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The Effect of Experimental Neck Pain on Pressure Pain Sensitivity and Axioscapular Motor Control
The Journal of Pain, Vol 16, No 4 (April), 2015: pp 367-379 Available online at www.jpain.org and www.sciencedirect.com
The Effect of Experimental Neck Pain on Pressure Pain Sensitivity and Axioscapular Motor Control Steffan W. Christensen, Rogerio P. Hirata, and Thomas Graven-Nielsen Laboratory for Musculoskeletal Pain and Motor Control, Center for Sensory-Motor Interaction (SMI), Department of Health Science and Technology, Aalborg University, Aalborg, Denmark.
Abstract: Clinical neck pain affects pain sensitivity and coordination of neck muscles, but the impact on the shoulder muscles is unclear. This study investigated the effect of experimental neck pain on the activity of the axioscapular muscles during arm movements and changes in pain sensitivity. Experimental neck pain was induced in 24 healthy volunteers by injecting hypertonic saline into the splenius capitis. Isotonic saline was injected as control. Before, during, and after injections, electromyography was recorded bilaterally from 8 muscles during standardized arm movements (140 scapular plane elevation), and the root mean square amplitude was extracted. Likewise, pressure pain thresholds were assessed bilaterally on 3 sites. The root mean square electromyography was decreased for the ipsilateral upper trapezius (P < .01) and increased for the ipsilateral middle deltoid (P < .03) during upward movements. The root mean square electromyography was reduced for the ipsilateral upper trapezius (P < .01) during downward movement, whereas an increase was recorded in the contralateral external oblique (P < .02). At the injection site, the pressure pain threshold increased during pain compared with the post condition (5 minutes after potential pain had subsided; P < .03). In this study, trunk and axioscapular muscle activities were reorganized in response to localized and referred pain evoked by hypertonic saline injection into an intrinsic neck muscle with no direct attachments to the trunk or shoulder girdle. Perspective: Reorganized activity of the axioscapular muscles has been shown previously in neck pain patients and is believed to happen during the transition from acute to chronic pain. The present study demonstrates for the first time that such reorganization may happen acutely, adding to our understanding of the effects of acute neck pain. ª 2015 by the American Pain Society Key words: Neck, shoulder, pain, experimental, axioscapular.
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eck pain is a frequent problem in the general population,29,34 affecting up to 54% of adults during a 6-month period15 (many of whom will develop prolonged or recurrent symptoms), making this a serious problem and a burden to the health care system.4,15,46 Several studies on neck pain have proposed a link between neck pain and changed motor control of cervical muscles, that is, deep neck flexors and extensors and the sternocleidomastoid.5,8,14,33,45 Moreover, inclusion Received August 17, 2014; Revised December 5, 2014; Accepted January 19, 2015. Internal funding was used for this study. The authors have no conflicts of interests. Address reprint requests to Thomas Graven-Nielsen, DMSc, PhD, Laboratory for Musculoskeletal Pain and Motor Control Center for SensoryMotor Interaction (SMI), Department of Health Science and Technology, Faculty of Medicine, Aalborg University, Fredrik Bajers Vej 7D-3, 9220 Aalborg E, Denmark. E-mail: [email protected] 1526-5900/$36.00 ª 2015 by the American Pain Society http://dx.doi.org/10.1016/j.jpain.2015.01.008
of the shoulder girdle as part of both assessment and targeted neck pain management has been suggested.6,32,34,44,58 This is based on clinical observations of abnormal axioscapular function during upper limb tasks in neck pain patients34,44 and studies showing abnormal shoulder girdle alignment, with neck pain patients displaying protracted shoulders and less scapular upward rotation than healthy controls.20,55 Helgadottir et al19 found reduced activity of the serratus anterior but no changes in the trapezius in neck pain patients during abduction in the scapular plane (scaption). This is in contrast to Falla et al,10 who reported reduced activity in the upper trapezius in neck pain patients during arm movement. Recently, Zakharova-Luneva et al58 could not demonstrate reduced activity in the upper or middle part of the trapezius but found increased activity of the lower part in neck pain patients. These varied findings of different studies could be attributed to the different tasks and movement speeds investigated. Previous studies assessing muscle 367
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activation patterns during arm movements have found these to be related to movement speed, showing faster muscle onset and increased activity during fast movements compared to slow.28,37 In addition, studies have shown that both clinical and experimental pain can affect muscle onsets as well as activity levels,13,19,26,50 and some changes were visible for only fast but not slow movements.25 So far, changes in axioscapular muscle activity during scaption (arm movements in the scapular plane) have been found in patients who have suffered from neck pain for at least 3 months, so it is unknown if acute neck pain causes these changes or if a change in axioscapular muscle activity is a predisposing factor for neck pain. Because of logistical problems recruiting neck pain patients immediately after the initial pain onset, a model utilizing experimental pain might be optimal for investigating the effect of acute neck pain and may indicate relevant changes during the initial stage of clinical neck pain. Along with changes in motor control, localized hyperalgesia to pressure is generally found in neck pain patients when compared with healthy controls.35,36,49,52-54 Interestingly, chronic but not acute idiopathic neck pain patients demonstrated widespread changes with hyperalgesia at the anterior tibial muscle when compared with healthy controls.30 This is in agreement with recent suggestions that a prolonged localized nociception may drive sensitization of central mechanisms, causing spreading sensitization.18 This is in contrast to experimental studies with injection of hypertonic saline into a neck muscle17,48 that found no local changes but instead found evidence of hypoalgesia in the surrounding tissue.17 It is still to be investigated if experimentally induced neck pain causes widespread changes. The purpose of this study was to investigate if experimentally induced neck pain affects motor control of axioscapular muscles during arm movements (scaption) and increases the pain sensitivity when compared to a nonpainful control condition. It was hypothesized that experimental neck pain reorganizes coordination of the axioscapular muscles during slow and fast arm movements. Muscle onsets were expected to be affected during fast movements in a painful condition. Further, segmental hypoalgesia was expected as a result of experimental pain. No gender effects were expected.
Experimental Neck Pain and Axioscapular Motor Control disorders that could influence the results, current use of pain medication, or pregnancy. All subjects had normal pain-free ranges of motion of the neck and shoulder.43 Subjects gave informed consent after having received written and verbal information on the study protocol. The study was conducted in accordance with the Helsinki declaration and was approved by the local ethics committee (N20120018).
Protocol The study used a single-blinded, randomized, crossover design (Fig 1). Subjects were seated in an upright position for muscle activity measurements during scaption or leaning over a bench for pressure algometry assessments. Pressure algometry and electromyography (EMG) were assessed bilaterally, and the order of which measurement was recorded first was randomized in a balanced design. Experimental pain was induced by injecting hypertonic saline into a neck muscle. The side selected for the experimental pain was randomized in a balanced way between the right and left sides. A control injection of isotonic saline was used on the contralateral side. Participants were blinded to which injection they would receive, and the sequence of injections (hypertonic first or isotonic first) was randomized although balanced. The measurements were recorded at baseline, immediately after the injection, and 5 minutes after the potential pain had subsided. Thus, the time between the last 2 recordings was different between the isotonic and hypertonic saline recordings. ’’Post‘‘ recording was conducted 5 minutes after the potential pain had vanished. After the first post recording, there was a gap of 5 minutes before the next baseline were recorded. Data collection was completed in 1 session.
Experimental Neck Muscle Pain Experimental muscle pain was induced in the splenius capitis by injection of sterile hypertonic saline (.5 mL,
Methods Subjects Twenty-five healthy volunteers (13 women) were included. Female participants had a mean age of 25.9 years (standard deviation [SD] = 3.8) and body mass index equal to 22.7 (SD = 2.3), whereas male participants had a mean age of 28 years (SD = 5.4) and a body mass index equal to 23.7 (SD = 3.8). Analysis of demographic data revealed no significant difference of age and body mass index between genders. One participant was left handed. Exclusion criteria were any history of neck or shoulder pain within the past 6 months, signs or symptoms indicating neurologic or rheumatologic
Figure 1. Single-blinded randomized crossover design. Order of saline type or PPT/EMG data collected first was randomized in a balanced way. The measurements were recorded at baseline, immediately after the injection (During), and 5 minutes after the potential pain had subsided (Post).
Christensen, Hirata, and Graven-Nielsen 5.8%). The injection site was found by palpation at the midpoint between the lateral border of the upper trapezius and the posterior border of the sternocleidomastoid at the level of the spinous process C3.11 The injection site was confirmed, and muscle depth was measured using real-time ultrasound imaging (Acuson 128XP10, Native; Siemens Medical Solutions, Malvern, PA). The needle was inserted to a depth equivalent to the middle of the muscle bulk of the splenius capitis where the injection was made. Injection of isotonic saline (.5 mL, .9%) was used as a control condition. The perceived pain intensity was recorded using a 10-cm electronic visual analog scale (VAS) with an external handheld slide, anchored with ‘‘no pain’’ (0 cm) and ‘‘maximum pain’’ (10 cm). Participants were repeatedly reminded to update the VAS between pressure sensitivity measurements or during the intervals between arm movements. Pain duration (time with VAS score > 0), maximum VAS scores (VAS peak), and the area under the VAS-time curve (VAS area) were extracted. After both injections, the participants were asked to complete a McGill Pain Questionnaire describing the quality of perceived pain7,40 and mark the area in which they felt any pain on a body chart. The areas of the body chart drawings were calculated in arbitrary units (a.u.) using a scanning program (VistaMetrix, v.1.38.0; SkillCrest, LLC, Tucson, AZ).
