Effects of dietary inorganic nitrate on static and dynamic breath-holding in humans

Respiratory Physiology and Neurobiology

Volumn 185, Issue 2, 2013, Pages 339-348

  Schiffer, Tomas A ^a   Larsen, Filip J ^a   Lundberg, Jon O ^a   Weitzberg, Eddie ^a,b   Lindholm, Peter ^a,b  

^a KAROLINSKA INSTITUTE   (Sweden)

^b KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

Author keywords

Apnea; Breath holding; Hypoxia; Nitric oxide; Nitrite

Indexed keywords

PLACEBO; POTASSIUM NITRATE;

ADULT; APNEA; ARTERIAL OXYGEN SATURATION; ARTICLE; BLOOD CHEMISTRY; BLOOD SAMPLING; BREATH HOLDING; CARDIOVASCULAR RESPONSE; CONTROLLED STUDY; CROSSOVER PROCEDURE; DIET SUPPLEMENTATION; DIVER; DYNAMIC APNEA; ERGOMETER; HUMAN; HUMAN EXPERIMENT; MALE; NORMAL HUMAN; OXYGEN CONSUMPTION; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL; STATIC APNEA; TIDAL VOLUME; VITAL CAPACITY;

ADULT; APNEA; BLOOD PRESSURE; BREATH HOLDING; CYCLIC GMP; DIETARY SUPPLEMENTS; DOUBLE-BLIND METHOD; ERGOMETRY; EXPIRATORY RESERVE VOLUME; HUMANS; MALE; MIDDLE AGED; NITRATES; OXYGEN CONSUMPTION; PULMONARY GAS EXCHANGE; RESPIRATION; TIME FACTORS; VITAL CAPACITY; YOUNG ADULT;

EID: 84871919434     PISSN: 15699048     EISSN: 18781519     Source Type: Journal    
DOI: 10.1016/j.resp.2012.09.008     Document Type: Article

References (77)

