Abstract
The aim of the present study was to identify the response of the autonomic nervous system (ANS) to passive lower limb movement and to determine whether there are gender differences. The experimental sets included 5 cycles per minute (CPM5), 10 cycles per minute (CPM10) and 15 cycles per minute (CPM15) on the passive cycling machine. ANS activity was measured using heart rate variability time domain analysis (RR interval, pNN50, RMSSD and SDNN), frequency domain analysis (TF, LF, HF and LF/HF) and Poincaré plot analysis (SD1, SD2 and SD1/SD2 ratio). The collected signal at rest served as the baseline (rest). Compared with the parameters at rest, the male subjects had decreased pNN50, decreased SDNN, lower TP and LF power (ms2), suppressed LF (n.u.), augmented HF (n.u.), suppressed LF/HF, decreased SD2 and increased SD1/SD2 ratios in response to CPM5 or CPM10 (all P < 0.05). Compared with the parameters at rest, decreased LF/HF and increased SD1/SD2 in response to CPM5 or CPM10 (all P < 0.05) were the only changes in the female subjects. LF/HF and SD1/SD2 differed between both groups for the same level of passive lower limb movement (all P < 0.05). These results suggest that passive lower limb movement leads to an ANS response and that male subjects are more sensitive to passive lower limb movements. During passive leg movements, sympathetic nervous activity is largely suppressed, and vagal activity achieves dominance. The response of the ANS to passive leg movement is determined by gender.
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Adekunle AE, Akintomide AO (2012) Gender differences in the variables of exercise treadmill test in type 2 diabetes mellitus. Ann Afr Med 11(2):96–102
Agel J, Arendt EA, Bershadsky B (2005) Anterior cruciate ligament injury in national collegiate athletic association basketball and soccer: a 13-year review. Am J Sports Med 33(4):524–530
Arendt EA, Agel J, Dick R (1999) Anterior cruciate ligament injury patterns among collegiate men and women. J Athl Train 34(2):86–92
Birch B, Haslam E, Heerah I, Dechev N, Park EJ (2008) Design of a continuous passive and active motion device for hand rehabilitation. Conf Proc IEEE Eng Med Biol Soc 2008:4306–4309
Brown R, Kemp U, Macefield V (2013) Increases in muscle sympathetic nerve activity, heart rate, respiration, and skin blood flow during passive viewing of exercise. Front Neurosci 7:102
Camargo Pires-Neto R, Fogaca Kawaguchi YM, Sayuri Hirota A, Fu C, Tanaka C, Caruso P, Park M, Ribeiro Carvalho CR (2013) Very early passive cycling exercise in mechanically ventilated critically ill patients: physiological and safety aspects—a case series. PLoS ONE 8(9):e74182
De Vito G, Galloway SDR, Nimmo MA, Maas P, McMurray JJV (2002) Effects of central sympathetic inhibition on heart rate variability during steady-state exercise in healthy humans. Clin Physiol Funct Imaging 22(1):32–38
Decety J, Jeannerod M, Durozard D, Baverel G (1993) Central activation of autonomic effectors during mental simulation of motor actions in man. J Physiol 461:549–563
Doering TJ, Resch KL, Steuernagel B, Brix J, Schneider B, Fischer GC (1998) Passive and active exercises increase cerebral blood flow velocity in young, healthy individuals. Am J Phys Med Rehabil 77(6):490–493
Dutra SGV, Pereira APM, Tezini GCSV, Mazon JH, Martins-Pinge MC, Souza HCD (2013) Cardiac autonomic modulation is determined by gender and is independent of aerobic physical capacity in healthy subjects. PLoS One 8(10):e77092
Eckberg DL (1997) Sympathovagal balance: a critical appraisal. Circulation 96(9):3224–3232
Felici F (2006) Neuromuscular responses to exercise investigated through surface EMG. J Electromyogr Kinesiol 16(6):578–585
Gladwell VF, Coote JH (2002) Heart rate at the onset of muscle contraction and during passive muscle stretch in humans: a role for mechanoreceptors. J Physiol 540(Pt 3):1095–1102
Gonzalez-Alonso J, Mortensen SP, Jeppesen TD, Ali L, Barker H, Damsgaard R, Secher NH, Dawson EA, Dufour SP (2008) Haemodynamic responses to exercise, ATP infusion and thigh compression in humans: insight into the role of muscle mechanisms on cardiovascular function. J Physiol 586(9):2405–2417
Hellsten Y, Rufener N, Nielsen JJ, Hoier B, Krustrup P, Bangsbo J (2008) Passive leg movement enhances interstitial VEGF protein, endothelial cell proliferation, and eNOS mRNA content in human skeletal muscle. Am J Physiol Regul Integr Comp Physiol 294(3):R975–R982
Herbold JA, Bonistall K, Blackburn M (2012) Effectiveness of continuous passive motion in an inpatient rehabilitation hospital after total knee replacement: a matched cohort study. PM R 4(10):719–725
Kamen PW, Tonkin AM (1995) Application of the Poincare plot to heart rate variability: a new measure of functional status in heart failure. Aust NZ J Med 25(1):18–26
Krustrup P, Hellsten Y, Bangsbo J (2004) Intense interval training enhances human skeletal muscle oxygen uptake in the initial phase of dynamic exercise at high but not at low intensities. J Physiol 559(Pt 1):335–345
Lattanzio PJ, Petrella RJ (1998) Knee proprioception: a review of mechanisms, measurements, and implications of muscular fatigue. Orthopedics 21(4):463–470 (discussion 470-61; passim)
