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(Stroke. 1996;27:1221-1225.)
© 1996 American Heart Association, Inc.

Articles

Assessment of Normal Flow Velocity in Basal Cerebral Veins

A Transcranial Doppler Ultrasound Study

Jose Manuel Valdueza, MD; Klaus Schmierer, MD; Susan Mehraein, MD Karl Max Einhaupl, MD

the Department of Neurology, University Hospital Charite, Humboldt University, Berlin, Germany.

Correspondence to Jose Manuel Valdueza, MD, Department of Neurology, University Hospital Charite, Humboldt University, Schumannstraße 20/21, 10117 Berlin, Germany.

	Abstract

Top Abstract Introduction Subjects and Methods Results Discussion References

 
Background and Purpose Transcranial Doppler ultrasound has not yet been applied systematically to the analysis of the venous system and cerebrovenous disorders. Assessment of the intracranial venous system, however, would contribute to the understanding of cerebral hemodynamics and thus allow new possibilities for clinical application of the Doppler technique. Therefore, we demonstrated the validity of the transcranial Doppler technique in analyzing the basal cerebral veins.

Methods Venous transcranial Doppler ultrasound was performed with a range-gated 2-MHz transducer in 60 healthy volunteers and patients without central nervous disorders ranging in age from 10 to 71 years (mean±SD, 41.9±15 years).

Results A venous signal away from the probe and adjacent to the posterior cerebral artery, considered to correspond to the basal vein of Rosenthal, was found in all subjects on at least one side. Mean blood flow velocity ranged from 4 to 17 cm/s (mean±SD, 10.1±2.3 cm/s). Analysis for age dependency revealed a trend of decreasing values with increasing age, exclusively caused by a significant reduction of velocity in men aged 40 years or older. No significant intraindividual side-to-side differences were found. A venous signal away from the probe and paralleling the middle cerebral artery, interpreted as corresponding to the deep middle cerebral vein, was found in 21.7% of the subjects with similar velocities.

Conclusions We have shown that transcranial Doppler methods can also be used for evaluation of the basal cerebral veins in both sexes, in differing age groups, and without major difficulty. The cerebral basal veins could be identified on the basis of their anatomic relation to specific arteries.

Key Words: blood flow velocity • cerebral veins • transcranial Doppler

	Introduction

Top Abstract Introduction Subjects and Methods Results Discussion References

 
Since its introduction in 1982,¹ TCD has been shown to be a reliable and noninvasive method for examining the large basal cerebral arteries. Over the ensuing years, the major basal arteries have been identified by different approaches, reference values of blood flow velocities have been established, and the influence of age, sex, and physiological variables has been demonstrated.^{2 3 4}

In contrast to the advances made in the evaluation of the arterial system, the usefulness of TCD in the analysis of venous blood flow has not yet been established systematically. Major reasons for this neglect have been technical problems in the detection of low-flow velocities, the presumed variability of cerebral veins, and lack of clinical interest in cerebrovenous disorders compared with arterial diseases. Normal venous blood flow velocities in a small number of healthy young volunteers have been reported by insonation of the straight sinus through a transoccipital approach⁵ and in the BVR through the temporal window.⁶ In consideration of these findings, we conducted a study with three major objectives: to present anatomic data for the identification of the cerebral basal veins, to establish normal reference values of venous mean blood flow velocities, and to validate the influence of age, sex, and side-to-side and vessel-to-vessel differences.

