Advertisement

Strength Training of the Nonhemiplegic Side Promotes Motor Function Recovery in Patients With Stroke: A Randomized Controlled Trial

Open AccessPublished:October 15, 2022DOI:https://doi.org/10.1016/j.apmr.2022.09.012

      Abstract

      Objective

      To observe the effect of strength training of the nonhemiplegic side (NHS) on balance function, mobility, and muscle strength of patients with stroke.

      Design

      A single-blinded (evaluator) randomized controlled trial.

      Setting

      A tertiary hospital rehabilitation center.

      Participants

      139 patients with first stroke (N=139) were recruited and randomly separated into a trial (n=69) or control group (n=70).

      Interventions

      The control group underwent usual rehabilitation training, including step training and trunk control training in standing position. The trial group underwent strength training of NHS on the basis of usual rehabilitation training. The strength training of NHS included lower limb stepping training with resisting elastic belt and upper limb pulling elastic belt training in standing position. The training for both groups was 45 min, once a day, 5 days a week for 6 weeks.

      Main Outcome Measures

      Balance evaluation was done with the Berg Balance Scale (BBS); mobility assessment with the 6-minute walk test (6-MWT); activities of daily life was examined via the modified Barthel Index (MBI); muscle strengths of the biceps brachii, iliopsoas, and quadriceps were measured via the isokinetic muscle strength testing system. All assessments were performed at baseline (T0) and after intervention (T1).

      Results

      The trial group performed better than control group in BBS scores (adjusted mean difference: 6.83; 95% confidence interval [CI]: 4.71-8.94) and 6-MWT (adjusted mean difference: 50.32; 95% CI: 40.58-60.05) after intervention. In terms of muscle strength of the hemiplegic side, the trial group displayed greater gains in biceps brachii, iliopsoas, and quadriceps than control group after intervention.

      Conclusion

      Strength training of the NHS can promote recovery of balance, mobility, and muscle strength of the paretic side of patients with stroke.

      Keywords

      List of abbreviations:

      6-MWT (6-minute walk test), ADL (activities of daily living), BBS (Berg Balance Scale), CI (confidence interval), HS (hemiplegic side), MBI (modified Barthel Index), NHS (nonhemiplegic side)
      Stroke is a common cause of disability, which induces a marked decline in activities of daily life (ADL) and social participation. Motor function recovery is a major rehabilitation target for patients with stroke. Stroke not only paralyzes the affected side but also reduces muscle strength of the contralateral side.
      • Hunnicutt JL
      • Gregory CM.
      Skeletal muscle changes following stroke: a systematic review and comparison to healthy individuals.
      • Durand MJ
      • Murphy SA
      • Schaefer KK
      • et al.
      Impaired hyperemic response to exercise post stroke.
      • Fröhlich-Zwahlen AK
      • Casartelli NC
      • Item-Glatthorn JF
      • et al.
      Validity of resting myotonometric assessment of lower extremity muscles in chronic stroke patients with limited hypertonia: a preliminary study.
      Harris et al
      • Harris ML
      • Polkey MI
      • Bath PMW
      • et al.
      Quadriceps muscle weakness following acute hemiplegic stroke.
      demonstrated that leg weakness develops on the nonhemiplegic side (NHS) in the first week after acute stroke. This decline in NHS muscle strength must not be ignored in patients with stroke, because it is highly associated with functional performance,
      • Nozoe M
      • Kanai M
      • Kubo H
      • Yamamoto M
      • Shimada S
      • Mase K.
      Non-paretic lower limb muscle wasting during acute phase is associated with dependent ambulation in patients with stroke.
      and it can be used as an independent predictor of short-term functional gain and outcomes after stroke.
      • Kim CM
      • Eng JJ.
      The relationship of lower-extremity muscle torque to locomotor performance in people with stroke.
      ,
      • Yi Y
      • Shim JS
      • Oh BM
      • et al.
      Grip strength on the unaffected side as an independent predictor of functional improvement after stroke.
      From this point of view, enhancing NHS muscle strength may be beneficial for motor functional recovery in patients with stroke. Previous studies revealed that NHS strength training improves muscle strength of the hemiplegic side (HS) in patients with stroke.
      • Green LA
      • Gabriel DA.
      The cross education of strength and skill following unilateral strength training in the upper and lower limbs.
      • Manca A
      • Dragone D
      • Dvir Z
      • et al.
      Cross-education of muscular strength following unilateral resistance training: a meta-analysis.
      • Ehrensberger M
      • Simpson D
      • Broderick P
      • et al.
      Cross-education of strength has a positive impact on post-stroke rehabilitation: a systematic literature review.
      • Yurdakul OV
      • Kilicoglu MS
      • Rezvani A
      • et al.
      How does cross-education affects muscles of paretic upper extremity in subacute stroke survivors?.
      This procedure of strength transfer, also called cross training, is generally attributed to neural adaptations.
      • Lee M
      • Carroll TJ.
      Cross education: possible mechanisms for the contralateral effects of unilateral resistance training.
      However, the aforementioned investigations primarily focused on the alteration of muscle strength. Whether this strength enhancement can translate into functional task improvement or promote motor recovery in patients with stroke is still unclear. So far, studies on the effect of NHS muscle strength training on motor function in patients with stroke is lacking. Therefore, we conducted a randomized controlled trial to observe the effect of NHS strength training on balance function, mobility, and muscle strength of patients with stroke. Our findings may be helpful in reducing stroke-related disability.

