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DE GRUYTER Current Directions in Biomedical Engineering 2022;8(3): 21-24 Marie Ostermeier* and Martin Schmoll Exploring methods for targeted activation of the sympathetic nervous system without exercise Finding solutions to enhance FES-cycling performance for individuals with SCI https://doi.org/10.1515/cdbme-2022-2006 Keywords: FES-cycling, heart rate, sympathetic nervous system, stress reaction, cold pressor test, Capsaicin, hot Abstract: When using functional electrical stimulation water immersion test, Wim Hof method, virtual reality (FES) for cycling in individuals with spinal cord injury (SCI) during FES-cycling, a rapid onset of muscular fatigue can be observed. Among other reasons, missing neural 1 Introduction feedback from the lower extremities might be responsible for a reduced sympathetic response during stimulation. Functional electrical stimulation (FES) is often used to train Therefore, this project explores different methods to paralysed muscles in individuals with spinal cord injury activate the sympathetic nervous system to increase the (SCI). The technique allows to regain certain strength and heart rate to allow better blood circulation and oxygenation functionality, even though patients are unable to in the working muscles. Six techniques were selected to be voluntarily contract affected muscles or feel any sensory tested on 10 healthy participants in the context of pilot stimuli. After a dedicated training of the muscles, some measurements. Those were the cold pressor test with both patients are eligible for advanced training modalities such hands, a virtual reality rollercoaster ride, the hot water as FES-Cycling on an instrumented trike. Besides the immersion test with two hands, the Wim Hof breathing maximal power output, a rapid onset of muscular fatigue method, the Valsalva manoeuvre and the ingestion of remains an open challenge in any functional application of Capsaicin through Prik Jinda chilli peppers. The results FES. This might be linked to a rather crude motor-control showed a significant increase in average as well as peak and missing neural feedback leading to an inappropriate heart rate during all methods performed. From baselines of response of the cardiovascular system not fully around 68±1.3 bpm, the strongest increases in both compensating for the increased blood oxygen. ,  A parameters were found for the Valsalva manoeuvre (to potential solution to that problem is the targeted activation 118±20.9 bpm peak, 91±14.2 bpm average), the Wim Hof of the sympathetic nervous system (SNS) to enhance blood breathing method (to 112±13.5 bpm peak, 86±11.8 bpm circulation and therefore oxygen supply in the muscles. average) and Capsaicin ingestion (to 103±18.9 bpm peak, Existing studies that already present methods to increase 80±16.7 bpm average). The methods as they were the heart rate, which is an indicator for an increased SNS performed in this project, are not all directly applicable to activity, were evaluated and the strategies adapted or FES-Cycling but rather serve as exploration how efficiently replicated, while analysing the heart rate of the subjects. which stimuli can increase the heart rate. In future research, In previous studies, an increased heart rate (HR) has adaptation or combination of techniques might help to been used as a marker to assess the activity of the SNS – increase performance during FES-Cycling. . A popular breathing technique known as the Wim Hof method (WHM), is composed of phases of hyperventilation and breath holds to increase the heart rate to well over 100 ______ bpm compared to a resting heart rate of about 60 bpm. The *Corresponding author: Marie Ostermeier: UAS Technikum heart rate is mainly elevated during hyperventilation Wien, Vienna, Austria; and Center for Medical Physics and phases.  Another method related to breathing is the Biomedical Engineering, Medical University of Vienna, Vienna, Valsalva manoeuvre, which induces complex effects in Austria, e-mail: email@example.com Martin Schmoll: Center for Medical Physics and Biomedical heart rate and blood pressure. Through a strong build-up of Engineering, Medical University of Vienna, Vienna, Austria Open Access. © 2022 The Author(s), published by De Gruyter. This work is licensed under the Creative Commons Attribution 4.0 International License. 21 pressure in the airways a previous study reported an up to 2.2 Preliminary measurements 44 bpm increase in HR . Other techniques such as the Prior to the pilot experiments, the author herself thoroughly cold pressor test (CPT) and hot water immersion test (HIT) explored various existing methods (CPT, HIT, WHM, are typically performed by putting one hand in water with CAP, VM, VR, whole body heat stress in an infrared heat temperatures of 0 – 4 °C and 46 – 48 °C, respectively. chamber, musical stimuli, creepy scenarios and caffeine When immersed in such extreme tempered water, thermo- ingestion) during preliminary measurements. Based on the sensors in the skin recognize the demand to regulate the outcome of these measurements, previous achievements skin temperature and blood circulation, while pain found in literature and necessary equipment, six methods receptors are responsible for the additional stress. While the were selected to be further investigated in pilot CPT showed relatively small peak increases in heart rate of measurements. maximum 16 bpm , whole body heat stress can cause the HR go up to 130 bpm compared to a baseline of 82 bpm . Further, virtual