Arch Gerontol Geriatr. 2012 (Nov); 55 (3): 667–672 ~ FULL TEXT
Sureeporn Uthaikhup, Gwendolen Jull, Somporn Sungkarat, Julia Treleaven
Department of Physical Therapy,
Faculty of Associated Medical Sciences,
Chiang Mai University,
Greater disturbances in sensorimotor control have been demonstrated in younger to middle aged groups. However, it is unknown whether or not the impairments documented in these populations can be extrapolated to elders with neck pain. The aim of this study was to investigate the influence of neck pain on sensorimotor function in elders. Twenty elders with neck pain (12 women and 8 men) and 20 healthy elder controls (14 women and 6 men) aged 65 years and over were recruited from the general community. Tests for sensorimotor function included; cervical joint position sense (JPS); computerised rod-and-frame test (RFT); smooth pursuit neck torsion test (SPNT); standing balance (under conditions of eyes open, eyes closed on firm and soft surfaces in comfortable stance); step test and ten-meter walk test with and without head movement.
Elders with neck pain had greater deficits in the majority of sensorimotor function tests after controlling for effects of age and comorbidities. Significant differences were found in the SPNT (p<0.01), error in the RFT (frame angled at 10° and 15° anticlockwise) (p<0.05), standing balance (amplitude of sway) - eyes open on a firm surface in the medio-lateral (ML) direction (p=0.03), and total number of steps on the step test, both left and right sides (p<0.01).
Elders with neck pain have greater sensorimotor disturbances than elders without neck pain, supporting a contribution of altered afferent information originating from the cervical spine to such disturbances. The findings may inform falls prevention and management programs.
KEYWORDS: Balance; Falls risk; Mobility-limitation; Musculoskeletal pain; Older adults
From the FULL TEXT Article:
The prevalence of neck pain in community dwelling elders is
estimated as 40.5% in women and 36.1% in men (March et al.,
1998). It is important to understand the contribution of neck pain
to sensorimotor disturbances in elders as postural instability
increases the risk of falling (Shumway-Cook et al., 2000; Hawk
et al., 2006; Pajala et al., 2008).
Neck pain can be associated with dizziness, unsteadiness and
visual disturbances and it can also affect postural stability, cervical
proprioception and head and eye movement control (Treleaven,
2008a; Kristjansson and Treleaven, 2009). The vestibular and
visual systems are vital to sensorimotor control but there is also
evidence for the important contribution of cervical proprioception
(Bolton, 1998; Treleaven, 2008a; Kristjansson and Treleaven,
2009). The deep sub-occipital muscles contain a high density of
muscle spindles (Kogler et al., 2000; Rix and Bagust, 2001; Boyd-
Clark et al., 2002). Bove et al. (2002) and Courtine et al. (2003)
demonstrated that stimulation of the muscle spindle afferents via
neck muscle vibration not only influenced balance but also walking
and running in healthy individuals. In addition, a recent study of
experimentally induced neck pain illustrated the destabilizing
effect of neck muscle pain on standing balance (Vuillerme and
Increasing age is accompanied by changes in vestibular, visual
and neuromuscular function (Ahmed et al., 2005). Declines in these
systems are a normal consequence of aging. Greater disturbances
in sensorimotor control have been demonstrated in healthy elders
when compared to the middle aged in terms of larger cervical joint
position errors, postural imbalance and impaired gait (Woollacott
and Tang, 1997; Gill et al., 2001; Jacobson et al., 2008; Schrager
et al., 2008; Vuillerme et al., 2008; Liaw et al., 2009). In relation to
neck pain, increased cervical joint position error, poor eye
movement control and balance disturbances have been demonstrated
in younger to middle aged groups with both idiopathic and
whiplash induced neck pain (Field et al., 2008; Humphreys, 2008;
Treleaven, 2008a,b). These findings have informed rehabilitation
programs (Jull et al., 2008). It is unknown whether or not the
impairments documented in these populations can be extrapolated
to elders with neck pain. One study has investigated the
influence of neck pain on balance and gait parameters in
community-dwelling elders, with findings suggesting that neck
pain might contribute to disturbances in balance and gait over and
above that which occurs with normal aging (Poole et al., 2008). A
comprehensive range of sensorimotor functions is yet to be
investigated specifically in the elderly with neck pain.