      Methods

      Participants

      Patients with first-ever stroke were recruited from the Rehabilitation Medicine Center between July and December in 2021. The inclusion criteria were as follows: (1) non-functional ambulators (Hoffer's classification: Ⅱ)
      • Hoffer MM
      • Feiwell E
      • Perry R
      • Perry J
      • Bonnett C.
      Functional ambulation in patients with myelomeningocele.
      ; (2) 45-75 years of age; (3) within 6 weeks after onset; (4) has sufficient cognitive and language abilities to complete rehabilitation treatment and assessment. The exclusion criteria were as follows: (1) has severe cardiopulmonary diseases or liver or kidney dysfunction; (2) has severe bone or joint diseases (3) co-morbid other neurologic disorders; (4) refusal to participate. This study received ethical approval from the hospital (No: 202104044K01). Signed informed consent was obtained from all participants.

      Design

      This was a single-blinded (the evaluators) randomized controlled trial. The participants were randomly separated into a trial or control group. The sample size was determined using the Berg Balance Scale (BBS), with a suggested minimal detectable change of 4.66.
      • Hiengkaew V
      • Jitaree K
      • Chaiyawat P.
      Minimal detectable changes of the Berg Balance Scale, Fugl-Meyer Assessment Scale, Timed “Up & Go” Test, gait speeds, and 2-minute walk test in individuals with chronic stroke with different degrees of ankle plantar flexor tone.
      Assuming that the standard deviation value was 9, then 116 patients were required at a 5% significance level (2-tailed) and 80% power to detect a difference of 4.66 between 2 groups. Considering a possible dropout rate of 20%, a total of 139 participants were included for analysis.

      Intervention

      The control group underwent usual rehabilitation training, including step training and trunk control training in standing position. Methods: (1) Non-hemiplegic lower limb stepping forward training repeatedly, 10-15 times as a group, 3 groups. (2) Hemiplegic lower limb stepped over an obstacle or climbed a platform repeatedly, 10-15 times as a group, 3 groups. (3) The patients stretched arms to touch distant objects repeatedly in standing position. The training time was 45 min, once a day, 5 days a week for 6 weeks. The participants were allowed to rest for 3-5 min during each training.
      In the trial group, the participants underwent strength training of NHS (fig 1) on the basis of usual rehabilitation training. Methods: (1) Non-hemiplegic lower limb stepping forward training repeatedly with resisting elastic belt (Thera-Band), 10-15 times as a group, 3 groups. (2) Non-hemiplegic upper limb pulling elastic belt repeatedly in standing position, 10-15 times as a group, 3 groups. The elastic belt (red, green, or blue) was selected according to the patient's own state, and the elastic belt should be stretched double during the training. (3) Hemiplegic lower limb stepped over an obstacle or climbed a platform repeatedly, 10-15 times as a group, 3 groups. (4) The patients stretched arms to touch distant objects repeatedly in standing position. The training time was also 45 min, once a day, 5 days a week for 6 weeks. The participants were allowed to rest for 3-5 min during each training.
      Fig 1
      Fig 1Muscle strength training of nonhemiplegic limbs.
      In addition, both groups also received ADL training for 30 min (dressing, transfers), bicycle dynamometer training for 15 min, hand function training for 30 min, and electrotherapy for 30 min. The treatments were performed daily over 5 days a week for a total of 6 weeks.

      Outcome measures

      Primary outcome

      The balance function was assessed using a 14-item BBS. Each item is a 5-point ordinal scale ranging from 0 to 4, with 0 representing complete inability to finish a task, and 4 representing the ability to finish a task. The total score can be between 0 and 56. An elevated score denotes enhanced postural control. The BBS has excellent internal consistency (Cronbach's alpha=0.92) and test-retest reliability for patients with stroke (ICC=0.98).
      • Blum L
      • Korner-Bitensky N.
      Usefulness of the Berg Balance Scale in stroke rehabilitation: a systematic review.

