Erector spinae SEMG activity during forward flexion and re-extension in ankylosing spondylitis patients

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1 Pathophysiology 12 (2005) Erector spinae SEMG activity during forward flexion and re-extension in ankylosing spondylitis patients Pirkko Heinonen, Hannu Kautiainen, Marja Mikkelsson Rheumatism Foundation Hospital, Rehabilitation Center, Pikijärventie 1, Heinola, Finland Received 30 December 2004; received in revised form 13 September 2005; accepted 16 September 2005 Abstract Objective: To compare erector spinae muscle (ESM) activity as measured by surface electromyography (SEMG) in lumbar flexion from the upright position in men with ankylosing spondylitis (AS) and healthy males, and to study associations between pain, lumbar mobility and ESM activity. Methods: Surface EMG was undertaken at the L1-2 and L4-5 levels in 11 men with AS taking part in a rehabilitation course at the Rheumatism Foundation Hospital, and in 10 pain-free male controls, while the subjects were bending forward. Results: During full flexion ESM SEMG activity was significantly greater in patients with AS than in the controls. Relaxation was evident during flexion in all of the controls but in only some patients with AS. Lumbar mobility correlated negatively with ESM activities. No relationship between pain and ESM activity was evident. Some AS patients reported pain while ESM activity was being measured. Conclusion: Decreased lumbar mobility rather than pain explains ESM activity during full flexion in patients with AS Elsevier Ireland Ltd. All rights reserved. Keywords: Ankylosing spondylitis; EMG; Erector spinae; Lumbopelvic rhythm 1. Introduction Ankylosing spondylitis (AS) is a chronic inflammatory disease predominantly affecting the axial skeleton and sacroiliac joints. It is also associated with peripheral joint inflammation and extra-articular-system symptoms. In AS, in addition to progressive decreases in ranges of motion, changes in body posture, stiffness, pain and fatigue patients experience difficulties with activities of daily life [1]. Diagnosis of AS is based on assessment of symptoms, evidence of decreased mobility and radiological changes in the sacro-iliac joints [2,3]. Despite stiffening, spinal mobility should be maintained in AS [4]. AS patients benefit from rehabilitation [5] and physiotherapy is regarded as an important element in treatment [6]. Several tests of mobility (determination of finger-to-floor distance, and of capacities for chest expansion, thoracolumbar rotation and lateral rotation) have shown to be sensitive Corresponding author. Fax: address: pirkko.heinonen@reuma.fi (P. Heinonen). in relation to detection of improvements during short-term clinical trials. Other tests (Schober, and determination of thoracolumbar flexion and occiput-wall distance) were not sufficiently sensitive [7]. Results of the Schobers test and of measurement of thoracolumbar flexion correlated significantly with specific radiologically demonstrable spinal changes, and reproducibilities of results between and within testers were also good (ICC range from 0.84 to 0.98) [8]. Although changes in results of mobility tests provide useful short- and long-term follow-up information, they do not indicate how the back muscles are functioning. Back-muscle function can be evaluated by means of needle or surface electromyography (SEMG). Surface EMG has been used in numerous studies of low back pain (LBP) [9 15]. No information on changes in the lumbopelvic rhythms of AS patients as determined by SEMG has been published. Spinal pain and stiffening in AS patients can alter lumbopelvic rhythm, can lead to absence of the flexion relaxation phenomenon and can result in differences in activation patterns of erector spinae muscles (ESM). The aim of rehabilitation is to ease the spinal pain and restore spinal mobility. Traditionally, progression of AS is followed /$ see front matter 2005 Elsevier Ireland Ltd. All rights reserved. doi: /j.pathophys

2 290 P. Heinonen et al. / Pathophysiology 12 (2005) by means of measurement of flexion mobility. If the aims of rehabilitation are achieved, changes in the activation of paraspinal muscles could be evident. Reproducible methods of evaluation of function and of changes in activation of paraspinal muscles are needed. Normally, in the upright position, ESM activity is scarcely noticeable. However, it increases markedly during flexion. During full flexion no activity is evident but during reextension, activity increases significantly. Patients with nonspecific low back pain exhibit ESM activity when standing at rest [9]. Normally, there are no significant differences between lumbar segments in relation to symmetrical flexion extension movement [16,17]. EMG activities in individuals with low back pain is lower than those activities of healthy individuals doing similar work [10,11]. This study was part of a project aimed to clarify the possibilities of using surface EMG to follow up the effects of rehabilitation of AS patients. The purpose of this study was to compare the effects of mobility of the spine and pain on ESM activity as measured by EMG in patients with AS and controls during forward flexion. 