Summary
Companion animals, like household dogs, are an overlooked transmission point for zoonotic pathogens such as nontyphoidal Salmonella (NTS). Given the proximity of dogs to humans and the use of critically important antibiotics in companion animal medicine, household dogs represent a risk for spread of antimicrobial resistant (AMR) Salmonella. To this end, we aimed to leverage existing biosurveillance infrastructure to investigate AMR and zoonotic potential of NTS isolated from dogs and humans. We identified all NTS strains isolated from domestic dogs via the Veterinary Laboratory Investigation and Response Network between May 2017 and March 2023 (N=87), and spatiotemporally matched strains isolated from humans in the NCBI Pathogen Isolate Browser (N=77). These 164 strains, collected from 17 states in the United States, formed the basis of our analysis.
Strains isolated from dogs comprised diverse serovars, with most being clinically relevant to human health. All strains possessed AMR determinants for drug classes deemed critically or highly important by the World Health Organization. We identified sixteen NTS isolates from humans closely related to ≥1 of six dog-associated strains. Collectively, our data emphasize the importance of antimicrobial stewardship and sustained biosurveillance beyond human- and agriculture-associated veterinary medicine, using a One-Health framework that accounts for all transmission points including companion animals.
Keywords: Antibiotic Resistance, Genomics, Salmonella
Introduction
Non-typhoidal Salmonella enterica (NTS) is a significant cause of human and animal illness (Centers for Disease Control, US, 2019). Zoonotic transmission of AMR Salmonella to humans occurs through 1) contact with or consumption of contaminated food products or 2) via contact with animals and animal waste. Though Salmonella infections primarily arise from contaminated food, their broad host infectivity and dissemination potential necessitates a One-Health approach to account for all transmission points, including companion animals like dogs (Chantharothaiphaichit et al., 2022; Cherry et al., 2004; Dróżdż et al., 2021; Leahy et al., 2016; Wright et al., 2005).
Salmonella infections in dogs can be clinical or asymptomatic with numerous studies reporting Salmonella isolation from clinically healthy dogs (Carter & Quinn, 2000). In many of these instances, isolates were resistant to ≥1 antibiotics with 45.2% of isolates being multidrug resistant (MDR; resistance to ≥1 agent in >3 antimicrobial classes) (Chantharothaiphaichit et al., 2022; Kiflu et al., 2017; Seepersadsingh et al., 2004; Sweeney et al., 2018). Concerningly, proximity of humans and pet dogs creates ample opportunity for Salmonella zoonosis, and pet management decisions involving food contamination, improper food handling, or both can increase infection likelihood (Behravesh et al., 2010; Finley et al., 2006, 2007; Leonard et al., 2012).
AMR biosurveillance is increasingly applying whole-genome sequencing (WGS), enabling foodborne outbreak investigation and monitoring of AMR potential in relevant pathogens. The National Antimicrobial Resistance Monitoring System (NARMS) uses WGS to understand AMR trends in enteric bacteria with a One-Health approach (Karp et al., 2017). In 2017, the FDA began monitoring AMR in pathogens, like NTS isolated from dogs, collected through the Veterinary Laboratory Investigation and Response Network (Vet-LIRN) (Ceric et al., 2019).
Given the proximity of companion animals to humans, and the human and veterinary significance of AMR emergence, we aimed to leverage available WGS data, collected via Vet-LIRN and NARMS activities, to investigate the AMR and zoonotic potential of NTS isolated from dogs and humans.
Materials and Methods
Using NCBI Sequence Read Archive BioProjects specific to Vet-LIRN Salmonella surveillance (PRJNA481328, PRJNA324575, PRJNA324570, PRJNA316457, PRJNA316452, PRJN284276, PRJNA230403), we identified all NTS strains collected from domestic dogs (Canis lupus familiaris, N = 87) within the United States (U.S.) in the NCBI Pathogen Isolate Browser (National Library of Medicine (US), National Center for Biotechnology Information, 2016). With the collection states and date range of the 87 dog-associated strains as inclusion criteria, we queried NCBI’s Pathogen Isolate Browser and identified all available NTS strains collected from humans (N = 77). These 164 isolates, collected between May 2017 and March 2023 from 17 states in the U.S., formed the basis of our analysis (Table 1; Supplementary Table 1).
Table 1.
