ORIGINAL ARTICLE
Relationship Between Electromyographic Signal Amplitude and Thickness Change of the Trunk Muscles in Patients With and Without Low Back Pain Olivera Djordjevic, MD,*w Ljubica Konstantinovic, MD, DSc, PhD,*w Nadica Miljkovic, DSc, PhD,zy and Goran Bijelic, MScy
Objectives: To compare the relative thickness change of the transversal abdominal (TrA) and lumbar multifidus (LM) muscles during activation in individuals with and without low back pain (LBP), and to establish a relationship between surface electromyography (sEMG) signal amplitude and the relative thickness change of the corresponding muscle during clinically relevant activity, with preferential activation of TrA/LM. Materials and Methods: Thirty-seven pain-free participants and 36 LBP patients were assessed by ultrasound for thickness changes of TrA and LM and by sEMG for changes of electrical activity of the same muscles. sEMG is done with wireless LUMBIA system. The position of the sEMG sensors and activation maneuvers were chosen carefully. Results: Significant group effect was found for relative thickness change of TrA (F1,142 = 60.69, P < 0.0001) and LM (F1,142 = 36.01, P < 0.0001). We found significant correlations between relative thickness change of TrA and sEMG signal amplitude on both sides for LBP (r = 0.46 to 0.63, P < 0.05) and pain-free patients (r = 0.43-0.47, P < 0.05). The correlation between LM thickness change and sEMG was significant in pain-free participants for both sides (r = 0.36 to 0.38 P < 0.05), and right LM in LBP participants (r = 0.43, P < 0.05), but not for LM in LBP group (r = 0.16, P = 0.351). Discussion: US and sEMG measurements can be used for objective TrA/LM assessment. Correlation results suggest that the relative change of the muscle thickness could be used as the indicator of the muscle activity. Insight into the activity of TrA/LM in pain-free individuals and LBP patients during and after painful episodes may clarify the role of functional abnormalities of these muscles in LBP. Key Words: low back pain, ultrasound, electromyography
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ow back pain (LBP) is a highly prevalent condition with great socioeconomic impact. It is estimated that 9.2% of a global population have LBP and LBP-related disability is the leading cause of disability in the world.1 Unfortunately,
Received for publication May 9, 2014; revised November 29, 2014; accepted October 22, 2014. From the *Clinic for Rehabilitation, “Dr M. Zotovic”; wFaculty of Medicine; zFaculty of Electrical Engineering, University of Belgrade, Belgrade; and yTecnalia Serbia Ltd., Belgrade, Serbia. This research was registered at public trial registry ClinicalTrials.gov. Study ID Number: EMGUS, ClinicalTrials.gov Identifier: NCT01979783. Supported in part by the Ministry of Education, Science, and Technological Development, Republic of Serbia, Belgrade, Serbia, No. 175016. The authors declare no conflict of interest. Reprints: Olivera Djordjevic, MD, Clinic for Rehabilitation, “Dr M. Zotovic,” Sokobanjska 13a, Belgrade 11000, Serbia (e-mail: odordev@ eunet.rs). Copyright r 2014 Wolters Kluwer Health, Inc. All rights reserved. DOI: 10.1097/AJP.0000000000000179
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we still lack the optimal therapeutic strategy, which partially may be because the etiopathogenesis of certain forms of LBP is not fully explained. The incompetent motor control of muscles that act as deep stabilizers of a lumbosacral spine has been identified in certain forms of LBP, but the causal relationship between the 2 has not been established. Structural abnormalities such as hypotrophy,2–6 excessive fat infiltration,7 abnormal distribution of slow twitch versus fast twitch muscular fibers types8 in these muscles have been reported in patients with LBP. Functional deficits such as decrease of relative thickness change of transversal abdominal (TrA) and lumbar multifidus (LM) muscle during activation9–11 and delayed anticipatory activation of TrA12–15 and LM16 during trunk or limb movement, in these muscles have been reported in patients with LBP, even in iatrogenic-induced LBP.17 The muscle discoordination, shown in chronic LBP14,18,19 persists after the resolution of the painful episode, so, hypothetically, it may induce recurrent or chronic pain and disability.20,21 This delayed feed-forward activation of TrA is found to be associated with a posterolateral shift of TrA cortical presentation in chronic LBP compared with healthy patients, and this deviation is reversed with the skilled training of the TrA and approximates its motor cortical presentation in the pain-free individuals.22 Unfortunately, we still do not know what is the real clinical relevance of these abnormalities, nor we are aware of the real sequence of events: LBP-functional and morphologic changes of these muscles-resolution of pain. The gold standard for evaluating muscle function is electromyography (EMG). Function of TrA and LM has been evaluated by fine-wire EMG during specific activities and exercises in controlled laboratory settings.12,13,16,23 Fine-wire EMG is an invasive procedure, that requires highly trained staff and as such, is not convenient for routine clinical practice or research settings aimed to screen a larger sample of patients. Also, it is not suitable for investigating the activity of the larger sample of the muscle tissue9,14,15,24,25 In an attempt to overcome the limitations of the finewire EMG, surface EMG (sEMG) of TrA and LM emerged as an alternative. Although more convenient for application, it must be interpreted with great caution due to interference from surrounding muscles.26,27 To control the effect of cross-talk to the validity of sEMG signal, the position of the electrodes and functional tasks related to the specific activation of the muscles must be chosen carefully. The Surface Electromyography for the Non-Invasive Assessment of Muscles (SENIAM) project 28,29 has proposed clinical tests and location for surface sensors (electrodes) for 30 human muscles, including LM. Activation of LM was elicited for research purposes in numerous ways by choosing back extension in various positions and types of contractions.10,16,28–30 There is no recommendation on www.clinicalpain.com |
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sensor position for TrA in SENIAM protocol. Surface electrodes positioned over the internal oblique (IO) muscle and TrA, located just superior to the projection of the inguinal ligament and approximately 15 cm from the midline have been demonstrated to represent the fine-wire activity of TrA to within 10% to 15% of the contraction amplitude.31 It has also been demonstrated that TrA/IO sEMG signal, captured from the location just inferomedial to the anterior superior iliac spine (ASIS), is separate and distinct from the signal for rectus abdominis muscle, for specific tasks such as the drawing-in technique and the rapid limb movement task.26 The abdominal draw in maneuver (ADIM) was identified to preferentially activate TrA32–34 and that minimal superficial abdominal muscle activity occurs during this task.35–37 Ultrasound (US) has been used extensively and proven to be a valid and a reliable method for assessing the thickness and thickness change of the trunk muscles in a healthy and LBP population.38 Estimating function of the trunk muscles on the basis of US findings on changes of muscles’ morphometry, so far, has been proven to be a more challenging task.9,30,39–42 The basic rationale for engaging US as a tool for assessing muscular behavior is that muscle morphology (muscle length, muscle fascicle length, pennation angle, and muscle thickness) changes with activation.39 When the muscle produces contraction, we expect to record a deflection of its EMG signal and the muscle thickness increase on its US image. However, the association between recorded amplitude of EMG signal and the size of the muscle thickness change is not so straightforward and must be viewed in more complex context of numerous physical factors that influence the thickness of TrA and LM at rest and during contraction. The relationship between changes of muscle thickness (assessed on the US) and muscle activity (registered by EMG) have been studied for LM30 and abdominal muscles9,25,39–41,43 and dissimilar conclusions have been reported. Not only that small number of these studies have been done so far, but they mostly included small samples9,25,30,39,41,43 or healthy patients only.25,30,39–42 Only 2 of those studies40,41 explored the relationship between the abdominal muscles thickness with the sEMG signal, but neither have measured the thickness of TrA. However, the linear relationship between sEMG signal and thickness change of OE has been shown for clinically relevant OE activation (isometric trunk rotation).40 Studies on the relationship between fine-wire EMG and US of TrA have opposing conclusions: from poor correlation between EMG and US on TrA activity43; across curvilinear association which was found between the muscle activity and it’s thickness change in narrow range of 0% to 20% of maximal voluntary contraction (MVC),39 to a strong linear relationship for TrA25 and TrA and OI9 thickness change and activity recorded by fine-wire EMG. Kiesel et al30 found significant correlation between LM signal’s amplitude obtained by fine-wire EMG and thickness change assessed by US in 5 pain-free patients in a range 19% to 34% of maximal voluntary isometric contraction. Having in mind methodological differences between the conducted studies and complex factors that determine the measured thickness of the muscles,38 more comparative research of US against EMG, under controlled conditions, are warranted. The aims of this study were to investigate: (1) If there is a difference between LBP and pain-free individuals patients in relative thickness change and in sEMG signal amplitude of LM and TrA muscles, during a clinically relevant activity.
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(2) The relationship between the amplitude of sEMG signal and the relative thickness change of the corresponding LM and TrA muscle assessed by US during a clinically relevant task in patients with and without LBP.
