In order to examine the prevalence of Staphylococcus aureus on retail pork, three hundred ninety-five pork samples were collected from a total of 36 stores in Iowa, Minnesota, and New Jersey. S. aureus was isolated from 256 samples (64.8%, 95% confidence interval [CI] 59.9%–69.5%). S. aureus was isolated from 67.3% (202/300) of conventional pork samples and from 56.8% (54/95) of alternative pork samples (labeled “raised without antibiotics” or “raised without antibiotic growth promotants”). Two hundred and thirty samples (58.2%, 95% CI 53.2%–63.1%) were found to carry methicillin-sensitive S. aureus (MSSA). MSSA was isolated from 61.0% (183/300) of conventional samples and from 49.5% (47/95) of alternative samples. Twenty-six pork samples (6.6%, 95% CI 4.3%–9.5%) carried methicillin-resistant S. aureus (MRSA). No statistically significant differences were observed for the prevalence of S. aureus in general, or MSSA or MRSA specifically, when comparing pork products from conventionally raised swine and swine raised without antibiotics, a finding that contrasts with a prior study from the Netherlands examining both conventional and “biologic” meat products. In our study spa types associated with “livestock-associated” ST398 (t034, t011) were found in 26.9% of the MRSA isolates, while 46.2% were spa types t002 and t008—common human types of MRSA that also have been found in live swine. The study represents the largest sampling of raw meat products for MRSA contamination to date in the U.S. MRSA prevalence on pork products was higher than in previous U.S.-conducted studies, although similar to that in Canadian studies.
Citation: O'Brien AM, Hanson BM, Farina SA, Wu JY, Simmering JE, Wardyn SE, et al. (2012) MRSA in Conventional and Alternative Retail Pork Products. PLoS ONE7(1): e30092. https://doi.org/10.1371/journal.pone.0030092
Editor: Bernhard Kaltenboeck, Auburn University, United States of America
Received: August 6, 2011; Accepted: December 9, 2011; Published: January 19, 2012
Copyright: © 2012 O'Brien et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: This study was funded, in part, with support from the Claneil Foundation. No additional external funding was received for this study. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: The authors have declared that no competing interests exist.
Staphylococcus aureus is estimated to cause around 185,000 cases of food poisoning annually . It also can cause serious, often life threatening human infections of the bloodstream, skin, lungs, and other organs . In 2003–2004, a nationally representative survey found nearly a third (28.6%) of the U.S. population was colonized in their nares with S. aureus .
This same study found the prevalence of Americans carrying S. aureus resistant to methicillin, or MRSA, was 1.5% . While once mainly a hospital problem, MRSA infections occurring in community settings have increased in incidence over the last decade , with community-associated MRSA strains now constituting the most frequent cause of skin and soft tissue infections presenting to emergency departments , . In the U.S., these community-associated MRSA (CA-MRSA) strains have been of apparent human origin. In parts of Europe, however, livestock-associated MRSA–in particular, the swine-associated ST398 strain–appears to be an important, emerging strain of human MRSA in the community , , and has been reported as a cause of human disease in several countries , , and of deaths in Spain and France , .
The finding of MRSA ST398 in farm environments has been accompanied by a rising concern regarding the presence of ST398 in the food supply, which may allow food to serve as a vehicle to transmit animal-associated MRSA into the human population. In North America, MRSA ST398 has been detected in pigs and farmers in Canada and the United States (U.S.) , , and human ST398 infections have been demonstrated in Canada . As not all patients diagnosed with ST398 infections had known contact with livestock, the possibility of acquisition of ST398 via handling of contaminated pork products was suggested.
There has been less study overall of MRSA in retail meat products than in the farming environment. Studies conducted outside the U.S. have detected MRSA strains in 1.2 percent to 35.3 percent of samples from a variety of such products including retail meats in Canada , , Spain  and the Netherlands , . Thirty-two percent of the MRSA strains in pork samples from one Canadian study were identified as ST398 , but none in the second study , while 50 percent from the Spanish study (1 of 2) and 85 percent of MRSA strains in the Dutch meat samples were ST398 , .
Preliminary testing of limited numbers of retail meat products in the U.S. have produced mixed results. MRSA was detected in five of 90 (5.6 percent) pork samples and one of 30 (3.3 percent) beef samples in Louisiana ; none of 36 meat samples (12 beef, 12 chicken, 12 pork) collected from stores in Rhode Island ; and two of 55 pork samples (3.6 percent) tested in an study of Iowa retail meats . Only one of the MRSA strains identified in these prior studies was ST398. A recent study by Waters et al found S. aureus in 47 percent of 136 meat samples collected from 4 states and the District of Columbia. While ST398 strains were found in methicillin-susceptible S. aureus from this study, no MRSA ST398 was detected .
