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Differences in electrical stimulation thresholds between men and women.

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Differences in Electrical Stimulation
Thresholds between Men and Women
Nicola A. Maffiuletti, PhD,1 Azael J. Herrero, PhD,2 Marc Jubeau, PhD,3 Franco M. Impellizzeri, MSc,1
and Mario Bizzini, MSc, PT1
Objective: Surface electrical stimulation (ES) of skeletal muscle is used in a variety of clinical settings in healthy and unhealthy
subjects of both sexes. Although women generally present larger amounts of subcutaneous adipose tissue than men, which could
limit current flow to the stimulated muscle, sex-related differences in ES current levels have not been clearly demonstrated to
date. We report data from healthy men and wom
Methods: Sensory (current perception), motor (minimal knee extension torque production), and supramotor thresholds (10% of
the maximal voluntary knee extension torque) and perceived pain during surface ES of the quadriceps femoris muscle were
investigated in 40 healthy volunteers (20 men, 20 women).
Results: Sensory threshold was lower in women than in men (⫺43%; p ⬍ 0.001). Similarly, female muscles required lower
current amplitudes to attain the supramotor threshold (⫺17%; p ⬍ 0.01). The Visual Analogue Scale pain score was significantly greater in women than in men at motor threshold (⫹112%; p ⬍ 0.01) but not at supramotor threshold (⫹36%; p ⬎
0.05).
Interpretation: Collectively, our data demonstrate higher sensory and supramotor excitability to surface ES in female subjects
and provide further evidence for a neurophysiological explanation for more pronounced pain perception in women. These
observations may help clinicians to better understand the sex-specific response to ES and to design more rational stimulation
treatments with the ultimate goal of optimizing patient care and safety.
Ann Neurol 2008;63:507–512
Surface electrical stimulation (ES) of skeletal muscle
has several clinical applications, including restoration/
improvement of muscle function (eg, in neurorehabilitation)1 and pain management.2,3 Depending on treatment objectives, ES can be applied with a variety of
protocols and parameters. Low-amplitude currents are
adopted for stimulation of sensory nerves. At these current levels, ES is perceived by the subject through somatic sensory receptors mainly located in cutaneous
and subcutaneous tissues.4 When current amplitude is
increased above sensory levels, an increasing number of
efferent terminal axon branches,5 in addition to myelinated afferents, are excited. This results in contractile
protein interaction. At these high current levels, fat
cells, located between the skin and the sarcolemma, inevitably limit current diffusion to the targeted muscle.6
Individual current levels are determined on an empirical basis by clinicians and practitioners.7 Men are
generally considered to be more electrically excitable
than women,8 because the former have proportionately
more muscle mass and less adipose mass.9 However, to
our knowledge, few or no data exist regarding sex differences in ES current levels. Because men and women
can respond to ES differently and would therefore require different current doses to optimize treatment effectiveness, it is important to determine the influence
of sex on ES thresholds and perceived pain. The main
objective of this study was to examine sex differences in
electrical sensory, motor, and supramotor thresholds
with associated pain scores. We selected the quadriceps
femoris because it is the muscle most often stimulated.10
From the 1Neuromuscular Research Laboratory, Schulthess Clinic,
Zurich, Switzerland; 2Faculty of Health Sciences, European University Miguel de Cervantes, Valladolid, Spain; and 3Institut National
de la Sante et de la Recherche Médicale U887, University of Burgundy, Dijon, France.
Published online Feb 25, 2008, in Wiley InterScience
(www.interscience.wiley.com). DOI: 10.1002/ana.21346
Received Aug 28, 2007, and in revised form Dec 12. Accepted for
publication Jan 2, 2008.
