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Stroke. 2002;33:640-642

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(Stroke. 2002;33:640.)
© 2002 American Heart Association, Inc.

Letters to the Editor

Effect of Age on Cerebral Blood Flow Velocity in Patients After Aneurysmal Subarachnoid Hemorrhage

Jaroslaw Krejza, MD, PhD

Department of Radiology, Bialystok Medical Academy, Bialystok, Poland

Zenon Mariak, MD, PhD

Department of Neurosurgery, Bialystok Medical Academy, Bialystok, Poland

To the Editor:

We read with interest the article by Torbey et al1 on effect of age on cerebral blood flow velocity in patients after aneurysmal subarachnoid hemorrhage, published in the September issue of Stroke. Using conventional transcranial Doppler ultrasonography, the authors report an unexpectedly large decrease in flow velocity in the middle cerebral artery (MCA) in patients older than 68 years in comparison to those younger than 68 years. The mean flow velocity in the MCA was found to be 42 cm/s in the former and 81 cm/s in the latter group. Thus, the difference was as much as 48%, whereas elsewhere, in other large groups of healthy subjects, the range of difference was only between 17% and 22%.2,3 The fact that the authors found a higher incidence of vasospasm in the younger group cannot explain the discrepancy because such significant differences in flow velocity were found at admission, ie, before the vasospasm usually develops. The authors have addressed only superficially a fundamental question: why does subarachnoid hemorrhage affect cerebral vessels in older patients differently? The problem is even more intriguing given the fact that vasoreactivity appears not to be affected by normal aging.4,5

We suspect that the decline in flow velocity in reality does not need to be as substantial as the authors state. The conventional Doppler technique they used does not allow measurement of the angle of insonation of the vessel, which is crucial in their setup of the study. In young persons the horizontal portion of the MCA projects laterally toward the temporal acoustic window, whereas in older subjects it bows ventrally, which results in a wider angle of insonation.6 No exact data on the real magnitude of this angle in normal elderly subjects have been published to date. It is nevertheless important to add that our recent data7 suggest that the MCA escapes even more from the optimal line of insonation when pathologies such as intracranial arterial stenosis and/or mass are present. It is apparent that the incidence of the MCA atherosclerosis and/or stenosis must be higher in an older group of subjects, and it surely must have been in the group examined by Torbey and colleagues. We have found with color Doppler technique that the angle of insonation of the MCA was 47±11° on the side of its stenosis and 34±18° on the opposite side in 18 patients with MCA M1 stenosis.7 If we measured the flow velocity in these patients with no angle correction, the decline of the MCA from the optimal (ie, 0°) angle of insonation would introduce an error of 46% reduction of the blood flow velocity. This figure matches well the 48% of flow velocity reduction found by Torbey and colleagues in their elder patients.

With these factors taken into consideration, our opinion is that no reliable conclusions on flow velocity in the MCA in old patients with cerebral pathologies can be drawn from measurements obtained with conventional transcranial Doppler ultrasonography. This problem can be much more reliably addressed with the use of transcranial color Doppler ultrasonography, which enables the sonographer to obtain angle-corrected blood flow velocities.

References

  1. Torbey MT, Hauser TK, Bhardway A, Williams MA, Ulatowski JA, Mirski MA, Razumovsky AY. Effect of age on cerebral blood flow velocity and incidence of vasospasm after aneurysmal subarachnoid hemorrhage. Stroke. 2001; 32: 2005–20011.[Abstract/Free Full Text]
  2. 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]
  3. Martin PJ, Evans DH, Naylor AR. Transcranial color-coded sonography of the basal cerebral circulation: reference data from 115 volunteers. Stroke. 1994; 25: 390–396.[Abstract]
  4. Carey BJ, Eames PJ, Blake MJ, Panerai RB. Dynamic cerebral autoregulation is unaffected by aging. Stroke. 2000; 31: 2895–2900.[Abstract/Free Full Text]
  5. Lipsitz LA, Mukai S, Hamner J, Gagnon M, Babikian V. Dynamic regulation of middle cerebral artery blood flow velocity in aging and hypertension. Stroke. 2000; 31: 1897–1903.[Abstract/Free Full Text]
  6. Krejza J, Mariak Z, Melhem ER, Bert R. A guide to the identification of major cerebral arteries with transcranial color Doppler sonography. AJR Am J Roentgenol. 2000; 174: 1297–1303.[Free Full Text]
  7. Krejza J, Mariak Z, Babikian VL. Importance of angle correction in measurement of blood flow velocity with transcranial Doppler sonography. AJNR Am J Neuroradiol. 2001; 22: 1743–1747.[Abstract/Free Full Text]

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

Department of Anesthesiology/Critical Care Medicine, Department of Neurology, The Johns Hopkins Medical Institutions, Baltimore, Md

Response

We appreciate the comments of Drs Krejza and Mariak and their interest in our article on the effect of age on cerebral blood flow velocity (CBFV) measured by transcranial Doppler ultrasonography (TCD) after aneurysmal subarachnoid hemorrhage (SAH).1 We are in accord with Krejza and Mariak that transcranial color-coded ultrasonography (TCCS) provides angle correction and represents a reliable tool for the assessment of cerebral vasculature. Regarding their other comments on our article, we would like to offer the following response.

