Restoration of brain circulation and cellular functions hours post-mortem

Nature

Volumn 568, Issue 7752, 2019, Pages 336-343

  Vrselja, Zvonimir ^a   Daniele, Stefano G ^a   Silbereis, John ^a   Talpo, Francesca ^a,b   Morozov, Yury M ^a   Sousa, André M M ^a   Tanaka, Brian S ^a,c   Skarica, Mario ^a   Pletikos, Mihovil ^a,d   Kaur, Navjot ^a   Zhuang, Zhen W ^a   Liu, Zhao ^a   Alkawadri, Rafeed ^a,e   Sinusas, Albert J ^a   Latham, Stephen R ^f   Waxman, Stephen G ^a,c   Sestan, Nenad ^a,g,h  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF PAVIA   (Italy)

^c VA CONNECTICUT HEALTHCARE SYSTEM   (United States)

^d BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^f YALE UNIVERSITY   (United States)

^g Department of Comparative Medicine ^*  (United States)

^h YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANOXIC CONDITIONS; BLOOD; BRAIN; IMMUNE RESPONSE; METABOLISM; OXYGEN; PHYSIOLOGICAL RESPONSE; PIG;

ARTICLE; AUTOPSY; BRAIN CIRCULATION; BRAIN EDEMA; BRAIN HYPOXIA; BRAIN METABOLISM; BRAIN MICROCIRCULATION; CELL ACTIVITY; CELL DEATH; CELL FUNCTION; CEREBRAL ISCHEMIA REPERFUSION INJURY; ELECTROCORTICOGRAPHY; GLIA; PRIORITY JOURNAL; SYNAPSE; ANIMAL; BLOOD; BRAIN; BRAIN ARTERY; BRAIN ISCHEMIA; CELL SURVIVAL; CYTOLOGY; DISEASE MODEL; INFLAMMATION; METABOLISM; MICROCIRCULATION; NERVE CELL; PATHOLOGY; PERFUSION; PHYSIOLOGY; PIG; REPERFUSION INJURY; TIME FACTOR; VASCULARIZATION; VASODILATATION;

MAMMALIA; SUIDAE;

CASPASE 3;

ANIMALS; AUTOPSY; BRAIN; BRAIN ISCHEMIA; CASPASE 3; CELL SURVIVAL; CEREBRAL ARTERIES; CEREBROVASCULAR CIRCULATION; DISEASE MODELS, ANIMAL; HYPOXIA, BRAIN; INFLAMMATION; MICROCIRCULATION; NEUROGLIA; NEURONS; PERFUSION; REPERFUSION INJURY; SWINE; SYNAPSES; TIME FACTORS; VASODILATION;

EID: 85064567941     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/s41586-019-1099-1     Document Type: Article

References (47)

