Skip to main content
Top
Published in: Critical Care 5/2009

Open Access 01-10-2009 | Research

Changes in skeletal muscle oxygenation during exercise measured by near-infrared spectroscopy on ascent to altitude

Authors: Daniel S Martin, Denny ZH Levett, Michael Mythen, Mike PW Grocott, the Caudwell Xtreme Everest Research Group

Published in: Critical Care | Special Issue 5/2009

Login to get access

Abstract

Introduction

We sought to quantify changes in skeletal muscle oxygenation during exercise using near-infrared spectroscopy (NIRS) in healthy volunteers ascending to high altitude.

Methods

Using NIRS, skeletal muscle tissue oxygen saturation (StO2) was measured in the vastus lateralis of 24 subjects. Measurements were performed at sea level (SL; 75 m), at 3,500 m, on arrival at 5,300 m (5,300 m-a; days 15 to 17) and at 5,300 m again (5,300 m-b; days 69 to 71). Amongst the subjects, nine remained at 5,300 m whilst 14 climbed to a maximum of 8,848 m. Exercise was 3 minutes of unloaded cycling followed by an incremental ramp protocol to exhaustion. The absolute StO2 at different stages of exercise along with the difference between StO2 at stages and the rate of change in StO2 were compared between altitudes. Resting peripheral oxygen saturation was recorded.

Results

NIRS data achieving predefined quality criteria were available for 18 subjects at 75 m, 16 subjects at 3,500 m, 16 subjects on arrival at 5,300 m and 16 subjects on departure from 5,300 m. At SL, mean StO2 declined from 74.4% at rest to 36.4% at maximal oxygen consumption (P < 0.0001) and then rose to 82.3% (P < 0.0001) 60 seconds after exercise had ceased. At 3,500 m-a and 5,300 m-b, the pattern was similar to SL but absolute values were approximately 15% lower at all stages. At 5,300 m-a, the resting StO2 was similar to SL and the change in StO2 at each exercise stage less marked. At 5,300 m-b, the rate of decline in StO2 during exercise was more rapid than SL (P = 0.008); here the climbers had a smaller decline in StO2 during exercise (41.0%) and a slower rate of desaturation (0.086%/second) than those who had remained at 5,300 m (62.9% and 0.127%/second) (P = 0.031 and P = 0.047, respectively).