      Secondary outcomes

      Mobility was evaluated via the 6-minute walk test (6-MWT). Method: The participants was instructed to walk as far as possible for 6 minutes at their own speed, along a length of 30-m walking track marked by a cone at each end, which instructed to the participants to walk back.
      ADL was evaluated via the modified Barthel Index (MBI). The MBI score includes feeding, grooming, dressing, bathing, toileting, bladder and bowel continence, transfers, ambulation, and stair climbing. A total score of 0-20 points suggests total dependence in ADL; 21-60 points suggests severe dependence; 61-90 points suggests moderate dependence; 91-99 points suggests slight dependence. 100 points suggests complete independence.
      • Shah S
      • Vanclay F
      • Cooper B.
      Improving the sensitivity of the Barthel Index for stroke rehabilitation.
      The maximum muscle strength (peak torque) of the iliopsoas, quadriceps, and biceps brachii were assessed via the isokinetic muscle test (IsoMed2000, German). The isokinetic dynamometry has good reliability for maximal strength test in patients with stroke (ICC from 0.85 to 0.97 for knee and ankle).
      • Kristensen OH
      • Stenager E
      • Dalgas U.
      Muscle strength and poststroke hemiplegia: a systematic review of muscle strength assessment and muscle strength impairment.
      The entire procedure of isokinetic testing was explained to participants to achieve maximum orientation. Each action was carried out with 5 maximal contractions at 60°/s angular velocity. The test protocol was as follows: (1) Iliopsoas evaluation: The participants were in supine position. Transverse line passing through greater trochanter of femur was accepted as the motion axis for hip joint. Dynamometer effort arm was parallel to the femur, and resistance action point was fixed at the distal femur. Shoulder supports and thigh restraint adapter were employed to fix the trunk and contralateral lower limb. (2) Quadriceps evaluation: The participants remained seated, with the seat back adjusted to 70 degrees from the horizontal plane. Transverse line through the femoral condyles was regarded as the motion axis of the knee joint. Dynamometer effort arm was determined according to the crus length. Waist belt and shoulder supports were employed to provide trunk stabilization. (3) Biceps brachii evaluation: The participants remained seated, with the seat back tilted to 70 degrees from the horizontal plane. A transverse line passing through the ulnar olecranon was regarded as the motion axis for the elbow joint. Resistance action point was fixed at the distal forearm femur or palm, and a shoulder support was used to fix the contralateral shoulder joint.
      All outcome assessments were completed by a physician or physiotherapist at baseline (T0) and post-intervention (T1). The evaluators were blinded to the study aim and participants allocation.

      Statistical analysis

      SPSS 22.0 was employed for all data analyses. Descriptive statistics are presented as mean ± SD for continuous parameters and frequency for categorical parameters. Baseline inter-group differences were examined via t test for continuous data, and Chi-square tests for dichotomous variables. The Mann-Whitney test was used for inter-group comparison of non-normally distributed variables. The ANCOVA analyses were conducted to compare the primary and secondary outcomes after intervention, adjusting for baseline scores, and the magnitude of inter-group differences were calculated using η2. We also calculated the muscle strength gains of hemiplegic limbs from baseline to post-intervention (△T1-T0), the effect size were calculated via Cohen's d to assess the clinical importance of the measured changes. Significance levels were set at P<.05.

      Results

      Overall, 163 patients with stroke were screened for eligibility. Among them, 24 were excluded (18 patients with severe cardiopulmonary diseases and 6 declined participation). Ultimately, 139 patients were selected, and they were randomly separated into a trial (n=69) or control group (n=70). During the study period, 6 patients dropped out from the trial group and control group, respectively. Finally, 63 patients in trial group and 64 patients in control group were analyzed. Figure 2 shows a flow diagram of patient recruitment and retention. The baseline characteristics showed no significant differences between 2 groups (table 1). There were no associated undesirable effects either during or after treatment.
      Table 1Baseline demographics of both groups
      VariablesTrial Group n= 63Control Group n= 64P
      Age, y(64.56±7.08)(65.72±5.95)0.318
      By Student t test.
      Sex, n (%)0.802
       Men41 (65.1%)43 (67.1%)
       Women22 (34.9%)21 (32.8%)
      BMI (kg/m2)19.14±4.1618.42±4.070.326
      By Student t test.
      BMI<18.5, n (%)21 (33.33%)25 (39.06%)0.502
      NIHSS16.25±3.6915.97±3.300.647
      By Student t test.
      Course of disease (days)21.78±4.0721.50±3.600.685
      By Student t test.
      Etiology, n (%)0.767
       Ischemic40 (63.5%)39 (60.9%)
       Hemorrhage23 (36.5%)25 (39.1%)
      Paretic side, n (%)0.783
       Right28 (44.5%)30 (46.9%)
       Left35 (55.5%)34 (53.1%)
      With hypertension, n (%)43 (68.2%)47 (73.4%)0.520
      With diabetes, n (%)35 (55.5%)31 (48.4%)0.422
      With hyperlipidemia, n (%)19 (30.1%)17 (26.5%)0.653
      ADL (MBI)35.30±5.5835.84±5.930.597
      By Student t test.
      Balance function (BBS)23.37±4.9524.98±5.670.089
      By Student t test.
      6-MWT56.31±25.6760.51±21.990.354
      By Student t test.
      Muscle strength of paretic limb
       Biceps brachii5.90±4.296.36±4.060.541
      By Mann-Whitney U test; otherwise by Chi-square test.
       Iliopsoas14.56±7.8615.03±8.080.737
      By Student t test.
       Quadriceps18.08±7.6819.13±11.450.923
      By Mann-Whitney U test; otherwise by Chi-square test.
      Muscle strength of non-paretic limb
       Biceps brachii38.46±9.2737.13±11.120.464
      By Student t test.
       Iliopsoas65.70±14.6864.72±16.420.724
      By Student t test.
       Quadriceps96.16±28.1193.48±26.010.579
      By Student t test.
      Abbreviations: BMI, body mass index; NIHSS, National Institute of Health Stroke Scale.
      By Student t test.
      By Mann-Whitney U test; otherwise by Chi-square test.

