ARTICLE IN PRESS Ann Anat 189 (2007) 191—195
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Preureteric inferior vena cava with possible rudiment of the proper inferior vena cava Satoru Honma, Akinari Tokiyoshi, Katsushi Kawai, Masahiro Koizumi, Kodo Kodama Department of Anatomy, Graduate School of Medical Sciences, Kumamoto University, 1-1-1 Honjo, Kumamoto 860-8556, Japan Received 4 April 2006; accepted 5 September 2006
KEYWORDS Inferior vena cava; Ureter; Gonadal vein; Lumbar splanchnic nerve; Subcardinal vein
Summary A right single preureteric inferior vena cava (IVC) was found in the cadaver of a 77-year-old Japanese male during a student dissection course at Kumamoto University School of Medicine in 2003. The ureter emerged from the lower end of the hilum of the right kidney at the second lumbar vertebral level. It ran inferomedially to pass behind the IVC, and turned inferolaterally to cross the vein superficially at the level of the third to the fourth lumbar vertebrae. Then, the ureter was situated to the right of the IVC, and descended ordinarily. The second lumbar vein of each side united bilaterally, as did the third lumbar veins. The common stem of the second lumbar veins drained into the left side of the IVC posterolaterally at the level of the second intervertebral disc, and the third common stem opened into the left border of the IVC at the fourth lumbar vertebral level. The ureter hooked around the IVC between the openings of those common stems. There was a small continuation (0.2 mm in diameter) between the left second lumbar and the right third lumbar veins along the vertebral column slightly right of the midline. It passed superficial to the right third lumbar artery, as did the IVC. The right testicular vein opened into the IVC at the level of the lower end of the third lumbar vertebral body. Generally, the level of the opening of the gonadal vein corresponds to the level of the caudal end of the remaining subcardinal vein, but it is lower than usual in this case. Furthermore, the segment from the confluence of the common iliac veins to the common trunk of the third lumbar veins, and to the small continuation can be regarded as the proper IVC, and the part where the ureter hooks around it may have derived from the anastomosis between the common trunk of the third lumbar veins and the subcardinal vein. & 2006 Elsevier GmbH. All rights reserved.
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Introduction A preureteric inferior vena cava (IVC) is a wellknown variation, showing the disposition of the ureter and the IVC. The ureter in that case is called a retrocaval ureter, and may present with symptoms of obstruction (Gray and Skandalakis, 1972; Retik and Schlussel, 2003). More than a 100 years ago, anatomists described this anomaly, as being a result of the unusual development of the IVC (Hochstetter, 1893; Kolisko, 1909; Gladstone, 1911; Rotter, 1935; Adachi, 1940; Pick and Anson, 1940; Gruenwald and Surks, 1943). This variation has also motivated embryologists to clarify its developmental background, and led them to the investigations of the development of the IVC (Hochstetter, 1893, 1906; Huntington and McClure, 1920; McClure and Butler, 1925; Gru ¨nwald, 1938). Anatomical, embryological, and clinical textbooks (Hollinshead, 1971; Gray and Skandalakis, 1972; Hinman, 1993; Retik and Schlussel, 2003) adopt such results for the explanation of the preureteric IVC. In the right single preureteric IVC, we found two features which reveal the developmental background of this case. Here, we report on the gross anatomical configuration in detail, and discuss its composition based on the findings.
S. Honma et al. vertebral level (Fig. 1). As the renal pelvis of each side was not funnel-shaped, the ureteropelvic junctions were not distinct. The right ureter ran inferomedially to pass behind the IVC, and turned inferolaterally to cross the vein superficially at the level of the third to the fourth lumbar vertebrae. The ureter, now situated to the right of the IVC, then descended ordinarily. The second lumbar vein of each side united bilaterally, as did the third lumbar veins. The common stem of the second lumbar veins drained into the left side of the IVC posterolaterally at the
Materials and methods The anomaly was found in the cadaver of a 77-year-old Japanese male who died of hepatocellular carcinoma. No scars or surgical incisions were observed in the skin. After removing the gastrointestinal viscera, the kidneys, ureters and related vessels in the retroperitoneal cavity were carefully examined. Gross anatomical observations revealed no signs of either hydronephrosis or other anomalies in the urinary tract. According to the same procedures, an additional 19 bodies (13 male, 6 female) of the 25 without prominent deformities of the vertebral columns were further examined at the sites of the openings of the gonadal veins and the prevertebral distributions of the lumbar veins. Three of the cases were excluded because of obvious pathological changes of the vertebral column, and another two for lack of the 12th costa. The results were recorded by photographs and sketches.
