Suggested citation for this article: Bhargava K, Wang X, Donabedian S, Zervos M, da Rocha L, Zhang Y. Methicillin-resistant Staphylococcus aureus in retail meat, Detroit, Michigan, USA [letter]. Emerg Infect Dis. 2011 Jun; [Epub ahead of print]
Methicillin-resistant Staphylococcus aureus in Retail Meat, Detroit, Michigan, USA
To the Editor: Because methicillin-resistant Staphylococcus aureus (MRSA) has been identified in retail meat worldwide (1–4), the potential exists for its transmission to humans. Of the various meat products surveyed, pork had the highest contamination rate in the United States and Canada (1,2), as did beef in Korea (3) and poultry in the Netherlands (4). The study in Korea also observed MRSA from chicken, which demonstrated sequence type (ST) 692 by multilocus sequence typing (MLST), a type distinct from that isolated in beef and pork. Despite sample size variations, these studies suggested that MRSA contamination in different meat categories can vary by location and that molecular distinction may exist among MRSA isolates in meat of different origin.
We collected 289 raw meat samples (156 beef, 76 chicken, and 57 turkey) from 30 grocery stores in Detroit, Michigan, USA, during August 2009–January 2010. Up to 3 presumptive S. aureus colonies per sample were identified by coagulase test and species-specific PCR (1). Antimicrobial drug MICs were determined and interpreted according to Clinical and Laboratory Standards Institute guidelines (5). S. aureus were characterized by pulsed-field gel electrophoresis (PFGE), mecA identification, SCCmec typing, Panton-Valentine leukocidin identification, agr typing, MLST, and spa typing as described (1,6).
Sixty-five (22.5%) samples yielded S. aureus: 32 beef (20.5%), 19 chicken (25.0%), and 14 turkey (24.6%) samples. Six samples, consisting of 2 beef (1.3%), 3 chickens (3.9%), and 1 turkey (1.7%), were positive for MRSA as evidenced by the presence of mecA. The overall lower prevalence of S. aureus and MRSA than found in a previous study in the United States (40% and 5%, respectively) (1) might be explained by our exclusion of pork because pork and swine production have been major reservoirs of MRSA (4,7). However, different geographic location Page 2 of 4
and cold sampling seasons in this study also might have caused the variations. The only multidrug-resistant MRSA isolate in this study (MRSA1) was from beef and was resistant to ß-lactams, macrolides, and fluoroquinolones (Figure).
Although an extra band was generated in MRSA2a, 2b, 3, 5, and 6 by PFGE, all 9 MRSA isolates belonged to USA300 (Figure). Multiple isolates from the same samples (MRSA2a and 2b; MRSA4a, 4b, and 4c) demonstrated indistinguishable PFGE patterns and other characteristics, which suggested identical MRSA clones. Moreover, MLST, SCCmec typing, agr typing, and pvl detection showed all strains to be positive for ST8, SCCmec IVa, agr I, and Panton-Valentine leukocidin, which are typical characteristics of USA300 clones. However, spa typing identified 2 distinct spa types, t008 (11–19–12-21–17-34–24–34–22–25) and t2031 (11–19–12-12–34-34–24–34–22–25) (repeat variants in boldface), which differed by 5 nucleotides. t008, the most common spa type of USA300, was identified in 6 isolates of beef, chicken, and turkey origin, whereas t2031 was recovered from MRSA4a, 4b, and 4c from a chicken sample. The nucleotide variation in t2031 caused amino acid changes from glycine-asparagine in t008 to asparagine-lysine. The single nucleotide difference between repeats 12 (GGT) and 21 (GGC) and repeats 34 (AAA) and 17 (AAG) resulted in no amino acid change, with glycine and lysine encoded, respectively.
