1 INTRODUCTION

After stroke, increased muscle tone and spasticity may have a negative impact on health-related quality of life (Gillard et al., 2015), motor control recovery (Singer, Nishihara, & Mochizuki, 2016), muscle architecture (Dias et al., 2016), and daily activities (Duncan et al., 1997). Increased muscle tone is also associated with fourfold higher direct costs related to hospitalization, municipality services, 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., 2018; Sommerfeld, Eek, Svensson, Holmqvist, & von Arbin, 2004; Urban et al., 2010; Watkins et al., 2002), probably because of differences in the case-mix and study design. Studies beyond the first year are scarce. At 18 months after ischemic or hemorrhagic stroke, increased muscle tone was found in 20% of 66 individuals (Welmer, von Arbin, Widen Holmqvist, & Sommerfeld, 2006). However, less is known about the extent to which increased muscle tone affects long-term stroke survivors.

Most studies investigating increased muscle tone after stroke (Lundstrom, Smits, Borg, et al., 2010; Lundstrom et al., 2008; Opheim et al., 2014; Shin et al., 2018; Sommerfeld et al., 2004; Urban et al., 2010; Watkins et al., 2002) assessed muscle tone using the Modified Ashworth scale (Bohannon & Smith, 1987; Peacock & Staudt, 1991). The Modified Ashworth scale quantifies the resistance that is felt when muscles are passively stretched, but it does not necessarily indicate whether there is classic spasticity or another type of increased muscle tone. According to Lance, spasticity is defined as “a motor disorder characterized by a velocity-dependent increase in 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 reported prevalence of increased muscle tone after stroke may not directly be translated into the prevalence of spasticity in the classical meaning. The distinction may be of importance when adults with limb spasticity are considered for focal pharmacotherapy drugs (Simpson et al., 2016).

The early identification of those who are at risk of developing increased muscle tone late after stroke may offer possibilities for the early treatment and prevention of negative effects on recovery. 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, 2010; Opheim, Danielsson, Alt Murphy, Persson, & Sunnerhagen, 2015; Urban et al., 2010). The role of age is less clear (Lundstrom et al., 2008; Shin et al., 2018). The present study aimed to investigate the long-term prevalence of increased muscle tone, classical spasticity, and contracture and to identify the predictors of increased muscle tone seven years after stroke.

2 METHODS

3 RESULTS

Of the included 411 patients, 13% had died 7 years after stroke onset. Of the 358 participants who were still alive at the time of follow-up, 292 (82%) agreed to participate. Forty-eight of the follow-ups were home visits. Muscle tone data were collected from 288 participants (Figure 1).

Table 1 summarizes the baseline characteristics at index stroke for those participating and not participating in the follow-up assessments 7 years after inclusion to the study. Those declining/nonresponders or lost to follow-up at 7 years poststroke were slightly younger, had somewhat more severe neurological deficits at acute stroke, and were more often smokers. Table 2 shows the Scandinavian Stroke Scale subscores at index stroke for 287 of the participants. At the follow-up 7 years after the index stroke, the mean and median Scandinavian Stroke Scale scores at follow-up were 52.0 (8.9 SD) and 56.7 (52.3–56.7 IQR), respectively. This corresponds to scores 2.1 (4.1 SD) and 0.0 (0.0–2.0 IQR) for the National Institutes of Health Stroke Scale (Gray et al., 2009). At the follow-up, 35 participants (12%) had experienced a recurrent stroke compared with 6 (9%) among those who did not participate in the follow-up.

Tables 3 and 4 illustrate the response categories of the Modified Ashworth scale seven years after the index stroke. Increased muscle tone (a Modified Ashworth scale score ≥2), regardless of location, was found in 99 participants (34%); of these 94 (95%) had increased muscle tone in the upper extremities, and 72 (73%) in the legs. For the majority, the increased muscle tone was mild or moderate in both the upper and lower extremities. Increased muscle tone was most prevalent in the elbow flexors (upper extremities) and the knee flexors (lower extremities). 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 muscle tone, eight reported that they had been treated with local botulinum toxin injections. One used oral baclofen, seven had orthosis, and 32 reported that they had ongoing physiotherapy. Of the 189 without any increased muscle tone, none had botulinum toxin or baclofen, one had orthosis, and three had ongoing physiotherapy.

