Chronic Stroke Patients Show Early and Robust Improvements in Muscle and Functional Performance in Response To..

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Chronic stroke patients show early and robust


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performance in response to...

Article in Journal of NeuroEngineering and Rehabilitation · October 2014


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Fernandez-Gonzalo et al. Journal of NeuroEngineering and Rehabilitation 2014, 11:150
http://www.jneuroengrehab.com/content/11/1/150 JNER JOURNAL OF NEUROENGINEERING
AND REHABILITATION

RESEARCH Open Access

Chronic stroke patients show early and robust


improvements in muscle and functional
performance in response to eccentric-overload
flywheel resistance training: a pilot study
Rodrigo Fernandez-Gonzalo1*, Catarina Nissemark2, Birgitta Åslund2, Per A Tesch1 and Peter Sojka2,3

Abstract
Background: Resistance exercise comprising eccentric (ECC) muscle actions enhances muscle strength and
function to aid stroke patients in conducting daily tasks. The purpose of this study was to assess the efficacy of a
novel ECC-overload flywheel resistance exercise paradigm to induce muscle and functional performance adaptations
in chronic stroke patients.
Methods: Twelve patients (~8 years after stroke onset) performed 4 sets of 7 coupled concentric (CON) and ECC actions
using the affected limb on a flywheel leg press (LP) device twice weekly for 8 weeks. Maximal CON and ECC isokinetic
torque at 30, 60 and 90°/s, isometric knee extension and LP force, and CON and ECC peak power in LP were measured
before and after training. Balance (Berg Balance Scale, BBS), gait (6-Min Walk test, 6MWT; Timed-Up-and-Go, TUG),
functional performance (30-s Chair-Stand Test, 30CST), spasticity (Modified Ashworth Scale) and perceived participation
(Stroke Impact Scale, SIS) were also determined.
Results: CON and ECC peak power increased in both the trained affected (34 and 44%; P < 0.01), and the untrained,
non-affected leg (25 and 34%; P < 0.02). Power gains were greater (P = 0.008) for ECC than CON actions. ECC isokinetic
torque at 60 and 90°/s increased in the affected leg (P < 0.04). The increase in isometric LP force for the trained, affected
leg across tests ranged 10-20% (P < 0.05). BBS (P = 0.004), TUG (P = 0.018), 30CST (P = 0.024) and SIS (P = 0.058) scores
improved after training. 6MWT and spasticity remained unchanged.
Conclusions: This novel, short-term ECC-overload flywheel RE training regime emerges as a valid, safe and viable
method to improve muscle function, balance, gait and functional performance in men and women suffering from
chronic stroke.
Keywords: Balance, Bilateral asymmetry, Muscle strength, Neuro-rehabilitation

Background target for stroke rehabilitation [9]. Indeed, RE training,


Stroke is a leading cause for long-term disability [1] that challenging the more conservative approach of cau-
often compromises muscle strength, power, balance and tiousness, employing high-intensity muscle actions, has
gait [2-5] frequently accompanied by spasticity [6,7]. To proven efficacy to ameliorate vital physical functions in
overcome adverse neuromuscular changes and associ- stroke patients [10,11] without exacerbating spasticity
ated impairments consequent to stroke, various exercise [12,13]. More importantly, improvements in neuromus-
intervention strategies have been implemented [8]. More cular function achieved through RE training interven-
recently, resistance exercise (RE) has become a primary tions appear to be carried over to long lasting benefits
aiding patients in daily physical tasks [14].
* Correspondence: [email protected]
For unknown reason(s) stroke patients show greater
1
Department of Physiology & Pharmacology, Karolinska Institutet, 171 77 discrepancy in shortening (concentric; CON) relative to
Stockholm, Sweden lengthening (eccentric; ECC) maximal voluntary force
Full list of author information is available at the end of the article