Unlike studies in Europe, where researchers have reported the animal MRSA clone ST398 from various meat products (4), all MRSA isolates in our study were USA300, which suggests a possible human source of contamination during meat processing (1). The failure to identify ST398 in the US retail meat also indicates that the human MRSA clones might be better adapted in meat processing than ST398 in this country. Since ST398 is widespread in animals and meat in Europe and has been isolated from other parts of the world (8), it is not too bold to predict that ST398 might appear in US meat in the future, especially after the recent report of ST398 from US swine (7).
The 5-nt difference between t2031 and t008 implicates multiple MRSA clones in poultry. Previous studies have shown spa variants of USA300 from clinical cases associated with distinctive symptoms (9,10). A single repeat variant, t024, showed substantial genetic, epidemiologic, and clinical differences from t008 in Denmark (10). Researchers in Japan also recovered 2 spa variants of USA300: t024, which causes blood infections, and t711, which is Page 3 of 4
associated with subcutaneous abscesses (9). In both studies, t024 behaved as hospital-associated MRSA, suggesting that spa variants of USA300 could lead to different clinical outcomes. Therefore, we can reasonably assume that variants with a meat origin also might have different public health implications; further research on their virulence potential would be helpful to elucidate this possibility.
Despite the recovery of MRSA from retail chicken and t2031 that has an antibiogram distinct from t008, except for ß-lactam resistance, several questions remain about whether more spa variants are present in poultry (or meat). These include whether t2031 is more adaptable to chicken production because of the 2 amino acid difference from t008, or whether t2031 is linked with specific antimicrobial drug resistance phenotypes other than ß-lactam resistance.
Kanika Bhargava, Xiaogang Wang, Susan Donabedian, Marcus Zervos, Liziane da Rocha, and Yifan Zhang
Author affiliations: Wayne State University, Detroit, Michigan, USA (K. Bhargava, X. Wang, L. da Rocha, Y. Zhang) and Henry Ford Health Systems, Detroit (S. Donabedian, M. Zervos)
1. Pu S, Han F, Ge B. Isolation and characterization of methicillin-resistant Staphylococcus aureus strains from Louisiana retail meats. Appl Environ Microbiol. 2009;75:265–7. PubMed doi:10.1128/AEM.01110-08
2. Weese JS, Avery BP, Reid-Smith RJ. Detection and quantification of methicillin-resistant Staphylococcus aureus (MRSA) clones in retail meat products. Lett Appl Microbiol. 2010;51:338–42. PubMed doi:10.1111/j.1472-765X.2010.02901.x
3. Lim SK, Nam HM, Park HJ, Lee HS, Choi MJ, Jung SC, et al. Prevalence and characterization of methicillin-resistant Staphylococcus aureus in raw meat in Korea. J Microbiol Biotechnol. 2010;20:775–8. PubMed
4. de Boer E, Zwartkruis-Nahuis JT, Wit B, Huijsdens XW, de Neeling AJ, Bosch T, et al. Prevalence of methicillin-resistant Staphylococcus aureus in meat. Int J Food Microbiol. 2009;134:52–6. PubMed doi:10.1016/j.ijfoodmicro.2008.12.007
5. Clinical and Laboratory Standards Institute. Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically, 7th ed. Wayne (PA): The Institute; 2006. Page 4 of 4
6. Strommenger B, Cuny C, Werner G, Witte W. Obvious lack of association between dynamics of epidemic methicillin-resistant Staphylococcus aureus in central Europe and agr specificity groups. Eur J Clin Microbiol Infect Dis. 2004;23:15–9. PubMed doi:10.1007/s10096-003-1046-8
7. Smith TC, Male MJ, Harper AL, Kroeger JS, Tinkler GP, Moritz ED, et al. Methicillin-resistant Staphylococcus aureus (MRSA) strain ST398 is present in midwestern U.S. swine and swine workers. PLoS ONE. 2009;4:e4258. PubMed doi:10.1371/journal.pone.0004258
8. Weese JS, Reid-Smith R, Rousseau J, Avery B. Methicillin-resistant Staphylococcus aureus (MRSA) contamination of retail pork. Can Vet J. 2010;51:749–52. PubMed
