Cardiorespiratory profiling during simulated lunar mission using impedance pneumography

Biomedical Signal Processing and Control 51 (2019) 216–221

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Cardiorespiratory profiling during simulated lunar mission using impedance pneumography a,∗ ´ Marcel Młynczak , Agata Kołodziejczyk b,1 , Hubert Krysztofiak c , a ˙ nski ´ Grzegorz Ambroszkiewicz d , Marek Zyli , Gerard Cybulski a a

Warsaw University of Technology, Department of Mechatronics, Institute of Metrology and Biomedical Engineering, Warsaw, Poland European Space Agency, ESTEC Advanced Concepts Team, Noordwijk, the Netherlands c Polish Academy of Sciences, Department of Applied Physiology, Mossakowski Medical Research Centre, Warsaw, Poland d PIAP Space, Warsaw, Poland b

a r t i c l e

i n f o

Article history: Received 26 September 2018 Received in revised form 23 January 2019 Accepted 24 February 2019 Keywords: Simulated lunar mission Physiology Monitoring Impedance pneumography Cardiorespiratory parameters Analogue astronauts

a b s t r a c t Manned spaceflight requires research in diverse areas, including neuropsychology and human physiology. For these subjects, the Lunares Analog Research Station was established in Pila, Poland. It allows testing of crew members under space-like conditions. One experiment, Lunar Expedition I, was performed on a group of 6 analogue astronauts over 14 days. All were studied for their subjective perception of time and also asked to carry out mission-specific activities, like digging or repairing a rover during an extravehicular activity (EVA). The aims of the study were to measure cardiorespiratory signals using ECG and impedance pneumography devices under those conditions; to evaluate the quality of the data and the level of motion artefacts; and to assess the subjects’ status and adaptation. We used our own prototype, Pneumonitor 2, that enables registering respiratory-related impedance curve, a single-lead ECG and 3-axis accelerometer signals. Due to problems with a detachment of electrodes, we ultimately collected 10 full registrations from 5 astronauts. All signals were pre-processed and annotated. The set of cardiorespiratory parameters, including heart and respiratory activity indicators, was calculated for 3 main states: at rest, doing squats and performing various activities during EVA. We compared the results with normative values collected from elite athletes. The considered parameters were found to be in the normal range, typically slightly worse than the average for the athletes. The physiological responses are in line with expectations. Impedance pneumography enables to measure quantitative parameters of breathing like tidal volume and may be used during dynamic conditions. Combined with the ECG signal provides an objective astronaut’s cardiorespiratory profile. One can use it to assess the adaptation and to plan the schedule of the mission. However, there is a need for development of a wearable electronic textile solution for the target electrodes, to deal with sweating occurring while wearing a three-layer EVA suit. © 2019 Elsevier Ltd. All rights reserved.

1. Introduction Heart activity monitoring is routine practice in many cases, e.g., in sport, fitness or clinical and ambulatory conditions. Thanks to easy access to ECG, pulse oximeters, pulsometers, etc., frameworks enabling beat-by-beat registration and analysis are widely used [1–6]. Heart rate variability (HRV) and RR interval curves are common techniques to evaluate the normative data from healthy participants. They have been utilized in many sport-related situa-

∗ Corresponding author at: 8 Sw. A. Boboli Street, 02-525, Warsaw, Poland. ´ E-mail address: [email protected] (M. Młynczak). 1 Space Garden www.space.garden, www.lunares.space. https://doi.org/10.1016/j.bspc.2019.02.015 1746-8094/© 2019 Elsevier Ltd. All rights reserved.

tions, like quantitative assessment of training load [7], monitoring of futsal players during the preseason to evaluate high vagal activity [8] and analysis of training adaptation [9]. Several parameters were proposed to jointly serve as a convenient biomarker reflecting the state of a subject’s body, to monitor homeostasis, maximize efficiency or avoid over-training [10]. However, separate heart activity parametrization seems insufficient in many cases, especially when one must evaluate the subject under realistic functional conditions, when breathing activity may be uncontrolled, deviated and more chaotic [11]. It is known that the physiological relation between heart rate and breathing is complex. Firstly, inspirations and expirations influence resting ECG by the sinus respiratory arrhythmia phenomenon [12]. On the other hand, cardiorespiratory coupling and baroreflex effects are also observed

