Ventilatory oscillations at exercise: Effects of hyperoxia, hypercapnia, and acetazolamide

Physiological Reports

Volumn 3, Issue 6, 2015, Pages

  Hermand, Eric ^a   Lhuissier, François J ^a,b   Larribaut, Julie ^a   Pichon, Aurélien ^a   Richalet, Jean Paul ^a,b  

^a UNIVERSITÉ PARIS 13   (France)

^b AVICENNE HOSPITAL   (France)

Author keywords

Acetazolamide; Exercise; Hypercapnia; Hyperoxia; Hypoxia; Periodic breathing; Ventilatory oscillations

Indexed keywords

ACETAZOLAMIDE; PLACEBO;

ADULT; AEROBIC CAPACITY; ARTICLE; BICYCLE ERGOMETER; CLINICAL ARTICLE; CLINICAL TRIAL; CROSSOVER PROCEDURE; DOUBLE BLIND PROCEDURE; END TIDAL CARBON DIOXIDE TENSION; EXERCISE; FOURIER TRANSFORMATION; HEART OUTPUT; HUMAN; HYPERCAPNIA; HYPEROXIA; INFRARED SPECTROSCOPY; INSPIRATORY TIME; MALE; MEDICAL PROCEDURES; NORMAL HUMAN; NORMOXIA; OXYGEN SATURATION; PULSE OXIMETRY; RESPIRATORY FUNCTION; RESPIRATORY TRACT PARAMETERS; TIDAL VOLUME; TOTAL RESPIRATORY CYCLE TIME; VENTILATORY OSCILLATION; YOUNG ADULT;

EID: 85006062430     PISSN: None     EISSN: 2051817X     Source Type: Journal    
DOI: 10.14814/phy2.12446     Document Type: Article

References (61)

