Donate Help Contact The AHA Sign In Home
American Heart Association
Stroke
Search: search_blue_button Advanced Search
« Previous Article | Table of Contents | Next Article »
Stroke. 2001;32:2005-2011
doi: 10.1161/hs0901.094622
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
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrow Request Permissions
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Torbey, M. T.
Right arrow Articles by Razumovsky, A. Y.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Torbey, M. T.
Right arrow Articles by Razumovsky, A. Y.
Related Collections
Right arrow Aneurysm, AVM, hematoma
Right arrow Brain Circulation and Metabolism
Right arrow Cerebral Aneurysm, AVM, & Subarachnoid hemorrhage
Right arrow Angiography
Right arrow Doppler ultrasound, Transcranial Doppler etc.

(Stroke. 2001;32:2005.)
© 2001 American Heart Association, Inc.

Original Contributions

Effect of Age on Cerebral Blood Flow Velocity and Incidence of Vasospasm After Aneurysmal Subarachnoid Hemorrhage

Michel T. Torbey, MD, MPH; Till-Karsten Hauser, MD; Anish Bhardwaj, MD; Michael A. Williams, MD; John A. Ulatowski, MD, PhD; Marek A. Mirski, MD, PhD Alexander Y. Razumovsky, PhD

From the Neurosciences Critical Care Division (M.T.T., T.-K.H., A.B., M.A.W., J.A.U., M.A.M., A.Y.R.), Johns Hopkins University, School of Medicine, Baltimore, Md.

Correspondence to Michel T. Torbey, MD, MPH, Neurosciences Critical Care Division, Johns Hopkins University, School of Medicine, 600 N Wolfe St, Meyer 8-140, Baltimore, MD 21287. E-mail mitorbey{at}jhmi.edu


*    Abstract
up arrowTop
 *Abstract
down arrowIntroduction
 down arrowSubjects and Methods
 down arrowResults
 down arrowDiscussion
 down arrowReferences
 
Background and Purpose—— Current transcranial Doppler criteria for vasospasm after aneurysmal subarachnoid hemorrhage are not age specific. We analyzed the effect of age on cerebral blood flow velocity changes after subarachnoid hemorrhage and constructed an age-adjusted predictive model of cerebral blood flow velocity in subarachnoid hemorrhage patients.

Methods—— We identified patients with aneurysmal subarachnoid hemorrhage admitted between 1991 and 1999 with a prospective transcranial Doppler database. Eighty-one patients, with complete medical records and transcranial Doppler examinations of the vessels of interest, were included. Patients were subdivided into 2 groups by age: younger, <68 years of age (n=47) and older, >=68 years of age (n=34). Maximum mean flow velocity and incidence of symptomatic vasospasm were reported. Linear and nonlinear regression analyses were performed.

Results—— Middle cerebral artery and internal carotid artery mean flow velocity were lower in older patients (median 76 versus 114 cm/s and 76 versus 126 cm/s, respectively; P<0.003). Incidence of symptomatic vasospasm was lower in older patients (44% versus 66%; P=0.05). Older patients developed symptomatic vasospasm at lower middle cerebral artery (median 57 versus 103 cm/s; P=0.04) and internal carotid artery (median 54 versus 81 cm/s, P=0.02) mean flow velocity. Relationship between middle cerebral artery and internal carotid artery mean flow velocity and age was quadratic (ANOVA, P<0.0001).

Conclusions—— Older patients have a lower incidence of symptomatic vasospasm, and such vasospasm develops at lower cerebral blood flow velocity than younger patients. A quadratic relationship was found between age and cerebral blood flow velocity. This model could be used to create an age-adjusted nomogram that might improve diagnostic capabilities of transcranial Doppler.


Key Words: aging • cerebral angiography • subarachnoid hemorrhage • ultrasonography, Doppler, transcranial • vasospasm


*    Introduction
up arrowTop
 up arrowAbstract
 *Introduction
down arrowSubjects and Methods
 down arrowResults
 down arrowDiscussion
 down arrowReferences
 
Cerebral angiography remains the gold standard for diagnosis of cerebral vasospasm (VSP). Since the introduction of transcranial Doppler (TCD),1 various authors2,3 have reported on its usefulness as a noninvasive measurement of cerebral blood flow velocity (CBFV) within the circle of Willis for the evaluation of VSP in patients after aneurysmal subarachnoid hemorrhage (SAH). Currently patients are reported to have transcranial Doppler-defined VSP if CBFV is above a threshold velocity. This threshold varies among studies, even those pertaining to the same vessel.4,5 Sensitivity of TCD for detection of angiographic VSP in the middle cerebral artery (MCA) ranges from 39% to 85%.4,6

With advancing age, a decrease in CBFV and a concomitant increase in indexes of peripheral resistance are found in all vessels. These findings are more pronounced in subjects of age >40 years.5,7,8 Current criteria for TCD-defined VSP are based predominantly on CBFV in younger patients without adjusting for factors such as age and days after SAH, which potentially limits their predictive power in older patients. Various studies have mentioned the effect of age on CBFV after SAH.9–12 Only 1 study12 described a negative linear correlation between measured MCA maximum mean flow velocity (MMFV) and age (r=-0.525, P<0.01) in SAH patients. Data-driven age-adjusted criteria may improve diagnostic capabilities of TCD.

