doi:10.1111/j.1365-2761.2009.01031.x
Journal of Fish Diseases 2009, 32, 473–475
Short Communication Cardiac cholesterol granulomas in a piper gurnard, Trigla lyra (L.) G E Magi1, M Iannaccone2, C Gili2 and G Rossi1 1 Department of Veterinary Science, University of Camerino, Italy 2 Acquario di Genova, Ponte Spinola, Genova, Italy
Keywords: cholesterol, granuloma, gurnard, heart, histopathology, Trigla lyra. Cholesterol granulomas are well-recognized, but uncommon granulomatous lesions resulting from cholesterol crystal accumulation, with a foreign body-type giant cell reaction. In human beings, cholesterol granulomas usually develop in the mastoid region in association with chronic middle ear disease (Eisenberg, Haddad & Al-Mefty 1997). Reports of such lesions are comparatively rare in domestic animals with the exception of the horse, in fact up to 20% of older horses have cholesterol granulomas in the choroid plexus of the lateral and fourth ventricles (Jackson, deLahunta, Dykes & Divers 1994). Cholesterol granulomas have also been rarely reported in dog, cat and parrot (Jubb & Huxtable 1993; Bavelaar & Beynen 2004; Fliegner, Jubb & Lording 2007). As yet, there has been no report of this entity affecting the heart of a fish. We describe such a case in a piper gurnard, Trigla lyra (L.). An adult male piper gurnard, with tachypnea, swimming difficulty and loss of appetite was examined at the clinical laboratory of the Genoa Aquarium. The fish weighed 2.5 kg and had a total length of 59 cm. The animal had been kept in a community tank for more than 4 years. Parasitological examination revealed skin infection by ciliates. Despite a specific antiparasitological
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Correspondence G E Magi, Department of Veterinary Science, University of Camerino, Via Circonvallazione 93/95, 62024 Matelica, Italy (e-mail:
[email protected])
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treatment, lethargy and debilitation progressed and the animal died after 1 month from the appearance of the first clinical signs. The necropsy revealed a large, adherent, yellowish, multinodular cardiac mass occupying all the surface of the atrium and partially covering the ventricle below (Fig. 1). At the base of the gills multiple or solitary bulging red nodules from 3 mm to 1 cm in diameter, that grossly looked like haemangiomas, were also observed. Samples from cardiac masses, gill nodules and various organs (liver, spleen, gut, kidney, skin) were fixed in 10% buffered formalin, processed for histology and embedded in paraffin. Tissue sections (4 lm) were stained with haematoxylin and eosin (H & E) and PearlÕs Prussian blue. Histologically, the cardiac masses were composed of numerous formations constituted from clear, elongated, irregularly arranged, cholesterol clefts surrounded by aggregates of lymphocytes, numerous eosinophilic granular cells and fibroblasts (Figs 2–4). Rare Tuton-type giant cells as well as haemosiderin-laden macrophages stained with PerlÕs Prussian blue were shown. The granulomatous formations were localized in the atrium and they affected the epicardium and the spongy atrial wall. The latter appeared almost completely occupied by the granulomatous formations. Histopathology was clearly diagnostic of cardiac cholesterol granulomas. Beside the lipid granulomas, other histological lesions were represented by the presence of angiomatous/pseudoangiomatous nodular formations on the gills. These lesions appeared to be located at the base of the primary lamellae and were
Journal of Fish Diseases 2009, 32, 473–475
Figure 1 Trigla lyra heart. Gross appearance showing yellowish nodular formations on the surface of the atrium (arrow).
Figure 2 Elongated empty clefts typical of cholesterol crystals (arrows) and granuloma formation (haematoxylin and eosin, ·4).
Figure 3 Cholesterol clefts surrounded by inflammatory cells (haematoxylin and eosin, ·20).
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surrounded by an epithelium, underneath which there was connective tissue delimiting large vascular spaces filled with erythrocytes and plasma material 474
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Figure 4 Eosinophilic granular cells, haemosiderin-laden macrophages and lymphocyte infiltrates (haematoxylin and eosin, ·60).
