Abstract
Cardiac and respiratory rhythms are highly nonlinear and nonstationary. As a result traditional time-domain techniques are often inadequate to characterize their complex dynamics. In this article, we introduce a novel technique to investigate the interactions between R–R intervals and respiratory phases based on their joint symbolic dynamics. To evaluate the technique, electrocardiograms (ECG) and respiratory signals were recorded in 13 healthy subjects in different body postures during spontaneous and controlled breathing. Herein, the R–R time series were extracted from ECG and respiratory phases were obtained from abdomen impedance belts using the Hilbert transform. Both time series were transformed into ternary symbol vectors based on the changes between two successive R–R intervals or respiratory phases. Subsequently, words of different symbol lengths were formed and the correspondence between the two series of words was determined to quantify the interaction between cardiac and respiratory cycles. To validate our results, respiratory sinus arrhythmia (RSA) was further studied using the phase-averaged characterization of the RSA pattern. The percentage of similarity of the sequence of symbols, between the respective words of the two series determined by joint symbolic dynamics, was significantly reduced in the upright position compared to the supine position (26.4 ± 4.7 vs. 20.5 ± 5.4%, p < 0.01). Similarly, RSA was also reduced during upright posture, but the difference was less significant (0.11 ± 0.02 vs. 0.08 ± 0.01 s, p < 0.05). In conclusion, joint symbolic dynamics provides a new efficient technique for the analysis of cardiorespiratory interaction that is highly sensitive to the effects of orthostatic challenge.
Similar content being viewed by others
References
Akselrod, S., S. Eliash, O. Oz, and S. Cohen. Hemodynamic regulation in SHR: investigation by spectral analysis. Am. J. Physiol. Heart Circ. Physiol. 253:H176–H183, 1987.
Baier, V., M. Baumert, P. Caminal, M. Vallverdu, R. Faber, and A. Voss. Hidden Markov models based on symbolic dynamics for statistical modeling of cardiovascular control in hypertensive pregnancy disorders. IEEE Trans. Biomed. Eng. 53:140–143, 2006.
Bartsch, R., J. W. Kantelhardt, T. Penzel, and S. Havlin. Experimental evidence for phase synchronization transitions in the human cardiorespiratory system. Phys. Rev. Lett. 98:054102, 2007.
Baselli, G., S. Cerutti, S. Civardi, D. Liberati, F. Lombardi, A. Malliani, and M. Pagani. Spectral and cross-spectral analysis of heart rate and arterial blood pressure variability signals. Comput. Biomed. Res. 19:520–534, 1986.
Baumert, M., V. Baier, S. Truebner, A. Schirdewan, and A. Voss. Short- and long-term joint symbolic dynamics of heart rate and blood pressure in dilated cardiomyopathy. IEEE Trans. Biomed. Eng. 52:2112–2115, 2005.
Baumert, M., T. Walther, J. Hopfe, H. Stepan, R. Faber, and A. Voss. 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, 2002.
Berens, P. CircStat: a Matlab toolbox for circular statistics. J. Stat. Softw. 31:1–21, 2009.
Bernardi, L., C. Porta, A. Gabutti, L. Spicuzza, and P. Sleight. Modulatory effects of respiration. Auton. Neurosci. Basic Clin. 90:47–56, 2001.
Berntson, G. G., J. T. Cacioppo, and K. S. Quigley. Respiratory sinus arrhythmia: autonomic origins, physiological mechanisms, and psychophysiological implications. Psychophysiology 30:183–196, 1993.
Buchheit, M., H. A. Haddad, P. B. Laursen, and S. Ahmaidi. Effect of body posture on postexercise parasympathetic reactivation in men. Exp. Physiol. 94:795–804, 2009.
Caminal, P., B. Giraldo, M. Vallverdú, S. Benito, R. Schroeder, and A. Voss. Symbolic dynamic analysis of relations between cardiac and breathing cycles in patients on weaning trials. Ann. Biomed. Eng. 38:2542–2552, 2010.
Caminal, P., M. Vallverdu, B. Giraldo, S. Benito, G. Vazquez, and A. Voss. Optimized symbolic dynamics approach for the analysis of the respiratory pattern. IEEE Trans. Biomed. Eng. 52:1832–1839, 2005.
Censi, F., G. Calcagnini, S. Lino, S. Seydnejad, R. Kitney, and S. Cerutti. Transient phase locking patterns among respiration, heart rate and blood pressure during cardiorespiratory synchronisation in humans. Med. Biol. Eng. Comput. 38:416–426, 2000.
