Drivers and Dynamics of Methicillin-Resistant Livestock-Associated <named-content content-type="genus-species">Staphylococcus aureus</named-content> CC398 in Pigs and Humans in Denmark

ABSTRACT The spread of livestock-associated methicillin-resistant Staphylococcus aureus clonal complex 398 (LA-MRSA CC398) within the Danish pig production system has been linked to an increased number of human infections. Yet, the population structure and transmission dynamics of this important pat...

Descripción completa

Guardado en:
Detalles Bibliográficos
Autores principales: Raphael N. Sieber, Robert L. Skov, Jens Nielsen, Jana Schulz, Lance B. Price, Frank M. Aarestrup, Anders R. Larsen, Marc Stegger, Jesper Larsen
Formato: article
Lenguaje:EN
Publicado: American Society for Microbiology 2018
Materias:
Acceso en línea:https://doaj.org/article/f2f7e58316f74794ae801df0b5b5e134
Etiquetas: Agregar Etiqueta
Sin Etiquetas, Sea el primero en etiquetar este registro!
id oai:doaj.org-article:f2f7e58316f74794ae801df0b5b5e134
record_format dspace
spelling oai:doaj.org-article:f2f7e58316f74794ae801df0b5b5e1342021-11-15T15:52:19ZDrivers and Dynamics of Methicillin-Resistant Livestock-Associated <named-content content-type="genus-species">Staphylococcus aureus</named-content> CC398 in Pigs and Humans in Denmark10.1128/mBio.02142-182150-7511https://doaj.org/article/f2f7e58316f74794ae801df0b5b5e1342018-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02142-18https://doaj.org/toc/2150-7511ABSTRACT The spread of livestock-associated methicillin-resistant Staphylococcus aureus clonal complex 398 (LA-MRSA CC398) within the Danish pig production system has been linked to an increased number of human infections. Yet, the population structure and transmission dynamics of this important pathogen remain poorly understood. In this study, whole-genome sequences from 371 LA-MRSA CC398 isolates collected between 2004 and 2015 were subjected to bioinformatic analyses. The isolates originated from Danish pig farms (n = 209) and people having livestock contact (n = 79). In addition, whole-genome sequence data from 82 isolates representing an international reference collection and 83 isolates from Danish patients were included in the analysis. The results demonstrated that the increasing prevalence of LA-MRSA CC398 in Danish pigs and patients was caused by clonal expansion of three dominant lineages. The results also showed that these lineages were enriched for the tetracycline resistance gene tet(K) and other determinants conferring resistance to some of the most frequently used antimicrobials in Danish pigs. The association between pig movements and the spread of LA-MRSA CC398 was assessed in a Poisson regression analysis of 17,009 pig movements into 273 farms with known LA-MRSA CC398 status. The results demonstrated that animal movements have played a critical role in the dissemination of LA-MRSA CC398 within the Danish pig production system, although other transmission routes may also have contributed. Consistent with this scenario, the genetic relatedness of isolates from different farms was positively correlated with the number of animal movements between the farms. IMPORTANCE Livestock-associated methicillin-resistant Staphylococcus aureus clonal complex CC398 (LA-MRSA CC398) is resistant to nearly all β-lactams and several non-β-lactam antimicrobials. Over the last decade, it has become widespread in pig farms across Europe and is now an important cause of human infections in countries with previously low levels of MRSA, such as the Netherlands and Denmark. The hitherto uncontrolled spread of LA-MRSA CC398 underscores an urgent need to understand its epidemiology in order to develop evidence-based interventions. This study demonstrates that pig movements between farms in combination with increased bacterial resistance to specific antibiotics and heavy metals were important drivers of the rapid spread of LA-MRSA CC398 in the Danish pig production system. These findings should be taken into consideration when researchers and policy makers evaluate and decide on actions and policies to limit the spread of LA-MRSA CC398 and other pathogens in food animals.Raphael N. SieberRobert L. SkovJens NielsenJana SchulzLance B. PriceFrank M. AarestrupAnders R. LarsenMarc SteggerJesper LarsenAmerican Society for MicrobiologyarticleCC398MRSAST398animal movementslivestockmolecular epidemiologyMicrobiologyQR1-502ENmBio, Vol 9, Iss 6 (2018)
institution DOAJ
collection DOAJ
language EN
topic CC398
MRSA
ST398
animal movements
livestock
molecular epidemiology
Microbiology
QR1-502
spellingShingle CC398
MRSA
ST398
animal movements
livestock
molecular epidemiology
Microbiology
QR1-502
Raphael N. Sieber
Robert L. Skov
Jens Nielsen
Jana Schulz
Lance B. Price
Frank M. Aarestrup
Anders R. Larsen
Marc Stegger
Jesper Larsen
Drivers and Dynamics of Methicillin-Resistant Livestock-Associated <named-content content-type="genus-species">Staphylococcus aureus</named-content> CC398 in Pigs and Humans in Denmark
