Evolution of cardiorespiratory interactions with age

Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences

Volumn 371, Issue 1997, 2013, Pages

  Iatsenko, D ^a   Bernjak, A ^a,b,e   Stankovski, T ^a   Shiogai, Y ^a,f   Owen Lynch, P J ^c   Clarkson, P B M ^d   McClintock, P V E ^a   Stefanovska, A ^a,b  

^a LANCASTER UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF LJUBLJANA   (Slovenia)

^c LANCASTER UNIVERSITY   (United Kingdom)

^d RAIGMORE HOSPITAL   (United Kingdom)

^e UNIVERSITY OF SHEFFIELD   (United Kingdom)

^f Omron Healthcare Co   (Japan)

Author keywords

Ageing; Cardiorespiratory interactions; Coupled oscillators; Coupling function; Phase coherence; Synchronization

Indexed keywords

BAYESIAN NETWORKS; INFERENCE ENGINES; SYNCHRONIZATION;

AGEING; CARDIORESPIRATORY INTERACTION; COUPLED OSCILLATORS; COUPLING FUNCTIONS; PHASE COHERENCE;

OSCILLATORS (MECHANICAL);

ADOLESCENT; ADULT; AGED; AGING; ARTICLE; BIOLOGICAL MODEL; BIOLOGICAL RHYTHM; BREATHING RATE; CARDIORESPIRATORY INTERACTIONS; COMPUTER SIMULATION; COUPLED OSCILLATORS; COUPLING FUNCTION; FEMALE; HEART RATE; HUMAN; MALE; MIDDLE AGED; PHASE COHERENCE; PHYSIOLOGY; SYNCHRONIZATION; VERY ELDERLY;

AGEING; CARDIORESPIRATORY INTERACTIONS; COUPLED OSCILLATORS; COUPLING FUNCTION; PHASE COHERENCE; SYNCHRONIZATION;

ADOLESCENT; ADULT; AGED; AGED, 80 AND OVER; AGING; BIOLOGICAL CLOCKS; COMPUTER SIMULATION; FEMALE; HEART RATE; HUMANS; MALE; MIDDLE AGED; MODELS, BIOLOGICAL; RESPIRATORY RATE; YOUNG ADULT;

EID: 84880536388     PISSN: 1364503X     EISSN: None     Source Type: Journal    
DOI: 10.1098/rsta.2011.0622     Document Type: Article

References (71)

