Dietary nitrate improves muscle but not cerebral oxygenation status during exercise in hypoxia

Journal of Applied Physiology

Volumn 113, Issue 5, 2012, Pages 736-745

  Masschelein, Evi ^a   Van Thienen, Ruud ^a   Wang, Xu ^a   Van Schepdael, Ann ^a   Thomis, Martine ^a   Hespel, Peter ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

Altitude; Exercise performance; Near infrared spectroscopy; Nitric oxide

Indexed keywords

NITRATE;

ADULT; ANOXIA; ARTICLE; BLOOD; BRAIN; CONTROLLED CLINICAL TRIAL; CONTROLLED STUDY; CROSSOVER PROCEDURE; DIET SUPPLEMENTATION; DIET THERAPY; DRUG EFFECT; EXERCISE; EXERCISE TOLERANCE; HUMAN; LUNG GAS EXCHANGE; MALE; METABOLISM; OXYGEN CONSUMPTION; PHYSIOLOGY; RANDOMIZED CONTROLLED TRIAL; SINGLE BLIND PROCEDURE; SKELETAL MUSCLE;

ANOXIA; BRAIN; CROSS-OVER STUDIES; DIETARY SUPPLEMENTS; EXERCISE; EXERCISE TOLERANCE; HUMANS; MALE; MUSCLE, SKELETAL; NITRATES; OXYGEN CONSUMPTION; PULMONARY GAS EXCHANGE; SINGLE-BLIND METHOD; YOUNG ADULT;

EID: 84865798735     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.01253.2011     Document Type: Article

References (56)