Pressure Algometry Pressure pain thresholds (PPTs) were recorded using a € rby, Sweden) handheld pressure algometer (Somedic, Ho with a 1-cm2 probe (shielded by a disposable latex cover). Pressure was applied progressively at a rate of 30 kPa/s. The threshold was defined as the first time where the perceived pressure became painful and the participants pressed a push button, after which the PPT value was noted. Assessment sites were marked at 1) the injection site, as previously described, over the splenius capitis between the borders of the sternocleidomastoid and the upper trapezius at the level of C3; 2) the temporalis at the intermediate portion35; and 3) over the belly of the extensor carpi radialis brevis just distal to the extensor aponeurosis between the extensor carpi radialis longus and the extensor digitorum.51 The m. temporalis site was chosen as a segmental point because of its innervation by the trigeminal nerve, which has considerable convergence with afferents from C1 to C3, from which the splenius capitis is also innervated (C2–C3).3 Moreover, it is a known site for referred pain from the splenius capitis.48 The extensor carpi radialis brevis site was chosen as an extrasegmental site because of its easy accessibility in the test position (ie, leaning over a bench). For each site, the PPT was measured in triplicates, and the average value was used for the analysis. The assessments for the entire session were always performed first on the site of the first injection followed by the opposite side, allowing an approximately 25-second interval between measurements of specific assessment sites. The PPTs obtained after the in-
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jections were normalized to the respective baseline recordings (100%).
Standardized Arm Movements Participants were sitting in a comfortable upright position with both arms by their side on a customized chair. Feet were placed flat on the floor, and a modified backrest on the chair supported only the sacrum. The posture was visually inspected throughout the study, and subjects were repeatedly reminded to keep an upright posture before a movement series, each lasting no longer than 2 minutes 15 seconds. The arm movement was performed against a flat vertical surface, to which the back of the hand (thumb pointing up) was touching while abducting the stretched arm in the scapular plane, that is, scaption (30 to the frontal plane). A physical marker was placed on the vertical surface, marking the 140 range of motion during scaption. A customized program (Aalborg University, Denmark) provided 3 ‘‘beep’’ cues, which indicated when to start the arm movement, when to be at maximum scaption, and when the arm should be back at the starting position. Both up and down movements lasted 3 seconds without break at the top level. In addition, 3 movements were performed with subjects instructed to initiate the up movement as fast as possible on the sound of the cue signal. The down movement was not investigated for these trials. Six scaptions were done bilaterally, alternating sides (ie, 3 for each side) for each movement with a 6-second break between movements. In the slow scaptions, the time used by subjects to perform the arm movements, that is, from the first cue to the maximum angle and from the maximum angle to the third cue, was monitored using accelerometers (EVAL-ADXL327Z; Analog Devices, Norwood, MA) mounted above the humeral lateral epicondyle. For the fast movements, the time window that was monitored was from the first cue signal to the maximum angle. The extracted durations were averaged among the 3 repetitions for each movement type (slow up, slow down, and fast up) on each side for further analysis. The participants were asked to rate the perceived difficulty of lifting the arm on a 6-point Likert-type scale (0 = ‘‘no problems,’’ 2 = ‘‘minimally difficult,’’ 3 = ‘‘fairly difficult,’’ 4 = ‘‘very difficult,’’ and 5 = ‘‘unable to perform’’).
EMG During Arm Movements The skin was shaved and cleaned before mounting bipolar adhesive surface electrodes (Neuroline 72001-k; Ambu A/S, Ballerup, Denmark) in accordance with the SENIAM (Surface Electromyography for the NonInvasive Assessment of Muscles) recommendations.21 Each pair of electrodes was placed in the direction of the muscle fibers over 8 muscles bilaterally as follows: serratus anterior, anterior to the border of the latissimus dorsi, in the direction of the muscle fibers at the level of ribs 6 to 81; upper trapezius, midpoint on a line from the spinous process of C7 to the acromion22; middle trapezius, midpoint between the medial border of the scapula
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and the spine, at the level of T3 ; lower trapezius, twothirds on the line from the trigonum spinae on scapula toward vertebra T822; anterior deltoid, approximately 2 cm distal and anterior to the acromion on a line toward the thumb22; middle deltoid, over the greatest muscle bulge on a line from the acromion to the lateral epicondyle of the elbow22; erector spinae, approximately 3.5 cm lateral to the spinous process of L122; and external oblique, just below the rib cage on a line connecting the inferior costal margin with the contralateral pubic tubercle.42 The reference electrode (WS1; OT Bioelettronica, Turin, Italy) was placed over the right wrist. The EMG signal was amplified (gain 500), band-width filtered at 25 to 450 Hz, and sampled at 2,048 Hz (OT Bioelettronica). Before further analysis, the raw EMG signals were filtered (Butterworth second order, band-pass 25–450 Hz; MATLAB, Natick, MA) and full-wave rectified. Root mean square (RMS) values were extracted in 2 separate windows of 3 seconds representing the slow up and slow down movements. For the fast movements, this time window was calculated using the time from the first cue signal to the maximum angle from the accelerometer data. EMG onset was automatically detected for the fast movements and quantified using a method previously described in detail by Santello et al.47 In short, epochs for the fast movements were extracted as previously described, and all data points were then continuously integrated using time intervals defined as 1/sample rate (1/2,048 Hz). The integrated EMG (IEMG) was then normalized so that the accumulated IEMG at the end of the task and the time to complete the task receive the value 1. The IEMG line was then compared to a reference line with the slope of 1 (representing the association between normalized IEMG and time). The onset was defined as the time point when the difference between the 2 lines was the greatest: the time point from where a continuous increase of EMG activity is seen and the slope of the curve is >1. Using this method, it was possible to ignore small bursts of activity and to detect the time point where the muscle activity started to increase continuously. A visual inspection of the EMG onset was performed, and if needed, manual correction was allowed. The EMG onsets for all muscles were normalized to the anterior deltoid of the moving arm and an average of the 3 trials used for further analysis.
Statistics Data are presented as mean and standard error of the mean in text and figures. VAS parameters and pain areas on the body chart were compared between the 2 injections using a Wilcoxon test. The data were evaluated in a 2-step procedure where baseline data were analyzed first, and later differences from baseline in the 2 experimental conditions were detected and analyzed. Accelerometer, PPT, and raw RMS EMG data were initially assessed for carryover effect between baselines (before each of the 2 injections) using a repeated measures analysis of variance (RM-ANOVA)
with time (first and second baseline) and, if relevant, assessment site (6 PPT or 16 EMG electrode locations) as dependent factors, and with injection type first (hypertonic or isotonic), injection side first (right or left), and side of investigation (right or left) as between-group factors. For accelerometer and raw RMS EMG data, a separate analysis of baseline data was conducted for each type of arm movement (slow up, slow down, and fast up). Second, baseline data were investigated to ensure comparability between side of injections (or between the opposite sides of the 2 injections) and to identify any baseline gender effect. This was done using an RMANOVA as described above, with time and assessment site for PPT or raw RMS EMG as dependent factors and with side of investigation (injection side or the opposite side) and gender as between-group factors. The analysis for accelerometer and RMS EMG data was conducted separately for each arm movement (slow up, slow down, and fast up). Accelerometer, RMS EMG, and PPT data were normalized to baseline (percentage), and an RM-ANOVA with saline (hypertonic and isotonic) and time (during, after) as dependent factors and with gender as a betweengroup factor was used to analyze the data for all individual EMG and PPT locations and accelerometer data (16 EMG, 6 PPT). This was done for the 2 sides where movements were performed (side of injection and the opposite side) and for each arm movement (slow up, slow down, and fast up). The muscle activity onset data were analyzed using an ANOVA with saline (hypertonic and isotonic) and time (before, during, after) as dependent factors and with gender as a between-group factor. In case of significant factors or interactions, the Newman-Keuls (NK) post hoc test was used accordingly. A post hoc power calculation was conducted to help clarify the strength of PPT and EMG results. In case of significant EMG or PPT findings, Pearson’s correlations were used to investigate associations between VAS peak and the normalized EMG/PPT after the 2 different injection types. The Likert scale scores were compared between the 2 painful conditions using a Fisher’s exact test. STATISTICA 7.0 (StatSoft Inc, Tulsa, OK) was used for all analysis. A P value of .05 was accepted as significant.
Results Of the 25 included participants, data from 1 woman were discarded because of technical problems with the EMG recordings immediately after the painful injection. Accelerometer data (and the related RMS EMG data during fast movements) from 3 subjects had to be discarded because of equipment malfunction.
Experimental Neck Muscle Pain Compared with isotonic saline, injection of hypertonic saline caused a longer pain duration (423 6 21 seconds vs 29 6 14 seconds, P < .001), higher VAS peaks (5.1 6 .5 cm vs .2 6 .1 cm, P < .001), and larger VAS area (1,551 6 357 cm$seconds vs 20 6 12 cm$seconds,
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P < .001). The 3 most common words selected from the McGill Pain Questionnaire after the hypertonic injection were pressing (38% of subjects), intense (29%), and tight (25%), whereas the isotonic injection only caused 2 words to be selected by more than 1 participant, which were pressing (17%) and tight (8%). The perceived pain was distributed distally from the spine of the scapula and up to the base of the skull, with 1 subject perceiving pain in the whole occipital and temporal area (Fig 2). Medially, it was enclosed approximately by the midline, and laterally, it went to the side of the neck. In the shoulder area, it was bordered laterally at the level of the acromioclavicular joint, covering an area approximately the size of the upper half of the trapezius. Two subjects perceived a sensation of pain above the ipsilateral jaw right after the hypertonic saline injection, and 1 subject experienced the same distribution after the isotonic injection. The areas of pain after hypertonic and isotonic saline injections were significantly different in the posterior view (16.8 6 4.8 a.u. vs 1.9 6 .7 a.u., P < .001) and in the lateral view (10.7 6 7.0 a.u. vs .2 6 .2 a.u., P < .006).
neck site on the side of injection revealed a significant RM-ANOVA interaction between time and saline (RM-ANOVA: F[1, 22] = 4.9; P < .04). Post hoc analysis showed a significantly increased PPT immediately after the injection of hypertonic saline compared with 5 minutes after the pain had subsided (NK: P < .03; Fig 3), but no significant differences were found when compared to the control condition (isotonic saline). A significant interaction was also found for the PPT assessed at the extensor carpi radialis brevis on the side of injection (RM-ANOVA: F[1,22] = 4.7; P < .04), but the post hoc test did not indicate any significant differences. On the side opposite to the injection sites, an interaction between saline and time was found for the neck site (RM-ANOVA: F[1,22] = 4.3; P < .05), but no significant differences were found after the post hoc test. No significant correlation was found between VAS peak and PPT measurements. The post hoc power analysis for the nonsignificant PPT results with P values ranging from >.603 to <.054 corresponded to an observed power of 8 to 49.7%.
