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The relation between neuromuscular control and pain intensity in fibromyalgia
Journal of Electromyography and Kinesiology 21 (2011) 519–524
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Journal of Electromyography and Kinesiology journal homepage: www.elsevier.com/locate/jelekin
The relation between neuromuscular control and pain intensity in fibromyalgia Andreas Holtermann a,⇑, Christer Grönlund b, Karin Roeleveld c, Björn Gerdle d,e a
National Research Centre for the Working Environment, Lersø Parkallé 105, DK-2100 Copenhagen, Denmark Biomedical Engineering and Informatics, Radiation Sciences, Umeå University, SE-901 85 Umeå, Sweden c Department of Human Movement Science, Dragvoll, Norwegian University of Science and Technology, N-7491 Trondheim, Norway d Rehabilitation Medicine, Department of Clinical and Experimental Medicine, Linköping University, SE-581 85 Linköping, Sweden e Pain and Rehabilitation Centre, University Hospital, SE-581 85 Linköping, Sweden b
a r t i c l e
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Article history: Received 30 August 2010 Received in revised form 14 January 2011 Accepted 14 January 2011
Keywords: Neuromuscular activation Musculoskeletal disorder Muscle pain Fibromyalgia Differential activations
a b s t r a c t Fibromyalgia patients are shown to have a different neuromuscular control (differential activation) than healthy persons. Before clinical trials can be initiated, the relation between differential activations and pain intensity among fibromyalgia patients needs to be investigated. Twenty-seven fibromyalgia patients performed 3 min bilateral shoulder elevations with different loads (0–4 kg) with a high-density surface electromyographical (EMG) grid placed on the upper trapezius. Differential activation was quantified by the power spectral median frequency of the difference in EMG amplitude between the cranial and caudal parts of the upper trapezius. The average duration of the differential activation was described by the inverse of the median frequency of the differential activations. The relation between frequency and duration of differential activations as an average of the 4 loads and pain intensity the same day prior to the experiment was explored by Pearson’s correlation coefficients. A strong negative relation between frequency of differential activations and pain intensity (R = 0.67, p < 0.001) and a strong positive association between duration of differential activations and pain intensity (R = 0.66, p < 0.001) were found. The significant association between frequency and duration of differential activations and pain intensity among the fibromyalgia patients indicates a relation between this neuromuscular control pattern and pain intensity. This finding support initiation of clinical trials for investigating effects on pain intensity of modifying differential activations among fibromyalgia patients. Ó 2011 Elsevier Ltd. All rights reserved.
1. Introduction The association between neuromuscular control and chronic muscle pain has been a topic of clinical interest for decades (Hough, 1902). Early observations of enhanced muscle activity and tender muscles at clinical examination in persons with pain (Abraham, 1977; Asmussen, 1956; Cobb et al., 1975; De Vries, 1966) supported the viscous circle model (Travell et al., 1942). This model proposes that a painful condition causes reflexive mediated muscle hyperactivity (spasm) which further enhances pain and dysfunction (Johansson and Sojka, 1991). However, acute muscle pain has predominantly been observed to inhibit rather than increase muscle activity (Falla et al., 2007; Farina et al., 2004; Lund et al., 1991; Svensson et al., 1998). Therefore, the pain adaptation model (Lund et al., 1991) has received increasingly attention. This model states that a painful condition reduces muscle activity when active as agonist and increases activity when active as antagonist which would limit movement and protect against further injury (Lund et al., 1991). ⇑ Corresponding author. Tel.: +45 39165352. E-mail address: [email protected] (A. Holtermann). 1050-6411/$ - see front matter Ó 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.jelekin.2011.01.004
However, neither of the models are unequivocally supported by the literature, and the changes in muscle activity is considered to be more complicated than stated in the pain adaptation model (Murray and Peck, 2007). Therefore, the integrated pain adaptation model has been proposed (Murray and Peck, 2007). The model emphasizes how the redundancy of skeletal muscles provides many motor unit subpopulations available for performing a task, making different recruitment strategies plausible for avoiding or minimizing pain. An example of such a recruitment strategy is reciprocal reversals of activity between regions within a single muscle, defined as differential activation (Chanaud et al., 1991). Accordingly, we recently reported a lowered frequency of differential activations (shifts in activity between the caudal and cranial parts) of the upper trapezius in fibromyalgia patients compared with healthy controls (Gerdle et al., 2010). The lower frequency (measured as a lowered median frequency domain) of differential activations in fibromyalgia patients may cause overexertion and fatigue of the muscle region, and therefore be a plausible explanation for the maintenance of the peripheral nociception and the central alterations (i.e., central hyperexcitability and altered descending inhibition) resulting in severe pain of the fibromyalgia patients (Gerdle et al., 2010).
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This observation of a different neuromuscular control between fibromyalgia patients and healthy persons may provide the basis for treatment strategies for fibromyalgia. However, before clinical trials for investigating effects on pain intensity from modulating differential activations among fibromyalgia patients should be initiated, it is a need to know if and how the frequency of differential activation is related to the pain intensity of the fibromyalgia patients. Moreover, although the relation between neuromuscular control and pain intensity has been debated for decades (Hough, 1902; Lund et al., 1991; Travell et al., 1942), documentation of a relation between neuromuscular control and pain intensity is lacking. Therefore, the aim of this study was to investigate the relation between frequency of differential activations and pain intensity among fibromyalgia patients. 2. Materials and methods 2.1. Subjects Female patients with fibromyalgia (N = 29; age: 37 ± 5 years, weight: 69.3 ± 9.5 kg, height: 166 ± 5 cm) were recruited from the Pain and Rehabilitation Centre, University Hospital, Linköping, Sweden. It should be noted that not all of these patients were able to perform all tasks (see Section 3, drop-out and activity levels at the different loads). The patients were offered participation in the study after examination of medical records, positive response to information letter, and a phone conversation with a physician. The patients were clinically diagnosed according to the ACR criteria of 1990 for the classification of fibromyalgia (FM) (Wolfe et al., 1990). The mean duration of FM was 6.6 ± 3.2 years (minimum 2 years. Descriptive data of the fibromyalgia patients (i.e., age, anthropometric data, pain intensity recent week (minimum, average and maximum intensity), and data from ultrasound recording) have been presented previously (Gerdle et al., 2008). All subjects gave written informed consent to participate. The study conformed to the Declaration of Helsinki and the study protocol was approved by the local ethics committee at Linköping University. 2.2. Experimental setup First, a high-density surface electromyographic (EMG) electrode-grid (modified ActiveOne, BioSemi, Amsterdam, Netherlands) consisting of 13 by 10 active electrodes (0.5 cm interelectrode distance), covering 6 4.5 cm of the skin surface was placed on the skin above the right trapezius muscle in the middle of the line between the processus spinosus of the seventh cervical vertebra and the lateral edge of acromion. The base of the electrode-grid device is concave and semiflexible and thereby fitted well with the convex recordings area of the upper trapezius muscle. In this way, the recorded signals of all subjects were not affected by muscle–tendon transitions and similarly affected by the motor end plate region. To generate a stable pressure between electrodes and the skin, the electrode grid was held in place by two elastic straps around the shoulder and torso of the subject. The surface EMG signals were recorded from all electrodes (monopolar) with a common reference on the processus spinosus of the seventh cervical vertebra at 2048 Hz. Then, the subjects performed symmetrical bilateral shoulder elevations with different loads. The loads were applied through the attachment of different weights on a harness. The harness consisted of 2 belts hanging on both shoulders on the level of the acromion to allow attachment of the weights. One additional belt was placed around the torso in order to fixate the other two belts. After attaching the harness and weights, the subjects were asked to lift the weights such that the shoulders were in a horizontal plane,
