Human testicular arterial supply: gross anatomy, corrosion cast, and radiologic study
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1 Human testicular arterial supply: gross anatomy, corrosion cast, and radiologic study Taymour Mostafa, M.D., a Ibrahim Labib, M.D., b Yasser El-Khayat, M.D., a Abd El-Rahman El-Shahat, M.D., b and Amr Gadallah, M.D. a a Department of Andrology & Sexology and b Department of Anatomy, Faculty of Medicine, Cairo University, Cairo, Egypt Objective: To study human testicular arterial supply. Design: Prospective. Setting: Academic setting. Patient(s): Forty fresh male cadavers. Intervention(s): Gross anatomy of 20 cadavers, corrosion casting of 10, and radiography of 10. Main Outcome Measure(s): Testicular vascular supply, course, branching, and anastomosis. Result(s): The testicular artery descends bilaterally in a straight course (85%) and in a convoluted course (15%). There were three sites of terminations: along the upper pole of the mediastinum testis (78.8%), giving terminal branches (16.2%) or descends without division (5%). Four patterns of termination were found, but in the majority (69.7%) it terminates as upper and lower polar branches. The cremasteric artery arises from the inferior epigastric artery and terminates close to the lower end of the testis, anastomosing with the lower polar branch of the testicular artery. The artery of the vas arises from the inferior vesical artery, terminates by several capsular branches close to the mediastinum testis, anastomosing with branches of the testicular artery along the mediastinum testis. Conclusion(s): The testis gets its arterial supply mainly from the testicular artery supplemented with the cremastric artery and the artery of the vas. The testis has rich vascular areas in the upper polar, mediastinum testis, and posterolateral segments. (Fertil Steril Ò 2008;90: Ó2008 by American Society for Reproductive Medicine.) Key Words: Testis, testicular artery, corrosion cast, cremasteric artery, anatomy Many investigators described the arterial testicular vasculature, as a result we have an idea about the variability of the testicular artery regarding its origin, course, and modes of termination (1). Although the arterial supply of the human testis, through the testicular artery, is a well-studied subject, the approach that this vessel takes when reaching the testis is not as well described (2). The distribution and the anastomosis of the cremasteric artery and the artery of the vas, which supply the testis, with the testicular artery have also been described. At present, testicular surgical procedures requiring extensive testicular biopsies are the procedure of choice to get precious sperms from some patients with nonobstructive azoospermia to carry out intracytoplasmic sperm injection (ICSI). Testicular biopsy is far from an innocuous procedure; it has the potential to cause permanent damage of spermatogenesis with reported side effects of hematoma, linear scars, and later calcifications (3). Therefore, an understanding of the testicular blood supply is necessary for the efficient function of the organ, to define areas of poor vascular anastomosis that could result from testicular surgery and avoid deliberate or inadvertent ligature of the testicular artery in orchiopexy, herniorrhaphy, or ligation for varicocele (4). Received August 3, 2007; revised October 11, 2007; accepted October 16, Reprint requests: Taymour Mostafa, M.D., Andrology & Sexology Department, Faculty of Medicine, Cairo University, Cairo 11562, Egypt. ( taymour1155@link.net). This work aimed to study the human testicular arterial supply by different methods to assess the course, variations, and sites of anastomosis. MATERIALS AND METHODS Gross Anatomy of the Testicular Vasculature Twenty fresh adult human cadavers (aged years) were subjected to gross anatomical dissection of the testicular vasculature after Institutional Review Board (IRB) approval. Through an inguinoscrotal incision on both sides of each cadaver, the spermatic cord and its related testis were exposed to identify the testicular artery, the vas deferens, and related venous plexus. The anatomy of the testicular artery its course, termination, sites of division and branching was recorded and photographed. Then, the anterior abdominal wall was incised; all abdominal viscera with their mesenteries were removed to explore the posterior abdominal wall. Testicular arteries were traced from their origin to their exit from the deep inguinal rings. Variations in origin, course, and branches were recorded. Injection Corrosion Study Vascular corrosion casts were used to observe the minute features of blood vessels and their three-dimensional structures (5). Testicular arteries were dissected and explored in 20 adult testes and then cannulated. The renal, femoral, and all 2226 Fertility and Sterility â Vol. 90, No. 6, December /08/$34.00 Copyright ª2008 American Society for Reproductive Medicine, Published by Elsevier Inc. doi: /j.fertnstert
