doi:10.1111/jfd.12364
Journal of Fish Diseases 2016, 39, 309–315
Liposarcoma or invasive lipomatosis in flower horn fish, hybrid cichlid: clinical, radiological, ultrasonographical and histopathological study H Rahmati-Holasoo1, S Shokrpoor2, A Tavakkoli3, A Vajhi2 and H Ebrahimzadeh Mousavi1 1 Department of Aquatic Animal Health, Faculty of Veterinary Medicine, University of Tehran, Tehran, Iran 2 Department of Pathology, Faculty of Veterinary Medicine, University of Tehran, Tehran, Iran 3 Department of Surgery and Radiology, Faculty of Veterinary Medicine, University of Tehran, Tehran, Iran
Abstract
Liposarcoma or invasive lipomatosis affecting three indoor aquarium fish (flower horn fish, hybrid cichlid) is characterized, by the presence of mature adipocytes of variable sizes and by an invasive behaviour, which affected internal organs and eyes of all cases. Detailed macroscopic, radiological, ultrasonographical and histopathological features are presented. All fish had bilateral exophthalmia with some masses around the eyes. Ultrasonography confirmed the presence of hyperechoic masses in the eyes. Histopathology of all cases described the presence of variable-sized adipose cells in the eyes. The suggested diagnosis is well-differentiated liposarcoma or invasive lipomatosis. This is the first report of liposarcoma or invasive lipomatosis in flower horn fish, hybrid cichlid. Keywords: flower horn fish, invasive lipomatosis, liposarcoma.
Introduction
The flower horn fish belongs to the Cichlid family. It is believed that this fish has been emerged through selective cross-breeding of three spot cichlid, Cichlasoma trimaculatum (G€ unther), guayas cichlid, Cichlasoma festae (Boulenger) and Correspondence H Rahmati-Holasoo, Department of Aquatic Animal Health, Faculty of Veterinary Medicine, University of Tehran, P.O. Box: 14155-6453, Tehran, Iran (e-mail: rahmatih@ ut.ac.ir) Ó 2015 John Wiley & Sons Ltd
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Jingang Blood Parrot, hybrid cichlid, in 1996 (Lin et al. 2008; Rahmati-holasoo et al. 2010, 2014b). This fish is becoming increasingly popular as a pet, especially in South-East Asia and Iran (Lin et al. 2008; Rahmati-holasoo et al. 2010, 2015). Tumours arising from adipose tissue are classified as either benign (lipoma, infiltrative-invasive lipoma and angiolipoma) or malignant (liposarcoma) (Hendrick et al. 1998). Lipomas arise from mature adipocytes. Lipomas have been reported from a number of fish species including bream, Abramis brama (L.) (Mawdesley-Thomas & Bucke 1968), largemouth bass, Micropterus salmoides (Lacepede) (Mawdesley-Thomas 1972), black crappie, Pomoxis nigromaculatus (Lesueur) (Harshbarger 1972), southern bluefin tuna, Thunnus maccoyii (Castelnau) (Lester & Kelly 1983; Johnston et al. 2008), channel catfish, Ictalurus punctatus (Rafinesque) (McCoy et al. 1985), European eel, Anguilla anguilla (L.) (Easa et al. 1989a), striped mullet, Mugil cephalus (L.) (Easa, Harshbarger & Hetrick 1989b), common dab, Limanda limanda (L.) (Bruno, McVicar & Fraser 1991), striped seabream, Lithognathus mormyrus (L.) (Volpatti et al. 1998; Gomez 2009), northern bluefin tuna, Thunnus thynnus (L.) (Marino et al. 2006), European seabass, Dicentrarchus labrax (L.), (Marino et al. 2011), and molly, Poecilia velifera (Regan), (De Stefano, Bonfiglio & Montalbano 2012). Angiolipoma has been described in a male Siamese fighting fish, Betta splendens, Regan (Rahmati-Holasoo et al. 2014a). Liposarcoma is a malignant
Journal of Fish Diseases 2016, 39, 309–315
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tumour originating from adipose cells. In humans, this tumour is one of the most common malignant mesenchymal tumours (Dei Tos 2000). Among domestic animals, liposarcoma has been most frequently described in dogs (Baez et al. 2004). Liposarcomas have rarely been diagnosed in fish (Harshbarger 2001). Liposarcomas in fish have been reported in dragonet, Callionymus lyra L. (Haddow & Blake 1933), striped bream, Lithognathus mormyrus (L.) (Volpatti et al. 1998), juvenile halibut, Hippoglossus hippoglossus (L.) (Bambir et al. 2000), and clownfish, Amphiprion ocellaris Cuvier (Sharon et al. 2014). This is the first report of liposarcoma or invasive lipomatosis in flower horn fish, hybrid cichlid. Materials and methods
In August, November and December of 2013, three male flower horn fish, hybrid cichlid, were referred to the Faculty of Veterinary Medicine, University of Tehran. All of these fish had been obtained as a fry and maintained individually in an aquarium. Case 1 and Case 2 were referred with progressive bilateral exophthalmia, anorexia Ó 2015 John Wiley & Sons Ltd
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H Rahmati-Holasoo et al. Liposarcoma or invasive lipomatosis
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Figure 1 Flower horn fish, Case 1. (a) Severe bilateral exophthalmia in different views. Note the masses (arrowheads) around the eyes. (b) Right lateral digital radiograph showing a soft tissue density (arrowheads). (c) DV digital radiograph showing severe bilateral exophthalmia (arrows). (d) Dorsal ultrasonographic scan of left abdomen reveals hyperechoic foci (arrowheads) in the liver (liv). Spleen (sp). (e) Dorsal ultrasonographic scan of the kidney shows small hyperechoic dots (arrowhead) within the kidney (kid). (f) Dorsal ultrasonographic view of the right eye showing a hyperechoic mass (arrowheads).