and to hold this position for 3 min. Weights of 0, 1, 2, and 4 kg were applied successively. The subjects were given 1-min rest between each contraction. The choice of absolute weights and not relative weights in relation to maximum performance was based on the difficulties for obtaining valid maximum voluntary contractions (MVC) in FM patients due to pain and/or psychological aspects such as fear-avoidance or kinesiophobia. 2.3. Ultrasound recordings Ultrasound measurements were taken of the thickness (mm) of the trapezius muscle and the subcutaneous soft tissue (skin and fat tissue taken together) 2 cm lateral of the midpoint between the seventh process of the cervical spine and the lateral part of the acromion process using an Acuson 128XP/10 (Siemens). 2.4. Pain intensity recordings The participants reported the pain intensity prior to the experiment (the same day) on a 100 mm visual analogue scale (VAS). As previously presented, the pain intensity prior to the experiment was highly correlated with the average pain intensity the last week (Gerdle et al., 2008). 2.5. Surface EMG analysis – quantification of differential activation The differential activation analysis was previously described (Gerdle et al., 2010). The essence of the analysis was to examine the temporal changes of the difference in myoelectric activity between two regions within a muscle. While the EMG signals were recorded using a 2-D high-density EMG grid, a large part of the processing (most of step III below) was undertaken in order to reduce the data to signals originating from the caudal and cranial regions of the trapezius muscle. Multiple channels covering a large area were recorded to get a better estimate of the activation of the two muscle parts (Staudenmann et al., 2005). In short, the procedure involved; (I) Pre-processing: Prior to analysis, poor quality signals were omitted (Grönlund et al., 2005). The remaining signals were high-pass filtered at 10 Hz, and bipolar spatial filtering in the fiber direction (medial–lateral) was carried out. (II) Muscle activity: The muscle activity level of the EMG signals was described using the root-mean-square (RMS), calculated in 0.5 s non-overlapping time-windows. In order to compare the activity between regions within the muscle, the muscle activity signals were de-trended and normalized to their corresponding maximum RMS values (maximum over the whole 3 min contraction). (III) Muscle activity in the cranial – caudal direction: Muscle activity in the cranial – caudal direction (perpendicular to fibre orientation) was calculated by averaging the muscle activity recorded by electrodes of the grid along the fibre orientation (medial–lateral), providing 10 activity signals in the cranial – caudal direction. (IV) Activity difference: The difference in the normalized muscle activity between the cranial (average of the three most superior electrode positions) and the caudal (average of the three most inferior electrode positions) regions of the upper trapezius was calculated. (V) Median frequency and average duration of the differential activations: Differential activation was quantified using the power spectral median frequency (MDF) of the whole activity difference signal. The inverse of the median frequency of the differential activations was calculated to quantify the average duration of the differential activations.
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2.6. Statistics All statistical analyses were performed using MATLAB (The Mathworks, Nattick, USA; version 2007b). For variables and indices mean value with one standard deviation (±1 SD) are generally reported. The relation between frequency of differential activation and pain intensity was investigated with Pearson’s correlation coefficients. For investigating differences in median frequency of differential activation at the different loads, a 1-way ANOVA was performed among the fibromyalgia patients with lowest (n 6 13) and highest (n 6 12) pain intensity, respectively. A probability of 60.05 (two-tailed) was used as criteria for significance in all tests. 3. Results 3.1. Pain intensity and anthropometric data These data of the fibromyalgia patients are previously reported (Gerdle et al., 2010, 2008). The pain intensity prior to the experiment was 35 ± 21 mm according to a 100 mm VAS scale. The average thickness of the trapezius muscle was 11.7 ± 2.4 mm over the examination area of the trapezius. The thickness of the superjacent tissues (skin and subcutaneous tissue) was 6.6 ± 1.6 mm over the examination area. 3.2. Drop-outs and activity levels at the different load levels These data of the fibromyalgia patients are previously reported (Gerdle et al., 2010, 2008). Among the fibromyalgia patients (N = 29), 2 (6.9%), 2 (6.9%), 4 (13.8%), and 8 (27.6%) patients were not able to perform the tasks during 3 min with the 4 different external loads, respectively, and were therefore excluded in the subsequent analyses for these load levels. The activity levels of the fibromyalgia patients at the 4 different load levels (0, 1, 2 and 4 kg) were 0.54 ± 0.24, 0.57 ± 0.32, 0.68 ± 0.33 and 0.82 ± 0.41 mV. 3.3. Frequency and duration of differential activations versus pain intensity Fig. 1 illustrates typical examples of a normalized muscle activity from the high-density EMG recording from a fibromyalgia patient with low pain intensity (A) and a fibromyalgia patient with high pain intensity (B) performing a 1 kg weight of isometric shoulder elevation. The lower frequency (MDF) of differential activation of the fibromyalgia patient with low pain intensity (Fig. 1A
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and C) compared with the fibromyalgia patient with high pain intensity (Fig. 1B and D) is clearly demonstrated. The association between frequency of differential activations between the caudal and cranial regions of the trapezius muscle and pain intensity of the fibromyalgia patients at the four load levels are presented in Fig. 2. Significant negative associations between frequency of differential activations and pain intensity were found for 3 (i.e., 0, 2 and 4 kg) of the 4 loads (p < 0.05). Moreover, the frequency of differential activations as a mean of all loads and pain intensity among the fibromyalgia patients was highly significant (R = 0.67, p < 0.001) (Fig. 3). Accordingly, significant positive associations between duration of differential activations and pain intensity were found for 3 (i.e., 0, 2 and 4 kg) of the 4 loads (p < 0.05). The duration of differential activations as a mean of all loads and pain intensity among the fibromyalgia patients was highly significant (R = 0.66, p < 0.001) (Fig. 3). Table 1 illustrates the median frequency of differential activation in the fibromyalgia patients with lowest (n 6 13) and highest (n 6 12) pain intensity at the different loads. No significant differences in median frequency of differential activation at the different loads were observed among those with lowest (p = 0.66) and highest (p = 0.74) pain intensity. 4. Discussion The main finding of this study was the observed significant association between frequency and duration of differential activations and pain intensity among fibromyalgia patients indicating a close relation between this neuromuscular activation pattern and pain intensity. The observed association between frequency and duration of differential activations and pain intensity among fibromyalgia patients extends upon the previous observations that fibromyalgia patients have a lower frequency and longer duration of differential activation compared with healthy controls (Gerdle et al., 2010). The observation that a low frequency and long duration of differential activation not only differs between healthy controls and fibromyalgia patients, but that there exists a relation between frequency and duration of differential activations and pain intensity among the fibromyalgia patients supports the clinical significance of these electromyographic findings. The findings of this study can be caused by 2 mechanisms. First, a low frequency and long duration of differential activation of activity within the upper trapezius may be an underlying neuromuscular control mechanism associated with increased risk for acute and chronic musculoskeletal symptoms. This would further
Fig. 1. Examples of activity difference in normalized activity between caudal and cranial regions for a subject with low and high pain (A and B, respectively). C and D present the corresponding power spectral density estimates (psd) of the signals in A and B, respectively. The values of the estimated median frequencies (MDF) of the difference in activity between the caudal and cranial regions are also given in C and D (dotted vertical lines). Its inverse was used to calculate the corresponding duration. For illustrational purpose, only one minute of the total three minutes is shown in A and B.
