Sage Journals: Discover world-class research

Abstract

Liposarcomas are malignant tumors of adipocytes. The current report describes a liposarcoma in a 2.5-year-old, mixed-breed commercial sow that was detected during meat inspection. On gross examination, a firm, whitish, multinodular, 20 cm ×10 cm mass was observed in the perirenal area along with smaller nodules multifocally scattered within the renal parenchyma. Histological examination revealed an anaplastic sarcoma with clear intracytoplasmic lipidic vacuoles that were positive for Sudan black staining. Most of the cells were also positive for S100 and vimentin immunohistochemistry. Based on these results, a diagnosis of a perirenal liposarcoma was established. To the authors’ knowledge, no previous reports of liposarcomas in pigs have been published. This report also includes a review of the literature published on animal liposarcomas.

Keywords

Adipose tissue animal liposarcoma porcine Sudan black

A 2.5-year-old commercial sow was slaughtered in an abattoir in Catalonia, Spain, and samples were submitted for examination. On questioning, the inspectors that submitted the sample reported no antemortem alterations. Regrettably, no further information could be obtained from the farm of origin. The macroscopic description referred from the veterinary inspector was that during the postmortem inspection, a multinodular, whitish mass, of firm consistency and measuring 20 cm × 10 cm, was observed in the right perirenal region. The cut section revealed different areas with grainy surface and small white nodules (Fig. 1A). Multiple nodules with the same macroscopic features were observed unilaterally scattered within the right kidney parenchyma (Fig. 1B).

Figure 1.

A, perirenal liposarcoma, pig. Multinodular, whitish mass of firm consistency observed in the right perirenal region with several scattered yellowish areas of necrosis. B, multiple renal lesions with the same macroscopic characteristics as those described in panel A, in the renal parenchyma. C, perirenal liposarcoma, pig. Different patterns of neoplastic cells were observed within the tumor. In the upper half of the picture, cells are shown immersed in abundant collagenous stroma; in the lower half, the stroma was scant and the majority of cells showed big, clear, and well-defined lipidic cytoplasmic vacuoles. Hematoxylin and eosin. Bar = 20 μm. D, renal liposarcoma cells containing small- to medium-sized lipid vacuoles. Hematoxylin and eosin. Bar = 25 μm. E, perirenal liposarcoma, pig. Eighty percent of neoplastic cells had strong and diffuse cytoplasmic positive staining for S100 immunohistochemistry. Bar = 50 μm. F, perirenal liposarcoma, pig. Staining of the neoplastic cells from the perirenal mass, note positively stained intracytoplasmic lipid filled vacuoles. Sudan black. Bar = 25 μm.

The kidney and different sections from the perirenal mass were collected, fixed in 10% formalin, and submitted to the Slaughterhouse Support Network (Servei de Suport a Escorxadors [SESC]) of the Center for Research in Animal Health (Centre de Recerca en Sanitat Animal [CReSA]; Barcelona, Spain) for diagnosis. The differential diagnosis by the meat inspectors included lymphosarcoma or an adrenal gland tumor. In the laboratory, samples were routinely processed for histology. Sections were processed for hematoxylin and eosin staining. Immunohistochemical staining (IHC) with antibodies against cluster of differentiation (CD)3^a and CD20^b were performed in order to rule out a possible lymphoid origin. Lysozyme^c IHC was also performed to discard a macrophagic origin of the tumor and S100^d IHC to rule out a fibrosarcoma, which lacks immunoreactivity for this protein.⁴ Finally, IHC against vimentin^e was performed to confirm the mesenchymal origin of the neoplasm.

Briefly, heat-induced antigen retrieval was performed in an autostainer,^f at 95°C with low pH target retrieval solution for 20 min before application of primary antibodies for CD3, CD20, S100, and vimentin. For the lysozyme IHC, slides were pretreated with proteinase K for 10 min at room temperature.

For IHC control purposes, porcine lymph node tissue for CD3 and CD20 was used. A cerebellum section was chosen as a control for S100 IHC, a tongue tissue section for vimentin IHC, and, for lysozyme IHC, skin with granulomatous dermatitis was used. Omission of the primary antibody in each slide served as nonspecific reaction control.