The aim of this retrospective analysis is to determine the effect of age after SAH on (1) time profile of changes in TCD measured CBFV and (2) incidence of VSP. A secondary aim is to construct an age-adjusted predictive model of CBFV in SAH.


*    Subjects and Methods
up arrowTop
 up arrowAbstract
 up arrowIntroduction
 *Subjects and Methods
down arrowResults
 down arrowDiscussion
 down arrowReferences
 
Patients
We evaluated retrospectively all patients admitted to the Neurosciences Critical Care Unit with the diagnosis of aneurysmal SAH between 1991 and 1999. Patients were identified using a prospective TCD database maintained in the Neurosciences Critical Care Unit. Patients with traumatic and nonaneurysmal SAH were excluded. We reviewed medical records of all patients and collated data regarding demographic characteristics, clinical presentation, location of aneurysm, Fisher grade,13 Hunt and Hess score,14 and symptomatic VSP. Onset of SAH was presumed to be at headache onset.

Symptomatic VSP
Diagnosis of symptomatic VSP was based on onset of new focal or global neurological deficit not explained by hydrocephalus, hemorrhage, surgical complications, fever, infections, or metabolic abnormalities. Retrospective diagnosis was not attempted and was considered only (1) if made during the patient’s hospital stay and (2) if symptoms resolved after either hypervolemic-hypertensive or endovascular therapy.

TCD Ultrasonography
MFV of the anterior circulation vessels was recorded in centimeters per second by a 2-MHz transducer (CDS, Medasonics; Intraview, RIMED) by use of a transtemporal approach. All vessels were insonated according to the method described by Aaslid et al.1 Because it was shown that most patients with anterior circulation aneurysms who develop VSP have involvement of the basal arteries15 and absence of accurate interdependence between VSP symptoms and actual arterial territory involved,16,17 our analysis was restricted to the M1 segment of the MCA and the C1 segment of the internal carotid artery (ICA) insonation. In addition, insonation of the MCA and of ICA segment C1 is more accurate and reproducible4,18 than of the ACA.2,5 We report MFV of the right M1 and left ICA segment C1. If the patient developed focal symptoms, we reported MFV of the side correlating with the symptoms.

Lindegaard ratio also was calculated to differentiate between hyperemia and VSP.19 Patients were reported to have TCD VSP when mean CBFV was >=100 cm/s20 and Lindegaard ratio was >3.19 We reported the following: (1) Gosling pulsatility index (PI)21 and maximum MFV (MMFV); (2) baseline MFV defined as velocities recorded on the first 2 days of admission; (3) percentage change in MFV, defined as the difference between MMFV and baseline MFV divided by the baseline MFV; and (4) proportion of patients with >=50-cm/s increase in MFV per 24 hours.22 Length of the period between recording MMFV and diagnosis of symptomatic VSP was calculated.

Cerebral Angiography
Cerebral angiograms obtained during the patient’s hospital stay were interpreted by a neuroradiologist and compared with those performed on admission. We defined angiographic VSP as a vessel lumen diameter reduction >=51% because of the strong correlation between >50% reduction in vessel diameter and ischemic reduction in regional cerebral blood flow.23

Statistical Analysis
We analyzed data using SPSS 10.0 statistical software package (SPSS Inc). Patient characteristics were summarized with frequency distributions, means, SEMs, median, range, and percentiles as appropriate. Pearson {chi}2 was calculated for 2x2 tables. Fisher’s Exact Test was computed when tables had cells with an expected frequency of <5. A matrix scatterplot was created to examine the data and determine the best age to dichotomize patients. Nonparametric Mann-Whitney or Wilcoxon rank sum tests were used to compare groups. Linear and nonlinear regression analyses were performed to detect a correlation between age and CBFV. For each model, regression coefficients, R2, SEE, predicted values, and residuals were calculated. Contingency tables (2x2) were constructed to calculate sensitivity and specificity of TCD for detecting symptomatic VSP. A P value <0.05 was considered significant.