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Fig. 2. Median frequency (MDF) of the difference in activity between the caudal and cranial regions of the trapezius muscle as function of pain intensity (VAS) at the different load levels.
Fig. 3. Median frequency (MDF) (A) and duration (B) of the difference in activity between the caudal and cranial regions of the trapezius muscle as function of pain intensity (VAS) after averaging over load levels.
Table 1 Median frequency of differential activation in fibromyalgia patients with lowest (n 6 13) and highest (n 6 12) pain intensity; mean values ±1 standard deviation (SD) and minimum and maximum values. At the bottom row, results of the 1-way ANOVA statistical comparisons (p-values) of median frequency of differential activations between the load levels for the subjects with lowest and highest pain intensity are presented. Variable and load
Frequency (Hz) 0 kg 1 kg 2 kg 4 kg p-Value
Lowest pain
Highest pain
Mean ± SD
Min–Max
Mean ± SD
Min–Max
0.39 0.35 0.36 0.39 0.66
0.28–0.53 0.12–0.49 0.17–0.48 0.23–0.56
0.32 0.32 0.28 0.34 0.74
0.14–0.53 0.14–0.60 0.15–0.42 0.16–0.60
(0.08) (0.11) (0.11) (0.09)
(0.12) (0.14) (0.09) (0.14)
support that the ability to shift activity between regions within the upper trapezius may be a preventive mechanism for avoiding
reflexive mediated muscle hyperactivity from acute painful condition further enhancing pain and a chronic condition (Johansson and Sojka, 1991). An alternative mechanism is that the observed relation between differential activations and pain intensity among fibromyalgia patients may be a result of intensity-related effects of the chronic painful condition on the central nervous system (central sensitizing processes, alterations in function of neuromatrix of pain in the brain or in descending inhibition) (Banic et al., 2004; Giesecke et al., 2004; Gracely et al., 2002; Graven-Nielsen et al., 2000) and/or in the muscle (Bengtsson, 2002; Elvin et al., 2006; Sandberg et al., 2005; Staud et al., 2009). To get more insight in to the mechanism behind the relation between neuromuscular control strategies and chronic pain, prospective investigations are necessary. However, very few exist (Veiersted et al., 1993). Moreover, clinical trials can investigate the potential pain relieving effects of modifying differential activations among fibromyalgia patients. Differential activation of different parts of the trapezius
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muscle can be learned by electromyographic biofeedback among healthy persons (Holtermann et al., 2010, 2009). Therefore, modifications of differential activations among fibromyalgia patients may be plausible using this technique. Healthy subjects performing the same task had an average differential activation frequency of 0.4 Hz, with a 95% confidence interval between about 0.3 and 0.5 Hz, about 0.2 Hz higher for the 2 lowest load levels and 0.2 Hz lower for the 2 highest ones (Gerdle et al., 2010). This is significantly higher than the frequency of fibromyalgia patients for the two lowest load levels. However, compared to the fibromyalgia patients scoring 0 on VAS, this is, on average, slightly lower for the two highest load levels and the same for the two lowest load levels. Before discussing possible physiological mechanisms behind a load effect, data of more subjects should be collected to investigate whether or not this load effect is physiological of origin. Moreover, to get insight in the causality of the relation between differential activation and pain intensity in the trapezius muscle, it is necessary to investigate if changes in frequency of differential activations of the trapezius muscle correspond to changes in pain intensity in other groups than patients with fibromyalgia. The findings of this study should therefore be investigated by repetitive measures among populations with chronic muscle pain, or during artificially induced pain. With respect to the previously presented models explaining the relation between muscle activity and chronic muscle pain, our findings support the integrated pain adaptation model (Murray and Peck, 2007). This model emphasizes on how the redundancy of skeletal muscles provides different recruitment strategies plausible for avoiding or minimizing pain (Murray and Peck, 2007). This corresponds well with the observed relation between shifts in activity between intra-muscular parts of the trapezius and pain intensity of this study. The observed relation between differential activations and pain intensity may be influenced by other factors. One factor may be systematic differences in maximal strength or muscle activity with pain intensity. Because the validity of maximal strength and muscle activity can be questioned due to factors such as pain intensity, increase in pain with increasing contraction level, anxiety and different aspects of fear and fear behaviour these were not tested in this study. However, because a positive relation between differential activations and pain intensity among fibromyalgia patients was found at very low force levels, potential differences in maximal strength and muscle activity are not likely to have materially influenced the findings of this study. Another potential factor influencing the findings of this study is a relation between subcutaneous layer thickness and pain intensity among the fibromyalgia patients. The thickness of subcutaneous layers can affect the EMG amplitude and intra-muscular distribution and therefore the observed differential activations. However, no significant associations between pain intensity and subcutaneous layer thickness or EMG amplitude were found. It is therefore not likely that subcutaneous layer thickness or EMG amplitude have influenced the findings of this study. A methodological limitation of this study may be that the sequence of the loads was not balanced, but increased from 0 to 4 kg. However, because the frequency of differential activations was not different between the loads among both the fibromyalgia patients with highest and lowest levels of pain, the non-balance of sequence could not have any materially influence on the findings of this study.
