REVIEW ARTICLE

Sports Medicine 14 (2): 100-113, 1992 OI12-1642f92fOOO8~IOO/$7.00fO

© Adis International Limited. All rights reserved.

SPO'157

Neuromuscular Electrical Stimulation and Voluntary Exercise Karl Hainaut and Jacques Duchateau Laboratory of Biology, Universite Libre de Bruxelles, Brussels, Belgium

Contents /00 /0/

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Summary

Summary I. Protocol Diversity of NMES 1.1 Pulse Parameters and Stimulus Regimens 1.2 Training Protocols and Testing Procedures 1.3 Electrically Induced Force of Contraction 2. Muscle Strengthening 2.1 Disused Muscles 2.2 Healthy Muscles 2.2.1 Strength Gain 2.2.2 Contractile Kinetics 2.2.3 Endurance and Fatigue 3. Mechanisms Underlying Adaptations 3.1 Muscle Hypertrophy 3.2 Neural Changes 3.3 Enzymatic Activity Changes 4. NMES and Voluntary Exercise 5. Conclusions

Neuromuscular electrical stimulation (NMES) has been in practice since the eighteenth century for the treatment of paralysed patients and the prevention and/or restoration of muscle function after injuries, before patients are capable of voluntary exercise training. More recently NMES has been used as a modality of strengthening in healthy subjects and highly trained athletes, but it is not clear whether NMES is a substitute for, or a complement to, voluntary exercise training. Moreover the discussion of the mechanisms which underly the specific effects of NMES appears rather complex at least in part because of the disparity in training protocols, electrical stimulation regimens and testing procedures that are used in the various studies. It appears from this review of the literature that in physical therapy, NMES effectively retards muscle wasting during denervation or immobilisation and optimises recovery of muscle strength during rehabilitation. It is also effective in athletes with injured, painful limbs, since NMES contributes to a shortened rehabilitation time and aids a safe return to competition. In healthy muscles, NMES appears to be a complement to voluntary training because it specifically induces the activity of large motor units which are more difficult to activate during voluntary contraction. However, there is a consensus that the force increases induced by NMES are similar to, but not greater than, those induced by voluntary training. The rationale for the complementarity between

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101

NMES and voluntary exercise is that in voluntary contractions motor units are recruited in order, from smaller fatigue resistant (type I) units to larger quickly fatiguable (type II) units, whereas in NMES the sequence appears to be reversed. As a training modality NMES is, in nonextreme situations such as muscle denervation, not a substitute for, but a complement of, voluntary exercise of disused and healthy muscles.

The triggering of muscle contraction by electrical stimulation or neuromuscular electrical stimulation (NMES) has been in practice since the middle of the eighteenth century for purposes of physical therapy and the treatment of paralysed patients (Kratzenstein 1744, quoted in McNeal 1976), using electrostatic generators (cf. also Jallabert 1748, quoted in Licht 1961). Later in the eighteenth century Galvani (1791) published the first results of in vitro experimental stimulation of neuromuscular preparations with galvanic currents. In the early nineteenth century, Faraday conceived a generator of faradic current, which is used in most of our modem stimulators, and initiated a new approach to the study of the effects of electrostimulation in medicine (Duchenne de Boulogne 1867). By the twentieth century, it appeared that in denervated muscles electrostimulation reduced loss of muscle weight and prevented atrophy (Langley & Kato 1915; Osborne 1951), and 'electrotherapy' soon became a common practice in physical medicine for the restoration of muscle function after injuries, before patients are capable of voluntary exercise training. Physicians and coaches have also used NMES to prevent immobilisation-induced muscle atrophy in athletes and to shorten the rehabilitation period (Knight 1980). Today NMES is in widespread use during and immediately after limb immobi1isation. More recently, attention has been drawn to NMES as a modality for strength training in healthy subjects and highly trained athletes and it is suggested that NMES may be superior to voluntary contractions for increasing muscle strength (Kots 1971). This suggestion has not received much support in recent years, although there is experimental evidence that NMES effectively increases strength in healthy muscles (cf. table I and for a review see Enoka 1988; Lloyd et al. 1986). Moreover, it has

