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EQUINE VETERINARY JOURNAL 671

Equine vet. J. (2010) 42 (Suppl. 38) 671-675


doi: 10.1111/j.2042-3306.2010.00180.x

Evaluation of neuromuscular electrical stimulation on fibre


characteristics and oxidative capacity in equine
skeletal muscles evj_180 671..675

A. BERGH*, H. NORDLÖF† and B. ESSÉN-GUSTAVSSON‡

Departments of Anatomy, Physiology and Biochemistry and Department of Animal Environment and Health, and ‡Department of Clinical
Sciences, Swedish University of Agricultural Sciences, Sweden; and †Department of Community Medicine and Rehabilitation, Umeå
University, Sweden.

Keywords: horse; fibre type; fibre area; glycogen; enzyme activity; rehabilitation

Summary Introduction

Reasons for performing study: Neuromuscular electrical Physical rehabilitation of equine musculoskeletal injuries is an
stimulation (NMES) is used to increase or maintain muscle expanding field (McGowan et al. 2007). Methods used in man are
strength during rehabilitation. Human studies investigating often extrapolated to veterinary medicine without sufficient
different protocols show that some treatments induce changes scientific evidence of their effects. One modality used is
in muscle characteristics. Despite the frequent use of NMES in neuromuscular electrical stimulation (NMES), where electrodes
horses, no studies have been published describing its efficacy. are placed on the skin and contractions in the muscle are produced
Objectives: To investigate the effects of a NMES protocol on by electrical stimulation (Lake 1992). With NMES, it is possible to
equine fibre types and areas, glycogen concentrations and induce contraction patterns different from those during voluntary
enzyme activities. contraction (Delitto and Snyder-Mackler 1990). It is generally
Methods: NMES was administrated to m. gluteus medius and accepted that NMES first recruits force-producing type II muscle
m. longissimus dorsi, on one side of 6 healthy Standardbred fibres and then type I fibres, which is the reverse of the muscle
horses. The contralateral side of each muscle served as a recruitment pattern in a voluntary contraction (Hainaut and
nonstimulated control. The horses were stimulated at 50 Hz a Duchateau 1992; Requena-Sánchez et al. 2005).
day, with 21–39 mA, for 45–60 min, 5 days a week for 4 weeks. The main purpose of using NMES is to improve the maximal
Needle biopsies were obtained from the muscles on both sides voluntary strength of weakened and/or healthy muscles. Human
before and after the experimental period. Muscle samples reviews report increased muscle strength due to NMES in athletic
were analysed for fibre type proportions and area using training, training during immobilisation and pathology treatments
histochemical methods and for glycogen and enzyme activities (Laughman et al. 1983; Gibson et al. 1988; Wigerstad-Lossing
(citrate synthase, 3-OH-acyl CoA dehydrogenase, hexokinase et al. 1988; Hainaut and Duchateau 1992; Parker et al. 2003;
and lactate dehydrogenase) using biochemical methods. Gondin et al. 2006; Herrero et al. 2006; Colson et al. 2009). It can
Muscle contractions at the location and depth of the muscle be concluded that the effect of NMES on healthy subjects is equal
biopsy were confirmed by diagnostic ultrasound. to but not superior to voluntary strength training, that the protocols
Nonparametric tests (Mann-Whitney, Wilcoxon sign-rank) that associate electrostimulation with voluntary muscle
were used for statistical analysis. contractions seem to have more effect than electrostimulation
Results: No significant differences were observed in alone, and that NMES is effective in reducing muscle wasting
the percentage of types I, IIA or IIX fibres, fibre areas, during immobilisation (Bax et al. 2005; Requena-Sánchez et al.
glycogen levels or enzyme activities either when comparing 2005; Vanderthommen and Duchateau 2007). In man, NMES has
stimulated and nonstimulated muscles before and after the been shown to cause fibre type changes towards fewer fast
NMES treatment, or when comparing the left and right contracting type II fibres, increased cross-sectional area and
muscle samples. increased citrate synthase (CS) activity indicating a higher
Conclusions: The NMES treatment was well tolerated by oxidative capacity in the muscle (Gauthier et al. 1992; Thériault
the horses, but the present protocol did not induce significant et al. 1994; Pérez et al. 2002; Nuhr et al. 2003, 2004; Del Corso
muscle adaptations. Further studies are needed to describe et al. 2007). The above results are contradicted by other human
the effect of more intense and/or prolonged NMES studies where no significant differences in muscle strength, muscle
treatment protocols on muscles of healthy horses, and to mass, fibre types or CS activity were seen after electrical
describe if stimulation protocols induce positive changes in stimulation (Eriksson et al. 1981; Arvidsson et al. 1986; Suetta
atrophied muscles. et al. 2004, 2008).