Results Variation of IVC The ureter emerged from the lower end of the hilum of the right kidney at the second lumbar
Figure 1. Drawing of the case. The right testicular vein opened into the right side of the IVC at the level of the lower end of the third lumbar vertebral body. The small continuation between the right third lumbar vein and the left second lumbar vein (asterisk) runs along the vertebral column slightly right of the midline. It passes superficial to the right third lumbar artery. Additionally, there is a venous island, with its proximal end opened to the origin of IVC and its distal end to the external iliac vein (double asterisk), that surrounds a proximal part of the right external iliac artery. AL3, third lumbar artery; Ao, aorta; Az, azygos vein; At, testicular artery; EI, external iliac artery; Haz, hemiazygos veis; IVC, inferior vena cava; Lspl, lumbar splanchnic nerve; L3/4 (4/5), third (fourth) lumbar disc; Th11, 11th thoracic vertebra; Ur, ureter; VL2 (3), second (third) lumbar vein; Vt, testicular vein.
ARTICLE IN PRESS Preureteric inferior vena cava level of the second intervertebral disc, and the common stem of the third lumbar veins opened into the left border of the IVC at the fourth lumbar vertebral level. The ureter hooked the IVC between the openings of those common stems, and the right lumbar splanchnic nerve ran deep to the IVC at that point. There was a small continuation (0.2 mm in diameter) from the right third lumbar to the left second lumbar vein (asterisk, in Fig. 1). It ran along the vertebral column slightly right to the midline, and ran deep to the right ureter and the lumbar splanchnic nerve, superficial to the right third lumbar artery. The right testicular vein opened into the right side of the IVC at the level of the lower end of the third lumbar vertebral body. In addition, on the right side, a small vein was found forming a venous island, with its proximal end open to the origin of IVC and its distal end to the external iliac vein (double asterisk, in Fig. 1). No vein opened to the island, which surrounded a proximal part of the right external iliac artery. The azygos and hemiazygos veins did not continue to the IVC directly.
Level of the openings of the right gonadal veins, and prevertebral longitudinal anastomosis between the second and the third lumbar veins In the 19 cases examined, all 22 of the right gonadal veins (doubled in 3 cases) flowed either into the caudal angle formed by the IVC and the right renal vein or into the IVC, with 16 of the veins flowing into the latter. In 11 of these 16 veins, the levels of the openings were higher than the third lumbar vertebral body, three were at the level of the cranial half of the third vertebral body, and two were at the level of the middle of the third lumbar intervertebral disc. All of the left gonadal veins opened into the left renal veins. The longitudinal anastomosis between the second lumbar vein and the third lumbar vein, running medial or paramedial to the vertebral column on the surface of the anterior longitudinal ligament, were not observed except in an instance of the preureteric IVC.
Discussion The preureteric IVC is an uncommon variation, and is thought to represent an unusual development of the IVC (Hochstetter, 1893; Kolisko, 1909; Gladstone, 1911; Rotter, 1935; Adachi, 1940; Pick
193 and Anson, 1940; Hollinshead, 1971; Gray and Skandalakis, 1972; Hinman, 1993; Retik and Schlussel, 2003). Those authors had two explanations for it: they assumed that a part of the postrenal segment of the IVC was composed of the posterior cardinal vein, instead of the supracardinal vein (Hochstetter, 1893; Kolisko, 1909; Gladstone, 1911; Rotter, 1935; Adachi, 1940; Pick and Anson, 1940; Hollinshead, 1971; Gray and Skandalakis, 1972; Hinman, 1993; Retik and Schlussel, 2003), or it was formed by the caudal anastomosis between the subcardinal and the sacrocardinal veins (Gruenwald and Surks, 1943). However, gross anatomical examination of the venous branches with relation to the surrounding structure have not been described sufficiently. So we examined even the small or rudimentally veins, because they may be decisive in explaining the configuration of the main venous stem, and we actually found two such clues for this case. One is the right testicular vein, and the other is the longitudinal anastomosis from the right third lumbar vein to the left second lumbar vein (Figs. 1 and 2). The right renal vein ends in this preureteric vena cava at the level of the first lumbar intervertebral disc and is not anomalous, but the right testicular vein opens into the IVC at the level of the lower end of the third lumbar vertebral body. This is lower than usual; actually 11 of 16 gonadal veins ended in the IVC higher than that level. We think this is one of the characteristics of the present preureteric IVC. Actually, Hochstetter (1893) reported the retrocaval ureter in a male infant a few weeks after birth, and stated that ‘‘yV. spermatica dextra etwas weiter caudalwa ¨rts mu ¨ndet’’. After this, there are no references made to the level of the opening of the right gonadal vein, but the figures in some of the reports in the literature reveal this fact (Kolisko, 1909; Gladstone, 1911; Rotter, 1935; Adachi, 1940; Gruenwald and Surks, 1943). The gonadal veins are said to be the remnants of the subcardinal veins below the kidneys, and their opening to the IVC indicate the level of the caudal end of the subcardinal vein (Huntington and McClure, 1920; McClure and Butler, 1925; Gru ¨nwald, 1938; Gruenwald and Surks, 1943; Arey, 1965; Patten, 1968; Schmidt, 1975). Applying this to the present preureteric IVC, it is possible that the subcardinalis persisted more caudally than usual. Hence, we think the caudal persistence of the subcardinal vein is one of the causes in the formation of the preureteric IVC. Gruenwald and Surks (1943) have also proposed a similar explanation for their case based on their embryological observations.
