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Journal of Electromyography and Kinesiology 13 (2003) 305–318

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Surface electromyography assessment of back muscle intrinsic


properties
Christian Larivière a,∗, A. Bertrand Arsenault b, Denis Gravel b, Denis Gagnon c,
Patrick Loisel d
a
Occupational Health and Safety Research Institute Robert-Sauvé, Montreal, Quebec, Canada
b
School of Rehabilitation, University of Montreal, Montreal, Quebec, Canada
c
Department of Kinanthropology, University of Sherbrooke, Sherbrooke, Quebec, Canada
d
Department of Surgery, Faculty of Medicine, University of Sherbrooke, Sherbrooke, Quebec, Canada

Received 2 October 2002; received in revised form 27 November 2002; accepted 29 November 2002

Abstract

The purpose of this study was to assess (1) the reliability and (2) the sensitivity to low back pain status and gender of different
EMG indices developed for the assessment of back muscle weakness, muscle fiber composition and fatigability. Healthy subjects
(men and women) and chronic low back pain patients (men only) performed, in a static dynamometer, maximal and submaximal
static trunk extension tasks (short and long duration) to assess weakness, fiber composition and fatigue. Surface EMG signals were
recorded from four (bilateral) pairs of back muscles and three pairs of abdominal muscles. To assess reliability of the different
EMG parameters, 40 male volunteers (20 controls and 20 chronic low back pain patients) were assessed on three occasions. Reliable
EMG indices were achieved for both healthy and chronic low back pain subjects when specific measurement strategies were applied.
The EMG parameters used to quantify weakness and fiber composition were insensitive to low back status and gender. The EMG
fatigue parameters did not detect differences between genders but unexpectedly, healthy men showed higher fatigability than back
pain patients. This result was attributed to the smaller absolute load that was attributed to the patients, a load that was defined
relative to their maximal strength, a problematic measure with this population. An attempt was made to predict maximal back
strength from anthropometric measurements but this prediction was prone to errors. The main difficulties and some potential sol-
utions related to the assessment of back muscle intrinsic properties were discussed.
 2003 Elsevier Science Ltd. All rights reserved.

Keywords: Low back pain; Back muscles; Fatigue; Recovery; Electromyography; Impairment evaluation; Reliability; Weakness; Dynamometry;
Muscle composition

1. Introduction muscles, namely their fiber composition, strength and


endurance. To fully understand these ‘muscle intrinsic
Chronic low back pain (CLBP) is associated with sev- properties’, the influence of some control mechanisms
eral anatomical or structural abnormalities such as atro- must be also considered. For example, muscle synergies
phy of muscle mass or alteration of muscle fiber [43,57] and co-contraction as well as sharing of moment across
characteristics and organizational abnormalities such as muscles will be discussed in this paper. The assessment
altered muscle coordination patterns [76,30], impaired of control mechanisms of trunk muscles is certainly a
proprioceptive abilities or slow psychomotor reaction field of research that needs developments to better under-
time [15]. The focus of the present paper was placed on stand the way the central nervous operates to compensate
the evaluation of some intrinsic properties of back for lumbar instability [60].
The alterations in the structure of back muscles might
lead to weakness and fatigability, two back muscle

Corresponding author. Tel.: +1-514-288-1551x217; fax: +1-514- impairments recognized as a potential cause of the recur-
288-6097. rent nature of LBP [43]. Muscle composition is usually
E-mail address: lariviere.christian@irsst.qc.ca (C. Larivière). assessed through biopsy techniques [43]. Back muscle

1050-6411/03/$ - see front matter  2003 Elsevier Science Ltd. All rights reserved.
doi:10.1016/S1050-6411(03)00039-7
306 C. Larivière et al. / Journal of Electromyography and Kinesiology 13 (2003) 305–318

