- Email: [email protected]
The Male Urethral Sphincter Complex Revisited: An Anatomical Concept and its Physiological Correlate
The Male Urethral Sphincter Complex Revisited: An Anatomical Concept and its Physiological Correlate Mamdouh M. Koraitim From the Department of Urology, College of Medicine, University of Alexandria, Alexandria, Egypt
Purpose: The anatomy of the male urethral sphincter has not been stable since it was first described more than 150 years ago. Although 18th and 19th century historical descriptions of the urethral sphincter are most accurate and comprehensive, modern textbooks lack details and include inaccuracies and misleading illustrations. This is an attempt to achieve a revised concept of the male urethral sphincter complex. Materials and Methods: A thorough review of the English literature in the last 100 years, and of pertinent Germinal publications and textbooks of the 19th and 20th centuries was done. Also, we reviewed urodynamic findings in male patients in whom the urethral sphincters had been expectedly damaged in the proximal or distal part by surgery during the last 20 years. Results: The current concept of urethral sphincter anatomy does not differ much from that described and illustrated in the 19th century. The disagreement between the historical and recent descriptions is primarily concerned with the cranial extension of the skeletal muscle component and the caudal extension of the smooth muscle component in the urethral wall. Conclusions: The male urethral sphincter complex is composed of an inner lissosphincter of smooth muscle and an outer rhabdosphincter of skeletal muscle. It extends in the form of a cylinder around the urethra from the vesical orifice to the perineal membrane. While the rhabdosphincter is most marked around the membranous urethra and becomes gradually less distinct toward the bladder, the lissosphincter has its main part at the vesical orifice and is thinner in its further course in the urethra. The lissosphincter is primarily concerned with the function of continence at rest. On the other hand, the rhabdosphincter has a dual genitourinary function, namely active continence during stress conditions and antegrade semen propulsion. Key Words: urethra, anatomy, history of medicine, urodynamics, male
he anatomy of the urethral sphincter complex has not been stable, as would be expected since it was first described early in the 18th century. The history behind its anatomical description is rich with fervent debate, keen scientific observations, deletions and misleading illustrations spanning almost 150 years of literary publication. This is readily explained by several factors. 1) Morphological depictions of the urethral sphincter have commonly been derived from gross cadaveric dissection of the pelvis, which is fraught with the inevitable distortion and alteration of anatomical structures.1 2) Anatomical observations in fetuses and children have been applied to adults, notwithstanding the necessary modifications in the urethral sphincter resulting from accelerated prostate growth after puberty. 3) Different terms and synonyms have been used interchangeably at various times but referring to totally different structures. For example, the external sphincter was originally so called because it is located distal, ie caudal, to the internal sphincter but with time the term external sphincter has tended to focus urological attention on the periurethral muscles lying external, ie outside or lateral, to the urethra.2 4) Most important is the language barrier since the most influential and detailed descriptions have been those of German authors of the 18th and 19th centuries. Of 55 cited references in a renowned book published in 1900 about
T
Submitted for publication May 14, 2007.
0022-5347/08/1795-1683/0 THE JOURNAL OF UROLOGY® Copyright © 2008 by AMERICAN UROLOGICAL ASSOCIATION
urogenital musculature 42 are in German, 10 are in French and only 3 are in English.3 In addition to misinterpretation due to the language barrier, we cannot exclude active deletion by French authors, who had probably been dominated by political factors, especially after the Franco-Prussian War.4 The paragraphs that follow represent a distillation of a modest amount of study on the subject of the male urethral sphincter complex, intended to elucidate some of its aspects. This article is based on experimental and clinical studies of the male urethral sphincter by the author in the last 40 years as well as on his experience with surgical reconstruction of the bladder neck and sphincter-active posterior urethra in more than 500 patients. As a prerequisite for writing this article, almost all of what has been published about the male urethral sphincter in the English literature in the last 100 years was thoroughly reviewed. Also, pertinent original German publications and textbooks of the 19th and 20th centuries were targeted for certain anatomical information.
EVOLUTION OF THE URETHRAL SPHINCTER FROM THE 19TH THROUGH THE 20TH CENTURY Skeletal Muscle Component Of the many investigators who have made original contributions that became the groundwork for subsequent study of
1683
Vol. 179, 1683-1689, May 2008 Printed in U.S.A. DOI:10.1016/j.juro.2008.01.010
1684
MALE URETHRAL SPHINCTER COMPLEX REVISITED
FIG. 1. Median section of bladder and urethra according to Henle.5 1, bladder muscle wall. 2, ureteral orifice. 3, vas deferens. 4, seminal vesicle. 5, sphincter vesicae internus. 6, trigone longitudinal muscle layer. 7, prostate. 8, sphincter vesicae externus.
the urethral sphincter 3 are especially prominent, namely Henle,5 Holl6 and Kalischer.3 Henle has the distinction as the first (1866) to recognize that the urethral sphincter is composed of a smooth and a skeletal muscle component.5 He named the striped fiber component the sphincter vesicae externus to distinguish it from the smooth fiber sphincter vesicae internus (fig. 1). In his study the external sphincter extended from the prostatovesical furrow down to the apex of the prostate but it did not include the muscle mass around the membranous urethra, which he termed the muscle transverses perinei. The muscle fibers of the sphincter vesicae externus completely surrounded the prostatic apex as a ring shape, whereas more proximally they formed half circles around the anterolateral surface of the prostate. In 1897 Holl gave the name diaphragma urogenital to the muscle plate within the pubic arch.6 He noted that the greater part of this muscle is arranged sphincter-wise around the membranous urethra and named it the muscle sphincter urethrae membranaceae. The rest of the muscle has a transverse course and he named it the muscle transverse perinei profundus. Also, he was able to confirm that the muscle fibers behind the membranous urethra end in the midline in a fibroelastic band, from which originates the perineal body. More importantly Holl should be specifically credited with finding that the muscle fibers of the sphincter urethrae membranaceae extend uninterrupted to cover the anterolateral surface of the prostate as the sphincter urethrae prostaticae.6 He considered that the urethra throughout its course from bladder to membranous urethra is placed within a single tubular sphincter, which necessarily has different sites of attachment (fig. 2). The findings of Henle5 and Holl6 were confirmed by many German investigators. In addition, in 1900 Kalischer convincingly reported that in children the skeletal urethral sphincter forms a distinctly marked muscle cap on the prostate, whereas in adults the muscle fibers are partially atro-
FIG. 2. Sagittal section of male pelvis according to Holl.6 1, sphincter urethrae prostaticae. 2, dorsal vein of penis. 3, pubic venous plexus. 4, sphincter urethrae membranaceae. 5, fibroelastic raphe. 6, bulbocavernosus muscle. 7, deep external anal sphincter. 8, superficial external anal sphincter. 9, subcutaneous external anal sphincter. 10, internal anal sphincter.