5. Conclusions For the first time, significant associations between a neuromuscular control mechanism involving shifts between regions within a
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single muscle (differential activations) and pain intensity among chronic pain patients are observed. The lower frequency and longer duration of differential activations among the fibromyalgia patients with highest pain may be a plausible explanation for the severe pain of the fibromyalgia patients with this recruitment strategy. These findings support initiation of clinical trials for investigating the potential pain reliving effects of modifying differential activations among fibromyalgia patients. Acknowledgements This study was supported by the Swedish Council for Working Life and Social Research (2004-0289 and 2007-0760). We would like to thank Stefan J. Karlsson for initiating and coordinating the study. References Abraham WM. Factors in delayed muscle soreness. Med Sci Sports Exercise 1977;9:11–20. Asmussen E. Observations on experimental muscular soreness. Acta Rheumatol Scand 1956;2:109–16. Banic B, Petersen-Felix S, Andersen OK, Radanov BP, Villiger PM, Arendt-Nielsen L, et al. Evidence for spinal cord hypersensitivity in chronic pain after whiplash injury and in fibromyalgia. Pain 2004;107:7–15. Bengtsson A. The muscle in fibromyalgia. Rheumatology 2002;41:721–4. Chanaud CM, Pratt CA, Loeb GE. Functionally complex muscles of the cat hindlimb. V. The roles of histochemical fiber-type regionalization and mechanical heterogeneity in differential muscle activation. Exp Brain Res 1991;85:300–13. Cobb CR, deVries HA, Urban RT, Luekens CA, Bagg RJ. Electrical-activity in muscle pain. Am J Phys Med Rehab 1975;54:80–7. De Vries HA. Quantitative electromyographic investigation of the spasm theory of muscle pain. Am J Physiol Med 1966;45:119–34. Elvin A, Siosteen AK, Nilsson A, Kosek E. Decreased muscle blood flow in fibromyalgia patients during standardised muscle exercise: a contrast media enhanced colour doppler study. Eur J Pain 2006;10:137–44. Falla D, Farina D, Graven-Nielsen T. Experimental muscle pain results in reorganization of coordination among trapezius muscle subdivisions during repetitive shoulder flexion. Exp Brain Res 2007;178:385–93. Farina D, Merletti R, Enoka RM. The extraction of neural strategies from the surface EMG. J Appl Physiol 2004;96:1486–95. Gerdle B, Grönlund C, Karlsson SJ, Holtermann A, Roeleveld K. Altered neuromuscular control mechanisms of the trapezius muscle in fibromyalgia. BMC Musculoskelet Disord 2010;11:42. Gerdle B, Östlund N, Grönlund C, Roeleveld K, Karlsson JS. Firing rate and conduction velocity of single motor units in the trapezius muscle in fibromyalgia patients and healthy controls. J Electromyogr Kinesiol 2008;18:707–16. Giesecke T, Gracely RH, Grant MAB, Nachemson A, Petzke F, Williams DA, et al. Evidence of augmented central pain processing in idiopathic chronic low back pain. Arthritis Rheum 2004;50:613–23. Gracely RH, Petzke F, Wolf JM, Clauw DJ. Functional magnetic resonance imaging evidence of augmented pain processing in fibromyalgia. Arthritis Rheum 2002;46:1333–43. Graven-Nielsen T, Kendall SA, Henriksson KG, Bengtsson M, Sorensen J, Johnson A, et al. Ketamine reduces muscle pain, temporal summation, and referred pain in fibromyalgia patients. Pain 2000;85:483–91. Grönlund C, Roeleveld K, Holtermann A, Karlsson JS. On-line signal quality estimation of multichannel surface electromyograms. Med Biol Eng Comput 2005;43:357–64. Holtermann A, Mork PJ, Andersen LL, Olsen HB, Søgaard K. The use of EMG biofeedback for learning of selective activation of intra-muscular parts within the serratus anterior muscle A novel approach for rehabilitation of scapular muscle imbalance. J Electromyogr Kinesiol 2010;20:359–65. Holtermann A, Roeleveld K, Mork PJ, Grönlund C, Karlsson JS, Andersen LL, et al. Selective activation of neuromuscular compartments within the human trapezius muscle. J Electromyogr Kinesiol 2009;19:896–902. Hough T. Ergographic studies in muscular soreness. Am J Physiol 1902;7:76–92. Johansson H, Sojka P. Pathophysiological mechanisms involved in genesis and spread of muscular tension in occupational muscle pain and in chronic musculoskeletal pain syndromes: a hypothesis. Med Hypotheses 1991;35:196–203. Lund JP, Donga R, Widmer CG, Stohler CS. The pain-adaptation model: a discussion of the relationship between chronic musculoskeletal pain and motor activity. Can J Physiol Pharmacol 1991;69:683–94. Murray GM, Peck CC. Orofacial pain and jaw muscle activity: a new model. J Orofacial Pain 2007;21:263–78. Sandberg M, Larsson B, Lindberg LG, Gerdle B. Different patterns of blood flow response in the trapezius muscle following needle stimulation (acupuncture) between healthy subjects and patients with fibromyalgia and work-related trapezius myalgia. Eur J Pain 2005;9:497–510.
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Andreas Holtermann received his master degree in Human Movement Science from the Norwegian University of Science and Technology, Norway, in 2002. In 2008, he received the Ph.D. in Health Science from the same University. Now, he is working at the National Research Centre for the Working Environment, Copenhagen, Denmark with main focus on prevention and rehabilitation of musculoskeletal disorders, sickness absence and cardiovascular diseases.
Christer Grönlund received his M.Sc. in engineering physics from the University of Umeå, Sweden in 2002, and the Ph.D. from the University of Umeå, Sweden in 2007. Since then he is working as a researcher at the Department of Biomedical Engineering - R&D at Radiation Sciences, Umeå University Hospital, Umeå. His current research projects include skeletal and cardiovascular ultrasound imaging, multimodal signal processing, and diffuse optical imaging.
Karin Roeleveld was born in The Netherlands in 1969. She received the M.Sc. degree in human movement sciences from the Vrije Universiteit in Amsterdam, The Netherlands, in 1992. Thereafter, she joined the University Hospital in Nijmegen, The Netherlands and received her Ph.D. degree in 1997 on the fundamentals of surface electromyography using multi electrode surface electromyography. Thereafter she spent two years working as a post doc at the Friedrich-Schiller-University Jena, Germany. Since 1998 she is working at the human movement sciences programme, at the Norwegian University of Science and Technology (NTNU). Her research interests are related to the neuromuscular system and signal analysis in surface electromyography and focus on motor control and how this adapts with activity, disease and age.
Björn Gerdle was born in 1953, in Kalmar, Sweden. He is a physician (M.D.) and specialist in rehabilitation medicine since 1991 and in pain alleviation since 1997. The Ph.D. in rehabilitation medicine was earned in 1985 at Umeå University. Since 1992 he is working, as Professor in Rehabilitation Medicine at Linköping University, Sweden and since 1997 also as the Director of the Pain and Rehabilitation Centre, University Hospital, Linköping. He has written approximately 145 papers in peer-reviewed international journals mainly within the fields of muscle fatigue, electromyography, clinical pain and rehabilitation. The specific research fields are now: Muscle pain (work-related muscle pain, whiplash associated disorders and fibromyalgia). Muscle histochemistry and morphology in patients with chronic pain. Muscle tension/pain and surface electromyography (EMG). The effects of multimodal rehabilitation programmes.
