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Home , Ascending lumbar vein, Iliolumbar vein, Internal iliac vein, Internal thoracic vein, Lumbar veins, Small cardiac vein

Okaiimas Fol. anat. jap., 48: 413-426, 1972

A Case of the Bilateral Superior With Some Other Anomalous

By

Yasumichi Fujimoto, Hitoshi Okuda and Mihoko Yamamoto

Department of Anatomy, Osaka Dental University, Osaka (Director : Prof. Y. Ohta)

With 8 Figures in 2 Plates and 2 Tables

-Received for Publication, July 24, 1971-

A case of the so-called bilateral superior venae cavae after the persistence of the left has appeared relatively frequent. The present authors would like to make a report on such a persistence of the left superior vena cava, which was found in a routine cadaver of their school. This case is accompanied by other anomalies on the venous system ; a complete pair of the azygos veins, the double subclavian veins of the right side and the ring-formation in the left external iliac .

Findings

Cadaver : Mediiim nourished male (Japanese), about 157 cm in stature. No other anomaly in the as well as in the great is recognized. The extracted heart is about 350 gm in weight and about 380 ml in volume.

A. Bilateral superior venae cavae 1) Right superior vena cava (figs. 1, 2, 4) It measures about 23 mm in width at origin, about 25 mm at the pericardiac end, and about 31 mm at the opening to the right ; about 55 mm in length up to the and about 80 mm to the opening. The vein is formed in the usual way by the union of the right

This report was announced at the forty-sixth meeting of Kinki-district of the Japanese Association of Anatomists, February, 1971,Kyoto. 413 414 Y. Fujimoto,H. Okudaand M. Yamamoto

internal jugular and the two subclavian veins, and passes downward, attached to the right phrenic nerve anterolaterally and the posteromedially, up to the right atrium. It en route receives the following veins :—Into the anterior wall the right internal thoracic (ca. 9 mm in width), the inferior thyroid (ca. 2.3 mm) and the right pericardiacophrenic (ca. 3.8 mm) ; into the medial wall the thymic (two in number, ca. 6 mm and 1.5 mm) ; into the posterior wall the right vertebral (ca. 11 mm) and the right azygos veins (ca. 15.7 mm). 2) Left superior vena cava (figs. 1, 2, 3, 4) It measures about 23 mm in width at the origin, about 25 mm at the pericardiac end, about 32 mm at the opening to the coronary sinus ; about 58 mm in length up to the pericardium and about 118 mm to the sinus. This vessel, formed by the union of the left internal jugular and the subclavian veins, descends, crossing in front of the aortic arch, then pierces the pericardium in front of the left pulmo- nary , and reaches the back of the heart passing between the left auricle and the left upper pulmonary vein. Distal to the piercing, the vessel is attached to the left phrenic nerve anterolaterally and the vagus nerve posteromedially. Then it obliquely passes over the surface of the left atrium and bends along the . It transfers to the coronary sinus receiving the great cardiac vein, and finally continues rightward for the opening into the right atrium. This vessel is the same in width as the right corresponding vessel before piercing the pericardium, then gradually grows larger. It en route gathers the left internal thoracic (ca. 6 mm) and the left pericardiacophrenic (ca. 1.5 mm) into its anterior wall, the Rr. mediastinales (ca. 1.5 mm) into its medial wall, and the left vertebral (ca. 9 mm) and the left azygos veins (ca. 9 mm) into its posterior wall. No anastomotic branch is observed between the right and left superior venae cavae. 3) Coronary sinus (figs. 3, 4) The sinus is the continuation of the left superior vena cava. It becomes dilated in the shape of a wide spindle (ca. 32 mm in width, ca. 40 mm in length). The great cardiac vein (ca. 6 mm in width) ascends in the anterior interventricular sulcus and turns rightward in the coronary sulcus being covered with the left auricle, parallel with the left superior vena cava, then finally enters the sinus at about 36 mm from its right lower end, where the vessel has a bicuspid valve. The (ca. 8 mm) has a monocuspid valve. The posterior veins of the left are fine, four in number. The sinus which receives the above-mentioned branches flows into the right atrium A Case of the Bilateral Superior Venae Cavae 415