MATERIALS AND METHODS Participants We recruited convenient sample of 37 pain-free participants and 36 participants with mechanic LBP who were referred for evaluation and treatment to the Rehabilitation Clinic “Dr Miroslav Zotovic” during the period November 2013 to January 2014. Inclusion criteria for patients with LBP were: pain that lasted 3 to 6 months, with self-reported pain levels of Z3 on the Visual Analog Scale, and the ability to remain in prone and supine hook-lying positions for 10 minutes each to ensure compliance. LBP was defined as pain localized below the costal margin and above the inferior gluteal folds, with or without leg pain.44 The exclusion criteria for all participants were: pregnancy, spinal fractures, surgery, infectious diseases, tumors, spina bifida, advanced forms of spinal deformity, hip diseases, neuromuscular disorders, and corticosteroid therapy administrated for any reason in at least 1 month before participating in the study. Clinical evaluation and magnetic resonance imaging of the lumbosacral spine has been performed in all the patients with LBP. The participants signed the informed consent form and the rights of human patients were protected. The study was approved by the Medical Research Ethic Committee of our institution. The whole procedure for LBP patients was completed before they started the treatment for LBP at the Clinic.
Procedure Demographic data and past medical history were acquired in LBP group by the examiner O.D., who also administered the 11-point Visual Analog Scale (VAS); (range, 0 to 10)45 to assess pain intensity and Oswestry Low Back Pain Disability Questionnaire (range, 0 to 100)46 to assess self-reported disability in everyday life. EMG signals were recorded with the wireless LUMBIA system (BTS Bioengineering, Padova, Italy and Tecnalia Research and Innovation, San Sebastian, Spain) presented in Figure 1. LUMBIA device (LUMBIA Studio; Tecnalia Research and Innovation) was used to acquire raw EMG data. Acquisition parameters were: sample rate of 1000 samples per second, gain of 1000, and resolution of A/D conversion of 16 bits. Bluetooth-based communication was used to transfer data from the device to the computer. The BTS FREEEMG Preamplifiers (BTS Bioengineering) are placed in the belt garment.47 We cleaned the skin with Nuprep abrasive gel (BioMedical Instruments Inc., Warren, MI) and placed the disposable surface Ag/AgCl electrodes Skintact F-TC1 (Leonhard Lang GmbH, Innsbruck, Austria), for LM, according to SENIAM protocol28,29 (Fig. 2). The electrodes for TrA were positioned on the anterior abdominal wall, just medial to the ASIS and just superior to the projection of the inguinal ligament26,31 (Fig. 3). Bipolar sensors were placed parallel to the dominant muscle fibers orientation, with the interelectrode (center to center) distance of 20 mm. The electrodes for LM were placed while the participant was in prone, and for TrA while the patient was in supine hook-lying position. The reference electrode was placed on the projection of the C7 vertebral spinous process. Ultrasound Toshiba Diagnostic Ultrasound System (Nemio SSA-550 A, 3.75 [3-6] MHz curvilinear probe) was used. The images were acquired in B—mode by examiner
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Electromyographic Signal Amplitude and Thickness Change of the Trunk Muscles
FIGURE 1. Lumbia device. The pairs of white circles are the attached surface electrodes that will be placed on the designated location for surface electromyography signal acquisition. The maximal 6 pairs of the electrodes can be attached to this device at the same time. We used 4 pairs: 1 pair for lumbar multifidus muscle on each side, and a pair for right and left transversal abdominal muscle.
FIGURE 3. Two pairs of surface electrodes applied in supine position, just medioinferior to the anterior superior iliac spine, represent the sensors’ position for the acquisition of the electromyography signal from right and left transversal abdominal muscle.
O.D., who previously proven to be able to take reliable measures of TrA and LM for LBP and healthy patients with the same tasks and using the same US unit (O.D., unpublished data, 2013): the intrarater intraclass correlation coefficients (ICC2,1) during rest and contraction ranged from 0.94 to 1.00 in 56 LBP and 42 pain-free participants. The ICC values for relative thickness change were from 0.79 to 0.99 for both LBP and pain-free participants. The intrarater SEM ranged from 0.16 to 0.33 mm, except for LM in healthy patients (0.86 to 0.88 mm). TrA and LM muscle thickness was measured bilaterally using the onscreen calipers. The side measured first was counterbalanced. The raters were not blind to group allocation. The raters who performed US and EMG recordings were blind to each other’s measurements.
US Measurement and sEMG of TrA TrA muscle was assessed in the supine hook-lying position with the US transducer placed transversely just above the iliac crest in the mid-axillary line.10 The participant was instructed to breathe normally. The ultrasonography image at rest was taken at the end of quiet inspiration.25,34 The US image in maximal contraction of TrA was captured when the participant followed the instruction to exhale and to draw the stomach in slowly as much as possible. The hypoechoic tissue of the muscle was measured only, and no hyperechoic fascial thickness was taken into account (Fig. 4). SEMG from the TrA was captured in the same position of the patient, first during voluntary expiration and then during maximal drawing in
FIGURE 2. Two pairs of the white circles in the lumbar region represent the position of the surface electrodes for acquisition of the electromyography signal from right and left lumbar multifidus muscle. Also the flexible goniometer with the Angle Display Unit for assessing the lumbosacral junction angle is shown.
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FIGURE 4. Examples of thickness measurements in transverse abdominal muscles from a pain-free participant during relaxation (right) and contraction (left). The vertical bar spans the boundary between the muscle and fascia (calibration 1 cm between each dot). The values for transversal abdominal are 7.5 mm (left) and 4.9 mm (right).
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of the front abdominal wall (ADIM) at the end of the selfchosen expiration.
US Measurements and sEMG of LM The LM muscle thickness was assessed in the prone position with the pillow placed under the abdomen to reduce lumbosacral junction angle to 0.05. BMI indicates body mass index; LBP, low back pain; ODS, Oswestry Disability Score; VAS, Visual Analog Scale.
TABLE 3. Group Mean ± SD Values for the Normalized Amplitude sEMG Signal of Transverse Abdominal (TrA) and Lateral Multifidus (LM) Muscles in Low Back Pain (LBP) and Painfree Participants
sEMG Side TrA* LM*
LBP
Pain-free
Normalized Signal Amplitude
Normalized Signal Amplitude
0.16 ± 0.19 0.15 ± 0.18 0.81 ± 0.18 0.81 ± 0.23
0.69 ± 0.38 0.54 ± 0.30 0.69 ± 0.31 0.71 ± 0.28
Right Left Right Left
*Significant effect of the group factor (Fb1, P < 0.05). LBP indicates low back pain; LM, lumbar multifidus muscle; TrA, transversal abdominal muscle.
RESULTS Age, body mass index, and distribution by sex are displayed in Table 1. The groups were age matched (P = 0.804). The LPB patients reported on average moderate levels of pain (5.25 ± 2.74) that lasted 3 to 6 months before the enrollment and caused moderate disability (28.75 ± 11.26) (Table 1). Twenty-seven of 36 LBP participants (75%) had radicular leg pain.
The Main Effects of the Group, Side, and Interaction Group¾Side (Tables 2 and 3) US (Table 2) TrA: The effect of group (F1,36 = 7.527, P = 0.009, Z2 = 0.84, large effect), sides (F3,108 = 144,47, P < 0.0001, Z2 = 0.32, large effect), and interaction between the 2 factors (F3,108 = 20.18, P < 0.0001, Z2 = 0.36, large effect) has been found to be significant for TrA thickness at rest and contraction. According to post hoc analysis (Turkey HSD), significant difference between groups was due to the thickness both at rest and contraction (Turkey HSD > 0.42) for each side. Also, each group reached significantly thicker TrA at contraction comparing to its thickness at rest (Turkey HSD > 0.78), whereas the thickness of the TrA both at rest and contraction was symmetrical within each group (Turkey HSD < 0.78). The relative change of the TrA was significantly different between LBP and non-LBP group (F1,142 = 60.69, P < 0.0001, Z2 = 0.3, large effect). No significant effect of the side (F1,142 = 1.2, P = 0.275, Z2 = 0.008, small effect), nor interaction between groupside (F1,142 = 0.24, P = 0.673, Z2 = 0.0016, small effect) was found (Table 2).
LM: No statistically significant effect of the group factor was found for the thickness of LM at rest and maximal contraction (F1,36 = 0.1635, P = 0.688, Z2 = 0.92, large effect). The effect of the side at rest and contraction was significant (F3,108 = 302.15, P < 0.0001, Z2 = 0.02, medium effect), and this was due to the significant difference between rest and contraction within each group (post hoc HSD > 2.3) on both sides. Interaction group side was significant (F3,108 = 6.6867 P = 0.000350, Z2 = 0.16, large effect). The effect of the group was found to be significant for the relative thickness change of the LM (F1,142 = 36.01, P < 0.0001, Z2 = 0.2, large effect), whereas the effect of the side and interaction groupside was not found to be significant (F1,142 = 0.34, P = 0.5608, Z2 = 0.002, small effect) (Table 2).
sEMG (Table 3) TrA: The normalized amplitudes of the sEMG for TrA were significantly different between the 2 groups (F1,142 = 31.05, P < 0.0001, Z2 = 0.18, large effect), whereas the effect of the side or interaction group side was not found to be significant (F1,142 = 1.05, P = 0.307, Z2 = 0.007 small effect; F1,142 = 0.8, P = 0.373, Z2 = 0.0007 small effect, respectively) (Table 3). LM: The normalized amplitudes of the sEMG for LM were significantly different between the 2 groups (F1,142 = 5.81, P = 0.0173, Z2 = 0.04, medium effect), whereas the effect of the side or interaction groupside was not found to be significant (F1,142 = 0.12, P = 0.7296, F1,142 = 0.12, P = 0.7296, respectively, Z2 = 810 4, small effect) (Table 3).
