Measurement of quadriceps endurance by fnirs

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1 Measurement of quadriceps endurance by fnirs Devrim Erdem a, Ömer Şayli a, Mustafa Karahan b, A. Akın a a Biomedical Engineering Institute, Boğaziçi University, Bebek - İstanbul, Turkey b Faculty of Medicine, Orthopaedics & Traumatology Department, Marmara University, Haydarpaşa/İstanbul, Turkey ABSTRACT In this paper, the changes in muscle deoxygenation trends during a sustained isometric quadriceps (chair squat/half squat) endurance exercise were evaluated among twelve male subjects and the relationship between muscle oxygenation and endurance times was investigated by means of functional near-infrared spectroscopy (fnirs). Neuromuscular activation and predictions of muscle performance decrements during extended fatiguing task was investigated by means of surface electromyography (semg). The results of the study showed that in the subjects who maintained exercise longer than five minutes (group 1), mean Hb recovery time (33 [sec.]) was 37.4% less than the others (group 2, 52.7 [sec.]). Also mean HbO 2 decline amplitude (2.53 [a.u.] in group 1 and 2.7 [a.u.] in group 2) and oxy decline amplitude (8.4 [a.u.] in group 1 and 3.4 [a.u.] in group 2) in the beginning of squat exercise are found to be 22.6% and 176.9% bigger in these group. For the EMG parameters, mean slope of MNF and MDF decline are found to be 57.5% and 42.2% bigger in magnitude in group 2 which indicates higher degree of decrement in mean and median frequencies although their mean squat duration time is less. This indicates higher index of fatigue for this group. It is concluded that training leads to altered oxygenation and oxygen extraction capability in the exercising muscle and investigated fnirs parameters could be used for endurance evaluation. Keywords: Functional near-infrared spectroscopy (fnirs), surface electromyography (semg), muscle, muscular endurance, training, vastus lateralis 1. INTRODUCTION Providing the ability to track concentration changes and trends of oxyhemoglobin, deoxyhemoglobin, the use of functional Near Infrared Spectroscopy (fnirs) technology finds widespread use in sports medicine. fnirs offers a safe, non-invasive means of monitoring cerebral and muscle function without the use of radioisotopes or other contrast agents 1. This technology is based on the fact that light in the wavelength range nm is weakly absorbed by tissue. Light in this range (called optical window ) has a good penetration depth. In NIRS, a light source sends a light to the tissue in the near-infrared range and this light diffuses in the tissue. Light is absorbed and scattered in the tissue and part of the scattered light reaches the light detector placed typically cm apart from the source (called optode distance). By measuring the change in the intensity for multiple wavelengths, it is possible to calculate change in the concentrations of oxyhemoglobin (HbO 2 ) and deoxyhemoglobin (Hb). Since light passing through the large vessels is mostly absorbed, light that reaches the detector comes mainly from small blood vessels 2 (arterioles, capillaries and venules). This technique gives dynamic balance information between O 2 supply and consumption while it offers noninvasive and inexpensive method for the study of aerobic metabolism and hemodynamics 3,4 and it has become a widely used technology for the oxidative metabolism investigation in tissues, especially in brain and muscle. During recent decades, there is a growing interest in examining the changes in skeletal muscle respiration during a variety of exercise conditions 5. Scientists have successfully used this noninvasive technique to investigate the diseases associated with impaired tissue oxygenation as well as human muscle performance, oxygen consumption and metabolic processes. Efforts for evaluating muscle performance expose muscular endurance are a particular issue to explore. In addition to the use of various exhaustive exercise protocols, Electromyography (EMG) for evaluation of fatigue, Magnetic Resonance Spectroscopy (MRS) for chemical information -inorganic phosphate (Pi), phosphocreatine (PCr) and ph levels- about tissues under investigation, gas exchange and cardiac output measures, Doppler ultrasound for blood flow measures, are being utilized. At that point, Functional Near-Infrared Spectroscopy (fnirs) emerges as a valuable ata.akin@boun.edu.tr, phone: ; fax: ; Multimodal Biomedical Imaging, edited by Fred S. Azar, Dimitris N. Metaxas, Proc. of SPIE Vol. 681, 6812, (26) /6/$15 doi: / Proc. of SPIE Vol

