Abstract
Salmonellosis is a significant public health threat responsible for millions of human cases annually but is also of significance to domestic and wild animals around the globe. While human infections are often foodborne, an increasing number of cases arise from environmental sources and contact with animals, including wild birds. Understanding the persistence of Salmonella in shared environments is critical for mitigating zoonotic transmission risks and understanding transmission dynamics for pets and free-living wildlife. Two experiments were conducted to investigate Salmonella persistence on surfaces relevant to wild bird-people interactions. One was a controlled experiment to compare the persistence of an avian-derived Salmonella Typhimurium isolate on bird feeders made of different materials. A total of 9 (7%) swabs were culture positive for Salmonella. Although there was no statistical difference in prevalence rates and persistence, Salmonella was primarily reisolated from plastic feeders. The second experiment investigated the prevalence and persistence of Salmonella on picnic tables in a South Florida park that were contaminated with bird feces. Salmonella prevalence on the picnic tables was 27%. When tracking fecal piles over time, 33% to 42% of fecal piles were Salmonella culture positive for 1 to 4 days. A total of 13 to 14 serotypes were detected, of which 5 serovars are in the top 20 for human infections. Our trials indicate that Salmonella can persist on bird feeders and picnic tables and precautionary measures should be adopted to reduce exposure. The companion Currents in One Health by Seixas et al, JAVMA, forthcoming 2025, addresses in-depth information about Salmonella epidemiology in free-living birds.
Salmonella enterica infections are a significant public health threat, responsible for over 93 million annual cases of human illness worldwide.1 In the US, there are an estimated 1.35 million cases of salmonellosis, and 420 deaths are reported annually, although only an estimated 1 of every 30 cases are diagnosed.2 Most cases of human salmonellosis are caused by food-borne Salmonella strains associated with produce or undercooked meat. However, a rising subset of human infections are often associated with environmental exposure to unidentified sources or contact with animals such as pet reptiles or backyard poultry.2 Salmonella, primarily S enterica subspecies enterica serovar Typhimurium, is also responsible for large-scale mortality events of free-living birds,3–7 although some wild birds can also be asymptomatic carriers,8,9 with significance to other wildlife and people. The key to understanding Salmonella transmission among birds, and from birds to people, is environmental persistence. The persistence of Salmonella can be affected by various factors such as ambient temperature, moisture, biofilm, and environmental nutrient conditions.10–13 Under ideal conditions (eg, optimal temperature 35 to 43 °C, pH 7 to 7.5.), Salmonella is thought to persist in the environment for extended periods of time, yet most persistence studies are conducted under controlled experimental conditions or are performed for the application of commercial agriculture or food products and may not represent in situ conditions or natural environments.13–18 For example, most persistence studies have examined Salmonella in soil, surface water, vegetation, and poultry litter, yet there is a lack of information on the persistence of Salmonella from wild birds on various surfaces that are relevant sources for its transmission to people and other birds.
In 2021, following an epidemiological investigation of 29 human cases of gastrointestinal disease caused by S Typhimurium, the CDC documented a relationship between human cases and a concurrent avian salmonellosis outbreak.7 Of the 29 cases, nearly half (n = 14) of the individuals were hospitalized, and the epidemiological outbreak surveys determined that the source was contact with bird feeders, sick or dead wild birds, or pets that had contact with wild birds.7 Salmonellosis has been increasing in wild birds in the US and internationally for several decades.4,19,20 Correspondingly, globally, human outbreaks have been associated with direct contact with birds and bird feeders.21–25 Patel et al7 proposed that different factors, including avian density, season, and feeder type, might influence Salmonella transmission among wild birds. The feeding of wild birds has become a popular activity in the US and Europe, and it drives a US multibillion-dollar industry.26 Other animals (ie, domestic cats and dogs and other wildlife) can develop salmonellosis when they have contact with sick birds at feeders, which may facilitate or enhance transmission back to people.7,27–30