As MRSA has been found in a higher percentage of retail meats in other countries and there are significant limitations in the U.S. studies conducted to date (including variability in the methods used between studies, limiting the comparisons between states, see Table 1), we designed our study to include a higher number of samples (n = 395) of one type of meat (pork) from three geographic areas: two of them being Midwestern states among the nation's top three pork producers, and one in the outskirts of New York City, a major U.S. population center. We tested a wide range of raw pork products, both pre-packaged and individually wrapped at point of purchase from the meat counter. Products were collected from retail chain stores, some of which could be found in all three states, but most of which were part of local or regional chains. Furthermore, as no U.S. study had specifically tested potential differences in S. aureus contamination between conventional and “alternative” pork products (labeled and/or marketed as raised without antibiotics or raised without antibiotic growth promotants), we also included these meats in our sample.
Materials and Methods
Sample collection and culture
Three hundred ninety-five raw pork samples were collected from 36 retail food stores in Iowa, Minnesota, and New Jersey in four rounds of sampling carried out at weekly intervals in September and October 2010. Stores were chosen to include a mix of national and regional supermarkets and retail chains, specialty food markets and cooperative grocery stores. Pork cuts collected included pork chop, ground pork, riblets, ribs, sausage, blade steak, cube steaks, pork loin, pork roast, and pork cutlet; all were either identified as fresh on the package label and did not appear to have been previously frozen or were verbally confirmed as fresh at the meat counter. Pork packages were double-bagged upon purchase to avoid cross-contamination, shipped overnight on blue ice following Federal Express guidelines for shipping perishable foods, and analyzed within 24 hours of purchase.
Upon arrival at the laboratory, packaging was removed using a sterile razor blade and pork samples were transferred into stomacher bags (VWR, West Chester, PA) with sterile tongs. Sample weight was recorded and 100 g was used as a minimal sample size. Two hundred and fifty mL of sterile 0.1% peptone broth was added to the sample by sterile graduated cylinder. Samples were then mixed vigorously by hand for one minute. A 30 ml aliquot from the peptone wash was added to 30 ml of Baird Parker broth (2× concentration) with tellurite enrichment (Sigma products – Sigma-Aldrich, St. Louis MO) in a 250 ml sterile Erlenmeyer flask and incubated at 35°C for 18–24 hours. After enrichment, 10 µl was plated onto Baird Parker agar (BPA) with EY tellurite enrichment (BD) and incubated at 35°C 18–24 hours for growth. Ten µL were also plated onto CHROMagar MRSA plates (BD) and incubated at 35°C 24–48 hours and examined for growth. Presumptive S. aureus (black colonies with clear halos on BPA) and presumptive MRSA (mauve colonies on CHROMagar) were confirmed by examining their appearance on Gram stain, and by doing the catalase test, the tube coagulase test and the S. aureus latex agglutination assay (Pastorex Staph-plus, Bio-Rad). Methicillin resistance was assessed by testing for the presence of penicillin binding protein (PBP2') (MRSA latex agglutination test, Oxoid Ltd., Hants, UK) and confirmed with mecA polymerase chain reaction (PCR). S. aureus isolates were stored at −80°C.
One MRSA isolate per positive specimen was subjected to molecular typing. Genomic DNA was extracted using the Wizard Genomic DNA preparation kit (Promega). The presence of mecA and PVL were determined by PCR , . Multi locus sequence typing (MLST) was performed on a subset of isolates . spa typing was carried out using the alternate forward primer described in  and the reverse primer noted on the Ridom website (http://www.ridom.de/doc/Ridom_spa_sequencing.pdf). All molecular procedures employed known positive and negative controls.
Antimicrobial susceptibility testing (AST)
All presumptive MRSA isolates were also tested for antimicrobial susceptibility by the broth dilution method described by the Clinical and Laboratory Standards Institute . Isolates were tested for susceptibility to the following 10 antibiotics using this method: oxacillin, tetracycline, erythromycin, clindamycin, trimethoprim-sulfamethoxazole, quinupristin/dalfopristin, levofloxacin, linezolid, daptomycin, and vancomycin. Mupirocin resistance and inducible clindamycin resistance were also examined .
