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http://dx.doi.org/10.5851/kosfa.2021.e74

Profiles of Non-aureus Staphylococci in Retail Pork and Slaughterhouse Carcasses: Prevalence, Antimicrobial Resistance, and Genetic Determinant of Fusidic Acid Resistance  

Yang, Yu Jin (Department of Veterinary Microbiology, College of Veterinary Medicine and Research Institute for Veterinary Science, Seoul National University)
Lee, Gi Yong (Department of Animal Science and Technology, School of Bioresources and Bioscience, Chung-Ang University)
Kim, Sun Do (Department of Animal Science and Technology, School of Bioresources and Bioscience, Chung-Ang University)
Park, Ji Heon (Department of Animal Science and Technology, School of Bioresources and Bioscience, Chung-Ang University)
Lee, Soo In (Department of Animal Science and Technology, School of Bioresources and Bioscience, Chung-Ang University)
Kim, Geun-Bae (Department of Animal Science and Technology, School of Bioresources and Bioscience, Chung-Ang University)
Yang, Soo-Jin (Department of Veterinary Microbiology, College of Veterinary Medicine and Research Institute for Veterinary Science, Seoul National University)
Publication Information
Food Science of Animal Resources / v.42, no.2, 2022 , pp. 225-239 More about this Journal
Abstract
As commensal colonizers in livestock, there has been little attention on staphylococci, especially non-aureus staphylococci (NAS), contaminating meat production chain. To assess prevalence of staphylococci in retail pork and slaughterhouse carcass samples in Korea, we collected 578 samples from Korean slaughterhouses (n=311) and retail markets (n=267) for isolation of staphylococci and determined antimicrobial resistance phenotypes in all the isolates. The presence of and prevalence of fusB-family genes (fusB, fusC, fusD, and fusF) and mutations in fusA genes were examined in fusidic acid resistant isolates. A total of 47 staphylococcal isolates of 4 different species (Staphylococcus aureus, n=4; S. hyicus, n=1; S. epidermidis, n=10; Mammaliicoccus sciuri, n=32) were isolated. Fusidic acid resistance were confirmed in 9/10 S. epidermidis and all of the 32 M. sciuri (previously S. sciuri) isolates. Acquired fusidic acid resistance genes were detected in all the resistant strains; fusB and fusC in S. epidermidis and fusB/C in M. sciuri. Multi-locus sequence type analysis revealed that ST63 (n=10, 31%) and ST30 (n=8, 25%) genotypes were most prevalent among fusidic acid resistant M. sciuri isolates. In conclusion, the high prevalence of fusB-family genes in S. epidermidis and M. sciuri strains isolated from pork indicated that NAS might act as a reservoir for fusidic acid resistance gene transmissions in pork production chains.
Keywords
non-aureus staphylococci; antimicrobial resistance; retail pork; slaughterhouse carcass;
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1 Davis CP. 1996. Chapter 6 Normal flora. In Medical microbiology. 4th ed. Baron S (ed). University of Texas Medical Branch at Galveston, Galveston, TX, USA.
2 Fessler AT, Billerbeck C, Kadlec K, Schwarz S. 2010. Identification and characterization of methicillin-resistant coagulase-negative staphylococci from bovine mastitis. J Antimicrob Chemother 65:1576-1582.   DOI
3 Founou LL, Founou RC, Essack SY. 2016. Antibiotic resistance in the food chain: A developing country-perspective. Front Microbiol 7:1881.
