Journal of Electromyography and Kinesiology 15 (2005) 27–36 www.elsevier.com/locate/jelekin
Experimental muscle pain increases mechanomyographic signal activity during sub-maximal isometric contractions P. Madeleine *, L. Arendt-Nielsen Center for Sensory-Motor Interaction (SMI), Department of Health Science and Technology, Aalborg University, Building D-3, Fredrik Bajers Vej 7, DK-9220 Aalborg, Denmark Received 16 March 2004; received in revised form 3 June 2004; accepted 16 June 2004
Abstract This study was designed to investigate the local effect of experimental muscle pain on the MMG and the surface EMG during a range of sub-maximal isometric contractions. Muscle pain was induced by injections of hypertonic saline into the biceps brachii muscle in 12 subjects. Injections of isotonic saline served as a control. Pain intensity and location, MMG and surface EMG from the biceps brachii were assessed during static isometric (0%, 10%, 30%, 50% and, 70% of the maximal voluntary contraction) and ramp isometric (0–50% of the maximal voluntary contraction) elbow flexions. MMG and surface EMG signals were analyzed in the time and frequency domain. Experimentally induced muscle pain induced an increase in root mean square values of the MMG signal while no changes were observed in the surface EMG. Most likely this increase reflects changes in the mechanical contractile properties of the muscle and indicates compensatory mechanisms, i.e. decreased firing rate and increased twitch force to maintain a constant force output in presence of experimental muscle pain. Under well-controlled conditions, MMG recordings may be more sensitive than surface EMG recordings and clinically useful for detecting non-invasively increased muscle mechanical contributions during muscle pain conditions. Ó 2004 Elsevier Ltd. All rights reserved. Keywords: Muscle pain; Surface electromyography; Mechanomyography; Neurophysiological models
1. Introduction Musculoskeletal disorders (MSD) often accompanied by pain are one of the most important and challenging health problems. A better understanding of the basic mechanisms of human muscle pain and of the interaction with the motor system is of significant importance for developing new strategies aiming to prevent MSD. Intra-muscular injection of hypertonic saline is a welldescribed method for eliciting exogenously acute experimental muscle pain mimicking muscle pain observed in clinical conditions, e.g. work-related pain [3,28,40]. Sur-
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1050-6411/$ - see front matter Ó 2004 Elsevier Ltd. All rights reserved. doi:10.1016/j.jelekin.2004.06.006
face electromyography (EMG) furnishes generally valuable information about the influence of muscle pain on the motor system during static and dynamic contractions [3,20,24,29,42]. The maximal voluntary contraction level is reduced in presence of experimental muscle pain [20] resulting in different absolute contraction levels. During dynamic contraction, a functional reorganization of the muscle synergies, i.e. reduced level of activity of the painful muscle, is reported during experimental muscle pain [3,20,24,29]. However, in well-controlled conditions during low sub-maximal isometric contractions, no changes are seen in the surface EMG parameters [9,17,38,39]. A reason for this could be that no reorganization or changes occur in the motor control system during isometric contraction. It may also be due to the fact that the sensitivity of the surface EMG
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in such conditions is too low or inadequate and that other assessment methods should be investigated. The EMG signal reflects the generation–propagation–extinction of MU action potentials while the mechanomyographic (MMG) signal reflects contraction phenomena that are triggered by, but not related to, sarcolemmal events [26]. Indeed, changes in muscle fiber geometry related to sarcomere shortening during a muscle contraction produces tension at the tendon level. Such changes or oscillations recorded as the MMG signal reflect slow bulk movement of the muscle, oscillations generated by the muscle at its own resonance frequency [5,19], and pressure waves due to muscle fiber dimensional changes [32]. Recently, isometric ramp contraction has been used to follow the influence of MU activation strategy on MMG signal [2,33]. Surface MMG has been used to study the mechanical activity of a contracting muscle. It seems complementary to surface EMG [26,27,32] and hence may also be used to assess changes following muscle pain. For example, MMG assessments have been made to examine muscle fatigue [6,26,27,36], post exercise muscle soreness [4], and neuromuscular diseases [1,7]. So far, the effect of experimentally induced muscle pain on the MMG signal during sub-maximal isometric contraction has not been described compared with surface EMG recorded during the same conditions. The aim of the study was to describe and compare the local effects of experimentally induced muscle pain on the MMG and surface EMG signal activity during sub-maximal isometric contractions.