      Comparison of the primary outcome measure

      Both groups exhibited significant improvement in BBS scores after intervention, with adjusted baseline values, and there was a significant mean difference of 6.83 points between the 2 groups after intervention (95% confidence interval [CI]: 4.71-8.94, P<0.001) (table 2).
      Table 2Comparison of the primary and secondary outcomes between 2 groups
      MeasuresTimeTrial Group M (SD)Control Group M (SD)Adjusted Mean Difference (95% CI)Effect Size η2P Value
      Test for heterogeneity between 2 groups using F-criteria.
      Primary outcome
      BBST023.37±4.9524.98±5.67
      T139.33±8.5634.44±8.82
      T1 (adjusted)
      Adjusted for baseline values (mean ± SE).
      40.30±0.7533.47±0.746.83 (4.71 8.94)0.24<0.001
      Secondary outcomes
      6-MWTT056.31±25.6760.51±21.99
      T1194.13±43.05149.16±41.91
      T1 (adjusted)
      Adjusted for baseline values (mean ± SE).
      196.82±3.48146.45±3.4550.32 (40.58 60.05)0.45<0.001
      MBIT035.30±5.5835.84±5.93
      T174.84±13.8171.56±14.80
      T1 (adjusted)
      Adjusted for baseline values (mean ± SE).
      75.10±1.6671.30±1.653.80 (-0.85 8.46)0.0210.108
      Abbreviations: T0, at baseline; T1, at post-intervention.
      low asterisk Test for heterogeneity between 2 groups using F-criteria.
      Adjusted for baseline values (mean ± SE).

      Comparison of secondary outcome measures

      The trial group performed better than the control group in mobility (6-MWT) after intervention (adjusted mean difference: 50.32; 95% CI: 40.58-60.05, P<0.001). No significant difference was observed in ADL between the trial and control group after intervention (adjusted mean difference: 3.80; 95% CI: -0.85 to 8.64, P=.108) (table 2).
      In terms of HS muscle strength, the trial group performed better than the control group after intervention (fig 3). The trial group displayed greater muscle strength gains in the biceps brachii (9.83±3.95 vs 6.58±4.11, P<.001), iliopsoas (19.11±9.04 vs 13.08±7.85, P<.001), and quadriceps (31.68±12.16 vs 22.80±11.57, P<.001) than control group after intervention (table 3, fig 4).
      Fig 3
      Fig 3Comparison of muscle strength of hemiplegic limbs between two groups after intervention. *P<0.05 vs control group, by Mann-Whitney U test. P<0.05 vs control group, by Student t test.
      Table 3Comparison of muscle strength of hemiplegic limbs (mean ± SD)
      MeasuresGroupT0T1ΔT1 - T0Between-Group Comparison ΔT1 - T0 t (P), ES
      Biceps brachiiTrial5.90±4.2915.73±6.98
      P<0.05 vs control group, by Mann-Whitney U test.
      9.83±3.954.53 (<0.001), 0.80
      Control6.36±4.0612.94±7.586.58±4.11
      IliopsoasTrial14.56±7.8633.67±14.80
      P<0.05 vs control group, by Student t test; ES: by Cohen's d.
      19.11±9.045.23 (<0.001), 0.71
      Control15.03±8.0828.11±12.9613.08±7.85
      QuadricepsTrial18.08±7.6849.76±18.64
      P<0.05 vs control group, by Student t test; ES: by Cohen's d.
      31.68±12.164.21 (<0.001), 0.74
      Control19.13±11.4541.92±17.5922.80±11.57
      low asterisk P<0.05 vs control group, by Mann-Whitney U test.
      P<0.05 vs control group, by Student t test; ES: by Cohen's d.
      Fig 4
      Fig 4Comparison of muscle strength gains of hemiplegic limbs between two groups after intervention. P<0.01 vs control group, by Student t test.
      In terms of NHS muscle strength, both groups revealed significant enhancements in the biceps brachii, iliopsoas, and quadriceps after intervention. However, the trial group performed significantly better than the control group after intervention (table 4).
      Table 4Comparison of muscle strength of nonhemiplegic limbs (mean ± SD)
      MeasuresGroupT0T1Mean Difference (95% CI)Intra-Group Comparison t (P)
      Biceps brachiiTrial38.46±9.2746.67±11.15
      P<0.01 vs control group, by Student t test.
      8.20 (5.51, 10.90)6.08 (<0.001)
      Control37.13±11.1240.84±10.912.71 (0.51, 6.92)2.31 (0.024)
      IliopsoasTrial65.70±14.6882.84±13.39
      P<0.01 vs control group, by Student t test.
      17.14 (13.33, 20.94)9.04 (<0.001)
      Control64.72±16.4270.77±15.786.04 (1.83, 10.25)2.87 (0.006)
      QuadricepsTrial96.16±28.11130.06±25.86
      P<0.01 vs control group, by Student t test.
      33.90 (28.31, 39.49)12.11 (<0.001)
      Control93.48±26.01106.20±24.3812.71 (7.87, 17.56)5.24 (<0.001)
      P<0.01 vs control group, by Student t test.

