Oral Squamous Cell Carcinoma in a Red Deer (Cervus elaphus) Source: Journal of Wildlife Diseases, 50(1):113-116. Published By: Wildlife Disease Association URL: http://www.bioone.org/doi/full/10.7589/2012-03-090
BioOne (www.bioone.org) is a nonprofit, online aggregation of core research in the biological, ecological, and environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published by nonprofit societies, associations, museums, institutions, and presses. Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of BioOne’s Terms of Use, available at www.bioone.org/page/ terms_of_use. Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder.
BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research.
DOI: 10.7589/2012-03-090
Journal of Wildlife Diseases, 50(1), 2014, pp. 113–116 # Wildlife Disease Association 2014
Oral Squamous Cell Carcinoma in a Red Deer (Cervus elaphus) Reiner Ulrich,1,4 Jens Peter Teifke,2 Ulrich Voigt,3 and Frauke Seehusen1 1Department of Pathology, University of Veterinary Medicine Hannover, Bu¨nteweg 17, 30559 Hannover, Germany; 2Friedrich-LoefflerInstitut, Federal Research Institute for Animal Health, Su¨dufer 10, 17493 Greifswald, Insel Riems, Germany; 3 Institute for Terrestrial and Aquatic Wildlife Research, University of Veterinary Medicine Hannover, Bischofsholer Damm 15, 30173 Hannover, Germany; 4Corresponding author (email: [email protected])
An infiltrative, multilobulated, white to grey, rubbery to firm, 123636-cm mass extended from the oral cavity into the right maxilla, nasal turbinates, and nasal septum (Fig. 1). The right upper jaw displayed focally extensive osteolysis and loss of all premolars and the first and second molars. The right retropharyngeal lymph node was moderately enlarged. Histopathology revealed an infiltrative, moderately cellular mass extending from the oral squamous mucosa into the underlying soft tissues and bone. The mass consisted of cords and nests of epithelial cells within an abundant collagenous stroma, interpreted as desmoplasia (Fig. 2A). The epithelial cells had distinct borders, a variable diameter of ,25 mm, a moderate to abundant amount of eosinophilic cytoplasm, and oval nuclei with coarsely granulated chromatin and one–three nucleoli. There was moderate anisocytosis and anisokaryosis. There were up to two mitotic figures per highpower (4003) field. A few scattered cells displayed cytoplasmic hypereosinophilia combined with nuclear condensation and loss, interpreted as dyskeratosis (Fig. 2B). The oral mucosa was multifocally ulcerated and the adjacent mass displayed a focally extensive infiltration of mainly neutrophils, eosinophils, fewer macrophages, and granulation tissue. There was a mild, diffuse infiltration of lymphocytes and fewer macrophages and plasma cells. The cortical sinus of the right retropharyngeal lymph node contained a cluster of densely packed polygonal epithelial cells resembling those described for the oral mass, interpreted as metastasis.
ABSTRACT: We describe the pathomorphologic and immunophenotypic characteristics of an oral squamous cell carcinoma in a 13-yr-old, free-ranging red deer (Cervus elaphus) in Lower Saxony, Germany. Key words: Cervus elaphus, neoplasia, oral cavity, red deer, squamous cell carcinoma.
