Archives of Physical Medicine and Rehabilitation
Volume 90, Issue 4 , Pages 564-570, April 2009

A Comparison of Functional Electrical and Magnetic Stimulation for Propelled Cycling of Paretic Patients

  • Johann Szecsi, MD

      Affiliations

    • Center for Sensorimotor Research, Department of Neurology, Ludwig-Maximillians University, Munich, Germany
    • Corresponding Author InformationCorrespondence to Johann Szecsi, MD, Center for Sensorimotor Research, Dept of Neurology, Ludwig-Maximillians University, Marchioninistrasse 23, 81377 Munich, Germany
  • ,
  • Martin Schiller, MD

      Affiliations

    • Center for Sensorimotor Research, Department of Neurology, Ludwig-Maximillians University, Munich, Germany
  • ,
  • Andreas Straube, MD

      Affiliations

    • Center for Sensorimotor Research, Department of Neurology, Ludwig-Maximillians University, Munich, Germany
  • ,
  • Dieter Gerling, PhD

      Affiliations

    • Department of Electrical Drives, University of Federal Defense, Munich, Germany

Article Outline

Abstract 

Szecsi J, Schiller M, Straube A, Gerling D. A comparison of functional electrical and magnetic stimulation for propelled cycling of paretic patients.

Objective

To compare isometric torque and cycling power, smoothness and symmetry using repetitive functional magnetic stimulation (FMS) and functional electrical stimulation (FES) in patients with paretic legs with preserved sensibility and in patients without sensibility.

Design

Repeated-measures design.

Setting

Laboratory setting.

Participants

Eleven subjects with complete spinal cord injury (SCI) and 29 subjects with chronic hemiparesis (16.6±5.5mo poststroke) volunteered.

Interventions

Using a tricycle testbed, participants were exposed to isometric measurements and ergometric cycling experiments, performed during both 20Hz FMS and FES stimulation. Subjects with hemiparesis and with complete SCI were stimulated at maximally tolerable level and maximal intensity, respectively.

Main Outcome Measures

Maximal isometric pedaling torque and mean ergometric power, smoothness, and symmetry were recorded for voluntary, FES, and FMS conditions.

Results

Two different patterns of the efficacy of FMS were identified. (1) Patients with complete SCI did not benefit (less torque and power was evoked with FMS than with FES, P<.003 and 10−4 respectively). (2) Patients with hemiplegia and preserved sensibility could improve their torque output (P<.05), smoothness, and symmetry of pedaling (P<.05) with FMS more than with FES.

Conclusions

FMS is a potential alternative to surface FES of the large thigh musculature in stimulation-supported cycling of patients with partially or completely preserved sensibility.

Key Words: Magnetic stimulation therapy, Pain, Power, Rehabilitation, Spinal cord injuries, Stroke, Torque

List of Abbreviations: FES, functional electrical stimulation, FMS, functional magnetic stimulation, MAS, Modified Ashworth Scale, SCI, spinal cord injury

 

FUNCTIONAL ELECTRICAL stimulation is a promising rehabilitation technique for artificially activating muscles that are not under voluntary control after an SCI or a cerebrovascular insult.1 Possible applications of FES are to propel or support mobility (gait or cycling) and to make possible conditioning exercises. The advantage of cycling is that it can be maintained for reasonably long periods and the risk of fall is low.

FES-propelled cycling in persons with complete SCI is known to train the cardiovascular system,2 to strengthen the muscles,3 and to improve cycling mobility.4, 5

Most of the literature on FES cycling focuses on patients with complete SCI, although the stroke population is approximately 10-fold that of the SCI population.6 It is thought that electrical stimulation can also be used in the latter case for training purposes as well as for achieving ultimate functional improvement.

However, FES can be clinically impractical in the stroke population, because it induces pain7, 8 as a result of unavoidable stimulation of the skin receptors, including Aδ myelinated heat nociceptors and C-fiber nociceptors.9, 10, 11 For this reason, 8 of 46 subjects in a study on the efficacy of FES in patients with acute stroke12 could not tolerate FES treatment. In the study by Yan et al,13 thigh stimulation intensities of 20 to 30mA were used to achieve weight-supported knee joint movement. In 2 studies on leg stimulation–supported gait in the same group,14, 15 the stimulation intensity was set to 50 to 85mA in an effort to achieve limb movement at the subject's comfort threshold. However, only small or submaximal isometric torques could be generated at those intensities, as seen in the torque recruitment curve of the quadriceps.16 It has been shown17 that increases in quadriceps femoris strength in a healthy population who trained with FES correlated with training contraction intensity and duration. It was concluded that the relative increase in isometric strength resulting from training with FES might be determined by the ability of the subjects to tolerate longer and more forceful contractions. Our previous study18 also demonstrated that cycling power and smoothness in patients with acute stroke are limited by the patient's ability to tolerate stimulation current.

