Disorders of gait: Classification and differential diagnosis

E. Ruzicka The classification of disorders of gait has not yet been unified. In clinical practice, there is a certain tradition in the use of terms (e.g. paretic, ataxic, senile, parkinsonian gait, etc.) that are well-founded in clinical experience but lack generally accepted definitions and therefore they may be comprehended in a different way and may not always reflect identical disorders of gait. In this Atlas and in practice, we recommend the use of a phenomenological classification based on a description of the basic features and clinical signs brought out during posture and gait examination. However, phenomenological classification may not reflect an explicit diagnostic category. Specific categorization of the gait disorder according to affected systems or diseases may be difficult because of the combination of patterns and mutually overlapping clinical features. Thus, for instance, the stiff gait pattern may indicate spasticity in pyramidal lesions, dystonia or rigidity arising from basal ganglia, but also restricted leg movement due to joint and musculoskeletal problems. The clinical-anatomical classification then proceeds from the site of the damage usually responsible for the complex gait disorder pattern resulting from a combination of several basic phenomenological features.

A. Phenomenological classification of gait disorders (basic gait disorder patterns) A1. Gait disorders due to muscular weakness Owing to muscular weakness (in primary muscle diseases and in peripheral nerve involvement), motion in the segment and direction concerned is affected by reduced strength or is altogether impossible. Weakness severe enough to result in abnormalities of gait is usually noticeable during the basic neurological examination, due to abnormal posture of the segment, decreased muscle tone and reduced strength. Depending on whether the proximal or distal muscles of the leg are affected, gait patterns are classified as proximal weakness (waddling gait, duck gait) and distal weakness (cock gait, steppage). A1.1 Proximal weakness (waddling gait, duck gait) Weakness affects the pelvic girdle muscles and proximal muscles of the leg normally responsible for support hip abduction and for keeping the pelvis in horizontal position while walking. Owing to gluteal muscle weakness, the hip tends to tip toward the swing leg. To compensate for this abnormal situation, lumbar hyperlordosis develops with the trunk flexing toward the support leg. The hip and trunk swing from side to side to compensate for the difficulties in lifting the leg. The alternate collapsing of the hip gives the impression of waddling, hence the term duck gait. Due to muscle weakness, arising from a chair is often feasible only with the support of the upper extremities. The difficulties are even more conspicuous when getting up from lying or sitting on the ground, with the patient forced to lean against the floor, surrounding objects or his/her own lower extremities (myopathic climb). Walking up and downstairs will also reveal weakness. This pattern of gait is typical of muscle disorders (myopathy, myositis, mechanical trauma) but, allied with other relevant symptoms, may also accompany neuropathies, lesions of lumbar plexus, cauda equina and conus medullaris.

A1.2 Distal weakness (cock gait, steppage, slapping gait) The most frequent pattern of gait disorder due to weakness of the anterolateral (peroneal) muscle group of the leg takes the form of footdrop as the patient lifts the foot to clear the ground. While walking, in order to keep the tip of the foot clear of the floor, he/she must flex the extremity excessively in the hip and lift the knee (cock gait). In the touch-down phase, the foot first rubs against the floor with the great toe or with the anterolateral edge before all of the sole of the foot steps down (steppage gait). Weakened dorsal flexion of the foot renders the patients unable to walk on their heels as they cannot lift the tip of the foot on the affected side. Injury to the peroneal nerve may be caused by a range of peripheral neuropathic processes or a local trauma. Features of peroneal nerve lesion may also develop in lumbar plexus lesion and in fifth lumbar nerve root (L5) affection, usually as a result of intervertebral disc herniation. The involvement of the posterior group of crural muscles, especially of the triceps surae (separate or in combination with peroneal paresis), is characterized by weakened plantar flexion and leg adduction. While walking, the patient has problems rolling the sole of the foot off the floor and pushing off with the tip of the foot. Instead, the foot comes down flat like a flail (slapping gait, flail foot). In efforts to walk on tiptoe, the foot collapses on the affected side, or the patient is totally unable to assume the tiptoe position. The posterior group of muscles is usually affected in circumstances similar to peroneal nerve lesion and also in radicuopathy (nerve root S1). B. Anatomic-clinical classification of gait disorders Assessment of basic gait pattern (see phenomenological classification) is an important prerequisite for a proper diagnosis. A clinical disorder of gait is often a combination of basic dysfunction and related compensatory changes. In the course of time and with the progression of a disease, the pattern of a particular patients gait may evolve and change. However, many entities are characterized by typical gait disorder reflecting the location (and perhaps even etiology) of corresponding lesion.The anatomic-clinical classification is based on the categories defined by three basic anatomical levels of affection: corticosubcortical (top level), subcortical and cortico-spinal (medium level) and peripheral (lowest level) disorders of gait. Despite some overlap, in the majority of cases these broad categories do permit fairly accurate differentiation. B1. Cortico-subcortical gait disorder Frontal corticosubcortical disorder of gait is usually a combination of disordered locomotion and balance. The mildest forms can be seen as manifestations of the cautious gait which is normal in clearing poorly negotiable terrain or in old age. The rest go beyond what is a rather fuzzy dividing line into the broad spectrum of frontal apraxia of gait.Corticosubcortical disorders of gait also include subjects with a dominating pattern of disorders of gait initiation and maintenance. Admittedly, the pathological mechanisms of start hesitation or freezing gait are connected with disordered implementation of motor programs which, however, are not perturbed in themselves. These, then, are no manifestations of apraxia as used to be believed. In addition, attention and processing of sensory information is critical to the execution of walking. Involvement of frontal cortical dysfunction is assumed, especially in the supplemental motor area. B1.1 Cautious gait The term cautious gait refers to a careful gait that resembles a gait designed to prevent a

