The Potential of Gait Analysis to Contribute to Differential Diagnosis of Early Stage Dementia: Current Research and Future Directions
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The Potential of Gait Analysis to
Contribute to Differential Diagnosis of
Early Stage Dementia: Current Research
and Future Directions*
Debra Morgan,1 Melanie Funk,2 Margaret Crossley,3 Jenny Basran,3 Andrew Kirk,3 and
Vanina Dal Bello-Haas3
RÉSUMÉ
Le diagnostic différentiel précoce entre les formes de démence revêt de plus en plus d’importance au fil de l’émergence
de nouveaux traitements médicamenteux qui sont efficaces dans certaines formes de démence et pas dans d’autres. La
détection et le diagnostic différentiel précoces ont également pour avantages de permettre à la famille de prendre des
décisions éclairées et de faciliter l’accès opportun aux services appropriés. Les caractéristiques de la démarche sont l’un
des éléments essentiels du diagnostic et cette information serait utile dans la distinction entre les formes de démence.
Le présent exposé de synthèse fait le point sur la recherche concernant le lien entre la démarche et la démence en
présentant notamment des systèmes de classification et des méthodes d’évaluation de la démarche, les caractéristiques
de la démarche selon le type de démences, dont la maladie d’Alzheimer, la démence vasculaire, la démence à corps de
Lewy et la démence frontotemporale, et l’utilité de l’analyse de la démarche dans le diagnostic à un stade précoce.
L’exposé se termine par les perspectives de la recherche à l’avenir.
ABSTRACT
Early differential diagnosis of dementia is becoming increasingly important as new pharmacologic therapies are
developed, as these treatments are not equally effective for all types of dementia. Early detection and differential
diagnosis also facilitates informed family decision making and timely access to appropriate services. Information about
gait characteristics is informative in the diagnostic process and may have important implications for discriminating
among dementia subtypes. The aim of this review paper is to summarize existing research examining the relationships
between gait and dementia, including gait classification systems and assessment tools, gait patterns characteristic of
different dementias (Alzheimer’s disease, vascular dementia, dementia with Lewy Bodies, and fronto-temporal dem-
entia), and the utility of gait analysis in early-stage diagnosis. The paper concludes with implications for future research.
1 Canadian Centre for Health and Safety in Agriculture / Institute of Agricultural Rural and Environmental Health
2 Victoria Hospital, Prince Albert, SK
3 University of Saskatchewan
* Thanks to Allison Cammer, Maxine Holmqvist, Lisa Lejbak, and Tasha Thornhill for their contributions to preparing this
manuscript. The authors gratefully acknowledge the support of the Canadian Institutes of Health Research (Institute of
Aging, Institute of Health Services and Policy Research, Rural and Northern Health Initiative), the Alzheimer Society of
Saskatchewan, Saskatchewan Health Research Foundation, and the University of Saskatchewan.
Manuscript received: / manuscrit reçu : 05/12/05
Manuscript accepted: / manuscrit accepté : 10/11/06
Mots clés : vieillissement, démarche, démence, diagnostic différentiel, évaluation, synthèse
Keywords: aging, gait, dementia, differential diagnosis, measurement, review
Requests for offprints should be sent to: / Les demandes de tirés-à-part doivent être adressées à :
Debra Morgan, Ph.D., R.N.
Canadian Centre for Health and Safety in Agriculture/Institute of Agricultural Rural and Environmental Health
Box 120, Royal University Hospital
University of Saskatchewan
103 Hospital Drive
Saskatoon, SK S7N 0W8
(debra.morgan@usask.ca)
Canadian Journal on Aging / La Revue canadienne du vieillissement 26 (1) : 19 - 32 (2007) 19
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Table 1: Gait Parameters
Term Definition
Step Length The distance from the point-of-heel strike of one extremity to the point-of-heel strike of the opposite extremity
Step Time Amount of time required to complete a step
Stride Length The distance from the point-of-heel strike of one extremity to the point-of-heel strike of the same extremity
Stride Time Amount of time required to complete a stride
Velocity Distance divided by the ambulation time—a measure of a body’s motion in a given direction
Cadence Number of steps per unit of time
Adapted from Perry (1992).
The prevalence of dementia is increasing worldwide, Methods
with an increase predicted in the industrialized world
Medline was the primary database searched. Other
from 13.5 million currently affected to 36.7 million in
databases searched included CINAHL, Cochrane
2050 and even greater increases predicted for devel-
Central Register of Controlled Trials, PsychInfo, and
oping nations (Vale, 2000). Incidence rates from the
Sport Discus, with MESH terms, locomotion, gait
Canadian Study of Health and Aging (CSHA)
analysis, gait disorders, ambulation, mobility, walking,
translate into 60,150 new cases of dementia per year
and each of the dementia types. The search was
in Canada (CSHA Working Group, 2000). It is
limited to peer-reviewed original research and review
predicted that by 2011 there will be 475,000
papers published after 1993. Earlier literature is cited
Canadians who have some type of dementia (CSHA
if it was referenced in several recent key articles or is
Working Group, 1994). Alzheimer’s disease (AD)
thought to be a significant contributor to current
accounts for the majority of all cases of dementia
research. The reference lists for key articles were
but needs to be accurately distinguished from other
investigated for pertinent sources. From the 145
causes, including fronto-temporal dementia (FTD),
articles originally identified and retrieved, 78 were
vascular dementia (VaD), dementia with Lewy Bodies
considered directly relevant and were included in this
(DLB), normal pressure hydrocephalus (NPH),
review.
dementia due to Parkinson’s disease (PD),
Creutzfeldt-Jakob disease (CJD), and other less
common forms of dementia. Early differential diag-
Challenges in Identifying Gait Patterns
nosis becomes increasingly important as new phar-
macological therapies are developed, particularly
Unique to Dementia Subtypes
since current treatments are not equally effective for The term gait refers to the pattern or manner of
all types of dementia. Early detection and differential walking and includes parameters such as cadence,
diagnosis also provide more opportunities for velocity, step length and frequency, and symmetry of
patients and family members to make informed limb movement (see Table 1 for definitions). Gait
decisions and facilitate timely access to appropriate or ambulation requires a coordinated action of the
behavioural and supportive interventions designed to neuromuscular and musculoskeletal systems and the
improve quality of life for patients and their maintenance of balance in order to move the body
caregivers. through the environment via locomotion. Balance,
the ability to maintain postural control, also requires a
Information about gait characteristics is informative
coordinated response of the neuromuscular and
in the diagnostic process, in identifying dementia
musculoskeletal systems as well as of the visual and
patients at risk for falling, and may be an indicator
other sensory systems. Gait and balance can some-
of future functional and cognitive decline. The
times be separated, but moving through the environ-
primary aim of this review paper is to summarize
ment and maintaining postural control are
existing research examining the relationships
intertwined. Thus, disorders of gait may also be
between gait and dementia, including gait classifica-
reflective of balance disorders and vice versa.
