This is “Advance Publication Article” Kurume Medical Journal, 64, 103-107, 2017 Case Report A Retroaortic Left Renal in a Female Cadaver

YOSHIKO FUJISHIMA, KOICHI WATANABE*, YOKO TABIRA*, JOE IWANAGA*,**, †, YUI ODO, TSUYOSHI SAGA*, R. SHANE TUBBS**, ‡ AND KOH-ICHI YAMAKI*

Medical student, Kurume University School of Medicine, *Department of Anatomy, Kurume University School of Medicine, Kurume, 830-0011 Japan, **Seattle Science Foundation, Seattle, 98122 United States, †Dental and Oral Medical Center, Kurume University School of Medicine, Kurume 830-0011, Japan, ‡Department of Anatomical Sciences, St. George’s University, St. George’s, Grenada.

Received 4 October 2017, accepted 23 November 2017 J-STAGE advance publication 21 May 2018 Edited by TOSHI ABE

Summary: We encountered a case of retroaortic left (RLRV) during an anatomical dissection course at our medical school in 2017. The case was a female cadaver who was 88 years old at death. Six roots of the left renal vein (RV) arose from the hilus of the kidney and joined to form one left renal vein, crossed dorsal to the abdominal aorta (AA) at the level of the second lumbar vertebra, and then drained into the inferior vena cava (IVC). Two roots joined at the right renal hilus to become the right RV to then drain into the IVC at the level of the first lumbar vertebral body. The reported frequency of RLRV is approximately 2%. Embryologically, the normal anastomosis of the left and right sub-cardinal results in the left RV traveling on the ventral surface of the AA. However, in the case presented here, the left RV traveled on the dorsal side of the AA due to the anastomosis of the left and right supra-cardinal veins and regression of the anastomosis between the left and right sub-cardinal veins. If both the dorsal and ventral anastomoses remain, the left RV travels on the dorsal and ventral sides of the aorta. Some of the clinical problems reported in association with RLRV are hematuria and abdominal pain, and the risk of damaging the RLRV during surgery of the posterior abdominal wall. Venous vari- ants as reported herein should be kept in mind when interpreting imaging of the posterior abdominal wall or per- forming surgery or other invasive procedures near the RLRV.

Key words retroaortic left renal vein, inferior vena cava, kidney, renal , cadaver, dissection, anatomy

INTRODUCTION CASE REPORT A retroaortic left renal vein (RLRV) was found dur- The RLRV was found in a female Japanese ca- ing routine anatomical dissection. This variation occurs daver whose age at death was 88 years old. (Figure 1, in approximately 2% of the population. Clinically, the 2) The cause of death was cancer of an unknown pri- nutcracker phenomenon, caused by narrowing of the mary origin. There were no scars around the skin of left RV between the descending aorta and the spinal the . column, places this vessel at risk during abdominal aortic surgery. Therefore, awareness of this variation Inferior vena cava (IVC) has clinical and surgical significance. The right and left common iliac veins joined at the position of the fourth lumbar vertebral body to become

Corresponding Author: Joe Iwanaga DDS, Ph.D, Department of Anatomy, Kurume University School of Medicine, 67 Asahi-machi, Kurume, Fukuoka 830- 0011, Japan. Tel: +81-942-31-7540, Fax: +81-942-33-3233, E-mail: [email protected]

Abbreviations: AA, abdominal aorta; IVC, inferior vena cava; RLRV, retroaortic left renal vein; RV, renal vein 104 FUJISHIMA ET AL.

Fig. 1. The abdominal cavity Arterial system; A superior mesenteric artery, a right renal artery, two left renal , inferior mesenteric artery and right and left common iliac artery arising Fig. 2. Arteries, veins, kidney and from the descending abdominal aorta. removed from abdominal cavity. Venous system; Right and left common join- Arterial system; Abdominal aorta branching superior ing to become inferior vena cava and right ovarian mesenteric artery, inferior mesenteric artery, right and vein, right and left renal vein, and hepatic vein flow- left common iliac arteries. ing into inferior vena cava. Venous system; Right renal vein flowing into inferior AA, abdominal aorta; AG, adrenal gland; CIA, com- vena cava and left renal vein running transversely mon iliac artery; CIV, ; IMA, infe- behind abdominal aorta and flowing into inferior vena rior mesenteric artery; IVC, inferior vena cava; K, kid- cava. ney; LRA, left renal artery; RRV, right renal veins; AA, abdominal aorta; AG, adrenal gland; CIA, com- SMA, superior mesenteric artery; SRA, suprarenal mon iliac artery; IMA, inferior mesenteric artery; IVC, artery; U, ureter. inferior vena cava; K, kidney; RRV, right renal veins; SMA, superior mesenteric artery; SRV, suprarenal vein; U, ureter. the IVC. The fourth and third drained into the IVC posteriorly at the level of the fourth lum- bar vertebral body where the left and right common was at the level of the inferior border of the twelfth iliac veins joined, and at the level of the third lumbar thoracic vertebra, with a length of 105.2 mm and width vertebral body, respectively. The left RV and the right of 36.7 mm. The position of the upper border of the fl owed into the IVC at the level of the right kidney was at the level of the superior border of second lumbar vertebral body, the right adrenal vein the twelfth thoracic vertebra, with a length of 106.45 fl owed into the IVC at the level of the fi rst lumbar mm and width of 40.7 mm. Although the right kidney vertebral body, and the hepatic veins drained into the was slightly larger than the left, no abnormality was IVC at the vena caval foramen. seen in regard to shape or size.

