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Chapter 2 Applied Anatomy of the Spine 43
e internal venous plexus is of more functional and ana­tomic interest. is plexus is essentially a series of irregular, valveless epidural sinuses that extend from the coccyx to the foramen magnum. Its channels are embedded in the epidural fat and are supported by a network of collagenous bers, but their walls are so thin that their extent or conguration cannot be discerned by gross dissection. is latter property may account for the fact that the epidural venous sinuses have been periodically “rediscovered.” e epidural vertebral veins were known to Vesalius and his contemporaries and were described and illustrated in the rst part of the 19th century by Breschet.81 Batson,82 Clemens,83 and others made the functional and pathologic signicance of these vessels apparent (Fig. 2.34).
e plexus does not entwine the dura in a completely hap­hazard fashion but is arranged in a series of cross-connected expansions that produce anterior and posterior ladderlike congurations up the vertebral canal. e main anterior components of the epidural plexus consist of two continu­ous channels that course along the posterior surface of the vertebral bodies just medial to the pedicles. ese channels expand medially to create cross anastomoses over the central dorsal area of each vertebral body and are thinnest where they overlie the intervertebral discs. When injected with a contrast medium, the main channels may appear as a segmental chain of rhomboid beads. Chaynes and colleagues84 studied the internal venous plexus using silicon injection techniques. ey found that anterior longitudinal veins were located in a “dehiscence” within the periosteum along the lateral aspect of the spinal canal and that veins of each side communicated with each other through a retrocorporeal vein. In the cervical
spine, the retrocorporeal vein was found deep to the posterior longitudinal ligament, whereas it was supercial to the liga-
ment in the thoracic and lumbar regions.
Where the main anterior sinuses cross connect, they receive the large unpaired basivertebral sinus that arises within the dorsal central concavity of the spongiosa and drains the intraosseous labyrinth of sinusoids. Regional visualization of the epidural plexus can be accomplished by introducing a radiopaque medium directly into the spongiosa or the cancel­lous bone of the spinous process (intraosseous venography).
e major external connections of the epidural plexus consist of the veins that pass through the intervertebral foramen and eventually empty into the segmentally avail­able intercostal or lumbar veins (Fig. 2.35). Because these sinuses are valveless, one cannot refer accurately to directions of drainage and ow. e greatest functional signicance of these vessels lies in their ability to pass blood in any direc­tion according to the constantly shiing intraabdominal and intrathoracic pressures. Breschet81 surmised that the epidural plexus served as a collateral route for the valveless caval and azygos systems. is ability has been shown by experimental ligation of either the superior vena cava or the inferior vena cava. In addition, the Queckenstedt maneuver, which tests the patency of the spinal subarachnoid space by compressing the jugular or intraabdominal veins, causes an increase in cerebrospinal uid pressure through dural compression from the expansion of the collaterally loaded epidural plexus.
e plexus is evidently capable of passing large quantities of blood without developing varices. Clemens claimed that this feature was due to the intricate network of collagenous bers that supports the thin walls of the sinuses. Also, passive
SECTION
I
A
FIG. 2.34 (A) Posterior and (B) lateral illustrations of the spinal epidural venous plexus taken from hand-colored
copies of Breschet’s original work (ca. 1835). (Courtesy Scott Memorial Library, Jeerson Medical College.)
B
44 BASIC SCIENCE
21
1
6
2
3
9
8
3
7
FIG. 2.35 Schema showing venous relationships of a lumbar vertebra.
Engorgement and relative venous hypertension in the epidural vessels exacerbate neuroischemic conditions in the lumbosacral roots. 1, Dorsal external vertebral plexus. 2, Dorsal epidural plexus. 3, Ascending lumbar veins. 4, Basivertebral vein. 5, Ventral external vertebral plexus. 6, Lumbar segmental vein. 7, Muscular vein from posterior abdominal wall. 8, Circumferential channels (sinuses) of epidural plexus. 9, ventral internal vertebral plexus. 10, anterior and posterior longitudinal sinuses of internal vertebral plexus.
10
4
5
congestion of the spinal cord is prevented by minute valves in the radicular branches draining the spinal cord.83 is latter fact is anatomically unique because valves exist nowhere else in the venous channels associated with the central nervous system. An ancillary function of the epidural plexus may be to act in a mechanical capacity as a hydraulic shock-absorbing sheath that helps buer the spinal cord during movements of
the vertebral column, similar to the epidural fat.
e vertebral sinuses are largest in the suboccipital and upper cervical region. Here they also receive numerous nerve endings from the sinuvertebral nerves and are associated with glomerular arteriovenous anastomoses, which suggests a pos­sible baroceptive function.85 e patency of these anastomoses is most easily shown in the fetus, in which arterial injections of a contrast medium may also ll the upper cervical epidural sinuses. Similarly, the coccygeal bodies of the same specimen pass the arterial injection directly into the epidural veins of the lower sacral region.
e detrimental aspects of the vertebral epidural veins have been well stated by Batson.82 Retrograde ow from venous connections to the lower pelvic organs provides an obvious route of metastasis for pelvic neoplasms to the spine itself and to the regions of the trunk associated with valveless connec­tions to the plexus. Batson82 claimed that direct metastatic transfer can occur between the pelvic organs and the brain via the vertebral epidural route.
Another extraspinal-intraspinal venous connection impli­cated in the transfer of pathologic processes involves the pharyngovertebral veins.86 ese vessels constitute a system that drains the superior posterolateral regions of the naso­pharynx and coalesces into two to several veins that penetrate
1
2
23
3
4
5
6
7
8
10
9
11
T5
14
2
15
18
12
13
5
16
17
23
T11
22
24
21
20
19
FIG. 2.36 Composite schema of blood supply to spinal cord and nerve
roots showing two regions of the cord. Note the distinction between medullary arteries and true radicular arteries and that the medullary arteries usually run a course that is independent of the roots. 1, Dorsolateral longitudinal artery. 2, Proximal radicular artery (of dorsal root). 3, Dorsal medullary artery. 4, Dorsal root of thoracic spinal nerve. 5, Distal radicular artery (of dorsal root). 6, Sinuvertebral nerve. 7, Dorsal ramus of spinal nerve. 8, Segmental artery. 9, Dorsal central artery. 10, Dorsal root ganglion. 11, Anterior laminar artery. 12, Ventral ramus of spinal nerve. 13, Rami communicantes. 14, Ventral root of spinal nerve. 15, Proximal radicular artery of ventral root. 16, Periradicular theca of dura. 17, Dorsal meningeal branch of vertebromedullary artery. 18, Dura. 19, Ventral meningeal plexus. 20, Great ventral medullary artery (great “radicular” artery of Adamkiewicz). 21, Anterior (ventral) spinal artery. 22, Vasa corona of spinal cord. 23, Spinal nerve. 24, Ventral medullary artery of thoracic cord.
the anterior atlanto-occipital membrane to discharge into the venous complex surrounding the median and lateral atlanto­axial joints. Because posterior pharyngeal infections have been linked with the atlantoaxial rotatory subluxations char­acteristic of Grisel syndrome,87 it is believed that the pharyn­govertebral veins are instrumental in transporting infectious processes that may produce a hyperemic relaxation of the atlantoaxial ligaments. e existence of this venous system also explains the ease in transfer of superior pharyngeal meta­static processes to the upper cervical epidural veins.

