Breath-hold diving as a brain survival response

Translational Neuroscience

Volumn 4, Issue 3, 2013, Pages 302-313

  Dujic, Zeljko ^a   Breskovic, Toni ^a   Bakovic, Darija ^a  

^a UNIVERSITY OF SPLIT   (Croatia)

Author keywords

Apnea; Brain oxygenation; Brain perfusion; Breath hold diving

Indexed keywords

ACTION POTENTIAL; ADAPTATION; APNEA; BLOOD PRESSURE; BRAIN; BRAIN BLOOD FLOW; BRAIN PERFUSION; BREATH HOLD DIVING; BREATH HOLDING; BREATHING MECHANICS; DIVING; FAINTNESS; HEART OUTPUT; HEART RHYTHM; HUMAN; HYDROSTATIC PRESSURE; HYPERCAPNIA; HYPOXIA; INVOLUNTARY MOVEMENT; MUSCLE SYMPATHETIC NERVE ACTIVITY; NONHUMAN; PRIORITY JOURNAL; REVIEW; SPLEEN; SYMPATHETIC NERVE CELL; TISSUE OXYGENATION; TOTAL LUNG CAPACITY;

EID: 84893018784     PISSN: 20813856     EISSN: 20816936     Source Type: Journal    
DOI: 10.2478/s13380-013-0130-5     Document Type: Review

References (81)

