Surg Radiol Anat DOI 10.1007/s00276-013-1206-1 REVIEW Contribution of embryology in the understanding of cervical venous system anatomy within and around the transverse foramen: a review of the classical literature Elsa Magro • Bernard Sénécail • Jean-Christophe Gentric Zarrin Alavi • Olivier Palombi • Romuald Seizeur • Received: 10 June 2013 / Accepted: 6 September 2013 Ó Springer-Verlag France 2013 Abstract Anatomic arrangement of venous system within the transverse foramen is a controversial topic among authors. Precise knowledge of this arrangement is necessary in imaging where vertebral artery dissection is suspected, as well as in surgical approaches of cervical spine. This knowledge objective cannot be achieved without a prerequisite knowledge of primitive venous system. We present here an update on the development of the transverse foramen venous system through a literature review. Our review of the classical literature aimed at E. Magro (&)
R. Seizeur Service de Neurochirurgie, Pôle Neurolocomoteur, CHU de la Cavale Blanche, Boulevard Tanguy Prigent, 29200 Brest, France e-mail: elsa.magro@chu-brest.fr R. Seizeur e-mail: romuald.seizeur@chu-brest.fr E. Magro
B. Sénécail
R. Seizeur Faculté de médecine, Laboratoire d’anatomie, Avenue Camille Desmoulin, 29200 Brest, France e-mail: bernard.senecail@univ-brest.fr E. Magro
R. Seizeur INSERM, UMR 1101 LaTIM, Brest, France B. Sénécail
J.-C. Gentric Service de Radiologie, CHU Morvan, Avenue Foch, 29200 Brest, France e-mail: jean-christophe.gentric@chu-brest.fr Z. Alavi INSERM CIC 0502, CHU de la Cavale Blanche, Boulevard Tanguy Prigent, 29200 Brest, France e-mail: zarrin.alavi@chu-brest.fr O. Palombi Service de Neurochirurgie, CHU Michallon, Boulevard de la Tronche, 38700 Grenoble, France e-mail: OPalombi@chu-grenoble.fr synthesis of available related embryological knowledge and relating this synthesis to cervical vertebrae anatomy. Our findings with regard to different primitive descriptions were consistent and often complementary across the studies. The description has varied from a single vertebral vein to a single vein divided at certain areas, or even to a confluence of venous plexus. In this manner, the embryonic knowledge for instance on venous system can help us to better understand the segmental development of vertebral veins and their plexus arrangement. Furthermore, the cranial–caudal embryology, in particular of the nervous system, conveys the initial plexiform arrangement of vertebral veins, which ends into a single venous trunk joining the subclavian vein. Keywords Anatomy Vertebral veins
Embryology
Introduction Anatomic arrangement of venous system within the transverse foramen is a controversial topic among authors as Labbé and Trolard. Labbé proposed a description involving a ‘‘venous confluence’’ and Trolard described a ‘‘transversovertebral venous sinus’’, as written in the article of Laux et al. [8]. The description has varied from a single vertebral vein to a single vein divided at certain areas, or even to a confluence of venous plexus [5–7, 12, 18]. In this manner the embryonic knowledge for instance on venous system can help us to better understand the segmental development of vertebral veins and their plexus arrangement. Precise knowledge of this arrangement is necessary in imaging where vertebral artery dissection is suspected, as well as in surgical approaches of cervical 123 Surg Radiol Anat spine. This knowledge objective cannot be achieved without a prerequisite knowledge of primitive venous system. Our review of the classical literature aimed at synthesis of available related embryological knowledge and relating this synthesis to cervical vertebrae venous anatomy. Our findings in regard to different primitive descriptions were consistent and often complementary across the studies. Embryologic knowledge In this review, we focus primarily on the venous system development. However, the knowledge of arterial system being useful in our understanding of the whole blood network, a brief summary of their development is given hereunder. Primitive venous system development and superior cava network Tuchmann-Duplessis [18], Pansky [12], and Langman [6] provided close descriptions of primitive circulatory network being developed almost simultaneously with the development of the heart and three networks: intraembryonic, vitelline and umbilical-allantoic (Fig. 1). Fig. 1 Illustration of general characteristics of primitive cardiovascular network in a 25-day human embryo. This is an original drawing by the author inspired by TuchmanDuplessis [18] and Pansky [12] showing in particular the segmentary features of the vascular network 123 These vascular networks arise from mesenchymal vascular network. These vessels deepen into capillary plexus inside which run early vascular flows. Then, their protective tissue and muscular coat arise