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Medical & Biological Engineering & Computing

, Volume 49, Issue 11, pp 1249–1259 | Cite as

Time delay correction of the synchrogram for optimized detection of cardiorespiratory coordination

  • Muammar M. KabirEmail author
  • David A. Saint
  • Eugene Nalivaiko
  • Derek Abbott
  • Mathias Baumert
Original Article

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.

Keywords

Heart Heart rate variability Coupling Breathing frequency Respiratory sinus arrhythmia Phase locking Synchronization 

Notes

Acknowledgments

The research was supported by the Australian Research Council (Grant # DP 110102049).

References

  1. 1.
    Alvarez-Ramirez J, Rodriguez E, Echeverria JC (2009) Delays in the human heartbeat dynamics. Chaos 19:028502PubMedCrossRefGoogle Scholar
  2. 2.
    Bahraminasab A, Kenwright D, Stefanovska A, Ghasemi F, McClintock PVE (2008) Phase coupling in the cardiorespiratory interaction. IET Syst Biol 2:48–54PubMedCrossRefGoogle Scholar
  3. 3.
    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 40:241–245PubMedCrossRefGoogle Scholar
  4. 4.
    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 52:2112–2115PubMedCrossRefGoogle Scholar
  5. 5.
    Berens P (2009) CircStat: a matlab toolbox for circular statistics. J Stat Softw 31:1–21Google Scholar
  6. 6.
    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 10:2349–2360Google Scholar
  7. 7.
    Buchheit M, Haddad HA, Laursen PB, Ahmaidi S (2009) Effect of body posture on postexercise parasympathetic reactivation in men. Exp Physiol 94:795–804PubMedCrossRefGoogle Scholar
  8. 8.
    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 90:147–154PubMedGoogle Scholar
  9. 9.
    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 38:416–426PubMedCrossRefGoogle Scholar
  10. 10.
    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 95:409–417PubMedCrossRefGoogle Scholar
  11. 11.
    Cimponeriu L, Rosenblum M, Pikovsky A (2004) Estimation of delay in coupling from time series. Phys Rev E 70:046213CrossRefGoogle Scholar
  12. 12.
    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 3:44PubMedCrossRefGoogle Scholar
  13. 13.
    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–H587PubMedCrossRefGoogle Scholar
  14. 14.
    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–H510PubMedCrossRefGoogle Scholar
  15. 15.
    Hoyer D, Hader O, Zwiener U (1997) Relative and intermittent cardiorespiratory coordination. IEEE Eng Med Biol Mag 16:97–104PubMedCrossRefGoogle Scholar
  16. 16.
    Hoyer D, Kaplan D, Schaaff F, Eiselt M (1998) Determinism in bivariate cardiorespiratory phase-space sets. IEEE Eng Med Biol Mag 17:26–31PubMedCrossRefGoogle Scholar
  17. 17.
    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 24:33–43PubMedCrossRefGoogle Scholar
  18. 18.
    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 456–459Google Scholar
  19. 19.
    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:e10602PubMedCrossRefGoogle Scholar
  20. 20.
    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
  21. 21.
    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 65:051923PubMedCrossRefGoogle Scholar
  22. 22.
    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–H1489PubMedCrossRefGoogle Scholar
  23. 23.
    Leder U, Hoyer D, Sommer M, Baier V, Haueisen J, Zwiener U, Figulla HR (2000) Cardiorespiratory desynchronization after acute myocardial infarct. Z Kardiol 89:630–637PubMedCrossRefGoogle Scholar
  24. 24.
    Lotric MB, Stefanovska A (2000) Synchronization and modulation in the human cardiorespiratory system. Physica A 283:451–461CrossRefGoogle Scholar
  25. 25.
    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 32:245–258PubMedCrossRefGoogle Scholar
  26. 26.
