Hydrogen inhalation during normoxic resuscitation improves neurological outcome in a rat model of cardiac arrest independently of targeted temperature management

Circulation

Volumn 130, Issue 24, 2014, Pages 2173-2180

  Hayashida, Kei ^a   Sano, Motoaki ^a   Kamimura, Naomi ^b   Yokota, Takashi ^b   Suzuki, Masaru ^a   Ohta, Shigeo ^b   Fukuda, Keiichi ^a   Hori, Shingo ^a  

^a KEIO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b NIPPON MEDICAL SCHOOL GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

antioxidants; cardiopulmonary resuscitation; heart arrest; ischemia; reperfusion injury

Indexed keywords

HYDROGEN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTIFICIAL VENTILATION; BRAIN CORTEX; BRAIN REGION; CONTROLLED STUDY; HEART ARREST; HEART VENTRICLE FIBRILLATION; HIPPOCAMPUS; HYPEROXIA; MALE; MICROGLIA; MOTOR ACTIVITY; NERVE CELL DEGENERATION; NERVE CELL NECROSIS; NERVE DEGENERATION; NONHUMAN; RAT; RESUSCITATION; RETURN OF SPONTANEOUS CIRCULATION; REVIEW; SURVIVAL RATE; TARGETED TEMPERATURE MANAGEMENT; THERMOREGULATION; TREATMENT OUTCOME; ADVERSE EFFECTS; ANIMAL; BODY TEMPERATURE; CIRCULATION; COMPLICATION; DISEASE MODEL; ELECTROSTIMULATION; INHALATIONAL DRUG ADMINISTRATION; MAZE TEST; NERVOUS SYSTEM DISEASES; PATHOPHYSIOLOGY; PHYSIOLOGY; PROCEDURES; WISTAR RAT;

ADMINISTRATION, INHALATION; ANIMALS; BLOOD CIRCULATION; BODY TEMPERATURE; CEREBRAL CORTEX; DISEASE MODELS, ANIMAL; ELECTRIC STIMULATION; HEART ARREST; HIPPOCAMPUS; HYDROGEN; MALE; MAZE LEARNING; NERVOUS SYSTEM DISEASES; RATS; RATS, WISTAR; RESUSCITATION; VENTRICULAR FIBRILLATION;

EID: 84918520486     PISSN: 00097322     EISSN: 15244539     Source Type: Journal    
DOI: 10.1161/CIRCULATIONAHA.114.011848     Document Type: Review

References (47)

