Salmonellosis

During 1996-1998, CDC received reports from approximately 16 state health departments of Salmonella infections in persons who had direct or indirect contact with reptiles (i.e., lizards, snakes, or turtles). Salmonella infection can result in invasive illness including sepsis and meningitis, particularly in infants. Despite educational efforts, some reptile owners remain unaware that reptiles place them and their children at risk for salmonellosis. This report summarizes clinical and epidemiologic information in four cases and provides information about state regulations to prevent transmission of Salmonella spp. from reptiles to humans.

Case Reports

Arizona. During October 1996, a 3-week-old boy was admitted to a hospital emergency department with fever (103.6 F [40 C]), vomiting, and bloody diarrhea of 15 days' duration. Stool and blood cultures yielded Salmonella serotype IV 44:z4,z23-, an extremely rare serotype. The infant was hospitalized for 10 days and treated with intravenous fluids and amoxicillin. To determine the cause of the infant's illness, a stool specimen was obtained from the family's pet iguana, which also yielded Salmonella IV 44:z4,z23-. In an attempt to prevent reinfection, local health officials informed the parents of the importance of the infant avoiding direct and indirect contact with the reptile, and the iguana was moved to a relative's home. One month later, the infant spent 2 days in the relative's home where the iguana was housed; 48 hours after this visit, the infant was again treated at an emergency department for fever and diarrhea. A stool culture again yielded Salmonella IV 44:z4,z23-.

Kansas. During April 1997, a 6-year-old boy had bloody diarrhea of 10 days' duration, abdominal cramps, vomiting, and fever (104.9 F [41 C]). Stool culture yielded Salmonella serotype Typhimurium. The child was treated with ceftriaxone and amoxicillin/clavulanate. Nine days after the boy started therapy, his 3-year-old brother also developed diarrhea, and a stool sample yielded S. Typhimurium. No other family members became ill. The two boys shared a room with two corn snakes that they handled regularly. Stool cultures from the corn snakes yielded S. Typhimurium. The parents reported to health department staff that they were unaware that snakes are a source of salmonellosis.

Massachusetts. During May 1997, an 8-year-old boy with a congenital immune deficiency developed severe vomiting, abdominal cramps, bloody diarrhea, and headaches. Stool samples yielded Salmonella serotype St. Paul. The boy was ill for 14 days and received extensive supportive care at home. Three days before the boy became ill, the family had purchased two iguanas from a local pet store. The family was not informed by pet store personnel that reptiles are a source of salmonellosis; the child handled the reptiles, including putting them on his head and face. Before diagnostic testing could be performed, the reptiles were returned to the pet store. The parents informed the pet store owner of the child's illness, and the pet store owner reportedly was unaware that reptiles carry Salmonella spp.

Wisconsin. In December 1998, a previously healthy 5-month-old boy suddenly died at home. No significant macroscopic or histologic findings were revealed during autopsy; however, culture of a heart blood sample yielded Salmonella serotype Marina. The cause of death was attributed to S. Marina septicemia. The family had a pet iguana that had not come into direct contact with the infant. Culture of a stool sample taken from the iguana yielded S. Marina. Based on an interview, the parents were unaware that the infant was at risk for salmonellosis from indirect or direct contact with the iguana.

State Regulations for Preventing Reptile-Associated Salmonellosis

During March 1999, CDC contacted all 50 state health departments to determine whether state regulations existed for sale of reptiles and distribution of information about salmonellosis. Of the 48 states that responded, three (California, Connecticut, and Michigan) had regulations requiring pet stores to provide information about salmonellosis to persons purchasing a turtle; two states (Kansas and Maryland) require salmonellosis information to be provided to persons purchasing any reptile. Three states (Arizona, Minnesota, and Wyoming) prohibit reptiles in day care centers and long-term--care facilities.

Reported by: C Levy, MS, M Finnerty, Arizona Dept of Health Svcs. G Hansen, DVM, Kansas Dept of Health and Environment. J Cory, MPH, M McGuill, DVM, B Matyas, MD, A DeMaria, Jr, MD, State Epidemiologist, Massachusetts Dept of Public Health. G Schmunk, MD, J Grantham, MD, Brown County Medical Examiner's Office, Green Bay, Wisconsin; J Archer, MS, J Kazmierczak, DVM, J Davis, MD, State Epidemiologist for Communicable Diseases, Wisconsin Dept of Health and Family Svcs. Foodborne and Diarrheal Diseases Br, Div of Bacterial and Mycotic Diseases, National Center for Infectious Diseases, CDC.

Editorial Note: In the United States, pet turtles were an important source of salmonellosis until commercial distribution of pet turtles [less than]4 inches long was banned in 1975 [1]. This ban led to a 77% reduction in the frequency of turtle-associated Salmonella serotypes isolated from humans during 1970-1976 [1]. The popularity of other reptiles as pets is growing and has raised concerns about their impact on public health. This and other reports [2] demonstrate that reptile-related salmonellosis continues to pose a substantial threat to human health. Approximately 93,000 (7%) cases per year of Salmonella spp. infections are attributable to pet reptile or amphibian contact [3]. An estimated 3% of households in the United States have a reptile (CDC, unpublished data, 1999). Many reptiles are colonized with Salmonella spp. and intermittently shed the organism in their feces [4]. Persons become infected by ingesting Salmonella after handling a reptile or objects contaminated by a reptile and then failing to wash their hands properly. Either direct or indirect contact with infected reptiles and their environment can cause human illness [5,6].

