Abstract
Staphylococcus aureus (S. aureus) is a fearsome bacterial pathogen that can colonize and infect humans and animals. Depending on the different sources, MRSA is classified as hospital-associated methicillin-resistant S. aureus (HA-MRSA), community-associated MRSA (CA-MRSA), and livestock-associated MRSA (LA-MRSA). LA-MRSA is initially associated with livestock, and clonal complexes (CCs) were almost always 398. However, the continued development of animal husbandry, globalization, and the widespread use of antibiotics have increased the spread of LA-MRSA among humans, livestock, and the environment, and other clonal complexes such as CC9, CC5, and CC8 have gradually emerged in various countries. This may be due to frequent host switching between humans and animals, as well as between animals. Host-switching is typically followed by subsequent adaptation through acquisition and/or loss of mobile genetic elements (MGEs) such as phages, pathogenicity islands, and plasmids as well as further host-specific mutations allowing it to expand into new host populations. This review aimed to provide an overview of the transmission characteristics of S. aureus in humans, animals, and farm environments, and also to describe the main prevalent clones of LA-MRSA and the changes in MGEs during host switching.
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References
Abd El-Hamid MI, Bendary MM, Merwad AMA, Elsohaby I, Mohammad Ghaith D, Alshareef WA (2019) What is behind phylogenetic analysis of hospital-, community- and livestock-associated methicillin-resistant Staphylococcus aureus? Transbound Emerg Dis 66(4):1506–1517. https://doi.org/10.1111/tbed.13170
Agersø Y, Hasman H, Cavaco LM, Pedersen K, Aarestrup FM (2012) Study of methicillin resistant Staphylococcus aureus (MRSA) in Danish pigs at slaughter and in imported retail meat reveals a novel MRSA type in slaughter pigs. Vet Microbiol 157(1-2):246–250. https://doi.org/10.1016/j.vetmic.2011.12.023
Agnoletti F, Mazzolini E, Bacchin C, Bano L, Berto G, Rigoli R et al (2014) First reporting of methicillin-resistant Staphylococcus aureus (MRSA) ST398 in an industrial rabbit holding and in farm-related people. Vet Microbiol 170(1-2):172–177. https://doi.org/10.1016/j.vetmic.2014.01.035
Al-Amery K, Elhariri M, Elsayed A, El-Moghazy G, Elhelw R, El-Mahallawy H et al (2019) Vancomycin-resistant Staphylococcus aureus isolated from camel meat and slaughterhouse workers in Egypt. Antimicrob Resist Infect Control 8:129. https://doi.org/10.1186/s13756-019-0585-4
Alba P, Feltrin F, Cordaro G, Porrero MC, Kraushaar B, Argudín MA et al (2015) Livestock-associated methicillin resistant and methicillin susceptible Staphylococcus aureus sequence type (CC)1 in European farmed animals: high genetic relatedness of isolates from Italian cattle herds and humans. PLoS One 10(8):e0137143. https://doi.org/10.1371/journal.pone.0137143
Angen Ø, Skade L, Urth TR, Andersson M, Bækbo P, Larsen AR (2018) Controlling transmission of MRSA to humans during short-term visits to swine farms using dust masks. Front Microbiol 9:3361. https://doi.org/10.3389/fmicb.2018.03361
Attili AR, Bellato A, Robino P, Galosi L, Papeschi C, Rossi G et al (2020) Analysis of the antibiotic resistance profiles in methicillin-sensitive S. aureus pathotypes isolated on a commercial rabbit farm in Italy. Antibiotics (Basel) 9(10):673. https://doi.org/10.3390/antibiotics9100673
Avberšek J, Golob M, Papić B, Dermota U, Grmek Košnik I, Kušar D et al (2021) Livestock-associated methicillin-resistant Staphylococcus aureus: establishing links between animals and humans on livestock holdings. Transbound Emerg Dis 68(2):789–801. https://doi.org/10.1111/tbed.13745
Back SH, Eom HS, Lee HH, Lee GY, Park KT, Yang SJ (2020) Livestock-associated methicillin-resistant Staphylococcus aureus in Korea: antimicrobial resistance and molecular characteristics of LA-MRSA strains isolated from pigs, pig farmers, and farm environment. J Vet Sci 21(1):e2. https://doi.org/10.4142/jvs.2020.21.e2
Bal AM, Coombs GW, Holden MTG, Lindsay JA, Nimmo GR, Tattevin P et al (2016) Genomic insights into the emergence and spread of international clones of healthcare-, community- and livestock-associated meticillin-resistant Staphylococcus aureus: blurring of the traditional definitions. J Glob Antimicrob Resist 6:95–101. https://doi.org/10.1016/j.jgar.2016.04.004
Ballhausen B, Jung P, Kriegeskorte A, Makgotlho PE, Ruffing U, von Müller L et al (2014) LA-MRSA CC398 differ from classical community acquired-MRSA and hospital acquired-MRSA lineages: functional analysis of infection and colonization processes. Int J Med Microbiol 304(7):777–786. https://doi.org/10.1016/j.ijmm.2014.06.006
Barberio A, Mazzolini E, Dall'Ava B, Rosa G, Brunetta R, Zandonà L et al (2019) A longitudinal case study on dissemination of ST398 methicillin-resistant Staphylococcus aureus within a dairy cow herD. Foodborne Pathog Dis 16(11):761–768. https://doi.org/10.1089/fpd.2019.2622