Classical spasticity (Lance, 1980), regardless of localization, was recognized in 51 participants (18%), all of whom also had a Modified Ashworth scale score ≥2. Of these, 46 participants (90%) had spasticity in the upper extremities, 34 participants (67%) in the lower extremities, and 29 participants (57%) in both the upper and lower extremities. Among those with spasticity, six participants reported that they had been treated with botulinum toxin, and one had received baclofen; four had orthosis, and 19 had ongoing physiotherapy. Twenty-six participants had contracture; among those, all but one also had increased muscle tone. Of those with contracture, 21 participants had contracture in the upper extremities, 17 in the lower limbs, and 11 in both.

Table 5 shows the results of univariable and multivariable stepwise logistic regression analysis for predictors of increased muscle tone seven years poststroke. In the univariable analysis, consciousness, eye movements, arm, hand and leg motor power, orientation, aphasia, facial palsy and gait were all statistically significant predictors, but there was no statistically significant association with age, sex, hypertension, diabetes, smoking, or recurrent stroke. In the multivariable analysis, higher age, arm paresis, aphasia, and facial palsy remained statistically significant predictors of increased muscle tone.

4 DISCUSSION

To our knowledge, this is the first study on ischemic stroke in which the prevalence of increased muscle tone and the number of patients meeting the classical spasticity criteria were investigated several years after acute stroke. Seven years after stroke onset, one-third had increased muscle tone; for the majority, the muscle tone was mildly or moderately increased. Increased muscle tone was predicted by higher age, arm paresis, aphasia, and facial palsy at index stroke. Further, half of those with increased muscle tone displayed classical spasticity, and almost one in ten participants had contractures.

The observed prevalences of both increased muscle tone and spasticity are within the range of the previously reported prevalence 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 in line with previous research (Picelli et al., 2014; Ryu, Lee, Lee, & Chun, 2010; Urban et al., 2010), motor impairment in the early phase of stroke predicts increased muscle tone at later stages. To our knowledge, aphasia has not been reported as a predictor for increased muscle tone. However, this finding is plausible because such an impairment can indicate larger cortical or subcortical damage. Our study lends further support to the literature on an association between increasing age and risk for increasing muscle tone. In contrast to some previous studies (Lundstrom et al., 2008; Urban et al., 2010; Watkins et al., 2002), sex did not predict the prevalence of increased muscle tone.

The clear difference in the prevalence of increased muscle tone based on the Modified Ashworth scale and classical spasticity indicates that the term spasticity, based on the Modified Ashworth scale data alone, may confuse researchers and clinicians. Thus, further research concerning different types of increased muscle tone in relation to different treatments and outcomes is warranted.

The finding that almost one out of every ten patients had one or more contractures is noteworthy. Our results may indicate suboptimal treatment, related to use, but also to intensity, duration, and frequency, of interventions such as physiotherapy, surgery, and pharmacological treatments. The explanations may include lack of knowledge and resources, limited periods of rehabilitation, and/or ambiguity regarding responsibility for the provision of care in a long-term perspective (hospital, municipality, and primary care). Thus, our results suggest a need for increased awareness to identify increased muscle tone both in the short- and long-term perspectives after stroke.

The strength of the current study includes the consecutive recruitment and the large and relatively young sample, the long follow-up time, and that stroke neurologists evaluated classical spasticity and contracture and assessed muscle tone by the Modified Ashworth scale. However, the results must be interpreted within the context of some limitations. The results may not be generalized to hemorrhagic stroke or to older stroke survivors. On the other hand, data on long-term outcomes are of particular importance for younger stroke survivors, who generally have a longer life expectancy. Although the participation rate was relatively high at the follow-up (82%), a potential selection bias exists in those who declined participation/did not respond to study invitation or were lost to follow-up had somewhat more severe strokes according to the Scandinavian Stroke Scale scores at admission. Thus, if anything, this bias is expected to underestimate the frequency of increased muscle tone. As the Modified Ashworth scale is a standard method to screen for increased muscle tone after stroke, we used this scale for the analysis of association between muscle tone at follow-up and baseline variables. However, as this scale does not take into account the angle of muscle contraction or different speeds (Patrick & Ada, 2006), it must be noted that this is an analysis of increased muscle tone in a broader sense and not specifically classical spasticity. Moreover, we did not use a validated instrument for the assessment of classical spasticity and contracture. However, the assessments were made by two study neurologists specifically trained for grading spasticity and contracture. Another study limitation is that the Scandinavian Stroke Scale was used at baseline in the acute period, while the National Institutes of Health Stroke Scale was used at the follow-up. However, these instruments show good agreement, and accordingly, an algorithm can be used to convert scores (Gray et al., 2009). Finally, the design did not include repeated assessments 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 CONCLUSION

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.

CONFLICT OF INTEREST

The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.