4 Godtfredsen WO, Jahnsen S, Lorck H, Roholt K, Tybring L. 1962. Fusidic acid: A new antibiotic. Nature 193:987.   DOI
5 Hanson BM, Dressler AE, Harper AL, Scheibel RP, Wardyn SE, Roberts LK, Kroeger JS, Smith TC. 2011. Prevalence of Staphylococcus aureus and methicillin-resistant Staphylococcus aureus (MRSA) on retail meat in Iowa. J Infect Public Health 4:169-174.   DOI
6 Hong SN, Kim J, Sung HH. 2016. A study on changes in antimicrobial resistant Staphylococcus aureus from wound isolates in a South Korean University Hospital for the past 10 years (2006, 2016). Korean J Clin Lab Sci 48:335-342.   DOI
7 Wang YT, Lin YT, Wan TW, Wang DY, Lin HY, Lin CY, Chen YC, Teng LJ. 2019. Distribution of antibiotic resistance genes among Staphylococcus species isolated from ready-to-eat foods. J Food Drug Anal 27:841-848.   DOI
8 Huber H, Ziegler D, Pfluger V, Vogel G, Zweifel C, Stephan R. 2011. Prevalence and characteristics of methicillin-resistant coagulase-negative staphylococci from livestock, chicken carcasses, bulk tank milk, minced meat, and contact persons. BMC Vet Res 7:6.   DOI
9 Hung WC, Chen HJ, Lin YT, Tsai JC, Chen CW, Lu HH, Tseng SP, Jheng YY, Leong KH, Teng LJ. 2015. Skin commensal staphylococci may act as reservoir for fusidic acid resistance genes. PLOS ONE 10:e0143106.   DOI
10 Kolbert CP, Connolly JE, Lee MJ, Persing DH. 1995. Detection of the staphylococcal mecA gene by chemiluminescent DNA hybridization. J Clin Microbiol 33:2179-2182.   DOI
11 Chen HJ, Tsai JC, Hung WC, Tseng SP, Hsueh PR, Teng LJ. 2011. Identification of fusB-mediated fusidic acid resistance islands in Staphylococcus epidermidis isolates. Antimicrob Agents Chemother 55:5842-5849.   DOI
12 Garza-Gonzalez E, Lopez D, Pezina C, Muruet W, Bocanegra-Garcia V, Munoz I, Ramirez C, LLaca-Diaz JM. 2010. Diversity of staphylococcal cassette chromosome mec structures in coagulase-negative staphylococci and relationship to drug resistance. J Med Microbiol 59:323-329.   DOI
13 Archer GL, Niemeyer DM. 1994. Origin and evolution of DNA associated with resistance to methicillin in staphylococci. Trends Microbiol 2:343-347.   DOI
14 Enright MC, Day NPJ, Davies CE, Peacock SJ, Spratt BG. 2000. Multilocus sequence typing for characterization of methicillin-resistant and methicillin-susceptible clones of Staphylococcus aureus. J Clin Microbiol 38:1008-1015.   DOI
15 EUCAST. 2021. European committee on antimicrobial susceptibility testing. Available from: https://www.eucast.org/clinical_breakpoints/. Accessed at Aug 2, 2021.
