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Alaria Infection in Companion Animals in North Central Oklahoma from 2006 Through 2015 and Detection in Wildlife

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Alaria Infection in Companion Animals in North Central Oklahoma from 2006 Through 2015 and Detection in Wildlife Small Animals Prevalence of Alaria infection in companion animals in north central Oklahoma from 2006 through 2015 and detection in wildlife Eileen M. Johnson DVM, PhD OBJECTIVE To determine the prevalence of Alaria infection in cats and dogs in north Yoko Nagamori DVM central Oklahoma over various periods and investigate whether wild animal Rebecca A. Duncan-Decocq MS species in this region were also infected. Patrick N. Whitley DESIGN Akhilesh Ramachandran BVSC&AH, PhD Combined cross-sectional study and case series. Mason V. Reichard PhD SAMPLE From the Department of Veterinary Pathobiology, Results of parasitological testing of fecal samples from 5,417 client-owned Center for Veterinary Health Sciences, Oklahoma dogs and 1,246 client-owned cats (2006 through 2014); fecal samples from State University, Stillwater, OK 74078 (Johnson, Naga- 837 shelter or rescue dogs and 331 shelter or rescue cats (2013 and 2014) mori, Duncan-Decocq, Ramachandran, Reichard); and and 268 feral cats (2015); tongue or jowl samples from cadavers of 43 wild the USDA APHIS Wildlife Service, 2800 N Lincoln Blvd, Oklahoma City, OK 73105 (Whitley). pigs, 3 opossums, and 1 raccoon; and intestinal tract segments from cadav- ers of 48 cats and 5 coyotes. Address correspondence to Dr. Johnson (eileen.johnson@ okstate.edu). PROCEDURES Various parasite recovery techniques were performed to detect various Alaria stages in samples. Recovered adult trematodes and mesocercariae were used for PCR assay and sequencing of the 28S rRNA gene. RESULTS Prevalence of Alaria infection was significantly higher in feral cats (9.0%) than in shelter or rescue cats (0.6%) and client-owned cats (1.4%) and in shelter or rescue dogs (1.8%) than in client-owned dogs (0.2%). Mesocer- cariae were recovered from tissue samples from 11 (26%) wild pigs and 1 opossum. Amplicon sequences from adult trematodes and mesocercariae were 100% identical to each other and 99% homologous to GenBank se- quences of Alaria alata and Alaria mustelae. CONCLUSIONS AND CLINICAL RELEVANCE Prevalence of Alaria infection in the study area has increased in dogs and cats since 1990, when infections were rare. Prevalence in wild pigs was similar to that in Eurasia, where A alata is considered an emerging zoonotic parasite. (J Am Vet Med Assoc 2017;250:881–886) iplostomatid trematodes in the genus Alaria Alaria arisaemoides, Alaria intermedia, Alaria Dhave a worldwide distribution. Domestic and taxidae, and Alaria marcianae.6 wild carnivores are the definitive hosts.1–6 Adult trem- In reported cases of human alariosis in North atodes in the small intestine pass eggs in the feces, America, Alaria infection was acquired through and the eggs embryonate and hatch in fresh water. consumption of improperly cooked game meat.9,10 Newly hatched miracidiae penetrate susceptible spe- The only Alaria sp recorded to date in Europe is cies of fresh water snails (eg, Helistoma, Planorbis, A alata.1,6,13,14 Although not definitively associated Lymnea, and Anisus spp) that support asexual devel- with human disease, A alata has been experimen- opment of miracidiae into sporocysts and furcocer- tally transmitted to a rhesus monkey.11,13 Over the cous cercariae.1,2,6,7 Cercariae penetrate the skin of past decade during mandatory testing of wild pigs tadpoles or frogs and become mesocercariae.1,2,8 Vari- (Sus scrofa scrofa) for Trichinella spp in the Euro- ous species of birds, reptiles, and mammals (includ- pean Union, A alata mesocercariae have been dis- ing humans) that ingest the infected frogs can serve covered in wild pig tissues, primarily in muscle fas- as collector (paratenic) hosts.1,2,6,9–13 cia and adipose tissue.1,6,14–19 Carnivores become infected when they ingest in- In Europe, alariosis had been classified as a low-risk fected frogs or paratenic hosts or through transmam- zoonosis.1,6,13,14 However, with expansion of wild pig pop- mary transmission.1–6 The mesocercariae migrate ulations, an increase in the prevalence of mesocercariae to the lungs and encyst as metacercariae that are in wild pigs, an increase in human consumption of coughed up and swallowed. Recognized Alaria spp meat from wild pigs, changes in cooking methods, include Alaria alata, Alaria mustelae, Alaria canis, and recognition of severe and fatal disease in hu- JAVMA • Vol 250 • No. 8 • April 15, 2017 881 Small Animals mans, A alata is now considered an emerging threat feral cats as part of the teaching hospital’s neuter-and- to human health.1,6,14–20 release program, Operation Catnip, in 2015 were also Surveillance of Trichinella spp in the United States included in the prospective portion of the study. is not mandatory and does not include wild pig popu- Forty-six cadavers of shelter cats, 1 stray cat, and lations.21 Control has been achieved in domesticated 1 client-owned cat submitted to the Oklahoma Animal pigs (Sus scrofa