1. Hales S. 1733 Statistical essays II, haemostatics. London, UK: Innings Manby.
2. Eckberg DL. 2009 Point:counterpoint: respiratory sinus arrhythmia is due to a central mechanism vs. respiratory sinus arrhythmia is due to the baroreflex mechanism. J. Appl. Physiol. 106, 1740-1742. (doi:10.1152/japplphysiol.91107. 2008).
3. Eckberg DL. 2003 The human respiratory gate. J. Physiol. (Lond.) 548, 339-352. (doi:10.1113/jphysiol.2003.037192). (Pubitemid 36527458)
4. Van de Louw A, Medigue C, Papelier Y, Cottin F. 2008 Breathing cardiovascular variability and baroreflex in mechanically ventilated patients. Am. J. Physiol. Regul. Integr. Comp. Physiol. 295, R1934-R1940. (doi:10.1152/ajpregu.90475.2008).
5. Pagani M, Montano N, Porta A, Malliani A, Abboud FM, Birkett C, Somers VK. 1997 Relationship between spectral components of cardiovascular variabilities and direct measures of muscle sympathetic nerve activity in humans. Circulation 95, 1441-1448. (doi:10.1161/01.CIR.95.6.1441). (Pubitemid 27142801)
6. Stefanovska A, Brǎcǐc M, Kvernmo HD. 1999 Wavelet analysis of oscillations in the peripheral blood circulation measured by laser Doppler technique. IEEE Trans. Biomed. Eng. 46, 1230- 1239. (doi:10.1109/10.790500). (Pubitemid 29451084)
7. Kvandal P, Stefanovska A, Veber M, Kvernmo HD, Kirkebøen K-A. 2003 Regulation of human cutaneous circulation evaluated by laser Doppler flowmetry, iontophoresis, and spectral analysis: importance of nitric oxide and prostaglandines. Microvasc. Res. 65, 160-171. (doi:10.1016/S0026-2862(03)00006- 2). (Pubitemid 36438682)
8. Kvandal P, Landsverk SA, Bernjak A, Stefanovska A, Kvernmo HD, Kirkebøen KA. 2006 Low frequency oscillations of the laser Doppler perfusion signal in human skin. Microvasc. Res. 72, 120-127. (doi:10.1016/j.mvr.2006.05.006). (Pubitemid 44692748)
9. Landsverk SA, Kvandal P, Kjelstrup T, Benko U, Bernjak A, Stefanovska A, Kvernmo H, Kirkebøen KA. 2006 Human skin microcirculation after brachial plexus block evaluated by wavelet transform of the laser Doppler flowmetry signal. Anesthesiology 105, 478-484. (doi:10.1097/00000542-200609000-00010). (Pubitemid 44310429)
10. Stewart JM, Taneja I, Goligorsky MS, Medow MS. 2007 Noninvasive measure ofmicrovascular nitric oxide function in humans using very low-frequency cataneous laser Doppler flow spectra. Microcirculation 14, 169-180. (doi:10.1080/10739680601139179). (Pubitemid 46547096)
11. Söderström T, Stefanovska A, Veber M, Svenson H. 2003 Involvement of sympathetic nerve activity in skin blood flow oscillations in humans. Am. J. Physiol. Heart Circ. Physiol. 284, H1638-H1646. (doi:10.1152/ajpheart.00826.2000). (Pubitemid 36460777)
12. Landsverk SA, Kvandal P, Bernjak A, Stefanovska A, Kirkebøen KA. 2007 The effects of general anesthesia on human skin microcirculation evaluated by wavelet transform. Anesth. Analg. 105, 1012-1019. (doi:10.1213/01.ane. 0000281932.09660.96). (Pubitemid 47479315)
13. Folkow B. 1964 Description of myogenic hypothesis. Circ. Res. 15, 279-287.
14. Johnson PC. 1991 The myogenic response. News Physiol. Sci. 6, 41-42.
15. Kenner T, Passenhofer H, Schwaberger G. 1976 Method for the analysis of the entrainment between heart rate and ventilation rate. Pflügers Arch. 363, 263-265. (doi:10.1007/BF00594612).
16. Hildebrandt G. 1987 The autonomous time structure and its reactive modifications in the human organism. In Temporal disorder in human oscillatory systems (eds L Rensing, U an der Heiden, MC Mackey), pp. 160-174. Berlin, Germany: Springer.
17. Galletly DC, Larsen PD. 1997 Cardioventilatory coupling during anaesthesia. Br. J. Anaesth. 79, 35-40. (doi:10.1038/32567). (Pubitemid 27326757)
18. Schäfer C, Rosenblum MG, Kurths J, Abel HH. 1998 Heartbeat synchronised with ventilation. Nature 392, 239-240. (doi:10.1038/32567). (Pubitemid 28155089)
