Received: 18 April 2019
|
Revised: 21 October 2019
|
Accepted: 24 November 2019
DOI: 10.1002/brb3.1509
ORIGINAL RESEARCH
Increased muscle tone and contracture late after ischemic
stroke
Carina U. Persson1,2
| Lukas Holmegaard3,4
Christian Blomstrand3,6 | Katarina Jood3,4
| Petra Redfors3,4 | Christina Jern5,6,7 |
Institute of Neuroscience and Physiology, Department of Clinical Neuroscience, Rehabilitation Medicine, Sahlgrenska Academy at the University of
Gothenburg, Gothenburg, Sweden
1
2
Region Västra Götaland, Department of Physiotherapy, Sahlgrenska University Hospital/Östra, Gothenburg, Sweden
3
Department of Clinical Neuroscience, Institute of Neuroscience and Physiology, Sahlgrenska Academy at the University of Gothenburg, Gothenburg, Sweden
4
Region Västra Götaland, Department of Neurology, Sahlgrenska University Hospital, Gothenburg, Sweden
5
Department of Clinical Pathology and Genetics, Institute of Biomedicine, Sahlgrenska Academy at the University of Gothenburg, Gothenburg, Sweden
6
Stroke Centre West, Sahlgrenska Academy at the University of Gothenburg, Gothenburg, Sweden
7
Region Västra Götaland, Department of Clinical Genetics and Genomics, Sahlgrenska University Hospital, Gothenburg, Sweden
Correspondence
Carina U. Persson, Institute of Neuroscience
and Physiology, Department of Clinical
Neuroscience, Rehabilitation Medicine,
Sahlgrenska Academy, University
of Gothenburg, Per Dubbsgatan 14,
Gothenburg S-413-45, Sweden.
Email: carina.persson@neuro.gu.se
Funding information
The Swedish Stroke Association; Renée
Eander’s Foundation, Grant/Award
Number: 2017-01-20; The Swedish
Research Council, Grant/Award Number:
K2014-64X-14605-12-5; The Swedish
Hypertension Society; The Yngve Land
Foundation for Neurological Research; The
Local Research and Development Board for
Gothenburg and Södra Bohuslän, Grant/
Award Number: VGFOUGSB-669461
and VGFOUGSB-701851; The Rune and
Ulla Amlöv Foundation for Neurological
Research; The Swedish State under the
ALF agreement, Grant/Award Number:
ALFGBG-508331 and ALFGBG-720081;
The Swedish Heart Lung Foundation, Grant/
Award Number: HLF-20160316; The John
and Brit Wennerström Foundation for
Neurological Research; The Region Västra
Götaland
Abstract
Background: Systematic studies on increased muscle tone and spasticity late after
ischemic stroke, without any selection, are limited. Therefore, we aimed to determine
the prevalence of increased muscle tone, classical spasticity and contracture and predictors of increased muscle tone seven years after stroke.
Methods: Consecutive patients with acute ischemic stroke <70 years of age (n = 411)
were recruited to the Sahlgrenska Academy Study on Ischemic Stroke. Symptoms
at index stroke were assessed using the Scandinavian Stroke Scale. Seven years
after stroke, survivors (n = 358) were invited for follow-up assessments, of whom
292 agreed to participate and 288 contributed data. Muscle tone according to the
Modified Ashworth scale, classical spasticity, and contracture was assessed by a
neurologist. The associations between increased muscle tone and characteristics at
index stroke and recurrent strokes during follow-up were investigated using logistic
regression analysis.
Results: Increased muscle tone was recognized in 99 participants (34%): 94 (33%)
in the upper limbs, and 72 (25%) in the lower limbs. Classical spasticity was found
in 51 participants (18%) and contracture in 26 (9%). Age (odds ratio [OR] 1.03 [95%
confidence interval [CI] 1.00–1.06]), arm paresis (OR 1.76 [95% CI 1.40–2.2]), aphasia
(OR 1.68 [95% CI 1.12–2.51]), and facial palsy (OR 2.12 [95% CI 1.10–4.07]) were
independent predictors of increased muscle tone.
The peer review history for this article is available at https://doi.org/10.1002/brb3.1509
This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium,
provided the original work is properly cited.
© 2020 The Authors. Brain and Behavior published by Wiley Periodicals, Inc.