1. Abu-Soud H.M., Ichimori K., Presta A., Stuehr D.J. Electron transfer, oxygen binding, and nitric oxide feedback inhibition in endothelial nitric-oxide synthase. Journal of Biological Chemistry 2000, 275:17349-17357.
2. Allen J.D., Giordano T., Kevil C.G. Nitrite and nitric oxide metabolism in peripheral artery disease. Nitric Oxide: Biology and Chemistry/Official Journal of the Nitric Oxide Society 2012, 26:217-222.
3. Andersson J.P., Biasoletto-Tjellstrom G., Schagatay E.K. Pulmonary gas exchange is reduced by the cardiovascular diving response in resting humans. Respiratory Physiology & Neurobiology 2008, 160:320-324.
4. Antunes F., Boveris A., Cadenas E. On the biologic role of the reaction of NO with oxidized cytochrome c oxidase. Antioxidants and Redox Signalling 2007, 9:1569-1579.
5. Bailey S.J., Fulford J., Vanhatalo A., Winyard P.G., Blackwell J.R., DiMenna F.J., Wilkerson D.P., Benjamin N., Jones A.M. Dietary nitrate supplementation enhances muscle contractile efficiency during knee-extensor exercise in humans. Journal of Applied Physiology 2010, 109:135-148.
6. 2 cost of low-intensity exercise and enhances tolerance to high-intensity exercise in humans. Journal of Applied Physiology 2009, 107:1144-1155.
7. Basu S., Azarova N.A., Font M.D., King S.B., Hogg N., Gladwin M.T., Shiva S., Kim-Shapiro D.B. Nitrite reductase activity of cytochrome c. The Journal of Biological Chemistry 2008, 283:32590-32597.
8. Benamar A., Rolletschek H., Borisjuk L., Avelange-Macherel M.H., Curien G., Mostefai H.A., Andriantsitohaina R., Macherel D. Nitrite-nitric oxide control of mitochondrial respiration at the frontier of anoxia. Biochimica et Biophysica Acta 2008, 1777:1268-1275.
9. Benjamin N., O'Driscoll F., Dougall H., Duncan C., Smith L., Golden M., McKenzie H. Stomach NO synthesis. Nature 1994, 368:502.
10. Benoit H., Costes F., Feasson L., Lacour J.R., Roche F., Denis C., Geyssant A., Barthelemy J.C. Accuracy of pulse oximetry during intense exercise under severe hypoxic conditions. European Journal of Applied Physiology and Occupational Physiology 1997, 76:260-263.
11. Bescos R., Rodriguez F.A., Iglesias X., Ferrer M.D., Iborra E., Pons A. Acute administration of inorganic nitrate reduces VO(2peak) in endurance athletes. Medicine and Science in Sports and Exercise 2011, 43:1979-1986.
12. Bescos R., Sureda A., Tur J.A., Pons A. The effect of nitric-oxide-related supplements on human performance. Sports Medicine 2012, 42:99-117.
13. Boveris A., Costa L.E., Poderoso J.J., Carreras M.C., Cadenas E. Regulation of mitochondrial respiration by oxygen and nitric oxide. Annals of the New York Academy of Sciences 2000, 899:121-135.
14. Bryan N.S., Calvert J.W., Elrod J.W., Gundewar S., Ji S.Y., Lefer D.J. Dietary nitrite supplementation protects against myocardial ischemia-reperfusion injury. Proceedings of the National Academy of Sciences of the United States of America 2007, 104:19144-19149.
15. Butler P.J., Jones D.R. Physiology of diving of birds and mammals. Physiological Reviews 1997, 77:837-899.
16. Butler P.J., Woakes A.J. Heart rate in humans during underwater swimming with and without breath-hold. Respiration Physiology 1987, 69:387-399.
17. Castello P.R., David P.S., McClure T., Crook Z., Poyton R.O. Mitochondrial cytochrome oxidase produces nitric oxide under hypoxic conditions: implications for oxygen sensing and hypoxic signaling in eukaryotes. Cell Metabolism 2006, 3:277-287.
18. Chung S.Y., Kim J.S., Kim M., Hong M.K., Lee J.O., Kim C.M., Song I.S. Survey of nitrate and nitrite contents of vegetables grown in Korea. Food Additives and Contaminants 2003, 20:621-628.
19. Clerc P., Rigoulet M., Leverve X., Fontaine E. Nitric oxide increases oxidative phosphorylation efficiency. Journal of Bioenergetics and Biomembranes 2007, 39:158-166.
20. Cooper C.E., Giulivi C. Nitric oxide regulation of mitochondrial oxygen consumption II: molecular mechanism and tissue physiology. American Journal of Physiology - Cell Physiology 2007, 292:C1993-C2003.
21. Cosby K., Partovi K.S., Crawford J.H., Patel R.P., Reiter C.D., Martyr S., Yang B.K., Waclawiw M.A., Zalos G., Xu X., Huang K.T., Shields H., Kim-Shapiro D.B., Schechter A.N., Cannon R.O., Gladwin M.T. Nitrite reduction to nitric oxide by deoxyhemoglobin vasodilates the human circulation. Nature Medicine 2003, 9:1498-1505.