© 2014 Fernandez-Gonzalo et al.; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of
the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use,
distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public
Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this
article, unless otherwise stated.
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compared with healthy individuals [3,4,15]. As skeletal


muscle inherently produces much less force in CON
than ECC actions [16], traditional RE regimes executed
by lifting and lowering weights or weight stacks, offer
modest and insufficient stimulus providing the goal is
maximizing neural drive and muscle activity. In support,
stroke patients subjected to isokinetic RE, showed more
robust neural adaptations following ECC than CON
mode training [17], potentially translated into the more
substantial benefits evident in functional daily activities
[18]. Additionally, ECC training using the affected limb
only, may elicit cross-transfer adaptations such that
muscle strength and power of the non-affected limb in-
crease as well [17]. Nevertheless, CON muscle actions
should be incorporated in any rehabilitation program
prescribed to stroke patients as they are equally import-
ant in daily tasks, e.g., rising from a chair or lifting a
shopping bag, and obviously orchestrating with ECC ac-
tions in most activities of locomotion of coupled CON
and ECC actions involving the stretch-shortening cycle.
In contrast to weight training employing constant ex-
ternal load, iso-inertial exercise [19] offers coupled CON
and ECC actions, and maximal voluntary resistance
through the full range of motion during CON actions, Figure 1 Cartoon showing the flywheel leg press resistance
exercise device for stroke patients.
and if desired, brief episodes of ECC overload [19,20].
This method, using inertial resistance provided by rotat-
ing flywheel(s) set in motion by the trainee, has shown force, and CON and ECC peak power during flywheel
efficacy in counteracting deleterious disuse effects pro- LP exercise) were assessed before, and after the training
ducing muscle atrophy and dysfunction [21,22]. Like- period. Time of the day was replicated (±2 h) from pre
wise, healthy individuals subjected to ECC-overload to post training tests. Prior to any test, patients had
flywheel RE training experienced more profound in- completed 3 familiarization sessions on the LP flywheel
creases in force and power via increased neural activation, device.
than subjects performing conventional RE training [23,24].
Given the unique features, ECC-overload flywheel RE Participants
emerges as an attractive approach to be offered to stroke Subjects were community dwelling and had been treated
patients. at the Östersunds Rehabcenter (Östersund Hospital,
The current study investigated the efficacy of an ECC- Östersund, Sweden). Inclusion criteria were (a) a history
overload flywheel RE training challenge to enhance of stroke (>2 years post stroke) with unilateral motor
muscle strength and power in patients suffering from deficits affecting gait pattern and/or speed, (b) independ-
chronic stroke. We hypothesized the 8-week unilateral ent walking ability with or without walking aid at least
training intervention, using the affected lower limb, 10 m, (c) to have completed standard rehabilitation, yet
would increase force and power of both limbs, and these not to be involved in any structured rehabilitation program
effects to be accompanied by improvements in balance for the last 6 month prior to the study and, (d) ability to
and daily task functional performance, without provok- perform closed-chain exercise using the prescribed LP
ing increased spasticity. training device. Significant psychiatric or cognitive deficits,
major cardiorespiratory diseases (treated and controlled
Methods arterial hypertension were not considered exclusion
General design criterion), chronic pain or joint affection were exclusion
Twelve chronic stroke patients with gait deficits per- criteria factors. After a preliminary selection using hos-
formed unilateral flywheel leg press (LP) RE (Figure 1) pital records, candidate participants were familiarized
using the affected limb twice weekly for 8 weeks. Bal- with training and test procedures, and examined by a
ance, gait, functional performance, and muscle function physiotherapist and a rehabilitation medicine consultant.
(i.e. maximal CON and ECC isokinetic torque at 30, 60 Possible risks and discomforts associated with the study
and 90°/s, maximal knee extension and LP isometric protocols were explained and written informed consent
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was obtained. In particular, our pre-study assessments subsequent sessions. A standardized warm-up comprised
revealed a clear-cut risk for muscle strains and joint three submaximal unilateral isometric actions at 90° knee
(mainly knee and hip) injury as the affected leg exhibited flexion. Beginning with the non-affected leg, three max-
diminished joint stiffness and stability while performing imal isometric actions, each sustained for 5 s, were exe-
unrestricted force through the entire range of motion cuted 1 min apart. Peak torque (Nm) averaged over a 1-s