Pressure Pain Sensitivity
Performance of Scaption
No significant difference was found between the 2 baseline PPT recordings (before each injection). The average baseline PPTs recorded bilaterally at the neck, temporalis, and extensor carpi radialis brevis were 170 6 7 kPa, 265 6 9 kPa, and 275 6 8 kPa, respectively. Analysis of the normalized PPT at the
During the painful contractions, 33% of subjects indicated a Likert scale score of 1 or higher, whereas none of the subjects scored higher than 0 in the control condition (isotonic saline), which was significantly different (Fisher: P < .004). The time from the cue signal to the maximum angle (slow and fast movement) and from the maximum angle to the last cue signal (only slow movement) was not different in the 2 baseline recordings. Analysis of the normalized movement time did not show any difference compared to baseline for the slow up (3.2 6 .1 seconds), slow down (2.8 6 .1 seconds), and fast up (1.6 6 .1 seconds) movements on the injection side or for the slow up (3.3 6 .0 seconds), down (2.7 6 .0 seconds), and fast up (1.6 6 .1 seconds) movements on the noninjection side for any of the conditions.
EMG During Nonpainful Scaption
Figure 2. Superimposed body chart drawings (n = 24) of the pain distribution after saline injection into the splenius capitis. Drawings on the left illustrate the pain area after injections of isotonic saline and on the right after hypertonic saline injections.
No significant difference was found in the RMS EMG from all muscles between the 2 baseline recordings during slow or fast arm movements. The prime movers of the glenohumeral joint, the middle and anterior deltoids, showed the largest RMS EMG values, closely followed by the muscles responsible for controlling and moving the scapula (Fig 4A). The lowest RMS EMG activity on the ipsilateral side of movement was shown by the external obique, followed by the erector spinae. On the side contralateral to the movement, the 3 parts of the trapezius showed the highest RMS EMG values, though substantially less compared with the ipsilateral muscles. When comparing the RMS EMG of the slow up and slow down movements, a reduction is seen for most muscles (Figs 4A and 4B). In general, higher RMS EMG values were seen after fast up compared with slow up movements (Figs 4A and 4C).
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Figure 3. Mean (6standard error of the mean, n = 24) normalized PPTs recorded at the injection side (A) and contralateral side (B) over the splenius capitis, temporalis (Temp), and extensor carpi radialis brevis (ECRB) immediately after injections of hypertonic (Hyp) and isotonic (Iso) saline and 5 minutes after the potential pain had vanished (Post pain). Significantly increased compared with Post pain (*NK: P < .05).
EMG During Slow Scaptions of the Arm in the Painful Side During the slow up movement on the injection side, a significant interaction between saline and time was found for the normalized RMS EMG recorded from the ipsilateral upper trapezius (RMANOVA: F[1, 22] = 13.9, P < .002; Fig 5A). Post hoc test showed a significantly decreased upper trapezius activity during the painful condition compared with post pain and the isotonic saline condition (NK: P < .001). However, the post hoc test also revealed a significant, but smaller, decrease ‘‘during’’ compared with ‘‘after’’ for the isotonic saline condition (NK: P < .04). For the ipsilateral anterior deltoid, an interaction between time and saline was found for the normalized RMS EMG (RM-ANOVA: F[1, 22] = 5.2; P < .04) and similarly for the middle deltoid (RM-ANOVA: F[1, 22] = 15.4; P < .001). Although the post hoc test did not support any significant difference for the anterior deltoid, it showed a significant increase in RMS EMG for the middle deltoid during the painful condition when compared with the post pain and the isotonic saline condition (NK: P < .03; Fig 5A). For the down movement, a significant interaction between saline and time was found in RMS EMG
for the ipsilateral upper trapezius (RM-ANOVA: F[1, 22] = 28.4; P < .001), and the post hoc test showed a significant decrease in RMS EMG during the painful condition when compared with post pain and the isotonic saline condition (NK: P < .001; Fig 5B). Furthermore, a slight increase in RMS EMG of the upper trapezius was found in the post condition when comparing to the isotonic saline condition (NK: P < .04). For the ipsilateral erector spinae muscle, a gender interaction was found (RM-ANOVA: F[1, 22] = 4.5; P < .05), with women showing an increased activity during the painful condition when compared with post pain and the isotonic saline condition (NK: P < .04), which was not the case for men (Fig 6A). On the contralateral side, a significant interaction between time and saline was found for the RMS EMG from the external oblique during slow down movements (RMANOVA: F[1, 22] = 5.2; P < .04). The post hoc test showed a significant increase in activity immediately after the painful injection when compared with post pain and isotonic saline conditions (NK: P < .02; Fig 5B). The correlation analysis showed a moderate negative correlation between VAS peak and the ipsilateral upper trapezius activity during the slow up movement (r = .47; n = 24, P < .03).
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Figure 4. Mean RMS EMG values (6standard error of the mean, n = 24) of baseline recordings during slow up (A), slow down (B), and fast up movements (C) of the arm on the side of injection. EMG was recorded from the serratus anterior (SA), upper trapezius (UT), middle trapezius (MT), lower trapezius (LT), anterior deltoid (AD), middle deltoid (MD), external oblique (OE), and erector spinae (ES) from the ipsilateral (Ipsi) and contralateral (Contra) side.
EMG During Slow Scaptions of the Arm Opposite to the Pain During the slow movements on the opposite side of the injection site, a significant interaction was found for the RMS EMG of the ipsilateral lower trapezius for the up (RM-ANOVA: F[1, 22] = 6.72; P < .02) and down movements (RM-ANOVA: F[1, 22] = 5.0; P < .04), but the post hoc test did not detect specific differences.
EMG During Fast Scaptions of the Arm on the Painful Side For the arm movement on the side of injection, a significant interaction between time and saline was found for the RMS EMG of the contralateral upper trapezius (RM-ANOVA: F[1, 19] = 4.7; P < .05) but the post hoc test did not result in significant differences. However, for this muscle, a gender effect was also found (RMANOVA: F[1, 19] = 4.6; P < .05), with the post hoc test showing men having an increased RMS EMG in the
post condition compared with immediately after the isotonic saline injection (NK: P < .03), which was not seen for the painful condition, nor were any changes seen for women (Fig 6B). For the RMS EMG of the contralateral anterior deltoid, an interaction between time and saline was found (RM-ANOVA: F[1, 19] = 5.5; P < .04), but no significant differences were detected in the post hoc test. For all movements, slow and fast, the RM-ANOVA of RMS EMG showing nonsignificant values, revealed by P values ranging from >.993 to >.051, corresponded to an observed power ranging from 5 to 51%. For nonsignificant gender results, the P value ranged from >.999 to >.056, corresponding to an observed power of 5 to 48.9%. The onset of muscle activation was investigated in the fast arm movements on both the side of injection and the opposite side, but no interaction between saline and time was found for any of the 16 muscles. Baseline onsets can be seen for all muscles in Figs 7A and 7B.
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Figure 5. Mean (6standard error of the mean, n = 24) normalized RMS EMG recorded from the upper trapezius (UT), middle deltoid (MD), and external oblique (OE) immediately after injections of hypertonic (Hyp) and isotonic (Iso) saline into the splenius capitis and 5 minutes after the potential pain had vanished (Post pain) in slow up (A) slow down (B) movements. Significant difference compared with the Post condition (*NK: P < .05) and with the isotonic saline condition (#NK: P < .05) is illustrated.
Discussion This study is the first to demonstrate reorganized trunk and axioscapular muscle activities in response to localized and referred pain—evoked by hypertonic saline injection into an intrinsic neck muscle with no direct attachments to the trunk or shoulder girdle—during arm movement. Moreover, the experimental pain caused localized pressure hypoalgesia.
