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History of Preclinical Models of Intracerebral Hemorrhage

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Intracerebral Hemorrhage Research

Part of the book series: Acta Neurochirurgica Supplementum ((NEUROCHIRURGICA,volume 111))

Abstract

In order to understand a disease process, effective modeling is required that can assist scientists in understanding the pathophysiological processes that take place. Intracerebral hemorrhage (ICH), a devastating disease representing 15% of all stroke cases, is just one example of how scientists have developed models that can effectively mimic human clinical scenarios. Currently there are three models of hematoma injections that are being used to induce an ICH in subjects. They include the microballoon model introduced in 1987 by Dr. David Mendelow, the bacterial collagenase injection model introduced in 1990 by Dr. Gary Rosenberg, and the autologous blood injection model introduced by Dr. Guo-Yuan Yang in 1994. These models have been applied on various animal models beginning in 1963 with canines, followed by rats and rabbits in 1982, pigs in 1996, and mice just recently in 2003. In this review, we will explore in detail the various injection models and animal subjects that have been used to study the ICH process while comparing and analyzing the benefits and disadvantages of each.

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References

  1. Rosenberg GA, Mun-Bryce S, Wesley M, Kornfeld M (1990) Collagenase-induced intracerebral hemorrhage in rats. Stroke 21:801–807

    PubMed  CAS  Google Scholar 

  2. Sinar EJ, Mendelow AD, Graham DI, Teasdale GM (1987) Experimental intracerebral hemorrhage: effects of a temporary mass lesion. J Neurosurg 66:568–576. doi:10.3171/jns.1987.66.4.0568

    Article  PubMed  CAS  Google Scholar 

  3. Yang GY, Betz AL, Chenevert TL, Brunberg JA, Hoff JT (1994) Experimental intracerebral hemorrhage: relationship between brain edema, blood flow, and blood-brain barrier permeability in rats. J Neurosurg 81:93–102. doi:10.3171/jns.1994.81.1.0093

    Article  PubMed  CAS  Google Scholar 

  4. Rojas H, Zhang JH (2008) Animal models of spontaneous intracerebral hemorrhage. In: Zhang JH (ed) Advancements in neurological research. Research SignPost, pp 39–89, ISBN:978-81-308-0225-1

    Google Scholar 

  5. Nath FP, Jenkins A, Mendelow AD, Graham DI, Teasdale GM (1986) Early hemodynamic changes in experimental intracerebral hemorrhage. J Neurosurg 65:697–703. doi:10.3171/jns.1986.65.5.0697

    Article  PubMed  CAS  Google Scholar 

  6. Wu B, Ma Q, Khatibi N, Chen W, Sozen T, Cheng O, Tang J (2010) Ac-YVAD-CMK decreases blood-brain barrier degradation by inhibiting caspase-1 activation of interleukin-1beta in intracerebral hemorrhage mouse model. Transl Stroke Res 1(1):57–64

    Article  PubMed  CAS  Google Scholar 

  7. Harris ED Jr, Krane SM (1974) Collagenases (third of three parts). N Engl J Med 291:652–661

    Article  PubMed  Google Scholar 

  8. Montfort I, Perez-Tamayo R (1975) The distribution of collagenase in normal rat tissues. J Histochem Cytochem 23:910–920

    Article  PubMed  CAS  Google Scholar 

  9. James ML, Warner DS, Laskowitz DT (2008) Preclinical models of intracerebral hemorrhage: a translational perspective. Neurocrit Care 9:139–152. doi:10.1007/s12028-007-9030-2

    Article  PubMed  Google Scholar 

  10. Andaluz N, Zuccarello M, Wagner KR (2002) Experimental animal models of intracerebral hemorrhage. Neurosurg Clin N Am 13:385–393

    Article  PubMed  Google Scholar 

  11. Fujii Y (1972) Studies on induced hypothermia for open heart surgery. II. Adequate flow of hypothermic perfusion in the dog. Nippon Geka Hokan 41:149–159

    PubMed  CAS  Google Scholar 

  12. Kazui S, Naritomi H, Yamamoto H, Sawada T, Yamaguchi T (1996) Enlargement of spontaneous intracerebral hemorrhage. Incidence time course. Stroke 27:1783–1787

    PubMed  CAS  Google Scholar 

  13. Ropper AH, Zervas NT (1982) Cerebral blood flow after experimental basal ganglia hemorrhage. Ann Neurol 11:266–271. doi:10.1002/ana.410110306

    Article  PubMed  CAS  Google Scholar 

  14. Bullock R, Mendelow AD, Teasdale GM, Graham DI (1984) Intracranial haemorrhage induced at arterial pressure in the rat. Part 1: description of technique, ICP changes and neuropathological findings. Neurol Res 6:184–188