Subjects and Methods
Subjects
Forty healthy volunteers (20 men, 20 women) without any
known orthopedic, neuromuscular, or cardiovascular problems participated in this study (Table 1). Subjects were recruited from the Burgundy University (Dijon, France) community. The majority of them were graduate students (85%
of women, 80% of men), French mother tongue (85% of
both women and men), and residents in urban or semiurban
areas of Dijon at the time of the study (100% of women,
Address correspondence to Dr Maffiuletti; Neuromuscular Research
Laboratory, Schulthess Clinic, Lengghalde 2, 8008 Zurich, Switzerland. E-mail: nicola.maffiuletti@kws.ch
© 2008 American Neurological Association
Published by Wiley-Liss, Inc., through Wiley Subscription Services
507
Table 1. General Characteristics (means ⴞ Standard
Deviation) of the Experimental Subjects by Sex
Characteristics
Men
(n ⴝ 20)
Women
(n ⴝ 20)
Age (yr)
27.3 ⫾ 4.7
25.6 ⫾ 4.5
Height (m)
1.79 ⫾ 0.07
1.68 ⫾ 0.06a
Body mass (kg)
75.8 ⫾ 12.7
60.9 ⫾ 8.1a
Femur length (cm)
45.4 ⫾ 2.6
43.1 ⫾ 1.9a
Thigh circumference
(cm)
54.2 ⫾ 3.7
51.2 ⫾ 4.1
Skinfold thickness
(mm)
6.9 ⫾ 2.9
22.0 ⫾ 5.4a
Quadriceps crosssectional area
(cm2)
77.1 ⫾ 6.3
53.1 ⫾ 8.4a
301.7 ⫾ 52.8
176.0 ⫾ 44.9a
MVC torque (Nm)
a
p ⱕ 0.006 different from men.
MVC ⫽ maximal voluntary contraction.
95% of men). None of them had previously engaged in systematic ES training. The local ethical committee approved
the study, and written informed consent was always obtained. The study was conducted according to the Declaration of Helsinki.
Protocol
Subjects were asked not to take part in vigorous physical activity for 2 days before their test date. On arrival at the laboratory, the dominant lower extremity was determined by
asking subjects which limb they preferred to use when kicking a ball. All the assessments were subsequently performed
on this limb.
Measurements
First, femur length, thigh circumference, and skinfold thickness were measured while the subject was seated with an angle of 90 degrees at the hip and knee joints. Femur length
was measured from the greater trochanter to the lateral epicondyle of the knee. Thigh circumference was obtained at
half of femur length while the thigh muscles were relaxed.
Femur length and thigh circumference were measured to the
nearest 1mm with a tape measure. Skinfold thickness was
measured using a commercially available caliper (Harpenden;
British Indicators, West Sussex, United Kingdom) at two
different sites: half of femur length on the anterior aspect of
the thigh, and distal one-third of femur length on the lateral
aspect of the thigh (ie, under the stimulating electrode; see
later). All circumferences and skinfolds were the average of
two measurements (same observer). Quadriceps crosssectional area was estimated according to the following formula: (2.52 ⫻ thigh circumference [in cm]) ⫺ (1.25 ⫻
skinfold thickness at half of femur length [in mm]) ⫺
45.13.11
Subsequently, subjects were positioned into the chair of an
isokinetic device with the hip at 90 degrees and the knee
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April 2008
joint at 60 degrees of flexion. In these conditions, electrical
sensory, motor, and supramotor thresholds with the associated pain scores (see later) were quantified at two experimental frequencies. Isometric knee extension torque was continuously recorded throughout the testing session by means of
an isokinetic dynamometer (Biodex, Shirley, NY). Torque
signal was fed directly from the dynamometer into a 16-bit
A/D converter, then into a computer sampling at 1,000Hz
using Tida software (Tida, Heka Elektronik, Lambrecht/
Pfalz, Germany). Weight of the tested limb was assessed by
the dynamometer to allow torque to be corrected for that
resistance. The dynamometer lever arm was attached 2 to
3cm above the lateral malleolus by using a strap. Extraneous
movements of the upper body were limited by two crossover
shoulder harnesses and a belt across the abdomen.
The quadriceps femoris muscle was stimulated using a
battery-powered ES unit (Compex Sport-P; Medicompex SA,
Ecublens, Switzerland) and two surface electrodes. One electrode (5 ⫻ 10cm) was placed on the proximal (anterior) aspect of the quadriceps femoris muscle (5cm below the femoral triangle), and the other electrode (5 ⫻ 5cm) was
positioned on the distal third of femur length (lateral aspect
of the thigh), over the vastus lateralis muscle belly. An electroconductive gel was consistently applied between the electrodes and skin to minimize impedance. We used the following ES parameters: 400-microsecond pulse duration, 10/5second on/off ratio, and 2 different experimental frequencies,
randomly presented. Frequencies of 10 and 75Hz were considered representative of low-frequency (LF) ES,12 which is
generally used to mimic endurance exercise,13 and highfrequency (HF) ES,14 which is generally adopted to mimic
resistance exercise.13 Following electrode positioning and instructions, current amplitude (in mA) was progressively increased by the investigator from zero to the following levels:
(1) sensory threshold (current perception), when the subject
indicated initial (lowest) perception of stimulus sensation
(tingling, itching, heat); and (2) motor threshold, when minimal knee extension torque was produced at the knee joint
(usually 5–10Nm). Current amplitude was increased until
one of the thresholds was reached at a rate of about 1mA/sec;
then it was reduced (approximately 3–5mA) and subsequently reincreased, to accurately determine each threshold
level. Rest periods of at least 30 seconds were provided between thresholds. Subjects were consistently asked to relax
during ES.
