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Characterization of Extended-Spectrum -Lactamase-Producing and Ampc antibiotics Article Characterization of Extended-Spectrum β-Lactamase-Producing and AmpC β-Lactamase-Producing Enterobacterales Isolated from Companion Animals in Korea Se Ra Shin 1,2 , Seong Mi Noh 1,2, Woo Kyung Jung 1,*, Sook Shin 1, Young Kyung Park 1, Dong Chan Moon 3 , Suk-Kyung Lim 3, Yong Ho Park 1 and Kun Taek Park 4,* 1 Department of Pathobiology and Preventive Medicine, College of Veterinary Medicine and Research Institute for Veterinary Science, Seoul National University, Seoul 08826, Korea; [email protected] (S.R.S.); [email protected] (S.M.N.); [email protected] (S.S.); [email protected] (Y.K.P.); [email protected] (Y.H.P.) 2 BK21 PLUS Creative Veterinary Research Center, Seoul National University, Seoul 08826, Korea 3 Bacterial Disease Division, Animal and Plant Quarantine Agency, Gimcheon 39660, Korea; [email protected] (D.C.M.); [email protected] (S.-K.L.) 4 Department of Biotechnology, Inje University, Gimhae 50834, Korea * Correspondence: [email protected] (W.K.J.); [email protected] (K.T.P.) Abstract: The emergence of extended-spectrum cephalosporin (ESC)-resistant Gram-negative bac- teria is of great concern in both human and veterinary medicine. The aim of this study was to investigate ESC-resistant bacterial isolates from companion animals in South Korea between 2017 and 2019. Isolates with ESC resistance genes, which were identified by PCR, were assessed for genetic Citation: Shin, S.R.; Noh, S.M.; Jung, relatedness by multi-locus sequence typing (MLST) and pulsed-field gel electrophoresis (PFGE). In W.K.; Shin, S.; Park, Y.K.; Moon, D.C.; total, 91 ESC-resistant Escherichia coli, Klebsiella spp., Serratia spp., and Enterobacter cloacae isolates har- Lim, S.-K.; Park, Y.H.; Park, K.T. bored the blaTEM gene. Among other ESC resistance genes, blaCTX-M-15, blaCIT, and blaCTX-M-55 were Characterization of Extended- predominantly detected in E. coli isolates, whereas bla and bla were more frequently detected Spectrum β-Lactamase-Producing SHV DHA and AmpC β-Lactamase-Producing in Klebsiella pneumoniae isolates. In addition, all blaEBC-positive isolates were classified as E. cloacae. Enterobacterales Isolated from From the MLST results, blaCTX-M-9-carrying ST131, blaCIT-carrying ST405, and blaCTX-M-1-carrying Companion Animals in Korea. ST3285 strains were dominant among E. coli isolates. ST273 and ST275 strains harboring blaSHV were Antibiotics 2021, 10, 249. https:// frequently detected in K. pneumoniae isolates. Various sequence types were obtained in E. cloacae and doi.org/10.3390/antibiotics10030249 Klebsiella oxytoca isolates. All isolates demonstrated unique PFGE profiles (<57–98% similarity) and were unlikely to be derived from a single clone. The present study reveals the presence and wide Academic Editor: Krisztina genetic distribution of ESC-resistant bacterial species in South Korean companion animals. M. Papp-Wallace Keywords: extended-spectrum cephalosporins; extended-spectrum β-lactamases; AmpC β-lactamases; Received: 5 January 2021 antimicrobial resistance; Gram-negative bacteria; companion animal Accepted: 25 February 2021 Published: 3 March 2021 Publisher’s Note: MDPI stays neutral 1. Introduction with regard to jurisdictional claims in published maps and institutional affil- The emergence and prevalence of β-lactam resistance in Gram-negative bacteria has iations. increased consistently over the past few decades [1,2]. Resistance to β-lactams is mostly caused by bacterially produced β-lactamases that hydrolyze and inactivate extended- spectrum cephalosporins (ESCs), such as third and fourth generation cephalosporins [1]. ESC resistance is mainly caused by the expression of extended-spectrum β-lactamase (ESBL) and AmpC β-lactamase (AmpC) genes that are normally encoded on mobile genetic Copyright: © 2021 by the authors. Licensee MDPI, Basel, Switzerland. elements, mostly plasmids [1]. β This article is an open access article The first ESBLs have evolved from the native -lactamases TEM and SHV via genetic distributed under the terms and mutations [3]. CTX-M β-lactamases, a new group of plasmid-mediated ESBLs, were first conditions of the Creative Commons reported in Japan in 1986 [4]. However, since 2000, CTX-M β-lactamases have increasingly Attribution (CC BY) license (https:// been reported in both human and animal populations and are now the dominant type creativecommons.org/licenses/by/ of ESBL, replacing classical TEM- and SHV-type ESBLs in most areas of the world [5]. 