In the current study, 2 separate experiments were conducted to investigate the persistence of Salmonella on surfaces relevant to interactions among wild birds and people. One was a controlled experiment to investigate the persistence on bird feeders made of different materials (wood, plastic, and wood or plastic coated with an antimicrobial coating). We hypothesized that wooden feeders would facilitate the growth and persistence of Salmonella and that the antimicrobial coating would inhibit Salmonella growth on either plastic or wooden feeders. The second was a seminatural experiment intended to mimic real-life conditions to investigate the contamination and persistence of Salmonella on picnic tables in a city park by a wading bird (American white ibis [Eudocimus albus]), which was previously established as a reservoir of Salmonella.4,31,32
Methods
Bird feeder trial
Design and study site—This trial was conducted in Clarke County, GA, from February to March 2022. To develop an inoculant, 18 g of fresh chicken feces were collected from a local private flock with no history of Salmonella infection and homogenized. A 1-g sample was aliquoted into individual 15-mL polypropylene conical tubes and then sterilized in an autoclave (121 °C for 30 minutes at 15 psi of pressure). The individual aliquots were allowed to come to room temperature and were then inoculated with 1.5 X 107 CFU of a Salmonella Typhimurium isolate obtained during a previous avian salmonellosis outbreak in Pinellas County, FL. The isolate was grown overnight in lysogeny broth at 37 °C, pelleted by centrifugation, and washed in 1X PBS before inoculation. The inoculant was then homogenized by vortexing. Inoculated samples were immediately transported to a modified shade house at Whitehall Experimental Forest (Athens, GA) where a total of 12 feeders of 4 feeder types (3 plastic, 3 plastic + antimicrobial coating, 3 wood, and 3 wood + antimicrobial coating) were randomized by feeder type and seeded with 1 g of Salmonella-inoculated feces and 0.5 mL of sterile physiologic saline along a 0.889-cm2 ledge (Figure 1). The coated feeders had been previously treated with spray-coated antimicrobial polymers patented and developed by Locklin and others.33–36 These quaternary ammonium materials were permanently attached to the plastic or wood feeder surfaces using photochemical irradiation. The shade house was enclosed by nylon shade cloth to exclude vertebrate animals from entering the house, both for biosafety and to prevent contamination, but allowed adequate airflow. Feeders were swabbed daily for 1 week, every other day for 1 week, and weekly for an additional week for a total of 11 sampling events. Sterile cotton-tipped applicators (McKesson) were prewetted in sterile dulcitol selenite (HiMedia) and swabbed over 0.889 cm2. The same area was swabbed at each time point. Swabs were placed into 10 mL of dulcitol selenite broth and transported back to the University of Georgia (Athens campus) for processing.
Schematic of bird feeder placement and study design for Salmonella persistence trial. Photos show shade house and bird feeders as well as inoculation of feeders.
Citation: American Journal of Veterinary Research 2025; 10.2460/ajvr.24.12.0397
Picnic table trial
Design and study site—All animal procedures were reviewed and approved by the University of Georgia's IACUC (A2019 10-009-Y1-A0). This experiment was conducted in Palm Beach County, FL, in a public park where white ibis form large flocks, people routinely feed ibis human food, and there are structures used by people and ibis (pavilions with picnic tables). We selected 3 tables under a single pavilion. Each table was divided into 4 quadrants (each half of the tabletop plus each side bench; Figure 2). Photos were taken of every quadrant every day to facilitate the counting of new fecal piles per day. Each day for 8 days, to mimic the natural behavior of birds walking on tables to steal food, birds were encouraged to feed on top of the tables for ∼30 minutes or until all quadrants had fresh feces for that day. This time was based on behavior observed by researchers during a concurrent study on white ibis at the park and the typical number of feces observed on other tables in that park.
Schematic of picnic table placement for the South Florida Salmonella persistence trial. Each table had 4 quadrants (Q) with fecal samples present (light green dots in schematic and circles in photo). A single fecal sample was selected as a persistence sample (dark green dots and black circle).
