Anda di halaman 1dari 13

Clinical Neurophysiology 119 (2008) 2424–2436

Contents lists available at ScienceDirect

Clinical Neurophysiology
journal homepage: www.elsevier.com/locate/clinph

Invited review

The clinical utility of posturography


Jasper E. Visser a, Mark G. Carpenter b, Herman van der Kooij c, Bastiaan R. Bloem a,*
a
Department of Neurology, Parkinson Center Nijmegen (ParC), Donders Center for Neuroscience, Radboud University Nijmegen Medical Centre,
P.O. Box 9101, 6500 HB Nijmegen, The Netherlands
b
School of Human Kinetics, University of British Columbia, Vancouver, BC, Canada
c
Department of Biomechanical Engineering, University of Twente, The Netherlands

a r t i c l e i n f o a b s t r a c t

Article history: Postural instability and falls are common and devastating features of ageing and many neurological,
Accepted 30 July 2008 visual, vestibular or orthopedic disorders. Current management of these problems is hampered by the
Available online 12 September 2008 subjective and variable nature of the available clinical balance measures. In this narrative review, we dis-
cuss the clinical utility of posturography as a more objective and quantitative measure of balance and
Keywords: postural instability, focusing on several areas where clinicians presently experience the greatest difficul-
Posturography ties in managing their patients: (a) to make an appropriate differential diagnosis in patients presenting
Clinical utility
with falls or balance impairment; (b) to reliably identify those subjects who are at risk of falling; (c) to
Balance
Postural control
objectively and quantitatively document the outcome of therapeutic interventions; and (d) to gain a bet-
ter pathophysiological understanding of postural instability and falls, as a basis for development of
improved treatment strategies to prevent falling. In each of these fields, posturography offers several the-
oretical advantages and, when applied correctly, provides a useful tool to gain a better understanding of
pathophysiological mechanisms in patients with balance disorders, at the group level. However, based on
the available evidence, none of the existing techniques is currently able to significantly influence the clin-
ical decision making in individual patients. We critically review the shortcomings of posturography as it
is presently used, and conclude with several recommendations for future research.
Ó 2008 International Federation of Clinical Neurophysiology. Published by Elsevier Ireland Ltd. All rights
reserved.

1. Introduction insecure gait or balance – has relatively limited accuracy when


deciding how balance regulation is affected.
Balance impairment is common in elderly people and in pa- Reliably identifying subjects who are at risk of falling is another
tients with a wide range of disorders, including vestibular pathol- clinical challenge. Several clinical tests, e.g. the ‘‘stops walking
ogy, visual or oculomotor impairment, neurological diseases and while talking” test, are able to identify subjects at risk for falls rea-
musculoskeletal disorders (Tinetti, 2003; Voermans et al., 2007). sonably well, but the proportion of false-negative predictions re-
The impact of these balance disorders is enormous, both for af- mains high (Woollacott and Shumway-Cook, 2002; Bloem et al.,
fected individuals and for the society at large. One major concern 2006). Moreover, test execution varies considerably between dif-
includes falls, which are associated with a considerable morbidity, ferent clinicians, and interpretation of the outcome is variable
including trauma, immobilization, and fear of renewed falls (King due to the subjective scoring system.
and Tinetti, 1995; Cumming et al., 2000; Bloem et al., 2001d; Stel A further example of a clinical need is the development of im-
et al., 2004). As a consequence, the quality of life of patients with proved treatment strategies to prevent falls, tailored to individual
balance impairment and falls is markedly diminished. needs. This requires insight into the primary pathological pro-
Against this background, patients with balance impairment re- cesses and secondary compensatory strategies that are employed
quire optimal medical attention, for both diagnostic and therapeu- by patients to reduce falls. What clinicians see in their examination
tic reasons (Table 1). First, it is necessary to make a reliable room is the net result of primary disease processes, plus what the
differential diagnosis in patients presenting with falls or balance patient tries to make of this, both in terms of behavioral compen-
impairment. This may be difficult, probably because the ‘‘disease sation and adaptive plasticity in the nervous system (Bloem et al.,
focused” eye of an experienced clinician – although undoubtedly 2001e; Palop et al., 2006). Unfortunately, clinical balance tests can-
sensitive in detecting that something is wrong in patients with an not reliably separate these two aspects, despite potential therapeu-
tic implications. Moreover, it remains difficult for the naked eye to
* Corresponding author. Tel.: +31 24 3615202; fax: +31 24 3541122. differentiate between causes (i.e. specific abnormalities in postural
E-mail address: B.Bloem@neuro.umcn.nl (B.R. Bloem). control) and effects (i.e. the consequential imbalance).

1388-2457/$34.00 Ó 2008 International Federation of Clinical Neurophysiology. Published by Elsevier Ireland Ltd. All rights reserved.
doi:10.1016/j.clinph.2008.07.220
J.E. Visser et al. / Clinical Neurophysiology 119 (2008) 2424–2436 2425

Table 1 different body parts with respect to each other. Most frequently,
Purposes for assessing balance impairment in clinical practice however, posturography techniques are used to investigate the ac-
 Diagnostic – Differential diagnosis in patients with falls or balance tive and passive regulation of balance under a variety of conditions.
purposes impairment Essential elements of most posturography techniques include the
– Early detection of subjects at risk of falling ability to actively manipulate posture or balance, and evaluate
 Therapeutic – Development of optimal treatment strategies tailored to the subject’s response to such interventions. Available posturogra-
purposes individual needs phy techniques and possible applications have recently been re-
– Objective documentation of therapeutic efficacy
viewed extensively (Bloem et al., 2003). We will now discuss
 Long-term – Improved understanding of underlying pathophysiology, several major principles behind posturography techniques.
purpose as a basis for renewed treatment strategies
It is common practice to allocate a particular posturography
technique to one of two major categories: static posturography
or dynamic posturography (Furman et al., 1993). In static postur-
Finally, clinicians require a reliable tool that can be used to ography, postural control is assessed while subjects maintain
objectively and quantitatively document the outcome of therapeu- stance in a relatively unperturbed state (usually quiet stance on
tic interventions. This is desirable not only in clinical practice to a fixed support surface). However, even unperturbed stance is far
evaluate the success of treatment in individual patients, but also from static due the combined influence of gravity and small self-
in a research setting to assess the outcome in clinical trials. initiated corrective movements (Kuo et al., 1998; Creath et al.,
The current management of patients with postural instability is 2002).
hampered by the intricate assessment of balance disorders. The Dynamic posturography involves the use of experimentally in-
current standard in clinical practice is a combination of history tak- duced balance perturbations (Table 2). A common variant is the
ing and physical examination, but neither approach is infallible. use of a movable support surface upon which subjects are stand-
Asking about the presence of prior falls is unreliable because pa- ing. Platforms can usually move in only one direction, but more re-
tients often forget their falls (Cummings et al., 1988). Clinically cent versions allow for perturbations in multiple directions (Henry
used balance tests are hampered by their variable execution and et al., 1998; Allum et al., 2002). Balance can then be perturbed
subjective scoring system (Munhoz et al., 2004; Jacobs et al., when the support surface makes sudden horizontal translations,
2006). As such, clinical examination of postural control provides rotations, vertical displacements or a combination thereof (Bloem
only a relatively crude and subjective estimate of potential abnor- et al., 2003). Most investigators use rapid and brief perturbations
malities in balance regulation, and may well miss abnormal func- in order to study immediate defensive postural reactions, but slow
tioning of selective elements of the balance repertoire. and oscillatory movements have been used to investigate adapta-
In this narrative review, we discuss the clinical utility of postur- tion, stimulus anticipation and feed-forward postural control
ography, as a more objective and quantitative measure of balance mechanisms (Diener et al., 1982; Dietz et al., 1993). An alternative
and postural instability. ‘‘Utility” is here interpreted in a broad approach is to apply external perturbations aimed directly at upper
sense, i.e. as the answer to the challenges posed in Table 1. This body segments, for example by pushing and pulling the trunk,
also includes the more statistical interpretation of utility in terms shoulder or pelvis (Wolfson et al., 1986; Rietdyk et al., 1999).
of diagnostic yield, for example the sensitivity, specificity or In the remainder of this review, we will discuss static and dy-
responsiveness of a particular posturography application. namic posturography studies together, because many studies use
This narrative review does not intend to provide a comprehensive both techniques simultaneously to address a certain topic.
listing of all available publications, but rather presents a synopsis of
the different applications of posturography in clinical practice. This 2.2. Standardized postural perturbations
will be illustrated using selected key examples from the literature.
Following a brief summary of the potential advantages of various Unlike clinical tests, the specific parameters of the balance dis-
posturography techniques, we will outline several main approaches turbance used in computerized posturography can be controlled by
that are presently available to investigate balance in health and dis- the experimenter, e.g. the peak and time-to-peak acceleration,
ease. We then focus on specific areas where clinicians currently peak velocity or amplitude of the support surface displacements.
experience difficulties in managing their patients. We specifically Each of these variables can affect postural control (Diener et al.,
address the ability of the existing techniques to support the individ- 1984b; Szturm and Fallang, 1998; Brown et al., 2001; Carpenter
ual decision making by clinicians in these areas. In addition, we will et al., 2005). A theoretical advantage is that most motor driven
critically review the shortcomings of posturography as it is presently platforms are independent of inter-subject variations in body mass
used, and provide several recommendations for future research. or mass distribution, as opposed to many clinical balance tests.

