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Neosporosis

Preferred citation: Anipedia, www.anipedia.org: JAW Coetzer and P Oberem (Directors) In: Infectious Diseases of Livestock, JAW Coetzer, GR Thomson,
NJ Maclachlan and M-L Penrith (Editors). JP Dubey, Neosporosis, 2018.
Neosporosis

Neosporosis

Previous authors: J P DUBEY

Current authors:
J P DUBEY - Senior scientist, M.V.Sc., PhD.,DSc, Animal Parasitic Diseases Laboratory, U.S.Department of Agriculture, Building 1001, Beltsville Agricultural Research Center, 10300 Baltimore Avenue, Beltsville, Maryland, 20705, USA

Introduction

Neospora caninum is a relatively recently recognized protozoan parasite that occurs in a wide range of animals species. Until 1988 it was misdiagnosed as Toxoplasma gondii because of structural and biological similarities.52 The disease was first described in dogs by Bjerkås et al.25 in Norway in 1984 but the parasite was not named at that time. Dubey and his co-workers in 198852 described the parasite and proposed a new genus, Neospora, with N. caninum as the type species. In vitro isolation of the parasite in cell culture inoculated with tissues of paralysed dogs contributed to a better understanding of its biology.57 In 1988, neosporosis was recognized as a cause of abortion in cattle163 and in the subsequent three years infections were induced experimentally in most species of livestock.63 The genome of N. caninum was sequenced in 2012,146 suggesting that N. caninum and T. gondii diverged from their common ancestor approximately 28 million years ago. A book authored by Dubey58 devoted solely to neosporosis listed more than 2000 references: much of the information in this chapter is extracted from that book and only selected references are cited here.58

Aetiology and life cycle

Neospora caninum is a coccidian parasite closely related to T. gondii (Figure 1). Dogs (both domestic and feral or wild, Canis familiaris), coyote (Canis latrans), and gray wolf (Canis lupus) are   intermediate and definitive hosts.61, 78, 104, 122  Cattle, sheep, white- tailed deer, European bison and water buffalo are  intermediate hosts, as proven by isolation of  viable parasites.58 Clinical neosporosis has been reported in numerous hosts including alpaca (Vicugna pacos), captive antelope (Tragelaphus imberbis), Axis deer (Axis axis), black-tailed deer (Oedocoileus hemionus columbianus), cattle, dog, Eld’s deer (Panolia eldii siamensis), goat, llama (Lama glama), Parma wallaby (Macropus parma), Pine marten (Martes martes), red fox (Vulpes vulpes), white rhinoceros (Ceratotherium simum), and sheep.58, 97-101, 171 Antibodies and DNA to N. caninum without evidence of disease have been detected in many mammalian and avian species.58

Only an asexual cycle occurs in the intermediate hosts that consists of tachyzoites and tissue cysts. Both tachyzoites and tissue cysts are microscopic in size and intracellular. Tachyzoites are ovoid, lunate or globular and measure 3–7 μm × 1–5 μm, depending on the stage of division (Figures 2 and 3). Tachyzoites are found in the cytoplasm in many cells including neurons, macrophages, fibroblasts, vascular endothelial cells, myocytes, hepatocytes and dermal cells. Tachyzoites are usually located in a parasitophorous vacuole in the host cell. Ultrastructurally,  the tachyzoites of N. caninum resembles the tachyzoites of T. gondii  except that the rhoptries in N. caninum are electron-dense and more numerous, with some extending the entire length of the parasite, whereas in T. gondii, they are electron-lucent, few, and located anterior to the nucleus.58

Figure 1  Life cycle of Neospora caninum

Figure 2  Tachyzoites of Neospora caninum

  1. Impression smear. Note organisms dividing (arrowheads) into two are bigger than single tachyzoites (arrows). Giemsa stain
  2. Tachyzoites in parasitophorous vacuoles in cell culture. Giemsa stain
  3. Sections of the skin of a dog. Note suppurative inflammation associated with two groups of tachyzoites (arrows) and individual tachyzoites (arrowheads). Tachyzoites in sections are much smaller than those in smears. Haematoxylin and eosin stain

