Parasitic Diseases

Parelaphostrongylosis and Elaphostrongylosis

Infection with the meningeal worm P. tenuis is subclinical in its only definitive host, the whitetail deer. In aberrant hosts, including goats, sheep, camelids, and other wild cer- vids, clinical signs of focal myelitis or encephalomyelitis are produced.

In Norway, a similar clinical syndrome of cerebrospinal nematodiasis in goats has been identified. The condition results from infection with Elaphostrongylus rangiferi, the elaphostrongyloid nematode of reindeer (Handeland and Sparboe 1991). Though not completely elucidated, the nat­ural history of this disease in goats appears quite similar to parelaphostrongylosis as seen in North America.

A similar clinical syndrome has been reported in goats in Switzerland associated with Elaphostrongylus cervi, the elaphostrongyloid nematode of several species of Eurasian deer, including red deer, roe deer, maral deer, and sika deer.

Etiology and Pathogenesis

P. tenuis is a hair-like nematode in the family Protostrongylidae. The definitive host is the whitetail deer, Odocoileus virginianus. The parasite has an indirect life cycle that involves terrestrial slugs and snails as intermedi­ate hosts. Adult worms reside in the subdural spaces and cranial venous sinuses of the CNS of deer. Eggs laid on the meninges hatch, enter the circulation, and localize in the lungs. Eggs laid in the venous sinuses are carried to the lungs and hatch there. In either case, larvae migrate up the airways, are swallowed, and passed in the deer's feces. They are subsequently ingested by gastropods, where they develop into infective larvae over a three- to four-week period. Infective larvae are released from snails and slugs when the gastropods are ingested by grazing mammals. In the deer, larvae penetrate the intestine and migrate to the spinal cord through the peritoneum, reaching the CNS within 10 days, where they mature in the dorsal horns of spinal gray matter for an additional 20-30 days.

When infective mollusks are ingested by goats and other aberrant hosts, migration to the spinal cord via the perito­neum also takes place over a 10-day period. However, beyond this point the normal life cycle goes awry. Maturation of larvae is erratic, and subsequent migrations through the spinal cord are random and unsuccessful in reaching the cranial venous sinuses. Randomly migrating larvae are responsible for the parenchymal destruction and inflammation that lead to clinical neurologic disease in aberrant hosts. The wide variety of neurologic abnormali­ties observed in clinical cases reflects the frequently multi­focal nature and diverse distribution of lesions in the spinal cord or brain. The goat is able to control P. tenuis infection in some cases, as recovery has been observed in experimen­tally challenged animals and in natural outbreaks. In kids experimentally infected orally with 200 or more larvae, severe colitis and peritonitis developed within 4-11 days of infection caused by larval migration through the intestinal wall (Anderson and Strelive 1969). The occurrence of peri­tonitis in naturally occurring goat cases has not yet been reported.

The life cycles of E. rangiferi and E. cervi are similar to that of P. tenuis, involving gastropods as intermediate hosts. The life cycle of these parasites is completed without dam­age to the natural hosts, except in the case of reindeer (Rangifer tarandus ssp.) (Davidson et al. 2020). In goats, as with P. tenuis infection, the life cycle is not completed and aberrant migration through the spinal cord and brain results in clinical disease. Experimental challenges of goats with E. cervi did not produce patent infections (Scandrett and Gajadhar 2002)

Epidemiology

Cerebrospinal nematodiasis caused by P. tenuis is restricted to North America, reflecting the geographic distribution of the definitive host.

The deer favors forested areas as natural habitat, but commonly grazes pastures and croplands adjacent to woodlands. Goats grazing pastures where deer feed are at increased risk of exposure to P. tenuis. Although the inter­mediate gastropod hosts are terrestrial, there appears to be increased risk of exposure to snails and slugs in low-lying, wet, and poorly drained fields and pastures.

Cool, moist weather is believed to enhance the infectivity of the first-stage larvae passed by deer and to promote the activity of intermediate host snails. Pastures in the north­ern half of North America are most dangerous during late summer to early fall and most cases of clinical disease in goats are seen in fall and early winter. In Texas, clinical dis­ease has been reported in April (Guthery et al. 1979). Additional reports of P. tenuis in goats have come from Minnesota, Michigan, and New York (Mayhew et al. 1976; O'Brien et al. 1986; Kopcha et al. 1989). It can be presumed that grazing goats are at risk wherever whitetail deer are found.

In experimental infection of goat kids, clinical signs of neurologic disease appeared between 11 and 52 days after introduction of infective larvae into the peritoneum (Anderson and Strelive 1972). In natural infection, onset of clinical signs has been noted as late as nine weeks after removal of goats from pasture. Morbidity rates in affected herds have been reported from 10 to 27%, with mortality rates as high as 65%.

E. rangiferi is naturally found in reindeer in Scandinavia, and the disease has been well documented in goats in Norway (Handeland and Sparboe 1991). The occurrence of cerebrospinal elaphostrongylosis in goats and sheep in northern Norway is associated with high mean tempera­tures during the preceding summers and the presence of reindeer in pastures (Handeland and Slettbakk 1995).

