This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Request Permissions Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Manno, E. M. Articles by Ogilvy, C. S. Search for Related Content PubMed PubMed Citation Articles by Manno, E. M. Articles by Ogilvy, C. S.

(Stroke. 1998;29:422-428.)
© 1998 American Heart Association, Inc.

Original Contributions

Effects of Induced Hypertension on Transcranial Doppler Ultrasound Velocities in Patients After Subarachnoid Hemorrhage

E. M. Manno, MD; D. R. Gress, MD; L. H. Schwamm, MD; M. N. Diringer, MD; C. S. Ogilvy, MD

From the Neurology/Neurosurgery Intensive Care Unit, Washington University School of Medicine, St Louis, Mo (E.M.M., M.N.D.); Neurovascular Stroke Service, University of California at San Francisco (D.R.G.); and Acute Stroke Service and Department of Neurosurgery, Harvard Medical School and Massachusetts General Hospital, Boston, Mass (L.H.S., C.S.O.).

Correspondence to Edward M. Manno, MD, Washington University School of Medicine, Department of Neurology, Campus Box 8111, 660 S Euclid Ave, St Louis, MO 63110. E-mail mannoe{at}neuro.wustl.edu

	Abstract

Top Abstract Introduction Subjects and Methods Results Discussion References

 
Background and Purpose—Transcranial doppler ultrasound (TCD) is used after subarachnoid hemorrhage to detect cerebral vasospasm and is often treated with induced hypertension. Cerebral autoregulation, however, may be disturbed in this population, raising the possibility that TCD velocities may be elevated by induced hypertension. To study this possibility, we performed continuous TCD monitoring of the middle cerebral artery during the induction and withdrawal of induced hypertension in patients after subarachnoid hemorrhage.

Methods—Twenty-eight patients were studied during the induction and withdrawal of hypertension using primarily phenylephrine. Continuous monitoring was performed on the middle cerebral artery with the highest flow velocity. Treatment was based on rising TCD velocities or clinical evidence for cerebral vasospasm. Mean arterial pressure and mean TCD velocities were recorded every minute. A change of >15% from starting TCD values was considered significant. Cerebral autoregulation was calculated as a percentage of intact autoregulation. Patients were subsequently divided into groups of disturbed and intact autoregulation.

Results—In 10 of 19 patients (53%), TCD velocities changed by >15% and paralleled changes in mean arterial pressure. This directly altered the TCD interpretation of the grade of vasospasm in 7 of 19 patients (36%). Three additional patients had smaller absolute changes in TCD velocities. No clinical difference could be identified between patients with disturbed and intact autoregulation.

Conclusions—In patients with disturbed autoregulation after subarachnoid hemorrhage, induced hypertension can alter cerebral blood flow velocities. The level of autoregulation needs to be considered when interpreting TCD velocities in patients after subarachnoid hemorrhage.

Key Words: ultrasonography, Doppler • subarachnoid hemorrhage • hypertension

	Introduction

Top Abstract Introduction Subjects and Methods Results Discussion References

 
Cerebral vasospasm is a pathological luminal narrowing of the cerebral arteries that occurs in patients after SAH and is a leading cause of morbidity and mortality in these patients. A critical reduction of CBF caused by this narrowing leads to a clinical syndrome of delayed ischemia, which develops in 25% to 30% of SAH patients.¹ The medical management of cerebral vasospasm uses volume expansion and induced hypertension in an attempt to increase CBF.^{2 3}

TCD is a noninvasive means of measuring flow velocities in the basal cerebral arteries and is used routinely to detect vasospasm.^{4 5} Traditionally, rising TCD velocities have been interpreted as signifying progressive vessel narrowing and have been used by some centers to guide medical therapies. More recently, TCD velocities have been shown to parallel changes in CBF and have been used to assess cerebral autoregulation.⁶ Because cerebral autoregulation may be disturbed in patients after SAH, it is possible that the medical maneuvers designed to increase CBF (ie, induced hypertension, volume loading) may increase TCD velocities and complicate the interpretation of TCD data. Despite this possible complication, TCD velocities have not been studied during hemodynamic manipulation.

