Physiological Challenges of Space Travel and Ground-Based Simulation Possibilities for Monitoring Brain Circulatory Changes: A Rheoencephalography Study
Copyright (c) 2024 Szabó Sándor, Bodó Michael, Nagy-Bozsoky József, Pintér István, Bagány Mihály, Kora Szilvia, Dunai Pál
This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.
Abstract
The functional integrity of brain perfusion and oxygen transport profoundly determines mental performance during military flight missions and spaceflight. Presently, at the selection phase of pilot candidates, there are no screening methods to evaluate cerebral circulation and its autonomous regulation (AR), meanwhile the pilot information processing capacity could be insufficient in dangerous flight situations with high mental workload or during high “head-to-foot” G loads. On-board ISS (International Space Station) and during deep-space missions circulatory changes can be evolved in the opposite direction due to the microgravity: blood shift toward the head-neck region can increase ICP (Intracranial Pressure) and tenfold increase of carbon-dioxide concentration can provoke complaints and disturbances in eye and brain blood circulation (Space Associated Neuro-Ocular Syndrome – SANS). The alteration of brain perfusion dynamics and oxygen utilisation was investigated on the head-down tilting table (HDT) test and in the hypobaric (low-pressure) chamber. We registered the brain regional pulse wave changes by the bioimpedance (Rheoencephalography – REG) on 19 volunteers in rest and after the breath-holding manoeuvre. We found that during the head-down tilt (HDT) position, the amplitude of the second peak of the REG pulse wave increased, like the ICP pulse wave, being an unfavourable sign for intracranial pressure increase in clinical cases. Manual readings resulted in significant differences during HDT between the female (P = 0.0007) and male (P < 0.0001) groups. With automated analysis, the increase in REG P2 wave was significant, and the ratio was 4/5 (80%) for women and 10/14 (71%) for men. The newly written automatic program script was able to detect this in 92% of the cases. The calculated values detected the state of cerebral circulatory autoregulation and the identity between the male and female groups. Based on this result and previous REG correlation studies, it can be concluded that REG could be used to monitor fighter pilots, astronauts, and neurocritical care patients in real-time as emergency alert in the transitory cessation of brain perfusion.
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Z. Dudás, ‘Interpretations of Human Error in Aviation’. Repüléstudományi Közlemények, Vol. 33, no. 1, pp. 49–57. 2021. Online: https://doi.org/10.32560/rk.2021.1.5
G. G. Cable, ‘In-Flight Hypoxia Incidents in Military Aircraft: Causes and Implications for Training’. Aviation Space and Environmental Medicine, Vol. 74, no. 2, pp. 169–172. 2003.
J. J. Elliott, D.R. Schmitt, ‘Unexplained Physiological Episodes. A Pilot’s Perspective’. Air & Space Power Journal, Vol. 33, no. 3, pp. 15–32. 2019.
E. G. Damato, et al., ‘Neurovascular and Cortical Responses to Hyperoxia: Enhanced Cognition and Electroencephalographic Activity despite Reduced Perfusion’. The Journal of Physiology, Vol. 598, no. 18, pp. 3941–3956. 2020. Online: https://doi.org/10.1113/JP279453
D. M. Shaw, et al., ‘Recovery from Acute Hypoxia: A Systematic Review of Cognitive and Physiological Responses during the 'Hypoxia Hangover'’. PLoS One, Vol. 18, no. 8, pp. e0289716. 2023. Online: https://doi.org/10.1371/journal.pone.0289716
CanaryTM Pilot physiological monitoring system. Elbit Systems Ltd. Haifa, Israel. Online: https://www.elbitsystems-uk.com/what-we-do/air-space/aircraft-systems/helmet-mounted-displays
Szabó, S. A. et al., ‘Az oxigéndeficit repülésbiztonsági jelentősége és lehetséges magyarázata agyi pulzoximetria NIRS eredményei alapján, szimulált repülési stresszhelyzetben’. in Repüléstudományi tanulmányok, Eds., L. Szilvássy, B. Békési, Budapest, Ludovika, pp. 11–42. 2020.