TABLE 2. Group Mean ± SD Values for the Thickness of Transverse Abdominal (TrA) and Lateral Multifidus (LM) Muscles at Rest (mm), During Contraction (mm), Maximal Contration (mm), and the Relative Thickness Change (Unitless) From Rest to Maximal Contraction in Low Back Pain (LBP) and Pain-free Participants Measured by Ultrasound
LBP Muscles Side
Rest (mm)
TrA*,** Right 4.3 ± 1.1 Left 4.3 ± 1.2 LM Right 27.0 ± 4.7 Left 28.2 ± 5.2
Contracted (mm)
Maximum Contracted (mm)
NA NA 34.2 ± 5.0 35.0 ± 6.9
6.6 ± 1.9 6.5 ± 2.2 35.7 ± 5.8 36.8 ± 6.6
Pain-free Change
Rest (mm)
0.6 ± 0.3 4.0 ± 1.0 0.5 ± 0.3 4.1 ± 1.3 0.3 ± 0.2* 26.9 ± 4.7 0.3 ± 0.2* 27.4 ± 5.6
Contracted (mm)
Maximum Contracted (mm)
Change
NA NA 35.1 ± 5.2 35.9 ± 6.2
8.4 ± 2.8 8.5 ± 3.0 37.9 ± 4.8 38.6 ± 5.4
1.1 ± 0.5 1.0 ± 0.5 0.4 ± 0.2* 0.4 ± 0.2*
*Significant effect of the group factor (Fb1, P < 0.05). **Significant effects of the group factor and significant interaction group side (Fb1, P < 0.05). LBP indicates low back pain; LM, lumbar multifidus muscle; TrA, transversal abdominal muscle.
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TABLE 4. Correlation Coefficient (r) Between Relative Thickness Change With sEMG Signal of the Corresponding Muscle During Relevant Clinical Activity, Displayed Along With 95% Confidence Interval (95% CI)
Correlation Coefficient r (95% CI) Muscles
Side
TrA
Right Left Right Left
LM
LBP 0.46* 0.63* 0.43* 0.16
(0.16-0.69) (0.38-0.79) (0.12-0.66) ( 0.18 to 0.46)
Pain-free 0.43* 0.47* 0.38* 0.36*
(0.12-0.66) (0.17-0.69) (0.06-0.63) (0.04-0.61)
*P < 0.05. CI indicates confidence interval; LBP, low back pain; LM, lumbar multifidus muscle; TrA, transversal abdominal muscle.
Correlation Between the Muscles’ Relative Thickness Change and the Amplitude of EMG Signal From the Corresponding Muscle (Table 4)
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studies.9,10,39,49 These findings are considered to demonstrate functional deficits of deep stabilizers of lumbosacral spine in chronic LBP.1,9
The Correlation Between US Measurements and sEMG Signal On the basis of the correlation results, we might assume that surface EMG and TrA thickness change assessed by US in both LBP and healthy patients can be used interchangeably, and more important, that the relative thickness of the muscle can be used as an indicator of muscle activity; this pertains for LM muscles in healthy participants, but the results for LM muscles in LBP group are not so conclusive. As stated earlier, numerous physical factors contribute to the relationship between EMG signal and muscle thickness change and the results of the correlation between the 2 must be viewed in a more complex context: (1) Muscular geometry changes during contraction are 3-dimensional. Although this would probably change in
LBP Patients (Fig. 7) Pearson coefficient of correlation between the relative thickness change of right TrA and the amplitude of sEMG signal from ipsilateral TrA was significant (r = 0.46, P = 0.005). The correlation between left TrA thickness and left TrA sEMG signal amplitude was also statistically significant (r = 0.63, P = 0.000038). Correlation coefficient between the sEMG amplitude signal and relative thickness change for right LM was found to be significant (r = 0.43, P = 0.009). We did not find significant correlation between relative thickness change and amplitude of the sEMG signal for left LM (r = 0.16 P = 0.351).
Pain-free Participants (Fig. 8) The significant Pearson correlation coefficient was found for LM and TrA on both sides, between the relative thickness change and the sEMG signal for the corresponding location: for right LM r = 0.38, P = 0.02; for left LM r = 0.36, P = 0.028; for right TrA r = 0.43, P = 0.0079; for left TrA r = 0.47, P = 0.0033). Correlation coefficients (r) for LBP and pain-free participants are displayed in Table 4, along with the corresponding 95% confidence interval of the r.
DISCUSSION The results of our study indicate that the relative thickness change of the TrA and LM are significantly smaller in LBP than healthy individuals in selected, clinically relevant activity. Relative thickness change of the TrA assessed by US correlated significantly with the sEMG signal from the anterior abdominal wall just inferomedial to the SIAS, on both sides for LBP and healthy participants during ADIM. The correlation between LM thickness change and correspondent sEMG signal was significant in pain-free participants for both sides, and for right LM in LBP participants. Left LM thickness change did not correlate with the normalized EMG signal amplitude during the selected task in the LBP group.
Difference Between the Relative Thickness Change of the TrA and LM The significantly smaller increase of the TrA and LM thickness during the contraction in LBP group comparing to pain-free individuals was also found in previous
FIGURE 7. Relationship between relative thickness change and surface electromyography (sEMG) of the corresponding muscle in low back pain (LBP) patients. LM indicates lumbar multifidus.
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Electromyographic Signal Amplitude and Thickness Change of the Trunk Muscles
FIGURE 8. Relationship between relative thickness change and surface electromyography (sEMG) of the corresponding muscle in healthy patients. LM indicates lumbar multifidus; TrA, transversal abdominal.
the near future, the images of the muscles have, so far, been assessed in 2-dimensional US, and as such does not provide full information on muscle thickness change. (2) Muscle activity is only one of the factors that influence the measured thickness of the muscle. The change in muscle length is influenced by the type of contraction, resting state of the muscle, external forces the muscle is competing against (compression by intra-abdominal pressure, surrounding muscle forces), extensibility, and the orientation of the muscle fibers.38 Conflicting findings of several studies that researched the relationship between EMG and US of abdominal wall muscles9,25,39–41,43 reflect not only methodological differences between them, but also not so easily controlled parallelism between EMG and US findings on these muscles thickness changes. Illustrative example of this complexity are findings in Whitakker et al,43 where 2 patients who, during the active straight leg test, demonstrated an increase in TrA EMG signal amplitude that was associated with either no change or a decrease in TrA thickness. The conclusions on the relationship between EMG and US become even more debatable if the EMG is done with surface electrode, with its major drawback in mind, cross-talk of the surrounding muscles. In contrast, surface EMG is user friendly, easily applicable in routine clinical and research practice for examining a larger sample of participants. As fine-wire EMG reflects the muscle activity of a small sample of muscle, and regional differences in TrA activity have been established during ADIM maneuver,35 sEMG may be more informative for estimating overall muscle Copyright
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activity. Fine-wire EMG studies of abdominal muscles activity showed that TrA is predominantly active during ADIM, whereas the rest of the abdominal muscles are minimally active or silent.35 Nevertheless, we can only assume that sEMG of anterior abdominal wall, from the point just medial to the ASIS, reflected predominantly TrA signal during voluntary expiration and ADIM. Comparison with the results of the other studies of the association between EMG recordings and thickness change for TrA is not so informative, due to the fact that the only 2 studies who investigated the relationship of surface EMG and abdominal wall muscle thickness did not measure TrA, but either OE40 or OE and OI.41 Different conclusion have been reached in the studies of that employed fine-wire EMG of the TrA: from poor correlation,43 across curvilinear association in narrow range of 0% to 20% of MVC,39 to strong linear relationship for TrA25 and TrA and OI.9 Although lying under OE and OI, TrA is predominantly active during ADIM, while the more superficial muscles are minimally involved.32–35 Thus, we may assume that TrA would dominantly contribute to the signal amplitude of the anterior abdominal wall muscle during ADIM, and we considered that research of the relationship between sEMG from the given location and TrA thickness change deserved attention. In our sample, significant correlation between TrA sEMG and thickness change in both LBP and healthy patients on both right and left side could be more grounded if we used ramped muscle contraction and this is one of the limitations of our study.
