Methicillin-resistant Staphylococcus aureus among animals: current overview

Clinical Microbiology and Infection

Volumn 23, Issue 6, 2017, Pages 373-380

  Aires de Sousa, M ^a  

^a Portuguese Red Cross Higher Health School   (Portugal)

Author keywords

Animal adapted S. aureus strains; Animals; CC398; Livestock associated methicillin resistant S. aureus; mecC; Methicillin resistant S. aureus; Staphylococcus aureus; Transmission from animals to humans

Indexed keywords

VIRULENCE FACTOR;

BACTERIAL COLONIZATION; BACTERIAL STRAIN; CLONE; COMMUNITY ACQUIRED INFECTION; DOMESTICATION; EXPOSURE; FOOD CHAIN; GEOGRAPHIC DISTRIBUTION; HOSPITAL INFECTION; HUMAN; LIVESTOCK; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; NONHUMAN; PATHOGENICITY; PET ANIMAL; PRIORITY JOURNAL; REVIEW; WILDLIFE; ZOONOSIS; AFRICA; ANIMAL; ASIA; AUSTRALIA; CLASSIFICATION; EUROPE; FOOD CONTROL; GENETICS; ISOLATION AND PURIFICATION; MICROBIOLOGY; PHYLOGEOGRAPHY; STAPHYLOCOCCUS INFECTION; VETERINARY;

AFRICA; ANIMALS; ASIA; AUSTRALIA; EUROPE; FOOD MICROBIOLOGY; LIVESTOCK; METHICILLIN-RESISTANT STAPHYLOCOCCUS AUREUS; PETS; PHYLOGEOGRAPHY; STAPHYLOCOCCAL INFECTIONS;

EID: 85008205737     PISSN: 1198743X     EISSN: 14690691     Source Type: Journal    
DOI: 10.1016/j.cmi.2016.11.002     Document Type: Review

References (66)

