Revisiting The Vertebral Venous Plexus Batson

Literature Review
Revisiting the Vertebral Venous PlexuseA Comprehensive Review of the Literature

Kennedy Carpenter1,4, Tess Decater5, Joe Iwanaga1,2,6, Christopher M. Maulucci1, C.J. Bui4, Aaron S. Dumont1,
R. Shane Tubbs1-5
Key words The venous drainage of the vertebral and paravertebral regions is important for a
- Anatomy better understanding of hematogenous disease spread. Moreover, the spine
- Cadaver
- Hematoma
surgeon must be well acquainted with this anatomy to minimize intraoperative
- Spine and postoperative complications. A comprehensive review of the vertebral
- Vertebral venous plexus venous plexus (Batson plexus) was performed with a concentration on the
Abbreviations and Acronyms
clinical and surgical correlations of this venous network.
AVF: Arteriovenous fistula
AVM: Arteriovenous malformation
CES: Cauda equina syndrome spinal cord.1 This observation was later the superior longitudinal sinus, the gluteal
CSVS: Cerebrospinal venous system
confirmed by fellow anatomist, Sylvius, artery, the superior vena cava, the azygos
CT: Computed tomography
EVVP: External vertebral venous plexus in 1555. Following this development, vein, and the mouth of the inferior vena
IJV: Internal jugular vein Falloppio (1562), Vidus-Vidius (1611), cava (IVC). Through these tubes, a
IVC: Inferior vena cava Willis (1664), and Vieussens (1685) all Prussian-blue stain was injected simulta-
IVVP: Internal vertebral venous plexus made contributions to the anatomy of the neously for visualization, which was able
MRI: Magnetic resonance imaging VVP and helped to describe the basic to document the vertebral veins as a large-
OSAM: Overshunting-associated myelopathy composition of the VVP. Falloppio first capacitance plexiform system without any
PCE: Pulmonary cement emboli
SEAVF: Spinal extradural arteriovenous fistula
described it as longitudinal veins in the valves. Breschet described the venae cavae
SSEH: Spontaneous spinal epidural hematoma cervical spine, and then Vidus-Vidius re- as parallel to this longitudinal plexus with
VVP: Vertebral venous plexus ported the presence of transverse connec- multiple intercommunications. This
tions at 1 vertebral level. Willis and plexus contained connections to the cra-
From the Departments of 1Neurosurgery and 2Neurology, Vieussens reported the presence of trans- nial dural sinuses and spanned the entire
Tulane Center for Clinical Neurosciences and 3Department of
Structural and Cellular Biology, Tulane University School of
verse connections along the entire VVP spinal column.2
Medicine, New Orleans, Louisiana, USA; 4Department of and vertebral column.1,2 Little changed Breschet divided the venous network into
Neurosurgery and Ochsner Neuroscience Institute, Ochsner regarding the knowledge of the VVP until 3 interconnecting divisions. He described
Health System, New Orleans, Louisiana, USA; 5Department the contributions of Breschet in the early the first and largest division as the internal
of Anatomical Sciences, St. George’s University, St.
nineteenth century and then later with peridural network. This network is con-
George’s, Grenada, West Indies; and 6Division of Gross and
Clinical Anatomy, Department of Anatomy, Kurume Batson’s contributions in the mid- tained within the spinal canal and sur-
University School of Medicine, Kurume, Fukuoka, Japan twentieth century. rounds the spinal cord. The second division
To whom correspondence should be addressed: is a group of veins that act to connect the
Joe Iwanaga, D.D.S., Ph.D. internal-to-external vertebral venous net-
[E-mail: [email protected]] Nineteenth Century works and lie completely within the verte-
Citation: World Neurosurg. (2021) 145:381-395. Gilbert Breschet (1784e1845), a French brae. The third division is composed of the
https://doi.org/10.1016/j.wneu.2020.10.004 anatomist and physician, is credited with external vertebral veins, which form a
Journal homepage: www.journals.elsevier.com/world- the first detailed anatomic description of plexus around the spinal column. This third
neurosurgery the VVP in 1819. When competing for the division joins with various other veins to
Available online: www.sciencedirect.com position of inspector general of anatomy connect the VVP to the cervical, thoracic,
1878-8750/$ - see front matter ª 2020 Published by Elsevier at the Faculty of Medicine Paris, Breschet abdominal, and pelvic regions. Breschet
Inc. chose the anatomy of spinal veins as the reported that the third division connected
topic for 1 of his 3 (anatomy, physiology, freely with the other 2 as well as receiving
HISTORY OF THE VERTEBRAL VENOUS and surgery) required essays for the posi- blood from the deep musculature of the
PLEXUS tion.2 He compiled the 3 essays in 12 days back. Breschet attempted to further describe
and earned the position. In the same year, the VVP in a 22-part serial publication in the
Sixteenth and Seventeenth Centuries his spinal vein essay containing 9 sections late 1820s but completed only 8 parts before
Before the nineteenth century, little was was published.2 his death in 1845.2
mentioned about the vertebral venous Within Breschet’s essay on spinal veins,
plexus (VVP) (Figure 1). Its first recorded he described how to select subjects as well
recognition was by anatomist and as how to inject the venous system so that Twentieth Century
physician Andreas Vesalius in 1543, who the spinal veins could be visualized. He After Breschet’s work in the early nine-
described the plexus as veins leaving the used 5 tubes, 1 tube connected to each of teenth century, the VVP was not further
WORLD NEUROSURGERY 145: 381-395, JANUARY 2021 www.journals.elsevier.com/world-neurosurgery 381