In contrast, by using time-varying electromagnetic fields to induce eddy currents in the adjacent volume without passing the skin, repetitive FMS activates the nerve innervating the muscle without stimulating the skin nociceptors.19, 20, 21 Moreover, magnetic stimulation does not produce radial current, which activates pain nerves in the skin best.21

However, compared with electrical stimulators, magnetic stimulators are bulkier, and they cannot provide focal stimulation.21 Nonetheless, stationary cycling with FMS stimulates the large muscles of the thigh and is considered an adequate application of magnetic stimulation. Human movement, particularly cycling, is equally dependent on isometric force and power output.22 To our knowledge, the reports on magnetic stimulation to generate muscle force in legs of healthy persons are rare,23, 24 and there are no reports at all on the generation of power in persons with only partially preserved or lost sensibility. Because it is painless compared with electrical stimulation, magnetic stimulation is used as a nonvolitional assessment technique of quadriceps muscle strength25 and endurance.26

The goal of the present study was to compare stimulation-induced isometric forces, power, smoothness of movement, and symmetry of pedal forces during cycling using electrical and magnetic stimulation in paretic persons with preserved residual sensibility (stroke group) or with complete loss of sensibility (SCI group). We were also interested in determining whether electrical stimulation and magnetic stimulation induce contraction in different parts of the muscle (superficial vs deep).

Back to Article Outline

Methods 

Subjects 

Stroke group 

Twenty-nine subjects (14 women, 15 men; age, 65.1±10.1y) with chronic poststroke hemiparesis (16.6±5.5mo poststroke) in a stable condition took part in the study. Mobility ranged from impaired to wheelchair confinement (Functional Ambulation Category 1.86±1.1). Most of these subjects were not able to stand independently and were therefore considered unsuitable candidates for treadmill therapy.27 Moderately increased muscle tone during knee extension was obvious in all hemiparetic subjects (MAS 1.0±0.7).

SCI group 

Eleven otherwise healthy subjects (3 women, 8 men; age, 46.8±12.1y) with chronic (10.9±8.1y since injury) complete SCI (ASIA-A) and low levels of muscle spasm (MAS range, 0–2) participated in this study. The muscle fiber composition of their paralyzed muscles was stable.28

All subjects were able to comprehend simple instructions. The University of Munich ethics committee had approved the study, and the subjects gave their informed consent prior to their participation.

Study Design 

Each subject underwent 3 different experimental sessions: (1) isometric measurements using FES and FMS, (2) ergometry using FES, and (3) ergometry using FMS. The session order was randomized, and the 3 types of experiments were performed first in the SCI group and later in the stroke group. Each session was performed on a different day over a period of 6 weeks (SCI group) and 15 weeks (stroke group).

Electrical Stimulation 

The quadriceps and hamstrings muscle groups were electrically stimulated during ergometric cycling (in the stroke group only on the affected side). For isometric measurements, only the left quadriceps group was stimulated in the SCI group and only the affected side in the stroke group. Pairs of autoadhesive gel electrodes (4.5×9.5cm2,a) were placed on the skin over the proximal and distal fourth of each muscle bulk (see similar studies16, 23, 29). A constant-current 8-channel stimulatorb provided the stimulation current (rectangular, biphasic, charged balanced pulses; frequency, 20Hz30; maximum pulse amplitude, 127mA; constant pulse width, 300μs).

Magnetic Stimulation 

Two repetitive magnetic stimulators were used. The Magstim Rapid stimulatorc provided double cosine pulses (2 cosine half-periods, each with 125μs pulse width) and with a 2-tesla maximal magnetic induction. The P-Stim 160 magnetic stimulatord generated double cosine pulses (each with 160μs pulse width) and with a 1-tesla maximal magnetic induction. The frequency was 20Hz, the same as in electrical stimulation. Two round magnetic coilse (diameter, 90mm; 23.3μH inductance) were placed on the subject's clothes overlying the quadriceps muscle and were tilted 45° to the frontal plane. They were fastened to the proximal half of the muscle bulk by straps made of foam and Velcro (fig 1).

  • View full-size image.
  • Fig 1. 

    Isometric and cycling measurement setup. Both FMS and FES stimulation are possible. A subject with complete SCI performing FMS-propelled cycling using 2 magnetic stimulators can be seen. (1) torque transducer, (2) angular encoder, (3) right side repetitive magnetic stimulator, (4) left side coil, (4, 5) straps made of foam and Velcro. Inset: definition of the crank angle.

The stimulation burst durations (see below) were chosen according to the maximally tolerable coil heating.

