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Strix Varia) from the Eastern United States T ⁎ Kevin D Veterinary Parasitology: Regional Studies and Reports 16 (2019) 100281 Contents lists available at ScienceDirect Veterinary Parasitology: Regional Studies and Reports journal homepage: www.elsevier.com/locate/vprsr Original Article Trichomonosis due to Trichomonas gallinae infection in barn owls (Tyto alba) and barred owls (Strix varia) from the eastern United States T ⁎ Kevin D. Niedringhausa, ,1, Holly J. Burchfielda,2, Elizabeth J. Elsmoa,3, Christopher A. Clevelanda,b, Heather Fentona,4, Barbara C. Shocka,5, Charlie Muisec, Justin D. Browna,6, Brandon Munka,7, Angela Ellisd, Richard J. Halle, Michael J. Yabsleya,b a Southeastern Cooperative Wildlife Disease Study, 589 D.W. Brooks Drive, Wildlife Health Building, College of Veterinary Medicine, The University of Georgia, Athens, GA 30602, USA b Warnell School of Forestry and Natural Resources, 180 E Green Street, University of Georgia, Athens, GA 30602, USA c Georgia Bird Study Group, Barnesville, GA 30204, USA d Antech Diagnostics, 1111 Marcus Ave., Suite M28, Bldg 5B, Lake Success, NY 11042, USA e Odum School of Ecology and Department of Infectious Diseases, College of Veterinary Medicine, University of Georgia, Athens, GA 30602, USA ARTICLE INFO ABSTRACT Keywords: Trichomonosis is an important cause of mortality in multiple avian species; however, there have been relatively Owl few reports of this disease in owls. Two barn owls (Tyto alba) and four barred owls (Strix varia) submitted for Strix varia diagnostic examination had lesions consistent with trichomonosis including caseous necrosis and inflammation Tyto alba in the oropharynx. Microscopically, these lesions were often associated with trichomonads and molecular Trichomonosis testing, if obtainable, confirmed the presence of Trichomonas gallinae, the species most commonly associated Trichomonas gallinae with trichomonosis in birds. The T. gallinae genotype in one barn owl and two barred owls was identified as ITS- OBT-Tg-1 by sequence analysis. Columbids are the primary hosts for T. gallinae, and columbid remains found within the nest box of the barn owls were the likely source of infection. This study is the first to formally describe the strains and genetic variation of T. gallinae samples from clinical cases of trichomonosis in barn and barred owls in the eastern USA. 1. Introduction (oropharynx and crop) (Amin et al., 2014). Mortality in affected birds are typically the result of starvation from reduced ability to forage, Trichomonosis is a potentially severe disease of multiple avian respiratory failure from lesions obstructing the trachea, sepsis due to species, particularly doves and pigeons as well as predatory birds that secondary infections, or visceral organ failure following disseminated may feed on infected prey. The causative agents are flagellated pro- infection (Kocan and Herman, 1971; Narcisi et al., 1991). The parasite tozoa within the genus Trichomonas (Family Trichomonadidae), most can cause significant effects at the population level, particularly when commonly Trichomonas gallinae (Rivolta, 1878) (Forrester and Foster, introduced into naïve populations. For example, the introduction of T. 2009). The disease is characterized by severe inflammation and ne- gallinae to Mauritius is considered a major threat to the endangered crosis of multiple tissues, primarily the upper gastrointestinal tract pink pigeon (Columba mayeri)(Bunbury et al., 2008). Additionally, T. ⁎ Corresponding author. E-mail addresses: [email protected] (K.D. Niedringhaus), [email protected] (E.J. Elsmo), [email protected] (H. Fenton), [email protected] (B.C. Shock), [email protected] (J.D. Brown), [email protected] (B. Munk), [email protected] (A. Ellis), [email protected] (R.J. Hall), [email protected] (M.J. Yabsley). 1 Present Address: Southeastern Cooperative Wildlife Disease Study, 589 D.W. Brooks Drive, Wildlife Health Building, College of Veterinary Medicine, The University of Georgia, Athens GA 30602. 2 Present Address: For Pet’s Sake- The Avian and Exotic Animal Hospital of Atlanta, 3761 N Druid Hills Rd, Decatur, GA 30033, USA. 3 Present Address: Wisconsin Veterinary Diagnostic Laboratory, University of Wisconsin-Madison, 445 Easterday Lane, Madison WI 53706, USA. 4 Present address: Government of the Northwest Territories, 5th Floor, Scotia Centre, P. O. Box 1320, Yellowknife, NT, X1A 2L9, Canada. 