Journal of Fish Diseases 2015, 38, 833–838
doi:10.1111/jfd.12292
Short Communication Cystic lesions in the kidney of flower horn fish, hybrid cichlid H Rahmati-holasoo1, M Masoudifard2, H Ebrahimzadeh Mousavi1, S Shokrpoor3, A Tavakkoli2 and M S Farazandemehr1 1 Department of Aquatic Animal Health, Faculty of Veterinary Medicine, University of Tehran, Tehran, Iran 2 Department of Surgery and Radiology, Faculty of Veterinary Medicine, University of Tehran, Tehran, Iran 3 Department of Pathology, Faculty of Veterinary Medicine, University of Tehran, Tehran, Iran
Keywords: cystic lesions, flower horn fish, kidney. The flower horn fish belongs to the Cichlid family and has emerged through selective cross-breeding of three spot cichlid, Cichlasoma trimaculatum (G€ unther), guayas cichlid Cichlasoma festae (Boulenger) and Jingang Blood Parrot, hybrid cichlid, in 1996 (Lin et al. 2008; Rahmati-holasoo et al. 2010, 2014). In fish, cystic lesions were reported in ovary of Atlantic Cod, Gadus morhua L. (Wiles 1969), spleen of wild brown trout, Salmo trutta L. (Roberts & MacRitchie 1971), and the liver of Pacific electric ray, Torpedo californica Ayres (Smith & Little 1969), Atlantic salmon, Salmo salar L. (Bruno & Ellis 1986), medaka, Oryzias latipes (Temminck & Schlegel) (Boorman et al. 1997), rainbow trout, Oncorhynchus mykiss (Walbaum) (Evensen 2006), white sturgeon, Acipenser transmontanus Richardson (Taylor, Smith & Blair 2009), farmed turbot, Scopthalmus maximus (L.) (Jeronimo, Cruz & Saraiva 2011), goldfish, Carassius auratus (L.) (Rezaie et al. 2012), zebrafish, Danio rerio (Hamilton) (Tietz Bogert et al. 2013) and flower horn fish, hybrid cichlid (Rahmati-holasoo et al. 2014). The first polycystic lesions in the kidney of common carp, Cyprinus carpio L., were reported by Plehn (Plehn 1924). Since then, polycystic kidneys have been described in diamond Correspondence H Rahmati-holasoo, Department of Aquatic Animal Health, Faculty of Veterinary Medicine, University of Tehran, PO Box: 14155-6453, Tehran, Iran (e-mail: [email protected]) Ó 2014 John Wiley & Sons Ltd
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tetra, Moenkhausia pittieri Eigenmann (Stolk 1956a,b) and goldfish, Carassius auratus (L.) (Stolk 1956a,b; Munkittrick, Moccia & Leatherland 1985; Gill 1994; Wildgoose 2007). This is the first report of cystic lesions in kidney of flower horn fish. In January and February 2014, 2 flower horn fish, hybrid cichlid, (Case 1: a long bodied and Case 2: a short bodied flower horn fish) were referred to the Faculty of Veterinary Medicine, University of Tehran. Case 1 was referred with progressive anorexia and positive buoyancy. Case 2 was referred with progressive anorexia, abdominal distention, protruding scales (Fig. 2a) and increased respiratory rate. No parasite or ova was observed in wet smears of skin, gills and faeces of both fish. The cases were anaesthetized in 100 mg L 1 tricaine methane sulphonate (MS-222, Finquelâ; Argent Chemical Laboratories) buffered with 200 mg L 1 sodium bicarbonate. Standard digital radiographs were taken in right lateral and dorsoventral (DV) projections. Right lateral radiographs showed a soft tissue density superimposed on posterior part of swim bladder in both cases (Figs 1a & 2b). DV radiographs showed abdominal distention with protruding scales in Case 2 (Fig. 2c), and no significant change was observed in Case 1 (Fig 1b). Ultrasonography was performed from the left side of both fish. Ultrasonography of visceral organs showed a fluid-filled urinary bladder and hypo to anechoic cysts in the kidney (Fig. 1c) of Case 1 and free fluid in abdominal cavity and
Journal of Fish Diseases 2015, 38, 833–838
