Salmonellosis

During 1998-2002, CDC received reports from state health departments regarding Salmonella infections in persons who had contact with reptiles (e.g., lizards, snakes, and turtles). Salmonella infections usually cause gastroenteritis but can result in invasive illness (e.g., septicemia and meningitis), especially in infants and immunocompromised persons. For decades, reptiles have been known as a source for salmonellosis (1); however, numerous reptile owners remain unaware that reptile contact places them and other household members, including children, at greater risk for salmonellosis (2). Increasing evidence suggests that amphibians (e.g., frogs, toads, newts, and salamanders) also can pose risks for salmonellosis in humans (3,4). This report describes cases of reptile-associated salmonellosis in six states *, offers recommendations on preventing transmission of Salmonella from reptiles and amphibians to humans (Box), and provides an update on state regulations mandating education at per stores about salmonellosis.

Case Reports

California. During December 2001, an infant aged 3 months was taken to an emergency department (ED) after 1 day of bloody diarrhea and fever. The infant was sent home with no therapy and recovered in 2 days; a stool specimen yielded Salmonella serotype Nima. Although no reptiles lived in the home, the infant's father was a high school biology teacher who handled reptiles in the classroom, including a large snake (i.e., a boa) that he often draped over his shoulders. A stool culture from the snake grew S. Nima. When interviewed, the father indicated that he knew reptiles carry Salmonella and was careful to wash his hands after handling them or their containers. However, he did not change clothing when he came home from work before holding his child.

Connecticut. During June 2002, a child aged 21 months was admitted to a hospital with fever, abdominal cramps, and bloody diarrhea. The child received no antibiotic therapy and was discharged the next day. Blood and stool cultures yielded Salmonella serotype Poona. A sibling aged 6 years also had fever and bloody diarrhea and a stool culture that yielded S. Poona. The family had purchased an iguana approximately 1 month earlier. The children had cleaned the iguana's cage and handled the iguana 2 days before their illness onsets. A stool culture from the iguana grew S. Poona; isolates from the iguana and the two siblings were indistinguishable by pulsed-field gel electrophoresis (PFGE).

Florida. During January 2000, an infant aged 1 month visited a clinic with fever and diarrhea; the infant was not hospitalized. A stool specimen yielded Salmonella serotype Tennessee. One week before illness onset, the infant's family moved into a household that contained a bearded dragon (i.e., Pogona vitticeps). The pet reptile's cage had been washed in the kitchen near the infant's bottle nipples. A stool culture from the bearded dragon yielded S. Tennessee. Isolates from the infant and the bearded dragon were indistinguishable by PFGE. An adult in the house reported being aware that turtles and iguanas are reservoirs for Salmonella but unaware that all reptiles can carry Salmonella. The bearded dragon was placed outside the home and later donated to a zoo.

North Dakota. During March 1998, twin infants aged 2 weeks were admitted to a hospital after 1 day of poor feeding, diarrhea, and fever. They were treated intravenously with ampicillin for 6 days. The infants' mother and a child aged 3 years in the home also had diarrhea. Stool specimens from one of the twins, the mother, and the older child yielded Salmonella with the partial serotype O group 44, 45, 47, 48, of 50, H antigen G complex. The family recently had acquired an iguana, which was not allowed out of its cage. Only the mother handled the reptile and cleaned the cage. When the family learned that the iguana was the probable source of Salmonella infections, the iguana was euthanized. Culture of intestinal contents from the iguana yielded Salmonella with the same partial serotype as the patients' isolates. The clinical isolate from the twin was sent to CDC for complete serotyping and found to be Salmonella serotype IV 48:g, [z.sub.51]:-(known formerly as S. Marina).

Ohio. During August-October 2000, local health departments reported seven gastrointestinal illnesses associated with iguanas or turtles acquired at county fairs. In one incident, two siblings aged 11 and 13 years with diarrhea and abdominal cramping visited an ED. No stool specimens were collected from the children. However, stool specimens from a turtle that the siblings received at a county fair yielded Salmonella serotype Sandiego. During the same period, a stool specimen from a man aged 20 years with diarrhea also yielded S. Sandiego; he recently had won a turtle at a county fair. Isolates from the children's turtle and the man were indistinguishable by PFGE.

Wisconsin. During November 2002, an infant aged 24 days was admitted to a hospital after 1 day of bloody diarrhea. The infant was hospitalized for 3 days and received intravenous fluids and supportive care. A stool culture yielded Salmonella serotype IV 44:[z.sub.4][z.sub.23]:-. The infant was treated for 14 days with oral amoxicillin. An iguana was reported living in the home of the infant's father; however, attempts to collect stool samples from the iguana were unsuccessful.

Two weeks later, an infant aged 4 months in a neighboring county visited a hospital after 8 days of fever of 100.3[degrees]F (37.9[degrees]C) and 3 days of decreased range of motion in the left hip. Salmonella serotype IV 44:[z.sub.4][z.sub.23]:- was isolated from both left hip aspirate and blood cultures. The infant was hospitalized for 6 days and treated intravenously with cefotaxime and gentamicin. An iguana was reported living in the infant's home, but the reptile was removed before it could be tested. Both iguanas associated with the infants were traced back by the state health department to the same distributor in Florida.

