Vet Pathol 29:35 1-354 (1992)
BRIEF COMMUNICATIONS and CASE REPORTS Six Cases of Malignant Fibrous Histiocytoma of the Canine Spleen M. J. HENDRICK, J. J. BROOKS, AND E. H. BRUCE Key words: Dogs; malignant fibrous histiocytoma; spleen. Malignant fibrous histiocytoma (MFH) is the most common soft tissue sarcoma of human beings but has been described in dogs, cats, pigs, and rats only rarely.2.3,5,9J1,12 In human beings, MFH is an expansile tumor, usually involving the extremities or retroperitoneum. It may invade local tissues, and metastasis may occur to lung, lymph node, liver, and bone. In most reported animal cases, MFH has been described as a single, often invasive, soft tissue mass, usually in the limb^.^,^ Metastasis is only rarely reported. A report on spontaneous MFH in the forelimb of a rat described metastasis to lung and lymph node.5 There is one report of MFH involving the spleen, liver, and kidney of a pig.“ The largest nodule, 6 cm, was found in the spleen, which was presumed to be the primary site of origin of the neoplasm. One “fibrous histiocytoma” was mentioned briefly in a previous report on 57 nonlymphoid neoplasms of the canine spleen, but the lesion was not described in any detail.I2This report describes and classifies MFH of the canine spleen as a distinct clinicopathologic entity that should be recognized by veterinary pathologists. From June 1989 to July 1990, MFH was diagnosed in six canine spleens received by the biopsy service of the Laboratory of Pathology at the University of Pennsylvania, Philadelphia, Pennsylvania. The formalin-fixed specimens were routinely processed for histologic examination. Five-micrometer sections were cut from paraffin-embedded blocks and stained with hematoxylin and eosin. One section was stained with Giemsa. An avidin biotin immunoperoxidase complex technique was used, as previously described.6 Paraffin-embedded sections, 5 pm in thickness, were cut and carefully melted at 58-60 C. After deparaffinization and rehydration, slides were incubated in 0.3% H202in absolute methanol for 45 minutes. Sequential incubations in 20% normal goat serum (30 minutes), primary antiserum (1 hour at room temperature or overnight at 4 C), secondary biotinylated antibody (45 minutes), and avidin biotin complex reagent (45 minutes) followed. Sections were then exposed to the chromagen reaction solution (0.035°/o diaminobenzidine in 10 ml Tris buffer, filtered, and brought to 0.03% H202) for 5 minutes. Sections were counterstained in Mayer’s hematoxylin, dehydrated, cleared, and mounted. For certain antisera reactions (see below), sections were pretreated with a 0.1% solution of trypsin (Sigma Co., St. Louis, MO) in phosphate-buffered serum with 0.1 Yo CaCl for 30 minutes at 37 C. Sources of reagents and dilutions of antisera and modifi-
cations were as follows: avidin biotin reagents (Vector Laboratory System, Burlingame, CA); diaminobenzidine (Sigma Co.); antibody to cytokeratin (1/100, trypsinized, Lab Systems, Chicago, IL); desmin (1/450,2 hour room temperature, Dako, Santa Barbara, CA); vimentin (1/20, Dako); musclespecific actin (MSA, 1/4,000, Enzo, New York, NY);factor VIII antigen ( ~ 7 5 0 trypsinized, , Dako); SlOO antigen (11 1,000, Dako); a,-antichymotrypsin (ACT, 1/1,500, Dako); Leu M 1 (1/50, Becton-Dickinson, Rutherford, NJ); and leukocyte common antigen (LCA, 1/40, Dako). Both negative and substitution serum controls and positive tissue controls were employed. The signalment and immunohistochemical findings are listed in Table 1. There was no breed or sex predilection, but all dogs were between 9 and 14 years of age. The clinical history in each case was rather vague: lethargy, anorexia, and in most cases, a palpable splenic mass. One mass (case No. 5), was an incidental finding in a dog that had been euthanatized because of chronic renal failure. All masses were well circumscribed, white-grey, and multilobulated. Two of the five had reached a diameter > 15 cm. There was no gross evidence of involvement of any other organs or tissues. Histologically, all neoplasms were well circumscribed but unencapsulated. They were composed of a heterogeneous cell population that included rounded to polygonal histiocytoid cells, some of which were quite large with bizarre nuclei and prominent nucleoli, and spindled fibroblastic cells sometimes arranged in a storiform or fingerprint pattern. Lymphocytes, plasma cells, and eosinophils were found in all tumors but were prominent in four cases. Occasional large foamy “xanthoma” cells