American Journal of Emergency Medicine xxx (2013) xxx–xxx
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American Journal of Emergency Medicine journal homepage: www.elsevier.com/locate/ajem
Original Contribution
Electromyography activity of selected trunk muscles during cardiopulmonary resuscitation☆ Jui-Yi Tsou, PT, PHD a, Fong-Chin Su, PHD b, c,⁎, Pai-Chin Tsao, PT, MS b, Ming-Yuan Hong, MD d, Su-Chun Cheng, PT, PHD a, Hsun-Wen Chang, PT, PHD a, Jin-Shiou Yang, PT, MS a, Chih-Hsien Chi, MD d,⁎ a
Department of Physical Therapy, Fooyin University, Kaohsiung, Taiwan Department of Biomedical Engineering, National Cheng Kung University, Tainan, Taiwan Medical Device Innovation Center, National Cheng Kung University, Tainan, Taiwan d Department of Emergency Medicine, National Cheng Kung University, Tainan, Taiwan b c
a r t i c l e
i n f o
Article history: Received 25 August 2013 Received in revised form 21 October 2013 Accepted 21 October 2013 Available online xxxx
a b s t r a c t Background: Understanding trunk muscle activity during chest compression may improve cardiopulmonary resuscitation (CPR) training strategies of CPR or prevent low back pain. This study investigates the trunk muscle activity pattern of chest compression in health care providers to determine the pattern alternation during chest compression. Methods: Thirty-one experienced health care providers performed CPR for 5 minutes at a frequency of 100 compressions per minute. An electromyography (EMG) system was used to record muscle activity in the first minute, the third minute, and the fifth minute. Electrodes were placed bilaterally over the pectoralis major, latissimus dorsi, rectus abdominis, erector spinae, and gluteus maximus. We calculated the root mean square (RMS) value and maximal amplitude of the EMG activity, median frequency, and delivered force. Results: The maximal amplitude of EMG of the pectoralis major, erector spinae, and rectus abdominis showed large muscle activity above 45% of maximal voluntary contraction under chest compression. There were no significant differences in the RMS value of one chest compression cycle (RMS100%) and median frequency for all muscles at the first, third, and fifth minutes. Only gluteus maximus showed significant imbalance. The EMG ratios (erector spinae/rectus abdominis; erector spinae/gluteus maximus) increased significantly over time. The delivered force, compression depth, and number of correct depth decreased significantly over time. Conclusion: We suggest that the muscle power training for the pectoralis major, erector spinae, and rectus abdominis could be helpful for health care providers. Keeping muscle activity balance of bilateral gluteus maximus and maintaining the same level of EMG ratios might be the keys to prevent low back pain while performing CPR. © 2013 Elsevier Inc. All rights reserved.
1. Introduction Low back pain (LBP) is frequent among hospital staff personnel [1]. Previous studies have shown that more than 80% of nurses and 96% of ambulance officers experience back discomfort that is highly associated with the delivery of cardiopulmonary resuscitation (CPR) [2,3]. A study in Taiwan suggested that 58.1% of ambulance personnel suffered from back pain after performing CPR. Of this group, 15.7% were absent from work, 40.4% required bed rest, 44.3% took medication to relieve pain, and 68.7% felt that their LBP was related ☆ Conflict of interest statement: none. ⁎ Corresponding authors. Fong-Chin Su is to be contacted at Department of Biomedical Engineering, National Cheng Kung University, Tainan 70401, Taiwan. Tel.: +886 6 2760665; fax: +886 6 2343270. Chih-Hsien Chi, Department of Emergency Medicine, National Cheng Kung University, Tainan 70403, Taiwan. Tel.: +886 6 2766120; fax: +886 6 2359562. E-mail addresses: [email protected] (F.-C. Su), [email protected] (C.-H. Chi).
to CPR [4]. Chest compression is a repetitive and strenuous movement. The mechanical loading of the lower back during chest compression might be an important factor inducing LBP [5]. Trunk muscle activity pattern can influence the mechanical loading of the lower back [6]. Therapeutic exercise is a widely used treatment strategy for LBP. Therapeutic exercise includes various types of interventions, ranging from general physical fitness or aerobic exercise to muscle strengthening and stretching exercises [7]. Therapeutic exercise is based on the mechanisms of controlling muscle activation for specific movement. The surface electromyography (EMG) method provides an easy way to assess the mechanisms causing muscles to generate force and produce movement [8,9]. Understanding trunk muscle activity during chest compression might improve the effectiveness of therapeutic exercise for the management or prevention of LBP in health care providers. However, relatively few studies have discussed trunk muscle activity during CPR. This study investigates the trunk muscle activity patterns of health care providers to identify the pattern alternation at
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Please cite this article as: Tsou J-Y, et al, Electromyography activity of selected trunk muscles during cardiopulmonary resuscitation, Am J Emerg Med (2013), http://dx.doi.org/10.1016/j.ajem.2013.10.044
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various time intervals during chest compression. The results of this study could be useful to health care providers responsible for performing CPR. 2. Experimental design and methods 2.1. Participants We recruited the participants from 2 medical centers and 1 emergency medical service in southern Taiwan. Eligibility criteria were as follows: health care providers working in the emergency department, intensive care unit, or emergency medical service; CPR experience more than 1 year; and no musculoskeletal pain during the past 3 months. Thirty-one participants comprising 4 physicians, 6 nurses, and 19 emergency medical technician firefighters (6 women, 25 men, age: 30 ± 5.3 years, height: 166.0 ± 5.8 cm, weight: 66 ± 11.2 kg, CPR experience: 4.3 ± 3.5 years) were recruited. The institutional review board of National Cheng Kung University Hospital approved this observational study, and each participant provided written informed consent. 