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Mechanisms of ventilatory periodicities

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Abstract

The study of ventilatory periodicities is relevant to the problem of obstructive sleep apnea. Apneas occur at the nadirs of periodicities during sleep. Periodicities can be caused by chemical instability, related to unstable action of the closed loop feedback system for the chemical regulation of breathing. Such instability occurs when overall loop gain is greater than or equal to unity and the phase lag around the loop is 180°. Periodic breathing during hypoxia and in patients with congestive heart failure is likely to be explained by this mechanism. Periodic breathing can also be the result of state instability. Here ventilation declines at sleep onset and the resultant changes in blood gases trigger an arousal, i.e., sudden transition to a lighter stage of sleep. With arousal, ventilation increases. Thus, periodic breathing is secondary to these changes in sleep state. These processes, chemical instability and state instability, can interact and produce complex patterns of oscillation in ventilation.

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References

  1. Ancoli-Israel, S.; Kripke, D.F.; Mason, W.; Kaplan, O.J. Sleep apnea and periodic movements in an aging sample. J. Gerontol. 40:419–425; 1985.

    PubMed  CAS  Google Scholar 

  2. Asmussen, E. Regulation of respiration: “The black box”. Acta Physiol. Scand. 99:85–90; 1977.

    Article  PubMed  CAS  Google Scholar 

  3. Berssenbrugge, A.; Dempsey, J.; Iber, C.; Skatrud, J.; Wilson, P. Mechanisms of hypoxia-induced periodic breathing during sleep in humans. J. Physiol. Lond. 343:507–526; 1983.

    PubMed  CAS  Google Scholar 

  4. Berthon-Jones, M.; Sullivan, C.E. Ventilation and arousal responses to hypercapnia in normal sleeping humans. J. Appl. Physiol. 57:59–67; 1984.

    PubMed  CAS  Google Scholar 

  5. Brouillette, R.T.; Thach, B.T. Control of genioglossus muscle inspiratory activity. J. Appl. Physiol. 49:801–808; 1980.

    PubMed  CAS  Google Scholar 

  6. Bulow, K. Respiration and wakefulness in man. Acta Physiol. Scand. Suppl. 209:5–110; 1963.

    Google Scholar 

  7. Carley, D.W.; Önal, E.; Aronson, R.; Lopata, M. Associations of electroencephalographic arousal with apnea resolution and apnea onset in obstructive sleep apnea syndrome. Am. Rev. Respir. Dis. 137:60; 1988 Abstract.

    Google Scholar 

  8. Carskadon, M.A.; Dement, W.C. Respiration during sleep in the aged human. J. Gerontol. 36:420–423; 1981.

    PubMed  CAS  Google Scholar 

  9. Chapman, K.R.; Bruce, E.N.; Gothe, B.; Cherniack, N.S. Possible mechanisms of periodic breathing during sleep. J. Appl. Physiol. 64:1000–1008; 1988.

    Article  PubMed  CAS  Google Scholar 

  10. Cherniack, N.S. Sleep apnea and its causes. J. Clin. Invest. 73:1501–1506; 1984.

    PubMed  CAS  Google Scholar 

  11. Colrain, I.M.; Trinder, J.; Fraser, G.; Wilson, G.V. Ventilation during sleep onset. J. Appl. Physiol. 63:2067–2074; 1987.

    PubMed  CAS  Google Scholar 

  12. Dark, D.S.; Pingleton, S.K.; Kerby, G.R.; Crabb, J.E.; Gollub, S.B.; Glatter, T.R.; Dunn, M.I. Breathing pattern abnormalities and arterial oxygen desaturation during sleep in the congestive heart failure syndrome. Chest 91:833–836; 1987.

    PubMed  CAS  Google Scholar 

  13. Eldridge, F.L. Maintenance of respiration by central neural feedback mechanisms. Fed. Proc. 36:2400–2404; 1977.

    PubMed  CAS  Google Scholar 

  14. Findley, L.J.; Zwillich, C.W.; Ancoli-Israel, S.; Kripke D.; Tisi, G.; Moser, K.M. Cheyne-Stokes breathing during sleep in patients with left ventricular heart failure. S. Med. J. 78:11–14, 1985.

    CAS  Google Scholar 

  15. Fink, B.R. Influence of cerebral activity in wakefulness on regulation of breathing. J. Appl. Physiol. 16:15–20; 1961.

    PubMed  CAS  Google Scholar 

  16. Gath, I.; Bar-On, E. Classical sleep stages and the spectral content of the EEG signal. Int. J. Neurosci. 22:147–155; 1983.