Sudan black staining^g was performed on cryotome-obtained sections from formalin-fixed tissue, to identify the content of the cytoplasmic vacuoles. Regular adipose tissue was used as the technique control.

The mass was a densely cellular, infiltrative, and partially encapsulated neoplasm. Cells were arranged in compacted but disorganized bundles with abundant collagenous stroma, scant myxoid matrix, and a few blood vessels. Cells were medium sized and spindle shaped, with poorly defined borders. The cells had a moderate amount of fibrillar, pale, and eosinophilic cytoplasm. In some areas, cells had medium to large, well-defined, lipid intracytoplasmic vacuoles (Fig. 1C). Nuclei were paracentral, oval, and large with finely stippled chromatin and 1 or 2 eosinophilic nucleoli. Anisocytosis and anisokaryosis were evident, and some karyomegalic cells could be observed. Mitotic index was low (0–1 mitotic figures in 10 random fields at 400×). Mature eosinophils with some lymphocytes were scattered among the neoplastic cells. There were also multifocal large areas of necrosis and mineralization. In contrast, in the kidney, most neoplastic cells were polygonal and just a few had spindle shapes and intracytoplasmic lipid vacuoles. Foci of these tumor cells multifocally present within the renal cortex. Pleomorphism and mitotic index were higher (2–3 mitotic figures in 10 random fields at 400×). Based on the histological features of the perirenal mass, and a positive result against vimentin IHC on over 90% of the tumor cells, a diagnosis of anaplastic malignant mesenchymal cell tumor was established.

Differential diagnosis included histiocytic sarcoma, fibrosarcoma, and liposarcoma. Eighty percent of the cells, particularly those with spindle shapes, were intensely positive for S100 IHC within the cytoplasm and nuclei (Fig. 1E). The Sudan black–positive result confirmed the lipid-nature of the cytoplasmic vacuoles of the neoplastic cells (Fig. 1F). Hence, macroscopic and histological features of the perirenal mass, along with Sudan black and IHC, led to the diagnosis of a malignant liposarcoma. Although the cells of the kidney mass were initially suggestive of a round cell tumor, IHC of CD3,^b CD20,^c and lysozyme^d were negative for the 3 markers in the kidney and perirenal tumors. These results ruled out the possibility of a round cell tumor and supported the hypothesis of a common mesenchymatous origin of both neoplastic lesions. The renal lesion was considered to be a metastasis from the primary liposarcoma. Based on the cellular morphology, the remitted masses were classified as a pleomorphic liposarcoma.

The most commonly reported swine tumors are those affecting young pigs, such as lymphosarcoma, embryonal nephroma, and melanoma.¹⁵ This is because of the fact that a majority of pigs are slaughtered before reaching adulthood, when tumors often develop.¹⁵ Based on abattoir surveys, lymphoma is the most frequent tumor of swine, commonly affecting 1-year-old or younger pigs.^22,40 In a retrospective study in 63 pot-bellied pigs, the tumor incidence was summarized and a variety of neoplasms in pigs was described without any evidence of liposarcomas. The mean age of the tumor development in that study was 11.3 years.³⁹ There are very few reported cases of lipomas in pigs.⁶²

To the best of the authors’ knowledge, liposarcomas have not been reported in pigs. In the current report, we describe a liposarcoma that developed presumably from the perirenal fat, with metastasis to the renal parenchyma.

In most cases of liposarcomas reviewed in this article, IHC and histological (lipid) stainings have been used to reach the final diagnosis because histological examination revealed a poorly defined neoplastic proliferation.^42,59 Such methods have also been used to confirm the microscopic diagnosis in some well-differentiated liposarcomas.⁴² Frequently used markers are lipid stainings (such as oil red O) and vimentin and S100 IHC. All of these markers yield positive results, regardless of the subtype of liposarcoma and species in which they have been used.^{1,16,42,59,65} Although rare, this diagnosis should be included in the differential diagnosis of swine neoplasms.

