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Ceftiofur treatment of sows results in long-term alterations in the nasal microbiota of the offspring that can be ameliorated by inoculation of nasal colonizers

BACKGROUND: The nasal microbiota of the piglet is a reservoir for opportunistic pathogens that can cause polyserositis, such as Glaesserella parasuis, Mycoplasma hyorhinis or Streptococcus suis. Antibiotic treatment is a strategy to control these diseases, but it has a detrimental effect on the micr...

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Autores principales: Blanco-Fuertes, Miguel, Sibila, Marina, Franzo, Giovanni, Obregon-Gutierrez, Pau, Illas, Francesc, Correa-Fiz, Florencia, Aragón, Virginia
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10588210/
https://www.ncbi.nlm.nih.gov/pubmed/37864263
http://dx.doi.org/10.1186/s42523-023-00275-3
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author Blanco-Fuertes, Miguel
Sibila, Marina
Franzo, Giovanni
Obregon-Gutierrez, Pau
Illas, Francesc
Correa-Fiz, Florencia
Aragón, Virginia
author_facet Blanco-Fuertes, Miguel
Sibila, Marina
Franzo, Giovanni
Obregon-Gutierrez, Pau
Illas, Francesc
Correa-Fiz, Florencia
Aragón, Virginia
author_sort Blanco-Fuertes, Miguel
collection PubMed
description BACKGROUND: The nasal microbiota of the piglet is a reservoir for opportunistic pathogens that can cause polyserositis, such as Glaesserella parasuis, Mycoplasma hyorhinis or Streptococcus suis. Antibiotic treatment is a strategy to control these diseases, but it has a detrimental effect on the microbiota. We followed the piglets of 60 sows from birth to 8 weeks of age, to study the effect of ceftiofur on the nasal microbiota and the colonization by pathogens when the treatment was administered to sows or their litters. We also aimed to revert the effect of the antibiotic on the nasal microbiota by the inoculation at birth of nasal colonizers selected from healthy piglets. Nasal swabs were collected at birth, and at 7, 15, 21 and 49 days of age, and were used for pathogen detection by PCR and bacterial culture, 16S rRNA amplicon sequencing and whole shotgun metagenomics. Weights, clinical signs and production parameters were also recorded during the study. RESULTS: The composition of the nasal microbiota of piglets changed over time, with a clear increment of Clostridiales at the end of nursery. The administration of ceftiofur induced an unexpected temporary increase in alpha diversity at day 7 mainly due to colonization by environmental taxa. Ceftiofur had a longer impact on the nasal microbiota of piglets when administered to their sows before farrowing than directly to them. This effect was partially reverted by the inoculation of nasal colonizers to newborn piglets and was accompanied by a reduction in the number of animals showing clinical signs (mainly lameness). Both interventions altered the colonization pattern of different strains of the above pathogens. In addition, the prevalence of resistance genes increased over time in all the groups but was significantly higher at weaning when the antibiotic was administered to the sows. Also, ceftiofur treatment induced the selection of more beta-lactams resistance genes when it was administered directly to the piglets. CONCLUSIONS: This study shed light on the effect of the ceftiofur treatment on the piglet nasal microbiota over time and demonstrated for the first time the possibility of modifying the piglets’ nasal microbiota by inoculating natural colonizers of the upper respiratory tract. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s42523-023-00275-3.
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spelling pubmed-105882102023-10-21 Ceftiofur treatment of sows results in long-term alterations in the nasal microbiota of the offspring that can be ameliorated by inoculation of nasal colonizers Blanco-Fuertes, Miguel Sibila, Marina Franzo, Giovanni Obregon-Gutierrez, Pau Illas, Francesc Correa-Fiz, Florencia Aragón, Virginia Anim Microbiome Research BACKGROUND: The nasal microbiota of the piglet is a reservoir for opportunistic pathogens that can cause polyserositis, such as Glaesserella parasuis, Mycoplasma hyorhinis or Streptococcus suis. Antibiotic treatment is a strategy to control these diseases, but it has a detrimental effect on the microbiota. We followed the piglets of 60 sows from birth to 8 weeks of age, to study the effect of ceftiofur on the nasal microbiota and the colonization by pathogens when the treatment was administered to sows or their litters. We also aimed to revert the effect of the antibiotic on the nasal microbiota by the inoculation at birth of nasal colonizers selected from healthy piglets. Nasal swabs were collected at birth, and at 7, 15, 21 and 49 days of age, and were used for pathogen detection by PCR and bacterial culture, 16S rRNA amplicon sequencing and whole shotgun metagenomics. Weights, clinical signs and production parameters were also recorded during the study. RESULTS: The composition of the nasal microbiota of piglets changed over time, with a clear increment of Clostridiales at the end of nursery. The administration of ceftiofur induced an unexpected temporary increase in alpha diversity at day 7 mainly due to colonization by environmental taxa. Ceftiofur had a longer impact on the nasal microbiota of piglets when administered to their sows before farrowing than directly to them. This effect was partially reverted by the inoculation of nasal colonizers to newborn piglets and was accompanied by a reduction in the number of animals showing clinical signs (mainly lameness). Both interventions altered the colonization pattern of different strains of the above pathogens. In addition, the prevalence of resistance genes increased over time in all the groups but was significantly higher at weaning when the antibiotic was administered to the sows. Also, ceftiofur treatment induced the selection of more beta-lactams resistance genes when it was administered directly to the piglets. CONCLUSIONS: This study shed light on the effect of the ceftiofur treatment on the piglet nasal microbiota over time and demonstrated for the first time the possibility of modifying the piglets’ nasal microbiota by inoculating natural colonizers of the upper respiratory tract. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s42523-023-00275-3. BioMed Central 2023-10-20 /pmc/articles/PMC10588210/ /pubmed/37864263 http://dx.doi.org/10.1186/s42523-023-00275-3 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research
Blanco-Fuertes, Miguel
Sibila, Marina
Franzo, Giovanni
Obregon-Gutierrez, Pau
Illas, Francesc
Correa-Fiz, Florencia
Aragón, Virginia
Ceftiofur treatment of sows results in long-term alterations in the nasal microbiota of the offspring that can be ameliorated by inoculation of nasal colonizers
title Ceftiofur treatment of sows results in long-term alterations in the nasal microbiota of the offspring that can be ameliorated by inoculation of nasal colonizers
title_full Ceftiofur treatment of sows results in long-term alterations in the nasal microbiota of the offspring that can be ameliorated by inoculation of nasal colonizers
title_fullStr Ceftiofur treatment of sows results in long-term alterations in the nasal microbiota of the offspring that can be ameliorated by inoculation of nasal colonizers
title_full_unstemmed Ceftiofur treatment of sows results in long-term alterations in the nasal microbiota of the offspring that can be ameliorated by inoculation of nasal colonizers
title_short Ceftiofur treatment of sows results in long-term alterations in the nasal microbiota of the offspring that can be ameliorated by inoculation of nasal colonizers
title_sort ceftiofur treatment of sows results in long-term alterations in the nasal microbiota of the offspring that can be ameliorated by inoculation of nasal colonizers
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10588210/
https://www.ncbi.nlm.nih.gov/pubmed/37864263
http://dx.doi.org/10.1186/s42523-023-00275-3
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