    PubMed  CAS  Google Scholar 

  17. Gleeson, K.; Zwillich, C.W.; White, D.P. The influence of increasing ventilatory effort on arousal from sleep. Am. Rev. Respir. Dis. 142:295–300, 1990.

    PubMed  CAS  Google Scholar 

  18. Guyton, A.C.; Crowell, J.W.; Moore, J.W. Basic oscillating mechanism of Cheyne-Stokes breathing. Am. J. Physiol. 187:395–398; 1968.

    Google Scholar 

  19. Haponik, E.F.; Smith, P.L.; Bohlman, M.E.; Allen, R.P.; Goldman, S.M.; Bleecker, E.R. Computerized tomography in obstructive sleep apnea. Am. Rev. Respir. Dis. 127:221–226; 1983.

    PubMed  CAS  Google Scholar 

  20. Hasan, J. Differentiation of normal and disturbed sleep by automatic analysis. Acta. Physiol. Scand. Suppl. 526:1–103; 1983.

    PubMed  CAS  Google Scholar 

  21. Haxhiu, M.A.; van Lunteren, E.; van de Graffe, W.B.; Strohl, D.P.; Bruce, E.N.; Mitra, J.; Cherniack, N.S. Action of nicotine on the respiratory activity of the diaphragm and genioglossus muscle and the nerves that innervate them. Respir. Physiol. 57:153–169; 1984.

    Article  PubMed  CAS  Google Scholar 

  22. Issa, F.G.; Sullivan, C.E. Arousal and breathing response to airway occlusion in healthy sleeping adults. J. Appl. Physiol. 55:1113–1119; 1983.

    PubMed  CAS  Google Scholar 

  23. Khoo, M.C.K.; Gottschalk, A.; Pack, A.I. Sleep induced periodic breathing and apnea: A theoretical study. J. Appl. Physiol. 70:2014–2024; 1991.

    PubMed  CAS  Google Scholar 

  24. Khoo, M.C.K.; Kronauer, K.E.; Strohl, K.P.; Slutsky, A.S. Factors inducing periodic breathing in humans: A general model. J. Appl. Physiol. 53:644–659; 1982.

    PubMed  CAS  Google Scholar 

  25. Krol, R.C.; Knuth, S.L.; Bartlett, Jr., D. Selective reduction of genioglossal muscle activity by alcohol in normal human subjects. Am. Rev. Respir. Dis. 129:247–250; 1984.

    PubMed  CAS  Google Scholar 

  26. Kronenberg, R.S.; Drage, C.W. Attenuation of the ventilatory and heart rate responses to hypoxia and hypercapnia with aging in normal men. J. Clin. Invest. 52:1812–1819; 1973.

    Article  PubMed  CAS  Google Scholar 

  27. Lahiri, S.; Maret, K.; Sherpa, M.G. Dependence of high altitude sleep apnea on ventilatory sensitivity to hypoxia. Respir. Physiol. 53:281–301; 1983.

    Article  Google Scholar 

  28. Littner, M.; Young, E.; McGinty, D.; Beahm, E.; Riege, W.; Sowers, J. Awake abnormalities of control of breathing and of the upper airway. Occurrence in healthy older men with nocturnal disordered breathing. Chest 86:573–579; 1984.

    PubMed  CAS  Google Scholar 

  29. Longobardo, G.S.; Cherniack, N.S.; Gothe, B. Factors affecting respiratory system stability. Ann. Biomed. Eng. 17:377–396; 1989.

    Article  PubMed  CAS  Google Scholar 

  30. Longobardo, G.S.; Gothe, B.; Goldman, M.D.; Cherniack, N.S. Sleep apnea considered as a control system instability. Respir. Physiol. 50:311–333; 1982.

    Article  PubMed  CAS  Google Scholar 

  31. Neubauer, J.A.; Santiago, T.V.; Edelman, N.H. Hypoxia arousal in intact and carotid chemodenervated sleeping cats. J. Appl. Physiol. 51:1294–1299; 1981.

    PubMed  CAS  Google Scholar 

  32. Önal, E.; Lopata, E. Periodic breathing and the pathogenesis of occlusive sleep apneas. Am. Rev. Respir. Dis. 126: 676–680; 1982.

    PubMed  Google Scholar 

  33. Önal, E.; Lopata, M.; O'Connor, T.D. Diaphragmatic and genioglossal electromyogram responses to CO2 rebreathing in humans. J. Appl. Physiol. 50:1052–1055; 1981.