Morphology of the kidney Left renal vein The position of the upper border of the left kidney Six roots of the left RV arose from the hilus and

Kurume Medical Journal Vol. 64, No. 4 2017 RETROAORTIC LEFT RENAL VEIN 105 joined into one left renal, received the left ovarian vein vein and merged with the IVC at the level of the fi rst (4.2 mm in diameter) and the left suprarenal vein (4.4 lumbar vertebral body. The width of the right RV at the mm in diameter), crossed dorsal to the abdominal aorta junction of the two roots was 13.60 mm and the length (AA) slightly downward at the level of the second of the right RV from the right renal hilus to the point lumbar vertebra, and then drained into the IVC. The where the right RV drained into the IVC was 18.20 mm. left RV dorsal to the AA received the fi rst lumbar vein from the upper wall, and the and Left renal artery the second lumbar vein from the lower wall. (Figure Two left renal arteries were observed, the upper and 3) At the upper wall of the left RV where it drained into lower renal arteries. The upper one arose from the AA the IVC, a small branch ascended behind the AA to just below the origin of the superior mesentery artery become the hemiazygos vein. The diameter of the left and drained into the renal parenchyma, which was RV was 9.00 mm where the six roots joined to become above the renal hilus. The lower one originated from the single left RV with a maximum of 21.00 mm and a the AA at the level of the second lumbar vertebra, minimum of 14.80 mm posterior to the abdominal coursed behind the right suprarenal vein and drained aorta. Total length of the left renal vein was 75.20 mm, into the renal hilus. with a part 23.30 mm in length behind the AA. Right renal artery Right renal vein The right renal artery arose from the AA at the same Two roots joined at the right renal hilus to become level as the upper left renal artery and traveled upward the right RV, which received the right inferior phrenic toward the renal hilus.

Fig. 3. Posterior view of Figure 2. Artery The descending abdominal aorta giving rise to the middle suprarenal artery, left renal artery, and right renal artery. The first, second, third lumbar arteries branching from the posterior aspect of the abdominal aorta. Vein The right renal vein draining from the right kidney and passing behind the descending abdominal aorta and then draining into the inferior vena cava. The first, second, and third lumbar veins flow into the infe- rior vena cava at the same level as each lumbar artery. AA, abdominal aorta; AG, adrenal gland; G, left ovarian vein; IVC, inferior vena cava; K, kidney; LRA, left renal artery; L1, the first lumber vein; L2, the second lumber vein; L3, the third lumber vein; MSA, middle suprarenal artery; RLRV, retroaortic left renal vein; RRA, right renal artery.