*    Results
up arrowTop
 up arrowAbstract
 up arrowIntroduction
 up arrowSubjects and Methods
 *Results
down arrowDiscussion
 down arrowReferences
 
Demographic Data
We identified 311 patients with SAH. Of those, 25 had a traumatic SAH and 83 had a nonaneurysmal SAH. Only 81 of 203 (40%) had complete medical records and TCD examinations that included the vessels of interest (619 TCD studies were reviewed). Median patient age was 62 years (range 21 to 84 years); 75% were women. On presentation to the hospital, 41% had mild headache (Hunt and Hess score 1) and 4% were comatose (Hunt and Hess score 5). Forty-two percent had diffuse SAH on CT scan of the head (Fisher grade 2). Most of the aneurysms were in the anterior circulation (94%), of which 44% were anterior communicating artery aneurysms. Mean time to surgical or endovascular intervention was 2 days. A total of 90% (73 of 81) of the patients underwent clipping, and 8% (6 of 81) underwent endovascular coiling. One patient had no intervention, and both clipping and coiling was performed on another.

Scatterplot of CBFV by age (Figure 1) demonstrated a sharper decline in CBFV for patients >=68 years of age. This finding led us to dichotomize patients into 2 age groups: younger (n=47), defined as age <68 years; and older, (n=34) defined as age >=68 years. No difference was seen between groups in relation to race, sex, Glasgow coma scale score, Hunt and Hess score and Fisher grade, aneurysm location, or type of vascular intervention performed.



View larger version (24K):
[in this window]
[in a new window]
  		Figure 1. Scatterplot of all MCA MFV recorded during patient hospital stay, which delineates a sharper decline in velocity for patients of age >=68 years. This finding led to dichotomization of patients into either a younger age group defined as age <68 years or an older age group defined as age >=68 years.

Effect of Age on CBFV and PI
Older patients had a significantly lower baseline MFV and MMFV in both MCA and ICA. Table 1 illustrates the effect of age on MCA and ICA MFV. The number of days to MMFV was not significantly different between the 2 age groups. A total of 50% of patients reached MMFV on day 7 of SAH. We found a similar percentage change from baseline to MMFV in older and younger patients. We noted a trend toward a faster rise in MFV in younger patients. A total of 30% of younger patients versus 15% of older patients had MFV rise >=50 cm/s per 24 hours (P=0.07). We found a significantly higher proportion of younger patients with MMFV >160 cm/s (P=0.05). Conversely, a higher proportion of older patients have MMFV <80 cm/s (P=0.05).


View this table:
[in this window]
[in a new window]
  		Table 1. Effect of Age on MCA and ICA Velocity

We found a significant increase in PI with advancing age. The MCA PI was 0.88 in younger and 1.09 in older patients (P<0.0005). Similarly, ICA PI was 0.86 in younger and 1.2 in older patients (P<0.0005).

Effect of Age on Diagnosis of VSP
The most common presentation of symptomatic VSP in our study was confusion (66.7% in older and 55.6% in younger patients). Focal symptoms were found in 13.3% of older patients and 13% of younger patients. No significant difference was found in the presenting symptoms of VSP between older and younger patients. Older patients had a lower incidence and earlier onset of symptomatic VSP (Table 2) and developed symptomatic VSP at lower CBFV. Median time to symptomatic VSP was 5 and 7 days after SAH in older and younger patients, respectively (P=0.06). MMFV preceded diagnosis of symptomatic VSP by 2 days in older and 1 day in younger patients (P=0.7). A Kaplan-Meier curve (Figure 2) demonstrated that none of the older patients developed symptomatic VSP after day 10 following SAH, whereas younger patients continued to develop symptomatic VSP until day 16.


View this table:
[in this window]
[in a new window]
  		Table 2. Effect of Age on VSP



View larger version (18K):
[in this window]
[in a new window]
  		Figure 2. Kaplan-Meier onset of VSP curve for patients with aneurysmal SAH. — indicates patients of age <68 years; ----, patients of age >=68 years.

Incidence of TCD-defined VSP was significantly higher in younger (42%) versus older (23%) patients (P<0.0001). Only 36 (44%) patients had cerebral angiograms performed as follow up or for possible VSP. Incidence of radiological VSP was 74% in younger and 47% in older patients (P=0.1). Twenty-eight patients (35%) underwent TCD and angiographic studies on the same day symptomatic VSP was suspected. The incidence of angiographically confirmed TCD VSP was 53% in younger patients and 33% in older patients (P=0.2).

Effect of Age on TCD Sensitivity and Specificity: Sensitivity and Specificity of TCD to Detect Symptomatic VSP Varied With Age
For the MCA, TCD sensitivity was higher in younger (60%) versus older (38%) patients. Conversely, specificity was higher in older (77%) compared with younger (58%) patients. For the ICA, TCD sensitivity was higher in younger (42.9%) compared with older (20%) patients; specificity was not different between groups (80%).

