PII: S0301-5629(00)00293-3

● Original Contribution

FLOW VELOCITY AND FLOW VOLUME MEASUREMENTS IN THEEXTRACRANIAL CAROTID AND VERTEBRAL ARTERIES IN HEALTHY

ADULTS: REFERENCE DATA AND THE EFFECTS OF AGE

PETER SCHEEL, CHRISTIAN RUGE and MARTIN SCHONING

Division of Child Neurology, Children’s Hospital of the University of Tu¨bingen, D-72076 Tu¨bingen, Germany

(Received24 November1999; in final form 20 July 2000)

Abstract—To establish reference data and to investigate the development of haemodynamics in the extracranialcarotid and vertebral arteries, we performed a prospective study in 78 age- and gender-matched healthy adultsfrom 20 to 85 y old. Angle-corrected flow velocities and luminal diameters were measured and waveformparameters and flow volumes calculated in all the arteries. Side-to-side differences and the influence of age onthese parameters were also investigated. In the common carotid arteries, the internal carotid arteries and thevertebral arteries (CCA, ICA and VA, respectively) all flow velocities decreased significantly during ageing. Theluminal diameter remained constant in all the carotid arteries, but increased slightly with age in the VA. Anage-related decline of intravascular flow volume was observed in the ICA. Due to a pronounced decrease inend-diastolic flow velocity, the resistance index decreased in ICA and VA during ageing. There were nosignificant side-to-side differences in flow velocities and flow volumes in any of the extracranial arteries. Theluminal diameters of the CCA, ICA and ECA were significantly smaller in women than in men. No relevantgender-related differences in flow velocities or waveform parameters were found in the extracranial arteries.There was no gender-linked difference in the flow volumes of the brain-feeding arteries and, in the ECA, flowvolumes were significantly higher in men. Reference data on all flow velocities and waveform parameters, luminaldiameters and flow volumes were established for different age groups between 20 and 85 y old. These data allowus to outline the development of cerebral haemodynamics during “benign ageing” and to utilise flow volumemeasurements in clinical practice, especially in patients with cerebrovascular diseases. © 2000 World Feder-ation for Ultrasound in Medicine & Biology.

Key Words:Duplex ultrasound, Carotid artery, Doppler ultrasound, Volumetry, Vertebral artery, Volume flowmeasurement, Reference data.

INTRODUCTION

A number of publications exist on the clinical applicationof Doppler and duplex techniques in the examination ofthe extracranial brain-supplying arteries in adults. How-ever, only a few studies report on normal values andreference data for flow velocities, waveform parametersand flow volumes of the carotid and the vertebral arteries(Schoning et al. 1994; Scho¨ning and Hartig 1998).

Flow volume measurements in the extracranial ce-rebral arteries could contribute significantly to our un-derstanding of cerebral haemodynamics in patients withcerebrovascular diseases. For the most part, these pa-tients belong to the group of elderly more than 60 y old.

No reference data on intravascular flow volumes andflow velocities are available yet for this age group.

The purpose of this study was to noninvasivelystudy cerebral haemodynamics during benign ageing, toinvestigate the natural influence of age and gender onangle-corrected flow velocities, waveform parameters,luminal diameters and flow volumes in all the extracra-nial carotid and vertebral arteries, and to provide refer-ence data for these parameters in different age groups(between 20 and 85 y old). Ultimately, we hope that ourresults will make possible the introduction of colourduplex flowmetry into clinical and scientific application,especially in the examination of patients suffering fromcerebrovascular disorders.

METHODS

A prospective study on colour duplex sonographyof the extracranial arteries was performed in 78 healthy

Address correspondence to: Martin Scho¨ning, M.D., Division ofChild Neurology, Children’s Hospital of the University of Tu¨bingen,Hoppe-Seyler Str. 1, D-72076 Tu¨bingen, Germany. E-mail: martin.schoening@med.uni-tuebingen.de

Ultrasound in Med. & Biol., Vol. 26, No. 8, pp. 1261–1266, 2000Copyright © 2000 World Federation for Ultrasound in Medicine & Biology

Printed in the USA. All rights reserved0301-5629/00/$–see front matter

1261

adults from 20 to 85 y old (mean age 526 19 y). Toachieve as homogeneous a distribution of age and genderin the study group as possible, we planned to examinecohorts of 3 women and 3 men in each 5-y age groupbetween 20 and 85 y old. In practice, only one exceptionwas made to this rule: one healthy 87-y-old woman wasenrolled in the group of 80- to 85-y-olds. The mean agewas 51.96 19.1 y in the group of 39 women and, in thegroup of 39 men, it was 51.86 19.4 y.

