Experimental muscle pain results in reorganization of coordination among trapezius muscle subdivisions during repetitive shoulder Xexion

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1 Exp Brain Res (27) 178: DOI 1.17/s RESEARCH ARTICLE Experimental muscle pain results in reorganization of coordination among trapezius muscle subdivisions during repetitive shoulder Xexion Deborah Falla Dario Farina Thomas Graven-Nielsen Received: 25 June 26 / Accepted: 3 September 26 / Published online: 19 October 26 Springer-Verlag 26 Abstract The aim of the study was to examine the evect of experimental unilateral upper trapezius muscle pain on the relative activation of trapezius muscle subdivisions bilaterally during repetitive movement of the upper limb. Surface EMG signals were detected from nine healthy subjects from the upper, middle and lower divisions of trapezius during a repetitive bilateral shoulder Xexion task. Measurements were performed before and after injection of.5 ml hypertonic (pain condition) and isotonic (control) saline into the upper division of the right trapezius muscle in two experimental sessions. On the painful side, upper trapezius showed decreased EMG amplitude (average rectiwed value, ARV) and lower trapezius increased ARV throughout the entire task following the injection of hypertonic saline ( vs μv, and vs μv, respectively, at the beginning of the contraction). On the side contralateral to pain, greater estimates of ARV were identiwed for the upper division of trapezius as the task progressed ( vs μv, at the end of the contraction). Muscle Wber conduction velocity did not change with pain in all three divisions of the right trapezius muscle. The results suggest that local elicitation of nociceptive averents in the upper division of the trapezius induces reorganization in the coordinated activity of the three subdivisions of the trapezius in repetitive dynamic tasks. D. Falla (&) D. Farina T. Graven-Nielsen Center for Sensory-Motor Interaction (SMI), Department of Health Science and Technology, Aalborg University, Fredrik Bajers Vej 7D-3, 922 Aalborg, Denmark deborahf@hst.aau.dk Keywords Experimental pain Trapezius muscle Muscle Wber conduction velocity Dynamic contraction Electromyography Introduction Experimental muscle pain induced by injection of chemical substances, e.g. hypertonic saline, provides a method to assess changes in motor control due to altered averent feedback. Progressively increased muscle pain intensity results in a gradual decrease in motor unit discharge rate during isometric contractions which are not associated with a change in muscle Wber membrane properties (Farina et al. 24a). In addition, experimental muscle pain provides a means to explore the evect of pain on motor control in the absence of pathological or inxammatory changes within the muscle and joint structures. Muscle pain inxuences motor control strategies via central mechanisms (Le Pera et al. 21; Thunberg et al. 22), both in the muscle investigated (Graven-Nielsen et al. 1997) as well as in synergistic and antagonist muscles (Graven-Nielsen et al. 1997; Ciubotariu et al. 24). Due to central inhibitory mechanisms, maximal voluntary contraction force and endurance time during isometric sub-maximal contractions are reduced by experimental muscle pain (Graven-Nielsen et al. 1997, 22). Muscle activation during dynamic tasks is also altered by pain. For example, injection of hypertonic saline into the biceps and triceps brachii muscles resulted in modiwcation of the elbow Xexor and extensor muscles during a repetitive elbow movement task (Ervilha et al. 25).