Liposarcoma is a malignant tumor of adipocytes, first described by Rudolf Virchow in 1857.⁴⁸ Traditionally, great emphasis has been placed on the identification of lipoblasts for diagnosing liposarcomas, but their importance in some situations has been overemphasized as lipoblast-like cells may be seen in a variety of conditions.⁶⁷

Liposarcoma is among the most commonly described soft tissue sarcomas in adult human beings.^10,11 The most recent World Health Organization (WHO) classification of soft tissue tumors recognizes 5 categories of liposarcomas: well-differentiated (which includes the adipocytic, sclerosing, and inflammatory subtypes), dedifferentiated liposarcoma, myxoid liposarcoma, round cell liposarcoma, and pleomorphic liposarcoma.³⁸ Although liposarcomas are divided into these subtypes, the categories most frequently used are well-differentiated liposarcoma, myxoid liposarcoma, and pleomorphic liposarcoma.⁶⁷ Well-differentiated liposarcomas are the most common form of reported malignant adipocytic neoplasms, accounting for approximately 40–45% of all liposarcomas followed by myxoid liposarcoma (30–35%).^11,67 Pleomorphic liposarcoma is the least common malignant adipocytic neoplasm, accounting for approximately 5% of all cases.¹¹ The limited presence of cytoplasmatic lipid vacuoles may have led to misdiagnosis of liposarcomas as undifferentiated pleomorphic sarcoma.⁴¹

In veterinary medicine, there is no accepted classification of liposarcomas, but based on cellular morphology and following the WHO classification, liposarcomas in animals are divided into 3 categories: well-differentiated, pleomorphic, and myxoid liposarcomas.^3,22,38 In animals, liposarcomas are rare but can occur in many domestic and nondomestic species^{1,12,16,29,36,43,45,46,61} (Table 1). Liposarcoma has been described most commonly in dogs and, in this species, its incidence increases with age.^{3,13,22,31,66} The average age of affected dogs is 9–10 years.^3,13,32,66 The etiology of canine liposarcomas is largely unknown although it has been associated with the presence of foreign bodies.^34,63 In an 11-year-old dog, a liposarcoma in the forelimb was associated with a glass foreign body.³⁴ A low-grade liposarcoma was diagnosed in another 11-year-old dog with a subcutaneous mass located in the lateral region of the neck, at the site of a microchip implantation.⁶³ In cats, it has been associated with vaccination sites²¹ and retrovirus infection even though it could not be proved that the tumor was caused by the virus.⁵⁷ The majority of liposarcomas are aggressive, locally invasive neoplasms. Location is unpredictable (Table 1). Recurrence is common but metastatic spread is rare except in cases with evident cellular anaplasia. In myxoid liposarcomas, metastatic rate can reach 60% and, in pleomorphic liposarcomas, between 30% and 50%.¹¹ In dogs, metastases have been reported mainly in lung, spleen, liver, kidney, and lymph nodes.^3,17,38,65

Table 1.

