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POSTURAL CONTROL IN PEOPLE WITH OSTEOARTHRITIS

OF THE CERVICAL SPINE


Pierre Boucher, DC, PhD, a Martin Descarreaux, DC, PhD, a and Martin C. Normand, DC, PhD a

ABSTRACT

Objective: This study examines whether there is a relationship between clinical correlates of osteoarthritic changes of
the cervical spine and changes in postural stability.
Methods: This was a control group study with repeated measures. Twenty-three patients were recruited from the
chiropractic University Clinic to participate in this study. The presence and severity of osteoarthritic changes of the
cervical spine were determined radiologically. Balance control was evaluated by testing subjects' postural stability on a
force platform with and without vision. A general clinical assessment of the neuromusculoskeletal system was performed
to screen for any physical condition that could affect postural stability. Participants' characteristics were compared
between each group using a 1-way analysis of variance for independent samples, and postural stability variables were
submitted to a 2-way repeated measures analysis of variance.
Results: Subjects with signs of osteoarthritis of the cervical spine showed an increased range of sway, a faster sway
speed, and a greater excursion than control subjects. They also showed a larger degree of lower limb neuropathy than
control subjects.
Conclusion: The postural instability shown by the osteoarthritic group may be due to the effects of the lower limb
peripheral neuropathy alone or due to a combination of both cervical degenerative changes and peripheral changes.
Further research is needed to clearly isolate the effects of the degeneration of the cervical spine on postural control.
(J Manipulative Physiol Ther 2008;31:184-190)
Key Indexing Terms: Posture; Osteoarthritis; Musculoskeletal Equilibrium; Peripheral Nervous System Disease; Aging

P
ostural stability is achieved, in part, through spatial An experiment conducted by de Jong et al,4 where animals
and temporal integration of proprioceptive, visual, and man were injected with local anesthetics into the deep
and vestibular information, producing the perception tissues of the neck, clearly illustrates the role of neck
of our body's orientation in space and how external objects afferents. After the injection with local anesthetics, vertigo,
are located relative to us. Diminished sensory functions and ataxia, and nystagmus were observed in animals and human
slowing of sensorimotor processing occur with normal subjects. The authors of this study suggested that ataxia,
aging.1 Besides, older people are at higher risk of developing dizziness, and vertigo could arise from disorders affecting
multiple impairments affecting different components of the the afferent flow of impulses from deep tissues of the neck.
nervous system such as sensory loss, weakness, orthopedic Besides, loss of proprioceptors in cervical joints,5 osteoar-
constraints, and cognitive impairments.2,3 thritis of the cervical spine,6-12 and neck motion limit-
More specifically, pathology in peripheral systems can ation13,14 are frequently mentioned as factors contributing
affect the sensory components of postural control, including to loss of balance and falls in the elderly.
the accurate detection of head and body position and motion.2 Among the factors mentioned above, osteoarthritis is of
A change in the quantity and the quality of peripheral sensory particular interest because it is the most frequent articular
information may deprive the central nervous system of disease.15 It affects the integrity of cartilage and produces
important information and compromise postural stability.4 modifications in other tissues such as synovial membrane
inflammation, thickening of articular capsules, and periarti-
a
cular amyotrophy.15 These modifications may also alter the
Professor, Dpartement de Chiropratique, Universit du neurophysiologic properties of cervical joint receptors,
Qubec Trois-Rivires, Canada.
Submit requests for reprints to: Pierre Boucher, DC, PhD, which exert powerful tonic reflexogenic influences on the
Dpartement de Chiropratique, Universit du Qubec Trois- motoneuron pools of the cervical and limb musculature, on
Rivires, 3351 boul. des Forges, CP 500, Trois-Rivires, QC, the external ocular muscles, as well as contribute signifi-
Canada G9A 5H7 (e-mail: pierre.b.boucher@uqtr.ca). cantly to postural and kinesthetic sensations.16,17 Cervical
Paper submitted June 28, 2007; in revised form October 18, facet joint capsules contain a significant density and
2007; accepted October 18, 2007.
0161-4754/$34.00 distribution of different mechanoreceptors,18 and some
Copyright 2008 by National University of Health Sciences. authors have suggested that the intrinsic suboccipital
doi:10.1016/j.jmpt.2008.02.008 muscles might also play an important role in signaling the

