ORTHOPAEDIC OR NEUROLOGIC? A PRACTICAL APPROACH TO GAIT PROBLEMS

Gualtiero Gandini, DVM, Dipl. ECVN; Dipartimento di Scienze Mediche Veterinarie - Università di Bologna Via Tolara di Sopra, 50 – 40064 – Ozzano Emilia (BO) Email: [email protected]

Gait examination is of crucial importance and is a relevant part of the neurological examination. The correct evaluation of gait requires experience and, especially during the first steps of the veterinary profession, may be necessary to observe carefully and for long time the gait of a patient in order to “decode” adequately what is appreciated during the examination. Re-evaluation of video recording and the use of slow motion video can be very helpful. During gait evaluation, the first aim should be the pure description of what was noticed. The interpretation of the observed signs should be done only in a second time, matching them with the categories of gait abnormalities.

FUNCTIONAL ANATOMY: the normal gait –Normal gait in the dog and cat depends on the functional integrity of the cerebral cortex, the brainstem, cerebellum, spinal cord (including ascending and descending pathways), peripheral nerves (sensory and motor), neuromuscular junctions and muscles. A voluntary movement is initiated by nerve impulses generated in the cerebral cortex or brainstem. The cerebellum coordinates these voluntary movements and the vestibular system maintains balance during the performance of the movement. The nerve impulses from the brain to the peripheral nerves and, subsequently, to the muscles, travel along the descending tracts of the spinal cord. Information on the position of the limbs during movements reach the cerebellum and the forebrain from the periphery through the ascending tracts of the spinal cord and brainstem. For didactical purposes, it can be said that voluntary movement is the result of synergism between motor function (descending pathways) and sensory function (ascending pathways). Motor function – grossly, it can be said that two types of motor neurons form the descending motor tracts. The upper motor neurons, whose cell bodies are located in the encephalon, are the neurons that initiate a voluntary movement: the axons leaving these cells run down the central nervous system forming the descending tracts of the spinal cord and synapse with the lower motor neurons, bulky cells in the ventral horn of the spinal cord. The axons of the lower motor neurons exit from the spinal cord and, joining other motor fibres, form the spinal roots of the nerves, then the spinal nerves and, when appropriately grouped, the peripheral nerves. These axons connect to the striated muscle through the neuromuscular junction. Traditionally, the descending motor pathways are divided into the pyramidal and extrapyramidal tracts. These latter are formed of a series of interconnected and functionally related structures that run from the neurons of the forebrain to the lower motor neurons in the ventral horn of the spinal cord (in the brainstem for the cranial nerves). In the dog and the cat, the direct contribution of the forebrain (pyramidal pathways) to the control of gait is much less important than in anthropomorphic primates. In the dog and cat, lesions to the forebrain often cause modest or barely perceptible changes in gait, while lesions to the brainstem or spinal cord provoke fairly obvious abnormalities. Animals with lesions in the frontal or prefrontal cortex can have normal or almost normal gait as far as concerns coordination and strength of movements (sometimes there can be a mild hemiparesis on the opposite side of the lesion). In presence of a forebrain lesion, the gait can be compulsive: in severe cases the animal tends to walk continuously and aimlessly until it encounters an obstacle, where he can push its head against it. This particular compulsive behaviour is described as “head pressing”. Sensory function - proprioception – Kinaesthesia is the awareness of the position and movement of one’s own body and, in particular, the limbs. Kinaesthetic information is detected and conveyed by general proprioceptive neurons. The general proprioception system is, for teaching purposes, traditionally divided into the conscious proprioception system, which projects into the somatosensory cortex, and the unconscious proprioception system, which projects into the cerebellum. The general proprioceptive system is schematically formed of a peripheral receptor, part of the sensory component of the peripheral nerve, the ascending tracts carrying information to the cerebellum or, through the medial lemniscus, to the cerebral cortex. General proprioception, by providing continuous information on the position of the limbs during movement, is essential for the coordination of the movement itself. Other information inputs necessary for the coordination of movement derive from the vestibular system (special proprioception) and the visual system, with integration from the cerebellum.

