0022-5347/04/1725-1973/0 THE JOURNAL OF UROLOGY® Copyright © 2004 by AMERICAN UROLOGICAL ASSOCIATION
Vol. 172, 1973–1976, November 2004 Printed in U.S.A.
DOI: 10.1097/01.ju.0000142131.37693.05
COMPARISON OF HYPOSPADIAC AND NORMAL PREPUTIAL VASCULAR ANATOMY SELCUK YUCEL,* EROL GUNTEKIN, ERDAL KUKUL, GUNGOR KARAGUZEL, AKIF CIFTCIOGLU, MUSTAFA MELIKOGLU AND MEHMET BAYKARA From the Departments of Urology, Pediatric Surgery and Pathology, Akdeniz University School of Medicine, Antalya, Turkey
ABSTRACT
Purpose: Data about the differences between the vascularization of normal and hypospadiac prepuce are lacking. We investigated the course of the preputial arterial blood vessels in normal controls and children with hypospadias by using transillumination, arterial methylene blue injection and 3-dimensional (3-D) reconstruction of serial histological sections focusing on arterial vessels. Materials and Methods: Prepuce of 48 normal controls and 15 children with hypospadias was transilluminated by a front and back lighting technique and then photographed. All of the normal and 12 of hypospadiac prepuces not used for urethroplasty or penile body skin reconstruction were removed. The blood vessels of normal prepuce were also identified after arterial injection of methylene blue. Selected prepuce of normal controls and children with hypospadias was serially sectioned, and arterial and venous vessels were histologically distinguished. A 3-D computer reconstruction of the arterial system of normal and hypospadiac prepuces was performed. Results: We confirmed the reliability of the transillumination technique to describe the arterial vascular anatomy of the prepuce by comparing the transillumination to methylene blue injection and 3-D reconstruction of histological sections. We classified the arterial vascular anatomy of normal prepuce as 1 artery predominant (41.67%), 2 arteries predominant (25%), H-type arching artery (12.5%) and net-like arterial system (20.83%). However, hypospadiac prepuce revealed a net-like arterial system more frequently (50%). We noted that the frequency of net-like arterial system was higher in more severe hypospadiac prepuce. Conclusions: Understanding the differences between normal and hypospadiac prepuce vascular anatomy is germane to hypospadias surgery. The arterial blood supply of the hypospadiac prepuce is different than normal. A better knowledge of the vascular anatomy of the hypospadiac prepuce may improve the surgical results of hypospadias repair. KEY WORDS: penis/blood supply, hypospadias, blood vessels/anatomy and histology
The blood supply of the hypospadiac prepuce is crucial for successful hypospadias surgery. The hypospadiac prepuce can be used for neourethra reconstruction and penile body skin closure. Well vascularized flap is the main factor for a successful outcome of hypospadias surgery. Although the severity of the hypospadias and macroscopic morphology of penis and prepuce generally determine the type of operative technique, the vascular anatomy of the prepuce is also proposed as an important factor in the decision.1, 2 The vascular anatomy of the prepuce in normal subjects has been well studied.3– 6 Surgical techniques to form preputial flaps in normal children as well as those with hypospadias are mainly dependent on these classic anatomical studies.7, 8 However, to our knowledge there are scarce data about the differences in vascular anatomy between the normal and hypospadiac prepuce.1, 2, 9, 10 Since the vascular anatomy of the normal prepuce is known, preputial vascularization in hypospadias surgery has predominantly been estimated empirically. A better understanding of the hypospadiac prepu-
tial vascular anatomy may affect hypospadias surgery outcomes, particularly when the preputial flaps are used. This study was undertaken to compare the normal preputial vascular anatomy to the hypospadiac prepuce by using transillumination, arterial methylene blue injection and 3-dimensional (3-D) reconstruction of serial histological sections with depth analysis.
