• 1.

    Muhsen K, Cohen D, 2013. Helicobacter pylori infection and anemia. Am J Trop Med Hyg 89: 398.

  • 2.

    Righetti AA, Koua AYG, Adiossan LG, Glinz D, Hurrell RF, N'Goran EK, Niamké S, Wegmüller R, Utzinger J, 2012. Etiology of anemia among infants, school-aged children, and young non-pregnant women in different settings of south-central Côte d'Ivoire. Am J Trop Med Hyg 87: 425434.

    • Search Google Scholar
    • Export Citation
  • 3.

    Crawley J, 2004. Reducing the burden of anemia in infants and young children in malaria-endemic countries of Africa: from evidence to action. Am J Trop Med Hyg 71 (Suppl): 2534.

    • Search Google Scholar
    • Export Citation
  • 4.

    Tolentino K, Friedman JF, 2007. An update on anemia in less developed countries. Am J Trop Med Hyg 77: 4451.

  • 5.

    Staubli-Asobayire F, Adou P, Davidsson L, Cook JD, Hurrell RF, 2001. Prevalence of iron deficiency with and without concurrent anemia in population groups with high prevalences of malaria and other infections: a study in Côte d'Ivoire. Am J Clin Nutr 74: 776782.

    • Search Google Scholar
    • Export Citation
  • 6.

    Rohner F, Zimmermann MB, Amon RJ, Vounatsou P, Tschannen AB, N'Goran EK, Nindjin C, Cacou MC, Té-Bonlé MD, Aka H, Sess DE, Utzinger J, Hurrell RF, 2010. In a randomized controlled trial of iron fortification, anthelmintic treatment, and intermittent preventive treatment of malaria for anemia control in Ivorian children, only anthelmintic treatment shows modest benefit. J Nutr 140: 635641.

    • Search Google Scholar
    • Export Citation
  • 7.

    Righetti AA, Adiossan LG, Ouattara M, Glinz D, Hurrell RF, N'Goran EK, Wegmüller R, Utzinger J, 2013. Dynamics of anemia in relation to parasitic infections, micronutrient status, and increasing age in south-central Côte d'Ivoire. J Infect Dis 207: 16041615.

    • Search Google Scholar
    • Export Citation
  • 8.

    Righetti AA, Wegmüller R, Glinz D, Ouattara M, Adiossan LG, N'Goran EK, Utzinger J, Hurrell RF, 2013. Effects of inflammation and Plasmodium falciparum infection on soluble transferrin receptor and plasma ferritin concentration in different age groups: a prospective longitudinal study in Côte d'Ivoire. Am J Clin Nutr 97: 13641374.

    • Search Google Scholar
    • Export Citation
  • 9.

    Muhsen K, Cohen D, 2008. Helicobacter pylori infection and iron stores: a systematic review and meta-analysis. Helicobacter 13: 323340.

  • 10.

    Annibale B, Marignani M, Monarca B, Antonelli G, Marcheggiano A, Martino G, Mandelli F, Caprilli R, Delle Fave G, 1999. Reversal of iron deficiency anemia after Helicobacter pylori eradication in patients with asymptomatic gastritis. Ann Intern Med 131: 668672.

    • Search Google Scholar
    • Export Citation
  • 11.

    Choe YH, Kwon YS, Jung MK, Kang SK, Hwang TS, Hong YC, 2001. Helicobacter pylori-associated iron-deficiency anemia in adolescent female athletes. J Pediatr 139: 100104.

    • Search Google Scholar
    • Export Citation
  • 12.

    Fagan RP, Dunaway CE, Bruden DL, Parkinson AJ, Gessner BD, 2009. Controlled, household-randomized, open-label trial of the effect of treatment of Helicobacter pylori infection on iron deficiency among children in rural Alaska: results at 40 months. J Infect Dis 199: 652660.

    • Search Google Scholar
    • Export Citation
  • 13.