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The estimates of sensitivity of surface EMG sensors for LM are conflicting.27,50 Analyzing the correlation between surface and intramuscular EMG signal in 3 patients, Stokes et al27 suggested that the surface electrodes placed over multifidus muscles were more sensitive to activity in the adjacent longissimus than to activity in the underlying multifidus muscles. No detailed description of the position of the surface electrode for LM was provided. The report by Arokoski et al50 suggested that surface electrodes were sensitive to multifidus muscle activity. Although placed carefully according to SENIAM protocol for LM, we also cannot exclude that surface sensors were selective for LM only during back extension and contralateral arm lift. To our knowledge, no studies of the relationship between surface EMG signal and LM thickness change for both pain-free and LBP groups have been done so far. Kiesel et al30 found significant correlation between LM signal’s amplitude obtained by fine-wire EMG and thickness change assessed by US in 5 pain-free individuals in a range 19% to 34% of maximal voluntary isometric contraction. Significant correlation between LM EMG amplitude and its thickness change that we found in the pain-free individuals has to be considered with caution, as we used sEMG during the 2 levels of the LM contraction. The relationship between the 2 is less clear in LBP group, where the signal amplitude for left LM did not correlate with thickness change. Analyzing the data more closely, we identified 10 patients whose voluntary contraction of left LM had larger amplitude EMG signal than contraction against resistance of the examiner (which was supposed to be maximal contraction). This was also recorded in the pain-free group and in right LM sEMG measurements in the LBP group, but to a much lesser extent (only 2 of 37 pain-free individuals for right and left LM, and 4 of 36 in right LM sEMG). Analyzing the distribution of pain in the patients with unilateral presence of pain, 7 of these 10 patients who performed voluntary contraction of left LM stronger than the contraction against the resistance, had unilateral left back pain. Although expected to some degree (and frequently mentioned as a drawback of normalization procedures to MVCs), we feel that this rate (7 of 10) is rather high, and could be the reflection of the inability of these patients to perform MVC against resistance competently. For example, analyzing of the self-reported pain intensity VAS, we noticed that VAS in these unilateral left painful patients whose left LM sEMG signal during voluntary contraction was higher than in contraction against resistance, was 6.44, whereas in those unilateral left painful LBP patients whose voluntary contraction has a lower EMG amplitude than the contraction against the resistance, VAS was 4.10. Alternatively, we could perform another type of normalization procedure, but with considerable reservation for comparing EMG signals across patients.51–53 Relative thickness change of TrA and LM is different between LBP and non-LBP participants. It correlates with the sEMG amplitude, so relative thickness change can be, cautiously, viewed as an objective measure of the level of the muscle activation during contraction. Currently, we are unaware of the clinical relevance of the morphologic and functional deficits findings of our study. Objective assessment of the TrA and LM is lacking in clinical practice. These muscles are designated as the key stabilizing muscles of the lumbar spine. We do not know whether their morphologic and functional deficits, already
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described in LBP, are primary event or adaptive behavior regarding to pain occurrence. Introducing objective and simple method for estimation and monitoring these muscles’ function in healthy patients and in LBP during and after pain episodes in a longer period could be beneficial in better understanding the sequence of events (pain-changes in TrA and/or LM-resolution of pain-potential reversibility of the muscles changes). Clarifying of this etiopatologic conundrum could also implicate therapeutic strategies of certain forms of LBP, which are, currently insufficiently embedded in evidence-based practice.
Limitations of the Study (1) sEMG and US were not simultaneously recorded, but US measurements followed EMG recordings of the corresponding muscle. (2) No reliability study for sEMG recordings was conducted. (3) Muscle tasks comprised of only 2 levels of contraction for each muscle. Ramped contraction of LM and TrA would give a more detailed relationship between the thickness change and EMG amplitude. (4) No additional stratification according to key examination findings, aimed for subsequent interventions according to the treatment-based classification system, among LBP patients was performed. Also, all the patients were moderately disabled, so additional stratification according to the level of disability was not possible, either. (5) Cross-talk cannot be excluded with surface EMG.
CONCLUSIONS The relative thickness change of TrA and LM, assessed on US, are significantly smaller in LBP than painfree individuals in selected, clinically relevant activity. We found significant correlations between relative thickness change of the TrA and sEMG signal amplitude on both sides, for LBP and healthy patients. The correlation between LM thickness change and sEMG signal was significant in pain-free individuals for both the sides, and for right LM in LBP participants. Left LM thickness change did not correlate with the sEMG signal amplitude during selected tasks in LBP group. REFERENCES 1. Wong AY, Parent EC, Funabashi M, et al. Do various baseline characteristics of transversus abdominis and lumbar multifidus predict clinical outcomes in nonspecific low back pain? A systematic review. Pain. 2013;154:2589–2602. 2. Wallwork TL, Stanton WR, Freke M, et al. The effect of chronic low back pain on size and contraction of the lumbar multifidus muscle. Man Ther. 2009;14:496–500. 3. Hides JA, Stokes MJ, Saide M, et al. Evidence of lumbar multifidus muscle wasting ipsilateral to symptoms in patients with acute/subacute low back pain. Spine (Phila Pa 1976). 1994;19:16572. 4. Danneels LA, Vanderstraeten GG, Cambier DC, et al. CT imaging of trunk muscles in chronic low back pain patients and healthy control subjects. Eur Spine J. 2000;9:266–272. 5. Hyun JK, Lee JY, Lee SJ, et al. Asymmetric atrophy of multifidus muscle in patients with unilateral lumbosacral radiculopathy. Spine (Phila Pa 1976). 2007;32:E598–E602. 6. Campbell WW, Vasconcelos O, Laine FJ. Focal atrophy of the multifidus muscle in lumbosacral radiculopathy. Muscle Nerve. 1998;21:1350–1353.
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7. Parkkola R, Rytokoski U, Kormano M. Magnetic resonance imaging of the discs and trunk muscles in patients with chronic low back pain and healthy control subjects. Spine (Phila Pa 1976). 1993;18:830–836. 8. Mannion AF, Kaser L, Weber E, et al. Influence of age and duration of symptoms on fibre type distribution and size of the back muscles in chronic low back pain patients. Eur Spine J. 2000;9:273–281. 9. Ferreira PH, Ferreira ML, Hodges PW. Changes in recruitment of the abdominal muscles in people with low back pain: ultrasound measurement of muscle activity. Spine (Phila Pa 1976). 2004;29:2560–2566. 10. Kiesel KB, Underwood FB, Mattacola CG, et al. A comparison of select trunk muscle thickness change between subjects with low back pain classified in the treatment-based classification system and asymptomatic controls. J Orthop Sports Phys Ther. 2007;37:596–607. 11. Teyhen DS, Williamson JN, Carlson NH, et al. Ultrasound characteristics of the deep abdominal muscles during the active straight leg raise test. Arch Phys Med Rehabil. 2009;90: 761–767. 12. 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. 1999;80: 1005–1012. 13. Hodges PW, Richardson CA. Delayed postural contraction of transversus abdominis in low back pain associated with movement of the lower limb. J Spinal Disord. 1998;11:46–56. 14. 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). 1996;21:2640–2650. 15. Hodges PW, Richardson CA. Feedforward contraction of transversus abdominis is not influenced by the direction of arm movement. Exp Brain Res. 1997;114:362–370. 16. MacDonald D, Moseley GL, Hodges PW. Why do some patients keep hurting their back? Evidence of ongoing back muscle dysfunction during remission from recurrent back pain. Pain. 2009;142:183–188. 17. Hodges PW, Moseley GL, Gabrielsson A, et al. Experimental muscle pain changes feedforward postural responses of the trunk muscles. Exp Brain Res. 2003;151:262–271. 18. Arendt-Nielsen L, Graven-Nielsen T, Svarrer H, et al. The influence of low back pain on muscle activity and coordination during gait: a clinical and experimental study. Pain. 1996;64: 231–240. 19. Zedka M, Prochazka A, Knight B, et al. Voluntary and reflex control of human back muscles during induced pain. J Physiol. 1999b;520:591–604. 20. Hodges PW, Moseley GL. Pain and motor control of the lumbopelvic region: effect and possible mechanisms. J Electromyogr Kinesiol. 2003;13:361–370. 21. Van Dieen JH, Selen LPJ, Cholewicki J. Trunk muscle activation in low-back pain patients, an analysis of the literature. J Electromyogr Kinesiol. 2003;13:333–351. 22. Tsao H, Galea MP, Hodges PW. Driving plasticity in the motor cortex in recurrent low back pain. Eur J Pain. 2010; 14:832–839. 23. Okubo Y, Kaneoka K, Imai A, et al. Electromyographic analysis of transversus abdominis and lumbar multifidus using wire electrodes during lumbar stabilization exercises. J Orthop Sports Phys Ther. 2010;40:743–750. 24. Hodges PW, Richardson CA. Relationship between limb movement speed and associated contraction of the trunk muscles. Ergonomics. 1997;40:1220–1230. 25. McMeeken JM, Beith ID, Newham DJ, et al. The relationship between EMG and change in thickness of transversus abdominis. Clin Biomech (Bristol, Avon). 2004;19:337–342. 26. Marshall P, Murphy B. The validity and reliability of surface EMG to assess the neuromuscular response of the abdominal muscles to rapid limb movement. J Electromyogr Kinesiol. 2003;13:477–489.