1. Kety, S. S. Circulation and metabolism of the human brain. Brain Res. Bull. 50, 415–416 (1999).
2. Dirnagl, U., Iadecola, C. & Moskowitz, M. A. Pathobiology of ischaemic stroke: an integrated view. Trends Neurosci. 22, 391–397 (1999).
3. Kisler, K., Nelson, A. R., Montagne, A. & Zlokovic, B. V. Cerebral blood flow regulation and neurovascular dysfunction in Alzheimer disease. Nat. Rev. Neurosci. 18, 419–434 (2017).
4. Wagner, S. R., IV & Lanier, W. L. Metabolism of glucose, glycogen, and high-energy phosphates during complete cerebral ischemia. A comparison of normoglycemic, chronically hyperglycemic diabetic, and acutely hyperglycemic nondiabetic rats. Anesthesiology 81, 1516–1526 (1994).
5. Hoxworth, J. M., Xu, K., Zhou, Y., Lust, W. D. & LaManna, J. C. Cerebral metabolic profile, selective neuron loss, and survival of acute and chronic hyperglycemic rats following cardiac arrest and resuscitation. Brain Res. 821, 467–479 (1999).
6. Borjigin, J. et al. Surge of neurophysiological coherence and connectivity in the dying brain. Proc. Natl Acad. Sci. USA 110, 14432–14437 (2013).
7. Cole, S. L. & Corday, E. Four-minute limit for cardiac resuscitation. J. Am. Med. Assoc. 161, 1454–1458 (1956).
8. Grenell, R. G. Central nervous system resistance: the effects of temporary arrest of cerebral circulation for periods of two to ten minutes. J. Neuropathol. Exp. Neurol. 5, 131–154 (1946).
9. Greer, D. M. Mechanisms of injury in hypoxic-ischemic encephalopathy: implications to therapy. Semin. Neurol. 26, 373–379 (2006).
10. 2+ influx during anoxia in mammalian central nervous system white matter. Ann. Neurol. 30, 375–380 (1991).
11. Viel J. J., McManus, D. Q., Cady, C., Evans, M.S. & Brewer, G. J. Temperature and time interval for culture of postmortem neurons from adult rat cortex. J. Neurosci. Res. 64, 311-211 (2001).
12. Verwer, R. W. et al. Cells in human post-mortem brain tissue slices remain alive for several weeks in culture. FASEB J. 16, 54–60 (2002).
13. Onorati, M. et al. Zika virus disrupts phospho-TBK1 localization and mitosis in human neuroepithelial stem cells and radial glia. Cell Rep. 16, 2576-2592 (2016).
14. Charpak, S. & Audinat, E. Cardiac arrest in rodents: maximal duration compatible with a recovery of neuronal activity. Proc. Natl. Acad. Sci. 95, 4748–4753 (1998).
15. Barksdale, K. A. et al. Mitochondrial viability in mouse and human post-mortem brain. FASEB J. 24, 3590–3599 (2010).
16. Hossmann, K. A. & Zimmermann, V. Resuscitation of the monkey brain after 1 h complete ischemia. I. Physiological and morphological observations. Brain Res. 81, 59–74 (1974).
17. Zimmermann, V. & Hossmann, K. A. Resuscitation of the monkey brain after one hour’s complete ischemia. II. Brain water and electrolytes. Brain Res. 85, 1–11 (1975).
18. Kleihues, P., Hossmann, K. A., Pegg, A. E., Kobayashi, K. & Zimmermann, V. Resuscitation of the monkey brain after one hour complete ischemia. III. Indications of metabolic recovery. Brain Res. 95, 61–73 (1975).
19. Hossmann, K. A. & Sato, K. Recovery of neuronal function after prolonged cerebral ischemia. Science 168, 375–376 (1970).
20. Hughes, A., Riou, P. & Day, C. Full neurological recovery from profound (18.0 °C) acute accidental hypothermia: successful resuscitation using active invasive rewarming techniques. Emerg. Med. J. 24, 511–512 (2007).
21. Albers, G. W. et al. Thrombectomy for stroke at 6 to 16 hours with selection by perfusion imaging. N. Engl. J. Med. 378, 708–718 (2018).
22. Haws, C. W., Gourley, J. K. & Heistad, D. D. Effects of nimodipine on cerebral blood flow. J. Pharmacol. Exp. Ther. 225, 24–28 (1983).
23. Schmidt, V. Comparative Anatomy of the Pig Brain: an Integrative Magnetic Resonance Imaging (MRI) Study of the Porcine Brain with Special Emphasis on the External Morphology of the Cerebral Cortex. Thesis, Justus-Liebig-Universität Gießen (2015).