1. Agostoni, P. 2008. Mechanisms of periodic breathing during exercise in patients with chronic heart failure. CHEST J. 133:197.
2. Ainslie, P. N., S. J. E. Lucas, and K. R. Burgess. 2013. Breathing and sleep at high altitude. Respir. Physiol. Neurobiol. 188:233-256.
3. Andreas, S., C. Clemens, H. Sandholzer, H. R. Figulla, and H. Kreuzer. 1996. Improvement of exercise capacity with treatment of Cheyne-Stokes respiration in patients with congestive heart failure. J. Am. Coll. Cardiol. 27:1486-1490.
4. Andreas, S., K. Weidel, G. Hagenah, and S. Heindl. 1998. Treatment of Cheyne-Stokes respiration with nasal oxygen and carbon dioxide. Eur. Respir. J. 12:414-419.
5. Apostolo, A., P. Agostoni, M. Contini, L. Antonioli, and E. R. Swenson. 2014. Acetazolamide and inhaled carbon dioxide reduce periodic breathing during exercise in patients with chronic heart failure. J. Card. Fail. doi:10.1016/j.cardfail.2014.01.007.
6. Basner, R. C. 2011. Loop gain: can it help close the heart failure-periodic breathing loop? Am. J. Respir. Crit. Care Med. 184:996-997.
7. Berssenbrugge, A., J. Dempsey, C. Iber, J. Skatrud, and P. Wilson. 1983. Mechanisms of hypoxia-induced periodic breathing during sleep in humans. J. Physiol. 343:507-524.
8. 2: peripheral-central chemoreceptor interdependence. J. Physiol. 588:2455-2471.
9. Bourdillon, N., J.-L. Fan, and B. Kayser. 2014. Cerebral oxygenation during the Richalet hypoxia sensitivity test and cycling time-trial performance in severe hypoxia. Eur. J. Appl. Physiol. 114:1037-1048.
10. Brack, T., W. Randerath, and K. E. Bloch. 2012. Cheyne-Stokes respiration in patients with heart failure: prevalence, causes, consequences and treatments. Respiration 83:165-176.
11. Burgess, K. R. 2012. New insights from the measurement of loop gain in obstructive sleep apnoea. J. Physiol. 590:1781-1782.
12. Canouï-Poitrine, F., K. Veerabudun, P. Larmignat, M. Letournel, S. Bastuji-Garin, and J.-P. Richalet. 2014. Risk prediction score for severe high altitude illness: a cohort study. PLoS ONE 9:e100642.
13. Charloux, A., E. Lonsdorfer-Wolf, R. Richard, E. Lampert, M. Oswald-Mammosser, B. Mettauer, et al. 2000. A new impedance cardiograph device for the non-invasive evaluation of cardiac output at rest and during exercise: comparison with the “direct” Fick method. Eur. J. Appl. Physiol. 82:313-320.
14. Cherniack, N. S. 2005. Mathematical models of periodic breathing and their usefulness in understanding cardiovascular and respiratory disorders. Exp. Physiol. 91:295-305.
15. Dempsey, J. A., C. A. Smith, T. Przybylowski, B. Chenuel, A. Xie, H. Nakayama, et al. 2004. The ventilatory responsiveness to CO(2) below eupnoea as a determinant of ventilatory stability in sleep. J. Physiol. 560:1-11.
16. Dempsey, J. A., S. C. Veasey, B. J. Morgan, and C. P. O’Donnell. 2010. Pathophysiology of sleep apnea. Physiol. Rev. 90:47-112.
17. Dhakal, B. P., R. M. Murphy, and G. D. Lewis. 2012. Exercise oscillatory ventilation in heart failure. Trends Cardiovasc. Med. 22:185-191.
18. Duffin, J., and J. H. Mateika. 2013. Cross-Talk opposing view: peripheral and central chemoreflexes have additive effects on ventilation in humans. J. Physiol. 591:4351-4353.
19. Edwards, B. A., S. A. Sands, D. J. Eckert, D. P. White, J. P. Butler, R. L. Owens, et al. 2012. Acetazolamide improves loop gain but not the other physiological traits causing obstructive sleep apnoea. J. Physiol. 590:1199-1211.
20. Fan, J.-L., K. R. Burgess, K. N. Thomas, S. J. E. Lucas, J. D. Cotter, B. Kayser, et al. 2012. Effects of acetazolamide on cerebrovascular function and breathing stability at 5,050 m. J. Physiol. 590:1213-1225.
21. Fischer, R., S. M. Lang, M. Leitl, M. Thiere, U. Steiner, and R. M. Huber. 2004. Theophylline and acetazolamide reduce sleep-disordered breathing at high altitude. Eur. Respir. J. 23:47-52.
