Livestock-Associated Staphylococcus aureus: The United States Experience

PLoS Pathogens

Volumn 11, Issue 2, 2015, Pages

  Smith, Tara C ^a  

^a KENT STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGAL PROTEIN; RNA POLYMERASE II; TELOMERE BINDING PROTEIN; TRANSCRIPTION FACTOR;

ANTIBIOTIC RESISTANCE; BACTERIAL INFECTION; BACTERIAL STRAIN; BACTERIUM ISOLATION; COMMUNITY ACQUIRED INFECTION; DISEASE TRANSMISSION; HUMAN; LIVESTOCK; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; NONHUMAN; PATHOGENESIS; PREVALENCE; REVIEW; RISK FACTOR; UNITED STATES; ANIMAL; MICROBIOLOGY; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS AUREUS; TRANSMISSION; VETERINARY;

STAPHYLOCOCCUS AUREUS;

ANIMALS; DISEASE TRANSMISSION, INFECTIOUS; HUMANS; LIVESTOCK; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS AUREUS; UNITED STATES;

EID: 84924352842     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1004564     Document Type: Review

References (58)

1. Weese JS, (2010) Methicillin-resistant Staphylococcus aureus in animals. ILAR J 51: 233–244. doi: 10.1093/ilar.51.3.233
2. McNamee PT, Smyth JA, (2000) Bacterial chondronecrosis with osteomyelitis (‘femoral head necrosis’) of broiler chickens: a review. Avian Pathol 29: 253–270. doi: 10.1080/030794500750047243 19184815
3. Viana D, Selva L, Segura P, Penades JR, Corpa JM, (2007) Genotypic characterization of Staphylococcus aureus strains isolated from rabbit lesions. Vet Microbiol 121: 288–298. doi: 10.1016/j.vetmic.2006.12.003 17208392
4. Shepheard MA, Fleming VM, Connor TR, Corander J, Feil EJ, et al. (2013) Historical zoonoses and other changes in host tropism of Staphylococcus aureus, identified by phylogenetic analysis of a population dataset. PLoS One 8: e62369. doi: 10.1371/journal.pone.0062369 23667472
5. Silbergeld EK, Graham J, Price LB, (2008) Industrial food animal production, antimicrobial resistance, and human health. Annu Rev Public Health 29: 151–169. doi: 10.1146/annurev.publhealth.29.020907.090904 18348709
6. Fluit AC, (2012) Livestock-associated Staphylococcus aureus. Clin Microbiol Infect 18: 735–744. doi: 10.1111/j.1469-0691.2012.03846.x 22512702
7. Smith TC, Pearson N, (2011) The emergence of Staphylococcus aureus ST398. Vector Borne Zoonotic Dis 11: 327–339. doi: 10.1089/vbz.2010.0072 20925523
8. Johnson AP, (2011) Methicillin-resistant Staphylococcus aureus: the European landscape. J Antimicrob Chemother 66 Suppl 4: iv43–iv48. doi: 10.1093/jac/dkr076 21521706
9. Kock R, Mellmann A, Schaumburg F, Friedrich AW, Kipp F, et al. (2011) The epidemiology of methicillin-resistant Staphylococcus aureus (MRSA) in Germany. Dtsch Arztebl Int 108: 761–767. doi: 10.3238/arztebl.2011.0761 22163252
10. Larsen J, Imanishi M, Hinjoy S, Tharavichitkul P, Duangsong K, et al. (2012) Methicillin-resistant Staphylococcus aureus ST9 in pigs in Thailand. PLoS One 7: e31245. doi: 10.1371/journal.pone.0031245 22363594
11. Neela V, Arif MZ, Nor Shamsudin M, van Belkum A, Khoon LY, et al. (2009) Prevalence of ST9 MRSA among Pigs and Pig Handlers in Malaysia. J Clin Microbiol 47: 4138–4140. doi: 10.1128/JCM.01363-09 19812280
12. Wagenaar JA, Yue H, Pritchard J, Broekhuizen-Stins M, Huijsdens X, et al. (2009) 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: 405–409. doi: 10.1016/j.vetmic.2009.06.014 19608357
13. Patchanee P, Tadee P, Arjkumpa O, Love D, Chanachai K, et al. (2014) Occurrence and characterization of livestock associated-methicillin resistant Staphylococcus aureus in pig industries of northern Thailand. J Vet Sci 15: 529–536. doi: 10.4142/jvs.2014.15.4.529 25530702