around the heart (Fig. 2d) and hypo to anechoic cysts in the kidney of Case 2 (Fig. 2e). Both fish died after 2 h, and necropsy was performed under sterile conditions. Aerobic and anaerobic bacterial cultures from multiple internal organs incubated at 25 °C resulted in no growth. At necropsy, several cysts (Fig. 1d) in posterior kidney of Case 1 and pale liver, free fluid in the abdominal cavity and around the heart (Fig. 2f) and several cysts (Fig. 3a) in the posterior kidney of Case 2 were observed. Cysts of Case 1 were filled with yellowish fluid, and cysts of Case 2 filled with clear fluid. Other organs exhibited normal appearance. No parasites were observed in both fish. For histological assessments, samples of heart, liver, kidney, urinary bladder, spleen, gills and gastrointestinal tract of both fish were dissected and preserved in 10% buffered formalin, dehydrated and embedded in paraffin, sectioned at 5 lm and stained with haematoxylin-eosin (H&E). Histologically, kidney had large and multiple cysts causing displacement of the normal kidney architecture in Case 1. The cysts walls were composed of a translucent proteinous membrane, and
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most cysts were empty (Fig. 1e). There was also no significant inflammatory response in kidney, and most of tubules were normal. In Case 2, histological lesions in the kidney were different. The renal tubules were mostly dilated; however, their epithelial components were normal (Fig. 3b,c), and subcapsular oedema in kidney was seen (Fig. 3c). There were some large cysts that their walls were composed of flat squamous epithelium (Fig. 3b). Occasionally, dilation of Bowman’s spaces (Fig. 3b,c) was observed. Hyperaemia and severe oedema in urinary bladder (Figs 1f & 3d) of both of fish, hydropericardium (Fig 3e) and severe fatty changes in liver (Fig. 3f) of Case 2 were observed. In the kidney of both cases, no calcium crystals were detected within the tubules. Histologically, gastrointestinal tract, spleen and gills were normal. Polycystic kidney disease is a common hereditary disease in human being (Hostetter, SullivanBrown & Burdine 2003; Hashimoto et al. 2009) and is one of the leading causes of end-stage renal disease (Sun et al. 2004) that is characterized by progressive formation of multiple liquid-filled cysts in kidney (Hostetter et al. 2003; Bouvrette
Figure 1 Flower horn fish, Case 1. (a) Right lateral digital radiograph showing a soft tissue density (arrowheads) superimposed on posterior part of swim bladder (SB). (b) No significant change is detectable in DV view. (c) Transverse ultrasonographic scan of left abdomen reveals two hypoechoic cyst-like echogenicity (arrows) within the kidney dorsal to the urinary bladder (UB). (d) Gross necropsy images showing three macroscopic cysts (Cs) in the kidney. The cyst fluid (CF) is yellowish, while urine (Ur) is clear. Urinary bladder (UB) and gonad (G). (e) Multiple cysts (C) and tubules (arrows) are seen (H&E). (f) Severe edema (E) in submocsa of urinary bladder (H&E).
H Rahmati-holasoo et al. Cystic lesions in kidney
Journal of Fish Diseases 2015, 38, 833–838
Figure 2 The flower horn fish, Case 2. (a) Right and left lateral view of abdominal distention (arrows) and protruding scales (arrowheads). (b) Right lateral digital radiograph showing a soft tissue density (arrowheads) overlying the most posterior part of the swim bladder (SB). Arrows show vertebral column deformities. (c) DV digital radiograph showing abdominal distention, protruding scales (arrowheads) and concave edge of swim bladder (arrows). (d) Frontal ultrasonographic scan showing free fluid (FF) in the abdominal cavity and around the heart. Fat (F), gallbladder (GB), H (heart) and Liver (L). (e) Transverse ultrasonographic scans showing two hypoechoic cyst-like echogenicity within the kidney (arrowheads). (f) Gross necropsy image showing pale liver (L), fat (F) in the abdominal cavity and free fluid (FF) around the heart (H). Gonad (G), spleen (Sp) and urinary bladder (UB).
