JOURNAL HOME CME HOME THIS MONTH PAST ISSUES ETOC COLLECTIONS
AUTHORS REVIEWERS EDITORIAL BOARD FEEDBACK RSS HELP
A&A International Anesthesia Research Society
QUICK SEARCH:   [advanced]


     

This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Email this article to a colleague
Right arrow Similar articles in this journal
Right arrow Similar articles in ISI Web of Science
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via ISI Web of Science (16)
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Soehle, M.
Right arrow Articles by Kirkpatrick, P. J.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Soehle, M.
Right arrow Articles by Kirkpatrick, P. J.
Related Collections
Right arrow Resuscitation
Right arrow Neuroanesthesia
Right arrow Critical Care

Anesth Analg 2004;98:1133-1139
© 2004 International Anesthesia Research Society
doi: 10.1213/01.ANE.0000111101.41190.99

NEUROSURGICAL ANESTHESIA

Continuous Assessment of Cerebral Autoregulation in Subarachnoid Hemorrhage

Martin Soehle, MD*,{dagger}, Marek Czosnyka, PhD{dagger}, John D. Pickard, MCh, FRCS{dagger}, and Peter J. Kirkpatrick, FRCS(SN){dagger}

*Department of Anaesthesiology and Intensive Care Medicine, University of Bonn, Bonn, Germany; and {dagger}Academic Neurosurgery Unit, Addenbrooke’s Hospital, University of Cambridge, Cambridge, United Kingdom

Address correspondence and reprint requests to Martin Soehle, MD, Klinik für Anästhesiologie und Spezielle Intensivmedizin, Universität Bonn, Sigmund-Freud-Straße 25, 53105 Bonn, Germany. Address e-mail to martin.soehle{at}ukb.uni-bonn.de


   Abstract
Top
 Abstract
Introduction
 Methods
 Results
 Discussion
 References
 
Cerebral vasospasm remains a leading cause of morbidity and mortality after subarachnoid hemorrhage (SAH). Cerebral ischemia may ensue when autoregulation fails to compensate for spasm. We examined how autoregulation is affected by vasospasm by using transcranial Doppler. The moving correlation coefficient between slow changes of arterial blood pressure and mean or systolic flow velocity (FV), termed "Mx" and "Sx," respectively, was used to characterize cerebral autoregulation. Vasospasm was declared when the mean FV increased to more than 120 cm/s and the Lindegaard ratio was more than 3. This occurred in 15 of 32 SAH patients. On the basis of the bilateral transcranial Doppler recordings of the middle cerebral artery in vasospastic patients, Mx and Sx were calculated for baseline and vasospasm. Mx increased during vasospasm (0.46 ± 0.32; mean ± SD) and was significantly higher (P = 0.021) than at baseline (0.21 ± 0.24). Sx was also increased (0.22 ± 0.26 vs 0.05 ± 0.21 at baseline; P = 0.03). Mx correlated with mean FV (r = 0.577; P = 0.025) and the Lindegaard ratio (r = 0.672; P < 0.006). Mx (P = 0.006) and Sx (P = 0.044) were higher on the vasospastic side (Mx, 0.44 ± 0.27; Sx, 0.24 ± 0.23) when compared with the contralateral side (Mx, 0.34 ± 0.29; Sx, 0.16 ± 0.25). The increased Mx and Sx during cerebral vasospasm demonstrate impaired cerebral autoregulation. Mx and Sx provide additional information on changes in autoregulation in SAH patients.

IMPLICATIONS: The moving correlation coefficients between slow changes of arterial blood pressure and mean or systolic flow velocity, termed "Mx" and "Sx," respectively, characterize cerebral autoregulation but have not been applied to subarachnoid hemorrhage. A study in 15 patients revealed that Mx and Sx were significantly increased, indicating impaired autoregulation during vasospasm as compared with baseline, as well as on the side of vasospasm in comparison with the contralateral side.


   Introduction
Top
 Abstract
 Introduction
Methods
 Results
 Discussion
 References
 
Cerebral autoregulation refers to the intrinsic capacity of the brain to maintain constant cerebral blood flow (CBF) despite changes in perfusion pressure (1,2). After subarachnoid hemorrhage (SAH), when cerebral autoregulation is frequently impaired (3–5), reductions in perfusion may contribute to delayed ischemic deficits (DID). Indeed, impaired cerebral autoregulation itself is a predictor of DID (5–8).