Analyses were conducted for two groups: all S. aureus (MSSA and MRSA together) and MRSA specifically. Exact 95% confidence intervals (CI) were calculated for unadjusted prevalence rates. Heterogeneity of S. aureus or MRSA positivity among categorical variables was addressed using Pearson's chi-square test with Yates' correction or by Fisher's exact test. To control for correlation of samples within each store, cluster-adjusted odds ratios (OR) and CIs were calculated using PROC GENMOD in SAS 9.2 (SAS Institute, Cary, NC), with an exchangeable correlation matrix structure. Significance was assessed at alpha = 0.05.
Prevalence of S. aureus in pork samples
Three hundred ninety-five pork samples were collected from a total of 36 stores in Iowa, Minnesota, and New Jersey. S. aureus was isolated from 256 samples (64.8%, 95% CI 59.9%–69.5%). S. aureus prevalence in retail pork from Iowa, Minnesota, and New Jersey was 59.7% (74/124, 95% CI 50.5%–68.4%), 72.3% (102/141, 95% CI 64.2%–79.5%), and 61.5% (80/130, 95% CI 52.6%–69.9%), respectively. These differences among states were not statistically significant (χ2 = 5.548, degrees of freedom (df) = 2, p = 0.062; adjusted for clustering within stores, p = 0.306). Likewise, no significant difference was observed for S. aureus prevalence between conventional and alternative pork samples (χ2 = 3.482, df = 1, p = 0.062; adjusted OR 1.56, 95% CI 0.86—2.83). Of 300 conventional pork samples, S. aureus was isolated from 202 samples (67.3%, 95% CI 61.7%–72.6%) while S. aureus was isolated from 54/95 (56.8%, 95% CI 46.3%–67.0%) of pork labeled raised without antibiotics or raised without antibiotic growth promotants.
Prevalence of MRSA in pork samples
Twenty-six MRSA positive samples were identified (6.6%, 95% CI 4.3%–9.5%). Prevalence was 8.1% in Iowa (10/124, 95% CI 3.9%–14.3%); 7.1% (10/141, 95% CI 3.5%—12.7%) in Minnesota; and 4.6% (6/130, 95% CI 1.7%–9.8%) in New Jersey (χ2 = 1.321, df = 2, p = 0.517; adjusted for clustering within stores, p = 0.409). MRSA-positive samples were collected from 41.7% (15/36) of the stores included in the study. Similar prevalences of MRSA-positivity were found in conventional pork (6.3% [19/300], 95% CI 3.9%—9.7%) and in alternative pork (7.4% [7/95], 95% CI 3.0%–14.6%; adjusted OR 0.93, 95% CI 0.276—3.16). Six of the seven MRSA positive alternative pork samples came from the same retail chain (17.1% [6/35] of samples from the chain) in two different states and four from the same store (21.1% [4/19] of samples from the store), the largest number of MRSA isolates associated with any one store in this study. Of the six MRSA isolates from this chain, five (83%) were spa type t008.
By pork cut, MRSA prevalence ranged from 0% (riblets, blade steak, cube steak, pork loin) to 50% (pork cutlet). In all types of pork products, on the other hand, prevalence of MSSA equaled or exceeded 50% of samples (see Figure 1). No statistically significant differences in S. aureus or MRSA prevalence were seen between different cuts of pork (p = 0.725 [Pearson's Chi-square test] and p = 0.133 [Fisher's exact test] for S. aureus and MRSA, respectively).
All 26 isolates identified as MRSA via positive PBP2' latex tests and mecA PCR were subjected to AST. Twenty-two (84.6%) were resistant to oxacillin; interestingly, four were found to be susceptible to oxacillin by broth microdilution, despite harboring the mecA gene, as we have seen in previous research . Seventeen (65.4%) were resistant to tetracycline, 10 (38.5%) were resistant to erythromycin and 9 (34.6%) were resistant to clindamycin. One isolate was resistant only to TMP-SMX; another isolate was resistant to oxacillin, tetracycline, clindamycin, erythromycin, and quinupristin-dalfopristin (see Table 2). Twenty isolates (76.9%) were resistant to two or more antibiotics and ten isolates (38.5%) were resistant to three or more antibiotics tested.
