The effects of iron fortification on the gut microbiota in African children: a randomized controlled trial in Côte d'Ivoire1234

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Background: Iron is essential for the growth and virulence of many pathogenic enterobacteria, whereas beneficial barrier bacteria, such as lactobacilli, do not require iron. Thus, increasing colonic iron could select gut microbiota for humans that are unfavorable to the host.Objective: The objective was to determine the effect of iron fortification on gut microbiota and gut inflammation in African children.Design: In a 6-mo, randomized, double-blind, controlled trial, 6–14-y-old Ivorian children (n = 139) received iron-fortified biscuits, which contained 20 mg Fe/d, 4 times/wk as electrolytic iron or nonfortified biscuits. We measured changes in hemoglobin concentrations, inflammation, iron status, helminths, diarrhea, fecal calprotectin concentrations, and microbiota diversity and composition (n = 60) and the prevalence of selected enteropathogens.Results: At baseline, there were greater numbers of fecal enterobacteria than of lactobacilli and bifidobacteria (P < 0.02). Iron fortification was ineffective; there were no differences in iron status, anemia, or hookworm prevalence at 6 mo. The fecal microbiota was modified by iron fortification as shown by a significant increase in profile dissimilarity (P < 0.0001) in the iron group as compared with the control group. There was a significant increase in the number of enterobacteria (P < 0.005) and a decrease in lactobacilli (P < 0.0001) in the iron group after 6 mo. In the iron group, there was an increase in the mean fecal calprotectin concentration (P < 0.01), which is a marker of gut inflammation, that correlated with the increase in fecal enterobacteria (P < 0.05).Conclusions: Anemic African children carry an unfavorable ratio of fecal enterobacteria to bifidobacteria and lactobacilli, which is increased by iron fortification. Thus, iron fortification in this population produces a potentially more pathogenic gut microbiota profile, and this profile is associated with increased gut inflammation. This trial was registered at controlled-trials.com as ISRCTN21782274.

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1

From the Institute of Food, Nutrition and Health, Swiss Federal Institute of Technology (ETH) Zurich, Zurich, Switzerland (MBZ, CC, FR, AD, CL, and RFH); the Division of Human Nutrition, Wageningen University, Wageningen, Netherlands (MBZ); the Centre Suisse de Recherches Scientifiques, Abidjan, Côte d'Ivoire (EKN and CN); the UFR Biosciences, Université de Cocody-Abidjan, Abidjan, Côte d'Ivoire (ENK); the Department of Public Health and Epidemiology, Swiss Tropical Institute, Basel, Switzerland (JU); and the London School of Hygiene and Tropical Medicine, London, United Kingdom (HG).

2

The sponsors of the study played no role in the design of the trial, analyses of data, or preparation of the manuscript.

3

Supported by the Medicor Foundation (Vaduz, Liechtenstein), the Swiss National Science Foundation (Bern, Switzerland), the Swiss Foundation for Research in Nutrition (Zurich, Switzerland), and the Swiss Federal Institute of Technology (ETH) Zurich (Zurich, Switzerland). Escherichia coli O157H45 was provided by Roger Stephan.

4

Address correspondence to M Zimmermann, Laboratory for Human Nutrition, Swiss Federal Institute of Technology (ETH) Zurich, Schmelzbergstrasse 7, LFV E19, CH-8092 Zurich, Switzerland. E-mail: [email protected].