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First Molecular Confirmation of Equine Ocular Setaria Digitata in China

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First Molecular Confirmation of Equine Ocular Setaria Digitata in China veterinary sciences Case Report First Molecular Confirmation of Equine Ocular Setaria digitata in China Feng Yu 1,†, Bo Liu 1,†, Shulei Chen 1, Ziwen Yi 1, Xianyong Liu 2 , Yiping Zhu 1,* and Jing Li 1,* 1 Equine Clinical Diagnostic Center, College of Veterinary Medicine, China Agricultural University, No. 2 Yuanmingyuan West Road, Beijing 100093, China; [email protected] (F.Y.); [email protected] (B.L.); [email protected] (S.C.); [email protected] (Z.Y.) 2 Department of Veterinary Parasitology, College of Veterinary Medicine, China Agricultural University, Beijing 100193, China; [email protected] * Correspondence: [email protected] (Y.Z.); [email protected] (J.L.) † These authors contributed equally to this work. Abstract: A 5-year-old Mongolian mare (Equus caballus Linnaeus, 1758) was observed to have corneal opacity and excessive ocular discharge. An ophthalmic examination revealed a moving thread-like cylindrical worm in the anterior chamber of the right eye. The parasite was successfully removed surgically. The worm was observed under light microscopy and confirmed as Setaria digitata by 12S rRNA gene amplification and sequencing. Phylogenetic analysis demonstrated similarity with Setaria digitata in the National Center for Biotechnology Information (NCBI) GenBank database isolated from other Asian countries. This report is the first confirmed case of equine ocular setariasis by molecular diagnosis in China, which may indicate its presence in livestock and promote research on its epidemiology. Keywords: horses; ophthalmology; setariasis; molecular diagnosis; China Citation: Yu, F.; Liu, B.; Chen, S.; Yi, Z.; Liu, X.; Zhu, Y.; Li, J. First Molecular Confirmation of Equine Ocular Setaria digitata in China. Vet. 1. Introduction Sci. 2021, 8, 55. https://doi.org/ 10.3390/vetsci8040055 Setaria is a genus of roundworms (Nematoda: Filariodea), among which Setaria digitata is mainly found in Asia. Setaria digitata often affects cattle and buffalos, with common Academic Editor: predilection site in peritoneal cavity [1]. Within its natural hosts, these nematodes are non- Annamaria Passantino pathogenic in most cases. However, the parasite exhibits migratory behaviors in aberrant hosts including goats, sheep and horses [2]. The most common form of migration in infected Received: 23 February 2021 horses is ocular migration [3,4]. Infected goats and sheep can experience cerebrospinal Accepted: 26 March 2021 nematodiasis, which leads to lumbar paralysis and death [5]. Vectors of S. digitata include Published: 28 March 2021 biting insects like mosquitoes (genera Aedes, Culex, Anopheles, Hyrcanus and Armigeres)[6]. Setariosis poses a serious threat to susceptible animals in tropical areas. When mosquitoes Publisher’s Note: MDPI stays neutral feed on the blood of infected hosts, they become infected with microfilariae, which develop with regard to jurisdictional claims in into infective larvae (L3) inside the mosquitoes within 2 to 3 weeks. Infected mosquitoes published maps and institutional affil- transmit L3 to susceptible hosts during blood meals, after which it matures in the definitive iations. host within 8–10 months [7]. Equine ocular setariasis is caused by S. digitata, S. equina or S. marshalli, with most cases reported by countries in south and southeast Asia [8–11]. According to a retrospective study conducted in India, 57% (138/242) of the regional cases of equine ocular disorders Copyright: © 2021 by the authors. were diagnosed as ocular setariasis [12]. Infected horses displayed multiple ocular signs Licensee MDPI, Basel, Switzerland. including lacrimation, photophobia, corneal opacity, conjunctivitis and blindness, espe- This article is an open access article cially when treatment was delayed [12–14]. Corneal edema, synechia, cataract and retinal distributed under the terms and detachments may occur with toxins released from worms in the anterior chamber [15]. conditions of the Creative Commons Setaria digitata infecting horses in China has never been identified. This report is Attribution (CC BY) license (https:// the first time S. digitata has been identified in the eye of an equine patient in China by creativecommons.org/licenses/by/ molecular diagnosis. 4.0/). Vet. Sci. 2021, 8, 55. https://doi.org/10.3390/vetsci8040055 https://www.mdpi.com/journal/vetsci Vet. Sci. 2021, 8, 55 2 of 6 Vet. Sci. 2021, 8, 55 Setaria digitata infecting horses in China has never been identified. This report is the2 of 6 first time S. digitata has been identified in the eye of an equine patient in China by molec- ular diagnosis. 