Approach to the Neurologic Camelid: Clinical Neurological Examination, Lesion Localization & Diagnostics
ACVIM 2008
Claire E. Whitehead, BVM&S, MS, DACVIM, MRCVS
London, UK

The presentation of neurological disease in camelids, as in other species, varies widely. There are many different causes of neurological signs (Table 1) and the clinician must be aware that metabolic and musculoskeletal disease can also present with neurologic signs. These conditions must be differentiated from those of true neurological origin by careful history-taking, physical examination and use of appropriate diagnostic tests.

Table 1. Differential diagnoses of neurologic disease in South American camelids.

Congenital Diseases

 Hydrocephalus

 Kyphosis

 Atlanto-occipital malalignment

Traumatic

 Vertebral body subluxation/luxation*

 Vertebral body fracture*

 Trauma without subluxation/ luxation/ fracture*

Infectious/Parasitic Diseases

 Meningeal worm (P tenuis infestation)--United States*

 Listeriosis

 Otitis media/interna*

 Brain abscess

 Vertebral body abscess

 Septicaemia/meningitis*

 Viral, eg EHV-1, West Nile, EEE

 Clostridial myositis

 Rabies

Metabolic Diseases

 Pregnancy toxaemia*

 Hypo/hyper-glycaemia

 Hepatic encephalopathy

 Uraemic encephalopathy

 Hypomagnesaemia

 Nutritional problems

Degenerative

 Degenerative myelopathy

 Spondylosis

Toxicities

 Tetanus

 Botulism

 Rye grass staggers

 Cerebral hypoxia

 Tick paralysis

 Ionophore toxicosis

Musculoskeletal

 Bilaterally luxating patellae

 Hip problems

 Peripheral nerve damage

 Gait abnormality

Other

 Hypo/hyperthermia*

 Mega-oesophagus

 Brain/spinal cord neoplasia

 Facial nerve paralysis

Determine Whether the Neurologic Signs are Due to a Lesion in the Nervous System

Firstly, it is vital to obtain a thorough history of the problem, especially whether the clinical signs were acute or chronic in onset, the duration of clinical signs, deworming programme (parasitic myelopathy), diet and any dietary changes, and of course signalment. Determine whether or not a traumatic incident was observed, whether there have been any seizure episodes, and also how the problem began. For example, for a recumbent camelid, knowing whether the problem began with the forelimbs, hindlimbs or both can be useful historical information. In heat stress cases, patients often develop weakness in the forelimbs primarily, whereas patients with parasitic myelopathy develop ataxia and weakness typically in the hindlimbs first.

When performing the basic clinical examination, look especially for evidence of cranial nerve deficits, postural or proprioceptive deficits, and ataxia, differentiating this from weakness. These may be difficult to assess in the recumbent animal, especially adults. However, with alpacas and youngsters, it is usually possible to assist the animal to stand, possibly with the use of a sling, so that placing reflexes can be tested. Sometimes, it may be hard to distinguish one condition from another clinically, and do not discount the possibility that two conditions may be present together, e.g., parasitic myelopathy with secondary heat stress in summer.

Hematological and biochemical profiles may help identify metabolic causes. A spinal tap is easily performed in camelids from the lumbosacral space, and changes in the cerebrospinal fluid (CSF) will help establish whether a disease process involves the central nervous system (the technique is described later).

Localisation of a Lesion Within the Nervous System

This is a continuation of the clinical exam. Observe the resting animal, preferably while unstimulated, and assess mental status. Look for any head tilt, circling behavior, leaning to one side or head-pressing. A head tilt may be due to otitis, a vestibular lesion or possibly neck pain. If tremors are present and the head is involved, the lesion is likely to involve the cerebellum. Tremors may also occur with electrolyte imbalances (mainly hypocalcemia and hypomagnesemia), myelin disorders, with some toxins or with diffuse encephalitis. The presence of seizures indicates brain involvement, but this may be secondary to a metabolic abnormality such as hypoglycemia or be due to a primary lesion. Depression, cortical blindness, and slow PLRs (not ophthalmic in origin) may indicate presence of a brain lesion. If the animal can walk, look for weakness versus ataxia, single or multiple limb involvement, whether the problem is unilateral or bilateral, or if one side of the animal or one half (front or back) is worse than the other. Assess the animal's gait and ability to turn in circles etc.