2. Advantages of posturography
Table 2
Types of physical perturbations, as used in dynamic posturography (after Bloem et al.
In this section, we will discuss the available posturography
(2003), with permission from the authors)
techniques, and how these applications can overcome the main
drawbacks to the clinically based balance examination: (a) the var- External perturbations
 Moving support surface
iability in test performance (within and across different examin-
– Translation, rotation or vertical displacement
ers); (b) the subjective nature of the scoring system; and (c) the – Unidirectional vs. multidirectional
inability to unravel details of the underlying pathophysiology in – Abrupt vs. continuous (e.g. sinusoidal)
individual patients. Where appropriate, we will illustrate the – Predictable vs. non-predictable stimuli
advantages of posturography by showing a salient application in  Stimuli applied to upper body parts
– Hips
a specific patient population. – Trunk
– Head
2.1. Static and dynamic posturography Self-inflicted perturbations
 Voluntary weight shifts
 Anticipatory postural responses
The term posturography refers – literally – to the description of
 Balancing on unstable support surface
posture, which we interpret as the rather static relative position of
2426 J.E. Visser et al. / Clinical Neurophysiology 119 (2008) 2424–2436

2.3. Manipulating specific elements of postural control 2.3.2. Cognitive manipulation


Another form of manipulation involves the application of sec-
Several manipulations can be introduced to render the stance or ondary or tertiary tasks while subjects maintain their balance.
balancing task more challenging, for example by reducing the size of Such a ‘‘dual task” or multitask paradigm provides insights into
the base of support (e.g. assuming a tandem stance), by decreasing the subject’s ability to simultaneously process tasks of increasing
visual feedback (e.g. eye closure) or by decreasing proprioceptive complexity, and what strategies are employed to deal with such
feedback (e.g. standing on a compliant surface) (Allum et al., complex balance tasks. When the secondary task draws upon cog-
2001a; Bloem et al., 2003; Adkin et al., 2005). It is also possible to nitive resources or demands attention, this paradigm also reveals
use ‘‘sensory perturbations” to selectively manipulate one or more to what extent the primary task, i.e. maintaining balance, is under
specific elements of postural control, and this may provide a better cognitive control. By adding a secondary cognitive task while bal-
understanding of mechanistic, physiological and pathophysiologi- ancing, many researchers have found a deterioration of the pri-
cal principles. Examples include movements of the visual scene mary balance task in normals, in particular when subjects were
(Soechting and Berthoz, 1979), galvanic vestibular stimulation (Fitz- old (see for example Brown et al., 1999; Bloem et al., 2001c)
patrick et al., 1996) or tendon vibration (Polonyova and Hlavacka, although this was not a consistent finding (Bootsma-van der
2001). An unusual manipulation was to test subjects while standing et al., 2003). Such inconsistencies between studies are likely ex-
underwater, and this helped to unveil the presence of graviception plained by differences in experimental design, including the diffi-
as a possible fourth source of afferent information for postural con- culty of the primary (postural) task, the nature and complexity of
trol (Dietz et al., 1992). We will discuss in some detail the clinical the secondary tasks, and in particular by the specific instructions
lessons learned from using two commonly used manipulations: given to the subjects, as this determines where they place their pri-
changes to sensory reweighing, and changes in cognitive load. orities (and where they are willing to accept penalties).
The dual task paradigm also lends itself well for the studies of
2.3.1. Sensory re-weighing patients with balance impairment, and theoretically helps to dis-
Clinically based studies in patients with ‘‘focal” lesions had al- entangle the motor and cognitive contributions to postural insta-
ready pointed to the importance of the three main afferent sensory bility. Although nuances can be found in the literature, the
systems for maintaining postural control – visual, vestibular and overall conclusion is that both secondary motor tasks and second-
proprioceptive – but it took carefully controlled posturography ary cognitive tasks negatively affect postural performance in a
studies to reveal how information from these different systems wide range of patient populations, over and above the effect seen
was centrally weighed and processed (Peterka, 2002; Oie et al., in matched controls (Bloem et al., 2006). More complex tasks have
2002). The starting point in such studies is that sensory perturba- a greater effect than simple secondary tasks (Bond and Morris,
tions provide unreliable cues about body sway and velocity. Under 2000; Bloem et al., 2001b). These effects are seen not only in pa-
ideal circumstances, the sensory flow of such a perturbed sensory tients with predominantly cognitive disorders (such as Alzheimer’s
system should be ignored since it does not serve to stabilize pos- disease) (Alexander et al., 1995; Camicioli et al., 1997) but also in
ture, but rather has a destabilizing effect. As such, sensory pertur- patients with predominantly motor disorders (such as patients
bations clarify how each sensory afferent system contributes to recovering from limb-saving surgery) (De Visser et al., 2001).
balance, and how well subjects can reweigh the available sensory
information in order to maintain balance. 2.4. Objective and quantitative outcome measures
A commercially available application in this field is the Sensory
Organization Test (SOT) or Equitest (NeuroCom International, Posturography allows for a detailed and objective analysis of
Clackamas, Oregon). In the SOT, sensory modalities can be absent postural responses, by using a range of quantifiable measures of pos-
(visual) or conflicting (visual, proprioceptive) by blindfolding and tural control (Table 3). This includes kinetic measures (the causes of
moving the visual surround and/or platform coupled to body sway. movement; related to momentum, inertia, mass, weight and force),
This creates conditions where either visual feedback, propriocep- kinematic measures (actual movements of body segments) or
tive feedback, or both are minimized, forcing the non-perturbed measures of muscle activity such as electromyography (EMG).
sensory channels to compensate. This compensatory ability is com- Combinations are preferable as the different outcome measures pro-
pared to normative data. The SOT is commonly used in clinical re- vide complementary information (‘‘multimodal posturography”).
search. For example, a reduced capacity to weigh different sensory
inputs depending on changes in the environment has been identi- 2.4.1. Kinetics
fied in populations with different balance deficits, including e.g. Kinetic information includes recordings of the center of (foot)
patients with Parkinson’s disease (PD) (Colnat-Coulbois et al., pressure (COP), reactive torques and shear forces applied to the
2005), peripheral vestibular deficits (Peterka, 2002), peripheral
neuropathy (Di Nardo et al., 1999; Reid et al., 2002) or stroke
(Marigold et al., 2004). A recurrent observation (and apparently
one that is irrespective of the specific disorder that is being stud- Table 3
Recording equipment and outcome measures in posturography (after Bloem et al.
ied) is that patients cannot maintain equilibrium under the more (2003), with permission from the authors)
difficult SOT conditions, especially when they are forced to rely
on vestibular input only. A positive approach is that such findings Modality Recording equipment Outcome measure

identify impairments in re-weighing and integrating afferent infor- Kinetics – Forceplates – Center of foot pressure
mation as important and common contributors to postural insta- – Torques
– Shear forces and moments
bility and falls. A more critical interpretation is that this is a very
aspecific finding, simply showing that patients with balance Kinematics – Motion sensors – Center of gravity
– Segment motion
impairment become extra unstable when their postural defence
mechanisms are stressed to the limits. Indeed, it has been ques- – Optical motion analysis – 3-D spatial representation
of body (parts) in time
tioned to what extent the SOT truly addresses vestibulospinal func-
tion (Evans and Krebs, 1999): in patients with bilateral vestibular Electromyography – Surface electrodes – Background muscle activity
– Needle electrodes – Individual postural responses
loss, SOT scores correlate poorly with clinical measures of balance
– Inserted wire electrodes – Postural synergies
control and dynamic gait performance.
J.E. Visser et al. / Clinical Neurophysiology 119 (2008) 2424–2436 2427

support surface, as a function of time. In static posturography resulting in co-contraction, as in patients with PD (Carpenter
experiments, several descriptive measures can be derived from et al., 2004a).
COP information to characterize human postural sway, either in At a group level, some of these changes in postural responses
the time-domain or in the frequency-domain (Prieto et al., 1996). are fairly specific for certain pathological conditions, even though
This approach has been used with reasonable success to demon- this may not be obvious to the clinical eye. For example, a classical
strate, at the group level, abnormalities of the postural control sys- clinical study suggested that balance deficits caused by PD and ves-
tem in various patient populations. Examples include a higher tibular loss could have similar origins (Martin, 1965). This claim
mean velocity in the COP movements due to ageing (Prieto et al., was based on the inspection of simple videographic data which
1996); excessive sway expressed by a larger root mean square of for both groups revealed a similar fall pattern in response to sup-
COP velocities in stroke survivors (Haart et al., 2004); a larger port surface tilts. It took a detailed posturography analysis to iden-
COP displacement and mean velocity after limb saving surgery in tify that PD patients and vestibular loss patients in fact have
certain dual task conditions with eyes closed (De Visser et al., distinct neuromuscular patterns, despite similarities in gross pat-
2001); and a larger COP displacement in vestibular loss patients, terns of instability. Thus, vestibular loss patients have significantly
particularly in the more challenging conditions of the SOT (Black decreased amplitudes of long latency postural responses, followed
et al., 1988). The effect of treatment has been assessed as well, by excessive compensatory activation of muscles (Carpenter
e.g. by showing that the excessive sway in stroke survivors im- et al., 2001a). In contrast, PD is associated with significant increases
proves during the course of rehabilitation (Haart et al., 2004), or in the amplitude of medium and long latency responses in both
that a 1 Hz body sway oscillation – associated with abnormal large agonist and antagonist muscle groups, resulting in co-contraction
and fast COP sway – in PD patients vanishes with levodopa treat- (Schieppati and Nardone, 1991; Dimitrova et al., 2004; Carpenter
ment and deep brain stimulation of the subthalamic nucleus et al., 2004a). The net effect on balance is identical, namely a fall
(Maurer et al., 2004). ‘‘like a log” into the direction of the imposed perturbation, but
the pathophysiology is distinct: hypotonic falls in vestibular loss
2.4.2. Kinematics patients, and stiff falls in PD patients.
The body’s kinematics can be measured using lightweight mo-
tion sensors attached to the body or using optical motion analysis 2.4.4. Biomechanical modeling
systems (Bloem et al., 2003). The latter approach interferes less In addition to actual data derived from human subjects, inverse
with natural body motion, but is more expensive and complex. biomechanical models can be used to calculate joint torques that
The kinematic information can be used to estimate the three- can be fed into a forward biomechanical model to quantify how
dimensional coordinates of the center of mass (COM) (Winter much of the movements are caused by the net actions of muscles
et al., 2003) or to provide insight into postural strategies. This ap- and ligaments crossing a joint. This technique can also calculate
proach has been used to objectively document the magnitude of the effect of gravity, centrifugal and external perturbations on
postural instability (i.e. the amount of COM displacement in re- body movements. This type of analysis showed that in moving
sponse to a postural perturbation) in specific patient populations platform studies, the deceleration counteracts the effects of the
with balance impairment (Bloem et al., 2001c). In addition, de- acceleration, and that the time between acceleration and decelera-
tailed studies of individual body segment displacements have tion is so short that only the first part of the response can be stud-
helped to unravel the pathophysiology of postural instability in ied – and not the complete response to the acceleration (van
specific disorders, sometimes revealing abnormalities that were Asseldonk et al., 2007). This technique has thus far not been used
not immediately apparent clinically. We will provide two exam- in patients.
ples. The first is a dynamic posturography study of patients with
cerebellar ataxia who, unexpectedly, were found to stiffen their
2.4.5. System identification techniques
knees in response to sudden platform tilts (Bakker et al., 2006).
It is difficult to distinguish between cause and effect in patients
This stiffening strategy interfered with the normal rapid compen-
with balance disorders. System identification techniques can offer
satory knee movements that are needed to minimize body sway.
advantages here, as this technique applies an external stimulus
The second example involves the use of kinematic analyses to
and thereby ‘opens the loop’ of a system in which the controlled
study the regulation of protective arm movements (Bateni et al.,
variable (body sway) is fed back to the control variable (muscle
2004), and their changes with, e.g. ageing or neurological disease
activations) (Fitzpatrick et al., 1996). Opening the loop in human
(Allum et al., 2002; Carpenter et al., 2004a).
balance control makes it possible to disentangle different neural
and muscular stabilizing mechanisms from the unstable body
2.4.3. Electromyography
dynamics. Without perturbations, it is impossible to determine if,
The muscular response to postural perturbations can also be
for example, changes in EMG activity result in changes in muscle
quantified, usually with surface EMG techniques. Other techniques
force that will affect body sway, or that the opposite is true, i.e.
include needle EMG to record from very specific and deeply located
changes in body sway angle are detected by sensors and transmit-
muscles (Cresswell et al., 1994), and ultrasound technology to
ted to the nervous system that excites the muscle groups reflected
track muscle movements (Loram et al., 2004). Changes in postural
in EMG changes (Van der Kooij et al., 2005). For example, system
responses can be identified by measuring onset latencies, response
identification techniques have been applied to assess asymmetries
amplitudes or postural strategies (the activation pattern among
in the contribution of the ankle joints of each leg of patients with
different muscles working together). Different techniques for mea-
hemispheric stroke (van Asseldonk et al., 2006) and PD (Van der
suring EMG in posturography experiments have been comprehen-
Kooij et al., 2007), which could not be recognized with the naked
sively reviewed elsewhere (Bloem et al., 2003). EMG studies have
clinical eye.
helped to clarify the nature of balance deficits in many different
disorders, for example by showing delayed (but appropriately
scaled) muscular responses in patients with lower-leg propriocep- 3. Current clinical use of posturography
tive loss (Bloem et al., 2000); or responses that are appropriately
timed, but with excessive or insufficient amplitude, as in patients In the prior section, posturography has been discussed as a tool
with bilateral vestibular loss (Carpenter et al., 2001a); or a poor to objectively and quantitatively assess balance in a standardized
co-ordination of responses between different muscle groups, manner and to understand the physiology and pathophysiology
2428 J.E. Visser et al. / Clinical Neurophysiology 119 (2008) 2424–2436