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kidneys, the left and right supracardinal veins form an DISCUSSION anastomosis between the azygos and hemiazygos veins. The RV is normally a large vein and runs trans- In the area around the kidney, the supracardinal-sub- versely in front of the renal artery. The left RV is longer cardinal veins anastomose and the left and right supra- than the right RV and runs just inferior to the origin of cardinal venous anastomosis is formed. Caudal to the the superior mesenteric artery anterior to the AA. The kidney, the left subcardinal vein disappears and the left testicular (or ovarian), left inferior phrenic, and right subcardinal vein becomes part of the IVC [8]. left suprarenal veins drain into the left RV. The left RV The renal collar in this case consisted of the three drains into the IVC at a higher position than the right different venous anastomoses described above sur- one because the left kidney is slightly higher than the rounding the descending aorta, namely the left and right kidney. The right RV is shorter and wider than right subcardinal venous anastomosis on the ventral the left RV and the descending part of the duodenum side of the aorta, the left and right supracardinal venous crosses in front of the right RV. The RV occasionally anastomosis on the dorsal side, and the ipsilateral sup- has other tributaries that include a communicating racardinal-subcardinal venous anastomosis on both tributary and origin of the azygos vein [1]. sides. The vein formed by the remnant of the left and The RV has fewer variations than the renal artery. right subcardinal venous anastomosis ventral to the The right RV has been found to have one to three ac- abdominal aorta is the normal left vein. The retroaortic cessory veins and the left RV may have one or two left RV in the present case is considered to be a remnt- accessory veins. In addition, the left RV forms a ret- ant of the anastomosis between the left and right sup- roaortic left RV and circumaortic left RV when it trav- racardinal veins dorsal to the abdominal aorta. Hoeltl els dorsal to the AA. Also, the left RV may anastomose et al. [9] classified RLRV into two types; type I has a with the splenic vein and receive the lumbar veins [2]. single retroaortic but orthotopic left renal vein, type II Detailed anatomical reports describing a retroaor- has a single retroaortic left renal vein which lies at the tic left renal vein are rare. The reported prevalences of level of L4 to L5 and joins the testicular (or ovarian) retroaortic left RV were 1.8% (5/270) [3], 2%(2/100) and ascending lumber veins to drain the left kidney. The [4], 2.1%(3/176) [5], 2.4% (12/500) [6], 3.4%(7/202) present case was classified as type I. When both the [7]. Based on these reports, a retroaortic left RV is dorsal and ventral anastomosis remains, the left RV seen in approximately 2% of individuals. runs on both the dorsal and ventral sides of the aorta. Embryologically, the venous system consists of Various clinical problems have been reported in as- the right and left cardinal veins. The anterior cardinal sociation with a retroaortic left RV, such as Nutcracker vein drains blood from above the heart and the poste- phenomenon, which might result in macroscopic or rior cardinal vein drains blood caudal to the heart. microscopic hematuria and abdominal pain [10, 11, 12]. Those two veins join to become the common cardinal There is also a report on the risk of damaging the RLRV vein and drain into the heart. The IVC is formed by during abdominal aortic aneurysm surgery [13, 14]. transformation of the posterior cardinal vein, and sub- Therefore, further anatomical studies for this variation cardinal and supracardinal veins which appear later. are needed. The posterior cardinal vein develops as the vein of the mesonephros, which atrophies with the mesonephros, CONCLUSION and then disappears except for the common iliac vein and the junction of the superior vena cava (SVC) with We report a case of RLRV. This variation is due to the azygos vein. The right and left subcardinal veins a remnant of the anastomosis between the left and right run parallel and mesioventral to the posterior cardinal supracardinal veins dorsal to the aorta with regression vein and flow into the posterior cardinal vein, which of the anastomosis between the left subcardinal veins also communicates with the ipsilateral posterior cardi- ventral to the aorta. This variation might result in he- nal vein through sinusoidal capillaries of the mesone- maturia and could be at risk of injury during abdomi- phros. The right and left subcardinal veins anastomose nal operations such as abdominal aortic aneurysm sur- to become the left RV, the other part of the subcardinal gery. vein becomes the right RV, part of the IVC, the supra- renal vein, and testicular (ovarian) vein. In addition, the ACKNOWLEDGEMENT: The authors wish to thank the indi- supracardinal vein runs parallel and mesiodorsal to the viduals who donated their bodies for the advancement of edu- posterior cardinal vein, flows into the posterior cardi- cation and research. nal vein as well as the subcardinal vein. Superior to the

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REFERENCES 8. Arey LB. Developmental anatomy: a textbook and labora- tory manual of embryology. 7th Ed. WB Saunders. 1. Clement CD. Gray’s anatomy of the human body. American Philadelphia and London 1966, pp360-368. Ed. 1985; 30:835-836. 9. Hoeltl W, Hruby W, and Aharinejad S. Renal vein anatomy 2. Tubbs RS, Loukas M, and Shoja MM (eds). Bergman’s and its implicatios for retroperitoneal surgery. J Urol. 1990; comprehensive encyclopedia of human anatomic variation. 143:1108-1114. John Wiley & Sons; 2016 Jul 12. 10. Nam JK, Park SW, Lee SD, and Chung MK. The clinical 3. Davis Jr CJ, and Lundberg GD. Retroaortic left renal vein: significance of a ret-roaortic left renal vein. Korean J Urol. a relatively frequent anomaly. Am J Clin Pathol. 1968; 2010; 51:276-280. 50:700-703. 11. Karaman B, Koplay M, Özturk E, Basekim CC, Ogul H et 4. Davis RA, Milloy Jr FJ, and Anson BJ. Lumbar, renal, and al. Retroaortic left renal vein: multidetector computed to- associated parie-tal and visceral veins based upon a study mography angiography findings and its clinical impor- of 100 specimens. Surg Gynecol Obstet. 1958; 107:1-22. tance. Acta Radiol. 2007; 48:355-360. 5. Seib GA. The azygos system of veins in American whites 12. Calàbria HC, Gómez SQ, Cerqueda CS, de la Presa RB, and American negroes, including observations on the infe- Miranda A et al. Nutcracker or left renal vein compression rior caval venous system. Am J Phys Anthropol. 1934; phenomenon: multidetector computed tomography findings 19:39-163. and clinical significance. Euro Radiol. 2005; 15:1745-1751. 6. Reis RH, and Esenther G. Variations in the pattern of renal 13. Shindo S, Kubota K, Kojima A, Iyori K, Ishimoto T et al. vessels and their relation to the type of posterior vena cava Anomalies of inferior vena cava and left renal vein: risks in in man. Dev Dyn. 1959; 104:295-318. aortic surgery. Ann Vasc Surg. 2000; 14:393-396. 7. Pick JW, and Anson BJ. The Renal Vascular Pedicle: An 14. Karkos CD, Bruce IA, Thomson GJ, and Lambert ME. Anatomical Study of 430 Body-Halves1. J Urol. 1940; Retroaortic left renal vein and its implications in abdomi- 44:411-434. nal aortic surgery. Ann Vasc Surg. 2001; 15:703-708.

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