Review

Neurological gait disorders in elderly people: clinical approach and classication

Anke H Snijders, Bart P van de Warrenburg, Nir Giladi, Bastiaan R Bloem

Gait disorders are common and often devastating companions of ageing, leading to reductions in quality of life and increased mortality. Here, we present a clinically oriented approach to neurological gait disorders in the elderly population. We also draw attention to several exciting scientic developments in this specialty. Our rst focus is on the complex and typically multifactorial pathophysiology underlying geriatric gait disorders. An important new insight is the recognition of gait as a complex higher order form of motor behaviour, with prominent and varied eects of mental processes. Another relevant message is that gait disorders are not an unpreventable consequence of ageing, but implicate the presence of underlying diseases that warrant specic diagnostic tests. We next discuss the core clinical features of common geriatric gait disorders and review some bedside tests to assess gait and balance. We conclude by proposing a practical three-step approach to categorise gait disorders and we present a simplied classication system based on clinical signs and symptoms.

Lancet Neurol 2007; 6: 6374 Department of Neurology and Parkinson Center Nijmegen, Radboud University Nijmegen Medical Centre, Nijmegen, Netherlands (A H Snijders MD, B P van de Warrenburg MD, B R Bloem MD); and Movement Disorders Unit, Parkinson Center, Department of Neurology, Tel-Aviv Sourasky Medical Center, Sackler School of Medicine, Tel-Aviv University, Tel-Aviv, Israel (N Giladi MD) Correspondence to: Dr Bastiaan R Bloem, Medical Director, Parkinson Center Nijmegen (ParC), Department of Neurology, Radboud University Nijmegen Medical Centre, PO Box 9101, 6500 HB Nijmegen, Netherlands b.bloem@neuro.umcn.nl

Introduction
Gait disorders are common in elderly populations and their prevalence increases with age. At the age of 60 years, 85% of people have a normal gait, but at the age of 85 years or older this proportion has dropped to 18%.1,2 Gait disorders have devastating consequences. Perhaps the most notorious corollary is falling, which is often caused by an underlying gait problem. Injuries caused by accidental falls range from relatively innocent bruises to major fractures or head trauma. Another important consequence is reduced mobility, which leads to loss of independence. This immobility is often compounded by a fear of falling, which further immobilises patients and aects their quality of life.3 Importantly, gait disturbances are also a marker for future development of cardiovascular disease and dementia.46 These associations suggest that gait disturbanceseven when they present in isolation can reect an early, preclinical, underlying cerebrovascular or neurodegenerative disease. Finally, gait disorders are associated with reduced survival, which can be attributed to a combination of fatal falls, reduced cardiovascular tness, and death from underlying disease.79 Elderly patients regularly present with complex gait disorders, with concurrent contributions from multiple causal factors.10 To describe specic gait disorders accurately is often dicult. Here, we provide a practical approach that may support clinicians in their everyday management of neurological gait disorders in elderly people. We briey address the pathophysiology of gait disorders and discuss the eects of mental function and normal ageing on gait. We conclude by describing a practical clinical approach and simplied classication system to dierentiate gait disorders in everyday practice, based on clinically discernable gait patterns. Treatments for geriatric gait disorders are not reviewed.

initiation and maintenance of rhythmic stepping; balance; and ability to adapt to the environment. Dysfunction in any of these systems can disturb gait. Most ambulatory problems in elderly people are caused by concurrent dysfunction of multiple systems. Virtually all levels of the nervous system are needed for normal gait.1114 Recent studies have drawn attention to pattern generators in the spinal cord that generate rhythmic stepping.15 Neuroimaging studies point to the role of the frontal cortex in controlling gait and in coordinating automatic and voluntary movements.16 One interesting study used functional MRI to identify patterns of brain activity while participants imagined standing, walking, or running while lying in the scanner.17 With running (automated locomotion), spinal pattern generators and the cerebellum were involved, whereas slow walking evoked activity in the parahippocampal region, presumably because spatial navigation becomes more important.

Gait and mental function

Walking is traditionally seen as an automatic motor task that requires little, if any, higher mental functions. In the past decade, new insights have drawn attention to the importance of cognition in daily walking.18 Normal walking requires strategic planning of the best route, as well as continuous interaction with the environment and with internal factors. Failing to understand the signicance of an obstacle, choosing an inappropriate route, or misinterpreting ones own physical abilities can all lead to falls. The safety and ecacy of normal walking rely not only on sensorimotor systems, but also critically depend on the interaction between the executive control dimension (integration and decision of action) with the cognitive dimension (eg, navigation, visuospatial perception, or attention) and the aective dimension (mood, cautiousness, and risk-taking). A common situation where such an integration is challenged is when people must walk while performing one or more secondary tasks. Lundin-Olsson and colleagues19 were
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Pathophysiology of gait disorders

Normal gait requires a delicate balance between various interacting neuronal systems (gure 1) and consists of three primary components: locomotion, including
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Feedback: Vestibular system Visual system Sensory nerves

