In this study, we investigated the prevalence and characteristics of methicillin-resistant Staphylococcus aureus (MRSA) isolates from pigs and pig farmers in Korea. A total of 1245 nasal swabs were collected from pigs and farmers at 53 pig farms in nine provinces from 2012 to 2016. The prevalence of MRSA was 7.9% (88/1119) in pigs and 16.7% (21/126) in farmers. Among 119 farmers working on conventional farms, 21 (17.6%) tested positive for MRSA. However, no MRSA was detected in either pigs or farmers at four organic farms. The individual pig-level prevalence of MRSA differed between age groups, with the percentage of positive samples being highest in weaners (17.3%), followed by growers (9.0%), piglets (6.5%), finishers (4.4%), and sows (0%). Two different lineages of MRSA were detected among the 109 isolates from pigs and farmers: (1) livestock-associated types of MRSA belonging to 27 isolates of ST541-t034-V, 24 isolates of ST398-t571-V, 17 isolates of ST398-t034 variant (G420A)-V, and one isolate of ST541-t8588-V; and (2) community-associated types of MRSA belonging to 21 isolates of ST188-t189-IV, 14 isolates of ST72-t324-IV, three isolates of ST72-t664-IV, one isolate of ST72-t148-IV, and one isolate of ST72-t5440-IV. Identical genotypes were detected in both pigs and farmers at six farms. New MRSA clones were isolated from pigs (ST398-t034 (G420A)-V, ST188-t189-IV, and ST398-t571-V) and pig farmers (ST541-t8588-V and ST72-t5440-IV). The prevalence of MRSA was also correlated with antibiotic usage, and the clones showed diversification between pigs and farmers. Ultimately, the increased frequency and diversification of livestock-associated MRSA could be a potential threat to public health in Korea. To our knowledge, this is the first study to report the prevalence and characteristics of MRSA in pigs and pig farmers in Korea.
Get full access to this article
View all access options for this article.
References
1.
Armand-LefevreL, RuimyR, AndremontA. Clonal comparison of Staphylococcus aureus isolates from healthy pig farmers, human controls, and pigs. Emerg Infect Dis, 2005; 11:711–714.
2.
BoostMV, O'DonoghueM, GuardabassiL. Prevalence of carriage and characterisation of methicillin-resistant Staphylococcus aureus in slaughter pigs and personnel exposed to pork carcasses. Hong Kong Med J, 2015; 21Suppl 7:S36–S40.
3.
BoyeK, BartelsMD, AndersenIS, MollerJA, WesthH. A new multiplex PCR for easy screening of methicillin-resistant Staphylococcus aureus SCCmec types I-V. Clin Microbiol Infect, 2007; 13:725–727.
4.
BroensEM, GraatEA, Van der WolfPJ, Van de GiessenAW, De JongMC. Prevalence and risk factor analysis of livestock associated MRSA-positive pig herds in The Netherlands. Prev Vet Med, 2011; 102:41–49.
5.
ChuangYY, HuangYC. Livestock-associated meticillin-resistant Staphylococcus aureus in Asia: An emerging issue?. Int J Antimicrob Agents, 2015; 45:334–340.
6.
CunyC, FriedrichAW, WitteW. Absence of livestock-associated methicillin-resistant Staphylococcus aureus clonal complex CC398 as a nasal colonizer of pigs raised in an alternative system. Appl Envirom Microbiol, 2012; 78:1296–1297.
7.
DierikxCM, HengeveldPD, VeldmanKT, de HaanA, van der VoordeS, DopPY, BoschT, van DiujkerenE. Ten years later: Still a high prevalence of MRSA in slaughter pigs despite a significant reduction in antimicrobial usage in pigs the Netherlands. J Antimicrob Chemother, 2016; 71:2414–2418.
8.
EFSA (European Food Safety Authority). Analysis of the baselinesurvey on the prevalence of methicillin-resistant Staphylococcus aureus (MRSA) in holdings with breeding pigs, in the EU, 2008. Part A. MRSA prevalence estimates; on request from the European Commission. 2009.
9.
EnrightMC, DayNP, DaviesCE, PeacockSJ, SprattBG. Multilocus sequence typing for characterization of methicillin-resistant and methicillin-susceptible clones of Staphylococcus aureus. J Clin Microbiol, 2000; 38:1008–1015.
10.
Ghasemzadeh-MoghaddamH, Ghaznavi-RadE, SekawiZ, Yun-KhoonL, Nazri-AzizM, Awang-HamatR, MellesDC, van BelkumA, Nor-ShamsudinM, NeelaV. Methicillin-susceptible Staphylococcus aureus from clinical and community sources are genetically diverse. Int J Med Microbiol, 2011; 301:347–353.
11.
GoergeT, LorenzMB, van AlenS, HubnerNO, BeckerK, KockR. MRSA colonization and infection among persons with occupational livestock exposure in Europe: Prevalence, preventive options and evidence. Vet Microbiol, 2017; 200:6–12.
12.
Gomez-SanzE, TorresC, LozanoC, Fernandez-PerezR, AspirozC, Ruiz-LarreaF, ZaragagaM. Detection, molecular characterization, and clonal diversity of methicillin-resistant Staphylococcus aureus CC398 and CC97 in Spanish slaughter pigs of different age groups. Foodborne Pathog Dis, 2010; 7:1269–1277.
13.
HarmsenD, ClausH, WitteW, RothgangerJ, ClausH, TurnwaldD, VogelU. Typing of methicillin-resistant Staphylococcus aureus in a university hospital setting by using novel software for spa repeat determination and database management. J Clin Microbiol, 2003; 41:5442–5448.