M. Mły´ nczak et al. / Biomedical Signal Processing and Control 51 (2019) 216–221

and it is usually understood that heart activity (and even blood pressure) are drivers for breathing [13]. Thus, considering heart action and cardiovascular conditions without respiratory activity appears simplistic and improper in the context of more robust physiological inference, in so-called dynamic situations [14–16]. Therefore, we prepared our own prototype, Pneumonitor 2, to register the tidal-volume-related signal using impedance pneumography (IP), as well as a single-lead ECG and 3-axis accelerometer to allow synchronized analysis of cardiorespiratory relationships along with the activity of the subject [17]. A more detailed description is presented in the Material and Methods section. One of the possible situations referred to above is the simulated lunar mission. In order to test human response (including isolation, loneliness, and life-and-work in a very small space, with conditions analogous to a future base on the Moon), the Lunares Analog Research Station was created in July 2017 in Pila, Poland. It consists of several modules (e.g., biological laboratory, analytical laboratory, hardware warehouse); is connected by a simulated airlock with the interior of the hangar where the lunar surface is simulated and where astronauts may conduct extravehicular activity (EVA). The first experiment, Lunar Expedition I was held in August 2017 (for 14 days), with the Mission Control Centre at the European Space Research and Technology Centre (ESTEC, in Noordwijk, the Netherlands) and 6 astronauts carefully selected due to their psychophysical skills and professional work. The most important experiment was research on the subjective perception of time and the biological clock when completely isolated from sunlight, whose absence which might cause sleep disturbances, changes in circadian rhythm and problems with concentration. Physiological data was also gathered during the mission using Pneumonitor 2. The aims of this pilot study were to measure and evaluate the quality of cardiorespiratory signals before EVA (at rest and during simulated squats), after donning a helmet and while operating; to check the level of motion artefacts; and to assess the subjects’ status and adaptation with comparison to parameters obtained from elite athletes. 2. Materials and methods The study device was Pneumonitor 2 [17]. It enables collection of single-lead ECG signals (primarily with lead 2) alongside IP data (the amplitude and shape of which are linearly related to respiratory activity – tidal volume [18–20]). The IP signal was measured using the tetrapolar method, with the specified electrode configuration, quite similar to that presented by Seppa et al. [21]. Receiving electrodes were placed on the mid-axillary line at about 5th-rib level. Application electrodes were positioned at the same level on the insides of the arms. The sampling frequency for all signals (and for the 3-axis accelerometer) was 250 Hz, sufficient in terms of heart rate variability analysis [22]. Standard Ag/AgCl ECG electrodes were used. The group of 6 healthy astronauts participated in the study. Due to problems with detachment of electrodes (due to sweating or physical activity while wearing the three-layer EVA suits), we ultimately collected 10 full registrations (out of 15 attempts) from 5 astronauts (4 males, 1 female), ages 24-33. All signals were preprocessed (ECG baseline wander was not removed) and annotated according to the schedule (see Table 1). RR intervals were calculated from the R peaks and interpolated using splines to obtain the same number of samples as the original signals. All subjects were asked to carry out mission-specific activities, like digging or repairing a rover during EVA. No calibration of the respiratory-related signals was performed; however, we assume that the shape of the impedance curve is related to the tidal volume, as a linear model appears to be the

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Table 1 The schedule for a particular astronaut. Start Time

Description

Reason

00:00 07:00 12:30

Pneumonitor recording 5 minutes relax 1 minute of holding breath

14:00

1 minute of squats

16:00

EVA

– Rest state establishing Similar to Valsalva manoeuvre for ANS assessment (not included in this study) Adaptation evaluation in dynamic conditions Motion artefact appearances checking

best for electrode configuration [19,21]. A set of cardiorespiratory parameters was estimated for each recording, comprising: • average Heart Rate (HR) – from R peaks found using the PanTompkins algorithm; • Root-Mean-Square Differences in Successive RR intervals (RMSSD) – estimating the vagally mediated changes reflected in HRV; • average Respiratory Rate (RR) – from the established inspiratory onsets; and • Breathing Regularity (BR) – based on the proposed formula in Eq. (1), indicating the deviation of breathing phases timing and tidal volume amplitudes [11]; and all of initial coefficients of type SD/mean.