*Corresponding author email: Anna.Bergh@afb.slu.se


[Paper received for publication 08.01.10; Accepted 30.05.10]

© 2010 EVJ Ltd


672 Effect of NMES on horses

TABLE 1: Amperage interval (mA) for the horses at the beginning and the end of the weeks of (NMES) neuromuscular electrical stimulation treatment

Week 1 Week 2 Week 3 Week 4

Start End Start End Start End Start End


Mean Range Mean Range Mean Range Mean Range Mean Range Mean Range Mean Range Mean Range

M. gluteus 25 28.5 29 33 33.5 34.5 33.5 36


medius 22.5–28 27–30.5 28–30.5 32–34.5 32–35 32.5–36 31.5–36 34.5–39
M. longissimus 22.5 26.5 27 31.5 31.5 32 32 34
dorsi 21–24 25.5–28 26.5–28 30–32.5 30.5–32.5 30.5–34 30.5–33 32.5–36

To the best of our knowledge, there is nothing reported in the which was held for 10 s followed by a 2 s decrease to 0 mA. The
literature on NMES and its effect on horse muscle tissue. Changes total stimulation time was therefore 15 s. In order to achieve a
in strength cannot be measured directly in horses as in man, but comparable degree of muscle contraction, the stimulation current
alterations in muscle histochemical and fibre type properties can be was set individually for each horse (Table 1) with such intensity
studied with the muscle biopsy technique. Therefore, the aim of that it produced an obvious visual and palpable contraction in the
present study was to use this technique to investigate if a NMES muscle, without any apparent discomfort for the horse.
protocol has any effect on muscle characteristics in healthy
untrained horses. Muscle biopsies: Muscle biopsies (Lindholm and Piehl 1974)
were performed with a Bergström biopsy needle2 (external
diameter 5 mm). Biopsy samples were taken by the same
Materials and methods
investigator from both the stimulated and nonstimulated m.
gluteus medius and m. longissimus dorsi before and after the
Horses and environment
treatment period, at a site halfway between the 2 electrodes for
each muscle. The biopsy needle was inserted to a depth of
The study comprised 6 healthy Standardbred trotters (3 mares and
4–5 cm and the collected muscle sample was frozen in liquid
3 geldings), with a mean age of 6 years (range 4–13 years) and a
nitrogen and then stored at -80°C until analysed. The muscle
mean weight of 471 kg (range 420–492 kg). During the treatment
sample for histochemical analysis was rolled in talcum powder
period, the horses were out on pasture for 4–5 h/day. The
before being frozen in liquid nitrogen.
experiments were approved by the Ethical Committee on Animal
Experiments in Uppsala, Sweden.
Histochemical analysis: Transverse serial sections (10 mm) of
muscle biopsy specimen were cut in a cryostat at -20°C. These
Muscles sections were stained for myosin ATPase after both acid (pH 4.3
and 4.6) and alkaline (pH 10.3) pre-incubation. Muscle fibres were
The muscles chosen for stimulation were m. gluteus medius and m. identified as type I, type II A, type II B or type II C (Brooke and
longissimus dorsi on one side, while the muscles on the other side Kaiser 1970; Essén et al. 1980). Type I fibres stained black, type II
did not receive any intervention and thereby served as within- A fibres white and type II B fibres grey or brown after pre-
subject controls. incubation at pH 4.6. Type II C fibres stained black or grey after
pre-incubation at pH 4.3, 4.6 and 10.3. Type II B fibres identified