Liposarcoma reports in the veterinary literature.*

Species	Age	Sex	Subtype	Location	Metastasis	Reference
Cat (Felis silvestris catus)	4 mo	M	L	Cervical region	Kidney, liver	57
	13 y	M	WDL	Axillary subcutis	Kidney	8
Chukar partridge (Alectoris chukar)	NA	NA	NA	Unspecified viscera	NA	46
Cockatiel (Nymphicus hollandicus)	NA	NA	NA	Unspecified viscera	NA	46
Common eland (Taurotragus oryx)	16 y	F	ML	Pericardial	None	16
Cow (Bos taurus)	7 y	F	PL	Nasal cavity	None	52
	31 mo	F	PL	Cheek subcutis	Lymph nodes	59
Dog (Canis lupus familiaris)	NA	NA	NA	Cutaneous	NA	54
	NA	NA	NA	Lung	NA	23
	NA	NA	NA	Spleen	NA	56
	NA	NA	NA	Spleen	NA	66
	NA	F	PL	Liver	None	19
	NA	F (25), M (31)	WDL (3), ML (7), PL (37)	Axial region (26), appendicular region (23), within viscera (6), bone marrow (1)	Spleen, liver	3
	16 mo	M	L	Bone	Spleen, liver, lymph node	17
	3 y	M	L	Bone marrow	Lymph node, pericardium, liver, spleen, kidney	9
	5 y	M	ML	Thorax	None	4
	6 y	M		Shoulder subcutis	NA	13
	7 y	F	WDL	Thigh	Spleen, liver, lung, lymph node	49
	7 y	F	L	Lung	None	50
	8 y	M	ML	Cranial mediastinum	None	35
	8 y	F	ML	Lumbar vertebrae (extradural mass)	None	32
	8 y	M	PL	Mesojejunoileum	Liver	7
	8 y	M	NA	Thigh muscle	NA	13
	9 y	F	NA	Omentum	NA	13
	9 y	F	ML	Subarachnoid space between C1-C2	None	47
	9 y	F	WDL	Tongue	None	42
	9 y	F	NA	L6 vertebrae	Heart, pericardium, lungs, spleen, kidneys	65
	10 y	F	NA	Shoulder subcutis	NA	13
	10 y	M	NA	Abdominal subcutis	NA	13
	11 y	F	L	Forelimb	None	34
	11 y	M	L	Cervical subcutis	None	63
	15 y	F	NA	Tongue	None	37
Ferret (Mustela putoriusfuro)	NA	NA	L	Subcutaneous	NA	14
	4 y	F	L	Inguinal region	None	20
	2 y	M	PL	Mandibular bone marrow	None	18
Goose (Branta canadensis)	NA	F	L	Skeletal muscles	None	12
Guinea pig (Cavia porcellus)	18 mo	M	WDL	Eyelid	None	43
Hen (Gallus gallus)	NA	NA	NA	Leg musculature	NA	36
Horse (Equus ferus caballus)	23 y	F	WDL	Mediastinum	None	29
Kudu (Tragelaphus strepsiceros)	NA	NA	WDL	Bone marrow	None	45
Macaque (Macaca fuscata)	5 y	F	ML	Omentum,retroperitoneum	None	30
Meerkat (Suricata suricatta)	NA	F	PL	Thoracic cavity	Lung, spleen, thoracic, lymph nodes	1
Pigeon (Columba livia)	NA	F	L	Mesentery	None	51
	NA	NA	NA	Unspecified viscera	NA	46
Quaker parrot (Myiopsitta monachus)	5 y	NA	WDL	Wing extremity	None	61
Rabbit(Oryctolagus cuniculus)	4 y	F	NA	Thoracic cavity	None	64
Rat (Rattus spp.)	NA	M (530), F (530)	L	Kidney	None	6

y = years; mo = months; F = female; M = male; PL = pleomorphic liposarcoma; WDL = well-differentiated liposarcoma; ML = myxoid liposarcoma; L = liposarcoma; NA = data not available. Numbers in parentheses indicate number of cases.

Well-differentiated variant

Considered the most common histologic subtype,³¹ well-differentiated variant consists of multilobular, fairly well-circumscribed but unencapsulated neoplasms that arise from the subcutis.^8,31 Cells can be round to polygonal and arranged in solid sheets. A moderate number of cells are well-differentiated adipocytes, with a single clear fat vacuole and peripheral nuclear displacement.^22,49 Other cells have a central, round to oval nuclei and abundant cytoplasm that contains variably sized lipid droplets resembling large pleomorphic lipoblasts of varying maturity.^22,45 Mitotic activity is low. The diagnosis in these cases is clear.^{8,22,31,42,45,49} This subtype must be differentiated from invasive lipomas (also named infiltrative lipomas), which are histologically similar but lack mitotic figures and show no evidence of anaplasia.^24,28,54