2 method to assess levels of tissue oxygenation/deoxygenation trends in evaluating oxygen supply at the capillary level, which is one of the critical determinants of muscular endurance, to the contracting muscle during the effort. In this study, we considered a hypothesis that a longer duration of isometric contraction is related to an increased oxygenation status of the muscle. By this motivation the variation of deoxygenation trends in the muscle by means of fnirs and neuromuscular activation and predictions of performance decrements during extended fatiguing task was investigated by means of semg. 2. METHODS 2.1 fnirs In this study a continuous wave NIRS device is used to study the hemodynamics of vastus lateralis muscle (NIROXCOPE 21, Boğaziçi University, Biophotonics Lab.). The device consists of i) a probe containing light sources and detectors on a flexible printed circuit board (PCB), ii) a software to control the device and store the data on the computer for offline analysis and iii) transmitter/receiver circuits which control the LEDs, light sources with the software and LED currents. The distance between light sources (LEDs) and detectors is 2.5 cm, which enables nearly 1.25 cm penetration depth in the tissue 2. Six light source-detector pairs are available in the probe. LEDs emit light at wavelengths 73 nm and 85 nm. By transmitting and receiving light at multiple wavelengths in the near-infrared range and using modified Beer-Lambert law, concentration changes of oxyhemoglobin ( [HbO 2 ]) and deoxyhemoglobin ( [Hb]) are calculated as well as oxy signal which is the difference between concentration changes of [HbO 2 ] and [Hb] in the probed tissue. Operation of the device can be controlled by a program written in MS Visual C++. Frame rate (one complete data reading from all 4 quadrants) can be changed using the graphical user interface provided 6. The NIROXCOPE 21 provides 16 channels spatial and 2 Hz temporal resolution NIRS measurements. 2.2 semg Electromyography measurements are based on changes in electrical potential of a muscle when it is caused to contract by a motor nerve impulse. It is accepted that variations in motor neuron firing patterns and muscle fiber conduction velocity (MFCV) are reflected in changes in signal energy and frequency content of the signal which provide information about fatigue existence and endurance period of the muscle. It has been proposed that the root mean square (RMS) and median frequency (MDF) provide information relative to the number and location of the active motor units, the recruitment of motor units, the shape of the motor unit action potentials, the mean firing rate of the individual motor units, and the extent of superposition of action potentials from concurrently active motor units 7. The majority of the literature states that MDF 8-1 and mean frequency 11 (MNF) are the most reliable spectral parameters in monitoring changes in the muscle fiber propagation, muscle temperature, muscle fatigue and muscle fiber type. Each electrode site was shaved, abraded, and cleaned with alcohol to facilitate electrode adherence and conduction of EMG signals. Adhesive silver-silver chloride (Ag-AgCl) surface electrodes, having a diameter of.5 cm, were placed over the belly of the right vastus lateralis muscle with a 2.5 cm inter electrode distance. Signals were acquired with BIOPAC Model MP3 hardware and BIOPAC Student Lab. Pro Software systems. It is well known that the bandwidth of the surface EMG signals (semg) is less than 1 Hz. The EMG signals were therefore sampled at a rate of 2 Hz. System passed signals between 3-1Hz. Notch filter was used to remove power line interference at 5 Hz. During data acquisition data were passed to hard disc for storage. 2.3 Experiment Protocol In this study, twelve healthy male subjects aged between 2 and 27, with no reported history of neurological or orthopedic disorder comprised of trained and less trained or sedentary individuals, volunteered to exercise unloaded squat with the knee angle at 7 flexion from full extension until fatigue set in. Both fnirs and semg measurements were gathered from vastus lateralis of the quadriceps muscle. Each subject was seated upright in a specially constructed exercise chair which permitted adjustment for differences in height and leg length to enable maintenance of constant body position during contraction. Two tests were conducted separated by an interval of 5 minutes. The first test involved maximum voluntary isometric contraction of quadriceps muscle group enabling optimum contraction of vastus lateralis with the foot was in full dorsi flexion and eversion for 1 seconds while sitting on a chair. After the break the second test was performed in chair squat or modified half squat. This second test lasted until subject experienced the feeling of fatigue and was not able to keep the angle at 11 between the lower leg and upper leg. Initially baseline measurement Proc. of SPIE Vol

