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Hemodynamic challenges in traumatic subarachnoid hemorrhage complicated by cerebral vasospasm
American Journal of Emergency Medicine xxx (2016) xxx–xxx
Contents lists available at ScienceDirect
American Journal of Emergency Medicine journal homepage: www.elsevier.com/locate/ajem
Correspondence
Hemodynamic challenges in traumatic subarachnoid hemorrhage complicated by cerebral vasospasm To the Editor We have read with great interest the recent review by Varvarousi et al [1] on the role of levosimendan in the clinical setting of aneurysmal subarachnoid hemorrhage (SAH). Previous work by us [2] and others [3,4] proposed depressed cardiac output (CO), mainly attributed to catecholamine-mediated myocardial dysfunction, as a critical determinant of delayed cerebral ischemia (DCI) and poor neurologic outcome. In this respect, rapid hemodynamic augmentation, with either levosimendan [5] or other agents [6], has the potential to reverse cerebral ischemia and prevent further brain damage. However, analogous data are sparse in the setting of traumatic SAH. We present herein the clinical course of 2 patients with traumatic SAH and cardiovascular derangement and emphasize the potential influence of early CO optimization and levosimendan administration in preventing delayed neurologic complications. A 70-year-old man with traumatic SAH (Figure A) was intubated with Glasgow Coma Scale (GCS) of 8/15. At the time of admission in the intensive care unit, he was bradycardic (b 50 per minute), yet normotensive. Echocardiography [3] revealed slightly depressed CO (cardiac index [CI], 2.06 L/min/m 2). Transtemporal transcranial Doppler (TCD) was suggestive of vasospasm [7–10] in the distribution of the left middle cerebral artery (Table). Electroencephalograms were negative for seizure activity. The patient was treated appropriately [11,12]; cerebral perfusion pressure (CPP) greater than 70 mm Hg and intracerebral pressures less than 20 mm Hg were maintained through noradrenaline infusion (≤0.2 μg/kg per minute), mannitol administration, and/or cerebral spinal fluid drainage. Serial TCDs demonstrated a typical for traumatic SAH vasospasm course [11,12], with an early onset and duration of approximately 1 week. During this period, persistent bradycardia (≤52 per minute) was recorded; bradycardia apparently led to CO decline (CI ≤2.2 L/min/m2), which was asymptomatic, as mean blood pressure, CPP and blood lactate (b 1 mmol/L) maintained within normal limits. Follow-up brain computed tomography disclosed extensive ischemic lesions; interestingly, TCD studies were indicative of regional distribution of DCI (Figure B). The patient finally died due to sepsisassociated multiorgan failure. A 28-year-old woman was admitted in intensive care unit with severe clinical (GCS of 4/15) and neuroimaging features (hemorrhagic contusions, diffuse hemorrhagic pattern) of traumatic SAH (Figure C). In addition, she manifested clinically devastating cardiogenic shock, with hypotension (noradrenaline dose 1.45 μg/kg per minute), diuresis less than 30 mL/h, pulmonary edema, hypoxemia (PaO2, 74 mm Hg), metabolic acidosis (pH 7.18), and worsening lacticemia (blood lactate, 4.7 mmol/L). Echocardiography revealed underlying “neurogenic stress cardiomyopathy” [1,3] as the cause of cardiogenic shock (left ventricular ejection fraction, 20%; CI, 1.038 L/min/m 2), whereas TCD indicated
vasospasm in the anterior circulation (Table). Apart from conventional treatment to maintain adequate CPP and intracerebral pressure levels [11,12], levosimendan was administered to improve cardiac contractility (0.2 μg/kg per minute for 3 days; no bolus dose) [3]; this resulted in restoration of oxygenation (PaO2, 147 mm Hg; fraction of inspired oxygen, 0.45) and serum lactate levels (b 1.5 mmol/L) after 48 hours, and left ventricular systolic function (ejection fraction, N50%) and CO (CI, N4/min/m2) after 96 hours. Transcranial Doppler–evidenced vasospasm lasted for a week [11,12]. Interestingly, despite the dramatic initial cardiocerebral status, follow-up computed tomographies manifested rapid absorption of the contusion lesions and no posttraumatic cerebral ischemia (Figure D), whereas the patient showed gradual clinical improvement (discharge GCS of 15/15). Despite several differences from aneurysmal SAH, such as earlier onset and shorter vasospasm duration, traumatic SAH may also represent a challenging yet underestimated and potentially dismal clinical entity [11,12]. The typical strategy in aneurysmal SAH of hemodynamic augmentation, by inducing hypertension and hypervolemiahemodilution (“triple H” therapy), may be harmful in traumatic SAH, by worsening brain and pulmonary edema and increasing the risk of hemorrhage [11]. Furthermore, poorer response to calcium-channel blockers has been reported in traumatic compared to aneurysmal SAH [11]. These limitations highlight the need for reconsidering the optimal hemodynamic management in traumatic SAH. Our cases may suggest that both components of depressed CO, decreased heart rate and cardiac contractility, may adversely affect cerebral perfusion and, when unopposed, may lead to DCI. In our case 1, TCD-detected vasospasm was indicative of cerebral regions at risk for necrosis. Despite the established management [11,12], the possible impact of the otherwise asymptomatic bradycardia and depressed CO on cerebral perfusion might have been underestimated. Case 2 also presented TCD findings compatible with cerebral hypoperfusion. In this specific patient, though, the beneficial systemic and local effects of levosimendan [1] may have compensated for vasospasm-induced problematic cerebral blood flow. The clinical impact of acute cardiovascular derangement in traumatic SAH remains largely unknown [11,12]. Certainly, case reports may advance scientific knowledge in such rare clinical entities. Whether CO augmentation and levosimendan administration may be of clinical benefit in the subset of patients with pure bradycardia and ensuing organ hypoperfusion, especially in the asymptomatic ones, still remains a question. In our experience, even subclinical CO reductions should be meticulously assessed and early optimized, especially in the setting of confirmed vasospasm. In traumatic SAH–related cardiogenic shock, though, levosimendan may be a promising agent in preventing delayed cerebral damage, in line with aneurysmal SAH [1]. Nevertheless, the possible role of early hemodynamic optimization and levosimendan
0735-6757/© 2016 Elsevier Inc. All rights reserved.
Please cite this article as: Papanikolaou J, et al, Hemodynamic challenges in traumatic subarachnoid hemorrhage complicated by cerebral vasospasm, Am J Emerg Med (2016), http://dx.doi.org/10.1016/j.ajem.2016.01.041
2
Correspondence / American Journal of Emergency Medicine xxx (2016) xxx–xxx
Figure. Neuroimaging evolution in our two patients with traumatic subarachnoid hemorrhage.
Table Serial TCD examinations in our 2 head trauma patients Examined vessel
Case 1
Case 2
Right
ACA1 MCA PCA1 ex ICA
Left
ACA1 MCA PCA1 ex ICA
Right
ACA1 MCA PCA1 ex ICA
Left
ACA1 MCA PCA1 ex ICA
TCD criteria
Serial TCD velocities, cm/s
for vasospasm [7–10]
Days 1-2
Days 3-4
Days 4-7
Day 10
112 104 67 44 2.36 117 144 78 32 4.5 1.38 78 120 79 72 1.67 77 163 48 63 2.59 1.36
91 79 73 38 2.08 94 121 46 24 5.04 1.53 75 134 82 58 2.31 103 158 87 46 3.43 1.18
82 85 65 44 1.93 91 128 75 35 3.65 1.51 94 82 67 47 1.74 105 122 75 45 2.71 1.49
67 94 66 52 1.8 77 88 61 33 2.67 0.94 84 82 56 48 1.71 88 109 77 47 2.32 1.33
Mean velocity N90 cm/s [10] Mean velocity N120 cm/s [7] Mean velocity N80 cm/s [10] LR N3 [8] Mean velocity N90 cm/s [10] Mean velocity N120 cm/s [7] Mean velocity N80 cm/s [10] LR N3 [8] I/C mBFV N1.5 [9] Mean velocity N90 cm/s [10] Mean velocity N120 cm/s [7] Mean velocity N80 cm/s [10] LR N3 [8] Mean velocity N90 cm/s [10] Mean velocity N120 cm/s [7] Mean velocity N80 cm/s [10] LR N3 [8] I/C mBFV N1.5 [9]
Boldface values indicate vasospasm, according to established criteria. Abbreviations: ACA1, anterior cerebral artery, segment 1; MCA, middle cerebral artery; PCA1, posterior cerebral artery, segment 1; ex ICA, extracranial part of internal carotid artery; LR (Lindegaard ratio), the ratio of flow velocity in the MCA to flow velocity in ex ICA; I/C mBFV, ipsilateral (highest value) to contralateral middle cerebral artery blood flow velocity ratio.
