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A livestock-associated, multidrug-resistant, methicillin-resistant Staphylococcus aureus clonal complex 97 lineage spreading in dairy cattle and pigs in Italy

Fabiola Feltrin, Patricia Alba, Britta Kraushaar, Angela Ianzano, María Angeles Argudín, Paola Di Matteo, María Concepcíon Porrero, Frank M Aarestrup, Patrick Butaye UGent, Alessia Franco, et al. (2016) APPLIED AND ENVIRONMENTAL MICROBIOLOGY. 82(3). p.816-821
abstract
Pandemic methicillin-resistant Staphylococcus aureus (MRSA) clonal complex 97 (CC97) lineages originated from livestock-to-human host jumps. In recent years, CC97 has become one of the major MRSA lineages detected in Italian farmed animals. The aim of this study was to characterize and analyze differences in MRSA and methicillin-susceptible S. aureus (MSSA) mainly of swine and bovine origins. Forty-seven CC97 isolates, 35 MRSA isolates, and 6 MSSA isolates from different Italian pig and cattle holdings; 5 pig MRSA isolates from Germany; and 1 human MSSA isolate from Spain were characterized by macrorestriction pulsed-field gel electrophoresis (PFGE) analysis, multilocus sequence typing (MLST), spa typing, staphylococcal cassette chromosome mec (SCCmec) typing, and antimicrobial resistance pattern analysis. Virulence and resistance genes were investigated by PCR and microarray analysis. Most of the isolates were of SCCmec type V (SCCmec V), except for two German MRSA isolates (SCCmec III). Five main clusters were identified by PFGE, with the German isolates (clusters I and II) showing 60.5% similarity with the Italian isolates, most of which (68.1%) grouped into cluster V. All CC97 isolates were Panton-Valentine leukocidin (PVL) negative, and a few (n = 7) tested positive for sak or scn. All MRSA isolates were multidrug resistant (MDR), and the main features were erm(B)-or erm(C)-mediated (n = 18) macrolide-lincosamide-streptogramin B resistance, vga(A)-mediated (n = 37) pleuromutilin resistance, fluoroquinolone resistance (n = 33), tet(K) in 32/37 tet(M)-positive isolates, and blaZ in almost all MRSA isolates. Few host-associated differences were detected among CC97 MRSA isolates: their extensive MDR nature in both pigs and dairy cattle may be a consequence of a spillback from pigs of a MRSA lineage that originated in cattle as MSSA and needs further investigation. Measures should be implemented at the farm level to prevent spillover to humans in intensive farming areas.
Please use this url to cite or link to this publication:
author
organization
year
type
journalArticle (original)
publication status
published
subject
keyword
PROTEIN, ANIMALS, MULTIPLEX PCR ASSAY, FIELD GEL-ELECTROPHORESIS, STRAINS, GENES, MECA, BAP
journal title
APPLIED AND ENVIRONMENTAL MICROBIOLOGY
Appl. Environ. Microbiol.
volume
82
issue
3
pages
816 - 821
Web of Science type
Article
Web of Science id
000369373800006
JCR category
BIOTECHNOLOGY & APPLIED MICROBIOLOGY
JCR impact factor
3.807 (2016)
JCR rank
31/158 (2016)
JCR quartile
1 (2016)
ISSN
0099-2240
DOI
10.1128/AEM.02854-15
language
English
UGent publication?
