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Neospora Caninum and Hammondia Heydorni Are Two Coccidian Parasites with Found N 66 Opinion TRENDS in Parasitology Vol.18 No.2 February 2002 from the infective larval stage of Toxocara canis 22 Hunter, S.J. et al. (1999) The isolation of extracellular CuZn superoxide dismutases in by an expressed sequence tag strategy. Infect. differentially expressed cDNA clones from the the human parasitic nematode Onchocerca Immun. 67, 4771–4779 filarial nematode Brugia pahangi. Parasitology. volvulus. Mol. Biochem. Parasitol. 88, 20 Gregory, W.F. et al. (2000) The abundant larval 119, 189–198 187–202 transcript-1 and 2 genes of Brugia malayi encode 23 Au, X. et al. (1995) Brugia malayi: Differential 25 Selkirk, M.E. et al. (2001) Acetylcholinesterase stage-specific candidate vaccine antigens for susceptibility to and metabolism of hydrogen secretion by nematodes. In Parasitic filariasis. Infect. Immun. 68, 4174–4179 peroxide in adults and microfilariae. Exp. Nematodes: Molecular Biology, Biochemistry 21 Blaxter, M.L. et al. (1996) Genes expressed in Parasitol. 80, 530–540 and Immunology (Kennedy, M.W. and Brugia malayi infective third stage larvae. Mol. 24 Henkle-Dührsen, K. et al. (1997) Localization Harnett, W., eds), pp. 211–228, CABI Biochem. Parasitol. 77, 77–93 and functional analysis of the cytosolic and Publishing N. caninum and T.gondii Neospora caninum In 1984, Bjerkås et al. [5] first discovered a toxoplasmosis-like disease of Norwegian dogs that had no demonstrable antibodies to T. gondii. In 1988, and Hammondia Dubey et al. [6] described in detail a similar neurological disease of dogs in the USA, distinguished the parasite from T. gondii based on antigenic and heydorni are separate ultrastructural differences, and proposed the genus Neospora with N. caninum as the type species. Isolation and in vitro cultivation of N. caninum [7,8] species led to the development of serological and immunohistochemical tests [7,9], which confirmed that N. caninum is distinct from T. gondii. Today, J.P.Dubey, Dolores E. Hill, David S. Lindsay, N. caninum is recognized as a major cause of abortion Mark C. Jenkins, Arvid Uggla and in cattle worldwide [10,11]. In 1998, Marsh et al. [12] described another species Clarence A. Speer of Neospora, N. hughesi, as a cause of neurological disease in horses. The full life cycle of N. caninum was not discovered until 1998, when McAllister et al. [13] Neospora caninum and Hammondia heydorni are two coccidian parasites with found N. caninum oocysts in the feces of dogs fed morphologically similar oocysts in canine feces. It was recently proposed that tissues from experimentally infected mice. When they are one species. In this paper, we review the biology and morphology of these oocysts were inoculated into immunodeficient these parasites and present evidence that N. caninum and H. heydorni are mice [13] and normal gerbils [14], neosporosis was separate species. induced. Recently, Lindsay et al.[15] found that dogs fed tissues of mice infected with cloned N. caninum Toxoplasma gondii, Neospora caninum, Hammondia tachyzoites produced N. caninum oocysts, thus hammondi and Hammondia heydorni are closely confirming the dog as a definitive host of N. caninum. related coccidian parasites with similarly sized oocysts Since the discovery of N. caninum in 1988, >500 [1]. Cats (felids) are definitive hosts for T. gondii and papers have been published on this parasite in H. hammondi, and dogs (canids) are definitive hosts peer-reviewed scientific journals. The description of for N. caninum and H. heydorni. However, these numerous morphological, biological, antigenic and species have important biological and ultrastructural molecular differences [10,16–20] between N. caninum differences. Whereas T. gondii causes a disseminated and T. gondii leave no doubt that they are separate infection in humans and animals, and N. caninum is species, and this issue will not be discussed further in one of the most important causes of abortion in cattle, this communication. H. hammondi and H. heydorni are not known to be of clinical significance. Recently, Mehlhorn and Heydorn N. caninum and H. heydorni [2] and Heydorn and Mehlhorn [3] questioned the Much of the confusion regarding the identity of validity of the genera Hammondia and Neospora and N. caninum and H. heydorni results from incomplete argued that, in this group, only T. gondii and T. heydorni knowledge of the details of the life cycles of these are valid. In a rebuttal paper, Frenkel and Dubey [4] parasites. Mugridge et al. [21] and Mehlhorn and stressed the ultrastructural, biological and genetic Heydorn [2] tabulated differences and similarities differences between T. gondii and H. hammondi. between the two species. They gave reasons why Hammondia and Toxoplasma Heydorn [22] discovered that dogs fed naturally should be deemed separate genera, and why T. gondii infected beef shed sporulated oocysts (which should be regarded as a species distinct from were of a species of Sarcocystis) and small, H. hammondi. This discussion is