AJR 2001; 176:1059-1065
© American Roentgen Ray Society
Topographic Anatomy of the Vertebral Venous System in the Thoracic Inlet
Kenji Ibukuro1,
Hozumi Fukuda,
Koichi Mori and
Yoshihiro Inoue
1
All authors: Department of Radiology, Mitsui Memorial Hospital, 1-Kanda
Izumicho Chiyoda-ku, Tokyo 101-8643, Japan.
Received August 14, 2000;
accepted after revision September 15, 2000.
Address correspondence to K. Ibukuro.
Introduction
The vertebral venous system in the thoracic inlet consists of the vertebral
veins and perivertebral venous plexuses such as the anterior and posterior
external plexuses and the internal plexus. Metastatic tumors can appear in
locations that do not seem to be in the line of direct spread from their
primary focus, which is called paradoxical metastasis. The vertebral venous
system is well known as the pathway of paradoxical metastasis, as in bone
metastases in patients with prostate cancer and breast cancer, which was
reported by Batson [1] on the
basis of cadaver and animal injection experiments in 1940. Anderson
[2] proved that contrast
material backs up into the deep cervical veins, and that the vertebral venous
system is shown on upper extremity venography when intrathoracic pressure is
elevated, as during Valsalva's maneuver. The clinical significance of the
vertebral venous system as collateral vessels is also recognized in patients
with upper extremity venous thrombosis
[3] and various other
conditions [4].
In this pictorial essay, we illustrate the topographic anatomy of the
vertebral venous system in the thoracic inlet as shown on CT scans in patients
with venous stenosis and in cadaver dissections (Fig.
1A,1B).
We describe the clinical significance of recognizing this venous system.
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Fig. 1A. —Diagrams of vertebral venous system in thoracic inlet.
Anterior view. Az = azygos vein, EDV = epidural venous plexus, DCV = deep
cervical vein, IVV = intervertebral vein, LBCV = left brachiocephalic vein,
LPV = longitudinal prevertebral vein, RSICV = right superior intercostal vein,
VV = vertebral vein, ICV = intercostal vein. Asterisk indicates esophageal
veins, dotted line indicates peripheral branches of deep cervical vein in back
neck.
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Fig. 1B. —Diagrams of vertebral venous system in thoracic inlet. Axial
view. A = anterior epidural venous plexus, B = basivertebral veins, C =
musculus longissimus colli, D = deep cervical veins, I = intervertebral veins,
L = longitudinal prevertebral veins, P = posterior epidural venous plexus, S =
musculus semispinalis cervicis, V = vertebral veins.
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Vertebral Veins
The cervical vertebral vein accompanies the vertebral artery in the
transverse process foramen in the upper cervical vertebrae, emerges from the
transverse process foramen of the sixth cervical vertebra, joins the deep
cervical vein [5], descends
laterally, then drains into the upper portion of the brachiocephalic vein.
The cervical vertebral vein is a U- or ring-shaped structure surrounding
the vertebral artery in the transverse process foramen of the upper cervical
vertebrae [6]. The vertebral
vein below the level of the sixth cervical vertebra is seen as a round
opacification adjacent to the vertebral artery located anterolateral to the
musculus longissimus colli on contrast-enhanced CT (Figs.
1B and
2A,2B,2C).
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Fig. 2A. —Vertebral veins in 70-year-old woman with bladder cancer.
Transverse contrast-enhanced CT scans of neck show vertebral arteries (A,
arrowheads) and vertebral veins (V, short arrows). Internal
jugular veins (asterisks), common carotid arteries (stars),
and subclavian arteries (SC, long arrows, B and C) are
also seen.
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Fig. 2B. —Vertebral veins in 70-year-old woman with bladder cancer.
Transverse contrast-enhanced CT scans of neck show vertebral arteries (A,
arrowheads) and vertebral veins (V, short arrows). Internal
jugular veins (asterisks), common carotid arteries (stars),
and subclavian arteries (SC, long arrows, B and C) are
also seen.
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Fig. 2C. —Vertebral veins in 70-year-old woman with bladder cancer.