22. Curtis E., Hsu L.L., Noguchi A.C., Geary L., Shiva S. Oxygen regulates tissue nitrite metabolism. Antioxidants & Redox Signaling 2012, 17:951-961.
23. Duncan C., Dougall H., Johnston P., Green S., Brogan R., Leifert C., Smith L., Golden M., Benjamin N. Chemical generation of nitric oxide in the mouth from the enterosalivary circulation of dietary nitrate. Nature Medicine 1995, 1:546-551.
24. Duranski M.R., Greer J.J., Dejam A., Jaganmohan S., Hogg N., Langston W., Patel R.P., Yet S.F., Wang X., Kevil C.G., Gladwin M.T., Lefer D.J. Cytoprotective effects of nitrite during in vivo ischemia-reperfusion of the heart and liver. The Journal of Clinical Investigation 2005, 115:1232-1240.
25. Engan H.K., Jones A.M., Ehrenberg F., Schagatay E. Acute dietary nitrate supplementation improves dry static apnea performance. Respiratory Physiology & Neurobiology 2012, 182:53-59.
26. Ferrigno M., Ferretti G., Ellis A., Warkander D., Costa M., Cerretelli P., Lundgren C.E. Cardiovascular changes during deep breath-hold dives in a pressure chamber. Journal of Applied Physiology 1997, 83:1282-1290.
27. Gladwin M.T., Schechter A.N., Kim-Shapiro D.B., Patel R.P., Hogg N., Shiva S., Cannon R.O., Kelm M., Wink D.A., Espey M.G., Oldfield E.H., Pluta R.M., Freeman B.A., Lancaster J.R., Feelisch M., Lundberg J.O. The emerging biology of the nitrite anion. Nature Chemical Biology 2005, 1:308-314.
28. Gnaiger E., Mendez G., Hand S.C. High phosphorylation efficiency and depression of uncoupled respiration in mitochondria under hypoxia. Proceedings of the National Academy of Sciences of the United States of America 2000, 97:11080-11085.
29. Hentsch U., Ulmer H.V. Trainability of underwater breath-holding time. International Journal of Sports Medicine 1984, 5:343-347.
30. Hernandez A., Schiffer T.A., Ivarsson N., Cheng A.J., Bruton J.D., Lundberg J.O., Weitzberg E., Westerblad H. Dietary nitrate increases tetanic [Ca2+]i and contractile force in mouse fast-twitch muscle. The Journal of Physiology 2012, 590:3575-3583.
31. Hochachka P.W., Liggins G.C., Guyton G.P., Schneider R.C., Stanek K.S., Hurford W.E., Creasy R.K., Zapol D.G., Zapol W.M. Hormonal regulatory adjustments during voluntary diving in Weddell seals. Comparative Biochemistry and Physiology. Part B: Biochemistry and Molecular Biology 1995, 112:361-375.
32. Horvat S., Beyer C., Arnold S. Effect of hypoxia on the transcription pattern of subunit isoforms and the kinetics of cytochrome c oxidase in cortical astrocytes and cerebellar neurons. Journal of Neurochemistry 2006, 99:937-951.
33. Huang Z., Shiva S., Kim-Shapiro D.B., Patel R.P., Ringwood L.A., Irby C.E., Huang K.T., Ho C., Hogg N., Schechter A.N., Gladwin M.T. Enzymatic function of hemoglobin as a nitrite reductase that produces NO under allosteric control. The Journal of Clinical Investigation 2005, 115:2099-2107.
34. Hurford W.E., Hong S.K., Park Y.S., Ahn D.W., Shiraki K., Mohri M., Zapol W.M. Splenic contraction during breath-hold diving in the Korean ama. Journal of Applied Physiology 1990, 69:932-936.
35. Idema R.N., Van Den Meiracker A.H., Imholz B.P., Man in 't Veld A.J., Settels J.J., Ritsema van Eck H.J., Schalekamp M.A. Comparison of Finapres non-invasive beat-to-beat finger blood pressure with intrabrachial artery pressure during and after bicycle ergometry. Journal of Hypertension. Supplement: Official Journal of the International Society of Hypertension 1989, 7:S58-S59.
36. Jansson E.A., Huang L., Malkey R., Govoni M., Nihlen C., Olsson A., Stensdotter M., Petersson J., Holm L., Weitzberg E., Lundberg J.O. A mammalian functional nitrate reductase that regulates nitrite and nitric oxide homeostasis. Nature Chemical Biology 2008, 4:411-417.
37. Kenjale A.A., Ham K.L., Stabler T., Robbins J.L., Johnson J.L., Vanbruggen M., Privette G., Yim E., Kraus W.E., Allen J.D. Dietary nitrate supplementation enhances exercise performance in peripheral arterial disease. Journal of Applied Physiology 2011, 110:1582-1591.
