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Diagnostic Challenge
DIAGNOSTIC CHALLENGE
FIGURE 1. Dwarf hamster presented with a growth on left foot.
Journal of Exotic Pet Medicine 22 (2013), pp 85– 89
History A 1-year-old, intact, 57-g, male dwarf hamster (Phodopus sungorus) was presented to a veterinary teaching hospital with a 3-week history of a 0.5 ⫻ 1– cm mass located on the dorsal aspect of the left foot (Fig. 1). The hamster was housed in a commercial wire cage with a plastic hide box, cotton nesting material and an exercise wheel. The animal was fed a diet consisting of commercial pellets, mixed seeds, hay, and vegetables and had free access to water. On physical examination, the animal was bright and alert and there were no other external abnormalities noted. At this time, please evaluate the history, physical examination, and clinical presentation (Fig. 1). From the preliminary information, develop a differential disease diagnosis list and plan for additional diagnostics and treatment.
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FIGURE 2. Dwarf hamster prepared for surgery to remove growth.
DIAGNOSIS The initial differential diagnoses for this case were bacterial abscess, follicular cyst, epidermal neoplasia, or follicular neoplasia. A Romanowsky-type stain– cytology study of a fineneedle aspiration sample showed the presence of keratinized squamous cells and what appeared to be a group of glandular epithelial cells. The suspect glandular epithelial cells were likely sebaceous gland in origin. Therefore the top differential diagnoses after cytologic evaluation were follicular cyst and neoplasia. The owners agreed to the recommendation of surgical removal of the mass. The hamster was hospitalized. The initial treatment plan included enrofloxacin (10 mg/kg orally every 12 hours) (Baytril 2.5%; Bayer, Shawnee Mission, KS USA) and ibuprofen (10 mg/kg orally every 12 hours) (Dalsy; Abbott Labs, Madrid, Spain). Surgery was performed the following day. The patient was premedicated with buprenorphine (0.1 mg/kg subcutaneously) (Buprex injectable, 0.3 mg; Schering-Plough, Madrid, Spain) for analgesia and midazolam (0.5 mg/kg subcutaneously) (Dormicum injectable solution, 15 mg/3 mL; Roche, Nutley, NJ USA). General anesthesia was induced and maintained with 5% and 1% to 3% isoflurane, respectively, and supported with oxygen therapy directly to the nose with an Ayre’s T-piece breathing circuit maintained in place with surgical tape. The animal was positioned over a heating pad and was surrounded with warm water gloves to prevent hypothermia (Fig. 2). The surgical site 8 6
was prepared with chlorhexidine scrub (Cristalmina 1%; Laboratorios Salvat, S.A.). The hamster was positioned in sternal recumbency and covered with a clear drape. Cardiovascular monitoring of the patient was accomplished with an ultrasound blood detector (Vet BP Doppler; Mano Medical, Warsaw, Poland), whereas his respiratory rate was visually monitored. Ophthalmic surgical instruments and a binocular magnification loupe were used by the surgeon during the surgical procedure. For complete removal of the mass, an initial incision was made over the lesion so that the skin could be dissected away from the tissue growth. Hemostasis was performed with mosquito forceps and a monopolar electrocautery (Micromed MDIII; Micromed, Tuttlingen, Germany) (Fig. 3). The mass was dissected from the dorsal aspect of the foot at its base, with care taken to avoid damaging nearby soft-tissue structures that included the cranial tibial muscle, the tendon of the long digital extensor muscle, the tendon of the long peroneal muscle, the fourth common dorsal digital vein (branch of lateral saphenous vein), the cranial branch of the saphenous artery, and the common peroneal nerve. After the