Cerebrovascular resistance in patients with severe combined traumatic brain injury

Trofimov A.O.; Kalent’ev G.V.; Agarkova D.I.

doi:https://doi.org/10.17116/neiro201579528-33

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Abstract:

Cerebrovascular resistance is an important parameter of the microcirculation. The main objective of cerebrovascular resistance is to maintain the constancy of cerebral blood flow and protect downstream vessels when changing perfusion pressure. The purpose of the study was to assess cerebrovascular resistance (CVR) in patients with severe combined traumatic brain injury (CTBI) with and without intracranial hematomas (IHs). Material and methods. We analyzed treatment outcomes in 70 patients with severe CTBI (42 males and 28 females). The mean age was 35.5±14.8 years (min 15 years; max 73 years). All patients were divided into 2 groups, depending on the presence of intracranial hemorrhage. The first group included 34 patients without IH, and the second group included 36 patients with epidural (6), subdural (26), and multiple (4) hematomas. The GCS score was 10.4±2.6 in the first group and 10.6±2.8 in the second group. The ISS severity injury score was 32±8 in the first group and 31±11 in the second group. All patients were operated on within the first 3 days, with 30 (83.3%) patients being operated on during the first day. Perfusion computed tomography (PCT) of the brain was performed within 1—14 days after TBI in the first group and within 2—8 days after surgical evacuation of hematoma in the second group. After PCT, the mean arterial pressure was measured, and the blood flow rate in the middle cerebral artery was determined using transcranial dopplerography. Cerebrovascular resistance was calculated using the formula modificated by P. Scheinberg. Comparisons between the groups were performed using the Student t-test and χ2 criterion. Results. The mean CVR values in each group (both with and without hematomas) were statistically significantly higher than the mean normal value of this parameter. Intergroup comparison of CVR values demonstrated a statistically significant increase in the CVR level in group 2 on the side of removed hematoma compared to group 1 (p=0.037). CVR in the perifocal zone of removed hematoma remained significantly higher compared to the symmetrical zone of the contralateral hemisphere (p=0.0009). Conclusions. Cerebrovascular resistance in patients with combined traumatic brain injury is significantly increased compared to the normal value. Cerebrovascular resistance in the perifocal zone after evacuation of hematoma in patients with multiple injury remains significantly increased compared to the symmetrical zone in the contralateral hemisphere.

Keywords:

combined traumatic brain injury

intracranial hematoma

cerebrovascular resistance

critical closing pressure

Authors:

Trofimov A.O.

The N.A. Semashko Nizhny Novgorod Regional Hospital

Kalent’ev G.V.

The N.A. Semashko Nizhny Novgorod Regional Hospital

Agarkova D.I.

The N.A. Semashko Nizhny Novgorod Regional Hospital

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References:

Oshorov A, Savin I, Goryachev A, Popugaev K, Polupan A, Sychev A, Zakharova N, Gavrilov A, Danilov G, Potapov A. Plateau-waves of the intracranial pressure in patients with severe brain injury. Anesteziologiya i reanimotologiya. 2013;4:44-50. (In Russ.).
Furuya Y, Hlatky R, Valadka A. Comparison of cerebral blood flow in computed tomographic hypodense areas of the brain in head-injured patients. Neurosurgery. 2003;52:340-346. doi:10.1227/01.neu.0000043931.83041.aa
Potapov A, Zakharova N, Pronin I, Kornienko V, Gavriolv A, Kravchuk A, Oshorov A, Sychev A, Zaitsev O, Fadeev L, Takush S. Predictive value of intracranial and cerebral perfusion pressure monitoring, values of regional blood flow in diffuse and focal brain injuries. Vopr Neirokhir. 2011;75:3:3-18. (In Russ.).
Etminan N, Hänggi D. Perfusion CT imaging as a radiological surrogate for early brain injury — Summary of current data on aneurysmal subarachnoid hemorrhage (Part А). Paper presented at: «Brain Edema 2014» The 16th International Conference on Brain Edema and Cellular Injury. Huntington Beach (California) 2014 September 27-30. Available at: http://brainedema2014.com/program_outline.html
Hattingen E, Blasel S, Dumesnil R. MR angiography in patients with subarachnoid hemorrhage: adequate to evaluate vasospasm-induced vascular narrowing? Neurosurgical Review. 2010;33:4:431-439. doi:10.1007/s10143-010-0267-4
Ursino M, Lodi C. A simple mathematical model of the interaction between intracranial pressure and cerebral hemodynamics. Journal of Applied Physiology. 1997;82:1256-1269. doi:10.1007/bf02368459
Westermaier T, Pham M, Stetter C. Value of transcranial Doppler, perfusion-CT and neurological evaluation to forecast secondary ischemia after aneurysmal SAH. Neurocritical Care. 2014 Jun;20(3):406-412. doi: 10.1007/s12028-013-9896-0
Aries M. Cerebral hemodynamics in stroke and traumatic brain injury: the interplay between blood pressure, cerebral perfusion, body position and autoregulation. The interplay between blood pressure, cerebral perfusion, body position and autoregulation. [dissertation]. Gröningen. The Netherlands. 2012.
Avezaat CJ, Eijndhoven JH. Cerebrospinal fluid pulse pressure and craniospatial dynamics. A theoretical, clinical and experimental study. [dissertation]. Erasmus University, Rotterdam, The Netherlands. 1984.
Rhee C, Kibler K, Easley B. The Ontogeny of Cerebral Blood Flow Autoregulation and Critical Closing Pressure. Paper presented at: The 15th International Conference on Intracranial Pressure and Brain Monitoring. Singapore 2013 November 6–10;66. Available at: http://www.icp2013.com.sg/
Heldt T, Noraky J, Verghese G. Noninvasive Intracranial Pressure Determination in Patients with Subarachnoid Hemorrhage. Paper presented at: The 15th International Conference on Intracranial Pressure and Brain Monitoring. Singapore. 2013 November 6—10;40. Available at: http://www.icp2013.com.sg/
Kapinos G, Sadoughi A, Narayan R. Intracranial Pressure Treatment Tailored to Transcranial Doppler-Derived Compliance and Perfusion. Paper presented at: The 15th International Conference on Intracranial Pressure and Brain Monitoring. Singapore. 2013 November 6—10;44. Available at: http://www.icp2013.com.sg/
Dewey R, Pierer H, Hunt W. Experimental cerebral hemodynamics-vasomotor tone, critical closing pressure, and vascular bed resistance. Journal of Neurosurgery. 1974;41. doi:10.3171/jns.1974.41.5.0597
Kasprowicz M. Badania hemodynamiki mózgowej na podstawie analizy pulsacji ciśnienia wewnᶏtrzczaszkowego, ciśnienia tᶒtniczego i przepływu krwi mózgowej. [dissertation]. Oficyna Wydawnicza Politechniki Wrocławskiej. Wrocław. 2012. (In Polish.).
Kasprowicz M., Diedler J., Reinhard M. Time constant of the cerebral arterial bed in normal subjects. Ultrasound in Medicine & Biology. 2012;38:1129-1137. doi:10.1016/j.ultrasmedbio.2012.02.014
Laan ter Mark. Neuromodulation of cerebral blood flow. [dissertation]. Gröningen (The Netherlands). 2014.
Narayanan N, Leffler C, Czosnyka M. Assessment of cerebrovascular resistance with model of cerebrovascular pressure transmission. Acta Neurochirurgica Supplement. 2008;102:37-41. doi:10.1016/j.medengphy.2008.07.002
Sharples PM, Matthews DSF, Eyre JA. Cerebral blood flow and metabolism in children with severe head injuries. Part 2: cerebrovascular resistance and its determinants. Journal of Neurology Neurosurgery and Psychiatry. 1995;58:153-159. doi:10.1136/jnnp.58.2.153