1. Bailey DM, Davies B, Young IS, Hullin DA, Seddon PS. A potential role for free radical-mediated skeletal muscle soreness in the pathophysiology of acute mountain sickness. Aviat Space Environ Med 72: 513-521, 2001. (Pubitemid 32479983)
2. Bailey SJ, Fulford J, Vanhatalo A, Winyard PG, Blackwell JR, Dimenna FJ, Wilkerson DP, Benjamin N, Jones AM. Dietary nitrate supplementation enhances muscle contractile efficiency during knee-extensor exercise in humans. J Appl Physiol 109: 135-148, 2010.
3. Bailey SJ, Winyard P, Vanhatalo A, Blackwell JR, Dimenna FJ, Wilkerson DP, Tarr J, Benjamin N, Jones AM. Dietary nitrate supplementation reduces the O2 cost of low-intensity exercise and enhances tolerance to high-intensity exercise in humans. J Appl Physiol 107: 1144-1155, 2009.
4. Bailey SJ, Winyard PG, Vanhatalo A, Blackwell JR, Dimenna FJ, Wilkerson DP, Jones AM. Acute L-arginine supplementation reduces the O2 cost of moderate-intensity exercise and enhances high-intensity exercise tolerance. J Appl Physiol 109: 1394-1403, 2010.
5. Baumgartner RW, Bartsch P, Maggiorini M, Waber U, Oelz O. Enhanced cerebral blood flow in acute mountain sickness. Aviat Space Environ Med 65: 726-729, 1994. (Pubitemid 24242633)
6. Beall CM, Laskowski D, Strohl KP, Soria R, Villena M, Vargas E, Alarcon AM, Gonzales C, Erzurum SC. Pulmonary nitric oxide in mountain dwellers. Nature 414: 411-412, 2001. (Pubitemid 34173716)
7. Benjamin N, O'Driscoll F, Dougall H, Duncan C, Smith L, Golden M, McKenzie H. Stomach NO synthesis. Nature 368: 502, 1994.
8. Boushel R, Langberg H, Olesen J, Gonzales-Alonzo J, Bulow J, Kjaer M. Monitoring tissue oxygen availability with near infrared spectroscopy (NIRS) in health and disease. Scand J Med Sci Sports 11: 213-222, 2001. (Pubitemid 33643508)
9. Brouwer E. On simple formulae for calculating the heat expenditure and the quantities of carbohydrate and fat oxidized in metabolism of men and animals, from gaseous exchange (oxygen intake and carbonic acid output) and urine-N. Acta Physiol Pharmacol Neerl 6: 795-802, 1957.
10. Brown DE, Beall CM, Strohl KP, Mills PS. Exhaled nitric oxide decreases upon acute exposure to high-altitude hypoxia. Am J Hum Biol 18: 196-202, 2006.
11. Bryan NS, Fernandez BO, Bauer SM, Garcia-Saura MF, Milsom AB, Rassaf T, Maloney RE, Bharti A, Rodriguez J, Feelisch M. Nitrite is a signaling molecule and regulator of gene expression in mammalian tissues. Nat Chem Biol 1: 290-297, 2005.
12. Calbet JA, Boushel R, Radegran G, Sondergaard H, Wagner PD, Saltin B. Determinants of maximal oxygen uptake in severe acute hypoxia. Am J Physiol Regul Integr Comp Physiol 284: R291-R303, 2003. (Pubitemid 36120144)
13. Calbet JA, Lundby C. Air to muscle O2 delivery during exercise at altitude. High Alt Med Biol 10: 123-134, 2009.
14. Casey DP, Madery BD, Curry TB, Eisenach JH, Wilkins BW, Joyner MJ. Nitric oxide contributes to the augmented vasodilatation during hypoxic exercise. J Physiol 588: 373-385, 2010.
15. Clerc P, Rigoulet M, Leverve X, Fontaine E. Nitric oxide increases oxidative phosphorylation efficiency. J Bioenerg Biomembr 39: 158-166, 2007. (Pubitemid 46870546)
16. Droma Y, Hanaoka M, Ota M, Katsuyama Y, Koizumi T, Fujimoto K, Kobayashi T, Kubo K. Positive association of the endothelial nitric oxide synthase gene polymorphisms with high-altitude pulmonary edema. Circulation 106: 826-830, 2002.
17. Duncan A, Meek JH, Clemence M, Elwell CE, Fallon P, Tyszczuk L, Cope M, Delpy DT. Measurement of cranial optical path length as a function of age using phase resolved near infrared spectroscopy. Pediatr Res 39: 889-894, 1996. (Pubitemid 26130033)
18. Duplain H, Sartori C, Lepori M, Egli M, Allemann Y, Nicod P, Scherrer U. Exhaled nitric oxide in high-altitude pulmonary edema: role in the regulation of pulmonary vascular tone and evidence for a role against inflammation. Am J Respir Crit Care Med 162: 221-224, 2000. (Pubitemid 30469824)