phied and irregularly dispersed among the smooth muscles of the prostate and, thus, the muscle cap appears much less distict.3 He concluded that the prostatic part of the skeletal sphincter is too weak to act as a urinary sphincter and it is mainly concerned with sexual function. Hence, he gave the name rhabdosphincter urogenitalis to the whole skeletal urethral sphincter, which is composed most proximally of the rhabdosphincter prostaticus in a half ring formation, the rhabdosphincter infraprostaticus completely encircling the prostatic apex and most distal the rhabdosphincter diaphragmaticus, which surrounds the membranous urethra. Kalischer stressed that all 3 parts of the muscle are not separated from each other but form a uniform-appearing single muscle layer (figs. 3 and 4).3 However, English textbooks often showed drawings of the sphincter vesicae externus to be reduced with no extension into the bladder or not drawn at all.4 It soon was forgotten for in 1876 and 1877 the French authors Paulet7 and Ca-
FIG. 3. Schematic sagittal section of bladder and urethra according to Kalischer.3 1, transverse muscle layer of bladder. 2, longitudinal muscle layer of bladder. 3, smooth circular muscle layer of urethra. Blase, bladder.
MALE URETHRAL SPHINCTER COMPLEX REVISITED
1685
contained within it. In accord with the historical descriptions he found that the sphincter muscle lies in contact with the urethra ventral from the base of the bladder to the perineal membrane. Furthermore, Oelrich reiterated that there is no distinct superior fascia of the so-called urogenital diaphragm separating the sphincter from the prostate.
FIG. 4. Schematic transverse section of prostatic urethra according to Kalischer.3 1, blood vessel. 2, smooth circular muscle layer of urethra. 3, urethra.
diat,8 respectively, on whose studies modern accounts are based, made no mention of any German author and applied the name sphincter externe de la vessie to the skeletal muscle around the membranous urethra, in contrast to the smooth muscle internal sphincter around the vesical orifice.7,8 This paved the way for later authors to erroneously equate the external urethral sphincter with that portion of the skeletal muscle around the membranous urethra, as perpetuated in most English and American textbooks. Almost 100 years elapsed since Henle described his sphincter vesicae externus5 before it was revisited in the English literature in 1966 by Manley9 and in 1969 by Haines.4 Confirming the original descriptions of the German investigators, they found that the skeletal urethral sphincter surrounds the membranous urethra in the form of an inverted horseshoe and continues proximal over the anterolateral surface of the prostate as a semilunar cap. They repeatedly insisted on complete continuity between the prostatic and membranous parts of the rhabdosphincter, and reiterated that there is no superior fascia of the urogenital diaphragm between them. Also, Manley9 confirmed the findings of Kalischer3 that in adults the skeletal muscle fibers gradually decrease in size as the bladder is approached and become more separated by intervening smooth muscle fibers. These descriptions should have guided the authors of anatomical textbooks to provide accurate information about the skeletal urethral sphincter but this has not been the case. More recently Oelrich not only confirmed the anatomical findings of the 19th century, which have never been illustrated more clearly, but also offered its embryological basis.10 In an extensive study of pelvic specimens ranging in age from term to 70 years he noted that the skeletal urethral sphincter is derived from a single primordium before the development of the prostate, which grows into the overlying sphincter. At puberty accelerated prostate growth causes further invasion and thinning of the sphincter, and results in what may appear to be isolated segments of the sphincter muscle, which partly overlap the prostate and partly are
Smooth Muscle Component The presence of a sphincter of annular fibers at the passage from the bladder into the urethra was denied as early as 1836 by Guthrie,11 more recently in 1958 by Clegg12 and in 1960 by Woodburne.13 Possibly in 1854 Kohlrausch was the first to introduce the concept of an internal sphincter.14 He claimed that the muscle fibers of the bladder condense near the vesical orifice to form a true sphincter vesicae of circular fibers and the sphincter is more thick on the posterior than on the anterior side. However, in 1866 Henle conceived the muscle fibers of the sphincter as independent of the bladder musculature and identified it as the sphincter vesicae internus (fig. 1).5 In 1897 Versari ascertained the existence of the internal sphincter as an anatomical entity independent of and completely different in appearance and structure from the bladder musculature.15 Also, he observed that the dorsal, thicker sector of the sphincter lies in the vesical trigone. In 1900 Kalischer, confirming the findings of Versari,15 ascertained that the internal sphincter is derived from the musculature of the urethra, with which it has several characters in common, and is entirely different from the bladder musculature.3 It is composed of thin fiber bundles that are closely packed together with only scant amounts of connective tissue. Also, the urethra as well as the trigone is provided with many elastic fibers, which are missing in the bladder. Hence, he identified the internal sphincter as the sphincter trigonalis (fig. 3). These findings were recently confirmed by computer generated 3-dimensional reconstruction of the male pelvis that showed the trigone to migrate at the bladder neck anterior to the urethra and continue down the front of the prostate as the anterior fibromuscular stroma, forming with it a single unit in continuity.16 However, it is difficult to understand how the trigone, while flattening during bladder filling, can act as a sphincter. An anatomical finding of the urethral sphincter complex that has usually been underestimated is the fact that the urethra is invested with a wide coat of smooth muscle from the bladder neck to the perineal membrane.17,18 This smooth muscle coat lies between the mucosa and the skeletal urethral muscle, making up with the connective tissue the bulk of the urethral wall. It consists of a distinct layer of longitudinal smooth muscle surrounded by a wider layer of circular smooth muscle.19 While contraction of the circular fibers causes narrowing of the urethra to maintain urinary continence, as described, contraction of the longitudinal fibers widens the urethra during the evacuation of urine.3 Needless to say, the current concept of the anatomy of the urethral sphincter complex does not differ much from that described and illustrated in the 19th century. Actually the improved depiction of pelvic anatomy by new reconstructive imaging modalities have offered a revised view of the urethral sphincter as it was described about 150 years ago with little modification.16 The disagreement between the historical and recent descriptions is primarily concerned with cranial extension of the skeletal muscle component and caudal
1686
MALE URETHRAL SPHINCTER COMPLEX REVISITED