Boost MV, Wong A, Ho J, O'Donoghue M (2013) Isolation of methicillin-resistant Staphylococcus aureus (MRSA) from retail meats in Hong Kong. Foodborne Pathog Dis 10(8):705–710. https://doi.org/10.1089/fpd.2012.1415
Bootsma MC, Wassenberg MW, Trapman P, Bonten MJ (2011) The nosocomial transmission rate of animal-associated ST398 meticillin-resistant Staphylococcus aureus. J R Soc Interface 8(57):578–584. https://doi.org/10.1098/rsif.2010.0349
Bouchami O, Fraqueza MJ, Faria NA, Alves V, Lawal OU, de Lencastre H et al (2020) Evidence for the dissemination to humans of methicillin-resistant Staphylococcus aureus ST398 through the pork production chain: a sTUDY in a Portuguese slaughterhouse. Microorganisms 8(12):1892. https://doi.org/10.3390/microorganisms8121892
Bouiller K, Bertrand X, Hocquet D, Chirouze C (2020) Human infection of methicillin-susceptible Staphylococcus aureus CC398: a review. Microorganisms 8(11):1737. https://doi.org/10.3390/microorganisms8111737
Broens EM, Graat EA, van de Giessen AW, Broekhuizen-Stins MJ, de Jong MC (2012) Quantification of transmission of livestock-associated methicillin resistant Staphylococcus aureus in pigs. Vet Microbiol 155(2-4):381–388. https://doi.org/10.1016/j.vetmic.2011.09.010
Butaye P, Devriese LA, Haesebrouck F (2003) Antimicrobial growth promoters used in animal feed: effects of less well known antibiotics on gram-positive bacteria. Clin Microbiol Rev 16(2):175–188. https://doi.org/10.1128/cmr.16.2.175-188.2003
Bystroń J, Podkowik M, Piasecki T, Wieliczko A, Molenda J, Bania J (2010) Genotypes and enterotoxin gene content of S. aureus isolates from poultry. Vet Microbiol 144(3-4):498–501. https://doi.org/10.1016/j.vetmic.2010.01.029
Carfora V, Giacinti G, Sagrafoli D, Marri N, Giangolini G, Alba P et al (2016) Methicillin-resistant and methicillin-susceptible Staphylococcus aureus in dairy sheep and in-contact humans: an intra-farm study. J Dairy Sci 99(6):4251–4258. https://doi.org/10.3168/jds.2016-10912
Casey JA, Curriero FC, Cosgrove SE, Nachman KE, Schwartz BS (2013) High-density livestock operations, crop field application of manure, and risk of community-associated methicillin-resistant Staphylococcus aureus infection in Pennsylvania. JAMA Intern Med 173(21):1980–1990. https://doi.org/10.1001/jamainternmed.2013.10408
Chambers HF, Deleo FR (2009) Waves of resistance: Staphylococcus aureus in the antibiotic era. Nat Rev Microbiol 7(9):629–641. https://doi.org/10.1038/nrmicro2200
Chen CJ, Lauderdale TY, Lu CT, Chuang YY, Yang CC, Wu TS et al (2018) Clinical and molecular features of MDR livestock-associated MRSA ST9 with staphylococcal cassette chromosome mecXII in humans. J Antimicrob Chemother 73(1):33–40. https://doi.org/10.1093/jac/dkx357
Chen K, Stephanou AS, Roberts GA, White JH, Cooper LP, Houston PJ et al (2016) The Type I restriction enzymes as barriers to horizontal gene transfer: determination of the DNA target sequences recognised by livestock-associated methicillin-resistant Staphylococcus aureus clonal complexes 133/ST771 and 398. Adv Exp Med Biol 915:81–97. https://doi.org/10.1007/978-3-319-32189-9_7
Coates R, Moran J, Horsburgh MJ (2014) Staphylococci: colonizers and pathogens of human skin. Future Microbiol 9(1):75–91. https://doi.org/10.2217/fmb.13.145
Coombs GW, Daley D, Shoby P, Yee NWT, Robinson JO, Murray R et al (2022) Genomic characterisation of CC398 MRSA causing severe disease in Australia. Int J Antimicrob Agents 59(4):106577. https://doi.org/10.1016/j.ijantimicag.2022.106577
Cuny C, Nathaus R, Layer F, Strommenger B, Altmann D, Witte W (2009) Nasal colonization of humans with methicillin-resistant Staphylococcus aureus (MRSA) CC398 with and without exposure to pigs. PLoS One 4(8):e6800. https://doi.org/10.1371/journal.pone.0006800
Cuny C, Layer F, Hansen S, Werner G, Witte W (2019) Nasal colonization of humans with occupational exposure to raw meat and to raw meat products with methicillin-susceptible and methicillin-resistant Staphylococcus aureus. Toxins (Basel) 11(4):190. https://doi.org/10.3390/toxins11040190
Devriese LA, Van Damme LR, Fameree L (1972) Methicillin (cloxacillin)-resistant Staphylococcus aureus strains isolated from bovine mastitis cases. Zentralbl Veterinarmed B 19(7):598–605. https://doi.org/10.1111/j.1439-0450.1972.tb00439.x
Egyir B, Hadjirin NF, Gupta S, Owusu F, Agbodzi B, Adogla-Bessa T et al (2020) Whole-genome sequence profiling of antibiotic-resistant Staphylococcus aureus isolates from livestock and farm attendants in Ghana. J Glob Antimicrob Resist 22:527–532. https://doi.org/10.1016/j.jgar.2020.03.029
Elston DM (2007) Community-acquired methicillin-resistant Staphylococcus aureus. J Am Acad Dermatol 56(1):1–16. https://doi.org/10.1016/j.jaad.2006.04.018
Elstrøm P, Grøntvedt CA, Gabrielsen C, Stegger M, Angen Ø, Åmdal S et al (2019) Livestock-associated MRSA CC1 in Norway; introduction to pig farms, zoonotic transmission, and eradication. Front Microbiol 10:139. https://doi.org/10.3389/fmicb.2019.00139
Enright MC, Day NP, 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(3):1008–1015. https://doi.org/10.1128/jcm.38.3.1008-1015.2000
