Skip to content
BY-NC-ND 3.0 license Open Access Published by De Gruyter Open Access June 29, 2014

Identification of hyperacute ischemic stroke with a more homogenous nature

  • Kyung Yi EMAIL logo , Hong Lee , Sang-Rae Lee , Youngjeon Lee , Seung Lee , Chulhyun Lee and Sang-Hoon Cha

Abstract

Previous reports revealed that middle cerebral artery occlusion (MCAO) models in rats were very diverse in nature, and experimental stroke of a more homogenous nature had not been previously documented. This paper aims to present our novel observations of experimental stroke in rats with similar MRI characteristics after MCAO. Immediately after MCAO, 19 rats were placed into a 4.7 T MRI scanner, and diffusion weighted imaging (DWI) of axial and coronal planes was repeated every 10 minutes up to post-occlusion 115 minutes. Apparent diffusion coefficient (ADC) values of the ischemic lesions were calculated and compared to those of the unaffected contra-lateral hemispheres. Successful MCAO was defined when the whole left MCA territory showed ADC abnormality on DWI. Percentage of hemispheric lesion volume (% HLV), relative ADC value (rADC), and relative DWI signal intensity (rDWI) were serially evaluated for quantitative analysis of ADC-derived lesion characteristics. Successful MCA territorial infarction was induced in nine rats (9/19, 47.4%). In quantitative analysis of ADC-derived lesion characteristics, lesion volumes of seven rats (group 1) were very similar, but larger than those of the other two rats (group 2): % HLV of initial MRI = 45.4 ± 2.5 / 19.1 ± 6.6. rADCs and rDWIs of group 1 showed similar patterns of temporal change, which was different from those of group 2. Using prospective diffusion MRI after MCAO in rats, we identified territorial hyperacute ischemic lesions with similar MRI characteristics. This observation would contribute to the establishment of more homogenous rodent models for ischemic stroke translational research.

[1] Kilkenny C., Browne W.J., Cuthill I.C., Emerson M., Altman D.G., Improving bioscience research reporting: the ARRIVE guidelines for reporting animal research, J. Pharmacol.Pharmacother., 2010, 1, 94–99 http://dx.doi.org/10.4103/0976-500X.7235110.4103/0976-500X.72351Search in Google Scholar

[2] Donnan G.A., Fisher M., Macleod M., Davis S.M., Stroke, Lancet, 2008, 371, 1612–1623 http://dx.doi.org/10.1016/S0140-6736(08)60694-710.1016/S0140-6736(08)60694-7Search in Google Scholar

[3] Philip M., Benatar M., Fisher M., Savitz S.I., Methodological quality of animal studies of neuroprotective agents currently in phase II/III acute ischemic stroke trials, Stroke, 2009, 40, 577–581 http://dx.doi.org/10.1161/STROKEAHA.108.52433010.1161/STROKEAHA.108.524330Search in Google Scholar

[4] Koizumi JY.Y., Nakazawa T, Ooneda G., Experimental studies of ischemic brain edema, I: a new experimental model of cerebral embolism in rats in which recirculation can be introduced in the ischemic area, Jpn. J. Stroke, 1986, 1–8 10.3995/jstroke.8.1Search in Google Scholar

[5] Macrae I.M., Preclinical stroke research — advantages and disadvantages of the most common rodent models of focal ischaemia, Br. J. Pharmacol., 2011, 164, 1062–1078 http://dx.doi.org/10.1111/j.1476-5381.2011.01398.x10.1111/j.1476-5381.2011.01398.xSearch in Google Scholar

[6] Laing R.J., Jakubowski J., Laing R.W., Middle cerebral artery occlusion without craniectomy in rats. Which method works best?, Stroke, 1993, 24, 294–297; discussion 297–298 http://dx.doi.org/10.1161/01.STR.24.2.29410.1161/01.STR.24.2.294Search in Google Scholar

[7] Kuge Y., Minematsu K., Yamaguchi T., Miyake Y., Nylon monofilament for intraluminal middle cerebral artery occlusion in rats, Stroke, 1995, 26, 1655–1657; discussion 1658 http://dx.doi.org/10.1161/01.STR.26.9.1655Search in Google Scholar

