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A Review of Neospora Caninum and Neospora-Like Infections in Animals

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A Review of Neospora Caninum and Neospora-Like Infections in Animals J. Protozool. Res., 2. 40-52 (1992) Copyright © 1992 , Research Center for Protozoan Molecular Immunology A Review of Neospora caninum and Neospora-like Infections in Animals J. P. DUBEY Zoonotic Diseases Laboratory, Livestock and Poultry Sciences Institute, Agricultural Research Service, U. S. Department of Agriculture, BARC-East, Beltsville, Maryland 20705-2350, U. S. A. Received 27 January 1992/ Accepted 15 March 1992 Key words: Neospora caninum, neosporosis, tachyzoites, tissue cysts, paralysis, abortion ABSTRACT: Neospora caninum is a recently recognized protozoan parasite of animals. Until 1988, it was misdiagnosed as Toxoplasma gondii. Neospora caninum or Neospora-like parasites cause paralysis and death in dogs and neonatal mortality and abortion in cattle, sheep, goats and horses. Its life cycle is not known. Tachyzoites and tissue cysts are the only asexual stages known and the carnivorous definitive host is not known. Transplacental transmission is the only known natural route of infection. INTRODUCTION AND HISTORY Neospora caninum is a recently recognized protozoon of dogs and other animals. Until 1988, it was misdiagnosed as Toxoplasma gondii. Neosporosis is not a new disease because in retrospective studies N. caninum was found in dogs in the United States that died in 1957 and 1958 (Dubey et al., 1988a; Dubey et al., 1990e). Historically, a neosporosis-like disease was first reported by Bjerkas et al. (1984). They identified a cyst-forming protozoon in a litter of six Boxer dogs in Norway. Five of these dogs developed neurologic disorders two to six months after birth. Toxoplasma gondii-like parasites were found in lesions in brain and muscles. However, T. gondii antibodies were not found in the sera of the dogs, nor was the parasite from dogs infective to mice. Dubey et al. (1988a) found a similar parasite in ten dogs in the United States, distinguished it from T. gondii, and named the parasite N. caninum. Dubey et al. (1988b) recovered live N. caninum in cell cultures and mice inoculated with tissues from naturally infected dogs and they induced 40 NEOSPOROSIS IN ANIMALS neosporosis in dogs experimentally. The development of an immunohistochemical test to specifically stain N. caninum in formalin-fixed tissues using anti-N. caninum serum raised in rabbits made it possible to diagnose Neospora infections in animals (Lindsay and Dubey, 1989a). Bjerkas and Dubey (1992) compared structure and antigenicity of the parasites in fixed tissues from dogs from Norway and U. S. A. and concluded that the parasite originally reported from Norwegian dogs was N. caninum or closely related to it. In this review the N. caninum-like parasites from livestock are considered Neospora although N. caninum has not been yet isolated and characterized from livestock. STRUCTURE AND LIFE CYCLE The life cycle is unknown but the close similarities of the organism to T. gondii suggest that the parasite is a coccidian with a carnivore as the definitive host. Tachyzoites and tissue cysts are the only known stages. Tachyzoites are ovoid, lunate or globular 3 to 7 x 1 to 5 µm, depending on the stage of division (Figs. 1, 2). They divide into two zoites by endodyogeny. In infected animals, tachyzoites are found in neural cells (axons, Schwann cells, neurons, ependymal cells, retinal cells, astrocytes), macrophages, fibroblasts, vascular endothelial cells, myocytes, renal tubular epithelial cells, hepatocytes and other cells of the body (Cummings et al., 1988; Dubey et al., 1988a; Bjerkas and Presthus, 1989; Dubey and Lindsay, 1989b; Speer and Dubey, 1989). Host cells may contain as many as 100 tachyzoites. Tachyzoites are located within the host cell cytoplasm with or without a parasitophorous vacuole (PV). Few, many or no intravacular tubules may be present in the PV (Fig. 2). Why some tachyzoites are in a PV and others are without a PV is unknown. Neospora caninum tachyzoites have organelles typically found in T. gondii tachyzoites. Tachyzoites have a three layered plasmalemma, 22 subpellicular microtubules, two apical rings, a conoid, a polar ring, one to three mitochondria, up to 150 micronemes, eight to twelve rhoptries anterior to the nucleus and four to six rhoptries posterior to the nucleus, a Golgi complex, rough and smooth endoplasmic reticulum, a nucleus and a nucleolus (Bjerkas and Presthus, 1988; Speer and Dubey, 1989). Some of the micronemes may be perpendicular to the inner parasite membrane. The rhoptries contain solid electron dense material and are two to four times thicker than the diameter of the micronemes (Fig. 2). The descrepancy in the number of rhoptries reported to be up to 30 by Bjerkas and Presthus (1989) and up to 18 by Speer and Dubey (1989) may be due to difficulty in distinguishing rhoptries from dense granules (Bjerkas and Dubey, 1992). Micropores have not been seen in tachyzoites in