Lesions of Neonatally Induced Toxoplasmosis in Cats
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1 Vet Pathol33: (1 996) Lesions of Neonatally Induced Toxoplasmosis in Cats J. P. DUBEY, M. E. MATTIX, AND T. P. LIPSCOMB Parasite Biology and Epidemiology Laboratory, Livestock and Poultry Sciences Institute, Agricultural Research Service, US Department of Agriculture, Beltsville, MD; and Department of Veterinary Pathology, Armed Forces Institute of Pathology, Washington, DC Abstract. Five pregnant queens were inoculated orally with Toxoplasma gondii tissue cysts. Twenty-two live and three dead kittens were born 16 to 3 1 days after inoculation. Four kittens were eaten by queens and, thus, were not available for histologic examination. Twenty-one kittens that died or were euthanatized on day 2 (two kittens), 4 (one kitten), 5 (five kittens), 6 (five kittens), 7 (one kitten), 8 (four kittens), 16 (two kittens), and 29 (one kitten) after birth were studied histologically. T. gondii was detected by bioassay and was seen in histologic sections of tissues from all 2 1 kittens. The histologic lesions associated with neonatal toxoplasmosis were widely disseminated infiltrates of macrophages and neutrophils often accompanied by necrosis; lymphocytes and plasma cells were occasionally present. The most consistent lesions were proliferative interstitial pneumonia (2 1/2 1); necrotizing hepatitis (20/21); myocarditis (2 1/2 1); skeletal myositis (2 1/2 1); glossal myositis (1 9/19); nonsuppurative encephalitis affecting the cerebrum (1 8/18), brain stem ( ), and spinal cord (9/9); uveitis (1 9/ 19); necrotizing adrenal adenitis (1 8/ 18); and interstitial nephritis ( ). Placental lesions (2/2) consisted of grossly visible areas of necrosis and mineralization. Key words: Lesions; tachyzoites; tissue cysts; Toxoplasma gondii; toxoplasmosis; transplacental. Cats are the key animal species in the life cycle of the protozoan parasite Toxoplasma gondii because they are the only hosts that excrete the environmentally resistant oocysts in their feces.'x2 Most cats infected with T. gondii remain clinically normal but a small proportion die from severe toxoplasmosis.3~4 Although lesions of toxoplasmosis in naturally infected cats have been described in several reports, little is known of pathological changes of feline neonatal toxoplasmosis.1,4,7,8j1j2 Lesions in postnatally infected cats were characterized previo~sly.~.~ There is no report describing lesions in cats congenitally infected with T. gondii. The objective of this study was to characterize lesions of experimentally induced toxoplasmosis in neonatal luttens. Materials and Methods Sixteen pregnant Toxoplasma gondii-free queens were inoculated orally with tissue cysts of the ME-49 strain of T. gondii, and the products of conception were examined histologically and tested for T. gondii by bioassay in mice as previously de~cribed.~ Eight queens were euthanatized on the day of parturition or after a predetermined period of time following T. gondii inoculation. Eight queens were allowed to deliver and nurse their kittens nat~rally;~ kittens from only five of these eight queens were selected for the present study of histologic lesions. Clinical signs, biochemical evaluations, and serologic examination of neonatally infected kittens were reported previo~sly.~ All kittens that died or were euthanatized were necropsied. 