    PubMed  CAS  Google Scholar 

  15. Deinsberger W, Vogel J, Kuschinsky W, Auer LM, Boker DK (1996) Experimental intracerebral hemorrhage: description of a double injection model in rats. Neurol Res 18:475–477

    PubMed  CAS  Google Scholar 

  16. Segal R, Dujovny M, Nelson D et al. (1982) Local urokinase treatment for spontaneous intracerebral hematoma. Clin Res 30:412A

    Google Scholar 

  17. Bullock R, Brock-Utne J, van Dellen J, Blake G (1988) Intracerebral hemorrhage in a primate model: effect on regional cerebral blood flow. Surg Neurol 29:101–107

    Article  PubMed  CAS  Google Scholar 

  18. Fujii Y, Tanaka R, Takeuchi S, Koike T, Minakawa T, Sasaki O (1994) Hematoma enlargement in spontaneous intracerebral hemorrhage. J Neurosurg 80:51–57. doi:10.3171/jns.1994.80.1.0051

    Article  PubMed  CAS  Google Scholar 

  19. Whisnant JP, Sayre GP, Millikan CH (1963) Experimental intracerebral hematoma. Arch Neurol 9(6):586–592

    Google Scholar 

  20. Sugi T, Fujishima M, Omae T (1975) Lactate and pyruvate concentrations, and acid-base balance of cerebrospinal fluid in experimentally induced intracerebral and subarachnoid hemorrhage in dogs. Stroke 6:715–719

    PubMed  CAS  Google Scholar 

  21. Qureshi AI, Wilson DA, Hanley DF, Traystman RJ (1999) No evidence for an ischemic penumbra in massive experimental intracerebral hemorrhage. Neurology 52:266–272

    PubMed  CAS  Google Scholar 

  22. Qureshi AI, Wilson DA, Traystman RJ (1999) Treatment of elevated intracranial pressure in experimental intracerebral hemorrhage: comparison between mannitol and hypertonic saline. Neurosurgery 44:1055–1063, discussion 1063–1054

    Article  PubMed  CAS  Google Scholar 

  23. Lee EJ, Hung YC, Lee MY (1999) Anemic hypoxia in moderate intracerebral hemorrhage: the alterations of cerebral hemodynamics and brain metabolism. J Neurol Sci 164:117–123. doi:S0022-510X(99)00068-4 [pii]

    Article  PubMed  CAS  Google Scholar 

  24. Takasugi S, Ueda S, Matsumoto K (1985) Chronological changes in spontaneous intracerebral hematoma – an experimental and clinical study. Stroke 16:651–658

    PubMed  CAS  Google Scholar 

  25. Wagner KR, Xi G, Hua Y, Kleinholz M, de Courten-Myers GM, Myers RE, Broderick JP, Brott TG (1996) Lobar intracerebral hemorrhage model in pigs: rapid edema development in perihematomal white matter. Stroke 27:490–497

    PubMed  CAS  Google Scholar 

  26. Kuker W, Thiex R, Rohde I, Rohde V, Thron A (2000) Experimental acute intracerebral hemorrhage. Value of MR sequences for a safe diagnosis at 1.5 and 0.5 T. Acta Radiol 41:544–552

    Article  PubMed  CAS  Google Scholar 

  27. Mun-Bryce S, Wilkerson AC, Papuashvili N, Okada YC (2001) Recurring episodes of spreading depression are spontaneously elicited by an intracerebral hemorrhage in the swine. Brain Res 888:248–255. doi:S0006-8993(00)03068-7 [pii]

    Article  PubMed  CAS  Google Scholar 

  28. Kaufman HH, Pruessner JL, Bernstein DP, Borit A, Ostrow PT, Cahall DL (1985) A rabbit model of intracerebral hematoma. Acta Neuropathol 65:318–321

    Article  PubMed  CAS  Google Scholar 

  29. Koeppen AH, Dickson AC, McEvoy JA (1995) The cellular reactions to experimental intracerebral hemorrhage. J Neurol Sci 134(Suppl):102–112. doi:0022510X9500215N [pii]

    Article  PubMed  Google Scholar 

  30. Qureshi AI, Ling GS, Khan J, Suri MF, Miskolczi L, Guterman LR, Hopkins LN (2001) Quantitative analysis of injured, necrotic, and apoptotic cells in a new experimental model of intracerebral hemorrhage. Crit Care Med 29:152–157

    Article  PubMed  CAS  Google Scholar 

  31. Gustafsson O, Rossitti S, Ericsson A, Raininko R (1999) MR imaging of experimentally induced intracranial hemorrhage in rabbits during the first 6 hours. Acta Radiol 40:360–368