During the isometric measurements and ergometric cycling, the electrical and the magnetic stimulators were controlled from a personal computer by serial communication. The muscle stimulator was directed to induce muscle contractions on both sides in the SCI group in order to propel cycling and on the affected side in the stroke group to support volitional pedaling. Muscle contractions were induced at the appropriate crank angles.4

Isometric Measurements 

A stationary tricycle with its front wheel replaced by a torque transducerf served as the test bed for isometric torque measurements (see fig 1). An 11-bit incremental encoder, synchronized to turn with the crankshaft, determined the actual position of the crank. Angular and force data were read in by the personal computer at a sample rate of 20Hz. The ankle joint was immobilized at 90°, and leg movement was restricted to the sagittal plane using shank and foot orthoses. The crank angle was set and held automatically by an alternate current-servomotorg position-controlled by a servo-controller. Volitionally or electrically evoked maximal isometric torques of the left leg were measured at a 100° crank angle (see fig 1, inset), with reference to the 0° defined by the left, backward-pointing crank arm (280° for the right leg because of a shift of 180°).

Stroke group 

The maximal torque generated by the quadriceps group was considered only on the affected side. After peak volitional torque on this side was recorded, the subject was instructed to relax for 20 to 30 seconds. Then, beginning at the motor threshold, the muscle was stimulated by FES bursts (fig 2) with amplitudes increasing stepwise (5mA) until the maximally tolerated intensity (indicated by the subject) was reached. Next, while the muscle had been electrically stimulated for 50 seconds at the maximally tolerated FES intensity, FMS bursts that increased stepwise (15%) until the maximally tolerated FMS intensity was reached were applied to the muscle. Finally, the muscle was stimulated twice by the same sequence of FMS bursts as before. The peak torque and corresponding stimulation intensities were recorded in the sequence FES, FMS+FES, and FMS (see fig 2). The burst duration amounted to 1.5 seconds.

  • View full-size image.
  • Fig 2. 

    Isometric measurements performed on a representative subject belonging to the stroke group. Starting from the motor threshold, stepwise-increasing FES and FMS burst amplitudes were applied until maximum tolerable intensity was reached in the first and the last part of the protocol, respectively. Combined stimulation (the FMS burst sequence was superimposed on the FES) was applied in the middle part of the protocol.

SCI group 

The maximal torque generated by the quadriceps group was recorded only at the left side. The muscle was successively stimulated by FMS pulses of amplitudes of 40%, 60%, 80%, and 100%, and with a burst duration of 1.5 seconds (fig 3).

  • View full-size image.
  • Fig 3. 

    Isometric measurements performed on a representative subject belonging to the SCI group. In the first part of the test, starting from the motor threshold, stepwise-increasing FMS burst amplitudes were used until maximal intensity was reached. In the second part of the test, combined stimulation was applied (the FMS burst sequence was superimposed twice on the FES).

Next, while the muscle had been electrically stimulated for 50 seconds at the maximal intensity, the same sequence of FMS bursts as used before was applied to the muscle. Peak torque and corresponding stimulation intensities were recorded in the sequence FMS, FES, and FES+FMS (see fig 3).

Ergometric Measurements 

Dynamic measurements were performed on the stationary tricycle test bed by controlling the resistance torque (motor-powered brake). The braking torque on the crank measured by the torque transducer ranged from 0.15Nm to 7.30Nm. It was set individually at the maximal magnitude at which the patient could cycle for about 3 minutes at a cadence of 35 to 55 rpm. FES and FMS were applied in a randomized order, each in a separate session.

Stroke group 

The subjects cycled for 3 minutes. This consisted solely of volitional cycling in alternation with stimulation-supported cycling, each time for periods of 30 seconds. Patients were instructed to try to achieve smooth pedaling. The maximally tolerable stimulation intensity, determined in isometric tests for each subject, was also used in the ergometric tests. Data for the last 15 seconds of the 30-second periods were collected for each subject and each condition (3 FES, 3 FMS, 6 nonstimulated periods).

SCI group 

Data for 2 minutes of pedaling propelled by stimulation were recorded. The stimulation intensity was gradually increased over about 10 to 30 seconds to the maximum intensity (FES, 127mA; and FMS, 100%) while maintaining the cadence in the range of 35 to 55 rpm.

Data Processing 

Crank angular position and torque were recorded; cadence and power were calculated (also cycling smoothness and symmetry in the stroke group). Cadence was computed from the change in crank position over time. This was digitally filtered with a second-order Butterworth filter with a cutoff frequency of 4Hz by using Matlab v. 6.1.0.h Power was defined as the product of cadence and torque. To measure the smoothness of reciprocal pedaling, a method proposed in the literature31 was used. The smoothness, defined as the summation of the curvature for each instantaneous cranking speed, is given as

where R is the instantaneous cranking speed after tenth-order polynomial curve fitting and s is the crank position. In smooth pedaling, the smoothness will approach 0. The definition of the smoothness is illustrated by the upper graph of fig 4.