All the subjects lived an independent life, were freeof (and indeed had no history of) cardiac, neurologic orcerebrovascular disease. Only subjects without sono-graphic evidence of plaque formation in the carotid bulbwere included in this study. One 82-y-old man was onmild antihypertensive therapy, but none of the otherparticipants were taking any regular medication. In-formed consent was obtained before the examination.The study was approved by the local Ethical Committeeof the university.

During an initial 20 min of rest in a supine position,the intracranial arteries were examined by transcranialcolour-coded duplex sonography, the results of which arenot part of this study. Then, the extracranial arteries (i.e.,the common carotid arteries (CCA), the external (ECA)and internal carotid arteries (ICA), and the vertebralarteries (VA) of both sides) were explored using the7.0-MHz linear-array transducer of a computed sonog-raphy system (Acuson 128/XP10, Mountain View, CA).

The test people continued to lie supine with theirheads slightly elevated and turned to the contralateralside by'10° for CCA and VA measurements and by 25to 40° for the ICA and ECA measurements. Flow volumemeasurements were most frequently taken in the C4–C5intertransverse segment of the VA, 1.5 to 2 cm below thecarotid bulb in the CCA, and 1 to 2 cm above the carotidbulb in ECA and ICA. For an exact measurement of theluminal width, the diameter (d) must be taken on amagnified B-mode image under visual control of thevessel’s course by setting the calipers exactly perpendic-ular to its course as the distance between the brightinternal layers of the parallel-running walls. In the CCA,pulsatile changes of the diameter can be distinguishedduring a cardiac cycle. Therefore, we always tried to takediameter measurements during the end-diastolic phase.Pulsatile changes were not observed in the ICA, ECA orVA. The mean of two diameter measurements was de-termined for each vessel. The calipers could be adjustedin 0.1-mm increments. At the same site, a sample volumewas positioned to cover the entire luminal width. Exactangle correction was performed. We aimed to keep theangle of insonation as low as possible, in most casesabout 60°. The angle-corrected time-averaged flow ve-locity (TAV) was determined as the integral of the meanflow velocities of all moving particles passing the sample

volume over three to five complete cardiac cycles. In thisway, the pulsatile parabolic flow is mathematically trans-formed into a continuous plug flow. The intravascularflow volume (FV) was calculated as the product ofTAVand the cross-sectional area (A) of the circular vesselusing the formulaFV 5 TAV 3 A 5 TAV 3 [(d/2)2 3p]. Each measurement was recorded with a video printer.The complete examination took about 20 min. To main-tain the exclusively noninvasive character of the exam-ination and to avoid any stress for the subjects, bloodparameters (such as haematocrit or arterial blood gasanalysis) were not determined.

The program SAS (Version 6.12, SAS-Institute,Cary, NC) was used for the statistical analysis. All pa-rameters are shown as the mean6 SD. Student’st-testwas used to reveal side-to-side differences and any dif-ferences between the genders. Age correlation and side-to-side correlation of flow volume parameters were eval-uated using Spearman’s rank correlation coefficient. Thelevel of statistical significance was set top # 0.01 for alltests.

RESULTS

Colour duplex examination and volumetry could beperformed in all the extracranial arteries of all the sub-jects with the exception of one ECA in a 25-y-old man.

In the study group as a whole, we found significantgender-linked differences in the following parameters:luminal diameters were significantly smaller in womenthan in men in the CCA (5.96 0.6 mm vs. 6.46 0.9mm,p , 0.001), as well as in the ICA (4.66 0.5 mm vs.5.1 6 0.7 mm,p , 0.001) and the ECA (3.86 0.5 mmvs. 4.56 0.6 mm,p , 0.0001); there was no genderdifference in the diameter of the VA (3.46 0.4 mm inboth genders). With the exception of a higher meanmaximum flow velocity (TAMX) of the ICA in womenthan in men (396 8 cm/s vs. 346 6 cm/s,p , 0.01),there were no significant gender differences in any flowvelocities or waveform parameters in the extracerebralvessels. Flow volumes were not gender-dependent in theCCA, ICA and VA; however, in the ECA, it was signif-icantly lower in women than in men (1446 50 mL/minvs. 1846 54 mL/min; p , 0.001).