1. Lindholm P., Loss of motor control and/or loss of consciousness during breath-hold competitions, Int. J. Sports Med., 2007, 28, 295-299
2. Dujic Z., Breskovic T., Impact of breath holding on cardiovascular respiratory and cerebrovascular health, Sports Med., 2012, 42, 459-472
3. Muth C.M., Radermacher P., Pittner A., Steinacker J., Schabana R., Hamich S., et al., Arterial blood gases during diving in elite apnea divers, Int. J. Sports Med., 2003, 24, 104-107
4. Breskovic T., Uglesic L., Zubin P., Kuch B., Kraljevic J., Zanchi J., et al., Cardiovascular changes during underwater static and dynamic breath-hold dives in trained divers, J. Appl. Physiol, 2011, 111, 673-678
5. Kuch B., Koss B., Dujic Z., Buttazzo G., Sieber A., A novel wearable apnea dive computer for continuous plethysmographic monitoring of oxygen saturation and heart rate, Diving. Hyperb. Med., 2010, 40, 34-40
6. Tocco F., Marongiu E., Pinna M., Roberto S., Pusceddu M., Angius L., et al., Assessment of circulatory adjustments during underwater apnoea in elite divers by means of a portable device, Acta. Physiol. (Oxf), 2013, 207, 290-298
7. 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, 2005, 94, 646-651
8. Novalija J., Lindholm P., Loring S.H., Diaz E., Fox J.A., Ferrigno M., Cardiovascular aspects of glossopharyngeal insufflation and exsufflation, Undersea Hyperb. Med., 2007, 34, 415-423
9. Ferrigno M., Hickey D.D., Liner M.H., Lundgren C.E., Cardiac performance in humans during breath holding, J. Appl. Physiol, 1986, 60, 1871-1877
10. Potkin R., Cheng V., Siegel R., Effects of glossopharyngeal insufflation on cardiac function: an echocardiographic study in elite breath-hold divers, J. Appl. Physiol, 2007, 103, 823-827
11. Batinic T., Utz W., Breskovic T., Jordan J., Schulz-Menger J., Jankovic S., et al., Cardiac magnetic resonance imaging during pulmonary hyperinflation in apnea divers, Med. Sci. Sports Exerc., 2011, 43, 2095-2101
12. Palada I., Bakovic D., Valic Z., Obad A., Ivancev V., Eterovic D., et al., Restoration of hemodynamics in apnea struggle phase in association with involuntary breathing movements, Respir. Physiol. Neurobiol., 2008, 161, 174-181
13. Palada I., Obad A., Bakovic D., Valic Z., Ivancev V., Dujic Z., Cerebral and peripheral hemodynamics and oxygenation during maximal dry breath-holds, Respir. Physiol. Neurobiol., 2007, 157, 374-381
14. Bakovic D., Valic Z., Eterovic D., Vukovic I., Obad A., Marinovic-Terzic I., et al., Spleen volume and blood flow response to repeated breathhold apneas, J. Appl. Physiol., 2003, 95, 1460-1466
15. Heusser K., Dzamonja G., Tank J., Palada I., Valic Z., Bakovic D., et al., Cardiovascular regulation during apnea in elite divers, Hypertension, 2009, 53, 719-724
16. Joulia F., Steinberg J.G., Wolff F., Gavarry O., Jammes Y., Reduced oxidative stress and blood lactic acidosis in trained breath-hold human divers, Respir. Physiol. Neurobiol., 2002, 133, 121-130
17. Liner M.H., Ferrigno M., Lundgren C.E., Alveolar gas exchange during simulated breath-hold diving to 20 m, Undersea Hyperb. Med., 1993, 20, 27-38
18. Ferretti G., Extreme human breath-hold diving, Eur. J. Appl. Physiol., 2001, 84, 254-271
19. Fagius J., Sundlof G., The diving response in man: effects on sympathetic activity in muscle and skin nerve fascicles, J. Physiol., 1986, 377, 429-443
20. Kiviniemi A.M., Breskovic T., Uglesic L., Kuch B., Maslov P.Z., Sieber A., et al., Heart rate variability during static and dynamic breath-hold dives in elite divers, Auton. Neurosci., 2012, 169, 95-101
21. Schagatay E., Andersson J.P., Hallen M., Palsson B., Selected contribution: role of spleen emptying in prolonging apneas in humans, J. Appl. Physiol., 2001, 90, 1623-1629
22. Palada I., Eterovic D., Obad A., Bakovic D., Valic Z., Ivancev V., et al., Spleen and cardiovascular function during short apneas in divers, J. Appl. Physiol., 2007, 103, 1958-1963