been observed in animals that muscle contractile properties adapt to the frequency of stimulation (Lomo et al. 1974; Pette & Vrbova 1985; Salmons & Sreter 1976) and in humans there is evidence that changes in contraction kinetics occur during voluntary training, but that these changes in themselves vary according to the type of contraction (maximal isometric vs submaximal dynamic) [Duchateau & Hainaut 1984]. These observations raise the question of whether training effects of NMES are similar to those obtained with voluntary activation of muscle. This question is difficult to answer from the existing literature because of a lack of consensus. Comparison between experimental results is difficult because of the diversity in training protocols, electrical stimulation regimens and testing procedures that are used in the various studies. Another point which adds to the complexity is that during voluntary contractions, motor units are recruited according to the size principle (Milner-Brown et al. 1973), which is not the case during NMES (Solomonow 1984; Trimble & Enoka 1991). The purpose of this paper is to review the literature and discuss whether NMES is a substitute for, or a complement to, voluntary exercise. The paper focuses on 3 topics with regard to NMES: (1) diversity; (2) specific effects; (3) possible underlying mechanisms.

1. Protocol Diversity of NMES 1.1 Pulse Parameters and Stimulus Regimens Transcutaneous electrical stimulation activates pain afferents as well as muscle fibres; thus, one of the major difficulties posed by NMES is the triggering of a strong contraction with as little discomfort as possible. This can be optimally achieved by adequate positioning of stimulating electrodes

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Table I. NMES-induced strength gain, tested by isometric contractions Reference

Muscle

Frequency of stimulation (Hz)

Training modalities 8 [No. of trials x (stim.-rest)]

Kots' protocol and similar protocols Kots (1971) BB OF Lysens (1981) OF Laughman et al. (1983) Currier & Mann (1983) OF Selkowitz (1985) OF Stefanovska & Vodovnik (1985) OF Miller & Thepaut-Mathieu (1990) BB

2500 2500 2500 2500 2200 2500 2500

Other protocols Halbach & Strauss (1980) Eriksson et al. (1981) Romero et al. (1982)

OF OF OF

50 200 2000

10 x (10-50 sec) 12 x (15-15 sec) 112 x (4-4 sec)

FDI OF OF TS TS AP AP

60 25 50 50 2000 50 100

80 10 30 15 15 15 10

Davies et al. (1985) Stefanovska & Vodovnik (1985) Farrance et al. (1987) Cabric & Appel (1987a) Cannon & Cafarelli (1987) Duchateau & Hainaut (1988) a b

mod mod mod mod mod mod mod

50 50 50 50 50 25 88

10 10 10 10 10 10 5

x x x x x x x

(10-50 sec) (10-50 sec) (10-50 sec) (10-50 sec) (10-100 sec) (10-50 sec) 5 x (5-30 sec)b

x (10-20 sec) x (10-50 sec) x (12-48 sec) to 25 x (5-20 sec) to 25 x (5-20 sec) x (3 to 4-10 sec) x 20 x (1-1 sec)b

Number of training sessions

Gain in strength (MVC) [%]

Gain/session (%)

19 14 25 15 12 21 15

38 11 22 16 44 13 30

2.0 0.8 0.9 1.1 3.6 0.6 2.0

15 20-25 10

22 18 21 c 31 d -11 25 9 50 59 15 13

1.5 0.8 2.1 3.1 -0.3 1.2 0.3 2.4 2.8 1.0 0.4

40 21 30 21 21 15 30

Training modalities: figures between brackets are respectively durations of stimulation and rest periods in each trial. Interrupted series of trials; others are continuous series.

c Dominant leg. d Nondominant leg. Abbreviations: OF = quadriceps femoris; TS = triceps surae; BB pollicis; MVC = maximal voluntary contraction.

(Nelson et al. 1981) and adequate definition of electrical stimuli parameters (Moreno-Aranda & Seireg 1981a,b,c). The muscle motor point, which is the area overlying peripheral neuromuscular junctions, appears to be the most effective site for electrode placement (c£ Duchateau 1991). The rationale for this is that NMES triggers muscle contractions via the activation of motor nerve terminals (Hultman et al. 1983) which are more excitable than muscle cell membranes (Wynn Parry 1961) and the motor point presents on average the closest area of the skin to the end-plates throughout the cross-sectional area of the muscle. Some authors have suggested the use of a small cathode in order to localise the stimulating current

= biceps

brachii; FDI

= first dorsal

interosseus; AP

= adductor

on the motor point, and a larger anode to disperse the electrical current throughout the muscle (Bouman & Shaffer 1956). Other authors prefer to use 2 large electrodes, especially in muscles with more than 1 motor point, for more efficient diffusion of the electrical stimulus (Halbach & Strauss 1980; Trnkoczy 1978). In addition to electrode configuration several pulse parameters should be considered: intensity, duration, frequency of repetition and shape (c£ Alon et al. 1983). Briefly, the rise time of the pulse should be as short as possible in order to avoid the well known membrane accommodation phenomenon; its duration should also be short enough to avoid discomfort but long enough to elicit efficient contractile activity (Hultman et al. 1983). Short

