Abstract

BackgroundApproximately 30% of children worldwide are infected with gastrointestinal parasites. Depending on the species, parasites can disrupt intestinal bacterial microbiota affecting essential vitamin biosynthesis.MethodsStool samples were collected from 37 asymptomatic children from a previous cross-sectional Argentinian study. A multi-parallel real-time quantitative PCR was implemented for Ascaris lumbricoides, Ancylostoma duodenale, Necator americanus, Strongyloides stercoralis, Trichuris trichiura, Cryptosporidium spp., Entamoeba histolytica and Giardia duodenalis. In addition, whole-genome sequencing analysis was conducted for bacterial microbiota on all samples and analyzed using Livermore Metagenomic Analysis Toolkit and DIAMOND software. Separate analyses were carried out for uninfected, Giardia-only, Giardia + helminth co-infections, and helminth-only groups.ResultsFor Giardia-only infected children compared to uninfected children, DNA sequencing data showed a decrease in microbiota biodiversity that correlated with increasing Giardia burden and was statistically significant using Shannonʼs alpha diversity (Giardia-only > 1 fg/µl 2.346; non-infected group 3.253, P = 0.0317). An increase in diversity was observed for helminth-only infections with a decrease in diversity for Giardia + helminth co-infections (P = 0.00178). In Giardia-only infections, microbiome taxonomy changed from Firmicutes towards increasing proportions of Prevotella, with the degree of change related to the intensity of infection compared to uninfected (P = 0.0317). The abundance of Prevotella bacteria was decreased in the helminths-only group but increased for Giardia + helminth co-infections (P = 0.0262). Metagenomic analysis determined cobalamin synthesis was decreased in the Giardia > 1 fg/µl group compared to both the Giardia < 1 fg/µl and the uninfected group (P = 0.0369). Giardia + helminth group also had a decrease in cobalamin CbiM genes from helminth-only infections (P = 0.000754).ConclusionThe study results may provide evidence for an effect of parasitic infections enabling the permissive growth of anaerobic bacteria such as Prevotella, suggesting an altered capacity of vitamin B12 (cobalamin) biosynthesis and potential impact on growth and development in children .

Highlights

  • 30% of children worldwide are infected with gastrointestinal parasites

  • Samples consisted of four groups: (i) a control group with no parasites detected by Multi-parallel real-time quantitative polymerase chain reaction (qPCR); (ii) a Giardia-only infected group; (iii) a Giardia and helminth co-infection group; and (iv) a helminth-only infected group

  • Alpha diversity was lower for the Giardia + helminth co-infected group compared to the helminth-only group U(19) = 7, Z = 2.958, P = 0.00178 (Fig. 1b)

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Summary

Introduction

30% of children worldwide are infected with gastrointestinal parasites. Gastrointestinal (GI) parasites are estimated to infect more than two billion people throughout the world [1] Both soil-transmitted helminths (STH) (Ascaris lumbricoides, hookworms, Strongyloides stercoralis, Trichuris trichiura) and protozoans (Giardia duodenalis, Cryptosporidium spp., Entamoeba histolytica) are prevalent in resource-limited areas [2, 3]. Disadvantaged children have recurrent infections and malnutrition that may lead to growth and cognitive delays [4]. The link between intestinal helminths and malnutrition leading to growth stunting and anemia has been found by others [5,6,7,8,9,10,11,12], and a Global Burden of Disease Study points to evidence that hookworm is a leading cause of anemia in resource-poor settings [13]. Large numbers of infected children are not being diagnosed correctly and treated

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