GAIT EVALUATION - The gait of a dog must be evaluated by observing the animal from the side, from the front and from behind while it walks on a non-slippery surface in a straight line and turning, while it goes up and down stairs or while it walks on a slope. For dogs, it is advisable to carry out the examination in the open air and, if necessary, in a room in which the animal can move freely. Evaluating the gait of a cat can be much more difficult: a useful strategy can be to release the animal in the centre of the consulting room and observe its movements as it tries to reach the transport container, deliberately placed at a certain distance, or any other shelter. Video recordings from the owners may be very helpful in evaluating the gait of cats. It is important to be familiar with the normal gait of different species, breeds and age groups of animals. Subjects that have difficulty in remaining in a standing position and walking should be supported if necessary. Obviously, it is essential to ensure immediate and adequate immobilisation of the spine in patients suspected to have an unstable lesion of the vertebral column and gait evaluation should be performed only when after vertebral luxation/fractures have been excluded.

GAIT ABNORMALITIES - From the neurological point of view, the pathological gait can be the consequence of changes in coordination (ataxia), decrease in the strength of voluntary movements (paresis) or both.

ATAXIA- Ataxia can be classified into proprioceptive (or spinal or sensory), cerebellar and vestibular. Proprioceptive ataxia derives from lesions to nervous structures involved in the control of general proprioception (sensory fibres of the peripheral nerves, dorsal nerve roots, spinal cord, brainstem, forebrain). In clinical practice, proprioceptive ataxia is often associated with disorders of the spinal cord. This type of ataxia is characterized by a loss of the awareness of the spatial position of the body and, in particular, of the limbs (kinaesthesia). The severity of the ataxia depends on the extent of the lesion and can range from just perceptible changes to obvious deficits. In the latter cases the limbs are excessively abducted and/or adducted during walking, they cross and, sometimes, there is a tendency to stand on the dorsum of the foot (“knuckling”). It is important to remember that, neuroanatomically, the proprioceptive and motor pathways are intimately related throughout the spinal cord and caudal brainstem and proprioceptive ataxia is, therefore, often associated with paresis. Ataxia can affect the hindlimbs (for spinal lesions caudal to the T2 vertebra) or all four limbs (for spinal lesions cranial to the T2 vertebra). Cerebellar ataxia is caused by disorders of the cerebellum or, more rarely, lesions that selectively affect the spino-cerebellar tracts. This type of ataxia is characterized by inability to regulate the force and range of movements with consequent dysmetria, often detected as hypermetria (an exaggerated elevation and protraction of the step). This type of ataxia is often associated with other cerebellar symptoms such as a broad- based stance and intention tremors. Cerebellar ataxia, unlike proprioceptive ataxia, is not associated with paresis. Vestibular ataxia associated with unilateral vestibular lesions is characterized by a tendency to sheer, fall or roll to one side (usually ipsilateral to that of the lesion). This type of ataxia is associated with vestibular signs such as head tilt, resting nystagmus, positional strabismus and the tendency to circle. In case of peripheral bilateral vestibular disorder, the animal develops symmetrical ataxia with loss of balance on both sides and movements of the head from one side to the other. In order to show defects in coordination it can be useful to make the animal walk up and down a flight of stairs. Animals with ataxia usually have more pronounced difficulties descending the stairs, where the imperfect control of the movements can cause the animal to fall.

PARESIS/PARALYSIS - Paresis is the partial loss of voluntary motor function. Paralysis (or -plegia) is the complete loss of this function. Paresis and paralysis are, therefore, two terms that define the same type of defect (motor deficit or defect of the descending function), differing only in quantitative terms. Paralysis is a more severe condition than paresis, although not necessarily irreversible.