in contact with the orifice of the inferior vena cava (fig. 4). 4) Interior of the right atrium (fig. 5) The attitude of the openings of the right superior and inferior venae cavae follows the usual way. The foramen ovale is completely closed. The opening of the coronary sinus is oval (ca. 28 x 18 mm), and is protected by the valvula of the sinus which adheres to the anterior end of the valvula of the inferior vena cava and makes a _ small sac (ca. 7 mm in depth) between both valvulae.

B. The azygos veins (figs. 4, 6) This venous system is made up of bilaterally symmetrical azygos veins, though the left fellow (ca. 9 mm in width) is thinner than the right one (ca. 15 mm). The vein of each side from the runs upward on the anterolateral surface of the thoracic column after piercing the diaphragm, then arches forward in the height of Th IV. The vein passes above the pulmonary root to flow into the superior vena cava of the respective side just before it pierces the pericardium. The opening of the left azygos is slightly lower than the right one. The tributaries of the veins are almost same on both sides. The second and third (second to fourth on left side) posterior . are drained by a common stem, the superior intercostal vein, then flow into the upper end of the azygos. The fourth to eleventh (fifth to eleventh on left side) posterior inter- costal and the subcostal veins directly open into the azygos. The first posterior intercostal vein follows the supreme intercostal vein which drains into the vertebral vein, and communicates with the second posterior intercostal vein. No communication is observed be- tween the azygos veins of both sides.

C. Right double subclavian veins (figs. 1, 2, 4, 7) The veins (ca. 33 mm in length) in this case consist of two chan- nels, anterior (ca. 30 mm in width) and posterior (ca. 10 mm). They, holding the M. subclavius between them, drain into the right internal ; the anterior channel into the lateral wall of the lower end of the internal jugular and the posterior channel into it in con- tact with the anterior channel inferoposteriorly. (a) Veins joining the anterior channel i) : It (ca. 5 mm) begins by the confluence of the posterior auricular and the occipital veins, and enters the superior wall of the middle of the channel. It is provided with two bicuspid valves both at lower end and in the middle. ii) (ca. 3.5 mm), anteromedial to the join- ing of the external jugular. 416 Y. Fujimoto, H. Okuda and M. Yamamoto

iii) Thoracoacromial vein (ca. 5 mm), lateral to the external jugular. iv) Vv. pectrales (ca. 1 mm). v) A confluence (ca. 4 mm) of the transverse cervical and the suprascapular veins, near the termination of the anterior channel. Besides the right lymphatic duct joins the confluence. vi) Corresponding vein (ca. 2 mm) of the ascending cervical artery, at the right venous angle. (b) Veins joining the posterior channel Only the dorsal scapular vein (ca. 1 mm) unites with the con- fluence of the transverse cervical and suprascapular veins. The left is single and not noteworthy.

D. Left external (figs. 6, 8) The vein divides into two channels, lateral and medial, just before joining the left internal iliac, so a ring-formation (ca. 20 mm in length) is observed. The lateral channel (ca. 5 mm in width and 9 mm in length) receives the communicating with the ascending lumbar into the superolateral wall. The medial one (ca. 11 mm in width and 13 mm in length) does not receive any vein. Both channels hold the from the internal iliac between them.

Discussion

The present report was the second case of the bilateral superior venae cavae found in the cadavers which have been dissected at this university. The latest case of the bilateral superior venae cavae in Japan was reported by Chiba et al. (1971). Hitherto in Japan 45 cases have been reported ; 43 Japanese, 1 Chinese and 1 Formosan. Of them, adults who died at ages over 16 years numbered only 26. On the other hand in Europe and America 216 cases were reported by 1946 (Sanders 1946). On the frequency of the bilateral superior venae cavae have been described by many authors as follows ; Adachi (1933) 4 in 821 cases (0.5%), Mukai (1934) 1 in 679 cases, Yamada (1934) 2 in 125 cases (fetuses and newborns), Sanders about once per 348 cadavers. The bilateral superior venae cavae have been classified by Mc- Cotter (1915), Donadio (1925), McManus (1941), Nandy et al. (1965), and Yamadori et al. (1966) etc. ; it was considered that the classifi- cation made by Yamadori et al. might be considerably adequate. Compared with other author's classification, the modification of A Case of the Bilateral Superior Venae Cavae 417