Figure 3 Transmission electron micrograph of dividing tachyzoites in two parasitophorous vacuoles (Pv). The Pv have many tubular networks. Arrows point to the conoidal end of daughter tachyzoites forming inside the mother tachyzoites. Note electron-dense rhoptries (R), micronemes (Mn), microtubules (Mt) or subpellicullar tubules, conoid (C), host cell nucleus (Hcn). Cardiopulmonary artery endothelial cell culture. (Courtesy of Dr C.A. Speer, Montana State University, Bozeman, Montana, USA)

Tissue cysts are often round to oval in shape (Figure 4). Most tissue cysts studied were from the brain and spinal cord, the majority from naturally infected dogs. Tissue cysts in the brain are round to oval and up to 107 µm in diameter. The cyst wall is 0.5 to 4.0 µm thick, both in live, unstained preparations and in histological sections.51 The cysts in myocytes are elongated and may be up to 100 µm long, and have a thin cyst wall.71, 141 Histologically tissue cysts are rare in other organs or tissues of naturally infected animals. The tissue cyst wall is smooth and up to 4 µm thick, presumably depending on the duration of the infection. Septa are absent in the cysts and there is no secondary cyst wall (Figure 5). The tissue cyst wall is elastic, argyrophilic, has a wavy contour, and stains negative with Periodic-acid Schiff (PAS). Bradyzoites are slender and contain the same organelles as tachyzoites except that there are fewer rhoptries and more PAS-positive (amylopectin) granules in the bradyzoites. Tissue cysts may degenerate and cause an inflammatory reaction by the host (Figure 6).

Oocysts in freshly passed faeces are unsporulated  and  sporulate outside the host within 24 hours. Sporulated oocysts contain two sporocysts each with four sporozoites. Neospora caninum oocysts are 10-11 µm in diameter (Figure 7) and are morphologically indistinguishable from Hammondia heydorni found in canine faeces and T. gondii and Hammondia hammondi in cat faeces.51, 153 Sporulated oocysts are slightly bigger in size than the unsporulated oocysts, namely 11.7 x 11.3 mm (10.6-12.4 x 10.6-12.0) with a length-to-width ratio of 1.04. The oocyst wall is colourless, and 0.6-0.8 mm thick. The developmental stages (ie. schizonts, gamonts) in  the intestines of dogs  preceding the formation of oocysts are unknown. Oocysts have been found in faeces of naturally infected dogs9, 18, 20, 21, 153 and gray wolf.61

Figure 4  Tissue cysts (arrows) of Neospora caninum

  1. Section of a calf brain. Note small tissue cyst with thin cyst wall. Haematoxylin and eosin stain
  2. Intraneuronal tissue cyst in a section of the spinal cord of a calf. Haematoxylin and eosin stain
  3. Intraneuronal tissue cyst in a section of spinal cord of a calf. Note silver-positive cyst wall. Silver stain
  4. Tissue cyst in a brain squash of an experimentally infected mouse. Note thick cyst wall (opposing arrowheads). Unstained

Figure 5 Transmission electron micrograph of dividing tachyzoites in two parasitophorous vacuoles (Pv). The Pv have many tubular networks. Arrows point to conoidal end of daughter tachyzoites forming inside the mother tachyzoites. Note electron-dense rhoptries (R), micronemes (Mn), microtubules (Mt) or subpellicullar tubules, conoid (C), host cell nucleus (Hcn). Cardiopulmonary artery endothelial cell culture. (Courtesy of Dr C.A. Speer, Montana State University, Bozeman, Montana, USA)

Figure 6 Degenerated tissue cyst (arrow) in the brain of a goat. Note glial cells and mononuclear cells surrounding the tissue cyst. Haematoxylin and eosin stain

Figure 7 Oocysts of Neospora caninum

  1. = Unsporulated
  2. = Sporulated

Note two sporocysts (arrows) and sporozoites (arrowheads). Unstained

Susceptible hosts can become infected by ingesting food and water contaminated with N. caninum oocysts from canid faeces. Transplacental transmission occurs when tachyzoites from the dam cross the placenta during the second week after infection. Neospora tachyzoites initially multiply in the maternal part of the placenta and then spread to the foetal part, and eventually to foetal tissues. Transplacental transmission is common in cattle. The two terms “exogenous transplacental transmission” and “endogenous transplacental transmission” have been proposed to describe more precisely the origin of the transplacental infection of the foetus.165 “Exogenous transplacental transmission” occurs after a primary, oocyst-derived infection of a pregnant dam, while “endogenous transplacental transmission” occurs in a persistently infected dam after reactivation (recrudescence) of the infection during pregnancy.

