FROM THE INSTITUTE OF PATHOLOGY, SECTION OF NEUROPATHOLOGY, UNIVERSITY OF OSLO, RIKSHOSPITALET, OSLO, NORWAY.
SPINAL CORD VASCULARITY II. Extraspinal sources of spinal cord arteries in the rat LEON TVETEN
The main purpose of the present series of investigations of the spinal cord vascularity was to obtain a basis allowing an estimate of functional disturbances following injury of arteries of the spinal cord. A thorough knowledge of the anatomy of the vascular supply is then a prerequisite, and previously (TVETEN 1976 a) conditions in man were reported. Evaluation of the dynamics of cord dysfunction necessitates animal experiments. Rats were chosen, because GREENE (1959) reported a close similarity of the vascularity in rat and man. Admittedly, only the larger aortic branches were described, while the arrangement of arterial tributaries to the spinal cord were not recorded in sufficient detail for experimental application. Therefore, a detailed investigation of the extraspinal arteries and potential collateral pathways regarding the spinal cord circulation in the rat was performed.
Material and Methods The material included a total of 115 rats of both sexes, 72 were adults and 43 young' or newborn rats belonging to eight litters. Each litter comprised 3 to 7 animals and the age ranged from 1, 2 and 4 days to 1, 2, 4, 6 and 8 weeks. The vascular system Submitted for publication 5 December 1974. Acta Radiologica Diagnosis /7 (/976) Fasc, 2 March
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in rats is considered fully developed already at 13 to 15 days of fetal life (MOFFAT 1957).
Injection technique. Heparin (50 unitsjlOO g body weight) and Pentobarbital sodium (Nembutal, Abbott, 3.3 mg/IOO g body weight) was administered into the peritoneal cavity. About half an hour later injection of the contrast medium was performed by the method of CAMMERMEYER (1960), except that in adult animals, the injection pressure was controlled by a manometer connected to the injection tube. The animals died during or immediately after the contrast injection. A warm (37 to 38°C), 80 or 50 (X) aqueous suspension of coloured contrast medium (Chromopaque Blue, Damancy & Co. Ltd., England) with 4 % formalin and 10 % gelatine, kept in a water bath on a magnetic stirrer, was used to demonstrate the vessels. The viscosity of the 80 % suspension as a rule prevented penetration of the capillary network. The injection pressure was kept at 120 to 130 mm Hg and the procedure was usually accomplished in 10 to 15 min. A blue discoloration of the mouth and eyes was a reliable indication of adequate filling of the vascular system. Three to four ml of the contrast medium was sufficient to fill the arteries in adult animals. Following the injection the skin and the viscera were removed while the aorta and its main branches were kept intact with the specimen and placed in a solution of 10% formalin and physiologic saline overnight. Thereafter the specimen was processed for radiography and stereomicroscopy as previously described (TVETEN 1976 a). The tube with a focal size of 0.4 mm x 8 mm was run at 20 to 35 k V, 15 to 25 mA for 20 to 30 min, FFD 25 to 150 cm, all adjusted to the thickness of the specimen.
Results The main sources of blood supply to the spinal cord of the rat may be divided into two groups. The subclavian-vertebral system supplies the cervical cord and the upper 3 or 4 segments of the thoracic cord. The descending aorta supplies the remaining part of the cord and the cauda equina by way of the aortic intercostal, the subcostal, the lumbar and the sacral arteries. The lumbar and sacral arteries are mainly distributed to the nerve roots and the dorsal root ganglia of the cauda equina. The origin, course and branching of the vertebral artery in the rat to a large extent corresponds to conditions in man (Fig. I). The arrangement of the spinal branches, however, differs somewhat in the two species. In the rat the vertebral artery supplies regular branches to all intervertebral foramina of the cervical region, frequently even to the one between the seventh cervical and the first thoracic vertebra (Fig. 2). Contrary to conditions in man, no additional branches from other neck arteries enter the foramina. The spinal branches of the cervical region in the rat divide and interconnect in a manner similar to that in man, i.e. small branches from each artery anastomose with
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Fig. 1 Fig. 2 Fig. 1. Angiography. The arrangement of neck arteries in the rat. Descending aorta (A), Carotid artery (Ca), Vertebral artery (Va), Ascending cervical artery (As), Costocervical trunk (Ct), Deep cervical artery (Pa), Superior intercostal artery (sia). Spinal branches (asb, ssb) from the first posterior intercostal (aia) and the superior intercostal (sia) artery. Displacement of the right vertebral artery (Va) at C6 (+--+). 1 = first, 4 = fourth rib. Fig. 2. Transparent specimen of cervical region, photography. Origin of root arteries (r), all derived from the vertebral artery (Va) even that at CB segment (rCB). Spinal cord (Sc), ventral (asa) and dorsal (psa) spinal arteries.
similar branches from above and below as well as with branches from the opposite side. These interconnections form transverse and longitudinal anastomotic chains, being most evident on the dorsal surface of the vertebral bodies. Additional transverse connections are also formed by small penetrating twigs inside the vertebral bodies.
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Fig. 3
Fig. 4
Fig. 3. Angiography. Hypoplastic right vertebral (Va) artery. Basilar artery (Ba). Fig. 4. Angiography. Left vertebral artery (Va) dividing into a medial branch (mb) which runs along the C7 nerve root to join the ventral spinal artery (asa) and a lateral branch (Ib) entering the vertebral canal at C5 (++). Displacement of the right vertebral artery (Va) into the spinal canal at C6 and C5. Distal parts of the common carotid arteries (c).
