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Cerebral Blood Flow Monitoring by Diffuse Speckle Contrast Analysis during MCAO Surgery in the Rat

  • Yeo, Chaebeom (Department of Robotics Engineering, Daegu Gyeongbuk Institute of Science and Technology (DGIST)) ;
  • Kim, Heejaung (Laboratory Animal Center, Daegu Gyeongbuk Medical Innovation Foundation (DGMIF)) ;
  • Song, Cheol (Department of Robotics Engineering, Daegu Gyeongbuk Institute of Science and Technology (DGIST))
  • Received : 2017.06.21
  • Accepted : 2017.09.07
  • Published : 2017.10.25

Abstract

The rodent model has been used frequently to understand stroke pathophysiology, due to its low cost and the large spectrum of genetic strains available. Here, we present a diffuse speckle contrast analysis system (DSCA) with a $1{\times}2$ optical switch that was used to non-invasively assess cerebral blood flow (CBF) changes in the rat during intraluminal suturing for middle cerebral artery occlusion (MCAO) surgery. The blood flow index (BFI) in the left hemisphere was lower than that in the right hemisphere because the left middle cerebral artery was occluded. Furthermore, the performance of the DSCA system was compared with that of commercial laser Doppler flowmetry. The changes in the BFI measured by the two systems were correlated strongly. The DSCA system was less sensitive to motion artifacts and able to measure relatively deep tissue flow in the rat's brain. In conclusion, the DSCA system secured CBF monitoring during surgery in a rodent model without craniotomy.