Venereal or lactogenic transmission may occur rarely.58, 133, 167

 Neospora caninum is efficiently transmitted vertically in cattle ; horizontal transmission is necessary to introduce new infections in a herd.5, 27, 48 It can be transmitted transplacentally also in naturally infected sheep, goats, deer and horses, and experimentally in several other species of animals.58 Transplacental infection can occur repeatedly in the same animal and through its progeny for several generations. The mechanisms of primary and repeat congenital transmission of infection are unknown.

Neosporosis in cattle

Neosporosis occurs in dairy and beef cattle worldwide.56, 58, 92, 138, 163, 169 It is a major cause of abortion in dairy cattle including in the USA,2-4, 13, 38, 163 New Zealand,164 Argentina,34, 127 The Netherlands,174, 176, 177 UK countries, and Australia.33, 132

Abortion is the only clinical sign observed in cattle. Cows of all ages may abort from three months of gestation to term. Most Neospora-induced abortions occur at five to six months of gestation.3, 174 Foetuses may die in utero and be resorbed, mummified or aborted, or may be stillborn, born alive but diseased, or born clinically normal but chronically infected. Isolated or sporadic abortions or abortion storms (epidemic) may occur in herds58, 121, 130, 163, 174, 178 and may occur all year round.3 Cows with N. caninum antibodies (seropositive) are more likely to abort than seronegative cows.126, 139, 174 Congenital deformities are rare:50 exophthalmia or an asymmetrical appearance of the eyes may occur.

Neospora caninum-infected calves may be born underweight, unable to rise and with neurological signs such as ataxia. Hind limbs and/or forelimbs may be flexed or hyperextended and neurological examination may reveal decreased patellar reflexes and loss of conscious proprioception.5, 16, 17, 32, 49, 53, 56, 62, 65, 84, 107, 125, 141 Neosporosis rarely occurs  in calves older than two weeks old.

Neosporosis in goats and sheep

Historically, congenital neosporosis was first reported in a lamb in 197589 before the discovery of N. caninum and retrospectively confirmed as neosporosis in 1990.65 The affected lamb was born weak, partially ataxic, and died at one week of age. The most prominent findings were in the spinal cord that showed myelitis, unilateral reduction of grey matter in the ventral horn and focal cavitation, associated with intact and degenerated N. caninum tissue cysts; tachyzoites were not seen.

Neospora caninum infections are less common in goats than in cattle and sheep.58 Neosporosis-associated abortion and neonatal mortality have been reported from Brazil,42, 124, 129, 168 Costa Rica,66 Italy,72 and USA.15 The encephalomyelitis is characterized by necrosis and glial nodules with numerous tissue cysts (predominantly smaller than 20 µm in diameter); only a few tachyzoites were seen. Teratology of the brain including hydrocephalus, hypoplasia of the cerebellum, and porencephaly have also been described.

Although antibodies to N. caninum in sheep have been reported from many countries, the economic, clinical, and epidemiologic importance of N. caninum infection in sheep remains uncertain.58 In one of the largest investigations of protozoal abortion in England, there was no evidence of congenital N. caninum infection in sheep.135 In that investigation, antibodies to N. caninum were not found in pleural fluid of 179 foetuses and 141 lambs. Neospora caninum was also not identified in tissues from 281 foetuses/lambs by immunohistochemistry (IHC). In contrast, N. caninum was identified in some sheep flocks in Italy, New Zealand and Spain.79, 81, 94, 118, 128