3 was taken for 1 minute for the two experiments. Duration of squat exercise varied among subjects and experiments ended according to subjects own decision or when they were unable to maintain the specific knee angle determined at the onset of the trial. Lastly participants returned to baseline position again for recovery time measurements for 5 minutes. This half chair modified squat exercise model was chosen for three reasons. First, it is a well-controlled model in which the rate of work can be regulated easily. Second, it is a pure isometric model, and third, it avoids motion artifacts and enables application of two different methods at the same time. A variety of muscular endurance assessment strategies are available, yet isometric endurance testing seems to be cost-effective and requires less equipment for testing 12. Squat wall endurance test for the evaluation of quadriceps muscle group is found to be safe due to being a closed chain exercise (CKC) for anatomical components of knee joint and suitable to use prolonged periods of time 13. Another factor that makes squat endurance test advantageous is that isometric contracting muscle, which is held for an extended period of time, causes blood flow to be either compromised or occluded because of the high intramuscular pressure. Depending on the anatomical relationship of muscle and bone, blood flow may be occluded at forces only slightly higher than 15% MVC. When the muscle is deprived of its capability of supply and removal it becomes a closed system which makes NIRS measurement possible without applying occlusion. Ri (a) (h) Figure 1 a) Measurement of maximum voluntary isometric contraction (MVIC) for 1 seconds b) Measurements during squat exercise until fatigue Electrode placement was determined by placing subjects in the appropriate test positions and a thigh girth measurement was taken at a point 5% of the distance between the inguinal ligament and the superior pole of the patella. The electrode was placed lateral to an imaginary line bisecting the anterior superior iliac spine and the superior patellar pole at the 5% position described above. The lateral distance equaled 15% of the thigh girth measurement and electrode placed after controlling the muscle bellies by palpation 13. All electrodes were positioned parallel to the muscle fibers. A common ground electrode was placed laterally on the lateral epicondyl of tibia. fnirs probe was placed just below the surface EMG electrodes. Elastic wraps were applied to maintain electrode and probe placement during the test. 2.4 Data Analysis [Hb], [HbO 2 ] and [OXY] parameters are used in evaluation of fnirs measurements. A typical trace is shown in Figure 2. Hb recovery half times and slopes, HbO 2 and OXY decline amplitudes and slopes were determined as an indicator of endurance performance yet, BV (Blood Volume) measurements are not evaluated. After the end of squat test, change of concentration between minimum point and maximum point is taken as the full range and time to reach half of the 95% of the full range is calculated as half-time value 2 (t1/2) for Hb. For Hb, recovery slope is also calculated considering maximum point at the end of squat and minimum point afterwards. Decline slope and decline amplitude Proc. of SPIE Vol

4 parameters were calculated in the beginning of the squat exercise for HbO 2 and oxy signal as shown in the Figure 2. It is thought that these would give valuable information for the oxidative metabolism since oxygen supply and substrates would be enough for the oxidative metabolism work. Squat exercise = :::i: c -: :II:IIII:III J tf1f'n4* t f i t t 1-_i_ 11 (half value of recovery time) (N r -ID ID I H62 decline s1op Oxydeclineslope I T:fl:::::1cç: /:::v:::::::il:::::::r: IOU BUD Time [Sec.] Figure 2 Typical traces of [Hb], [HbO 2 ] and oxy signal during squat and used parameters Surface EMG data analysis was performed off-line using MATLAB 6.5 (Release 13) software. The power spectrum was derived from the raw EMG signal using the Fast Fourier Transform (FFT) algorithm. The median frequency (MDF) and the mean frequency (MNF) of the power spectrum were computed from the EMG signal with consecutive.5 seconds windows-(non-overlapping). This duration was chosen in order to remain in a wide-sense stationary region of the EMG signal and to get enough data for the analysis in each window. Root mean square (RMS) at each sample is calculated as the root of the average of the sum of square of semg values in the neighborhood of.25 sec (5 samples for 2 Hz sampling rate). From the measurements raw EMG data is examined and RMS, MNF and MDF slopes were obtained. 