tion systems and assessment tools, gait patterns
characteristic of different dementias, and the con- Several factors contribute to the difficulty in inter-
sequent utility of gait analysis in early-stage preting existing literature examining gait patterns in
diagnosis. persons with dementia. In the research literature,
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motor features of dementia are frequently described exhibit pronounced disequilibrium, with absent,
in general terms as extra pyramidal signs (EPS). diminished, or ineffective postural responses. Frontal
However, it has been argued that this lack of precision disequilibrium is also characterized by marked postural
in characterizing movement disorders in AD has been instability, with inability to sit or stand independently
a major barrier in distinguishing AD from other and the feet crossing each other when attempting to
degenerative disorders with cognitive, behavioural, walk. In isolated gait ignition failure, there is marked
and motor symptoms (Kurlan, Richard, Papka, & difficulty initiating gait (start hesitation) and main-
Marshall, 2000). Failure to define the quality of the taining locomotion (turn hesitation or freezing).
disordered movement also hinders interpretation of Shuffling may be seen initially in the gait cycle, but,
previous studies of movement disorders in patients as walking continues, foot clearance becomes more
with AD. Kurlan et al. (2000) argue that the term EPS regular. Those with frontal gait disorder display a
is too imprecise and suggest that specific motor variable base (narrow to wide), short steps, shuffling,
disorders should be accurately described and specific hesitation with starting and turning, and moderate
diagnostic terminology used. They propose a number disequilibrium (Nutt et al, 1993).
of diagnostic definitions aimed at precisely character-
izing the motor disturbances accompanying AD and Kurlan et al. (2000) propose clinical definitions of
other dementias and thereby facilitating differential parkinsonism and pseudo-parkinsonism, with asso-
diagnosis and the accuracy of future research. ciated features that are important in differentiating
the two. They define parkinsonism as a clinical
Others have observed the inconsistent use of terms in syndrome consisting of motor disturbances character-
the literature. For example, in a review of research istic of idiopathic PD: bradykinesia, Parkinsonian
examining EPS in AD, Ellis, Caligiuri, Galasko, and (lead pipe) rigidity, resting tremor, and Parkinsonian
Thal (1996) found that some studies defined EPS gait. Pseudo-parkinsonism consists of motor distur-
narrowly (e.g., rigidity alone), whereas others used bances that resemble parkinsonism but are qualita-
broader definitions, including stooped posture, tively different and do not result from basal ganglia
Parkinsonian gait, tremor, bradykinesia, and hypo- pathology. The most important features are ideomotor
phonia. In the review conducted by Ellis et al. (1996), apraxia, paratonic rigidity, and frontal gait disorder
mild abnormalities of gait and posture were com- (for a full description of each of these distinguishing
monly observed in AD; excluding these signs, the features, see Kurlan et al., 2000).
most frequent EPS in AD were rigidity, bradykinesia,
and facial masking. Clarifying the relationship In a more recent classification of gait abnormalities in
between EPS and AD and characterizing the gait dementia, Verghese et al. (2002) described the follow-
patterns of dementia subtypes are hampered by the ing groups: unsteady, ataxic, frontal, Parkinsonian,
likely inclusion in the AD group, in some early neuropathic, hemiparetic, and spastic. They describe
studies, of individuals with dementia with Lewy frontal gait as characterized by short steps, a wide
Bodies (DLB). DLB, which typically presents with base, and the magnetic foot response. There is some
EPS, was not recognized as a separate diagnosis prior overlap between this frontal gait classification and
to the introduction of the consensus guidelines for that of Nutt et al. (1993), but there are discrepancies
DLB (McKeith et al., 1996). that change the definitions and result in ambiguity.
For example, a varying base differs from a wide base,
Nutt, Marsden, and Thompson (1993) have classified and both terms are open to interpretation. Nutt et al.’s
the higher-level gait disorders, including those (1993) classification system includes disequilibrium
prevalent in persons with dementia, in an attempt to and start-and-turn hesitation in the definition of
bring some order to what O’Keefe et al. (1996) refer to frontal gait disorder, while the scheme of Verghese
as ‘‘terminological chaos’’. The term higher-level et al. (2002) does not.
disorders (also called gait apraxia, senile gait, lower-half
parkinsonism) is used to refer to gait disturbances that Other limitations in the literature include lack of
cannot be attributed to classical musculoskeletal, consistency in the criteria for dementia diagnosis, in
neuropathic, spastic, cerebellar, or extra pyramidal the classification systems for identifying stage of
syndromes (O’Keefe et al., 1996). Nutt et al. (1993) dementia, and in the tools used for gait assessment.
describe five such gait disorders. Cautious gait is A challenge in studies of gait impairments in older
described as a normal to slightly widened base, en adults with dementia is the presence of co-morbidities
bloc turns, shorter stride lengths, and a decrease in and medication use, both of which are prevalent in
walking velocity, with normal cadence and foot-to- this population. The majority of studies in this review
floor clearance. Mild disequilibrium is displayed, and excluded individuals with co-morbidities and/or
there is no shuffling, start hesitation, or freezing. those taking medications that might influence
Individuals with subcortical disequilibrium gait disorder outcomes of interest.
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Gait Characteristics of the Dementias using the Cambridge Examination for Mental
Disorders of the Elderly cognitive subsection
Although researchers and clinicians have described
(CAMCOG) (Roth, Tym, & Mountjoy, 1986). None
gait impairments associated with dementia for some
of the 14 participants with mild dementia
time (e.g., Galasko, Kwo-on-Yuen, Klauber, & Thai,
(CAMCOG > 65) due to AD had a gait and balance
1990; Visser, 1983) interest in identifying gait char-
disorder. The presence of such a disorder in mild
acteristics unique to the dementia subtypes has dementia was diagnostic of non-Alzheimer’s demen-
increased because of the current emphasis on early tia. Gait and balance disorders were observed in
differential diagnosis. A summary of these character- 33 per cent of those with moderate AD and 50 per cent
istics is presented in Table 2. of those with severe AD. The focus on identifying gait
Gait Characteristics Associated with Alzheimer’s disorders rather than specific gait impairments may
Disease have resulted in lack of sensitivity to early changes in
gait that did not yet meet criteria for a disorder.
