AltitudeOmics: Impaired pulmonary gas exchange efficiency and blunted ventilatory acclimatization in humans with patent foramen ovale after 16 days at 5,260 m

Journal of Applied Physiology

Volumn 118, Issue 9, 2015, Pages 1100-1112

  Elliott, Jonathan E ^a   Laurie, Steven S ^a   Kern, Julia P ^a   Beasley, Kara M ^a   Goodman, Randall D ^b   Kayser, Bengt ^c   Subudhi, Andrew W ^d,e   Roach, Robert C ^d   Lovering, Andrew T ^a  

^a UNIVERSITY OF OREGON   (United States)

^b Echocardiography   (United States)

^c UNIVERSITY OF LAUSANNE   (Switzerland)

^d UNIVERSITY OF COLORADO   (United States)

^e UNIVERSITY OF COLORADO   (United States)

Author keywords

Acute mountain sickness; High altitude; Shunt

Indexed keywords

CARBON DIOXIDE;

ACCLIMATIZATION; ADULT; ALTITUDE; ALTITUDE DISEASE; BLOOD GAS ANALYSIS; EXERCISE; FEMALE; HUMAN; LUNG; LUNG GAS EXCHANGE; MALE; METABOLISM; PATENT FORAMEN OVALE; PATHOPHYSIOLOGY; PHYSIOLOGY; PROCEDURES; REST; YOUNG ADULT;

ACCLIMATIZATION; ADULT; ALTITUDE; ALTITUDE SICKNESS; BLOOD GAS ANALYSIS; CARBON DIOXIDE; EXERCISE; FEMALE; FORAMEN OVALE, PATENT; HUMANS; LUNG; MALE; PULMONARY GAS EXCHANGE; REST; YOUNG ADULT;

EID: 84929359172     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.00879.2014     Document Type: Article

References (83)