14. Fang HW, Chiang PH, Huang YC, (2014) Livestock-associated methicillin-resistant Staphylococcus aureus ST9 in pigs and related personnel in Taiwan. PLoS One 9: e88826. doi: 10.1371/journal.pone.0088826 24551168
15. Argudin MA, Cariou N, Salandre O, Le Guennec J, Nemeghaire S, et al. (2013) Genotyping and antimicrobial resistance of Staphylococcus aureus isolates from diseased turkeys. Avian Pathol 42: 572–580. doi: 10.1080/03079457.2013.854308 24224550
16. Wendlandt S, Kadlec K, Fessler AT, Monecke S, Ehricht R, et al. (2013) Resistance phenotypes and genotypes of methicillin-resistant Staphylococcus aureus isolates from broiler chickens at slaughter and abattoir workers. J Antimicrob Chemother 68: 2458–2463. doi: 10.1093/jac/dkt239 23798670
17. Nemeghaire S, Roelandt S, Argudin MA, Haesebrouck F, Butaye P, (2013) Characterization of methicillin-resistant Staphylococcus aureus from healthy carrier chickens. Avian Pathol 42: 342–346. doi: 10.1080/03079457.2013.805183 23777220
18. Buyukcangaz E, Velasco V, Sherwood JS, Stepan RM, Koslofsky RJ, et al. (2013) Molecular typing of Staphylococcus aureus and methicillin-resistant S. aureus (MRSA) isolated from animals and retail meat in North Dakota, United States. Foodborne Pathog Dis 10: 608–617.
19. van Duijkeren E, Jansen MD, Flemming SC, de Neeling H, Wagenaar JA, et al. (2007) Methicillin-resistant Staphylococcus aureus in pigs with exudative epidermitis. Emerg Infect Dis 13: 1408–1410. doi: 10.3201/eid1309.061268 18252124
20. Graveland H, Duim B, van Duijkeren E, Heederik D, Wagenaar JA, (2011) Livestock-associated methicillin-resistant Staphylococcus aureus in animals and humans. Int J Med Microbiol 301: 630–634. doi: 10.1016/j.ijmm.2011.09.004 21983338
21. Lowder BV, Guinane CM, Ben Zakour NL, Weinert LA, Conway-Morris A, et al. (2009) Recent human-to-poultry host jump, adaptation, and pandemic spread of Staphylococcus aureus. Proc Natl Acad Sci U S A 106: 19545–19550. doi: 10.1073/pnas.0909285106 19884497
22. Price LB, Stegger M, Hasman H, Aziz M, Larsen J, et al. (2012) Staphylococcus aureus CC398: host adaptation and emergence of methicillin resistance in livestock. mBio 3: e00305–11. doi: 10.1128/mBio.00305-11 22354957
23. Smith TC, Male MJ, Harper AL, Kroeger JS, Tinkler GP, et al. (2009) Methicillin-resistant Staphylococcus aureus (MRSA) strain ST398 is present in midwestern U.S. swine and swine workers. PLoS ONE 4: e4258. doi: 10.1371/journal.pone.0004258 19145257
24. Hanson BM, Dressler AE, Harper AL, Scheibel RP, Wardyn SE, et al. (2011) Prevalence of Staphylococcus aureus and methicillin-resistant Staphylococcus aureus (MRSA) on retail meat in Iowa. Journal of Infection and Public Health 4: 169–174. doi: 10.1016/j.jiph.2011.06.001 22000843
25. Bhat M, Dumortier C, Taylor BS, Miller M, Vasquez G, et al. (2009) Staphylococcus aureus ST398, New York City and Dominican Republic. Emerg Infect Dis 15: 285–287. doi: 10.3201/eid1502.080609 19193274
26. Uhlemann AC, Porcella SF, Trivedi S, Sullivan SB, Hafer C, et al. (2012) Identification of a highly transmissible animal-independent Staphylococcus aureus ST398 clone with distinct genomic and cell adhesion properties. mBio 3: e00027–12. doi: 10.1128/mBio.00027-12 22375071
27. David MZ, Siegel J, Lowy FD, Zychowski D, Taylor A, et al. (2013) Asymptomatic carriage of sequence type 398, spa type t571 methicillin-susceptible Staphylococcus aureus in an urban jail: a newly emerging, transmissible pathogenic strain. J Clin Microbiol 51: 2443–2447. doi: 10.1128/JCM.01057-13 23658269
28. Dressler AE, Scheibel RP, Wardyn S, Harper AL, Hanson BM, et al. (2012) Prevalence, antibiotic resistance and molecular characterisation of Staphylococcus aureus in pigs at agricultural fairs in the USA. Vet Rec 170: 495. doi: 10.1136/vr.100570 22505242