domesticus) through enforcement of Disease Diagnostic Laboratory for disposal between laws that prevent feeding of raw garbage and through March and July 2015 and 5 cadavers of coyotes that had improvements in biosecurity and hygiene in confine- recently been hit by cars and submitted to the same ment-type swine production units. Serologic testing laboratory between September 10, 2014, and March 5, (ELISA) is used in swine production herds to deter- 2015, were included in the study. Also included were mine Trichinella status. No information is available on tongues or jowl tissues collected from 43 wild pigs the role of wild pigs as a source of human infection through the cooperation of the USDA APHIS Wildlife with Alaria mesocercariae in the United States. Service during routine hunting and disease surveil- Efforts to control expanding wild pig populations lance in 6 Oklahoma counties (Jefferson, Love, Osage, in the United States through regulated hunting and Pawnee, Pittsburg, and Tillman) between February 23 trapping have been unsuccessful.22,23 This population and May 12, 2015, as well as tongue and jowl tissues expansion is believed to be due to periodic release of from 1 raccoon and 3 opossums that had been recently wild pigs from Eurasia into different areas of the Unit- hit by cars. Tissues were shipped on ice overnight to ed States for hunting and the escape of domesticated the Oklahoma Animal Disease Diagnostic Laboratory pigs that subsequently interbreed with these released for evaluation. wild pigs.22,23 Adaptability of wild pigs is related to their omnivorous feeding habits, high reproductive potential, Parasitological evaluation intelligence, and reclusive nature. They are considered of fecal samples large game and are used for hunting purposes and hu- Historical laboratory results for fecal samples man consumption in many parts of the world.20,24 from owned cats and dogs were reviewed retro- Studies1,6,13,18,25 in Europe have revealed a high spectively for findings of Alaria ova. All other fecal prevalence of A alata infection in red fox and wolf samples were prospectively evaluated specifically populations, which are also believed to be expanding. for the study. For all fecal samples, including those In North America, most reports4,5,26–32 of Alaria infec- represented in the retrospective portion of the study, tions in domesticated and wild carnivores pertain to a centrifugal fecal flotation technique with Sheath- Canada, the northern United States, and Florida. In a er sucrose or 33% zinc sulfate solution was used to study33 of endoparasitism in client-owned dogs con- evaluate samples for evidence of parasites.34 Slides ducted in north central Oklahoma from 1981 through prepared in this manner were examined at 100X and 1990, no Alaria ova were detected in 12,515 fecal sam- 400X magnification with a binocular microscope. ples. The purpose of the study reported here was to obtain an updated estimate of the prevalence of Alaria Parasitological evaluation of cadavers infection in various dog and cat populations and to de- Cadavers were processed and examined for gastro- termine whether infection existed in wildlife reservoir intestinal parasites by use of the following technique. hosts, primarily wild pigs, in north central Oklahoma. Intestinal tracts were removed. Segments (stomach, small intestine, and colon) were separated and placed Materials and Methods into individual buckets. Each segment was opened into a bucket and washed with running tap water. Washed Animals and samples intestinal contents were allowed to sit undisturbed for This study involved a retrospective and a prospec- 15 to 30 minutes, and the supernatant was carefully tive portion. For the retrospective portion, all results decanted. This procedure was repeated until the su- of parasitological examination of fecal samples from pernatant fluid appeared clear. Portions of sediment client-owned dogs and cats submitted to the Boren from each segment were transferred to clear glass pie Veterinary Medical Hospital of Oklahoma State Uni- plates, and grossly detectable parasites were removed versity or the Oklahoma Animal Disease Diagnostic and stored in jars containing 70% ethanol at 4°C. The Laboratory from 2006 through 2014 were included. sediment was then examined in 95 X 15-mm disposable In the prospective portion approved by the Insti- polystyrene Petri dishes with a dissecting microscope tutional Animal Care and Use Committee of Oklahoma (0.8X to 5.6X objective lenses) until all of the sediment State University, fecal samples were collected from from each segment had been examined and all para- shelter or rescue dogs and cats for 2 years (2013 and sites recovered. Trematode parasites from the intestinal 2014) through a newly implemented spay-neuter pro- tracts were identified by use of a taxonomic key.35 gram of the Boren Veterinary Medical Hospital. Dur- ing this 2-year period, additional fecal samples from Parasitological evaluation rescue cats were provided by 2 private feline practi- of tissue samples tioners located within 50 miles of the study area of Individual tissue samples were evaluated with Stillwater, Okla.
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