Okajimas Folia Anat. Jpn., 71(1): 13-20, May, 1994

Venous Drainage of the Thoracic Esophagus Toward the Pulmonary Vein

By

Gen MURAKAMI, Norihiko ADACHI, Iwao SATO, Tooru SATO and Hajime HOSHI

Department of Anatomy, Nihon University School of Medicine, Tokyo 173, Japan (G. M., N. A., H. H.), Department of Anatomy, Nippon Dental University at Tokyo, Tokyo 102, Japan (I. S., T. S.).

-Received for Publication, February 25, 1994-

Key Words: Esophagus, Veins, Pulmonary veins, Anastomosis, Human anatomy

Summary: Venous drainage of the thoracic esophagus toward the pulmonary vein (PV) was investigated in 52 human specimens in which the veins around the esophagus were clearly observed owing to venous blood retention after injection of 10 L of formol solution into the femoral artery. Below the level of the tracheal bifurcation, 43 cases (right, 21; left, 22) of venous drainage toward the PV were observed in 29 of the 52 specimens examined (55.8%). The direct drainage to the PV was observed mainly on the left side (19 of the 22 cases). In contrast, drainage via the bronchial vein toward the PV existed mainly on the right side (18 of the 21 cases). These drainage routes merged into the tributaries of the inferior PV, such as the inferior or superior basal vein. The draining veins often communicated with the azygos vein system on the right side (10 of the 21 cases). The veins passed through the pulmonary ligament, and also often along the vagus nerve or the bronchial artery. No venous valves were found during the course of direct drainage from the esophagus to the PV. Venous drainage toward the PV was considered to be one of the main drainage routes from the thoracic esophagus.

In anatomy textbooks (Clemente, 1985; Williams cardial sac, 52 cadaveric specimens (40 males and 12 and Warwick, 1980), veins of the thoracic esophagus females), aged 57-87 years, in which the veins are described as tributaries of the azygos vein system. around the esophagus were clearly visible, were It is well known that anastomosis between the eso- obtained from an original total of 105 after injection phageal veins and the portal vein system, i.e. the of about 10 L of 10% formol solution into the femoral portocaval shunt, leads to development of esopha- artery. Clear observation of fine veins was facilitated geal varices in patients with portal hypertension by retention of the venous blood. In these 52 speci- (Hollinshead, 1969; McVay, 1984). Moreover, anas- mens, the esophageal veins were minutely dissected tomosis with other vein systems, including the phar- under naked eye observation from the ventral to the yngeal or the pulmonary vein (PV) systems, has also dorsal aspect of the esophagus after removal of most been pointed out (reviewed by Butler, 1951). of the lung except for the part facing the mediastinum. Konaschko (1929) described a few case in which the Special attention was paid to the Im region of the vein from the thoracic esophagus located immediately esophagus as defined by the Japanese Society for below the tracheal bifurcation joined the bronchial Esophageal Disease (1992), which corresponded to vein and then emptied into the PV. Recently, the region in which Takiguchi et al. (1983) reported Takiguchi et al. (1983) described direct venous drain- direct venous drainage to the PV. Numbers of the age to the PV from the thoracic esophagus. However, veins were counted at their terminal portions even if they considered that such venous drainage was the vein connected with others along its course. anomalous. The aim of this study was to clarify the After gross observation in situ, the vein which drained incidence and courses of the esophageal venous drain- directly into the PV system was removed and its age toward the PV. lumen was opened under a stereomicroscope (10x-20x) in order to examine the venous valves. In addition to these stereomicroscopic observations, Materials and Methods the original portion of the vein was removed along with a fragment of the esophagus for histological After removal of the heart along with the peri- examination of serial sections stained with hemato-

Address correspondence to Dr. Gen Murakami M.D., Ph.D. Department of Anatomy, Nihon University School of Medicine, 30 Ohyaguchi-kamimachi, Itabashi-ku, Tokyo 173, Japan.

13 14 G. Murakami et al . xylin and eosin. described in anatomy textbooks (Clemente, 1985; Williams and Warwick, 1980), were also observed along with direct drainage to the PV. Moreover, the Results esophageal vein draining toward the PV sometimes communicated with the azygos vein system (12 of the 1. Venous drainage of the Im region of the 43 cases), particularly on the right side (10 of 12 esophagus. cases). On the right side, the esophageal vein as well Venous drainage of the esophagus toward the PV as the bronchial vein tended to empty into the azygos was observed in 29 of the 52 specimens examined. In vein system, possibly owing to their location close to these 29 specimens, 43 cases of drainage toward the the terminal portion of the azygos vein. On the left PV were divided into two types, type A and type B. side, in contrast, the descending aorta seemed to The type A esophageal vein (22 cases) emptied prevent the esophageal and bronchial veins from directly into the PV, whereas the type B vein joining large tributaries of the azygos vein. It was (21 cases) joined the bronchial vein and then termin- noted that the venous plexus on the mediastinal ated at the PV (Plate 1, Table 1). However, three pleura also communicated with the esophageal vein other patterns of venous drainage toward the azygos as well as the PV and the azygos vein system (see vein system (a, b, c in Plate 1), which have been Discussion). The nomenclature for the PV system

Table 1. Observations of esophageal venous drainage to the pulmonary vein.

