Meta-Analysis

Sara Z. Hamdan
1   Department of Community Medicine, Faculty of Medicine, Al-Neelain University, Khartoum, Sudan
,
Hamdan Zaki Hamdan 
2   Department of Basic Medical Sciences, Unaizah College of Medicine and Medical Sciences, Qassim University, Unaizah, Kingdom of Saudi Arabia
3   Department of Biochemistry and Molecular Biology, Faculty of Medicine, Al-Neelain University, Khartoum, Sudan
,
Mustafa Nimieri
1   Department of Community Medicine, Faculty of Medicine, Al-Neelain University, Khartoum, Sudan
,
Ishag Adam
4   Department of Obstetrics and Gynecology, Unaizah College of Medicine, Qassim University, Unaizah, Saudi Arabia
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Abstract

Objectives This study, comprising a systematic review and meta-analysis, was conducted to assess the association between Helicobacter pylori infection and the risk of iron deficiency anemia (IDA) in children.

Methods We followed Preferred Reporting Items for Systematic Reviews and Meta-Analyses guidelines. Relevant published studies were searched in the databases. Retrieved studies were assessed for quality using the Modified Newcastle-Ottawa Scale for quality assessment. The “meta” package of statistical software “R 4.0.3 was used for statistical analysis.

Results Overall, 22 eligible studies (eight cross-sectional, six randomized control trials, five case-control, two surveys, and one cohort), including nine (40.9%) from Asia, four (18.1%) from America, four (18.1%) from Africa, four (18.1%) from Europe, and one (4.5%) from Australia with a total of 3,434 cases and 4,455 controls were included in this systematic review and meta-analysis. We found that H. pylori infection was associated with a high risk of IDA (odds ratio 1.70, 95% confidence interval 1.21 − 2.38) in a random-effects model. Meta-regression analysis showed that none of the investigated factors that may affect the prevalence of IDA reached statistical significance. There was statistically significant difference between results when studies were categorized according to the methods used to diagnose H. pylori and level of incomes based on World Bank classification. The GRADEpro Guideline Development Tool evidence for the risk of IDA was of a “moderate certainty.”

Conclusions This meta-analysis with a “moderate certainty” of evidence showed an association between H. pylori infection and a high risk of developing IDA in children.

Keywords

breath test - children - H. pylori - iron deficiency anemia - meta-analysis

Supplementary Material



Publication History

Received: 13 August 2021

Accepted: 25 January 2022

Article published online:
08 March 2022

© 2022. Thieme. All rights reserved.

Georg Thieme Verlag KG
Rüdigerstraße 14, 70469 Stuttgart, Germany

 