of postural control, by studying groups of healthy subjects or pa- with bilateral vestibular loss, patients with cerebellar atrophy
tients. The clinical utility of posturography, however, lies in the and healthy controls (Baloh et al., 1998). These examples illustrate
support of decision making in individual patients. We will demon- that group differences do not automatically imply good discrimina-
strate that even the presence of clear differences at the group level tive value.
does not automatically imply that a certain posturography test is
also helpful in managing individual patients. 3.1.2. Diagnostic utility based on disease-specific abnormalities
Another approach focuses on identifying postural abnormalities
3.1. Diagnostic utility that are pathognomonic for specific disorders. For example, a 3 Hz
postural sway is a characteristic posturography finding in anterior
Several studies have attempted to use posturography as a sup- lobe cerebellar atrophy (Diener et al., 1984a). However, its clinical
plement or even surrogate to clinical tests that could assist clini- value is limited as the tremor is clearly visible at the bedside (Baloh
cians in establishing the correct diagnosis. Many techniques have et al., 1998). Another example relates to the patients with primary
been studied, in a wide variety of disease entities (Table 4). Most orthostatic tremor, who manifest a characteristic increase in sway
studies assessed sway using COP recordings or used the commer- activity in higher power spectra frequency bands, with a typical
cially available SOT. The results of these studies were inconsistent, peak between 12 and 19 Hz (Yarrow et al., 2001; Fung et al.,
and frequently the diagnostic yield was unsatisfactory. Neverthe- 2001). This sway frequency nicely correlates to the tremor fre-
less, some evidence for clinical utility of posturography has accu- quency which is usually not discernable to the naked clinical eye,
mulated in selective areas, and several recent developments are but which can be detected using tremor registration with surface
promising, as will be illustrated below. EMG in standing subjects (Piboolnurak et al., 2005). This finding
is perhaps the most specific and best defined abnormality that
3.1.1. Diagnostic utility based on group differences can be identified using posturography. However, application in
Several studies examined whether posturography could assist clinical practice is virtually obviated by the availability of simple
in the differential diagnosis of balance disorders by comparing dif- tremor registration with EMG, which is less complex and much
ferences between groups. For example, analysis of COP displace- cheaper.
ment during quiet stance has been used to discriminate between
41 patients with different types of cerebellar pathology and 20 3.1.3. Diagnostic utility characterized by sensitivity and specificity
controls (Diener et al., 1984a). Although up to 86% of all patients Only few studies have tested the sensitivity and specificity of
showed pathological results, only atrophy of the anterior cerebellar posturography techniques, let alone positive or negative predictive
lobe could be differentiated from other cerebellar pathology, and values. The results varied widely, were often incomplete, or the
some cerebellar lesions could not be differentiated from controls. operational definitions of sensitivity and specificity were inade-
In another study, analysis of COP recordings under static and dy- quate or lacking (Di Fabio, 1995). Moreover, most studies are based
namic conditions could not discriminate well between patients on retrospectively ascertained clinical data, and only few studies

Table 4
Major categories of conditions that have been addressed in studies aiming to evaluate posturography as diagnostic tool: for making the (differential) diagnosis, for estimating fall
risks and for assessing the effect of treatment

Condition (Differential) diagnosis Estimating fall risk Assessing treatment effect


Central nervous system
 Cerebellar diseases Diener et al. (1984a); Baloh et al.
(1998)
 Progressive supranuclear palsy Ondo et al. (2000)
 Parkinson’s disease Bloem et al. (1992) Blaszczyk et al. (2007) Melnick et al. (1999); Rocchi et al. (2002);
Hirsch et al. (2003); Maurer et al. (2003);
Colnat-Coulbois et al. (2005); Shivitz et al.
(2006); Visser et al. (2008)
 Orthostatic tremor Yarrow et al. (2001); Piboolnurak
et al. (2005)
 Stroke Bonan et al. (2004)
 Multipele sclerosis Williams et al. (1997)
 Migraine Dimitri et al. (2001)
 Non-peripheral vertigo and/or Kammerlind et al. (2001)
unsteadiness
Peripheral nervous system
 Peripheral neuropathy Ledin et al. (1990); Uccioli et al.
(1995); Di Nardo et al. (1999); Bloem
et al. (2000); Allum et al. (2001b);
Reid et al. (2002); Nardone and
Schieppati (2007)
 Peripheral vestibular loss Barin et al. (1992); Allum et al. Whitney et al. (2006) O’Neill et al. (1998); Rine et al. (2004)
(2001b)
 Neuritis vestibularis Uimonen et al. (1995)
 Menière’s disease Dimitri et al. (2001)
Other
 Ageing n/a Baloh et al. (1994); n/a
Piirtola and Era (2006)
 Non-organic Goebel et al. (1997)
 Orthopedic disorders Sinaki and Lynn (2002)

Please note that the list of publications is not meant to be exhaustive, but merely to provide an illustration of the wide range of diseases studied.
J.E. Visser et al. / Clinical Neurophysiology 119 (2008) 2424–2436 2429

provide validation of potential diagnostic value in prospective re- sponses, for simple toe-up rotations under eyes-closed conditions.
search (e.g.Buatois et al., 2006). We will discuss a few examples. Although accurate classification was achieved in 71–100% (i.e. sen-
One study found that COP recordings during quiet stance had a sitivity), the results need to be interpreted with caution due to the
sensitivity of 77% and a specificity of 71% for the differentiation be- small number of subjects (5 in each patient group, 15 controls) and
tween simulated vertigo and acute vertigo due to vestibular neuri- lack of specificity measures.
tis (Uimonen et al., 1995). Another study used the aforementioned Taken together, the sensitivity and specificity of posturography
SOT and investigated various criteria by which (volunteering) techniques reported thus far were at best modest. This is illus-
malingerers could be differentiated from both patients with a gen- trated by two meta-analyses (performed over a decade ago), which
uine balance disorder and healthy controls: sensitivity ranged be- showed an overall sensitivity and specificity of only 50% for both
tween 57% and 89%, and specificity between 88% and 100%, static and dynamic posturography (Di Fabio, 1995; Di Fabio,
depending on the criteria used. (Goebel et al., 1997). In PD, pres- 1996). Note, however, that these meta-analyses merely addressed
ence of abnormal postural responses in the lower legs (i.e. en- vestibular function, using vestibular function tests such as electro-
hanced medium latency responses, reduced long latency nystagmography as criterion standard. Therefore, these figures
responses, or both) correctly identified patients with a sensitivity may not apply to other fields of interest. Moreover, there is a need
of 65% and a specificity of 75% (Bloem et al., 1992). This rather poor to perform new meta-analyses to incorporate the latest research
diagnostic yield was explained by the marked overlap between pa- findings.
tients and controls (Fig. 1). Indeed, the clear group differences in Attempts to improve the sensitivity of dynamic posturography
this study were almost exclusively explained by the presence of included modified experimental conditions, e.g. the introduction
abnormal postural responses in severely affected patients – where of a 45 degree lateral head tilt during testing for diagnosing periph-
a screening tool for PD would be useless. Better results were ob- eral vestibular loss – a promising technique at a group level (Barin
tained when the SOT was used to differentiate PD from progressive et al., 1992). However, another study could not extend this group
supranuclear palsy (PSP) (Ondo et al., 2000). For patients in early result to the individual level: the sensitivity of identifying subjects
disease stages, this differential diagnosis can be difficult. The SOT with abnormal caloric testing, rotatory chair testing, or both, was
results showed that postural instability occurred earlier in the only 24% – although the specificity was 90% (Chandra and Shepard,
course of the disease and was more pronounced in PSP compared 1996). The additional value of lateral head tilt compared to stan-
to PD. The best discriminative value was found for the SOT condi- dard testing, i.e. a comparison between analyses with and without
tion with inaccurate visual and proprioceptive input (sensitivity lateral head tilt, was not reported.
95%, specificity 85%), and for a leaning task where subjects actively The use of artificial neural network techniques is a promising
controlled their COP (sensitivity 100%, specificity 95%). However, approach which apparently yields a rather good sensitivity and
average disease duration in these patients was about four years – specificity for distinguishing between different disease entities.
a time when the diagnosis can usually be made based upon clinical For example, postural sway patterns have been used to discrimi-
grounds. A final example is a study that aimed to differentiate be- nate between normal subjects, postural phobic vertigo, anterior
tween bilateral peripheral vestibular loss, proprioceptive deficits lobe cerebellar atrophy, primary orthostatic tremor and acute uni-
due to sensory neuropathy and healthy controls, using different lateral vestibular neuritis (Krafczyk et al., 2006). Sway measures
types of platform perturbations (Allum et al., 2001b). Measures were derived from COP recordings during upright stance. Data
that provided the greatest diagnostic utility were the amplitude from 10 test conditions (e.g. standing on a firm foot support or
of trunk angular velocity, the amplitude of balance-correcting on foam) were fed into a standard 3-layer feed-forward back-prop-
paraspinal responses and the amplitude of trapezius stabilising re- agation neural network, which properly classified the controls and
four patient groups with an overall sensitivity and specificity of
0.93 – with controls and orthostatic tremor being differentiated
best from the other conditions. Further research is obviously justi-
fied to further establish the clinical utility of artificial neural net-
work techniques.