extension of the smooth muscle component in the urethral wall. However, it seems that we are still entrenched in the same uncertainty that existed in that old time. This confusion cannot be resolved by dissecting new cadaveric specimens with its potential complication for altering normal anatomy, which may introduce more inaccuracies and new complexity to the subject. One must consider that the urethral sphincter mechanism essentially involves a functional problem, of which the solution does not lie only in the autopsy room. Rather, this confusion can best be resolved by critical appraisal of the literature to discriminate correct from incorrect information and consequently to build an anatomical concept of this structure. The validity of this concept depends on its ability to provide correct inferences regarding function, including passive and active urinary continence, voluntary interruption of the urinary stream and the genital function of ejaculation. THE ANATOMICAL CONCEPT The presence of more than 1 sphincter is not peculiar to the bladder and is in line with the duplication of safety mechanism generally found in the structural plan of humans. It is noteworthy that the bladder does not form a sphincter of its own from its musculature. Rather, it is formed exclusively by the urethra. Also, irrespective of all different views about the anatomy of the urethral sphincter complex there has been complete agreement that it is formed of smooth and skeletal muscle components. Hence, in this anatomical concept the urethral sphincter is composed of 2 morphologically related but functionally unrelated components, namely an inner lissosphincter of smooth muscle and an outer rhabdosphincter of skeletal muscle. The urethral sphincter complex extends in the form of a cylinder around the urethra from the vesical orifice to the distal end of the membranous urethra. While the outer component of skeletal muscle is most marked and thickest around the membranous urethra, and becomes gradually less distinct toward the bladder, in contrast, the inner component of smooth muscle has its main part at the vesical orifice and is thinner in its further course in the urethra (fig. 5). Also, whereas the lissosphincter forms a complete cylinder of circular muscle fibers around the urethra, the rhabdosphincter does not. From the perineal membrane to the prostatic apex the skeletal muscle fibers unite behind the urethra in a central fibrous raphe, while more proximal they form a cap on the anterolateral side of the prostate. Furthermore, while after puberty the lissosphincter does not show appreciable change, the rhabdosphincter shows atrophy of its prostatic part, of which the fibers become indistinctly dispersed among the smooth muscles and glands of the prostate. THE PHYSIOLOGICAL CORRELATE Passive Continence by the Lissosphincter Passive continence is the involuntary aspect of micturition since no conscious effort is required to achieve continence. There is good reason to believe and much evidence to show that passive continence is primarily and exclusively a function of the urethral lissosphincter. 1) Urine is normally held at the level of the vesical orifice, which is a smooth muscle function. Also, after transurethral prostatectomy urine is
FIG. 5. Revised concept of male urethral sphincter complex. 1, bladder musculature. 2, proximal part of lissosphincter internal sphincter. 3, distal part of lissosphincter smooth circular muscle layer of urethra. 4, rhabdosphincter. 5, prostatic part of rhabdosphincter. 6, perineal membrane. 7, prostate.
held at the lower limit of the prostatic cavity, where the lissosphincter is intact, and well proximal to the membranous urethra, where the main part of the rhabdosphincter is located. 2) Post-prostatectomy incontinence results from resecting a few mm in depth distal to the verumontanum, which obviously injures the lissosphincter but leaves the more distal rhabdosphincter intact, as proved by the increase in MUCP during the hold maneuver in these patients in this and previous studies.20 3) After posterior anastomotic urethroplasty, which includes excision of the main part of the rhabdosphincter, continence is achieved only by the bladder neck and supramontanal urethra, where the proximal part of the lissosphincter is located, and only scattered and insignificant striated muscle fibers are present.21,22 4) There is no effect on passive continence after rhabdosphincter paralysis by curare injection, as demonstrated by Lapides on himself,23 or by pudendal nerve anesthesia in patients after prostatectomy.24 All of this evidence leads to the inescapable conclusion that continence at rest primarily depends on the lissosphincter. On the other hand, the presence of the rhabdosphincter does not guarantee continence and its loss does not cause incontinence in the presence of an intact lissosphincter. The lissosphincter maintains continence at rest by contraction of its circular muscle fibers, resulting in closure of the vesical orifice and concentric narrowing of the posterior urethra. Maximum closure may be assumed to be at the level of the vesical orifice, where the lissosphincter is most thick, and in the membranous urethra, where the urethra is most narrow. The presence of the whole length of the lissosphincter is not essential to maintain continence. This may be accomplished by the proximal or the distal part of the sphincter alone, as demonstrated in patients after pos-
MALE URETHRAL SPHINCTER COMPLEX REVISITED terior urethroplasty or prostatectomy, respectively.20-22 Of course, a minimal length of lissosphincter is crucial for this function, below which incontinence is inevitable. This is the rationale of modified apical dissection of the prostate during radical prostatectomy, as advocated by Myers, which entails isolation and careful division of the dorsal vein complex, preservation of the neurovascular bundles and meticulous dissection around the prostatic apex.25
Genitourinary Function of the Rhabdosphincter The rhabdosphincter has a dual genitourinary function. The arrangement of muscle fibers in its caudal and cranial parts determines the urinary and genital roles, respectively. The attachment of the caudal part of the muscle to its posterior median raphe would result in movement of the anterior urethral wall toward the posterior wall with contraction. Denonvilliers’ fascia and the rectourethralis muscle together form a relatively rigid posterior plate, against which compression of the pliable anterior urethral wall produces a transversely flattened urethral lumen.26 This results in a larger surface area of coaptation than could be achieved by concentric contraction of the lissosphincter, thus, creating much higher urethral resistance. This forceful occlusion of the urethra is the principle of active continence, such as that which occurs during events of increased intra-abdominal pressure or during voluntary interruption of micturition. Occlusion of the urethra during these events occurs in the region of the membranous urethra, as evidenced by the increase in MUP during UPP, or by the site of contrast medium arrest under fluoroscopy. In this regard it is still not widely appreciated that the rhabdosphincter is not a purely slow twitch muscle, as originally described by Gosling et al,27 but rather a mixed slow and fast twitch striated muscle with fast twitch fibers more predominant in the caudal part of the sphincter.28,29 This relatively recent finding endorses the view that this part of the rhabdosphincter around the membranous urethra is especially concerned with the rapid and forceful closure of the urethra during active continence. Also, it is not generally remembered that Denny-Brown and Robertson