  • References

  • 1 Stoltzfus RJ. Iron deficiency: global prevalence and consequences. Food Nutr Bull 2003; 24 (04, Suppl): S99-S103
    CrossrefPubMedGoogle Scholar
  • 2 WHO. Haemoglobin concentrations for the diagnosis of anaemia and assessment of severity. 2011 . Accessed October 26, 2020 at: www.who.int/vmnis/indicators/haemoglobin.pdf
    PubMedGoogle Scholar
  • 3 WHO. World Malaria Report 2018. 2018 . Accessed October 27, 2020 at: www.who.int/malaria
    PubMedGoogle Scholar
  • 4 WHO. The Global Prevalence of Anaemia in 2011 the Global Prevalence of Anaemia in 2011 II WHO Library Cataloguing-in-Publication Data. 2015 . Accessed October 26, 2020 at: www.who.int
    PubMedGoogle Scholar
  • 5 Eltayeb MSE, Elsaeed AE, Mohamedani AA, Assayed AA. Prevalence of anaemia among Quranic school (Khalawi) students (Heiran) in Wad El Magboul village, rural Rufaa, Gezira State, Central Sudan: a cross sectional study. Pan Afr Med J 2016; 24: 244
    PubMedGoogle Scholar
  • 6 Qu XH, Huang XL, Xiong P. et al. Does Helicobacter pylori infection play a role in iron deficiency anemia? A meta-analysis. World J Gastroenterol 2010; 16 (07) 886-896
    PubMedGoogle Scholar
  • 7 Muhsen K, Barak M, Shifnaidel L, Nir A, Bassal R, Cohen D. Helicobacter pylori infection is associated with low serum ferritin levels in Israeli Arab children: a seroepidemiologic study. J Pediatr Gastroenterol Nutr 2009; 49 (02) 262-264
    CrossrefPubMedGoogle Scholar
  • 8 Magalhães Queiroz DM, Luzza F. Epidemiology of Helicobacter pylori infection. Helicobacter 2006; 11 (Suppl 1): 1-5
    CrossrefPubMedGoogle Scholar
  • 9 Suerbaum S, Michetti P. Helicobacter pylori infection. N Engl J Med 2002; 347 (15) 1175-1186
    CrossrefPubMedGoogle Scholar
  • 10 Pacifico L, Osborn JF, Tromba V, Romaggioli S, Bascetta S, Chiesa C. Helicobacter pylori infection and extragastric disorders in children: a critical update. World J Gastroenterol 2014; 20 (06) 1379-1401
    CrossrefPubMedGoogle Scholar
  • 11 Cardenas VM, Mulla ZD, Ortiz M, Graham DY. Iron deficiency and Helicobacter pylori infection in the United States. Am J Epidemiol 2006; 163 (02) 127-134
    CrossrefPubMedGoogle Scholar
  • 12 Darvishi M, Ziari K, Mohebi H, Alizadeh K. Association between iron deficiency anemia and Helicobacter pylori infection among children under six years in Iran. 2015 53. . Accessed October 26, 2020 at: https://acta.tums.ac.ir/index.php/acta/article/view/4903
    PubMedGoogle Scholar
  • 13 Xia W, Zhang X, Wang J, Sun C, Wu L. Survey of anaemia and Helicobacter pylori infection in adolescent girls in Suihua, China and enhancement of iron intervention effects by H. pylori eradication. Br J Nutr 2012; 108 (02) 357-362
    CrossrefPubMedGoogle Scholar
  • 14 Queiroz DMM, Harris PR, Sanderson IR. et al. Iron status and Helicobacter pylori infection in symptomatic children: an international multi-centered study. PLoS One 2013; 8 (07) e68833
    CrossrefPubMedGoogle Scholar
  • 15 Baggett HC, Parkinson AJ, Muth PT, Gold BD, Gessner BD. Endemic iron deficiency associated with Helicobacter pylori infection among school-aged children in Alaska. Pediatrics 2006; 117 (03) e396 –e404
    CrossrefPubMedGoogle Scholar
  • 16 Afifi RAR, Ali DK, Shaheen IAM. A localized case-control study of extra-gastric manifestations of Helicobacter pylori infection in children. Indian J Pediatr 2011; 78 (04) 418-422
    CrossrefPubMedGoogle Scholar
  • 17 Vendt N, Kool P, Teesalu K, Lillemäe K, Maaroos HI, Oona M. Iron deficiency and Helicobacter pylori infection in children. Acta Paediatr 2011; 100 (09) 1239-1243
    CrossrefPubMedGoogle Scholar
  • 18 Zahmatkeshan M, Karimi M, Geramizadeh B, Eslaminasab S, Esmailnejad A, Safarpour AR. Association between Helicobacter pylori infection and iron deficiency anemia in school-aged Iranian children. Ind Pediatr 2019; 56: 387-389
    CrossrefPubMedGoogle Scholar
  • 19 Sandström G, Rödjer S, Kaijser B, Börjesson M. Helicobacter pylori antibodies and iron deficiency in female adolescents. PLoS One 2014; 9 (11) e113059
    CrossrefPubMedGoogle Scholar
  • 20 Bazmamoun H, Razavi Z, Esfahani H. Arefian. Evaluation of iron deficiency anemia and BMI in children suffering from Helicobacter pylori infection. Iran J Ped Hematol Oncol 2014; 4 (04) 167-171
    PubMedGoogle Scholar
  • 21 Süoglu ÖD, Gökçe S, Saglam AT, Sökücü S, Saner G. Association of Helicobacter pylori infection with gastroduodenal disease, epidemiologic factors and iron-deficiency anemia in Turkish children undergoing endoscopy, and impact on growth. Pediatr Int 2007; 49 (06) 858-863
    CrossrefPubMedGoogle Scholar
  • 22 Salameh JP, Bossuyt PM, McGrath TA. et al. Preferred reporting items for systematic review and meta-analysis of diagnostic test accuracy studies (PRISMA-DTA): explanation, elaboration, and checklist. BMJ 2020; 370 (12) m2632
    CrossrefPubMedGoogle Scholar
  • 23 Munn Z, Tufanaru C, Aromataris E. JBI's systematic reviews: data extraction and synthesis. Am J Nurs 2014; 114 (07) 49-54
    CrossrefPubMedGoogle Scholar
  • 24 Balduzzi S, Rücker G, Schwarzer G. How to perform a meta-analysis with R: a practical tutorial. Evid Based Ment Health 2019; 22 (04) 153-160