Support: Cardiovascular system Bones Joints Ligaments Feet

Execution: Frontal cortex planning Basal ganglia initiation, automatisation Brainstem integration Cerebellum coordination, adaptation Spinal cord spinal pattern generators Nerve roots Peripheral nerves (both motor and sensory) Muscles

circumstances, young healthy people begin to neglect the secondary task and lend more priority to walking safely. This prudent posture-rst strategy is diminished in elderly people,20 and failure to prioritise gait under dicult circumstances is weakly associated with falls.25 Research has shown that frontal executive functions are especially important for maintaining walking stability. Dysexecutive functions can be the primary cause of falls in a group of idiopathic elderly fallers.26,27 The involvement of cognitive control in normal gait could explain why falls are so common in patients with dementia and why demented patients are so vulnerable to dual task performance while walking.28,29 Interestingly, patients with Parkinsons disease whose phenotype is dominated by postural instability and gait disorder have a much greater risk of cognitive decline and dementia than do patients with tremor-dominant Parkinsons disease.30,31 Additionally, adverse eects on cognitive gait control might explain the high incidence of falls and injuries in individuals taking psychoactive medication.32 Aective disorders are also associated with gait problems in elderly people. For example, depression, anxiety, and particularly fear of falling are common consequences of unsecured gait and falls among elderly people.3335 In view of these complex interactions between walking, cognition, and mood, new interventional strategies should be developed to promote secured mobility of elderly people by improving attention, dual task performance, mood, and executive functions.36

Eect of normal ageing on locomotion and gait

Ageing is typically equated with abnormalities, and this association certainly applies to gait. Many older people accept their gait diculty as being normal for their age and their doctors often support them in this view. But are gait disorders truly an inevitable consequence of ageing itself? This question is illustrated by the evolving concepts around the so-called senile gait disorder: the slow, shuing, and cautious walking pattern commonly seen in older age. Because clinical examination reveals no apparent cause, normal ageing was long held responsible for this disorder. However, recent ndings have challenged this concept. Up to 20% of very old individuals walk normally, hence gait disorders are certainly not an inevitable feature of old age.1 This nding indirectly implies that those who have gait impairment in fact suer from underlying disease. This assumption is lent support by the fact that individuals with a senile gait disorder have an increased risk of becoming demented5 and have reduced survival compared with age-matched individuals who walk normally at a high age (gure 2).4 These ndings suggest that senile gait disorders are an early manifestation of underlying pathology, most notably subtle white-matter changes, vestibular dysfunction, visual changes, or oculomotor changes.3743 Such
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Figure 1: Levels of the central and peripheral nervous system required for normal gait

the rst to note the signicance of a failure to maintain a conversation while walking (stop walking while talking) as a marker for future falls. The ability to maintain normal walking while performing a secondary task (dual task paradigm) has become the classic way to assess the interaction between cognition and gait.20 In elderly people, this dual task ability deteriorates because central resources decline, secondary to subclinical disease processes or medication. This deterioration leads to a mismatch between the limited personal resources of elderly people and the complexity of the demand (the combined walking and secondary task). As a consequence, elderly people slow down or have an increased stride variability (suggesting reduced automaticity) while performing a secondary task during walking.21 Gait becomes less secure and the risk of falling increases. In patients with overt disease, such as stroke or Parkinsons disease, gait deteriorates even more during dual tasking.2224 Another form of dual task impairment is when elderly people fail to get their priorities right.25 Under complex
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Cumulative survival

disorders might alter gait directly, but may also act in an indirect way by causing a subjective sensation of instability and insecurity, forcing individuals to purposely adopt a more cautious gait. The message for clinicians is that gait disorders in elderly people are not merely the unpreventable consequence of ageing. Instead, these gait disturbances more likely result from the increased prevalence and severity of (clinical or subclinical) diseases with increasing age (gure 3). For this reason, we suggest abandoning the term senile gait as a specic gait category.

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Dierentiation of gait disorders

Only few studies describe the distribution of geriatric gait disorders. Obviously, the spectrum of underlying illnesses will depend on the population under consideration and the assessment technique. Within a relatively healthy subgroup of 153 community residents aged 88 years and older, about 61% reported distinct diseases as a cause of gait impairment.1 Non-neurological disorders were the leading causes of gait impairment, in particular joint pain (52 of 87 people), whereas many others had multiple causes for their gait impairment. Stroke was the most common neurological cause. In another study of 120 elderly outpatients seen in a neurological reference practice, the most common causes for gait disorders were sensory ataxia (18%), myelopathy (17%), multiple strokes (15%), and parkinsonism (12%).2 Largely the same causes dominated in a series of 493 neurological inpatients, 60% of whom had a gait disorder.44

04

02

Normal gait Senile gait disorder Gait disorder due to disease

00 0 1 2 3 Survival (years) 4 5 6

Figure 2: Kaplan-Meier curves showing cumulative survival due to all causes of death Results are shown for patients with a completely normal gait (n=25), those with senile gait disorders (n=14), and those with gait disorders due to known disease (n=87). Mean age was 90 years in all groups (range 8797 years). Survival was dierent between the groups (log-rank p=001). All-cause-mortality risk was increased in people with senile gait disorders compared with those with a normal gait (RR=28; 95% CI 1173, p = 003) and was similar to those with gait disorders due to known disease (RR=12; 95% CI 0625, p=06). Mortality due to cardiovascular disease also diered among the three groups, with a two-fold increased risk of cardiovascular death in people with senile gait disorders compared with those with normal gait (data not shown). Reproduced with permission from Blackwell Publishing.4

Recognition of specic gait disorders

Table 1 summarises the main features of the weak, spastic, and ataxic gait disorders (for reviews, see references 13,15,45,46). Because these categories usually cause little diculty in clinical practice, we focus next on the remaining gait disorders.