Transverse contrast-enhanced CT scans of neck show vertebral arteries (A,
arrowheads) and vertebral veins (V, short arrows). Internal
jugular veins (asterisks), common carotid arteries (stars),
and subclavian arteries (SC, long arrows, B and C) are
also seen.
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Perivertebral Venous Plexuses
Perivertebral venous plexuses in and around the lower cervical and upper
thoracic vertebrae are classified as four plexuses on the basis of location:
anterior external plexus (longitudinal prevertebral veins), internal plexus
(epidural venous plexus), posterior external plexus (deep cervical and
posterior intercostal veins), and basivertebral veins (Fig.
1A,1B).
These plexuses communicate with each other, and the blood flow can reverse. In
addition, anastomoses exist between the vertebral venous system and the azygos
and esophageal veins.
Anterior External Plexus (Longitudinal Prevertebral Vein)
Two longitudinal prevertebral veins are located medially to the musculus
longissimus colli on the anterior surface of the cervical vertebrae and
anastomose with the vertebral veins on each side. Both longitudinal
prevertebral veins are united with segmental transverse anastomoses
[7]; therefore, there are
stepladderlike anastomoses between the bilateral vertebral veins at the
anterior aspect of the cervical vertebrae (Fig.
3A,3B,3C,3D).
The longitudinal prevertebral veins are seen as two opacified dots in front of
the cervical vertebrae on contrast-enhanced CT (Fig.
4A,4B).
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Fig. 3A. —Photographs of dissection of perivertebral venous plexus in
cadaver of 80-year-old with no evidence of neck or chest disease. Anterior
view. Trachea, pharynx, and surrounding soft tissue have been removed. Right
and left longitudinal prevertebral veins (stars) are located medially
to musculus longissimus colli (L) and in front of cervical vertebrae.
Anastomosis (arrowheads) between bilateral longitudinal prevertebral
veins and anastomoses (long thick arrows) between longitudinal
prevertebral and vertebral veins (V) are identified. Caudal portion of right
(short arrow) and left (long thin arrow) longitudinal
prevertebral veins communicate with right superior intercostal vein (SIC) and
esophageal vein (E), respectively. D = deep cervical vein, A = vertebral
artery.
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Fig. 3B. —Photographs of dissection of perivertebral venous plexus in
cadaver of 80-year-old with no evidence of neck or chest disease. Posterior
view. musculus trapezius, musculus semispinalis capitis, musculus splenius
cervicis and capitis, and musculus longissimus cervicis have been removed.
Peripheral branches (arrows) and trunk (arrowheads) of deep
cervical veins are seen on surface of musculus semispinalis cervicis.
Bilateral peripheral branches of deep cervical veins are anastomosed around
spinous process of cervical vertebrae.
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Fig. 3C. —Photographs of dissection of perivertebral venous plexus in
cadaver of 80-year-old with no evidence of neck or chest disease. View from
right. Right lung and part of right brachiocephalic artery and vein have been
removed. Esophagotracheal vein (arrowheads) is identified at right
aspect of trachea (T), which drains into posterior aspect of right
brachiocephalic vein. Anastomoses (long arrow) between right
longitudinal prevertebral vein (LP) and right superior intercostal vein (SIC,
short arrow) are seen. A = azygos vein.
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Fig. 3D. —Photographs of dissection of perivertebral venous plexus in
cadaver of 80-year-old with no evidence of neck or chest disease. View from
left. Aortic arch has been removed. Two branches of left longitudinal
prevertebral veins (arrows) enter posterior aspect of upper esophagus
(E). S = left superior intercostal vein.
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Fig. 4A. —Longitudinal prevertebral veins in 72-year-old man with left
brachiocephalic vein obstruction after left upper lobectomy because of lung
cancer. Transverse contrast-enhanced CT scan shows anastomosis (black
arrow) between two longitudinal prevertebral veins behind esophagus.
Anastomosis (white arrow) between right vertebral vein (V,
arrowhead) and longitudinal prevertebral vein is also noted.