29. 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: 234–243. doi: 10.1111/j.1863-2378.2012.01527.x 22883566
30. Gordoncillo MJ, Abdujamilova N, Perri M, Donabedian S, Zervos M, et al. (2012) Detection of methicillin-resistant Staphylococcus aureus (MRSA) in backyard pigs and their owners, Michigan, USA. Zoonoses Public Health 59: 212–216. doi: 10.1111/j.1863-2378.2011.01437.x 21914153
31. Frana TS, Beahm AR, Hanson BM, Kinyon JM, Layman LL, et al. (2013) Isolation and characterization of methicillin-resistant Staphylococcus aureus from pork farms and visiting veterinary students. PLoS One 8: e53738. doi: 10.1371/journal.pone.0053738 23301102
32. Molla B, Byrne M, Abley M, Mathews J, Jackson CR, et al. (2012) Epidemiology and genotypic characteristics of methicillin-resistant Staphylococcus aureus strains of porcine origin. J Clin Microbiol 50: 3687–3693. doi: 10.1128/JCM.01971-12 22972820
33. Smith TC, Gebreyes WA, Abley MJ, Harper AL, Forshey BM, et al. (2013) Methicillin-resistant Staphylococcus aureus in pigs and farm workers on conventional and antibiotic-free swine farms in the USA. PLoS One 8: e63704. doi: 10.1371/journal.pone.0063704 23667659
34. Rinsky JL, Nadimpalli M, Wing S, Hall D, Baron D, et al. (2013) Livestock-associated methicillin and multidrug resistant Staphylococcus aureus is present among industrial, not antibiotic-free livestock operation workers in North Carolina. PLoS One 8: e67641. doi: 10.1371/journal.pone.0067641 23844044
35. Neyra RC, Frisancho JA, Rinsky JL, Resnick C, Carroll KC, et al. (2014) Multidrug-Resistant and Methicillin-Resistant Staphylococcus aureus (MRSA) in Hog Slaughter and Processing Plant Workers and Their Community in North Carolina (USA). Environ Health Perspect 122: 471–477. doi: 10.1289/ehp.1306741 24508836
36. Nadimpalli M, Rinsky JL, Wing S, Hall D, Stewart J, et al. (2014) Persistence of livestock-associated antibiotic-resistant Staphylococcus aureus among industrial hog operation workers in North Carolina over 14 days. Occup Environ Med. E-pub ahead of print. doi: 10.1136/oemed-2014-102095
37. 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: 1980–1990. doi: 10.1001/jamainternmed.2013.10408 24043228
38. Carrel M, Schweizer ML, Sarrazin MV, Smith TC, Perencevich EN, (2014) Residential proximity to large numbers of swine in feeding operations is associated with increased risk of methicillin-resistant Staphylococcus aureus colonization at time of hospital admission in rural Iowa veterans. Infect Control Hosp Epidemiol 35: 190–193. doi: 10.1086/674860 24442084
39. Rasigade JP, Laurent F, Hubert P, Vandenesch F, Etienne J, (2010) Lethal necrotizing pneumonia caused by an ST398 Staphylococcus aureus strain. Emerging Infectious Diseases 16: 1330. doi: 10.3201/eid1608.100317 20678343
40. Valentin-Domelier AS, Girard M, Bertrand X, Violette J, Francois P, et al. (2011) Methicillin-susceptible ST398 Staphylococcus aureus responsible for bloodstream infections: an emerging human-adapted subclone? PLoS ONE 6: e28369. doi: 10.1371/journal.pone.0028369 22163008
41. van Belkum A, Melles DC, Peeters JK, van Leeuwen WB, van Duijkeren E, et al. (2008) Methicillin-resistant and—susceptible Staphylococcus aureus sequence type 398 in pigs and humans. Emerg Infect Dis 14: 479–483. doi: 10.3201/eid1403.0760 18325267
42. Mediavilla JR, Chen L, Uhlemann AC, Hanson BM, Rosenthal M, et al. (2012) Methicillin-Susceptible Staphylococcus aureus ST398, New York and New Jersey, USA. Emerging Infectious Diseases 18: 700–702. doi: 10.3201/eid1804.111419 22469250