reality (VR) immersion seems to 2.3 Pilot measurements increase heart rate especially in individuals susceptible to motion sickness or when having other negative experiences with VR . Motion sickness itself has also proven to 2.3.1 Participants increase heart rate  and therefore might be the main cause to elevate HR, since during VR a mismatch between 10 healthy participants (8 male, 2 female) were voluntarily visual and vestibular information exists . When taking part in the pilot measurements. They received a Capsaicin containing substances are ingested, Capsaicin thorough explanation of all processes and potential side binds to the receptor Transient Receptor Potential Vanilloid effects. Everyone gave their informed written consent 1 (TRPV1), usually activated by painful stimuli . before start of the measurements. Table 1 shows the subject Therefore, the central nervous system is receiving a demographics of the participants of the pilot measurements. nociceptive stimulus, causing the SNS to be activated . The aim of our project was to explore and compare Table 1: Subject demographics of the 10 subjects (8 male, different strategies for increasing the sympathetic activity 2 female) taking part in the pilot measurements without exercise, by analysing the heart rate of a group of healthy volunteers. These pilot measurements are intended Age [years] Height [cm] Weight [kg] to serve as basis for future measurements in the SCI Mean ± SD 26.3 ± 3.9 179.2 ± 11.5 73.7 ± 12.3 population with the goal of increasing the performance during FES-Cycling. 2.3.2 Measurement protocol All measurements were performed in the Vienna general 2 Materials and Methods hospital at the Centre for Medical Physics and Biomedical Engineering of the Medical University of Vienna. The total time required for all procedures was about 2.5 h. After 2.1 Measurement equipment detailed information, the ECG electrodes were placed and To determine the heart rate, an ECG was recorded. Three the measurement devices tested. All tests were performed Ag/AgCl surface electrodes (Skintact, Leonhard Lang in the trike (ICE VTX, ICE, Cornwall, United Kingdom) to GmbH, Innsbruck, Austria) were placed on the skin in a simulate the position during FES-Cycling. Before each lead II configuration. A bio signal amplifier (Bio Amp stressor was applied, a baseline measurement at rest was FE231, ADInstruments Inc, Colorado Springs, USA) done for 3 min. After every procedure, the participant was recorded the data, which was received by a Powerlab given a few minutes to rest in order to minimize influences (Powerlab 16/35, ADInstruments Inc, Colorado Springs, from the previous method. Test 1 (CPT): The cold pressor USA). The digital signal was transferred to a PC so that in test was carried out two hands immersed in 0 °C water for the LabChart 8.0 software (ADInstruments Inc, Colorado 5 min, or as long as tolerable for the participant. Test 2 Springs, USA) the data could be analysed in real-time. (VR): The subjects experienced three rounds on a virtual tropical island rollercoaster (“Epic Roller Coasters”, B4T Games) through the VR headset “Oculus Go” (Facebook 22 technologies, Menlo Park, CA, United States) and 3 Results headphones. Test 3 (HIT): The hot water immersion test was conducted the same way as the CPT, only the water Two subjects tolerated the 0 °C water in the CPT for only had a temperature of 48 °C. Test 4 (WHM): The Wim Hof 1 min and one person endured the HIT for only 1 min. method was executed guided by the interactive training in Further, one participant endured the chilli chewing for only the WHM app (Innerfire B.V., Stroe, Netherlands). For 35 1 min instead of 2 min. One subject was not able to do the breaths, it was necessary to inhale as deeply as possible, Capsaicin ingestion at all, due to a wound on the lip. followed by exhaling passively. This is called Figure 1 presents the mean values of average, peak and hyperventilation phase, which is followed by the retention baseline heart rate for all the performed tests. phase, where the breath is held after fully exhaling. In a Mean values of average, peak and baseline heart rate third phase, one single deep breath is held for 15 s before for every stressor the first phase starts again. In total, three cycles of the method were performed. Test 5 (VM): The Valsalva manoeuvre begins by taking one deep inhale. After closing mouth and nose, the participant strongly presses the * * enclosed air against the hands to create pressure, which is held for 15 – 20 s. Test 6 (CAP): To realize the ingestion of Capsaicin, a teaspoon of chopped up fresh Prik Jinda peppers (75 000 Scoville Heat Units ) was chewed for 2 min or as long as tolerable. Swallowing was not recommended and after spitting out the chilli, measurement continued for 8 mins to record aftereffects. CPT VR HIT WHM VM CAP baseline average peak Figure 1: Values (mean ± SD) of all participants are displayed for 2.3.3 Data analysis average heart rate at rest (baseline, grey), average heartrate during stressor (blue), peak heart rate during stressor (red). Stressors: CPT = cold pressor test, VR = Virtual reality, HIT = The LabChart 8.0 software allows visualization and Hot water immersion test, WHM = Wim Hof method, VM = analysis of the received data. By applying an automatic R- Valsalva maneouvre, CAP = Capsaicin ingestion, ‘*’ marks peak detection algorithm to the ECG data, the heart rate values significantly different from the previous baseline value was calculated and presented in real-time. The HR data was The