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27. Stokes IA, Henry SM, Single RM. Surface EMG electrodes do not accurately record from lumbar multifidus muscles. Clin Biomech (Bristol, Avon). 2003;18:9–13. 28. Hermens HJ, Freriks B, Merletti R, et al. European Recommendations for Surface ElectroMyoGraphy, Deliverable of the SENIAM Project. Roessingh Research and Development b.v.; 1999. 29. Freriks B, Hermens HJ. European Recommendations for Surface ElectroMyoGraphy, Results of the SENIAM Project. Roessingh Research and Development b.v.; 1999. CD-rom. Vi20. 30. Kiesel KB, Uhl TL, Underwood FB, et al. Measurement of lumbar multifidus muscle contraction with rehabilitative ultrasound imaging. Man Ther. 2007;12:161–166. 31. McGill S, Juker D, Kropf P. Appropriately placed surface EMG electrodes reflect deep muscle activity (psoas, quadratus lumborum, abdominal wall) in the lumbar spine. J Biomech. 1996;29:1503–1507. 32. Goldman JM, Lehr RP, Millar AB, et al. An electromyographic study of the abdominal muscles during postural and respiratory manoeuvres. J Neurol Neurosurg Psychiatry. 1987;50:866–869. 33. Strohl KP, Mead J, Banzett RB, et al. Regional differences in abdominal muscle activity during various maneuvers in humans. J Appl Physiol Respir Environ Exerc Physiol. 1981; 51:1471–1476. 34. De Troyer A, Estenne M, Ninane V, et al. Transversus abdominis muscle function in humans. J Appl Physiol 1985. 1990;68:1010–1016. 35. Urquhart DM, Hodges PW, Allen TJ, et al. Abdominal muscle recruitment during a range of voluntary exercises. Man Ther. 2005;10:144–153. 36. Jull GA, Richardson CA, Hamilton CA, et al. Towards the Validation OFA Clinical Test for the Deep Abdominal Muscles in Back Pain Patients. Australia: Proceedings of Ninth Biennial Conference of the Manipulative Physiotherapists Association of Australia, Gold Coast; 1995:22–32. 37. Richardson CA, Jull GA, Richardson BA. A Dysfunction of the Deep Abdominal Muscles Exists in Low Back Pain Patients. Washington, DC: Proceedings of World Confederation of Physical Therapists; 1995:932. 38. WhittakerJ L, Stokes M. Ultrasound imaging and muscle function. J Orthop Sports Phys Ther. 2011;41:572–580. 39. Hodges PW, Pengel LH, Herbert RD, et al. Measurement of muscle contraction with ultrasound imaging. Muscle Nerve. 2003;27:682–692. 40. John EK, Beith ID. Can activity within the external abdominal oblique be measured using real time ultrasound imaging? Clin Biomech (Bristol, Avon). 2007;22:972–979. 41. Brown SH, McGill SM. A comparison of ultrasound and electromyography measures of force and activation to examine the mechanics of abdominal wall contraction. Clin Biomech (Bristol, Avon). 2010;25:115–123. 42. Cuesta-Vargas AI, Gonzalez-Sanchez M. Relationship of moderate and low isometric lumbar extension through architectural and muscular activity variables: a cross sectional study. BMC Med Imaging. 2013;13:38. 43. Whittaker JL, McLean L, Hodder J, et al. Association between changes in electromyographic signal amplitude and abdominal muscle thickness in individuals with and without lumbopelvic pain. J Orthop Sports Phys Ther. 2013;43: 466–477. 44. Krismer M, van Tulder M. Strategies for prevention and management of musculoskeletal conditions. Low back pain (non-specific). Best Pract Res Clin Rheumatol. 2007;21:77–91. 45. Price DD, McGrath PA, Rafii A, et al. The validation of visual analogue scales as ratio scale measures for chronic and experimental pain. Pain. 1983;17:45–56. 46. Fritz JM, Irrgang JJ. A comparison of a modified Oswestry Low Back Pain Disability Questionnaire and the Quebec Back Pain Disability Scale. Phys Ther. 2001;81:776–788.
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47. Miljkovic N, Bijelic G, Dordevic O, et al. EMG and Ultrasound Imaging Measurements of Low Back Muscles. San Sebastia´n, Spain: Proceedings of the 18th IFESS Annual Conference; 2013:199–202. 48. Cohen J. Statistical Power Analysis for the Behavioral Sciences. New York, NY: Routledge Academic; 1988. 49. Teyhen DS, Bluemle LN, Dolbeer JA, et al. Changes in lateral abdominal muscle thickness during the abdominal drawing-in maneuver in those with lumbopelvic pain. J Orthop Sports Phys Ther. 2009;39:791–798. 50. Arokoski JP, Kankaanpaa M, Valta T, et al. Back and hip extensor muscle function during therapeutic exercises. Arch Phys Med Rehabil. 1999;80:842–850.
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51. Bolgla LA, Uhl TL. Reliability of electromyographic normalization methods for evaluating the hip musculature. J Electromyogr Kinesiol. 2007;17:102–111. 52. Knutson LM, Soderberg GL, Ballantyne BT, et al. A study of various normalization procedures for within day electromyographic data. J Electromyogr Kinesiol. 1994;4: 47–59. 53. Halaki M, Ginn K. Normalization of EMG signals: to normalize or not to normalize and what to normalize to? Computational Intelligence in Electromyography Analysis—A Perspective on Current Applications and Future Challenges, Intech; 2012:176–194.
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Relationship Between Electromyographic Signal Amplitude and Thickness Change of the Trunk Muscles in Patients With and Without Low Back Pain Olivera Djordjevic, MD,*w Ljubica Konstantinovic, MD, DSc, PhD,*w Nadica Miljkovic, DSc, PhD,zy and Goran Bijelic, MScy
Objectives: To compare the relative thickness change of the transversal abdominal (TrA) and lumbar multifidus (LM) muscles during activation in individuals with and without low back pain (LBP), and to establish a relationship between surface electromyography (sEMG) signal amplitude and the relative thickness change of the corresponding muscle during clinically relevant activity, with preferential activation of TrA/LM. Materials and Methods: Thirty-seven pain-free participants and 36 LBP patients were assessed by ultrasound for thickness changes of TrA and LM and by sEMG for changes of electrical activity of the same muscles. sEMG is done with wireless LUMBIA system. The position of the sEMG sensors and activation maneuvers were chosen carefully. Results: Significant group effect was found for relative thickness change of TrA (F1,142 = 60.69, P < 0.0001) and LM (F1,142 = 36.01, P < 0.0001). We found significant correlations between relative thickness change of TrA and sEMG signal amplitude on both sides for LBP (r = 0.46 to 0.63, P < 0.05) and pain-free patients (r = 0.43-0.47, P < 0.05). The correlation between LM thickness change and sEMG was significant in pain-free participants for both sides (r = 0.36 to 0.38 P < 0.05), and right LM in LBP participants (r = 0.43, P < 0.05), but not for LM in LBP group (r = 0.16, P = 0.351). Discussion: US and sEMG measurements can be used for objective TrA/LM assessment. Correlation results suggest that the relative change of the muscle thickness could be used as the indicator of the muscle activity. Insight into the activity of TrA/LM in pain-free individuals and LBP patients during and after painful episodes may clarify the role of functional abnormalities of these muscles in LBP. Key Words: low back pain, ultrasound, electromyography
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L
ow back pain (LBP) is a highly prevalent condition with great socioeconomic impact. It is estimated that 9.2% of a global population have LBP and LBP-related disability is the leading cause of disability in the world.1 Unfortunately,
Received for publication May 9, 2014; revised November 29, 2014; accepted October 22, 2014. From the *Clinic for Rehabilitation, “Dr M. Zotovic”; wFaculty of Medicine; zFaculty of Electrical Engineering, University of Belgrade, Belgrade; and yTecnalia Serbia Ltd., Belgrade, Serbia. This research was registered at public trial registry ClinicalTrials.gov. Study ID Number: EMGUS, ClinicalTrials.gov Identifier: NCT01979783. Supported in part by the Ministry of Education, Science, and Technological Development, Republic of Serbia, Belgrade, Serbia, No. 175016. The authors declare no conflict of interest. Reprints: Olivera Djordjevic, MD, Clinic for Rehabilitation, “Dr M. Zotovic,” Sokobanjska 13a, Belgrade 11000, Serbia (e-mail: odordev@ eunet.rs). Copyright r 2014 Wolters Kluwer Health, Inc. All rights reserved. DOI: 10.1097/AJP.0000000000000179
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we still lack the optimal therapeutic strategy, which partially may be because the etiopathogenesis of certain forms of LBP is not fully explained. The incompetent motor control of muscles that act as deep stabilizers of a lumbosacral spine has been identified in certain forms of LBP, but the causal relationship between the 2 has not been established. Structural abnormalities such as hypotrophy,2–6 excessive fat infiltration,7 abnormal distribution of slow twitch versus fast twitch muscular fibers types8 in these muscles have been reported in patients with LBP. Functional deficits such as decrease of relative thickness change of transversal abdominal (TrA) and lumbar multifidus (LM) muscle during activation9–11 and delayed anticipatory activation of TrA12–15 and LM16 during trunk or limb movement, in these muscles have been reported in patients with LBP, even in iatrogenic-induced LBP.17 The muscle discoordination, shown in chronic LBP14,18,19 persists after the resolution of the painful episode, so, hypothetically, it may induce recurrent or chronic pain and disability.20,21 This delayed feed-forward activation of TrA is found to be associated with a posterolateral shift of TrA cortical presentation in chronic LBP compared with healthy patients, and this deviation is reversed with the skilled training of the TrA and approximates its motor cortical presentation in the pain-free individuals.22 Unfortunately, we still do not know what is the real clinical relevance of these abnormalities, nor we are aware of the real sequence of events: LBP-functional and morphologic changes of these muscles-resolution of pain. The gold standard for evaluating muscle function is electromyography (EMG). Function of TrA and LM has been evaluated by fine-wire EMG during specific activities and exercises in controlled laboratory settings.12,13,16,23 Fine-wire EMG is an invasive procedure, that requires highly trained staff and as such, is not convenient for routine clinical practice or research settings aimed to screen a larger sample of patients. Also, it is not suitable for investigating the activity of the larger sample of the muscle tissue9,14,15,24,25 In an attempt to overcome the limitations of the finewire EMG, surface EMG (sEMG) of TrA and LM emerged as an alternative. Although more convenient for application, it must be interpreted with great caution due to interference from surrounding muscles.26,27 To control the effect of cross-talk to the validity of sEMG signal, the position of the electrodes and functional tasks related to the specific activation of the muscles must be chosen carefully. The Surface Electromyography for the Non-Invasive Assessment of Muscles (SENIAM) project 28,29 has proposed clinical tests and location for surface sensors (electrodes) for 30 human muscles, including LM. Activation of LM was elicited for research purposes in numerous ways by choosing back extension in various positions and types of contractions.10,16,28–30 There is no recommendation on www.clinicalpain.com |