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418 Y. Fujimoto, H. Okuda and M. Yamamoto

Yamadori's was shown in the table 1. According to the table, the present case might belong to Type 1 (RL). While the frequency of these types was followed the table 2.

Table 2. The Reported Cases of the Bilateral Superior Venae Cavae.

( ) : by McCotter (1915) * included our case Children mean 1-15 year-old in Japan, while 1-11 year-old in America.

In case of the typical persistent left superior vena cava, thirteen reporters (Halberstma 1862, MAusert 1899, Gruber 1908, Niitzel 1914, Dietrich 1915, Kodama 1931, Mukai et al., Prows 1943, Sanders, Yoshida et al. 1957, Otsuka 1961, Nandy et al., Takagi et al.) described that the hemiazygos and the accessory hemiazygos veins nearly resembled to the feature of the right azygos vein, and ran upward parallel with it for the opening into the left superior vena cava. The present case also was the same as their descriptions. And, any communication between the azygos veins of both sides was not seen as Kodama pointed out. This might be due to the persistence of the left which would empty to the future azygos vein. In this case, the fact that both azygos veins had a connection with the vertebral vein via the supreme intercostal vein, showed that the ascending lumbar, the azygos and the vertebral veins have developed from the identical system of the intersegmental vein. Accordingly, in survey of the azygos system, it has been necessary to observe the features of the supreme intercostal and the vertebral veins. In literature, any report about the double subclavian veins has not been seen. It was very interesting that the main anterior channel passed between the clavicle and the M. subclavius. In figure 403 in Human Embyology by Patten (1953) such a double subclavian vein was drawn on 6 week-old fetus, so the present case might be a developing arrest of this stage. Rarely the simple subclavian A Case of the Bilateral Superior Venae Cavae 419 vein passed through between the clavicle and the M. subclavius by Cunningham (1953), the anterior channel might correspond to this anomalous vein. About the ring-formation of the , Adachi illustrated the similar case in figure 174 (but on right side) of his publication, in which a branch from the pierced through it.

Summary 1) A newly discovered case of the double superior venae cavae was described, in which the left superior vana cava descended sym- metrically to the right one and connected with the coronary sinus. 2) An anastomosis between the right and left superior venae cavae was not found. The present case belonged to Type 1 (RL) by the modified Yamadori's classification. 3) The complete paired azygos veins did not anatomose with each other. Both vessels communicated with the supreme intercostal vein emptying to the vertebral vein. 4) The right subclavian vein consisted of two channels, between which the M. subclavius was held. The bigger anterior channel was the main stream of the subclavian proper. 5) The left external iliac vein made a ring-formation through which the left iliolumbar artery passed.

Grateful acknowledgementis made to Prof. Y. Ohta and Dr. T. Tokioka, lecturer, for their constant interest and guidance in this work.

References 1) Abe, K. 1964: An abnormal case of the coronary sinus with no opening into the right atrium (A case of the so-called left superior vena cava). Acta Anat. Nippon., 39 249-251.(in Japanese) 2) Adachi, B. 1933: Das Venensystem der Japaner. 1 Lieferung, Kyoto, 68-76 83-87. , 3) Akiyama, S., T. Nakanishi, S. Iwasaki and T. Abe, 1965: A case of unilateral left superior vena cava. Fukushima J. Med. Sci., 12 : 137-145. 4) Ancel, P. and F. Villemin, 1908: Sur la persistence de la veine cava superieure gauche chez l'homme. J. de l'anat., 44: 46-62. 5) Aso, M. 1931: Ein Fall von Verdoppelung der Vena cava superior bei einem japanischen FOtus. Acta Anat. Nippon., 4: 492-497. (in Japanese) 6) Chiba, T., K. Inoue and Y. Yoshida, 1971: A case of a left superior vena cava Swithout any corresponding vessel on the right side. Acta Anat. Nippon., 46(3) : upplements 1-2. (abstract in Japanese) 7) RChouke, K. S. 1939: A case of bilateral superior venae cavae in an adult. Anat. ec., 14: 151-157. 8) Cunningham, D. J. 1953: Cunningham's text-book of anatomy. 9th Ed., London, 420 Y. Fujimoto, H. Okuda and M. Yamamoto