and abnormal buoyancy. Bilateral exophthalmia started from 2 months before referral time and changed from slight form to severe exophthalmia with some masses around the base of eyes (Figs 1a & 2a). Case 3 was referred with progressive anorexia, progressive bilateral exophthalmia, large holes in the head and a small mass on the base of left eye (Fig. 3a) and increased respiratory rate. Because of aggressive behaviour of flower horn fish, all cases had been kept lonely in a separated aquarium. Water parameters of all cases were in normal range (Temperature 28–30 °C, pH 6.8– 7.4 and O2 7.7–8.1 mg L 1) at the referral time. These cases had been fed with different commercial fish feed. Fish were anaesthetized in 100 mg L 1 tricaine methane sulphonate (MS222, Finquelâ; Argent Chemical Laboratories) buffered with 200 mg L 1 sodium bicarbonate. Wet smears of gills and skin were prepared. Standard digital radiographs (DirectView Classic CR System; Kodak) were taken in right lateral and dorsoventral (DV) projections. Ultrasonography (diagnostic ultrasound machine Voluson 730 Pro; GE Medical Systems) was performed from the left side of all fish. Because Case 1 and Case 2 had
Journal of Fish Diseases 2016, 39, 309–315
The prognosis of liposarcoma is reserved, depending on the characteristics of local growth, histological structure and the risk of post-operative recurrence (Hendrick et al. 1998). In all of our cases, bilateral metastasis in eyes was seen and made it difficult to treat the fish. Acknowledgements Mr. Davood Faskhodi is thanked for assisting with the radiological images. Conflict of interest
No conflict of interest declared. References Azumi N., Curtis J., Kempson R.L. & Hendrickson M.R. (1987) Atypical and malignant neoplasms showing lipomatous differentiation. American Journal of Surgical Pathology 11, 161–183. Baez J.L., Hendrick M.J., Shofer F.S., Goldkamp C. & Sorenmo K.U. (2004) Liposarcomas in dogs: 56 cases (1989-2000). Journal of the American Veterinary Medical Association 224, 887–891. Bambir S., Helgason S., Marino F. & Macri‘ B. (2000) Some interesting tumours in fish. 11th Ljudevit Jurak International Symposium on Comparative Pathology, June 2000, Zagreb, Croatia. Bruno D.W., McVicar A.H. & Fraser C.O. (1991) Multiple lipoma in the common dab, Limanda limanda L. Journal of Applied Ichthyology 7, 238–243. Chen H.C., Pan I.J., Tu W.J., Lin W.H., Hong C.C. & Brittelli M.R. (1996) Neoplastic Response in Japanese medaka and channel catfish exposed to N-Methyl-N’-NitroN-Nitrosoguanidine. Environmental Toxicologic Pathology 24, 696–706.
Hard G.C., Williams R. & Lee J. (1979) Survey of demersal fish in Port Phillip Bay for incidence of neoplasia. Australian Journal of Marine and Freshwater Research 30, 73–79. Harshbarger J.C. (1972) Work of the registry of tumours in lower animals with emphasis on fish neoplasms. Symposia of the Zoological Society of London 30, 285–303. Harshbarger J.C. (2001) Neoplasia and developmental anomalies. In: BSAVA Manual of Ornamental Fish, 2nd edn (ed. by W.H. Wildgoose), pp. 219–224. British Small Animal Veterinary Association, Gloucester. Hendrick M.J., Mahaffey E.A., Moore F.M., Vos J.H. & Walder E.J. (1998) Tumors of adipose tissue. In: Histological Classification of Mesenchymal Tumours of Skin and Soft Tissues of Domestic Animals. 2nd Series, vol. 2 (ed. by F.Y. Schulman), pp. 19–20. Armed Forces Institute of Pathology, Washington, DC. Johnston C.J., Deveney M.R., Bayly T. & Nowak B.F. (2008) Gross and histopathological characteristics of two lipomas and a neurofibrosarcoma detected in aquacultured southern bluefin tuna, Thunnus maccoyii (Castelnau), in South Australia. Journal of Fish Diseases 31, 241–247. Kabak Y.B., Yardimci C., Okur-Gumusova S. & Gulbahar M.Y. (2011) Myxoid liposarcoma in a cat. Ankara € niversitesi Veteriner Fak€ U u ltesi Dergisi 58, 141–144. Laurino L., Furlanetto A., Orvieto E. & Dei Tos A.P. (2001) Well-differentiated liposarcoma (atypical lipomatous tumors). Seminars in Diagnostic Pathology 18, 258–262. Lester R.J.G. & Kelly W.R. (1983) Tumour-like growths from southern Australian marine fish. Tasmanian Fisheries Research 25, 27–32. Lin C.C., Hung S.W., Tu C.Y., Tsou L.T., Shieh M.T., Lin S.L., Liu P.C. & Wang W.S. (2008) Spontaneous stomach lymphoma and liver metastases in flower horn fish, hybrid cichlid. Bulletin of European Association of Fish Pathologists 28, 115–120. Marino F., Monaco S., Salvaggio A. & Macri B. (2006) Lipoma in a farmed northern bluefin tuna, Thunnus thynnus (L.). Journal of Fish Diseases 29, 697–699.
De Stefano C., Bonfiglio R. & Montalbano G. (2012) Multicentric lipoma in a molly (Poecilia velifera). Bulletin of the European Association of Fish Pathologists 32, 220–224.
Marino F., Chiofalo B., Mazzullo G. & Panebianco A. (2011) Multicentric infiltrative lipoma in a farmed Mediterranean seabass, Dicentrarchus labrax: a pathological and biochemical case study. Diseases of Aquatic Organisms 96, 259–264.
Dei Tos A.P. (2000) Liposarcomas: new entities and evolving concepts. Annals of Diagnostic Pathology 4, 252–266.
Mawdesley-Thomas L.E. (1972) Some tumours of fish. Symposia of the Zoological Society of London 30, 191–283.
Easa M.E.S., Faisal M., Harshbarger J.C. & Hetrick F.M. (1989a) A pseudocystic lipoma in the European eel, Anguilla anguilla. Journal of Applied Ichthyology 5, 85–87.
Mawdesley-Thomas L.E. & Bucke D. (1968) A lipoma in a bream, Abramis brama (L.). Veterinary Record 82, 673–674.
Easa M.E.S., Harshbarger J.C. & Hetrick F.M. (1989b) Hypodermal lipoma in a striped (grey) mullet, Mugil cephalus. Diseases of Aquatic Organisms 6, 157–160. Gomez S. (2009) Multiple dermal lipomas in farmed striped seabream Lithognathus mormyrus on the Spanish Mediterranean coast. Diseases of Aquatic Organisms 85, 77–79. Haddow A. & Blake I. (1933) Neoplasms in fish: a report of six cases with a summary of the literature. The Journal of Pathology and Bacteriology 36, 41–47. Ó 2015 John Wiley & Sons Ltd
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McCoy C.P., Bowser P.R., Steeby J., Bleau M. & Schwedler T.E. (1985) Lipoma in channel catfish, Ictalurus punctatus (Rafinesque). Journal of Wildlife Diseases 21, 74–76. Novotny L., Halouzka R., Matlova L., Vavra O., Bartosova L., Slany M. & Pavlik I. (2010) Morphology and distribution of granulomatous inflammation in freshwater ornamental fish infected with mycobacteria. Journal of Fish Diseases 33, 947–955. Rahmati-holasoo H., Hobbenaghi R., Tukmechi A., Seyrafi R., Homayounimehr A. & Ghavami R. (2010) Lymphocystis in
Journal of Fish Diseases 2016, 39, 309–315
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greasy wax-like areas were found on the ventral surface of posterior kidney (Fig. 4c). On the heart of Case 1 and Case 3 and spleen of Case 3, small white to yellowish spots were observed (Fig. 3d). Also, fatty mass were seen on the base of eyes of 312
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Ó 2015 John Wiley & Sons Ltd
H Rahmati-Holasoo et al. Liposarcoma or invasive lipomatosis
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Figure 3 Flower horn fish, Case 3. (a) Slight bilateral exophthalmia and three large holes in the head (H). Small white mass on the ventral surface of left eye is seen (arrowhead). (b) Right lateral digital radiograph showing a soft tissue density (arrowheads). (c) Dorsal ultrasonographic scan of left abdomen reveals hyperechoic parts (arrowheads) in the liver (liv) and hyperechoic dots in the spleen (Sp). Urinary bladder (UB). (d) Gross necropsy image showing small (white arrowheads) to large (black arrowheads) multifocal white to yellowish foci in the liver and whitish foci on the surface of heart (white arrows) and spleen (black arrow). F (fatty mass). (e) Variable-sized adipose cells are seen in the liver (B) and around pancreatic cells (A). (f) Aggregation of atypical lipocytes (arrows) in the kidney and subcapsule of kidney (H&E).