290 Euthanasia was accomplished by intravenous administration of pentobarbital sodium. Samples of thymus, lungs, heart, liver, spleen, kidneys, adrenal glands, mesentenc and bronchial lymph nodes, urinary bladder, ureter, stomach, intestines, skeletal muscle, tongue, haired skin, brain, spinal cord, and eyes were fixed in 10% neutral buffered formalin. From euthanatized kittens, entire spinal cord, brains, and small intestines were removed, and transverse sections were made at 0.5-cm intervals. Tissues were embedded in paraffin and sections were cut at 5-pm thickness and routinely stained with hematoxylin and eosin (HE). Selected tissues were embedded in methylacralate, cut 3-pm thick and stained with HE. Certain sections were deparaffinized and stained with anti- T. gondii serum in an avidin-biotin immunohistochemical stain procedure as described.13 Results The five queens selected for this study had 25 fullterm kittens. Queen No. 1 had 5 kittens (Nos. 1-5) 16 days after inoculation (DAI) with Toxoplasma gondii. Kitten No. 1, the runt, was born dead and was eaten by the queen. Qtten Nos. 2 and 3 were found dead on the 6th day after birth. Kitten Nos. 4 and 5 were hypothermic, vocalized often, and were ignored by the queen; they were euthanatized at 6 days of age. Queen No. 2 had four apparently healthy kittens (Nos. 6-9) 23 DAI. Kitten Nos. 6 and 7 were eaten by the queen between 7 and 8 days after birth. Kitten No. 8 was unconscious and was euthanatized on the 8th day after birth. Kitten No. 9 appeared to be normal
2 Vet Pathol 33:3, 1996 Neonatal Toxoplasmosis in Cats 29 1 Fig. 1. Liver and heart; lutten No. 24. Disseminated throughout the hepatic parenchyma there are multifocal and coalescing pale zones of necrosis. There are multiple pale foci of necrosis throughout the atrial and ventricular myocardium. Bar = 1 cm. Fig. 2. Placenta; kitten No. 25. The allantochorion contains numerous pale foci of necrosis. Bar = 1 cm. until day 29 when it was found to be weak and lethargic; euthanasia was performed. Queen No. 3 had six kittens (Nos ) 24 DAI. The queen ate two kittens on the 2nd day after birth. IOtten No. 12 was euthanatized at 2 days of age because of weakness. Kitten No. 13 died on the 8th day after birth and the queen ate the head and part of thorax. Kitten No. 14 died on the 16th day after birth. EOtten No. 15 was unconscious on the 16th day after birth and was euthanatized. Queen No. 4 had four kittens (Nos ) 24 DAI. Kittens died 2,4,5, and 5 days after birth, respectively. Queen No. 5 had six kittens (Nos ) 31 DAI. IOtten Nos. 20 and 2 1 died on the 5th day after birth. Kitten No. 22 died on the 8th day after birth. Kitten No. 23 was euthanatized on the 6th day after birth. IOtten No. 24 died on the 8th day after birth, and kitten No. 25 was euthanatized on the 8th day after birth in apparent good health. T. gondii was isolated by bioassay in mice inoculated with tissues from each of 21 kittens9 and was seen in histologic sections of all 2 1 kittens. Gross lesions were identified in 19 kittens. In all 19, the liver was enlarged and friable and had disseminated yellowish white 1-4 mm foci (Fig. 1). The heart had similar yellowish white foci in four kittens. Edema, congestion, or foci of consolidation were seen in the lungs of 10 kittens. Foci of hemorrhage (1-2 mm) and yellow-to-white areas (1-3 mm) were present on the cortical surfaces of the kidneys of two kittens. Two to 5 ml of clear or blood-tinged fluid was found in the peritoneal cavities of two kittens. Multifocal pale areas up to 2 mm in diameter were observed within the placental labyrinth (Fig. 2) of two kittens. Histologic lesions associated with neonatal toxoplasmosis were similar in all kittens evaluated and consisted of infiltrates of macrophages and neutrophils often accompanied by necrosis; lymphocytes and plasma cells were also present occasionally. The organs most consistently affected were the lungs (2 112 l), liver (20/21), heart (2 1/2 l), skeletal muscle (2 1/2 l), tongue (1 9/19), cerebrum (1 8/ 1 S), brain stem (1 5/ 1 5), spinal cord (9/9), eye (1 9/ 19), adrenal gland (1 8/1 S), and kidney (1 6/2 1). Throughout the liver, there were random multifocal to coalescing zones of coagulative and lytic hepatocellular necrosis (Fig. 3). Small