    Malik R, Guleria K, Kaur I, Sikka M, Radhakrishnan G, 2011. Effect of Helicobacter pylori eradication therapy in iron deficiency anaemia of pregnancy—a pilot study. Indian J Med Res 134: 224231.

    • Search Google Scholar
    • Export Citation
  • 14.

    Banic M, Franceschi F, Babic Z, Gasbarrini A, 2012. Extragastric manifestations of Helicobacter pylori infection. Helicobacter 17 (Suppl 1): 4955.

    • Search Google Scholar
    • Export Citation
  • 15.

    Amedei A, Cappon A, Codolo G, Cabrelle A, Polenghi A, Benagiano M, Tasca E, Azzurri A, D'Elios MM, Del Prete G, de Bernard M, 2006. The neutrophil-activating protein of Helicobacter pylori promotes Th1 immune responses. J Clin Invest 116: 10921101.

    • Search Google Scholar
    • Export Citation
  • 16.

    Diomande MI, Flejou JF, Potet F, Dago-Akribi A, Ouattara D, Kadjo K, Niamkey E, Beaumel A, Gbe K, Beda BY, 1991. Chronic gastritis and Helicobacter pylori infection on the Ivory Coast. A series of 277 symptomatic patients. Gastroenterol Clin Biol 15: 711716 (in French).

    • Search Google Scholar
    • Export Citation
  • 17.

    Koffi KS, Attia KA, Adonis-Koffy LY, Faye-Kette H, Coulibaly KJ, Dosso M, 2010. Is the mother a risk factor for transmission of Helicobacter pylori infection in children between the ages of 6 months and 5 years in Côte d'Ivoire? Med Trop 70: 359363.

    • Search Google Scholar
    • Export Citation
  • 18.

    Siekmann JH, Allen LH, Watnik MR, Nestel P, Neumann CG, Shoenfeld Y, Peter JB, Patnik M, Ansari AA, Coppel RL, Gershwin ME, 2003. Titers of antibody to common pathogens: relation to food-based interventions in rural Kenyan schoolchildren. Am J Clin Nutr 77: 242249.

    • Search Google Scholar
    • Export Citation
  • 19.

    Farag TH, Stoltzfus RJ, Khalfan SS, Tielsch JM, 2007. Helicobacter pylori infection is associated with severe anemia of pregnancy on Pemba Island, Zanzibar. Am J Trop Med Hyg 76: 541548.

    • Search Google Scholar
    • Export Citation
  • 20.

    Vaira D, Malfertheiner P, Mégraud F, Axon AT, Deltenre M, Hirschl AM, Gasbarrini G, O'Morain C, Garcia JM, Quina M, Tytgat GN, 1999. Diagnosis of Helicobacter pylori infection with a new non-invasive antigen-based assay. HpSA European study group. Lancet 354: 3033.

    • Search Google Scholar
    • Export Citation
  • 21.

    de Carvalho Costa Cardinali L, Rocha GA, Rocha AMC, de Moura SB, de Figueiredo Soares T, Esteves AMB, Nogueira AMMF, Cabral MMDA, de Carvalho AST, Bitencourt P, Ferreira A, Queiroz DMM, 2003. Evaluation of [13C] urea breath test and Helicobacter pylori stool antigen test for diagnosis of H. pylori infection in children from a developing country. J Clin Microbiol 41: 33343335.

    • Search Google Scholar
    • Export Citation

 

 

 

 

