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Outbreak of Multidrug-Resistant Salmonella Newport --- United States, January--April 2002

During January--April 2002, Salmonella serotype Newport was isolated from 47 persons in five states: New York (34 cases), Michigan (five), Pennsylvania (four), Ohio (two), and Connecticut (two). Antimicrobial-susceptibility testing of three isolates by CDC revealed resistance to amoxicillin/clavulanate, ampicillin, cefoxitin, ceftiofur, cephalothin, chloramphenicol, streptomycin, sulfamethoxazole, and tetracycline. In addition, two of three isolates were resistant to kanamycin; two had decreased susceptibility or resistance to ceftriaxone. To determine the cause of the outbreak, the New York State Department of Health (NYSDOH) and CDC conducted a case-control study. This report summarizes the results of this investigation, which implicated exposure to raw or undercooked ground beef as the vehicle of transmission. The findings also highlight the emergence of multidrug-resistant S. Newport in the United States. These strains exhibit decreased susceptibility or resistance to ceftriaxone, thereby complicating empiric therapy for serious Salmonella infections. Clinicians should be informed of the emergence of these S. Newport strains, and persons should refrain from eating undercooked ground beef and wash their hands after handling raw ground beef.

The outbreak was identified on February 11, when a county health department notified NYSDOH of seven cases of S. Newport infection. Pulsed-field gel electrophoresis (PFGE) testing by the NYSDOH laboratory revealed that six isolates had an indistinguishable pattern, and one isolate had a single band difference. NYSDOH defined a case as isolation of S. Newport with a PFGE pattern that was indistinguishable or one band different from the outbreak pattern. Additional cases were reported from Connecticut, Michigan, Ohio, and Pennsylvania through the National Molecular Subtyping Network for Foodborne Disease Surveillance (PulseNet).

A total of 47 cases from the five states was identified. The median age of infected persons was 45 years (range: 2--81 years); 33 (70%) were females. Symptom onsets occurred during January 1--April 4, with 33 (73%) occurring during February 1--15. Of the 47 patients, 46 were interviewed. The median duration of illness was 9 days (range: 3--60 days). Predominant symptoms included diarrhea (100%), abdominal pain (91%), fever (78%), blood-tinged stools (52%), and vomiting (48%). Six (13%) patients reported other symptomatic household members. A total of 33 (72%) patients received antimicrobial agents, and 17 (37%) were hospitalized. One patient from New York with leukemia developed sepsis and died; S. Newport was identified in both blood and stool cultures from this patient. A total of 44 isolates had an indistinguishable PFGE pattern after analysis with two enzymes (XbaI and AvrII); three isolates differed by one band.

To identify exposures associated with illness, NYSDOH and CDC compared 36 patients (28 from New York, four from Michigan, and four from Pennsylvania) with 85 controls, who were interviewed through random-digit--dialing in case-patients' home area codes and frequency-matched by age group. A multivariate logistic regression analysis indicated that 22 (67%) of 35 case-patients had eaten ground beef during the 3 days before illness onset compared with 31 (53%) of 58 controls (odds ratio [OR]=2.3; 95% confidence interval [CI]=0.9--5.7). Case-patients and controls were asked about eating raw or undercooked ground beef during the 3 days before illness onset. Of the 26 case-patients who answered definitively, 12 (46%) had eaten raw or undercooked ground beef compared with one (1%) of 80 controls (OR=50.9; 95% CI=5.3--489.0). A total of 11 patients recalled the type of ground beef eaten; seven (64%) had eaten lean or extra-lean ground beef. The U.S. Department of Agriculture (USDA) Food Safety and Inspection Service (FSIS) was notified after this investigation implicated ground beef as a potential vehicle for exposure.

One New York patient had a leftover, frozen, uncooked meatloaf prepared with the same package of ground beef that was used to prepare meals eaten during the 3 days before onset of symptoms. A culture of the meatloaf yielded S. Newport with a PFGE pattern indistinguishable from the outbreak pattern. Traceback by FSIS of ground beef eaten by 12 New York patients identified a meat packing plant that could have supplied the meat eaten by all those identified in the outbreak. Review of distribution records, grinding logs, and purchasing information did not identify any specific lot of ground beef, and no intact ground beef sample processed by the plant during the outbreak period was available for testing by FSIS. On April 19, USDA issued a Public Health Alert reminding consumers of food safety guidelines. FSIS is examining practices that might contribute to contamination of meat by this pathogen.