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duration pulses favour the recruitment of large diameter motor unit axons which innervate type II fibres and are generally more superficially located in the muscle (Lexell et al. 1983). The intensity of the pulse which causes discomfort is closely related to its duration (Lapicque 1938) and it is generally accepted that for a pulse duration of 0.1 to 1.0 msec the corresponding intensity triggers the largest nonpainful force of contraction. With alternating current, which is used in NMES to avoid electrode polarisation, carrier frequencies of the stimulus appear to present the optimal strength-pain ratio in the range from 5 kHz to 10kHz (of course at these frequencies, many stimuli will be ignored by the membrane because of its refractory period). The most efficient frequency of repetitive stimulation (or frequency modulation), i.e. that producing the maximal force, appears to range from 50 to 120Hz. It should be noted that in fast-twitch muscle tetanic fusion is reached at higher stimulation frequencies than in slow-twitch muscle (Bigland-Ritchie et al. 1983; Edwards et al. 1977; Miller et al. 1981; Sale et al. 1982b). These optimal frequencies of electrical stimulation are considerably higher than the maximal motor unit firing frequencies during sustained maximal voluntary contraction (MVC) which never exceed 50Hz (Bellemare et al. 1983; Duchateau & Hainaut 1990; Marsden et al. 1983). The stimulus regimens should include periodic rest periods to minimise muscle fatigue and maintain a high enough level of contraction throughout the NMES training session. Two types of stimulus regimen have been investigated: (a) Kots (1971) investigated the effects of NMES for rather long durations of sustained stimulation (10 seconds, 2500Hz carrier frequency modulated at 50Hz) followed by 50 seconds of rest; and (b) Moreno-Aranda and Seireg (l981a) suggested that an optimal stimulus regimen should consist of a high frequency carrier (10 kHz) modulated at low frequency (100Hz) with a short duration (1.5 seconds) repeated every 6 seconds for 60 seconds and followed by a 60-second rest. An NMES regimen which appears to be efficient in one muscle group might not be applicable to other groups, and large differences between muscle groups

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have been observed (cf. Strauss & De Domenico 1986). Moreover, there is considerable variation between subjects' tolerance of electrical stimulation. Optimising electrical stimulation for training of disused and healthy muscles appears rather difficult and may relate more to the individual subject, the state of the muscle and the muscle group than to the pulse parameters and stimulus regimens themselves. An alternative method of activating the neuromuscular system is magnetic stimulation which was found to elicit a response in nerve and muscle at a lower threshold than electric stimulation. This method was suggested to be a useful tool in studies on muscle fatigue (Lotz et al. 1988). 1.2 Training Protocols and Testing Procedures A NMES training protocol must specify the duration of stimulation, the duration of the rest period, number of repetitions, and the frequency and total number of training sessions. Many studies fail to report enough detailed information concerning not only stimulus regimens but also training protocols. Other studies use a considerable variety of intensities, durations of contraction and of rest periods, number of repetitions and total training sessions (ranging from 10 to 40 sessions; daily or 2 to 3 times a week). This diversity adds to the difficulty of analysing the efficiency of NMES for strengthening muscles. Kots (1971), using a daily protocol of 10 repetitions of 10-second sustained contractions followed by 50-second rest period, observed a 38% gain in strength in human biceps brachii after a total of 19 sessions. In most other studies using Kots's protocol, the observed strength gain per session is only roughly half (0.8 to 1.1 %) of the gain (2.0%) reported by Kots (1971) and by Miller and Thepaut Mathieu (1990). Selkowitz (1985) used a similar protocol but doubled the duration of the rest periods to 100 seconds and observed a larger gain in force per session in healthy but nontrained subjects (3.6%). This result demonstrates the significance of the rest periods between contractions, which minimise the effects of fatigue on muscle