2. Subjects and methods The study involved 11 male patients having AS diagnosis and who attended a rehabilitation course at the Rheumatism Foundation Hospital in Heinola, and 10 male controls free from pain. The mean age of the patients was 36.5 years (S.D years), that of controls 38.3 years (S.D years). The mean duration of AS in the patients was 8.4 years (range 1 30 years). The mean weight of the patients was 78.4 kg (S.D kg), of the controls 79.4 kg (S.D. 8.4 kg). The mean height of the patients was cm (S.D. 6.8 cm), of the controls (S.D. 6.5 cm). All of the patients met the modified New York criteria for AS [18]. Among the exclusion criteria for the controls were back pain or any diagnosed back disease. Seven of the patients were taking sulphasalazine medication (Salazopyrin). One was taking a corticosteroid orally. All of the patients were taking non-steroidal anti-inflammatory drugs as necessary. This study was approved by the ethical committee of Rheumatism Foundation Hospital. Lumbar mobility was measured in the sagittal plane by means of the Schober test [14], and by measurement of finger to floor distance [14], of thoracolumbar flexion [5] (in cm), and of lumbar flexion, using an inclinometer [19]. The patients were asked to indicate their present back pain on a drawing and a visual analogue scale (VAS) before and after the experiment Measurement of performance Each subject was asked to perform the experimental task three times while standing with his feet 15 cm apart. Each task was divided into three phases. In phase 1 each subject had to flex his trunk forward from the erect position as far as possible. In phase 2, each subject had to maintain full flexion. In phase 3 each subject had to revert to the initial upright position. Ten seconds were allowed for performance of each task (3 s for phase 1, 4 s for phase 2, 3 s for phase 3). Timing was controlled by means of a metronome (9). Before measurement each subject could practice forward flexion and re-extension once Electromyographic recordings During tasks, ESM activity was monitored by means of SEMG, and the picture was synchronized with the EMG curve, using ME3000p equipment (Mega Electronics Ltd., Kuopio, Finland). Skin-surface electrodes were placed over the ESM, at the level of the spinous process, at L1-2 and L4-5, 2 cm bilaterally from the midline. While the electrodes were being positioned, each subject stood slightly flexed forward, to prevent the electrodes becoming detached once full flexion had been achieved. Recording of raw EMG signals took place at a frequency of 1000 Hz, via four channels, with EMG data were normalized by determining the signal amplitude percentage of reference voluntary contraction (RVC). Each subject flexed forward then stood upright again three times. Each phase of the second task performance was analyzed. EMG activity at levels L1-2 and L4-5 was determined in the upright position. EMG activity during the excentric work (phase 1) was also determined at both levels. The beginning of the excentric work phase was defined from the EMG curve. The first 0.1 s was ignored and the next 0.5 s was analyzed. EMG activity during relaxation (phase 2) was determined back from the beginning of the concentric phase. Again, the first 0.1 s was ignored. One second of the relaxation phase was analyzed. Because it was difficult to define the beginning of the concentric phase (phase 3) the first 0.5 s of it was ignored. A one-second period was then analyzed. In all phases, the maximum activity level (90%) was analyzed. Reproducibility of measurement of surface EMG between testers was determined. Two physiotherapists (PT) blind to each others findings, measured surface EMG activity of the back muscles in six male patients with AS and five healthy male controls. During measurement, the subjects bent forward from a standing position. Each PT placed the electrodes independently. The sites for the electrodes had not been marked. The reproducibility of measurements in the standing position at rest was good (Lin s concordance coefficients [20] (CCC) 0.91 and 0.71) at both L4-5 and L1-2 levels. Reproducibility in relation to movement was better at the L4-5 level. Reproducibility in relation to subjects completely bent forward was poor unless flexion relaxation had occurred [21] Statistical analyses Student s t-test was used to determine significances of differences between results relating to normally distributed paired samples. For asymmetrically distributed or categorial variables, the non-parametric Mann Whitney test was used.