184
Journal of Manipulative and Physiological Therapeutics Boucher et al 185
Volume 31, Number 3 Postural Control and Osteoarthritis

cervical proprioceptive information involved in the con- Table 1. Inclusion and exclusion criteria
scious perception of equilibrium, position, and spatial Inclusion criteria
orientation when vision is occluded.19-21 It has also been To be an adult patient of the chiropractic University Clinic
suggested that atrophy and fatty infiltration in the deep To have received a radiologic examination of the cervical spine during
suboccipital muscles may lead to diminished or altered the last 18 months
proprioceptive input to higher centers22,23 as evidenced by a To have radiologic evidence of osteoarthritis of the cervical spine
(experimental group)
reduced standing balance performance.24
Pain may also be associated with osteoarthritis. Many Exclusion criteria
authors have investigated the effect of pain in cervical con- Signs and/or symptoms of motor or sensory dysfunctions
ditions to detect disturbances in sensorimotor control. Recent History of chronic alcohol or drug consumption
data indicate that cervical joint positioning error, balance, and Consumption of prescription drugs affecting the nervous system
Exposure to toxic substances
eye movement control can all be altered by posttraumatic History of any medical condition susceptible to affect postural stability
cervical pain.25-27 However, although the cervical region
plays an important role in the postural control mechanisms,
few studies have investigated the potential effect of cervical
spine degenerative changes on postural control. ensure that the protocol was properly followed and
Therefore, the aim of this study was to quantify postural authorized the recruitment of each subject in this study.
balance in patients with osteoarthritis and age-matched Before proceeding to the patients' selection, interns met
healthy control subjects. Because osteoarthritis prevalence with a specialist in chiropractic radiology who reviewed
increases dramatically with age, with a greater incidence in the patients' radiographs and classified the degree of
subjects between 40 and 50 years,28 postural balance was articular degeneration according to the criteria described by
also evaluated in a group of young healthy subjects to Petersen et al.30
evaluate the potential aging and cervical osteoarthritis
interaction. We hypothesized that a group of patients with Patient Recruitment According to Experimental Groups
Group 1 (clinical/high OA). The clinical records of new
cervical osteoarthritis will exhibit poorer postural balance
when compared with both a group of aged-matched and
patients showing moderate to severe radiologic signs of
young control subjects without osteoarthritis.
osteoarthritis of the cervical spine were analyzed to exclude
those who could not meet the inclusion-exclusion criteria
(Table 1). After this screening procedure, subjects meeting
METHODS the criteria were contacted by telephone and invited to
Experimental Design participate in the study. Six males and 3 females (mean age,
The following experimental design was used: control 64 years) were recruited.
group studies with repeated measures. Group 2 (age-matched low OA control group). The clinical records
of new patients showing none to mild radiologic signs of
osteoarthritis of the cervical spine were analyzed. Those who
Subjects
could match age and sex of the subjects of group 1 and met
Three groups of patients (n = 23) were formed for this the inclusion-exclusion criteria were contacted by telephone
experiment: (1) patients with moderate to severe radiologic and invited to participate in the study. Three males and 4
signs of osteoarthritis of the cervical spine (clinical/high females (mean age, 59.3 years) were recruited.
OA), (2) patients with none to mild radiologic signs of Group 3 (healthy young controls). After the formation of groups
osteoarthritis of the cervical spine (age-matched low OA 1 and 2, 3 male and 4 female chiropractic students (mean
control group), and (3) young subjects without any sign of age, 24.4 years) who were under chiropractic care and had
osteoarthritis of the cervical spine (healthy young controls). radiographs of their cervical spine as part of their clinical
Direct recruitment and snowball sampling were used to examination were recruited.
recruit the patients.29 Subjects of groups 1 and 2 were
recruited from the pool of presenting new patients of the
outpatient clinic at the Universit du Qubec Trois- Examination Protocol
Rivires, Canada, who were referred to the radiology The purpose of the clinical examination was to detect any
department for cervical spine radiographs as part of their condition that could affect postural stability. All tests were
clinical examination. Subjects of group 3 were all patients at performed according to the University Clinic standards.
the University Clinic at the time of the experiment and were Subjects who agreed to participate in the experiment were
recruited from the chiropractic student body at Universit du invited to a first interview during which they were informed
Qubec Trois-Rivires. Two fifth year chiropractic interns about both the goal of the experiment and its protocol. All
were in charge of evaluating the subjects and collecting the subjects gave informed consent according to the university
data. The principal investigator (PB) reviewed all files to ethics committee. Two fifth year chiropractic interns were in
186 Boucher et al Journal of Manipulative and Physiological Therapeutics
Postural Control and Osteoarthritis March/April 2008