[8] Hata R., Mies G., Wiessner C., Fritze K., Hesselbarth D., Brinker G., et al., A reproducible model of middle cerebral artery occlusion in mice: hemodynamic, biochemical, and magnetic resonance imaging, J. Cereb. Search in Google Scholar

[9] Pierpaoli C., Alger J.R., Righini A., Mattiello J., Dickerson R., Des Pres D., et al., High temporal resolution diffusion MRI of global cerebral ischemia and reperfusion, J. Cereb. Blood Flow Metab., 1996, 16, 892–905 http://dx.doi.org/10.1097/00004647-199609000-0001310.1097/00004647-199609000-00013Search in Google Scholar

[10] Kastrup A., Engelhorn T., Beaulieu C., de Crespigny A., Moseley M.E., Dynamics of cerebral injury, perfusion, and blood-brain barrier changes after temporary and permanent middle cerebral artery occlusion in the rat, J. Neurol. Sci., 1999, 166, 91–99 http://dx.doi.org/10.1016/S0022-510X(99)00121-510.1016/S0022-510X(99)00121-5Search in Google Scholar

[11] Gerriets T., Stolz E., Walberer M., Muller C., Kluge A., Kaps M., et al., Middle cerebral artery occlusion during MR-imaging: investigation of the hyperacute phase of stroke using a new in-bore occlusion model in rats, Brain Res. Protoc., 2004, 12, 137–143 http://dx.doi.org/10.1016/j.brainresprot.2003.08.00610.1016/j.brainresprot.2003.08.006Search in Google Scholar PubMed

[12] Gerriets T., Stolz E., Walberer M., Muller C., Rottger C., Kluge A., et al., Complications and pitfalls in rat stroke models for middle cerebral artery occlusion: a comparison between the suture and the macrosphere model using magnetic resonance angiography, Stroke, 2004, 35, 2372–2377 http://dx.doi.org/10.1161/01.STR.0000142134.37512.a710.1161/01.STR.0000142134.37512.a7Search in Google Scholar PubMed

[13] Meng X., Fisher M., Shen Q., Sotak C.H., Duong T.Q., Characterizing the diffusion/perfusion mismatch in experimental focal cerebral ischemia, Ann. Neurol., 2004, 55, 207–212 http://dx.doi.org/10.1002/ana.1080310.1002/ana.10803Search in Google Scholar PubMed PubMed Central

[14] Bardutzky J., Shen Q., Henninger N., Schwab S., Duong T.Q., Fisher M., Characterizing tissue fate after transient cerebral ischemia of varying duration using quantitative diffusion and perfusion imaging, Stroke, 2007, 38, 1336–1344 http://dx.doi.org/10.1161/01.STR.0000259636.26950.3b10.1161/01.STR.0000259636.26950.3bSearch in Google Scholar PubMed PubMed Central

[15] Bardutzky J., Shen Q., Henninger N., Bouley J., Duong T.Q., Fisher M., Differences in ischemic lesion evolution in different rat strains using diffusion and perfusion imaging, Stroke, 2005, 36, 2000–2005 http://dx.doi.org/10.1161/01.STR.0000177486.85508.4d10.1161/01.STR.0000177486.85508.4dSearch in Google Scholar PubMed PubMed Central

[16] Alonso de Leciñana M., Diez-Tejedor E., Gutierrez M., Guerrero S., Carceller F., Roda J.M., New goals in ischemic stroke therapy: the experimental approach — harmonizing science with practice, Cerebrovasc. Dis., 2005, 20(Suppl. 2), 159–168 http://dx.doi.org/10.1159/00008937010.1159/000089370Search in Google Scholar PubMed

[17] Mergenthaler P., Meisel A., Do stroke models model stroke?, Dis. Model. Mech., 2012, 5, 718–725 http://dx.doi.org/10.1242/dmm.01003310.1242/dmm.010033Search in Google Scholar PubMed PubMed Central

[18] Gerriets T., Stolz E., Walberer M., Muller C., Kluge A., Bachmann A., et al., Noninvasive quantification of brain edema and the spaceoccupying effect in rat stroke models using magnetic resonance imaging, Stroke, 2004, 35, 566–571 http://dx.doi.org/10.1161/01.STR.0000113692.38574.5710.1161/01.STR.0000113692.38574.57Search in Google Scholar PubMed