Conclusions

In most individuals, NIRS can be used to measure exercising skeletal muscle oxygenation in the field. During exercise the patterns of absolute oxygenation are broadly similar at altitude and SL. Following prolonged adaptation to altitude, the rate of muscle desaturation is more rapid than observed at SL but less so in those exposed to extreme hypoxia above 5,300 m.
Literature
1.
go back to reference Grocott M, Montgomery H, Vercueil A: High-altitude physiology and pathophysiology: implications and relevance for intensive care medicine. Crit Care 2007, 11: 203. 10.1186/cc5142PubMedCentralCrossRefPubMed Grocott M, Montgomery H, Vercueil A: High-altitude physiology and pathophysiology: implications and relevance for intensive care medicine. Crit Care 2007, 11: 203. 10.1186/cc5142PubMedCentralCrossRefPubMed
2.
go back to reference Ferretti G, Antonutto G, Denis C, Hoppeler H, Minetti AE, Narici MV, Desplanches D: The interplay of central and peripheral factors in limiting maximal O 2 consumption in man after pro-longed bed rest. J Physiol 1997, 501: 677-686. 10.1111/j.1469-7793.1997.677bm.xPubMedCentralCrossRefPubMed Ferretti G, Antonutto G, Denis C, Hoppeler H, Minetti AE, Narici MV, Desplanches D: The interplay of central and peripheral factors in limiting maximal O 2 consumption in man after pro-longed bed rest. J Physiol 1997, 501: 677-686. 10.1111/j.1469-7793.1997.677bm.xPubMedCentralCrossRefPubMed
3.
go back to reference Mancini DM, Bolinger L, Li H, Kendrick K, Chance B, Wilson JR: Validation of near-infrared spectroscopy in humans. J Appl Physiol 1994, 77: 2740-2747.PubMed Mancini DM, Bolinger L, Li H, Kendrick K, Chance B, Wilson JR: Validation of near-infrared spectroscopy in humans. J Appl Physiol 1994, 77: 2740-2747.PubMed
4.
go back to reference Belardinelli R, Barstow TJ, Porszasz J, Wasserman K: Changes in skeletal muscle oxygenation during incremental exercise measured with near infrared spectroscopy. Eur J Appl Physiol Occup Physiol 1995, 70: 487-492. 10.1007/BF00634377CrossRefPubMed Belardinelli R, Barstow TJ, Porszasz J, Wasserman K: Changes in skeletal muscle oxygenation during incremental exercise measured with near infrared spectroscopy. Eur J Appl Physiol Occup Physiol 1995, 70: 487-492. 10.1007/BF00634377CrossRefPubMed
5.
go back to reference Bhambhani Y, Maikala R, Esmail S: Oxygenation trends in vastus lateralis muscle during incremental and intense anaerobic cycle exercise in young men and women. Eur J Appl Physiol 2001, 84: 547-556. 10.1007/s004210000372CrossRefPubMed Bhambhani Y, Maikala R, Esmail S: Oxygenation trends in vastus lateralis muscle during incremental and intense anaerobic cycle exercise in young men and women. Eur J Appl Physiol 2001, 84: 547-556. 10.1007/s004210000372CrossRefPubMed
6.
go back to reference Grassi B, Quaresima V, Marconi C, Ferrari M, Cerretelli P: Blood lactate accumulation and muscle deoxygenation during incremental exercise. J Appl Physiol 1999, 87: 348-355.PubMed Grassi B, Quaresima V, Marconi C, Ferrari M, Cerretelli P: Blood lactate accumulation and muscle deoxygenation during incremental exercise. J Appl Physiol 1999, 87: 348-355.PubMed
7.
go back to reference Cerretelli P: Limiting factors to oxygen transport on Mount Everest. J Appl Physiol 1976, 40: 658-667.PubMed Cerretelli P: Limiting factors to oxygen transport on Mount Everest. J Appl Physiol 1976, 40: 658-667.PubMed
8.
go back to reference Pugh LGCE, Gill MB, Lahiri S, Milledge JS, Ward MP, West JB: Muscular exercise at great altitudes. J Appl Physiol 1964, 19: 431-440.PubMed Pugh LGCE, Gill MB, Lahiri S, Milledge JS, Ward MP, West JB: Muscular exercise at great altitudes. J Appl Physiol 1964, 19: 431-440.PubMed