The current criteria for clinical diagnosis of dementia,
including the DSM-IV-TR (American Psychiatric In contrast to the findings described earlier of no
Association [APA], 2000), National Institute of gait disorders in mild AD, Pettersson et al. (2002)
Neurological and Communicative Disease and concluded that gait impairments are evident in early
Stroke/Alzheimer’s Disease and Related Disorders AD and can be identified with increased accuracy by
Association (NINCDS-ADRDA) (McKhann et al., performing a clinical gait assessment utilizing a valid,
1984), and the Canadian Consensus Conference on standardized tool. The authors employed the Berg
Dementia (Patterson et al., 1999) do not include gait Balance Scale (BBS) (Berg, Wood-Dauphinee,
disturbance as part of the clinical profile for early- Williams, & Gayton, 1989), the timed Up-and-Go
test (TUG) (Podsiadlo & Richardson, 1991), and
stage AD, although it is listed as being characteristic of
walking in figure of eight (Johansson & Jarnloo,
patients with more advanced disease (McKhann et al.,
1991). The mild AD patients demonstrated impair-
1984). The NINCDS-ADRDA criteria indicate that gait
ments on all of these measures when compared to the
disturbances at the onset or early in the course of the
control group—they had lower BBS scores, took
disease make the diagnosis of probable AD uncertain
longer to complete the TUG, and took more steps
or unlikely. In a validation study of these criteria, Ala
outside the figure of eight. Similarly, O’Keefe et al.
and Frey (1995) conducted a qualitative review of
(1996) utilized the classification system of Nutt et al.
cases of autopsy-proven AD to look for documentation
(1993) and the Tinetti battery to evaluate patients with
of gait impairments at first presentation. None of the
mild (clinical dementia rating scale [CDR] ¼ 1), moder-
36 patients presenting with mild dementia had ate (CDR ¼ 2), or severe AD (CDR ¼ 3) and age- and
reported gait abnormalities, although 16 per cent of sex-matched controls. Gait abnormalities were
patients with moderate dementia and 32 per cent of observed in all stages, and the frequency of disequili-
those with severe dementia had gait symptoms. The brium increased with the severity of dementia.
researchers acknowledged limitations in the study, Patients with mild AD typically had cautious gait
including the absence of a standardized gait assess- (i.e., impaired balance, decreased gait velocity,
ment tool and reliance on a relatively small sample of and shorter and more variable stride lengths). The
retrospectively collected data reported by many frequency of so-called frontal gait disorder increased
different physicians. Subtle gait abnormalities may with the severity of dementia. O’Keefe et al. (1996)
have been present but not reported. concluded that diagnostic criteria for AD should
Similar findings of no gait and balance disorders in take into account these data on the frequency and
early AD were reported in a recent study of 245 type of higher-level gait disorders at different stages
participants (Allan, Ballard, Burn, & Kenny, 2005) that of AD.
compared the prevalence, severity, and type of gait Goldman et al., (1999) used the CDR to compare AD
and balance disorders in AD, VaD, Parkinson’s patients with very mild (CDR ¼ 0.5) and mild AD
disease with dementia (PDD), DLB, Parkinson’s (CDR ¼ 1) to healthy controls. Patients with mild
disease without dementia (PD), and age-matched dementia were slowed on all three measures of
controls. Gait and balance disorders were assessed assessed motor function (i.e., gait velocity, reaction
using the Tinetti (1986) gait and balance scales. time, movement time) but clinically evident EPS was
Disorders were considered present if the Tinetti gait absent. A study of changes in equilibrium and limb
score was less than 7 (maximum score ¼ 9) or the coordination in normal aging, mild cognitive impair-
balance score was less than 22 (maximum score ¼ 26). ment, and mild AD groups (Franssen, Souren,
Gait disorder types were classified using the Nutt Torossian, & Reisberg, 1999) found early impairments
et al. (1993) system. Severity of dementia was assessed that increased with progression of cognitive
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Table 2: Gait Characteristics by Dementia Subtype