5 Present Address: Department of Biology, Lincoln Memorial University, Harrogate, TN, 37752, USA. 6 Present Address: Pennsylvania Game Commission, Animal Diagnostic Laboratory, University Park, PA 16802, USA. 7 Present Address: California Department of Fish and Wildlife, Wildlife Investigations Laboratory, 1701 Nimbus Road, Suite D, Rancho Cordova, CA 95670, USA. https://doi.org/10.1016/j.vprsr.2019.100281 Received 11 December 2018; Received in revised form 26 February 2019; Accepted 4 March 2019 Available online 07 March 2019 2405-9390/ © 2019 Elsevier B.V. All rights reserved. K.D. Niedringhaus, et al. Veterinary Parasitology: Regional Studies and Reports 16 (2019) 100281 gallinae-associated disease was implicated as a potential cause of de- clining greenfinch (Carduelis chloris) and chaffinch (Fringilla coelebs) populations in the British Isles (Lawson et al., 2012). It is speculated that the most common mechanisms of transmission are via contact with infected food material, water, or saliva, which is supported by the ability of trichomonads to persist in these environments (Amin et al., 2014; Purple et al., 2015; McBurney et al., 2017). N/A ITS sequence: genbank N/A JN007005 JN007005 ITS-OBT-Tg-1: KC215387 ITS-OBT-Tg-1: KC215387 Birds in the Order Columbiformes are the primary hosts, and many species in this order are considered to have widespread subclinical in- fections (Amin et al., 2014). Other hosts, including species in the Orders Passeriformes and Falconiformes, may subclinically harbor the pa- thogen, but sporadic cases of overt disease in these hosts can occur (Cooper and Petty, 1988; Boal et al., 1998; Anderson et al., 2009; Dudek et al., 2018). Numerous cases of Trichomonas infections have been reported in raptors, but are relatively uncommon in owls. How- ever, the disease is less-studied in owls compared to other raptor species (Forrester and Foster, 2009). Infection has been reported in at least nine species of owls within the genera Bubo, Tyto, Otus, Megascops, Strix, and Athene (Forrester and Foster, 2009). Clinical disease has been docu- mented in barred owls (Strix varia), great horned owls (Bubo virgi- nianus), spotted owls (Strix occidentalis), and barn owls (Tyto alba) in the USA, and trichomonosis is considered a major cause of mortality in barn owls in the state of Hawai'i (Jessup, 1980; Pokras et al., 1993; Work and ltrates fi Hale, 1996; Rogers et al., 2016). Molecular characterization of parasites Granulomatous stomatitis with bacteria Main microscopic lesions Heterophilic stomatitis with bacteria and trichomonads ITS-OBT-Tg-1: Fibrinous stomatitis and perivascularin lymphoplasmacytic from owls from the USA is limited to one study on the relatedness of trichomonads from spotted owls and band-tailed pigeons (Patagioenas uid in fasciata monilis) in California (Rogers et al., 2016). fl genotype detected. Trichomonas gallinae is cosmopolitan, largely due to the wide geo- graphical range of its primary host, the rock dove (Columba livia) (Stabler, 1947). However, multiple genetically distinct strains and subtypes of T. gallinae circulate within many avian species across the Trichomonas globe (Gerhold et al., 2008; McBurney et al., 2015; Martínez-Herrero et al., 2017). Within the last ten years, numerous studies have examined the genetic variation in Trichomonas strains from a wide variety of hosts, which has led to the detection of many strains or lineages of T. gallinae as well as several novel Trichomonas species, some of which have been formally described and can cause clinical disease (e.g., Tri- chomonas stableri and Trichomonas gypaetinii)(Anderson et al., 2009; lled with yellow-white debris obstructing pharynx Heterophilic stomatitis with trichomonads fi Girard et al., 2014; Martínez-Díaz et al., 2015). Avian Trichomonas species and strains can occur subclinically or in association with dis- ease, and individual animals can be co-infected with multiple strains uid Oropharyx Tan mass on the palate extending to esophagus Multiple friable plaques on caudal palate and sublingual mucosaFriable plaque Heterophilic on stomatitis dorsal with palate, bacteria nasal sinuses and contained trichomonads opaque Oropharyngeal mass extending into maxilla, opaque air sacs ITS-OBT-Tg-1: Heterophilic stomatitis with trichomonads fl Caseous plaque surrounding glottisnasal and sinuses choanae, gray (Grabensteiner et al., 2010; Kelly-Clark et al., 2013; Girard et al., 2014). Due to the increasingly complex genetic variability in both patho- genic and commensal trichomonads in avian species, characterizing the genetic variability of trichomonads in uncommon avian hosts is im- portant to improve our understanding of the epizootiology of this pa- thogen (Martínez-Herrero et al., 2017). We conducted a review of tri- chomonosis cases diagnosed in owls submitted to the Southeastern Nutritional condition Main gross lesions Good Cooperative Wildlife Disease Study (SCWDS, University of Georgia, Athens, GA, USA). We also present the case details and the first genetic characterization of T. gallinae samples from barn owls (Tyto alba) and barred owls (Strix varia) from the southeastern and midwestern United States.
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