3.2. Predicting the risk of falling

Only few studies specifically aimed to predict falls, mainly in


older people. One outcome measure that was felt to be promising
included sway velocity – particularly in the anterior-posterior
direction – because this is higher in groups of older subjects com-
pared to younger people (Baloh et al., 1994). Subsequent work
showed that sway velocity is higher in subjects with subjective
imbalance compared to age-matched controls who considered
their balance to be normal (Baloh et al., 1995). However, sway
velocity during static and dynamic conditions did not correlate
with the frequency of falls in the previous year (Baloh et al.,
1994). Moreover, self-reported fear of falling was inconsistently
correlated with sway velocity in these studies. Note that posturog-
raphy is not the only one to blame for these poor correlations: a
Fig. 1. Group means (with 95% confidence interval) and individual values for the
normalized amplitude of medium latency balance correcting responses after a toe- general drawback is that many studies ascertained falls retrospec-
up perturbation of the support platform in 23 PD patients with various degree of tively based on self-report, but this approach is unreliable (Cum-
disease severity (Bloem et al., 1992). Although PD patients had a significantly mings et al., 1988).
increased ML amplitude (on the left), there was a marked overlap between patients A recent meta-analysis (including the studies mentioned above)
and controls (on the right). In addition, clear group differences in this study were
explained by the presence of abnormal postural responses in only a few severely
investigated whether posturography measurements can predict
affected patients (i.e. those above the 95% normality threshold). Modified from falls among elderly people (Piirtola and Era, 2006). Associations be-
Bloem et al. (1992), with permission of the authors. tween falls and certain sway parameters (obtained from COP
2430 J.E. Visser et al. / Clinical Neurophysiology 119 (2008) 2424–2436

recordings) were found in only five of nine prospective studies. The rehabilitation program, improvements in SOT were not predictive
key findings were as follows. First, particularly indicators of lateral of changes in a battery of clinical and functional performance tests
balance control could predict subsequent falls. Second, measures (O’Neill et al., 1998).
derived from dynamic posturography tests were not predictive of
future falls. Unfortunately, this analysis did not report sensitivity 4. Drawbacks to current posturography
and specificity measures, which renders the results difficult to
interpret in terms of clinical utility. The preceding sections demonstrate the limited clinical utility
Studies addressing the risk of falling in specific patient popula- of posturography, particularly within individual patients. In the
tions yielded similarly inconsistent results. For example, one study following section, we discuss several poignant dilemmas that
among PD patients found no correlation between sway measures may explain this conclusion (Table 5), and propose several recom-
and falls in the previous year (Blaszczyk et al., 2007). An example mendations for future research.
of a (retrospective) study that aimed to estimate the risk of falling
in individual patients included 100 patients with otherwise 4.1. Subject selection
unspecified vestibular disorders, showing that the composite SOT
equilibrium score was associated with recurrent falls (Whitney 4.1.1. Inter- and intra-subject variability
et al., 2006). In this study, receiver operating characteristic analysis The poor discriminative ability (between health and disease; or
indicated a rather unsatisfactory sensitivity of 53% and a specificity between different diseases) of posturography measures may relate
of 87% – indicating that about half of the recurrent fallers would be to the substantial inter-subject and intra-subject variability
missed by dynamic posturography alone. Another prospective (Fig. 2). Even healthy subjects without postural impairment can
study demonstrated that loss of balance in the most demanding show considerable variability in their postural responses (Geurts
SOT test with inappropriate somatosensory and visual input (i.e. et al., 1993; Chandra and Shepard, 1996). This variability will neg-
with sway referenced support platform and visual surround) atively affect the test-retest reliability of posturography, but only
would predict recurrent falls within the next 16 months in healthy few studies have specifically examined this – and reports are
volunteers over 65 years, with an odds-ratio of 3.6 (Buatois et al., inconclusive (Geurts et al., 1993; Benvenuti et al., 1999; Helbostad
2006). In this study, however, other types of COP derived measures et al., 2004). It appears that the test-retest reliability of posturo-
were not associated with falling, and sensitivity and specificity graphic measures is highly dependent on the type of measure;
were not given. age and disease conditions of the subjects; and the difficulty of
the balance task involved. To reduce inter-subject variability, it is
3.3. Evaluating the effect of therapeutic interventions important to select homogeneous groups. For example, including
subjects who differ widely in age may introduce extra variability
Various posturography studies investigated the effects of spe- because balance reactions change substantially with ageing (Ledin
cific treatment strategies on balance and postural control – usually et al., 1990; Baloh et al., 1994; Uimonen et al., 1995; Allum et al.,
at the group level. An area that received considerable attention is 2002).
the possible effect of bilateral deep brain stimulation on postural
control in PD. The results of static posturography were inconsis- 4.1.2. Single or multiple disease entities
tent: the effect of STN stimulation has been reported to either de- Additional variability may be caused by lumping different con-
crease (Rocchi et al., 2002; Colnat-Coulbois et al., 2005) or increase ditions into one ‘‘disease group”, because disease-specific abnor-
sway amplitudes (Maurer et al., 2003). This inconsistency may be malities could create inconsistency in the outcome measures. The
explained by differences in patient selection, in particular the exact nature of the disease is sometimes insufficiently specified,
severity of concurrent dyskinesias. Certain aspects of the SOT have e.g. ‘‘vestibular disorders” or ‘‘disturbances in the nervous system”.
been reported to improve with bilateral STN stimulation (but not Another source of heterogeneity is introduced when the systems
with antiparkinson medication) in a subset of patients who per- affected by the disease differ among subjects, such as in multiple
formed poorly before surgery, suggesting better sensory-motor sclerosis or stroke. Likewise, interventions should be applied uni-
integration (Shivitz et al., 2006). Another study found no overall formly across subjects to reduce variability in outcome. And for
improvement in stability over and above optimal medication, obvious reasons, study groups should be carefully matched for age.
although individual subjects seemed to benefit substantially (Vis-
ser et al., 2008). This has also been demonstrated for pallidotomy
in PD (Melnick et al., 1999), and is in line with clinical experience
in most studies (Bakker et al., 2004). Table 5
Summary of potential drawbacks of posturography as it is currently experienced
The effect of balance training has also been investigated in dif-
ferent disease populations, usually with the SOT as primary out- Study phase Examples
come. In PD, balance and resistance training improved Subject selection  Inter- and intra-subject variability
performance on the SOT, particularly for the more difficult condi-  Single or multiple disease entities
tions (Hirsch et al., 2003). In addition, the numbers of falls during  Disease severity
 Selection bias
testing decreased, and stance duration without falling lengthened.
Similar improvements have been reported in stroke patients (Bo- Data collection  Sample duration (static posturography)
 Platform deceleration (dynamic posturography)
nan et al., 2004), elderly subjects with otherwise unspecified cen-
 EMG processing
tral nervous system dysfunction (Kammerlind et al., 2001),  Habituation and ‘‘first trial effects”
children with bilateral vestibular loss (Rine et al., 2004) and oste-  Influence of cognitive and emotional factors
oporotic women (Sinaki and Lynn, 2002).  Influence of pre-stimulus posture
Such studies illustrate the potential role for posturography in  Presence of external support

evaluating the effect of treatment on postural control, but it re- Data analysis and  Choice of descriptive measures for postural
mains to be determined whether posturography provides a helpful interpretation control
 Meaning of sway
tool over and above clinical judgment. One study suggested that
 Statistical concerns
this may not be the case: among 37 subjects with peripheral ves-  Ecological validity
tibular hypofunction who were tested before and after a vestibular
J.E. Visser et al. / Clinical Neurophysiology 119 (2008) 2424–2436 2431

4.2. Data collection

4.2.1. Sampling duration


One factor which significantly affects posturography measures
is the sampling duration and frequency. Across and within static
posturography studies, sampling duration has varied from several
seconds to 30 min. Several studies have shown that the sampling
duration significantly affects descriptive measures in both the time
and frequency domain (Le Clair and Riach, 1996; Carpenter et al.,
2001c). Extended periods of standing may reveal aspects of pos-
tural sway that are not otherwise observable during shorter sam-
pling periods (Duarte and Zatsiorsky, 2000), because longer
sample durations allow the large amplitude, low frequency compo-
nents of the COP signal to be adequately represented in descriptive
measures (Carpenter et al., 2001c).

4.2.2. Effect of platform deceleration


In dynamic posturography studies using a movable platform,
the acceleration of the support surface represents the true
mechanical perturbation – not the platform displacement or veloc-
ity. What is often forgotten is that the support surface, after the ini-
tial acceleration, by necessity also needs to decelerate when the
maximum excursion has been reached. Importantly, this decelera-
tion of support platform movements may be another potential
source of misinterpretation of posturography data. Because the
stroke of the platform is limited to a few decimeters in most labo-
ratories, the acceleration–deceleration interval is short, so reactive
postural responses elicited by platform acceleration could mix and
interfere with responses triggered by deceleration (McIlroy and
Maki, 1994). This is especially true for the measured COP, joint tor-
que and body sway. In addition, anticipatory mechanisms could be
Fig. 2. Illustration of large inter-subject variability in posturography: the mean and used to adjust the initial response to, and utilize, non-muscular
standard deviation for two joint angles are shown, as measured with optical 3D torques generated by platform deceleration (Bothner and Jensen,
tracking. Both trunk roll angle after a rightward directed platform perturbation 2001). As shown in Fig. 3, support-surface translations with a long
(relative to a baseline position set at 0 deg, A) and left knee angle for a forward
directed perturbation (absolute values, B) in a group of 18 healthy volunteers and
acceleration–deceleration interval (i.e. 2 s) compared to a short
14 patients with Parkinson disease (PD). Note that while mean values can differ interval (i.e. 100 ms) induce larger trunk displacements and also
considerably between groups, differences are obscured by the substantial standard require larger amplitude EMG responses. During perturbations
deviation. The onset of the perturbation is denoted by the vertical dashed line with a short acceleration–deceleration interval, activity in some
(Visser, unpublished data).
antagonists muscles was associated with the deceleration and
not with the initial acceleration of the support surface (Carpenter
et al., 2005). Finally, the deceleration may also help to stabilize up-
right posture by mechanically countering the effect of the preced-
4.1.3. Disease severity ing acceleration, thereby possibly obscuring more pronounced
Compared to controls, standard deviations are usually greater in balance difficulties (van Asseldonk et al., 2007). This inherent lim-
patient populations, for several reasons. First, abnormalities may itation applies to the vast majority of currently available movable
depend upon disease severity, and patients in various disease platform systems, and limits the ecological validity of the obtained
stages are usually included in posturography studies. Furthermore, findings.
including patients with very advanced disease tend to be very
unstable and become easily fatigued, and this can negatively affect 4.2.3. EMG processing
the quality of the data. Patients with late-stage disease are also Many issues regarding EMG processing have not been standard-
prone to develop secondary disease complications, for example ized. The resultant methodological inconsistency across labs ham-
drug-induced dyskinesias in advanced PD or joint deformations pers an easy comparison among different studies. Examples
in advanced polyneuropathy, and this further increases variability include the many variants that are available to correct for the con-
in the data. Finally, patients often have co-morbid conditions that founding influence of variations in background muscle activity
are independent from the disease under study, but that need to be (Bloem et al., 1993), or to normalize EMG data. It would be desir-
carefully controlled for in order to reduce variability. able to reach consensus about such issues.

