Current status and future recommendations for feral swine disease surveillance in the United States

Abstract

USDA APHIS Wildlife Services (WS) responded to the threat of feral swine as a pathogen reservoir as early as 2004. To increase awareness and knowledge on that risk, WS began opportunistic sampling of animals harvested by its operational component to curtail swine damage to agriculture and property. Initially, pseudorabies and swine brucellosis were of most concern, as both serve as a potential threat to the domestic swine industry and the latter also possesses zoonotic implications. In 2006, classical swine fever, a foreign animal disease, became the main driver for feral swine pathogen surveillance. Subsequent years of surveillance identified numerous other disease risks inherent within populations of feral swine. Presently, feral swine surveillance falls under the purview of the APHIS National Feral Swine Damage Management Program, which began in 2014. In January 2018, a panel of animal disease experts representing industry, government, and academia were invited to Fort Collins, Colorado to discuss successes of this surveillance, identify any shortcomings or needs, and propose future feral swine surveillance. This manuscript serves to synthesize WS’ surveillance and the future direction of these efforts.

MEETING PARTICIPANTS

Dr. Angela Arenas, Texas A&M University; Dr. Angela Bosco-Lauth, Colorado State University; Dr. Richard Bowen, Colorado State University; Dr. Vienna Brown, Colorado State University; Dr. Fred Cunningham, Wildlife Services, National Wildlife Research Center Mississippi Field Station; Dr. Peter Fernandez, USDA APHIS International Services (retired); Dr. Tom Gidlewski, USDA APHIS Wildlife Services; Dr. Tom Kasari, USDA APHIS Veterinary Services; Dr. James LaCour, Louisiana State Wildlife Veterinarian; Dr. Tom Ray, USDA APHIS Veterinary Services; Dr. Kent Schwartz, Iowa State University, Veterinary Diagnostic Laboratory; Dr. Harry Snelson, American Association of Swine Veterinarians; Dr. Paul Sundberg, Swine Health Information Center; Dr. Patrick Webb, National Pork Board; Dr. Pam Zaabel, Iowa State University, Center for Food Security and Public Health.

INTRODUCTION

Nearly 6 million feral swine (Sus scrofa), which include released and escaped domestic swine as well as wild Eurasian boars and their hybrids, roam in at least 35 U.S. states (Goedbloed et al. 2013). Feral swine are highly invasive causing damage and destruction to agricultural products, riparian areas, and native flora and fauna (Seward et al. 2004; Bevins et al. 2014). In recent years, high fecundity, adaptable biology, flexible and opportunistic diet, and capacity to thrive in a number of different landscapes have allowed the range of feral swine to expand (Bevins et al. 2014; Baroch et al. 2015). Anthropogenic factors such as translocation to create local hunting opportunities and baiting have also facilitated dispersion and high densities, respectively.

Feral swine can transmit multiple pathogens significant for domestic livestock, humans, and companion animals (Hutton et al. 2006; Meng et al. 2009; Miller et al. 2017). They are a highly gregarious species and, not surprisingly, GPS data have shown interaction between backyard domestic swine and their feral counterparts (Wyckoff et al. 2009). Additionally, feral swine hunting has become a popular activity, especially in the southeastern United States, and dressing harvested animals and consuming feral swine pork provides a platform for human exposure to additional zoonoses (Ruiz-Fons, 2017). In light of the concern for animal agriculture and public health, experts from industry, academia, and government met for 2 days in Fort Collins, CO, herein referred to as the Feral Swine Workshop, to discuss current and future directions of feral swine disease surveillance as conducted through the guidance of the APHIS National Feral Swine Damage Management Program. This manuscript summarizes the workshop.

CURRENT FERAL SWINE DISEASE SURVEILLANCE ACTIVITIES

Historically, porcine reproductive and respiratory syndrome (PRRS), avian influenza (AI), classical swine fever (CSF), swine brucellosis (SB), and pseudorabies (PRV) were identified as the diseases for which to survey feral swine. Subsequently, surveillance for PRRS and AI was discontinued as priorities changed and the current disease surveillance program includes only CSF, SB, and PRV.