Rare Salmonella serotypes, such as Java, Marina, Stanley, Poona, and Chameleon associated with reptiles, increasingly have been isolated from humans [7] (Figure 1). For example, S. Marina isolates from humans increased from two in 1989 to 47 in 1998, and S. Poona increased from 199 in 1989 to 341 in 1998 [8]. Isolation of rare serotypes of Salmonella spp. can alert public health staff about trends in the transmission of infection from reptiles to humans.

Most persons who contract reptile-associated salmonellosis are infants and young children. In 1994, 413 (81%) of 513 S. Marina cases occurred in children aged [less than]1 year, whereas 4301 (14%) of 30,723 reported salmonellosis cases occurred in children aged [less than]1 year [6]. During 1989-1998, 516 (24%) of 2150 Salmonella isolates with reptile-associated serotypes were from children aged [less than]4 years, whereas 50,755 (19%) of 267,131 other serotypes were from this age group (CDC, unpublished data, 1999). Because infants and immunocompromised persons are more susceptible to illness, many reptile-associated Salmonella infections involve serious complications, including septicemia and meningitis [9].

The risks for transmission of Salmonella spp. from reptiles to humans can be reduced by thoroughly washing hands with soap and water after handling reptiles or objects that have been in contact with reptiles and by preventing reptile contact with food-preparation areas. Children aged [less than]5 years and immunocompromised persons should avoid direct and indirect contact with reptiles. Reptiles also should not be kept in homes of persons with children aged [less than]1 year and in child care facilities (see box). All pet store personnel and reptile owners should be aware that reptiles can carry and transmit Salmonella spp. Pet stores are in a unique position to educate consumers because reptile owners obtain most of their information about their pet from pet store personnel. CDC and the Pet Industry Joint Advisory Council (PIJAC) have developed educational posters and brochures for use by veterinarians and pet stores on safe pet reptile handling. [*]

The effectiveness of educating the public about reptile-associated salmonellosis needs to be evaluated. To enhance efforts to educate the public in a systematic, consistent, and timely manner, the National Association of State Public Health Veterinarians and the Council of State and Territorial Epidemiologists jointly recommend "that the appropriate state and local agencies enact legislation prohibiting the sale or gift of reptiles unless there is written point-of-sale education provided to consumers on the risks for and prevention of reptile-associated salmonellosis" [10]. CDC will provide assistance to states interested in developing point-of-sale educational material; however, if these educational efforts should prove unsuccessful, states may wish to adopt restrictions for the sale of reptiles similar to those for turtles.

(*.) Posters are available on request from PIJAC, telephone (800) 553-7387.

References

(1.) Cohen ML, Potter M, Pollard R, et al. Turtle-associated salmonellosis in the United States, effect of public health action, 1970 to 1976. JAMA 1980;243:1247-9.

(2.) CDC. Reptile-associated salmonellosis--selected states, 1994-1995. MMWR 1995;44:347-50.

(3.) Mermin J, Hutwagner L, Vugia D, et al. Salmonella infections from reptiles in FoodNet sites: the resurgence of a preventable illness. Presented at the annual meeting of the Infectious Diseases Society of America. Denver, Colorado, 1998.

(4.) Burnham BR, Atchley DH, DeFusco RP, et al. Prevalence of fecal shedding of Salmonella organisms among captive green iguanas and potential public health implications. J Am Vet Med Assoc 1998;213:48-50.

(5.) Freidman C, Torigian C, Shillam P, et al. An outbreak of salmonellosis among children attending a reptile exhibit at a zoo. J Pediatr 1998;132:802-7.

(6.) Mermin J, Hoar B, Angulo FJ. Iguanas and Salmonella Marina infection in children: a reflection of the increasing incidence of reptile-associated salmonellosis in the United States. Pediatrics 1997;99:399-402.

(7.) Ackman DM, Drabkin P, Birkhead G, Cieslak P. Reptile-associated salmonellosis in New York State. Pediatr Infect Dis J 1995;14:955-9.

(8.) CDC. Salmonella surveillance annual tabulation summary 1998. Atlanta, Georgia: US Department of Health and Human Services, CDC, 1998.

(9.) Angulo FJ, Swerdlow DL. Bacterial enteric infections in persons infected with human immunodeficiency virus. Clin Infect Dis 1995;21(suppl 1):S84-S93.

(10.) Council of State and Territorial Epidemiologists. Reptile-associated salmonellosis and prevention education. Atlanta, Georgia: Council of State and Territorial Epidemiologists, 1999; position statement no. ID-13.

Recommendations for Preventing Transmission of Salmonella from Reptiles to Humans

* Pet store owners, veterinarians, and pediatricians should provide information to owners and potential purchasers of reptiles about the risk for acquiring salmonellosis from reptiles.

* Persons should always wash their hands thoroughly with soap and water after handling reptiles or reptile cages.

* Persons at increased risk for infection or serious complications of salmonellosis (e.g., children aged [less than]5 years and immunocompromised persons) should avoid contact with reptiles.

* Pet reptiles should be kept out of households where children aged [less than]1 year and immunocompromised persons live. Families expecting a new child should remove the pet reptile from the home before the infant arrives.

* Pet reptiles should not be kept in child care centers.

* Pet reptiles should not be allowed to roam freely throughout the home or living area.

* Pet reptiles should be kept out of kitchens and other food-preparation areas to prevent contamination. Kitchen sinks should not be used to bathe reptiles or to wash their dishes, cages, or aquariums. If bathtubs are used for these purposes, they should be cleaned thoroughly and disinfected with bleach.

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