Sympathetic and cardiovascular responses to glossopharyngeal insufflation in trained apnea divers

Journal of Applied Physiology

Volumn 109, Issue 6, 2010, Pages 1728-1735

  Heusser, Karsten ^a   Dzamonja, Gordan ^b   Breskovic, Toni ^c   Steinback, Craig D ^d   Diedrich, André ^e   Tank, Jens ^a   Jordan, Jens ^a   Dujic, Zeljko ^c  

^a HANNOVER MEDICAL SCHOOL   (Germany)

^b UNIVERSITY HOSPITAL SPLIT   (Croatia)

^c UNIVERSITY OF SPLIT   (Croatia)

^d UNIVERSITY OF WESTERN ONTARIO   (Canada)

^e VANDERBILT UNIVERSITY   (United States)

Author keywords

Baroreflex; Breath hold diving; Chemoreflex; Sympathetic nervous system

Indexed keywords

ADRENERGIC SYSTEM; ADULT; AERATION; APNEA; ARTICLE; BLOOD PRESSURE; CARDIOVASCULAR SYSTEM; CLINICAL TRIAL; CONTROLLED CLINICAL TRIAL; CONTROLLED STUDY; CROSSOVER PROCEDURE; DIVING; FEMALE; GLOSSOPHARYNGEAL NERVE; HEART OUTPUT; HEART RATE; HEMODYNAMICS; HUMAN; INNERVATION; MALE; PATHOPHYSIOLOGY; PERONEUS NERVE; PRESSORECEPTOR REFLEX; PROSPECTIVE STUDY; RANDOMIZED CONTROLLED TRIAL; TIME; VASODILATATION;

ADULT; APNEA; BAROREFLEX; BLOOD PRESSURE; CARDIAC OUTPUT; CARDIOVASCULAR SYSTEM; CROSS-OVER STUDIES; DIVING; FEMALE; GLOSSOPHARYNGEAL NERVE; HEART RATE; HEMODYNAMICS; HUMANS; INSUFFLATION; MALE; PERONEAL NERVE; PROSPECTIVE STUDIES; SYMPATHETIC NERVOUS SYSTEM; TIME FACTORS; VASODILATION; YOUNG ADULT;

EID: 78651316711     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.00522.2010     Document Type: Article

References (59)

