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U.S. Department of Agriculture U.S. Government Publication Animal and Plant Health Inspection Service Wildlife Services Pedersen et al. BMC Veterinary Research (2018) 14:388 https://doi.org/10.1186/s12917-018-1718-3 CASEREPORT Open Access Pseudorabies detected in hunting dogs in Alabama and Arkansas after close contact with feral swine (Sus scrofa) Kerri Pedersen1* , Clinton T. Turnage2, Wesson D. Gaston3, Paulo Arruda4, Scott A. Alls5 and Thomas Gidlewski1 Abstract Background: Pigs (Sus scrofa) are the natural hosts of pseudorabies virus (PRV), also known as Aujeszky’s disease. Infection in mammals, with the exception of humans, typically causes extreme itching, facial swelling, and excessive salivation, followed by death in non-suid species. The risk to susceptible mammals was assumed to decrease when PRV was eliminated from U.S. commercial swine in 2004, though the virus remains endemic in feral swine. Infected feral swine pose a threat to the disease-free status of the commercial swine industry, and to other animals, including dogs, that come in direct or indirect contact with them. Since dogs are commonly used for hunting feral swine, they are at high risk of exposure. Case presentation: The following report describes the progression of pseudorabies infection in dogs in two states after exposure to feral swine. The first case occurred in a dog in Alabama after participation in a competitive wild hog rodeo. The second case occurred in multiple dogs in Arkansas after hunting feral swine, and subsequent consumption of the offal. The antibody prevalence of feral swine in the two states where the dogs were exposed is also examined. Conclusions: Dogs that are used for hunting feral swine are at high risk of exposure to pseudorabies because the disease is considered endemic in feral swine in the U.S. Keywords: Aujeszky’s disease, Dogs, Feral swine, Hunting, Pseudorabies, Sus scrofa,Wildpig Background endemic in feral swine, thus posing a threat to the Pseudorabies (PRV), also referred to as Aujeszky’s dis- industry’s disease-free status [5], and potentially causing ease, is a viral disease caused by Suid alphaherpesvirus 1 substantial economic losses [6]. Prior to elimination of [1]. Though swine (i.e., suids) are the only known reser- the disease in commercial swine, infection in dogs voirs or natural hosts of the disease, numerous mam- (Canis lupus familaris) was commonly reported [7–9]. mals, with the exception of humans, are susceptible to Even though PRV is prevalent in feral swine, most dog infection [2]. Adult swine usually recover after infection, owners, veterinarians, hunters, and wildlife biologists are but high mortality rates in piglets, and abortions in preg- unaware of the risk. Dogs become infected after direct nant sows are typical [3]. The virus can also establish la- or indirect contact with infected swine; infected dogs do tency in swine with reactivation occurring after natural not shed enough virus to transmit to other dogs [10]. In- stimuli, or as a result of stressors [2]. gestion is the most common route, but transmission can Feral swine (Sus scrofa) are an invasive species in the also occur via inhalation or minor wounds [1]. The dis- U.S. with a widespread geographic range extending ease is suspected when relentless itching (pruritus), ex- across the country [4]. Although PRV was eradicated cessive salivation, and sudden death are observed, from U.S. commercial swine in 2004, the disease is still especially when exposure to feral swine has occurred [7]. In some parts of the U.S., dogs are used for hunting * Correspondence: [email protected] feral swine. This typically involves dogs that are used to 1U.S. Department of Agriculture, Animal and Plant Health Inspection Service, bay (e.g., Catahoula, Black Mouth Cur, Rhodesian ridge- Wildlife Services, National Wildlife Research Center, 4101 LaPorte Avenue, Fort Collins, Colorado 80521, USA back) and then dogs used to catch (e.g., Pit bull, Ameri- Full list of author information is available at the end of the article can bulldog) the pig. However, some hunters only use © The Author(s). 