Paresis can show different degrees of severity and can be distinguished into ambulatory (when the animal, despite the motor deficit, is able to stand on its four limbs and walk autonomously) and non-ambulatory (when the animal needs to be supported in order to be able to stand and try to walk). In these latter cases it is very important to take the animal outside and support it correctly in order to detect evidence of any, even minimal, voluntary motor activity. This enables to distinguish severe paresis from paralysis, which provides useful prognostic information. Different terms are used to define which limbs are affected by the motor deficit: monoparesis/monoplegia (a single limb), paraparesis/paraplegia (both hind limbs), hemiparesis/hemiplegia (the fore and hind limb on the same side), tetraparesis/tetraplegia (all four limbs). There are two types of paresis/paralysis: spastic paresis/paralysis, caused by dysfunction of upper motor neurons, and flaccid paresis/paralysis, caused by dysfunction of lower motor neurons. Spastic paresis/-plegia occurs because the upper motor neurons have a modulating effect on the lower motor neurons which, among other functions, maintain muscle tone. A lesion of upper motor neurons causes a deficit in the modulating input to lower motor neurons and, therefore, “frees” these latter from the upper control. The effect is disorganized recruitment of lower motor neurons, with consequent hypertonicity of muscles and spasticity. In contrast, if the lesion affects the lower motor neurons, there is flaccid paresis/paralysis, precisely because those neurons responsible in the first place for maintaining muscle tone are damaged. It should be remembered that lesions of moderate entity of the spinal cord give rise to mixed gait disorders, with concomitant paresis and proprioceptive ataxia, given the contiguity of the ascending proprioceptive tracts and the descending motor ones. From the clinical point of view, in presence of moderate spinal cord lesions it is almost impossible to distinguish the part of the proprioceptive deficit from that of the motor deficit. In those cases, it is preferred to use simply the term “ataxia and paresis”. Usually, in these ambulatory cases, ataxia is much more prominent than paresis. In animals with generalized lesions to the efferent part of the peripheral nervous system (neuromuscular system) the efferent motor component is specifically affected and can produce severe motor deficits. These cases are described usually as paresis (“weakness”) or paralysis with reduced muscle tone and strength, because the lower motor neuron system is affected. A typical sign of paresis due to neuromuscular disorders is exercise intolerance, characterized by an inability to perform a normal workload, usually not involving any particular effort. In this case, the gait initiates almost normally but rapidly changes to an increasingly short-strided gait. Furthermore, the animal develops joint hypometria and hyperflexion, inability to support its own weight, tremor and breathlessness, to the point that it needs to lie down on the ground and rest.

The presence of lameness usually suggests an orthopaedic problem, Nevertheless, lameness can also be caused by neurological pathologies involving the nerve roots (for example a lateral extrusion of an intervertebral disc or neoplasia of the nerve sheaths) which give rise to the nerves to the limbs. This type of limping is called “nerve root signature”. Ataxia and paresis are signs of dysfunction of specific structures of the nervous system. In this perspective, the finding of gait alterations must be assessed together with any other sign found during the neurological examination in order to identify the site of the lesion. It is on the basis of this anatomical localization of the lesion that all the clinical differential diagnoses are hypothesized, and the consequent appropriate diagnostic protocol formulated.