Gait disorders

Falls Injuries

Mortality

Age-related pathology

Fear of falling Morbidity (cardiovascular disease, cognitive decline)

Hypokinetic-rigid gait disorders

Diseases of the basal ganglia and the frontal lobe mostly present with a hypokinetic-rigid gait. However, frontal pathology can also cause a higher level gait disorder in which truncal imbalance and frequent falls are a key feature. Other associated features of this higher level gait disorder are depression, frontal release signs, and impaired executive function.47 Specic features of gait, posture, or balance can assist in the dierential diagnosis of these dierent disorders (table 2). A characteristic feature of hypokinetic-rigid gait is shuing with a reduced step height, often with a reduced stride length, leading to slowness of gait. The base of support is typically normal in Parkinsons disease, but is often widened in patients with atypical parkinsonism. Other characteristic features include reduced arm swing (asymmetrical in Parkinsons disease, but more symmetrical in atypical parkinsonism), which can present in isolation and
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Ageing Immobility

Reduced quality of life

Figure 3: Indirect association between ageing and geriatric gait disorders This association occurs mainly, if not exclusively, via the intermediate of age-related pathology. Adverse consequences of gait disorders in elderly people include reduced quality of life and, eventually, reduced survival.

precede the onset of other hypokinetic-rigid features by many years. Turning movements become slow and are executed en bloc. Festination is a feature of more advanced disease, where patients take rapid small steps in an attempt to maintain the feet beneath the forward moving trunk. Poorly mobile patients with advanced disease can sometimes respond quickly to environmental eventstypically emotional or threatening circumstancesand move unexpectedly well (kinesia paradoxica). Apparently, patients with Parkinsons disease
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Elements of the clinically based diagnostic work-up Main features of gait Antalgic gait Paretic/hypotonic gait Reduced stance phase on aected limb Limping High steppage Dropping foot Waddling Circumduction Intermittent abduction of ipsilateral arm with each step Foot dragging: audible scung toe Scissoring; bilateral circumduction Deviation to one side Staggering, wide based Staggering, wide based Extra movements that aect gait Aggravated by eye closure Positive Unterberger test Aggravated by eye closure Not aggravated by eye closure Can be task-specic (eg, dystonic gait) Trendelenburgs sign Specic gait or balance test* Associated symptoms and signs Pain Limited range of movements Lower motor neuron features (eg, weakness, atrophy, low to absent tendon reexes) Pyramidal syndrome Anterior-medial side of the shoe sole worn out

Spastic gait

Vestibular gait Sensory ataxic gait Cerebellar ataxic gait Dyskinetic gait Hypokinetic-rigid gait Cautious gait Higher level gait disorder

Vestibular features (eg, nystagmus, abnormal tilting test) Disturbed proprioception Cerebellar ataxia (eg, dysarthria, hypermetria, nystagmus) Features of dystonia, chorea, myoclonus or tics Hypokinetic-rigid features (eg, bradykinesia, resting tremor) Postural instability (mild to moderate) Excessive fear of falling

Shuing (slow speed, short stride, rigidity, reduced step height) Improves with external cues Hesitation and freezing Aggravation by secondary task Walking on ice; slow, wide base, short steps Striking improvement with external support Severe balance impairment (no rescue reactions with the pull test; falling like a log) Inadequate synergies Inappropriate or bizarre foot placement Crossing of the legs Leaning into wrong direction when turning or standing Variable performance (inuenced by environment and emotion) Hesitation and freezing (ignition failure) Abnormal interaction with environment (eg, trouble adapting with walking aids; no benet from cues) Sometimes better able to perform cycling leg movements while recumbent (gait apraxia)

Frontal release signs Executive dysfunction Depression Frequent falls

A clinically based diagnosis for each gait syndrome can usually be reached with a systematic approach: rst, a description of the core gait features; next, the use of specic gait or balance tests; and nally, a search for associated symptoms and signs. *Simple diagnostic tests that can be done at the bedside include: providing external support (eg, a walking aid); imposing secondary tasks while walking (dual or multiple tasking); eye closure; walking backwards; inuence of external cues (visual; auditory; or mental). Peripheral neuropathy and radiculopathy are among the most common causes of gait diculties in the elderly.

