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Disease of Aquatic Organisms 134:57 Vol. 134: 57–64, 2019 DISEASES OF AQUATIC ORGANISMS Published online April 25 https://doi.org/10.3354/dao03358 Dis Aquat Org NOTE Epidemic nodular facial myxomatous dermatitis in juvenile Cranwell’s horned frogs Ceratophrys cranwelli Kenichi Tamukai1, Junichi Sugiyama2, Yuta Nagata2, Omatsu Tsutomu3, Yukie Katayama3, Tetsuya Mizutani3, Masanobu Kimura4, Yumi Une5,* 1Den-en-chofu Animal Hospital, 2-1-3 Denenchofu, Ota-ku, Tokyo 145-0071, Japan 2Laboratory of Veterinary Pathology, Azabu University,1-17-71 Fuchinobe, Chuo-ku, Sagamihara, Kanagawa 252-5201, Japan 3Research and Education Center for Global Infectious Diseases of Animals, Tokyo University of Agriculture and Technology, 3-5-8 Fuchu, Tokyo 183-8507, Japan 4Department of Veterinary Science, National Institute of Infectious Diseases, 1-23-1 Toyama, Shinjuku-ku, Tokyo 162-8640, Japan 5Laboratory of Veterinary Pathology, Okayama University of Science, 1-3 Ikoino-oka, Imabari, Ehime 794-8555, Japan ABSTRACT: In 2017, approximately 40 out of 100 captive Cranwell’s horned frogs Ceratophrys cranwelli from several facilities in Japan exhibited protruding facial lesions. Histopathological examination was performed on 6 specimens with such lesions randomly selected from 2 facilities. Lesions consisted of scattered stellate to spindle-shaped cells without atypia in an abundant myxoid matrix and occasional lymphocytic infiltrates. Maxillary bone was resorbed. No etiological organisms were detected using light microscopy or metagenomic analysis of the lesions. Macro- scopic and histological assessments indicate that the lesions are associated with nodular facial myxomatous dermatitis, which has never been reported in amphibians. KEY WORDS: Myxomatous · Facial lesions · Pacman frog · Ceratophryidae · Morphological Resale or republication not permitted without written consent of the publisher 1. INTRODUCTION Myxoid soft tissue dermal masses include neoplas- tic and viral-induced lesions. Myxomas, which origi- The 8 species of Ceratophrys, from the family Cer- nate from fibroblasts or multipotent mesenchymal atophryidae, are found in South America and are gen- cells, are benign soft-tissue tumors that have abun- erally called horned frogs or Pacman frogs. Although dant myxoid matrices rich in mucopolysaccharides. some species are very popular pets, few studies have Myxomas are rare in domesticated animals, typically focused on the diseases that affect these species. The occurring in middle-aged or older dogs and cats most common disorders include nutritional disorders (Hendric 2016). Myxomatosis is a generalized, fulmi- (nutritional hyperparathyroidism complex, obesity, and nant, and frequently lethal disease in rabbits caused corneal lipidosis), the impact of substrates, trauma, by the myxoma virus, a poxvirus that is associated atypical bacterial infections, and chytridiomycosis with the appearance of mucoid subcutaneous tumors (Wright 2001, Une et al. 2008). While amphibian tu- on the face (Fenner & Fantini 1994). Cunningham et mors are regularly reported, little is known about tu- al. (1993) reported unusual mortality associated with mors in the Ceratophryidae (Asashima et al. 1987, poxvirus-like particles in European common frogs Green & Harshbarger 2001, Stacy & Parker 2004). Rana temporaria. *Corresponding author: [email protected] © Inter-Research 2019 · www.int-res.com 58 Dis Aquat Org 134: 57–64, 2019 Healthy and blemish-free animals are important facilities A and B. Subjects were less than 6 mo old from an economic point of view given their value as and had vigor and good appetite. Progressive lesions pets. It is also necessary to elucidate the mode of began to appear from 2 mo after metamorphosis and disease progression in captive populations, which were primarily located in the facial region and max- may provide useful insights for the conservation of illa (Fig. 1). However, the lesions were not fatal if wild populations. Juvenile horned frogs with facial feeding was not impeded. deformities caused by bulbous lesions emerged in several distribution facilities in Japan in 2017. Therefore, the aim of this study was to evaluate 2.2. Animals these pathologic findings and elucidate the mecha- nism of pathogenesis in the lesions through mor- Specimens were housed in plastic containers with a phological, microbiological, and molecular biologi- water depth of 0.5 cm. Each facility used a com- cal examination including metagenomic analyses. pletely different source of well water. The daytime ambient temperature ranged from 23 to 28°C. Speci- mens from facility A were fed commercial food (Pac- 2. MATERIALS AND METHODS man Food; Samurai Japan Reptiles). The specimens from facility B and pet shop C were fed captive-bred 2.1. Case history house crickets Acheta domesticus, pinky mice, and goldfish. They were also given small quantities of Horned frogs with deformed faces were found in vitamins and mineral supplements. succession from breeding facility A in Saitama pre- Six specimens were randomly selected from 2 facil- fecture, breeding facility B in Ibaraki prefecture, and ities (4 from breeding