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Fig. 4B. —Longitudinal prevertebral veins in 72-year-old man with left
brachiocephalic vein obstruction after left upper lobectomy because of lung
cancer. Transverse contrast-enhanced CT scan obtained 1 cm below A
shows longitudinal prevertebral veins (LP, arrows).
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Internal Plexus (Epidural Venous Plexus)
The anterior and posterior epidural venous plexuses are in the spinal
canal; however, the anterior half is much larger and more regular than the
posterior half [8]. The
bilateral vertebral veins are united with the epidural venous plexus
(Fig. 5) via the
intervertebral veins, in which the blood flow may be reversed.
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Fig. 5. —Photograph shows dissection (viewed from back) of anterior
epidural venous plexus in cadaver of 68-year-old with no evidence of neck and
chest disease. Back neck muscle and all of arches of cervical vertebrae have
been removed. Anterior epidural venous plexuses (asterisks) are seen
at posterior surface of cervical vertebral body and lateral to posterior
longitudinal ligament. Anterior epidural venous plexuses anastomose vertebral
vein through intervertebral vein (arrow).
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The anterior epidural venous plexus is seen as a high-density band at the
posterior aspect of the vertebral body on contrast-enhanced CT
(Fig. 6). Compared with the
anterior epidural venous plexus, the posterior half is rarely seen. Russell et
al. [6] showed that
visualization of the posterior displacement of the enhanced epidural veins
provides excellent delineation of disk extrusion on contrast-enhanced CT.
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Fig. 6. —Anterior epidural venous plexus in 67-year-old man with left
upper lobectomy because of lung cancer. Transverse contrast-enhanced CT scan
shows anterior epidural venous plexus (arrow) located at anterior
aspect of spinal canal, through which right and left vertebral veins
anastomose. Note no evidence of opacification of venous plexus located at
posterior aspect of spinal canal.
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Posterior External Plexus (Deep Cervical and Posterior Intercostal
Veins)
The deep cervical vein receives tributaries from the deep muscles at the
back of the neck, runs forward above the neck of the first rib, and terminates
in the lower part of the vertebral vein
[5]. The bilateral deep
cervical veins are united with each other via the plexuses around the spinous
process of the cervical vertebrae (Fig.
3A,3B,3C,3D)
and also anastomose with the posterior intercostal vein. Therefore, those
veins form a venous plexus on the posterior surface of the laminae and the
spinous and transverse processes of vertebrae.
The posterior external plexus is seen as a Y-shaped opacification at the
posterior aspect of the arch of vertebrae on contrast-enhanced CT
(Fig. 7).
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Fig. 7. —Posterior external plexus in 66-year-old man with prostate
cancer. Transverse contrast-enhanced CT scan shows posterior external plexus
as Y-shaped opacification (arrow) around spinous process of
vertebrae.
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Basivertebral Veins
Basivertebral veins are tortuous vascular channels in the vertebral bodies
and unite with the longitudinal prevertebral veins and the anterior epidural
venous plexus. Basivertebral veins are seen as high-density streaks between
the longitudinal prevertebral veins and the anterior epidural venous plexus in
the vertebral body on contrast-enhanced CT
(Fig. 8).
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Fig. 8. —Basivertebral vein in 70-year-old man with stenosis of left
brachiocephalic vein resulting from aortic arch aneurysm. Transverse
contrast-enhanced CT scan shows basivertebral vein (arrowheads)
through which right longitudinal prevertebral vein (LP, white arrow)
located behind esophagus anastomoses anterior epidural venous plexus (AE,
black arrow). Bilateral vertebral veins (asterisks) running
posteriorly from brachiocephalic veins are well opacified.
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Communications Between Vertebral Venous System and Systemic
Veins
Longitudinal Prevertebral Vein and Azygos System
The longitudinal prevertebral vein runs downward and unites with the azygos
venous system via the superior intercostal vein in the upper thorax (Figs.
3A,3B,3C,3D
and
9A,9B).