There were no significant side-to-side differences inflow velocities, waveform parameters or flow volumes inthe paired extracranial vessels. The side-to-side correla-tion of TAV, dandFV was high in all the homologouscarotid arteries (the correlation coefficients r for therespectiveTAV, luminal diameter and flow volumesamounted to 0.62, 0.74, 0.55 in the CCA, 0.53, 0.60, 0.38in the ECA, 0.55, 0.51, 0.41 in the ICA;p , 0.001 for allparameters). In the vertebral arteries, no significant side-to-side correlation was found.

1262 Ultrasound in Medicine and Biology Volume 26, Number 8, 2000

An age-dependent decline in all flow velocities wasfound in the CCA, the ICA and the VA and, in the ECA,only the end-diastolic flow velocity decreased signifi-cantly with age (see Table 1). There was a significantincrease in the resistance index (but not the pulsatilityindex) in the ICA and VA with increasing age. Theluminal diameter of the VA increased slightly with age.Only in the ICA and in the CCA, but not in the VA andthe ECA, did the flow volume decrease significantlyduring ageing (Fig. 1, Table 1).

When the whole study group was divided into threegroups (20 to 39 y, 40 to 59 y, 60 to 85 y), no significantage-related changes in flow volume could be foundwithin these subgroups in any of the extracranial arteries.Reference data covering all the parameters of all thearteries for these age groups are shown in Table 2.

DISCUSSION

To our knowledge, only two analogous studies ex-ist. In a first paper on flow volume measurements in allthe extracranial arteries, Scho¨ning et al. (1994) investi-gated a slightly inhomogeneous group of healthy adultsbetween 20 and 63 y old. In a further study on a group ofchildren and adolescents equally distributed for age andgender, the natural development of these parametersbetween 3 and 18 y old could be shown (Scho¨ning andHartig 1998).

Comparable data exist for some aspects of thepresent study. Similar gender-related differences in theluminal diameter of the CCA (Donis et al. 1988; Marosiand Ehringer 1984; Weskott and Holsing 1997; Zborni-kova and Lassvik 1986), the ECA (Marosi and Ehringer1984; Zbornikova and Lassvik 1986) and the ICA (Doniset al. 1988; Marosi and Ehringer 1984; Zbornikova andLassvik 1986) were found by other groups. A largerluminal diameter of the VA in males than in females(Zbornikova and Lassvik 1986) could not be confirmedin our cohort. In contrast to our data, Mu¨ller et al. (1987)found a significantly higher CCA flow volume in men. Inthe present study, the only gender-linked difference in

flow volume is found in the ECA, where the flow volumerate is higher in men. To date, there are no similarobservations in the literature, and we have no physiolog-ical explanation for this phenomenon.

As in the previous study on healthy children andadolescents (Scho¨ning and Hartig 1998), there were norelevant side-to-side differences in any of the parametersin the extracranial carotid arteries, and a significant sidecorrelation of the parameters concerning flow volumemeasurement could be found. In contrast to these find-ings, Donis et al. (1988) and Zbornikova and Lassvik(1986) described higher flow velocities in the left CCAthan in the right.

Different conclusions are reached about the side-to-side differences in the luminal diameter of the vertebralartery. Some authors have found that the right VA wassignificantly smaller (Delcker and Diener 1992; Scho¨n-ing and Hartig 1998; Simon et al. 1994), and othersdescribed a significantly larger diameter in the right VA(Bendick and Glover 1990; Pfadenhauer and Mueller1995). In the present study, no side-to-side differences inluminal diameter (or, indeed, in any other flow parame-ter) could be found in the vertebral arteries. As in aprevious report by Scho¨ning and Walter (1992), the sidecorrelation of the flow volume parameters (d, TAV, FV)was low or even negative in the vertebral arteries. Asym-metry of the luminal diameter and of the flow volumeseems to be more the rule than the exception in thevertebral arteries.