LITERATURE REVIEW
KENNEDY CARPENTER ET AL. REVISITING THE VERTEBRAL VENOUS PLEXUS
rather than 3 divisions. He suggested that

because of its physiologic and pathologic
importance, the vertebral system of veins
should be added to the caval, pulmonary,
and portal venous systems.5
Batson continued his research beyond
describing the structure of the VVP by
attempting to identify its physiologic
functions. Through the many in-
terconnections among the VVP and other
veins, Batson reported the flow as
frequently reversed during physiologic
processes including straining, coughing,
and Valsalva maneuvers, showing its
bidirectional capabilities.1 From his
experiments, he was able to show that
the Valsalva maneuver prevents blood
from entering the body cavities and
simultaneously pushes blood out into the
extracavitary veins. In addition, during
the Valsalva maneuver, the cerebrospinal
fluid pressure increases because of the
transfer of blood from the cavities
through the valveless venous network
into the VVP. Through this mechanism
of increasing the spinal fluid pressure,
the brain is protected from increases in
intracranial pressure.6
Beyond the anatomic structure of the
VVPs, one of Batson’s vital contributions
to the field was his research regarding the
role of the VVP in metastatic spread of
various cancers, spread of infections, and
formation and propagation of emboli.
Because of the vital role of the VVP in
venous drainage from different regions of
the body, Batson theorized a link between
Figure 1. The vertebral venous plexus from anterior (left) and posterior views metastatic spread between the VVP and
(right) (after Bourgery).
the intrapelvic connections, particularly
regarding the classic distribution of pros-
tate metastases to the spine.3-5
studied in great detail until the American anatomic structure of the VVP. He
otolaryngologist Oscar V. Batson’s reported the VVP as a thin-walled, valve-
research and contributions. In the 1940s, less venous network, which helped him ANATOMY OF THE VVP
Batson (1894e1979) further developed the draw conclusions regarding the plexus as
work proposed by Breschet not only by a low-pressure system. He described the Modern Description
rearticulating and elaborating on the veins as a large-capacitance network with Since Batson’s contributions to the VVP,
anatomy of the VVP but also by proposing duplications along each segment of the improvements and advances in imaging
its function and clinical significance.1,3-5 spinal column. The network has many modalities including computed tomogra-
His research on the VVP began while interconnections among the veins within phy (CT) (Figure 2), magnetic resonance
studying the diploic veins of the skull and around the spinal canal, the veins venography as well as improvements in
using plain radiography, corrosion within the vertebral column, the inter- corrosion casting (Figure 3) and injection
models, and cadaveric injections.1 This costal (segmental) veins, and the azygos techniques including angiography have
research led him to the work of Breschet veins. In addition, from his research, expanded the knowledge regarding this
and a starting point to his own research Batson’s formative publication in 1940 venous system.7-11 In 2006, Tobinick and
focused on the VVP. Using more suggested a reclassification of the venous Vega12 proposed the reclassification of
advanced techniques than did Breschet, systems in humans. He proposed that the the cerebral and spinal venous systems.
Batson attempted to further describe the venous system can be separated into 4 Their new classification took into
382 www.SCIENCEDIRECT.com WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2020.10.004

LITERATURE REVIEW
Figure 2. Lateral and posterior computed tomography components of the vertebral venous plexus (asterisks).
angiography views of the craniocervical junction noting
account the anatomic and functional system (CSVS) to encompass all these dural sinuses, cavernous sinuses, and the
continuity of the veins and venous venous networks. The CSVS was split ophthalmic veins. Groen et al. further
plexuses of the brain and spine as well into 2 divisions: the cranial venous divided the VVP into 3 separate plexuses
as the cerebral venous sinuses. They system and the VVP. The cranial venous in accordance with the location of the
coined the term cerebrospinal venous system included the intracranial veins, plexus as well as in which plane they
coursed, similar to Breschet’s original
description. The 3 divisions include the
internal VVP (IVVP) (with anterior and
posterior parts), the external VVP (EVVP)
(with anterior and posterior parts), and
the basivertebral veins (Figure 4).7 The
IVVP lies within the spinal canal but
external to the dura and courses
longitudinally from the cranial vault to
the sacrum (Figures 5 and 6). The EVVP
surrounds the vertebral column and
similar to the IVVP courses longitudinally
from the cranial vault to the sacrum.
Contrary to the IVVP and EVVP, the
basivertebral veins run horizontally and
lie within the vertebrae.7
One important aspect highlighted by
multiple studies and experiments is the
valveless nature of the VVP. These studies
used injection techniques and dyes to
show that all divisions of the VVP lack
valves.7,13,14 A newer study reported in
2012 by Stringer et al.15 found evidence
Figure 3. Corrosion cast of the dural venous sinuses and vertebral venous plexus (left) and schematic contrary to these early experiments, that
drawing (right) showing the connections between the emissary veins of the posterior occipital region
and vertebral venous plexus.
one third of patients have valves in the
posterior EVVP, although all other