19. Dweik RA, Laskowski D, Abu-Soud HM, Kaneko F, Hutte R, Stuehr DJ, Erzurum SC. Nitric oxide synthesis in the lung. Regulation by oxygen through a kinetic mechanism. J Clin Invest 101: 660-666, 1998. (Pubitemid 28084250)
20. Erzurum SC, Ghosh S, Janocha AJ, Xu W, Bauer S, Bryan NS, Tejero J, Hemann C, Hille R, Stuehr DJ, Feelisch M, Beall CM. Higher blood flow and circulating NO products offset high-altitude hypoxia among Tibetans. Proc Natl Acad Sci USA 104: 17593-17598, 2007. (Pubitemid 350210880)
21. Feddersen B, Ausserer H, Neupane P, Thanbichler F, Depaulis A, Waanders R, Noachtar S. Right temporal cerebral dysfunction heralds symptoms of acute mountain sickness. J Neurol 254: 359-363, 2007. (Pubitemid 46399202)
22. Ferrari M, Mottola L, Quaresima V. Principles, techniques, and limitations of near infrared spectroscopy. Can J Appl Physiol 29: 463-487, 2004. (Pubitemid 39107953)
23. Gladwin MT, Raat NJ, Shiva S, Dezfulian C, Hogg N, Kim-Shapiro DB, Patel RP. Nitrite as a vascular endocrine nitric oxide reservoir that contributes to hypoxic signaling, cytoprotection, and vasodilation. Am J Physiol Heart Circ Physiol 291: H2026-H2035, 2006.
24. Grau M, Hendgen-Cotta UB, Brouzos P, Drexhage C, Rassaf T, Lauer T, Dejam A, Kelm M, Kleinbongard P. Recent methodological advances in the analysis of nitrite in the human circulation: nitrite as a biochemical parameter of the L-arginine/NO pathway. J Chromatogr B Analyt Technol Biomed Life Sci 851: 106-123, 2007. (Pubitemid 46720145)
25. Green DJ, O'Driscoll G, Blanksby BA, Taylor RR. Control of skeletal muscle blood flow during dynamic exercise: contribution of endotheliumderived nitric oxide. Sports Med 21: 119-146, 1996.
26. Haseler LJ, Hogan MC, Richardson RS. Skeletal muscle phosphocreatine recovery in exercise-trained humans is dependent on O2 availability. J Appl Physiol 86: 2013-2018, 1999. (Pubitemid 29275578)
27. Hord NG, Tang Y, Bryan NS. Food sources of nitrates and nitrites: the physiologic context for potential health benefits. Am J Clin Nutr 90: 1-10, 2009.
28. Imray CH, Myers SD, Pattinson KT, Bradwell AR, Chan CW, Harris S, Collins P, Wright AD. Effect of exercise on cerebral perfusion in humans at high altitude. J Appl Physiol 99: 699-706, 2005. (Pubitemid 41061168)
29. Jobgen WS, Jobgen SC, Li H, Meininger CJ, Wu G. Analysis of nitrite and nitrate in biological samples using high-performance liquid chromatography. J Chromatogr B Analyt Technol Biomed Life Sci 851: 71-82, 2007. (Pubitemid 46720130)
30. Kemp GJ, Taylor DJ, Radda GK. Control of phosphocreatine resynthesis during recovery from exercise in human skeletal muscle. NMR Biomed 6: 66-72, 1993.
31. Kenjale AA, Ham KL, Stabler T, Robbins JL, Johnson JL, Vanbruggen M, Privette G, Yim E, Kraus WE, Allen JD. Dietary nitrate supplementation enhances exercise performance in peripheral arterial disease. J Appl Physiol 110: 1582-1591, 2011.
32. Lansley KE, Winyard PG, Bailey SJ, Vanhatalo A, Wilkerson DP, Blackwell JR, Gilchrist M, Benjamin N, Jones AM. Acute dietary nitrate supplementation improves cycling time trial performance. Med Sci Sports Exerc 43: 1125-1131, 2011.
33. Lansley KE, Winyard PG, Fulford J, Vanhatalo A, Bailey SJ, Blackwell JR, Dimenna FJ, Gilchrist M, Benjamin N, Jones AM. Dietary nitrate supplementation reduces the O2 cost of walking and running: a placebo-controlled study. J Appl Physiol 110: 591-600, 2011.
34. Larsen FJ, Schiffer TA, Borniquel S, Sahlin K, Ekblom B, Lundberg JO, Weitzberg E. Dietary inorganic nitrate improves mitochondrial efficiency in humans. Cell Metab 13: 149-159, 2011.
35. Larsen FJ, Weitzberg E, Lundberg JO, Ekblom B. Dietary nitrate reduces maximal oxygen consumption while maintaining work performance in maximal exercise. Free Radic Biol Med 48: 342-347, 2010.
36. Larsen FJ, Weitzberg E, Lundberg JO, Ekblom B. Effects of dietary nitrate on oxygen cost during exercise. Acta Physiol (Oxf) 191: 59-66, 2007. (Pubitemid 47221195)