Myxoid variant

The myxoid variant is an uncommon variant of liposarcoma, and is described as multilobular and nonencapsulated with poorly defined mass margins.^4,30,31,35 This subtype is usually composed of a mixture of lipocytes, with a single large and clear cytoplasmic lipid vacuole compressing the nuclei, lipoblasts, and scattered spindle and stellate cells interspersed in a myxoid background with small number of collagen fibrils.^4,35,47 A few multinucleated tumor cells can also be present.^4,21,30,47 Anastomosing capillary vasculature is likewise present.^31,35 Resembling myxosarcoma, this tumor is differentiated by the presence of cytoplasmic lipid-filled vacuoles.^{4,21,30,31,35,42,47}

Pleomorphic liposarcoma

This variant has pleomorphic cells of variable size and shape,⁵² and large bizarre multinucleated cells might be observed.^7,31 Cells have abundant eosinophilic cytoplasm that may appear glassy or foamy. A few cells have intracytoplasmic distinct fat vacuoles.^31,52 Nuclei also exhibit variability in size, shape, and chromatin pattern. Nuclear hyperchromatism is common, and single or multiple conspicuous nucleoli can be observed.^7,52 Mitoses are frequent.^7,22,52 This tumor mimics other pleomorphic mesenchymal malignancies, especially when they have scant lipoblasts.⁶⁷ Liposarcomas resemble a pleomorphic variant of histiocytic sarcoma but, in the case of liposarcomas, they lack significant collagenous stroma and spindle-cell population.^{1,7,22,31,42,52,59} Unlike histiocytic sarcoma, pleomorphic liposarcomas demonstrate focal labeling for S100 protein in their lipoblastic elements.⁵ Even though there are many unclassified liposarcomas in the veterinary medicine literature, in a study including 56 liposarcoma reports in dogs, this was the most prevalent subtype.³ In Table 1, a summary of the liposarcomas described in veterinary medicine literature is presented, including information on the animal species, age, sex, tumor site, and the occurrence of metastasis.

Regarding diagnosis, soft tissue sarcomas with a pleomorphic histological appearance can manifest similar immunoreactivity patterns.¹⁶ Nevertheless, immunohistochemical characterization of the tumor is useful for definitive diagnosis.⁴² The presence of vacuolated cells with positive vimentin and S100 immunostaining is suggestive of a liposarcoma.^{1,16,42,59,65} All pleomorphic dedifferentiated liposarcomas are intensely vimentin positive,^1,59,65 approximately 70% are S100 positive, and just 30% of them are collagen type IV positive. Diagnostic intracytoplasmic fat vacuoles are usually present, but only in a small percentage of cells.^22,59 The lack of cytokeratin labeling is useful in differentiating liposarcomas from other lipid-rich neoplasias, such as mesotheliomas.^16,42

The histological staining reviewed in the literature of veterinary liposarcomas include oil red O,^{7,9,12,14,16,18,29,30,45,46,49,52,66} periodic acid–Schiff,^1,34 osmium tetroxide,^18,45,52 alcian blue, and toluidine.^17,45 The immunohistochemical markers most frequently used were vimentin,^{1,14,16,42,43,47,59,52,65} S100,^{1,16,42,47,59,65} cytokeratin,^{1,16,42,43,47,50,52,59,65} CD3,⁵¹ actin,^14,51,65 and desmin.^42,47,66

Liposarcomas can be diagnosed cytologically, by fine-needle aspiration, where dense aggregates of mesenchymal cells containing variable amount of lipid vacuoles can be recognized.^4,20,35 Multinucleated cells may be present.^35,44 In contrast, other authors consider cytological examination not suitable to reach a definitive diagnosis of liposarcoma, and limit this technique to support the choice between incisional or excisional biopsy.⁵⁸ Some studies suggest that oil red O staining may be an easy, inexpensive, and useful diagnostic tool for cytological diagnosis of canine liposarcoma and the differentiation from other mesenchymal neoplasms,³³ such as fibrosarcoma, undifferentiated sarcoma, and anaplastic carcinoma.⁴⁴

The first choice of treatment for human beings and animals is a wide surgical excision, the current established treatment for soft tissue sarcoma.²⁶ Although used in combination in some contexts to control recurrence,⁷ the efficacy of radiation therapy and chemotherapy remains uncertain at this time.²⁶