Regression Analysis
To analyze the age-related decline of MFV in the MCA and ICA, linear and quadratic regression models were constructed. Models are described in formulas 1 through 4. We entered the following variables into the model: (1) age, (2) SAH day (PSAHD), (3) SAH day category (SAHDC), and (4) clinical spasm (CSPASM). The variable SAHDC was introduced into the model to emphasize the change in CBFV seen late in the course of SAH. SAHDC was defined as 0 if SAH day was <=12 and PSAHD-12 if SAH day was >12. CSPASM was defined as 0 when VSP was absent and "1" when VSP was present.

The MCA linear model equation is as follows.


The MCA quadratic model equation is as follows.


The ICA linear model equation is as follows.


The ICA quadratic model equation is as follows.


The quadratic model fit the data best for both MCA (R2=0.14, P<0.0001) and ICA (R2=0.093, P<0.0001; Figure 3). In the MCA, most of the decline in MFV occurred in older patients. The slope of this MFV decline is 9-fold in patients of age >=68 versus <68 years. As for the ICA, most of the decline was in the younger patients. The slope of the decline is 8-fold in patients of age <68 versus >=68 years.



View larger version (17K):
[in this window]
[in a new window]
  		Figure 3. Plot of quadratic model for SAH patients at days 9 and 10 after SAH without evidence of symptomatic VSP. A, In MCA, slope of MFV decline is 9-fold in patients >=68 vs <68 years of age. B, In ICA, slope of decline is 8-fold in patients <68 vs >=68 years of age.


*    Discussion
up arrowTop
 up arrowAbstract
 up arrowIntroduction
 up arrowSubjects and Methods
 up arrowResults
 *Discussion
down arrowReferences
 
Results of the present study provide new insights into the effect of aging on CBFV in patients after aneurysmal SAH. First, we have shown that older SAH patients have lower MMFV and baseline MFV. Second, older patients developed symptomatic VSP at normal-range MFV. Third, older patients may have a shorter high-risk period to development of symptomatic VSP. Finally, the age-related decline in CBFV was not linear but instead was quadratic, and the slope of this decline varied with the type of vessel insonated.

Effect of age on CBFV and PI
Age-related decline in CBFV has been reported in previous studies.9–11,24 Although these studies clearly demonstrated an inverse relationship between age and CBFV, a small sample size of patients >60 years of age did not allow the authors to perform multivariate logistic regression analysis and adjust for factors such as SAH day and presence of symptomatic VSP. The decline in CBFV with age may be associated with certain changes in cerebrovascular hemodynamics such as (1) decreased CBF or metabolic demands,25,26 (2) vessel-size changes,27 and (3) lower cardiac output.28,29

Aging is associated with a 20% to 30% decrease in CBF in healthy individuals between the ages of 20 and 80 years.25,26 Several authors have examined the relationship between relative changes in CBFV and changes in CBF in normal subjects.30,31 A linear relationship has been reported between CBFV and the mean cerebral transit time of Tc30 and between percentage change in MCA MFV and percentage change in CBF.31 Although the linear relationships found in these studies do not meet the criterion of having a slope of 1 and a y intercept of 0, they suggest that changes in CBFV reflect changes in CBF.30

Aging is also associated with dilatation of major extracranial arteries and reduction of flow within parenchymal vessels.27 Kusunoki et al27 demonstrated poor visibility of the intracerebral ICA and M1 segment of the MCA on magnetic resonance angiography secondary to progressive kinking, elongation, and stenosis with advancing age.

Several authors have examined the effect of aging on the cardiovascular system.28,29 These studies demonstrate an age-related prolongation of isovolumic cardiac relaxation,28 which results in reduced efficacy of early ventricular diastolic filling and an age-related drop in cardiac index.29

In the present study, along with a decrease in CBFV with advancing age comes an increase in PI. This may be secondary to age-related stiffening of the arteries, which often dilate and become tortuous.32 The more-elastic (younger) vessels damp the pulse and pressure wave more effectively than do stiff, aged vessels.33 Thus, aging increases the systolic-diastolic pressure ratio, which results in an increase in PI.

Effect of Age on VSP
VSP remains a major complication associated with aneurysmal SAH that results in delayed ischemic deficits in 2% to 24% of all cases.34,35 Our symptomatic VSP incidence was higher compared with Boecher-Schwarz et al.12 They reported a 23% incidence of VSP in patients <55 and 0% in patients >55 years of age. Higher incidence of symptomatic VSP in our series is probably secondary to a higher degree of severity of SAH. Of our patients, 42% had a Hunt and Hess score >=3 on admission, compared with 25% in the Boecher-Schwarz series.