22. Fontana, M., M. Emdin, A. Giannoni, G. Iudice, R. Baruah, and C. Passino. 2011. Effect of acetazolamide on chemosensitivity, Cheyne-Stokes respiration, and response to effort in patients with heart failure. Am. J. Cardiol. 107:1675-1680.
23. Forster, H., J. Bonis, K. Krause, J. Wenninger, S. Neumueller, M. Hodges, et al. 2014. Contributions of the pre-B€otzinger complex and the K€olliker-fuse nuclei to respiratory rhythm and pattern generation in awake and sleeping goats. Prog. Brain Res. 209:73-89.
24. Francis, D. P., K. Willson, L. C. Davies, A. J. Coats, and M. Piepoli. 2000. Quantitative general theory for periodic breathing in chronic heart failure and its clinical implications. Circulation 102:2214-2221.
25. Franklin, K. A., P. Eriksson, C. Sahlin, and R. Lundgren. 1997. Reversal of central sleep apnea with oxygen. Chest 111:163-169.
26. Garde, A., B. F. Giraldo, R. Jane, T. D. Latshang, A. J. Turk, T. Hess, et al. 2012. Periodic breathing during ascent to extreme altitude quantified by spectral analysis of the respiratory volume signal. Conf. Proc. IEEE Eng. Med. Biol. Soc. 2012:707-710.
27. Giannoni, A., M. Emdin, F. Bramanti, G. Iudice, D. P. Francis, A. Barsotti, et al. 2009. Combined increased chemosensitivity to hypoxia and hypercapnia as a prognosticator in heart failure. J. Am. Coll. Cardiol. 53:1975-1980.
28. Gold, A. R., E. R. Bleecker, and P. L. Smith. 1985. A shift from central and mixed sleep apnea to obstructive sleep apnea resulting from low-flow oxygen. Am. Rev. Respir. Dis. 132:220-223.
29. Gonzales, J. U., and B. W. Scheuermann. 2013. Effect of acetazolamide on respiratory muscle fatigue in humans. Respir. Physiol. Neurobiol. 185:386-392.
30. Hermand, E., A. Pichon, F. J. Lhuissier, and J.-P. Richalet. 2015. Periodic breathing in healthy humans at exercise in hypoxia. J. Appl. Physiol. 118:115-123.
31. Hudgel, D. W., C. Hendricks, and A. Dadley. 1988. Alteration in obstructive apnea pattern induced by changes in oxygenand carbon-dioxide-inspired concentrations. Am. Rev. Respir. Dis. 138:16-19.
32. Javaheri, S., S. A. Sands, and B. A. Edwards. 2014. Acetazolamide attenuates hunter-cheyne-stokes breathing but augments the hypercapnic ventilatory response in patients with heart failure. Ann. Am. Thorac. Soc. 11:80-86.
33. Kumar, P., and N. R. Prabhakar (2012). Peripheral chemoreceptors: function and plasticity of the carotid body in R. Terjung, ed. Comprehensive physiology. John Wiley & Sons, Inc., Hoboken, NJ, USA. Available at: http://doi.wiley.com/10.1002/cphy.c100069 [Accessed March 31, 2014].
34. 2/H(+) sensing: peripheral and central chemoreception. Int. J. Biochem. Cell Biol. 35:1413-1435.
35. Lahiri, S., A. Roy, S. M. Baby, T. Hoshi, G. L. Semenza, and N. R. Prabhakar. 2006. Oxygen sensing in the body. Prog. Biophys. Mol. Biol. 91:249-286.
36. Lalande, S., E. M. Snyder, T. P. Olson, M. L. Hulsebus, M. Orban, V. K. Somers, et al. 2009. The effects of sildenafil and acetazolamide on breathing efficiency and ventilatory control during hypoxic exercise. Eur. J. Appl. Physiol. 106:509-515.
37. Lhuissier, F. J., M. Brumm, D. Ramier, and J.-P. Richalet. 2012. Ventilatory and cardiac responses to hypoxia at submaximal exercise are independent of altitude and exercise intensity. J. Appl. Physiol. 112:566-570.
38. Lorenzi-Filho, G., F. Rankin, I. Bies, and T. Douglas Bradley. 1999. Effects of inhaled carbon dioxide and oxygen on cheyne-stokes respiration in patients with heart failure. Am. J. Respir. Crit. Care Med. 159:1490-1498.
39. 2 in heart failure patients: reliability of the single-breath test. Physiol. Meas. 34:1123-1132.
40. 2 saturation without changing control of ventilation. High Alt. Med. Biol. 1:197-206.
41. Mohan, R., and J. Duffin. 1997. The effect of hypoxia on the ventilatory response to carbon dioxide in man. Respir. Physiol. 108:101-115.
42. Moraga, F. A., D. Jim_enez, J. P. Richalet, M. Vargas, and J. Osorio. 2014. Periodic breathing and oxygen supplementation in Chilean miners at high altitude (4200 m). Respir. Physiol. Neurobiol. 203:109-115.
