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A Rat Model of Surgical Brain Injury

  • Prativa Sherchan
  • Devin W. McBride
  • Lei Huang
  • Cesar Reis
  • Onat Akyol
  • Yuechun Wang
  • Cherine Kim
  • Ishan Solaroglu
  • Jiping Tang
  • John H. ZhangEmail author
Chapter
Part of the Springer Series in Translational Stroke Research book series (SSTSR)

Abstract

The rat model of surgical brain injury (SBI) mimics deleterious sequelae resulting from the unavoidable damage to healthy tissue during many neurosurgical procedures, such as peri-operative hemorrhage, brain edema, and neuroinflammation. The SBI model is ideal for evaluating pre-conditioning, pre-treatment, and peri-operative therapies. The SBI model is characterized by partial frontal lobe resection. First, a 5 × 5 mm cranial window in the right frontal bone is made to expose the underlying brain tissue. Next, partial resection of the frontal lobe is performed along margins of the bone window which is followed by saline irrigation and intraoperative packing to ensure complete hemostasis. The total time for completion of the SBI surgery in a rat is 30–40 min. The partial resection of frontal lobe results in contralateral sensorimotor deficits and anxiety-like behavior in rats. Neurological tests to evaluate anxiety-related behavior in SBI rats have been described in this chapter and are recommended for studies using the SBI rat model. The elevated plus maze test and open field test showed greater sensitivity than the forced swim test to detect anxiety-like behavior in rats after SBI. The rat model of SBI allows for investigation of therapeutics that target SBI-induced complications including intraoperative hemorrhage, post-operative hematoma, brain edema, blood brain barrier disruption, neuroinflammation, cell death and oxidative stress which are also briefly described in this chapter.