strength is generally assessed under volitional effort present paper [22,37,39–41]. Different sub-samples of
using dynamometry, while endurance is quantified by subjects and tasks were analyzed in these studies. The
measuring the maximum time that the subject can hold reader is referred to the original articles for details con-
a given load. However, biopsy measurements are invas- cerning the inclusion–exclusion criteria and demo-
ive and maximal performance measurements (strength, graphic characteristics of each sub-sample. The number
endurance) depend heavily on psychological [20,29] fac- of subjects and specific analyses corresponding to each
tors and the capacity of subjects to activate all motor of these studies were summarized in the results section.
units [1]. Previous findings suggest that it may also be
possible to assess muscle weakness [10,55], muscle 2.1. Subjects and tasks
composition [24,35,77] and muscle fatigue [43] through
the use of surface electromyography (EMG). Healthy subjects (men and women) and male patients
The assessment of muscle intrinsic properties is poss- with a chronic low back pain (CLBP) syndrome were
ible only if the influence of control mechanisms is con- recruited. The healthy females (n = 13; age: 26 ± 4 yr;
sidered. This can be achieved with adequate standardiz- height: 1.67 ± 0.05 m; mass: 61 ± 7 kg) were similar in
ation of the measurement protocol, but previous studies age to the healthy males (n = 12; age: 27 ± 5 yr; height:
indicate that it is a difficult task. Some investigators 1.75 ± 0.05 m; mass: 74 ± 11 kg). Briefly, CLBP was
show poor reliability of EMG spectral variables for test- defined as a daily or almost daily lumbar or lumbosacral
ing the left–right difference between back muscles pain with or without proximal radicular pain (limited dis-
[62,69], or for estimating the rate of increase in back tally to the knees) for at least three months. Exclusion
muscle fatigue through the slope decay of the median or criteria for the healthy subjects (men and women) were
mean frequency [54]. This might be explained by the as follows: had back pain in the previous year or
variability in the electromyographic (EMG) signal exceeding one week; lost a working day because of back
caused by the variability of load-sharing between bilat- pain; and consulted for a back problem. All subjects
eral muscles [75]. This could be particularly true if varia- (healthy and CLBP) that went through a surgery of the
bility of load sharing increases with muscle fatigue and pelvis or spinal column were excluded.
back pain to minimize fatigue and pain symptoms. If this At the arrival in the laboratory, questionnaires about
is correct, it would explain the poor reliability results perception of functional disability (Oswestry question-
reported by the only reliability study on EMG fatigue naire [19]), pain intensity (10 cm visual analogue scale),
parameters involving CLBP subjects [54]. However, physical activity level [2] were self-administered and
most studies assessing back muscle function have not anthropometric measures were collected. The effect of
controlled the coupled lumbar moments (lateral bending, electromechanical delay was neglected in the compu-
axial rotation) during ‘purely sagittal’ extension efforts. tation of both NME EMG indices and MFT10–80. Each
This has often been identified as a possible cause of the electrode site was marked and the thickness of the sub-
alternating EMG activity or the uneven EMG activity cutaneous tissues was measured twice (left side electrode
between the left and right muscles of the erector spinae sites only) with a Harpenden skinfold caliper.
[3,44,64,72]. In an effort to further standardize previous The subjects performed, while standing in a dyna-
measurement protocols, our group developed a triaxial mometer (Fig. 1), different static trunk extension efforts
static dynamometer to control coupled lumbar moments using the L5/S1 extension and axial rotation moments
(lateral bending, axial rotation) during trunk extension (to be minimized) as visual feedback. The minimization
tasks [38] and then reduce the variability in EMG vari- of lateral bending moments with the use of an extra vis-
ables by potentially decreasing the load-sharing between ual feedback was not possible without interfering with
back muscles. The present paper summarizes results the extension task (too much visual feedback at a time).
obtained using this measurement protocol. The protocol followed the following sequence: two to
More specifically, the purpose of this study was to four submaximal contractions to become familiar with
assess (1) the reliability and (2) the sensitivity to low the visual feedback, two maximal voluntary contractions
back pain status and gender of different EMG indices (MVC), three 7 s ramps (0–100% MVC) and two static
developed for the assessment of back muscle weakness, trunk extension tasks at 75% MVC, that correspond to
muscle fiber composition and fatigability. Another a 30 s fatigue task and a 5 s contraction task to estimate
objective was to discuss the main difficulties related to the recovery. These two tasks were separated by a 60 s
the use of these indices and to propose some potential rest period. At the end of the measurement protocol, two
solutions. MVC trials were performed to obtain the maximal EMG
of abdominal muscles. A padded bar was fixed to the
2. Methods apparatus in front of the subject to stabilize the thorax
when producing trunk flexion or rotation efforts. Three
This section describes the general methodology used 4 s maximal efforts were produced consecutively in the
in the different articles that were summarized in the same trial: (1) flexion, (2) rotation to the left and (3)
C. Larivière et al. / Journal of Electromyography and Kinesiology 13 (2003) 305–318 307

Fig. 2. EMG recording and nomenclature used to identify the elec-


trode sites. The active bipolar electrodes were positioned bilaterally
on the multifidus at the L5 level (MU-L5-Left and MU-L5-Right),
iliocostalis lumborum at L3 (IL-L3-L and IL-L3-R), longissimus at L1
(LO-L1-L and LO-L1-R) and over the belly of the longissimus at the
T10 level (LO-T10-L and LO-T10-R) following the recommendations
of Defoa et al. [14] with regard to muscle fiber direction. A reference
silver-silver chloride electrode was positioned over the T8 spinous pro-
cess.

Fig. 1. Experimental setup. The dynamometer consists of a triaxial


force platform (Advanced Mechanical Technology Incorporated, peak L5/S1 extension moment was computed. For each
model MC6-6-1000) mounted on a steel frame that allows the stabiliz- ramp contraction, EMG RMS values of 250 ms windows
ation of the feet, knees and pelvis (details in [38]). The subjects stood at each 5% force level from 10 to 80% MVC were com-
in the dynamometer with the trunk erect and the knees straight. Trunk
extension was generated against a padded bar fixed on the surface of
puted and spectral analysis (512 points, Hanning window
the force platform and adjusted at the T4 level. processing, fast Fourier transform) was applied to extract
the corresponding median frequency (MF) values.
Finally, a series of 250 ms windows of EMG data, 75%
rotation to the right. At least two minutes of rest was overlapping, were taken from the data of the fatigue and
given between efforts except between the 75% MVC recovery tests and spectral analysis was applied to each
fatigue and recovery tasks (60 s rest). time-window to obtain the corresponding MF values.
Different EMG indices were then calculated (list of
2.2. Electromyography abbreviations in Table 1) as described below.

The EMG signals from four pairs of back muscles 2.3.1. Weakness EMG indices [37]
(Fig. 2) and three pairs of abdominal muscles were col- Back muscle weakness was assessed using the neuro-
lected (bandpass filter: 20–450 Hz; preamplification muscular efficiency (NME) concept which was defined
gain: 1000; sampling rate: 2048 Hz) with active surface as the slope of the relationship (quantified by linear
electrodes (Delsys Inc., MA). After the skin was shaved regression) between the extension moment at L5/S1 (Y
and abraded with alcohol, the electrodes on the back axis) and RMS (X axis) across the force levels (NME10–
muscles were positioned. Fig. 2 shows the selected 80). A second NME parameter was computed from the
muscles and the corresponding abbreviations. Electrodes MVC contraction as the ratio of the peak L5/S1 exten-
on the abdominal muscles (rectus abdominis, external sion moment to its RMS value (NMEmvc). More efficient
oblique and internal oblique) were positioned according muscle contractions are characterised by steeper slope
to McGill [50]. (NME10–80) and higher ratio (NMEmvc).