Blood Supply of the Spinal Cord

roughout the length of the spinal cord, a system of three longitudinal vessels receives blood from the irregularly located medullary branches of the segmental spinal arteries and dis­tributes it to the substance of the cord. is system consists of the single median ventral anterior spinal artery and two smaller dorsolateral spinal arteries (Fig. 2.36).
Chapter 2 Applied Anatomy of the Spine 45
Anterior Spinal Artery
Despite its great functional signicance, the anterior spinal artery remains one of the more inaccurately described and inadequately understood blood vessels. Derived from the fusion of bilateral pairs of ascending and descending anasto­motic branches of the original segmental arteries of the devel­oping spinal cord,88 this median ventral pial vessel supplies approximately 80% of the intrinsic spinal cord vasculature. It is usually depicted in texts as a single continuous artery of nearly uniform caliber that extends from the medulla oblongata to the conus. e anterior spinal artery is actually a longitudinal series of functionally independent vessels that may show wide luminal variations and anatomic discontinuities.
Although the investigations of Crock and Yoshizawa75 have tended to minimize the signicance of predominant regional feeders, many functionally oriented reports have claimed that the cord has three major arterial domains along its vertical axis: (1) the cervicothoracic region (C1–T3), (2) the mid­thoracic region (T3–T8), and (3) the thoracolumbar (includ­ing sacral cord) region (T8-conus). e reports have also claimed that these areas have little anastomotic exchange between their junctions (Fig. 2.37).
Brewer and colleagues89 and Lazorthes and associates90 maintained that a series of human anterior spinal arteries consistently show interruptions, or critically narrow zones,
VA
T3
88-90
in the mid-thoracic region, and these inuence the potential collateral blood ow along the longitudinal axis of the cord. It is not only the observed size of the vessel that is of physi­ologic signicance, however. e existence of a marked auto­regulatory control of the intrinsic spinal cord blood ow has been independently shown in many mammalian species.
32,91
Microscopic investigation92 of sections of the descending and ascending contributions of the arteria medullaris magna (artery of Adamkiewicz, also known as the arteria radicularis magna) to the anterior spinal artery showed that these arteries, in addition to their well-developed circumferential muscle of the tunica media, also possess a layer of predominantly lon­gitudinal intimal musculature. Located between the internal elastic lamina and the endothelium, this layer ranges in thick­ness from one-h to one-half of the tunica media (Fig. 2.38).
In following a series of cranial to caudal sections of the thoracolumbar anterior spinal artery, it was noted that the intimal muscle layer did not extend into any of its branches. At the mouth of the central (sulcal) arteries, which are the largest anterior spinal artery derivatives, the intimal muscu­lature stops abruptly, oen forming a liplike projection over the opening of the branch vessel, but no intimal muscle bers extend into the central arteries. A sphincter-like thickening of the central artery tunica media, seen at the ostium of the vessels, indicates that this muscle layer has a greater contractile inuence at this point (see Fig. 2.38). e intimal musculature, in addition to enhancing the luminal control of the anterior spinal artery, also is involved in controlling the blood ow into the central arteries. Where the intimal layer shows the liplike projections, successive serial sections indicate that contraction of the longitudinally disposed intimal muscle bers forms an ellipsoidal buttonhole-shaped orice whose long axis is parallel to that of the ber orientation. Such an arrangement permits exquisite muscular control of the blood ow from the anterior spinal artery to its central artery branches.
SECTION
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T8
AMM
FIG. 2.37 Schema illustrating sources and relationships of medullary feeder
arteries to the spine and the spinal cord. Anterior spinal artery (ASA) is shown to be formed by an anastomotic chain of ascending and descending branches of medullary feeders. Cervicothoracic, mid-thoracic, and thoracolumbar (includes sacral cord) regions are indicated, and their usual boundaries at vertebral levels T3 and T8 are shown. Medullary feeders range from 6 to 14, but the respective domains persist. Dotted line indicates frequent position of a smaller accessory medullary feeder to the thoracolumbar area. AMM, Arteria medullaris magna; VA, vertebral artery. (From Parke WW, Whalen JL, Bunger PC, et al. Intimal musculature of the lower anterior spinal artery. Spine. 1995;20:2074.)
2
ASA LUM
1
5
4
7
10 mm
FIG. 2.38 High-power cross section of thoracolumbar anterior spinal artery
(ASA) wall at junction with one side of a central artery. The intimal musculature (1) may extend as a liplike projection (6) over the central artery orice. This muscle layer stops at this point and does not extend into branch vessels. A sphincter-like enlargement of the conventional circular muscle of the central artery (7) is indicated. Endothelium (3) and internal elastic lamina (4), tunica media (2), and adventitia-pia (5) are labeled. ART, artery; LUM, lumbar. (From Parke WW, Whalen JL, Bunger PC, et al: Intimal musculature of the lower anterior spinal artery. Spine 1995;20:2075.)
6
Central
ART LUM
3
46 BASIC SCIENCE
a ASA
d ASA
AMM
FIG. 2.39 Schema derived from sections of arteria medullaris magna