All MRSA isolates were subjected to spa typing. Six isolates (23.1%) were t034, and 1 (3.8%) was t011, both associated with ST398. Six isolates (23.1%) each were t002 (associated with USA100/ST5) and t008 (associated with USA300/ST8). Other types included t094 (n = 2); t078 (n = 1); t273 (n = 1); t803 (n = 1); t2922 (n = 1), and a new spa type, t8314 (n = 1). Two of these isolates, both from Minnesota pork samples, were spa type t094, but were from different cuts of pork purchased from different stores and were different lines of meat, though they were from the same brand. t8314 was a novel spa type and also corresponded to a new sequence type (ST2007). Five isolates (19.2%) were found to carry PVL, a genotype epidemiologically associated with increased virulence , ; all were spa type t008 (see Table 2). A similar percentage of both conventional and alternative pork harbored spa types associated with ST398 (2/7, 28.6% in alternative samples; 5/19, 26.3% in conventional samples). However, 4/5 (80%) of the PVL-positive t008 isolates were found in alternative pork samples.
This study confirms the presence of S. aureus on raw pork products in the United States, regardless of whether produced conventionally or from animals raised without antibiotics/antibiotic growth promotants. No statistically significant differences were observed when comparing S. aureus (whetherMSSA or MRSA) positivity on conventional and alternative pork products.
This is in contrast to findings from the Netherlands, where a lower prevalence of MRSA in meat from “biological” reared chickens (raised using no growth promotants) and wild fowl and game was found, in comparison to the prevalence of MRSA found in conventionally raised poultry in the same study , suggesting a link between antibiotic use and prevalence of MRSA on meat products in Europe. This was also shown in a study of U.S. pigs, where MRSA was found in four of nine “conventional” pig farms, but was absent from pigs raised without antibiotics (Smith, unpublished findings). It is possible that a difference in MRSA contamination between conventional and alternative meats does not exist in our sampling areas. Alternatively, in the U.S., it is possible that a link between on-farm antibiotic use and MRSA on meat products may be obscured by human contamination of meat with MRSA post-slaughter, as human carriage of MRSA in the U.S. is approximately 50 times higher than what has been reported in the Netherlands (1.5% vs. .03%) . However, given that 85.7% (6/7) of the MRSA-positive alternative pork samples in our study came from the same retail chain in two different states and four from the same store, there could be other explanations for our findings. Both antibiotic claims used to identify alternative products for this study, “raised without antibiotics” and “raised without antibiotic growth promotants”, are not typically verified by an independent third party, unlike USDA-certified Organic meat products, which are also raised without antibiotics. While certified organic pork products were available at some of the stores included in this study, they were not available in an appropriate form for our testing, e.g., they were smoked, frozen or pre-cooked.
Additionally, similar to meats raised conventionally, pork raised without antibiotics can be contaminated with MRSA at the processing plant, either from contaminated products processed on the same equipment or by colonized workers. Processing equipment must be cleaned out between runs of certified organic and non-certified organic meats, which may help to prevent this type of cross-contamination (http://www.mda.state.mn.us/en/sitecore/content/Global/MDADocs/food/organic/organicmeatprod.aspx). Two Dutch studies showed MRSA colonization of slaughterhouse workers: one swine-based study that found MRSA ST398 and one broiler-focused study , . In both studies transmission appeared to go from animals to humans, but exact transmission routes were not determined. To our knowledge, no similar research has been published in the U.S.
Overall, MRSA prevalence on pork products was similar to what has been found in other studies conducted in Canada, but higher than that previously identified in studies conducted in the U.S. , , , . Strengths of our study include the sampling of three different geographic areas and the inclusion of both urban and rural areas, as well as the inclusion of a wide variety of pork cuts and brands, both conventional and raised without antibiotics. This study also represents the largest sampling of raw meat products for MRSA contamination carried out to date in the U.S.
A significant proportion of MRSA isolates (26.9%) were spa types associated with ST398 (t034, t011), a “livestock-associated” strain . An additional 23.1% each were spa types t002 and t008, common human types that have also been found in live swine , . A limitation of this study is our inability to determine the ultimate origin of these isolates, e.g., whether they are a result of contamination from the farming environment, human contamination post-slaughter, or both. Previous research has shown that there is a poultry-adapted ST5 lineage (a type which contains spa type t002) that originated in humans and subsequently spread amongst commercial poultry ; a similar cross-species transfer event could have occurred in American swine herds, resulting in a swine-adapted t002 strain. Additional genomic studies are necessary to examine this possibility.
