Comp Clin Pathol DOI 10.1007/s00580-016-2295-0
BRIEF COMMUNICATION
Neoplasia in flat head grey mullet, Mugil cephalus Linnaeus, 1758 (Perciforms: Mugilidae): two case reports of myxoinflammatory fibroblastic sarcoma and leiomyoma Vijayapoopathi Singaravel 1 & Ayyaru Gopalakrishnan 1 & Kuzhanthaivel Raja 1 & Ramalingam Vijayakumar 1 & Syed Asrafuzzaman 2
Received: 18 April 2016 / Accepted: 28 June 2016 # Springer-Verlag London 2016
Abstract The presence of cutaneous neoplasms is reported in two cases of wild female grey mullet (Mugil cephalus) from Pazhayar and Parangipettai fish landing centre, southeast coast of India. A gross morphological examination case 1 revealed obvious reddish white, solitary and fleshy appearance of tumour located on behind the right-side of the anal fin, and the overlying epidermis was ulcerated, hyperemic and hyperchromatic. The tumour had a gelatinous consistency and released jelly-like matters. The tumour-affected case 2 revealed well-circumscribed, solitary and reddish fleshy appearance of tumour located on the left-side of the deep margin of the flank, the lesion covered with whitish-grey thin epidermal layer. Histolopathologically, the (case 1) tumour growth had distinct simulate bizarre tumour cells embedded in myxoid matrix with inflammatory infiltrates. The (case 2) tumour lesion showed interlacing bundles of spindled to elongated tumour cells with cigar-shaped nuclei. On the basis of the clinical and histolopathological findings, these tumours are diagnosed as myxoinflammatory fibroblastic sarcoma and leiomyoma.
Keywords Neoplasm . Mugil cephalus . Myxoinflammatory fibroblastic sarcoma . Leiomyoma
* Ayyaru Gopalakrishnan
[email protected]
1
Centre of Advanced Study in Maine Biology, Faculty of Marine Sciences, Annamalai University, Parangipettai 608 502, Tamilnadu, India
2
Department of Zoology, North Orissa University, Mayurbhanj, Baripada 757 001, Odisha, India
Introduction The flat head grey mullet, Mugil cephalus (Linnaeus 1758), belongs to the family Mugilidae. It is widely distributed in the tropical and subtropical waters worldwide and found in mari ne, est uarine and freshwater environments (Whitfield et al. 2012). Tumours arising from mesenchymal soft tissues are classified as either fibroblastic or myofibroblastic (Schlumberger and Lucke 1948; Fletcher et al. 2002). Myxoinflammatory fibroblastic sarcoma (MIFS) is a rare, distinct low-grade tumour of modified fibroblast and is characterized by myxoid stroma, inflammatory infiltrate and virocyte or ReedSternberg-like cells (Kindblom and Meis-Kindblom 2002). The soft tissue mesenchymal tumour has been reported in humans and occurs in the distal extremities (Raghavan et al. 2012). MIFS is rare tumour in lower vertebrates and has not been reported earlier in fish. However, myxoma and fibrosarcoma have been reported in fish. Fibrosarcomas are rare tumours in both higher and lower vertebrates including fish. Among fish, dermal fibrosarcoma has been reported in goldfish, Carassius auratus (Ahmed and Egusa 1980; Schamberg and Lucke 1922), three species of salmonid fish (Meyers and Hendricks 1983), yellow perch, Perca flavescens (Bowser et al. 2005), and fork-tailed catfish Hemiarius dioctes (Dennis and Diggles 2015). Myxomas have rarely been diagnosed in fish (Keller et al. 2011). Myxomas in fish have been reported in California yellowtail, Seriola lalandi (Keller et al. 2011), and blackfin sea catfish, Arius jella (Singaravel et al. 2016). Leiomyoma is a rare benign soft tissue tumour and is characterized by intersecting bundles of smooth muscles (Hashimoto and Quade 2003). The soft tissue mesenchymal tumours have been reported in many species of vertebrates including fish. Among fish, leiomyoma has been reported in
Comp Clin Pathol
gold fish, C. auratus (Schlumberger 1949; Ciltas and Hisar 2005; Oryan et al. 2015). Leiomyomas are most frequently located in the vena cava, saphenous vein, femoral vein, pulmonary artery and femoral artery but have also been reported in retroperitonium, superficial or deep soft tissues, rarely in the joints, bones, breast, colon and genital organs (Hashimoto and Quade 2003). They are classified histologically as leiomyoma, leiomyoblastoma, leiomyomatosis and leiomyosarcoma (Hashimoto and Quade 2003). Besides, other related neoplasms also have been reported in M. cephalus such as multiple cutaneous fibromas (Lopez and Raibaut 1981), hypodermal lipoma (Easa et al. 1989) tumour-like growths in the olfactory organ (Byankin 2001) and squamous cell carcinoma (Jithendran et al. 2011). To our knowledge, this is the first report of myxoinflammatory fibroblastic sarcoma and cutaneous leiomyoma in feral flat head grey mullet (M. cephalus).