tissue growth was removed, the skin was closed in a continuous suture pattern with 4-0 polyglactin 910 (Vicryl; Ethicon, Somerville, NJ USA) (Fig. 4). Once the mass was excised, it was placed in formalin and submitted for histopathologic examination. Postsurgical therapy consisted of tramadol (5 mg/kg orally every 12 hours) (Adolonta Gotas; Grünenthal Pharma, Madrid, Spain) and sulfamethoxazole-trimethoprim (30 mg/kg orally every 12 hours) (Septrin Pediátrico; Medeva Pharma, Madrid, Spain), both administered for 7 days. In addition, a bandage was applied over the surgical site to prevent postsurgical automutilation. Histopathologic examination of the suspect tissue showed a well-circumscribed, non-encapsulated dermal mass. This mass was composed of multiple accumulations of tumor epithelial cells and cystic cavities with an abundance of keratin (Fig. 5). The epithelial aggregates were predominantly composed of basaloid cells that had prominent peripheral palisading, similar to matricial cells of follicular bulbs. Although the growth was determined not to be invasive, neoplastic cells were observed at the tissue borders. This confirmed that the final diagnosis was a trichoepithelioma. Two days after the surgical procedure, the animal automutilated the left dis-
Martorell and Melero/Journal of Exotic Pet Medicine 22 (2013), pp 85– 89
tal limb. Subsequently, the affected limb was amputated. The hamster recovered well from the amputation surgery, and there was no recurrence of the tumor. DISCUSSION The most likely disease differential diagnoses in this case upon patient presentation were bacterial abscess, pseudomycetoma, follicular cyst, and epidermal or follicular neoplasia. Bacterial abscesses and pseudomycetomas are predisposed by injury or trauma, bite wounds, rough or dirty bedding, foreign bodies, and parasites. Bacterial abscesses often appear in hamsters as localized, soft to firm, usually nonpainful swellings that contain a thick and caseous exudate. Pyrexia, anorexia, and depression are clinical signs in rodents that are often associated with abscesses and pseudomycetomas.1,2 The most common bacterial organisms isolated from these lesions in rodents include Pasteurella pneumotropica, Staphylococcus dermatitis, and Staphylococcus aureus, but others have also been identified (e.g., Streptococcus spp, Actinomyces bovis, and Mycobacterium spp).1,2 Bacterial or fungal infections were ruled out because the cytologic evaluation of the fineneedle aspirate sample harvested from the mass did not contain caseous exudate or any bacterial or fungal organisms. Consequently, an excisional biopsy was performed to reach a final diagnosis. The most common skin neoplasms reported in hamsters are highly metastatic melanomas (melanotic or amelanotic) and melanocytomas, with a higher incidence in male hamsters and often localized in the head, back, and flank gland.3-5 Another common skin neoplasm in hamster species is lymphoma. There are 3 recognized forms of lymphoma that have been diagnosed in hamsters: multicentric, epitheliotropic, and epizootic.3 Epitheliotropic lymphoma is an uncommon progressive disease characterized by neoplastic infiltration of the epidermis and adnexal structures.6 Epitheliotropic neoplasms are divided into the classic nodular form, or mycosis fungoides (human epidermotropic T-cell lymphoma), and pagetoid reticulosis.6 The clinical signs of epitheliotropic neoplasms include patchy alopecia, pruritus, exfoliative erythroderma, lethargy, anorexia, and weight loss.3,5,6 This neoplasm has also been described in guinea pigs.3,5,6 There is no treatment, and affected animals are usually euthanized.3,5,6 Other epidermal neo-
FIGURE 3. Monopolar electrocautery was used for hemostasis during surgery.
FIGURE 4. Surgical site after removal of tissue mass.