16 Fernandes P. 2016. Fusidic acid: A bacterial elongation factor inhibitor for the oral treatment of acute and chronic staphylococcal infections. Cold Spring Harb Perspect Med 6:a025437.   DOI
17 Fijalkowski K, Peitler D, Karakulska J. 2016. Staphylococci isolated from ready-to-eat meat - Identification, antibiotic resistance and toxin gene profile. Int J Food Microbiol 238:113-120.   DOI
18 Geha DJ, Uhl JR, Gustaferro CA, Persing DH. 1994. Multiplex PCR for identification of methicillin-resistant staphylococci in the clinical laboratory. J Clin Microbiol 32:1768-1772.   DOI
19 Mendoza M, Meugnier H, Bes M, Etienne J, Freney J. 1998. Identification of Staphylococcus species by 16S-23S rDNA intergenic spacer PCR analysis. Int J Syst Bacteriol 48:1049-1055.   DOI
20 Okoli CE, Njoga EO, Enem SI, Godwin EE, Nwanta JA, Chah KF. 2018. Prevalence, toxigenic potential and antimicrobial susceptibility profile of Staphylococcus isolated from ready-to-eat meats. Vet World 11:1214-1221.   DOI
21 Piette A, Verschraegen G. 2009. Role of coagulase-negative staphylococci in human disease. Vet Microbiol 134:45-54.   DOI
22 Thomas JC, Vargas MR, Miragaia M, Peacock SJ, Archer GL, Enright MC. 2007. Improved multilocus sequence typing scheme for Staphylococcus epidermidis. J Clin Microbiol 45:616-619.   DOI
23 Ruppe E, Barbier F, Mesli Y, Maiga A, Cojocaru R, Benkhalfat M, Benchouk S, Hassaine H, Maiga I, Diallo A, Koumare AK, Ouattara K, Soumare S, Dufourcq JB, Nareth C, Sarthou JL, Andremont A, Ruimy R. 2009. Diversity of staphylococcal cassette chromosome mec structures in methicillin-resistant Staphylococcus epidermidis and Staphylococcus haemolyticus strains among outpatients from four countries. Antimicrob Agents Chemother 53:442-449.   DOI
24 Schauer B, Szostak MP, Ehricht R, Monecke S, Fessler AT, Schwarz S, Spergser J, Krametter-Frotscher R, Loncaric I. 2021. Diversity of methicillin-resistant coagulase-negative Staphylococcus spp. and methicillin-resistant Mammaliicoccus spp. isolated from ruminants and New World camelids. Vet Microbiol 254:109005.   DOI
25 Sugden R, Kelly R, Davies S. 2016. Combatting antimicrobial resistance globally. Nat Microbiol 1:16187.   DOI
26 Turnidge J, Collignon P. 1999. Resistance to fusidic acid. Int J Antimicrob Agents 12: Suppl 2:S35-S44.   DOI
27 Clinical and Laboratory Standards Institute [CLSI]. 2015. Performance standards for antimicrobial disk and dilution susceptibility tests for bacteria isolated from animals. 3rd ed. Clinical and Laboratory Standards Institute, Wayne, PA, USA.
28 von Wintersdorff CJH, Penders J, van Niekerk JM, Mills ND, Majumder S, van Alphen LB, Savelkoul PHM, Wolffs PFG. 2016. Dissemination of antimicrobial resistance in microbial ecosystems through horizontal gene transfer. Front Microbiol 7:173.   DOI
29 Wu S, Huang J, Wu Q, Zhang J, Zhang F, Yang X, Wu H, Zeng H, Chen M, Ding Y, Wang J, Lei T, Zhang S, Xue L. 2018. Staphylococcus aureus isolated from retail meat and meat products in China: Incidence, antibiotic resistance and genetic diversity. Front Microbiol 9:1-14.   DOI
30 Chuang YY, Huang YC. 2015. Livestock-associated meticillin-resistant Staphylococcus aureus in Asia: An emerging issue? Int J Antimicrob Agents 45:334-340.   DOI
31 Lozano C, Lopez M, Gomez-Sanz E, Ruiz-Larrea F, Torres C, Zarazaga M. 2009. Detection of methicillin-resistant Staphylococcus aureus ST398 in food samples of animal origin in Spain. J Antimicrob Chemother 64:1325-1326.   DOI