The red deer (Cervus elaphus) is a common wildlife species in Europe, Asia, and North Africa, and a frequent subject of ecologic science and popular hunting reports (Ludt et al. 2004). However, little is known about the type and frequency of its naturally occurring noninfectious diseases, especially neoplasms. The most frequently reported tumors of red deer are papillomavirus (PV) -associated dermal fibropapillomas and papillomas (Boch and Schneidawind 1988; Erdelyi et al. 2009). Further reports include hepatic carcinoid, auricular chondromas, oral fibrosarcomas, testicular fibroma, metastatic cavernous hemangiosarcoma of bone, subcutis, and lung, testicular interstitial cell tumor, dermal malignant melanoma, anaplastic oligodendroglioma, malignant schwannoma, and ovarian teratoma (Boch and Schneidawind 1988; Perez et al. 1998; Hofle et al. 2004; Scandrett and Wobeser 2004; Gregoire et al. 2008; Peters and Wohlsein 2008; Zele et al. 2011). In August 2010, an emaciated, freeranging, adult, female red deer was killed by a forest ranger in Lower Saxony, Germany. The age of the deer, determined by counting annual cementum layers in both first incisors (I1; Azorit et al. 2004) was 13 yr. The head and neck were submitted for pathologic investigation of a grossly evident mass in the right maxilla. 113
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FIGURE 1. Macroscopic view of a squamous cell carcinoma from the oral cavity in a red deer. Transverse section of the skull displaying an infiltrative neoplastic mass (stars) focally effacing the maxilla, nasal turbinates and nasal septum; c5left nasal conchae; p5hard palate; s5nasal septum.
Immunohistochemical (IHC) staining was performed with the avidin–biotin– peroxidase complex method (Vector Laboratories, Burlingame, California, USA) with the use of two monoclonal anti-cytokeratin antibodies (clone AE1/AE3, reacts with human cytokeratins 1, 2, 3, 4, 5, 6, 7, 8, 10, 13, 14, 15, 16, and 19; clone MNF116, reacts with human cytokeratins 5, 6, 8, 17, and probably 19), a monoclonal antivimentin antibody (clone V9; Ulrich et al. 2009), and a polyclonal rabbit anti-bovine PV (BPV) antibody (Teifke et al. 2003; all from Dako Deutschland GmbH, Hamburg, Germany). The specificity of the IHC reactions was confirmed with the use of normal red deer oral mucosa and BPV 1induced bovine cutaneous fibropapilloma. As a negative control, serial sections were treated with Balb/c mouse ascites fluid or rabbit hyperimmune-serum directed
FIGURE 2. Histologic and immunohistologic characterization of a squamous cell carcinoma from the oral cavity in a red deer. (A) Cords and nests of neoplastic epithelial cells (arrows) within an abundant collagenous stroma; m5oral mucosa; s5stroma; hematoxylin and eosin; bar5100 mm. (B) Few multifocal neoplastic epithelial cells displaying keratinization (arrow). Hematoxylin and eosin, bar525 mm. (C) Most neoplastic epithelial cells (arrow) display cytoplasmic cytokeratin (clone MNF116) immunoreactivity, whereas the stromal cells are negative. Avidin–biotin–peroxidase complex method, hematoxylin counterstain, Nomarski differential interference contrast, bar550 mm.
SHORT COMMUNICATIONS
against the major capsid protein pUL19 of pseudorabies virus (Klupp et al. 2000), instead of the primary monoclonal or polyclonal antibodies, respectively. Most of the neoplastic epithelial cells in the oral mass and the lymph node displayed a variably strong cytoplasmic immunoreactivity employing both pan-cytokeratin markers. In general, more cells were immunoreactive and the label was of stronger quality with clone MNF116 (Fig. 2C). Although most spindloid stromal fibroblasts and vessels displayed moderate cytoplasmic vimentin immunoreactivity, neoplastic epithelial cells were uniformly negative. No PV immunoreactivity was detected. We performed a PCR reaction with the use of the previously described consensus primer pair set IFNR2 and IDNT2, which allows the detection of a 102 base-pair fragment of the L1 gene of multiple PVs, including BPV1, BPV2, ovine PV (OPV)1, OPV2, European elk PV, deer PV, canine oral PV, and the PV of Mastomys coucha in formalin-fixed, paraffin-embedded tissues (Teifke et al. 2003). Cloned genomic DNA of BPV1 (kindly provided by P.M. Howley, Maryland) was used as positive control and a sample without DNA was included in each run to check for contamination. However, no PV DNA was detectable within the tumor tissue of the present case. Squamous cell carcinoma (SCC) is a locally invasive and occasionally metastatic malignant neoplasm of the epidermal cells of the skin and the squamous epithelia of the mucous membranes with varying degree of keratinocyte (squamous cell) differentiation. Etiologic risk factors for SCCs include ultraviolet light, PV infection, bracken fern ingestion, and carcinogens in tobacco, coal tar, soot, arsenic, and smegma (Brown et al. 2007). There has been a marked increase in the incidence of human SCC over the last 50 yr, with UV light representing the most important risk factor (Dal et al. 2008), and PV infection as a possible cofactor (Munday and Kiupel
