2008 THE AUTHORS . JOURNAL COMPILATION 2008 BJU INTERNATIONAL Reconstructive and Paediatric OF THE CARRERA

et al.

Arteries of the scrotum: a microvascular study and its application to urethral reconstruction with scrotal flaps BJUIBJU INTERNATIONAL Anna Carrera, Alfredo Gil-Vernet*, Pau Forcada, Rosa Morro, Manuel Llusa and Octavio Arango† Department of Human , Faculty of Medicine, University of Barcelona, * Department of Urology, Centro Médico Teknon, and †Department of Urology, Hospital del Mar, Barcelona, Spain Accepted for publication 10 July 2008

cases to evaluate the number, distribution branches of two main scrotal arteries which Study Type – Aetiology (case series) and anastomosis of the cutaneous arteries are a continuation of the perineal arteries Level of Evidence 4 of the scrotum. and which access via the posterior face, running deeply on both sides of the septum. OBJECTIVE RESULTS CONCLUSIONS To study scrotal microvascularization and Scrotal skin is irrigated by two main vascular apply the findings to the design of reliable systems, through the inferior external The special anatomical distribution of scrotal skin flaps for reconstructive surgery of and the perineal arteries, branches stemming from perineal arteries complex urethral or panurethral stenoses. which branch into multiple scrotal arteries. enables the construction of adequate reliable These arteries are distributed in three longitudinal median island scrotal flaps for MATERIALS AND METHODS cutaneous territories, two lateral and one the reconstructive surgery of panurethral central, which are widely inter-anastomosed. stenosis, as profuse axial vascularization is In 15 cryopreserved male cadavers, scrotal Each lateral territory receives an inferior ensured. skin vascularization was explored using external pudendal which accesses macro- and microdissections, and the scrotal at the midpoint of the scrotal root and fans KEYWORDS sac made transparent using the Spalteholtz out to cover the entire corresponding method. A meticulous descriptive analysis of hemiscrotum. The central cutaneous arteries, blood supply, scrotum, surgical the arterial network was conducted out in all territory is vascularized through the flaps, urethral stricture,

INTRODUCTION scrotum and apply the findings to improving To evaluate specific characteristics, the results of complex urethral surgery. disposition and anastomosis of the In any reconstructive surgery, axial flaps are skin arteries, the scrotum was made more reliable than grafts, as the blood supply transparent using the Spalteholtz is always guaranteed when vascular MATERIALS AND METHODS technique [11] in which tissue is cleared continuity is well preserved [1]. Many penile by alcohol dehydration and impregnation and scrotal skin flaps to reconstruct complex Fifteen cadavers of men aged 53–92 years, with benzyl benzoate/methyl salicylate urethral stenosis have been described, but cryopreserved and with arterial black latex mixture. Sections were made in the frontal or most were not supported by previous injected through the internal and external sagittal planes in some of these preparations microvascular studies, which could explain iliac arteries, were studied using a to attain better visualization of the vascular their variable outcomes. combination of different techniques. disposition. The bilateral inguinal regions and the Scrotal skin is well vascularized due to the perineoscrotal area were dissected to identify confluence of two main arterial systems, the origin of the main arterial vessels that RESULTS the external iliac and the internal iliac, as vascularize the scrotum. described in classic anatomical texts and Scrotal blood supply from the external iliac atlases [2–7], and specialized books and texts Microdissections of scrotal cutaneous arteries system: Two external pudendal arteries on microvascular anatomy [8–10]; however, using magnifying lenses (×2.5) were carried (superior and inferior) were found stemming recent and well-detailed descriptions are out from inside and outside the scrotal wall, from the at a mean distance of scarce or unavailable. Our aim was to study with each layer identified and raised 5 cm below the inguinal ligament in 95% of the arterial microvascular distribution of the successively. cases. One arterial trunk dividing into these