Also unknown is the role that MRSA contamination of raw meats in the U.S., now confirmed by several studies , , , may play in the overall ecology and transmission of this organism. Bacterial contamination was not quantitated in this study; as such, the amount of initial colonies present on the pork samples is unknown. Also unknown is the frequency of MRSA transmission to humans, via colonization or infection from food service professional and consumer handling and consumption of raw, undercooked and cooked MRSA-positive meat. A study in the Netherlands examining MRSA carriage by food handlers did not find any MRSA-positive individuals, even though some had been handling meat products which were contaminated with MRSA . However, it is difficult to directly apply these findings to consumers, who may not receive as much training in proper food handling. Future studies are necessary to examine this aspect.
The authors thank Carla Kaiser and Katie Rojas-Jahn for assistance with sample collection.
Conceived and designed the experiments: TCS MEK DBW. Performed the experiments: TCS AMO BMH SAF JYW JES SEW. Analyzed the data: TCS AMO MEK BMF. Wrote the paper: TCS AMO MEK DBW BMH SEW BMF.
- 1. Mead PS, Slutsker L, Dietz V, McCaig LF, Bresee JS, et al. (1999) Food-related illness and death in the United States. Emerging infectious Diseases 5: 607–625.PS MeadL. SlutskerV. DietzLF McCaigJS Bresee1999Food-related illness and death in the United States.Emerging infectious Diseases5607625
- 2. Noskin GA, Rubin RJ, Schentag JJ, Kluytmans J, Hedblom EC, et al. (2005) The burden of Staphylococcus aureus infections on hospitals in the United States: an analysis of the 2000 and 2001 Nationwide Inpatient Sample Database. Arch Intern Med 165: 1756–1761.GA NoskinRJ RubinJJ SchentagJ. KluytmansEC Hedblom2005The burden of Staphylococcus aureus infections on hospitals in the United States: an analysis of the 2000 and 2001 Nationwide Inpatient Sample Database.Arch Intern Med16517561761
- 3. Gorwitz RJ, Kruszon-Moran D, McAllister SK, McQuillan G, McDougal LK, et al. (2008) Changes in the prevalence of nasal colonization with Staphylococcus aureus in the United States, 2001–2004. J Infect Dis 197: 1226–1234.RJ GorwitzD. Kruszon-MoranSK McAllisterG. McQuillanLK McDougal2008Changes in the prevalence of nasal colonization with Staphylococcus aureus in the United States, 2001–2004.J Infect Dis19712261234
- 4. David MZ, Daum RS (2010) Community-associated methicillin-resistant Staphylococcus aureus: epidemiology and clinical consequences of an emerging epidemic. Clin Microbiol Rev 23: 616–687.MZ DavidRS Daum2010Community-associated methicillin-resistant Staphylococcus aureus: epidemiology and clinical consequences of an emerging epidemic.Clin Microbiol Rev23616687
- 5. Moran GJ, Krishnadasan A, Gorwitz RJ, Fosheim GE, McDougal LK, et al. (2006) Methicillin-resistant S. aureus infections among patients in the emergency department. N Engl J Med 355: 666–674.GJ MoranA. KrishnadasanRJ GorwitzGE FosheimLK McDougal2006Methicillin-resistant S. aureus infections among patients in the emergency department.N Engl J Med355666674
- 6. Frazee BW, Lynn J, Charlebois ED, Lambert L, Lowery D, et al. (2005) High prevalence of methicillin-resistant Staphylococcus aureus in emergency department skin and soft tissue infections. Ann Emerg Med 45: 311–320.BW FrazeeJ. LynnED CharleboisL. LambertD. Lowery2005High prevalence of methicillin-resistant Staphylococcus aureus in emergency department skin and soft tissue infections.Ann Emerg Med45311320
- 7. van Cleef BA, Monnet DL, Voss A, Krziwanek K, Allerberger F, et al. (2011) Livestock-associated Methicillin-Resistant Staphylococcus aureus in Humans, Europe. Emerg Infect Dis 17: 502–505.BA van CleefDL MonnetA. VossK. KrziwanekF. Allerberger2011Livestock-associated Methicillin-Resistant Staphylococcus aureus in Humans, Europe.Emerg Infect Dis17502505