2.3. Data processing 2.3.2. Muscle composition EMG indices [37]


Back muscle composition was assessed by three EMG
For the best MVC contraction, the EMG root mean parameters presumably sensitive to muscle fiber compo-
square (RMS) value of a 250 ms window centered at the sition: (1) the slope (MFT10–80) and (2) the intercept
308 C. Larivière et al. / Journal of Electromyography and Kinesiology 13 (2003) 305–318

Table 1
List of abbreviations (by category) used to identify the EMG indices and recording sites (muscles)

EMG index Description (units)

Weakness EMG indices (neuromuscular efficiency)


NME10-80 Gradient (slope) of the linear relationship between the extension moment at L5/S1 (Y axis) and RMS (X axis) across
the force levels (ramp contractions)
NMEmvc Ratio of the peak L5/S1 extension moment to its RMS value (MVC contraction)
Muscle composition EMG indices
IMF75 Initial median frequency of the EMG power spectrum (intercept of time-series) at the start of the fatigue test (Hz)
IMFT10-80 Intercept of the linear relationship between the MF (Y axis) and the extension moment at L5/S1 (X axis) across the
force levels (ramp contractions)
MFT10-80 Gradient (slope) of the linear relationship between the MF (Y axis) and the extension moment at L5/S1 (X axis) across
the force levels (ramp contractions)
Fatigue and recovery EMG indices
IMF Initial median frequency of the EMG power spectrum (intercept of time-series) at the start of the fatigue test (Hz)
IMFrec Initial median frequency of the EMG power spectrum (intercept of time-series) at the start of the recovery test (Hz)
IRMS Initial EMG root mean square (intercept of time-series) at the start of the fatigue test (µV)
MFslp Gradient (slope of time-series) of the Median Frequency of the EMG power spectrum during the fatigue test (Hz/s)
REC Recovery of IMF (absolute value in Hz)
%REC Relative recovery of IMF (%)
RMSslp Gradient (slope of time-series) of the EMG root mean square during the fatigue test (µV/s)
EMG recording sites (muscles)
IL-L3-L & R Iliocostalis lumborum at the L3 level, left & right sides
LO-L1-L & R Longissimus at the L1 level, left & right sides
LO-T10-L & R Longissimus at the T10 level, left & right sides
MU-L5-L & R Multifidus at the L5 level, left & right sides

(IMFT10–80) of the relationship between the MF (Y axis) tions (NME10–80; MFT10–80; IMFT10–80) were averaged
and the extension moment at L5/S1 (X axis) across the across bilateral muscle pairs and the three ramps.
force levels (ramp contractions) as quantified by linear
regression, and (3) the intercept (IMF75) of the linear 2.4. Reliability assessment
regression applied to the time-series of MF (fatigue
contraction). Analyses of the power in different fre- Forty (20 healthy and 20 CLBP male subjects) were
quency bands (20–60, 60–120, 120–180, 180–240, 240– assessed on three sessions at least two days apart within
300 Hz) of the power spectrum were also examined a two-week period. The generalizability theory [67] was
between healthy and CLBP male subjects. used as a framework to estimate the reliability of EMG
indices and to estimate the reliability for various
2.3.3. Fatigue and recovery EMG indices [40] measurement designs. Reliability was assessed for all
Linear regression was applied to the time-series of EMG parameters, each group (healthy and CLBP male
RMS and MF to get their initial values or intercept subjects) and each muscle or muscle pair by the intra-
(IRMS, IMF) and to estimate their rate of change (slope class correlation coefficient (ICC) and standard error of
of their respective linear regression) corresponding to the measurement (SEM) expressed as a percentage of the
fatigue increase (RMSslp, MFslp). The lowest MFslp grand mean (across days) [37,40,41].
and the highest RMSslp among all muscles, correspond-
ing to the most fatigable muscle, were also retained as 2.5. Estimation of recovery time required after the
EMG fatigue indices. The same procedure (spectral fatigue test to perform a second fatigue trial
analysis, linear regression) was applied on the MF esti-
mates of the 75% MVC recovery test to compute the It was predicted from the reliability assessment of
corresponding IMF (IMFrec). Two recovery EMG indices EMG fatigue indices that the averaging of measures
(%REC and REC) were computed as illustrated in Fig. 3. across two fatigue tests performed within the same ses-
All the EMG indices described above were computed sion would increase the reliability by about 13% [40].
for each muscle (n = 8), all muscle pairs (mean of left However, enough rest between fatigue tests is required
and right homologous muscles), and for the back to allow a complete recovery. Thus, a study was conduc-
muscles as a whole (mean of all eight muscles). The ted to evaluate if rest intervals of 10 or 15 min allow
effect of electromechanical delay was neglected in the the back muscles to recover completely, from an EMG
computation of both NME EMG indices and MFT10–80. point of view, after performing a fatiguing contraction
Each EMG parameters computed from the ramp contrac- [41]. Twelve healthy males performed the fatigue trials
C. Larivière et al. / Journal of Electromyography and Kinesiology 13 (2003) 305–318 309

Fig. 3. Illustration of the computation of fatigue and recovery EMG indices based on median frequency (MF) estimates. The upper plots show
the L5/S1 extension moment during the 30 s fatigue (upper-left) and 5 s recovery (upper-right) contractions separated by a 60 s rest period. The
lower plots show the corresponding MF estimates for a given back muscle. The fatigue index is represented by the slope of the MF-time linear
relationship (lower-left plot). Two recovery indices were computed (lower-right plot): (1) the percent recovery of the IMFr (%REC), where IMFf
and IMFr represents the intercept of the linear regression equation computed from the fatigue and recovery MF time-series and FMFf the final MF
of the fatigue contraction MF time-series, and (2) the difference between IMFr and FMFf (REC).

(30 s contractions at 75% MVC) three times separated instant of the task. This was performed for the first and
successively by a 15 min (between trial 1 and 2) and a last 5 s of the fatigue test to quantify the effect of fatigue
10 min (between trial 2 and 3) rest period. on coactivity.