Table 2. Participants' demographic data and clinical examination


scores
Group 1 Group 2 Group 3
Age (y) 64.0 (7.6) 59.3 (5.9) 24.2 (2.2)
Sex 6 men, 3 women 3 men, 3 women 3 men, 4 women
Valk score 6.2 (3.1) 0.6 (1.5) 0 (0)
NDI score (%) 25.8 (28.1) 10.6 (14.6) 1.1 (2.0)
Pain 21.1 (24.9) 16.3 (29.4) 1.1 (3.0)
(VAS, 100 mm)
MMSE 28.1 (1.4) 29.7 (0.8) 29.7 (0.8)
VAS, Visual analog scale.

Fig 1. Visual conditions and temporal intervals selected for the


postural analyses.
charge of evaluating the subjects and collecting the data. The
principal investigator (PB) reviewed all files to ensure that
the protocol was properly followed and authorized the gastrocnemius are scored separately as 0, normal; 2,
recruitment of each subject in this study. impaired; and 4, absent. Ankle jerks are scored as 0, normal;
Interns then reviewed the patients' clinical record for past 2, impaired in comparison with other reflexes (eg, knee jerk)
or present conditions that could affect neuropsychologic or and 4, absent. The total score varies between 0 and 33. A
postural performance. Data were collected to gather score of 0 indicates an absence neuropathy; 1 to 9, mild
information on (1) general health status. (2) medication neuropathy; 10 to 18, moderate neuropathy; and 19 to 33,
consumption, (3) daily activities, (4) integrity of the severe neuropathy.
neuromusculoskeletal system, and (5) any other aspect that No patient had to be rejected after the clinical examina-
could affect postural stability. tions. Table 2 presents details of the clinical examination for
Patients were then asked to complete 3 self-administered each group.
questionnaires. To measure disability in activities of daily
living as a result of neck pain, patients completed a validated Postural Stability Evaluation
French version of the Neck Disability Index (NDI).31 This An AMTI force platform (Model OR6-5; Advance
questionnaire was used for the 3 groups to control for any Mechanical Technology Inc, Watertown, MA) was used to
significant disabilities that could impair postural control. measure the displacement of the center of foot pressure
Pain severity was recorded on an analog 10-cm scale labeled (CoP). The force platform signal was sampled at 100 Hz, and
no pain at 0 cm and worst pain possible at 10 cm. Mental diagonal entries from the calibration matrix provided by the
status was measured with a validated French version of manufacturer were used to calibrate the platform. For each
Folstein's Mini-Mental State Examination (MMSE).32 A trial, subjects stood barefoot on the force platform using a
clinical assessment was performed to screen for any physical comfortable stance with feet together. They were asked to
condition that could affect postural stability. Those examina- fixate a cross located 2 m away at eye level. A total of twenty
tions include the following: examination of the spine 20-second trials were given under 2 visual conditions. In
(palpation, range of motion); postural stability and walking condition 1, vision was available throughout the 20-second
(Romberg, normal walking, heel to toe, on the heels, on the trial. In condition 2, subjects initiated the trials with their eyes
toes); eye examination (ophthalmoscopic, visual acuity, closed and opened them 10 seconds into the trial upon a
visual fields); autonomic nervous system (pupillary reflexes, signal generated by the computer. For both conditions,
arterial pressure standing and lying); carotid artery ausculta- subjects were simply asked to maintain a stable upright
tion; and lower extremities examination (pulse and neuro- posture. The 2 conditions were presented randomly. Famil-
logic examination according to Valk et al33). iarization with the experimental conditions was provided
The neurologic examination designed by Valk et al33 is before testing.
used to quantify the level of lower extremity neuropathy To examine the postural stability, we selected temporal
found in some patients. This examination uses a scoring intervals of 5 seconds for analysis. For each trial, the sway
system having 4 levels of neuropathy: normal, mild, behavior was evaluated (1) between the fourth and the ninth
moderate, and severe. It consists of the following tests: pain seconds (vision under condition 1 and no vision under
and light touch of the dorsum of the foot, vibration sense at condition 2) and (2) between the 11th and the 16th seconds
the ankle and position sense of the first toe. These tests are (vision under condition 1 and vision after a period of non-
scored separately as 0, normal; 2, impaired in comparison vision under condition 2). Figure 1 schematically illustrates
with proximal sensation; and 4, absent. Light touch is also these temporal intervals.30
evaluated in relation with the anatomic level below which it is Six dependent variables were used to characterize the
impaired and is scored as 1, toe; 2, midfoot; 3, ankle; 4, sway behavior during these 5-second intervals: range
midcalf; 5, knee. Strengths of the hallucis longus and (anteroposterior and mediolateral), velocity (anteroposterior
Journal of Manipulative and Physiological Therapeutics Boucher et al 187
Volume 31, Number 3 Postural Control and Osteoarthritis

