Cerebral blood flow during reperfusion predicts later brain damage in a mouse and a rat model of neonatal hypoxic-ischemic encephalopathy

Experimental Neurology

Volumn 233, Issue 1, 2012, Pages 481-489

  Ohshima, Makiko ^a   Tsuji, Masahiro ^a   Taguchi, Akihiko ^a   Kasahara, Yukiko ^a   Ikeda, Tomoaki ^a  

^a NATIONAL CEREBRAL AND CARDIOVASCULAR CENTER   (Japan)

Author keywords

Cerebral blood flow; Dexamethasone; Hypoxic ischemic brain injury; Laser speckle flowmetry; Mouse; Neonatal; Rat; Reperfusion

Indexed keywords

DEXAMETHASONE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN BLOOD FLOW; BRAIN DAMAGE; CAROTID ARTERY OBSTRUCTION; CONTROLLED STUDY; DISEASE ASSOCIATION; FEMALE; FLOW MEASUREMENT; HEMISPHERIC DOMINANCE; HEMODYNAMICS; HISTOPATHOLOGY; HYPOXIC ISCHEMIC ENCEPHALOPATHY; INJURY SCALE; LASER SPECKLE FLOWMETRY; MALE; MOUSE; NEONATAL HYPOXIC ISCHEMIC ENCEPHALOPATHY; NEUROPATHOLOGY; NEWBORN; NONHUMAN; PRIORITY JOURNAL; RAT; REPERFUSION;

ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; BRAIN; BRAIN INJURIES; CEREBROVASCULAR CIRCULATION; DEXAMETHASONE; DISEASE MODELS, ANIMAL; FEMALE; FUNCTIONAL LATERALITY; HYPOXIA-ISCHEMIA, BRAIN; LASER-DOPPLER FLOWMETRY; MALE; MICE; NEUROPROTECTIVE AGENTS; PREDICTIVE VALUE OF TESTS; RATS; RATS, WISTAR; REGIONAL BLOOD FLOW; REPERFUSION; STATISTICS AS TOPIC; TIME FACTORS;

EID: 84856219575     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2011.11.025     Document Type: Article

References (41)