E. cervi is naturally found in Europe and western Asia in a number of native cervids, but was introduced into New Zealand through the importation of red deer (Mason et al. 1976). There are several well-documented case reports of cerebrospinal nematodiasis due to E. cervi from Switzerland (Pusterla et al. 1997, 1999, 2001).

Aberrant hosts such as the goat are most commonly exposed to these parasites by grazing on pastures that also have been grazed by infected wild ungulate hosts. Goats grazing on these contaminated pastures ingest gastropods that contain infective larvae. As this occurs most com­monly in summer and early fall, clinical cases of disease are seen most commonly in late fall and winter.

Clinical Findings

All breeds, sexes, and ages of goats can be affected. Animals usually have been on pasture within the past two months. Observation of deer on pasture can often be elicited in the history. Affected animals can have a variable history regarding duration of signs, ranging from a gradual pro­gression of lameness or paresis over several days to a sudden onset of recumbency since the previous day. Angora goats on range have been found dead, entangled in brush, presumably because of limb weakness and locomo­tor difficulties associated with spinal cord lesions.

The most common clinical presentations suggest involve­ment of the spinal cord. Signs include paresis or paralysis of one or more limbs, ataxia, postural reaction deficits, knuckling, toe dragging, abnormal gait, limb weakness, recumbency in a dog-sitting posture, or inability to rise.

Indications of brain involvement in affected goats include circling and blindness, separation from the flock, abnormal posture, and head tilt. Hypopyon has also been noted.

The duration and severity of clinical signs vary. Animals that remain ambulatory should be given at least one month to demonstrate if they will stabilize or recover. Animals unable to rise have a poorer prognosis.

Clinical Pathology and Necropsy

Analysis of CSF from affected animals frequently demon­strates a moderate increase in total protein and white blood cell counts, with eosinophils frequently noted. In one study of 14 cases, CSF protein concentration ranged from 29 to 360 mg/dL, with a median of 69.5 mg/dL. The white blood cell counts ranged from 0 to 1000/mm³, with a median of 54/mm³. Eosinophils were present in CSF in 57% of cases (Smith 1982). Hemograms are usually normal. The life cycle of P. tenuis is not completed in goats. Therefore, first- stage larvae are not found in goat feces.

No serologic tests are currently available commercially, but the potential for serologic diagnosis exists. In experi­mental infection of two goat kids, antibodies to P. tenuis were detectable in the serum and CSF using ELISA. Serum antibodies were detectable before, during, and after the onset of clinical signs and peaked at eight weeks post infec­tion. CSF antibodies peaked at five to eight weeks post infection (Dew et al. 1992).

There are no gross lesions associated with P.

Microscopically, lesions are usually confined to the spi­nal cord and brain stem. There are focal areas of malacia and necrosis, especially in white matter, with evidence of degenerating axons. Adjacent to malacic areas there is perivascular cuffing with lymphocytes, sometimes eosino­phils, and occasionally plasma cells. The degree of general inflammation is mild, although focal granuloma formation has been reported (Kopcha et al. 1989). Hemorrhage is sometimes observed, and a mononuclear or eosinophilic meningitis may occur. PCR is now being used to confirm the presence of P. tenuis DNA in spinal cord at necropsy in aberrant host species, including horses (Mittelman et al. 2017) and cattle (Mitchell et al. 2011), and there is one report of its application in goats (Dobey et al. 2014).

Diagnosis

No definitive antemortem diagnosis is currently possible. Presumptive diagnosis is based on a history of goats graz­ing where deer are found, a seasonal occurrence of neuro­logic disease in goats with diverse clinical signs, and the presence of eosinophils in CSF when found. Definitive diagnosis depends on identifying the parasite or its DNA in nervous tissue at time of necropsy.

Treatment

Currently, there is no proven effective therapy for P. tenuis or Elaphostrongylus spp. in goats and other aberrant hosts. Reports of successful therapy to date must be viewed cau­tiously, because no controlled studies have been reported and spontaneous recoveries are known to occur in untreated animals.

Diethylcarbamazine has been used at doses ranging from 40 to 100 mg/kg for one to three days, on the basis of its reported efficacy in treatment of cerebrospinal nematodia- sis caused by S. digitata in Asia. However, this filarial worm is not a member of the family Protostrongylidae and has a different pattern of anthelmintic susceptibility. Ivermectin also has been a focus of therapeutic interest. However, studies in whitetail deer indicate no effect against P. tenuis once the larvae have entered the CNS, although larvae are killed during the preceding migration period (Kocan 1985). A newer avermectin, moxidectin, has higher lipid solubil­ity and is more hydrophobic than other avermectins, and may therefore be better able to cross the blood-brain bar­rier to reach nematodes already present in the CNS. Benzimidazoles, notably fenbendazole, also are used empirically, though levamisole has shown no efficacy (Nagy 2004). Dexamethasone or other steroids may have some value in reducing inflammation in nervous tissue, although their effect on subsequent migratory or develop­mental activity of larvae is unknown. Non-steroidal anti­inflammatory drugs such as flunixin meglumine have also been used empirically.