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Pedersen et al. BMC Veterinary Research (2018) 14:388 Page 2 of 7 bay dogs. The bay dog tracks, follows, and locates a feral polymerase chain reaction (PCR) testing for PRV, and swine, whereas the catch dog holds the animal with its virus isolation [19, 20]. jaws until the hunter dispatches it. Depending on the A direct fluorescent antibody test was also con- temperament of the dog and the size of the feral swine, ducted on brain tissue for detection of rabies antigen the bay dog and the catch dog often come in direct con- [21]. Though no antigen was detected, rabies testing tact with the pig, especially once the catch dog seizes was considered inconclusive because the cerebellum the feral swine. As such, it is not surprising that dogs and brainstem, which are the preferred tissues for ra- can be exposed to various pathogens carried by feral bies testing, were unavailable because they had been swine, including PRV [11]. used for PRV testing. Histopathologic examination of Though PRV infection has been described in hunt- the liver and spleen did not reveal any significant le- ing dogs previously, these reports are limited. In the sions, but moderate lymphoplasmacytic encephalitis U.S., infection was described in three dogs after hunt- was detected in the brainstem. Virchow-Robin spaces ing feral swine in southern Oklahoma [12]. Two spe- were often infiltrated and expanded by low to moder- cific cases were reported in Florida in hunting dogs ate numbers of lymphocytes, plasma cells, and rare after direct contact with feral swine, and at least six macrophages (Fig. 1); multifocal areas of gliosis were other dogs displayed signs of infection after hunting also observed. Endothelial cells within affected vessels feralswineinthesameareaofFlorida[13]. In were moderately enlarged (hypertrophied). Occasion- addition, confirmed cases of PRV in dogs after direct ally neurons and astrocytes contained an intranuclear contact with wild boar have been reported in various eosinophilic inclusion that often peripheralized the countries including Belgium [14], Italy [15, 16], chromatin (Fig. 2). Tonsil was negative but brain tis- France [17], and Germany [18]. Our objective was to suetestedpositive(cyclethreshold(Ct)=30;value< report the disease progression of PRV in hunting dogs 40 considered positive) for PRV by PCR. Pseudorabies in two U.S. states after close contact with feral swine. virus was isolated from central nervous system tissue We also examined the antibody prevalence of PRV in in porcine kidney-15 cells, and confirmed by im- feral swine in those same states in order to further munofluorescence staining (Fig. 3). Based on the clin- elucidate the potential risk to dogs. ical presentation, histologic lesions, PCR results, and virus isolation, the dog was diagnosed with PRV. Case presentation Alabama Arkansas A 6-year old intact male Plott hound dog was pre- Two hunters (Hunters A and B) used nine mixed sented to a veterinarian on September 18, 2014 with breed dogs (six belonging to Hunter A, and three to severe self-induced facial trauma including unilateral periocular swelling, and intense pruritus. The dog had participated in a benefit wild hog rodeo in Wilcox County, Alabama from September 11–13, 2014. Dur- ing the course of the three-day spectator event that included dog, trapping, and stalk hunting categories, the dog was involved in the capture and removal of 13 feral swine. On September 19, 2014, the dog had further self-induced trauma, intense pruritus, ery- thema, and vomited blood. The animal was vocalizing and self-mutilation of the facial region resulted in se- vere and diffuse lacerations and bleeding. The attend- ing veterinarian administered morphine, but the clinical presentation including facial self-mutilation remained unaltered. By the next day (September 20th- Day 9 or 10), the dog was dead. Fresh and 10% formalin-fixed sections of cerebrum, cerebellum, brainstem, liver, spleen and tonsil from the dog were submitted to Iowa State University Veterinary Fig. 1 Virchow-Robin spaces expanded by low to moderate numbers Diagnostic Laboratory (ISUVDL) in Ames, Iowa for test- of lymphocytes, plasma cells, and rare macrophages. The sample was ing. Histopathologic examination was performed on all collected from the brain tissue of a hunting dog in Alabama formalin-fixed tissues. Fresh tissue sections of cerebrum, that developed symptoms compatible with pseudorabies virus after interacting with feral swine cerebellum, and brainstem were submitted for real-time Pedersen et al. BMC Veterinary Research (2018) 14:388 Page 3 of 7 However, the three dogs along with the hunter’s three other dogs (six total) reportedly consumed the offal once he finished butchering the animal at his house. On December 17, 2014 (Day 4), one of Hunter A’s dogs refused to eat, scratched its head profusely, and was whining and moaning. By Decem- ber 18, 2014 (Day 5), three of Hunter A’sdogshad swollen heads and appeared to have vomited prior to dying. Two more of Hunter A’s dogs had diarrhea. Two of Hunter B’sdogsweredeadandonewassick. On December 19, 2014 (Day 6), Hunter A had one dog that started vomiting, and another that was sali- vating excessively and then died a few hours later.

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