found as early as 1933 that contraction of the skeletal urethral muscle is vigorous but capable of only briefly sustained activity lasting only a few seconds.30 The arrangement of the muscle fibers of the prostatic rhabdosphincter, whether as a distinct muscle cap in children or as indistinctly scattered fibers in adults, would prohibit it from having a significant role in urinary continence. Contraction of this part of the rhabdosphincter would only produce side-to-side compression of the prostatic urethra, which is not sufficient to produce continence but could result in antegrade propulsion of semen in the presence of a closed vesical orifice. Accordingly the prostatic rhabdosphincter has essentially a sexual function. This was well recognized as early as 1900 by Kalischer, who rightly coined the term rhabdosphincter urogenitalis for the skeletal urethral sphincter.3 Inaccurate oversimplified explanations, such as the 2 opposing loops of detrusor muscle or base plate mechanism of the bladder neck, or even the traditionally upheld concept of proximal and distal urethral mechanisms are often easier to understand than the real thing and they tend to instill a false sense of comprehension.2 The so-called 2 opposing loops or arches of detrusor muscle at the bladder neck that
1687
pull it closed as they contract were first described in 1900 by Toldt.31 Although this anatomical observation was verified in 1915 by Heiss32 and in 1920 by Wesson,33 it has been disputed by later investigators.34 Also, we must emphasize that there is no anatomical evidence for 2 separate urethral sphincteric mechanisms, that is a proximal one of smooth muscles, and a distal one of mixed smooth and skeletal muscles. Rather, there are 2 functionally independent components of the urethral sphincter complex, namely an inner (internal) lissosphincter of smooth muscle and an outer (external) rhabdosphincter of skeletal muscle that are responsible for passive and active continence, respectively. The 2 components form 1 continuous layer that extends uninterrupted from the perineal membrane up to the vesical orifice. URODYNAMIC PROOF OF THE PHYSIOLOGICAL CORRELATE In the last 20 years we have been using urodynamic studies to learn the mechanism of continence in male patients in whom the urethral sphincters were damaged in the proximal or distal part by surgery, as expected. We thought that if the findings of these separate studies were compared and correlated with the anatomical concept, we might reach certain useful conclusions. Thus, we reviewed urodynamic findings in 2 prospective studies including 5 groups of male patients. Group 1 consisted of 23 patients with a mean age of 69 years who had undergone retropubic prostatectomy for benign prostatic hyperplasia and were continent of urine. Conceivably these patients had lost the proximal half of the lissosphincter and still had the distal half or inframontanal part plus the rhabdosphincter. Group 2 consisted of 11 patients with a mean age of 71 years with post-prostatectomy incontinence after transurethral (8) and retropubic (3) prostatectomy. Groups 3 and 4 consisted of 8 continent and 2 incontinent patients, respectively, with a mean age of 31 years who had undergone bulboprostatic anastomotic urethroplasty for strictures complicating a pelvic fracture urethral disruption. The only sphincteric element left in these patients was the proximal half or supramontanal part of the lissosphincter, in addition to a few insignificant skeletal muscle fibers scattered in the prostate.21,22 Group 5 consisted of 8 patients with a mean age of 32.5 years with a normal urethra who served as controls for patients with urethroplasty.22 All patients in the 5 groups underwent UPP at rest and with hold maneuvers. The UPP technique has been previously described in detail.22 The table lists UPP findings at rest in the 5 groups. The hold maneuver significantly increased MUP, MUCP and FPL in patients in groups 1, 2 and 5 (p ⬍0.025). Although arguments about the clinical applicability of UPP will continue, it may reveal the functional status of different parts of the urethral sphincter complex.25 This is especially true if we consider recorded values as relative to each other rather than as absolute values. In the light of our urodynamic findings the described anatomical concept and its physiological correlate is readily explainable. 1) Continence at rest is primarily a function of the lissosphincter (group 3). 2) An intact rhabdosphincter does not guarantee continence (group 2) and its absence does not produce incontinence in the presence of an intact lissosphincter (group 3). 3) The whole length of the urethral sphincter is not essential
1688
MALE URETHRAL SPHINCTER COMPLEX REVISITED UPP findings at rest in 5 groups Mean ⫾ SD Group
MUP (cm H2O) MUCP (cm H2O) FPL (cm)
1*
2
3†
4
5
59.0 ⫾ 11.2‡ 54.0 ⫾ 10.8‡ 2.7 ⫾ 0.7
32.0 ⫾ 09.2 27.0 ⫾ 09.4 1.3 ⫾ 0.5
48.0 ⫾ 12.9 39.0 ⫾ 11.3 2.4 ⫾ 0.5
11.0 ⫾ 1.7 8.0 ⫾ 1.3 1.5 ⫾ 0.2
75.0 ⫾ 7.1 65.0 ⫾ 6.2 4.8 ⫾ 0.9
* Vs group 2 p ⬍0.001. † Vs groups 4 and 5 p ⬍0.0003. ‡ Vs group 3 p ⬍0.001.
to maintain continence. FPL may be shortened to almost half that of normal controls and the patient would remain continent (groups 1 and 3). 4) A minimal length of the urethral sphincter complex is essential to maintain continence, below which incontinence is inevitable (groups 2 and 4). This length is suggested to be more than 1.5 cm, as found in this and other studies.25 5) The main urinary function of the rhabdosphincter is to maintain continence during stress conditions, as shown by the results of UPP during the hold maneuver in patients in groups 1, 2 and 5. In regard to the genital function of the rhabdosphincter we have noted in a previous study in dogs that the ventral part of the bladder neck and the striated external sphincter showed a typical electromyographic pattern during artificial ejaculation.35 In fact, and as Turner-Warwick expressed the advance as a result of developing hypotheses,2 if this anatomical concept and its physiological correlate are held in the right hand and continually tested against urodynamic findings held in the left hand, and vice versa, we may achieve a more comprehensive understanding of the urethral sphincter complex and hopefully have begun to lay the questions around it at rest.
8.
9. 10. 11.
12. 13. 14. 15. 16.
17. 18. 19.
Abbreviations and Acronyms FPL MUCP MUP UPP
⫽ ⫽ ⫽ ⫽
functional profile length maximum urethral closure pressure maximum urethral pressure urethral pressure profilometry
REFERENCES 1.
Burnett AL and Mostwin JL: In situ anatomical study of the male urethral sphincteric complex: relevance to continence preservation following major pelvic surgery. J Urol 1998; 160: 1301. 2. Turner-Warwick R: Observations on the function and dysfunction of the sphincter and detrusor mechanisms. Urol Clin North Am 1979; 6: 13. 3. Kalischer O: Die Urogenitalmuskulatur des Dammes mit besonderer Berucksichtigung des Harnblasenverschlusses. Berlin: Verlag von S Karger 1900. 4. Haines RW: The striped compressor of the prostatic urethra. Br J Urol 1969; 41: 481. 5. Henle J: Handbuch der systematischen Anatomie des Menschen. Bd 2. Eingeweidelehre. Braunschweig 1866. 6. Holl M: Die Muskeln und Fascien des Beckenausganges. In: K. v. Bardeleben Handbuch der Anatomie des Menschen. Bd. 7. Jena: Gustav Fischer 1897. 7. Paulet M: Recherches sur l’anatomie compare du périnée. Paris: J l’Anat Phys 1877.
20.
21. 22.
23. 24.
25. 26.
27.
28.
29.