Incidence of TCD-defined VSP was higher in our series compared with the series of Sloan.36 Sloan demonstrated that TCD VSP occurred in 28% of patients >=55 and 13% of patients >=65 years of age. Our higher incidence may be related to a lower CBFV cutoff (>=100 cm/s) compared with the cutoff used by Sloan (120 cm/s).36

Our incidence of angiographic VSP was comparable to published data.37,38 In 1 study,37 the reported incidence of angiographic VSP was 75% in patients <60 and 45% in patients >=60 years of age. Another study38 reported angiographic VSP in 44% of patients <65 and 23% of patients >=65 years of age.

The lower incidence of VSP in older patients may be secondary to the age-related increase in atherosclerosis, which results in impairment of contractility and elasticity of the muscle wall of small arteries and arterioles.39,40 Postmortem histological studies41 have demonstrated that aging is accompanied by the appearance of collagen fibers in major intracranial arteries, which is usually associated with loss of elasticity of the vessel wall. Dewey et al42 described a collapse of downstream vasculature as diastolic pressure falls below the critical closing pressure of cerebral blood vessels. He reported that younger patients, due to more compliant and collapsible vessels, may have greater diminution in CBF as cerebral perfusion pressure reaches a critical closing pressure.42 Hence, elderly subjects with stiffer vessels may be able to maintain small-vessel patency at similar pressures.

In our series, older patients not only had a low CBFV, but also developed symptomatic VSP at normal-range CBFV. For older patients with SAH (whose resting CBF is lowest), the margin between adequate CBF and the ischemic threshold may become especially narrow.43 Accordingly, we think that older patients would be susceptible to ischemic neurological deficits induced by small changes in vessel caliber. This discordance between TCD measured CBFV and CBF in older patients with SAH may be due to disturbances in cerebral autoregulation.44

The high-risk period to development of symptomatic VSP usually extends from days 4 to 21, with a peak incidence around day 14 after SAH.34 We found similar risk period in our younger patients, in whom the risk of symptomatic VSP was present until day 16 of SAH. Surprisingly, older patients had a shorter risk period. None of these patients developed symptomatic VSP after day 10 of SAH. We do not have a clear explanation as to the difference in risk-period duration. However, because the diagnosis of symptomatic VSP was not made prospectively, this finding will need to be tested prospectively before therapeutic inferences can be made.

Effect of Age on TCD Sensitivity and Specificity
High specificity and low sensitivity for detecting symptomatic VSP characterize TCD data after SAH in the present study. Specificity and sensitivity in MCA and ICA varied from 85% to 100% and from 25% to 94%, respectively, in the studies of Grolimund et al5 and Sloan et al.6 Neither of these studies have taken into account the effect of age on CBFV. Sloan36 demonstrated that lowering the criterion for diagnosis of TCD VSP from 110 to 80 cm/s improved TCD specificity. In the present study, the high specificity and low sensitivity of TCD in elderly patients may be secondary to lower incidence of VSP and higher false-positive rate in those patients. The false-positive rate in older patients was 40% compared with 27% in younger patients.

Regression Model
Boecher-Schwarz et al12 was the first to describe a negative linear correlation between the measured MCA MMFV and age (r=-0.525, P<0.01) in SAH patients. In this linear model, the authors did not adjust for days of SAH when CFBV was measured and for presence of symptomatic VSP on that day. To our knowledge, the present study is the first to report an effect of age on CBFV using nonlinear regression analysis and adjusting for factors such as days after SAH and presence or absence of symptomatic VSP.

The slope of the age-related decline in CBFV varied with the vessel insonated and age group of the patients. Why the slopes of the MCA and ICA were not concordant is unclear. In the ICA, most patient MFV decline occurred at a younger age. In the MCA, the major decline in MFV occurred in older patients (>=68 years). This pattern of CBFV changes appears to fit a quadratic model better than a linear model, as our analysis demonstrated. This predictive model could be extrapolated to create an age-adjusted nomogram for CBFV to improve sensitivity and specificity of TCD.

Finally, the present study has a few limitations. Our quadratic model is limited by the retrospective nature of some of the variables included in the analysis. The diagnosis of symptomatic VSP, although it was established through accurate chart review, is retrospective and could overestimate the incidence of VSP in the study. This diagnosis also could affect interpretation of the accuracy parameters of CBFV measured by TCD.

Despite these limitations, we were able to demonstrate in the present study the important nonlinear effect of age on CBFV in patients after SAH. The present study is the first to show that older patients develop symptomatic VSP at normal-range CBFV, which thus limits the application of TCD in the management of elderly SAH patients. An age-adjusted CBFV nomogram in SAH may improve accuracy of TCD in olderpatients.


