Host innate immune responses and microbiome profile of neonatal calves challenged with Cryptosporidium parvum and the effect of bovine colostrum supplementation
IntroductionCalves are highly susceptible to gastrointestinal infection with Cryptosporidium parvum (C. parvum), which can result in watery diarrhea and eventually death or impaired development. With little to no effective therapeutics, understanding the host’s microbiota and pathogen interaction at...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2023-05-01
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| Series: | Frontiers in Cellular and Infection Microbiology |
| Subjects: | |
| Online Access: | https://www.frontiersin.org/articles/10.3389/fcimb.2023.1165312/full |
| _version_ | 1827955193000493056 |
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| author | Lisa Gamsjäger Karina M. Cirone Steffany Schluessel Mackenzie Campsall Aydin Herik Priyoshi Lahiri Daniel Young Daniel Young Antoine Dufour Antoine Dufour Panagiotis Sapountzis Saria Otani Diego E. Gomez M. Claire Windeyer Eduardo R. Cobo |
| author_facet | Lisa Gamsjäger Karina M. Cirone Steffany Schluessel Mackenzie Campsall Aydin Herik Priyoshi Lahiri Daniel Young Daniel Young Antoine Dufour Antoine Dufour Panagiotis Sapountzis Saria Otani Diego E. Gomez M. Claire Windeyer Eduardo R. Cobo |
| author_sort | Lisa Gamsjäger |
| collection | DOAJ |
| description | IntroductionCalves are highly susceptible to gastrointestinal infection with Cryptosporidium parvum (C. parvum), which can result in watery diarrhea and eventually death or impaired development. With little to no effective therapeutics, understanding the host’s microbiota and pathogen interaction at the mucosal immune system has been critical to identify and test novel control strategies.MethodsHerein, we used an experimental model of C. parvum challenge in neonatal calves to describe the clinical signs and histological and proteomic profiling of the mucosal innate immunity and microbiota shifts by metagenomics in the ileum and colon during cryptosporidiosis. Also, we investigated the impact of supplemental colostrum feeding on C. parvum infection.ResultsWe showed that C. parvum challenged calves experienced clinical signs including pyrexia and diarrhea 5 days post challenge. These calves showed ulcerative neutrophil ileitis with a proteomic signature driven by inflammatory effectors, including reactive oxygen species and myeloperoxidases. Colitis was also noticed with an aggravated mucin barrier depletion and incompletely filled goblet cells. The C. parvum challenged calves also displayed a pronounced dysbiosis with a high prevalence of Clostridium species (spp.) and number of exotoxins, adherence factors, and secretion systems related to Clostridium spp. and other enteropathogens, including Campylobacter spp., Escherichia sp., Shigella spp., and Listeria spp. Daily supplementation with a high-quality bovine colostrum product mitigated some of the clinical signs and modulated the gut immune response and concomitant microbiota to a pattern more similar to that of healthy unchallenged calves.DiscussionC. parvum infection in neonatal calves provoked severe diarrheic neutrophilic enterocolitis, perhaps augmented due to the lack of fully developed innate gut defenses. Colostrum supplementation showed limited effect mitigating diarrhea but demonstrated some clinical alleviation and specific modulatory influence on host gut immune responses and concomitant microbiota. |
| first_indexed | 2024-04-09T14:42:00Z |
| format | Article |
| id | doaj.art-1bc03cea11c541a2afb7c5cce34a8cca |
| institution | Directory Open Access Journal |
| issn | 2235-2988 |
| language | English |
| last_indexed | 2024-04-09T14:42:00Z |
| publishDate | 2023-05-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Cellular and Infection Microbiology |
| spelling | doaj.art-1bc03cea11c541a2afb7c5cce34a8cca2023-05-03T05:23:18ZengFrontiers Media S.A.Frontiers in Cellular and Infection Microbiology2235-29882023-05-011310.3389/fcimb.2023.11653121165312Host innate immune responses and microbiome profile of neonatal calves challenged with Cryptosporidium parvum and the effect of bovine colostrum supplementationLisa Gamsjäger0Karina M. Cirone1Steffany Schluessel2Mackenzie Campsall3Aydin Herik4Priyoshi Lahiri5Daniel Young6Daniel Young7Antoine Dufour8Antoine Dufour9Panagiotis Sapountzis10Saria Otani11Diego E. Gomez12M. Claire Windeyer13Eduardo R. Cobo14Faculty of Veterinary Medicine, University of Calgary, Calgary, AB, CanadaLaboratorio de Bacteriología, Grupo de Sanidad Animal, Unidad Integrada INTA, Universidad Nacional de Mar del Plata (UNMdP), Balcarce, Buenos Aires, ArgentinaFaculty of Veterinary Medicine, University of Calgary, Calgary, AB, CanadaFaculty of Veterinary Medicine, University of Calgary, Calgary, AB, CanadaFaculty of Veterinary Medicine, University of Calgary, Calgary, AB, CanadaFaculty of Veterinary Medicine, University of