BR =



100 − 20

+tanh

 (InsV ) InsV

tanh

 (iRR)

+ tanh

iRR

+ tanh

 (ExpV ) ExpV



 (InsT ) InsT [%]

+ tanh

 (ExpT ) ExpT (1)

where: ␴ is the standard deviation of the parameter from brackets, iRR is instantaneous breathing rate (calculated between a pair of inspiratory onsets), InsT is the duration of the inspiration phase, ExpT is the duration of the expiration phase, InsV is the amplitude of the inspiration-phase signal (in Ohms) and ExpV is the amplitude of the expiration-phase signal. Every part of the set was obtained for 3 states: • at rest (initial, static session of free breathing in the supine body position); • doing squats; and • performing EVA (e.g. digging, soldering, repairing a rover, physical activity with a hammer). Estimated parameters were then compared to those obtained from elite athletes near the peak of their performance, ahead of the Rio de Janeiro 2016 Olympic Games; the protocol was described in [11]. Signals were processed and visualised using MATLAB and parameters compared using R. 3. Results As indicated in Table 1 and described in Material and Methods, we gathered ECG, IP and accelerometer (presented later as 3-axis vector, for clarity) signals in three main states: at rest (to establish the relaxed profile), doing squats (to evaluate subject adaptation) and during EVA (to check the level of motion artefacts). Figs. 1–3 present sample signals for those cases, respectively. One can observe a regular, but relatively high, heart rate, along with a slightly chaotic and quick respiratory rhythm at rest (Fig. 1). The adaptation to the activity is well visible in the Fig. 2., when the heart rate peaks during squats and then decreases during the activity and finally returns to the initial level. As conditions were

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Fig. 1. Sample signals from a single astronaut, acquired at rest.

Fig. 2. Sample signals from a single astronaut, acquired during squats.

dynamic then, respiratory activity appeared a bit more regular, as could be expected. Finally, digging during EVA (lasting about 6.5 min) caused 1 motion artefact in the ECG signal and about 15 in the IP signal (still quite reasonable). All the estimated parameters were compared visually with the values obtained for elite athletes, using combined box-and-violin plots. Fig. 4 (left and right part) presents heart activity, and Fig. 5 – respiratory activity parameters. We did not carry out statistical comparisons, firstly because it was not a basic objective of this paper, and furthermore because the number of participants in this pilot study is too low for frequentist and Bayesian approaches.

The heart rates of the astronauts were usually greater than those of the elite athletes. The highest median of heart rates was achieved for squats. RMSSD values, indicating the diversity of heart activity, were at expectable ranges, both for elite athletes and analogue astronauts. Standing body position seems to decrease its value, what is also visible for squat and EVA activities (from the astronauts’ perspective). The average respiratory rates do not reflect the level of activity, are quite invariable; the relation between the increase caused by activity and inhibition coming from greater regularity is not so obvious for astronauts. Finally, breathing regularity, showing indirectly the adaptation of respiratory regulation, was visibly worse for astronauts (all coefficients from Eq. (1) put similar role into the decrease). This could be related to the need to don a three-

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Fig. 3. Sample signals from a single astronaut, acquired during EVA - digging.

Fig. 4. Visual comparison of heart activity parameters; left – heart rate, right – RMSSD.

Fig. 5. Visual comparison of respiratory activity parameters; left – respiratory rate, right – breathing regularity.