and mediolateral), and excursion (anteroposterior and


mediolateral). The range indicates how far the participant's
CoP deviates from the base of support. The excursion is the
sum of the displacement in each direction over time. The
velocity is the sum of the displacement vectors divided by
the sampling time. Previous data indicate that postural
balance parameters can be used to assess the age-related
changes of the postural steadiness and are good predictors
for risk of falling.34

Statistical Analysis
Using a 1-way analysis of variance (ANOVA) for
independent samples, participants' characteristics were
compared between each group (Table 2). All dependent
variables were found to be distributed normally and were
submitted to a 2-way repeated measures ANOVA. This
analysis tested for the main effect of Group, the main effect
of Condition and the possible Group Condition interaction.
Post hoc comparisons were performed using lysergic acid
diethylamide tests. For all analyses, statistical significance
was set at P b .05.

RESULTS
The subjects of group 1 presented a significantly higher
Valk score (P = .0001) and a significantly lower MMSE
score (P = .0232) when compared with subjects of groups 2
and 3. According to Crum et al,35 any score more than 24 (of
30) is considered normal. The scores are corrected for degree
of schooling and age in the English version of the test. There
are no validated corrective factors for degree of schooling
and age available yet for the French version. Although we
did not take into consideration the degree of schooling of our
subjects in this experiment, the results show that all our
subjects were well above the 24 score limit. Hence, the
observed statistical difference does not reflect any cognitive
incapacity of group 1 subjects.
No group difference in pain scores was noted at the time
of testing. Finally, a significant increase in the NDI scores
was noted in group 1 when compared with group 3 (P =
.0059). Subjects' demographic data and clinical examination
scores are presented in Table 2.
Each subject was able to complete all trials throughout
every experimental condition. The 2-way ANOVA (Group
Condition) yielded a significant effect of condition for all 6
dependent variables (P b .0001). These differences were
characterized by a systematic significant increase of ranges,
velocity, and excursion under the no vision condition and Fig 2. Mean range (A), velocity (B), and excursion in the antero-
posterior plane (C). Group 1, clinical/high OA; group 2, age-
the vision after a period of no vision condition. matched low OA control group; group 3, healthy young controls.
Statistically significant group differences were only
present in the anteroposterior variables, whereas no group
differences were present for the mediolateral variables. anteroposterior excursion (F2,20 = 4.2474, P = .0290) were
Anteroposterior range (F2,20 = 5.1597, P = .0156), higher in group 1 when compared with group 2 (aged paired
anteroposterior velocity (F2,20 = 4.2468, P = .0290), and subjects) and group 3 (young adults). None of the Group
188 Boucher et al Journal of Manipulative and Physiological Therapeutics
Postural Control and Osteoarthritis March/April 2008