*    Acknowledgments
 
Dr Torbey is supported in part by a postdoctoral fellowship award from the Mid-Atlantic affiliate of the American Heart Association. Dr Bhardwaj is supported in part by an Established Investigator Award from the American Heart Association.


*    Footnotes
 
Presented in part at the 26th American Heart Association International Stroke Conference, Fort Lauderdale, Fla, February 14–16, 2001, and published in abstract form (Stroke. 2001;32:340).

Received February 27, 2001; revision received May 16, 2001; accepted May 29, 2001.


*    References
up arrowTop
 up arrowAbstract
 up arrowIntroduction
 up arrowSubjects and Methods
 up arrowResults
 up arrowDiscussion
 *References
 

  1. Aaslid R, Markwalder TM, Nornes H. Noninvasive transcranial Doppler ultrasound recording of flow velocity in basal cerebral arteries. J Neurosurg. 1982; 57: 769–774.[Medline] [Order article via Infotrieve]
  2. Wozniak MA, Sloan MA, Rothman MI, Burch CM, Rigamonti D, Permutt T, Numaguchi Y. Detection of vasospasm by transcranial Doppler sonography: the challenges of the anterior and posterior cerebral arteries. J Neuroimaging. 1996; 6: 87–93.[Medline] [Order article via Infotrieve]
  3. Vora YY, Suarez-Almazor M, Steinke DE, Martin ML, Findlay JM. Role of transcranial Doppler monitoring in the diagnosis of cerebral vasospasm after subarachnoid hemorrhage [published discussion appears in Neurosurgery. 1999;44:1247–1248]. Neurosurgery. 1999; 44: 1237–1247.[Medline] [Order article via Infotrieve]
  4. Burch CM, Wozniak MA, Sloan MA, Rothman MI, Rigamonti D, Permutt T, Numaguchi Y. Detection of intracranial internal carotid artery and middle cerebral artery vasospasm following subarachnoid hemorrhage. J Neuroimaging. 1996; 6: 8–15.[Medline] [Order article via Infotrieve]
  5. Grolimund P, Seiler RW, Aaslid R, Huber P, Zurbruegg H. Evaluation of cerebrovascular disease by combined extracranial and transcranial Doppler sonography. Experience in 1039 patients. Stroke. 1987; 18: 1018–1024.[Abstract/Free Full Text]
  6. Sloan MA, Haley EC Jr, Kassell NF, Henry ML, Stewart SR, Beskin RR, Sevilla EA, Torner JC. Sensitivity and specificity of transcranial Doppler ultrasonography in the diagnosis of vasospasm following subarachnoid hemorrhage. Neurology. 1989; 39: 1514–1518.[Abstract/Free Full Text]
  7. 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: 213–218.[Abstract/Free Full Text]
  8. Vriens EM, Kraaier V, Musbach M, Wieneke GH, van Huffelen AC. Transcranial pulsed Doppler measurements of blood velocity in the middle cerebral artery: reference values at rest and during hyperventilation in healthy volunteers in relation to age and sex. Ultrasound Med Biol. 1989; 15: 1–8.
  9. Seiler RW, Grolimmund P. Transcranial Doppler evaluation of cerebral vasospasm.In: Wilkins RH, ed. Cerebral Vasospasm New York, NY: Raven Publishing Co; 1988: 19–23.
  10. Harders AG, Gilsbach JM, Hornyak ME. Transcranial Doppler evaluation of cerebral vasospasm.In: Wilkins RH, ed. Cerebral Vasospasm New York: Raven; 1988: 33–52.
  11. Sloan MA, Zagardo MT, Jones DA. TCD diagnosis of vasospasm following subarachnoid hemorrhage in persons 55 years and older. J Neuroimaging. 1997; 7: 227.Abstract.[Medline] [Order article via Infotrieve]
  12. Boecher-Schwarz HG, Ungersboeck K, Ulrich P, Fries G, Wild A, Perneczky A. Transcranial Doppler diagnosis of cerebral vasospasm following subarachnoid haemorrhage: correlation and analysis of results in relation to the age of patients. Acta Neurochir. 1994; 127: 32–36.[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. 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]
  15. 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]
  16. Ekelund A, Saveland H, Romner B, Brandt L. Is transcranial Doppler sonography useful in detecting late cerebral ischaemia after aneurysmal subarachnoid haemorrhage? Br J Neurosurg. 1996; 10: 19–25.[Medline] [Order article via Infotrieve]
  17. Laumer R, Steinmeier R, Gonner F, Vogtmann T, Priem R, Fahlbusch R. Cerebral hemodynamics in subarachnoid hemorrhage evaluated by transcranial Doppler sonography, part 1: reliability of flow velocities in clinical management. Neurosurgery. 1993;33:1–8. Discussion. Neurosurgery. 1993; 33: 8–9.
  18. Proust F, Callonec F, Clavier E, Lestrat JP, Hannequin D, Thiebot J, Freger P. Usefulness of transcranial color-coded sonography in the diagnosis of cerebral vasospasm. Stroke. 1999; 30: 1091–1098.[Abstract/Free Full Text]
  19. Lindegaard KF, Nornes H, Bakke SJ, Sorteberg W, Nakstad P. Cerebral vasospasm after subarachnoid haemorrhage investigated by means of transcranial Doppler ultrasound. Acta Neurochir Suppl. 1988; 42: 81–84.[Medline] [Order article via Infotrieve]
  20. Sloan MA, Rigamonti D, Wozniak MA, Aldrich EF, Acosta JA, Shotts P, Jones D, Macko RF. Prevalence of anterior circulation vasospasm: a transcranial Doppler study. Stroke. 1994; 25: 744.Abstract.
  21. Gosling RG, King DH. Arterial assessment by Doppler-shift ultrasound. Proc R Soc Med. 1974; 67: 447–449.