The term “VA hypoplasia” is not yet definedclearly. In different reports on healthy subjects, the rateof unilateral VA hypoplasia ranges from 1.9 to 9.5%(Bartels 1991; Delcker and Diener 1992; Scho¨ning et al.1994; Scho¨ning and Hartig 1998; Touboul et al. 1986;Trattnig et al. 1990). Some of the authors define VAhypoplasia as a luminal diameter of less than 3 mm(Bartels 1991; Touboul et al. 1986), but others require aluminal diameter of less than 2.0 mm (Delcker andDiener 1992; Scho¨ning et al. 1994). A flow volumebelow 20 mL/min was set as an additional criterion by

Table 1. Age-dependence of flow velocities, waveform parameters, vessel diameters and flow volumes

Vessel Vs Ved TAV TAMX RI PI d Flow Vol

CCA 20.46‡ 20.48‡ 20.37† 20.33* 0.23 20.02 0.16 20.28†

ICA 20.41† 20.60‡ 20.41† 20.40† 0.40† 0.19 20.01 20.45‡

ECA 20.17 20.31† 0.03 0.06 0.22 20.13 0.16 0.18VA 20.31† 20.56‡ 20.49‡ 20.33† 0.29* 0.18 0.33* 20.16

Sperman’s rank correlation coefficient is indicated.Vs 5 peak systolic velocity;Ved 5 maximum end-diastolic velocity;TAV 5 time-averaged velocity;TAMX 5 time-averaged

maximum velocity;RI 5 resistance index5 [(Vs2 Ved)/Vs]; PI 5 pulsatility index5 [(Vs2 Ved)/TAMX]; d 5 diameter of the vessel;Flow Vol 5 flow volume; CCA5 common carotid artery; ICA5 internal carotid artery; ECA5 external carotid artery; VA5vertebral artery. *p , 0.01; †p , 0.001; ‡p , 0.0001.

Flow volume measurements in the extracranial carotid and vertebral arteries● P. SCHEEL et al. 1263

Schoning and Hartig (1998). In the present study, a VAdiameter of less than 2 mm was found in 2 subjects(2.5%), and a unilateral VA flow volume of less than 20mL/min was found in 7 cases (9%;cf. Fig. 1). There wasno sign of vertebrobasilar insufficiency in any of thesesubjects. Therefore, we think that even a pronounced VAasymmetry can be regarded as a normal variant.

As to the age-dependent decline in flow velocitiesfound in this study, other groups have described a com-parable decrease in flow velocities in the CCA (Uematsuet al. 1983) and the ICA (Donis et al. 1988; Zbornikovaand Lassvik 1986), as well as in the VA (Pfadenhauerand Mueller 1995; Zbornikova and Lassvik 1986) withincreasing age. These findings are also consistent with anage-dependent flow velocity decrease found in the intra-cranial basal cerebral arteries (Aaslid et al. 1982;Grolimund and Seiler 1988; Krejza et al. 1999; Martin1994; Tsuchiya et al. 1991).

Only in the VA did we find an age-dependent in-crease in luminal diameter in our study. A comparableincrease was found in 1986 by Zbornikova and Lassvik(1986). In contrast to our data, some groups found anincrease in the luminal diameter of the ICA (Donis et al.1988; Zbornikova and Lassvik 1986), the ECA (Zborni-kova and Lassvik 1986) and the CCA (Donis et al. 1988;Samijo et al. 1998; Zbornikova and Lassvik 1986).

In our study group, a significant decrease in ICAflow volume with age could be attributed to a markeddecrease inTAV while the luminal diameter remainedconstant. These findings agree with those of other studiesthat found a decrease in flow volume with age in theCCA and the ICA (Donis et al. 1988; Uematsu et al.1983; Muller et al. 1987). Parallel with the decrease inflow volume in the ICA, a reduction in CBF volume withage could also be demonstrated in the same population(Scheel et al. 2000).1

In previously published studies, flow volumesranged from 300 to 574 mL/min in the CCA and from245 to 339 mL/min in the ICA (see Table 2). Similarvalues for flow volumes in the VA and the ECA (84633 vs. 796 24 mL/min, 1606 66 vs. 1646 56 mL/min)

1Transcranial colour duplex and global cerebral blood flow mea-surements were performed in the same study group. Some of the resultsof these distinct study parts have been published separately (Scheel etal. 2000).

Fig. 1. Development of flow volumes in the extracranial carotidand vertebral arteries from 20 to 85 y. Scatterplots show the flowvolume measurements and the correlation analyses with age in thecommon carotid arteries (CCA), external carotid arteries (ECA),internal carotid arteries (ICA) and the verebral arteries (VA) on

either side of each subject between 20 and 85 y old.