19. Paluš M, Hoyer D. 1998 Detecting nonlinearity and phase synchronization with surrogate data. IEEE Eng. Med. Biol. 17, 40-45. (doi:10.1109/51.731319). (Pubitemid 28523662)
20. Lotrǐc MB, Stefanovska A. 2000 Synchronization and modulation in the human cardiorespiratory system. Physica A 283, 451-461. (doi:10.1016/S0378- 4371(00)00204-1).
21. Mrowka R, Patzak A, Rosenblum M. 2000 Quantitative analysis of cardiorespiratory synchronization in infants. Int. J. Bifurcation Chaos 10, 2479-2488. (doi:10.1142/S0218127400001754). (Pubitemid 33218727)
22. Giardino ND, Glenny RW, Borson S, Chan L. 2002 Respiratory sinus arrhythmia is associated with efficiency of pulmonary gas exchange in healthy humans. Am. J. Physiol. Heart Circ. Physiol. 284, H1585-H1591. (Pubitemid 36460770)
23. Prokhorov MD, Ponomarenko VI, Gridnev VI, Bodrov MB, Bespyatov AB. 2003 Synchronization between main rhythmic processes in the human cardiovascular system. Phys. Rev. E 68, 041913. (doi:10.1103/PhysRevE.68.041913).
24. Jamšek J, Stefanovska A, McClintock PVE. 2004 Nonlinear cardio-respiratory interactions resolved by time-phase bispectral analysis. Phys. Med. Biol. 49, 4407-4425. (doi:10.1088/0031-9155/49/18/015). (Pubitemid 39302696)
25. Kenwright DA, Bahraminasab A, Stefanovska A, McClintock PVE. 2008 The effect of lowfrequency oscillations on cardio-respiratory synchronization. Eur. Phys. J. B 65, 425-433. (doi:10.1140/epjb/e2008-00199-4).
26. Bahraminasab A, Kenwright D, Stefanovska A, Ghasemi F, McClintock PVE. 2008 Phase coupling in the cardiorespiratory interaction. IET Syst. Biol. 2, 48-54. (doi:10.1049/iet-syb:20060087). (Pubitemid 351222115)
27. Lachaux JP, Rodriguez E, Martinerie J, Varela FJ. 1999 Measuring phase synchrony in brain signals. Hum. Brain Mapp. 8, 194-208. (doi:10.1002/(SICI) 1097-0193(1999)8:4<194:: AID-HBM4>3.0.CO;2-C).
28. Le Van Quyen M, Foucher J, Lachaux JP, Rodriguez E, Lutz A, Martinerie, J, Varela FJ. 2001 Comparison of Hilbert transform and wavelet methods for the analysis of neuronal synchrony. J. Neurosci. Methods 111, 83-98. (doi:10.1016/S0165-0270(01)00372-7). (Pubitemid 32930045)
29. Bandrivskyy A, Bernjak A, McClintock PVE, Stefanovska A. 2004 Wavelet phase coherence analysis: application to skin temperature and blood flow. Cardiovasc. Eng. 4, 89-93. (doi:10.1023/B:CARE.0000025126.63253.43). (Pubitemid 39136187)
30. Bob P, Paluš M, Susta M, Glaslova K. 2008 EEG phase synchronization in patients with paranoid schizophrenia. Neurosci. Lett. 447, 73-77. (doi:10.1016/j.neulet.2008.09.055).
31. Keissar K, Davrath LR, Akselrod S. 2009 Coherence analysis between respiration and heart rate variability using continuous wavelet transform. Phil. Trans. R. Soc. A 367, 1393-1406. (doi:10.1098/rsta.2008.0273).
32. Bernjak A, McClintock PVE, Stefanovska A, Owen-Lynch PJ, Clarkson PBM. 2012 Coherence of fluctuations in blood flow with those in tissue oxygen saturation. Fluct. Noise Lett. 11, 1240013. (doi:10.1142/S0219477512400135).
33. Rosenblum MG, Pikovsky AS. 2001 Detecting direction of coupling in interacting oscillators. Phys. Rev. E 64, 045202. (doi:10.1103/PhysRevE.64. 045202).
34. Paluš M, Stefanovska A. 2003 Direction of coupling from phases of interacting oscillators: an information-theoretic approach. Phys. Rev. E 67, 055201(R). (doi:10.1103/PhysRevE.67.055201).
35. Nollo G, Faes L, Porta A, Antolini R, Ravelli F. 2005 Exploring directionality in spontaneous heart period and systolic pressure variability interactions in humans: implications in the evaluation of baroreflex gain. Am. J. Physiol. Heart Circ. Physiol. 288, H1777-H1785. (doi:10.1152/ajpheart.00594. 2004). (Pubitemid 40418004)
36. Bahraminasab A, Ghasemi F, Stefanovska A, McClintock PVE, Kantz H. 2008 Direction of coupling from phases of interacting oscillators: A permutation information approach. Phys. Rev. Lett. 100, 084101. (doi:10.1103/PhysRevLett. 100.084101). (Pubitemid 351399008)