23. Dujic Z., Uglesic L., Breskovic T., Valic Z., Heusser K., Marinovic J., et al., Involuntary breathing movements improve cerebral oxygenation during apnea struggle phase in elite divers, J. Appl. Physiol., 2009, 107, 1840-1846
24. Ferrigno M., Ferretti G., Ellis A., Warkander D., Costa M., Cerretelli P., et al., Cardiovascular changes during deep breath-hold dives in a pressure chamber, J. Appl. Physiol., 1997, 83, 1282-1290
25. Sieber A., L'abbate A., Passera M., Garbella E., Benassi A., Bedini R., Underwater study of arterial blood pressure in breath-hold divers, J. Appl. Physiol., 2009, 107, 1526-1531
26. Perini R., Gheza A., Moia C., Sponsiello N., Ferretti G., Cardiovascular time courses during prolonged immersed static apnoea, Eur. J. Appl. Physiol., 2010, 110, 277-283
27. Irving L., Bradycardia in Human Divers, J. Appl. Physiol., 1963, 18, 489-491
28. Hong S.K., Song S.H., Kim P.K., Suh C.S., Seasonal observations on the cardiac rhythm during diving in the Korean ama, J. Appl. Physiol., 1967, 23, 18-22
29. Somers V.K., Mark A.L., Zavala D.C., Abboud F.M., Contrasting effects of hypoxia and hypercapnia on ventilation and sympathetic activity in humans, J. Appl. Physiol., 1989, 67, 2101-2106
30. Lindholm P., Lundgren C.E., Alveolar gas composition before and after maximal breath-holds in competitive divers, Undersea Hyperb. Med., 2006, 33, 463-467
31. Overgaard K., Friis S., Pedersen R.B., Lykkeboe G., Influence of lung volume, glossopharyngeal inhalation and P(ET) O2 and P(ET) CO2 on apnea performance in trained breath-hold divers, Eur. J. Appl. Physiol., 2006, 97, 158-164
32. Macefield V.G., Wallin B.G., Effects of static lung inflation on sympathetic activity in human muscle nerves at rest and during asphyxia, J. Auton. Nerv. Syst., 1995, 53, 148-156
33. Morgan B.J., Denahan T., Ebert T.J., Neurocirculatory consequences of negative intrathoracic pressure vs. asphyxia during voluntary apnea, J. Appl. Physiol., 1993, 74, 2969-2975
34. 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., 2010, 154, 42-47
35. Breskovic T., Valic Z., Lipp A., Heusser K., Ivancev V., Tank J., et al., Peripheral chemoreflex regulation of sympathetic vasomotor tone in apnea divers, Clin. Auton. Res., 2010, 20, 57-63
36. Breskovic T., Steinback C.D., Salmanpour A., Shoemaker J.K., Dujic Z., Recruitment pattern of sympathetic neurons during breath-holding at different lung volumes in apnea divers and controls, Auton. Neurosci., 2011, 164, 74-81
37. Steinback C.D., Breskovic T., Banic I., Dujic Z., Shoemaker J.K., Autonomic and cardiovascular responses to chemoreflex stress in apnoea divers, Auton. Neurosci., 2010, 156, 138-143
38. Dujic Z., Ivancev V., Heusser K., Dzamonja G., Palada I., Valic Z., et al., Central chemoreflex sensitivity and sympathetic neural outflow in elite breath-hold divers, J. Appl. Physiol., 2008, 104, 205-211
39. Macefield V.G., Wallin B.G., Firing properties of single vasoconstrictor neurones in human subjects with high levels of muscle sympathetic activity, J. Physiol., 1999, 516, 293-301
40. Elam M., Sverrisdottir Y.B., Rundqvist B., McKenzie D., Wallin B.G., Macefield V.G., Pathological sympathoexcitation: how is it achieved?, Acta Physiol. Scand., 2003, 177, 405-411
41. Salmanpour A., Brown L.J., Shoemaker J.K., Spike detection in human muscle sympathetic nerve activity using a matched wavelet approach, J. Neurosci. Methods, 2010, 193, 343-355
42. Steinback C.D., Salmanpour A., Breskovic T., Dujic Z., Shoemaker J.K., Sympathetic neural activation: an ordered affair, J. Physiol., 2010, 588, 4825-4836
43. Henneman E., Somjen G., Carpenter D.O., Functional siginifcance of cell size in spinal motoneurons, J. Neurophysiol., 1965, 28, 560-580