In Response

View More View Less
  • 1 Department of Epidemiology and Public Health
  • 2 Swiss Tropical and Public Health Institute
  • 3 and University of Basel
  • 4 Basel, Switzerland
  • 5 E-mails: aurelierighetti@gmail.com, juerg.utzinger@unibas.ch
  • 6 Laboratoire de Biotechnologies
  • 7 Unité de Formation et de Recherche Biosciences
  • 8 Université Félix Houphouët-Boigny
  • 9 Abidjan, Côte d'Ivoire
  • 10 E-mail: kouayahgisele@yahoo.fr, niamkes@yahoo.fr
  • 11 Hôpital Général de Taabo
  • 12 Taabo Cité, Côte d'Ivoire
  • 13 E-mail: adiossanlukas@yahoo.fr
  • 14 Laboratory of Human Nutrition
  • 15 Institute of Food, Nutrition, and Health
  • 16 ETH Zurich
  • 17 Zurich, Switzerland
  • 18 E-mails: dominik.glinz@hest.ethz.ch, richard.hurrell@hest.ethz.ch, rita.wegmueller@hest.ethz.ch
  • 19 Laboratoire de Zoologie Biologie Animale
  • 20 Unité de Formation et de Recherche Biosciences
  • 21 Université Félix Houphouët-Boigny
  • 22 and Centre Suisse de Recherches Scientifiques en Côte d'Ivoire
  • 23 Abidjan, Côte d'Ivoire
  • 24 E-mail: eliezerngoran@yahoo.fr

Dear Sir:

We thank Muhsen and Cohen1 for their informative letter to the editor in connection with our findings reported in the September 2012 issue of the American Journal of Tropical Medicine and Hygiene.2 In response, three points are offered for discussion.

First, the aim of our work was to deepen the understanding of the etiology of anemia in a typical rural setting of West Africa. Taking into consideration general reviews3,4 and prior research conducted in different parts of Côte d'Ivoire,5,6 emphasis was placed on parasitic infections (i.e., Plasmodium falciparum and helminths), inflammation, and micronutrient deficiencies (i.e., iron, riboflavin, and vitamin A). Available financial, technical, and human resources were constrained, which is often the case while conducting research in the humid tropics. Three cohorts (i.e., infants, school-aged children, and women of childbearing age) were followed prospectively over a 14-month period.7,8 These cohorts were selected, because they are at high risk of parasitic infection and vulnerable to anemia. At the baseline cross-sectional survey, we found that anemia was significantly and positively associated with P. falciparum infection in infants, cellular iron deficiency (ID) in school-aged children and women of childbearing age, and chronic inflammation in school-aged children.2 As the subjects grew older, these associations altered.7

Second, Muhsen and Cohen1 emphasize that Helicobacter pylori, a Gram-negative spiral-shaped bacterium that the World Health Organization classifies as a carcinogen of class I, is associated with increased odds of ID anemia (IDA) and that anti-H. pylori therapy reduces the risk of IDA. The evidence derives from a systematic review and meta-analysis,9 and it is further supported by intervention studies among children and adults in middle- and high-income countries.1013 However, other studies did not find any association between iron stores and H. pylori infection,14 and the causal mechanisms of H. pylori infection and IDA remain to be fully characterized. In addition to an increased requirement for iron needed to support bacterial growth and the gastric mucosal damage that can decrease gastric acid production, H. pylori induces inflammation—polarized to a T-helper 1 response15—and chronic bleeding, both of which might lead to anemia.

Third, while reviewing the literature, we could not identify any studies that investigated H. pylori infection in community surveys in Côte d'Ivoire. However, data derived from two hospital-based studies indicate that H. pylori infection does occur in Côte d'Ivoire among both children and adults, particularly among patients who present with abdominal pain.16,17 Overall, the epidemiology of H. pylori is poorly characterized in sub-Saharan Africa.18,19 Hence, considering the paucity of published data, it is difficult to appreciate whether and to what extent H. pylori infection might have contributed to the high level of anemia among infants, children, and women of childbearing age observed in a rural part of south-central Côte d'Ivoire.