3. RESULTS The subjects were grouped into two according to the duration of squat exercise they performed as; the subjects maintaining modified squat position longer than five minutes (Group I, three subjects, age 23.3±2.9 years) or shorter than five minutes (Group II, three subjects, age 26.3±1.2 years). Group I and II have body mass index (BMI) with the values of ±2.25 kg/m 2 and 24.9 ±3.29 kg/m 2 respectively (P=.6). As an index of contraction force, EMG amplitude during the initial phase of half chair squat is computes with respect to the value computed in the maximum Proc. of SPIE Vol

5 voluntary contraction protocol. It was obtained as 3.8±2.6% and 31.6±9.5% for group 1 and group 2 respectively (P=.9), hence implying each group was exposed to nearly the same intramuscular pressure and occlusion due to exercise they performed which was aimed at first. Squat duration time difference between groups was statistically significant (394 [sec.] v.s. 213 [sec.], P=.49). In Group 1, mean Hb recovery time (33 [sec.]) was 37.4% less than group 2 (52.7 [sec.]). Mean HbO 2 decline amplitude (2.53 [a.u.] in group 1 and 2.7 [a.u.] in group 2) and oxy decline amplitude (8.4 [a.u.] in group 1 and 3.4 [a.u.] in group 2) in the beginning of squat exercise are found to be 22.6% and 176.9% bigger in group 1. For the EMG parameters, mean slope of MNF and MDF decline are found to be 57.5% and 42.2% bigger in magnitude in group 2 which indicates higher degree of decrement in mean and median frequencies although their mean squat duration time is less. This indicates higher index of fatigue for this group. 5 1 [sec.] Group 6 1 [a.u.] 8 Group Group 1 Group 2 Hb half time (t1/2) Squat time HbO2 decline amplitude OXY decline amplitude 4. DISCUSSION The major findings of this study demonstrate that fnirs parameters may point out higher O2 exctraction capability of muscle in group I which may be related to muscular endurance. It is known that training induces adaptive changes in skeletal muscle, such as increases in oxidative fiber types (type I fibres) which possess a higher capillary density and oxidative potential than type II fibres 14,15. Consistent with the findings of this study Kalliokoski et al. 16 investigated differences in oxygen uptake and blood flow in skeletal muscle between endurance-trained and untrained subjects and found that oxygen extraction fraction was significantly higher in the exercising muscle in athletes. In addition blood transit time in the exercising muscle was longer and perfusion was more homogeneous, which may be associated with enhanced oxygen supply to muscle cells, resulting in improved exercise efficiency in the exercising muscle in the trained subjects. Additionally, augmented the arterio venous O 2 difference as a result of training may contribute to an elevated muscular endurance and delay in fatigue 17. Thomas et al. 18 proved that training status influenced the relationship between blood lactate removal ability and the maximal muscle oxidative capacity associated with the delay in the fatigue. In relation to this particular study, in terms of Hb recovery times, it is seen that more exercising group obviously had the adaptations, which increase with training such as the rise of lactate transporters in the sarcolemmal membrane 19 enhanced capillary density 2 and enhanced mitochondrial content. It has been demonstrated that the rate of O 2 resaturation after exercise is faster in the endurance trained athlete (rowers) than in sedentary controls 2,21. Also it is found that oxygen saturation and the relative value of the effective decrease in muscle oxygenation may be distinctive variables that can be used to characterize muscle oxidative metabolism during human body movement 21. In previous studies it was proved that an improvement in maximal oxygen consumption (VO 2max ) induces by short-term endurance training 17,22. In EMG measurements the increase in RMS amplitude, decrease in MNF and MDF was observed. The MNF decrease and the increase of amplitude in a fatiguing contraction mainly results from a conduction velocity decrease in the muscle fibers due to alteration in the energy metabolism 23. A decrease in the conduction velocity of the muscle fiber causes a shift in the power spectra toward lower frequencies 24. The muscle tissue and the surface electrodes act as low- Proc. of SPIE Vol

