Persistent effects of intramammary ceftiofur treatment on the gut microbiome and antibiotic resistance in dairy cattle
Abstract Background Intramammary (IMM) ceftiofur treatment is commonly used in dairy farms to prevent mastitis, though its impact on the cattle gut microbiome and selection of antibiotic-resistant bacteria has not been elucidated. Herein, we enrolled 40 dairy (Holstein) cows at the end of the lactat...
| Main Authors: | , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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BMC
2023-11-01
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| Series: | Animal Microbiome |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s42523-023-00274-4 |
| _version_ | 1827764148026474496 |
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| author | Karla A. Vasco Samantha Carbonell Rebekah E. Sloup Bailey Bowcutt Rita R. Colwell Karlis Graubics Ronald Erskine Bo Norby Pamela L. Ruegg Lixin Zhang Shannon D. Manning |
| author_facet | Karla A. Vasco Samantha Carbonell Rebekah E. Sloup Bailey Bowcutt Rita R. Colwell Karlis Graubics Ronald Erskine Bo Norby Pamela L. Ruegg Lixin Zhang Shannon D. Manning |
| author_sort | Karla A. Vasco |
| collection | DOAJ |
| description | Abstract Background Intramammary (IMM) ceftiofur treatment is commonly used in dairy farms to prevent mastitis, though its impact on the cattle gut microbiome and selection of antibiotic-resistant bacteria has not been elucidated. Herein, we enrolled 40 dairy (Holstein) cows at the end of the lactation phase for dry-cow therapy: 20 were treated with IMM ceftiofur (Spectramast®DC) and a non-antibiotic internal teat sealant (bismuth subnitrate) and 20 (controls) received only bismuth subnitrate. Fecal grab samples were collected before and after treatment (weeks 1, 2, 3, 5, 7, and 9) for bacterial quantification and metagenomic next-generation sequencing. Results Overall, 90% and 24% of the 278 samples had Gram-negative bacteria with resistance to ampicillin and ceftiofur, respectively. Most of the cows treated with ceftiofur did not have an increase in the number of resistant bacteria; however, a subset (25%) shed higher levels of ceftiofur-resistant bacteria for up to 2 weeks post-treatment. At week 5, the antibiotic-treated cows had lower microbiota abundance and richness, whereas a greater abundance of genes encoding extended-spectrum β-lactamases (ESBLs), CfxA, ACI-1, and CMY, was observed at weeks 1, 5 and 9. Moreover, the contig and network analyses detected associations between β-lactam resistance genes and phages, mobile genetic elements, and specific genera. Commensal bacterial populations belonging to Bacteroidetes most commonly possessed ESBL genes followed by members of Enterobacteriaceae. Conclusion This study highlights variable, persistent effects of IMM ceftiofur treatment on the gut microbiome and resistome in dairy cattle. Antibiotic-treated cattle had an increased abundance of specific taxa and genes encoding ESBL production that persisted for 9 weeks. Fecal shedding of ESBL-producing Enterobacteriaceae, which was classified as a serious public health threat, varied across animals. Together, these findings highlight the need for additional studies aimed at identifying factors associated with shedding levels and the dissemination and persistence of antibiotic resistance determinants on dairy farms across geographic locations. |
| first_indexed | 2024-03-11T11:01:38Z |
| format | Article |
| id | doaj.art-debeec842951491fb511162737f818ef |
| institution | Directory Open Access Journal |
| issn | 2524-4671 |
| language | English |
| last_indexed | 2024-03-11T11:01:38Z |
| publishDate | 2023-11-01 |
| publisher | BMC |
| record_format | Article |
| series | Animal Microbiome |