to moderate numbers of neutrophils and macrophages, and sometimes fewer lymphocytes and plasma cells were scattered in the cellular debris. Necrotic cells were often mineralized. There were areas of hepatocellular loss with collapse of reticular stroma. Adjacent hepatocytes frequently had vacuolated cytoplasm. Portal areas contained small aggregates of lymphocytes, plasma cells, macrophages, and fewer neutrophils. Multifocally, blood vessel walls were infiltrated by degenerate and viable neutrophils and fewer lymphocytes. Often the tunica media of affected blood vessels was disrupted by karyorrhectic debris. There were multifocal, often perivascular, aggregates of hematopoietic cells. Diffusely, pulmonary alveolar septa were greatly expanded by infiltrates of macrophages and fewer lymphocytes and neutrophils. There was hyperplasia of type I1 pneumocytes and septa1 capillaries were con-
3 292 Dubey, Mattix, and Lipscomb Vet Pathol 33: Fig. 3. Liver; kitten No. 8. Normal hepatic architecture is disrupted by multifocal and coalescing zones of hepatocellular lytic necrosis and mineralization. HE. Bar = 100 pm. Fig. 4. Lung; kitten No. 14. Alveolar septa are markedly expanded by macrophages, lymphocytes, fewer neutrophils, and type I1 pneumocytes. Alveoli contain edema fluid and histiocytes. HE. Bar = 50 km. Fig. 5. Kidney, cortex; kitten No. 9. Two intracellular tachyzoites (arrow) are within the glomerulus. HE. Bar = 29 pm. Fig. 6. Tongue; kitten No Glossal myocytes are separated by a mixed leukocytic infiltrate. Note tachyzoites within focus of inflammation (arrow). HE. Bar = 70 pm gested. Alveoli contained edema fluid, erythrocytes, and numerous large macrophages with vacuolated cytoplasm (Fig. 4). Multifocal necrosis of alveolar septa was present in the lung of one kitten. Within the renal cortices, aggregates of macrophages, neutrophils, and fewer lymphocytes surrounded and replaced tubules. Tubular epithelial cells within these foci were often necrotic. In one kitten, there was suppurative pyelonephritis, characterized by abundant viable and degenerate neutrophils that filled the pelvis and infiltrated the adjacent renal parenchyma. The interstitium surrounding arcuate arteries was often edematous and contained small numbers of similar inflammatory cells. Tachyzoites were seen in tubular epithelium, interstitium, and within glomeruli (Fig. 5). Lymph nodes were similar in most cases. Subcapsular and medullary sinuses were mildly expanded by edema fluid and increased numbers of histiocytes. In several lymph nodes many histiocytes contained erythrocytes and hemosiderin. In four kittens, sinuses contained moderate numbers of neutrophils and cellular debris. Disseminated throughout the adrenal cortex and rarely extending into the medulla were multifocal to
4 Vet Pathol 33:3, 1996 Neonatal Toxoplasmosis in Cats 293 Fig. 7. Eye, retina; kitten No. 15. A nodular aggregate of macrophages and neutrophils expands the inner retina. Note intracellular tachyzoites (arrows). HE. Bar = 50 pm. Fig. 8. Cerebrum; kitten No. 9. A capillary endothelial cell contains four dividing tachyzoites (arrow). HE. Bar = 20 pm. Fig. 9. Cerebrum; kitten No. 9. Within the neuropil is a penvascular nodular aggregate of macrophages, lymphocytes, and glial cells. HE. Bar = 50 pm. Fig. 10. Cerebellum; kitten No. 48. A glial nodule surrounds a Toxoplasma gondzi tissue cyst. HE. Bar = 70 pm. coalescing areas of lytic necrosis that contained scattered neutrophils and macrophages and fewer lymphocytes. Loss of parenchymal cells, collapse of stroma, and hemorrhage were also present. Ventricular and atrial myocardium had multifocal to coalescing areas of necrosis that contained and were surrounded by neutrophils, macrophages, and fewer lymphocytes. Skeletal muscle including that of the tongue was similarly affected (Fig. 6). Throughout the red pulp of the spleen there were aggregates of large histiocytes. In three kittens, there were random areas of necrosis surrounded by neutrophils and macrophages. Within the white pulp of two kittens there was frequent lymphocytolysis. Ocular lesions were restricted to the vascular tunic and, occasionally, the retina. The iris, ciliary body, and choroid were expanded multifocally by moderate numbers of macrophages, neutrophils, lymphocytes, and plasma cells. The retina contained widely scattered nodular aggregates of macrophages and fewer neutro-
