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Fungal and Parasitic Infections

Ascaris Larval Infection and Lung Invasion Directly Induce Severe Allergic Airway Disease in Mice

Jill E. Weatherhead, Paul Porter, Amy Coffey, Dana Haydel, Leroy Versteeg, Bin Zhan, Ana Clara Gazzinelli Guimarães, Ricardo Fujiwara, Ana M. Jaramillo, Maria Elena Bottazzi, Peter J. Hotez, David B. Corry, Coreen M. Beaumier
John H. Adams, Editor
Jill E. Weatherhead
Department of Pediatrics, Baylor College of Medicine, Houston, Texas, USADepartment of Medicine, Baylor College of Medicine, Houston, Texas, USANational School of Tropical Medicine, Baylor College of Medicine, Houston, Texas, USA
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Paul Porter
Department of Medicine, Baylor College of Medicine, Houston, Texas, USA
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Amy Coffey
Department of Pathology and Immunology, Baylor College of Medicine, Houston, Texas, USA
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Dana Haydel
Department of Pathology and Immunology, Baylor College of Medicine, Houston, Texas, USA
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Leroy Versteeg
Department of Pediatrics, Baylor College of Medicine, Houston, Texas, USA
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Bin Zhan
Department of Pediatrics, Baylor College of Medicine, Houston, Texas, USANational School of Tropical Medicine, Baylor College of Medicine, Houston, Texas, USA
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Ana Clara Gazzinelli Guimarães
Departamento de Parasitologia, Federal University of Minas Gerais, Minas Gerais, Brazil
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Ricardo Fujiwara
Departamento de Parasitologia, Federal University of Minas Gerais, Minas Gerais, Brazil
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Ana M. Jaramillo
Department of Pulmonary Medicine, University of Texas MD Anderson Cancer Center, Houston, Texas, USA
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Maria Elena Bottazzi
Department of Pediatrics, Baylor College of Medicine, Houston, Texas, USANational School of Tropical Medicine, Baylor College of Medicine, Houston, Texas, USADepartment of Molecular Virology and Microbiology, Baylor College of Medicine, Houston, Texas, USATexas Children’s Hospital Center for Vaccine Development-Product Development Partnership, Houston, Texas, USA
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Peter J. Hotez
Department of Pediatrics, Baylor College of Medicine, Houston, Texas, USANational School of Tropical Medicine, Baylor College of Medicine, Houston, Texas, USADepartment of Molecular Virology and Microbiology, Baylor College of Medicine, Houston, Texas, USATexas Children’s Hospital Center for Vaccine Development-Product Development Partnership, Houston, Texas, USA
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David B. Corry
Department of Medicine, Baylor College of Medicine, Houston, Texas, USADepartment of Pathology and Immunology, Baylor College of Medicine, Houston, Texas, USABiology of Inflammation Center, Baylor College of Medicine, Houston, Texas, USAMichael E. DeBakey Center for Translational Research in Inflammatory Diseases, Houston, Texas, USA
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Coreen M. Beaumier
Department of Pediatrics, Baylor College of Medicine, Houston, Texas, USADepartment of Molecular Virology and Microbiology, Baylor College of Medicine, Houston, Texas, USA
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John H. Adams
University of South Florida
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DOI: 10.1128/IAI.00533-18
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ABSTRACT

Ascaris lumbricoides (roundworm) is the most common helminth infection globally and a cause of lifelong morbidity that may include allergic airway disease, an asthma phenotype. We hypothesize that Ascaris larval migration through the lungs leads to persistent airway hyperresponsiveness (AHR) and type 2 inflammatory lung pathology despite resolution of infection that resembles allergic airway disease. Mice were infected with Ascaris by oral gavage. Lung AHR was measured by plethysmography and histopathology with hematoxylin and eosin (H&E) and periodic acid-Schiff (PAS) stains, and cytokine concentrations were measured by using Luminex Magpix. Ascaris-infected mice were compared to controls or mice with allergic airway disease induced by ovalbumin (OVA) sensitization and challenge (OVA/OVA). Ascaris-infected mice developed profound AHR starting at day 8 postinfection (p.i.), peaking at day 12 p.i. and persisting through day 21 p.i., despite resolution of infection, which was significantly increased compared to controls and OVA/OVA mice. Ascaris-infected mice had a robust type 2 cytokine response in both the bronchoalveolar lavage (BAL) fluid and lung tissue, similar to that of the OVA/OVA mice, including interleukin-4 (IL-4) (P < 0.01 and P < 0.01, respectively), IL-5 (P < 0.001 and P < 0.001), and IL-13 (P < 0.001 and P < 0.01), compared to controls. By histopathology, Ascaris-infected mice demonstrated early airway remodeling similar to, but more profound than, that in OVA/OVA mice. We found that Ascaris larval migration causes significant pulmonary damage, including AHR and type 2 inflammatory lung pathology that resembles an extreme form of allergic airway disease. Our findings indicate that ascariasis may be an important cause of allergic airway disease in regions of endemicity.

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Ascaris Larval Infection and Lung Invasion Directly Induce Severe Allergic Airway Disease in Mice
Jill E. Weatherhead, Paul Porter, Amy Coffey, Dana Haydel, Leroy Versteeg, Bin Zhan, Ana Clara Gazzinelli Guimarães, Ricardo Fujiwara, Ana M. Jaramillo, Maria Elena Bottazzi, Peter J. Hotez, David B. Corry, Coreen M. Beaumier
Infection and Immunity Nov 2018, 86 (12) e00533-18; DOI: 10.1128/IAI.00533-18

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Ascaris Larval Infection and Lung Invasion Directly Induce Severe Allergic Airway Disease in Mice
Jill E. Weatherhead, Paul Porter, Amy Coffey, Dana Haydel, Leroy Versteeg, Bin Zhan, Ana Clara Gazzinelli Guimarães, Ricardo Fujiwara, Ana M. Jaramillo, Maria Elena Bottazzi, Peter J. Hotez, David B. Corry, Coreen M. Beaumier
Infection and Immunity Nov 2018, 86 (12) e00533-18; DOI: 10.1128/IAI.00533-18
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KEYWORDS

Ascaris
airway hyperreactivity
allergic airway disease
asthma
hygiene hypothesis

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