To define this relationship, we performed continuous TCD monitoring of patients after SAH. Velocities were monitored during the induction and withdrawal of induced hypertension and compared with velocity changes that would occur naturally over a similar time period without hemodynamic manipulation. The purpose of this study is to assess whether induced hypertension could result in increased TCD velocities that could be misinterpreted as worsening vasospasm.

	Subjects and Methods

Top Abstract Introduction Subjects and Methods Results Discussion References

 
Patients
Inclusion criteria were (1) age >18 years; (2) SAH due to an angiographically demonstrated cerebral aneurysm (All Hunt-Hess and Fisher grades were included); (3) post-SAH day 3 to 21; (4) initiation or withdrawal from induced hypertension for vasospasm; (5) adequate transtemporal visualization of the MCA; and (6) available personnel and equipment at the time of initiation or withdrawal of treatment.

Exclusion criteria were (1) patients intolerant of pressors due to hemodynamic instability (ie, congestive heart failure, acute myocardial infarction); (2) baseline TCD values that could not be established due to continued cyclic variations; and (3) cyclic variations >15% of baseline TCD values (see below).

A total of 36 studies were performed on 24 patients. Twenty-eight studies were performed on 19 patients at the time of induction and/or withdrawal of induced hypertension. The control group consisted of 8 patients who were monitored during a period of time when hemodynamic manipulation was not performed. In 7 control patients, no drug was present at the time of study. In 1 patient, pressors were present but not adjusted during the time of study. Three patients were monitored at a separate time during hemodynamic manipulation and thus served in both control and experimental groups. All patients were monitored in the neurological intensive care unit with invasive arterial pressure monitors, central venous or pulmonary artery catheters, and when appropriate, intracranial pressure monitors. Daily TCD recordings were performed under conditions of eucapnea confirmed by arterial blood gas sampling just before the study. All patients were afebrile at the time of study. For each patient demographic data, location of aneurysm, side of study, Hunt-Hess grade, and Fisher grade on presentation were recorded. The study was approved by the Human Studies Committee of the Massachusetts General Hospital.

Routine management of the patients included 60 mg nimodipine PO every 4 hours, 100 mg phenytoin PO/IV every 8 hours, and early surgery (day 1 to 3) to repair the aneurysm.⁷ Hydrocephalus was treated with a ventriculostomy. After aneurysm repair, patients were given 250 mL of 5% albumin every 4 hours and isotonic saline as needed to maintain either a central venous pressure of >9 or a capillary wedge pressure of >14 mm Hg. The decision to initiate treatment for vasospasm was based on rising TCD velocities (see below), angiographic evidence of vasospasm, or the onset of delayed ischemic deficits.

Induced Hypertension
TCD criteria for inducing hypertension were as follows: if mean TCD velocities were 120 to 150 cm/s, systolic blood pressure was raised to 140 to 159 mm Hg; for TCD velocities of 151 to 200 cm/s, SBP was elevated to 160 to 179 mm Hg; and for TCD velocities >200 cm/s, systolic blood pressure was raised to >180 mm Hg. Hypertension was usually induced with a continuous infusion of phenylephrine. If phenylephrine alone was ineffective in achieving the systolic blood pressure goals, dopamine or norepinephrine was used alone or in combination with phenylephrine. Withdrawal of induced hypertension was accomplished using the same TCD criteria. In 3 patients, dopamine was added or withdrawn from a patient on phenylephrine. TCD velocity changes reflect the changes in dopamine levels with stable phenylephrine dosage.