5 294 Dubey, Mattix, and Lipscomb Vet Pathol 33:3, 1996 phils in nine of 17 kittens in which retina was available for examination. T. gondii tachyzoites were commonly seen within the choroid and less frequently in the retina (Fig. 7). The immunohistochemical procedure demonstrated more organisms than were found in adjacent sections stained with hematoxylin and eosin (HE). Lesions at all levels of the central nervous system were similar. Disseminated throughout the cerebrum, brain stem, and spinal cord and less frequently in the cerebellum, were discrete, multifocal, often perivascular, nodular aggregates of macrophages, lymphocytes, and scattered neutrophils admixed with cellular debris (Figs. 8-10). Multifocal mild gliosis and hemorrhage were also present. Occasionally, adjacent axons were swollen and brightly eosinophilic. Choroid plexus was multifocally expanded by small numbers of lymphocytes, plasma cells, macrophages, and fewer neutrophils. T. gondii tachyzoites were observed in capillary endothelium (Fig. S), in perivascular tissue, and in neurons. Tissue cysts (Fig. 10) were rare. In both placentas there were multifocal areas of necrosis with frequent mineralization of necrotic cells (Figs. 1 1, 12). Multifocally within the chorionic villi, there were aggregates of neutrophils admixed with necrotic cellular debris. T. gondii tachyzoites were few, often degenerate, and were not readily seen in HEstained sections. Immunohistochemical staining aided in recognition of tachyzoites. Discussion All 21 kittens were considered to be congenitally infected because queens were inoculated with Toxoplasma gondii during pregnancy, all littermates were infected, at least three kittens had severe toxoplasmosis at 2 days of age, and 18 of 21 kittens died or were ill and were euthanatized within 8 days of age. Lesions in ludneys, lymph nodes, intestines, and lungs in congenitally (parenterally) infected cats differ from those in postnatally (orally) infected cats. After ingestion, T. gondii multiplies initially in the small intestine and associated lymph nodes and infection then spreads to liver and other organs. The stage of T. gondii ingested and the age of the cat significantly affect the course of the diseases. Newborn kittens (< 1 week old) fed tissue cysts became ill and most died from enteritis, mesenteric lymph node necrosis, and he pa ti ti^.^ Weaned kittens (> 6 weeks old) fed tissue cysts often developed mild illness and the predominant lesion was encephalitis whereas mature cats (> 6 months) did not develop clinical toxoplasmosis.5 Newborn kittens fed tachyzoites and oocysts did not develop clinical toxoplasmosis. The predominant lesions in parenterally inoculated cats were pneumonia, hepatitis, and encephalitis, but enteritis was not seen (J. P. Dubey, unpublished). Therefore, the absence of intestinal and mes- Fig. 11. Placental labyrinth; kitten No. 25. The normal lamellar architecture of the allantochorion is disrupted by a large focus of necrosis and mixed leukocytic infiltration. The overlying chorionic mesenchyme is unaffected (arrows). HE. Bar = 200 pm. Fig. 12. Placental labyrinth; kitten No. 25. Edema and macrophages expand the allantochorion. Note both free and intracellular tachyzoites (arrows). HE. Bar = 20 pm.