9.
go back to reference 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 1988, 64: 1309-1321.PubMed 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 1988, 64: 1309-1321.PubMed
10.
go back to reference West JB, Boyer SJ, Graber DJ, Hackett PH, Maret KH, Milledge JS, Peters RMJ, Pizzo CJ, Samaja M, Sarnquist FH, et al.: Maximal exercise at extreme altitudes on Mount Everest. J Appl Physiol 1983, 55: 688-698.PubMed West JB, Boyer SJ, Graber DJ, Hackett PH, Maret KH, Milledge JS, Peters RMJ, Pizzo CJ, Samaja M, Sarnquist FH, et al.: Maximal exercise at extreme altitudes on Mount Everest. J Appl Physiol 1983, 55: 688-698.PubMed
11.
go back to reference Roach RC, Maes D, Sandoval D, Robergs RA, Icenogle M, Hinghofer-Szalkay H, Lium D, Loeppky JA: Exercise exacerbates acute mountain sickness at simulated high altitude. J Appl Physiol 2000, 88: 581-585.PubMed Roach RC, Maes D, Sandoval D, Robergs RA, Icenogle M, Hinghofer-Szalkay H, Lium D, Loeppky JA: Exercise exacerbates acute mountain sickness at simulated high altitude. J Appl Physiol 2000, 88: 581-585.PubMed
12.
go back to reference ATS/ACCP statement on cardiopulmonary exercise testing Am J Respir Crit Care Med 2003, 167: 211-277. 10.1164/rccm.167.2.211 ATS/ACCP statement on cardiopulmonary exercise testing Am J Respir Crit Care Med 2003, 167: 211-277. 10.1164/rccm.167.2.211
13.
go back to reference Hansen JE, Sue DY, Wasserman K: Predicted values for clinical exercise testing. Am Rev Respir Dis 1984, 129: S49-S55.CrossRefPubMed Hansen JE, Sue DY, Wasserman K: Predicted values for clinical exercise testing. Am Rev Respir Dis 1984, 129: S49-S55.CrossRefPubMed
14.
go back to reference Wilson JR, Mancini DM, McCully K, Ferraro N, Lanoce V, Chance B: Noninvasive detection of skeletal muscle underperfusion with near-infrared spectroscopy in patients with heart failure. Circulation 1989, 80: 1668-1674.CrossRefPubMed Wilson JR, Mancini DM, McCully K, Ferraro N, Lanoce V, Chance B: Noninvasive detection of skeletal muscle underperfusion with near-infrared spectroscopy in patients with heart failure. Circulation 1989, 80: 1668-1674.CrossRefPubMed
15.
go back to reference Ferretti G, Moia C, Thomet JM, Kayser B: The decrease of maximal oxygen consumption during hypoxia in man: a mirror image of the oxygen equilibrium curve. J Physiol 1997, 498: 231-237.PubMedCentralCrossRefPubMed Ferretti G, Moia C, Thomet JM, Kayser B: The decrease of maximal oxygen consumption during hypoxia in man: a mirror image of the oxygen equilibrium curve. J Physiol 1997, 498: 231-237.PubMedCentralCrossRefPubMed
16.
go back to reference Delpy DT, Cope M: Quantification in tissue near-infrared spectroscopy. Philos Trans Biol Sci 1997, 352: 649-659. 10.1098/rstb.1997.0046CrossRef Delpy DT, Cope M: Quantification in tissue near-infrared spectroscopy. Philos Trans Biol Sci 1997, 352: 649-659. 10.1098/rstb.1997.0046CrossRef
17.
go back to reference Cooper CE, Springett R: Measurement of cytochrome oxidase and mitochondrial energetics by near-infrared spectroscopy. Philos Trans R Soc Lond B Biol Sci 1997, 352: 669-676. 10.1098/rstb.1997.0048PubMedCentralCrossRefPubMed Cooper CE, Springett R: Measurement of cytochrome oxidase and mitochondrial energetics by near-infrared spectroscopy. Philos Trans R Soc Lond B Biol Sci 1997, 352: 669-676. 10.1098/rstb.1997.0048PubMedCentralCrossRefPubMed
18.
