Impact of Seasonal Variations on Spasticity Assessment
and Treatment
Martha
Miller, Lisa Martin, Farooq Ismail, Chris Boulias, Lisa Lyons, Chetan P Phadke
Martha
Miller, Lisa Martin, Farooq Ismail, Chris Boulias, Chetan P. Phadke, Faculty of Medicine, University of Toronto, Toronto,
Canada
Farooq
Ismail, Chris Boulias, Lisa Lyons, Chetan P. Phadke, West Park Healthcare Centre, Toronto, Canada
Chetan
P. Phadke, Faculty of Health, York University, Toronto, Canada
Correspondence to: Chetan P. Phadke, Spasticity
Research Program, West Park Healthcare Centre, 82 Buttonwood Ave., Toronto,
Canada
Email: chetan.phadke@westpark.org
Telephone: +1-416-243-3600
Received: March 13,
2015
Revised: April 18, 2015
Accepted: April 21, 2015
Published online: May 13, 2015
ABSTRACT
Background:
Spasticity is treated using intramuscular botulinum toxin injections. Previous
reports of worsening of spasticity in cold weather suggest that spasticity
levels and botulinum toxin dose may both be influenced by seasonal temperature
changes.
AIMI: The aim of this
study was to determine the effect of seasonal temperature variation on
spasticity and botulinum toxin dosage.
Methods:
Medical charts of 132 participants in 3 diagnostic groups: (1) stroke (n=60);
(2) multiple sclerosis (n=34); and (3) cerebral palsy (n=38)
receiving treatment in an outpatient spasticity clinic were reviewed. Age, sex,
diagnosis, number of muscles injected, botulinum toxin dose, and spasticity
(Modified Ashworth Scale) were collected for summer and winter. Spasticity and botulinum toxin dose were
compared between summer and winter using separate paired t-tests for each
diagnostic group.
Results:
The spasticity level, botulinum toxin dosage, and total number of muscles in
summer versus winter months were not significantly different (p>0.05)
in any diagnostic group. Conclusions: Seasonal temperature variations appear to
have no effect on spasticity or botulinum toxin dosage. Performance of
spasticity measurements in warm indoor environment may have negated the impact
of seasonal temperature differences. Future studies should perform spasticity
measurements in temperature controlled rooms to mimic seasonal variations.
© 2015 ACT. All
rights reserved.
Key words: Muscle spasticity, Botulinum toxin, Stroke, Multiple
sclerosis, Cerebral palsy, Cold temperature, Hot temperature
Miller M, Martin L, Ismail F, Boulias C, Lyons L, Phadke
CP. Impact of Seasonal Variations on Spasticity Assessment and Treatment. International Journal of Neurology Research 2015; 1(2): 83-87 Available from: URL:
http://www.ghrnet.org/index.php/ijnr/article/view/1113
INTRODUCTION
Spasticity is a velocity-dependent increase in muscle tone, and is
associated with a variety of upper motor neuron lesions[1]. Although
the exact physiological mechanisms of spasticity are not fully understood, it
is thought to be caused by hyperexcitability of the stretch reflex, which
occurs after an upper motor neuron lesion[2]. Spasticity can result
in reduced range of motion, pain, stiffness, and loss of function, all of which
may decrease one’s ability to participate in activities of daily living[3].
Spasticity is commonly seen in a number of diagnostic groups such as cerebral
palsy (CP), multiple sclerosis (MS), stroke, brain injuries, and spinal cord
injuries[2].
A diverse
range of internal and environmental factors can contribute to an increase in
spasticity[4]. One such factor known to worsen spasticity is cold,
outdoor (weather) and indoor (air-conditioning), which is especially relevant
in geographic areas of the globe with extreme seasonal temperature variation[5].
Much of our current understanding on the effects of seasonal temperature
variations on spasticity are the result of anecdotal reports, with little objective
evidence[4,6]. While these anecdotal reports provide the basis of
our understanding of the relationship between temperature and spasticity, they
are biased because of self-reporting, which by nature is subjective and open to
interpretation.