Materials and methods In February and March 2014, a 1020-g weight, 43.5-cm long (case 1) and 1076.5-g weight, 45.7-cm long (case 2), wild adult female flat head grey mullet (M. cephalus) were collected from Pazhayar and Parangipettai landing centre, southeast Fig. 1 Macroscopic view of the tumour lesions located on the right side of fish attached to the behind of the anal fin, case 1 (a). Neoplasm located on the left side of the fish arose deep soft tissues of the flank, case 2 (b). Ulcerated, hyperemic and hyperchromatic overlying epidermis, case 1 closeup view (c). Reddish fleshy lesion covered with whitish-grey thin epidermal layer, case 2 close-up view (d). Rulers show centimetre
coast of India. The fish was brought to the laboratory for further investigation; the fish was identified based on the morphological character by De Bruin et al. (1995). The size of the tumours was measured by Vernier caliper, and their nature was observed. Ecto- and endo-parasites were examined. Blood samples and other internal organs were collected for fungal and bacteriological examination. The tumour biopsies were fixed in 10 % neutral phosphate-buffered formalin for 24 h. Then, biopsies were processed and embedded into a paraffin wax. The thin section of 4 μm was incised with rotary microtome (Yorco YSI-115) and stained with Harris haematoxylin and counter stained with eosin. The lesions were observed under a phase contrast microscope (Nikon Eclipse TS 100).
Results The well-circumscribed, pedunculated, reddish-white, solitary and fleshy tumour growth on the right side of the fish (case 1) was attached to the behind of the anal fin, which measured 24 × 30 × 28 mm (Fig. 1a). The overlying epidermis was ulcerated, hyperemic and hyperchromatic (Fig. 1c). The tumour had a gelatinous consistency and released jelly-like matters. Case 2: deeply circumscribed, solitary and fleshy tumour
Comp Clin Pathol
Fig. 2 Mugil cephalus, case 1. The lesion shows prominent myxoid and hyalinized matrix, as well as fibrosis and numerous inflammatory cells (a). The lesion infiltrating with hetetrogeneous bizarre tumour cells with eccentric, pleomorphic and hperchromatic nuclei, and pleomorphic multinucleated giant cells with vesicular neuclei, inclusion-like nucleoli and intracytoplasmic eosinophilic inclusion bodies (b) (H&E)
growth on the left-side of the deep soft tissue of the flank, which measured 32 × 44 × 26 mm (Fig. 1b). The reddish fleshy tumour was present within the musculature and covered
Fig. 3 Mugil cephalus, case 2. The tumour mass was covered with a thin attenuated layer of epidermis (a). The lesion shows the bundles of respectable straplike smooth muscle fibres, being composed of intersecting fascicles of spindle cells with intracytoplasmic eosinophilic inclusion bodies (b). The spindloid cells had pleomorphic (bland and elongated) and hyperchromatic nuclei with blunt ends (box-car or cigar-shaped appearance) (c) (H&E)
with a thin layer of epidermis (Fig. 1d). Surgically excised lesions revealed that both tumours were attached to the musculature. The excised lesions were vascularized, and no lesions were visible in other visceral organs, as necropsy examination exhibited no gross evident of invasion and metastasis. The detailed investigations of parasitological and microbiological clinical findings were not given significant results. Histopathologically, the case-1 tumour lesion was well circumscribed and multi-nodular; the nodules had prominent myxoid and hyalinized matrix, as well as fibrosis. The lesions had numerous inflammatory cells, including polymorphonuclear leukocytes, eosinophil, lymphocytes and plasma cells. The epidermal cells were loosely packed and disorganized, and basal layer was usually normal to thickened (Fig. 2b). The lesion infiltrated with heterogeneous bizarre tumour cells with eccentric, pleomorphic and hyperchromatic nuclei and clear cytoplasm, and pleomorphic multinucleated giant cells with vesicular nuclei, inclusion-like nucleoli and abundant eosinophilic cytoplasm, which had homogeneous to vacuolated and often contained intracytoplasmic eosinophilic inclusion bodies. The mitotic figures were less evident, mitotic index averaged 1.4 per 10 HPF. The lesions are hypercellularity with lesser collagen fibres, while some were vascularized (Fig. 2b). The case 2 tumour mass was present within the deep soft tissue musculature and covered with a thin attenuated layer of epidermis (Fig. 3a). The lesion contains interlacing bundles of respectable strap-like smooth muscle fibres, being composed of intersecting fascicles of spindle cells with intracytoplasmic eosinophilic inclusion bodies (Fig. 3b). The spindloid cells had pleomorphic (bland and elongated) and hyperchromatic nuclei with blunt ends (boxcar or cigar-shaped appearance). The smooth muscle fibres
Comp Clin Pathol
tend to intersect at right angles rather than blend in curving bundles. Stomas are minimal, and degenerative changes are infrequent. The mitotic figures were less evident, mitotic index averaged 2.0 per 10 HPF (Fig. 3c).
