Differences in the control of breathing between Himalayan and sea-level residents

Journal of Physiology

Volumn 588, Issue 9, 2010, Pages 1591-1606

  Slessarev, M ^a   Prisman, E ^a   Ito, S ^a   Watson, R R ^b   Jensen, D ^c   Preiss, D ^d   Greene, R ^e   Norboo, T ^f   Stobdan, T ^f   Diskit, D ^g   Norboo, A ^g   Kunzang, M ^h   Appenzeller, O ⁱ   Duffin, J ^a   Fisher, J A ^a  

^a UNIVERSITY HEALTH NETWORK   (Canada)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^c QUEEN S UNIVERSITY   (Canada)

^d BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e NEW MEXICO HIGHLANDS UNIVERSITY   (United States)

^f Ladakh Institute of Prevention and Ladakh Heart Foundation   (India)

^g Sonam Norboo Memorial Hospital Leh   (India)

^h Ladakh Autonomous Hill Development Council   (India)

ⁱ NMHEMC Research Foundation   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON DIOXIDE;

ADULT; ALTITUDE; ARTICLE; BREATHING MECHANICS; CAUCASIAN; CHEMORECEPTOR REFLEX; CONTROLLED STUDY; HUMAN; HUMAN EXPERIMENT; LUNG ALVEOLUS CARBON DIOXIDE TENSION; MALE; NORMAL HUMAN; PRIORITY JOURNAL; REBREATHING; RESPIRATION CONTROL; SEA LEVEL;

ALTITUDE; CARBON DIOXIDE; CEREBROVASCULAR CIRCULATION; HUMANS; HYPERCAPNIA; MALE; OXIMETRY; OXYGEN; RECRUITMENT, NEUROPHYSIOLOGICAL; RESPIRATORY MECHANICS; TIDAL VOLUME; YOUNG ADULT;

EID: 77952893673     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2009.185504     Document Type: Article

References (81)