Combination of multiple anthelmintics and anti­inflammatory drugs is commonly reported in the treat­ment of cerebrospinal nematodiasis, perhaps reflecting the uncertainty of what actually is known to be effective (Nagy 2004). For example, there is a report of treatment of goats for clinical E. cervi infections in 17 goats using flun­ixin meglumine at 1.1 mg/kg bw IM, and oral administra­tion of fenbendazole at 50 mg/kg and ivermectin at 200 gg/kg SC for five days (Pusterla et al. 1999). Eleven (64.7%) showed an immediate improvement in neuro­logic signs. Three of them had a complete recovery, while eight had some persistent ataxia. Six recumbent goats (35.3%) were killed because of a lack of response. It was concluded that the therapy was effective if neurologic deficits were not already severe when treatment was initiated.

In an incident of parelaphostrongylosis affecting five calves, the most severely affected calf was euthanized and the four remaining calves were treated with ivermectin at a dose of 0.2 mg/kg SC for five days, fenbendazole at 10 mg/ kg orally for five days, and dexamethasone at a dose of 0.05 mg/kg IM, with one dose on each of days 1 and 3. Three of the four calves responded rapidly to treatment and were asymptomatic two months later, while the fourth calf continued to show neurologic deficits (Mitchell et al. 2011).

In a recent case report, a 9-month-old Boer buck pre­sented for an acute onset of pelvic limb ataxia and CSF analysis revealed an eosinophilic pleocytosis (Breuer et al. 2019). On admission, the goat was treated empiri­cally with a single dose of flunixin meglumine at 2.2 mg/ kg bw IV for inflammation and a single dose of 1% iver­mectin at 0.2 mg/kg bw SC to treat the suspected cerebro­spinal nematodiasis. This was followed by initiation of a five-day course of oral high-dose fenbendazole at 50 mg/ kg bw q24h (every 24 hours). On the second day of hospi­talization, the buck was switched to meloxicam at 1 mg/ kg bw orally q24h, to avoid the potential long-term adverse effects of flunixin meglumine. The goat showed a notable return of pelvic limb function by the fifth day of hospitalization and five months later was ambulating normally.

Because goats have been known to recover spontane­ously from cerebrospinal nematodiasis, affected animals should be allowed time to show signs of improvement when the situation permits. Supportive care is extremely important during that period. Because animals may be recumbent from paresis or paralysis, ample dry bedding is necessary and periodic lifting or slinging may be appropri­ate. The prognosis is worse in animals showing signs of brain involvement such as circling.

Control

Control methods are currently limited to reducing deer access to livestock grazing areas and reducing exposure of goats to gastropods and infective larvae. Practical means of reducing deer access are constrained by regulatory limita­tions on deer hunting and the ability of deer to jump fences. Livestock guardian dogs may be very helpful if they drive the deer away. The benefits of dogs are more evident begin­ning a year after their introduction, presumably because of turnover in the mollusk population. It may be helpful to limit goat pasturing to fields without contiguous wood­lands and to pastures that are on high ground and well drained. When feasible, goats should be removed from pas­ture earlier in the grazing season, before the weather turns wet and cool. No other practical means of snail and slug control have been reported.

Based on knowledge of the life cycle of the parasite and the effectiveness of ivermectin against migrating larvae, control is theoretically possible by anthelmintic prophy­laxis every 10-16 days while goats are at pasture; this, how­ever, is costly and may be impractical. It would be useful to have larvicidal anthelmintics that can be administered regularly and inexpensively during grazing periods to pre­vent entry of ingested larvae into the CNS. Benzimidazoles effective against the larval stages of other Protostrongylidae such as Muellerius that are available as salt or feed addi­tives are potential candidates in non-lactating goats. Pyrantel tartrate has also been recommended for use in this manner because it is formulated to be fed on a daily basis (Rickard 1994), but anecdotally has not been effective in camelids. Empirically, ivermectin has been given to cattle on affected farms at a dose of 0.2 mg/kg SC every 30 days until after the first frost (Mitchell et al. 2011). However, the regular use of anthelmintics to control cerebrospinal nem- atodiasis could contribute negatively to the growing prob­lem of anthelmintic resistance in gastrointestinal nematodes, a far more common and costly problem, par­ticularly in small ruminants.

Setariasis

The filarial worm S. digitata is non-pathogenic in definitive ungulate hosts, but can produce a cerebrospinal nemato- diasis in goats, sheep, and other aberrant hosts in Asia. The disease is commonly referred to as lumbar paralysis or kumri. It is clinically similar to the conditions produced by P. tenuis, E. rangiferi, and E. cervi.

Etiology and Pathogenesis

S. digitata is a non-pathogenic parasite of the peritoneal cavity of cattle, buffalo, and zebu. It occurs only in Asia. There was some debate whether S. Iabiatopapillosa, found in the peritoneum of cattle, antelope, deer, and giraffe, was a separate or identical species, but phylogenetic analysis now indicates that the two species are distinct (Jayasinghe and Wijesundera 2003). The life cycle of these filarids is not completely understood, but is known to be indirect. Mosquitoes of various genera, including Anopheles, Aedes, and Armigeres spp., serve as the intermediate hosts.

