History
A 9-year-old 18-kg (39.6-lb) castrated male mixed-breed dog that had been euthanized was submitted to the applied pathology service at The Ohio State University for necropsy. The owner reported that the dog had had an unspecified hair follicle neoplasm in the neck > 2 years prior to euthanasia. The mass was removed along with a regional lymph node. Four months prior to euthanasia, the dog became lame in the right hind limb. One week prior to euthanasia, a new neck mass was noted by the owner in the same location as the first neck mass.
Clinical and Gross Findings
On dissection, an encapsulated 2.0-cm-diameter white firm dermal mass was noted on the lateral aspect of the right side of the neck. The right tibial metaphysis was markedly swollen on palpation; sectioning revealed 2 firm, white masses (4.0 and 5.0 cm in diameter) that effaced the tibial cortex and medulla. All lobes of the lungs contained dozens of firm, raised, white masses ranging from 0.2 to 2.0 cm in diameter (Figure 1). Within the left atrial endocardium, there was a firm, raised, pedunculated, 3.0-cm-diameter, multinodular, red mass. The left kidney was approximately 1.5 times the size of the right kidney and was effaced by firm, white tissue; the renal pelvis was markedly dilated. The renal mass extended into the ureter and invaded the caudal vena cava. The right kidney was considered normal in size and contained a firm, well-demarcated, 0.5-cm-diameter, white mass. The mesentery contained approximately 10 to 15 firm, white masses ranging from 0.2 to 1.5 cm in diameter.
Photographs of the lungs (A), left atrium (B), and left kidney (C) from a dog that had been euthanized > 2 years after excision of an unspecified hair follicle neoplasm. Right hind limb lameness had developed 4 months prior to euthanasia, and a new neck mass was detected in the same location as the first neck mass 1 week prior to euthanasia. All lung lobes contained dozens of firm, raised, tan masses ranging from 0.2 to 2.0 cm in diameter. In the left atrium, there was a firm, pedunculated, red mass originating from the endocardium. The renal cortex and pelvis of the left kidney were infiltrated by a firm, tan mass with secondary hydronephrosis.
Citation: Journal of the American Veterinary Medical Association 249, 6; 10.2460/javma.249.6.607
Formulate differential diagnoses from the history, clinical findings, and Figure 1—then turn the page→
Histopathologic Findings
Sections of skin, lungs, left atrium (Figure 2), kidneys, and bones were evaluated histologically. In all tissues, the masses were morphologically similar. The masses were well-demarcated, unencapsulated, densely cellular, and composed of neoplastic epithelial cells arranged in nests and anastomosing streams on a fine fibrovascular stroma. The neoplastic population was characterized by polygonal cells with indistinct cell borders, moderate amounts of eosinophilic cytoplasm, and a central large round to oval nucleus with fine stippled chromatin and prominent nucleoli. There was moderate anisocytosis and anisokaryosis with frequent apoptotic cells and approximately 5 to 10 mitotic figures/ten 400× fields.
Photomicrographs of sections of the mass in the left atrium and lung tissue from the dog in Figure 1. A—In a subgross image of a cross-section of the pedunculated pilomatricoma arising from left atrial wall (asterisk), notice the unique outgrowth of the mass from the endocardial surface. H&E stain; bar = 1 cm. B—In a section of lung tissue, abrupt transition to a large mass of keratinized ghost cells (asterisk) is present. H&E stain; bar = 90 μm. C—In another section of lung tissue, there is evidence of osseous metaplasia (asterisk); H&E stain; bar = 90 μm.
Citation: Journal of the American Veterinary Medical Association 249, 6; 10.2460/javma.249.6.607
In all tissue sections, large areas of coagulation necrosis within the masses were evident. There were frequent areas of abrupt keratinization by the neoplastic cells as well as many keratinized ghost cells (Figure 2). Osseous metaplasia was also noted. Frequently within and surrounding the masses was an abundant desmoplastic stroma.
Morphologic Diagnosis and Case Summary
Morphologic diagnosis: malignant pilomatricoma (pilomatrix carcinoma).
Case summary: rare case of metastasis of a pilomatricoma to multiple sites including lungs, left atrium, kidneys, and bone in a middle-aged dog.