and brief eccentric overload. Thus, a custom made device window was chosen for data analysis. After 2 min recov-
offered lateral leg support avoiding involuntary abduction ery, unilateral CON and ECC isokinetic torque was
of the affected limb such that the limb was stabilized assessed at 30, 60 and 90°/s, respectively. One min was
and ankle, knee and hip joints positioned in the same allowed between different speed settings, and 2 min be-
vertical plane during leg flexion/extension. Subjects were tween CON and ECC actions. Three submaximal actions
instructed not to perform any additional strenuous lower- preceded each maximal attempt. The highest peak torque
limb activity during the intervention. The study protocol for each muscle action and speed mode was chosen for
was approved by the Regional Ethical Review Board in further analysis.
Umeå (No. 09-190aM; 2009-1394-31).
Peak power
Balance, gait, functional performance, spasticity and Peak power was assessed ~6 days before and ~5 days
perceived participation after the intervention. Patients completed 2 sets of 7
Tests were performed ~12 days before and after the train- maximal CON-ECC unilateral actions for either limb
ing period by an independent physiotherapist blinded to using a flywheel leg press (YoYo® Technology AB,
the intervention and purpose of the study. The Berg Stockholm, Sweden; Figure 1) device with a lateral leg
Balance Scale (BBS; [25]) assessed balance. This test support to avoid involuntary abduction of the affected
includes 14 different items to determine dynamic and limb during exercise. This apparatus provides unlimited
static balance. Gait performance was assessed by the resistance during coupled CON and ECC actions using
Timed-Up-and-Go (TUG; [26]) and the 6-Minute Walk the inertia of a spinning flywheel (0.036 kg · m-2) set in
tests (6MWT; [27]). In the TUG test, patients were rotation by the trainee. Following initiation of flywheel
instructed to rise from a chair, walk at a fast, still comfort- momentum using modest effort, 7 consecutive repeti-
able speed 3 m, turn around, walk back and sit down in tions were performed with maximal effort, accelerating
the chair. Time to the nearest second was recorded in rotation and hence speed of the wheel during CON, and
three trials, and the best value was used for data analysis. produce deceleration in the subsequent ECC action. Pa-
The 6MWT consisted of walking 6 min at a self-selected tients were instructed to push with maximal effort
speed. The distance was recorded to the nearest meter. through the entire range of motion in the CON action
Functional performance was also measured by means of (i.e., from ~70° to almost full extension), then, and as
the 30-s Chair-Stand Test (30CST; [28]). From a seated the strap rewinds about the flywheel shaft, aim at resist-
position, patients were requested to raise from a chair to ing the inertial force. Thus, patients were requested to
standing, and sit down as many times as possible during gently resist during the first third of the ECC action, and
30 s. The Modified Ashworth Scale [29] was used to assess then apply maximal breaking force to stop the move-
spasticity of the lower limbs. Perceived participation was ment at about 70° knee flexion. Once the flywheel comes
assessed using the Stroke Impact Scale (SIS-Patient-v.2.0 to a stop, a subsequent CON action is instantly initiated.
[30]). Items from the SIS related to physical deficits, every- This methodology and strategy has successfully been used
day activities and ability to move in- and outside home to elicit ECC overload [20,23]. Peak power was measured
(domains 1, 5 and 6) were completed by the participants. in all repetitions using an encoder (100 Hz) and associated
Analysis of SIS was performed following Duncan et al. software (SmartCoach™, Stockholm, Sweden). Three min
[30]. Briefly, mean values for domains 1, 5, and 6 were cal- recovery was allowed between sets. A 10-min warm-up on
culated (100 x (mean value of domains 1, 5 and 6 – 1)/ a cycle ergometer preceded the peak power tests.
(5 – 1)) for each patient. The greater the relative value,
the fewer the restrictions in perceived participation. Isometric leg press force
Isometric LP force was measured using the flywheel de-
Isometric and isokinetic knee extension torque vice ~3 days before and ~7 days after the intervention.
Unilateral knee extension torque of either leg was A foot-platform with a load cell was mounted for each
assessed ~10 days before and ~3 days after completing foot on the exercise device, allowing individual force
the training intervention. The patient was positioned in measurements (100 Hz) of each leg. Isometric tests were
the testing device (IsoMed2000 dynamometer; D&R performed bilaterally and unilaterally for either leg at 90
Ferstl GmbH, Hemau, Germany; 200 Hz). Individual and 120° knee angle. Patients were instructed to push
machine settings were recorded, saved and replicated in as hard as possible for 5 s against the foot-platform,
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adjusted and fixed in the desired position using a chain unrelated to the intervention per se prevented three in-