Summary of Salmonella strain metadata.
| Dog, N = 871 | Human, N = 771 | Overall, N = 1641 | |
|---|---|---|---|
| Specimen Type | |||
| Abdominal Fluid | 1 | 0 | 1 |
| Abscess | 3 | 1 | 4 |
| Bladder | 1 | 0 | 1 |
| Blood | 1 | 4 | 5 |
| Cerebrospinal Fluid | 1 | 0 | 1 |
| Colon | 2 | 0 | 2 |
| Draining Tract | 1 | 0 | 1 |
| Ear | 2 | 0 | 2 |
| Feces | 41 | 53 | 94 |
| Intestine | 7 | 0 | 7 |
| Liver | 1 | 0 | 1 |
| Lung | 1 | 0 | 1 |
| Lymph Node | 2 | 0 | 2 |
| Mammary Gland | 1 | 0 | 1 |
| Peritoneum | 1 | 0 | 1 |
| Rectal | 0 | 1 | 1 |
| Skin | 2 | 0 | 2 |
| Spleen | 1 | 0 | 1 |
| Stifle Fluid | 1 | 0 | 1 |
| Stomach | 1 | 0 | 1 |
| Synovial Fluid | 1 | 0 | 1 |
| Tissue Swab | 1 | 0 | 1 |
| Tracheal Wash | 1 | 0 | 1 |
| Unspecified | 2 | 7 | 9 |
| Urine | 11 | 11 | 22 |
| Location (State) | |||
| Florida | 5 | 0 | 5 |
| Georgia | 5 | 2 | 7 |
| Illinois | 4 | 0 | 4 |
| Indiana | 2 | 0 | 2 |
| Kansas | 8 | 0 | 8 |
| Kentucky | 8 | 0 | 8 |
| Michigan | 5 | 1 | 6 |
| Minnesota | 1 | 0 | 1 |
| Montana | 1 | 0 | 1 |
| Mississippi | 2 | 1 | 3 |
| North Carolina | 4 | 1 | 5 |
| North Dakota | 1 | 0 | 1 |
| New Jersey | 1 | 0 | 1 |
| Ohio | 5 | 0 | 5 |
| Oklahoma | 3 | 0 | 3 |
| Pennsylvania | 7 | 1 | 8 |
| Texas | 25 | 71 | 96 |
| Collection Year | |||
| 2017 | 2 | 0 | 2 |
| 2018 | 9 | 71 | 80 |
| 2019 | 9 | 0 | 9 |
| 2020 | 13 | 6 | 19 |
| 2021 | 32 | 0 | 32 |
| 2022 | 17 | 0 | 17 |
| 2023 | 5 | 0 | 5 |
Number of Salmonella strains
Raw sequence reads were trimmed with Trimmomatic (Bolger et al., 2014). Following de novo genome assembly with Unicycler (Wick et al., 2017), assembly quality and contamination were assessed with QUAST (Gurevich et al., 2013) and CheckM (Parks et al., 2015), respectively. Genome assemblies were in silico serotyped with both SeqSero2 (Zhang et al., 2019) and SISTR (Yoshida et al., 2016) for concordance. Assembly contigs were screened for AMR- and virulence-associated genes using Abricate (Seemann, 2020) with MEGARes v2.0 (Doster et al., 2020) and Virulence Factor Databases (Chen et al., 2016), respectively.
We performed a reference-based phylogenetic analysis using PhaME (Shakya et al., 2020) and FastTree2 (Price et al., 2010) with Salmonella enterica ser. Typhimurium LT2 (GCA_000006945.2) as the reference genome. Using a matrix of pairwise single-nucleotide polymorphism (SNP) differences, hierarchical clustering was performed. All results were visualized using ape (v5.7), dendextend (1.17.1), ggtree (v3.9.0), and ggpubr (v0.6.0) packages in R version 4.3.0.
Results
Of the 87 dog-associated isolates, 82 were serotyped as Salmonella enterica subspecies I. Among the remaining five, four were typed as Salmonella enterica subspecies IV and one was typed as Salmonella bongori. Though these strains represented 31 different serotypes, the five most common were Newport (N=16), Typhimurium (N=9), Infantis (N=8), Enteritidis (N=6), and Anatum (N=5) (Table 2). All 77 human-associated isolates were typed as Salmonella enterica subspecies I serotypes. Eleven different serotypes were identified, and the five most common were Enteritidis (N=36), Newport (N=9), Typhimurium (N=8), Oranienburg (N=6), and Infantis (N=5) (Table 2).
Table 2. Serotype distribution between human- and dog-associated sources.