MATERIAL AND METHODS
In 48 normal and 15 hypospadiac males 18 months to 9 years old (mean age 62 months) who underwent circumcision and hypospadias repair the prepuce was transilluminated by a front and back lighting technique using endoscopic cold light and photographed. Particularly, blood vessel course and development were focused. Transillumination of the preputial flap was performed in intact and degloved penis. In 48 normal and 12 hypospadiac males in whom the prepuce was not used for penile reconstruction prepuces were removed for methylene blue injection and 3-D reconstruction. During removal of the preputial flap final incision to open the circular tissue was done between the 5 and 7-o’clock positions so that the dorsal preputial tissue and its vascular supply were preserved for further study. In 1 hypospadiac and 12 normal prepuces using a 10⫻ magnification stereomicroscope, we made an incision at the level of transition of the prepuce to the penile skin, leaving the dartos fascia and blood
Accepted for publication June 18, 2004. Supported by Akdeniz University Scientific Research and Project Unit. Study was approved by committee on human research at Akdeniz University School of Medicine, Antalya, Turkey. * Correspondence: Department of Urology, Akdeniz University School of Medicine, Kampus, 07070, Antalya, Turkey (telephone: ⫹90242-227-4480; FAX: ⫹90-242-227-4482; e-mail:
[email protected]). 1973
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vessels intact. Careful dissection continued until we noted blood vessels large enough for successful cannulation. Arteries and veins were differentiated based on anatomical characteristics. The arterial wall was thicker and had an uncollapsed lumen, while the vein was thinner, collapsed, transparent and less visible. After partial dissection of the adventitia to dilate the lumen we introduced a 24 gauge plastic cannula into the predominant arteries. The arterial blood vessels were initially injected with normal saline and then with half diluted methylene blue. After injection was performed under satisfactory illumination prepuce with blue stained arterial vessels was photographed. Representative normal and hypospadiac prepuce of each vascular anatomy group was fixed in formalin, embedded in paraffin and serially sectioned at 10 microns. Sections were preserved with 2 to 4 histological sections per glass slide. Every third section was stained with hematoxylin and eosin, and arteries and veins were differentiated based on histological characteristics. As described previously, structural anatomical computer reconstruction images were created with a digital camera, SURFdriver 3.5 software (SURFdriver, University of Hawaii, Honolulu, Hawaii, and University of Alberta, Edmonton, Alberta, Canada) and a Power Macintosh G3 (Apple Computer, Inc., Cupertino, California).11 Every third to fifth section was digitized. The arteries were manually outlined and checked against the original histological sections. Three-D analysis of the localization and sizes of arteries was performed in the x and y-axes as an animated motion picture, and views of interest were captured as static images. Transillumination, methylene blue injection and 3-D reconstruction image results were compared between normal and hypospadiac prepuce. RESULTS
The results of gross examination of vessels of the prepuce in normal and hypospadiac males demonstrated subtle differences. Gross examination was not effective in distinguishing the vascularization of normal and hypospadiac specimens. The results of identification of preputial flap vascular anatomy by transillumination, arterial methylene blue injection and 3-D reconstruction of histological sections were similar (figs. 1 to 3). Based on the transillumination technique, we defined 4 types of preputial vascularization in normal boys—1 artery predominant (41.67%), 2 arteries predominant (25%), H-type (12.5%) and net-like (no predominant artery) (20.83%) (see table). Similarly, hypospadiac preputial vascular anatomy was classified according to the same 4 types—1 artery predominant (27%), 2 arteries predominant (13%), H-type (13%) and net-like (no predominant artery) (47%) (fig. 3 and table).
FIG. 2. Serial cross-sectional histological analysis of normal and hypospadiac preputial flap. A and B represent normal preputial flap with 2 artery predominant vascularization in 3-year-old boy. C and D represent hypospadiac preputial flap with net-like (no predominant artery) vascularization in a 3.5-year-old boy. A and C represent most distal sections, and B and D represent most proximal. Tissue is open form of circular preputial flap around penis. Both edges were attached to each other at 5 to 7 o’clock positions. Note vascularization at most proximal site (B and D) occupies only dorsal site of flap. In B (normal) note there are only 2 arteries (a) (B1 and B4), whereas in D (hypospadiac) there are 4 small diameter arteries (a) (D1 to D4). In A smaller arteries (a) (A1 to A3 and A5) and a vein (v) (A4) are visible, indicating that 2 arteries branched into smaller ones to supply outer skin (os) and inner mucosa (im) layers of preputial flap. However, in C, which is distal part of hypospadiac preputial flap, same arteries (a) (C1 to C4) are observed without prominent branching as seen in normal prepuce.