    Mrowka R, Patzak A, Rosenblum M (2000) Quantitative analysis of cardiorespiratory synchronization in infants. Int J Bifurcat Chaos 10:2479–2488Google Scholar
  27. 27.
    Navajas D, Farre R, Rotger MM, Milic-Emili J, Sanchis J (1988) Effect of body posture on respiratory impedance. J Appl Physiol 64:194–199PubMedGoogle Scholar
  28. 28.
    Niebur E, Schuster HG, Kammen DM (1991) Collective frequencies and metastability in networks of limit-cycle oscillators with time delay. Phys Rev Lett 67:2753–2756PubMedCrossRefGoogle Scholar
  29. 29.
    Ramana Reddy DV, Sen A, Johnston GL (2000) Experimental evidence of time-delay-induced death in coupled limit-cycle oscillators. Phys Rev Lett 85:3381–3384PubMedCrossRefGoogle Scholar
  30. 30.
    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 19:400–411PubMedGoogle Scholar
  31. 31.
    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 172:184–191PubMedCrossRefGoogle Scholar
  32. 32.
    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 17:46–53PubMedCrossRefGoogle Scholar
  33. 33.
    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 279–321Google Scholar
  34. 34.
    Rowell LB (1993) Reflex control during orthostasis. In: Rowell LB (ed) Human cardiovascular control. Oxford University Press, New York, pp 37–80Google Scholar
  35. 35.
    Rybski D, Havlin S, Bunde A (2003) Phase synchronization in temperature and precipitation records. Phys A Stat Mech Appl 320:601–610CrossRefGoogle Scholar
  36. 36.
    Schafer C, Rosenblum MG, Kurths J, Abel HH (1998) Heartbeat synchronized with ventilation. Nature 392:239–240PubMedCrossRefGoogle Scholar
  37. 37.
    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 60:857–870PubMedCrossRefGoogle Scholar
  38. 38.
    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 85:4831–4834PubMedCrossRefGoogle Scholar
  39. 39.
    Toledo E, Akselrod S, Pinhas I, Aravot D (2002) Does synchronization reflect a true interaction in the cardiorespiratory system? Med Eng Phys 24:45–52PubMedCrossRefGoogle Scholar
  40. 40.
    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–H1977PubMedCrossRefGoogle Scholar
  41. 41.
    Tzeng YC, Sin PYW, Galletly DC (2009) Human sinus arrhythmia: inconsistencies of a teleological hypothesis. Am J Physiol Heart Circ Physiol 296:H65–H70PubMedCrossRefGoogle Scholar
  42. 42.
    Vellody VP, Nassery M, Druz WS, Sharp JT (1978) Effects of body position change on thoracoabdominal motion. J Appl Physiol 45:581–589PubMedGoogle Scholar
  43. 43.
    Wessel N et al (2009) Detection of time-delayed interactions in biosignals using symbolic coupling traces. EPL 87:10004CrossRefGoogle Scholar
  44. 44.
    Yeung MKS, Strogatz SH (1999) Time delay in the Kuramoto model of coupled oscillators. Phys Rev Lett 82:648–651CrossRefGoogle Scholar
  45. 45.
    Zar JH (1999) Circular distributions: hypothesis testing. In: Ryu T (ed) Biostatistical analysis. Prentice-Hall, New Jersey, pp 616–663Google Scholar
  46. 46.
    Zhang J, Yu X, Xie D (2010) Effects of mental tasks on the cardiorespiratory synchronization. Respir Physiol Neurobiol 170:91–95PubMedCrossRefGoogle Scholar

Copyright information

© International Federation for Medical and Biological Engineering 2011

Authors and Affiliations

  • Muammar M. Kabir
    • 1
    • 2
    Email author
  • David A. Saint
    • 1
    • 3
  • Eugene Nalivaiko
    • 4
  • Derek Abbott
    • 1
    • 2
  • Mathias Baumert
    • 1
    • 2
  1. 1.Centre for Heart Rhythm DisordersThe University of AdelaideAdelaideAustralia
  2. 2.School of Electrical and Electronic EngineeringThe University of AdelaideAdelaideAustralia
  3. 3.School of Medical SciencesThe University of AdelaideAdelaideAustralia
  4. 4.School of Biomedical Sciences and PharmacyUniversity of NewcastleCallaghanAustralia

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