Censi, F., G. Calcagnini, S. Strano, P. Bartolini, and V. Barbaro. Nonlinear coupling among heart rate, blood pressure, and respiration in patients susceptible to neuromediated syncope. Ann. Biomed. Eng. 31:1097–1105, 2003.
Cysarz, D., H. Bettermann, S. Lange, D. Geue, and P. van Leeuwen. A quantitative comparison of different methods to detect cardiorespiratory coordination during night-time sleep. Biomed. Eng. Online 3:44, 2004.
Devaney, R. L. An Introduction to Chaotic Dynamical Systems. New York: Westview Press, 2003.
Galletly, D. C., and P. D. Larsen. Cardioventilatory coupling during anaesthesia. Br. J. Anaesth. 79:35–40, 1997.
Galletly, D. C., and P. D. Larsen. Relationship between cardioventilatory coupling and respiratory sinus arrhythmia. Br. J. Anaesth. 80:164–168, 1998.
Galletly, D. C., and P. D. Larsen. The determination of cardioventilatory coupling from heart rate and ventilatory time series. Res. Exp. Med. 199:95–99, 1999.
Gilad, O., C. A. Swenne, L. R. Davrath, and S. Akselrod. Phase-averaged characterization of respiratory sinus arrhythmia pattern. Am. J. Physiol. Heart. Circ. Physiol. 288:H504–H510, 2005.
Hayano, J., F. Yasuma, A. Okada, S. Mukai, and T. Fujinami. Respiratory sinus arrhythmia: a phenomenon improving pulmonary gas exchange and circulatory efficiency. Circulation 94:842–847, 1996.
Hoyer, D., O. Hader, and U. Zwiener. Relative and intermittent cardiorespiratory coordination. IEEE Eng. Med. Biol. Mag. 16:97–104, 1997.
Hoyer, D., D. Kaplan, F. Schaaff, and M. Eiselt. Determinism in bivariate cardiorespiratory phase-space sets. IEEE Eng. Med. Biol. Mag. 17:26–31, 1998.
Hoyer, D., U. Leder, H. Hoyer, B. Pompe, M. Sommer, and U. Zwiener. Mutual information and phase dependencies: measures of reduced nonlinear cardiorespiratory interactions after myocardial infarction. Med. Eng. Phys. 24:33–43, 2002.
Kabir, M. M., H. Dimitri, P. Sanders, R. Antic, E. Nalivaiko, D. Abbott, and M. Baumert. Cardiorespiratory phase-coupling is reduced in patients with obstructive sleep apnea. PLoS One 5:e10602, 2010.
Kabir, M. M., E. Nalivaiko, D. Abbott, and M. Baumert. Impact of movement on cardiorespiratory coordination in conscious rats. In: Engineering in Medicine and Biology Society (EMBC), 2010 Annual International Conference of the IEEE, 2010, pp. 1938–1941.
Kitchens, B. P. Symbolic Dynamics: One-Sided, Two-Sided and Countable State Markov Shifts. Berlin: Springer, 1998.
Kotani, K., K. Takamasu, Y. Ashkenazy, H. E. Stanley, and Y. Yamamoto. Model for cardiorespiratory synchronization in humans. Phys. Rev. E Stat. Nonlinear Soft Matter Phys. 65:051923, 2002.
Krishnamurthy, S., X. Wang, D. Bhakta, E. Bruce, J. Evans, T. Justice, and A. Patwardhan. Dynamic cardiorespiratory interaction during head-up tilt-mediated presyncope. Am. J. Physiol. Heart Circ. Physiol. 287:H2510–H2517, 2004.
Kurths, J., A. Voss, P. Saparin, A. Witt, H. J. Kleiner, and N. Wessel. Quantitative analysis of heart rate variability. Chaos Interdiscipl. J. Nonlinear Sci. 5:88–94, 1995.
Lotric, M. B., and A. Stefanovska. Synchronization and modulation in the human cardiorespiratory system. Physica A 283:451–461, 2000.
Moser, M., M. Lehofer, A. Sedminek, M. Lux, H. Zapotoczky, T. Kenner, and A. Noordergraaf. Heart rate variability as a prognostic tool in cardiology. A contribution to the problem from a theoretical point of view. Circulation 90:1078–1082, 1994.
Mrowka, R., L. Cimponeriu, A. Patzak, and M. G. Rosenblum. Directionality of coupling of physiological subsystems: age-related changes of cardiorespiratory interaction during different sleep stages in babies. Am. J. Physiol. Regul. Integr. Comp. Physiol. 285:R1395–R1401, 2003.
