Correlated sodium and potassium imbalances within the ischemic core in experimental stroke: A 23Na MRI and histochemical imaging study

Brain Research

Volumn 1527, Issue , 2013, Pages 199-208

  Yushmanov, Victor E ^a   Kharlamov, Alexander ^a   Yanovski, Boris ^a   Laverde, George ^b,d   Boada, Fernando E ^b,e   Jones, Stephen C ^a,b,c  

^a ALLEGHENY SINGER RESEARCH INSTITUTE   (United States)

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

^c CARNEGIE MELLON UNIVERSITY   (United States)

^d YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e NEW YORK UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Focal ischemia; MCAO 23Na; MRI; Permanent; Rat brain; Tissue potassium; Tissue sodium

Indexed keywords

MICROTUBULE ASSOCIATED PROTEIN 2; POTASSIUM; SODIUM; SODIUM 23;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN ISCHEMIA; BRAIN REGION; DIFFUSION WEIGHTED IMAGING; FLAME PHOTOMETRY; IMAGE PROCESSING; IMMUNOHISTOCHEMISTRY; MALE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; RAT; SODIUM TRANSPORT; TREATMENT PLANNING;

RATTUS;

(23)NA MRI; 3D; ADC; APPARENT DIFFUSION COEFFICIENT; BBB; BLOOD-BRAIN BARRIER; BRAIN TISSUE SODIUM AND POTASSIUM CONCENTRATION, RESPECTIVELY; FOCAL ISCHEMIA; MAP2; MCA, MCAO, MCAT; MICROTUBULE-ASSOCIATED PROTEIN 2; MIDDLE CEREBRAL ARTERY, MCA OCCLUSION, AND MCA TRANSECTION WITH BILATERAL COMMON CAROTID ARTERY OCCLUSION, RESPECTIVELY; PERMANENT MCAO; RADIOFREQUENCY; RAT BRAIN; REGION OF INTEREST; RF; ROI; THREE-DIMENSIONAL; TISSUE POTASSIUM; TISSUE SODIUM; [NA(+)](BR) AND [K(+)](BR);

ANIMALS; BRAIN ISCHEMIA; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; POTASSIUM; RATS; RATS, SPRAGUE-DAWLEY; SODIUM; STROKE;

EID: 84881132224     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2013.06.012     Document Type: Article

References (40)