Figure 4 Flower horn fish, Case 1. (a) Transverse ultrasonographic view of the right eye showing hyperechoic mass (arrowheads). (b) Gross necropsy image showing diffuse and multifocal (arrowheads) whitish parts in the liver. Fat (F) and gonad (G). (c) Gross necropsy image showing small greasy wax-like areas on the ventral surface of posterior kidney (arrowheads). Light reflection (L) and urinary bladder (UB). (d) Lipocytes surrounding the optic nerve (ON) and peripheral nerve trunk (N) of eye. Higher magnification of atypical lipocytes (insert) (H&E).
all cases. No internal parasites were observed in Case 1 and Case 2. Hexamita sp. in the intestine of Case 3 was found. Histologically, lipocytes surrounded the internal organs and invaded the liver, eye and subcapsule of
H Rahmati-Holasoo et al. Liposarcoma or invasive lipomatosis
Journal of Fish Diseases 2016, 39, 309–315
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Figure 5 Flower horn fish, Case 1. (a) Variable-sized adipose cells are present in the liver (L) and associated pancreatic tissue (P). (b) Adipose cells (*) surround the kidney (K) and aggregation of atypical lipocytes in subcapsule of kidney (arrows) are seen. Corpuscle of Stannius (Cs). (c) Lipocytes around the bulbus arteriosus (BA).
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kidney. In the liver of all cases, lipocytes were present in large areas (Fig. 5a) associated with localized hepatocellular atrophy and necrosis. These cells were also surrounding and within regions of pancreatic cells (Fig. 3e & 5a). Microscopically, lipocytes surrounded the kidney (Fig. 5b) and heart (Fig. 5c) of Case 1 and Case 3. Aggregation of atypical lipocytes in spleen of Case 3 (not shown) and subcapsule of kidney of Case 1 and Case 3 were observed (Fig. 3f & 5b). Related to the finding of exophthalmia, similar adipose cells surrounded the orbit and optic nerve (Fig. 4d) and invaded the adjacent muscular tissue (not shown). Also lipocytes were observed around the choroid, hyaline cartilage of sclera (not shown) and behind the retina (Fig. 2f). The lipocytes were characterized by variability in size; most were well-differentiated adipocyte-type cells. Some of the cells exhibited a single, large, clear and intracytoplasmic vacuole that displaced the nucleus to the periphery. There was no evidence of mitotic figures. Discussion
Lipomas have been reported in a large number of fish species (Easa et al. 1989a,b; Marino et al. 2006; Gomez 2009; De Stefano et al. 2012). Dermis-associated lipomas have been reported to infiltrate muscle tissue (Hard, Williams & Lee 1979; McCoy et al. 1985; Johnston et al. 2008; Marino et al. 2011) without invading internal organs, and the occurrences were interpreted as benign but, in our study, the lipocytes invaded some internal Ó 2015 John Wiley & Sons Ltd
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organs and eye tissues. Lipomatosis, an overgrowth of mature fat, has been reported in freshwater ornamental fish, associated with mycobacterial infection (Novotny et al. 2010). Lipomatosis involves subcutaneous tissue and muscle, but has not been reported to involve nerves (Sharon et al. 2014). In humans, well-differentiated liposarcomas account for about 40–45% of all liposarcomas (Laurino et al. 2001). Mitotic figures are scarce in well-differentiated liposarcoma (Azumi et al. 1987; Yuri et al. 2011; Sharon et al. 2014) and were not observed in our study. We report the occurrence of what may be well-differentiated liposarcoma in three flower horn fish, hybrid cichlid. The simultaneous occurrence of the tumour in different, distant organs strongly suggests metastasis as also observed with clownfish, A. ocellaris liposarcoma (Sharon et al. 2014). Because well-defined cluster of lipoblasts with characteristic nuclear features was not evident in our case study, we cannot exclude a diagnosis of invasive lipomatosis. Nevertheless, this study is the first to suggest radiography and ultrasonography for diagnosis of liposarcoma or invasive lipomatosis in internal organs of fish. The aetiology of lipoma development is unknown. Errors in fat metabolism, endocrine or neurological disorders (Easa et al. 1989b), dysraphic status of bone (when lipomas arise close to the bone) (Marino et al. 2006) and exposure to N-methyl-N’-nitro-N-nitrosoguanidine (Chen et al. 1996) have been proposed as possible causes. In veterinary literature, vaccine-associated liposarcoma is a significant problem in veterinary medicine (Kabak et al. 2011).
Journal of Fish Diseases 2016, 39, 309–315
The prognosis of liposarcoma is reserved, depending on the characteristics of local growth, histological structure and the risk of post-operative recurrence (Hendrick et al. 1998). In all of our cases, bilateral metastasis in eyes was seen and made it difficult to treat the fish. Acknowledgements Mr. Davood Faskhodi is thanked for assisting with the radiological images. Conflict of interest
No conflict of interest declared. References Azumi N., Curtis J., Kempson R.L. & Hendrickson M.R. (1987) Atypical and malignant neoplasms showing lipomatous differentiation. American Journal of Surgical Pathology 11, 161–183. Baez J.L., Hendrick M.J., Shofer F.S., Goldkamp C. & Sorenmo K.U. (2004) Liposarcomas in dogs: 56 cases (1989-2000). Journal of the American Veterinary Medical Association 224, 887–891. Bambir S., Helgason S., Marino F. & Macri‘ B. (2000) Some interesting tumours in fish. 11th Ljudevit Jurak International Symposium on Comparative Pathology, June 2000, Zagreb, Croatia. Bruno D.W., McVicar A.H. & Fraser C.O. (1991) Multiple lipoma in the common dab, Limanda limanda L. Journal of Applied Ichthyology 7, 238–243. Chen H.C., Pan I.J., Tu W.J., Lin W.H., Hong C.C. & Brittelli M.R. (1996) Neoplastic Response in Japanese medaka and channel catfish exposed to N-Methyl-N’-NitroN-Nitrosoguanidine. Environmental Toxicologic Pathology 24, 696–706.