2 386 Exp Brain Res (27) 178: Activation of the upper division of the trapezius muscle is altered in people with chronic neck pain during repetitive movement of the upper limb (Elert et al. 21; Falla et al. 24; Falla and Farina 25; Mork and Westgaard 26). For example, when performing repetitive upper limb elevation, people with neck pain demonstrated a greater decrease in muscle Wber conduction velocity (CV) and greater increase in electromyographic (EMG) signal amplitude of the upper trapezius muscle compared to a group of healthy subjects (Falla and Farina 25). In addition to evidence of motor control dewcits in the upper trapezius muscle, there is accumulating evidence of impairment in the lower division of the trapezius muscle in people with painful shoulder conditions (Ludewig and Cook 2; Cools et al. 23; Lin et al. 25). Experimental muscle pain may provide a means to explore changes in trapezius motor control and help to diverentiate the mechanisms of muscle impairment identiwed in people with chronic work-related neck and shoulder pain. The aim of this study was to examine the evect of experimental unilateral upper trapezius muscle pain on the relative activation of trapezius muscle subdivisions bilaterally during repetitive movement of the upper limb. Methods Subjects Nine volunteers (four female) participated in the study after providing informed consent. Subjects (age, years) were free of shoulder and neck pain, had no past history of orthopaedic disorders avecting the shoulder or neck region and no history of neurological disorders. Ethical approval for the study was granted by the Ethics Committee (VN 25/38) and all procedures were conducted according to the Declaration of Helsinki. Procedure Subjects were comfortably positioned in sitting with their back resting against a height-adjustable chair with knees in 9 of Xexion and feet Xat on the ground. A target was positioned on a board in front of them so that their Wngertips touched the target when their arms were fully extended at 12 of shoulder Xexion with the elbow in full extension and the wrist in neutral position. A second target was placed mid position on the subject thighs. Subjects were asked to tap with their hands bilaterally in a cyclic manner between the two targets to the beat of a metronome set at 88 beats per minute for 2.5 min (Falla and Farina 25; Falla et al. 26). After a 3 min rest period, the subject repeated the procedure immediately following the injection of either hypertonic or isotonic saline into the right upper trapezius muscle. Experimental muscle pain Experimental muscle pain was induced by injection of.5 ml of sterile hypertonic saline (5.8%) into the upper division of the trapezius on the right side. The 27G cannula was inserted into the trapezius muscle at the midpoint between the spinous process of C7 and the acromion. The bolus was injected over a 1-s period. In a separate experimental session, subjects received an injection of isotonic saline (.5 ml,.9%) into the trapezius muscle at the same location. The type of injection received was randomized across the two experimental sessions. Each session was separated by a minimum of 7 days. Measures of perceived pain Subjects were asked to rate their level of perceived pain on an 11 point numerical rating scale (NRS) anchored with no pain and the worst possible pain imaginable. Pain intensity ratings were obtained immediately following the injection, every 3 s throughout the task and every 3 s following completion of the task until the pain subsided. Upon completion of the task, subjects documented the area of pain on a body chart. Multi-channel surface EMG Surface EMG signals were detected from the upper, mid and lower divisions of the trapezius muscle on the right side (ipsilateral to the injection) using linear adhesive arrays of eight electrodes (bar electrodes, 5 1mm size, 5mm apart; LISiN-SPES Medica, Italy). The detection surface was separated from the skin by a small cavity (»1mm deep) Wlled with 2 μl of conductive gel. Myoelectric signals were ampliwed (EMG-64, 64-channel ampliwer, LISiN Centro di Bioingegneria, Politecnico di Torino, Italy), Wltered ( 3 db bandwidth, 1 5 Hz), sampled at 2,48 Hz, and converted to 12-bit digital samples. Prior to electrode placement, each division of the trapezius muscle was assessed during preliminary test contractions with a dry array of eight electrodes (silver bars, 1 1 mm size, 1 mm apart) with the subject positioned in sitting. The main muscle innervation