1264 Ultrasound in Medicine and Biology Volume 26, Number 8, 2000

were described by Scho¨ning et al. (1994) but, in contrast,they found an increase in flow volume in the CCA andthe ECA with age.

The reasons for the large spread of estimated flowvolumes with the different Doppler sonography tech-niques are numerous, and several sources of errors inflow volume estimation have been described (Gill 1985;Hoskins 1990; Smith 1984). To minimise these errors,the examiner should be familiar with all the possiblesources of error. Furthermore, it must be stressed that thereliability of measurements is highly dependent on thetechnical skills of the examiner, and that a meticulousmeasurement technique has to be observed.

The main finding of our study group is a significantage-dependence of flow velocities and waveform param-eters. This was the reason why we formed different agegroups to supply the reference data. The reference dataprovided here, combined with the recently published datafrom other reports (Scho¨ning et al.1993, 1994; Scho¨ningand Hartig 1996, 1998) now give us the means to surveythe physiological evolution of the extracranial brain-supplying arteries from 3 to 85 y old. They also pave theway for a broader clinical and scientific application ofthis method in determining flow volumes. A combinationwith transcranial colour duplex examination of the intra-cranial arteries optimises the diagnostic possibilities and

Table 2. Reference data of flow velocities, waveform parameters, luminal diameters and flow volumes inextracranial arteries of different age groups

Vessel n Angle (°) Vs (cm/s) Ved (cm/s) TAV (cm/s) TAMX (cm/s) RI PI d (mm) FV (mL/min)

CCA (20–39) 24 656 2 1016 22 256 5 256 5 406 6 0.746 0.05 1.896 0.39 6.06 0.7 4266 99CCA (40–59) 24 646 3 896 17 266 5 256 5 426 7 0.716 0.06 1.516 0.37 6.16 0.8 4346 111CCA (60–85) 30 606 6 816 21 206 7 216 6 366 10 0.766 0.05 1.756 0.31 6.26 0.9 3736 80ECA (20–39) 24 616 5 866 14 166 4 196 3 306 5 0.816 0.04 2.326 0.46 4.06 0.4 1456 32ECA (40–59) 24 606 5 856 18 196 6 226 5 356 7 0.776 0.05 1.906 0.43 4.16 0.7 1756 73ECA (60–85) 30 546 6 816 30 156 6 206 7 336 11 0.826 0.05 2.066 0.39 4.36 0.7 1706 52ICA (20–39) 24 586 5 726 18 266 5 266 5 396 7 0.626 0.07 1.166 0.30 4.86 0.5 2776 49ICA (40–59) 24 596 4 656 10 266 5 256 5 386 6 0.606 0.06 1.046 0.20 4.76 0.6 2546 57ICA (60–85) 30 526 5 586 11 206 5 216 6 336 8 0.666 0.05 1.206 0.21 4.96 0.8 2246 43VA (20–39) 24 626 5 526 6 176 3 176 3 266 4 0.686 0.05 1.376 0.24 3.36 0.3 876 20VA (40–59) 24 606 4 476 8 156 3 146 2 246 4 0.676 0.08 1.386 0.44 3.26 0.4 746 18VA (60–85) 30 566 7 456 11 126 3 126 4 226 5 0.726 0.07 1.506 0.36 3.66 0.4 786 29

All parameters are mean6 SD. Angle indicates angle of course of vessel to Doppler beam.Vs 5 peak systolic velocity;Ved 5 maximumenddiastolic velocity;TAV 5 time-averaged velocity;TAMX 5 time-averaged maximum velocity;RI 5 resistance index [(Vs 2 Ved)/Vs]; PI 5pulsatility index [(Vs2 Ved)/TAMX]; d 5 luminal diameter of the vessel;FV 5 flow volume; CCA5 common carotid artery; ECA5 external carotidartery; ICA 5 internal carotid artery; VA5 vertebral artery; 20–395 age group from 20 to 39 y; 40–595 age group from 40 to 59 y; 60–855age group from 60 to 85 y.