Outlines serotype and species determinations from SISTR and SeqSero2.
| Dog, N = 871 | Human, N = 771 | Overall, N = 1641 | |
|---|---|---|---|
| Serotype | |||
| 48:z81:- | 1 | 0 | 1 |
| Agbeni | 1 | 0 | 1 |
| Anatum | 5 | 2 | 7 |
| Berta | 1 | 1 | 2 |
| Dublin | 4 | 0 | 4 |
| Enteritidis | 6 | 36 | 42 |
| Hartford | 4 | 0 | 4 |
| Heidelberg | 1 | 0 | 1 |
| I -:r:1,5 | 1 | 0 | 1 |
| I 16:l,v:- | 1 | 0 | 1 |
| I 4,[5],12:i:- | 4 | 4 | 8 |
| Infantis | 8 | 5 | 13 |
| Inverness | 1 | 0 | 1 |
| IV 43:z4,z32:- | 3 | 0 | 3 |
| IV 48:g,z51:- | 1 | 0 | 1 |
| Javiana | 2 | 0 | 2 |
| Kottbus | 1 | 0 | 1 |
| Litchfield | 1 | 0 | 1 |
| Mbandaka | 2 | 0 | 2 |
| Mississippi | 1 | 0 | 1 |
| Montevideo | 1 | 0 | 1 |
| Muenchen | 1 | 0 | 1 |
| Muenster | 0 | 4 | 4 |
| Newport | 16 | 9 | 25 |
| Norwich | 1 | 0 | 1 |
| Oranienburg | 3 | 6 | 9 |
| Paratyphi B var. Java | 2 | 1 | 3 |
| Rubislaw | 1 | 0 | 1 |
| Saintpaul | 1 | 0 | 1 |
| Sandiego | 1 | 0 | 1 |
| Schwarzengrund | 2 | 0 | 2 |
| Stanley | 0 | 1 | 1 |
| Typhimurium | 9 | 8 | 17 |
| Species | |||
| enterica (subspecies I) | 82 | 77 | 159 |
| houtenae (subspecies IV) | 4 | 0 | 4 |
| bongori | 1 | 0 | 1 |
Number of Salmonella strains
A total of 55 different antimicrobial resistance genes (ARGs) were identified in dog-associated strains. These ARGs are associated with specific drug class resistance (N=26), multi-drug resistance (N=4), and multi-compound resistance (N=25). (Table 3; Figure 1A). In human-associated isolates, 53 different ARGs were identified. These ARGs are associated with specific drug class resistance (N=23), multi-drug resistance (N=4), and multi-compound resistance (N=26). (Table 3; Figure 1B).
Table 3. Distribution of unique antimicrobial resistance genes by antimicrobial class.
Number of genes identified within each antimicrobial class, compared by strain host.
| Dog, N = 551 | Human, N = 531 | |
|---|---|---|
| Drug Class | ||
| Aminoglycosides | 8 | 6 |
| Bacitracin | 1 | 1 |
| Beta-lactams | 6 | 5 |
| Drug and biocide and metal resistance | 11 | 11 |
| Drug and biocide resistance | 13 | 14 |
| Drug and metal resistance | 1 | 1 |
| Fluoroquinolones | 1 | 2 |
| Fosfomycin | 1 | 0 |
| Glycopeptides | 1 | 0 |
| Macrolides, Lincosamides, Streptogramines | 2 | 1 |
| Multi-drug resistance | 4 | 4 |
| Phenicol | 1 | 2 |
| Sulfonamides | 2 | 2 |
| Tetracyclines | 2 | 3 |
| Trimethoprim | 1 | 1 |
Total number of unique genes
Figure 1. Presence of antimicrobial resistance genes in NTS from dogs (A) and humans (B).
Genes are rows with strain accession IDs as columns. Colors indicate the MEGARes (v2) database drug class category with which each gene is associated: Aminoglycosides, Bacitracin, ß-lactams, Multi-compound, Fluoroquinolones, Fosfomycin, Glycopeptides, MLS (macrolide-linocosamide-streptagramin), Multi-drug, Phenicol, Sulfonamide, or Trimethoprim.
Across dog- and human-associated strains respectively, 139 and 123 unique virulence genes primarily associated with invasion were identified. Additional functional categories include adherence, colonization, extraintestinal invasion, immune modulation, iron sequestration, and toxicity (Table 4; Figure 2A–B). The virulence gene shdA, associated with prolonged fecal shedding (Kingsley et al., 2000), was identified in 34 dog-associated isolates.
Table 4. Distribution of unique virulence-associated genes by category.
Number of genes identified within each virulence functional category, compared by strain host.
| Dog, N = 1391 | Human, N = 1231 | |
|---|---|---|
| Virulence Category | ||
| Adherence | 27 | 24 |
| Colonization | 3 | 3 |
| Extraintestinal Invasion | 1 | 1 |
| Immune Modulation | 4 | 4 |
| Invasion | 82 | 82 |
| Iron Sequestration | 18 | 5 |
| Other | 3 | 3 |
| Toxicity | 1 | 1 |
Total number of unique genes
Figure 2. Presence of virulence-associated genes in NTS from dogs (A) and humans (B).