3 Exp Brain Res (27) 178: zone location was identiwed for all divisions of the trapezius muscle in two shoulder joint angles, neutral and 12 of Xexion, from the surface EMG recordings, as described previously (Masuda et al. 1985). The subject s skin was prepared by gentle local abrasion using abrasive paste and cleaned with water. Electrode locations are illustrated in Fig. 1. For the upper division, the adhesive arrays were positioned between the most lateral detected innervation zone location and the distal tendon region of the muscle along the line between the acromion and the seventh cervical vertebra (Jensen et al. 1993; Hermens et al. 1999). For the mid division, the electrode contacts were aligned with the spinous process of the second thoracic vertebra and for the lower division, electrode contacts were positioned along the line between the acromion and the spinous process of the Wfth thoracic vertebra (Johnson and Pandyan 25). A reference electrode was placed over the upper thoracic spine. To provide a measure of shoulder joint angle, an electro-goniometer (Biometrics Ltd) was attached to the subject s right shoulder. The output was calibrated for shoulder joint angle and recorded simultaneously with the EMG signals. Skin temperature (Ellab, Copenhagen, Denmark) over the trapezius muscle was monitored before and after completion of the upper limb task across the experimental session. Bipolar surface EMG Bipolar surface EMG was recorded with pairs of surface electrodes positioned 2 mm apart (Neuroline 721-k; Medicotest, Denmark) over the left trapezius muscle (contralateral to the injection) following skin preparation (Fig. 1). For the upper division, the electrodes were positioned 2 mm lateral to the midpoint along the line between the acromion and the seventh cervical vertebra (Jensen et al. 1993). For the mid division, the electrode contacts were aligned with the spinous process of the second thoracic vertebra and for the lower division, electrode contacts were positioned along the line between the acromion and the spinous process of the Wfth thoracic vertebra (Johnson and Pandyan 25). Signals were bandpass Wltered (1 5 Hz); ampliwed (EMG ampliwer, Aalborg University, Denmark) and sampled at 2 khz. Signal analysis Fig. 1 Surface EMG signals were detected from the upper, mid and lower divisions of the trapezius muscle on the right side using linear adhesive arrays of eight electrodes and on the left side using bipolar surface electrodes. For the upper division of trapezius, the electrode centers were aligned along the line between the acromion and the seventh cervical vertebra. For the mid division, the electrode contacts of the most proximal array were aligned with the spinous process of the second thoracic vertebra and for the lower division, electrode contacts were positioned along the line between the acromion and the spinous process of the Wfth thoracic vertebra. An electro-goniometer was attached to the subject s right shoulder. Experimental muscle pain was induced by injection of hypertonic saline into the upper division of the trapezius on the right side at the midpoint between the spinous process of C7 and the acromion The goniometer signal was low-pass Wltered (anticausal Butterworth Wlter of order 4, cut-ov frequency 1 Hz). Muscle Wber CV was estimated from the array signals of the right side for each cycle at the time instant corresponding to 9 of Xexion with the method proposed by Farina et al. (24b). Average rectiwed value (ARV) was computed for both sides over time intervals of 25-ms centered at the same time instants where CV of the right side was estimated. The exercise duration was divided into Wve consecutive, non-overlapping intervals, each lasting 3 s. CV, and ARV values in each time interval were averaged, resulting in Wve average values during the exercise. Statistical analysis Since tests for normality indicated Gaussian distribution of all variables, a three-way ANOVA was applied to the values of CV and ARV for trapezius muscle subdivisions with injection (hypertonic and isotonic), contraction (pre and post injection) and time (3 s intervals of the contraction time) as repeated measures. In addition, a three-way ANOVA was applied to subjective ratings of pain intensity and skin temperature with injection (hypertonic and isotonic), contraction

4 388 Exp Brain Res (27) 178: (pre and post injection) and time (3 s intervals of the contraction time) as repeated measures. SigniWcant diverences revealed by ANOVA were followed by post-hoc Student Newman Keuls (SNK) pair-wise comparisons. Results are reported as mean and standard deviation (SD) in the text and standard error (SE) in the Wgures. Statistical signiwcance was set at P <.5. Results Perceived pain Pain intensity scores and area of pain following the injection of isotonic and hypertonic saline are presented in Fig. 2. Peak pain intensity was and.9.9 following injection of hypertonic and isotonic saline, respectively (P <.1). Following the injection of hypertonic saline, pain had subsided in all subjects by 69 s ( s). Muscle activity on the painful side Figure 3 shows representative EMG data for the ipsilateral upper, middle and lower divisions of the trapezius muscle pre and post the injection of hypertonic saline. Across all conditions, estimates of ARV for the upper division increased over time (ANOVA: F 4 = 16.8, P <.1). However, lower estimates of ARV ( % decrease across all time instants) were detected during the repetitive arm movement task following the injection of hypertonic saline (ANOVA: F 1 = 41.9, P <.1; SNK: P <.1; Fig. 4). Estimates of ARV for the lower division were signiwcantly greater throughout the entire task following the injection of hypertonic saline (ANOVA: F 4 =2.7, A 6 5 Pain Intensity (-1) Isotonic Injection B Isotonic Fig. 2 a Pain intensity scores (mean and standard error, SE) and b area of pain following the injection of isotonic and hypertonic saline into the right upper division of the trapezius muscle. Following injection of hypertonic saline, pain was present throughout the entire duration of the repetitive upper limb task (shaded area). The area of pain reported by subjects was over the upper trapezius muscle with some reports of referred pain into the head/ face (three out of nine subjects)

