Feline Histoplasmosis with Ocular Involvement

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1 Vet. Pathol. 18: (1981) Feline Histoplasmosis with Ocular Involvement D. H. PERCY Department of Microbiology and Immunology, Health Sciences Centre, University of Western Ontario, London, Ontario, Canada Abstract. A 12-year-old, castrated male cat with a history of respiratory disease developed bilateral endophthalmitis, retinal detachment, and granulomatous choroiditis, and unilateral glaucoma, and was killed. Other lesions included granulomatous optic neuritis, myositis involving extraocular muscles, and focal retinitis. Light and electron microscopy showed many intracellular organisms, interpreted to be Histoplusmu. Granulomatous inflammatory lesions and organisms were present in lung, liver, lymphoid tissues, and adrenals. Histoplasmosis is a mycotic infection that affects both animals and man in many countries throughout the world. It is transmitted via inhalation of spores from histoplasma-contaminated soil. In spite of the association between the organism and soil contaminated by bird droppings, spontaneous histoplasmosis has not been recognized in birds [7]. Spontaneous cases of histoplasmosis have been reported in several species [7], dogs being most commonly affected among domestic animals, but relatively few cases are reported in the cat. Lesions described in cats have included focal to diffuse granulomatous pneumonitis, interstitial myocarditis, granulomatous dermatitis, and mycotic osteomyelitis [l, 5, 161. This report describes a cat with generalized histoplasmosis with severe ocular involvement. Case History A Ityear-old, domestic short haired, neutered male cat had had periodic illness of approximately three months before death. Clinical signs included chronic dyspnea, coughing, stiffness, periodic anorexia, and intermittent pyrexia. Parenteral antibiotics were given during periods of high fever, with varied degrees of success. Bilateral cloudiness of the eyes became visible about three weeks before death. The progressive deterioration and the age of the patient led to a poor prognosis, and the animal was killed by parenteral administration of pentobarbitone sodium. Materials and Methods Tissues were futed in Bouin s fluid or 10% neutral buffered formalin, sectioned at 6 pm, and stained with hematoxylin and eosin (HE) or periodic acid-schiff (PAS). Tissues processed for electron microscopy were post-fixed in 3% glutaraldehyde, minced, dehydrated, and embedded I63

2 I64 Percy in Spurr's medium. One-micrometer sections were stained with toluidine blue or Gomori's methenamine silver [9]. Thin sections were stained with uranyl acetate and Reynold's lead citrate, and examined in an electron microscope. Gross findings Results The cat was thin, without body fat reserves. The right eye was markedly enlarged. On cut section, the diameter of the globe of the right eye was 2.5 cm and of the left eye 2.1 cm, measured along the meridional plane. There was bilateral retinal detachment, with the only points of attachment at the ora serrata and the optic disk (fig. I). Cloudy exudate was present in the vitreous cavity, including areas between the choroid and the detached retina. The lungs were mottled with diffuse, pale, grey to tan areas, and were of moderately-firm, rubbery consistency, particularly the diaphragmatic lobes. The liver was tan and enlarged, with many circumscribed, pale, solid to cystic areas up to 5 mm in diameter scattered throughout the parenchyma. The spleen was enlarged, with many pale fracture sites on the surface. The gastrointestinal tract contained scanty ingesta, and there was marked thickening of the intestinal wall. Subcutaneous and mesenteric lymph nodes were enlarged, with poorly delineated corticomedullary regions. Histology There was a severe granulomatous choroiditis and retinal detachment involving both eyes. Lesions were characterized by a marked infiltration of lymphocytic and histiocytic cells in the choroid, with virtual obliteration of the normal architecture, and proliferation of pigment epithelial cells. In some areas, the cellular infiltrate was one hundred or more cells in width (fig. 2). Some lesions were characterized by hemorrhagic choroiditis, with concurrent infiltration by histiocytes and neutrophils. Neutrophils were scattered throughout the affected choroid, and leukocytes, macrophages, and pigment-bearing cells were scattered between the detached retina and choroid, and to a lesser extent, throughout the vitreous cavity. There were many vacuolated histiocytes containing abundant minute spherical to oval structures with a distinct center surrounded by a clear area and a distinct border (fig. 3). PAS and silver stains showed these intracellular organisms to be 2 to 4 pm in diameter and circular, with a clearly delineated center and a distinct peripheral rim. Up to 20 organisms were present in the cytoplasm of some individual macrophages (fig. 3). In the detached retinas of both eyes, there were marked undulations and distortion of the normal architecture, and diffuse mononuclear cell infiltration in some areas, with lymphocytes predominating. The width of the neural retina varied in some areas, with moderate proliferation of capillaries, hyperplasia and hypertrophy of endotheiial cells lining vessels, and focal mononuclear cell infiltrates (fig. 4). PAS showed histoplasma organisms scattered sparsely in the optic fiber and inner plexiform layers of the retina. Electron microscopy of sections of choroid showed numerous circular structures 2 to 3.5 pm in diameter with electron-lucent and irregular electron-dense areas, and a peripheral halo of electron-lucent material in vacuoles of macrophages (fig. 5, 6).