Assessment of proprioception can be done, but may be difficult to assess in camelids with subtle problems since they often resent having their feet touched. Various reflexes can be assessed including withdrawal reflexes, anal tone, patellar reflex, gastrocnemius reflex etc. Withdrawal reflexes are best tested in camelids by squeezing the digits at the distal end of the digital pad using hemostats. Normal reflexes indicate that sensory and motor function are working normally. Absent or reduced reflexes indicate partial or complete loss of sensory or motor parts of the reflex (LMN). If unilateral, this is most likely to be due to a peripheral lesion whereas bilateral absence or reduction of reflexes is more likely to suggest the presence of a spinal cord lesion. Exaggerated reflexes indicate that there is an UMN defect. The panniculus reflex is difficult to assess in camelids, partly because of their thick skin but also because they may have be heavily fleeced for much of the year. I do not find this test particularly useful in camelids.

Palpation of muscle masses is useful in evaluation of muscle atrophy (symmetrical versus non-symmetrical) and general body condition.

Examination of the cranial nerves should also be performed in the neurologic camelid. This should include evaluation of the palpebral reflex, facial sensation, menace response, pupillary light reflexes, and assessment of pupil size and symmetry. Look for nystagmus or strabismus. Observe facial symmetry and determine whether or not ptosis, enophthalmos, or rotation of the globe are present. Hearing may be difficult to test in camelids except by observing their reactions to their environment when unrestrained. Where specific hearing deficits are suspected, these may be evaluated using the Brainstem Auditory-Evoked Response test.

The interpretation of data from the neurologic exam aids the clinician in determining the region affected and also whether the lesion is upper or lower motor neuron in origin (Tables 2 and 3). Lower motor neurons are the efferent nerves that connect the CNS to the muscles, while upper motor neurons initiate movements and control extensor muscle tone which is responsible for supporting the body at rest.

Table 2. Characteristics of lower and upper motor neuron lesions.

LMN lesions

UMN lesions

Paresis to paralysis

Paresis to paralysis

Reduced/absent reflexes

Normal or exaggerated reflexes

Loss of muscle tone

Normal/Increased muscle tone

Muscle atrophy appears quickly

Muscle atrophy is slow to appear

Table 3. Localisation of spinal cord disease based on clinical neurologic features.

Spinal cord region

Neurologic features

C1-5

UMN signs to all 4 limbs

C6-T2

LMN signs to FL: UMN to HL

T3-L3

Normal FL: UMN signs to HL

L4-S2

Normal FL: LMN signs to HL

S1-3

Partial LMN signs to HL, incontinence

Determine the Cause of the Neurologic Lesion

Once the clinician has established that he/she is dealing with a neurologic disease and then determined what neurological deficits are present, further diagnostics will be helpful in reaching a specific diagnosis. Some tests may be done easily in practice whereas others may be limited to specialist or referral facilities.

CSF Sample Collection

Normally CSF is taken from the lumbosacral space. Lumbosacral and atlanto-occipital CSF samples were compared in llamas that were experimentally infected with P tenuis.1 This study concluded that the site chosen would depend on the suspected location of the lesion. Welles et al (1994)2 stated that, based on work in horses, CSF from the lumbosacral space was more likely to have compositional abnormalities in neurological disease and that more useful information would therefore be obtained. In another report, samples from 3 llamas with suspected meningeal worm were collected simultaneously from the LS and AO spaces: the CSF collected from the LS space showed more significant elevations in protein and cell count.3

The lumbosacral tap is an easy procedure to perform in camelids and usually requires only a little local anaesthetic whereas the atlanto-occipital tap requires sedation or anaesthesia and is a risky procedure. A small area is clipped and prepared over the LS space after ensuring that the animal is squarely positioned and the hind legs are pulled forward in order to open up the LS space. The landmarks are the dorsal spinous process of L7 and the two wings of the ilia. These landmarks form a triangle within which an obvious depression can be palpated. Before the final scrub, inject 0.5-1ml local anaesthetic at the site using a 22G one inch needle. Using an 18G 3.5inch spinal needle in adults (20G in crias), insert the needle perpendicular to the skin on the midline about 3-5mm in front of an imaginary line drawn between the two ilia. It helps to anchor the wrist on the animal's pelvis as this is done because the skin is quite thick. In an adult, the needle needs to be advanced 2-4cm and "two pops" are usually felt as the needle goes through the dura into the subarachnoid space. If unsuccessful, ensure midline placement and try directing the needle a bit more cranially. Usually the patient will "jump" when the needle penetrates the dura. When the stylet is removed, CSF will be observed in the hub. Collect 2-3ml CSF and split the sample into a plain tube for CSF profile (protein/creatine kinase (CK)/electrolytes etc) and an EDTA tube for cytology (red and white cell counts and differential counts). Welles et al (1994)2 observed rapid deterioration of leukocytes in CSF after collection and advised careful handling and refrigeration as soon as possible following collection. Their method did not indicate that any preservative was used: it is likely that collecting CSF into EDTA tubes will reduce the deterioration of cells.