To date, there
is little research that objectively examines the relationship between
temperature and spasticity. A study
by Nilsagard et al (2006) examined the effect of a cooling vest on
spasticity in heat-sensitive patients with MS, and found no statistically
significant difference[7]. However, the use of a cooling vest is
problematic because individuals typically experience spasticity in their
extremities, which would be unaffected by the vest. A study by Chiara et al (1998)
found that immersion in a cold bath increased spasticity in participants with
MS[8]; however, the bath water was 24 degrees Celsius, and,
therefore, not comparable to the cold temperatures reflected in other studies.
The above studies lack ecological validity since use of cooling vests and cold
baths to simulate the effects of a cold environment might vary from what a
person experiences in the real world where ambient temperatures can fall down
to and below freezing.
Spasticity can
affect both upper and lower limbs and one of the available treatment is
localized intramuscular injections of botulinum toxin (BoNTA)[3].
From a physiological perspective, BoNTA works to relieve spasticity by
inhibiting the release of acetylcholine at the neuromuscular junction, thereby
producing paralytic effects on the injected muscle to decrease tone and to
allow stretching of the muscle fibers[3]. Treatment effects of BoNTA
are not permanent, and, therefore, injections are typically required every 3-4
months[3]. As such, patients will often receive injections in both
winter and summer months.
Typically, higher doses of BoNTA are associated with higher levels of
spasticity. Thus, if spasticity levels are higher in winter, it is possible for
the BoNTA dosage to be higher in winter as well.
Given the lack of objective data, there is a gap in the literature
regarding the relationship between temperature, spasticity, and BoNTA dosage.
There is a need to systematically examine the relationship between spasticity
levels and related BoNTA dosage in winter versus summer months. Thus, this study carried out a
retrospective chart review to objectively compare the differences in spasticity
levels, as measured by the Modified Ashworth Scale (MAS), and related BoNTA
dosage in winter versus summer months. The objective of this retrospective
study was to compare the differences in spasticity levels (MAS) and BoNTA
dosage in winter versus summer months.
METHODS
This was a quantitative, single site, retrospective chart review. In
compliance with Helsinki Declaration, ethical approval for this study was
provided by the West Park Healthcare Centre and University of Toronto Research
Ethics Boards. Since only patient past health records were accessed and no
patients directly observed in this study, the ethics board did not require us
to obtain informed consent from participants. Data was obtained from the
participants’ health records to objectively compare spasticity level and BoNTA
dosage in winter versus summer months. Because spasticity is most commonly
associated with stroke, MS, and CP[1], participants were selected
from these three diagnostic groups. Non-random, purposive sampling was used to
obtain 132 medical charts from adult patients age 18 and over with stroke (n=60),
MS (n=34), or CP (n=38) who were receiving, or had previously
received, treatment with BoNTA from an outpatient spasticity clinic. This was a
convenience sample since it was only feasible for students to collect data from
up to 132 patient medical charts.
The toxin dose
may be varied by physicians within the first three treatment cycles to
determine the optimal dosage of BoNTA required to best manage a client’s
spasticity. Thus, participants were
excluded from the study if they had received three or fewer treatments of BoNTA
injections. All patients were treated with two physicians with experience
>10 years of working together in spasticity management and BoNTA injections
and similar practice patterns. Participants were also excluded if they had not
received BoNTA injections in consecutive summer and winter months. Summer
months were considered June 21 to September 21 (± two weeks), and winter months
were considered December 21 to March 21 (± two weeks). Maximum and minimum
temperature (º Celsius) data on the day of spasticity assessments was gathered
using climate data from Government of Canada[9] and The Weather
Network[10]. All medical data was collected from participants’
electronic and paper medical records at an outpatient spasticity clinic in
Toronto, Canada. The following pieces of data were collected from participant
charts: total BoNTA dosage, injection location, number of injections, MAS
scores, age, sex, and body weight.