44. Salmanpour A., Brown L.J., Steinback C.D., Usselman C.W., Goswami R., Shoemaker J.K., Relationship between size and latency of action potentials in human muscle sympathetic nerve activity, J. Neurophysiol., 2011, 105, 2830-2842
45. Pan A.W., He J., Kinouchi Y., Yamaguchi H., Miyamoto H., Blood flow in the carotid artery during breath-holding in relation to diving bradycardia, Eur. J. Appl. Physiol. Occup. Physiol., 1997, 75, 388-395
46. Przybylowski T., Bangash M.F., Reichmuth K., Morgan B.J., Skatrud J.B., Dempsey J.A., Mechanisms of the cerebrovascular response to apnoea in humans, J. Physiol., 2003, 548, 323-332
47. Vantanajal J.S., Ashmead J.C., Anderson T.J., Hepple R.T., Poulin M.J., Differential sensitivities of cerebral and brachial blood flow to hypercapnia in humans, J. Appl. Physiol., 2007, 102, 87-93
48. Ainslie P.N., Barach A., Murrell C., Hamlin M., Hellemans J., Ogoh S., Alterations in cerebral autoregulation and cerebral blood flow velocity during acute hypoxia: rest and exercise, Am. J. Physiol. Heart Circ. Physiol., 2007, 292, H976-H983
49. Andersson J.P., Liner M.H., Jonsson H., Increased serum levels of the brain damage marker S100B after apnea in trained breath-hold divers: a study including respiratory and cardiovascular observations, J. Appl. Physiol., 2009, 107, 809-815
50. Riuzzi F., Sorci G., Beccafico S., Donato R., S100B engages RAGE or bFGF/FGFR1 in myoblasts depending on its own concentration and myoblast density. Implications for muscle regeneration, PLoS One, 2012, 7, e28700
51. Kohshi K., Katoh T., Abe H., Okudera T., Neurological accidents caused by repetitive breath-hold dives: two case reports, J. Neurol. Sci., 2000, 178, 66-69
52. Potkin R., Uszler J.M., Brain function imaging in asymptomatic elite breath-hold divers, In: Lindholm P., Pollock N.W., Lundgren C.E., eds., Breath-hold diving. Proceedings of the Undersea and Hyperbaric Medical Society/Divers Alert Network, June 20-21 Workshop, NC: Divers Alert Network, Durham, 2006, 135-137
53. Lin Y.C., Breath-hold diving in terrestrial mammals, Exerc. Sport Sci. Rev., 1982, 10, 270-307
54. Dejours P., Hazards of hypoxia during diving, In: Rahn H., ed., Physiology of breath-hold diving and the Ama of Japan papers, National Academy of Sciences - National Research Council, Washington, 1965, 183-193
55. Cross T.J., Breskovic T., Sabapathy S., Zubin M.P., Johnson B.D., Dujic Z., Respiratory muscle pressure development during breath holding in apnea divers, Med. Sci. Sports Exerc., 2013, 45, 93-101
56. Breskovic T., Lojpur M., Maslov P.Z., Cross T.J., Kraljevic J., Ljubkovic M., et al., The influence of varying inspired fractions of O(2) and CO(2) on the development of involuntary breathing movements during maximal apnoea, Respir. Physiol. Neurobiol., 2012, 181, 228-233
57. Cross T.J., Kavanagh J.J., Breskovic T., Zubin M.P., Lojpur M., Johnson B.D., et al., The effects of involuntary respiratory contractions on cerebral blood flow during maximal apnoea in trained divers, PLoS One, 2013, 8, e66950
58. Dzamonja G., Tank J., Heusser K., Palada I., Valic Z., Bakovic D., et al., Glossopharyngeal insufflation induces cardioinhibitory syncope in apnea divers, Clin. Auton. Res., 2010, 20, 381-384
59. Hurford W.E., Hochachka P.W., Schneider R.C., Guyton G.P., Stanek K.S., Zapol D.G., et al., Splenic contraction, catecholamine release, and blood volume redistribution during diving in the Weddell seal, J. Appl. Physiol., 1996, 80, 298-306
60. Laub M., Hvid-Jacobsen K., Hovind P., Kanstrup I.L., Christensen N.J., Nielsen S.L., Spleen emptying and venous hematocrit in humans during exercise, J. Appl. Physiol., 1993, 74, 1024-1026
61. Bakovic D., Eterovic D., Saratlija-Novakovic Z., Palada I., Valic Z., Bilopavlovic N., et al., Effect of human splenic contraction on variation in circulating blood cell counts, Clin. Exp. Pharmacol. Physiol., 2005, 32, 944-951