European Food Safety Authority, European Centre for Disease Prevention and Control (2020) The European Union Summary Report on Antimicrobial Resistance in zoonotic and indicator bacteria from humans, animals and food in 2017/2018. EFSA Journal 18(3):e06007
Fang HW, Chiang PH, Huang YC (2014) Livestock-associated methicillin-resistant Staphylococcus aureus ST9 in pigs and related personnel in Taiwan. PLoS One 9(2):e88826. https://doi.org/10.1371/journal.pone.0088826
Feßler AT, Scholtzek AD, Schug AR, Kohn B, Weingart C, Schink AK et al (2022) Antimicrobial and biocide resistance among feline and canine Staphylococcus aureus and Staphylococcus pseudintermedius isolates from diagnostic submissions. Antibiotics (Basel) 11(2):127. https://doi.org/10.3390/antibiotics11020127
Frana TS, Beahm AR, Hanson BM, Kinyon JM, Layman LL, Karriker LA et al (2013) Isolation and characterization of methicillin-resistant Staphylococcus aureus from pork farms and visiting veterinary students. PLoS One 8(1):e53738. https://doi.org/10.1371/journal.pone.0053738
Frénay HM, Bunschoten AE, Schouls LM, van Leeuwen WJ, Vandenbroucke-Grauls CM, Verhoef J et al (1996) Molecular typing of methicillin-resistant Staphylococcus aureus on the basis of protein A gene polymorphism. Eur J Clin Microbiol Infect Dis 15(1):60–64. https://doi.org/10.1007/bf01586186
Gao FZ, He LY, He LX, Zou HY, Zhang M, Wu DL et al (2020) Untreated swine wastes changed antibiotic resistance and microbial community in the soils and impacted abundances of antibiotic resistance genes in the vegetables. Sci Total Environ 741:140482. https://doi.org/10.1016/j.scitotenv.2020.140482
Garcia-Graells C, Antoine J, Larsen J, Catry B, Skov R, Denis O (2012) Livestock veterinarians at high risk of acquiring methicillin-resistant Staphylococcus aureus ST398. Epidemiol Infect 140(3):383–389. https://doi.org/10.1017/s0950268811002263
Gómez-Sanz E, Torres C, Lozano C, Fernández-Pérez R, Aspiroz C, Ruiz-Larrea F et al (2010) 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 7(10):1269–1277. https://doi.org/10.1089/fpd.2010.0610
Graveland H, Wagenaar JA, Bergs K, Heesterbeek H, Heederik D (2011) Persistence of livestock associated MRSA CC398 in humans is dependent on intensity of animal contact. PLoS One 6(2):e16830. https://doi.org/10.1371/journal.pone.0016830
Haaber J, Penadés JR, Ingmer H (2017) Transfer of antibiotic resistance in Staphylococcus aureus. Trends Microbiol 25(11):893–905. https://doi.org/10.1016/j.tim.2017.05.011
Hansen JE, Stegger M, Pedersen K, Sieber RN, Larsen J, Larsen G et al (2020) Spread of LA-MRSA CC398 in Danish mink (Neovison vison) and mink farm workers. Vet Microbiol 245:108705. https://doi.org/10.1016/j.vetmic.2020.108705
Hata E (2016) Bovine mastitis outbreak in Japan caused by methicillin-resistant Staphylococcus aureus New York/Japan clone. J Vet Diagn Invest 28(3):291–298. https://doi.org/10.1177/1040638716643126
Hau SJ, Haan JS, Davies PR, Frana T, Nicholson TL (2018a) Antimicrobial resistance distribution differs among methicillin resistant Staphylococcus aureus sequence type (ST) 5 isolates from health care and agricultural sources. Front Microbiol 9:2102. https://doi.org/10.3389/fmicb.2018.02102
Hau SJ, Kellner S, Eberle KC, Waack U, Brockmeier SL, Haan JS et al (2018b) Methicillin-resistant Staphylococcus aureus sequence type (ST) 5 isolates from health care and agricultural sources adhere equivalently to human keratinocytes. Appl Environ Microbiol 84(2):e02073–e02017. https://doi.org/10.1128/aem.02073-17
He L, Zheng HX, Wang Y, Le KY, Liu Q, Shang J et al (2018) Detection and analysis of methicillin-resistant human-adapted sequence type 398 allows insight into community-associated methicillin-resistant Staphylococcus aureus evolution. Genome Med 10(1):5. https://doi.org/10.1186/s13073-018-0514-9
He W, Liu Y, Qi J, Chen H, Zhao C, Zhang F et al (2013) Food-animal related Staphylococcus aureus multidrug-resistant ST9 strains with toxin genes. Foodborne Pathog Dis 10(9):782–788. https://doi.org/10.1089/fpd.2012.1452
Hetem DJ, Bootsma MC, Troelstra A, Bonten MJ (2013) Transmissibility of livestock-associated methicillin-resistant Staphylococcus aureus. Emerg Infect Dis 19(11):1797–1802. https://doi.org/10.3201/eid1911.121085
Islam MA, Parveen S, Rahman M, Huq M, Nabi A, Khan ZUM et al (2019) Occurrence and characterization of methicillin resistant Staphylococcus aureus in processed raw foods and ready-to-eat foods in an urban setting of a developing country. Front Microbiol 10:503. https://doi.org/10.3389/fmicb.2019.00503
Ito T, Katayama Y, Asada K, Mori N, Tsutsumimoto K, Tiensasitorn C et al (2001) Structural comparison of three types of staphylococcal cassette chromosome mec integrated in the chromosome in methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother 45(5):1323–1336. https://doi.org/10.1128/aac.45.5.1323-1336.2001