Mrowka, R., A. Patzak, and M. Rosenblum. Quantitative analysis of cardiorespiratory synchronization in infants. Int. J. Bifurc. Chaos 10:2479–2488, 2000.
Neff, R. A., J. Wang, S. Baxi, C. Evans, and D. Mendelowitz. Respiratory sinus arrhythmia: endogenous activation of nicotinic receptors mediates respiratory modulation of brainstem cardioinhibitory parasympathetic neurons. Circ. Res. 93:565–572, 2003.
Porta, A., S. Guzzetti, N. Montano, M. Pagani, V. Somers, A. Malliani, G. Baselli, and S. Cerutti. Information domain analysis of cardiovascular variability signals: evaluation of regularity, synchronisation and co-ordination. Med. Biol. Eng. Comput. 38:180–188, 2000.
Robinson, C. Dynamical Systems: Stability, Symbolic Dynamics, and Chaos. Boca Raton: CRC Press, 1999.
Robinson, B. F., S. E. Epstein, G. D. Beiser, and E. Braunwald. 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, 1966.
Rosenblum, M. G., J. Kurths, A. Pikovsky, C. Schafer, P. Tass, and H. H. Abel. Synchronization in noisy systems and cardiorespiratory interaction. IEEE Eng. Med. Biol. Mag. 17:46–53, 1998.
Rowell, L. B. Reflex control during orthostasis. In: Human Cardiovascular Control, edited by L. B. Rowell. New York: Oxford University Press, 1993, pp. 37–80.
Rybski, D., S. Havlin, and A. Bunde. Phase synchronization in temperature and precipitation records. Phys. A Stat. Mech. Appl. 320:601–610, 2003.
Saul, J. P., R. D. Berger, P. Albrecht, S. P. Stein, M. H. Chen, and R. J. Cohen. Transfer function analysis of the circulation: unique insights into cardiovascular regulation. Am. J. Physiol. Heart Circ. Physiol. 261:H1231–H1245, 1991.
Schafer, C., M. G. Rosenblum, H. H. Abel, and J. Kurths. Synchronization in the human cardiorespiratory system. Phys. Rev. E Stat. Phys. Plasmas Fluids Relat. Interdiscipl. Top. 60:857–870, 1999.
Schafer, C., M. G. Rosenblum, J. Kurths, and H. H. Abel. Heartbeat synchronized with ventilation. Nature 392:239–240, 1998.
Stefanovska, A., H. Haken, P. V. E. McClintock, M. Hozic, F. Bajrovic, and S. Ribaric. Reversible transitions between synchronization states of the cardiorespiratory system. Phys. Rev. Lett. 85:4831–4834, 2000.
Taha, B. H., P. M. Simon, J. A. Dempsey, J. B. Skatrud, and C. Iber. Respiratory sinus arrhythmia in humans: an obligatory role for vagal feedback from the lungs. J. Appl. Physiol. 78:638–645, 1995.
Tzeng, Y., P. Larsen, and D. Galletly. Cardioventilatory coupling in resting human subjects. Exp. Physiol. 88:775–782, 2003.
Tzeng, Y. C., P. D. Larsen, and D. C. Galletly. 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, 2007.
Voss, A., J. Kurths, H. J. Kleiner, A. Witt, N. Wessel, P. Saparin, K. J. Osterziel, R. Schurath, and R. Dietz. The application of methods of non-linear dynamics for the improved and predictive recognition of patients threatened by sudden cardiac death. Cardiovasc. Res. 31:419–433, 1996.
Zar, J. H. Circular distributions: hypothesis testing. In: Biostatistical Analysis, 4th ed., edited by T. Ryu. New Jersey: Prentice-Hall, 1999, pp. 616–663.
Acknowledgments
The research was supported by the Australian Research Council (grant # DP 110102049).
Conflict of Interest
There is no conflict of interest.
Author information
Authors and Affiliations
Corresponding author
Additional information
Associate Editor Jane Grande-Allen oversaw the review of this article.
Rights and permissions
About this article
Cite this article
Kabir, M.M., Saint, D.A., Nalivaiko, E. et al. Quantification of Cardiorespiratory Interactions Based on Joint Symbolic Dynamics. Ann Biomed Eng 39, 2604–2614 (2011). https://doi.org/10.1007/s10439-011-0332-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10439-011-0332-3