    PubMed  Google Scholar 

  34. Orem, J.; Osorio, I.; Brooks, E.; Dick, T. Activity of respiratory neurons during NREM sleep. J. Neurophysiol. 54:1144–1156; 1985.

    PubMed  CAS  Google Scholar 

  35. Pack, A.I.; Cola, M.F.; Goldszmidt, A.; Ogilvie, M.D.; Gottschalk, A. Correlation between oscillations in ventilation and frequency content of the electroencephalogram. J. Appl. Physiol. 72:985–992; 1992.

    PubMed  CAS  Google Scholar 

  36. Pack, A.I.; Silage, D.A.; Millman, R.P., Knight, H.; Shore, E.T.; Chung, D.C. Spectral analysis of ventilation in elderly subjects awake and asleep. J. Appl. Physiol. 64:1257–1267; 1988.

    PubMed  CAS  Google Scholar 

  37. Peterson, D.D.; Pack, A.I.; Silage, D.A.; Fishman, A.P. Effects of aging on ventilatory and occlusion pressure responses to hypoxia and hypercapnia. Am. Rev. Respir. Dis. 124:387–391, 1981.

    PubMed  CAS  Google Scholar 

  38. Rajagopal, K.R.; Abbrecht, P.H.; Derderian, S.S.; Pickett, C.; Hofeldt, F.; Tellis, C.J.; Zwillich, C.W. Obstructive sleep apnea in hypothyroidism. Ann. Intern. Med. 101:491–494; 1984.

    PubMed  CAS  Google Scholar 

  39. Sauerland, E.K.; Harper, R.M. The human tongue during sleep: Electromyographic activity of the genioglossus muscle. Exp. Neurol. 51:160–170; 1976.

    Article  PubMed  CAS  Google Scholar 

  40. Skatrud, J.B.; Dempsey, J.A.; Badr, S.; Begle, R.L. Effect of airway impedance on CO2 retention and respiratory muscle activity during NREM sleep. J. Appl. Physiol. 65:1676–1685; 1988.

    PubMed  CAS  Google Scholar 

  41. Suratt, P.M.; Dee, P.; Atkinson, R.L.; Armstrong, P.; Wilhoit, S.C. Fluoroscopic and computed tomographic features of the pharyngeal airway in obstructive sleep apnea. Am. Rev. Respir. Dis. 127:487–492; 1983.

    PubMed  CAS  Google Scholar 

  42. Waggener, T.B.; Brusil, P.J.; Kronauer, R.E.; Gabel, R.A.; Inbar, G.F. Strength and cycle time of high-altitude ventilatory patterns in unacclimatized humans. J. Appl. Physiol. 56:576–581; 1984.

    PubMed  CAS  Google Scholar 

  43. Waggener, T.B.; Stark, A.R.; Cohlan, B.A.; Frantz, III, I.D. Apnea duration is related, to ventilatory oscillation characteristics in newborn infants. J. Appl. Physiol. 57:536–544; 1984.

    PubMed  CAS  Google Scholar 

  44. Weiner, D.; Mitra, J.; Salamone, J.; Cherniack, N.S. Effect of chemical stimuli on nerves supplying upper airway muscles. J. Appl. Physiol. 52:530–536; 1982.

    PubMed  CAS  Google Scholar 

  45. White, D.P.; Gleason, K.; Pickett, C.K.; Rannels, A.M.; Cymerman, A.; Weil, J.V. Altitude acclimatization: Influence on periodic breathing and chemoresponsiveness during sleep. J. Appl. Physiol. 63:401–412; 1987.

    PubMed  CAS  Google Scholar 

  46. Younes, M. The physiologic basis of central apnea and periodic breathing. Curr. Pulmonol. 10:265–326; 1989.

    Google Scholar 

  47. Zwillich, C.W.; Pierson, D.J.; Hofeldt, F.D.; Lufkin, E.G.; Weil, J.W. Ventilatory control in myxedema and hypothyroidism. N. Engl. J. Med. 292:662–665; 1975.

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Pulmonary and Critical Care Division, Department of Medicine, University of Pennsylvania Medical Center, Philadelphia, PA

    Allan I. Pack

  2. Department of Anesthesia, University of Pennsylvania Medical Center, Philadelphia, PA

    Allan I. Pack & Allan Gottschalk

  3. Center for Sleep and Respiratory Neurobiology, University of Pennsylvania Medical Center, Philadelphia, PA

    Allan Gottschalk

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  1. Allan I. Pack
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Pack, A.I., Gottschalk, A. Mechanisms of ventilatory periodicities. Ann Biomed Eng 21, 537–544 (1993). https://doi.org/10.1007/BF02584336

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