Jans C, Merz A, Johler S, Younan M, Tanner SA, Kaindi DWM et al (2017) East and West African milk products are reservoirs for human and livestock-associated Staphylococcus aureus. Food Microbiol 65:64–73. https://doi.org/10.1016/j.fm.2017.01.017
Jiménez-Truque N, Saye EJ, Soper N, Saville BR, Thomsen I, Edwards KM et al (2016) Longitudinal assessment of colonization with Staphylococcus aureus in healthy collegiate athletes. J Pediatric Infect Dis Soc 5(2):105–113. https://doi.org/10.1093/jpids/piu108
Johnson LB, Ramani A, Guervil DJ (2019) Use of ceftaroline fosamil in osteomyelitis: CAPTURE Study Experience. BMC Infect Dis 19(1):183. https://doi.org/10.1186/s12879-019-3791-z
Katale BZ, Misinzo G, Mshana SE, Chiyangi H, Campino S, Clark TG et al (2020) Genetic diversity and risk factors for the transmission of antimicrobial resistance across human, animals and environmental compartments in East Africa: a review. Antimicrob Resist Infect Control 9(1):127. https://doi.org/10.1186/s13756-020-00786-7
Kinross P, Petersen A, Skov R, Van Hauwermeiren E, Pantosti A, Laurent F et al (2017) Livestock-associated meticillin-resistant Staphylococcus aureus (MRSA) among human MRSA isolates, European Union/European Economic Area countries, 2013. Euro Surveill 22(44). https://doi.org/10.2807/1560-7917.Es.2017.22.44.16-00696
Kobusch I, Schröter I, Linnemann S, Schollenbruch H, Hofmann F, Boelhauve M (2022) Prevalence of LA-MRSA in pigsties: analysis of factors influencing the (De)colonization process. Sci Rep 12(1):18000. https://doi.org/10.1038/s41598-022-21903-z
Köck R, Becker K, Cookson B, van Gemert-Pijnen JE, Harbarth S, Kluytmans J et al (2010) Methicillin-resistant Staphylococcus aureus (MRSA): burden of disease and control challenges in Europe. Euro Surveill 15(41):19688. https://doi.org/10.2807/ese.15.41.19688-en
Köck R, Loth B, Köksal M, Schulte-Wülwer J, Harlizius J, Friedrich AW (2012) Persistence of nasal colonization with livestock-associated methicillin-resistant Staphylococcus aureus in pig farmers after holidays from pig exposure. Appl Environ Microbiol 78(11):4046–4047. https://doi.org/10.1128/aem.00212-12
Krupa P, Bystroń J, Bania J, Podkowik M, Empel J, Mroczkowska A (2014) Genotypes and oxacillin resistance of Staphylococcus aureus from chicken and chicken meat in Poland. Poult Sci 93(12):3179–3186. https://doi.org/10.3382/ps.2014-04321
Kukułowicz A, Steinka I, Siwek A (2021) Presence of antibiotic-resistant staphylococcus aureus in fish and seafood originating from points of sale in the Tri-City Area (Poland). J Food Prot 84(11):1911–1914. https://doi.org/10.4315/jfp-21-115
Kumar P (2020) A review on quinoline derivatives as anti-methicillin resistant Staphylococcus aureus (MRSA) agents. BMC Chem 14(1):17. https://doi.org/10.1186/s13065-020-00669-3
Lagos AC, Sundqvist M, Dyrkell F, Stegger M, Söderquist B, Mölling P (2022) Evaluation of within-host evolution of methicillin-resistant Staphylococcus aureus (MRSA) by comparing cgMLST and SNP analysis approaches. Sci Rep 12(1):10541. https://doi.org/10.1038/s41598-022-14640-w
Lakhundi S, Zhang K (2018) Methicillin-resistant Staphylococcus aureus: molecular characterization, evolution, and epidemiology. Clin Microbiol Rev 31(4). https://doi.org/10.1128/cmr.00020-18
Landers TF, Cohen B, Wittum TE, Larson EL (2012) A review of antibiotic use in food animals: perspective, policy, and potential. Public Health Rep 127(1):4–22. https://doi.org/10.1177/003335491212700103
Larsen J, Petersen A, Sørum M, Stegger M, van Alphen L, Valentiner-Branth P et al (2015) Meticillin-resistant Staphylococcus aureus CC398 is an increasing cause of disease in people with no livestock contact in Denmark, 1999 to 2011. Euro Surveill 20(37). https://doi.org/10.2807/1560-7917.Es.2015.20.37.30021
Leijon M, Atkins E, Persson Waller K, Artursson K (2021) Longitudinal study of Staphylococcus aureus genotypes isolated from bovine clinical mastitis. J Dairy Sci 104(11):11945–11954. https://doi.org/10.3168/jds.2021-20562
Lim SK, Nam HM, Jang GC, Lee HS, Jung SC, Kwak HS (2012) The first detection of methicillin-resistant Staphylococcus aureus ST398 in pigs in Korea. Vet Microbiol 155(1):88–92. https://doi.org/10.1016/j.vetmic.2011.08.011
Lim SK, Nam HM, Jang GC, Lee HS, Jung SC, Kim TS (2013) Transmission and persistence of methicillin-resistant Staphylococcus aureus in milk, environment, and workers in dairy cattle farms. Foodborne Pathog Dis 10(8):731–736. https://doi.org/10.1089/fpd.2012.1436
Luini M, Cremonesi P, Magro G, Bianchini V, Minozzi G, Castiglioni B et al (2015) Methicillin-resistant Staphylococcus aureus (MRSA) is associated with low within-herd prevalence of intra-mammary infections in dairy cows: genotyping of isolates. Vet Microbiol 178(3-4):270–274. https://doi.org/10.1016/j.vetmic.2015.05.010
Luzzago C, Locatelli C, Franco A, Scaccabarozzi L, Gualdi V, Viganò R et al (2014) Clonal diversity, virulence-associated genes and antimicrobial resistance profile of Staphylococcus aureus isolates from nasal cavities and soft tissue infections in wild ruminants in Italian Alps. Vet Microbiol 170(1-2):157–161. https://doi.org/10.1016/j.vetmic.2014.01.016