3 Fig. 1: Meridional section of right eye from cat with ocular histoplasmosis. Abundant flocculent exudate between choroid and detached retina. Portions of displaced retina close to posterior surface of lens (arrow). Fig. 2 Histological section of sclera (S) and choroid (C) from same eye as fig. I. Granulomatous choroiditis with massive cellular infiltration. Inflammation extends into globe beyond Bruch's membrane (arrow). PAS. Fig. 3 a. Higher magnification of choroid, I-pm section. Many epithelial cells, spherical histoplasma organisms (arrows) in cytoplasm. Toluidine Blue. b. Choroid. Many organisms in phagocytic cells (arrows). Dense central area, halo and clearly delineated periphery of individual organisms. Gomori's methenamine silver. Fig. 4 Focus of granulomatous retinitis in section of detached retina. Mononuclear cells present in optic fiber layer (arrow), inner plexiform layer (P), and bipolar cell layer (B).

4 I66 Percy Fig. 5: Macrophages contain many histoplasma organisms in membrane-bound vacuoles (arrow). Indentation of cell nucleus, electron-dense and electron-lucent areas in organisms, and distinct, clear halo interpreted to be cell wall, surrounding each organism. Bar = 3 pm. Fig. 6 Higher magnification of macrophage containing organisms in membrane-bound vacuole. Internal structure of organisms and clear peripheral halo (arrow) are evident. Bar = 2 pm. The morphologic and staining properties of these organisms by light and electron microscopy were compatible with those described for Histoplusmu cupsulutum [3]. In the right eye only, there was an extensive histiocytic and lymphocytic cell infiltrate in the optic nerve, which obliterated the normal architecture, and many histoplasma organisms were found in inflammatory cells. The granulomatous inflammation extended into segments of the extraocular muscles and periorbital soft tissue adjacent to the sclera. Some segments of extraocular muscle had a granulomatous myositis, with marked lymphocytic and histiocytic cell infiltrates and partial to complete obliteration of the normal architecture of individual myofibers. Typical histoplasma organisms were present in scattered macrophages in affected muscle. Nerve trunks associated with affected extraocular muscle were spared from the inflammatory process. In general, the sclera was histologically normal, but with scattered foci of segmental separation of scleral fibers and mononuclear cell infiltration. The cornea and lens of both eyes were histologically normal and no organisms were found in the sclera, cornea, or lens. There was also a chronic conjunctivitis characterized by subepithelial lymphocytic infiltration. The leptomeninges of the brain had sparse, scattered aggregates of lymphocytes

5 Feline Ocular Histoplasmosis and histiocytes. The lung showed a diffuse, disseminated chronic interstitial pneumonitis characterized by thick alveolar septa and infiltration with mononuclear and a sprinkling of polymorphonuclear cells. PAS showed many H. cupsulutum organisms in macrophages. There was a focal interstitial myocarditis and chronic granulomatous hepatitis, characterized by diffuse lymphocytic and histiocytic cell infiltrations in the periportal regions and throughout the parenchyma of individual lobules. In some areas, the infiltrate obliterated the normal architecture of the liver. Many PASpositive organisms were present in the cytoplasm of Kupffer cells and free macrophages. The spleen had prominent lymphoid follicles, and scattered macrophages in the sinusoids contained histoplasma organisms. In subcutaneous lymph nodes, there was a marked granulomatous lymphadenitis. Some histiocytic cells in the medullary and peripheral sinuses contained histoplasma organisms. In the adrenal gland, a granulomatous inflammatory reaction involved the subcapsular and interstitial regions of the cortex and medulla. Moderate hyperplasia of Peyer s patches was evident in the intestine, but few organisms were seen. A few histoplasma-bearing histiocytic cells were present in the bone marrow. Discussion I know of no previously reported cases of feline histoplasmosis in Canada. Histoplasmin sensitivity, however, has been found among the human population, and winter climates apparently do not kill the fungus [2]. Canine histoplasmosis has been found in Ontario, and the importance of the dog as a sentinal animal in areas where H. capsulutum may occur as a soil-borne infection has been emphasized [2]. Current reports suggest that cats are less susceptible than dogs [6, 101. In one study, H. cupsulutum was isolated from several cats sampled in Virginia. There were no characteristic lesions associated with the isolation of the organism, however, and histoplasma was not demonstrated microscopically in tissues from these cats [ 101. A recent study of histoplasmosis in three cats in Kansas reported granulomatous pulmonary lesions, and microscopic examination showed histoplasma organisms in the lungs [5]. The distribution and extent of lesions varied in the three cats and included focal granulomatous dermatitis, focal hepatitis, mycotic osteomyelitis and granulomatous lymphadenitis. Eyes from two cats were examined histologically; they were normal in one. The second cat had bilateral granulomatous chorioretinitis with retinal detachment [5]. Choroiditis was seen recently in another case of disseminated histoplasmosis in a cat [4]. No mention was made of lesions in other structures such as optic nerve and periorbital tissue. Deep seated mycotic infections involving the eye have been reported for a variety of fungi, usually associated with a more generalized infection. In one report of ocular lesions in two dogs with disseminated coccidioidomycosis, one eye of each dog was affected, with granulomatous uveitis, retinitis, and keratitis [ 141. A report on blastomycosis in a coonhound with bilateral ocular involvement described retinal detachment, subretinal exudation and leukocytic infiltration, granulomatous optic neuritis, retinitis, and secondary glaucoma [ 151. A case of feline cryptococcosis, with extension I67