Martorell and Melero/Journal of Exotic Pet Medicine 22 (2013), pp 85– 89
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cally in Syrian hamsters.3,5 The HaPV infection can be subclinical. In older infected animals, a cutaneous form of HaPV is occasionally diagnosed, with affected animals being presented with keratinizing skin tumors of the hair follicles (epitheliomas) that primarily involve the face and feet.3,5 In naive breeding groups, when the virus is first introduced, it results in epizootic lymphoma among young hamsters.3,5 The virus is highly contagious, being spread by urine, and very resistant in the environment; moreover, it may result in a high mortality rate during an epizootic outbreak.3,5 HaPV is controlled by depopulation and good hygiene practices. In this case there was no evidence of HaPV infection based on histopathologic results of the tissue mass and patient response to treatment. This case was submitted by Jaime Martorell, DVM, PhD, Dip ECZM (small mammal) and Adria Melero, DVM, from the Departament de Medicina i Cirurgia Animals, Servei de Clínica d’Animals Exòtics, Hospital Clínic Veterinari Facultat de Veterinària, UAB, 08193 Barcelona, Spain. ACKNOWLEDGMENTS The author thanks Dr A. Ramis from the Servei de Diagnòstic de Patologia Veterinària de la Facultat de Veterinaria de la UAB for collaboration in the diagnostic process. © 2013 Elsevier Inc. All rights reserved. 1557-5063/13/2201-$30.00 http://dx.doi.org/10.1053/j.jepm.2012.12.014
FIGURE 5. Histology (hematoxylin-eosin staining) of excised foot mass. (A) The mass was composed of multiple accumulations of epithelial tumor cells and cystic cavities with an abundance of keratin (arrows). (B) Magnification of A.
plasms described in the hamster are papillomas and squamous cell carcinomas; these often affect the cheek pouch or the ear.4,7,8 In this case the histopathologic diagnosis was a trichoepithelioma, a benign neoplasm. This type of tumor typically originates in the hair follicle, develops as a round to ovoid dermal mass, and does not metastasize; in dogs these tumors are very small, usually less than 2 cm.9 Frequently, trichoepitheliomas have a similar clinical appearance to other neoplasms such as trichofolliculoma, keratoacanthoma, or tricholemmoma.9 Trichoepithelioma has also been described in guinea pigs and rabbits.7,10,11 Epithelioma/trichoepithelioma has been related to hamster polyomavirus (HaPV), specifi8 8
REFERENCES 1. Hoppmann E, Wilson H: Rodent dermatology. J Exot Pet Med 16:238-255, 2007 2. Martorell J, Gallifa N, Fondevila D, et al: Bacterial pseudomycetoma in dwarf hamster, Phodopus sungorus. Vet Dermatol 17:449-452, 2006 3. Donnelly TM: Disease problems of small rodents, in Quesenberry KE, Carpenter JW (eds): Ferrets, Rabbits, and Rodents. St Louis, MO, Elsevier/WB Saunders (ed 2), pp 299-315, 2004 4. Martorell J, Martínez A, Soto S: Complete ablation of vertical auditive conduct and ear pinna in a dwarf hamster (Phodopus sungorus) with an aural spontaneous squamous cell carcinoma. J Exot Pet Med 19:96-100, 2010 5. Orr H: Rodents: neoplastic and endocrine disease, in Keeble E, Meredith A (eds): BSAVA Manual of Rodents and Ferrets. Gloucester, UK, BSAVA, pp 181-192, 2009 6. Martorell J, Such R, Fondevila D, et al: Cutaneous epitheliotropic T-cell lymphoma with systemic spread in a
Martorell and Melero/Journal of Exotic Pet Medicine 22 (2013), pp 85– 89
guinea pig (Cavia porcellus). J Exot Pet Med 20:313-317, 2011 7. Garner MM: Cytologic diagnosis of diseases of rabbits, guinea pigs, and rodents. Vet Clin North Am Exot Anim Pract 10:25-49, 2007 8. Martorell J, Fondevila D, Ramis A: Spontaneous squamous cell carcinoma of the cheek pouch in two dwarf hamsters (Phodopus sungorus). Vet Rec 156:650-651, 2005
9. Medleau L, Hnilica KA: Neoplastic and nonneoplastic tumors, in Small Animal Dermatology: a Color Atlas and Therapeutic Guide. St Louis, MO, Elsevier/W. B. Saunders (ed 2), pp 393-448, 2006 10. Greenacre CB: Spontaneous tumors of small mammals. Vet Clin North Am Exot Anim Pract 7:627-651, 2004 11. Heatley JJ, Smith AN: Spontaneous neoplasms of lagomorphs. Vet Clin North Am Exot Anim Pract 7:561-577, 2004
Martorell and Melero/Journal of Exotic Pet Medicine 22 (2013), p 85– 89
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FIGURE 1. Dwarf hamster presented with a growth on left foot.