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contractility (cf. also Duchateau & Hainaut 1985; Moreno-Aranda & Seireg 1981a). Strength gains induced by NMES have been tested by various procedures involving mainly voluntary isometric or isokinetic contractions. In most NMES training protocols, NMES mimics an isometric voluntary contraction at a constant articular position and may induce a specific adaptation of voluntary contraction to this position (Currier et al. 1979; Lindh 1979; Miller & Thepaut-Mathieu 1990). Romero et al. (1982) concluded that there was a training specificity in relation with articular position. Thus, testing NMES-induced strength gain by isokinetic procedures may explain some conflicting results: Eriksson et al. (1981), gain at all speeds; Romero et al. (1982), gain only a low speed; Currier & Mann (1983), no gain at all. Another way to test strength gain which is not affected by possible 'habituation or learning factors' is the triggering of muscle contraction via electrostimulation of the motor nerve. This procedure appeared helpful in the comparison of effects of NMES and voluntary contraction in human adductor pollicis (Duchateau & Hainaut 1988). 1.3 Electrically Induced Force of Contraction The force of contraction elicited by NMES has been found to be larger than MVC in very few studies (Ikai et al. 1967; Kots & Hvilon 1975). In all other studies NMES-induced force was significantly smaller or equal to MVC (cf. Kramer & Mendryk 1982). According to Kots (1971), during maximal NMES all motor units are activated and thus a greater force of contraction than in MVC is elicited. However, most other workers have not been able to reproduce the results reported by Kots, possibly because of differences in methodology and/ or equipment. Although in some untrained subjects it is possible to induce larger forces by NMES than by MVC (De Domenico & Strauss 1986; Selkowitz 1985), it is generally reported that maximal NMES-induced force is equal to or smaller than MVC. The large force during an MVC is probably due to the activation of synergistic and postural muscles that are not normally activated with

NMES. Other methods of electrostimulation which induce muscle contraction via stimulation of the motor nerve trunk have reported forces equal to or greater than MVC (Ikai et al. 1967; Jones et al. 1979; Moritani et al. 1985; Rutherford & Jones 1988). Maximal stimulation of a motor nerve trunk can be achieved more efficiently than maximal NMES and this is obviously evident in large muscles. Moreover, during voluntary contractions, the neural drive on the muscles is not always maximal and may be affected by the subject's motivation (Bigland-Ritchie & Woods 1984). The reported differences in force of contraction during NMES and MVC appear to result from (a) the difficulty of maximally stimulating muscles by NMES (especially in large muscles); (b) the subject's motivation during MVC and impaired ability to produce a maximal motor drive.

2. Muscle Strengthening Several studies have reported that training by NMES induces strength gains in disused (Eriksson & Haggmark 1979; Eriksson et al. 1981; Godfrey et al. 1979; Wigerstad-Lossing et al. 1988; Williams et al. 1986) and healthy muscles (Cabric et al. 1987a; Currier et al. 1979; Duchateau & Hainaut 1988; Romero et al. 1982; Selkowitz 1985; Stefanovska & Vodovnik 1985). A few studies, however, reported no strength gain during NMES training; possibly because the stimulating pulse was of very short duration (0.045-0.100 msec) [Davies et al. 1985; Mohr et al. 1985] or the number of training sessions was rather limited (St Pierre et al. 1986). The main evidence is that short duration (6 weeks or less) NMES training induces muscle strengthening similar to, but not greater than, voluntary exercise. Whether long term NMES training would be superior to voluntary exercise remains an open question (cf. Enoka 1988). 2.1 Disused Muscles It is generally reported that NMES retards muscle force loss during immobilisation (Morissey et al. 1985; Wigerstad-Lossing et al. 1988) and is

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sufficient to increase muscle strength during rehabilitation (Boutelle et a1. 1985; Johnson et a1. 1977; Lainey et a1. 1983; Morissey et a1. 1985; Munsat et a1. 1976; Singer 1986; Williams & Street 1976; cf. Almekinders 1984 for a brief review). NMES training is considered by some authors as superior to voluntary exercise (Godfrey et a1. 1979) and by others as a supplement to training by voluntary contractions (Eriksson & Haggmark 1979) for increasing muscle strength. Thus, there is a consensus that NMES is effective in preserving muscle force of contraction during immobilisation and improving muscle strength during rehabilitation. However, there is no consensus in the literature that NMES is superior to voluntary contractions for strengthening disused muscles. The observations of Eriksson and Haggmark (1979) and Morissey et a1. (1985) suggest that NMES is complementary to voluntary exercise because in the early phase of rehabilitation it elicits a strength increase which is necessary to perform voluntary training during the later rehabilitation sessions. It has also been suggested that NMES, which stimulates not only motor nerve endings but also pain receptors, induces pain relief (Hymes et a1. 1974). The 'gate control' theory (Melzack & Wall 1965) is the basis of discussion of this apparently paradoxical effect ofNMES which suggests that: (a) manoeuvres such as transcutaneous electrical stimulation activate not only slow conduction pain afferents, but also fast conduction skin afferents; (b) slow pain afferents facilitate the medullar dorsal horn relay of the spino-thalamic pathway to the brain, via a presynaptic inhibitory interneuron or control cell, whereas fast skin afferents inhibit this relay; and (c) fast afferents will 'close the gate' to the transmission of slow pain afferents to the brain (for more details, cf. fig. I). 2.2 Healthy Muscles 2.2.1 Strength Gain Since the work ofKots (1971), attention has been drawn to NMES as a means to increase strength in healthy muscles. Kots reported force increases of about 38 to 50% after only 19 days ofNMES train-