This study investigated eye movement control, cervical
proprioception, postural stability and gait parameters in elders
with neck pain to determine if there were any deficits in
sensorimotor function above those which could be attributed to
aging. It has been shown that fear of falling is associated with gait
and balance abnormalities (Chamberlin et al., 2005) even without a
history of falls (Maki, 1997). Thus fear of falling and its association
with postural stability and gait were also assessed.
Subjects and methods
Forty elderly volunteers aged 65 years or older, with (n = 20) and
without neck pain (n = 20) were included in the study. Participants
were recruited from a metropolitan area using a method of
convenience sampling and through advertising. To be eligible for
the neck pain group, participants had to have neck pain as a
predominant complaint, where neck pain is defined as pain and
stiffness in the neck with or without radiating pain to shoulders and
the upper limbs. Neck pain was to be of no less than 3 months
duration with a score of at least 10 out of 100 on the Neck Disability
Index (NDI) (Vernon and Mior, 1991). Participants were excluded if
they had major comorbidities which could affect measures
including: previous history of orthopedic surgery, a current acute
musculoskeletal injury, lumbar spine or lower limb arthritis for
which they had sought active management, neurological problems
(e.g. stroke, Parkinson’s disease), diabetes, and cognitive impairment.
Ethical approval for the study was granted by the Institutional
Medical Ethics Review Committee and the study was conducted in
accordance with the declaration of Helsinki. Written informed
consent was provided before participation.
Questionnaires were administered to collect demographic data,
intensity of neck pain (VAS), patient’s self-rated neck pain and
disability (NDI), (Vernon and Mior, 1991) and balance confidence
in daily activities (ABC) (Powell and Myers, 1995). As many
conditions which are common with aging can influence gait,
balance and other measures in this study, information concerning
the presence of comorbidities (not encompassed in exclusion
criteria) was also collected from each participant and coded as
present or not in five categories.
The categories were
(1) musculoskeletal conditions affecting the lumbar spine or lower limb;
(4) previous traumatic neck injury;
(5) taking more than four medications.
Joint position error (JPE): The Fastrak system was used to
measure the subjects’ ability to relocate the natural starting head
position following active movements from left and right rotation
and extension. The method is similar to that previously described
(Treleaven et al., 2003) and adapted from Revel et al. (1991).
Absolute error was calculated with a customised software program
(Matlab (7.0), Mathworks Inc., USA). Three repetitions of each
movement direction were undertaken and the mean value of the
error used for analysis.
RFT: The RFT was used to measure the subjects’ perception of
verticality (Bagust, 2005). The test was presented with a white
square (the frame) and a white line (the rod) on a plain black
background. The rod was positioned within the frame and rotated
independently of the frame. A sequence of 12 random presentations
was administered for the vertical perception test. The frame
was set at 08, and at 108 and 158 in both clockwise and
anticlockwise directions from the vertical. For two presentations,
there was no frame. The initial position of the rod was angled at 308
clockwise and anticlockwise. Subjects wore video goggles to
reduce the presence of visual cues. They used a computer mouse to
rotate the rod to what he/she perceived as the vertical. Two
practices were undertaken for familiarization. Subjects wore their
normal corrective lenses if necessary. The absolute error values
from the true vertical were calculated for each test.
Head and eye movement control
SPNT: Electro-oculography was used in the SPNT to assess
disturbances in eye movement control. The method has been
described elsewhere in detail (Tjell and Rosenhall, 1998; Treleaven
et al., 2005a). The test was performed with the subject’s head and
trunk in a neutral forward-looking position and then a torsioned
position (head neutral, trunk in 458 rotation to the left and right).
