Persistently altered brain mitochondrial bioenergetics after apparently successful resuscitation from cardiac arrest

Journal of the American Heart Association

Volumn 4, Issue 9, 2015, Pages

  Kilbaugh, Todd J ^a   Sutton, Robert M ^a   Karlsson, Michael ^c   Hansson, Magnus J ^c   Naim, Maryam Y ^a   Morgan, Ryan W ^a   Bratinov, George ^a   Lampe, Joshua W ^b   Nadkarni, Vinay M ^a   Becker, Lance B ^b   Margulies, Susan S ^d   Berg, Robert A ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b HOSPITAL OF THE UNIVERSITY OF PENNSYLVANIA   (United States)

^c LUND UNIVERSITY   (Sweden)

^d UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Acute brain injury; Brain; Cardiac arrest; Electron transport system; Mitochondria; Neuroprotection

Indexed keywords

CITRATE SYNTHASE; CYTOCHROME C OXIDASE; HYPERTENSIVE FACTOR; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); SUCCINATE DEHYDROGENASE (UBIQUINONE); MULTIENZYME COMPLEX;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOENERGY; BRAIN HYPOXIA; BRAIN MITOCHONDRION; BRAIN TISSUE; CELL DAMAGE; CONTROLLED STUDY; CORONARY ARTERY BLOOD FLOW; ENZYME ACTIVITY; FEMALE; FRONTAL CORTEX; HEART ARREST; HEART VENTRICLE FIBRILLATION; HIPPOCAMPUS; MITOCHONDRIAL ENERGY TRANSFER; NONHUMAN; OXIDATIVE PHOSPHORYLATION; OXYGEN CONSUMPTION; PORCINE MODEL; PRIORITY JOURNAL; RESPIROMETRY; RESUSCITATION; SYSTOLIC BLOOD PRESSURE; ANIMAL; ASPHYXIA; BRAIN CORTEX; CELL RESPIRATION; COMPLICATION; DISEASE MODEL; ENERGY METABOLISM; HEMODYNAMICS; METABOLISM; MITOCHONDRION; PATHOPHYSIOLOGY; PHOSPHORYLATION; PIG; TIME FACTOR;

ANIMALS; ASPHYXIA; CELL RESPIRATION; CEREBRAL CORTEX; DISEASE MODELS, ANIMAL; ELECTRON TRANSPORT CHAIN COMPLEX PROTEINS; ENERGY METABOLISM; FEMALE; HEART ARREST; HEMODYNAMICS; HIPPOCAMPUS; MITOCHONDRIA; PHOSPHORYLATION; RESUSCITATION; SWINE; TIME FACTORS; VENTRICULAR FIBRILLATION;

EID: 84991521038     PISSN: None     EISSN: 20479980     Source Type: Journal    
DOI: 10.1161/JAHA.115.002232     Document Type: Article

References (53)