Cerebral vasospasm is often seen after SAH and is associated with DID (9,10). Initial studies suggest that patients with initially preserved autoregulation may be at less risk or even no risk of subsequently developing DID as compared with patients with an initial autoregulation disturbance (11,12), but evaluation with a large number of patients is desirable. When vasospasm joins preexisting autoregulation impairment, the risk of DID increases (11).

To identify patients at risk for DID, vasospasm and impaired autoregulation should be recognized early. Transcranial Doppler (TCD) sonography is a suitable technique for assessing vasospasm of the middle cerebral artery (MCA) (10,13–15) and impaired autoregulation by using methods such as the cuff deflation test (16) or the transient hyperemic response test (17). Autoregulation tests are often performed by manipulating arterial blood pressure (ABP) by using external stimuli and observing the related changes in CBF or blood flow velocity.

A less invasive method based on spontaneous changes in ABP has been introduced (18). The indices of autoregulation are calculated as moving correlation coefficients between spontaneous slow changes in ABP and slow changes in systolic (systolic index; Sx) or mean (mean index; Mx) flow velocities (FV). Sx and Mx have been shown to be indicators of autoregulation (19) and predictors for outcome in head injury (18). However, Sx and Mx have not yet been applied to SAH patients.

Mx can be interpreted as an indicator of autoregulation: a positive correlation between ABP and FV, as expressed by positive values of Mx, indicates passive dependence of blood flow on ABP (impaired autoregulation). Negative or zero values suggest active cerebrovascular responses to changes in ABP (preserved autoregulation). This preliminary study describes the first application of autoregulation assessment by means of Mx and Sx determination in patients with SAH and explores the effects of cerebral vasospasm on these indices.


   Methods
Top
 Abstract
 Introduction
 Methods
Results
 Discussion
 References
 
The study was performed according to the requirements of the local ethics committee. The data was recorded using standard neurointensive care monitoring and analyzed as a part of clinical audit. Thirty-two patients (mean age, 50 yr) admitted to Addenbrooke’s Hospital with aneurysmal SAH were studied. Diagnosis of SAH was confirmed by computed tomography, and aneurysms were identified from cerebral angiography. Bilateral TCD examinations of the MCAs and extracranial internal carotid arteries were performed on alternate days, starting from admission until approximately 2 wk after the hemorrhage or until any detected vasospasm had resolved. Patients were considered to have cerebral vasospasm if the mean MCA FV exceeded 120 cm/s (15) and the Lindegaard ratio exceeded 3.0, according to established TCD criteria (13).

All patients received treatment according to a standard protocol (20,21) that included the routine use of nimodipine and surgery for aneurysm clipping, except for two cases, in which coiling was performed. Patients who satisfied TCD criteria for vasospasm were treated by standard triple-H therapy (22).

ABP was measured invasively from the radial artery. A TCD (Neurogard, 2 MHz; Medasonics, Fremont, CA) was used for bitemporal insonation of the MCA at a depth of 50 mm. The TCD probes were fixed to a headband. The power of the TCD signal and the amplifier gain settings were adjusted to achieve a reasonable signal with the lowest possible power. Once settings were determined during the first examination in each patient, they were adopted for subsequent examinations. All examinations were performed by the same examiner (MS).

ABP and bilateral FV recordings were acquired simultaneously and continuously over a 20-min epoch for alternate days. Care was taken to monitor during periods of stable respiratory conditions that were free from clinical maneuvers. After the recordings, arterial blood gas samples were drawn from the radial artery line and analyzed.

The analog signals from the ABP monitor and TCD device were digitized with a DT 2814 analog-to-digital converter (Data Translation, Marlboro, MA) and sampled at a frequency of 50 Hz by using a laptop computer (ALT 386 SX; Amstrad, Rheinland, Germany). Software was written especially for the recording of time series (WREC; W. Zabolotny, Warsaw University of Technology), and this allowed data to be stored for later offline analysis.

Cerebral autoregulation was assessed by calculating the Mx as follows: values of ABP and FV were averaged over 5-s intervals to minimize the effect of pulse and respiratory waves. Two examples of such 5-s-averaged ABP data (n = 60 samples; ABP1, ABP2, ... ABP60) and FV (n = 60 samples; FV1, FV2, ... FV60) are shown in the upper part of Figure 1. Subsequently, Pearson’s correlation coefficient r1...60 was calculated among those 60 consecutive time-averaged samples of ABP1...60 and FV1...60 by using software developed in house (ICMR; M. Czosnyka). Two examples of such correlations between FV and ABP obtained from patients with preserved and impaired autoregulation are demonstrated in the lower part of Figure 1. Then Pearson’ correlation coefficient r was calculated again after shifting the time frame by 5 s, e.g., correlating ABP2??...61 with FV2...61, yielding r2...61. By further shifting the time frame, the correlation coefficients r3...62, r4...63, r5...64 ... r179...238, and r180...239 were calculated. Finally, the Mx (18) was obtained as the mean average of those correlation coefficients r1...60, r2...61, r3...62 ... r179...238, and r180...239. Calculation of the Sx was performed in the same way as for Mx, with the exception that systolic FV instead of mean FV was used for correlation with ABP.