Malachowa N, Sabat A, Gniadkowski M, Krzyszton-Russjan J, Empel J, Miedzobrodzki J et al (2005) Comparison of multiple-locus variable-number tandem-repeat analysis with pulsed-field gel electrophoresis, spa typing, and multilocus sequence typing for clonal characterization of Staphylococcus aureus isolates. J Clin Microbiol 43(7):3095–3100. https://doi.org/10.1128/jcm.43.7.3095-3100.2005
Malachowa N, Kobayashi SD, Porter AR, Braughton KR, Scott DP, Gardner DJ et al (2016) Contribution of Staphylococcus aureus coagulases and clumping factor A to abscess formation in a rabbit model of skin and soft tissue infection. PLoS One 11(6):e0158293. https://doi.org/10.1371/journal.pone.0158293
Matuszewska M, Murray GGR, Ba X, Wood R, Holmes MA, Weinert LA (2022) Stable antibiotic resistance and rapid human adaptation in livestock-associated MRSA. Elife 11:e74819. https://doi.org/10.7554/eLife.74819
Milheiriço C, Oliveira DC, de Lencastre H (2007) Multiplex PCR strategy for subtyping the staphylococcal cassette chromosome mec type IV in methicillin-resistant Staphylococcus aureus: 'SCCmec IV multiplex'. J Antimicrob Chemother 60(1):42–48. https://doi.org/10.1093/jac/dkm112
Mlynarczyk-Bonikowska B, Kowalewski C, Krolak-Ulinska A, Marusza W (2022) Molecular mechanisms of drug resistance in Staphylococcus aureus. Int J Mol Sci 23(15):8088. https://doi.org/10.3390/ijms23158088
Moon BY, Park JY, Hwang SY, Robinson DA, Thomas JC, Fitzgerald JR et al (2015) Phage-mediated horizontal transfer of a Staphylococcus aureus virulence-associated genomic island. Sci Rep 5:9784. https://doi.org/10.1038/srep09784
Moon DC, Jeong SK, Hyun BH, Lim SK (2019) Prevalence and characteristics of methicillin-resistant Staphylococcus aureus isolates in pigs and pig farmers in Korea. Foodborne Pathog Dis 16(4):256–261. https://doi.org/10.1089/fpd.2018.2509
Mork RL, Hogan PG, Muenks CE, Boyle MG, Thompson RM, Sullivan ML et al (2020) Longitudinal, strain-specific Staphylococcus aureus introduction and transmission events in households of children with community-associated meticillin-resistant S aureus skin and soft tissue infection: a prospective cohort study. Lancet Infect Dis 20(2):188–198. https://doi.org/10.1016/s1473-3099(19)30570-5
Müller A, Seinige D, Jansen W, Klein G, Ehricht R, Monecke S et al (2016) Variety of antimicrobial resistances and virulence factorS in Staphylococcus aureus isolates from meat products legally and illegally introduced to Germany. PLoS One 11(12):e0167864. https://doi.org/10.1371/journal.pone.0167864
Nakaminami H, Kawasaki H, Takadama S, Kaneko H, Suzuki Y, Maruyama H et al (2021) Possible dissemination of a Panton-Valentine leukocidin-positive livestock-associated methicillin-resistant Staphylococcus aureus CC398 clone in Tokyo, Japan. Jpn J Infect Dis 74(1):82–84. https://doi.org/10.7883/yoken.JJID.2020.345
Neela V, Mohd Zafrul A, Mariana NS, van Belkum A, Liew YK, Rad EG (2009) Prevalence of ST9 methicillin-resistant Staphylococcus aureus among pigs and pig handlers in Malaysia. J Clin Microbiol 47(12):4138–4140. https://doi.org/10.1128/jcm.01363-09
Nemeghaire S, Argudín MA, Haesebrouck F, Butaye P (2014) Epidemiology and molecular characterization of methicillin-resistant Staphylococcus aureus nasal carriage isolates from bovines. BMC Vet Res 10:153. https://doi.org/10.1186/1746-6148-10-153
Nübel U, Roumagnac P, Feldkamp M, Song JH, Ko KS, Huang YC et al (2008) Frequent emergence and limited geographic dispersal of methicillin-resistant Staphylococcus aureus. Proc Natl Acad Sci U S A 105(37):14130–14135. https://doi.org/10.1073/pnas.0804178105
Oliver JP, Gooch CA, Lansing S, Schueler J, Hurst JJ, Sassoubre L et al (2020) Invited review: fate of antibiotic residues, antibiotic-resistant bacteria, and antibiotic resistance genes in US dairy manure management systems. J Dairy Sci 103(2):1051–1071. https://doi.org/10.3168/jds.2019-16778
Osadebe LU, Hanson B, Smith TC, Heimer R (2013) Prevalence and characteristics of Staphylococcus aureus in Connecticut swine and swine farmers. Zoonoses Public Health 60(3):234–243. https://doi.org/10.1111/j.1863-2378.2012.01527.x
Otter JA, Kearns AM, French GL, Ellington MJ (2010) Panton-Valentine leukocidin-encoding bacteriophage and gene sequence variation in community-associated methicillin-resistant Staphylococcus aureus. Clin Microbiol Infect 16(1):68–73. https://doi.org/10.1111/j.1469-0691.2009.02925.x
Park S, Jung D, O'Brien B, Ruffini J, Dussault F, Dube-Duquette A et al (2022) Comparative genomic analysis of Staphylococcus aureus isolates associated with either bovine intramammary infections or human infections demonstrates the importance of restriction-modification systems in host adaptation. Microb Genom 8(2). https://doi.org/10.1099/mgen.0.000779
Penadés JR, Chen J, Quiles-Puchalt N, Carpena N, Novick RP (2015) Bacteriophage-mediated spread of bacterial virulence genes. Curr Opin Microbiol 23:171–178. https://doi.org/10.1016/j.mib.2014.11.019