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sensor position for TrA in SENIAM protocol. Surface electrodes positioned over the internal oblique (IO) muscle and TrA, located just superior to the projection of the inguinal ligament and approximately 15 cm from the midline have been demonstrated to represent the fine-wire activity of TrA to within 10% to 15% of the contraction amplitude.31 It has also been demonstrated that TrA/IO sEMG signal, captured from the location just inferomedial to the anterior superior iliac spine (ASIS), is separate and distinct from the signal for rectus abdominis muscle, for specific tasks such as the drawing-in technique and the rapid limb movement task.26 The abdominal draw in maneuver (ADIM) was identified to preferentially activate TrA32–34 and that minimal superficial abdominal muscle activity occurs during this task.35–37 Ultrasound (US) has been used extensively and proven to be a valid and a reliable method for assessing the thickness and thickness change of the trunk muscles in a healthy and LBP population.38 Estimating function of the trunk muscles on the basis of US findings on changes of muscles’ morphometry, so far, has been proven to be a more challenging task.9,30,39–42 The basic rationale for engaging US as a tool for assessing muscular behavior is that muscle morphology (muscle length, muscle fascicle length, pennation angle, and muscle thickness) changes with activation.39 When the muscle produces contraction, we expect to record a deflection of its EMG signal and the muscle thickness increase on its US image. However, the association between recorded amplitude of EMG signal and the size of the muscle thickness change is not so straightforward and must be viewed in more complex context of numerous physical factors that influence the thickness of TrA and LM at rest and during contraction. The relationship between changes of muscle thickness (assessed on the US) and muscle activity (registered by EMG) have been studied for LM30 and abdominal muscles9,25,39–41,43 and dissimilar conclusions have been reported. Not only that small number of these studies have been done so far, but they mostly included small samples9,25,30,39,41,43 or healthy patients only.25,30,39–42 Only 2 of those studies40,41 explored the relationship between the abdominal muscles thickness with the sEMG signal, but neither have measured the thickness of TrA. However, the linear relationship between sEMG signal and thickness change of OE has been shown for clinically relevant OE activation (isometric trunk rotation).40 Studies on the relationship between fine-wire EMG and US of TrA have opposing conclusions: from poor correlation between EMG and US on TrA activity43; across curvilinear association which was found between the muscle activity and it’s thickness change in narrow range of 0% to 20% of maximal voluntary contraction (MVC),39 to a strong linear relationship for TrA25 and TrA and OI9 thickness change and activity recorded by fine-wire EMG. Kiesel et al30 found significant correlation between LM signal’s amplitude obtained by fine-wire EMG and thickness change assessed by US in 5 pain-free patients in a range 19% to 34% of maximal voluntary isometric contraction. Having in mind methodological differences between the conducted studies and complex factors that determine the measured thickness of the muscles,38 more comparative research of US against EMG, under controlled conditions, are warranted. The aims of this study were to investigate: (1) If there is a difference between LBP and pain-free individuals patients in relative thickness change and in sEMG signal amplitude of LM and TrA muscles, during a clinically relevant activity.
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(2) The relationship between the amplitude of sEMG signal and the relative thickness change of the corresponding LM and TrA muscle assessed by US during a clinically relevant task in patients with and without LBP.
MATERIALS AND METHODS Participants We recruited convenient sample of 37 pain-free participants and 36 participants with mechanic LBP who were referred for evaluation and treatment to the Rehabilitation Clinic “Dr Miroslav Zotovic” during the period November 2013 to January 2014. Inclusion criteria for patients with LBP were: pain that lasted 3 to 6 months, with self-reported pain levels of Z3 on the Visual Analog Scale, and the ability to remain in prone and supine hook-lying positions for 10 minutes each to ensure compliance. LBP was defined as pain localized below the costal margin and above the inferior gluteal folds, with or without leg pain.44 The exclusion criteria for all participants were: pregnancy, spinal fractures, surgery, infectious diseases, tumors, spina bifida, advanced forms of spinal deformity, hip diseases, neuromuscular disorders, and corticosteroid therapy administrated for any reason in at least 1 month before participating in the study. Clinical evaluation and magnetic resonance imaging of the lumbosacral spine has been performed in all the patients with LBP. The participants signed the informed consent form and the rights of human patients were protected. The study was approved by the Medical Research Ethic Committee of our institution. The whole procedure for LBP patients was completed before they started the treatment for LBP at the Clinic.
Procedure Demographic data and past medical history were acquired in LBP group by the examiner O.D., who also administered the 11-point Visual Analog Scale (VAS); (range, 0 to 10)45 to assess pain intensity and Oswestry Low Back Pain Disability Questionnaire (range, 0 to 100)46 to assess self-reported disability in everyday life. EMG signals were recorded with the wireless LUMBIA system (BTS Bioengineering, Padova, Italy and Tecnalia Research and Innovation, San Sebastian, Spain) presented in Figure 1. LUMBIA device (LUMBIA Studio; Tecnalia Research and Innovation) was used to acquire raw EMG data. Acquisition parameters were: sample rate of 1000 samples per second, gain of 1000, and resolution of A/D conversion of 16 bits. Bluetooth-based communication was used to transfer data from the device to the computer. The BTS FREEEMG Preamplifiers (BTS Bioengineering) are placed in the belt garment.47 We cleaned the skin with Nuprep abrasive gel (BioMedical Instruments Inc., Warren, MI) and placed the disposable surface Ag/AgCl electrodes Skintact F-TC1 (Leonhard Lang GmbH, Innsbruck, Austria), for LM, according to SENIAM protocol28,29 (Fig. 2). The electrodes for TrA were positioned on the anterior abdominal wall, just medial to the ASIS and just superior to the projection of the inguinal ligament26,31 (Fig. 3). Bipolar sensors were placed parallel to the dominant muscle fibers orientation, with the interelectrode (center to center) distance of 20 mm. The electrodes for LM were placed while the participant was in prone, and for TrA while the patient was in supine hook-lying position. The reference electrode was placed on the projection of the C7 vertebral spinous process. Ultrasound Toshiba Diagnostic Ultrasound System (Nemio SSA-550 A, 3.75 [3-6] MHz curvilinear probe) was used. The images were acquired in B—mode by examiner
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Electromyographic Signal Amplitude and Thickness Change of the Trunk Muscles
FIGURE 1. Lumbia device. The pairs of white circles are the attached surface electrodes that will be placed on the designated location for surface electromyography signal acquisition. The maximal 6 pairs of the electrodes can be attached to this device at the same time. We used 4 pairs: 1 pair for lumbar multifidus muscle on each side, and a pair for right and left transversal abdominal muscle.
FIGURE 3. Two pairs of surface electrodes applied in supine position, just medioinferior to the anterior superior iliac spine, represent the sensors’ position for the acquisition of the electromyography signal from right and left transversal abdominal muscle.
O.D., who previously proven to be able to take reliable measures of TrA and LM for LBP and healthy patients with the same tasks and using the same US unit (O.D., unpublished data, 2013): the intrarater intraclass correlation coefficients (ICC2,1) during rest and contraction ranged from 0.94 to 1.00 in 56 LBP and 42 pain-free participants. The ICC values for relative thickness change were from 0.79 to 0.99 for both LBP and pain-free participants. The intrarater SEM ranged from 0.16 to 0.33 mm, except for LM in healthy patients (0.86 to 0.88 mm). TrA and LM muscle thickness was measured bilaterally using the onscreen calipers. The side measured first was counterbalanced. The raters were not blind to group allocation. The raters who performed US and EMG recordings were blind to each other’s measurements.
US Measurement and sEMG of TrA TrA muscle was assessed in the supine hook-lying position with the US transducer placed transversely just above the iliac crest in the mid-axillary line.10 The participant was instructed to breathe normally. The ultrasonography image at rest was taken at the end of quiet inspiration.25,34 The US image in maximal contraction of TrA was captured when the participant followed the instruction to exhale and to draw the stomach in slowly as much as possible. The hypoechoic tissue of the muscle was measured only, and no hyperechoic fascial thickness was taken into account (Fig. 4). SEMG from the TrA was captured in the same position of the patient, first during voluntary expiration and then during maximal drawing in
FIGURE 2. Two pairs of the white circles in the lumbar region represent the position of the surface electrodes for acquisition of the electromyography signal from right and left lumbar multifidus muscle. Also the flexible goniometer with the Angle Display Unit for assessing the lumbosacral junction angle is shown.
