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Musculoskeletal reflex function in the joint hypermobility syndrome.

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Arthritis & Rheumatism (Arthritis Care & Research)
Vol. 57, No. 7, October 15, 2007, pp 1329 –1333
DOI 10.1002/art.22992
© 2007, American College of Rheumatology
CONTRIBUTIONS FROM THE FIELD
Musculoskeletal Reflex Function in the Joint
Hypermobility Syndrome
WILLIAM R. FERRELL,1 NICOLA TENNANT,2 RONALD H. BAXENDALE,3 MARION KUSEL,3
ROGER D. STURROCK4
Introduction
Joint hypermobility syndrome (JHS) is a heritable disorder
of the connective tissues characterized by hypermobility
and musculoskeletal pain in the absence of overt signs of
systemic inflammatory joint disease. The gene defect remains unknown and diagnosis relies upon clinical signs
and symptoms (1). Although there is as yet no firm pathologic basis, this condition is increasingly recognized as a
clinical entity (2) but has no definitive treatment and
therefore poses a challenge to treatment. We previously
observed a proprioceptive deficit at the proximal interphalangeal joint (3) and the knee joint (4) of patients with JHS
compared with age- and sex-matched controls, suggesting
a neurophysiologic deficit. More recently, we demonstrated that a home-based program of closed kinetic chain
exercises resulted not only in quality of life and symptomatic improvement (as assessed by the Short Form 36 Health
Survey and visual analog scores) as well as increased
muscle power, but also, more significantly, in enhanced
knee joint proprioception (5). Having demonstrated the
effectiveness of this home-based exercise program, we describe a more focused investigation of reflex function of
muscles acting at the knee joint in patients with JHS. The
question we sought to answer was whether, in addition to
the known proprioceptive deficits in patients with JHS,
abnormalities of musculoskeletal reflex function occur and
Supported by the Arthritis Research Campaign (15451).
1
William R. Ferrell, MB, ChB, PhD, FRCP: Centre for
Rheumatic Diseases, Royal Infirmary, Glasgow, and the Institute of Biomedical and Life Sciences, University of Glasgow, Scotland, UK; 2Nicola Tennant, MA, MSc, MCS: Royal
Infirmary, Glasgow, Scotland, UK; 3Ronald H. Baxendale,
BSc, PhD, Marion Kusel, HND: Institute of Biomedical & Life
Sciences, University of Glasgow, Scotland, UK; 4Roger D.
Sturrock, MD, FRCP: Centre for Rheumatic Diseases, Royal
Infirmary, Glasgow, Scotland, UK.
Dr. Sturrock has received consultancies and/or honoraria
(less than $10,000 each) from Abbott and Schering-Plough.
Address correspondence to William R. Ferrell, MB, ChB,
PhD, FRCP, Centre for Rheumatic Diseases, Royal Infirmary, 10 Alexandra Parade, Glasgow, Scotland, UK G31
2ER. E-mail: w.ferrell@bio.gla.ac.uk.
Submitted for publication October 18, 2006; accepted in
revised form February 22, 2007.
AND
if the same exercise program we previously found to be of
benefit in these patients could improve such dysfunction.
Neurophysiologic analysis of reflex function in patients
with JHS is presently lacking and this study is the first to
investigate this aspect.
Patients and Methods
Patients. Fifteen patients with JHS were recruited from
the hypermobility clinic at Glasgow Royal Infirmary. The
diagnosis of JHS was based on the revised Brighton criteria
(1), which for the present study required the presence of 2
major criteria or 1 major and at least 2 minor criteria. Major
criteria included joint hypermobility score ⱖ4, based on
the 0 –9 scoring system developed by Beighton et al (6), or
arthralgia in ⱖ4 joints for ⱖ3 months. Minor criteria included other features associated with the syndrome such
as dislocation/subluxation of joints, abnormal skin signs,
herniae or prolapse, or soft tissue rheumatism (1). An
additional entry criterion for the study was knee joint
pain. Patients with JHS were predominantly female (13 of
15) with a mean ⫾ SD age of 25.9 ⫾ 8.1 years (range 14 –39
years). The mean ⫾ SD Beighton score was 6.6 ⫾ 1.8 (range
4 –9). Hypermobility was also scored using a modification
of the Contompasis system (maximum score 56) (7), and
the mean ⫾ SD score was 34.6 ⫾ 4.4 (range 26 – 41).