Table 1: Main features of specic gait syndromes

can use such external triggers to engage alternative motor circuits and thereby bypass the defective basal ganglia circuitry.48 Hypokinetic-rigid gait disorders can be classied according to the underlying anatomical substrate. One main group involves lesions within the basal ganglia and their connections to the frontal cortex, brainstem, or both. Pathological changes in the frontal lobe itself can also contribute to a hypokinetic-rigid gait. There are no well-dened clinical markers for frontal-lobe contribution, but suggestive features include a wide-based or variable stance and truncal imbalance. Some would also include gait apraxia here, often dened as a marked discrepancy between the severity of the gait disorder and the ability to perform other leg movements, such as cycling in the air while lying down. Associated features include urinary urgency and cognitive changes and a poor response to external cues. Hypokinetic-rigid gait disorders can also be classied according to the underlying disease process. One important group includes neurodegenerative disorders such as Parkinsons disease and various forms of atypical parkinsonism (eg, multiple system atrophy or progressive supranuclear palsy). Another common group includes
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underlying cerebrovascular disease. Gait disorders with a mixed hypokinetic-rigid and ataxic character are a common occurrence in patients with subcortical arteriosclerotic encephalopathy.49 A less common feature of cerebrovascular disease is lower body parkinsonism, a predominance of symptoms and signs in the legs, with a relatively preserved arm swing and little bradykinesia of the hands.50,51 The term lower body parkinsonism is a useful descriptive term in clinical practice because it refers to a recognisable phenotype that is often associated with underlying cerebrovascular disease, including whitematter changes and lacunar infarcts in the basal ganglia. However, lower-body parkinsonism is not synonymous with vascular parkinsonism. Occasional patients can present with a clinical presentation resembling Parkinsons disease (with upper-limb involvement) or even progressive supranuclear palsy. Hypokinetic-rigid gait disorders due to cerebrovascular disease can develop acutely or with an insidious onset.50 The acute syndrome mainly involves infarcts in the putamen, globus pallidus, or thalamus, whereas the gradual form is associated with diuse white-matter changes. A third type of underlying disease process is ventricular widening, as occurs in patients with normal pressure
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Main anatomical substrate Parkinsons disease (PD) Substantia nigra

Disease process Neurodegenerative

Characteristic features Narrow-based gait Asymmetrical presentation Stooped posture Early freezing and falls rare Early phase like PD gait Later phase more wide-based Pisa syndrome Antecollis Vertical falls (due to syncope) Wide-based gait Freezing common Erect posture, but with retrocollis Early/spontaneous/backward falls Motor recklessness Frequent and severe injuries Asymmetrical presentationeg, unilateral leg apraxia, dystonia, or myoclonus Later: wide-based gait, freezing, shuing Like PD gait More symmetric Small steps Wide-based gait Start hesitation Variable timing and amplitude of steps Lower body parkinsonism More wide based Less stooped Relatively preserved arm swing Lower body parkinsonism Freezing/severe gait akinesia Severe disequilibrium Drifting to one side

Associated features Good response to levodopa Resting tremor hand(s) Cerebellar ataxia Autonomic features Pyramidal signs

Multiple system atrophy, parkinsonian type

Basal ganglia Cerebellum Pyramidal tracts Autonomic nervous system Diuse brainstem pathology

Neurodegenerative

Progressive supranuclear palsy

Neurodegenerative

Vertical gaze palsy Pseudobulbar palsy Frontal dementia Applause sign

Corticobasal degeneration

Basal ganglia Cortex Basal ganglia Cortex Subcortical white matter

Neurodegenerative

Apraxia Alien limb Cortical sensory loss Dementia Fluctuations Visual hallucinations Urinary incontinence Cognitive decline Stepwise progression Urinary incontinence Cognitive decline Stepwise progression

Dementia with Lewy bodies

Neurodegenerative

Subcortical arteriosclerotic encephalopathy

Vascular

Vascular parkinsonism

Diuse white matter Basal ganglia

Vascular

Strategic vascular lesion

Putamen Globus pallidus Thalamus Dorsal mesencephalon

Vascular

Normal pressure hydrocephalus

Frontostriatal (periventricular) Ventricular widening Wide-based gait, freezing, gait apraxia Truncal imbalance Preserved arm swing Mild gait impairment, rarely freezing Preserved postural reexes Pisa syndrome

Urinary incontinence Cognitive decline Upper limb tremor Symmetrical presentation

Drug-induced parkinsonism Basal ganglia (postsynaptic)

Table 2: Dierential diagnosis of parkinsonian disorders, based on specic features of gait, balance, or posture

hydrocephalus. Whether normal pressure hydrocephalus truly exists as a separate entity with its own unique pathophysiology is unknown. Typically, the disorder presents with a recognisable triad of hypokinetic-rigid gait impairment, urinary incontinence, and (frontal) dementia. Gait is characterised by marked slowing and small shuing steps and regular freezing, but usually with largely preserved arm movements.52,53 Ataxic elements are also seen, including a broad stance width and an increased variability in timing and amplitude of the steps. The pathophysiology has not been claried, but may relate to an excessive volume of intraventricular cerebrospinal uid that is not explained by cerebral atrophy. The classic radiological appearance includes widened lateral ventricles (especially aecting the anterior horns), often accompanied by periventricular white-matter lesions. An unresolved question (yet one with direct implications for treatment) is whether these periventricular white-matter lesions are the cause or consequence of ventricular widening.54
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Clinical examination alone cannot always disentangle these dierent anatomical and pathophysiological causes of hypokinetic-rigid gait disorders, especially in early stages where overlap is substantial. In such patients, it is best to refrain from confusing terminology. It initially suces to classify the patient as having a hypokineticrigid gait disorder and to base a more denitive anatomical or aetiological diagnosis on ancillary investigations (MRI) and sometimes the response to treatment (eg, a trial of levodopa).