  • View full-size image.
  • Fig 4. 

    Cadence (upper graph) and crank torque (lower graph) profiles measured in a subject of the stroke group with right hemiparesis during volitional (gray) and FMS-supported volitional (black) cycling conditions taken over 15-second periods. Measurement points and 10th-order polynomial fitting curve are represented. Abbreviation: QUAD, stimulation interval of the right quadriceps.

To measure symmetry,31 the maximum of the circular autocorrelation coefficient of the crank torque profile (see fig 4, lower graph) was calculated

where j is the angular lag between the 2 highest peaks of the crank torque profile taken over 1 pedaling cycle of 360°. The higher symmetry is as it approaches the maximum value of 1, the higher the side symmetry in torque generation during cycling movement.

The polynomial regression and interpolation of the cadence and the torque to 1° crank angle of the pedaling cycle for the 30-second periods corresponding to each subject and condition were averaged together, yielding 1 cadence and torque profile (see fig 4). By taking the mean value over the cycle, 1 observation of the power resulted for each subject and condition (FES, FMS, no stimulation). Roughness and symmetry were similarly processed for the stroke group.

Statistical Analysis 

The isometric torque evoked and the power generated by electrical and magnetic stimulation were compared. Additionally, volitional and combined (electrically + magnetically) stimulated torques were considered for the stroke group, as well as the smoothness and symmetry of pedaling in electrical and magnetic stimulation conditions. Statistical comparisons were made in the stroke group with the 1-way repeated-measures analysis of variance test with the stimulation mode as factor (FES, FMS, no stimulation) and in the SCI group with the paired t test. Post hoc multiple comparisons in the stroke group were based on the Tukey honestly significant difference criterion. To determine the individual torque response variability to stimulation, linear correlation was used. Comparisons and correlation were considered significant at P<.05. The analysis was performed with the Statistics Toolbox in Matlab v. 6.1.0.h

Back to Article Outline

Results 

Isometric Measurements 

Stroke group 

Significantly more torque was produced volitionally (100%) than electrically (11%) or magnetically (27%) on the affected side of the study participants (P<.001; fig 5). Magnetically evoked torque evoked at 100% stimulation intensity was in all subjects higher than electrically evoked torque (at 62±33mA intensity). Figure 2 illustrates the complete stimulation protocol for a representative patient with stroke. FES produced a maximal isometric torque of about 7.5Nm at a stimulation intensity of 75mA. Using FMS, the torque achieved was about 15Nm at 100% intensity. Combined application of FES+FMS evoked 20Nm torque—that is, the deviation from the sum of torques (15+7.5=22.5Nm) amounts to only about 10%, showing that a summation effect of FES and FMS occurred. The torque produced by FES during combined stimulation showed some decay (about 30% in 50s) caused by fatigue.

  • View full-size image.
  • Fig 5. 

    Isometric torque, power, smoothness, and symmetry of n=29 chronic poststroke patients with hemiplegia measured under volitional, FMS, and FES stimulation conditions. Bars and segments plotted represent group means ± SDs. *FMS compared with FES with significance of P<.05; ##stimulation compared with volitional with significance of P<.001. Abbreviation: VOL, volitional.

As a group, magnetic torque was significantly higher than electrical torque (13.4±3.8Nm vs 5.5±1.73Nm; P<.05; see fig 5). Investigation of individual response variability showed that a moderate correlation (r2=0.53; P<.001) existed between electrically and magnetically evoked torque. The sum of electrical and magnetic evoked torques did not significantly differ from the combined (electrical + magnetic) torque (P=.11).

SCI group 

Magnetically evoked torque (at 100% stimulation intensity) was in all subjects less than electrically evoked torque (at 127mA intensity). While considerable fatigue occurred during continuous electrical stimulation at 127mA (causing electrically evoked torque to vanish), typically positive torque pulses evoked by additionally pulsed magnetic stimulation at 100% occurred (see fig 3). In a group comparison, FMS produced significantly less isometric torque than FES (11.86±3.2Nm vs 16.6±3.5Nm; P=.003). Assessment of individual response variability showed that electrically and magnetically evoked torques correlated well (r2=0.71; P<.001).

In some patients, maximal FMS bursts applied additionally to the FES produced negative break-ins instead of positive peaks.

In the group comparison, the sum of electrical and magnetic evoked torques differed significantly from the combined (electrical + magnetic) torque (P<10−4).

Ergometric Measurements 

Stroke group 

Power generated during volitional and supported cycling (by FES and FMS), amounted to 51.5±22.4W, 53±21.7W, and 55.2±23.4W, respectively. Power did not show significant dependency on the cycling modality (P=.79 in the analysis of variance test).

