The development of the bronchial veins with special reference to anomalies of the pulmonary veins.код для вставкиСкачать
The Development of the Bronchial Veins, with Special Reference to Anomalies of the Pulmonary Veins RALPH F. SHANER Department of Anatomy, University of Alberta, Edmonton, Alberta, Canada This communication reports a restudy of the venous drainage of the lungs and bronchi, aimed to match the greatly increased knowledge of anomalies of the pulmonary veins brought about by modern thoracic surgery. Nearly all workers on pulmonary vein anomalies have depended upon the early work of Brown (’13) and have manipulated his schema to explain the anomaly they are concerned with. For this purpose Brown’s schema is inadequate; it lacks important additions found in older embryos, and especially the venae .cornitantes of the vagus nerves. Butler (’50, ’52a, b ) has recently emphasized the significance of these vessels in the development of pulmonary drainage. Neither worker, however, says anything about the development of the bronchial veins, vessels which must be involved in some of the graver pulmonary vein abnormalities. My work is an extension of Butler’s careful study, using the same methods. I first studied the veins of 60 pig embryos ranging in length from 9 to 70 mm. The veins of each embryo were injected with drawing ink through a no. 28 cannula into the primary vein of the head, or into the heart, or into the mesonephros. Each embryo was fixed in fonnalin and cut into serial sections. Its veins could then be reconstructed by the graphic method. Next, I made a similar study of a corresponding group of human embryos. These could not be injected. However, if one chooses embryos with veins dilated with blood, it is possible to follow the vessels already found in the pig, and to reconstruct them graphically. With the results of the two parallel studies before me, I surveyed the chief recorded anomalies of the pulmonary veins in an attempt to make them more understandable. Normal development in the pig One may start with the schema of Brown (’13), reproduced here as figure 1. It is a reconstruction of the vessels of a 4.5-mm cat embryo. At this stage the foregut is undivided and the lung buds faintly indicated. All are enclosed in a tight fitting splanchnic plexus. The plexus is drained laterally through several taps into the cardinal veins, and ventrally into the heart by the primitive pulmonary vein and a second caudal tap. Each component of Brown’s schema: the splanchnic plexus, the cardinal vein taps, the pulmonary vein, and the caudal tap-can be identified in a 12-mm pig embryo, whose veins are graphically reconstructed in figures 2 to 5. A portion of the splanchnic plexus of the 12-mm pig embryo is shown separately in figure 3. As compared to Brown’s earlier schema, the pig’s plexus has been modified by the division of the foregut into trachea and esophagus, and still more by the growth of the vagus nerves. The plexus around the esophagus and trachea remains plexiform, but the lateral part of the plexus around the vagus nerve and its recurrent branch has been made over into venae comitantes. The full extent of these venae comitantes is shown in figure 2; they can be traced more or less continuously down to the stomach. The second feature of Brown’s schema, the venous taps into the cardinal veins, also appears in the 12-mm pig. The taps arise, not from the general splanchnic plexus but from the venae comitantes of the vagus nerves (fig. 2). The number of taps vanes from embryo to embryo, but the taps that face the origins of the recurrent vagi are invariably the largest and most 159 160 RALPH F. SHANER constant. Their constancy and size foreshadows their later significance as origins of the bronchial veins. The third feature of Brown's schema, the primitive pulmonary vein, drains the growing lung buds of the 12-mm pig (figs. 2 and 4). The lung buds are clothed with a portion of the early splanchnic pIexus (fig. 4) with which the terminal branches of the pulmonary vein interosculate. In addition, the primitive pulmonary vein receives a constant branch that descends along the esophagus to join the vena comitans of the left vagus (fig. 2). This is the caudal tap of Brown's schema and the vitello-umbilical tap of Butler ('52a). A better name would be esophageal tap. The esophageal tap communicates through the left vagus vein with the gastric plexus, which in turn communicates with the duc- TUDUCTUSVENO LEVEL flG.5. 