    Article  PubMed  CAS  Google Scholar 

  32. Rohde V, Rohde I, Thiex R, Ince A, Jung A, Duckers G, Groschel K, Rottger C, Kuker W, Muller HD, Gilsbach JM (2002) Fibrinolysis therapy achieved with tissue plasminogen activator and aspiration of the liquefied clot after experimental intracerebral hemorrhage: rapid reduction in hematoma volume but intensification of delayed edema formation. J Neurosurg 97:954–962. doi:10.3171/jns.2002.97.4.0954

    Article  PubMed  CAS  Google Scholar 

  33. Masuda T, Dohrmann GJ, Kwaan HC, Erickson RK, Wollman RL (1988) Fibrinolytic activity in experimental intracerebral hematoma. J Neurosurg 68:274–278. doi:10.3171/jns.1988.68.2.0274

    Article  PubMed  CAS  Google Scholar 

  34. Nakamura T, Xi G, Hua Y, Schallert T, Hoff JT, Keep RF (2004) Intracerebral hemorrhage in mice: model characterization and application for genetically modified mice. J Cereb Blood Flow Metab 24:487–494. doi:00004647-200405000-00002 [pii]

    Article  PubMed  Google Scholar 

  35. Belayev L, Saul I, Curbelo K, Busto R, Belayev A, Zhang Y, Riyamongkol P, Zhao W, Ginsberg MD (2003) Experimental intracerebral hemorrhage in the mouse: histological, behavioral, and hemodynamic characterization of a double-injection model. Stroke 34:2221–2227. doi:10.1161/01.STR.0000088061.06656.1E

    Article  PubMed  Google Scholar 

  36. Ma B, Zhang J (2006) Nimodipine treatment to assess a modified mouse model of intracerebral hemorrhage. Brain Res 1078:182–188. doi:S0006-8993(06)00158-2 [pii]

    Article  PubMed  CAS  Google Scholar 

  37. Rynkowski MA, Kim GH, Komotar RJ, Otten ML, Ducruet AF, Zacharia BE, Kellner CP, Hahn DK, Merkow MB, Garrett MC, Starke RM, Cho BM, Sosunov SA, Connolly ES (2008) A mouse model of intracerebral hemorrhage using autologous blood infusion. Nat Protoc 3:122–128. doi:nprot.2007.513 [pii]

    Article  PubMed  CAS  Google Scholar 

  38. Choudhri TF, Hoh BL, Solomon RA, Connolly ES Jr, Pinsky DJ (1997) Use of a spectrophotometric hemoglobin assay to objectively quantify intracerebral hemorrhage in mice. Stroke 28:2296–2302

    PubMed  CAS  Google Scholar 

  39. Clark W, Gunion-Rinker L, Lessov N, Hazel K (1998) Citicoline treatment for experimental intracerebral hemorrhage in mice. Stroke 29:2136–2140

    PubMed  CAS  Google Scholar 

  40. Thiex R, Mayfrank L, Rohde V, Gilsbach JM, Tsirka SA (2004) The role of endogenous versus exogenous tPA on edema formation in murine ICH. Exp Neurol 189:25–32. doi:10.1016/j.expneurol.2004.05.021

    Article  PubMed  CAS  Google Scholar 

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Acknowledgement

This study is partially supported by NIH NS053407 to J.H. Zhang and NS060936 to J. Tang.

Conflict of interest statement We declare that we have no conflict of interest.

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Authors and Affiliations

  1. Department of Physiology and Pharmacology, Loma Linda University, School of Medicine, Risley Hall, Room 219, Loma Linda, CA, 92354, USA

    Qingyi Ma, Hank Chen, Jiping Tang & John H. Zhang

  2. Department of Anesthesiology, Loma Linda University, School of Medicine, Loma Linda, CA, USA

    Nikan H. Khatibi & John H. Zhang

  3. Department of Neurosurgery, Loma Linda University, School of Medicine, Loma Linda, CA, USA

    John H. Zhang

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  1. Qingyi Ma
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  2. Nikan H. Khatibi
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  3. Hank Chen
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  4. Jiping Tang
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  5. John H. Zhang
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Corresponding author

Correspondence to Jiping Tang .

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Editors and Affiliations

  1. , Neurosurgery, Physiology, Loma Linda University, Campus Street 11041, Loma Linda, 92530, USA

    John Zhang

  2. School of Medicine, Dept. Neurosurgery, Loma Linda University, Anderson St. 11234, Loma Linda, 92354, California, USA

    Austin Colohan

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Ma, Q., Khatibi, N.H., Chen, H., Tang, J., Zhang, J.H. (2011). History of Preclinical Models of Intracerebral Hemorrhage. In: Zhang, J., Colohan, A. (eds) Intracerebral Hemorrhage Research. Acta Neurochirurgica Supplementum, vol 111. Springer, Vienna. https://doi.org/10.1007/978-3-7091-0693-8_1

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  • DOI: https://doi.org/10.1007/978-3-7091-0693-8_1

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  • Online ISBN: 978-3-7091-0693-8

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