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FIG. 1. Dissection of the inguinal region. 1. Femoral FIG. 2. Spalteholtz technique. A, Lateral view of FIG. 3. Landmarks of the emergence point of the artery. 2. Superior external pudendal artery. 3. scrotal sac. Scrotal arteries are long, tortuous and (lithotomy position). A, As indicated Inferior external pudendal artery. 4. Femoral . 5. follow a descending course in scrotal layers. They with the red ellipse, 75% of perineal arteries emerge Great saphenous vein. 6. Inguinal ligament. fan out into branches emerging at acute angle from at the middle third of the line between median raphe the main trunk. B, Superior view of the scrotal sac and . The remaining arteries after removing the testes. Anastomosis is visible emerge in the lateral third of this line but with a between great branches of scrotal vascularization clear tendency to move away from the ischial from the external iliac and internal iliac systems. 1. tuberosity, as indicated by the green circle. B, Inferior external pudendal artery. 2. Great branch of Dissection of the course of perineal arteries to the perineal artery. 3. Corpus spongiosum. scrotum. During their course, these arteries give off branches towards neighbouring anatomical A structures. In the root of the scrotum, both perineal arteries are attached to the septum. 1. Perineal artery. 2. Superficial transverse perineal muscle. 3. . 4. .

A

two branches was found in 65% of cases B (Fig. 1).

Scrotal vascularization was exclusively through branches of the inferior external pudendal artery in 89.5% of cases. Both external pudendal arteries or a single external pudendal artery were responsible for scrotal blood supply in the remaining cases. These arteries enter the scrotal sac laterally at the mid-point of its base or root, then B bifurcate and are distributed throughout the entirety of the skin of each hemi-scrotum (Fig. 2).

Scrotal blood supply from the internal iliac system: A perineal artery (superficial perineal artery) branching from the was located bilaterally in the perineal muscles (Fig. 3). At the root of the scrotum, area in all cases. All these vessels gain access each perineal artery splits into fine branches in the perineal region, perforating the perineal that are distributed in the skin of this area, membrane in the triangular space formed and a main branch, of larger diameter, which in front of the superficial transverse continues a deep course towards the interior muscle of the , and between the of the scrotal sac (Fig. 4). This main branch ischiocavernosus and bulbospongiosus runs ventrally along the urethral corpus muscles. This emergence point was found spongiosum at each side of the scrotal at a mean distance of 1.9 cm lateral to the septum insertion, following an anterior median , along the line joining direction, and branching out into several the two ischial tuberosities passing through arteries that descend obliquely over the the anterior margin of the anal orifice. In septum (Fig. 5). When these septal arteries depth, the arterial emergence point was at a reach the superficial end of the septum, they mean of 4.5 cm from the cutaneous surface. turn towards the skin of each hemiscrotum at Both superficial perineal arteries traced an the median line where they are distributed anterosuperior route towards the rear face (Figs 6,7). supplementary irrigation from a lateral of the scrotum (lithotomy position), being artery originating in the medial femoral located deep in the space between the In addition, in 70% of cases the skin of the circumflex artery (83% of cases) or in ischiocavernosus and bulbospongiosus superolateral region of the scrotum had the (17%). There were

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FIG. 4. The great branch of the perineal artery only gives off small, scant branches to the skin of the scrotal FIG. 5. A, Internal microdissection of scrotal sac. The root. A, Microdissection of the posterior aspect of the scrotum (lithotomy position). All the skin has been and skin are in the same plane. removed laterally to the scrotal raphe. B, Spalteholtz technique. Posterior view of the scrotum. C, Spalteholtz Scrotal arteries run at different levels of the technique. Frontal section and internal view of the posterior aspect of the left hemiscrotum. 1. Great branch subcutaneous tissue of the scrotum. B, of perineal artery on its route inside scrotal sac. 2. Branches of perineal artery to the skin of the scrotal root. Transillumination of scrotal septum in the internal 3. Scrotal septum. 4. Corpus spongiosum. 5. Skin. microdissection of the scrotal sac. C, Spalteholtz technique and frontal section of scrotum. The A B scrotal septum has two arterial planes with fine, scant communications between them. 1. Great branch of perineal artery. 2. Septal arteries. 3. Branches from inferior external pudendal artery. 4. Corpus spongiosum. 5. Scrotal septum.