In the definitive cattle host, adult worms live in the peri­toneal cavity and produce microfilaria that circulate in the bloodstream. Mosquitoes ingest the microfilaria along with blood during feeding. Within two weeks, these microfilaria mature into infective larvae and enter the salivary glands of the mosquito. During subsequent feedings, they are intro­duced into the bloodstream of new ungulate hosts. In the definitive host these larvae migrate to and mature to adults in the peritoneal cavity to complete the life cycle. In aber­rant hosts such as the goat, sheep, and horse, the microfi­laria migrate to the CNS, sometimes the eye, and occasionally the fetus of pregnant animals, where they cause mechanical damage and an inflammatory reaction. Clinical signs usually develop one month after infection. The life cycle is rarely completed in aberrant hosts, and microfilaria are not detectable in the bloodstream.

Epidemiology

The disease was first suspected in imported goats in Japan in 1927, but its parasitic nature was not confirmed until much later. It has since been reported in goats in Japan, Korea, and Sri Lanka (Innes et al. 1952), India (Patnaik 1966), China (Wang et al. 1985), Taiwan (Fan et al. 1998), Saudi Arabia (Mahmoud et al. 2004), and Iran (Bazargani et al. 2008). The disease occurs as a seasonal epizootic; it is associated with increased numbers of mos­quitoes. In Japan, most cases are seen in August and September, in China, June through October, and in India, September through December, after the rains and before winter. Morbidity rates can be high, with as many as 30-40% of susceptible animals affected. There appears to be some natural immunity in local animals, with higher morbidity and mortality observed in imported goats. Keeping goats in close proximity to cattle populations infected with S. digitata predisposes to infection.

The goat is considered an aberrant host for S. digitata. Microfilaria are introduced into the goat via the bites of mosquitoes and the parasite generally is considered not to reach maturity in this host. However, patent infections in Saudi goats have now been reported, with adult worms detected in 5 of 48 goats examined at a veterinary diagnostic laboratory. These animals did not show clinical signs of disease, but had male and female S. digitata in the abdominal cavities, mostly on the omentum as well as microfilaria in the blood (El-Azazy and Ahmed 1999). It was speculated that the genetic constitution of this local Saudi goat breed may be predisposed to the establishment of patent infection.

Clinical Findings

All ages, sexes, and breeds of goats may be affected. The appearance of clinical signs may be acute or subacute, and mild to severe. Variable outcomes occur, including acute death, progressive worsening of neurologic signs, stabiliza­tion of neurologic deficits, and occasionally spontaneous recovery. Most typically, affected animals show evidence of spinal cord involvement with ataxia, lack of propriocep­tion, paresis, or paralysis. Any or all limbs may be affected, but most often hindlimbs are involved. Sensory deficits are minimal. Additional signs suggesting brain involvement include cranial nerve deficits, nystagmus, and circling. In most cases, animals remain mentally alert. Fever is not observed.

Clinical Pathology and Necropsy

As with other parasitic infections of the CNS, eosinophilia of the CSF can occur in caprine setariasis. Gross necropsy lesions are rarely identified, and diagnosis depends on thorough microscopic examination of the brain and spinal cord, concentrating especially on those areas that correlate with the clinical neurologic examination. In most cases only a single larva is involved, and rarely more than three. Microscopically, lesions are characterized by a focal mala- cia that can be identified in serial sections as the migratory tract or channel of the offending parasite. In adjacent areas there may be evidence of axonal degeneration, demyelina­tion, astrocytosis, and perivascular cuffing with mononu­clear cells and eosinophils. Hemorrhage is variable. Locating the actual offending larvae in histologic sections is uncommonly achieved.

Diagnosis

Antemortem diagnosis is presumptive based on the sea­sonal observation of epizootic neurologic disease, charac­terized principally by locomotor dysfunction in countries where setariasis occurs. Definitive diagnosis depends on identification of the parasitic larvae in the CNS of affected animals at time of necropsy.

Treatment

The filaricide diethylcarbamazine can be effective in goats and sheep when animals are treated early in the course of disease. Early signs may represent meningeal irritation or radiculitis caused by the parasite before its entry into the brain or spinal cord, and the parasite may still be suscepti­ble to anthelmintic therapy at this stage.

Diethylcarbamazine, suspended in water, is given orally once at a dose of 100 mg/kg bw, or at a dose of 40-60 mg/kg daily for one to six days (Shoho 1952, 1954). Once the para­site has crossed the meninges, response to therapy is poor. Avermectins may also show efficacy against some species of microfilaria in other livestock species, but reports on the use of ivermectins specifically against S. digitata in goats are lacking.

Control

To reduce the incidence of setariasis in aberrant hosts such as goats, the parasite should be controlled in the normal host, cattle, particularly at the beginning of the mosquito season. Because the infection is subclinical in cattle, rou­tine treatment of cattle by farmers may be difficult to effect. When possible, goats should be housed separately from cattle. The use of diethylcarbamazine in sheep at an oral dose of 40 mg/kg given one time every three weeks before and during the mosquito season appeared to reduce the number of clinical cases observed in the field compared with untreated controls (Shoho 1954). Reduction of mos­quito populations could also reduce the transmission of the parasite from cattle to goats.

