A COMPARATIVE STUDY of the AZYGOS VENOUS SYSTEM in MAN, MONKEY, DOG, CAT, RAT and RABBIT by DAVID BOWSHER Department of Anatomy, University of Liverpool
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[ 400 ] A COMPARATIVE STUDY OF THE AZYGOS VENOUS SYSTEM IN MAN, MONKEY, DOG, CAT, RAT AND RABBIT BY DAVID BOWSHER Department of Anatomy, University of Liverpool It has been generally considered that the azygos vein acts as a by-pass between the inferior and superior caval systems, and most research has centred on the con- nexions of its caudal end. In view of the correlation between changes in the pressures of the azygos vein and the cerebrospinal fluid, it was decided to investigate the functional value of the azygos venous system, and the importance of its connexions with the internal vertebral venous system. HISTORICAL INTRODUCTION The azygos vein has excited interest since the earliest days of anatomical study, and is mentioned in the third century by Galen (ed. 1822). Vesalius (1555) wrote of it at some length, and alluded to its connexion with the internal vertebral veins and inferior vena cava. Eustachius (1722) shows, without comment, the hemiazygos arising from the left renal vein. Winslow (1776) gives a fairly accurate description of the vein, together with the branches draining the spinal canal into the intercostal veins. The definitive anatomy of the spinal (internal vertebral) veins and their con- nexions was established by the Paris school in the first half of the nineteenth century, and undoubtedly the most important of these writers was Breschet (1829). He pointed out that a large vein emerges from each thoracic intervertebral foramen and ascends over the body of the vertebra to join the azygos or hemiazygos vein, having first joined forces with the posterior intercostal vein; and that this 'vein of the intervertebral foramen' is larger than the intercostal vein which overlies it. The description of the azygos and internal vertebral venous systems in the text- book of Poirier & Charpy (1902) is based mainly on the work of Breschet (1829) and of Walther (1885). These authors, and Breschet independently of them, state that there are no valves in the internal vertebral veins or in the azygos or hemiazygos, except that there is sometimes an incompetent valve in the arch of the azygos. It should be mentioned, however, that there is a valve in the posterior intercostal vein just before it joins the vein of the intervertebral foramen. Research has centred mainly upon the tenuous connexions of the caudal end of the azygos system, starting with Lejars's description of the 'canal reno-azygo- lombaire' (1888) said to be present in 80 % of cases. Seib (1934) dissected 100 white and 100 negro cadavers and classified the inferior caval and renal origins of the azygos and hemiazygos veins. Analysis of his tables shows that in 83 % of cases the azygos is connected with the inferior vena cava or the left renal vein. Comparative study of the azygos venous system 401 The azygos system has also been studied by authors whose main interest was in the collateral circulation following obstruction of the inferior vena cava. Among the more important of these are Sappey & Dumontpallier (1861), Pleasants (1911) and Batson (1940). Recently, Robinson (1949) ha§ studied the collateral circulation in stillborn foetuses after ligation of the inferior vena cava, and has indicated the connexions between the azygos and internal vertebral systems. Coman & de Long (1951) have made vinilyte corrosion preparations in the rat showing the normal anastomoses between the azygos and internal vertebral systems. Herlihy (1948) has studied the internal vertebral venous plexus of the cat, demonstrating the topography and mentioning its connexions with the azygos venous system, to which he also refers in an earlier publication (1947). Much of the literature on the internal vertebral venous system has been reviewed by Harris (1941). MATERIAL AND METHODS The material consisted of four full-term stillborn (but otherwise normal) human foetuses, three macaque (Macaca mulatta) monkeys, three dogs, two cats, twenty albino rats, and six rabbits. All the material except the human was adult. In all cases the azygos vein was injected retrogradely with either 20% bismuth oxy- chloride ('Chlorbismol') or a dispersion of barium sulphate ('Micropaque'), pre- paratory to radiography and dissection. Four of the rats underwent operative ligature of the vena azygos at its junction with the superior vena cava. In the operative technique, positive pressure anaesthesia was provided by a modi- fication of the method of Porter & Small (1947), details of which will be published elsewhere. The rat azygos is left-sided (see Beddard, 1907), so a lateral thoracotomy was performed in the third left intercostal space and the third rib resected. A ligature was passed under the azygos vein at its point of entry into the superior vena cava, immediately medial