Cadiat M: Etude sur le muscles du périnée, en particulier sur les muscles dites de Wilson et du Guthrie. Paris: J l’Anat Phys 1877; p 29. Manley CB Jr: The striated muscle of the prostate. J Urol 1966; 95: 234. Oelrich TM: The urethral sphincter muscle in the male. Am J Anat 1980; 158: 229. Guthrie J: Ueber die Krankheiten der Harnrohre, der Prostata und des Blasenhalses. Leipzig: Deutsch von Dr Behrend 1836. Clegg EJ: The musculature of the human prostatic urethra. J Anat 1957; 91: 345. Woodburne R: Structure and function of the urinary bladder. J Urol 1960; 84: 79. Kohlrausch O: Zur Anatomie und Physiologie der Beckenorgane. Leipzig 1854. Versari RS: Annales des maladies des organs genitor-urinaires par Guyon et Lanceraux. Paris 1897; t 15, p 1089, u 1151. Brooks JD, Chao WM and Kerr J: Male pelvic anatomy reconstructed from the visible human data set. J Urol 1998; 159: 868. Eberth CJ: Die mannlichen Geschlechtsorgane. In: Bardeleben Handbuch der Anatomie. Bd. 7. Jena 1904. Elliot JS: Postoperative urinary incontinence, a revised concept of the external sphincter. J Urol 1954; 71: 49. Colapinto V and McCallum RW: Urinary continence after repair of membranous urethral stricture in prostatectomized patients. J Urol 1976; 115: 392. Gudziak MR, McGuire EJ and Gormley EA: Urodynamic assessment of urethral sphincter function in post-prostatectomy incontinence. J Urol 1996; 156: 1131. Koraitim M and Sabry A: Mechanism of continence after transpubic urethroplasty. Urology 1986; 27: 187. Koraitim MM, Atta MA, Fattah GA and Ismail HR: Mechanism of continence after repair of post-traumatic posterior urethral strictures. Urology 2003; 61: 287. Lapides J, Sweat R and Lewis L: Role of striated muscle in micturition. J Urol 1957; 77: 247. Krahn HP and Morales PA: The effect of pudendal nerve anesthesia on urinary continence after prostatectomy. J Urol 1965; 94: 282. Myers RP: Male urethral sphincteric anatomy and radical prostatectomy. Urol Clin North Am 1991; 18: 211. Lowe BA: Preservation of the anterior urethral ligamentous attachments in maintaining post-prostatectomy urinary continence: a comparative study. J Urol 1997; 158: 2137. Gosling JA, Dixon JS, Critchley HO and Thompson SA: A comparative study of the human external sphincter and periurethral levator ani muscles. Br J Urol 1981; 53: 35. Elbadawi A, Mathews R, Light JK and Wheeler TM: Immunohistochemical and ultrastructural study of rhabdosphincter component of the prostatic capsule. J Urol 1997; 158: 1819. Tokunaka S, Murakami U, Fujii H, Okamura K, Miyata M, Hashimoto H et al: Coexistence of fast and slow myosin
MALE URETHRAL SPHINCTER COMPLEX REVISITED
30. 31. 32.
isozymes in human external urethral sphincter: a preliminary report. J Urol 1987; 138: 659. Denny-Brown D and Robertson E: On the physiology of micturition. Brain 1933; 56: 149. Toldt C: Anatomischer Atlas, Bd. 2. 1. Aufl. Wien 1900. ¨ ber den Sphincter vesicae internus. Arch Anat Heiss R: U Physiol 1915: 367.
33.
1689
Wesson M: Anatomical, embryological and physiological study of the trigone and bladder neck. J Urol 1920; 4: 279. 34. Tanagho EA and Smith DR: The anatomy and function of the bladder neck. Br J Urol 1966; 38: 55. 35. Koraitim M, Schaefer W, Melchior H and Lutzeyer W: Dynamic activity of bladder neck and external sphincter in ejaculation. Urology 1977; 10: 130.
Purpose: The anatomy of the male urethral sphincter has not been stable since it was first described more than 150 years ago. Although 18th and 19th century historical descriptions of the urethral sphincter are most accurate and comprehensive, modern textbooks lack details and include inaccuracies and misleading illustrations. This is an attempt to achieve a revised concept of the male urethral sphincter complex. Materials and Methods: A thorough review of the English literature in the last 100 years, and of pertinent Germinal publications and textbooks of the 19th and 20th centuries was done. Also, we reviewed urodynamic findings in male patients in whom the urethral sphincters had been expectedly damaged in the proximal or distal part by surgery during the last 20 years. Results: The current concept of urethral sphincter anatomy does not differ much from that described and illustrated in the 19th century. The disagreement between the historical and recent descriptions is primarily concerned with the cranial extension of the skeletal muscle component and the caudal extension of the smooth muscle component in the urethral wall. Conclusions: The male urethral sphincter complex is composed of an inner lissosphincter of smooth muscle and an outer rhabdosphincter of skeletal muscle. It extends in the form of a cylinder around the urethra from the vesical orifice to the perineal membrane. While the rhabdosphincter is most marked around the membranous urethra and becomes gradually less distinct toward the bladder, the lissosphincter has its main part at the vesical orifice and is thinner in its further course in the urethra. The lissosphincter is primarily concerned with the function of continence at rest. On the other hand, the rhabdosphincter has a dual genitourinary function, namely active continence during stress conditions and antegrade semen propulsion. Key Words: urethra, anatomy, history of medicine, urodynamics, male
he anatomy of the urethral sphincter complex has not been stable, as would be expected since it was first described early in the 18th century. The history behind its anatomical description is rich with fervent debate, keen scientific observations, deletions and misleading illustrations spanning almost 150 years of literary publication. This is readily explained by several factors. 1) Morphological depictions of the urethral sphincter have commonly been derived from gross cadaveric dissection of the pelvis, which is fraught with the inevitable distortion and alteration of anatomical structures.1 2) Anatomical observations in fetuses and children have been applied to adults, notwithstanding the necessary modifications in the urethral sphincter resulting from accelerated prostate growth after puberty. 3) Different terms and synonyms have been used interchangeably at various times but referring to totally different structures. For example, the external sphincter was originally so called because it is located distal, ie caudal, to the internal sphincter but with time the term external sphincter has tended to focus urological attention on the periurethral muscles lying external, ie outside or lateral, to the urethra.2 4) Most important is the language barrier since the most influential and detailed descriptions have been those of German authors of the 18th and 19th centuries. Of 55 cited references in a renowned book published in 1900 about
T
Submitted for publication May 14, 2007.
0022-5347/08/1795-1683/0 THE JOURNAL OF UROLOGY® Copyright © 2008 by AMERICAN UROLOGICAL ASSOCIATION
urogenital musculature 42 are in German, 10 are in French and only 3 are in English.3 In addition to misinterpretation due to the language barrier, we cannot exclude active deletion by French authors, who had probably been dominated by political factors, especially after the Franco-Prussian War.4 The paragraphs that follow represent a distillation of a modest amount of study on the subject of the male urethral sphincter complex, intended to elucidate some of its aspects. This article is based on experimental and clinical studies of the male urethral sphincter by the author in the last 40 years as well as on his experience with surgical reconstruction of the bladder neck and sphincter-active posterior urethra in more than 500 patients. As a prerequisite for writing this article, almost all of what has been published about the male urethral sphincter in the English literature in the last 100 years was thoroughly reviewed. Also, pertinent original German publications and textbooks of the 19th and 20th centuries were targeted for certain anatomical information.