Axioscapular Muscle Activity During Neck Pain During experimental neck pain, reduced muscle activity was recorded in the ipsilateral upper trapezius along with increased activity in the middle deltoid during slow up movements. For slow down movements, a reduced activity was still observed for the upper trapezius, whereas the contralateral external oblique demonstrated increased activity. The reduced activity of the upper trapezius is in line with a previous study showing
decreased EMG activity of the upper trapezius and increased activity of the lower trapezius during repetitive shoulder flexion when pain was induced in the upper trapezius.12 In this study, pain was induced in the splenius capitis, which might be a better experimental model to investigate the effect of neck pain on the axioscapular muscle activity because this muscle is not connected to the scapula and consequently not involved in arm movement.38 However, EMG activity of the splenius capitis was not investigated, and a stabilizing effect on the cervical spine cannot be excluded; such an effect could indirectly affect muscles linking the cervical spine and the scapula during arm movements. In addition, it is not possible to determine if the altered activity of the upper trapezius was due to referred pain in the area or due to pain at the injection site. The decreased activity of the upper trapezius in the present study supports findings by Falla et al10 observing reduced EMG in the upper trapezius in idiopathic neck pain during arm movements. This was interpreted as
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Figure 6. Mean (6standard error of the mean, n = 24) normalized RMS EMG values for both genders recorded from the ipsilateral erector spinae during slow down movement (A, n = 24, 12 women) and from the contralateral upper trapezius during fast up movement (B, n = 21, 10 women) immediately after injections of hypertonic (Hyp) and isotonic (Iso) saline into the splenius capitis and 5 minutes after the potential pain had vanished (Post pain). Significant difference compared with the Post condition (*NK: P < .05) and with other pain conditions (#NK: P < .05) is illustrated. pain causing reduced activity in the agonistic or synergistic muscles and was therefore suggested to be in line with pain adaptation theory.39 This theory would explain the present findings if referred pain in the upper trapezius was the cause of the decreased activity. However, if this was not the case, that theory cannot explain the findings because the experimental pain was induced in the splenius capitis and thereby did not directly affect muscles involved in arm movements. Second, the theory cannot explain changes in nonpainful muscles as seen in this study with increased EMG activity for middle deltoid during the up movement in addition to the increase in the contralateral external oblique and the gender-specific changes in the ipsilateral erector spinae when lowering the arm. Nonetheless, the present findings are in line with the recently proposed updated adaptation theory27 where such redistribution of muscle activity is expected during painful movements to protect from further pain or injury. Another interesting observation is that although reduced during the painful condition, the upper trapezius exhibits a trend toward increased
activity compared with baseline for both up and down movements during the post measurement. This response could be similar to that seen in patients where increased trapezius activity in postexercise conditions is regarded as a sign of altered motor strategy to reduce the painful muscle activity.10 The redistribution of muscle activity during slow movements may also explain the increased difficulty of lifting the arm during the painful condition, which was supported by a negative correlation between pain and muscle activity. In this study, most of the reorganized activities were in muscles directly involved in arm movement and thereby in muscles with much activity,56 whereas the increase in the contralateral external oblique was in a muscle with lower activity, although these levels cannot be directly compared because of anatomical and architectural differences. In regard to gender effects, only the ipsilateral erector spinae showed a gender-specific reorganization during slow down movements, and for fast up movements, this was evident for the contralateral upper trapezius. Movement speed and onset of
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Experimental Neck Pain and Axioscapular Motor Control
Figure 7. Mean (6standard error of the mean, n = 24) baseline onset values during fast up movements of the arm on the side of injection (A) and the noninjection side (B). Onsets are presented as relative values from the anterior deltoid onset on the side of movement. Onsets were recorded from the serratus anterior (SA), upper trapezius (UT), middle trapezius (MT), lower trapezius (LT), anterior deltoid (AD), middle deltoid (MD), external oblique (OE), and erector spinae (ES) from the ipsilateral (Ipsi) and contralateral (Contra) side to the injection.
Christensen, Hirata, and Graven-Nielsen muscle activities were not significantly affected, indicating that the reorganization involved in this type of movements is mainly linked to the activity levels. A study by Helgadottir et al19 evaluating slow scaptions reported a delayed onset of the serratus anterior in a neck pain population when compared with controls, although it was only evident when data were pooled for both arms. In neck pain patients, another study showed delayed muscle onset in the deep cervical flexors during shoulder flexion but not extension compared to controls.13 It was argued that this was due to an altered central strategy for controlling the cervical spine. In other body regions, a delayed onset of specific muscles seems related to tasks challenging postural control, such as delayed onset of the transversus abdominis during standing shoulder flexion in a low back pain population.26 The opposite, an earlier onset, has been seen for the biceps femoris in experimental knee pain during a similar task.50 During fast movements, the reorganized activity caused by neck pain was exclusively gender specific and limited to a contralateral axioscapular muscle when moving the arm on the side of the injection. One possible explanation could be that fast movements do not allow for adaptation or redistribution of muscle activity as seen during slow movements. This difference in EMG activity between 2 related tasks is similar to the findings of Birch et al,2 who induced experimental pain in the extensor carpi ulnaris and reported that only a low-precision task, and not a highprecision task, caused decreased muscle activity during pain. Another explanation could be that unilateral pain is not enough to cause significant changes during fast movements. A previous study on experimental knee pain found that only bilateral pain caused significant difference in total DEMG response.23 It was hypothesized that only bilateral pain was enough to affect a system with multiple degrees of freedom. Although these findings were in knee pain, this might also be true for neck pain, and studies investigating bilateral neck pain are warranted. Gender differences have previously been shown for the trapezius, with men showing a tendency to have higher absolute RMS EMG values.31 Furthermore, studies using experimental pain have caused decreased RMS EMG in the trapezius, with men showing larger reductions16 and women showing reduced shift of muscle activity within the same muscle.9 Nevertheless, this would still not explain the gender difference found in this study, and more studies are needed to ensure that these are truly features of experimental neck pain. As part of the updated pain adaptation theory, it has been proposed that pain causes the nervous system to respond by increasing trunk muscle activity in order to protect the spine, as observed during low back pain.24,27 This is in line with a previous study in which a larger proportion of individuals with neck pain compared to healthy controls displayed abnormal motor control of abdominal muscles, and this was
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proposed as a possible predisposing factor for a later development of low back pain.41 The present study is the first to indicate a direct link between neck pain and altered trunk muscle activity. The redistributed EMG activity found in this study may help explain the disturbed function of the shoulder girdle found in neck pain patients34,44 and supports inclusion of the shoulder girdle in assessment and rehabilitation6,32,34,44,58 but could also indicate that these changes might take place much earlier than what has been observed in patients with chronic conditions. Although the effect sizes of this study are in line with findings in a patient population,10 the clinically relevant change is unknown. Additionally, the relatively low observed power for the nonsignificant findings indicate that part of the results should be interpreted with caution.
Pressure Pain Sensitivity in Neck Muscle Pain The present findings, showing no significant difference between hypertonic and isotonic conditions, are in line with previous studies using hypertonic saline injections into neck muscles and found unaffected PPT in the injected area,17,48 but when a second hypertonic injection was administered to the contralateral side, hypoalgesia was found in areas away from the injection site.17 Studies on chronic neck pain have showed decreased PPTs locally, segmentally, and widespread depending on the subgroup investigated.36,49,53,54 In contrast, the present study found localized hypoalgesia during the painful condition, although it was not significant when compared with the isotonic saline condition. The hypoalgesia immediately after the painful condition is interpreted as a descending inhibitory capacity or conditioned pain modulation, which is a normal response from healthy subjects, whereas conditioned pain modulation has shown less efficiency in persistent painful conditions.57 This is in line with a study assessing acute versus chronic idiopathic neck pain patients, which found that in chronic and not acute pain, PPTs were decreased over the cervical spine and trigeminal nerve trunks.30
Conclusion For the first time it was demonstrated that localized and referred pain evoked by hypertonic saline injection into an intrinsic neck muscle with no direct attachments to the trunk or shoulder girdle caused decreased activity of the upper trapezius while increasing the activity level of the middle deltoid during a standardized arm movement. Moreover, a possible link between neck pain and increased trunk muscle activity has been demonstrated. In combination, such findings may have implications for understanding the complex adaptations in neck pain patients.
