Changes in muscle architecture on ultrasound in patients early after stroke

Abstract

BACKGROUND:

Early muscle changes are believed to occur in patients with stroke. However, there are insufficient data on the changes in muscle mass and architecture of these patients.

OBJECTIVES:

This study investigates differences in ultrasound-derived muscle architecture parameters of the hemiplegic upper and lower limbs in patients with subacute stroke.

METHODS:

This is a prospective observational study, which recruited 40 adult patients who had experienced a first ever unilateral stroke (ischemic or hemorrhagic), with a duration of < 1 month post stroke. The brachialis, vastus lateralis and medial gastrocnemius on both the hemiplegic and normal side were evaluated via ultrasound. We recorded clinical variables including Motricity Index, Modified Ashworth Scale (MAS) and Functional Independence Measure (FIM)-walk.

RESULTS:

We found reduced mean muscle thickness (p < 0.001) and increased echo intensity (p < 0.001) in the brachialis muscle, increased echo intensity (p = 0.002) in the vastus lateralis muscle, and reduced muscle thickness (p < 0.001) with increased echo intensity (p < 0.001) in the medial gastrocnemius muscle compared to the normal side. There were no significant correlations between ultrasound findings and Motricity Index.

CONCLUSIONS:

We report changes in ultrasound-derived muscle architecture in the hemiplegic limbs of patients with subacute stroke, with consistent findings of decreased muscle mass and increased echo intensity.

Keywords

Ultrasonography skeletal muscle hemiplegia neurologic disorders

1 Introduction

Muscle weakness is a common cause of functional impairment after stroke, with severe weakness predicting poor recovery (Johnston et al., 1992). Initial hemiparetic muscle weakness is usually attributed to impaired cortical activation, but subsequent immobility of the affected limbs and limb spasticity are also contributory factors (Metoki et al., 2003; Ones et al., 2009). Hence, it is believed that a combination of denervation, disuse, remodeling and spasticity result in a loss of muscle mass and increased intramuscular fat deposition at 6 months or more after the stroke event (Hunnicutt et al., 2017).

These structural findings have been demonstrated in studies of patients with chronic stroke using dual-energy x-ray absorptiometry (DEXA), magnetic resonance imaging (MRI) and computed tomography (CT). These studies show decreased lean mass, decreased muscle area and increased intramuscular fat in the paretic limb compared to the nonparetic limb, most commonly in the lower limb musculature (Metoki et al., 2003). Ultrasound, a portable and cost-effective musculoskeletal imaging modality, has also been used to study muscle architecture in patients with chronic stroke. These ultrasound studies have documented changes in the paretic brachialis, quadriceps and gastrocnemius, with findings of reduced muscle thickness or increased echo intensity (Li et al., 2007; English et al., 2012; Cho et al., 2014; Akazawa et al., 2018).

Muscle weakness results in reduced lean mass, with radiological changes occurring as early as 3 weeks (Gao et al., 2009). There is also emerging evidence that muscle architecture may be associated with functional outcomes, though this has mainly been demonstrated in chronic stroke survivors (Li et al., 2007; Cho et al., 2014; Akazawa et al., 2018). Ultrasound measurements of the vastus lateralis and medial gastrocnemius, which are key muscles in locomotion, have good measurement reliability (English et al., 2012; Cho et al., 2014). Ultrasound studies have also shown that reduced muscle mass in the paretic lower limb muscles correlate with reduced impairment scores in chronic stroke (Monjo et al., 2018). Similarly, the brachialis muscle, which contributes the largest force to elbow flexion torque, has been shown to have altered muscle architectural parameters on ultrasound in the paretic arms of patients with chronic stroke (Li et al., 2007).

Although these findings have been demonstrated in chronic stroke, only a limited number of ultrasonographic studies have been performed in patients with acute or subacute stroke. These studies have focused on lower limb musculature, and report reduced quadriceps muscle thickness in patients after acute aneurysmal subarachnoid hemorrhage and stroke (Nozoe et al., 2016; Nozoe et al., 2018).

Therefore, the purpose of this study was to investigate changes in muscle mass and architecture in the affected upper and lower limbs in patients with subacute stroke through the use of ultrasound. As muscle mass has been thought to be reduced in the quadriceps muscle as early as 2 weeks after stroke (Nozoe et al., 2016), we also investigated if muscle architecture measurements in the upper and lower limbs were also affected within 2 weeks post-stroke.