from the neighboring mesenchyme. Intra-embryonic network is made by ventral and dorsal cardinal veins. These vessels are formed later than the aortae but according to the same process, i.e. within each ventral branchial arch, gradually five vessels appear and anastomose with ventral and dorsal cardinal veins. The cardinal veins at the heart anastomose forming the common cardinal veins (ducts of Cuvier) which drain into the sinus venosus neighboring the vitelline and umbilical veins. Vitelline network is developed on the vitelline vesicle (‘‘yolk sac’’) surface in particular within the caudal end. Both vitelline veins run ventrally through the embryo and drain into sinus venosus. Umbilical-allantoic network is developed within the mesenchyma around the allantoic. Both umbilical veins which drain into the sinus venosus, anastomose prematurely into a single trunk at the umbilical cord. Primitive circulation system evolved into a primitive venous network followed by the development of cava system. In this manner, at week 4 of embryogenesis, the venous system comprises a dorsal systemic network, returning the intra-embryonic blood, formed by ventral Surg Radiol Anat cardinal veins. Furthermore, the venous system comprises also a double nutritional network returning the extraembryonic blood: the omphalomesenteric network (duct) for the blood from the vitelline vesicle, and the umbilicalallantoic network for the blood from placenta. These networks are initially symmetrical and paired which transform into major unpaired trunks via transversal anastomosis system. These trunks are displaced toward the right end of the embryo around the week 6. Cranial cava system development The bulky anastomosis, at gestation week 8, derived from thymic and thyroidian veins, hinders the blood from left cranial cardinal vein to the right one, becoming the future left branchio-cephalic venous trunk. Above this anastomosis, ventral cardinal veins become internal jugular veins. The mandibular ventral veins give rise to external jugular veins. The upper limbs venous plexuses join to give rise to subclavian vein. The cranial vena cava is finally formed by the right common cardinal vein and the proximal part of right ventral cardinal vein. Venous cardinal system development Larsen [7] gave a detailed description of venous system from the head to the neck: the venous cardinal system is part of previously described intra-embryonic network. The cardinal system collects the blood from the head, the neck and the body walls. This bilateral and initially symmetric system constitutes ventral and dorsal cardinal veins, which form common cardinal veins near the heart. The ventral cardinal veins drain the blood from the head and the neck. The cranial parts of the ventral cardinal veins, i.e. those within the cervical region, are originally internal jugular veins. The latter anastomose with facial capillary plexuses forming external jugular veins. Simultaneously, a median anastomosis, arising from thyroidian and thymic veins, between left and right ventral cardinal veins is formed. This anastomosis drains the left part of the head and the neck into the right ventral cardinal vein. Dorsal cardinal veins drain the blood from the body walls. These veins are substituted for and replaced by subcardinal and supracardinal veins. The latter veins are medial to the dorsal cardinal veins. The subcardinal system drains all of the medial dorsal structures of the body, in particular, the kidneys and the gonads. This subcardinal system gives rise to part of the caudal vena cava and the azygos veins which drain the chest wall. Encephalic venous system development The descriptions on the development of encephalic venous system by Paturet [13] and Guidoni [5] are complementary. Pansky [12] provided a layout drawing on the cerebral plexus formation that we used in our Fig. 2. The development of dural venous sinuses is related to the development and evolution of: cerebral vesicles (prosencephalon, mesencephalon, rhombencephalon), the skull and the ventral cardinal veins. In the early embryo Fig. 2 Illustration of cerebral plexuses around the week six of human embryo, at stage of five cerebral vesicles. This is an original drawing by the author inspired by Pansky [12], Paturet [13], and Guidoni [5] showing the arrangement of caudal, middle and rostral venous plexuses, as well as the lateral sinus formation through anastomosis of middle and rostral plexuses 123 Surg Radiol Anat within the cerebral vesicles mesenchyme, three dural venous plexuses are formed: rostral, middle and caudal. These plexuses drain into the encephalic end of the ventral cardinal vein called lateral vein of the head or vena capitis prima. – – – Rostral plexus returns the venous blood from the prosencephalon and the mesencephalon. The prosencephalon gives rise to the telencephalon (future