View larger version (42K):
[in this window]
[in a new window]
  		Figure 1. Data from a patient with preserved autoregulation (left) and a patient with impaired autoregulation (right) are shown to illustrate the concept of Mx calculation. Synchronized time series (n = 60 samples; 5 min) of arterial blood pressure (ABP1, ABP2, ... ABP60) and mean flow velocity (FV1, FV2, ... FV60) as obtained from the middle cerebral artery are shown in the upper part. The lower graphs were obtained by plotting those time series of FV and ABP against each other (FV1 versus ABP1, FV2 versus ABP2, ... FV60 versus ABP60). Pearson’s correlation coefficient r1...60 was calculated between those 60 samples and is shown (r = 0.01, left; r = 0.87, right) with the linear regression line. A coefficient close to 0 (left) indicates preserved autoregulation, whereas positive values (right) suggest impaired autoregulation. Mx was calculated as mean average of the time-shifted Pearson’s correlation coefficients (e.g., r1...60, r2...61, r3...62, ..., r179...238, r180...239). MABP = mean arterial blood pressure.

 
Two datasets describe 18 patients who developed TCD-detected vasospasm: indices of cerebral autoregulation were compared during periods of no vasospasm and vasospasm in each patient and between the side of vasospasm and the contralateral side in each patient. Patient age, patient sex, and severity of SAH as expressed with the World Federation of Neurological Surgeons grading (23) are shown in Table 1; 13 patients underwent open surgery, and 2 patients were treated by coiling. Three patients were excluded from the first dataset because they showed vasospasm throughout the entire examination period, and there was no opportunity to derive indices during a nonvasospastic period. Whenever achievable, Mx and Sx data obtained before vasospasm were referred to as baseline, and this was the case in 11 of 15 patients. The remaining 4 patients showed vasospasm during the first examination; therefore, values measured after the resolution of vasospasm were considered as baseline. In the group in which the side of vasospasm was compared with the contralateral nonvasospastic side, 3 patients were excluded in whom vasospasm occurred bilaterally.


View this table:
[in this window]
[in a new window]
  		Table 1. Characteristics of Both Vasospasm Datasets: The Severity of Subarachnoid Hemorrhage Is Expressed by Using the World Federation of Neurological Surgeons (WFNS) Grading System (23)
 
With a duration of several days for both the baseline and vasospastic periods, several examinations, and, hence, Mx and Sx values, were obtained within both periods. For statistical analysis, data assessed within the same period were averaged in each patient, resulting in an averaged Mx and Sx value during the baseline and vasospastic periods. The same applied for ipsilateral versus contralateral comparisons, for which all Mx and Sx values obtained during vasospasm were averaged among the same side in a given patient. Thus, 22 and 28 datasets were pooled in the 15 patients of the groups in which baseline and vasospasm were compared, respectively. For comparison of the ipsilateral versus contralateral side of vasospasm, 28 datasets were pooled in 15 patients.

A paired Student’s t-test was performed after values were evaluated for normal distribution. Statistical significance was assumed at P < 0.05. Whenever applicable, data are shown as mean ± SD.


   Results
Top
 Abstract
 Introduction
 Methods
 Results
Discussion
 References
 
In the 15 patients who developed vasospasm, no difference was found in arterial blood gases between periods assessed at baseline and during vasospasm. In addition, arterial PCO2 was stable within patients during examination, excluding confounding effects of respiration on cerebrovascular resistance. However, the mean ABP was higher (P = 0.007) during vasospasm (100 ± 12.6 mm Hg) than at baseline (93.4 ± 14.5 mm Hg; Table 2). This difference may, in part, be a consequence of ABP support therapy.


View this table:
[in this window]
[in a new window]
  		Table 2. Arterial Blood Pressure, Blood Flow Velocity, and Cerebrovascular Reactivity in Comparison Between Baseline and Vasospasm on the Same Side and Between the Side of Vasospasm and the Contralateral Side
 
The Mx was increased (P = 0.021) during vasospasm (0.46 ± 0.32; n = 15) when compared with baseline conditions (0.21 ± 0.24; Table 2 and Fig. 2a). Two-way analysis of variance revealed that the observed difference in Mx was not due to the difference in mean ABP (P = 0.369). During vasospasm, Mx correlated with mean FV (r = 0.577; P = 0.025) and the Lindegaard ratio (r = 0.672; P = 0.006). Thus, for higher values of FV (and, hence, more cerebral vasospasm), there was a correspondingly more pronounced impairment in cerebral autoregulation.



