Salmonella enterica serovar Heidelberg frequently causes food-borne illness in humans. There are few data on the prevalence, antimicrobial susceptibility, and genetic diversity of Salmonella serovar Heidelberg isolates in retail meats. We compared the prevalences of Salmonella serovar Heidelberg in a sampling of 20,295 meats, including chicken breast (n ؍ 5,075), ground turkey (n ؍ 5,044), ground beef (n ؍ 5,100), and pork chops (n ؍ 5,076), collected during 2002 to 2006. Isolates were analyzed for antimicrobial susceptibility and compared genetically using pulsed-field gel electrophoresis (PFGE) and PCR for the bla CMY gene. A total of 298 Salmonella serovar Heidelberg isolates were recovered, representing 21.6% of all Salmonella serovars from retail meats. One hundred seventy-eight (59.7%) were from ground turkey, 110 (36.9%) were from chicken breast, and 10 (3.4%) were from pork chops; none was found in ground beef. One hundred ninety-eight isolates (66.4%) were resistant to at least one compound, and 49 (16.4%) were resistant to at least five compounds. Six isolates (2.0%), all from ground turkey, were resistant to at least nine antimicrobials. The highest resistance in poultry isolates was to tetracycline (39.9%), followed by streptomycin (37.8%), sulfamethoxazole (27.7%), gentamicin (25.7%), kanamycin (21.5%), ampicillin (19.8%), amoxicillin-clavulanic acid (10.4%), and ceftiofur (9.0%). All isolates were susceptible to ceftriaxone and ciprofloxacin. All ceftiofur-resistant strains carried bla CMY . PFGE using XbaI and BlnI showed that certain clones were widely dispersed in different types of meats and meat brands from different store chains in all five sampling years. These data indicate that Salmonella serovar Heidelberg is a common serovar in retail poultry meats and includes widespread clones of multidrug-resistant strains.
Salmonella isolates were recovered from a monthly sampling of chicken breasts, ground turkey, ground beef, and pork chops purchased from selected grocery stores in six participating FoodNet sites (Connecticut, Georgia, Maryland, Minnesota, Oregon, and Tennessee) in 2002 and an additional two sites in 2003 (California and New York). In 2002 and 2003, a total of 6,046 retail meats were examined, including 1,513 chicken breasts, 1,499 ground turkey samples, 1,522 ground beef samples, and 1,502 pork chops. Retail meat samples tested increased to 3,533 in 2003 as compared to 2,513 in 2002. Overall, six percent of 6,046 retail meat samples (n = 365) were contaminated with Salmonella, the bulk recovered from either ground turkey (52%) or chicken breast (39%). Salmonella isolates were serotyped and susceptibility tested using a panel of 16 antimicrobial agents. S. Heidelberg was the predominant serotype identified (23%), followed by S. Saintpaul (12%), S. Typhimurium (11%), and S. Kentucky (10%). Overall, resistance was most often observed to tetracycline (40%), streptomycin (37%), ampicillin (26%), and sulfamethoxazole (25%). Twelve percent of isolates were resistant to cefoxitin and ceftiofur, though only one isolate was resistant to ceftriaxone. All isolates were susceptible to amikacin and ciprofloxacin; however, 3% of isolates were resistant to nalidixic acid and were almost exclusive to ground turkey samples (n = 11/12). All Salmonella isolates were analyzed for genetic relatedness using pulsed-field gel electrophoresis (PFGE) patterns generated by digestion with Xba1 or Xba1 plus Bln1. PFGE fingerprinting profiles showed that Salmonella, in general, were genetically diverse with a total of 175 Xba1 PFGE profiles generated from the 365 isolates. PFGE profiles showed good correlation with serotypes and in some instances, antimicrobial resistance profiles. Results demonstrated a varied spectrum of antimicrobial resistance and PFGE patterns, including several multidrug resistant clonal groups among Salmonella isolates, and signify the importance of sustained surveillance of foodborne pathogens in retail meats.
The presence and antimicrobial susceptibility of foodborne pathogens and indicator organisms in animal feed are not well understood. In this study, a total of 201 feed ingredient samples (animal byproducts, n=122; plant byproducts, n=79) were collected in 2002 and 2003 from representative rendering plants and the oilseed (or cereal grain) industry across the United States. The occurrence and antimicrobial susceptibility of four bacterial genera (Salmonella, Campylobacter, Escherichia coli, and Enterococcus) were determined. Salmonella isolates were further characterized by serotyping and pulsed-field gel electrophoresis (PFGE). None of the samples yielded Campylobacter or E. coli O157:H7, whereas Salmonella, generic E. coli, and Enterococcus were present in 22.9%, 39.3%, and 86.6% of samples, respectively. A large percentage (47.8%) of Salmonella-positive samples harbored two serovars, and the vast majority (88.4%) of Enterococcus isolates were E. faecium. Animal byproducts had a significantly higher Salmonella contamination rate (34.4%) than plant byproducts (5.1%) (p<0.05). Among 74 Salmonella isolates recovered, 27 serovars and 55 PFGE patterns were identified; all were pan-susceptible to 17 antimicrobials tested. E. coli isolates (n=131) demonstrated similar susceptibility to these antimicrobials except for tetracycline (15.3% resistance), sulfamethoxazole (7.6%), streptomycin (4.6%), ampicillin (3.8%), and nalidixic acid (1.5%). Enterococcus isolates (n=362) were also resistant to five of 17 antimicrobials tested, ranging from 1.1% to penicillin to 14.6% to tetracycline. Resistance rates were generally higher among isolates recovered from animal byproducts. Taken together, our findings suggest that diverse populations of Salmonella, E. coli, and Enterococcus are commonly present in animal feed ingredients, but antimicrobial resistance is not common. Future large-scale studies to monitor these pathogenic and indicator organisms in feed commodities is warranted.