(AMM)–anterior spinal artery (ASA) junction to show distribution of intimal musculature (solid black) in this region. Intimal cushions are shown guarding the orice of the ascending ASA (a ASA) and a typical distribution is found in the arch of the descending ASA (d ASA). (From Parke WW, Whalen JL, Bunger PC, et al. Intimal musculature of the lower anterior spinal artery. Spine. 1995;20:2076.)
In addition to the fairly uniform layer of the intimal mus­culature throughout the walls of the examined sections of the thoracolumbar anterior spinal artery, serial sections cut through the arch-shaped junction of the arteria medullaris magna and the descending anterior spinal artery branches show that this intimal layer, in most cases, is organized into prominent intimal cushions. ese muscular thickenings are erratically distributed along the lumen of the hairpin-shaped arterial arch and the initial segment of the ascending branch of the anterior spinal artery (Figs. 2.39 and 2.40). is latter loca­tion is of considerable interest because its prominent cushions, with reinforced thickenings of the underlying tunica media, could exert considerable inuence over the quantity of blood ow between the thoracolumbar and mid-thoracic vascular domains. is intimal control system, when coupled with the intramedullary arteriovenous anastomoses (described in a subsequent section on intrinsic vascularity), provides an anatomic basis for the dramatic range of spinal cord blood ow autoregulation. e presence of the intimal cushions explains the oen-noted failure of the arteria medullaris magna to supply adequately the mid-thoracic cord region above the arteria medullaris magna–anterior spinal artery junction during aortic cross clamping.
e ventral position of the anterior spinal artery and its nutritional importance may have consequence in spinal ste­nosis. Particularly in the lower cervical region, its compression by dorsal osteophytes and cartilaginous protrusions related to cervical disc degeneration may lead to the neurologically disastrous anterior spinal artery syndrome.93 e medullary feeder arteries that supply the anterior spinal artery may arise from any spinal segmental artery. Studies by Dommissee94 showed, however, that there are statistical preferences for certain segmental levels. ere are usually three anterior
5
2
4
FIG. 2.40 Sagittal section through junction of arteria medullaris magna
(AMM) arch and ascending anterior spinal artery (aASA) showing the intimal cushions guarding the aASA orice (1). These may be reinforced by underlying enhancement of the circular bers of the tunica media (2). Endothelium (3) and elastic lamina (4) are indicated. The longitudinal disposition of the intimal muscle bers is apparent, particularly in the intimal cushion on the right side. The contraction of these muscular systems would dramatically alter the radius of the aASA lumen. 5, Adventitia-pia. (From Parke WW, Whalen JL, Bunger PC, et al. Intimal musculature of the lower anterior spinal artery. Spine. 1995;20:2076.)
4
3
aASA
1
1
AMM
10mm
4
2
medullary arteries for the cervical region, one or two for the thoracic region, and a conspicuous medullary vessel (the arteria medullaris magna) for the lumbosacral cord region. e levels of origin for all these vessels center around certain “average” locations in each region. e anterior spinal artery is usually of greatest caliber in the lumbosacral part of the cord, where it supplies the considerable tissue mass of the proximal cauda equina in addition to the lumbosacral cord intumescence.
e dorsolateral spinal arteries arise from the posterior
inferior cerebellar vessels and are of lesser caliber and nutri­tional signicance. ey also are less likely to be longitudinally
continuous and oen present a more plexiform distribution over the dorsum of the cord. ey have a greater frequency of smaller medullary sources.
e larger intradural spinal arteries are unusual in that, similar to the cerebral arteries, they have no signicant vasa vasorum. In all other regions of the body, a vessel with an external diameter approaching 1 mm shows a ne vascular plexus (vasa vasorum) on its external surface that supplies nutrients to its outer layers of tissue. Because the cerebral and spinal vessels are bathed in the nutrient-rich cerebrospi­nal uid, their external layers presumably derive metabolic exchange from this source.
Chapter 2 Applied Anatomy of the Spine 47

Lateral Spinal Arteries of the Cervical Cord

e highest three to four segments of the cervical spinal cord receive blood from a unique pair of vessels, the lateral spinal arteries. Although, ontogenetically, these seem to be the most rostral expressions of the dorsolateral spinal arteries, they have a more extensive distribution and are without equivalents in other levels of the cord. ey usually arise from the intradural parts of the vertebral arteries near the origins of the posterior inferior cerebellar arteries, or they may arise from the proxi­mal sections of the posterior inferior cerebellar arteries themselves. eir typical course carries them anterior to the posterior roots of the cervical spinal nerves C1 to C4, dorsal to the denticulate ligaments, and parallel to the spinal compo­nents of the 11th cranial nerve. eir general distribution is to the dorsolateral and ventrolateral cord regions caudad to the olives.
Although these vessels were observed in the later 19th century, they were usually regarded as variants, and their functional signicance was not appreciated. Lasjaunias and colleagues95 compiled an extensive report on the variations and selective angiography of these important vessels.