Equipment with the ATPase staining method will be called type II X fibres in
the present study. The reason for this is to not confuse with the
Neuromuscular electrical stimulation was performed with the nomenclature used when 4 fibre types are identified due to different
1
muscle stimulator CEFAR MYO . The electrodes were 50 ¥ MHC isoforms (MHCI, MHCIIA, MHCIIX, MHCIIB). Since
100 mm carbon-impregnated rubber electrodes1. Blue Gel1 was MHCIIB fibres, which are expressed in small mammals, do not
used to create good contact between the electrode and the skin. exist in horse muscle type II B fibres are more related to MHCIIX
fibres (Rivero and Serrano 1999).
Electrode placement: After identifying the motor points (the area Muscle composition was determined by typing at least 200
where the motor nerve enters the muscle), the positions of the 4 fibres. In a few cases, the samples contained a lower number of
electrodes (2 for each muscle) were shaved to improve the fibres (the range was 125–286 fibres). In a computerised image
contact between the electrodes and the skin and to assist the analysis system (BIO-RAD)3, fibre type distribution (%) and mean
investigator in finding the motor point during subsequent fibre type area (mm2) for each fibre type were investigated. All
stimulation sessions. measurements were carried out blind, and the codes were broken
only after collection of all the data.
Stimulation protocol: The horses were stimulated once a day,
between 45 and 60 min, 5 days a week for 4 weeks. Both muscles Biochemical analysis: Whole muscle biochemical analyses were
were stimulated simultaneously. The number of contractions was performed on freeze-dried muscle, weighing 1–3 mg, after blood,
increased from 3 ¥ 10 during week 1, 3 ¥ 15 during weeks 2 and 3, fat and connective tissues had been dissected free under a
to 3 ¥ 20 contractions week 4. There was a two-minute rest between microscope. One muscle sample was homogenised in ice cooled
the sets of contractions. The stimulation was a biphasic rectangular 0.1 mol/l phosphate buffer at pH 7.3 and the activities of
pulse form with a frequency of 50 Hz and with a pulse width set to citrate synthase (CS), 3-OH-acyl-CoA-dehydrogenase (HAD),
300 ms. The protocol included a 3 s rise to the full contraction, hexokinase (HK) and lactate dehydrogenase (LDH) were analysed
© 2010 EVJ Ltd
A. Bergh et al. 673

TABLE 2: Mean ⫾ s.d. for fibre type composition and fibre type areas in m. gluteus medius and m. longissimus dorsi of 6 horses without (control) and
with (NMES) neuromuscular electrical stimulation for 4 weeks

M. gluteus medius M. longissimus dorsi

Before After 4 weeks Before After 4 weeks

Fibre type (%)


I
Control 14 ⫾ 5 13 ⫾ 2 20 ⫾ 5 18 ⫾ 3
NMES 17 ⫾ 5 15 ⫾ 7 21 ⫾ 2 20 ⫾ 3
II A
Control 42 ⫾ 3 43 ⫾ 4 41 ⫾ 3 40 ⫾ 4
NMES 42 ⫾ 8 43 ⫾ 8 43 ⫾ 6 42 ⫾ 6
II X
Control 44 ⫾ 6 44 ⫾ 3 39 ⫾ 4 42 ⫾ 4
NMES 41 ⫾ 10 42 ⫾ 9 36 ⫾ 6 38 ⫾ 5
Fibre area (mm2)
I
Control 2190 ⫾ 457 2075 ⫾ 709 2690 ⫾ 716 2725 ⫾ 841
NMES 2014 ⫾ 339 1787 ⫾ 575 2733 ⫾ 391 2611 ⫾ 327
II A
Control 2635 ⫾ 392 2430 ⫾ 755 2866 ⫾ 623 2786 ⫾ 584
NMES 2772 ⫾ 316 2138 ⫾ 419 2962 ⫾ 470 2999 ⫾ 476
II X
Control 4494 ⫾ 673 4476 ⫾ 1265 5057 ⫾ 1714 5161 ⫾ 984
NMES 4552 ⫾ 1155 3622 ⫾ 1076 5465 ⫾ 989 5357 ⫾ 594
Mean area (mm2)
Control 3446 ⫾ 505 3389 ⫾ 896 3654 ⫾ 922 3799 ⫾ 840
NMES 3436 ⫾ 404 2735 ⫾ 554 3792 ⫾ 557 3819 ⫾ 428