4.2.4. Habituation and ‘‘first trial” effects


4.1.4. Selection bias To reduce the high variability of human postural responses,
Selection bias may be introduced when studies focusing on the most investigators average their data over multiple trials. How-
clinical utility of posturography use baseline posturography results ever, postural responses typically habituate, i.e. the response
to define the groups (i.e. baseline posturography is used to define magnitude decreases when the subjects are serially exposed to
inclusion criteria). For example, this occurs when subjects are re- balance perturbations, especially if the stimuli are identical
quired to have normal posturography tests in order to be included (e.g. same perturbation direction and size) (Keshner et al.,
in the control group (Chandra and Shepard, 1996; Goebel et al., 1987; Hansen et al., 1988; Bloem et al., 1998). The response to
1997). very first and fully unpracticed trial is typically excluded from
2432 J.E. Visser et al. / Clinical Neurophysiology 119 (2008) 2424–2436

negative emotional responses (Facchinetti et al., 2006). Also,


amplitudes of long latency muscular responses to unexpected sup-
port-surface rotations increase when subjects stand on high com-
pared to low surface heights (Carpenter et al., 2004b). Based on
these findings, fear and anxiety should be considered as a poten-
tially confounding variable that needs to be controlled, or at least
measured. In particular, comparisons of postural performance in
groups that may have different levels of fear or anxiety may mask
or mimic physiological differences. Furthermore, emotional state
may change over time, or with increasing familiarity with test con-
ditions, and thereby influence results that are based upon time-
dependent measurements.

4.2.6. Influence of pre-stimulus posture


An often neglected factor is the prestimulus posture and base-
line COP position of subjects. Subjects may purposely adjust their
prestimulus posture in order to brace themselves against upcom-
ing perturbations. This anticipatory postural leaning is common
when subjects have prior information about the direction of an
upcoming perturbation. For example, subjects who are exposed
to a predictable series of identical toe-up rotational platform dis-
placements gradually assume a stooped posture (Maki and White-
law, 1993; Tarantola et al., 1997). In addition, prestimulus posture
can be abnormal in patients with neurological disorders, e.g. the
stooped posture in PD or the asymmetric stance in patients with
stroke. Such changes in baseline posture can in turn affect the on-
set latencies and amplitudes of lower leg postural responses
(Bloem et al., 1999). Interestingly, quiet standing is also associated
with continuous ‘‘spontaneous” changes in COM and COP, and even
these subtle changes are sufficient to influence postural reactions
to unpredictable perturbations. For example, both onset latency
Fig. 3. Single subject average of trunk angular displacement recorded from an older and amplitude of postural muscle responses to support-surface
adult highlights the increased challenge induced by support-surface translations
translations are significantly influenced by spontaneous fluctua-
with a LONG (2000 ms = solid lines) compared to a SHORT (100 ms = dashed lines)
acceleration–deceleration interval (Carpenter, unpublished data). tions in position of the COP at the time of perturbation onset (Tok-
uno et al., 2006). Baseline stance should therefore be controlled
and monitored carefully, for example by providing subjects with
further analysis, because this response appears to be very differ- visual feedback about their own initial stance and by stalling the
ent from the reactions seen in subsequent trials (Hansen et al., experiment while baseline posture is outside predefined accept-
1988). This ‘‘first trial reaction” is sometimes referred to as a able ranges (Bakker et al., 2006; Visser et al., 2008). Any residual
startle-like response, although the relation to the startle proper differences in baseline stance could be entered into the statistical
– as evoked by loud acoustic stimuli – remains unclear. A draw- analyses as covariate.
back to this averaging procedure is a potential loss of valuable
information which was only present in the first few trials. Spe- 4.2.7. Presence of external support
cifically, the first trial reaction may provide useful insights into A relevant environmental factor is the presence and character-
the mechanisms associated with truly unexpected falls, and istics of any external support in order to reduce the risk of falls,
thereby provide ecologically information about falling in every- for example by equipping subjects with a safety harnesses, by
day life where perturbations are also singular (i.e. ‘‘the first”) providing handrails or by positioning research assistants close
and unpredictable events. to the tested subject. While understandable for ethical reasons,
use of such protective measures may falsely increase the subject’s
4.2.5. Influence of cognitive and emotional factors balance confidence and reduce their fear of falling, and thereby
Another relevant factor is the contribution of cognitive and unintentionally change postural performance from that experi-
emotional factors. Fear of falling is common in older adults (Yard- enced by the patient in everyday life. A further – theoretical –
ley and Smith, 2002) and is particularly pronounced in patients disadvantage of the safety harness is that it provides subjects
with balance disorders (Bloem et al., 2001a; Watanabe, 2005). Fear with tactile or pressure-sensitive feedback about their amount
of falling can, its own right, affect postural performance. For exam- of sway and thereby may affect postural performance. Indeed,
ple, elderly persons who are afraid of falling have significantly lar- even small amounts of proprioceptive feedback (a finger lightly
ger spontaneous COP displacements compared to non-fearful touching an external frame) can markedly affect postural re-
elderly (Maki et al., 1991). Likewise, patients with phobic postural sponses (Dickstein et al., 2001). Despite this concern, the few
vertigo have significantly higher frequency components of COP dis- studies that have formally studied the influence of safety har-
placements compared to controls (Krafczyk et al., 1999). There is nesses, deny that a safety harness significantly alters balance re-
growing evidence to support a direct link between fear or anxiety sponses to external perturbations (Freitas et al., 2005) or sway
and ‘‘postural performance”. Significant changes in the amplitude during quiet standing (Hill et al., 1994). It has been demonstrated,
and frequency of COP displacements have been observed when however, that handrails can influence the ensuing postural re-
subjects are required to stand in conditions of increased postural sponses, and this apparently depends on their proximity to the
threat, e.g. standing on the edge of a high surface (Carpenter subjects and the prior instructions (Bateni et al., 2004; Maki
et al., 2001b) or when presented with pictures designed to elicit and McIlroy, 2006).
J.E. Visser et al. / Clinical Neurophysiology 119 (2008) 2424–2436 2433

4.3. Data analysis and interpretation we already alluded to the confounding effect of decelerations in
moving platform experiments which are absent in daily life. An-
4.3.1. Choice of descriptive measures for postural control other problem is the need to test subjects repeatedly in order to
Comparisons between posturography studies are difficult be- better separate signals from noise, but this leads to habituation ef-
cause of the vast number of descriptive measures used to charac- fects that do not occur when subjects suddenly fall in daily life. Fi-
terize balance. There is currently no agreement within the field nally, most studies limit the number of available response
which parameters should be considered standard, or are superior strategies, i.e. by restricting subjects to respond with feet-in-place
in describing balance control.One of the reasons for this lack of responses, despite the tendency for other ‘change in support reac-
agreement regarding choice of outcome measures in posturogra- tions’, such as stepping and reaching responses, to be employed
phy experiments is probably the absence of a widely accepted gold during unrestricted falls (see for review: Maki and McIlroy, 2006).
standard for balance, i.e. a definitive test that could serve as refer- A final drawback of current posturography techniques is that
ence for the evaluation of posturography variables and tests. A these usually address a small subset of the actual balance reper-
popular outcome measure is recording of COP, which is often equa- toire. Virtually all studies focus on erect standing, while in daily life
ted with ‘‘body sway”. However, this is only correct if the body more dynamic balance skills are required – involving complex
moves as a rigid pendulum – which is often not the case – and only coordination, e.g. standing up, reaching or picking object, stum-
when sway angles and inertial forces are small. It is also unknown bling and turning. Importantly, falls in daily life occur mostly dur-
how the COP signal is optimally described. Depending on the spe- ing such more complex skills. So perhaps we are looking at the
cific cause, postural instability can be identified better using veloc- wrong – or too few – aspects of everyday balance.
ity-related sway measures compared to displacement-related
sway measures. This was demonstrated for PD (Rocchi et al.,
2002; Maurer et al., 2003), peripheral neuropathy (Uccioli et al., 5. Conclusions and future recommendations
1995) and ageing (Prieto et al., 1996).
By using carefully controlled experimental conditions, with cal-
4.3.2. Meaning of sway ibrated control of the environment, standardized bodily perturba-
Sway is interpreted as the reflection of noise and regulatory tions and use of a comprehensive set of quantitative outcome
activity within postural control loops. It is, however, unknown measures, posturography has allowed for a detailed analysis of
why postural sway occurs during stance and what potential char- the complex pathophysiology of balance disorders in groups of pa-
acteristics of a change in sway behavior represent a balance defi- tients. Relatively few studies have addressed the clinical utility in
ciency. There is in fact little scientific agreement on what sway individual patients, and despite some promising initial findings,
actually represents. In biomechanical terms, the COP displacement the results have not convincingly shown superiority over clinically
is the controlling variable, reflecting the net-neuromuscular re- available parameters. The lack of a standardized protocol for quan-
sponses generated by the CNS to maintain control over the COM, titative posturography makes it difficult to compare the results of
the controlled variable (Winter et al., 2003). In this view, the different studies, and this hampers easy implementation in clinical
COM displacement is an undesired effect, which needs to be min- practice. An important concern is the lack of ecological validity,
imized by the CNS through adjustments in COP either through and this may explain why currently available posturography mea-
feedforward (Gatev et al., 1999) or feedback (Johansson et al., sures correlate poorly with the clinical performance and the pro-
1988) mechanisms. However, the reasons for why the COM is con- pensity to fall in daily life. The high costs and the dependence on
tinuously moving remain unknown, and there is no consensus as to technical expertise also render posturography less attractive for
whether sway is beneficial or unhelpful. Consequently, it remains clinicians. Taken together, it is still too early for posturography –
unclear how to separate ‘‘good” from ‘‘bad” sway. as it is currently used – to be applied in current clinical practice
and influence the day-to-day management of individual patients.
4.3.3. Statistical concerns Further work is needed to improve the clinical utility of postur-
Given the many uncertainties, many researchers therefore re- ography, and we would like to propose a few suggestions. First, fu-
cord a broad range of different parameters. Such ‘‘multimodal” ture studies should include homogeneous patient groups, in terms
assessments may be advantageous in being comprehensive, but of, e.g. diagnosis and stage of disease. Second, there is a clear need
interpretation of a significant finding must be made with care be- for standardized protocols if meaningful interpretation and com-
cause individual measures may be interrelated (Maurer and Peter- parisons are to be derived from posturography experiments in dif-
ka, 2005). Multivariate analyses are required, with appropriate ferent labs. The test-retest reliability of such protocols should be
statistical correction for multiple comparisons. It can be helpful determined. Third, when studies aim to test the clinical utility of
to increase the strength of the statistics through data reduction, a certain posturography approach, the results should be character-
e.g. by merging variables into a single variable. For example, in a ized in terms of sensitivity and specificity, and preferably also the
study determining the effect of STN deep brain stimulation on bal- positive and negative predictive value.
ance control in PD, all optically derived kinetic data of 11 body seg- Insufficient methodological detail found in papers evaluating
ments were congregated into one single variable: the vector length the clinical utility of a measure is not unique to the field of postur-
of three-dimensional COM displacement (Visser et al., 2008). And, ography research (Reid et al., 1995). As a guideline for future re-
in order to prove clinical utility, e.g. for diagnosing individual pa- search, researchers could follow the Standards for Reporting of
tients, tests should be characterized by sensitivity and specificity Diagnostic criteria (STARD) – a consensus statement published
– as mentioned before. integrally in several leading journals in 2003, about how to con-
duct and report studies of medical tests (Bossuyt et al., 2003).
4.3.4. Ecological validity More work is also needed to improve the ecological validity of
An overriding concern is the lack of ecological validity in pos- posturography. An interesting development is the use of moving
turography experiments. This begins with the simple fact that sub- platforms capable of delivering perturbations with delayed decel-
jects know that their balance is about to be tested, under highly erations, as this comes closer to real-life conditions such as those
artificial conditions where subjects are equipped with multiple experienced on a bus or subway (De Graaf and Van Weperen,
EMG electrodes or LEDs, and perhaps are being viewed by a set 1997). Others are working to incorporate moving support surfaces
of cameras. The postural perturbations are usually very unnatural; into natural environments such as a living room.
2434 J.E. Visser et al. / Clinical Neurophysiology 119 (2008) 2424–2436