- 8. van Loo I, Huijsdens X, Tiemersma E, de Neeling A, van de Sande-Bruinsma N, et al. (2007) Emergence of Methicillin-Resistant Staphylococcus aureus of Animal Origin in Humans. Emerging Infectious Diseases 13: 1834–1839.I. van LooX. HuijsdensE. TiemersmaA. de NeelingN. van de Sande-Bruinsma2007Emergence of Methicillin-Resistant Staphylococcus aureus of Animal Origin in Humans.Emerging Infectious Diseases1318341839
- 9. Declercq P, Petre D, Gordts B, Voss A (2008) Complicated community-acquired soft tissue infection by MRSA from porcine origin. Infection 36: 590–592.P. DeclercqD. PetreB. GordtsA. Voss2008Complicated community-acquired soft tissue infection by MRSA from porcine origin.Infection36590592
- 10. Van Hoecke H, Piette A, De Leenheer E, Lagasse N, Struelens M, et al. (2009) Destructive otomastoiditis by MRSA from porcine origin. Laryngoscope 119: 137–140.H. Van HoeckeA. PietteE. De LeenheerN. LagasseM. Struelens2009Destructive otomastoiditis by MRSA from porcine origin.Laryngoscope119137140
- 11. Lozano C, Aspiroz C, Ezpeleta AI, Gomez-Sanz E, Zarazaga M, et al. (2011) Empyema caused by MRSA ST398 with atypical resistance profile, Spain. Emerging infectious diseases 17: 138–140.C. LozanoC. AspirozAI EzpeletaE. Gomez-SanzM. Zarazaga2011Empyema caused by MRSA ST398 with atypical resistance profile, Spain.Emerging infectious diseases17138140
- 12. van der Mee-Marquet N, Francois P, Domelier-Valentin AS, Coulomb F, Decreux C, et al. (2011) Emergence of unusual bloodstream infections associated with pig-borne-like Staphylococcus aureus ST398 in France. Clin Infect Dis 52: 152–153.N. van der Mee-MarquetP. FrancoisAS Domelier-ValentinF. CoulombC. Decreux2011Emergence of unusual bloodstream infections associated with pig-borne-like Staphylococcus aureus ST398 in France.Clin Infect Dis52152153
- 13. Khanna T, Friendship R, Dewey C, Weese JS (2008) Methicillin resistant Staphylococcus aureus colonization in pigs and pig farmers. Vet Microbiol 128: 298–303.T. KhannaR. FriendshipC. DeweyJS Weese2008Methicillin resistant Staphylococcus aureus colonization in pigs and pig farmers.Vet Microbiol128298303
- 14. 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.TC SmithMJ MaleAL HarperJS KroegerGP Tinkler2009Methicillin-resistant Staphylococcus aureus (MRSA) strain ST398 is present in midwestern U.S. swine and swine workers.PLoS ONE4e4258
- 15. 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.GR GoldingL. BrydenPN LevettRR McDonaldA. Wong2010Livestock-associated methicillin-resistant Staphylococcus aureus sequence type 398 in humans, Canada.Emerg Infect Dis16587594
- 16. Weese JS, Reid-Smith R, Rousseau J, Avery B (2010) Methicillin-resistant Staphylococcus aureus (MRSA) contamination of retail pork. Can Vet J 51: 749–752.JS WeeseR. Reid-SmithJ. RousseauB. Avery2010Methicillin-resistant Staphylococcus aureus (MRSA) contamination of retail pork.Can Vet J51749752
- 17. Weese JS, Avery BP, Reid-Smith RJ (2010) Detection and quantification of methicillin-resistant Staphylococcus aureus (MRSA) clones in retail meat products. Lett Appl Microbiol 51: 338–342.JS WeeseBP AveryRJ Reid-Smith2010Detection and quantification of methicillin-resistant Staphylococcus aureus (MRSA) clones in retail meat products.Lett Appl Microbiol51338342
- 18. Lozano C, Lopez M, Gomez-Sanz E, Ruiz-Larrea F, Torres C, et al. (2009) Detection of methicillin-resistant Staphylococcus aureus ST398 in food samples of animal origin in Spain. J Antimicrob Chemother 64: 1325–1326.C. LozanoM. LopezE. Gomez-SanzF. Ruiz-LarreaC. Torres2009Detection of methicillin-resistant Staphylococcus aureus ST398 in food samples of animal origin in Spain.J Antimicrob Chemother6413251326
- 19. de Boer E, Zwartkruis-Nahuis JT, Wit B, Huijsdens XW, de Neeling AJ, et al. (2009) Prevalence of methicillin-resistant Staphylococcus aureus in meat. Int J Food Microbiol 134: 52–56.E. de BoerJT Zwartkruis-NahuisB. WitXW HuijsdensAJ de Neeling2009Prevalence of methicillin-resistant Staphylococcus aureus in meat.Int J Food Microbiol1345256