[19] Porter D.A., Heidemann R.M., High resolution diffusion-weighted imaging using readout-segmented echo-planar imaging, parallel imaging and a two-dimensional navigator-based reacquisition, Magn. Reson. Med., 2009, 62, 468–475 http://dx.doi.org/10.1002/mrm.2202410.1002/mrm.22024Search in Google Scholar PubMed

[20] Durukan A., Tatlisumak T., Acute ischemic stroke: overview of major experimental rodent models, pathophysiology, and therapy of focal cerebral ischemia, Pharmacol. Biochem. Behav., 2007, 87, 179–197 http://dx.doi.org/10.1016/j.pbb.2007.04.01510.1016/j.pbb.2007.04.015Search in Google Scholar PubMed

[21] Seo H.S., Na D.G., Kim J.H., Kim K.W., Son K.R., Correlation between CT and diffusion-weighted imaging of acute cerebral ischemia in a rat model, AJNR Am. J. Neuroradiol., 2011, 32, 728–733 http://dx.doi.org/10.3174/ajnr.A236210.3174/ajnr.A2362Search in Google Scholar PubMed PubMed Central

[22] Kim J.H., Na D.G., Chang K.H., Song I.C., Choi S.H., Son K.R., et al., Serial MR analysis of early permanent and transient ischemia in rats: diffusion tensor imaging and high b value diffusion weighted imaging, Korean J. Radiol., 2013, 14, 307–315 http://dx.doi.org/10.3348/kjr.2013.14.2.30710.3348/kjr.2013.14.2.307Search in Google Scholar PubMed PubMed Central

[23] Shen Q., Meng X., Fisher M., Sotak C.H., Duong T.Q., Pixel-bypixel spatiotemporal progression of focal ischemia derived using quantitative perfusion and diffusion imaging, J. Cereb. Blood Flow Metab., 2003, 23, 1479–1488 http://dx.doi.org/10.1097/01.WCB.0000100064.36077.0310.1097/01.WCB.0000100064.36077.03Search in Google Scholar

[24] Gill R., Sibson N.R., Hatfield R.H., Burdett N.G., Carpenter T.A., Hall L.D., et al., A comparison of the early development of ischaemic damage following permanent middle cerebral artery occlusion in rats as assessed using magnetic resonance imaging and histology, J. Cereb. Blood Flow Metab., 1995, 15, 1–11 http://dx.doi.org/10.1038/jcbfm.1995.110.1038/jcbfm.1995.1Search in Google Scholar

[25] Kohno K., Hoehn-Berlage M., Mies G., Back T., Hossmann K.A., Relationship between diffusion-weighted MR images, cerebral blood flow, and energy state in experimental brain infarction, Magn. Reson. Imaging, 1995, 13, 73–80 http://dx.doi.org/10.1016/0730-725X(94)00080-M10.1016/0730-725X(94)00080-MSearch in Google Scholar

[26] Zille M., Farr T.D., Przesdzing I., Muller J., Sommer C., Dirnagl U., et al., Visualizing cell death in experimental focal cerebral ischemia: promises, problems, and perspectives, J. Cereb. Blood Flow Metab., 2012, 32, 213–231 http://dx.doi.org/10.1038/jcbfm.2011.15010.1038/jcbfm.2011.150Search in Google Scholar PubMed PubMed Central

[27] Benveniste H., Hedlund L.W., Johnson G.A., Mechanism of detection of acute cerebral ischemia in rats by diffusion-weighted magnetic resonance microscopy, Stroke, 1992, 23, 746–754 http://dx.doi.org/10.1161/01.STR.23.5.74610.1161/01.STR.23.5.746Search in Google Scholar PubMed

[28] Mintorovitch J., Yang G.Y., Shimizu H., Kucharczyk J., Chan P.H., Weinstein P.R., Diffusion-weighted magnetic resonance imaging of acute focal cerebral ischemia: comparison of signal intensity with changes in brain water and Na+,K(+)-ATPase activity, J. Cereb. Blood Flow Metab., 1994, 14, 332–336 http://dx.doi.org/10.1038/jcbfm.1994.4010.1038/jcbfm.1994.40Search in Google Scholar PubMed