Brain and Behavior. 2020;10:e01509.
https://doi.org/10.1002/brb3.1509
wileyonlinelibrary.com/journal/brb3
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Conclusions: One-third of patients with ischemic stroke before 70 years of age
showed increased muscle tone at 7-year follow-up. Half of them also had classical
spasticity. Age, arm paresis, aphasia, and facial palsy at index stroke were predictors
of increased muscle tone poststroke.
KEYWORDS
muscle spasticity, rehabilitation, stroke
1 | I NTRO D U C TI O N
Previous studies have consistently shown that initial impairments in
sensorimotor function are associated with the risk of developing increased muscle tone after stroke (Lundstrom, Smits, Terent, & Borg,
After stroke, increased muscle tone and spasticity may have a neg-
2010; Opheim, Danielsson, Alt Murphy, Persson, & Sunnerhagen,
ative impact on health-related quality of life (Gillard et al., 2015),
2015; Urban et al., 2010). The role of age is less clear (Lundstrom et
motor control recovery (Singer, Nishihara, & Mochizuki, 2016), mus-
al., 2008; Shin et al., 2018). The present study aimed to investigate
cle architecture (Dias et al., 2016), and daily activities (Duncan et
the long-term prevalence of increased muscle tone, classical spas-
al., 1997). Increased muscle tone is also associated with fourfold
ticity, and contracture and to identify the predictors of increased
higher direct costs related to hospitalization, municipality services,
muscle tone seven years after stroke.
primary care, and medication (Lundstrom, Smits, Borg, & Terent,
2010). The prevalence of increased muscle tone during the first
12 months after stroke varies between 4% and 46% (Lundstrom,
Smits, Borg, et al., 2010; Lundstrom, Terent, & Borg, 2008; Opheim,
Danielsson, Alt Murphy, Persson, & Sunnerhagen, 2014; Shin et al.,
2 | M E TH O DS
2.1 | Population
2018; Sommerfeld, Eek, Svensson, Holmqvist, & von Arbin, 2004;
Urban et al., 2010; Watkins et al., 2002), probably because of dif-
The Sahlgrenska Academy Study on Ischaemic Stroke is a pro-
ferences in the case-mix and study design. Studies beyond the first
spective and longitudinal study (Jood, Ladenvall, Rosengren,
year are scarce. At 18 months after ischemic or hemorrhagic stroke,
Blomstrand, & Jern, 2005), in which 600 consecutive patients suf-
increased muscle tone was found in 20% of 66 individuals (Welmer,
fering a first-ever or a recurrent acute ischemic stroke at the age of
von Arbin, Widen Holmqvist, & Sommerfeld, 2006). However, less
18–69 years were recruited at four stroke units in Western Sweden
is known about the extent to which increased muscle tone affects
between August 1998 and December 2003. The current study in-
long-term stroke survivors.
cludes the 411 participants who were recruited at the stroke unit at
Most studies investigating increased muscle tone after stroke
Sahlgrenska University Hospital at Sahlgrenska. Seven years post-
(Lundstrom, Smits, Borg, et al., 2010; Lundstrom et al., 2008; Opheim
stroke, those who were still alive (n = 358) were invited for follow-up
et al., 2014; Shin et al., 2018; Sommerfeld et al., 2004; Urban et al.,
assessments. The procedures followed were in concordance with
2010; Watkins et al., 2002) assessed muscle tone using the Modified
the institutional guidelines. All patients gave their written informed
Ashworth scale (Bohannon & Smith, 1987; Peacock & Staudt, 1991).
consent at baseline. For those patients who were unable to com-
The Modified Ashworth scale quantifies the resistance that is felt
municate, the next of kin consented. Surviving participants declin-
when muscles are passively stretched, but it does not necessarily
ing participation in assessments at the seven-year follow-up did not
indicate whether there is classic spasticity or another type of in-
withdraw their consent for data collected at baseline. The Regional
creased muscle tone. According to Lance, spasticity is defined as “a
Ethical Review Board in Gothenburg, Sweden, approved this study
motor disorder characterized by a velocity-dependent increase in
(REC number: 413–04).