Keywords

References

  1. J. V. Gijn and M. S. Dennis, "Issues and answers in stroke care," Lancet 352 Suppl. 3, SIII23-27 (1998).
  2. G. Pignataro, A. Scorziello, G. Di Renzo, and L. Annunziato, "Post-ischemic brain damage: effect of ischemic preconditioning and postconditioning and identification of potential candidates for stroke therapy," FEBS J. 276(1), 46-57 (2009). https://doi.org/10.1111/j.1742-4658.2008.06769.x
  3. T. Kirino, "Ischemic tolerance," J. Cereb. Blood Flow Metab. 22(11), 1283-1296 (2002). https://doi.org/10.1097/01.WCB.0000040942.89393.88
  4. A. Durukan, D. Strbian, and T. Tatlisumak, "Rodent models of ischemic stroke: a useful tool for stroke drug development," Curr. Pharm. Des. 14(4), 359-370 (2008). https://doi.org/10.2174/138161208783497688
  5. H. Memezawa, M. L. Smith, and B. K. Siesjo, "Penumbral tissues salvaged by reperfusion following middle cerebral artery occlusion in rats," Stroke 23(4) 552-559 (1992). https://doi.org/10.1161/01.STR.23.4.552
  6. H. Nagasawa and K. Kogure "Correlation between cerebral blood flow and histologic changes in a new rat model of middle cerebral artery occlusion," Stroke 20(8), 1037-1043 (1989). https://doi.org/10.1161/01.STR.20.8.1037
  7. B. Schaller and R. Graf, "Cerebral ischemic preconditioning," J. Neurol. 249(11), 1503-1511 (2002). https://doi.org/10.1007/s00415-002-0933-8
  8. M. I. Macrae, "New models of focal cerebral ischaemia," Br. J. Clin. Pharmacol. 34(4), 302-308 (1992). https://doi.org/10.1111/j.1365-2125.1992.tb05634.x
  9. R. M. K. W. Lee, "Morphology of cerebral arteries," Pharmac. Ther. 66, 149-173 (1995). https://doi.org/10.1016/0163-7258(94)00071-A
  10. M. Boquillon, J. P. Boquillon, and J. Bralet, "Photochemically induced, graded cerebral infarction in the mouse by laser irradiation evolution of brain edema," J. Pharmacol. Toxicol. Methods 27(1), 1-6 (1992). https://doi.org/10.1016/1056-8719(92)90013-Q
  11. A. H. Hainsworth and H. S. Markus, "Do in vivo experimental models reflect human cerebral small vessel disease? A systematic review," J. Cereb. Blood Flow Metab. 28(12), 1877-1891 (2008). https://doi.org/10.1038/jcbfm.2008.91
  12. Q. Liu, Y. Li, H. Lu, and S. Tong, "Real-time high resolution laser speckle imaging of cerebral vascular changes in a rodent photothrombosis model," Biomed. Opt. Express 5(5), 1483-1493 (2014). https://doi.org/10.1364/BOE.5.001483
  13. J. Sharkey and S. P. Butcher, "Characterisation of an experimental model of stroke produced by intracerebral microinjection of endothelin-1 adjacent to the rat middle cerebral artery," J. Neurosci. Methods 60(1-2), 125-131 (1995). https://doi.org/10.1016/0165-0270(95)00003-D
  14. S. K. McCann, G. J. Dusting, and C. L. Roulston, "Early increase of Nox4 NADPH oxidase and superoxide generation following endothelin-1-induced stroke in conscious rats," J. Neurosci. Res. 86(11), 2524-2534 (2008). https://doi.org/10.1002/jnr.21700
  15. J. Koizumi, Y. Yoshida, T. Nakazawa, and G. Ooneda, "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 8, 1-8 (1986). https://doi.org/10.3995/jstroke.8.1
  16. E. Z. Longa, P. R. Weinstein, S. Carlson, and R. Cummins, "Reversible middle cerebral artery occlusion without craniectomy in rats," Stroke 20(1) 84-91 (1989). https://doi.org/10.1161/01.STR.20.1.84
  17. K. Uluc, A. Miranpuri, G. C. Kujoth, E. Akture, and M. K. Baskaya, "Focal cerebral ischemia model by endovascular suture occlusion of the middle cerebral artery in the rat," J. Vis. Exp. (48) e1978 (2011).
  18. E. Toyota, D. C. Warltier, T. Brock, E. Ritman, C. Kolz, P. O'Malley, P. Rocic, M. Focardi, and W. M. Chilian, "Vascular endothelial growth factor is required for coronary collateral growth in the rat," Circulation 112(14), 2108-2113 (20005). https://doi.org/10.1161/CIRCULATIONAHA.104.526954
  19. K. H. Bockhorst, P. A. Narayana, R. Liu, P. Ahobila-Vijjula, J. Ramu, M. Kamel, J. Wosik, T. Bockhorst, K. Hahn, K. M. Hasan, and J. R. Perez-Polo, "Early postnatal development of rat brain: in vivo diffusion tensor imaging," J. Neurosci. Res. 86(7), 1520-1528 (2008). https://doi.org/10.1002/jnr.21607
  20. P. R. Allegrini and D. Sauer, "Application of magnetic resonance imaging to the measurement of neurodegeneration in rat brain: MRI data correlate strongly with histology and enzymatic analysis," Magn. Reson. Imaging 10(5), 773-778 (1992). https://doi.org/10.1016/0730-725X(92)90411-R
  21. Y. F. Wang, S. E. Tsirka, S. Strickland, P. E. Stieg, S. G. Soriano, and S. A. Lipton, "Tissue plasminogen activator (tPA) increase neuronal damage after focal cerebral ischemia in wild-type and tPA-deficient mice," Nat. Med. 4(2), 228-231 (1998). https://doi.org/10.1038/nm0298-228