Intrinsic Vascularity of the Spinal Cord

e tissues of the spinal cord are supplied by two systems of vessels that enter its substance. e rst is a centripetal arrangement of arteries that supplies the supercial tracts of the ventral and lateral funiculi, all of the dorsal funiculus, and the extremities of the dorsal horns. ey are radially penetrat­ing branches of the vasa corona and the dorsolateral spinal arteries, which serve only a little more than one-fourth of the cord. e greater part of the cord and almost all of its gray matter is supplied by a second centrifugal system of vessels derived from the sulcal (or central) arteries.96 ese arteries are a repetitive series of branches derived from the dorsal aspect of the anterior spinal artery that penetrate the depths of the anterior median ssure. In the mid-sagittal plane, they form a close palisade of vessels that occur with a frequency of 3 to 8 arteries per 1 cm in the cervical region and 2 to 6 per 1 cm in the thoracic cord; they are densest in the lumbar region, where they number 5 to 12 per 1 cm of the anterior spinal artery. e average diameters of the sulcal arteries are greater in the cervical (0.21 mm) and lumbosacral (0.23 mm) regions than in the thoracic cord (0.14 mm).
As these vessels approach the anterior commissure, most turn to either the right or the le and supply only the corre­sponding side of the cord.
14,73,98,99
is unilateral proclivity reects their origins in the early embryonic stages when the anterior spinal arteries rst condensed from a primitive plexus as a symmetrical pair of longitudinal vessels, each supplying its respective half of the cord. In subsequent development, these two vessels fused in the midline to form the denitive single median anterior spinal artery, but their sulcal branches retained their original unilateral anities. Bilateral distribu­tions occur in 9%, 7%, and 14% of the cervical, thoracic, and lumbar vessels.
97,100
97
Although the sulcal arteries may give infrequent branches
to the septomarginal white bers as they extend into the
median anterior ssure, their major distribution is derived aer they enter the substance of the cord, just ventral to the anterior white commissure. Here the individual right and le arteries subdivide into dorsal and ventral branches. A group of ventral branches supplies the ventral horns and, through more radial extensions, provides vessels to Clarke column and the deeper bers of the anterior and lateral funiculi. e smaller, more dorsal group of branches supplies the gray commissure and the ventral one-half to two-thirds of the dorsal horns. A few second-order or third-order branches form anastomotic arcades with their counterparts of adjacent sulcal artery territories. All these vessels provide the ner arterioles that eventually lead to the spinal capillary beds.
e greater metabolic requirements of the spinal gray matter, in contrast to the funicular tissue, are dramatically reected in their relative capillary densities. Quantication of the microvascularity in the spinal cord has shown that the capillary density of the gray matter is four to ve times as great as the white matter.
101
e capillary distribution within the gray matter is not homogeneous, however, and varies with the regional concentrations of the nuclei. e nuclei of the dorsal horn are fairly uniformly distributed. e ventral horn shows segmental nuclear clusters, which display distinct nerve cell groups.
As noted by Feeney and Watterson,
102
the capillary densities of the white and gray matter of the central nervous system are established at a level that is minimally requisite for the meta­bolic needs of the given tissue. is situation is in contrast to most other body tissues, which have a capillary “reserve” and normally function with only part of their capillary channels open, varying their intrinsic vascular resistance by dilation of the accessory channels. Nevertheless, despite the lack of this method of control, the spinal cord exhibits a remarkable range of blood ow autoregulation.
1,32,103
e intrinsic cord vasculature maintains a constant blood ow throughout a wide range of systemic blood pressure alterations, although each animal species has a denite upper and lower limit to the systemic blood pressure at which the regulation decom­pensates. Because transection of the upper cervical cord has no eect on this autoregulatory capacity, it may be assumed that this reex is local and independent of autonomic nerve control.
Numerous third-order branches of the sulcal arteries com­municate directly with veins through convoluted anastomoses. ese vascular structures are located primarily in the area that divides the ventral two-thirds of the dorsal horn from the dorsal one-third and in the more central regions of the ventral horn. ey show a paucity of contractile elements and instead exhibit an “epithelioid” type of media that seems capable of swelling and diminishing its thickness. Because this action could rapidly control the caliber of the anastomotic lumina in immediate response to local metabolic changes, these anasto­motic convolutions may be the site of the reex adjustment in the ow resistance of the spinal cord vasculature.
104
Perhaps the most essential part of knowledge of the vascu­lar supply of the spinal cord is awareness of the ranges of
SECTION
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48 BASIC SCIENCE
individual variability. e numerous successful surgical cases in which the arteria medullaris magna has been inadvertently interrupted without producing a disastrous spinal cord ischemia give the impression that an adequate collateral vas­cularity may protect the cord in most individuals when a single major artery is compromised. In procedures involving the interruption of blood ow in numerous consecutive seg­mental branches of the aorta, such as aortic cross clamping for abdominal vascular surgery, the maintenance of adequate spinal cord blood ow, particularly in the thoracic area, seems to depend more on the regional competence of the anterior spinal artery than on the number of collateral sources to the cord. Spinal cord injury aer cross clamping without adjunc­tive vascular support has been reported to range from 15% to 25%, depending on the series of cases reviewed.
105,106
Proximal­to-distal aortic shunting may alleviate the undesirable hyper­tension in the aortic distribution proximal to the rst clamp and the hypotension in the segments distal to the second clamp. e work of Molina and colleagues
105
on dogs indicated, however, that the shunt capacity should provide more than 60% of the baseline descending aortic ow and have a diameter greater than one-half of the descending aorta to be eective.
Of particular signicance was the study by Svensson and
colleagues
107
on the blood ow in the baboon spinal cord and its implications in aortic cross clamping. is animal was chosen because its spinal vascularity is similar to humans in that its anterior spinal artery is a continuous vessel without the occasional interruptions noted in some quadrupeds. is study indicated that in baboons, as in humans, the caliber of the anterior spinal artery is oen critically narrowed where the thoracic anterior spinal artery joins the lumbar segment of this vessel at their common junction with the arteria medullaris magna. e functional implication is that the shunting of the cross-clamped aorta may help maintain an adequate ow in the lumbosacral sections of the cord but is of little help to the supply of the lower sections of the thoracic cord, owing to the marked discrepancy that usually exists between the anterior spinal artery diameters above and below the junction of the arteria medullaris magna.
In accordance with the hemodynamic principles of Poi­seuille’s equation, the resistance to blood ow upward from the arteria medullaris magna junction was more than 50 times greater than the ow resistance downward into the lumbosa­cral anterior spinal artery in the baboon. Because a series of direct measurements showed that this discrepancy in the anterior spinal artery diameters was even greater in humans, Svensson and colleagues
107
concluded that even the lowest segments of the thoracic cord were dependent on a blood ow from the superior end of the thoracic anterior spinal artery despite the shunting.

