Abstract
The cardiorespiratory synchrogram, a graphical tool based on the stroboscopic technique, is an established method for evaluating phase-locking between cardiac and respiratory oscillators. In the original method, the phase of the respiratory oscillator is observed at the instants of time when the phase of the cardiac oscillator attains a certain value. In this article, we introduced an additional adaptive delay in the cardiac oscillator based on the maximisation of the cross-correlation or symbolic coupling traces between the phases of respiration and the delayed R–R intervals. We then investigated phase coordination in thirteen normal subjects (five males, eight females; age: 19–24 years) for different body postures. Cardiorespiratory coordination was observed to be significantly reduced in the upright position (supine vs. upright: 11.9 ± 5.1 vs. 6.9 ± 3.6, P < 0.05). Compared to the original algorithm we observed an increase in the detection of average cardiorespiratory coordination (supine original vs. delay: 11.9 vs. 18.9%), together with a decrease in standard deviation of the percentage of coordination in all the subjects, after introducing the heart rate delay (supine original vs. delay: 5.1 vs. 4.4%). In conclusion, the performance of the synchrogram technique was improved by including an adaptive delay in the cardiac oscillator.
Similar content being viewed by others
References
Alvarez-Ramirez J, Rodriguez E, Echeverria JC (2009) Delays in the human heartbeat dynamics. Chaos 19:028502
Bahraminasab A, Kenwright D, Stefanovska A, Ghasemi F, McClintock PVE (2008) Phase coupling in the cardiorespiratory interaction. IET Syst Biol 2:48–54
Baumert M, Walther T, Hopfe J, Stepan H, Faber R, Voss A (2002) Joint symbolic dynamic analysis of beat-to-beat interactions of heart rate and systolic blood pressure in normal pregnancy. Med Biol Eng Comput 40:241–245
Baumert M, Baier V, Truebner S, Schirdewan A, Voss A (2005) Short- and long-term joint symbolic dynamics of heart rate and blood pressure in dilated cardiomyopathy. IEEE Trans Biomed Eng 52:2112–2115
Berens P (2009) CircStat: a matlab toolbox for circular statistics. J Stat Softw 31:1–21
Bettermann H, Cysarz D, Leeuwen PV (2000) Detecting cardiorespiratory coordination by respiratory pattern analysis of heart period dynamics: the musical rhythm approach. Int J Bifurcat Chaos 10:2349–2360
Buchheit M, Haddad HA, Laursen PB, Ahmaidi S (2009) Effect of body posture on postexercise parasympathetic reactivation in men. Exp Physiol 94:795–804
Butler JE, McKenzie DK, Gandevia SC (2001) Discharge frequencies of single motor units in human diaphragm and parasternal muscles in lying and standing. J Appl Physiol 90:147–154
Censi F, Calcagnini G, Lino S, Seydnejad S, Kitney R, Cerutti S (2000) Transient phase locking patterns among respiration, heart rate and blood pressure during cardiorespiratory synchronisation in humans. Med Biol Eng Comput 38:416–426
Chang AT, Boots RJ, Brown MG, Paratz JD, Hodges PW (2005) Ventilatory changes following head-up tilt and standing in healthy subjects. Eur J Appl Physiol 95:409–417
Cimponeriu L, Rosenblum M, Pikovsky A (2004) Estimation of delay in coupling from time series. Phys Rev E 70:046213
Cysarz D, Bettermann H, Lange S, Geue D, van Leeuwen P (2004) A quantitative comparison of different methods to detect cardiorespiratory coordination during night-time sleep. Biomed Eng Online 3:44
Cysarz D, von Bonin D, Lackner H, Heusser P, Moser M, Bettermann H (2004) Oscillations of heart rate and respiration synchronize during poetry recitation. Am J Physiol Heart Circ Physiol 287:H579–H587
Gilad O, Swenne CA, Davrath LR, Akselrod S (2005) Phase-averaged characterization of respiratory sinus arrhythmia pattern. Am J Physiol Heart Circ Physiol 288:H504–H510
Hoyer D, Hader O, Zwiener U (1997) Relative and intermittent cardiorespiratory coordination. IEEE Eng Med Biol Mag 16:97–104
Hoyer D, Kaplan D, Schaaff F, Eiselt M (1998) Determinism in bivariate cardiorespiratory phase-space sets. IEEE Eng Med Biol Mag 17:26–31
Hoyer D, Leder U, Hoyer H, Pompe B, Sommer M, Zwiener U (2002) Mutual information and phase dependencies: measures of reduced nonlinear cardiorespiratory interactions after myocardial infarction. Med Eng Phys 24:33–43
Kabir MM, Beig MI, Nalivaiko E, Abbott D, Baumert M (2009) Cardiorespiratory coordination in rats is influenced by autonomic blockade. In: 13th International conference on biomedical engineering, Singapore, p 456–459
Kabir MM, Dimitri H, Sanders P, Antic R, Nalivaiko E, Abbott D, Baumert M (2010) Cardiorespiratory phase-coupling is reduced in patients with obstructive sleep apnea. PLoS ONE 5:e10602
