Abstract
This report describes fomite transmission of Salmonella enteritidis to visitors of the Denver Zoological Gardens during a temporary exhibition of Komodo dragons (Varanus komodoensis). The zoo cooperated with state health department officials and the Centers for Disease Control and Prevention (CDC) in conducting an epidemiological investigation of the incident. Thirty-three confirmed cases of S. enteritidis and 17 suspect cases were reported in Denver and surrounding counties. Visitor behaviors that were found to be significant in disease transmission included touching the exhibit barrier, and failure to wash hands prior to eating or drinking after visiting the exhibit.
Introduction
Between 13 January and 21 January of 1996, the Denver Zoological Gardens hosted a temporary exhibition of its four resident Komodo dragons (Varanus komodoensis). The event known as “Komodo Days” was kicked off with a VIP party on 11 January 1996. The purpose of the event was to help raise funding necessary to build a permanent exhibit for the Komodos. Approximately 15,000 people visited the zoo during the 7-day exhibition.
The exhibition was set up in the Denver Zoological Garden’s Tropical Discovery building. The building contains a large indoor plaza referred to as the Discovery Center. It was in the Discovery Center that the temporary Komodo exhibit was located. A temporary barrier made of painted ply-wood, 2 ft in height, was constructed to separate the animals from the visitors. Bark mulch was placed on the floor as substrate for the animals. The plywood barrier was surrounded by decorative plants and a chain and post barrier, creating a space of approximately 2–3 feet between the public and the animals. Also located in the Discovery Center was an education department station, typically manned by docents to allow visitors contact with biofacts and a variety of reptiles; this station was closed during the exhibition.
Case Report
On 26 January 1996 the Animal Health Department of the Denver Zoo Hospital (DZH) was notified by the Colorado Department of Public Health and Environment (CDPHE) that seven children from the Denver Metro area were infected with Salmonella enteritidis, with a characteristic rough colony morphology. The children had all visited Tropical Discovery during the “Dragon Days” event. Eventually, 33 cases were confirmed by culture; 17 other cases were considered to be suspect.
At the time of the initial report, all animals in the building with the potential for public contact were considered possible sources of the infection. The majority of the exhibits in Tropical Discovery are inaccessible to the public. Some exhibits do have open tops which the public, with some difficulty, can physically access. The Komodo dragon exhibit and the educational animals were considered the most likely sources of S. enteritidis for the following reasons: first, these exhibits afforded visitors the greatest access to animals and second, the timing of the human outbreak coincided with the dates of the Komodo exhibition.
Samples were obtained for culture from the skin and cloaca of animals known to have been in contact with the public: four Komodo dragons and education animals including a corn snake (Elaphe guttata), a blue tongued skink (Tiliqua scincoides), and a common boa (Boa constrictor). A preserved skin from a Malayan water monitor (Varanus salvator) used as a biofact was also cultured. Additional samples for culture were obtained from two rats intended to be fed to the Komodos. S. enteritidis with rough colony morphology was isolated from the skin of one Komodo and the cloaca of another.2 Salmonella arizonae was isolated from the corn snake and another Komodo. Salmonella blukwa was isolated from the blue tongued skink.2 No Salmonella species were isolated from the other culture samples.2
On 27 January 1996, officials from the CDPHE inspected the Tropical Discovery building. Cloacal and some fecal samples were obtained for culture from all of the animals previously tested. S. enteritidis with rough colony morphology was isolated from the cloaca of one of the two Komodo dragons that previously tested positive for this organism.1
On 1 February 1996, investigators from the CDC arrived in Denver at the invitation of the CDPHE. The goal of this visit was to identify modes of transmission of this strain of S. enteritidis and to determine appropriate prevention measures for exhibits of this kind. Initially an environmental investigation was performed.1 Samples for culture were obtained from the wooden barrier, from rectal swabs of five of the six zookeepers involved with care of the Komodos, and from gut contents of a freshly killed feeder rat.1 S. enteritidis was isolated from the wooden barrier.1
The CDC investigation indicated that the following factors likely contributed to infection with this species of Salmonella. The majority of people infected, reported touching the exhibit barrier.1 Failure to wash hands after visiting Tropical Discovery or failure to wash hands before consuming food or drink were also considered to be significantly associated with illness.1 Among those who had touched the barrier surrounding the Komodo exhibit, not washing hands either at the zoo, after visiting Tropical Discovery, or before the next meal was significantly associated with illness.1
Discussion
The outbreak of S. enteritidis in visitors led to the formulation of a policy regarding public contact with reptiles at the Denver Zoological Gardens. This policy is based on the AZA guidelines for animal contact with the general public. The following should be considered in the formulation of a reptile contact policy:
1. All reptiles should be handled as though they are Salmonella spp. positive.
2. Cultures positive for Salmonella may identify carrier animals. However, failure to isolate Salmonella does not provide the animals’ Salmonella status.
3. Treatment with antibiotics has not been shown to be beneficial in the elimination of Salmonella carrier states.
4. Visitors should not be allowed access to reptile holding areas, as they may be contaminated by animal waste products.
5. If visitors are allowed to handle reptiles under controlled situations, the animal should be wiped down with an antiseptic solution prior to handling.
6. Under no circumstances should reptiles be allowed to crawl or perch on visitors.
7. Visitors should not be allowed contact with species that may be considered to have a greater likelihood of carrying Salmonella species, such as iguanas, Varanid lizards, and aquatic turtles.
8. All persons handling reptiles should be required to thoroughly wash their hands when finished.
9. The risks of handling reptiles should be explained to parents or guardians and signed waivers from them should be received prior to allowing children to contact or handle reptiles.
10. Eating and drinking should be prohibited in areas in which reptiles are being handled.
11. Individuals considered at high risk (e.g., pregnant women, children less than 5-years-old, and immunocompromised persons) should not handle reptiles.
This incident demonstrates the importance of serotyping isolates of Salmonella, especially in the face of a disease outbreak. Serotyping helped to establish the relationship between the human infections and the Salmonella cultured from the Komodo dragons. It is suggested that all isolates of Salmonella be submitted for serotyping regardless of human involvement. This incident also provides evidence of the intermittent nature of Salmonella shedding by reptiles.
Literature Cited
1. Hoffman RE. Salmonella and reptiles. Colorado Disease Bulletin. 1996;23:1–2.
2. Poston JB. Salmonella spp. Update. In: Proceedings of the Association of Zoo Veterinary Technicians. 1996;16:91–93.