Strongyloidiasis

St. papillosus is a nematode parasite of ruminants normally associated with gastrointestinal parasitism. It is discussed in more detail in Chapter 10 in the section on nematode gastroenteritis. However, there were several instances of mortality occurring in young kids and lambs in Namibia, in which St. papillosus was identified as the cause and in which signs of neurologic disease were noted in addition to the characteristic signs of gastrointestinal parasitism. Neurologic signs included gnashing of teeth, aimless wandering, and persistent head pressing against objects. The presence of neurologic signs was so unexpected that experimental challenge studies were undertaken to better characterize the clinical syndrome and the underlying pathology seen in the field and to confirm St. papillosus as the etiology (Pienaar et al. 1999).

In the experimental studies, some but not all challenged goats showed signs of CNS involvement in their clinical presentation. Signs included gnashing of teeth, wide-based stance, ataxia, stupor, nystagmus, and head pressing (“pushing syndrome”). At necropsy, no gross lesions were seen in the CNS, but histopathologic lesions were found in the brain and spinal cord. These lesions were characterized as status spongiosus with marked vacuolation of the white matter, but also in the gray matter and in some nuclei. The most common sites for lesions were the roof nuclear area of the cerebellum, corpus striatum, thalamus, and mid­brain and medulla; less common sites included the cere­brum, granular layer of the cerebellum, spinal cord, and optic tracts. The severity of lesions was closely correlated with the presence of neurologic signs in challenged goats.

To date, neurologic signs associated with St. papillosus have not been reported elsewhere, either under field condi­tions or in experimental challenge studies. It is not clear why neurologic disease was noted in these Boer cross goats in Namibia. Possible explanations include the intensity of the challenge dose; variations in breed susceptibility; or the presence of other toxic, metabolic, or infectious causes that were not recognized in the field outbreaks or the experi­mental animals. Further documentation of the occurrence of neurologic disease associated with St. papillosus infec­tion is needed. When unexplained head pressing, ataxia, or gnashing of teeth is noted in goats, particularly if signs of gastrointestinal parasitism are present as well, then fecal samples should be checked for St. papillosus and goats that die should be necropsied with examination of the brain.

Coenurosis

Coenurosis, also known as gid, sturdy, or staggers, is a metacestodal infection of ungulates, especially sheep and goats. It primarily causes a focal encephalopathy.

Etiology and Pathogenesis

The metacestode involved in this disease is the intermedi­ate stage of the tapeworm of carnivores, Taenia multiceps, formerly known as Multiceps multiceps. The metacestode is identified in sheep as Coenurus cerebralis and in goats as either C. cerebralis or, historically, as C. gaigeri. It was thought that a separate species existed because cysts are frequently located outside the CNS in the goat. However, current evidence indicates that the difference lies with the host, not the parasite (Oryan et al. 2015).

T. multiceps is a large intestinal tapeworm of dogs, foxes, coyotes, and jackals. Eggs or gravid tapeworm segments are passed in the feces of the host, contaminate herbage, and are ingested by grazing ruminants. Embryos are released after ingestion and penetrate the small intestine, enter portal vessels, and are distributed widely throughout the tissues via the circulation. In sheep, only larvae that reach the CNS develop into metacestodes; all others die.

In goats, metacestode development occurs primarily in the CNS, but frequently in the skeletal musculature, the heart, and other organs. The muscular form of the disease is discussed in Chapter 4. Cysts also have been found in mesenteric lymph nodes, within the eye (Islam et al. 2006), behind the eye causing exophthalmia (Sharma et al. 2017), and subcutaneously, causing swellings on the face (Abbas et al. 2017) and elsewhere on the body (Saidul Islam et al. 2016).

There is a period of migration through nervous tissue that may result in clinical signs of acute meningoen­cephalitis if large numbers of larvae are present. In most cases, however, this migratory phase is subclinical. After migration, the stationary phase of metacestode matura­tion lasts from two to seven months. The mature metaces­todes are cystic structures up to 7 cm in diameter, transparent, thin-walled, and filled with clear fluid. They contain up to several hundred scolices that are visible as white plaques on the clear cyst wall in excised cysts. The majority of mature cysts are located superficially in the parietal or frontal region of the cerebral cortex, but loca­tion is variable throughout the CNS and musculature. The life cycle of the tapeworm is completed when carnivores ingest mature cysts while feeding on tissues of infected ruminants.

During the early growth of cysts, irritation of adjacent nervous tissue occurs and may be reflected in some cases by early excitatory signs. As the metacestode enlarges, pressure on adjacent tissues increases, and neuronal death occurs, leading to signs of neurologic deficit. The pressure that develops is considerable and is reflected in a high inci­dence of papilledema and rarefaction of cranial bone adja­cent to superficial cysts. CSF pressure also can be markedly elevated. The clinical signs that develop reflect the location of the cyst or cysts present.