1. L. Alic, J.C. Haeck, K. Bol, S. Klein, S.T. van Tiel, P.A. Wielepolski, J.M. de, W.J. Niessen, M. Bernsen, and J.F. Veenland Facilitating tumor functional assessment by spatially relating 3D tumor histology and in vivo MRI: image registration approach PLoS ONE 6 2011 e22835
2. L. Belayev, O.F. Alonso, R. Busto, W. Zhao, and M.D. Ginsberg Middle cerebral artery occlusion in the rat by intraluminal suture. Neurological and pathological evaluation of an improved model Stroke 27 1996 1616 1622
3. A.L. Betz, R.F. Keep, M.E. Beer, and X. Ren Blood-brain barrier permeability and brain concentration of sodium, potassium, and chloride during focal ischemia J. Cereb. Blood Flow Metab. 14 1994 29 37
4. F.E. Boada, J.S. Gillen, D.C. Noll, G.X. Shen, S.Y. Chang, and K.R. Thulborn Data acquisition and postprocessing strategies for fast quantitative sodium imaging Int. J. Imaging Syst. Technol. 8 1997 544 550
5. F.E. Boada, J.S. Gillen, G.X. Shen, S.Y. Chang, and K.R. Thulborn Fast three dimensional sodium imaging Magn. Reson. Med. 37 1997 706 715
6. F.E. Boada, Y. Qian, E. Nemoto, T. Jovin, C. Jungreis, S.C. Jones, W. Weimar, and V. Lee Sodium MRI and the assessment of irreversible tissue damage during hyper-acute stroke Transl. Stroke Res. 3 2012 236 245
7. D.A. Dawson, and J.M. Hallenbeck Acute focal ischemia-induced alterations in MAP2 immunostaining: description of temporal changes and utilization as a marker for volumetric assessment of acute brain injury J. Cereb. Blood Flow Metab. 16 1996 170 174
8. J.J. Iliff, M. Wang, Y. Liao, B.A. Plogg, W. Peng, G.A. Gundersen, H. Benveniste, G.E. Vates, R. Deane, S.A. Goldman, E.A. Nagelhus, and M. Nedergaard A paravascular pathway facilitates CSF flow through the brain parenchyma and the clearance of interstitial solutes, including amyloid beta Sci. Transl. Med. 4 2012 147ra111
9. U. Ito, K. Ohno, R. Nakamura, F. Suganuma, and Y. Inaba Brain edema during ischemia and after restoration of blood flow: measurement of water, sodium, potassium content and plasma protein permeability Stroke 10 1979 542 547
10. 2 reactivity and heterogeneity of cerebral blood flow in ischemic, border zone, and normal cortex Am. J. Physiol. Heart Circ. Physiol. 257 1989 H473 H482
11. S.C. Jones, W. Hu, Y. Wang, A.D. Perez-Trepichio, V.E. Yushmanov, A. Kharlamov, and F.E. Boada Stability and abrupt fall of brain tissue potassium in rat focal cerebral ischemia and the blood-brain barrier J. Cereb. Blood Flow Metab. 27 Suppl. S1 2007 BO05 BO09, http://www.nature.com/jcbfm/journal/v27/n1s/ pdf/jcbfm.2007.100a.pdf
12. S.C. Jones, A. Kharlamov, B. Yanovski, D.K. Kim, K.A. Easley, V.E. Yushmanov, S.K. Ziolko, and F.E. Boada Stroke onset time using sodium MRI in rat focal cerebral ischemia Stroke 37 2006 883 888
13. H. Kato, K. Kogure, N. Sakamoto, and T. Watanabe Greater disturbance of water and ion homeostasis in the periphery of experimental focal cerebral ischemia Exp. Neurol. 96 1987 118 126
14. A. Kharlamov, D.K. Kim, and S.C. Jones Early visual changes in reflected light on non-stained brain sections after focal ischemia mirror the area of ischemic damage J. Neurosci. Methods 111 2001 67 73
15. br, in the peripheral regions of ischemic core evaluated by quantitative histological potassium staining J. Cereb. Blood Flow Metab. 27 Suppl. S1 2007 BP53-07W, http://www.nature.com/ jcbfm/journal/v27/n1s/pdf/jcbfm.2007.100a.pdf
16. D. Le Bihan, E. Breton, D. Lallemand, P. Grenier, E. Cabanis, and M. Laval-Jeantet MR imaging of intravoxel incoherent motions: application to diffusion and perfusion in neurologic disorders Radiology 161 1986 401 407
17. A.M. Loening, and S.S. Gambhir AMIDE: a free software tool for multimodality medical image analysis Mol. Imaging 2 2003 131 137
18. 2+ exchanger in ischemic damage J. Cereb. Blood Flow Metab. 28 2008 737 746