GAIT ABNORMALITIES OF DIFFICULT INTERPRETATION: ORTHOPAEDIC OR NEUROLOGIC? – As a rule, orthopedic diseases affecting the locomotor system produce abnormalities related to pain and consequent lameness. In addition to the lameness, the typical signs of an orthopedic disorder include the reluctance to make movements and the difficulty in standing. In addition, an orthopedic problem usually does not produce neurological sings and, in most cases, affects a single limb, less frequently two, or rarely four limbs. Typically, problem localization and problem definition may occur especially in those cases where only one limb is affected. During gait examination, the thoracic limb lameness produces the reluctance to load the body weight on the affected limb. It is important for the veterinarian to know how to distinguish between a gait that is an expression of lameness and one that is instead expression of monoparesis. In most cases, these two alterations underlie dysfunctions from different systems. In the first case, the limb takes shorter steps, the support phase is greatly reduced and the animal uses all the mechanisms, such as the so-called "head kick", to reduce the load of the weight of the body on the affected limb. The lame limb, when touches the ground, has a shorter support phase and, simultaneously, the animal raises the head to move back the weight of the body. Immediately afterwards, in the movement sequence, the contralateral limb is entirely loaded with all the bodyweight. In most severe cases, the limb is even lifted and is not nearly able to touch the ground. A neurological problem, instead, produces different degrees of limitation of the voluntary movement. If it is relatively easy to recognize monoplegia, characterized by the total absence of voluntary movement and the knuckling of the hand, it is more difficult to grasp the difference between a moderate monoparesis and lameness. The paretic limb does not tend to subtract load of the body weight. Conversely, especially if the radial nerve is affected, it tends to collapse under the weight of the body and maintain a posture with the knuckled hand. The stride is typically hypometric and may show hints of proprioceptive deficits, culminating in spontaneous dorsiflexion of the hand. Monoparetic limbs may exhibit hypotrophic and hypotonic muscle due to neurogenic atrophy. Typically, acute limb monoparesis / plegia is the result of a traumatic avulsion of the brachial plexus.

However, there are neurological disorders representing important exceptions, where the clinical dysfunction is represented by pain and lameness rather than the traditional neurologic deficits such as paresis and proprioceptive deficits. Diseases responsible for signs mimicking an orthopaedic pathology are represented mainly by lateralized disk extrusion and tumour of the nerve roots of the brachial plexus. Lateralized disk extrusions may be responsible for a severe and typically acute-onset presentation, characterized by lameness and cervical rigidity. This clinical presentation is defined “root sign”, as it is due to the compression of the nervous root emerging from foramen of the affected intervertebral space. Very often, there are no other neurological signs that may help the veterinarian in logging the clinical differential diagnoses and the subsequent diagnostic work-up. Neoplasms of the nerve roots are tumours originating from the cells of the axon sheaths. One of the most frequent seat of these neoplasms is the brachial plexus. Growth is usually centripetal, with subsequent involvement and infiltration of the other roots of the brachial plexus. These tumours become responsible for insidious onset and chronic progressive pain. When the disease progresses over time, other signs on the affected limb, such as neurogenic atrophy of the muscles innervated by the affected root, paresis, and decreased spinal reflexes, become evident. In specific cases, a concomitant Horner’s Syndrome (myosis, enophthalmos, and third eyelid prolapse) and decreased cutaneous trunci reflex may also be observed due to the specific involvement of the nerve roots. In the most protracted cases in which the spinal canal invasion has occurred, motor and proprioceptive deficits in the ipsilateral hind limb may be recorded. The hind limbs, especially in the dog, are affected by a variety of orthopaedic diseases producing varying degrees of pain and difficulty in walking. Even in this case, some pathologies belonging to the sphere of competence of the neurologist should be considered in the differential diagnosis. It is essential to recognize and differentiate incoordination and weakness (paresis) from the most frankly orthopaedic deficits, such as the abovementioned lameness. In the early stages, many veterinarians still misdiagnose chronic-progressive neurologic disorders, such as degenerative myelopathy, for orthopaedic pathologies. Careful gait examination may show an incoordination (ataxia) not justified by orthopaedic diseases. Postural and proprioceptive reactions, normal in animals affected by orthopaedic pathologies, may be abnormal in cases of a neurologic disorder. Special importance must be dedicated to the evaluation of the integrity of the proprioceptive pathways, especially through the proprioceptive positioning test. As with the forelimb, there are some neurological disorders producing signs that may be confused with the effects of an orthopaedic problem. Degenerative lumbosacral stenosis (DLS), commonly (though improperly) described as "cauda equina syndrome", plays an extremely important role in pathologies that may produce hind limbs "orthopaedic" signs. DLS is characterized by pain associated with the L7-S1 junction, which is manifested by reluctance to perform all the movements, such as jumping on the owner's machine or jumping over obstacles, producing a sharp extension of the lumbosacral joint. The majority of DLS produces pain in the absence of clear neurological deficits. The pain can be lateralized and apparent on a single limb if compression of the nerve root occurs at the foraminal level. Pain is also suggested by the posture of the lower back, kept in kyphosis, and reluctance to change abruptly position: the animal can show extreme caution in the act of getting up, lying down or jumping. These sings may induce the vet to consider an orthopaedic disease. The palpation of the back (a complex of test inducing pressure and hyperextension of the lumbosacral junction) and, particularly, the lordosis test, can elicit a marked reaction of the affected animal. In the most severe cases, there are also obvious neurological deficits in the hind limbs, characterized by hypometry, mild paraparesis, mild proprioceptive deficits (useful in differentiating thoracolombar disorders, in which proprioceptive deficits are much more obvious, from those of the cauda equina).