      Discussion

      Cross-education is a process whereby unilateral strength training is employed to enhance muscular strength of the contralateral side. More recently, emerging reports demonstrated larger contralateral gains. A recent meta-analysis estimated a 16.4% rise in contralateral lower limb strength after unilateral training.
      • Manca A
      • Dragone D
      • Dvir Z
      • et al.
      Cross-education of muscular strength following unilateral resistance training: a meta-analysis.
      This study explored the effect of strength training of NHS on motor function of patients with stroke and showed that it was effective in promoting the recovery of balance, mobility, and muscle strength of HS in patients with stroke. In terms of ADL (MBI scores), no significant difference was observed between the 2 groups after intervention.
      In current rehabilitation practice for patients with stroke, balance and mobility remain essential goals. This is because poor balance and mobility exert adverse effect on social and mental activities.
      • Grau-Pellicer M
      • Chamarro-Lusar A
      • Medina-Casanovas J
      • Serdà Ferrer BC
      Walking speed as a predictor of community mobility and quality of life after stroke.
      ,
      • van de Port I
      • Punt M
      • Meijer JW.
      Walking activity and its determinants in free-living ambulatory people in a chronic phase after stroke: a cross-sectional study.
      Sun et al
      • Sun Y
      • Ledwell NMH
      • Boyd LA
      • Zehr EP.
      Unilateral wrist extension training after stroke improves strength and neural plasticity in both arms.
      assessed the extent of cross-education after arm strength training of NHS in 24 chronic patients with stroke, the results showed that the 4 participants had clinically meaningful increases in Fugl-Meyer scores, which indicated that the NHS strength training may exert a positive effect on the global motion recovery in patients with stroke. Recent studies revealed that NHS ankle dorsiflexion exercise significantly improves the ankle dorsiflexion muscle activity on the HS, along with balance and gait abilities in chronic patients with stroke.
      • Park SC
      • Ryu JN
      • Oh SJ
      • Cha YJ.
      Cross training effects of non-paralytic dorsiflexion muscle strengthening exercise on paralytic dorsiflexor muscle activity, gait ability, and balancing ability in patients with chronic stroke: a randomized, controlled, pilot trial.
      • Park C
      • Son H
      • Yeo B.
      The effects of lower extremity cross-training on gait and balance in stroke patients: a double-blinded randomised controlled trial.
      • Jeon HJ
      • Hwang BY.
      Effect of bilateral lower limb strengthening exercise on balance and walking in hemiparetic patients after stroke: a randomized controlled trial.
      However, the aforementioned studies were experiments involving a relatively small sample size.
      In this study, the trial group exhibited better balance function (BBS scores) than control group after intervention. Given that the suggested minimal detectable change and estimated minimal clinically important difference of BBS scores were 4.66 and 5, respectively,
      • Hiengkaew V
      • Jitaree K
      • Chaiyawat P.
      Minimal detectable changes of the Berg Balance Scale, Fugl-Meyer Assessment Scale, Timed “Up & Go” Test, gait speeds, and 2-minute walk test in individuals with chronic stroke with different degrees of ankle plantar flexor tone.
      ,
      • Tamura S
      • Miyata K
      • Kobayashi S
      • Takeda R
      • Iwamoto H.
      The minimal clinically important difference in Berg Balance Scale scores among patients with early subacute stroke: a multicenter, retrospective, observational study.
      our finding of a significant mean difference of 6.83 points between 2 groups after intervention further indicated the effectiveness of NHS strength training at promoting balance function recovery in patients with stroke. In terms of mobility (6-MWT), the trial group performed better than control group after intervention, with an adjusted mean difference of 50.32, which was higher than the minimum clinical difference of 44 meters of 6-MWT in a prior study.
      • Fulk GD
      • He Y.
      Minimal clinically important difference of the 6-Minute Walk Test in people with stroke.
      This suggested that this training was also clinically significant at promoting mobility in patients with stroke.
      Previous studies confirmed that strength of hip flexor and knee extensor on the HS are closely associated with balance function and walking endurance (6-MWT) in patients with stroke.
      • Khan F
      • Chevidikunnan MF.
      Prevalence of balance impairment and factors associated with balance among patients with stroke. A cross sectional retrospective case control study.
      • Wagatsuma M