Intrinsic Venous Drainage of the Spinal Cord

Compared with the arterial anatomy, the structural and func­tional aspects of the venous drainage of the spinal cord have been relatively neglected. In contrast to other organ systems in which the equivalent orders of veins and arteries tend to
course in a common vascular bundle, the veins of the central nervous system are generally less numerous than the arter­ies, they are larger than their corresponding eerent vessels,
the larger branches may not show a pattern concurrent with the arterial distribution, and they are not accompanied by lymphatics.
e internal substance of the dorsal half of the cord drains by a centrifugal arrangement of intrinsic vessels that are tribu­taries, by way of a venous vasa corona, to a large median dorsal longitudinal spinal vein; the ventral half sends tributaries to sulcal veins that empty into a large median ventral longitudinal vein that runs parallel to the anterior spinal artery. Both of these longitudinal vessels are circumferentially connected by a prominent venous vasa corona. is entire system drains into the epidural venous plexus by medullary (previously called radicular) veins that are as infrequent in their distribu­tion as the medullary arteries.
108
e proximal sections of the spinal nerve roots drain centripetally into the vasa corona and longitudinal veins of the cord and then to the epidural system via the medullary veins.

Vascularization of the Spinal Nerve Roots

Although it has been generally recognized that much of the pain consequent to degenerative changes in the spinal motion segment is associated with compression or tension on the spinal nerve roots, the mechanisms that initiate the actual nerve discharge have remained obscure. Because experimental studies on peripheral nerves and observations on numerous cases of neurogenic claudication have suggested that much of the pain may have a neuroischemic basis, investigations were undertaken to determine the nature of the intrinsic vascularity of the spinal nerve root and its response to localized compres­sion or tension. e nerve roots had long been regarded as part of the peripheral nervous system and were viewed as histologically and vascularly similar to peripheral nerves. Consequently, research on the latter was oen uncritically extrapolated to apply to the nerve roots.
e very long roots of the lumbosacral spinal nerves seemed to be particularly vulnerable because their vascularity was initially believed to be supplied only from their distal ends without the access to the frequent collateral support that is characteristic of peripheral nerves. Because the nerve root fasciculi do not have a strong connective tissue support, it also seemed that the ne vascularity they possessed would be at risk from the repeated tension and relaxation resulting from the exion and extension of the spine. Parke and colleagues and Parke and Watanabe
110
showed by vascular injection that
the roots receive their arterial supply from both ends (Fig.
2.41; see Fig. 2.36), however, a fact physiologically conrmed
by Yamamoto.
111
e existence of many redundant coils along the branches of the true radicular arteries ameliorates the stresses that would result from the interfascicular movements that accom­pany the repeated stretch and relaxation. A signicant nding was the occurrence of numerous, relatively large arteriovenous anastomoses throughout the length of the root (Fig. 2.42).
109
Chapter 2 Applied Anatomy of the Spine 49
SECTION
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FIG. 2.41 Schema indicating directions of normal blood ow in cauda
equina. The anterior spinal artery of the lumbosacral part of the cord is supplied by medullary arteries and supplies 75% at the cord substance and upper parts of the cauda equina via the proximal radicular arteries. This accounts for enlargement of the anterior spinal artery in the lumbosacral region.
ese vascular cross connections apparently allow blood ow to be maintained in sections of the root above and below a point of compression. Of particular signicance to root nutri­tion is the work of Rydevik and colleagues
111a
who, using isotopically labeled methylglucose, showed that approximately 50% of the root nutrition is derived from the ambient cere­brospinal uid; this necessitates a gauzelike architecture of the radicular pia-arachnoid sheath (Fig. 2.43; see Fig. 2.42B).
A study by Watanabe and Parke
112,113
of chronically com­pressed roots indicated that the compressed segment is most likely metabolically deprived. It has been suggested that radicular pain is related to root ischemia because a reduction of oxygen intake in patients with neurogenic claudication exacerbates the symptoms.
114
e arterial side of the vasa radiculorum seems to be well compensated, however, and maintains a continuity despite severe chronic compression. Further study has indicated that the venous side of the radiculomedullary circulation is more vulnerable.
113