were seen. The relative percentages of these cells varied from tumor to tumor, but all tumors fit the classification scheme of MFH in human beings, as described by Enzinger and W e k 2No other specific morphologic patterns were identified in any of these tumors such as an alternating fascicular pattern or herringbone pattern, such as would be seen in a fibrosarcoma or leiomyosarcoma, or prominent cytoplasmic vacuolization, such as would be seen in liposarcoma. In one tumor (case No. 5), bizarre tumor giant cells dominated the histologic picture and inflammatory cells were only rarely seen. These were present against a background of fibroblastic cells, often arranged in a storiform pattern (Fig. 1). This pattern corresponded to the typical storiform/pleomorphic type of human MFH. In four tumors (case Nos. 1, 3, 4, and 6), there was a
35 1
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Vet Pathol 29(4), 1992
prominent inflammatory cell infiltrate (Fig. 2). The diagnosis of malignant fibrous histiocytoma was prompted by the presence of histiocytoid cells with nuclear enlargement, nuclear atypia, and atypical mitoses. Truly bizarre cells were widely scattered and partially concealed by the inflammatory infiltrate. A storiform pattern was usually inconspicuous or present only focally in these cases. Although these tumors could be considered equivalent to the “inflammatory” type of human MFH, neutrophils were scarce or absent; thus, they are more appropriately classified as subvariants of the stonform/ pleomorphic type with marked inflammation. One case (No. 2) had an unusual morphologic appearance (Fig. 3). Sheets of clear xanthomatous epithelioid cells were present and dissected by small capillaries in a manner reminiscent of renal cell carcinoma; however, the tumor was clearly confined to the spleen grossly, and no epithelial markers were present. The histologic appearance was somewhat similar to that of a rare variant of human MFH-the histiocytoid or epithelioid type with rounded histiocytoid cells in sheets without spindling.lJOThe clear cells feature sets this case apart and imparts an appearance perhaps restricted to the canine. Marker staining varied according to the histologic changes defined above (Table 1). In the four cases (Nos. 1, 3, 4, and 6) with the inflammatory component, the underlying spindled cells and the scattered larger pleomorphic cells showed strong staining for muscle-specific actin but only moderate desmin and weak vimentin staining. Muscle-specific actin was weaker in the highly pleomorphic case (but desmin was strong) and weak to absent in the xanthomatous case (No. 2). Four cases (Nos. 1,2, 3, and 5) contained weak and focal positivity for SlOO protein; none showed reactivity for aIantichymotrypsin, a common protein found in human MFH. All tumor cells were negative for cytokeratin (CAM 5.2), epithelial membrane antigen, factor VIII-related antigen, Leu M1, and leukocyte common antigen. The last two markers failed to stain the normal neutrophils and lymphocytes, respectively. Malignant fibrous histiocytoma in human beings has five major variants: storiform/pleomorphic, myxoid, giant cell, inflammatory, and angiomatoid.*This classification scheme is incomplete, and various morphologic types may be seen in any one tumor; therefore, tumors are usually classified by their predominant feature(s). Based on this paradigm, our canine splenic neoplasms have been classified as stonform/ pleomorphic (5/6; one typical and four with marked inflammation) and epithelioid/xanthomatous ( 1/6). The distinction between variants of MFH has some clinical significance in human beings in that the myxoid variant and tumors with
c
Fig. 1. Spleen; dog No. 5. Typical storiform/pleomorphic variant of malignant fibrous histiocytoma (MFH). Note the storiform arrangement of spindle cells with many large bizarre cells (arrows) and scattered inflammatory cells. HE. Bar = 50 fim.
Fig. 2. Spleen; dog No. 4. Storiform/pleomorphic vanant of MFH with marked inflammation. The field is dominated by lymphocytes mixed with mononuclear histiocytoid cells, a few of which have karyomegaly (arrow). HE. Bar = 50 fim. Fig. 3. Spleen; dog No. 2. Epithelioidxanthomatous variant. Note the clusters of large foamy “xanthoma” cells intermingled with lymphocytes. HE. Bar = 40 pm.
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Table 1. Signalment and immunohistochemical findings in six dogs with malignant fibrous histiocytomas of the spleen. Immunohistochemical results? Case No.