EVOLUTION OF THE URETHRAL SPHINCTER FROM THE 19TH THROUGH THE 20TH CENTURY Skeletal Muscle Component Of the many investigators who have made original contributions that became the groundwork for subsequent study of
1683
Vol. 179, 1683-1689, May 2008 Printed in U.S.A. DOI:10.1016/j.juro.2008.01.010
1684
MALE URETHRAL SPHINCTER COMPLEX REVISITED
FIG. 1. Median section of bladder and urethra according to Henle.5 1, bladder muscle wall. 2, ureteral orifice. 3, vas deferens. 4, seminal vesicle. 5, sphincter vesicae internus. 6, trigone longitudinal muscle layer. 7, prostate. 8, sphincter vesicae externus.
the urethral sphincter 3 are especially prominent, namely Henle,5 Holl6 and Kalischer.3 Henle has the distinction as the first (1866) to recognize that the urethral sphincter is composed of a smooth and a skeletal muscle component.5 He named the striped fiber component the sphincter vesicae externus to distinguish it from the smooth fiber sphincter vesicae internus (fig. 1). In his study the external sphincter extended from the prostatovesical furrow down to the apex of the prostate but it did not include the muscle mass around the membranous urethra, which he termed the muscle transverses perinei. The muscle fibers of the sphincter vesicae externus completely surrounded the prostatic apex as a ring shape, whereas more proximally they formed half circles around the anterolateral surface of the prostate. In 1897 Holl gave the name diaphragma urogenital to the muscle plate within the pubic arch.6 He noted that the greater part of this muscle is arranged sphincter-wise around the membranous urethra and named it the muscle sphincter urethrae membranaceae. The rest of the muscle has a transverse course and he named it the muscle transverse perinei profundus. Also, he was able to confirm that the muscle fibers behind the membranous urethra end in the midline in a fibroelastic band, from which originates the perineal body. More importantly Holl should be specifically credited with finding that the muscle fibers of the sphincter urethrae membranaceae extend uninterrupted to cover the anterolateral surface of the prostate as the sphincter urethrae prostaticae.6 He considered that the urethra throughout its course from bladder to membranous urethra is placed within a single tubular sphincter, which necessarily has different sites of attachment (fig. 2). The findings of Henle5 and Holl6 were confirmed by many German investigators. In addition, in 1900 Kalischer convincingly reported that in children the skeletal urethral sphincter forms a distinctly marked muscle cap on the prostate, whereas in adults the muscle fibers are partially atro-
FIG. 2. Sagittal section of male pelvis according to Holl.6 1, sphincter urethrae prostaticae. 2, dorsal vein of penis. 3, pubic venous plexus. 4, sphincter urethrae membranaceae. 5, fibroelastic raphe. 6, bulbocavernosus muscle. 7, deep external anal sphincter. 8, superficial external anal sphincter. 9, subcutaneous external anal sphincter. 10, internal anal sphincter.
phied and irregularly dispersed among the smooth muscles of the prostate and, thus, the muscle cap appears much less distict.3 He concluded that the prostatic part of the skeletal sphincter is too weak to act as a urinary sphincter and it is mainly concerned with sexual function. Hence, he gave the name rhabdosphincter urogenitalis to the whole skeletal urethral sphincter, which is composed most proximally of the rhabdosphincter prostaticus in a half ring formation, the rhabdosphincter infraprostaticus completely encircling the prostatic apex and most distal the rhabdosphincter diaphragmaticus, which surrounds the membranous urethra. Kalischer stressed that all 3 parts of the muscle are not separated from each other but form a uniform-appearing single muscle layer (figs. 3 and 4).3 However, English textbooks often showed drawings of the sphincter vesicae externus to be reduced with no extension into the bladder or not drawn at all.4 It soon was forgotten for in 1876 and 1877 the French authors Paulet7 and Ca-
FIG. 3. Schematic sagittal section of bladder and urethra according to Kalischer.3 1, transverse muscle layer of bladder. 2, longitudinal muscle layer of bladder. 3, smooth circular muscle layer of urethra. Blase, bladder.
MALE URETHRAL SPHINCTER COMPLEX REVISITED
1685
contained within it. In accord with the historical descriptions he found that the sphincter muscle lies in contact with the urethra ventral from the base of the bladder to the perineal membrane. Furthermore, Oelrich reiterated that there is no distinct superior fascia of the so-called urogenital diaphragm separating the sphincter from the prostate.
FIG. 4. Schematic transverse section of prostatic urethra according to Kalischer.3 1, blood vessel. 2, smooth circular muscle layer of urethra. 3, urethra.