TCD Monitoring
TCD recording of the M1 segment of the MCA were recorded using the MedaSonics CDS system. Ultrasonography was performed at a depth of 45 to 55 mm to obtain the highest mean velocity for both MCAs. Continuous monitoring was then performed on the MCA with the highest velocity using a 2-MHz probe secured by a sliding wheel head frame. To control for large or cyclic variations noted during continuous monitoring,⁸ velocities were continuously recorded for 1 to 3 minutes to establish a baseline and then during the induction and withdrawal of hypertension. Studies were only concluded when a new baseline level could be established and maintained. This value was defined as a mean TCD velocity that did not vary by greater than 2 cm/s. Patients were excluded if baseline values could not be obtained or maintained or if cyclic variations varied by >15% of baseline TCD values. Mean TCD velocity, MAP, and when available intracranial pressure (ICP) were recorded every minute during the entire procedure. CPP was calculated as MAP-ICP. A significant change in velocity that could not be attributed to variations in time, side to side differences, or cerebral activation was considered to occur if the velocities varied by >15% from baseline during the study.^{9 10}

Assessment of Cerebral Autoregulation
Cerebral autoregulation was evaluated using a method developed by Tiecks et al.¹¹ Autoregulation was assessed at baseline and after the target blood pressure had been reached and was stable for 1 to 3 minutes. It was calculated as % change in CVR/% change in MAP (or CPP)x100. CVR was defined as MAP (or CPP)/mean TCD velocity, and the percentage was calculated as (CVR₂-CVR₁/CVR₁)x100. Similarly, a percentage change in MAP was calculated as (MAP₂-MAP₁/MAP₁) or CPP₂-CPP₁/CPP₁x100. Using this method, autoregulation is expressed as a percentage, with 100% signifying intact autoregulation and 0% indicating that CBF is completely pressure passive. For the purposes of this study, we used an estimated index of cerebral autoregulation of >50% to signify intact autoregulation.

Statistical Analysis
Patients were grouped into hemodynamic or control groups. The hemodynamic group was later divided into those patients with intact and disturbed autoregulation. Comparisons of the clinical and testing data between these groups were performed using unpaired t tests. All percentage changes in MAP or TCD velocities were converted to positive numbers, and the mean change in MAP and TCD velocities were compared using an unpaired t test. Comparisons of Hunt-Hess¹² and Fisher¹³ groups, along with comparisons of autoregulation, were performed using a Mann-Whitney U test. A value of P<.05 was considered to indicate statistical significance.

	Results

Top Abstract Introduction Subjects and Methods Results Discussion References

 
The demographic data and conditions during testing for this population are outlined in Table 1. Twenty-eight studies were performed during blood pressure manipulation in 19 patients. Fourteen studies were performed in 13 patients during both the induction and withdrawal of hypertension. Eight patients were studied while blood pressure was not being manipulated. The majority of patients showed Hunt-Hess grades 3 and 4 and Fisher group 3 (Table 1). Tests were performed between days 3 and 18 (average, 9.3) after SAH. Phenylephrine was used as the sole agent to induce hypertension in 23 studies; in 3 studies, dopamine was added or withdrawn in combination with phenylephrine. Blood pressure changes in these patients represented the effect of addition or withdrawal of dopamine. In 1 control patient, phenylephrine was used with norepinephrine. In 2 experimental studies, norepinephrine alone was used. The average time to reach the blood pressure goal was 17.3 minutes (range, 6 to 36).

View this table: [in this window] [in a new window]   Table 1. General Patient Data and Conditions of Testing

Table 2 outlines the hemodynamic data during continuous TCD testing. MAP during TCD testing ranged from 66 to 134 mm Hg. Blood pressure varied between 7% and 44% (mean 20.1±9.5% SD) from baseline blood pressure during the infusion or withdrawal of pressors. Baseline MCA TCD velocities ranged from 38 to 249 cm/s. TCD velocities varied from baseline TCD velocities by 1.6% to 32% (mean 13.7±9.5% SD) during hemodynamic manipulation. Using Aaslid criteria at the time of initial testing, 13 patients during 16 studies had no evidence of vessel narrowing (TCD velocities <120 cm/s), 7 patients in 7 studies were in mild vasospasm (TCD velocities >120 cm/s), 4 patients in 5 studies were in moderate vasospasm (TCD velocities >150 cm/s), and 1 patient in 1 study was in severe vasospasm (TCD velocities >200 cm/s).