FIG. 3. Three-D reconstructions of 4 different arterial systems in hypospadiac preputial flap. A and B, single artery predominant. C and D, 2 arteries predominant. E and F, H-type arch artery. G and H, no predominant artery but net-like system with fewer distal branchings.
Net-like vascular anatomy was noted in 4 of 5 more severe hypospadiac prepuces. In histological sections it was possible to differentiate the preputial tissues with no predominant arteries from those with 1 or 2 predominant arteries, since they showed few distal branchings into smaller arteries (fig. 2). Additionally, 3-D reconstruction images revealed a better understanding of vascular anatomy in normal and hypospadiac males (fig. 3). DISCUSSION
FIG. 1. Comparison of transillumination (A) and arterial methylene blue (B) techniques to describe arterial system of preputial flap. Single artery predominant preputial flap was observed in transillumination, and arterial methylene blue injection showed that it supplies most of prepuce.
General principles of successful hypospadias surgery include meticulous technique with delicate tissue handling and use of well vascularized tissue. The prepuce is the ideal tissue for neourethra reconstruction and penile body skin
HYPOSPADIAC AND NORMAL PREPUTIAL VASCULAR ANATOMY Diversity of vascular anatomy in normal and hypospadiac prepuces Group
No. Pts (%) Normal
1 Artery 2 Arteries H-type Net-like
20 (41.67) 12 (25) 6 (12.5) 10 (20.83) Hypospadiac
Anterior hypospadias: 1 Artery 2 Arteries H-type Net-like Middle hypospadias: 1 Artery 2 Arteries H-type Net-like
10 3 (30.0) 2 (20.0) 2 (20.0) 3 (30.0) 5 1 (20.0) — — 4 (80.0)
repair. To provide a well vascularized preputial flap, a perfect knowledge of preputial vascularization is essential. Nevertheless, the hypospadiac preputial vascular anatomy and its anatomical variations have not yet been defined. The arterial system of the normal prepuce is empirically extrapolated to the hypospadiac prepuce. In this study we tested the accuracy of preputial vascular anatomy identification by transillumination to arterial methylene blue injection (fig. 1), and 3-D reconstruction of histological sections (figs. 2 and 3). When we compared the prepuces we observed that the types of preputial vascular anatomy were similar between normal and hypospadiac males. However, the frequency of each variation type was different between these 2 groups (see table). Particularly, the net-like arterial system (no predominant artery) was more common in the hypospadiac prepuce (fig. 2, C and D, and fig. 3, G and H, and table). As seen in figure 3, the use of 3-D reconstruction of serial histological sections focusing on the arterial vessels (fig. 2) provided a unique opportunity for better visualization and understanding of vascular anatomy of normal and hypospadiac prepuces. Previous elegant studies have demonstrated the blood supply to the normal penis and prepuce.3– 6 In his description of the superficial anatomy of the penis Hinman has shown 5 layers of tissue.9 These are skin, superficial layer of the penile fascia or dartos fascia, tela subfascialis, deep layer of the penile fascia or Buck’s fascia and tunica albuginea. Buck’s fascia covers the tunica albuginea of the corpora cavernosa and the corpus spongiosum. It encloses the deep dorsal veins, arteries and nerves. These vessels are derived from the internal pudendal vessels. Apart from this deep vascular system the penis is supplied by a superficial system, which is of importance for the preputial flap and which originates from the inferior and superior external pudendal arteries. The dartos fascia, the skin of the penis and the prepuce are supplied by the superficial penile arteries, which arise from the inferior external pudendal arteries. The superior external pudendal arteries only supply the skin on the dorsal side of the base of the penile shaft. The variations of the penile vascular anatomy have been reported previously. Marty et al distinguished 3 main patterns of vascularization of the penile shaft skin.4 First, both inferior external pudendal arteries vascularize half of the skin of the shaft of the penis, whereby each vessel divides into 2 superficial penile arteries, running dorsolaterally and ventrolaterally in the dartos fascia. In addition, the arterial vasculature of the skin of the complete penile shaft is derived from one side through one inferior external pudendal artery. Finally, both inferior external pudendal arteries supply the skin of the penile shaft but one is dominant. These findings have been confirmed by the cadaveric dissection study of Werker et al, who indicated the importance of variations of preputial flap vascularization for free preputial flaps.6