1. Ayata C., Dunn A.K., Gursoy O.Y., Huang Z., Boas D.A., Moskowitz M.A. Laser speckle flowmetry for the study of cerebrovascular physiology in normal and ischemic mouse cortex. J. Cereb. Blood Flow Metab. 2004, 24:744-755.
2. Bonnin P., Leger P.L., Deroide N., Fau S., Baud O., Pocard M., et al. Impact of intracranial blood-flow redistribution on stroke size during ischemia-reperfusion in 7-day-old rats. J. Neurosci. Methods 2011, 198:103-109.
3. Comi A.M., Johnston M.V., Wilson M.A. Strain variability, injury distribution, and seizure onset in a mouse model of stroke in the immature brain. Dev. Neurosci. 2005, 27:127-133.
4. Derugin N., Wendland M., Muramatsu K., Roberts T.P., Gregory G., Ferriero D.M., et al. Evolution of brain injury after transient middle cerebral artery occlusion in neonatal rats. Stroke 2000, 31:1752-1761.
5. Dunn A.K., Bolay H., Moskowitz M.A., Boas D.A. Dynamic imaging of cerebral blood flow using laser speckle. J. Cereb. Blood Flow Metab. 2001, 21:195-201.
6. Fabian R.H., Perez-Polo J.R., Kent T.A. Perivascular nitric oxide and superoxide in neonatal cerebral hypoxia-ischemia. Am. J. Physiol. Heart Circ. Physiol. 2008, 295:H1809-H1814.
7. Fellman V., Raivio K.O. Reperfusion injury as the mechanism of brain damage after perinatal asphyxia. Pediatr. Res. 1997, 41:599-606.
8. Forrester K.R., Stewart C., Tulip J., Leonard C., Bray R.C. Comparison of laser speckle and laser doppler perfusion imaging: measurement in human skin and rabbit articular tissue. Med. Biol. Eng. Comput. 2002, 40:687-697.
9. Fujita Y., Ihara M., Ushiki T., Hirai H., Kizaka-Kondoh S., Hiraoka M., et al. Early protective effect of bone marrow mononuclear cells against ischemic white matter damage through augmentation of cerebral blood flow. Stroke 2010, 41:2938-2943.
10. Ilves P., Talvik R., Talvik T. Changes in Doppler ultrasonography in asphyxiated term infants with hypoxic-ischaemic encephalopathy. Acta Paediatr. 1998, 87:680-684.
11. Ioroi T., Yonetani M., Nakamura H. Effects of hypoxia and reoxygenation on nitric oxide production and cerebral blood flow in developing rat striatum. Pediatr. Res. 1998, 43:733-737.
12. Johnston M.V., Ferriero D.M., Vannucci S.J., Hagberg H. Models of cerebral palsy: which ones are best?. J. Child Neurol. 2005, 20:984-987.
13. Karlsson B.R., Grogaard B., Gerdin B., Steen P.A. The severity of postischemic hypoperfusion increases with duration of cerebral ischemia in rats. Acta Anaesthesiol. Scand. 1994, 38:248-253.
14. Kirimi E., Tuncer O., Atas B., Sakarya M.E., Ceylan A. Clinical value of color doppler ultrasonography measurements of full-term newborns with perinatal asphyxia and hypoxic ischemic encephalopathy in the first 12hours of life and long-term prognosis. Tohoku J. Exp. Med. 2002, 197:27-33.
15. Lindström K., Lagerroos P., Gillberg C., Fernell E. Teenage outcome after being born at term with moderate neonatal encephalopathy. Pediatr. Neurol. 2006, 35:268-274.
16. Liu X.H., Kwon D., Schielke G.P., Yang G.Y., Silverstein F.S., Barks J.D. Mice deficient in interleukin-1 converting enzyme are resistant to neonatal hypoxic-ischemic brain damage. J. Cereb. Blood Flow Metab. 1999, 19:1099-1108.
17. Matsiukevich D., Randis T.M., Utkina-Sosunova I., Polin R.A., Ten V.S. The state of systemic circulation, collapsed or preserved defines the need for hyperoxic or normoxic resuscitation in neonatal mice with hypoxia-ischemia. Resuscitation 2010, 81:224-229.
18. Mujsce D.J., Christensen M.A., Vannucci R.C. Cerebral blood flow and edema in perinatal hypoxic-ischemic brain damage. Pediatr. Res. 1990, 27:450-453.
19. Pryds O., Greisen G., Lou H., Friis-Hansen B. Vasoparalysis associated with brain damage in asphyxiated term infants. J. Pediatr. 1990, 117:119-125.
20. Qiao M., Latta P., Foniok T., Buist R., Meng S., Tomanek B., et al. Cerebral blood flow response to a hypoxic-ischemic insult differs in neonatal and juvenile rats. MAGMA 2004, 17:117-124.
21. Rice J.E., Vannucci R.C., Brierley J.B. The influence of immaturity on hypoxic-ischemic brain damage in the rat. Ann. Neurol. 1981, 9:131-141.