system. Additional instructions and verbal encourage- dividuals to complete the prescribed study protocol. In-
ment to ensure maximal voluntary effort in tests using dividual characteristics of the remaining 12 patients
both the affected and non-affected limbs were offered. showing 100% compliance to the study protocol are
Two repetitions, with 1 min recovery in between, were depicted in Table 1. Six individuals were cognitively in-
carried out for each action mode. A third repetition was tact; 6 exhibited mild aphasia (5 showed expressive form
allowed if values differed >5%. Peak force averaged over and 1 individual combined expressive and impressive).
a 1 s window was chosen for data analysis. A warm-up Eleven patients were on medication i.e., antihypertensive,
consisting of 10 min cycling and 3 submaximal bilateral lipid lowering or anti-thrombotic, or combinations of
isometric repetitions preceded these tests. these; 3 were prescribed anti-depressants i.e., selective
serotonin reuptake inhibitors; 3 patients were on anti-
Training intervention epileptic drugs i.e., lamotrigin and levetiracetam or
Patients performed unilateral RE training using the af- carbamazepine. Medication was neither altered nor intro-
fected leg on the flywheel LP device (Figure 1), 2 days duced during the study. Four patients had received botulli-
per week during 8 weeks with ≥48 h of rest between ses- num toxin injection at some time i.e., injection to arm and
sions. Four sets of 7 repetitions at maximal effort were leg muscles 3 months (n = 1) or 24 months (n = 3) prior to
performed from ~70° knee flexion to almost full exten- the study.
sion, with 3 min recovery between sets. Peak CON and
ECC power was measured (see above) in all repetitions. Training intervention
Real time performance feedback was offered to the There was a session x muscle action interaction for peak
trainees at all times. Any training session followed a power (F = 5.5, P <0.0005; Figure 2). CON and ECC
warm-up consisting of 10-min cycling at a submaximal peak power increased from session 5 to 16 (P <0.05;
load and one set of 7 coupled CON/ECC actions using except for CON in session 6; P = 0.082). Peak power
modest effort on the LP apparatus. was greater for ECC than CON in sessions 5, 8-9 and
11-16 (P <0.04).
Data analysis
Results are presented as mean ± standard deviation (SD), Isometric and isokinetic knee extension torque
unless otherwise indicated. Balance, gait and functional The non-affected showed 1.4-fold greater isometric knee
performance variables were analyzed by a one-way extension torque than the affected leg both pre and post
ANOVA over time. Isometric knee extension torque was training (Table 2; main effect of leg; F = 63.9, P <0.0005).
analyzed using a two-way ANOVA with repeated mea- There was no change over time for either leg. CON
surements for time and leg. CON and ECC isokinetic isokinetic peak torque was 1.3-fold greater in the non-
torque were examined independently employing a three- affected than the affected leg (main effect of leg; F = 15.5,
way ANOVA (factors time, leg and speed). Peak power P = 0.002), and higher at low compared with high angular
was analyzed independently for CON and ECC muscle velocities (main effect of speed; F = 40.6, P <0.0005).
actions by a two-way ANOVA with repeated measure- CON isokinetic torque was unaltered after training
ments for time and leg. In addition, a two-way ANOVA (Table 2). ECC isokinetic peak torque showed leg x time
(factors time x muscle action) was performed to assess interaction (F = 5.6, P = 0.038). Thus, only the affected,
differences between CON and ECC actions. Isometric LP trained leg showed increased ECC-torque from pre to post
force at 90 and 120° was examined separately using training at 60 (8%; P = 0.036) and 90°/s (7%; P <0.0005;
a three-way ANOVA with factors time, leg and mode Table 2). Overall ECC torque was greater in the non-
(bilateral/unilateral). Training data were examined employ- affected than the affected leg (main effect of leg; F = 56.1,
ing a two-way ANOVA (factors session and muscle action). P <0.0005).
Data normality was assessed through histograms and the
Shapiro-Wilk test. When significant interactions were Peak power
found, simple effect tests were employed. To compen- There was a time x muscle action interaction (F = 11.0,
sate for multiple post hoc comparisons, the false discovery P = 0.008) in peak power. Thus, ECC peak power in-
rate procedure was used [31]. The level of significant was creased more than CON in both the affected and the
set at 5% (P <0.05). non-affected leg (Figure 3A). There was a time x leg
interaction in ECC peak power (F = 5.1, P = 0.046).
Results Thus, although ECC peak power increased in both the
Fifteen patients, most of them being habitually active affected and non-affected leg (affected; P = 0.019; non-
who recently had experienced infrequent low intensity affected; P = 0.003), the gains were greater for the af-
strength training, were initially recruited. Medical issues, fected leg (44% vs. 35%). In addition, the non-affected
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Table 1 Characteristics of the 12 patients that completed the study at baseline