Cautious and careless gaits

Typically, people with a cautious gait move slowly, with a wide base and short strides, with little movement of the trunk, while the knees and elbows are bent. Cautious gait is common in elderly people and originates in part from fear of falling, which is sometimes present to the degree of panic.33 There are two main subgroups. In the rst, fear of falling is excessive relative to the degree of actual instability. In fact, balance can be fully normal, as in people with a
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pathological fear of falling (fall phobia) caused by a single fall. In these individuals, the remaining neurological examination is completely normal, and provision of external support or reassurance can substantially improve gait. In the second subgroup, fear of falling is justied by a recent history of recurrent falls or by a self-perceived instability due to overt or sometimes otherwise subclinical underlying disease. These individuals might show mild freezing of gait, occurring mainly with gait initiation and while turning.33 Neurological examination can further reveal mild hypokinetic-rigid signs, disturbed postural responses, and frontal release signs. With time, these patients may develop other subcortical or frontal disturbances, or progress to having a more disabling gait impairment. A therapeutic levodopa trial is justiable, but it has been our clinical impression that after a short positive response that could represent a placebo eect, patients with cautious gait no longer improve. Fear has to be treated medically or behaviourally. Careless gait is the counterpart of the cautious gait. Some patients seem overly condent and walk inappropriately fast, perhaps because of lack of insight or frontal-lobe disinhibition. Notorious examples are patients with progressive supranuclear palsy and Huntingtons disease who typically move too abruptly despite a severe balance decit and who seem unable to properly judge the risk of their actions. This motor recklessness probably underlies the high incidence of fall-related injuries in these disorders.55,56 A similar recklessness contributes to falls and injuries in ageing disorders such as Alzheimers disease. Confusion and delirium can also contribute to a careless gait. A recent study showed that gait velocity should be judged in the context of the patients physical capabilities. Thus, although frail elderly patients with dementia walked slowly, they still walked relatively too fast, given their overall degree of physical impairment, which should have warranted an even much slower gait.57 For some cognitively impaired patients, restriction of unsupervised physical activities is an ultimate measure to prevent wandering behaviour and to reduce injurious falls.58

patients are caught unprepared.59 An example is freezing of gait, where patients suddenly experience a characteristic feeling as if the feet become glued to the oor. Various terms have been used in dierent contexts, including gait ignition failure or slipping clutch phenomenon. We propose to use the term freezing of gait to describe all gait initiation disturbances. Although freezing of gait is most often observed when initiating gait, it also occurs when walking through a narrow passage, during turning, while executing a secondary task (eg, responding to a question), or upon reaching a destination. In severely aected patients, it can occur seemingly spontaneously while walking in open terrain. Three dierent clinical presentations are recognised: shuing with small steps; trembling in place, while attempting to overcome the block; or being fully unable to start or continue walking, which is relatively rare.59 Freezing of gait can present largely in isolation, as occurs in primary progressive freezing gait. This usually results from frontal lobe damage, irrespective of the specic disease process.49 However, freezing of gait is mostly seen as part of a hypokinetic-rigid syndrome, including Parkinsons disease and various forms of atypical parkinsonism.60,61

Dyskinetic gait disorders

The term dyskinesias includes all involuntary movements or postureseg, chorea or dystonia. Presence of such involuntary movements during walking suggests a dyskinetic gait. A well-known example is the gait in patients with postanoxic encephalopathy, in which the positive and negative action myoclonus (Lance-Adams syndrome) produces a bouncing gait and stance. Dyskinesias can contribute to falls by causing excessive trunk movements beyond the limits of stability, as occurs in patients with Parkinsons disease with medicationinduced dyskinesias62 or in patients with Huntingtons disease.56 Note that dyskinesias might be absent during clinical examination because of their uctuating character or because patients suppress them intentionally. Cognitive distractions can help to elicit the involuntary movements during examination. Patients with dystonia require specic attention because their gait or balance impairment can be task-specic. For example, patients may have severe gait impairment due to leg dystonia, but can easily walk backwards or even run. This is easily misinterpreted as a psychogenic sign. Examples of gait dystonia include early onset Parkinsons disease presenting with a foot dystonia while walking, or patients with idiopathic torsion dystonia who can present with unusual gait patterns. Other forms of gait dystonia include retrocollis in patients with progressive supranuclear palsy, antecollis or a Pisa syndrome (severe and persistent lateroexion of the trunk) in patients with multiple system atrophy, and an asymmetrical arm or leg dystonia during walking in patients with corticobasal degeneration. Many dystonic patients tend to walk on their toes (cock walk). Axial forms of dystonia, including
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Fluctuating or episodic gait disorders

A curious feature of some gait disturbances is their uctuating or frank episodic nature. The specic provoking factor can dierentiate these gait disturbances. Some gait disorders uctuate more or less predictably because of exercise intolerance or pain. In elderly people, walking diculties after exercise are often due to fatigue (cardiopulmonary or neuromuscular disease), but might also indicate vascular or neurogenic claudication. Psychogenic gait disorders can also present with an episodic character, for example an aggravation when bystanders are present. Other gait disorders are truly episodic. The sudden and largely unpredictable nature of these episodes is incapacitating, commonly leading to falls because
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dystonic scoliosis, hyperlordosis, or torticollis can also interfere with walking and standing. This is particularly true if extensor or exor spasms are present.