The most important variables to consider in the CSF are protein concentration and cytology but in certain disease situations other variables such as sodium and glucose may be useful. CK concentration may also be of value in indicating CNS disease although some studies have shown that it may increase due to the presence of epidural fat in the sample. Normal CSF protein concentration in camelids is less than 45-50 mg/dl, normal CK concentration is less than 10 IU/L and white cell count should be less than 3 cells/µl. The normal white cell population may be predominantly lymphocytes or neutrophils depending on the amount of blood contamination (more neutrophils with increasing blood contamination). In the absence of blood contamination there should be no eosinophils. In camelids, the proportion of eosinophils increases in meningeal worm (parasitic myelopathy)1,2,3,4,5 and can be up to 99% of total white cells--eosinophilic pleocytosis with increased protein concentration in the CSF is present in most affected camelids. However, a normal eosinophil count does not necessarily rule out meningeal worm: in experimental infection of llamas with P tenuis, the time post-inoculation at which eosinophils increased in CSF varied. Also, prior treatment with anthelmintics may affect cell counts. Clinical observations suggest that the length of time following initial development of clinical signs until CSF is collected can result in lower percentages of eosinophils seen on cytology. P tenuis infestation is the only parasitic myelopathy so far reported in camelids.

Increased protein indicates a disturbance of the blood-brain-barrier and this may occur in any inflammatory disease process including trauma, parasite migration, meningitis and otitis: if protein electrophoresis shows increased globulin only, this indicates intrathecal synthesis of globulins. Welles et al2 found in their study that in healthy llamas with red cell counts <1400 /µl, the protein concentration was only minimally altered.

Glucose concentration in llama CSF is approximately 40% of serum concentration.2 This compares with cattle in which CSF glucose is approximately equivalent and monogastric species in which it is 60-80% of serum concentrations: rapid changes in serum glucose, as in stress for example, will take 30mins to 3hours to equilibrate in CSF.2 Bacterial infections will decrease CSF glucose and also increase neutrophil count--for example, in bacterial meningitis in crias.

Increased sodium concentration in the CSF could reflect severe metabolic derangements and may occur in salt toxicity due to unavailability of water, and in crias with hyperosmolar syndrome. This can cause intense CNS depression and needs to be carefully managed. Sodium concentrations should not be reduced too rapidly or cerebral oedema and herniation of the brainstem may occur.

Radiographs

Depending on the clinical signs, localisation of lesion, and CSF findings, spinal or skull radiographs may be useful. These may highlight obvious luxations, fractures or soft tissue injuries as well as demonstrate congenital malformations such as kyphosis. Two views are essential for cervical films as single view films may not pick up subluxations etc. For more subtle lesions, a myelogram may be indicated but is rarely found to be necessary in order to reach a diagnosis. Camelids have 7 cervical, 12 thoracic, 7 lumbar, 5 sacral vertebrae and 10-15 coccygeal vertebrae.

Ultrasonography

May be useful in evaluation of soft tissue injuries and hydrocephalus.

Computed Tomography (CT)

CT may be required to visualise a suspect area, especially where the head is involved. We have found that, in the case of suspected otitis interna, CT gives a significantly better image of the tympanic bullae than plain radiographs and the extent of soft tissue involvement can be delineated using contrast CT. CT also guides the surgical approach in these cases. It is also useful if a brain mass/abscess or vertebral body abscess is suspected, although MRI is likely to be preferred if soft tissue or subtle lesions are suspected. General anaesthesia is required.

Electromyography (EMG)

Measures the electrical activity of muscle. It is useful to detect denervation and can allow localisation to specific spinal cord segments. It may be used to direct the clinician to a particular problem area. This is a good tool for investigating myopathies and neuropathies.

Muscle Biopsy

Muscle biopsies may be useful if a myopathy is suspected rather than a neuropathy.

References

1.  Rickard LG et al. J Zoo Wildlife Med 1994;25(3):390.

2.  Welles EG, et al. Am J Vet Res 1994;55(8):1075.

3.  Scarratt WK, et al. Prog Vet Neurology 1996;7(4):124.

4.  Pugh DG, et al. Comp Cont Ed 1995;17(4):600.

5.  Baumgärtner W, et al. JAVMA 1985;187(11):1243.

Speaker Information
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Claire Whitehead, BVM&S, MS, DACVIM, MRCVS
The Royal Veterinary College
Hatfield, Hertfordshire, United Kingdom


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