animals (Speer and Dubey, 1989; Bjerkas and Presthus, 1989) but were found in tachyzoites grown in cell cultures (Speer and Dubey, 1989). Tissue cysts are often round to oval, up to 107 µm long and are found only in neural tissues (brain, spinal cord and retina). The cyst wall is smooth and up to 4 µm thick, depending upon how long the infection has existed (Figs. 3, 4, 5). In most tissue cysts the cyst wall is 1 to 2 µm thick. The cyst wall contains branched tubule-like structures (Bjerkas and Presthus, 1988). Septa are absent and there is no secondary cyst wall. 41 NEOSPOROSIS IN ANIMALS Figures 1-5 Photographs of Neospora caninum. Figure 1.Tachyzoites (arrowheads) in section of liver of an experimentally infected rat. Note dividing tachyzoites (arrow) are larger in size than nondividing tachyzoites. H&E stain. x 750. Figure 2. Transmission electron micrograph of tachyzoites. Note six rhoptries (arrowheads), nucleus (N), a conoid (C), and parasitophorous vacuole (PV). x23,810. Figure 3. Tissue cyst in mouse brain 13 months after experimental infection. Unstained x 750. Note thick cystwall (opposing arrowheads). Figure 4. Tissue cyst in a neuron in spinal cord of a naturally infected bovine calf. Note thick cyst wall (arrowhead). The host cell nucleus is on left. H&E stain. x 750. Figure 5. Tissue cyst in the spinal cord of a bovine calf. Avidin-biotin complex immunohistochemcial reaction with anti-W. caninum serum. x 750. 42 NEOSPOROSIS IN ANIMALS Bradyzoites are slender (6 to 8 x 1 to 1.8 µm) and contain the same organelles as are found in tachyzoites except that there are fewer rhoptries in bradyzoites and more PAS-positive (amylopectin) granules in the bradyzoites. The cyst wall stains variably with PAS and is argyrophilic. Tubular vesicular structures are present in between bradyzoites and bradyzoites may contain micropores (Bjerkas and Presthus, 1989). Bjerkas and Presthus (1989) found micropores in bradyzoites in tissue cysts from the Norwegian dogs whereas micropores were not seen in bradyzoites from dogs in U.S.A. However, it must be emphasized that bradyzoites from only one well fixed tissue cyst were examined by Speer and Dubey (1989). Fixation and the age of tissue cysts might also affect structure of organelles. These fine points can only be resolved when tissue cysts can be produced in large number in experimentally infected animals. Neospora or a Neospora-like parasite has been found in dogs, cattle, sheep, horses and goats in nature and the parasite can be transmitted to dogs, cats, mice, rats, gerbils, cattle and sheep experimentally (Dubey, 1990; Cudden et al., 1992). The only natural mode of infection identified so far is congenital (Dubey and Lindsay, 1989b, c). Transplacental infection was induced experimentally in dogs, cats, sheep, mice, and cattle (Dubey and Lindsay, 1989b, c; 1990a; Cole et al., 1991; Dubey et al., 1992b). Transplacental infection can occur repeatedly in the same animal. Up to three litters of congenitally infected pups were born from the same bitch (Bjerkas et al., 1984; Dubey et al., 1988b; Dubey et al., 1990e). Neospora infection in a cat before pregnancy led to congenital infection in a kitten (Dubey and Lindsay, 1989c). Neospora caninum tachyzoites were found in placenta and the uterus (Dubey and Lindsay, I989c). In experimental animals N. caninum is infective by the subcutaneous, intraperitoneal, intramuscular and oral routes. Bradyzoites in tissue cysts are resistant to acidic-pepsin solution indicating that carnivorism may be a part of the life cycle of N. caninum (Lindsay and Dubey, 1990c). Oocysts were not detected in feces of experimentally infected dogs and cats (Dubey et al., 1988b; Dubey and Lindsay, 1989a, b, c; Cudden et al., 1992). Neospora caninum tissue cysts can survive up to 14 days at 4OC but were rendered noninfective at –20OC for 1 day (Lindsay et al., 1991, 1992). CULTIVAT ION Neospora caninum was initially cultivated in vitro in bovine monocytes (BM) and bovine cardio-pulmonary arterial (CPA) endothelial cells (Lindsay and Dubey, 1989b). Since that time N. caninum has been grown in Madin-Darby bovine kidney, fetal mouse brain and several other well established cell lines (Cole et al., 1990). More organisms are produced in BM than in CPA cells. Only tachyzoites have been identified in cultivated cells. Organisms from cell cultures are infective to animals (Dubey et al., 1988b; Lindsay and Dubey, 1989c, 1990c). Neospora caninum does not produce infection consistently in normal immunocompetent mice and rats. One way to infect rodents with N. caninum experimentally is to give 2 injections of 2 to 4 mg of 43 NEOSPOROSIS IN ANIMALS methylprednisolone acetate on seven days before and on the 0 day of the inoculation with ten or more N. caninum tachyzoites. Varying degrees of acute to chronic infection can be induced by varying the dose of N. caninum and corticosteroids given. Pneumonia and encephalomyelitis are the predominant signs of neosporosis in mice whereas rats develop hepatitis primarily (Lindsay and Dubey, 1989c, 1990b, c).
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