In contrast, in a comparison of the symmetry and the smoothness of cycling with FMS versus volitional and also FES, most subjects showed improvements both in symmetry (24 and 24 of 29, respectively) and in smoothness (27 and 21 of 29, respectively). In the case of the representative subject exemplified in figure 4, the right-sided hemiplegia caused asymmetrical torque production during purely volitional cycling (symmetry=0.07). Supportive FMS on the right side led to a larger symmetry (0.21). Smoothness improved, decreasing from 44 without FMS to 21 with FMS.

Likewise, the smoothness of cycling in a group analysis (volitional, 56±13.73; FES, 49±14.26; FMS, 40±11.97) was significantly improved (P<.001) by FMS support. It did not significantly improve (P=.65) with FES support compared with volitional cycling. Moreover, FMS-supported cycling was significantly smoother than FES-supported cycling (P<.05).

As the smoothness improved, the symmetry increased significantly under FMS-supported cycling (0.15±0.02) compared with volitional cycling (0.09±0.02; P<.001) or FES-supported cycling (0.13±0.03; P<.05).

SCI group 

Although contiguous and smooth pedaling could be achieved in all subjects by magnetic stimulation (see fig 1), less power was generated with FMS than with FES in all cases. Correspondingly, significantly less power was produced with FMS (2.61±0.88W) than with FES stimulation (7±2.75W; P<10−4; fig 6). This is in line with the observation that less torque is generated by FMS than FES stimulation in fresh or moderately exhausted muscle.

  • View full-size image.
  • Fig 6. 

    Isometric torque and power of n=11 patients with chronic complete SCI measured under FMS and FES stimulation conditions. Bars and segments plotted represent group means ± SDs. Significant comparisons of FES and FMS: *P=.003, **P<10−4, respectively.

Back to Article Outline

Discussion 

Stroke group 

The first important finding of this study is that under our conditions (devices, parameters, stimulation sites), magnetic stimulation supports more effective cycling (in terms of more torque production and better dynamic parameters of cycling like smoothness and symmetry) of subjects with poststroke hemiplegia than electrical stimulation does. This is a result of the partially or completely preserved sensibility in these subjects, which hinders the application of FES more than that of FMS.

Torques evoked by FES and FMS amounted in average to 5.5Nm and 13.4Nm, respectively. Therefore, the ratio of FES-generated and FMS-generated torque in the stroke group is comparable to a similar ratio found in 17 healthy persons by others23 (mean isometric peak torques evoked by FES and FMS amounted to 4.4Nm and 9.5Nm, respectively).

While the FMS-produced torque represents a significant increase of the volitional torque (volitional + FMS compared with volitional; P<.05), this is not true for the FES-produced torque. The magnetically and electrically produced torques correlated only moderately (r2=0.53) because subjects do not respond to both stimulation modes in the same manner. One can speculate that the torque-producing capability depends on the subject's muscle “intrinsic torque capacity,”32p251 and also on the pain tolerance of each subject.

In the ergometric experiment, the power did not increase significantly with any stimulation support. From the viewpoint of kinematic analysis, one would expect a smoother and more symmetrical pedaling with stimulation than without. However, this was achieved only with FMS, presumably because of the higher torques produced with magnetic stimulation.

The summation effect of combined stimulation (FES+FMS), which we observed in the quadriceps musculature of some subjects with stroke, could be interpreted as an additional torque produced by a new, fresh pool of muscle fibers being mobilized by additional magnetic stimulation (see fig 2). A similar summation effect was described earlier33 in a healthy population who received stimulation of the ulnar nerve in a combined (FES+FMS) manner. Therefore, such combined stimulation could be a means to improve mechanical output in patients with preserved sensibility.

SCI group 

Although magnetic stimulation–propelled cycling was possible, it was less effective than electrical stimulation in terms of torque and power-generating capability.

In the combined stimulation (FES+FMS) produced torque, the contribution of FES was more important than the contribution of FMS in the fresh muscle of the SCI group (see fig 3). This was the opposite of the situation found in the stroke group, where FMS made the main contribution of torque (see fig 2). This is explicable in terms of the decay of the electrical field with distance; the decay is less pronounced if induced by magnetic stimulation than by surface electrodes. Thus, muscle tissue can be stimulated at a greater depth with magnetic stimulation.19, 20 Because a summation effect could be shown in the SCI group, we propose that only a few deeper, fresh muscle parts could be mobilized by adding magnetic stimulation to electrical stimulation (see fig 3). Moreover, the occurrence of negative peaks suggests that parts of the antagonistic muscle were activated by FMS. The muscle tissue stratification and thickness that affect penetration depth of FES and FMS stimulation are presumably different in patients with chronic SCI and chronic stroke.