1339. 9) Dietrich, A. 1915 : Uber ein Fibroxanthosarkom mit eigenartiger Ausbreitung und Uber eine Vena cava superior sinistra bei dem gleichen Fall. Virchows Arch. path. Anat. Physiol., 212. Cited from Mukai et al. 10) Donadio, N. 1925 : Ein Fall von Verdoppelung der Vena cava superior. Anat. Anz., 59 : 321-327. 11) Fujimoto, K., Y. Sato, T. Shiba, N. Oku and T. Morinaga, 1956 : A case of persistent left superior vena cava. Jap. J. Clin. Med., 14 : 37-46. (in Japanese) 12) Gibson, A. 1921 : Note on a persistent left duct of Cuvier. Anat. Rec., 20: 420-422. 13) Gruber. 1908 Ein Fall von Einmiindung der Vena pulmonalis dextra in die Vena cava superior. Virchows Arch. path. Anat. Physiol., 193. Cited from Mukai et al. 14) Halberstma. 1862 : Ned. T. Geneesk., 610. Cited from Ancel et al. 15) Hanzawa, S. et al., 1955 : A case of congenital heart disease with bilateral superior vena cava and dextrocardia. Resp. Circ., 3 : 575. (abstract in Japanese) 16) Hashimoto, M. 1940 : A case of the double superior vena cava and the double inferior vena cava in North Chinese. Mansyu Med. J., 33 : 821-824. (in Japanese) 17) Hayashi, I., N. Okamoto, T. Matsunaga, H. Tsuchiyama and T. Yamabe, 1953: Malformations in the fetuses and neonatal corpses. (Report III) The cardio- vascular system. Trans. Soc. Path. Jap., 42 : 189-190. 18) Kikkawa, F. 1961 : A case of the double superior venae cavae. J. Nihon Med. College, 28 : 33-34. (abstract in Japanese) 19) Kino, 0. 1939 : Uber die Venen der Wirbelsaule der Japaner. Acta Anat. Nip- pon., 14 : 287-304. (in Japanese) 20) Kinoshita, Y., 0. Arai, S. Shimada, H. Kameyama, Y. Katagiri, K. Kasai, M. Kurashige, Y. Yokoyama and R. Horikawa, 1957: A case of the with the bilateral superior venae cavae. Resp. Circ., 5: 502-506. (in. Japanese) 21) Kodama, K. 1931 : Persistenz des Ductus Cuvieri sinister bei einem Japaner. Okajimas Fol. Anat. Jap., 9: 365-369. 22) Konda, T. and Y. Ohta, 1949: A case of the left superior vena cava. Acta Anat. Nippon., 25: 40. (abstract in Japanese) 23) Matsumoto, T., Y. Tonoue and K. Arihara, 1963 : Anomalous cases detected at the time of routine dissection of systematic anatomy. III. A case of the double superior vena cava. J. Kansai Med. College, 15: 73-77. (in Japanese) 24) Matsuyama, M. 1940 : A case of the double superior venae cavae in Formosan. Taiwan Med. J., 39 : 116-121. (in Japanese) 25) Mausert. 1899 : Zur Kasuistik der Vena cava superior sinistra und der Spitzen- lappen der rechten Lunge abschniirenden Anomalie der Vena azygos. I-Diss. Giessen. Cited from Schtitz. 26) McCotter, R. E. 1915 Three cases of the persistence of the left superior vena cava. Anat. Rec., 10: 371-383. 27) McClure, C. F. W. and E. G. Butler, 1925 : Development of inferior vena cava in man. Amer. J. Anat., 35: 331-383. 28) McClure, C. F. W. and G. S. Huntington, 1929 : The mammalian vena cava posterior. An ontogenetic interpretation of the atypical forms of vena cava posterior (inferior) found in the adult domestic cat (Felis domestica) and in man. Amer. Anat. Mem., 15, Phila. 29) McManaus, F. A. 1941 : Canad. M. A. J., 45: 261. Cited from Fujimoto et al. 30) Miura, M. 1897: Congenital anomaly in vessels. Tokyo Med. J., 11: 817-819. (in Japanese) 31) Mori, K. and H. Moriwaki, 1941: A case of the double superior venae cavae. A Case of the Bilateral Superior Venae Cavae 421