A standardized warm-up, consisting of 5 minutes of submaximal ES (frequency: 5Hz; pulse duration: 350 microseconds), to further familiarize the subjects with ES, and approximately 10 submaximal voluntary (isometric) contractions of
the knee extensor muscles (intensity range: 10 – 80% of the
estimated maximum strength) was completed. Then participants were asked to exert two maximal voluntary contractions (MVCs). Visual feedback and consistent verbal encouragement from the investigator were provided throughout the
maximal effort repetitions. Subjects were instructed to produce their maximal force (“hard”) without any concern for
the rate of force development. The duration of these contractions was approximately 5 seconds, and 60 seconds of
rest were interspersed between trials. A third trial was completed only if the difference between the first two MVCs was
greater than 5%. The average of the two highest MVCs was
retained.
After 10 minutes of passive recovery, the supramotor
threshold was determined by progressively increasing current
amplitude beyond motor threshold, until the stimulated
quadriceps produced a torque level of 10% of knee extension
MVC. Considering that there is no consensus on the minimal clinically useful contraction intensity using ES,15 this
relatively low force level was selected because it corresponds
to the stimulated quadriceps force that can be recorded by
almost all subjects (both male and female subjects) at the
beginning of their first ES session.15
Immediately after stimulations at motor and supramotor
thresholds, subjects were asked to place a vertical mark on a
horizontal line (100mm) to rate the pain intensity, that is,
Visual Analogue Scale (VAS) for pain.16 The scale therefore
ranges from 0 to 100mm, with the zero value representing
“no pain” and the 100 mm value representing “worst possible pain.”
Statistics
After check for normality, differences in age, anthropometric
characteristics, and MVC torque between men and women
were examined using a Student’s unpaired t test. A corrected
␣ level of p ⱕ 0.006 (0.05/8) was accepted as significant. A
two-factor analysis of variance (sex ⫻ frequency) was performed on thresholds (sensory, motor, and supramotor
thresholds) and on pain scores at motor and supramotor
thresholds. Repeated measures on the last factor were used. If
significant main effects or interactions were present, a
Tukey’s (honestly significant difference) post hoc test was
conducted. After correction for multiple comparisons (0.05/
5), the significance level was set at p ⱕ 0.01. The Pearson
product-moment correlation coefficients were calculated for
pairs of variables (thresholds vs anthropometric characteristics), and r values ⱖ 0.60 were considered to be acceptable
(with n ⫽ 40; ␣ ⫽ 0.01; ␤ ⫽ 0.05).17
Between-session reliability of ES thresholds and of the associated VAS scores at both HF and LF were assessed in a
group of 10 healthy men (age: 34 ⫾ 5 years; body mass:
Table 2. Summary of Two-Factor Analysis of
Variance Results for Electrical Stimulation
Thresholds and Pain Scores
Sex Effect
p
Frequency
Effect
Threshold
F
F
p
Sensory threshold
Motor threshold
Supramotor
threshold
VAS motor
threshold
VAS supramotor
threshold
27.7
0.0
7.3
⬍0.001 22.4
NS
79.6
⬍0.01 121.4
7.5
⬍0.01
5.2
NS
3.1
NS
29.3
⬍0.001
⬍0.001
⬍0.001
⬍0.001
No significant sex ⫻ frequency interaction was found.
VAS ⫽ visual analogue scale; NS ⫽ non significant.
Fig 1. (A) Current amplitude at sensory threshold, (B) current
amplitude at supramotor threshold, and (C) Visual Analogue
Scale (VAS) scores at motor threshold by sex. Data (mean and
standard error of the mean) are collapsed across frequencies.
***p ⬍ 0.001 different between men (gray bars) and women
(white bars). **p ⬍ 0.01 different between men and women.
