Introduction

CDC collaborated with public health, veterinary, and agriculture officials in many states and the U.S. Department of Agriculture National Veterinary Services LaboratoriesExternal (NVSL) to investigate an outbreak of Salmonella Cotham infections linked to contact with pet bearded dragons purchased from multiple stores in different states. Bearded dragons are popular pet lizards, native to Australia, that come in a variety of colors.

Public health investigators used the PulseNet system to identify cases of illness that were part of this outbreak. PulseNet, the national subtyping network of public health and food regulatory agency laboratories coordinated by CDC, receives DNA “fingerprints” of Salmonella bacteria obtained through diagnostic testing using pulsed-field gel electrophoresis, or PFGE.

On January 22, 2014, CDC was notified by the Wisconsin Department of Health Services of a cluster of Salmonella Cotham infections with a high proportion of ill persons reporting exposure to pet reptiles. It was noted that since 2012, there were a total of 12 ill persons infected with Salmonella Cotham in Wisconsin, and 10 (83%) of 12 persons reported contact with pet bearded dragons. Wisconsin receives funding under the CDC FoodCORE (Foodborne Diseases Centers for Outbreak Response Enhancement) program. These centers work together to develop new and better methods to detect, investigate, respond to, and control multistate outbreaks of foodborne diseases.

Salmonella Cotham is a rare serotype. Through a search of historical Salmonella databases, CDC determined that Salmonella Cotham represented only 0.01% of all human isolates in the United States since 1963. Before this outbreak, typically less than 25 Salmonella Cotham infections were reported to PulseNet annually. Given the rarity of the Cotham serotype and the information gathered by Wisconsin, CDC conducted a search of PulseNet for all Salmonella Cotham infections reported since 2012. A second rarely reported serotype, Salmonella Kisarawe, was added to this outbreak investigation after culture of a sample from a bearded dragon collected from an ill person’s home yielded both Salmonella Kisarawe and Salmonella Cotham. A search of the PulseNet database identified six ill persons infected with Salmonella Kisarawe as well as five isolates collected from bearded dragons.

A total of 166 persons infected with the outbreak strains of Salmonella Cotham (160 persons) or Salmonella Kisarawe (6 persons) were reported from 36 states since February 21, 2012. The number of ill persons identified in each state was as follows: Alaska (1), Arizona (5), California (27), Colorado (3), Florida (3), Georgia (3), Idaho (3), Illinois (8), Indiana (4), Kansas (6), Kentucky (4), Maryland (7), Massachusetts (2), Michigan (7), Minnesota (3), Missouri (8), Nebraska (1), New Hampshire (1), New Jersey (3), Nevada (3), New York (12), North Carolina (4), North Dakota (1), Ohio (1), Oklahoma (1), Oregon (2), Pennsylvania (6), South Carolina (1), South Dakota (1), Tennessee (5), Texas (7), Utah (3), Virginia (3), Washington (4), West Virginia (1), and Wisconsin (12).

Among 115 persons for whom information was available, dates that illnesses began ranged from February 20, 2012, to June 30, 2014. Ill persons ranged in age from younger than 1 year to 79 years, with a median age of 3 years. Fifty-nine percent of ill persons were children 5 years of age or younger. Fifty-five percent of ill persons were female. Among 118 ill persons with available information, 44 (37%) were hospitalized. No deaths were reported.

Investigation of the Outbreak

Epidemiologic, laboratory, and traceback investigations conducted by officials in local, state, and federal public health agencies indicated that contact with pet bearded dragons was the likely source of this outbreak of Salmonella Cotham and Salmonella Kisarawe infections. This investigation is over; however, the illnesses linked to contact with pet bearded dragons are expected to continue at a low level since pet owners might be unaware of the risk of Salmonella infection from bearded dragons. If properly cared for, bearded dragons have an average life expectancy of 3 to 10 years. Bearded dragons can continue to shed Salmonella, including these outbreak strains, and potentially make people sick throughout their life.

Epidemiologic Investigation

In interviews, ill persons answered questions about contact with animals and foods consumed during the week before becoming ill. Eighty-six (83%) of 104 persons interviewed reported contact with reptiles or their environments before becoming ill. When asked about the type of reptile, 87 (78%) of 112 persons reported contact with lizards; of 74 persons specifically mentioning the type of lizard, 71 (96%) reported contact with bearded dragons. The percentage of ill persons in this outbreak reporting contact with a reptile was significantly higher than the percentage of U.S. households that reported owning a pet reptile in a survey conducted in 2013-2014 by the American Pet Products Association (4.6%).

Laboratory Investigation

Several State Public Health Laboratories isolated the outbreak strains of Salmonella Cotham and Salmonella Kisarawe from samples from pet bearded dragons or their habitats collected from ill persons’ homes.

The National Antimicrobial Resistance Monitoring SystemExternal (NARMS) is a U.S. public health surveillance system that tracks antibiotic resistance in foodborne and other enteric bacteria found in people, raw meat and poultry, and food-producing animals. NARMS is an interagency partnership among CDC, the U.S. Food and Drug Administration (FDA), the U.S. Department of Agriculture (USDA), and state and local health departments.

The NARMS human surveillance program at CDC monitors antibiotic resistance in Salmonella and several other bacteria isolated from clinical specimens and submitted to NARMS by public health laboratories. CDC’s NARMS laboratory tested Salmonella Cotham isolates collected from ten ill persons infected with the outbreak strain. One (10%) of the ten isolates tested was multidrug resistant (defined as resistance to at least one antibiotic in three or more antibiotic classes), and the other nine (90%) isolates tested were pansusceptible (susceptible to all antibiotics tested). The multidrug-resistant isolate showed resistance to the following antibiotics: ceftriaxone, amoxicillin/clavulanic acid, ampicillin, cefoxitin, ceftiofur, chloramphenicol, gentamicin, streptomycin, sulfisoxazole and tetracycline and an intermediate level of resistance to ciprofloxacin. Ceftriaxone is commonly used to treat serious Salmonella infections in both children and adults. Ciprofloxacin is also commonly used to treat serious Salmonella infections in adults but is not routinely used in children. CDC’s NARMS laboratory also tested Salmonella Cotham isolates collected from two infected bearded dragons. Both of these isolates were pansusceptible.

Traceback Investigation

The pet industry worked closely with CDC to determine the source of the bearded dragons linked to this outbreak in order to prevent additional illnesses. Through this collaboration, multiple potential bearded dragon breeders were identified that supply lizards to stores in the United States where ill persons reported purchasing their animals.

Environmental and reptile samples were collected during investigations at multiple domestic and international bearded dragon breeding operations and at a large national pet retail chain. A total of 454 samples were obtained, of which 320 (71%) yielded Salmonella. Of 291 Salmonella isolates serotyped, a total of 46 (16%) yielded Salmonella Cotham and 23 (8%) yielded Salmonella Kisarawe. Of these 69 Salmonella Cotham and Kisarawe samples, 4 (6%) yielded both serotypes.