2 Methods

2.1 Study design

This was a single-center observational cross-sectional study which recruited consecutive patients with stroke admitted to Tan Tock Seng Hospital Rehabilitation Centre from October 2019 to August 2020. These were all inpatients undergoing stroke rehabilitation. Tan Tock Seng Hospital Rehabilitation Centre is a tertiary-level rehabilitation facility, providing comprehensive inpatient rehabilitation services for patients who are directly transferred from acute stroke units of affiliated National Healthcare Group hospitals. Ethical approval was obtained from National Healthcare Group Domain Specific Research Board (NHG DSRB 2018/00385), and all patients or their legal representative provided written informed consent. This study conforms to all STROBE guidelines.

Inclusion criteria were: age between 21 and 80 years old, first ever clinical unilateral stroke (ischemic or hemorrhagic) confirmed on brain CT or MRI, duration of < 1 month post stroke, premorbid modified Rankin scale (mRS) score of < 2 and presence of hemiplegic weakness in both the upper and lower limbs defined as elbow flexion and knee extension strength of less than 4/5 measured by manual muscle testing on the Medical Research Council (MRC) scale.

Exclusion criteria were: a history of prior stroke or other central nervous system lesions that could result in spasticity, fixed contractures or bony deformities of the extremities and other neurological or orthopedic conditions involving the extremities.

2.2 Evaluation of muscle architectural parameters using ultrasound

The muscles chosen for evaluation were the brachialis, vastus lateralis and medial gastrocnemius on both the hemiplegic and normal side. Ultrasound images were obtained via B-mode real-time imaging (Terason t3200, Terason, Burlington, MA, USA) using a 15-4 MHz linear array transducer. The muscle architecture measurements obtained for each muscle were pennation angle, fascicle length, muscle thickness and echo intensity. Ultrasonographic evaluation was performed with patients in a supine position, with elbow joints in full extension, hip joints in neutral position, knee joints in full extension and ankle joints in a neutral position (Perkisas et al., 2018).

Ultrasonography imaging was performed at the following anatomical sites: The brachialis was measured at 1cm proximal to elbow crease on the anterior part of the upper arm (Li et al., 2007), the vastus lateralis was measured midway between the lateral condyle of femur and the greater trochanter, and the medial gastrocnemius was measured at 30% proximal between the lateral malleolus of the fibula and the lateral condyle of the tibia (Sanada et al., 2006).

On longitudinal views, the anterior pennation angle and fascicle length were measured between the humeral surface and the most clearly visualized fascicle for the brachialis (Hodges et al., 2003), and measured between the fascicle and deep aponeurosis for the vastus lateralis and medial gastrocnemius (Kubo et al., 2003). In cases where the fascicle extended outside the acquired image, the fascicle length was derived by dividing the muscle thickness by the hypotenuse of the anterior pennation angle (Kubo et al., 2003). The anterior pennation angle is believed to be increased in association with muscle hypertrophy, representing the amount of in-parallel sarcomeres, while a longer muscle fascicle is associated with faster contraction speed and larger range of motion (Blazevich et al., 2006).

Ultrasonography imaging was performed in the aforementioned anatomical positions to determine muscle thickness and echo intensity (Pillen et al., 2006). The muscle thickness was measured using the longest distance between the superficial aponeurosis and uppermost part of the bone echo of the humerus for the brachialis (Hodges et al., 2003), and the longest distance between the superficial and deep aponeurosis for the vastus lateralis and medial gastrocnemius (Caresio et al., 2015). Increased muscle thickness is associated with increased muscle mass and strength (Hunnicutt et al., 2017).

Muscle echo intensity was determined from ultrasound images using quantitative grey scale analysis (Schneider et al., 2012). A square region of interest was selected in each muscle to include as much of the muscle as possible without any bone or surrounding fascia (Caresio et al., 2015). The mean echo intensity of the region of interest was calculated, with the echo intensity of each muscle expressed as a number between 0 (black) and 255 (white) arbitrary units. Muscle echo intensity indicates muscle quality, with increased echo intensity representing increased intramuscular fibrosis and adipose tissue (Hunnicutt et al., 2017).

All ultrasonography measurements were taken using ImageJ software (National Institutes of Health, Bethesda, USA) (Schneider et al., 2012).