Panel: Features suggestive of a psychogenic gait disturbance Suggestive features Incongruous with known gait disorders Bizarre presentation Variable, inconsistent pattern Non-physiological pattern Rare falls or injuries* Abrupt onset Extreme slowness Unusual or uneconomic posture Exaggerated eort Sudden buckling of the knees Associated features Incongruous aect (belle indierence) Secondary gain Prior history of psychiatric disease
*Striking exemptions with sometimes severe injuries have been described.65 Rare, but diagnostic yield is higher with an intensive interview.

Psychogenic gait disorders

Although suspicion of psychogenic gait disorders is highest in younger patients, they can occur in elderly patients. Psychogenic gait is often not compatible with known gait patterns and they can take unusual forms (panel).6365 Falls and injuries are thought to be rare in patients with a psychogenic gait, but we encountered one such patient who sustained severe injuries (epidural haematomas and a skull base fracture).65 Care must be taken not to miss underlying organic disease, in particular frontal-lobe dysfunction. The dierential diagnosis includes organic gait disorders that can mimic psychogenic gait disturbances; examples include choreatic gait in Huntingtons disease, task-specic dystonic gait, episodic weakness in myasthenia gravis, and cataplexy. Gait in sti person syndrome can also look strange; gait abnormalities typically aggravate when patients are instructed to hurry up.66

Comments

Gait disorders and falls caused by medication

Gait disorders and falls in elderly people are commonly associated with adverse eects of drugs (table 3).32,6776 The precise underlying pathophysiological mechanism is unclear in many cases. Commonly implicated factors include sedation, orthostatic hypotension, behavioural abnormalities, extrapyramidal side-eects, or ataxia. However, there can also be confouding by indicationie, falls that are caused by the underlying disorder for which the drugs were prescribed in the rst place. Thus, falls or a disturbed gait in patients taking anti-diabetic medication might simply be caused by an underlying diabetic polyneuropathy. Polypharmacy is particularly associated with falls, but only if a patient daily takes at least one drug with an established risk of increasing falls.77 A critical review of medication is therefore important in elderly people. For example, a recent randomised controlled trial showed that when a pharmacist reduced the number of drugs in elderly care-home residents, the number of falls was reduced by 40%.78

Antipsychotics67,68 Antidepressants68,69 Anticonvulsants68,70 Antiparkinson drugs71

Occurs with both typical and atypical antipsychotics Occurs with both SSRIs and tricyclic antidepressants Occurs with both older anti-epileptic drugs (eg, phenobarbital) and newer anti-epileptic drugs (eg, lamotrigine), but possibly less with the newer drugs Occurs with all classes of antiparkinson drugs. Underlying mechanism is complex, but mainly includes excessive dyskinesias, orthostatic hypotension, and behavioural abnormalities Occurs with both short and long-acting benzodiazepines. Newer Z-compound hypnotics such as zopiclone are thought to be safer Occurs with opiates, NSAIDs, and paracetamol. Some studies nd stronger eects of opiates, others of NSAIDs Diuretics, beta-blockers, ACE inhibitors, and nitrates Evidence is stronger for inpatients than for outpatients, probably due to a stronger eect of orthostatic hypotension after prolonged bed-rest Both sedation and orthostatic hypotension may contribute Perhaps via underlying pathologyeg, diabetic polyneuropathy or cerebrovascular disease .. Quinine and derivates

Benzodiazepines/ other hypnotics68,72 Analgesics68,73,74 Antihypertensive74

Anticholinergics68,75 Antidiabetics76 Anti-arrhythmics74 Quinine68

SSRIs=selective serotonin reuptake inhibitors. NSAID=non-steroidal anti-inammatory drug. ACE=angiotensinconverting enzyme.

Assessment of gait disorders

Assessment includes a full physical and neurological examination and a systematic gait assessment. Use of standard rating scales, such as the Tinetti mobility index79 or gait and balance scale,80 help to score all dierent elements of gait and balance. Most examination rooms are too small, so it is often necessary to examine the patients while walking in the corridor. Simple undisturbed gait can be informative, but additional abnormalities come to light when gait is challenged. For example, walking with eyes closed might provoke or aggravate ataxia in patients with a sensory neuropathy, or cause a consistent deviation to one side in patients with unilateral
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Table 3: Drugs with adverse eects on gait, posture, and balance