Kabir MM, Saint DA, Nalivaiko E, Abbott D, Voss A, Baumert M (2011) Quantification of cardiorespiratory interactions based on joint symbolic dynamics. Ann Biomed Eng. doi:10.1007/s10439-10011-10332-10433
Kotani K, Takamasu K, Ashkenazy Y, Stanley HE, Yamamoto Y (2002) Model for cardiorespiratory synchronization in humans. Phys Rev E Stat Nonlin Soft Matter Phys 65:051923
Kotani K, Takamasu K, Jimbo Y, Yamamoto Y (2008) Postural-induced phase shift of respiratory sinus arrhythmia and blood pressure variations: insight from respiratory-phase domain analysis. Am J Physiol Heart Circ Physiol 294:H1481–H1489
Leder U, Hoyer D, Sommer M, Baier V, Haueisen J, Zwiener U, Figulla HR (2000) Cardiorespiratory desynchronization after acute myocardial infarct. Z Kardiol 89:630–637
Lotric MB, Stefanovska A (2000) Synchronization and modulation in the human cardiorespiratory system. Physica A 283:451–461
Miyamoto Y, Tamura T, Hiura T, Nakamura T, Higuchi J, Mikami T (1982) The dynamic response of the cardiopulmonary parameters to passive head-up tilt. Jpn J Physiol 32:245–258
Mrowka R, Patzak A, Rosenblum M (2000) Quantitative analysis of cardiorespiratory synchronization in infants. Int J Bifurcat Chaos 10:2479–2488
Navajas D, Farre R, Rotger MM, Milic-Emili J, Sanchis J (1988) Effect of body posture on respiratory impedance. J Appl Physiol 64:194–199
Niebur E, Schuster HG, Kammen DM (1991) Collective frequencies and metastability in networks of limit-cycle oscillators with time delay. Phys Rev Lett 67:2753–2756
Ramana Reddy DV, Sen A, Johnston GL (2000) Experimental evidence of time-delay-induced death in coupled limit-cycle oscillators. Phys Rev Lett 85:3381–3384
Robinson BF, Epstein SE, Beiser GD, Braunwald E (1966) Control of heart rate by the autonomic nervous system: studies in man on the interrelation between baroreceptors mechanisms and exercise. Circ Res 19:400–411
Romei M, Mauro AL, D’Angelo MG, Turconi AC, Bresolin N, Pedotti A, Aliverti A (2010) Effects of gender and posture on thoraco-abdominal kinematics during quiet breathing in healthy adults. Respir Physiol Neurobiol 172:184–191
Rosenblum MG, Kurths J, Pikovsky A, Schafer C, Tass P, Abel HH (1998) Synchronization in noisy systems and cardiorespiratory interaction. IEEE Eng Med Biol Mag 17:46–53
Rosenblum MG, Pikovsky A, Kurths J, Schafer C, Tass PA (2001) Phase synchronization: from theory to data analysis. In: Moss F, Gielen S (eds) Handbook of biological physics. Elsevier Science, Amsterdam, pp 279–321
Rowell LB (1993) Reflex control during orthostasis. In: Rowell LB (ed) Human cardiovascular control. Oxford University Press, New York, pp 37–80
Rybski D, Havlin S, Bunde A (2003) Phase synchronization in temperature and precipitation records. Phys A Stat Mech Appl 320:601–610
Schafer C, Rosenblum MG, Kurths J, Abel HH (1998) Heartbeat synchronized with ventilation. Nature 392:239–240
Schafer C, Rosenblum MG, Abel HH, Kurths J (1999) Synchronization in the human cardiorespiratory system. Phys Rev E Stat Phys Plasmas Fluids Relat Interdiscip Topics 60:857–870
Stefanovska A, Haken H, McClintock PVE, Hozic M, Bajrovic F, Ribaric S (2000) Reversible transitions between synchronization states of the cardiorespiratory system. Phys Rev Lett 85:4831–4834
Toledo E, Akselrod S, Pinhas I, Aravot D (2002) Does synchronization reflect a true interaction in the cardiorespiratory system? Med Eng Phys 24:45–52
Tzeng YC, Larsen PD, Galletly DC (2007) Mechanism of cardioventilatory coupling: insights from cardiac pacing, vagotomy, and sinoaortic denervation in the anesthetized rat. Am J Physiol Heart Circ Physiol 292:H1967–H1977
Tzeng YC, Sin PYW, Galletly DC (2009) Human sinus arrhythmia: inconsistencies of a teleological hypothesis. Am J Physiol Heart Circ Physiol 296:H65–H70
Vellody VP, Nassery M, Druz WS, Sharp JT (1978) Effects of body position change on thoracoabdominal motion. J Appl Physiol 45:581–589
Wessel N et al (2009) Detection of time-delayed interactions in biosignals using symbolic coupling traces. EPL 87:10004
Yeung MKS, Strogatz SH (1999) Time delay in the Kuramoto model of coupled oscillators. Phys Rev Lett 82:648–651
Zar JH (1999) Circular distributions: hypothesis testing. In: Ryu T (ed) Biostatistical analysis. Prentice-Hall, New Jersey, pp 616–663
Zhang J, Yu X, Xie D (2010) Effects of mental tasks on the cardiorespiratory synchronization. Respir Physiol Neurobiol 170:91–95
Acknowledgments
The research was supported by the Australian Research Council (Grant # DP 110102049).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Kabir, M.M., Saint, D.A., Nalivaiko, E. et al. Time delay correction of the synchrogram for optimized detection of cardiorespiratory coordination. Med Biol Eng Comput 49, 1249–1259 (2011). https://doi.org/10.1007/s11517-011-0822-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11517-011-0822-3