2.2. Instrumentation We used a 10-channel MA-300 EMG system (Motion Lab Systems, Baton Rouge, LA) with bipolar Ag/AgCl surface electrodes to record muscle activity at a 1000-Hz sampling rate. A 6-axis load cell (AMTI MC3A-6-1000, Advanced Mechanical Technology, Inc, Watertown, MA) attached to a standard Resusci Anne manikin (Laerdal Medical, Wappingers Falls, NY) was used to record the delivered force at a sampling frequency of 1000 Hz. The EMG and applied force measured by the load cell were synchronized using an external trigger. 2.3. Procedure The study was undertaken at the motion analysis laboratory in the department of biomedical engineering. For electrode attachment, the skin was cleaned with an alcohol pad; and EMG electrodes were placed bilaterally over the muscle belly in the direction parallel to the muscle fibers. We collected EMG data from 5 pairs of trunk muscles: the pectoralis major (PMr, PMl), latissimus dorsi (LDr, LDl), rectus abdominis (RAr, RAl, 3 cm lateral to the umbilicus), erector spinae (ESr, ESl, 3 cm lateral to the L3 spinous process), and gluteus maximus (GMr, GMl, middle third of the muscle belly). Before testing, we recorded the maximum voluntary isometric contraction (MVC) of the muscles for an EMG normalization procedure [10]. Each MVC was held for 5 seconds, and the best 1second mean value was recorded. Prior to testing, the participants performed 30 seconds of CPR for familiarization warmup and practiced the CPR task using audio cues and visual feedback by the SkillGuide device(Laerdal Medical), which provided immediate objective feedback on compression depth and hand position before data were recorded. Five-minute resting was between the practice and formal testing. The participants knelt beside the manikin and performed standard CPR for 5 minutes at a 30/2 compressionventilation ratio and frequency of 100 compressions per minute without the SkillGuide device. Three 10-second data samples of EMG were recorded at the end of the first, third, and fifth minutes. Participants completed at least 12 chest compression cycles. 2.4. Data processing The EMG data were full-wave rectified, filtered (second-order Butterworth filter with 0.5- to 400-Hz passband and 60-Hz notch filter), and normalized by MVC [11]. The delivered force from the load cell data was smoothed forward and backward using a second-order
Butterworth filter with a 4-Hz cutoff frequency before being used for parameter calculations. We calculated the root mean square (RMS) value and maximal amplitude of EMG activity, median frequency (MF), the EMG ratio (erector spinae/rectus abdominis [ES/RA]; erector spinae/gluteus maximus [ES/GM]), delivered force, compression depth, number of correct depth in percentage of total compression number, and compression rate. We averaged the data from at least 12 chest compression cycles, defined from the minimal delivered force to next minimal delivered force. We also calculated the RMS value of 1 chest compression cycle (RMS100%), 50% of the cycle (RMS50%), and 20% of the cycle (RMS20%). We applied spectral analysis (Hanning window processing and 1024-point fast Fourier transform) to each time window (a series of 45% of the compression cycle of EMG data with 50% overlapping) to obtain the MF value [12]. 2.5. Statistical analysis We used descriptive statistics to calculate all outcome variables. We also applied repeated-measures analysis of variance to the mean of the delivered force, compression depth, number of correct depth, compression rate, RMS100%, MF, and RMS20% data within participants to compare the time effect. We applied the Bonferroni adjustment a priori to pairwise comparisons and used Scheffé post hoc analysis to identify differences in analysis of variance if the main effect was significant. We used a paired t test to compare the RMS50% differences within participants. The significance level of this study was set at P b .05. All parameters were statistically analyzed using SPSS 19 software for Windows (SPSS Inc, Chicago, IL). 3. Results Table 1 shows the maximal amplitude of EMG for 10 muscles during chest compression. The pectoralis major, ES, and RA exhibited the greatest muscle activity of all muscles during chest compression, whereas the latissimus dorsi and gluteus maximus exhibited the least muscle activity. Fig. 1 shows the RMS50% of EMG for 10 muscle groups. The RMS50% of the push-down phase is significantly larger than that of the release phase for PMr, PMl, LDr, RAr, RAl, ESr, ESl, GMr, and GMl. A comparison of these results with the contralateral muscle in RMS50% shows no significant differences between most bilateral muscles. Only the RMS50% of GMl is significantly greater than that of GMr in the release phase (P = .02). An RMS50% discrepancy of 40% appeared. Fig. 2 shows the RMS20% of EMG for 10 muscles. The total compression cycle of each muscle consists of 5 phases. Each phase accounts for 20% of the compression cycle (RMS20%). The RMS20% varies significantly among the 5 phases of the same muscle for all muscles, except the bilateral latissimus dorsi. The results of post hoc Table 1 The mean and standard deviation of the maximal amplitude of EMG Muscle
Right/left
Pectoris major
R L R L R L R L R L
Latissimus dorsi Rectus abdominis Erector spinae Gluteus maximus
Maximal amplitude of EMG in percentage of MCV Mean
SD
56% 59% 31% 32% 49% 45% 56% 52% 24% 34%
20% 15% 20% 23% 21% 22% 15% 21% 15% 21%
R means right side, and L means left side.
Please cite this article as: Tsou J-Y, et al, Electromyography activity of selected trunk muscles during cardiopulmonary resuscitation, Am J Emerg Med (2013), http://dx.doi.org/10.1016/j.ajem.2013.10.044
J.-Y. Tsou et al. / American Journal of Emergency Medicine xxx (2013) xxx–xxx
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*
Push-down Release
*
P < .001 P < .001
Table 2 The results of post hoc test between the phase of maximal RMS20% and others P value Right/ The left phase Phase 1 Phase 2 Phase 3 Phase 4 Phase 5 of max. RMS20%
Muscle
%MVC
*
*
20
*
*
*
*
*
P = .008 P = .192 P < .001 P < .001 P < .001 P < .001 P = .019 P = .004
15
Pectoris major
R L Rectus abdominis R L Erector spinae R L Gluteus maximus R L
10 5 0 PMr PMl
LDr
LDl
RAr
RAl
ESr
3
Phase 2 Phase 2 Phase 2 Phase 2 Phase 4 Phase 4 Phase 4 Phase 4
.000 * .000 * .012 * .002 * .000 * .000 * .040 * .042 *
– – – – .000 .000 .019 .039
* * * *
.681 .007 * .012 * .001 * 1.000 1.000 1.000 1.000
.006 .000 .001 .000 – – – –
* * * *
.000 * .000 * .001 * .000 * .000 * .000 * .067 .024 *
ESl GMr GMl
Muscle Fig. 1. The average RMS50% of EMG for 10 muscles during a chest compression cycle. *Significant differences between push-down phase and release phase in the same muscle. Error bars denote standard deviation.