62. Aster R.H., Pooling of platelets in the spleen: role in the pathogenesis of "hypersplenic" thrombocytopenia, J. Clin. Invest., 1966, 45, 645-657
63. Branehog I., Weinfeld A., Roos B., The exchangeable splenic platelet pool studied with epinephrine infusion in idiopathic thrombocytopenic purpura and in patients with splenomegaly, Br. J. Haematol., 1973, 25, 239-248
64. Schmidt K.G., Rasmussen J.W., Are young platelets released in excess from the spleen in response to short-term physical exercise?, Scand. J. Haematol., 1984, 32, 207-214
65. Chamberlain K.G., Tong M., Penington D.G., Properties of the exchangeable splenic platelets released into the circulation during exercise-induced thrombocytosis, Am. J. Hematol., 1990, 34, 161-168
66. van der Loo B., Martin J.F., A role for changes in platelet production in the cause of acute coronary syndromes, Arterioscler. Thromb. Vasc. Biol., 1999, 19, 672-679
67. Ojiri Y., Noguchi K., Shiroma N., Matsuzaki T., Sakanashi M., Sakanashi M., Uneven changes in circulating blood cell counts with adrenergic stimulation to the canine spleen, Clin. Exp. Pharmacol. Physiol., 2002, 29, 53-59
68. Kjeldsen S.E., Weder A.B., Egan B., Neubig R., Zweifler A.J., Julius S., Effect of circulating epinephrine on platelet function and hematocrit, Hypertension, 1995, 25, 1096-1105
69. Sloand J.A., Hooper M., Izzo J.L. Jr., Effects of circulating norepinephrine on platelet, leukocyte and red blood cell counts by alpha 1-adrenergic stimulation, Am. J. Cardiol., 1989, 63, 1140-1142
70. Wadenvik H., Kutti J., The effect of an adrenaline infusion on the splenic blood flow and intrasplenic platelet kinetics, Br. J. Haematol., 1987, 67, 187-192
71. Bakovic D., Eterovic D., Palada I., Valic Z., Dujic Z., Does breath-holding increase the risk of a thrombotic event?, Platelets, 2008, 19, 314-315
72. Butterworth R.J., Bath P.M., The relationship between mean platelet volume, stroke subtype and clinical outcome, Platelets, 1998, 9, 359-364
73. Khandekar M.M., Khurana A.S., Deshmukh S.D., Kakrani A.L., Katdare A.D., Inamdar A.K., Platelet volume indices in patients with coronary artery disease and acute myocardial infarction: an Indian scenario, J. Clin. Pathol., 2006, 59, 146-149
74. Greisenegger S., Endler G., Hsieh K., Tentschert S., Mannhalter C., Lalouschek W., Is elevated mean platelet volume associated with a worse outcome in patients with acute ischemic cerebrovascular events?, Stroke, 2004, 35, 1688-1691
75. Bakovic D., Pivac N., Eterovic D., Breskovic T., Zubin P., Obad A., et al., The effects of low-dose epinephrine infusion on spleen size, central and hepatic circulation and circulating platelets, Clin. Physiol. Funct. Imaging, 2013, 33, 30-37
76. Varol E., Ozturk O., Gonca T., Has M., Ozaydin M., Erdogan D., et al., Mean platelet volume is increased in patients with severe obstructive sleep apnea, Scand. J. Clin. Lab. Invest., 2010, 70, 497-502
77. Parish J.M., Somers V.K., Obstructive sleep apnea and cardiovascular disease, Mayo Clin. Proc., 2004, 79, 1036-1046
78. Kohli P., Balachandran J.S., Malhotra A., Obstructive sleep apnea and the risk for cardiovascular disease, Curr. Atheroscler. Rep., 2011, 13, 138-146
79. Waradekar N.V., Sinoway L.I., Zwillich C.W., Leuenberger U.A., Influence of treatment on muscle sympathetic nerve activity in sleep apnea, Am. J. Respir. Crit. Care Med., 1996, 153, 1333-1338
80. Sahota P., Vahidy F., Nguyen C., Bui T.T., Yang B., Parsha K., et al., Changes in spleen size in patients with acute ischemic stroke: a pilot observational study, Int. J. Stroke, 2013, 8, 60-67
81. Dujic Z., Breskovic T., Ljubkovic M., Breath hold diving: in vivo model of the brain survival response in man?, Med. Hypotheses, 2011, 76, 737-740