3 P. Heinonen et al. / Pathophysiology 12 (2005) The Pearson correlation coefficient was used to assess significances of correlations between lumbar mobility and ESM activity as measured by means of EMG, and between pain and ESM activity as measured by EMG during full flexion. The significance level was taken to be P lower than Results Table 1 shows results relating to spinal mobility. Spinal mobility was less in the AS patients than in the controls. Statistically significant differences were found between the groups in relation to finger-floor distance, Schober test results and thoracolumbar flexion. Table 2 shows EMG-signal levels (in V) during the different phases of measurement in AS patients and controls. Flexion relaxation occurred in five AS patients (45%) at a mean of 66 of forward flexion (range ). Flexion relaxation occurred in all of the controls at a mean of 72 of forward flexion (range ). During full flexion ESM activity at both L1-2 and L4-5-levels was significantly greater in the AS patients than in the controls. Patients with AS performed less concentric work at the L4-5-level than controls but the difference is not statistically significant. During the other phases no differences were found between the AS patients and controls. The mean pain measured using a VAS in the AS patients before experiment was 19 mm (range 0 61 mm). Three of the 11 AS patients were totally pain-free. There was no correlation between pain and ESM activity during flexion (r = 0.01 at the L1-2 level, r = 0.16 at the L4-5 level). Three of the five AS patients who exhibited flexion relaxation reported pain. Table 1 Spinal mobility (cm) in ankylosing spondylitis (AS) patients and controls AS patients, mean (S.D.) Controls, mean (S.D.) P-value FFD (16.50) 0.70 (2.21) Schober 3.50 (1.81) 5.55 (0.58) TLF 7.46 (3.59) (1.42) Lumbar flexion ( ) (19.65) (8.47) Table 2 Levels of surface EMG signals ( V) during different phases of forward flexion and re-extension Ankylosing spondylitis patients, N = 11, mean (S.D.) Control, N =10 P-value Standing L (20.6) (10.30) Standing L (26.6) (9.41) Excentric L (34.54) (37.01) Excentric L (33.71) (43.76) Relaxation L (61.82) (14.36) Relaxation L (45.61) (20.15) Concentric L (71.72) (61.29) Concentric L (47.73) (63.94) Lumbar mobility (Schober test) correlated negatively with ESM activity (r = 0.41at the L1-2 level, r = 0.40 at the L4-5 level) in AS patients. Decreased lumbar mobility correlated moderately with increased ESM activity during full flexion. In healthy controls no correlation between lumbar mobility and ESM activity was seen (r = 0.16 at the L1-2 level, r = 0.01 at the L4-5-level). 4. Discussion In this study ESM activities measured by SEMG during forward bending and re-extension were compared in male patients with AS and healthy pain-free male controls. Flexion relaxation was observed in 45% of the patients with AS but in all of the controls. Lumbar mobility correlated negatively with ESM activity in the AS patients. No allowance was made in this study for any effect of a tight hamstring on lumbar mobility. However, flexion relaxation of the hamstring muscles does not depend on and is not closely linked to back-muscle behavior [22]. In AS the zygopohyseal joints are often affected. Irritation of zygopophyseal joints or the intervertebral discs can increase the activity of segmental back muscles [23]. Such irritation might also be found in AS patients. However, in this study extents of spinal radiological changes were not evaluated. Stiffness and pain in AS patients could also lead to deterioration in neuromuscular control. This has been demonstrated in other kinds of patients with LBP [10], and could lead to abnormal lumbopelvic rhythm. Reasons for changes in paravertebral EMG activity in LBP patients include postural aberrations such as guarding and splinting, disuse related to chronic pain, and overstrain injuries because of lessened stability [11,24,25]. Patients with AS may exhibit serious postural changes and disuse related to pain. The sample in the study was too small to allow any conclusions to be drawn about associations between these factors and SEMG activity. To maximize the reliability of the study results and minimize sources of error, one PT carried out all measurements. Earlier, Ahern et al. had shown within-session reproducibility of lumbar paravertebral EMG to be high, and greater than between-session reproducibility [13]. In our study reproducibilities within and between observers differed from stage to stage of lumbopelvic rhythm but were mostly adequate [21]. In the present study no correlation between pain and muscle activity during flexion was found but the sample was too small to allow conclusions to be drawn, especially because only some of the AS patients reported pain. Pain did not increase during flexion and re-extension. On the contrary, movement decreased pain in some patients. This effect is usual in patients with chronic AS. To determine whether improvement in mobility reduces ESM activity as measured by EMG during full flexion in AS patients further studies are needed.