      • Kim T
      • Sitagata P
      • Lee E
      • Vrongistinos K
      • Jung T.
      The biomechanical investigation of the relationship between balance and muscular strength in people with chronic stroke: a pilot cross-sectional study.
      • Patterson SL
      • Forrester LW
      • Rodgers MM
      • et al.
      Determinants of walking function after stroke: differences by deficit severity.
      • Pang MY
      • Eng JJ
      • Dawson AS.
      Relationship between ambulatory capacity and cardiorespiratory fitness in chronic stroke: influence of stroke-specific impairments.
      • Flansbjer UB
      • Downham D
      • Lexell J.
      Knee muscle strength, gait performance, and perceived participation after stroke.
      In this study, the trial group performed significantly better than control group in strength of hip flexor, knee extensor, and elbow flexor on the HS after intervention. This proved that the NHS strength training can effectively enhance HS muscle strength in patients with stroke. We speculated that this was 1 of the reasons for the enhanced recovery of balance function and mobility in trial group. Several studies proposed the mechanisms of power transfer, including that the non-lesioned hemisphere-originating ipsilateral corticospinal projections play an important role in inter-limb associations during chronic stroke,
      • Chang SH
      • Durand-Sanchez A
      • Ditommaso C
      • et al.
      Interlimb interactions during bilateral voluntary elbow flexion tasks in chronic hemiparetic stroke.
      ,
      • Stinear CM
      • Walker KS
      • Byblow WD.
      Symmetric facilitation between motor cortices during contraction of ipsilateral hand muscles.
      unilateral strength training generally creates a “spillover” of neural drive to the untrained side, which, in turn, facilitates the adaptations of the contralateral limb.
      • Carroll TJ
      • Herbert RD
      • Munn J
      • Lee M
      • Gandevia SC.
      Contralateral effects of unilateral strength training: evidence and possible mechanisms.
      Similar studies
      • Kim CY
      • Lee JS
      • Kim HD
      • Kim JS.
      The effect of progressive task-oriented training on a supplementary tilt table on lower extremity muscle strength and gait recovery in patients with hemiplegic stroke.
      ,
      • Dragert K
      • Zehr EP.
      High-intensity unilateral dorsiflexor resistance training results in bilateral neuromuscular plasticity after stroke.
      reported that the NHS dorsiflexor strength training and task-oriented training (such as kick ball) enhanced muscle strength of contralateral lower limb, and the results also revealed a translation of strength gains toward gait velocity enhancement and motor recovery. When we compared the strength gain of the trial group in our study with the above study,
      • Kim CY
      • Lee JS
      • Kim HD
      • Kim JS.
      The effect of progressive task-oriented training on a supplementary tilt table on lower extremity muscle strength and gait recovery in patients with hemiplegic stroke.
      the knee extensor strength gain was higher, whereas, the hip flexor strength gain was similar. This difference may be related to the heterogeneity among studies (baseline scores, measurement methods, intervention method, duration, and so on).
      In addition, cardiopulmonary decline is a common complication in patients with stroke
      • Fan Q
      • Jia J.
      Translating research into clinical practice: importance of improving cardiorespiratory fitness in stroke population.
      and is intricately linked to walking endurance.
      • Chen CK
      • Huang MH
      • Liang WL
      • Lin RT
      • Juo SH.
      Early functional improvement after stroke correlates with cardiovascular fitness.
      It is reported that resistance training has a positive effect on cardiopulmonary activity in patients with stroke.
      • Lee J
      • Stone AJ.
      Combined aerobic and resistance training for cardiorespiratory fitness, muscle strength, and walking capacity after stroke: a systematic review and meta-analysis.
      ,
      • Marzetti E
      • Calvani R
      • Tosato M
      • et al.
      Physical activity and exercise as countermeasures to physical frailty and sarcopenia.
      In this study, the trial group underwent strength training of the NHS, which was beneficial to the cardiopulmonary fitness, and it may contribute to mobility recovery. With regard to ADL, no significant difference was observed between 2 groups after intervention in this study. One explanation may be that MBI has low sensitivity in assessing patients with stroke and relatively good ADL outcome. Moreover, this study targeted patients with stroke who have walking function at baseline. If targeting patients with stroke who were unable to walk, different findings may be obtained with respect to MBI.