37. Stankovski T. 2012 Tackling the inverse problem for non-autonomous systems: application to the life sciences. PhD thesis, Lancaster University, UK.
38. Stankovski T, Duggento A, McClintock PVE, Stefanovska A. 2012 Inference of timeevolving coupled dynamical systems in the presence of noise. Phys. Rev. Lett. 109, 024101. (doi:10.1103/PhysRevLett.109.024101).
39. Daubechies I, Lu J, Wu H. 2011 Synchrosqueezed wavelet transforms: an empirical mode decomposition-like tool. Appl. Comput. Harmon. Anal. 30, 243-261. (doi:10.1016/j.acha.2010. 08.002).
40. Kralemann B, Cimponeriu L, Rosenblum M, Pikovsky A, Mrowka R. 2008 Phase dynamics of coupled oscillators reconstructed from data. Phys. Rev. E 77, 066205. (doi:10.1103/PhysRevE.77.066205).
41. Shiogai Y, Stefanovska A, McClintock PVE. 2010 Nonlinear dynamics of cardiovascular ageing. Phys. Rep. 488, 51-110. (doi:10.1016/j.physrep.2009.12. 003).
42. Rompelman O, Coenen AJRM, Kitney RI. 1977 Measurement of heart rate variability: I. Comparative study of heart-rate variability analysis methods. Med. Biol. Eng. Comput. 15, 233-239. (doi:10.1007/BF02441043). (Pubitemid 8122584)
43. deBoer RW, Karemaker JM, Strackee J. 1984 Comparing spectra of a series of point events particularly for heart rate variability data. IEEE Trans. Biomed. Eng. 31, 384-387. (doi:10.1109/TBME.1984.325351).
44. Mateo J, Laguna P. 2000 Improved heart rate variability signal analysis from the beat occurrence times according to the IPFM model. IEEE Trans. Biomed. Eng. 47, 985-996. (doi:10.1109/10.855925). (Pubitemid 30614831)
45. Nakao M, Norimatsu M, Mizutani Y, Yamamoto M. 1997 Spectral distortion properties of the integral pulse frequency modulation model. IEEE Trans. Biomed. Eng. 44, 419-426. (doi:10.1109/10.568918). (Pubitemid 27183864)
46. deBoer RW, Karemaker JM, Strackee J. 1985 Spectrum of a series of point events, generated by the integral pulse frequency modulation model. Med. Biol. Eng. Comput. 23, 138-142. (doi:10.1007/BF02456750). (Pubitemid 15136684)
47. Merri M, Farden DC, Mottley JG, Titlebaum EL. 1990 Sampling frequency of the electrocardiogram for spectral analysis of the heart rate variability. IEEE Trans. Biomed. Eng. 37, 99-106. (doi:10.1109/10.43621). (Pubitemid 20123440)
48. Antelmi I, De Paula RS, Shinzato AR, Peres CA, Mansur AJ, Grupi CJ. 2004 Influence of age, gender, body mass index, and functional capacity on heart rate variability in a cohort of subjects without heart disease. Am. J. Cardiol. 93, 381-385. (doi:10.1016/j.amjcard.2003.09.065). (Pubitemid 38167447)
49. Beckers F, Verheyden B, Aubert AE. 2006 Aging and nonlinear heart rate control in a healthy population. Am. J. Physiol. Heart Circ. Physiol. 290, H2560-H2570. (doi:10.1152/ajpheart.00903.2005). (Pubitemid 43846087)
50. AgelinkMW, Malessa R, Baumann B, Majewski T, Akila F, Zeit T, Ziegler D. 2001 Standardized tests of heart rate variability: normal ranges obtained from 309 healthy humans, and effects of age, gender, and heart rate. Clin. Autonom. Res. 11, 99-108. (doi:10.1007/BF02322053). (Pubitemid 33027945)
51. Camm AJ, Malik M, Bigger JT. 1996 Heart rate variability: standards of measurement, physiological interpretation, and clinical use. Circulation 93, 1043-1065. (doi:10.1161/01.CIR. 93.5.1043). (Pubitemid 26074841)
52. Schreiber T, Schmitz A. 2000 Surrogate time series. Physica D 142, 346-382. (doi:10.1016/S0167-2789(00)00043-9).
53. Faes L, Pinna GD, Porta A, Maestri R, Nollo GI. 2004 Surrogate data analysis for assessing the significance of the coherence function. IEEE Trans. Biomed. Eng. 51, 1156-1166. (doi:10.1109/TBME.2004.827271). (Pubitemid 38787922)
54. Schreiber T, Schmitz A. 1996 Improved surrogate data for nonlinearity tests. Phys. Rev. Lett. 77, 635-638. (doi:10.1103/PhysRevLett.77.635). (Pubitemid 126624517)