LITERATURE REVIEW
nature of the VVP allows for both

forward and backward flow of blood.
Groen7 not only confirmed the lack of
valves within the VVP but also noted the
connections between the VVP and the
cranial sinuses, the subcutaneous cranial
veins, the intercostal veins, and the
sacral venous plexus, creating a
widespread open communication
network between the intracranial,
intrathoracic, and intra-abdominal veins.
The ability of the VVP to have retrograde
and bidirectional flow is a critical
distinction between the CSVS and the
systemic venous system. The systemic
venous system contains valves that force
blood to move in 1 direction toward the
heart, whereas the bidirectional flow of
the CSVS does not function to return
blood to the heart. Herlihy18 described
CSVS as having flow as an “ebb-and-
flow” system with a predominantly linear
and bidirectional nature. With this
knowledge of the bidirectional flow,
conclusions have been drawn regarding
Figure 4. Schematic view noting the vertebral venous plexus and its component parts.
its physiologic function including its role
as a large-capacity fluid reserve, its role
in the posture-dependent cerebral venous
outflow, and its role in brain and spinal
divisions of the VVP remained valveless. Overall, Breschet’s and Batson’s de- cord cooling.5
These investigators found these valves to scriptions were similar to the modern One important function of the VVP is its
be mostly bicuspid and all were oriented definition of the VVP. The CSVS is role in cerebral venous outflow. Previ-
toward the IVVP. described as a large-capacity, valveless ously, drainage from the cranial vault was
It has been theorized that the network that has bidirectional flow. It has believed to be exclusively through the in-
morphology of the VVP varies with age, an important role in the regulation of ternal jugular vein (IJV), but in 1966, Eck-
but there are few studies to show the intracranial pressure, particularly during enhoff21 proposed that although the IJV
anatomic variations of the VVP in changes in posture, venous outflow, and played a major role, the VVP also
younger persons. Groen et al. theorized physiologic processes, including cough, contributed significantly to cerebral
that physiologic and pathologic pro- sneezing, and the Valsalva maneuver. The outflow. Using rhesus monkeys, Epstein
cesses that occur as people age including CSVS also plays an important role in many et al.9 were able to prove this theory, and
gravitational force influences and pres- disease states because it allows for a direct later San Millán Ruíz et al.10 applied this
sure gradients within the valveless sys- route for metastatic and infectious spread to human cadavers to determine that this
tem might cause changes to the and air emboli travel. drainage is position dependent. This
morphology of the VVP. Groen et al.‘s study found that in the supine position,
study reported in 2005 evaluated the IVVP venous blood preferentially flowed out of
of fetuses aged 21e25 weeks. From their PHYSIOLOGIC FUNCTION OF THE VVP the cranium through the IJV, but in the
studies, these investigators found that Since Batson’s groundbreaking research upright or standing position, the IJVs are
the anterior IVVP was identical in fetuses regarding the VVP, many studies have collapsed. This process then forced
as in adults, but the posterior IVVP in the been performed in an attempt to deter- venous blood to leave the cranium
lower thoracic and lumbar regions in the mine how the anatomic structure of the through the VVP as the main outflow
fetus was very small and lacked promi- VVP relates to its physiologic roles. One tract from the brain.10 Niggemann
nent transverse venous bridges.7,16 important characteristic of the VVP is its et al.22 were able to reproduce these
Groen et al.16 postulated that this bidirectional flow. This characteristic has findings in living patients using magnetic
difference may be caused by been studied by multiple anatomists, resonance imaging (MRI) to show that
“developmental delay” or from including Batson,5 Anderson,17 Herlihy,18 the VVP is the physiologic outflow tract
functional and age-related factors that Lasjaunias and Berenstein,19 Gisolf in the standing position. However, an
trigger the development of the transverse et al.,20 and Groen.16 Each of these exception to this situation is during a
venous bridges during erect life. anatomists showed that the valveless Valsalva maneuver, which opens the IJVs,

LITERATURE REVIEW
theorize that the greater mechanism of

spinal cord cooling occurs by arterial
perfusion and by the extensive close
contacts of spinal dura and spinal
ganglia with the cooler blood of the
IVVP. That study also addresses possible
mechanisms behind the cooling of the
brain. Similar to the role of the VVP, the
vast number of anastomoses between the
CSVS composed of the intracranial veins,
dural sinuses, cavernous sinuses, and the
ophthalmic veins and the veins of the
scalp and face, cooling can occur
through convection through evaporation
of sweat. In a more recent study,
Hoogland et al.34 studied the
interconnections between the IVVP and
the posterior intercostal vein as a
thermoregulatory source for the spinal
cord. These investigators theorized that
cold-induced closure of certain veins
would help to divert warm blood to the
spinal cord to help maintain homeostasis.
Pregnancy and the VVP

During pregnancy, alterations in the
venous blood flow through the IVC occur
as a result of compression by the enlarging
uterus.35 This is an important clinical
Figure 5. Posterior view of the posterior cranial fossa and cervical spine in a
latex-injected cadaver. Note that the brain and upper cervical spinal cord and consequence because it impairs blood
dura have been removed. Observe the following: sigmoid sinus (SS), flow return from the lower extremities
cavernous sinus (CS), clivus, marginal sinus (MS), suboccipital venous plexus and pelvis. The VVP acts as an alternative
(SVP), segmental veins (SV), and posterior longitudinal ligament (PLL). The
arrows mark the posterior internal part of the vertebral venous plexus and the
route for venous return to the heart and
asterisks mark the anterior internal part of the vertebral venous plexus. the VVP becomes engorged. Takiguchi
et al.36 showed in a small sample that
the VVP becomes extensively engorged
from the lower thoracic to sacral
allowing them to once again become the vital role in drainage of the lower limbs vertebrae rather than at a localized level
main outflow system.23-27 The VVP also and pelvis if the IVC becomes blocked. as shown in previous studies.37 This
allows for an alternative route for blood Instead of venous blood returning to the study also showed a more significant
to flow if the bilateral IJVs become heart through the IVC, venous blood is compression of the subarachnoid space
occluded.28 Multiple studies have also rerouted through intrapelvic connections in the lower lumbar spine, with
shown that in patients with unilateral IJV to the VVP.19 In patients with congenital compression of the cauda equina nerve
occlusion secondary to radical neck agenesis of the IVC, the VVP becomes a roots and engorgement of the VVP
dissection, the VVP begins to play a major collateral drainage system.32 predominantly on the ventral rather than
larger role in cerebral venous. Although Another important function of the CSVS the dorsal side. The investigators
the contralateral IJV continues to play the as proposed by Zenker and Kubik33 is the theorized that these observations may
dominant role in drainage, the vertebral role that it plays in the cooling of the account for the route of distribution of
veins and VVP play contributing roles as brain and spinal cord. These anesthetic during epidural anesthesia as
well.29,30 In addition, 1 study performed investigators suggested that the VVP is well as the paresthesias experienced
in 201331 showed that the cross-sectional analogous to the cranial dural sinus during spinal puncture in late pregnancy.
area of the VVP decreases as people age topologically and that the connections An additional study of 23 patients
compared with the IJV cross-sectional between the EVVP and the skin of the showed that the VVP becomes engorged
area, which remains constant. This study back allow for the anatomic during the first trimester. Igarashi et al.38
theorized that this finding may suggest a preconditions for heat transfer by suggested that although compression of
decrease in the use of the VVP as an convection from the spinal cord to the the IVC by the gravid uterus likely causes
outflow tract in the older population. vascular plexuses of the skin of the back. engorgement during the third trimester,
Similar to IJV occlusion, the VVP plays a However, these investigators also the first trimester engorgement is likely