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layer EVA suit, distorting the natural ventilation. This probably implies that the suit prevents relaxation and regular ventilation. 4. Discussion In the presented study, we proposed to measure cardiac- and respiratory-related signals in astronauts during a simulated lunar mission. The protocol covered several physiological conditions and allowed estimation of the impact of a three-layer EVA suit on cardiac and respiratory activity. To our knowledge, this is the first work to use ambulatory-type respiratory measurement method (impedance pneumography) during simulated lunar mission, and also to compare cardiorespiratory parameters between elite athletes and astronauts, before and during simulated EVA activities. Despite specific conditions, breathing registration appeared relatively comfortable and of good quality, even during dynamic conditions. The device may capture a long period during the natural functioning of the subjects, without disturbing the breathing space much, like during spirometry testing. The technique utilizing the impedance as a modality of measurement is considered to be much better than breathing belts in terms of estimating quantitative parameters of breathing, like tidal volume. Therefore, high-quality respiration curve, synchronized with the ECG signal, is relevant enough to expand the range of covered physiological aspects. Such dataset makes possible to establish an astronaut’s cardiorespiratory profile, his or her adaptation during a simulated mission (the changes across conditions) and also to analyse the time-independent or temporal causal paths and links (which may supplement the classical time- and frequency-related approaches) [11,23]. All gathered together may become a valuable and impartial input for the mission schedule, even allowing the schedule’s adjustment during the mission. Also, many other applications combining cardiac and respiratory activity were presented, especially considering multi-directionalities of the causal relationships and cardiorespiratory coupling [24–29]; however, they were not performed particularly during more laboratory conditions. Several solutions have been also presented for long-term ECG monitoring recently. One of the problems of ambulatory measurements is the lower quality of the signals. This can be regenerated by various techniques of signal processing, e.g., by using phasedomain multiview dynamic time warping for establishing the instantaneous heart rate [30]. Another issue is the usability of the device. One example is single-arm-worn Holter-type monitor with artificial intelligence [31], or the Apple Watch Series 4, which enables to obtain single-lead ECG signal from wrist [32]. Still, regardless of continuous development, both approaches do not take into account respiratory activity, which may enrich the cardiac-related analysis. Impedance pneumography seems a convenient method in general; furthermore, one can use the same set of electrodes to measure both IP and ECG data. However, during the mentioned conditions, there seems to be the problem with the commonly used Ag/AgCl electrodes. Standard Holter-type ones are intended to operate for 24 h, but not on sweaty skin. According to the reports from the astronauts, there is a need to develop a better electrode interface for impedance pneumography via wearable electronic textiles. This could make measurements even more comfortable while wearing the suit. In fact, we are working on graphene/nanosilver-based electrodes positioned on a T-shirt or a band. The first technical test has already been presented [33] and further study comparing them to the reference methods is planned in a near future. Several limitations need to be mentioned. Foremost, due to the small number of measurement sessions completed (without electrode detachments), no reproducibility analysis was conducted. Also, as the main objective of the mission was the analysis of time

perception and the schedule was crowded, it was not possible to repeat similar procedures many times. The parametrization of the signals was carried out on data which was not fully curated against motion artefacts (particularly present during EVA), which may affect the obtained results. The participants were not studied outside the hangar, so the direct assessment of the impact of “being inside the hangar” and donning a three-layer EVA suit cannot be established. Therefore, the role of this study was rather preliminary and illustrative. 5. Conclusions Physiology research is as essential for manned spaceflight as for sports medicine or fitness. In all these applications, the relationships are analysed in healthy subjects and the inference must determine the subjects’ profiles, based on signal trend, complexity or adaptation to changing conditions. The Lunar Expedition I experiment, performed at the Lunares Analog Research Station on a group of 6 analogue astronauts, collected ECG, impedance pneumography and 3-axis accelerometer signals using our prototype, Pneumonitor 2. The quality of the data gathered before and during EVA, while wearing a three-layer EVA suit, is relevant to assess the subjects’ cardiorespiratory statuses, which comprise average heart and respiratory rates values, RMSSD and recently proposed breathing regularity parameter. The considered cardiac and respiratory parameters were found to be in the normal range, typically slightly worse than the average for elite athletes. The physiological responses are in line with expectations. The fact that impedance pneumography can measure both temporal- (respiratory rate) and amplitude-specific parameters (tidal volume and air-flows) distinguishes this method from other ambulatory ones. Extending the information with the ECG analysis delivers the objective cardiorespiratory profile, that may be utilized as input information for mission scheduling and monitoring. However, better electrode attachment, resistant to sweating or physical activity, is necessary for use in further missions. Conflicts of interests The authors declare that there is no conflict of interest regarding the publication of this paper. Acknowledgements Special thanks are given to the entire Lunares team (www. lunares.space) for establishing the experimental procedures and including them in the mission schedule; to the astronauts, who agreed to undergo recordings during the simulated lunar mission; and to Space Garden (www.space.garden) for approval and support related to the realization of this project inside the Lunares Analog Research Station. We also thank Martin Berka for linguistic adjustments. References [1] M. Buchheit, Monitoring training status with HR measures: do all roads lead to Rome? Front. Physiol. 5 (73) (2014). [2] L. Schmitt, J. Regnard, G.P. Millet, Monitoring fatigue status with HRV measures in elite athletes: an avenue beyond RMSSD? Front. Physiol. 6 (343) (2015). [3] P. Duking, A. Hotho, H.-C. Holmberg, F.K. Fuss, B. Sperlich, Comparison of non-invasive individual monitoring of the training and health of athletes with commercially available wearable technologies, Front. Physiol. 7 (71) (2016). [4] D. Giles, N. Draper, W. Neil, Validity of the polar V800 heart rate monitor to measure RR intervals at rest, Eur. J. Appl. Physiol. 116 (2016) 563–571. [5] C.R. Bellenger, J.T. Fuller, R.L. Thomson, K. Davison, E.Y. Robertson, J.D. Buckley, Monitoring athletic training status through autonomic heart rate regulation: a systematic review and meta-analysis, Sports Med. 46 (2016) 1461–1486.