22. Ringel M., Bryan R.M., Vannucci R.C. Regional cerebral blood flow during hypoxia-ischemia in the immature rat: comparison of iodoantipyrine and iodoamphetamine as radioactive tracers. Brain Res. Dev. Brain Res. 1991, 59:231-235.
23. Riyamongkol P., Zhao W., Liu Y., Belayev L., Busto R., Ginsberg M.D. Automated registration of laser Doppler perfusion images by an adaptive correlation approach: application to focal cerebral ischemia in the rat. J. Neurosci. Methods 2002, 122:79-90.
24. Rosenbaum J.L., Almli C.R., Yundt K.D., Altman D.I., Powers W.J. Higher neonatal cerebral blood flow correlates with worse childhood neurologic outcome. Neurology 1997, 49:1035-1041.
25. Sheldon R.A., Sedik C., Ferriero D.M. Strain-related brain injury in neonatal mice subjected to hypoxia-ischemia. Brain Res. 1998, 810:114-122.
26. Stern M.D., Lappe D.L., Bowen P.D., Chimosky J.E., Holloway G.A., Keiser H.R., et al. Continuous measurement of tissue blood flow by laser-Doppler spectroscopy. Am. J. Physiol. 1977, 232:H441-H448.
27. Strong A.J., Bezzina E.L., Anderson P.J., Boutelle M.G., Hopwood S.E., Dunn A.K. Evaluation of laser speckle flowmetry for imaging cortical perfusion in experimental stroke studies: quantitation of perfusion and detection of peri-infarct depolarisations. J. Cereb. Blood Flow Metab. 2006, 26:645-653.
28. Taguchi A., Soma T., Tanaka H., Kanda T., Nishimura H., Yoshikawa H., et al. Administration of CD34+ cells after stroke enhances neurogenesis via angiogenesis in a mouse model. J. Clin. Invest. 2004, 114:330-338.
29. Taguchi A., Kasahara Y., Nakagomi T., Stern D.M., Fukunaga M., Ishikawa M., et al. A reproducible and simple model of permanent cerebral ischemia in CB-17 and SCID mice. J. Exp. Stroke Transl. Med. 2010, 3:28-33.
30. Taniguchi H., Mohri I., Okabe-Arahori H., Aritake K., Wada K., Kanekiyo T., et al. Prostaglandin D2 protects neonatal mouse brain from hypoxic ischemic injury. J. Neurosci. 2007, 27:4303-4312.
31. Ten V.S., Wu E.X., Tang H., Bradley-Moore M., Fedarau M.V., Ratner V.I., et al. Late measures of brain injury after neonatal hypoxia-ischemia in mice. Stroke 2004, 35:2183-2188.
32. Todd N.V., Picozzi P., Crockard H.A., Russell R.R. Reperfusion after cerebral ischemia: influence of duration of ischemia. Stroke 1986, 17:460-466.
33. Tsuji M., Wilson M.A., Lange M.S., Johnston M.V. Minocycline worsens hypoxic-ischemic brain injury in a neonatal mouse model. Exp. Neurol. 2004, 189:58-65.
34. Tuor U.I. Dexamethasone and the prevention of neonatal hypoxic-ischemic brain damage. Ann. N. Y. Acad. Sci. 1995, 765:179-195.
35. Tuor U.I., Simone C.S., Barks J.D., Post M. Dexamethasone prevents cerebral infarction without affecting cerebral blood flow in neonatal rats. Stroke 1993, 24:452-457.
36. van Bel F., Dorrepaal C.A., Benders M.J., Zeeuwe P.E., van de Bor M., Berger H.M. Changes in cerebral hemodynamics and oxygenation in the first 24hours after birth asphyxia. Pediatrics 1993, 92:365-372.
37. van Handel M., Swaab H., de Vries L.S., Jongmans M.J. Long-term cognitive and behavioral consequences of neonatal encephalopathy following perinatal asphyxia: a review. Eur. J. Pediatr. 2007, 166:645-654.
38. van Velthoven C.T., Kavelaars A., van Bel F., Heijnen C.J. Nasal administration of stem cells: a promising novel route to treat neonatal ischemic brain damage. Pediatr. Res. 2010, 68:419-422.
39. Vannucci R.C., Lyons D.T., Vasta F. Regional cerebral blood flow during hypoxia-ischemia in immature rats. Stroke 1988, 19:245-250.
40. Wainwright M.S., Grundhoefer D., Sharma S., Black S.M. A nitric oxide donor reduces brain injury and enhances recovery of cerebral blood flow after hypoxia-ischemia in the newborn rat. Neurosci. Lett. 2007, 415:124-129.
41. Wendland M.F., Faustino J., West T., Manabat C., Holtzman D.M., Vexler Z.S. Early diffusion-weighted MRI as a predictor of caspase-3 activation after hypoxic-ischemic insult in neonatal rodents. Stroke 2008, 39:1862-1868.