37. Levett DZ, Fernandez BO, Riley HL, Martin DS, Mitchell K, Leckstrom CA, Ince C, Whipp BJ, Mythen MG, Montgomery HE, Grocott MP, Feelisch M. The role of nitrogen oxides in human adaptation to hypoxia. Sci Rep 1: 109, 2011.
38. Lundberg JO, Govoni M. Inorganic nitrate is a possible source for systemic generation of nitric oxide. Free Radic Biol Med 37: 395-400, 2004. (Pubitemid 38834005)
39. Lundberg JO, Weitzberg E. NO generation from nitrite and its role in vascular control. Arterioscler Thromb Vasc Biol 25: 915-922, 2005. (Pubitemid 40627834)
40. Lundberg JO, Weitzberg E, Gladwin MT. The nitrate-nitrite-nitric oxide pathway in physiology and therapeutics. Nat Rev Drug Discov 7: 156-167, 2008. (Pubitemid 351194063)
41. Millet GP, Roels B, Schmitt L, Woorons X, Richalet JP. Combining hypoxic methods for peak performance. Sports Med 40: 1-25, 2010.
42. Quaresima V, Ferrari M. Muscle oxygenation by near-infrared-based tissue oximeters. J Appl Physiol 107: 371-373, 2009.
43. Querido JS, Sheel AW. Regulation of cerebral blood flow during exercise. Sports Med 37: 765-782, 2007. (Pubitemid 47347391)
44. Reis DJ, Golanov EV, Ruggiero DA, Sun MK. Sympatho-excitatory neurons of the rostral ventrolateral medulla are oxygen sensors and essential elements in the tonic and reflex control of the systemic and cerebral circulations. J Hypertens Suppl 12: S159-S180, 1994.
45. Roach RC, Bartsch P, Oelz O, Hackett PH. The Lake Louise acute mountain sickness scoring system. Hypoxia and Molecular Medicine, edited by Sutton JR, Coates J, and Houston CS. Burlington, VT: Queen City, 1993, p. 272-274.
46. Schoene RB. Limits of human lung function at high altitude. J Exp Biol 204: 3121-3127, 2001. (Pubitemid 34861353)
47. Stamler JS, Meissner G. Physiology of nitric oxide in skeletal muscle. Physiol Rev 81: 209-237, 2001. (Pubitemid 32096176)
48. Takahashi H, Inaki M, Fujimoto K, Katsuta S, Anno I, Niitsu M, Itai Y. Control of the rate of phosphocreatine resynthesis after exercise in trained and untrained human quadriceps muscles. Eur J Appl Physiol Occup Physiol 71: 396-404, 1995.
49. van Beekvelt MC, Colier WN, Wevers RA, van Engelen BG. Performance of near-infrared spectroscopy in measuring local O(2) consumption and blood flow in skeletal muscle. J Appl Physiol 90: 511-519, 2001. (Pubitemid 32118910)
50. Vanhatalo A, Bailey SJ, Blackwell JR, Dimenna FJ, Pavey TG, Wilkerson DP, Benjamin N, Winyard PG, Jones AM. Acute and chronic effects of dietary nitrate supplementation on blood pressure and the physiological responses to moderate-intensity and incremental exercise. Am J Physiol Regul Integr Comp Physiol 299: R1121-R1131, 2010.
51. Vanhatalo A, Fulford J, Bailey SJ, Blackwell JR, Winyard PG, Jones AM. Dietary nitrate reduces muscle metabolic perturbation and improves exercise tolerance in hypoxia. J Physiol 589: 5517-5528, 2011.
52. Vogiatzis I, Louvaris Z, Habazettl H, Athanasopoulos D, Andrianopoulos V, Cherouveim E, Wagner H, Roussos C, Wagner PD, Zakynthinos S. Frontal cerebral cortex blood flow, oxygen delivery and oxygenation during normoxic and hypoxic exercise in athletes. J Physiol 589: 4027-4039, 2011.
53. Wagner PD. The physiological basis of reduced VO2max in Operation Everest II. High Alt Med Biol 11: 209-215, 2010.
54. Wang X, Masschelein E, Hespel P, Adams E, Van Schepdael A. Simultaneous determination of nitrite and nitrate in human plasma by on-capillary preconcentration with field amplified sample stacking. Electrophoresis 33: 402-405, 2012.
55. Webb AJ, Patel N, Loukogeorgakis S, Okorie M, Aboud Z, Misra S, Rashid R, Miall P, Deanfield J, Benjamin N, MacAllister R, Hobbs AJ, Ahluwalia A. Acute blood pressure lowering, vasoprotective, and antiplatelet properties of dietary nitrate via bioconversion to nitrite. Hypertension 51: 784-790, 2008. (Pubitemid 351301536)
56. Whipp BJ, Ward SA. Quantifying intervention-related improvements in exercise tolerance. Eur Respir J 33: 1254-1260, 2009.