go back to reference Miura H, McCully K, Hong L, Nioka S, Chance B: Regional difference of muscle oxygen saturation and blood volume during exercise determined by near infrared imaging device. Jpn J Physiol 2001, 51: 599-606. 10.2170/jjphysiol.51.599CrossRefPubMed Miura H, McCully K, Hong L, Nioka S, Chance B: Regional difference of muscle oxygen saturation and blood volume during exercise determined by near infrared imaging device. Jpn J Physiol 2001, 51: 599-606. 10.2170/jjphysiol.51.599CrossRefPubMed
19.
go back to reference Miura H, McCully K, Nioka S, Chance B: Relationship between muscle architectural features and oxygenation status determined by near infrared device. Eur J Appl Physiol 2004, 91: 273-278. 10.1007/s00421-003-0964-6CrossRefPubMed Miura H, McCully K, Nioka S, Chance B: Relationship between muscle architectural features and oxygenation status determined by near infrared device. Eur J Appl Physiol 2004, 91: 273-278. 10.1007/s00421-003-0964-6CrossRefPubMed
20.
go back to reference Miura H, McCully K, Chance B: Application of multiple NIRS imaging device to the exercising muscle metabolism. Spectroscopy 2003, 17: 549-558.CrossRef Miura H, McCully K, Chance B: Application of multiple NIRS imaging device to the exercising muscle metabolism. Spectroscopy 2003, 17: 549-558.CrossRef
21.
go back to reference van Beekvelt MC, Borghuis MS, van Engelen BG, Wevers RA, Colier WN: Adipose tissue thickness affects in vivo quantitative near-IR spectroscopy in human skeletal muscle. Clin Sci (Lond) 2001, 101: 21-28. 10.1042/CS20000247CrossRef van Beekvelt MC, Borghuis MS, van Engelen BG, Wevers RA, Colier WN: Adipose tissue thickness affects in vivo quantitative near-IR spectroscopy in human skeletal muscle. Clin Sci (Lond) 2001, 101: 21-28. 10.1042/CS20000247CrossRef
22.
go back to reference Buono MJ, Miller PW, Hom C, Pozos RS, Kolkhorst FW: Skin blood flow affects in vivo near-infrared spectroscopy measurements in human skeletal muscle. Jpn J Physiol 2005, 55: 241-244. 10.2170/jjphysiol.T649CrossRefPubMed Buono MJ, Miller PW, Hom C, Pozos RS, Kolkhorst FW: Skin blood flow affects in vivo near-infrared spectroscopy measurements in human skeletal muscle. Jpn J Physiol 2005, 55: 241-244. 10.2170/jjphysiol.T649CrossRefPubMed
23.
go back to reference Davis SL, Fadel PJ, Cui J, Thomas GD, Crandall CG: Skin blood flow influences near-infrared spectroscopy-derived measurements of tissue oxygenation during heat stress. J Appl Physiol 2006, 100: 221-224. 10.1152/japplphysiol.00867.2005CrossRefPubMed Davis SL, Fadel PJ, Cui J, Thomas GD, Crandall CG: Skin blood flow influences near-infrared spectroscopy-derived measurements of tissue oxygenation during heat stress. J Appl Physiol 2006, 100: 221-224. 10.1152/japplphysiol.00867.2005CrossRefPubMed
24.
go back to reference Ikossi DG, Knudson MM, Morabito DJ, Cohen MJ, Wan JJ, Khaw L, Stewart CJ, Hemphill C, Manley GT: Continuous muscle tissue oxygenation in critically injured patients: a prospective observational study. J Trauma 2006, 61: 780-788. discussion 788-790 10.1097/01.ta.0000239500.71419.58CrossRefPubMed Ikossi DG, Knudson MM, Morabito DJ, Cohen MJ, Wan JJ, Khaw L, Stewart CJ, Hemphill C, Manley GT: Continuous muscle tissue oxygenation in critically injured patients: a prospective observational study. J Trauma 2006, 61: 780-788. discussion 788-790 10.1097/01.ta.0000239500.71419.58CrossRefPubMed
25.
go back to reference Hamaoka T, Iwane H, Shimomitsu T, Katsumura T, Murase N, Nishio S, Osada T, Kurosawa Y, Chance B: Noninvasive measures of oxidative metabolism on working human muscles by near-infrared spectroscopy. J Appl Physiol 1996, 81: 1410-1417.PubMed Hamaoka T, Iwane H, Shimomitsu T, Katsumura T, Murase N, Nishio S, Osada T, Kurosawa Y, Chance B: Noninvasive measures of oxidative metabolism on working human muscles by near-infrared spectroscopy. J Appl Physiol 1996, 81: 1410-1417.PubMed