Occasionally, N. caninum can cause abortion,7, 90, 94, 95, 105, 118, 128, 152, 166 birth of weak lambs,65, 89 neonatal mortality81 and even clinical signs in adult sheep.24

Neosporosis in dogs

Serological surveys indicate a worldwide prevalence.58 There are numerous reports of clinical neosporosis in dogs.97, 98 Clinical neosporosis is most common in young, very old, and immunosuppressed dogs.11, 96 The most severe signs are seen in transplacentally infected puppies that develop ascending rear limb paresis and paralysis, with atrophy and rigid contracture of the muscles of the pelvic limbs (Figure 8). Initial clinical signs often start in the first weeks of life but most are diagnosed when they are two months old. Infection occurs most likely prenatally. Apart from the brain, N caninum has a tropism for the lumbosacral spinal nerve roots, resulting in meningoencephalomyelitis and polyradiculoneuritis and consequently neurogenic muscle atrophy. Although stillbirths and neonatal deaths have been reported in littermates of pups with neosporosis, the youngest pups with neosporosis were eight and 12 days old.143

Figure 8 Neospora caninum infected dog with hind limb paralysis. The first isolate of N. caninum was obtained from the neural tissues of this dog in 1988. Immunohistochemical staining, however, is required to differentiate the parasite from T. gondii because tachyzoites of the two parasites are indistinguishable from each other by light microscopy. Cerebrospinal fluid should be examined for tachyzoites in cases manifesting hind limb paralysis

Adult dogs may suffer from non-generalized neosporosis and may develop a wider range of manifestations, including encephalitis or meningoencephalomyelitis. Paraparesis is the most common neurological sign, but seizures, abnormal behaviour, and vestibular dysfunction may also occur.43 Signs of myositis include stiff gait, weakness, and pain or atrophy of skeletal muscles. Almost any other organ can be involved, including the lungs, liver, eyes, and heart. Dermatitis is another common presentation of neosporosis in dogs.31, 49, 52, 64, 76, 106, 108, 111, 115, 123, 140, 142, 162 Lesions may ulcerate with a purulent discharge. Most of these cases were in aged dogs or those that are immunosuppressed, but pups can also be affected. Severe hepatitis was reported in five dogs.39, 52, 77, 93, 98

Clindamycin, sulfadiazine, and pyrimethamine alone or in combination with other drugs have been administered to treat canine neosporosis.49, 54, 64, 71, 119 In adult dogs with acute paralysis from myositis, dysfunction is often more amenable to early treatment.

Subclinically infected bitches can transmit the parasite to their foetuses, and successive litters from the same bitch may be born infected.12, 49, 55, 63 There are no drugs that can eliminate tissue cysts. Thus, prophylactic treatment of bitches to prevent transplacental infection is not beneficial.

Neosporosis in horses

Unlike other species, neosporosis in horses would seem also to be caused by another species of Neospora, N. hughesi.117 To date, N. hughesi has been reported only from horses. Morphologically, there are minor differences between N. hughesi and N. caninum, and these species are distinguished primarily by molecular characterization.58 Antigenically, N. caninum  cross-reacts with N. hughesi and most serological surveys in horses used N. caninum as antigen.

Clinical neosporosis has been reported in seven horses, all from the USA.36, 44, 67, 68, 82, 88, 113, 116, 117 and one horse from Canada.36, 44, 68, 82, 88, 116, 117, 172  The first case was described in 1985 in a two-months aborted foetus. Only lung tissue was available from this case and numerous N. caninum tachyzoites were observed in the lesions.68 More recently, N. caninum infection was diagnosed by PCR in an aborted foetus in France.144

Neonatal neosporosis was diagnosed in a one-month-old Quarter horse filly in Wisconsin.113 She had circled her dam since birth and frequently tripped over obstacles. If separated from her dam she could not find her way back. Encephalitis associated with tissue cysts was revealed on histopathological examination.