The first point of Krejza and Mariak concerns our finding of relatively low mean CBFV (42 cm/s) in the middle cerebral artery (MCA) in the older compared with the younger group.1 Despite this, most publications dealing with cerebral blood flow (CBF) measurements in healthy adults report a decline in CBF with increasing age, mainly due to a reduction of cortical CBF.2,3 In addition, CBF declines as early as 2 days after SAH compared with volunteers of the same age.4 The relatively high difference (48%) in the MCA CBFV between the 2 groups in our study could be explained on the basis of advanced age (older than 68 years), presence of SAH, and atherosclerosis, any of which could contribute to the lower MCA CBFV values.

It is not surprising that CBFV decreases with age. Grolimund and Seiler5 have described the relationship between age and MCA CBFV measured by TCD as linear using the following model: CBFV=79.6-0.41age. When this formula is used in a 70-year-old hypothetical patient, the predicted MCA CBFV of 51 cm/s would not be too dissimilar to that of our older patients. Interestingly, Krejza et al,6 in measuring CBFV by TCCS, proposed another formula, CBFV=93-0.67age, which would estimate CBFV of 46 cm/s in a 70-year-old patient, equal to our own findings.

Krejza and Mariak raise questions about clinical value of the conventional "blind" TCD technique, specifically during MCA insonation in the elderly because of the lack of a visual image and ability of angle correction. Clearly, the addition of a visual image will improve evaluation of cerebral hemodynamics, but this does not negate the usefulness of conventional TCD. Conventional TCD has proved to be sufficiently sensitive and accurate to detect intracranial stenosis (including MCA) for patients of all ages.7–9 Since we used a blind TCD technique, it is impossible to ensure the same angle of insonation. However, once an audible Doppler signal is obtained, efforts routinely are made to acquire the strongest and highest-intensity Doppler signal possible by skilled ultrasonographers using visual waveform and audible feedback from the signal itself. The depth and angle of insonation yielding the best signal are then used as a starting point for each individual on subsequent studies. The TCD probe has a smaller diameter than that of the relatively large probe used with TCCS and can be easily manipulated at a variety of angles in all planes to optimize the signal. These maneuvers lead to the optimal angle of insonation and maximal mean CBFV in most cases.

The final issue is more sensitive. Krejza and Mariak make the strong assertion that TCD is limited for diagnosis of CBFV and favor TCCS. We would speculate otherwise at this point, especially in the elderly. It is well known that hyperostosis of the temporal bone is influenced by age, sex, and race. TCCS has a relatively high failure rate with the use of the transtemporal approach. The transtemporal window is not found in 30% of those older than 60 years with the use of TCCS.10 The failure rate of transtemporal insonation was 23% in the study of Martin et al11 using TCCS compared with 16% on the basis of a survey reviewing conventional TCD results from 60 laboratories in the United States.12 One of the reasons for a relatively high (23% to 30%) rate of unsuccessful insonation through the temporal bone in the elderly could be the relatively large surface of the TCCS probe, which limits the degree of freedom for limited temporal window insonation compared with the small surface of the conventional TCD probe. At the present stage, relatively high TCCS failure may prove a factor limiting the use of TCCS for imaging the anterior cerebral circulation in the elderly. The use of echo-contrast agents may partly overcome such difficulties by facilitating imaging in the future.

Direct comparisons between TCD and TCCS are limited. In a work by Krejza et al,6 baseline MCA CBFV value measured by TCCS for the younger population is identical (81 cm/s) to our value, which was obtained with the use of conventional TCD technique.1 In a study comparing the 2 techniques directly in healthy volunteers, Shoning et al13 observed that CBFV for the MCA was 61±13 cm/s by conventional TCD and 58±12 cm/s by TCCS. Bartels and Flugel14 and Proust et al15 showed that angle-corrected systolic CBFV values were higher in all vessels compared with uncorrected systolic CBFV findings by conventional TCD; however, the standard deviation was high for both methods, and there were no statistically significant differences. Proust et al also showed that there was no difference in mean CBFV between TCCS and TCD.15 Therefore, available data do not support a clear overall benefit of either technique.