* direct: the vein emptied directly into the pulmonary vein system; via br .v.: the vein joined the bronchial vein and then emptied into the pulmonary vein system. ** IB: (the vein emptied into) the inferior basal vein; SB: superior basal vein; CB: common basal vein; IP: inferior pulmonary vein; V6 or V10: pulmonary vein from the 6th or 10th pulmon- ary segment. *** +AZ: the vein draining toward the pulmonary vein system clearly communicated with the azygos vein system. Venous Drainage of the Esophagus to the Pulmonary Vein 15 used below was based on that of Yamashita (1978). Such venous drainage toward the PV was considered to be one of the main drainage routes from the 2. Direct venous drainage to the PV (Plate 2) thoracic esophagus below the level of the tracheal Twenty-two cases of the type A vein were found bifurcation, in particular the Im region of the esopha- in 17 of the 52 specimens examined. These veins gus defined by the Japanese Society for Esophageal were found mainly on the left side (19 of the total of Disease (1992). 22 cases). The vein merged into the main trunk of Since the PV as well as the esophageal veins are the inferior PV or its large tributaries, particularly thought to develop partly from the foregut venous the inferior basal vein (12 cases, Table 1). Two type plexus (reviewed by Butler, 1952), the esophageal A veins sometimes emptied into the left PV at venous drainage to the PV may also originate from different sites (specimen Nos. 2, 3, 7 and 8). The this plexus. However, the close fascial relationship diameter of the type A veins ranged from 0.5 to between the mediastinal pleura and the adventitia of 2 mm at the terminal portion. The type A veins the esophagusseemed to cause the two venous systems usually originated from the ventral surface or lateral to anastomose with each other, like Retzius' vein edge of the esophagus. The vein sometimes showed connecting the portal vein system to the inferior a long course of more than 10 cm through the caval vein system in the retroperitoneal space pulmonary ligament. Moreover, the vein often (Hollinshead, 1969), even though their developmen- accompanied the vagus nerve (Plate 2), resembling tal processes are different. In fact, the pleural venous the "venae comitantes of the vagus nerve" described plexus communicated with the PV, esophageal vein by Butler (1951). The pulmonary ligament appeared and the azygos vein system. Consequently, we con- to function as a kind of "esophageal mesentery" in sidered that the esophageal venous drainage toward which the veins, arteries and nerves passed longitudi- the PV develops from the anastomosis via the pleural nally along the esophagus and transversely connected venous plexus. it to the lung. Since the esophageal vein was too Viamonte et al. (1989)reported that the bronchial dilated by blood retention to allow clear observation vein arising from the distal part of the bronchial tree of the valves, we were unable to find any valves merges into the PV. However, in the present study, during the extramural course of direct drainage to we often observed the bronchial vein merging into the PV or at the point of exit from the muscle layer the PV without any special relationship to the origin of the esophagus. of the bronchial vein along the bronchial tree. More- over, the bronchial vein draining toward the PV was 3. Venous drainage toward the PV passing via the larger and longer on the right side than on the left, bronchial vein (Plate 3) since the vein frequently communicated with the The type B vein joined the terminal portion of the terminal portion of the azygos vein on the right side bronchial vein and then emptied into the inferior (Plate 3). This long and large bronchial vein on the PV. Twenty-one examples of this were found in right side showed a tendency to receive the type B 18 of the 52 specimens examined, mainly on the right esophageal vein more often than that on the left. side (18 of the 21 cases). On the right side, the type These findings suggest that the difference in the B vein emptied into various tributaries of the inferior bronchial vein causes laterality in the incidence of PV, but the tributaries were smaller than those on types A and B. the left, including the superior basal vein, inferior Anastomosis between the portal and PV systems basal vein, or the vein from the 6th pulmonary has been found along the esophagus, not only in segment. The bronchial vein, irrespective of whether anomalous cases (Butler, 1952) but also in acquired or not it terminated at the PV, tended to be well cases created by a shunt operation for treatment of developed on the right side, possibly because of portal hypertension (Akita, 1977;Blackburn, 1956). communication with the large tributaries of the azygos It seems likely that the venous drainage route from vein. On the left side, however, the bronchial vein the esophagus to the PV is susceptible to develop- was short and thin. The brochial vein which joined ment of porto-pulmonary anastomosis in patients the type B esophageal vein usually accompanied the with portal hypertension. In any event, it is still inferior bronchial artery (designated Type E by Kasai unclear whether the venous drainage of the thoracic and Chiba, 1979 and 1981). esophagus toward the PV plays a role as a route for hematogenous metastasis of esophageal cancer or is involved in the development of porto-pulmonary Discussion blood shunt, as suggested above.