The lateral segmental branches of the vertebral artery ramify into the deep muscles of the neck and connect with branches of other neck arteries. The incidence of extracranial variations of the vertebral artery was unexpectedly high. A hypoplastic vertebral artery similar to that in man occurred in about 8 per cent (9 of 115) of the animals, and twice as often on the left as on the right side (Fig. 3). In one specimen the left vertebral artery divided close to its origin into a small medial branch which entered the transverse foramen of the sixth cervical vertebra, and a large lateral branch extending to the fifth vertebra before it traversed the foramen (Fig. 4). In another specimen the same condition existed except that the two branches arose separately from the left subclavian artery. In a third specimen the
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Fig. 5
Fig. 6
Fig. 5. Angiography. Right vertebral artery (Va) branching from the cervical trunk (Cet) to enter the transverse foramen of the fifth cervical vertebra (-+ ).Common carotid artery (C). Fig. 6. Transparent specimen, photography. Interruption of. the left vertebral artery (Va) at C5, ( +- ) = the gap between the ends of the artery. Anastomoses between spinal branches (sb) from the upper and lower end of the interrupted artery and also connections with the ventral spinal artery (asa).
right vertebral artery branched off from the cervical trunk (which corresponds to the thyreocervical trunk in man) and entered the transverse foramen of the fifth cervical vertebra (Fig. 5). The most common variation was a segmental anomaly of the cervical part of the vertebral artery, usually at C4 or C5 and predominantly on the left side (Fig. 6). The anomaly was observed in about 17 per cent of the cases (9 adults and II youngsters) and consisted either of a complete interruption of the artery or in a displacement into the vertebral canal. In the latter case the artery extended one or two segments along the lateral surface of the cervical cord outside the dura mater (Figs 1,4).
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At the upper or the lower end of the defect the artery usually connected with the ventral spinal artery by way of radicular arteries, thus forming a large intraspinal pathway between the two broken parts of the vertebral artery (Fig. 7). Occasionally, a similar but less evident connection existed immediately outside the vertebral canal formed by the lateral segmental branches (Fig. 7). The transverse foramen of the cervical vertebra at the site of the interrupted or displaced artery was usually absent. At the upper end of the atlas the defective artery sometimes disappeared into the suboccipital region leaving no or only a tiny twig to join the intracranial part of the opposite vertebral artery (Fig. 7).
The ascending cervical artery arose from the cervical trunk which according to GREENE corresponds to the thyreocervical trunk in man. The artery soon divided into 2 or 3 branches (Fig. 1). The larger of these extended in front of the transverse processes of the cervical vertebrae from C6 or C7 to C2 or C3 giving off branches to the muscles and the nerve trunks, in addition to tiny connections with the lateral branches of the vertebral artery. Contrary to the situation in man, no significant branch from the ascending cervical artery in the rat entered the intervertebral foramina of the cervical region. The costocervical trunk in the rat gave rise to the deep cervical artery and the superior intercostal artery (Fig. 1). The former, often small-sized and difficult to identify, gave off spinal branches to the intervertebral foramen between the seventh cervical and the first thoracic vertebra but no significant spinal cord feeder was ever observed arising from this artery. It disappeared into the muscles at the back of the neck connecting with branches of other arteries in the neck. The superior intercostal artery in the rat was a conspicuous vessel distributing a series of branches to the upper four intercostal spaces on the right side, less constantly the upper three only on the left side (Fig. 1). The mode of branching and the number of spaces supplied by the artery, however, varied somewhat in individual cases, consistent with variations in the arrangement of the upper aortic intercostal arteries (see below). The spinal arteries of the costocervical trunk divided and interconnected in a manner similar to that of the spinal branches of the vertebral artery, but they rarely gave rise to significant root arteries extending to the surface of the cord. In fact, as emphasized in another report (TVETEN 1976 b), the poor supply of the upper thoracic cord was closely related to a scanty regional distribution of the costocervical trunk. The most common arrangement of the aortic intercostal arteries was nine arteries on the left side and eight on the right. They were distributed from the left fourth and the right fifth to the twelfth spaces and divided into one ventral and one dorsal branch. A large number of the animals, however, displayed variations in the origin and the branching of the vessels in the upper part of the thoracic cavity. Thus, in
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Fig. 7
Fig. 8
Fig. 7. Angiography. Interruption of both vertebral arteries (Va), on the right at C4 (the gap ++), on the left both at C4 and C5. Large intra- (ic) and extraspinal (ec) connections between the two broken parts of the right artery. On the left side a large ventral root artery (r) arises from the lower end of the interrupted artery to join the ventral spinal artery (asa). Fig. 8. Transparent specimen, photography. Dorsal view of the cervical and upper thoracic regions of the rat. Arrangement of the superior intercostal arteries (sia). Separate origin of the two branches in the left fourth intercostal space (4is), the dorsal branch (db) being supplied by the first aortic intercostal (aia), while the ventral branch (vb) originates from the superior intercostal artery (sia). The right superior intercostal artery branches in the regular way into a ventral (vb) and a dorsal (db) twig to the upper four intercostal spaces (is). Subclavian artery (sub).
about 20 per cent (22 of 115) of the specimens, the third intercostal artery on the left side branched off from the aorta. In about half of these cases, however, the aortic segmental artery was represented by its proximal part plus the dorsal branch only, the ventral branch being supplied by the superior intercostal artery (Fig. 8). The same feature was recorded in the left fourth intercostal space in about 25 per cent of the specimens, both in the left fourth and the third spaces in about 5 per cent of the cases. On the right side, similar variations confined to the fourth intercostal space were found in four animals only. Finally, 2 animals revealed 'aortic intercostals symmetrically arranged from the fifth to the twelfth spaces.
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Fig. 9. Angiography. The arrangement of extraspinal arteries in the lower thoracic and the upper two thirds of the lumbar region. The left aortic subcostal artery (asuba) furnishes the dorsal branch only, the ventral branch (vbr) being supplied by the twelfth intercostal artery (12ia). Ventral root arteries (r) arising from the left twelfth intercostal artery and the right subcostal artery to join the ventral spinal artery (asa) are discernible. The upper four lumbar arteries (I La-4La).