2 branches of the internal iliac arteries were ligated, except for the inferior vesical arteries. Through the cannula, the vessels were washed with physiological saline and then injected with a plastic resin (Astralon; Aldcroft Adhesives, Ltd., Bolton, UK) under a continuous sustained gentle pressure ( mm Hg). Injected specimens were excised and refrigerated for 24 hours at 4 C, then the specimens were subjected for subsequent corrosion in 50% HCl for 24 hours. The remnants were washed under gentle tap water to avoid destruction of the arterial tree casts, and then photographed. Radiographic Study Twenty testes were injected with a 40% barium sulfate suspension under controlled pressure ( mm Hg) through the testicular artery. Injected areas were radiographed and the sites of division, mode of termination, extratesticular or intratesticular branches, and sites of anastomosis with other arteries of the testicular arteries were recorded and photographed. RESULTS Testicular Artery In all dissected cases (n ¼ 20), the testicular artery originates directly from the abdominal aorta at L2 L3 just below the origin of the renal arteries descending in a straight course to its termination in 17/20 cases (85%). In 3/20 cases (15%), it showed a slight or marked convoluted course. Testicular arteries on both sides descend superficial to the psoas major muscles, ureters, and genitofemoral nerve, and then pass to the deep inguinal ring to enter the spermatic cord. There were three sites at which the testicular artery terminates. 1. In the majority of cases (63/80 testes, 78.8%), it terminated close to mediastinum testis; descended along the entire length of the mediastinum testis (46/63 testes) and terminated at the upper end of mediastinum testis close to the upper pole (17/63 testes). 2. In 13/80 testes (16.2%), its terminal branches were either 3 4 cm from the upper end of the testis or 4 8 cm from the mediastinum testis. 3. In 4/80 testes (5.0%), it descended without division along the mediastinum testis. [2] 12/76 cases, 15.8%, the upper polar branch, middle segmental branch near the middle of the mediastinum testis then continued to the lower end of the testis supplying it and the epididymis then it recoursed upward and forward (Fig. 2). [3] 6/76 cases, 7.9%, it descended along the mediastinum testis giving three extratesticular terminal branches: upper polar or segmental, middle segmental, and lower polar or segmental branches; each gave many centripetal branches supplying the testis from behind forward. [4] 5/76 cases, 6.6%, it gave out an upper polar branch before reaching the upper pole of the testis then continued along the mediastinum testis to reach the lower end of the testis and recoursed forward and upward to supply its anterolateral part. The most terminal part of the testicular artery anastomosed with branches from the cremasteric artery. In other cases, the artery did not divide (4/80, 5.0%), descending straight or wavy along the mediastinum testis without extratesticular terminal branches. Many centripetal branches originated directly from it to supply the testis, epididymis, and vas deferens. Cremasteric Artery The cremasteric artery arose from the inferior epigastric artery close to the deep inguinal ring to enter the inguinal canal supplying the cremasteric contents. It terminated with FIGURE 1 Dissected right testis (S) and its spermatic cord showing the first pattern (69.7%) of testicular artery (T) termination with upper polar (U) and lower polar (L) branches. D ¼ vas deferens; PV ¼ venous plexus. Patterns of Testicular Artery Termination The testicular artery has one to three branches of different calibers (most commonly upper and lower pole) that exhibited four different patterns (n ¼ 76): [1] 53/76 cases, 69.7%, two main terminal branches; upper polar (segmental) branch directed toward the upper anterior aspect of the testis and a lower polar (segmental) branch directed toward its lower posterior aspect. In 80% of this pattern the lower polar branch gave branches anastomosing with branches from the cremasteric artery. In 20%, each upper and lower polar branch anastomosed with the cremasteric artery (Fig. 1). Fertility and Sterility â 2227
3 FIGURE 2 Plastic cast of second pattern of testicular artery (15.8%) with single upper polar (U) branch and then descends by itself (long arrow). FIGURE 3 Schematic diagram showing intensity of arterial supply according to casting (lateral view). branches close to the lower end of the testis, anastomosing either with the lower polar branch of the testicular artery in 80% of the first pattern, with upper and lower segmental branches in 20% of the first pattern, or with branches that arise directly from the lower end of the artery in the fourth pattern. Artery of the Vas (deferential) The artery of the vas arose as a branch from the inferior vesical artery giving several branches to supply the vas deferens along its course and terminated by giving several capsular branches close to the mediastinum testis. Vasal branches anastomosed freely with branches of the testicular artery along the mediastinum testis close to the lower end of the testis. The current work could classify the testis into the vascular areas (Fig. 3). 