115
2010). To our knowledge SCC has not been previously reported in red deer. However, SCC has been reported in other Cervidae, including the skin of the front leg of an 18-yr-old female Pe`re David’s deer (Elaphurus davidianus; Agrimi et al. 1993) and the skin of the front leg with metastasis to the ipsilateral prescapular lymph node and lungs of a 9-yr-old female Indochina sika deer (Cervus nippon pseudaxis; Ensley et al. 1980). In addition, an oronasal SCC with metastasis to the ipsilateral retropharyngeal lymph node was described in a 3.5-yr-old white-tailed deer (Odocoileus virginianus; Stroud and Amundson 1983). Although SCCs of the oropharynx, esophagus, and forestomachs of cattle are rare, they are relatively common in certain geographic locations in England, Scotland, Brazil, and Bolivia. Suspected causes for this regional disparity include BPV4 infection and bracken fern ingestion (Brown et al. 2007). There is growing evidence that PVs are involved in the pathogenesis of SCCs in multiple species including humans, cats (Felis catus), dogs (Canis lupus familiaris), sheep (Ovis aries), rabbits (Sylvilagus floridanus and Oryctolagus cuniculus), western barred bandicoots (Perameles bougainville), Natal multimammate mice (Mastomys natalensis; Munday and Kiupel 2010), a ferret (Mustela putorius furo; Rodrigues et al. 2010), and horses (Equus ferus caballus; Knight et al. 2011). No cytopathic evidence of PV infection and no PV antigen or DNA were detectable in our case. This does not, however, rule out the possibility that PVs can be involved in the induction of SCCs in red deer, because PV-induced neoplastic transformation is often associated with restricted and nonproductive infection that may not be detectable in all cases (Teifke et al. 2003; Munday and Kiupel 2010; Knight et al. 2011). Many well-differentiated SCCs display formation of concentric lamellae of keratin (keratin pearls). In contrast, many poorly differentiated tumors, such as our case, only show keratinization of
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individual cells (Goldschmidt and Hendrick 2002). Immunohistochemistry for cytoskeletal intermediate filaments like cytokeratin and vimentin are commonly applied tools for the identification of the histogenetic origin of poorly differentiated tumors (Ulrich et al. 2009). Cytokeratin immunoreactivity of the neoplastic epithelial cells in the oral mass and lymph node metastasis prove the epithelial histogenesis of this tumor (Erdelyi et al. 2009). Continuous wildlife disease monitoring and documentation through published reports is essential to help identify environmental hazard-induced (e.g., radiation, carcinogens, and toxins) increases in disease frequencies among exposed sentinel species. We thank Gu¨nter Schro¨der, Enercity Forestry Office, Wedemark for submission of this case. LITERATURE CITED Agrimi U, Morelli L, Di Guardo G. 1993. Squamous cell carcinoma of the skin in a Pe`re David’s deer (Elaphurus davidianus). J Wildl Dis 29:616–617. Azorit C, Munoz-Cobo J, Hervas J, Analla M. 2004. Aging through growth marks in teeth of Spanish red deer. Wildl Soc Bull 32:702–710. Boch J, Schneidawind H. 1988. Rotwild (Cervus elaphus L.). In: Krankheiten des jagdbaren Wildes, Boch J and Schneidawind H (eds.). Paul Parey, Hamburg, Germany, pp. 20–63. Brown CC, Baker DC, Barker IK. 2007. Alimentary system. In: Jubb, Kennedy, and Palmer’s pathology of domestic animals. 5th Ed, Maxie MG (ed.). Elsevier, Edinburgh, Great Britain, pp. 3–296. Dal H, Boldemann C, Lindelof B. 2008. Trends during a half century in relative squamous cell carcinoma distribution by body site in the Swedish population: Support for accumulated sun exposure as the main risk factor. J Dermatol 35:55–62. Ensley PK, Janssen DL, Anderson MP. 1980. Squamous cell carcinoma in an Indochina sika deer. J Am Vet Med Assoc 177:932. Erdelyi K, Gal J, Sugar L, Ursu K, Forgach P, Szeredi L, Steineck T. 2009. Papillomavirusassociated fibropapillomas of red deer (Cervus elaphus). Acta Vet Hung 57:337–344. Goldschmidt MH, Hendrick MJ. 2002. Tumors of the skin and soft tissues. In: Tumors in domestic animals, Meuten DJ (ed.). Iowa State Press, Ames, Iowa, pp. 45–118.