6 I68 Percy of the granulomatous inflammatory process along the leptomeninges of the optic nerves and invasion of the optic disk and adjacent choroid, has been described [8]. Granulomatous lesions of cryptococcal infection in the canine eye also have been described [I I]. In the deep mycoses, the presence of disseminated lesions indicates a generalized disease, and invasion of the eye may occur as a hematogenous infection. In view of the frequent involvement of the optic nerve, however, the organism could invade the eye locally via this route. In this cat, the localization of the organisms in the optic fiber and ganglion cell layers of the retina with concurrent optic neuritis indicates that neurogenous spread may occur. Ocular histoplasmosis does occur in man, usually associated with hemorrhagic or nonhemorrhagic macular lesions, diskiform detachment of the sensory retina, and choroidal scarring [ 121. Organisms usually are not demonstrable in the affected human eye. Occasionally, a progressive, granulomatous form of ocular histoplasmosis occurs in man, sometimes with concurrent involvement of the lung, liver, and spleen [ 131. In general, lesions in this feline case are similar to those seen in the granulomatous form of ocular histoplasmosis in man [ 131. Acknowledgements Supported in part by NIH grant EYO1833-I. The technical assistance of Elaine Hunter and Kathy Fuller is acknowledged. References 1 AKUN, R.S.: Histoplasmosis in a cat. J Am Vet Med Assoc , DITCHFIELD, J.: Man, dogs, and histoplasmosis. Can J Public Health , DUMONT, A.; PICHB. C.: Electron microscopic study of human histoplasmosis. Arch Pathol 87: , GWIN, R.M.; MAKI-EY, T.A.; WYMAN, M.; WERLING, K.: Multifocal ocular histoplasmosis in a dog and cat. J Am Vet Med Assoc , MAHAFFEY, E.; GABBERT, N.; JOHNSON, D.; GUFFY, M.: Disseminated histoplasmosis in three cats. J Am Anim Hosp Assoc , MENGES, R.W.; FURCOLOW, M.L.; HABERMANN, R.T.: An outbreak of histoplasmosis involving animals and man. Am J Vet Res , MIGAKI, G.; VOELKER, F.A.; SAGARTZ, J.W.: Fungal diseases. In: Pathology of Laboratory Animals, ed. Benirschke, Garner and Jones, pp Springer-Verlag, N.Y., OLANDER, H.J.; REED, H.; PIER, A.C.: Feline cryptococcosis. J Am Vet Med Assoc , ROSENQUIST, T.H.; SLAVIN, B.S.; BERNICK, S.: The Pearson silver-gelatin method for light microscopy of p plastic sections. Stain Techno1 46: , ROWLEY, D.A.; HABERMAN, R.T.; EMMONS, C.W.: Histoplasmosis: Pathologic studies of fifty cats and fifty dogs from London County, Virginia. J Infect Dis %98-108, 1954 I1 RUBIN, L.F.; CRAIG, P.H.: Intraocular cryptococcosis in a dog. J Am Vet Med Assoc 147: 27-32, SCHLAEGEL, T.F.: Introduction to the proceedings of the ocular histoplasmosis symposium. Int Ophthalmol Clin , SCHWARTZ, J.: Granulomatous histoplasmosis of the eye: A rare disease. Int Ophthalmol Clin , 1975

7 Feline Ocular Histoplasmosis I69 14 SHIVELY, J.N.; WHITEMAN. C.E.: Ocular lesions in disseminated coccidioidomycosis in 2 dogs. Pathol Vet 7: 1-6, TREVINO, G.S.: Canine blastomycosis with ocular involvement. Pathol Vet , WEISSMAN, S.; ACAMPADO, E.E.: Primary pulmonary histoplasmosis in a cat. Feline Pract Request reprints from D.H. Percy, Health Sciences Centre, University of Western Ontario, London, Ontario, N6A 5C 1 (Canada).

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