Outbreak of multidrug-resistant Salmonella infections in people linked to pig ear pet treats, United States, 2015-2019: results of a multistate investigation

Abstract

Background: International distribution of contaminated foods can be a source of Salmonella infections in people and can contribute to the spread of antimicrobial-resistant bacteria across countries. We report an investigation led by the United States Centers for Disease Control and Prevention, the Food and Drug Administration (FDA), and state governmental officials into a multistate outbreak of salmonellosis linked to pig ear pet treats.

Methods: Pig ear treats and companion dogs were tested for Salmonella by state officials and the FDA. Products were traced back to the country of origin when possible. Cases were defined as outbreak illnesses in people associated with one of seven Salmonella serotypes genetically related to samples from pig ear pet treats, with isolation dates from June 2015 to September 2019. Whole genome sequencing (WGS) of isolates was used to predict antimicrobial resistance.

Findings: The outbreak included 154 human cases in 34 states. Of these, 107 of 122 (88%) patients reported dog contact, and 65 of 97 (67%) reported contact with pig ear pet treats. Salmonella was isolated from 137 pig ear treats, including some imported from Argentina, Brazil, and Colombia, and from four dogs. WGS predicted 77% (105/137) of human and 43% (58/135) of pig ear treat isolates were resistant to ≥3 antimicrobial classes.

Interpretation: This was the first documented United States multistate outbreak of Salmonella infections linked to pig ear pet treats. This multidrug-resistant outbreak highlights the interconnectedness of human health and companion animal ownership and the need for zoonotic pathogen surveillance to prevent human illness resulting from internationally transported pet food products.

Funding: Animal Feed Regulatory Program Standards award. Animal and product testing conducted by FDA Vet-LIRN was funded by Vet-LIRN infrastructure grants (PAR-22-063).

Keywords: Antimicrobial resistance; Outbreak; Public health; Salmonellosis.

Fig. 1

Human and dog cases of salmonellosis and pig ear pet treat isolates – United States, 2015–2019. Cases were defined as human infection with Salmonella serotypes Cerro, Derby, I 4,[5],12:i:-, London, Infantis, Newport, or Rissen genetically related to isolates from pig ear pet treats, with isolation dates from June 2015 to September 2019. Genetic relatedness of human and pig ear treat isolates was determined based on the identification of a matching pulsed field gel electrophoresis pattern or within a specific range of allele differences determined by whole genome sequencing analysis by core genome multi-locus sequence typing. A total of 34 states had human cases in this outbreak. The highest number of cases (24) occurred in Iowa. Black circles indicate states in which sampling of pig ear treats was conducted, and the number of positive samples is indicated. Dog icons indicate dogs testing positive for Salmonella.

Fig. 2

Epidemiologic curve of isolation dates of Salmonella from humans and dog isolates, June 10, 2015, to September 13, 2019. Cases were defined as human infection with Salmonella serotypes Cerro, Derby, I 4,[5],12:i:-, London, Infantis, Newport, or Rissen genetically related to isolates from pig ear pet treats. Dogs were tested for Salmonella following consumer complaints of illness in their dogs after feeding pig ear pet treats. ∗ Isolates obtained from dogs include Salmonella serotypes Infantis (n = 1) and Cerro (n = 2) and Salmonella enterica subspecies arizonae (n = 1).

Fig. 3

Age distribution of patients. Cases were defined as human infection with Salmonella serotypes Cerro, Derby, I 4,[5],12:i:-, London, Infantis, Newport, or Rissen genetically related to isolates identified from sampling of pig ear pet treats, with isolation dates from June 2015 through September 2019. Patient age was collected during routine interviews performed by state and local health officials. Median patient age was 40 years (range < 1–90 years).

Fig. 4

This dendrogram represents the genetic relatedness of Salmonella isolates included in this outbreak that were collected from 2015–2019 in the United States and reported to PulseNet, the national molecular subtyping network for foodborne disease surveillance at the Centers for Disease Control and Prevention. The shaded ring represents each Salmonella serotype (or Salmonella enterica subspecies arizonae) detected among isolates obtained from ill people, pig ear pet treats, or dogs. Red boxes indicate isolates obtained from pig ear treats. Light blue boxes indicate isolates obtained from dogs.

Fig. 5

Traceback diagram of pig ear pet treats yielding Salmonella isolates. Traceback conducted by FDA determined the routes of supply of pig ear pet treats between the South America suppliers and specific retail store locations (unique routes of supply are indicated by different colored arrows). Black arrows represent pig ear treats in retail stores that could be traced to supplying company B but not the country of origin. Pig ear treats were sampled from seven retail stores and from one distribution facility; pig ear treats at all of these locations were positive for Salmonella (as indicated by a star icon).