38. Kjeld T., Pott F.C., Secher N.H. Facial immersion in cold water enhances cerebral blood velocity during breath-hold exercise in humans. Journal of Applied Physiology 2009, 106:1243-1248.
39. Kozlov A.V., Dietrich B., Nohl H. Various intracellular compartments cooperate in the release of nitric oxide from glycerol trinitrate in liver. British Journal of Pharmacology 2003, 139:989-997.
40. 2 cost of walking and running: a placebo-controlled study. Journal of Applied Physiology 2011, 110:591-600.
41. Larsen F.J., Ekblom B., Sahlin K., Lundberg J.O., Weitzberg E. Effects of dietary nitrate on blood pressure in healthy volunteers. The New England Journal of Medicine 2006, 355:2792-2793.
42. Larsen F.J., Schiffer T.A., Borniquel S., Sahlin K., Ekblom B., Lundberg J.O., Weitzberg E. Dietary inorganic nitrate improves mitochondrial efficiency in humans. Cell Metabolism 2011, 13:149-159.
43. Larsen F.J., Weitzberg E., Lundberg J.O., Ekblom B. Effects of dietary nitrate on oxygen cost during exercise. Acta Physiology (Oxford) 2007, 191:59-66.
44. Larsen F.J., Weitzberg E., Lundberg J.O., Ekblom B. Dietary nitrate reduces maximal oxygen consumption while maintaining work performance in maximal exercise. Free Radical Biology and Medicine 2010, 48:342-347.
45. Lindholm P., Blogg S.L., Gennser M. Pulse oximetry to detect hypoxemia during apnea: comparison of finger and ear probes. Aviation Space, and Environmental Medicine 2007, 78:770-773.
46. Lindholm P., Conniff M., Gennser M., Pendergast D., Lundgren C. Effects of fasting and carbohydrate consumption on voluntary resting apnea duration. European Journal of Applied Physiology 2007, 100:417-425.
47. Lindholm P., Linnarsson D. Pulmonary gas exchange during apnoea in exercising men. European Journal of Applied Physiology 2002, 86:487-491.
48. Lindholm P., Lundgren C.E. The physiology and pathophysiology of human breath-hold diving. Journal of Applied Physiology 2009, 106:284-292.
49. Lindholm P., Nordh J., Linnarsson D. Role of hypoxemia for the cardiovascular responses to apnea during exercise. American Journal of Physiology Regulatory, Integrative and Comparative Physiology 2002, 283:R1227-R1235.
50. Lindholm P., Sundblad P., Linnarsson D. Oxygen-conserving effects of apnea in exercising men. Journal of Applied Physiology 1999, 87:2122-2127.
51. Lundberg J.O., Gladwin M.T., Ahluwalia A., Benjamin N., Bryan N.S., Butler A., Cabrales P., Fago A., Feelisch M., Ford P.C., Freeman B.A., Frenneaux M., Friedman J., Kelm M., Kevil C.G., Kim-Shapiro D.B., Kozlov A.V., Lancaster J.R., Lefer D.J., McColl K., McCurry K., Patel R.P., Petersson J., Rassaf T., Reutov V.P., Richter-Addo G.B., Schechter A., Shiva S., Tsuchiya K., van Faassen E.E., Webb A.J., Zuckerbraun B.S., Zweier J.L., Weitzberg E. Nitrate and nitrite in biology, nutrition and therapeutics. Nature Chemical Biology 2009, 5:865-869.
52. Lundberg J.O., Govoni M. Inorganic nitrate is a possible source for systemic generation of nitric oxide. Free Radical Biology and Medicine 2004, 37:395-400.
53. Lundberg J.O., Weitzberg E. The biological role of nitrate and nitrite: the times they are a-changin'. Nitric Oxide: Biology and Chemistry/Official Journal of the Nitric Oxide Society 2010, 22:61-63.
54. Lundberg J.O., Weitzberg E. NO-synthase independent NO generation in mammals. Biochemical and Biophysical Research Communications 2010, 396:39-45.
55. Lundberg J.O., Weitzberg E., Cole J.A., Benjamin N. Nitrate, bacteria and human health. Nature Reviews Microbiology 2004, 2:593-602.
56. Lundberg J.O., Weitzberg E., Gladwin M.T. The nitrate-nitrite-nitric oxide pathway in physiology and therapeutics. Nature Reviews Drug Discovery 2008, 7:156-167.
57. Lundberg J.O., Weitzberg E., Lundberg J.M., Alving K. Intragastric nitric oxide production in humans: measurements in expelled air. Gut 1994, 35:1543-1546.
58. Mason M.F. Drug impairment reviews: opiates, minor tranquilizers. NIDA Research Monograph Series 1977, 11:44-60.
59. Merial C., Bouloumie A., Trocheris V., Lafontan M., Galitzky J. Nitric oxide-dependent downregulation of adipocyte UCP-2 expression by tumor necrosis factor-alpha. American Journal of Physiology - Cell Physiology 2000, 279:C1100-C1106.