View this table: [in this window] [in a new window]   Table 2. Cerebral Autoregulation After SAH

In 10 of 19 patients (53%), TCD velocities changed >15% during the induction or withdrawal of pressors (P<.001 Mann-Whitney U). TCD velocities remained constant in the patients in whom blood pressure was not manipulated The changes in velocities that occurred during pressure manipulation were large enough to move 7 of 19 patients (36%) into another category of vasospasm.

Thirteen of 19 patients (63%) were judged to have impaired cerebral autoregulation at least once during continuous MCA TCD monitoring. These changes occurred over a range of 4 to 15 days after SAH. There was no difference in percentage of cerebral autoregulation when either CPP or MAP was used to calculate cerebral autoregulation in those patients that had intracranial pressure monitoring available.

There was no significant difference in age, presenting clinical status, or experimental conditions between patients grouped according to whether autoregulation was intact or disturbed.

	Discussion

Top Abstract Introduction Subjects and Methods Results Discussion References

 
The results of this study suggest that in a majority of patients with SAH, TCD velocities are altered by manipulation of blood pressure. This change occurred over a wide range of blood pressure and was of sufficient magnitude in several cases to alter the interpretation of MCA flow velocities being used to assess cerebral vasospasm (Fig 1).

View larger version (15K): [in this window] [in a new window]   Figure 1. Effect of MAP on TCD ultrasound velocities. A, Effects of MAP on TCD velocities during 10 studies in patients with disturbed autoregulation. A change of >15% in TCD velocities was considered significant. Note that in several cases the change in velocities were of sufficient magnitude to potentially lead to the misinterpretation of worsening or improving vasospasm. B, Effects of MAP on TCD velocities during 14 studies in patients with intact autoregulation.

This direct effect of blood pressure on TCD velocities indicates a loss of cerebral autoregulation. Cerebral autoregulation has been shown to be impaired after SAH in both animals^{14 15 16} and humans,^{17 18} with the extent of impairment related to the degree of vessel narrowing¹⁹ or the clinical condition of the patient.^{18 19} TCD ultrasound has been used to assess cerebral autoregulation in a post-SAH population. Giller²⁰ used a transient hyperemic response to carotid compression as a qualitative means to test cerebral autoregulation in patients after SAH. A computerized version of this response found a positive correlation between loss of autoregulation and worsening neurological status.²¹

The use of TCD flow velocities to estimate actual blood flow requires that the vessel diameter remains unchanged and that the perfusion territory of a given artery remains constant.²² It is possible that the medications used to induce hypertension may have had a direct effect on the cerebral vessels confounding our results. We doubt that any of the medications used would have had a significant effect of the cerebral vessels because receptors have been shown to be limited in both number and activity on the basal cerebral arteries.^{23 24} Similarly, no change in cerebral artery diameter has been noted under direct visualization when phenylephrine is used.²⁵ It is not known whether perfusion territories remain constant during induced hypertension. Sorteberg et al²⁶ have suggested that perfusion territories may be altered with acetazolamide. Whether this occurs with phenylephrine would require concurrent blood flow and flow velocity assessments.

There are a number of factors that may confound our results. Cyclic fluctuation of TCD velocities during continuous monitoring has been described and is thought to reflect phasic dilation and contraction of small distal regulating arteries.⁸ We noted similar variations in a majority of our population. The variations noted, however, were variable in onset and duration and averaged only 9% of baseline TCD values. We attempted to control for these by establishing baselines without variations and eliminating patients with large cyclic variations. In all cases, cyclic variations were significantly smaller than the mean change in TCD velocities. It is possible that in a few cases changes in CO₂ could account for variations in TCD velocities. However, we believe this to be highly unlikely because patient heart rate, temperature, and respiratory rate were monitored closely and did not change during the period of observation.