Because both magnetically and electrically produced torques in persons with complete SCI correlated well (r2=0.71), contrary to the stroke group, they presumably respond to both stimulation modes in a more similar manner. Perhaps their torque-producing capability depends mainly on the subject's muscle “intrinsic torque capacity.”32

Experimental Setup 

Fixed stimulation sequences (FES and FMS) were designed for subjects with stroke and subjects with SCI, respectively, thus allowing isometric measurements with FES, FMS, and combined stimulation (FES+FMS) during the same session. Because the interventions were not assigned to each subject in a random order in the isometric measurement protocol, interference effects, mainly fatigue, had to be considered.34 The rationale of the stimulation protocols used is based on our observations made in preliminary experiments that FMS (FES) evoked higher torques than FES (FMS) in subjects with stroke (SCI). Therefore, the adopted stimulation protocols decreased the studied effect rather than increased it.

Stimulation Conditions 

The results of the present study strongly depend on the electrical and magnetic stimulation conditions used. These factors can influence the torque produced and the pain perceived during FES.

While selecting stimulation parameters, one has to consider that the present study focused on optimization of stimulation-induced movement (particularly cycling) rather than solely on maximization of isometric torque. Therefore, torque has to be maximized and fatigue and discomfort minimized at the same time. While the literature is equivocal on the choice of an optimal frequency of FES of the lower extremity regarding isometric force and sensed discomfort (eg, 25Hz23, 35 and 30Hz13, 36), the use of 20Hz seems to be well founded.30

Moreover, previous work performed in our laboratory on the FES cycling of persons with complete paraplegia showed that a stimulation of 20Hz was superior to higher frequencies for average power produced during cycling. This is because higher frequencies cause more rapid fatigue.30 Furthermore, technical limitations of the magnetic stimulators require use of 20Hz stimulation. Therefore, this frequency was adopted during both electrical and magnetic stimulation. Other parameters were set to provide maximal mechanical output according to our laboratory standard (FES pulse shape, maximal amplitude and width, coil placement) or fixed at today's technical standard (FMS induction shape, width, maximal amplitude).

Electrode size and placement was similar to specifications in the literature16, 23, 29 but differed from others.13, 36 We favored this localization because it was in accordance with our previous work37, 38; however, it might have influenced our results.

Further, current induced by magnetic stimulation is strongly dependent on both coil shape and orientation.39, 40 While 2 kinds of coils are in use (circular and figure 8–shaped coils), the latter cannot be used in deep muscle stimulation because of the strong focalization of the induced eddy currents. To achieve mechanical output that overcomes realistic drive resistances, deep musculature like the quadriceps has to be stimulated relatively homogeneously, using a larger coil size, like the 90-mm diameter circular coil. Moreover, a combination of large circular coils (or perhaps elliptical or coils wrapped around the muscle26) with decreased muscle selectivity and mechanically constrained trajectories of the legs (as in cycling) seems to be an adequate application of magnetic stimulation. Another benefit of magnetic stimulation is that no direct skin contact is needed, unlike electrical stimulation, and therefore the patient can remain clothed during treatment.

Back to Article Outline

Conclusions 

The results of this study suggest that magnetic stimulation is a potential alternative to surface electrical stimulation of the large thigh musculature with regard to stimulation-supported cycling of patients with partially or completely preserved sensibility (with, for example, poststroke hemiplegia or multiple sclerosis). While the present study compared the biomechanical efficacy of magnetic and electrical stimulation, further studies have to be performed to determine whether long-term repetitive application of magnetic stimulation is therapeutically more advantageous than electrical stimulation.

Suppliers

Back to Article Outline

Acknowledgment 

We thank Winfried Mayr, PhD, from the Center for Biomedical Engineering and Physics of the Medical University of Vienna for his support and his belief in the applicability of functional magnetic stimulation.