Comments
The case described in the present report involved a 9-year-old mixed-breed dog that had previously had a hair follicle tumor, which was removed but then recurred with metastasis to multiple sites. The cervical dermal mass as well as the masses in the lungs, heart, kidneys, and right tibia was histologically consistent with a malignant pilomatricoma, a malignant follicular tumor. Compared with its benign counterpart that accounts for 1% to 3% of epithelial tumors in dogs, malignant pilomatricoma is extremely rare. Malignancy is characterized clinically by erratic or rapid growth and histologically by pronounced nuclear pleomorphism, anaplasia, infiltrative growth, and mitotic activity.1 These aggressive tumors typically invade deep into the subcutis and may incite a desmoplastic response,2 as occurred in the dog of this report. The classification of malignancy is also based on lymphatic invasion, local invasion of underlying bone, and distant metastasis.3
Malignant pilomatricomas are typically alopecic and frequently appear as ulcerated masses in the skin of the neck, dorsal aspect of the trunk, or tail.3 Among affected dogs, there is a wide range of ages, with 6 years being the median age.1,3 It has been suggested that breeds with continuous hair growth have higher susceptibility to follicular tumors because of the greater mitotic activity of their hair follicles.1,2,4 Some previously reported cases of malignant pilomatricomas in dogs describe distant metastases to bones and lungs.1,4 Local recurrence is the most common feature of malignancy. In people with malignant pilomatricomas, local recurrence occurs in approximately half of cases, with a 16% incidence of metastases.5
Histologically, malignant pilomatricomas are dermal neoplasms that extend to the subcutis and are composed of basaloid matrical epithelial cells arranged in anastomosing islands and trabeculae.3 There is often a moderate desmoplastic stroma, which may contain an inflammatory infiltrate. Occasionally, a granulomatous foreign-body type reaction to keratinized ghost cells develops. Metastasis occurs via the lymphatics to regional lymph nodes and lungs.2 Differential diagnoses based on gross and histologic appearance of malignant pilomatricoma include trichoepithelioma and basal cell carcinoma. Distinction of malignant pilomatricomas from malignant trichoepitheliomas can be difficult and is based on the larger epithelial aggregates, atypical matrical cells, and larger zones of ghost cells that are more characteristic of malignant pilomatricomas.3 In addition, ossification is not a feature of trichoepithelioma. Keratinizing basal cell carcinoma typically has a superficial architecture with a greater degree of connection to the epidermis.3
In a compilation of reported cases of malignant pilomatricomas in 12 dogs, there were 7 dogs with metastasis to the lungs, 6 dogs with metastasis to bones, 5 dogs with metastasis to lymph nodes, and 2 dogs with metastasis to other sites.1 In a case report4 published in 2013, the author described 9 previous reports of malignant pilomatricomas in dogs, with metastasis to the bones occurring most commonly. The dog of the present report had extensive and severe metastatic disease to multiple organs. Malignancy and metastasis of this type of tumor might be more common than previously reported cases have suggested.
References
1. Carroll EE, Fossey SL, Mangus LM, et al. Malignant pilomatricoma in 3 dogs. Vet Pathol 2010;47:937–943.
2. Goldschmidt MH, Hendrick MJ. Tumors of the skin and soft tissues. In: Meuten DJ, ed. Tumors in domestic animals. 4th ed. Ames, Iowa: Blackwell Publishing Co, 2002;61–63.
3. Gross TL, Ihrke PJ, Walder EJ, et al. Follicular tumors. In: Skin diseases of the dog and cat: clinical and histopathologic diagnosis. 2nd ed. Ames, Iowa: Blackwell Publishing Co, 2005; 624–625.
4. Martano M, Navas L, Meomartino L, et al. Malignant pilomatricoma with multiple bone metastases in a dog: histological and immunohistochemical study. Exp Ther Med 2013;5:1005–1008.
5. Hardisson D, Linares MD, Cuevas-Santos J, et al. Pilomatrix carcinoma: a clinicopathologic study of six cases and review of the literature. Am J Dermatopathol 2001;23:394–401.