facility A [Cases 1−4] and 2 pet shop C in Tokyo in 2017. Cranwell’s horned frogs from pet shop C [Cases 5 and 6]; mean body length: Ceratophrys cranwelli, Argentine horned frogs C. 58 mm [range 41−68 mm]; mean body weight: 23.5 g ornata, Surinam horned frogs C. cornuta, and fantasy [range 8.2−31 g]) (Table 1). horned frogs (C. cranwelli × C. cornuta) were housed All animals were euthanized by spinal cord disrup- in the same facilities and given the same diet tion after being anesthetized by a 5 min immersion in and water; however, only captive-bred Cranwell’s a bath of 0.1% eugenol solution, an anesthetic drug horned frogs were affected. All frogs from both facil- for fish and crustaceans (FA100, Tamura-Seiyaku). ities A and B were reared without the introduction of Consent from the 2 facilities was obtained for all any new frogs, either from the wild or from captivity. specimens, and they were handled and housed in The prevalence of affected individuals reached up accordance with Azabu University’s ethical guide- to 40% (approximately 40 of 100 frogs) at breeding lines for animal experimentation. Fig. 1. (A) Lateral view of facial lesions in an affected Ceratophrys cranwelli frog (case 5). The face was notably deformed, and multifocal to coalescing nodules of varying sizes extended around the eyes. The inset shows a section of the lesions. Mucoid liquid was emitted. (B) Appearance of an unaffected frog Tamukai et al.: Epidemic myxomatous dermatitis in horned frogs 59 Table 1. Case characteristics of 6 Ceratophrys cranwelli specimens. (+) positive, (−) negative Case Body Body Sex PCR testing for pathogens Isolation for Brucella weight length Rana- Brucella Facial Liver Femoral (g) (mm) virus Facial Liver Femoral lesion marrow lesion marrow 1 30.94 67 Male − − − − − + − 2 26.92 58 Male − − − + − + − 3 24.94 51 Male − − − + − + − 4 8.15 41 Male − − − − − − − 5 26.64 68 Unidentified − − − + − − + 6 19.37 61 Unidentified − − + + − − − 2.3. Histopathological examination supplement SR0083 (Oxoid), and incubated for 3 d at 37°C in a shaking incubator (BR-23FP, Taitec). Ali - Facial lesions, including the maxilla bone, were col- quots of the cultures were inoculated on brain−heart lected during necropsy, processed routinely, and em- infusion agar plates, and the plates were incubated bedded in paraffin wax. Sections (4 µm) were stained for 1 d at 37°C (Kimura et al. 2017). with hematoxylin and eosin. Selected sections of the facial lesions were stained with colloidal iron stain, Giemsa stain, Ziehl-Neelsen stain, and immunohisto- 2.6. High-throughput sequencing analysis chemical stain for Brucella spp. Primary antibodies for immunohistochemistry staining were obtained from Eight samples, including 6 from facial lesions and atypical Brucella strains originating from White’s tree 2 from eyes, were analyzed with high-throughput frog Litoria caerulea and Denny’s whipping frog Rha- sequencing. Total RNA was extracted from homo - cophorus dennysi (Kimura et al. 2017). For compari- genate tissue samples with a High Pure Viral Nucleic son, we also performed histological examinations on a Acid Kit (Roche), and contaminated ribosomal RNA normal frog (see Figs. 1B & 3C). was depleted with a RiboMinus Eukaryote Kit for RNA-Seq (Thermo Fisher Scientific). To determine the viral RNA genome, cDNA libraries for high- 2.4. PCR testing throughput sequencing were prepared with a NEB- Next® Ultra™ RNA Library Prep Kit for Illumina To test for ranavirus, total DNA was extracted from (New England Biolabs); sequencing was performed fresh kidney and facial lesion samples using a Nucle - using a MiSeq benchtop sequencer (Illumina) with a oSpin Tissue kit (Macherey-Nagel). Three primer MiSeq Reagent Kit v3 (150 cycles). The obtained sets (M68/M154, MCP4/MCP5, and RanaJP556F/ reads were analyzed using CLC Genomics Work- RanaJP772R) were used to amplify the major capsid bench 6.5.1 (https:// www. qiagenbioinformatics. com/). protein gene (MCP) fragments (Mao et al. 1997, Une The obtained raw reads were trimmed based on et al. 2013). sequence quality. Contigs were assembled from To test for Brucella, total DNA was extracted from trimmed reads, using de novo assembly command, facial lesions, liver, and femoral marrow tissue homo - and analyzed with local BLAST analysis based on genates and from isolated bacterial cells using a virus genome data from the National Center for DNA mini kit (Qiagen). Brucella DNA was detected Biotechnology Information. by PCRs specific for bcsP31, which encodes a cell surface protein, and omp2a, omp2b, and omp31 genes, which encode outer membrane proteins (Ima - 3. RESULTS oka et al. 2007). 3.1. Macroscopic findings 2.5. Culture and isolation of Brucella Exophytic and nodular facial lesions were ob - served on all specimens (Fig. 2). Variably sized, mul- Tissue homogenates were cultured on ATCC tifocal to coalescing nodules extended around the medium 488 broth containing Brucella-selective eyes (Fig. 1A). The face was notably deformed and 60 Dis Aquat Org 134: 57–64, 2019 Fig. 2. Macroscopic findings of facial lesions in Ceratophrys cranwelli specimens. (A−F) Cases 1−6, respectively.
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