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Giardia hinders growth by disrupting nutrient metabolism independent of inflammatory enteropathy

Author

Listed:
  • Natasa Giallourou

    (Imperial College London
    University of Cyprus)

  • Jason Arnold

    (University of North Carolina at Chapel Hill
    Duke University School of Medicine)

  • Elizabeth T. Rogawski McQuade

    (Emory University)

  • Muyiwa Awoniyi

    (University of North Carolina at Chapel Hill)

  • Rose Viguna Thomas Becket

    (The University of North Carolina at Chapel Hill)

  • Kenneth Walsh

    (The University of North Carolina at Chapel Hill)

  • Jeremy Herzog

    (University of North Carolina at Chapel Hill)

  • Ajay S. Gulati

    (The University of North Carolina at Chapel Hill)

  • Ian M. Carroll

    (The University of North Carolina at Chapel Hill)

  • Stephanie Montgomery

    (The University of North Carolina at Chapel Hill)

  • Pedro Henrique Quintela

    (Federal University of CearĂ¡)

  • Angela M. Faust

    (Waterborne, Inc)

  • Steven M. Singer

    (Georgetown University)

  • Anthony A. Fodor

    (The University of North Carolina Charlotte, Department of Bioinformatics and Genomics)

  • Tahmeed Ahmad

    (International Center for Diarrheal Disease Research)

  • Mustafa Mahfuz

    (International Center for Diarrheal Disease Research)

  • Esto Mduma

    (Haydom Lutheran Hospital)

  • Thomas Walongo

    (Haydom Lutheran Hospital)

  • Richard L. Guerrant

    (The University of Virginia Charlottesville)

  • R. Balfour Sartor

    (University of North Carolina at Chapel Hill)

  • Jonathan R. Swann

    (University of Southampton)

  • Margaret N. Kosek

    (The University of Virginia Charlottesville)

  • Luther A. Bartelt

    (University of North Carolina at Chapel Hill
    The University of North Carolina at Chapel Hill
    University of North Carolina at Chapel Hill)

Abstract

Giardia lamblia (Giardia) is among the most common intestinal pathogens in children in low- and middle-income countries (LMICs). Although Giardia associates with early-life linear growth restriction, mechanistic explanations for Giardia-associated growth impairments remain elusive. Unlike other intestinal pathogens associated with constrained linear growth that cause intestinal or systemic inflammation or both, Giardia seldom associates with chronic inflammation in these children. Here we leverage the MAL-ED longitudinal birth cohort and a model of Giardia mono-association in gnotobiotic and immunodeficient mice to propose an alternative pathogenesis of this parasite. In children, Giardia results in linear growth deficits and gut permeability that are dose-dependent and independent of intestinal markers of inflammation. The estimates of these findings vary between children in different MAL-ED sites. In a representative site, where Giardia associates with growth restriction, infected children demonstrate broad amino acid deficiencies, and overproduction of specific phenolic acids, byproducts of intestinal bacterial amino acid metabolism. Gnotobiotic mice require specific nutritional and environmental conditions to recapitulate these findings, and immunodeficient mice confirm a pathway independent of chronic T/B cell inflammation. Taken together, we propose a new paradigm that Giardia-mediated growth faltering is contingent upon a convergence of this intestinal protozoa with nutritional and intestinal bacterial factors.

Suggested Citation

  • Natasa Giallourou & Jason Arnold & Elizabeth T. Rogawski McQuade & Muyiwa Awoniyi & Rose Viguna Thomas Becket & Kenneth Walsh & Jeremy Herzog & Ajay S. Gulati & Ian M. Carroll & Stephanie Montgomery &, 2023. "Giardia hinders growth by disrupting nutrient metabolism independent of inflammatory enteropathy," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-38363-2
    DOI: 10.1038/s41467-023-38363-2
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    References listed on IDEAS

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    1. Eric M. Brown & Marta Wlodarska & Benjamin P. Willing & Pascale Vonaesch & Jun Han & Lisa A. Reynolds & Marie-Claire Arrieta & Marco Uhrig & Roland Scholz & Oswaldo Partida & Christoph H. Borchers & P, 2015. "Diet and specific microbial exposure trigger features of environmental enteropathy in a novel murine model," Nature Communications, Nature, vol. 6(1), pages 1-16, November.
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