Most of the ventral feeders of the upper thoracic cord follow the left Th3 nerve root (TvETEN 1976 b). The vast majority of these vessels originates from the aortic intercostals. In 2 cases only a significant ventral feeder of the third thoracic segment of the cord could be traced back to the spinal branch of the superior intercostal artery. This observation supports the view that the costocervical trunk is of minor importance regarding the spinal cord circulation in rats. The subcostal artery in the rat is the most important branch of the thoracic aorta because it frequently distributes large tributaries to the spinal cord, i.e. the great ventral radicular artery (TVETEN 1976 b). It runs along the lower border of the thirteenth rib and, as a rule, divides in the same way as the aortic intercostals. However, in about one-third (36/115) of the specimens the proximal part plus the dorsal branch only of the segmental artery was present while the ventral branch was supplied by the last intercostal or, occasionally, by the first lumbar artery (Fig. 9). This occurred twice as often on the left as on the right side, bilaterally in about 5 per cent of the
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Fig. 10. Angiography. Arteries of the lower lumbar and sacral region in the rat. The fifth pair of lumbar arteries (5La) arises from the aorta (A), while the sixth pair of lumbar arteries (6La) and the paired sacral arteries (lSa-3Sa) arise from the median sacral artery (Ma). The exact origin of the sixth pair of lumbar arteries is clearly visible in lateral position of the specimen only. Bifurcation of the aorta (A) into the common iliac arteries (Cia) at the border between the sixth lumbar (L6) and the first sacral (S 1) vertebral bodies. Ileolumbar arteries (la).
specimens. Characteristically, a significant tributary to the cord was never found originating from such a 'rudimentary' subcostal artery. Of the 6 pairs of lumbar arteries, the upper five arose from the dorsal aspect of the aorta while the sixth pair came from the median sacral artery (Figs 9, 10). The spinal branch of the latter passed through the foramen between the sixth lumbar and the first sacral vertebrae. Only the upper 2 or 3,"o'pairs of the lumbar arteries contributed to the supply of the spinal cord (TVETEN 1976 b). The other root arteries of the lumbo-sacral region terminated mainly on the nerve roots and the dorsal root ganglia. However, in the lumbo-sacral region a number of dorsal root arteries created evident anastomoses with central branches of the ventral spinal artery (described in more detail in another report, TVETEN 1976 b). The median sacral artery originated from dorsal aspect of the terminal part of the aorta at the level of the fifth or the sixth lumbar vertebra and extended into the tail
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Fig. 11. Transparent specimen, photography. Dorsal view of the lumbar region with intact spinal cord in a decalcified specimen. Tiny extraspinal connections between adjacent lumbar arteries (-+).
(Fig. 10). It gave rise to segmental arteries which distributed spinal branches to the sacral region. The ileolumbar arteries in the rat were constant branches of the lumbar aorta, though the origin varied somewhat on the two sides (Fig. 10). However, no evident spinal branch was ever observed originating from these arteries. At each level of the thoracic, lumbar and sacral regions tiny branches from the segmental arteries interconnected inside as well as outside the vertebral canal in a manner similar to that in man (F'g. 11). As in man evident anastomoses were found between the aortic segmental arteries and the internal mammary artery, and between the inferior and the superior epigastric arteries, respectively. Discussion
The anatomic arrangement of the main sources of spinal cord arteries in the rat resembles that in man. However, important differences exist. Thus, in the rat the vertebral artery appears to be the sole source of blood supply to the cervical cord. Contrary to the situation in man, no additional branches from other arteries in the neck enter the intervertebral foraminae of the cervical region in the rat. A high incidence of variations of the vertebral artery existed in the rat; some of
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these also being similar to those observed in man, such as different width of the two arteries, hypoplasia and abnormal origin or site of entrance into the cervical spine. The major abnormality, however, which does not seem to have been previously described in man or in experimental animals was a segmental defect or displacement of parts of the vertebral artery. This peculiar anomaly can be explained from developmental features of the brachiocephalic arteries in rats. MOFFAT (1957, 1961) states that the vertebral artery is formed by fusion of longitudinal anastomoses between the postcostal branches of the primitive intersegmental arteries. Evidently, when such anastomoses fail to develop, a defect involving one or more segments of the artery will ensue. The superior intercostal artery of the costocervical trunk is more prominent in the rat than in man, though GREENE believes that in the rat this artery supplies only the upper three intercostal spaces, and on the left side frequently the first and the second spaces only. She also believes that separate origins of the ventral and dorsal branches of the left third and the fourth intercostal artery occur in about two thirds of the specimens. The dorsal branch is then supplied by the aorta, the ventral one by the superior intercostal artery. Such variations were less frequently observed in the present material and in the vast majority of the rats the superior intercostal artery distributed a series of regular branches to the upper three intercostal spaces on the left side and the upper Iour on the right side. This is important to consider because of the paucity of significant spinal tributaries to the upper thoracic cord, described in closer detail in another report (TVETEN 1976 b). The poor supply of spinal feeders to the upper three or four thoracic segments of the cord in individual cases was closely related to the regional distribution of the superior intercostal artery. Thus, with regard to the spinal cord circulation in rats, the costocervical trunk seems merely to serve as an anastomotic link between the vertebral artery above and the aortic intercostals below by way of intra- as well as extraspinal connections between these arteries. In accordance with the arrangement of the superior intercostal artery and the fact that the rat possesses thirteen thoracic vertebrae, the most common number of the aortic intercostal arteries is nine on the left side and eight on the right side. In the rat two aortic intercostals arising from a common stem was a rare finding, contrary to the situation in man. The origin of the subcostal branches in the rat, similar to the condition in man, frequently varied. The high incidence of a rudimentary or hypoplastic aortic subcostal artery was remarkable considering the frequent occurrence of important spinal cord tributaries (the great ventral radicular artery, or Adamkiewicz' artery) arising from the subcostal space of the rat (TVETEN 1976 b). It was found, however, that an aortic subcostal artery with no ventral branch rarely gave rise to spinal cord tributaries, a feature probably reflecting a natural protective means (TVETEN 1976 a). GREENE described five pairs of lumbar segmental arteries in the rat, the upper four arising from the dorsal aspect of the aorta while the fifth pair branched off from the 12 - 765845
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median sacral artery. Moreover, this author claimed that the ileolumbar arteries not infrequently arise from the common iliac arteries and supply spinal branches to the intervertebral foramen between the last lumbar and the first sacral vertebrae. BRAITHWAITE (1954) in a schematic drawing also depicted only five lumbar segmental arteries although segmental branches from the median sacral artery entering the vertebral canal between the sixth lumbar and the first sacral vertebrae are clearly visible in his angiographic illustrations. In the present material the ileolumbar arteries were constant branches of the lumbar aorta and contrary to those in man, they never supplied significant branches to the spinal canal. As in man, the segmental branches of the vertebro-subclavian arteries and the aorta in the rat interconnected profusely along the entire length of the vertebral column, both inside and outside the spinal canal, forming transverse and longitudinal anastomotic chains. In addition, extensive anastomoses similar to those observed in man occur between the aortic segmental branches and the large arteries on the antero-lateral body-wall such as the internal mammary artery, the superior and inferior epigastric arteries.