2.2. Materials Materials andand MethodsMethods AllAll procedures procedures involving involving the the horse horse in in this this study study were were carried carried out out with with a a welfare welfare license li- (AW62201202-2-1)cense (AW62201202 issued-2-1) issued by the by Animal the Animal Care and Care Use and Committee Use Committee of the of China the China Agriculture Ag- Universityriculture University in Beijing. in Beijing. 2.1.2.1. Case Case ReportReport AA 5-year-old5-year-old MongolianMongolian mare mare ( (EquusEquus caballus caballus LinnaeusLinnaeus,, 1758 1758)) presented presented with with ble- ble- pharospasm,pharospasm, squinting squinting and and photophobia photophobia to to the the Equine Equine Clinical Clinical Diagnostic Diagnostic Center Center of Chinaof AgriculturalChina Agricultural University. University. A gross A gross ophthalmic ophthalmic examination examination identified identified aa corneal opac- opacity andity and ocular ocular discharge discharge in thein the patient’s patient’s right right eye eye (Figure (Figure1 ).1). Closer Closer observationobservation revealed a thread-likea thread-like cylindrical cylindrical worm, worm, moving moving in in a swirlinga swirling motion, motion, in in the the anterior anterior chamber chamber ofof the rightthe right eye. eye. Microfilariae Microfilariae were were not not detected detected on on aa peripheralperipheral blood blood smear, smear, and and a complete a complete bloodblood count count diddid notnot showshow major abnormalities. abnormalities. Surgical Surgical removal removal was was chosen chosen over over exclu- exclu- sivesive medical medical treatmenttreatment to remove the the worm worm immediately. immediately. The The mare mare was was sedated sedated with with XylazoleXylazole (an(anα α-2-2 agonistagonist sedative)sedative) 1.1 mg/kg intravenously intravenously and and was was induced induced with with and and maintainedmaintained on on Tiletamine-ZolazepamTiletamine-Zolazepam 2.0 mg/kg mg/kg intravenously. intravenously. The The right right eye eye was was flushed flushed multiplemultiple timestimes withwith 3% boric acid solution, solution, and and the the cornea cornea was was desensitized desensitized with with drops drops ofof proparacaine proparacaine hydrochloridehydrochloride ophthalmic ophthalmic solution. solution. Wrapped Wrapped tightly tightly in insterile sterile medical medical gauzesgauzes and and withwith 22 mmmm of its tip exposed, exposed, a a #11 #11 surgical surgical blade blade was was used used to topuncture puncture open open thethe anterior anterior chamberchamber of the right right eye eye at at the the 6 6 o’clock o’clock position position of ofthe the cornea, cornea, about about 2 mm 2 mm insideinside the the limbus.limbus. TheThe worm moved moved towards towards the the puncture puncture site site and and was was easily easily removed removed withwith minimal minimal aqueousaqueous leakage. The The puncture puncture site site was was left left to tohe healal with with a 2 a mm 2 mm surgical surgical lesion.lesion. Terramycin Terramycin ophthalmic ophthalmic ointmentointment waswas administeredadministered four times daily daily for for one one week week as prophylaxis,as prophylaxis, and and flunixin flunixin meglumine meglumine was was injected injected intravenously intravenously at 1.1at 1.1 mg/kg mg/kg once once daily daily for three days as an anti-inflammatory medication. The extracted worm was washed for three days as an anti-inflammatory medication. The extracted worm was washed three three times with phosphate buffer saline (PBS), observed under a light microscope, then times with phosphate buffer saline (PBS), observed under a light microscope, then pre- preserved in 70% ethanol until its DNA was extracted. The ocular opacity completely served in 70% ethanol until its DNA was extracted. The ocular opacity completely cleared cleared approximately 4 weeks after surgery. No other medications were prescribed con- approximately 4 weeks after surgery. No other medications were prescribed considering sidering the horse recovered without complications. the horse recovered without complications. Figure 1. Corneal edema and ocular discharge in the right eye upon examination (A). Extracted S. digitata worm from the Figure 1. Corneal edema and ocular discharge in the right eye upon examination (A). Extracted S. digitata worm from the eye (B). eye (B). 2.2. Worm Identification Light microscopy was used to identify the worm’s species based on referenced mor- phological criteria [16]. DNA was extracted from the worm by following the instructions specified in the genomic DNA extraction kit (TSINGKE, Beijing, China). The worm was digested with 20 uL Proteinase K and 200 uL distilled water in a 1.5 mL centrifuge tube. The tube was vortexed for 10 s, then 200 uL buffer gA1 was added. The tube was then Vet. Sci. 2021, 8, 55 3 of 6 2.2. Worm Identification Light microscopy was used to
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