60. Nohl H., Staniek K., Sobhian B., Bahrami S., Redl H., Kozlov A.V. Mitochondria recycle nitrite back to the bioregulator nitric monoxide. Acta Biochimica Polonica 2000, 47:913-921.
61. Richardson R.S., Newcomer S.C., Noyszewski E.A. Skeletal muscle intracellular PO(2) assessed by myoglobin desaturation: response to graded exercise. Journal of Applied Physiology 2001, 91:2679-2685.
62. Schagatay E., Andersson J.P., Hallen M., Palsson B. Selected contribution: role of spleen emptying in prolonging apneas in humans. Journal of Applied Physiology 2001, 90:1623-1629. discussion 1606.
63. Shen W., Xu X., Ochoa M., Zhao G., Bernstein R.D., Forfia P., Hintze T.H. Endogenous nitric oxide in the control of skeletal muscle oxygen extraction during exercise. Acta Physiologica Scandinavica 2000, 168:675-686.
64. Shiva S., Huang Z., Grubina R., Sun J., Ringwood L.A., MacArthur P.H., Xu X., Murphy E., Darley-Usmar V.M., Gladwin M.T. Deoxymyoglobin is a nitrite reductase that generates nitric oxide and regulates mitochondrial respiration. Circulation Research 2007, 100:654-661.
65. Spiegelhalder B., Eisenbrand G., Preussmann R. Influence of dietary nitrate on nitrite content of human saliva: possible relevance to in vivo formation of N-nitroso compounds. Food and Cosmetics Toxicology 1976, 14:545-548.
66. Stromme S.B., Kerem D., Elsner R. Diving bradycardia during rest and exercise and its relation to physical fitness. Journal of Applied Physiology 1970, 28:614-621.
67. Tannenbaum S.R., Correa P. Nitrate and gastric cancer risks. Nature 1985, 317:675-676.
68. Tocco F., Crisafulli A., Melis F., Porru C., Pittau G., Milia R., Concu A. Cardiovascular adjustments in breath-hold diving: comparison between divers and non-divers in simulated dynamic apnoea. European Journal of Applied Physiology 2012, 112:543-554.
69. van Faassen E.E., Bahrami S., Feelisch M., Hogg N., Kelm M., Kim-Shapiro D.B., Kozlov A.V., Li H., Lundberg J.O., Mason R., Nohl H., Rassaf T., Samouilov A., Slama-Schwok A., Shiva S., Vanin A.F., Weitzberg E., Zweier J., Gladwin M.T. Nitrite as regulator of hypoxic signaling in mammalian physiology. Medicinal Research Reviews 2009, 29:683-741.
70. van Maanen J.M., Pachen D.M., Dallinga J.W., Kleinjans J.C. Formation of nitrosamines during consumption of nitrate- and amine-rich foods, and the influence of the use of mouthwashes. Cancer Detection and Prevention 1998, 22:204-212.
71. Vanhatalo A., Bailey S.J., Blackwell J.R., DiMenna F.J., Pavey T.G., Wilkerson D.P., Benjamin N., Winyard P.G., Jones A.M. Acute and chronic effects of dietary nitrate supplementation on blood pressure and the physiological responses to moderate-intensity and incremental exercise. American Journal of Physiology - Regulatory, Integrative, and Comparative Physiology 2010, 299:R1121-R1131.
72. Vanhatalo A., Fulford J., Bailey S.J., Blackwell J.R., Winyard P.G., Jones A.M. Dietary nitrate reduces muscle metabolic perturbation and improves exercise tolerance in hypoxia. The Journal of Physiology 2011, 589:5517-5528.
73. Vanin A.F., Bevers L.M., Slama-Schwok A., van Faassen E.E. Nitric oxide synthase reduces nitrite to NO under anoxia. Cellular and Molecular Life Sciences 2007, 64:96-103.
74. Webb A., Bond R., McLean P., Uppal R., Benjamin N., Ahluwalia A. Reduction of nitrite to nitric oxide during ischemia protects against myocardial ischemia-reperfusion damage. Proceedings of the National Academy of Sciences of the United States of America 2004, 101:13683-13688.
75. Webb A.J., Patel N., Loukogeorgakis S., Okorie M., Aboud Z., Misra S., Rashid R., Miall P., Deanfield J., Benjamin N., MacAllister R., Hobbs A.J., Ahluwalia A. Acute blood pressure lowering, vasoprotective, and antiplatelet properties of dietary nitrate via bioconversion to nitrite. Hypertension 2008, 51:784-790.
76. Weitzberg E., Hezel M., Lundberg J.O. Nitrate-nitrite-nitric oxide pathway: implications for anesthesiology and intensive care. Anesthesiology 2010, 113:1460-1475.
77. Zhang Z., Naughton D.P., Blake D.R., Benjamin N., Stevens C.R., Winyard P.G., Symons M.C., Harrison R. Human xanthine oxidase converts nitrite ions into nitric oxide (NO). Biochemical Society Transactions 1997, 25:524S.