An unusual case of visceral neosporosis has been reported in a 10-year-old Appaloosa mare with a history of weight loss and anaemia. Lesions associated with N. caninum tachyzoites were confined to the intestines and mesenteric lymph nodes. This is the first reported case of Neospora-associated enteritis in any animal species.82

Neosporosis has been diagnosed in an aged Pinto mare suffering from a pituitary adenoma with a history of hind limb paralysis, bizarre behaviour and masticatory difficulty.44 Lesions were present in the central nervous system, peripheral nerves and myocardium, and consisted of multifocal non-suppurative encephalomyelitis, polyradiculoneuritis and multifocal myocarditis. Neospora tachyzoites and tissue cysts were demonstrated by IHC examination in the brain, spinal cord and peripheral nerves. Neosporosis has  also been diagnosed in a 20-year-old horse with a pituitary tumour.88

All of the abovementioned cases were diagnosed on post-mortem examination. Ante-mortem diagnosis was reported in four equids from California, USA.73, 74 The diagnosis was based on clinical signs, serology, and improvement with treatment with ponazuril.

Neosporosis in other animal species

Although antibodies to N. caninum have been detected in water buffalo (Bubalus bubalis) sera, and viable parasites have been isolated from adult buffaloes,147 little information is available regarding clinical neosporosis in this species. Neospora caninum DNA was detected in one out of nine foetuses tested from buffaloes slaughtered at an abattoir in Brazil,37 indicating congenital transmission. Suggestive evidence of neonatal neosporosis in buffaloes has been reported from Italy.8, 83 In the first report, encephalitis and myocarditis were found in two of four foetuses examined histologically,83 but the parasite identity was not confirmed. Additional evidence was provided in the second report describing three foetuses from a seropositive buffalo herd that were examined at necropsy: N caninum DNA was detected in the brains of all three foetuses by pNc5 gene-based PCR , all three foetuses had encephalitis and myocarditis, but N. caninum was not demonstrable.8

There are no reports of clinical neosporosis in camels (Camelus spp.) but abortion has been reported in seven of 18 llama and 12 of 32 alpacas  from Peru.155, 156

White-tailed deer (Odocoileus virginianus ) are considered an important reservoir host of N. caninum in the USA.58-60 Antibodies to N. caninum were found in 162 of 400 (40,5 per cent) white-tailed deer in Illinois, USA.59 Fatal neosporosis has been diagnosed in a wild two-month-old female black-tailed deer  that was found dead in California.173 Lesions and N. caninum were present histologically in sections of the lungs, liver, and kidneys. Tachyzoites were most numerous in the lungs and were associated with interstitial pneumonia, while in the kidneys interstitial nephritis associated with parasites in tubular epithelium and lumens was noted. Tachyzoites within hepatocytes and Kupffer cells were found in the liver. Congenital neosporosis was diagnosed in captive deer, namely, the fawns of Axis deer from Argentina,19 an Eld’s deer in France,69 a fallow deer in Switzerland (Dama dama)158 and three lesser kudu (Tragelaphus imberbis) in Germany. Neosporosis was also been diagnosed in a full-term stillborn brown-antlered deer (Panolia eldii siamensis) from the Paris Zoo, France:66 N. caninum tissue cysts associated with non-suppurative encephalitis were present. Neosporosis was thought to be the main disease involved in the decline of the population of this endangered species in the zoo.

Fatal neosporosis was diagnosed in a white rhinoceros  in South Africa that died of massive myocardial necrosis171 (Figures 9 and 10), and another case in Thailand with severe hepatic necrosis.159 An aborted rhinoceros in Australia had extensive hepatic necrosis.150 Numerous tachyzoites were found in lesions in all three animals.

Figure 9 White rhinoceros: extensive myocarditis. H&E stained tissue section

Figure 10 White rhinoceros: immunohistochemical stained myocardial section

Diagnosis

In congenitally infected calves, precolostral serum collected from live or dead calves, as well as brain and spinal cord from dead calves or aborted foetuses are the specimens of choice. Ideally the entire aborted foetus should be submitted for diagnostic purposes but if this is not possible then samples from the brain, heart and liver should be collected in 10 per cent bufferedformalin for histopathological and immunohistochemical (IHC) examinations3, 112 (Figures 10 and 11), and body fluids or serum for serological evaluation.