Table 3. Group means for the postural dependent variables in the proposed that disturbances of postural control in chronic neck
anteroposterior plane pain are dependent on the etiology. At this point, it is not clear
Group Mean SD CI 95% CI + 95% in the literature that postural balance is affected in
AP range 1 12.2 0.78 10.5 13.8 nontraumatized patients to the same extent as in traumatized
2 9.36 0.88 7.53 11.2 patients, and future studies should evaluate postural dis-
3 8.67 0.88 6.83 10.5 turbances in different cervical spine conditions.
AP velocity 1 6.29 0.41 5.43 7.15 It is the first time, to our knowledge, that postural control
2 4.81 0.47 3.83 5.78
3 4.70 0.47 3.73 5.68
in subjects with cervical osteoarthritis is studied. Postural
AP excursion 1 31.5 2.06 27.2 35.8 stability has been investigated in subjects with knee
2 24.0 2.34 19.2 28.9 osteoarthritis. 39,40 Those studies showed that postural
3 23.5 2.34 18.6 28.4 control is worse when these subjects are compared with
AP, Anteroposterior. healthy controls. Unfortunately, in these studies, the
presence of pain at the time of testing cannot be ruled out,
and therefore, changes in postural control may have been
Condition interactions were significant. Figure 2 illustrates triggered by the presence of pain rather than osteoarthritis.
the anteroposterior range, anteroposterior velocity, and Hassan et al41 investigated the effect of pain alleviation on
anteroposterior excursion for all 3 groups of subjects. quadriceps function and postural stability in subjects with
Group means for the postural dependent variables in the knee osteoarthritis. The authors showed that, even though
anteroposterior plane are presented in Table 3. marked knee pain reduction was associated with increased
activation and maximal voluntary contraction of the
quadriceps, postural sway did not change after significant
DISCUSSION decrease of pain. These results seem to indicate that
degenerative changes in articular tissues can affect postural
The main objective of this study was to determine if
control in presence or absence of pain. Conversely, Arokoski
postural balance parameters were modified in a group of
et al42 recently showed that hip osteoarthritis had no effect
patients with cervical osteoarthritis. The second objective
on static balance in men. Postural control can be modulated
was also to evaluate the possible combined effect of aging
by several factors such as joint flexibility, lower limb joint
and cervical osteoarthritis.
degeneration,39 vision problems,43,44 vestibular patholo-
gies,45 peripheral neuropathies,30 aging,46 muscle force, and
The Influence of Pain on Postural Control obesity.47,48 Conflicting results might be explained by
The present study suggests that postural sway quantified insufficient control of these different variables.
by anteroposterior range, anteroposterior velocity, and The association between pain and osteoarthritis remains
anteroposterior excursion is increased in patients with controversial, but many studies showed a relatively low
cervical osteoarthritis. In the past, postural stability and correlation between the 2 conditions. For instance, van der
trunk sway measures have been evaluated in whiplash Donk et al49 showed that osteoarthritis of the cervical facet
subjects with and without dizziness/vertigo.36,37 Sjstrm joints diagnosed by spinal x-rays was not related to neck
et al36 quantified postural stability of whiplash subjects pain, either in the men or the women. In the present study,
during 2-legged stance and 1-legged stance tasks. Their the significant differences in postural control between
results showed that whiplash subjects presented an increased subjects with cervical osteoarthritis and healthy age-paired
trunk sway in the 2-legged (eyes open) stance task performed subjects cannot be explained by the presence of pain because
on normal and foam surfaces. It is somehow difficult to visual analog scale scores were relatively low and similar for
compare subjects with cervical osteoarthritis and the all groups.
whiplash population studied by Sjstrm et al because most
of the whiplash subjects included in their study presented Influence of Somatosensory Changes in Postural Control
with vertigo or dizziness. Nevertheless, it was suggested that In this experiment, subjects with osteoarthritis of the
postural sway modifications in whiplash subjects may be due cervical spine showed clinical signs of degenerative
to a change weighting of sensory cues for balance control. neuropathy of the lower limbs. On one hand, it is well
Madeleine et al37 showed a greater center of pressure known that aging may affect all aspects of the nervous
displacement and greater displacement path values in system, from mental status to motor and sensory function
whiplash subjects compared with healthy controls. The and reflexes.50 For example, decreases in the number of hair
authors proposed that chronic whiplash subjects have a cells in both the canals and the otolith organs, and in the
distortion of the postural control system originating from number of nerve fibers in the vestibular nerve, may
cervical facet joints. Michaelson et al38 showed that whiplash eventually result in reduced vestibular excitability.51 On
subjects' postural balance was affected more than postural the other hand, this is a surprising result considering the fact
balance in chronic work-related cervical pain and therefore that group 2 patients showed very few signs of peripheral
Journal of Manipulative and Physiological Therapeutics Boucher et al 189
Volume 31, Number 3 Postural Control and Osteoarthritis

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