Gait disturbances related to dysfunction of the Peripheral Nervous System Patients suffering from a peripheral nervous system disease show extremely variable clinical signs depending on several factors including the severity, the extension and the onset and course of the pathological process. Mononeuropathies can be easily distinguished by polyneuropathies. In the first case, the involvement of a single nerve is observed and the resulting clinical presentation is extremely localized. Sometimes in the same limb multiple nerves, generally anatomically related, can be affected. Even in this case the extension of the process is always confined to a restricted district. Polyneuropathies produce generalized peripheral nervous dysfunction and the clinical signs, due to the involvement of the whole body, are usually present symmetrically and affect different districts. It is important to remember that in domestic animals polyneuropathies mainly affect selectively the efferent fibers, namely the motor component. The resulting clinical presentation consists in weakness and exercise intolerance. Although not immediately recognizable by an inexperienced eye, the alterations of the gait in a polyneuropathic patient are characterized exclusively by paresis and not by ataxia. The apparent incoordination observed in some cases, reflects the weakness of the patient and not the primary damage of the proprioceptive system. In these cases, to properly localize the lesion,it is crucial to pay close attention not only to the features of the gait but also to the spinal reflexes (uniformly diminished) and to the postural and proprioceptive reactions. In the neuromuscular patient, abnormal postural reactions can only testify the extreme weakness impeding the normal motor response phase. In case of mononeuropathies, the distinction between spinal cord injuries and orthopaedic disorders is mainly done by evaluating spinal reflexes, muscle tone and gait.

The material used for this abstract is partially taken by the material prepared by the Author for the website www.vetpedia.net . In this website, there is the possibility to look at some videos that may help to clarify the above discussed gait abnormalities.

REFERENCES:

1. Gandini G. e D’Angelo A. “Esame del sistema nervoso (esame neurologico)” (2014). In: Semeiologia Clinica Veterinaria. Editor: P.Ciaramella – Poletto Editore Milano pp. 245- 290. 2. Parent J. “Clinical approach and lesion localization in patients with spinal diseases”. Vet Clin North Am Small Anim Pract. 2010 Sep;40(5):733-53 3. Bernardini M. “L’esame neurologico”. In: Neurologia del cane e del gatto. Seconda Edizione (2010) – Poletto Editore Milano, pp.31 - 69. 4. Braund KG: Clinical Neurology in Small Animals. International Veterinary Information Service, IVIS (www.ivis.org), Ithaca, New York, 2010 5. De Lahunta A, Glass E, Kent M: Veterinary neuroanatomy and clinical neurology, 4th ed, WB Saunders, Philadelphia, 2014 6. Dewey CW Da Costa: A practical guide to canine and feline neurology 3rd ed, Blackwell, Iowa State Press, 2015 7. Lorenz MD, Coates J Kent M: Handbook of Veterinary Neurology, 5th ed, WB Saunders, Philadelphia, 2011 8. Platt SR, Olby NJ: BSAVA Manual of Canine and Feline Neurology, 4th ed, BSAVA Publications, 2013 9. McDonnell JJ, Platt SR, Clayton LA “Neurologic conditions causing lameness in companion animals”. Vet Clin North Am Small Anim Pract. 2001 Jan;31(1):17-38.