Gregoire F, Mousset B, Hanrez D, Cassart D, Desmecht D, Linden A. 2008. Cavernous haemangiosarcoma in a free-living red deer (Cervus elaphus). Vet Rec 162:692–693. Hofle U, Vicente J, Gortazar C. 2004. Bilateral ovarian teratoma in a free-living Iberian red deer (Cervus elaphus hispanicus). N Z Vet J 52:44–45. Klupp BG, Granzow H, Mettenleiter TC. 2000. Primary envelopment of pseudorabies virus at the nuclear membrane requires the UL34 gene product. J Virol 74:10063–10073. Knight CG, Munday JS, Peters J, Dunowska M. 2011. Equine penile squamous cell carcinomas are associated with the presence of equine papillomavirus type 2 DNA sequences. Vet Pathol 48:1190–1194. Ludt CJ, Schroeder W, Rottmann O, Kuehn R. 2004. Mitochondrial DNA phylogeography of red deer (Cervus elaphus). Mol Phylogenet Evol 31:1064– 1083. Munday JS, Kiupel M. 2010. Papillomavirus-associated cutaneous neoplasia in mammals. Vet Pathol 47:254–264. Perez J, de las Mulas JM, Arenas A, Luque I, Carrasco L. 1998. Malignant schwannoma in a red deer (Cervus elaphus). Vet Rec 143:585–587. Peters M, Wohlsein P. 2008. Anaplastic oligodendroglioma with meningeal infiltration in a freeranging red deer (Cervus elaphus). J Comp Pathol 138:59–62. Rodrigues A, Gates L, Payne HR, Kiupel M, Mansell J. 2010. Multicentric squamous cell carcinoma in situ associated with papillomavirus in a ferret. Vet Pathol 47:964–968. Scandrett B, Wobeser G. 2004. Malignant melanoma in a captive red deer (Cervus elaphus elaphus). J Wildl Dis 40:808–810. Stroud RK, Amundson TE. 1983. Squamous cell carcinoma in a free-ranging white-tailed deer (Odocoileus virginianus). J Wildl Dis 19:162– 164. Teifke JP, Kidney BA, Lohr CV, Yager JA. 2003. Detection of papillomavirus-DNA in mesenchymal tumour cells and not in the hyperplastic epithelium of feline sarcoids. Vet Dermatol 14:47–56. Ulrich R, Eydner M, Gru¨n A, Haydn J, Baumga¨rtner W. 2009. A biphasic malignant mesothelioma of the peritoneum and pleura in a horse. Dtsch Tiera¨rztl Wochenschr 116:186–191. Zele D, Gombac M, Svara T, Vengust G. 2011. A case of hepatic carcinoid in a red deer hind (Cervus elaphus). Acta Vet Hung 59:319–325.