A single examiner with more than 10 years of experience in musculoskeletal ultrasound performed all ultrasonographic imaging.

2.3 Clinical evaluation

The following clinical variables were captured:

Motricity Index for assessment of motor impairment of the hemiplegic upper and lower limbs (Collin et al., 1990). This measures shoulder abduction, elbow flexion and pinch grip in the upper limb, and hip flexion, knee extension and ankle dorsiflexion in the lower limb. It is scored from 0 – 100 for each limb, with 100 indicating normal motor power.

Modified Ashworth Scale (MAS) for assessment of muscle spasticity. The muscle groups assessed were the elbow flexors, knee extensors, and ankle plantarflexors. The 6-point Modified Ashworth Scale (MAS) ranges from 0 (no increase in muscle tone) to 4 (rigid in flexion or extension) (Bohannon et al., 1987). For statistical purposes, a value of 1.5 for MAS was assigned to ratings of 1 + to maintain equal intervals (Mutlu et al., 2008). The tone of the elbow flexors was tested with the patient in a sitting position. The tone of the knee extensors and ankle plantarflexors were tested with the patients in the supine position.

Ambulatory status was classified using the Functional Independence Measure (FIM)-walk subscore. This is scored based on the distance travelled over 150 feet and the level of assistance or device required, with the score ranging from 1–7 (Hamilton et al., 1994).

Other data captured include patient demographics and stroke characteristics.

2.4 Statistical analysis

Descriptive statistics were utilized to illustrate patient demographics and clinical characteristics. Paired sample t-test was used to test the differences between the normal and abnormal limbs for continuous outcomes. A subgroup analysis was also performed, looking at differences in muscle architecture measurements between the paretic and normal limbs in patients recruited within 2 weeks of stroke.

Spearman coefficient was used to test the association between the upper or lower limb motricity index with the differences in the muscle architecture measurements of the hemiplegic muscles compared to the normal limb. A p value < 0.05 was considered statistically significant for a two-tailed test. Statistical analyses were generated using SPSS Version 25.0 (IBM Corp., Armonk, NY, USA).

3 Results

There were 40 patients recruited, with a mean age of 56.3±12.5 years. The majority of the patients were male (70.0%) and of Chinese ethnicity (80.0%). There were 25 (65.0%) of patients who had stroke of an ischemic etiology. The average duration after stroke to study recruitment was 17.7±6.73 days. All patients had a premorbid mRS score of 0 or 1, with a mean FIM-walk subscore of 1.6±0.871. Of the patients recruited, 37.5%, 25.0% and 42.5% of them had spasticity in the elbow flexors, knee extensors and ankle plantarflexors respectively. The mean UL motricity index and LL motricity index were 18.8±24.0 and 30.8±22.7 respectively (Table 1).

Table 1
Characteristics of the study cohort (n = 40)

Characteristics N (%) / median (25th centile-75th centile) /mean±SD

Age 56.3±12.5

Gender

Male 28 (70.0%)

Female 12 (30.0%)

Ethnicity

Chinese 32 (80.0%)

Malay 7 (17.5%)

Indian 1 (2.5%)

Premorbid mRS

0 39 (97.5%)

1 1 (2.5%)

Etiology

Ischemic 25 (62.5%)

Hemorrhagic 15 (37.5%)

Duration post stroke (days) 17.7±6.73

Side of hemiparesis (left) 26 (65.0%)

Elbow flexor spasticity on hemiparetic side

MAS 0 25 (62.5%)

MAS 1 8 (20.0%)

MAS 1+ 5 (12.5%)

MAS 2 2 (5.0%)

MAS 3 0 (0%)

Knee extensor spasticity on hemiparetic side

MAS 0 30 (75.0%)

MAS 1 5 (12.5%)

MAS 1+ 4 (10.0%)

MAS 2 0 (0%)

MAS 3 1 (2.5%)

Ankle plantarflexor spasticity on hemiparetic side

MAS 0 23 (57.5%)

MAS 1 9 (22.5%)

MAS 1+ 5 (12.5%)

MAS 2 3 (7.5%)

MAS 3 0 (0%)

Sensation on hemiparetic side

Normal 10 (25.0%)

Reduced 30 (75.0%)

Hemispatial neglect 17 (42.5%)