1. Oliveira, D.C., Tomasz, A., de Lencastre, H., Secrets of success of a human pathogen: molecular evolution of pandemic clones of methicillin-resistant Staphylococcus aureus. Lancet Infect Dis 2 (2002), 180–189.
2. Enright, M.C., The evolution of a resistant pathogen-the case of MRSA. Curr Opin Pharmacol 3 (2003), 474–479.
3. Grundmann, H., Schouls, L.M., Aanensen, D.M., Pluister, G.N., Tami, A., Chlebowicz, M., et al. The dynamic changes of dominant clones of Staphylococcus aureus causing bloodstream infections in the European region: results of a second structured survey. Euro Surveill, 19, 2014.
4. Aanensen, D.M., Feil, E.J., Holden, M.T., Dordel, J., Yeats, C.A., Fedosejev, A., et al. Whole-genome sequencing for routine pathogen surveillance in public health: a population snapshot of invasive Staphylococcus aureus in Europe. mBio, 7, 2016.
5. Rodriguez-Noriega, E., Seas, C., Guzman-Blanco, M., Mejia, C., Alvarez, C., Bavestrello, L., et al. Evolution of methicillin-resistant Staphylococcus aureus clones in Latin America. Int J Infect Dis 14 (2010), e560–e566.
6. Chen, C.J., Huang, Y.C., New epidemiology of Staphylococcus aureus infection in Asia. Clin Microbiol Infect 20 (2014), 605–623.
7. Abdulgader, S.M., Shittu, A.O., Nicol, M.P., Kaba, M., Molecular epidemiology of methicillin-resistant Staphylococcus aureus in Africa: a systematic review. Front Microbiol, 6, 2015, 348.
8. Coombs, G., Pearson, J., Christiansen, K., Nimmo, G., Staphylococcus aureus programme 2010 (SAP 2010). Community survey. MRSA epidemiology and typing report on behalf of the Australian Group for Antimicrobial Resistance (AGAR). 2011 http://www.agargroup.org/files/FED%20REPORT%20SAP210%20MRSA%20FINAL%20shrink.pdf.
9. CDC, Four pediatric deaths from community-acquired methicillin-resistant Staphylococcus aureus—Minnesota and North Dakota, 1997–1999. Morb Mortal Wkly Rep 48 (1999), 707–710.
10. Planet, P.J., Diaz, L., Kolokotronis, S.O., Narechania, A., Reyes, J., Xing, G., et al. Parallel epidemics of community-associated methicillin-resistant Staphylococcus aureus USA300 infection in North and South America. J Infect Dis 212 (2015), 1874–1882.
11. Diekema, D.J., Richter, S.S., Heilmann, K.P., Dohrn, C.L., Riahi, F., Tendolkar, S., et al. Continued emergence of USA300 methicillin-resistant Staphylococcus aureus in the United States: results from a nationwide surveillance study. Infect Control Hosp Epidemiol 35 (2014), 285–292.
12. Tavares, A., Miragaia, M., Rolo, J., Coelho, C., de Lencastre, H., group C-MMw. High prevalence of hospital-associated methicillin-resistant Staphylococcus aureus (HA-MRSA) in the community in Portugal: evidence for the blurring of community-hospital boundaries. Eur J Clin Microbiol Infect Dis 32 (2013), 1269–1283.
13. Conceição, T., Diamantino, F., Coelho, C., de Lencastre, H., Aires-de-Sousa, M., Contamination of public buses with MRSA in Lisbon Portugal: a possible transmission route of major MRSA clones within the community. PLoS One, 8, 2013, e77812.
14. Simoes, R.R., Aires-de-Sousa, M., Conceicao, T., Antunes, F., da Costa, P.M., de Lencastre, H., High prevalence of EMRSA-15 in Portuguese public buses: a worrisome finding. PLoS One, 6, 2011, e17630.
15. Malik, S., Coombs, G.W., O'Brien, F.G., Peng, H., Barton, M.D., Molecular typing of methicillin-resistant staphylococci isolated from cats and dogs. J Antimicrob Chemother 58 (2006), 428–431.
16. Wedley, A.L., Dawson, S., Maddox, T.W., Coyne, K.P., Pinchbeck, G.L., Clegg, P., et al. Carriage of Staphylococcus species in the veterinary visiting dog population in mainland UK: molecular characterisation of resistance and virulence. Vet Microbiol 170 (2014), 81–88.
