Binswanger's disease

Introduction

Gait disturbance is a characteristic feature of patients with vascular dementia [1]. In contrast, the NINCDS-ADRDA criteria for Alzheimer's disease (AD) state that: `gait disturbance at the onset or very early in the course of the illness' makes the diagnosis of probable AD uncertain or unlikely [2]. However, clinical studies suggest that gait disturbance is not restricted to the later stages of AD [3-6]. Also, studies in gait laboratories have identified abnormalities of gait and balance in patients with early AD [7-9].

Many of the gait disturbances found in elderly people and in those with dementia cannot be attributed to classical musculoskeletal, neuropathic, spastic, cerebellar or extrapyramidal syndromes [10]; these have been called higher-level gait disorders [11]. Terms used to describe these disorders include `gait apraxia', `senile gait', `lower-half parkinsonism' and `marche a petit pas'. Recently, Nutt et al. have attempted to bring some order to this terminological chaos by describing a clinical classification of higher-level gait disorders [11].

The clinical pattern of gait disturbance in patients with AD has attracted little attention to date. In this study, we used Nutt's classification to analyse higher-level gait disorders in patients with AD and controls.

Methods

Subjects: Patients with dementia and controls pair-matched for age ([+ or -]2 years), sex and location were recruited from the clinics and day-hospitals of a geriatric and a psychogeriatric unit. Patients referred specifically because of mobility problems or falls, and those who were bed- or chair-bound, had a history of stroke or Parkinson's disease, a Hachinski Ischaemic Score more than 4 [12], had been treated with neuroleptic medications within the previous year or had musculoskeletal, neuropathic or spastic causes of gait disturbance were excluded.

All patients with dementia satisfied the criteria for the clinical diagnosis of probable AD proposed by the NINCDS-ADRDA work group [2] (for the purpose of this study, gait disturbance was not considered when applying these criteria). Severity of dementia was defined using the Clinical Dementia Rating (CDR) scale, a global rating instrument comprising cognitive and behavioural domains: CDR 1 corresponds to mild, CDR 2 to moderate and CDR 3 to severe dementia [13].

Falls within the previous year and the presence of hypertension (defined as at least three blood pressure readings greater than 160/90 or on treatment for hypertension) were determined from the medical chart and by questioning patients, carers and staff.

Physical examination: Patients were examined in a standardized manner by a single experienced examiner. Balance was assessed using the procedure described by Tinetti [14]. In brief, stability is rated while the patient is sitting in a chair, rising from the chair, standing with eyes open and eyes closed, following a nudge on the chest, turning through 360[degrees] and sitting down. The better a subject's performance during these manocuvres, the higher the score; maximum score is 15.

Subjects used their usual walking aids. Initiation of walking, width of the base, step length, foot clearance, arm swing, cadence of gait and path deviation were assessed while subjects walked 50 feet, turning around a chair. While in a seated position, subjects were examined for apraxia by asking them to perform (without prior demonstration) the following movements. `Salute with your right/left hand', `Play a violin' (upper limb tests), `Kick out with your right/left foot', `Walk' (lower limb tests), `Bow' (truncal test) and `Drink through a straw' (buccofacial test) (maximum total score 8). Grasp, palmomental, snout and sucking reflexes were assessed using the approach of Tweedy et al. [15]. The presence or absence of gegenhalten (paratonic rigidity) was noted during irregular passive extension and flexion of the elbow and wrist joints. The presence of extrapyramidal signs was rated using the Webster scale [16]. As Girling and Berrios have noted, cognitive impairment is likely to reduce the discriminative power of some items on this scale [17]. Therefore, we followed their example and used a cut-off score of greater than five to define significant extrapyramidal signs.

Classification of gait: Gait disturbance was classified using the criteria proposed by Nutt et al. [11]; these criteria are summarized in Table I. For the purpose of this study, mild disequilibrium was arbitrarily defined as a balance score of 10-14 on the Tinetti battery, moderate disequilibrium as a score of 5-9 and severe disequilibrium as a score less than 5. In our experience, many elderly people without gait disturbance have mild disequilibrium. Therefore, we permitted a diagnosis of isolated gait ignition failure even if mild disequilibrium was present, provided gait was entirely normal once walking was under way.