Patient Age (yr) Sex Years since onset Mechanism of stroke Affected side Walking aid
1 57.1 M 12.2 Hemorrhagic R None
2 57.8 F 5.9 Ischemic L Walking stick
3 62.3 M 17.2 Hemorrhagic L Forearm crutch
4 51.9 F 9.9 Ischemic R None
5 71.6 M 3.9 Ischemic L Walking stick
6 75.4 M 9.6 Ischemic R Walking stick
7 58.1 M 10.2 Hemorrhagic R None
8 66.2 M 3.0 Ischemic L None
9 69.3 F 3.9 Hemorrhagic R None
10 70.6 M 4.5 Ischemic L Rollator
11 68.6 M 2.4 Ischemic R None
12 50.7 M 10.9 Hemorrhagic R None
Mean 63.3 ± 8.1 7.8 ± 4.5

leg produced more ECC peak power both pre (P = 0.001) (F = 9.4, P = 0,011; Figure 3B). Thus, while the affected
and post training (P <0.0005), compared with the af- leg produced similar force during bilateral and unilat-
fected limb. CON peak power showed no time x leg eral conditions, the non-affected leg produced higher
interaction. However, there was a main effect of time force in the unilateral than the bilateral test, both at
(F = 10.2, P = 0.009) as CON peak power increased in pre (P = 0.036) and post (P = 0.001) training.
both the affected (34%) and the non-affected (24%) leg. Isometric LP force at 120° knee angle. There was a
In addition, there was a main effect of leg (F = 31.7, time x leg interaction (F = 8.6, P = 0.014; Figure 3C).
P <0.0005) due to greater overall CON peak power Thus, while the affected leg showed increased isometric
in the non-affected than the affected leg. force both bilaterally (17%, P = 0.045) and unilaterally
(20%, P = 0.021), force of the non-affected leg remained
Isometric leg press force unchanged. Force was greater for the non-affected
Isometric LP force at 90° knee angle. There was a main than the affected leg at pre training in both the bilateral
effect of time (F = 5.1, P = 0.045) mainly as the affected (P = 0.027) and unilateral (P <0.0005) mode. Force was
leg produced greater force at post compared with pre greater in the affected vs. non-affected limb in the unilat-
training (P = 0.003 and P = 0.008 for unilateral and bilateral eral mode only at post training (P = 0.025). There was a
mode, respectively). There was a leg x mode interaction leg x mode interaction (F = 10.7, P = 0.008). Thus, the
non-affected leg produced more force in unilateral than
bilateral modes at pre (P = 0.01) and post (P = 0.004)
training. Force of the affected leg was similar across
modes.