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et al. 2010), renal enlargement and abnormal tubular development (Sun et al. 2004). Chemical compounds are known to induce renal cysts in laboratory animals (Safouch, Crocker & Vernier 1970; Dobyan et al. 1981). Polycystic kidneys in fish can occur as a developmental anomaly or as a result of pollutants and obstruction of urine flow (Reimschuessel & Ferguson 2006). Nephrocalcinosis caused swollen appearance of the kidneys and presence of cysts in Myxus capensis (Valenciennes) and Mugil cephalus L. (McHugh et al. 2013). Dilation of renal tubules may be due to obstruction, and nephrocalcinosis is a possible cause of renal tubules obstruction in fish (Harrison & Richards 1979; Smart et al. 1979). Similar to observations made on nephrocalcinosis in affected salmonids (Harrison & Richards 1979), McHugh et al. (2013) mentioned that dilation of renal tubules in M. capensis and M. cephalus may have been a result of obstruction due to the presence of the calcium deposits or as a result of inflammation. There are several reports of cystic enlargement of the kidneys of cyprinids, and aetiology is either unknown in the goldfish, C. auratus (Schlumberger 1950; Stolk 1956a,b; Besse Ó 2014 John Wiley & Sons Ltd
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et al. 1959), or diamond tetra, Moenkhausia pittieri (Stolk 1956a,b). The presence of a sporozoan parasite, Mitraspora cyprini (Wakabayashi et al. 1969; Ahmed 1973, 1974; Hoffman 1981) and Hoferellus carassii (Molnar et al. 1989) are mentioned as reasons of cyst formation in goldfish. Environmental pollution (Munkittrick et al. 1985) and inheritance (Gill 1994) have been suggested as other causes of polycystic kidneys in goldfish, C. auratus. Knockdown of bicaudal C gene (Bicc1) expression causes cystic kidneys in zebrafish, Danio rerio (Bouvrette et al. 2010), and also, injection of zebrafish embryos with a morpholino antisense oligonucleotide caused formation of pronephric cysts (Liu et al. 2002). In addition, a mutation in the pc/glis3 gene causes polycystic kidneys in medaka, Oryzias latipes, because pc/ glis3 is involved in the renal ciliary function that is required for the production of urine flow (Mochizuki et al. 2005; Hashimoto et al. 2009). Munkittrick et al. (1985) reported a normal appearance in the tubular component of the kidney, except in fish with large cysts that tubules were dilated and their epithelial components were squamous. Mochizuki et al. (2005) reported that
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the cysts were lined by highly flat squamous epithelial cells, and histologic changes were not observed in the liver and heart. In the present report, large cysts in Case 2 were surrounded by flat squamous epithelium that was similar to cysts in the kidney of medaka, Oryzias latipes (Mochizuki et al. 2005); however, histological changes in liver and heart were observed. Munkittrick et al. (1985) reported that large cysts were filled with amorphous material along with a few red blood cells, phagocytic cells and/or pigmented macrophages, in six goldfish collected from a heavily polluted industrial basin, whereas most of cysts in present study were empty. Hoferellus carassii was seen in cylindrical epithelium that was lining renal cysts and in metaplastic epithelium of infected tubules of goldfish, C. auratus and gibel carp, Carassius auratus gibelio (Molnar et al. 1989). Unlike the present study, H. carassiirelated cyst walls were composed of a proliferating, cylindrical epithelium and a basement membrane, and in some parts, cysts were also bordered by several layers of connective tissue (Molnar et al. 1989), and cysts in copper-exposed mussels were composed of two cell layers that Ó 2014 John Wiley & Sons Ltd
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Figure 3 The flower horn fish, Case 2. (a) Gross necropsy image showing macroscopic cysts in the kidney. Urinary bladder (UB). (b) A large cyst (C), dilated tubules (arrowheads) and dilation of Bowman’s spaces (arrows) (H&E). (c) Dilated tubules (arrows), dilation of Bowman’s spaces (arrowheads) and subcapsular edema (black line) in kidney (H&E). (d) Hyperemia (arrow) and severe edema (E) in submucosa of urinary bladder (H&E). (e) Hydropericardium (HP) (H&E). Ventricle (V) and Bulbus arteriosus (BA). (f) Severe fatty change in the hepatocytes. Central vein (CV) (H&E).