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Our dissection, methylene blue injection (fig. 1) and histological studies (fig. 2) revealed that the main vascular supply of the normal and hypospadiac prepuce was always derived from the superficial penile arteries, which were confined within the dartos fascia. On reaching the preputial ring the branches of the superficial penile arteries were becoming tortuous and minute (fig. 2, A), and the terminal branches were running circumferentially toward the coronal sulcus. Although the deep and superficial vascular systems anastomose at the level of the coronal sulcus, only some marginal blood supply of the prepuce was derived from the deep arterial system. This preputial vascularization enables the creation of well vascularized longitudinal flaps following the axial course of blood vessels along the outer preputial layer (fig. 2, A). The inner layer of the prepuce remains well vascularized because after the minute terminal and communicating branches are severed it still receives a blood supply from the glans. Therefore, as Hinman stated, in hypospadiac and normal males 2 preputial layers remain well vascularized, and can be used for urethral and penile body reconstruction.9 Based on the anatomical studies of Marty4 and Werker6 et al, in which superficial penile artery variations are mentioned, we can justify the variations of preputial vessels in normal subjects in which the one predominant vessel type is the most common. Baskin et al studied the fetal hypospadiac penis in detail.10 They observed extensive vessel formation under the urethral plate compared to normal. However, they did not focus on the preputial vascularization. We think that it should not be surprising to observe abnormal vascularization of prepuce in hypospadias. We defined the variation types of arterial system in hypospadias as the same as normal prepuce (fig. 3 and table). However, the majority of net-like artery formation (no predominant artery) was noteworthy compared to normal prepuce (see table). Interestingly, as the severity of hypospadias increased, the net-like vascularization (no predominant artery) became more common (see table). We can speculate that the underlying cause leading to more severe hypospadias also affects preputial development and its vascularization. Classic preputial flap development in hypospadias repair has been based on the normal penile vascular anatomy.7, 8 Nevertheless, data about the vascularization types and frequency rates in hypospadiac prepuce are lacking. Hinman also presented the fundamental studies about the blood supply of the hypospadiac preputial flap.9 Also, Duckett and others have studied the vascular supply of preputial flaps by immunofluorescence and transillumination techniques.1, 8 Recently, Perovic and Radojicic reported the diversity of hypospadiac prepuce vascular anatomy by using transillumination and arterial india ink injection.2 They suggested the same classification of vascularization types as we observed. However, they reported 1 or 2 vessel predominance with or without H-type communication in 70% of hypospadiac males. We observed this type of vascularization in 50% of the cases. The discrepancy between these studies can be explained by the ratios of different severity types of hypospadias cases, since most of the cases in our study with more severe hypospadias had a net-like arterial system (no predominant artery). As Perovic and Radojicic tested the accuracy of the transillumination technique with arterial india ink and gelatin mixture injection, we tested the accuracy of transillumination with arterial methylene blue injection.2 In our study histological evaluation of the normal and hypospadiac prepuce provided better identification of the arterial and venous vessels (fig. 2). Additionally, as seen in figure 3, 3-D reconstruction images of the histologically defined arterial vessels in prepuce allowed a better understanding of preputial vascular anatomy. By using different techniques, including histological analysis, we demonstrated the difference between