tonic stretch reflexes (muscle tone) with exaggerated tendon jerks,
resulting from hyperexitability of the stretch reflex, as one component of the upper motor neuron syndrome”(Lance, 1980). Thus, the
2.2 | Assessments at index stroke
reported prevalence of increased muscle tone after stroke may not
directly be translated into the prevalence of spasticity in the clas-
At index stroke, all patients were examined with brain computed
sical meaning. The distinction may be of importance when adults
tomography and/or magnetic resonance imaging. Stroke severity
with limb spasticity are considered for focal pharmacotherapy drugs
was assessed during the first week after admission to the stroke
(Simpson et al., 2016).
unit using the Scandinavian Stroke Scale (Barber, Fail, Shields,
The early identification of those who are at risk of developing
Stott, & Langhorne, 2004). Scandinavian Stroke Scale is an or-
increased muscle tone late after stroke may offer possibilities for
dinal scale that includes nine items representing consciousness;
the early treatment and prevention of negative effects on recovery.
eye movements; arm, hand and leg motor function; orientation;
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PERSSON Et al.
speech; facial palsy; and gait, and each item has 2–5 response cat-
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(muscle tone) with exaggerated tendon jerks, corresponding to the
egories. Scandinavian Stroke Scale gives a total score between 0
Tardieu scale grade 2–4 (Haugh, Pandyan, & Johnson, 2006), and
and 58. Higher scores indicate better neurological function. In all
contractures referring to a restricted range of passive joint mo-
patients, the lowest Scandinavian Stroke Scale score during the
tion The participants were asked whether they had any ongoing
first week was registered.
therapy for spasticity. Information about recurrent strokes during follow-up was obtained from the Swedish National Hospital
2.3 | Assessments seven year after index stroke
Seven years after index stroke, neurological deficits were assessed
according to the National Institute of Health Stroke Scale (NIHSS)
Discharge Registry and medical records as described (Redfors et
al., 2012).
2.4 | Statistical methods
(Brott et al., 1989), which was part of the clinical practice at that
time, instead of using the Scandinavian Stroke Scale (Barber et al.,
The data were analyzed using SAS Software version 9.4 (SAS
2004). A trained study neurologist conducted passive movements
Institute Inc). Ordinal data are presented as medians, min-max, and
of seven muscle functions in the upper extremities and legs, tak-
interquartile ranges. Seven-year NIHSS scores were converted
ing into account hyperreflexia and the velocity-dependent nature
into Scandinavian Stroke Scale scores using the 90-day algorithm:
of spasticity. Increased muscle tone was defined as a Modified
Scandinavian Stroke Scale = 56.68–2.20 × NIHSS (Gray, Ali, Lyden,
Ashworth scale score ≥2 in any of the assessed muscle groups. The
& Bath, 2009). Univariable and multivariable logistic regressions
Modified Ashworth scale is an ordinal scale with five response cat-
were performed to assess the impact of baseline variables and
egories where 0 represents hypotonic, 1 normal, 2 mild, 3 moder-
recurrent strokes on increased muscle tone seven years post-
ate, 4 severe, and 5 extreme muscle tone. During this examination,
stroke. The dependent variable was increased muscle tone (i.e., a
the neurologist also assessed both spasticity in the classical sense
Modified Ashworth scale score ≥2 in any extremity). The covari-
referring to velocity-dependent increase in tonic stretch reflexes
ates were age, sex, vascular risk factors, smoking, recurrent stroke
SAHLSIS
Consecuve consenng paents
<70 years of age presenng with
acute stroke at the Stroke Unit at
Sahlgrenska University hospital
n = 411
Died within seven years post-stroke
n = 53
Invited to parcipate in a
follow-up study seven years
post-stroke
n= 358
Declined assessments at seven year follow-up
n = 44
Lost to follow-up
n = 22
Agreed parcipaon in
assessments at seven year
follow-up
n = 292
Did not contribute muscle tone data
n=4
(Moved far away from Gothenburg n=1
Severe co-morbidies n=3:
Polycythemia vera and demena,
Reumatoid Arthris with artogenic contractures,
Severe cardiomyopathy and Diabetes Mellitus)
FIGURE 1
Study flow chart
Included in the analyses
n = 288
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during follow-up, and neurological deficits expressed by different
stroke compared with 6 (9%) among those who did not participate
items of the Scandinavian Stroke Scale at index stroke. The items
in the follow-up.
were handled as ordinal scales in the logistic regression, with odds
Tables 3 and 4 illustrate the response categories of the Modified
ratios expressing the effect for one-unit increase for each item.