[TABULAR DATA I OMITTED]

Analysis: Gait features and associated findings were compared between patients and controls using McNemar's test or Wilcoxon signed rank test as appropriate. Chi-square or exact tests were used to compare the frequency of signs between patients with gait disturbance and those without gait disturbance and between patients with frontal gait disorder and those with other gait disturbance. Among patients with dementia, the relationship between neurological signs and the severity of dementia was examined using the chi-square test for trend or the Kruskal-Wallis test.

Results

Fifty-five patients (34 women and 21 men) with dementia and 55 control subjects were recruited. Mean age (standard deviation) was 78(5) years. Twenty-one patients had mild dementia (CDR 1), 20 had moderately severe dementia (CDR 2) and 14 had severe dementia (CDR 3).

Gait features and associated findings in patients and controls are shown in Table II. Disequilibrium, short-stepping gait, gegenhalten, primitive reflexes and apraxia were more common in AD patients. With increasing severity of dementia, there was a significant increase in the frequency of disequilibrium (mild dementia 43%, moderate dementia 60%, severe dementia 79%; [chi square] = 4.4, p < 0.05), gegenhalten (5%, 15%, 43%; [chi square] = 7.6, p < 0.01) and primitive reflexes (0%, 10%, 36%; [chi square] = 9 0, p < 0.005).

Discussion

Many writers have reported that gait and balance remain normal until the late stages of AD [10, 18, 19]. However, Molloy et al. reported gait abnormalities in 19% of 136 patients presenting with AD [3]; other studies have reported similar findings [4-6]. Our finding that the frequency of different gait disorders differs with the severity of dementia provides some explanation for the disagreement between previous reports.

A cautious gait is a nonspecific finding in diverse conditions including arthritis and peripheral sensory and motor abnormalities. In this study, cautious gait was the most common gait disturbance in patients with mild dementia `(and in the control subjects). This disorder has been described as an appropriate response to `real or perceived instability' [11]. Thus, our findings are consistent with gait laboratory studies which have shown that patients with mild dementia exhibit impaired static balance, slow gait speed and short stride length compared with age-matched controls [7, 8].

Our results suggest that frontal gait disorder is the most common gait disturbance in patients with moderate to severe AD. This disorder is characterized by prominent disequilibrium, short steps, shuffling and start and turn hesitation and has been reported as a consequence of multiple lacunar infarcts, Binswanger's disease, frontal lobe tumour and hydrocephalus [11, 20, 21].

Previous studies have reported that a substantial proportion of AD patients develop extrapyramidal and frontal release signs [3-6, 22]. These patients appear to have more severe cognitive impairment and more rapid cognitive decline and may represent a distinct neuropathological and clinical subtype of AD [23, 24]. Our results indicate that frontal gait disorder is particularly characteristic of such patients. Our results are similar to those of Sjogren who noted gait disturbance in 13 (72%) of 18 patients with histologically proven AD and noted progressive unsteadiness and asynchrony of gait and development of prominent extrapyramidal rigidity with increasing severity of dementia [25].

Strict diagnostic and exclusion criteria and standardized assessment instruments were used in this study. Although we excluded patients referred specifically because of difficulties with mobility, the recruitment of subjects in hospital clinics may have led to over-representation of patients with gait disturbance. Nevertheless the prevalence of gait disturbance in this study is similar to that noted in other studies of AD patients [3-6]. Relatively few of the AD patients with gait disturbance had hypertension, the most important risk factor for vascular dementia and Binswanger's disease [1, 20].

Further studies are necessary to determine the clinical and neuropathological significance of abnormal gait patterns in AD patients. Nevertheless, our results suggest that diagnostic criteria for AD should take account of the frequency of different higher-level gait disorders at different stages of AD.