A

C

B

anastomoses between the arteries of each suitability and reliability. As classically C scrotal vascular region. described, scrotal skin has a dual blood supply through branches from the external and internal iliac systems, respectively, distributed DISCUSSION in anterior and posterior faces of the scrotum [2,3,8]. However, our results show The use of scrotal and penile skin flaps in the existence of three cutaneous territories; reconstructive surgery of bulbar urethral two lateral and one central (Fig. 8). Classically stenosis has declined since the advent of and in recent texts, perineal arteries were free buccal mucosa grafts. However, there considered to only irrigate the posterior are cases of complex bulbar stenosis (very face of the scrotum [9,10,16]; however, extensive, multi-operated and with chronic the present study showed that all the skin urinary infection) or panurethral disease in from the scrotal midline to its insertion which reconstruction with a scrotal skin into the mid penile raphe receives its Regarding the exit point of these arteries in flap is an option to be considered before a vascularization via the perineal arteries and the perineal region, incisions at the base of a definitive perineal urethrostomy. their branches. flap of the scrotal midline must move away laterally from ischial tuberosities to avoid Different urethroplasty techniques with Understanding of the exact anatomical injury. Fortunately, the characteristic deep exit scrotal flaps have been described [12–16]; location of these vessels is necessary to site of both perineal arteries prevents them however, the design of most was based on ensure their inclusion in the skin flap and from being injured in their main trunk when a the understanding of classical anatomy avoid surgical manoeuvres that could harm superficial skin incision is made. and not on microvascular studies, which them. In this respect, several surgical might support the existence of axial-type landmarks should be considered throughout To ensure inclusion in the scrotal flap of vascularization and thus assure their their route. the main trunk of both perineal arteries

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FIG. 6. Spalteholtz technique. A, Cutaneous surface of the scrotal midline. B,C, Frontal section of the scrotal FIG. 7. Spalteholtz technique. Inferior view of septum and midline skin. Anastomoses are visible between vessels from septal arteries and vessels from scrotum. Anastomoses are apparent among the inferior external pudendal artery. There are many vessels in the midline skin of the scrotum. 1. Septal arteries. arterial territories of the scrotum. 1. Branches from 2. Branches from inferior external pudendal artery. 3. Septum. inferior external pudendal artery. 2. Branches from septal arteries. AB

C

FIG. 8. Vascular scrotal territories. Branches from inferior external pudendal artery (in red) and branches from septal arteries (in orange). A, Anterior face of scrotum. B, Posterior face of scrotum.

situated between the ischiocavernosus can be adequately designed in length and and bulbospongiosus muscles, it will be width without their vascularization being necessary to raise them within the plane of compromised. the of these muscles or, even more safely, subfascially, while taking special care in As the median line of scrotal skin, on the the intermuscular space, as indicated in a posterior and anterior faces, depends on perineally based scrotal flap urethroplasty vascularization through perineal arteries, [15]. posterior scrotal midline flaps are not limited several authors [8–10], permits the design in length and could be raised, with no risk, up of flaps of the scrotal central line with The particular ventral route of both to the anterior face of the scrotum. Thus, this variable amplitude, without endangering perineal arteries with respect to the corpus permits long cutaneous island flaps to be the vascularization of their lateral zones. spongiosum of the and exit of obtained that can be moved and sutured free its branches towards the scrotal septum, from tension. Finally, direct connections between the advocate the routine inclusion of the septum arteries of the right- and left-hand sides at in scrotal flap construction, and thus preserve Confirmation of the existence of anastomosis the level of the scrotal skin of the median line this important vascularization. However, between the arteries of the two lateral arterial could ensure vascularization of the whole flap anatomical findings have shown that territories with a central territory, forming in the event of lesions to the vascular supply perineally based flaps of the scrotal midline a true scrotal network as described by of one of the sides of the septum.