Pérez-Moreno MO, Centelles-Serrano MJ, Nogales-López J, Domenech-Spanedda MF, Lozano C, Torres C (2017) Unusual presence of the immune evasion gene cluster in livestock-associated MRSA of lineage CC398 causing peridural and psoas abscesses in a poultry farmer. Enferm Infecc Microbiol Clin 35(10):651–654. https://doi.org/10.1016/j.eimc.2016.07.008
Petersen A, Stegger M, Heltberg O, Christensen J, Zeuthen A, Knudsen LK et al (2013) Epidemiology of methicillin-resistant Staphylococcus aureus carrying the novel mecC gene in Denmark corroborates a zoonotic reservoir with transmission to humans. Clin Microbiol Infect 19(1):E16–e22. https://doi.org/10.1111/1469-0691.12036
Porrero MC, Wassenaar TM, Gómez-Barrero S, García M, Bárcena C, Alvarez J et al (2012) Detection of methicillin-resistant Staphylococcus aureus in Iberian pigs. Lett Appl Microbiol 54(4):280–285. https://doi.org/10.1111/j.1472-765X.2012.03207.x
Price LB, Stegger M, Hasman H, Aziz M, Larsen J, Andersen PS et al (2012) Staphylococcus aureus CC398: host adaptation and emergence of methicillin resistance in livestock. mBio 3(1):10–128. https://doi.org/10.1128/mBio.00305-11
Purrello SM, Daum RS, Edwards GF, Lina G, Lindsay J, Peters G et al (2014) Meticillin-resistant Staphylococcus aureus (MRSA) update: new insights into bacterial adaptation and therapeutic targets. J Glob Antimicrob Resist 2(2):61–69. https://doi.org/10.1016/j.jgar.2014.02.003
Randad PR, Larsen J, Kaya H, Pisanic N, Ordak C, Price LB et al (2021) Transmission of antimicrobial-resistant Staphylococcus aureus Clonal Complex 9 between pigs and humans, United States. Emerg Infect Dis 27(3):740–748. https://doi.org/10.3201/eid2703.191775
Rao S, Linke L, Magnuson R, Jauch L, Hyatt DR (2022) Antimicrobial resistance and genetic diversity of Staphylococcus aureus collected from livestock, poultry and humans. One Health 15:100407. https://doi.org/10.1016/j.onehlt.2022.100407
Ren Q, Liao G, Wu Z, Lv J, Chen W (2020) Prevalence and characterization of Staphylococcus aureus isolates from subclinical bovine mastitis in southern Xinjiang, China. J Dairy Sci 103(4):3368–3380. https://doi.org/10.3168/jds.2019-17420
Resch G, François P, Morisset D, Stojanov M, Bonetti EJ, Schrenzel J et al (2013) Human-to-bovine jump of Staphylococcus aureus CC8 is associated with the loss of a β-hemolysin converting prophage and the acquisition of a new staphylococcal cassette chromosome. PLoS One 8(3):e58187. https://doi.org/10.1371/journal.pone.0058187
Roberts GA, Houston PJ, White JH, Chen K, Stephanou AS, Cooper LP et al (2013) Impact of target site distribution for Type I restriction enzymes on the evolution of methicillin-resistant Staphylococcus aureus (MRSA) populations. Nucleic Acids Res 41(15):7472–7484. https://doi.org/10.1093/nar/gkt535
Rosen K, Roesler U, Merle R, Friese A (2018) Persistent and transient airborne MRSA colonization of piglets in a newly established animal model. Front Microbiol 9:1542. https://doi.org/10.3389/fmicb.2018.01542
Ruiz-Ripa L, Bellés-Bellés A, Fernández-Fernández R, García M, Vilaró A, Zarazaga M et al (2021) Linezolid-resistant MRSA-CC398 carrying the cfr gene, and MRSA-CC9 isolates from pigs with signs of infection in Spain. J Appl Microbiol 131(2):615–622. https://doi.org/10.1111/jam.14988
Sahibzada S, Abraham S, Coombs GW, Pang S, Hernández-Jover M, Jordan D et al (2017) Transmission of highly virulent community-associated MRSA ST93 and livestock-associated MRSA ST398 between humans and pigs in Australia. Sci Rep 7(1):5273. https://doi.org/10.1038/s41598-017-04789-0
Salgado-Pabón W, Herrera A, Vu BG, Stach CS, Merriman JA, Spaulding AR et al (2014) Staphylococcus aureus β-toxin production is common in strains with the β-toxin gene inactivated by bacteriophage. J Infect Dis 210(5):784–792. https://doi.org/10.1093/infdis/jiu146
Salgueiro V, Manageiro V, Bandarra NM, Ferreira E, Clemente L, Caniça M (2020) Genetic relatedness and diversity of Staphylococcus aureus from different reservoirs: humans and animals of livestock, poultry, zoo, and aquaculture. Microorganisms 8(9):1345. https://doi.org/10.3390/microorganisms8091345
Saud B, Khatri G, Amatya N, Paudel G, Shrestha V (2023) Methicillin-resistant and biofilm-producing Staphylococcus aureus in nasal carriage among health care workers and medical students. Can J Infect Dis Med Microbiol 2023:8424486. https://doi.org/10.1155/2023/8424486
Schijffelen MJ, Boel CH, van Strijp JA, Fluit AC (2010) Whole genome analysis of a livestock-associated methicillin-resistant Staphylococcus aureus ST398 isolate from a case of human endocarditis. BMC Genomics 11:376. https://doi.org/10.1186/1471-2164-11-376
Schürch AC, Arredondo-Alonso S, Willems RJL, Goering RV (2018) Whole genome sequencing options for bacterial strain typing and epidemiologic analysis based on single nucleotide polymorphism versus gene-by-gene-based approaches. Clin Microbiol Infect 24(4):350–354. https://doi.org/10.1016/j.cmi.2017.12.016