Figure 5 Angiomatous/pseudoangiomatous formation at the base of the gill (haematoxylin and eosin, ·4).
and lined by a layer of endothelial cells (Fig. 5). No further histopathological findings were observed in the other tissues. The pathophysiologic process leading to cholesterol granuloma formation is not known. Some authors believe that cholesterol granuloma develops at sites of old haemorrhages and/or tissue necrosis as a result of an inflammatory focus (Luckraz, Coulston & Azzu 2006). Cholesterol is rich in erythrocyte membranes and high density lipoprotein serum. In human beings, the pathogenesis for cholesterol granuloma of the middle ear and air sinuses is believed to be a trauma coupled with impaired lymphatic drainage and ventilation that account for the precipitation of cholesterol crystals (Eisenberg et al. 1997; Luckraz et al. 2006). In the mastoid region, cholesterol deposition occurs in or adjacent to the mastoid air cells following blockage
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of the air cell system in which negative pressure and hypoxia lead to local tissue and blood cell necrosis. Poor lymphatic drainage is considered when the cholesterol granulomas occur in the brain of horses following haemorrhage, as described in the wellknown cholesteatoma of the choroid plexus (Jackson et al. 1994). Otherwise, hypercholesterolaemia may predispose to development of cholesterol granulomas by transudation of serum cholesterol. In human beings, two cases of cerebral cholesterol granulomas have been associated with familial hypercholesterolaemia (Francis, Johnson, Findlay, Wang & Hegele 2005). In captive meerkats, five cases of cholesterol granulomas affecting different tissues associated with high levels of serum cholesterol have been reported (Sladky, Dalldorf, Steinberg, Wright & Loomis 2000; Allan, Waters, Ashton & Patterson-Kane 2006). A link between inflammation/haemorrhage and cholesterol granuloma formation in the heart as described in this report is unlikely. Also, the presence of scanty macrophages containing haemosiderin excludes the hypothesis of a previous haemorrhage phenomenon. In this case, the serum lipid profile as well as the serum cholesterol level were unknown, although hypercholesterolaemia seems to be the more likely determinant factor. The angiomatous/pseudoangiomatous formations observed at the base of the gills could originate next to a hypertension condition produced by the compressing activity of cholesterol granulomas on the atrium. In wild and domestic animals, an occurrence of cardiac cholesterol granulomas seems to be very rare as only a unique case affecting the pericardium of a captive meerkat has been reported (Sladky et al. 2000). Considering fish species, the sole report of cholesterol granuloma is in three smooth dogfish, Mustelus canis (Mitchill), where the authors describe cholesterol and foreign body granulomas in the epigonal organ (Borucinska & Frasca 2002). Although a variety of lesions of the fish heart have been previously described, especially in salmonids (Roberts & Rodger 2001), to our
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knowledge there have been no previous reports of cardiac cholesterol granulomas in a fish. References Allan K.J., Waters M., Ashton D.G. & Patterson-Kane J.C. (2006) Meningeal cholesterol granulomas in two meerkats (Suricata suricatta). Veterinary Record 158, 636–637. Bavelaar F.J. & Beynen A.C. (2004) Atherosclerosis in parrots. A review. The Veterinary Quarterly 26, 50–60. Borucinska J.D. & Frasca S. (2002) Naturally occurring lesions and micro-organisms in two species of free-living sharks: the spiny dogfish, Squalus acanthias L., and the smooth dogfish, Mustelus canis (Mitchill), from the north-western Atlantic. Journal of Fish Diseases 25, 287–296. Eisenberg M.B., Haddad G. & Al-Mefty O. (1997) Petrous apex cholesterol granulomas: evolution and management. Journal of Neurosurgery 86, 822–829. Fliegner R.A., Jubb K.V.F. & Lording P.M. (2007) Cholesterol granuloma associated with otitis media and destruction of the tympanic bulla in a dog. Veterinary Pathology 44, 547–549. Francis G.A., Johnson R.L., Findlay J.M., Wang J. & Hegele R.A. (2005) Cerebral cholesterol granuloma in homozygous familial hypercholesterolemia. Canadian Medical Association Journal 172, 495–497. Jackson C.A., deLahunta A., Dykes N.L. & Divers T.J. (1994) Neurological manifestation of cholesterinic granulomas in three horses. Veterinary Record 135, 228–230. Jubb K.V.F. & Huxtable C.R. (1993) The nervous system. In: Pathology of Domestic Animals, Vol. 1, 4th edn (ed. by K.V.F. Jubb, P.C. Kennedy & W. Palmer), pp. 267–269. Academic Press, San Diego, USA. Luckraz H., Coulston J. & Azzu A. (2006) Cholesterol granuloma of the superior mediastinum. The Annals of Thoracic Surgery 81, 1509–1510. Roberts R.J. & Rodger H.T. (2001) The pathophysiology and systemic pathology of teleosts. In: Fish Pathology, 3rd edn (ed. by R.J. Roberts), pp. 53–132. WB Saunders, Edinburgh, UK. Sladky K.K., Dalldorf F.G., Steinberg H., Wright J.F. & Loomis M.R. (2000) Cholesterol granulomas in three meerkats (Suricata suricatta). Veterinary Pathology 37, 684–686. Received: 13 June 2008 Revision received: 17 September 2008 Accepted: 3 October 2008