SUMMARY The arrangement of extravertebral sources of spinal cord arteries in the rat is similar to that in man. Some differences, however, do exist, concerning mainly the arrangement of spinal branches supplied by the subclavian-vertebral arteries. Contrary to the situation in man, the vertebral artery in the rat appears to be the sole source of blood supply to the cervical cord. A high incidence of variations or anomalies of the vertebral artery in the rat existed. Vascular variations in the upper left thoracic spaces were frequent in the rat and more complicated than in man. In both species, a poor supply of significant spinal cord feeders from the superior intercostal artery of the costocervical trunk was found. Variations in the origin and branching of the aortic segmental arteries occur in both species. In man the major variation consists of two or more intercostal arteries arising from a common stem, while the rat more often displays a rudimentary subcostal artery. Finally, the ileolumbar arteries in the rat are constant branches of the lumbar aorta. Despite these differences in the vascular anatomy, the rat seems to be well suited for experimental comparative investigations, not feasible in man.
ZUSAMMENFASSUNG Die Anordnung der extravertebralen Versorgungen der Arterien der Wirbelsaule bei der Ratte ist der dem Menschen ahnlich, Einige Unterschiede betreffen hauptsachlich den Aufbau der Spinalaste, die durch die A. subclavia-A, vertebral is versorgt werden. Im Gegensatz zur Situation beim Menschen scheint die Vertebralarterie bei der Ratte die einzige Blutversorgungsquelle der Wirbelsaule zu sein. Es besteht bei der Ratte eine hohe Frequenz von Variationen oder Anomalien der Vertebralarterie. Vaskulare Variationen in den oberen linken Thoraxabschnitten waren bei der Ratte haufiger komplizierter als beim Menschen. Bei beiden Spezies fand sich eine geringfiigige Versorgung signifikanter Wirbelsaulen Aste von der oberen lnterkostal-Arterie des costo-cervikalen Stamms. Variationen im Ursprung und der Verzweigung der Aorta-Segment-Arterien fand sich bei beiden Spezies.
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Beim Menschen besteht die wesentliche Abweichung in zwei oder mehr Intercostal-Arterien, die von einem gemeinsamen Stamm ausgehen, wahrend die Ratte haufiger eine rudimentaren subcostale Arterie aufweist. Schliesslich sind die ileo-lumbal Arterien bei der Ratte konstante Aste der lumbalen Aorta. Trotz dieser Unterschiede in der vaskularen Anatomie scheint die Ratte gut geeignet fur vergleichende experimentelle Untersuchungen zu sein, die beim Menschen nicht vorgenommen werden konnen.
RESUME La disposition des sources extra vertebrales des arteres de la moelle chez Ie rat est semblable
a celIe de l'homme. Cependant certaines differences existent, concernant surtout la disposition des branches spinales fournies par les arteres sous-clavieres-vertebrales, A la difference de ce qui se passe chez l'homme, l'artere vertebrale du rat parait etre la seule source d'irrigation sanguine de la moelle cervicale. II y a de nombreuses variations ou anomalies de l'artere vertebrale chez le rat. Les variations vasculaires des espaces thoraciques superieurs gauches sont frequentes chez le rat et plus compliquees que chez l'homme. Dans ces deux especes, l'auteur a trouve une faible irrigation d'importants vaisseaux nourriciers de la moelle provenant de l'artere intercostale superieure du tronc costocervical. Des variations de l'origine et de la ramification des arteres segmentaires arterielles se produisent dans ces 2 especes. Chez l'homme la variation principale consiste dans l'origine par un tronc commun de 2 ou plusieurs arteres intercostales alors que le rat a plus souvent une artere sous-costale rudimentaire. Enfin, les arteres ilio-Iombaires du rat sont des branches constantes de l'aorte lombaire. Malgre ces differences dans l'anatomie vasculaire, Ie rat parait convenir pour des recherches experimentales comparatives qui ne peuvent pas etre faites chez l'homme.
REFERENCES BRAITHWAITE J. L.: The morphology of the collateral circulation following complete interruption of the abdominal aorta in the rat. J. Anat. (Lond.) 88 (1954), 204. CAMMERMEYER J.: Differences in shape and size of neuroglial nuclei in the spinal cord due to individual regional and technical variations. Acta anat. 40 (1960), 149. GREENE E. c.: Anatomy of the rat. Hafner Publishing Co., New York 1959. MOFFAT D. B.: The development of the hindbrain arteries in the rat. J. Anat. (Lond.) 91 (1957), 25. - The development of the anterior cerebral artery and its related vessels in the rat. Amer. J. Anat. 108 (1961), 17. TVETEN L. (a): Spinal cord vascularity. I. Extraspinal sources of spinal cord arteries in man. Acta radiol. Diagnosis 17 (1976), 1. - (b): Spinal cord vascularity. IV. The spinal cord arteries in the rat. To be published in Acta radiol. Diagnosis 17 (1976).