Because the roots are part of the central nervous system, the relation­ships of the arteries to the veins resemble those of the brain more than those of peripheral nerves. e radicular veins do not follow the arterial pattern. ey are fewer in number and run a separate and usually deeper (more central) course. Being thin-walled, they are more liable to the spatial restrictions imposed by degenerative changes in the dimensions of the spinal canal and intervertebral foramina and show complete interruption in the chronically compressed root. e meta­bolically deprived, or inamed, nerve root becomes hypersen­sitive to any mechanical deformation, and any additional insult to such a nerve may initiate ectopic impulses that produce pain.
6
5
4
5
5
3
A
1
2
3
7
6
4
B
FIG. 2.42 (A) Low-power (×20) transillumination photomicrograph of
midsection from part of L4 nerve root treated with hydrogen peroxide after vascular injection with latex–India ink but before clearing in a solution of tributyl-tricresyl phosphates. The peroxidases within the residual blood elements inated the radicular veins (4) to provide a temporary contrast medium. Note the frequency of the large arteriovenous anastomoses (5) that permitted the latex–India ink to enter the veins. (B) Compilation showing structure of a typical lumbosacral nerve root derived from data obtained by injection studies and scanning electron microscopy (see
Fig. 2.38). The gauzelike pia-arachnoid membranes permit the cerebrospinal
uid to percolate into nerve tissues and assist metabolic support. Numbers in (A) and (B) are common to equivalent structures. 1, Fascicular pia. 2, Interfascicular and intrafascicular arteries showing compensating coils to allow interfascicular movement. 3, Longitudinal radicular artery. 4, Large radicular vein (does not course with arteries). 5, Arteriovenous anastomosis. 6, Collateral radicular artery. 7, Gauzelike pia-arachnoid that permits percolation of cerebrospinal uid to assist in metabolic support.
6
4
FIG. 2.43 Scanning electron photomicrograph of section of proximal part
of L5 ventral nerve root. The gauzelike pia-arachnoid sheath is very evident. The numbers correspond to the structures labeled in Fig. 2.42.
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3
1
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50 BASIC SCIENCE
Impedance of the radiculomedullary venous return can occur without topographically related venous constriction. e exacerbation of neurogenic pain in cases in which spinal stenosis has been associated with venous hypertension has been recorded by clinical investigators. LaBan and Wesolowski
116
noted that patients with diminished right-
115
and LaBan
sided heart compliance and spinal stenosis may eventually exhibit neurogenic pain even in static or recumbent situations. ey attributed this phenomenon to an increased external pressure on the already sensitized roots by the engorgement of the epidural venous sinuses (see Fig. 2.35), but the venous hypertension alone may be sucient to impede the venous return from an already compromised radicular circulation. Madsen and Heros
117
showed that “arterialization” of spinal veins by abnormal arteriovenous shunts in the region of the conus medullaris exacerbates the neurogenic pain in patients with spinal stenosis. eir hypothesis suggested that a vari­able combination of increased mechanical constriction by dilated epidural veins and the direct increased resistance to the radicular circulation by the venous hypertension could contribute to the elicitation of pain. Aboulker and col-
118
leagues
also concluded that epidural venous hypertension alone may produce radicular symptoms or cord symptoms or both without adjunctive stenotic compression.
If the intrinsic circulation of the nerve root is impeded in either its arterial input or its venous outow, the net eect seems to be the same: a neuroischemia of the compressed root segment that may enhance the generation of ectopic nerve impulses. A phenomenon that could be related to radicular venous stasis is the swelling of the disc-distorted nerve root that Takata and colleagues
119
showed in CT myelograms. is phenomenon is dicult to explain because extravasated uids in the root tissues should have free access to the surround­ing cerebrospinal uid. Nevertheless, the uid balance of the root tissues seems to be altered, particularly in the segment proximal to the level of the oending disc. e intricacies of the hemodynamic relationships responsible for this change remain unknown.
e role of the ubiquitous arteriovenous anastomosis in autoregulation of the intrinsic radicular vasculature also oers a fertile eld for clinical investigations. Because these vascular shunts are mostly without contractile elements but seem instead to control their lumina by the thickening response of an epi­thelioid endothelium, they probably react to chemical changes in the blood within their lumina and can oer an immediate local reex to alterations in the nerve root metabolism.