Back to Article Outline

References 

  1. Gorman PH, Alon G, Peckham PH. Functional electrical stimulation in neurorehabilitation. In:  Selzer ME,  Clark S,  Cohen LG,  Duncan PW,  Gage FH editor. Neural repair and rehabilitation. Cambridge: Cambridge University Press; 2006;p. 119–135
  2. Glaser RM. Functional neuromuscular stimulation: exercise conditioning of spinal cord injured patients. Int J Sports Med. 1994;15:142–148
  3. Mohr T, Podenphant J, Biering-Sorensen F, Galbo H, Thamsborg G, Kjaer M. Increased bone mineral density after prolonged electrically induced cycle training of paralyzed limbs in spinal cord injured man. Calcif Tissue Int. 1997;61:22–25
  4. Perkins TA, Donaldson NN, Hatcher NA, Swain ID, Wood DE. Control of leg-powered paraplegic cycling using stimulation of the lumbo-sacral anterior spinal nerve roots. IEEE Trans Neural Syst Rehabil Eng. 2002;10:158–164
  5. Hunt KJ, Stone B, Negard NO, et al. Control strategies for integration of electric motor assist and functional electrical stimulation in paraplegic cycling: utility for exercise testing and mobile cycling. IEEE Trans Neural Syst Rehabil Eng. 2004;12:89–101
  6. Kirsch RF, Kilgore KL. The future of motor neuroprostheses. In:  Horch KW,  Dhillon GS editor. Neuroprosthetics. 1st ed. River Edge (NJ): World Scientific; 2004;p. 981–1004
  7. Liberson WT, Holmquest HJ, Scot D, Dow M. Functional electrotherapy: stimulation of the peroneal nerve synchronized with the swing phase of the gait of hemiplegic patients. Arch Phys Med Rehabil. 1961;42:101–105
  8. Takebe K, Kukulka C, Narayan MG, Milner M, Basmajian JV. Peroneal nerve stimulator in rehabilitation of hemiplegic patients. Arch Phys Med Rehabil. 1975;56:237–239
  9. Chae J, Hart R. Comparison of discomfort associated with surface and percutaneous intramuscular electrical stimulation for persons with chronic hemiplegia. Am J Phys Med Rehabil. 1998;77:516–522
  10. Adriaensen H, Gybels J, Handwerker HO, Van Hees J. Response properties of thin myelinated (A-delta) fibers in human skin nerves. J Neurophysiol. 1983;49:111–122
  11. Van Hees J, Gybels JM. Pain related to single afferent C fibers from human skin. Brain Res. 1972;48:397–400
  12. Chae J, Bethoux F, Bohine T, Dobos L, Davis T, Friedl A. Neuromuscular stimulation for upper extremity motor and functional recovery in acute hemiplegia. Stroke. 1998;29:975–979
  13. Yan T, Hui-Chan CW, Li LS. Functional electrical stimulation improves motor recovery of the lower extremity and walking ability of subjects with first acute stroke: a randomized placebo-controlled trial. Stroke. 2005;36:80–85
  14. Tong RK, Ng MF, Li LS. Effectiveness of gait training using an electromechanical gait trainer, with and without functional electric stimulation, in subacute stroke: a randomized controlled trial. Arch Phys Med Rehabil. 2006;87:1298–1304
  15. Tong RK, Ng MF, Li LS, So EF. Gait training of patients after stroke using an electromechanical gait trainer combined with simultaneous functional electrical stimulation. Phys Ther. 2006;86:1282–1294
  16. Benton LA, Baker LL, Bowman BR, Waters RL. Functional electrical stimulation—a practical guide. 2nd ed.. Downey: Rancho Los Amigos Rehabilitation Engineering Center; 1981;
  17. Selkowitz DM. Improvement in isometric strength of the quadriceps femoris muscle after training with electrical stimulation. Phys Ther. 1985;65:186–196
  18. Szecsi J, Krewer C, Muller F, Straube A. Functional electrical stimulation assisted cycling of patients with subacute stroke: kinetic and kinematic analysis. Clin Biomech (Bristol, Avon). 2008;23:1086–1094
  19. Barker AT, Freeston IL, Jalinous R, Jarratt JA. Magnetic stimulation of the human brain and peripheral nervous system: an introduction and the results of an initial clinical evaluation. Neurosurgery. 1987;20:100–109
  20. Barker AT. An introduction to the basic principles of magnetic nerve stimulation. J Clin Neurophysiol. 1991;8:26–37
  21. Cohen D, Cuffin BN. Developing a more focal magnetic stimulator: part I: some basic principles. J Clin Neurophysiol. 1991;8:102–111
  22. Newham DJ, Donaldson NN. FES cycling. Acta Neurochir Suppl. 2007;97:395–402
  23. Han TR, Shin HI, Kim IS. Magnetic stimulation of the quadriceps femoris muscle: comparison of pain with electrical stimulation. Am J Phys Med Rehabil. 2006;85:593–599
  24. Kremenic IJ, Ben-Avi SS, Leonhardt D, McHugh MP. Transcutaneous magnetic stimulation of the quadriceps via the femoral nerve. Muscle Nerve. 2004;30:379–381