were proliferative (Sunila 1989). Radiogeraphs showed displacement of the posterior chamber of the swim bladder due to a polycystic kidney disease in goldfish, C. auratus (Wildgoose 2007). Radiology and ultrasonography were helpful in diagnosis of polycystic liver in flower horn fish (Rahmati-holasoo et al. 2014). Our radiological and ultrasonographical findings support that radiology and ultrasonography can be suggested as non-invasive methods for diagnosis of cystic lesions in internal organs of fish (Rahmati-holasoo et al. 2014) and identifying polycystic kidneys (Wildgoose 2007). In this study, the relationship between polycystic lesions in kidney and oedema in urinary bladder was unclear. We were unable to identify an obvious aetiologic agent, and cause of these cystic conditions remained unknown. However, genetic predisposition appears to be the best explanation for these lesions. Acknowledgements The authors would like to thank Dr. Mohammad Molazem for his assistance in comments on radiographs.
Journal of Fish Diseases 2015, 38, 833–838
Conflict of interest
No conflict of interest declared. Publication History
Hoffman G.L. (1981) Two fish pathogens, Parvicapsula sp. and Mitraspora cyprini (Myxosporea), new to North America. In: Fish Pathogens and Environment in European Polyculture (ed. by J. Olah, K. Molnar & Z. Jeney), pp. 184–197. Proceedings of International Seminar, Fisheries Research Institute, Szarvas, Hungary.
Received: 13 April 2014 Revision received: 21 June 2014 Accepted: 22 June 2014
Hostetter C.L., Sullivan-Brown J.L. & Burdine R.D. (2003) Zebrafish pronephros: a model for understanding cystic kidney disease. Developmental Dynamics 228, 514–522.
This paper was edited and accepted under the Editorship of Professor Ron Roberts.
Jeronimo D., Cruz C. & Saraiva A. (2011) Polycystic liver in farmed turbot, Scopthalmus maximus (L.). Journal of Fish Diseases 34, 937–938.
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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 the European Association of Fish Pathologists 28, 115–120. Liu S., Lu W., Obara T., Kuida S., Lehoczky J., Dewar K., Drummond I.A. & Beier D.R. (2002) A defect in a novel Nek-family kinase causes cystic kidney disease in the mouse and in zebrafish. Development 129, 5839–5846. McHugh K.J., Van Dyk J.C., Weyl O.L.F. & Smit N.J. (2013) First report of nephrocalcinosis in a wild population of Mugil cephalus L. and Myxus capensis (Valenciennes). Journal of Fish Diseases 36, 887–889. Mochizuki E., Fukuta K., Tada T., Harada T., Watanabe N., Matsuo S., Hashimoto H., Ozato K. & Wakamatsu Y. (2005) Fish mesonephric model of polycystic kidney disease in medaka, (Oryzias latipes) pc mutant. Kidney International 68, 23–34. Molnar K., Fischer-Scherl T., Baska F. & Hoffmann R.W. (1989) Hoferellosis in goldfish Carassius auratus and gibel carp Carassius auratus gibelio. Diseases of Aquatic Organisms 7, 89–95. Munkittrick K.R., Moccia R.D. & Leatherland J.F. (1985) Polycystic kidney disease in goldfish (Carassius auratus) from Hamilton Harbour, Lake Ontario, Canada. Veterinary Pathology 22, 232–237. Plehn M. (1924) Praktikum der Fischkrankheiten. [Handbook of Fish Diseases.], pp. 89–91. Schweizbart, Stuttgart, Germany. Rahmati-holasoo H., Hobbenaghi R., Tukmechi A., Seyrafi R., Homayounimehr A. & Ghavami R. (2010) Lymphocystis in a flower horn fish. Comparative Clinical Pathology 19, 433– 435. Rahmati-holasoo H., Ebrahimzadeh Mousavi H., Vajhi A., Shokrpoor S., Tavakkoli A., Mirdamadi M.A. & Fayyaz S. (2014) Polycystic liver in flower horn fish, hybrid cichlid. Journal of Fish Diseases. (In Press) Doi:10.1111/jfd.12245. Reimschuessel R. & Ferguson H.W. (2006) Kidney. In: Systemic Pathology of Fish: A text and Atlas of Normal Tissues in Teleosts and Their Responses in Diseases, 2nd edn (ed. by H.W. Ferguson), pp. 100. Scotian Press, Edinburgh. Rezaie A., Mousavi S.M., Ahmadmoradi E. & Mohammadi F. (2012) Polycystic liver in a goldfish, Carassius auratus (L.). Journal of Fish Diseases 35, 785–787. Roberts R.J. & MacRitchie G. (1971) Multiple congenital splenic cysts in wild trout. Journal of Wildlife Diseases 7, 155–156.