3 Fig. 1 Schema of venous drainage of foregut of a 4.5-mm cat embryo. After Brown ('13). X 65. Fig. 2 Graphic reconsbction of the veins of a 12-mm pig embryo. Splanchnic plexus omitted. X 25. Fig. 3 Schema of the splanchnic plexus of a 12-mm pig embryo. Fig. 4 Section through the lung buds of a 12-mm pig embryo. X 25. Fig. 5 Section through the stomach and liver of a 12-mm pig embryo. x 25. DEVELOPMENT OF BRONCHIAL VEINS tus venosus (figs. 2 and 5). This collateral pathway has potential significance. Of the later development of the main pulmonary vein nothing can be added to the usual text-book description. I will deal henceforth with the venae comitantes of the vagi and their recurrent branches, the 161 cardinal taps, and their bronchial derivatives. The venae comitantes of the vagus nerves of a 22.5-mm pig embryo are reconstructed in figure 6. Well injected veins parallel the recurrent vagi, and follow the main vagi as far as the stomach. Fig. 6 Graphic reconstruction of the veins of a 22.5-mm pig embryo. x 8. Fig. 7 Graphic reconstruction of the veins of a 37-mm pig embryo. x 13. Fig. 8 Graphic reconstruction of the veins of a 15-mm human embryo. x 25. Fig. 9 Graphic reconstruction of the veins of a 29-mm human embryo. x 12. 162 RALPH F. SHANER Both nerves and veins have been affected by the downward shift of the heart and great arteries. The cardinal taps draining the vagus veins are mostly restricted to a narrow zone below the origin of the recurrent nerves. As before, the taps that follow the hook of each recurrent vagus are far better developed than the rest and form the chief outlets of the venae comitantes of the recurrent vagi. At the same time the cardinal veins are undergoing their complex metamorphosis. The azygos and hemiazygos veins have formed along the sympathetic trunks; they drain into the terminations of the posterior cardinal veins. The terminations of the azygos and hemiazygos veins into the cardinal system lie opposite the recurrent vagus taps. The 37-mm pig embryo (fig. 7) is characterized by the appearance of the bronchial veins and a general breakup of the cardinal system of veins. The left bronchial vein appears as a leash of small veins that arise from the termination of the left recurrent vagusi vein. The leash uses the part of the recurrent vagus vein that hooks beneath the ductus arteriosus to enter the posterior cardinal vein. The right bronchial vein appears as a similar leash of vessels from the right vagus vein. This leash uses a cardinal tap to enter the termination of the azygos vein. The bronchial veins are, therefore, outgrowths from the venae comitantes of the vagus nerves. The human anatomist, expecting the left bronchial vein to enter the hemiazygos and the right bronchial to end in the azygos, may be confused by the pig’s arrangement. The pig’s arrangement is really the same as in man, only it is masked by a different development of the azygos and hemiazygos veins. In the pig the hemiazygos is the larger vein (Reagan, ’19); it uses the end of the left posterior cardinal to enter the coronary sinus, and retains this outlet in the adult. Hence the left bronchial of the pig seems to enter the coronary sinus. On the right side the pig’s azygos disappears save for a terminal fragment, which persists as the cervico-thoracic vein of Reagan. The pig’s right bronchial drains into this termi- nal part of the azygos-just as the right bronchial vein does in man. Normal development in man After one has followed the injected veins o i pig embryos, one can trace similar vessels in human embryos, provided the vessels are well dilated with blood. The veins of a 15-mm human embryo (fig. 8) are a fair copy of those of a 12mm pig (fig. 2). A well defined vena comitans follows each recurrent vagus nerve and the main vagus nerve below. Each vein drains through several taps into the cardinal veins. The largest taps face the origin of the recurrent nerves. The pulmonary vein is a short vessel, with a well developed esophageal branch which mingles caudally with the vessels around the vagi and esophagus. Farther caudad a fragment of the gastric plexus can be traced; it has connections across the lesser omentum with the ductus venosus. The human bronchial veins appear in a 29-mm embryo (fig. 9). The left bronchial arises as a leash of vessels from the left recurrent vagus vein, where the latter hooks beneath the ductus arteriosus. In man, as in the pig, the left bronchid vein uses the recurrent vein tap to drain into the cardinal system. In man, however, the left cardinal system is broken into a lower fragment which becomes the coronary sinus, and an upper remnant that connects the accessory hemiazygos to the left innominate. Through the upper remnant the left bronchial vein enters the accessory hemiazygos. The sight bronchial vein of man is somewhat irregular. The human right recurrent vagus vein is too high up in the chest to serve as an origin for a bronchial vein. Some lower cardinal taps or other adventitious veins drain the bronchi into the arch of the azygos. The right bronchial vein resembles the renal veins, which are also formed in a haphazard fashion from 16cal adventitious vessels. I add figure 10, a reconstruction of a 50-mm abnormal human embryo, because it confirms the preceding embryo and suggests some normal variations of the bronchial vessels. This 50-mm embryo has a blind coronary sinus, which drains backward into a persisting