32 Nemeghaire S, Argudin MA, Haesebrouck F, Butaye P. 2014b. Molecular epidemiology of methicillin-resistant Staphylococcus sciuri in healthy chickens. Vet Microbiol 171:357-363.   DOI
33 Chen HJ, Hung WC, Tseng SP, Tsai JC, Hsueh PR, Teng LJ. 2010. Fusidic acid resistance determinants in Staphylococcus aureus clinical isolates. Antimicrob Agents Chemother 54:4985-4991.   DOI
34 Golding GR, Bryden L, Levett PN, McDonald RR, Wong A, Wylie J, Graham MR, Tyler S, van Domselaar G, Simor AE, Gravel D, Mulvey MR. 2010. Livestock-associated methicillin-resistant Staphylococcus aureus sequence type 398 in humans, Canada. Emerg Infect Dis 16:587-594.   DOI
35 McLaws F, Chopra I, O'Neill AJ. 2008. High prevalence of resistance to fusidic acid in clinical isolates of Staphylococcus epidermidis. J Antimicrob Chemother 61:1040-1043.   DOI
36 O'Brien AM, Hanson BM, Farina SA, Wu JY, Simmering JE, Wardyn SE, Forshey BM, Kulick ME, Wallinga DB, Smith TC. 2012. MRSA in conventional and alternative retail pork products. PLOS ONE 7:e30092.   DOI
37 Lim YJ, Hyun JE, Hwang CY. 2020. Identification of fusidic acid resistance in clinical isolates of Staphylococcus pseudintermedius from dogs in Korea. Vet Dermatol 31:267-e62.   DOI
38 Bagcigil FA, Moodley A, Baptiste KE, Jensen VF, Guardabassi L. 2007. Occurrence, species distribution, antimicrobial resistance and clonality of methicillin- and erythromycin-resistant staphylococci in the nasal cavity of domestic animals. Vet Microbiol 121:307-315.   DOI
39 Chen HJ, Hung WC, Lin YT, Tsai JC, Chiu HC, Hsueh PR, Teng LJ. 2015. A novel fusidic acid resistance determinant, fusF, in Staphylococcus cohnii. J Antimicrob Chemother 70:416-419.   DOI
40 Kondo Y, Ito T, Ma XX, Watanabe S, Kreiswirth BN, Etienne J, Hiramatsu K. 2007. Combination of multiplex PCRs for staphylococcal cassette chromosome mec type assignment: Rapid identification system for mec, ccr, and major differences in junkyard regions. Antimicrob Agents Chemother 51:264-274.   DOI
41 Nam HM, Lee AL, Jung SC, Kim MN, Jang GC, Wee SH, Lim SK. 2011. Antimicrobial susceptibility of Staphylococcus aureus and characterization of methicillin-resistant Staphylococcus aureus isolated from bovine mastitis in Korea. Foodborne Pathog Dis 8:231-238.   DOI
42 Nemeghaire S, Argudin MA, Fessler AT, Hauschild T, Schwarz S, Butaye P. 2014a. The ecological importance of the Staphylococcus sciuri species group as a reservoir for resistance and virulence genes. Vet Microbiol 171:342-356.   DOI
43 Norstrom T, Lannergard J, Hughes D. 2007. Genetic and phenotypic identification of fusidic acid-resistant mutants with the small-colony-variant phenotype in Staphylococcus aureus. Antimicrob Agents Chemother 51:4438-4446.   DOI
44 O'Neill AJ, Chopra I. 2006. Molecular basis of fusB-mediated resistance to fusidic acid in Staphylococcus aureus. Mol Microbiol 59:664-676.   DOI
45 Lee JYH, Monk IR, Goncalves da Silva A, Seemann T, Chua KYL, Kearns A, Hill R, Woodford N, Bartels MD, Strommenger B, Laurent F, Dodemont M, Deplano A, Patel R, Larsen AR, Korman TM, Stinear TP, Howden BP. 2018. Global spread of three multidrug-resistant lineages of Staphylococcus epidermidis. Nat Microbiol 3:1175-1185.   DOI
46 O'Neill AJ, McLaws F, Kahlmeter G, Henriksen AS, Chopra I. 2007. Genetic basis of resistance to fusidic acid in staphylococci. Antimicrob Agents Chemother 51:1737-1740.   DOI
47 Tang Y, Larsen J, Kjeldgaard J, Andersen PS, Skov R, Ingmer H. 2017. Methicillin-resistant and -susceptible Staphylococcus aureus from retail meat in Denmark. Int J Food Microbiol 249:72-76.   DOI