Dementia Subtype Gait Characteristics
1, 2, 3
Normal Aging Decreased gait velocity
1, 2, 4
Decreased stride length
2
Disturbed rhythm of motion
2, 5
Less vertical displacement of centre of mass
5
Ineffective stepping responses
2, 3, 4
Longer double support
2, 6
Decreased cadence
6
Decreased duration of swing phase
4
Slightly widened base of support
7, 8, 9
Alzheimer’s Disease (mild) Impaired balance
8, 9, 10, 11, 12
Decreased gait velocity
8
Short stepping gait
7, 10, 11, 12, 13, 14, 15
Alzheimer’s Disease (moderate-severe AD) Reduction in gait velocity
7, 8, 13, 14, 16
Shorter stride/step length
7, 15
Higher double support ratio
8, 15
Increased postural instability/disequilibrium
7, 12, 14, 15
Increased stride length variability
13, 17
Decreased arm swing
8, 17
Shuffling
8, 17
Start-and-turn hesitation
7
Retropulsion
14, 18
Decreased erect posture
14, 19, 20
Vascular Dementia Slow velocity
14, 19, 21, 22, 23, 24
Short stepping gait
19, 21, 22
En bloc turns
19, 21, 23
Postural instability
19, 22, 23
Wide-based gait
19
Start hesitation or freezing
19
Decreased cadence
21
Increased variability of gait lines
25
Increased tandem gait
18
Decreased arm swing
25, 26, 27, 28, 29
Dementia with Lewy Bodies Slower gait velocity
25
Marked ataxic tandem gait
25
Increased cadence
25
Decreased arm swing
25, 28, 30
Increased postural flexion and impaired balance
25
Shorter step lengths
27, 31, 32
Rigid posture
continued
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Table 2: Continued
Dementia Subtype Gait Characteristics
28, 30
Stooped posture
28, 29
Shuffling gait
33, 34
Normal Pressure Hydrocephalus Decreased gait velocity
33, 34
Variable stride lengths
33
Broad-based gait
33
Externally rotated feet
33, 34
Reduced foot-to-floor clearance
34
Decreased step height
34
Magnetic gait
5
Fronto-temporal Dementia Short shuffling steps
5
Initiation hesitation
5
Freezing
5
Exaggerated arm swing
5
Slow steps and movement
5
Freezing on turning
1 Hagemen & Thomas, 2002. 19 Thajeb, 1993.
2 Mbourou, Lajoie, & Teasdale, 2003. 20 van Iersel, Hoefsloot, Munneke, Bloem, & Olde
3 Kressig et al., 2004. Rikkert, 2004.
4 Sudarsky, 2001. 21 Hennerici et al., 1994.
5 Shkuratova, Morris, & Huxham, 2004. 22 Román et al., 1993.
6 Laufer, 2005. 23 Verghese et al., 2002.
7 Nakamura et al., 1997. 24 Zijlmans et al., 1996.
8 O’Keefe et al., 1996. 25 Waite, Broe, Grayson, & Creasey, 2000.
9 Petterson, Engardt, & Wahlund, 2002. 26 Louis, Goldman, Powers, & Fahn, 1995.
10 Ott, Ellias, & Lannon, 1995. 27 McKeith, 2002.
11 Goldman, Baty, Buckles, Sahrmann, & Morris, 28 McKeith et al., 1996.
1999. 29 Hohl, Tiraboschi, Hansen, Thai, & Corey-Bloom,
12 Sheridan, Solomont, Kowall, & Hausdorff, 2003. 2000.
13 Alexander et al., 1995. 30 Galasko, Atzman, Salmon, & Hansen, 1996.
14 Franssen, Kluger, Torossian, & Reisberg, 1993. 31 Weiner et al., 2003.
15 Tanaka, Okuzumi, Kobayashi, Murai, & Meguro, 32 Gnanalingham, Byrne, Thorton, Sambrook, &
1995. Bannister, 1997.
16 Ala & Frey, 1995. 33 Stolze et al., 2001.
17 Funkenstein et al., 1993. 34 Krauss et al., 2001.
18 Galasko et al., 1990.
impairment as classified using the Global EPS, to that in normal controls. Results were not
Deterioration Scale (GDS) (Reisberg, Ferris, DeLeon, reported by stage of illness, but AD patients moved
& Crook, 1982). There were significantly poorer more slowly than controls on all speeded motor
performances on each of the five equilibrium and tasks, including finger tapping, arm movement,
limb-coordination tasks for both the mild cognitive and walking.
impairment (GDS stage 3) and mild AD groups (GDS
stage 4), when compared to normal older adults (GDS Verghese et al. (2002), whose gait classification system
stages 1 and 2). Ott et al. (1995) compared motor was described above, conducted a prospective study
performance in patients with mild to moderately of 422 community-dwelling individuals aged 75 and
severe AD (MMSE scores 14–24), none of whom had older who did not have dementia at baseline to
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explore the role of gait abnormalities in predicting Nakamura et al. (1997) found that in AD patients
risk of AD versus non-AD dementias. Of the 125 with mild dementia (CDR ¼ 1) there was evidence of
participants who developed dementia during the postural instability but little decrease in gait function,
follow-up phase of the study (median duration whereas those with moderate dementia (CDR ¼ 2)
6.6 years), 70 were diagnosed with AD and 55 with displayed reduced gait velocity, shorter stride lengths,
non-AD dementias (47 were diagnosed with VaD and and more postural instability than did the mild AD
8 with other dementia subtypes). Although abnormal group. Those with severe dementia (CDR ¼ 3) exhib-
gait was observed more frequently during follow-up ited even more decline in these features, and retro-
among those with non-AD dementias (65%), gait pulsion (20%) and frozen gait (20%) were also evident.
impairments were also exhibited by 35 per cent of Moderate and severe AD patients had increased
subjects with AD. The specific gait patterns of AD double support time and more stride-length varia-
patients were not reported. A potential limitation bility than the control group. As noted earlier,
reported by the authors was the use of clinical O’Keeffe et al. (1996) found that those with severe
observation to assess gait, rather than quantitative AD typically had frontal gait disorder (as defined by
gait analysis, which may be more reliable and more Nutt et al., 1993), characterized by marked disequili-
sensitive to subtle impairments. brium, shuffling, start-and-turn hesitation, and short-
A similar pattern of gait impairments was observed in er step lengths; in early stage AD, cautious gait was
a study aimed at describing the natural history of AD more common.
and determining early observable clinical signs and Walking velocity in patients with AD is significantly
symptoms (Becker, Boller, Lopez, Saxton, & decreased when they are compared to age-matched
McGonigle, 1994). Becker et al. (1994) compared 181 control groups and worsens with disease progression
individuals with AD (mean MMSE 18.4, SD ¼ 5.2) to (Alexander et al., 1995; Goldman et al., 1999;
102 normal controls. AD patients were significantly Nakamura et al., 1997; Tanaka et al., 1995). With the
more likely to exhibit gait impairments compared to exception of Goldman et al. (1999) (who did not
controls (26% vs. 2%), although details about the gait
measure step length), these studies confirmed that AD
assessment were not described. Becker et al. (1994)
patients also had a reduced step length in contrast to
reported impaired limb praxis in 74 per cent of AD
that of healthy control groups. Funkenstein et al.
patients and 7 per cent of controls. Another study
(1993) compared AD patients at various stages of the
investigating the course of AD after diagnosis, as well
disease to controls and observed that gait impair-
as factors associated with survival (Larson et al.,
ments—including decreased arm swing, prolonged
2004), found that gait disturbances and falling were
turning, and shuffling—were strongly associated with
correlated with a significantly increased risk for death
AD. Individuals who displayed shuffling in addition
in older persons with AD. Together, the results of
to prolonged turning were almost 7 times as likely to
these studies indicate that gait impairments are
evident in early stage AD, particularly impaired have AD.
balance (Nakamura et al., 1997; O’Keefe et al., 1996; In summary, past research indicates that individuals
Pettersson et al., 2002) and decreased gait velocity with moderate or severe AD exhibit gait impairments,
(Goldman et al., 1999; O’Keefe et al., 1996; Ott et al., including decreased gait velocity (Alexander et al.,
1995; Pettersson et al. 2002) but also shortened stride 1995; Goldman et al., 1999; Nakamura et al., 1999;
length (O’Keefe et al., 1996) and impaired limb praxis O’Keefe et al., 1996; Ott et al., 1995), decreased step
(Becker et al., 1994). length (Alexander et al., 1995; Nakamura et al., 1997;
Gait disorders become more prominent as AD O’Keefe et al., 1996), and impaired balance
progresses and have long been recognized as a feature (Nakamura et al., 1997; O’Keefe et al., 1996). Results
of later-stage AD, although, as noted earlier, inter- must be interpreted cautiously, however, since it is
preting studies published prior to 1996 is difficult possible that patient groups were not specifically AD
because of the possible inclusion of recently recog- and were inclusive of other dementia subtypes.
nized dementia subtypes such as DLB. A frequently Nevertheless, subtle gait abnormalities are often
cited early paper by Visser (1983) compared ambula- seen in earliest stages of dementia and are more
tory AD patients with severe memory impairment to pronounced in the later stages, regardless of
normal controls and reported that the AD patients diagnostic subtype.