Keywords

Surgical brain injury SBI Rat Animal model Neurosurgery Anxiety tests 

References

  1. 1.
    Dautremont JF, et al. Cost-effectiveness analysis of a postoperative clinical care pathway in head and neck surgery with microvascular reconstruction. J Otolaryngol Head Neck Surg. 2013;42:59.CrossRefGoogle Scholar
  2. 2.
    Andrews RJ, Muto RP. Retraction brain ischaemia: cerebral blood flow, evoked potentials, hypotension and hyperventilation in a new animal model. Neurol Res. 1992;14:12–8.CrossRefGoogle Scholar
  3. 3.
    Deletis V, Sala F. The role of intraoperative neurophysiology in the protection or documentation of surgically induced injury to the spinal cord. Ann N Y Acad Sci. 2001;939:137–44.CrossRefGoogle Scholar
  4. 4.
    Hellwig D, Bertalanffy H, Bauer BL, Tirakotai W. Pontine hemorrhage. J Neurosurg. 2003;99:796; author reply: 796–7.PubMedGoogle Scholar
  5. 5.
    Jadhav V, Solaroglu I, Obenaus A, Zhang JH. Neuroprotection against surgically induced brain injury. Surg Neurol. 2007;67:15–20; discussion 20.CrossRefGoogle Scholar
  6. 6.
    Borshchagovskii ML, Dubikaitis IuV. [Clinico-electroencephalographic characteristics of the condition of brain stem systems following surgical and non-surgical brain injury]. Zhurnal nevropatologii i psikhiatrii imeni S.S. Korsakova. 1976;76:337–344.Google Scholar
  7. 7.
    Eckermann JM, et al. Hydrogen is neuroprotective against surgically induced brain injury. Med Gas Res. 2011;1:7.CrossRefGoogle Scholar
  8. 8.
    Frontczak-Baniewicz M, Walski M. New vessel formation after surgical brain injury in the rat’s cerebral cortex I. Formation of the blood vessels proximally to the surgical injury. Acta Neurobiol Exp. 2003;63:65–75.Google Scholar
  9. 9.
    Jadhav V, Zhang JH. Surgical brain injury: prevention is better than cure. Front Biosci. 2008;13:3793–7.CrossRefGoogle Scholar
  10. 10.
    Sherchan P, Kim CH, Zhang JH. Surgical brain injury and edema prevention. Acta Neurochir Suppl. 2013;118:129–33.PubMedGoogle Scholar
  11. 11.
    McBride DW, Wang YC, Sherchan P, Tang JP, Zhang JH. Correlation between subacute sensorimotor deficits and brain water content after surgical brain injury in rats. Behav Brain Res. 2015;290:161–71.CrossRefGoogle Scholar
  12. 12.
    Frumberg DB, Fernando MS, Lee DE, Biegon A, Schiffer WK. Metabolic and behavioral deficits following a routine surgical procedure in rats. Brain Res. 2007;1144:209–18.CrossRefGoogle Scholar
  13. 13.
    Lee DH, et al. Reproducible and persistent weakness in adult rats after surgical resection of motor cortex: evaluation with limb placement test. Childs Nerv Syst. 2009;25:1547–53.CrossRefGoogle Scholar
  14. 14.
    Frontczak-Baniewicz M, et al. Morphological evidence of the beneficial role of immune system cells in a rat model of surgical brain injury. Folia Neuropathol. 2013;51:324–32.CrossRefGoogle Scholar
  15. 15.
    Frontczak-Baniewicz M, Walski M, Madejska G, Sulejczak D. MMP2 and MMP9 in immature endothelial cells following surgical injury of rat cerebral cortex—a preliminary study. Folia Neuropathol. 2009;47:338–46.PubMedGoogle Scholar
  16. 16.
    Frontczak-Baniewicz M, Walski M, Sulejczak D. Diversity of immunophenotypes of endothelial cells participating in new vessel formation following surgical rat brain injury. J Physiol Pharmacol. 2007;58(Suppl 5):193–203.PubMedGoogle Scholar
  17. 17.
    Sulejczak D, Grieb P, Walski M, Frontczak-Baniewicz M. Apoptotic death of cortical neurons following surgical brain injury. Folia Neuropathol. 2008;46:213–9.PubMedGoogle Scholar
  18. 18.
    Ayer RE, et al. Preoperative mucosal tolerance to brain antigens and a neuroprotective immune response following surgical brain injury. J Neurosurg. 2012;116:246–53.CrossRefGoogle Scholar
  19. 19.
    Bravo TP, et al. Role of histamine in brain protection in surgical brain injury in mice. Brain Res. 2008;1205:100–7.CrossRefGoogle Scholar
  20. 20.