Hard G.C., Williams R. & Lee J. (1979) Survey of demersal fish in Port Phillip Bay for incidence of neoplasia. Australian Journal of Marine and Freshwater Research 30, 73–79. Harshbarger J.C. (1972) Work of the registry of tumours in lower animals with emphasis on fish neoplasms. Symposia of the Zoological Society of London 30, 285–303. Harshbarger J.C. (2001) Neoplasia and developmental anomalies. In: BSAVA Manual of Ornamental Fish, 2nd edn (ed. by W.H. Wildgoose), pp. 219–224. British Small Animal Veterinary Association, Gloucester. Hendrick M.J., Mahaffey E.A., Moore F.M., Vos J.H. & Walder E.J. (1998) Tumors of adipose tissue. In: Histological Classification of Mesenchymal Tumours of Skin and Soft Tissues of Domestic Animals. 2nd Series, vol. 2 (ed. by F.Y. Schulman), pp. 19–20. Armed Forces Institute of Pathology, Washington, DC. Johnston C.J., Deveney M.R., Bayly T. & Nowak B.F. (2008) Gross and histopathological characteristics of two lipomas and a neurofibrosarcoma detected in aquacultured southern bluefin tuna, Thunnus maccoyii (Castelnau), in South Australia. Journal of Fish Diseases 31, 241–247. Kabak Y.B., Yardimci C., Okur-Gumusova S. & Gulbahar M.Y. (2011) Myxoid liposarcoma in a cat. Ankara € niversitesi Veteriner Fak€ U u ltesi Dergisi 58, 141–144. Laurino L., Furlanetto A., Orvieto E. & Dei Tos A.P. (2001) Well-differentiated liposarcoma (atypical lipomatous tumors). Seminars in Diagnostic Pathology 18, 258–262. Lester R.J.G. & Kelly W.R. (1983) Tumour-like growths from southern Australian marine fish. Tasmanian Fisheries Research 25, 27–32. Lin C.C., Hung S.W., Tu C.Y., Tsou L.T., Shieh M.T., Lin S.L., Liu P.C. & Wang W.S. (2008) Spontaneous stomach lymphoma and liver metastases in flower horn fish, hybrid cichlid. Bulletin of European Association of Fish Pathologists 28, 115–120. Marino F., Monaco S., Salvaggio A. & Macri B. (2006) Lipoma in a farmed northern bluefin tuna, Thunnus thynnus (L.). Journal of Fish Diseases 29, 697–699.
De Stefano C., Bonfiglio R. & Montalbano G. (2012) Multicentric lipoma in a molly (Poecilia velifera). Bulletin of the European Association of Fish Pathologists 32, 220–224.
Marino F., Chiofalo B., Mazzullo G. & Panebianco A. (2011) Multicentric infiltrative lipoma in a farmed Mediterranean seabass, Dicentrarchus labrax: a pathological and biochemical case study. Diseases of Aquatic Organisms 96, 259–264.
Dei Tos A.P. (2000) Liposarcomas: new entities and evolving concepts. Annals of Diagnostic Pathology 4, 252–266.
Mawdesley-Thomas L.E. (1972) Some tumours of fish. Symposia of the Zoological Society of London 30, 191–283.
Easa M.E.S., Faisal M., Harshbarger J.C. & Hetrick F.M. (1989a) A pseudocystic lipoma in the European eel, Anguilla anguilla. Journal of Applied Ichthyology 5, 85–87.
Mawdesley-Thomas L.E. & Bucke D. (1968) A lipoma in a bream, Abramis brama (L.). Veterinary Record 82, 673–674.
Easa M.E.S., Harshbarger J.C. & Hetrick F.M. (1989b) Hypodermal lipoma in a striped (grey) mullet, Mugil cephalus. Diseases of Aquatic Organisms 6, 157–160. Gomez S. (2009) Multiple dermal lipomas in farmed striped seabream Lithognathus mormyrus on the Spanish Mediterranean coast. Diseases of Aquatic Organisms 85, 77–79. Haddow A. & Blake I. (1933) Neoplasms in fish: a report of six cases with a summary of the literature. The Journal of Pathology and Bacteriology 36, 41–47. Ó 2015 John Wiley & Sons Ltd
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McCoy C.P., Bowser P.R., Steeby J., Bleau M. & Schwedler T.E. (1985) Lipoma in channel catfish, Ictalurus punctatus (Rafinesque). Journal of Wildlife Diseases 21, 74–76. Novotny L., Halouzka R., Matlova L., Vavra O., Bartosova L., Slany M. & Pavlik I. (2010) Morphology and distribution of granulomatous inflammation in freshwater ornamental fish infected with mycobacteria. Journal of Fish Diseases 33, 947–955. Rahmati-holasoo H., Hobbenaghi R., Tukmechi A., Seyrafi R., Homayounimehr A. & Ghavami R. (2010) Lymphocystis in
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a flower horn fish. Comparative Clinical Pathology 19, 433– 435. Rahmati-Holasoo H., Alishahi M., Shokrpoor S., Jangarannejad A. & Mohammadian B. (2014a) Invasion of melanoma to angiolipoma in a male Siamese fighting fish, Betta splendens, Regan. Journal of Fish Diseases (in press) doi:10.1111/jfd.12301. Rahmati-holasoo H., Ebrahimzadeh Mousavi H., Vajhi A., Shokrpoor S., Tavakkoli A., Mirdamadi M.A. & Fayyaz S. (2015) Polycystic liver in flower horn fish, hybrid cichlid. Journal of Fish Diseases 38, 325–328 doi:10.1111/ jfd.12245. Rahmati-holasoo H., Masoudifard M., Ebrahimzadeh Mousavi H., Shokrpoor S., Tavakkoli A. & Farazandemehr M.S. (2014b) Cystic lesions in the kidney of flower horn fish, hybrid cichlid. Journal of Fish Diseases (in press) Doi:10.1111/jfd.12292.