9. Higuchi W, Mimura S, Kurosawa Y, Takano T, Iwao Y, Yabe S, et al. Emergence of the community-acquired methicillin-resistant Staphylococcus aureus USA300 clone in a Japanese child, demonstrating multiple divergent strains in Japan. J Infect Chemother. 2010;16:292–7. PubMed doi:10.1007/s10156-010-0051-y
10. Larsen AR, Goering R, Stegger M, Lindsay JA, Gould KA, Hinds J, et al. Two distinct clones of methicillin-resistant Staphylococcus aureus (MRSA) with the same USA300 pulsed-field gel electrophoresis profile: a potential pitfall for identification of USA300 community-associated MRSA. J Clin Microbiol. 2009;47:3765–8. PubMed doi:10.1128/JCM.00934-09
Address for correspondence: Yifan Zhang, Department of Nutrition and Food Science, Wayne State University, 3009 Science Hall, 5045 Cass Ave, Detroit, MI 48202, USA; email: email@example.com
Figure. Dendrogram showing comparison of SmaI pulsed-field gel electrophoresis patterns, SCCmec type, PVL content, and agr type of methicillin-resistant Staphylococcus aureus (MRSA) isolated from meat samples. All MRSA isolates were resistant to ß-lactam antimicrobial drugs (ampicillin, penicillin, and oxacillin) and grew on the 6 µg/mL of cefoxitin for screening methicillin resistance. *Isolates with the same arabic numbers were from the same sample; †only resistance to non–ß-lactam antimicrobial drugs was listed. ID, identification; MLST, multilocus sequence typing; PVL, Panton-Valentine leukocidin; CIP, ciprofloxacin; ERY, erythromycin; LEVO, levofloxacin; TET, tetracycline.
May 11, 2011
Human-type MRSA found in Detroit raw meat
Researchers testing retail meat samples in Detroit found that almost a fourth contained Staphylococcus aureus and 2% contained methicillin-resistant S aureus (MRSA). In a letter to Emerging Infectious Diseases today, the scientists report that they collected 289 raw meat samples (156 beef, 76 chicken, and 57 turkey) from 30 grocery stores from August 2009 through January 2010. Of those samples, 65 (22.5%) yielded S aureus via coagulase test and polymerase chain reaction (PCR): 32 beef (20.5%), 19 chicken (25.0%), and 14 turkey (24.6%) samples. Six samples (2 beef [1.3%], 3 chicken [3.9%], and 1 turkey [1.7%]), were positive for MRSA, while only one sample, a beef one, contained multidrug-resistant MRSA. Furthermore, the MRSA was the human type, USA300, which the authors said could indicate a human rather than animal source of meat contamination. They said similar studies in European meat typically show ST398, an animal MRSA clone. They noted that the percentage of positive MRSA samples is lower than in an earlier study in Louisiana meat, perhaps because the Michigan researchers didn't test pork, noting that swine production has been identified as a reservoir of MRSA. They wrote that although USA300 might be better adapted to meat processing in the United States, ST398 might someday appear as a contaminant in US meat, given its recent identification in US swine.
Monday, April 18, 2011
Multidrug-Resistant Staphylococcus aureus in US Meat and Poultry
Tuesday, May 10, 2011
Food safety for whom? Corporate wealth versus people's health
Horizon Acres 3/18/11
Department of Health and Human Services Public Health Service Food and Drug Administration Cincinnati District Office Central Region 6751 Steger Drive Cincinnati, OH 45237-30977 Telephone: (513) 679-2700 FAX: (513) 679-2761
WARNING LETTER CIN-11-65585-06
March 18, 2011
United Parcel Service
Mr. Kenneth D. Weaver, General Manager Horizon Acres 6728 Zuercher Road
Dalton, Ohio 44618
Dear Mr. Weaver:
On November 10, 12, 19,24, 2010, and December 20, 2010, the U.S. Food and Drug Administration (FDA) conducted an investigation of your veal calf operation located at 6728 Zuercher Road, Dalton, Ohio 44618. This letter notifies you of the violations of the Federal Food, Drug, and Cosmetic Act (the FD&C Act) that we found during our investigation of your operation. You can find the FD&C Act and its associated regulations on the Internet through links on FDA's web page at www.fda.gov1.