Citation: American Journal of Veterinary Research 2025; 10.2460/ajvr.24.12.0397
To determine Salmonella persistence, on the first day of the experiment, after having fed the birds and encouraged defecation on the tables, 1 large fecal pile from each quadrant was selected to be the “persistence pile” to be followed for several days (Figure 2). A portion of that fecal pile was sampled every day for 4 days. After 4 days, all tables were pressure washed with water by the park maintenance crew, and the experiment was repeated for another 4 days. To determine table prevalence, a pooled sample was taken from each quadrant every day by swabbing a sampling sponge (3M Sponge-Stick saturated with neutralizing buffer; Neogen) along the entire surface, while avoiding the designated persistence pile. Because other park patrons may have used the tables while researchers were absent, new fecal piles were not smeared with the sampling sponge. Instead, the sponge was rubbed across the entire quadrant surface, avoiding all fecal piles, and then was dipped into each new fecal pile to ensure collection, but not smearing of bacteria across the table surface. After the sponge was rubbed across the quadrant or on the persistence pile, it was placed into a sterile Whirlpak and stored in a cooler with a frozen gel pack until enrichment broth was added. Within 4 to 6 hours, 20 mL of dulcitol selenite broth was pipetted into each bag. The bags were sealed, maintained at room temperature, and shipped to the University of Georgia (Athens campus) for processing every 2 to 4 days.
Salmonella isolation methodology for both trials
Salmonella isolation procedures were the same for both trials. Once samples arrived in the lab, the dulcitol selenite broth samples were incubated at 37 °C overnight. Each sample was vortexed and a 100-μL aliquot was inoculated into 10 mL of Rappaport Vassiliadis broth (Oxoid). The broth was incubated in a shaking incubator for 24 hours at 39.5 °C at 100 rpm. The Rappaport Vassiliadis broth was then streaked onto XLT4 agar (Criterion) plates and incubated at 37 °C for 24 hours, followed by an additional 24 hours on the lab bench at room temperature. If colonies morphometrically consistent with Salmonella were present, 1 colony per plate was chosen, and a stab in lysogeny broth agar was created. To confirm the presence of Salmonella, patch plates were made on CHROMagar Salmonella Plus for each presumptive isolate. Patches that turned magenta were considered positive for Salmonella.37
Salmonella serotyping
Presumptive Salmonella isolates were confirmed using an invA qPCR.38–40 The DNA was isolated from 600 µL of overnight culture in lysogeny broth using the Genome Wizard kit (Promega). Serovars were identified using the intergenic sequence ribotyping typing method.40 For isolates whose serovars could not be determined by intergenic sequence ribotyping typing, CRISPR typing was used. The primers and cycling conditions were as described in Shariat et al39 and the amplicon sequences were compared to the data presented by Fabre et al38 to determine serovar. All Sanger sequencing was performed at Eton Bioscience.
Data analysis
To evaluate the association between Salmonella prevalence and feeder type, a Fisher exact test was conducted. A Kaplan-Meier survival analysis was performed to evaluate the relationship between persistence and feeder type, while effect size was evaluated using a Cox proportional hazards model. All analyses were performed using R Studio, version 2023.6.0.421 (The R Foundation).
Results
Bird feeder trial
To confirm that the Salmonella inoculum used to seed the bird feeders had viable Salmonella, we collected a sample from all of the feeders on the day of inoculation or day postinoculation (DPI) 0 (February 22, 2022), and each sample was culture positive for Salmonella. Sampling of the 12 bird feeders after DPI 0 resulted in 132 samples (Table 1); of those samples, 9 (6.8% [9/132]) were culture positive for Salmonella. Prevalence rates for feeders varied upon feeder type with total prevalence rates being highest for plastic + antimicrobial coating (15.2% [5/33]) and lowest for wood (3% [1/33]) and wood + antimicrobial coating (0%); however, there was no statistical difference between feeder type and Salmonella detection (P = .08; Figure 3).
Prevalence and persistence of Salmonella on 4 distinct feeder types (plastic, plastic coated, wood, and wood coated) across 132 samples (33 samples per feeder type) during 11 sampling times from February 22 to March 14, 2022.
| Salmonella prevalence | |||
|---|---|---|---|
| Feeder type | No. of days Salmonella present | Total prevalence per feeder type (%) (n = 33) | No. of DPI Salmonella isolated |
| Plastic | 2 | 9.1 | 2 |
| Plastic coated | 3 | 15.2 | 5 |
| Wood | 1 | 3 | 5 |
| Wood coated | 0 | 0 | 0 |
The number of days Salmonella is present represents the presence of Salmonella in at least 1 of the 3 bird feeder type replicates per sampling period. The number of days postinoculation (DPI) Salmonella was isolated was defined by the last day Salmonella was isolated in at least 1 of 3 replicates per feeder type.
