J Appl Physiol 94: 1802–1805, 2003.
First published January 10, 2003; 10.1152/japplphysiol.00782.2002.
Extrajugular pathways of human cerebral venous blood
drainage assessed by duplex ultrasound
Stephan J. Schreiber,1 Frank Lürtzing,1 Rainer Götze,1
Florian Doepp,1 Randolf Klingebiel,2 and José M. Valdueza1
1
Department of Neurology and 2Neuroradiological Section, Department of Radiology,
University Hospital Charité, Humboldt University, 10098 Berlin, Germany
Submitted 26 August 2002; accepted in final form 2 January 2003
Schreiber, Stephan J., Frank Lürtzing, Rainer
Götze, Florian Doepp, Randolf Klingebiel, and José M.
Valdueza. Extrajugular pathways of human cerebral venous
blood drainage assessed by duplex ultrasound. J Appl
Physiol 94: 1802–1805, 2003. First published January 10,
2003; 10.1152/japplphysiol.00782.2002.—Cerebral venous
drainage in humans is thought to be ensured mainly via the
internal jugular veins (IJVs). However, anatomic, angio-
graphic, and ultrasound studies suggest that the vertebral
venous system serves as an important alternative drainage
route. We assessed venous blood volume flow in vertebral
veins (VVs) and IJVs of 12 healthy volunteers using duplex
ultrasound. Measurements were performed at rest and dur-
ing a transient bilateral IJV and a circular neck compression.
Total venous blood volume flow at rest was 766 ⫾ 226 ml/min
(IJVs: 720 ⫾ 232, VVs: 47 ⫾ 33 ml/min). During bilateral IJV
compression, VV flow increased to 128 ⫾ 64 ml/min. Circular
neck compression, causing an additional deep cervical vein
obstruction, led to a further rise in VV volume flow (186 ⫾ 70
ml/min). As the observed flow increase did not compensate
for IJV flow cessation, other parts of the vertebral venous
system, like the intraspinal epidural veins and the deep
cervical veins, have to be considered as additional alternative
drainage pathways.
blood volume flow; vertebral veins; deep neck veins; internal
jugular veins
THE INTERNAL JUGULAR VEINS (IJVs) are thought to repre-
sent the main outflow pathway for cerebral venous
blood in humans. However, the clinical observation
that bilateral resection of the IJV is usually well toler-
ated suggests the presence of alternative, nonjugular
pathways (9). Such a route exists in the form of the
anatomically complex vertebral venous system (1, 7, 8,
16). Part of this system are the vertebral veins (VVs),
which have been shown to serve as venous collaterals
in cases of jugular flow obstruction (5, 9). A recent
ultrasound study of healthy volunteers demonstrated
that the pattern of cerebral venous drainage changes,
even under physiological conditions, depending on the
body position (23). Whereas flow in the IJVs dominated
in the supine position, a marked jugular flow reduction
and a concomitant flow rise in the VVs were seen when
the subjects changed into the erect body position. How-
Address for reprint requests and other correspondence: S. J. Schrei-
ber, Dept. of Neurology, Univ. Hospital Charité, Schumannstrasse
20/21, 10098 Berlin, Germany (E-mail: Stephan.Schreiber@charite.de).
1802 8750-7587/03 $5.00 Copyright © 2003 the American Physiological Society
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ever, the magnitude of flow increase in the VVs did not
match the decrease measured in the IJVs. The authors,
therefore, posed the hypothesis that alternative path-
ways, like the spinal epidural veins as a part of the
internal vertebral venous system, might have been the
reason for the observed difference (23). In addition, the
deep cervical veins and other ultrasound inaccessible
parts of the external vertebral venous system have to
be considered (1, 4). To study the potential role of the
deep neck veins, venous blood volume flow (VBVF) was
measured by duplex ultrasound in both VVs during
bilateral IJV and during circular neck compression.
MATERIALS AND METHODS
The study was conducted in 12 volunteers [3 women, 9
men, age 29 ⫾ 6 (SD) years], free of cardiovascular disease.
All subjects gave informed consent. Color-coded duplex
sonography was performed by using a 3- to 11-MHz linear
transducer (HP Sonos 5500, Hewlett Packard). Insonation
was carried out in a head straight and supine body position
at a midcervical level during normal breathing of the pro-
bands. VBVF was calculated as described previously (13, 14,
20, 23) by multiplication of vessel area and time-averaged
velocity (mean of all frequencies over two to three heart
cycles) by using the HP Sonos 5500 software (Fig. 1). In case
of marked respiratory variations of time-averaged velocity
and vessel cross-sectional area (CSA), measurements were
performed during brief apnea after a normal expiration. The
CSA of the IJV was measured in the horizontal plane by
using the B-mode image, whereas VV-CSA was calculated
from VV diameters obtained in the sagittal plane, assuming
a circular vessel shape. VBVF at rest was assessed in both
IJVs and VVs. Additional VBVF measurements were then
carried out in the VVs during a transient complete blood flow
obstruction of both IJV, lasting ⬃1–2 min. Flow cessation,
confirmed by duplex ultrasound, was achieved by applying a
constant manual pressure on both IJVs at the submandibu-
lar level. A third VV flow analysis was performed during
circular neck compression at the same level by using an
elastic band. This procedure also led to IJV flow cessation.
For statistical analysis, nonparametric repeated-measures
ANOVA (Friedman test) and Dunn’s multiple-comparison
posttest were performed. A P value of ⬍0.05 was considered
significant.
The costs of publication of this article were defrayed in part by the
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 EXTRAJUGULAR PATHWAYS OF CEREBRAL VENOUS BLOOD DRAINAGE 1803