Functional Anatomy of the Spine

e biomechanics of the spine is a very complex and extensive subject. A comprehensive discussion is beyond the scope of this chapter, so the reader is directed to the work of White and Panjabi, this eld. Because an appreciation of the essential functional relationships of the spinal components does enhance an understanding of their anatomy, however, a brief overview follows.
120
which is generally regarded as the major book in
e spine is capable of ventroexion, extension, lateral exion, and rotation. is remarkable universal mobility may seem at odds with the fact that its most essential function is to provide a rm support for the trunk and appendages. e apparent contradiction may be resolved when one realizes that the total ranges of motion are the result of a summation of limited movements permitted between the individual verte­brae and that the total length of the spine changes very little during its movements. e role of the musculature in the performance of the supportive functions cannot be minimized, as the disastrous scolioses that result from their unilateral loss in a few motor segment units may attest.
e degree and combination of the individual types of motion described earlier vary considerably in the dierent vertebral regions. Although all subaxial-presacral vertebrae are united in a tripod arrangement consisting of the interver­tebral disc and the two zygapophyseal articulations, the rela­tive size and shape of the former and the articular planes of the latter determine the range and types of motion that an individual set of intervertebral articulations contributes to the total mobility of the spine. In general, exion is the most pronounced movement of the vertebral column as a whole. It requires an anterior compression of the intervertebral disc and a gliding separation of the articular facets, in which the infe­rior set of an individual vertebra tends to move upward and forward over the opposing superior set of the adjacent inferior vertebra. e movement is checked mainly by the posterior ligaments and epaxial muscles.
Extension tends to be a more limited motion, producing posterior compression of the disc, with the inferior articular process gliding posteriorly and downward over the superior set below. It is checked by the anterior longitudinal ligament and all ventral muscles that directly or indirectly ex the spine. Also, the laminae and spinous processes may sharply limit extension. Lateral exion is accompanied by some degree of rotation. It involves a rocking of the bodies on their discs, with a sliding separation of the diarthroses on the convex side and an overriding of the diarthroses related to the concavity. e rotational component brings the anterior surface of the bodies toward the convexity of the exure and the spinous processes toward its concavity. is phenomenon is well illustrated in a dried preparation of a scoliotic spine. Lateral exion is checked by the intertransverse ligaments and the extensions of the ribs or their costal homologues.
Pure rotation is directly proportional to the relative thick­ness of the intervertebral disc and is mainly limited by the geometry of the planes of the diarthrodial surfaces. Although the architecture of the disc permits limited rotation between the bodies, it also serves to check this movement by its resis­tance to compression. e consecutive layers of the anulus brosus have their bers arranged in an alternating helical fashion, and rotation in either direction can be accompanied only by increasing the angularity of the opposing bers to the horizontal, which requires compression of the disc.
e entire vertebral column rotates approximately 90 degrees to either side of the sagittal plane, but most of this traversion is accomplished in the cervical and thoracic sec­tions. It exes nearly the same amount, using primarily the
Chapter 2 Applied Anatomy of the Spine 51
cervical and thoracic regions. Approximately 90 degrees of extension is permitted by the cervical and lumbar regions, whereas lateral exion with rotation is allowed to 60 degrees to both sides, again primarily by the cervical and lumbar areas.
Specic Regional Considerations
e atlanto-occipital joints mostly permit exion and exten­sion with a limited lateral action, all being checked by the suboccipital musculature and the atlanto-occipital ligaments. e atlantoaxial articulations allow only rotation, the pivoted joint being stabilized and checked by the alar ligaments and the ligaments forming the capsules of the atlantoaxial diarthroses.
One-half of the rotational mobility of the entire cervical region takes place between the atlas and the axis, and the remainder is distributed among the joints of the subaxial vertebrae. e atlanto-occipital joint accounts for approxi­mately half of the cervical exion. e remaining 50% is not evenly distributed among the cervical vertebrae but is greater in the upper section.
e subaxial part of the cervical region shows the ranges of motion that are the most free of all the presacral vertebrae. e discs are quite thick in relation to the heights of the ver­tebral bodies and contribute about one-fourth of the height of this part of the column. In addition, a sagittal section shows the middle part of the cervical disc to be lenticular, so that the anteroinferior lips of the bodies are more capable of sliding slightly forward and overriding one another. e range of spinal exion is greatest in the cervical region, and although the posterior nuchal ligaments and muscles may tend to resist this motion, it is ultimately checked by the chin coming to rest on the chest.
e cervical spine is normally carried in a moderately extended position and shows a median variation of 91 degrees between extension and exion. Extension is checked by the anterior longitudinal ligament and the combined resistances of the anterior cervical musculature, fascia, and visceral structures, all three of which may be traumatized in hyperex­tension injuries.
Cervical lateral exion is quite limited by the articular pillars and the intertransverse ligaments, and most lateral motion involves considerable rotation. e nearly horizontal position of the planes of the cervical articular facets provides good supportive strength to the articular pillars but increases the lateral rigidity, so that hyperextension injuries may be more disastrous if the head is rotated at the time of impact from the rear.
e mobility of the thoracic region is also not uniform throughout its length. Although the upper segments resemble the cervical vertebrae with respect to the size of the bodies and the discs, the ribs attached to the sternum greatly impair the ranges of motion. e circumferential arc of the plane of the articular facets shows that rotation is the movement least restricted by these structures.
Flexion and extension become freer in the lower thoracic region, where the discs and vertebral bodies progressively
increase in size and the more mobile and less restrictive they become. e last few thoracic vertebrae are transitional with respect to the surfaces of the articular facets. ese begin to turn more toward the sagittal plane and tend to limit rotation and permit greater extension.
e articulations of the lumbar region permit ventroex-
ion, lateral exion, and extension, but the facets of the synovial joints lie in a ventromedial to dorsolateral plane that virtually locks them against rotation. is lumbar nonrotatory rigidity is a feature shared with most mammals and achieves its great­est manifestation in certain quadrupeds in which the inferior articulation ts like a cylindric tenon into the semicircular mortise of the corresponding superior process of the vertebra below. It provides a gliding action that permits the neural arches to separate or approximate each other only during extension and exion. e morphology of the joints can be well appreciated in an appropriate cut of loin chop or T-bone steak.
e synovial articulations at the lumbosacral junctions are unique. In contrast to the more superior lumbar joints, the facets of the inferior articulating processes of the h lumbar vertebra face forward and slightly downward, to engage the reciprocally corresponding articular processes of the sacrum. Because of the position of these joint surfaces, a certain amount of rotation should be possible between the h lumbar segment and the sacrum, but the presence of the strong iliolumbar ligaments quite likely restricts much motion of this type.
e most essential function of the synovial lumbosacral articulations involves their role as buttresses against the forward and downward displacement of the h lumbar vertebra in relation to the sacrum. When one considers that each region of the spine has its own characteristic curvature, the tracing of the vertical line indicating the center of gravity shows that it intersects the column through the bodies of the transitional vertebrae. e normal cervical lordosis places most of the cervical vertebrae anterior to the center of gravity, and the compensating thoracic kyphosis places the thoracic vertebrae posterior to the center of gravity. e lumbar lor­dosis brings the middle lumbar vertebrae anterior to the line. e transitional vertebrae between each region intersect the center of gravity and seem to be the most unstable regions of the spine; this is emphasized by the fact that disc prob­lems and fractures most frequently occur in the transitional vertebrae.
Because the sacrovertebral angle produces the most abrupt change of direction in the column, and the center of gravity, which passes through the h lumbar body, falls anterior to the sacrum, there is a marked tendency for the thick, wedge­shaped h lumbar disc to give way to the shearing vector that the lumbosacral angularity produces. e resulting condition, spondylolisthesis, most frequently reveals a deciency in the laminae (spondylolysis) that fails to anchor the h vertebral body to the sacrum and allows its forward displacement. ere has been considerable discussion as to whether spon­dylolysis is congenital or acquired, but the spondylolisthesis seldom occurs without the laminar deciencies as a preceding condition.
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Biomechanics of the Intervertebral Disc