Table 3. Published results of ultrasound-based flow volume in the CCA, the ICA, the ECA and the VA

Authors (Year)Ultrasoundtechnique n Age (y) Vessel

Flow volume(mL/min)

Age-dependence

Keller et al. (1976) QFM 22 23–45 CCA 300–480 NMFitzgerald et al. (1982) QFM 25 42 CCA 5366 104 NMUematsu et al. (1983) QFM 16 21–40 CCA 4796 90 2

14 41–60 CCA 4336 69Mueller et al. (1984) QFM 100 16–65 CCA 4646 75 2Leopold et al. (1987) TAV 20 32 ICA 2546 56 NMDonis et al. (1988) TAV 116 16–78 –

16–19 CCA 4006 27 270–78 CCA 3226 114 2

Fortune et al. (1992) TAV 20 33 ICA 3306 19 NMHamada et al. (1993) TAV 28 716 7 CCA 574 7Schoning et al. (1994) TAV 46 20–63 CCA 4706 120 1

ICA 2656 26 7ECA 1606 66 1VA 84 6 33 7

Weskott and Holsing (1997) TDP 174 20–87 CCA 4156 87 NM

CCA 5 common carotid artery; ECA5 external carotid artery; ICA5 internal carotid artery; VA5 vertebral artery; QFM5quantitative flow measurement;TAV5 time-averaged velocity;TDP 5 time domain processing; NM5 not mentioned;7 5 no agedependence;2 5 decrease of flow volume with age;1 5 increase of flow volume with age.

Flow volume measurements in the extracranial carotid and vertebral arteries● P. SCHEEL et al. 1265

can lead to a better understanding of cerebral perfusionin healthy and pathologic situations such as arterio-venous malformations, stenoses or dissections andstrokes.

Acknowledgements—The authors are indebted to C. Meisner for hisexpert assistance in the statistical evaluation of the data. This study wassupported by the Deutsche Forschungsgemeinschaft (DFG).

REFERENCES

Aaslid R, Markwalder TM, Nornes H. Noninvasive transcranial Dopp-ler ultrasound recording of flow velocity in basal cerebral arteries.J Neurosurg 1982;57:769–774.

Bartels E. Duplexsonographie der Vertebralarterien. 2. Teil: KlinischeAnwendungen. Ultraschall Med 1991;12:63–69.

Bendick PJ, Glover JL. Hemodynamic evaluation of vertebral arteriesby duplex ultrasound. Surg Clin North Am 1990;70:235–244.

Delcker A, Diener HC. Die verschiedenen Ultraschallmethoden zurUntersuchung der Arteria Vertebralis—eine vergleichende Wer-tung. Ultraschall Med 1992;13:213–220.

Donis J, Graf M, Sluga E. Flussmessungen an den extrakraniellenKarotiden mit Hilfe der Duplex-Sonographie. Ergebnisse bei Nor-malpersonen. Ultraschall Med 1988;9:216–222.

Fitzgerald DE, O’Shaugnessy AM, Keaveny VT. Pulsed Doppler:Determination of blood velocity and volume flow in normal anddiseased common carotid arteries in man. Cardiovasc Res 1982;16:220–224.

Fortune JB, Bock D, Kupinski AM, et al. Human cerebrovascularresponse to oxygen and carbon dioxide as determined by internalcarotid artery duplex scanning. J Trauma 1992;32:618–627.

Gill RW. Measurement of blood flow by ultrasound: Accuracy andsources of error. Ultrasound Med Biol 1985;11:625–641.

Grolimund P, Seiler RW. Age dependence of the flow velocity in thebasal cerebral arteries—a transcranial Doppler ultrasound study.Ultrasound Med Biol 1988;14:191–198.

Hamada T, Takita M, Kawano H, Noh tomi A, Okayama M. Differencein blood flow volume of the common carotid artery between vas-cular and non-vascular dementia detected by colour duplex sonog-raphy. J Neurol 1993;240:191–194.

Hoskins PR. Measurement of arterial blood flow by Doppler ultra-sound. Clin Phys Physiol Meas 1990;11:1–26.

Keller HM, Meier WE, Anliker M, Kumpe DA. Noninvasive measure-ment of velocity profiles and blood flow in the common carotidartery by pulsed Doppler ultrasound. Stroke 1976;7:370–377.

Krejza J, Mariak Z, Walecki J, et al. Transcranial color Dopplersonography of basal cerebral arteries in 182 healthy subjects: Ageand sex variability and normal reference values for blood flowparameters. Am J Roentgenol 1999;172:213–218.

Leopold PW, Shandall AA, Feustel P, et al. Duplex scanning of theinternal carotid artery: An assessment of cerebral blood flow. Br JSurg 1987;74:630–633.