Subjects were instructed to perform three blinks (for recognition
and elimination in data analysis) and then follow the light as
closely as possible with their eyes. The SPNT test value was
calculated as the difference between the average gain in the
neutral and torsioned positions.
Standing balance: Standing balance was measured using a
40 cm x 60 cm stable computerised force platform. Changes in
standing balance were measured in the ML and antero-posterior
(AP) directions using established methodology (Field et al., 2008;
Treleaven et al., 2008). Standing balance was tested in comfortable
stance on a firm surface and on a soft surface (a piece of high density
10-cm thick foam placed on the force platform) with eyes open and
closed. A 30-s time period was performed for each condition.
Step test: The step test was used to assess dynamic single limb
stance (Hill et al., 1996). Subjects were asked to step one foot on and
then off a 7.5 cm block as quickly as possible for 15 s and the number
of steps was recorded. Both left and right sides were tested.
Ten-meter walk (TMW) test without and with head movement: The
TMW test was used to measure self-selected walking speed, which is
proposed as a global indicator of self-perceived physical function
(Cress et al., 1995). Subjects were asked to walk along a 14-m walkway
at their comfortable speed under three conditions: head facing
straightforward, head turning from side to side, head moving updown.
Time and number of steps were recorded for the intermediate
10 m to allow for acceleration and deceleration (Poole et al., 2008).
Participants were initially screened for inclusion and exclusion
criteria and those meeting the inclusion criteria entered the study.
On the testing day, all eligible subjects completed the questionnaires
and then performed the tests. Standing balance was
tested before the step test and walking task to prevent fatigue. For
all postural stability tests, the investigator stood close to or walked
beside the subjects as a safety measure to prevent falls. Subjects
were given standardised instructions prior to the tests and were
allowed rest breaks between tests.
Independent t-test and chi-square analyses were used initially
to test for any between group differences in age, gender and
comorbidities. For standing balance measures, root mean square
(RMS) amplitude in millimeters (Labview, National Instruments)
and total energy (Wavelet analysis using Daubechie filter 6)
were analysed (Treleaven et al., 2005b). RMS was chosen to
demonstrate the average amplitude traveled by the center of
pressure and the total energy was the amount of energy of the
sway signal. Analysis was conducted for both the AP and ML
traces for each condition (Field et al., 2008; Poole et al., 2008).
Normality of all data was assessed using Q–Q plots and data
were transformed using log transformation.
multivariate analysis of variance (MANOVA) were used to
investigate any differences in outcome variables between the
neck pain and control groups. Age and comorbidity categories
are known to effect sensorimotor function (Tjell and Rosenhall,
1998; della Volpe et al., 2006; Akdal et al., 2009; Salzman, 2010).
To focus foremost on the contribution of the neck, age and all
comorbidity categories were entered separately as covariates in
all analyses, regardless of significant differences between
groups, to control for possible confounding factors. Statistical
analyses were performed using SPSS software and a significance
level was set at p < 0.05.
Demographic data for the neck pain and control groups are
presented in Table 1. Participants with neck pain were older and
had more comorbidities than those without neck pain, reaching
significance for the two categories of low back or lower limb pain
and dizziness (p < 0.05).
As indicated, we considered age and every comorbidity
category as covariates in analyses of all outcomes. Thus the results
shown below were obtained after controlling for all potential
The mean balance confidence (ABC) scores were 86.6 ± 10.9 for
the neck pain group and 97.0 ± 4.2 for the control group. There was a
significant between-group difference in the ABC scores (p = 0.05).
Table 2 presents the results of JPEs, SPNT and RFT between the
neck pain and control groups. The neck pain group had
significantly greater deficits in the SPNT and difficulty in
perceiving the vertical when the frame was angled at 108 and
158 anticlockwise and the rod positioned at an angle of 308
clockwise and anticlockwise (all p ≤ 0.05). There were no
significant differences between groups in JPEs (p > 0.05).