4.0/). Currently, there are >120 different CTX-M β-lactamases that are clustered into five groups Antibiotics 2021, 10, 249. https://doi.org/10.3390/antibiotics10030249 https://www.mdpi.com/journal/antibiotics Antibiotics 2021, 10, 249 2 of 11 (CTX-M-1, 2, 8, 9, and 25) [6]. Among CTX-M-type enzymes, the presence of CTX-M-15 and CTX-M-14 has increasingly been reported in most areas of the world, including South Korea [5,7]. Since the detection of CMY-1, the first reported AmpC type β-lactamases, in 1989 [6], various types of AmpCs have been identified in clinical isolates of Enterobacterales around the world [8]. Among AmpCs, CIT- and DHA-type enzymes are the most prevalent [2]. Especially, DHA-producing Klebsiella spp. isolates and CIT-producing Escherichia coli isolates have been repeatedly reported for Enterobacterales in South Korea [2,9]. Despite many studies on ESBL- and AmpC-producing bacteria from human or livestock isolates, studies concerning antimicrobial resistance (AMR) bacteria associated with companion animals are lacking, especially with respect to Serratia spp. and Enterobacter spp. [10–12]. The popularity of companion animals in South Korea has been growing, which pro- vides a potential reservoir of AMR bacteria, as pets are closely associated with humans, living in their homes and near their food [9]. Thus, the importance of profiling AMR bacte- ria was emphasized in the “One Health” initiative, which integrates veterinary medicine, human health, animal-production systems, and the environment [13]. Systematic control and prevention, through implementation of a national AMR surveillance program, is greatly needed and should be applied in both human and veterinary clinical medicine. The goal of the current study was to investigate AMR among bacterial isolates belonging to En- terobacterales in companion animals within the province of South Korea, with an emphasis on ESC resistance genes in E. coli, Klebsiella spp., Serratia spp., and Enterobacter cloacae. 2. Results 2.1. ESC Resistance Gene Detection Among the 91 ESC-resistant Enterobacterales isolates analyzed in this study, all of the isolates harbored the blaTEM gene. blaCTX-M (n = 42, 82.4%) was abundantly detected in E. coli isolates, whereas blaSHV (n = 16, 94.1%) was mainly detected in Klebsiella pneu- moniae isolates (Table1). None of the Serratia spp. and E. cloacae isolates, except one S. marcescens isolate from Serratia spp. that harbored blaSHV, were positive for blaSHV or blaCTX-M (Table1). Among 55 blaCTX-M-positive Enterobacterales isolates, blaCTX-M-15 (n = 23, 41.8%) and blaCTX-M-55 (n = 12, 21.8%) were the most commonly detected, followed by blaCTX-M-14 (n = 7, 12.7%) (Table2). Enterobacterales isolates carrying genes of blaCTX-M-3, blaCTX-M-61, blaCTX-M-27, and blaCTX-M-65 were also identified (Table2). blaCTX-M-2, blaCTX-M-8, and blaCTX-M-25 gene clusters were not detected in any isolates. Among blaAmpC genes, blaCIT was prevalent in E. coli isolates, blaDHA was predominantly detected in Klebsiella spp. isolates, and blaEBC was common in E. cloacae isolates (Table3). No isolates carrying genes for blaMOX or blaACC were detected. 2.2. Multi-Locus Sequence Typing (MLST) Various sequence types (STs) were revealed among E. coli, K. pneumoniae, K. oxytoca, and E. cloacae isolates. STs of Serratia spp. isolates were not defined due to the lack of an MLST scheme for this genus. Among E. coli isolates, five ST131 and two ST3285 strains were detected from hospital-admitted dogs, with one of each of the following STs: ST372, ST457, ST648, ST1981, ST2179, ST2505, ST4616, ST5150, ST5667, ST8451, ST8885, ST8908, ST10207, ST10220, and ST11000. Accordingly, five ST405, three ST354, two each of ST3285, ST410, ST448, and ST457, and one each of ST68, ST38, ST648, ST1193, ST2541, ST7644, and ST10459 strains were detected in stray dogs. Among six E. coli isolates from hospital-admitted cats, two ST131, two ST156, and one each of ST1262 and ST6105 strains were obtained. In a comprehensive analysis of 19 Klebsiella spp. isolates from hospital-admitted dogs, one ST285, eight ST275, and six ST273 stains were identified among K. pneumoniae isolates, whereas one each of ST34, ST145, ST273, and ST293 strains were identified among K. oxytoca isolates. All Klebsiella spp. isolates from hospital-admitted and stray cats were identified as ST273 strains. Among seven E. cloacae isolates, two ST114 and one each of ST110, ST171, ST198, ST1252, and ST1303 strains were identified (Table4). Antibiotics 2021, 10, 249 3 of 11 Table 1. Distribution of extended-spectrum β-lactamase (ESBL) genes among 91 Enterobacterales isolates from companion animals. Hospital-Admitted Dogs Hospital-Admitted Cats Stray Dogs (n = 23) Stray Cats (n = 1) Total Organism (n = 56) (n = 11) blaCTX-M blaSHV blaTEM blaCTX-M blaSHV blaTEM blaCTX-M blaSHV blaTEM blaCTX-M blaSHV blaTEM blaCTX-M blaSHV blaTEM 42 51 E. coli (n = 51) 21 − 22 15 − 23 6 − 6 − − − − (82.4%) (100%) K. pneumoniae 16 17 7 15 15 − − − 1 1 1 1 − 1 9 (17.6%) (n = 17) (94.1%) (100%) K. oxytoca (n = 5) 4 1 4 − − − − 1 1 − − − 4 (80.0%) 2 (40.0%) 5 (100%) S. marcescens − 1 3 − − − − − 1 − − − − 1 (45.0%) 4 (100%) (n = 4) S. liquefaciens − − 7 −−−−−−−−−−− 7 (100%) (n = 7) E. cloacae (n = 7) − − 5 − − − − − 2 − − − − − 7 (100%) Table 2. CTX-M subtype detection of 55 blaCTX-M-positive Enterobacterales isolates. blaCTX-M Subtype Group Organism Sample Origin CTX-M-1 CTX-M-9 Unidentified CTX-M-15 CTX-M-55 CTX-M-3 CTX-M-61 Total CTX-M-14 CTX-M-27 CTX-M-65 Total E.
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