LITERATURE REVIEW
In 1940, Batson used injected radi-

opaque dye and roentgenography to show
continuous flow between the VVP and the
cranial dural sinuses. The dye was injected
into the subcutaneous breast veins of hu-
man cadavers, after which radiographic
images taken showed flow into the VVP
and the cranial dural sinuses, including
the transverse sinus and the superior
sagittal sinus. Batson continued his work
on the VVP by studying venous blood flow
during simulated Valsalva maneuvers. He
obtained radiographic images during
simulated Valsalva maneuvers on rhesus
monkeys to show that venous blood is
diverted into the VVP, as discussed
earlier.5
Anderson was one of the next anato-
mists to study the VVP using modern im-
aging of that time. At the time of his
Figure 6. Latex-injected cadaveric dissection of the vertebral venous plexus of the upper cervical
region with posterior longitudinal ligament intact (left) and removed (right). experiments, most studies of the VVP used
either cadavers or living rhesus monkeys
as subjects. In his study in 1951, Ander-
son17 described using diodrast contrast
studies and radiographic films in both
secondary to the increased systemic blood observation contrasts the concept of the
cadavers and living subjects to evaluate
volume. Hirabayashi et al.39 showed using VVP being made up of “thin-walled
venous patterns during normal
MRI that positioning during pregnancy vessels.”5 The lack of further research
circulation. He was able to reaffirm
also affects engorgement of the VVP. In into the histologic structure of the VVP
Batson’s findings in cadavers by showing
the supine position, VVP engorgement is represents a major gap in the knowledge
that dye injection into the VVP leads to
seen with almost complete compression of this network of veins and is an area
the visualization of the cranial dural
of the IVC, whereas in the lateral that could be studied further in the future.
sinuses.
position, the IVC becomes free and the
Clemens, in 1961,14 contributed to the
VVP returns to near pre-pregnancy states.
knowledge regarding the VVP and its
communications to other venous
INJECTION TECHNIQUES AND IMAGING plexuses and veins by using corrosion
HISTOLOGY OF THE VVP OF THE VVP casting and injections of Araldite. Using
Few studies have been performed exam- Modern imaging techniques account for the Araldite injections, Clemens showed
ining the histology and immunohisto- much of the current knowledge regarding that the IVVP and EVVP freely
chemistry of the VVP. The oldest study the VVP and CSVS. Following Batson’s intercommunicate and the VVP
reported in 1961 by Clemens13 described work, there have been multiple imaging communicates with the systemic venous
the IVVP in 6 cadavers in which he studies to further develop knowledge of system, including the azygos system, the
described the presence of smooth muscle the VVP, its role in the drainage of the left renal and suprarenal veins, the portal
and collagen in the venous walls. A more brain and other body cavities, and its po- venous system, both the inferior and
recent histologic study brought up tential contribution to pathologic condi- superior vena cava, the pelvic and
multiple controversies regarding what tions. Ultrasonography, radiography, CT, prostatic veins, and the sacral venous
was previously known about the VVP. As MRI, and angiographic studies have all plexus. His work helped to establish that
described earlier, Stringer et al.15 been used to study this plexus. Many of the VVP provided a venous system that
performed a cadaveric study of 12 adults these studies were conducted throughout bypasses and communicates with the
in which they found the presence of the 1960s and later and often used both valve-bearing systemic venous system.12
valves in the posterior EVVP. Their rhesus monkeys and humans as subjects. In 1970, Vogelsang14 helped to confirm
second major finding that puts previous The rhesus monkeys were a comparable Clemens’s work. By using intraosseous
studies in question is the architecture of subject regarding humans because their spinal venography in >400 patients,
the longitudinal veins of the IVVP. They VVP shares a similar anatomic composi- Vogelsang showed that the IVVP and
found that transverse posterior IVVP tion.8,9 We summarize the most relevant EVVP freely intercommunicate. The work
veins and some longitudinal vein findings discovered and/or confirmed of Batson,3 Clemens,13 and Vogelsang14
segments were thin walled, but the IVVPs using radiologic techniques as they relate showed, each using their own
walls were complex and muscular. This to the anatomy of the VVP. methodology, that the EVVP connects