Classical swine fever is a foreign animal disease (FAD) and current surveillance in both commercial and feral swine serves to reassure trade partners that the United States is CSF free. Both SB and PRV have been eradicated from U.S. commercial swine operations (Center for Food Security and Public Health, 2017; Merck Veterinary Manual, 2018); however, as they are endemic diseases in feral swine populations, and there is frequent and regular spill-over of both diseases into outdoor-raised swine production systems, monitoring of feral swine for SB and PRV continues to be important to the swine industry as well as other livestock entities. Additionally, SB is a zoonotic disease which can cause severe illness in humans (Starnes et al. 2004; Carrington et al. 2012; Simoes and Justino, 2013; Franco-Paredes et al. 2017). APHIS Wildlife Services (WS) routinely culls feral swine for damage management purposes to protect agriculture, livestock, and other man-made or natural resources. Serum is collected from at least 2,800 animals annually for serologic tests on these three diseases. Sampling is distributed over space and time and is undertaken in much of the United States with counties being ranked as high, medium, or low priority based upon criteria including (i) existing feral swine populations, (ii) domestic hog production, and (iii) presence of landfills (Targeted Antibody Surveillance for National Diseases of Concern in Feral Swine in the United States, 2016).

Testing for CSF occurs in series using three tests to confirm a positive result. First, an ELISA is used. If the ELISA is negative, testing is complete for the sample. If the ELISA is positive, the sample is tested using an immunoperoxidase test. If this second test is negative, the sample is considered negative; however, a positive sample results in a third test, virus neutralization. This testing occurs at the Foreign Animal Disease Diagnostic Laboratory in Plum Island, New York. To date, no positives for CSF have been identified in samples from feral swine. Swine brucellosis diagnostics occur at the Kentucky Federal Brucellosis Laboratory and the fluorescence polarization assay is used. The average apparent seroprevalence for SB of the animals tested in the United States between fiscal years 2013 and 2017 was 7.3%, ranging between 4.6% and 10.3%. The Kentucky Federal Brucellosis Laboratory tests samples for PRV using the glycoprotein B ELISA. The average apparent seroprevalence of animals tested for PRV in the United States between fiscal years 2013 and 2017 was 18.7%, ranging between 17.8% and 20.2%. These prevalence values were derived from WS’ databases and used for internal reporting. Of note, there are no confirmatory assays being employed for SB or PRV.

DISCUSSION POINTS AND RECOMMENDATIONS FROM THE FERAL SWINE WORKSHOP

• Participants recommend serologic (antibody) surveillance for FADs; however, there was valid concern regarding the interpretation and implications of possible false-positive tests leading to unnecessary barriers to interstate and international trade.

• African swine fever (ASF) was of high concern for many participants. However, the lack of highly specific screening and confirmatory test(s) for ASF prevented a recommendation for any form of routine ASF surveillance. Improved diagnostic tests are necessary.

• The diseases included in the current feral swine disease surveillance program are CSF, SB, and PRV; all remain surveillance priorities. The pork industry’s position, however, is that routine surveillance for endemic diseases (SB and PRV) should not be at the cost of decreased funding for feral pig population control.

• Targeted, risk-based surveillance was appropriate to derive meaningful data and that continued engagement with appropriate partners would be highly beneficial in order to establish sample sizes and spatial targets. Also, improvements in several diagnostic tests are needed to allow valid and informative conclusions to be made (e.g., studies demonstrate that SB serology routinely underestimates the true disease prevalence).

• In addition to consideration of surveillance for CSF, SB, and PRV, there should be flexibility to conduct pilot, targeted surveillance studies on other diseases.

• Additional disease expertise to assist the National Feral Swine Damage Management Program would positively improve the program’s capacity to quickly respond to new disease threats from feral swine.

• Syndromic, but not serologic, surveillance for foot-and-mouth disease (FMD) is important as part of a national, comprehensive FMD surveillance program, and further hands-on training for field biologists would be beneficial.

• State-federal-industry collaboration on development of a response plan for disease outbreaks in feral swine, including a clear communication strategy for federal, industry, and state partners is needed.

CONCLUSION

Feral swine pose a significant health threat to domestic livestock and humans and their increasing home ranges, social behaviors, and opportunistic diet makes them a prime disease vector. The diseases included in the current feral swine disease surveillance program are all still high priority. The need for enhanced diagnostic capacities was noted for several diseases of importance (e.g., ASF and SB) and targeted, risk-based surveillance is essential to derive meaningful data. Based on this input, the feral swine program should work with APHIS partners and other cooperators to develop a surveillance strategy that is congruent with the recommendations provided.