1. Ohsawa I, Ishikawa M, Takahashi K, Watanabe M, Nishimaki K, Yamagata K, Katsura K, Katayama Y, Asoh S, Ohta S. Hydrogen acts as a therapeutic antioxidant by selectively reducing cytotoxic oxygen radicals. Nat Med. 2007;13:688-694.
2. Ohta S. Recent progress toward hydrogen medicine: potential of molecular hydrogen for preventive and therapeutic applications. Curr Pharm Des. 2011;17:2241-2252.
3. Zheng XF, Sun XJ, Xia ZF. Hydrogen resuscitation, a new cytoprotective approach. Clin Exp Pharmacol Physiol. 2011;38:155-163.
4. Hayashida K, Sano M, Ohsawa I, Shinmura K, Tamaki K, Kimura K, Endo J, Katayama T, Kawamura A, Kohsaka S, Makino S, Ohta S, Ogawa S, Fukuda K. Inhalation of hydrogen gas reduces infarct size in the rat model of myocardial ischemia-reperfusion injury. Biochem Biophys Res Commun. 2008;373:30-35.
5. Buchholz BM, Kaczorowski DJ, Sugimoto R, Yang R, Wang Y, Billiar TR, McCurry KR, Bauer AJ, Nakao A. Hydrogen inhalation ameliorates oxidative stress in transplantation induced intestinal graft injury. Am J Transplant. 2008;8:2015-2024.
6. Huang CS, Kawamura T, Lee S, Tochigi N, Shigemura N, Buchholz BM, Kloke JD, Billiar TR, Toyoda Y, Nakao A. Hydrogen inhalation ameliorates ventilator-induced lung injury. Crit Care. 2010;14:R234.
7. Nakao A, Kaczorowski DJ, Wang Y, Cardinal JS, Buchholz BM, Sugimoto R, Tobita K, Lee S, Toyoda Y, Billiar TR, McCurry KR. Amelioration of rat cardiac cold ischemia/reperfusion injury with inhaled hydrogen or carbon monoxide, or both. J Heart Lung Transplant. 2010;29:544-553.
8. Buchholz BM, Masutani K, Kawamura T, Peng X, Toyoda Y, Billiar TR, Bauer AJ, Nakao A. Hydrogen-enriched preservation protects the isogeneic intestinal graft and amends recipient gastric function during transplantation. Transplantation. 2011;92:985-992.
9. Kawamura T, Huang CS, Tochigi N, Lee S, Shigemura N, Billiar TR, Okumura M, Nakao A, Toyoda Y. Inhaled hydrogen gas therapy for prevention of lung transplant-induced ischemia/reperfusion injury in rats. Transplantation. 2010;90:1344-1351.
10. Terasaki Y, Ohsawa I, Terasaki M, Takahashi M, Kunugi S, Dedong K, Urushiyama H, Amenomori S, Kaneko-Togashi M, Kuwahara N, Ishikawa A, Kamimura N, Ohta S, Fukuda Y. Hydrogen therapy attenuates irradiation-induced lung damage by reducing oxidative stress. Am J Physiol Lung Cell Mol Physiol. 2011;301:L415-L426.
11. Yoshida A, Asanuma H, Sasaki H, Sanada S, Yamazaki S, Asano Y, Shinozaki Y, Mori H, Shimouchi A, Sano M, Asakura M, Minamino T, Takashima S, Sugimachi M, Mochizuki N, Kitakaze M. H(2) mediates cardioprotection via involvements of K(ATP) channels and permeability transition pores of mitochondria in dogs. Cardiovasc Drugs Ther. 2012;26:217-226.
12. Hayashida K, Sano M, Kamimura N, Yokota T, Suzuki M, Maekawa Y, Kawamura A, Abe T, Ohta S, Fukuda K, Hori S. H(2) gas improves functional outcome after cardiac arrest to an extent comparable to therapeutic hypothermia in a rat model. J Am Heart Assoc. 2012;1:e003459.
13. Colbourne F, Corbett D. Delayed and prolonged postischemic hypothermia is neuroprotective in the gerbil. Brain Res. 1994;654:265-272.
14. Che D, Li L, Kopil CM, Liu Z, Guo W, Neumar RW. Impact of therapeutic hypothermia onset and duration on survival, neurological function, and neurodegeneration after cardiac arrest. Crit Care Med. 2011;39:1423-1430.
15. Lin JY, Liao XX, Li H, Wei HY, Liu R, Hu CL, Huang GQ, Dai G, Li X. Model of cardiac arrest in rats by transcutaneous electrical epicardium stimulation. Resuscitation. 2010;81:1197-1204.