View larger version (18K):
[in this window]
[in a new window]
  		Figure 2. Mean index (Mx) (a) and systolic index (Sx) (b) in comparison between baseline and vasospasm. During vasospasm, Mx (0.46 ± 0.32 vs 0.21 ± 0.24; P = 0.021) and Sx (0.22 ± 0.26 vs 0.05 ± 0.21; P = 0.03) were significantly higher than during baseline, indicating impaired cerebrovascular reactivity during vasospasm. Data are mean ± SD; n = 15 patients.

 
The Sx was also higher (P = 0.03) during vasospasm (0.22 ± 0.26; n = 15) when compared with baseline values (0.05 ± 0.21; Table 2 and Fig. 2b). Two-way analysis of variance indicated that this difference was due to vasospasm (P = 0.046) and not to the observed difference in mean ABP (P = 0.445). Mx correlated (P < 0.001) with Sx during baseline (r = 0.89) and vasospasm (r = 0.82).

Mx was higher (P = 0.006) on the side of vasospasm (0.44 ± 0.27; n = 15) than on the contralateral side (0.34 ± 0.29; Table 2 and Fig. 3a). Likewise, Sx on the side of vasospasm (0.24 ± 0.23; n = 15) was also increased (P = 0.044) as compared with the contralateral side (0.16 ± 0.25; Table 2 and Fig. 3b). There was a correlation (P < 0.001) between Mx and Sx on the side of vasospasm (r = 0.76) and on the contralateral side (r = 0.82).



View larger version (19K):
[in this window]
[in a new window]
  		Figure 3. Mean index (Mx) (a) and systolic index (Sx) (b) as obtained on the side of vasospasm as well the contralateral side. On the side of vasospasm, both Mx (0.44 ± 0.27 vs 0.34 ± 0.29; P = 0.006) and Sx (0.24 ± 0.23 vs 0.16 ± 0.25; P = 0.044) were significantly increased as compared with the contralateral side. Data are mean ± SD; n = 15 patients.

 

   Discussion
Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
References
 
Autoregulation assessment based on TCD methods has the major advantage of being continuous, inexpensive, and noninvasive. Calculations are based on the response of FV to slow and spontaneous changes in ABP and remove the need to manipulate ABP. Our technique to obtain Mx and Sx could be easily applied by other investigators. The technique requires daily TCD and ABP recordings plus the calculation of statistic variables, such as the mean average and Pearson’s correlation coefficient, which are described in detail elsewhere (24). The calculation of Pearson’s correlation coefficient itself demands less complicated computation than other methods that depend on fast Fourier transformation, such as the phase relationship analysis (25,26), the cross-correlation analysis (27), or the transfer function analysis (28). It also does not require a specific respiration regimen (25,26).

We assessed MCA vasospasm derived from TCD (29), a noninvasive technique with an excellent specificity (99%) and a high positive predictive value (97%) combined with a sensitivity of 67% and a negative predictive value of 78%, as revealed by a meta-analysis of 26 studies that compared TCD with cerebral angiography (15). A considerable number of our patients had a dense SAH and often remained unconscious during the first days or weeks after the insult. Hence, we did not rely on the occurrence of DIDs for vasospasm assessment, because it would have been unrecognized in a considerable number of cases. For assessment of cerebral autoregulation, we adopted a TCD-derived technique that calculates the indices Mx and Sx. In both, the assessment of vasospasm and autoregulation are based on the same TCD recordings. We may have been monitoring an inherent mathematical effect of accelerated FV. If this were the case, Mx and Sx would have remained unchanged while FV increased during vasospasm, because their calculation is independent of the absolute values of FV.

Mx and Sx characterize cerebral autoregulation, whereas FV itself provides information on the degree of vasospasm. Therefore, both techniques supplement but do not replace each other. In addition, differences that are of clinical relevance in the time course of both properties can be monitored. Using a distinct method of autoregulation assessment, Lam et al. (11) reported a difference in the incidence of DIDs depending on whether autoregulation impairment preceded or followed vasospasm.