Submitted for publication 22 March 2012. Accepted 3 June 2013.
BioOne (www.bioone.org) is a nonprofit, online aggregation of core research in the biological, ecological, and environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published by nonprofit societies, associations, museums, institutions, and presses. Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of BioOne’s Terms of Use, available at www.bioone.org/page/ terms_of_use. Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder.
BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research.
DOI: 10.7589/2012-03-090
Journal of Wildlife Diseases, 50(1), 2014, pp. 113–116 # Wildlife Disease Association 2014
Oral Squamous Cell Carcinoma in a Red Deer (Cervus elaphus) Reiner Ulrich,1,4 Jens Peter Teifke,2 Ulrich Voigt,3 and Frauke Seehusen1 1Department of Pathology, University of Veterinary Medicine Hannover, Bu¨nteweg 17, 30559 Hannover, Germany; 2Friedrich-LoefflerInstitut, Federal Research Institute for Animal Health, Su¨dufer 10, 17493 Greifswald, Insel Riems, Germany; 3 Institute for Terrestrial and Aquatic Wildlife Research, University of Veterinary Medicine Hannover, Bischofsholer Damm 15, 30173 Hannover, Germany; 4Corresponding author (email: [email protected])
An infiltrative, multilobulated, white to grey, rubbery to firm, 123636-cm mass extended from the oral cavity into the right maxilla, nasal turbinates, and nasal septum (Fig. 1). The right upper jaw displayed focally extensive osteolysis and loss of all premolars and the first and second molars. The right retropharyngeal lymph node was moderately enlarged. Histopathology revealed an infiltrative, moderately cellular mass extending from the oral squamous mucosa into the underlying soft tissues and bone. The mass consisted of cords and nests of epithelial cells within an abundant collagenous stroma, interpreted as desmoplasia (Fig. 2A). The epithelial cells had distinct borders, a variable diameter of ,25 mm, a moderate to abundant amount of eosinophilic cytoplasm, and oval nuclei with coarsely granulated chromatin and one–three nucleoli. There was moderate anisocytosis and anisokaryosis. There were up to two mitotic figures per highpower (4003) field. A few scattered cells displayed cytoplasmic hypereosinophilia combined with nuclear condensation and loss, interpreted as dyskeratosis (Fig. 2B). The oral mucosa was multifocally ulcerated and the adjacent mass displayed a focally extensive infiltration of mainly neutrophils, eosinophils, fewer macrophages, and granulation tissue. There was a mild, diffuse infiltration of lymphocytes and fewer macrophages and plasma cells. The cortical sinus of the right retropharyngeal lymph node contained a cluster of densely packed polygonal epithelial cells resembling those described for the oral mass, interpreted as metastasis.
ABSTRACT: We describe the pathomorphologic and immunophenotypic characteristics of an oral squamous cell carcinoma in a 13-yr-old, free-ranging red deer (Cervus elaphus) in Lower Saxony, Germany. Key words: Cervus elaphus, neoplasia, oral cavity, red deer, squamous cell carcinoma.
The red deer (Cervus elaphus) is a common wildlife species in Europe, Asia, and North Africa, and a frequent subject of ecologic science and popular hunting reports (Ludt et al. 2004). However, little is known about the type and frequency of its naturally occurring noninfectious diseases, especially neoplasms. The most frequently reported tumors of red deer are papillomavirus (PV) -associated dermal fibropapillomas and papillomas (Boch and Schneidawind 1988; Erdelyi et al. 2009). Further reports include hepatic carcinoid, auricular chondromas, oral fibrosarcomas, testicular fibroma, metastatic cavernous hemangiosarcoma of bone, subcutis, and lung, testicular interstitial cell tumor, dermal malignant melanoma, anaplastic oligodendroglioma, malignant schwannoma, and ovarian teratoma (Boch and Schneidawind 1988; Perez et al. 1998; Hofle et al. 2004; Scandrett and Wobeser 2004; Gregoire et al. 2008; Peters and Wohlsein 2008; Zele et al. 2011). In August 2010, an emaciated, freeranging, adult, female red deer was killed by a forest ranger in Lower Saxony, Germany. The age of the deer, determined by counting annual cementum layers in both first incisors (I1; Azorit et al. 2004) was 13 yr. The head and neck were submitted for pathologic investigation of a grossly evident mass in the right maxilla. 113
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JOURNAL OF WILDLIFE DISEASES, VOL. 50, NO. 1, JANUARY 2014
FIGURE 1. Macroscopic view of a squamous cell carcinoma from the oral cavity in a red deer. Transverse section of the skull displaying an infiltrative neoplastic mass (stars) focally effacing the maxilla, nasal turbinates and nasal septum; c5left nasal conchae; p5hard palate; s5nasal septum.