2.6. Assessment of abdominal coactivity during the


fatigue test 2.7. Prediction of back strength using anthropometric
data
The flexion moment produced by the antagonist
muscles (abdominals) during the extension fatigue test
was estimated for 22 healthy males [22]. The maximal The assessment of back muscle relative endurance (%
EMG of each back and abdominal muscle was computed maximal strength) requires the measurement of maximal
across the corresponding MVC contractions to normalize back strength which remains problematic with CLBP
EMG signals. A detailed lumbar spine model [8,51] was patients. A study was conducted to evaluate if a multiple
implemented to partition the L5/S1 joint moment regression equation using anthropometric measurements
between 54 muscle fascicles and estimate joint forces. could predict the back strength of healthy men subjects
An EMG-assisted by optimization (EMGAO) approach with accuracy [39]. Briefly, several anthropometric mea-
[7] was used to adjust EMG predicted muscle forces to sures were collected on 42 healthy men. The possible
balance the joint moment. For all back muscles, the aver- anthropometric correlates to back strength were ident-
age EMG signals recorded during the first 5 s of the 30 ified based on previous literature and included global
s fatigue test were used as constant values to compensate indices of body size, specific measures of the trunk seg-
for fatigue progression. To estimate the degree of trunk ment and limbs, and derived variables related to body
muscle coactivity produced by the abdominals, all the composition and muscularity. Stepwise multiple linear
individual muscle moments were summed signwise.
regression analysis was performed to predict back
Coactivity was resolved axis by axis at each instant of
strength with age and 26 anthropometric variables as
the fatigue cycle by comparing the net L5/S1 moment
independent variables.
about a given axis to the signed sum of the individual
muscle moments about the same axis. The sum of all
the individual muscle moments opposed to the net joint
moment about a given axis represented coactivity at this
310 C. Larivière et al. / Journal of Electromyography and Kinesiology 13 (2003) 305–318

3. Results

3.1. Assessment of weakness

3.1.1. Reliability
The NME parameters (NME10–80 and NMEmvc) aver-
aged across bilateral muscles showed good to excellent
reliability results for both healthy and CLBP groups
(ICCs from 0.65 to 0.96; SEMs from 12 to 25%).

3.1.2. Sensitivity
The healthy subjects showed higher (t-test, P =
0.004) peak extension moment at L5/S1 (n = 20; 252
Nm, SD: 40) than CLBP subjects (n = 20; 202 Nm, SD:
62) and men generated a significantly (P = 0.000) higher Fig. 4. Median frequency (MF in Hz) as a function of the L5/S1
extension moment (n = 12; 274 Nm, SD: 38) than extension moment (Nm) during a 0–100% ramp contraction of the
women (n = 13; 191 Nm, SD: 26). However, only the multifidus muscles (MU-L5). Each curve represents the mean of all
NMEmvc index showed significant differences (P ⱕ healthy males (n = 20) and all CLBP (n = 20) subjects. The non-linear
0.05) between these groups. These differences occurred appearance of both curves and their apparent difference (not statisti-
cally significant) were observed only for this muscle group.
for the MU-L5 (healthy vs CLBP subjects) and for the
LO-L1 (men vs women) muscles. However, higher
values (more efficient muscle contractions) were involving the averaging of multiple measurements sites
obtained for the CLBP and female groups, which was can, at times, increase the reliability to an acceptable
in opposition to our expectations. level. Only the EMG indices based on MF estimates
(MFslp) showed acceptable reliability. Reliable EMG
3.2. Assessment of muscle composition indices were achieved for both healthy and CLBP sub-
jects in particular conditions, namely when (1) electrodes
3.2.1. Reliability are positioned on medial back muscles (MU-L5 level
The IMFT10–80 and IMF75 parameters showed excel- and LO-L1) instead of more laterally positioned back
lent reliability for both groups (ICCs from 0.68 to 0.91; muscles such as IL-L3 and LO-T10 and (2) measures
SEMs ⱕ10%) while modest results were achieved for were averaged across bilateral muscles. The most
MFT10–0 (ICCs from 0.36 to 0.71; SEMs from 189 to reliable EMG indices were the bilateral average of
598%). medial back muscles (ICC range: 0.68–0.91; SEM range:
5–35%) and the average of all back muscles (ICC range:
3.2.2. Sensitivity 0.77–0.91; SEM range: 5–30%). With regards to EMG
The MF based parameters (MFT10–80, IMFT10–80, indices of fatigue, the identification of the most fatigable
IMF75) were not sensitive to the differences in muscle muscle also lead to satisfactory results (ICC range: 0.74–
composition expected between groups. Between group 0.79; SEM range: 21–26%). However, among the EMG
differences were observed in the MF data across the recovery indices, only REC was reliable for medial
force levels (especially between healthy and CLBP men muscles (MU-L5 and LO-L1) and when bilateral averag-
for the MU-L5 muscles, Fig. 4) but large inter-individual ing was performed. According to the results of the D-
variability was present. Consequently, the difference was study (generalizability theory), it was predicted that the
not significant. averaging of measures across two fatigue tests perfor-
med within the same session would increase the
3.2.3. Frequency banding analysis reliability by about 13%.
The power contained in the different frequency bands
of the EMG power spectrum was equivalent for the same 3.3.2. Sensitivity
extension moment at L5/S1. A typical example is The EMG fatigue indices (RMSslp, MFslp) showed
depicted in Fig. 5 for the MU-L5 muscle group. no difference between men and women (Table 2). Even
accounting for skinfold thickness in an analysis of
3.3. Assessment of fatigability covariance was unsuccessful because this covariate
remained statistically unsignificant. Significant differ-
3.3.1. Reliability ences were observed between healthy and CLBP men
The level of reliability obtained in the present study for all but one comparison (MFslp, LO-T10) (Table 2).
for individual muscles was, at best, acceptable. How- Unexpectedly, the corresponding results suggest that the
ever, it was demonstrated that measurement strategies back muscles of healthy men fatigued more rapidly than
C. Larivière et al. / Journal of Electromyography and Kinesiology 13 (2003) 305–318 311