Epidemiology

T. multiceps is present in carnivores worldwide, but coen­urosis is not common in goats in most countries. There are numerous clinical reports originating from the Indian sub­continent: 32 caprine cases were recorded in one year at a single veterinary institution in India (Saikia et al. 1987). A slaughterhouse survey in Bangladesh demonstrated a prev­alence range of 1.9-13.3% for cerebral coenurosis (Ahamed and Ali 1972), while a slaughterhouse survey in Iran indi­cated a prevalence of 0.09% of goats with one or multiple visible swellings on the different muscles and visceral organs confirmed as coenurosis (Kheirandish et al. 2012). Caprine coenurosis is sporadic in Europe and Africa (Harwood 1986), though the local impact can be severe. In a report from northern Tanzania, where the disease is locally known as “ormilo,” a questionnaire survey con­ducted in four villages indicated that the 12-month period prevalence of clinically affected sheep and goats ranged from 11 to 34% in each village, representing about 25% of the total small ruminant population present in those vil­lages (Hughes et al. 2019). The disease is rare or absent in goats and sheep in North America, Australia, and New Zealand. The status of coenurosis in Africa and Asia has been reviewed (Sharma and Chauhan, 2006).

Inadequate stray dog control, ingestion by dogs of offal from slaughter, lack of tapeworm control in owned and stray dogs, and grazing of herbage contaminated with eggs or gravid tapeworm segments from dog feces contribute to the occurrence of coenurosis in small ruminants. Where goats and sheep are found together, goats may be less fre­quently affected, probably because they are primarily browsers rather than grazers.

The disease is more commonly reported in female goats, but this may reflect their disproportionately large presence in goat herds rather than a sex-based predilection to dis­ease. Given the slow course of development of cysts and the onset of clinical signs, the disease is rarely recognized in animals under 6 months of age. Morbidity rates are low, but mortality rates are high in untreated cases. The disease is infrequently reported in humans, with most documented cases reported from Africa. Humans become infected by consumption of embryonated eggs shed by the definitive canid hosts. Goats, and sheep, are not directly involved in the zoonotic aspect of the disease.

Clinical Findings

Because of the prolonged development phase for coenuro­sis, cases may be seen at any time of the year. Affected ani­mals may have a history of ill-defined, low-grade neurologic abnormalities for one month or longer. Animals with the neurologic form of the disease may show a variety of signs. A careful neurologic examination should be conducted in order to localize the site of the cyst responsible for the clini­cal signs present, though it is possible that multiple cysts may be present in a given case.

The clinical presentation is variable, but it has been sug­gested that there are three phases of development (Saikia et al. 1987). In the first stage, animals may be depressed and show intermittent periods of abnormal head carriage, especially head tilt. There may be short, intermittent con­vulsions or intermittent circling. This phase lasts for 4-8 days and may be overlooked. In the second phase, which usually begins 8-16 days after onset of signs, signs become more consistent. The most common findings are head tilt, unilateral blindness, circling, and loss of balance with a staggering gait. Some animals may show determined forward walking with the head held high and a hypermet­ric gait followed by head pressing against obstacles instead of circling. Other signs include grinding of the teeth, sali­vation, exophthalmos, nystagmus, and irregular rumen contractions. The third or terminal phase usually begins 12-25 days after onset of signs. Animals become recum­bent, exhibit extensor rigidity, and paddle frequently with the hindlimbs. These stages overlap considerably and the clinical course is frequently one month or longer.

Papilledema and hemorrhage of the optic papilla are common in coenurosis cases, so a fundic examination should be performed. In addition, firm, digital palpation of the head frequently identifies dissymmetry or softened areas of skull, suggestive of underlying superficial cysts. Digital pressure on such spots may exacerbate clinical signs. Cysts deep in the parenchyma are not associated with bony changes.

A case of coenurosis was reported in a 7-month-old goat in Mongolia, which presented with bilateral flaccid paraly­sis of the hindlimbs. The goat had been at pasture and had actually been grazing for some time, dragging its hindlimbs behind it. At necropsy, the goat had a metacestode cyst occupying the lumbar vertebral canal, extending along three vertebrae. Impingement of the spinal cord by this space-occupying cyst accounted for the clinical signs (Welchman and Bekh-Ochir 2006).

Clinical Pathology and Necropsy

Total protein, cell counts, and pressure are often elevated in the CSF. Mean total protein in affected goats has been reported at 80.3 mg/dL, mean cell counts at 85/mm³, and mean pressure at 262.4 mm water. Eosinophils and degen­erative cells may be common on cytologic examination (Sharma and Tyagi 1975).

Radiographs can reveal metacestode-associated rarefac­tion of the skull when bone softening has not yet reached the point of detection by digital palpation. Ultrasound has also been reported as effective in identifying intracranial coenuris cysts (Athar et al. 2018), as has MRI (Manunta et al. 2012) and CT (Gazioglu et al. 2017).

At necropsy, cysts ranging in size from 1 to 7 cm in diam­eter can be identified in predilection sites such as brain, spinal cord, and skeletal muscle.

Diagnosis

Though the clinical course is prolonged, it may not always be recognized as such, and animals may present with acute onset of circling, falling, or head pressing. The differential diagnosis should include listeriosis, CAE, PEM, brain abscesses, sinusitis, cerebral hematomas or tumors, cere­brospinal nematodiasis, and rabies. The nose bot, O. ovis, may occasionally penetrate the frontal sinuses and produce a clinical syndrome known as false gid, because the signs are similar to those seen in coenurosis.