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Experimental Neck Pain and Axioscapular Motor Control 17. Ge HY, Madeleine P, Wang K, Arendt-Nielsen L: Hypoalgesia to pressure pain in referred pain areas triggered by spatial summation of experimental muscle pain from unilateral or bilateral trapezius muscles. Eur J Pain 7:531-537, 2003 18. Graven-Nielsen T, Arendt-Nielsen L: Assessment of mechanisms in localized and widespread musculoskeletal pain. Nat Rev Rheumatol 6:599-606, 2010 19. Helgadottir H, Kristjansson E, Einarsson E, Karduna A, Jonsson H Jr: Altered activity of the serratus anterior during unilateral arm elevation in patients with cervical disorders. J Electromyogr Kinesiol 21:947-953, 2011 20. Helgadottir H, Kristjansson E, Mottram S, Karduna A, Jonsson H Jr: Altered alignment of the shoulder girdle and cervical spine in patients with insidious onset neck pain and whiplash-associated disorder. J Appl Biomech 27: 181-191, 2011
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25. Hodges PW, Richardson CA: Altered trunk muscle recruitment in people with low back pain with upper limb movement at different speeds. Arch Phys Med Rehabil 80: 1005-1012, 1999 26. Hodges PW, Richardson CA: Inefficient muscular stabilization of the lumbar spine associated with low back pain. A motor control evaluation of transversus abdominis. Spine (Phila Pa 1976) 21:2640-2650, 1996 27. Hodges PW, Tucker K: Moving differently in pain: A new theory to explain the adaptation to pain. Pain 152:S90-S98, 2011 28. Horak FB, Esselman P, Anderson ME, Lynch MK: The effects of movement velocity, mass displaced, and task certainty on associated postural adjustments made by normal and hemiplegic individuals. J Neurol Neurosurg Psychiatry 47:1020-1028, 1984
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16. Ge HY, Arendt-Nielsen L, Farina D, Madeleine P: Genderspecific differences in electromyographic changes and perceived pain induced by experimental muscle pain during sustained contractions of the upper trapezius muscle. Muscle Nerve 32:726-733, 2005
31. Johansen TI, Samani A, Antle DM, Cote JN, Madeleine P: Gender effects on the coordination of subdivisions of the trapezius muscle during a repetitive box-folding task. Eur J Appl Physiol 113:175-182, 2013
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35. Kasch H, Stengaard-Pedersen K, Arendt-Nielsen L, Staehelin Jensen T: Pain thresholds and tenderness in neck and head following acute whiplash injury: A prospective study. Cephalalgia 21:189-197, 2001
49. Scott D, Jull G, Sterling M: Widespread sensory hypersensitivity is a feature of chronic whiplash-associated disorder but not chronic idiopathic neck pain. Clin J Pain 21: 175, 2005
36. La Touche R, Fernandez-de-Las-Penas C, FernandezCarnero J, Diaz-Parreno S, Paris-Alemany A, ArendtNielsen L: Bilateral mechanical-pain sensitivity over the trigeminal region in patients with chronic mechanical neck pain. J Pain 11:256-263, 2010
50. Shiozawa S, Hirata RP, Graven-Nielsen T: Reorganised anticipatory postural adjustments due to experimental lower extremity muscle pain. Hum Mov Sci 32:1239-1252, 2013
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38. Lippert L, Lippert L: Clinical Kinesiology and Anatomy, 4th ed. Philadelphia, F.A. Davis, 2006 39. Lund JP, Donga R, Widmer CG, Stohler CS: The painadaptation model: A discussion of the relationship between chronic musculoskeletal pain and motor activity. Can J Physiol Pharmacol 69:683-694, 1991 40. Melzack R: The McGill Pain Questionnaire: Major properties and scoring methods. Pain 1:277-299, 1975 41. Moseley GL: Impaired trunk muscle function in subacute neck pain: Etiologic in the subsequent development of low back pain? Man Ther 9:157-163, 2004 42. Ng JK, Kippers V, Richardson CA: Muscle fibre orientation of abdominal muscles and suggested surface EMG electrode positions. Electromyogr Clin Neurophysiol 38:51-58, 1998 43. Oatis CA: Kinesiology: the Mechanics and Pathomechanics of Human Movement. Baltimore, MD, Lippincott Williams & Wilkins, 2009
52. Sterling M, Jull G, Vicenzino B, Kenardy J: Characterization of acute whiplash-associated disorders. Spine (Phila Pa 1976) 29:182, 2004 53. Sterling M, Treleaven J, Edwards S, Jull G: Pressure pain thresholds in chronic whiplash associated disorder: Further evidence of altered central pain processing. J Musculoskelat Pain 10:69-81, 2002 54. Stude P, Nebel K, Ludecke C, Wiese H, Diener HC, Keidel M: Quantification of acute neck pain following whiplash injury by computer-aided pressure algesimetry. Cephalalgia 24:1067-1075, 2004 55. Szeto GP, Straker L, Raine S: A field comparison of neck and shoulder postures in symptomatic and asymptomatic office workers. Appl Ergon 33:75-84, 2002 56. Wickham J, Pizzari T, Stansfeld K, Burnside A, Watson L: Quantifying ‘‘normal’’ shoulder muscle activity during abduction. J Electromyogr Kinesiol 20:212-222, 2010
44. O’Leary S, Falla D, Elliott JM, Jull G: Muscle dysfunction in cervical spine pain: Implications for assessment and management. J Orthop Sports Phys Ther 39:324-333, 2009
57. Yarnitsky D: Conditioned pain modulation (the diffuse noxious inhibitory control-like effect): Its relevance for acute and chronic pain states. Curr Opin Anaesthesiol 23: 611-615, 2010
45. O’Leary S, Falla D, Jull G: The relationship between superficial muscle activity during the cranio-cervical flexion test and clinical features in patients with chronic neck pain. Man Ther 16:452-455, 2011
58. Zakharova-Luneva E, Jull G, Johnston V, O’Leary S: Altered trapezius muscle behavior in individuals with neck pain and clinical signs of scapular dysfunction. J Manipulative Physiol Ther 35:346-353, 2012
The Effect of Experimental Neck Pain on Pressure Pain Sensitivity and Axioscapular Motor Control Steffan W. Christensen, Rogerio P. Hirata, and Thomas Graven-Nielsen Laboratory for Musculoskeletal Pain and Motor Control, Center for Sensory-Motor Interaction (SMI), Department of Health Science and Technology, Aalborg University, Aalborg, Denmark.
Abstract: Clinical neck pain affects pain sensitivity and coordination of neck muscles, but the impact on the shoulder muscles is unclear. This study investigated the effect of experimental neck pain on the activity of the axioscapular muscles during arm movements and changes in pain sensitivity. Experimental neck pain was induced in 24 healthy volunteers by injecting hypertonic saline into the splenius capitis. Isotonic saline was injected as control. Before, during, and after injections, electromyography was recorded bilaterally from 8 muscles during standardized arm movements (140 scapular plane elevation), and the root mean square amplitude was extracted. Likewise, pressure pain thresholds were assessed bilaterally on 3 sites. The root mean square electromyography was decreased for the ipsilateral upper trapezius (P < .01) and increased for the ipsilateral middle deltoid (P < .03) during upward movements. The root mean square electromyography was reduced for the ipsilateral upper trapezius (P < .01) during downward movement, whereas an increase was recorded in the contralateral external oblique (P < .02). At the injection site, the pressure pain threshold increased during pain compared with the post condition (5 minutes after potential pain had subsided; P < .03). In this study, trunk and axioscapular muscle activities were reorganized in response to localized and referred pain evoked by hypertonic saline injection into an intrinsic neck muscle with no direct attachments to the trunk or shoulder girdle. Perspective: Reorganized activity of the axioscapular muscles has been shown previously in neck pain patients and is believed to happen during the transition from acute to chronic pain. The present study demonstrates for the first time that such reorganization may happen acutely, adding to our understanding of the effects of acute neck pain. ª 2015 by the American Pain Society Key words: Neck, shoulder, pain, experimental, axioscapular.
N
eck pain is a frequent problem in the general population,29,34 affecting up to 54% of adults during a 6-month period15 (many of whom will develop prolonged or recurrent symptoms), making this a serious problem and a burden to the health care system.4,15,46 Several studies on neck pain have proposed a link between neck pain and changed motor control of cervical muscles, that is, deep neck flexors and extensors and the sternocleidomastoid.5,8,14,33,45 Moreover, inclusion Received August 17, 2014; Revised December 5, 2014; Accepted January 19, 2015. Internal funding was used for this study. The authors have no conflicts of interests. Address reprint requests to Thomas Graven-Nielsen, DMSc, PhD, Laboratory for Musculoskeletal Pain and Motor Control Center for SensoryMotor Interaction (SMI), Department of Health Science and Technology, Faculty of Medicine, Aalborg University, Fredrik Bajers Vej 7D-3, 9220 Aalborg E, Denmark. E-mail: [email protected] 1526-5900/$36.00 ª 2015 by the American Pain Society http://dx.doi.org/10.1016/j.jpain.2015.01.008
of the shoulder girdle as part of both assessment and targeted neck pain management has been suggested.6,32,34,44,58 This is based on clinical observations of abnormal axioscapular function during upper limb tasks in neck pain patients34,44 and studies showing abnormal shoulder girdle alignment, with neck pain patients displaying protracted shoulders and less scapular upward rotation than healthy controls.20,55 Helgadottir et al19 found reduced activity of the serratus anterior but no changes in the trapezius in neck pain patients during abduction in the scapular plane (scaption). This is in contrast to Falla et al,10 who reported reduced activity in the upper trapezius in neck pain patients during arm movement. Recently, Zakharova-Luneva et al58 could not demonstrate reduced activity in the upper or middle part of the trapezius but found increased activity of the lower part in neck pain patients. These varied findings of different studies could be attributed to the different tasks and movement speeds investigated. Previous studies assessing muscle 367
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activation patterns during arm movements have found these to be related to movement speed, showing faster muscle onset and increased activity during fast movements compared to slow.28,37 In addition, studies have shown that both clinical and experimental pain can affect muscle onsets as well as activity levels,13,19,26,50 and some changes were visible for only fast but not slow movements.25 So far, changes in axioscapular muscle activity during scaption (arm movements in the scapular plane) have been found in patients who have suffered from neck pain for at least 3 months, so it is unknown if acute neck pain causes these changes or if a change in axioscapular muscle activity is a predisposing factor for neck pain. Because of logistical problems recruiting neck pain patients immediately after the initial pain onset, a model utilizing experimental pain might be optimal for investigating the effect of acute neck pain and may indicate relevant changes during the initial stage of clinical neck pain. Along with changes in motor control, localized hyperalgesia to pressure is generally found in neck pain patients when compared with healthy controls.35,36,49,52-54 Interestingly, chronic but not acute idiopathic neck pain patients demonstrated widespread changes with hyperalgesia at the anterior tibial muscle when compared with healthy controls.30 This is in agreement with recent suggestions that a prolonged localized nociception may drive sensitization of central mechanisms, causing spreading sensitization.18 This is in contrast to experimental studies with injection of hypertonic saline into a neck muscle17,48 that found no local changes but instead found evidence of hypoalgesia in the surrounding tissue.17 It is still to be investigated if experimentally induced neck pain causes widespread changes. The purpose of this study was to investigate if experimentally induced neck pain affects motor control of axioscapular muscles during arm movements (scaption) and increases the pain sensitivity when compared to a nonpainful control condition. It was hypothesized that experimental neck pain reorganizes coordination of the axioscapular muscles during slow and fast arm movements. Muscle onsets were expected to be affected during fast movements in a painful condition. Further, segmental hypoalgesia was expected as a result of experimental pain. No gender effects were expected.
Experimental Neck Pain and Axioscapular Motor Control disorders that could influence the results, current use of pain medication, or pregnancy. All subjects had normal pain-free ranges of motion of the neck and shoulder.43 Subjects gave informed consent after having received written and verbal information on the study protocol. The study was conducted in accordance with the Helsinki declaration and was approved by the local ethics committee (N20120018).
Protocol The study used a single-blinded, randomized, crossover design (Fig 1). Subjects were seated in an upright position for muscle activity measurements during scaption or leaning over a bench for pressure algometry assessments. Pressure algometry and electromyography (EMG) were assessed bilaterally, and the order of which measurement was recorded first was randomized in a balanced design. Experimental pain was induced by injecting hypertonic saline into a neck muscle. The side selected for the experimental pain was randomized in a balanced way between the right and left sides. A control injection of isotonic saline was used on the contralateral side. Participants were blinded to which injection they would receive, and the sequence of injections (hypertonic first or isotonic first) was randomized although balanced. The measurements were recorded at baseline, immediately after the injection, and 5 minutes after the potential pain had subsided. Thus, the time between the last 2 recordings was different between the isotonic and hypertonic saline recordings. ’’Post‘‘ recording was conducted 5 minutes after the potential pain had vanished. After the first post recording, there was a gap of 5 minutes before the next baseline were recorded. Data collection was completed in 1 session.
