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Helminth infections predispose mice to pneumococcal pneumonia but not to other pneumonic pathogens

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Abstract

Pneumonia is the leading killer of children worldwide. Here, we report that helminth-infected mice develop fatal pneumonia when challenged with Streptococcus pneumoniae. Mice were chronically infected with either the flatworm Taenia crassiceps or the roundworm Heligmosomoides polygyrus. Upon challenge with a pneumonic type 3 strain of S. pneumoniae (A66.1), the worm-infected mice developed pneumonia at a rate and to a degree higher than age-matched control mice as measured by bioluminescent imaging and lung titers. This predisposition to pneumonia appears to be specific to S. pneumoniae, as worm-infected mice did not show evidence of increased morbidity when challenged with a lethal dose of influenza virus or sublethal doses of Staphylococcus aureus or Listeria monocytogenes. The defect was also present when worm-infected mice were challenged with a type 2 sepsis-causing strain (D39); an increased rate of pneumonia, decreased survival, and increased lung and blood titers were found. Pneumococcal colonization and immunity against acute otitis media were unaffected. Anti-helminthic treatment in the H. polygyrus model reversed this susceptibility. We conclude that helminth coinfection predisposes mice to fatal pneumococcal pneumonia by promoting increased outgrowth of bacteria in the lungs and blood. These data have broad implications for the prevention and treatment for pneumonia in the develo** world, where helminth infections are endemic and pneumococcal pneumonia is common.

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Acknowledgments

This work was supported by the American Lebanese Syrian Associated Charities (ALSAC). All authors declare that no conflict of interest exists. We would like to thank Dr. Maureen McGargill for provision of Listeria and helpful discussions on its use, and Ms. Amy Iverson and Melissa Morris for technical assistance.

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Authors and Affiliations

  1. Department of Pediatrics, University of Tennessee Health Sciences Center, 50 N. Dunlap St., Memphis, TN, 38103, USA

    Nopporn Apiwattanakul & Jonathan A. McCullers

  2. Department of Infectious Diseases, St. Jude Children’s Research Hospital, Memphis, TN, USA

    Nopporn Apiwattanakul & Jonathan A. McCullers

  3. Department of Immunology, St. Jude Children’s Research Hospital, Memphis, TN, USA

    Paul G. Thomas

  4. Department of Biology, Wake Forest University, Winston-Salem, NC, USA

    Raymond E. Kuhn

  5. Division of Experimental Medicine, University of California San Francisco, San Francisco, CA, USA

    De’Broski R. Herbert

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  1. Nopporn Apiwattanakul
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  5. Jonathan A. McCullers
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Correspondence to Jonathan A. McCullers.

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Apiwattanakul, N., Thomas, P.G., Kuhn, R.E. et al. Helminth infections predispose mice to pneumococcal pneumonia but not to other pneumonic pathogens. Med Microbiol Immunol 203, 357–364 (2014). https://doi.org/10.1007/s00430-014-0344-3

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  • DOI: https://doi.org/10.1007/s00430-014-0344-3

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