Sex*
Breed
Age (years)
1
Canaan
F/s
12
2
Cocker Spaniel
M/c
12
3
Irish Terrier
M
10
4
Mixed
F/s
9
5
Shetland Sheepdog
M/c
14
6
Terrier
F
14
* F/s = spayed female; M/c
=
Tumor Slassification L
Storiform/pleomorphic with inflammation Epithelioid/ xanthomatous Storiform/pleomorphic with inflammation Storiform/pleomorphic with inflammation Storiform/pleomorphic (typical) Storiform/pleomorphic with inflammation
castrated male.
t ... = negative staining; 2 = < 1% tumor cells staining; + = 2-10%
25-50% tumor cells staining;
++ + + = > 50% tumor cells staining.
marked inflammation have a slightly better prognosis than the storiform/pleomorphic variant.2 At present, the number of canine cases is too small to determine whether our classification scheme has any prognostic significance. The presence of muscle-specific actin, vimentin, and desmin in these tumors is consistent with a fibroblastic/myofibroblastic phenotype, as has been described in human MFH.8 In some of the tumors, the fibroblast component was minimal, obscured by the inflammatory cell infiltrate. In these, a preliminary misdiagnosis of Hodgkin’s disease was made because of the similarity of the polymorphic population of histiocytic cells, plasma cells, eosinophils, and xanthoma cells to those seen in Hodgkin’s disease. Additionally, some of the bizarre histiocytic cells in our canine spleens were reminiscent of ReedSternberg cells; however, the histiocytic cells were often polygonal and lacked huge nucleoli. Of the six dogs reported here, one (case No. 5) was euthanatized because of chronic renal failure. Another (case No. 2) was anorectic and depressed 2 weeks post-splenectomy and was euthanatized at that time. One dog (case No. 3) received six monthly chemotherapeutic treatments of Adriamycin (Adria Laboratories, Columbus, OH) after splenectomy but had focal metastatic MFH in the liver 9 months after the initial diagnosis. That dog and the remaining three dogs (case Nos. 1, 4, and 6) are alive and well at the time of this writing, although one (case No. 1) had a mild nonregenerative anemia for 2 months after surgery. A review of tissue sections of canine splenic sarcomas received through the biopsy service suggests that there is a recent increase in the incidence of the diagnosis of MFH in dog spleens. The six tumors reported here were received over a 1-year period, June 1989-July 1990, but no lesions compatible with MFH were found in specimens received from 1986 to 1989. The cause of this increased incidence is unknown; however, MFH of the canine spleen is probably far more common than that ofthe human spleen. Only two such instances have been reported in human Based on
tumor cells staining;
MUSclespecific Actin
Vimentin
+ + ++ + + ++ ++++ +++ +++ + + ++++ ++ + + + ++ + + + = 10-25%
Desmin
sloe
...
+
...
++
++++
+
... ++ ++++ + + + + + . ..
tumor cells staining;
+f + =
the known biologic behavior of these lesions in nonsplenic sites in animals and human beings and the metastatic capability displayed by one of the described tumors, MFH of the canine spleen should be given a guarded prognosis.
Acknowledgement We thank Mr. J. Hayden for photographic assistance.
References Bertoni F, Capanna R, Biagini R, Bacchini P, Guerra A, Ruggieri P, Present D, Campanacci M: Malignant fibrous histiocytoma of soft tissue. An analysis of 78 cases located and deeply seated in the extremities. Cancer 56: 356-357, 1985 Enzinger FM, Weiss SW: Soft Tissue Tumors, 2nd ed., pp. 269-300. CV Mosby, St. Louis, MO, 1988 Gleiser CA, Raulston GL, Jardine JH, Gray KN: Malignant fibrous histiocytoma in dogs and cats. Vet Pathol 16: 199-208, 1979 Govoni E, Bazzocchi F, Pilen S, Martinelli G: Primary malignant fibrous histiocytoma of the spleen: an ultrastructural study. Histopathology 6:35 1-36 1, 1982 Greaves P, Martin JM, Masson MT: Spontaneous rat malignant tumors of fibrohistiocytic origin: an ultrastructural study. Vet Pathol 19:497-505, 1982 Hsu SM, Raine L, Fanger H: A comparative study of the peroxidase-antiperoxidase method and an avidinbiotin complex method for studying polypeptide hormones with radioimmunoassay antibodies. Am J Clin Pathol 75734-738, 198 1 Jinno K, Moriwaki S: An autopsied case of malignant fibrous histiocytoma of the spleen. Jpn J Cancer Clin 33: 736-741, 1987 Miettinen M: Antibody specific to muscle actins in the diagnosis and classification of soft tissue tumors. Am J Pathol 130:205-2 15, I988
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9 Renlund RC, Pritzker KP: Malignant fibrous histiocytoma involving the digit in a cat. Vet Pathol 21:442444, 1984 10 Soule E, Enriquez P: Atypical fibrous histiocytoma, malignant fibrous histiocytoma, malignant histiocytoma, and epithelioid sarcoma: a comparative study of 65 tumors. Cancer 30:128-143, 1972 11 Tanimoto T, Ohtsuki Y, Sonobe H, Takahashi R, Nomura Y : Malignant fibrous histiocytoma in the spleen of a pig. Vet Pathol 25330-332, 1988
Vet Pathol 29(4), 1992
12 Weinstein MJ, Carpenter JL, Schunk CJ: Nonangiogenic and nonlymphomatous sarcomas of the canine spleen: 57 cases (1975-1987). J Am Vet Med Assoc 195:784788, 1989 Request reprints from Dr. M. Hendrick, Department of Pathobiology, School of Veterinary Medicine, University of Pennsylvania, 3800 Spruce Street, Philadelphia, PA 19104 (USA).