Ashworth scale seven years after the index stroke. Increased muscle
The multivariable model was obtained from a stepwise forward
tone (a Modified Ashworth scale score ≥2), regardless of location, was
logistic regression that included variables significant at the 0.10
found in 99 participants (34%); of these 94 (95%) had increased muscle
level from univariable models. The goodness-of-fit for the multi-
tone in the upper extremities, and 72 (73%) in the legs. For the major-
variable logistic model was tested by the Hosmer and Lemeshow
ity, the increased muscle tone was mild or moderate in both the upper
test. Descriptively, odds ratios with 95% confidence intervals, p-
and lower extremities. Increased muscle tone was most prevalent in
values, and area under the level of statistical significance were set
the elbow flexors (upper extremities) and the knee flexors (lower ex-
at p < .05 using a 2-tailed test.
tremities). The finger flexors in the upper extremities and the plantar
flexors in the lower extremities had the highest proportion of severe
and extreme muscle tone. Of the 99 participants with increased mus-
3 | R E S U LT S
cle tone, eight reported that they had been treated with local botulinum toxin injections. One used oral baclofen, seven had orthosis, and
Of the included 411 patients, 13% had died 7 years after stroke
32 reported that they had ongoing physiotherapy. Of the 189 without
onset. Of the 358 participants who were still alive at the time of fol-
any increased muscle tone, none had botulinum toxin or baclofen, one
low-up, 292 (82%) agreed to participate. Forty-eight of the follow-
had orthosis, and three had ongoing physiotherapy.
ups were home visits. Muscle tone data were collected from 288
participants (Figure 1).
Classical spasticity (Lance, 1980), regardless of localization, was
recognized in 51 participants (18%), all of whom also had a Modified
Table 1 summarizes the baseline characteristics at index stroke
Ashworth scale score ≥2. Of these, 46 participants (90%) had spastic-
for those participating and not participating in the follow-up as-
ity in the upper extremities, 34 participants (67%) in the lower extremi-
sessments 7 years after inclusion to the study. Those declining/
ties, and 29 participants (57%) in both the upper and lower extremities.
nonresponders or lost to follow-up at 7 years poststroke were
Among those with spasticity, six participants reported that they had
slightly younger, had somewhat more severe neurological deficits
been treated with botulinum toxin, and one had received baclofen;
at acute stroke, and were more often smokers. Table 2 shows the
four had orthosis, and 19 had ongoing physiotherapy. Twenty-six par-
Scandinavian Stroke Scale subscores at index stroke for 287 of the
ticipants had contracture; among those, all but one also had increased
participants. At the follow-up 7 years after the index stroke, the
muscle tone. Of those with contracture, 21 participants had contrac-
mean and median Scandinavian Stroke Scale scores at follow-up
ture in the upper extremities, 17 in the lower limbs, and 11 in both.
were 52.0 (8.9 SD) and 56.7 (52.3–56.7 IQR), respectively. This
Table 5 shows the results of univariable and multivariable step-
corresponds to scores 2.1 (4.1 SD) and 0.0 (0.0–2.0 IQR) for the
wise logistic regression analysis for predictors of increased muscle
National Institutes of Health Stroke Scale (Gray et al., 2009). At
tone seven years poststroke. In the univariable analysis, conscious-
the follow-up, 35 participants (12%) had experienced a recurrent
ness, eye movements, arm, hand and leg motor power, orientation,
Declined to participate in
assessment at follow-up N = 66
Variable
Participants N = 288
Age (years)
Median (Min-Max) (IQR)
56.7 (18.8–69.8)
(49.8–62.0)
54.3 (18.8–69.1) (44.7–61.2)
102 (35.4)
20 (30.3)
Stroke localization
Right hemisphere, n (%)
Left hemisphere, n (%)
128 (44.4)
33 (50.0)
Brainstem, cerebellum, n (%)
51 (17.7)
10 (15.2)
More than one location, n (%)
7 (2.4)
3 (4.5)
Female Sex, n (%)
109 (37.8)
23 (34.8)
Hypertension, n (%)
157 (54.5)
32 (48.5)
Diabetes mellitus, n (%)
50 (17.4)
10 (15.2)
Current smoker, n (%)
101 (35.1)
34 (51.5)
54.0 (2.0–58.0)
(46.0–57.0)
52.0 (4.0–58.0) (34.0–56.0)
Scandinavian Stroke Scale
Median score (Min-Max) (IQR)
Abbreviations: IQR, interquartile range; SD, standard deviation.