Colors indicate the virulence category with which each gene is associated.
Relative to the Salmonella Typhimurium LT2 reference genome, 446,396 SNPs were identified across the 164 strains. The SNP-based phylogeny is shown in Figure 3. Strain clustering was driven by Salmonella subspecies and serotype, with no apparent trends in location or time proximity. Within a clade of S. Enteritidis, two dog-associated strains were each closely related (<20 SNP differences) to six different human strains (Table 5). In a clade of S. Infantis, one dog-associated strain was closely related to five human-associated strains. Single dog-associated strains of S. Newport and S. I 4,[5],12:i:- were each closely related to a human-associated strain of the same serotype (Table 5).
Figure 3. Approximately maximum-likelihood phylogeny of dog and human NTS.
Inner rings denote host association and collection year. Tip colors indicate Salmonella species and/or subspecies. Tip labels denote strain SRA accession ID.
Table 5. Pairs of closely related non-typhoidal Salmonella strains from dogs and humans.
Includes related strain pairs from different hosts, associated number of SNP differences, and serotype.
| Dog Strain | Human Strain | SNP Differences1 | Serotype |
|---|---|---|---|
| SRR12641661 | SRR7094479 | 19 | Enteritidis |
| SRR12641661 | SRR7262457 | 17 | Enteritidis |
| SRR12641661 | SRR6986073 | 17 | Enteritidis |
| SRR12641661 | SRR7298832 | 15 | Enteritidis |
| SRR12641661 | SRR7262459 | 13 | Enteritidis |
| SRR12641661 | SRR7299302 | 13 | Enteritidis |
| SRR14704455 | SRR6973036 | 16 | Enteritidis |
| SRR15050790 | SRR7262137 | 10 | I 4,[5],12:i:- |
| SRR15277966 | SRR6903162 | 15 | Infantis |
| SRR15277966 | SRR6973597 | 11 | Infantis |
| SRR15277966 | SRR7299223 | 15 | Infantis |
| SRR15277966 | SRR7262823 | 17 | Infantis |
| SRR15277966 | SRR7299351 | 18 | Infantis |
| SRR18347379 | SRR7299295 | 20 | Newport |
| SRR23734591 | SRR7094479 | 14 | Enteritidis |
| SRR23734591 | SRR6986073 | 14 | Enteritidis |
| SRR23734591 | SRR7262459 | 20 | Enteritidis |
| SRR23734591 | SRR7299213 | 18 | Enteritidis |
| SRR23734591 | SRR7299302 | 20 | Enteritidis |
| SRR23734591 | SRR7262086 | 19 | Enteritidis |
Number of single nucleotide polymorphism differences between strains
Discussion
Non-typhoidal Salmonella (NTS) are recognized for their broad host range and zoonotic potential as animal and human pathogens. As NTS infections in companion animals are under-investigated, we leveraged surveillance activities of the FDA’s Vet-LIRN to characterize NTS isolated from dogs. We identified a diverse population of serotypes including those clinically relevant to human health and all isolates in this study, independent of host association, possessed AMR determinants ranging from general efflux capacities to drug-specific associations. Our examination of spatiotemporally matched strains from human clinical cases identified sixteen NTS isolates related to at least one of six dog-associated strains.
Given the absence of a dog-adapted serotype (Carter & Quinn, 2000; Ceric et al., 2019; Leahy et al., 2016; Leonard et al., 2012; Reimschuessel et al., 2017), the serotype diversity revealed by our study was expected. Of the non-S. enterica spp. enterica strains identified, all have been previously isolated from a domestic dog (Andruzzi et al., 2020; Giammanco et al., 2002). The most common dog-associated serotypes in this study overlapped with those most represented among human-associated strains, and align with the Laboratory-based Enteric Disease Surveillance 2016 report regarding those most frequently reported in human Salmonella infections (National Center for Emerging and Zoonotic Infectious Disease, 2016), suggesting transmission or possible common Salmonella exposures.
