Four Multistate Outbreaks of Human Salmonella Infections Linked to Small Turtles

Introduction

CDC collaborated with public health, veterinary, agriculture, and wildlife officials in many states, U.S Fish and Wildlife Service, the U.S. Department of Agriculture’s Animal and Plant Health Inspection Service (USDA-APHIS), and the U.S. Food and Drug Administration (FDA) Center for Veterinary Medicine to investigate four separate multistate outbreaks of human Salmonella infections. Results from these investigations indicated that contact with small turtles or their environment were the likely source of these outbreaks.

Contact with reptiles (such as turtles, snakes, and lizards) can be a source of human Salmonella infections. Reptiles can carry Salmonella germs and still appear healthy and clean. Salmonella germs are shed in reptile feces (droppings) and can easily contaminate their bodies and anything in areas where these animals live. Reptiles that live in tanks or aquariums can contaminate the water with germs, which can spread to people. Turtles with a shell length of less than 4 inches are a well-known source of human Salmonella infections, especially among young children. Because of this risk, the FDA banned the sale and distribution of these turtles in 1975.

Public health investigators are using the PulseNet system to identify illnesses that may be part of these outbreaks. PulseNet, coordinated by CDC, is the national subtyping network of public health and food regulatory agency laboratories. PulseNet performs DNA fingerprinting on Salmonella bacteria isolated from ill people by using techniques called pulsed-field gel electrophoresis (PFGE) and whole genome sequencing (WGS). CDC PulseNet manages a national database of these DNA fingerprints to identify possible outbreaks.

Investigation of the Outbreaks

In four separate multistate outbreaks, a total of 133 people infected with the outbreak strains of Salmonella were reported from 26 states between January 16, 2015 and April 8, 2016. In interviews, ill people answered questions about contact with animals during the week before becoming ill; 55 (50%) of the 110 people interviewed reported contact with small turtles or their environments, such as water from a turtle habitat, before their illness. Twenty-five (45%) of the 55 ill people who had contact with small turtles reported purchasing the turtle from a street vendor or receiving the turtle as a gift. One ill person received a small turtle purchased at a flea market vendor who obtained the turtles from Tangi Turtle Farm in Louisiana.

On April 28, 2016, the World Health Organization (WHO) posted on their Disease Outbreak News to inform the international health community about the CDC outbreak investigation. Because small turtles raised in the United States are exported to other countries, WHO indicated that there is a risk to people, especially to young children, in other countries.

The National Antimicrobial Resistance Monitoring System (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 a partnership among the 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 other bacteria isolated from clinical specimens submitted to NARMS by public health laboratories. CDC’s NARMS laboratory conducted antibiotic resistance testing on clinical isolates collected from 15 people infected with one of the four outbreak strains. One isolate was resistant to ampicillin, streptomycin, gentamicin, and tetracycline;  the other 14 isolates were susceptible to all antibiotics tested.

Summaries for each of the four separate multistate outbreak investigations are provided below.

Outbreak 1: Salmonella Sandiego Investigation

Seventeen people infected with the outbreak strain of Salmonella Sandiego were reported from 9 states. The number of ill people identified in each state was as follows: California (6), Florida (1), Illinois (3), Mississippi (1), Oklahoma (1), Pennsylvania (1), South Carolina (1), Texas (2), and Vermont (1).

In interviews, ill people answered questions about contact with animals in the week before they became ill. Of the 13 ill people who were interviewed, 8 (62%) reported contact with small turtles or their environments, such as water from a turtle habitat, in the week before they became ill.

Among people who reported the date they became ill, illnesses began between January 16, 2015 and November 22, 2015. Ill people ranged in age from younger than 1 year to 77 years, with a median age of 8. Sixty-five percent of ill people were female. Among the 15 ill people with available information, 5 (33 %) were hospitalized. No deaths were reported.

Outbreak 2: Salmonella Poona and Salmonella IIIb 61:i:z53 Investigation

Seventy people infected with the outbreak strains of Salmonella Poona and Salmonella IIIb 61:i:z53 were reported from 21 states. The number of ill people identified in each state was as follows: Alabama (1), Arizona (1), California (26), Connecticut (1), Florida (1), Illinois (3), Indiana (1), Kansas (1), Louisiana (1), Missouri (1), Nevada (2), New Jersey (2), North Carolina (2), New York City (7), Ohio (1), Oregon (1), Pennsylvania (3), South Carolina (4), Tennessee (1), Texas (9), and Virginia (1).

In interviews, ill people answered questions about contact with animals in the week before they became ill. Of the 59 ill people who were interviewed, 33 (56%) reported contact with small turtles or their environments, such as water from a turtle habitat, in the week before they became ill.

Among the people who reported the date they became ill, illnesses began between April 7, 2015 and April 8, 2016. Ill people ranged in age from younger than 1 year to 96 years, with a median age of 6. Forty-three percent of ill people were female. Among the 59 ill people with available information, 21 (36%) were hospitalized. No deaths were reported.

Several states collected samples from turtles and their environments at ill persons’ homes and isolated the outbreak strains of Salmonella Poona.

Outbreak 3: Salmonella Sandiego Investigation

Twenty-one people infected with a different outbreak strain of Salmonella Sandiego were reported from 7 states. The number of ill people identified in each state was as follows: Arizona (2), California (9), New Jersey (1), New Mexico (4), Oregon (2), Texas (2), and Washington (1).

In interviews, ill people answered questions about contact with animals in the week before they became ill. Of the 18 ill people who were interviewed, 7 (39%) reported contact with small turtles or their environments, such as water from a turtle habitat, in the week before they became ill.

Among the people who reported the date they became ill, illnesses began between February 8, 2015 and October 25, 2015. Ill people ranged in age from younger than 1 year to 65 years, with a median age of 19. Fifty-seven percent of ill people were female. Among the 18 ill people with available information, 5 (28%) were hospitalized. No deaths were reported.

Oregon public health officials collected samples from turtles and their environment at ill persons’ homes, and the Oregon State Laboratory isolated the outbreak strain of Salmonella Sandiego.

Outbreak 4: Salmonella Poona Investigation

Twenty-five people infected with a different outbreak strain of Salmonella Poona were reported from 6 states. The number of ill people identified in each state was as follows: Arizona (2), California (10), Nevada (2), New York City (1), Ohio (1), and Texas (9).

In interviews, ill people answered questions about contact with animals in the week before they became ill. Of the 20 ill people who were interviewed, 7 (35%) reported contact with small turtles or their environments, such as water from a turtle habitat, in the week before they became ill.

Among the people who reported the date they became ill, illnesses began between February 11, 2015 and November 14, 2015. Ill people ranged in age from younger than 1 year to 78 years, with a median age of 4. Fifty-four percent of ill people were female. Among the 22 ill people with available information, 7 (32%) were hospitalized. No deaths were reported.

Local health officials in California collected samples from the turtle environment at an ill person’s home, and isolated the outbreak strain of Salmonella Poona.