had significantly shorter step length, lower gait speed,
lower stepping frequency, greater step-to-step varia- Gait Characteristics of Vascular Dementia Compared
to AD and Other Disorders
bility, greater double-support ratio, and greater sway
path. Subsequent studies have continued to charac- The DSM-IV-TR criteria for vascular dementia (APA,
terize gait impairments in AD. For example, 2000) includes focal neurological signs and symptoms
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https://doi.org/10.3138/1457-2411-V402-62L126 Canadian Journal on Aging 26 (1) Debra Morgan et al.
such as gait abnormalities, and the NINDS-AIREN Several studies have examined gait disturbances
criteria for probable vascular dementia (Román et al., in subcortical arteriosclerotic encephalopathy or
1993) include early presence of gait disturbance Binswanger’s disease, a subtype of VaD. Although
(small-step gait, or magnetic, apraxic–ataxic, or clinical descriptions have stressed the similarity to
Parkinsonian gait) as well as a history of unsteadiness Parkinsonian gait (e.g., loss of truncal mobility, start
and frequent, unprovoked falls. Many subtypes of hesitation, freezing, short shuffling steps), signs of
VaD have been recognized, and studies are emerging ataxic gait have also been described, including broad-
that identify gait features thought to be characteristic based walking, instability with increased risk of
of these subtypes. falling (Thompson & Marsden, 1987), irregular gait
patterning, altered regulation of gait velocity, and
Thajeb (1993) studied 88 patients with VaD (then
absence of festination (i.e., rapid short stepping)
called multi-infarct dementia) and found that
(Ebersbach et al., 1999). Thompson and Marsden
25 patients exhibited significant gait difficulty.
(1987) concluded that the gait of persons with
A slow and short stepping gait was observed in all
subcortical arteriosclerotic encephalopathy has ele-
25 patients, and en bloc turns, freezing upon turning a
ments of both parkinsonism and cerebellar ataxia. The
corner, postural instability, wide-based gait, and start
most obvious difference from PD was the truncal
hesitation or freezing were observed in the majority of
ataxia and wide-based gait, compared to the narrow
patients with gait impairments. The prospective study
base in PD. Bazner, Oster, Daffertshofer, and
conducted by Verghese et al. (2002) found that the
Hennerici (2000) utilized a computerized gate-
presence of neurological gait abnormalities was a
analysis system to determine that, when compared
significant predictor for a future diagnosis of non-AD
to the control group, patients with subcortical
dementia, especially VaD (hazard ratio 3.46 [95% CI,
vascular encephalopathy displayed a decrease in
1.86–6.42]). Gait patterns that predicted VaD were
cadence, a reduction in the length of the single-
unsteady gait (loss of balance or falls), frontal gait (short
support phase, and an increase in the time spent in
steps, wide base, and magnetic foot response), and
the double support stance. Various gait patterns
hemiparetic gait (swinging legs outward). Gait abnorm-
associated with the subtypes of VaD are still emer-
alities were shown to predict and precede actual
ging, and studies are needed to gather more knowl-
diagnosis by several years. Allan et al. (2005) found
edge in this area.
that presence of a frontal gait disturbance (frontal gait
disorder or frontal disequilibrium) identified patients Gait Characteristics of Dementia with Lewy Bodies
with VaD with a sensitivity of 76 per cent and a Compared to AD and Other Disorders
specificity of 87 per cent. Of the 39 participants with
It has been suggested that dementia with Lewy Bodies
VaD, 79 per cent exhibited gait and balance disorders,
(DLB) may comprise the second-largest category of
with similar prevalence across all levels of dementia
age-related cognitive impairment after AD (Papka,
severity as measured by the CAMCOG.
Rubio, & Schiffer, 1998). Of the various sets of criteria
Hennerici et al. (1994) evaluated gait disturbances in for the clinical diagnosis of DLB, those proposed by
24 patients with possible vascular dementia, using McKeith, Perry, Fairbairn, Jabeen, and Perry (1992)
both clinical observation and objective data obtained were most influential. These were modified at an
using shoe insoles embedded with force transducers. international consortium on DLB (McKeith et al.,
On inspection, 7 patients were observed to have short 1996) and include parkinsonism as a core feature
slow steps, difficulty turning, and postural instability, essential for the diagnosis, along with fluctuating
but freezing, start hesitation, wide-based walking, cognition and recurrent visual hallucinations. Other
rigidity, and tremor were absent. On objective supportive features are described, including repeated
gait analysis, however, all patients had abnormal falls. These criteria were subsequently reviewed
gait patterns, particularly increased variability of gait and endorsed at a second international consensus
lines. In a study comparing individuals with AD, conference (McKeith, Perry, & Perry, 1999), with the
VaD, and normal healthy controls, Tanaka et al. (1995) recommendation that research focus on increasing
found significantly slower velocity and shorter step sensitivity of case detection. Assessments of the
length in individuals with VaD, compared to controls accuracy of these and other clinical criteria have
and those with AD. Postural instability was evident in produced mixed results. Del Ser et al. (2000) con-
those with AD. Thus, there is consistent evidence in ducted a study involving participants with DLB in
the literature for slow, short-stepping, and wide-based 17 centres from Spain, UK, and Italy to examine the
gait and difficulty turning in individuals with VaD usefulness of the McKeith et al. (1996) consensus
(Hennerici et al., 1994; Tanaka et al., 1995; Thajeb, criteria in different countries. The results supported
1993; Verghese et al., 2002). the criteria, including parkinsonism and repeated
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https://doi.org/10.3138/1457-2411-V402-62L1Gait and Dementia La Revue canadienne du vieillissement 26 (1) 27
falls. However, in a study of patients who were in DLB there was a higher incidence of left/right
autopsied (Hohl et al., 2000), 4 of the 10 patients asymmetry, a less prominent resting tremor, and more
presumed to have had DLB had pathologic findings pronounced rigidity. Louis et al. (1995) found that
of AD. Features included in the criteria for DLB, resting tremor and muscular rigidity were equally
including repeated falls and early onset of gait prevalent in DLB and PD and that bradykinesia was
impairments, were not helpful in distinguishing observed in 86 per cent of the DLB cases and 56 per
between autopsy-proved DLB groups and the mis- cent of PD patients. McKeith (2002) reported that up to
diagnosed DLB group who had actually had AD. 70 per cent of DLB patients have Parkinsonian
symptoms, with bradykinesia, rigidity, and gait
Papka, Rubio, Schiffer, and Cox (1998) evaluated the
impairments being the most common features.