	Subjects and Methods

Top Abstract Introduction Subjects and Methods Results Discussion References

 
Venous Doppler studies were performed in 60 presumably healthy volunteers and neurological patients without cardiac, pulmonary, or central nervous system disorders (33 males and 27 females; age range, 7 to 71 years [mean age, 41.9±15 years]). Doppler ultrasound was performed with the patient in the supine position with a range-gated 2-MHz transducer (Multidop-X, Firma Elektronische Systeme GmbH, DWL). The basal arteries were bilaterally identified with the use of a posterior transtemporal approach. Once the P2 segment of the PCA was identified at a depth of approximately 60 mm, low values for scale, gain, filter setting, and sample volume were selected to facilitate the visual and acoustic recognition of a low-flow venous signal, which otherwise would be masked by the PCA. After identifying the vein that was thought to be the BVR on the basis of its anatomic proximity to the PCA, we determined the minimal and maximal depths from which the venous signal could be obtained by varying the sample volume depth by 2-mm increments and performing small angle corrections. The orientation and depth were then adjusted until the Doppler signals were maximal. A second venous signal away from the probe at a depth of approximately 50 mm, paralleling the MCA, was interpreted to be the DMCV. Its boundaries and maximal Doppler signal were processed in the same way. V_max (the time-averaged mean over the cardiac cycle of the spectral outline) was recorded in centimeters per second. The PI was calculated as systolic velocity minus diastolic velocity divided by V_max. For purposes of statistical evaluation, two-tailed t tests and regression analyses were performed. A value of P<.05 was considered significant.

	Results

Top Abstract Introduction Subjects and Methods Results Discussion References

 
Ages ranged from 10 to 71 years (mean±SD, 41.9±15 years). The BVR, characterized by a whispering sound and a low-amplitude pulsatile flow signal away from the probe (Fig 1), was found on the right side at a depth ranging from a minimum of 44 to a maximum of 88 mm (mean±SD, 55.4±4.6 to 73.7±5.4 mm) in all 60 individuals and on the left side at a depth of 46 to 90 mm (mean±SD, 56.1±4.5 to 73.2±5.8 mm) in 56 of 60 subjects (93.3%). V_max ranged from 4 to 17 cm/s (mean±SD, 10.1±2.3 cm/s). Table 1 summarizes the basic data. No statistically significant differences were found in age, blood pressure, or heart rate between both sexes. No side-to-side differences were noted regarding V_max. Regression analysis between age and flow velocity showed a nonsignificant age-related decline in V_max. An additional sex-related evaluation revealed unchanged V_max in females, whereas a statistically significant (P=.006) decline in blood flow velocity could be found in males (Fig 2). For purposes of further analysis, two age groups (<40 and 40 years) were separately studied for both sexes. As shown in Table 2, no sex-related difference in V_max could be observed in the younger age group. In individuals aged 40 years or older, a highly significant difference became obvious as a result of a marked decline of V_max in men (P=.002).

View larger version (44K): [in this window] [in a new window]   Figure 1. Venous TCD signal away from the probe has been obscured by the P2 segment of the PCA when common Doppler parameters are used (A). Decreasing the sample volume, the filter setting, and the power intensity facilitate detection of the BVR. Note a mean blood flow velocity of 11 cm/s and a PI of 0.36 (B).

View this table: [in this window] [in a new window]   Table 1. Summary of Demographic Data, Insonation Depths, and Blood Flow Velocities in the BVR

View larger version (17K): [in this window] [in a new window]   Figure 2. Correlation of age and sex with velocities in the BVR. Vmax shows a nonsignificant tendency to decrease in all individuals (P=.078, r=.16) (116 insonated vessels) (A). No decrease was noted in females (P=.773, r=.04) (B). A significant decrease in venous blood flow velocities was found in males (P=.006, r=.34) (C).

View this table: [in this window] [in a new window]   Table 2. Influence of Age and Sex on Blood Flow Velocity in BVR

Venous signals of the basal veins were characterized by low pulsatility in a more bandlike or sinusoid fashion, revealing minor differences between systolic and end-diastolic blood flow velocities. The PI ranged from 0.2 to 0.5 (Fig 3). The accuracy of calculating PI, however, was limited by the low-flow characteristic of the vein signal and the technical boundaries of the Doppler instrument. Thus, a clearly shaped outside envelope could not be displayed in all instances.

View larger version (57K): [in this window] [in a new window]   Figure 3. Simultaneous insonation of the M1 segment of the MCA enables the identification of the DMCV. Note a more bandlike appearance of the vein signal, with a PI of 0.22 (A), and a more pulsatile, sinusoid pattern, with a PI of 0.43 (B).

A venous signal away from the probe and paralleling the MCA was considered to be the DMCV. It was recorded 18 times either unilaterally or bilaterally in 13 (6 females, 7 males) of 60 individuals (21.7%). Ages ranged from 23 to 39 years (mean±SD, 30.6±3.8 years). The vein was recorded at a depth ranging from 36 to 72 mm (mean±SD, 48.2±3.8 to 60.2±3.6 mm). V_max ranged from 6 to 18 cm/s (mean±SD, 11.1±2.7 cm/s). No statistical differences between V_max of the BVR and DMCV were found, and no special side-to-side or sex-related differences were noted.