Sieber RN, Larsen AR, Urth TR, Iversen S, Møller CH, Skov RL et al (2019) Genome investigations show host adaptation and transmission of LA-MRSA CC398 from pigs into Danish healthcare institutions. Sci Rep 9(1):18655. https://doi.org/10.1038/s41598-019-55086-x
Sieber RN, Urth TR, Petersen A, Møller CH, Price LB, Skov RL et al (2020) Phage-mediated immune evasion and transmission of livestock-associated methicillin-resistant Staphylococcus aureus in humans. Emerg Infect Dis 26(11):2578–2585. https://doi.org/10.3201/eid2611.201442
Silva V, Capelo JL, Igrejas G, Poeta P (2020a) Molecular epidemiology of Staphylococcus aureus lineages in wild animals in Europe: a review. Antibiotics (Basel) 9(3):122. https://doi.org/10.3390/antibiotics9030122
Silva V, Sousa T, Gómez P, Sabença C, Vieira-Pinto M, Capita R et al (2020b) Livestock-associated methicillin-resistant Staphylococcus aureus (MRSA) in purulent subcutaneous lesions of farm rabbits. Foods 9(4):439. https://doi.org/10.3390/foods9040439
Simpson VR, Davison NJ, Kearns AM, Pichon B, Hudson LO, Koylass M et al (2013) Association of a lukM-positive clone of Staphylococcus aureus with fatal exudative dermatitis in red squirrels (Sciurus vulgaris). Vet Microbiol 162(2-4):987–991. https://doi.org/10.1016/j.vetmic.2012.10.025
Sineke N, Asante J, Amoako DG, Abia ALK, Perrett K, Bester LA et al (2021) Staphylococcus aureus in intensive pig production in South Africa: antibiotic resistance, virulence determinants, and clonality. Pathogens 10(3):317. https://doi.org/10.3390/pathogens10030317
Smith TC, Pearson N (2011) The emergence of Staphylococcus aureus ST398. Vector Borne Zoonotic Dis 11(4):327–339. https://doi.org/10.1089/vbz.2010.0072
Smith TC, Thapaliya D, Bhatta S, Mackey S, Engohang-Ndong J, Carrel M (2018) Geographic distribution of livestock-associated Staphylococcus aureus in the United States. Microbes Infect 20(6):323–327. https://doi.org/10.1016/j.micinf.2018.05.004
Snyder HL, Niebuhr SE, Dickson JS (2013) Transfer of methicillin-resistant Staphylococcus aureus from retail pork products onto food contact surfaces and the potential for consumer exposure. J Food Prot 76(12):2087–2092. https://doi.org/10.4315/0362-028x.Jfp-13-143
Sonola VS, Misinzo G, Matee MI (2021) Occurrence of multidrug-resistant Staphylococcus aureus among humans, rodents, chickens, and household soils in Karatu, Northern Tanzania. Int J Environ Res Public Health 18(16). https://doi.org/10.3390/ijerph18168496
Spoor LE, McAdam PR, Weinert LA, Rambaut A, Hasman H, Aarestrup FM et al (2013) Livestock origin for a human pandemic clone of community-associated methicillin-resistant Staphylococcus aureus. mBio 4(4):10–128. https://doi.org/10.1128/mBio.00356-13
Stegger M, Lindsay JA, Moodley A, Skov R, Broens EM, Guardabassi L (2011) Rapid PCR detection of Staphylococcus aureus clonal complex 398 by targeting the restriction-modification system carrying sau1-hsdS1. J Clin Microbiol 49(2):732–734. https://doi.org/10.1128/JCM.01970-10
Stegger M, Aziz M, Chroboczek T, Price LB, Ronco T, Kiil K et al (2013) Genome analysis of Staphylococcus aureus ST291, a double locus variant of ST398, reveals a distinct genetic lineage. PLoS One 8(5):e63008. https://doi.org/10.1371/journal.pone.0063008
Sun J, Liao XP, D'Souza AW, Boolchandani M, Li SH, Cheng K et al (2020) Environmental remodeling of human gut microbiota and antibiotic resistome in livestock farms. Nat Commun 11(1):1427. https://doi.org/10.1038/s41467-020-15222-y
Suzuki H, Lefébure T, Bitar PP, Stanhope MJ (2012) Comparative genomic analysis of the genus Staphylococcus including Staphylococcus aureus and its newly described sister species Staphylococcus simiae. BMC Genomics 13:38. https://doi.org/10.1186/1471-2164-13-38
Thwala T, Madoroba E, Basson A, Butaye P (2021) Prevalence and characteristics of Staphylococcus aureus associated with meat and meat products in African countries: a review. Antibiotics (Basel) 10(9):1108. https://doi.org/10.3390/antibiotics10091108
Tiseo K, Huber L, Gilbert M, Robinson TP, Van Boeckel TP (2020) Global trends in antimicrobial use in food animals from 2017 to 2030. Antibiotics (Basel) 9(12):918. https://doi.org/10.3390/antibiotics9120918
Tong C, Xiao D, Xie L, Yang J, Zhao R, Hao J et al (2022) Swine manure facilitates the spread of antibiotic resistome including tigecycline-resistant tet(X) variants to farm workers and receiving environment. Sci Total Environ 808:152157. https://doi.org/10.1016/j.scitotenv.2021.152157
van Cleef BA, Graveland H, Haenen AP, van de Giessen AW, Heederik D, Wagenaar JA et al (2011) Persistence of livestock-associated methicillin-resistant Staphylococcus aureus in field workers after short-term occupational exposure to pigs and veal calves. J Clin Microbiol 49(3):1030–1033. https://doi.org/10.1128/jcm.00493-10
Vandendriessche S, Vanderhaeghen W, Larsen J, de Mendonça R, Hallin M, Butaye P et al (2014) High genetic diversity of methicillin-susceptible Staphylococcus aureus (MSSA) from humans and animals on livestock farms and presence of SCCmec remnant DNA in MSSA CC398. J Antimicrob Chemother 69(2):355–362. https://doi.org/10.1093/jac/dkt366
