Prevalence of Clostridium difficile in Uncooked Ground Meat Products from Pittsburgh, Pennsylvania

Division of Infectious Diseases, University of Pittsburgh School of Medicine, and Department of Epidemiology, Graduate School of Public Health, University of Pittsburgh, Pittsburgh, Pennsylvania, USA.
Applied and Environmental Microbiology (Impact Factor: 3.67). 04/2012; 78(12):4183-6. DOI: 10.1128/AEM.00842-12
Source: PubMed


The prevalence of Clostridium difficile in retail meat samples has varied widely. The food supply may be a source for C. difficile infections. A total of 102 ground meat and sausage samples from 3 grocers in Pittsburgh, PA, were cultured for C. difficile. Brand A pork sausages were resampled between May 2011 and January 2012. Two out of 102 (2.0%) meat products initially sampled
were positive for C. difficile; both were pork sausage from brand A from the same processing facility (facility A). On subsequent sampling of brand A products,
10/19 samples from processing facility A and 1/10 samples from 3 other facilities were positive for C. difficile. The isolates recovered were inferred ribotype 078, comprising 6 genotypes. The prevalence of C. difficile in retail meat may not be as high as previously reported in North America. When contamination occurs, it may be related to
events at processing facilities.

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    • "Antigenic confirmation of toxigenicity was verified on the isolates using two ELISA kits, one for toxins A/B and another for toxin A (TechLab/Wampole), and Vero cell cultures using products and reagents exactly as previously described [18], ensuring the prevention of refrigeration-induced false-positive reactions as recently reported [19]. All antiseptic measures were in place to prevent sample cross-contamination in the laboratory as deemed necessary for C. difficile studies on food safety [20]. In addition, the fire-resistant countertop used during sample processing was in the following order: (i) swabbed every 5–10 samples with autoclaved unscented commercial cloths (Swiffer, 10 × 15 cm) premoistened with 5 mL of phosphate buffer saline, (ii) disinfected with 10% bleach, then with 70% ethanol, and (iii) finally flamed with a laboratory torch at a pace we had proved that eliminates spores of C. difficile PCR ribotypes 078 and 027 (common strains identified in foods and animals). "
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    ABSTRACT: We (i) determined the prevalence of Clostridium difficile and their antimicrobial resistance to six antimicrobial classes, in a variety of fresh vegetables sold in retail in Ohio, USA, and (ii) conducted cumulative meta-analysis of reported prevalence in vegetables since the 1990s. Six antimicrobial classes were tested for their relevance as risk factors for C. difficile infections (CDIs) (clindamycin, moxifloxacin) or their clinical priority as exhaustive therapeutic options (metronidazole, vancomycin, linezolid, and tigecycline). By using an enrichment protocol we isolated C. difficile from three of 125 vegetable products (2.4%). All isolates were toxigenic, and originated from 4.6% of 65 vegetables cultivated above the ground (; outer leaves of iceberg lettuce, green pepper, and eggplant). Root vegetables yielded no C. difficile. The C. difficile isolates belonged to two PCR ribotypes, one with an unusual antimicrobial resistance for moxifloxacin and clindamycin (lettuce and pepper; 027-like, A+B+CDT+; tcdC 18 bp deletion); the other PCR ribotype (eggplant, A+B+ CDT−; classic tcdC) was susceptible to all antimicrobials. Results of the cumulative weighted meta-analysis (6 studies) indicate that the prevalence of C. difficile in vegetables is 2.1% and homogeneous since the first report in 1996 (2.4%). The present study is the first report of the isolation of C. difficile from retail vegetables in the USA. Of public health relevance, antimicrobial resistance to moxifloxacin/clindamycin (a bacterial-associated risk factor for severe CDIs) was identified on the surface of vegetables that are consumed raw.
    Full-text · Article · Dec 2014
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    • "Our finding of C. difficile and its toxigenic strains in meat are supported by similar reports from other counters [9,15,16,20-23]. The low prevalence of C. difficile in cow, beef, goat and sheep meat samples are comparable with those reported by others [16,20-23]. However, higher contamination rates (20% to 50%) have also been reported [9,15]. "
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    ABSTRACT: Clostridium difficile has been shown to be a nosocomial pathogen associated with diarrhoea and pseudomembranous colitis in hospitalised patients and the infection is believed to be acquired nosocomially. Recent studies have shown the occurrence of C. difficile in food animals which may act as a source of infection to humans.The aim of this study was to determine the occurrence of C. difficile in retail raw beef, cow, sheep, goat, camel and buffalo meat in Iran. From April to October 2012, a total of 660 raw meat samples from beef, cow, sheep, goat, camel and buffalo were purchased from 49 butcheries in Isfahan and Khuzestan provinces, Iran, and were evaluated for the presence of C. difficile using a method including selective enrichment in C. difficile broth, subsequent alcohol shock-treatment and plating onto C. difficile selective medium. C. difficile isolates were tested for the presence of toxin genes and were typed using PCR ribotyping. In this study, 13 of 660 meat samples (2%) were contaminated with C. difficile. The highest prevalence of C. difficile was found in buffalo meat (9%), followed by goat meat (3.3%), beef meat (1.7%), cow (0.94%) and sheep meat (0.9%). Seven of the 13C. difficile strains (53.9%) were positive for tcdA, tcdB and cdtB toxin genes and were classified as ribotype 078. Four strains (30.8%) were positive tcdA, and tcdB, and one strain (7.7%) was possessed only tcdB. The remaining isolate was non-toxigenic. Susceptibilities of 13C. difficile isolates were determined for 11 antimicrobial drugs using the disk diffusion assay. Resistance to clindamycin, gentamycin, and nalidixic acid was the most common finding. To our knowledge, the present study is the first report of the isolation of C. difficile from raw buffalo meat. This study indicates the potential importance of food, including buffalo meat, as a source of transmission of C. difficile to humans.
    Full-text · Article · Feb 2014 · BMC Public Health
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    • "Studies in various countries have determined differences in the prevalence of C. difficile in animals just before slaughter (Baker et al., 2010; Hoffer et al., 2010; Houser et al., 2012; Keeseen et al., 2011; Rodriguez et al., 2012). In addition, many types, including PCR-ribotype 078, are present in humans, animals (Debast et al., 2009; Janezic et al., 2012) and meat (Boer et al., 2011; Curry et al., 2012; Weese et al., 2009). The PCRribotype 078 was among the three most prevalent ribotypes of C. difficile isolated from humans in Europe in 2009 (Bauer et al., 2011), and it also appears to be associated with increased virulence (Goorhuis et al., 2008) as the highly virulent epidemic strain C. difficile 027 (Kuijper et al., 2006). "
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    ABSTRACT: The objective of this study was to evaluate the presence of Clostridium difficile in intestinal and carcass samples collected from pigs and cattle at a single slaughterhouse. C. difficile was isolated in 1% and 9.9% of the pig and cattle intestinal contents and in 7.9% and 7% of cattle and pig carcass samples respectively. A total of 19 different PCR-ribotypes were identified, among them types 078 and 014. Seven of 19 ribotypes correlated with the PCR-ribotypes involved in human C. difficile infections in Belgium. This study confirms that animals are carriers of C. difficile at slaughter and ribotypes are identical than those in humans, and that carcass contamination occurs inside the slaughterhouse.
    Full-text · Article · Jul 2013 · International journal of food microbiology
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