View larger version (31K): [in this window] [in a new window]   Figure 4. Anatomy of basal cerebral veins and position of sample volume during Doppler insonation by a transtemporal approach (adapted from Lang et al10 ): 1, DMCV; 2, anterior cerebral vein; 3, BVR, anterior segment; 4, peduncular vein; 5, BVR, middle segment; and 6, BVR, posterior segment.

	Discussion

Top Abstract Introduction Subjects and Methods Results Discussion References

 
In comparison to the vast amount of knowledge on cerebral arterial physiology and pathophysiology that has been achieved with the aid of TCD, little is known about the cerebral venous circulation. Technical advances of the newer Doppler instruments allowing optimization of sample volume, filter setting, and power intensity have facilitated the examination of the venous system. In previous studies, venous TCD has been used in the investigation of normal cerebral hemodynamics⁵ as well as cerebrovenous disorders in a limited number of healthy subjects and patients suffering from dural sinus thrombosis.^{6 7} Therefore, the major goals of our study were to elaborate on the procedure for identifying the basal cerebral veins through a transtemporal approach, to establish normal reference values, and to discuss variables such as age and sex.

Anatomic Considerations
Similar to the cisternal basal arteries, the cerebral basal veins form a venous circuit. The BVR represents the most prominent basal venous vessel, which can be separated into three segments: anterior, middle, and posterior.⁸ Hypoplasia seldom occurs. Variations are restricted to the anterior and posterior segments, whereas the middle segment of the BVR is almost always standard in location and size, with a diameter of 2 to 3 mm. The DMCV is the second most important vein. It passes through the anterior perforated substance, where it joins the anterior cerebral vein to form the anterior segment of the BVR.^{9 10}

For Doppler purposes, three anatomic considerations are relevant: first, the common viewpoint regarding the anatomic variability of the BVR cannot be confirmed, particularly in regard to its middle segment, which is detectable by TCD. Inability to visualize the BVR on angiography (in 20% of cases) has been attributed to technical causes.⁸ However, the BVR has been visualized on MR angiographic studies in nearly 100% of cases.^{11 12} Apart from variations in the anterior and posterior segments of the BVR, anatomic examinations confirmed that the middle segment of the BVR is present in all cases.¹³ The high percentage of insonation of the BVR (100% on the right and 93.3% on the left side) reflects its stable anatomy. Second, the DMCV usually reveals an orthograde flow signal away from the probe. The flow may change to a retrograde signal toward the probe if there is no communication between the middle and anterior segments of the BVR. The flow in the middle segment of the BVR remains orthograde in such cases. Finally, the simultaneous insonation of the PCA not only ensures the identification of the BVR but may facilitate distinction between the PCA and MCA, which in some instances is not easily performed. Fig 4 shows the relevant anatomy of the basal cerebral veins detectable by TCD through a transtemporal approach.

Reference Values
Analysis of 60 subjects revealed modest variations of V_max in the BVR, ranging from 4 to 17 cm/s (mean±SD, 10.1±2.3 cm/s). Normal adult venous TCD findings were first reported by Aaslid et al⁵ in 1991. Analysis of the straight sinus in 9 of 12 healthy subjects revealed a V_max of 20±3 cm/s when the transoccipital approach was used. Valdueza et al⁶ recently reported a V_max of 12.1±3.5 cm/s in a group of 10 healthy young volunteers after insonating the BVR using a transtemporal approach. Systolic flow velocities of 19.1 cm/s in the straight sinus of healthy subjects have been determined by color-coded real-time sonography.¹⁴ Before the reports in adults, normal venous blood flow velocities were established for newborns and infants by various groups with the use of the cranial duplex ultrasound method. This was facilitated by the transparency of young skulls. Established values were as follows: 5.4 to 6.6 cm/s for systolic blood flow velocities in the vein of Galen of young infants¹⁵ ; 5.5±1.6 cm/s in the internal cerebral vein and 12.6±7.8 cm/s in the straight sinus of healthy neonates¹⁶ ; and 13.2, 5.6, 5.9, and 5.6 cm/s in the straight sinus, the vein of Galen, and the right and left BVR of neonates and young infants, respectively.¹⁷ With the use of color-coded duplex sonography, the following values were found in newborns: mean blood flow velocities of 3.3 cm/s in the internal cerebral vein, 4.3 cm/s in the vein of Galen, 5.9 cm/s in the straight sinus, and 9.2 cm/s in the superior sagittal sinus.¹⁸ The velocities measured by Doppler technique correlate excellently with velocities calculated from MRI. With the use of a phase-sensitive, limited-flip-angle, gradient-echo-recalled method, V_max ranged from 9.9 to 14.4 cm/s in the transverse and superior sagittal sinuses of normal subjects.¹⁹ Analysis of our data and the reported findings in neonates and infants suggests that V_max correlates positively with increasing vessel size, thus reflecting the large amount of blood in the greater veins and sinuses.