It is axiomatic in mechanical engineering that a well-designed machine automatically reveals its function through the analy­sis of its structure. ere are few instances in biologic circum­stances in which this statement is more applicable than in the case of the intervertebral disc. Even when the disc is simply divided with a knife and examined grossly, it is apparent that one is dealing with an organ that is remarkably constructed simultaneously to alleviate shock and transmit forces from every conceivable combination of vectors. is appreciation of the functional competency of the disc increases as its structure is analyzed at the ner levels of organization.
e internal composition of the disc has evolved to with­stand great stresses through the liquid and elastic properties of nucleus and anulus acting in combination. e nucleus is distorted by compression forces, but being liquid it is in itself incompressible. It serves to receive primarily vertical forces from the vertebral bodies and redistribute them radially in a horizontal plane. It is the distortion of the anulus by the internal pressure of the nucleus that gives the disc its com­pressibility, and its resilience makes possible the recovery from pressure.
Were the nucleus pulposus simply a cavity lled with water, it would momentarily act in the same capacity, but the ability to maintain the appropriate quantity of uid during the con­tinual compression and recovery cycle would be lacking. is ability to absorb and retain relatively large amounts of water is the unique property of the living tissue of the nucleus. essential compound involved in this process is a protein­polysaccharide gel, which through a high imbibition pressure binds nearly nine times its volume of water. It is apparent that the hydrophilia is not a form of biochemical bonding because a quantity of water can be expressed from the nucleus by prolonged mechanical pressure. is accounts for the diurnal decrease in the total length of the spine and its recovery in the supine position at night.
e anulus must receive the ultimate eects of most forces transmitted from one vertebral body to another. Because the major loading of the intervertebral disc is in the form of verti­cal compression, it may seem paradoxical that the anulus is best constructed to resist tension, but the nucleus transforms the vertical thrust into a radial pressure that is resisted by the tensile properties of the lamellae. Although the basic plan of alternating bands of bers is one of the obvious sources of the tensile strength of the anulus, this arrangement is not uniform with respect to the directions of the bers or the degrees of resistance and resilience encountered throughout the anulus. e bers generally become longer, and the angle of their spiral course becomes more horizontal near the circumference of the disc because it is here that the shearing stresses of vertebral torsions would be most eective. Experimental analysis has also shown that various parts of the anulus do not respond equally to the same degree of tension, and the dis­crepancies were related to the plane of section and the location of the sample.
122
e anulus proved to have the greatest
resistance and the greatest recovery in horizontal sections of
121
e
the peripheral lamellae, whereas vertical and more medial sections were more distensible.
Because the spine acts as a exible boom to the guidewire
actions of the erector spinae muscles, it is essentially the fulcrum of a lever system of the rst class, in which the loading has a considerable mechanical advantage. Pure vector analysis has indicated that a theoretical pressure of approximately three-fourths of a ton could be applied to a disc when 100 lb is lied by the hands,21 but this is considerably in excess of the actual pressures achieved. Increased intrathoracic and intra­abdominal pressures alleviate much of the fulcrum compres­sion of the discs by eectively counteracting the load of the anterior lever arm.
e actual pressure variations occurring with postural changes have been recorded by inserting transducers into the third lumbar disc.
123,124
is procedure indicated that the internal disc pressure increases from approximately 100 kg in a standing position with the spine erect to 150 kg when the trunk is bent forward and to 220 kg when a 70-kg man lis a 50-kg weight. It was particularly revealing that the pressure showed a considerable increase when the equivalent maneuvers were repeated in a sitting position, and the weight liing ultimately created a pressure of 300 kg on the third lumbar disc.
e disc is also “preloaded.” e inherent tensions of the intervertebral ligaments and the anulus exert a pressure of about 15 kg because this weight is required to restore the original thickness of the disc aer the ligaments have been divided.
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From a comparative standpoint, this preloading probably oers increased stability to the spine as a functional exible rod. One is almost induced unconsciously to use teleo­logic thinking in terms of the vertical thrust resistance when regarding the structure of the disc. In perspective, however, the intervertebral disc shows a consistent morphology in all mammals, yet humans are the only species that truly stand erect. Although analysis of muscular action would most likely show that all mammalian discs must dissipate and transfer axial thrusts, the preloading would enhance the “beam strength” that is obviously necessary in the vertebral column of quadrupeds.
Acknowledgments
e authors acknowledge Wesley W. Parke, PhD (deceased), an original author of this chapter in previous editions who was responsible for much of the critical information included in this work.
e vascular studies presented in this chapter were supported by National Institutes of Health research grant HL-14035.

KEY REFERENCES

1. Bajwa NS, Toy JO, Ahn NU. L5 pedicle length is increased in subjects with spondylolysis: an anatomic study of 1072 cadavers. Clin Orthop Relat Res. 2012;470(11):3202-3206.
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Goldstein RY, Sunde CD, Assaad P, et al. Location of the
vertebral artery at C1 in children: how far out laterally can one safely dissect? J Bone Joint Surg Am. 2014;96(18):1552-1556.