26.
go back to reference Esaki K, Hamaoka T, Radegran G, Boushel R, Hansen J, Katsumura T, Haga S, Mizuno M: Association between regional quadriceps oxygenation and blood oxygen saturation during normoxic one-legged dynamic knee extension. Eur J Appl Physiol 2005, 95: 361-370. 10.1007/s00421-005-0008-5CrossRefPubMed Esaki K, Hamaoka T, Radegran G, Boushel R, Hansen J, Katsumura T, Haga S, Mizuno M: Association between regional quadriceps oxygenation and blood oxygen saturation during normoxic one-legged dynamic knee extension. Eur J Appl Physiol 2005, 95: 361-370. 10.1007/s00421-005-0008-5CrossRefPubMed
27.
go back to reference Tran TK, Sailasuta N, Kreutzer U, Hurd R, Chung Y, Mole P, Kuno S, Jue T: Comparative analysis of NMR and NIRS measurements of intracellular PO 2 in human skeletal muscle. Am J Physiol 1999, 276: R1682-R1690.PubMed Tran TK, Sailasuta N, Kreutzer U, Hurd R, Chung Y, Mole P, Kuno S, Jue T: Comparative analysis of NMR and NIRS measurements of intracellular PO 2 in human skeletal muscle. Am J Physiol 1999, 276: R1682-R1690.PubMed
28.
go back to reference Subudhi AW, Dimmen AC, Roach RC: Effects of acute hypoxia on cerebral and muscle oxygenation during incremental exercise. J Appl Physiol 2007, 103: 177-183. 10.1152/japplphysiol.01460.2006CrossRefPubMed Subudhi AW, Dimmen AC, Roach RC: Effects of acute hypoxia on cerebral and muscle oxygenation during incremental exercise. J Appl Physiol 2007, 103: 177-183. 10.1152/japplphysiol.01460.2006CrossRefPubMed
29.
go back to reference Matsui S, Tamura N, Hirakawa T, Kobayashi S, Takekoshi N, Murakami E: Assessment of working skeletal muscle oxygenation in patients with chronic heart failure. Am Heart J 1995, 129: 690-695. 10.1016/0002-8703(95)90317-8CrossRefPubMed Matsui S, Tamura N, Hirakawa T, Kobayashi S, Takekoshi N, Murakami E: Assessment of working skeletal muscle oxygenation in patients with chronic heart failure. Am Heart J 1995, 129: 690-695. 10.1016/0002-8703(95)90317-8CrossRefPubMed
30.
go back to reference Boyer SJ, Blume FD: Weight loss and changes in body composition at high altitude. J Appl Physiol 1984, 57: 1580-1585.PubMed Boyer SJ, Blume FD: Weight loss and changes in body composition at high altitude. J Appl Physiol 1984, 57: 1580-1585.PubMed
31.
go back to reference Maggiorini M, Buhler B, Walter M, Oelz O: Prevalence of acute mountain sickness in the Swiss Alps. Br Med J 1990, 301: 853-855. 10.1136/bmj.301.6756.853CrossRef Maggiorini M, Buhler B, Walter M, Oelz O: Prevalence of acute mountain sickness in the Swiss Alps. Br Med J 1990, 301: 853-855. 10.1136/bmj.301.6756.853CrossRef
32.
go back to reference Hoppeler H, Kleinert E, Schlegel C, Claassen H, Howald H, Kayar SR, Cerretelli P: Morphological adaptations of human skeletal muscle to chronic hypoxia. Int J Sports Med 1990,11(Suppl 1):S3-S9. 10.1055/s-2007-1024846CrossRefPubMed Hoppeler H, Kleinert E, Schlegel C, Claassen H, Howald H, Kayar SR, Cerretelli P: Morphological adaptations of human skeletal muscle to chronic hypoxia. Int J Sports Med 1990,11(Suppl 1):S3-S9. 10.1055/s-2007-1024846CrossRefPubMed
33.
go back to reference Pugh LGCE: Cardiac output in muscular exercise at 5,800 m (19,000 ft). J Appl Physiol 1964, 19: 441-447. Pugh LGCE: Cardiac output in muscular exercise at 5,800 m (19,000 ft). J Appl Physiol 1964, 19: 441-447.
34.