43. Orscheln RC, Hunstad DA, Fritz SA, Loughman JA, Mitchell K, et al. (2009) Contribution of genetically restricted, methicillin-susceptible strains to the ongoing epidemic of community-acquired Staphylococcus aureus infections. Clinical Infectious Diseases 49: 536–542. doi: 10.1086/600881 19589082
44. Golding GR, Bryden L, Levett PN, McDonald RR, Wong A, et al. (2010) Livestock-associated methicillin-resistant Staphylococcus aureus sequence type 398 in humans, Canada. Emerg Infect Dis 16: 587–594. doi: 10.3201/eid1604.091435 20350371
45. Waters AE, Contente-Cuomo T, Buchhagen J, Liu CM, Watson L, et al. (2011) Multidrug-Resistant Staphylococcus aureus in US Meat and Poultry. Clin Infect Dis 52: 1227–1230. doi: 10.1093/cid/cir181 21498385
46. O’Brien AM, Hanson BM, Farina SA, Wu JY, Simmering JE, et al. (2012) MRSA in conventional and alternative retail pork products. PLoS ONE 7: e30092. doi: 10.1371/journal.pone.0030092 22276147
47. Pu S, Han F, Ge B, (2008) Isolation and Characterization of Methicillin-Resistant Staphylococcus aureus from Louisiana Retail Meats. Appl Environ Microbiol 75: 265–267. doi: 10.1128/AEM.01110-08 18978079
48. Bhargava K, Wang X, Donabedian S, Zervos M, de Rocha L, et al. (2011) Methicillin-resistant Staphylococcus aureus in retail meat, Detroit, Michigan, USA. Emerg Infect Dis 17: 1135–1137. doi: 10.3201/eid1706.101095 21749794
49. Jackson CR, Davis JA, Barrett JB, (2013) Prevalence and characterization of methicillin-resistant Staphylococcus aureus isolates from retail meat and humans in Georgia. J Clin Microbiol 51: 1199–1207. doi: 10.1128/JCM.03166-12 23363837
50. Hetem DJ, Bootsma MC, Troelstra A, Bonten MJ, (2013) Transmissibility of livestock-associated methicillin-resistant Staphylococcus aureus. Emerg Infect Dis 19: 1797–1802. doi: 10.3201/eid1911.121085 24207050
51. Spoor LE, McAdam PR, Weinert LA, Rambaut A, Hasman H, et al. (2013) Livestock origin for a human pandemic clone of community-associated methicillin-resistant Staphylococcus aureus. MBio 4: e00356–13. doi: 10.1128/mBio.00356-13 23943757
52. Wu S, Piscitelli C, de Lencastre H, Tomasz A, (1996) Tracking the evolutionary origin of the methicillin resistance gene: cloning and sequencing of a homologue of mecA from a methicillin susceptible strain of Staphylococcus sciuri. Microb Drug Resist 2: 435–441. doi: 10.1089/mdr.1996.2.435 9158816
53. (1978) Ebola haemorrhagic fever in Zaire, 1976. Bull World Health Organ 56: 271–293. 307456
54. Garcia-Alvarez L, Holden MT, Lindsay H, Webb CR, Brown DF, et al. (2011) 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: 595–603. doi: 10.1016/S1473-3099(11)70126-8 21641281
55. Shore AC, Deasy EC, Slickers P, Brennan G, O’Connell B, et al. (2011) Detection of staphylococcal cassette chromosome mec type XI carrying highly divergent mecA, mecI, mecR1, blaZ, and ccr genes in human clinical isolates of clonal complex 130 methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother 55: 3765–3773. doi: 10.1128/AAC.00187-11 21636525
56. Stegger M, Liu CM, Larsen J, Soldanova K, Aziz M, et al. (2013) Rapid differentiation between livestock-associated and livestock-independent Staphylococcus aureus CC398 clades. PLoS One 8: e79645. doi: 10.1371/journal.pone.0079645 24244535
57. WHO (2014) Antimicrobial resistance: global report on surveillance Geneva, Switzerland. pp. 257.
58. Smith DL, Harris AD, Johnson JA, Silbergeld EK, Morris JG, Jr. (2002) Animal antibiotic use has an early but important impact on the emergence of antibiotic resistance in human commensal bacteria. Proc Natl Acad Sci U S A 99: 6434–6439. doi: 10.1073/pnas.082188899 11972035