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Safouch M., Crocker J.F.S. & Vernier R.L. (1970) Experimental cystic disease of the kidney: sequential, functional and morphological studies. Laboratory Investigation 23, 392–400.
Sun Z., Amsterdam A., Pazour G.J., Cole D.G., Miller M.S. & Hopkins N. (2004) A genetic screen in zebrafish identifies cilia genes as a principal cause of cystic kidney. Development 131, 4085–4093.
Schlumberger H.G. (1950) Polycystic kidney (mesonephros) in the goldfish. AMA Archives of Pathology 50, 400–410.
Sunila I. (1989) Cystic kidneys in copper exposed mussels. Disease of Aquatic Organisms 6, 63–66.
Smart G.R., Knox D., Harrison J.G., Ralph J.A., Richards R.H. & Cowey C.B. (1979) Nephrocalcinosis in rainbow trout Salmo gairdneri Richardson; the effect of exposure to elevated CO2 concentrations. Journal of Fish Diseases 2, 279–289.
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Smith A.C. & Little H.F. (1969) Liver lesions by hydatid-like cysts in the elasmobranch, the electric ray, Torpedo californica. National Cancer Institute Monograph 31, 251–254. Stolk A. (1956a) Polycystic kidneys in the characid Moenkhausia pittieri. Proceedings of Koninklijke Nederlandse Akademie van Wetenschappen (C) 59, 506–519. Stolk A. (1956b) Polycystic kidneys in the veiltail Carassius auratus var. Japonicus Bicaudatus, Zernecke. Proceedings of Koninklijke Nederlandse Akademie van Wetenschappen (C) 58, 70–73.
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Tietz Bogert P.S., Huang B.Q., Gradilone S.A., Masyuk T.V., Moulder G.L., Ekker S.C. & Larusso N.F. (2013) The zebrafish as a model to study polycystic liver disease. Zebrafish 10, 211–217. Wakabayashi H., Kaku M., Nakajima K. & Egusa S. (1969) Kidney enlargement of goldfish. Fish Pathology 4, 47–51. Wildgoose W.H. (2007) Buoyancy disorders of ornamental fish: a review of cases seen in veterinary practice. Fish Veterinary Journal 9, 22–37. Wiles M. (1969) Fibrous and cystic lesions in the ovaries of aged Atlantic Cod, Gadus morhua: a preliminary report. Journal of the Fisheries Research Board of Canada 26, 3242–3246.
doi:10.1111/jfd.12292
Short Communication Cystic lesions in the kidney of flower horn fish, hybrid cichlid H Rahmati-holasoo1, M Masoudifard2, H Ebrahimzadeh Mousavi1, S Shokrpoor3, A Tavakkoli2 and M S Farazandemehr1 1 Department of Aquatic Animal Health, Faculty of Veterinary Medicine, University of Tehran, Tehran, Iran 2 Department of Surgery and Radiology, Faculty of Veterinary Medicine, University of Tehran, Tehran, Iran 3 Department of Pathology, Faculty of Veterinary Medicine, University of Tehran, Tehran, Iran
Keywords: cystic lesions, flower horn fish, kidney. The flower horn fish belongs to the Cichlid family and has emerged through selective cross-breeding of three spot cichlid, Cichlasoma trimaculatum (G€ unther), guayas cichlid Cichlasoma festae (Boulenger) and Jingang Blood Parrot, hybrid cichlid, in 1996 (Lin et al. 2008; Rahmati-holasoo et al. 2010, 2014). In fish, cystic lesions were reported in ovary of Atlantic Cod, Gadus morhua L. (Wiles 1969), spleen of wild brown trout, Salmo trutta L. (Roberts & MacRitchie 1971), and the liver of Pacific electric ray, Torpedo californica Ayres (Smith & Little 1969), Atlantic salmon, Salmo salar L. (Bruno & Ellis 1986), medaka, Oryzias latipes (Temminck & Schlegel) (Boorman et al. 1997), rainbow trout, Oncorhynchus mykiss (Walbaum) (Evensen 2006), white sturgeon, Acipenser transmontanus Richardson (Taylor, Smith & Blair 2009), farmed turbot, Scopthalmus maximus (L.) (Jeronimo, Cruz & Saraiva 2011), goldfish, Carassius auratus (L.) (Rezaie et al. 2012), zebrafish, Danio rerio (Hamilton) (Tietz Bogert et al. 2013) and flower horn fish, hybrid cichlid (Rahmati-holasoo et al. 2014). The first polycystic lesions in the kidney of common carp, Cyprinus carpio L., were reported by Plehn (Plehn 1924). Since then, polycystic kidneys have been described in diamond Correspondence H Rahmati-holasoo, Department of Aquatic Animal Health, Faculty of Veterinary Medicine, University of Tehran, PO Box: 14155-6453, Tehran, Iran (e-mail: [email protected]) Ó 2014 John Wiley & Sons Ltd