VM showed the highest increase in peak heart rate imported into MATLAB (R2021b, The MathWorks Inc., (118±20.9 bpm), followed by the WHM (112±13.5 bpm), Natick, MA, USA), where the mean and peak HR values of CAP (103±18.9 bpm), CPT (100±16.1 bpm), HIT (98±9.6 the baseline measurements and the methods are computed. bpm) and lastly VR immersion (92±15.4 bpm). Throughout the entire duration of applying the stressor, the HR was increased to an average of 91±14.2 bpm in the VM, 2.3.4 Statistical analysis 86±11.8 bpm in the WHM, 80±16.7 bpm during CAP, 80±10.1 bpm during the HIT, 76±14.3 bpm during the CPT It was not possible to demonstrate normal distribution in all and 73±14.1 bpm in the VR experience. Therefore, almost tests by using the Shapiro-Wilk test. Thus, the Wilcoxon- the same order was found for the average and peak HR signed-rank-test was conducted with a significance level of values, only the HIT had a higher average heart rate than α = 0.05 to test the hypothesis that there is a difference the CPT. For all methods, average as well as peak values between the applied method and their respective baseline were significantly different from the respective baseline at measurement. The data of the baseline measurements was α = 0.05. Comparing the baselines of the individual found to be normally distributed by using the Shapiro-Wilk stressors did not reveal a significant difference. test, so that a one way repeated measures ANOVA was performed to test the hypothesis that the baselines are not different from each other. 4 Discussion The Valsalva manoeuvre achieved the highest heart rates but its effect was only short-term. While the VM with its Heart rate [bpm]  E. H. Estigoni, C. Fornusek, R. M. Smith, and G. M. short duration can elevate the heart rate for about a minute, Davis, “Evoked EMG and Muscle Fatigue During the hyperventilation phase of the WHM could be performed Isokinetic FES-Cycling in Individuals With SCI,” for much longer, creating a long-lasting elevation of the Neuromodulation: Technology at the Neural Interface, heart rate. Thinking about the application in FES-Cycling, vol. 14, no. 4, pp. 349–355, Aug. 2011, doi: the WHM could probably be adapted so that the breath hold 10.1111/j.1525-1403.2011.00354.x. phases are left out, since they let the heart rate decrease and  M. Kox et al., “Voluntary activation of the sympathetic don’t oxygenate the blood. nervous system and attenuation of the innate immune The result that the peak HR is higher during the CPT response in humans,” Proc Natl Acad Sci U S A, vol. 111, than the HIT, but for the average HR the HIT reached a no. 20, pp. 7379–7384, May 2014, doi: higher value than the CPT, suggests that the cold water 10.1073/pnas.1322174111. induces a slightly higher pain stimulus than hot water. This  B. D. Johnson, J. R. Sackett, Z. J. Schlader, and J. J. was confirmed by the subjective feeling of the participant. Leddy, “Attenuated Cardiovascular Responses to the Cold Pressor Test in Concussed Collegiate Athletes,” J Over the course of the CPT, the heart rate tended to Athl Train, vol. 55, no. 2, pp. 124–131, Feb. 2020, doi: decrease after the initial peak response while it increased or 10.4085/1062-6050-573-18. remained rather stable during the HIT. This might explain  M. Iguchi, A. E. Littmann, S.-H. Chang, L. A. Wester, J. the higher values in average heart rate. The rising tendency S. Knipper, and R. K. Shields, “Heat Stress and of the heart rate during whole body heat exposure could be Cardiovascular, Hormonal, and Heat Shock Proteins in confirmed in preliminary tests using an infrared heat Humans,” J Athl Train, vol. 47, no. 2, pp. 184–190, 2012. chamber. Those measurements were going on for up to an  V. Minatel et al., “Maximal expiratory pressure and hour or longer, which would not have been feasible in the Valsalva manoeuvre do not produce similar pilot testing. For Virtual reality it was observed that cardiovascular responses in healthy men,” Experimental especially in subjects that reported motion sickness and Physiology, vol. 101, no. 5, pp. 599–611, 2016, doi: nausea, or even ended the test early, the heart rate was 10.1113/EP085203. increased while other subjects appeared completely relaxed  K. A. Fadeev, A. S. Smirnov, O. P. Zhigalova, P. S. Bazhina, A. V. Tumialis, and K. S. Golokhvast, “Too Real and showed only little rise in heart rate. Thus, the increase to Be Virtual: Autonomic and EEG Responses to in HR might depend a lot on the subjective susceptibility to Extreme Stress Scenarios in Virtual Reality,” Behav motion sickness or other factors like fear of hight. Neurol, vol. 2020, p. 5758038, Mar. 2020, doi: The results of these pilot experiments demonstrate 10.1155/2020/5758038. clear beneficial effects for the investigated breathing  J. Dahlman, A. Sjörs, J. Lindström, T. Ledin, and T. methods. A combination of performing the WHM and the Falkmer, “Performance and Autonomic Responses VM in alternation might be able to effectively increase During Motion Sickness,” Hum Factors, vol. 51, no. 1, pp. heart rate and muscular oxygenation, potentially useful to 56–66, Feb. 2009, doi: 10.1177/0018720809332848. achieve higher performances in FES-Cycling  S. 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Current Directions in Biomedical Engineering – de Gruyter
Published: Sep 1, 2022
Keywords: FES-cycling; heart rate; sympathetic nervous system; stress reaction; cold pressor test; Capsaicin; hot water immersion test; Wim Hof method; virtual reality
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