Marosi L, Ehringer H. Die extrakranielle Arteria carotis im hochau-flosenden Ultraschallechtzeit-Darstellungssystem: MorphologischeBefunde bei gesunden Erwachsenen. Ultraschall Med 1984;5:174–181.

Martin PJ, Evans DH, Naylor AR. Transcranial color-coded sonogra-phy of the basal cerebral circulation. Reference data from 115volunteers. Stroke 1994;25:390–396.

Mueller HR, Radue EW, Palotti C, Gratzl O. Common carotid CWDoppler flow measurement in neurovascular surgery. In: Kurjak A,Kossoff G, eds. Recent advantages in ultrasound diagnosis. Am-sterdam: Elsevier, 1984:17–36.

Mueller HR, Radue EW, Buser M, Spencer MP, eds. Ultrasonic diag-nosis of cerebrovascular disease. Dordrecht Boston Manchester:Martinus Nijhoff Publishers, 1987:87–102.

Pfadenhauer K, Mueller H. Farbkodierte Duplexsonographie der Arte-ria vertebralis: Normalbefunde und pathologische Befunde bei Ob-struktionen an der Arteria vertebralis und den u¨brigen hirnversor-genden Arterien. [Color-coded duplex ultrasound of the vertebralartery: Normal findings and pathologic findings in obstruction ofthe vertebral artery and remaining cerebral arteries.] UltraschallMed 1995;16:228–233.

Samijo, SK, Willigers JM, Barkhuysen R, Kitslaar PJ, Reneman RS,Brands PJ, Hoeks AP. Wall shear stress in the human commoncarotid artery as function of age and gender. Cardiovasc Res 1998;39:515–522.

Scheel P, Ruge C, Scho¨ning M. Color duplex measurement of cerebralblood flow volume in healthy adults. Stroke 2000;31:147–150.

Schoning M, Hartig B. Age dependence of total cerebral blood flowvolume from childhood to adulthood. J Cereb Blood Flow Metab1996;16:827–833.

Schoning M, Hartig B. The development of hemodynamics in theextracranial carotid and vertebral arteries. Ultrasound Med Biol1998;24:655–662.

Schoning M, Walter J. Evaluation of the vertebrobasilar-posteriorsystem by transcranial color duplex sonography in adults. Stroke1992;23:1280–1286.

Schoning M, Staab M, Walter J, Niemann G. Transcranial color duplexsonography in childhood and adolescence. Age dependence of flowvelocities and waveform parameters. Stroke1993;24:1305–1309.

Schoning M, Walter J, Scheel P. Estimation of cerebral blood flowthrough color duplex sonography of the carotid and vertebral ar-teries in healthy adults. Stroke 1994;25:17–22.

Simon H, Niederkorn K, Horner S, Duft M, Schrockenfuchs M. Ein-fluss der Halsdrehung auf das vertebrobasila¨re System. Ein transk-raniell-dopplersonographischer Beitrag zur Physiologie. [Effect ofhead rotation on the vertebrobasilar system. A transcranial Dopplerultrasound contribution to the physiology.] HNO 1994;42:614–618.

Smith HJ. Quantitative Doppler flowmetry. II. Reliability of a duplexscanning system under in vitro conditions. Acta Radiol Diagn1984;25:535–543.

Touboul PJ, Bousser MG, LaPlane D, Castaigne P. Duplex scanning ofnormal vertebral arteries. Stroke 1986;17:921–923.

Trattnig S, Hubsch P, Schuster H, Po¨lzleitner D. Color-coded Dopplerimaging of normal vertebral arteries. Stroke 1990;21:1222–1225.

Tsuchiya T, Yasaka M, Yamaguchi T, Kimura K, Omae T. Imaging ofthe basal cerebral arteries and measurement of blood velocity inadults by using transcranial real-time color flow Doppler sonogra-phy. AJNR 1991;12:497–502.

Uematsu S, Yang A, Preziosi TJ, Kouba R, Toung TJ. Measurement ofcarotid blood flow in man and its clinical application. Stroke1983;14:256–266.

Weskott HP, Holsing K. US-based evaluation of hemodynamic param-eters in the common carotid artery: A nomogram trial. Radiology1997;205:353–359.

Zbornikova V, Lassvik C. Duplex scanning in presumably normalpersons of different ages. Ultrasound Med Biol 1986;12:371–378.

1266 Ultrasound in Medicine and Biology Volume 26, Number 8, 2000