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BY-NC-ND 3.0 license Open Access Published by De Gruyter Open Access September 13, 2013

Breath-hold diving as a brain survival response

  • Zeljko Dujic EMAIL logo , Toni Breskovic and Darija Bakovic


Elite breath-hold divers are unique athletes challenged with compression induced by hydrostatic pressure and extreme hypoxia/hypercapnia during maximal field dives. The current world records for men are 214 meters for depth (Herbert Nitsch, No-Limits Apnea discipline), 11:35 minutes for duration (Stephane Mifsud, Static Apnea discipline), and 281 meters for distance (Goran Čolak, Dynamic Apnea with Fins discipline). The major physiological adaptations that allow breath-hold divers to achieve such depths and duration are called the “diving response” that is comprised of peripheral vasoconstriction and increased blood pressure, bradycardia, decreased cardiac output, increased cerebral and myocardial blood flow, splenic contraction, and preserved O2 delivery to the brain and heart. This complex of physiological adaptations is not unique to humans, but can be found in all diving mammals. Despite these profound physiological adaptations, divers may frequently show hypoxic loss of consciousness. The breath-hold starts with an easy-going phase in which respiratory muscles are inactive, whereas during the second so-called “struggle” phase, involuntary breathing movements start. These contractions increase cerebral blood flow by facilitating left stroke volume, cardiac output, and arterial pressure. The analysis of the compensatory mechanisms involved in maximal breath-holds can improve brain survival during conditions involving profound brain hypoperfusion and deoxygenation.

[1] Lindholm P., Loss of motor control and/or loss of consciousness during breath-hold competitions, Int. J. Sports Med., 2007, 28, 295–299 in Google Scholar PubMed

[2] Dujic Z., Breskovic T., Impact of breath holding on cardiovascular respiratory and cerebrovascular health, Sports Med., 2012, 42, 459–472 in Google Scholar PubMed

[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 in Google Scholar PubMed

[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 in Google Scholar PubMed

[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 Search in Google Scholar

[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 in Google Scholar PubMed

[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 in Google Scholar PubMed

[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 Search in Google Scholar

[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 10.1152/jappl.1986.60.6.1871Search in Google Scholar PubMed

[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 in Google Scholar PubMed

[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 in Google Scholar PubMed

[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 in Google Scholar PubMed

[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 in Google Scholar

[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 10.1152/japplphysiol.00221.2003Search in Google Scholar

[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 in Google Scholar

[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 in Google Scholar

[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 Search in Google Scholar

[18] Ferretti G., Extreme human breath-hold diving, Eur. J. Appl. Physiol., 2001, 84, 254–271 in Google Scholar PubMed

[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 10.1113/jphysiol.1986.sp016196Search in Google Scholar PubMed PubMed Central

[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 in Google Scholar PubMed

[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 10.1152/jappl.2001.90.4.1623Search in Google Scholar PubMed

[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 in Google Scholar PubMed

[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 in Google Scholar PubMed

[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 10.1152/jappl.1997.83.4.1282Search in Google Scholar

[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 in Google Scholar

[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 in Google Scholar

[27] Irving L., Bradycardia in Human Divers, J. Appl. Physiol., 1963, 18, 489–491 10.1152/jappl.1963.18.3.489Search in Google Scholar

[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 10.1152/jappl.1967.23.1.18Search in Google Scholar

[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 10.1152/jappl.1989.67.5.2101Search in Google Scholar

[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 Search in Google Scholar

[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 in Google Scholar

[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 in Google Scholar

[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 10.1152/jappl.1993.74.6.2969Search in Google Scholar PubMed

[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 in Google Scholar PubMed

[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 in Google Scholar PubMed

[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 in Google Scholar PubMed

[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 in Google Scholar PubMed

[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 in Google Scholar PubMed

[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 in Google Scholar PubMed PubMed Central

[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 in Google Scholar PubMed

[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 in Google Scholar PubMed

[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 in Google Scholar PubMed PubMed Central

[43] Henneman E., Somjen G., Carpenter D.O., Functional siginifcance of cell size in spinal motoneurons, J. Neurophysiol., 1965, 28, 560–580 10.1152/jn.1965.28.3.560Search in Google Scholar PubMed

[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 in Google Scholar PubMed

[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 in Google Scholar

[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 10.1113/jphysiol.2002.029678Search in Google Scholar

[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 in Google Scholar

[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 in Google Scholar

[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 in Google Scholar

[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 in Google Scholar

[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 in Google Scholar

[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 Search in Google Scholar

[53] Lin Y.C., Breath-hold diving in terrestrial mammals, Exerc. Sport Sci. Rev., 1982, 10, 270–307 in Google Scholar

[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 Search in Google Scholar

[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 in Google Scholar PubMed

[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 in Google Scholar PubMed

[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 in Google Scholar PubMed PubMed Central

[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 in Google Scholar PubMed

[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 10.1152/jappl.1996.80.1.298Search in Google Scholar PubMed

[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 10.1152/jappl.1993.74.3.1024Search in Google Scholar PubMed

[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 in Google Scholar PubMed

[62] Aster R.H., Pooling of platelets in the spleen: role in the pathogenesis of “hypersplenic” thrombocytopenia, J. Clin. Invest., 1966, 45, 645–657 in Google Scholar PubMed PubMed Central

[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 in Google Scholar PubMed

[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 in Google Scholar PubMed

[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 in Google Scholar PubMed

[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 in Google Scholar

[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 in Google Scholar

[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 in Google Scholar

[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 in Google Scholar

[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 in Google Scholar PubMed

[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 in Google Scholar PubMed

[72] Butterworth R.J., Bath P.M., The relationship between mean platelet volume, stroke subtype and clinical outcome, Platelets, 1998, 9, 359–364 in Google Scholar PubMed

[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 in Google Scholar PubMed PubMed Central

[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 in Google Scholar PubMed

[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 10.1111/j.1475-097X.2012.01156.xSearch in Google Scholar PubMed

[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 in Google Scholar PubMed

[77] Parish J.M., Somers V.K., Obstructive sleep apnea and cardiovascular disease, Mayo Clin. Proc., 2004, 79, 1036–1046 in Google Scholar PubMed

[78] Kohli P., Balachandran J.S., Malhotra A., Obstructive sleep apnea and the risk for cardiovascular disease, Curr. Atheroscler. Rep., 2011, 13, 138–146 in Google Scholar PubMed PubMed Central

[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 in Google Scholar PubMed

[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 10.1111/ijs.12022Search in Google Scholar PubMed

[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 in Google Scholar PubMed

Published Online: 2013-9-13
Published in Print: 2013-9-1

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