105

J Fig. 1. Schematic illustration of medullar mechanisms of the gate theory: I fast skin afferents; 2 slow pain afferents; 3 medullar interneuron control cell; 4 medullar relay cell of the spinothalamic pathway; 5 output from 4; + and - indicate synaptic facilitation or inhibition, respectively.

ing and claimed that strength increase could be achieved not only in normal healthy subjects but also in trained athletes. However, the training and testing protocols are not well defined and thereafter, other studies in healthy subjects, using NMES training alone or in combination with voluntary exercises, observed strength gains (cf. table I). The degree of force increase is mainly related to the intensity of stimulation that is accepted by the subject and the initial status of the muscle. The higher the intensity of stimulation the greater the number of muscle fibres that will be activated by the stimulus and thus experience a training effect due to NMES. This is especially true for large muscle (e.g. quadriceps femoris) in which the electrically elicited contraction often only achieves 40 to 60% of MVC (Duchateau 1991). Greater increases in muscle strength were recorded in weaker muscles (Johnson et a1. 1977), nondominant limbs (Romero et a1. 1982) and women compared with men (Fahey et a1. 1985; Selkowitz 1985). Thus NMES should be more effective in weaker and disused muscles than in muscles of trained athletes. It appears from the literature that strength gains induced by NMES training in healthy muscles may be as large as but not greater than those induced by voluntary exercise (cf. table II).

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Table II. Comparison of strength gains induced by NMES and voluntary contractions (VC) Muscle

NMES (%)

VC(%)

Eriksson et al. (1981)

OF

Laughman et al. (1983) McMiken et al. (1983)

OF OF

Miller & Thepaut-Mathieu (1990) Canon & Cafarelli (1987)

BB AP OF

+ 14 + 22 + 22 + 30 + 15 + 16 + 33 + 22 +1

+ 16 + 18 + 25 + 28 + 15 + 30 + 43 + 42 + 15 + 33 + 21

Reference

Currier & Mann (1983) Kubiak et al. (1977) Halbach & Strauss (1980) Mohr et al. (1985) Davies et al. (1985) Duchateau & Hainaut (1988)

OF OF OF FDI AP

- 11

+ 13

NMES vs VC NS NS NS NS NS NS P < 0.01 Not tested P < 0.05 P < 0.02 P < 0.05

Abbreviations: OF = quadriceps femoris; BB = biceps brachii; AP = adductor pollicis; FDI = first dorsal interosseus; NS = not

statistically significant.

2.2.2 Contractile Kinetics Previous experimentation in animals has shown that long duration chronic electrical stimulation (8 to 24h per day for several weeks) induces adaptation of the contractile kinetics that is specific to the frequency of stimulation. A slow muscle which has been stimulated at 100Hz shows contractile kinetics comparable with fast muscles (Lomo et al. 1974), whereas a fast muscle stimulated at 10Hz shows the opposite adaptation (Salmons & Sreter 1976). It was thus tempting to suggest that these changes would also occur in humans during NMES. Training the adductor pollicis for 6 weeks by electrostimulation via the motor point at 100Hz (although the maximal motor unit discharge rate during MVC ranges from 30 to 50Hz) did not significantly change its contractile kinetics, whereas voluntary exercise increased the maximal rate of tension development by 16% (Duchateau & Hainaut 1988). In this study the effects of electrostimulation on the twitch-tetanus ratio (Pt/Po) is consistent with the observation that 6 weeks' e1ectrostimulation does not change the muscle contractile kinetics. Pt/Po ratio is related to the muscle contractile kinetics, and in fast muscles, the ratio is smaller compared with slow muscles. The comparison of the Pt/Po ratio during training by e1ectrostimulation and by voluntary contractions indicates that the ratio is not changed by electrically induced contractions, but is significantly reduced

during voluntary exercise (-36%). Neither of these 2 training procedures changes the muscle twitch surface action potential (SAP) elicited by a brief submaximal electrical stimulation of the motor nerve. Thus, in this study the difference in adaptation of muscle contractile kinetics during the 2 training methods should be related to intracellular processes. 2.2.3 Endurance and Fatigue