14.
KoKS, LimSK, JungSC, YoonJM, ChoiJY, SongJH. Sequence type 72 meticillin-resistant Staphylococcus aureus isolates from humans, raw meat and soil in South Korea. J Med Microbiol, 2011; 60:442–445.
15.
LiJ, JiangN, KeY, FeblerAT, WangY, ScwartzS, WuC. Characterization of pig-associated methicillin-resistant Staphylococcus aureus. Vet Microbiol, 2017; 201:183–187.
16.
LimSK, NamHM, JangGC, LeeHS, JungSC, KwakHS. The first detection of methicillin-resistant Staphylococcus aureus ST398 in pigs in Korea. Vet Microbiol, 2012; 155:88–92.
17.
LiuC, ChenZJ, SunZ, FengX, ZouM, CaoW, WangS, ZengJ, WangY. Molecular characteristics and virulence factors in methicillin-susceptible, resistant, and heterogeneous vancomycin-intermediate Staphylococcus aureus from central-southern China. J Microbiol Immunol Infect, 2015; 48:490–496.
18.
MasonWJ, BlevinsJS, BeenkenK, WibowoN, OjhaN, SmeltzerMS. Multiplex PCR protocol for the diagnosis of staphylococcal infection. J Clin Microbiol, 2001; 39:3332–3338.
19.
MoonDC, KimBY, NamHM, JangG-C, JungS-C, LeeH-S, ParkY-H, LimS-K. Draft Genome sequences of a unique t324-ST541-V methicillin-resistant Staphylococcus aureus strain from a pig. J Microbiol Biotechnol, 2016; 26:799–805.
20.
MoonDC, TamangMD, NamHM, JeongJ-H, JangG-C, JungS-C, ParhJ-H, LimS-K. Identification of livestock-associated methicillin-resistant Staphylococcus aureus isolates in Korea and molecular comparison between isolates from animal carcasses and slaughterhouse workers. Foodborne Pathog Dis, 2015; 12:327–334.
21.
MuttersNT, BieberCP, HauckC, ReinerG, MalekV, FrankU. Comparison of livestock-associated and health care-associated MRSA-genes, virulence, and resistance. Diagn Microbiol Infect Dis, 2016; 86:417–421.
22.
NamHM, LeeAL, JungSC, KimM-N, JangG-C, WeS-H, LimS-K. Antimicrobial susceptibility of Staphylococcus aureus and characterization of methicillin-resistant Staphylococcus aureus isolated from bovine mastitis in Korea. Foodborne Pathog Dis, 2011; 8:231–238.
23.
OhSH, WhitleyNC. Pork production in China, Japan and South Korea. Asian-Australas J Anim Sci, 2011; 24:1629–1636.
24.
ParkSH, KimKJ, KimBK, HwangSM. Molecular characterization of community-associated methicillin-resistant and methicillin-susceptible Staphylococcus aureus isolates from children with skin infections in Busan, Korea. J Bacteriol Virol, 2015; 45:104–111.
25.
ParkSY, ChungDR, YooJR, BaekJR, KimSH, HaYE, KangC-I, PeckKR, LeeNY, SongJ-H. Sequence type 72 community-associated meticillin-resistant Staphylococcus aureus emerged as a predominant clone of nasal colonization in newly admitted patients. J Hosp Infect, 2016; 93:386–389.
26.
PeckKR, BaekJY, SongJH, KoKS. Comparison of genotypes and enterotoxin genes between Staphylococcus aureus isolates from blood and nasal colonizers in a Korean hospital. J Korean Med Sci, 2009; 24:585–591.
27.
PletinckxLJ, VerheggheM, CrombèF, DewulfJ, De BleekerY, RasschaertG, ButayeP, GoddeerisBM, De ManI. Evidence of possible methicillin-resistant Staphylococcus aureus ST398 spread between pigs and other animal and people residing on the same farm. Prev Vet Med, 2013; 109:293–303.
28.
ReynagaE, NavarroM, VilamalaA, RooreP, QuintanaM, Garcia-NunezM, FiguerasR, TorresC, LucchettiG, SabriM. Prevalence of colonization by methicillin-resistant Staphylococcus aureus ST398 in pigs and pig farm workers in an area of Catalonia, Spain. BMC Infect Dis, 2016; 16:716.
29.
SatoT, UsuiM, MotoyaT, SugiyamaT, TamuraY. Characterisation of meticillin-resistant Staphylococcus aureus ST97 and ST5 isolated from pigs in Japan. J Glob Antimicrob Resist, 2015; 3:283–285.
30.
TenhagenBA, FetschA, StuhrenbergB, ScheuterG, GueraGB, HammeriJA, HertwigS, KowellJ, KampeV, SchroeterA, BraunigJ, KasbohrerA, AppelB. Prevalence of MRSA types in slaughter pigs in different German abattoirs. Vet Rec, 2009; 165:589–593.
31.
van de VijverLP, TulinskiP, BondtN, MeviusD, VerwerC. Prevalence and molecular characteristics of methicillin-resistant Staphylococcus aureus (MRSA) in organic pig herds in The Netherlands. Zoonoses Public health, 2014; 61:338–345.
32.
VerheggheM, PletinckxLJ, CrombeF, et al.Vandermissen T, Haesbrouck F, Butaye P, Heyndrickx M, Rosschaert G. Methicillin-resistant Staphylococcus aureus (MRSA) ST398 in pig farms and multispecies farms. Zoonoses Public health, 2013; 60:366–374.