Vet Pathol 29:354-356 (1992)
Malignant Melanomas in a Penguin (Eudyptes chrysolophus) and a Red-tailed Hawk (Buteojamaicensis) E. KUFUOR-MENSAH AND G. L. WATSON Key words: Avian species; malignant melanoma; penguin; red-tailed hawk. Melanocytic tumors are relatively common in the dog, horse, and certain breeds of swine. They are less frequently observed in cattle and goats and are quite rare in cats and sheep.2 Malignant melanomas are extremely rare in avian species. The only previous reports are a perivascular melanosarcoma in a fowl (1 9 19),3.4a metastatic malignant melanoma of ovarian origin in an Emerald duck (1978),6 and other melanomas of primary ovarian origin in fowl (1928, 1929, and 1932)’ and in a budgerigar (1991).* The present case report describes malignant melanomas in a penguin and a red-tailed hawk. Case No. 1 was an adult female macaroni penguin (Eudyptes chrysolophus), acquired in 1968 by the Detroit Zoological Park, that was presented to the zoo’s veterinary hospital with severe progressive weight loss. At the time of physical examination, the bird weighed 4 kg. The cere was surrounded by a caseous and necrotic mass that extended into the rostra1 sinuses, engulfed the upper beak, distorted the face and eyes, and compromised normal respiration. The bird was euthanatized, and multiple tissues were collected at necropsy by the zoo’s veterinarian. The specimens were fixed in 10% neutral buffered formalin and submitted to the Animal Health Diagnostic Laboratory for examination. The submitted tissues were trimmed, paraffin embedded, sectioned at 6 pm thickness, and stained with hematoxylin and eosin for histopathologic examination. Some sections were “bleached” with potassium permanganate to facilitate interpretation. The most significant changes were in the skin of the beak region, the skeletal muscle, and the adrenal glands. Tissues from the beak area contained an infiltrative, deeply pigmented melanocytic neoplasm that extended from superficial to deep dermal regions and had effaced normal tissue architecture (Fig. 1). In the superficial dermis, the neoplastic melanocytes were arranged in clusters and packets of various sizes interspersed with irregular collagenous tissue. The neoplastic
cells coalesced in the deep dermis, forming dense sheets separated by thin collagenous stroma, and had infiltrated adjacent skeletal muscle. The tumor cells had round to ovoid vesicular nuclei of various sizes with marginated chromatin, one to two prominent nucleoli, and moderate amounts of indistinct cytoplasm containing abundant melanin pigment. The mitotic index was low and ranged from 0 to 2 per highpower field (0.23 mm in diameter). There were extensive regions of coagulative necrosis within the neoplasm. There was extensive infiltration of subjacent skeletal muscle with focal obliteration and segmental atrophy of fibers, hyalinization, and zones of necrosis. Each adrenal gland contained a discrete, solitary nodule of neoplastic melanocytes that involved approximately 20% of the glandular parenchyma (Fig. 2). Neoplastic cells in the muscle and adrenal glands were histologically similar to those described in the beak region. The liver had a mild diffuse periportal hepatitis with accumulations of lymphocytes and heterophils. The spleen had moderate lymphoid hyperplasia and scattered heterophilic aggregates. The kidney contained multiple small foci of mineralization and rare interstitial lymphoid infiltrates. The hepatic, splenic, and renal changes were those commonly seen in birds and are nonspecific.’ There were no abnormalities in the trachea, intestine, esophagus, heart, aorta, or ovary. Gross pulmonary lesions were not described by the prosector, and lung sections were not submitted. Neoplastic metastases were not found in tissues other than those described. Case No. 2 was an emaciated adult female red-tailed hawk (Buteojamaicensis) that had been found in a corn crib. The hawk had a fractured and overgrown upper beak and was euthanatized. At necropsy, necrotic bony tissue was found at the beak fracture site. The lungs were 75% consolidated, and there were two distinct nodules within the lung parenchyma, one yellowish white and the other greenish black. The liver appeared enlarged with rounded margins. The pan-