Experimental Neck Muscle Pain Experimental muscle pain was induced in the splenius capitis by injection of sterile hypertonic saline (.5 mL,
Methods Subjects Twenty-five healthy volunteers (13 women) were included. Female participants had a mean age of 25.9 years (standard deviation [SD] = 3.8) and body mass index equal to 22.7 (SD = 2.3), whereas male participants had a mean age of 28 years (SD = 5.4) and a body mass index equal to 23.7 (SD = 3.8). Analysis of demographic data revealed no significant difference of age and body mass index between genders. One participant was left handed. Exclusion criteria were any history of neck or shoulder pain within the past 6 months, signs or symptoms indicating neurologic or rheumatologic
Figure 1. Single-blinded randomized crossover design. Order of saline type or PPT/EMG data collected first was randomized in a balanced way. The measurements were recorded at baseline, immediately after the injection (During), and 5 minutes after the potential pain had subsided (Post).
Christensen, Hirata, and Graven-Nielsen 5.8%). The injection site was found by palpation at the midpoint between the lateral border of the upper trapezius and the posterior border of the sternocleidomastoid at the level of the spinous process C3.11 The injection site was confirmed, and muscle depth was measured using real-time ultrasound imaging (Acuson 128XP10, Native; Siemens Medical Solutions, Malvern, PA). The needle was inserted to a depth equivalent to the middle of the muscle bulk of the splenius capitis where the injection was made. Injection of isotonic saline (.5 mL, .9%) was used as a control condition. The perceived pain intensity was recorded using a 10-cm electronic visual analog scale (VAS) with an external handheld slide, anchored with ‘‘no pain’’ (0 cm) and ‘‘maximum pain’’ (10 cm). Participants were repeatedly reminded to update the VAS between pressure sensitivity measurements or during the intervals between arm movements. Pain duration (time with VAS score > 0), maximum VAS scores (VAS peak), and the area under the VAS-time curve (VAS area) were extracted. After both injections, the participants were asked to complete a McGill Pain Questionnaire describing the quality of perceived pain7,40 and mark the area in which they felt any pain on a body chart. The areas of the body chart drawings were calculated in arbitrary units (a.u.) using a scanning program (VistaMetrix, v.1.38.0; SkillCrest, LLC, Tucson, AZ).
Pressure Algometry Pressure pain thresholds (PPTs) were recorded using a € rby, Sweden) handheld pressure algometer (Somedic, Ho with a 1-cm2 probe (shielded by a disposable latex cover). Pressure was applied progressively at a rate of 30 kPa/s. The threshold was defined as the first time where the perceived pressure became painful and the participants pressed a push button, after which the PPT value was noted. Assessment sites were marked at 1) the injection site, as previously described, over the splenius capitis between the borders of the sternocleidomastoid and the upper trapezius at the level of C3; 2) the temporalis at the intermediate portion35; and 3) over the belly of the extensor carpi radialis brevis just distal to the extensor aponeurosis between the extensor carpi radialis longus and the extensor digitorum.51 The m. temporalis site was chosen as a segmental point because of its innervation by the trigeminal nerve, which has considerable convergence with afferents from C1 to C3, from which the splenius capitis is also innervated (C2–C3).3 Moreover, it is a known site for referred pain from the splenius capitis.48 The extensor carpi radialis brevis site was chosen as an extrasegmental site because of its easy accessibility in the test position (ie, leaning over a bench). For each site, the PPT was measured in triplicates, and the average value was used for the analysis. The assessments for the entire session were always performed first on the site of the first injection followed by the opposite side, allowing an approximately 25-second interval between measurements of specific assessment sites. The PPTs obtained after the in-
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jections were normalized to the respective baseline recordings (100%).
Standardized Arm Movements Participants were sitting in a comfortable upright position with both arms by their side on a customized chair. Feet were placed flat on the floor, and a modified backrest on the chair supported only the sacrum. The posture was visually inspected throughout the study, and subjects were repeatedly reminded to keep an upright posture before a movement series, each lasting no longer than 2 minutes 15 seconds. The arm movement was performed against a flat vertical surface, to which the back of the hand (thumb pointing up) was touching while abducting the stretched arm in the scapular plane, that is, scaption (30 to the frontal plane). A physical marker was placed on the vertical surface, marking the 140 range of motion during scaption. A customized program (Aalborg University, Denmark) provided 3 ‘‘beep’’ cues, which indicated when to start the arm movement, when to be at maximum scaption, and when the arm should be back at the starting position. Both up and down movements lasted 3 seconds without break at the top level. In addition, 3 movements were performed with subjects instructed to initiate the up movement as fast as possible on the sound of the cue signal. The down movement was not investigated for these trials. Six scaptions were done bilaterally, alternating sides (ie, 3 for each side) for each movement with a 6-second break between movements. In the slow scaptions, the time used by subjects to perform the arm movements, that is, from the first cue to the maximum angle and from the maximum angle to the third cue, was monitored using accelerometers (EVAL-ADXL327Z; Analog Devices, Norwood, MA) mounted above the humeral lateral epicondyle. For the fast movements, the time window that was monitored was from the first cue signal to the maximum angle. The extracted durations were averaged among the 3 repetitions for each movement type (slow up, slow down, and fast up) on each side for further analysis. The participants were asked to rate the perceived difficulty of lifting the arm on a 6-point Likert-type scale (0 = ‘‘no problems,’’ 2 = ‘‘minimally difficult,’’ 3 = ‘‘fairly difficult,’’ 4 = ‘‘very difficult,’’ and 5 = ‘‘unable to perform’’).
EMG During Arm Movements The skin was shaved and cleaned before mounting bipolar adhesive surface electrodes (Neuroline 72001-k; Ambu A/S, Ballerup, Denmark) in accordance with the SENIAM (Surface Electromyography for the NonInvasive Assessment of Muscles) recommendations.21 Each pair of electrodes was placed in the direction of the muscle fibers over 8 muscles bilaterally as follows: serratus anterior, anterior to the border of the latissimus dorsi, in the direction of the muscle fibers at the level of ribs 6 to 81; upper trapezius, midpoint on a line from the spinous process of C7 to the acromion22; middle trapezius, midpoint between the medial border of the scapula
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and the spine, at the level of T3 ; lower trapezius, twothirds on the line from the trigonum spinae on scapula toward vertebra T822; anterior deltoid, approximately 2 cm distal and anterior to the acromion on a line toward the thumb22; middle deltoid, over the greatest muscle bulge on a line from the acromion to the lateral epicondyle of the elbow22; erector spinae, approximately 3.5 cm lateral to the spinous process of L122; and external oblique, just below the rib cage on a line connecting the inferior costal margin with the contralateral pubic tubercle.42 The reference electrode (WS1; OT Bioelettronica, Turin, Italy) was placed over the right wrist. The EMG signal was amplified (gain 500), band-width filtered at 25 to 450 Hz, and sampled at 2,048 Hz (OT Bioelettronica). Before further analysis, the raw EMG signals were filtered (Butterworth second order, band-pass 25–450 Hz; MATLAB, Natick, MA) and full-wave rectified. Root mean square (RMS) values were extracted in 2 separate windows of 3 seconds representing the slow up and slow down movements. For the fast movements, this time window was calculated using the time from the first cue signal to the maximum angle from the accelerometer data. EMG onset was automatically detected for the fast movements and quantified using a method previously described in detail by Santello et al.47 In short, epochs for the fast movements were extracted as previously described, and all data points were then continuously integrated using time intervals defined as 1/sample rate (1/2,048 Hz). The integrated EMG (IEMG) was then normalized so that the accumulated IEMG at the end of the task and the time to complete the task receive the value 1. The IEMG line was then compared to a reference line with the slope of 1 (representing the association between normalized IEMG and time). The onset was defined as the time point when the difference between the 2 lines was the greatest: the time point from where a continuous increase of EMG activity is seen and the slope of the curve is >1. Using this method, it was possible to ignore small bursts of activity and to detect the time point where the muscle activity started to increase continuously. A visual inspection of the EMG onset was performed, and if needed, manual correction was allowed. The EMG onsets for all muscles were normalized to the anterior deltoid of the moving arm and an average of the 3 trials used for further analysis.
Statistics Data are presented as mean and standard error of the mean in text and figures. VAS parameters and pain areas on the body chart were compared between the 2 injections using a Wilcoxon test. The data were evaluated in a 2-step procedure where baseline data were analyzed first, and later differences from baseline in the 2 experimental conditions were detected and analyzed. Accelerometer, PPT, and raw RMS EMG data were initially assessed for carryover effect between baselines (before each of the 2 injections) using a repeated measures analysis of variance (RM-ANOVA)
with time (first and second baseline) and, if relevant, assessment site (6 PPT or 16 EMG electrode locations) as dependent factors, and with injection type first (hypertonic or isotonic), injection side first (right or left), and side of investigation (right or left) as between-group factors. For accelerometer and raw RMS EMG data, a separate analysis of baseline data was conducted for each type of arm movement (slow up, slow down, and fast up). Second, baseline data were investigated to ensure comparability between side of injections (or between the opposite sides of the 2 injections) and to identify any baseline gender effect. This was done using an RMANOVA as described above, with time and assessment site for PPT or raw RMS EMG as dependent factors and with side of investigation (injection side or the opposite side) and gender as between-group factors. The analysis for accelerometer and RMS EMG data was conducted separately for each arm movement (slow up, slow down, and fast up). Accelerometer, RMS EMG, and PPT data were normalized to baseline (percentage), and an RM-ANOVA with saline (hypertonic and isotonic) and time (during, after) as dependent factors and with gender as a betweengroup factor was used to analyze the data for all individual EMG and PPT locations and accelerometer data (16 EMG, 6 PPT). This was done for the 2 sides where movements were performed (side of injection and the opposite side) and for each arm movement (slow up, slow down, and fast up). The muscle activity onset data were analyzed using an ANOVA with saline (hypertonic and isotonic) and time (before, during, after) as dependent factors and with gender as a between-group factor. In case of significant factors or interactions, the Newman-Keuls (NK) post hoc test was used accordingly. A post hoc power calculation was conducted to help clarify the strength of PPT and EMG results. In case of significant EMG or PPT findings, Pearson’s correlations were used to investigate associations between VAS peak and the normalized EMG/PPT after the 2 different injection types. The Likert scale scores were compared between the 2 painful conditions using a Fisher’s exact test. STATISTICA 7.0 (StatSoft Inc, Tulsa, OK) was used for all analysis. A P value of .05 was accepted as significant.