diat,8 respectively, on whose studies modern accounts are based, made no mention of any German author and applied the name sphincter externe de la vessie to the skeletal muscle around the membranous urethra, in contrast to the smooth muscle internal sphincter around the vesical orifice.7,8 This paved the way for later authors to erroneously equate the external urethral sphincter with that portion of the skeletal muscle around the membranous urethra, as perpetuated in most English and American textbooks. Almost 100 years elapsed since Henle described his sphincter vesicae externus5 before it was revisited in the English literature in 1966 by Manley9 and in 1969 by Haines.4 Confirming the original descriptions of the German investigators, they found that the skeletal urethral sphincter surrounds the membranous urethra in the form of an inverted horseshoe and continues proximal over the anterolateral surface of the prostate as a semilunar cap. They repeatedly insisted on complete continuity between the prostatic and membranous parts of the rhabdosphincter, and reiterated that there is no superior fascia of the urogenital diaphragm between them. Also, Manley9 confirmed the findings of Kalischer3 that in adults the skeletal muscle fibers gradually decrease in size as the bladder is approached and become more separated by intervening smooth muscle fibers. These descriptions should have guided the authors of anatomical textbooks to provide accurate information about the skeletal urethral sphincter but this has not been the case. More recently Oelrich not only confirmed the anatomical findings of the 19th century, which have never been illustrated more clearly, but also offered its embryological basis.10 In an extensive study of pelvic specimens ranging in age from term to 70 years he noted that the skeletal urethral sphincter is derived from a single primordium before the development of the prostate, which grows into the overlying sphincter. At puberty accelerated prostate growth causes further invasion and thinning of the sphincter, and results in what may appear to be isolated segments of the sphincter muscle, which partly overlap the prostate and partly are
Smooth Muscle Component The presence of a sphincter of annular fibers at the passage from the bladder into the urethra was denied as early as 1836 by Guthrie,11 more recently in 1958 by Clegg12 and in 1960 by Woodburne.13 Possibly in 1854 Kohlrausch was the first to introduce the concept of an internal sphincter.14 He claimed that the muscle fibers of the bladder condense near the vesical orifice to form a true sphincter vesicae of circular fibers and the sphincter is more thick on the posterior than on the anterior side. However, in 1866 Henle conceived the muscle fibers of the sphincter as independent of the bladder musculature and identified it as the sphincter vesicae internus (fig. 1).5 In 1897 Versari ascertained the existence of the internal sphincter as an anatomical entity independent of and completely different in appearance and structure from the bladder musculature.15 Also, he observed that the dorsal, thicker sector of the sphincter lies in the vesical trigone. In 1900 Kalischer, confirming the findings of Versari,15 ascertained that the internal sphincter is derived from the musculature of the urethra, with which it has several characters in common, and is entirely different from the bladder musculature.3 It is composed of thin fiber bundles that are closely packed together with only scant amounts of connective tissue. Also, the urethra as well as the trigone is provided with many elastic fibers, which are missing in the bladder. Hence, he identified the internal sphincter as the sphincter trigonalis (fig. 3). These findings were recently confirmed by computer generated 3-dimensional reconstruction of the male pelvis that showed the trigone to migrate at the bladder neck anterior to the urethra and continue down the front of the prostate as the anterior fibromuscular stroma, forming with it a single unit in continuity.16 However, it is difficult to understand how the trigone, while flattening during bladder filling, can act as a sphincter. An anatomical finding of the urethral sphincter complex that has usually been underestimated is the fact that the urethra is invested with a wide coat of smooth muscle from the bladder neck to the perineal membrane.17,18 This smooth muscle coat lies between the mucosa and the skeletal urethral muscle, making up with the connective tissue the bulk of the urethral wall. It consists of a distinct layer of longitudinal smooth muscle surrounded by a wider layer of circular smooth muscle.19 While contraction of the circular fibers causes narrowing of the urethra to maintain urinary continence, as described, contraction of the longitudinal fibers widens the urethra during the evacuation of urine.3 Needless to say, the current concept of the anatomy of the urethral sphincter complex does not differ much from that described and illustrated in the 19th century. Actually the improved depiction of pelvic anatomy by new reconstructive imaging modalities have offered a revised view of the urethral sphincter as it was described about 150 years ago with little modification.16 The disagreement between the historical and recent descriptions is primarily concerned with cranial extension of the skeletal muscle component and caudal
1686
MALE URETHRAL SPHINCTER COMPLEX REVISITED
extension of the smooth muscle component in the urethral wall. However, it seems that we are still entrenched in the same uncertainty that existed in that old time. This confusion cannot be resolved by dissecting new cadaveric specimens with its potential complication for altering normal anatomy, which may introduce more inaccuracies and new complexity to the subject. One must consider that the urethral sphincter mechanism essentially involves a functional problem, of which the solution does not lie only in the autopsy room. Rather, this confusion can best be resolved by critical appraisal of the literature to discriminate correct from incorrect information and consequently to build an anatomical concept of this structure. The validity of this concept depends on its ability to provide correct inferences regarding function, including passive and active urinary continence, voluntary interruption of the urinary stream and the genital function of ejaculation. THE ANATOMICAL CONCEPT The presence of more than 1 sphincter is not peculiar to the bladder and is in line with the duplication of safety mechanism generally found in the structural plan of humans. It is noteworthy that the bladder does not form a sphincter of its own from its musculature. Rather, it is formed exclusively by the urethra. Also, irrespective of all different views about the anatomy of the urethral sphincter complex there has been complete agreement that it is formed of smooth and skeletal muscle components. Hence, in this anatomical concept the urethral sphincter is composed of 2 morphologically related but functionally unrelated components, namely an inner lissosphincter of smooth muscle and an outer rhabdosphincter of skeletal muscle. The urethral sphincter complex extends in the form of a cylinder around the urethra from the vesical orifice to the distal end of the membranous urethra. While the outer component of skeletal muscle is most marked and thickest around the membranous urethra, and becomes gradually less distinct toward the bladder, in contrast, the inner component of smooth muscle has its main part at the vesical orifice and is thinner in its further course in the urethra (fig. 5). Also, whereas the lissosphincter forms a complete cylinder of circular muscle fibers around the urethra, the rhabdosphincter does not. From the perineal membrane to the prostatic apex the skeletal muscle fibers unite behind the urethra in a central fibrous raphe, while more proximal they form a cap on the anterolateral side of the prostate. Furthermore, while after puberty the lissosphincter does not show appreciable change, the rhabdosphincter shows atrophy of its prostatic part, of which the fibers become indistinctly dispersed among the smooth muscles and glands of the prostate. THE PHYSIOLOGICAL CORRELATE Passive Continence by the Lissosphincter Passive continence is the involuntary aspect of micturition since no conscious effort is required to achieve continence. There is good reason to believe and much evidence to show that passive continence is primarily and exclusively a function of the urethral lissosphincter. 1) Urine is normally held at the level of the vesical orifice, which is a smooth muscle function. Also, after transurethral prostatectomy urine is
FIG. 5. Revised concept of male urethral sphincter complex. 1, bladder musculature. 2, proximal part of lissosphincter internal sphincter. 3, distal part of lissosphincter smooth circular muscle layer of urethra. 4, rhabdosphincter. 5, prostatic part of rhabdosphincter. 6, perineal membrane. 7, prostate.
