Effect of regulation and education on reptile-associated salmonellosis

Emerging Infectious Diseases,  March, 2005  by Birgitta de Jong,  Yvonne Andersson,  Karl Ekdahl

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Reptiles have become increasingly common as domestic pets, and with them reptile-associated Salmonella infections in humans. From 1990 to 2000, a total of 339 reptile-associated Salmonella cases were reported in Sweden. In 1996, as part of its efforts to adapt its import regulations to those of the European Union, Sweden no longer required certificates stating that imported animals were free of Salmonella. A subsequent increase was noted in the incidence of reptile-associated cases from 0.15/100,000 in the period 1990-1994 to 0.79/100,000 in 1996 and 1997. After a public education campaign was begun through the news media, the incidence dropped to 0.46/100,000. Children were the most affected age group among patients (incidence 1.3/100,000). Salmonella enterica serotype Enteritidis was the most frequent serotype (24% of isolates), followed by S. Typhimurium (9% of isolates). Import restrictions and public information campaigns are effective public health measures against reptile-associated salmonellosis.

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Salmonellosis is an important worldwide health problem, affecting both humans and animals. In the United States, Salmonella causes an estimated 1.4 million episodes of infection and 400 deaths annually in humans (1). Salmonella usually causes a moderate gastrointestinal disorder, but it may result in more severe disease, such as bacteremia or meningitis, sometimes with fatal outcome (2,3).

For decades, reptiles have been recognized as a source of human salmonellosis. Salmonella species were first isolated from snakes, turtles, and lizards in the 1940s (4,5), and more recent studies have shown that at least 50%-90% of these animals are carriers of Salmonella (6-8). The bacteria are excreted intermittently in the feces but can also be isolated from the cloacae, skin, and throat of water-living reptiles.

Reptiles have become increasingly common as domestic pets. In Canada, pet turtle-associated salmonellosis was recognized as a serious health problem in the 1960s and 1970s, and the country banned imported turtles in 1975 (9).

Sweden has a long tradition of combating and controlling Salmonella in feed, animals, and humans, dating back to a large outbreak of salmonellosis in 1953 that affected >9,000 persons and caused 90 deaths (10,11). From 1970 to 1994, these control measures also included import restrictions on reptiles; anyone who wanted to import reptiles or turtles needed a certificate stating that the animals were free of Salmonella, and importing of turtles with shells <10 cm was not allowed.

In 1995, Sweden dropped its requirement for a Salmonella certificate and instead required an import permit issued by the Swedish Board of Agriculture. When Sweden became a member of the European Union (EU) in January 1995, a number of new rules were adopted. As a result of these changes, Sweden no longer required import permits for reptiles and turtles, and it also lifted the import ban on small turtles. The adaptation of import regulations for reptiles took effect on March 1, 1996.

Our study had 2 goals. First, we studied the impact of strict import regulations on the epidemiology of reptile-associated salmonellosis (RAS). Secondly, we assessed whether awareness campaigns can decrease the number of such cases.

Methods

Swedish Surveillance System for Salmonellosis

Salmonellosis is a reportable disease in Sweden. Case-patients, who need to have a Salmonella-positive stool or blood sample confirmed by a laboratory, are reported both by the physician who has seen the patient (clinical notification) and the laboratory that identified the bacterium (laboratory notification). Notification is submitted concurrently to the Swedish Institute for Infectious Disease Control, the county medical officer, and the municipal Environmental Health Board. Clinical notification includes relevant epidemiologic information, including suspected source of infection. If the county medical officer's initial investigation indicates an environmental source of infection (such as food, water, or animals), the Environmental Health Board samples the suspected source.

Reptile-associated Cases

We reviewed all reported domestic cases (patient reported to be infected in Sweden) of salmonellosis from 1990 to 2000 for association with reptiles. A patient was considered to have RAS if reference was made to direct or indirect contact with a reptile or turtle, and the notification did not indicate other sources of infection. All Salmonella strains were sent to the national Salmonella Reference Laboratory at the Swedish Institute for Infectious Disease Control, which performed serotyping according to the Kauffman and White scheme (12). In the case of Salmonella enterica serotype Typhimurium or S. Enteritidis, the laboratory also carried out phage typing according to the Colindale scheme. The Department of Epidemiology at the Swedish Institute for Infectious Disease Control compiled and analyzed all of these sources of information, together with reports on outbreaks from county medical officers.