test were shown in Table 2 to identify differences between the phase of maximal RMS20% and others if the main effect was significant. During a chest compression cycle, the maximal RMS20% of PMr, PMl, RAr, and RAl occurs during Phase 2. The maximal RMS20% of ESr, ESl, GMr, and GMl occurs during Phase 4. A comparison of bilateral muscle activity in RMS20% shows that bilateral muscles exhibit similar muscle recruitment patterns. There is no significant difference between bilateral muscles in the same phase except for Phase 1 of bilateral GM (P = .028). Figs. 3 and 4, respectively, show the average RMS100% of EMG and the MF of EMG in the first, third, and fifth minutes. These figures show no significant differences in RMS100% and MF for all muscles. A comparison of these results with the contralateral muscle in RMS100% during the same periods shows no significant differences between bilateral muscles. Table 3 shows the average maximal delivered force, compression depth, number of correct depth, compression rate, and EMG ratio in the first, third, and fifth minutes. The delivered force, compression depth, and number of correct depth during these 3 periods decreased significantly over time. The EMG ratios (ES/RA and ES/GM) increased significantly over time. The compression rate had no significant difference in the 3 periods. 4. Discussion This study presents the trunk EMG patterns of the healthy and experienced health care providers. The maximal EMG amplitude of Phase1 Phase2 Phase3 Phase4 Phase5
*
*
*
RMS (% MVC)
* 20 P = .171 P = .415
* *
15
*
10
1st min 3rd min 5th min
20 18 16
RMS (% MVC)
* 25
the pectoralis major, ES, and RA exhibited muscle activity exceeding 45% of the maximal voluntary contraction during chest compression. The pectoralis major, RA, and latissimus dorsi exhibited higher muscle activity during the push-down phase, whereas the ES and GM exhibited greater activation during the release phase. Muscle activity was categorized during the exercise as minimal (0%-20% MVC), moderate (21%-50% MVC), or high (N50% MVC) [13,14]. According to these categories, the bilateral pectoralis major and ES generated high muscle effort; and the bilateral RA, latissimus dorsi, and GM produced moderate intensity of muscle activity during a compression cycle. Although the RA activity was categorized as moderate, it was near the border of the high level. Therefore, muscle training programs designed for CPR professionals should include muscle power training for the pectoralis major, ES, and RA. Ideally, the duration of the push-down (compression) phase should be equivalent to the duration of the release (decompression) phase [5]. The pectoralis major, RA, and latissimus dorsi had higher muscle activity during the push-down phase, especially during Phase 2. These results indicate that these muscles generate the push-down force. During the release phase, the ES and GM, which lift the trunk to the starting position of compression, exhibit more obvious RMS to produce hip extension and trunk extension. In addition to the agonist function, the muscles also play a synergistic or antagonistic role in co-contraction with the agonist muscle. The strengthening of core muscles is often involved in the rehabilitation of LBP. The core muscles can be described as a muscular box with the abdominals in the front, paraspinals and gluteals in the back, the diaphragm as the roof, and the pelvic floor and hip girdle musculature as the bottom [15]. The core muscles works synergistically to provide a proper force distribution and maximal force
14 12 10 8 6 4
5
2
0
0 PMr PMl LDr
LDl
RAr RAl ESr
ESl GMr GMl
Muscle Fig. 2. The average RMS20% of EMG for 10 muscles during a chest compression cycle. Error bars denote standard deviation. *P b .000.
PMr PMl LDr LDl RAr RAl ESr ESl GMr GMl
Muscle Fig. 3. The average RMS100% of EMG in the first, third, and fifth minutes. Error bars denote standard deviation.
Please cite this article as: Tsou J-Y, et al, Electromyography activity of selected trunk muscles during cardiopulmonary resuscitation, Am J Emerg Med (2013), http://dx.doi.org/10.1016/j.ajem.2013.10.044
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1st min 3rd min 5th min
180
Median Frequency (Hz)
160 140 120 100 80 60 40 20 0 PMr PMl LDr LDl RAr RAl ESr ESl GMr GMl
Muscle Fig. 4. The MF of EMG in the first, third, and fifth minutes. Error bars denote standard deviation.
generation with minimal compressive or shearing forces at the spine [16]. Core muscles also provide proximal stability for distal movement [17]. During compression, the RA and ES co-contract to stabilize the pelvis and lumbar spine against the pull of the iliopsoas muscle during active hip flexion (push-down phase) to avoid increased lumbar lordosis and anterior shearing of the vertebrae. The bilateral RA, ES, pectoralis major, and latissimus dorsi synergistically stabilize the rib cage and shoulder girdle to transfer the pushing force to the upper extremity. We used EMG ratios (ES/RA and ES/GM) to present the synergistic features of core muscle [18]. Research used this ratio to compare the trunk muscle recruitment patterns in LBP patients with the healthy participants during trunk flexion-extension [19]. They found that the ratio of antagonist over agonist of lumbar EMG amplitude was greater in the patients. During compression, ES is an antigonist muscle and RA is an agonist muscle. Our results show that ES/RA ratio increased significantly over time. These means that the relationship of ES and RA muscle activity is more and more similar to the LBP participants' with increasing operating time. The ES and GM are synergistic muscles coworking for trunk lifting. The ES/GM ratio also increased significantly over time. The GM muscles are more fatigable in chronic LBP [20]. The increasing of EMG ratios (ES/RA and ES/GM) might lead to increase lumbar mobility and decrease hip mobility, which would increase lumbar loading and decrease delivered force. Muscle training should be focused on keeping EMG ratios at the same level with increasing operation time. Surface EMG has been used to understand the function of trunk muscles in both healthy controls and LBP patients during specific postures and movements [9,21,22]. Contralateral muscle balance has been one issue of surface EMG. The EMG contralateral imbalances of trunk muscles are often related to back pain [22,23]. Chest compression is a relatively symmetric movement for the bilateral Table 3 The mean and standard deviation of the EMG ratio, the maximal delivered force, compression depth, number of correct depth, and compression rate in the first, third, and fifth minutes Measurement
1st min Mean
3rd min SD
Mean
5th min SD
Mean
P value SD
ES/RA ratio 0.99 0.11 1.02 0.06 1.06 0.07 ES/GM ratio 1.38 0.25 1.42 0.26 1.44 0.28 Delivered force (N) 470.6 55.5 461.0 60.2 446.6 64.0 Compression 53.3 2.6 51.9 3.4 50.2 4.5 depth (mm) No. of correct depth (%) 97.7 9.0 93.9 13.2 91.2 17.2
.047 .032 .001 .000 .019