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Sharon G., Benharroch D., Kachko L., Reis-Hevlin N. & Zilberg D. (2014) Liposarcoma in clownfish, Amphiprion ocellaris Cuvier, produced in indoor aquaculture. Journal of Fish Diseases (in press) doi:10.1111/jfd.12269. Volpatti D., Patarnello P., Novelli A., D’Angelo L., Musetti R. & Galeotti M. (1998) Lipoma, fibrolipoma, liposarcoma in mormore, Lithognatus mormyrus (L.) allevate: osservazioni istologiche e ultrastrutturali. V convegno, Societa Italiana di Patologia Ittica (SIPI), Roma, Italy. Yuri T., Miyaso T., Kitade H., Takasu K., Shikata N., Takada H. & Tsubura A. (2011) Well differentiated liposarcoma, an atypical lipomatous tumor, of the mesentery: a case report and review of the literature. Case Reports in Oncology 4, 178–185. Received: 23 September 2014 Revision received: 2 February 2015 Accepted: 2 February 2015
Journal of Fish Diseases 2016, 39, 309–315
Liposarcoma or invasive lipomatosis in flower horn fish, hybrid cichlid: clinical, radiological, ultrasonographical and histopathological study H Rahmati-Holasoo1, S Shokrpoor2, A Tavakkoli3, A Vajhi2 and H Ebrahimzadeh Mousavi1 1 Department of Aquatic Animal Health, Faculty of Veterinary Medicine, University of Tehran, Tehran, Iran 2 Department of Pathology, Faculty of Veterinary Medicine, University of Tehran, Tehran, Iran 3 Department of Surgery and Radiology, Faculty of Veterinary Medicine, University of Tehran, Tehran, Iran
Abstract
Liposarcoma or invasive lipomatosis affecting three indoor aquarium fish (flower horn fish, hybrid cichlid) is characterized, by the presence of mature adipocytes of variable sizes and by an invasive behaviour, which affected internal organs and eyes of all cases. Detailed macroscopic, radiological, ultrasonographical and histopathological features are presented. All fish had bilateral exophthalmia with some masses around the eyes. Ultrasonography confirmed the presence of hyperechoic masses in the eyes. Histopathology of all cases described the presence of variable-sized adipose cells in the eyes. The suggested diagnosis is well-differentiated liposarcoma or invasive lipomatosis. This is the first report of liposarcoma or invasive lipomatosis in flower horn fish, hybrid cichlid. Keywords: flower horn fish, invasive lipomatosis, liposarcoma.
Introduction
The flower horn fish belongs to the Cichlid family. It is believed that this fish has been emerged through selective cross-breeding of three spot cichlid, Cichlasoma trimaculatum (G€ unther), guayas cichlid, Cichlasoma festae (Boulenger) and Correspondence H Rahmati-Holasoo, Department of Aquatic Animal Health, Faculty of Veterinary Medicine, University of Tehran, P.O. Box: 14155-6453, Tehran, Iran (e-mail: rahmatih@ ut.ac.ir) Ó 2015 John Wiley & Sons Ltd
309
Jingang Blood Parrot, hybrid cichlid, in 1996 (Lin et al. 2008; Rahmati-holasoo et al. 2010, 2014b). This fish is becoming increasingly popular as a pet, especially in South-East Asia and Iran (Lin et al. 2008; Rahmati-holasoo et al. 2010, 2015). Tumours arising from adipose tissue are classified as either benign (lipoma, infiltrative-invasive lipoma and angiolipoma) or malignant (liposarcoma) (Hendrick et al. 1998). Lipomas arise from mature adipocytes. Lipomas have been reported from a number of fish species including bream, Abramis brama (L.) (Mawdesley-Thomas & Bucke 1968), largemouth bass, Micropterus salmoides (Lacepede) (Mawdesley-Thomas 1972), black crappie, Pomoxis nigromaculatus (Lesueur) (Harshbarger 1972), southern bluefin tuna, Thunnus maccoyii (Castelnau) (Lester & Kelly 1983; Johnston et al. 2008), channel catfish, Ictalurus punctatus (Rafinesque) (McCoy et al. 1985), European eel, Anguilla anguilla (L.) (Easa et al. 1989a), striped mullet, Mugil cephalus (L.) (Easa, Harshbarger & Hetrick 1989b), common dab, Limanda limanda (L.) (Bruno, McVicar & Fraser 1991), striped seabream, Lithognathus mormyrus (L.) (Volpatti et al. 1998; Gomez 2009), northern bluefin tuna, Thunnus thynnus (L.) (Marino et al. 2006), European seabass, Dicentrarchus labrax (L.), (Marino et al. 2011), and molly, Poecilia velifera (Regan), (De Stefano, Bonfiglio & Montalbano 2012). Angiolipoma has been described in a male Siamese fighting fish, Betta splendens, Regan (Rahmati-Holasoo et al. 2014a). Liposarcoma is a malignant
Journal of Fish Diseases 2016, 39, 309–315
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tumour originating from adipose cells. In humans, this tumour is one of the most common malignant mesenchymal tumours (Dei Tos 2000). Among domestic animals, liposarcoma has been most frequently described in dogs (Baez et al. 2004). Liposarcomas have rarely been diagnosed in fish (Harshbarger 2001). Liposarcomas in fish have been reported in dragonet, Callionymus lyra L. (Haddow & Blake 1933), striped bream, Lithognathus mormyrus (L.) (Volpatti et al. 1998), juvenile halibut, Hippoglossus hippoglossus (L.) (Bambir et al. 2000), and clownfish, Amphiprion ocellaris Cuvier (Sharon et al. 2014). This is the first report of liposarcoma or invasive lipomatosis in flower horn fish, hybrid cichlid. Materials and methods
In August, November and December of 2013, three male flower horn fish, hybrid cichlid, were referred to the Faculty of Veterinary Medicine, University of Tehran. All of these fish had been obtained as a fry and maintained individually in an aquarium. Case 1 and Case 2 were referred with progressive bilateral exophthalmia, anorexia Ó 2015 John Wiley & Sons Ltd
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Figure 1 Flower horn fish, Case 1. (a) Severe bilateral exophthalmia in different views. Note the masses (arrowheads) around the eyes. (b) Right lateral digital radiograph showing a soft tissue density (arrowheads). (c) DV digital radiograph showing severe bilateral exophthalmia (arrows). (d) Dorsal ultrasonographic scan of left abdomen reveals hyperechoic foci (arrowheads) in the liver (liv). Spleen (sp). (e) Dorsal ultrasonographic scan of the kidney shows small hyperechoic dots (arrowhead) within the kidney (kid). (f) Dorsal ultrasonographic view of the right eye showing a hyperechoic mass (arrowheads).