A parallel control group of 11 healthy individuals with
normal mobility (9 female, mean ⫾ SD age 27.3 ⫾ 6.3
years, range 15–39 years, mean ⫾ SD Beighton score 0.7 ⫾
1.0), recruited from staff and student volunteers unaware
of the objectives of the study, was also examined on one
occasion only. The study received approval from the local
ethics research committee.
Musculoskeletal reflex testing. Electromyographic (EMG)
recordings were obtained from the rectus femoris muscle
using a small skin mounted preamplifier with integrated
surface electrodes. Prior to application, the skin was
cleaned with alcohol to reduce impedance and improve
the signal-to-noise ratio. Electrical signals were amplified
⫻1,000 (NL104; Digitimer, Welwyn Garden City, UK) and
band pass filtered (10 –3,000 Hz). The power spectrum of
recorded EMG signals ranged from 10 to 300 Hz. A constant current stimulator (DS7A; Digitimer) was used to
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Ferrell et al
voluntary contraction, as judged by monitoring on a screen
the integrated EMG recorded from quadriceps femoris and
maintaining this at a fixed level on the screen. A total of 60
pulses were delivered and the responses were digitized
using a CED 1401 interface (Cambridge Electronic Design,
Cambridge, UK) at 1 kHz and stored on a personal computer for detailed offline analysis using Spike 2 software,
version 2.15 (Cambridge Electronic Design). The recorded
signal was processed by averaging poststimulus time, and
segmental reflex responses typically occurred within
20 – 40 msec of the stimulus (Figure 1B). A reflex response
was considered to have occurred if the rectified averaged
signal exceeded 2 SDs from the baseline, calculated from
an average of the 30-msec period preceding the electrical
stimulus. Previous work (8) has demonstrated that in
healthy persons with normal mobility the reflex is stable,
with the coefficient of variation between trials ranging
from 0.08 to 0.18 (mean ⫾ SEM 0.13 ⫾ 0.02). Reflex modulation was calculated by dividing the reflex area by the
control area. The reflex area was defined as the product of
the magnitude of the EMG signal by the time interval
during which the reflex response exceeded 2 SDs. For the
control area, the area of the EMG signal was calculated for
the same time interval but during the prestimulus period.
Study design. The study design involved repeated pretesting on 2 occasions followed by postintervention testing. Reflex function was assessed in patients with JHS on
2 occasions 8 weeks apart, during which time no intervention was performed. The second measurement permitted
assessment of the stability of the reflex across the 8-week
period. The patients then undertook an 8-week homebased exercise program of closed kinetic chain exercises as
previously described (5), after which reflex function was
tested once again. For the control group, measurements
were only obtained on 1 occasion. Two patients moved
away and therefore dropped out of the study before the
second measurement and the exercise program, but the
first measurement was obtained for both patients.
Figure 1. A, Diagrammatic representation of the recording and
stimulation arrangements. B, Electromyographic (EMG) recordings (average of 60 sweeps) obtained from one subject with normal
mobility with the knee extended (0° flexion) and flexed (20°
flexion). Electrical stimulus applied at time 0. QF ⫽ quadriceps
femoris; F ⫽ femur; P ⫽ patella; T ⫽ tibia.
deliver rectangular pulses (width 0.2 msec) at 1 Hz transcutaneously via monopolar electrodes to the common peroneal nerve at the fibular neck at 1.3 times the motor
threshold. This was sufficient to cause a minor twitch of
the anterior tibial muscles accompanied by a mild tapping
sensation. The experimental setup is illustrated in Figure
1A. The knee joint was fixed at a specified position and
participants were required to perform an isometric contraction of the thigh extensors at 20% of the maximum
Statistical analysis. Data are presented as the mean ⫾
SD or mean ⫾ SEM. Comparisons were performed using
analysis of variance (ANOVA) or t-tests as appropriate for
interval scale data and chi-square or Fisher’s exact test for
nominal scale data (Sigmastat; SPSS, Chicago, IL), all tests
being 2-tailed with P values less than 0.05 being considered significant.