  22. Grosset DG, Straiton J, du Trevou M, Bullock R. Prediction of symptomatic vasospasm after subarachnoid hemorrhage by rapidly increasing transcranial Doppler velocity and cerebral blood flow changes. Stroke. 1992; 23: 674–679.[Abstract/Free Full Text]
  23. Kelly PJ, Gorten RJ, Grossman RG, Eisenberg HM. Cerebral perfusion, vascular spasm, and outcome in patients with ruptured intracranial aneurysms. J Neurosurg. 1977; 47: 44–49.[Medline] [Order article via Infotrieve]
  24. Hassler W, Chioffi F. CO2 reactivity of cerebral vasospasm after aneurysmal subarachnoid haemorrhage. Acta Neurochir. 1989; 98: 167–175.[Medline] [Order article via Infotrieve]
  25. Melamed E, Lavy S, Bentin S, Cooper G, Rinot Y. Reduction in regional cerebral blood flow during normal aging in man. Stroke. 1980; 11: 31–35.[Abstract/Free Full Text]
  26. Murphy DG, DeCarli C, McIntosh AR, Daly E, Mentis MJ, Pietrini P, Szczepanik J, Schapiro MB, Grady CL, Horwitz B, Rapoport SI. Sex differences in human brain morphometry and metabolism: an in vivo quantitative magnetic resonance imaging and positron emission tomography study on the effect of aging. Arch Gen Psychiatry. 1996; 53: 585–594.[Abstract]
  27. Kusunoki K, Oka Y, Saito M, Sadamoto K, Sakaki S, Miki H, Nagasawa K. Changes in visibility of intracranial arteries on MRA with normal ageing. Neuroradiology. 1999; 41: 813–819.[Medline] [Order article via Infotrieve]
  28. Safar M. Ageing and its effects on the cardiovascular system. Drugs. 1990; 39: 1–8.
  29. Lund-Johansen P. The hemodynamics of the aging cardiovascular system. J Cardiovasc Pharmacol. 1988; 12: S20–S32.
  30. Naylor AR, Merrick MV, Slattery JM, Notghi A, Ferrington CM, Miller JD. Parametric imaging of cerebral vascular reserve, 2: reproducibility, response to CO2 and correlation with middle cerebral artery velocities. Eur J Nucl Med. 1991; 18: 259–264.[Medline] [Order article via Infotrieve]
  31. Kofke WA, Brauer P, Policare R, Penthany S, Barker D, Horton J. Middle cerebral artery blood flow velocity and stable xenon-enhanced computed tomographic blood flow during balloon test occlusion of the internal carotid artery. Stroke. 1995; 26: 1603–1606.[Abstract/Free Full Text]
  32. Baker AB, Iannone A. Cerebrovascular disease, III: the intracerebral arterioles. Neurology. 1959; 9: 441–446.
  33. Kerber CW, Liepsch D. Flow dynamics for radiologists, II: practical considerations in the live human. AJNR Am J Neuroradiol. 1994; 15: 1076–1086.[Abstract]
  34. Allen GS, Ahn HS, Preziosi TJ, Battye R, Boone SC, Chou SN, Kelly DL, Weir BK, Crabbe RA, Lavik PJ, Rosenbloom SB, Dorsey FC, Ingram CR, Mellits DE, Bertsch LA, Boisvert DP, Hundley MB, Johnson RK, Strom JA, Transou CR. Cerebral arterial spasm-a controlled trial of nimodipine in patients with subarachnoid hemorrhage. N Engl J Med. 1983; 308: 619–624.[Abstract]
  35. Kassell NF, Torner JC, Haley EC Jr, Jane JA, Adams HP, Kongable GL. The International Cooperative Study on the Timing of Aneurysm Surgery, part 1: overall management results. J Neurosurg. 1990; 73: 18–36.[Medline] [Order article via Infotrieve]
  36. Sloan M, Wozniak M, Rigamonti D, Aldrich F, simard M, Macko R, Deaver R, Jones D. Effect of age on transcranial Doppler diagnosis of vasospasm following subarachnoid hemorrhage. Stroke. 1995; 26: 726.Abstract.
  37. Artiola L, Fortuny I, Adams CB. Predicting outcome in patients with intracranial aneurysms with the help of microsurgery. J Neurol Neurosurg Psychiatry. 1981; 44: 615–620.[Medline] [Order article via Infotrieve]
  38. Oka K, Kuromatsu C, Takaki T, Maeyama R, Fukui M, Kitamura K. Therapeutic problems in aged patients with intracranial aneurysms [in Japanese]. No Shinkei Geka. 1987; 15: 375–379.[Medline] [Order article via Infotrieve]
  39. Meyer JS, Terayama Y, Takashima S. Cerebral circulation in the elderly. Cerebrovasc Brain Metab Rev. 1993; 5: 122–546.[Medline] [Order article via Infotrieve]
  40. Claus JJ, Breteler MM, Hasan D, Krenning EP, Bots ML, Grobbee DE, Van Swieten JC, Van Harskamp F, Hofman A. Regional cerebral blood flow and cerebrovascular risk factors in the elderly population. Neurobiol Aging. 1998; 19: 57–64.[Medline] [Order article via Infotrieve]
  41. Hegedus K, Molnar P. Age-related changes in reticulin fibers and other connective tissue elements in the intima of the major intracranial arteries. Clin Neuropathol. 1989; 8: 92–97.[Medline] [Order article via Infotrieve]
  42. Dewey RC, Pieper HP, Hunt WE. Experimental cerebral hemodynamics: vasomotor tone, critical closing pressure, and vascular bed resistance. J Neurosurg. 1974; 41: 597–606.[Medline] [Order article via Infotrieve]
  43. Meyer CH, Lowe D, Meyer M, Richardson PL, Neil-Dwyer G. Progressive change in cerebral blood flow during the first three weeks after subarachnoid hemorrhage. Neurosurgery. 1983; 12: 58–76.[Medline] [Order article via Infotrieve]
  44. 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]



