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Pseudocowpox Virus Infection in an American Bison (Bison Bison) Vinay Shivanna, A

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Pseudocowpox Virus Infection in an American Bison (Bison Bison) Vinay Shivanna, A Shivanna et al. BMC Veterinary Research (2020) 16:241 https://doi.org/10.1186/s12917-020-02464-7 CASE REPORT Open Access Pseudocowpox virus infection in an American bison (Bison bison) Vinay Shivanna, A. Giselle Cino-Ozuna, Cody Heskett, Douglas G. Marthaler and Charan Ganta* Abstract Background: The present report describes a case of pseudocowpox virus (PCPV) infection in a seven-year-old female bison euthanized due to a history of declining condition and sores on the vulva and udder. Case presentation: External examination revealed multifocal, raised, keratinized plaques (0.5–2 cm) covering the skin of the ventral surface of the tail, perineum, caudoventral abdomen, udder, both inguinal recesses, and the medial aspects of both thighs. No significant gross lesions were present in the reminder of the tissues examined. Histopathological examination of the affected skin showed moderate epidermal hyperplasia with rete pegs, marked parakeratotic hyperkeratosis with crusts of degenerate neutrophils and cell debris, and few epithelial cells undergoing ballooning degeneration with occasional eosinophilic intracytoplasmic inclusion bodies (3–5 μm Bollinger body). Negative staining electron microscopy from skin revealed typical Parapoxvirus (PPV) particles, which were also confirmed by real-time PCR (Ct =18.6). Metagenomic analysis of the skin samples revealed only poxviruses. The bison parapox B2L envelope gene clustered with other parapox sequences identified from ruminants. Conclusions: This is the first report of PCPV virus infection in an American bison. Identification of novel susceptible hosts of parapox viruses sheds light on the viral evolution and highlights the importance of potential economic impact of this disease to the bison industry. Keywords: Pseudocowpox virus, Bison, Zoonotic, Electron microscopy, Inclusions, Deep-sequencing Background through macules, papules, pustules and formation of The genus Parapoxvirus (PPV) within the family Poxviri- scabs [3]. Lesions are commonly seen on muzzle of dae is composed of four viruses: bovine popular stoma- calves and teats of affected cows [4, 5]. In uncomplicated titis virus, orf virus, pseudocoxpox virus (PCPV) and infections, scabs usually heal in a few days. PPV of red deer in New Zealand [1]. PPVs are ovoid PPVs are of zoonotic importance and cause cutaneous (250–300 nm long and 160–190 nm in diameter) with lesions in humans from direct contact with infected ani- thread-like surface tubules arranged in crisscross fash- mals commonly cows and sheep [6]. ion. Their genome is composed of linear double PPVs are epitheliotropic viruses with varying severity stranded DNA of 130 kbp. PCPV infections were re- of infections been reported in several ungulate species ported from most parts of the world and most com- such as red deer [7], reindeer [8], chamois, ibex [9], monly in dairy cows [2]. The common disease musk oxen [10], camels [11], gazelles [12] and wild Japa- presentation of PPV infections includes progression nese serows [13]. Infections have also been reported in non-ungulates such as red squirrels, gray squirrels [14], * Correspondence: [email protected] seals [15] and pygmy chimpanzee [16]. Occurrence of Kansas State University Veterinary Diagnostic Laboratory, Department of PPV infections in new species can cause severe infec- Diagnostic Medicine/Pathobiology, College of Veterinary Medicine, Kansas State University, Manhattan, Kansas 66506, USA tions and pose a significant threat to the entire © The Author(s). 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. 