Nothing Special   »   [go: up one dir, main page]

Academia.eduAcademia.edu
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 | 1 of 9 2 of 9 | PERSSON Et al. 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; | PERSSON Et al. speech; facial palsy; and gait, and each item has 2–5 response cat- 3 of 9 (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 4 of 9 | PERSSON Et al. 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 | PERSSON Et al. TA B L E 2 Scandinavian Stroke Scale subscores at index stroke (N = 287) 5 of 9 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, 6 of 9 | 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 | 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 7 of 9 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 | 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 REFERENCES Barber, M., Fail, M., Shields, M., Stott, D. J., & Langhorne, P. (2004). Validity and reliability of estimating the Scandinavian stroke scale score from medical records. Cerebrovascular Disease, 17(2–3), 224– 227. https://doi.org/10.1159/000075795 Bohannon, R. W., & Smith, M. B. (1987). Interrater reliability of a modified Ashworth scale of muscle spasticity. Physical Therapy, 67(2), 206–207. https://doi.org/10.1093/ptj/67.2.206 Brott, T., Adams, H. P., Olinger, C. P., Marler, J. R., Barsan, W. G., Biller, J., … Hertzberg, V. (1989). Measurements of acute cerebral infarction: A clinical examination scale. Stroke, 20(7), 864–870. https://doi. org/10.1161/01.STR.20.7.864 Dias, C. P., Freire, B., Goulart, N. B. A., Onzi, E. S., Becker, J., Gomes, I., … Vaz, M. A. (2016). Muscle architecture and torque production in stroke survivors: An observational study. Topics in Stroke Rehabilitation, 24(3), 206–213. https://doi.org/10.1080/10749357.2016.1210873 Duncan, P. W., Samsa, G. P., Weinberger, M., Goldstein, L. B., Bonito, A., Witter, D. M., … Matchar, D. (1997). Health status of individuals with mild stroke. Stroke, 28(4), 740–745. https://doi.org/10.1161/01. STR.28.4.740 Gillard, P. J., Sucharew, H., Kleindorfer, D., Belagaje, S., Varon, S., Alwell, K., … Kissela, B. (2015). The negative impact of spasticity on the health-related quality of life of stroke survivors: A longitudinal cohort study. Health and Quality of Life Outcomes, 13, 159. https://doi. org/10.1186/s12955-015-0340-3 Gray, L. J., Ali, M., Lyden, P. D., & Bath, P. M. (2009). Interconversion of the national institutes of health stroke scale and Scandinavian stroke scale in acute stroke. Journal of Stroke and Cerebrovascular Diseases, 18(6), 466–468. https://doi.org/10.1016/j.jstrokecerebrov asdis.2009.02.003 Haugh, A. B., Pandyan, A. D., & Johnson, G. R. (2006). A systematic review of the Tardieu Scale for the measurement of spasticity. Disability and Rehabilitation, 28(15), 899–907. https://doi.org/10.1080/09638 28050 0404305 Jood, K., Ladenvall, C., Rosengren, A., Blomstrand, C., & Jern, C. (2005). Family history in ischemic stroke before 70 years of age: The Sahlgrenska Academy Study on Ischemic Stroke. Stroke, 36(7), 1383–1387. https://doi.org/10.1161/01.str.00001 69944.46025.09 Lance, J. W. (1980). The control of muscle tone, reflexes, and movement: Robert Wartenberg Lecture. Neurology, 30(12), 1303–1313. Lundstrom, E., Smits, A., Borg, J., & Terent, A. (2010). Four-fold increase in direct costs of stroke survivors with spasticity compared with stroke survivors without spasticity: The first year after the event. Stroke, 41(2), 319–324. https://doi.org/10.1161/strok eaha.109.558619 Lundstrom, E., Smits, A., Terent, A., & Borg, J. (2010). Time-course and determinants of spasticity during the first six months following firstever stroke. Journal of Rehabilitation Medicine, 42(4), 296–301. https ://doi.org/10.2340/16501977-0509 Lundstrom, E., Terent, A., & Borg, J. (2008). Prevalence of disabling spasticity 1 year after first-ever stroke. European Journal of Neurology, 15(6), 533–539. https://doi. org/10.1111/j.1468-1331.2008.02114.x