Please cite this article as: Papanikolaou J, et al, Hemodynamic challenges in traumatic subarachnoid hemorrhage complicated by cerebral vasospasm, Am J Emerg Med (2016), http://dx.doi.org/10.1016/j.ajem.2016.01.041
Correspondence / American Journal of Emergency Medicine xxx (2016) xxx–xxx
infusion in the setting of traumatic SAH warrants further investigation in the future. Conflict of interest The authors report no relationship that could be construed as a conflict of interest. John Papanikolaou PhD⁎ Konstantinos Spathoulas MD Demosthenes Makris PhD Triantafillia Koukoubani MD Epaminondas Zakynthinos PhD Department of Critical Care, School of Medicine, University of Thessaly University Hospital of Larissa, Thessaly, Greece ⁎ Corresponding author. Biopolis, 41110 Larissa, Greece Tel.: +30 241 068 2960; fax: +30 241 067 0838 E-mail address: [email protected] http://dx.doi.org/10.1016/j.ajem.2016.01.041 References [1] Varvarousi G, Xanthos T, Sarafidou P, Katsioula E, Georgiadou M, Eforakopoulou M, et al. Role of levosimendan in the management of subarachnoid hemorrhage. Am J Emerg Med 2015 [in press].
3
[2] Papanikolaou J, Makris D, Karakitsos D, Saranteas T, Karabinis A, Kostopanagiotou G, et al. Cardiac and central vascular functional alterations in the acute phase of aneurysmal subarachnoid hemorrhage. Crit Care Med 2012;40:223–32. [3] van der Bilt I, Hasan D, van den Brink R, Cramer MJ, van der Jagt M, van Kooten F, et al. Cardiac dysfunction after aneurismal subarachnoid hemorrhage: relationship with outcome. Neurology 2014;82(4):351–8. [4] Yoneda H, Nakamura T, Shirao S, Tanaka N, Ishihara H, Suehiro E, et al. Multicenter prospective cohort study on volume management after subarachnoid hemorrhage: hemodynamic changes according to severity of subarachnoid hemorrhage and cerebral vasospasm. Stroke 2013;44(8):2155–61. [5] Papanikolaou J, Tsolaki V, Makris D, Zakynthinos E. Early levosimendan administration may improve outcome in patients with subarachnoid hemorrhage complicated by acute heart failure. Int J Cardiol 2014;176:1435–7. [6] Joseph M, Ziadi S, Nates J, Dannenbaum M, Malkoff M. Increases in cardiac output can reverse flow deficits from vasospasm independent of blood pressure: a study using xenon computed tomographic measurement of cerebral blood flow. Neurosurgery 2003;53(5):1044–51. [7] Aaslid R, Huber P, Nornes H. Evaluation of cerebrovascular spasm with transcranial Doppler ultrasound. J Neurosurg 1984;60:37–41. [8] Lindegaard KF, Nornes H, Bakke SJ, Sorteberg W, Nakstad P. Cerebral vasospasm diagnosis by means of angiography and blood velocity measurements. Acta Neurochir 1989;100:12–24. [9] Nakae R, Yokota H, Yoshida D, Teramoto A. Transcranial Doppler ultrasonography for diagnosis of cerebral vasospasm after aneurysmal subarachnoid hemorrhage: mean blood flow velocity ratio of the ipsilateral and contralateral middle cerebral arteries. Neurosurgery 2011;69(4):876–83. [10] Bathala L, Mehndiratta MM, Sharma VK. Transcranial doppler: technique and common findings (part 1). Ann Indian Acad Neurol 2013;16(2):174–9. [11] Izzy S, Muehlschlegel S. Cerebral vasospasm after aneurysmal subarachnoid hemorrhage and traumatic brain injury. Curr Treat Options Neurol 2014; 16(1):278. [12] Oertel M, Boscardin WJ, Obrist WD, Glenn TC, McArthur DL, Gravori T, et al. Posttraumatic vasospasm: the epidemiology, severity and time course of an underestimated phenomenon: a prospective study performed in 299 patients. J Neurosurg 2005; 103:812–24.