as previously described (Essén et al. 1980; Essén-Gustavsson et al. started, there were no significant differences in muscle
1984). CS and HAD were analysed to evaluate the muscle oxidative characteristics between the NMES and the control side. NMES
capacity, HK to evaluate the capacity for phosphorylation of treatment for 4 weeks did not induce any significant changes in
glucose and LDH was analysed as a marker for glycolytic capacity fibre type composition, fibre area, enzyme activities and glycogen
as this enzyme is needed for lactate production. The muscle sample content in any of the muscles. Furthermore, no differences were
for glycogen determination was boiled for 2 h in 1 mol/l HCl and seen in these parameters when comparing the left and right side of
the glucose residues determined fluorometrically (Lowry and the muscles. No apparent discomfort or skin irritation was detected
Passonneau 1972). in any horse. The result from the evaluation with diagnostic
ultrasound shows a clear visual muscle contraction down to a depth
Additional study on an anaesthetised horse: On one occasion, of 8 cm in the m. gluteus medius muscle and a depth of 6 cm in the
one anaesthetised healthy Standardbred trotter was placed in m. longissimus dorsi muscle.
lateral recumbency and stimulated with the identical programme
as the standing horses. The intensity required to produce Discussion
an obvious visual and palpable contraction comparable with
those of the standing horses was 34.5–39.0 mA. During Results from the present study demonstrate that daily treatment
stimulation, an experienced radiologist confirmed the localisation with the current NMES-protocol for 5 days a week over 4 weeks
and depth of the muscle contraction with a diagnostic does not cause any significant changes in muscle fibre types, fibre
ultrasound (Mindray)4, using a linear probe at the frequency of areas, glycogen content or enzyme activities in healthy horses.
7 MHz. Data on muscle characteristics in the present study are in
good agreement with earlier findings on Standardbred trotters
Statistics: SPSS for Windows version 10 was used for data (Ronéus et al. 1992; Karlström et al. 1994). Data obtained from
analysis. The Wilcoxon sign-rank tests were applied for the right side of the muscle did not differ from those obtained on
comparison of the differences between pre- and post values for both the left side, which also agrees with results from an earlier study
stimulated side and control side. The Mann-Whitney test was used (Essén-Gustavsson et al. 1989). In man, NMES may influence the
for comparisons between horses. Statistical significance was set to muscle properties in both legs, when stimulation was performed
P<0.05. only in one leg (Carrol et al. 2006). However, such a crossover
effect is not likely in the present study as no changes were seen
Results in either stimulated or nonstimulated side, before or after
stimulation.
The stimulation intensity to the horses is reported in Table 1, results Our results diverge from some results found in human studies,
on muscle fibre characteristics are shown in Table 2 and results on where NMES has been shown to induce fibre type changes. The
enzyme activities and glycogen in Table 3. Type II C fibres were amount of type II A fibres increased while the amount of type II X
found in only some samples and, since there were so few fibres, and type I fibres decreased after electrical stimulation for 30 min, 3
they were added to the type II A fibre pool, since II C fibre areas days/week for 6 weeks (Pérez et al. 2002) and stimulation for 10
mostly resembled this fibre type. Before the treatment period weeks, 4 h/day and 7 days/week caused a decrease in II X fibres and
© 2010 EVJ Ltd
674 Effect of NMES on horses

