Transient Ascaris suum larval migration induces intractable chronic pulmonary disease and anemia in mice
Ascariasis is one of the most common infections in the world and associated with significant global morbidity. Ascaris larval migration through the host's lungs is essential for larval development but leads to an exaggerated type-2 host immune response manifesting clinically as acute allergic a...
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Published in | PLoS neglected tropical diseases Vol. 15; no. 12; p. e0010050 |
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Main Authors | , , , , , , , , , |
Format | Journal Article |
Language | English |
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Public Library of Science
01.12.2021
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Abstract | Ascariasis is one of the most common infections in the world and associated with significant global morbidity. Ascaris larval migration through the host's lungs is essential for larval development but leads to an exaggerated type-2 host immune response manifesting clinically as acute allergic airway disease. However, whether Ascaris larval migration can subsequently lead to chronic lung diseases remains unknown. Here, we demonstrate that a single episode of Ascaris larval migration through the host lungs induces a chronic pulmonary syndrome of type-2 inflammatory pathology and emphysema accompanied by pulmonary hemorrhage and chronic anemia in a mouse model. Our results reveal that a single episode of Ascaris larval migration through the host lungs leads to permanent lung damage with systemic effects. Remote episodes of ascariasis may drive non-communicable lung diseases such as asthma, chronic obstructive pulmonary disease (COPD), and chronic anemia in parasite endemic regions. |
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AbstractList | Ascariasis is one of the most common infections in the world and associated with significant global morbidity. Ascaris larval migration through the host’s lungs is essential for larval development but leads to an exaggerated type-2 host immune response manifesting clinically as acute allergic airway disease. However, whether Ascaris larval migration can subsequently lead to chronic lung diseases remains unknown. Here, we demonstrate that a single episode of Ascaris larval migration through the host lungs induces a chronic pulmonary syndrome of type-2 inflammatory pathology and emphysema accompanied by pulmonary hemorrhage and chronic anemia in a mouse model. Our results reveal that a single episode of Ascaris larval migration through the host lungs leads to permanent lung damage with systemic effects. Remote episodes of ascariasis may drive non-communicable lung diseases such as asthma, chronic obstructive pulmonary disease (COPD), and chronic anemia in parasite endemic regions. Ascariasis is one of the most common infections in the world and associated with significant global morbidity. Ascaris larval migration through the host’s lungs is essential for larval development but leads to an exaggerated type-2 host immune response manifesting clinically as acute allergic airway disease. However, whether Ascaris larval migration can subsequently lead to chronic lung diseases remains unknown. Here, we demonstrate that a single episode of Ascaris larval migration through the host lungs induces a chronic pulmonary syndrome of type-2 inflammatory pathology and emphysema accompanied by pulmonary hemorrhage and chronic anemia in a mouse model. Our results reveal that a single episode of Ascaris larval migration through the host lungs leads to permanent lung damage with systemic effects. Remote episodes of ascariasis may drive non-communicable lung diseases such as asthma, chronic obstructive pulmonary disease (COPD), and chronic anemia in parasite endemic regions. Ascariasis is one of the most common infections in the world and associated with significant global morbidity. Ascaris larval migration through the host’s lungs is essential for larval development but leads to an exaggerated type-2 host immune response manifesting clinically as acute allergic airway disease. However, whether Ascaris larval migration can subsequently lead to chronic lung diseases remains unknown. Here, we demonstrate that a single episode of Ascaris larval migration through the host lungs induces a chronic pulmonary syndrome of type-2 inflammatory pathology and emphysema accompanied by pulmonary hemorrhage and chronic anemia in a mouse model. Our results reveal that a single episode of Ascaris larval migration through the host lungs leads to permanent lung damage with systemic effects. Remote episodes of ascariasis may drive non-communicable lung diseases such as asthma, chronic obstructive pulmonary disease (COPD), and chronic anemia in parasite endemic regions. Ascariasis is the most common helminth infection and leads to significant global morbidity. Transient Ascaris larval migration through the host’s lungs is essential for larval development but leads to an exaggerated type-2 host immune response. Our work demonstrates that transient Ascaris spp. larval migration through the lungs has significant long-term consequences including changes in lung structure and function as well as vascular damage causing chronic lung disease and anemia. We propose that Ascaris spp. larval migration through the host lungs is a risk factor for the development of chronic lung disease and anemia in parasite-endemic regions globally. |
Audience | Academic |
Author | Burns, Alan R Gazzinelli-Guimaraes, Ana Clara Knight, Morgan Adeniyi-Ipadeola, Grace Weatherhead, Jill E Song, Li-Zhen Fujiwara, Ricardo Bottazzi, Maria Elena Wu, Yifan Li, Evan |