43. Ogoh, S., and P. N. Ainslie. 2009. Cerebral blood flow during exercise: mechanisms of regulation. J. Appl. Physiol. 107:1370-1380.
44. Okazawa, H., H. Yamauchi, K. Sugimoto, H. Toyoda, Y. Kishibe, and M. Takahashi. 2001. Effects of acetazolamide on cerebral blood flow, blood volume, and oxygen metabolism: a positron emission tomography study with healthy volunteers. J. Cereb. Blood Flow Metab. 21:1472-1479.
45. Pinna, G. D., R. Maestri, A. Mortara, and M. T. La Rovere. 2000. Cardiorespiratory interactions during periodic breathing in awake chronic heart failure patients. Am. J. Physiol. Heart Circ. Physiol. 278:H932-H941.
46. Ponikowski, P., S. D. Anker, T. P. Chua, D. Francis, W. Banasiak, P. A. Poole-Wilson, et al. 1999. Oscillatory breathing patterns during wakefulness in patients with chronic heart failure: clinical implications and role of augmented peripheral chemosensitivity. Circulation 100:2418-2424.
47. Read, D. J. 1967. A clinical method for assessing the ventilatory response to carbon dioxide. Australas Ann. Med. 16:20-32.
48. Richalet, J.-P., M. Rivera, P. Bouchet, E. Chirinos, I. Onnen, O. Petitjean, et al. 2005. Acetazolamide: a treatment for chronic mountain sickness. Am. J. Respir. Crit. Care Med. 172:1427-1433.
49. Richalet, J.-P., P. Larmignat, E. Poitrine, M. Letournel, and F. Canouï-Poitrine. 2012. Physiological risk factors for severe high-altitude illness: a prospective cohort study. Am. J. Respir. Crit. Care Med. 185:192-198.
50. Richard, R., E. Lonsdorfer-Wolf, A. Charloux, S. Doutreleau, M. Buchheit, M. Oswald-Mammosser, et al. 2001. Noninvasive cardiac output evaluation during a maximal progressive exercise test, using a new impedance cardiograph device. Eur. J. Appl. Physiol. 85:202-207.
51. Rivera-Ch, M., L. Huicho, P. Bouchet, J. P. Richalet, and F. León-Velarde. 2008. Effect of acetazolamide on ventilatory response in subjects with chronic mountain sickness. Respir. Physiol. Neurobiol. 162:184-189.
52. Sinski, M., J. Lewandowski, J. Przybylski, P. Zalewski, B. Symonides, P. Abramczyk, et al. 2014. Deactivation of carotid body chemoreceptors by hyperoxia decreases blood pressure in hypertensive patients. Hypertens. Res. 37:858-862.
53. Skow, R. J., M. M. Tymko, C. M. MacKay, C. D. Steinback, and T. A. Day. 2014. The effects of head-up and head-down tilt on central respiratory chemoreflex loop gain tested by hyperoxic rebreathing. Prog. Brain Res. 212:149-172.
54. Solin, P., T. Roebuck, D. P. Johns, E. H. Walters, and M. T. Naughton. 2000. Peripheral and central ventilatory responses in central sleep apnea with and without congestive heart failure. Am. J. Respir. Crit. Care Med. 162:2194-2200.
55. Swenson, E. R. 1998. Carbonic anhydrase inhibitors and ventilation: a complex interplay of stimulation and suppression. Eur. Respir. J. 12:1242-1247.
56. Swenson, E. R., K. L. Leatham, R. C. Roach, R. B. Schoene, W. J. Jr Mills, and P. H. Hackett. 1991. Renal carbonic anhydrase inhibition reduces high altitude sleep periodic breathing. Respir. Physiol. 86:333-343.
57. Teppema, L. J. 2014. Multifaceted clinical effects of acetazolamide: will the underlying mechanisms please stand up? J. Appl. Physiol. 116:713-714.
58. Vovk, A., J. Duffin, J. M. Kowalchuk, D. H. Paterson, and D. A. Cunningham. 2000. Changes in chemoreflex characteristics following acute carbonic anhydrase inhibition in humans at rest. Exp. Physiol. 85:847-856.
59. Waggener, T. B., P. J. Brusil, R. E. Kronauer, R. A. Gabel, and G. F. Inbar. 1984. Strength and cycle time of high-altitude ventilatory patterns in unacclimatized humans. J. Appl. Physiol. 56:576-581.
60. White, D. P. 2005. Pathogenesis of Obstructive and Central Sleep Apnea. Am. J. Respir. Crit. Care Med. 172:1363-1370.
61. Younes, M., M. Ostrowski, W. Thompson, C. Leslie, and W. Shewchuk. 2001. Chemical control stability in patients with obstructive sleep apnea. Am. J. Respir. Crit. Care Med. 163:1181-1190.