1. Ainslie PN, Duffin J. Integration of cerebrovascular CO2 reactivity and chemoreflex control of breathing: mechanisms of regulation, measurement, and interpretation. Am J Physiol Regul Integr Comp Physiol 2009, 296:R1473-R1495.
2. Aldenderfer MS. Moving up in the world. Am Sci 2003, 91:542-549.
3. Appenzeller O, Claydon VE, Gulli G, Qualls C, Slessarev M, Zenebe G, Gebremedhin A, Hainsworth R. Cerebral vasodilatation to exogenous NO is a measure of fitness for life at altitude. Stroke 2006, 37:1754-1758.
4. Arias-Stella J, Valcarcel J. Chief cell hyperplasia in the human carotid body at high altitudes; physiologic and pathologic significance. Hum Pathol 1976, 7:361-373.
5. Beall CM. Two routes to functional adaptation: Tibetan and Andean high-altitude natives. Proc Natl Acad Sci U S A 2007, 104:8655-8660.
6. Beall CM, Strohl KP, Blangero J, Williams-Blangero S, Almasy LA, Decker MJ. Ventilation and hypoxic ventilatory response of Tibetan and Aymara high altitude natives. Am J Phys Anthropol 1997, 104:427-447.
7. Bell HJ. Respiratory control at exercise onset: an integrated systems perspective. Respir Physiol Neurobiol 2006, 152:1-15.
8. Berkenbosch A, Bovill JG, Dahan A, DeGoede J, Olievier IC. The ventilatory CO2 sensitivities from Read's rebreathing method and the steady-state method are not equal in man. J Physiol 1989, 411:367-377.
9. Brutsaert TD. Population genetic aspects and phenotypic plasticity of ventilatory responses in high altitude natives. Respir Physiol Neurobiol 2007, 158:151-160.
10. Brutsaert TD, Parra EJ, Shriver MD, Gamboa A, Rivera-Ch M, Leon-Velarde F. Ancestry explains the blunted ventilatory response to sustained hypoxia and lower exercise ventilation of Quechua altitude natives. Am J Physiol Regul Integr Comp Physiol 2005, 289:R225-R234.
11. Byrne-Quinn E, Sodal IE, Weil JV. Hypoxic and hypercapnic ventilatory drives in children native to high altitude. J Appl Physiol 1972, 32:44-46.
12. Chiodi H. Respiratory adaptations to chronic high altitude hypoxia. J Appl Physiol 1957, 10:81-87.
13. Claydon VE, Gulli G, Slessarev M, Appenzeller O, Zenebe G, Gebremedhin A, Hainsworth R. Cerebrovascular responses to hypoxia and hypocapnia in Ethiopian high altitude dwellers. Stroke 2008, 39:336-342.
14. Cudkowicz L, Spielvogel H, Zubieta G. Respiratory studies in women at high altitude (3,600 m or 12,200 ft and 5,200 m or 17,200 ft). Respiration 1972, 29:393-426.
15. Cunningham DJ. Studies on arterial chemoreceptors in man. J Physiol 1987, 384:1-26.
16. Curran LS, Zhuang J, Droma T, Land L, Moore LG. Hypoxic ventilatory responses in Tibetan residents of 4400 m compared with 3658 m. Respir Physiol 1995, 100:223-230.
17. Curran LS, Zhuang J, Sun SF, Moore LG. Ventilation and hypoxic ventilatory responsiveness in Chinese-Tibetan residents at 3,658 m. J Appl Physiol 1997, 83:2098-2104.
18. Dempsey JA. Challenges for future research in exercise physiology as applied to the respiratory system. Exerc Sport Sci Rev 2006, 34:92-98.
19. Duffin J. Role of acid-base balance in the chemoreflex control of breathing. J Appl Physiol 2005, 99:2255-2265.
20. Duffin J. Measuring the ventilatory response to hypoxia. J Physiol 2007, 584:285-293.
21. Duffin J, McAvoy GV. The peripheral-chemoreceptor threshold to carbon dioxide in man. J Physiol 1988, 406:15-26.
22. Duffin J, Mohan RM, Vasiliou P, Stephenson R, Mahamed S. A model of the chemoreflex control of breathing in humans: model parameters measurement. Respir Physiol 2000, 120:13-26.
23. Fan JL, Burgess KR, Basnyat R, Thomas KN, Peebles KC, Lucas SJ, Lucas RA, Donnelly J, Cotter JD, Ainslie PN. Influence of high altitude on cerebrovascular responsiveness to CO2. J Physiol 2010, 588:539-549.
24. Fatemian M, Gamboa A, Leon-Velarde F, Rivera-Ch M, Palacios JA, Robbins PA. Selected contribution: ventilatory response to CO2 in high-altitude natives and patients with chronic mountain sickness. J Appl Physiol 2003, 94:1279-1287.
25. Fink BR. Influence of cerebral activity in wakefulness on regulation of breathing. J Appl Physiol 1961, 16:15-20.
26. Forster HV, Dempsey JA, Birnbaum ML, Reddan WG, Thoden J, Grover RF, Rankin J. Effect of chronic exposure to hypoxia on ventilatory response to CO2 and hypoxia. J Appl Physiol 1971, 31:586-592.