- 20. van Loo IH, Diederen BM, Savelkoul PH, Woudenberg JH, Roosendaal R, et al. (2007) Methicillin-resistant Staphylococcus aureus in meat products, the Netherlands. Emerg Infect Dis 13: 1753–1755.IH van LooBM DiederenPH SavelkoulJH WoudenbergR. Roosendaal2007Methicillin-resistant Staphylococcus aureus in meat products, the Netherlands.Emerg Infect Dis1317531755
- 21. Pu S, Han F, Ge B (2008) Isolation and Characterization of Methicillin-Resistant Staphylococcus aureus from Louisiana Retail Meats. Appl Environ Microbiol. S. PuF. HanB. Ge2008Isolation and Characterization of Methicillin-Resistant Staphylococcus aureus from Louisiana Retail Meats.Appl Environ Microbiol
- 22. Chan P, Wakeman S, Angelone A, Mermel L (2008) Investigation of multi-drug resistant microbes in retail meats. Food, Agriculture & Environment 6: 71–75.P. ChanS. WakemanA. AngeloneL. Mermel2008Investigation of multi-drug resistant microbes in retail meats.Food, Agriculture & Environment67175
- 23. 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.BM HansonAE DresslerAL HarperRP ScheibelSE Wardyn2011Prevalence of Staphylococcus aureus and methicillin-resistant Staphylococcus aureus (MRSA) on retail meat in Iowa.Journal of Infection and Public Health4169174
- 24. 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.AE WatersT. Contente-CuomoJ. BuchhagenCM LiuL. Watson2011Multidrug-Resistant Staphylococcus aureus in US Meat and Poultry.Clin Infect Dis5212271230
- 25. Bosgelmez-Tinaz G, Ulusoy S, Aridogan B, Coskun-Ari F (2006) Evaluation of different methods to detect oxacillin resistance in Staphylococcus aureus and their clinical laboratory utility. Eur J Clin Microbiol Infect Dis 25: 410–412.G. Bosgelmez-TinazS. UlusoyB. AridoganF. Coskun-Ari2006Evaluation of different methods to detect oxacillin resistance in Staphylococcus aureus and their clinical laboratory utility.Eur J Clin Microbiol Infect Dis25410412
- 26. Lina G, Piemont Y, Godail-Gamot F, Bes M, Peter MO, et al. (1999) Involvement of Panton-Valentine leukocidin-producing Staphylococcus aureus in primary skin infections and pneumonia. Clin Infect Dis 29: 1128–1132.G. LinaY. PiemontF. Godail-GamotM. BesMO Peter1999Involvement of Panton-Valentine leukocidin-producing Staphylococcus aureus in primary skin infections and pneumonia.Clin Infect Dis2911281132
- 27. 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: 1008–1015.MC EnrightNP DayCE DaviesSJ PeacockBG Spratt2000Multilocus sequence typing for characterization of methicillin-resistant and methicillin-susceptible clones of Staphylococcus aureus.J Clin Microbiol3810081015
- 28. Koreen L, Ramaswamy SV, Graviss EA, Naidich S, Musser JM, et al. (2004) spa typing method for discriminating among Staphylococcus aureus isolates: implications for use of a single marker to detect genetic micro- and macrovariation. J Clin Microbiol 42: 792–799.L. KoreenSV RamaswamyEA GravissS. NaidichJM Musser2004spa typing method for discriminating among Staphylococcus aureus isolates: implications for use of a single marker to detect genetic micro- and macrovariation.J Clin Microbiol42792799
- 29. CLSI (2006) Methods for Dilution Antimicrobial Susceptibility Tests for Bacteria that Grow Aerobically. Approved standard M07-A7. In: Institute CaLS, editor. Villanova, PA: Clinical and Laboratory Standards Institute. CLSI2006Methods for Dilution Antimicrobial Susceptibility Tests for Bacteria that Grow Aerobically. Approved standard M07-A7.CaLS InstituteVillanova, PAClinical and Laboratory Standards Institute
- 30. CLSI (2009) CLSI2009Performance standards for antimicrobial susceptibility testing; nineteenth informational supplement. Performance standards for antimicrobial susceptibility testing; nineteenth informational supplement.