As companion animals, dogs represent an understudied transmission point in Salmonella zoonoses (Hoelzer et al., 2011). We identified six dog-associated strains with 10–20 SNP differences relative to human strains, suggesting strain relatedness between Salmonella in human and dog reservoirs – which could indicate zoonotic, reverse-zoonotic, and common source as potential transmission points. Probable transmission of NTS between companion animals and humans has been reported primarily in susceptible populations, such as infants, young children and the elderly; however, probable transmission to healthy adults has also been reported in veterinary clinic and animal shelter outbreaks (Cherry et al., 2004; Morse et al., 1976; Sato et al., 2000; Wright et al., 2005). As with animal products for human consumption, improper handling of contaminated pet food products, including dry food and raw food, can also introduce Salmonella into household environments, increasing transmission risk (Arsevska et al., 2017; Behravesh et al., 2010; Davies et al., 2019; Finley et al., 2006, 2007; Hellgren et al., 2019; Schotte et al., 2007).
While the isolates studied here were from clinical cases, most dog-associated NTS infections do not yield clinical disease, apparently healthy dogs may shed Salmonella in their feces (Demirbilek, 2018; Leahy et al., 2016; Reimschuessel et al., 2017; Schotte et al., 2007). Notably, we identified shdA, a gene associated with prolonged fecal shedding, in 39% of strains (Kingsley et al., 2000). Thus, seemingly healthy dogs may be carriers of Salmonella, disseminating the bacteria for longer durations.
Though antibiotic treatment of salmonellosis is reserved for severe and invasive disease, drug resistant NTS are nonetheless considered a serious threat. In our study, we identified strains with resistance determinants to World Health Organization-defined, critically and highly important antibiotic classes. Although antibiotics are not typically prescribed for diarrheal Salmonella infections diagnosed in dogs, there are no universally accepted guidelines for antibiotic treatment of Salmonella gastroenteritis or more complicated infections in companion animal medicine, and little regulation exists regarding the use of antimicrobials in companion animals (Andruzzi et al., 2020).
Despite this study’s sampling limitations and selection bias which preclude any direct causal or epidemiological conclusions related to source attribution, we provide documentation of AMR in NTS from dogs, supporting the rationale for ongoing surveillance via Vet-LIRN and other entities, and reporting of AMR pathogens in companion animals as noted in the NARMS 2021–2025 Strategic Plan (The National Antimicrobial Resistance Monitoring System Strategic Plan 2021–2025, 2020). Our findings highlight the need to continue AMR surveillance within the One-Health paradigm.
Supplementary Material
Supplementary Table 1. Comprehensive Salmonella strain metadata.
Impacts.
Companion animals, like household dogs, are an overlooked zoonotic pathogen transmission point.
The Veterinary Laboratory Investigation and Response Network can be leveraged to characterize non-outbreak-associated strains of zoonotic pathogens.
Antimicrobial stewardship in companion animal veterinary medicine is crucial for mitigating antimicrobial resistance within the One-Health paradigm.
Acknowledgements
We are grateful to the staff from FDA Vet-LIRN and CDC-NARMS programs for their help with characterization of NTS isolates from dogs and humans. We are indebted to Dr. Heather Tate (FDA-NARMS) for her guidance during preparation and revision of the manuscript. We thank Dr. Olgica Ceric with the FDA-CVM/Office of Research/Vet-LIRN for assistance with clarification of data on Salmonella from dogs and valuable insights.
We gratefully acknowledge funding provided by U.S. FDA for collaboration in the National Antimicrobial Resistance Monitoring System (grant number 1U01FD006253-01 to PADOH) and the CDC Epidemiology and Laboratory Capacity (ELC) for collaboration in National Antimicrobial Resistance Monitoring (CDC-RFA-CI10-101204PPHF13), the National Institutes of Health /Penn State University for the Computation, Bioinformatics and Statistics (CBIOS) Predoctoral Training Program (T32 GM102057), the USDA APHIS NBAF Scientists Training Program (NSTP) (AP23VSD&B000C001), and the USDA National Institute of Food and Agriculture and Hatch Appropriations under Projects #PEN04752 and #PEN04731 Accessions #1023328 and #1022444.
Footnotes
Conflict of Interest Statement
The authors declare no conflict of interest.
Ethical Approval Statement
Ethics approval was not required as this study does not involve human or animal participants and was conducted using publicly accessible data.
Data Availability Statement
All sequence data was obtained from NCBI under BioProjects: PRJNA481328, PRJNA324575, PRJNA324570, PRJNA316457, PRJNA316452, PRJN284276, and PRJNA230403. The code used in this analysis is available at https://github.com/gandalab/pet-salmonella.
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Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Supplementary Materials
Supplementary Table 1. Comprehensive Salmonella strain metadata.
Data Availability Statement
All sequence data was obtained from NCBI under BioProjects: PRJNA481328, PRJNA324575, PRJNA324570, PRJNA316457, PRJNA316452, PRJN284276, and PRJNA230403. The code used in this analysis is available at https://github.com/gandalab/pet-salmonella.