Fig. 5. L5/S1 extension moment (Nm) as a function of power in the different frequency bands (µV2×Hz) during a 0–100% ramp contraction for
the multifidus muscles (MU-L5). From top to bottom, the plots corresponding to the frequency band 1 (20–60 Hz) to 5 (240–300 Hz). Each curve
represents the mean of all healthy (n = 20) and all CLBP (n = 20) subjects. The curve corresponding to the CLBP men follow exactly the course
of the curve corresponding to healthy men, and this at each frequency band.

Table 2
Effect of gender (healthy men vs healthy women) and low back status (healthy and CLBP men) on EMG fatigue indicesa

Healthy men Healthy women P (t-test) Healthy men CLBP Men P (t-test)
(n=12) (n=13) (n=20) (n=20)

MFslp: slope of the MF to time relationship (Hz/s)


Multifidus ⫺1.50 (0.91) ⫺1.27 (0.54) 0.441 ⫺1.34 (0.52) ⫺0.82 (0.49) 0.003
Ilioc. lumb. ⫺0.60 (0.42) ⫺0.60 (0.34) 0.977 ⫺0.60 (0.33) ⫺0.35 (0.23) 0.008
Longissimus-L1 ⫺0.99 (0.58) ⫺0.75 (0.29) 0.203 ⫺0.79 (0.45) ⫺0.46 (0.30) 0.010
Longissimus-T10 ⫺0.49 (0.39) ⫺0.58 (0.29) 0.496 ⫺0.40 (0.27) ⫺0.26 (0.22) 0.088
Mean all muscles ⫺0.89 (0.54) ⫺0.80 (0.32) 0.594 ⫺0.78 (0.35) ⫺0.47 (0.28) 0.004
Most fatigable ⫺1.64 (0.93) ⫺1.39 (0.54) 0.400 ⫺1.46 (0.55) ⫺0.97 (0.52) 0.006
RMSslp: slope of the RMS to time relationship (µV/s)
Multifidus 1.50 (1.47) 0.87 (0.52) 0.159 0.93 (0.70) 0.29 (0.32) 0.000
Ilioc. lumb. 2.59 (3.38) 1.24 (0.60) 0.168 1.84 (1.91) 0.52 (0.58) 0.005
Longissimus-L1 1.34 (1.08) 1.24 (0.83) 0.798 1.27 (0.83) 0.41 (0.44) 0.000
Longissimus-T10 1.44 (1.43) 1.52 (1.03) 0.880 1.51 (0.99) 0.61 (0.54) 0.001
Mean all muscles 1.72 (1.80) 1.22 (0.55) 0.346 1.39 (0.97) 0.45 (0.42) 0.000
Most fatigable 3.01 (3.54) 2.42 (1.45) 0.583 2.66 (2.09) 1.02 (0.85) 0.002

a
Significant differences (P ⱕ 0.05) are identified by bold characters

those of CLBP men and both fatigue indices demon- 3.4. Estimation of recovery time required after the
strates consistent results in this respect. fatigue test to perform a second fatigue trial

No significant differences (one-way ANOVAs


3.3.3. Assessment of the cocontraction of abdominals between the three trials, α = 0.05) were obtained for the
During the fatigue test, coactivity increased for most different EMG indices (RMSslp, MFslp, IRMS, IMF)
subjects (18 out of 22) while the L5/S1 moments computed across the three fatigue trials. This suggested
(extension, lateral bending, axial rotation) remained that complete muscle recovery was allowed with either
stable. The model predicted an average coactivity a 10 or 15 min rest period. The corresponding reliability
increase from 21 Nm (SD: 15) to 33 Nm (SD: 21). results showed that the averaging of two measures lead
312 C. Larivière et al. / Journal of Electromyography and Kinesiology 13 (2003) 305–318

to an ICC increase ranging from 0.02 to 0.10 and a SEM of MF estimates to muscle force or by a curvilinear
decrease ranging from 2 to 10% depending on the EMG relationship (bell shaped), depending on the back muscle
index of fatigue. investigated [36].