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BRIEF COMMUNICATIONS and CASE REPORTS Six Cases of Malignant Fibrous Histiocytoma of the Canine Spleen M. J. HENDRICK, J. J. BROOKS, AND E. H. BRUCE Key words: Dogs; malignant fibrous histiocytoma; spleen. Malignant fibrous histiocytoma (MFH) is the most common soft tissue sarcoma of human beings but has been described in dogs, cats, pigs, and rats only rarely.2.3,5,9J1,12 In human beings, MFH is an expansile tumor, usually involving the extremities or retroperitoneum. It may invade local tissues, and metastasis may occur to lung, lymph node, liver, and bone. In most reported animal cases, MFH has been described as a single, often invasive, soft tissue mass, usually in the limb^.^,^ Metastasis is only rarely reported. A report on spontaneous MFH in the forelimb of a rat described metastasis to lung and lymph node.5 There is one report of MFH involving the spleen, liver, and kidney of a pig.“ The largest nodule, 6 cm, was found in the spleen, which was presumed to be the primary site of origin of the neoplasm. One “fibrous histiocytoma” was mentioned briefly in a previous report on 57 nonlymphoid neoplasms of the canine spleen, but the lesion was not described in any detail.I2This report describes and classifies MFH of the canine spleen as a distinct clinicopathologic entity that should be recognized by veterinary pathologists. From June 1989 to July 1990, MFH was diagnosed in six canine spleens received by the biopsy service of the Laboratory of Pathology at the University of Pennsylvania, Philadelphia, Pennsylvania. The formalin-fixed specimens were routinely processed for histologic examination. Five-micrometer sections were cut from paraffin-embedded blocks and stained with hematoxylin and eosin. One section was stained with Giemsa. An avidin biotin immunoperoxidase complex technique was used, as previously described.6 Paraffin-embedded sections, 5 pm in thickness, were cut and carefully melted at 58-60 C. After deparaffinization and rehydration, slides were incubated in 0.3% H202in absolute methanol for 45 minutes. Sequential incubations in 20% normal goat serum (30 minutes), primary antiserum (1 hour at room temperature or overnight at 4 C), secondary biotinylated antibody (45 minutes), and avidin biotin complex reagent (45 minutes) followed. Sections were then exposed to the chromagen reaction solution (0.035°/o diaminobenzidine in 10 ml Tris buffer, filtered, and brought to 0.03% H202) for 5 minutes. Sections were counterstained in Mayer’s hematoxylin, dehydrated, cleared, and mounted. For certain antisera reactions (see below), sections were pretreated with a 0.1% solution of trypsin (Sigma Co., St. Louis, MO) in phosphate-buffered serum with 0.1 Yo CaCl for 30 minutes at 37 C. Sources of reagents and dilutions of antisera and modifi-
cations were as follows: avidin biotin reagents (Vector Laboratory System, Burlingame, CA); diaminobenzidine (Sigma Co.); antibody to cytokeratin (1/100, trypsinized, Lab Systems, Chicago, IL); desmin (1/450,2 hour room temperature, Dako, Santa Barbara, CA); vimentin (1/20, Dako); musclespecific actin (MSA, 1/4,000, Enzo, New York, NY);factor VIII antigen ( ~ 7 5 0 trypsinized, , Dako); SlOO antigen (11 1,000, Dako); a,-antichymotrypsin (ACT, 1/1,500, Dako); Leu M 1 (1/50, Becton-Dickinson, Rutherford, NJ); and leukocyte common antigen (LCA, 1/40, Dako). Both negative and substitution serum controls and positive tissue controls were employed. The signalment and immunohistochemical findings are listed in Table 1. There was no breed or sex predilection, but all dogs were between 9 and 14 years of age. The clinical history in each case was rather vague: lethargy, anorexia, and in most cases, a palpable splenic mass. One mass (case No. 5), was an incidental finding in a dog that had been euthanatized because of chronic renal failure. All masses were well circumscribed, white-grey, and multilobulated. Two of the five had reached a diameter > 15 cm. There was no gross evidence of involvement of any other organs or tissues. Histologically, all neoplasms were well circumscribed but unencapsulated. They were composed of a heterogeneous cell population that included rounded to polygonal histiocytoid cells, some of which were quite large with bizarre nuclei and prominent nucleoli, and spindled fibroblastic cells sometimes arranged in a storiform or fingerprint pattern. Lymphocytes, plasma cells, and eosinophils were found in all tumors but were prominent in four cases. Occasional large foamy “xanthoma” cells were seen. The relative percentages of these cells varied from tumor to tumor, but all tumors fit