Abstract
Background
Transcranial Doppler (TCD) is widely used to detect and follow up cerebral vasospasm after subarachnoid hemorrhage (SAH). Therapeutic hypothermia might influence blood flow velocities assessed by TCD. The aim of the study was to evaluate the effect of hypothermia on Doppler blood flow velocity after SAH.
Methods
In 20 patients treated with hypothermia (33°) due to refractory intracranial hypertension or delayed cerebral ischemia (DCI), mean flow velocity of the middle cerebral artery (MFVMCA) was assessed by TCD. Thirteen patients were treated with combined hypothermia and barbiturate coma and seven with hypothermia alone. MFVMCA was obtained within 24 h before and after induction of hypothermia as well as before and after rewarming.
Results
Hypothermia was induced on average 5 days after SAH (range 1–12) and maintained for 144 h (range 29–270). After hypothermia induction, MFVMCA decreased from 113.7 ± 49.0 to 93.8 ± 44.7 cm/s (p = 0.001). The decrease was independent of SAH-related complications and barbiturate coma. MFVMCA further decreased by 28.2 cm/s between early and late hypothermia (p < 0.001). This second decrease was observed in patients with DCI (p < 0.001), but not in patients with intracranial hypertension (p = 0.715). Compared to late hypothermia, MFVMCA remained unchanged after rewarming (65.6 ± 32.1 vs 70.3 ± 36.8 cm/s; p = 0.219). However, patients treated with hypothermia alone showed an increase in MFVMCA after rewarming (p = 0.016).
Conclusion
Therapeutic hypothermia after SAH decreases Doppler blood flow velocity in both intracranial hypertension and DCI cases. The results can be the effect of hypothermia-related mechanisms or resolving cerebral vasospasm during prolonged hypothermia.
This is a preview of subscription content, access via your institution.


References
Heuer GG, Smith MJ, Elliott JP, Winn HR, LeRoux PD. Relationship between intracranial pressure and other clinical variables in patients with aneurysmal subarachnoid hemorrhage. J Neurosurg. 2004;101:408–16.
Vergouwen MD, Ilodigwe D, Macdonald RL. Cerebral infarction after subarachnoid hemorrhage contributes to poor outcome by vasospasm-dependent and -independent effects. Stroke. 2011;42:924–9.
Thome C, Schubert G, Piepgras A, Elste V, Schilling L, Schmiedek P. Hypothermia reduces acute vasospasm following SAH in rats. Acta Neurochir Suppl. 2001;77:255–8.
Schubert GA, Poli S, Mendelowitsch A, Schilling L, Thome C. Hypothermia reduces early hypoperfusion and metabolic alterations during the acute phase of massive subarachnoid hemorrhage: a laser-Doppler-flowmetry and microdialysis study in rats. J Neurotrauma. 2008;25:539–48.
Schubert GA, Poli S, Schilling L, Heiland S, Thome C. Hypothermia reduces cytotoxic edema and metabolic alterations during the acute phase of massive SAH: a diffusion-weighted imaging and spectroscopy study in rats. J Neurotrauma. 2008;25:841–52.
Piepgras A, Elste V, Frietsch T, Schmiedek P, Reith W, Schilling L. Effect of moderate hypothermia on experimental severe subarachnoid hemorrhage, as evaluated by apparent diffusion coefficient changes. Neurosurgery. 2001;48:1128–34 discussion 34–5.
Wang ZP, Chen HS, Wang FX. Influence of plasma and cerebrospinal fluid levels of endothelin-1 and no in reducing cerebral vasospasm after subarachnoid hemorrhage during treatment with mild hypothermia, in a dog model. Cell Biochem Biophys. 2011;61:137–43.
Todd MM, Hindman BJ, Clarke WR, Torner JC. Mild intraoperative hypothermia during surgery for intracranial aneurysm. N Engl J Med. 2005;352:135–45.
Gasser S, Khan N, Yonekawa Y, Imhof HG, Keller E. Long-term hypothermia in patients with severe brain edema after poor-grade subarachnoid hemorrhage: feasibility and intensive care complications. J Neurosurg Anesthesiol. 2003;15:240–8.
Seule MA, Muroi C, Mink S, Yonekawa Y, Keller E. Therapeutic hypothermia in patients with aneurysmal subarachnoid hemorrhage, refractory intracranial hypertension, or cerebral vasospasm. Neurosurgery. 2009;64:86–92 discussion 3.
