Muscle Oxygen Saturation Correlates with Muscle Mechanomyography during Prolonged Electrical Stimulation-Evoked Wrist Extension Exercise

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1 Muscle Oxygen Saturation Correlates with Muscle Mechanomyography during Prolonged Electrical Stimulation-Evoked Wrist Extension Exercise Nurul Salwani Mohamad Saadon 1 Nur Azah Hamzaid 1 Nazirah Hasnan 2 Muhammad Afiq Dzulkifli 1 Mira Teoh 1 Gan Kok Beng 3 Glen M. Davis 4 1 Department of Biomedical Engineering, Faculty of Engineering, University of Malaya Dr. Nur Azah Hamzaid azah.hamzaid@um.edu.my 2 Department of Rehabilitation Medicine, Faculty of Medicine, University of Malaya 3 Department of Electrical and Electronic & Systems Engineering, Faculty of Engineering & Built Environment, Universiti Kebangsaan Malaysia 4 Clinical Exercise and Rehabilitation Unit, Discipline of Exercise and Sports Sciences, Faculty of Health Sciences, University of Sydney, Lidcombe, Australia Abstract. This study assessed electrically-evoked sustained muscle contractions with real-time changes in near-infrared spectroscopy and mechanomyography signals. Twenty healthy volunteers performed electrical-evoked wrist extension for 10 minutes. Root mean square derived from MMG (%RMS-MMG) and tissue oxygen saturation (%StO2) from NIRS of the extensor carpi radialis muscle were monitored throughout the sessions. The correlated responses of these two measures comprised 7 consecutive sets of 10 contractions each. %StO2 revealed an initial decline from muscle contraction 1 to 10 and then an increase from contraction 11 to 70. For %RMS-MMG, a significant decrease was observed from contraction 1 to 10 as well as from contraction 41 to 60 while an increase was seen from contraction 11 to 40 and from contraction 61 to 70. Positive low-order correlations were found between %StO2 and %RMS-MMG during the start of the exercise while later on, the two variables were negatively correlated. As the number of contractions increased over time, increased %StO2 revealed good oxygen saturation aligned with decreased %RMS-MMG values, suggesting decreased muscle fiber activation and strength. In this study, the physiological muscle responses were associated with its mechanical characteristics. Keywords: Functional Electrical Stimulation, Muscle Strength, Muscle Oxygenation, Rehabilitation, Upper Limb 1 Introduction Functional electrical stimulation (FES) training has become very popular for rehabilitation purposes. Through FES exercise, muscle function can be improved leading to improved health [1]. During FES-evoked muscle contractions, muscle fatigue occurs quickly [2] due to the non-physiological pattern of motor unit recruitment and the preferential stimulation of large diameter neurons innervating fast-fatiguing muscle fibers [3]. Mechanomyography (MMG) records the mechanical activity of muscles in order to monitor muscle vibrations as the muscle fibers contract [4].The decreasing amplitude

