Clinical Neurophysiology
journal homepage: www.elsevier.com/locate/clinph
Invited review
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.
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
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
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.
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
4.3. 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
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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
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