1. Merchant RM, Yang L, Becker LB, Berg RA, Nadkarni V, Nichol G, Carr BG, Mitra N, Bradley SM, Abella BS, Groeneveld PW; American Heart Association Get With The Guidelines-Resuscitation Investigators. Incidence of treated cardiac arrest in hospitalized patients in the United States. Crit Care Med. 2011;39:2401-2406.
2. Girotra S, Chan PS. Trends in survival after in-hospital cardiac arrest. N Engl J Med. 2013;368:680-681.
3. Ayoub IM, Radhakrishnan J, Gazmuri RJ. Targeting mitochondria for resuscitation from cardiac arrest. Crit Care Med. 2008;36:S440-S446.
4. Gazmuri RJ, Radhakrishnan J. Protecting mitochondrial bioenergetic function during resuscitation from cardiac arrest. Crit Care Clin. 2012;28:245-270.
5. Han F, Da T, Riobo NA, Becker LB. Early mitochondrial dysfunction in electron transfer activity and reactive oxygen species generation after cardiac arrest. Crit Care Med. 2008;36:S447-S453.
6. Chen S-D, Yang D-I, Lin T-K, Shaw F-Z, Liou C-W, Chuang Y-C. Roles of oxidative stress, apoptosis, PGC-1a and mitochondrial biogenesis in cerebral ischemia. Int J Mol Sci. 2011;12:7199-7215.
7. Almeida A, Brooks KJ, Sammut I, Keelan J, Davey GP, Clark JB, Bates TE. Postnatal development of the complexes of the electron transport chain in synaptic mitochondria from rat brain. Dev Neurosci. 1995;17:212-218.
8. Del Maestro R, McDonald W. Distribution of superoxide dismutase, glutathione peroxidase and catalase in developing rat brain. Mech Ageing Dev. 1987;41:29-38.
9. Sutton RM, Friess SH, Maltese MR, Naim MY, Bratinov G, Weiland TR, Garuccio M, Bhalala U, Nadkarni VM, Becker LB, Berg RA. Hemodynamic-directed cardiopulmonary resuscitation during in-hospital cardiac arrest. Resuscitation. 2014;85:983-986.
10. Sutton RM, Friess SH, Naim MY, Lampe JW, Bratinov G, Weiland TR, Garuccio M, Nadkarni VM, Becker LB, Berg RA. Patient-centric blood pressure-targeted cardiopulmonary resuscitation improves survival from cardiac arrest. Am J Respir Crit Care Med. 2014;190:1255-1262.
11. Armstead WM. Age and cerebral circulation. Pathophysiology. 2005;12:5-15.
12. Durham SR, Duhaime A-C. Basic science; maturation-dependent response of the immature brain to experimental subdural hematoma. J Neurotrauma. 2007;24:5-14.
13. Neurauter A, Nysaether J, Kramer-Johansen J, Eilevstjønn J, Paal P, Myklebust H, Wenzel V, Lindner KH, Schmölz W, Pytte M, Steen PA, Strohmenger H-U. Comparison of mechanical characteristics of the human and porcine chest during cardiopulmonary resuscitation. Resuscitation. 2009;80:463-469.
14. Duhaime A-C. Large animal models of traumatic injury to the immature brain. Dev Neurosci. 2006;28:380-387.
15. Missios S, Harris BT, Dodge CP, Simoni MK, Costine BA, Lee Y-L, Quebada PB, Hillier SC, Adams LB, Duhaime A-C. Scaled cortical impact in immature swine:effect of age and gender on lesion volume. J Neurotrauma. 2009;26:1943-1951.
16. Friess SH, Sutton RM, French B, Bhalala U, Maltese MR, Naim MY, Bratinov G, Arciniegas Rodriguez S, Weiland TR, Garuccio M, Nadkarni VM, Becker LB, Berg RA. Hemodynamic directed CPR improves cerebral perfusion pressure and brain tissue oxygenation. Resuscitation. 2014;85:1298-1303.
17. Sutton RM, Friess SH, Bhalala U, Maltese MR, Naim MY, Bratinov G, Niles D, Nadkarni VM, Becker LB, Berg RA. Hemodynamic directed CPR improves short-term survival from asphyxia-associated cardiac arrest. Resuscitation. 2013;84:696-701.
18. Berg RA, Sutton RM, Holubkov R, Nicholson CE, Dean JM, Harrison R, Heidemann S, Meert K, Newth C, Moler F, Pollack M, Dalton H, Doctor A, Wessel D, Berger J, Shanley T, Carcillo J, Nadkarni VM; Eunice Kennedy Shriver National Institute of Child Health and Human Development Collaborative Pediatric Critical Care Research Network and for the American Heart Association's Get With the Guidelines-Resuscitation (formerly the National Registry of Cardiopulmonary Resuscitation) Investigators. Ratio of PICU versus ward cardiopulmonary resuscitation events is increasing. Crit Care Med. 2013;41:2292-2297.