K. Domján, G. Vada, ‘Katonai pilóták élettani paramétereinek monitorozása szimulált repülési körülmények között’. Haditechnika, Vol. 2020, no. 3. Online: https://doi.org/10.23713/HT.54.3.01
R. SETLOW, ‘The Hazards of Space Travel’. EMBO Reports, Vol. 4, no. 11, pp. 1013–1016. 2003. Online: https://doi.org/10.1038/sj.embor.7400016
A. G. Lee et al., ‘Space Flight-Associated Neuro-Ocular Syndrome (SANS)’. Eye, Vol. 32, no. 7, pp. 1164–1167. 2018. Online: https://doi.org/10.1038/s41433-018-0070-y
Y. Martin Paez, L. I. Mudie, P. S. Subramanian, ‘Spaceflight Associated Neuro-Ocular Syndrome (SANS): A Systematic Review and Future Directions’. Eye and Brain, Vol. 19, no. 12, pp. 105–117. 2020. Online: https://doi.org/10.2147/EB.S234076
J. Ong, A. et al., ‘Neuro-Ophthalmic Imaging and Visual Assessment Technology for Spaceflight Associated Neuro-Ocular Syndrome (SANS)’. Survey of Ophthalmology, Vol. 67, no. 5, pp. 1443–1466. 2022. Online: https://doi.org/10.1016/j.survophthal.2022.04.004
K. Marshall-Goebel, R. Damani, E. M. Bershad, ‘Brain Physiological Response and Adaptation during Spaceflight’. Neurosurgery, Vol. 85, no. 5, pp. E815–E821. 2019. Online: https://doi.org/10.1093/neuros/nyz203
A. P. Michael, K. Marshall-Bowman, ‘Spaceflight-Induced Intracranial Hypertension’. Aerospace Medicine and Human Performance, Vol. 86, no. 6, pp. 557–562. 2015. Online: https://doi.org/10.3357/AMHP.4284.2015
L. F. Zhang, A. R. Hargens, ‘Spaceflight-Induced Intracranial Hypertension and Visual Impairment: Pathophysiology and Countermeasures’. Physiological Reviews, Vol. 98, no. 1, pp. 59–87. 2018. Online: https://doi.org/10.1152/physrev.00017.2016
P. Liu, J. B. De Vis, H. Lu, ‘Cerebrovascular Reactivity (CVR) MRI with CO2 Challenge: A Technical Review’. NeuroImage, Vol. 15, no. 187, pp. 104–115. 2019. Online: https://doi.org/10.1016/j.neuroimage.2018.03.047
J. Law et al. ‘Relationship between Carbon Dioxide Levels and Reported Headaches on the International Space Station’. Journal of Occupational and Environmental Medicine, Vol. 56, no. 5, pp. 477–483. 2014. Online: https://doi.org/10.1097/JOM.0000000000000158
K. A. Zuj et al. ‘Impaired Cerebrovascular Autoregulation and Reduced CO₂ Reactivity after Long-Duration Spaceflight’. American Journal of Physiology- Heart and Circulatory Physiology, Vol. 302, no. 12, pp. 2592–2598. 2012. Online: https://doi.org/10.1152/ajpheart.00029.2012
M. Boerma, et al. ‘Space Radiation and Cardiovascular Disease Risk.’ World Journal of Cardiology, Vol. 26, no. 7(12), pp. 882–888. 2015. Online: https://doi.org/10.4330/wjc.v7.i12.882
A. F. Sagirov et al. ‘Postural Influence on Intracranial Fluid Dynamics: An Overview’. Journal of Physiological Anthropology, Vol. 13, no. 42, pp. 3013. 2023. Online: https://doi.org/10.1186/s40101-023-00323-6