Both Mx and Sx have been evaluated in healthy volunteers, in head injury (18,19,30–34), and in carotid artery occlusive disease (CAOD) (35). In Table 3, Mx and Sx values obtained in different studies and pathologies are summarized. Even though somewhat similar values were observed in different diseases, they should not be overvalued, because comparison is limited by the differences in the underlying pathophysiology. In healthy volunteers, an Mx of 0.21 (19) or 0.18 (36) and an Sx of -0.07 (19) were obtained; these are similar to the baseline values (Mx, 0.21; Sx, 0.05) assessed in our study. In head injury, an Mx value of 0.50 was measured during episodes of intracranial hypertension (37), and a value of 0.43 was measured in impaired autoregulation (33), which is held in contrast to an Mx of 0.46 during vasospasm in our investigation. Reinhard et al. (35) evaluated patients with CAOD and reported an Mx of 0.51 on the side of (90%–99%) carotid stenosis, compared with 0.44 on the side of vasospasm in our study. On the contralateral side, Mx was assessed as 0.30 in CAOD and 0.34 in our investigation. In our study, the Mx was approximately 0.2 higher than the Sx, which is comparable to the difference of 0.28 reported by Piechnik et al. (19).


View this table:
[in this window]
[in a new window]
  		Table 3. Summary of Mx and Sx Values Obtained in Different Pathologies
 
In head injury, the indices correlate with the transient hyperemic response test (38) and are prognostic for outcome (18). Furthermore, a good correlation between the rate of regulation as assessed by the cuff deflation test (16) and both Mx and Sx has been reported (19), supporting the hypothesis that Mx and Sx are measures of cerebral autoregulation.

Theoretically, both Mx and Sx describe the same phenomenon and hence correlate well with each other, even though Mx exhibits higher values than Sx. Piechnik et al. (19) reported a Pearson correlation coefficient of 0.89 and an Mx - Sx difference of 0.28, which is consistent with our data. However, Mx and Sx diverge when mean and systolic FV exhibit different behavior (39,40); this occurs particularly in situations of increased intracranial pressure (39,41) or decreased ABP (42). We calculated both Mx and Sx, because in SAH it is unknown which index is superior in terms of predictive power.

In comparison to other tests of cerebral autoregulation, such as the cuff deflation test (16) or the transient hyperemic response test (17), Mx and Sx assessment is less invasive because no artifical changes in ABP or carotid artery compression, respectively, are required. Furthermore, Mx and Sx provide continuous information on the status of autoregulation. However, with a minimal time for evaluation of approximately 20 minutes, calculation of Mx and Sx is more time consuming than cuff deflation or the hyperemic response test.

Mx and Sx have been evaluated under conditions in which significant changes in the diameter of the insonated vessels do not or rarely occur (e.g., in healthy volunteers and in head-injured patients). During vasospasm (characterized as narrowing of the major cerebral arteries), we found both Mx and Sx to be significantly increased as compared with baseline, which is an indication of impaired autoregulation. Impairment of autoregulation and cerebral vasospasm is anatomically distinct, because cerebral autoregulation occurs at the level of the arterioles (43,44) more distal to arteries affected by vasospasm as determined by TCD recordings. The higher the degree of TCD cerebral vasospasm, the more pronounced the impairment of autoregulation determined from the correlation among Mx, FV, and the Lindegaard ratio. This is in keeping with the observations of Voldby et al. (4), who described a close correlation between the degree of vasospasm assessed from angiography and the degree of autoregulatory impairment measured by CBF changes in arterial hypotension.

This is a preliminary study showing that autoregulation assessment by means of Mx and Sx calculation is applicable in SAH, a pathology—unlike previously studied ones—associated with diameter changes of the insonated vessels. Studies on the predictive value of Mx and Sx on outcome require more patients. The described technique may offer a tool to investigate the effect of triple-H therapy or of specific drugs on cerebral autoregulation and may guide the therapy of cerebral vasospasm. However, further evidence needs to be gathered before recommendations can be given regarding the therapy of vasospasm based on Mx and Sx assessment.

In conclusion, we observed significantly increased Mx and Sx values during—and on the side of—vasospasm and have attributed these to impairment of cerebral autoregulation and not to vasospasm alone. The higher the FV, the more impaired the cerebral autoregulation. Mx and Sx assessment supplements the sole determination of FV in SAH patients. It is a noninvasive and continuous method that provides information on autoregulation impairment, although it requires confirmation by further prospective studies in patients with SAH.


   Acknowledgments
 
Supported by Technology Foresight Challenge Award FCA234/95; G4200005 and Medical Research Council Programme Grant G9439390 (JDP).