utility of consensus criteria and the presence of EPS in
Clearly, there is an ongoing debate concerning the
accurate clinical diagnosis of DLB, by comparing the
prevalence and diagnostic significance of EPS in DLB.
accuracy of several existing criteria (McKeith et al.,
1992; McKeith et al., 1996) and their own proposed The most recent study comparing gait and balance
criteria. Overall, results failed to confirm that any of disorders in the dementia subtypes (Allan et al., 2005)
the sets of criteria had sufficient accuracy to predict found that the presence of a Parkinsonian gait,
Lewy Body pathology when it presented with con- defined using the criteria of Nutt et al. (1993),
comitant AD changes. Contrary to their expectations, identified participants with DLB or Parkinson’s
in their sample, the presence of EPS did not facilitate disease with dementia with a sensitivity of 87 per
more accurate diagnosis of DLB (n ¼ 39). cent and a specificity of 84 per cent. Among the
32 participants with DLB, the prevalence of gait and
Waite et al. (2000) evaluated gait in patients diagnosed balance disorders in those with mild, moderate,
with AD, VaD, mixed dementia, and DLB. When and severe dementia was 40 per cent, 87 per cent,
compared to the control group, patients with all of and 100 per cent, respectively.
these conditions displayed lower gait velocities and
had more severe ataxic tandem gait, took more steps Gait Characteristics Associated with
over a certain distance, and had decreased arm swing Fronto-temporal Dementias
and increased postural flexion. Interestingly, out of all
Diagnostic criteria for fronto-temporal dementia
groups, those with DLB exhibited the most impaired
(FTD) are still evolving. The DSM-IV-TR (APA, 2000)
balance, slowed gait, and shortened stride length.
does not include criteria for any of the FTDs.
When compared to AD and PD patients, DLB patients
Although the international consensus criteria pro-
have also been shown to require more time to rise
posed by Neary et al. (1998), which describes three
from a chair, walk 6 metres, and return to the chair;
FTD subtypes, appears to be accepted in the literature
they also take more steps to perform this task
and have been used in recent studies, McKhann et al.
(Gnanalingham et al., 1997). Inclusion in the
(2001) have proposed simplifying FTD into a single
Gnanalingham et al. study required a clinical diag-
set of criteria. The subtypes included in Neary et al.’s
nosis of idiopathic PD, probable or possible AD, or
(1998) criteria are frontal variant, progressive non-
DLB. Mean scores on the MMSE and Clinical fluent aphasia and semantic dementia. All of these
Dementia Rating (CDR) were highest for the PD subtypes may present with signs and symptoms of
group and lowest for the DLB group. motor neuron disease (e.g., bulbar palsy, muscle
Weiner et al. (2003) sought to determine whether DLB weakness, and wasting) and parkinsonism may be
could be differentiated from other dementias at the displayed (e.g., bradykinesia, rigidity, tremor, festina-
crucial time of the initial assessment. EPS were rated as tion) early in the course of the illness (Neary et al.,
present or absent using the Unified Parkinson’s 1998), which may cause gait abnormalities.
Disease Rating Scale (Fahn, Elton, & Members of the
UPDRS Development Committee, 1987). Increased Gait Characteristics Associated with Other Dementias
muscle tone, rigidity, a flexed posture, and falls were A relatively uncommon yet important condition
significantly more likely to be characteristic of the DLB resulting in dementia is normal pressure
group when compared to the AD group. In addition, hydrocephalus (NPH), which is characterized by the
those in the DLB group were more susceptible to clinical triad of gait disturbance, symptoms of
developing EPS after using neuroleptics, differentiat- dementia, and urinary incontinence. Disturbance of
ing them from those with AD, findings that support gait is often an early sign (Stolze et al., 2001). Stolze
those of Hohl et al. (2000). The development of et al. (2001) compared the gait of NPH and PD
spontaneous EPS was not found to be a distinguishing patients and controls. A key diagnostic marker for the
factor. Gnanalingham et al. (1997) reported that, NPH group was a slow gait, with lower-extremity
although EPS in DLB and idiopathic PD are similar, external rotation, variable stride lengths, increased
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https://doi.org/10.3138/1457-2411-V402-62L128 Canadian Journal on Aging 26 (1) Debra Morgan et al.
step width, and reduced foot-to-floor clearance; A major barrier to furthering research and enhancing
disturbed dynamic equilibrium was a striking feature knowledge about gait impairments in persons with
and was interpreted as a protective strategy to dementia is the need for more and better measure-
stabilize locomotion. These findings were in contrast ment tools that are sensitive, reliable, and valid for
to those for PD patients, where increased foot angles individuals with dementia. Gait disorders are typi-
and step widths were rarely seen. Similarly, cally assessed by means of clinical observation, and,
Creutzfeld-Jakob disease is another rare form of although useful for describing abnormalities, findings
dementia that presents with early and rapidly are subjective and open to interpretation and therefore
progressing decline in both cognitive and motor may not reveal subtle gait characteristics or be
systems. The DSM-IV-TR (APA, 2000) does not sensitive to change over time. Some studies have
include specific criteria for NPH or Creutzfeld-Jakob used computerized gate-analysis methods or other
disease; both are included under ‘‘Dementia due to more sophisticated gait laboratory equipment to
other general medical conditions’’. quantify gait variables. These detailed and time-
consuming strategies are useful for research purposes
Together, the findings reported above suggest that
but are not practical or feasible in most clinical
careful assessment of gait, balance, and movement
settings, where time, trained personnel, adequate
in the earliest stages of cognitive decline has the space, and access to sophisticated equipment may
potential to contribute significantly to differential be limited.
diagnosis. The importance of early and accurate
diagnosis will increase as new pharmacological Several strategies would be useful in addressing these
treatments and behavioural interventions are targeted measurement issues. In order to take full advantage of
to specific dementia subtypes. Although it is assumed existing gait classification systems, further clarifica-
that subtle but measurable gait characteristics can tion of and consistency in use of terms is needed. For
distinguish dementia subtypes, autopsy studies are example, Nutt et al.’s (1993) classification system may
needed to verify the presumed linkages between provide a useful means of organizing gait disorders
pathological brain changes and movement disorders into categories and qualitatively describing certain
(Hohl et al., 2000; Kurlan et al., 2000). In addition to gait patterns, but the ambiguity of the terms is an
contributing to differential diagnosis, gait analysis impediment to accurate measurement. For example,
during early-stage assessment may be useful in how broad must a stance be in order to be considered
identifying individuals at high risk for falls. wide-based? How short should steps be in order to
qualify for the frontal-gait category? Developing these
categorical approaches into standardized quantitative
Directions for Future Research rating scales could potentially enable us to further our
Evidence is mounting that specific types of dementia understanding of gait disorders and assist in classify-
may have characteristic gait abnormalities, but more ing the various gait patterns of dementia patients.