17. Coelho, C., Torres, C., Radhouani, H., Pinto, L., Lozano, C., Gomez-Sanz, E., et al. Molecular detection and characterization of methicillin-resistant Staphylococcus aureus (MRSA) isolates from dogs in Portugal. Microb Drug Resist 17 (2011), 333–337.
18. Lin, Y., Barker, E., Kislow, J., Kaldhone, P., Stemper, M.E., Pantrangi, M., et al. Evidence of multiple virulence subtypes in nosocomial and community-associated MRSA genotypes in companion animals from the upper midwestern and northeastern United States. Clin Med Res 9 (2011), 7–16.
19. Loeffler, A., Kearns, A.M., Ellington, M.J., Smith, L.J., Unt, V.E., Lindsay, J.A., et al. First isolation of MRSA ST398 from UK animals: a new challenge for infection control teams?. J Hosp Infect 72 (2009), 269–271.
20. Witte, W., Strommenger, B., Stanek, C., Cuny, C., Methicillin-resistant Staphylococcus aureus ST398 in humans and animals, Central Europe. Emerg Infect Dis 13 (2007), 255–258.
21. Cuny, C., Strommenger, B., Witte, W., Stanek, C., Clusters of infections in horses with MRSA ST1, ST254, and ST398 in a veterinary hospital. Microb Drug Resist 14 (2008), 307–310.
22. Tokateloff, N., Manning, S.T., Weese, J.S., Campbell, J., Rothenburger, J., Stephen, C., et al. Prevalence of methicillin-resistant Staphylococcus aureus colonization in horses in Saskatchewan, Alberta, and British Columbia. Canadian Vet J / Rev vet canadienne 50 (2009), 1177–1180.
23. Scott, G.M., Thomson, R., Malone-Lee, J., Ridgway, G.L., Cross-infection between animals and man: possible feline transmission of Staphylococcus aureus infection in humans?. J Hosp Infect 12 (1988), 29–34.
24. Faires, M.C., Tater, K.C., Weese, J.S., An investigation of methicillin-resistant Staphylococcus aureus colonization in people and pets in the same household with an infected person or infected pet. J Am Vet Med Assoc 235 (2009), 540–543.
25. Weese, J.S., Caldwell, F., Willey, B.M., Kreiswirth, B.N., McGeer, A., Rousseau, J., et al. An outbreak of methicillin-resistant Staphylococcus aureus skin infections resulting from horse to human transmission in a veterinary hospital. Vet Microbiol 114 (2006), 160–164.
26. Schwaber, M.J., Navon-Venezia, S., Masarwa, S., Tirosh-Levy, S., Adler, A., Chmelnitsky, I., et al. Clonal transmission of a rare methicillin-resistant Staphylococcus aureus genotype between horses and staff at a veterinary teaching hospital. Vet Microbiol 162 (2013), 907–911.
27. Cuny, C., Abdelbary, M.M.H., Köck, R., Layer, F., Scheidemann, W., Werner, G., et al. Methicillin-resistant Staphylococcus aureus from infections in horses in Germany are frequent colonizers of veterinarians but rare among MRSA from infections in humans. One Health 2 (2016), 11–17.
28. Haenni, M., Saras, E., Chatre, P., Medaille, C., Bes, M., Madec, J.Y., et al. A USA300 variant and other human-related methicillin-resistant Staphylococcus aureus strains infecting cats and dogs in France. J Antimicrob Chemother 67 (2012), 326–329.
29. Bierowiec, K., Ploneczka-Janeczko, K., Rypula, K., Is the colonisation of Staphylococcus aureus in pets associated with their close contact with owners?. PLoS One, 11, 2016, e0156052.
30. Voss, A., Loeffen, F., Bakker, J., Klaassen, C., Wulf, M., Methicillin-resistant Staphylococcus aureus in pig farming. Emerg Infect Dis 11 (2005), 1965–1966.
31. EFSA, 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 Journal, 7, 2009, 1376.
32. Smith, T.C., Male, M.J., Harper, A.L., Kroeger, J.S., Tinkler, G.P., Moritz, E.D., et al. Methicillin-resistant Staphylococcus aureus (MRSA) strain ST398 is present in midwestern U.S. swine and swine workers. PLoS One, 4, 2009, e4258.
33. Neela, V., Mohd Zafrul, A., Mariana, N.S., van Belkum, A., Liew, Y.K., Rad, E.G., Prevalence of ST9 methicillin-resistant Staphylococcus aureus among pigs and pig handlers in Malaysia. J Clin Microbiol 47 (2009), 4138–4140.