The excellent secretarial assistance of Susan Hatley and Meryl Madakbas is gratefully acknowledged. Marek Czosnyka is on unpaid leave from Warsaw University of Technology, Poland.


   References
Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 References
 

  1. Lassen NA. Cerebral blood flow and oxygen consumption in man. Physiol Rev 1959; 39: 183–238.[Free Full Text]
  2. Strandgaard S, Paulson OB. Cerebral autoregulation. Stroke 1984; 15: 413–6.[Free Full Text]
  3. Yundt KD, Grubb RL, Diringer MN, Powers WJ. Autoregulatory vasodilatation of parenchymal vessels is impaired during cerebral vasospasm. J Cereb Blood Flow Metab 1998; 18: 419–24.[ISI][Medline]
  4. Voldby B, Enevoldsen EM, Jensen FT. Cerebrovascular reactivity in patients with ruptured intracranial aneurysms. J Neurosurg 1985; 62: 59–67.[ISI][Medline]
  5. Dernbach PD, Little JR, Jones SC, Ebrahim ZY. Altered cerebral autoregulation and CO2 reactivity after aneurysmal subarachnoid hemorrhage. Neurosurgery 1988; 22: 822–6.[ISI][Medline]
  6. Messeter K, Brandt L, Ljunggren B, et al. Prediction and prevention of delayed ischemic dysfunction after aneurysmal subarachnoid hemorrhage and early operation. Neurosurgery 1987; 20: 548–53.[ISI][Medline]
  7. Pickard JD, Matheson M, Patterson J, Wyper D. Prediction of late ischemic complications after cerebral aneurysm surgery by the intraoperative measurement of cerebral blood flow. J Neurosurg 1980; 53: 305–8.[ISI][Medline]
  8. Touho H, Ueda H. Disturbance of autoregulation in patients with ruptured intracranial aneurysms: mechanism of cortical and motor dysfunction. Surg Neurol 1994; 42: 57–64.[ISI][Medline]
  9. Fisher CM, Roberson GH, Ojemann RG. Cerebral vasospasm with ruptured saccular aneurysm: the clinical manifestations. Neurosurgery 1977; 1: 245–8.[Medline]
  10. Harders AG, Gilsbach JM. Time course of blood velocity changes related to vasospasm in the circle of Willis measured by transcranial Doppler ultrasound. J Neurosurg 1987; 66: 718–28.[ISI][Medline]
  11. Lam JM, Smielewski P, Czosnyka M, et al. Predicting delayed ischemic deficits after aneurysmal subarachnoid hemorrhage using a transient hyperemic response test of cerebral autoregulation. Neurosurgery 2000; 47: 819–26.[ISI][Medline]
  12. Rätsep T, Asser T. Cerebral hemodynamic impairment after aneurysmal subarachnoid hemorrhage as evaluated using transcranial Doppler ultrasonography: relationship to delayed cerebral ischemia and clinical outcome. J Neurosurg 2001; 95: 393–401.[ISI][Medline]
  13. Lindegaard KF, Nornes H, Bakke SJ, et al. Cerebral vasospasm diagnosis by means of angiography and blood velocity measurements. Acta Neurochir (Wien) 1989; 100: 12–24.[Medline]
  14. Clyde BL, Resnick DK, Yonas H, et al. 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.[ISI][Medline]
  15. Lysakowski C, Walder B, Costanza MC, Tramer MR. Transcranial Doppler versus angiography in patients with vasospasm due to a ruptured cerebral aneurysm: a systematic review. Stroke 2001; 32: 2292–8.[Abstract/Free Full Text]
  16. Aaslid R, Lindegaard KF, Sorteberg W, Nornes H. Cerebral autoregulation dynamics in humans. Stroke 1989; 20: 45–52.[Abstract/Free Full Text]
  17. Giller CA. A bedside test for cerebral autoregulation using transcranial Doppler ultrasound. Acta Neurochir (Wien) 1991; 108: 7–14.[Medline]
  18. Czosnyka M, Smielewski P, Kirkpatrick P, et al. Monitoring of cerebral autoregulation in head-injured patients. Stroke 1996; 27: 1829–34.[Abstract/Free Full Text]
  19. Piechnik SK, Yang X, Czosnyka M, et al. The continuous assessment of cerebrovascular reactivity: a validation of the method in healthy volunteers. Anesth Analg 1999; 89: 944–9.[Abstract/Free Full Text]
  20. Hutchinson PJ, Seeley HM, Kirkpatrick PJ. Factors implicated in deaths from subarachnoid haemorrhage: are they avoidable? Br J Neurosurg 1998; 12: 37–40.[ISI][Medline]
  21. Whitfield PC, Moss H, O’Hare D, et al. An audit of aneurysmal subarachnoid haemorrhage: earlier resuscitation and surgery reduces inpatient stay and deaths from rebleeding. J Neurol Neurosurg Psychiatry 1996; 60: 301–6.[Abstract]
  22. Kassel NF, Peerless SJ, Durward QJ, et al. Treatment of ischemic deficits from vasospasm with intravascular volume expansion and induced arterial hypertension. Neurosurgery 1982; 11: 337–43.[ISI][Medline]