Many authors have expressed concern about using TCD alone to estimate blood flow.^{27 28} The ratio of the extracranial internal carotid artery mean flow velocity to the MCA mean flow velocity has been used to distinguish hyperemia from vessel narrowing.²⁹ Romner et al³⁰ reported a good correlation with this ratio and CBF in six head trauma patients. The lack of Lindegaard ratios represents a limitation of this work. This limitation, however, is attenuated by our control group, which demonstrated that vessel narrowing did not occur during the period of observation. Therefore, increases in flow velocity must be secondary to increases in volume flow. Theoretically, Lindegaard ratios should verify this response; however, like other authors, we found these ratios difficult to use in our intensive care unit population. We abandoned the use of these ratios because of concerns that the insonation angle of the extracranial internal carotid artery could not be reliably reproduced in the neck.^{28 31}

We were unable to define a demographic or clinical feature that was predictive of which patients may have had disturbed autoregulation. Because this was designed as an observational study of the clinical practice at the Massachusetts General Hospital, where treatment of vasospasm was based on TCD velocities, many patients did not have cerebral autoregulation assessed. A more structured protocol might have been better able to delineate the time course and clinical factors involved in determining which patients may have disturbed autoregulation.

There are important implications of the observation that TCD velocities change when blood pressure is manipulated. Increasing MCA TCD flow velocities in patients being treated with vasopressors could be misinterpreted as indicating worsening vasospasm (Fig 2). In this report, changes in velocity were of sufficient magnitude in 25% of the studies to suggest that vasospasm was actually worsening or improving. This misinterpretation would likely occur if TCD studies were performed intermittently and continuous assessments were not made during blood pressure manipulations. If TCD velocities increase during the induction of hypertension and these are misinterpreted as worsening vasospasm, invasive procedures or medical therapies designed to treat vasospasm may be unnecessarily initiated or prolonged. Similarly, a decrease in TCD velocities seen with a reduction of induced hypertension could be misinterpreted as improving vasospasm and subsequently lead to a premature withdrawal of medical treatments.

View larger version (29K): [in this window] [in a new window]   Figure 2. Examples of TCD flow velocity profiles during hemodynamic manipulations. A, Patient 13: Continuous MCA TCD profile during induced hypertension over a 15-minute period. Note how an increase in velocity in a patient with poor autoregulation could be misinterpreted as worsening vasospasm. B, Patient 11: Example of a continuous MCA TCD profile in a patient with poor autoregulation during reduction in blood pressure. Decreasing velocities could be misinterpreted as improving vasospasm. C, Repeat testing of patient 13. Induced hypertension is withdrawn 12 days after initial testing. Note improved autoregulation with little change in the TCD profile during reduction in blood pressure.

We believe that in patients with disturbed autoregulation, measures designed to increase CBF will increase TCD velocities. Levy et al³² noted a "paradoxical increase" in TCD velocities and a reversal of neurological deficits in patients after SAH who were given dobutamine. Dobutamine is a ß1 agonist that is used to increased cardiac output and has been shown to increase ocular blood flow and MCA TCD velocities.³³ These results are consonant with our findings that TCD velocities will parallel CBF changes in patients with disturbed autoregulation. This may seem intuitively obvious; however, this is not routinely considered in the interpretation of TCD velocities. We speculate that much of the current controversy that exists over the use of TCD to monitor vasospasm could be explained by the differences in medical therapies applied to patients that have impaired cerebral autoregulation.^{34 35} To avoid confusing loss of autoregulation with changes in the severity of vasospasm, we would recommend that all TCD studies in the setting of vasospasm have hemodynamic parameters documented before and after blood pressure manipulation or that continuous monitoring be performed to determine TCD changes with blood pressure manipulation.