cerebral hemispheres) and the diencephalon (optic vesicle, thalamus, hypothalamus, mammilary bodies). The mesencephalon gives rise to cerebral and superior cerebellar peduncles, colliculus, red nucleus and gray matter. Middle plexus returns the blood from part of the rhombencephalon (hindbrain giving rise to the metencephalon and the myelencephalon) which gives rise to the metencephalon (middle cerebellar peduncles, cerebellum and pons). Caudal plexus drains part of the rhombencephalon which gives rise to the myelencephalon and cranial part of cervical spinal cord. The myelencephalon gives rise to medulla oblongata and inferior cerebellar peduncles. Toward the end of the second month, while ventral part of the lateral vein of the head backs up, there occurs an anastomosis between middle and caudal plexuses, above and behind the auditory vesicle. This anastomosis evolves into sigmoid part of the lateral sinus whereas part of the vena capitis prima (i.e. situated before trigeminal ganglion) gives rise to cavernous sinus inside which ophthalmic vein ends. Skull base venous blood drains toward transverse sinus via superior petrosal sinus, part of the middle plexus (i.e. situated between cavernous sinus and lateral sinus) and via inferior petrous sinus that comes after the cavernous sinus. The transverse sinus is then continued by the ventral cardinal vein, i.e. future internal jugular vein. There are two secondary bypass pathways: the mastoid emissary vein exiting the skull via mastoid foramen and the petrosquamous sinus. These venous pathways represent the anastomoses between the lateral sinus and the external jugular system. Thereafter, these emissary veins atrophy, and a remnant small portion of the mastoid emissary vein anastomose with suboccipital plexus that is the origin of vertebral veins. The calvarium venous system after an anastomosis with rostral and middle plexuses, unite on the midline ending in the superior sagittal sinus. Then, a separation occurs between cranial lateral vein and right and inferior sagittal sinuses. Finally, the torcular Hérophile is born, i.e. the confluence point at which the drainage systems of skull base and calvarium meet. 123 Anatomic knowledge Anatomic arrangement of venous system within the transverse foramen is a controversial topic among authors. Trolard [17] stated the hypothesis of a vertebral transverse venous sinus similar in arrangement to intracranial venous sinuses. Labbé [8], Walther [19], Gérard [4], Chevrel [2] and Davies [3] described a confluence of veins in plexus. Poirier [14] and Paturet [13] stated the presence of single vertebral vein divided in certain areas. Testut [16] and Rouviére [15] described a single vertebral vein within the transverse foramen canal. According to Walther [19], vertebral veins are always multiple except at the caudal end where a single vertebral trunk is found. Different classifications of vertebral veins have been found in the literature. Poirier [14], Testut and Latarjet [16], classified these veins as the veins of the spine. Whereas, Gérard [4], Davies [3], Paturet [13], Chevrel [2], Rouvière and Delmas [15], respectively, classified vertebral veins as the neck veins, the cranial cava veins, the head and the neck deep veins, and the large venous trunks of the base of the neck. Spinal venous system has been described in three parts [14, 16]: collecting emissary veins, intrarachidial plexuses, and extrarachidial plexuses. In the neck area, vertebral veins and posterior jugular veins are among emissary (collecting) veins which drain plexus blood into the cranial cava system. When vertebral veins are classified as the neck veins [4] or as the large venous trunks of base of the neck [15], their role is the same as that of jugular veins (i.e. internal, external, anterior and posterior), and caudal thyroid veins. Vertebral veins along with posterior jugular veins belong to the back of the neck and spine, in contrast with other cited veins belonging to the anterior of the neck. Each venous trunk of the neck has its separate drainage zone, however, shares anastomoses with numerous neighboring veins. When vertebral veins are classified as cranial cava veins [13], they are the input branches of the branchio-cephalic trunks. Vertebral vein or internal vertebral vein Even though a satellite of the vertebral artery, the vertebral vein only matches the cervical part of the vertebral artery (Fig. 3). Normally described as single [15], sometimes divided in certain areas [13], or even as several venous trunks forming a plexus around the vertebral artery [4]. Or finally accompanied by secondary veins, the vertebral vein runs down anterolaterally to the vertebral artery, i.e. within the concave part of artery’s loop [14]. Indeed, the vertebral vein appears semilunar on imaging cuts. Surg Radiol Anat Fig. 3 Illustration of the vertebral