the three trials was considered as the MVC. Five minutes after, the ‘‘before pain’’ recordings consisting of short duration (5 s) static contractions at 0–10–30–50– 70% MVC, and a ramp contraction (Fig. 1) from 0% to 50% MVC in 25 s (2%/s) were performed in a random order. Visual feedback (force control) was given to the subjects for static and ramp isometric contractions. After another 5-min break, acute experimental muscle pain was elicited by means of hypertonic saline injection in the right biceps brachii muscle. The ‘‘after injection’’ measurements were identical to the ‘‘before injection’’ ones and were also recorded in a random order. In another experimental session, an identical procedure was performed with isotonic saline injection in the right biceps brachii muscle as a control condition to the experimental muscle pain induced by hypertonic saline. 2.3. Induction of experimental muscle pain Intra-muscular injections of 0.5 ml of sterile hypertonic (6%) and isotonic (0.9%) saline were performed, the bolus was injected over 15 s. A 27Gx1-1/2’’ cannula was inserted (1.5–2 cm) into the muscle belly, on the line between the acromion and the fossa cubit at 1/3 from the fossa cubit of the right arm biceps brachii muscle. Prior and after each static contraction, the actual pain intensity was registered on a visual analogue scale with the lower limit corresponding to ‘‘no pain’’ and the higher limit ‘‘most intense pain’’. Once the recordings performed, the subjects were asked to locate the painful region(s) on an anatomical map. 2.4. Data collection
2. Materials and methods 2.1. Subjects Twelve healthy male volunteers without any history of neuromuscular or orthopedic diseases participated in the study (age: 25.8 ± 2.7 (±SD) years, body mass: 78.4 ± 9.8 kg, height: 179.8 ± 4.5 cm). The study was conducted in conformity with the Declaration of Helsinki. 2.2. Experimental protocol The subjects received first information regarding the experiment, signed the informed consent and were installed in a comfortable chair with the back in an upright position and the right elbow flexed at 90°. The right forearm was semi-pronated and positioned on an armrest. A belt was tightened around the right wrist of the subject and attached to a force transducer. Afterwards, three 5 s maximum voluntary isometric elbow flexions (MVC) separated by 3 min were performed by the right arm. The highest force value obtained among
A piezoelectric force transducer type 9311A (Kistler, Bern, Switzerland) was used to measure the force exerted by the subjects. The force signal was sampled at 500 Hz and off-line digitally low-pass filtered at 20 Hz (Butterworth, 2nd order) prior to analysis. MMG of the biceps brachii muscle was recorded by an uniaxial piezoelectric accelerometer (Bang & Olufsen Technology, Struer, Denmark). The technical specifications of the accelerometer were the following: diameter: 17.6 mm, weight: 2.9 g, sensitivity: 30 pC/m s 2, linear transmission within a frequency range from 0.1 to 800 Hz. The accelerometer was placed with the axis of acceleration perpendicular to the fiber direction on the belly (on the line between the acromion and the fossa cubit at 1/3 from the fossa cubit) of the right arm biceps brachii muscle and attached to the skin with double-sided adhesive tape. The transducer was coupled to a Nexus charge amplifier (Bru¨el and Kjær, Nærum, Denmark) operating with a selected bandwidth of 0.1–100 Hz and sampled at 1 kHz. Bipolar EMG surface electrodes (Neuroline 720-01-k, Ølstykke, Denmark) with circular recording area (diam-
P. Madeleine, L. Arendt-Nielsen / Journal of Electromyography and Kinesiology 15 (2005) 27–36
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Fig. 1. Example (subject 3) of a ramp contraction consisting of an elbow flexion from 0% to 50% MVC in 25 s (2%/s). The filtered (a, b, c) MMG (ms 2), surface EMG (mV) and force signals are displayed vs. time (s).
eter: 6 mm) were placed proximal and distal to the accelerometer corresponding to an inter-electrode distance of 37 mm on abraded ethanol-cleaned skin in the direction of the muscle fibers of the right arm biceps brachii muscle. This position represented a compromise between not covering the end plate zone or getting too close to the musculotendinous region and measuring MMG and surface EMG from the same part of the muscle relative to the innervation zone. The surface EMG signal was amplified 2000 times, band-pass filtered at 2–500 Hz and sampled at 1 kHz. Force, MMG and surface EMG signals were collected synchronously and digitized via an AmpliconÒ (Brighton, United Kingdom) liveline PC226 A/D board and stored on a PC for further analysis. Prior to data analysis, the MMG and surface EMG signals were offline digitally band-pass filtered at 2–100 and 10–400 Hz, respectively.
force) value as an index of steadiness, the RMS value and the mean power frequency (MPF) values of the MMG and surface EMG signals were computed in epochs of 1 s, without overlapping. For the short duration, the median value was chosen for statistical analysis. The MMG/EMG ratio for RMS values was computed to estimate the electromechanical efficiency [7]. The outcome measures were: the mean force, SD force, RMS and MPF values of the MMG and surface EMG signal as well as the RMS MMG/EMG ratio. 2.6. Statistical analysis Mann-Whitney rank sum test for pain intensity and two-way repeated measures analysis of variance
2.5. Data analysis The maximum force was computed in epochs of 1 s, with 100 ms overlapping, from the intermediate 3 s of each of the three MVC trials. The highest force value obtained among the three trials was considered as the MVC. For the short duration and ramp contraction, the mean force value, the force standard deviation (SD
Fig. 2. Distribution of local and referred pain from infusion of 0.5 ml hypertonic saline over 15 s in the right biceps brachii muscle.
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Fig. 3. Means ± SE parameters at contraction levels corresponding to 0%, 10%, 30%, 50% and, 70% of the maximum voluntary contraction (MVC) recorded before (h) and after (n) injection of hypertonic saline. (a) MMG/EMG root mean square (RMS) ratio values, (b) MMG RMS values and (c) surface EMG RMS values.
Table 1 Results of the two-way repeated measures ANOVA of outcome parameters before and during experimental muscle pain in the biceps brachii muscle Ramp contraction
Contraction timing
Before/during pain
Interaction
F
P value
F
P value
F
P value
Mean force SD force RMS EMG RMS MMG MMG/EMG RMS MPF EMG MPF MMG
159.3 2.9 26.6 42.7 1.7 1.7 26.9
