Approach to the Neurologic Camelid: Case-Based Signs, Diagnostic Findings & Treatment Plans
Claire E. Whitehead, BVM&S, MS, DACVIM, MRCVS
Meningeal worm is a relatively common condition in camelids in the Eastern United States. Nearly one third of cases presented at The Ohio State University between 1993 and 2003 for neurological signs were diagnosed with meningeal worm.1 It is caused by the nematode parasite Parelaphostrongylus tenuis whose definitive host is the white-tailed deer (Odocoileus virginianus). When camelids ingest infected molluscs (the intermediate host), aberrant migration in the CNS causes neurological signs. Experimental infection of 6 llamas with the parasite caused clinical signs of meningeal worm 45-53 days post-inoculation.2
The majority of meningeal worm cases are seen in the fall and winter (October to March), but can occur throughout the year, especially in wet weather years. Adults are affected more commonly than younger animals.
The characteristic clinical signs of meningeal worm include a wide-based hindlimb stance and hindlimb ataxia progressing to recumbency. Typically the forelimbs are unaffected or less affected until recumbency becomes prolonged and affected animals are usually bright and alert, maintaining good appetites. Since the spinal cord damage tends to be diffuse and random, the clinical presentation may vary and there may be forelimb involvement as well as lateralised signs. The onset of clinical signs may be gradual with affected animals presenting with only ataxia, or affected individuals may suddenly be found as "downers". Most affected camelids will exhibit an eosinophilic pleocytosis of the CSF as well as increased CSF protein concentration. Haematological and serum biochemistry findings are often normal unless there are secondary issues. For example, heat stress as this may exacerbate the clinical signs of meningeal worm, or dehydration. CK and AST are often elevated dependent on the duration of the condition and degree of recumbency. Generally, the prognosis is usually good while the affected animal is able to stand when assisted and continues to have a good appetite. Recumbent, inappetant animals usually have a poorer prognosis.
There is an atypical form of meningeal worm that occurs in a small proportion of cases. In these, parasitic migration extends into the brain. These animals often present with acute onset brain or vestibular signs including depression, seizures, circling, leaning, head tilt and slow PLRs. In this presentation, there is usually a rapid progression of clinical signs and the prognosis is guarded. This particular form of meningeal worm needs differentiating from other causes of intracranial disease such as listeriosis, brain abscess/tumor, otitis interna, encephalitis, meningitis, trauma and polioencephalomalacia. In a retrospective study at Ohio State, CSF collected from the lumbosacral space exhibited eosinophilic pleocytosis less reliably than when only spinal cord signs were demonstrated.1
A typical treatment program for meningeal worm includes fenbendazole at 50mg/kg PO for 5 days, NSAIDs (flunixin meglumine at 1mg/kg q12-24hrs), DMSO in severe cases, vitamin E (antioxidant), B vitamins, and fluid therapy as required. Physical therapy is also very important in aiding recovery. Recumbent animals should be well-bedded and encouraged to stand 3-4 times daily. If they cannot stand, their position should be changed regularly and passive extension/flexion of the limbs with muscle massage performed with the animal in lateral recumbency. Hydrotherapy or elevation in a sling may be required. Improvement usually occurs rapidly within a few days of beginning therapy and then more gradually: any neurological deficits remaining at 6 months post-treatment are likely to remain permanently.
The definitive diagnosis of meningeal worm is obtained at necropsy with characteristic histopathological findings associated with parasite migration. The lesions of parasite migration include randomly distributed axonal degeneration progressing to pannecrosis characterized by axon and axon sheath swelling, axon drop out, axonophagia and accumulation of gitter cells. This predominantly affects the white matter. Actual larvae are only found rarely.
This is a common condition in much of the United States except the Rocky Mountains. Llamas and alpacas are not well adapted to hot or humid climates. In summer in the US, the ambient temperature often exceeds 85°F and this is often accompanied by high humidity around 90%. The tendency of llama breeders to only barrel-clip rather than shear completely like alpaca breeders, together with a higher body volume: surface area ratio means that llamas seem to be more susceptible to heat stress. Camelids may cope with chronic heat stress for a while and the introduction of any new stressor such as transportation, change in weather, or meningeal worm may precipitate a sudden deterioration into clinical hyperthermia. Therefore, downer camelids presenting in hot weather must be thoroughly evaluated for presence of other disease conditions.
Clinically affected camelids will have elevated body temperatures (often >105°F, sometimes up to 108°F) if they have not been transported to a clinic. They are usually displaying signs of respiratory distress and this may be severe in terminal cases due to pulmonary edema. Tachycardia is a common finding. They will normally be unable to rise and often it is found that the forelimbs are weaker than the hindlimbs. Some affected animals may be depressed. Serum chemistry often reveals marked elevations in CK and AST, as well as hypoproteinemia (albumin leaks out of cells due to heat damage) despite dehydration (haemoconcentration). There may be severe electrolyte imbalances especially hypokalemia and metabolic acidosis.