Discussion MIFS is a rare tumour in vertebrates and has not been reported earlier in fish. However, the MIFS has been described in humans (Kindblom and Meis-Kindblom 2002; Raghavan et al. 2012). The clinical observations revealed the single, bilobed or multiple external lesions (Kindblom and MeisKindblom 2002; Raghavan et al. 2012). In the present study, neoplasm was located on the behind of the anal fin, and the neoplasm was reddish white, because most of the prominent gross lesions are skin tumours and obvious cutaneous and subcutaneous edema and erythema. In a previous study, nodules measured 6 × 3.5 × 2 cm (Raghavan et al. 2012). In the present study, the neoplasm was measured 24 × 30 × 28 mm. The lesions observed in this study have similarities with those described by Raghavan et al. (2012), which demonstrated that the predominance of inflammatory, myxoid and bizarre cell components is between non-tumoral lesions and tumoral lesions such as giant cell tumour, inflammatory fibrosarcoma, inflammatory myofibroblastic tumour or myxofibrosarcoma. However, inflammatory myofibroblastic tumour and inflammatory fibrosarcoma are most frequent (Chahdi et al. 2010). In the present study, tumour was categorized as malignant based on cellular atypia and angiogenesis. However, local invasion and metastases were not detected in spite of a complete post-mortem examination. In earlier, cutaneous leiomyoma has been described only in gold fish, C. auratus (Schlumberger 1949; Ciltas and Hisar 2005; Oryan et al. 2015). The clinical observations revealed single or multiple external lesions of cutaneous leiomyoma in a gold fish but mostly located on the trunk, head and fins of the fish (Schlumberger 1949). In the present study, neoplasm was located on the deep soft tissue of the trunk. Golden orange and orange yellow tumours were observed in gold fish (Schlumberger 1949; Oryan et al. 2015). In contrast, in the present study, the neoplasm was reddish fleshy tumour covered with whitish-grey thin layer of epidermis. In a previous study, nodules measured 3.5 × 2 × 1 and 2 × 2.5 × 0.7 cm in the gold fish (Ciltas and Hisar 2005; Oryan et al. 2015). In the present study, the neoplasm was measured 32 × 44 × 26 mm. The cutaneous leiomyoma lesion results are similar to the gold fish, C. auratus, report by Oryan et al. (2015), which demonstrated the interlacing bundles of spindled to elongated tumour cells with cigar-shaped nuclei with no malignancy observed (Schlumberger 1949; Ciltas and Hisar 2005; Oryan et al. 2015). In the present study, tumour was categorized as benign based on cellular atypia and mitotic rate. The local invasion
and metastases were not detected in spite of a complete postmortem examination. On the basis of clinical and histopathological findings, the tumours are diagnosed as myxoinflammatory fibroblastic sarcoma and leiomyoma. Acknowledgments The authors acknowledge the Ministry of Environment Forest and Climate Change (MoEF&CC), Government of India, New Delhi, for the financial support for the project entitled BPrevalence of tumours in food fishes of Tamil Nadu coast^ (D.O. No.22-31/2010-CS-I). We also acknowledge the fishing communities at sampling localities for their help during the fish collection and the supply of fish samples. Compliance with ethical standard Ethical approval This article does not contain any experimental studies with human participants or animals performed by any of the authors. Tumour-infected fish samples are directly collected from the fisherman at landing centre. Conflict of interest The corresponding author (Dr. A. Gopalakrishnan) has received research grant from Ministry of Environment Forest and Climate Change (MoEF&CC), Government of India. The first author (Mr. V. Singaravel) and third author (Dr. K. Raja) has received fellowship from the mentioned project. The forth and last author (Dr. R. Vijayakumar and Dr. Syed Asrafuzzaman) declares that he has no conflict of interest. Informed consent This article does not contain any studies with human participants. Funding This study was funded by Ministry of Environment Forest and Climate Change (MoEF&CC), Government of India (Grant No. D.O. No.22-31/2010-CS-I).