Results
The reflex response was present in all controls (n ⫽ 11)
with the knee extended (0° flexion) and the magnitude
reduced on knee flexion, as illustrated in Figure 1B for a
single participant. The latency of the reflex was 18 – 41
msec, consistent with a segmental oligosynaptic spinal
reflex pathway. By contrast, responses in patients with JHS
were more variable (Figure 2A), with the reflex present in
8 (53%) of 15 patients but absent in 7 (47%) of 15 patients;
the difference between the control and JHS groups was
significant (␹2 ⫽ 4.85, 1 df, P ⬍ 0.01). However, the reflex
latency onset in the control group did not differ signifi-
Musculoskeletal Reflex Function in Joint Hypermobility Syndrome
1331
cantly (unpaired t-test; t[17] ⫽ 0.43, P ⫽ 0.64) from the JHS
group (mean ⫾ SEM 26.1 ⫾ 1.4 msec versus 27.1 ⫾ 1.0
msec).
When reflex testing was repeated in the patients with
JHS (2 of whom dropped out from the study after the first
test) after 8 weeks, we found that the reflex remained
absent in patients who did not show the reflex at the first
assessment (Fisher’s exact test; P ⫽ not significant [NS];
n ⫽ 6), whereas it persisted in the other patients (Fisher’s
exact test; P ⫽ NS; n ⫽ 7). Mean ⫾ SEM reflex modulation,
expressed as the percent change of the reflex area divided
by the control area, was 104% ⫾ 2.3% in patients with JHS
whose reflex was absent compared with 133% ⫾ 6.3% in
patients showing the reflex; this difference was significant
(unpaired t-test; t[13] ⫽ 4.08, P ⫽ 0.0013).
The effect of home-based exercise was tested in the
patients with JHS to establish whether the reflex could
now be elicited. Following the 8-week exercise program,
the reflex was demonstrable in all patients in whom the
reflex could not previously be elicited (Fisher’s exact test;
P ⫽ 0.002), as illustrated in Figure 2B for one patient. For
the 7 of 13 patients who showed the reflex at the previous
2 tests, this was unchanged by the exercise program (Fisher’s exact test; P ⫽ NS).
Although it is well recognized that in individuals with
normal mobility the reflex is modulated by knee joint
position and invariably diminishes on movement into
flexion, the effect of hyperextension is unknown and was
investigated. As anticipated, the reflex was maximal with
the knee at 0° flexion and decreased on flexion, but surprisingly the reflex also diminished upon hyperextension
of the knee, as shown in Figure 3A for a single patient.
This was true for all 7 patients with JHS who were tested
(Figure 3B), and this finding was significant (one-way
ANOVA; F[2] ⫽ 4.32, P ⫽ 0.02). Interestingly, the magnitude of reflex attenuation was similar despite the fact that
the degree of hyperextension (10°) was much less than the
extent of flexion (30°).
Discussion
Figure 2. A, Electromyographic (EMG) recordings (averages of 60
sweeps) from one patient with joint hypermobility syndrome
(JHS) showing a reflex response (upper panel, reflex denoted by
arrow) and another patient with JHS whose response was absent
(lower panel). Knee held at 0° flexion in both patients. B, Three EMG
recordings (average of 60 sweeps) obtained from the same JHS
patient showing the absence of a reflex response on initial testing
(pre-exercise 1), after 8 weeks without intervention (pre-exercise
2), and following an 8-week home-based exercise program of
closed kinetic chain exercises (post-exercise) when a segmental
reflex is present (arrow). Knee held at 0° flexion in all cases.
There is increasing evidence indicating that subtle neurophysiologic abnormalities occur in patients with JHS. Autonomic dysfunction has been described in this patient
group (9) and we previously demonstrated reduced proprioceptive acuity in the finger joints (3) and knee joints
(4) of these patients. Therefore, it is perhaps not unexpected to discover that reflex function is also impaired,
although not in all patients with JHS. This reflex arises
from stimulation of group I afferent fibers in the common
peroneal nerve that evoke non-monosynaptic excitation of
quadriceps motoneurons (10). Group Ib afferent fibers are
thought to constitute the afferent limb of the musculoskeletal reflex through an oligosynaptic pathway (11), which is
consistent with the short reflex latency observed in the
present study. The reflex is invariably present in individuals with normal mobility with the knee at 0° of flexion
(12), therefore its absence in almost half of the patients
with JHS is striking, although it is unclear why the reflex
could be elicited in the other half of this patient group.