55. Porta A, Baselli G, Rimoldi O, Malliani A, Pagani M. 2000 Assessing baroreflex gain from spontaneous variability in conscious dogs: role of causality and respiration. Am. J. Physiol. Heart Circ. Physiol. 279, H2558-H2567.
56. Porta A, Furlan R, Rimoldi O, Pagani M, Malliani A, van de Borne P. 2002 Quantifying the strength of the linear causal coupling in closed loop interacting cardiovascular variability signals. Biol. Cybern. 86, 241-251. (doi:10.1007/s00422-001-0292-z). (Pubitemid 135689574)
57. Porta A, Bari TBV, Tobaldiniand E, Takahashi ACM, Catai AM, Montano N. 2012 Model-based assessment of baroreflex and cardiopulmonary couplings during graded head-up tilt. Comput. Biol. Med. 42, 298-305. (doi:10.1016/j.compbiomed. 2011.04.019).
58. Triedman JK, Saul JP. 1994 Blood-pressure modulation by central venous pressure and respiration. Buffering effects of the heart-rate reflexes. Circulation 89, 169-179. (doi:10.1161/01.CIR.89.1.169). (Pubitemid 24026487)
59. Smelyanskiy VN, Luchinsky DG, Stefanovska A, McClintock PVE. 2005 Inference of a nonlinear stochastic model of the cardiorespiratory interaction. Phys. Rev. Lett. 94, 098101. (doi:10.1103/PhysRevLett.94.098101). (Pubitemid 40629909)
60. Luchinsky DG, Millonas MM, Smelyanskiy VN, Pershakova A, Stefanovska A, McClintock PVE. 2005 Nonlinear statistical modeling and model discovery for cardiorespiratory data. Phys. Rev. E 72, 021905. (doi:10.1103/PhysRevE.72. 021905). (Pubitemid 41520886)
61. Luchinsky DG, Smelyanskiy VN, Duggento A, McClintock PVE. 2008 Inferential framework for nonstationary dynamics. I. Theory. Phys. Rev. E 77, 061105. (doi:10.1103/PhysRevE. 77.061105).
62. Duggento A, Luchinsky DG, Smelyanskiy VN, Khovanov I, McClintock PVE. 2008 Inferential framework for nonstationary dynamics. II. Application to a model of physiological signaling. Phys. Rev. E 77, 061106. (doi:10.1103/ PhysRevE.77.061106).
63. Bartsch R, Kantelhardt JW, Penzel T, Havlin S. 2007 Experimental evidence for phase synchronization transitions in the human cardiorespiratory system. Phys. Rev. Lett. 98, 054102. (doi:10.1103/PhysRevLett.98.054102). (Pubitemid 46203533)
64. Bartsch RP, Schumann AY, Kantelhardt JW, Penzel T, Ivanov PC. 2012 Phase transitions in physiologic coupling. Proc. Natl Acad. Sci. USA 109, 10181-10186. (doi:10.1073/pnas. 1204568109).
65. Mormann F, Lehnertz K, David P, Elger CE. 2000 Mean phase coherence as a measure for phase synchronization and its application to the EEG of epilepsy patients. Physica D 144, 358-369. (doi:10.1016/S0167-2789(00)00087-7).
66. Tass P, Rosenblum MG, Weule J, Kurths J, Pikovsky A, Volkmann J, Schnitzler A, Freund H-J. 1998 Detection of n:m phase locking fromnoisy data: application to magnetoencephalography. Phys. Rev. Lett. 81, 3291-3294. (doi:10.1103/PhysRevLett.81.3291). (Pubitemid 128629556)
67. Stefanovska A, Haken H, McClintock PVE, Hožǐc M, Bajrovíc F, Ribarǐc S. 2000 Reversible transitions between synchronization states of the cardiorespiratory system. Phys. Rev. Lett. 85, 4831-4834. (doi:10.1103/PhysRevLett.85.4831). (Pubitemid 32070433)
68. Hirsch JA, Bishop B. 1981 Respiratory sinus arrhythmia in humans: how breathing pattern modulates heart rate. Am. J. Physiol. 241, H620-H629.
69. Saul JP, Berger RD, Chen MH, Cohen RJ. 1989 Transfer function analysis of autonomic regulation: 2. Respiratory sinus arrythmmia. Am. J. Physiol. 256(part 2), H153-H161.
70. Laitinen T, Hartikainen J, Vanninen E, Niskanen L, Geelen G, Lansimies E. 1998 Age and gender dependency of baroreflex sensitivity in healthy subjects. J. Appl. Physiol. 84, 576-583. (Pubitemid 28081111)
71. Monahan KD, Dinenno FA, Seals DR, Clevenger CM, Desouza CA, Tanaka H. 2001 Age-associated changes in cardiovagal baroreflex sensitivity are related to central arterial compliance. Am. J. Physiol. Heart Circ. Physiol. 281, H284-H289.