Malliani A, Pagani M, Lombardi F, Cerutti S (1991) Cardiovascular neural regulation explored in the frequency domain. Circulation 84(2):482–492
McDaniel J, Hayman MA, Ives S, Fjeldstad AS, Trinity JD, Wray DW, Richardson RS (2010) Attenuated exercise induced hyperaemia with age: mechanistic insight from passive limb movement. J Physiol 588(Pt 22):4507–4517
Mortensen SP, Askew CD, Walker M, Nyberg M, Hellsten Y (2012) The hyperaemic response to passive leg movement is dependent on nitric oxide: a new tool to evaluate endothelial nitric oxide function. J Physiol Lond 590(17):4391–4400
Muraki S, Yamasaki M, Ehara Y, Kikuchi K, Seki K (1996) Cardiovascular and respiratory responses to passive leg cycle exercise in people with spinal cord injuries. Eur J Appl Physiol Occup Physiol 74(1–2):23–28
Nagai T, Sell TC, Abt JP, Lephart SM (2012) Reliability, precision, and gender differences in knee internal/external rotation proprioception measurements. Phys Ther Sport Off J Assoc Chart Physiother Sports Med 13(4):233–237
Nobrega AC, Araujo CG (1993) Heart rate transient at the onset of active and passive dynamic exercise. Med Sci Sports Exerc 25(1):37–41
Nobrega AC, O’Leary D, Silva BM, Marongiu E, Piepoli MF, Crisafulli A (2014) Neural regulation of cardiovascular response to exercise: role of central command and peripheral afferents. Biomed Res Int 2014:478965
Nobrega AC, Williamson JW, Friedman DB, Araujo CG, Mitchell JH (1994) Cardiovascular responses to active and passive cycling movements. Med Sci Sports Exerc 26(6):709–714
Ogata H, Higuchi Y, Ogata T, Hoshikawa S, Akai M, Nakazawa K (2009) Pressor response to passive walking-like exercise in spinal cord-injured humans. Clin Auton Res 19(2):113–122
Proctor DN, Beck KC, Shen PH, Eickhoff TJ, Halliwill JR (1985) Joyner MJ (1998) Influence of age and gender on cardiac output-VO2 relationships during submaximal cycle ergometry. J Appl Physiol 84(2):599–605
Radegran G, Saltin B (1998) Muscle blood flow at onset of dynamic exercise in humans. Am J Physiol 274(1 Pt 2):H314–H322
Shi P, Zhu Y, Allen J, Hu S (2009) Analysis of pulse rate variability derived from photoplethysmography with the combination of lagged Poincare plots and spectral characteristics. Med Eng Phys 31(7):866–871
Shultz SJ, Perrin DH (1999) Using surface electromyography to assess sex differences in neuromuscular response characteristics. J Athl Train 34(2):165–176
Stevenson JR, Blake JM, Douglas TF, Kercheval DM (2005) Does continuous passive motion during keyboarding affect hand blood flow and wrist function? A prospective case report. Work 24(2):145–155
Strange S (1999) Cardiovascular control during concomitant dynamic leg exercise and static arm exercise in humans. J Physiol 514(Pt 1):283–291
Task Force of the European Society of Cardiology and the North American Society of Pacing and Electrophysiology (1996) Heart rate variability: standards of measurement, physiological interpretation and clinical use. Circulation 93(5):1043–1065
Ter Woerds W, De Groot PCE, van Kuppevelt DHJM, Hopman MTE (2006) Passive leg movements and passive cycling do not alter arterial leg blood flow in subjects with spinal cord injury. Phys Ther 86(5):636–645
Tulppo MP, Makikallio TH, Takala TE, Seppanen T, Huikuri HV (1996) Quantitative beat-to-beat analysis of heart rate dynamics during exercise. Am J Physiol 271(1 Pt 2):H244−H252
Uhl TL, Muir TA, Lawson L (2010) Electromyographical assessment of passive, active assistive, and active shoulder rehabilitation exercises. PM R 2(2):132–141
Weippert M, Behrens K, Rieger A, Stoll R, Kreuzfeld S (2013) Heart rate variability and blood pressure during dynamic and static exercise at similar heart rate levels. PLoS ONE 8(12):e83690
Williamson JW (2010) The relevance of central command for the neural cardiovascular control of exercise. Exp Physiol 95(11):1043–1048
Williamson JW, Nobrega AC, McColl R, Mathews D, Winchester P, Friberg L, Mitchell JH (1997) Activation of the insular cortex during dynamic exercise in humans. J Physiol 503(Pt 2):277–283
Willoughby DS, Priest JW, Nelson M (2002) Expression of the stress proteins, ubiquitin, heat shock protein 72, and myofibrillar protein content after 12 weeks of leg cycling in persons with spinal cord injury. Arch Phys Med Rehabil 83(5):649–654
Wu Y, Chen B, Hong K, Hu W, Peng Q, Li Y, Cheng X, Su H (2013) Passive leg movement enhances diuresis and decline of plasma NT-proBNP level in patients with decompensated heart failure treated with furosemide. Int J Cardiol 168(4):4289–4290
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This work was supported by the Innovation Program of the Shanghai Municipal Education Commission (Grant No. 14YZ091).
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All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards. The study was approved by the ethics committee of University of Shanghai for Science and Technology, Shanghai, China (Ref. No. 2013-9010-14YZ091).
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Shi, P., Hu, S. & Yu, H. The response of the autonomic nervous system to passive lower limb movement and gender differences. Med Biol Eng Comput 54, 1159–1167 (2016). https://doi.org/10.1007/s11517-015-1378-4
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DOI: https://doi.org/10.1007/s11517-015-1378-4