LITERATURE REVIEW
directly with the veins overlying the their study, these investigators showed cancer, 90% of patients were found to
posterior spinous processes, the veins the numerous interconnections of the have metastases in their spine. In this
draining the interspinous space, and the suboccipital cavernous sinus with varying study, Bubendorf et al.47 postulated that
veins draining the deep back muscles. structures including the VVP. After this the inverse relationship seen between
In 1970, Epstein9 provided more development, Caruso et al. in 199941 spinal metastases and pulmonary
information regarding the physiologic showed that the suboccipital cavernous metastases (the second most common
function of the VVP regarding its role in sinus can be identified on contrast- location in 46% of patients) suggests
cerebral venous drainage. Using rhesus enhanced, fat-suppressed T1-weighted that they are independent entities. These
monkeys, injection of radiopaque MRI. These investigators also showed investigators provided 3 supporting
contrast material, and radiographic films, that the suboccipital cavernous sinus acts explanations for this conclusion. First,
Epstein showed that the VVP acts as the as an alternative pathway of cranial venous the hematogenous spread of prostate
major outflow tract for cerebral venous drainage because of its connections to the cancer must in part be a result of
blood in the erect position and plays a cranial dural sinuses, the VVP, and the retrograde flow through the veins of the
minor role in the supine position. In jugular venous system. In 2005, Takahashi prostate to the VVP rather than
2000, Valdueza et al.23 used color-coded et al.42 further developed the work of traditional flow through the IVC. Second,
duplex ultrasonography to study venous Arnautovic and Caruso’s studies by using spine metastases precede lung and liver
drainage from the brain. Their work three-dimensional fast spoiled gradient- metastases in many prostate cancers
confirmed that Epstein’s studies in rhesus recalled echo technique MRI to show because these spinal metastases were
monkeys were directly applicable to better definition of the venous anatomy at seen with smaller primary tumors. Third,
humans. They were able to prove the the craniocervical junction for various in- there was a higher tumor burden in the
physiologic function of the VVP as a ce- terventions including embolization of lumbar spine compared with the cervical
rebral outflow tract in the upright posi- dural arteriovenous fistulas (AVFs) or spine, suggesting an upward spread
tion, whereas, in the prone position, venous sampling for Cushing disease. along the VVP. In addition, through
cerebral outflow preferentially used the studies of animal models, it has been
IJV. This study was then repeated in 2003 suggested that 15%e30% of prostate
using duplex ultrasonography by Schreiber PATHOLOGIC CONSEQUENCES AND cancer metastases can be directly
et al.27 Again, the VVP was found to be an SURGICAL APPLICATIONS OF THE VVP attributed to passage through the VVP to
alternative drainage route for cerebral the lumbar spine.48-51 Seeding of
blood flow in the upright position. These Metastases metastases to the VVP has been fairly
investigators also postulated that the Batson was one of the first to propose a well established in the literature, but 1
deep cervical veins and the intraspinal logical mechanism for the dissemination rare complication of prostate
epidural venous system should be of metastases from primary pelvic tumors, brachytherapy that has been reported is
considered to play a role in cerebral such as prostate cancer. Before his pos- seed migration to the VVP using the
drainage with IJV occlusion. tulations, the leading theory of metastases pelvic venous pathway. There have been
In 1997, Groen et al.7 improved on to the spine and brain was that tumor cells at least 4 reported cases in the literature
Clemens’ Araldite injection technique, entered systemic circulation from the of this finding, as reported by Nakano
and by doing so, they were able to filtering capabilities of the pulmonary et al. in 2006,52 Wagner et al. in 2010,53
confirm that all 3 divisions of the VVP capillaries. This explanation did not and Hau et al. in 2011.54 Similar to seed
(IVVP, EVVP, and the basivertebral veins) explain why there were metastases in the migration in brachytherapy for prostate
freely intercommunicate and that all spine and brain without pulmonary cancer, there has been a report of
divisions of this system lack valves. They metastases.43 pacemaker lead migration through the
also were able to confirm Batson and Regarding the VVP, metastases were VVP into the spinal canal.55
Anderson’s work, when they found that first described as traveling cranially from As a result of Batson’s research as well
Araldite distributed in the cranial dural the pelvis to the spine and brain in a as the work of many other anatomists, the
sinuses and the major cerebral and retrograde fashion.9 As discussed earlier, VVP is considered continuous with not
cerebellar cortical veins. the VVP is unique compared with the only the pelvic cavity but also the cranium,
As more advanced imaging techniques systemic venous circulation because of its thoracic cavity, and abdominal cavity.
have become readily available, additional absence of valves, allowing for flow to be With this knowledge, there have been
studies have been undertaken using MRI bidirectional. Multiple studies have found speculations and suggestions of cancers
to detail identical findings, as previously that after injecting a suspension of tumor other than prostate cancer that use the
noted. In 1997, Arnautovic et al.40 used cells into the tail vein of mice with VVP as a hematogenous route for the
cadavers to study the venous circulation occluded IVCs, they were able to spread of cancer. For example, Batson
at the craniocervical junction. In their reproduce metastatic spread to the used cadavers to show that flow between
study, they coined the term the lumbar vertebrae. These studies the subcutaneous breast veins and the VVP
suboccipital cavernous sinus, which is concluded that the spread of the tumor and cranial dural venous sinuses was
described as the venous compartment cells to the spinal column could be possible.5 There have been reports of cases
surrounding the horizontal segment of attributed to the VVP.44-46 In a study of with the initial presenting symptom of
the vertebral artery at the skull base. In >1500 patients with metastatic prostate metastatic breast cancer being cavernous