Kaplan-Meier survival curves illustrating Salmonella persistence on various feeder material (plastic, plastic + antimicrobial coating, wood, and wood + antimicrobial coating) over a 5-day period. The y-axis indicates the proportion of inoculated feeders with persistent Salmonella. The x-axis represents the days since the start of the project. The “Number at risk” table represents the number of feeders remaining under observation at each time point. P = .23, suggesting no statistical significance in Salmonella persistence between feeder types.
Citation: American Journal of Veterinary Research 2025; 10.2460/ajvr.24.12.0397
Like prevalence, Salmonella persistence varied by feeder type (Table 1) with the longest persistence period being 5 DPI on the plastic + antimicrobial and wood feeders. Although other feeder types only had persistence for 1 DPI (plastic) or not at all (wood + antimicrobial coating), there was no significant relationship between feeder type and Salmonella persistence (P = .23). When effect size was assessed using a Cox proportional hazards model, plastic-coated feeders had a 68% higher risk of Salmonella persistence compared to plastic (hazard ratio, 1.68; 95% CI, 0.40 to 7.04). In contrast, wood feeders showed a 67% lower risk (hazard ratio, 0.33; 95% CI, 0.03 to 3.16). However, the wide CIs for both feeder types indicate variability.
Picnic table trial
On day 1 of the study, 4 fecal piles per table (1 per quadrant; n = 12) were designated for tracking the persistence of Salmonella. Of these, 4 (33% [4/12]) were culture positive for Salmonella on day 1. Two of these piles remained culture positive for Salmonella until day 4 (Figure 4). After pressure washing, 5 of 12 (41.7% [5/12]) were culture positive on day 1; of these, 1 pile was positive on day 2 and another on day 4.
A—Persistence of Salmonella in persistence piles that were positive on day 1 and a subsequent sampling day. Black dots are positive, and white dots are negative. There were 4 tables that had persistence beyond the first day of Salmonella detection. DP = Park name. Q# = Quadrant number. T# = Table number. B—Proportion of Salmonella-positive quadrants per table per day.
Citation: American Journal of Veterinary Research 2025; 10.2460/ajvr.24.12.0397
Of the 96 pooled samples collected over 8 days to determine prevalence on the picnic tables, 26 (27% [26/96]) were culture positive for Salmonella. Over the course of the study, Salmonella was isolated at least once from each of the tables, and each day of the total 8-day study had at least 1 detection between the 3 tables (Figure 4), except for day 3 of the second set of persistence piles, from which no Salmonella was recovered.
Serotyping
A total of 13 to 14 serotypes were detected (Table 2). Nine samples contained isolates that could have been 1 of 2 serotypes, Brandenburg and Sandiego, because they could not be differentiated based on our methods used (Table 2). The most common serotypes detected included Newport (22.3% [15/67] isolates), Brandenburg or Sandiego (13.4% [9/67]), Johannesburg (13.4% [9/67]), Weltrevreden (5.9% [4/67]), and Paratypi B (5.9% [4/67]). The remaining 9 serotypes represented 3 or fewer isolates. A total of 10 isolates could not be typed (14.9% [10/67]), and we suspect that some of these belong to other Salmonella subspecies than enterica.
Serotypes detected from the picnic table experiment and the percentage that each serotype is associated with human infections from 2018 to 2022.
| Serotype | No. detected (%) | Percent of human infections (2018–2022) |
|---|---|---|
| Newporta,b | 15 (22.3) | 9.3%c |
| Brandenburg or Sandiegoa | 9 (13.4) | 0.12%; 0.4% |
| Johannesburgb | 9 (13.4) | 0.06% |
| Weltrevredenb | 4 (5.9) | 0.21% |
| Paratypi Bb | 4 (5.9) | 0.14% |
| Agonab | 3 (4.5) | 0.63%c |
| Muenchena,b | 3 (4.5) | 1.78%c |
| Litchfieldb | 2 (2.9) | 0.29% |
| Braenderupb | 2 (2.9) | 1.74%c |
| Rubislawb | 2 (2.9) | 0.33% |
| Anatumb | 1 (1.5) | 0.5% |
| Hartfordb | 1 (1.5) | 0.44% |
| Oranienburgb | 1 (1.5) | 1.82%c |
| Ugandab | 1 (1.5) | 0.35% |
| Untypable | 10 (14.9) |
Discussion
As human cases of salmonellosis that are not associated with food increase throughout the US, the environments that individuals encounter on a regular basis need to be evaluated to better understand microbial transmission.4 We investigated Salmonella persistence to better inform public health agencies and mitigate seasonal outbreaks or sporadic cases in humans and wildlife. These 2 studies confirmed that Salmonella can persist for at least 4 days on surfaces frequently contacted by people (ie, bird feeders and picnic tables) and represent a potential risk for transmission to people or other animals. Our data contradict the findings of 2 previous studies41,42 on bird feeders in Canada and Poland where no Salmonella was isolated from feeders or feed. Yet, differences in isolation methods, ambient temperature (ambient temperatures are colder in both Canada and Poland compared to Georgia), humidity, and feeder types (Poland used wooden feeders only) may explain these differences. Also, Prescott et al41 noted that because volunteers were more aware of hygiene due to the study, they may have cleaned feeders more often than usual, decreasing the probability of Salmonella detection.