Contents lists available at ScienceDirect
Journal of Electromyography and Kinesiology journal homepage: www.elsevier.com/locate/jelekin
The relation between neuromuscular control and pain intensity in fibromyalgia Andreas Holtermann a,⇑, Christer Grönlund b, Karin Roeleveld c, Björn Gerdle d,e a
National Research Centre for the Working Environment, Lersø Parkallé 105, DK-2100 Copenhagen, Denmark Biomedical Engineering and Informatics, Radiation Sciences, Umeå University, SE-901 85 Umeå, Sweden c Department of Human Movement Science, Dragvoll, Norwegian University of Science and Technology, N-7491 Trondheim, Norway d Rehabilitation Medicine, Department of Clinical and Experimental Medicine, Linköping University, SE-581 85 Linköping, Sweden e Pain and Rehabilitation Centre, University Hospital, SE-581 85 Linköping, Sweden b
a r t i c l e
i n f o
Article history: Received 30 August 2010 Received in revised form 14 January 2011 Accepted 14 January 2011
Keywords: Neuromuscular activation Musculoskeletal disorder Muscle pain Fibromyalgia Differential activations
a b s t r a c t Fibromyalgia patients are shown to have a different neuromuscular control (differential activation) than healthy persons. Before clinical trials can be initiated, the relation between differential activations and pain intensity among fibromyalgia patients needs to be investigated. Twenty-seven fibromyalgia patients performed 3 min bilateral shoulder elevations with different loads (0–4 kg) with a high-density surface electromyographical (EMG) grid placed on the upper trapezius. Differential activation was quantified by the power spectral median frequency of the difference in EMG amplitude between the cranial and caudal parts of the upper trapezius. The average duration of the differential activation was described by the inverse of the median frequency of the differential activations. The relation between frequency and duration of differential activations as an average of the 4 loads and pain intensity the same day prior to the experiment was explored by Pearson’s correlation coefficients. A strong negative relation between frequency of differential activations and pain intensity (R = 0.67, p < 0.001) and a strong positive association between duration of differential activations and pain intensity (R = 0.66, p < 0.001) were found. The significant association between frequency and duration of differential activations and pain intensity among the fibromyalgia patients indicates a relation between this neuromuscular control pattern and pain intensity. This finding support initiation of clinical trials for investigating effects on pain intensity of modifying differential activations among fibromyalgia patients. Ó 2011 Elsevier Ltd. All rights reserved.
1. Introduction The association between neuromuscular control and chronic muscle pain has been a topic of clinical interest for decades (Hough, 1902). Early observations of enhanced muscle activity and tender muscles at clinical examination in persons with pain (Abraham, 1977; Asmussen, 1956; Cobb et al., 1975; De Vries, 1966) supported the viscous circle model (Travell et al., 1942). This model proposes that a painful condition causes reflexive mediated muscle hyperactivity (spasm) which further enhances pain and dysfunction (Johansson and Sojka, 1991). However, acute muscle pain has predominantly been observed to inhibit rather than increase muscle activity (Falla et al., 2007; Farina et al., 2004; Lund et al., 1991; Svensson et al., 1998). Therefore, the pain adaptation model (Lund et al., 1991) has received increasingly attention. This model states that a painful condition reduces muscle activity when active as agonist and increases activity when active as antagonist which would limit movement and protect against further injury (Lund et al., 1991). ⇑ Corresponding author. Tel.: +45 39165352. E-mail address: [email protected] (A. Holtermann). 1050-6411/$ - see front matter Ó 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.jelekin.2011.01.004
However, neither of the models are unequivocally supported by the literature, and the changes in muscle activity is considered to be more complicated than stated in the pain adaptation model (Murray and Peck, 2007). Therefore, the integrated pain adaptation model has been proposed (Murray and Peck, 2007). The model emphasizes how the redundancy of skeletal muscles provides many motor unit subpopulations available for performing a task, making different recruitment strategies plausible for avoiding or minimizing pain. An example of such a recruitment strategy is reciprocal reversals of activity between regions within a single muscle, defined as differential activation (Chanaud et al., 1991). Accordingly, we recently reported a lowered frequency of differential activations (shifts in activity between the caudal and cranial parts) of the upper trapezius in fibromyalgia patients compared with healthy controls (Gerdle et al., 2010). The lower frequency (measured as a lowered median frequency domain) of differential activations in fibromyalgia patients may cause overexertion and fatigue of the muscle region, and therefore be a plausible explanation for the maintenance of the peripheral nociception and the central alterations (i.e., central hyperexcitability and altered descending inhibition) resulting in severe pain of the fibromyalgia patients (Gerdle et al., 2010).
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This observation of a different neuromuscular control between fibromyalgia patients and healthy persons may provide the basis for treatment strategies for fibromyalgia. However, before clinical trials for investigating effects on pain intensity from modulating differential activations among fibromyalgia patients should be initiated, it is a need to know if and how the frequency of differential activation is related to the pain intensity of the fibromyalgia patients. Moreover, although the relation between neuromuscular control and pain intensity has been debated for decades (Hough, 1902; Lund et al., 1991; Travell et al., 1942), documentation of a relation between neuromuscular control and pain intensity is lacking. Therefore, the aim of this study was to investigate the relation between frequency of differential activations and pain intensity among fibromyalgia patients. 2. Materials and methods 2.1. Subjects Female patients with fibromyalgia (N = 29; age: 37 ± 5 years, weight: 69.3 ± 9.5 kg, height: 166 ± 5 cm) were recruited from the Pain and Rehabilitation Centre, University Hospital, Linköping, Sweden. It should be noted that not all of these patients were able to perform all tasks (see Section 3, drop-out and activity levels at the different loads). The patients were offered participation in the study after examination of medical records, positive response to information letter, and a phone conversation with a physician. The patients were clinically diagnosed according to the ACR criteria of 1990 for the classification of fibromyalgia (FM) (Wolfe et al., 1990). The mean duration of FM was 6.6 ± 3.2 years (minimum 2 years. Descriptive data of the fibromyalgia patients (i.e., age, anthropometric data, pain intensity recent week (minimum, average and maximum intensity), and data from ultrasound recording) have been presented previously (Gerdle et al., 2008). All subjects gave written informed consent to participate. The study conformed to the Declaration of Helsinki and the study protocol was approved by the local ethics committee at Linköping University. 2.2. Experimental setup First, a high-density surface electromyographic (EMG) electrode-grid (modified ActiveOne, BioSemi, Amsterdam, Netherlands) consisting of 13 by 10 active electrodes (0.5 cm interelectrode distance), covering 6 4.5 cm of the skin surface was placed on the skin above the right trapezius muscle in the middle of the line between the processus spinosus of the seventh cervical vertebra and the lateral edge of acromion. The base of the electrode-grid device is concave and semiflexible and thereby fitted well with the convex recordings area of the upper trapezius muscle. In this way, the recorded signals of all subjects were not affected by muscle–tendon transitions and similarly affected by the motor end plate region. To generate a stable pressure between electrodes and the skin, the electrode grid was held in place by two elastic straps around the shoulder and torso of the subject. The surface EMG signals were recorded from all electrodes (monopolar) with a common reference on the processus spinosus of the seventh cervical vertebra at 2048 Hz. Then, the subjects performed symmetrical bilateral shoulder elevations with different loads. The loads were applied through the attachment of different weights on a harness. The harness consisted of 2 belts hanging on both shoulders on the level of the acromion to allow attachment of the weights. One additional belt was placed around the torso in order to fixate the other two belts. After attaching the harness and weights, the subjects were asked to lift the weights such that the shoulders were in a horizontal plane,