19. Meaney PA, Nadkarni VM, Kern KB, Indik JH, Halperin HR, Berg RA. Rhythms and outcomes of adult in-hospital cardiac arrest. Crit Care Med. 2010;38:101-108.
20. Berg RA, Hilwig RW, Kern KB, Ewy GA. "Bystander" chest compressions and assisted ventilation independently improve outcome from piglet asphyxial pulseless "cardiac arrest". Circulation. 2000;101:1743-1748.
21. Berg RA, Hilwig RW, Kern KB, Babar I, Ewy GA. Simulated mouth-to-mouth ventilation and chest compressions (bystander cardiopulmonary resuscitation) improves outcome in a swine model of prehospital pediatric asphyxial cardiac arrest. Crit Care Med. 1999;27:1893-1899.
22. Karlsson M, Hempel C, Sjövall F, Hansson MJ, Kurtzhals JAL, Elmér E. Brain mitochondrial function in a murine model of cerebral malaria and the therapeutic effects of rhEPO. Int J Biochem Cell Biol. 2013;45:151-155.
23. Kilbaugh TJ, Karlsson M, Byro M, Bebee A, Ralston J, Sullivan S, Duhaime A-C, Hansson MJ, Elmér E, Margulies SS. Mitochondrial bioenergetic alterations after focal traumatic brain injury in the immature brain. Exp Neurol. 2015;271:136-144.
24. Gnaiger E. Capacity of oxidative phosphorylation in human skeletal muscle:new perspectives of mitochondrial physiology. Int J Biochem Cell Biol. 2009;41:1837-1845.
25. Pecinová A, Drahota Z, Nůsková H, Pecina P, Houštěk J. Evaluation of basic mitochondrial functions using rat tissue homogenates. Mitochondrion. 2011;11:722-728.
26. Sims NR, Blass JP. Expression of classical mitochondrial respiratory responses in homogenates of rat forebrain. J Neurochem. 1986;47:496-505.
27. Bowling AC, Mutisya EM, Walker LC, Price DL, Cork LC, Beal MF. Agedependent impairment of mitochondrial function in primate brain. J Neurochem. 1993;60:1964-1967.
28. Chepelev NL, Bennitz JD, Wright JS, Smith JC, Willmore WG. Oxidative modification of citrate synthase by peroxyl radicals and protection with novel antioxidants. J Enzyme Inhib Med Chem. 2009;24:1319-1331.
29. Larsen S, Nielsen J, Hansen CN, Nielsen LB, Wibrand F, Stride N, Schroder HD, Boushel R, Helge JW, Dela F, Hey-Mogensen M. Biomarkers of mitochondrial content in skeletal muscle of healthy young human subjects. J Physiol (Lond). 2012;590:3349-3360.
30. Aidt FH, Nielsen SMB, Kanters J, Pesta D, Nielsen TT, Nørremølle A, Hasholt L, Christiansen M, Hagen CM. Dysfunctional mitochondrial respiration in the striatum of the Huntington's disease transgenic R6/2 mouse model. PLoS Curr. 2013;2:5.
31. Pesta D, Gnaiger E. High-resolution respirometry: OXPHOS protocols for human cells and permeabilized fibers from small biopsies of human muscle. Methods Mol Biol. 2012;810:25-58.
32. Rosenthal RE, Bogaert YE, Fiskum G. Delayed therapy of experimental global cerebral ischemia with acetyl-L-carnitine in dogs. Neurosci Lett. 2005;378:82-87.
33. Niatsetskaya ZV, Sosunov SA, Matsiukevich D, Utkina-Sosunova IV, Ratner VI, Starkov AA, Ten VS. The oxygen free radicals originating from mitochondrial complex I contribute to oxidative brain injury following hypoxia-ischemia in neonatal mice. J Neurosci. 2012;32:3235-3244.
34. Suchadolskiene O, Pranskunas A, Baliutyte G, Veikutis V, Dambrauskas Z, Vaitkaitis D, Borutaite V. Microcirculatory, mitochondrial, and histological changes following cerebral ischemia in swine. BMC Neurosci. 2014;15:2.
35. Robertson CL, Scafidi S, McKenna MC, Fiskum G. Mitochondrial mechanisms of cell death and neuroprotection in pediatric ischemic and traumatic brain injury. Exp Neurol. 2009;218:371-380.