1. Rich vascular areas: upper polar, mediastinum testis, and posterolateral segments. 2. Moderate vascular areas: middle third of the lateral surfaces. 3. Poor vascular areas: anterior border and anterolateral surfaces. DISCUSSION In the present study the testicular arteries originated directly from the abdominal aorta at the level of L2 L3, just below the renal arteries passing down to the testis bilaterally either in a straight course in the majority of cases or in a variable, convoluted course in the remainder of the cases. Many investigators (6 9) reported that the right testicular artery lies anterior to the inferior vena cava and posterior to the third part of the duodenum, right colic, ileocolic arteries, root of mesentery, and the terminal part of the ileum. The left testicular artery lies posterior to the inferior mesenteric vein, left colic artery, and the lower part of the descending colon. They cross anteriorly to the genitofemoral nerve, the ureter, and the lower part of the external iliac artery, passing to the deep inguinal ring to enter the spermatic cord. Terayama et al. (5) showed that the testicular arteries run from the abdominal aorta to the testes, with various configurations (straight, meandering, spiral, or coiled). They suggested that these configurations may play several roles in protecting normal spermatogenesis, such as allowing wide mobility of the testes on physical attack, heat emission with the entangled pampiniform plexus, and reduction of the blood flow rate. Different researchers (10 13) described abnormal variations of the testicular artery course, origin, or number. In less than 20% of cases, it passes behind the inferior vena cava and in 12% it arches over the renal vein (14, 15). Loukas and Stewart (16) reported an accessory left testicular artery originating from the ventrolateral wall of the descending aorta communicating with the left renal artery in addition to the normal right and left testicular arteries. Deepthinath et al. (17) reported extratesticular arteries. Bhaskar et al. (18) reported an abnormal course and branching of the right testicular artery arising from the anterior surface of the abdominal aorta dividing into two branches: one coursed inferiorly behind the inferior vena cava as the 2228 Mostafa et al. Testicular arterial supply Vol. 90, No. 6, December 2008
4 testicular artery proper, whereas the other passed behind it emerging on the anterior surface of the right kidney. After crossing, it bifurcated into an ascending branch to the right suprarenal gland and a descending branch ending in the posterior abdominal wall. Naito et al. (19) reported two cases of the left testicular artery arching over the left renal vein before running downward to the testis. Mano et al. (20) indicated that even with insitus inversus, testicular vessels did not exhibit an inverted morphology. Rusu (21) associated anatomical variants with the bilateral doubled testicular arteries: the right side the medial testicular artery emerged from abdominal aorta, whereas the lateral one arised from the superior renal artery. On the left side, both arteries emerged as a common trunk from the abdominal aorta. We described three main sites of division of testicular arteries and four patterns of its terminations. The first pattern is in agreement with Cooper (22), demonstrating its division into two branches one passing to the upper and anterior part of the testicle and the other to its posterior and lower part. Hill (23) reported its division into two branches at the mediastinum testis. Harrison and Barclay (24) described its division into two branches, but they added that these branches passed in various directions over the free surface of the testis toward the mediastinum testis. Williams et al. (8) and McMinn (9) considered that the commonest pattern of the testicular artery showed little or no convolutions and gave branches to both the spermatic cord and the epididymis before dividing into two terminal branches. Our results were in contradiction with Cooper (22), Hill (23), Harrison and Barclay (24), Williams et al. (8), and McMinn (9), who described only one pattern. Regardless of the patterns of distribution of the testicular artery, the testis seems to be supplied always by centripetal branches that arise either from the terminal branches of the testicular artery or from the testicular artery itself, as shown by corrosion casting. These branches penetrate deeply into the substance of the testis, agreeing with Cordier et al. (25), Kormano (26), Kormano and Suoranta (7, 27), and McMinn (9). On the other hand, Corner and Nitch (28) showed that the testicular artery enters the testis through its mediastinum and not from the surface. Our findings postulated that the artery of the vas and the cremasteric artery are minor additional arterial supply of the human testis. Harrison (29) in his study indicated that the sum of the diameters of the cremasteric and vasal arteries was at least