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SPINAL CORD VASCULARITY II. Extraspinal sources of spinal cord arteries in the rat LEON TVETEN
The main purpose of the present series of investigations of the spinal cord vascularity was to obtain a basis allowing an estimate of functional disturbances following injury of arteries of the spinal cord. A thorough knowledge of the anatomy of the vascular supply is then a prerequisite, and previously (TVETEN 1976 a) conditions in man were reported. Evaluation of the dynamics of cord dysfunction necessitates animal experiments. Rats were chosen, because GREENE (1959) reported a close similarity of the vascularity in rat and man. Admittedly, only the larger aortic branches were described, while the arrangement of arterial tributaries to the spinal cord were not recorded in sufficient detail for experimental application. Therefore, a detailed investigation of the extraspinal arteries and potential collateral pathways regarding the spinal cord circulation in the rat was performed.
Material and Methods The material included a total of 115 rats of both sexes, 72 were adults and 43 young' or newborn rats belonging to eight litters. Each litter comprised 3 to 7 animals and the age ranged from 1, 2 and 4 days to 1, 2, 4, 6 and 8 weeks. The vascular system Submitted for publication 5 December 1974. Acta Radiologica Diagnosis /7 (/976) Fasc, 2 March
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in rats is considered fully developed already at 13 to 15 days of fetal life (MOFFAT 1957).
Injection technique. Heparin (50 unitsjlOO g body weight) and Pentobarbital sodium (Nembutal, Abbott, 3.3 mg/IOO g body weight) was administered into the peritoneal cavity. About half an hour later injection of the contrast medium was performed by the method of CAMMERMEYER (1960), except that in adult animals, the injection pressure was controlled by a manometer connected to the injection tube. The animals died during or immediately after the contrast injection. A warm (37 to 38°C), 80 or 50 (X) aqueous suspension of coloured contrast medium (Chromopaque Blue, Damancy & Co. Ltd., England) with 4 % formalin and 10 % gelatine, kept in a water bath on a magnetic stirrer, was used to demonstrate the vessels. The viscosity of the 80 % suspension as a rule prevented penetration of the capillary network. The injection pressure was kept at 120 to 130 mm Hg and the procedure was usually accomplished in 10 to 15 min. A blue discoloration of the mouth and eyes was a reliable indication of adequate filling of the vascular system. Three to four ml of the contrast medium was sufficient to fill the arteries in adult animals. Following the injection the skin and the viscera were removed while the aorta and its main branches were kept intact with the specimen and placed in a solution of 10% formalin and physiologic saline overnight. Thereafter the specimen was processed for radiography and stereomicroscopy as previously described (TVETEN 1976 a). The tube with a focal size of 0.4 mm x 8 mm was run at 20 to 35 k V, 15 to 25 mA for 20 to 30 min, FFD 25 to 150 cm, all adjusted to the thickness of the specimen.
Results The main sources of blood supply to the spinal cord of the rat may be divided into two groups. The subclavian-vertebral system supplies the cervical cord and the upper 3 or 4 segments of the thoracic cord. The descending aorta supplies the remaining part of the cord and the cauda equina by way of the aortic intercostal, the subcostal, the lumbar and the sacral arteries. The lumbar and sacral arteries are mainly distributed to the nerve roots and the dorsal root ganglia of the cauda equina. The origin, course and branching of the vertebral artery in the rat to a large extent corresponds to conditions in man (Fig. I). The arrangement of the spinal branches, however, differs somewhat in the two species. In the rat the vertebral artery supplies regular branches to all intervertebral foramina of the cervical region, frequently even to the one between the seventh cervical and the first thoracic vertebra (Fig. 2). Contrary to conditions in man, no additional branches from other neck arteries enter the foramina. The spinal branches of the cervical region in the rat divide and interconnect in a manner similar to that in man, i.e. small branches from each artery anastomose with
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Fig. 1 Fig. 2 Fig. 1. Angiography. The arrangement of neck arteries in the rat. Descending aorta (A), Carotid artery (Ca), Vertebral artery (Va), Ascending cervical artery (As), Costocervical trunk (Ct), Deep cervical artery (Pa), Superior intercostal artery (sia). Spinal branches (asb, ssb) from the first posterior intercostal (aia) and the superior intercostal (sia) artery. Displacement of the right vertebral artery (Va) at C6 (+--+). 1 = first, 4 = fourth rib. Fig. 2. Transparent specimen of cervical region, photography. Origin of root arteries (r), all derived from the vertebral artery (Va) even that at CB segment (rCB). Spinal cord (Sc), ventral (asa) and dorsal (psa) spinal arteries.
similar branches from above and below as well as with branches from the opposite side. These interconnections form transverse and longitudinal anastomotic chains, being most evident on the dorsal surface of the vertebral bodies. Additional transverse connections are also formed by small penetrating twigs inside the vertebral bodies.
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Fig. 3
Fig. 4
Fig. 3. Angiography. Hypoplastic right vertebral (Va) artery. Basilar artery (Ba). Fig. 4. Angiography. Left vertebral artery (Va) dividing into a medial branch (mb) which runs along the C7 nerve root to join the ventral spinal artery (asa) and a lateral branch (Ib) entering the vertebral canal at C5 (++). Displacement of the right vertebral artery (Va) into the spinal canal at C6 and C5. Distal parts of the common carotid arteries (c).