the classification scheme of MFH in human beings, as described by Enzinger and W e k 2No other specific morphologic patterns were identified in any of these tumors such as an alternating fascicular pattern or herringbone pattern, such as would be seen in a fibrosarcoma or leiomyosarcoma, or prominent cytoplasmic vacuolization, such as would be seen in liposarcoma. In one tumor (case No. 5), bizarre tumor giant cells dominated the histologic picture and inflammatory cells were only rarely seen. These were present against a background of fibroblastic cells, often arranged in a storiform pattern (Fig. 1). This pattern corresponded to the typical storiform/pleomorphic type of human MFH. In four tumors (case Nos. 1, 3, 4, and 6), there was a
35 1
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Brief Communications and Case Reports
Vet Pathol 29(4), 1992
prominent inflammatory cell infiltrate (Fig. 2). The diagnosis of malignant fibrous histiocytoma was prompted by the presence of histiocytoid cells with nuclear enlargement, nuclear atypia, and atypical mitoses. Truly bizarre cells were widely scattered and partially concealed by the inflammatory infiltrate. A storiform pattern was usually inconspicuous or present only focally in these cases. Although these tumors could be considered equivalent to the “inflammatory” type of human MFH, neutrophils were scarce or absent; thus, they are more appropriately classified as subvariants of the stonform/ pleomorphic type with marked inflammation. One case (No. 2) had an unusual morphologic appearance (Fig. 3). Sheets of clear xanthomatous epithelioid cells were present and dissected by small capillaries in a manner reminiscent of renal cell carcinoma; however, the tumor was clearly confined to the spleen grossly, and no epithelial markers were present. The histologic appearance was somewhat similar to that of a rare variant of human MFH-the histiocytoid or epithelioid type with rounded histiocytoid cells in sheets without spindling.lJOThe clear cells feature sets this case apart and imparts an appearance perhaps restricted to the canine. Marker staining varied according to the histologic changes defined above (Table 1). In the four cases (Nos. 1, 3, 4, and 6) with the inflammatory component, the underlying spindled cells and the scattered larger pleomorphic cells showed strong staining for muscle-specific actin but only moderate desmin and weak vimentin staining. Muscle-specific actin was weaker in the highly pleomorphic case (but desmin was strong) and weak to absent in the xanthomatous case (No. 2). Four cases (Nos. 1,2, 3, and 5) contained weak and focal positivity for SlOO protein; none showed reactivity for aIantichymotrypsin, a common protein found in human MFH. All tumor cells were negative for cytokeratin (CAM 5.2), epithelial membrane antigen, factor VIII-related antigen, Leu M1, and leukocyte common antigen. The last two markers failed to stain the normal neutrophils and lymphocytes, respectively. Malignant fibrous histiocytoma in human beings has five major variants: storiform/pleomorphic, myxoid, giant cell, inflammatory, and angiomatoid.*This classification scheme is incomplete, and various morphologic types may be seen in any one tumor; therefore, tumors are usually classified by their predominant feature(s). Based on this paradigm, our canine splenic neoplasms have been classified as stonform/ pleomorphic (5/6; one typical and four with marked inflammation) and epithelioid/xanthomatous ( 1/6). The distinction between variants of MFH has some clinical significance in human beings in that the myxoid variant and tumors with
c
Fig. 1. Spleen; dog No. 5. Typical storiform/pleomorphic variant of malignant fibrous histiocytoma (MFH). Note the storiform arrangement of spindle cells with many large bizarre cells (arrows) and scattered inflammatory cells. HE. Bar = 50 fim.
Fig. 2. Spleen; dog No. 4. Storiform/pleomorphic vanant of MFH with marked inflammation. The field is dominated by lymphocytes mixed with mononuclear histiocytoid cells, a few of which have karyomegaly (arrow). HE. Bar = 50 fim. Fig. 3. Spleen; dog No. 2. Epithelioidxanthomatous variant. Note the clusters of large foamy “xanthoma” cells intermingled with lymphocytes. HE. Bar = 40 pm.
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Table 1. Signalment and immunohistochemical findings in six dogs with malignant fibrous histiocytomas of the spleen. Immunohistochemical results? Case No.