Seule M, Keller E. Hypothermia after aneurysmal subarachnoid hemorrhage. Crit Care. 2012;16(Suppl 2):21–3.
Erecinska M, Thoresen M, Silver IA. Effects of hypothermia on energy metabolism in mammalian central nervous system. J Cereb Blood Flow Metab. 2003;23:513–30.
Yenari M, Wijman C, Stienberg G. Effects of hypothermia on cerebral metabolism, blood flow and autoregulation. New York: Marcel Dekker; 2004.
Rosomoff HL, Holaday DA. Cerebral blood flow and cerebral oxygen consumption during hypothermia. Am J Physiol. 1954;179:85–8.
Ehrlich MP, McCullough JN, Zhang N, et al. Effect of hypothermia on cerebral blood flow and metabolism in the pig. Ann Thorac Surg. 2002;73:191–7.
Marion DW, Obrist WD, Carlier PM, Penrod LE, Darby JM. The use of moderate therapeutic hypothermia for patients with severe head injuries: a preliminary report. J Neurosurg. 1993;79:354–62.
Shiozaki T, Sugimoto H, Taneda M, et al. Effect of mild hypothermia on uncontrollable intracranial hypertension after severe head injury. J Neurosurg. 1993;79:363–8.
Metz C, Holzschuh M, Bein T, et al. Moderate hypothermia in patients with severe head injury: cerebral and extracerebral effects. J Neurosurg. 1996;85:533–41.
Keller E, Krayenbuhl N, Bjeljac M, Yonekawa Y. Cerebral vasospasm: results of a structured multimodal treatment. Acta Neurochir Suppl. 2005;94:65–73.
Aaslid R, Markwalder TM, Nornes H. Noninvasive transcranial Doppler ultrasound recording of flow velocity in basal cerebral arteries. J Neurosurg. 1982;57:769–74.
Krejza J, Mariak Z, Walecki J, Szydlik P, Lewko J, Ustymowicz A. Transcranial color Doppler sonography of basal cerebral arteries in 182 healthy subjects: age and sex variability and normal reference values for blood flow parameters. AJR Am J Roentgenol. 1999;172:213–8.
Clyde BL, Resnick DK, Yonas H, Smith HA, Kaufmann AM. The relationship of blood velocity as measured by transcranial doppler ultrasonography to cerebral blood flow as determined by stable xenon computed tomographic studies after aneurysmal subarachnoid hemorrhage. Neurosurgery. 1996;38:896–904 discussion-5.
Bishop CC, Powell S, Rutt D, Browse NL. Transcranial Doppler measurement of middle cerebral artery blood flow velocity: a validation study. Stroke. 1986;17:913–5.
Lindegaard KF, Lundar T, Wiberg J, Sjoberg D, Aaslid R, Nornes H. Variations in middle cerebral artery blood flow investigated with noninvasive transcranial blood velocity measurements. Stroke. 1987;18:1025–30.
Baumgartner RW, Mathis J, Sturzenegger M, Mattle HP. A validation study on the intraobserver reproducibility of transcranial color-coded duplex sonography velocity measurements. Ultrasound Med Biol. 1994;20:233–7.
ter Minassian A, Melon E, Leguerinel C, Lodi CA, Bonnet F, Beydon L. Changes in cerebral blood flow during PaCO2 variations in patients with severe closed head injury: comparison between the Fick and transcranial Doppler methods. J Neurosurg. 1998;88:996–1001.
Giller CA, Bowman G, Dyer H, Mootz L, Krippner W. Cerebral arterial diameters during changes in blood pressure and carbon dioxide during craniotomy. Neurosurgery. 1993;32:737–41 discussion 41–2.
Fontanella M, Valfre W, Benech F, et al. Vasospasm after SAH due to aneurysm rupture of the anterior circle of Willis: value of TCD monitoring. Neurol Res. 2008;30:256–61.
Weir B, Macdonald RL, Stoodley M. Etiology of cerebral vasospasm. Acta Neurochir Suppl. 1999;72:27–46.
Nemoto EM, Klementavicius R, Melick JA, Yonas H. Suppression of cerebral metabolic rate for oxygen (CMRO2) by mild hypothermia compared with thiopental. J Neurosurg Anesthesiol. 1996;8:52–9.
Steen PA, Newberg L, Milde JH, Michenfelder JD. Hypothermia and barbiturates: individual and combined effects on canine cerebral oxygen consumption. Anesthesiology. 1983;58:527–32.