Calgary, Calgary, AB, CanadaPhysiology and Pharmacology, Cumming School of Medicine, University of Calgary, Calgary, AB, CanadaMcCaig Institute for Bone and Joint Health, Cumming School of Medicine, University of Calgary, Calgary, AB, CanadaPhysiology and Pharmacology, Cumming School of Medicine, University of Calgary, Calgary, AB, CanadaMcCaig Institute for Bone and Joint Health, Cumming School of Medicine, University of Calgary, Calgary, AB, CanadaUniversité Clermont Auvergne, Institut national de recherche pour l'agriculture, l'alimentation et l'environnement, Clermont-Ferrand, FranceNational Food Institute, Technical University of Denmark, Kongens Lyngby, DenmarkDepartment of Clinical Studies, Ontario Veterinary College, University of Guelph, Guelph, ON, CanadaFaculty of Veterinary Medicine, University of Calgary, Calgary, AB, CanadaFaculty of Veterinary Medicine, University of Calgary, Calgary, AB, CanadaIntroductionCalves are highly susceptible to gastrointestinal infection with Cryptosporidium parvum (C. parvum), which can result in watery diarrhea and eventually death or impaired development. With little to no effective therapeutics, understanding the host’s microbiota and pathogen interaction at the mucosal immune system has been critical to identify and test novel control strategies.MethodsHerein, we used an experimental model of C. parvum challenge in neonatal calves to describe the clinical signs and histological and proteomic profiling of the mucosal innate immunity and microbiota shifts by metagenomics in the ileum and colon during cryptosporidiosis. Also, we investigated the impact of supplemental colostrum feeding on C. parvum infection.ResultsWe showed that C. parvum challenged calves experienced clinical signs including pyrexia and diarrhea 5 days post challenge. These calves showed ulcerative neutrophil ileitis with a proteomic signature driven by inflammatory effectors, including reactive oxygen species and myeloperoxidases. Colitis was also noticed with an aggravated mucin barrier depletion and incompletely filled goblet cells. The C. parvum challenged calves also displayed a pronounced dysbiosis with a high prevalence of Clostridium species (spp.) and number of exotoxins, adherence factors, and secretion systems related to Clostridium spp. and other enteropathogens, including Campylobacter spp., Escherichia sp., Shigella spp., and Listeria spp. Daily supplementation with a high-quality bovine colostrum product mitigated some of the clinical signs and modulated the gut immune response and concomitant microbiota to a pattern more similar to that of healthy unchallenged calves.DiscussionC. parvum infection in neonatal calves provoked severe diarrheic neutrophilic enterocolitis, perhaps augmented due to the lack of fully developed innate gut defenses. Colostrum supplementation showed limited effect mitigating diarrhea but demonstrated some clinical alleviation and specific modulatory influence on host gut immune responses and concomitant microbiota.https://www.frontiersin.org/articles/10.3389/fcimb.2023.1165312/fullCryptosporidium parvumcattleenterocolitiscolostrum administrationmicrobiota |
| spellingShingle | Lisa Gamsjäger Karina M. Cirone Steffany Schluessel Mackenzie Campsall Aydin Herik Priyoshi Lahiri Daniel Young Daniel Young Antoine Dufour Antoine Dufour Panagiotis Sapountzis Saria Otani Diego E. Gomez M. Claire Windeyer Eduardo R. Cobo Host innate immune responses and microbiome profile of neonatal calves challenged with Cryptosporidium parvum and the effect of bovine colostrum supplementation Frontiers in Cellular and Infection Microbiology Cryptosporidium parvum cattle enterocolitis colostrum administration microbiota |
| title | Host innate immune responses and microbiome profile of neonatal calves challenged with Cryptosporidium parvum and the effect of bovine colostrum supplementation |
| title_full | Host innate immune responses and microbiome profile of neonatal calves challenged with Cryptosporidium parvum and the effect of bovine colostrum supplementation |
| title_fullStr | Host innate immune responses and microbiome profile of neonatal calves challenged with Cryptosporidium parvum and the effect of bovine colostrum supplementation |
| title_full_unstemmed | Host innate immune responses and microbiome profile of neonatal calves challenged with Cryptosporidium parvum and the effect of bovine colostrum supplementation |
| title_short | Host innate immune responses and microbiome profile of neonatal calves challenged with Cryptosporidium parvum and the effect of bovine colostrum supplementation |
| title_sort | host innate immune responses and microbiome profile of neonatal calves challenged with cryptosporidium parvum and the effect of bovine colostrum supplementation |
| topic | Cryptosporidium parvum cattle enterocolitis colostrum administration microbiota |
| url | https://www.frontiersin.org/articles/10.3389/fcimb.2023.1165312/full |
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