Taken together, the study of H. pylori in sub-Saharan Africa deserves more attention. We, thus, agree with the proposal made by Muhsen and Cohen1 that future epidemiologic studies investigating the etiology of anemia in tropical settings should include appraisal of H. pylori, and therefore, the relationship between this bacterial infection and anemia can be further elucidated. Several direct and indirect techniques are available for the diagnosis of H. pylori. Gastric mucosal biopsy is a costly and invasive diagnostic method, whereas bacteria culture requires specific technical skills and is expensive. Hence, these two techniques are not suitable for large-scale epidemiologic studies in resources-constrained settings. However, a simple stool antigen assay and the [13C] urea breath test hold promise for community-based surveys in low-income countries.20,21 The stool antigen assay is particularly suitable for studies where fecal samples are collected for the diagnosis of helminth and intestinal protozoa infections. Should H. pylori infection emerge as an important contributor to the burden of anemia in sub-Saharan Africa, this information would further support the urgent need of implementing basic public health measures, such as improving access to clean water, sanitation, and hygiene.

  • 1.

    Muhsen K, Cohen D, 2013. Helicobacter pylori infection and anemia. Am J Trop Med Hyg 89: 398.

  • 2.

    Righetti AA, Koua AYG, Adiossan LG, Glinz D, Hurrell RF, N'Goran EK, Niamké S, Wegmüller R, Utzinger J, 2012. Etiology of anemia among infants, school-aged children, and young non-pregnant women in different settings of south-central Côte d'Ivoire. Am J Trop Med Hyg 87: 425434.

    • Search Google Scholar
    • Export Citation
  • 3.

    Crawley J, 2004. Reducing the burden of anemia in infants and young children in malaria-endemic countries of Africa: from evidence to action. Am J Trop Med Hyg 71 (Suppl): 2534.

    • Search Google Scholar
    • Export Citation
  • 4.

    Tolentino K, Friedman JF, 2007. An update on anemia in less developed countries. Am J Trop Med Hyg 77: 4451.

  • 5.

    Staubli-Asobayire F, Adou P, Davidsson L, Cook JD, Hurrell RF, 2001. Prevalence of iron deficiency with and without concurrent anemia in population groups with high prevalences of malaria and other infections: a study in Côte d'Ivoire. Am J Clin Nutr 74: 776782.

    • Search Google Scholar
    • Export Citation
  • 6.

    Rohner F, Zimmermann MB, Amon RJ, Vounatsou P, Tschannen AB, N'Goran EK, Nindjin C, Cacou MC, Té-Bonlé MD, Aka H, Sess DE, Utzinger J, Hurrell RF, 2010. In a randomized controlled trial of iron fortification, anthelmintic treatment, and intermittent preventive treatment of malaria for anemia control in Ivorian children, only anthelmintic treatment shows modest benefit. J Nutr 140: 635641.

    • Search Google Scholar
    • Export Citation
  • 7.

    Righetti AA, Adiossan LG, Ouattara M, Glinz D, Hurrell RF, N'Goran EK, Wegmüller R, Utzinger J, 2013. Dynamics of anemia in relation to parasitic infections, micronutrient status, and increasing age in south-central Côte d'Ivoire. J Infect Dis 207: 16041615.

    • Search Google Scholar
    • Export Citation
  • 8.

    Righetti AA, Wegmüller R, Glinz D, Ouattara M, Adiossan LG, N'Goran EK, Utzinger J, Hurrell RF, 2013. Effects of inflammation and Plasmodium falciparum infection on soluble transferrin receptor and plasma ferritin concentration in different age groups: a prospective longitudinal study in Côte d'Ivoire. Am J Clin Nutr 97: 13641374.

    • Search Google Scholar
    • Export Citation
  • 9.

    Muhsen K, Cohen D, 2008. Helicobacter pylori infection and iron stores: a systematic review and meta-analysis. Helicobacter 13: 323340.

  • 10.

    Annibale B, Marignani M, Monarca B, Antonelli G, Marcheggiano A, Martino G, Mandelli F, Caprilli R, Delle Fave G, 1999. Reversal of iron deficiency anemia after Helicobacter pylori eradication in patients with asymptomatic gastritis. Ann Intern Med 131: 668672.

    • Search Google Scholar
    • Export Citation
  • 11.