Results Of the 25 included participants, data from 1 woman were discarded because of technical problems with the EMG recordings immediately after the painful injection. Accelerometer data (and the related RMS EMG data during fast movements) from 3 subjects had to be discarded because of equipment malfunction.
Experimental Neck Muscle Pain Compared with isotonic saline, injection of hypertonic saline caused a longer pain duration (423 6 21 seconds vs 29 6 14 seconds, P < .001), higher VAS peaks (5.1 6 .5 cm vs .2 6 .1 cm, P < .001), and larger VAS area (1,551 6 357 cm$seconds vs 20 6 12 cm$seconds,
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P < .001). The 3 most common words selected from the McGill Pain Questionnaire after the hypertonic injection were pressing (38% of subjects), intense (29%), and tight (25%), whereas the isotonic injection only caused 2 words to be selected by more than 1 participant, which were pressing (17%) and tight (8%). The perceived pain was distributed distally from the spine of the scapula and up to the base of the skull, with 1 subject perceiving pain in the whole occipital and temporal area (Fig 2). Medially, it was enclosed approximately by the midline, and laterally, it went to the side of the neck. In the shoulder area, it was bordered laterally at the level of the acromioclavicular joint, covering an area approximately the size of the upper half of the trapezius. Two subjects perceived a sensation of pain above the ipsilateral jaw right after the hypertonic saline injection, and 1 subject experienced the same distribution after the isotonic injection. The areas of pain after hypertonic and isotonic saline injections were significantly different in the posterior view (16.8 6 4.8 a.u. vs 1.9 6 .7 a.u., P < .001) and in the lateral view (10.7 6 7.0 a.u. vs .2 6 .2 a.u., P < .006).
neck site on the side of injection revealed a significant RM-ANOVA interaction between time and saline (RM-ANOVA: F[1, 22] = 4.9; P < .04). Post hoc analysis showed a significantly increased PPT immediately after the injection of hypertonic saline compared with 5 minutes after the pain had subsided (NK: P < .03; Fig 3), but no significant differences were found when compared to the control condition (isotonic saline). A significant interaction was also found for the PPT assessed at the extensor carpi radialis brevis on the side of injection (RM-ANOVA: F[1,22] = 4.7; P < .04), but the post hoc test did not indicate any significant differences. On the side opposite to the injection sites, an interaction between saline and time was found for the neck site (RM-ANOVA: F[1,22] = 4.3; P < .05), but no significant differences were found after the post hoc test. No significant correlation was found between VAS peak and PPT measurements. The post hoc power analysis for the nonsignificant PPT results with P values ranging from >.603 to <.054 corresponded to an observed power of 8 to 49.7%.
Pressure Pain Sensitivity
Performance of Scaption
No significant difference was found between the 2 baseline PPT recordings (before each injection). The average baseline PPTs recorded bilaterally at the neck, temporalis, and extensor carpi radialis brevis were 170 6 7 kPa, 265 6 9 kPa, and 275 6 8 kPa, respectively. Analysis of the normalized PPT at the
During the painful contractions, 33% of subjects indicated a Likert scale score of 1 or higher, whereas none of the subjects scored higher than 0 in the control condition (isotonic saline), which was significantly different (Fisher: P < .004). The time from the cue signal to the maximum angle (slow and fast movement) and from the maximum angle to the last cue signal (only slow movement) was not different in the 2 baseline recordings. Analysis of the normalized movement time did not show any difference compared to baseline for the slow up (3.2 6 .1 seconds), slow down (2.8 6 .1 seconds), and fast up (1.6 6 .1 seconds) movements on the injection side or for the slow up (3.3 6 .0 seconds), down (2.7 6 .0 seconds), and fast up (1.6 6 .1 seconds) movements on the noninjection side for any of the conditions.
EMG During Nonpainful Scaption
Figure 2. Superimposed body chart drawings (n = 24) of the pain distribution after saline injection into the splenius capitis. Drawings on the left illustrate the pain area after injections of isotonic saline and on the right after hypertonic saline injections.
No significant difference was found in the RMS EMG from all muscles between the 2 baseline recordings during slow or fast arm movements. The prime movers of the glenohumeral joint, the middle and anterior deltoids, showed the largest RMS EMG values, closely followed by the muscles responsible for controlling and moving the scapula (Fig 4A). The lowest RMS EMG activity on the ipsilateral side of movement was shown by the external obique, followed by the erector spinae. On the side contralateral to the movement, the 3 parts of the trapezius showed the highest RMS EMG values, though substantially less compared with the ipsilateral muscles. When comparing the RMS EMG of the slow up and slow down movements, a reduction is seen for most muscles (Figs 4A and 4B). In general, higher RMS EMG values were seen after fast up compared with slow up movements (Figs 4A and 4C).
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Figure 3. Mean (6standard error of the mean, n = 24) normalized PPTs recorded at the injection side (A) and contralateral side (B) over the splenius capitis, temporalis (Temp), and extensor carpi radialis brevis (ECRB) immediately after injections of hypertonic (Hyp) and isotonic (Iso) saline and 5 minutes after the potential pain had vanished (Post pain). Significantly increased compared with Post pain (*NK: P < .05).
EMG During Slow Scaptions of the Arm in the Painful Side During the slow up movement on the injection side, a significant interaction between saline and time was found for the normalized RMS EMG recorded from the ipsilateral upper trapezius (RMANOVA: F[1, 22] = 13.9, P < .002; Fig 5A). Post hoc test showed a significantly decreased upper trapezius activity during the painful condition compared with post pain and the isotonic saline condition (NK: P < .001). However, the post hoc test also revealed a significant, but smaller, decrease ‘‘during’’ compared with ‘‘after’’ for the isotonic saline condition (NK: P < .04). For the ipsilateral anterior deltoid, an interaction between time and saline was found for the normalized RMS EMG (RM-ANOVA: F[1, 22] = 5.2; P < .04) and similarly for the middle deltoid (RM-ANOVA: F[1, 22] = 15.4; P < .001). Although the post hoc test did not support any significant difference for the anterior deltoid, it showed a significant increase in RMS EMG for the middle deltoid during the painful condition when compared with the post pain and the isotonic saline condition (NK: P < .03; Fig 5A). For the down movement, a significant interaction between saline and time was found in RMS EMG
for the ipsilateral upper trapezius (RM-ANOVA: F[1, 22] = 28.4; P < .001), and the post hoc test showed a significant decrease in RMS EMG during the painful condition when compared with post pain and the isotonic saline condition (NK: P < .001; Fig 5B). Furthermore, a slight increase in RMS EMG of the upper trapezius was found in the post condition when comparing to the isotonic saline condition (NK: P < .04). For the ipsilateral erector spinae muscle, a gender interaction was found (RM-ANOVA: F[1, 22] = 4.5; P < .05), with women showing an increased activity during the painful condition when compared with post pain and the isotonic saline condition (NK: P < .04), which was not the case for men (Fig 6A). On the contralateral side, a significant interaction between time and saline was found for the RMS EMG from the external oblique during slow down movements (RMANOVA: F[1, 22] = 5.2; P < .04). The post hoc test showed a significant increase in activity immediately after the painful injection when compared with post pain and isotonic saline conditions (NK: P < .02; Fig 5B). The correlation analysis showed a moderate negative correlation between VAS peak and the ipsilateral upper trapezius activity during the slow up movement (r = .47; n = 24, P < .03).
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Figure 4. Mean RMS EMG values (6standard error of the mean, n = 24) of baseline recordings during slow up (A), slow down (B), and fast up movements (C) of the arm on the side of injection. EMG was recorded from the serratus anterior (SA), upper trapezius (UT), middle trapezius (MT), lower trapezius (LT), anterior deltoid (AD), middle deltoid (MD), external oblique (OE), and erector spinae (ES) from the ipsilateral (Ipsi) and contralateral (Contra) side.
EMG During Slow Scaptions of the Arm Opposite to the Pain During the slow movements on the opposite side of the injection site, a significant interaction was found for the RMS EMG of the ipsilateral lower trapezius for the up (RM-ANOVA: F[1, 22] = 6.72; P < .02) and down movements (RM-ANOVA: F[1, 22] = 5.0; P < .04), but the post hoc test did not detect specific differences.