34. Wagenaar, J.A., Yue, H., Pritchard, J., Broekhuizen-Stins, M., Huijsdens, X., Mevius, D.J., et al. Unexpected sequence types in livestock associated methicillin-resistant Staphylococcus aureus (MRSA): MRSA ST9 and a single locus variant of ST9 in pig farming in China. Vet Microbiol 139 (2009), 405–409.
35. Bardiau, M., Yamazaki, K., Duprez, J.N., Taminiau, B., Mainil, J.G., Ote, I., Genotypic and phenotypic characterization of methicillin-resistant Staphylococcus aureus (MRSA) isolated from milk of bovine mastitis. Lett Appl Microbiol 57 (2013), 181–186.
36. Garcia-Alvarez, L., Holden, M.T., Lindsay, H., Webb, C.R., Brown, D.F., Curran, M.D., et al. Meticillin-resistant Staphylococcus aureus with a novel mecA homologue in human and bovine populations in the UK and Denmark: a descriptive study. Lancet Infect Dis 11 (2011), 595–603.
37. Worthing, K.A., Coombs, G.W., Pang, S., Abraham, S., Saputra, S., Trott, D.J., et al. Isolation of mecC MRSA in Australia. J Antimicrob Chemother 71 (2016), 2348–2349.
38. Walther, B., Wieler, L.H., Vincze, S., Antao, E.M., Brandenburg, A., Stamm, I., et al. MRSA variant in companion animals. Emerg Infect Dis 18 (2012), 2017–2020.
39. Haenni, M., Chatre, P., Dupieux, C., Metayer, V., Maillard, K., Bes, M., et al. mecC-positive MRSA in horses. J Antimicrob Chemother 70 (2015), 3401–3402.
40. Becker, K., Ballhausen, B., Kock, R., Kriegeskorte, A., Methicillin resistance in Staphylococcus isolates: the “mec alphabet” with specific consideration of mecC, a mec homolog associated with zoonotic S. aureus lineages. Int J Med Microbiol 304 (2014), 794–804.
41. Gomez, P., Lozano, C., Camacho, M.C., Lima-Barbero, J.F., Hernandez, J.M., Zarazaga, M., et al. Detection of MRSA ST3061-t843-mecC and ST398-t011-mecA in white stork nestlings exposed to human residues. J Antimicrob Chemother 71 (2016), 53–57.
42. Concepcion Porrero, M., Harrison, E.M., Fernandez-Garayzabal, J.F., Paterson, G.K., Diez-Guerrier, A., Holmes, M.A., et al. Detection of mecC-Methicillin-resistant Staphylococcus aureus isolates in river water: a potential role for water in the environmental dissemination. Environ Microbiol Reports 6 (2014), 705–708.
43. Lowder, B.V., Guinane, C.M., Ben Zakour, N.L., Weinert, L.A., Conway-Morris, A., Cartwright, R.A., et al. Recent human-to-poultry host jump, adaptation, and pandemic spread of Staphylococcus aureus. Proc Natl Acad Sci U S A 106 (2009), 19545–19550.
44. Nemati, M., Hermans, K., Lipinska, U., Denis, O., Deplano, A., Struelens, M., et al. Antimicrobial resistance of old and recent Staphylococcus aureus isolates from poultry: first detection of livestock-associated methicillin-resistant strain ST398. Antimicrob Agents Chemother 52 (2008), 3817–3819.
45. van Loo, I., Huijsdens, X., Tiemersma, E., de Neeling, A., van de Sande-Bruinsma, N., Beaujean, D., et al. Emergence of methicillin-resistant Staphylococcus aureus of animal origin in humans. Emerg Infect Dis 13 (2007), 1834–1839.
46. Hanselman, B.A., Kruth, S.A., Rousseau, J., Low, D.E., Willey, B.M., McGeer, A., et al. Methicillin-resistant Staphylococcus aureus colonization in veterinary personnel. Emerg Infect Dis 12 (2006), 1933–1938.
47. Gilbert, M.J., Bos, M.E., Duim, B., Urlings, B.A., Heres, L., Wagenaar, J.A., et al. Livestock-associated MRSA ST398 carriage in pig slaughterhouse workers related to quantitative environmental exposure. Occup Environ Med 69 (2012), 472–478.
48. van Rijen, M.M., Van Keulen, P.H., Kluytmans, J.A., Increase in a Dutch hospital of methicillin-resistant Staphylococcus aureus related to animal farming. Clin Infect Dis 46 (2008), 261–263.
49. Feingold, B.J., Silbergeld, E.K., Curriero, F.C., van Cleef, B.A., Heck, M.E., Kluytmans, J.A., Livestock density as risk factor for livestock-associated methicillin-resistant Staphylococcus aureus, the Netherlands. Emerg Infect Dis 18 (2012), 1841–1849.