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S. Honma et al. laparoscopic treatment for the retrocaval ureter is performed (Franke et al., 2003). The small longitudinal anastomosis from the right third lumbar vein to the left second lumbar vein runs along the vertbral column slightly to the right of the midline, and does not continue to the azygos or to the hemiazygos vein. Such an anastomosis was not found in the 19 bodies examined. In the extensive study of the lumbar azygos vein made by Ogura (1984), no anastomosis like this was found. The small vein seems to belong to the subcentral vein or to the lumbar azygos vein (Gladstone, 1929; Hamilton and Mossman, 1978) judging from its running course. Gladstone wrote that the subcentral vein differs from the azygos vein in that it lies dorsomedial to the segmental arteries. On the other hand, the small vein passes superficial to the right third lumbar artery, and continues to neither the azygos vein, nor to the
Figure 2. Schematic drawing of the preureteric vena cava and aorta with their branches. The level of opening of the right testicular vein to the IVC is lower (more caudal) than usual. The small longitudinal vein (asterisk) runs along the vertebral column slightly right of the midline and passes superficial to the right third lumbar artery. These characteristics are similar to the IVC, even the vein is small in diameter. Double asterisk indicates the venous island surrounding the external iliac vein. AL2 (3), second (third) lumbar artery; Ao, aorta; Az, azygos vein; EI, external iliac artery; Haz, hemiazygos veis; IVC, inferior vena cava; Lasc, ascending lumbar vein; L2, second lumbar vertebra; L3/4, third lumbar disc; Th11, 11th thoracic vertebra; Ur, ureter; VL2 (3), second (third) lumbar vein; VRr (l), right (left) renal vein; Vt, testicular vein.
Clinically, our result of the level of the openings of the right gonadal veins will be useful for surgeons in avoiding gonadal vein injury, when
Figure 3. Possible courses of the proper IVC in this case. (a) The course from the longitudinal anastomosis (asterisk) to the IVC through the left second lumbar vein. (b) The topographic relation between the lumbar splanchnic nerve and the anastomotic vein suggests the complete disappearance of the superficial course to the nerve. IVC, inferior vena cava; Lspl, lumbar splanchnic nerve; Ur, ureter; VL2 (3), second (third) lumbar vein; Vt, testicular vein.
ARTICLE IN PRESS Preureteric inferior vena cava hemiazygos. Thus we think that it does not belong to either of those veins, but is actually a part of the proper IVC replaced by the preureteric IVC. However, the problem remains as to where the longitudinal anastomosis, or the proper IVC continues cranially. The simple course from the right third lumbar vein, through the longitudinal anastomosis and the left lumbar vein, to the IVC seems to reveal a part of the proper IVC (a, in Fig. 3). On the other hand, the right lumbar splanchnic nerve generally passes deep to the IVC (Woodburne and Burkel, 1994) while the nerve in this case passed superficial to that venous course (Figs. 1 and 3). Hence the part of the proper IVC, which crosses superficial to the lumbar splanchnic nerve (b, in Fig. 3), may have disappeared completely. Finally, regarding the venous island surrounding the right external iliac artery, Gruenwald and Surks (1943) observed a similar venous island. They surmised that the preureteric IVC in their case may also have had a close relation in forming the island, but in our case, there was no gross anatomical finding to suggest its developmental background, and further examples are needed before a better explanation can be made.
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