Krejza et al16 stress the importance of their recent data that suggest that the MCA is distorted from the optimal line of insonation in patients with stenosis or mass effect. However, their data set consisted of a relatively young population (median age, 53 years) with a wide age range of between 22 and 72 years. Furthermore, the significant angle of insonation (47±11°) reported was the average for patients with stenosis (n=11) and intraparenchymal hematoma (n=6). Grouping does not allow separate analysis of elderly patients in this study. Since the presence of an intracranial mass (tumor, hematoma, hydrocephalus) could severely influence the location and consequent insonation of the MCA, their overall mean angle of insonation may be shifted to a higher value than MCA stenosis alone.

In the final analysis, we believe that the age factor should not be ignored in the attempt to establish CBFV thresholds for the diagnosis of cerebral vasospasm. Both TCD and TCCS techniques are exciting developments in neurosonology. However, we can not yet validate the superiority of one over the another. Both methods have their intrinsic benefits and limitations that must be recognized by all users. The availability of TCCS devices is still limited because of the relatively high cost. Some disagreements between the diagnostic findings of conventional TCD and TCCS methods need further evaluation and validation by other CBF studies as well as direct comparison of the techniques in expert hands.

References

  1. Torbey MT, Hauser T-K, Bhardwaj A, Williams MA, Ulatowski JA, Mirski MA, Razumovsky AY. Effect of age on cerebral blood flow velocity and incidence of vasospasm after aneurysmal subarachnoid hemorrhage. Stroke. 2001; 32: 2005–2011.
  2. 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]
  3. Martin AJ, Friston KJ, Colebatch JG, Frackowiak RS. Decreases in regional cerebral blood flow with normal aging. J Cereb Blood Flow Metab. 1991; 11: 684–689.[Medline] [Order article via Infotrieve]
  4. 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]
  5. Grolimund P, Seiler RW. Age dependence of the flow velocity in the basal cerebral arteries: a transcranial Doppler ultrasound study. Ultrasound Med Biol. 1988; 14: 191–198.[CrossRef][Medline] [Order article via Infotrieve]
  6. 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 references values for blood flow parameters. AJR Am J Roentgenol. 1999; 172: 213–218.
  7. Ley-Pozo J, Ringelstein EB. Noninvasive detection of occlusive disease of the carotid siphon and middle cerebral artery. Ann Neurol. 1990; 28: 640–647.[CrossRef][Medline] [Order article via Infotrieve]
  8. Babikian V, Sloan MA, Tegeler CH, DeWitt LD, Fayad PB, Feldmann E, Gomez CR. Transcranial Doppler validation pilot study. J Neuroimaging. 1993; 3: 242–249.[Medline] [Order article via Infotrieve]
  9. Rorick MB, Nichols FT, Adams RJ. Transcranial Doppler correlation with angiography in detection of intracranial stenosis. Stroke. 1994; 25: 1931–1934.[Abstract]
  10. Wada T, Kodaira K, Fujishiro K, Maie KI, Satoi T, Tsukiyama E, Mikawa H, Shimizu H, Fukumoto T, Okamura T. Quantitative measurement of middle cerebral artery flow velocity using transcranial Doppler tomography. Arteries et Veines. 1990; 9: 682–685.
  11. Martin PJ, Evans DH, Naylor AR. Transcranial color-coded sonography of the basal cerebral circulation: reference data from 115 volunteers. Stroke. 1994; 25: 390–396.
  12. Gomez CR, Brass LM, Tegeler CH, Babikian VL, Sloan MA, Feldman E, Wechsler LR. The transcranial Doppler standardization project. J Neuroimaging. 1993; 3: 190–192.[Medline] [Order article via Infotrieve]
  13. Schoning M, Buchholz R, Walter J. Comparative study of transcranial color duplex sonography and transcranial Doppler sonography in adults. J Neurosurg. 1993; 78: 776–784.[Medline] [Order article via Infotrieve]
  14. Bartels E, Flugel KA. Quantitative measurements of blood flow velocity in basal cerebral arteries with transcranial duplex color-flow imaging: a comparative study with conventional transcranial Doppler sonography. J Neuroimaging. 1994; 4: 77–81.[Medline] [Order article via Infotrieve]
  15. Proust E, 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]
  16. Krejza J, Mariak Z, Babikian VL. Importance of angle correction in the measurement of blood flow velocity with transcranial Doppler sonography. AJNR Am J Neuroradiol. 2001; 22: 1743–1747.




This Article
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