    Jadhav V, et al. Hyperbaric oxygen preconditioning reduces postoperative brain edema and improves neurological outcomes after surgical brain injury. Acta Neurochir Suppl. 2010;106:217–20.CrossRefGoogle Scholar
  21. 21.
    Jadhav V, et al. Cyclo-oxygenase-2 mediates hyperbaric oxygen preconditioning-induced neuroprotection in the mouse model of surgical brain injury. Stroke. 2009;40:3139–42.CrossRefGoogle Scholar
  22. 22.
    Jafarian N, et al. Mucosal tolerance to brain antigens preserves endogenous TGFbeta-1 and improves neurological outcomes following experimental craniotomy. Acta Neurochir Suppl. 2011;111:283–7.CrossRefGoogle Scholar
  23. 23.
    Zheng Y, et al. An experimental study on thymus immune tolerance to treat surgical brain injury. Chin Med J. 2014;127:685–90.PubMedGoogle Scholar
  24. 24.
    Frontczak-Baniewicz M, Chrapusta SJ, Sulejczak D. Long-term consequences of surgical brain injury—characteristics of the neurovascular unit and formation and demise of the glial scar in a rat model. Folia Neuropathol. 2011;49:204–18.PubMedGoogle Scholar
  25. 25.
    Xu FF, et al. Effects of progesterone vs. dexamethasone on brain oedema and inflammatory responses following experimental brain resection. Brain Inj. 2014;28:1594–601.CrossRefGoogle Scholar
  26. 26.
    Benggon M, Chen H, Applegate R, Martin R, Zhang JH. Effect of dexmedetomidine on brain edema and neurological outcomes in surgical brain injury in rats. Anesth Analg. 2012;115:154–9.CrossRefGoogle Scholar
  27. 27.
    Di F, et al. Role of aminoguanidine in brain protection in surgical brain injury in rat. Neurosci Lett. 2008;448:204–7.CrossRefGoogle Scholar
  28. 28.
    Hao W, Wu XQ, Xu RT. The molecular mechanism of aminoguanidine-mediated reduction on the brain edema after surgical brain injury in rats. Brain Res. 2009;1282:156–61.CrossRefGoogle Scholar
  29. 29.
    Hyong A, et al. Rosiglitazone, a PPAR gamma agonist, attenuates inflammation after surgical brain injury in rodents. Brain Res. 2008;1215:218–24.CrossRefGoogle Scholar
  30. 30.
    Jadhav V, Matchett G, Hsu FP, Zhang JH. Inhibition of Src tyrosine kinase and effect on outcomes in a new in vivo model of surgically induced brain injury. J Neurosurg. 2007;106:680–6.CrossRefGoogle Scholar
  31. 31.
    Jadhav V, Yamaguchi M, Obenaus A, Zhang JH. Matrix metalloproteinase inhibition attenuates brain edema after surgical brain injury. Acta Neurochir Suppl. 2008;102:357–61.CrossRefGoogle Scholar
  32. 32.
    Khatibi NH, et al. Prostaglandin E2 EP1 receptor inhibition fails to provide neuroprotection in surgically induced brain-injured mice. Acta Neurochir Suppl. 2011;111:277–81.CrossRefGoogle Scholar
  33. 33.
    Lee S, et al. The antioxidant effects of melatonin in surgical brain injury in rats. Acta Neurochir Suppl. 2008;102:367–71.CrossRefGoogle Scholar
  34. 34.
    Lo W, et al. NADPH oxidase inhibition improves neurological outcomes in surgically-induced brain injury. Neurosci Lett. 2007;414:228–32.CrossRefGoogle Scholar
  35. 35.
    Manaenko A, et al. PAR-1 antagonist SCH79797 ameliorates apoptosis following surgical brain injury through inhibition of ASK1-JNK in rats. Neurobiol Dis. 2013;50:13–20.CrossRefGoogle Scholar
  36. 36.
    Westra D, Chen W, Tsuchiyama R, Colohan A, Zhang JH. Pretreatment with normobaric and hyperbaric oxygenation worsens cerebral edema and neurologic outcomes in a murine model of surgically induced brain injury. Acta Neurochir Suppl. 2011;111:243–51.CrossRefGoogle Scholar
  37. 37.
    Yamaguchi M, Jadhav V, Obenaus A, Colohan A, Zhang JH. Matrix metalloproteinase inhibition attenuates brain edema in an in vivo model of surgically-induced brain injury. Neurosurgery. 2007;61:1067–75; discussion 1075–6.CrossRefGoogle Scholar
  38. 38.
    Fan D, et al. The protective mechanism for the blood-brain barrier induced by aminoguanidine in surgical brain injury in rats. Cell Mol Neurobiol. 2011;31:1213–9.CrossRefGoogle Scholar
  39. 39.