Balance, gait, functional performance, spasticity and


perceived participation
Balance (BBS, 7%, P = 0.004), TUG (17%, P = 0.018) and
30CST (17%, P = 0.024) improved with training (Table 3).
There were no changes in 6MWT distance (P = 0.68) or
Modified Ashworth Scale score (P = 0.24; Table 3). There
was an increase in perceived participation (SIS) after
training that was at the limit of statistical significance
Figure 2 Concentric (CON) and eccentric (ECC) leg press peak (P = 0.058).
power (W) of the affected limb over 16 exercise sessions.
Significant main effects (P <0.05); a = interaction session x action, Discussion
b = main effect of session, c = main effect of action. Significant The current study assessed the efficacy of a novel ECC-
simple effects (P <0.05); *vs. session 1; #vs. CON action. Data
overload flywheel RE training paradigm to improve
presented as mean ± standard error of the mean.
force, power, balance and functional performance in
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Table 2 Isometric and isokinetic knee extension torque (Nm) pre and post training
Affected leg Non-affected leg
Pre Post Δ% Pre Post Δ%
Isometric torqueb 135 ± 34 138 ± 39 2 195 ± 41# 187 ± 35# -4
b, c # #
CON torque at 30°/s 113 ± 29 120 ± 32 6 147 ± 33 144 ± 37 -2
CON torque at 60°/sb, c
99 ± 28 102 ± 32 3 123 ± 42# 131 ± 40# 6
b, c # #
CON torque at 90°/s 86 ± 26 88 ± 34 2 111 ± 46 115 ± 50 4
ECC torque at 30°/sb 144 ± 40 149 ± 40 3 171 ± 36# 172 ± 35# 1
a b # #
ECC torque at 60°/s 143 ± 41 154 ± 45* 8 178 ± 40 175 ± 37 -2
ECC torque at 90°/sa b 141 ± 36 151 ± 39* 7 173 ± 36# 174 ± 36# 1
a b c
CON; concentric, ECC; eccentric. Significant main effects (P <0.05); interaction leg x time; main effect of leg; main effect of speed; Significant simple effects
(P <0.05); *vs. pre value within a leg; #vs. affected leg for a time point.