EMG During Fast Scaptions of the Arm on the Painful Side For the arm movement on the side of injection, a significant interaction between time and saline was found for the RMS EMG of the contralateral upper trapezius (RM-ANOVA: F[1, 19] = 4.7; P < .05) but the post hoc test did not result in significant differences. However, for this muscle, a gender effect was also found (RMANOVA: F[1, 19] = 4.6; P < .05), with the post hoc test showing men having an increased RMS EMG in the
post condition compared with immediately after the isotonic saline injection (NK: P < .03), which was not seen for the painful condition, nor were any changes seen for women (Fig 6B). For the RMS EMG of the contralateral anterior deltoid, an interaction between time and saline was found (RM-ANOVA: F[1, 19] = 5.5; P < .04), but no significant differences were detected in the post hoc test. For all movements, slow and fast, the RM-ANOVA of RMS EMG showing nonsignificant values, revealed by P values ranging from >.993 to >.051, corresponded to an observed power ranging from 5 to 51%. For nonsignificant gender results, the P value ranged from >.999 to >.056, corresponding to an observed power of 5 to 48.9%. The onset of muscle activation was investigated in the fast arm movements on both the side of injection and the opposite side, but no interaction between saline and time was found for any of the 16 muscles. Baseline onsets can be seen for all muscles in Figs 7A and 7B.
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Figure 5. Mean (6standard error of the mean, n = 24) normalized RMS EMG recorded from the upper trapezius (UT), middle deltoid (MD), and external oblique (OE) immediately after injections of hypertonic (Hyp) and isotonic (Iso) saline into the splenius capitis and 5 minutes after the potential pain had vanished (Post pain) in slow up (A) slow down (B) movements. Significant difference compared with the Post condition (*NK: P < .05) and with the isotonic saline condition (#NK: P < .05) is illustrated.
Discussion This study is the first to demonstrate reorganized trunk and axioscapular muscle activities in response to localized and referred pain—evoked by hypertonic saline injection into an intrinsic neck muscle with no direct attachments to the trunk or shoulder girdle—during arm movement. Moreover, the experimental pain caused localized pressure hypoalgesia.
Axioscapular Muscle Activity During Neck Pain During experimental neck pain, reduced muscle activity was recorded in the ipsilateral upper trapezius along with increased activity in the middle deltoid during slow up movements. For slow down movements, a reduced activity was still observed for the upper trapezius, whereas the contralateral external oblique demonstrated increased activity. The reduced activity of the upper trapezius is in line with a previous study showing
decreased EMG activity of the upper trapezius and increased activity of the lower trapezius during repetitive shoulder flexion when pain was induced in the upper trapezius.12 In this study, pain was induced in the splenius capitis, which might be a better experimental model to investigate the effect of neck pain on the axioscapular muscle activity because this muscle is not connected to the scapula and consequently not involved in arm movement.38 However, EMG activity of the splenius capitis was not investigated, and a stabilizing effect on the cervical spine cannot be excluded; such an effect could indirectly affect muscles linking the cervical spine and the scapula during arm movements. In addition, it is not possible to determine if the altered activity of the upper trapezius was due to referred pain in the area or due to pain at the injection site. The decreased activity of the upper trapezius in the present study supports findings by Falla et al10 observing reduced EMG in the upper trapezius in idiopathic neck pain during arm movements. This was interpreted as
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Figure 6. Mean (6standard error of the mean, n = 24) normalized RMS EMG values for both genders recorded from the ipsilateral erector spinae during slow down movement (A, n = 24, 12 women) and from the contralateral upper trapezius during fast up movement (B, n = 21, 10 women) immediately after injections of hypertonic (Hyp) and isotonic (Iso) saline into the splenius capitis and 5 minutes after the potential pain had vanished (Post pain). Significant difference compared with the Post condition (*NK: P < .05) and with other pain conditions (#NK: P < .05) is illustrated. pain causing reduced activity in the agonistic or synergistic muscles and was therefore suggested to be in line with pain adaptation theory.39 This theory would explain the present findings if referred pain in the upper trapezius was the cause of the decreased activity. However, if this was not the case, that theory cannot explain the findings because the experimental pain was induced in the splenius capitis and thereby did not directly affect muscles involved in arm movements. Second, the theory cannot explain changes in nonpainful muscles as seen in this study with increased EMG activity for middle deltoid during the up movement in addition to the increase in the contralateral external oblique and the gender-specific changes in the ipsilateral erector spinae when lowering the arm. Nonetheless, the present findings are in line with the recently proposed updated adaptation theory27 where such redistribution of muscle activity is expected during painful movements to protect from further pain or injury. Another interesting observation is that although reduced during the painful condition, the upper trapezius exhibits a trend toward increased
activity compared with baseline for both up and down movements during the post measurement. This response could be similar to that seen in patients where increased trapezius activity in postexercise conditions is regarded as a sign of altered motor strategy to reduce the painful muscle activity.10 The redistribution of muscle activity during slow movements may also explain the increased difficulty of lifting the arm during the painful condition, which was supported by a negative correlation between pain and muscle activity. In this study, most of the reorganized activities were in muscles directly involved in arm movement and thereby in muscles with much activity,56 whereas the increase in the contralateral external oblique was in a muscle with lower activity, although these levels cannot be directly compared because of anatomical and architectural differences. In regard to gender effects, only the ipsilateral erector spinae showed a gender-specific reorganization during slow down movements, and for fast up movements, this was evident for the contralateral upper trapezius. Movement speed and onset of
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Figure 7. Mean (6standard error of the mean, n = 24) baseline onset values during fast up movements of the arm on the side of injection (A) and the noninjection side (B). Onsets are presented as relative values from the anterior deltoid onset on the side of movement. Onsets were recorded from the serratus anterior (SA), upper trapezius (UT), middle trapezius (MT), lower trapezius (LT), anterior deltoid (AD), middle deltoid (MD), external oblique (OE), and erector spinae (ES) from the ipsilateral (Ipsi) and contralateral (Contra) side to the injection.
Christensen, Hirata, and Graven-Nielsen muscle activities were not significantly affected, indicating that the reorganization involved in this type of movements is mainly linked to the activity levels. A study by Helgadottir et al19 evaluating slow scaptions reported a delayed onset of the serratus anterior in a neck pain population when compared with controls, although it was only evident when data were pooled for both arms. In neck pain patients, another study showed delayed muscle onset in the deep cervical flexors during shoulder flexion but not extension compared to controls.13 It was argued that this was due to an altered central strategy for controlling the cervical spine. In other body regions, a delayed onset of specific muscles seems related to tasks challenging postural control, such as delayed onset of the transversus abdominis during standing shoulder flexion in a low back pain population.26 The opposite, an earlier onset, has been seen for the biceps femoris in experimental knee pain during a similar task.50 During fast movements, the reorganized activity caused by neck pain was exclusively gender specific and limited to a contralateral axioscapular muscle when moving the arm on the side of the injection. One possible explanation could be that fast movements do not allow for adaptation or redistribution of muscle activity as seen during slow movements. This difference in EMG activity between 2 related tasks is similar to the findings of Birch et al,2 who induced experimental pain in the extensor carpi ulnaris and reported that only a low-precision task, and not a highprecision task, caused decreased muscle activity during pain. Another explanation could be that unilateral pain is not enough to cause significant changes during fast movements. A previous study on experimental knee pain found that only bilateral pain caused significant difference in total DEMG response.23 It was hypothesized that only bilateral pain was enough to affect a system with multiple degrees of freedom. Although these findings were in knee pain, this might also be true for neck pain, and studies investigating bilateral neck pain are warranted. Gender differences have previously been shown for the trapezius, with men showing a tendency to have higher absolute RMS EMG values.31 Furthermore, studies using experimental pain have caused decreased RMS EMG in the trapezius, with men showing larger reductions16 and women showing reduced shift of muscle activity within the same muscle.9 Nevertheless, this would still not explain the gender difference found in this study, and more studies are needed to ensure that these are truly features of experimental neck pain. As part of the updated pain adaptation theory, it has been proposed that pain causes the nervous system to respond by increasing trunk muscle activity in order to protect the spine, as observed during low back pain.24,27 This is in line with a previous study in which a larger proportion of individuals with neck pain compared to healthy controls displayed abnormal motor control of abdominal muscles, and this was
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proposed as a possible predisposing factor for a later development of low back pain.41 The present study is the first to indicate a direct link between neck pain and altered trunk muscle activity. The redistributed EMG activity found in this study may help explain the disturbed function of the shoulder girdle found in neck pain patients34,44 and supports inclusion of the shoulder girdle in assessment and rehabilitation6,32,34,44,58 but could also indicate that these changes might take place much earlier than what has been observed in patients with chronic conditions. Although the effect sizes of this study are in line with findings in a patient population,10 the clinically relevant change is unknown. Additionally, the relatively low observed power for the nonsignificant findings indicate that part of the results should be interpreted with caution.
Pressure Pain Sensitivity in Neck Muscle Pain The present findings, showing no significant difference between hypertonic and isotonic conditions, are in line with previous studies using hypertonic saline injections into neck muscles and found unaffected PPT in the injected area,17,48 but when a second hypertonic injection was administered to the contralateral side, hypoalgesia was found in areas away from the injection site.17 Studies on chronic neck pain have showed decreased PPTs locally, segmentally, and widespread depending on the subgroup investigated.36,49,53,54 In contrast, the present study found localized hypoalgesia during the painful condition, although it was not significant when compared with the isotonic saline condition. The hypoalgesia immediately after the painful condition is interpreted as a descending inhibitory capacity or conditioned pain modulation, which is a normal response from healthy subjects, whereas conditioned pain modulation has shown less efficiency in persistent painful conditions.57 This is in line with a study assessing acute versus chronic idiopathic neck pain patients, which found that in chronic and not acute pain, PPTs were decreased over the cervical spine and trigeminal nerve trunks.30
Conclusion For the first time it was demonstrated that localized and referred pain evoked by hypertonic saline injection into an intrinsic neck muscle with no direct attachments to the trunk or shoulder girdle caused decreased activity of the upper trapezius while increasing the activity level of the middle deltoid during a standardized arm movement. Moreover, a possible link between neck pain and increased trunk muscle activity has been demonstrated. In combination, such findings may have implications for understanding the complex adaptations in neck pain patients.
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