LITERATURE REVIEW
sinus syndrome. Although the exact venous side (VVP) is still to be determined. SSEHs. Because of the valveless, thin-
mechanism of the spread of the disease With this knowledge, the VVP has been walled nature of the VVP, it is relatively
is unknown, the VVP may play a role postulated by Tobinik and Vega12 to be a vulnerable to increases in intra-abdominal
through retrograde flow from the primary route for leptomeningeal metastases pressure.98 In a series of 333 cases of
tumor through the VVP to the CSVS.56,57 from various cancers, including SSEH, Groen found that most SSEHs are
In addition to breast cancer, it has been intrapelvic cancers such as prostate, found in the posterior and posterolateral
suggested that the VVP plays a role in cervical,83-86 and bladder87-90 and intra- part of the epidural space, where the
the spread of multiple other cancers to abdominal cancers (e.g., gastric cancer).91 posterior IVVP lies. Groen theorized that
the bone, including malignant Tobinick and Vega12 continued their the reason for most symptomatic SSEHs
melanoma,58,59 ileal carcinoid tumor,60 postulations to suggest that tumor cells being located in this region was the
esophageal carcinoma,61-63 colorectal can also travel in an antegrade fashion posterior longitudinal ligament
carcinoma,64,65 renal cell carcinoma,66,67 from the cranium using the VVP and protecting the anterior IVVP, whereas the
head and neck carcinoma,68 and gastric CSVS because of its continuous, valveless posterior IVVP lies free in the epidural
carcinoma.69 Many of these cases failed nature. These investigators suggested space.12,98 In addition, using the work by
to show any evidence of pulmonary or that multiple tumors including squamous Clemens, Groen postulated that the
visceral metastases, suggesting that these cell carcinoma of the face use facial veins regional differences in the morphology of
tumors, like prostate cancer, may use to access the CSVS and subsequently the the posterior IVVP account for the
retrograde hematogenous flow through VVP to result in metastases in the distribution of the hematomas along the
the VVP. Other possible mechanisms cavernous sinus and spine, causing entire length of the vertebral column.
suggested for the spinal metastases cranial neuropathies and cauda equina Groen reported that SSEHs occur at
include arterial hematogenous spread or syndrome (CES), respectively.12,92,93 In a locations with the highest density of
direct extension. case series of 30 patients, Rochkind veins.98 For example, in the younger
A study in 201970 evaluated bone et al. studied the prevalence of population (0e40 years), SSEHs most
metastases patterns in patients with extracranial metastases from commonly occur at the lower cervical
cancer without visceral metastasis to medulloblastoma. These investigators and upper thoracic (C6-T3), where there
focus on spread likely through the VVP. found that bone was the most common is a higher proportion of veins. Groen also
The study concluded that metastases to site (71%) and drew the conclusion that suggested that degenerative changes of
the bone are typically close to the hematogenous spread from direct the spinal column and/or the spinal
primary tumor and that this may be of invasion of the dural veins by the epidural veins from hydrostatic forces and
use in determining the source of primary tumor was the most probable loss of tissue elasticity in the venous wall
unknown primary cancer. This finding cause of the distribution of these over time account for the change in loca-
reiterated other studies that showed lesions.94-96 In addition, there have been tion of SSEH in the older population (41e
differences in the distribution of bone cases of metastatic meningiomas to the 80 years).98
metastases from prostate, pulmonary, vertebra, with the belief that the tumor
and breast primary cancers.71,72 It has uses the VVP to spread from the cranium Infection
also been theorized that certain cancers to the spine.97 Another clinical correlation suggested by
use the VVP as a route of dissemination Overall, there are many different types Batson was the possibility of infection
to other areas of the body, including the of primary cancers from the intrapelvic, disseminating through the VVP, similar to
lungs, the pleura, the pharynx, and the intra-abdominal, and thoracic cavities that that of metastatic spread.1 Vertebral
bones of the hands and feet. There have have been found to have metastases to the osteomyelitis is most commonly caused
been case reports of colorectal spine, brain, leptomeninges, and remote by hematogenous spread or less
carcinoma73 using this route to reach the locations such as the pleura. Batson’s and commonly from the spread of adjacent
lungs, renal cell carcinoma metastasis to others’ postulations regarding the bidi- soft tissue infection. Tobinik and Vega12
the pleura74 and to the head and rectional flow of the VVP is a possible suggested that vertebral osteomyelitis
neck,75,76 hepatocellular carcinoma mechanism behind the spread of these from prostate procedures, a rare
metastasis to the pharynx,77 and tumors. complication, might be the result of
subdiaphragmatic neoplasms to the dissemination through the VVP.
bones of the feet.78 Spinal Epidural Hematoma Although rare, there is an increase in the
The VVP has also been suggested as a Spontaneous spinal epidural hematomas reported cases after prostate biopsy,
possible route for the spread of lep- (SSEH) are a rare, but important patho- surgery, and acute bacterial
tomeningeal, skull, and brain metastases. logic consequence related to the IVVP. prostatitis.99-104
With the continuous nature of the VVP to There are 3 main theories proposed by In addition to bacteremia after prostate
the CSVS and thus the cranial dural si- Groen regarding the cause of SSEHs: the procedures, there have been reported
nuses, seeding of the leptomeninges may arterial theory, the vascular malformation cases of vertebral osteomyelitis after uri-
be possible.79-82 Hematogenous spread is theory, and the venous theory.98 Here, the nary tract infections, which may also be
regarded as the most common mechanism venous theory is discussed with respect to caused by embolic spread of infection
for these metastases, although whether the VVP. Groen proposed this theory as through the VVP.105-111 Tsutsumi et al.112
the spread is through the arterial or the most probable mechanism for reported a patient with group B

