Evidence for the Dissemination to Humans of Methicillin-Resistant Staphylococcus aureus ST398 through the Pork Production Chain: A Study in a Portuguese Slaughterhouse

Abstract

Livestock-associated methicillin-resistant Staphylococcus aureus (LA-MRSA) ST398 was recovered from infections in humans exposed to animals, raising public health concerns. However, contact with food producing chain as a means of transmission of LA-MRSA to humans remains poorly understood. We aimed to assess if pork production chain is a source of MRSA ST398 for human colonization and infection. MRSA from live pigs, meat, the environment, and slaughterhouse workers were analyzed by Pulsed-Field Gel Electrophoresis (PFGE), spa, MLST typing, SNPs and for antibiotic resistance and virulence gene profiles. We compared core and accessory genomes of MRSA ST398 isolated from slaughterhouse and hospital. We detected MRSA ST398 (t011, t108, t1451) along the entire pork production chain (live pigs: 60%; equipment: 38%; meat: 23%) and in workers (40%). All MRSA ST398 were multidrug resistant, and the majority carried genes encoding biocide resistance and enterotoxins. We found 23 cross-transmission events between live pigs, meat, and workers (6–55 SNPs). MRSA ST398 from infection and slaughterhouse environment belonged to the same clonal type (ST398, t011, SCCmec V), but differed in 321–378 SNPs. Pork production chain can be a source of MRSA ST398 for colonization of human slaughterhouse workers, which can represent a risk of subsequent meat contamination and human infection.

Livestock-associated methicillin-resistant Staphylococcus aureus in slaughtered pigs in England

“…A predominant spa -type was detected in each abattoir (apart from abattoir B); the predominant spa -type was generally either t011 or t034, types which are both relatively frequently detected in herd level studies of pigs in Europe [ 10 ]. The detection of MRSA in batches of pigs may represent contamination from between batches, from other sources within the abattoir, during transport to the abattoir, or persistence of MRSA in the abattoir after initial introduction, rather than accurately reflecting the status of the farm of origin [ 11 , 12 , 15 , 36 ]. In abattoir E, which was sampled over 2 days, t011 was present on both days possibly suggesting that batches may have been contaminated at the abattoir, which was acting as a reservoir, although t011 tends to be a frequently detected spa -type of MRSA CC398 in pigs in Europe and repeated introduction is equally possible.…”

“…Numerous European and North American surveillance and research studies have described the occurrence of MRSA at slaughter [9,10], from pigs on arrival [11,12], after stunning [13,14,15], and on carcasses during chilling [16,17]. The majority of the studies .…”

“…Numerous European and North American surveillance and research studies have described the occurrence of MRSA at slaughter [9,10], from pigs on arrival [11,12], after stunning [13][14][15] and on carcases during chilling [16,17]. The majority of the studies performed in European countries reported data on the occurrence of MRSA from nasal swabs along the slaughter process, where the prevalence ranged from 0% in Ireland to 49-71% in Germany and 99.5% in Netherlands [14,18,19].…”

Ecology and Genetic Lineages of Nasal Staphylococcus aureus and MRSA Carriage in Healthy Persons with or without Animal-Related Occupational Risks of Colonization: A Review of Global Reports

“…Aside from HA- and CA-MRSA infections, the emergence of livestock-associated (LA)-MRSA, especially of the lineage MRSA-CC398, has also caused alarming rates of staphylococcal colonization and infection among humans in contact with livestock, mostly with pigs, suggesting an increased risk of zoonotic transmission [ 14 ]. This MRSA-CC398 lineage could, subsequently, be dispersed to the environment and to other species of animals through the food chain and direct contact [ 15 ]. In this sense, a recent study performed in Spain demonstrated a significant association between the rate of MRSA-CC398 at hospital level and the density of pig farming in the surrounding regions [ 16 ].…”

Occurrence of methicillin-resistant staphylococci in the pig-production chain in Ibadan, Nigeria

“…Methicillin-resistant staphylococci (MRS) emerged in a variety of livestock animals, apparently through different mechanisms (De Boer et al 2009 ). The close proximity amongst humans, livestock and antimicrobial use in animals presumably facilitates the emergence and spread of MRS (Bouchami et al 2020 ). Methicillin-resistant staphylococci have been recovered from various retail products (Bouchami et al 2020 ; De Boer et al 2009 ) leading to an interest in MRS colonisation and infection in animals.…”