fall on a slippery or unsteady surface, e.g., on ice, on board ship or on a rickety footbridge. Widened base, slow and short steps are the characteristic features of this particular gait. Even when walking over uncomplicated terrain, this pattern may indicate a more or less adequate adaptation in the elderly who are aware of their age-related sensory weakening and locomotor apparatus fragility. The kinesiologic records of elderly healthy persons show a slowed-down walking speed, shortened strides, reduced synkinesias of the arms, flexed knees and reduced toe lift. In some cases, though, cautious gait evolves quite abruptly, e.g., as a result of a fall with or without injury. Following such a fall, patients lose confidence in their ability to walk and maintain balance and begin to walk on a wide base with the need to hold on to the walls or other persons (post-fall syndrome). Similarly, fear of moving in an open space may develop (pseudoagoraphobia), but with the ability to walk about ones home remaining preserved. Some patients become totally incapable of walking due to an exaggerated fear of falling, which bears no relation to the degree of their motor or sensory deficit. Patients with this overcautious gait thus become totally disabled, and only some of them can benefit from intensive gait training and anxiolytic medication. B1.2 Frontal apraxia of gait ( astasia-abasia, basophobia, lacunar gait, senile gait, lower body parkinsonism, magnetic gait, Bruns ataxia, marche a petits pas ) It follows from the many different synonyms applied to this group of gait disorders that their classification poses some difficulties. Although the term parkinsonism is sometimes used in describing gait disorders from this group, the patients show few of the signs characteristic of Parkinsons disease such as tremor at rest, hypomimia, dysarthria, or upper limb bradykinesia. Nor does the term senile gait seem to fit, since even young persons may display a similar gait pattern in the setting of frontal lobe dysfunction. In reality, the clinical picture is, to a variable degree, characterized by a combination of features of a number of abnormal gait patterns in particular, disordered initiation, ataxia and stiff gait. Patients usually complain of slowing down and lower confidence in their gait, maybe of fear of falling. There is often abnormal body posture while standing, with the trunk held upright, sometimes in a hyperextension, bended knees and pelvic decline. The base is mostly widened, in walking almost excessively so, whether or not disequilibrium is present. As a rule, there is often disordered gait initiation with start hesitation, shortened stride and shuffling feet stepping down with the full surface of the sole. The double-support phase is markedly prolonged in the walking cycle. Patients exhibit a marked tendency to retropulsion leading to backward toppling falls (or so called crescendo retropulsion, in which accelerating short-stepped backward locomotion ends up in a fall). The upper limb synkinesis usually remains unaffected. If there is simultaneous gait freezing it may be accompanied by bizarre signs of an effort to initiate or maintain walking with excessive arm-swinging, with the trunk swaying from side to side, and so on. Anxious concern over maintaining the greatest possible stability leads to using one of the legs as leading and pushing the second leg forward. Such locomotion can not be characterized as nothing but a gait caricature. In marked contrast to this severe disorder of gait, leg motor function is well preserved when examined in the supine position, including the ability to perform stepping and pedaling movements. Hence, this group of disorders is sometimes referred to as apraxia of gait. Indeed, patients may exhibit apraxia while getting up or sitting down; attempts at changing position are marked by bizarre and purposeless movements. In