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´ Marcel Młynczak, PhD, completed (2014) a master degree in Biomedical Engineering at the Faculty of Mechatronics, Warsaw University of Technology, Poland; he defended (2018) his doctoral thesis in Biocybernetics and Biomedical Engineering there, both regarding noninvasive cardiorespiratory measurements and related signal analysis. Now, he is engaged as Assistant Professor in the same Faculty and with MedTech projects comprising sleep-disordered breathing diagnostics and obstetric anal sphincter injury syndrome screening. His other research interests include wearable systems, mHealth, and data science for applications in clinical research. Agata Kołodziejczyk, PhD, Neuroscientist and astrobiologist. Both her master thesis at Jagiellonian University in Kraków, as well as doctoral thesis at Stockholm University concerned the influence of light on nervous systems. After PhD, she worked on neurobiological mechanisms of aggression, then got a postdoc in biomimetics at the European Space Agency in Advanced Concepts Team. She developed a prototype of lighting system to synchronize biological clocks. Initiator and co-founder of analogue space research station in Poland called Lunares. She organized Lunar and Martian analogue missions. Currently, she develops the Analogue Astronaut Training Centre to accelerate human spaceflight studies. Hubert Krysztofiak MD, PhD, head of the National Centre for Sports Medicine in Warsaw and a researcher at the Department of Applied Physiology, Mossakowski Medical Research Centre, Polish Academy of Sciences. The main area of scientific activity: exercise physiology, cardiovascular and pulmonary adaptation to exercise and clinical approach to cardiac and pulmonary pathology in athletes. The Chairmen of the Medical Commission of the Polish Olympic Committee and the Chief Medical Officer for the Polish Olympic Team. A member of the Advisory Board of the International Olympic Committee Diploma program in Sport Medicine. Grzegorz Ambroszkiewicz, MSc in Biomedical Engineering from Warsaw University of Technology. He was involved in PW-SAT2 student satellite project where he was responsible for Sun Sensor development. He worked as Mechanical Engineer at Space Research Centre of the Polish Academy of Sciences and participated in two European Space Agency’s projects: PROBA-3 Solar Coronagraph and JUICE Jupiter Icy Moons Explorer. Currently he is Technical Leader and Systems Engineer at PIAP Space where he designs systems for on-orbit satellite servicing and planetary projects. He was also Analog Astronaut in Lunar Simulation in Lunares Habitat. ˙ nski ´ Marek Zyli received the B.S. and M.S. degrees, both in biomedical engineering, from Warsaw University of Technology, Poland, where he is currently working toward the Ph.D. degree. His current research interests include noninvasive cardiac output measurement during autonomic nervous system tests.

Gerard Cybulski received MSc in electronic medical equipment (in 1984) from the Warsaw University of Technology. In 1990, he defended Ph.D. thesis on the transient changes of central hemodynamic in response to the orthostatic manoeuvre. During his postdoctoral training (1991–1993) at the Centre for Biological and Medical Systems, Imperial College, London, he worked on the measurement of arterial distensibility using MRI. Since 2009 he is the Associate Professor at Department of Mechatronics of Warsaw University of Technology working on development and applications of impedance methods in ambulatory monitoring of cardiovascular, respiratory and autonomic system analysis.