Nationwide outbreak of multidrug-resistant Salmonella Heidelberg infections associated with ground Turkey: United States, 2011

Epidemiology and Infection

Volumn 143, Issue 15, 2015, Pages 3227-3234

  Routh, J A ^a   Pringle, J ^a   Mohr, M ^b   Bidol, S ^c   Arends, K ^c   Adams Cameron, M ^d   Hancock, W T ^a   Kissler, B ^e   Rickert, R ^a   Folster, J ^a   Tolar, B ^a   Bosch, S ^a   Barton Behravesh, C ^a   Williams, I T ^a   Gieraltowski, L ^a  

^a CENTERS FOR DISEASE CONTROL AND PREVENTION   (United States)

^b OHIO DEPARTMENT OF HEALTH   (United States)

^c MICHIGAN DEPARTMENT OF COMMUNITY HEALTH   (United States)

^d NEW MEXICO DEPARTMENT OF HEALTH   (United States)

^e U S DEPARTMENT OF AGRICULTURE   (United States)

Author keywords

food safety; Food borne infections; outbreaks; Salmonella; salmonellosis

Indexed keywords

AMPICILLIN; GENTAMICIN; STREPTOMYCIN; TETRACYCLINE;

AGED; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL STRAIN; BACTERIUM CULTURE; BACTERIUM ISOLATE; CASE FINDING; CONTROLLED STUDY; DISEASE ASSOCIATION; EPIDEMIC; FEMALE; FOOD ANALYSIS; FOOD CONTAMINATION; FOOD INTAKE; FOOD SAFETY; GROUND TURKEY; HOSPITALIZATION; HUMAN; INFANT; INTERVIEW; MAJOR CLINICAL STUDY; MALE; MEAT; MORTALITY; MULTIDRUG RESISTANCE; PULSED FIELD GEL ELECTROPHORESIS; QUESTIONNAIRE; SALMONELLA ENTERICA SEROVAR HEIDELBERG; TYPHOID FEVER; UNITED STATES; ADOLESCENT; ADULT; ANIMAL; CHILD; DRUG EFFECTS; FOOD CONTROL; ISOLATION AND PURIFICATION; MEAT INDUSTRY; MICROBIOLOGY; MIDDLE AGED; PHYSIOLOGY; PRESCHOOL CHILD; SALMONELLA; SALMONELLA FOOD POISONING; TURKEY (BIRD); VERY ELDERLY; YOUNG ADULT;

ADOLESCENT; ADULT; AGED; AGED, 80 AND OVER; ANIMALS; CHILD; CHILD, PRESCHOOL; DISEASE OUTBREAKS; DRUG RESISTANCE, MULTIPLE, BACTERIAL; ELECTROPHORESIS, GEL, PULSED-FIELD; FEMALE; FOOD MICROBIOLOGY; HUMANS; INFANT; MALE; MEAT-PACKING INDUSTRY; MIDDLE AGED; SALMONELLA; SALMONELLA FOOD POISONING; TURKEYS; UNITED STATES; YOUNG ADULT;

EID: 84944145298     PISSN: 09502688     EISSN: 14694409     Source Type: Journal    
DOI: 10.1017/S0950268815000497     Document Type: Article

References (30)