6 pass filters of the myoelectric signal 24. Thus more signal energy passes through the tissue when a shift to lower frequencies occurs in the myoelectric power spectrum. This is recorded by surface electrodes as an increase of RMS amplitude 25. Additionally, in Hagberg s study 26 a nonlinear relationship found between RMS amplitude and time during the fatiguing exercises which have also been reported by other investigators. The time constants of the RMS myoelectric amplitude and the MDF were correlated with both the contraction level and the endurance time in the studied exercises 27. The major findings of this study showed that Hb recovery slope, HbO 2 decline slope, HbO 2 amplitude, oxy decline slope, oxy amplitude and recovery time parameters may be used as good predictors for evaluation of muscular performance and endurance. Therefore, the use of NIRS can be beneficial in having information about muscular performance in terms of muscular endurance by assessing levels of tissue oxygenation/deoxygenation trends. Moreover, by means of NIRS measurements used in this study, it is concluded that a longer duration of isometric contraction is related to an increased oxygenation status of the muscle and higher O 2 extraction capability of muscle may be related to muscle endurance. However, investigating solely slopes of surface EMG parameters was found to be improper to evaluate muscular endurance and it is concluded that a more broad investigation of these parameters is required. Yet, EMG measurement provided an objective sight about fatigue occurrence rather than subjective inspection. In addition to the insight derived from this study about muscle O 2 kinetics and influence of training on muscular endurance, investigations using similar exercise protocols can be beneficial which should be performed with more controlled variable such as blood pressure, heart rate, gas exchange cardiac output, blood lactate level measurement. ACKNOWLEDGMENTS This study was supported by the Boğaziçi University Research Fund through projects 4X12D, 4S11 and by Turkish State Planning Organization through projects 3K1225 and 3K1224. The doctoral fellowship for Ömer Şayli provided within the framework of the integrated Ph.D. program sponsored by TUBITAK (The Turkish Scientific & Technological Research Council) is gratefully acknowledged. REFERENCES 1. Macnab, A. J., M.D., FRCPC; Gagnon, Roy E. DTech; Gagnon, Faith A. HBSc. Near Infrared Spectroscopy for Intraoperative Monitoring of the Spinal Cord. Spine., Vol. 27(1), pp. 17-2, January Chance, B., Dait, M. T., Zhang, C., Hamaoka, T., Hagerman, F., Recovery from exercise-induced desaturation in the quadriceps muscles of elite competitive rowers, American Journal of Physiology., Vol. 262, pp. C766-C775, Ferrari, M., Binzoni, T., Uaresima, V., Oxidative metabolism in muscle Phil. Trans. R. Soc. Lond. B., Vol. 352, pp , Kragelj, R., Jarm, T., Erjavec, T., Prešern-Štrukelj, M., Miklav, D., (21), Parameters of postocclusive reactive hyperemia measured by near infrared spectroscopy in patients with peripheral vascular disease and in healthy volunteers, Ann. Biomed. Eng., vol. 29(4), pp Kouzaki, M., Shinohara, M., Masani, K., Tachi, M., Kanehisa, H., Fukunaga, T., Local blood circulation among knee extensor synergists in relation to alternate muscle activity during low-level sustained contraction, J. Appl. Physiol., Vol. 95, pp , Emir, U. E., System Characterization for a Fast Optical Imager, M.S. Thesis, Boğaziçi University, Felici, F., Colace, L., Sbriccoli, P., Surface EMG Modifications After Eccentric Exercise, J. Electromogr. Kinesiol., Vol. 7, no. 3, pp , Merletti, R., Knaflits, M., Luca, D., Myoelectric Manifestations of Fatigue in Voluntary and Electrically Elicited Contractions, J. Appl. Physiol., Vol. 69, no. 5 pp , Solomonow, M., et al., Eloctromyogram Power Spectra Frequencies Associated with Motor Dnit Recruitment Strategies, J. Appl. Physiol., Vol. 68, no. 3, pp , Bilodeau, M., Arsenault, A. B., et al., EMG Power Spectrum of Elbow Extensors, Electromyogr. Clin. Neurophysiol., Vol. 34, no. 3, pp , Kabbara, A. A., Allen, D. G., The use of fluo-5n to measure sarcoplasmic reticulum calcium in single muscle fibre of the cane toad, J. Physiol. (Lond), Vol. 534, pp , Kvist, J., Gillquist, J., Sagittal Plane Knee Translation and Electromyographic Activity During Closed and Open Kinetic Chain Exercises in Anterior Cruciate Ligament-Deficient Patients and Control Subjects, The American Journal of Sports Medicine, Vol. 29, pp , 21. Proc. of SPIE Vol

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