1. Agostoni P, Swenson ER, Bussotti M, Revera M, Meriggi P, Faini A, Lombardi C, Bilo G, Giuliano A, Bonacina D, Modesti PA, Mancia G, Parati G. High-altitude exposure of three weeks duration increases lung diffusing capacity in humans. J Appl Physiol 110: 1564-1571, 2011.
2. Allemann Y, Hutter D, Lipp E, Sartori C, Duplain H, Egli M, Cook S, Scherrer U, Seiler C. Patent foramen ovale and high-altitude pulmonary edema. JAMA 296: 2954-58, 2006.
3. Bartsch P, Maggiorini M, Ritter M, Noti C, Vock P, Oelz O. Prevention of high-altitude pulmonary edema by nifedipine. N Engl J Med 325: 1284-1289, 1991.
4. Bebout DE, Story D, Roca J, Hogan MC, Poole DC, Gonzalez-Camarena R, Ueno O, Haab P, Wagner PD. Effects of altitude acclimatization on pulmonary gas exchange during exercise. J Appl Physiol 67: 2286-2295, 1989.
5. Berggren S. The oxygen deficit of arterial blood caused by non-ventilating parts of the lung. Acta Physiol Scand 4, Suppl 11: 1942.
6. Bogert LWJ, Wesseling KH, Schraa O, Van Lieshout EJ, de Mol BAJM, van Goudoever J, Westerhof BE, van Lieshout JJ. Pulse contour cardiac output derived from non-invasive arterial pressure in cardiovascular disease. Anaesthesia 65: 1119-1125, 2010.
7. Cabanes L, Coste J, Derumeaux G, Jeanrenaud X, Lamy C, Zuber M, Mas JL. Interobserver and intraobserver variability in detection of patent foramen ovale and atrial septal aneurysm with transesophageal echocardiography. J Am Soc Echocardiogr 15: 441-446, 2002.
8. 2max in lowlanders acclimatized to altitude. Am J Physiol Heart Circ Physiol 287: H1214-H1224, 2004.
9. 2 content? Am J Physiol Regul Integr Comp Physiol 284: R304-R316, 2003.
10. 2max and cardiovascular function in lowlanders acclimatised to 5260 m. J Physiol 545: 715-728, 2002.
11. Dempsey JA, Powell FL, Bisgard GE, Blain GM, Poulin MJ, Smith CA. Role of chemoreception in cardiorespiratory acclimatization to, and deacclimatization from, hypoxia. J Appl Physiol 116: 858-866, 2014.
12. Dempsey JA, Reddan WG, Birnbaum ML, Forster HV, Thoden JS, Grover RF, Rankin J. Effects of acute through life-long hypoxic exposure on exercise pulmonary gas exchange. Respir Physiol 13: 62-89, 1971.
13. Dempsey JA, Wagner PD. Exercise-induced arterial hypoxemia. J Appl Physiol 87: 1997-2006, 1999.
14. Dominelli PB, Foster GE, Dominelli GS, Querido JS, Henderson WR, Koehle MS, Sheel AW. Repeated exercise-induced arterial hypoxemia in a healthy untrained woman. Respir Physiol Neurobiol 183: 201-205, 2012.
15. Duke JW, Elliott JE, Laurie SS, Beasley KM, Mangum TS, Hawn JA, Gladstone IM, Lovering AT. Pulmonary gas exchange efficiency during exercise breathing normoxic and hypoxic gas in adults born very preterm with low diffusion capacity. J Appl Physiol 117: 473-481, 2014.
16. Elliott JE, Choi Y, Laurie SS, Yang X, Gladstone IM, Lovering AT. Effect of initial gas bubble composition on detection of inducible intrapulmonary arteriovenous shunt during exercise in normoxia, hypoxia, or hyperoxia. J Appl Physiol 110: 35-45, 2011.
17. 2. J Physiol 592: 4537-4553, 2014.
18. Elliott JE, Nigam SM, Laurie SS, Beasley KM, Goodman RD, Hawn JA, Gladstone IM, Chesnutt MS, Lovering AT. Prevalence of left heart contrast in healthy, young, asymptomatic humans at rest breathing room air. Respir Physiol Neurobiol 188: 71-78, 2013.
19. 2 to hypoxic inspired gas on cerebral blood flow velocity and breathing during incremental exercise. PLos One 8: e81130, 2013.
20. Felici M, Filoche M, Sapoval B. Diffusional screening in the human pulmonary acinus. J Appl Physiol 94: 2010-2016, 2003.
21. Fenster BE, Curran-Everett D, Freeman AM, Weinberger HD, Kern Buckner J, Carroll JD. Saline contrast echocardiography for the detection of patent foramen ovale in hypoxia: a validation study using intracardiac echocardiography. Echocardiography 31: 420-427, 2014.
22. Freeman JA, Woods TD. Use of saline contrast echo timing to distinguish intracardiac and extracardiac shunts: failure of the 3- to 5-beat rule. Echocardiography 25: 1127-1130, 2008.