and abnormal buoyancy. Bilateral exophthalmia started from 2 months before referral time and changed from slight form to severe exophthalmia with some masses around the base of eyes (Figs 1a & 2a). Case 3 was referred with progressive anorexia, progressive bilateral exophthalmia, large holes in the head and a small mass on the base of left eye (Fig. 3a) and increased respiratory rate. Because of aggressive behaviour of flower horn fish, all cases had been kept lonely in a separated aquarium. Water parameters of all cases were in normal range (Temperature 28–30 °C, pH 6.8– 7.4 and O2 7.7–8.1 mg L 1) at the referral time. These cases had been fed with different commercial fish feed. Fish were anaesthetized in 100 mg L 1 tricaine methane sulphonate (MS222, Finquelâ; Argent Chemical Laboratories) buffered with 200 mg L 1 sodium bicarbonate. Wet smears of gills and skin were prepared. Standard digital radiographs (DirectView Classic CR System; Kodak) were taken in right lateral and dorsoventral (DV) projections. Ultrasonography (diagnostic ultrasound machine Voluson 730 Pro; GE Medical Systems) was performed from the left side of all fish. Because Case 1 and Case 2 had
Journal of Fish Diseases 2016, 39, 309–315
The prognosis of liposarcoma is reserved, depending on the characteristics of local growth, histological structure and the risk of post-operative recurrence (Hendrick et al. 1998). In all of our cases, bilateral metastasis in eyes was seen and made it difficult to treat the fish. Acknowledgements Mr. Davood Faskhodi is thanked for assisting with the radiological images. Conflict of interest
No conflict of interest declared. References Azumi N., Curtis J., Kempson R.L. & Hendrickson M.R. (1987) Atypical and malignant neoplasms showing lipomatous differentiation. American Journal of Surgical Pathology 11, 161–183. Baez J.L., Hendrick M.J., Shofer F.S., Goldkamp C. & Sorenmo K.U. (2004) Liposarcomas in dogs: 56 cases (1989-2000). Journal of the American Veterinary Medical Association 224, 887–891. Bambir S., Helgason S., Marino F. & Macri‘ B. (2000) Some interesting tumours in fish. 11th Ljudevit Jurak International Symposium on Comparative Pathology, June 2000, Zagreb, Croatia. Bruno D.W., McVicar A.H. & Fraser C.O. (1991) Multiple lipoma in the common dab, Limanda limanda L. Journal of Applied Ichthyology 7, 238–243. Chen H.C., Pan I.J., Tu W.J., Lin W.H., Hong C.C. & Brittelli M.R. (1996) Neoplastic Response in Japanese medaka and channel catfish exposed to N-Methyl-N’-NitroN-Nitrosoguanidine. Environmental Toxicologic Pathology 24, 696–706.
Hard G.C., Williams R. & Lee J. (1979) Survey of demersal fish in Port Phillip Bay for incidence of neoplasia. Australian Journal of Marine and Freshwater Research 30, 73–79. Harshbarger J.C. (1972) Work of the registry of tumours in lower animals with emphasis on fish neoplasms. Symposia of the Zoological Society of London 30, 285–303. Harshbarger J.C. (2001) Neoplasia and developmental anomalies. In: BSAVA Manual of Ornamental Fish, 2nd edn (ed. by W.H. Wildgoose), pp. 219–224. British Small Animal Veterinary Association, Gloucester. Hendrick M.J., Mahaffey E.A., Moore F.M., Vos J.H. & Walder E.J. (1998) Tumors of adipose tissue. In: Histological Classification of Mesenchymal Tumours of Skin and Soft Tissues of Domestic Animals. 2nd Series, vol. 2 (ed. by F.Y. Schulman), pp. 19–20. Armed Forces Institute of Pathology, Washington, DC. Johnston C.J., Deveney M.R., Bayly T. & Nowak B.F. (2008) Gross and histopathological characteristics of two lipomas and a neurofibrosarcoma detected in aquacultured southern bluefin tuna, Thunnus maccoyii (Castelnau), in South Australia. Journal of Fish Diseases 31, 241–247. Kabak Y.B., Yardimci C., Okur-Gumusova S. & Gulbahar M.Y. (2011) Myxoid liposarcoma in a cat. Ankara € niversitesi Veteriner Fak€ U u ltesi Dergisi 58, 141–144. Laurino L., Furlanetto A., Orvieto E. & Dei Tos A.P. (2001) Well-differentiated liposarcoma (atypical lipomatous tumors). Seminars in Diagnostic Pathology 18, 258–262. Lester R.J.G. & Kelly W.R. (1983) Tumour-like growths from southern Australian marine fish. Tasmanian Fisheries Research 25, 27–32. Lin C.C., Hung S.W., Tu C.Y., Tsou L.T., Shieh M.T., Lin S.L., Liu P.C. & Wang W.S. (2008) Spontaneous stomach lymphoma and liver metastases in flower horn fish, hybrid cichlid. Bulletin of European Association of Fish Pathologists 28, 115–120. Marino F., Monaco S., Salvaggio A. & Macri B. (2006) Lipoma in a farmed northern bluefin tuna, Thunnus thynnus (L.). Journal of Fish Diseases 29, 697–699.
De Stefano C., Bonfiglio R. & Montalbano G. (2012) Multicentric lipoma in a molly (Poecilia velifera). Bulletin of the European Association of Fish Pathologists 32, 220–224.
Marino F., Chiofalo B., Mazzullo G. & Panebianco A. (2011) Multicentric infiltrative lipoma in a farmed Mediterranean seabass, Dicentrarchus labrax: a pathological and biochemical case study. Diseases of Aquatic Organisms 96, 259–264.
Dei Tos A.P. (2000) Liposarcomas: new entities and evolving concepts. Annals of Diagnostic Pathology 4, 252–266.
Mawdesley-Thomas L.E. (1972) Some tumours of fish. Symposia of the Zoological Society of London 30, 191–283.
Easa M.E.S., Faisal M., Harshbarger J.C. & Hetrick F.M. (1989a) A pseudocystic lipoma in the European eel, Anguilla anguilla. Journal of Applied Ichthyology 5, 85–87.
Mawdesley-Thomas L.E. & Bucke D. (1968) A lipoma in a bream, Abramis brama (L.). Veterinary Record 82, 673–674.
Easa M.E.S., Harshbarger J.C. & Hetrick F.M. (1989b) Hypodermal lipoma in a striped (grey) mullet, Mugil cephalus. Diseases of Aquatic Organisms 6, 157–160. Gomez S. (2009) Multiple dermal lipomas in farmed striped seabream Lithognathus mormyrus on the Spanish Mediterranean coast. Diseases of Aquatic Organisms 85, 77–79. Haddow A. & Blake I. (1933) Neoplasms in fish: a report of six cases with a summary of the literature. The Journal of Pathology and Bacteriology 36, 41–47. Ó 2015 John Wiley & Sons Ltd
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McCoy C.P., Bowser P.R., Steeby J., Bleau M. & Schwedler T.E. (1985) Lipoma in channel catfish, Ictalurus punctatus (Rafinesque). Journal of Wildlife Diseases 21, 74–76. Novotny L., Halouzka R., Matlova L., Vavra O., Bartosova L., Slany M. & Pavlik I. (2010) Morphology and distribution of granulomatous inflammation in freshwater ornamental fish infected with mycobacteria. Journal of Fish Diseases 33, 947–955. Rahmati-holasoo H., Hobbenaghi R., Tukmechi A., Seyrafi R., Homayounimehr A. & Ghavami R. (2010) Lymphocystis in
Journal of Fish Diseases 2016, 39, 309–315
(a)
(d)
(e)
(f)
(a)
(b)
greasy wax-like areas were found on the ventral surface of posterior kidney (Fig. 4c). On the heart of Case 1 and Case 3 and spleen of Case 3, small white to yellowish spots were observed (Fig. 3d). Also, fatty mass were seen on the base of eyes of 312
(b)
(c)
(c)
Ó 2015 John Wiley & Sons Ltd
H Rahmati-Holasoo et al. Liposarcoma or invasive lipomatosis
(d)
Figure 3 Flower horn fish, Case 3. (a) Slight bilateral exophthalmia and three large holes in the head (H). Small white mass on the ventral surface of left eye is seen (arrowhead). (b) Right lateral digital radiograph showing a soft tissue density (arrowheads). (c) Dorsal ultrasonographic scan of left abdomen reveals hyperechoic parts (arrowheads) in the liver (liv) and hyperechoic dots in the spleen (Sp). Urinary bladder (UB). (d) Gross necropsy image showing small (white arrowheads) to large (black arrowheads) multifocal white to yellowish foci in the liver and whitish foci on the surface of heart (white arrows) and spleen (black arrow). F (fatty mass). (e) Variable-sized adipose cells are seen in the liver (B) and around pancreatic cells (A). (f) Aggregation of atypical lipocytes (arrows) in the kidney and subcapsule of kidney (H&E).