| spelling | doaj.art-debeec842951491fb511162737f818ef2023-11-12T12:31:01ZengBMCAnimal Microbiome2524-46712023-11-015111910.1186/s42523-023-00274-4Persistent effects of intramammary ceftiofur treatment on the gut microbiome and antibiotic resistance in dairy cattleKarla A. Vasco0Samantha Carbonell1Rebekah E. Sloup2Bailey Bowcutt3Rita R. Colwell4Karlis Graubics5Ronald Erskine6Bo Norby7Pamela L. Ruegg8Lixin Zhang9Shannon D. Manning10Department of Microbiology and Molecular Genetics, Michigan State UniversityDepartment of Microbiology and Molecular Genetics, Michigan State UniversityDepartment of Microbiology and Molecular Genetics, Michigan State UniversityDepartment of Microbiology and Molecular Genetics, Michigan State UniversityUniversity of Maryland, Institute for Advanced Computer StudiesCosmos ID, IncDepartment of Large Animal Clinical Sciences, Michigan State UniversityDepartment of Large Animal Clinical Sciences, Michigan State UniversityDepartment of Large Animal Clinical Sciences, Michigan State UniversityDepartment of Microbiology and Molecular Genetics, Michigan State UniversityDepartment of Microbiology and Molecular Genetics, Michigan State UniversityAbstract Background Intramammary (IMM) ceftiofur treatment is commonly used in dairy farms to prevent mastitis, though its impact on the cattle gut microbiome and selection of antibiotic-resistant bacteria has not been elucidated. Herein, we enrolled 40 dairy (Holstein) cows at the end of the lactation phase for dry-cow therapy: 20 were treated with IMM ceftiofur (Spectramast®DC) and a non-antibiotic internal teat sealant (bismuth subnitrate) and 20 (controls) received only bismuth subnitrate. Fecal grab samples were collected before and after treatment (weeks 1, 2, 3, 5, 7, and 9) for bacterial quantification and metagenomic next-generation sequencing. Results Overall, 90% and 24% of the 278 samples had Gram-negative bacteria with resistance to ampicillin and ceftiofur, respectively. Most of the cows treated with ceftiofur did not have an increase in the number of resistant bacteria; however, a subset (25%) shed higher levels of ceftiofur-resistant bacteria for up to 2 weeks post-treatment. At week 5, the antibiotic-treated cows had lower microbiota abundance and richness, whereas a greater abundance of genes encoding extended-spectrum β-lactamases (ESBLs), CfxA, ACI-1, and CMY, was observed at weeks 1, 5 and 9. Moreover, the contig and network analyses detected associations between β-lactam resistance genes and phages, mobile genetic elements, and specific genera. Commensal bacterial populations belonging to Bacteroidetes most commonly possessed ESBL genes followed by members of Enterobacteriaceae. Conclusion This study highlights variable, persistent effects of IMM ceftiofur treatment on the gut microbiome and resistome in dairy cattle. Antibiotic-treated cattle had an increased abundance of specific taxa and genes encoding ESBL production that persisted for 9 weeks. Fecal shedding of ESBL-producing Enterobacteriaceae, which was classified as a serious public health threat, varied across animals. Together, these findings highlight the need for additional studies aimed at identifying factors associated with shedding levels and the dissemination and persistence of antibiotic resistance determinants on dairy farms across geographic locations.https://doi.org/10.1186/s42523-023-00274-4CattleMastitisAntibiotic resistanceMicrobiomeResistomeCeftiofur |
| spellingShingle | Karla A. Vasco Samantha Carbonell Rebekah E. Sloup Bailey Bowcutt Rita R. Colwell Karlis Graubics Ronald Erskine Bo Norby Pamela L. Ruegg Lixin Zhang Shannon D. Manning Persistent effects of intramammary ceftiofur treatment on the gut microbiome and antibiotic resistance in dairy cattle Animal Microbiome Cattle Mastitis Antibiotic resistance Microbiome Resistome Ceftiofur |
| title | Persistent effects of intramammary ceftiofur treatment on the gut microbiome and antibiotic resistance in dairy cattle |
| title_full | Persistent effects of intramammary ceftiofur treatment on the gut microbiome and antibiotic resistance in dairy cattle |
| title_fullStr | Persistent effects of intramammary ceftiofur treatment on the gut microbiome and antibiotic resistance in dairy cattle |
| title_full_unstemmed | Persistent effects of intramammary ceftiofur treatment on the gut microbiome and antibiotic resistance in dairy cattle |
| title_short | Persistent effects of intramammary ceftiofur treatment on the gut microbiome and antibiotic resistance in dairy cattle |
| title_sort | persistent effects of intramammary ceftiofur treatment on the gut microbiome and antibiotic resistance in dairy cattle |
| topic | Cattle Mastitis Antibiotic resistance Microbiome Resistome Ceftiofur |
| url | https://doi.org/10.1186/s42523-023-00274-4 |
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