77 ⫾ 13kg; test-retest interval: 7 days). Average intraclass
correlation coefficients for the three thresholds (HF: 0.93;
LF: 0.86) and for the two VAS scores (HF: 0.90; LF: 0.91)
were high and demonstrated, according to standard definition,18 excellent test-retest reliability.
Results
Body height, body mass, femur length, skinfold thickness, estimated cross-sectional area, and MVC torque
differed significantly between men and women (see Table 1).
Electrical Stimulation Thresholds
Two-factor analysis of variance results are shown in
Table 2. Motor threshold was not significantly affected
by sex, whereas sensory ( p ⬍ 0.001; Fig 1A) and supramotor ( p ⬍ 0.01; see Fig 1B) thresholds were lower
in women than in men (⫺43 and ⫺17%). Interestingly, the lowest sensory thresholds were observed in
those subjects with the largest skinfold thicknesses and
vice versa (r ⫽ ⫺0.71; p ⬍ 0.001; Fig 2). The slope of
the regression lines did not differ significantly between
men and women ( p ⫽ 0.32; ␩2 ⫽ 0.03, analysis of
covariance) probably because of the small sample size
and low r value (see Fig 2). Moreover, the lowest sensory currents were observed in those subjects with the
smallest cross-sectional area and vice versa (r ⫽ 0.65;
p ⬍ 0.001). For the motor and supramotor thresholds,
no correlation coefficients greater than 0.6 were found.
All the ES thresholds were significantly lower at HF
than at LF, that is, ⫺19% for sensory (HF: 3.8 ⫾
1.7mA; LF: 4.6 ⫾ 1.9mA), ⫺28% for motor (HF:
22.2 ⫾ 5.1mA; LF: 30.6 ⫾ 9.6mA), and ⫺40% for
supramotor threshold (HF: 38.8 ⫾ 9.5mA; LF:
64.9 ⫾ 18.9mA). No significant sex ⫻ frequency interaction was observed.
Pain Scores
VAS score at motor threshold (see Fig 1C) was significantly higher in women than in men (⫹112%). Pain
Maffiuletti et al: Electric Current Thresholds
509
Fig 2. The lowest sensory thresholds were observed in those
subjects with the largest skinfold thicknesses and vice versa
(r ⫽ ⫺0.71; p ⬍ 0.001). The slope of the regression lines
did not differ significantly between men (solid circles) and
women (open circles) ( p ⫽ 0.32, analysis of covariance).
score (range, 0 –100mm) at supramotor threshold was
higher at LF (66 ⫾ 28mm) than at HF (44 ⫾ 31mm)
(⫹34%; p ⬍ 0.01). No significant sex ⫻ frequency
interaction was observed.
Discussion
The main findings of this study were that electrical
sensory and supramotor thresholds were significantly
lower in women than in men; that is, female subjects
perceived the current (sensory threshold) and produced
a predetermined submaximal (10% MVC) torque output (supramotor threshold) with lower current amplitudes. Our findings also showed that self-reported pain
at motor threshold was significantly greater in women
than in men, and that LF ES evoked more pain than
HF ES at supramotor threshold.
In this investigation, sensory threshold was defined
as the lowest stimulus sensation perceived by the subjects. This painless sensation was commonly described
as tingling, itching, and superficial heat. Although
these sensations may be mediated by both A␤ and A␦
fibers,19 it has been suggested that detection-threshold
levels of stimulation predominantly activate largediameter A␤ afferents.20,21 Therefore, somatic sensory
receptors activated at this first threshold would mainly
include encapsulated nerve endings (eg, Pacinian corpuscles and Merkel disks) located in cutaneous and
subcutaneous tissues.4 Our female subjects had a threefold larger skinfold thickness than men in the thigh
area beneath the stimulating electrodes. Interestingly,
women demonstrated significantly lower sensory
thresholds both at LF and HF, which confirms the
greater female sensitivity for electrical,22 mechanical,
and thermal stimuli applied at the sensory level.23 The
lowest sensory currents were observed in those subjects
with the largest skinfold thicknesses (mainly women),
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therefore suggesting a link between subcutaneous adipose tissue mass and sensory excitability. This allows us
to speculate that the number and/or sensitivity of cutaneous and subcutaneous receptors activated by
detection-threshold current could differ between men
and women.