Figure 4 Flower horn fish, Case 1. (a) Transverse ultrasonographic view of the right eye showing hyperechoic mass (arrowheads). (b) Gross necropsy image showing diffuse and multifocal (arrowheads) whitish parts in the liver. Fat (F) and gonad (G). (c) Gross necropsy image showing small greasy wax-like areas on the ventral surface of posterior kidney (arrowheads). Light reflection (L) and urinary bladder (UB). (d) Lipocytes surrounding the optic nerve (ON) and peripheral nerve trunk (N) of eye. Higher magnification of atypical lipocytes (insert) (H&E).
all cases. No internal parasites were observed in Case 1 and Case 2. Hexamita sp. in the intestine of Case 3 was found. Histologically, lipocytes surrounded the internal organs and invaded the liver, eye and subcapsule of
H Rahmati-Holasoo et al. Liposarcoma or invasive lipomatosis
Journal of Fish Diseases 2016, 39, 309–315
(a)
Figure 5 Flower horn fish, Case 1. (a) Variable-sized adipose cells are present in the liver (L) and associated pancreatic tissue (P). (b) Adipose cells (*) surround the kidney (K) and aggregation of atypical lipocytes in subcapsule of kidney (arrows) are seen. Corpuscle of Stannius (Cs). (c) Lipocytes around the bulbus arteriosus (BA).
(c)
kidney. In the liver of all cases, lipocytes were present in large areas (Fig. 5a) associated with localized hepatocellular atrophy and necrosis. These cells were also surrounding and within regions of pancreatic cells (Fig. 3e & 5a). Microscopically, lipocytes surrounded the kidney (Fig. 5b) and heart (Fig. 5c) of Case 1 and Case 3. Aggregation of atypical lipocytes in spleen of Case 3 (not shown) and subcapsule of kidney of Case 1 and Case 3 were observed (Fig. 3f & 5b). Related to the finding of exophthalmia, similar adipose cells surrounded the orbit and optic nerve (Fig. 4d) and invaded the adjacent muscular tissue (not shown). Also lipocytes were observed around the choroid, hyaline cartilage of sclera (not shown) and behind the retina (Fig. 2f). The lipocytes were characterized by variability in size; most were well-differentiated adipocyte-type cells. Some of the cells exhibited a single, large, clear and intracytoplasmic vacuole that displaced the nucleus to the periphery. There was no evidence of mitotic figures. Discussion
Lipomas have been reported in a large number of fish species (Easa et al. 1989a,b; Marino et al. 2006; Gomez 2009; De Stefano et al. 2012). Dermis-associated lipomas have been reported to infiltrate muscle tissue (Hard, Williams & Lee 1979; McCoy et al. 1985; Johnston et al. 2008; Marino et al. 2011) without invading internal organs, and the occurrences were interpreted as benign but, in our study, the lipocytes invaded some internal Ó 2015 John Wiley & Sons Ltd
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(b)
organs and eye tissues. Lipomatosis, an overgrowth of mature fat, has been reported in freshwater ornamental fish, associated with mycobacterial infection (Novotny et al. 2010). Lipomatosis involves subcutaneous tissue and muscle, but has not been reported to involve nerves (Sharon et al. 2014). In humans, well-differentiated liposarcomas account for about 40–45% of all liposarcomas (Laurino et al. 2001). Mitotic figures are scarce in well-differentiated liposarcoma (Azumi et al. 1987; Yuri et al. 2011; Sharon et al. 2014) and were not observed in our study. We report the occurrence of what may be well-differentiated liposarcoma in three flower horn fish, hybrid cichlid. The simultaneous occurrence of the tumour in different, distant organs strongly suggests metastasis as also observed with clownfish, A. ocellaris liposarcoma (Sharon et al. 2014). Because well-defined cluster of lipoblasts with characteristic nuclear features was not evident in our case study, we cannot exclude a diagnosis of invasive lipomatosis. Nevertheless, this study is the first to suggest radiography and ultrasonography for diagnosis of liposarcoma or invasive lipomatosis in internal organs of fish. The aetiology of lipoma development is unknown. Errors in fat metabolism, endocrine or neurological disorders (Easa et al. 1989b), dysraphic status of bone (when lipomas arise close to the bone) (Marino et al. 2006) and exposure to N-methyl-N’-nitro-N-nitrosoguanidine (Chen et al. 1996) have been proposed as possible causes. In veterinary literature, vaccine-associated liposarcoma is a significant problem in veterinary medicine (Kabak et al. 2011).
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The prognosis of liposarcoma is reserved, depending on the characteristics of local growth, histological structure and the risk of post-operative recurrence (Hendrick et al. 1998). In all of our cases, bilateral metastasis in eyes was seen and made it difficult to treat the fish. Acknowledgements Mr. Davood Faskhodi is thanked for assisting with the radiological images. Conflict of interest
No conflict of interest declared. References Azumi N., Curtis J., Kempson R.L. & Hendrickson M.R. (1987) Atypical and malignant neoplasms showing lipomatous differentiation. American Journal of Surgical Pathology 11, 161–183. Baez J.L., Hendrick M.J., Shofer F.S., Goldkamp C. & Sorenmo K.U. (2004) Liposarcomas in dogs: 56 cases (1989-2000). Journal of the American Veterinary Medical Association 224, 887–891. Bambir S., Helgason S., Marino F. & Macri‘ B. (2000) Some interesting tumours in fish. 11th Ljudevit Jurak International Symposium on Comparative Pathology, June 2000, Zagreb, Croatia. Bruno D.W., McVicar A.H. & Fraser C.O. (1991) Multiple lipoma in the common dab, Limanda limanda L. Journal of Applied Ichthyology 7, 238–243. Chen H.C., Pan I.J., Tu W.J., Lin W.H., Hong C.C. & Brittelli M.R. (1996) Neoplastic Response in Japanese medaka and channel catfish exposed to N-Methyl-N’-NitroN-Nitrosoguanidine. Environmental Toxicologic Pathology 24, 696–706.