Immunohistochemical (IHC) staining was performed with the avidin–biotin– peroxidase complex method (Vector Laboratories, Burlingame, California, USA) with the use of two monoclonal anti-cytokeratin antibodies (clone AE1/AE3, reacts with human cytokeratins 1, 2, 3, 4, 5, 6, 7, 8, 10, 13, 14, 15, 16, and 19; clone MNF116, reacts with human cytokeratins 5, 6, 8, 17, and probably 19), a monoclonal antivimentin antibody (clone V9; Ulrich et al. 2009), and a polyclonal rabbit anti-bovine PV (BPV) antibody (Teifke et al. 2003; all from Dako Deutschland GmbH, Hamburg, Germany). The specificity of the IHC reactions was confirmed with the use of normal red deer oral mucosa and BPV 1induced bovine cutaneous fibropapilloma. As a negative control, serial sections were treated with Balb/c mouse ascites fluid or rabbit hyperimmune-serum directed
FIGURE 2. Histologic and immunohistologic characterization of a squamous cell carcinoma from the oral cavity in a red deer. (A) Cords and nests of neoplastic epithelial cells (arrows) within an abundant collagenous stroma; m5oral mucosa; s5stroma; hematoxylin and eosin; bar5100 mm. (B) Few multifocal neoplastic epithelial cells displaying keratinization (arrow). Hematoxylin and eosin, bar525 mm. (C) Most neoplastic epithelial cells (arrow) display cytoplasmic cytokeratin (clone MNF116) immunoreactivity, whereas the stromal cells are negative. Avidin–biotin–peroxidase complex method, hematoxylin counterstain, Nomarski differential interference contrast, bar550 mm.
SHORT COMMUNICATIONS
against the major capsid protein pUL19 of pseudorabies virus (Klupp et al. 2000), instead of the primary monoclonal or polyclonal antibodies, respectively. Most of the neoplastic epithelial cells in the oral mass and the lymph node displayed a variably strong cytoplasmic immunoreactivity employing both pan-cytokeratin markers. In general, more cells were immunoreactive and the label was of stronger quality with clone MNF116 (Fig. 2C). Although most spindloid stromal fibroblasts and vessels displayed moderate cytoplasmic vimentin immunoreactivity, neoplastic epithelial cells were uniformly negative. No PV immunoreactivity was detected. We performed a PCR reaction with the use of the previously described consensus primer pair set IFNR2 and IDNT2, which allows the detection of a 102 base-pair fragment of the L1 gene of multiple PVs, including BPV1, BPV2, ovine PV (OPV)1, OPV2, European elk PV, deer PV, canine oral PV, and the PV of Mastomys coucha in formalin-fixed, paraffin-embedded tissues (Teifke et al. 2003). Cloned genomic DNA of BPV1 (kindly provided by P.M. Howley, Maryland) was used as positive control and a sample without DNA was included in each run to check for contamination. However, no PV DNA was detectable within the tumor tissue of the present case. Squamous cell carcinoma (SCC) is a locally invasive and occasionally metastatic malignant neoplasm of the epidermal cells of the skin and the squamous epithelia of the mucous membranes with varying degree of keratinocyte (squamous cell) differentiation. Etiologic risk factors for SCCs include ultraviolet light, PV infection, bracken fern ingestion, and carcinogens in tobacco, coal tar, soot, arsenic, and smegma (Brown et al. 2007). There has been a marked increase in the incidence of human SCC over the last 50 yr, with UV light representing the most important risk factor (Dal et al. 2008), and PV infection as a possible cofactor (Munday and Kiupel
115