and to hold this position for 3 min. Weights of 0, 1, 2, and 4 kg were applied successively. The subjects were given 1-min rest between each contraction. The choice of absolute weights and not relative weights in relation to maximum performance was based on the difficulties for obtaining valid maximum voluntary contractions (MVC) in FM patients due to pain and/or psychological aspects such as fear-avoidance or kinesiophobia. 2.3. Ultrasound recordings Ultrasound measurements were taken of the thickness (mm) of the trapezius muscle and the subcutaneous soft tissue (skin and fat tissue taken together) 2 cm lateral of the midpoint between the seventh process of the cervical spine and the lateral part of the acromion process using an Acuson 128XP/10 (Siemens). 2.4. Pain intensity recordings The participants reported the pain intensity prior to the experiment (the same day) on a 100 mm visual analogue scale (VAS). As previously presented, the pain intensity prior to the experiment was highly correlated with the average pain intensity the last week (Gerdle et al., 2008). 2.5. Surface EMG analysis – quantification of differential activation The differential activation analysis was previously described (Gerdle et al., 2010). The essence of the analysis was to examine the temporal changes of the difference in myoelectric activity between two regions within a muscle. While the EMG signals were recorded using a 2-D high-density EMG grid, a large part of the processing (most of step III below) was undertaken in order to reduce the data to signals originating from the caudal and cranial regions of the trapezius muscle. Multiple channels covering a large area were recorded to get a better estimate of the activation of the two muscle parts (Staudenmann et al., 2005). In short, the procedure involved; (I) Pre-processing: Prior to analysis, poor quality signals were omitted (Grönlund et al., 2005). The remaining signals were high-pass filtered at 10 Hz, and bipolar spatial filtering in the fiber direction (medial–lateral) was carried out. (II) Muscle activity: The muscle activity level of the EMG signals was described using the root-mean-square (RMS), calculated in 0.5 s non-overlapping time-windows. In order to compare the activity between regions within the muscle, the muscle activity signals were de-trended and normalized to their corresponding maximum RMS values (maximum over the whole 3 min contraction). (III) Muscle activity in the cranial – caudal direction: Muscle activity in the cranial – caudal direction (perpendicular to fibre orientation) was calculated by averaging the muscle activity recorded by electrodes of the grid along the fibre orientation (medial–lateral), providing 10 activity signals in the cranial – caudal direction. (IV) Activity difference: The difference in the normalized muscle activity between the cranial (average of the three most superior electrode positions) and the caudal (average of the three most inferior electrode positions) regions of the upper trapezius was calculated. (V) Median frequency and average duration of the differential activations: Differential activation was quantified using the power spectral median frequency (MDF) of the whole activity difference signal. The inverse of the median frequency of the differential activations was calculated to quantify the average duration of the differential activations.
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2.6. Statistics All statistical analyses were performed using MATLAB (The Mathworks, Nattick, USA; version 2007b). For variables and indices mean value with one standard deviation (±1 SD) are generally reported. The relation between frequency of differential activation and pain intensity was investigated with Pearson’s correlation coefficients. For investigating differences in median frequency of differential activation at the different loads, a 1-way ANOVA was performed among the fibromyalgia patients with lowest (n 6 13) and highest (n 6 12) pain intensity, respectively. A probability of 60.05 (two-tailed) was used as criteria for significance in all tests. 3. Results 3.1. Pain intensity and anthropometric data These data of the fibromyalgia patients are previously reported (Gerdle et al., 2010, 2008). The pain intensity prior to the experiment was 35 ± 21 mm according to a 100 mm VAS scale. The average thickness of the trapezius muscle was 11.7 ± 2.4 mm over the examination area of the trapezius. The thickness of the superjacent tissues (skin and subcutaneous tissue) was 6.6 ± 1.6 mm over the examination area. 3.2. Drop-outs and activity levels at the different load levels These data of the fibromyalgia patients are previously reported (Gerdle et al., 2010, 2008). Among the fibromyalgia patients (N = 29), 2 (6.9%), 2 (6.9%), 4 (13.8%), and 8 (27.6%) patients were not able to perform the tasks during 3 min with the 4 different external loads, respectively, and were therefore excluded in the subsequent analyses for these load levels. The activity levels of the fibromyalgia patients at the 4 different load levels (0, 1, 2 and 4 kg) were 0.54 ± 0.24, 0.57 ± 0.32, 0.68 ± 0.33 and 0.82 ± 0.41 mV. 3.3. Frequency and duration of differential activations versus pain intensity Fig. 1 illustrates typical examples of a normalized muscle activity from the high-density EMG recording from a fibromyalgia patient with low pain intensity (A) and a fibromyalgia patient with high pain intensity (B) performing a 1 kg weight of isometric shoulder elevation. The lower frequency (MDF) of differential activation of the fibromyalgia patient with low pain intensity (Fig. 1A
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and C) compared with the fibromyalgia patient with high pain intensity (Fig. 1B and D) is clearly demonstrated. The association between frequency of differential activations between the caudal and cranial regions of the trapezius muscle and pain intensity of the fibromyalgia patients at the four load levels are presented in Fig. 2. Significant negative associations between frequency of differential activations and pain intensity were found for 3 (i.e., 0, 2 and 4 kg) of the 4 loads (p < 0.05). Moreover, the frequency of differential activations as a mean of all loads and pain intensity among the fibromyalgia patients was highly significant (R = 0.67, p < 0.001) (Fig. 3). Accordingly, significant positive associations between duration of differential activations and pain intensity were found for 3 (i.e., 0, 2 and 4 kg) of the 4 loads (p < 0.05). The duration of differential activations as a mean of all loads and pain intensity among the fibromyalgia patients was highly significant (R = 0.66, p < 0.001) (Fig. 3). Table 1 illustrates the median frequency of differential activation in the fibromyalgia patients with lowest (n 6 13) and highest (n 6 12) pain intensity at the different loads. No significant differences in median frequency of differential activation at the different loads were observed among those with lowest (p = 0.66) and highest (p = 0.74) pain intensity. 4. Discussion The main finding of this study was the observed significant association between frequency and duration of differential activations and pain intensity among fibromyalgia patients indicating a close relation between this neuromuscular activation pattern and pain intensity. The observed association between frequency and duration of differential activations and pain intensity among fibromyalgia patients extends upon the previous observations that fibromyalgia patients have a lower frequency and longer duration of differential activation compared with healthy controls (Gerdle et al., 2010). The observation that a low frequency and long duration of differential activation not only differs between healthy controls and fibromyalgia patients, but that there exists a relation between frequency and duration of differential activations and pain intensity among the fibromyalgia patients supports the clinical significance of these electromyographic findings. The findings of this study can be caused by 2 mechanisms. First, a low frequency and long duration of differential activation of activity within the upper trapezius may be an underlying neuromuscular control mechanism associated with increased risk for acute and chronic musculoskeletal symptoms. This would further
Fig. 1. Examples of activity difference in normalized activity between caudal and cranial regions for a subject with low and high pain (A and B, respectively). C and D present the corresponding power spectral density estimates (psd) of the signals in A and B, respectively. The values of the estimated median frequencies (MDF) of the difference in activity between the caudal and cranial regions are also given in C and D (dotted vertical lines). Its inverse was used to calculate the corresponding duration. For illustrational purpose, only one minute of the total three minutes is shown in A and B.