The lateral segmental branches of the vertebral artery ramify into the deep muscles of the neck and connect with branches of other neck arteries. The incidence of extracranial variations of the vertebral artery was unexpectedly high. A hypoplastic vertebral artery similar to that in man occurred in about 8 per cent (9 of 115) of the animals, and twice as often on the left as on the right side (Fig. 3). In one specimen the left vertebral artery divided close to its origin into a small medial branch which entered the transverse foramen of the sixth cervical vertebra, and a large lateral branch extending to the fifth vertebra before it traversed the foramen (Fig. 4). In another specimen the same condition existed except that the two branches arose separately from the left subclavian artery. In a third specimen the
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Fig. 5
Fig. 6
Fig. 5. Angiography. Right vertebral artery (Va) branching from the cervical trunk (Cet) to enter the transverse foramen of the fifth cervical vertebra (-+ ).Common carotid artery (C). Fig. 6. Transparent specimen, photography. Interruption of. the left vertebral artery (Va) at C5, ( +- ) = the gap between the ends of the artery. Anastomoses between spinal branches (sb) from the upper and lower end of the interrupted artery and also connections with the ventral spinal artery (asa).
right vertebral artery branched off from the cervical trunk (which corresponds to the thyreocervical trunk in man) and entered the transverse foramen of the fifth cervical vertebra (Fig. 5). The most common variation was a segmental anomaly of the cervical part of the vertebral artery, usually at C4 or C5 and predominantly on the left side (Fig. 6). The anomaly was observed in about 17 per cent of the cases (9 adults and II youngsters) and consisted either of a complete interruption of the artery or in a displacement into the vertebral canal. In the latter case the artery extended one or two segments along the lateral surface of the cervical cord outside the dura mater (Figs 1,4).
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At the upper or the lower end of the defect the artery usually connected with the ventral spinal artery by way of radicular arteries, thus forming a large intraspinal pathway between the two broken parts of the vertebral artery (Fig. 7). Occasionally, a similar but less evident connection existed immediately outside the vertebral canal formed by the lateral segmental branches (Fig. 7). The transverse foramen of the cervical vertebra at the site of the interrupted or displaced artery was usually absent. At the upper end of the atlas the defective artery sometimes disappeared into the suboccipital region leaving no or only a tiny twig to join the intracranial part of the opposite vertebral artery (Fig. 7).
The ascending cervical artery arose from the cervical trunk which according to GREENE corresponds to the thyreocervical trunk in man. The artery soon divided into 2 or 3 branches (Fig. 1). The larger of these extended in front of the transverse processes of the cervical vertebrae from C6 or C7 to C2 or C3 giving off branches to the muscles and the nerve trunks, in addition to tiny connections with the lateral branches of the vertebral artery. Contrary to the situation in man, no significant branch from the ascending cervical artery in the rat entered the intervertebral foramina of the cervical region. The costocervical trunk in the rat gave rise to the deep cervical artery and the superior intercostal artery (Fig. 1). The former, often small-sized and difficult to identify, gave off spinal branches to the intervertebral foramen between the seventh cervical and the first thoracic vertebra but no significant spinal cord feeder was ever observed arising from this artery. It disappeared into the muscles at the back of the neck connecting with branches of other arteries in the neck. The superior intercostal artery in the rat was a conspicuous vessel distributing a series of branches to the upper four intercostal spaces on the right side, less constantly the upper three only on the left side (Fig. 1). The mode of branching and the number of spaces supplied by the artery, however, varied somewhat in individual cases, consistent with variations in the arrangement of the upper aortic intercostal arteries (see below). The spinal arteries of the costocervical trunk divided and interconnected in a manner similar to that of the spinal branches of the vertebral artery, but they rarely gave rise to significant root arteries extending to the surface of the cord. In fact, as emphasized in another report (TVETEN 1976 b), the poor supply of the upper thoracic cord was closely related to a scanty regional distribution of the costocervical trunk. The most common arrangement of the aortic intercostal arteries was nine arteries on the left side and eight on the right. They were distributed from the left fourth and the right fifth to the twelfth spaces and divided into one ventral and one dorsal branch. A large number of the animals, however, displayed variations in the origin and the branching of the vessels in the upper part of the thoracic cavity. Thus, in
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Fig. 8
Fig. 7. Angiography. Interruption of both vertebral arteries (Va), on the right at C4 (the gap ++), on the left both at C4 and C5. Large intra- (ic) and extraspinal (ec) connections between the two broken parts of the right artery. On the left side a large ventral root artery (r) arises from the lower end of the interrupted artery to join the ventral spinal artery (asa). Fig. 8. Transparent specimen, photography. Dorsal view of the cervical and upper thoracic regions of the rat. Arrangement of the superior intercostal arteries (sia). Separate origin of the two branches in the left fourth intercostal space (4is), the dorsal branch (db) being supplied by the first aortic intercostal (aia), while the ventral branch (vb) originates from the superior intercostal artery (sia). The right superior intercostal artery branches in the regular way into a ventral (vb) and a dorsal (db) twig to the upper four intercostal spaces (is). Subclavian artery (sub).
about 20 per cent (22 of 115) of the specimens, the third intercostal artery on the left side branched off from the aorta. In about half of these cases, however, the aortic segmental artery was represented by its proximal part plus the dorsal branch only, the ventral branch being supplied by the superior intercostal artery (Fig. 8). The same feature was recorded in the left fourth intercostal space in about 25 per cent of the specimens, both in the left fourth and the third spaces in about 5 per cent of the cases. On the right side, similar variations confined to the fourth intercostal space were found in four animals only. Finally, 2 animals revealed 'aortic intercostals symmetrically arranged from the fifth to the twelfth spaces.
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Fig. 9. Angiography. The arrangement of extraspinal arteries in the lower thoracic and the upper two thirds of the lumbar region. The left aortic subcostal artery (asuba) furnishes the dorsal branch only, the ventral branch (vbr) being supplied by the twelfth intercostal artery (12ia). Ventral root arteries (r) arising from the left twelfth intercostal artery and the right subcostal artery to join the ventral spinal artery (asa) are discernible. The upper four lumbar arteries (I La-4La).