If future studies with CBF measurements suggest that changes in TCD velocities can provide an approximation of CBF and that loss of cerebral autoregulation can be correlated with clinical symptoms, then TCD testing may be able to be used more effectively to tailor medical therapies in treating cerebral vasospasm (ie, treatment could be initiated and maintained during loss of autoregulation and withdrawn only after cerebral autoregulation returned to baseline).

In summary, TCD velocities can be affected by hemodynamic manipulations that occur during the treatment of patients with cerebral vasospasm and are of sufficient magnitude to lead to the misinterpretation of these values. Future work delineating the effects of hemodynamic augmentation on TCD velocities may provide guidance as to when hemodynamic therapies should be initiated or withdrawn.

	Selected Abbreviations and Acronyms

 

CBF = cerebral blood flow CPP = cerebral perfusion pressure CVR = cerebrovascular resistance MAP = mean arterial blood pressure MCA = middle cerebral artery SAH = subarachnoid hemorrhage TCD = transcranial Doppler sonography

Received June 6, 1997; revision received November 24, 1997; accepted December 2, 1997.

	References

Top Abstract Introduction Subjects and Methods Results Discussion References

 
1. Kasell NF, Torner JC, Haley EC, Jane JA, Adams HP, Kongable GL. The International Cooperative Study on the timing of aneurysm surgery, I: overall management results. J Neurosurg. 1990;73:18–36.[Medline] [Order article via Infotrieve]

2. Muizelaar JP, Becker DP. Induced hypertension for the treatment of cerebral ischemia after subarachnoid hemorrhage: direct effect on cerebral blood flow. Surg Neurol. 1986;25:317–325.[Medline] [Order article via Infotrieve]

3. Origitano TL, Wascher TM, Reichman OH, Anderson DE. Sustained increased cerebral blood flow with prophylactic hypertensive hypervolemia hemodilution (`triple-H') therapy after subarachnoid hemorrhage. Neurosurgery. 1990;27:729–740.[Medline] [Order article via Infotrieve]

4. Aaslid R, Huber P, Nornes H. A transcranial Doppler method in the evaluation of cerebrovascular spasm. Neuroradiology. 1986;28:11–16.[Medline] [Order article via Infotrieve]

5. Newell DW, Grady MS, Eskridge JM, Winn HR. Distribution of angiographic vasospasm after subarachnoid hemorrhage: implications for diagnosis by transcranial Doppler ultrasonography. Neurosurgery. 1990;27:574–577.[Medline] [Order article via Infotrieve]

6. Larsen FS, Olsen KS, Hansen BA, Paulson OB, Knudsen GM. Transcranial Doppler is valid for determination of the lower limit of cerebral blood flow autoregulation. Stroke. 1994;25:1985–1988.[Abstract]

7. Romner B, Ljunggren B, Brandt L, Saveland H. Correlation of transcranial Doppler sonography findings with timing of aneurysm surgery. J Neurosurg. 1990;73:72–76.[Medline] [Order article via Infotrieve]

8. Newell DW, Aaslid R, Stooss R, Reulen HJ. The relationship of blood flow velocity fluctuations to intracranial pressure B waves. J Neurosurg. 1992;76:415–421.[Medline] [Order article via Infotrieve]

9. Sorteberg W, Langmoen IA, Lindegaard K-F, Nornes H. Side-to-side differences and day-to-day variations of transcranial Doppler parameters in normal subjects. J Ultrasound Med. 1990;9:403–409.[Abstract]

10. Droste DW, Harders AG, Rastogi E. Two transcranial Doppler studies of blood flow velocity in both middle cerebral arteries during rest and the performance of cognitive tasks. Neuropsychologia. 1989;27:1221–1230.[Medline] [Order article via Infotrieve]

11. Tiecks FP, Lam AM, Aaslid R, Newell DW. Comparison of static and dynamic cerebral autoregulation measurements. Stroke. 1995;26:1014–1019.[Abstract/Free Full Text]