Treatment

None of the anthelmintic therapies used for elimination of the metacestode in clinically affected animals has been shown to provide consistently reliable results in goats (Sharma and Chauhan 2006). Praziquantel administered orally at dose of 50 mg/kg bw has given unreliable results in sheep. The drug was more reliably effective at a higher dose of 100 mg/kg bw given orally (Verster and Tustin 1990). As praziquantel is expensive, alternate therapies such as albendazole and fenbendazole have been explored. The efficacy of albendazole has been studied in experimentally infected goats. Treatment with albendazole at an oral dose of 10 mg/kg bw daily for three days at two months post infection resulted in a high level of non-viable cysts identi­fied at necropsy, while a similar treatment given at five months post infection did not (Afonso et al. 2014). However, most of the cysts assessed were outside the brain, so the effect on cerebral coenurosis was unclear. In a different study involving experimentally infected sheep, groups of sheep were treated with different treatment regimes after the onset of clinical signs consistent with cerebral coenuro­sis, and all groups showed clinical improvement along with evidence at necropsy that cerebral cysts had degenerated and were non-viable. The most effective treatment regime was albendazole at a dose of 25 mg/kg daily for six days, and the next most effective was a combination of praziqu­antel and fenbendazole, each given at a dose of 50 mg/kg daily for six days, which produced better outcomes than either of the two drugs given separately (Ghazaei 2007).

When bone softening is pronounced so the site of the cyst is obvious, aspiration of cyst contents is accomplished via an aseptic needle passed through the softened or perfo­rated bone. Afterward, a mild antiseptic is introduced, such as 0.1% acriflavine solution. Surgical treatment is possible when bone is still firm, but the outcome of surgery is enhanced if the precise location of the lesions can first be identified by radiography or other imaging techniques. Though a number of surgical techniques have been reported, a recent review provides details on presurgical preparation, anesthesia, and the surgery itself, which involves trephination (Scott 2012). The surgical approach is based upon the neurologic findings. For a cerebral cyst, a trephine site 1-2 cm lateral to the midline and immediately rostral to the coronal (parietofrontal) suture line is recom­mended. For a cerebellar cyst, the recommended trephine site is midline between the nuchal line and the suture line between the occipital and parietal bones. A 1 cm diameter bone core should be removed and then the dura mater incised, at which point the increased intracranial pressure caused by the cyst will force brain tissue into the trephine hole. An 18-gauge IV catheter connected to a 20 mL syringe is then used to drain the cyst and withdraw a portion of the cyst wall to the trephine hole, where it can be grasped with forceps and the entire cyst wall and protoscolices carefully removed. In two separate studies, 90% of 30 goats and 87.5% of 16 goats survived and showed good recovery after surgery (Sharma and Tyagi 1975; Ahmed and Haque 1975). Either general or local anesthesia has been used.

Control

Control methods involve reducing stray dog populations, ensuring strict hygiene at slaughterhouses, restricting the feeding of small ruminant carcasses and offal to dogs, and ensuring regular anthelmintic use in dogs kept with live­stock for control of mature tapeworms. There are no vac­cines commercially available, though research efforts suggest that vaccination could be useful in control of this disease.

Tick Paralysis

Ascending paralysis and death can result from the feeding activity of certain species of ticks on domestic animals, including goats. The disease has been reported sporadically in goats in parts of Europe, the Middle East, and South America. It is considered a major constraint on small rumi­nant production in parts of South Africa, where the disease is known as Karoo tick paralysis.

Etiology

At least 59 species of hard ticks in the Ixodidae family and 14 species of soft ticks of the Argasidae family can produce tick paralysis in mammals and birds. These 73 species rep­resent ten different genera, but the majority come from four genera, namely Argas, which target mainly avian hosts, and Ixodes, Dermacentor, and Rhipicephalus, which target mainly mammalian hosts, including livestock spe­cies and humans (Pienaar et al. 2018). In goats, the condi­tion has long been associated primarily with Ixodes rubicundus in South Africa, and then later with Rhipicephalus punctatus as well (Stampa 1959; Fourie et al. 1991). In Israel, Crete, Turkey, and Bulgaria, Ix. rici- nus causes the disease in goats (Hadani et al. 1971; Trifonov 1975). In 1983, tick paralysis was reported for the first time in Brazil, associated with Amblyomma cajenn- ense (Serra Freire 1983). In Australia, Ixodes holocyclus causes tick paralysis in goats as well as sheep, cattle, horses, pigs, dogs, cats, and humans (Hall-Mendelin et al. 2011).

Most reports of tick paralysis involve adult ticks rather than larvae or nymphs, and when such ticks have a two- or three-year life cycle, disease outbreaks may be seen only every second or third year. In many cases, the immature tick stages show different host feeding preferences. For example, immature forms of Ix. rubicundus are found pri­marily on hares and shrews. This is not always the case, however; in Brazil, there is experimental evidence that lar­val and nymphal stages of Am. cajennense may also pro­duce the disease; and in Australia, all feeding stages of the tick Ix. holocyclus may produce paralysis, though it is most often associated with feeding by adult females (Bowman 2014). Development of disease appears to be less associated with the number of ticks actually feeding than with the stage of engorgement of the ticks present on the host.