Most of the ventral feeders of the upper thoracic cord follow the left Th3 nerve root (TvETEN 1976 b). The vast majority of these vessels originates from the aortic intercostals. In 2 cases only a significant ventral feeder of the third thoracic segment of the cord could be traced back to the spinal branch of the superior intercostal artery. This observation supports the view that the costocervical trunk is of minor importance regarding the spinal cord circulation in rats. The subcostal artery in the rat is the most important branch of the thoracic aorta because it frequently distributes large tributaries to the spinal cord, i.e. the great ventral radicular artery (TVETEN 1976 b). It runs along the lower border of the thirteenth rib and, as a rule, divides in the same way as the aortic intercostals. However, in about one-third (36/115) of the specimens the proximal part plus the dorsal branch only of the segmental artery was present while the ventral branch was supplied by the last intercostal or, occasionally, by the first lumbar artery (Fig. 9). This occurred twice as often on the left as on the right side, bilaterally in about 5 per cent of the
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Fig. 10. Angiography. Arteries of the lower lumbar and sacral region in the rat. The fifth pair of lumbar arteries (5La) arises from the aorta (A), while the sixth pair of lumbar arteries (6La) and the paired sacral arteries (lSa-3Sa) arise from the median sacral artery (Ma). The exact origin of the sixth pair of lumbar arteries is clearly visible in lateral position of the specimen only. Bifurcation of the aorta (A) into the common iliac arteries (Cia) at the border between the sixth lumbar (L6) and the first sacral (S 1) vertebral bodies. Ileolumbar arteries (la).
specimens. Characteristically, a significant tributary to the cord was never found originating from such a 'rudimentary' subcostal artery. Of the 6 pairs of lumbar arteries, the upper five arose from the dorsal aspect of the aorta while the sixth pair came from the median sacral artery (Figs 9, 10). The spinal branch of the latter passed through the foramen between the sixth lumbar and the first sacral vertebrae. Only the upper 2 or 3,"o'pairs of the lumbar arteries contributed to the supply of the spinal cord (TVETEN 1976 b). The other root arteries of the lumbo-sacral region terminated mainly on the nerve roots and the dorsal root ganglia. However, in the lumbo-sacral region a number of dorsal root arteries created evident anastomoses with central branches of the ventral spinal artery (described in more detail in another report, TVETEN 1976 b). The median sacral artery originated from dorsal aspect of the terminal part of the aorta at the level of the fifth or the sixth lumbar vertebra and extended into the tail
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Fig. 11. Transparent specimen, photography. Dorsal view of the lumbar region with intact spinal cord in a decalcified specimen. Tiny extraspinal connections between adjacent lumbar arteries (-+).
(Fig. 10). It gave rise to segmental arteries which distributed spinal branches to the sacral region. The ileolumbar arteries in the rat were constant branches of the lumbar aorta, though the origin varied somewhat on the two sides (Fig. 10). However, no evident spinal branch was ever observed originating from these arteries. At each level of the thoracic, lumbar and sacral regions tiny branches from the segmental arteries interconnected inside as well as outside the vertebral canal in a manner similar to that in man (F'g. 11). As in man evident anastomoses were found between the aortic segmental arteries and the internal mammary artery, and between the inferior and the superior epigastric arteries, respectively. Discussion
The anatomic arrangement of the main sources of spinal cord arteries in the rat resembles that in man. However, important differences exist. Thus, in the rat the vertebral artery appears to be the sole source of blood supply to the cervical cord. Contrary to the situation in man, no additional branches from other arteries in the neck enter the intervertebral foraminae of the cervical region in the rat. A high incidence of variations of the vertebral artery existed in the rat; some of
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these also being similar to those observed in man, such as different width of the two arteries, hypoplasia and abnormal origin or site of entrance into the cervical spine. The major abnormality, however, which does not seem to have been previously described in man or in experimental animals was a segmental defect or displacement of parts of the vertebral artery. This peculiar anomaly can be explained from developmental features of the brachiocephalic arteries in rats. MOFFAT (1957, 1961) states that the vertebral artery is formed by fusion of longitudinal anastomoses between the postcostal branches of the primitive intersegmental arteries. Evidently, when such anastomoses fail to develop, a defect involving one or more segments of the artery will ensue. The superior intercostal artery of the costocervical trunk is more prominent in the rat than in man, though GREENE believes that in the rat this artery supplies only the upper three intercostal spaces, and on the left side frequently the first and the second spaces only. She also believes that separate origins of the ventral and dorsal branches of the left third and the fourth intercostal artery occur in about two thirds of the specimens. The dorsal branch is then supplied by the aorta, the ventral one by the superior intercostal artery. Such variations were less frequently observed in the present material and in the vast majority of the rats the superior intercostal artery distributed a series of regular branches to the upper three intercostal spaces on the left side and the upper Iour on the right side. This is important to consider because of the paucity of significant spinal tributaries to the upper thoracic cord, described in closer detail in another report (TVETEN 1976 b). The poor supply of spinal feeders to the upper three or four thoracic segments of the cord in individual cases was closely related to the regional distribution of the superior intercostal artery. Thus, with regard to the spinal cord circulation in rats, the costocervical trunk seems merely to serve as an anastomotic link between the vertebral artery above and the aortic intercostals below by way of intra- as well as extraspinal connections between these arteries. In accordance with the arrangement of the superior intercostal artery and the fact that the rat possesses thirteen thoracic vertebrae, the most common number of the aortic intercostal arteries is nine on the left side and eight on the right side. In the rat two aortic intercostals arising from a common stem was a rare finding, contrary to the situation in man. The origin of the subcostal branches in the rat, similar to the condition in man, frequently varied. The high incidence of a rudimentary or hypoplastic aortic subcostal artery was remarkable considering the frequent occurrence of important spinal cord tributaries (the great ventral radicular artery, or Adamkiewicz' artery) arising from the subcostal space of the rat (TVETEN 1976 b). It was found, however, that an aortic subcostal artery with no ventral branch rarely gave rise to spinal cord tributaries, a feature probably reflecting a natural protective means (TVETEN 1976 a). GREENE described five pairs of lumbar segmental arteries in the rat, the upper four arising from the dorsal aspect of the aorta while the fifth pair branched off from the 12 - 765845
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median sacral artery. Moreover, this author claimed that the ileolumbar arteries not infrequently arise from the common iliac arteries and supply spinal branches to the intervertebral foramen between the last lumbar and the first sacral vertebrae. BRAITHWAITE (1954) in a schematic drawing also depicted only five lumbar segmental arteries although segmental branches from the median sacral artery entering the vertebral canal between the sixth lumbar and the first sacral vertebrae are clearly visible in his angiographic illustrations. In the present material the ileolumbar arteries were constant branches of the lumbar aorta and contrary to those in man, they never supplied significant branches to the spinal canal. As in man, the segmental branches of the vertebro-subclavian arteries and the aorta in the rat interconnected profusely along the entire length of the vertebral column, both inside and outside the spinal canal, forming transverse and longitudinal anastomotic chains. In addition, extensive anastomoses similar to those observed in man occur between the aortic segmental branches and the large arteries on the antero-lateral body-wall such as the internal mammary artery, the superior and inferior epigastric arteries.