Table 3 presents total number of steps on the step test and the
features measured in the TMW test for the neck pain and control
groups. The neck pain group took significantly less steps than the
control group on both left and right sides (p < 0.01). Deficits in gait
parameters in the conditions of walking while turning the head
from side to side and moving the head up-down were greater in the
neck pain group compared to the control group however
differences did not reach statistical significance (p > 0.05).
Figure 1a and b present the means, standard errors and the
significant between group differences for the logged values for
each condition in AP and ML directions for the total energy of the
sway signal. Figure 2a and b present the values for the amplitude of
sway (RMS). There were no differences between the groups in total
energy of the sway signal over all tests (p > 0.05). The RMS
amplitude values were significantly less in the neck pain group in
the tests of eyes open on the firm surface in the ML direction
(p = 0.03). There were also trends for greater RMS amplitude values
in the tests of eyes open (p = 0.07) and closed (p = 0.07) on the firm
surface in the AP direction.
This study revealed that elders with neck pain demonstrated
greater deficits in eye movement control, perception of verticality
and balance when compared to healthy elders even after
controlling for all potential confounding factors (age and
comorbidities) that may have influences on the outcome measures.
Additionally, they also had significantly lower levels of selfconfidence
in performing activities. The greater deficits in elders
with neck pain, beyond those occurring with normal aging, support
the premise of cervical afferent dysfunction as a contributor to
sensorimotor disturbances (Treleaven, 2008a; Kristjansson and
Deficits in eye movement control were greater in elders with
neck pain, in accordance with previous findings that patients with
neck disorders may have smooth pursuit eye movement disturbances
(Tjell and Rosenhall, 1998; Tjell et al., 2002; Treleaven
et al., 2005a; Storaci et al., 2006). The receptors in the cervical
region have central and reflex connections to the visual, vestibular
and central nervous systems (Treleaven, 2008a; Kristjansson and
Treleaven, 2009). An increase in cervico-ocular reflex (COR) gain is
thought to compensate for any natural decline in vestibuloocular
reflex (VOR) function in the healthy and elderly (Kelders et al.,
2003; Montfoort et al., 2008). However, Montfoort et al. (2008)
found that this compensation did not occur in patients with
cervical injury (whiplash) and reasoned that these subjects were
possibly unable to modify both the COR and VOR eye movement
responses. They suggested that adaptive processes of the COR and
VOR may take a longer time to operate adequately and there may
be an imbalance between the reflexes caused by abnormal cervical
afferent input. Thus it is possible that disturbances of smooth
pursuit eye movements identified in elders with neck pain are
more related to altered afferent information from the neck.
Our results indicate that the RFT of vertical perception may be
useful in testing an aspect of spatial orientation dysfunction in
patients with neck pain. There was a trend for greater errors in the
perception of verticality in elders with neck pain than those without
neck pain. The pattern of errors showed maximal effect at frame tilts
of 108 to 158 with smaller errors at 08 frame tilt and with no frame, in
agreement with previous studies (Grod and Diakow, 2002; Bagust,
2005). Perception of verticality requires visual information (external
cues) to be integrated with sensory inputs from the vestibular
system and neck proprioceptors (internal cues). Altered proprioceptive
afferent input originating from the cervical region may result
in difficulty in perceiving the vertical orientation. There is, however,
an argument that disturbances of spatial orientation may be affected
by perceptual style (i.e. field dependence and independence)
(Storaci et al., 2006). As yet, this has not been determined in any
studies of neck pain. Further research is needed into perceptual style,
although this is an unlikely cause of vertical perception difficulty in
patients with neck pain.
There was a trend toward greater deficits in balance responses
in elders with neck pain than healthy elders. Significant deficits
were evident in amplitude of sway, greater in the AP than ML
direction, which supports the preliminary findings by Poole et al.