1. Scallan E, et al. Foodborne illness acquired in the United States-major pathogens. Emerging Infectious Disease 2011; 1: 7-15.
2. CLSI. Performance standards for antimicrobial susceptibility testing; twenty-fourth informational supplement. CLSI document M100-S24. Wayne, PA: Clinical and Laboratory Standards Institute, 2014.
3. Crump JA, et al. Antimicrobial resistance among invasive nontyphoidal Salmonella enterica isolates in the United States: National Antimicrobial Resistance Monitoring System, 1996-2007. Antimicrobial Agents and Chemotherapy 2011; 55: 1148-1154.
4. Varma JK, et al. Antimicrobial-resistant nontyphoidal Salmonella is associated with excess bloodstream infections and hospitalizations. Journal of Infectious Disease 2005; 191: 554-561.
5. Molbak K. Human health consequences of antimicrobial drug-resistant Salmonella and other foodborne pathogens. Clinical Infectious Disease 2005; 41: 1613-1620.
6. Centers for Disease Control and Prevention (CDC). Number and incidence of laboratory-confirmed Salmonella infections caused by the top 10 Salmonella serotypes. 2012. (http://www.cdc.gov/foodnet/data/trends/tables/2012/table5.html). Accessed 18 September 2013.
7. Jones TF, et al. Salmonellosis outcomes differ substantially by serotype. Journal of Infectious Diseases 2008; 198: 109-114.
8. Zhao S, et al. Antimicrobial resistance and genetic relatedness among Salmonella from retail foods of animal origin: NARMS retail meat surveillance. Foodborne Pathogens and Disease 2006; 3: 106-117.
9. National Antimicrobial Resistance Monitoring System for Enteric Bacteria (NARMS). Annual Retail Meat Report. CDC, 2013 (http://www.fda.gov/AnimalVeterinary/Safety Health/AntimicrobialResistance/NationalAntimicrobial ResistanceMonitoringSystem/ucm334828.htm). Accessed 18 September 2013.
10. Folster JP, et al. Characterization of extended-spectrum cephalosporin-resistant Salmonella enterica serovar Heidelberg isolated from food animals, retail meat, and humans in the United States 2009. Foodborne Pathogens and Diease 2012; 9: 638-645.
11. Lynne AM, et al. Characterization of antimicrobial resistance in Salmonella enterica serotype Heidelberg isolated from food animals. Foodborne Pathogens and Disease 2009; 6: 207-215.
12. Zhao S, et al. Antimicrobial resistance in Salmonella enterica serovar Heidelberg isolates from retail meats, including poultry, from 2002 to 2006. Applied Environmental Microbiology 2008; 74: 6656-6662.
13. Haley M. Changing consumer demand for meat: The US example, 1970-2000. In: Regmi A, ed. Changing Stucture of Global Food Consumption and Trade. Market and Trade Economics Division, Economic Research Service, U.S. Department of Agriculture, Agriculture and Trade Report, WRS-01-1, 2001, pp. 41-49.
14. United States Department of Agriculture/Food Safety and Inspection Service (USDA/FSIS). Quarterly progress report on Salmonella testing of selected raw meat and poultry products: preliminary results, January-March 2011. (http://www.fsis.usda.gov/wps/wcm/connect/ec88dd42-25d3-4183-a29f-c52ccbcb9da5/Q1-2011-Salmonella-Testing.pdf?MOD=AJPERES). Accessed 18 September 2013.
15. CDC. Multistate outbreak of Salmonella Hadar infections associated with turkey burgers, 2011 (http://www.cdc.gov/salmonella/hadar0411/040411/index. html). Accessed 18 September 2013.
16. Khaitsa ML, et al. Occurrence of antimicrobial-resistant salmonella species in raw and ready to eat turkey meat products from retail outlets in the midewestern United States. Foodborne Pathogens and Disease 2007; 4: 517-525.
17. FSIS Food Recalls, 4 October 2013. (http://www.fsis. usda.gov/wps/portal/fsis/topics/food-safety-education/get-answers/food-safety-fact-sheets/production-and-inspection/fsis-food-recalls/fsis-food-recalls). Accessed 22 March 2015.