Please cite this article as: Papanikolaou J, et al, Hemodynamic challenges in traumatic subarachnoid hemorrhage complicated by cerebral vasospasm, Am J Emerg Med (2016), http://dx.doi.org/10.1016/j.ajem.2016.01.041
Contents lists available at ScienceDirect
American Journal of Emergency Medicine journal homepage: www.elsevier.com/locate/ajem
Correspondence
Hemodynamic challenges in traumatic subarachnoid hemorrhage complicated by cerebral vasospasm To the Editor We have read with great interest the recent review by Varvarousi et al [1] on the role of levosimendan in the clinical setting of aneurysmal subarachnoid hemorrhage (SAH). Previous work by us [2] and others [3,4] proposed depressed cardiac output (CO), mainly attributed to catecholamine-mediated myocardial dysfunction, as a critical determinant of delayed cerebral ischemia (DCI) and poor neurologic outcome. In this respect, rapid hemodynamic augmentation, with either levosimendan [5] or other agents [6], has the potential to reverse cerebral ischemia and prevent further brain damage. However, analogous data are sparse in the setting of traumatic SAH. We present herein the clinical course of 2 patients with traumatic SAH and cardiovascular derangement and emphasize the potential influence of early CO optimization and levosimendan administration in preventing delayed neurologic complications. A 70-year-old man with traumatic SAH (Figure A) was intubated with Glasgow Coma Scale (GCS) of 8/15. At the time of admission in the intensive care unit, he was bradycardic (b 50 per minute), yet normotensive. Echocardiography [3] revealed slightly depressed CO (cardiac index [CI], 2.06 L/min/m 2). Transtemporal transcranial Doppler (TCD) was suggestive of vasospasm [7–10] in the distribution of the left middle cerebral artery (Table). Electroencephalograms were negative for seizure activity. The patient was treated appropriately [11,12]; cerebral perfusion pressure (CPP) greater than 70 mm Hg and intracerebral pressures less than 20 mm Hg were maintained through noradrenaline infusion (≤0.2 μg/kg per minute), mannitol administration, and/or cerebral spinal fluid drainage. Serial TCDs demonstrated a typical for traumatic SAH vasospasm course [11,12], with an early onset and duration of approximately 1 week. During this period, persistent bradycardia (≤52 per minute) was recorded; bradycardia apparently led to CO decline (CI ≤2.2 L/min/m2), which was asymptomatic, as mean blood pressure, CPP and blood lactate (b 1 mmol/L) maintained within normal limits. Follow-up brain computed tomography disclosed extensive ischemic lesions; interestingly, TCD studies were indicative of regional distribution of DCI (Figure B). The patient finally died due to sepsisassociated multiorgan failure. A 28-year-old woman was admitted in intensive care unit with severe clinical (GCS of 4/15) and neuroimaging features (hemorrhagic contusions, diffuse hemorrhagic pattern) of traumatic SAH (Figure C). In addition, she manifested clinically devastating cardiogenic shock, with hypotension (noradrenaline dose 1.45 μg/kg per minute), diuresis less than 30 mL/h, pulmonary edema, hypoxemia (PaO2, 74 mm Hg), metabolic acidosis (pH 7.18), and worsening lacticemia (blood lactate, 4.7 mmol/L). Echocardiography revealed underlying “neurogenic stress cardiomyopathy” [1,3] as the cause of cardiogenic shock (left ventricular ejection fraction, 20%; CI, 1.038 L/min/m 2), whereas TCD indicated
vasospasm in the anterior circulation (Table). Apart from conventional treatment to maintain adequate CPP and intracerebral pressure levels [11,12], levosimendan was administered to improve cardiac contractility (0.2 μg/kg per minute for 3 days; no bolus dose) [3]; this resulted in restoration of oxygenation (PaO2, 147 mm Hg; fraction of inspired oxygen, 0.45) and serum lactate levels (b 1.5 mmol/L) after 48 hours, and left ventricular systolic function (ejection fraction, N50%) and CO (CI, N4/min/m2) after 96 hours. Transcranial Doppler–evidenced vasospasm lasted for a week [11,12]. Interestingly, despite the dramatic initial cardiocerebral status, follow-up computed tomographies manifested rapid absorption of the contusion lesions and no posttraumatic cerebral ischemia (Figure D), whereas the patient showed gradual clinical improvement (discharge GCS of 15/15). Despite several differences from aneurysmal SAH, such as earlier onset and shorter vasospasm duration, traumatic SAH may also represent a challenging yet underestimated and potentially dismal clinical entity [11,12]. The typical strategy in aneurysmal SAH of hemodynamic augmentation, by inducing hypertension and hypervolemiahemodilution (“triple H” therapy), may be harmful in traumatic SAH, by worsening brain and pulmonary edema and increasing the risk of hemorrhage [11]. Furthermore, poorer response to calcium-channel blockers has been reported in traumatic compared to aneurysmal SAH [11]. These limitations highlight the need for reconsidering the optimal hemodynamic management in traumatic SAH. Our cases may suggest that both components of depressed CO, decreased heart rate and cardiac contractility, may adversely affect cerebral perfusion and, when unopposed, may lead to DCI. In our case 1, TCD-detected vasospasm was indicative of cerebral regions at risk for necrosis. Despite the established management [11,12], the possible impact of the otherwise asymptomatic bradycardia and depressed CO on cerebral perfusion might have been underestimated. Case 2 also presented TCD findings compatible with cerebral hypoperfusion. In this specific patient, though, the beneficial systemic and local effects of levosimendan [1] may have compensated for vasospasm-induced problematic cerebral blood flow. The clinical impact of acute cardiovascular derangement in traumatic SAH remains largely unknown [11,12]. Certainly, case reports may advance scientific knowledge in such rare clinical entities. Whether CO augmentation and levosimendan administration may be of clinical benefit in the subset of patients with pure bradycardia and ensuing organ hypoperfusion, especially in the asymptomatic ones, still remains a question. In our experience, even subclinical CO reductions should be meticulously assessed and early optimized, especially in the setting of confirmed vasospasm. In traumatic SAH–related cardiogenic shock, though, levosimendan may be a promising agent in preventing delayed cerebral damage, in line with aneurysmal SAH [1]. Nevertheless, the possible role of early hemodynamic optimization and levosimendan
0735-6757/© 2016 Elsevier Inc. All rights reserved.
Please cite this article as: Papanikolaou J, et al, Hemodynamic challenges in traumatic subarachnoid hemorrhage complicated by cerebral vasospasm, Am J Emerg Med (2016), http://dx.doi.org/10.1016/j.ajem.2016.01.041
2
Correspondence / American Journal of Emergency Medicine xxx (2016) xxx–xxx
Figure. Neuroimaging evolution in our two patients with traumatic subarachnoid hemorrhage.
Table Serial TCD examinations in our 2 head trauma patients Examined vessel
Case 1
Case 2
Right
ACA1 MCA PCA1 ex ICA
Left
ACA1 MCA PCA1 ex ICA
Right
ACA1 MCA PCA1 ex ICA
Left
ACA1 MCA PCA1 ex ICA
TCD criteria
Serial TCD velocities, cm/s
for vasospasm [7–10]
Days 1-2
Days 3-4
Days 4-7
Day 10
112 104 67 44 2.36 117 144 78 32 4.5 1.38 78 120 79 72 1.67 77 163 48 63 2.59 1.36
91 79 73 38 2.08 94 121 46 24 5.04 1.53 75 134 82 58 2.31 103 158 87 46 3.43 1.18
82 85 65 44 1.93 91 128 75 35 3.65 1.51 94 82 67 47 1.74 105 122 75 45 2.71 1.49
67 94 66 52 1.8 77 88 61 33 2.67 0.94 84 82 56 48 1.71 88 109 77 47 2.32 1.33
Mean velocity N90 cm/s [10] Mean velocity N120 cm/s [7] Mean velocity N80 cm/s [10] LR N3 [8] Mean velocity N90 cm/s [10] Mean velocity N120 cm/s [7] Mean velocity N80 cm/s [10] LR N3 [8] I/C mBFV N1.5 [9] Mean velocity N90 cm/s [10] Mean velocity N120 cm/s [7] Mean velocity N80 cm/s [10] LR N3 [8] Mean velocity N90 cm/s [10] Mean velocity N120 cm/s [7] Mean velocity N80 cm/s [10] LR N3 [8] I/C mBFV N1.5 [9]
Boldface values indicate vasospasm, according to established criteria. Abbreviations: ACA1, anterior cerebral artery, segment 1; MCA, middle cerebral artery; PCA1, posterior cerebral artery, segment 1; ex ICA, extracranial part of internal carotid artery; LR (Lindegaard ratio), the ratio of flow velocity in the MCA to flow velocity in ex ICA; I/C mBFV, ipsilateral (highest value) to contralateral middle cerebral artery blood flow velocity ratio.