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Fig. 9A. —Bilateral superior intercostal veins in 54-year-old woman
with left upper lobectomy because of lung cancer. Transverse contrast-enhanced
CT scan shows opacified left longitudinal prevertebral vein (LP, thick
white arrow). Bilateral superior intercostal veins (SIC, thin white
arrows) are opacified via epidural venous plexus (AE,
arrowheads) and intervertebral veins (IV, black arrows).
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Fig. 9B. —Bilateral superior intercostal veins in 54-year-old woman
with left upper lobectomy because of lung cancer. Transverse contrast-enhanced
CT scan obtained 2 cm below A shows right superior intercostal vein
(RSIC, thick white arrow) running forward to join azygos vein and
left longitudinal prevertebral vein uniting with left superior intercostal
vein (LSIC, thin white arrow). AE and arrowheads indicate anterior
epidural venous plexus.
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Longitudinal Prevertebral Vein and Esophageal Vein
The longitudinal prevertebral vein sometimes unites with the veins of the
upper esophagus (Fig.
3A,3B,3C,3D).
This pathway is not usually seen on contrast-enhanced CT; however, it plays an
important role in "downhill" varices, which we will soon describe,
in patients with superior vena cava syndrome.
Epidural Venous Plexus and Azygos System
In the upper thorax, the epidural venous plexuses are anastomosed with the
superior intercostal veins via the intervertebral veins. Therefore, the blood
of the neck and upper extremities can run downward in the epidural venous
plexuses, reach the superior intercostal vein, and then drain into the azygos
vein (Fig.
9A,9B).
Clinical Significance
Although the vertebral venous system may not consist of principal
collaterals, it is useful to know its existence for analyzing venograms and CT
images.
Collateral Pathways in Upper Extremity Venous Thrombosis
Four potential collateral pathways bypass the axillary—subclavian
vein region [3]: shoulder to
chest wall, shoulder to ipsilateral anterior neck, shoulder to ipsilateral
posterior neck, and shoulder to contralateral neck. The vertebral venous
system plays an important role in the pathways of shoulder to ipsilateral
posterior neck and shoulder to contralateral neck.
Ipsilateral Posterior Neck Pathway
Collateral pathways tend to develop in the intramuscular venous network in
the posterior neck, and those veins reconstitute the vertebral vein (Fig.
10A,10B).
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Fig. 10A. —Ipsilateral posterior neck pathway in 54-year-old woman with
spontaneous thrombosis of axillary vein termed "effort
thrombosis." Right upper extremity venogram shows that right axillary
vein (Ax, arrowhead) is thrombosed and that contrast material runs
forward to posterior neck and reconstitutes right vertebral vein (V,
straight arrow) via veins of posterior neck. Right vertebral vein
empties into brachiocephalic vein distal to obstruction. Anterior jugular arch
(Aj, curved arrow) is also opacified.
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Fig. 10B. —Ipsilateral posterior neck pathway in 54-year-old woman with
spontaneous thrombosis of axillary vein termed "effort
thrombosis." Transverse contrast-enhanced CT scan shows opacified right
vertebral vein (V, arrow) located at right aspect of trachea (T).
Note right brachiocephalic vein (BC, arrowhead) is located
anterolateral to right vertebral vein.
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Contralateral Neck Pathway
Although the most prominent neck pathway is the jugular venous arch
connecting the bilateral anterior jugular veins in the suprasternal space, the
contralateral vertebral vein is also opacified through the perivertebral
venous plexuses (Fig.
11A,11B).
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Fig. 11A. —Contralateral posterior neck pathway in 23-year-old woman
with stenosis of left brachiocephalic vein resulting from anterior mediastinal
tumor. Early phase left upper extremity venogram shows that most of contrast
material runs forward to right brachiocephalic vein through anterior jugular
arch (A), then drains into superior vena cava (S); however, left vertebral
vein (V, arrowheads) and internal jugular vein (IJ, arrow)
are also opacified. Left brachicephalic vein is compressed and occluded by
tumor.