We found that you offered for sale an animal for slaughter as food that was adulterated. Under section 402(a)(2)(C)(ii) of the FD&C Act, 21 U.S.C. § 342(a)(2)(C)(ii), a food is deemed to be adulterated if it bears or contains a new animal drug that is unsafe under section 512 of the FD&C Act, 21 U.S.C. § 360b. Further, under section 402(a)(4) of the FD&C Act, 21 U.S.C. § 342(a)(4), a food is deemed to be adulterated if it has been held under insanitary conditions whereby it may have been rendered injurious to health.
Specifically, our investigation revealed that on or about June 22, 2010, you sold an unidentified, untagged veal calf for slaughter as food. On or about June 22, 2010, (b)(4) slaughtered this animal. United States Department of Agriculture, Food Safety and Inspection Service (USDA/FSIS) analysis of tissue samples collected from this animal identified the presence 0.28 parts per million (ppm) of flunixin in the liver tissue. FDA has established a tolerance of 0.125 ppm for residues of flunixin in the liver of cattle as codified in 21 C.F.R. 556.286(b)(1)(i). However, this tolerance does not apply to use of Suppressor (flunixin meglumine) Injectable Solution, ANADA 200-308, in veal calves (pre-ruminating calves), and there is no acceptable level of residue associated with use of flunixin meglumine in veal calves (pre-ruminating calves). The presence of this drug in edible tissue from this animal in this amount causes the food to be adulterated within the meaning of section 402(a)(2)(C)(ii) of the FD&C Act, 21 U.S.C. § 342(a)(2)(C)(ii).
Our investigation also found that you hold animals under conditions that are so inadequate that medicated animals bearing potentially harmful drug residues are likely to enter the food supply. For example, you failed to maintain complete treatment records and segregate treated animals. Food from animals held under such conditions is adulterated within the meaning of section 402(a)(4) of the FD&C Act, 21 U.S.C. § 342(a)(4).
We also found that you adulterated the new animal drugs Suppressor (flunixin meglumine) ANADA 200-308, Dexamethasone ANADA 200-312, Ceftiflex sterile powder (ceftiofur sodium) ANADA 200-420, PennOne Pro (penicillin G procaine) NADA 65-010, Amoxicillin capsules NDC 65862-017-05, Sulfamethoxazole and Trimethoprim Double Strength tablets NDC 53746-272-05 (SMZ-TMP tablets), and Pennchlor 64 (chlortetracycline HCI) ANADA 200-295. Specifically, our investigation revealed that you did not use these drugs as directed by their approved labeling. Use of these drugs in this manner is an extralabel use. 21 C.F.R. § 530.3(a).
The extralabel use of approved animal or human drugs in animals is allowed under the FD&C Act only if the extralabel use complies with sections 512(a)(4) and (5) of the FD&C Act, 21 U.S.C. § 360b(a)(4) and (5), and 21 C.F.R. Part 530, including that the use must be by or on the lawful order of a licensed veterinarian within the context of a valid veterinarian/client/patient relationship.
Our investigation found that you administered flunixin meglumine to veal calves without following the withdrawal period as stated in the approved labeling. Your extralabel use of flunixin meglumine was not under the supervision of a licensed veterinarian, in violation of 21 C.F.R. § 530.11(a) and your extralabel use of flunixin meglumine resulted in an illegal drug residue, in violation of 21 C.F.R. § 530.11(c).
Our investigation found that you administered dexamethasone to veal calves without following the route of administration and the withdrawal period as stated in the approved labeling. Your extralabel use of Dexamethasone was not under the supervision of a licensed veterinarian, in violation of 21 C.F.R. § 530.11 (a).