24. Conrad, M. S., Dilger, R. N. & Johnson, R. W. Brain growth of the domestic pig (Sus scrofa) from 2 to 24 weeks of age: a longitudinal MRI study. Dev. Neurosci. 34, 291–298 (2012).
25. Watanabe, H. et al. MR-based statistical atlas of the Göttingen minipig brain. Neuroimage 14, 1089–1096 (2001).
26. Sarwar, M. & McCormick, W. F. Decrease in ventricular and sulcal size after death. Radiology 127, 409–411 (1978).
27. Offiah, C. E. & Dean, J. Post-mortem CT and MRI: appropriate post-mortem imaging appearances and changes related to cardiopulmonary resuscitation. Br. J. Radiol. 89, 20150851 (2016).
28. Schmidt-Kastner, R. & Freund, T. F. Selective vulnerability of the hippocampus in brain ischemia. Neuroscience 40, 599–636 (1991).
29. Crain, B. J., Westerkam, W. D., Harrison, A. H. & Nadler, J. V. Selective neuronal death after transient forebrain ischemia in the Mongolian gerbil: a silver impregnation study. Neuroscience 27, 387–402 (1988).
30. Horn, M. & Schlote, W. Delayed neuronal death and delayed neuronal recovery in the human brain following global ischemia. Acta Neuropathol. 85, 79–87 (1992).
31. Holm, I. E. & West, M. J. Hippocampus of the domestic pig: a stereological study of subdivisional volumes and neuron numbers. Hippocampus 4, 115–125 (1994).
32. Félix, B. et al. Stereotaxic atlas of the pig brain. Brain Res. Bull. 49, 1–137 (1999).
33. Olmos-Serrano, J. L. et al. Down syndrome developmental brain transcriptome reveals defective oligodendrocyte differentiation and myelination. Neuron 89, 1208–1222 (2016).
34. Budde, M. D. & Frank, J. A. Neurite beading is sufficient to decrease the apparent diffusion coefficient after ischemic stroke. Proc. Natl Acad. Sci. USA 107, 14472–14477 (2010).
35. Shin, W. H. et al. Microglia expressing interleukin-13 undergo cell death and contribute to neuronal survival in vivo. Glia 46, 142–152 (2004).
36. Park, K. W., Lee, H. G., Jin, B. K. & Lee, Y. B. Interleukin-10 endogenously expressed in microglia prevents lipopolysaccharide-induced neurodegeneration in the rat cerebral cortex in vivo. Exp. Mol. Med. 39, 812–819 (2007).
37. Kowalski, J., Gan, J., Jonas, P. & Pernía-Andrade, A. J. Intrinsic membrane properties determine hippocampal differential firing pattern in vivo in anesthetized rats. Hippocampus 26, 668–682 (2016). 10.1002/hipo.22550.
38. + channel function and expression. J. Neurosci. 35, 13206–13218 (2015).
39. Lam, T. I. et al. Intracellular pH reduction prevents excitotoxic and ischemic neuronal death by inhibiting NADPH oxidase. Proc. Natl Acad. Sci. USA 110, E4362–E4368 (2013).
40. Hinzen, D. H. et al. Metabolism and function of dog’s brain recovering from longtime ischemia. Am. J. Physiol. 223, 1158–1164 (1972).
41. Hirsch, H., Oberdorster, G., Zimmer, R., Benner, K. U. & Lang, R. The recovery of the electrocorticogram of normothermic canine brains after complete cerebral ischemia. Arch. Psychiatr. Nervenkr. 221, 171–179 (1975).
42. Hirsch, H., Euler, K. H. & Schneider, M. Recovery and resuscitation of the brain after ischemia in normothermia. Pflugers Arch. Gesamte Physiol. Menschen Tiere 265, 281–313 (1957).
43. Hossmann, K. A. & Sato, K. Effect of ischaemia on the function of the sensorimotor cortex in cat. Electroencephalogr. Clin. Neurophysiol. 30, 535–545 (1971).
44. Siesjö, B. K. Cell damage in the brain: a speculative synthesis. J. Cereb. Blood Flow Metab. 1, 155–185 (1981).
45. Farahany, N. A. et al. The ethics of experimenting with human brain tissue. Nature 556, 429–432 (2018).
46. Stacy, M. R. et al. Multimodality imaging approach for serial assessment of regional changes in lower extremity arteriogenesis and tissue perfusion in a porcine model of peripheral arterial disease. Circ. Cardiovasc. Imaging 7, 92–99 (2014).
47. Keep, R. F., Hua, Y. & Xi, G. Brain water content. A misunderstood measurement? Transl. Stroke Res. 3, 263–265 (2012).