M. Kermorgant et al., ‘Impacts of Microgravity Analogs to Spaceflight on Cerebral Autoregulation’. Frontiers in Physiology, Vol. 3, no. 11, pp. 778. 2020. Online: https://doi.org/10.3389/fphys.2020.00778
M. Czosnyka, et al., ‘Monitoring of Cerebrovascular Autoregulation: Facts, Myths, and Missing Links.’ Neurocrit Care. Vol. 10, no. 3, pp. 373–386. 2009. Online: https://doi.org/10.1007/s12028-008-9175-7
M. Rubin et al., ‘Noninvasive Monitoring’. in Neurotrauma and Critical Care of the Brain, Eds., J. Jallo, C. M. Loftus, New York, Thieme, 2009, p. 53
University of Cambridge, ICM+. Online: https://icmplus.neurosurg.cam.ac.uk/
J. Donnelly, M. J. Aries, M. Czosnyka, ‘Further Understanding of Cerebral Autoregulation at the Bedside: Possible Implications for Future Therapy’. Expert Review of Neurotherapeutics, Vol. 15, no. 2, pp. 169–185. 2015. Online: https://doi.org/10.1586/14737175.2015.996552
S. Brasil, ‘Intracranial Pressure Pulse Morphology: the Missing Link?’ Intensive Care Medicine, Vol. 48, no. 11, pp. 1667–1669. 2022. Online: https://doi.org/10.1007/s00134-022-06855-2
M. Harary, R. G. F. Dolmans, W. B. Gormley, ‘Intracranial Pressure Monitoring – Review and Avenues for Development’. Sensors, Vol. 18, no. 2, pp. 1–15. 2018. Online: https://doi.org/10.3390/s18020465
M. Czosnyka, Z. Czosnyka, ‘Origin of Intracranial Pressure Pulse Waveform.’ Acta Neurochirurgica, Vol. 162, pp. 1815–1817. 2020. Online: https://doi.org/10.1007/s00701-020-04424-4
T. Ellis, J. McNames, M. Aboy, ‘Pulse Morphology Visualization and Analysis with Applications in Cardiovascular Pressure Signals’. IEEE Transactions on Biomedical Engineering, Vol. 54, no. 9, pp. 1552–1559. 2007. Online: https://doi.org/10.1109/TBME.2007.892918
G. Cucciolini, V. Motroni, M. Czosnyka, ‘Intracranial Pressure for Clinicians: It Is Not Just a Number’. Journal of Anesthesia, Analgesia and Critical Care, Vol. 3, no. 31, 2023. Online: https://doi.org/10.1186/s44158-023-00115-5
M. Kasprowicz, et al., ‘Pattern Recognition of Overnight Intracranial Pressure Slow Waves Using Morphological Features of Intracranial Pressure Pulse’. Journal of Neuroscience Methods, Vol. 190, no. 2, pp. 310–318. 2010. Online: https://doi.org/10.1016/j.jneumeth.2010.05.015
C. Mataczyński, A. et al., ‘End-to-End Automatic Morphological Classification of Intracranial Pressure Pulse Waveforms Using Deep Learning’. IEEE Journal of Biomedical and Health Informatics, 2022 Vol. 26, no. 2, pp. 494–504. 2022. Online: https://doi.org/10.1109/JBHI.2021.3088629
Code of Federal Regulations, Rheoencephalograph (a) Identification Code of Federal Regulations Title 21, vol 8, Sec 882. 1825. Online: https://www.ecfr.gov/current/title-21/chapter-I/subchapter-H/part-882/subpart-B/section-882.1825
F. L. Jenkner, Clinical Rheoencephalography: A Non-Invasive Method for Automatic Evaluation of Cerebral Hemodynamics. Vienna, Ertldruck, 1986.