References

[1.] Thajeb P. Gait disorders of multi-infarct dementia. CT and clinical correlation. Acta Neurol Scand 1993;87:239-42. [2.] McKhann G, Drachman D, Folstein M, Katzman R, Price D, Stadlan EM. Clinical diagnosis of Alzheimer's disease: report of the NINCDS-ADRDA work group under the auspices of Department of Health and Human Services Task Force on Alzheimer's disease. Neurology 1984;34:939-44. [3.] Molloy DW, Clarnette RM, McIlroy WE, Guyatt G, Rees L, Lever J. Clinical significance of primitive reflexes in Alzheimer's disease. J Am Geriatr Soc 1991;39:1160-3. [4.] Becker JT, Boller F, Lopez OL, Saxton J, McGonigle KL. The natural history of Alzheimer's disease: description of study cohort and accuracy of diagnosis. Arch Neurol 1994;51:585-94. [5.] Galasko D, Kwo-on-Yuen P, Klauber M, Thai LJ. Neurological findings in Alzheimer's disease and normal aging. Arch Neurol 1990;47:625-7. [6.] Davous P, Lamour Y, Roudier M. Etude neurologique standardisee dans la demence senile de type Alzheimer. Encephale 1989;15:387-96. [7.] Visser H. Gait and balance in senile dementia of Alzheimer's type. Age Ageing 1983;12:296-301. [8.] Wooley SM, Lecso PA, McGreevey JF. Balance and gait in Alzheimer-type dementia. J Am Geriatr Soc 1992 40: SA36. [9.] Reed RL, Yochum K, Alcott S, Meredith K. Gait characteristics of subjects with senile dementia of the Alzheimer's type. J Am Geriatr Soc 1992;40:SA79. [10]. Sabin TD. Biologic aspects of falls and mobility limitations in the elderly. J Am Geriatr Soc 1982;30:51-8. [11.] Nutt JG, Marsden CD, Thompson PD. Human walking and higher-level gait disorders, particularly in the elderly. Neurology 1993;43:268-79. [12.] Hachinski VC, Lassen NA, Marshall J. Multi-infarct dementia. Lancet 1974;2:297-309. [13.] Hughes C, Berg L, Danziger WL, Coben LA, Martin RL. A new clinical scale for the staging of dementia. Br J Psychiatry 1982;140:566-72. [14.] Tinetti ME. Performance-oriented assessment of mobility problems in elderly patients. J Am Geriatr Soc 1986;34:119-26. [15.] Tweedy J, Reding M, Garcia C, Schulman P, Deutsch G, Antin S. Significance of cortical disinhibition signs. Neurology 1982;32. [16.] Webster DD. Clinical analysis of the disability of Parkinson's disease. Mod Treat 1968;5:257-82. [17.] Girling DM, Berrios GE. Extrapyramidal signs, primitive reflexes and frontal lobe function in senile dementia of the Alzheimer type. Br J Psychiatry 1990;157:888-93. [18.] Cummings JL, Benson DF. Dementia of the Alzheimer type: an inventory of diagnostic clinical features. J Am Geriatr Soc 1986;34:12-19. [19.] Koller WC, Wilson RC, Glass SL, Fox JH. Motor signs are infrequent in dementia of the Alzheimer type. Ann Neurol 1984;16:514-15. [20.] Caplan LR. Binswanger's disease--revisited. Neurology 1995;45:626-33. [21.] Meyer JS, Baron DW. Apraxia of gait: a clinicophysiological study. Brain 1960;83:261-84. [22.] Pearce JMS. The extrapyramidal disorder of Alzheimer's disease. Eur Neurol 1974;12:94-103. [23.] Funkerstein HH, Albert MS, Cook N, et al. Extrapyramidal signs and other neurological findings in clinically diagnosed Alzheimer's disease: a community based study. Arch Neurol 1993;50:51-6. [24.] Forstl H, Burns A, Levy R, Cairns N, Luthert P, Lantos P. Neurologic signs in Alzheimer's disease: results of a prospective clinical and pathophysiologic study. Arch Neurol 1992;49:1038-42. [25.] Sjogren H. Clinical analysis of morbus Alzheimer and morbus Pick. Acta Psychiatr Scand 1952;27(suppl 82):67-115.

Author's address Department of Geriatric Medicine, Royal Liverpool University Hospital, P.O. Box 147, Prescot Street, Liverpool L69 3BX

Received in revised form 2 February 1996

COPYRIGHT 1996 Oxford University Press
COPYRIGHT 2004 Gale Group