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Fig. 2. Median frequency (MDF) of the difference in activity between the caudal and cranial regions of the trapezius muscle as function of pain intensity (VAS) at the different load levels.
Fig. 3. Median frequency (MDF) (A) and duration (B) of the difference in activity between the caudal and cranial regions of the trapezius muscle as function of pain intensity (VAS) after averaging over load levels.
Table 1 Median frequency of differential activation in fibromyalgia patients with lowest (n 6 13) and highest (n 6 12) pain intensity; mean values ±1 standard deviation (SD) and minimum and maximum values. At the bottom row, results of the 1-way ANOVA statistical comparisons (p-values) of median frequency of differential activations between the load levels for the subjects with lowest and highest pain intensity are presented. Variable and load
Frequency (Hz) 0 kg 1 kg 2 kg 4 kg p-Value
Lowest pain
Highest pain
Mean ± SD
Min–Max
Mean ± SD
Min–Max
0.39 0.35 0.36 0.39 0.66
0.28–0.53 0.12–0.49 0.17–0.48 0.23–0.56
0.32 0.32 0.28 0.34 0.74
0.14–0.53 0.14–0.60 0.15–0.42 0.16–0.60
(0.08) (0.11) (0.11) (0.09)
(0.12) (0.14) (0.09) (0.14)
support that the ability to shift activity between regions within the upper trapezius may be a preventive mechanism for avoiding
reflexive mediated muscle hyperactivity from acute painful condition further enhancing pain and a chronic condition (Johansson and Sojka, 1991). An alternative mechanism is that the observed relation between differential activations and pain intensity among fibromyalgia patients may be a result of intensity-related effects of the chronic painful condition on the central nervous system (central sensitizing processes, alterations in function of neuromatrix of pain in the brain or in descending inhibition) (Banic et al., 2004; Giesecke et al., 2004; Gracely et al., 2002; Graven-Nielsen et al., 2000) and/or in the muscle (Bengtsson, 2002; Elvin et al., 2006; Sandberg et al., 2005; Staud et al., 2009). To get more insight in to the mechanism behind the relation between neuromuscular control strategies and chronic pain, prospective investigations are necessary. However, very few exist (Veiersted et al., 1993). Moreover, clinical trials can investigate the potential pain relieving effects of modifying differential activations among fibromyalgia patients. Differential activation of different parts of the trapezius
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muscle can be learned by electromyographic biofeedback among healthy persons (Holtermann et al., 2010, 2009). Therefore, modifications of differential activations among fibromyalgia patients may be plausible using this technique. Healthy subjects performing the same task had an average differential activation frequency of 0.4 Hz, with a 95% confidence interval between about 0.3 and 0.5 Hz, about 0.2 Hz higher for the 2 lowest load levels and 0.2 Hz lower for the 2 highest ones (Gerdle et al., 2010). This is significantly higher than the frequency of fibromyalgia patients for the two lowest load levels. However, compared to the fibromyalgia patients scoring 0 on VAS, this is, on average, slightly lower for the two highest load levels and the same for the two lowest load levels. Before discussing possible physiological mechanisms behind a load effect, data of more subjects should be collected to investigate whether or not this load effect is physiological of origin. Moreover, to get insight in the causality of the relation between differential activation and pain intensity in the trapezius muscle, it is necessary to investigate if changes in frequency of differential activations of the trapezius muscle correspond to changes in pain intensity in other groups than patients with fibromyalgia. The findings of this study should therefore be investigated by repetitive measures among populations with chronic muscle pain, or during artificially induced pain. With respect to the previously presented models explaining the relation between muscle activity and chronic muscle pain, our findings support the integrated pain adaptation model (Murray and Peck, 2007). This model emphasizes on how the redundancy of skeletal muscles provides different recruitment strategies plausible for avoiding or minimizing pain (Murray and Peck, 2007). This corresponds well with the observed relation between shifts in activity between intra-muscular parts of the trapezius and pain intensity of this study. The observed relation between differential activations and pain intensity may be influenced by other factors. One factor may be systematic differences in maximal strength or muscle activity with pain intensity. Because the validity of maximal strength and muscle activity can be questioned due to factors such as pain intensity, increase in pain with increasing contraction level, anxiety and different aspects of fear and fear behaviour these were not tested in this study. However, because a positive relation between differential activations and pain intensity among fibromyalgia patients was found at very low force levels, potential differences in maximal strength and muscle activity are not likely to have materially influenced the findings of this study. Another potential factor influencing the findings of this study is a relation between subcutaneous layer thickness and pain intensity among the fibromyalgia patients. The thickness of subcutaneous layers can affect the EMG amplitude and intra-muscular distribution and therefore the observed differential activations. However, no significant associations between pain intensity and subcutaneous layer thickness or EMG amplitude were found. It is therefore not likely that subcutaneous layer thickness or EMG amplitude have influenced the findings of this study. A methodological limitation of this study may be that the sequence of the loads was not balanced, but increased from 0 to 4 kg. However, because the frequency of differential activations was not different between the loads among both the fibromyalgia patients with highest and lowest levels of pain, the non-balance of sequence could not have any materially influence on the findings of this study.