12. Hunt WE, Hess RM. Surgical risk as related to time of intervention in the repair of intracranial aneurysms. J Neurosurg. 1968;28:14–20.[Medline] [Order article via Infotrieve]

13. Fisher CM, Kistler JP, Davis JM. Relation of cerebral vasospasm to subarachnoid hemorrhage visualized by computerized tomographic scanning. Neurosurgery. 1980;6:1–9.[Medline] [Order article via Infotrieve]

14. Boisvert DP, Overton TR, Weir B, Grace MG. Cerebral arterial responses to induced hypertension following subarachnoid hemorrhage in the monkey. J Neurosurg. 1978;49:75–83.[Medline] [Order article via Infotrieve]

15. Pickard JD, Boisvert DP, Graham DI, Fitch W. Late effects of subarachnoid hemorrhage on the response of the primate circulation to drug induced changes in arterial blood pressure. J Neurol Neurosurg Psychiatry. 1979;42:899–903.[Abstract/Free Full Text]

16. Takeuchi H, Handa Y, Kobayashi H, Kawano H, Hayashi M. Impairment of cerebral autoregulation during the development of chronic cerebral vasospasm after subarachnoid hemorrhage in primates. Neurosurgery. 1991;28:41–48.[Medline] [Order article via Infotrieve]

17. Grubb RL, Raichle ME, Eichling JO, Gado MH. Effects of subarachnoid hemorrhage on cerebral blood volume, blood flow and oxygen utilization in humans. J Neurosurg. 1977;46:446–453.[Medline] [Order article via Infotrieve]

18. Dernbach PD, Little JR, Jones SC, Ebrahim ZY. Altered cerebral autoregulation and CO₂ reactively after aneurysmal subarachnoid hemorrhage. Neurosurgery. 1988;22:822–826.[Medline] [Order article via Infotrieve]

19. Volby B, Enevoldsen EM, Jensen FT. Regional CBF, intraventricular pressure, and cerebral metabolism in patients with ruptured intracranial aneurysms. J Neurosurg. 1985;62:48–58.[Medline] [Order article via Infotrieve]

20. Giller CA. A bedside test for cerebral autoregulation using transcranial Doppler ultrasound. Acta Neurochir (Wien). 1991;108:7–14.[Medline] [Order article via Infotrieve]

21. Smielewski P, Czosnyka M, Iyer V, Piechnik S, Whitehouse H, Pickard J. Computerised transient hyperemia response test 190: a method for the assessment of cerebral autoregulation. Ultrasound Med Biol. 1995;21:599–611.[Medline] [Order article via Infotrieve]

22. Sorteberg W. Cerebral artery blood velocity and cerebral blood flow. In: Newell DW, Aaslid R, eds. Transcranial Doppler. New York, NY: Raven Press Publishers; 1992:57–66.

23. Bevan JA, Duckworth J, Laher I, Oriowo MA, McPherson GA, Bevan RD. Sympathetic control of cerebral arteries: specialization in receptor type, reserve, affinity, and distribution. FASEB J. 1987;1:193–198.[Abstract]

24. Duckworth JW, Wellman GC, Walters CL, Bevan JA. Aminergic histofluorescence and contractile responses to transmural electrical field stimulation and norepinephrine of human middle cerebral arteries obtained promptly after death. Circ Res. 1989;65:316–324.[Abstract/Free Full Text]

25. 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;32:737–742.[Medline] [Order article via Infotrieve]

26. Sorteberg W, Lindegaard KF, Rootwelt K, Dahl A, Nyberg-Hansen D, Russell D, Nornes H. Effect of acetazolamide on cerebral artery blood velocity and regional cerebral blood flow in normal subjects. Acta Neurochir (Wien). 1989;97:139–145.[Medline] [Order article via Infotrieve]

27. Lewis DH, Hsu S, Eskridge J, Cohen W, Dalley R, Newell D, Douville C, Pendleton G, Chestnut CH, Winn HR. Brain SPECT and transcranial Doppler ultrasound in vasospasm-induced delayed cerebral ischemia after subarachnoid hemorrhage J Stroke Cerebrovasc Dis. 1992;2:12–21.