research is needed to identify further which gait Objective measures with clear criteria for scoring
patterns and abnormalities are unique and which are would enhance the reliability of the tool and build
common across dementia types. Of special impor- upon existing qualitative information supporting
tance is information on gait changes in the early characteristic gait patterns.
stages of dementia, when differential diagnosis is Little is known about the reliability and validity of
especially difficult but also critical in developing existing gait scales in assessing individuals with
treatment and management approaches. Gait and dementia. A diagnosis of dementia is an excluding
balance assessments should be conducted through- factor in many studies, due to uncertainty about the
out the course of dementia because impairment reliability of physical performance measures in this
may predict fall risk and functional decline in population. This is not surprising, given the decline in
activities of daily living. More accurate measurement memory, attention, understanding, motor ability, and
strategies would also facilitate studies exploring the reaction time. Although Rockwood, Awalt, Carver,
impact of cholinesterase inhibitors and other and MacKnight (2000) reported poor test–retest
pharmacological treatments on gait patterns in indi- reliability for the timed Up-and-Go (TUG), which
viduals with dementia. It has been argued that was used in the Canadian Study of Health and Aging,
quantitative gait assessment tools would be useful in other studies have reported good to excellent relia-
detecting both drug side effects and positive effects of bility. For example, Thomas and Hageman (2003), in
therapy (van Iersel et al., 2004). Future studies need to their study with dementia patients, found that the
determine which methods are responsive enough to reliability estimates for the TUG and for usual and
identify small, yet clinically significant, changes that fast-gait speed were excellent (intra-class correlations
may be seen in gait over time. ranging from 0.75 to 1.00). Although these tests may
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https://doi.org/10.3138/1457-2411-V402-62L1Gait and Dementia La Revue canadienne du vieillissement 26 (1) 29
require some minor modifications when used with (Shumway-Cook & Woollacott, 2001) are examples of
dementia participants, such as physical and verbal functionally relevant gait-analysis scales that may
cueing, the findings of this study parallel other prove useful in gauging patients’ mobility levels.
findings confirming that physical performance mea- Since the TUG has been found to correlate with gait
sures can indeed be utilized with a high degree of speed and balance (Podsiadlo & Richardson, 1991), it
reliability for this population (Brill, Drimmer, Morgan, would be interesting to study whether similar results
& Gordon, 1995; Podsiadlo & Richardson, 1991; could be discerned with a more sophisticated func-
Tappen, Roach, Buchner, Barry, & Edelstein, 1997). tional analysis. Given that the more detailed gait tools
Further studies are needed to confirm the degree of are time-consuming and considering the mounting
reliability of the TUG and other gait-analysis scales in emphasis on functional abilities during geriatric
persons with dementia. evaluation, this avenue of research may be of
particular interest.
There have been few studies conducted with the
intent of gauging change in gait over time in dementia As previously mentioned, Pettersson et al. (2002)
patients, although two studies have utilized practical utilized the Berg Balance Scale, TUG, and walking in a
gait instruments to measure a change in gait perfor- figure of eight to discern that gait impairments do
mance in individuals with dementia in response to exist in those with mild AD. Future studies could look
resistance training programs (Hageman & Thomas, beyond gait variables such as speed and cadence to
2002; Thomas & Hageman, 2003). These methods take advantage of available gait-analysis scales fea-
included the TUG; the gait subscale of the sible for clinical settings. Examples of simple and
Performance Oriented Mobility Assessment (Tinetti, easily administered tools that could be further
1986); the Gait Assessment Rating Scale (GARS) evaluated for reliability, validity, and feasibility
(Wolfson, Whipple, Amerman, & Tobin, 1990); Sit-to- include the TUG, walking in a figure of eight, and
Stand; measuring comfortable and fast speed over Tinetti’s Performance Oriented Mobility Assessment
6 meters; and step length. Gait speed has been shown (Tinetti, 1986).
to be sensitive to change (Fiatarone & Evans, 1993) In conclusion, research is beginning to uncover the
but, to our knowledge, the sensitivity of the GARS or associations between dementia subtypes and gait
Tinetti gait subscale have not been estimated. characteristics, although the value of gait analysis in
Normative values for the various gait measurement the diagnostic process has yet to be fully recognized.
approaches, such as comfortable and maximum velocity Future research, including autopsy studies, will
by decade of age and gender, have been reported continue to expand knowledge in this area, contribut-
(Bohannon, 1997), but there is limited information ing to the efficacy of the assessment process for
available for those with dementia. One source of individuals suspected of having dementia and enhan-
normative values is the Canadian Study of Health and cing patient care throughout the disease process.
Aging, which conducted the TUG test with partici-
pants diagnosed with dementia and with healthy References
age- and sex-matched controls (CSHA Working Ala, T., & Frey, W. (1995). Validation of the NINCDS-
Group, 2004). Developing norms across stages for ADRDA criteria regarding gait in the clinical diagnosis
the dementia subtypes would be useful in under- of Alzheimer disease. Alzheimer Disease and Associated
standing the natural history of these diseases and in Disorders, 9(3), 152–159.
developing individual patient-care plans.
Allan, L., Ballard, C., Burn, D., & Kenny, R. (2005).
Another suggestion for future research and clinical Prevalence and severity of gait disorders in
applications would be to conduct functional gait Alzheimer’s and Non-Alzheimer’s dementias. Journal
analysis with individuals with suspected or diag- of the American Geriatrics Society, 53, 1681–1687.
nosed dementia. To date, no such studies have been
Alexander, N., Mollo, J., Giordani, B., Ashton-Miller, J.,
reported. Although having a patient walk a certain Schultz, A., Grunawalt, J., et al. (1995). Maintenance
number of feet may yield useful information, such as of balance, gait patterns, and obstacle clearance in
gait speed and cadence, this assessment does not Alzheimer’s disease. Neurology, 45(5), 908–914.
mimic the setting in which patients find themselves
on a typical day. Everyday living requires individuals American Psychiatric Association. (2000). Diagnostic and
to be able to modify their gait speed, change direction, statistical manual of mental disorders (DSM-IV-TR)
(4th ed.). Washington, DC: Author.
perform another task at the same time, and overcome
obstacles on the path. The Duke Mobility Skills Profile Bazner, H., Oster, M., Daffertshofer, M., & Hennerici, M.