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the vascular anatomies of normal and hypospadiac prepuce. On the basis of our study, we do not advise empirical surgical techniques in hypospadias repair. We strongly advocate defining the blood vessels of the flap for preservation of blood supply of the preputial flap, particularly in more severe hypospadias cases. CONCLUSIONS
Although the frequency of anatomical variations may differ, the normal and hypospadiac prepuce vascular anatomy is similar. However, identification of the type of the preputial vascular supply may help to decide the surgical technique to improve hypospadias repair outcome. Dr. Laurence S. Baskin reviewed this article. REFERENCES
1. Ferro, F. and Bloom, D. A.: Medical photography and genitourinary surgery. Br J Urol, 82: 325, 1998 2. Perovic, S. V. and Radojicic, Z. I.: Vascularization of the hypospadiac prepuce and its impact on hypospadias repair. J Urol, 169: 1098, 2003 3. Ninomiya, H. and Nakamura, T.: Vascular architecture of the canine prepuce. Anat Histol Embryol, 10: 351, 1981 4. Marty, B., Perruchoud, C., Wicky, S., Guillou, L. and Von Segesser, L. K.: Atheroembolization: a harmful complication of therapeutic internal iliac artery occlusion. J Vasc Surg, 36: 1062, 2002 5. Heitz, M., Pottek, T. and Schreiter, F.: Anatomy and blood supply of the penis and urethra. Urologe A, 37: 2, 1998 6. Werker, P. M., Terng, A. S. and Kon, M.: The prepuce free flap: dissection feasibility study and clinical application of a superthin new flap. Plast Reconstr Surg, 102: 1075, 1998 7. Duckett, J. W., Jr.: Transverse preputial island flap technique for repair of severe hypospadias. Urol Clin North Am, 7: 423, 1980 8. Duckett, J. W.: The island flap technique for hypospadias repair. Urol Clin North Am, 8: 503, 1981 9. Hinman, F., Jr.: The blood supply to preputial island flaps. J Urol, 145: 1232, 1991 10. Baskin, L. S., Erol, A., Li, Y. W. and Cunha, G. R.: Anatomical studies of hypospadias. J Urol, 160: 1108, 1998
11. Yucel, S. and Baskin, L. S.: Identification of communicating branches among the dorsal, perineal and cavernous nerves of the penis. J Urol, 170: 153, 2003 EDITORIAL COMMENT This article contributes to the otherwise poorly reported field of hypospadiac prepuce vascularization, and confirms the usefulness and accuracy of transillumination, which is confirmed to be a simple method for intraoperative identification of the preputial blood supply. The histological studies and computer images are well done and I particularly appreciate the effort of the authors to separate the arterial from venous tiny blood vessels. The comparative study of the vascular anatomy of normal and hypospadiac penises is interesting as regarding the origin and development of the hypospadiac anomaly. However, it does not have a significant impact on hypospadias repair. Nonetheless, it can be of importance in hypospadias with an intact prepuce. The results and discussion on the vascularization of 45 prepuces without hypospadias are in agreement with already published data in the literature. The authors made a complete analysis of only 12 hypospadiac prepuces. They also reported the classification of prepuce blood supply, which we have already published (reference 2 in article), but they reported a different rate from us. Hypospadias is a common anomaly of the penis, and to reach such a conclusion, investigation of a greater number of patients is necessary. We agree that the prepuce with net-like form is unfavorable for the creation of a well vascularized flap, especially its most distal part, which is usually poorly vascularized and is the cause of complications after urethroplasty (reference 2 in article). Also, one should pay attention to the morphology of the prepuce, which is correlated to the preputial blood supply.1 We should thank the authors for their effort to identify the preputial hypospadiac blood supply, which is essential in the surgery of hypospadias. Sava Perovic University Children’s Hospital Belgrade, Serbia Yugoslavia 1. Radojicic, Z. I. and Perovic, S. V.: Classification of prepuce in hypospadias according to morphological abnormalities and their impact on hypospadias repair. J Urol, 172: 301, 2004
