Molecular characterization of methicillin-resistant Staphylococcus aureus isolated from the pig production chain in Northern Italy
https://doi.org/10.4081/ijfs.2020.8412
Accepted: 28 November 2019
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This study aimed to evaluate the molecular characteristics of methicillin resistant Staphylococcus aureus (MRSA) isolated in the swine chain in Northern Italy. A sample of 50 fattening units located in Lombardy was selected. Five cutaneous samples at slaughtering and three environmental samples at farm were collected from each unit giving a total of 250 and 150 samples, respectively. A total of 25 MRSA isolates were isolated from 400 samples, in 17 different fattening units. At farm, 12 out of 250 samples were positive for MRSA (4,8 %), and 13 out of 150 samples at slaughter were identified as MRSA (8,7 %), giving an overall incidence among samples of 6,25 % (n = 25). Molecular characterization was carried out using multi-locus sequence typing (MLST) and spa-typing. Outcomes showed that most of the isolates belonged to ST398, carrying spa-types t899, t011, t18498, t1939, t1200, and t304. Nonetheless, three isolates were identified as ST97 (t1730 and t4795), and one as ST30, showing spa-type t318. Furthermore, a novel ST was identified, namely 5422, showing spa-type t1730. Heterogeneity in genotypes within the same farm was also found in different fattening units, with concern for the possibility of the exchange of genetic determinants among different lineages. Genetic diversity among MRSA isolates in pig fattening units has been observed, highlighting the possibility that some isolates could be able to infect different hosts, including human.
Abdelbary, M. M. H., Basset, P., Blanc, D. S., & Feil, E. J. (2017). The Evolution and Dynamics of Methicillin-Resistant Staphylococcus aureus. In Genetics and Evolution of Infectious Diseases: Second Edition.
Aires-de-Sousa M, 2017. Methicillin-resistant Staphylococcus aureus among animals: current overview. Clin Microbiol Infect 23:373–380.
Alkharsah KR, Rehman S, Alnimr A, Diab A, Hawwari A, Tokajian S, 2018. Molecular typing of MRSA isolates by spa and PFGE. J King Saud Univ - Sci
Battisti A, Franco A, Merialdi G, Hasman H, Iurescia M, Lorenzetti R, Feltrin F, Zini M, Aarestrup FM, 2010. Heterogeneity among methicillin-resistant Staphylococcus aureus from Italian pig fattening holdings. Vet Microbiol 142:361–366.
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:e6800.
Doulgeraki AI, Di Ciccio PA, Ianieri A, Nychas G-JE, 2016. Methicillin-resistant food-related Staphylococcus aureus: a review of current knowledge and biofilm formation for future studies and applications. Res Microbiol 168:1–15.
European Food Safety Authority (EFSA), 2009a. Analysis of the baseline survey on the prevalence of methicillin-resistant Staphylococcus aureus (MRSA) in holdings with breeding pigs, in the EU, 2008 - Part A: MRSA prevalence estimates. EFSA J 7:1376.
European Food Safety Authority (EFSA), 2009b. Assessment of the Public Health significance of meticillin resistant Staphylococcus aureus (MRSA) in animals and foods. EFSA J 7:.
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.
Jiang W, Zhou Z, Zhang K, Yu Y, 2013. Epidemiological investigation of community-acquired Staphylococcus aureus infection. Genet Mol Res 12:6923–6930.
Lassok B, Tenhagen B-A, 2013. From pig to pork: Methicillin-resistant Staphylococcus aureus in the pork production chain. J Food Prot 76:1095–1108.
Locatelli C, Cremonesi P, Caprioli A, Carfora V, Ianzano A, Barberio A, Morandi S, Casula A, Castiglioni B, Bronzo V, Moroni P, 2017. Occurrence of methicillin-resistant Staphylococcus aureus in dairy cattle herds, related swine farms, and humans in contact with herds. J Dairy Sci 100:608–619.
Normanno G, Dambrosio A, Lorusso V, Samoilis G, Di Taranto P, Parisi A, 2015. Methicillin-resistant Staphylococcus aureus (MRSA) in slaughtered pigs and abattoir workers in Italy. Food Microbiol 51:51-56
Oniciuc, E. A., Nicolau, A. I., Hernández, M., Rodríguez-Lázaro, D. (2017). Presence of methicillin-resistant Staphylococcus aureus in the food chain. Trends in Food Science and Technology, 61, 49–59.