Daley M, Narayanan N, Leffler C. Model-derived assessment of cerebrovascular resistance and cerebral blood flow following traumatic brain injury. Experimental Biology and Medecine (Maywood). 2010 Apr;235(4):539-545. doi: 10.1258/ebm.2010.009253
Smirl J, Tzeng Y, Monteleone B. Influence of cerebrovascular resistance on the dynamic relationship between blood pressure and cerebral blood flow in humans. Journal of Applied Physiology. 2014;116:1614-1622. doi:10.1152/japplphysiol.01266.2013
Bragin D, Bush R, Muller W. High intracranial pressure effects on cerebral cortical microvascular flow in rats. Journal of Neurotrauma. 2011;28:775-785. doi: 10.1089/neu.2010.1692
Muizelaar JP, Marmarou A, DeSalles AAF. Cerebral blood flow and metabolism in severely head injured children. Part 1: relationship with GCS score, outcome, ICP and PVI. Journal of Neurosurgery. 1989;71:63-71. doi:10.3171/jns.1989.71.1.0063
Pluta RM. Delayed cerebral vasospasm and nitric oxide: review, new hypothesis, and proposed treatment. Pharmacology and Therapy. 2005;105:23-56. doi:10.1016/j.pharmthera.2004.10.002
Siemkowicz E. Cerebrovascular resistance in ischemia. Pflügers Archiv European Journal of Physiology. 1980;388:3:243-247. doi:10.1007/bf00658489
Potapov A, Zakharova N, Kornienko V, Pronin I, Alexandrova E, Zaitsev O, Likhterman L, Gavrilov A, Danilov G, Oshorov A, Sychev A, Polupan A. Neuroanatomic basis of traumatic coma: clinical and magnetic-resonance correlates. Vopr Neirokhir. 2014;78:4-14.
Czosnyka M, Smielewski P, Kirkpatrick P. Continuous assessment of the cerebral vasomotor reactivity in head injury. Neurosurgery. 1997;41(1):11-17. doi:10.1097/00006123-199707000-00005
Scheinberg P, Stead E. The cerebral blood flow in male subjects as measured by the nitrous oxide technique. Normal values for blood flow, oxygen utilisation, glucose utilisation, and peripheral resistance, with observations on the effect of tilting and anxiety. Journal of Clinical Investigation. 1949;28:1163-1171. doi:10.1172/jci102150
Lassen NA. Autoregulation of cerebral blood flow. Circulation Reseach. 1964;15: Supplement: 201-204.
Marmarou A. A review of progress in understanding the pathophysiology and treatment of brain edema. Neurosurgical Focus. 2007; 15.22(5): E1. doi:10.3171/foc.2007.22.5.2
Cernak I, Vink R, Zapple D. The pathobiology of moderate diffuse traumatic brain injury as identified using a new experimental model of injury in rats. Neurobiological Disease. 2004; 17: 29-43. doi:10.1016/j.nbd.2004.05.011
Rey F, Li X, Carretero O. Perivascular superoxide anion contributes to impairment of endothelium-dependent relaxation: role of gp91(phox). Circulation. 2002;106(19):2497-2502. doi:10.1161/01.cir.0000038108.71560.70
Østergaard, Engedal T, Aamand R, Mikkelsen R, Iversen N, Anzabi M. Capillary transit time heterogeneity and flow-metabolism coupling after traumatic brain injury. Journal of Cerebral Blood Flow & Metabolism. 2014;34:1585-1598. doi:10.1038/jcbfm.2014.131
Bullock R, Maxwell W, Graham D. Glial swelling following human cerebral contusion: an ultrastructural study. Journal of Neurology Neurosurgery Psychiatry. 1991;54:427-434. doi:10.1136/jnnp.54.5.427
Armulik A, Genove G, Mae M. Pericytes regulate the blood-brain barrier. Nature. 2010;468:557-561. doi: 10.1038/nature09522
Dore-Duffy P, Wang S, Mehedi A. Pericyte-mediated vasoconstriction underlies TBI-induced hypoperfusion. Neurological Research. 2011;33:176-186. doi:10.1179/016164111x12881719352372
Hall C, Reynell C, Gesslein B. Capillary pericytes regulate cerebral blood flow in health and disease. Nature. 2014;508:55-60. doi:10.1038/nature13165
Kreipke C, Schafer PC, Rossi NF. Differential effects of endothelin receptor A and B antagonism on cerebral hypoperfusion following traumatic brain injury. Neurological Research. 2010;32:209-214. doi:10.1179/174313209x414515
Yemisci M, Gursoy-Ozdemir Y, Vural A. Pericyte contraction induced by oxidative-nitrative stress impairs capillary reflow despite successful opening of an occluded cerebral artery. Natural Medicine. 2009;15:1031-1037. doi:10.1038/nm.2022
Vollmar B, Westermann S, Menger M. Microvascular response to compartment syndrome-like external pressure elevation: an in vivo fluorescence microscopic study in the hamster striated muscle. The Journal of Trauma: Injury Infection and Critical Care. 1999;46:91-96. doi:10.1097/00005373-199901000-00015
Cragin D, Bush R, Nemoto E. Effect of cerebral perfusion pressure on cerebral cortical microvascular shunting at high intracranial pressure in rats. Stroke. 2013;44:177-181. doi:10.1161/STROKEAHA.112.668293