This article has been cited by other articles:


Home page
 NeurologyHome page
L. A. Lanterna, M. Rigoldi, G. Tredici, F. Biroli, C. Cesana, S. M. Gaini, and L. Dalpra
APOE influences vasospasm and cognition of noncomatose patients with subarachnoid hemorrhage
Neurology, April 12, 2005; 64(7): 1238 - 1244.
[Abstract] [Full Text] [PDF]

Home page
 NeurologyHome page
A. B. Singhal, M. A. Topcuoglu, D. J. Dorer, C. S. Ogilvy, B. S. Carter, and W. J. Koroshetz
SSRI and statin use increases the risk for vasospasm after subarachnoid hemorrhage
Neurology, March 22, 2005; 64(6): 1008 - 1013.
[Abstract] [Full Text] [PDF]

Home page
 Am. J. Roentgenol.Home page
J. Krejza, Z. Mariak, and J. Lewko
Standardization of Flow Velocities with Respect to Age and Sex Improves the Accuracy of Transcranial Color Doppler Sonography of Middle Cerebral Artery Spasm
Am. J. Roentgenol., July 1, 2003; 181(1): 245 - 252.
[Abstract] [Full Text] [PDF]

Home page
 StrokeHome page
J. Krejza, Z. Mariak, A. Y. Razumovsky, A. Bhardwaj, T.-K. Hauser, M. A. Williams, J. A. Ulatowski, M. A. Mirski, and M. T. Torbey
Effect of Age on Cerebral Blood Flow Velocity in Patients After Aneurysmal Subarachnoid Hemorrhage
Stroke, February 1, 2002; 33(2): 640 - 642.
[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
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrow Request Permissions
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Torbey, M. T.
Right arrow Articles by Razumovsky, A. Y.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Torbey, M. T.
Right arrow Articles by Razumovsky, A. Y.
Related Collections
Right arrow Aneurysm, AVM, hematoma
Right arrow Brain Circulation and Metabolism
Right arrow Cerebral Aneurysm, AVM, & Subarachnoid hemorrhage
Right arrow Angiography
Right arrow Doppler ultrasound, Transcranial Doppler etc.

Stroke Home | Subscriptions | Archives | Feedback | Authors | Help | AHA Journals Home | Search
Copyright © 2001 American Heart Association, Inc. All rights reserved. Unauthorized use prohibited.