Our feeder trial investigated the persistence of Salmonella on feeders made of 2 common materials (plastic and wood) and if application of a novel antimicrobial coating would minimize transmission risk. Although prevalence and persistence were not significantly different between feeder types, Salmonella was primarily reisolated from plastic feeders and only a single sample from a wood feeder was positive (DPI 5). The lower detection from wood feeders may be explained by increased water absorption by the wood, which would more rapidly dehydrate the fecal inoculum.43 In fact, prior research suggested that Salmonella persistence improves with higher moisture levels, for example, up to 21 days in soil and 15 days in septic system effluent, from leach fields. The 1 wood feeder was only positive on DPI 5 and that detection was preceded by a large rain event the evening before sampling which wet all of the feeders. Salmonella is also more likely to be detected in fresh avian feces,44,45 presumably because of moisture. The wooden feeders in the current study were made of cedar (Cedar atlantica), which may contain natural antimicrobial secondary compounds, but more research would be needed to understand if and how it limits microbial persistence. In contrast to our hypothesis, the antimicrobial coating did not lower the prevalence or persistence of Salmonella. While this finding was surprising, this coating was developed for, and tested against aerosolized bacterial contamination (eg, through sneezing, coughing, etc),33 rather than against a matrix rich in organic material, like the fecal inoculum contained used in this study, which could have prevented full contact between feces and the antimicrobial coating.
Furthermore, our experiment involved a single inoculum of feces, whereas, in natural conditions, several inoculums of varying quantities of Salmonella may be deposited daily. Because bird feeders act as a source of food, they are utilized by a diversity of bird species and allow for frequent contact among birds. Bird feeder use is highly variable among individuals, but some may visit feeders several hundred times a day and reencounter rates are high.46,47 This provides numerous opportunities for birds to both contaminate bird feeders and, in turn, be exposed to pathogens from other birds. Data from experimental trials and surveillance of naturally infected birds show that large numbers of Salmonella can be shed by individual birds. For example, house sparrows (Passer domesticus), rock dove (Columba livia), cattle egret (Bubulcus ibis), herring gulls (Larus argentatus), and wild geese (species not given) may shed from 1.5 X 104 and 2 X 109 CFU daily.48–52 The infectious dose (minimum number of Salmonella needed to establish an infection) is highly variable among bird species and individuals, but experimental inoculation of house sparrows with 102 CFU resulted in infection and shedding and exposure to 108 CFU resulted in shedding and death within 8 days.49 Sick birds shed higher numbers of Salmonella, and they are also more likely to revisit bird feeders, further contaminating surfaces.49 Thus, we consider feeders to present a significant risk factor for Salmonella transmission between birds and humans who may handle contaminated feeders.
Similar to the feeder experiment, Salmonella persisted for at least 4 days on picnic tables in South Florida. The tables and benches were made of painted wood. The painted surface may facilitate the sample remaining moist, making it more similar to plastic bird feeders. Importantly, we detected Salmonella nearly every day that tables were sampled, likely because new fecal piles were naturally deposited on picnic tables each day. Our observations of bird and human behavior in that park, and in other urban parks in general, is that there is considerable risk of exposure. People generally avoid placing food or personal items directly on fresh fecal piles; however, they do not always avoid older/dry feces, and regardless, ibis were frequently observed walking through fecal piles and spreading fecal material across the table, which would be much less noticeable to people. The prevalence of Salmonella initially detected on the picnic tables (33% to 42%) and pooled swabs from tables (27%) was generally consistent with previous studies4,32 of white ibis in Palm Beach County, where prevalence ranged between 13% and 27% among adult and subadult ibis depending on site characteristics, with higher prevalences associated with urban areas.