1. Abboud FM, Eckberg DL, Johannsen UJ, Mark AL. Carotid and cardiopulmonary baroreceptor control of splanchnic and forearm vascular resistance during venous pooling in man. J Physiol 286:173-184, 1979.
2. Andersson JP, Liner MH, Jonsson H. Asystole and increased serum myoglobin levels associated with "packing blackout" in a competitive breath-hold diver. Clin Physiol Funct Imaging 29:458-461, 2009.
3. Baily RG, Prophet SA, Shenberger JS, Zelis R, Sinoway LI. Direct neurohumoral evidence for isolated sympathetic nervous system activation to skeletal muscle in response to cardiopulmonary baroreceptor unloading. Circ Res 66:1720-1728, 1990.
4. Berg JT, Deem S, Kerr ME, Swenson ER. Hemoglobin and red blood cells alter the response of expired nitric oxide to mechanical forces. Am J Physiol Heart Circ Physiol 279: H2947-H2953, 2000.
5. Breskovic T, Ivancev V, Banic I, Jordan J, Dujic Z. Peripheral chemoreflex sensitivity and sympathetic nerve activity are normal in apnea divers during training season. Auton Neurosci 154:42-47, 2010.
6. Breskovic T, Valic Z, Lipp A, Heusser K, Ivancev V, Tank J, Dzamonja G, Jordan J, Shoemaker JK, Eterovic D, Dujic Z. Peripheral chemoreflex regulation of sympathetic vasomotor tone in apnea divers. Clin Auton Res 20:57-63, 2010.
7. Cannon RO 3rd, Schechter AN, Panza JA, Ognibene FP, Pease-Fye ME, Waclawiw MA, Shelhamer JH, Gladwin MT. Effects of inhaled nitric oxide on regional blood flow are consistent with intravascular nitric oxide delivery. J Clin Invest 108:279-287, 2001.
8. De Wet CJ, Affleck DG, Jacobsohn E, Avidan MS, Tymkew H, Hill LL, Zanaboni PB, Moazami N, Smith JR. Inhaled prostacyclin is safe, effective, and affordable in patients with pulmonary hypertension, right heart dysfunction, and refractory hypoxemia after cardiothoracic surgery. J Thorac Cardiovasc Surg 127:1058-1067, 2004.
9. Dejours P. Hazards of hypoxia during diving. In: Physiology of Breath-Hold Diving and the Ama of Japan Papers, edited by Rahn H. Washington, DC: National Academy of Sciences-National Research Council, 1965, p. 183-193.
10. Duffy SJ, Tran BT, New G, Tudball RN, Esler MD, Harper RW, Meredith IT. Continuous release of vasodilator prostanoids contributes to regulation of resting forearm blood flow in humans. Am J Physiol Heart Circ Physiol 274: H1174-H1183, 1998.
11. Dujic Z, Ivancev V, Heusser K, Dzamonja G, Palada I, Valic Z, Tank J, Obad A, Bakovic D, Diedrich A, Joyner MJ, Jordan J. Central chemoreflex sensitivity and sympathetic neural outflow in elite breath-hold divers. J Appl Physiol 104:205-211, 2008.
12. 2) in the dog. Br J Pharmacol 64:315-320, 1978.
13. Eichinger M, Walterspacher S, Scholz T, Tetzlaff R, Puderbach M, Tetzlaff K, Kopp-Schneider A, Ley S, Choe K, Kauczor HU, Sorichter S. Glossopharyngeal insufflation and pulmonary hemodynamics in elite breath hold divers. Med Sci Sports Exerc 42:1688-1695, 2010.
14. Eling TE, Ally AI. Pulmonary biosynthesis and metabolism of prostaglandins and related substances. Environ Health Perspect 55:159-168, 1984.
15. Ellsworth ML, Gregory TJ, Newell JC. Pulmonary prostacyclin production with increased flow and sympathetic stimulation. J Appl Physiol 55:1225-1231, 1983.
16. Ferretti G. Extreme human breath-hold diving. Eur J Appl Physiol 84:254-271, 2001.
17. Ferrigno M, Hickey DD, Liner MH, Lundgren CE. Cardiac performance in humans during breath holding. J Appl Physiol 60:1871-1877, 1986.
18. Hawkings HJ, Smith JB, Nicolaou KC, Eling TE. Studies of the mechanisms involved in the fate of prostacyclin (PGI2) and 6-keto-PGF1alpha in the pulmonary circulation. Prostaglandins 16:871-884, 1978.