TABLE 3: Mean ⫾ s.d. for citrate synthase (CS), 3-OH acyl CoA dehydrogenase (HAD), lactate dehydrogenase (LDH) and hexokinase (HK) and glycogen
in m. gluteus medius and m. longissimus dorsi activities of 6 horses without (control) and with (NMES) neuromuscular electrical stimulation for 4
weeks

M. gluteus medius M. longissimus dorsi

Before After 4 weeks Before After 4 weeks

CS (mmol/kg/min)
Control 53 ⫾ 13 52 ⫾ 10 54 ⫾ 12 49 ⫾ 9
NMES 53 ⫾ 10 53 ⫾ 13 53 ⫾ 15 51 ⫾ 13
HAD (mmol/kg/min)
Control 22 ⫾ 5 24 ⫾ 4 32 ⫾ 5 30 ⫾ 5
NMES 23 ⫾ 4 24 ⫾ 4 28 ⫾ 3 31 ⫾ 5
LDH (mmol/kg/min)
Control 1300 ⫾ 174 1284 ⫾ 189 2015 ⫾ 177 1887 ⫾ 114
NMES 1291 ⫾ 95 1258 ⫾ 59 1936 ⫾ 95 1991 ⫾ 95
HK (mmol/kg/min)
Control 3.9 ⫾ 0.7 3.6 ⫾ 0.6 2.7 ⫾ 0.7 3.2 ⫾ 1.3
NMES 4.1 ⫾ 0.8 3.9 ⫾ 0.6 2.7 ⫾ 0.5 2.6 ⫾ 1.3
Glycogen (mmol/kg)
Control 495 ⫾ 62 500 ⫾ 101 522 ⫾ 84 535 ⫾ 57
NMES 493 ⫾ 70 500 ⫾ 93 546 ⫾ 41 567 ⫾ 50

an increase in type I fibres (Nuhr et al. 2003, 2004). These studies types occurred after a longer duration of training, while metabolic
also showed changes in enzyme activities that indicated an changes occurred earlier.
increased oxidative capacity in the muscle. Although the NMES protocol used in the present study was
Other studies have shown increased CS activity after designed to simulate strength-training with an increasing number
electrical stimulation; 3 h/day, 6 days/week for 6 weeks (Gauthier of contractions over the experimental period, it was used on the
et al. 1992) and after 8 h/day, 6 days/week for 4 weeks (Thériault back muscles of healthy horses - muscles that are more or less
et al. 1994). A slight increase in fibre cross-sectional area has constantly engaged where an animal stands for 18–22 h/day
been reported (Pérez et al. 2002; Del Corso et al. 2007). (Dallaire 1986). It is likely that the stimulation level given to the
There are, however, studies that show no changes in enzymes healthy horses in the present study may have been lower than their
and muscle fibre characteristics after similar stimulation normal work load and therefore not sufficient to induce any
(Eriksson et al. 1981; Arvidsson et al. 1986; Suetta et al. significant changes in muscle characteristics.
2004, 2008). The influence of NMES on muscle phenotype One of the limitations of NMES is the lack of evidence-based
depends primarily on the total number of impulses delivered and knowledge on how to maximise elicited torque output and to
is less dependent on the stimulation frequency (Salmons 2009). quantify optimal parameter settings. It has been indicated that an
The fact that neither fibre type and fibre area changes nor increase in current amplitude and pulse duration increases both
any alterations in enzymes were observed in the present study the maximum voluntary isometric torque, as well as the
may be related to the fact that NMES was used for 4 weeks in percentage of muscle group activated (Han et al. 2007; Gorgey
contrast to the longer durations employed in the previously and Dudley 2008). However, a rise of stimulus duration was
described studies. connected to an increase in patient discomfort (Kaczmarek et al.
An important methodological question is whether the muscle 2009). The stimulation characteristics of the present NMES
specimens obtained with the biopsy needle had actually been protocol were selected according to previous recommendations
activated. The depth of biopsy corresponded to the depth taken in (Hainaut and Duchateau 1992). It was chosen to mimic strength
human studies on m. quadriceps, which shows that a depletion of training used in clinical practices. It is generally accepted
glycogen and phosphagen stores occurs in the muscle after that the skin produces resistance to current flow by patient
electrical stimulation (Eriksson et al. 1981; Söderlund et al. 1992). dependent capacitive impedance (Dorgan and Reilly 1999).
Further, the evaluation with diagnostic ultrasound on the Therefore, the current intensity was individually set in
anaesthetised horse showed a clear visible contraction in the order to create the comparable highest work load and muscle
muscles at the depth of the muscle biopsy, thus indicating muscle contraction possible, without causing serious discomfort. If the
activation. The intensity used on the anaesthetised horse produced protocol had used the same intensity for each horse, there had
contractions of the same degree as those in standing horses, been a major risk of having some horses not showing any
estimated by visualisation and palpation. muscle contractions and some experiencing discomfort during
Training studies on horses show that changes can occur in fibre the stimulation.
characteristics and oxidative capacity in muscles, evaluated by On the basis of present results, it may be of little clinical use
muscle biopsies taken at the same depth as in the present study. No to stimulate a healthy horse less than according to the
changes in fibre type composition but an increase in CS activity and protocol described. In conclusion, healthy horses tolerated the
a decrease in type II A fibre area was seen after 5 weeks training NMES protocol used in the present study and no changes in
(Essén-Gustavsson et al. 1989). Fibre type changes with a muscle characteristics were seen after 4 weeks. If muscle
reduction in type II X fibres and a concomitant increase in type II A adaptations occur after more intense and/or longer stimulation
fibres, as well as an increase in oxidative capacity and glycogen periods needs to be investigated in future studies and also if
levels has been shown in horses after 3 months of endurance there is an effect of NMES in rehabilitation of horses with
training (Serrano et al. 2000). This indicates that changes in fibre muscle hypotrophy.
© 2010 EVJ Ltd
A. Bergh et al. 675