Kyoto Med. J., 38 : 513-514. (in Japanese) 32) Mukai, I. and K. Nomura, 1934 : A case of the left superior vena cava. Hok- kaido Med. J., 12 : 82-92. (in Japanese) 33) Murakami, M., S. Nagano and H. Fukuda, 1957 : Uber 2 Falle von der Persis- tenz der linken Hohlvene. Kurume Med. J., 20 : 133-139. (in Japanese) 34) Nandy, K. and K. B. Blair, Jr., 1965 : Double superior venae cavae with com- pletely paired azygos veins. Anat. Rec., 151 : 1-9. Cited from Takagi et al. 35) Nishii, H. and Y. Suga, 1939 : Ein Sektionsfall von verdoppelten oberen Hohl- venen. Okayama Med. J., 51 : 206-211. (in Japanese) 36) Niitzel, H.1914 : Beitrag zur Kenntnis der Missbildungen imBereiche der oberen Hohlvene. Frankfurter Zeitschr. f. Path., 15 : 1-19. Cited from Mukai et al. 37) Omori, I. and T. Shirnamoto, 1956 : A case of the heart with the left superior vena cava and without a typical coronary sinus. Kagoshima Med. J., 29 : 19-20. (in Japanese) 38) Otsuka, N. 1961 : Ein Fall mit doppelter Vena cava superior bei einer japanischen. Frau. Acta Anat. Nippon., 36 : 298-304. (in Japanese) 39) Patten, B.M. 1953 Human . 2nd Ed., New York, 637-649. 40) Prows, M. S. 1943 : Two cases of bilateral superior vena cava, one draining a closed coronary sinus. Anat. Rec., 87 : 99-106. Cited from Sanders. 41) Roberts, J. T. 1961 : Arteries, veins and lymphatic vessels of the heart. Develop- ment and structure of the cardiovascular system. New York, 85-118. 42) Sanders, J.M. 1946 : Bilateral superior venae cavae. Anat. Rec., 94 : 657-662. 43) Sato, H. 1952 : A case of double superior venae cavae. Fukushima Med. J., 2: 183-188. (in Japanese) 44) Schatz, H. 1919 : Einige Falle von Entwicklungsanom alien der Vena cava superior (Persistenz des linken Ductus Cuvieri). Virchows Arch. path. Anat. Physiol., 216 : .35-45. 45) Seib, G.A. 1934 : The azygos system of veins in American Whites and Negros, including observations on the inferior caval venous system. Amer. J. Phys. Anthropol., 19: 39. 46) Taguchi, K., K. Tago, T. Sunada, T. Kimoto and S. Tsuda, 1956: A case of atrial septal defect with abnormalities of the great veins and the right atrium. Resp. Circ., 6: 507-512. (in Japanese) 47) Takagi, T. and T. Osuga, 1967 : A case of bilateral superior venae cavae with paired azygos veins in a Japanese male. Acta Anat. Nippon., 43 : 131-137. 48) Tanaka, M., C. Takaoka, H. Matsuzaki, K. Ookawa and S. Saito, 1966: Uber einen Fall von der kompletten Heterotaxie. Kurume Med. J., 29 : 520-534. (in Japanese) 49) Tochinai, I. and T. Ohta, 1944: A case of double superior venae cavae. J. Iwate Med. College, 7: 82-87. (in Japanese) 50) Yamada, S. 1934: Uber zwei Falle von Verdoppelung der Vena cava superior. Acta Anat. Nippon., 7: 348-356. (in Japanese) 51) Yamadori, T., S. Takashima and S. Takashima, 1966: A case of the double superior vena cava. Acta Anat. Nippon., 41 : 213-221. (in Japanese) 52) Yamamoto, S. 1939: Zwei Falle seltener Missbildungen. Acta Anat. Nippon., 13: 262-276. (in Japanese) 53) Yoshida, Y., T. Ohashi, K. Takano, H. Kusaka and T. Aoki, 1957 : A case of the double cranial caval vein. Mie Med. J., 7: 95-99. 422 Y. Fujimoto, H. Okuda and M. Yamamoto