yes
classification
A1
copyright statement
I have transferred the copyright for this publication to the publisher
id
7139244
handle
http://hdl.handle.net/1854/LU-7139244
date created
2016-03-08 16:16:50
date last changed
2016-12-19 15:42:38
@article{7139244,
  abstract     = {Pandemic methicillin-resistant Staphylococcus aureus (MRSA) clonal complex 97 (CC97) lineages originated from livestock-to-human host jumps. In recent years, CC97 has become one of the major MRSA lineages detected in Italian farmed animals. The aim of this study was to characterize and analyze differences in MRSA and methicillin-susceptible S. aureus (MSSA) mainly of swine and bovine origins. Forty-seven CC97 isolates, 35 MRSA isolates, and 6 MSSA isolates from different Italian pig and cattle holdings; 5 pig MRSA isolates from Germany; and 1 human MSSA isolate from Spain were characterized by macrorestriction pulsed-field gel electrophoresis (PFGE) analysis, multilocus sequence typing (MLST), spa typing, staphylococcal cassette chromosome mec (SCCmec) typing, and antimicrobial resistance pattern analysis. Virulence and resistance genes were investigated by PCR and microarray analysis. Most of the isolates were of SCCmec type V (SCCmec V), except for two German MRSA isolates (SCCmec III). Five main clusters were identified by PFGE, with the German isolates (clusters I and II) showing 60.5\% similarity with the Italian isolates, most of which (68.1\%) grouped into cluster V. All CC97 isolates were Panton-Valentine leukocidin (PVL) negative, and a few (n = 7) tested positive for sak or scn. All MRSA isolates were multidrug resistant (MDR), and the main features were erm(B)-or erm(C)-mediated (n = 18) macrolide-lincosamide-streptogramin B resistance, vga(A)-mediated (n = 37) pleuromutilin resistance, fluoroquinolone resistance (n = 33), tet(K) in 32/37 tet(M)-positive isolates, and blaZ in almost all MRSA isolates. Few host-associated differences were detected among CC97 MRSA isolates: their extensive MDR nature in both pigs and dairy cattle may be a consequence of a spillback from pigs of a MRSA lineage that originated in cattle as MSSA and needs further investigation. Measures should be implemented at the farm level to prevent spillover to humans in intensive farming areas.},
  author       = {Feltrin, Fabiola and Alba, Patricia and Kraushaar, Britta and Ianzano, Angela and Argud{\'i}n, Mar{\'i}a Angeles and Di Matteo, Paola and Porrero, Mar{\'i}a Concepc{\'i}on and Aarestrup, Frank M and Butaye, Patrick and Franco, Alessia and Battisti, Antonio},
  issn         = {0099-2240},
  journal      = {APPLIED AND ENVIRONMENTAL MICROBIOLOGY},
  keyword      = {PROTEIN,ANIMALS,MULTIPLEX PCR ASSAY,FIELD GEL-ELECTROPHORESIS,STRAINS,GENES,MECA,BAP},
  language     = {eng},
  number       = {3},
  pages        = {816--821},
  title        = {A livestock-associated, multidrug-resistant, methicillin-resistant Staphylococcus aureus clonal complex 97 lineage spreading in dairy cattle and pigs in Italy},
  url          = {http://dx.doi.org/10.1128/AEM.02854-15},
  volume       = {82},
  year         = {2016},
}

Chicago
Feltrin, Fabiola, Patricia Alba, Britta Kraushaar, Angela Ianzano, María Angeles Argudín, Paola Di Matteo, María Concepcíon Porrero, et al. 2016. “A Livestock-associated, Multidrug-resistant, Methicillin-resistant Staphylococcus Aureus Clonal Complex 97 Lineage Spreading in Dairy Cattle and Pigs in Italy.” Applied and Environmental Microbiology 82 (3): 816–821.
APA
Feltrin, F., Alba, P., Kraushaar, B., Ianzano, A., Argudín, M. A., Di Matteo, P., Porrero, M. C., et al. (2016). A livestock-associated, multidrug-resistant, methicillin-resistant Staphylococcus aureus clonal complex 97 lineage spreading in dairy cattle and pigs in Italy. APPLIED AND ENVIRONMENTAL MICROBIOLOGY, 82(3), 816–821.
Vancouver
1.
Feltrin F, Alba P, Kraushaar B, Ianzano A, Argudín MA, Di Matteo P, et al. A livestock-associated, multidrug-resistant, methicillin-resistant Staphylococcus aureus clonal complex 97 lineage spreading in dairy cattle and pigs in Italy. APPLIED AND ENVIRONMENTAL MICROBIOLOGY. 2016;82(3):816–21.
MLA
Feltrin, Fabiola, Patricia Alba, Britta Kraushaar, et al. “A Livestock-associated, Multidrug-resistant, Methicillin-resistant Staphylococcus Aureus Clonal Complex 97 Lineage Spreading in Dairy Cattle and Pigs in Italy.” APPLIED AND ENVIRONMENTAL MICROBIOLOGY 82.3 (2016): 816–821. Print.