Reported by: S Zansky, PhD, Emerging Infections Program; B Wallace, MD, Bur of Communicable Disease Control; D Schoonmaker-Bopp, MS, Wadsworth Center; P Smith, MD, State Epidemiologist, New York State Dept of Health. F Ramsey, MS, Food Safety and Inspection Svc, US Dept of Agriculture. J Painter, DVM, Div of Bacterial and Mycotic Diseases, National Center for Infectious Diseases; A Gupta, MD, P Kalluri, MD, S Noviello, MD, EIS officers, CDC.

Editorial Note:

An estimated 1.4 million cases of Salmonellosis occur annually in the United States (1). S. Newport is the third most common Salmonella serotype in the United States. During 1997--2001, the number of laboratory-confirmed S. Newport infections reported to CDC increased from 1,584 (5%) of 34,608 reported Salmonella infections to 3,152 (10%) of 31,607 (CDC, unpublished data, 2002). The increasing number of S. Newport infections in the United States appears to be associated with the emergence and rapid dissemination of multidrug-resistant strains of S. Newport.

Since 1996, the National Antimicrobial Resistance Monitoring System (NARMS) for Enteric Bacteria has identified an increasing number of S. Newport isolates that are resistant to at least nine of 17 antimicrobial agents tested: amoxicillin/clavulanate, ampicillin, cefoxitin, ceftiofur, cephalothin, chloramphenicol, streptomycin, sulfamethoxazole, and tetracycline. In addition, these isolates exhibit decreased susceptibility (minimal inhibitory concentrations [MIC] >16mg/ml) or resistance (MIC >64mg/ml) to ceftriaxone, an antimicrobial agent commonly used to treat serious infections in children. Isolates with this resistance pattern have plasmids that carry a blaCMY gene. These genes produce AmpC-type enzymes, which confer resistance to penicillin-inhibitor combinations (e.g., amoxicillin/clavulanate), cephamycins (e.g., cefoxitin), and expanded-spectrum cephalosporins (e.g., ceftiofur and ceftriaxone). To distinguish this type of resistance from other multidrug-resistant strains, these strains are referred to as Newport MDR-AmpC. In 1998, one (1%) of 78 S. Newport isolates tested in NARMS was Newport MDR-AmpC compared with 33 (26%) of 128 in 2001. Although the full clinical significance of Newport MDR-AmpC is unknown, treatment of these infections with ceftriaxone might be ineffective. In addition, antimicrobial-resistant Salmonella infections have been associated with an increased hospitalization rate, morbidity, and mortality (2,3).

During 2001--2002, several state health departments, including California, Connecticut, and Massachusetts, documented association of exposure to dairy farms, ill cattle, and cheese made from unpasteurized milk with increased human Newport MDR-AmpC infections (4--6). In the outbreak described in this report, most patients for whom information is available ate lean or extra-lean ground beef; dairy cattle are an important source of lean or extra-lean ground beef (7). These data suggest that cattle, particularly dairy cattle, might be a source for human Newport MDR-AmpC infection.

This report is the first to associate eating of ground beef, specifically raw or undercooked ground beef, with Newport MDR-AmpC infection. Recent U.S. surveys indicate that 11%--28% of persons report eating raw or undercooked ground beef, and approximately one third of persons do not use safe food-handling practices to prevent cross-contamination in the kitchen (8).

The USDA Pathogen Reduction/Hazard Analysis and Critical Control Points (PR/HACCP) inspection system in meat and poultry plants has reduced Salmonella prevalence in raw ground beef from 7.5% in 1998 to 2.8% in 2001(9). The emergence of Newport MDR-AmpC suggests that further measures might be necessary. Potential strategies include 1) evaluating practices on the farm to determine factors that might contribute to multidrug-resistant S. Newport and developing interventions to eliminate these factors; 2) implementing the Public Health Action Plan to Combat Antimicrobial Resistance (10); 3) encouraging industry to implement processes such as steam pasteurization or irradiation of ground beef; and 4) increasing efforts to educate consumers on the importance of safe handling and cooking practices.