19. Menon, P.G., Kharlamov, A., Yushmanov, V.E., Yutzy, S.R., Schornack, P.A., Wiener, E.C., Boada, F.E., Jones, S.C., 2012. Automatic spatial identification and 4D tracking of peri-infarct depolarizations in ischemic rat brain using fast ADC MRI. In: Neuroscience Meeting Planner, Neuroscience 2012, New Orleans, LA, October 13-17. Program# 506.24.
20. G. Mies, O. Kloiber, L.R. Drewes, and K.A. Hossmann Cerebral blood flow and regional potassium distribution during focal ischemia of gerbil brain Ann. Neurol. 16 1984 232 237
21. M.E. O'Donnell, L. Tran, T.I. Lam, X.B. Liu, and S.E. Anderson Bumetanide inhibition of the blood-brain barrier Na-K-Cl cotransporter reduces edema formation in the rat middle cerebral artery occlusion model of stroke J. Cereb. Blood Flow Metab. 24 2004 1046 1056
22. L.C. Pettigrew, M.L. Holtz, S.D. Craddock, S.L. Minger, N. Hall, and J.W. Geddes Microtubular proteolysis in focal cerebral ischemia J. Cereb. Blood Flow Metab. 16 1996 1189 1202
23. G.P. Schielke, H.C. Moises, and A.L. Betz Potassium activation of the Na,K-pump in isolated brain microvessels and synaptosomes Brain Res. 524 1990 291 296
24. C.A. Schneider, W.S. Rasband, and K.W. Eliceiri NIH Image to ImageJ: 25 years of image analysis Nat. Methods 9 2012 671 675
25. F.J. Schuier, and K.A. Hossmann Experimental brain infarcts in cats. II. Ischemic brain edema Stroke 11 1980 593 601
26. 1 pattern for sodium and proton imaging of the human brain at 1.5 T Magn. Reson. Med. 38 1997 717 725
27. S. Shibata, C.P. Hodge, and H.M. Pappius Effect of experimental ischemia on cerebral water and electrolytes J. Neurosurg. 41 1974 146 159
28. J.M. Simard, S.K. Woo, G.T. Schwartzbauer, and V. Gerzanich Sulfonylurea receptor 1 in central nervous system injury: a focused review J. Cereb. Blood Flow Metab. 32 2012 1699 1717
29. K.R. Thulborn, T.S. Gindin, D. Davis, and P. Erb Comprehensive MRI protocol for stroke management: tissue sodium concentration as a measure of tissue viability in non-human primate studies and in clinical studies Radiology 213 1999 156 166
30. P. Vigne, G. Champigny, R. Marsault, P. Barbry, C. Frelin, and M. Lazdunski A new type of amiloride-sensitive cationic channel in endothelial cells of brain microvessels J. Biol. Chem. 264 1989 7663 7668
31. B.K. Wallace, S. Foroutan, and M.E. O'Donnell Ischemia-induced stimulation of Na-K-Cl cotransport in cerebral microvascular endothelial cells involves AMP kinase Am. J. Physiol. Cell Physiol. 301 2011 C316 C326
32. Y. Wang, W. Hu, A.D. Perez-Trepichio, T.C. Ng, A.J. Furlan, A.W. Majors, and S.C. Jones Brain tissue sodium is a ticking clock telling time after arterial occlusion in rat focal cerebral ischemia Stroke 31 2000 1386 1392
33. F. Wetterling, L. Gallagher, I.M. Macrae, S. Junge, and A.J. Fagan Regional and temporal variations in tissue sodium concentration during the acute stroke phase Magn. Reson. Med. 67 2012 740 749
34. M. Yang, F. Gao, H. Liu, W.H. Yu, and S.Q. Sun Temporal changes in expression of aquaporin-3, -4, -5 and -8 in rat brains after permanent focal cerebral ischemia Brain Res. 1290 2009 121 132
35. V.E. Yushmanov, A. Kharlamov, F.E. Boada, and S.C. Jones Monitoring of brain potassium with rubidium flame photometry and MRI Magn. Reson. Med. 57 2007 494 500
36. V.E. Yushmanov, A. Kharlamov, F.E. Boada, and S.C. Jones Transient blood-brain barrier disruption and changes in brain electrolytes at the edge of the ischemic core Proc. Int. Soc. Magn. Reson. Med 17 2009 3280
37. 23Na MRI J. Magn. Reson. Imaging 30 2009 18 24
38. 23Na MRI J. Magn. Reson. Imaging 29 2009 962 966
39. 87Rb MRI at 7 T NMR Biomed. 24 2011 778 783
40. V.E. Yushmanov, A. Kharlamov, S.R. Yutzy, P.A. Schornack, P.G. Menon, E.C. Wiener, F.E. Boada, and S.C. Jones 3D tracking of transient peri-infarct depolarizations in ischemic rat brain by fast ADC mapping Proc. Int. Soc. Magn. Reson. Med. 20 2012 3063