Figure 3 Concentric (CON) and eccentric (ECC) leg press peak power (W) of the affected and non-affected limbs (A), and isometric force in
the leg press at 90° (B) and 120° (C) knee angle for the affected and non-affected leg during unilateral and bilateral tests performed pre and
post training. Significant main effects (P <0.05); a = interaction time x leg, b = interaction time x muscle action, c = interaction leg x mode, d = main
effect of time, e = main effect of leg, f = main effect of mode. Significant simple effects (P <0.05); *vs. Pre within a leg; #vs. affected leg; §vs. bilateral mode
within a leg and time point.
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Table 3 Balance, gait, functional performance and accompanied by an increase of nearly the same magnitude
perceived participation pre and post training in the untrained non-affected leg. Such cross-education ef-
Pre Post fect has previously been reported in stroke patients sub-
Berg Balance Scale (a.u.) 48.5 ± 8.7 51.7 ± 6.4* jected to RE employing ECC actions only [17], inferring
Timed Up-and-Go (s) 16.9 ± 9.1 14.1 ± 7.3* RE favoring ECC actions prompts important central ner-
vous system adaptations [35]. In support, cortical activity
6-minute Walk Test (m) 292.9 ± 144.5 295.3 ± 146.8
is greater during ECC than CON actions [36]. Hence,
30-second Chair-Stand (reps) 8.5 ± 3.5 9.9 ± 4.6*
neural signaling evoked by ECC exercise, and perhaps
Modified Ashworth Scale (a.u.) 0.77 ± 0.54 0.88 ± 0.55 ECC-overload flywheel RE even more so, may reinforce
Stroke Impact Scale (a.u.) 62.2 ± 14.5 66.0 ± 12.8§ certain neural strategies due to the variable velocity, and
a.u.: arbitrary units, s: seconds, m: meter, reps: repetitions. Significant differences: accelerating and decelerating coupled CON-ECC muscle
*vs. Pre (P <0.05); §at the limit of statistical significance vs. Pre (P = 0.058). actions, executed at maximal effort [37]. In support, ECC-
overload flywheel RE elicited more prominent neural ad-
aptations than constant load CON-ECC RE training in
physically active chronic stroke patients (2-17 years post healthy individuals [24]. Altogether, the specific fea-
stroke). Patients complying with the 8-week intervention tures of the current exercise modality appear to facili-
showed marked gains in muscle power of the trained af- tate more favorable stimulus than traditional constant
fected, but of the untrained non-affected limb as well. load or velocity (i.e., isokinetic) RE training paradigms,
Also, there were increases in isometric leg press force because of the emphasis on stretch-shortening cycle
and isokinetic ECC, not CON, knee extension torque, and stretch reflex, resulting in increased afferent traffic
accompanied by improved balance and functional per- and proprioception, and/or the unique motor unit re-
formance without exaggerating spasticity. Thus, the cruitment strategy typical of ECC actions. Indeed, the
results of this investigation suggest that short-term current resistance exercise paradigm seems to induce
ECC-overload flywheel RE training is a valid, safe and greater cross-education adaptations than more trad-
viable method to improve muscle function, balance, gait itional training protocols [17,38].
and functional performance in men and women suffering Isometric leg press force was higher, and increases in
from stroke. response to training greater, at 120 than 90° knee angle,
The ECC-overload flywheel RE training was well re- suggesting stroke patients not only exhibit more weak-
ceived by chronic patients, as indicated by the overall ness in the innermost part of the range of motion of a
37% increase in peak power across sessions (Figure 2), joint [4], but are also less prone to benefit from the exer-
without exacerbating spasticity. Despite the low vol- cise stimulus imposed in that particular range of motion.
ume or exercise dose carried out in each training The overall increase in leg press force for the paretic
session, i.e., 28 coupled CON-ECC actions equivalent limb amounted to 10-20%. Neither limb showed in-
to <1 min of contractile activity, power and balance im- creased isometric knee extension torque post training.
provements induced by the current intervention were This finding concerts the principle of training specificity
robust and comparable to those achieved after more ex- suggesting the transfer effect is most evident in func-
tended (i.e., 12 weeks) training [11,32] using conservative tional mode(s) mimicking the particular exercise exe-
methods employing either isokinetic or gravity dependent cuted during training [39].
loading. Thus, unique features characteristic of the exer- Bilateral maximal voluntary force deficits, such that
cise training paradigm used here and elsewhere [19-24], the summed force produced by each limb alone exceeds
allowing for brief episodes of ECC-overload, unrestricted force in a bilateral action, are well documented in
CON force of any action through the entire range of healthy individuals. In the current investigation, bilateral
motion, variable velocity, and call for acceleration and asymmetry was evident for the non-affected leg (<15%
deceleration of each coupled CON-ECC action, appear to force in the bilateral action), both pre and post training,
reinforce the positive effects of RE, beyond what has been and regardless of knee angle. This observation is consist-
noted in stroke patients subjected to more conservative ent with the report of McQuade et al. [40], noting bilat-
RE methods [11,32]. eral asymmetries in the non-paretic m. biceps brachii of