equal to the diameter of the testicular artery. Yalcin et al. (30) demonstrated that all the testes, including the undescended one, had testicular, deferential, and cremasteric arteries with arterial diameters of 1.7, 1.1, and 0.5 mm, respectively, with clear anastomotic channels between testicular and deferential arteries in both normal and undescended conditions. According to the distributions, terminations, and anastomosis, corrosion casts showed that the testis has its arterial supply mainly from testicular artery supplemented with both the cremastric artery and the artery of the vas deferens. Rich vascular areas were located in its upper pole, lower pole, mediastinum testis, and the postero-lateral aspects. These areas should be looked for to avoid side effects during extra-testicular surgical procedures as well as extensive testicular biopsies. REFERENCES 1. Skowronski A, Jedrzejewski K. The human testicular artery and the pampiniform plexus where is the connection? Folia Morphol (Warsz) 2003;62: Pais D, Fontoura P, Esperanca-Pina JA. The transmediastinal arteries of the human testis: an anatomical study. Surg Radiol Anat 2004;26: Amer M, Ateyah A, Hany R, Zohdy W. Prospective comparative study between microsurgical and conventional testicular sperm extraction in nonobstructive azoospermia: follow-up by serial ultrasound examination. Hum Reprod 2000;15: Asala S, Chaudhary SC, Masumbuko Kahambo N, Bidmos M. Anatomical variations in the human testicular blood vessels. Ann Nat 2001;138: Terayama H, Naito M, Nakamura Y, Iimura A, Itoh M, Tamatsu Y, et al. Corrosion casts of convoluted testicular arteries in mice and rats. Arch Androl 2005;5: Hundeiker M, Keller L. Die Gefassarchitektur des Mesenchlichen Hodens. Morph J 1963;105: Kormano M, Suoranta H. An angiographic study of the arterial pattern of the human testis. Anat Anz 1971;128: Williams PL, Berry MM, Collins P, Dyson M, Dussek JE, Ferguson MWJ, et al. Gray s anatomy. 38th ed. Edinburgh: Churchill Livingstone, McMinn RML. Last s anatomy, regional and applied. 9th ed. Edinburgh: Churchill Livingstone, Merklin RJ, Michels NA. The variant renal and suprarenal blood supply with data on the inferior phrenic, ureteral and gonadal arteries: a statistical analysis based on 185 dissections and review of the literature. J Int Coll Surg 1958;29: Nathan H, Tobias PV, Wellsted MD. An unusual case of right and left testicular arteries arching over the left renal vein. Br J Urol 1976;48: Onderoglu S, Yuksel M, Arik Z. Unusual branching and course of the testicular artery. Ann Anat 1993;175: Ozan H, Gumusalan Y, Onderoglu S, Simsek C. High origin of gonadal arteries associated with other variations. Ann Anat 1995;177: Notkovich H. Testicular artery arching over renal vein: clinical and pathological considerations with special reference to varicocele. Br J Urol 1955;27: Mirapeix RM, Sa~nudo JR, Ferreira B, Domenech-Mateu JM. A retrocaval right testicular artery passing through a hiatus in a bifid right renal vein. J Anat 1996;189: Loukas M, Stewart D. A case of an accessory testicular artery. Folia Morphol (Warsz) 2004;63: Deepthinath R, Satheesha Nayak B, Mehta RB, Bhat S, Rodrigues V, et al. Multiple variations in the paired arteries of the abdominal aorta. Clin Anat 2006;19: Bhaskar PV, Bhasin V, Kumar S. Abnormal branch of the testicular artery. Clin Anat 2006;19: Naito M, Terayama H, Nakamura Y, Hayashi S, Miyaki T, Itoh M. Left testicular artery arching over the ipsilateral renal vein. Asian J Androl 2006;8: Mano Y, Adachi N, Murakami G, Yokoyama T, Dodo Y. Human situs inversus of the thoracoabdominal structures. Anat Sci Int 2006;81: Rusu MC. Human bilateral doubled renal and testicular arteries with a left testicular arterial arch around the left renal vein. Rom J Morphol Embryol 2006;47: Cooper A. On the anatomy of the testis. Observations on the structure and diseases of the testis. 1. London, UK: Longman, Hill EC. The vascularization of the human testis. Am J Anat 1909;9:463. 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5 24. Harrison RG, Barclay AE. The distribution of the testicular (internal spermatic) artery to the human testis. Brit J Urol 1948;20: Cordier P, Devos L, Delcroix A, Renier M. Variations du trajet de l artere spermatique. Annales d Anatomie Pathologique 1938;15: Kormano M. An angiographic study of the testicular vasculature in the post-natal rats. Z Anat Entwicklungsgesch 1967;126: Kormano M, Suoranta H. Microvascular organization of the adult human testis. Anat Rec 1971;170: Corner EM, Nitch CAR. The immediate and remote results of the high operation for varicocele. Brit Med J 1906;1: Harrison RG. The distribution of the vasal and cremasteric arteries to the testis and their functional importance. J Anat 1949;83: Yalcin B, Komesli GH, Ozgok Y, Ozan H. Vascular anatomy of normal and undescended testes: surgical assessment of anastomotic channels between testicular and deferential arteries. Urology 2005;66: Mostafa et al. Testicular arterial supply Vol. 90, No. 6, December 2008
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