FIM walk subscore 1.6±0.871

Upper limb motricity index 18.7±24.0

Lower limb motricity index 30.8±22.7

Characteristics	N (%) / median (25th centile-75th centile) /mean±SD
Age	56.3±12.5
Gender
Male	28 (70.0%)
Female	12 (30.0%)
Ethnicity
Chinese	32 (80.0%)
Malay	7 (17.5%)
Indian	1 (2.5%)
Premorbid mRS
0	39 (97.5%)
1	1 (2.5%)
Etiology
Ischemic	25 (62.5%)
Hemorrhagic	15 (37.5%)
Duration post stroke (days)	17.7±6.73
Side of hemiparesis (left)	26 (65.0%)
Elbow flexor spasticity on hemiparetic side
MAS 0	25 (62.5%)
MAS 1	8 (20.0%)
MAS 1+	5 (12.5%)
MAS 2	2 (5.0%)
MAS 3	0 (0%)
Knee extensor spasticity on hemiparetic side
MAS 0	30 (75.0%)
MAS 1	5 (12.5%)
MAS 1+	4 (10.0%)
MAS 2	0 (0%)
MAS 3	1 (2.5%)
Ankle plantarflexor spasticity on hemiparetic side
MAS 0	23 (57.5%)
MAS 1	9 (22.5%)
MAS 1+	5 (12.5%)
MAS 2	3 (7.5%)
MAS 3	0 (0%)
Sensation on hemiparetic side
Normal	10 (25.0%)
Reduced	30 (75.0%)
Hemispatial neglect	17 (42.5%)
FIM walk subscore	1.6±0.871
Upper limb motricity index	18.7±24.0
Lower limb motricity index	30.8±22.7

Legend: mRS: modified Rankin Scale; MAS: Modified Ashworth Scale; FIM: Functional Independence Measure.

Table 2 displays the differences in muscle architecture measurements between the hemiparetic and normal side.

Table 2

Difference in ultrasound muscle architectural parameters between normal and hemiparetic side (n = 40)

Muscle architecture measurements	Hemiparetic side	Normal side	p value
Brachialis fascicle length (mm), mean±SD	126.6±35.4	121.0±24.9	0.299
Brachialis pennation angle (deg), mean±SD	9.82±2.95	10.6±2.50	0.108
Brachialis muscle thickness (mm), mean±SD	19.8±3.25	21.2±3.61	< 0.001
Brachialis echo intensity (AU), mean±SD	63.6±12.0	55.2±11.2	< 0.001
Vastus lateralis fascicle length (mm), mean±SD	90.0±26.4	76.4±19.8	0.002
Vastus lateralis pennation angle (deg), mean±SD	11.4±3.03	12.5±3.17	0.075
Vastus lateralis muscle thickness (mm), mean±SD	17.6±3.56	17.5±3.40	0.891
Vastus lateralis echo intensity (AU), mean±SD	53.4±11.2	49.5±12.4	0.011
Medial gastrocnemius fascicle length (mm), mean±SD	48.1±9.95	50.4±11.0	0.085
Medial gastrocnemius pennation angle (deg), mean±SD	17.1±4.29	18.2±3.57	0.035
Medial gastrocnemius muscle thickness (mm), mean±SD	14.4±2.95	15.6±2.53	< 0.001
Medial gastrocnemius echo intensity (AU), mean±SD	53.8±8.66	49.4±9.20	< 0.001

Legend: AU: Arbitrary Units.

The mean muscle thickness of the brachialis was 19.8±3.25 mm in the hemiparetic side compared to 21.2±3.61 mm on the normal side (p < 0.001). Additionally, the mean echo intensity in the hemiparetic side was 63.6±12.0 arbitrary units, which was significantly increased compared to a mean value of 55.2±11.2 arbitrary units on the normal side (p < 0.001). There were no differences in the fascicle length or pennation angle for the brachialis.

For the vastus lateralis, although the fascicle length in the hemiparetic side (90.0±26.4 mm) was longer than the normal side (76.4±19.8 mm; p = 0.002), there were no significant differences in the pennation angle or muscle thickness. However, vastus lateralis echo intensity in the hemiparetic side (53.4±11.2) was increased compared to the normal side (49.5±12.4; p = 0.011).