50. Boost, M., Ho, J., Guardabassi, L., O'Donoghue, M., Colonization of butchers with livestock-associated methicillin-resistant Staphylococcus aureus. Zoonoses and Public Health 60 (2013), 572–576.
51. Cuny, C., Nathaus, R., Layer, F., Strommenger, B., Altmann, D., Witte, W., Nasal colonization of humans with methicillin-resistant Staphylococcus aureus (MRSA) CC398 with and without exposure to pigs. PLoS One, 4, 2009, e6800.
52. Verkade, E., Kluytmans-van den Bergh, M., van Benthem, B., van Cleef, B., van Rijen, M., Bosch, T., et al. Transmission of methicillin-resistant Staphylococcus aureus CC398 from livestock veterinarians to their household members. PLoS One, 9, 2014, e100823.
53. Bosch, T., Witteveen, S., Haenen, A., Landman, F., Schouls, L.M., Next generation sequencing confirms presumed nosocomial transmission of LA-MRSA in the Netherlands. Appl Environ Microbiol 82 (2016), 4081–4089.
54. van Cleef, B.A., Monnet, D.L., Voss, A., Krziwanek, K., Allerberger, F., Struelens, M., et al. Livestock-associated methicillin-resistant Staphylococcus aureus in humans, Europe. Emerg Infect Dis 17 (2011), 502–505.
55. Nielsen, R.T., Kemp, M., Holm, A., Skov, M.N., Detlefsen, M., Hasman, H., et al. Fatal septicemia linked to transmission of MRSA clonal complex 398 in hospital and nursing home, Denmark. Emerg Infect Dis 22 (2016), 900–902.
56. Sakwinska, O., Giddey, M., Moreillon, M., Morisset, D., Waldvogel, A., Moreillon, P., Staphylococcus aureus host range and human-bovine host shift. Appl Environ Microbiol 77 (2011), 5908–5915.
57. Herron-Olson, L., Fitzgerald, J.R., Musser, J.M., Kapur, V., Molecular correlates of host specialization in Staphylococcus aureus. PLoS One, 2, 2007, e1120.
58. Guinane, C.M., Ben Zakour, N.L., Tormo-Mas, M.A., Weinert, L.A., Lowder, B.V., Cartwright, R.A., et al. Evolutionary genomics of Staphylococcus aureus reveals insights into the origin and molecular basis of ruminant host adaptation. Genome Biol Evol 2 (2010), 454–466.
59. Price, L.B., Stegger, M., Hasman, H., Aziz, M., Larsen, J., Andersen, P.S., et al. Staphylococcus aureus CC398: host adaptation and emergence of methicillin resistance in livestock. mBio, 3, 2012.
60. Spoor, L.E., McAdam, P.R., Weinert, L.A., Rambaut, A., Hasman, H., Aarestrup, F.M., et al. Livestock origin for a human pandemic clone of community-associated methicillin-resistant Staphylococcus aureus. mBio, 4, 2013.
61. de Boer, E., Zwartkruis-Nahuis, J.T., Wit, B., Huijsdens, X.W., de Neeling, A.J., Bosch, T., et al. Prevalence of methicillin-resistant Staphylococcus aureus in meat. Int J Food Microbiol 134 (2009), 52–56.
62. Costa, W.L., Ferreira Jdos, S., Carvalho, J.S., Cerqueira, E.S., Oliveira, L.C., Almeida, R.C., Methicillin-resistant Staphylococcus aureus in raw meats and prepared foods in public hospitals in Salvador, Bahia, Brazil. J Food Sci 80 (2015), M147–M150.
63. Chairat, S., Gharsa, H., Lozano, C., Gomez-Sanz, E., Gomez, P., Zarazaga, M., et al. Characterization of Staphylococcus aureus from raw meat samples in Tunisia: detection of clonal lineage ST398 from the African continent. Foodborne Pathogens Dis 12 (2015), 686–692.
64. Hammad, A.M., Watanabe, W., Fujii, T., Shimamoto, T., Occurrence and characteristics of methicillin-resistant and -susceptible Staphylococcus aureus and methicillin-resistant coagulase-negative staphylococci from Japanese retail ready-to-eat raw fish. Int J Food Microbiol 156 (2012), 286–289.
65. Pu, S., Han, F., Ge, B., Isolation and characterization of methicillin-resistant Staphylococcus aureus strains from Louisiana retail meats. Appl Environ Microbiol 75 (2009), 265–267.
66. Weese, J.S., Reid-Smith, R., Rousseau, J., Avery, B., Methicillin-resistant Staphylococcus aureus (MRSA) contamination of retail pork. Canadian Vet J 51 (2010), 749–752.