  23. Drake CG. Report of World Federation of Neurological Surgeons Committee on a universal subarachnoid hemorrhage grading scale. J Neurosurg 1988; 68: 985–6.[ISI][Medline]
  24. Campbell MJ, Machin D. Appendix 1: techniques. In: Medical statistics: a commonsense approach. Chichester, UK: Wiley, 1999: 165.
  25. Diehl RR, Linden D, Lucke D, Berlit P. Phase relationship between cerebral blood flow velocity and blood pressure: a clinical test of autoregulation. Stroke 1995; 26: 1801–4.[Abstract/Free Full Text]
  26. Lang EW, Diehl RR, Mehdorn HM. Cerebral autoregulation testing after aneurysmal subarachnoid hemorrhage: the phase relationship between arterial blood pressure and cerebral blood flow velocity. Crit Care Med 2001; 29: 158–63.[ISI][Medline]
  27. Steinmeier R, Bauhuf C, Hubner U, et al. Slow rhythmic oscillations of blood pressure, intracranial pressure, microcirculation, and cerebral oxygenation: dynamic interrelation and time course in humans. Stroke 1996; 27: 2236–43.[Abstract/Free Full Text]
  28. Zhang R, Zuckerman JH, Giller CA, Levine BD. Transfer function analysis of dynamic cerebral autoregulation in humans. Am J Physiol 1998; 274: H233–41.[ISI][Medline]
  29. Lindegaard KF. The role of transcranial Doppler in the management of patients with subarachnoid haemorrhage: a review. Acta Neurochir Suppl (Wien) 1999; 72: 59–71.[Medline]
  30. Czosnyka M, Smielewski P, Piechnik S, et al. Continuous assessment of cerebral autoregulation: clinical verification of the method in head injured patients. Acta Neurochir Suppl 2000; 76: 483–4.[Medline]
  31. Czosnyka M, Smielewski P, Piechnik S, et al. Cerebral autoregulation following head injury. J Neurosurg 2001; 95: 756–63.[ISI][Medline]
  32. Czosnyka M, Smielewski P, Kirkpatrick P, et al. Continuous assessment of the cerebral vasomotor reactivity in head injury. Neurosurgery 1997; 41: 11–9.[ISI][Medline]
  33. Lang EW, Lagopoulos J, Griffith J, et al. Cerebral vasomotor reactivity testing in head injury: the link between pressure and flow. J Neurol Neurosurg Psychiatry 2003; 74: 1053–9.[Abstract/Free Full Text]
  34. Lang EW, Lagopoulos J, Griffith J, et al. Noninvasive cerebrovascular autoregulation assessment in traumatic brain injury: validation and utility. J Neurotrauma 2003; 20: 69–75.[ISI][Medline]
  35. Reinhard M, Roth M, Muller T, et al. Cerebral autoregulation in carotid artery occlusive disease assessed from spontaneous blood pressure fluctuations by the correlation coefficient index. Stroke 2003; 34: 2138–44.[Abstract/Free Full Text]
  36. Schmidt EA, Piechnik SK, Smielewski P, et al. Symmetry of cerebral hemodynamic indices derived from bilateral transcranial Doppler. J Neuroimaging 2003; 13: 248–54.[Medline]
  37. Czosnyka M, Smielewski P, Piechnik S, et al. Hemodynamic characterisation of intracranial pressure plateau waves in head-injured patients. J Neurosurg 1999; 91: 11–9.[ISI][Medline]
  38. Smielewski P, Czosnyka M, Kirkpatrick P, Pickard JD. Evaluation of the transient hyperemic response test in head-injured patients. J Neurosurg 1997; 86: 773–8.[ISI][Medline]
  39. Czosnyka M, Guazzo E, Iyer V, et al. Testing of cerebral autoregulation in head injury by waveform analysis of blood flow velocity and cerebral perfusion pressure. Acta Neurochir Suppl (Wien) 1994; 60: 468–71.[Medline]
  40. Czosnyka M, Richards H, Kirkpatrick P, Pickard J. Assessment of cerebral autoregulation with ultrasound and laser Doppler wave forms: an experimental study in anesthetized rabbits. Neurosurgery 1994; 35: 287–92;discussion 292–3.
  41. Ungersbock K, Tenckhoff D, Heimann A, et al. Transcranial Doppler and cortical microcirculation at increased intracranial pressure and during the Cushing response: an experimental study on rabbits. Neurosurgery 1995; 36: 147–56;discussion 156–7.
  42. Nelson RJ, Czosnyka M, Pickard JD, et al. Experimental aspects of cerebrospinal hemodynamics: the relationship between blood flow velocity waveform and cerebral autoregulation. Neurosurgery 1992; 31: 705–9;discussion 709–10.
  43. Kontos HA, Wei EP, Navari RM, et al. Responses of cerebral arteries and arterioles to acute hypotension and hypertension. Am J Physiol 1978; 234: H371–83.[ISI][Medline]
  44. MacKenzie ET, Farrar JK, Fitch W, et al. Effects of hemorrhagic hypotension on the cerebral circulation. I. Cerebral blood flow and pial arteriolar caliber. Stroke 1979; 10: 711–8.[Free Full Text]
Accepted for publication November 13, 2003.