For the medial gastrocnemius, the pennation angle was reduced in the hemiparetic side (17.1±4.29 vs 18.2±3.57; p = 0.035). Additionally, there were reduced muscle thickness (14.4±2.95 vs 15.6±2.53; p < 0.001) and increased echo intensity (53.8±8.66 vs 49.4±9.20; p < 0.001) on the hemiparetic side compared to the normal side.

Table 3 displays the subgroup analysis of the differences in muscle architecture measurements between the hemiparetic and normal sides for patients recruited within 2 weeks of stroke. The brachialis fascicle length was increased (p = 0.015) and pennation angle was reduced (p = 0.028) compared to the normal side. The muscle thickness of the vastus lateralis and medial gastrocnemius were reduced on the hemiparetic side (p = 0.005, p = 0.036 respectively). Additionally, the echo intensity of the brachialis, vastus lateralis and medial gastrocnemius were increased on the hemiparetic side (p = 0.001; p = 0.001; p = 0.005 respectively).

Table 3

Subgroup analysis of difference in ultrasound muscle architectural parameters between the normal and hemiparetic side in patients recruited within 2 weeks of stroke (n = 16)

Muscle architecture measurements	Hemiparetic side	Normal side	p value
Brachialis fascicle length (mm), mean±SD	133.1±39.9	116.8±32.3	0.015
Brachialis pennation angle (deg), mean±SD	9.30±2.07	10.7±2.78	0.028
Brachialis muscle thickness (mm), mean±SD	19.5±3.49	20.4±3.59	0.095
Brachialis echo intensity (AU), mean±SD	65.8±9.85	57.6±10.8	0.001
Vastus lateralis fascicle length (mm), mean±SD	93.2±31.2	76.6±12.8	0.060
Vastus lateralis pennation angle (deg), mean±SD	10.6±2.89	11.7±2.18	0.188
Vastus lateralis muscle thickness (mm), mean±SD	17.0±3.33	17.7±3.38	0.005
Vastus lateralis echo intensity (AU), mean±SD	58.0±7.97	50.5±10.4	0.001
Medial gastrocnemius fascicle length (mm), mean±SD	48.4±9.66	50.5±12.4	0.314
Medial gastrocnemius pennation angle (deg), mean±SD	16.0±4.73	17.7±3.79	0.168
Medial gastrocnemius muscle thickness (mm), mean±SD	14.3±3.28	15.3±2.86	0.036
Medial gastrocnemius echo intensity (AU), mean±SD	55.1±9.79	51.3±9.65	0.005

Legend: AU: Arbitrary Units.

We did not find any significant correlations between the brachialis muscle architecture measurements and upper limb motricity index. There were also no significant correlations between the vastus lateralis or gastrocnemius with the lower limb motricity index (Table 4).

Table 4

Correlation coefficient between differences in ultrasound muscle architectural parameters of normal and hemiparetic side with motricity index (n = 40)

Differences in muscle architecture measurements	Correlation coefficient (Spearman’s rho)	p value
Upper limb motricity index
Brachialis fascicle length (mm)	0.151	0.352
Brachialis pennation angle (deg)	–0.082	0.614
Brachialis muscle thickness (mm)	–0.144	0.374
Brachialis echo intensity (AU)	0.021	0.899
Lower limb motricity index
Vastus lateralis fascicle length (mm)	0.173	0.293
Vastus lateralis pennation angle (deg)	–0.240	0.141
Vastus lateralis muscle thickness (mm)	0.232	0.154
Vastus lateralis echo intensity (AU)	0.230	0.158
Medial gastrocnemius fascicle length (mm)	–0.125	0.448
Medial gastrocnemius pennation angle (deg)	–0.042	0.801
Medial gastrocnemius muscle thickness (mm)	0.139	0.429
Medial gastrocnemius echo intensity (AU)	–0.046	0.782

Legend: AU: Arbitrary Units.

4 Discussion

Studies of muscle architecture in patients with acute and subacute stroke are under-represented compared to patients with chronic stroke. Studies using various imaging modalities including CT, MRI and DEXA in patients with chronic stroke have demonstrated reduced skeletal muscle mass, volume or cross-sectional area in paretic muscles. For example, Jorgensen et al. reported a reduction in lean muscle mass in the paretic leg on DEXA within 1 year after stroke (Jørgensen et al., 2001), while Ploutz-Snyder et al. demonstrated reduced triceps muscle cross-sectional area on MRI in the hemiplegic arm compared to the unaffected arm in chronic stroke survivors (Ploutz-Snyder et al., 2006). Our ultrasound findings of reduced muscle thickness in paretic muscles are consistent with these reports, and suggests that muscle changes start early after stroke.