Therapy clearly involves cooling. This may be achieved using ice packs in the axillary and inguinal areas, cold water hosing or bathing, and must include complete shearing if this has not already been done by the owner. Exercise caution if fluid therapy is required due to hypoalbuminemia since pulmonary oedema occurs readily in heat-stress cases due to cellular damage. Correction of acidosis and electrolyte imbalances should be the goal of fluid therapy while providing maintenance fluid needs until the animal is able to drink. NSAIDs may be beneficial for muscle soreness and as a general anti-inflammatory. Hydrotherapy using a float-tank, or slinging may be useful in order to allow damaged muscles to rest. Vitamin E may be given as an antioxidant therapy. If meningeal worm cannot be ruled out, then a 5 day course of fenbendazole at 50mg/kg may be initiated. In chronic cases, ongoing muscle damage may result in fibrosis of muscle tissue. Once the initial hyperthermia has been brought under control, there are often subsequent wide fluctuations in body temperature due to an upset thermoregulatory centre.
Cervical Vertebral Injuries
Spinal injuries in the cervical region are more common in camelids than injuries to other regions. The initial complaint with these cases is often of a "bump" on the neck or that the neck has a kink in it. These animals may be able to walk around normally for some time following an injury: owners may not even notice a defect until shearing. Other cases will present with varying degrees of neurologic deficits--ataxia, recumbency, low head carriage, Therefore, cases may be present acutely or chronically. In chronic injuries, the neurological symptoms are caused by progressive callus formation or fibroplasia of the longitudinal ligaments of the spinal column. Most injuries seem to be associated with fencing although traumatic events are often not observed. Fighting in males does not appear to be a risk factor. Affected animals will begin to show abnormal head/neck posture and may then develop neurological deficits, UMN to the HLs and UMN/LMN to the FLs. However, due to the cervical vertebral canal being quite wide, often neurologic signs will not develop in adults, provided that the defect is not severe or unstable, once the initial pain and inflammation have subsided. Note that muscle weakness can also cause a "kinky" neck appearance, especially in hypokalaemia and cachexia. In young animals, the effects of cervical spinal injuries are more severe as any defect will worsen as the animal grows producing more severe neurological defects.
Radiographs are required to determine the location and severity of the lesion and whether or not surgical intervention is appropriate. Articular facet fractures are commonly associated with sub/luxations. Myelography is not normally required. CSF analysis helps to rule out parasitic myelopathy and to support a traumatic etiology: protein elevation may be marked but may not be increased at all in some cases. There is no associated eosinophilic pleocytosis.
Non-surgical management involves stall rest and NSAIDs. This is appropriate when there are minimal to no neurological signs in an acute subluxation, and in adult animals. Surgical intervention is more often required in growing animals, and is normally a stabilisation procedure with the aim of producing fusion between neighboring cervical vertebrae. It is difficult to produce perfect re-alignment. Camelids do not tolerate neck casts well. Surgical options usually involve external fixation (halo-type or Type II). Several cases treated at The Ohio State University have subsequently developed secondary luxations at cervical joints either side of a fused joint.
The etiology of otitis interna/media may be an extension of otitis externa but is more often presumed to be a consequence of ascending infection up the Eustachian tubes in the absence of otitis externa. Spinous ear ticks have been associated with several cases in animals from Texas.
These cases normally present with a head tilt with or without facial nerve deficits (droopy ear, flaccid facial muscles--animals tend to pack food in the affected cheek, drop food or drool saliva--ptosis, inability to blink +/- exposure keratitis). Some animals may be ataxic or circling. Vestibular signs can be more severe including nystagmus, circling and leaning to one side. One case seen by the author also exhibited a head "tick" which was thought to be an exaggeration of the vestibular nystagmus: all signs resolved following surgical drainage and intensive medical management of an abscess that had ruptured from the tympanic bulla into the surrounding tissues. This animal had extensive bulla osteitis but had presented for acute onset of neurological signs with no prior history of ear pain/infection or head tilt.
CSF analysis is useful to rule out listeriosis or other causes of vestibular disease. About half of the cases seen in the retrospective study had increased CSF protein concentrations.1 Radiographs are useful if bony changes are present: however, soft tissue involvement can be extensive and only CT will show these adequately. Even impressive abscessation may not be palpable in these cases. We usually recommend CT for this reason and CT is also advised for guiding surgical treatment (lateral approach to a bulla osteotomy). Haemorrhage and permanent facial nerve deficits are potential complications of this surgery although prognosis is generally good. Various bacteria have been isolated from otitis cases including A pyogenes, Staphylococcus and Bacillus most frequently.
This is not a particularly common disease in camelids but it does occur. As in other small ruminants, the prognosis in camelids is guarded. Cases seen at The Ohio State University have been acute in onset with rapid progression of clinical signs including seizures. Most camelids present with lateralising signs--circling, ataxia, leaning to one side, nystagmus, but also recumbency, depression and seizures. CSF may show increased protein and CK and characteristic monocytosis. One reported case of listeriosis in a llama cria3 also exhibited rapid progression of clinical signs with uncontrollable seizures and was ultimately euthanased. The CSF in the described case had a very high WCC with 41% monocytes. Treatment in these cases often requires a lot of supportive care--intravenous fluids as most will be unable to eat or drink, anti-inflammatories, thiamine and nursing care. The author usually uses oxytetracline at 20mg/kg IV once daily for 5 days, but high dose penicillin given intravenously could also be used (80,000 IU/kg IV q6). Most cases fail to respond to treatment and the diagnosis can be confirmed at necropsy.