Modified Ashworth
Scale (MAS)
The MAS is an assessment of the clinician’s perception of resistance
after moving the affected joint through passive range of motion[11]. Craven and Morris (2010) found the
intra-rater reliability for the MAS to be fair-to-perfect (0.20<k<1.0),
and inter-rater reliability was found to be poor-to- moderate (k<0.60)[12-14].
Although measures of reliability are low, there is evidence to suggest that a
change in MAS scores indicates a change in muscle spindle excitability[15]
and level of excitation at the spinal cord neurons[16]. MAS remains
the primary choice for clinicians to measure spasticity. MAS in this study was
performed by clinicians with experience in spasticity assessment of >5
years. All spasticity assessments were performed by the same two clinicians
(upper limb – occupational therapists and lower limb – physiotherapist) in
supine position.
Data Analysis
Since MAS is an ordinal scale, we chose to use non-parametric tests
(Wilcoxon signed rank test) to make statistical comparisons for data in summer
versus winter months (p<0.05). Rather than assessing spasticity
levels for each individual muscle, specific muscle groups were chosen; namely,
wrist flexors, elbow flexors, and ankle plantar flexors, as these groups have
been found to be most commonly treated for spasticity[1]. The MAS
scores for each muscle group, the sum of BoNTA dosage, and the total number of
muscles injected were compared in summer versus winter months using paired
t-tests. The above analyses were carried out for the whole group, as well as
separately for each of the three diagnostic groups using IBM SPSS software
version 22 (IBM Corporation, New York). Graphs were prepared using a Microsoft
Excel add-on (XL Toolbox © 2008-2011 Daniel Kraus, Würzburg,
Germany).
RESULTS
A total of 132 participants were recruited with a diagnosis of either
stroke (n=60), MS (n=34), or CP (n=38). The age range of
participants was 19-88 years (Mean=55.6, SD=17.1). The male:female ratio was
64:68 (total participant group), 22:16 (stroke), 10:24 (MS), and 32:28 (CP) in
our participants. For other demographic data, see table 1. Average total number
of muscles injected was 6 muscles in summer and 6 muscles in winter. Average
summer temperatures (º Celsius) on the day of testing were 26±6℃ (maximum) and 16±4℃ (minimum) and average winter
temperatures were -2 ±6℃ (maximum) and -7 ±6℃ (minimum).
MAS score and
BoNTA in summer versus winter
Spasticity levels and BoNTA dosage in summer versus winter months were
not significantly different (p>0.05) for any of the diagnostic
groups, as well as for the group as a whole (Figures 1 and 2). There was no
significant difference between total number of muscles injected in summer
versus winter for any of the diagnostic groups, as well as for the group as a whole
(p>0.05).
Not all
muscles were injected in all patients; however, data from individual muscles
did not show a significant change in either BoNTA dosage (Table 2) or
spasticity measured using MAS (Table 3) between summer and winter. Only in the
gastrocnemius muscle in the MS group 37 units more were injected in winter vs.
summer; however this number is unlikely to be significant because of high
standard deviation (100 units; see Table 2). Finger flexors and soleus muscle
in the stroke group showed a slightly higher median MAS score in winter (MAS=2)
compared to summer (MAS=1.5 or 1+; p>0.05); see Table 3. Similarly,
the hip adductors in the MS group showed higher median MAS in winter than
summer.
Discussion
In this study, seasonal temperature variations although significant,
appear to have no effect on spasticity level, BoNTA dosage, or total number of
muscles injected. These findings are inconsistent with previous research[5],
demonstrating that patients perceive that cold weather worsens their
spasticity. A study by Shirado et al (1995) investigated outdoor winter
activities of spinal cord-injured patients, and found that 17% of participants
who were able to go outside in the winter reported experiencing increased
spasticity in their upper and lower extremities[6]. Additionally,
all of these participants believed that their spasticity worsened with direct
exposure to cold weather[6]. A similar study conducted by Fleuren et
al (2009), which also explored the perceptions of spasticity in patients
with spinal cord injury, found that 58% of participants identified other
factors that contributed to spasticity, which were not listed on the
questionnaire provided[17]. Temperature/climate (both hot and cold) was
among the other factors that were listed.