TA B L E 1 Baseline characteristics at
index stroke
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PERSSON Et al.
TA B L E 2 Scandinavian Stroke Scale
subscores at index stroke (N = 287)
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Variable
Response category
N
(%)
Consciousness
Fully conscious
263
(91.6)
Eye movements
Somnolent, can be awakened to fully
conscious
18
(6.3)
Reacts to verbal command, not fully
conscious
5
(1.8)
Reacts to pain only
1
(0.3)
No gaze palsy
Gaze palsy present
Conjugate eye deviation
Arm, motor power
61
(21.4)
21
(7.3)
Normal strength
Gait
aphasia, facial palsy and gait were all statistically significant predic-
5
47
(1.4)
(16.5)
143
(49.8)
Reduced strength in full range
80
(27.9)
Some movement, fingertips do not
reach palm
19
(6.6)
45
(15.7)
165
(57.5)
Raises straight leg with reduced
strength
63
(22.0)
Raises leg with flexion of knee
15
(5.2)
Normal strength
Can move, but not against gravity
19
(6.6)
Paresis
25
(8.7)
Correct for time, place and person
271
4
(94.4)
(1.4)
One of these correct
3
(1.1)
Completely disoriented
9
(3.1)
225
(78.4)
Limited vocabulary or incoherent
speech
No aphasia
36
(12.5)
More than yes/no, but no longer
sentences
8
(2.8)
18
(6.3)
None/dubious
187
(65.2)
Present
100
(34.8)
Walks 5 m without aids
184
(64.1)
Only yes/no or less
Facial palsy
(2.4)
Raises hand with reduced strength
Two of these correct
Speech
7
Raises hand with flexion in elbow
Paresis
Orientation
(6.3)
(53.4)
Can move, but not against gravity
Leg, motor power
(91.3)
18
153
Raises hand with normal strength
Paresis
Hand, motor power
262
Walks with aids
18
(6.3)
Walks with help of another person
18
(6.3)
Sits without support
26
(9.0)
Bedridden wheelchair
41
(14.3)
4 | D I S CU S S I O N
tors, but there was no statistically significant association with age,
sex, hypertension, diabetes, smoking, or recurrent stroke. In the
To our knowledge, this is the first study on ischemic stroke in
multivariable analysis, higher age, arm paresis, aphasia, and facial
which the prevalence of increased muscle tone and the number of
palsy remained statistically significant predictors of increased mus-
patients meeting the classical spasticity criteria were investigated
cle tone.
several years after acute stroke. Seven years after stroke onset,
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PERSSON Et al.
TA B L E 3 Modified Ashworth scale score for upper extremities
7 years after ischemic stroke (N = 288)
TA B L E 4 Modified Ashworth scale score for lower extremities
seven years after ischemic stroke (N = 287)
Muscles
Muscle tone
N
(%)
Muscles
Muscle tone
N
(%)
Shoulder adductors,
N = 288
Normal
238
(82.6)
Normal
244
(85.0)
Mild
24
(8.3)
Hip adductors,
N = 287
Moderate
18
(6.3)
Severe
6
(2.1)
Extreme
2
(0.7)
Normal
229
(79.5)
Mild
27
(9.4)
Moderate
11
(3.8)
Moderate
20
(7.0)
Severe
4
(1.4)
Severe
9
(3.1)
Extreme
1
(0.4)
Extreme
3
(1.0)
Normal
228
(79.7)
Normal
206
(71.5)
Mild
27
(9.4)
Mild
39
(13.5)
Moderate
23
(8.1)
Moderate
22
(7.6)
Severe
15
(5.3)
Shoulder inward
rotators,
N = 288
Elbow flexors,
N = 288
Forearm pronators,
N = 288
Wrist flexors,
N = 288
Finger flexors,
N = 288
Thumb adductors,
N = 288
Extreme
6
(2.1)
Normal
228
(79.2)
Mild
23
(8.0)
Moderate
19
(6.6)
Hip flexors,
N = 287
Knee flexors,
N = 286
Knee extensors,
N = 286
Ankle flexors,
N = 286
Mild
23
(8.0)