not repeated here; unsporulated oocysts (which he then called instead, this article discusses the relationships Isospora bigemina). Isospora bigemina was first between N. caninum, T. gondii and H. heydorni. named Coccidium bigeminum in 1891, based on the http://parasites.trends.com 1471-4922/02/$ – see front matter © 2002 Elsevier Science Ltd. All rights reserved. PII: S1471-4922(01)02172-9 Opinion TRENDS in Parasitology Vol.18 No.2 February 2002 67 (a) (b) to dogs, coyotes and foxes have been identified as definitive hosts for H. heydorni [1]. Tissue cyst stage of H. heydorni The tissue cyst stage of H. heydorni has not been conclusively identified in naturally infected animals. The only report describing tissue cysts of H. heydorni is by Matsui [26], who examined tissues of guinea pigs inoculated with oocysts. He found two tissue cysts in the brain of an animal killed 77 days post-infection, and in a brain smear of a guinea pig killed 189 days post-infection. The tissue cysts were 10.7 × 10.6 µm in the histological section and 13.0 × 12.1 µm in the tissue smear [26]. They had thin walls and were indistinguishable from T. gondii tissue cysts. Guinea pigs are generally resistant to T. gondii, but latent infections have been reported. Furthermore, it cannot be completely ruled out that the cysts were young Fig. 1. A comparison of tachyzoites of (a) Neospora caninum and (b) Hammondia heydorni in cell N. caninum tissue cysts. Thus, the nature of the tissue culture. Both organisms are located in parasitophorous vacuoles (P). In both figures, tachyzoites have cysts described by Matsui remains in doubt. divided and remain attached to each other at one end. Tachyzoites of N. caninum have many more micronemes (M), few amylopectin granules (A) and no vacuole (V) compared with tachyzoites of H. heydorni. Abbreviations: C, conoid; D, dense granules; N, nucleus; R, rhoptry. Differences between tachyzoites of N. caninum and H. heydorni finding of oocysts with two sporocysts in the intestinal Neospora caninum has been cultivated in vitro in mucosa of a dog [1,23]. Oocysts morphologically different cell lines [8,16]. It can be maintained resembling those of I. bigemina were later reported continuously in cell culture by sub-inoculation of new J.P.Dubey∗ from several other hosts including cats and humans, cultures. The NC-1 isolate of N. caninum isolated in Dolores E. Hill and dogs and cats were found to shed sporulated 1988 [7] has been cultivated in this way for >12 years. Mark C. Jenkins oocysts of several species of Sarcocystis [23]. Because Unlike N. caninum, there is only one report of cell Parasite Biology, the name I. bigemina was first used for the parasite culture of H. heydorni [27]induced with sporozoites. Epidemiology and Systematics Laboratory, developing in the lamina propria of the dog (which is The parasite grew in several cell lines, but died out Animal and Natural now Sarcocystis bigemina), a new name, after a few asexual cycles and could not be transferred Resources Institute, Isospora heydorni, was proposed by Tadros and to other cell lines by inoculation with merozoites [27]. Agriculture Research Service, United States Laarman [24] for the canine I. bigemina developing in Although H. heydorni and N. caninum both multiply Dept of Agriculture, the intestinal surface epithelium. Dubey and Fayer in cell culture by endodyogeny, the organisms are Building 1001, Beltsville, [25] described I. bigemina-like oocysts in the feces, ultrastructurally distinct [28] (Fig. 1). A noticeable MD 20705-2350, USA. and asexual and sexual stages in the intestine, of a difference is the presence of a large vacuole near the ∗e-mail: jdubey@ anri.barc.usda.gov naturally infected dog. Dubey [23] proposed that the conoidal end in H. heydorni (Fig. 1), a feature that is canine I. bigemina to be transferred to the genus absent in N. caninum. Furthermore, H. heydorni has David S. Lindsay Center for Molecular Hammondia because of its biology, including an several amylopectin granules that are absent or rare Medicine and Infectious obligatory two-host life cycle; Isospora species in N. caninum tachyzoites, and N. caninum has more Diseases, Dept of generally have a fecal–oral one-host life cycle. micronemes than H. heydorni (Fig. 1a,b). In addition, Biomedical Sciences and Dogs fed H. heydorni oocysts became infected, N. caninum can be transmitted to a variety of hosts by Pathobiology, Virginia-Maryland but did not shed oocysts, and the organism could subcutaneous inoculation of infected tissues, whereas Regional College of not be transmitted to mice by subcutaneous H. heydorni has an obligatory two-host cycle. Veterinary Medicine, inoculation of infected tissues. Thus, the name Following the single report of successful in vitro Virginia Tech, 1410 Prices Fork Road, Blacksburg, became Hammondia heydorni [23,24]. Because cultivation of H. heydorni [27], the oocysts used in this VA 24061-0342, USA. it is now impossible to determine the true culture were morphologically described by Blagburn identity of I.
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