Hard G.C., Williams R. & Lee J. (1979) Survey of demersal fish in Port Phillip Bay for incidence of neoplasia. Australian Journal of Marine and Freshwater Research 30, 73–79. Harshbarger J.C. (1972) Work of the registry of tumours in lower animals with emphasis on fish neoplasms. Symposia of the Zoological Society of London 30, 285–303. Harshbarger J.C. (2001) Neoplasia and developmental anomalies. In: BSAVA Manual of Ornamental Fish, 2nd edn (ed. by W.H. Wildgoose), pp. 219–224. British Small Animal Veterinary Association, Gloucester. Hendrick M.J., Mahaffey E.A., Moore F.M., Vos J.H. & Walder E.J. (1998) Tumors of adipose tissue. In: Histological Classification of Mesenchymal Tumours of Skin and Soft Tissues of Domestic Animals. 2nd Series, vol. 2 (ed. by F.Y. Schulman), pp. 19–20. Armed Forces Institute of Pathology, Washington, DC. Johnston C.J., Deveney M.R., Bayly T. & Nowak B.F. (2008) Gross and histopathological characteristics of two lipomas and a neurofibrosarcoma detected in aquacultured southern bluefin tuna, Thunnus maccoyii (Castelnau), in South Australia. Journal of Fish Diseases 31, 241–247. Kabak Y.B., Yardimci C., Okur-Gumusova S. & Gulbahar M.Y. (2011) Myxoid liposarcoma in a cat. Ankara € niversitesi Veteriner Fak€ U u ltesi Dergisi 58, 141–144. Laurino L., Furlanetto A., Orvieto E. & Dei Tos A.P. (2001) Well-differentiated liposarcoma (atypical lipomatous tumors). Seminars in Diagnostic Pathology 18, 258–262. Lester R.J.G. & Kelly W.R. (1983) Tumour-like growths from southern Australian marine fish. Tasmanian Fisheries Research 25, 27–32. Lin C.C., Hung S.W., Tu C.Y., Tsou L.T., Shieh M.T., Lin S.L., Liu P.C. & Wang W.S. (2008) Spontaneous stomach lymphoma and liver metastases in flower horn fish, hybrid cichlid. Bulletin of European Association of Fish Pathologists 28, 115–120. Marino F., Monaco S., Salvaggio A. & Macri B. (2006) Lipoma in a farmed northern bluefin tuna, Thunnus thynnus (L.). Journal of Fish Diseases 29, 697–699.
De Stefano C., Bonfiglio R. & Montalbano G. (2012) Multicentric lipoma in a molly (Poecilia velifera). Bulletin of the European Association of Fish Pathologists 32, 220–224.
Marino F., Chiofalo B., Mazzullo G. & Panebianco A. (2011) Multicentric infiltrative lipoma in a farmed Mediterranean seabass, Dicentrarchus labrax: a pathological and biochemical case study. Diseases of Aquatic Organisms 96, 259–264.
Dei Tos A.P. (2000) Liposarcomas: new entities and evolving concepts. Annals of Diagnostic Pathology 4, 252–266.
Mawdesley-Thomas L.E. (1972) Some tumours of fish. Symposia of the Zoological Society of London 30, 191–283.
Easa M.E.S., Faisal M., Harshbarger J.C. & Hetrick F.M. (1989a) A pseudocystic lipoma in the European eel, Anguilla anguilla. Journal of Applied Ichthyology 5, 85–87.
Mawdesley-Thomas L.E. & Bucke D. (1968) A lipoma in a bream, Abramis brama (L.). Veterinary Record 82, 673–674.
Easa M.E.S., Harshbarger J.C. & Hetrick F.M. (1989b) Hypodermal lipoma in a striped (grey) mullet, Mugil cephalus. Diseases of Aquatic Organisms 6, 157–160. Gomez S. (2009) Multiple dermal lipomas in farmed striped seabream Lithognathus mormyrus on the Spanish Mediterranean coast. Diseases of Aquatic Organisms 85, 77–79. Haddow A. & Blake I. (1933) Neoplasms in fish: a report of six cases with a summary of the literature. The Journal of Pathology and Bacteriology 36, 41–47. Ó 2015 John Wiley & Sons Ltd
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McCoy C.P., Bowser P.R., Steeby J., Bleau M. & Schwedler T.E. (1985) Lipoma in channel catfish, Ictalurus punctatus (Rafinesque). Journal of Wildlife Diseases 21, 74–76. Novotny L., Halouzka R., Matlova L., Vavra O., Bartosova L., Slany M. & Pavlik I. (2010) Morphology and distribution of granulomatous inflammation in freshwater ornamental fish infected with mycobacteria. Journal of Fish Diseases 33, 947–955. Rahmati-holasoo H., Hobbenaghi R., Tukmechi A., Seyrafi R., Homayounimehr A. & Ghavami R. (2010) Lymphocystis in
Journal of Fish Diseases 2016, 39, 309–315
a flower horn fish. Comparative Clinical Pathology 19, 433– 435. Rahmati-Holasoo H., Alishahi M., Shokrpoor S., Jangarannejad A. & Mohammadian B. (2014a) Invasion of melanoma to angiolipoma in a male Siamese fighting fish, Betta splendens, Regan. Journal of Fish Diseases (in press) doi:10.1111/jfd.12301. Rahmati-holasoo H., Ebrahimzadeh Mousavi H., Vajhi A., Shokrpoor S., Tavakkoli A., Mirdamadi M.A. & Fayyaz S. (2015) Polycystic liver in flower horn fish, hybrid cichlid. Journal of Fish Diseases 38, 325–328 doi:10.1111/ jfd.12245. Rahmati-holasoo H., Masoudifard M., Ebrahimzadeh Mousavi H., Shokrpoor S., Tavakkoli A. & Farazandemehr M.S. (2014b) Cystic lesions in the kidney of flower horn fish, hybrid cichlid. Journal of Fish Diseases (in press) Doi:10.1111/jfd.12292.
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Sharon G., Benharroch D., Kachko L., Reis-Hevlin N. & Zilberg D. (2014) Liposarcoma in clownfish, Amphiprion ocellaris Cuvier, produced in indoor aquaculture. Journal of Fish Diseases (in press) doi:10.1111/jfd.12269. Volpatti D., Patarnello P., Novelli A., D’Angelo L., Musetti R. & Galeotti M. (1998) Lipoma, fibrolipoma, liposarcoma in mormore, Lithognatus mormyrus (L.) allevate: osservazioni istologiche e ultrastrutturali. V convegno, Societa Italiana di Patologia Ittica (SIPI), Roma, Italy. Yuri T., Miyaso T., Kitade H., Takasu K., Shikata N., Takada H. & Tsubura A. (2011) Well differentiated liposarcoma, an atypical lipomatous tumor, of the mesentery: a case report and review of the literature. Case Reports in Oncology 4, 178–185. Received: 23 September 2014 Revision received: 2 February 2015 Accepted: 2 February 2015