      Limitations

      This study was associated with several limitations. Firstly, we did not assess the spasticity of hemiplegic limbs, although no record of drug usage or botulinum toxin administration was found to reduce spasticity in the trial group. However, spasticity still requires further evaluation. Secondly, we only observed differences between 2 groups after intervention. Hence, further studies are required to elucidate its long-term rehabilitation efficacy.

      Conclusion

      The present study demonstrated that NHS strength training can promote the recovery of balance, mobility, and HS muscle strength in patients with stroke. Therefore, we recommend NHS strength training as a potential rehabilitation treatment item for patients with stroke, even though it is opposite to the forced usage paradigm that is characteristic of most stroke rehabilitation procedures.

      References

        • Hunnicutt JL
        • Gregory CM.
        Skeletal muscle changes following stroke: a systematic review and comparison to healthy individuals.
        Top Stroke Rehabil. 2017; 24: 463-471
        • Durand MJ
        • Murphy SA
        • Schaefer KK
        • et al.
        Impaired hyperemic response to exercise post stroke.
        PLoS One. 2015; 10e0144023
        • Fröhlich-Zwahlen AK
        • Casartelli NC
        • Item-Glatthorn JF
        • et al.
        Validity of resting myotonometric assessment of lower extremity muscles in chronic stroke patients with limited hypertonia: a preliminary study.
        J Electromyogr Kinesiol. 2014; 24: 762-769
        • Harris ML
        • Polkey MI
        • Bath PMW
        • et al.
        Quadriceps muscle weakness following acute hemiplegic stroke.
        Clin Rehabil. 2001; 15: 274-281
        • Nozoe M
        • Kanai M
        • Kubo H
        • Yamamoto M
        • Shimada S
        • Mase K.
        Non-paretic lower limb muscle wasting during acute phase is associated with dependent ambulation in patients with stroke.
        J Clin Neurosci. 2020; 74: 141-145
        • Kim CM
        • Eng JJ.
        The relationship of lower-extremity muscle torque to locomotor performance in people with stroke.
        Phys Ther. 2003; 83: 49-57
        • Yi Y
        • Shim JS
        • Oh BM
        • et al.
        Grip strength on the unaffected side as an independent predictor of functional improvement after stroke.
        Am J Phys Med Rehabil. 2017; 96: 616-620
        • Green LA
        • Gabriel DA.
        The cross education of strength and skill following unilateral strength training in the upper and lower limbs.
        J Neurophysiol. 2018; 120: 468-479
        • Manca A
        • Dragone D
        • Dvir Z
        • et al.
        Cross-education of muscular strength following unilateral resistance training: a meta-analysis.
        Eur J Appl Physiol. 2017; 117: 2335-2354
        • Ehrensberger M
        • Simpson D
        • Broderick P
        • et al.
        Cross-education of strength has a positive impact on post-stroke rehabilitation: a systematic literature review.
        Top Stroke Rehabil. 2016; 23: 126-135
        • Yurdakul OV
        • Kilicoglu MS
        • Rezvani A
        • et al.
        How does cross-education affects muscles of paretic upper extremity in subacute stroke survivors?.
        Neurol Sci. 2020; 41: 3667-3675
        • Lee M
        • Carroll TJ.
        Cross education: possible mechanisms for the contralateral effects of unilateral resistance training.
        Sports Med. 2007; 37: 1-14
        • Hoffer MM
        • Feiwell E
        • Perry R
        • Perry J
        • Bonnett C.
        Functional ambulation in patients with myelomeningocele.
        J Bone Joint Surg Am. 1973; 55: 137-148
        • Hiengkaew V
        • Jitaree K
        • Chaiyawat P.
        Minimal detectable changes of the Berg Balance Scale, Fugl-Meyer Assessment Scale, Timed “Up & Go” Test, gait speeds, and 2-minute walk test in individuals with chronic stroke with different degrees of ankle plantar flexor tone.
        Arch Phys Med Rehabil. 2012; 93: 1201-1208
        • Blum L
        • Korner-Bitensky N.
        Usefulness of the Berg Balance Scale in stroke rehabilitation: a systematic review.
        Phys Ther. 2008; 88: 559-566
        • Shah S
        • Vanclay F
        • Cooper B.
        Improving the sensitivity of the Barthel Index for stroke rehabilitation.
        J Clin Epidemiol. 1989; 42: 703-709
        • Kristensen OH
        • Stenager E
        • Dalgas U.
        Muscle strength and poststroke hemiplegia: a systematic review of muscle strength assessment and muscle strength impairment.
        Arch Phys Med Rehabil. 2017; 98: 368-380
        • Grau-Pellicer M
        • Chamarro-Lusar A
        • Medina-Casanovas J
        • Serdà Ferrer BC
        Walking speed as a predictor of community mobility and quality of life after stroke.
        Top Stroke Rehabil. 2019; 26: 349-358
        • van de Port I
        • Punt M
        • Meijer JW.