sum of VV and IJV volume flow at rest, was 766 ⫾ 226

ml/min, ranging from 390 to 1,130 ml/min. The IJVs
contributed 94% (720 ⫾ 232 ml/min) and the VVs 6%
(47 ⫾ 33 ml/min) of total VBVF (Table 1). The following
compression tests led to a significant VV flow increase
(P ⬍ 0.0001). Bilateral manual IJV compression re-
sulted in a VV flow of 128 ⫾ 64 ml/min (P ⬍ 0.05),
comprising now 17% of the total VBVF. The circular
compression led to a further nonsignificant mean flow
rise (186 ⫾ 70 ml/min, P ⬎ 0.05, 24% of total VBVF).
This increase, however, was only seen in 7 of the 12
subjects.

DISCUSSION

Although the extracranial portion of the arterial

Fig. 1. Example of blood volume flow measurements in 1 subject.
Right and left vertebral vein (VV) at rest, during bilateral jugular
vein compression (comp 1), and during circular neck compression
(comp 2) are shown.
Two volunteers (subjects 6 and 7) were additionally stud-
ied by venous magnetic resonance angiography (Magnetom
Vision, 1.5 T, Siemens, Germany) during manual jugular
vein compression to analyze whether flow changes in the
nonjugular venous system could be visualized. For data ac-
quisition, a saturated FLASH two-dimensional sequence was
used (repetition time 33 ms, echo time 9 ms, one signal
acquired, 3-mm slice thickness, 260-mm field of view, 192 ⫻
256 pixel matrix).
RESULTS
All vessels were successfully insonated at rest and
during the two modes of venous compression (Fig. 1).
Compression tests were well tolerated, with subjects
mainly noticing the applied neck pressure and some
degree of facial swelling but no other side effects like
headaches or visual disturbances. IJV flow cessation
during circular neck compression was achieved by a
mean neck circumference reduction of 4.5 cm (range
3–7 cm). Mean total venous outflow, calculated as the
cerebral inflow has been investigated in detail by dif-
ferent modalities, only little attention has been paid to
the venous drainage of the brain. The IJVs have been
considered to present the most important pathway for
venous blood returning from the brain. This assump-
tion was based on angiographic studies and cerebral
blood flow analyses with nitrous oxide, labeled eryth-
rocytes, and thermodilution techniques (12, 21, 15, 25),
which were all performed in a supine body position.
However, anatomic investigations as well as clinical
observations in patients after bilateral radical neck
dissection suggest coexisting IJV-independent alterna-
tive venous drainage pathways (9).
Venous anatomy. The main jugular blood drainage
pathway leads from the superior sagittal and the
transverse sinuses via the sigmoid sinuses into the
IJVs, which meet the superior cava vein via the bra-
chiocephalic vein. Competent valves usually impede
retrograde flow in the IJV. In contrast, the vertebral
venous system forms a freely communicating, valveless
“network” of longitudinal and transverse venous ves-
sels. It consists of an internal part, the intraspinal
epidural venous plexus, and an external paravertebral
part, both continuing throughout the entire length of
the spinal column. The system communicates with
deep thoracic and lumbar veins, intercostal veins, azy-
gos and hemiazygos veins, as well as with the inferior