Sex*
Breed
Age (years)
1
Canaan
F/s
12
2
Cocker Spaniel
M/c
12
3
Irish Terrier
M
10
4
Mixed
F/s
9
5
Shetland Sheepdog
M/c
14
6
Terrier
F
14
* F/s = spayed female; M/c
=
Tumor Slassification L
Storiform/pleomorphic with inflammation Epithelioid/ xanthomatous Storiform/pleomorphic with inflammation Storiform/pleomorphic with inflammation Storiform/pleomorphic (typical) Storiform/pleomorphic with inflammation
castrated male.
t ... = negative staining; 2 = < 1% tumor cells staining; + = 2-10%
25-50% tumor cells staining;
++ + + = > 50% tumor cells staining.
marked inflammation have a slightly better prognosis than the storiform/pleomorphic variant.2 At present, the number of canine cases is too small to determine whether our classification scheme has any prognostic significance. The presence of muscle-specific actin, vimentin, and desmin in these tumors is consistent with a fibroblastic/myofibroblastic phenotype, as has been described in human MFH.8 In some of the tumors, the fibroblast component was minimal, obscured by the inflammatory cell infiltrate. In these, a preliminary misdiagnosis of Hodgkin’s disease was made because of the similarity of the polymorphic population of histiocytic cells, plasma cells, eosinophils, and xanthoma cells to those seen in Hodgkin’s disease. Additionally, some of the bizarre histiocytic cells in our canine spleens were reminiscent of ReedSternberg cells; however, the histiocytic cells were often polygonal and lacked huge nucleoli. Of the six dogs reported here, one (case No. 5) was euthanatized because of chronic renal failure. Another (case No. 2) was anorectic and depressed 2 weeks post-splenectomy and was euthanatized at that time. One dog (case No. 3) received six monthly chemotherapeutic treatments of Adriamycin (Adria Laboratories, Columbus, OH) after splenectomy but had focal metastatic MFH in the liver 9 months after the initial diagnosis. That dog and the remaining three dogs (case Nos. 1, 4, and 6) are alive and well at the time of this writing, although one (case No. 1) had a mild nonregenerative anemia for 2 months after surgery. A review of tissue sections of canine splenic sarcomas received through the biopsy service suggests that there is a recent increase in the incidence of the diagnosis of MFH in dog spleens. The six tumors reported here were received over a 1-year period, June 1989-July 1990, but no lesions compatible with MFH were found in specimens received from 1986 to 1989. The cause of this increased incidence is unknown; however, MFH of the canine spleen is probably far more common than that ofthe human spleen. Only two such instances have been reported in human Based on
tumor cells staining;
MUSclespecific Actin
Vimentin
+ + ++ + + ++ ++++ +++ +++ + + ++++ ++ + + + ++ + + + = 10-25%
Desmin
sloe
...
+
...
++
++++
+
... ++ ++++ + + + + + . ..
tumor cells staining;
+f + =
the known biologic behavior of these lesions in nonsplenic sites in animals and human beings and the metastatic capability displayed by one of the described tumors, MFH of the canine spleen should be given a guarded prognosis.
Acknowledgement We thank Mr. J. Hayden for photographic assistance.
References Bertoni F, Capanna R, Biagini R, Bacchini P, Guerra A, Ruggieri P, Present D, Campanacci M: Malignant fibrous histiocytoma of soft tissue. An analysis of 78 cases located and deeply seated in the extremities. Cancer 56: 356-357, 1985 Enzinger FM, Weiss SW: Soft Tissue Tumors, 2nd ed., pp. 269-300. CV Mosby, St. Louis, MO, 1988 Gleiser CA, Raulston GL, Jardine JH, Gray KN: Malignant fibrous histiocytoma in dogs and cats. Vet Pathol 16: 199-208, 1979 Govoni E, Bazzocchi F, Pilen S, Martinelli G: Primary malignant fibrous histiocytoma of the spleen: an ultrastructural study. Histopathology 6:35 1-36 1, 1982 Greaves P, Martin JM, Masson MT: Spontaneous rat malignant tumors of fibrohistiocytic origin: an ultrastructural study. Vet Pathol 19:497-505, 1982 Hsu SM, Raine L, Fanger H: A comparative study of the peroxidase-antiperoxidase method and an avidinbiotin complex method for studying polypeptide hormones with radioimmunoassay antibodies. Am J Clin Pathol 75734-738, 198 1 Jinno K, Moriwaki S: An autopsied case of malignant fibrous histiocytoma of the spleen. Jpn J Cancer Clin 33: 736-741, 1987 Miettinen M: Antibody specific to muscle actins in the diagnosis and classification of soft tissue tumors. Am J Pathol 130:205-2 15, I988
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Brief Communications and Case Reports
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9 Renlund RC, Pritzker KP: Malignant fibrous histiocytoma involving the digit in a cat. Vet Pathol 21:442444, 1984 10 Soule E, Enriquez P: Atypical fibrous histiocytoma, malignant fibrous histiocytoma, malignant histiocytoma, and epithelioid sarcoma: a comparative study of 65 tumors. Cancer 30:128-143, 1972 11 Tanimoto T, Ohtsuki Y, Sonobe H, Takahashi R, Nomura Y : Malignant fibrous histiocytoma in the spleen of a pig. Vet Pathol 25330-332, 1988
Vet Pathol 29(4), 1992
12 Weinstein MJ, Carpenter JL, Schunk CJ: Nonangiogenic and nonlymphomatous sarcomas of the canine spleen: 57 cases (1975-1987). J Am Vet Med Assoc 195:784788, 1989 Request reprints from Dr. M. Hendrick, Department of Pathobiology, School of Veterinary Medicine, University of Pennsylvania, 3800 Spruce Street, Philadelphia, PA 19104 (USA).