3.5. Prediction of back strength using anthropometric 4.2. Back muscle weakness
data
Even though CLBP male and healthy female subjects
The peak L5/S1 extension moment identified as the showed lower back strength than healthy male subjects
back strength was used as the dependent variable. The according to the dynamometry results, the NME EMG
Pearson correlation coefficients revealed poor to valu- parameter showed no between group difference with the
able relationship (range: 0.01–0.60) between inde- exception of the counter-intuitive results (CLBP men
pendent variables and back strength. The final prediction and healthy women with higher NME than healthy men)
regression model included two variables (FFM: fat free obtained for 2 of the 16 comparisons.
mass and THORD: thoracic depth) that accounted for Pain and fear of injury may have confounded the
39% of the variance and the corresponding equation was: strength measures for CLBP subjects. Hence, the use of
dynamometry to report back muscle weakness might at
Back strength ⫽ 14.740 ⫹ 5.814 ⫻ FFM ⫺ 4.959 least partly explain the lower strength results observed
⫻ THORD for CLBP subjects relative to healthy individuals in some
studies. Studies that report no differences between CLBP
(adjusted R 2 = 0.391, standard error of the estimate = and healthy subjects support this assertion [31,70].
42.5 Nm) Nevertheless, it appears reasonable to hypothesize that
back muscle weakness occurs for some CLBP patients
given that the muscle structure (decrease of muscle
4. Discussion mass, alteration of muscle fiber characteristics) is modi-
fied [28,43] and that these modifications are time depen-
4.1. Reliability dent relative to pain symptoms [46].
The pain or fear of injury bias was unlikely between
In general, similar reliability was obtained for the con- healthy males and females, which confirmed that the
trol subjects and CLBP patients for all EMG indices. NME parameter was not a sensitive indicator of back
These results were not expected because the only strength. The NME concept, which might be a useful
reliability study available for CLBP patients [54] demon- tool to assess weakness at simple joints, does not seem
strates moderate ICCs of 0.47 and 0.39 for the left and applicable to the spine where multiple muscles span sev-
right longissimus at L3, respectively, for the MFslp eral joints. The use of the net moments to compute the
index. We attribute our satisfactory results to the stable NME parameter might represent a significant problem
clinical status of the CLBP patients (Oswestry score, when load sharing among back synergic muscles and
VAS pain rating) during the reliability assessment and coactivation of abdominal antagonist muscles occurs.
to the minimization of axial rotation moments using the
visual feedback from the dynamometer [40]. 4.3. Back muscle composition
In most cases (especially for MFslp), averaging meas-
ures across bilateral muscles or across all electrode sites None of the EMG spectral parameters were sensitive
increased the reliability of EMG indices of back to low back status or gender. However, it is possible that
muscles. The averaging across bilateral muscles ignores the CLBP subjects involved in the present study were
the difference that may exist between bilateral muscles not impaired enough to show detectable changes in mus-
when, for example, unilateral pain occurs. However, cle fiber size and/or proportion. In the present study, the
even if these bilateral differences exist, it appears that CLBP subjects were at work at the time of testing and
they cannot be detected reliably as shown in our showed minimal disability according to the gradation
reliability study [40] and in other studies [62,69]. We proposed by Fairbank et al. [19]. However, females have
conclude from our reliability studies that the assessment smaller muscle fiber than in men irrespective of fiber
of back muscle impairments through EMG analysis types or back muscles [44,71]. Then, the absence of dif-
necessitates the use of multiple electrodes to achieve ference between men and women suggested that these
reliable results. spectral parameters were not sensitive to muscle fiber
The reliability of the MFT10–80 slope parameter com- size.
puted during ramp contractions was the only EMG index Given the discrepancy between the MF curves of heal-
showing poor reliability. This was attributed to the flat- thy and CLBP (Fig. 4), MU-L5 muscle), it was hypo-
ness of the MF to moment relationship (slopes close to thesized that between group differences could be com-
zero), which was explained by either a lack of sensitivity prised in specific frequency bands of the power
C. Larivière et al. / Journal of Electromyography and Kinesiology 13 (2003) 305–318 313

spectrum. Unfortunately, this was not the case. However, 4.4.2. Sensitivity to low back status
time-frequency analyses such as wavelet transforms Unexpectedly, healthy males showed more back mus-
might give different results, given their expected ability cle fatigue than CLBP males. This concurred with other
to analyze the EMG signal with specific time resolutions. findings [6] and strongly suggested that our CLBP did
Wavelet analysis decrease the variability of spectral esti- not produce a ‘true’ MVC at the beginning of the assess-
mates [34]. This might be especially useful for ramp ment so that the ‘true’ relative load (function of the
contractions where the force level is changing through MVC) during the fatigue test was smaller (in absolute
the contraction, also implying a possible change in mus- and relative terms) for them. It becomes evident that the
cle length. However, the relationship between muscle main drawback in the measurement of relative endurance
fiber composition (proportions, areas) and spectral para- is the need to get a valid estimate the MVC level. Thus,
meters is confusing [4,25,26,35]. Our results suggested an attempt was made to predict back strength with the
that the role of many confounding factors must be clari- use of anthropometric measurements [39]. However, as
fied before EMG can provide a non invasive alternative demonstrated previously [48,53] and further substan-
to muscle biopsy. tiated in the present paper, this prediction was prone to
errors. Thus, other measurement protocols must be
developed to overcome this situation.
4.4. Back muscle fatigability The task generally used for EMG fatigue assessments
does not correspond to a work task, and hence the mus-
cle fatigue mechanisms involved are different, a con-
4.4.1. Sensitivity to gender dition which makes difficult the inference to muscle
The effect of gender on back muscle fatigability is not endurance in relation to work. The use of a fixed load
trivial. Muscle physiology studies generally demonstrate to induce muscle fatigue would eliminate the need for
a higher muscular endurance in women [11,21]. This measurement of back strength. At first sight, this
could be explained by the greater capacity of women to measurement approach may appear inappropriate for the
use oxidative phosphorylation to produce ATPs [21], evaluation of endurance because absolute endurance
given that muscle composition in terms of muscle fiber partly depends on subject strength [63]. Practically, it is
proportion type (type I vs type II) is the same in both however important to test this form of endurance con-
genders for back muscles [44,71] and that the absolute sidering that a same force level is required for all indi-
load produced is apparently unrelated to gender differ- viduals to be able to perform many working tasks.
ences [21]. Another common characteristic of most EMG fatigue
assessments is the use of a sustained static effort at a
Many studies comparing men to women through the
high level of back strength [44,65]. Although this allows
Sorensen test report lower fatigue in women
the phenomenon of muscle fatigue to be quickly revealed
[13,33,45,59,73]. However, the relative weight of the
through EMG, muscle endurance is not evaluated in con-
trunk is generally lower for women resulting in a longer
ditions that correspond to tasks performed in the work-
holding time in this test [32,33,59] but this hypothesis
place (intermittent contractions at a low to moderate
has yet to be tested adequately.
level of strength). The endurance of muscle fibers at high
Few studies contrasting men and women involved a
levels of strength (60–80% of the MVC) would be evalu-
fatigue test with the subject standing erect (trunk ated with complete occlusion of intramuscular blood
vertical) to eliminate the possible bias of relative trunk flow instead of conditions with low to moderate levels
weight [16,32]. They showed conflicting results with of strength (25–60% of the MVC) creating partial inter-
Jorgensen & Nicolaisen [32], who demonstrate lower mittent occlusion of blood flow, and completely different
fatigue in women using a mechanical muscle fatigue cri- fatigue mechanisms [17]. There is a need to apply EMG
terion, and Elfving et al. [16] and the present study who measurements to quantify muscle fatigue in more com-
show no difference using an EMG muscle fatigue cri- plex tasks performed intermittently at low to moderate
terion. It is possible that EMG is not sensitive enough intensity to better mimic occupational tasks [58]. Given
to detect differences in muscle fatigue. However, these the larger proportion of type II fibers in CLBP subjects
three studies also use a high intensity relative load [47], this form of muscle fatigue assessment should be
(Elfving et al. [16]: 80% MVC; Jorgensen & Nicolaisen efficient to demonstrate their reduced capacity to use the
[32]: 60% MVC; the present study: 75% MVC) that aerobic energy pathways (oxidative phosphorylation)
would halt the circulation of blood flow within the back which is generally more developed in type I fibers. Fur-
muscles [5]. The use of a fatigue test allowing partial or thermore, given that changes in muscle capillarity gener-
intermittent blood circulation might magnify the gender ally accompany the oxidative capacity of a muscle [27],
effect if women use more the oxidative phosphorylation allowing partial blood flow could possibly highlight the
pathway to produce ATPs. This is supported by previous impairment in muscle capillarity that would be expected
studies performed on other muscle groups [18,49]. in CLBP subjects (more type II fibers = decrease of oxi-
314 C. Larivière et al. / Journal of Electromyography and Kinesiology 13 (2003) 305–318