In experimental animals results consistently indicate that low frequency electrostimulation of long duration (4 to 20 weeks) increases muscle endurance (Edstrom & Grimby 1986; Eerbeek et al. 1984). In humans, a 20 to 58% improvement of resistance to fatigue has been reported after 6 weeks of nearly maximal intensity electrostimulation (5 to 10Hz) for 3 hours daily: in adductor pollicis (Edwards et al. 1982); in tibialis anterior (Scott et al. 1985); in adductor pollicis and first dorsal interosseous (Rutherford & Jones 1988). The maximal muscle force output, which has been found to decrease during low frequency NMES, can be preserved if periods of high frequency stimulation are combined (Rutherford & Jones 1988). In human adductor pollicis, 6 weeks of 10 minutes' electrostimulation (100Hz) daily did not improve muscle endurance (Duchateau & Hainaut 1988), whereas voluntary exercises for a comparable duration significantly reduced muscle fatigue. In this latter

107

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study, the observation that dissociation between the effects of both training methods on muscle fatigue only appears to be significantly different after 30 seconds of contraction suggests that 6 weeks of daily electrostimulation for 10 minutes does not change the anaerobic lactic processes, which are found to be modified in muscles trained by voluntary contractions (for a review cf. Hainaut & Duchateau 1989). These experimental results suggest that improvement of muscle resistance to fatigue requires NMES training sessions of longer duration compared to exercise training by voluntary contractions. The results also indicate that high frequency of stimulation preserves the muscle's maximal force output.

3. Mechanisms Underlying Adaptations In the last decade, adaptation of muscle contractility to exercise has been discussed with much interest as it applies to disused and healthy skeletal muscles (see Almekinders 1984; Enoka 1988; Hainaut & Duchateau 1989; Komi 1986; Lloyd et al. 1986; McDonagh & Davies 1984; Sale 1988; Salmons & Henriksson 1981). These papers, among others, provide a strong basis for our understanding of possible mechanisms which underlie NMES training and its significance compared with voluntary exercise, with regard to muscle strength and contractile kinetics. 3.1 Muscle Hypertrophy It is generally considered that there is a close relationship between muscle tetanic force and muscle fibre cross-sectional area and that long duration training by voluntary contractions induces strength increase and fibre hypertrophy (cf. Alway et al. 1989; Ikai & Fukunaga 1968, 1970; McDonagh & Davies 1984; McDougall et aL 1980; Schantz et al. 1983). Girth increases during NMES have been reported in weakened muscles (Eriksson & Haggmark 1979; Johnson et aL 1977; Williams & Street 1976), but no significant girth change was observed by Godfrey et al. (1979). In these studies

on the effects of NMES on muscle morphological changes, only limb girth changes have been considered, but it is obvious that exercise training may induce increased muscle fibre cross-sectional area and decreased fat tissue volume simultaneously. Using ultrasonography or computed tomography, Singer (1986) found no significant increase in cross-sectional muscle area after 4 weeks ofNMES. Singer's observations are in line with the conclusion of Maughan et al. (1983) that traininginduced changes of muscle strength are not closely correlated with concomitant changes of muscle cross-sectional area (cf. also St Pierre et al. 1986). Eriksson et al. (1981) observed no change in muscle fibre diameter; but for high training intensity, larger force and augmented muscle fibre size have been reported (Cabric et al. 1987b; 1988), and it is suggested that electrical stimulation induces effective morphological changes (Hoppeler 1986; Salmons & Henriksson 1981) provided adequate intensity is used. These experimental results suggest that both NMES and voluntary exercise induce not only muscle morphological changes, but also neural changes (cf. McDonagh & Davies 1984; Moritani & de Vries 1979; Sale 1988). 3.2 Neural Changes The above morphological adaptations to NMES have been discussed on the basis of direct observations. Neural changes are numerous but they can only be discussed indirectly (c£ the review on muscle strength by Enoka 1988). An observation which supports the idea of neural changes is that most studies on the effect ofNMES have been performed in 5 to 6 weeks or less, which appears to be insufficient to explain a major effect of muscle morphological changes (Davies et al. 1988; Eriksson et al. 1981; Moritani & de Vries 1979; Rutherford & Jones 1986; Sale 1988). Other experimental evidence which indicates that neural changes are evoked by NMES is the finding that effective strength increases can be achieved in few training sessions (Alon 1985; Howard & Enoka 1991) and for smaller intensities compared with