LITERATURE REVIEW
Streptococcus meningitis and infection Intracranial Hypotension legs, motor and sensory dysfunction of the
surrounding the spinal cord secondary to The VVP has been implicated in several lower extremities, bladder and/or bowel
a rectal ulcer. These investigators other pathologic processes. In their study, dysfunction, sexual dysfunction, and sad-
suggested that this complication of the Yousry et al.132 found that the most dle anesthesia because of compression of
ulcer was likely secondary to common finding in patients with the spinal cord, nerves and/or nerve roots
dissemination through the valveless VVP, postural headaches was an enlarged arising from L1-L5.145 The most common
which communicates with the sacral anterior IVVP on MRI. This finding was cause of CES is herniation of an
venous plexus. Vertebral tuberculosis seen in 85% of patients, with the next intervertebral lumbar disc; other causes
(Pott disease) has been linked to using most common findings being subdural include epidural abscess, spinal epidural
both an arterial and venous route with hygromas in 70% of patients and C1-C2 hematoma, discitis, tumor, trauma,
theorizations that central and extraspinal fluid collections in 50%. The spinal stenosis, and aortic obstruction.145
noncontiguous vertebral involvement investigators suggested that these 3 find- Neurogenic claudication is most
results from dissemination through the ings may help in the diagnosis of intra- commonly caused by lumbar spinal
VVP and paradiscal vertebral involvement cranial hypotension. This dilation of the stenosis from degenerative spondylosis
occurs through the arterial route.113 VVP (specifically the anterior IVVP) has and presents with lower back and leg
Other parasitic and fungal organisms been shown in multiple studies evaluating pain with or without lower extremity
that have been postulated to use the VVP patients with orthostatic headaches for numbness and tingling exacerbated by
as a route for dissemination include spontaneous intracranial hypoten- prolonged ambulation, standing, and
schistosomiasis, sparganosis, and sion.133-135 In addition, there have been with lumbar extension.146 Sciatica is
Aspergillus.114-117 cases of spontaneous intracranial hypo- typically caused by disc herniation
tension secondary to CSF venous fis- impinging on lumbar or sacral nerve
tulas.136 This is an important cause to be roots causing radicular pain in the
Embolism aware of in the absence of detectable distribution of the sciatic nerve.147
Another important clinical consequence of epidural CSF leaks so that a more A rarer cause for all 3 of these condi-
the VVP and CSVS is as a route for air, targeted treatment can be approached. In tions (CES, lumbar spinal stenosis with
thrombus, and/or cement emboli. Air 1 study,136 the most common locations of neurogenic claudication, and sciatica) is
emboli can have major and devastating the CSF fistula were in the thoracic and VVP varices causing compression of the
consequences and are thus an important thoracolumbar regions. cauda equina,148-152 the lumbar spinal
surgical consideration. Venous air embo- cord,153,154 or the sciatic nerve roots,155-159
lisms have been reported after surgery in Overshunting-Associated Myelopathy respectively. One cause of VVP
the sitting position,118-120 spinal surgery in Overshunting-associated myelopathy engorgement is compression of the IVC.
the prone position,121-123 and after the use (OSAM) or Miyazaki syndrome is an There have been multiple cases reported
of hydrogen peroxide in surgery.124,125 additional pathologic condition associated in which the IVC or iliac veins are
Cement embolization after trans- with the VVP. Barami137 suggests that the occluded through
cutaneous vertebroplasty and kyphoplasty cervical venous engorgement after thrombosis,148,149,151,152,157 agenesis,150
is a dangerous complication of this pro- ventriculoperitoneal shunt placement and external compression by pathologic
cedure. Preventing extrusion of cement CSF diversion results from cerebral lymph nodes,153,154 or portacaval
into the vertebral venous system can help venous overdrainage with preferential hypertension.160 This obstruction is
to prevent serious neurologic and cardio- flow into the VVP. This process leads to transmitted to the VVP, specifically the
pulmonary complications, as suggested by engorgement of the VVP and subsequent IVVP, which then becomes engorged and
Groen et al.126 They suggest using a prone compression of the spinal cord. Multiple compresses the different neural
position and increasing intrathoracic case reports have shown this rare structures. A second cause of the VVP
pressure during instrumentation and complication of CSF diversion.137-144 One varices as reported by Zimmerman
cement injection. Cement extrusion can study in 2009139 highlighted the et al.161 is that intervertebral disc
have devastating consequences because it importance of recognizing this rare herniation causes compression and
has been shown to cause cerebral cement condition and distinguishing it from occlusion of the anterior longitudinal
emboli, pulmonary cement emboli (PCE), mass lesions and extradural hematomas, veins, which is transmitted to the VVP.
and cement emboli into the spinal which require different intervention. A Others report that the intervertebral
canal.126-131 One study128 reported that 44 recent study reported in 2020142 used foraminal stenosis disrupts blood flow,
of 85 patients had extravertebral leaks endoscopic third ventriculostomy instead resulting in the varices.162
and zero of 85 patients had PCE after of shunt revision or removal as treatment
cement injection under CT fluoroscopy for OSAM and found successful relief of Cervical Myelopathy
for vertebroplasty (rather than myelopathy with no recurrence of Cervical myelopathy is caused by
conventional fluoroscopy). The hydrocephalus or OSAM after 2 years. compression at the level of the cervical
investigators suggested that larger spine and results in spasticity, hyper-
prospective vertebroplasty may help CES, Sciatica, and Lumbar Spinal Stenosis reflexia, pathologic reflexes, and hand
compare the rates of PCE for CT versus CES is a neurosurgical emergency that clumsiness, among other possible symp-
conventional fluoroscopic guidance. presents with back pain radiating to the toms. Cord compression is often caused