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FIGURE 4. Examples of thickness measurements in transverse abdominal muscles from a pain-free participant during relaxation (right) and contraction (left). The vertical bar spans the boundary between the muscle and fascia (calibration 1 cm between each dot). The values for transversal abdominal are 7.5 mm (left) and 4.9 mm (right).
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of the front abdominal wall (ADIM) at the end of the selfchosen expiration.
US Measurements and sEMG of LM The LM muscle thickness was assessed in the prone position with the pillow placed under the abdomen to reduce lumbosacral junction angle to 0.05. BMI indicates body mass index; LBP, low back pain; ODS, Oswestry Disability Score; VAS, Visual Analog Scale.
TABLE 3. Group Mean ± SD Values for the Normalized Amplitude sEMG Signal of Transverse Abdominal (TrA) and Lateral Multifidus (LM) Muscles in Low Back Pain (LBP) and Painfree Participants
sEMG Side TrA* LM*
LBP
Pain-free
Normalized Signal Amplitude
Normalized Signal Amplitude
0.16 ± 0.19 0.15 ± 0.18 0.81 ± 0.18 0.81 ± 0.23
0.69 ± 0.38 0.54 ± 0.30 0.69 ± 0.31 0.71 ± 0.28
Right Left Right Left
*Significant effect of the group factor (Fb1, P < 0.05). LBP indicates low back pain; LM, lumbar multifidus muscle; TrA, transversal abdominal muscle.
RESULTS Age, body mass index, and distribution by sex are displayed in Table 1. The groups were age matched (P = 0.804). The LPB patients reported on average moderate levels of pain (5.25 ± 2.74) that lasted 3 to 6 months before the enrollment and caused moderate disability (28.75 ± 11.26) (Table 1). Twenty-seven of 36 LBP participants (75%) had radicular leg pain.
The Main Effects of the Group, Side, and Interaction Group¾Side (Tables 2 and 3) US (Table 2) TrA: The effect of group (F1,36 = 7.527, P = 0.009, Z2 = 0.84, large effect), sides (F3,108 = 144,47, P < 0.0001, Z2 = 0.32, large effect), and interaction between the 2 factors (F3,108 = 20.18, P < 0.0001, Z2 = 0.36, large effect) has been found to be significant for TrA thickness at rest and contraction. According to post hoc analysis (Turkey HSD), significant difference between groups was due to the thickness both at rest and contraction (Turkey HSD > 0.42) for each side. Also, each group reached significantly thicker TrA at contraction comparing to its thickness at rest (Turkey HSD > 0.78), whereas the thickness of the TrA both at rest and contraction was symmetrical within each group (Turkey HSD < 0.78). The relative change of the TrA was significantly different between LBP and non-LBP group (F1,142 = 60.69, P < 0.0001, Z2 = 0.3, large effect). No significant effect of the side (F1,142 = 1.2, P = 0.275, Z2 = 0.008, small effect), nor interaction between groupside (F1,142 = 0.24, P = 0.673, Z2 = 0.0016, small effect) was found (Table 2).
LM: No statistically significant effect of the group factor was found for the thickness of LM at rest and maximal contraction (F1,36 = 0.1635, P = 0.688, Z2 = 0.92, large effect). The effect of the side at rest and contraction was significant (F3,108 = 302.15, P < 0.0001, Z2 = 0.02, medium effect), and this was due to the significant difference between rest and contraction within each group (post hoc HSD > 2.3) on both sides. Interaction group side was significant (F3,108 = 6.6867 P = 0.000350, Z2 = 0.16, large effect). The effect of the group was found to be significant for the relative thickness change of the LM (F1,142 = 36.01, P < 0.0001, Z2 = 0.2, large effect), whereas the effect of the side and interaction groupside was not found to be significant (F1,142 = 0.34, P = 0.5608, Z2 = 0.002, small effect) (Table 2).
sEMG (Table 3) TrA: The normalized amplitudes of the sEMG for TrA were significantly different between the 2 groups (F1,142 = 31.05, P < 0.0001, Z2 = 0.18, large effect), whereas the effect of the side or interaction group side was not found to be significant (F1,142 = 1.05, P = 0.307, Z2 = 0.007 small effect; F1,142 = 0.8, P = 0.373, Z2 = 0.0007 small effect, respectively) (Table 3). LM: The normalized amplitudes of the sEMG for LM were significantly different between the 2 groups (F1,142 = 5.81, P = 0.0173, Z2 = 0.04, medium effect), whereas the effect of the side or interaction groupside was not found to be significant (F1,142 = 0.12, P = 0.7296, F1,142 = 0.12, P = 0.7296, respectively, Z2 = 810 4, small effect) (Table 3).
TABLE 2. Group Mean ± SD Values for the Thickness of Transverse Abdominal (TrA) and Lateral Multifidus (LM) Muscles at Rest (mm), During Contraction (mm), Maximal Contration (mm), and the Relative Thickness Change (Unitless) From Rest to Maximal Contraction in Low Back Pain (LBP) and Pain-free Participants Measured by Ultrasound
LBP Muscles Side
Rest (mm)
TrA*,** Right 4.3 ± 1.1 Left 4.3 ± 1.2 LM Right 27.0 ± 4.7 Left 28.2 ± 5.2
Contracted (mm)
Maximum Contracted (mm)
NA NA 34.2 ± 5.0 35.0 ± 6.9
6.6 ± 1.9 6.5 ± 2.2 35.7 ± 5.8 36.8 ± 6.6
Pain-free Change
Rest (mm)
0.6 ± 0.3 4.0 ± 1.0 0.5 ± 0.3 4.1 ± 1.3 0.3 ± 0.2* 26.9 ± 4.7 0.3 ± 0.2* 27.4 ± 5.6
Contracted (mm)
Maximum Contracted (mm)
Change
NA NA 35.1 ± 5.2 35.9 ± 6.2
8.4 ± 2.8 8.5 ± 3.0 37.9 ± 4.8 38.6 ± 5.4
1.1 ± 0.5 1.0 ± 0.5 0.4 ± 0.2* 0.4 ± 0.2*
*Significant effect of the group factor (Fb1, P < 0.05). **Significant effects of the group factor and significant interaction group side (Fb1, P < 0.05). LBP indicates low back pain; LM, lumbar multifidus muscle; TrA, transversal abdominal muscle.
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TABLE 4. Correlation Coefficient (r) Between Relative Thickness Change With sEMG Signal of the Corresponding Muscle During Relevant Clinical Activity, Displayed Along With 95% Confidence Interval (95% CI)
Correlation Coefficient r (95% CI) Muscles
Side
TrA
Right Left Right Left
LM
LBP 0.46* 0.63* 0.43* 0.16
(0.16-0.69) (0.38-0.79) (0.12-0.66) ( 0.18 to 0.46)
Pain-free 0.43* 0.47* 0.38* 0.36*
(0.12-0.66) (0.17-0.69) (0.06-0.63) (0.04-0.61)
*P < 0.05. CI indicates confidence interval; LBP, low back pain; LM, lumbar multifidus muscle; TrA, transversal abdominal muscle.
Correlation Between the Muscles’ Relative Thickness Change and the Amplitude of EMG Signal From the Corresponding Muscle (Table 4)
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studies.9,10,39,49 These findings are considered to demonstrate functional deficits of deep stabilizers of lumbosacral spine in chronic LBP.1,9
The Correlation Between US Measurements and sEMG Signal On the basis of the correlation results, we might assume that surface EMG and TrA thickness change assessed by US in both LBP and healthy patients can be used interchangeably, and more important, that the relative thickness of the muscle can be used as an indicator of muscle activity; this pertains for LM muscles in healthy participants, but the results for LM muscles in LBP group are not so conclusive. As stated earlier, numerous physical factors contribute to the relationship between EMG signal and muscle thickness change and the results of the correlation between the 2 must be viewed in a more complex context: (1) Muscular geometry changes during contraction are 3-dimensional. Although this would probably change in
LBP Patients (Fig. 7) Pearson coefficient of correlation between the relative thickness change of right TrA and the amplitude of sEMG signal from ipsilateral TrA was significant (r = 0.46, P = 0.005). The correlation between left TrA thickness and left TrA sEMG signal amplitude was also statistically significant (r = 0.63, P = 0.000038). Correlation coefficient between the sEMG amplitude signal and relative thickness change for right LM was found to be significant (r = 0.43, P = 0.009). We did not find significant correlation between relative thickness change and amplitude of the sEMG signal for left LM (r = 0.16 P = 0.351).
Pain-free Participants (Fig. 8) The significant Pearson correlation coefficient was found for LM and TrA on both sides, between the relative thickness change and the sEMG signal for the corresponding location: for right LM r = 0.38, P = 0.02; for left LM r = 0.36, P = 0.028; for right TrA r = 0.43, P = 0.0079; for left TrA r = 0.47, P = 0.0033). Correlation coefficients (r) for LBP and pain-free participants are displayed in Table 4, along with the corresponding 95% confidence interval of the r.