108

voluntary exercises (Laughman et al. 1983; Stefanovska & Vodovnik 1985). Indirect evidence of neural adaptation during voluntary exercises was suggested by the finding that strength increase induced by a particular training method is largest when tested by the same type of voluntary contraction. Thus, muscle force increase does not only result from intracellular changes, but also from neural adaptation. Similar observations have been reported when training by NMES in some studies (Currier & Man 1983; Miller & Thepaut-Mathieu 1990; Romero et al. 1982), but Eriksson et al. (1981) did not observe this training specificity using isokinetic contractions after NMES at constant joint angulation. Moreover, neural adaptation during voluntary strength training is supported by EMG studies which reported increased motor unit activity (Komi & Tesch 1979; Moritani & de Vries 1979; Thepaut-Mathieu et al. 1988), improved motor unit synchronisation (Milner-Brown et al. 1975) and potentiation of reflex activity (Milner-Brown et al. 1975; Sale et al. 1982a). During muscle strengthening by NMES, Singer (1986) observed motor unit synchronisation similar to that observed during training by voluntary contractions. The intriguing cross-transfer phenomenon during NMES also supports the idea of the presence of neural adaptation during electrostimulation. Cross-transfer which has been reported in relation with motor learning and voluntciry exercise training (Coleman 1969; Hellebrandt et al. 1947; Hellebrandt 1951; Moritani & de Vries 1979) has also been observed during NMES (Laughman et al. 1983; Singer 1986). This contralateral effect of electrostimulation has been quantitatively analysed by Howard and Enoka (1987) who concluded that 'electromyostimulation can have an effect that is not accessible by voluntary activation' (Enoka 1988). In conclusion, it appears that there is indirect but consistent evidence of neural adaptation during NMES stimulation as well as during voluntary exercise.

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3.3 Enzymatic Activity Changes Disuse atrophy is associated with decreased muscle content in the oxydative enzyme succinic dehydrogenase (SDH) [Edstrom 1970; cf. also St Pierre et al. 1988, for other enzymes) and thus muscle oxidative capacity and consequently its endurance are impaired. NMES was found to preserve this capacity and prevented SDH decrease during immobilisation following sports injuries of the knee ligaments (Eriksson 1976). When comparing NMES and voluntary exercise training during recovery after knee surgery, Eriksson and Haggmark (1979) reported that NMES in combination with voluntary contractions showed an increase in SDH which was not present during voluntary training alone. Moreover, Curwin et al. (1980) observed that high frequency NMES plus voluntary exercise induced increased muscle myofibrillar ATPase activity. In healthy muscles, however, the addition of NMES to intense voluntary exercise had no additional effect on enzymatic activity (Eriksson et al. 1981). In conclusion, NMES training and voluntary exercise induce complementary enzymatic activity changes in muscles which are additive during submaximal contractions, such as those recorded from disused muscles.

4. NMES and Voluntary Exercise NMES and voluntary exercise induce both neural and muscle intracellular processes adaptation. However, it is difficult to decide from the literature whether one training method is more efficient for a given intensity. This difficulty probably results from the wide variety of training and testing protocols used in the comparison of NMES and voluntary exercise (see Enoka 1988; Lloyd et al. 1986). In an attempt to resolve this issue, Duchateau and Hainaut (1988) compared standardised submaximal NMES with voluntary contractions of similar intensity and duration and tested the effects on muscle contractility by MVC and maximal electrical stimulation of the motor nerve. The results confirm previous conclusions that NMES and