Verhoeven PO, Gagnaire J, Botelho-Nevers E, Grattard F, Carricajo A, Lucht F et al (2014) Detection and clinical relevance of Staphylococcus aureus nasal carriage: an update. Expert Rev Anti Infect Ther 12(1):75–89. https://doi.org/10.1586/14787210.2014.859985
Voss A, Loeffen F, Bakker J, Klaassen C, Wulf M (2005) Methicillin-resistant Staphylococcus aureus in pig farming. Emerg Infect Dis 11(12):1965–1966. https://doi.org/10.3201/eid1112.050428
Waldron DE, Lindsay JA (2006) Sau1: a novel lineage-specific type I restriction-modification system that blocks horizontal gene transfer into Staphylococcus aureus and between S. aureus isolates of different lineages. J Bacteriol 188(15):5578–5585. https://doi.org/10.1128/JB.00418-06
Wan MT, Lauderdale TL, Chou CC (2013) Characteristics and virulence factors of livestock associated ST9 methicillin-resistant Staphylococcus aureus with a novel recombinant staphylocoagulase type. Vet Microbiol 162(2-4):779–784. https://doi.org/10.1016/j.vetmic.2012.10.003
Wang D, Wang Z, Yan Z, Wu J, Ali T, Li J et al (2015) Bovine mastitis Staphylococcus aureus: antibiotic susceptibility profile, resistance genes and molecular typing of methicillin-resistant and methicillin-sensitive strains in China. Infect Genet Evol 31:9–16. https://doi.org/10.1016/j.meegid.2014.12.039
Wang W, Lin X, Jiang T, Peng Z, Xu J, Yi L et al (2018) Prevalence and characterization of Staphylococcus aureus cultured from raw milk taken from dairy cows with mastitis in Beijing, China. Front Microbiol 9:1123. https://doi.org/10.3389/fmicb.2018.01123
Wassenberg MW, Bootsma MC, Troelstra A, Kluytmans JA, Bonten MJ (2011) Transmissibility of livestock-associated methicillin-resistant Staphylococcus aureus (ST398) in Dutch hospitals. Clin Microbiol Infect 17(2):316–319. https://doi.org/10.1111/j.1469-0691.2010.03260.x
Weterings V, Bosch T, Witteveen S, Landman F, Schouls L, Kluytmans J (2017) Next-generation sequence analysis reveals transfer of methicillin resistance to a methicillin-susceptible Staphylococcus aureus strain that subsequently caused a methicillin-resistant Staphylococcus aureus outbreak: a descriptive study. J Clin Microbiol 55(9):2808–2816. https://doi.org/10.1128/jcm.00459-17
Wulf MW, Sørum M, van Nes A, Skov R, Melchers WJ, Klaassen CH et al (2008) Prevalence of methicillin-resistant Staphylococcus aureus among veterinarians: an international study. Clin Microbiol Infect 14(1):29–34. https://doi.org/10.1111/j.1469-0691.2007.01873.x
Xie X, Bao Y, Ouyang N, Dai X, Pan K, Chen B et al (2016) Molecular epidemiology and characteristic of virulence gene of community-acquired and hospital-acquired methicillin-resistant Staphylococcus aureus isolates in Sun Yat-sen Memorial hospital, Guangzhou, Southern China. BMC Infect Dis 16:339. https://doi.org/10.1186/s12879-016-1684-y
Yadav R, Kumar A, Singh VK, Yadav SK (2018) Prevalence and antibiotyping of Staphylococcus aureus and methicillin-resistant S. aureus (MRSA) in domestic animals in India. J Glob Antimicrob Resist 15:222–225. https://doi.org/10.1016/j.jgar.2018.08.001
Yan J, Yang R, Yu S, Zhao W (2021) The application of the lytic domain of endolysin from Staphylococcus aureus bacteriophage in milk. J Dairy Sci 104(3):2641–2653. https://doi.org/10.3168/jds.2020-19456
Yu F, Cienfuegos-Gallet AV, Cunningham MH, Jin Y, Wang B, Kreiswirth BN et al (2021) Molecular evolution and adaptation of livestock-associated methicillin-resistant Staphylococcus aureus (LA-MRSA) sequence Type 9. mSystems 6(3) e0049221. https://doi.org/10.1128/mSystems.00492-21
Zhang YJ, Hu HW, Chen QL, Singh BK, Yan H, Chen D et al (2019) Transfer of antibiotic resistance from manure-amended soils to vegetable microbiomes. Environ Int 130:104912. https://doi.org/10.1016/j.envint.2019.104912
Zoppi S, Dondo A, Di Blasio A, Vitale N, Carfora V, Goria M et al (2021) Livestock-associated methicillin-resistant Staphylococcus aureus and related risk factors in holdings of veal calves in Northwest Italy. Microb Drug Resist 27(8):1136–1143. https://doi.org/10.1089/mdr.2020.0226
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All authors contributed to the study conception and design. Conceptualization, Ying Wang, Peihua Zhang and Haiyan Yang; methodology, Ying Wang, Peihua Zhang and Shuaiyin Chen; software, Peihua Zhang and Jian Wu; writing-original draft preparation, Ying Wang and Peihua Zhang; writing-review and editing, Ying Wang, Jian Wu and Haiyan Yang; visualization, Ying Wang, Peihua Zhang, Yuefei Jin and Jinzhao Long; supervision, Haiyan Yang and Guangcai Duan; project administration, Haiyan Yang; funding acquisition, Haiyan Yang.
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Wang, ., Zhang, P., Wu, J. et al. Transmission of livestock-associated methicillin-resistant Staphylococcus aureus between animals, environment, and humans in the farm. Environ Sci Pollut Res 30, 86521–86539 (2023). https://doi.org/10.1007/s11356-023-28532-7
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DOI: https://doi.org/10.1007/s11356-023-28532-7