Studies on ultrasound-derived muscle architectural parameters in acute stroke have mainly focused on the quadriceps. A study in patients with acute intracerebral hemorrhage or ischemic stroke found a significant reduction in the quadriceps of the paretic limb as early as 1-2 weeks after stroke (Nozoe et al., 2016). Another prospective study also reports reduced quadriceps muscle thickness within the 1st 2 weeks, albeit in a cohort of patients with aneurysmal subarachnoid hemorrhage (Nozoe et al., 2018). We therefore extend these findings by demonstrating that the muscle thickness of other muscle groups (brachialis and gastrocnemius) were similarly reduced in the early stroke period.

In patients with stroke, the finding of increased echo intensity has only been reported in the quadriceps of patients with chronic stroke (Akazawa et al., 2018). We found similar findings in not just the vastus lateralis (part of the quadriceps), but also in the brachialis and gastrocnemius in patients with subacute stroke. Increased echo intensity is believed to be reflective of reduced muscle quality (Hunnicutt et al., 2017). We also report larger differences in echo intensity between the hemiparetic and normal muscles, compared to the differences in muscle thickness. This suggests that loss of muscle thickness may be partially attenuated by connective tissue replacement or fatty infiltration. Hence, measuring echo intensity in addition to muscle thickness may be useful to assess muscle function, rather than relying on muscle thickness alone.

We also found a smaller pennation angle, reflecting muscle atrophy (Blazevich et al., 2006), in the hemiparetic gastrocnemius compared to the unaffected side. This finding has also been reported in patients with chronic stroke (Gao et al., 2009). We also found that the fascicle length was increased together with a decreased pennation angle in the hemiparetic brachialis. We are unable to account for these findings. It is possible that many of these patients had flaccid tone on the hemiparetic arm as they were examined early after stroke, which we speculate may have led to a longer fascicle length and a corresponding decrease in the pennation angle (Fukunaga et al., 1997).

We did not find a significant correlation between muscle architectural parameters and muscle MRC. This is in contrast with a cohort of patients with subacute stroke with a mean post-stroke duration of 66 days, where quadriceps muscle thickness was found to be correlated with the leg motor selectivity score in the paretic limb (Monjo et al., 2018). Additionally, a study in patients with chronic stroke with a mean post stroke duration of 53.2 months found that muscle strength was significantly associated with quadriceps thickness and echo intensity (Akazawa et al., 2018). We hypothesize that these correlations in patients with chronic stroke may not hold true during the early subacute phase of stroke. Even though early changes in ultrasound features may be present, the structural changes of muscle atrophy may not be advanced enough to be truly reflective of the degree of muscle impairment. Indeed, our findings of a muscle thickness of 17.0±3.33 mm and echo intensity of 58.0±7.97 arbitrary units of the vastus lateralis in patients who were 2 weeks or less from onset of stroke, appear to be less severe that that found in a cohort of patients with chronic stroke, which reported a mean vastus lateralis muscle thickness of 13.1±3.5 mm and an echo intensity of 70.3±12.6 arbitrary units (Monjo et al., 2018). Similarly, the differences in the pennation angle and fascicle length of the paretic brachialis, and the pennation angle and muscle thickness for the paretic gastrocnemius, when compared to the normal side, do not appear as large as that reported in patients with chronic stroke (Li et al., 2007).

4.1 Limitations

There are a few limitations in our study worth highlighting. First, we did not study changes in muscle architecture of patients with stroke in a prospective manner. Second, we were unable to independently assess the effects of spasticity (Thielman & Yourey, 2019), although it should be noted that the majority of our patients did not have significant spasticity. Third, although disease severity, deconditioning, nutritional deficiencies and inflammation have been proposed as pathological mechanisms for acute muscle atrophy, we were unable to study if these factors were correlated with changes in muscle architectural parameters. Lastly, due to the small sample size in this study, larger studies are required to verify our results.