AuthorAffiliation | 3 College of Optometry, University of Houston, Houston, Texas, United States of America 5 National School of Tropical Medicine, Baylor College of Medicine, Houston, Texas, United States of America University of Utah, UNITED STATES 6 Texas Children’s Hospital Center for Vaccine Development, Baylor College of Medicine, Houston, Texas, United States of America 7 Department of Medicine, Infectious Diseases, Baylor College of Medicine, Houston, Texas, United States of America 1 Department of Pediatrics, Pediatric Tropical Medicine, Baylor College of Medicine, Houston, Texas, United States of America 4 Departamento de Parasitologia, Universidade Federal de Minas Gerais, Belo Horizonte, Brazil 2 Department of Medicine, Pathology and Immunology, and the Biology of Inflammation Center, Baylor College of Medicine, Houston, Texas, United States of America |
AuthorAffiliation_xml | – name: 1 Department of Pediatrics, Pediatric Tropical Medicine, Baylor College of Medicine, Houston, Texas, United States of America – name: 6 Texas Children’s Hospital Center for Vaccine Development, Baylor College of Medicine, Houston, Texas, United States of America – name: 2 Department of Medicine, Pathology and Immunology, and the Biology of Inflammation Center, Baylor College of Medicine, Houston, Texas, United States of America – name: 7 Department of Medicine, Infectious Diseases, Baylor College of Medicine, Houston, Texas, United States of America – name: University of Utah, UNITED STATES – name: 4 Departamento de Parasitologia, Universidade Federal de Minas Gerais, Belo Horizonte, Brazil – name: 3 College of Optometry, University of Houston, Houston, Texas, United States of America – name: 5 National School of Tropical Medicine, Baylor College of Medicine, Houston, Texas, United States of America |
Author_xml | – sequence: 1 givenname: Yifan surname: Wu fullname: Wu, Yifan organization: Department of Medicine, Pathology and Immunology, and the Biology of Inflammation Center, Baylor College of Medicine, Houston, Texas, United States of America – sequence: 2 givenname: Evan surname: Li fullname: Li, Evan organization: Department of Medicine, Pathology and Immunology, and the Biology of Inflammation Center, Baylor College of Medicine, Houston, Texas, United States of America – sequence: 3 givenname: Morgan surname: Knight fullname: Knight, Morgan organization: Department of Medicine, Pathology and Immunology, and the Biology of Inflammation Center, Baylor College of Medicine, Houston, Texas, United States of America – sequence: 4 givenname: Grace orcidid: 0000-0003-2076-414X surname: Adeniyi-Ipadeola fullname: Adeniyi-Ipadeola, Grace organization: Department of Pediatrics, Pediatric Tropical Medicine, Baylor College of Medicine, Houston, Texas, United States of America – sequence: 5 givenname: Li-Zhen surname: Song fullname: Song, Li-Zhen organization: Department of Medicine, Pathology and Immunology, and the Biology of Inflammation Center, Baylor College of Medicine, Houston, Texas, United States of America – sequence: 6 givenname: Alan R surname: Burns fullname: Burns, Alan R organization: College of Optometry, University of Houston, Houston, Texas, United States of America – sequence: 7 givenname: Ana Clara orcidid: 0000-0003-1716-328X surname: Gazzinelli-Guimaraes fullname: Gazzinelli-Guimaraes, Ana Clara organization: Departamento de Parasitologia, Universidade Federal de Minas Gerais, Belo Horizonte, Brazil – sequence: 8 givenname: Ricardo orcidid: 0000-0002-4713-575X surname: Fujiwara fullname: Fujiwara, Ricardo organization: Departamento de Parasitologia, Universidade Federal de Minas Gerais, Belo Horizonte, Brazil – sequence: 9 givenname: Maria Elena orcidid: 0000-0002-8429-0476 surname: Bottazzi fullname: Bottazzi, Maria Elena organization: Texas Children's Hospital Center for Vaccine Development, Baylor College of Medicine, Houston, Texas, United States of America – sequence: 10 givenname: Jill E orcidid: 0000-0002-8043-3177 surname: Weatherhead fullname: Weatherhead, Jill E organization: Department of Medicine, Infectious Diseases, Baylor College of Medicine, Houston, Texas, United States of America |
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CitedBy_id | crossref_primary_10_1371_journal_pntd_0011930 crossref_primary_10_1002_clt2_12232 crossref_primary_10_1002_clt2_12291 crossref_primary_10_1016_j_micpath_2024_106567 crossref_primary_10_1177_00494755241226488 crossref_primary_10_3389_fimmu_2022_941977 crossref_primary_10_1016_j_micpath_2023_106483 crossref_primary_10_3389_fcimb_2022_852900 |
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Copyright | COPYRIGHT 2021 Public Library of Science 2021 Wu et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. 2021 Wu et al 2021 Wu et al |
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Notes | new_version ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 The authors have declared that no competing interests exist. |
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SubjectTerms | Allergic diseases Anaemia Anemia Anemia - genetics Anemia - immunology Anemia - parasitology Anemia - pathology Animals Ascariasis Ascariasis - genetics Ascariasis - immunology Ascariasis - parasitology Ascariasis - pathology Ascaris Ascaris suum - genetics Ascaris suum - physiology Asthma Biology and Life Sciences Chemokines Chronic Disease Chronic obstructive pulmonary disease Complications and side effects Cytokines Cytokines - genetics Cytokines - immunology Defence mechanisms Development and progression Developmental stages Diseases Emphysema Female Haemorrhage Health aspects Hemorrhage Humans Immune response Immunity Infections Inflammation Larva - genetics Larva - physiology Larvae Larval development Larval stage Lavage Ligands Lung - immunology Lung - parasitology Lung - pathology Lung diseases Lung Diseases - genetics Lung Diseases - immunology Lung Diseases - parasitology Lung Diseases - pathology Lungs Medicine and Health Sciences Mice Mice, Inbred BALB C Morbidity Obstructive lung disease Parasites Pathology Research and Analysis Methods Respiratory system Respiratory tract diseases Risk factors Tropical diseases |
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Title | Transient Ascaris suum larval migration induces intractable chronic pulmonary disease and anemia in mice |
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