5 Exp Brain Res (27) 178: Upper Middle Lower 3 ARV (µv) Pre Injection Post Injection Fig. 3 Representative average rectiwed value (ARV) data are shown for the three divisions of the trapezius muscle on the injected side during performance of the 2.5 min repetitive upper limb task pre and post the injection of hypertonic saline Upper Trapezius ARV (µv) 1 Isotonic Lower Trapezius ARV (µv) Middle Trapezius ARV (µv) * * Pre Injection Post Injection Fig. 4 Mean and SE of the ARV are shown for the upper, middle and lower trapezius muscle during performance of the 2.5 min repetitive upper limb task before and after the injection of hypertonic (pain condition) and isotonic (control) saline. Asterisk: signiwcant diverence pre to post injection (SNK: P <.1), hash: signiwcant diverence pre to post injection (SNK: P <.1) P <.5; SNK: P <.1; Fig. 4). However, this diverence decreased over time ( vs % increase in ARV at the Wrst and last time intervals, respectively). Estimates of ARV for the middle division increased over time (ANOVA: F 4 =1.6, P <.1) but did not depend on the injection type. No signiwcant diverences were identiwed for estimates of CV for the upper, middle and lower divisions of the trapezius muscle throughout the task following injection of hypertonic saline ( , , m/s, for the upper, middle, and lower division at the beginning of the contraction; Fig. 5). Skin temperature did not signiwcantly change during the task in both experimental sessions. Muscle activity on side contralateral to pain Estimates of ARV for the upper division of the trapezius muscle on the left side (non-injected side) were signiwcantly greater towards the end of the task following the injection of hypertonic saline into the right upper trapezius (ANOVA: F 4 = 3., P <.5; SNK:

6 39 Exp Brain Res (27) 178: Upper Trapezius CV (m/s) Isotonic Lower Trapezius CV (m/s) Middle Trapezius CV (m/s) Pre Injection Post Injection Fig. 5 Mean and SE of muscle Wber conduction velocity (CV) are shown for the upper, middle and lower trapezius muscle during performance of the 2.5 min repetitive upper limb task before and P <.1; Fig.6). No diverences in ARV following the injection of hypertonic saline were found for the other two subdivisions. Discussion This study demonstrates a reorganization in the coordination among the divisions of the trapezius muscle without a change in the membrane Wber properties (as assessed by CV) in response to muscle pain during repetitive movement of the upper limb. In addition to a reduced activity of the painful muscle, which is in agreement with the pain adaptation model (Lund et al. 1991), increased activity was observed in non-painful muscle subdivisions both ipsilateral and contralateral to the side of pain. Trapezius muscle activation after the injection of hypertonic (pain condition) and isotonic (control) saline. No signiwcant diverences were identiwed following both injections A decrease in EMG activity of the upper division of the trapezius muscle was observed throughout the entire duration of the task following injection of hypertonic saline. Accordingly, excitation of nociceptive muscle averents (group III and IV) with hypertonic saline has been shown consistently to decrease EMG activity in the painful muscle both in isometric and dynamic tasks (Graven-Nielsen et al. 1997, 22; Madeleine et al. 1999; Sohn et al. 2; Ervilha et al. 25; Ge et al. 25). Increased activity was identiwed for the lower subdivision of the trapezius muscle, following injection of hypertonic saline into the upper division. Although the upper division of the trapezius muscle is considered a primary scapular elevator and the lower division a primary scapular depressor, during shoulder elevation coordinated activity of all three divisions of the trapezius muscle is necessary (Johnson et al. 1994). Accordingly, increased activity of the lower trapezius in the presence of decreased activity of the upper trapezius, most likely served to control the scapular during elevation and rexects a reorganization of coordination within the trapezius muscle to complete the required task. The relative increase in EMG activity of the lower division of the ipsilateral trapezius muscle was reduced towards the end of the task. This may be due to the reduction in