  25. Polkey MI, Kyroussis D, Hamnegard CH, Mills GH, Green M, Moxham J. Quadriceps strength and fatigue assessed by magnetic stimulation of the femoral nerve in man. Muscle Nerve. 1996;19:549–555
  26. Swallow EB, Gosker HR, Ward KA, et al. A novel technique for nonvolitional assessment of quadriceps muscle endurance in humans. J Appl Physiol. 2007;103:739–746
  27. Malezic M, Hesse S. Restoration of gait by functional electrical stimulation in paraplegic patients: a modified programme of treatment. Paraplegia. 1995;33:126–131
  28. Castro MJ, Apple DF, Staron RS, Campos GE, Dudley GA. Influence of complete spinal cord injury on skeletal muscle within 6 mo of injury. J Appl Physiol. 1999;86:350–358
  29. Noel G, Belanger AY. Relation entre la force maximale volontaire, force tetanique et douleur lors de l'electrostimulation du quadriceps femoris. Physiother Can. 1987;39:377–383
  30. Naaman SC, Stein RB, Thomas C. Minimizing discomfort with surface neuromuscular stimulation. Neurorehabil Neural Repair. 2000;14:223–228
  31. Chen HY, Chen SC, Chen JJ, Fu LL, Wang YL. Kinesiological and kinematical analysis for stroke subjects with asymmetrical cycling movement patterns. J Electromyogr Kinesiol. 2005;15:587–595
  32. Horstman AM, Beltman MJ, Gerrits KH, Koppe P, Janssen TW, Elich P, et al. Intrinsic muscle strength and voluntary activation of both lower limbs and functional performance after stroke. Clin Physiol Funct Imaging. 2008;28:251–261
  33. Garnham CW, Barker AT, Freeston IL. Measurement of the activating function of magnetic stimulation using combined electrical and magnetic stimuli. J Med Eng Technol. 1995;19:57–61
  34. Neter J, Wassermann W. Applied linear statistical models. Homewood: Irvin, Inc; 1974;
  35. Malezic M, Hesse S, Schewe H, Mauritz KH. Restoration of standing, weight-shift and gait by multichannel electrical stimulation in hemiparetic patients. Int J Rehabil Res. 1994;17:169–179
  36. Bogataj U, Gros N, Kljajic M, Acimovic R, Malezic M. The rehabilitation of gait in patients with hemiplegia: a comparison between conventional therapy and multichannel functional electrical stimulation therapy. Phys Ther. 1995;75:490–502
  37. Szecsi J, Krause P, Krafczyk S, Brandt T, Straube A. Functional output improvement in FES cycling by means of forced smooth pedaling. Med Sci Sports Exerc. 2007;39:764–780
  38. Szecsi J, Fornusek C, Krause P, Straube A. Low-frequency rectangular pulse is superior to middle frequency alternating current stimulation in cycling of people with spinal cord injury. Arch Phys Med Rehabil. 2007;88:338–345
  39. Amassian VE, Maccabee PJ, Cracco RQ. Focal stimulation of human peripheral nerve with the magnetic coil: a comparison with electrical stimulation. Exp Neurol. 1989;103:282–289
  40. Maccabee PJ, Amassian VE, Cracco RQ, Cracco JB, Eberle L, Rudell A. Stimulation of the human nervous system using the magnetic coil. J Clin Neurophysiol. 1991;8:38–55
  • a Flextrode 4.5×9 cm2 rectangular self-adhering electrodes; Krauth+Timmermann Ltd, Poppenbütteler Bogen 11, 22399 Hamburg, Germany.
  • b Motionstim 8 channel stimulator; Krauth+Timmermann Ltd, Poppenbütteler Bogen 11, 22399 Hamburg, Germany.
  • c Magstim Rapid stimulator with Booster Setup; Magstim Co Ltd, Spring Gardens, Whitland Carmarthenshire, Wales, United Kingdom, SA34 OHR.
  • d P-Stim 160 magnetic stimulator; MAG & More GmbH, Theresienstrasse 90, 80333 München, Germany.
  • e Round magnetic coil (large HP 90); Magstim Co Ltd, Spring Gardens, Whitland Carmarthenshire, Wales, United Kingdom, SA34 OHR.
  • f T30FN torque wave; Hottinger Baldwin Messtechnik Ltd, Am Tiefen See 45, D-6100 Darmstadt 1, Germany.
  • g AC-servomotor MR 7434; ESR Pollmeier Ltd, Lindenstrasse 20, 64372 Ober-Ramstadt, Germany. servo-controler TrioDrive, ESR Pollmeier Ltd, Lindenstrasse 20, 64372 Ober-Ramstadt, Germany.
  • h Matlab v. 6.1.0; Mathworks Inc, Natick, 24 Prime Park Way, MA 01760-1500.

 Supported by the Else-Kröner Fresenius Foundation, Bad-Homburg, Germany (grant no. P35/06//A09/06).

 No commercial party having a direct financial interest in the results of the research supporting this article has or will confer a benefit on the authors or on any organization with which the authors are associated.

 Reprints are not available from the author.

PII: S0003-9993(08)01707-3

doi:10.1016/j.apmr.2008.09.572

Archives of Physical Medicine and Rehabilitation
Volume 90, Issue 4 , Pages 564-570, April 2009