description ABSTRACT The spread of livestock-associated methicillin-resistant Staphylococcus aureus clonal complex 398 (LA-MRSA CC398) within the Danish pig production system has been linked to an increased number of human infections. Yet, the population structure and transmission dynamics of this important pathogen remain poorly understood. In this study, whole-genome sequences from 371 LA-MRSA CC398 isolates collected between 2004 and 2015 were subjected to bioinformatic analyses. The isolates originated from Danish pig farms (n = 209) and people having livestock contact (n = 79). In addition, whole-genome sequence data from 82 isolates representing an international reference collection and 83 isolates from Danish patients were included in the analysis. The results demonstrated that the increasing prevalence of LA-MRSA CC398 in Danish pigs and patients was caused by clonal expansion of three dominant lineages. The results also showed that these lineages were enriched for the tetracycline resistance gene tet(K) and other determinants conferring resistance to some of the most frequently used antimicrobials in Danish pigs. The association between pig movements and the spread of LA-MRSA CC398 was assessed in a Poisson regression analysis of 17,009 pig movements into 273 farms with known LA-MRSA CC398 status. The results demonstrated that animal movements have played a critical role in the dissemination of LA-MRSA CC398 within the Danish pig production system, although other transmission routes may also have contributed. Consistent with this scenario, the genetic relatedness of isolates from different farms was positively correlated with the number of animal movements between the farms. IMPORTANCE Livestock-associated methicillin-resistant Staphylococcus aureus clonal complex CC398 (LA-MRSA CC398) is resistant to nearly all β-lactams and several non-β-lactam antimicrobials. Over the last decade, it has become widespread in pig farms across Europe and is now an important cause of human infections in countries with previously low levels of MRSA, such as the Netherlands and Denmark. The hitherto uncontrolled spread of LA-MRSA CC398 underscores an urgent need to understand its epidemiology in order to develop evidence-based interventions. This study demonstrates that pig movements between farms in combination with increased bacterial resistance to specific antibiotics and heavy metals were important drivers of the rapid spread of LA-MRSA CC398 in the Danish pig production system. These findings should be taken into consideration when researchers and policy makers evaluate and decide on actions and policies to limit the spread of LA-MRSA CC398 and other pathogens in food animals.
format article
author Raphael N. Sieber
Robert L. Skov
Jens Nielsen
Jana Schulz
Lance B. Price
Frank M. Aarestrup
Anders R. Larsen
Marc Stegger
Jesper Larsen
author_facet Raphael N. Sieber
Robert L. Skov
Jens Nielsen
Jana Schulz
Lance B. Price
Frank M. Aarestrup
Anders R. Larsen
Marc Stegger
Jesper Larsen
author_sort Raphael N. Sieber
title Drivers and Dynamics of Methicillin-Resistant Livestock-Associated <named-content content-type="genus-species">Staphylococcus aureus</named-content> CC398 in Pigs and Humans in Denmark
title_short Drivers and Dynamics of Methicillin-Resistant Livestock-Associated <named-content content-type="genus-species">Staphylococcus aureus</named-content> CC398 in Pigs and Humans in Denmark
title_full Drivers and Dynamics of Methicillin-Resistant Livestock-Associated <named-content content-type="genus-species">Staphylococcus aureus</named-content> CC398 in Pigs and Humans in Denmark
title_fullStr Drivers and Dynamics of Methicillin-Resistant Livestock-Associated <named-content content-type="genus-species">Staphylococcus aureus</named-content> CC398 in Pigs and Humans in Denmark
title_full_unstemmed Drivers and Dynamics of Methicillin-Resistant Livestock-Associated <named-content content-type="genus-species">Staphylococcus aureus</named-content> CC398 in Pigs and Humans in Denmark
title_sort drivers and dynamics of methicillin-resistant livestock-associated <named-content content-type="genus-species">staphylococcus aureus</named-content> cc398 in pigs and humans in denmark
publisher American Society for Microbiology
publishDate 2018
url https://doaj.org/article/f2f7e58316f74794ae801df0b5b5e134
work_keys_str_mv AT raphaelnsieber driversanddynamicsofmethicillinresistantlivestockassociatednamedcontentcontenttypegenusspeciesstaphylococcusaureusnamedcontentcc398inpigsandhumansindenmark
AT robertlskov driversanddynamicsofmethicillinresistantlivestockassociatednamedcontentcontenttypegenusspeciesstaphylococcusaureusnamedcontentcc398inpigsandhumansindenmark
AT jensnielsen driversanddynamicsofmethicillinresistantlivestockassociatednamedcontentcontenttypegenusspeciesstaphylococcusaureusnamedcontentcc398inpigsandhumansindenmark
AT janaschulz driversanddynamicsofmethicillinresistantlivestockassociatednamedcontentcontenttypegenusspeciesstaphylococcusaureusnamedcontentcc398inpigsandhumansindenmark
AT lancebprice driversanddynamicsofmethicillinresistantlivestockassociatednamedcontentcontenttypegenusspeciesstaphylococcusaureusnamedcontentcc398inpigsandhumansindenmark
AT frankmaarestrup driversanddynamicsofmethicillinresistantlivestockassociatednamedcontentcontenttypegenusspeciesstaphylococcusaureusnamedcontentcc398inpigsandhumansindenmark
AT andersrlarsen driversanddynamicsofmethicillinresistantlivestockassociatednamedcontentcontenttypegenusspeciesstaphylococcusaureusnamedcontentcc398inpigsandhumansindenmark
AT marcstegger driversanddynamicsofmethicillinresistantlivestockassociatednamedcontentcontenttypegenusspeciesstaphylococcusaureusnamedcontentcc398inpigsandhumansindenmark
AT jesperlarsen driversanddynamicsofmethicillinresistantlivestockassociatednamedcontentcontenttypegenusspeciesstaphylococcusaureusnamedcontentcc398inpigsandhumansindenmark
_version_ 1718427314065244160