Journal of Exotic Pet Medicine 22 (2013), pp 85– 89
History A 1-year-old, intact, 57-g, male dwarf hamster (Phodopus sungorus) was presented to a veterinary teaching hospital with a 3-week history of a 0.5 ⫻ 1– cm mass located on the dorsal aspect of the left foot (Fig. 1). The hamster was housed in a commercial wire cage with a plastic hide box, cotton nesting material and an exercise wheel. The animal was fed a diet consisting of commercial pellets, mixed seeds, hay, and vegetables and had free access to water. On physical examination, the animal was bright and alert and there were no other external abnormalities noted. At this time, please evaluate the history, physical examination, and clinical presentation (Fig. 1). From the preliminary information, develop a differential disease diagnosis list and plan for additional diagnostics and treatment.
8 5
FIGURE 2. Dwarf hamster prepared for surgery to remove growth.
DIAGNOSIS The initial differential diagnoses for this case were bacterial abscess, follicular cyst, epidermal neoplasia, or follicular neoplasia. A Romanowsky-type stain– cytology study of a fineneedle aspiration sample showed the presence of keratinized squamous cells and what appeared to be a group of glandular epithelial cells. The suspect glandular epithelial cells were likely sebaceous gland in origin. Therefore the top differential diagnoses after cytologic evaluation were follicular cyst and neoplasia. The owners agreed to the recommendation of surgical removal of the mass. The hamster was hospitalized. The initial treatment plan included enrofloxacin (10 mg/kg orally every 12 hours) (Baytril 2.5%; Bayer, Shawnee Mission, KS USA) and ibuprofen (10 mg/kg orally every 12 hours) (Dalsy; Abbott Labs, Madrid, Spain). Surgery was performed the following day. The patient was premedicated with buprenorphine (0.1 mg/kg subcutaneously) (Buprex injectable, 0.3 mg; Schering-Plough, Madrid, Spain) for analgesia and midazolam (0.5 mg/kg subcutaneously) (Dormicum injectable solution, 15 mg/3 mL; Roche, Nutley, NJ USA). General anesthesia was induced and maintained with 5% and 1% to 3% isoflurane, respectively, and supported with oxygen therapy directly to the nose with an Ayre’s T-piece breathing circuit maintained in place with surgical tape. The animal was positioned over a heating pad and was surrounded with warm water gloves to prevent hypothermia (Fig. 2). The surgical site 8 6
was prepared with chlorhexidine scrub (Cristalmina 1%; Laboratorios Salvat, S.A.). The hamster was positioned in sternal recumbency and covered with a clear drape. Cardiovascular monitoring of the patient was accomplished with an ultrasound blood detector (Vet BP Doppler; Mano Medical, Warsaw, Poland), whereas his respiratory rate was visually monitored. Ophthalmic surgical instruments and a binocular magnification loupe were used by the surgeon during the surgical procedure. For complete removal of the mass, an initial incision was made over the lesion so that the skin could be dissected away from the tissue growth. Hemostasis was performed with mosquito forceps and a monopolar electrocautery (Micromed MDIII; Micromed, Tuttlingen, Germany) (Fig. 3). The mass was dissected from the dorsal aspect of the foot at its base, with care taken to avoid damaging nearby soft-tissue structures that included the cranial tibial muscle, the tendon of the long digital extensor muscle, the tendon of the long peroneal muscle, the fourth common dorsal digital vein (branch of lateral saphenous vein), the cranial branch of the saphenous artery, and the common peroneal nerve. After the tissue growth was removed, the skin was closed in a continuous suture pattern with 4-0 polyglactin 910 (Vicryl; Ethicon, Somerville, NJ USA) (Fig. 4). Once the mass was excised, it was placed in formalin and submitted for histopathologic examination. Postsurgical therapy consisted of tramadol (5 mg/kg orally every 12 hours) (Adolonta Gotas; Grünenthal Pharma, Madrid, Spain) and sulfamethoxazole-trimethoprim (30 mg/kg orally every 12 hours) (Septrin Pediátrico; Medeva Pharma, Madrid, Spain), both administered for 7 days. In addition, a bandage was applied over the surgical site to prevent postsurgical automutilation. Histopathologic examination of the suspect tissue showed a well-circumscribed, non-encapsulated dermal mass. This mass was composed of multiple accumulations of tumor epithelial cells and cystic cavities with an abundance of keratin (Fig. 5). The epithelial aggregates were predominantly composed of basaloid cells that had prominent peripheral palisading, similar to matricial cells of follicular bulbs. Although the growth was determined not to be invasive, neoplastic cells were observed at the tissue borders. This confirmed that the final diagnosis was a trichoepithelioma. Two days after the surgical procedure, the animal automutilated the left dis-
Martorell and Melero/Journal of Exotic Pet Medicine 22 (2013), pp 85– 89
tal limb. Subsequently, the affected limb was amputated. The hamster recovered well from the amputation surgery, and there was no recurrence of the tumor. DISCUSSION The most likely disease differential diagnoses in this case upon patient presentation were bacterial abscess, pseudomycetoma, follicular cyst, and epidermal or follicular neoplasia. Bacterial abscesses and pseudomycetomas are predisposed by injury or trauma, bite wounds, rough or dirty bedding, foreign bodies, and parasites. Bacterial abscesses often appear in hamsters as localized, soft to firm, usually nonpainful swellings that contain a thick and caseous exudate. Pyrexia, anorexia, and depression are clinical signs in rodents that are often associated with abscesses and pseudomycetomas.1,2 The most common bacterial organisms isolated from these lesions in rodents include Pasteurella pneumotropica, Staphylococcus dermatitis, and Staphylococcus aureus, but others have also been identified (e.g., Streptococcus spp, Actinomyces bovis, and Mycobacterium spp).1,2 Bacterial or fungal infections were ruled out because the cytologic evaluation of the fineneedle aspirate sample harvested from the mass did not contain caseous exudate or any bacterial or fungal organisms. Consequently, an excisional biopsy was performed to reach a final diagnosis. The most common skin neoplasms reported in hamsters are highly metastatic melanomas (melanotic or amelanotic) and melanocytomas, with a higher incidence in male hamsters and often localized in the head, back, and flank gland.3-5 Another common skin neoplasm in hamster species is lymphoma. There are 3 recognized forms of lymphoma that have been diagnosed in hamsters: multicentric, epitheliotropic, and epizootic.3 Epitheliotropic lymphoma is an uncommon progressive disease characterized by neoplastic infiltration of the epidermis and adnexal structures.6 Epitheliotropic neoplasms are divided into the classic nodular form, or mycosis fungoides (human epidermotropic T-cell lymphoma), and pagetoid reticulosis.6 The clinical signs of epitheliotropic neoplasms include patchy alopecia, pruritus, exfoliative erythroderma, lethargy, anorexia, and weight loss.3,5,6 This neoplasm has also been described in guinea pigs.3,5,6 There is no treatment, and affected animals are usually euthanized.3,5,6 Other epidermal neo-
FIGURE 3. Monopolar electrocautery was used for hemostasis during surgery.
FIGURE 4. Surgical site after removal of tissue mass.