6 Vet Pathol 33:3, 1996 Neonatal Toxoplasmosis in Cats 295 enteric lymph node lesions and the presence of severe hepatitis in the present study are compatible with parenteral rather than oral acquisition of T. gondii infection in these congenitally infected kittens. Hepatic lesions were extensive and severe, and, thus, probably contributed to the fatal outcome in some cases. Although much of the hepatic parenchyma was necrotic, only a few T. gondii were seen in the lesions; thus, ischemia secondary to necrotizing vasculitis may have caused much of the hepatic necrosis. Alternatively, the hepatic necrosis may have occurred by other mechanisms and resulted in the destruction of many tachyzoites leaving a paucity of detectable organisms. The lack of intestinal lesions and the presence of severe hepatic lesions suggest that fetal tissues are invaded by systemic circulation rather than via ingestion of T. gondii from the amniotic fluid. Pneumonia is the most predominant lesion of naturally occurring fatal toxoplasmosis in cats. In one study, interstitial pneumonia with necrosis was found in 84 of 86 cats with fatal to~oplasmosis.~ In congenitally infected kittens of the present study, pulmonary lesions were primarily inflammatory with little necrosis. Encephalomyelitis was an important lesion in congenitally infected httens. The predominant lesion in the central nervous system was nodular gliosis, with rare necrosis. The glial nodules were probably a reaction to focal vasculitis, because T. gondii proliferated in capillary endothelium and tachyzoites were seen among inflammatory cells in the earliest lesions. Glial nodules might also result from the rupture of tissue cysts, but no evidence of this was found in the present study. Renal lesions similar to those seen in the kittens in the present study were reported in young (<4 weeks old) naturally infected kitten~.~f,~j Although observations are limited to a few litters of naturally congenitally infected cats, nephritis appears to be a consistent feature of congenitally acquired toxoplasmosis in cats. This is the first report of placental toxoplasmosis in cats or other species of carnivores. It was fortuitous that placentas were obtained from cats in the present study because cats quickly consume the afterbirth. T. gondii produces pathognomonic lesions in the placenta of sheep and goats, consisting of multifocal necrosis and mineralization of cotyledonary villi; T. gondii is never numerous even when macroscopic lesions are present.2 Placental lesions in pigs were rarely macroscopic although they contained large numbers of T. gondii. lo References 1 Dubey JP: Toxoplasmosis in cats. Feline Pract 16:12-26, Dubey JP, Beattie CP: Toxoplasmosis of Animals and Man, pp CRC Press, Boca Raton, FL, Dubey JP, Carpenter JL: Neonatal toxoplasmosis in littermatecats. JAmVetMedAssoc203: , Dubey JP, Carpenter JL: Histologically confirmed clinical toxoplasmosisincats- 100 cases ( ). J Am Vet Med Assoc 203: , Dubey JP, Frenkel JK: Cyst-induced toxoplasmosis in cats. J Protozool 19: , Dubey JP, Frenkel JK Immunity to feline toxoplasmosis: modification by administration of corticosteroids. Vet Pathol 11: , Dubey JP, Johnstone I: Fatal neonatal toxoplasmosis in cats. J Am Anim Hosp Assoc 1k , Dubey JP, Johnstone I, Menrath VH, Topper MJ: Congenital toxoplasmosis in Abyssinian cats. Vet Parasitol 32~ , Dubey JP, Lappin MR, Thulliez P: Diagnosis of induced toxoplasmosis in neonatal cats. J Am Vet Med Assoc 207: , Dubey JP, Schlafer DH, Urban JF Jr, Lindsay DS: Lesions in fetal pigs with transplacentally-induced toxoplasmosis. Vet Pathol 27: , Henriksen P, Dietz HH, Henriksen SA: Fatal toxoplasmosis in five cats. Vet Parasitol 55: 15-20, Hirth RS, Nielsen SW: Pathology of feline toxoplasmosis. J Small Anim Pract 10: , Lindsay DS, Dubey JP: Immunohistochemical diagnosis of Neospora caninum in tissue sections. Am J Vet Res 50: , 1989 Request reprints from Dr. J. P. Dubey, Parasite Biology and Epidemiology Laboratory, Building 1040, BARC-East, US Department of Agriculture, Beltsville, MD (USA).
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