Increasing current amplitude beyond the sensory
threshold results in the excitation of efferent terminal
axon branches,5 in addition to myelinated afferents,
which, in turn, triggers visible muscle contractions. Because subcutaneous fat thickness, which limits current
propagation between the electrode and the efferent axons, is greater in women than in men,24 we expected
lower motor and supramotor excitability in the former
subjects. Surprisingly, we observed insignificant differences in motor threshold between sexes, and supramotor threshold was even significantly lower in the female
group. Considering that both motor and supramotor
threshold assessments were based on torque recordings,
we speculate that two mechanisms could explain, at
least in part, the observed results. First, central contributions to contractions evoked by ES, such as ESspecific brain activation (dose–response) in specific sensorimotor regions (possibly related to pain),25 and/or
spinal motoneuron recruitment via electrically evoked
sensory volleys (which is consistent with the development of persistent inward currents in spinal motoneurons or interneurons),26 would have been greater in
women, therefore promoting central in addition to peripheral torque development.26 Second, because electrode area was the same for all subjects (25cm2),
whereas quadriceps cross-sectional area was significantly larger in men (approximately 77cm2) than in
women (approximately 53cm2), the relative area of
stimulated muscle was inevitably greater in the female
sample. This would mean that, for a given dose of electric current, a larger portion of the quadriceps muscle
(relative to total muscle area) can be activated in
women, particularly in those subjects presenting the
smallest muscle cross-sectional areas. The contribution
of these mechanisms would have been greater at higher
current levels, therefore accounting for sex-related differences at supramotor but not at motor threshold.
Women reported significantly higher pain scores
than men at the motor threshold. Because of the large
interindividual variability, sex differences at the supramotor level did not reach significance ( p ⫽ 0.086).
However, four female subjects (20%), but no men,
were unable to attain supramotor threshold at LF because of intolerable pain. These findings confirm that
noxious electrical stimuli are perceived as more painful
by healthy women than by healthy men, in line with
previous research.27 For example, male subjects have
been shown to have higher pain thresholds than their
female peers and greater electrically induced pain tolerance,28 even if some investigators did not observe
these sex differences.27 Although pain was not the
main focus of this study, it is interesting to remember
that thermal29 and acute pain19 sensations associated to
surface ES are mediated by medium-diameter, lightly
myelinated fibers (A␦) that innervate the skin (free
nerve endings).20,21 Interestingly, greater epidermal
nerve fiber density has recently been observed in
women when compared with their male counterparts,30,31 which would explain, at least in part, their
greater sensitivity to painful stimuli. Our findings add
to those obtained in recent skin biopsy and cadaveric
studies,30,31 and favor a neurophysiological rather than
a psychological or sociocultural explanation for more
pronounced pain perception in female individuals.
We demonstrated significant influences of frequency
modulation on ES thresholds and on the associated
self-reported pain for both men and women. The finding that motor and supramotor thresholds were significantly lower at 75Hz (fused tetanus) than at 10Hz
(unfused tetanus) may be explained by the fact that
torque is essentially derived from a single pulse in the
latter condition. This inevitably resulted in significantly
greater pain scores at LF than at HF for the supramotor threshold. At the motor threshold, frequency effect
was significant only before correction for multiple
comparisons ( p ⫽ 0.028). The fact that pain response
was reduced with increasing stimulation frequency in
both sexes weighs against C-fiber involvement
(“windup” phenomenon)32 in surface ES.20,21 Pain levels associated with single shocks need to be determined
to rule out the possibility of windup occurrence with
this ES paradigm.
Further research is also required to investigate the
present ES thresholds: (1) at torque levels greater than
10% MVC, (2) on muscles other than the quadriceps
femoris, (3) on male and female subjects having wide
ranges of subcutaneous fat, as well as the effect of (4)
electrode size, (5) skin temperature, (6) anthropometrical factors,33 and (7) menstrual cycle34 on electric current thresholds.
Our findings may help clinicians and practitioners
better understand the sex-specific response to surface
ES (current thresholds and pain) and to design more
rational stimulation strategies. Because the choice of
optimal current amplitudes is paramount to the effectiveness of ES treatments, neurorehabilitation settings
in particular, we recommend that clinicians consider
that women may present lower current thresholds than
men, particularly for sensory level stimulation. Our results also provide further insights into the neurophysiological mechanisms underlying ES of intact human
muscles. Within the limits of this study, female quadriceps femoris muscle appears to be more electrically
excitable than male quadriceps, contrary to what is
generally believed.
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