2 2 of MMG signal portrays the force developed by the muscle wherein it continues to decline throughout fatiguing contractions [5]. Near Infrared Spectroscopy (NIRS) has been widely used to assess muscle oxygen saturation (StO 2) and indirectly mitochondrial activity within muscle [6] during exercise, thus NIRS could be an alternative method in characterizing muscle fatigue during repetitive movements [7]. There are no studies that have measured both MMG and NIRS simultaneously to assess muscle performance during prolonged FES-evoked exercise, especially during upper limb isometric exercise. Accordingly study investigated the relationship between MMG and NIRS during sustained repetitive electrically-evoked wrist extension exercise. 2 Materials & Methods 2.1 Subjects Twenty subjects (N=20: 9 males, 11 females; age: 23.5±2.1 y; weight: 68.1± 18.8 kg and height: 161.8± 6.8 m) participated in the study after giving their informed written consent. The Medical Ethics Committee, University Malaya Medical Centre approved this study (MECID.NO: ). All were in good health with no history of upper extremity musculoskeletal disorder or surgeries. 2.2 Functional Electrical Stimulation An Ottobock STIWELL med4 surface stimulator (MED-EL Elektromedizinische Geräte GmbH, Austria) was used to provide electrical stimulation to the muscles with a pulse width of 250µs and frequency of 30Hz to produce a full joint extension. 2.3 Near Infrared Spectroscopy An InSpectra tissue spectrometer model 650 (Hutchinson Technology Inc., Hutchinson, MN) measured the tissue oxygen saturation (%StO 2) and was able to measure StO 2 at a depth of 14 mm, suitable for small muscles. 2.4 Mechanomyography Accelerometer-based MMG sensors, Sonostics VMG BPS II Transducer (MP150, Biopac System Inc, USA) with 2k Hz of sampling rate was used to measure muscle force development. Data was then filtered with a bandpass filter (20Hz lower cut off frequency and 200Hz higher cut off frequency). MMG-RMS was extracted from the raw MMG signal and was normalized to %RMS-MMG. 2.5 Study Procedure Subjects were seated with their right hand positioned on the table and pneumatic cuff was placed on the forearm. Two electrodes were placed, one just above the wrist and the other one was placed close to the lateral epicondyle of the humerus. NIRS and

3 3 MMG s probes were placed along the ECR muscle belly and a double-sided tape was used to ensure consistent contact pressure. After 3-min of rest, super-systolic arterial occlusion was performed whereby the cuff was inflated to 250mmHg until %StO 2 reached a nadir lasting at least 5s, then the cuff was released immediately. Subsequently, the subjects muscles were electrically (FES)- evoked to perform sustained repetitive 4sec rest 4sec wrist extension for 10 minutes and super-systolic occlusion was performed for the second time. NIRS and MMG measurements were taken continuously during rest, occlusion and 10 minutes of exercise. 2.6 Data Analysis The mean of %StO 2 during the 3-min rest period before exercise was taken as an indicator for each subject s resting StO 2. Mean % StO 2 from NIRS were obtained from each 4sec contractions, while %RMS-MMG were normalized and mean amplitude for every 4sec contractions were computed using epoch analysis. 2.7 Statistical Analysis Contractions were grouped to set 1 (contraction 1-10), set 2 (contraction 11-20), set 3 (contraction 21-30), set 4 (contraction 31-40), set 5 (contraction 41-50), set 6 (contraction 51-60) and set 7 (contraction 61-70). Statistical analyses were performed using IBM SPSS Statistics 24 (SPSS Inc., USA). For both %StO 2 and %RMS-MMG, paired t-test were deployed and correlation analyses for both data were done on every set of contractions for the whole exercise session. Data are presented as means ± standard deviations and p<0.05 was considered significant. 3 Results 3.1 Overview Fig. 1 portrays %StO 2 and %RMS-MMG plotted contractions set. Fig. 1 %StO2 and %RMS-MMG by set of contractions. * indicates a significant difference from the preceding set (p<0.05)