2010). To our knowledge SCC has not been previously reported in red deer. However, SCC has been reported in other Cervidae, including the skin of the front leg of an 18-yr-old female Pe`re David’s deer (Elaphurus davidianus; Agrimi et al. 1993) and the skin of the front leg with metastasis to the ipsilateral prescapular lymph node and lungs of a 9-yr-old female Indochina sika deer (Cervus nippon pseudaxis; Ensley et al. 1980). In addition, an oronasal SCC with metastasis to the ipsilateral retropharyngeal lymph node was described in a 3.5-yr-old white-tailed deer (Odocoileus virginianus; Stroud and Amundson 1983). Although SCCs of the oropharynx, esophagus, and forestomachs of cattle are rare, they are relatively common in certain geographic locations in England, Scotland, Brazil, and Bolivia. Suspected causes for this regional disparity include BPV4 infection and bracken fern ingestion (Brown et al. 2007). There is growing evidence that PVs are involved in the pathogenesis of SCCs in multiple species including humans, cats (Felis catus), dogs (Canis lupus familiaris), sheep (Ovis aries), rabbits (Sylvilagus floridanus and Oryctolagus cuniculus), western barred bandicoots (Perameles bougainville), Natal multimammate mice (Mastomys natalensis; Munday and Kiupel 2010), a ferret (Mustela putorius furo; Rodrigues et al. 2010), and horses (Equus ferus caballus; Knight et al. 2011). No cytopathic evidence of PV infection and no PV antigen or DNA were detectable in our case. This does not, however, rule out the possibility that PVs can be involved in the induction of SCCs in red deer, because PV-induced neoplastic transformation is often associated with restricted and nonproductive infection that may not be detectable in all cases (Teifke et al. 2003; Munday and Kiupel 2010; Knight et al. 2011). Many well-differentiated SCCs display formation of concentric lamellae of keratin (keratin pearls). In contrast, many poorly differentiated tumors, such as our case, only show keratinization of
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individual cells (Goldschmidt and Hendrick 2002). Immunohistochemistry for cytoskeletal intermediate filaments like cytokeratin and vimentin are commonly applied tools for the identification of the histogenetic origin of poorly differentiated tumors (Ulrich et al. 2009). Cytokeratin immunoreactivity of the neoplastic epithelial cells in the oral mass and lymph node metastasis prove the epithelial histogenesis of this tumor (Erdelyi et al. 2009). Continuous wildlife disease monitoring and documentation through published reports is essential to help identify environmental hazard-induced (e.g., radiation, carcinogens, and toxins) increases in disease frequencies among exposed sentinel species. We thank Gu¨nter Schro¨der, Enercity Forestry Office, Wedemark for submission of this case. LITERATURE CITED Agrimi U, Morelli L, Di Guardo G. 1993. Squamous cell carcinoma of the skin in a Pe`re David’s deer (Elaphurus davidianus). J Wildl Dis 29:616–617. Azorit C, Munoz-Cobo J, Hervas J, Analla M. 2004. Aging through growth marks in teeth of Spanish red deer. Wildl Soc Bull 32:702–710. Boch J, Schneidawind H. 1988. Rotwild (Cervus elaphus L.). In: Krankheiten des jagdbaren Wildes, Boch J and Schneidawind H (eds.). Paul Parey, Hamburg, Germany, pp. 20–63. Brown CC, Baker DC, Barker IK. 2007. Alimentary system. In: Jubb, Kennedy, and Palmer’s pathology of domestic animals. 5th Ed, Maxie MG (ed.). Elsevier, Edinburgh, Great Britain, pp. 3–296. Dal H, Boldemann C, Lindelof B. 2008. Trends during a half century in relative squamous cell carcinoma distribution by body site in the Swedish population: Support for accumulated sun exposure as the main risk factor. J Dermatol 35:55–62. Ensley PK, Janssen DL, Anderson MP. 1980. Squamous cell carcinoma in an Indochina sika deer. J Am Vet Med Assoc 177:932. Erdelyi K, Gal J, Sugar L, Ursu K, Forgach P, Szeredi L, Steineck T. 2009. Papillomavirusassociated fibropapillomas of red deer (Cervus elaphus). Acta Vet Hung 57:337–344. Goldschmidt MH, Hendrick MJ. 2002. Tumors of the skin and soft tissues. In: Tumors in domestic animals, Meuten DJ (ed.). Iowa State Press, Ames, Iowa, pp. 45–118.
