Discussion

This investigation identified an MDR strain of Salmonella Newport with decreased susceptibility to azithromycin and nonsusceptibility to ciprofloxacin, two oral agents recommended for treatment of Salmonella infections. The presence of resistance genes on a plasmid is concerning because of the potential for spread to other bacteria (5). The outbreak strain appears to have emerged recently because Newport with decreased susceptibility to azithromycin was not detected in animal, retail meat, or human isolates in NARMS surveillance before 2016 (4). During 2016–2017, two smaller multistate clusters of MDR Newport infections with decreased susceptibility to azithromycin were investigated among U.S. residents; isolates were within 11 alleles of the current outbreak isolates. No source of the infections was identified, but a high percentage of patients reported recent travel to Mexico (Division of Foodborne, Waterborne, and Environmental Diseases, National Center for Emerging and Zoonotic Infectious Diseases, CDC, unpublished data, 2019). Routine monitoring in 2016 detected an isolate from a sample of beef imported from Mexico that was indistinguishable (0 allele difference) from the outbreak strain isolated from cheese in 2018.

In this MDR outbreak, consumption of cheese and consumption of beef were both associated with illness, indicating that dairy cattle were a likely source of these infections. The detection of the outbreak strain in cheese purchased in Mexico and the high percentage of travelers to Mexico who reported eating Mexican-style soft cheese suggest that soft cheese from Mexico was a source of infection. Mexican-style soft cheese has been previously identified as a source of other Salmonella outbreaks (6). The reported consumption of queso fresco, travel to various regions in Mexico, and detection of indistinguishable Newport strains in beef and cheese suggest that contamination of soft cheese resulted from carriage by cattle rather than poor hygiene during cheese production. Dairy cattle often are used as a source of ground beef and have been implicated in previous MDR Newport outbreaks (5).

Among patients who did not travel to Mexico, beef was identified as a source of infection by the close genetic relatedness between isolates from patients and beef samples, and from the higher percentage of patients who ate beef compared with the percentage of healthy persons who ate beef. It is also possible that beef was a source of infection among some travelers to Mexico; nearly 90% of them also reported eating beef, and in 2016 the outbreak strain was detected in beef imported from Mexico.

The genetic similarity between isolates from beef in Mexico, beef in the United States, and a steer in the United States strongly suggests that the outbreak strain is present in cattle in both countries. Because use of antibiotics in livestock can cause selection of resistant strains (7), the reported 41% rise in macrolide use in U.S. cattle from 2016 to 2017 (8) might have accelerated carriage of the outbreak strain among U.S. cattle. Avoiding the unnecessary use of antibiotics in cattle, especially those that are important for the treatment of human infections, could help prevent the spread of MDR Newport with decreased susceptibility to azithromycin. Further investigation is warranted to determine the prevalence of Newport with decreased susceptibility to azithromycin in U.S. and Mexican cattle, and to identify measures to prevent transmission among cattle.

Whole genome sequencing was valuable in linking human infections to food sources, distinguishing the MDR outbreak strain from an antibiotic-susceptible strain causing a simultaneous outbreak, and predicting antibiotic resistance. In this outbreak, one in three patients received an antibiotic that was likely to have been ineffective. Clinicians should limit use of antibiotics for patients with an acute diarrheal illness to those with clinical indications (9), and antibiotic selection should be based on susceptibility results whenever possible. For empiric treatment of patients with suspected Newport with decreased susceptibility to azithromycin, ceftriaxone or alternative agents should be considered. To prevent infection, consumers should avoid eating soft cheese that could be made with unpasteurized milk, and when preparing beef they should use a thermometer to ensure appropriate cooking temperatures are reached: 145°F (62.8°C) for steaks and roasts followed by a 3-minute rest time, and 160°F (71.1°C) for ground beef or hamburgers (10).