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tetra, Moenkhausia pittieri Eigenmann (Stolk 1956a,b) and goldfish, Carassius auratus (L.) (Stolk 1956a,b; Munkittrick, Moccia & Leatherland 1985; Gill 1994; Wildgoose 2007). This is the first report of cystic lesions in kidney of flower horn fish. In January and February 2014, 2 flower horn fish, hybrid cichlid, (Case 1: a long bodied and Case 2: a short bodied flower horn fish) were referred to the Faculty of Veterinary Medicine, University of Tehran. Case 1 was referred with progressive anorexia and positive buoyancy. Case 2 was referred with progressive anorexia, abdominal distention, protruding scales (Fig. 2a) and increased respiratory rate. No parasite or ova was observed in wet smears of skin, gills and faeces of both fish. The cases were anaesthetized in 100 mg L 1 tricaine methane sulphonate (MS-222, Finquelâ; Argent Chemical Laboratories) buffered with 200 mg L 1 sodium bicarbonate. Standard digital radiographs were taken in right lateral and dorsoventral (DV) projections. Right lateral radiographs showed a soft tissue density superimposed on posterior part of swim bladder in both cases (Figs 1a & 2b). DV radiographs showed abdominal distention with protruding scales in Case 2 (Fig. 2c), and no significant change was observed in Case 1 (Fig 1b). Ultrasonography was performed from the left side of both fish. Ultrasonography of visceral organs showed a fluid-filled urinary bladder and hypo to anechoic cysts in the kidney (Fig. 1c) of Case 1 and free fluid in abdominal cavity and
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around the heart (Fig. 2d) and hypo to anechoic cysts in the kidney of Case 2 (Fig. 2e). Both fish died after 2 h, and necropsy was performed under sterile conditions. Aerobic and anaerobic bacterial cultures from multiple internal organs incubated at 25 °C resulted in no growth. At necropsy, several cysts (Fig. 1d) in posterior kidney of Case 1 and pale liver, free fluid in the abdominal cavity and around the heart (Fig. 2f) and several cysts (Fig. 3a) in the posterior kidney of Case 2 were observed. Cysts of Case 1 were filled with yellowish fluid, and cysts of Case 2 filled with clear fluid. Other organs exhibited normal appearance. No parasites were observed in both fish. For histological assessments, samples of heart, liver, kidney, urinary bladder, spleen, gills and gastrointestinal tract of both fish were dissected and preserved in 10% buffered formalin, dehydrated and embedded in paraffin, sectioned at 5 lm and stained with haematoxylin-eosin (H&E). Histologically, kidney had large and multiple cysts causing displacement of the normal kidney architecture in Case 1. The cysts walls were composed of a translucent proteinous membrane, and
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most cysts were empty (Fig. 1e). There was also no significant inflammatory response in kidney, and most of tubules were normal. In Case 2, histological lesions in the kidney were different. The renal tubules were mostly dilated; however, their epithelial components were normal (Fig. 3b,c), and subcapsular oedema in kidney was seen (Fig. 3c). There were some large cysts that their walls were composed of flat squamous epithelium (Fig. 3b). Occasionally, dilation of Bowman’s spaces (Fig. 3b,c) was observed. Hyperaemia and severe oedema in urinary bladder (Figs 1f & 3d) of both of fish, hydropericardium (Fig 3e) and severe fatty changes in liver (Fig. 3f) of Case 2 were observed. In the kidney of both cases, no calcium crystals were detected within the tubules. Histologically, gastrointestinal tract, spleen and gills were normal. Polycystic kidney disease is a common hereditary disease in human being (Hostetter, SullivanBrown & Burdine 2003; Hashimoto et al. 2009) and is one of the leading causes of end-stage renal disease (Sun et al. 2004) that is characterized by progressive formation of multiple liquid-filled cysts in kidney (Hostetter et al. 2003; Bouvrette
Figure 1 Flower horn fish, Case 1. (a) Right lateral digital radiograph showing a soft tissue density (arrowheads) superimposed on posterior part of swim bladder (SB). (b) No significant change is detectable in DV view. (c) Transverse ultrasonographic scan of left abdomen reveals two hypoechoic cyst-like echogenicity (arrows) within the kidney dorsal to the urinary bladder (UB). (d) Gross necropsy images showing three macroscopic cysts (Cs) in the kidney. The cyst fluid (CF) is yellowish, while urine (Ur) is clear. Urinary bladder (UB) and gonad (G). (e) Multiple cysts (C) and tubules (arrows) are seen (H&E). (f) Severe edema (E) in submocsa of urinary bladder (H&E).