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Some authors have described flaps for the base of the ) and variable width, System, Vol. 8, Part I. Philadelphia: WB complex urethral reconstruction based on the thereby guaranteeing axial vascularization. Saunders, 1988 distribution of perineal artery branches in The surgical execution of these flaps must 8 Salmon M. Arteries of the Skin. Taylor GI other territories [14,16,17] or exclusively on respect certain important surgical landmarks ed. London: Churchill Livingstone, 1988 the septal blood supply [13]. Without doubt, and preferentially include the septum. 9 Cormack GC, Lamberty GH. The Arterial according to our results, a raised flap in the Anatomy of Skin Flaps, 2nd edn. London: posterolateral scrotal skin is vascularized by Churchill Livingstone, 1994 fine branches of the ipsilateral perineal artery ACKNOWLEDGEMENTS 10 Quartey JKM. Microcirculation of penile that are distributed in the area. Such a flap and scrotal skin. Atlas Urol Clin N Am must be considered as a ‘random’ flap, The authors thank Christine O’Hara for 1997; 5: 1–9 given that it will remain nourished through valuable help with the English version of the 11 Culling CF. Handbook of arterial interconnections of the , but manuscript. Histopathological and Histochemical will not count on an axial vessel making its Techniques (Including Museum vascularization totally predictable. Septum Techniques), 3rd edn. London: pedicled scrotal skin flaps are randomly CONFLICT OF INTEREST Butterworth, 1974 vascularized by fine septal arteries that can be 12 Blandy JP, Singh M. The technique and easily damaged when surgical incisions are None. results of one-stage island patch deepened in the scrotal septum to obtain an urethroplasty. Br J Urol 1975; 47: 83–7 adequate mobilization of the flap. 13 Yachia D. A new, one-stage pedicled REFERENCES scrotal skin graft urethroplasty. J Urol In no case did we find a distribution of 1986; 136: 589–92 perineal artery branches in the superficial 1 McGregor IA, Morgan G. Axial and 14 Gattegno B, Cohen L, Coloby P et al. Le fascia of the internal laterally random pattern flaps. Br J Plast Surg traitement des sténoses de l’urètre par contiguous to the inguinal fold, as described 1973; 26: 202–13 patch pédiculé de peau scrotale. Ann Urol in diagrams of a urethroplasty technique for 2 Rouvière H, Delmas A. Anatomía 1990; 24: 43–7 complex cases [16,17]. Humana, 10th edn, Vol. II. Barcelona: 15 Gil-Vernet JM, Arango O, Gil-Vernet A, Masson, 1999 Gil-Vernet JM Jr, Gelabert-Mas A. A In conclusion, the scrotum receives a good 3 Testut L, Latarjet A. Anatomía new biaxial epilated scrotal flap for arterial supply from two main arterial Humana, 8th edn, Vol. II/IV. Barcelona: reconstructive urethral surgery. J Urol systems that determine the existence of Salvat, 1940 1997; 158: 412–20 three cutaneous territories; two lateral, each 4 Gray H, Bannister LH, Berry MM, 16 Jordan GH. Scrotal and perineal flaps for dependent on an inferior external pudendal Williams PL. Gray’s Anatomy. The anterior urethral reconstruction. Urol Clin artery, and one central, dependent on perineal Anatomical Basis of Medicine and N Am 2002; 29: 411–6 arteries, which includes the anterior and Surgery, 38th edn. London: Churchill 17 Zinman L. Perineal artery axial posterior faces and the septum. The three Livingstone, 1995 fasciocutaneous flap in urethral territories are widely interconnected by a 5 Pernkopf E. Atlas of Topographical and reconstruction. Atlas Urol Clin N Am 1997; veritable scrotal arterial network. Applied Human Anatomy, 3rd edn. 5: 91–108 Baltimore: Williams & Wilkins, 1989 Microvascular anatomical study of the 6 Moore KL, Dalley AF. Clinically Oriented Correspondence: Anna Carrera Burgaya, distribution of scrotal branches of the Anatomy, 5th edn. Philadelphia: Department of Human Anatomy, Faculty of perineal artery permits the design of Lippincott, Williams & Wilkins, 2005 Medicine, University of Barcelona, Calle skin flaps of the central scrotal territory, 7 Netter FH. The Netter Collection of Casanova, 143, 08034 Barcelona, Spain. sufficiently long (from the scrotal root to Medical Illustrations – Musculoskeletal e-mail: [email protected]

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