Editorial Note: Salmonellosis associated with reptiles is a continuing public health concern (5,6). During the 1970s, small pet turtles were a major source of Salmonella infections in the United States (1). In 1975, the Food and Drug Administration banned commercial distribution of small (i.e., <4 in. long) turtles; the majority of states prohibited the sale of such turtles. These measures prevented an estimated 100,000 cases of salmonellosis among children each year (1). However, reptiles remain popular pets in the United States; during 1991-2001, the estimated number of households with reptiles doubled from approximately 850,000 to 1.7 million (7). The increase in pet reptile popularity has been paralleled by an increase in the number of reptile-related Salmonella serotypes isolated from humans (2,6).

Reptiles are commonly colonized with Salmonella and shed the organism intermittently in their feces (6). Attempts to treat reptiles with antibiotics to eliminate Salmonella carriage have been unsuccessful and might lead to increased antibiotic resistance (5). Salmonella survives well in the environment and can be isolated for prolonged periods from surfaces contaminated by reptile feces (8). For this reason, even minimal indirect contact with reptiles can result in illness (2,5).

Increasing evidence suggests that amphibians also are a source for salmonellosis (3,4). Frogs and toads are frequent carriers of Salmonella and have been linked by epidemiologic evidence to outbreaks (3,4). In a population-based, case-control study, housing an amphibian was associated independently with Salmonella infection (3). Overall, reptile and amphibian contacts are estimated to account for 74,000 (6%) of the approximately 1.2 million sporadic Salmonella infections that occur each year in the United States (3).

Gaps remain in the public's understanding of amphibian-and reptile-associated salmonellosis. In one study, fewer than half the families with salmonellosis and known iguana exposure suspected their iguanas might have been the cause of illness (2). Per-store owners, health-care providers, and veterinarians should provide information and prevention messages about salmonellosis to owners and potential purchasers of reptiles and amphibians. Educational materials are available from the Per Industry Joint Advisory Council, telephone 800-553-7387.

In 1999, the National Association of State Public Health Veterinarians and the Council of State and Territorial Epidemiologists recommended that state and local agencies adopt regulations to prohibit the sale of gift of reptiles without written point-of-sale education to consumers about the risks for and prevention of reptile-associated salmonellosis (9). In February 2003, CDC polled health departments in all 50 states and New York City (NYC) to determine whether such regulations existed. Among the 49 health departments responding, four states (Colorado, Illinois, Kansas, and Texas) required pet stores to provide information about salmonellosis to persons purchasing any reptile; tire (California, Connecticut, Maryland, Michigan, and New York) required providing salmonellosis information to persons purchasing a turtle but not other reptiles. Tennessee prohibited sale of all turtles. NYC prohibited sale of certain reptiles, including iguanas, small turtles, and boas, and required posting of information about reptile-associated salmonellosis where other reptiles were sold.

Evaluation of the effectiveness of mandated point-of-sale education in reducing amphibian- and reptile-associated salmonellosis could help guide future prevention efforts, in the meantime, areas such as NYC have adopted restrictions on the sale of certain reptiles similar to those for small turtles.

* California, Connecticut, Florida, North Dakota, Ohio, and Wisconsin. At least six other states (Kansas, Maine, Maryland, Oklahoma, Washington, and Wyoming) reported similar cases.

References

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

(2.) 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.

(3.) Mermin J, Hurwagner I., Vugia D, et al. Reptiles, amphibians, and human Salmonella infection: a population-based, case-control study. Clin Infect Dis Suppl (in press).

(4.) Srikantiah P, Lay JC, Crump JA, et al. An outbreak of Salmonella Javiana associated with amphibian contact--Mississippi, 2001. Presented at the International Conference on Emerging Infectious Diseases, Atlanta, Georgia, 2002.

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

(6.) CDC. Reptile-associated salmonellosis--selected states, 1996-1998. MMWR 1999;48:1009-13.

(7.) Wise JK, Heathcott BL, Gonzalez MI,. Results of the AVMA survey on companion animal ownership in U.S. pet-owning households. J Am Vet Med Assoc 2002;221:1572-3.

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

(9.) Council of State and Territorial Epidemiologists. Reptile-associated salmonellosis and prevention education. CSTE position statement 1999-ID 13. Available at http://www.cste.org/ps/1999/1999-id-13.htm.

Reported by: R Reporter, MD, Los Angeles County. Health Dept; B Sun, DVM, California Dept of Health Svcs. J Monopoli, MPH, East Shore Health District, Branford; Q Phan, MPH, J Hadler, MD, Connecticut Dept of Public Health. P Tiffany, Osceola County Health Dept; Z Mulla, PhD, R Baker, MS, PD Fiorella, PhD, Florida Dept of Health. K Kruger, L Shireley, MPH, D Johnson, MS, D Steinbach, North Dakota Dept of Health. K Smith, DVM, E Salehi, MPIL Ohio Dept of Health. N Joseph, J Archer, MS, J Davis, MD, Wisconsin Dept of Health and Family Svcs. N Snipes, DVM, J Ovitt, DVM, F Angulo, DVM, Div of Bacterial and Mycotic Diseases, National Center for Infectious Diseases; S Gottlieb, MD, EIS Officer, CDC.

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