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The Rumen Microbiota Contributes to the Development of Mastitis in Dairy Cows
Mastitis, a highly prevalent disease in dairy cows, is commonly caused by local infection of the mammary gland. Our previous studies have suggested that the gut microbiota plays an important role in the development of mastitis in mice. However, the effects of rumen microbiota on bovine mastitis and...
Autores principales: | , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
American Society for Microbiology
2022
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8865570/ https://www.ncbi.nlm.nih.gov/pubmed/35196821 http://dx.doi.org/10.1128/spectrum.02512-21 |
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author | Hu, Xiaoyu Li, Shuang Mu, Ruiying Guo, Jian Zhao, Caijun Cao, Yongguo Zhang, Naisheng Fu, Yunhe |
author_facet | Hu, Xiaoyu Li, Shuang Mu, Ruiying Guo, Jian Zhao, Caijun Cao, Yongguo Zhang, Naisheng Fu, Yunhe |
author_sort | Hu, Xiaoyu |
collection | PubMed |
description | Mastitis, a highly prevalent disease in dairy cows, is commonly caused by local infection of the mammary gland. Our previous studies have suggested that the gut microbiota plays an important role in the development of mastitis in mice. However, the effects of rumen microbiota on bovine mastitis and the related mechanisms remain unclear. In this study, we assessed the effects and mechanisms of rumen microbiota on bovine mastitis based on the subacute rumen acidosis (SARA) model induced by feeding Holstein Frisian cows a high-concentrate diet for 8 weeks. Then, the inflammatory responses in the mammary gland and the bacterial communities of rumen fluid, feces, and milk were analyzed. The results showed that SARA induced mastitis symptoms in the mammary gland; activated a systemic inflammatory response; and increased the permeability of the blood-milk barrier, gut barrier, and rumen barrier. Further research showed that lipopolysaccharides (LPS), derived from the gut of SARA cows, translocated into the blood and accumulated in the mammary glands. Furthermore, the abundance of Stenotrophomonas was increased in the rumen of SARA cows, and mastitis was induced by oral administration of Stenotrophomonas in lactating mice. In conclusion, our findings suggested that mastitis is induced by exogenous pathogenic microorganisms as well as by endogenous pathogenic factors. Specifically, the elevated abundance of Stenotrophomonas in the rumen and LPS translocation from the rumen to the mammary gland were important endogenous factors that induced mastitis. Our study provides a foundation for novel therapeutic strategies that target the rumen microbiota in cow mastitis. IMPORTANCE Mastitis is a common and frequently occurring disease of humans and animals, especially in dairy farming, which has caused huge economic losses and brought harmful substance residues, drug-resistant bacteria, and other public health risks. The traditional viewpoint indicates that mastitis is mainly caused by exogenous pathogenic bacteria infecting the mammary gland. Our study found that the occurrence of mastitis was induced by the endogenous pathway. Evidence has shown that rumen-derived LPS enters the mammary gland through blood circulation, damaging the blood-milk barrier and then inducing inflammation of the mammary gland in cows. In addition, a higher abundance of Stenotrophomonas in the rumen was closely associated with the development of mastitis. This study provides a basis for novel therapeutic strategies that exploit the rumen microbiota against mastitis in cows. |
format | Online Article Text |
id | pubmed-8865570 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | American Society for Microbiology |
record_format | MEDLINE/PubMed |
spelling | pubmed-88655702022-03-04 The Rumen Microbiota Contributes to the Development of Mastitis in Dairy Cows Hu, Xiaoyu Li, Shuang Mu, Ruiying Guo, Jian Zhao, Caijun Cao, Yongguo Zhang, Naisheng Fu, Yunhe Microbiol Spectr Research Article Mastitis, a highly prevalent disease in dairy cows, is commonly caused by local infection of the mammary gland. Our previous studies have suggested that the gut microbiota plays an important role in the development of mastitis in mice. However, the effects of rumen microbiota on bovine mastitis and the related mechanisms remain unclear. In this study, we assessed the effects and mechanisms of rumen microbiota on bovine mastitis based on the subacute rumen acidosis (SARA) model induced by feeding Holstein Frisian cows a high-concentrate diet for 8 weeks. Then, the inflammatory responses in the mammary gland and the bacterial communities of rumen fluid, feces, and milk were analyzed. The results showed that SARA induced mastitis symptoms in the mammary gland; activated a systemic inflammatory response; and increased the permeability of the blood-milk barrier, gut barrier, and rumen barrier. Further research showed that lipopolysaccharides (LPS), derived from the gut of SARA cows, translocated into the blood and accumulated in the mammary glands. Furthermore, the abundance of Stenotrophomonas was increased in the rumen of SARA cows, and mastitis was induced by oral administration of Stenotrophomonas in lactating mice. In conclusion, our findings suggested that mastitis is induced by exogenous pathogenic microorganisms as well as by endogenous pathogenic factors. Specifically, the elevated abundance of Stenotrophomonas in the rumen and LPS translocation from the rumen to the mammary gland were important endogenous factors that induced mastitis. Our study provides a foundation for novel therapeutic strategies that target the rumen microbiota in cow mastitis. IMPORTANCE Mastitis is a common and frequently occurring disease of humans and animals, especially in dairy farming, which has caused huge economic losses and brought harmful substance residues, drug-resistant bacteria, and other public health risks. The traditional viewpoint indicates that mastitis is mainly caused by exogenous pathogenic bacteria infecting the mammary gland. Our study found that the occurrence of mastitis was induced by the endogenous pathway. Evidence has shown that rumen-derived LPS enters the mammary gland through blood circulation, damaging the blood-milk barrier and then inducing inflammation of the mammary gland in cows. In addition, a higher abundance of Stenotrophomonas in the rumen was closely associated with the development of mastitis. This study provides a basis for novel therapeutic strategies that exploit the rumen microbiota against mastitis in cows. American Society for Microbiology 2022-02-16 /pmc/articles/PMC8865570/ /pubmed/35196821 http://dx.doi.org/10.1128/spectrum.02512-21 Text en Copyright © 2022 Hu et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) . |
spellingShingle | Research Article Hu, Xiaoyu Li, Shuang Mu, Ruiying Guo, Jian Zhao, Caijun Cao, Yongguo Zhang, Naisheng Fu, Yunhe The Rumen Microbiota Contributes to the Development of Mastitis in Dairy Cows |
title | The Rumen Microbiota Contributes to the Development of Mastitis in Dairy Cows |
title_full | The Rumen Microbiota Contributes to the Development of Mastitis in Dairy Cows |
title_fullStr | The Rumen Microbiota Contributes to the Development of Mastitis in Dairy Cows |
title_full_unstemmed | The Rumen Microbiota Contributes to the Development of Mastitis in Dairy Cows |
title_short | The Rumen Microbiota Contributes to the Development of Mastitis in Dairy Cows |
title_sort | rumen microbiota contributes to the development of mastitis in dairy cows |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8865570/ https://www.ncbi.nlm.nih.gov/pubmed/35196821 http://dx.doi.org/10.1128/spectrum.02512-21 |
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