One clue might be that those patients in whom the reflex
1332
Figure 3. A, Averaged rectified electromyographic (EMG) recordings (60 sweeps) from the same patient with joint hypermobility
syndrome (JHS) at 3 knee joint positions: flexed, extended, and
hyperextended. Dashed lines indicate 2 SDs and reflex responses
are considered to be significant when the signal exceeds 2 SDs
(shaded area). Both flexion and hyperextension resulted in reduced magnitude of responses compared with the control position (0° flexion). B, Comparison of reflex responses (expressed as
a percentage of the response in the control position, 0° flexion) at
different knee joint positions in 7 patients with JHS (mean ⫾
SEM). * P ⬍ 0.05, significant difference from the control position.
could be elicited were more physically active when questioned about their daily activities. Unfortunately, quantitative data were not collected as part of this investigation,
so this hypothesis remains unproven.
A remarkable observation was that in all patients failing
to show a reflex initially, a reflex could be elicited following the exercise program. This finding parallels our previous observation that proprioception improved following
the same exercise program, and suggests that similar
mechanisms may be at work, perhaps via facilitation of
interneuronal pathways.
As anticipated, the reflex diminished on knee flexion,
but surprisingly, hyperextending the knee diminished
rather than enhanced the reflex. This finding implies that
there is an optimal position for eliciting the reflex and
Ferrell et al
hyperextension of the joint is disadvantageous. In functional terms, the significance of the reflex is that it clearly
indicates facilitation of thigh extensor motoneurons as the
knee is extended, but only up to a point. Such facilitation
is likely to be important for bracing the knee at heel strike
in anticipation of load bearing, and it is interesting in this
context that patients with JHS can describe the knee as
“giving way,” often when negotiating stairs. The decreasing facilitation of knee extensor motoneurons upon hyperextension of the knee provides a plausible neurophysiologic explanation for this phenomenon.
The study design had clear limitations, being semicontrolled and lacking a patient-oriented outcome. Future
studies should be designed to incorporate appropriate patient-oriented outcome measures as well as improved control of the variables. It is conceivable that pain could have
affected the reflex. However, this is unlikely to be the case
because all patients experienced knee joint pain at the
beginning of the study, and yet in 7 patients the reflex was
absent whereas in 8 patients it was present, suggesting that
pain does not influence this reflex pathway. It has been
shown that proprioception is unaffected by pain (13),
therefore it is likely that a segmental spinal reflex is even
less likely to be affected.
The advantage of reflex testing is that it provides a
highly objective method for assessing neurophysiologic
function in patients and is not readily subject to conscious
influences. A disadvantage is the requirement for recording equipment and procedures, which are not translatable
to the clinical environment. However, the robustness of
the technique and absence of subjective bias make it suitable for investigating neurophysiologic function in other
musculoskeletal diseases where reflex dysfunction is suspected. Analysis of neurophysiologic function in rheumatologic diseases has been limited, but such an approach
offers the prospect of better understanding of neurologic
dysfunction and assessment of the effectiveness of physiotherapeutic intervention.
AUTHOR CONTRIBUTIONS
Dr. Ferrell had full access to all of the data in the study and
takes responsibility for the integrity of the data and the accuracy
of the data analysis.
Study design. Ferrell, Tennant, Sturrock.
Acquisition of data. Tennant, Baxendale, Kusel, Sturrock.
Analysis and interpretation of data. Ferrell, Baxendale.
Manuscript preparation. Ferrell, Tennant, Sturrock.
Statistical analysis. Ferrell, Baxendale, Sturrock.
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Musculoskeletal Reflex Function in Joint Hypermobility Syndrome
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9. Gazit Y, Nahir AM, Grahame R, Jacob G. Dysautonomia in the
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10. Fournier E, Meunier S, Pierrot-Deseilligny E, Shindo M. Evidence for interneuronally mediated Ia excitatory effects to human quadriceps motoneurones. J Physiol 1986;377:143– 69.
11. Brooke JD, McIlroy WE. Vibration insensitivity of a short
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