Footnotes

Acknowledgements

The authors thank Agència de Salut Pública de Catalunya (ASPC), slaughterhouse veterinary meat inspectors for macroscopic pictures and case description, and the technical assistance of Blanca Pérez and Aida Neira of the Veterinary Pathology Diagnostic Service (SDPV-UAB). The authors thank also the Slaughterhouse Support Network (Servei de Suport a Escorxadors, SESC-CReSA), which is funded by ASPC of the Departament de Salut, Generalitat de Catalunya.

a.

CD3 (ref. A-0452), Dako Denmark A/S, Glostrup, Denmark.

b.

CD20 (ref. PAS-35313), Dako Denmark A/S, Glostrup, Denmark.

c.

Lysozyme (ref. A-0099), Dako Denmark A/S, Glostrup, Denmark.

d.

S100 (ref. Z0311), Dako Denmark A/S, Glostrup, Denmark.

e.

Vimentin (ref. M0725), Dako Denmark A/S, Glostrup, Denmark.

f.

PTLink autostainer, EnVision FLEX; Dako Denmark A/S, Glostrup, Denmark.

g.

Sudan black, Merck KGaA, Darmstadt, Germany.

Declaration of conflicting interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) received no financial support for the research, authorship, and/or publication of this article.

References

Aihara

Une

. Pleomorphic liposarcoma of the intrathoracic cavity in a meerkat (Suricata suricatta). J Vet Med Sci 2009;71:685–688.

Bacon

. Evaluation of primary re-excision after recent inadequate resection of soft tissue sarcomas in dogs: 41 cases (1999–2004). J Am Vet Med Assoc 2007;230:548–554.

Baez

. Liposarcomas in dogs: 56 cases (1989–2000). J Am Vet Med Assoc 2004;224:887–891.

Boyd

. Matrix “blues”: clue to a cranial thoracic mass in a dog. Vet Clin Pathol 2005;34:271–274.

Cerilli

Wick

. Immunohistology of soft tissue and osseous neoplasms. In: Dabbs

, ed. Diagnostic Immunohistochemistry. 2nd ed. Pittsburgh, PA: Churchill Livingstone, 2006:65–120.

Chandra

. Spontaneous renal neoplasms in rats. J Appl Toxicol 1993;13:109–116.

Chang

Liao

. Mesojejunoileac liposarcoma with intrahepatic metastasis in a dog. J Vet Med Sci 2008;70:637–640.

Cramer

. Pathology in practice. Liposarcoma. J Am Vet Med Assoc 2011;239:757–759.

Davis

. Multiple liposarcoma of bone marrow origin in a Greyhound. J Small Anim Pract 1974;15:445–456.

10.

Dei Tos

. Liposarcoma: new entities and evolving concepts. Ann Diagn Pathol 2000;4:252–266.

11.

Dei Tos

. Liposarcomas: diagnostic pitfalls and new insights. Histopathology 2014;64:38–52.

12.

Doster

. Liposarcoma in a Canada goose (Branta canadensis). Avian Dis 1987;31:918–920.

13.

Doster

. Canine liposarcoma. Vet Pathol 1986;23:84–87.

14.

D’Ovidio

. Subcutaneous liposarcoma in a ferret (Mustela putorius furo). J Exot Pet Med 2012;21:238–242.

15.

Edwards

. Genetic, developmental, and neoplastic diseases. In: Straw

., ed. Diseases of Swine. 8th ed. Ames, IA: Iowa State University Press, 1999:695–712.

16.

Foster

. Pericardial myxoid liposarcoma in a common eland (Taurotragus oryx). J Comp Pathol 2011; 145:103–106.

17.

Frase

. Metastasising liposarcoma of bone in a young dog. Vet Rec 2009;164:372–373.

18.

Fuentealba

Blue-McLendon

. Liposarcoma arising from the mandibular bone marrow in a ferret. Can Vet J 1995;36:779–780.

19.