Cost-effectiveness is another aspect that deserves more atten- Bloem BR, Beckley DJ, van Dijk JG. Are automatic postural responses in patients with
Parkinson’s disease abnormal due to their stooped posture? Exp Brain Res
tion in future studies, because this is an important factor in the
1999;124(4):481–8. Feb.
evaluation of the clinical, day-to-day, usefulness of posturography. Bloem BR, Beckley DJ, van Dijk JG, Zwinderman AH, Roos RA. Are medium and long
However, this aspect has not been addressed systematically. latency reflexes a screening tool for early Parkinson’s disease? J Neurol Sci
Although posturography has been considered among the more 1992;113(1):38–42. Nov.
Bloem BR, Grimbergen YA, Cramer M, Willemsen M, Zwinderman AH. Prospective
cost-effective tests for diagnosing vertigo in a retrospective study assessment of falls in Parkinson’s disease. J Neurol 2001a;248(11):950–8. Nov.
(Stewart et al., 1999), posturography experiments are usually Bloem BR, Grimbergen YA, van Dijk JG, Munneke M. The ‘‘posture second” strategy:
rather labor-intensive and typically require expensive equipment. a review of wrong priorities in Parkinson’s disease. J Neurol Sci 2006;248(1–
2):196–204. Oct 25.
Data processing and interpretation can also be time-consuming, Bloem BR, Valkenburg VV, Slabbekoorn M, van Dijk JG. The multiple tasks test.
although some standardized and automated procedures are avail- Strategies in Parkinson’s disease. Exp Brain Res 2001b;137(3–4):478–86. Apr.
able for commercially available equipment. Bloem BR, Valkenburg VV, Slabbekoorn M, Willemsen MD. The Multiple Tasks Test:
development and normal strategies. Gait Posture 2001c;14(3):191–202. Dec.
Finally, one question – and perhaps the most important one – Bloem BR, van Dijk JG, Beckley DJ, Zwinderman AH, Remler MP, Roos RA. Correction
remains unanswered: what is the ‘‘ultimate value” of posturogra- for the influence of background muscle activity on stretch reflex amplitudes. J
phy, in particular to improve clinical care – for example by afford- Neurosci Methods 1993;46(2):167–74. Feb.
Bloem BR, van Vugt JP, Beckley DJ. Postural instability and falls in Parkinson’s
ing more appropriate treatment because of a better diagnosis, or an disease. Adv Neurol 2001d;87:209–23.
improved outcome in a therapeutic setting. Until these results be- Bloem BR, van Vugt JP, Beckley DJ, Remler MP, Roos RA. Habituation of lower leg
come available, posturography remains a useful scientific tool to stretch responses in Parkinson’s disease. Electroencephalogr Clin Neurophysiol
1998;109(1):73–7. Feb.
unravel the complex pathophysiology of balance disorders.
Bloem BR, Visser JE, Allum JH. Posturography. In: Hallett M, editor. Movement
disorders – handbook of clinical neurophysiology. Elsevier; 2003. p. 295–336.
Acknowledgements Bloem BR, Visser JE, Carpenter MG. Compensatory strategies in patients with
longstanding balance impairment. In: Van de Burg JCE, Fong BF, Hijl MIJ, Huys R,
Pijnappels M, Post AA, editors. Balance at all times. Proceedings of the fifth
This project was sponsored by a grant from the Prinses Beatrix symposium of the institute for fundamental and clinical human movement
Fonds to Dr. J.E. Visser and Dr. B.R. Bloem. Dr. Bloem was also sup- sciences.Amsterdam: IFKB; 2001e. p. 51–73.
ported by an NWO VIDI research Grant (#016.076.352). Dr. M.G. Bonan IV, Yelnik AP, Colle FM, Michaud C, Normand E, Panigot B, et al. Reliance on
visual information after stroke. Part II: Effectiveness of a balance rehabilitation
Carpenter was supported by funding from the Natural Sciences program with visual cue deprivation after stroke: a randomized controlled trial.
and Engineering Research Council of Canada. Dr. ir. H. van der Kooij Arch Phys Med Rehabil 2004;85(2):274–8. Feb.
was supported by the Netherlands Organization of Scientific Re- Bond JM, Morris M. Goal-directed secondary motor tasks: their effects on gait in
subjects with Parkinson disease. Arch Phys Med Rehabil 2000;81(1):110–6. Jan.
search (’Vernieuwings-impuls’ 2001, #016027011). Bootsma-van der WA, Gussekloo J, de Craen AJ, van EE, Bloem BR, Westendorp RG.
Walking and talking as predictors of falls in the general population: the Leiden
References 85-Plus Study. J Am Geriatr Soc 2003;51(10):1466–71. Oct.
Bossuyt PM, Reitsma JB, Bruns DE, Gatsonis CA, Glasziou PP, Irwig LM, et al. The
STARD statement for reporting studies of diagnostic accuracy: explanation and
Adkin AL, Bloem BR, Allum JH. Trunk sway measurements during stance and gait
elaboration. Ann Intern Med 2003;138(1):W1–W12. Jan 7.
tasks in Parkinson’s disease. Gait Posture 2005;22(3):240–9. Nov.
Bothner KE, Jensen JL. How do non-muscular torques contribute to the kinetics of
Alexander NB, Mollo JM, Giordani B, shton-Miller JA, Schultz AB, Grunawalt JA, et al.
postural recovery following a support surface translation? J Biomech
Maintenance of balance, gait patterns, and obstacle clearance in Alzheimer’s
2001;34(2):245–50. Feb.
disease. Neurology 1995;45(5):908–14. May.
Brown LA, Jensen JL, Korff T, Woollacott MH. The translating platform paradigm:
Allum JH, Adkin AL, Carpenter MG, Held-Ziolkowska M, Honegger F, Pierchala K.
perturbation displacement waveform alters the postural response. Gait Posture
Trunk sway measures of postural stability during clinical balance tests: effects
2001;14(3):256–63. Dec.
of a unilateral vestibular deficit. Gait Posture 2001a;14(3):227–37. Dec.
Brown LA, Shumway-Cook A, Woollacott MH. Attentional demands and postural
Allum JH, Bloem BR, Carpenter MG, Honegger F. Differential diagnosis of
recovery: the effects of aging. J Gerontol A Biol Sci Med Sci
proprioceptive and vestibular deficits using dynamic support-surface
1999;54(4):M165–71. Apr.
posturography. Gait Posture 2001b;14(3):217–26. Dec.
Buatois S, Gueguen R, Gauchard GC, Benetos A, Perrin PP. Posturography and risk of
Allum JH, Carpenter MG, Honegger F, Adkin AL, Bloem BR. Age-dependent variations
recurrent falls in healthy non-institutionalized persons aged over 65.
in the directional sensitivity of balance corrections and compensatory arm
Gerontology 2006;52(6):345–52.
movements in man. J Physiol 2002;542(Pt 2):643–63. Jul 15.
Camicioli R, Howieson D, Lehman S, Kaye J. Talking while walking: the effect of a
Bakker M, Allum JH, Visser JE, Gruneberg C, van de Warrenburg BP, Kremer BH, et al.
dual task in aging and Alzheimer’s disease. Neurology 1997;48(4):955–8. Apr.
Postural responses to multidirectional stance perturbations in cerebellar ataxia.
Carpenter MG, Allum JH, Honegger F. Vestibular influences on human postural
Exp Neurol 2006;202(1):21–35. Nov.
control in combinations of pitch and roll planes reveal differences in
Bakker M, Esselink RA, Munneke M, Limousin-Dowsey P, Speelman HD, Bloem BR.
spatiotemporal processing. Exp Brain Res 2001a;140(1):95–111. Sep.
Effects of stereotactic neurosurgery on postural instability and gait in
Carpenter MG, Allum JH, Honegger F, Adkin AL, Bloem BR. Postural abnormalities to
Parkinson’s disease. Mov Disord 2004;19(9):1092–9. Sep.
multidirectional stance perturbations in Parkinson’s disease. J Neurol
Baloh RW, Fife TD, Zwerling L, Socotch T, Jacobson K, Bell T, et al. Comparison of
Neurosurg Psychiatry 2004a;75(9):1245–54. Sep.
static and dynamic posturography in young and older normal people. J Am
Carpenter MG, Frank JS, Adkin AL, Paton A, Allum JH. Influence of postural anxiety
Geriatr Soc 1994;42(4):405–12. Apr.
on postural reactions to multi-directional surface rotations. J Neurophysiol
Baloh RW, Jacobson KM, Beykirch K, Honrubia V. Static and dynamic posturography
2004b;92(6):3255–65. Dec.
in patients with vestibular and cerebellar lesions. Arch Neurol
Carpenter MG, Frank JS, Silcher CP, Peysar GW. The influence of postural threat on
1998;55(5):649–54. May.
the control of upright stance. Exp Brain Res 2001b;138(2):210–8. May.
Baloh RW, Spain S, Socotch TM, Jacobson KM, Bell T. Posturography and balance
Carpenter MG, Frank JS, Winter DA, Peysar GW. Sampling duration effects on centre
problems in older people. J Am Geriatr Soc 1995;43(6):638–44. Jun.
of pressure summary measures. Gait Posture 2001c;13(1):35–40. Feb.
Barin K, Seitz CM, Welling DB. Effect of head orientation on the diagnostic
Carpenter MG, Thorstensson A, Cresswell AG. Deceleration affects anticipatory and
sensitivity of posturography in patients with compensated unilateral lesions.
reactive components of triggered postural responses. Exp Brain Res
Otolaryngol Head Neck Surg 1992;106(4):355–62. Apr.
2005;167(3):433–45. Dec.
Bateni H, Zecevic A, McIlroy WE, Maki BE. Resolving conflicts in task demands
Chandra NS, Shepard NT. Clinical utility of lateral head tilt posturography. Am J Otol
during balance recovery: does holding an object inhibit compensatory
1996;17(2):271–7. Mar.
grasping? Exp Brain Res 2004;157(1):49–58. Jul.
Colnat-Coulbois S, Gauchard GC, Maillard L, Barroche G, Vespignani H, Auque J, et al.
Benvenuti F, Mecacci R, Gineprari I, Bandinelli S, Benvenuti E, Ferrucci L, et al.
Bilateral subthalamic nucleus stimulation improves balance control in
Kinematic characteristics of standing disequilibrium: reliability and validity of a
Parkinson’s disease. J Neurol Neurosurg Psychiatry 2005;76(6):780–7. Jun.
posturographic protocol. Arch Phys Med Rehabil 1999;80(3):278–87. Mar.
Creath R, Kiemel T, Horak F, Jeka JJ. Limited control strategies with the loss of
Black FO, Shupert CL, Horak FB, Nashner LM. Abnormal postural control associated
vestibular function. Exp Brain Res 2002;145(3):323–33. Aug.
with peripheral vestibular disorders. Prog Brain Res 1988;76:263–75.
Cresswell AG, Oddsson L, Thorstensson A. The influence of sudden perturbations on
Blaszczyk JW, Orawiec R, Duda-Klodowska D, Opala G. Assessment of postural
trunk muscle activity and intra-abdominal pressure while standing. Exp Brain
instability in patients with Parkinson’s disease. Exp Brain Res
Res 1994;98(2):336–41.
2007;183(1):107–14. Oct.
Cumming RG, Salkeld G, Thomas M, Szonyi G. Prospective study of the impact of
Bloem BR, Allum JH, Carpenter MG, Honegger F. Is lower leg proprioception
fear of falling on activities of daily living, SF-36 scores, and nursing home
essential for triggering human automatic postural responses? Exp Brain Res
admission. J Gerontol A Biol Sci Med Sci 2000;55(5):M299–305. May.
2000;130(3):375–91. Feb.
J.E. Visser et al. / Clinical Neurophysiology 119 (2008) 2424–2436 2435