Our investigation found that you administered ceftiofur sodium to veal calves without following the withdrawal period as stated in the approved labeling. Your extralabel use of ceftiofur sodium was not under the supervision of a licensed veterinarian, in violation of 21 C.F.R. § 530.11(a).
Our investigation found that you administered penicillin G procaine to veal calves without following the route of administration and the withdrawal period as stated in the approved labeling. Your extralabel use of penicillin G procaine was not under the supervision of a licensed veterinarian, in violation of 21 C.F.R. § 530.11(a).
Our investigation found that you administered amoxicillin and sulfamethoxazole and trimethoprim (SMZ-TMP) to veal calves without following the route of administration and duration of the treatment as stated in their approved labeling. Your extralabel use of Amoxicillin and SMZ-TMP were not under the supervision of a licensed veterinarian, in violation of 21 C.F.R. § 530.11 (a) and your use of amoxicillin and SMZ-TMP in or on feed, is in violation of 21 C.F.R. § 530.11(b).
Our investigation found that you administered chlortetracycline HCI to veal calves without following the duration of treatment. Your use of chlortetracycline HCI was not under the supervision of a licensed veterinarian, and is in violation of 21 C.F.R. § 530.11
(a) and your use of pennchlor 64 in or on feed, is in violation of 21 C.F.R. § 530.11
(b). Because your use of these drugs was not in conformance with their approved labeling and did not comply with 21 C.F.R. Part 530, you caused the drug(s) to be unsafe under section 512(a) of the FD&C Act, 21 U.S.C. § 360b(a), and adulterated within the meaning of section 501(a)(5) of the FD&C Act, 21 U.S.C. § 351(a)(5).
In addition, you adulterated the liquid animal feed within the meaning of section 501(a)(6) of the FD&C Act, 21 U.S.C. § 351(a)(6), when you added sulfamethoxazole and trimethoprim, Amoxicillin, and chlortetracycline HCI, and you failed to use the medicated feed in conformance with its approved labeling. Your use of this medicated feed without following the animal class as directed by the approved labeling caused this medicated feed to be unsafe under section 512(a)(2) of the FD&C Act, 21 U.S.C. § 360b(a)(2), and adulterated under section 501(a)(6) of the FD&C Act, 21 U.S.C. § 351(a)(6). Section 512 of the FD&C Act, 21 U.S.C. § 360b, and 21 C.F.R. 530.11(b) do not permit the extralabel use of medicated feed.
The above is not intended to be an all-inclusive list of violations. As a producer of animals offered for use as food, you are responsible for ensuring that your overall operation and the food you distribute is in compliance with the law.
You should take prompt action to correct the violations described in this letter and to establish procedures to ensure that these violations do not recur. Failure to do so may result in regulatory action without further notice such as seizure and/or injunction.
You should notify this office in writing of the steps you have taken to bring your firm into compliance with the law within fifteen (15) working days of receiving this letter.
Your response should include each step that has been taken or will be taken to correct the violations and prevent their recurrence. If corrective action cannot be completed within fifteen (15) working days of receiving this letter, state the reason for the delay and the time frame within which the corrections will be completed. Please include copies of any available documentation demonstrating that corrections have been made.
Your written response should be sent to Allison C. Hunter, Compliance Officer, U.S. Food and Drug Administration, 6751 Steger Drive, Cincinnati, Ohio 45237. If you have any questions about this letter, please contact Compliance Officer Hunter at 513-679-2700 ext. 134.
Sincerely yours, /S/
Teresa Thompson District Director Cincinnati District
p.s. update prion disease ;
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STUDY OF ATYPICAL BSE 2010 Annual Report May 2011
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MAD COW ATYPICAL CJD PRION TSE CASES WITH CLASSIFICATIONS PENDING ON THE RISE IN NORTH AMERICA