36. Singh IN, Sullivan PG, Deng Y, Mbye LH. Time course of post-traumatic mitochondrial oxidative damage and dysfunction in a mouse model of focal traumatic brain injury: implications for neuroprotective. J Cereb Blood Flow Metab. 2006;26:1407-1418.
37. Gilmer LK, Roberts KN, Joy K, Sullivan PG, Scheff SW. Early mitochondrial dysfunction after cortical contusion injury. J Neurotrauma. 2009;26:1271-1280.
38. Gilland E, Puka-Sundvall M, Hillered L, Hagberg H. Mitochondrial function and energy metabolism after hypoxia-ischemia in the immature rat brain:involvement of NMDA-receptors. J Cereb Blood Flow Metab. 1998;18:297-304.
39. Sims NR. Selective impairment of respiration in mitochondria isolated from brain subregions following transient forebrain ischemia in the rat. J Neurochem. 1991;56:1836-1844.
40. Allen KL, Almeida A, Bates TE, Clark JB. Changes of respiratory chain activity in mitochondrial and synaptosomal fractions isolated from the gerbil brain after graded ischaemia. J Neurochem. 1995;64:2222-2229.
41. Piantadosi CA, Zhang J. Mitochondrial generation of reactive oxygen species after brain ischemia in the rat. Stroke. 1996;27:327-331; discussion 332.
42. Starkov AA. The role of mitochondria in reactive oxygen species metabolism and signaling. Ann N Y Acad Sci. 2008;1147:37-52.
43. Tahara EB, Navarete FDT, Kowaltowski AJ. Tissue-, substrate-, and site-specific characteristics of mitochondrial reactive oxygen species generation. Free Radic Biol Med. 2009;46:1283-1297.
44. Walker KR, Tesco G. Molecular mechanisms of cognitive dysfunction following traumatic brain injury. Front Aging Neurosci. 2013;5:29.
45. Navarro A, Boveris A. Brain mitochondrial dysfunction and oxidative damage in Parkinson's disease. J Bioenerg Biomembr. 2009;41:517-521.
46. Jiang J, Fang X, Fu Y, Xu W, Jiang L, Huang Z. Impaired cerebral mitochondrial oxidative phosphorylation function in a rat model of ventricular fibrillation and cardiopulmonary resuscitation. Biomed Res Int. 2014;2014:1-9.
47. Hansson MJ, Mánsson R, Mattiasson G, Ohlsson J, Karlsson J, Keep MF, Elmér E. Brain-derived respiring mitochondria exhibit homogeneous, complete and cyclosporin-sensitive permeability transition. J Neurochem. 2004; 89:715-729.
48. Sugawara T, Fujimura M, Morita-Fujimura Y, Kawase M, Chan PH. Mitochondrial release of cytochrome c corresponds to the selective vulnerability of hippocampal CA1 neurons in rats after transient global cerebral ischemia. J Neurosci. 1999;19:RC39.
49. Berg RA, Chapman FW, Berg MD, Hilwig RW, Banville I, Walker RG, Nova RC, Sherrill D, Kern KB. Attenuated adult biphasic shocks compared with weightbased monophasic shocks in a swine model of prolonged pediatric ventricular fibrillation. Resuscitation. 2004;61:189-197.
50. Rosenthal G, Hemphill JC III, Sorani M, Martin C, Morabito D, Obrist WD, Manley GT. Brain tissue oxygen tension is more indicative of oxygen diffusion than oxygen delivery and metabolism in patients with traumatic brain injury. Crit Care Med. 2008;36:1917-1924.
51. Kilbaugh TJ, Bhandare S, Lorom DH, Saraswati M, Robertson CL, Margulies SS. Cyclosporin a preserves mitochondrial function after traumatic brain injury in the immature rat and piglet. J Neurotrauma. 2011;28:763-774.
52. Wright MJ, Mcarthur DL, Alger JR, Van Horn J, Irimia A, Filippou M, Glenn TC, Hovda DA, Vespa PM. Early metabolic crisis-related brain atrophy and cognition in traumatic brain injury. Brain Imaging Behav. 2013;7:307-315.
53. Zhang Y, Dong Y, Wu X, Lu Y, Xu Z, Knapp A, Yue Y, Xu T, Xie Z. The mitochondrial pathway of anesthetic isoflurane-induced apoptosis. J Biol Chem. 2010;285:4025-4037.