Skip to main content

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

Medical & Biological Engineering & Computing volume 49, pages 1249–1259 (2011)Cite this 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.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

References

  1. Alvarez-Ramirez J, Rodriguez E, Echeverria JC (2009) Delays in the human heartbeat dynamics. Chaos 19:028502

    PubMed  Article  Google Scholar 

  2. Bahraminasab A, Kenwright D, Stefanovska A, Ghasemi F, McClintock PVE (2008) Phase coupling in the cardiorespiratory interaction. IET Syst Biol 2:48–54

    PubMed  Article  CAS  Google Scholar 

  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 40:241–245

    PubMed  Article  CAS  Google Scholar 

  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 52:2112–2115

    PubMed  Article  Google Scholar 

  5. Berens P (2009) CircStat: a matlab toolbox for circular statistics. J Stat Softw 31:1–21

    Google Scholar 

  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 10:2349–2360

    Google Scholar 

  7. Buchheit M, Haddad HA, Laursen PB, Ahmaidi S (2009) Effect of body posture on postexercise parasympathetic reactivation in men. Exp Physiol 94:795–804

    PubMed  Article  CAS  Google Scholar 

  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 90:147–154

    PubMed  CAS  Google Scholar 

  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 38:416–426

    PubMed  Article  CAS  Google Scholar 

  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 95:409–417

    PubMed  Article  Google Scholar 

  11. Cimponeriu L, Rosenblum M, Pikovsky A (2004) Estimation of delay in coupling from time series. Phys Rev E 70:046213

    Article  Google Scholar 

  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 3:44

    PubMed  Article  Google Scholar 

  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–H587

    PubMed  Article  CAS  Google Scholar 

  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–H510

    PubMed  Article  CAS  Google Scholar 

  15. Hoyer D, Hader O, Zwiener U (1997) Relative and intermittent cardiorespiratory coordination. IEEE Eng Med Biol Mag 16:97–104

    PubMed  Article  CAS  Google Scholar 

  16. Hoyer D, Kaplan D, Schaaff F, Eiselt M (1998) Determinism in bivariate cardiorespiratory phase-space sets. IEEE Eng Med Biol Mag 17:26–31

    PubMed  Article  CAS  Google Scholar 

  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 24:33–43

    PubMed  Article  Google Scholar 

  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 456–459

  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:e10602

    PubMed  Article  Google Scholar 

  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. 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

    PubMed  Article  Google Scholar 

  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–H1489

    PubMed  Article  CAS  Google Scholar 

  23. Leder U, Hoyer D, Sommer M, Baier V, Haueisen J, Zwiener U, Figulla HR (2000) Cardiorespiratory desynchronization after acute myocardial infarct. Z Kardiol 89:630–637

    PubMed  Article  CAS  Google Scholar 

  24. Lotric MB, Stefanovska A (2000) Synchronization and modulation in the human cardiorespiratory system. Physica A 283:451–461

    Article  Google Scholar 

  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 32:245–258

    PubMed  Article  CAS  Google Scholar 

  26. Mrowka R, Patzak A, Rosenblum M (2000) Quantitative analysis of cardiorespiratory synchronization in infants. Int J Bifurcat Chaos 10:2479–2488

    Google Scholar 

  27. Navajas D, Farre R, Rotger MM, Milic-Emili J, Sanchis J (1988) Effect of body posture on respiratory impedance. J Appl Physiol 64:194–199

    PubMed  CAS  Google Scholar 

  28. Niebur E, Schuster HG, Kammen DM (1991) Collective frequencies and metastability in networks of limit-cycle oscillators with time delay. Phys Rev Lett 67:2753–2756

    PubMed  Article  Google Scholar 

  29. Ramana Reddy DV, Sen A, Johnston GL (2000) Experimental evidence of time-delay-induced death in coupled limit-cycle oscillators. Phys Rev Lett 85:3381–3384

    PubMed  Article  CAS  Google Scholar 

  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 19:400–411

    PubMed  CAS  Google Scholar 

  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 172:184–191

    PubMed  Article  CAS  Google Scholar 

  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 17:46–53

    PubMed  Article  CAS  Google Scholar 

  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 279–321

  34. Rowell LB (1993) Reflex control during orthostasis. In: Rowell LB (ed) Human cardiovascular control. Oxford University Press, New York, pp 37–80

    Google Scholar 

  35. Rybski D, Havlin S, Bunde A (2003) Phase synchronization in temperature and precipitation records. Phys A Stat Mech Appl 320:601–610

    Article  Google Scholar 

  36. Schafer C, Rosenblum MG, Kurths J, Abel HH (1998) Heartbeat synchronized with ventilation. Nature 392:239–240

    PubMed  Article  CAS  Google Scholar 

  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 60:857–870

    PubMed  Article  CAS  Google Scholar 

  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 85:4831–4834

    PubMed  Article  CAS  Google Scholar 

  39. Toledo E, Akselrod S, Pinhas I, Aravot D (2002) Does synchronization reflect a true interaction in the cardiorespiratory system? Med Eng Phys 24:45–52

    PubMed  Article  CAS  Google Scholar 

  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–H1977

    PubMed  Article  CAS  Google Scholar 

  41. Tzeng YC, Sin PYW, Galletly DC (2009) Human sinus arrhythmia: inconsistencies of a teleological hypothesis. Am J Physiol Heart Circ Physiol 296:H65–H70

    PubMed  Article  CAS  Google Scholar 

  42. Vellody VP, Nassery M, Druz WS, Sharp JT (1978) Effects of body position change on thoracoabdominal motion. J Appl Physiol 45:581–589

    PubMed  CAS  Google Scholar 

  43. Wessel N et al (2009) Detection of time-delayed interactions in biosignals using symbolic coupling traces. EPL 87:10004

    Article  Google Scholar 

  44. Yeung MKS, Strogatz SH (1999) Time delay in the Kuramoto model of coupled oscillators. Phys Rev Lett 82:648–651

    Article  CAS  Google Scholar 

  45. Zar JH (1999) Circular distributions: hypothesis testing. In: Ryu T (ed) Biostatistical analysis. Prentice-Hall, New Jersey, pp 616–663

    Google Scholar 

  46. Zhang J, Yu X, Xie D (2010) Effects of mental tasks on the cardiorespiratory synchronization. Respir Physiol Neurobiol 170:91–95

    PubMed  Article  Google Scholar 

Download references

Acknowledgments

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

Author information

Affiliations

  1. Centre for Heart Rhythm Disorders, The University of Adelaide, Adelaide, SA, 5005, Australia

    Muammar M. Kabir, David A. Saint, Derek Abbott & Mathias Baumert

  2. School of Electrical and Electronic Engineering, The University of Adelaide, Adelaide, SA, 5005, Australia

    Muammar M. Kabir, Derek Abbott & Mathias Baumert

  3. School of Medical Sciences, The University of Adelaide, Adelaide, SA, 5005, Australia

    David A. Saint

  4. School of Biomedical Sciences and Pharmacy, University of Newcastle, Callaghan, NSW, 2308, Australia

    Eugene Nalivaiko

Authors
  1. Muammar M. Kabir
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. David A. Saint
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Eugene Nalivaiko
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Derek Abbott
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mathias Baumert
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Muammar M. Kabir.

Rights and permissions

Reprints 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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11517-011-0822-3

Keywords

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