Pilot study on nasal microbiota dynamics and MRSA carriage of a pig cohort housed on straw bedding.
CC398
LA-MRSA
microbial ecology
pig husbandry
porcine nasal microbiome
Journal
Molecular microbiology
ISSN: 1365-2958
Titre abrégé: Mol Microbiol
Pays: England
ID NLM: 8712028
Informations de publication
Date de publication:
31 Jul 2023
31 Jul 2023
Historique:
revised:
17
07
2023
received:
07
02
2023
accepted:
21
07
2023
medline:
1
8
2023
pubmed:
1
8
2023
entrez:
1
8
2023
Statut:
aheadofprint
Résumé
Methicillin-resistant Staphylococcus aureus (MRSA) can be transmitted between pigs and humans on farms. Hence, the reduction of MRSA carriage in pigs could decrease the risk of zoonotic transmission. Recently, straw bedding has been found to significantly reduce MRSA carriage in pigs. The mechanisms behind this effect remain unclear but changes in the nasal microbiome may play a role. In this exploratory study, the nasal microbiota of pigs kept on straw was examined using V1/V2 16S rRNA gene sequencing. Nasal swabs were collected from 13 pigs at six different time points during the course of a full fattening cycle resulting in 74 porcine samples. In addition, straw samples were collected at each time point. Eleven out of 13 pigs were MRSA positive at housing-in. We found a strong temporal pattern in the microbial communities. Both microbial diversity and abundance of Staphylococcus species peaked in week 5 after introduction to the straw stable decreased in week 10, when all pigs turned MRSA-negative, and increased again toward the end of the fattening period. These findings show that the introduction of pigs into a new environment has a huge impact on their nasal microbiota, which might lead to unfavorable conditions for MRSA. Moreover, other Staphylococcus species may play a role in eliminating MRSA carriage. We designed a follow-up study including two different husbandry systems to further assess these effects.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Bundesministerium für Bildung und Forschung
ID : 01KI2009A
Organisme : Bundesministerium für Bildung und Forschung
ID : 01KI2009B
Informations de copyright
© 2023 The Authors. Molecular Microbiology published by John Wiley & Sons Ltd.
Références
Bray, J.R. & Curtis, J.T. (1957) An ordination of the upland forest communities of southern Wisconsin. Ecological Monographs, 27, 325-349. Available from: https://doi.org/10.2307/1942268
Bugenyi, A.W., Cho, H.S. & Heo, J. (2020) Association between oropharyngeal microbiome and weight gain in piglets during pre and post weaning life. Journal of Animal Science and Technology, 62, 247-262. Available from: http://www.ejast.org/archive/view_article?pid=jast-62-2-247 [Accessed 16th November 2021]
Callahan, B.J., McMurdie, P.J., Rosen, M.J., Han, A.W., Johnson, A.J.A. & Holmes, S.P. (2016) DADA2: high-resolution sample inference from Illumina amplicon data. Nature Methods, 13, 581-583. Available from: https://www.nature.com/articles/nmeth.3869 [Accessed 21st November 2022]
Caporaso, J.G., Lauber, C.L., Walters, W.A., Berg-Lyons, D., Huntley, J., Fierer, N. et al. (2012) Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. The ISME Journal, 6, 1621-1624.
Cuny, C., Friedrich, A.W. & Witte, W. (2012) Absence of livestock-associated methicillin-resistant Staphylococcus aureus clonal complex CC398 as a nasal colonizer of pigs raised in an alternative system. Applied and Environmental Microbiology, 78, 1296-1297. Available from: https://doi.org/10.1128/AEM.07260-11
Davis, N.M., Proctor, D.M., Holmes, S.P., Relman, D.A. & Callahan, B.J. (2018) Simple statistical identification and removal of contaminant sequences in marker-gene and metagenomics data. Microbiome, 6, 226. Available from: https://doi.org/10.1186/s40168-018-0605-2
Elstrøm, P., Grøntvedt, C.A., Gabrielsen, C., Stegger, M., Angen, Ø., Åmdal, S. et al. (2019) Livestock-associated MRSA CC1 in Norway; introduction to pig farms, zoonotic transmission, and eradication. Frontiers in Microbiology, 10, 139. Available from: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6376739/ [Accessed 4th July 2022]
Goerge, T., Lorenz, M.B., van Alen, S., Hubner, N.-O., Becker, K. & Kock, R. (2017) MRSA colonization and infection among persons with occupational livestock exposure in Europe: prevalence, preventive options and evidence. Veterinary Microbiology, 200, 6-12.
Kobusch, I., Schröter, I., Linnemann, S., Schollenbruch, H., Hofmann, F. & Boelhauve, M. (2022) Prevalence of LA-MRSA in pigsties: analysis of factors influencing the (de)colonization process. Scientific Reports, 12, 18000. Available from: https://www.nature.com/articles/s41598-022-21903-z [Accessed 27th October 2022]
Köck, R., Brakensiek, L., Mellmann, A., Kipp, F., Henderikx, M., Harmsen, D. et al. (2009) Cross-border comparison of the admission prevalence and clonal structure of meticillin-resistant Staphylococcus aureus. Journal of Hospital Infection, 71, 320-326. Available from: https://www.sciencedirect.com/science/article/pii/S0195670108004982 [Accessed 19th June 2019]
Köck, R., Loth, B., Köksal, M., Schulte-Wülwer, J., Harlizius, J. & Friedrich, A.W. (2012) Persistence of nasal colonization with livestock-associated methicillin-resistant Staphylococcus aureus in pig farmers after holidays from pig exposure. Applied and Environmental Microbiology, 78, 4046-4047. Available from: http://www.ncbi.nlm.nih.gov/pubmed/22447613 [Accessed 19th June 2019]
Lahti, L., and Shetty, S. (2012) Microbiome R package. Available from: http://microbiome.github.io [Accessed 21st November 2022].