- 31. Leedom Larson KR, Harper AL, Hanson BM, Male MJ, Wardyn SE, et al. (2011) Methicillin-resistant Staphylococcus aureus in pork production shower facilities. Appl Environ Microbiol 77: 696–698.KR Leedom LarsonAL HarperBM HansonMJ MaleSE Wardyn2011Methicillin-resistant Staphylococcus aureus in pork production shower facilities.Appl Environ Microbiol77696698
- 32. Maree CL, Daum RS, Boyle-Vavra S, Matayoshi K, Miller LG (2007) Community-associated methicillin-resistant Staphylococcus aureus isolates causing healthcare-associated infections. Emerg Infect Dis 13: 236–242.CL MareeRS DaumS. Boyle-VavraK. MatayoshiLG Miller2007Community-associated methicillin-resistant Staphylococcus aureus isolates causing healthcare-associated infections.Emerg Infect Dis13236242
- 33. Vandenesch F, Naimi T, Enright MC, Lina G, Nimmo GR, et al. (2003) Community-acquired methicillin-resistant Staphylococcus aureus carrying Panton-Valentine leukocidin genes: worldwide emergence. Emerg Infect Dis 9: 978–984.F. VandeneschT. NaimiMC EnrightG. LinaGR Nimmo2003Community-acquired methicillin-resistant Staphylococcus aureus carrying Panton-Valentine leukocidin genes: worldwide emergence.Emerg Infect Dis9978984
- 34. Wertheim HF, Vos MC, Boelens HA, Voss A, Vandenbroucke-Grauls CM, et al. (2004) Low prevalence of methicillin-resistant Staphylococcus aureus (MRSA) at hospital admission in the Netherlands: the value of search and destroy and restrictive antibiotic use. J Hosp Infect 56: 321–325.HF WertheimMC VosHA BoelensA. VossCM Vandenbroucke-Grauls2004Low prevalence of methicillin-resistant Staphylococcus aureus (MRSA) at hospital admission in the Netherlands: the value of search and destroy and restrictive antibiotic use.J Hosp Infect56321325
- 35. Van Cleef BA, Broens EM, Voss A, Huijsdens XW, Zuchner L, et al. (2010) High prevalence of nasal MRSA carriage in slaughterhouse workers in contact with live pigs in The Netherlands. Epidemiol Infect 1–8.BA Van CleefEM BroensA. VossXW HuijsdensL. Zuchner2010High prevalence of nasal MRSA carriage in slaughterhouse workers in contact with live pigs in The Netherlands.Epidemiol Infect18
- 36. Mulders MN, Haenen AP, Geenen PL, Vesseur PC, Poldervaart ES, et al. (2010) Prevalence of livestock-associated MRSA in broiler flocks and risk factors for slaughterhouse personnel in The Netherlands. Epidemiol Infect 1–13.MN MuldersAP HaenenPL GeenenPC VesseurES Poldervaart2010Prevalence of livestock-associated MRSA in broiler flocks and risk factors for slaughterhouse personnel in The Netherlands.Epidemiol Infect113
- 37. Smith TC, Pearson N (2011) The Emergence of Staphylococcus aureus ST398. Vector Borne Zoonotic Dis 11: 327–39.TC SmithN. Pearson2011The Emergence of Staphylococcus aureus ST398.Vector Borne Zoonotic Dis1132739
- 38. Sunde M, Tharaldsen H, Marstein L, Haugum M, Norstrom M, et al. (2011) Detection of methicillin-resistant Staphylococcus aureus sequence type 8 in pigs, production environment, and human beings. J Vet Diagn Invest 23: 348–350.M. SundeH. TharaldsenL. MarsteinM. HaugumM. Norstrom2011Detection of methicillin-resistant Staphylococcus aureus sequence type 8 in pigs, production environment, and human beings.J Vet Diagn Invest23348350
- 39. 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.BV LowderCM GuinaneNL Ben ZakourLA WeinertA. Conway-Morris2009Recent human-to-poultry host jump, adaptation, and pandemic spread of Staphylococcus aureus.Proc Natl Acad Sci U S A1061954519550
- 40. de Jonge R, Verdier JE, Havelaar AH (2010) Prevalence of meticillin-resistant Staphylococcus aureus amongst professional meat handlers in the Netherlands, March–July 2008. Euro Surveillance 15: 19712.R. de JongeJE VerdierAH Havelaar2010Prevalence of meticillin-resistant Staphylococcus aureus amongst professional meat handlers in the Netherlands, March–July 2008.Euro Surveillance1519712