M. Bodó et al., ‘Prevalence of Stroke/Cardiovascular Risk Factors in Rural Hungary – A Cross-Sectional Descriptive Study’. Ideggyógyászati Sz. Vol. 61, no. 3–4, pp. 87–96. 2008. Online: https://doi.org/10.1088/1742-6596/224/1/012115
M. Bodó, F. J. Pearce, L. Baranyi, R.A. Armonda, ‘Changes in the Intracranial Rheoencephalogram at Lower Limit of Cerebral Blood Flow Autoregulation’. Physiological Measurement, Vol. 26, no. 2, pp. S1–17. 2005. Online: https://doi.org/10.1088/0967-3334/26/2/001
M. Bodó et al., ‘Measurement of Cerebral Blood Flow Autoregulation with Rheoencephalography: A Comparative Pig Study’. Journal of Electrical Bioimpedance, Vol. 9, no. 1, pp. 123–132. 2018. Online: https://doi.org/10.2478/joeb-2018-0017
M. Bodó et al., ‘Rheoencephalographic Changes during Increased Intracranial Pressure’. in Pharmacology of Cerebral Ischemia. Ed., J. Krieglstein, Amsterdam, Elsevier, pp. 265–269. 1986.
M. Bodó et al., ‘Influence of Volume and Change on the Electrical Impedance Signal (In Vitro)’. Journal of Physics: Conference Series, Vol. 22, 012111. 2010. Online: https://doi.org/10.1088/1742-6596/224/1/012111
M. Bodó et al., ‘Correlation of Rheoencephalography and Laser Doppler Flow: A Rat Study’. Journal of Electrical Bioimpedance, Vol. 7, no. 1, pp. 55–58. 2016. Online: https://doi.org/10.5617/jeb.2985
K. M. Brady et al., ‘Monitoring Cerebrovascular Pressure Reactivity with Rheoencephalography’. Journal of Physics: Conference Series, Vol. 224, 012089. 2010. Online: https://doi.org/10.1088/1742-6596/224/1/012089
L. A. Cannizzaro et al., ‘Noninvasive Neuromonitoring with Rheoencephalography: A Case Report’. Journal of Clinical Monitoring and Computing, Vol. 37, no. 5, pp. 1413–1422. 2023. Online: https://doi.org/10.1007/s10877-023-00985-8
L. Baranyi et al., ‘DataLyser Program’. Online: https://doi.org/10.13140/RG.2.2.21169.25442
B. Hjorth, ‘The Physical Significance of Time Domain Descriptors in EEG Analysis’. Electroencephalography and Clinical Neurophysiology, Vol. 34, no. 3, pp. 321–325. 1973. Online: https://doi.org/10.1016/0013-4694(73)90260-5
J. N. Acharya et al., ‘Guideline 2: Guidelines for Standard Electrode Position Nomenclature’. Journal of Clinical Neurophysiology, Vol. 33, no. 4, pp. 308–311. Online: https://doi.org/10.1097/WNP.0000000000000316
C. Zweifel, C. Dias, P. Smielewski, M. Czosnyka, ‘Continuous Time-Domain Monitoring of Cerebral Autoregulation in Neurocritical Care’. Medical Engineering and Physics, Vol. 36, no. 5, pp. 638–645. 2014. Online: https://doi.org/10.1016/j.medengphy.2014.03.002
MATLAB Mathworks, Natick, MA. Online: https://www.mathworks.com/products/new_products/ latest_features.html
Wikipedia, SBD Dauntless. Online: https://en.wikipedia.org/wiki/Douglas_SBD_Dauntless
World War II Aviation, SBD Dauntless dive bomber – a pilot’s perspective. National Museum of World War II Aviation. Colorado Springs, CO. March 4, 2021. Online: https://www.worldwariiaviation.org/sbd-dauntless-dive-bomber-a-pilots-perspective
S. Srivastav, R. T. Jamil, R. Zeltser, Valsalva Maneuver. Online: https://www.ncbi.nlm.nih.gov/books/NBK537248/
Iwasaki KI, Ogawa Y, Kurazumi T, Imaduddin SM, Mukai C, Furukawa S, Yanagida R, Kato T, Konishi T, Shinojima A, Levine BD, Heldt T. Long-Duration Spaceflight Alters Estimated Intracranial Pressure and Cerebral Blood Velocity. The Journal of Physiology, Vol. 599, no. 4, pp. 1067–1081. 2021. Online: https://doi.org/10.1113/JP280318
A. D. Yegorov, Results of Medical Studies during Long-Term Manned Flights on the Orbital Salyut-6 and Soyuz Complex. NASA technical memorandum; NASA TM-76014. National Aeronautics and Space Administration, Washington, D. C. 1979, 20546.