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Fig. 11B. —Contralateral posterior neck pathway in 23-year-old woman
with stenosis of left brachiocephalic vein resulting from anterior mediastinal
tumor. Delayed phase left upper extremity venogram shows bilateral vertebral
veins (arrows) and perivertebral venous plexus (P) more clearly than
early phase. RV = right vertebral vein, LV = left vertebral vein, SVC =
superior vena cava.
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Downhill Varices
Esophageal varices in patients with superior vena cava obstruction are
called downhill varices because the direction of flow is the reverse of that
in the varices of portal hypertension. The varices are usually limited to the
upper third of the esophagus, and bleeding from the varices is rare
[9].
The submucosal enhancement of the esophagus is seen through the
longitudinal prevertebral veins on contrast-enhanced CT
(Fig. 12).
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Fig. 12. —Downhill varices in 62-year-old man with left upper lobectomy
because of lung cancer. Transverse contrast-enhanced CT scan shows that right
half (arrows) of esophagus (E) is opacified through longitudinal
prevertebral vein, indicating downhill varices.
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Pseudoparatracheal Node
When the right vertebral vein has not yet been fully enhanced in the early
phase of contrast-enhanced CT, the prominent right vertebral vein ending at
the lower portion of the right brachiocephalic vein looks like an unenhanced
nodule that resembles the right paratracheal lymph node (Fig.
13A,13B,13C,13D).
It is necessary to take additional scans of the lower neck and upper thorax in
the delayed phase and to observe the continuity of the "nodule" to
distinguish the right vertebral vein from the paratracheal lymph node.
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Fig. 13A. —Right vertebral vein resembles paratracheal node in
62-year-old man with lung cancer in left upper lobe. Early (A) and
delayed (B) phase scans of transverse contrast-enhanced CT show
nonenhancing small nodule (arrow, A) at right aspect of
trachea, which is similar to paratracheal node. On delayed phase scan, nodule
(arrow, B) adjacent to trachea is enhanced same as vessels.
Although vertebral vein usually ends at upper portion of brachiocephalic vein,
right vertebral vein ends at lower portion of right brachiocephalic vein in
this particular patient, which is why right vertebral vein resembles right
paratracheal node.
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Fig. 13B. —Right vertebral vein resembles paratracheal node in
62-year-old man with lung cancer in left upper lobe. Early (A) and
delayed (B) phase scans of transverse contrast-enhanced CT show
nonenhancing small nodule (arrow, A) at right aspect of
trachea, which is similar to paratracheal node. On delayed phase scan, nodule
(arrow, B) adjacent to trachea is enhanced same as vessels.
Although vertebral vein usually ends at upper portion of brachiocephalic vein,
right vertebral vein ends at lower portion of right brachiocephalic vein in
this particular patient, which is why right vertebral vein resembles right
paratracheal node.
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Fig. 13C. —Right vertebral vein resembles paratracheal node in
62-year-old man with lung cancer in left upper lobe. Transverse
contrast-enhanced delayed phase CT scans shows that right vertebral vein
(arrows) is accompanied by vertebral artery (arrowhead,
A) on upper axial image (C) and drains into posterior aspect of
right brachiocephalic vein (asterisk, D) on lower axial image
(D). S = right subclavian artery, star = left brachiocephalic vein.
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Fig. 13D. —Right vertebral vein resembles paratracheal node in
62-year-old man with lung cancer in left upper lobe. Transverse
contrast-enhanced delayed phase CT scans shows that right verterbal vein
(arrows) is accompanied by vertebral artery (arrowhead,
A) on upper axial image (C) and drains into posterior aspect of
right brachiocephalic vein (asterisk, D) on lower axial image
(D). S = right subclavian artery, star = left brachiocephalic vein.
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In summary, the vertebral venous system is a valveless plexiform network
with a longitudinal pattern
[8]. This venous system enables
communication of systemic veins and serves an important role as collateral
vessels, especially in patients with venous stenosis or obstruction.
Acknowledgments
We thank T. Sato, Department of Anatomy, Tokyo Medical and Dental
University, for cooperation in cadaver dissection, and Jan E. Oda-Biro for
manuscript preparation.
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Introduction
Vertebral Veins