    CrossrefPubMedGoogle Scholar
  • 25 Sedgwick P. Meta-analyses: heterogeneity and subgroup analysis. BMJ 2013;346(7914)
    PubMedGoogle Scholar
  • 26 GRADE handbook. Accessed December 13, 2021 at: https://gdt.gradepro.org/app/handbook/handbook.html
    PubMedGoogle Scholar
  • 27 Cherian S, Forbes DA, Cook AG. et al. An insight into the relationships between hepcidin, anemia, infections and inflammatory cytokines in pediatric refugees: a cross-sectional study. PLoS One 2008; 3 (12) e4030
    CrossrefPubMedGoogle Scholar
  • 28 Choi JW. Serum-soluble transferrin receptor concentrations in Helicobacter pylori-associated iron-deficiency anemia. Ann Hematol 2006; 85 (10) 735-737
    CrossrefPubMedGoogle Scholar
  • 29 Kady HME, Kahiry WA, Abdelsalam HST. Burden of Helicobacter pylori infections and associated risk factors among cases of iron deficiency anaemia in Egypt. Microbiol Res J Int 2020; 30 (07) 80-91
    CrossrefPubMedGoogle Scholar
  • 30 Sandström G, Rödjer S, Kaijser B, Börjesson M. Helicobacter pylori antibodies and iron deficiency in female adolescents. PLoS One 2014; 9 (11) e113059
    CrossrefPubMedGoogle Scholar
  • 31 El-Aziz Awad Mel-D, Amin SM, Abdou SM. Assessment of diagnostic and therapeutic approaches of Helicobacter pylori-associated iron deficiency and anemia in children with dyspeptic symptoms. J Egypt Soc Parasitol 2014; 44 (03) 695-708
    PubMedGoogle Scholar
  • 32 Thankachan P, Muthayya S, Sierksma A. et al. Helicobacter pylori infection does not influence the efficacy of iron and vitamin B(12) fortification in marginally nourished Indian children. Eur J Clin Nutr 2010; 64 (10) 1101-1107
    CrossrefPubMedGoogle Scholar
  • 33 Sarker SA, Mahmud H, Davidsson L. et al. Causal relationship of Helicobacter pylori with iron-deficiency anemia or failure of iron supplementation in children. Gastroenterology 2008; 135 (05) 1534-1542
    CrossrefPubMedGoogle Scholar
  • 34 Duque X, Moran S, Mera R. et al. Effect of eradication of Helicobacter pylori and iron supplementation on the iron status of children with iron deficiency. Arch Med Res 2010; 41 (01) 38-45
    CrossrefPubMedGoogle Scholar
  • 35 Buerkli S, Ndiaye NF, Cercamondi CI, Herter-Aeberli I, Moretti D, Zimmermann MB. Asymptomatic Helicobacter pylori infection in preschool children and young women does not predict iron bioavailability from iron-fortified foods. Nutrients 2019; 11 (09) E2093
    CrossrefPubMedGoogle Scholar
  • 36 Choe YH, Kim SK, Son BK, Lee DH, Hong YC, Pai SH. Randomized placebo-controlled trial of Helicobacter pylori eradication for iron-deficiency anemia in preadolescent children and adolescents. Helicobacter 1999; 4 (02) 135-139
    CrossrefPubMedGoogle Scholar
  • 37 Haghi-Ashtiani MT, Monajemzadeh M, Motamed F. et al. Anemia in children with and without Helicobacter pylori infection. Arch Med Res 2008; 39 (05) 536-540
    CrossrefPubMedGoogle Scholar
  • 38 Pacey A, Weiler H, Egeland GM. Low prevalence of iron-deficiency anaemia among Inuit preschool children: Nunavut Inuit Child Health Survey, 2007-2008. Public Health Nutr 2011; 14 (08) 1415-1423
    CrossrefPubMedGoogle Scholar
  • 39 Hudak L, Jaraisy A, Haj S, Muhsen K. An updated systematic review and meta-analysis on the association between Helicobacter pylori infection and iron deficiency anemia. Helicobacter 2017;22(01)
    PubMedGoogle Scholar
  • 40 Muhsen K, Cohen D. Helicobacter pylori infection and iron stores: a systematic review and meta-analysis. Helicobacter 2008; 13 (05) 323-340
    CrossrefPubMedGoogle Scholar
  • 41 Park JH, Kim SY, Kim DW, Lee WG, Rhee KH, Youn HS. Correlation between Helicobacter pylori infection and vitamin C levels in whole blood, plasma, and gastric juice, and the pH of gastric juice in Korean children. J Pediatr Gastroenterol Nutr 2003; 37 (01) 53-62
    CrossrefPubMedGoogle Scholar
  • 42 Yokota S, Toita N, Yamamoto S, Fujii N, Konno M. Positive relationship between a polymorphism in Helicobacter pylori neutrophil-activating protein a gene and iron-deficiency anemia. Helicobacter 2013; 18 (02) 112-116
    CrossrefPubMedGoogle Scholar
  • 43 Soares Magalhães RJ, Langa A, Pedro JM, Sousa-Figueiredo JC, Clements ACA, Nery SV. Role of malnutrition and parasite infections in the spatial variation in children's anaemia risk in northern Angola. Geospat Health 2013; 7 (02) 341-354
    CrossrefPubMedGoogle Scholar
  • 44 McClure EM, Meshnick SR, Mungai P. et al. The association of parasitic infections in pregnancy and maternal and fetal anemia: a cohort study in coastal Kenya. PLoS Negl Trop Dis 2014; 8 (02) e2724
    CrossrefPubMedGoogle Scholar
  • 45 Sousa-Figueiredo JC, Gamboa D, Pedro JM. et al. Epidemiology of malaria, schistosomiasis, geohelminths, anemia and malnutrition in the context of a demographic surveillance system in northern Angola. PLoS One 2012; 7 (04) e33189
    CrossrefPubMedGoogle Scholar
  • 46 Cutler AF. Diagnostic tests for H. pylori: a prospective evaluation of their accuracy, without selecting a single test as the gold standard. Am J Gastroenterol 1997; 92 (03) 538-539
    PubMedGoogle Scholar