trunk and extremities. The results of this study show that EMG activity is balanced for almost all selected muscles except the GM. Oddsson and De Luca [9] recorded bilateral paraspinal EMG activity in healthy men and chronic LBP patients. They found that the contralateral RMS amplitude in healthy controls was more symmetric than that in chronic LBP patients. This finding supports the current results regarding the symmetric EMG activity of chest compression in healthy participants. Previous studies found that the muscle imbalance of GM was associated with LBP occurrence in female athletes [24-26]. The GM muscle activity during the flexion-extension cycle was lower in patients with chronic LBP than in healthy participants [27]. Imbalance of GM might be a feature developing LBP while performing CPR. The relationship between imbalance of GM and LBP needs further examination. The power spectrum of the frequency domain of the surface EMG represents a summary of all the spectrum contributions of the active motor unit action potentials recorded by the EMG sensor. Shifts in the power spectrum often serve as indicators of muscle fatigue [28,29]. The MF is the most commonly used index of power spectral alterations to detect muscle fatigue [30]. The RMS and MF showed no significant differences over time; this means that the selective muscles might not experience fatigue. The overall delivered force, compression depth, and the percentage of number of correct depth decreased significantly over time. It indicates that the neuroelectrical activity (the motor output from the cortex and motor unit recruitment, detected by RMS and MF) did not change and the overall muscle contraction force (detected by delivered force) decreased. These suggest that overall muscle efficiency decreases. A previous study also reported that the relationship between dynamic contractions instantaneous MF and muscle fatigue is nonlinear and more complex during repetitive lifting [31]. They hypothesized that a complex strategy using muscle loadsharing provides periods of metabolic recovery to limit localized fatigue during strenuous dynamic exercise [31]. Researches evidenced that the depth or force of chest compression decays after 1 to 2 minutes of CPR [32-35]. These results are consistent with our finding that the compression depth and delivered force declined over time. Thus, we agree with the suggestion of the 2010 American Heart Association Guidelines: “When 2 or more rescuers are available it is reasonable to switch chest compressors approximately every 2 minutes to prevent decreases in the quality of compressions” [36]. However, the depth of compression decreased only 3.1 mm on average in the 5 minutes; and average depth was 50.2 mm above 5 cm according to the 2010 CPR guideline. A total of 91.2% of the compressions were still of the correct depth. Compression rate did not decrease significantly, and trunk muscle did not exhibit significant fatigue within 5 minutes. These indicates that the healthy and experienced rescuer performing CPR within 3 to 5 minutes still has acceptable CPR quality and low risk of LBP. The first limitation of this study is that it does not include the iliopsoas muscle. The iliopsoas may interfere with or distort the recording of surface EMG because it is a deep muscle, and chest compression has larger hip flexion movement. From a biomechanical view, keeping the lumbar spine straight and acting from the hip joint as the axis are the best strategies to reduce lumbar loading and reduce energy consumption. The iliopsoas muscle is a major agonist muscle for hip flexion. It may be an important muscle of the trunk for chest compression. The second limitation of this study is that upperextremity muscles also play an important role in chest compression, but this is beyond the scope of this study. Further research should focus on the analysis of upper-extremity muscles. 5. Conclusion This study presents a clear picture of the muscle activity and function of the trunk during chest compression in healthy experienced participants. The pectoralis major, ES, and RA generated larger
Please cite this article as: Tsou J-Y, et al, Electromyography activity of selected trunk muscles during cardiopulmonary resuscitation, Am J Emerg Med (2013), http://dx.doi.org/10.1016/j.ajem.2013.10.044
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muscle activity above 45% of MVC during chest compression. It indicated that designing muscle training programs for CPR professionals should emphasize muscle power training for the pectoralis major, ES, and RA. The results of this study indicate that the efficiency of the trunk muscle decreases over time during chest compression, but the healthy and experienced rescuer performing CPR within 3 to 5 minutes still has acceptable CPR quality and low risk of LBP. The GM showed imbalanced muscle activity, and the EMG ratios (ES/RA and ES/GM) increased over time. Thus, keeping bilateral GM balance and maintaining the same level of EMG ratios might be the keys to prevent LBP while performing CPR. Further researches should compare the alternated muscle recruitment pattern in the LBP patient with our findings. Acknowledgments The authors gratefully acknowledge the financial support of the National Science Council, Taiwan, ROC (grant no. NSC 98-2320-B-006001). Prof Soong-Yu Kuo is gratefully acknowledged for his suggestions. References [1] Bejia I, Younes M, Jamila HB, Khalfallah T, Ben Salem K, Touzi M, et al. Prevalence and factors associated to low back pain among hospital staff. Joint Bone Spine 2005;72(3):254–9. [2] Jones AY, Lee RY. Cardiopulmonary resuscitation and back injury in ambulance officers. Int Arch Occup Environ Health 2005;78(4):332–6. [3] Jones AY. Can cardiopulmonary resuscitation injure the back? Resuscitation 2004;61(1):63–7. [4] Hu KW, Guo HR, Lee HL, Lin HJ, Liao CK, Chen KT, et al. Cardiopulmonary resuscitation and back pain among emergency medical technicians. J Emerg Crit Care Med 2008;19(3):93–101. [5] Tsou JY, Chi CH, Hsu RM, Wu HF, Su FC. Mechanical loading of the low back during cardiopulmonary resuscitation. Resuscitation 2009;80(10):1181–6. [6] Takahashi I, Kikuchi S, Sato K, Sato N. Mechanical load of the lumbar spine during forward bending motion of the trunk—a biomechanical study. Spine (Phila Pa 1976) 2006;31(1):18–23. [7] Hayden JA, van Tulder MW, Malmivaara A, Koes BW. Exercise therapy for treatment of non-specific low back pain. Cochrane Database Syst Rev 2005;3(20): CD000335. [8] De Luca CJ. Use of the surface EMG signal for performance evaluation of back muscles. Muscle Nerve 1993;16(2):210–6. [9] Oddsson LI, De Luca CJ. Activation imbalances in lumbar spine muscles in the presence of chronic low back pain. J Appl Physiol 2003;94(4):1410–20. [10] Kendall FP, McCreary EK, Provance PG. Muscles: testing and function. 4th ed. Lippincott Williams & Wilkins; 1999. [11] Clancy EA, Morin EL, Merletti R. Sampling, noise-reduction and amplitude estimation issues in surface electromyography. J Electromyogr Kinesiol 2002;12(1):1–16. [12] Lariviere C, Arsenault AB, Gravel D, Gagnon D, Loisel P. Surface electromyography assessment of back muscle intrinsic properties. J Electromyogr Kinesiol 2003;13(4):305–18. [13] McCann PD, Wootten ME, Kadaba MP, Bigliani LU. A kinematic and electromyographic study of shoulder rehabilitation exercises. Clin Orthop Relat Res 1993;288:179–88. [14] Decker MJ, Hintermeister RA, Faber KJ, Hawkins RJ. Serratus anterior muscle activity during selected rehabilitation exercises. Am J Sports Med 1999;27(6): 784–91.