(Hogue, Studenski, & Duncan, 1990), the Berg Balance (2000). Assessment of gait in subcortical
Scale (Berg et al., 1989), and the Dynamic Gait Index vascular encephalopathy by computerized analysis:
Downloaded from https://www.cambridge.org/core. University of Athens, on 24 Feb 2021 at 17:03:47, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms.
https://doi.org/10.3138/1457-2411-V402-62L130 Canadian Journal on Aging 26 (1) Debra Morgan et al.
A cross-sectional and longitudinal study. Journal of disease: Relationship to functional decline. Archives of
Neurology, 415, 841–849. Neurology, 50, 1029–1039.
Becker, J., Boller, F., Lopez, O., Saxton, J., & McGonigle, K. Franssen, E., Souren, L., Torossian, C., & Reisberg, B. (1999).
(1994). The natural history of Alzheimer’s disease: Equilibrium and limb coordination in mild cognitive
Description of study cohort and accuracy of diagnosis. impairment and mild Alzheimer’s disease. Journal of the
Archives of Neurology, 51(6), 585–594. American Geriatrics Society, 47(4), 463–469.
Berg, K., Wood-Dauphinee, S., Williams, J., & Gayton, D. Funkenstein, H., Albert, M., Cook, N., West, C., Scherr, P.,
(1989). Measuring balance in the elderly: Preliminary Chown, M., et al. (1993). Extrapyramidal signs and
development of an instrument. Physiotherapy Canada, other neurologic findings in clinically diagnosed
41, 304–311. Alzheimer’s disease. Archives of Neurology, 50, 51–56.
Bohannon, R. (1997). Comfortable and maximum walking Galasko, D., Katzman, R., Salmon, D., & Hansen, L. (1996).
speed of adults aged 20–79 years: Reference values and Clinical and neuropathological findings in Lewy Body
determinants. Age and Ageing, 26, 15–19. dementias. Brain and Cognition, 31, 166–175.
Brill, P., Drimmer, A., Morgan, L., & Gordon, N. (1995). Galasko, D., Kwo-on-Yuen, P., Klauber, B., & Thai, L. (1990).
The feasibility of conducting strength and flexibility Neurological findings in Alzheimer’s disease and
programs for elderly nursing home residents with normal aging. Archives of Neurology, 47, 625–627.
dementia. Gerontologist, 35, 263–266.
Gnanalingham, K., Byrne, E., Thornton, A., Sambrook, M., &
Canadian Study of Health and Aging Working Group. Bannister, P. (1997). Motor and cognitive function in
(1994). Canadian Study of Health and Aging: Study Lewy Body dementia: Comparison with Alzheimer’s
methods and prevalence of dementia. Canadian Medical and Parkinson’s diseases. Journal of Neurosurgery and
Association Journal, 150, 899–913. Psychiatry, 62, 243–252.
Canadian Study of Health and Aging Working Group. Goldman, W., Baty, J., Buckles, V., Sahrmann, S., & Morris, J.
(2000). The incidence of dementia in Canada. Neurology, (1999). Motor dysfunction in mildly demented AD
55, 66–73. individuals without extrapyramidal signs. Neurology,
Canadian Study of Health and Aging Working Group. 53(5), 956–962.
(2004). Clinical Examination. Retrieved 15 December Hageman, P., & Thomas, V. (2002). Gait performance in
2004 from http://csha.ca/r_clinical_examination.asp. dementia: The effects of a 6-week resistance training
Del Ser, T., McKeith, I., Anand, R., Cicin-Sain, A., Ferrara, R., program in an adult day-care setting. International
& Spiegel, R. (2000). Dementia with Lewy Bodies: Journal of Geriatric Psychiatry, 17, 329–334.
Findings from an international multicentre study. Hennerici, J., Oster, J., Cohen, S., Schwartz, A., Motsch, L., &
International Journal of Geriatric Psychiatry 15, 1034–1045. Daffertshofer, M. (1994). Are gait disturbances and
Duncan, P. (1989). Duke Mobility Skills Profile. Durham, white matter degeneration early indicators of vascular
NC: Duke University, Centre for Human Aging. dementia? Dementia, 5, 197–202.
Ebersbach, G., Sojer, M., Valldeoriola, F., Wissel, J., Muller, J., Hogue, C., Studenski, S., & Duncan, P.W. (1990). Assessing
Tolosa, E., et al. (1999). Comparative analysis of gait in mobility: The first steps in preventing fall. In S.G. Funk,
Parkinson’s disease, cerebellar ataxia and subcortical E.M. Tornquist, M.T. Champagne, L.A. Copp, & R.A.
arteriosclerotic encephalopathy. Brain, 122, 1349–1355. Wiese (Eds.), Key aspects of recovery (pp. 275–281).
New York: Springer.
Ellis, R., Caligiuri, M., Galasko, D., & Thal, L. (1996).
Extrapyramidal motor signs in clinically diagnosed Hohl, U., Tiraboschi, P., Hansen, L., Thal, L., & Corey-
Alzheimer disease. Alzheimer Disease and Associated Bloom, J. (2000). Diagnostic accuracy of dementia with
Disorders, 10(2), 103–114. Lewy Bodies. Archives of Neurology, 57, 347–351.
Fahn, S., Elton, R., and Members of the UPDRS Johansson, G., & Jarnloo, G.B. (1991). Balance training in
Development Committee. (1987). Unified Parkinson’s 70-year-old women. Physiotherapy Theory and Practice, 7,
Disease Rating Scale. In S. Fahn, C. Marsden, D. Caine, 121–125.
& M. Goldstein (Eds.), Recent developments in Parkinson’s
Krauss, J., Faist, M., Schubert, M., Borremans, J., Lücking, C.,
disease (pp. 153–163, 293–304). Florham Park,
& Berger, W. (2001). Evaluation of gait in normal
NJ: Macmillan Health Care Information.
pressure hydrocephalus before and after shunting.
Fiatarone, M., & Evans, W. (1993). The etiology and Gait Disorders, Advances in Neurology, 87, 301–310.
reversibility of muscle dysfunction in the aged. Journal
of Gerontology, 48, M77–M83. Kressig, R., Gregor, R., Oliver, A., Waddell, D., Smith, W.,
O’Grady, M., et al. (2004). Temporal and spatial features
Franssen, E., Kluger, A., Torossian, C., & Reisberg, B. (1993). of gait in older adults transitioning into frailty. Gait and
The neurologic syndrome of severe Alzheimer’s Posture, 20, 30–35.
Downloaded from https://www.cambridge.org/core. University of Athens, on 24 Feb 2021 at 17:03:47, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms.
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