28. Giller CA, Purdy P, Giller A, Batjer HH, Kopitnik T. Elevated transcranial Doppler ultrasound velocities following therapeutic arterial dilation. Stroke. 1995;26:123–127.[Abstract/Free Full Text]

29. Lindegaard KF, Bakke SJ, Sorteberg W, Nakstad P. Cerebral vasospasm diagnosis by means of angiography and blood flow velocity measurements. Acta Neurochir (Wien). 1989;100:12–24.[Medline] [Order article via Infotrieve]

30. Romner B, Bellner J, Kongstad P, Sjoholm H. Elevated transcranial Doppler flow velocities after severe head injury: cerebral vasospasm or hyperemia? J Neurosurg. 1996;85:90–97.[Medline] [Order article via Infotrieve]

31. Jackson M, Thomas-Lukes K, McBride DQ, Martin NA. The use of transcranial Doppler to distinguish vasospasm from hyperemia in head trauma patients. Stroke. 1994;25:756. Abstract.

32. Levy ML, Rabb CH, Zelman V, Giannotta SL. Cardiac performance enhancement from dobutamine in patients refractory to hypervolemic therapy for cerebral vasospasm. J Neurosurg. 1993;79:494–499.[Medline] [Order article via Infotrieve]

33. Saha M, Muppala MR, Castaldo JE, Gee W, Reed JF, Morris L. The impact of cardiac index on cerebral hemodynamics. Stroke. 1993;24:1686–1690.[Abstract/Free Full Text]

34. Laumer R, Steinmeier R, Gönner F, Vogtmann T, Priem R, Fahlbusch R. Cerebral hemodynamics in subarachnoid hemorrhage evaluated by transcranial Doppler sonography, I: reliability of flow velocities in clinical management. Neurosurgery. 1993;33:1–9.[Medline] [Order article via Infotrieve]

35. Gomez CR, Malkoff MD. Cerebral hemodynamics in subarachnoid hemorrhage evaluated by transcranial Doppler sonography. Neurosurgery. 1994;34:1102–1105. Letter.

This article has been cited by other articles:

				M. Wintermark, N.U. Ko, W.S. Smith, S. Liu, R.T. Higashida, and W.P. Dillon Vasospasm after Subarachnoid Hemorrhage: Utility of Perfusion CT and CT Angiography on Diagnosis and Management AJNR Am. J. Neuroradiol., January 1, 2006; 27(1): 26 - 34. [Abstract] [Full Text] [PDF]

				J. Krejza, P. Szydlik, D. S. Liebeskind, J. Kochanowicz, O. Bronov, Z. Mariak, and E. R. Melhem Age and Sex Variability and Normal Reference Values for the VMCA/VICA Index AJNR Am. J. Neuroradiol., April 1, 2005; 26(4): 730 - 735. [Abstract] [Full Text] [PDF]

				E. F. M. Wijdicks, D. F. Kallmes, E. M. Manno, J. R. Fulgham, and D. G. Piepgras Subarachnoid Hemorrhage: Neurointensive Care and Aneurysm Repair Mayo Clin. Proc., April 1, 2005; 80(4): 550 - 559. [Abstract] [PDF]

				A J P Goddard, P P J Raju, and A Gholkar Does the method of treatment of acutely ruptured intracranial aneurysms influence the incidence and duration of cerebral vasospasm and clinical outcome? J. Neurol. Neurosurg. Psychiatry, June 1, 2004; 75(6): 868 - 872. [Abstract] [Full Text] [PDF]

This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Request Permissions Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Manno, E. M. Articles by Ogilvy, C. S. Search for Related Content PubMed PubMed Citation Articles by Manno, E. M. Articles by Ogilvy, C. S.