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Contents lists available at ScienceDirect
American Journal of Emergency Medicine journal homepage: www.elsevier.com/locate/ajem
Original Contribution
Electromyography activity of selected trunk muscles during cardiopulmonary resuscitation☆ Jui-Yi Tsou, PT, PHD a, Fong-Chin Su, PHD b, c,⁎, Pai-Chin Tsao, PT, MS b, Ming-Yuan Hong, MD d, Su-Chun Cheng, PT, PHD a, Hsun-Wen Chang, PT, PHD a, Jin-Shiou Yang, PT, MS a, Chih-Hsien Chi, MD d,⁎ a
Department of Physical Therapy, Fooyin University, Kaohsiung, Taiwan Department of Biomedical Engineering, National Cheng Kung University, Tainan, Taiwan Medical Device Innovation Center, National Cheng Kung University, Tainan, Taiwan d Department of Emergency Medicine, National Cheng Kung University, Tainan, Taiwan b c
a r t i c l e
i n f o
Article history: Received 25 August 2013 Received in revised form 21 October 2013 Accepted 21 October 2013 Available online xxxx
a b s t r a c t Background: Understanding trunk muscle activity during chest compression may improve cardiopulmonary resuscitation (CPR) training strategies of CPR or prevent low back pain. This study investigates the trunk muscle activity pattern of chest compression in health care providers to determine the pattern alternation during chest compression. Methods: Thirty-one experienced health care providers performed CPR for 5 minutes at a frequency of 100 compressions per minute. An electromyography (EMG) system was used to record muscle activity in the first minute, the third minute, and the fifth minute. Electrodes were placed bilaterally over the pectoralis major, latissimus dorsi, rectus abdominis, erector spinae, and gluteus maximus. We calculated the root mean square (RMS) value and maximal amplitude of the EMG activity, median frequency, and delivered force. Results: The maximal amplitude of EMG of the pectoralis major, erector spinae, and rectus abdominis showed large muscle activity above 45% of maximal voluntary contraction under chest compression. There were no significant differences in the RMS value of one chest compression cycle (RMS100%) and median frequency for all muscles at the first, third, and fifth minutes. Only gluteus maximus showed significant imbalance. The EMG ratios (erector spinae/rectus abdominis; erector spinae/gluteus maximus) increased significantly over time. The delivered force, compression depth, and number of correct depth decreased significantly over time. Conclusion: We suggest that the muscle power training for the pectoralis major, erector spinae, and rectus abdominis could be helpful for health care providers. Keeping muscle activity balance of bilateral gluteus maximus and maintaining the same level of EMG ratios might be the keys to prevent low back pain while performing CPR. © 2013 Elsevier Inc. All rights reserved.
1. Introduction Low back pain (LBP) is frequent among hospital staff personnel [1]. Previous studies have shown that more than 80% of nurses and 96% of ambulance officers experience back discomfort that is highly associated with the delivery of cardiopulmonary resuscitation (CPR) [2,3]. A study in Taiwan suggested that 58.1% of ambulance personnel suffered from back pain after performing CPR. Of this group, 15.7% were absent from work, 40.4% required bed rest, 44.3% took medication to relieve pain, and 68.7% felt that their LBP was related ☆ Conflict of interest statement: none. ⁎ Corresponding authors. Fong-Chin Su is to be contacted at Department of Biomedical Engineering, National Cheng Kung University, Tainan 70401, Taiwan. Tel.: +886 6 2760665; fax: +886 6 2343270. Chih-Hsien Chi, Department of Emergency Medicine, National Cheng Kung University, Tainan 70403, Taiwan. Tel.: +886 6 2766120; fax: +886 6 2359562. E-mail addresses: [email protected] (F.-C. Su), [email protected] (C.-H. Chi).
to CPR [4]. Chest compression is a repetitive and strenuous movement. The mechanical loading of the lower back during chest compression might be an important factor inducing LBP [5]. Trunk muscle activity pattern can influence the mechanical loading of the lower back [6]. Therapeutic exercise is a widely used treatment strategy for LBP. Therapeutic exercise includes various types of interventions, ranging from general physical fitness or aerobic exercise to muscle strengthening and stretching exercises [7]. Therapeutic exercise is based on the mechanisms of controlling muscle activation for specific movement. The surface electromyography (EMG) method provides an easy way to assess the mechanisms causing muscles to generate force and produce movement [8,9]. Understanding trunk muscle activity during chest compression might improve the effectiveness of therapeutic exercise for the management or prevention of LBP in health care providers. However, relatively few studies have discussed trunk muscle activity during CPR. This study investigates the trunk muscle activity patterns of health care providers to identify the pattern alternation at
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Please cite this article as: Tsou J-Y, et al, Electromyography activity of selected trunk muscles during cardiopulmonary resuscitation, Am J Emerg Med (2013), http://dx.doi.org/10.1016/j.ajem.2013.10.044
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various time intervals during chest compression. The results of this study could be useful to health care providers responsible for performing CPR. 2. Experimental design and methods 2.1. Participants We recruited the participants from 2 medical centers and 1 emergency medical service in southern Taiwan. Eligibility criteria were as follows: health care providers working in the emergency department, intensive care unit, or emergency medical service; CPR experience more than 1 year; and no musculoskeletal pain during the past 3 months. Thirty-one participants comprising 4 physicians, 6 nurses, and 19 emergency medical technician firefighters (6 women, 25 men, age: 30 ± 5.3 years, height: 166.0 ± 5.8 cm, weight: 66 ± 11.2 kg, CPR experience: 4.3 ± 3.5 years) were recruited. The institutional review board of National Cheng Kung University Hospital approved this observational study, and each participant provided written informed consent. 