19. Heistad DD, Wheeler RC. Effect of acute hypoxia on vascular responsiveness in man. I. Responsiveness to lower body negative pressure and ice on the forehead. II. Responses to norepinephrine and angiotensin. III. Effect of hypoxia and hypocapnia. J Clin Invest 49:1252-1265, 1970.
20. Heusser K, Dzamonja G, Tank J, Palada I, Valic Z, Bakovic D, Obad A, Ivancev V, Breskovic T, Diedrich A, Joyner MJ, Luft FC, Jordan J, Dujic Z. Cardiovascular regulation during apnea in elite divers. Hypertension 53:719-724, 2009.
21. Heusser K, Tank J, Diedrich A, Engeli S, Klaua S, Kruger N, Strauss A, Stoffels G, Luft FC, Jordan J. Influence of sibutramine treatment on sympathetic vasomotor tone in obese subjects. Clin Pharmacol Ther 79:500-508, 2006.
22. Jia L, Bonaventura C, Bonaventura J, Stamler JS. S-nitrosohaemoglobin: a dynamic activity of blood involved in vascular control. Nature 380:221-226, 1996. (Pubitemid 26090643)
23. Johnson JM, Rowell LB, Niederberger M, Eisman MM. Human splanchnic and forearm vasoconstrictor responses to reductions of right atrial and aortic pressures. Circ Res 34:515-524, 1974.
24. Joyner MJ, Dietz NM. Sympathetic vasodilation in human muscle. Acta Physiol Scand 177:329-336, 2003.
25. Kelm M, Schrader J. Control of coronary vascular tone by nitric oxide. Circ Res 66:1561-1575, 1990.
26. Kisch-Wedel H, Kemming G, Meisner F, Flondor M, Kuebler WM, Bruhn S, Koehler C, Zwissler B. The prostaglandins epoprostenol and iloprost increase left ventricular contractility in vivo. Intensive Care Med 29:1574-1583, 2003.
27. Lahana A, Costantopoulos S, Nakos G. The local component of the acute cardiovascular response to simulated apneas in brain-dead humans. Chest 128:634-639, 2005.
28. Lepori M, Sartori C, Duplain H, Nicod P, Scherrer U. Interaction between cholinergic and nitrergic vasodilation: a novel mechanism of blood pressure control. Cardiovasc Res 51:767-772, 2001.
29. Levy JV. Contractile responses to prostacyclin (PGI2) of isolated human saphenous and rat venous tissue. Prostaglandins 16:93-97, 1978.
30. Lindholm P, Nyren S. Studies on inspiratory and expiratory glossopharyngeal breathing in breath-hold divers employing magnetic resonance imaging and spirometry. Eur J Appl Physiol 94:646-651, 2005.
31. Loring SH, O'Donnell CR, Butler JP, Lindholm P, Jacobson F, Ferrigno M. Transpulmonary pressures and lung mechanics with glossopharyngeal insufflation and exsufflation beyond normal lung volumes in competitive breath-hold divers. J Appl Physiol 102:841-846, 2007.
32. Lundberg JO, Weitzberg E, Gladwin MT. The nitrate-nitrite-nitric oxide pathway in physiology and therapeutics. Nat Rev Drug Discov 7:156-167, 2008.
33. Macefield VG, Gandevia SC, Henderson LA. Neural sites involved in the sustained increase in muscle sympathetic nerve activity induced by inspiratory capacity apnea: a fMRI study. J Appl Physiol 100:266-273, 2006.
34. Macefield VG, Wallin BG. Effects of static lung inflation on sympathetic activity in human muscle nerves at rest and during asphyxia. J Auton Nerv Syst 53:148-156, 1995.
35. Mathews L, Singh RK. Cardiac output monitoring. Ann Card Anaesth 11:56-68, 2008.
36. Novalija J, Lindholm P, Loring SH, Diaz E, Fox JA, Ferrigno M. Cardiovascular aspects of glossopharyngeal insufflation and exsufflation. Undersea Hyperb Med 34:415-423, 2007.
37. CO2 on apnea performance in trained breath-hold divers. Eur J Appl Physiol 97:158-164, 2006.
38. Pang CC. Autonomic control of the venous system in health and disease: effects of drugs. Pharmacol Ther 90:179-230, 2001.
39. Persson MG, Lonnqvist PA, Gustafsson LE. Positive end-expiratory pressure ventilation elicits increases in endogenously formed nitric oxide as detected in air exhaled by rabbits. Anesthesiology 82:969-974, 1995.