Epidemiology

The incidence of tick paralysis is tied to the life cycle and ecology of the offending ticks and conditioned by livestock management and grazing practices. For example, in Australia, the distribution of Ix. holocyclus is mainly restricted to the eastern coastal strip of Queensland and New South Wales, which is the territory inhabited by its principal hosts, the short-nosed and long-nosed bandicoots (Bowman 2014). In Israel, the disease is seen only every third year between December and February when adult ticks are active, and only in the more temperate, inland regions of the country. It usually occurs only in flocks or herds grazing on the more densely vegetated, northern slopes of hills and not the barer, southern slopes (Hadani et al. 1971). In South Africa, Karoo tick paralysis is also seen primarily in the winter months (March to August), on the moister, hillier portions of the Karooveld, and tick den­sities vary with different vegetation types (Stampa 1959). The Rhipicephalus-associated disease is seen in September through November and again in February in South Africa. In Brazil, naturally occurring cases were observed between June and December.

Morbidity and mortality can be high in epizootics of tick paralysis. For example, 14 of 51 (27%) South African Angora kids younger than 1 month of age developed paral­ysis while grazing over a two-week period in September, and 71% of these died even after ticks were removed (Fourie et al. 1988).

In North America, the disease is reported in cattle, sheep, and New World camelids in western Canada and the west­ern United States, in association with Dermacentor and Argas spp. ticks (Schofield and Saunders 1992; Cebra et al. 1996), so veterinarians in North America should at least consider the disease as a possibility in goats. There are anecdotal reports in the United States of paralyzed goats with tick infestations in the axilla that recover when the ticks are removed.

Pathogenesis

In general, it appears that each of the various species of ticks responsible for paralysis produces a neurotoxic pro­tein in its salivary glands that is introduced into the host animal during active feeding, particularly when the tick reaches a certain stage of engorgement, usually after sev­eral days of feeding. The toxin produced by Ix. holocyclus, holocyclotoxin, is known to inhibit acetylcholine release at the neuromuscular junction. Other toxins produced in other species of ticks may have other mechanisms of action and these have been reviewed (Pienaar et al. 2018). In all cases there is a resulting flaccid paralysis that first involves the limbs and may progress to involve the diaphragm, with animals dying of respiratory compromise.

Clinical Findings

The disease is seen most often in grazing animals infested with ticks. Ticks are most common around the head and neck, especially in the ears, and around the tail head, but the entire body should be inspected. Affected goats show evidence of lower motor neuron involvement, including muscular weakness of the limbs, unsteady gait, knuckling, ataxia, and hypoesthesia. There is no fever, animals often remain bright and alert, and they continue to eat. Frequently the hindlimbs are affected first, but all four limbs may be affected simultaneously, especially in Karoo tick paralysis. As the disease progresses the animal becomes laterally recumbent due to flaccid paralysis. In terminal cases, death is caused by respiratory paralysis or aspiration pneumonia. The clinical course is usually one to three days. If ticks are identified and removed early in the course of disease, before recumbency, many but not all animals recover completely within 24 hours.

Clinical Pathology and Necropsy

There are no clinical pathologic or necropsy findings that support the diagnosis of tick paralysis, save for the pres­ence of offending species of ticks.

Diagnosis

Diagnosis is presumptive on the basis of identification of ticks known to cause tick paralysis on affected goats under circumstances of likely occurrence. The differential diag­noses for progressive limb paralysis in goats include rabies, enzootic ataxia or swayback, CAE, botulism, cerebrospinal nematodiasis, vertebral trauma or abscesses, and congeni­tal spinal abnormalities. IM injections affecting the sciatic nerves, nutritional muscular dystrophy, and skeletal trauma must also be considered in sudden loss of mobility in the hindlimbs.

Treatment and Control

While antitoxin or hyperimmune serum against specific tick toxins may be available in some countries for use in humans and companion animals, in general the treatment in livestock consists of removal of feeding ticks and provi­sion of supportive care. As more than one tick may be involved, the entire animal should be examined carefully for the presence of ticks to ensure that all are removed. Careful removal of offending ticks with their mouthparts intact can usually be expected to result in a diminution of clinical signs and is an essential element of treatment. However, at least in humans, it has been noted that removal of the offending tick has sometimes led to an exacerbation of signs. In those cases, it is presumed that disruption of the feeding site by extraction of the tick resulted in the release of additional toxin that was bound to cells or tissue at the feeding site (Hall-Mendelin et al. 2011). Therefore, patients should be observed carefully in the hours follow­ing tick removal. Similarly, advanced cases need to be observed for evidence of respiratory distress associated with possible paralysis of the diaphragm and, when feasi­ble and necessary, provided with ventilatory support. Feed and water should be withheld from affected animals to minimize the risk of aspiration pneumonia in case of paralysis involving the oral and pharyngeal cavities and fluid therapy provided as needed. Recumbent animals should be well bedded and repositioned regularly. The use of atropine is contraindicated in animals with tick paraly­sis (Bowman 2014).

Knowledge of the ecology of offending ticks may be used to restrict grazing in high-risk areas during seasons of known adult tick activity. When this is not possible, tick control with the use of topical acaricides is indicated dur­ing the high-risk seasons.