Galofaro

. Primary pleomorphic liposarcoma of the liver in a dog. Pol J Vet Sci 2008;11:385–388.

20.

Gardhouse

. Diagnosis and successful surgical treatment of an unusual inguinal liposarcoma in a pet ferret (Mustela putorius furo). Can Vet J 2013;54:739–742.

21.

Ginn

. Skin and appendages. In: Maxie

, ed. Jubb, Kennedy, and Palmer’s Pathology of Domestic Animals. 5th ed. Philadelphia, PA: Saunders, 2007:553–781.

22.

Goldschmidt

Hendrick

. Tumors of the skin and soft tissues. In: Meuten

, ed. Tumors in Domestic Animals. 4th ed. Ames, IA: Iowa State University Press, 2002:119–198.

23.

Hahn

Fletcher

. Primary mediastinal liposarcoma: clinicopathologic analysis of 24 cases. Am J Surg Pathol 2007; 31:1868–1874.

24.

Hershey

. Inhalation chemotherapy for macroscopic primary or metastatic lung tumors: proof of principle using dogs with spontaneously occurring tumors as a model. Clin Cancer Res 1999;5:2653–2659.

25.

Hobert

. Infiltrative lipoma compressing the spinal cord in 2 large-breed dogs. Can Vet J 2013;54:74–78.

26.

Hoffman

. New frontiers in the treatment of liposarcoma, a therapeutically resistant malignant cohort. Drug Resist Updat 2011;14:52–66.

27.

Kilpatrick

. The clinicopathologic spectrum of myxoid and round cell liposarcoma. A study of 95 cases. Cancer 1996;77:1450–1458.

28.

Kim

. Infiltrative lipoma in cervical bones in a dog. J Vet Med Sci 2005;67:1043–1046.

29.

Kondo

. Cranial mediastinal liposarcoma in a horse. Vet Pathol 2012;49:1040–1042.

30.

Kwon

. Round cell variant of myxoid liposarcoma in a Japanese Macaque (Macaca fuscata). Vet Pathol 2007;44:229–232.

31.

Lee Gross

. Mesenchimal neoplasms and other tumors. In: Lee Gross

., ed. Skin Diseases of the Dog and Cat: Clinical and Histopathologic Diagnosis. 2nd ed. Oxford, UK: Blackwell, 2005:709–734.

32.

Lewis

. Extradural spinal liposarcoma in a dog. J Am Vet Med Assoc 1991;199:1606–1607.

33.

Masserdotti

. Use of Oil Red O stain in the cytologic diagnosis of canine liposarcoma. Vet Clin Pathol 2006;35:37–41.

34.

McCarthy

. Liposarcoma associated with a glass foreign body in a dog. J Am Vet Med Assoc 1996;209:612–614.

35.

Messick

Radin

. Cytologic, histologic, and ultrastructural characteristics of a canine myxoid liposarcoma. Vet Pathol 1989;26:520–522.

36.

Mohiddin

Ramakrishna

. Liposarcoma in a fowl. Avian Dis 1972;16:680–684.

37.

Montinaro

Boston

. Tongue rotation for reconstruction after rostral hemiglossectomy for excision of a liposarcoma of the rostral quadrant of the tongue in a dog. Can Vet J 2013;54:591–594.

38.

Murphey

. World Health Organization classification of bone and soft tissue tumors: modifications and implications for radiologists. Semin Musculoskelet Radiol 2007;11:201–214.

39.

Newman

Rohrbach

. Pot-bellied pig neoplasia: a retrospective case series (2004–2011). J Vet Diagn Invest 2012;24:1008–1013.

40.

Ogihara

. Lymphoid neoplasms in swine. J Vet Med Sci 2012;74:149–154.

41.

Oliveira

Nascimento

. Pleomorphic liposarcoma. Semin Diagn Pathol 2001;18:274–285.

42.

Piseddu

. Cytologic, histologic, and immunohistochemical features of lingual liposarcoma in a dog. Vet Clin Pathol 2011;40:393–397.

43.