Acknowledgements Herrero, J.A., Izquierdo, M., Maffiuletti, N.A. and Garcia-López, J. (2006)
Electromyostimulation and plyometric training effects on jumping and sprint time.
Int. J. Sports Med. 27, 533-539.
The authors wish to express their sincere gratitude to AB Trav och
Kaczmarek, P., Huber, J., Lisinski, P., Witkowska, A. and Kasinski, A. (2009)
Galopp (ATG) for financial support, Cefar Medical AB for the use Investigation of the relationship between stimulus parameters and a human muscle
of equipment, Dr Nostell for taking the muscle biopsies and Dr contraction force during stimulation of the gastrocnemius muscle. Artif. Organs.
Uhlhorn for ultrasound evaluation. 34, 1525-1594.
Karlström, K., Essén-Gustavsson, B. and Lindholm, A. (1994) Fibre type distribution,
capillarization and enzymatic profile of locomotor and nonlocomotor muscles of
Manufacturers’ addresses horses and steers. Acta Anat. 151, 97-106.
Lake, D.A. (1992) Neuromuscular electrical stimulation - An overview and its
1
Cefar Medical AB, Lund, Sweden. application in the treatment of sports injuries. Sports Med. 13, 320-336.
2
Dixons surgical instruments Ltd, Wickford, Essex, UK. Laughman, R.K., Youdas, J.W., Garrett, T.R. and Chao, E.Y.S. (1983) Strength
3
Scan-Beam, Hadsun, Denmark. changes in the normal quadriceps femoris muscle as a result of electrical
4
Scandivet AB, Enköping, Sweden.
stimulation. Phys. Ther. 63, 494-499.
Lindholm, A. and Piehl, K. (1974) Fibre composition, enzyme activity and
References concentrations of metabolites and electrolytes in muscles of Standardbred horses.
Acta vet. Scand. 15, 287-309.