27. Gamboa A, Leon-Velarde F, Rivera-Ch M, Palacios JA, Pragnell TR, O'Connor DF, Robbins PA. Selected contribution: acute and sustained ventilatory responses to hypoxia in high-altitude natives living at sea level. J Appl Physiol 2003, 94:1255-1262.
28. Ge RL, Chen QH, He LG. Characteristics of hypoxic ventilatory response in Tibetan living at moderate and high altitudes (in Chinese). Zhonghua Jie He He Hu Xi Za Zhi 1994, 17:384-366.
29. Hackett PH, Reeves JT, Reeves CD. Control of breathing in Sherpas at low and high altitude. J Appl Physiol Respir Environ Exerc Physiol 1980, 49:374-379.
30. Haouzi P. Theories on the nature of the coupling between ventilation and gas exchange during exercise. Respir Physiol Neurobiol 2006, 151:267-279.
31. Heath D, Smith P, Fitch R, Harris P. Comparative pathology of the enlarged carotid body. J Comp Pathol 1985, 95:259-271.
32. Huang SY, Alexander JK, Grover RF. Hypocapnia and sustained hypoxia blunt ventilation on arrival at high altitude. J Appl Physiol Respir Environ Exerc Physiol 1984, 56:602-606.
33. Jensen D, Duffin J, Lam YM, Webb KA, Simpson JA, Davies GA, Wolfe LA, O'Donnell DE. Physiological mechanisms of hyperventilation during human pregnancy. Respir Physiol Neurobiol 2008, 161:76-86.
34. Jensen D, Mask G, Tschakovsky ME. Variability of the ventilatory response to Duffin's modified hyperoxic and hypoxic rebreathing procedure in healthy awake humans. Respir Physiol Neurobiol 2010, 170:185-197.
35. Jensen D, Wolfe LA, O'Donnell DE, Davies GA. Chemoreflex control of breathing during wakefulness in healthy men and women. J Appl Physiol 2005, 98:822-828.
36. Jones RL, Neary JM, Ryan TG. Normal values for the hypercapnic ventilation response: effects of age and the ability to ventilate. Respiration 1993, 60:197-202.
37. Kay JM, Laidler P. Hypoxia and the carotid body. J Clin Pathol Suppl (R Coll Pathol) 1977, 11:30-44.
38. Khan Q, Heath D, Smith P, Norboo T. The histology of the carotid bodies in highlanders from Ladakh. Int J Biometeorol 1988, 32:254-259.
39. Kumar P, Bin-Jaliah I. Adequate stimuli of the carotid body: more than an oxygen sensor?. Respir Physiol Neurobiol 2007, 157:12-21.
40. Lahiri S. Environmental physiology: aging, heat and altitude. 1980, 341-350.
41. Lahiri S, DeLaney RG, Brody JS. Relative role of environmental and genetic factors in respiratory adaptation to high altitude. Nature 1976, 261:133-135.
42. Lahiri S, Kao FF, Velasquez T, Mart-Inez C, Pezzia W. Irreversible blunted respiratory sensitivity to hypoxia in high altitude natives. Respir Physiol 1969, 6:360-374.
43. Lahiri S, Milledge JS, Chattopadhyay HP, Bhattacharyya AK, Sinha AK. Respiration and heart rate of Sherpa highlanders during exercise. J Appl Physiol 1967, 23:545-554.
44. Lahiri S, Rozanov C, Cherniack NS. Altered structure and function of the carotid body at high altitude and associated chemoreflexes. High Alt Med Biol 2000, 1:63-74.
45. Lefrancois R, Gauiter H, Pasquis P. Ventilatory oxygen drive in acute and chronic hypoxia. Respir Physiol 1968, 4:217-228.
46. Leon-Velarde F, Richalet JP. Respiratory control in residents at high altitude: physiology and pathophysiology. High Alt Med Biol 2006, 7:125-137.
47. Leon-Velarde F, Vargas M, Monge C, Torrance RW, Robbins PA. Alveolar and of high-altitude natives living at sea level. J Appl Physiol 1996, 81:1605-1609.
48. Lloyd BB, Cunningham DJ C. A quantitative approach to the regulation of human respiration. The Regulation of Human Respiration 1963, 331-349. Cunningham DJC, Lloyd BB. In, eds, pp, Blackwell, Oxford
49. Longobardo G, Evangelisti CJ, Cherniack NS. Effects of neural drives on breathing in the awake state in humans. Respir Physiol 2002, 129:317-333.
50. McGurk SP, Blanksby BA, Anderson MJ. The relationship of hypercapnic ventilatory responses to age, gender and athleticism. Sports Med 1995, 19:173-183.
51. Mahamed S, Cunningham DA, Duffin J. Changes in respiratory control after three hours of isocapnic hypoxia in humans. J Physiol 2003, 547:271-281.
52. Mahamed S, Duffin J. Repeated hypoxic exposures change respiratory chemoreflex control in humans. J Physiol 2001, 534:595-603.
53. Marcus CL, Glomb WB, Basinski DJ, Davidson SL, Keens TG. Developmental pattern of hypercapnic and hypoxic ventilatory responses from childhood to adulthood. J Appl Physiol 1994, 76:314-320.