16. Abella BS, Zhao D, Alvarado J, Hamann K, Vanden Hoek TL, Becker LB. Intra-arrest cooling improves outcomes in a murine cardiac arrest model. Circulation. 2004;109:2786-2791.
17. Janata A, Magnet IA, Uray T, Stezoski JP, Janesko-Feldman K, Tisherman SA, Kochanek PM, Drabek T. Regional TNFα mapping in the brain reveals the striatum as a neuroinflammatory target after ventricular fibrillation cardiac arrest in rats. Resuscitation. 2014;85:694-701.
18. Janata A, Drabek T, Magnet IA, Stezoski JP, Janesko-Feldman K, Popp E, Garman RH, Tisherman SA, Kochanek PM. Extracorporeal versus conventional cardiopulmonary resuscitation after ventricular fibrillation cardiac arrest in rats: a feasibility trial. Crit Care Med. 2013;41:e211-e222.
19. Katz LM, Young A, Frank JE, Wang Y, Park K. Neurotensin-induced hypothermia improves neurological outcome after hypoxic-ischemia. Crit Care Med. 2004;32:806-810.
20. Hickey RW, Ferimer H, Alexander HL, Garman RH, Callaway CW, Hicks S, Safar P, Graham SH, Kochanek PM. Delayed, spontaneous hypothermia reduces neuronal damage after asphyxial cardiac arrest in rats. Crit Care Med. 2000;28:3511-3516.
21. Neumar RW, Bircher NG, Sim KM, Xiao F, Zadach KS, Radovsky A, Katz L, Ebmeyer E, Safar P. Epinephrine and sodium bicarbonate during CPR following asphyxial cardiac arrest in rats. Resuscitation. 1995;29:249-263.
22. Sarnyai Z, Sibille EL, Pavlides C, Fenster RJ, McEwen BS, Toth M. Impaired hippocampal-dependent learning and functional abnormalities in the hippocampus in mice lacking serotonin(1A) receptors. Proc Natl Acad Sci U S A. 2000;97:14731-14736.
23. Schmued LC, Stowers CC, Scallet AC, Xu L. Fluoro-Jade C results in ultra high resolution and contrast labeling of degenerating neurons. Brain Res. 2005;1035:24-31.
24. Böttiger BW, Schmitz B, Wiessner C, Vogel P, Hossmann KA. Neuronal stress response and neuronal cell damage after cardiocirculatory arrest in rats. J Cereb Blood Flow Metab. 1998;18:1077-1087.
25. Horn M, Schlote W. Delayed neuronal death and delayed neuronal recovery in the human brain following global ischemia. Acta Neuropathol. 1992;85:79-87.
26. Hazelton JL, Balan I, Elmer GI, Kristian T, Rosenthal RE, Krause G, Sanderson TH, Fiskum G. Hyperoxic reperfusion after global cerebral ischemia promotes inflammation and long-term hippocampal neuronal death. J Neurotrauma. 2010;27:753-762.
27. Wiessner C, Brink I, Lorenz P, Neumann-Haefelin T, Vogel P, Yamashita K. Cyclin D1 messenger RNA is induced in microglia rather than neurons following transient forebrain ischemia. Neuroscience. 1996;72:947-958.
28. Peberdy MA, Callaway CW, Neumar RW, Geocadin RG, Zimmerman JL, Donnino M, Gabrielli A, Silvers SM, Zaritsky AL, Merchant R, Vanden Hoek TL, Kronick SL; American Heart Association. Part 9: post-cardiac arrest care: 2010 American Heart Association guidelines for cardiopulmonary resuscitation and emergency cardiovascular care. Circulation. 2010;122(suppl 3):S768-S786.
29. Bernard SA, Gray TW, Buist MD, Jones BM, Silvester W, Gutteridge G, Smith K. Treatment of comatose survivors of out-of-hospital cardiac arrest with induced hypothermia. N Engl J Med. 2002;346:557-563.
30. Hypothermia After Cardiac Arrest Study Group. Mild therapeutic hypothermia to improve the neurological outcome after cardiac arrest. N Engl J Med. 2002;346:549-556.