Lozano, C., Aspiroz, C., Lasarte, J.J., Gómez-Sanz, E., Zarazaga, M. & Torres, C. (2011) Dynamic of nasal colonization by methicillin-resistant Staphylococcus aureus ST398 and ST1 after mupirocin treatment in a family in close contact with pigs. Comparative Immunology, Microbiology and Infectious Diseases, 34, e1-e7. Available from: https://www.sciencedirect.com/science/article/pii/S0147957110000494 [Accessed 17th November 2022]
McMurdie, P.J. & Holmes, S. (2013) Phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One, 8, e61217. Available from: https://journals.plos.org/plosone/article?id=10.1371/journal.pone.0061217 [Accessed 21st November 2022]
Megahed, A., Zeineldin, M., Evans, K., Maradiaga, N., Blair, B., Aldridge, B. et al. (2019) Impacts of environmental complexity on respiratory and gut microbiome community structure and diversity in growing pigs. Scientific Reports, 9, 1-12. Available from: https://www.nature.com/articles/s41598-019-50187-z [Accessed 16th November 2021]
Oksanen, J., Simpson, G.L., Blanchet, F.G., Kindt, R., Legendre, P., Minchin, P.R. et al. (2022) Vegan: community ecology package. Available from: https://CRAN.R-project.org/package=vegan [Accessed 21st November 2022]
Pena Cortes, L.C., Leveque, R.M., Funk, J., Marsh, T.L. & Mulks, M.H. (2018) Development of the tonsillar microbiome in pigs from newborn through weaning. BMC Microbiology, 18, 1-13. Available from: https://doi.org/10.1186/s12866-018-1176-x
Pirolo, M., Espinosa-Gongora, C., Bogaert, D. & Guardabassi, L. (2021) The porcine respiratory microbiome: recent insights and future challenges. Animal Microbiome, 3, 1-13. Available from: https://doi.org/10.1186/s42523-020-00070-4
Pletinckx, L.J., Dewulf, J., De Bleecker, Y., Rasschaert, G., Goddeeris, B.M. & De Man, I. (2013) Effect of a disinfection strategy on the methicillin-resistant Staphylococcus aureus CC398 prevalence of sows, their piglets and the barn environment. Journal of Applied Microbiology, 114, 1634-1641. Available from: https://doi.org/10.1111/jam.12201
R Core Team. (2022) R: A language and environment for statistical computing. Available from: https://www.R-project.org/ [Accessed 24th November 2022].
Schloss, P.D. (2023) The riffomonas youtube channel: an educational resource to foster reproducible research practices. Microbiology Resource Announcements, 12, e0131022. Available from: https://doi.org/10.1128/mra.01310-22
Schoenfelder, S.M.K., Dong, Y., Feßler, A.T., Schwarz, S., Schoen, C., Köck, R. et al. (2017) Antibiotic resistance profiles of coagulase-negative staphylococci in livestock environments. Veterinary Microbiology, 200, 79-87. Available from: https://linkinghub.elsevier.com/retrieve/pii/S037811351630102X [Accessed 12th December 2022]
Schollenbruch, H., Kobusch, I., Schröter, I., Mellmann, A., Köck, R. & Boelhauve, M. (2021) Pilot study on alteration of LA-MRSA status of pigs during fattening period on straw bedding by two types of cleaning. Antibiotics, 10, 521. Available from: https://www.mdpi.com/2079-6382/10/5/521 [Accessed 21st July 2021]
Shannon, C.E. (1948) A mathematical theory of communication. Bell System Technical Journal, 27, 379-423. Available from: https://ieeexplore.ieee.org/document/6773024 [Accessed 24th November 2022]
Slifierz, M.J., Friendship, R.M. & Weese, J.S. (2015) Longitudinal study of the early-life fecal and nasal microbiotas of the domestic pig. BMC Microbiology, 15, 1-12. Available from: https://doi.org/10.1186/s12866-015-0512-7
Smith, T.C. & Wardyn, S.E. (2015) Human infections with Staphylococcus aureus CC398. Current Environmental Health Reports, 2, 41-51. Available from: https://doi.org/10.1007/s40572-014-0034-8
Strube, M.L., Hansen, J.E., Rasmussen, S. & Pedersen, K. (2018) A detailed investigation of the porcine skin and nose microbiome using universal and Staphylococcus specific primers. Scientific Reports, 8, 1-9. Available from: https://www.nature.com/articles/s41598-018-30689-y [Accessed 16th November 2021]
van de Vijver, L.P.L., Tulinski, P., Bondt, N., Mevius, D. & Verwer, C. (2014) Prevalence and molecular characteristics of methicillin-resistant Staphylococcus aureus (MRSA) in organic pig herds in The Netherlands. Zoonoses and Public Health, 61, 338-345. Available from: https://doi.org/10.1111/zph.12076
Weese, J.S., Slifierz, M., Jalali, M. & Friendship, R. (2014) Evaluation of the nasal microbiota in slaughter-age pigs and the impact on nasal methicillin-resistant Staphylococcus aureus (MRSA) carriage. BMC Veterinary Research, 10, 1-10. Available from: https://doi.org/10.1186/1746-6148-10-69