State health departments and veterinarians should investigate clusters of S. Newport and perform antimicrobial-susceptibility testing to determine if isolates are Newport MDR-AmpC. Epidemiologic investigations and PFGE comparison of outbreak isolates will help to identify food vehicles associated with Newport MDR-AmpC and to identify control points for reducing these infections. Because treatment with ceftriaxone might be ineffective, clinicians should be informed of the emergence of Newport MDR-AmpC strains. Persons should not eat undercooked ground beef and should wash their hands after handling raw ground beef.

Acknowledgments

This report is based on data contributed by G Balzano, S Kondracki, Bur of Communicable Disease Control; BJ Anderson, C Hidalgo, G Smith, Emerging Infections Program; R Woron, MPH, B Gerzonic, MBA, Bur of Community Sanitation and Food Protection; T Root, Wadsworth Center, New York State Dept of Health. S Hrabowy, MPH, Michigan Dept of Health. M Deasy, A Weltman, MD, Pennsylvania Dept of Health. S Nowicki, MPH, Ohio Dept of Health. Q Phan, MPH, J Hadler, MD, Connecticut Dept of Public Health. Office of Public Health and Science, Office of Field Operations, Congressional and Public Affairs Office, Food Safety and Inspection Svc, US Dept of Agriculture. S Van Duyne, Div of Bacterial and Mycotic Diseases, National Center for Infectious Diseases; A Shane, MD, EIS Officer, CDC.

References

  1. Mead PS, Slutsker L, Dietz V, et al. Food-related illness and death in the United States. Emerg Infect Dis 1999;5:607--25.
  2. Helms M, Vastrup P, Gerner-Smidt P, Molbak K. Excess mortality associated with antimicrobial drug-resistant Salmonella Typhimurium. Emerg Infect Dis 2002;8:490--5.
  3. Varma JK, Molbak K, Rossiter S, Hawkins MA, Jones TF, Mauvais SH. Antimicrobial resistance in Salmonella is associated with increased hospitalizations. Atlanta, Georgia: Presented at NARMS 1996--2000, International Conference on Emerging Infectious Diseases, 2002.
  4. Gupta A, Crowe C, Fontana J, et al. Multistate investigation of multidrug-resistant Salmonella serotype Newport infections in the Northeastern U.S.: human infections associated with dairy cows. San Francisco, California: Presented at Infectious Disease Society of America, 2001.
  5. McCarthy T, Phan Q, Mshar P, Mshar R, Howard R, Hadler JL. Outbreak of multidrug-resistant Salmonella Newport associated with consumption of Italian-style soft cheese, Connecticut. Atlanta, Georgia: Presented at International Conference on Emerging Infectious Diseases, 2002.
  6. Rankin SC, Aceto H, Munson R, et al. Transmission of the blaCMY-2 gene from Salmonella enterica serotype Newport in the dairy farm environment. Atlanta, Georgia: Presented at 3rd International Conference on Emerging Infectious Diseases, 2002.
  7. Spika JS, Waterman SH, Hoo GW, et al. Chloramphenicol-resistant Salmonella Newport traced through hamburger to dairy farms: a major persisting source of human salmonellosis in California. N Engl J Med 1987;316:565--70.
  8. Altekruse SF, Street DA, Fein SB, Levy AS. Consumer knowledge of foodborne microbial hazards and food-handling practices. J Food Prot 1996;59:287--94.
  9. U.S. Department of Agriculture. Progress Report on Salmonella Testing of Raw Meat and Poultry Products, 1998--2001. Available at http://www.fsis.usda.gov/OPHS/haccp/salm4year.htm.
  10. Interagency Task Force on Antimicrobial Resistance. A Public Health Action Plan to Combat Antimicrobial Resistance. Available at http://www.cdc.gov/drugresistance/actionplan/index.htm.

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