An overview of carbapenem-resistant organisms from food-producing animals, seafood, aquaculture, companion animals, and wildlife

Abstract

Carbapenem resistance (CR) is a major global health concern. CR is a growing challenge in clinical settings due to its rapid dissemination and low treatment options. The characterization of its molecular mechanisms and epidemiology are highly studied. Nevertheless, little is known about the spread of CR in food-producing animals, seafood, aquaculture, wildlife, their environment, or the health risks associated with CR in humans. In this review, we discuss the detection of carbapenem-resistant organisms and their mechanisms of action in pigs, cattle, poultry, seafood products, companion animals, and wildlife. We also pointed out the One Health approach as a strategy to attempt the emergency and dispersion of carbapenem-resistance in this sector and to determine the role of carbapenem-producing bacteria in animals among human public health risk. A higher occurrence of carbapenem enzymes in poultry and swine has been previously reported. Studies related to poultry have highlighted P. mirabilis, E. coli, and K. pneumoniae as NDM-5- and NDM-1-producing bacteria, which lead to carbapenem resistance. OXA-181, IMP-27, and VIM-1 have also been detected in pigs. Carbapenem resistance is rare in cattle. However, OXA- and NDM-producing bacteria, mainly E. coli and A. baumannii, are cattle's leading causes of carbapenem resistance. A high prevalence of carbapenem enzymes has been reported in wildlife and companion animals, suggesting their role in the cross-species transmission of carbapenem-resistant genes. Antibiotic-resistant organisms in aquatic environments should be considered because they may act as reservoirs for carbapenem-resistant genes. It is urgent to implement the One Health approach worldwide to make an effort to contain the dissemination of carbapenem resistance.

The European Union summary report on antimicrobial resistance in zoonotic and indicator bacteria from humans, animals and food in 2021–2022

“…The increasing occurrence of E. coli with bla NDM‐5 in Europe suggests that there is an ongoing global expansion of certain E. coli STs carrying this gene, and that this is now a significant concern in EU/EEA countries (ECDC, 2023a ). Based on nucleotide similarity between plasmids carrying CP‐encoding genes in human and food‐producing animal sources, it has been suggested that specific plasmids have been circulating among E. coli in different species, possibly increasing the risk of zoonotic transmission of carbapenem resistance (Ramírez‐Castillo et al., 2023 ). However, further studies including epidemiological and genetic analyses are required to elucidate the transmission dynamics.…”

“…CP‐producing Enterobacterales have not only been reported among isolates collected in the harmonised EU monitoring (Bortolaia et al., 2021 ; Carfora et al., 2022 ; Diaconu et al., 2020 ; EFSA and ECDC, 2023 ; Garcia‐Graells et al., 2020 ), but also from companion animals (Ramírez‐Castillo et al., 2023 ; Rincon‐Real & Suárez‐Alfonso, 2022 ), food‐producing animals and derived meat, seafood and vegetables (Brouwer et al., 2018 ; Irrgang et al., 2019 ; Irrgang et al., 2020 ; Köck et al., 2018 ; Liu et al., 2018 ; Ramírez‐Castillo et al., 2023 ; Slettemeås et al., 2017 ; Touati et al., 2017 ; Zurfluh et al., 2015 ). Carbapenems are not authorised for use in animals in the EU, and spill‐over from CP‐encoding genes and/or bacteria from humans has been suggested as a potential source of CP‐producers in the food production (Irrgang et al., 2020 ; Madec et al., 2017 ).…”

“…The class D carbapenemase bla OXA-181 has mainly been associated with humans, and its first isolation from porcine E. coli was reported from Italy (Pulss et al, 2017). Further, the New Delhi metallo-beta-lactamase bla NDM-5 has previously been isolated from dairy cows in Algeria, as well as dogs and humans, from pigs and poultry in China, and cattle in India (Ramírez-Castillo et al, 2023). A structured survey of carbapenemase-and/or colistin-resistant Enterobacterales conducted in 36 European countries in 2019 showed that bla NDM-5 was the most frequently reported carbapenemaseencoding gene in E. coli in humans in Europe (ECDC, 2018(ECDC, , 2023a(ECDC, , 2023b.…”

Antibiotic Susceptibility Profiles of Bacterial Isolates Recovered from Abscesses in Cattle and Sheep at a Slaughterhouse in Algeria

“…The presence of ESBLs, and in particular CTX-M-15, in animals has previously been linked to the human sector before it was also detected in animals and the environment [ 30 ]. Additionally, ceftiofur, a third-generation cephalosporin, is the main cephalosporin used in veterinary medicine due to its effectiveness in treating bacterial infections in food-producing animals; for this reason, these antibiotics could provide selection pressure that favors co-selection of plasmids carrying mobile genes (transposon, integron, cassette gene) that result in carbapenem-resistant (CR) strains [ 31 , 32 ]. Here, we identified a CTX-M-15 producing E. coli ST1706, an ST that has previously been described in Japan from different pig farms [ 33 ].…”

“…However, the clinical use of these antibiotics is presently at risk due to the global proliferation of β-lactamases (BLs) with the ability to degrade them, and the increase in the worldwide emergence of carbapenem-resistant organisms (CROs), which constitute a critical growing public health threat [ 34 ]. In livestock or veterinary fields, carbapenems are not licensed and have no legal indication, so their use is prohibited [ 32 , 35 , 36 ]. Nevertheless, many studies conducted in Algeria have reported CROs in livestock, companion animals, and birds [ 37 , 38 , 39 ].…”