Pan A, Battisti A, Zoncada A, Bernieri F, Boldini M, Franco A, Giorgi M, Iurescia M, Lorenzotti S, Martinotti M, Monaci M, Pantosti A, 2009. Community-acquired methicillin-resistant Staphylococcus aureus ST398 infection, Italy. Emerg Infect Dis 15:845–7.
Parisi A, Caruso M, Normanno G, Latorre L, Miccolupo A, Fraccalvieri R, Intini F, Manginelli T, Santagada G, 2019. MRSA in swine, farmers and abattoir workers in Southern Italy. Food Microbiol 82:287–293.
Petternel C, Galler H, Zarfel G, Luxner J, Haas D, Grisold AJ, Reinthaler FF, Feierl G, 2014. Isolation and characterization of multidrug-resistant bacteria from minced meat in Austria. Food Microbiol 44:41–46.
Pichon B, Hill R, Laurent F, Larsen AR, Skov RL, Holmes M, Edwards GF, Teale C, Kearns AM, 2012. Development of a real-time quadruplex PCR assay for simultaneous detection of nuc, panton-valentine leucocidin (PVL), mecA and homologue mecALGA251. J Antimicrob Chemother 67:2338–2341.
Rájová J, Pantůček R, Petráš P, Varbanovová I, Mašlaňová I, Beneš J, 2016. Necrotizing pneumonia due to clonally diverse Staphylococcus aureus strains producing Panton-Valentine leukocidin: the Czech experience. Epidemiol Infect 144:507–515.
Raphael N. Sieber, Robert L. Skov, Jens Nielsen, Jana Schulz, Lance B. Price, Anders R. Larsen, Marc Stegger (2018). Drivers and Dynamics of Methicillin-Resistant Livestock- Associated Staphylococcus aureus CC398 in Pigs and Humans in Denmark. 9(November/December), 1–12.
Shopsin B, Gomez M, Montgomery SO, Smith DH, Waddington M, Dodge DE, Bost DA, Riehman M, Naidich S, Kreiswirth BN, 1999. Evaluation of protein A gene polymorphic region DNA sequencing for typing of Staphylococcus aureus strains. J Clin Microbiol 37:3556–3563.
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S, 2013. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol 30:2725-2729.
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.
Taylor AR, 2013. Methicillin-resistant Staphylococcus aureus infections. Prim Care – Clin Off Pract 40:637-654
Van den Broek IVF, Van Cleef BAGL, Haenen A, Broens EM, Van der Wolf PJ, Van den Broek MJM, Huijsdens XW, Kluytmans JAJW, Van de Giessen AW, Tiemersma EW, 2009. Methicillin-resistant Staphylococcus aureus in people living and working in pig farms. Epidemiol Infect 137:700.
Van Cleef BAGL, Broens EMEM, Voss A, Huijsdens XW, Züchner L, Van Benthem BHB, Kluytmans JAJW, Mulders MN, Van De Giessen AW, 2010. High prevalence of nasal MRSA carriage in slaughterhouse workers in contact with live pigs in The Netherlands. Epidemiol Infect 138:756.
Van Duijkeren E, Ikawaty R, Broekhuizen-Stins MJ, Jansen MD, Spalburg EC, Neeling AJ de, Allaart JG, van Nes A, Wagenaar JA, Fluit AC, 2008. Transmission of methicillin-resistant Staphylococcus aureus strains between different kinds of pig farms. Vet Microbiol 126:383–389.
Verhegghe M, Pletinckx LJ, Crombé F, Vandersmissen T, Haesebrouck F, Butaye P, Heyndrickx M, Rasschaert G, 2013. Methicillin-resistant Staphylococcus aureus (MRSA) ST398 in pig farms and multispecies farms. Zoonoses Public Health 60:366–374.
Zarazaga M, Gómez P, Ceballos S, Torres C, 2017. Molecular epidemiology of Staphylococcus aureus lineages in the animal–human interface. In: Fetsch A., ed. Staphylococcus aureus. Academic Press, Cambridge, MA, pp 189-214.
Zehra A, Gulzar M, Singh R, Kaur S, Gill JPS, 2019. Prevalence, multidrug resistance and molecular typing of methicillin-resistant Staphylococcus aureus (MRSA) in retail meat from Punjab, India. J Glob Antimicrob Resist 16:152–158.
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This project has been chartered by the Italian Ministry of Health, project “Classyfarm”.PAGEPress has chosen to apply the Creative Commons Attribution NonCommercial 4.0 International License (CC BY-NC 4.0) to all manuscripts to be published.
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