Cummings SR, Nevitt MC, Kidd S. Forgetting falls. The limited accuracy of recall of Kammerlind AS, Hakansson JK, Skogsberg MC. Effects of balance training in elderly
falls in the elderly. J Am Geriatr Soc 1988;36(7):613–6. Jul. people with nonperipheral vertigo and unsteadiness. Clin Rehabil
De Graaf B, Van Weperen W. The retention of balance: an exploratory study into the 2001;15(5):463–70. Oct.
limits of acceleration the human body can withstand without losing Keshner EA, Allum JH, Pfaltz CR. Postural coactivation and adaptation in the sway
equilibrium. Hum Factors 1997;39(1):111–8. Mar. stabilizing responses of normals and patients with bilateral vestibular deficit.
De Visser E, Deckers JA, Veth RP, Schreuder HW, Mulder TW, Duysens J. Exp Brain Res 1987;69(1):77–92.
Deterioration of balance control after limb-saving surgery. Am J Phys Med King MB, Tinetti ME. Falls in community-dwelling older persons. J Am Geriatr Soc
Rehabil 2001;80(5):358–65. May. 1995;43(10):1146–54. Oct.
Di Fabio RP. Sensitivity and specificity of platform posturography for identifying Krafczyk S, Schlamp V, Dieterich M, Haberhauer P, Brandt T. Increased body sway at
patients with vestibular dysfunction. Phys Ther 1995;75(4):290–305. Apr. 3.5–8 Hz in patients with phobic postural vertigo. Neurosci Lett
Di Fabio RP. Meta-analysis of the sensitivity and specificity of platform 1999;259(3):149–52. Jan 15.
posturography. Arch Otolaryngol Head Neck Surg 1996;122(2):150–6. Feb. Krafczyk S, Tietze S, Swoboda W, Valkovic P, Brandt T. Artificial neural network: a
Di Nardo W, Ghirlanda G, Cercone S, Pitocco D, Soponara C, Cosenza A, et al. The use new diagnostic posturographic tool for disorders of stance. Clin Neurophysiol
of dynamic posturography to detect neurosensorial disorder in IDDM without 2006;117(8):1692–8. Aug.
clinical neuropathy. J Diabetes Complications 1999;13(2):79–85. Mar. Kuo AD, Speers RA, Peterka RJ, Horak FB. Effect of altered sensory conditions on
Dickstein R, Shupert CL, Horak FB. Fingertip touch improves postural stability in multivariate descriptors of human postural sway. Exp Brain Res
patients with peripheral neuropathy. Gait Posture 2001;14(3):238–47. Dec. 1998;122(2):185–95. Sep.
Diener HC, Dichgans J, Bacher M, Gompf B. Quantification of postural sway in Le Clair K, Riach C. Postural stability measures: what to measure and for how long.
normals and patients with cerebellar diseases. Electroencephalogr Clin Clin Biomech (Bristol, Avon) 1996;11(3):176–8. Apr.
Neurophysiol 1984a;57(2):134–42. Feb. Ledin T, Odkvist LM, Vrethem M, Moller C. Dynamic posturography in assessment of
Diener HC, Dichgans J, Bootz F, Bacher M. Early stabilization of human posture after polyneuropathic disease. J Vestib Res 1990;1(2):123–8.
a sudden disturbance: influence of rate and amplitude of displacement. Exp Loram ID, Maganaris CN, Lakie M. Paradoxical muscle movement in human
Brain Res 1984b;56(1):126–34. standing. J Physiol 2004;556(Pt 3):683–9. May 1.
Diener HC, Dichgans J, Bruzek W, Selinka H. Stabilization of human posture Maki BE, Holliday PJ, Topper AK. Fear of falling and postural performance in the
during induced oscillations of the body. Exp Brain Res 1982;45(1–2):126– elderly. J Gerontol 1991;46(4):M123–31. Jul.
32. Maki BE, McIlroy WE. Control of rapid limb movements for balance recovery: age-
Dietz V, Gollhofer A, Kleiber M, Trippel M. Regulation of bipedal stance: dependency related changes and implications for fall prevention. Age Ageing 2006;35(Suppl
on ‘‘load” receptors. Exp Brain Res 1992;89(1):229–31. 2):ii12–=0?>ii18. Sep.
Dietz V, Trippel M, Ibrahim IK, Berger W. Human stance on a sinusoidally Maki BE, Whitelaw RS. Influence of expectation and arousal on center-of-pressure
translating platform: balance control by feedforward and feedback responses to transient postural perturbations. J Vestib Res 1993;3(1):25–39.
mechanisms. Exp Brain Res 1993;93(2):352–62. Marigold DS, Eng JJ, Tokuno CD, Donnelly CA. Contribution of muscle strength and
Dimitri PS, Wall C, III, Oas JG, Rauch SD. Application of multivariate statistics to integration of afferent input to postural instability in persons with stroke.
vestibular testing: discriminating between Meniere’s disease and migraine Neurorehabil Neural Repair 2004;18(4):222–9. Dec.
associated dizziness. J Vestib Res 2001;11(1):53–65. Martin JP. Tilting reactions and disorders of the basal ganglia. Brain
Dimitrova D, Horak FB, Nutt JG. Postural muscle responses to multidirectional 1965;88(5):855–74. Dec.
translations in patients with Parkinson’s disease. J Neurophysiol Maurer C, Mergner T, Peterka RJ. Abnormal resonance behavior of the postural
2004;91(1):489–501. Jan. control loop in Parkinson’s disease. Exp Brain Res 2004;157(3):369–76. Aug.
Duarte M, Zatsiorsky VM. On the fractal properties of natural human standing. Maurer C, Mergner T, Xie J, Faist M, Pollak P, Lucking CH. Effect of chronic bilateral
Neurosci Lett 2000;283(3):173–6. Apr 14. subthalamic nucleus (STN) stimulation on postural control in Parkinson’s
Evans MK, Krebs DE. Posturography does not test vestibulospinal function. disease. Brain 2003;126(Pt 5):1146–63. May.
Otolaryngol Head Neck Surg 1999;120(2):164–73. Feb. Maurer C, Peterka RJ. A new interpretation of spontaneous sway measures based on
Facchinetti LD, Imbiriba LA, Azevedo TM, Vargas CD, Volchan E. Postural modulation a simple model of human postural control. J Neurophysiol 2005;93(1):189–200.
induced by pictures depicting prosocial or dangerous contexts. Neurosci Lett Jan.
2006;410(1):52–6. Dec 13. McIlroy WE, Maki BE. The ‘deceleration response’ to transient perturbation of
Fitzpatrick R, Burke D, Gandevia SC. Loop gain of reflexes controlling human upright stance. Neurosci Lett 1994;175(1–2):13–6. Jul 4.
standing measured with the use of postural and vestibular disturbances. J Melnick ME, Dowling GA, Aminoff MJ, Barbaro NM. Effect of pallidotomy on
Neurophysiol 1996;76(6):3994–4008. Dec. postural control and motor function in Parkinson disease. Arch Neurol
Freitas SM, Prado JM, Duarte M. The use of a safety harness does not affect body 1999;56(11):1361–5. Nov.
sway during quiet standing. Clin Biomech (Bristol, Avon) 2005;20(3):336–9. Munhoz RP, Li JY, Kurtinecz M, Piboolnurak P, Constantino A, Fahn S, et al.
Mar. Evaluation of the pull test technique in assessing postural instability in
Fung VS, Sauner D, Day BL. A dissociation between subjective and objective Parkinson’s disease. Neurology 2004;62(1):125–7. Jan 13.
unsteadiness in primary orthostatic tremor. Brain 2001;124(Pt 2):322–30. Feb. Nardone A, Schieppati M. Balance control under static and dynamic conditions in
Furman JMR, Baloh RW, Barin K, Hain TC, Herdman S, Horst RK, et al. Assessment: patients with peripheral neuropathy. G Ital Med Lav Ergon 2007;29(1):101–4.
posturography. Report of the Therapeutics and Technology Assessment Jan.
Subcommittee of the American Academy of Neurology. Neurology O’Neill DE, Gill-Body KM, Krebs DE. Posturography changes do not predict
1993;43(6):1261–4. Jun. functional performance changes. Am J Otol 1998;19(6):797–803. Nov.
Gatev P, Thomas S, Kepple T, Hallett M. Feedforward ankle strategy of balance Oie KS, Kiemel T, Jeka JJ. Multisensory fusion: simultaneous re-weighting of vision
during quiet stance in adults. J Physiol 1999;514(Pt 3):915–28. Feb 1. and touch for the control of human posture. Brain Res Cogn Brain Res
Geurts AC, Nienhuis B, Mulder TW. Intrasubject variability of selected force- 2002;14(1):164–76. Jun.
platform parameters in the quantification of postural control. Arch Phys Med Ondo W, Warrior D, Overby A, Calmes J, Hendersen N, Olson S, et al. Computerized
Rehabil 1993;74(11):1144–50. Nov. posturography analysis of progressive supranuclear palsy: a case-control
Goebel JA, Sataloff RT, Hanson JM, Nashner LM, Hirshout DS, Sokolow CC. comparison with Parkinson’s disease and healthy controls. Arch Neurol
Posturographic evidence of nonorganic sway patterns in normal subjects, 2000;57(10):1464–9. Oct.
patients, and suspected malingerers. Otolaryngol Head Neck Surg Palop JJ, Chin J, Mucke L. A network dysfunction perspective on neurodegenerative
1997;117(4):293–302. Oct. diseases. Nature 2006;443(7113):768–73. Oct 19.
Haart dM, Geurts AC, Huidekoper SC, Fasotti L, van LJ. Recovery of standing balance Peterka RJ. Sensorimotor integration in human postural control. J Neurophysiol
in postacute stroke patients: a rehabilitation cohort study. Arch Phys Med 2002;88(3):1097–118. Sep.
Rehabil 2004;85(6):886–95. Jun. Piboolnurak P, Yu QP, Pullman SL. Clinical and neurophysiologic spectrum of
Hansen PD, Woollacott MH, Debu B. Postural responses to changing task conditions. orthostatic tremor: case series of 26 subjects. Mov Disord
Exp Brain Res 1988;73(3):627–36. 2005;20(11):1455–61. Nov.
Helbostad JL, Askim T, Moe-Nilssen R. Short-term repeatability of body sway during Piirtola M, Era P. Force platform measurements as predictors of falls among older
quiet standing in people with hemiparesis and in frail older adults. Arch Phys people – a review. Gerontology 2006;52(1):1–16.
Med Rehabil 2004;85(6):993–9. Jun. Polonyova A, Hlavacka F. Human postural responses to different frequency
Henry SM, Fung J, Horak FB. EMG responses to maintain stance during vibrations of lower leg muscles. Physiol Res 2001;50(4):405–10.
multidirectional surface translations. J Neurophysiol 1998;80(4):1939–50. Oct. Prieto TE, Myklebust JB, Hoffmann RG, Lovett EG, Myklebust BM. Measures of
Hill KM, Harburn KL, Kramer JF, Noh S, Vandervoort AA, Matheson JM. Comparison postural steadiness: differences between healthy young and elderly adults. IEEE
of balance responses to an external perturbation test, with and without an Trans Biomed Eng 1996;43(9):956–66. Sep.
overhead harness safety system. Gait Posture 1994;2:27–31. Reid MC, Lachs MS, Feinstein AR. Use of methodological standards in diagnostic test
Hirsch MA, Toole T, Maitland CG, Rider RA. The effects of balance training and high- research. Getting better but still not good. JAMA 1995;274(8):645–51. Aug 23.
intensity resistance training on persons with idiopathic Parkinson’s disease. Reid VA, Adbulhadi H, Black KR, Kerrigan C, Cros D. Using posturography to detect
Arch Phys Med Rehabil 2003;84(8):1109–17. Aug. unsteadiness in 13 patients with peripheral neuropathy: a pilot study. Neurol
Jacobs JV, Horak FB, Tran VK, Nutt JG. Multiple balance tests improve the Clin Neurophysiol 2002;2002(4):2–8.
assessment of postural stability in subjects with Parkinson’s disease. J Neurol Rietdyk S, Patla AE, Winter DA, Ishac MG, Little CE. NACOB presentation CSB New
Neurosurg Psychiatry 2006;77(3):322–6. Mar. Investigator Award. Balance recovery from medio-lateral perturbations of the
Johansson R, Magnusson M, Akesson M. Identification of human postural dynamics. upper body during standing. North American Congress on Biomechanics. J
IEEE Trans Biomed Eng 1988;35(10):858–69. Oct. Biomech 1999;32(11):1149–58. Nov.
2436 J.E. Visser et al. / Clinical Neurophysiology 119 (2008) 2424–2436