54. Mateika JH, Mendello C, Obeid D, Badr MS. Peripheral chemoreflex responsiveness is increased at elevated levels of carbon dioxide after episodic hypoxia in awake humans. J Appl Physiol 2004, 96:1197-1205.
55. Milledge JS, Lahiri S. Respiratory control in lowlanders and sherpa highlanders at altitude. Respir Physiol 1967, 2:310-322.
56. Mohan R, Duffin J. The effect of hypoxia on the ventilatory response to carbon dioxide in man. Respir Physiol 1997, 108:101-115.
57. Mohan RM, Amara CE, Cunningham DA, Duffin J. Measuring central-chemoreflex sensitivity in man: rebreathing and steady-state methods compared. Respir Physiol 1999, 115:23-33.
58. Moore LG. Comparative human ventilatory adaptation to high altitude. Respir Physiol 2000, 121:257-276.
59. Nattie E, Li A. Central chemoreception is a complex system function that involves multiple brain stem sites. J Appl Physiol 2009, 106:1464-1466.
60. Nishimura M, Yamamoto M, Yoshioka A, Akiyama Y, Kishi F, Kawakami Y. Longitudinal analyses of respiratory chemosensitivity in normal subjects. Am Rev Respir Dis 1991, 143:1278-1281.
61. Norcliffe LJ, Rivera-Ch M, Claydon VE, Moore JP, Leon-Velarde F, Appenzeller O, Hainsworth R. Cerebrovascular responses to hypoxia and hypocapnia in high-altitude dwellers. J Physiol 2005, 566:287-294.
62. Nunn JF. Applied Respiratory Physiology with Special Reference to Anaesthesia 1993, 4th edn, Butterworth-Heinemann, London
63. Orem J, Lovering AT, Dunin-Barkowski W, Vidruk EH. Tonic activity in the respiratory system in wakefulness, NREM and REM sleep. Sleep 2002, 25:488-496.
64. Pedersen ME, Fatemian M, Robbins PA. Identification of fast and slow ventilatory responses to carbon dioxide under hypoxic and hyperoxic conditions in humans. J Physiol 1999, 521:273-287.
65. Poulin MJ, Cunningham DA, Paterson DH, Kowalchuk JM, Smith WD. Ventilatory sensitivity to CO2 in hyperoxia and hypoxia in older aged humans. J Appl Physiol 1993, 75:2209-2216.
66. Powell FL. The influence of chronic hypoxia upon chemoreception. Respir Physiol Neurobiol 2007, 157:154-161.
67. Powell FL, Milsom WK, Mitchell GS. Time domains of the hypoxic ventilatory response. Respir Physiol 1998, 112:123-134.
68. Read DJ. A clinical method for assessing the ventilatory response to carbon dioxide. Aust Ann Med 1967, 16:20-32.
69. Read DJ, Leigh J. Blood-brain tissue relationships and ventilation during rebreathing. J Appl Physiol 1967, 23:53-70.
70. Santolaya RB, Lahiri S, Alfaro RT, Schoene RB. Respiratory adaptation in the highest inhabitants and highest Sherpa mountaineers. Respir Physiol 1989, 77:253-262.
71. Severinghaus JW, Bainton CR, Carcelen A. Respiratory insensitivity to hypoxia in chronically hypoxic man. Respir Physiol 1966, 1:308-334.
72. Shea SA. Behavioural and arousal-related influences on breathing in humans. Exp Physiol 1996, 81:1-26.
73. Somogyi RB, Preiss D, Vesely A, Fisher JA, Duffin J. Changes in respiratory control after 5 days at altitude. Respir Physiol Neurobiol 2005, 145:41-52.
74. Sorensen SC, Severinghaus JW. Respiratory sensitivity to acute hypoxia in man born at sea level living at high altitude. J Appl Physiol 1968a, 25:211-216.
75. Sorensen SC, Severinghaus JW. Irreversible respiratory insensitivity to acute hypoxia in man born at high altitude. J Appl Physiol 1968b, 25:217-220.
76. Torrance RW. Prolegomena. Chemoreception upstream of transmitters. Adv Exp Med Biol 1996, 410:13-38.
77. Vargas M, Leon-Velarde F, Monge C, Palacios JA, Robbins PA. Similar hypoxic ventilatory responses in sea-level natives and high-altitude Andean natives living at sea level. J Appl Physiol 1998, 84:1024-1029.
78. Velasquez T, Martinez C, Pezzia W, Gallardo N. Ventilatory effects of oxygen in high altitude natives. Respir Physiol 1968, 5:211-220.
79. Weil JV, Byrne-Quinn E, Sodal IE, Filley GF, Grover RF. Acquired attenuation of chemoreceptor function in chronically hypoxic man at high altitude. J Clin Invest 1971, 50:186-195.
80. Xing G, Qualls C, Huicho L, Rivera-Ch M, Stobdan T, Slessarev M. Adaptation and mal-adaptation to ambient hypoxia; Andean, Ethiopian and Himalayan patterns. PLoS One 2008, 3:e2342.
81. Zhuang J, Droma T, Sun S, Janes C, McCullough RE, McCullough RG, Cymerman A, Shao YH, Reeves JT, Moore LG. Hypoxic ventilatory responsiveness in Tibetan compared with Han residents of 3,658 m. J Appl Physiol 1993, 74:303-311.