4 292 P. Heinonen et al. / Pathophysiology 12 (2005) In this study some AS patients exhibited flexion relaxation even though lumbar mobilities were low. Flexion relaxation occurred earlier than in the controls. ESM relaxation during full flexion may be based on limitation of mobility of lumbar vertebrae after flexion, or it may be a reflex action following distension of ligaments, muscles and zygopophyseal joints. ESM relaxation is spontaneous in healthy individuals. It is most likely explained by reflex control [10,13,26 28].In healthy individuals ESM relaxation has been found to occur only if every segment of the lumbar spine has reached the endpoint of flexion [29]. Sihvonen et al. have shown that absence of flexion relaxation in LPB patients was the commonest difference in relation to controls [9]. In LPB patients, there is evidence that lack of flexion relaxation correlates with duration of symptoms and extent of disturbance of lumbopelvic rhythm [15]. Results of measurement of ESM activity by means of EMG in AS patients in a static upright position did not differ from those in controls in the same position. In LPB patients, there have been both similar [11] and dissimilar findings [9]. Sihvonen et al. found markedly greater activity of paraspinal muscles, as measured by EMG, in LPB patients in the standing position than in controls in the same position. During flexion LPB patients exhibited higher average EMG activity as compared with the level of activity reached during reextension than controls [9]. In the present study reported, as in a previous study [27], surface EMG activities measured at two levels (L1-2, L4-5) did not differ significantly. During re-extension, muscle activity during concentric work was lower in the AS patients than in the controls but the difference is not statistically significant. Lower EMG activity at the L3 level has been found in LPB patients than in controls [10]. This study is the first in which ESM function has been evaluated using paravertebral surface EMG in AS patients. The method would seem to be adequately reproducible but it is recommended that a single therapist undertake measurements. Fewer than half of the AS patients exhibited flexion relaxation during full flexion. Lumbar mobility correlated negatively with EMG activity during full flexion. The possible association between pain and ESM activity as measured by EMG needs further study. Determinations of whether improvement in lumbar mobility or decrease of pain reduces ESM activity, for example during rehabilitation, are important aims for future studies. References [1] M.M. Ward, Health-related quality of life in ankylosing spondylitis: a survey of 175 patients, Arthritis Care Res. 4 (1999) [2] M. Leirisalo-Repo, K. Lehtinen, Spondylarthropatiat, in: H. Isomäki, M. Leirisalo-Repo, Hämäläinen M. Duodecim (Eds.), Reumataudit, Vammalan kirjapaino Oy, Vammala, 1994, pp (in Finnish). [3] T. Oh, V. Brander, S. Hinderer, N. Alpiner, Rehabilitation in joint and connective tissue diseases. 2. Inflammatory and degenerative spine diseases, Arch. Phys. Med. Rehabil. 76 (1995) [4] M. Dalyan, A. Güner, S. Tuncer, A. Bilgics, T. Arasil, Disability in ankylosing spondylitis, Disability Rehabil. 2 (1999) [5] J. Viitanen, Selän ja rintakehän liikkuvuusmitat selkärankareumassa, Tampereen yliopisto, Tampere, [6] H. Dagfinrud, K. Hagen, Physiotherapy interventions for ankylosing spondylitis (Cochrane Review), Cochrane Database Syst. Rev. 4 (2001) CD [7] S. Heikkilä, J.V. Viitanen, H. Kautiainen, M. Kauppi, Sensitivity to change of mobility tests; effect of short term intensive physiotherapy and exercise on spinal, hip, and shoulder measurements in spondylarthropathy, J. Rheumatol. 