SUMMARY The arrangement of extravertebral sources of spinal cord arteries in the rat is similar to that in man. Some differences, however, do exist, concerning mainly the arrangement of spinal branches supplied by the subclavian-vertebral arteries. Contrary to the situation in man, the vertebral artery in the rat appears to be the sole source of blood supply to the cervical cord. A high incidence of variations or anomalies of the vertebral artery in the rat existed. Vascular variations in the upper left thoracic spaces were frequent in the rat and more complicated than in man. In both species, a poor supply of significant spinal cord feeders from the superior intercostal artery of the costocervical trunk was found. Variations in the origin and branching of the aortic segmental arteries occur in both species. In man the major variation consists of two or more intercostal arteries arising from a common stem, while the rat more often displays a rudimentary subcostal artery. Finally, the ileolumbar arteries in the rat are constant branches of the lumbar aorta. Despite these differences in the vascular anatomy, the rat seems to be well suited for experimental comparative investigations, not feasible in man.
ZUSAMMENFASSUNG Die Anordnung der extravertebralen Versorgungen der Arterien der Wirbelsaule bei der Ratte ist der dem Menschen ahnlich, Einige Unterschiede betreffen hauptsachlich den Aufbau der Spinalaste, die durch die A. subclavia-A, vertebral is versorgt werden. Im Gegensatz zur Situation beim Menschen scheint die Vertebralarterie bei der Ratte die einzige Blutversorgungsquelle der Wirbelsaule zu sein. Es besteht bei der Ratte eine hohe Frequenz von Variationen oder Anomalien der Vertebralarterie. Vaskulare Variationen in den oberen linken Thoraxabschnitten waren bei der Ratte haufiger komplizierter als beim Menschen. Bei beiden Spezies fand sich eine geringfiigige Versorgung signifikanter Wirbelsaulen Aste von der oberen lnterkostal-Arterie des costo-cervikalen Stamms. Variationen im Ursprung und der Verzweigung der Aorta-Segment-Arterien fand sich bei beiden Spezies.
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Beim Menschen besteht die wesentliche Abweichung in zwei oder mehr Intercostal-Arterien, die von einem gemeinsamen Stamm ausgehen, wahrend die Ratte haufiger eine rudimentaren subcostale Arterie aufweist. Schliesslich sind die ileo-lumbal Arterien bei der Ratte konstante Aste der lumbalen Aorta. Trotz dieser Unterschiede in der vaskularen Anatomie scheint die Ratte gut geeignet fur vergleichende experimentelle Untersuchungen zu sein, die beim Menschen nicht vorgenommen werden konnen.
RESUME La disposition des sources extra vertebrales des arteres de la moelle chez Ie rat est semblable
a celIe de l'homme. Cependant certaines differences existent, concernant surtout la disposition des branches spinales fournies par les arteres sous-clavieres-vertebrales, A la difference de ce qui se passe chez l'homme, l'artere vertebrale du rat parait etre la seule source d'irrigation sanguine de la moelle cervicale. II y a de nombreuses variations ou anomalies de l'artere vertebrale chez le rat. Les variations vasculaires des espaces thoraciques superieurs gauches sont frequentes chez le rat et plus compliquees que chez l'homme. Dans ces deux especes, l'auteur a trouve une faible irrigation d'importants vaisseaux nourriciers de la moelle provenant de l'artere intercostale superieure du tronc costocervical. Des variations de l'origine et de la ramification des arteres segmentaires arterielles se produisent dans ces 2 especes. Chez l'homme la variation principale consiste dans l'origine par un tronc commun de 2 ou plusieurs arteres intercostales alors que le rat a plus souvent une artere sous-costale rudimentaire. Enfin, les arteres ilio-Iombaires du rat sont des branches constantes de l'aorte lombaire. Malgre ces differences dans l'anatomie vasculaire, Ie rat parait convenir pour des recherches experimentales comparatives qui ne peuvent pas etre faites chez l'homme.
REFERENCES BRAITHWAITE J. L.: The morphology of the collateral circulation following complete interruption of the abdominal aorta in the rat. J. Anat. (Lond.) 88 (1954), 204. CAMMERMEYER J.: Differences in shape and size of neuroglial nuclei in the spinal cord due to individual regional and technical variations. Acta anat. 40 (1960), 149. GREENE E. c.: Anatomy of the rat. Hafner Publishing Co., New York 1959. MOFFAT D. B.: The development of the hindbrain arteries in the rat. J. Anat. (Lond.) 91 (1957), 25. - The development of the anterior cerebral artery and its related vessels in the rat. Amer. J. Anat. 108 (1961), 17. TVETEN L. (a): Spinal cord vascularity. I. Extraspinal sources of spinal cord arteries in man. Acta radiol. Diagnosis 17 (1976), 1. - (b): Spinal cord vascularity. IV. The spinal cord arteries in the rat. To be published in Acta radiol. Diagnosis 17 (1976).
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