Although the
exact mechanism is unclear, there are several potential pathways that can
explain the worsening of spasticity in cold weather. One potential mechanism is
the hypersensitivity of the neurons in the spinal cord in patients with
spasticity as seen by testing the stretch reflexes. It is possible that on top
of this reflex hypersensitivity, cold exposure may further amplify the
shivering response designed to regulate body temperature[18,19]. It
is also possible that blood flow to the extremities when exposed to cold is
redirected to the body core in order to preserve heat and minimize heat loss
inadvertently amplifying the effect of cold exposure[19].
A potential
explanation as to why there was no significant change in MAS scores in winter
versus summer could be due to the fact that participants were seated in an
indoor waiting room prior to administering the MAS. Because participants were
seated in a temperature controlled room (heated in the winter and
air-conditioned in the summer), the temperatures they experienced were not
necessarily reflective of outdoor seasonal temperatures. Even if there was an
effect of temperature on spasticity, the effect may have dissipated by the time
patients were tested in the temperature controlled testing environment. There
is also some research data to suggest that a cold breeze or air-conditioned
environments can increase spasticity[20,21]. As such, even indoor
temperatures, if sufficiently cold enough, could potentially worsen spasticity.
Future studies should perform spasticity measurements in temperature controlled
rooms (cold and hot) to mimic seasonal outdoor temperature variations more
accurately.
There are
several factors that may explain the lack of change in BoNTA dosage between
summer and winter months. It is a complex process for physicians to determine
the most appropriate BoNTA dosage for an individual. Once a stable dose has
been achieved (usually after 2-3 injection cycles) physicians typically do not
vary doses from season to season. One explanation for this is that there are
multiple means of managing spasticity, including oral anti-spasticity
medications, as well as daily stretching exercises, which can both be used to
manage fluctuations in spasticity levels without altering the BoNTA dosage
(Graham, 2013). We did not record the dose of oral anti-spasticity medications
in summer vs. winter. In addition, an increase in spasticity – in particular
with respect to the lower extremities – may allow for improved function in
certain cases where the increased tone can assist with ambulation or transfers.
In these cases the goal may not be to reduce spasticity because it is serving a
functional purpose.
The use of the
MAS as a measure of spasticity could be considered a limitation of this study.
Despite being a commonly used clinical measure of spasticity, there remains a
high degree of subjectivity to the scale[3]. Although lengthier and
more complex to administer, the Tardieu Scale is considered a more objective
measure of spasticity[3] and could be used in future studies to
increase the reliability and validity of results. There are a variety of
environmental factors thought to increase levels of spasticity; however, this
study focused specifically on the effect of seasonal variations in temperature
on spasticity levels and related BoNTA dosage. There are a number of variables that
were not accounted for in this study that may affect spasticity, such as
fatigue, stress, illness, and injury, among many others[4]. We did
not include other data such as physiotherapy and occupational therapy
interventions in this chart review that may have potentially affected the
outcome measures. Future prospective studies should consider a research design
that would allow for more rigorous control of confounding variables.
Conclusions
Seasonal temperature variations were found to have no effect on either
spasticity level, as measured by the MAS, or BoNTA dosage. Future studies could
consider using a temperature controlled room to simulate outdoor temperature,
examine the use of additional spasticity management methods in conjunction with
BoNTA dosage, and use a more objective spasticity measure.
Acknowledgements
The authors wish to thank the West Park Foundation for their support.
CONFLICT OF INTERESTS
The Author have no conflicts of interest to declare.
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Peer reviewer: Fang Li, MD, PhD,
Department of Rehabilitation Medicine, Huashan Hospital, Fudan University,
Shanghai, 200040, China.
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