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Linking the effects of helminth infection, diet and the gut microbiota with human whole-blood signatures

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  • Soo Ching Lee
  • Mei San Tang
  • Alice V Easton
  • Joseph Cooper Devlin
  • Ling Ling Chua
  • Ilseung Cho
  • Foong Ming Moy
  • Tsung Fei Khang
  • Yvonne A L Lim
  • P’ng Loke

Abstract

Helminth infection and dietary intake can affect the intestinal microbiota, as well as the immune system. Here we analyzed the relationship between fecal microbiota and blood profiles of indigenous Malaysians, referred to locally as Orang Asli, in comparison to urban participants from the capital city of Malaysia, Kuala Lumpur. We found that helminth infections had a larger effect on gut microbial composition than did dietary intake or blood profiles. Trichuris trichiura infection intensity also had the strongest association with blood transcriptional profiles. By characterizing paired longitudinal samples collected before and after deworming treatment, we determined that changes in serum zinc and iron levels among the Orang Asli were driven by changes in helminth infection status, independent of dietary metal intake. Serum zinc and iron levels were associated with changes in the abundance of several microbial taxa. Hence, there is considerable interplay between helminths, micronutrients and the microbiota on the regulation of immune responses in humans.Author summary: Parasitic intestinal worms and gut bacteria occupy the same space, but we do not understand the nature and scope of their interaction. This is further complicated by dietary effects on the gut bacteria, as well as the immune responses of the host. To better understand these complex interactions, we compared individuals living in indigenous communities in Malaysia, where worm infections are common, with people living in the capital of Malaysia, who were not infected with worms. Data collected included burden of infection, a dietary survey, clinical tests, RNA profiles on blood samples and gut bacteria composition. By collecting data before and after treating the indigenous Malaysians with deworming medication, we could determine what was associated with changes in worm burden following deworming. We found that worm infection had a larger effect on gut bacteria composition than did dietary intake or blood profiles. Worm burden also had the strongest association with blood RNA profiles. We found that zinc and iron levels in the blood were associated with changes in helminth infection status, independent of dietary metal intake. Our results suggest that there is considerable interplay between intestinal worms and gut bacteria with zinc and iron levels in infected people.

Suggested Citation

  • Soo Ching Lee & Mei San Tang & Alice V Easton & Joseph Cooper Devlin & Ling Ling Chua & Ilseung Cho & Foong Ming Moy & Tsung Fei Khang & Yvonne A L Lim & P’ng Loke, 2019. "Linking the effects of helminth infection, diet and the gut microbiota with human whole-blood signatures," PLOS Pathogens, Public Library of Science, vol. 15(12), pages 1-30, December.
  • Handle: RePEc:plo:ppat00:1008066
    DOI: 10.1371/journal.ppat.1008066
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    References listed on IDEAS

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    1. Kuhn, Max, 2008. "Building Predictive Models in R Using the caret Package," Journal of Statistical Software, Foundation for Open Access Statistics, vol. 28(i05).
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