vein. This is an original drawing by the author inspired by Poirier [14], Gérard [4], and Chevrel [2] showing the origin, the course, the ending and the tributaries of the vertebral veins – – Origin: vertebral vein originates in major part from the superior intrarachidial plexuses. It descends near the midline forward to dorsal occipitoatlantal ligament and initially horizontally and externally until reaching the transverse foramen atlas [14]. The vertebral vein emerges above the foramen magnum descending as posterior jugular vein of the occipito-vertebral confluence that correlates it to the intrarachidial veins and the cranial sinuses [16]. Initially, it anastomoses with: dorsal condylar veins, posterior jugular veins, occipital vein and mastoid emissary vein [13]. Course and ending: vertebral vein, upon emerging from the occipital confluence, laterally runs above the vertebral artery, which separates it from the first cervical spinal nerve then, at the transverse process of the atlas, the vertebral vein curves at a right angle and descends vertically into the canal of the transverse process of cervical vertebrae next to the artery [14]. During this course, the artery is placed anterior to the vein [4, 13, 15] which goes around two-third of its perimeter [16], along with the vertebral nerve (of François Franck). According to Paturet, the vertebral vein passes through the transverse foramen of the seventh cervical vertebra, and rarely through the sixth one [13], in contrast with what was suggested by Rouvière [15]. According to Poirier, it passes, along with the artery above the transverse foramen of the sixth cervical vertebra and gains the transverse foramen plexus of the seventh cervical vertebra [14]. Once free, the vertebral vein bends ventrally and caudally, runs behind the internal jugular vein on the lateral and ventral part of vertebral artery. The vertebral vein accompanied by the vertebral artery runs ventrally to – – the caudal cervical ganglion of the sympathic nervous system, and at the left side, runs dorsally to the thoracic duct cross [15]. Then it runs above subclavian artery and ends at the neck base, behind internal jugular vein, draining separately or via a common trunk with posterior jugular vein into the subclavian jugular confluence [13]. Sometimes, the vertebral vein forms a common trunk with ventral vertebral vein, called cervico-vertebral venous trunk, which drains into posterior and caudal part of subclavian vein. It has a valve at its end, and all along its course, the vertebral vein is kept hollow [13]. Gérard described it as having no valves at all [4]. Tributaries [13]: on its course, the vertebral vein receives: primitive anastomotic branches, ventral branches from prevertebral muscles, emissary veins of the deep plexuses of the back of the neck, emissary veins of the intervertebrae foramen and of the spinal rami rising from intrarachidian plexuses [15]. All these primitive tributaries have a regular arrangement and drain into a collector trunk at each intervertebral foramen. The vertebral vein, then receives venous plexus of the seventh intervertebral foramen, branchial plexus network, descending cervical veins (Lauth’s anterior vertebral vein) and deep cervical veins (posterior vertebral vein). According to a few authors, the descending and deep cervical veins join forming a common trunk called common vertebral vein. The vertebral vein joins the upward and deep cervical vein at each level, i.e. it becomes a triple drainage around the transverse processes. Anastomoses [15]: the vertebral vein rises from the anastomosis of its primitive branches with cranial 123 Surg Radiol Anat – sinuses and occipital vein. It anastomoses with the posterior jugular vein at each intervertebral foramen. The vertebral vein joins the rachidian plexuses via its primitive branches and spinal rami. It also anastomoses with the sigmoid part of the lateral sinus via the mastoid emissary vein, and with the external jugular vein via the deep tributaries of occipital veins. Transverse canal: it is made by the overlapping of cervical vertebrae transverse foramina. The canal continues across these foramina, made of fibrous tissue and small ligaments insertions that connect these transverse processes, i.e. forming an osteofibrous tunnel. The vertebral vein is hollow along its course. Once inside of the osteofibrous canal, it is attached to the periosteum via ‘‘radiating fibrous cords’’ [14]. Posterior jugular vein It is a deep vein of the back of the neck. In size, it is usually inverse to the vertebral vein for which it becomes an auxiliary vein. It originates between occipital and atlas veins—result of multiple branches: occipitovertebral veins, uniting intrarachidian plexuses to large muscular veins of the back of the neck, deep occipital veins, magnum foramen plexus, and especially the