23. Hackett PH, Roach RC. High-altitude illness. N Engl J Med 345: 107-114, 2001.
24. Hagen PT, Edwards WD. Incidence and size of patent foramen ovale during the first 10 decades of life an autopsy study of 965 normal hearts. Mayo Clin Proc 59: 17-20, 1984.
25. Hammond MD, Gale GE, Kapitan KS, Ries A, Wagner PD. Pulmonary gas exchange in humans during exercise at sea level. J Appl Physiol 60: 1590-1598, 1986.
26. Hankinson JL, Odencrantz JR, Fedan KB. Spirometric reference values from a sample of the general U.S. population. Am J Respir Crit Care Med 159: 179-187, 1999.
27. Hansen JE, Vogel JA, Stelter GP, Consolazio CF. Oxygen uptake in man during exhaustive work at sea level and high altitude. J Appl Physiol 23: 511-522, 1967.
28. Harms CA, McClaran SR, Nickele GA, Pegelow DF, Nelson WB, Dempsey JA. Exercise-induced arterial hypoxaemia in healthy young women. J Physiol 507: 619-628, 1998.
29. Hill A. The possible effects of the aggregation of the molecules of haemoglobin on its dissociation curves. J Physiol 22: 208-210, 1910.
30. Hlastala MP, Van Liew HD. Absorption of in vivo inert gas bubbles. Respir Physiol 24: 147-158, 1975.
31. Hopkins SR, McKenzie DC, Schoene RB, Glenny RW, Robertson HT. Pulmonary gas exchange during exercise in athletes. I. Ventilation-perfusion mismatch and diffusion limitation. J Appl Physiol 77: 912-917, 1994.
32. Jones RS, Meade F. A theoretical and experimental analysis of anomalies in the estimation of pulmonary diffusing capacity by the single breath method. Q J Exp Physiol Cogn Med Sci 46: 131-143, 1961.
33. 2, pH, and base excess for time and temperature. J Appl Physiol 21: 1484-1490, 1966.
34. Kelman GR. Digital computer subroutine for the conversion of oxygen tension into saturation. J Appl Physiol 21: 1375-1376, 1966.
35. Kircher BJ, Himelman RB, Schiller NB. Noninvasive estimation of right atrial pressure from the inspiratory collapse of the inferior vena cava. Am J Cardiol 66: 493-496, 1990.
36. Knudson RJ, Kaltenborn WT, Knudson DE, Burrows B. The single-breath carbon monoxide diffusing capacity. Reference equations derived from a healthy nonsmoking population and effects of hematocrit. Am Rev Respir Dis 135: 805-811, 1987.
37. Lamy C, Giannesini C, Zuber M, Arquizan C, Meder JF, Trystram D, Coste J, Mas JL. Clinical and imaging findings in cryptogenic stroke patients with and without patent foramen ovale: The PFO-ASA Study. Stroke 33: 706-711, 2002.
38. Laurie SS, Elliott JE, Goodman RD, Lovering AT. Catecholamineinduced opening of intrapulmonary arteriovenous anastomoses in healthy humans at rest. J Appl Physiol 113: 1213-1222, 2012.
39. Laurie SS, Yang X, Elliott JE, Beasley KM, Lovering AT. Hypoxia-induced intrapulmonary arteriovenous shunting at rest in healthy humans. J Appl Physiol 109: 1072-1079, 2010.
40. Levine BD, Grayburn PA, Voyles WF, Greene ER, Roach RC, Hackett PH. Intracardiac shunting across a patent foramen ovale may exacerbate hypoxemia in high-altitude pulmonary edema. Ann Intern Med 114: 569-571, 1991.
41. Loeppky JA, Icenogle MV, Charlton GA, Conn CA, Maes D, Riboni K, Gates L, Melo MFV, Roach RC. Hypoxemia and acute mountain sickness: which comes first? High Alt Med Biol 9: 271-279, 2008.
42. Lovering AT, Goodman RD. Detection of intracardiac and intrapulmonary shunts at rest and during exercise using saline contrast echocardiography. In: Applied Aspects of Ultrasonography in Humans, edited by Ainslie PN. InTech, 2012, p. 159-174.
43. Lovering AT, Laurie SS, Elliott JE, Beasley KM, Yang X, Gust CE, Mangum TS, Goodman RD, Hawn JA, Gladstone IM. Normal pulmonary gas exchange efficiency and absence of exercise-induced arterial hypoxemia in adults with bronchopulmonary dysplasia. J Appl Physiol 115: 1050-1056, 2013.
44. Lovering AT, Stickland MK, Amann M, O'Brien MJ, Hokanson JS, Eldridge MW. Effect of a patent foramen ovale on pulmonary gas exchange efficiency at rest and during exercise. J Appl Physiol 110: 1354-1361, 2011.