dative capacity = decrease of capillarity) relative to heal- with Cooper and Stokes [12] who observed variable load
thy individuals. This should affect the EMG signal con- sharing only with the more strenuous tasks involving
tent, the MF being sensitive to the accumulation of higher levels of fatigue. Moreover, Oddsson et al. [59]
metabolic byproducts that is amplified by muscle observed this phenomenon only for their male sample
ischemia [52] or in other words, by an impairment in (n = 10) because seven of them reached exhaustion
muscle blood flow that would go along with a low capil- before the end of their 60 s Sorensen test. None of the
larity density. Unfortunately, this latter hypothesis is not women (n = 10) reached exhaustion and no drop in EMG
supported in the literature because back muscle biopsy activation was apparent.
studies contrasting healthy and CLBP subjects do not The drop in the EMG activation of lumbar muscles
include data on capillarity. might be linked to specific muscles (multifidus for
instance which are generally fatigued earlier than the
4.4.3. Assessment of the cocontraction of abdominals other components of the erector spinae (see MFslp—
It was assumed that abdominal muscles would not Table 2 and [64,68]). These muscles would be progress-
fatigue during sustained trunk extension so that time- ively switched off by the central nervous system when
related changes in the EMG of these muscles would they reach exhaustion. Thus, the load must be taken by
reflect force modulations after EMGAO adjustment. This other erector spinae components to keep the net moment
assumption appears reasonable because the relative level constant. Scheerlink-Bunkens and Jorgensen [66]
activation of the abdominal muscle remained below 20% observed a shift of the load from the lumbar to the tho-
of the maximal voluntary EMG on average (rectus abdo- racic erector spinae. However, the additional load put on
minis (left and right): 6 ± 4% and 7 ± 6%; external these muscles cannot be sustained for a long time and
oblique: 19 ± 13% and 17 ± 16%; internal oblique: 15 the subject rapidly reach exhaustion. An additional
± 10% and 18 ± 15%) at the beginning of the fatigue increase of EMG of the LO-T10 level was observable
test (first 5 s) and the contraction was relatively short in only two of our four cases (as in Fig. 6) but it is
(30 s). The increase in trunk muscle coactivity might possible that the load was sometimes shifted to muscles
indicate a protective strategy to stabilize the lumbar not recorded with our EMG setup.
spine but at the expense of additional shear and com- Variable load sharing between synergic muscles is
pression forces on lumbar joints. Furthermore, the back hypothesized as a muscle strategy to delay muscle
muscles must counteract this additional net flexion fatigue [75]. This phenomenon might partly explain the
moment produced by the abdominals, a situation that weak reliability of RMSslp relative to MFslp EMG para-
should precipitate muscle fatigue. We can hypothesize meters because EMG RMS amplitude is more sensitive
that CLBP subjects employ more abdominal coactivity than MF to the load [56]. The standardization of the task
to stabilize their lumbar spine [9,60,61], so they would and measurement protocol cannot exclude the influence
be more prone to back muscle fatigue. However, the of the central nervous system on the muscle recruitment
verification of these hypotheses requires the modification patterns. Thus, appropriate quantification of load sharing
of present EMG driven models to process adequately would be required to act as a complementary EMG para-
CLBP subjects data who cannot produce the required meter to explain muscle fatigue. However, to achieve
MVC to normalize EMG. this, the changes in amplitude and spectral EMG para-
meters due to fatigue and variations in muscle load must
4.4.4. Load sharing between back muscles be differentiated. A method has been proposed to achi-
A phenomenon that also deserves attention in the eve this goal [42] but it is based on the premise that MF
assessment of back muscle fatigue is the variability of increase monotonously with muscle force. Unfortu-
load sharing between the different components of the nately, we observed that the MF remains stable or even
erector spinae. Van Dieën et al. [75] have shown the decreases across the force levels [36] so that this method
presence of this phenomenon in back muscles, but others would be useless when applied to back muscles. Other
also suggest that it occurs in some circumstances. A drop methods must be developed and tested to resolve this
in the activation of the lumbar muscles is reported for problem.
some subjects at the end of a fatigue test while the lum- In summary, the assessment of back muscle fatigue to
bar net moment is kept constant [12,59]. We inspected infer back muscle capacity at work is a complex task
the results of our sample of 20 healthy subjects and that should be addressed in different ways. Van Dieen
observed this phenomenon in four of them (typical case et al. [75] identified three factors that explain muscular
in Fig. 6). Interestingly, the lowest MFslp among the endurance: (1) anatomical factors (muscle composition,
eight electrode sites corresponding to the most fatigable capillarization), (2) physiological factors (hormones,
muscle were all smaller than ⫺1.49 (MFslp range at all enzymes, energy stores), and (3) functional factors
electrode sites: ⫺0.67 to ⫺3.00 in our 20 healthy (motor control). Anatomical and physiological factors
subjects) for all of them meaning that these subjects were can be accommodated by fatigue tests involving the
getting more fatigued than the others. This concurred recruitment of the motor units commonly used in daily
C. Larivière et al. / Journal of Electromyography and Kinesiology 13 (2003) 305–318 315