18. FSIS. HACCP plan reassessment for not-ready-to-eat comminuted poultry products and related agency verification procedures. 2012. (http://www.fsis.usda.gov/OPPDE/rdad/FRPubs/2012-0007.pdf). Accessed 18 September 2013.
19. Murase T, et al. Evaluation of DNA fingerprinting by PFGE as an epidemiological tool for Salmonella infections. Microbiology and Immunology 1995; 39: 67367-6.
20. Tolar B. Pulsenet database. CDC, 2013. Accessed 19 September 2013.
21. Folster JP, et al. Characterization of multidrug-resistant Salmonella enterica serovar heidelberg from a ground turkey-associated outbreak in the United States in 2011. Antimicrobial Agents and Chemotherapy 2012; 56: 3465-3466.
22. CDC. Foodborne Active Surveillance Network (FoodNet) Population Survey Atlas of Exposures. Atlanta, Georgia: U.S. Department of Health and Human Services, Centers for Disease Control and Prevention, 2006-2007. (http://www.cdc.gov/foodnet/surveys/FoodNetExposure Atlas0607-508.pdf). Accessed 18 September 2013.
23. FSIS. FSIS issues public health alert for frozen, fresh ground turkey products: FSIS, 2011. (http://www.fsis. usda.gov/wps/portal/fsis/topics/recalls-and-public-healthalerts/current-recalls-and-alerts/recalls-and-public-healthalerts/! ut/p/a1/jZDBCoJAEIafpQdYdkwRPYpgaukikdle YjPThW2VVTv09Cl1yChy5jTD9-MxgynOMJXsxkv W8VoyMc7UPEICpma7EBLP8SCIdS-14pUGxByAww SwtRFIE7J2XbBifWb-RznwLx-OECxV5EYlpg3rKsTlpc ZZ3itVyA6pImdCtIjJM2KiUF2Ls-dd058Ez1FVMDFkX8 Qe06kVtKEH69bww1gHYnwCX97yBH7f3Vx32X3jAwcxQPrBMoV/? 1dmy¤t=true&urile=wcm%3apath%3a %2Ffsis-archives-content%2Finternet%2Fmain%2Fnews room%2Fnews-releases-statements-and-transcripts %2Fnews-release-archives-by-year%2Farchives%2Fct-index528). Accessed 15 January 2014.
24. USDA/FSIS. Arkansas firm recalls ground turkey products due to possible Salmonella Contamination, 2011 (http://www.fsis.usda.gov/wps/portal/fsis/topics/recalls-and-public-health-alerts/recall-case-archive/recallcase-archive-2011/!ut/p/a1/jZDBCoJAEIafpQdYdlZF9Cg Lppa7SGS2lxjEdMFUTDz09CmdDKVmTjN8Px8zVNG MqgZHXeKg2wbreVb2DRKwmcshkr7nQyhMP3XEno G0J-C6AFw2A2kiD5yDI8w-8xvlwa989IfA6GMel1R1 OFREN-eWZn2RY12THJ8FwT6v9FisLokBjNELVUs NsKknzckKImGCtL6BlT98gO1Du8c5ex0D0KG3ewMyXtGN/?1dmy¤t=true&urile=wcm%3apath% 3a%2Ffsis-archives-content%2Finternet%2Fmain%2Ftopics %2Frecalls-and-public-health-alerts%2Frecall-case-archive% 2Farchives%2Fct-index129a). Accessed 20 January 2014.
25. CDC NARMS. National Antimicrobial Resistance Monitoring System for Enteric Bacteria (NARMS): Human Isolates Final Report, 2011. U.S. Department of Health and Human Services, CDC, 2013. (http://www. Cdc.gov/narms/pdf/2011-annual-report-narms-508c.pdf). Accessed 18 September 2013.
26. Holmberg SD, Solomon SL, Blake PA. Health and economic impacts of antimicrobial resistance. Reviews of Infectious Disease 1987; 9: 1065-1078.
27. Lee LA, et al. Increase in antimicrobial-resistant Salmonella infections in the United States, 1989-1990. Journal of Infectious Disease 1994; 170: 128-134.
28. US DHHS/CDC. Antibiotic resistance threats in the United States, 2013. U.S. Department of Health and Human Services, CDC, 2013 (http://www.cdc.gov/drugresistance/threat-report-2013/pdf/ar-threats-2013-508.pdf). Accessed 13 December 2013.
29. US DHHS/FDA. The judicious use of medically important antimicrobial drugs in food-producing animals: U.S. Department of Health and Human Services, Food and Drug Administration, 13 April 2011 (http://www.fda. gov/downloads/AnimalVeterinary/GuidanceCompliance Enforcement/GuidanceforIndustry/UCM216936.pdf). Accessed 18 September 2013.
30. US DHHS/FDA. New animal drugs and new animal drug combination products administered in or on medicated feed or drinking water of food-producing animals: recommendations for drug sponsors for voluntarily aligning product use conditions with GFI #209 (http://www.fda.gov/downloads/AnimalVeterinary/Guidance ComplianceEnforcement/GuidanceforIndustry/UCM299624. Pdf). Accessed 13 December 2013.