27 (2000) [8] J.V. Viitanen, S. Heikkilä, M.L. Kokko, H. Kautiainen, Clinical assessment of spinal mobility measurements in ankylosing spondylitis: a compact set for follow-up and trials? Clin. Rheumatol. 19 (2000) [9] T. Sihvonen, J. Partanen, O. Hänninen, S. Soimakallio, Electric behavior of low back muscles during lumbar pelvic rhythm in low back pain patients and healthy controls, Arch. Phys. Med. Rehabil. 72 (1991) [10] O. Shirado, T. Ito, K. Kaneda, T. Strax, Flexion relaxation phenomenon in the back muscles. A comparative study between healthy subjects and patients with chronic low back pain, Am. J. Phys. Med. Rehabil. 2 (1995) [11] D. Ahern, M. Follick, J. Council, N. Laser-Wolston, H. Litchman, Comparison of lumbar paravertebral EMG patterns in chronic low back pain patients and non-patient controls, Pain 34 (1988) [12] D.K. Ahern, D.J. Hannon, A.J. Goreczny, M.J. Follick, J.R. Parziale, Correlation of chronic low-back pain behavior and muscle function examination of the flexion relaxation response, Spine 15 (1990) [13] D. Ahern, M. Follick, J. Council, N. Laser-Wolston, Reliability of lumbar paravertebral EMG assessment in chronic low back pain, Arch. Phys. Med. Rehabil. 67 (1986) [14] M. Gauvin, D. Riddle, J. Rothstein, Reliability of clinical measurements of forward bending using the modified finger-to-floor method, Phys. Ther. 70 (1990) [15] A.M. Kaigle, P. Wessberg, T.H. Hansson, Muscular and kinematic behavior of the lumbar spine during flexion extension, J. Spinal. Disord. 2 (1998) [16] T. Sihvonen, J. Partanen, O. Hänninen, Averaged (rms) surface EMG in testing back function, Electromyogr. Clin. Neurophysiol. 28 (1988) [17] F.P. Valencia, R.R. Munro, An electromyographic study of the lumbar multifidus in man, Electromyogr. Clin. Neurophysiol. 25 (1985) [18] H.A. Bird, W. Esselinckx, A.S. Dixon, A.G. Movat, P.H. Wood, An evaluation of criteria for polymyalgia rheumatica, Ann. Rheum. Dis. 37 (1979) [19] J. Viitanen, K. Lehtinen, Selkärankareuman diagnosointi ja hoito, Suomen Lääkärilehti 42 (2000) (in Finnish). [20] LI-K. Lin, Concordance correlation coefficient to evaluate reproducibility, Biometrics 45 (1989) [21] P. Heinonen, M. Mikkelsson, T. Salo, H. Kautiainen, Intertester repeatability of surface EMG measurement in Erector spinae muscles from upright position in AS patients and healthy controls, Fysioterapia 5 (2001) 9 13 (in Finnish). [22] T. Sihvonen, Flexion relaxation of the hamstring muscles during lumbar-pelvic rhythm, Arch. Phys. Med. Rehabil. 78 (1999) [23] A. Indahl, A.M. Kaigle, O. Reikerås, S.H. Holm, Interaction between the porcine lumbar intervertebral disc, zygopophyseal joints, and paraspinal muscles, Spine 24 (1997) [24] N. Paquet, F. Malouin, L. Richards, Hip-spine movement interaction and muscle activation patterns during sagittal trunk movements in low back pain patients, Spine 5 (1994)

5 P. Heinonen et al. / Pathophysiology 12 (2005) [25] S.L. Wolf, M. Nacht, J.L. Kelly, EMG biofeedback training during dynamic movement for low back pain patients, Behav. Ther. 13 (1982) [26] S. Taimela, S. Luoto, Onko selkävaivan kroonistumisen syynä liikkeiden säätelyn häiriö? Duodecim 116 (1999) (in Finnish). [27] M.A. Adams, W.C. Hutton, J.R.R. Stott, The resistance to flexion of the lumbar intervertebral joint, Spine 5 (1980) [28] J. Triano, A. Schultz, Correction of objective measure of trunk motion and muscle function with low back pain disability ratings, Spine 6 (1987) [29] S. Roy, L. Oddsson, Classification of paraspinal muscle impairments by surface electromyography, Phys. Ther. Rev. 8 (1998)

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