Rine RM, Braswell J, Fisher D, Joyce K, Kalar K, Shaffer M. Improvement of motor Uimonen S, Laitakari K, Kiukaanniemi H, Sorri M. Does posturography differentiate
development and postural control following intervention in children with malingerers from vertiginous patients? J Vestib Res 1995;5(2):117–24. Mar.
sensorineural hearing loss and vestibular impairment. Int J Pediatr van Asseldonk EH, Buurke JH, Bloem BR, Renzenbrink GJ, Nene AV, van der Helm FC,
Otorhinolaryngol 2004;68(9):1141–8. Sep. et al. Disentangling the contribution of the paretic and non-paretic ankle to
Rocchi L, Chiari L, Horak FB. Effects of deep brain stimulation and levodopa on balance control in stroke patients. Exp Neurol 2006;201(2):441–51. Oct.
postural sway in Parkinson’s disease. J Neurol Neurosurg Psychiatry van Asseldonk EH, Carpenter MG, van der Helm FC, van der KH. Use of induced
2002;73(3):267–74. Sep. acceleration to quantify the (de)stabilization effect of external and internal
Schieppati M, Nardone A. Free and supported stance in Parkinson’s disease. The forces on postural responses. IEEE Trans Biomed Eng 2007;54(12):2284–95.
effect of posture and ‘postural set’ on leg muscle responses to perturbation, Dec.
and its relation to the severity of the disease. Brain 1991;114(Pt 3):1227–44. Van der Kooij H, van Asseldonk E, van der Helm FC. Comparison of different
Jun. methods to identify and quantify balance control. J Neurosci Methods
Shivitz N, Koop MM, Fahimi J, Heit G, Bronte-Stewart HM. Bilateral subthalamic 2005;145(1–2):175–203. Jun 30.
nucleus deep brain stimulation improves certain aspects of postural control in Van der Kooij H, van Asseldonk EH, Geelen J, van Vugt JP, Bloem BR. Detecting
Parkinson’s disease, whereas medication does not. Mov Disord asymmetries in balance control with system identification: first experimental
2006;21(8):1088–97. Aug. results from Parkinson patients. J Neural Transm 2007;114(10):1333–7. Oct.
Sinaki M, Lynn SG. Reducing the risk of falls through proprioceptive dynamic Visser JE, Allum JH, Carpenter MG, Esselink RA, Speelman JD, Borm GF, et al.
posture training in osteoporotic women with kyphotic posturing: a randomized Subthalamic nucleus stimulation and levodopa-resistant postural instability in
pilot study. Am J Phys Med Rehabil 2002;81(4):241–6. Apr. Parkinson’s disease. J Neurol 2008;255(2):205–10. Feb.
Soechting JF, Berthoz A. Dynamic role of vision in the control of posture in man. Exp Voermans NC, Snijders AH, Schoon Y, Bloem BR. Why old people fall (and how to
Brain Res 1979;36(3):551–61. Aug 1. stop them). Pract Neurol 2007;7(3):158–71. Jun.
Stel VS, Smit JH, Pluijm SM, Lips P. Consequences of falling in older men and women Watanabe Y. Fear of falling among stroke survivors after discharge from inpatient
and risk factors for health service use and functional decline. Age Ageing rehabilitation. Int J Rehabil Res 2005;28(2):149–52. Jun.
2004;33(1):58–65. Jan. Whitney SL, Marchetti GF, Schade AI. The relationship between falls history and
Stewart MG, Chen AY, Wyatt JR, Favrot S, Beinart S, Coker NJ, et al. Cost- computerized dynamic posturography in persons with balance and vestibular
effectiveness of the diagnostic evaluation of vertigo. Laryngoscope disorders. Arch Phys Med Rehabil 2006;87(3):402–7. Mar.
1999;109(4):600–5. Apr. Williams NP, Roland PS, Yellin W. Vestibular evaluation in patients with early
Szturm T, Fallang B. Effects of varying acceleration of platform translation and toes- multiple sclerosis. Am J Otol 1997;18(1):93–100. Jan.
up rotations on the pattern and magnitude of balance reactions in humans. J Winter DA, Patla AE, Ishac M, Gage WH. Motor mechanisms of balance during quiet
Vestib Res 1998;8(5):381–97. Sep. standing. J Electromyogr Kinesiol 2003;13(1):49–56. Feb.
Tarantola J, Nardone A, Tacchini E, Schieppati M. Human stance stability improves Wolfson LI, Whipple R, Amerman P, Kleinberg A. Stressing the postural response. A
with the repetition of the task: effect of foot position and visual condition. quantitative method for testing balance. J Am Geriatr Soc 1986;34(12):845–50.
Neurosci Lett 1997;228(2):75–8. Jun 6. Dec.
Tinetti ME. Clinical practice. Preventing falls in elderly persons. N Engl J Med Woollacott M, Shumway-Cook A. Attention and the control of posture and gait: a
2003;348(1):42–9. Jan 2. review of an emerging area of research. Gait Posture 2002;16(1):1–14. Aug.
Tokuno CD, Carpenter MG, Thorstensson A, Cresswell AG. The influence of natural Yardley L, Smith H. A prospective study of the relationship between feared
body sway on neuromuscular responses to an unpredictable surface translation. consequences of falling and avoidance of activity in community-living older
Exp Brain Res 2006;174(1):19–28. Sep. people. Gerontologist 2002;42(1):17–23. Feb.
Uccioli L, Giacomini PG, Monticone G, Magrini A, Durola L, Bruno E, et al. Body sway Yarrow K, Brown P, Gresty MA, Bronstein AM. Force platform recordings in the
in diabetic neuropathy. Diabetes Care 1995;18(3):339–44. Mar. diagnosis of primary orthostatic tremor. Gait Posture 2001;13(1):27–34. Feb.

Anda mungkin juga menyukai