31. Nielsen N, Wetterslev J, Cronberg T, Erlinge D, Gasche Y, Hassager C, Horn J, Hovdenes J, Kjaergaard J, Kuiper M, Pellis T, Stammet P, Wanscher M, Wise MP, Aneman A, Al-Subaie N, Boesgaard S, Bro-Jeppesen J, Brunetti I, Bugge JF, Hingston CD, Juffermans NP, Koopmans M, Køber L, Langørgen J, Lilja G, Møller JE, Rundgren M, Rylander C, Smid O, Werer C, Winkel P, Friberg H; TTM Trial Investigators. Targeted temperature management at 33°C versus 36°C after cardiac arrest. N Engl J Med. 2013;369:2197-2206.
32. Rittenberger JC, Callaway CW. Temperature management and modern post-cardiac arrest care. N Engl J Med. 2013;369:2262-2263.
33. Ye S, Weng Y, Sun S, Chen W, Wu X, Li Z, Weil MH, Tang W. Comparison of the durations of mild therapeutic hypothermia on outcome after cardiopulmonary resuscitation in the rat. Circulation. 2012;125:123-129.
34. Ma L, Lu X, Xu J, Sun S, Tang W. Improved cardiac and neurological outcomes with postresuscitation infusion of cannabinoid receptor agonist WIN55, 212-2 depend on hypothermia in a rat model of cardiac arrest. Crit Care Med. 2014;42:e42-e48.
35. Endo J, Sano M, Katayama T, Hishiki T, Shinmura K, Morizane S, Matsuhashi T, Katsumata Y, Zhang Y, Ito H, Nagahata Y, Marchitti S, Nishimaki K, Wolf AM, Nakanishi H, Hattori F, Vasiliou V, Adachi T, Ohsawa I, Taguchi R, Hirabayashi Y, Ohta S, Suematsu M, Ogawa S, Fukuda K. Metabolic remodeling induced by mitochondrial aldehyde stress stimulates tolerance to oxidative stress in the heart. Circ Res. 2009;105:1118-1127.
36. Niki E. Lipid peroxidation: physiological levels and dual biological effects. Free Radic Biol Med. 2009;47:469-484.
37. Ohta S. Molecular hydrogen as a preventive and therapeutic medical gas: initiation, development and potential of hydrogen medicine. Pharmacol Ther. 2014;144:1-11.
38. Callaway CW, Rittenberger JC, Logue ES, McMichael MJ. Hypothermia after cardiac arrest does not alter serum inflammatory markers. Crit Care Med. 2008;36:2607-2612.
39. Polderman KH. Mechanisms of action, physiological effects, and complications of hypothermia. Crit Care Med. 2009;37(suppl):S186-S202.
40. Kawamura T, Wakabayashi N, Shigemura N, Huang CS, Masutani K, Tanaka Y, Noda K, Peng X, Takahashi T, Billiar TR, Okumura M, Toyoda Y, Kensler TW, Nakao A. Hydrogen gas reduces hyperoxic lung injury via the Nrf2 pathway in vivo. Am J Physiol Lung Cell Mol Physiol. 2013;304:L646-L656.
41. Nakao A, Sugimoto R, Billiar TR, McCurry KR. Therapeutic antioxidant medical gas. J Clin Biochem Nutr. 2009;44:1-13.
42. Itoh T, Fujita Y, Ito M, Masuda A, Ohno K, Ichihara M, Kojima T, Nozawa Y, Ito M. Molecular hydrogen suppresses FcepsilonRI-mediated signal transduction and prevents degranulation of mast cells. Biochem Biophys Res Commun. 2009;389:651-656.
43. George JF, Agarwal A. Hydrogen: another gas with therapeutic potential. Kidney Int. 2010;77:85-87.
44. Victor VM, Espulgues JV, Hernandez-Mijares A, Rocha M. Oxidative stress and mitochondrial dysfunction in sepsis: a potential therapy with mitochondria-targeted antioxidants. Infect Disord Drug Targets. 2009;9:376-389.
45. Xie K, Yu Y, Zhang Z, Liu W, Pei Y, Xiong L, Hou L, Wang G. Hydrogen gas improves survival rate and organ damage in zymosan-induced generalized inflammation model. Shock. 2010;34:495-501.
46. De Keyser J, Sulter G, Luiten PG. Clinical trials with neuroprotective drugs in acute ischemic stroke: are we doing the right thing? Trends Neurosci. 1999;22:535-540.
47. Yang XP, Liu YH, Rhaleb NE, Kurihara N, Kim HE, Carretero OA. Echocardiographic assessment of cardiac function in conscious and anesthetized mice. Am J Physiol. 1999;277(pt 2):H1967-H1974.