5 Conclusion

Changes in muscle architecture in the brachialis, vastus lateralis and lateral gastrocnemius of the hemiplegic limbs are common in patients with subacute stroke, with decreased muscle mass and increased echo intensity being consistent findings in this study. These findings demonstrate that early structural muscular changes occur even during post-stroke rehabilitation. Further research is needed to elucidate the changes in muscle architecture on ultrasound with time, as well as the optimal timing of rehabilitation protocols, neuromuscular electrical stimulation (Nozoe et al., 2017) and strength-based retraining for preserving muscle metabolic integrity and function.

Conflict of interest

The authors declare no conflict of interest.

References

Akazawa,

, Harada,

, Okawa,

, Tamura,

, & Moriyama,

(2018). Muscle mass and intramuscular fat of the quadriceps are related to muscle strength in non-ambulatory chronic stroke survivors: A cross-sectional study. PloS One, 13(8), e0201789.

Blazevich,

A. J.

, Gill,

N. D.

, & Zhou,

(2006). Intra- and intermuscular variation in human quadriceps femoris architecture assessed in vivo. Journal of Anatomy, 209(3), 289–310.

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

Cho,

K. H.

, Lee,

H. J.

, & Lee,

W. H.

(2014). Reliability of rehabilitative ultrasound imaging for the medial gastrocnemius muscle in poststroke patients. Clinical Physiology and Functional Imaging, 34(1), 26–31.

Caresio,

, Molinari,

, Emanuel,

, & Minetto,

M. A.

(2015). Muscle echo intensity: reliability and conditioning factors. Clinical Physiology and Functional Imaging, 35(5), 393–403.

Collin,

, & Wade,

(1990). Assessing motor impairment after stroke: a pilot reliability study. Journal of Neurology, Neurosurgery, and Psychiatry, 53(7), 576–579.

English,

C. K.

, Thoirs,

K. A.

, Fisher,

, McLennan,

, & Bernhardt,

(2012). Ultrasound is a reliable measure of muscle thickness in acute stroke patients, for some, but not all anatomical sites: a study of the intra-rater reliability of muscle thickness measures in acute stroke patients. Ultrasound in Medicine & Biology, 38(3), 368–376.

Fukunaga,

, Ichinose,

, Ito,

, Kawakami,

, & Fukashiro,

(1997). Determination of fascicle length and pennation in a contracting human muscle in vivo. Journal of Applied Physiology (Bethesda, Md.: 1985), 82(1), 354–358.

Gao,

, Grant,

T. H.

, Roth,

E. J.

, & Zhang,

L. Q.

(2009). Changes in passive mechanical properties of the gastrocnemius muscle at the muscle fascicle and joint levels in stroke survivors. Archives of Physical Medicine and Rehabilitation, 90(5), 819–826.

10.

Hamilton,

B. B.

, Laughlin,

J. A.

, Fiedler,

R. C.

, & Granger,

C. V.

(1994). Interrater reliability of the 7-level functional independence measure (FIM). Scandinavian Journal of Rehabilitation Medicine, 26(3), 115–119.

11.

Hodges,

P. W.

, Pengel,

L. H.

, Herbert,

R. D.

, & Gandevia,

S. C.

(2003). Measurement of muscle contraction with ultrasound imaging. Muscle & Nerve, 27(6), 682–692.

12.

Hunnicutt,

J. L.

, & Gregory,

C. M.

(2017). Skeletal muscle changes following stroke: a systematic review and comparison to healthy individuals. Topics in stroke rehabilitation, 24(6), 463–471.

13.

Johnston,

Mark V.

, Kirshblum,

, Zorowitz,

, & Shiflett,

Samuel C.

(1992). Prediction of outcomes following rehabilitation of stroke patients. NeuroRehabilitation, 2(4), 72–97.

14.

Jørgensen,

, & Jacobsen,

B. K.

(2001). Changes in muscle mass, fat mass, and bone mineral content in the legs after stroke: a 1 year prospective study. Bone, 28(6), 655–659.

15.

Kubo,

, Kanehisa,

, Azuma,

, Ishizu,

, Kuno,

S. Y.

, Okada,

, & Fukunaga,

(2003). Muscle architectural characteristics in young and elderly men and women. International Journal of Sports Medicine, 24(2), 125–130.

16.

Li,

, Tong,

K. Y.

, & Hu,

(2007). The effect of poststroke impairments on brachialis muscle architecture as measured by ultrasound. Archives of Physical Medicine and Rehabilitation, 88(2), 243–250.

17.