mastoid vein enlarged by posterior condyloid vein. It receives innumerable plexuses of the back of the neck, which run between muscular planes. Posterior jugular vein is connected: with internal jugular vein via a large anastomosis, with vertebral veins at every intervertebral foramen, with intrarachidian plexuses beneath every vertebral lamina, and with posterior jugular veins on the opposite side. The latter connection is made via a Fig. 4 Illustration of the cranial part the intrarachidian vertebral plexus. This is a drawing by the author inspired by Poirier [14], and Chevrel [2] showing the anastomoses of cranial sinuses with intrarachidian plexuses 123 transverse arcade where dorsal azygos vein originates, and follows the line of spinous process [4]. External vertebral vein This vein has been called trachea vein of Breschet [4] by the author G. Breschet who has also called the vertebral vein as internal. External vertebral vein is described as variable and descending dorsally to articular processes of cervical vertebrae. Internal and external vertebral veins are united via multiple anastomoses. Intrarachidian plexuses They are consisted of: four longitudinal plexuses arranged symmetrically two by two—some anterior and others posterior and a series of transverse plexuses evenly spread out by four—one anterior, one posterior, and two laterally. Transverse plexuses, by joining the longitudinal plexuses form an epidural venous ring. Intervertebral foramen plexuses are also considered as part of intrarachidian plexuses. – Anterior longitudinal plexuses or anterior longitudinal veins (Fig. 4) are placed symmetrically within the vertebrae pedicle and the intervertebral foramen— outside of posterior longitudinal ligament. These longitudinal veins are large flexing veins among which we find one major vein and many accessory veins. These veins form plexuses tightly knit, which are bulkier around the vertebrae than at the discs level. These anterior longitudinal veins do not follow a straight pathway. Their path consists of a series of arcades that follow the curve of the vertebra pedicle, i.e. the lateral concave part, while the ends run through intervertebral Surg Radiol Anat – – – foramen. These longitudinal veins are not sinuses, however, do have some of sinus’s characteristics. At their orifice, we can observe filamentous slants or even areolar membranes [14], immovable and hollow. The ligament system sheltered by the anterior longitudinal veins, sends out lateral extensions which cover these veins, securing them in a rigid manner [14]. These veins do not constitute an even duct and have branches that form anastomoses with each other. In this manner, these veins could rather be called anterior longitudinal plexuses [16]. Anterior transverse plexuses stretch out horizontally from an anterior longitudinal plexus to another one situated on the posterior side of each vertebra. These plexuses are placed between the bony surface and the posterior longitudinal plexus. Intervertebral foramen plexuses drain almost all of the intrarachidian plexuses blood. The intervertebral foramen is a large canal containing an intervertebral venous plexus, an arterial spinal branch, and both dorsal and ventral spinal roots. In the neck area, venous plexuses laterally lead into vertebral veins. These plexuses role via drainage is of outmost importance, they allow ‘‘systolic expansion of the spinal cord and the movement of cerebrospinal fluid’’ [14]. Magnum foramen plexuses constitute the cranial end of intrarachidian veins. They are composed of numerous large sinusoidal veins, anastomosed and arranged in a crown. They receive the veins from the medulla oblongata, basilar plexuses or anterior and posterior occipital sinuses, as well as the anastomoses of the hypoglossal nerve plexus. They flow from each side into the primitive vertebral and posterior jugular veins. These diverse vessels are partly pure veins, soft and sagged, and partly sinusoidal, rigid and hollow. Further away from the skull, and from each vertebra, weaker is the sinusoidal characteristic. In this manner, anterior longitudinal veins are described as ‘‘sinusal in the neck, halfsinusal in the posterior and venous in the lumbar and sacral regions’’ [14]. Extra-rachidian plexuses They are divided by the transverse plexuses into posterior and anterior plexuses. The anterior cervical plexus is placed partly opposite to the vertebrae, and partly forward to the prevertebral muscles. It is narrowed laterally either into the vertebral vein at the intervertebral foramens, or into the anterior vertebral vein. The vertebral veins form an anastomosing system between intra- and extra-rachidian plexuses [20]. Given this arrangement, the vertebral veins, which also ensure the membranes drainage, have a role of intrarachidian pressure adjustment [10]. The rachidian venous