DISCUSSION The results of our study indicate that the relative thickness change of the TrA and LM are significantly smaller in LBP than healthy individuals in selected, clinically relevant activity. Relative thickness change of the TrA assessed by US correlated significantly with the sEMG signal from the anterior abdominal wall just inferomedial to the SIAS, on both sides for LBP and healthy participants during ADIM. The correlation between LM thickness change and correspondent sEMG signal was significant in pain-free participants for both sides, and for right LM in LBP participants. Left LM thickness change did not correlate with the normalized EMG signal amplitude during the selected task in the LBP group.
Difference Between the Relative Thickness Change of the TrA and LM The significantly smaller increase of the TrA and LM thickness during the contraction in LBP group comparing to pain-free individuals was also found in previous
FIGURE 7. Relationship between relative thickness change and surface electromyography (sEMG) of the corresponding muscle in low back pain (LBP) patients. LM indicates lumbar multifidus.
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Electromyographic Signal Amplitude and Thickness Change of the Trunk Muscles
FIGURE 8. Relationship between relative thickness change and surface electromyography (sEMG) of the corresponding muscle in healthy patients. LM indicates lumbar multifidus; TrA, transversal abdominal.
the near future, the images of the muscles have, so far, been assessed in 2-dimensional US, and as such does not provide full information on muscle thickness change. (2) Muscle activity is only one of the factors that influence the measured thickness of the muscle. The change in muscle length is influenced by the type of contraction, resting state of the muscle, external forces the muscle is competing against (compression by intra-abdominal pressure, surrounding muscle forces), extensibility, and the orientation of the muscle fibers.38 Conflicting findings of several studies that researched the relationship between EMG and US of abdominal wall muscles9,25,39–41,43 reflect not only methodological differences between them, but also not so easily controlled parallelism between EMG and US findings on these muscles thickness changes. Illustrative example of this complexity are findings in Whitakker et al,43 where 2 patients who, during the active straight leg test, demonstrated an increase in TrA EMG signal amplitude that was associated with either no change or a decrease in TrA thickness. The conclusions on the relationship between EMG and US become even more debatable if the EMG is done with surface electrode, with its major drawback in mind, cross-talk of the surrounding muscles. In contrast, surface EMG is user friendly, easily applicable in routine clinical and research practice for examining a larger sample of participants. As fine-wire EMG reflects the muscle activity of a small sample of muscle, and regional differences in TrA activity have been established during ADIM maneuver,35 sEMG may be more informative for estimating overall muscle Copyright
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activity. Fine-wire EMG studies of abdominal muscles activity showed that TrA is predominantly active during ADIM, whereas the rest of the abdominal muscles are minimally active or silent.35 Nevertheless, we can only assume that sEMG of anterior abdominal wall, from the point just medial to the ASIS, reflected predominantly TrA signal during voluntary expiration and ADIM. Comparison with the results of the other studies of the association between EMG recordings and thickness change for TrA is not so informative, due to the fact that the only 2 studies who investigated the relationship of surface EMG and abdominal wall muscle thickness did not measure TrA, but either OE40 or OE and OI.41 Different conclusion have been reached in the studies of that employed fine-wire EMG of the TrA: from poor correlation,43 across curvilinear association in narrow range of 0% to 20% of MVC,39 to strong linear relationship for TrA25 and TrA and OI.9 Although lying under OE and OI, TrA is predominantly active during ADIM, while the more superficial muscles are minimally involved.32–35 Thus, we may assume that TrA would dominantly contribute to the signal amplitude of the anterior abdominal wall muscle during ADIM, and we considered that research of the relationship between sEMG from the given location and TrA thickness change deserved attention. In our sample, significant correlation between TrA sEMG and thickness change in both LBP and healthy patients on both right and left side could be more grounded if we used ramped muscle contraction and this is one of the limitations of our study.
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The estimates of sensitivity of surface EMG sensors for LM are conflicting.27,50 Analyzing the correlation between surface and intramuscular EMG signal in 3 patients, Stokes et al27 suggested that the surface electrodes placed over multifidus muscles were more sensitive to activity in the adjacent longissimus than to activity in the underlying multifidus muscles. No detailed description of the position of the surface electrode for LM was provided. The report by Arokoski et al50 suggested that surface electrodes were sensitive to multifidus muscle activity. Although placed carefully according to SENIAM protocol for LM, we also cannot exclude that surface sensors were selective for LM only during back extension and contralateral arm lift. To our knowledge, no studies of the relationship between surface EMG signal and LM thickness change for both pain-free and LBP groups have been done so far. Kiesel et al30 found significant correlation between LM signal’s amplitude obtained by fine-wire EMG and thickness change assessed by US in 5 pain-free individuals in a range 19% to 34% of maximal voluntary isometric contraction. Significant correlation between LM EMG amplitude and its thickness change that we found in the pain-free individuals has to be considered with caution, as we used sEMG during the 2 levels of the LM contraction. The relationship between the 2 is less clear in LBP group, where the signal amplitude for left LM did not correlate with thickness change. Analyzing the data more closely, we identified 10 patients whose voluntary contraction of left LM had larger amplitude EMG signal than contraction against resistance of the examiner (which was supposed to be maximal contraction). This was also recorded in the pain-free group and in right LM sEMG measurements in the LBP group, but to a much lesser extent (only 2 of 37 pain-free individuals for right and left LM, and 4 of 36 in right LM sEMG). Analyzing the distribution of pain in the patients with unilateral presence of pain, 7 of these 10 patients who performed voluntary contraction of left LM stronger than the contraction against the resistance, had unilateral left back pain. Although expected to some degree (and frequently mentioned as a drawback of normalization procedures to MVCs), we feel that this rate (7 of 10) is rather high, and could be the reflection of the inability of these patients to perform MVC against resistance competently. For example, analyzing of the self-reported pain intensity VAS, we noticed that VAS in these unilateral left painful patients whose left LM sEMG signal during voluntary contraction was higher than in contraction against resistance, was 6.44, whereas in those unilateral left painful LBP patients whose voluntary contraction has a lower EMG amplitude than the contraction against the resistance, VAS was 4.10. Alternatively, we could perform another type of normalization procedure, but with considerable reservation for comparing EMG signals across patients.51–53 Relative thickness change of TrA and LM is different between LBP and non-LBP participants. It correlates with the sEMG amplitude, so relative thickness change can be, cautiously, viewed as an objective measure of the level of the muscle activation during contraction. Currently, we are unaware of the clinical relevance of the morphologic and functional deficits findings of our study. Objective assessment of the TrA and LM is lacking in clinical practice. These muscles are designated as the key stabilizing muscles of the lumbar spine. We do not know whether their morphologic and functional deficits, already
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described in LBP, are primary event or adaptive behavior regarding to pain occurrence. Introducing objective and simple method for estimation and monitoring these muscles’ function in healthy patients and in LBP during and after pain episodes in a longer period could be beneficial in better understanding the sequence of events (pain-changes in TrA and/or LM-resolution of pain-potential reversibility of the muscles changes). Clarifying of this etiopatologic conundrum could also implicate therapeutic strategies of certain forms of LBP, which are, currently insufficiently embedded in evidence-based practice.
Limitations of the Study (1) sEMG and US were not simultaneously recorded, but US measurements followed EMG recordings of the corresponding muscle. (2) No reliability study for sEMG recordings was conducted. (3) Muscle tasks comprised of only 2 levels of contraction for each muscle. Ramped contraction of LM and TrA would give a more detailed relationship between the thickness change and EMG amplitude. (4) No additional stratification according to key examination findings, aimed for subsequent interventions according to the treatment-based classification system, among LBP patients was performed. Also, all the patients were moderately disabled, so additional stratification according to the level of disability was not possible, either. (5) Cross-talk cannot be excluded with surface EMG.
CONCLUSIONS The relative thickness change of TrA and LM, assessed on US, are significantly smaller in LBP than painfree individuals in selected, clinically relevant activity. We found significant correlations between relative thickness change of the TrA and sEMG signal amplitude on both sides, for LBP and healthy patients. The correlation between LM thickness change and sEMG signal was significant in pain-free individuals for both the sides, and for right LM in LBP participants. Left LM thickness change did not correlate with the sEMG signal amplitude during selected tasks in LBP group. REFERENCES 1. Wong AY, Parent EC, Funabashi M, et al. Do various baseline characteristics of transversus abdominis and lumbar multifidus predict clinical outcomes in nonspecific low back pain? A systematic review. Pain. 2013;154:2589–2602. 2. Wallwork TL, Stanton WR, Freke M, et al. The effect of chronic low back pain on size and contraction of the lumbar multifidus muscle. Man Ther. 2009;14:496–500. 3. Hides JA, Stokes MJ, Saide M, et al. Evidence of lumbar multifidus muscle wasting ipsilateral to symptoms in patients with acute/subacute low back pain. Spine (Phila Pa 1976). 1994;19:16572. 4. Danneels LA, Vanderstraeten GG, Cambier DC, et al. CT imaging of trunk muscles in chronic low back pain patients and healthy control subjects. Eur Spine J. 2000;9:266–272. 5. Hyun JK, Lee JY, Lee SJ, et al. Asymmetric atrophy of multifidus muscle in patients with unilateral lumbosacral radiculopathy. Spine (Phila Pa 1976). 2007;32:E598–E602. 6. Campbell WW, Vasconcelos O, Laine FJ. Focal atrophy of the multifidus muscle in lumbosacral radiculopathy. Muscle Nerve. 1998;21:1350–1353.
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