Figure 11  Neospora caninum tachyzoites and a tissue cyst stained immunohistochemically with N. caninum antibody

  1. Numerous tachyzoites (arrowheads) in the skin of a dog
  2. A tissue cyst (arrow) in a neuron in a congenitally infected calf

Several serological tests can be used to detect N. caninum antibodies, including enzyme-linked immunosorbent assay (ELISA),  indirect fluorescent antibody test (IFAT), and  direct agglutination test.22, 26, 28, 41, 60, 102, 136, 137, 149, 154, 170, 174 Reagents for some of these tests are available commercially. An IgG avidity ELISA with the potential to discriminate between recent and chronic N. caninum infections in cattle has been developed.29, 30 The value and pitfalls of the different serological tests were recently reviewed.58

Levels of specific antibodies may persist for life but are influenced by age of the animal and stage of gestation.35 In cattle antibody levels fluctuate especially in pregnant dams and sometimes are below the detection limits.131 Recrudescence of chronic infections in cattle as a putative factor responsible for “endogenous transplacental transmission” has been substantiated by several studies that showed an increase of antibody levels during gestation.6, 41, 45, 75, 79, 85, 131, 145, 148, 161 The observation that a rise in antibody levels usually occurs in the second half of gestation79, 85, 131 is suggestive of recrudescence of infection in these cows.

Most cows that delivered a N. caninum-infected foetus or calf had antibodies against N. caninum at the time of abortion47, 134, 160, 174 or after calving.5, 46 Consequently, a negative serological test result for the dam makes it unlikely that N. caninum was the cause of abortion, stillbirth or neonatal mortality. In cases of abortion antibody levels as determined by two different ELISAs were higher in aborting than in non-aborting dams at risk.1, 60, 70, 80, 91, 103, 114, 120, 121, 145, 151, 154, 161, 169, 175, 179

Some of the commercial ELISAs have been modified for assessment of antibody levels in individual bovine milk samples or bulk milk samples.58

For the IFAT a titre 1:20060 or 1:64041 has been considered indicative of N. caninum infection in adult cattle, whereas much lower values of 1:25 or 1:80 have been selected as cut-off values for samples from bovine foetuses14 due to  reduced foetal immunocompetence, especially in bovine foetuses younger than six months.176, 177

Although N. caninum infection can cause lesions in several organs, foetal brain is  most consistently affected,3, 13, 58  characterized by  multifocal non-suppurative encephalitis.13 (Figures 12 and 13)  Scattered inflammatory foci are also common in the liver,174 heart, tongue and diaphragm  and are noticeable even in autolysed foetuses. Usually only a few tachyzoites can be detected in the inflammatory foci. Lesions in the cotyledons consist of non-suppurative focal necrosis and occasional foci of mineralization. Rarely, tachyzoites are demonstrable in trophoblasts.23, 157

Figure 12 Foetal bovine brain infected with Neospora caninum. Note a central necrotic focus with glial cells and mononuclear cells at the periphery. Haematoxylin and eosin stain

Figure 13 Section of the spinal cord of a calf congenitally infected with N. caninum. Note glial proliferation, perivascular inflammation and three tissue cysts (arrows). Immunohistochemical stain with N. caninum antibody

Although a presumptive diagnosis can be made by examination of haematoxylin and eosin (HE) stained tissue sections, IHC is necessary to detect the few N. caninum present in autolysed tissues, as these are often not visible in haematoxylin and eosin (HE) stained sections.

Isolation of Neospora in cell culture is rarely possible because most organisms in bovine foetuses die when the host cells become autolysed.40

Several polymerase chain reaction (PCR) methods are available for the detection of N. caninum DNA.58

Control

Prevention of contamination of feed and water with oocysts and not feeding raw meat/tissues to canids are important in the  prevention and control of neosporosis.

There are no drugs that can eliminate tissue cysts: thus treatment of dams to prevent congenital transmission is not possible.

Different control measures including embryo transfer from infected cows to uninfected donors,10, 109 artificial insemination1, 114 and test-and-cull86, 87, 110 have been suggested to reduce the economic losses related to  transplacental transmission in infected cattle herds but none seems practical.

References

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