40. 2 stability. Thromb Res 88:41-49, 1997.
41. Potkin R, Cheng V, Siegel R. Effects of glossopharyngeal insufflation on cardiac function: an echocardiographic study in elite breath-hold divers. J Appl Physiol 103:823-827, 2007.
42. Rassaf T, Kleinbongard P, Preik M, Dejam A, Gharini P, Lauer T, Erckenbrecht J, Duschin A, Schulz R, Heusch G, Feelisch M, Kelm M. Plasma nitrosothiols contribute to the systemic vasodilator effects of intravenously applied NO: experimental and clinical study on the fate of NO in human blood. Circ Res 91:470-477, 2002.
43. Sandberg KL, Lindstrom DP, Krueger ED, Sundell H, Cotton RB. Measurement of tidal volume during high frequency ventilation by impedance plethysmography. Pediatr Res 23:253-256, 1988.
44. Scherhag A, Pfleger S, Grosselfinger R, Borggrefe M. Does competitive apnea diving have a long-term risk? Cardiopulmonary findings in breathhold divers. Clin J Sport Med 15:95-97, 2005.
45. Schuller-Petrovic S, Siedler S, Kern T, Meinhart J, Schmidt K, Brunner F. Imbalance between the endothelial cell-derived contracting factors prostacyclin and angiotensin II and nitric oxide/cyclic GMP in human primary varicosis. Br J Pharmacol 122:772-778, 1997.
46. Seccombe LM, Chung SC, Jenkins CR, Frater CJ, Mackey DW, Pearson MA, Emmett L, Peters MJ. Lung perfusion and chest wall configuration is altered by glossopharyngeal breathing. Eur Respir J 36:151-156, 2010.
47. Simmons GH, Minson CT, Cracowski JL, Halliwill JR. Systemic hypoxia causes cutaneous vasodilation in healthy humans. J Appl Physiol 103:608-615, 2007.
48. 2) contracts normal and varicose human saphenous veins. Vasa 13:228-230, 1984.
49. Skarphedinsson JO, Elam M, Jungersten L, Wallin BG. Sympathetic nerve traffic correlates with the release of nitric oxide in humans: implications for blood pressure control. J Physiol 501:671-675, 1997.
50. Skinner SJ, Somervell CE, Olson DM. The effects of mechanical stretching on fetal rat lung cell prostacyclin production. Prostaglandins 43:413-433, 1992.
51. Stamler JS, Jaraki O, Osborne J, Simon DI, Keaney J, Vita J, Singel D, Valeri CR, Loscalzo J. Nitric oxide circulates in mammalian plasma primarily as an S-nitroso adduct of serum albumin. Proc Natl Acad Sci USA 89:7674-7677, 1992.
52. Stromberg S, Lonnqvist PA, Persson MG, Gustafsson LE. Lung distension and carbon dioxide affect pulmonary nitric oxide formation in the anaesthetized rabbit. Acta Physiol Scand 159:59-67, 1997.
53. Szczeklik J, Szczeklik A, Nizankowski R. Haemodynamic changes induced by prostacyclin in man. Br Heart J 44:254-258, 1980.
54. Tamisier R, Norman D, Anand A, Choi Y, Weiss JW. Evidence of sustained forearm vasodilatation after brief isocapnic hypoxia. J Appl Physiol 96:1782-1787, 2004.
55. Vallbo AB, Hagbarth KE, Torebjork HE, Wallin BG. Somatosensory, proprioceptive, and sympathetic activity in human peripheral nerves. Physiol Rev 59:919-957, 1979.
56. van Grondelle A, Worthen GS, Ellis D, Mathias MM, Murphy RC, Strife RJ, Reeves JT, Voelkel NF. Altering hydrodynamic variables influences PGI2 production by isolated lungs and endothelial cells. J Appl Physiol 57:388-395, 1984.
57. von Bethmann AN, Brasch F, Nusing R, Vogt K, Volk HD, Muller KM, Wendel A, Uhlig S. Hyperventilation induces release of cytokines from perfused mouse lung. Am J Respir Crit Care Med 157:263-272, 1998. (Pubitemid 28071291)
58. Vonk-Noordegraaf A, van Wolferen SA, Marcus JT, Boonstra A, Postmus PE, Peeters JW, Peacock AJ. Noninvasive assessment and monitoring of the pulmonary circulation. Eur Respir J 25:758-766, 2005.
59. 15N-labelled S-nitrosoalbumin in the rat: possible mechanistic and biological implications. J Chromatogr B Analyt Technol Biomed Life Sci 877:1375-1387, 2009.