        Walking activity and its determinants in free-living ambulatory people in a chronic phase after stroke: a cross-sectional study.
        Disabil Rehabil. 2020; 42: 636-641
        • Sun Y
        • Ledwell NMH
        • Boyd LA
        • Zehr EP.
        Unilateral wrist extension training after stroke improves strength and neural plasticity in both arms.
        Exp Brain Res. 2018; 236: 2009-2021
        • Park SC
        • Ryu JN
        • Oh SJ
        • Cha YJ.
        Cross training effects of non-paralytic dorsiflexion muscle strengthening exercise on paralytic dorsiflexor muscle activity, gait ability, and balancing ability in patients with chronic stroke: a randomized, controlled, pilot trial.
        J Musculoskelet Neuronal Interact. 2021; 21: 51-58
        • Park C
        • Son H
        • Yeo B.
        The effects of lower extremity cross-training on gait and balance in stroke patients: a double-blinded randomised controlled trial.
        Eur J Phys Rehabil Med. 2021; 57: 4-12
        • Jeon HJ
        • Hwang BY.
        Effect of bilateral lower limb strengthening exercise on balance and walking in hemiparetic patients after stroke: a randomized controlled trial.
        J Phys Ther Sci. 2018; 30: 277-281
        • Tamura S
        • Miyata K
        • Kobayashi S
        • Takeda R
        • Iwamoto H.
        The minimal clinically important difference in Berg Balance Scale scores among patients with early subacute stroke: a multicenter, retrospective, observational study.
        Top Stroke Rehabil. 2022; 29: 423-429
        • Fulk GD
        • He Y.
        Minimal clinically important difference of the 6-Minute Walk Test in people with stroke.
        J Neurol Phys Ther. 2018; 42: 235-240
        • Khan F
        • Chevidikunnan MF.
        Prevalence of balance impairment and factors associated with balance among patients with stroke. A cross sectional retrospective case control study.
        Healthcare (Basel). 2021; 9: 320
        • Wagatsuma M
        • Kim T
        • Sitagata P
        • Lee E
        • Vrongistinos K
        • Jung T.
        The biomechanical investigation of the relationship between balance and muscular strength in people with chronic stroke: a pilot cross-sectional study.
        Top Stroke Rehabil. 2019; 26: 173-179
        • Patterson SL
        • Forrester LW
        • Rodgers MM
        • et al.
        Determinants of walking function after stroke: differences by deficit severity.
        Arch Phys Med Rehabil. 2007; 88: 115-119
        • Pang MY
        • Eng JJ
        • Dawson AS.
        Relationship between ambulatory capacity and cardiorespiratory fitness in chronic stroke: influence of stroke-specific impairments.
        Chest. 2005; 127: 495-501
        • Flansbjer UB
        • Downham D
        • Lexell J.
        Knee muscle strength, gait performance, and perceived participation after stroke.
        Arch Phys Med Rehabil. 2006; 87: 974-980
        • Chang SH
        • Durand-Sanchez A
        • Ditommaso C
        • et al.
        Interlimb interactions during bilateral voluntary elbow flexion tasks in chronic hemiparetic stroke.
        Physiol Rep. 2013; 1: e00010
        • Stinear CM
        • Walker KS
        • Byblow WD.
        Symmetric facilitation between motor cortices during contraction of ipsilateral hand muscles.
        Exp Brain Res. 2001; 139: 101-105
        • Carroll TJ
        • Herbert RD
        • Munn J
        • Lee M
        • Gandevia SC.
        Contralateral effects of unilateral strength training: evidence and possible mechanisms.
        J Appl Physiol (1985). 2006; 101: 1514-1522
        • Kim CY
        • Lee JS
        • Kim HD
        • Kim JS.
        The effect of progressive task-oriented training on a supplementary tilt table on lower extremity muscle strength and gait recovery in patients with hemiplegic stroke.
        Gait Posture. 2015; 41: 425-430
        • Dragert K
        • Zehr EP.
        High-intensity unilateral dorsiflexor resistance training results in bilateral neuromuscular plasticity after stroke.
        Exp Brain Res. 2013; 225: 93-104
        • Fan Q
        • Jia J.
        Translating research into clinical practice: importance of improving cardiorespiratory fitness in stroke population.
        Stroke. 2020; 51: 361-367
        • Chen CK
        • Huang MH
        • Liang WL
        • Lin RT
        • Juo SH.
        Early functional improvement after stroke correlates with cardiovascular fitness.
        Kaohsiung J Med Sci. 2018; 34: 643-649
        • Lee J
        • Stone AJ.
        Combined aerobic and resistance training for cardiorespiratory fitness, muscle strength, and walking capacity after stroke: a systematic review and meta-analysis.
        J Stroke Cerebrovasc Dis. 2020; 29104498
        • Marzetti E
        • Calvani R
        • Tosato M
        • et al.
        Physical activity and exercise as countermeasures to physical frailty and sarcopenia.
        Aging Clin Exp Res. 2017; 29: 35-42