This article has been cited by other articles:


Home page
 Anesth. Analg.Home page
M. Czosnyka, P. Smielewski, A. Lavinio, J. D. Pickard, and R. Panerai
An Assessment of Dynamic Autoregulation from Spontaneous Fluctuations of Cerebral Blood Flow Velocity: A Comparison of Two Models, Index of Autoregulation and Mean Flow Index
Anesth. Analg., January 1, 2008; 106(1): 234 - 239.
[Abstract] [Full Text] [PDF]

Home page
 StrokeHome page
M. Jaeger, M. U. Schuhmann, M. Soehle, C. Nagel, and J. Meixensberger
Continuous Monitoring of Cerebrovascular Autoregulation After Subarachnoid Hemorrhage by Brain Tissue Oxygen Pressure Reactivity and Its Relation to Delayed Cerebral Infarction
Stroke, March 1, 2007; 38(3): 981 - 986.
[Abstract] [Full Text] [PDF]

Home page
 Br J AnaesthHome page
L. A. Steiner and P. J. D. Andrews
Monitoring the injured brain: ICP and CBF
Br. J. Anaesth., July 1, 2006; 97(1): 26 - 38.
[Abstract] [Full Text] [PDF]

Home page
 NeurologyHome page
G. K.C. Wong, S. C.P. Ng, W. W.S. Poon, J. A. Frontera, and R. S. Marshall
Cerebrovascular reactivity and vasospasm after subarachnoid hemorrhage: A pilot study
Neurology, June 13, 2006; 66(11): 1787 - 1787.
[Full Text] [PDF]

Home page
 NeurologyHome page
J. A. Frontera, T. Rundek, J. M. Schmidt, J. Claassen, A. Parra, K. E. Wartenberg, R. E. Temes, S. A. Mayer, J. P. Mohr, and R. S. Marshall
Cerebrovascular reactivity and vasospasm after subarachnoid hemorrhage: A pilot study
Neurology, March 14, 2006; 66(5): 727 - 729.
[Abstract] [Full Text] [PDF]

Home page
 Am. J. Neuroradiol.Home page
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]

Home page
 StrokeHome page
M. Reinhard, M. Roth, B. Guschlbauer, A. Harloff, J. Timmer, M. Czosnyka, and A. Hetzel
Dynamic Cerebral Autoregulation in Acute Ischemic Stroke Assessed From Spontaneous Blood Pressure Fluctuations
Stroke, August 1, 2005; 36(8): 1684 - 1689.
[Abstract] [Full Text] [PDF]

This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Email this article to a colleague
Right arrow Similar articles in this journal
Right arrow Similar articles in ISI Web of Science
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via ISI Web of Science (16)
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Soehle, M.
Right arrow Articles by Kirkpatrick, P. J.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Soehle, M.
Right arrow Articles by Kirkpatrick, P. J.
Related Collections
Right arrow Resuscitation
Right arrow Neuroanesthesia
Right arrow Critical Care

Lippincott, Williams & Wilkins Anesthesia & Analgesia® is published for the International Anesthesia Research Society® by Lippincott Williams & Wilkins with the assistance of Stanford University Libraries' HighWire Press®. Copyright 2006 by the International Anesthesia Research Society. Online ISSN: 1526-7598   Print ISSN: 0003-2999 HighWire Press