LITERATURE REVIEW
by degenerative changes in the vertebra Here, we focus on spinal extradural embolization of feeder
and ligamentum flavum as well as devel- AVFs (SEAVFs) because they relate most arteries,181-184,191,196,200,203,210 surgical
opment of listhesis, osteophytes, and facet closely to VVP. SEAVFs are less common removal,187,194 or a combination of both
hypertrophy.149 Similar to cord than spinal dural AVFs, the most common interventions.180,198,199 A recent study
compression at lower vertebral levels, vascular malformation of the spine, mak- reported in 2020211 showed that primary
engorgement of the VVP is a rare cause ing up approximately 70% of spinal microsurgery was superior to
of cervical myelopathy.163-167 One case, vascular lesions.178 SEAVFs primarily form endovascular treatment SEAVFs because
first misdiagnosed as acute transverse as a result of dural or epidural arterial of a higher odd ratio of initial treatment
myelitis, showed that although a cervical branches draining into the IVVP. The failure.
disc herniation did not compress the arterial feeders could originate from
spinal cord, the herniation impaired multiple levels, often cross midline, and
Central Nervous System Drug Delivery
venous blood flow. This process resulted have a characteristic diamond shape.179
Another clinical application of the VVP is
in enlargement of the VVP and They can occur anywhere throughout the
its use to deliver drugs to the CNS. Tobi-
subsequently compression on the cervical cervical,180-186 thoracic,187-189 lumbar,190
nik describes this novel therapeutic
spine.164 This finding has also been and sacral191 spinal segments. Although
approach, in which perispinal injection of
reported in patients with Marfan the most common arterial feeders are the
drugs results in delivery to the CNS
syndrome, which may be caused by epidural and dural arteries, the aorta,
through the interconnections between the
vessel wall abnormalities associated with intercostal arteries, and the vertebral
EVVP, which drains this anatomic region
this condition.153 Posterior IVVP arteries have been found to be the
and the deeper venous plexuses of the VVP
engorgement has also been suggested to arterial source in SEAVFs.183,192-197 The
and CSVS.212
play a role in Hirayama disease/ cause of SEAVFs remains unknown, but
myelopathy, a slowly progressive, pure risk factors for their development may
motor upper extremity myelopathy that include previous trauma,189,195,196 spinal Spine Surgery in General
preferentially affects young adults of surgery,185,186,197 neurofibromatosis type Surgeons who operate on the spine are
Asian descent.168-170 1,194,198-200 and fibromuscular aware of the potential for substantial
dysplasia,201 although in some cases, bleeding from the VVP, especially its
there may be no identifiable intraspinal parts. For example, with lam-
Spinal Extradural AVFs predisposing factor.179,184,202-204 inectomy, the posterior external part of the
The classification of spinal vascular mal- Interruption of the normal epidural VVP is often encountered but is usually
formations has changed throughout the venous drainage through trauma or easily controlled with bipolar cautery. The
twentieth and twenty-first century as new surgery may predispose to development external part of the plexus can also be
diagnostic and treatment options have of such vascular lesions through venous encountered with anterior and far lateral
arisen.171 One classification scheme thrombosis and subsequent abnormal approaches to the vertebral bodies. Intra-
divided the malformations into 2 broad recanalization.205 The clinical spinal approaches can see more profuse
categories: intramedullary and presentations of SEAVFs are similar to bleeding caused by the VVP. Moreover, if
extramedullary malformations.172 Another their dural counterparts (spinal dural the dura mater is opened and CSF
classification system commonly used was AVFs) in that they typically present with released, the intraspinal tamponade
developed in the 1990s and divided symptoms of congestive myelopathy or afforded by the distended CSF-filled spinal
spinal vascular malformations into 4 radiculopathy secondary to compression dura is lost and hence, bleeding from the
main types: type I, dural AVFs; type II, or steal syndrome.180,205,206 Although VVP can be more difficult to control. In-
intramedullary glomus arteriovenous these patients typically present with jection of hemostatic agents into the
malformations (AVMs); type III, juvenile slowly progressive symptoms, there have epidural space can most often address
or combined AVMs; and type IV, been cases of rapidly progressive such bleeding when bipolar cautery is
intradural perimedullary AVFs.173 This neurologic deterioration, including lower ineffective. Other combined approaches
classification did not include extradural extremity paresis, loss of sphincter such as transforaminal lumbar interbody
AVFs. In 2002, Spetzler et al. proposed a function, or spinal cord infarction.205,206 fusion can encounter the external part of
modified classification that broke down Other more rare presentations include the VVP superficially and then the internal
spinal cord vascular malformations into 3 subarachnoid hemorrhage (particularly part of the VVP more deeply when the disc
general categories (neoplasms, with a predominance in the posterior space is dealt with.
aneurysms, and arteriovenous lesions fossa),207 symptoms mimicking a carotid-
[AVF and AVM]) and then included more cavernous fistula,208 symptoms
specific subtypes based on mimicking brachial CONCLUSIONS
neuroanatomy. AFVs can then be divided radiculoplexopathy,202 SSEH,209 Clinicians who treat and surgeons who
into intradural (ventral or dorsal) and vertebrobasilar hypoperfusion by steal operate on patients with spinal disease
extradural/epidural lesions.174 This is a through the steal phenomenon,203 acute should have a detailed knowledge of the
comprehensive classification scheme, but ischemic strokes,204 or unilateral venous drainage of the spine. The VVP is
new classification systems are still being pulsatile exophthalmos.195 Treatment of complex and necessitates a good under-
proposed.175-177 SEAVFs is typically through endovascular standing of its anatomy to better diagnose

LITERATURE REVIEW
and treat patients with disease that in- 14. Vogelsang H. Intraosseous Spinal Venography. blood flow assessed by Doppler ultrasound after
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15. Stringer MD, Restieaux M, Fisher AL, Crosado B.
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are muscular and external veins have valves. Clin venous reconstruction: a technique to minimize
Many of our figures are based on cadaveric Anat. 2012;25:609-618. morbidity of bilateral radical neck dissection.
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16. Groen RJ, Grobbelaar M, Muller CJ, et al.
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anatomic research could be performed. venous plexus: a cadaver study after latex injec- Intracranial nonjugular venous pathways: a
Results from such research can potentially tion in the 21-25-week fetus. Clin Anat. 2005;18: possible compensatory drainage mechanism.
397-403. AJNR Am J Neuroradiol. 2013;34:1348-1352.
increase humankind’s overall knowledge,
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Therefore, these donors and their families and cranial venous system to show their probable a rare cause of pelvic congestion syndrome. J Clin
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411-422.
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Revisiting The Vertebral Venous Plexus Batson

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Literature Review

Revisiting the Vertebral Venous PlexuseA Comprehensive Review of the Literature

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rather than 3 divisions. He suggested that

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nature of the VVP allows for both

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theorize that the greater mechanism of

Pregnancy and the VVP

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In 1940, Batson used injected radi-

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