left common car- DEVELOPMENT O F BRONCHIAL VEINS 163 plexus by a bronchial vein. The development of the bronchial veins enables one to explain some of the aberrant pulmonary venous patterns. According to 4 recent studies (Healey, ’52; Parson et al., ‘52; Keith et al., ’54; and Darling et al., ’57) total bilateral abnormal pulmonary drainage is more often diverted into a persisting left superior vena cava and the coronary sinus. Partial anomalous drainage, on the other hand, is found more commonly on the right side. Now the left bronchial vein is established quite early and is preserved intact. It is SUMMARY in an ideal position to capture the entire Zuckerhandl (1884) long ago demon- pulmonary plexus. The right bronchial strated the surprising number of routes vein is a more haphazard vessel, and by which blood may be returned from the would be unable to capture more than lungs and bronchi in the adult. From the the adjacent parts of the pulmonary standpoint of the embryo these can be plexus. summarized by a diagram (fig. 11). The According to Hickie et al. (‘56): “Anomproblem set is the drainage of a plexus alous veins from the right lung often occovering the bronchi and lungs. The cur without associated anomalous veins plexus around the lungs proliferates enor- from the left lung, but the reverse is unmously; it is drained by the pulmonary usual and left-sided anomalous pulmonary vein into the left atrium. The early pul- veins generally occur with complete transmonary vein is for a time connected by position of all pulmonary veins and an an esophageal tap with the gastric plexus atrial septal defect.” Such graver disorders and through it with the liver. The lesser must begin early in embryonic life and plexus around the bronchi, on the other would be more likely to involve the early hand, are drained by more circuitous well established left bronchial vein. routes made up of the venae comitantes There is in addition another kind of of the vagus nerves, the taps from the anomalous drainage of the pulmonary cardinal veins, and the body veins. veins which does not involve the bronchial The pattern of the left bronchial vein vessels. About a dozen cases are known is laid down early and is preserved. It where the lungs drain through a vein that begins with a leash of vessels from the descends through the esophageal hiatus left recurrent vagus vein, which uses that of the diaphram, follows the left vagus vein and its cardinal tap to enter the left nerve and lesser curvature of the stomach common cardinal vein. When the cardi- and ends in the ductus venosus or portal nal system breaks up, the left bronchial vein. Details of this anomaly are often enters the accessory hemiazygos, or the vague, but the accounts of Druepple (’57), left innominate. Should the left common Edwards and DuShane (’50) and Butler cardinal be preserved as a left superior (’52b) are explicit enough. Such an abvena cava, the left bronchial drains into dominal pulmonary vein is a combination the coronary sinus. The right bronchial of several normal embryonic vessels shown vein uses some of the lower cardinal taps in figure 11. The first part is a persisting to enter the azygos vein. The right bron- early common pulmonary vein. The secchial vein is more haphazard in its consti- ond part is its esophageal branch. The tution and course. third part is a fragment of the left vagus vein and the gastric plexus. The outlet is Anomalous drainage o f t h e lungs a communication of the gastric plexus It has long been thought that many ab- with the ductus venosus. This outlet is normal pulmonary veins are the result of near the outlet of the portal and may shift a capture of all or parts of the pulmonary to it. dinal vein. A retroesophageal right subclavian artery is also present. The bronchial veins of both sides run as in the previous embryo. But, where the left bronchial ends, the common cardinal is degenerating into a swamp. The left bronchial vein could end in the hemiazygos, or move upward to the left innominatea common variation. Or it could empty downward into a persisting left superior vena cava and the coronary sinus. The right bronchial vein again shows its haphazard origin from adventitious vessels. 