Influence of Age and Sex
Analysis of age dependence showed a nonsignificant decline in venous V_max with increasing age, which has also been demonstrated in the arterial system and may be due to age-related changes in cerebral blood flow.²⁰ One striking feature of our study was a significant decline in flow velocity in older men. These findings differ from known results in the basal arteries, which show sex-related differences in velocity that diminish with age.²¹

Conclusions
In conclusion, we have shown the capacity of TCD in examining the basal cerebral veins. In particular, the BVR was detectable in almost all cases. Its usefulness for noninvasive examination of the venous circulation and cerebral autoregulation has recently been shown.⁵ At present, one major clinical application may be the evaluation of venous collateral pathways in dural sinus thrombosis. Recently published case reports that involved venous TCD in adults have shown that V_max is elevated in the venous collateral vessels.^{6 7} The normalization of initially elevated venous V_max in the BVR in angiographically substantiated dural sinus thrombosis has also been successfully monitored with TCD.⁶ Similar findings were found in two adults with the use of transcranial color-coded real-time sonography when the straight sinus in dural sinus thrombosis was insonated.¹⁴ A flow reversal in the sagittal sinus and both BVR, due to a thrombosis at the confluence of sinuses, was observed in a child examined with the duplex ultrasound technique.¹⁷ Concomitantly performed conventional digital subtraction angiography and MR angiographic studies are necessary for purposes of evaluation before the Doppler technique can be routinely used as a monitoring tool in dural sinus thrombosis. The major disadvantage lies in the low-flow characteristics of the venous signal, which may be hidden by arterial signals. An intense venous signal may also be difficult to achieve in older patients. The use of contrast agents most probably will facilitate the recognition of intracranial veins in future studies. Despite these limitations, we believe that the extension of TCD to the venous system will open new perspectives for the noninvasive examination of venous cerebral blood flow.

	Selected Abbreviations and Acronyms

 

BVR = basal vein of Rosenthal DMCV = deep middle cerebral vein MCA = middle cerebral artery PCA = posterior cerebral artery PI = pulsatility index TCD = transcranial Doppler ultrasonography

	Acknowledgments

 
We wish to express our appreciation to Dr Thomas Davenport for linguistic assistance and to Gerd Dombrowsky for technical support.

Received December 27, 1995; revision received March 4, 1996; accepted March 5, 1996.

	References

Top Abstract Introduction Subjects and Methods Results Discussion References

 
1. Aaslid R, Markwalder TM, Nornes H. Non-invasive transcranial Doppler ultrasound recording of flow velocity in basal cerebral arteries. J Neurosurg. 1982;57:769-774.[Medline] [Order article via Infotrieve]

2. Arnold BJ, Von Reutern GM. Transcranial Doppler sonography: examination technique and normal reference values. Ultrasound Med Biol. 1986;12:115-123.[Medline] [Order article via Infotrieve]

3. Hennerici M, Rautenberg W, Sitzer G, Schwartz A. Transcranial Doppler ultrasound for the assessment of intracranial arterial flow velocity: part 1. Surg Neurol. 1987;27:439-448.[Medline] [Order article via Infotrieve]