Fig. 6. L5/S1 moment components (Nm) and electromyographic signals at eight electrode sites in function of time (s). The L5/S1 extension
moment (upper left plot) was kept constant throughout the fatigue test, while the L5/S1 moments coupled to the extension moment (upper right
plot: Mlat = lateral bending and Mrot = axial rotation) stayed at negligible values. See the decrease of MU-L5 activation (lower plots) and the
corresponding increase of LO-T10 activation at the end of the fatigue test (these events are identified with arrows). The decrease of activation was
also observed at IL-L3 and LO-L1 electrode sites but never at LO-T10 in other subjects.

activities and to some extent, allowing aerobic energy Safety Research Institute Robert-Sauvé (IRSST: Institut
pathways to come into play (e.g. intermittent de recherche Robert-Sauvé en santé et en sécurité du
contractions). However, even with the level of task stan- travail). Christian Larivière was supported by a post-
dardization of our measurement protocol, control mech- doctoral fellowship from the IRSST.
anisms were not adequately controlled to isolate intrinsic
muscle properties. Thus, these control mechanisms must
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299–309. Christian Larivière received a B.Sc. in physi-
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Ph.D. in Clinical sciences from the University
ences between males and females in EMG and fatiguability of
of Sherbrooke, Sherbrooke, Canada, in 1992,
lumbar back muscles, in: P.A. Anderson, D.J. Hobart, J.V. Danoff 1994 and 1999, respectively. From 1999 to
(Eds.), Electromyographical Kinesiology, Elsevier, Amsterdam, 2000, he was a post-doctoral fellow in biomed-
1991, pp. 295–298. ical sciences at the University of Montreal, Que-
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5 (4) (1992) 383–389. tute Robert-Sauvé, Montreal, Quebec, Canada.
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318 C. Larivière et al. / Journal of Electromyography and Kinesiology 13 (2003) 305–318

A. Bertrand Arsenault received a B.Sc. Denis Gagnon received a B.Sc. in physical edu-
(Physical Therapy), M.Sc. (Kinesiology) and cation (1980) and M.Sc. in kinanthropology
Ph.D. (Kinesiology) from University of Mon- (1985) from University of Sherbrooke, and a
treal, Simon Fraser University and University of Ph.D. in biomechanics in 1990 from University
Waterloo respectively. He practiced physical of Montreal. He is a Professor at the Department
therapy for several years before joining, in 1980, of Kinanthropology of the University of Sher-
the School of Rehabilitation of the University of brooke and Director of the Occupational Biome-
Montreal and the Research Center of the Mon- chanics Laboratory. His research interests focus
treal Rehabilitation Institute. Since 1980, he has on the study of trunk muscle coactivity stra-
acted as a professor, director of graduate studies tegies during dynamic lifting and on the investi-
and director of the physical therapy program at gation of back muscle fatigue during static effort
the University of Montreal and as a researcher in healthy and low back pain individuals.
and director of this research center. He is now director of the School of
Rehabilitation, Faculty of Medicine, University of Montreal. He has been
involved in research activities focussing on the evaluation of the musculos-
keletal system of stroke patients as well as of subjects suffering from back
and neck pain. Patrick Loisel received his MD degree in 1971
from the Faculty of Medicine of Paris VI
Denis Gravel is Professor at the School of (France). He is a Fellow of the Royal College
Rehabilitation of the University of Montreal and of Physicians and Surgeons of Canada
researcher at the Research Center of the Mon- (orthopaedic surgery) since 1986. He is full pro-
treal Rehabilitation Institute. After he received fessor at the Faculty of Medicine of the Univers-
his B. Sc. in Physical Therapy in 1970, he prac- ité de Sherbrooke and presently involved in
ticed physical therapy for two years. Then, he research, practice and teaching in work rehabili-
completed his M.Sc. degree at the department tation at Charles LeMoyne teaching Hospital
of anatomy of the University of Montreal. From (South Shore Montreal). His research work is in
1976 to 1983, he acted as a Professor at the the development and validation of programs and
School of Rehabilitation of the University of tools for the prevention of work disability for
Montreal. From 1984 to 1991, he completed his musculoskeletal disorders. He is the head of the PREVICAP multidiscipli-
Ph.D. degree in neurobiology at Laval Univer- nary clinical research team in work disability prevention. He is the director
sity. From 1992 to 1996, he was granted from the FRSQ (Fonds de of the Quebec network for work rehabilitation (RRTQ) and the head of
Recherche en Santé du Québec) as a clinical researcher. His research inter- the work disability prevention CIHR strategic training program. He holds
est focus on the evaluation of normal and pathologic motor function using the research chair Bombardier/Pratt & Whitney in work rehabilitation at
electromyography, biomechanics and dynamometry techniques. the Université de Sherbrooke.

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