Kim JH, Kim SH, Yoo SK, Kim JY, Nam YT. The effects of mild hypothermia on thiopental-induced electroencephalogram burst suppression. J Neurosurg Anesthesiol. 1998;10:137–41.
Schwab S, Schwarz S, Aschoff A, Keller E, Hacke W. Moderate hypothermia and brain temperature in patients with severe middle cerebral artery infarction. Acta Neurochir Suppl. 1998;71:131–4.
Iida K, Kurisu K, Arita K, Ohtani M. Hyperemia prior to acute brain swelling during rewarming of patients who have been treated with moderate hypothermia for severe head injuries. J Neurosurg. 2003;98:793–9.
Giannotta SL, Raisis JE, McGillicuddy JE, Kindt GW. The effect of temperature on cerebrovascular resistance and cerebral metabolism in the primate. J Surg Res. 1978;25:105–10.
Van Bel F, Zeeuwe PE, Dorrepaal CA, Benders MJ, Van de Bor M, Hardjowijono R. Changes in cerebral hemodynamics and oxygenation during hypothermic cardiopulmonary bypass in neonates and infants. Biol Neonate. 1996;70:141–54.
Keller E, Steiner T, Fandino J, Schwab S, Hacke W. Changes in cerebral blood flow and oxygen metabolism during moderate hypothermia in patients with severe middle cerebral artery infarction. Neurosurg Focus. 2000;8:e4.
Nakamura T, Nagao S, Kawai N, Honma Y, Kuyama H. Significance of multimodal cerebral monitoring under moderate therapeutic hypothermia for severe head injury. Acta Neurochir Suppl. 1998;71:85–7.
Bisschops LL, van der Hoeven JG, Hoedemaekers CW. Effects of prolonged mild hypothermia on cerebral blood flow after cardiac arrest. Crit Care Med. 2012;40:2362–7.
Török E, Klopotowski M, Trabold R, Thal SC, Plesnila N, Scholler K. Mild hypothermia (33 degrees C) reduces intracranial hypertension and improves functional outcome after subarachnoid hemorrhage in rats. Neurosurgery. 2009;65:352–9 discussion 9.
Kawamura S, Suzuki A, Hadeishi H, Yasui N, Hatazawa J. Cerebral blood flow and oxygen metabolism during mild hypothermia in patients with subarachnoid haemorrhage. Acta Neurochir (Wien). 2000;142:1117–11121 discussion 21–2.
Voldby B, Enevoldsen EM, Jensen FT. Regional CBF, intraventricular pressure, and cerebral metabolism in patients with ruptured intracranial aneurysms. J Neurosurg. 1985;62:48–58.
Grubb RL Jr, Raichle ME, Eichling JO, Gado MH. Effects of subarachnoid hemorrhage on cerebral blood volume, blood flow, and oxygen utilization in humans. J Neurosurg. 1977;46:446–53.
Macdonald RL, Pluta RM, Zhang JH. Cerebral vasospasm after subarachnoid hemorrhage: the emerging revolution. Nat Clin Pract Neurol. 2007;3:256–63.
Muroi C, Frei K, El Beltagy M, Cesnulis E, Yonekawa Y, Keller E. Combined therapeutic hypothermia and barbiturate coma reduces interleukin-6 in the cerebrospinal fluid after aneurysmal subarachnoid hemorrhage. J Neurosurg Anesthesiol. 2008;20:193–8.
Jarus-Dziedzic K, Juniewicz H, Wronski J, et al. The relation between cerebral blood flow velocities as measured by TCD and the incidence of delayed ischemic deficits. A prospective study after subarachnoid hemorrhage. Neurol Res. 2002;24:582–92.
Keller E, Imhof HG, Gasser S, Terzic A, Yonekawa Y. Endovascular cooling with heat exchange catheters: a new method to induce and maintain hypothermia. Intensive Care Med. 2003;29:939–43.
Acknowledgments
M. S. was supported by a personal research Grant from the University Zurich, Switzerland.
Conflict of interest
The other authors have no financial or institutional conflict of interest.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Seule, M., Muroi, C., Sikorski, C. et al. Therapeutic Hypothermia Reduces Middle Cerebral Artery Flow Velocity in Patients with Severe Aneurysmal Subarachnoid Hemorrhage. Neurocrit Care 20, 255–262 (2014). https://doi.org/10.1007/s12028-013-9927-x
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12028-013-9927-x
Keywords
- Hypothermia
- Subarachnoid hemorrhage
- Transcranial Doppler
- Flow velocity
- Cerebral blood flow