go back to reference Lundby C, Boushel R, Robach P, Moller K, Saltin B, Calbet JA: During hypoxic exercise some vasoconstriction is needed to match O 2 delivery with O 2 demand at the microcirculatory level. J Physiol 2008, 586: 123-130. 10.1113/jphysiol.2007.146035PubMedCentralCrossRefPubMed Lundby C, Boushel R, Robach P, Moller K, Saltin B, Calbet JA: During hypoxic exercise some vasoconstriction is needed to match O 2 delivery with O 2 demand at the microcirculatory level. J Physiol 2008, 586: 123-130. 10.1113/jphysiol.2007.146035PubMedCentralCrossRefPubMed
35.
go back to reference Lundby C, Calbet JA, 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 2004, 287: R1202-R1208.CrossRefPubMed Lundby C, Calbet JA, 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 2004, 287: R1202-R1208.CrossRefPubMed
36.
go back to reference Calbet JA, Boushel R, Radegran G, Sondergaard H, Wagner PD, Saltin B: Why is VO 2 max after altitude acclimatization still reduced despite normalization of arterial O 2 content? Am J Physiol Regul Integr Comp Physiol 2003, 284: R304-R316.CrossRefPubMed Calbet JA, Boushel R, Radegran G, Sondergaard H, Wagner PD, Saltin B: Why is VO 2 max after altitude acclimatization still reduced despite normalization of arterial O 2 content? Am J Physiol Regul Integr Comp Physiol 2003, 284: R304-R316.CrossRefPubMed
37.
go back to reference De Backer D, Creteur J, Preiser JC, Dubois MJ, Vincent JL: Microvascular blood flow is altered in patients with sepsis. Am J Respir Crit Care Med 2002, 166: 98-104. 10.1164/rccm.200109-016OCCrossRefPubMed De Backer D, Creteur J, Preiser JC, Dubois MJ, Vincent JL: Microvascular blood flow is altered in patients with sepsis. Am J Respir Crit Care Med 2002, 166: 98-104. 10.1164/rccm.200109-016OCCrossRefPubMed
38.
go back to reference Trzeciak S, Rivers EP: Clinical manifestations of disordered microcirculatory perfusion in severe sepsis. Crit Care 2005,9(Suppl 4):S20-S26. 10.1186/cc3744PubMedCentralCrossRefPubMed Trzeciak S, Rivers EP: Clinical manifestations of disordered microcirculatory perfusion in severe sepsis. Crit Care 2005,9(Suppl 4):S20-S26. 10.1186/cc3744PubMedCentralCrossRefPubMed
39.
go back to reference Spronk PE, Ince C, Gardien MJ, Mathura KR, Oudemans-van Straaten HM, Zandstra DF: Nitroglycerin in septic shock after intravascular volume resuscitation. Lancet 2002, 360: 1395-1396. 10.1016/S0140-6736(02)11393-6CrossRefPubMed Spronk PE, Ince C, Gardien MJ, Mathura KR, Oudemans-van Straaten HM, Zandstra DF: Nitroglycerin in septic shock after intravascular volume resuscitation. Lancet 2002, 360: 1395-1396. 10.1016/S0140-6736(02)11393-6CrossRefPubMed
41.
go back to reference Martin DS, Ince C, Goedhart P, Levett DZ, Grocott MP: Abnormal blood flow in the sublingual microcirculation at high altitude. Eur J Appl Physiol 2009, 106: 473-478. 10.1007/s00421-009-1023-8PubMedCentralCrossRefPubMed Martin DS, Ince C, Goedhart P, Levett DZ, Grocott MP: Abnormal blood flow in the sublingual microcirculation at high altitude. Eur J Appl Physiol 2009, 106: 473-478. 10.1007/s00421-009-1023-8PubMedCentralCrossRefPubMed
Metadata
Title
Changes in skeletal muscle oxygenation during exercise measured by near-infrared spectroscopy on ascent to altitude
Authors
Daniel S Martin
Denny ZH Levett
Michael Mythen
Mike PW Grocott
the Caudwell Xtreme Everest Research Group
Publication date
01-10-2009
Publisher
BioMed Central
Published in
Critical Care / Issue Special Issue 5/2009
Electronic ISSN: 1364-8535
DOI
https://doi.org/10.1186/cc8005

Other articles of this Special Issue 5/2009

Critical Care 5/2009 Go to the issue