Muscle Electrical Stimulation

voluntary exercise training are complementary. The results also indicate that submaximal voluntary exercises in healthy muscles are more efficient than submaximal NMES, because the gain in force and the muscle resistance to fatigue is larger after voluntary training of identical duration. However, when the neural command of contraction is altered, NMES training appears to be more efficient than voluntary exercise (cf. Almekinders 1984). One of the major questions which emerges from the literature is the discussion of the mechanisms which underlie muscle adaptation to training by NMES and its specificity compared with voluntary exercise. A possible explanation of the difference between the 2 protocols has to do with the motor unit activation. With voluntary exercise, submaximal force is controlled by the modulation of motor unit recruitment and discharge rate (Dorfman et al. 1990; Maton 1981). With NMES, however, there does not appear to be a similar modulation of motor unit activity during submaximal activation. Moreover, mammalian muscles contain slow twitch (type I) and fast twitch (type II) fibres which have different fatigue resistance (for more details cf. Burke et al. 1973; Gardiner & Olha 1987; McDonagh et al. 1980a,b). Knaflitz et al. (1990) reported identical motor unit recruitment order in voluntary and electrically elicited contractions of the tibialis anterior in 72% of their subjects. However, most authors conclude that slow and fast twitch fibres are involved differently in the 2 training procedures (cf. Enoka 1988) and this has recently been documented in an elegant experimental approach (Trimble & Enoka 1991). In submaximal voluntary contractions, type II fibres will not be activated throughout the contraction because the muscle strength is gradually increased (or decreased) and the motor units are recruited (and derecruited) according to the 'size principle' (Henneman et al. 1965; Milner-Brown et al. 1973). In these contractions, the motor units are activated by the synaptic current impinging on the motor neuron. As a consequence the smaller type I motor neurons with higher input resistance will be activated more easily (Burke & Edgerton 1975; Henne-

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Fig. 2. Schematic illustration of inward depolarising currents (I) efficiency in two motoneurons of different size, a small one (mn) and a larger one (MN). In mn the input resistance (Re) is greater compared with MN (re) and membrane depolarisation (V) is thus larger in mn than MN (v) for identical I.

man et al. 1965) [cf. fig. 2]. The situation is completely different in contractions triggered by NMES, because the muscle fibres of the motor units are activated by an electric current which is applied extracellularly to the nerve endings, and larger cells with lower axonal input resistance are more excitable (Blair & Erlanger 1933; Solomonow 1984). In fact, when the stimulus is applied from outside the cell, the electric current must first enter through the membrane before it depolarises the cell, but the extracellular medium shunts the current, and the smaller motor units will not be activated during submaxima1 NMES because of their higher axonal input resistance. Therefore, the smaller motor units which were shown to present the largest mechanical changes during submaximal voluntary exercise (Hainaut et al. 1981) do not adapt to training with submaximal NMES, but do with voluntary exercise at comparable force. The observation that the dissociation between the effects of both training methods on muscle fatigue appears to be significantly different after 30 seconds of contraction suggests that submaximal NMES does not change the anaerobic lactic processes, which are improved in muscles trained by voluntary contractions of comparable workloads (Hainaut & Duchateau 1989). In conclusion, submaximal NMES (the practical way of training by this method) is not superior but complementary to voluntary exercise of com-

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parable intensity. The complementarity of the 2 training methods, which was suggested in other studies perhaps appears more clearly today because the comparison of standard training by NMES and voluntary contractions indicates that not only type but also number of motor units trained by the 2 procedures are different.

5. Conclusions Training by NMES is found in most studies to induce strength gains in both disused and healthy muscles. These gains have been observed for various training protocols and stimulus regimens, but for periods which do not exceed 6 weeks. The main conclusion is that NMES can be a substitute for voluntary exercise in pathological or post-traumatic situations, but not in healthy muscles capable of normal voluntary contractions. In physical therapy, NMES effectively retards muscle wasting during denervation or immobilisation, and optimises recovery of muscle strength during rehabilitation. It is also effective in athletes with injured, painful limbs in which atrophy and reflex inhibition may be present. In these subjects NMES can substitute for and/or complement voluntary exercise, because it avoids excessive stress and pain due to voluntary contractions. NMES appears useful in shortening rehabilitation time and, in athletes, aids a safe return to competition. In healthy muscles NMES appears to be a complement to voluntary training because it specifically induces the activity of larger motor units which are more difficult to activate during voluntary contraction. However, there is a consensus that the force increases induced by NMES are similar to but not greater than those induced by voluntary training. In submaximal contractions of comparable workload voluntary exercise induces larger strength and endurance increases than NMES. The rationale for the complementarity between NMES and voluntary exercise is that in voluntary contractions motor units are recruited in order from smaller fatigue resistant (type I) units to larger fast fatiguable (type II) units, whereas in NMES the se-

Sports Medicine 14 (2) 1992

quence appears to be reversed. On the other hand, submaximal voluntary training induces greater strength and endurance because more small motor units, which were found to present the greatest adaptation to submaximal exercise, are recruited and thus trained.

Acknowledgements This invited review was supported by the Fonds National de la Recherche Scientifique of Belgium and the Conseil de la Recherche of the Universite Libre de Bruxelles. The authors thank Professor Phillip F. Gardiner for reading the manuscript and Miss Anne Deisser for assistance in the preparation of the manuscript.

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