vestibular loss. Patients suspected of having freezing of gait often walk normally in the examination room because excitement associated with the doctors visit can suppress this sign. In such patients, careful questioning supported by validated questionnaires81 is important. Additionally, walking in tight quarters, while turning or when doing secondary tasks may provoke freezing of gait. Next to challenging gait, observation of whether patients can improve their gaiteg, by beneting from walking aids or provision of external supportis equally instructive. Seemingly incapacitated patients with a
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cautious gait can show striking improvements in gait when provided with external support while walking. Similarly, providing individuals with external visual, auditory, or mental cues can help to reduce freezing of gait.36 By contrast, patients with a higher-level gait disorder typically do not benet from external cues and have troubles adapting with walking aids. Such patients are sometimes better able to perform cycling leg movements while lying recumbent, suggesting that their loss of control over leg movements is task-specic (gait apraxia). As mentioned earlier, this task-specicity can also be seen in patients with dystonia. The pull test (or retropulsion test) is commonly used to probe the reactive and defensive balance reactions.82,83 Many variants exist, but most commonly the investigator, standing behind the patient, suddenly pulls the patients shoulders. The test is typically used to score the severity of postural instability. However, failure to initiate a corrective stepdue to freezing of gaitalso produces an abnormal test result. We usually deliver one shoulder pull without specic prior warning, as this best mimics daily life circumstances where falls are usually unexpected events. We then repeat the test several times and regard failure to habituate to the test as another sign of balance impairment. A recently introduced variant is the push and release test, which rates the postural response to a sudden release of a patient pressing backward on an examiners hands placed on the subjects back. An advantage is that this test allows examiners to apply more consistent perturbation forces to the patients than with the conventional pull test, and the outcome seems to correlate better with self-reported falls.84 Timed tests can be used to quantify gait velocity (eg, to assess the eect of treatment), but these do not accommodate the quality of gait. A commonly used test is the timed up and go test, where patients are observed and timed while rising from a high chair with arms, walking 3 m, turning around, walking back, and sitting down again.85 Cognition and aect should be routinely examined in elderly patients with gait problems, with emphasis on frontal cognitive dysfunction. Fear of falling can be assessed directly or, preferably, by using a validated questionnaire.3 Finally, it is important to assess footwear and vision (with and without correction), as these contribute to gait disorders and falls in the elderly.86,87
Examples Hierarchical Lower level Intermediate level Higher level Frontal gait Cerebellar gait Vascular Neurodegenerative See table 1 Drawbacks

A relatively new method is physiological analysis of gait, by use of a treadmill and quantitative outcome measures: kinematics (joint motion), kinetics (reactive forces), and dynamic electromyography. An important disadvantage is that gait is assessed under constrained and highly unnatural circumstances, leading to lack of ecological validity.88 Less complex systems can be applied in freely moving individuals. Common tools are ambulatory goniometers or accelerometers, to quantify movement of the limbs or trunk,89 and shoes with pressure-sensitive insoles90,91 or a carpet with pressure-sensitive sensors92 to measure subtle changes in locomotion rhythmicity, variability, or leftright synchronisation. Although this type of gait analysis better approaches real-life situations, whether the currently available equipment provides any clinically relevant extra information is unknown. We therefore feel that it is currently not worth sending elderly patients for a quantitative study of gait in a sophisticated gait laboratory. Possible exceptions include a preoperative assessment to guide the surgeon before an orthopaedic intervention, detailed electromyography studies in spastic or dystonic patients to ne-tune subsequent treatments with botulinum toxin or selective surgical denervation, and kinematic gait analyses to assist rehabilitation specialists in their choice for specic segmental orthoses or adjusted footwear.9397 Physiological gait analysis is a very useful technique for scientic purposes.

Clinical approach and classication of gait disorders

We conclude our contribution by discussing a new, practically oriented approach to gait disorders, as well as a simplied modication of the classication originally proposed by Nutt and colleagues.98 A broadly accepted classication system would assist health professionals when they communicate about patients with gait disorders. Research will also benet from a good classication system, for example to ascertain that properly diagnosed patients and homogeneous groups are included in trials or gait experiments. Dierent types of gait classications currently exist, with dierent and partly overlapping starting points (hierarchical, anatomical, aetiological, or phenomenological). Every classication system has inconsistencies (table 4). We propose a practical three-step

Term higher level often abused as basket term for any poorly understood gait disorders Subdivisions of higher level gait disorders dicult to use in clinical practice Overlap in symptoms between middle and higher level gait disorders Dierent anatomical lesions may present with similar gait patterns Any given anatomical lesion may present with dierent gait patterns Ancillary studies or post-mortem examination often required to make denitive diagnosis Pathophysiology not taken into account

Anatomical Aetiological Phenomenological

Table 4: Drawbacks of currently available gait classication systems

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approach that begins with a gait classication based on clinical phenomenology, as observed in the consultation room (step 1 in gure 4). This rst step includes three elements: the core features of a patients gait; additional clinically based gait and balance tests; and associated neurological or physical abnormalities. These three elements are all listed systematically in table 1 for each of the main clinically discernable gait patterns. For example, patients with an ataxic gait typically have a wide-based, staggering gait (core clinical feature). By itself, this core feature can implicate either sensory ataxia or cerebellar ataxia, and this distinction can be made with additional gait and balance tests, such as the eect of eye closure (aggravates the gait impairment much more in sensory ataxia compared with cerebellar ataxia). The distinction between both types of ataxic gait disorders can be corroborated by a search for associated neurological or physical abnormalities: hypermetria, nystagmus, and cerebellar dysarthria suggest that the wide-based gait was in fact caused by cerebellar ataxia, whereas disturbed proprioception would suggest sensory ataxia. Taken together, the three elements of this rst step thus lead to a clinically based classication, determined by recognisable gait features (syndromes or possible gait disorders), as listed in the left column of table 1. Note that this rst step of the classication avoids anatomical, pathophysiological, and aetiological terminology because it is solely based on clinical impressions obtained in the examination room. For that reason, our clinical classication also avoids a distinct categorisation of low level and middle level gait disorders as proposed in the original Nutt classication98 because this hierarchical distinction formally requires ancillary studies to demonstrate the site of the lesion. Also, symptoms can overlap between middle level and higher level gait disorders. We propose to abandon the anatomically based term frontal gait disorders, as these may present with at least three dierent phenotypes: a shuing hypokinetic-rigid gait; a wide-based ataxic pattern; and an episodic gait disorder, dominated by freezing episodes. Furthermore, the frontal phenotype can be seen in a wide variety of disorders, including Parkinsons disease, various forms of atypical parkinsonism, or frontal mass lesions. How can we classify the gait disorders collectively grouped under the original term higher level gait disorders? These cannot be captured by a single, dominant, and consistently present gait feature, but do share a recognisable phenotype47,99 that can be identied using the rst step of our approach (table 1). We propose to maintain the original term higher level gait disorders until better insights arrive from pathophysiology. There is a growing consensus to avoid, for the time being, any further subdivisions of the higher level gait disorders, as these have little value in clinical practice.100 A more certain clinical diagnosis (which we would dene as a probable gait disorder) often requires an additional
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Core gait features Step 1