Please cite this article as: Papanikolaou J, et al, Hemodynamic challenges in traumatic subarachnoid hemorrhage complicated by cerebral vasospasm, Am J Emerg Med (2016), http://dx.doi.org/10.1016/j.ajem.2016.01.041
Correspondence / American Journal of Emergency Medicine xxx (2016) xxx–xxx
infusion in the setting of traumatic SAH warrants further investigation in the future. Conflict of interest The authors report no relationship that could be construed as a conflict of interest. John Papanikolaou PhD⁎ Konstantinos Spathoulas MD Demosthenes Makris PhD Triantafillia Koukoubani MD Epaminondas Zakynthinos PhD Department of Critical Care, School of Medicine, University of Thessaly University Hospital of Larissa, Thessaly, Greece ⁎ Corresponding author. Biopolis, 41110 Larissa, Greece Tel.: +30 241 068 2960; fax: +30 241 067 0838 E-mail address: [email protected] http://dx.doi.org/10.1016/j.ajem.2016.01.041 References [1] Varvarousi G, Xanthos T, Sarafidou P, Katsioula E, Georgiadou M, Eforakopoulou M, et al. Role of levosimendan in the management of subarachnoid hemorrhage. Am J Emerg Med 2015 [in press].
3
[2] Papanikolaou J, Makris D, Karakitsos D, Saranteas T, Karabinis A, Kostopanagiotou G, et al. Cardiac and central vascular functional alterations in the acute phase of aneurysmal subarachnoid hemorrhage. Crit Care Med 2012;40:223–32. [3] van der Bilt I, Hasan D, van den Brink R, Cramer MJ, van der Jagt M, van Kooten F, et al. Cardiac dysfunction after aneurismal subarachnoid hemorrhage: relationship with outcome. Neurology 2014;82(4):351–8. [4] Yoneda H, Nakamura T, Shirao S, Tanaka N, Ishihara H, Suehiro E, et al. Multicenter prospective cohort study on volume management after subarachnoid hemorrhage: hemodynamic changes according to severity of subarachnoid hemorrhage and cerebral vasospasm. Stroke 2013;44(8):2155–61. [5] Papanikolaou J, Tsolaki V, Makris D, Zakynthinos E. Early levosimendan administration may improve outcome in patients with subarachnoid hemorrhage complicated by acute heart failure. Int J Cardiol 2014;176:1435–7. [6] Joseph M, Ziadi S, Nates J, Dannenbaum M, Malkoff M. Increases in cardiac output can reverse flow deficits from vasospasm independent of blood pressure: a study using xenon computed tomographic measurement of cerebral blood flow. Neurosurgery 2003;53(5):1044–51. [7] Aaslid R, Huber P, Nornes H. Evaluation of cerebrovascular spasm with transcranial Doppler ultrasound. J Neurosurg 1984;60:37–41. [8] Lindegaard KF, Nornes H, Bakke SJ, Sorteberg W, Nakstad P. Cerebral vasospasm diagnosis by means of angiography and blood velocity measurements. Acta Neurochir 1989;100:12–24. [9] Nakae R, Yokota H, Yoshida D, Teramoto A. Transcranial Doppler ultrasonography for diagnosis of cerebral vasospasm after aneurysmal subarachnoid hemorrhage: mean blood flow velocity ratio of the ipsilateral and contralateral middle cerebral arteries. Neurosurgery 2011;69(4):876–83. [10] Bathala L, Mehndiratta MM, Sharma VK. Transcranial doppler: technique and common findings (part 1). Ann Indian Acad Neurol 2013;16(2):174–9. [11] Izzy S, Muehlschlegel S. Cerebral vasospasm after aneurysmal subarachnoid hemorrhage and traumatic brain injury. Curr Treat Options Neurol 2014; 16(1):278. [12] Oertel M, Boscardin WJ, Obrist WD, Glenn TC, McArthur DL, Gravori T, et al. Posttraumatic vasospasm: the epidemiology, severity and time course of an underestimated phenomenon: a prospective study performed in 299 patients. J Neurosurg 2005; 103:812–24.
Please cite this article as: Papanikolaou J, et al, Hemodynamic challenges in traumatic subarachnoid hemorrhage complicated by cerebral vasospasm, Am J Emerg Med (2016), http://dx.doi.org/10.1016/j.ajem.2016.01.041