to the arch of the aorta, and the vein tied off. The chest was then closed in layers without drainage. These rats were killed and injected at intervals between 10 days and 1 month after operation. Once the anaesthetic and operative technique had been perfected, the mortality was nil. In the earlier cases of the series, the animals were heparinized before being killed, in order to facilitate the flow of the injection material; but experience showed that, provided the injection was made immediately after death, this made no difference. In all cases of retrograde injection of the azygos vein, the following ligations were made before injection: (i) Inferior vena vava, cephalic to the renal veins, but below the liver. (ii) Inferior vena cava, between the diaphragm and heart. (iii) Both renal pedicles at the hilum. (iv) Both lung roots. (v) Inferior vena cava at its point of formation from the common iliac veins. The liver, gut and both lungs were removed before injection, and the abdominal vena cava between the two lower ligatures was removed after injection. In a few specimens (e.g. cat, PI. 3, figs. 7, 8), towards the end of the injection, the injection mass burst through into the surrounding connective tissue between the layers of the mediastinal pleura, but this did not affect the radiographic pattern. 402 David Bowsher RESULTS In all the species studied, the azygos and hemiazygos veins were well filled with injection mass. The degree of filling of the posterior intercostal veins was variable, depending upon the force of the injection and the competence of their valves. In the cases in which they did fill, it could be observed by direct vision that they were the last vessels to be filled, and injection was immediately stopped if and when the veins filled. In the human foetuses (P1. 2, figs. 3, 4) the intercostal veins were never in any case filled. This is testimonial to the statement of Poirier & Charpy (1902) that venous valves are more competent in infancy. Also in each species can be seen, at least in the thoracic region, in dorso-ventral views, the 'vein of the intervertebral foramen' joining the posterior intercostal vein just prior to its termination. In most cases it can be seen that this vessel is larger than the posterior intercostal vein prior to this union. Three other features of importance were noted in all species. First, in no case, save in the monkey, was any segment of the inferior vena cava filled by the injection mass. Even in the monkey, this was probably due to the fact that the left renal vein had been ligated lateral to its suprarenal tributary. Secondly, in all species (though not all specimens examined), the left suprarenal gland was outlined not through the suprareno-renal vein, but by a vessel which issues from the first lumbar intervertebral foramen and joins the plexus of vessels issuing from the gland. Lastly, in all species some or all of the torn ends of the lumbar veins were filled. In the Primates and Carnivora examined the internal vertebral venous plexus was constantly filled. In the four species studied, the main vessels seen are two lateral longitudinal trunks, whose position in relation to the vertebral bodies can be estimated by comparison of dorso-ventral and lateral radiographs. Dissection showed that they lay in the vertebral canal, outside the dura mater in the epidural fat. They received a large number of tributaries which emerge from the dura in company with the nerve roots. Certain differences in these veins between the Primates and Carnivora can be observed. Thus, in the Primates (Pls. 1, 2, figs. 1-4) there are a large number of cross-connexions between these two lateral longitudinal trunks, and the communications with the intradural vessels appear to be much richer than in the case of the Carnivora. In the cat (PI. 3, figs. 7, 8) there are no cross-connexions between the lateral longitudinal trunks; this confirms the observa- tions of Herlihy (1948). In the dog, the cross-connexions are very sparse (PI. 2, figs. 5, 6). In the Primates, the internal vertebral venous plexus connects at its lower end with the anterior sacral plexus (P1. 1, fig. 1; PI. 2, fig. 3), which lies on the anterior aspect of the bodies of the sacral vertebrae; this plexus is not apparent in the Carnivora. Inspection of the lateral radiographs (P1. 1, fig. 2; P1. 2, fig. 5; PI. 3, fig. 8) shows the lateral longitudinal trunks to be greater in diameter than the vena azygos itself. It should also be noted here that man is the only species examined which appears to possess ascending lumbar veins. In the normal rodent (P1. 4, figs. 9, 10) the lower end of the azygos venous system terminates at the level of the left suprarenal vein; and although the connexions of Comparative study of the azygos venous system 403 the azygos and hemiazygos veins with the veins of the intervertebral foramina in the thoracic region are apparent, the internal vertebral venous plexus is not filled.