Table 1. Individual IJV and VV blood volume flow measurements

Total IJV at Total VV at Total VV comp 1, Total VV comp 2,
Subject No. Age, yr Gender Rest, ml/min Rest, ml/min ml/min ml/min

1 24 F 450 110 180 320

2 29 M 340 50 100 100
3 44 F 670 50 110 240
4 30 M 440 30 110 130
5 28 M 1,060 20 160 240
6 30 M 730 90 310 300
7 36 M 810 90 90 190
8 35 M 890 20 120 130
9 24 M 1,110 30 100 150
10 27 M 620 0 40 140
11 23 F 640 10 120 120
12 23 M 880 60 100 170
Mean ⫾ SD 29 ⫾ 6 720 ⫾ 232 47 ⫾ 33 128 ⫾ 64 186 ⫾ 70
IJV, internal jugular vein; VV, vertebral vein; M, male; F, female. Total IJV flow is shown at rest. Total VV flow is shown at rest and during
bilateral manual IJV compression (comp 1) and circular neck compression (comp 2).

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1804 EXTRAJUGULAR PATHWAYS OF CEREBRAL VENOUS BLOOD DRAINAGE

vena cava (6, 7, 1). The VVs represent the main longi-
tudinal part of the external vertebral venous system.
VVs and the deep cervical veins, which are located
within the muscle layers of the nape, receive inflow
from the marginal and sigmoid sinuses via condylar
veins and emissaries and from the venous plexus sur-
rounding the foramen magnum (2, 10, 16, 24). In ad-
dition, there are several frequently segmental connec-
tions between the internal and external parts of the
vertebral venous system. VVs, deep cervical veins, and
the external jugular vein finally join the brachioce-
phalic vein. The CSA of the internal vertebral venous
system at scull base level has been estimated to reach
up to one-fourth of the combined jugular CSA, whereas
the total CSA of the vertebral venous system might
even surpass that of both IJVs (3, 4).
Ultrasound assessment of VBVF. In the midcervical
region, IJVs and VVs are easily accessible by duplex
ultrasound (11, 13, 14, 23). The presented VBVF mea-
surements are in good agreement with previously ob-
tained ultrasound data. Different research groups
found a combined mean IJV flow of 740 ⫾ 209 and
700 ⫾ 270 ml/min (14, 23) and a mean VV flow of 40 ⫾
20 ml/min (23) in the supine body position. The acces-
sible total mean venous outflow of 766 ⫾ 226 ml/min in
our group of healthy volunteers corresponds well with
ultrasound assessed global arterial inflow, which has
been reported within the range of ⬃500–950 ml/min
(18–20) and with a mean value of 727 ⫾ 102 ml/min for
subjects aged 20–39 yr (17). Therefore, the IJVs have Fig. 2. Magnetic resonance sagittal slice at the submandibular level
to be considered the main outflow pathways in the in subjects 6 (A and B) and 7 (C and D). A and C: resting condition.
supine position. This, however, was shown to change B and D: manual bilateral internal jugular vein compression. Solid
arrows outlined in white, internal jugular veins; shaded arrows
completely when the subjects turned into the upright outlined in white, external jugular veins; white arrows with solid
position, as IJV flow fell from 700 ⫾ 270 to 70 ⫾ 100 arrowheads, VVs; white arrows with nonsolid arrowheads, deep
ml/min in a group of volunteers, whereas VV rose from cervical veins; small shaded arrows, intraspinal vertebral system.
40 ⫾ 20 to 210 ⫾ 120 ml/min, leaving an unexplained Note the differently developed deep neck veins between A and C at
remaining mean difference of ⬃450 ml/min (23). In our rest and under compression.
study, a complete IJV flow cessation was ensured by
bilateral manual compression. This indeed caused the all, the additional cervical vein obstruction led to a
expected VV increase (mean 82 ⫾ 57 ml/min). Interest- further VV flow increase of 58 ⫾ 53 ml/min (range: ⫺10
ingly, individual values varied greatly from 220 ml/min to 140 ml/min), yielding VV flow values compensating
(subject 6) to one subject without a detectable flow rise 19% (one-fifth) of the jugular drainage capacity. A
(subject 7). Venous magnetic resonance angiography in similar VV capacity of 26% (one-fourth of jugular
subject 6 showed bilateral prominent IJVs at rest and venous flow) was seen within the upright body posi-
a noticeable signal increase in both VV as well as the tion (23).