Ampicillin-resistant (Amp r ) Salmonella enterica isolates (n ؍ 344) representing 32 serotypes isolated from retail meats from 2002 to 2006 were tested for susceptibility to 21 other antimicrobial agents and screened for the presence of five beta-lactamase gene families (bla CMY , bla TEM , bla SHV , bla OXA , and bla CTX-M ) and class 1 integrons. Among the Amp r isolates, 66.9% were resistant to five or more antimicrobials and 4.9% were resistant to 10 or more antimicrobials. Coresistance to other -lactams was noted for amoxicillin-clavulanic acid (55.5%), ceftiofur (50%), cefoxitin (50%), and ceftazidime (24.7%), whereas less than 5% of isolates were resistant to piperacillin-tazobactam (4.9%), cefotaxime (3.5%), ceftriaxone (2%), and aztreonam (1.2%). All isolates were susceptible to cefepime, imipenem, and cefquinome. No Salmonella producing extended-spectrum beta-lactamases was found in this study. Approximately 7% of the isolates displayed a typical multidrugresistant (MDR)-AmpC phenotype, with resistance to ampicillin, chloramphenicol, streptomycin, sulfonamide, tetracycline, plus resistance to amoxicillin-clavulanic acid, cefoxitin, and ceftiofur and with decreased susceptibility to ceftriaxone (MIC > 4 g/ml). Pulsed-field gel electrophoresis results showed that several MDR clones were geographically dispersed in different types of meats throughout the five sampling years. Additionally, 50% of the isolates contained bla CMY , 47% carried bla TEM-1 , and 2.6% carried both genes. Only 15% of the isolates harbored class I integrons carrying various combinations of aadA, aadB, and dfrA gene cassettes. The bla CMY , bla TEM , and class 1 integrons were transferable through conjugation and/or transformation. Our findings indicate that a varied spectrum of coresistance traits is present in Amp r Salmonella strains in the meat supply of the United States, with a continued predominance of bla CMY and bla TEM genes in -lactam-resistant isolates.
A 47-year-old woman presented with a 3-day history of right breast pain. The patient denied trauma to the area. The breast pain followed a 2-day episode of what she described as flu-like illness (stomach virus) after she ate crabmeat. She also complained of right arm and shoulder pain with stiffness. Her left breast was normal. On physical examination, her blood pressure was 134/82, her temperature was 98.1°F, and her pulse was 93. There was a palpable, tender, mobile mass measuring approximately 5 by 5 cm on the lower outer quadrant of the right breast. The area surrounding the aerola was tender, erythematous, and warm to the touch. The left breast was normal without masses, nipple discharge, or retraction. There were no other physical findings. The patient underwent an ultrasound of the right breast that revealed cystic fluid that was aspirated. A 20-gauge needle was used to aspirate a small amount of fluid with a milky appearance, which was sent for culture and sensitivity determinations. The culture of the aspirate was positive for Salmonella at the hospital laboratory, and the patient was treated with 500 mg of ciprofloxacin twice daily for 7 days. The hospital laboratory forwarded the Salmonella isolate to the Public Health Diagnostic Microbiology Laboratory at the State of Maryland Department of Health and Mental Hygiene, where the isolate was identified as S. enterica serotype Landwasser (3,10:Z:Z6). The Centers for Disease Control and Prevention have confirmed this finding. Antibiotic susceptibility testing of the isolate showed that the strain was susceptible to a wide variety of agents, including amikacin, ampicillin, aztreonam, ampicillin-sulbactam, ceftriaxone, cephalothin, ciprofloxacin, gentamicin, imipenem, tetracycline, and trimethoprim-sulfamethaxazole. The patient's symptoms resolved after aspiration of the cyst, and she had no further symptoms. Both the infection site (extraintestinal) and the fact that it is the first to be reported in humans make this case especially unique. The patient denied having pets, lizards in particular, and had no travel history. Stool culture was not done on the patient, and the source of this infection remains unknown to us. To our knowledge, this is the first case of S. enterica serotype Landwasser infection in a human host. A literature search did not reveal any other reported cases due to this serotype. The organism was originally isolated in 1979 from a lizard and reported by Le Minor et al. (5). Salmonella species cause a wide spectrum of infections,
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