7 Exp Brain Res (27) 178: Upper Trapezius ARV (µv) Isotonic * Lower Trapezius ARV (µv) Middle Trapezius ARV (µv) Pre Injection Post Injection Fig. 6 Mean and SE of the ARV are shown for the left (non-injected) upper, middle and lower trapezius muscle during performance of the 2.5 min repetitive upper limb task before and after the injection of hypertonic (pain condition) and isotonic (control) the subject s pain intensity over the course of the contraction (Fig. 1), rexecting a progressive modiwcation of the motor control strategy as a result of pain. Middle trapezius EMG activity was not modiwed following injection of hypertonic saline. The observation that experimental upper trapezius muscle pain did not result in a uniform modiwcation of EMG activity for all subdivisions but rather resulted in selective changes is consistent with an altered motor control strategy suycient to perform the dynamic task. A reorganization of synergistic muscle activity and modiwcation of the motor strategy probably acts to minimize disturbance to the motor task. ModiWcation of the relative contributions of muscles has been previously observed in response to experimentally induced pain in the absence of a change to the motor output during a cyclic task (Ervilha et al. 25). The increase in EMG activity of the upper trapezius contralateral to the injection site towards the end of the task is in agreement with the observed increase in contralateral upper trapezius muscle activity in patients with chronic neck pain when performing a unilateral repetitive task (Nederhand et al. 2). saline into the right upper trapezius. Asterisk: signiwcant diverence pre to post injection (SNK: P <.1), hash: signiwcant diverence pre to post injection (SNK: P <.1) Trapezius muscle Wber conduction velocity Prior to the injection of hypertonic saline, there was no evidence of change in upper trapezius CV estimates across the 2.5-min task, which is consistent with previous Wndings (Falla and Farina 25; Falla et al. 26). In addition, estimates of CV remained stable for both the middle and lower divisions of the trapezius muscle. A stable CV throughout the contraction could be attributed to maintenance of blood Xow throughout the muscle due to the dynamic nature of the task, thereby reducing the accumulation of metabolites (Masuda et al. 1999). Moreover, additional motor units may have been recruited during the task with respect to the initial active pool, as indicated by the increase in ARV during performance of the task. Following injection of hypertonic saline in the upper division of trapezius, no change was identiwed for estimates of CV for all three subdivisions of trapezius ipsilateral to the side of pain. The absence of a change in CV is consistent with previous studies which have observed that injection of hypertonic saline does not avect muscle Wber membrane properties (Farina et al.

8 392 Exp Brain Res (27) 178: a). Since average CV did not change following hypertonic saline, the change in EMG amplitude was likely due to modulation of motor unit discharge rate, in agreement with single motor unit studies (Sohn et al. 2; Farina et al. 24a). Average muscle Wber CV of the upper trapezius muscle during the same dynamic task, was previously shown (Falla and Farina 25) to be higher in people with chronic neck pain than in control subjects, with enhanced decrease in CV over time in the patient group. Similar diverences in CV estimates were not identiwed following experimental upper trapezius muscle pain which indicate that altered muscle activity due to pain by itself cannot explain the electrophysiological Wndings in patients. Thus, modiwcations in trapezius muscle EMG in people with neck pain are likely the result of a combination of altered neural input to muscle and changed muscle properties, in agreement with biopsy studies (Lindman et al. 1991; Kadi et al. 1998; Larsson et al. 1998). The Wnding that experimental upper trapezius muscle pain results in reorganization in the coordination among the divisions of trapezius muscle may have implications for the perpetuation and worsening of symptoms during repetitive upper limb work. This study demonstrates that an acute bout of pain within the upper trapezius muscle is suycient to result in altered motor control of the trapezius muscle, not only locally at the site of pain but also in non-painful regions within the muscle and on the contralateral side. A modiwcation of the motor strategy which results in compensatory muscle activity is likely to lead to muscle overload and perpetuate the symptom of pain. Moreover, it is not unlikely that such a disturbance in the motor control of the trapezius would play a role in the development of persistent symptoms and chronic modiwcation of the muscle properties and may explain some of the motor control dewcits which have been identiwed in people with chronic neck and shoulder pain (Nederhand et al. 2; Falla et al. 24). Acknowledgments Deborah Falla is supported by a John J. Bonica Fellowship received from the International Association for the Study of Pain and a C. J. Martin Fellowship received from the National Health and Medical Research Council of Australia (ID ). This study was partly supported by the Danish Technical Research Council and by the European project Cybernetic Manufacturing Systems (CyberManS; contract nr ). References Ciubotariu A, Arendt-Nielsen L, Graven-Nielsen T (24) The inxuence of muscle pain and fatigue on the activity of synergistic muscles of the leg. 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