4 4 3.2 T-test Analysis Paired t-test was done for both %StO 2 and %RMS-MMG respectively, where each set was compared to the set prior to it. For %StO 2, a negligible decrease of 0.7% was observed from set 1 to 2. Increasing trends were seen between set 2 and 3 (2.9%), set 3 and 4 (1.5%), set 4 and 5 (1.1%), set 5 and 6 (1.2%) and set 6 to 7 (0.4%). All increasing trends were statistically significant (p<0.05). %RMS-MMG showed a significant decrease of 13.8% that can be seen between set 1 and 2, set 4 and 5 (1.2%) and set 5 and 6 (0.2%) respectively. Increasing trends were observed between set 2 and 3 (3.6%), set 3 and 4 (2.3%) and set 6 and 7 (1.1%). 3.3 Correlation Analysis A linear correlation coefficient (r) measured the degree of association %StO 2 and %RMS-MMG. %StO 2 revealed weak positive correlation with number of contraction (r=0.16, p=0.00), while %RMS-MMG showed a weak negative correlation. Correlations analysis were divided into two parts; (i) %StO 2 vs %RMS-MMG for whole exercise and (ii) %StO 2 vs %RMS-MMG by set of contractions. The correlation between %StO 2 and %RMS-MMG was negatively correlated (r=-0.10, p=0.00) throughout the exercise. As by set of contractions, positive correlations between %StO 2 and %RMS- MMG were seen at set 1 and set 4 but they were not statistically significant while significantly negative correlations were observed at set 2 (r=-0.22, p=0.00), set 3 (r=-0.20, p=0.01), set 5 (r=-0.19, p=0.01), set 6 (r=-0.15, p=0.03) and set 7 (Table 1). Table 1. Correlations of %StO2 with %RMS for each set of contractions (N=20),* correlation is significant at the 0.05 level (2-tailed). Set of Overall Contractions Correlation -0.10* * -0.20* * -0.15* -0.16* 4 Discussion 4.1 Oxygen Saturation A decline in %StO 2 was observed between set 1 and 2 of the contractions. The same pattern has been seen during arm cranking in healthy subjects, whereby an initial decline of %StO 2 due to muscle deoxygenation has been noted [8]. In order to meet the metabolic demands of the ECR during exercise, a greater need for oxygen is needed compared to resting conditions as FES-evoked exercise has a greater energy demand compared to voluntary exercise [9]. The drop in %StO 2 may also have been due to a decrease in the ability of oxygen to bind with hemoglobin in the circulating blood within isotonically-contracting muscle when increasing contractions quicken the production of lactic acid thus increasing car-

5 5 bon dioxide output in the blood [10]. Hence, the decrease may not just be from augmented metabolic demand, but also due to a greater release of oxygen from hemoglobin due to metabolic acidosis. After the initial decrease of %StO 2, trends for increased muscle oxygen saturation was clearly observed during set 2 until set 7. Our findings revealed striking similarities with Muraki et al. where StO 2 started to increase along with total hemoglobin and oxyhemoglobin indicating good oxygen uptake during exercise [8]. The general trend of an initial drop followed by a steady increase of %StO 2 throughout the contraction was reportedly often found in healthy subjects [11]. 4.2 Muscle Mechanomyogram During set 1 and set 2 %RMS-MMG significantly declined, followed by a relatively small increase of %RMS-MMG between set 2 to 4 and set 6 to 7. The decline of muscle performance observed during the early phase of the exercise may be due to insufficient oxygen supply for ECR muscle activation, hence the decrease in muscle force represented by %RMS-MMG [12]. The decrease in %RMS-MMG might foreseeably occur in slow-twitch fibers at high contraction levels [13]. MMG also has been associated with intramuscular activities that are related to muscle blood flow. During sustained exercise, there may be an increase in intramuscular pressure that can cause muscle fiber dimensions to change, leading to inefficient activation [4]. After the initial decline, %RMS-MMG was observed to portray a steady increase. The increase of %RMS-MMG may have been due to the probable recruitment of new motor units [4] that occurs when exercising muscles started to fatigue [12]. The subjects in this study also might have had a faster muscle metabolic recovery rate. Such findings agreed with a previous study whereby an adaptation happened where the muscle was more resilient to damage and repaired at a quicker rate among healthy subjects during eccentric exercises [14]. 4.3 Relationship between %StO2 and %RMS-MMG The overall correlation from contraction 1 to 70 revealed a significantly weak negative relationship between %StO 2 and %RMS-MMG indicating that they tracked in different directions. Set 1 showed a positive correlation whereby %StO 2 decreased along with %RMS-MMG. %StO 2 declined due to the muscle consuming the oxygen during exercise, while %RMS-MMG decreased due to the reduction in muscle force. Significant negative relationships were observed from set 2 of contraction until set 7 except for set 4 which revealed that %StO 2 increased while %RMS-MMG declined. An increase of %StO 2 suggested that the ability of ECR muscle to extract oxygen from the muscle circulation became limited during progressively repeated exercise and this might also be due to poor oxygen uptake and/or low perfusion within the ECR itself [9]. Meanwhile, %RMS-MMG decreased as muscle performance declined due to fatigue [13].

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