5. Conclusions For the first time, significant associations between a neuromuscular control mechanism involving shifts between regions within a
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single muscle (differential activations) and pain intensity among chronic pain patients are observed. The lower frequency and longer duration of differential activations among the fibromyalgia patients with highest pain may be a plausible explanation for the severe pain of the fibromyalgia patients with this recruitment strategy. These findings support initiation of clinical trials for investigating the potential pain reliving effects of modifying differential activations among fibromyalgia patients. Acknowledgements This study was supported by the Swedish Council for Working Life and Social Research (2004-0289 and 2007-0760). We would like to thank Stefan J. Karlsson for initiating and coordinating the study. References Abraham WM. Factors in delayed muscle soreness. Med Sci Sports Exercise 1977;9:11–20. Asmussen E. Observations on experimental muscular soreness. Acta Rheumatol Scand 1956;2:109–16. Banic B, Petersen-Felix S, Andersen OK, Radanov BP, Villiger PM, Arendt-Nielsen L, et al. Evidence for spinal cord hypersensitivity in chronic pain after whiplash injury and in fibromyalgia. Pain 2004;107:7–15. Bengtsson A. The muscle in fibromyalgia. Rheumatology 2002;41:721–4. Chanaud CM, Pratt CA, Loeb GE. Functionally complex muscles of the cat hindlimb. V. The roles of histochemical fiber-type regionalization and mechanical heterogeneity in differential muscle activation. Exp Brain Res 1991;85:300–13. Cobb CR, deVries HA, Urban RT, Luekens CA, Bagg RJ. Electrical-activity in muscle pain. Am J Phys Med Rehab 1975;54:80–7. De Vries HA. Quantitative electromyographic investigation of the spasm theory of muscle pain. Am J Physiol Med 1966;45:119–34. Elvin A, Siosteen AK, Nilsson A, Kosek E. Decreased muscle blood flow in fibromyalgia patients during standardised muscle exercise: a contrast media enhanced colour doppler study. Eur J Pain 2006;10:137–44. Falla D, Farina D, Graven-Nielsen T. Experimental muscle pain results in reorganization of coordination among trapezius muscle subdivisions during repetitive shoulder flexion. Exp Brain Res 2007;178:385–93. Farina D, Merletti R, Enoka RM. The extraction of neural strategies from the surface EMG. J Appl Physiol 2004;96:1486–95. Gerdle B, Grönlund C, Karlsson SJ, Holtermann A, Roeleveld K. Altered neuromuscular control mechanisms of the trapezius muscle in fibromyalgia. BMC Musculoskelet Disord 2010;11:42. Gerdle B, Östlund N, Grönlund C, Roeleveld K, Karlsson JS. Firing rate and conduction velocity of single motor units in the trapezius muscle in fibromyalgia patients and healthy controls. J Electromyogr Kinesiol 2008;18:707–16. Giesecke T, Gracely RH, Grant MAB, Nachemson A, Petzke F, Williams DA, et al. Evidence of augmented central pain processing in idiopathic chronic low back pain. Arthritis Rheum 2004;50:613–23. Gracely RH, Petzke F, Wolf JM, Clauw DJ. Functional magnetic resonance imaging evidence of augmented pain processing in fibromyalgia. Arthritis Rheum 2002;46:1333–43. Graven-Nielsen T, Kendall SA, Henriksson KG, Bengtsson M, Sorensen J, Johnson A, et al. Ketamine reduces muscle pain, temporal summation, and referred pain in fibromyalgia patients. Pain 2000;85:483–91. Grönlund C, Roeleveld K, Holtermann A, Karlsson JS. On-line signal quality estimation of multichannel surface electromyograms. Med Biol Eng Comput 2005;43:357–64. Holtermann A, Mork PJ, Andersen LL, Olsen HB, Søgaard K. The use of EMG biofeedback for learning of selective activation of intra-muscular parts within the serratus anterior muscle A novel approach for rehabilitation of scapular muscle imbalance. J Electromyogr Kinesiol 2010;20:359–65. Holtermann A, Roeleveld K, Mork PJ, Grönlund C, Karlsson JS, Andersen LL, et al. Selective activation of neuromuscular compartments within the human trapezius muscle. J Electromyogr Kinesiol 2009;19:896–902. Hough T. Ergographic studies in muscular soreness. Am J Physiol 1902;7:76–92. Johansson H, Sojka P. Pathophysiological mechanisms involved in genesis and spread of muscular tension in occupational muscle pain and in chronic musculoskeletal pain syndromes: a hypothesis. Med Hypotheses 1991;35:196–203. Lund JP, Donga R, Widmer CG, Stohler CS. The pain-adaptation model: a discussion of the relationship between chronic musculoskeletal pain and motor activity. Can J Physiol Pharmacol 1991;69:683–94. Murray GM, Peck CC. Orofacial pain and jaw muscle activity: a new model. J Orofacial Pain 2007;21:263–78. Sandberg M, Larsson B, Lindberg LG, Gerdle B. Different patterns of blood flow response in the trapezius muscle following needle stimulation (acupuncture) between healthy subjects and patients with fibromyalgia and work-related trapezius myalgia. Eur J Pain 2005;9:497–510.
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Andreas Holtermann received his master degree in Human Movement Science from the Norwegian University of Science and Technology, Norway, in 2002. In 2008, he received the Ph.D. in Health Science from the same University. Now, he is working at the National Research Centre for the Working Environment, Copenhagen, Denmark with main focus on prevention and rehabilitation of musculoskeletal disorders, sickness absence and cardiovascular diseases.
Christer Grönlund received his M.Sc. in engineering physics from the University of Umeå, Sweden in 2002, and the Ph.D. from the University of Umeå, Sweden in 2007. Since then he is working as a researcher at the Department of Biomedical Engineering - R&D at Radiation Sciences, Umeå University Hospital, Umeå. His current research projects include skeletal and cardiovascular ultrasound imaging, multimodal signal processing, and diffuse optical imaging.
Karin Roeleveld was born in The Netherlands in 1969. She received the M.Sc. degree in human movement sciences from the Vrije Universiteit in Amsterdam, The Netherlands, in 1992. Thereafter, she joined the University Hospital in Nijmegen, The Netherlands and received her Ph.D. degree in 1997 on the fundamentals of surface electromyography using multi electrode surface electromyography. Thereafter she spent two years working as a post doc at the Friedrich-Schiller-University Jena, Germany. Since 1998 she is working at the human movement sciences programme, at the Norwegian University of Science and Technology (NTNU). Her research interests are related to the neuromuscular system and signal analysis in surface electromyography and focus on motor control and how this adapts with activity, disease and age.
Björn Gerdle was born in 1953, in Kalmar, Sweden. He is a physician (M.D.) and specialist in rehabilitation medicine since 1991 and in pain alleviation since 1997. The Ph.D. in rehabilitation medicine was earned in 1985 at Umeå University. Since 1992 he is working, as Professor in Rehabilitation Medicine at Linköping University, Sweden and since 1997 also as the Director of the Pain and Rehabilitation Centre, University Hospital, Linköping. He has written approximately 145 papers in peer-reviewed international journals mainly within the fields of muscle fatigue, electromyography, clinical pain and rehabilitation. The specific research fields are now: Muscle pain (work-related muscle pain, whiplash associated disorders and fibromyalgia). Muscle histochemistry and morphology in patients with chronic pain. Muscle tension/pain and surface electromyography (EMG). The effects of multimodal rehabilitation programmes.