Arvidsson, I., Arvidsson, H., Eriksson, E. and Jansson, E. (1986) Prevention of Lowry, O.H. and Passonneau, J.V. (1972). In: A Flexible System of Enzymatic
quadriceps wasting after immobilization: An evaluation of the effect of electrical Analysis, Academic Press, New York. pp 175.
stimulation. Orthop. 9, 1519-1528. McGowan, C.M., Stubbs, N.C. and Jull, G.A. (2007) Equine physiotherapy: a
Bax, L., Staes, F. and Verhagen, A. (2005) Does neuromuscular electrical stimulation comparative view of the science underlying the profession. Equine vet. J. 39, 90-94.
strengthen the quadriceps femoris? A systematic review of randomised controlled Nuhr, M.J., Crevenna, R., Gohlsch, B., Bittner, C., Pleiner, J., Wiesinger, G., Fialka-
trials. Sports Med. 35, 191-212. Moser, V., Quittan, M. and Pette, D. (2003) Functional and biochemical properties
Brooke, M.H. and Kaiser, K.K. (1970) Muscle fiber type: How many and what kind? of chronically stimulated human skeletal muscle. Eur. J. appl. Physiol. 89, 202-208.
Arch. Neuro. 23, 369-379. Nuhr, M.J., Pette, D., Berger, R., Quittan, M., Crevenna, R., Huelsman, M., Wiesinger,
Carrol, T.J., Herbert, R.D., Munn, J., Lee, E. and Gandevia, S.C. (2006) Contralateral G.F., Moser, P., Fialka-Moser, V. and Pacher, R. (2004) Beneficial effects of
effect of unilateral strength training: evidence and possible mechanisms. J. appl. chronic low-frequency stimulation of thigh muscles in patients with advanced
Physiol. 101, 1514-1522. chronic heart failure. Eur. Heart J. 25, 136-143.

Colson, S.S., Martin, A. and Van Hoecke, J. (2009) Effects of electrostimulation versus Parker, M.G., Bennett, M.J., Hieb, M.A., Hollar, A.C. and Roe, A.A. (2003) Strength
voluntary isometric training on elbow flexor muscle strength. J. Electromyogr. response in human femoris muscle during 2 neuromuscular electrical stimulation
Kinesiol. 19, 311-319. programs. J. Orthop. Sports Phys. Ther. 33, 719-726.