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 in a credit line to the data. Shivanna et al. BMC Veterinary Research (2020) 16:241 Page 2 of 6 population of the new species [14] . PPV in general and and became gradually fewer and smaller in size (0.2–0.5 PCPV infections in particular have not been reported cm) distal to the thighs. Smaller nodules (0.2–0.5 cm) previously in the American bison. We report and de- also covered both axillae and the hind limbs distal to the scribe the first case of PCPV in bison, potential patho- thigh. No significant gross lesions were observed in the genesis of PCPV in bison and highlight potential remaining of the organs examined. economic impact of this disease in the bison industry. Multiple skin sections were fixed in 10% neutral buff- ered formalin immediately after necropsy, and routinely Case presentation processed for histopathologic examination in an auto- Case history, gross and histopathological findings mated tissue processor and embedded in paraffin. Slide- A seven-year-old female intact American bison from the mounted tissue sections (~ 4 um thick) were stained Konza Prairie Biological Station (KPBS) was presented with hematoxylin and eosin and evaluated by a certified for necropsy examination at Kansas State Veterinary veterinary anatomic pathologist. Histopathology of mul- Diagnostic Laboratory (KSVDL). The bison was hu- tiple skin nodules (Fig. 1c, d) consistently showed mod- manely euthanized by KPBS following a clinical history erate epidermal hyperplasia, swollen keratinocytes with of poor and declining condition prior to submission to elongated rete pegs and parakeratotic hyperkeratosis that KSVDL. Humane euthanasia was performed by KPBS contain focal aggregates of degenerate neutrophils. Mul- using the gunshot method according to the American tifocally, within the epidermis, the hyperplastic stratum Veterinary Medical Association (AVMA) guidelines. spinosum and stratum corneum had undergone balloon- During the euthanasia, multiple cutaneous nodules were ing degeneration with occasional eosinophilic intracyto- noticed in the vulva and udder, and a mucus discharge plasmic inclusions measuring 5–15 μm diameter (white was seen from the nose. A complete postmortem exam- arrows) and pyknotic nuclei (Fig. 1c, d). ination revealed lesions limited to the skin. There were multiple wart-like proliferative nodules on the ventral Detection of PPV by real-time PCR and electron tail, perineum, caudoventral abdomen, udder, both in- microscopy guinal recesses, and the medial aspects of both thighs, Generic PPV real-time PCR testing occurred at Texas and axillary regions (Fig. 1a and b). Skin nodules were Veterinary Medical Diagnostic Laboratory (TVMDL). A keratinized, raised, proliferative, 0.5–2 cm in diameter representative section of the skin nodule submitted to Fig. 1 Gross and histopathological lesions of PPV infection in American bison. a, b Multiple raised keratinized nodules on the skin of ventral aspect of tail, perineum, caudoventral abdomen, udder, inguinal recesses, medial aspect of thighs and axilla. c, d Histopathological examination of the skin nodules. There is marked epidermal hyperplasia with parakeratotic hyperkeratosis and ballooning degeneration of keratinocytes within the stratum corneum and stratum spinosum. Multifocally, swollen keratinocytes contain eosinophilic intracytoplasmic inclusion bodies (white arrows) Shivanna et al. BMC Veterinary Research (2020) 16:241 Page 3 of 6 Texas Veterinary Medical Diagnostic Laboratory Phylogenetic analysis (TVMDL) was positive for PPV by real-time PCR with a B2L gene amplification, sequencing and phylogenetic Ct value of 18.6, confirming strong positivity for PPV. analysis has been used previously for identification and Skin nodules were processed for visualizing viral parti- classification of unknown PPVs [7, 8, 19]. To further cles by negative staining. The suspensions obtained from classify the PPV, the 594 bp part of the B2L gene was ground skin nodules were mixed with 2% phosphotung- amplified from the skin nodules and Sanger sequenced stic acid and nebulized onto EM grids. The negatively- (Genewiz) using previously described primers and stained grids examined by electron microscopy revealed methods [8, 9]. Phylogenetic analysis of the B2L gene in- characteristic parapox viral particles that were oval in cluded representative sequences previously described [9] shape (approx. 260 nm long and 160 nm wide) with a and our newly sequenced strain. Sequences were aligned spirally organized surface tubules (Fig. 2). using MUSCLE [20], Maximum likelihood phylogenetic tree with 500 bootstrap replicates was created using Deep sequencing PHyML [21]. Phylogenetic analysis illustrated that the Sample processing and metagenomic sequencing was per- bison PPV was closely related to bovine PCPV (Fig. 4). formed similar to previously described methods [17, 18]. Skin samples with lesions were processed using the Illu- Discussion and conclusions mina Nextera XT Library Preparation Kit, according to
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