45. Lundby C, Calbet JAL, van Hall G, Saltin B, Sander M. Pulmonary gas exchange at maximal exercise in Danish lowlanders during 8 wk of acclimatization to 4,100 m and in high-altitude Aymara natives. Am J Physiol Regul Integr Comp Physiol 287: R1202-R1208, 2004.
46. Macintyre N, Crapo RO, Viegi G, Johnson DC, van der Grinten CPM, Brusasco V, Burgos F, Casaburi R, Coates a Enright P, Gustafsson P, Hankinson J, Jensen R, McKay R, Miller MR, Navajas D, Pedersen OF, Pellegrino R, Wanger J. Standardisation of the single-breath determination of carbon monoxide uptake in the lung. Eur Respir J 26: 720-735, 2005.
47. Marriott K, Manins V, Forshaw A, Wright J, Pascoe R. Detection of right-to-left atrial communication using agitated saline contrast imaging experience with 1,162 patients and recommendations for echocardiography. J Am Soc Echocardiogr 26: 96-102, 2013.
48. Meerbaum S. Principles of echo contrast. In: In Advances in Echo Imaging Using Contrast Enhancement, edited by Nanda N, Schlief R. Dordrecht, The Netherlands: Kluwer Academic, 1993, p. 9-42.
49. Meltzer RS, Sartorius OEH, Lancee CT, Serruys PW, Verdouw PD, Essed CE, Roelandt J. Transmission of ultrasonic contrast through the lungs. Ultrasound Med Biol 7: 377-384, 1981.
50. Miller MR, Hankinson J, Brusasco V, Burgos F, Casaburi R, Coates A, Crapo R, Enright P, van der Grinten CPM, Gustafsson P, Jensen R, Johnson DC, MacIntyre N, McKay R, Navajas D, Pedersen OF, Pellegrino R, Viegi G, Wanger J. Standardisation of spirometry. Eur Respir J 26: 319-338, 2005.
51. Morse M, Cassels DE, Holder M. The position of the oxygen dissociation curve of the blood in cyanotic congenital heart disease. J Clin Invest 29: 1098-1103, 1950.
52. Norris HC, Mangum TS, Duke JW, Straley TB, Hawn JA, Goodman RD, Lovering AT. Exercise- and hypoxia-induced blood flow through intrapulmonary arteriovenous anastomoses is reduced in older adults. J Appl Physiol 116: 1324-1333, 2014.
53. Piiper J, Scheid P. Model for capillary-alveolar equilibration with special reference to O2 uptake in hypoxia. Respir Physiol 46: 193-208, 1981.
54. Piiper J, Schied P. Comparison of diffusion and perfusion limitations in alveolar gas exchange. Respir Physiol 51: 287-90, 1983.
55. Prommer N, Schmidt W. Loss of CO from the intravascular bed and its impact on the optimised CO-rebreathing method. Eur J Appl Physiol 100: 383-391, 2007.
56. Reeves JT, Dempsey JA, Grover RF. Pulmonary circulation during exercise. In: Lung Biology in Health and Disease, 1989, p. 107-33.
57. Rice AJ, Thornton AT, Gore CJ, Scroop GC, Greville HW, Wagner H, Wagner PD, Hopkins SR. Pulmonary gas exchange during exercise in highly trained cyclists with arterial hypoxemia. J Appl Physiol 87: 1802-1812, 1999.
58. Roach RC, Greene ER, Schoene RB, Hackett PH. Arterial oxygen saturation for prediction of acute mountain sickness. Aviat Space Environ Med 69: 1182-1185, 1998.
59. Roelandt J. Contrast echocardiography. Ultrasound Med Biol 8: 471-492, 1982.
60. Rudski LG, Lai WW, Afilalo J, Hua L, Handschumacher MD, Chandrasekaran K, Solomon SD, Louie EK, Schiller NB. Guidelines for the echocardiographic assessment of the right heart in adults: a report from the American Society of Echocardiography. J Am Soc Echocardiogr 23: 685-713, 2010.
61. Ryan BJ, Wachsmuth NB, Schmidt WF, Byrnes WC, Julian CG, Lovering AT, Subudhi AW, Roach RC. AltitudeOmics: rapid hemoglobin mass alterations with early acclimatization to and de-acclimatization from 5260 m in healthy humans. PLos One 9: e108788, 2014.
62. Saltin B, Grover RF, Blomqvist CG, Hartley LH, Johnson RL. Maximal oxygen uptake and cardiac output after 2 weeks at 4,300 m. J Appl Physiol 25: 400-409, 1968.
63. Sapoval B, Filoche M, Weibel ER. Smaller is better- but not too small: a physical scale for the design of the mammalian pulmonary acinus. Proc Natl Acad Sci USA 99: 10411-10416, 2002.