deep cervical veins during IJV compression (Fig. 2). In For interpretation of these data, a number of tech-
contrast, subject 7 demonstrated multiple cervical nical limitations as well as anatomic-specific charac-
veins at rest that showed a pronounced signal increase teristics of the insonated vessels have to be considered.
during compression. These veins probably explain why An unintentional concomitant carotid artery compres-
no ultrasonographic VV flow increase could be detected sion could, for instance, lead to a reduced arterial
during the bilateral IJV compression. However, circu- inflow and subsequent overestimation of the diverted
lar neck compression in this subject did result in a VV venous flow. However, this seems very unlikely as the
flow increase of 100 ml/min, confirming the predomi- applied jugular pressure was low, and B-mode in-
nating nonjugular pathway via the deep cervical veins. sonation of the carotid CSA during compression did not
In contrast, nonjugular drainage patterns in subject 6 show vessel deformation. In our VBVF measurements,
seem mainly to follow the VVs as fewer deep cervical a circular-shaped VV was postulated for flow calcula-
veins could be visualized. Combined with a deeper tions, whereas real vessel CSA at rest is probably
location of the cervical veins, predominantly surround- noncircular in most cases, changing into a more circu-
ing the splenius capiti muscles, circular neck compres- lar shape due to an intraluminal pressure rise during
sion probably did not result in any significant flow the compression tests (Fig. 2). This might have led to
obstruction, explaining the absent VV flow rise. Over- an under- or overestimation of VV flow, especially at
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 EXTRAJUGULAR PATHWAYS OF CEREBRAL VENOUS BLOOD DRAINAGE
rest. Furthermore, known venous anatomic variations,
like the doubling of VVs, might have been overlooked
or missed in our approach. However, even considering
these potential systematic errors, ⬎50% of jugular
blood flow seems to follow other routes so that the VVs
are unlikely to be the main nonjugular drainage path-
way. Our results suggest that the deep cervical veins
represent one of the relevant additional alternative
pathways, particularly as they turned out to be the
most prominent veins besides the VVs on our MRI
scans, all together probably extending the CSA of the
VV. The only moderate further VV flow increase during
circular neck compression (8% of total jugular flow) is
probably due to a limited compression effect on deep
cervical veins caused by their anatomic location (Fig.
2). This hypothesis is further supported by case reports
of patients in whom intraspinal pressure studies were
performed by lumbar puncture after bilateral radical
neck dissection (22). Under application of bilateral
manual pressure to the cervical muscle bed, the regis-
tered pressure in two patients rose from 22 and 25
cmH2O to 65 and 60 cmH2O, respectively (22).
Finally, the intraspinal epidural system, already
demonstrating a flow increase during IJV compression
on MRI, has to be considered. The distribution between
these two compartments remains unclear, as no vali-
dated technique exists to directly assess blood flow
within these regions.
In conclusion, we have shown in a group of young
healthy volunteers that powerful additional venous
pathways besides the IJVs exist and may compensate
for IJV flow cessation. The VVs as important parts of
the vertebral venous system are probably not the main
nonjugular drainage pathway. Instead, the variably
developed deep cervical veins as well as the intraspinal
epidural venous system have to be considered. Knowl-
edge of the individual venous drainage patterns might
be of clinical relevance in patients undergoing IJV
resection or patients suffering from raised intracranial
pressure.
We thank Bianca Müller for assistance in performing the MRI
scans.
The study was supported by a grant from the Schering For-
schungsgesellschaft (Berlin, Germany).
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