    Choe YH, Kwon YS, Jung MK, Kang SK, Hwang TS, Hong YC, 2001. Helicobacter pylori-associated iron-deficiency anemia in adolescent female athletes. J Pediatr 139: 100104.

    • Search Google Scholar
    • Export Citation
  • 12.

    Fagan RP, Dunaway CE, Bruden DL, Parkinson AJ, Gessner BD, 2009. Controlled, household-randomized, open-label trial of the effect of treatment of Helicobacter pylori infection on iron deficiency among children in rural Alaska: results at 40 months. J Infect Dis 199: 652660.

    • Search Google Scholar
    • Export Citation
  • 13.

    Malik R, Guleria K, Kaur I, Sikka M, Radhakrishnan G, 2011. Effect of Helicobacter pylori eradication therapy in iron deficiency anaemia of pregnancy—a pilot study. Indian J Med Res 134: 224231.

    • Search Google Scholar
    • Export Citation
  • 14.

    Banic M, Franceschi F, Babic Z, Gasbarrini A, 2012. Extragastric manifestations of Helicobacter pylori infection. Helicobacter 17 (Suppl 1): 4955.

    • Search Google Scholar
    • Export Citation
  • 15.

    Amedei A, Cappon A, Codolo G, Cabrelle A, Polenghi A, Benagiano M, Tasca E, Azzurri A, D'Elios MM, Del Prete G, de Bernard M, 2006. The neutrophil-activating protein of Helicobacter pylori promotes Th1 immune responses. J Clin Invest 116: 10921101.

    • Search Google Scholar
    • Export Citation
  • 16.

    Diomande MI, Flejou JF, Potet F, Dago-Akribi A, Ouattara D, Kadjo K, Niamkey E, Beaumel A, Gbe K, Beda BY, 1991. Chronic gastritis and Helicobacter pylori infection on the Ivory Coast. A series of 277 symptomatic patients. Gastroenterol Clin Biol 15: 711716 (in French).

    • Search Google Scholar
    • Export Citation
  • 17.

    Koffi KS, Attia KA, Adonis-Koffy LY, Faye-Kette H, Coulibaly KJ, Dosso M, 2010. Is the mother a risk factor for transmission of Helicobacter pylori infection in children between the ages of 6 months and 5 years in Côte d'Ivoire? Med Trop 70: 359363.

    • Search Google Scholar
    • Export Citation
  • 18.

    Siekmann JH, Allen LH, Watnik MR, Nestel P, Neumann CG, Shoenfeld Y, Peter JB, Patnik M, Ansari AA, Coppel RL, Gershwin ME, 2003. Titers of antibody to common pathogens: relation to food-based interventions in rural Kenyan schoolchildren. Am J Clin Nutr 77: 242249.

    • Search Google Scholar
    • Export Citation
  • 19.

    Farag TH, Stoltzfus RJ, Khalfan SS, Tielsch JM, 2007. Helicobacter pylori infection is associated with severe anemia of pregnancy on Pemba Island, Zanzibar. Am J Trop Med Hyg 76: 541548.

    • Search Google Scholar
    • Export Citation
  • 20.

    Vaira D, Malfertheiner P, Mégraud F, Axon AT, Deltenre M, Hirschl AM, Gasbarrini G, O'Morain C, Garcia JM, Quina M, Tytgat GN, 1999. Diagnosis of Helicobacter pylori infection with a new non-invasive antigen-based assay. HpSA European study group. Lancet 354: 3033.

    • Search Google Scholar
    • Export Citation
  • 21.

    de Carvalho Costa Cardinali L, Rocha GA, Rocha AMC, de Moura SB, de Figueiredo Soares T, Esteves AMB, Nogueira AMMF, Cabral MMDA, de Carvalho AST, Bitencourt P, Ferreira A, Queiroz DMM, 2003. Evaluation of [13C] urea breath test and Helicobacter pylori stool antigen test for diagnosis of H. pylori infection in children from a developing country. J Clin Microbiol 41: 33343335.

    • Search Google Scholar
    • Export Citation
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