Dallaire, A. (1986) Rest behaviour. Vet. Clin. N. Am.: Equine Pract. Behav. 2, 591-607. Pérez, M., Lucia, A., Rivero, J.L., Serrano, A.L., Calbet, J.A.L., Delgado, M.A. and
Chicharro, J.L. (2002) Effect of transcutaneous short-term electrical stimulation
Del Corso, S., Nápolis, L., Malaguti, C., Gimenes, A.C., Albuquerque, A., Nogueira, on m. vastus lateralis characteristics of healthy young men. Pflugers Arch. 443,
C.R., De Fuccio, M.B., Pereira, R.D., Bulle, A., McFariane, N., Nery, L.E. and 866-874.
Neder, J.A. (2007) Skeletal muscle structure and function in response to electrical
stimulation in moderately impaired COPD patients. Respir. Med. 101, 1236- Requena-Sánchez, B., Padial Puche, P. and González-Badillo, J.J. (2005) Percutaneous
1243. electrical stimulation in strength training an update. J. Strength Cond. Res. 19,
438-448.
Delitto, A. and Snyder-Mackler, L. (1990) Two theories of muscle strength
augmentation using percutaneous electrical stimulation. Phys. Ther. 70, 158-164. Rivero, J.L. and Serrano, A.L. (1999) Skeletal myosin heavy chain composition and
carriage training. Equine vet. J., Suppl. 30, 318-323.
Dorgan, S.J. and Reilly, R.B. (1999) A model for human skin impedance during surface
functional neuromuscular stimulation. IEEE Trans. Rehab. Eng. 7, 341-348. Ronéus, M., Essén-Gustavsson, B., Lindholm, A. and Persson, S.G. (1992) Skeletal
muscle characteristics in young trained and untrained standardbred trotters.
Eriksson, E., Häggmark, T., Kiessling, K.H. and Karlsson, J. (1981) Effect of electrical Equine vet. J. 24, 292-294.
stimulation on human skeletal muscle. Int. J. Sports Med. 2, 18-22.
Salmons, S. (2009) Adaptive changes in electrically stimulated muscle: A framework
Essén, B., Lindholm, A. and Thornton, J. (1980) Histochemical properties of muscle for the design of clinical protocols. Muscle Nerve. 40, 918-935.
fibre types and enzyme activities in skeletal muscles of Standardbred trotters of
different ages. Equine vet. J. 12, 175-180. Serrano, A.L., Quiroz-Rothe, E. and Rivero, J.L. (2000) Early and long-term changes
of equine skeletal muscle in response to endurance training and detraining.
Essén-Gustavsson, B., Karlström, K. and Lindholm, A. (1984) Fibre types, enzyme Pflugers Arch. 441, 263-274.
activities and substrate utilisation in skeletal muscles of horses competing in
endurance rides. Equine vet. J. 16, 197-202. Söderlund, K., Greenhaff, P.L. and Hultman, E. (1992) Energy metabolism in type I
and type II human muscle fibres during short term electrical stimulation at
Essén-Gustavsson, B., McMiken, D., Karlström, K., Lindholm, A., Persson, S. and different frequencies. Acta Physiol. Scand. 144, 15-22.
Thornton, J. (1989) Muscular adaptation of horses during intensive training and
detraining. Equine vet. J. 21, 27-33. Suetta, C., Aagaard, P., Rosted, A., Jakobsen, A.K., Duus, B., Kjaer, M. and
Magnusson, S.P. (2004) Training-induced changes in muscle CSA, muscle
Gauthier, J.M., Thériault, B., Thériault, G., Gélinas, Y. and Simeneau, J.A. (1992) strength, EMG, and rate of force development in elderly subjects after long
Electrical stimulation induced changes in skeletal muscle enzymes of men and unilateral disuse. J. appl. Physiol. 97, 1954-1961.
women. Med. Sci. Sports Exerc. 24, 1252-1256.
Suetta, C., Andersen, J.L., Dalgas, U., Berget, J., Koskinen, S., Aagaard, P.,
Gibson, J.N., Smith, K. and Rennie, M.J. (1988) Prevention of disuse muscle atrophy Magnusson, S.P. and Kjaer, M. (2008) Resistance training induces qualitative
by means of electrical stimulation: Maintenance of protein synthesis. Lancet 1, changes in muscle morphology, muscle architecture, and muscle function in
767-770. elderly postoperative patients. J. appl. Physiol. 105, 180-186.
Gondin, J., Guette, M., Ballay, Y. and Martin, A. (2006) Neural and muscular changes Thériault, R., Thériault, G. and Simoneau, J.A. (1994) Human skeletal muscle
to detraining after electrostimulation training. Eur. J. appl. Physiol. 97, 165-173. adaptation in response to chronic low-frequency electrical stimulation. J. appl.
Gorgey, A.S. and Dudley, G.A. (2008) The role of pulse duration and stimulation Physiol. 77, 1885-1889.
duration in maximizing the normalized torque during neuromuscular electrical Vanderthommen, M. and Duchateau, J. (2007) Electrical stimulation as a modality to
stimulation. J. Orthop. Sports Phys. Ther. 38, 508-516. improve performance of the neuromuscular system. Exerc. Sports Sci. Rev. 35,
Hainaut, K. and Duchateau, J. (1992) Neuromuscular electrical stimulation and 180-185.
voluntary exercise. Sports Med. 14, 100-113. Wigerstad-Lossing, I., Grimby, G., Jonsson, T., Morelli, B., Peterson, L. and
Han, T.R., Kim, D.Y., Lim, S.J. and Lee, K.J. (2007) The control parameters within the Renström, P. (1988) Effects of electrical muscle stimulation combined with
therapeutic range in neuromuscular electrical stimulation. Int. J. Neurosci. 117, voluntary contractions after knee ligament surgery. Med. Sci. Sports Exer. 20,
107-119. 93-98.

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