Clostridium difficile in Retail Meat Products, USA, 2007

To determine the presence of Clostridium difficile, we sampled cooked and uncooked meat products sold in Tucson, Arizona. Forty-two percent contained toxigenic C. difficile strains (either ribotype 078/toxinotype V [73%] or 027/toxinotype III [NAP1 or NAP1-related; 27%]). These findings indicate that food products may play a role in interspecies C. difficile transmission.

T he incidence and severity of Clostridium diffi cile infections (CDIs) are increasing in North America (1), probably because of emergence of an epidemic strain (NAP1/ BI/027, toxinotype [TT] III) (2,3). C. diffi cile transmission occurs primarily in healthcare facilities, but community-associated CDI (CA-CDI) appears to be increasing and may now account for 20%-45% of positive diagnostic assay results (4,5). Up to 35% of patients with CA-CDI report no antimicrobial agent use within 3 months before disease onset (4,5), although nonantimicrobial drugs (e.g., proton pump inhibitors, nonsteroidal antiinfl ammatory agents) are also implicated as risk factors (4). Sources of C. diffi cile acquisition in community settings are unknown.
CDI is increasingly important in food animals (6). Infection rates of >95% have been documented among neonatal pigs in farrowing facilities, resulting in diarrhea and typhlocolitis (6). Toxigenic C. diffi cile is also implicated as a cause of diarrhea in calves (7). C. diffi cile was identifi ed in raw meat intended for pet consumption (8) and in ≈20% of retail ground beef in Canada (9). We report the isolation of C. diffi cile from uncooked and ready-to-eat meats in retail markets in a US metropolitan area.

The Study
Packaged meats were purchased from 3 national-chain grocery stores in the Tucson, Arizona, area on 3 occasions at 1-month intervals from January to April 2007. Prod-ucts sampled were both uncooked (ground beef, ground pork, ground turkey, pork sausage, and pork chorizo) and ready to eat (beef summer sausage, pork braunschweiger) (Table). Pork chorizo was produced and distributed locally; all other samples were national brands. Products with different sell-by dates (a surrogate for production date) were sampled for each meat type. Samples were not representative of all meat products in each grocery store.
Proportions were compared by χ 2 or Fisher exact test. Thirty-seven (42.0%) of 88 retail meats yielded C. diffi cile, including 42.4% of beef, 41.3% of pork, and 44.4% of turkey products (Table). Ready-to-eat products were more commonly culture positive (11/23; 47.8%) than were uncooked meats (26/65; 40.0%), although the difference was not signifi cant (p = 0.34). The highest percentages of C. diffi cile isolates were recovered from pork braunschweiger (62.5%) and ground beef (50.0%). Culture-positive results came from both heat-shocked and non-heat-shocked cultures, whereas culture-negative specimens were negative in both types of culture, and no specimen was positive by both methods (not shown). No association was found with the meat processor, the sell-by date, the store, or the month sampled (not shown). Multiple independent cultures from 2 braunschweiger samples yielded indistinguishable isolates in the same meat sample (10/10 from 1 package and 12/12 from another; not shown), which suggests that a single strain may predominate when C. diffi cile is present. Our percentage of recovery of C. diffi cile from retail meat products is higher than that reported (20%) in a similar study of Canadian ground beef (9), possibly because of differences in culture methods, the meats sampled, or national or geographic variation.
Ribotype 027 isolates are described almost exclusively in context of the current human epidemic strain, NAP1/027/ TT III (2). In this study, we also found 027/TT III isolates that were only 78% similar to NAP1 (i.e., NAP1-related). Ribotype 078 strains were previously uncommon causes of healthcare-associated CDI in humans (12), but now they are emerging in pigs and calves with diarrhea (7; J.S. Weese, pers. comm.) and in persons with CDI (12). Two epidemiologically unrelated 078/TT V isolates from human CDI patients are indistinguishable by PFGE from pig isolates (12).
The 078/TT V isolates were uniformly susceptible to levofl oxacin, moxifl oxacin, and gatifl oxacin. Like human TT V isolates (12), most 078/TT V meat isolates were nonsusceptible to clindamycin (56% resistant, 41% intermediate). This may not be surprising given the widespread use of tylosin, erythromycin, virginiamycin, and lincomycin in food animals and the potential for selection of macrolidelincosamide-streptogramin resistance (14).

Conclusions
Fluoroquinolones are widely used in human therapy, and the current epidemic strain may have emerged because of its resistance to these agents. Fluoroquinolone use is limited in food animal production (14), with the exception of enrofl oxacin for treatment of bovine respiratory disease (now approved for use in swine).
The source of C. diffi cile in retail meats may involve antemortem deposition of spores in the animal's muscle or other tissues, fecal or environmental contamination of carcasses, or contamination during processing. Spores could persist in packing plants, resulting in contamination of carcasses or food products during processing. Contamination may also occur in retail meat markets.
Direct or indirect human-to-human transmission is responsible for most healthcare-related CDIs (15) and most likely contributes to CA-CDI. Therefore, stopping such  transmission remains the critical control point for preventing most human CDIs. Nonetheless, our fi ndings highlight the potential both for selection of virulent or resistant strains in animals and interspecies transmission through the food supply. Our data do not prove transmission of C. diffi cile from foods to humans but highlight the need for studies to characterize risks posed by this organism in the human food supply.
The study was partially supported by grant 2003-35204-13786 from the US Department of Agriculture-Cooperative State Research, Education, and Extension Service-National Research Initiative.
Dr Songer is professor of Veterinary Science and Microbiology at the University of Arizona. His research interests focus on bacterial diseases of food animals, mainly those affecting the gastrointestinal tract.