(2008). Decreased amplitude of sway was observed with eyes open
on a firm surface in the ML direction and a tendency for increased
amplitude of sway was observed with eyes open and closed on a
firm surface in the AP direction (p = 0.07). No differences in sway
energy were found between the groups, although there was a
tendency for increased energy of sway in the ML direction on a firm
surface in the neck pain group. These results suggest that our
elders with neck pain may have a decreased awareness of postural
stability (Field et al., 2008; Poole et al., 2008).
The balance deficits
were more clearly demonstrated on the firm surface rather than
the soft surface which may indicate that tests on soft surfaces were
challenging for all elders in our study. This is not surprising given
that a significant decline in ability to balance has been
demonstrated from the six decade when a soft surface is
introduced (with and without vision removed) (Choy et al.,
2003). The detrimental changes in the other sensory systems
(vestibular/visual) with age may have more influence on postural
stability than the role of cervical pain when standing on a softer
surface. Nevertheless, further research is required to confirm and
explore these findings in elderly populations from mechanistic and
best test viewpoints.
Elders with neck pain performed lesser steps in the step test,
suggesting disturbances in dynamic standing balance. Reference
values for the step test in healthy elderly are 17.4 steps on the left
side and 17.7 steps on the right side in 15 s (Hill et al., 1996). Our
elders in the neck pain group took 12.7 steps on the left side and
12.3 steps on the right side, which is considerably less than
reference values. In addition, the relatively decreased gait speed
and cadence while turning the head from side to side and moving
the head up-down were observed in elders with neck pain
compared to the control group, but significant differences were not
found. The gait parameter results do not strongly support Poole
et al.’s study demonstrating that elders with neck pain had a slower
gait speed and cadence in the head turn condition (Poole et al.,
However, there were differences in how comorbidities were
approached between Poole et al’s and this study. Cesari et al.
(2005) suggested that older persons with usual gait speed lower
than 100 cm/s were at high risk of adverse health-related
outcomes. In Bohannon’s study (1997), mean comfortable gait
speed ranged from 127.2 cm/s for women to 133.0 cm/s for men,
aged in their seventies. Given slight differences in gait measurements
between studies, the average gait speed of elders with neck
pain in this study (108.2–136.8 cm/s) may not be associated with
functional disturbances. Conversely, the decrease in the gait
parameters might be a consequence of the challenges inherent in
performing dual tasks. There is a need for better understanding of
the cause of gait disturbances during challenging walking
conditions in elders with neck pain.
Fear of falling as reflected by the mean ABC score was
significantly lower in elders with neck pain than those without
neck pain. Nevertheless, the ABC score reported by elders with
neck pain was still relatively good, suggesting that fear of falling
may not be strongly related to fall risk and self-induced restriction
of activities (Hatch et al., 2003). Further research is required to
explore the clinical significance between changes in balance
confidence and postural instability in elders with neck pain.
The sample size in this study was small. The statistical power
levels of the non significant results were less than 0.8, indicating
inadequate power to detect statistical significance. It was difficult
to recruit elders with neck pain without major comorbidities.
Nevertheless, age and the comorbidities remaining after exclusion
of major comorbidities, were entered as covariates to control for
any potential confounding factors in the analyses of all outcomes.
Dizziness could have been a consequence of the neck pain but was
included as a covariate and thus may have led to an underestimation
of the results. This adds strength to our findings that altered
cervical afferent input contributes to disturbances in sensorimotor
function in elders with neck pain. However, further research in this
area is still required.
The study has determined that overall, sensorimotor disturbances
were greater in elders with neck pain than without neck
pain after controlling for age and comorbidities. Elders with neck
pain have greater deficits in eye movement control, vertical
perception and balance, which supports the notion that altered
cervical afferent input may contribute to sensorimotor disturbances.
Assessment of disturbed sensorimotor function is indicated
in elders with neck pain as is assessment of neck disorders in
those with falls risk.
Conflict of interest
This work has been funded by Chiang Mai University.
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