Quinton

. A case of well-differentiated palpebral liposarcoma in a Guinea pig (Cavia porcellus). Vet Ophthalmol 2013;16(Suppl 1):155–159.

44.

Raskin

. Skin and subcutaneous tissues. In: Raskin

Meyer

, ed. Canine and Feline Cytology: A Color Atlas and Interpretation Guide. 2nd ed. St. Louis, MO: Elsevier, 2010:26–76.

45.

Raubenheimer

. Liposarcoma of bone marrow origin in a kudu (Tragelaphus strepsiceros). J Wildl Dis 1990;26:271–274.

46.

Reece

. Observations on naturally occurring neoplasms in birds in the state of Victoria, Australia. Avian Pathol 1992;21:3–32.

47.

Rodenas

. Combined use of surgery and radiation in the treatment of an intradural myxoid liposarcoma in a dog. J Am Anim Hosp Assoc 2006;42:386–391.

48.

Rodriguez

. Modeling sarcomagenesis using multipotent mesenchymal stem cells. Cell Res 2012;22:62–77.

49.

Saik

. Metastasis of a well-differentiated liposarcoma in a dog and a note on nomenclature of fatty tumours. J Comp Pathol 1987;97:369–373.

50.

Schwartz

. What is your diagnosis? Malignant liposarcoma of the right middle lung lobe. J Am Vet Med Assoc 2005;226:695–696.

51.

Shimonohara

. Naturally occurring neoplasms in pigeons in a research colony: a retrospective study. Avian Dis 2013;57:133–139.

52.

Shive

. Liposarcoma in the nasal cavity of a cow. Vet Pathol 2006;43:793–797.

53.

Sickinger

. Congenital infiltrative lipomas in a calf. J Vet Diagn Invest 2009;21:719–721.

54.

Simeonov

. Quantitative morphology in canine cutaneous soft tissue sarcomas. Vet Comp Oncol. doi:10.1111/vco.12099. Epub ahead of print.

55.

Smith

. Myxoid/round cell liposarcoma of the extremities. A clinicopathologic study of 29 cases with particular attention to extent of round cell liposarcoma. Am J Surg Pathol 1996;20:171–180.

56.

Spangler

. Primary mesenchymal (nonangiomatous/nonlymphomatous) neoplasms occurring in the canine spleen: anatomic classification, immunohistochemistry, and mitotic activity correlated with patient survival. Vet Pathol 1994;31:37–47.

57.

Stephens

. Virus-associated liposarcoma and malignant lymphoma in a kitten. J Am Vet Med Assoc 1983;183:123–125.

58.

Stevens

. Raises questions concerning liposarcomas in dogs. J Am Vet Med Assoc 2004;224:1583.

59.

Suto

. Epithelioid variant of pleomorphic liposarcoma in a heifer. J Comp Pathol 2007;137:133–136.

60.

Tallini

. Combined morphologic and karyotypic study of 28 myxoid liposarcomas. Implications for a revised morphologic typing (a report from the CHAMP Group). Am J Surg Pathol 1996;20:1047–1055.

61.

Trindade

. Lipossarcoma em caturrita (Myiopsitta monachus) [Liposarcoma in a caturrita (Myiopsitta monachus)]. Ciência Anim Bras 2010;11:971–976. Portuguese.

62.

Turnquist

Miller

. Intracranial ossifying lipoma in a juvenile pig. Vet Pathol 1993;30:580–582.

63.

Vascellari

. Liposarcoma at the site of an implanted microchip in a dog. Vet J 2004;168:188–190.

64.

von Bomhard

. Cutaneous neoplasms in pet rabbits: a retrospective study. Vet Pathol 2007;44:579–588.

65.

Wang

. Disseminated liposarcoma in a dog. J Vet Diagn Invest 2005;17:291–294.

66.

Weinstein

. Nonangiogenic and nonlymphomatous sarcomas of the canine spleen: 57 cases (1975–1987). J Am Vet Med Assoc 1989;195:784–788.

67.

Weiss

Goldblum

. Liposarcoma. In: Enzinger