[29] Wick M., Nagatomo Y., Prielmeier F., Frahm J., Alteration of intracellular metabolite diffusion in rat brain in vivo during ischemia and reperfusion, Stroke, 1995, 26, 1930–1933; discussion 1934 http://dx.doi.org/10.1161/01.STR.26.10.1930Search in Google Scholar

[30] van der Toorn A., Dijkhuizen R.M., Tulleken C.A., Nicolay K., Diffusion of metabolites in normal and ischemic rat brain measured by localized 1H MRS, Magn. Reson. Med., 1996, 36, 914–922 http://dx.doi.org/10.1002/mrm.191036061410.1002/mrm.1910360614Search in Google Scholar PubMed

[31] Duong T.Q., Ackerman J.J., Ying H.S., Neil J.J., Evaluation of extra- and intracellular apparent diffusion in normal and globally ischemic rat brain via 19F NMR, Magn. Reson. Med., 1998, 40, 1–13 http://dx.doi.org/10.1002/mrm.191040010210.1002/mrm.1910400102Search in Google Scholar PubMed

[32] Hoehn-Berlage M., Norris D.G., Kohno K., Mies G., Leibfritz D., Hossmann K.A., Evolution of regional changes in apparent diffusion coefficient during focal ischemia of rat brain: the relationship of quantitative diffusion NMR imaging to reduction in cerebral blood flow and metabolic disturbances, J. Cereb. Blood Flow Metab., 1995, 15, 1002–1011 http://dx.doi.org/10.1038/jcbfm.1995.12610.1038/jcbfm.1995.126Search in Google Scholar PubMed

[33] Miyabe M., Mori S., van Zijl P.C., Kirsch J.R., Eleff S.M., Koehler R.C., et al., Correlation of the average water diffusion constant with cerebral blood flow and ischemic damage after transient middle cerebral artery occlusion in cats, J. Cereb. Blood Flow Metab., 1996, 16, 881–891 http://dx.doi.org/10.1097/00004647-199609000-0001210.1097/00004647-199609000-00012Search in Google Scholar PubMed

[34] Rivers C.S., Wardlaw J.M., What has diffusion imaging in animals told us about diffusion imaging in patients with ischaemic stroke?, Cerebrovasc. Dis., 2005, 19, 328–336 http://dx.doi.org/10.1159/00008469110.1159/000084691Search in Google Scholar PubMed

[35] Kokubo Y., Matson G.B., Liu J., Mancuso A., Kayama T., Sharp F.R., et al., Correlation between changes in apparent diffusion coefficient and induction of heat shock protein, cell-specific injury marker expression, and protein synthesis reduction on diffusion-weighted magnetic resonance images after temporary focal cerebral ischemia in rats, J. Neurosurg., 2002, 96, 1084–1093 http://dx.doi.org/10.3171/jns.2002.96.6.108410.3171/jns.2002.96.6.1084Search in Google Scholar PubMed

[36] Lee S.K., Kim D.I., Kim S.Y., Kim D.J., Lee J.E., Kim J.H., Reperfusion cellular injury in an animal model of transient ischemia, AJNR Am. J. Neuroradiol., 2004, 25, 1342–1347 Search in Google Scholar

[37] Neumann-Haefelin T., Kastrup A., de Crespigny A., Yenari M.A., Ringer T., Sun G.H., et al., Serial MRI after transient focal cerebral ischemia in rats: dynamics of tissue injury, blood-brain barrier damage, and edema formation, Stroke, 2000, 31, 1965–1972; discussion 1972–1963 http://dx.doi.org/10.1161/01.STR.31.8.196510.1161/01.STR.31.8.1965Search in Google Scholar

Published Online: 2014-6-29
Published in Print: 2014-6-1

© 2014 Versita Warsaw

This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 3.0 License.

Downloaded on 8.5.2024 from https://www.degruyter.com/document/doi/10.2478/s13380-014-0215-9/html
Scroll to top button