Opheim, A., Danielsson, A., Alt Murphy, M., Persson, H. C., & Sunnerhagen, K. S. (2014). Upper-limb spasticity during the first year after stroke: Stroke arm longitudinal study at the University of Gothenburg. American Journal of Physical Medicine & Rehabilitation, 93(10), 884–896. https://doi.org/10.1097/phm.00000 00000 000157 Opheim, A., Danielsson, A., Alt Murphy, M., Persson, H. C., & Sunnerhagen, K. S. (2015). Early prediction of long-term upper limb spasticity after stroke: Part of the SALGOT study. Neurology, 85(10), 873–880. https:// doi.org/10.1212/wnl.0000000000001908 Patrick, E., & Ada, L. (2006). The Tardieu Scale differentiates contracture from spasticity whereas the Ashworth Scale is confounded by it. Clinical Rehabilitation, 20(2), 173–182. https://doi.org/10.1191/02692 15506cr922oa Peacock, W. J., & Staudt, L. A. (1991). Functional outcomes following selective posterior rhizotomy in children with cerebral palsy. Journal of Neurosurgery, 74(3), 380–385. https://doi.org/10.3171/ jns.1991.74.3.0380 Picelli, A., Tamburin, S., Dambruoso, F., Midiri, A., Girardi, P., Santamato, A., … Smania, N. (2014). Topical distribution of initial paresis of the limbs to predict clinically relevant spasticity after ischemic stroke: A retrospective cohort study. European Journal of Physical and Rehabilitation Medicine, 50(5), 489–494. Redfors, P., Jood, K., Holmegaard, L., Rosengren, A., Blomstrand, C., & Jern, C. (2012). Stroke subtype predicts outcome in young and middle-aged stroke sufferers. Acta Neurologica Scandinavica, 126(5), 329–335. https://doi.org/10.1111/j.1600-0404.2012.01653.x Ryu, J. S., Lee, J. W., Lee, S. I., & Chun, M. H. (2010). Factors predictive of spasticity and their effects on motor recovery and functional outcomes in stroke patients. Topics in Stroke Rehabilitation, 17(5), 380– 388. https://doi.org/10.1310/tsr1705-380 Shin, Y.-I., Kim, S.-Y., Lee, H. I., Kim, D. Y., Lee, J., Sohn, M. K., … Kim, Y.-H. (2018). Association between spasticity and functional impairments during the first year after stroke in Korea: The KOSCO study. American Journal of Physical Medicine & Rehabilitation, 97(8), 557–564. https://doi.org/10.1097/PHM.00000 00000 000916 | PERSSON Et al. Simpson, D. M., Hallett, M., Ashman, E. J., Comella, C. L., Green, M. W., Gronseth, G. S., … Yablon, S. A. (2016). Practice guideline update summary: Botulinum neurotoxin for the treatment of blepharospasm, cervical dystonia, adult spasticity, and headache: Report of the Guideline Development Subcommittee of the American Academy of Neurology. Neurology, 86(19), 1818–1826. https://doi.org/10.1212/ wnl.00000 00000 002560 Singer, J. C., Nishihara, K., & Mochizuki, G. (2016). Does poststroke lower-limb spasticity influence the recovery of standing balance control? A 2-year multilevel growth model. Neurorehabilitation and Neural Repair, 30(7), 626–634. https://doi.org/10.1177/1545968315 613862 Sommerfeld, D. K., Eek, E. U., Svensson, A. K., Holmqvist, L. W., & von Arbin, M. H. (2004). Spasticity after stroke: Its occurrence and association with motor impairments and activity limitations. Stroke, 35(1), 134–139. https://doi.org/10.1161/01.str.0000105386.05173.5e Urban, P. P., Wolf, T., Uebele, M., Marx, J. J., Vogt, T., Stoeter, P., … Wissel, Jörg (2010). Occurence and clinical predictors of spasticity after 9 of 9 ischemic stroke. Stroke, 41(9), 2016–2020. https://doi.org/10.1161/ strokeaha.110.581991 Watkins, C. L., Leathley, M. J., Gregson, J. M., Moore, A. P., Smith, T. L., & Sharma, A. K. (2002). Prevalence of spasticity post stroke. Clinical Rehabilitation, 16(5), 515–522. https://doi.org/10.1191/0269215502 cr512oa Welmer, A. K., von Arbin, M., Widen Holmqvist, L., & Sommerfeld, D. K. (2006). Spasticity and its association with functioning and health-related quality of life 18 months after stroke. Cerebrovascular Disease, 21(4), 247–253. https://doi.org/10.1159/000091222 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