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Figure 2 The flower horn fish, Case 2. (a) Right and left lateral view of abdominal distention (arrows) and protruding scales (arrowheads). (b) Right lateral digital radiograph showing a soft tissue density (arrowheads) overlying the most posterior part of the swim bladder (SB). Arrows show vertebral column deformities. (c) DV digital radiograph showing abdominal distention, protruding scales (arrowheads) and concave edge of swim bladder (arrows). (d) Frontal ultrasonographic scan showing free fluid (FF) in the abdominal cavity and around the heart. Fat (F), gallbladder (GB), H (heart) and Liver (L). (e) Transverse ultrasonographic scans showing two hypoechoic cyst-like echogenicity within the kidney (arrowheads). (f) Gross necropsy image showing pale liver (L), fat (F) in the abdominal cavity and free fluid (FF) around the heart (H). Gonad (G), spleen (Sp) and urinary bladder (UB).
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et al. 2010), renal enlargement and abnormal tubular development (Sun et al. 2004). Chemical compounds are known to induce renal cysts in laboratory animals (Safouch, Crocker & Vernier 1970; Dobyan et al. 1981). Polycystic kidneys in fish can occur as a developmental anomaly or as a result of pollutants and obstruction of urine flow (Reimschuessel & Ferguson 2006). Nephrocalcinosis caused swollen appearance of the kidneys and presence of cysts in Myxus capensis (Valenciennes) and Mugil cephalus L. (McHugh et al. 2013). Dilation of renal tubules may be due to obstruction, and nephrocalcinosis is a possible cause of renal tubules obstruction in fish (Harrison & Richards 1979; Smart et al. 1979). Similar to observations made on nephrocalcinosis in affected salmonids (Harrison & Richards 1979), McHugh et al. (2013) mentioned that dilation of renal tubules in M. capensis and M. cephalus may have been a result of obstruction due to the presence of the calcium deposits or as a result of inflammation. There are several reports of cystic enlargement of the kidneys of cyprinids, and aetiology is either unknown in the goldfish, C. auratus (Schlumberger 1950; Stolk 1956a,b; Besse Ó 2014 John Wiley & Sons Ltd
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et al. 1959), or diamond tetra, Moenkhausia pittieri (Stolk 1956a,b). The presence of a sporozoan parasite, Mitraspora cyprini (Wakabayashi et al. 1969; Ahmed 1973, 1974; Hoffman 1981) and Hoferellus carassii (Molnar et al. 1989) are mentioned as reasons of cyst formation in goldfish. Environmental pollution (Munkittrick et al. 1985) and inheritance (Gill 1994) have been suggested as other causes of polycystic kidneys in goldfish, C. auratus. Knockdown of bicaudal C gene (Bicc1) expression causes cystic kidneys in zebrafish, Danio rerio (Bouvrette et al. 2010), and also, injection of zebrafish embryos with a morpholino antisense oligonucleotide caused formation of pronephric cysts (Liu et al. 2002). In addition, a mutation in the pc/glis3 gene causes polycystic kidneys in medaka, Oryzias latipes, because pc/ glis3 is involved in the renal ciliary function that is required for the production of urine flow (Mochizuki et al. 2005; Hashimoto et al. 2009). Munkittrick et al. (1985) reported a normal appearance in the tubular component of the kidney, except in fish with large cysts that tubules were dilated and their epithelial components were squamous. Mochizuki et al. (2005) reported that
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(a)
(b)