    Asahi M, Asahi K, Wang X, Lo EH. Reduction of tissue plasminogen activator-induced hemorrhage and brain injury by free radical spin trapping after embolic focal cerebral ischemia in rats. J Cereb Blood Flow Metab. 2000;20:452–7.CrossRefGoogle Scholar
  40. 40.
    Choudhri TF, Hoh BL, Solomon RA, Connolly ES Jr, Pinsky DJ. Use of a spectrophotometric hemoglobin assay to objectively quantify intracerebral hemorrhage in mice. Stroke. 1997;28:2296–302.CrossRefGoogle Scholar
  41. 41.
    Tang JP, et al. MMP-9 deficiency enhances collagenase-induced intracerebral hemorrhage and brain injury in mutant mice. J Cereb Blood Flow Metab. 2004;24:1133–45.CrossRefGoogle Scholar
  42. 42.
    Sherchan P, et al. Recombinant Slit2 attenuates neuroinflammation after surgical brain injury by inhibiting peripheral immune cell infiltration via Robo1-srGAP1 pathway in a rat model. Neurobiol Dis. 2016;85:164–73.CrossRefGoogle Scholar
  43. 43.
    Huang L, et al. Phosphoinositide 3-kinase gamma contributes to neuroinflammation in a rat model of surgical brain injury. J Neurosci. 2015;35:10390–401.CrossRefGoogle Scholar
  44. 44.
    Walf AA, Frye CA. The use of the elevated plus maze as an assay of anxiety-related behavior in rodents. Nat Protoc. 2007;2:322–8.CrossRefGoogle Scholar
  45. 45.
    File SE, Lippa AS, Beer B Lippa MT. Animal tests of anxiety. Curr Protoc Neurosci. 2004;8:8.3.Google Scholar
  46. 46.
    Seibenhener ML, Wooten MC. Use of the open field maze to measure locomotor and anxiety-like behavior in mice. J Vis Exp. 2015;(96):e52434.Google Scholar
  47. 47.
    Abdollahnejad F, et al. Investigation of sedative and hypnotic effects of Amygdalus communis L. extract: behavioral assessments and EEG studies on rat. J Nat Med. 2016;70(2):190–7.CrossRefGoogle Scholar
  48. 48.
    Slattery DA, Cryan JF. Using the rat forced swim test to assess antidepressant-like activity in rodents. Nat Protoc. 2012;7:1009–14.CrossRefGoogle Scholar
  49. 49.
    Ohl F. Testing for anxiety. Clin Neurosci Res. 2003;3:233–8.CrossRefGoogle Scholar
  50. 50.
    Bertoglio LJ, Carobrez AP. Previous maze experience required to increase open arms avoidance in rats submitted to the elevated plus-maze model of anxiety. Behav Brain Res. 2000;108:197–203.CrossRefGoogle Scholar
  51. 51.
    Bertoglio LJ, Carobrez AP. Anxiolytic effects of ethanol and phenobarbital are abolished in test-experienced rats submitted to the elevated plus maze. Pharmacol Biochem Behav. 2002;73:963–9.CrossRefGoogle Scholar
  52. 52.
    Tatem KS, et al. Behavioral and locomotor measurements using an open field activity monitoring system for skeletal muscle diseases. J Vis Exp. 2014;(91):51785.Google Scholar
  53. 53.
    Cryan JF, Valentino RJ, Lucki I. Assessing substrates underlying the behavioral effects of antidepressants using the modified rat forced swimming test. Neurosci Biobehav Rev. 2005;29:547–69.CrossRefGoogle Scholar
  54. 54.
    Adhikari A, et al. Basomedial amygdala mediates top-down control of anxiety and fear. Nature. 2015;527:179–85.CrossRefGoogle Scholar
  55. 55.
    Uylings HB, Groenewegen HJ, Kolb B. Do rats have a prefrontal cortex? Behav Brain Res. 2003;146:3–17.CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Prativa Sherchan
    • 1
  • Devin W. McBride
    • 1
  • Lei Huang
    • 2
  • Cesar Reis
    • 1
  • Onat Akyol
    • 1
  • Yuechun Wang
    • 1
  • Cherine Kim
    • 1
  • Ishan Solaroglu
    • 1
    • 3
  • Jiping Tang
    • 1
  • John H. Zhang
    • 1
    • 2
    • 4
    Email author
  1. 1.Department of Physiology and PharmacologyLoma Linda University School of MedicineLoma LindaUSA
  2. 2.Department of AnesthesiologyLoma Linda University School of MedicineLoma LindaUSA
  3. 3.Department of NeurosurgeryKoç University, School of MedicineIstanbulTurkey
  4. 4.Department of NeurosurgeryLoma Linda University School of MedicineLoma LindaUSA

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