164 RALPH F. SHANER The ending of all pulmonary veins in the coronary sinus, without the mediation of a persisting left superior vena cava, has caused much discussion. In the well known case of Brody ('42) 4 separate veins enter an enlarged coronary sinus. The best explanation seems to be that of Auer ('48). Auer found in very young human embryos a second pulmonary vein orifice just caudal to the standard one. The second vein enters the area of the future coronary sinus. He thought the second tap might supplant the usual one and lead the pulmonary veins into the coronary sinus. I have seen Auer's accessory pulmonary outlet in a 4.7-mm human embryo; it is apparently a constant vessel. What seems to be a later stage of the same vessel turned up in an 18-rnrn pig embryo with an abnormal heart. A section through this heart (fig. 12) shows the early common RY LEFT ATRIUM Fig. 10 Graphic reconstruction of the veins of an abnormal 50-mm human embryo, with occluded coronary sinus and retroesophageal left subclavian artery. x 12. Fig. 11 Schema of the venous drainage of the bronchi and lungs in the human embryo. Fig. 12 Section from an abnormal 18-mm pig embryo heart. Pulmonary vein is transferred from its normal inlet to an accessory one into the coronary sinus. x 12. Fig. 13 Section from an abnormal 23-mm pig embryo heart. Pulmonary vein opens into right atrium. x 12. DEVELOPMENT OF BRONCHIAL VEINS pulmonary vein bypassing its normal outlet to enter the adjacent coronary sinus. With the subsequent absorption of the common stem, the 4 separate veins could enter the coronary sinus. The diversion of all the pulmonary veins into the right atrium is a more complex affair, involving heart anomalies. The early common pulmonary vein enters the common atrium just above the atrio-ventricular canal. When the atrial septum I descends, it just grazes the right side of the pulmonary o s c e (Davies and MacConaill, '37). It would seem a matter of chance into which atrium the vessel would go. In the rare case of Graham ('44) in which a common pulmonary vein enters the right atrium, the vein must have been diverted into the right atrium by a slight shift of the pulmonary orifice or of the descending atrial septum I. Figure 13 is a section through the heart of a 23-mm abnormal pig embryo that duplicates Graham's anomaly. The common pulmonary vein enters the right atrium about 6 sections above the free edge of atrial septum I. GENERAL SUMMARY The normal development of the pulmonary and bronchial veins is followed by means of injected pig embryos and corresponding stages of human ones. The early pulmonary vein has a constant esophageal branch which communicates through the gastric plexus with the ductus venosus. The bronchial veins are derived from the venae comitantes of the vagus nerves and their cardinal vein taps. The left vein is a constant derivative of the left recurrent vagus vein. The right bronchial is a more haphazard branch of some other cardinal vein tap. The normal findings are used to explain the nature and frequency of abnormal forms of pulmonary drainage, some of which are also illustrated by abnormal embryonic cases. ACKNOWLEDGMENTS This paper is a report of work done while the author held a Research Fellowship of the National Heart Foundation of Canada. The cost of technical assistance 165 was met by the Alberta Heart Foundation. For material the author is indebted to Swift Canadian Company. To all the author gives his thanks. LITERATURE CITED Auer, J. 1948 The development of the human pulmonary vein and its major variations. Anat. Rec., 101: 581-584. Brody, H. 1942 Drainage of the pulmonary veins into the right side of the heart. Arch. Path., 33: 221-240. Brown, A. J. 1913 The development of the pulmonary vein in the domestic cat. Anat. Rec., 7: 299-329. Butler, H. 1950 The development of the azygos veins in the albino rat. J. Anat., 84: 83-94. 1952a Some derivatives of the foregut venous plexus of the albino rat, with reference to man. Ibid., 86: 95-109. 1952b An abnormal disposition of the pulmonary veins. Thorax, 7: 249-254. Darling, R. C., W. B. Rothney and J. M. Craig 1957 Total pulmonary venous drainage into the right side of the heart: report of 17 autopsied cases not associated with other major cardiovascular anomalies, Lab. Invest., 6: 4464. Davies, F., and M. A. MacConaill 1937 Cor biloculare, with a note on the development of the pulmonary veins. J. Anat., 71: 437-446. Druepple, L. G. 1957 Complete pulmonary venous drainage into the portal vein with multiple congenital anomalies. Am. Heart J., 53: 790-794. Edwards, J. E., and J. W. DuShane 1950 Thoracic venous anomalies. Arch. Path., 49: 517537. Gilman, R. A., C. A. Skowron, B. G. Musser and C. P. Bailey 1957 Partial anomalous venous drainage. Am. J. Surg., 94: 688-694. Graham, P. M. 1944 A rare congenital abnormality of the pulmonary veins and heart. Med. J. Austr., 2: 545-546. Healey, J. E. 1952 An anatomical survey of anomalous pulmonary veins : Their clinical significance. J. Thorac. Surg., 23: 433-444. Hickie, J. B., T. M. D. Gimlette and A. P. Bacon 1956 Anomalous pulmonary venous drainage. Brit. Heart J., 18: 365-377. Keith, J. D., R. D. Rowe, P. Vlad and J. H. O'Hanley 1954 Complete anomalous p b o nary drainage. Am. J. Med., 16: 23-38. Parsons, H. G., A. Purdy and B. Jessup 1952 Anomalies of the pulmonary veins and their surgical significance. Pediatrics, 9: 152-166. Reagan, F. P. 1919 On the later development of the azygos veins of swine. Anat. Rec., 17: 111-125. Zuckerhandl, E. 1884 Vber die Anastomosen der Venae pulmonales mit den Bronchialvenen und mit dem mediastinalen Venennetze. Wien, Sitzungsb. d.k. Akad. d. W. math. naturw. Classe, 84: 110-152.