addition, there are some other signs of frontal lobe involvement disinhibition of behavior and primitive reflexes, cognitive disorders, and pseudobulbar palsy. The disorder is often due to multiple ischemic lesions of the frontal-lobe white matter corresponding to multi-infarct or subcortical encephalopathy (Binswangers disease), or to circumscribed encephalomalacia in the area supplied by the anterior cerebral artery. This type of gait disorder is also present in normal pressure hydrocephalus, Alzheimers disease, cortico-basal degeneration and in other bilateral affections of the frontal lobes. Treatment dispensed in accordance with the underlying cause will, as a rule, yield little success except perhaps for shunt operations for normal pressure hydrocephalus. Rehabilitation and gait training may offer at least temporary improvement and increased confidence. Support aids (walker, walking frame) remain largely without any great effect. Instructions for care providers, rearrangement of the domestic environment, or proper use of a wheelchair are important measures designed to improve quality of life and prevent fall-related injuries. B1.3 Disordered gait initiation (pure akinesia, primary progressive gait freezing, trepidant abasia, Petrns gait, motor blocks ) Disordered gait initiation and maintenance has been described in phenomenological classification as one of the basic patterns of gait disorder related to pathological involvement of the circuits involving the basal ganglia together with the brainstem nuclei, thalamus and frontal cortex. Apart from its crucial role in motor control, this system plays a role in triggering goal-directed activity and in the processes of attention. Damage to any component of the system may cause gait freezing and related disturbances. Hence it is seen often within the context of Parkinsons disease, other neurodegenerative diseases (mainly in progressive supranuclear palsy), and in secondary parkinsonian syndromes connected with multi-infarct encephalopathy, normal pressure hydrocephalus and in focal lesions of frontal lobes (together with other manifestations of frontal gait disorder see above). Disordered gait initiation is the principal sign of a nosological entity known as pure akinesia (gait ignition failure). In addition to start hesitation, festination and gait freezing, these patients may suffer from disequilibrium and falls. They may also have dysarthria and micrographia, but do not usually show rigidity, tremor or dementia. Treatment for disordered gait initiation is no easy task, so that many patients find their only help lies in performing diverse sensory and motor tricks. Dopaminergic medication may improve this symptom, mainly in those cases of Parkinsons disease where start hesitation and freezing appear in the off state and disappear in the on state. However, freezing is often also expressed in the on state and fails to respond to dopaminergic therapy (on-freezing). Gait and balance examination Simple observation remains the essential approach, the gold standard of gait investigation, from which an experienced observer can extract crucial information for differential diagnosis of the particular gait and balance problem. History Symptoms of balance and gait disorders often tend to be non-specific. As a rule, the patient complains of slowed-down walking, uncertainty in space, a perception of instability when standing or walking, or of falls. While gait or balance problems can (and should) be verified on examination, falls may not be observed during examination, and therefore finding more

about the circumstances is essential. Assessment On examination, the basic features of posture and gait are scrutinised to reveal signs of pathological involvement (see table 1). The comprehensive gait and balance evaluation comprises observation of spontaneous postural and locomotion patterns at rest (while standing) and while walking, followed by maneuvers designed to assess the overall execution of the required movement, muscular strength, postural reflexes, signs of lateral instability etc. The phenomenological classification of gait disorders is based on the integration of observed clinical characteristics with known anatomic and etiologic mechanisms: Muscular weakness can usually be detected during neurological examination of the lower limbs, and tends to be brought out on execution of functional changes of position sitting down, arising from a chair, standing and, in particular, walking. Base width is studied in spontaneous standing and in walking, when we take note of the base width changes and any possible deviations from the straight path suggesting disturbed lateral stability. Maneuvers while standing (feet close together, Romberg test), will help to reveal minor disturbances of lateral stability. Antero-posterior stability disturbance can be diagnosed with the push- and pull- (shoulder tug) tests (sudden posterior or anterior displacement produced by pushing or pulling on the shoulders). The gait parameters, such as stride length, cadence (number of strides per minute), gait speed and regularity, and fluidity of walking movements can all be ascertained by observing the subjects normal or usual gait. After commands to start walking, change direction and stop, we explore gait initiation, maintenance and adaptation to changes in environmental conditions (surface changes, narrow passages etc.) or to intentional gait changes. Maneuvers while walking (walking with closed eyes, walking on the heels and tiptoes, walking backwards etc.) will expose lateral instability, disorders of proprioception, distal muscle weakness and other abnormal gait patterns.

- table 1 A Neurological examination including assessment of the configuration of lower extremities, their attitude, range of active and passive movement, muscle tone and strength. B Getting up from lying to sitting, from sitting to standing position looking for possible muscular weakness, disorder of motor coordination. C Spontaneous stance

posture of trunk and extremities

base width (distance between the two feet)

D Maneuvers while standing

stance with feet close together, eyes open Romberg test (the same as above, with eyes closed) postural response to external stimuli in the antero-posterior direction sudden posterior displacement produced by pulling (or pushing) on the shoulders (pull-test, shoulder-tug test or push-test) (caution ensure protection against the risk of falling)

E Spontaneous gait (to be examined in the corridor or some other space offering at least 10 m of free space)

base width, stride length, cadence, fluidity of movements, deviations from given direction starting and stopping, turning on the spot and while walking, spontaneously and in response to commands walking through a constricted passage (doorway), clearing and avoiding obstacles

F Maneuvers while walking

tandem gait (feet placed toe-to-heel) walking with eyes closed (Romberg test while walking) walking backwards