I. I. Kas’yan et al., ‘Pattern of Blood Circulation in the Brain during Rest and Functional Tests by Salyut-4 Space Crewmen’. Biolgy Bulletin of the Academy of Sciences of the USSR, Vol. 7, no. 2, pp. 83–89. 1980.
P. A. Sibony, S. S. Laurie, C. R. Ferguson, L. P. Pardon, M. Young, F. J. Rohlf, B. R. Macias, Ocular Deformations in Spaceflight-Associated Neuro-Ocular Syndrome and Idiopathic Intracranial Hypertension. Investigative Ophthalmology and Visual Science, Vol. 64, No. 3, 2023. Online: https://doi.org/10.1167/iovs.64.3.32
Yang JW, Song QY, Zhang MX, Ai JL, Wang F, Kan GH, Wu B, Zhu SQ. Spaceflight-Associated Neuro-Ocular Syndrome: A Review of Potential Pathogenesis and Intervention. International Journal of Ophthalmology, Vol. 15, No. 2, pp. 336–341. 2021. Online: https://doi.org/10.18240/ijo.2022.02.21
Ong J, Tarver W, Brunstetter T, Mader TH, Gibson CR, Mason SS, Lee A. Spaceflight Associated Neuro-Ocular Syndrome: Proposed Pathogenesis, Terrestrial Analogues, and Emerging Countermeasures. International Journal of Ophthalmology, Vol. 107, No. 7, 895–900. 2023. Online: https://doi.org/10.1136/bjo-2022-322892
Martin Paez Y, Mudie LI, Subramanian PS. Spaceflight Associated Neuro-Ocular Syndrome (SANS): A Systematic Review and Future Directions. Eye Brain, Vol. 19, No. 12, pp. 105–117. 2020. Online: https://doi.org/10.2147/EB.S234076
I. Lehtinen, A. H. Lang, E. Keskinen, ‘Acute Effect of Small Doses of Alcohol on the NSD Parameters (Normalized Slope Descriptors) of Human EEG’. Psychopharmacology, Vol. 60, no. 1, pp. 87–92. 1978. Online: https://doi.org/10.1007/BF00429184
T. Takahashi, ‘Complexity of Spontaneous Brain Activity in Mental Disorders’. Progress in Neuropsychopharmacology and Biological Psychiatry, Vol. 45, pp. 258–266. 2013. Online: https://doi.org/10.1016/j.pnpbp.2012.05.001
G. V. Portnova, M. S. Atanov, ‘Nonlinear EEG Parameters of Emotional Perception in Patients with Moderate Traumatic Brain Injury, Coma, Stroke and Schizophrenia’. AIMS Neuroscience, Vol. 5, no. 4, pp. 221–235. 2018. Online: https://doi.org/10.3934/Neuroscience.2018.4.221
P. Remes, Az első magyar űrrepülés története. Kecskemét, 2020. Online: https://doi.org/10.29068/HO.2020.1-2.45-76
USU, Surgical Critical Care Initiative. Online: https://medschool.usuhs.edu/sur/research/sc2i
M. Bodó, F. J. Pearce, M. Sowd, ‘In Vitro and In Vivo Studies for a Bio-Impedance Vital-Sign Monitor.’ DTIC Technical Report, 2006. Online: https://apps.dtic.mil/dtic/tr/fulltext/u2/a460555.pdf
Szabo S, Totka Z, Nagy-Bozsoky J, Pinter I, Bagany M, Bodó M. Rheoencephalography: A Non-Invasive Method for Neuromonitoring. Journal of Electrical Bioimpedance, Vol. 15, No. 1, pp. 10–25. 2024. Online: https://doi.org/10.2478/joeb-2024-0003