In the present study, venous drainage of the tho- racic esophagus toward the PV was often observed. 16 G. Murakami et al.

Acknowledgement 7) Japanese Society for Esophageal Disease: Guidelines for Clinical and Pathologic Studies on Carcinoma of the Esopha- gus. 8th ed., p. 2-3, 1992. We thank Prof. Noboru Goto and Associate Prof. 8) Kasai T, Chiba S. Macroscopic anatomy of the bronchial Kazuyuki Shimada (Showa University) for their arteries. Anat. Anz., 1979;145:166-181. encouragement during our study. 9) Kasai T, Chiba S. The origin and course of the bronchial arteries. Horosaki Med. J., 1981;33:386-403. 10) Konaschko Pt. Uber das System der Anastomosen, die die Lungenvene und den linken Vorhof mit den venen des References grOen Kreislaufs verbinden. Z. Anat. EntwGesch. 1929:89: 672-695. 1) Akita H. Portopulmonaryshunt operation. Jpn. J. Gastro- 11) McVay CB. Anson & McVay Surgical Anatomy. 6th ed., enterol.Surg., 1977;10:749-755. 630-633, Saunders, Philadelphia, 1984. 2) BlackburnCRB. Acquiredportal-pulmonary venous anas- 12) Takiguchi T, Takahashi M, Sato K, Sato T . Extramural tomosiscomplicating partial oesophago-gastrectomy in a vessels of the esophagus. Jpn. J. Lymphol. 1983;6:38-45 . in patientwith portalhypertension. Thorax, 1956;11:30-35. Japanese 3) Butler H. The veins of the esophagus.Thorax, 1951;6: 13) Viamonte M, Viamonte M Jr., Camacho M, Liebow AA. 276-296. Corrosion cast studies of the bronchial arteries. Surg. Radio!. 4) Butler H. An abnormal disposition of the pulmonaryveins. Anat., 1989;11:215-219. Thorax,1952;7:249-254. 14) Yamashita H. Roentogenologic Anatomy of the Lung. 5) ClementeCD. Anatomyof the Human Body. 30th ed., p. 70-107, Igaku-shoin, Tokyo, 1978. p. 828,Lea & Febiger,Philadelphia, 1985. 15) Williams PL, Warwick R. Gray's Anatomy. 36th ed., 6) HollinsheadWH. Anatomyfor Surgeons.vol. 2, 2nd ed., p. 754-756, Churchill Livingstone, London, 1980. p. 175-177, Hoeber,New York, 1969. Venous Drainage of the Esophagus to the Pulmonary Vein 17

Plate I

Explanation of Figures

Plate I

Schematic representation showing two types of esophageal venous drainage toward the pulmonary vein system. An esophageal vein (black star) merges directly into the inferior pulmonary vein (IP) or into its tributaries in Type A. The usual forms of venous drainage to the azygos vein system (AZ) are also observed as follows: a, drainage to large tributaries of the azygos vein; b, drainage via the bronchial vein; c, drainage via the periaortic plexus. In Type B, the esophageal vein joins the terminal portion of the bronchial vein (arrow) and then empties into the IP. AO, descending aorta; ESO, esophagus; PA, pulmonary artery; SA: superior pulmonary vein; VC, vertebral column. 18 G. Murakami et al.

Plate II

Plate II

Photograph showing the direct venous drainage to the pulmonary vein (Type A), viewed from the ventral side. The esophageal veins (arrows) arise from the ventral surface of the esophagus (ESO), join together, and then empty into the terminal portion of the left inferior pulmonary vein (IP) at the small opening site (arrowhead). The esophageal vein accompanies the vagus nerve (X) in the pulmonary ligament (PL). The stippled line indicates the inferior margin of the left main bronchus. Scale: 1 cm. Venous Drainage of the Esophagus to the Pulmonary Vein 19 Plate III

Plate III

Line drawing showing a case of esophageal venous drainage to the pulmonary vein via the bronchial vein on the right side (Type B), viewed from the ventral side. The right lung (RL), including pulmonary arteries and veins, has been dissected and partly removed in order to demonstrate the terminal portion of the bronchial vein. Several veins (arrows) arise from the esophagus (ESO) and join to form a long vein (arrowheads) along the right vagus nerve (X) and the large bronchial artery (BA). The long vein joins a vein (asterisk) arising from the trachea and then empties into the terminal portion of the azygos vein (AZ) at its upper end. At the lower end (black star), the vein joins the bronchial vein (BV) and terminates at the pulmonary vein (PV; the number shown with PV indicates the draining segment). The bronchial artery (BA), arising from the descending aorta, gives rise to many esophageal arterial branches. Note the numerous fine veins on the mediastinal pleura (open stars) which communicate with the PV as well as the esophageal veins. Black triangle, Arterial branch supplying the visceral pleura; LN, Lymph node of the pulmonary ligament; PA, Pulmonary artery; PL, Pulmonary ligament; BR, Right main bronchus.