A high diversity of Salmonella serotypes was detected during the picnic table experiment. Many of these serotypes (8/14 [57%]) were previously detected in white ibis from the same county in Florida.4 Although we did not determine pulsed-field gel electrophoresis types in this study, 44% of the pulsed-field gel electrophoresis strain types shed by white ibis in South Florida in a previous study4 matched human strains in the CDC PulseNet USA database. Similarly, in Australia, a case-matched study53 on human cases of salmonellosis showed that cases had high rates of ibis contact compared with matched controls. We detected 6 serotypes that had not been previously reported in ibis (ie, Johannesburg, Weltrevreden, Paratypi B, Agona, Oranienburg, and Uganda); however, because this study was based on environmental samples, feces, and/or Salmonella that were present on the picnic tables could represent other sources (eg, flies or other invertebrates). To the trained eye, ibis feces are readily distinguishable from other avian species and ibis are the bird most frequently seen on top of the tables, but we cannot be 100% certain that other species such as boat-tailed grackles (Quiscalus major), ducks, and green iguanas (Iguana iguana), all of which are common in this urban park, did not walk on the tables. Many of the serovars detected in this study are important causes of human disease.54 Four of the serovars previously detected in white ibis, and also detected in this study, are in the top 10 for human infections, accounting for 14.6% of human infections from 2018 to 2022. Overall, 5 of the serovars detected in the current study are in the top 20 for human infections (15.3% of infections). Newport was 1 of the most common serovars we detected (22%), and it is the second leading serovar associated with human illness.54
These results show that environmental surfaces can become contaminated with Salmonella after exposure to bird feces and that it can persist for at least 4 days providing a potential window for heightened risk. Both experiments also link resource provisioning (feeding) of wildlife to the transmission of Salmonella, not just at the moment of feeding and by the people doing the feeding, but in subsequent days and to other bird feeder handlers or park visitors, as well as pets and other wildlife. Feeders and feeding sites can become foci that facilitate pathogen transmission, and future studies should determine if pets and other nontarget wildlife (eg, outdoor cats, squirrels, and other urban park birds) are exposed to and infected with Salmonella at these sites. These results reinforce that feeder hygiene is important to mitigate the transmission of Salmonella among birds, other wildlife, and humans. Cleaning recommendations often vary depending on the source. At a minimum, cleaning feeders with warm soapy water to remove organic debris can help reduce fecal contamination, but ideally, removal of excess debris from feeders every 2 weeks, followed by fully submerging feeders in a 10% bleach solution for 10 minutes will significantly reduce Salmonella levels on feeders.55 Feeders should be thoroughly rinsed and dried before being used again. Placing feeders in areas with full sunlight exposure will help keep them dry, which would be a more hostile environment for Salmonella. Park management authorities should consider regular pressure washing of picnic tables with disinfectant solutions. In addition, public education and enforcement regarding feeding birds would decrease habituating birds to human food and prevent birds from coming close to areas being used by people. In summary, as humans seek connections with wildlife through activities like bird feeding and wildlife interactions increase due to urbanization, it is important to take precautions to avoid pathogen transmission through indirect interactions with anthropogenic environments. We suspect that indirect transmission of Salmonella through environmental sources is common yet underestimated.
Acknowledgments
We thank Suzzanne Tate for access to the Whitehall Experimental Forest shade house. Members of the Lipp Lab provided laboratory support and assistance throughout the project, and Ashley Phillips provided help with preparing the Salmonella inoculation.
Disclosures
The authors have nothing to disclose. No AI-assisted technologies were used in the composition of this manuscript.
Funding
Funding for this project was primarily from the National Science Foundation (EEID 1518611). Additional support was provided by the wildlife management agencies of the Southeastern Cooperative Wildlife Disease Study member states through the Federal Aid to Wildlife Restoration Act (50 Stat. 917) and by a US Department of the Interior Cooperative Agreement.
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