2.2. Instrumentation We used a 10-channel MA-300 EMG system (Motion Lab Systems, Baton Rouge, LA) with bipolar Ag/AgCl surface electrodes to record muscle activity at a 1000-Hz sampling rate. A 6-axis load cell (AMTI MC3A-6-1000, Advanced Mechanical Technology, Inc, Watertown, MA) attached to a standard Resusci Anne manikin (Laerdal Medical, Wappingers Falls, NY) was used to record the delivered force at a sampling frequency of 1000 Hz. The EMG and applied force measured by the load cell were synchronized using an external trigger. 2.3. Procedure The study was undertaken at the motion analysis laboratory in the department of biomedical engineering. For electrode attachment, the skin was cleaned with an alcohol pad; and EMG electrodes were placed bilaterally over the muscle belly in the direction parallel to the muscle fibers. We collected EMG data from 5 pairs of trunk muscles: the pectoralis major (PMr, PMl), latissimus dorsi (LDr, LDl), rectus abdominis (RAr, RAl, 3 cm lateral to the umbilicus), erector spinae (ESr, ESl, 3 cm lateral to the L3 spinous process), and gluteus maximus (GMr, GMl, middle third of the muscle belly). Before testing, we recorded the maximum voluntary isometric contraction (MVC) of the muscles for an EMG normalization procedure [10]. Each MVC was held for 5 seconds, and the best 1second mean value was recorded. Prior to testing, the participants performed 30 seconds of CPR for familiarization warmup and practiced the CPR task using audio cues and visual feedback by the SkillGuide device(Laerdal Medical), which provided immediate objective feedback on compression depth and hand position before data were recorded. Five-minute resting was between the practice and formal testing. The participants knelt beside the manikin and performed standard CPR for 5 minutes at a 30/2 compressionventilation ratio and frequency of 100 compressions per minute without the SkillGuide device. Three 10-second data samples of EMG were recorded at the end of the first, third, and fifth minutes. Participants completed at least 12 chest compression cycles. 2.4. Data processing The EMG data were full-wave rectified, filtered (second-order Butterworth filter with 0.5- to 400-Hz passband and 60-Hz notch filter), and normalized by MVC [11]. The delivered force from the load cell data was smoothed forward and backward using a second-order
Butterworth filter with a 4-Hz cutoff frequency before being used for parameter calculations. We calculated the root mean square (RMS) value and maximal amplitude of EMG activity, median frequency (MF), the EMG ratio (erector spinae/rectus abdominis [ES/RA]; erector spinae/gluteus maximus [ES/GM]), delivered force, compression depth, number of correct depth in percentage of total compression number, and compression rate. We averaged the data from at least 12 chest compression cycles, defined from the minimal delivered force to next minimal delivered force. We also calculated the RMS value of 1 chest compression cycle (RMS100%), 50% of the cycle (RMS50%), and 20% of the cycle (RMS20%). We applied spectral analysis (Hanning window processing and 1024-point fast Fourier transform) to each time window (a series of 45% of the compression cycle of EMG data with 50% overlapping) to obtain the MF value [12]. 2.5. Statistical analysis We used descriptive statistics to calculate all outcome variables. We also applied repeated-measures analysis of variance to the mean of the delivered force, compression depth, number of correct depth, compression rate, RMS100%, MF, and RMS20% data within participants to compare the time effect. We applied the Bonferroni adjustment a priori to pairwise comparisons and used Scheffé post hoc analysis to identify differences in analysis of variance if the main effect was significant. We used a paired t test to compare the RMS50% differences within participants. The significance level of this study was set at P b .05. All parameters were statistically analyzed using SPSS 19 software for Windows (SPSS Inc, Chicago, IL). 3. Results Table 1 shows the maximal amplitude of EMG for 10 muscles during chest compression. The pectoralis major, ES, and RA exhibited the greatest muscle activity of all muscles during chest compression, whereas the latissimus dorsi and gluteus maximus exhibited the least muscle activity. Fig. 1 shows the RMS50% of EMG for 10 muscle groups. The RMS50% of the push-down phase is significantly larger than that of the release phase for PMr, PMl, LDr, RAr, RAl, ESr, ESl, GMr, and GMl. A comparison of these results with the contralateral muscle in RMS50% shows no significant differences between most bilateral muscles. Only the RMS50% of GMl is significantly greater than that of GMr in the release phase (P = .02). An RMS50% discrepancy of 40% appeared. Fig. 2 shows the RMS20% of EMG for 10 muscles. The total compression cycle of each muscle consists of 5 phases. Each phase accounts for 20% of the compression cycle (RMS20%). The RMS20% varies significantly among the 5 phases of the same muscle for all muscles, except the bilateral latissimus dorsi. The results of post hoc Table 1 The mean and standard deviation of the maximal amplitude of EMG Muscle
Right/left
Pectoris major
R L R L R L R L R L
Latissimus dorsi Rectus abdominis Erector spinae Gluteus maximus
Maximal amplitude of EMG in percentage of MCV Mean
SD
56% 59% 31% 32% 49% 45% 56% 52% 24% 34%
20% 15% 20% 23% 21% 22% 15% 21% 15% 21%
R means right side, and L means left side.
Please cite this article as: Tsou J-Y, et al, Electromyography activity of selected trunk muscles during cardiopulmonary resuscitation, Am J Emerg Med (2013), http://dx.doi.org/10.1016/j.ajem.2013.10.044
J.-Y. Tsou et al. / American Journal of Emergency Medicine xxx (2013) xxx–xxx
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*
Push-down Release
*
P < .001 P < .001
Table 2 The results of post hoc test between the phase of maximal RMS20% and others P value Right/ The left phase Phase 1 Phase 2 Phase 3 Phase 4 Phase 5 of max. RMS20%
Muscle
%MVC
*
*
20
*
*
*
*
*
P = .008 P = .192 P < .001 P < .001 P < .001 P < .001 P = .019 P = .004
15
Pectoris major
R L Rectus abdominis R L Erector spinae R L Gluteus maximus R L
10 5 0 PMr PMl
LDr
LDl
RAr
RAl
ESr
3
Phase 2 Phase 2 Phase 2 Phase 2 Phase 4 Phase 4 Phase 4 Phase 4
.000 * .000 * .012 * .002 * .000 * .000 * .040 * .042 *
– – – – .000 .000 .019 .039
* * * *
.681 .007 * .012 * .001 * 1.000 1.000 1.000 1.000
.006 .000 .001 .000 – – – –
* * * *
.000 * .000 * .001 * .000 * .000 * .000 * .067 .024 *
ESl GMr GMl
Muscle Fig. 1. The average RMS50% of EMG for 10 muscles during a chest compression cycle. *Significant differences between push-down phase and release phase in the same muscle. Error bars denote standard deviation.