Specic gait or balance tests

Associated symptoms and signs

Possible gait disorder (clinically based gait syndrome)

Ancillary investigations Step 2

Therapeutic investigations

Disease progression

Probable gait disorder

Post-mortem examination Step 3

Denite (aetiology-based) gait disorder

Figure 4: Practical three-step approach for the classication of geriatric gait disorders The rst level yields a temporary, clinically based diagnosis, according to phenotype (possible gait disorder). Further renement of the diagnosis can be based on tailored ancillary studies (eg, structural neuroimaging, nuclear imaging, or genetics), the response to treatment (eg, response to levodopa, or the eect of stopping sedative drugs), and the factor time (disease course). This second level yields a probable gait disorder. A denite aetiological diagnosis will often depend on post-mortem examination.

diagnostic step (step 2 in gure 4). This second diagnostic step again involves three elements. First, for some patients, the clinical diagnosis will serve as a guide for tailored ancillary investigations, such as structural neuroimaging to detect, for example, underlying cerebrovascular disease. Second, the response to treatment will further assist in making a denitive diagnosis. For example, a substantial improvement of a shuing gait disorder with levodopa suggests involvement of a presynaptic dopaminergic lesion, possibly due to Parkinsons disease. Third, the factor time may provide additional clues about the disease course, or reveal newly emerging neurological abnormalities. For example, prolonged follow-up (up to 16 years) of patients with a cryptogenic primary progressive freezing gait showed a progression to recognisable clinical diagnoses, including pallidonigroluysian degeneration, diuse Lewy body disease, progressive supranuclear palsy, and corticobasal degeneration.101 The third and nal step of our diagnostic approach will lead to a denitive, aetiology-based diagnosis (step 3 in gure 4). This step often depends on post-mortem examination. Further enhancement of our understanding of particular gait disorders by increasing the number of clinicopathological correlations will be a major challenge. Our classication does not include gait disorders that are secondary to a clear and overriding balance problem.
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Search strategy and selection criteria References for this review were identied by searches of PubMed up to August 2006. Papers were also identied from the authors own les and from references given in relevant articles. Search terms gait, gait disorder, locomotion, elderly, geriatric, and ageing were used.

We feel that these should be classied as primary balance disorders and managed as such. An example is the astasia-abasia syndrome due to thalamic stroke, where gait is severely hampered not due to a defect in the neural machinery that is responsible for maintaining gait, but to a severe balance decit.102

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Conclusions
This review shows that the eld of gait disorders is very much on the move, with exciting new insights in the underlying pathophysiology. There is an increasing awareness that gait disorders in old people are often not due to merely ageing, but rather are associated with diseases that are more common in elderly people and which are potentially amenable to therapeutic intervention. Clinical assessment of geriatric gait disorders may seem dicult, but is facilitated by the practical approach proposed here. Modern neuroscience methods such as functional MRI and virtual reality are now increasingly engaged in gait research, and there is good reason to believe that this will enhance our fundamental understanding of geriatric gait disorders, thereby opening new avenues to improve the management of this common and disabling problem.
Contributors All authors participated in the drafting of the paper and have seen and approved the nal version. AHS did the systematic literature search, wrote the rst draft of the paper, and assisted in drafting later revisions of the paper. BPW critically reviewed and rewrote early drafts of this review paper and contributed to the proposed new classication system. BRB and NG jointly formulated the outlines of this review paper, contributed to the proposed new classication system, wrote parts of the manuscript, and contributed to the editing process. BRB had overall supervision of writing this review paper. Conicts of interest We have no conicts of interest. Acknowledgments AHS and BRB were supported by a research grant of the Princess Beatrix Funds. NG is supported by grants from the Parkinson Disease Association and the National Parkinson Foundation, USA. References 1 Bloem BR, Haan J, Lagaay AM, van Beek W, Wintzen AR, Roos RA. Investigation of gait in elderly subjects over 88 years of age. J Geriatr Psychiatry Neurol 1992; 5: 7884. 2 Sudarsky L. Gait disorders: prevalence, morbidity, and etiology. Adv Neurol 2001; 87: 11117. 3 Jorstad EC, Hauer K, Becker C, Lamb SE. Measuring the psychological outcomes of falling: a systematic review. J Am Geriatr Soc 2005; 53: 50110. 4 Bloem BR, Gussekloo J, Lagaay AM, Remarque EJ, Haan J, Westendorp RGJ. Idiopathic senile gait disorders are signs of subclinical disease. J Am Geriatr Soc 2000; 48: 1098101.

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