Martorell and Melero/Journal of Exotic Pet Medicine 22 (2013), pp 85– 89
8 7
cally in Syrian hamsters.3,5 The HaPV infection can be subclinical. In older infected animals, a cutaneous form of HaPV is occasionally diagnosed, with affected animals being presented with keratinizing skin tumors of the hair follicles (epitheliomas) that primarily involve the face and feet.3,5 In naive breeding groups, when the virus is first introduced, it results in epizootic lymphoma among young hamsters.3,5 The virus is highly contagious, being spread by urine, and very resistant in the environment; moreover, it may result in a high mortality rate during an epizootic outbreak.3,5 HaPV is controlled by depopulation and good hygiene practices. In this case there was no evidence of HaPV infection based on histopathologic results of the tissue mass and patient response to treatment. This case was submitted by Jaime Martorell, DVM, PhD, Dip ECZM (small mammal) and Adria Melero, DVM, from the Departament de Medicina i Cirurgia Animals, Servei de Clínica d’Animals Exòtics, Hospital Clínic Veterinari Facultat de Veterinària, UAB, 08193 Barcelona, Spain. ACKNOWLEDGMENTS The author thanks Dr A. Ramis from the Servei de Diagnòstic de Patologia Veterinària de la Facultat de Veterinaria de la UAB for collaboration in the diagnostic process. © 2013 Elsevier Inc. All rights reserved. 1557-5063/13/2201-$30.00 http://dx.doi.org/10.1053/j.jepm.2012.12.014
FIGURE 5. Histology (hematoxylin-eosin staining) of excised foot mass. (A) The mass was composed of multiple accumulations of epithelial tumor cells and cystic cavities with an abundance of keratin (arrows). (B) Magnification of A.
plasms described in the hamster are papillomas and squamous cell carcinomas; these often affect the cheek pouch or the ear.4,7,8 In this case the histopathologic diagnosis was a trichoepithelioma, a benign neoplasm. This type of tumor typically originates in the hair follicle, develops as a round to ovoid dermal mass, and does not metastasize; in dogs these tumors are very small, usually less than 2 cm.9 Frequently, trichoepitheliomas have a similar clinical appearance to other neoplasms such as trichofolliculoma, keratoacanthoma, or tricholemmoma.9 Trichoepithelioma has also been described in guinea pigs and rabbits.7,10,11 Epithelioma/trichoepithelioma has been related to hamster polyomavirus (HaPV), specifi8 8
REFERENCES 1. Hoppmann E, Wilson H: Rodent dermatology. J Exot Pet Med 16:238-255, 2007 2. Martorell J, Gallifa N, Fondevila D, et al: Bacterial pseudomycetoma in dwarf hamster, Phodopus sungorus. Vet Dermatol 17:449-452, 2006 3. Donnelly TM: Disease problems of small rodents, in Quesenberry KE, Carpenter JW (eds): Ferrets, Rabbits, and Rodents. St Louis, MO, Elsevier/WB Saunders (ed 2), pp 299-315, 2004 4. Martorell J, Martínez A, Soto S: Complete ablation of vertical auditive conduct and ear pinna in a dwarf hamster (Phodopus sungorus) with an aural spontaneous squamous cell carcinoma. J Exot Pet Med 19:96-100, 2010 5. Orr H: Rodents: neoplastic and endocrine disease, in Keeble E, Meredith A (eds): BSAVA Manual of Rodents and Ferrets. Gloucester, UK, BSAVA, pp 181-192, 2009 6. Martorell J, Such R, Fondevila D, et al: Cutaneous epitheliotropic T-cell lymphoma with systemic spread in a
Martorell and Melero/Journal of Exotic Pet Medicine 22 (2013), pp 85– 89
guinea pig (Cavia porcellus). J Exot Pet Med 20:313-317, 2011 7. Garner MM: Cytologic diagnosis of diseases of rabbits, guinea pigs, and rodents. Vet Clin North Am Exot Anim Pract 10:25-49, 2007 8. Martorell J, Fondevila D, Ramis A: Spontaneous squamous cell carcinoma of the cheek pouch in two dwarf hamsters (Phodopus sungorus). Vet Rec 156:650-651, 2005
9. Medleau L, Hnilica KA: Neoplastic and nonneoplastic tumors, in Small Animal Dermatology: a Color Atlas and Therapeutic Guide. St Louis, MO, Elsevier/W. B. Saunders (ed 2), pp 393-448, 2006 10. Greenacre CB: Spontaneous tumors of small mammals. Vet Clin North Am Exot Anim Pract 7:627-651, 2004 11. Heatley JJ, Smith AN: Spontaneous neoplasms of lagomorphs. Vet Clin North Am Exot Anim Pract 7:561-577, 2004
Martorell and Melero/Journal of Exotic Pet Medicine 22 (2013), p 85– 89
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