4. Ringelstein EB, Kahlscheuer B, Niggemeyer E, Otis SM. Transcranial Doppler sonography: anatomical landmarks and normal velocity values. Ultrasound Med Biol. 1990;16:745-761.[Medline] [Order article via Infotrieve]

5. Aaslid R, Newell DW, Stooss R, Sorteberg W, Lindegaard KF. Assessment of cerebral autoregulation dynamics from simultaneous arterial and venous transcranial Doppler recordings in humans. Stroke. 1991;22:1148-1154.[Abstract/Free Full Text]

6. Valdueza JM, Schultz M, Harms L, Einhaupl KM. Venous transcranial Doppler ultrasound monitoring in acute dural sinus thrombosis: report of two cases. Stroke. 1995;26:1196-1199.[Abstract/Free Full Text]

7. Wardlaw JM, Vaughan GT, Steers AJW, Sellar RJ. Transcranial Doppler ultrasound findings in venous sinus thrombosis. J Neurosurg. 1994;80:332-335.[Medline] [Order article via Infotrieve]

8. Huber P. Cerebral Angiography. 2nd ed. Stuttgart, Germany: Thieme Verlag; 1982.

9. Lang J. Skull Base and Related Structures: Atlas of Clinical Anatomy. Stuttgart, Germany: Schattauer Verlag; 1995.

10. Lang J, Koth R, Reiss G. On the origin, course and influx-vessels of the v. basalis and the v. cerebri magna. Anat Anz.. 1981;150:385-423.[Medline] [Order article via Infotrieve]

11. Ikawa F, Sumida M, Uozumi T, Kiya K, Kurisu K, Arita K, Satoh H. Demonstration of the venous system with gadolinium-enhanced three-dimensional phase-contrast MR venography. Neurosurg Rev.. 1995;18:101-107.[Medline] [Order article via Infotrieve]

12. Mattle HP, Wentz KU, Edelman RR, Wallner B, Finn JP, Barnes P, Atkinson DJ, Kleefield J, Hoogewoud HM. Cerebral venography with MR. Radiology. 1991;178:453-458.[Abstract/Free Full Text]

13. Ono M, Rhoton AL, Peace D, Rodriguez RJ. Microsurgical anatomy of the deep venous system of the brain. Neurosurgery. 1984;15:621-657.[Medline] [Order article via Infotrieve]

14. Becker G, Bogdahn U, Gehlberg C, Frohlich T, Hofmann E, Schlief R. Transcranial color-coded real-time sonography of intracranial veins: normal values of blood flow velocities and findings in superior sagittal sinus thrombosis. J Neuroimaging.. 1994;5:87-94.

15. Grant EG, White EM, Schellinger D, Choyke PL, Sarcone AL. Cranial duplex sonography of the infant. Radiology. 1987;163:177-185.[Abstract/Free Full Text]

16. Pfannschmidt J, Jorch G. Transfontanelle pulsed Doppler measurement of blood flow velocity in the internal jugular vein, straight sinus and internal cerebral vein in preterm and term neonates. Ultrasound Med Biol. 1989;1:9-12.

17. Winkler P, Helmke K. Duplex-scanning of the deep venous drainage in the evaluation of blood flow velocity of the cerebral vascular system in infants. Pediatr Radiol. 1989;19:79-90.[Medline] [Order article via Infotrieve]

18. Taylor GA. Intracranial venous system in the newborn: evaluation of normal anatomy and flow characteristics with color Doppler ultrasound. Radiology. 1992;183:449-452.[Abstract/Free Full Text]

19. Tsuruda JS, Shimakawa A, Pelc NJ, Saloner D. Dural sinus occlusion: evaluation with phase-sensitive gradient-echo MR imaging. AJNR Am J Neuroradiol. 1991;12:481-488.[Abstract]

20. Grolimund P, Seiler RW. Age dependence of the flow velocity in the basal cerebral arteries: a transcranial Doppler ultrasound study. Ultrasound Med Biol. 1988;3:191-198.

21. Vriens EM, Kraaier V, Musbach M, Wieneke GH, van Huffelen AC. Transcranial pulsed Doppler measurements of blood flow velocity in the middle artery: reference values at rest and during hyperventilation in healthy volunteers in relation to age and sex. Ultrasound Med Biol. 1989;15:1-8.

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