  22. S. Rajdev, K. Hara, Y. Kokubo, R. Mestril, W. Dillmann, P. R. Weinstein, and F. R. Sharp, "Mice overexpressing rat heat shock protein 70 are protected against cerebral infarction," Ann Neurol. 47(6), 782-791 (2000). https://doi.org/10.1002/1531-8249(200006)47:6<782::AID-ANA11>3.0.CO;2-3
  23. N. E. Stagliano, M. A. Perez-Pinzon, M. A. Moskowitz, and P. L. Huang, "Focal ischemic preconditioning induces rapid tolerance to middle cerebral artery occlusion in mice," J. Cereb. Blood Flow Metab. 19(7), 757-761 (1999). https://doi.org/10.1097/00004647-199907000-00005
  24. J. Ma, C. Ayata, P. L. Huang, M. C. Fishman, and M. A. Moskowitz, "Regional cerebral blood flow response to vibrissal stimulation in mice lacking type I NOS gene expression," Am. J. Physiol. 270(3 Pt 2) H1085-1030 (1996).
  25. A. Y Shih, J. D Driscoll, P. J Drew, N. Nishimura, and C. B Schaffer, and D. Kleinfeld, "Two-photon microscopy as a tool to study blood flow and neurovascular coupling in the rodent brain," J. Cereb. Blood Flow Metab. 32(7) 1277-1309 (2012). https://doi.org/10.1038/jcbfm.2011.196
  26. A. Cho, C. Yeon, D. Kim, and E. Chung, "Laser speckle contrast imaging for measuring cerebral blood flow changes caused by electrical sensory stimulation," J. Opt. Soc. Korea 20(1), 88-93 (2016). https://doi.org/10.3807/JOSK.2016.20.1.088
  27. T. Durdurana and A. G. Yodh, "Diffuse correlation spectroscopy for non-invasive, micro-vascular cerebral blood flow measurement," Neuroimage 85(0 1), 51-63 (2014). https://doi.org/10.1016/j.neuroimage.2013.06.017
  28. Y. Shang, L. Chen, M. Toborek, and G. Yu, "Diffuse optical monitoring of repeated cerebral ischemia in mice," Opt. Express 19(21), 20301-20315 (2011). https://doi.org/10.1364/OE.19.020301
  29. S. Ansari, H. Azari, D. J. McConnell, A. Afzal, and J Mocco, "Intraluminal Middle Cerebral Artery Occlusion (MCAO) model for ischemic stroke with laser doppler flowmetry guidance in mice," J. Vis. Exp. (51), e2879 (2011).
  30. H. Harada, Y. Wang, Y. Mishima, N. Uehara, T. Makaya, and T. Kano, "A novel method of detecting rCBF with laser-Doppler flowmetry without cranial window through the skull for a MCAO rat model," Brain Res. Protoc. 14(3), 165-170 (2005). https://doi.org/10.1016/j.brainresprot.2004.12.007
  31. P. Li and T. H. Murphy, "Two-photon imaging during prolonged middle cerebral artery occlusion in mice reveals recovery of dendritic structure after reperfusion," J. Neurosci. 28(46), 11970-11979 (2008). https://doi.org/10.1523/JNEUROSCI.3724-08.2008
  32. Q. Guo, G. Wang, and S. Namura, "Fenofibrate improves cerebral blood flow after middle cerebral artery occlusion in mice," J. Cereb. Blood Flow Metab. 30(1), 70-78 (2010). https://doi.org/10.1038/jcbfm.2009.185
  33. M. Ren, Z. Lin, H. Qian, G. R. Choudhury, R. Liu, H. Liu, and S. Yang, "Embolic middle cerebral artery occlusion model using thrombin and fibrinogen composed clots in rat," J. Neurosci. Methods 211(2), 296-304 (2012). https://doi.org/10.1016/j.jneumeth.2012.09.006
  34. R. Bi, J. Dong, and K. Lee, "Deep tissue flowmetry based on diffuse speckle contrast analysis," Opt. Lett. 38(9), 1401-1403 (2013). https://doi.org/10.1364/OL.38.001401
  35. J. Dong, K. Lee, and P. M. Grant, "Multi-channel deep tissue flowmetry based on temporal diffuse speckle contrast analysis," Opt. Express 21(19), 22854-22861 (2013). https://doi.org/10.1364/OE.21.022854
  36. C. Yeo, H. C. Park. K. Lee, and C. Song, "Avian embryo monitoring during incubation using multi-channel diffuse speckle contrast analysis," Biomed. Opt. Express 7(1), 93-98 (2016). https://doi.org/10.1364/BOE.7.000093
  37. C. Yeo and C. Song, "Diffuse speckle contrast analysis with novel fiber-lens detection," Proc. of SPIE 100059, 1005904 (2017).
  38. R. L. Yeager, J. A. Franzosa, D. S. Millsap, J. L. Angell- Yeager, S. S. Heise, P. Wakhungu, J. Lim, H. T. Whelan, J. T. Eells, and D. S. Henshel, "Effects of 670-nm phototherapy on development," Photomed. Laser Surg. 23(3), 268-272 (2005). https://doi.org/10.1089/pho.2005.23.268
  39. G. Yu, T. Durduran, C. Zhou, R. Cheng, and A. G. Yodh, "Near-infrared diffuse correlation spectroscopy for assessment of tissue blood flow," in Handbook of Biomedical Optics, 195-216 (2011).
  40. M. J. Leahy, F. F. M. de Mul, G. E. Nilsson, and R. Maniewski, "Principles and practice of the laser-Doppler perfusion technique," Technol Health Care. 7(2-3), 143-162 (1999).