This is most often occurs as a sequel to failure of passive transfer in neonates. If neonatal septicemia is not recognised and controlled early enough, development of meningitis dramatically worsens prognosis. Affected crias may develop seizures but most often these crias appear extremely depressed, or are found to be sleeping more and more. In one case seen by the author, impaired CSF drainage presumably from cellular infiltrates resulted in a secondary hydrocephalus that was suspected on EEG and confirmed by CT. Following treatment with mannitol, the cria responded fairly rapidly by becoming more alert. Broad-spectrum antibiosis such as penicillin/gentamicin combinations should be used in septicemic crias while awaiting blood and/or CSF culture results together with intensive fluid and electrolyte therapy. If meningitis is suspected, third generation cephalosporins have quite good penetration into the CSF. Florphenicol is another antibiotic for consideration in such cases.
Cryptococcal meningitis was reported in an 8 year old alpaca in Australia which was possibly related to an episode of metritis 6 months earlier although the actual cause was not identified in this case.4 Cryptococcus is an opportunistic pathogen and usually only produces disease in immunocompromised animals. CSF cytology will identify the yeasts if present in reasonable numbers. Since it is rare, cryptococcosis is often not diagnosed until late in the disease process so that therapy is often ineffective.
Rye Grass Staggers/Toxicity
This is caused by ingestion of an endophyte growing within ryegrass species.5 This endophyte produces tremorgenic toxins called lolitrems and toxin levels are increased during dry weather. Rye grass staggers is normally a diagnosis of exclusion based on history and characteristic clinical appearance of head tremor since it is difficult to demonstrate toxic levels of endophyte in pasture. Also the toxic dose in camelids is not known. Animals normally recover when removed from affected pasture: however, permanent damage manifested by ataxia and head tremor may remain following prolonged exposure.
Cases of polioencephalomalacia have been described in the literature. Often the cause of polio in camelids is unknown but has been associated with dietary changes and excessive carbohydrate ingestion. We have seen it also as a result of inadvertent coccidiostat overdosage (amprolium). The classic presentation is a camelid presenting with acute-onset blindness and depression. Affected animals will usually be spotted wandering aimlessly or into fencing and other objects. Later, circling and head tremors may develop. Neurologic examination of the cranial nerves will typically show an absent or reduced menace response with normal or reduced PLRs: ophthalmic examination will reveal no obvious cause for the absent menace suggesting cortical blindness. Depending on the severity of the disease, the patient may also have reduced facial sensation and palpebral reflex. Depression may be intense. Occasionally, the author has seen a more atypical presentation in which affected individuals respond aggressively to handling and will charge into walls--these cases have been confirmed by subsequent necropsy evaluation. Bloodwork may be normal: acidosis was common in cases seen at OSU with carbohydrate overload or amprolium toxicity, but may also result from drooling saliva. Spinal fluid is usually unremarkable. When CT evaluation has been performed in affected animals, diffuse encephalitis is a typical finding. Response to therapy is often used to make a diagnosis in these cases. Treatment includes thiamine hydrochloride at 10-15mg/kg every 4 hours initially and thiamine administration should be continued until several days after resolution of clinical signs. Supportive and nursing care is very important. When patients are not eating or drinking, IV fluid therapy is usually initiated and the thiamine added to the intravenous fluids. Methylprednisolone may be used in animals exhibiting depression to help reduce any cerebral edema. If affected animals are likely to recover, they usually do so within 24 hours of starting therapy. It appears that early treatment is vital to the chances of success.
Equine herpesvirus (EHV-1) has previously been reported as causing blindness and encephalitis in alpacas and llamas and should be considered as a differential for camelids kept in close proximity to horses.6 In the last 5 years, West Nile Virus has been reported in camelids in the US, causing acute onset of progressive neurological signs and is usually fatal.7 Diagnostic confirmation is by PCR and immunohistochemistry of brainstem tissue. Eastern equine encephalitis (EEE) has also recently been reported as causing acute onset encephalitis which is again, usually fatal.8 These cases occurred on the east coast of the US where the disease is typically found in other species.
1. Whitehead et al. Unpublished. 2008.
2. Rickard LG, et al. J Zoo Wildlife Med 1994;25(3):390.
3. Van Metre DC, et al. JAVMA 1991;199(2):236.
4. Goodchild LM, et al. Aust Vet J 1996;74(6):428.
5. Holmes LA, et al. Vet Rec 1999;145:462.
6. Rebhun WC, et al. JAVMA 1988;192(7):953.
7. Kutzler MA, et al. JAVMA 2004;225(6):921.
8. Nolen-Watson R, JVIM 2007;21:846.