Moderate
14
(4.9)
Severe
6
(2.1)
Normal
244
(85.0)
Mild
27
(9.4)
Severe
8
(2.8)
Normal
231
(80.8)
Mild
29
(10.1)
Moderate
20
(7.0)
Severe
6
(2.1)
Normal
226
(79.0)
Severe
15
(5.2)
Mild
23
(8.0)
Extreme
3
(1.0)
Moderate
16
(5.6)
Hypotonic
1
(0.3)
Severe
14
(4.9)
Normal
222
(77.1)
Extreme
7
(2.5)
Mild
26
(9.0)
Normal
228
(79.7)
Moderate
18
(6.3)
Mild
20
(7.0)
Severe
15
(5.2)
Moderate
15
(5.3)
Extreme
6
(2.1)
Severe
17
(5.9)
Hypotonic
1
(0.3)
Extreme
6
(2.1)
Normal
222
(77.1)
Normal
230
(80.4)
Mild
24
(8.3)
Moderate
15
(5.2)
Severe
20
(7.0)
Severe
10
(3.5)
Extreme
6
(2.1)
Extreme
5
(1.8)
Hypotonic
1
(0.3)
Normal
226
(78.5)
Mild
26
(9.0)
The observed prevalences of both increased muscle tone and
Moderate
18
(6.3)
spasticity are within the range of the previously reported prev-
Severe
11
(3.8)
Extreme
6
(2.1)
Plantar flexors,
N = 286
Toe flexors,
N = 286
Mild
23
(8.0)
Moderate
18
(6.3)
alence of increased muscle tone, as assessed by the Modified
Ashworth scale, within the first 18 months after stroke onset
(Lundstrom et al., 2008; Opheim et al., 2014; Sommerfeld et al.,
2004; Urban et al., 2010; Welmer et al., 2006). As expected and
one-third had increased muscle tone; for the majority, the muscle
in line with previous research (Picelli et al., 2014; Ryu, Lee, Lee,
tone was mildly or moderately increased. Increased muscle tone
& Chun, 2010; Urban et al., 2010), motor impairment in the early
was predicted by higher age, arm paresis, aphasia, and facial palsy
phase of stroke predicts increased muscle tone at later stages. To
at index stroke. Further, half of those with increased muscle tone
our knowledge, aphasia has not been reported as a predictor for
displayed classical spasticity, and almost one in ten participants
increased muscle tone. However, this finding is plausible because
had contractures.
such an impairment can indicate larger cortical or subcortical
damage. Our study lends further support to the literature on an
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PERSSON Et al.
TA B L E 5 Univariable and multivariable
logistic regression showing the
associations between baseline clinical
variables, including the Scandinavian
Stroke Scale (SSS) subscores at index
stroke, as well as recurrent stroke and
increased muscle tone seven years
poststroke (N = 288)
Variable
Univariable analysis
Odds ratio (95% CI)
Multivariable
analysisa
Odds ratio (95% CI)
p
Age (years)
1.02 (1.00–1.05)
.061
Male sex
1.03 (0.62–1.70)
.90
Hypertension
1.44 (0.88–2.37)
.15
Diabetes mellitus
1.34 (0.72–2.51)
.36
Smoking
0.97 (0.58–1.66)
.90
Recurrent stroke
1.97 (0.97–4.02)
.063
SSS consciousness
2.91 (1.43–5.89)
.0031
SSS eye movements
2.48 (1.29–4.75)
.0064
SSS arm motor power
2.11 (1.63–2.57)
<.0001
SSS hand motor power
2.59 (1.99–3.37)
<.0001
SSS leg motor power
2.20 (1.75–2.77)
<.0001
SSS orientation
2.10 (1.27–3.47)
.0037
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p
1.03 (1.00–1.06)
.029
1.76 (1.40–2.21)
<.0001
SSS speech
2.13 (1.53–2.97)
<.0001
1.68 (1.12–2.51)
.012
SSS facial palsy
5.07 (2.99–8.61)
<.0001
2.12 (1.10–4.07)
.024
SSS gait
1.83 (1.54–2.18)
<.0001
Note: Increased muscle tone was defined as a Modified Ashworth scale score of ≥2 in any limb. SSS
indicates Scandinavian Stroke Scale. For the Scandinavian Stroke Scale items, the odds ratio for a
one-unit increase of the score is given.