test were shown in Table 2 to identify differences between the phase of maximal RMS20% and others if the main effect was significant. During a chest compression cycle, the maximal RMS20% of PMr, PMl, RAr, and RAl occurs during Phase 2. The maximal RMS20% of ESr, ESl, GMr, and GMl occurs during Phase 4. A comparison of bilateral muscle activity in RMS20% shows that bilateral muscles exhibit similar muscle recruitment patterns. There is no significant difference between bilateral muscles in the same phase except for Phase 1 of bilateral GM (P = .028). Figs. 3 and 4, respectively, show the average RMS100% of EMG and the MF of EMG in the first, third, and fifth minutes. These figures show no significant differences in RMS100% and MF for all muscles. A comparison of these results with the contralateral muscle in RMS100% during the same periods shows no significant differences between bilateral muscles. Table 3 shows the average maximal delivered force, compression depth, number of correct depth, compression rate, and EMG ratio in the first, third, and fifth minutes. The delivered force, compression depth, and number of correct depth during these 3 periods decreased significantly over time. The EMG ratios (ES/RA and ES/GM) increased significantly over time. The compression rate had no significant difference in the 3 periods. 4. Discussion This study presents the trunk EMG patterns of the healthy and experienced health care providers. The maximal EMG amplitude of Phase1 Phase2 Phase3 Phase4 Phase5
*
*
*
RMS (% MVC)
* 20 P = .171 P = .415
* *
15
*
10
1st min 3rd min 5th min
20 18 16
RMS (% MVC)
* 25
the pectoralis major, ES, and RA exhibited muscle activity exceeding 45% of the maximal voluntary contraction during chest compression. The pectoralis major, RA, and latissimus dorsi exhibited higher muscle activity during the push-down phase, whereas the ES and GM exhibited greater activation during the release phase. Muscle activity was categorized during the exercise as minimal (0%-20% MVC), moderate (21%-50% MVC), or high (N50% MVC) [13,14]. According to these categories, the bilateral pectoralis major and ES generated high muscle effort; and the bilateral RA, latissimus dorsi, and GM produced moderate intensity of muscle activity during a compression cycle. Although the RA activity was categorized as moderate, it was near the border of the high level. Therefore, muscle training programs designed for CPR professionals should include muscle power training for the pectoralis major, ES, and RA. Ideally, the duration of the push-down (compression) phase should be equivalent to the duration of the release (decompression) phase [5]. The pectoralis major, RA, and latissimus dorsi had higher muscle activity during the push-down phase, especially during Phase 2. These results indicate that these muscles generate the push-down force. During the release phase, the ES and GM, which lift the trunk to the starting position of compression, exhibit more obvious RMS to produce hip extension and trunk extension. In addition to the agonist function, the muscles also play a synergistic or antagonistic role in co-contraction with the agonist muscle. The strengthening of core muscles is often involved in the rehabilitation of LBP. The core muscles can be described as a muscular box with the abdominals in the front, paraspinals and gluteals in the back, the diaphragm as the roof, and the pelvic floor and hip girdle musculature as the bottom [15]. The core muscles works synergistically to provide a proper force distribution and maximal force
14 12 10 8 6 4
5
2
0
0 PMr PMl LDr
LDl
RAr RAl ESr
ESl GMr GMl
Muscle Fig. 2. The average RMS20% of EMG for 10 muscles during a chest compression cycle. Error bars denote standard deviation. *P b .000.
PMr PMl LDr LDl RAr RAl ESr ESl GMr GMl
Muscle Fig. 3. The average RMS100% of EMG in the first, third, and fifth minutes. Error bars denote standard deviation.
Please cite this article as: Tsou J-Y, et al, Electromyography activity of selected trunk muscles during cardiopulmonary resuscitation, Am J Emerg Med (2013), http://dx.doi.org/10.1016/j.ajem.2013.10.044
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1st min 3rd min 5th min
180
Median Frequency (Hz)
160 140 120 100 80 60 40 20 0 PMr PMl LDr LDl RAr RAl ESr ESl GMr GMl
Muscle Fig. 4. The MF of EMG in the first, third, and fifth minutes. Error bars denote standard deviation.
generation with minimal compressive or shearing forces at the spine [16]. Core muscles also provide proximal stability for distal movement [17]. During compression, the RA and ES co-contract to stabilize the pelvis and lumbar spine against the pull of the iliopsoas muscle during active hip flexion (push-down phase) to avoid increased lumbar lordosis and anterior shearing of the vertebrae. The bilateral RA, ES, pectoralis major, and latissimus dorsi synergistically stabilize the rib cage and shoulder girdle to transfer the pushing force to the upper extremity. We used EMG ratios (ES/RA and ES/GM) to present the synergistic features of core muscle [18]. Research used this ratio to compare the trunk muscle recruitment patterns in LBP patients with the healthy participants during trunk flexion-extension [19]. They found that the ratio of antagonist over agonist of lumbar EMG amplitude was greater in the patients. During compression, ES is an antigonist muscle and RA is an agonist muscle. Our results show that ES/RA ratio increased significantly over time. These means that the relationship of ES and RA muscle activity is more and more similar to the LBP participants' with increasing operating time. The ES and GM are synergistic muscles coworking for trunk lifting. The ES/GM ratio also increased significantly over time. The GM muscles are more fatigable in chronic LBP [20]. The increasing of EMG ratios (ES/RA and ES/GM) might lead to increase lumbar mobility and decrease hip mobility, which would increase lumbar loading and decrease delivered force. Muscle training should be focused on keeping EMG ratios at the same level with increasing operation time. Surface EMG has been used to understand the function of trunk muscles in both healthy controls and LBP patients during specific postures and movements [9,21,22]. Contralateral muscle balance has been one issue of surface EMG. The EMG contralateral imbalances of trunk muscles are often related to back pain [22,23]. Chest compression is a relatively symmetric movement for the bilateral Table 3 The mean and standard deviation of the EMG ratio, the maximal delivered force, compression depth, number of correct depth, and compression rate in the first, third, and fifth minutes Measurement
1st min Mean
3rd min SD
Mean
5th min SD
Mean
P value SD
ES/RA ratio 0.99 0.11 1.02 0.06 1.06 0.07 ES/GM ratio 1.38 0.25 1.42 0.26 1.44 0.28 Delivered force (N) 470.6 55.5 461.0 60.2 446.6 64.0 Compression 53.3 2.6 51.9 3.4 50.2 4.5 depth (mm) No. of correct depth (%) 97.7 9.0 93.9 13.2 91.2 17.2
.047 .032 .001 .000 .019