system veins have thin walls along with three usual tunics thus are distinguished from cranial sinuses. Valves are observed: at the orifice of the rachidian veins into the vertebral veins, i.e. the intercostal and lumbar, and at the orifice of the latter veins into the large collecting trunks, i.e. azygos and subclavian veins. These valves prevent the blood from flowing back into the vertebral canal [14]. Occipito-vertebral venous confluent or suboccipital venous plexus Vertebral veins along with posterior jugular veins are the major flow pathways of intra- and extra-rachidian plexuses. In the neck area, the posterior extra-rachidian plexus is especially developed within the space between the occipital and atlas veins, where it changes name and becomes occipito-vertebral venous confluent. This confluent anastomosed, on the one hand, with intrarachidian plexus and cranial sinus, and on the other hand, with the sub-cutaneous network, is where vertebral and posterior jugular veins originate [15]. Because of anatomical resemblance between the occipito-vertebral venous confluent and the cavernous sinus, this confluent was named ‘‘suboccipital cavernous sinus’’ by Arnautovic et al. [1]. Resume of the embryogenesis and anatomy of cervical vertebral venous system Embryology textbooks provide detailed descriptions of the development of encephalic veins [12, 13] and that of cranial vena cava system [6, 7, 12, 18]. However, the descriptions particularly in regard to the cervical part of the vertebral veins, are not detailed enough to have a better understanding of the development of its transverse foramen. Paturet [13] who described the venous system draining the skull base, designated the suboccipital plexus as the major origin of the vertebral veins. The knowledge of embryology is essential to understand the segmental development of vertebral veins, in particular, through understanding the segmental nature of the vertebral artery. The latter has been detailed in the past. According to Larsen [7]: ‘‘the intersegmental arteries of the cervical region anastomose with each other. Pairs of vertebral arteries arise from longitudinal anastomoses, which unite forming a vessel that then looses its intersegmental connections with the aorta’’. In line with the above observation, the knowledge of venous system helps at understanding the plexiform arrangement of vertebral 123 Surg Radiol Anat veins. [13]. Indeed, the dorsal dural venous plexus, which initially drains the medulla oblongata and the spinal cord, similar to the other cranial sinuses, goes by a plexiform stage during embryonic development. The cranial sinuses developmental plexiform stage explains their formation by the internal trabecular system. Several authors [12, 13] have described the embryonic plexiform arrangement of the encephalic venous system. The vertebral veins originate mostly from the suboccipital plexus, however, show a plexiform arrangement. The above observations are in contrast with and challenge the hypothesis of a transverse vertebral sinus put forward by Trolard [8, 11]. The vertebral vein as a single vessel was described by Rouviére [15] and others: Poirier [14] and Paturet [13]. The latter further stated that the vertebral vein was divided into halves at certain areas, matching a plexiform arrangement. Testut [16] also described the vertebral vein as a single vessel, referring to Walther [19] description, i.e. a multiple vessel but with a single inferior trunk. Last, Gérard [4] gave a description of several vessel trunks in plexus around the artery. The clinical application of transcondylar far lateral approach which can cause hemorrhage during this route opening rostral cervical vertebrae and craniovertebral junction and exposing V2 and V3 segment of the vertebral artery and peritransversous venous system [9]. Furthermore, the review of the literature on embryology, craniocaudal folding and, in particular, the nervous system [18] suggests an arrangement of ventral longitudinal veins as follows: ‘‘sinusal at the neck, half-sinusal in the dorsal region and venous at the lumbar and sacral regions’’ [14]. In line with the above, the vertebral veins originate from plexus, e.g. suboccipital plexus, and end in a single venous trunk draining into the subclavian vein. In this manner, once again, we observe a specific arrangement of vertebral venous system evolving in line with craniocaudal folding development. All of the above reviewed descriptions are consistent with regard to the location of the vertebral veins within the transverse canal, i.e. lateral to the vertebral artery. This description was further detailed by Poirier [14], placing these veins at the external end of the artery inside of the 123 concave part of its loop, exhibiting a semilunar arrangement on most imaging cuts. 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