The final multivariable model was obtained from a stepwise logistic regression including variables
significant at the 0.10 level from univariable models, and it included age and the items arm motor
power, speech and facial palsy from the Scandinavian Stroke Scale. The Hosmer and Lemeshow
goodness-of-fit had a p-value of .27.
a
association between increasing age and risk for increasing muscle
within the context of some limitations. The results may not be gen-
tone. In contrast to some previous studies (Lundstrom et al., 2008;
eralized to hemorrhagic stroke or to older stroke survivors. On the
Urban et al., 2010; Watkins et al., 2002), sex did not predict the
other hand, data on long-term outcomes are of particular impor-
prevalence of increased muscle tone.
tance for younger stroke survivors, who generally have a longer life
The clear difference in the prevalence of increased muscle tone
expectancy. Although the participation rate was relatively high at
based on the Modified Ashworth scale and classical spasticity in-
the follow-up (82%), a potential selection bias exists in those who
dicates that the term spasticity, based on the Modified Ashworth
declined participation/did not respond to study invitation or were
scale data alone, may confuse researchers and clinicians. Thus, fur-
lost to follow-up had somewhat more severe strokes according to
ther research concerning different types of increased muscle tone in
the Scandinavian Stroke Scale scores at admission. Thus, if anything,
relation to different treatments and outcomes is warranted.
this bias is expected to underestimate the frequency of increased
The finding that almost one out of every ten patients had one
muscle tone. As the Modified Ashworth scale is a standard method
or more contractures is noteworthy. Our results may indicate sub-
to screen for increased muscle tone after stroke, we used this scale
optimal treatment, related to use, but also to intensity, duration,
for the analysis of association between muscle tone at follow-up and
and frequency, of interventions such as physiotherapy, surgery, and
baseline variables. However, as this scale does not take into account
pharmacological treatments. The explanations may include lack of
the angle of muscle contraction or different speeds (Patrick & Ada,
knowledge and resources, limited periods of rehabilitation, and/or
2006), it must be noted that this is an analysis of increased mus-
ambiguity regarding responsibility for the provision of care in a long-
cle tone in a broader sense and not specifically classical spasticity.
term perspective (hospital, municipality, and primary care). Thus, our
Moreover, we did not use a validated instrument for the assessment
results suggest a need for increased awareness to identify increased
of classical spasticity and contracture. However, the assessments
muscle tone both in the short- and long-term perspectives after
were made by two study neurologists specifically trained for grad-
stroke.
ing spasticity and contracture. Another study limitation is that the
The strength of the current study includes the consecutive
Scandinavian Stroke Scale was used at baseline in the acute period,
recruitment and the large and relatively young sample, the long
while the National Institutes of Health Stroke Scale was used at the
follow-up time, and that stroke neurologists evaluated classi-
follow-up. However, these instruments show good agreement, and
cal spasticity and contracture and assessed muscle tone by the
accordingly, an algorithm can be used to convert scores (Gray et
Modified Ashworth scale. However, the results must be interpreted
al., 2009). Finally, the design did not include repeated assessments
8 of 9
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PERSSON Et al.
during follow-up. Thus, we cannot draw conclusions about the time
course or effects of earlier or ongoing treatments from baseline to
follow-up.
5 | CO N C LU S I O N
One-third of patients with ischemic stroke before 70 years of age
showed increased muscle tone at seven-year follow-up. Half of them
also had classical spasticity, and almost every tenth had one or more
contractures. Increased muscle tone was predicted by age, arm paresis, aphasia, and facial palsy at index stroke.
AC K N OW L E D G M E N T S
We wish to express our gratitude to the individuals with stroke
who participated in the Sahlgrenska Academy Study on Ischaemic
Stroke. We also thank research nurse Ingrid Eriksson for her excellent work and assistance with the study patients, and Aldina Pivodic
at Statistiska Konsultgruppen for her contribution.
C O N FL I C T O F I N T E R E S T
The authors declared no potential conflicts of interest with respect
to the research, authorship, and/or publication of this article.
DATA AVA I L A B I L I T Y S TAT E M E N T
The data that support the findings of this study are available from
the corresponding author upon reasonable request.
ORCID
Carina U. Persson
Lukas Holmegaard
https://orcid.org/0000-0002-9826-9483
https://orcid.org/0000-0003-3528-0316
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How to cite this article: Persson CU, Holmegaard L, Redfors
P, Jern C, Blomstrand C, Jood K. Increased muscle tone and
contracture late after ischemic stroke. Brain Behav.
2020;10:e01509. https://doi.org/10.1002/brb3.1509