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the cysts were lined by highly flat squamous epithelial cells, and histologic changes were not observed in the liver and heart. In the present report, large cysts in Case 2 were surrounded by flat squamous epithelium that was similar to cysts in the kidney of medaka, Oryzias latipes (Mochizuki et al. 2005); however, histological changes in liver and heart were observed. Munkittrick et al. (1985) reported that large cysts were filled with amorphous material along with a few red blood cells, phagocytic cells and/or pigmented macrophages, in six goldfish collected from a heavily polluted industrial basin, whereas most of cysts in present study were empty. Hoferellus carassii was seen in cylindrical epithelium that was lining renal cysts and in metaplastic epithelium of infected tubules of goldfish, C. auratus and gibel carp, Carassius auratus gibelio (Molnar et al. 1989). Unlike the present study, H. carassiirelated cyst walls were composed of a proliferating, cylindrical epithelium and a basement membrane, and in some parts, cysts were also bordered by several layers of connective tissue (Molnar et al. 1989), and cysts in copper-exposed mussels were composed of two cell layers that Ó 2014 John Wiley & Sons Ltd
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H Rahmati-holasoo et al. Cystic lesions in kidney
Figure 3 The flower horn fish, Case 2. (a) Gross necropsy image showing macroscopic cysts in the kidney. Urinary bladder (UB). (b) A large cyst (C), dilated tubules (arrowheads) and dilation of Bowman’s spaces (arrows) (H&E). (c) Dilated tubules (arrows), dilation of Bowman’s spaces (arrowheads) and subcapsular edema (black line) in kidney (H&E). (d) Hyperemia (arrow) and severe edema (E) in submucosa of urinary bladder (H&E). (e) Hydropericardium (HP) (H&E). Ventricle (V) and Bulbus arteriosus (BA). (f) Severe fatty change in the hepatocytes. Central vein (CV) (H&E).
were proliferative (Sunila 1989). Radiogeraphs showed displacement of the posterior chamber of the swim bladder due to a polycystic kidney disease in goldfish, C. auratus (Wildgoose 2007). Radiology and ultrasonography were helpful in diagnosis of polycystic liver in flower horn fish (Rahmati-holasoo et al. 2014). Our radiological and ultrasonographical findings support that radiology and ultrasonography can be suggested as non-invasive methods for diagnosis of cystic lesions in internal organs of fish (Rahmati-holasoo et al. 2014) and identifying polycystic kidneys (Wildgoose 2007). In this study, the relationship between polycystic lesions in kidney and oedema in urinary bladder was unclear. We were unable to identify an obvious aetiologic agent, and cause of these cystic conditions remained unknown. However, genetic predisposition appears to be the best explanation for these lesions. Acknowledgements The authors would like to thank Dr. Mohammad Molazem for his assistance in comments on radiographs.
Journal of Fish Diseases 2015, 38, 833–838
Conflict of interest
No conflict of interest declared. Publication History
Hoffman G.L. (1981) Two fish pathogens, Parvicapsula sp. and Mitraspora cyprini (Myxosporea), new to North America. In: Fish Pathogens and Environment in European Polyculture (ed. by J. Olah, K. Molnar & Z. Jeney), pp. 184–197. Proceedings of International Seminar, Fisheries Research Institute, Szarvas, Hungary.
Received: 13 April 2014 Revision received: 21 June 2014 Accepted: 22 June 2014
Hostetter C.L., Sullivan-Brown J.L. & Burdine R.D. (2003) Zebrafish pronephros: a model for understanding cystic kidney disease. Developmental Dynamics 228, 514–522.
This paper was edited and accepted under the Editorship of Professor Ron Roberts.
Jeronimo D., Cruz C. & Saraiva A. (2011) Polycystic liver in farmed turbot, Scopthalmus maximus (L.). Journal of Fish Diseases 34, 937–938.
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