Breath-hold diving as a brain survival response
Tóm tắt
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.
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Tài liệu tham khảo
Lindholm P., Loss of motor control and/or loss of consciousness during breath-hold competitions, Int. J. Sports Med., 2007, 28, 295–299
Dujic Z., Breskovic T., Impact of breath holding on cardiovascular respiratory and cerebrovascular health, Sports Med., 2012, 42, 459–472
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
Lindholm P., Lundgren C.E., Alveolar gas composition before and after maximal breath-holds in competitive divers, Undersea Hyperb. Med., 2006, 33, 463–467
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
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
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
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
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
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
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
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
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
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
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
Steinback C.D., Salmanpour A., Breskovic T., Dujic Z., Shoemaker J.K., Sympathetic neural activation: an ordered affair, J. Physiol., 2010, 588, 4825–4836
Henneman E., Somjen G., Carpenter D.O., Functional siginifcance of cell size in spinal motoneurons, J. Neurophysiol., 1965, 28, 560–580
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
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
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
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
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
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
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
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
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
Lin Y.C., Breath-hold diving in terrestrial mammals, Exerc. Sport Sci. Rev., 1982, 10, 270–307
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
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
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
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
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
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
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
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
Aster R.H., Pooling of platelets in the spleen: role in the pathogenesis of “hypersplenic” thrombocytopenia, J. Clin. Invest., 1966, 45, 645–657
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
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
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
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
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
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
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
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
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
Butterworth R.J., Bath P.M., The relationship between mean platelet volume, stroke subtype and clinical outcome, Platelets, 1998, 9, 359–364
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
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
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
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
Parish J.M., Somers V.K., Obstructive sleep apnea and cardiovascular disease, Mayo Clin. Proc., 2004, 79, 1036–1046
Kohli P., Balachandran J.S., Malhotra A., Obstructive sleep apnea and the risk for cardiovascular disease, Curr. Atheroscler. Rep., 2011, 13, 138–146
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
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