As muscle power, more so than strength, correlates stroke patients executing isometric elbow flexions, yet
with physical performance in individuals showing re- contrasts reports showing bilateral asymmetries of the
stricted mobility [33,34], rehabilitation programs pre- affected leg only [41] or both legs [42], when subjected
scribed to stroke patients with obvious gait deficits, to lower limb isometric actions. While ample evidence
should target muscle power as a primary outcome. Inter- suggests neural factors are responsible for these deficits
estingly, the marked increase in peak power of the [43,44], inconsistencies in outcome across the above
trained affected leg after the current intervention was studies remain to be explored, e.g., time since stroke,
Fernandez-Gonzalo et al. Journal of NeuroEngineering and Rehabilitation 2014, 11:150 Page 8 of 10
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severity of impairment, and muscle specific recruitment spasticity. Future research employing ECC-overload fly-
of neural pathways. wheel RE warrants investigations comprising more severely
Balance, a critical asset in any upright position with injured stroke victims, as well as control individuals, to af-
obvious impact on quality of life [45,46] and physical firm the applicability of this novel exercise rehabilitation
performance in daily activities [47], is typically impaired paradigm to a broader range of men and women suffering
after stroke. The current low-volume, high-load RE from stroke.
protocol induced early significantly enhanced balance,
assessed by means of BBS. Yet, only one patient attained Conclusions
the proposed limit for minimal clinically significant The current 8-week flywheel RE paradigm, prescribed
difference for the elderly, i.e., an 8-point increment to stroke patients, facilitated robust increases in muscle
[48]. It is worth noting that patients presenting lower strength and power of the affected trained limb, as well
BBS scores before training experienced the most sub- as improved power of the non-affected untrained leg.
stantial improvement in balance. Thus, while five pa- These adaptations were accompanied by significantly en-
tients displayed scores ≤45 (range 28-45), indicating hanced balance, gait and functional performance. While
increased risk of fall [49] prior to training, only one this particular iso-inertial exercise insult allows for unre-
patient appeared to be at risk after the intervention stricted force through the entire range of motion of any
(BBS score 34). Even though the current method asses- performed CON muscle action, it also offers brief epi-
sing balance, i.e., BBS, may have allowed for a “ceiling sodes of ECC-overload. Our novel exercise paradigm ap-
effect” in some patients, it remains the novel exercise pears to present a safe, viable and highly effective method
intervention employed here, improved balance in stroke to improve skeletal muscle function, and performance in
patients. daily living activities, in individuals suffering from chronic
The current training paradigm also improved 30CST stroke.
and TUG performance. Changes in 30CST between 2.0
and 2.6 are associated with improvements corresponding Competing interests
to minimum clinically important difference [50]. In the The authors declare that they have no competing interests.
present study, increases between 2 and 6 suggest 6 pa-
tients exhibited clinically important improvements. TUG Authors’ contributions
scores between 0.8 and 1.4 sec infer major improvement PS, RF-G and PAT designed the study protocol. PS managed and coordinated
the study. CN and BÅ assisted with subject recruitment and, conducted and
[50]. In the present study, 9 patients showed enhanced supervised training sessions. RF-G, CN and BÅ performed tests and data
TUG performance by 1 to 13 sec, indicating major sig- acquisition. RF-G performed data analysis. RF-G, PAT and PS drafted the
nificant clinical improvement. manuscript. All authors have read and approved the final version of the
manuscript.
Walking distance, as reflected in the 6MWT, was un-
changed. While our exercise regime did not intend to Acknowledgments
improve walking, some reports have inferred a causal re- This study was supported by grants from the European Space Agency (ESA;
lationship between muscle strength and walking capacity MAP Project AO-2004-032: PS and PAT), the T-Ö Stiftelsen (1301; RF-G) and
the STROKE-Riksförbundets (RF-G).
[51,52], or that RE may serve to improve comfortable
gait speed and total distance walked [53]. It is worth Author details
1
recalling that whereas use of the hip flexors is critical for Department of Physiology & Pharmacology, Karolinska Institutet, 171 77
Stockholm, Sweden. 2Östersund Rehabcentrum Remonthagen, Östersund,
walking in stroke patients [51], involvement of this Sweden. 3Department of Health Sciences, Mid Sweden University, Östersund,
muscle group was not emphasized with the current RE Sweden.
paradigm, which rather called for closed-chain, simul-
Received: 21 July 2014 Accepted: 20 October 2014
taneous knee- and hip extension. Further, given the par- Published: 30 October 2014
ticular exercise stimulus imposed in this investigation
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doi:10.1186/1743-0003-11-150
Cite this article as: Fernandez-Gonzalo et al.: Chronic stroke patients
show early and robust improvements in muscle and functional
performance in response to eccentric-overload flywheel resistance
training: a pilot study. Journal of NeuroEngineering and Rehabilitation
2014 11:150.

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