Metoki,

, Sato,

, Satoh,

, Okumura,

, & Iwamoto,

(2003). Muscular atrophy in the hemiplegic thigh in patients after stroke. American Journal of Physical Medicine & Rehabilitation, 82(11), 862–865.

18.

Monjo,

, Fukumoto,

, Asai,

, & Shuntoh,

(2018). Muscle thickness and echo intensity of the abdominal and lower extremity muscles in stroke survivors. Journal of Clinical Neurology (Seoul, Korea), 14(4), 549–554.

19.

Mutlu,

, Livanelioglu,

, & Gunel,

M. K.

(2008). Reliability of Ashand Modified Ashworth scales in children with spastic cerebral palsy. BMC Musculoskeletal Disorders, 9, 44.

20.

Nozoe,

, Kanai,

, Kubo,

, Kitamura,

, Yamamoto,

, Furuichi,

, Takashima,

, Mase,

, & Shimada,

(2016). Changes in quadriceps muscle thickness, disease severity, nutritional status, and c-reactive protein after acute stroke. Journal of Stroke and Cerebrovascular Diseases: The Official Journal of National Stroke Association, 25(10), 2470–2474.

21.

Nozoe,

, Kanai,

, Kubo,

, Takeuchi,

, Kobayashi,

, Yamamoto,

, Furuichi,

, Yamazaki,

, Shimada,

, & Mase,

(2017). Efficacy of neuromuscular electrical stimulation for preventing quadriceps muscle wasting in patients with moderate or severe acute stroke: A pilot study. NeuroRehabilitation, 41(1), 143–149.

22.

Nozoe,

, Kanai,

, Kubo,

, Kobayashi,

, Yamamoto,

, Shimada,

, & Mase,

(2018). Quadriceps muscle thickness changes in patients with aneurysmal subarachnoid hemorrhage during the acute phase. Topics in Stroke Rehabilitation, 25(3), 209–213.

23.

Oneş,

, Yalçinkaya,

E. Y.

, Toklu,

B. C.

, & Cağlar,

(2009). Effects of age, gender, and cognitive, functional and motor status on functional outcomes of stroke rehabilitation. NeuroRehabilitation, 25(4), 241–249.

24.

Perkisas,

, Bastijns,

, Baudry,

, Bauer,

, Beaudart,

, Beckwée,

, Cruz-Jentoft,

, Gasowski,

, Hobbelen,

, Jager-Wittenaar,

, Kasiukiewicz,

, Landi,

, Małek,

, Marco,

, Martone,

A. M.

, de Miguel,

A. M.

, Piotrowicz,

, Sanchez,

, Sanchez-Rodriguez,

, Scafoglieri,

, &... De Cock,

A. M.

(2021). Application of ultrasound for muscle assessment in sarcopenia: 2020 SARCUS update. European Geriatric Medicine, 12(1), 45–59.

25.

Pillen,

, van Keimpema,

, Nievelstein,

R. A.

, Verrips,

, van Kruijsbergen-Raijmann,

, & Zwarts,

M. J.

(2006). Skeletal muscle ultrasonography: Visual versus quantitative evaluation. Ultrasound in Medicine & Biology, 32(9), 1315–1321.

26.

Ploutz-Snyder,

L. L.

, Clark,

B. C.

, Logan,

, & Turk,

(2006). Evaluation of spastic muscle in stroke survivors using magnetic resonance imaging and resistance to passive motion. Archives of Physical Medicine and Rehabilitation, 87(12), 1636–1642.

27.

Sanada,

, Kearns,

C. F.

, Midorikawa,

, & Abe,

(2006). Prediction and validation of total and regional skeletal muscle mass by ultrasound in Japanese adults. European Journal of Applied Physiology, 96(1), 24–31.

28.

Scherbakov,

, Sandek,

, & Doehner,

(2015). Stroke-related sarcopenia: specific characteristics. Journal of the American Medical Directors Association, 16(4), 272–276.

29.

Schneider,

C. A.

, Rasband,

W. S.

, & Eliceiri,

K. W.

(2012). NIH Image to ImageJ: 25 years of image analysis. Nature Methods, 9(7), 671–675.

30.

Thielman,

, & Yourey,

(2019). Ultrasound imaging of upper extremity spastic muscle post-stroke and the correlation with function: A pilot study. NeuroRehabilitation, 45(2), 213–220.