Explanation of Figures

Key to Abbreviations

A je External jugular vein ac Common carotid artery ji ai Iliolumbar artery 1 Lateral channel of external aic Common iliac artery iliac vein aie External iliac artery la Ascending lumbar vein aii Internal iliac artery LA Lig. arteriosum al Left azygos vein liv Fourth lumbar vein AL Left atrium m R. mediastinalis ap md Medial channel of external ar Right azygos vein iliac vein AR Right atrium mr Right marginal veifi as Subclavian artery MS M. subclavius AU Right auricle 0 ax Axillary artery ob Obturator nerve ca Corresponding vein of OR Right atrioventricular orifice ascending cervical artery pe V. pectralis ce Cephalic vein ph Phrenic nerve cg Great cardiac vein pp Pericardiacophrenic vein ci Inferior vena cava ps Posterior vein of left ventricle CL Clavicle re Recurrent laryngeal nerve cm Middle cardiac vein s Subclavian vein co Confluence of transverse cervical sa Anterior channel of subclavian and suprascapular veins vein COI Costa I sb cs SC Coronary sinus csl Left superior vena cava sd Dorsal scapular vein csr Right superior vena cava sp Posterior channel of subclavian ct Transverse cervical vein vein dr Right lymphatic duct ss Suprascapular vein dt Thoracic duct ta Thoracoacromial vein f Femoral nerve th ic tm Thymic vein ie External iliac vein tr Inferior thyroid vein ii U i Iliolumbar vein v Vertebral vein ip Posterior intercostal vein va Vagus nerve isr Supreme intercostal vein vp Pulmonary vein isp Superior intercostal vein VR Right ventricle ja Anterior jugular vein 4 Case of the Bilateral Superior Venae Cavae 423

PLATES 424 Y. Fujimoto, H. Okuda and M. Yamamoto

Plate I

Figs. 1 & 2. Anterior view. Ca. x3/8 Fig. 3. Posterior veiw. The left superior vena cava flows into the coronary sinus. Ca. x1/2 Fig. 4. Posterior view. The coronary sinus opens into the right atrium (1=,-). Ca. x 3/8 Fig. 5. The interior of the right atrium, the wall of which is incised along the right superior and the inferior venae cavae. The stream is indicated with white arrows. Small sac (/). Ca. x1/2

Plate II

Fig. 6. The azygos and the . The iliolumbar artery (/) passes through the ring-formation of the external iliac vein. Ca. x3/10 Fig. 7. Inferoanterior view of the double subclavian veins. The clavicle and the medial half of the M. subclavius are removed. Ca. x2/3 Fig. 8. Anterior view of the ring-formation of the external iliac vein. Ca. x 5/8 425

A Case of Bilateral Superior Venae Cavae Plate I

i1 2

3

5 4

Y. Fujimoto. H. Okuda & M. Yamamoto 426

A Case of Bilateral Superior Venae Cavae Plate II

6

Y. , Fujimoto, H. Okuda & M. Ya mamoto