64. Schmidt W, Prommer N. The optimised CO-rebreathing method: a new tool to determine total haemoglobin mass routinely. Eur J Appl Physiol 95: 486-495, 2005.
65. Severinghaus JW. Blood gas calculator. J Appl Physiol 21: 1108-1116, 1966.
66. Subudhi AW, Bourdillon N, Bucher J, Davis C, Elliott JE, Eutermoster M, Evero O, Fan JL, Jameson-Van Houten S, Julian CG, Kark J, Kark S, Kayser B, Kern JP, Kim SE, Lathan C, Laurie SS, Lovering AT, Paterson R, Polaner DM, Ryan BJ, Spira JL, Tsao JW, Wachsmuth NB, Roach RC. AltitudeOmics: the integrative physiology of human acclimatization to hypobaric hypoxia and its retention upon reascent. PLos One 9: e92191, 2014.
67. Subudhi AW, Fan JL, Evero O, Bourdillon N, Kayser B, Julian CG, Lovering AT, Roach RC. AltitudeOmics: Effect of ascent and acclimatization to 5260 m on regional cerebral oxygen delivery. Exp Physiol 99: 772-781, 2014.
68. Sugawara J, Tanabe T, Miyachi M, Yamamoto K, Takahashi K, Iemitsu M, Otsuki T, Homma S, Maeda S, Ajisaka R, Matsuda M. Non-invasive assessment of cardiac output during exercise in healthy young humans: comparison between Modelflow method and Doppler echocardiography method. Acta Physiol Scand 179: 361-366, 2003.
69. Sutton JR, Reeves JT, Wagner PD, Groves BM, Cymerman A, Malconian MK, Rock PB, Young PM, Walter SD, Houston CS. Operation Everest II: oxygen transport during exercise at extreme simulated altitude. J Appl Physiol 64: 1309-1321, 1988.
70. Torre-Bueno JR, Wagner PD, Saltzman HA, Gale GE, Moon RE. Diffusion limitation in normal humans during exercise at sea level and simulated altitude. J Appl Physiol 58: 989-995, 1985.
71. Di Tullio M, Sacco RL, Gopal A, Mohr JP, Homma S. Patent foramen ovale as a risk factor for cryptogenic stroke. Ann Intern Med 117: 461-465, 1992.
72. Wagner PD, Gale GE, Moon RE, Torre-bueno JR, Stolp BW, Saltzman HA. Pulmonary gas exchange in humans exercising at sea level and simulated altitude. J Appl Physiol 61: 260-270, 1986.
73. 2 across the pulmonary blood gas barrier. Clin Physiol 2: 105-115, 1982.
74. 2max to hemoglobin-P50 at sea level and altitude. Respir Physiol 107: 205-212, 1997.
75. Wanger J, Clausen JL, Coates a Pedersen OF, Brusasco V, Burgos F, Casaburi R, Crapo R, Enright P, van der Grinten CPM, Gustafsson P, Hankinson J, Jensen R, Johnson D, Macintyre N, McKay R, Miller MR, Navajas D, Pellegrino R, Viegi G. Standardisation of the measurement of lung volumes. Eur Respir J 26: 511-522, 2005.
76. Wasserman K, Whipp BJ, Casaburi R. Respiratory control during exercise. In: Handbook of Physiology. The Respiratory System. Control of Breathing. Bethesda, MD: Am. Physiol. Soc., 1986, vol. 2, part 2, sect. 3, chapt. 17, p. 595-619.
77. Weil JV. Ventilatory control at high altitude. In: Handbook of Physiology. The Respiratory System. Control of Breathing. Bethesda, MD: Am. Physiol. Soc., 1986, vol. 2, part 2, sect. 3, chapt. 21, p. 703-727.
78. West JB, Wagner PD. Predicted gas exchange on the summit of Mt. Everest Respir Physiol 42: 1-16, 1980.
79. Wolfel EE, Groves BM, Brooks GA, Butterfield GE, Mazzeo RS, Moore LG, Sutton JR, Bender PR, Dahms TE, McCullough RE, Huang SY, Sun SF, Grover RF, Hultgren HN, Reeves JT. Oxygen transport during steady-state submaximal exercise in chronic hypoxia. J Appl Physiol 70: 1129-1136, 1991.
80. Wood SC. Effect of O2 affinity on arterial PO2 in animals with central vascular shunts. J Appl Physiol 53: 1360-1364, 1982.
81. Woods TD, Harmann L, Purath T, Ramamurthy S, Subramanian S, Jackson S, Tarima S. Small- and moderate-size right-to-left shunts identified by saline contrast echocardiography are normal and unrelated to migraine headache. Chest 138: 264-269, 2010.
82. Woods TD, Patel A. A critical review of patent foramen ovale detection using saline contrast echocardiography: when bubbles lie. J Am Soc Echocardiogr 19: 215-222, 2006.
83. Yock PG, Popp RL. Noninvasive estimation of right ventricular systolic pressure by Doppler ultrasound in patients with tricuspid regurgitation. Circulation 70: 657-662, 1984.