Gregoire F, Mousset B, Hanrez D, Cassart D, Desmecht D, Linden A. 2008. Cavernous haemangiosarcoma in a free-living red deer (Cervus elaphus). Vet Rec 162:692–693. Hofle U, Vicente J, Gortazar C. 2004. Bilateral ovarian teratoma in a free-living Iberian red deer (Cervus elaphus hispanicus). N Z Vet J 52:44–45. Klupp BG, Granzow H, Mettenleiter TC. 2000. Primary envelopment of pseudorabies virus at the nuclear membrane requires the UL34 gene product. J Virol 74:10063–10073. Knight CG, Munday JS, Peters J, Dunowska M. 2011. Equine penile squamous cell carcinomas are associated with the presence of equine papillomavirus type 2 DNA sequences. Vet Pathol 48:1190–1194. Ludt CJ, Schroeder W, Rottmann O, Kuehn R. 2004. Mitochondrial DNA phylogeography of red deer (Cervus elaphus). Mol Phylogenet Evol 31:1064– 1083. Munday JS, Kiupel M. 2010. Papillomavirus-associated cutaneous neoplasia in mammals. Vet Pathol 47:254–264. Perez J, de las Mulas JM, Arenas A, Luque I, Carrasco L. 1998. Malignant schwannoma in a red deer (Cervus elaphus). Vet Rec 143:585–587. Peters M, Wohlsein P. 2008. Anaplastic oligodendroglioma with meningeal infiltration in a freeranging red deer (Cervus elaphus). J Comp Pathol 138:59–62. Rodrigues A, Gates L, Payne HR, Kiupel M, Mansell J. 2010. Multicentric squamous cell carcinoma in situ associated with papillomavirus in a ferret. Vet Pathol 47:964–968. Scandrett B, Wobeser G. 2004. Malignant melanoma in a captive red deer (Cervus elaphus elaphus). J Wildl Dis 40:808–810. Stroud RK, Amundson TE. 1983. Squamous cell carcinoma in a free-ranging white-tailed deer (Odocoileus virginianus). J Wildl Dis 19:162– 164. Teifke JP, Kidney BA, Lohr CV, Yager JA. 2003. Detection of papillomavirus-DNA in mesenchymal tumour cells and not in the hyperplastic epithelium of feline sarcoids. Vet Dermatol 14:47–56. Ulrich R, Eydner M, Gru¨n A, Haydn J, Baumga¨rtner W. 2009. A biphasic malignant mesothelioma of the peritoneum and pleura in a horse. Dtsch Tiera¨rztl Wochenschr 116:186–191. Zele D, Gombac M, Svara T, Vengust G. 2011. A case of hepatic carcinoid in a red deer hind (Cervus elaphus). Acta Vet Hung 59:319–325.
Submitted for publication 22 March 2012. Accepted 3 June 2013.