Vet Pathol 29:354-356 (1992)
Malignant Melanomas in a Penguin (Eudyptes chrysolophus) and a Red-tailed Hawk (Buteojamaicensis) E. KUFUOR-MENSAH AND G. L. WATSON Key words: Avian species; malignant melanoma; penguin; red-tailed hawk. Melanocytic tumors are relatively common in the dog, horse, and certain breeds of swine. They are less frequently observed in cattle and goats and are quite rare in cats and sheep.2 Malignant melanomas are extremely rare in avian species. The only previous reports are a perivascular melanosarcoma in a fowl (1 9 19),3.4a metastatic malignant melanoma of ovarian origin in an Emerald duck (1978),6 and other melanomas of primary ovarian origin in fowl (1928, 1929, and 1932)’ and in a budgerigar (1991).* The present case report describes malignant melanomas in a penguin and a red-tailed hawk. Case No. 1 was an adult female macaroni penguin (Eudyptes chrysolophus), acquired in 1968 by the Detroit Zoological Park, that was presented to the zoo’s veterinary hospital with severe progressive weight loss. At the time of physical examination, the bird weighed 4 kg. The cere was surrounded by a caseous and necrotic mass that extended into the rostra1 sinuses, engulfed the upper beak, distorted the face and eyes, and compromised normal respiration. The bird was euthanatized, and multiple tissues were collected at necropsy by the zoo’s veterinarian. The specimens were fixed in 10% neutral buffered formalin and submitted to the Animal Health Diagnostic Laboratory for examination. The submitted tissues were trimmed, paraffin embedded, sectioned at 6 pm thickness, and stained with hematoxylin and eosin for histopathologic examination. Some sections were “bleached” with potassium permanganate to facilitate interpretation. The most significant changes were in the skin of the beak region, the skeletal muscle, and the adrenal glands. Tissues from the beak area contained an infiltrative, deeply pigmented melanocytic neoplasm that extended from superficial to deep dermal regions and had effaced normal tissue architecture (Fig. 1). In the superficial dermis, the neoplastic melanocytes were arranged in clusters and packets of various sizes interspersed with irregular collagenous tissue. The neoplastic
cells coalesced in the deep dermis, forming dense sheets separated by thin collagenous stroma, and had infiltrated adjacent skeletal muscle. The tumor cells had round to ovoid vesicular nuclei of various sizes with marginated chromatin, one to two prominent nucleoli, and moderate amounts of indistinct cytoplasm containing abundant melanin pigment. The mitotic index was low and ranged from 0 to 2 per highpower field (0.23 mm in diameter). There were extensive regions of coagulative necrosis within the neoplasm. There was extensive infiltration of subjacent skeletal muscle with focal obliteration and segmental atrophy of fibers, hyalinization, and zones of necrosis. Each adrenal gland contained a discrete, solitary nodule of neoplastic melanocytes that involved approximately 20% of the glandular parenchyma (Fig. 2). Neoplastic cells in the muscle and adrenal glands were histologically similar to those described in the beak region. The liver had a mild diffuse periportal hepatitis with accumulations of lymphocytes and heterophils. The spleen had moderate lymphoid hyperplasia and scattered heterophilic aggregates. The kidney contained multiple small foci of mineralization and rare interstitial lymphoid infiltrates. The hepatic, splenic, and renal changes were those commonly seen in birds and are nonspecific.’ There were no abnormalities in the trachea, intestine, esophagus, heart, aorta, or ovary. Gross pulmonary lesions were not described by the prosector, and lung sections were not submitted. Neoplastic metastases were not found in tissues other than those described. Case No. 2 was an emaciated adult female red-tailed hawk (Buteojamaicensis) that had been found in a corn crib. The hawk had a fractured and overgrown upper beak and was euthanatized. At necropsy, necrotic bony tissue was found at the beak fracture site. The lungs were 75% consolidated, and there were two distinct nodules within the lung parenchyma, one yellowish white and the other greenish black. The liver appeared enlarged with rounded margins. The pan-
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