trunk and extremities. The results of this study show that EMG activity is balanced for almost all selected muscles except the GM. Oddsson and De Luca [9] recorded bilateral paraspinal EMG activity in healthy men and chronic LBP patients. They found that the contralateral RMS amplitude in healthy controls was more symmetric than that in chronic LBP patients. This finding supports the current results regarding the symmetric EMG activity of chest compression in healthy participants. Previous studies found that the muscle imbalance of GM was associated with LBP occurrence in female athletes [24-26]. The GM muscle activity during the flexion-extension cycle was lower in patients with chronic LBP than in healthy participants [27]. Imbalance of GM might be a feature developing LBP while performing CPR. The relationship between imbalance of GM and LBP needs further examination. The power spectrum of the frequency domain of the surface EMG represents a summary of all the spectrum contributions of the active motor unit action potentials recorded by the EMG sensor. Shifts in the power spectrum often serve as indicators of muscle fatigue [28,29]. The MF is the most commonly used index of power spectral alterations to detect muscle fatigue [30]. The RMS and MF showed no significant differences over time; this means that the selective muscles might not experience fatigue. The overall delivered force, compression depth, and the percentage of number of correct depth decreased significantly over time. It indicates that the neuroelectrical activity (the motor output from the cortex and motor unit recruitment, detected by RMS and MF) did not change and the overall muscle contraction force (detected by delivered force) decreased. These suggest that overall muscle efficiency decreases. A previous study also reported that the relationship between dynamic contractions instantaneous MF and muscle fatigue is nonlinear and more complex during repetitive lifting [31]. They hypothesized that a complex strategy using muscle loadsharing provides periods of metabolic recovery to limit localized fatigue during strenuous dynamic exercise [31]. Researches evidenced that the depth or force of chest compression decays after 1 to 2 minutes of CPR [32-35]. These results are consistent with our finding that the compression depth and delivered force declined over time. Thus, we agree with the suggestion of the 2010 American Heart Association Guidelines: “When 2 or more rescuers are available it is reasonable to switch chest compressors approximately every 2 minutes to prevent decreases in the quality of compressions” [36]. However, the depth of compression decreased only 3.1 mm on average in the 5 minutes; and average depth was 50.2 mm above 5 cm according to the 2010 CPR guideline. A total of 91.2% of the compressions were still of the correct depth. Compression rate did not decrease significantly, and trunk muscle did not exhibit significant fatigue within 5 minutes. These indicates that the healthy and experienced rescuer performing CPR within 3 to 5 minutes still has acceptable CPR quality and low risk of LBP. The first limitation of this study is that it does not include the iliopsoas muscle. The iliopsoas may interfere with or distort the recording of surface EMG because it is a deep muscle, and chest compression has larger hip flexion movement. From a biomechanical view, keeping the lumbar spine straight and acting from the hip joint as the axis are the best strategies to reduce lumbar loading and reduce energy consumption. The iliopsoas muscle is a major agonist muscle for hip flexion. It may be an important muscle of the trunk for chest compression. The second limitation of this study is that upperextremity muscles also play an important role in chest compression, but this is beyond the scope of this study. Further research should focus on the analysis of upper-extremity muscles. 5. Conclusion This study presents a clear picture of the muscle activity and function of the trunk during chest compression in healthy experienced participants. The pectoralis major, ES, and RA generated larger
Please cite this article as: Tsou J-Y, et al, Electromyography activity of selected trunk muscles during cardiopulmonary resuscitation, Am J Emerg Med (2013), http://dx.doi.org/10.1016/j.ajem.2013.10.044
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muscle activity above 45% of MVC during chest compression. It indicated that designing muscle training programs for CPR professionals should emphasize muscle power training for the pectoralis major, ES, and RA. The results of this study indicate that the efficiency of the trunk muscle decreases over time during chest compression, but the healthy and experienced rescuer performing CPR within 3 to 5 minutes still has acceptable CPR quality and low risk of LBP. The GM showed imbalanced muscle activity, and the EMG ratios (ES/RA and ES/GM) increased over time. Thus, keeping bilateral GM balance and maintaining the same level of EMG ratios might be the keys to prevent LBP while performing CPR. Further researches should compare the alternated muscle recruitment pattern in the LBP patient with our findings. Acknowledgments The authors gratefully acknowledge the financial support of the National Science Council, Taiwan, ROC (grant no. NSC 98-2320-B-006001). Prof Soong-Yu Kuo is gratefully acknowledged for his suggestions. References [1] Bejia I, Younes M, Jamila HB, Khalfallah T, Ben Salem K, Touzi M, et al. Prevalence and factors associated to low back pain among hospital staff. Joint Bone Spine 2005;72(3):254–9. [2] Jones AY, Lee RY. Cardiopulmonary resuscitation and back injury in ambulance officers. Int Arch Occup Environ Health 2005;78(4):332–6. [3] Jones AY. Can cardiopulmonary resuscitation injure the back? Resuscitation 2004;61(1):63–7. [4] Hu KW, Guo HR, Lee HL, Lin HJ, Liao CK, Chen KT, et al. Cardiopulmonary resuscitation and back pain among emergency medical technicians. J Emerg Crit Care Med 2008;19(3):93–101. [5] Tsou JY, Chi CH, Hsu RM, Wu HF, Su FC. Mechanical loading of the low back during cardiopulmonary resuscitation. Resuscitation 2009;80(10):1181–6. [6] Takahashi I, Kikuchi S, Sato K, Sato N. Mechanical load of the lumbar spine during forward bending motion of the trunk—a biomechanical study. Spine (Phila Pa 1976) 2006;31(1):18–23. [7] Hayden JA, van Tulder MW, Malmivaara A, Koes BW. Exercise therapy for treatment of non-specific low back pain. Cochrane Database Syst Rev 2005;3(20): CD000335. [8] De Luca CJ. Use of the surface EMG signal for performance evaluation of back muscles. Muscle Nerve 1993;16(2):210–6. [9] Oddsson LI, De Luca CJ. Activation imbalances in lumbar spine muscles in the presence of chronic low back pain. J Appl Physiol 2003;94(4):1410–20. [10] Kendall FP, McCreary EK, Provance PG. Muscles: testing and function. 4th ed. Lippincott Williams & Wilkins; 1999. [11] Clancy EA, Morin EL, Merletti R. Sampling, noise-reduction and amplitude estimation issues in surface electromyography. J Electromyogr Kinesiol 2002;12(1):1–16. [12] Lariviere C, Arsenault AB, Gravel D, Gagnon D, Loisel P. Surface electromyography assessment of back muscle intrinsic properties. J Electromyogr Kinesiol 2003;13(4):305–18. [13] McCann PD, Wootten ME, Kadaba MP, Bigliani LU. A kinematic and electromyographic study of shoulder rehabilitation exercises. Clin Orthop Relat Res 1993;288:179–88. [14] Decker MJ, Hintermeister RA, Faber KJ, Hawkins RJ. Serratus anterior muscle activity during selected rehabilitation exercises. Am J Sports Med 1999;27(6): 784–91.
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