References Ahmed ATA, Egusa S (1980) Dermal fibrosarcoma in goldfish Carassius auratus (L.). J Fish Dis 3:249–254 Bowser PR, Abou-Madi N, Garner MM, Bartlett SL, Grimmett SG, Paul TA, Casey RN, Casey JW (2005) Fibrosarcoma in yellow perch, Perca flavescens (Mitchill). J Fish Dis 28:301–305 Byankin AG (2001) Tumour like formations in the olfactory organ of the striped mullet, Mugil cephalus from Sovetskaya Gavan bay Sea of Japan. Russ J Mar Biol 27:333–335 Chahdi H, Damiri A, Oukabli M, Albouzidi A, Bouabid S, Lazrek K (2010) Acral myxoinflammatory fibroblastic sarcoma. Orthop Traumatol Surg Res 96:597–599 Ciltas A, Hisar O (2005) Leiomyoma localized on the head of a goldfish (Carassius auratus). Turk J Vet Anim Sci 29:1077–1079 De Bruin GHP, Russell BC, Bogusch A (1995) The marine fishery resources of Sri Lanka: FAO species identification field guide for fishery purposes. FAO, Rome Dennis MM, Diggles BK (2015) Multicentric orocutaneous fibrosarcoma in a fork-tailed catfish (Hemiarius dioctes). J Fish Dis 38: 1077–1081 Easa ME, Harshbarger JC, Hetrick FM (1989) Hypodermal lipoma in a striped (grey) mullet Mugil cephalus. Dis Aquat Organ 6:157–160 Fletcher CDM, Unni KK, Mertens F (2002) Pathology and genetics of tumours of soft tissue and bone, WHO classification of tumours. IARC, Lyon, pp 47–107
Comp Clin Pathol Hashimoto H, Quade B (2003) Leiomyoma of deep soft tissue. In: Fletcher CDM, Krishnan Unni K, Mertens F (eds) Pathology and genetics of tumours of soft tissue and bone. IARC Press, Lyon Jithendran KP, Natarajan M, Pramoda KS, Thiagarajan G (2011) Squamous cell carcinoma in grey mullet, Mugil cephalus L. (Perciformes: Mugilidae). Compa Clini Pathol 20:673–675 Keller M, Han S, Snekvik K (2011) Severe anisakiasis and cutaneous myxoma in a California yellowtail, Seriola lalandi Valenciennes. J Fish Dis 34:635–639 Kindblom LG, Meis-Kindblom JM (2002) Myxoinflammatory fibroblastic sarcoma. In: Fletcher CDM, Unni KK, Mertens F (eds) Pathology and genetics of tumours of soft tissue and bone. IARC press, Lyon, pp 96–97 Lopez A, Raibaut A (1981) Multiple cutaneous fibromas in a mullet, Mugil cephalus L. J Fish Dis 4:169–174 Meyers TR, Hendricks JD (1983) Histopathology of four spontaneous neoplasms in three species of salmonid fishes. J Fish Dis 6:481–499 Oryan A, Alidadi S, Shayegh H, Geramizadeh B (2015) Cutaneous leiomyoma in a goldfish Carassius auratus. Fish Dis Res 50:112–114
Raghavan VH, Satish S, Ravishankar S, Manjunath GV (2012) Myxoinflammatory fibroblastic sarcoma of the thigh: a morphologic diversity. Avicenna J Med 2:74–76 Schamberg JF, Lucke B (1922) Fibrosarcoma of the skin in a gold fish (Carassus auratus). Cancer Res 7:151–161 Schlumberger HG (1949) Cutaneous leiomyoma of goldfish: I. Morphology and growth in tissure culture. The Am J Pathol 25:287 Schlumberger HG, Lucke B (1948) Tumors in fishes, amphibians, and reptiles. Can Res 8:657–754 Singaravel V, Gopalakrishnan A, Vijayakumar R, Raja K (2016) The case report on cutaneous myxoma or invasive myxomatosis in blackfin sea catfish (Arius jella Day, 1877). Comp Clini Pathol 25:491–495 Whitfield AK, Panfili J, Durand JD (2012) A global review of the cosmopolitan flathead mullet Mugil cephalus Linnaeus 1758 (Teleostei: Mugilidae), with emphasis on the biology, genetics, ecology and fisheries aspects of this apparent species complex. Rev Fish Biol Fish 22:641–681