held at the lower limit of the prostatic cavity, where the lissosphincter is intact, and well proximal to the membranous urethra, where the main part of the rhabdosphincter is located. 2) Post-prostatectomy incontinence results from resecting a few mm in depth distal to the verumontanum, which obviously injures the lissosphincter but leaves the more distal rhabdosphincter intact, as proved by the increase in MUCP during the hold maneuver in these patients in this and previous studies.20 3) After posterior anastomotic urethroplasty, which includes excision of the main part of the rhabdosphincter, continence is achieved only by the bladder neck and supramontanal urethra, where the proximal part of the lissosphincter is located, and only scattered and insignificant striated muscle fibers are present.21,22 4) There is no effect on passive continence after rhabdosphincter paralysis by curare injection, as demonstrated by Lapides on himself,23 or by pudendal nerve anesthesia in patients after prostatectomy.24 All of this evidence leads to the inescapable conclusion that continence at rest primarily depends on the lissosphincter. On the other hand, the presence of the rhabdosphincter does not guarantee continence and its loss does not cause incontinence in the presence of an intact lissosphincter. The lissosphincter maintains continence at rest by contraction of its circular muscle fibers, resulting in closure of the vesical orifice and concentric narrowing of the posterior urethra. Maximum closure may be assumed to be at the level of the vesical orifice, where the lissosphincter is most thick, and in the membranous urethra, where the urethra is most narrow. The presence of the whole length of the lissosphincter is not essential to maintain continence. This may be accomplished by the proximal or the distal part of the sphincter alone, as demonstrated in patients after pos-
MALE URETHRAL SPHINCTER COMPLEX REVISITED terior urethroplasty or prostatectomy, respectively.20-22 Of course, a minimal length of lissosphincter is crucial for this function, below which incontinence is inevitable. This is the rationale of modified apical dissection of the prostate during radical prostatectomy, as advocated by Myers, which entails isolation and careful division of the dorsal vein complex, preservation of the neurovascular bundles and meticulous dissection around the prostatic apex.25
Genitourinary Function of the Rhabdosphincter The rhabdosphincter has a dual genitourinary function. The arrangement of muscle fibers in its caudal and cranial parts determines the urinary and genital roles, respectively. The attachment of the caudal part of the muscle to its posterior median raphe would result in movement of the anterior urethral wall toward the posterior wall with contraction. Denonvilliers’ fascia and the rectourethralis muscle together form a relatively rigid posterior plate, against which compression of the pliable anterior urethral wall produces a transversely flattened urethral lumen.26 This results in a larger surface area of coaptation than could be achieved by concentric contraction of the lissosphincter, thus, creating much higher urethral resistance. This forceful occlusion of the urethra is the principle of active continence, such as that which occurs during events of increased intra-abdominal pressure or during voluntary interruption of micturition. Occlusion of the urethra during these events occurs in the region of the membranous urethra, as evidenced by the increase in MUP during UPP, or by the site of contrast medium arrest under fluoroscopy. In this regard it is still not widely appreciated that the rhabdosphincter is not a purely slow twitch muscle, as originally described by Gosling et al,27 but rather a mixed slow and fast twitch striated muscle with fast twitch fibers more predominant in the caudal part of the sphincter.28,29 This relatively recent finding endorses the view that this part of the rhabdosphincter around the membranous urethra is especially concerned with the rapid and forceful closure of the urethra during active continence. Also, it is not generally remembered that Denny-Brown and Robertson found as early as 1933 that contraction of the skeletal urethral muscle is vigorous but capable of only briefly sustained activity lasting only a few seconds.30 The arrangement of the muscle fibers of the prostatic rhabdosphincter, whether as a distinct muscle cap in children or as indistinctly scattered fibers in adults, would prohibit it from having a significant role in urinary continence. Contraction of this part of the rhabdosphincter would only produce side-to-side compression of the prostatic urethra, which is not sufficient to produce continence but could result in antegrade propulsion of semen in the presence of a closed vesical orifice. Accordingly the prostatic rhabdosphincter has essentially a sexual function. This was well recognized as early as 1900 by Kalischer, who rightly coined the term rhabdosphincter urogenitalis for the skeletal urethral sphincter.3 Inaccurate oversimplified explanations, such as the 2 opposing loops of detrusor muscle or base plate mechanism of the bladder neck, or even the traditionally upheld concept of proximal and distal urethral mechanisms are often easier to understand than the real thing and they tend to instill a false sense of comprehension.2 The so-called 2 opposing loops or arches of detrusor muscle at the bladder neck that
1687
pull it closed as they contract were first described in 1900 by Toldt.31 Although this anatomical observation was verified in 1915 by Heiss32 and in 1920 by Wesson,33 it has been disputed by later investigators.34 Also, we must emphasize that there is no anatomical evidence for 2 separate urethral sphincteric mechanisms, that is a proximal one of smooth muscles, and a distal one of mixed smooth and skeletal muscles. Rather, there are 2 functionally independent components of the urethral sphincter complex, namely an inner (internal) lissosphincter of smooth muscle and an outer (external) rhabdosphincter of skeletal muscle that are responsible for passive and active continence, respectively. The 2 components form 1 continuous layer that extends uninterrupted from the perineal membrane up to the vesical orifice. URODYNAMIC PROOF OF THE PHYSIOLOGICAL CORRELATE In the last 20 years we have been using urodynamic studies to learn the mechanism of continence in male patients in whom the urethral sphincters were damaged in the proximal or distal part by surgery, as expected. We thought that if the findings of these separate studies were compared and correlated with the anatomical concept, we might reach certain useful conclusions. Thus, we reviewed urodynamic findings in 2 prospective studies including 5 groups of male patients. Group 1 consisted of 23 patients with a mean age of 69 years who had undergone retropubic prostatectomy for benign prostatic hyperplasia and were continent of urine. Conceivably these patients had lost the proximal half of the lissosphincter and still had the distal half or inframontanal part plus the rhabdosphincter. Group 2 consisted of 11 patients with a mean age of 71 years with post-prostatectomy incontinence after transurethral (8) and retropubic (3) prostatectomy. Groups 3 and 4 consisted of 8 continent and 2 incontinent patients, respectively, with a mean age of 31 years who had undergone bulboprostatic anastomotic urethroplasty for strictures complicating a pelvic fracture urethral disruption. The only sphincteric element left in these patients was the proximal half or supramontanal part of the lissosphincter, in addition to a few insignificant skeletal muscle fibers scattered in the prostate.21,22 Group 5 consisted of 8 patients with a mean age of 32.5 years with a normal urethra who served as controls for patients with urethroplasty.22 All patients in the 5 groups underwent UPP at rest and with hold maneuvers. The UPP technique has been previously described in detail.22 The table lists UPP findings at rest in the 5 groups. The hold maneuver significantly increased MUP, MUCP and FPL in patients in groups 1, 2 and 5 (p ⬍0.025). Although arguments about the clinical applicability of UPP will continue, it may reveal the functional status of different parts of the urethral sphincter complex.25 This is especially true if we consider recorded values as relative to each other rather than as absolute values. In the light of our urodynamic findings the described anatomical concept and its physiological correlate is readily explainable. 1) Continence at rest is primarily a function of the lissosphincter (group 3). 2) An intact rhabdosphincter does not guarantee continence (group 2) and its absence does not produce incontinence in the presence of an intact lissosphincter (group 3). 3) The whole length of the urethral sphincter is not essential
1688
MALE URETHRAL SPHINCTER COMPLEX REVISITED UPP findings at rest in 5 groups Mean ⫾ SD Group
MUP (cm H2O) MUCP (cm H2O) FPL (cm)
1*
2
3†
4
5
59.0 ⫾ 11.2‡ 54.0 ⫾ 10.8‡ 2.7 ⫾ 0.7
32.0 ⫾ 09.2 27.0 ⫾ 09.4 1.3 ⫾ 0.5
48.0 ⫾ 12.9 39.0 ⫾ 11.3 2.4 ⫾ 0.5
11.0 ⫾ 1.7 8.0 ⫾ 1.3 1.5 ⫾ 0.2
75.0 ⫾ 7.1 65.0 ⫾ 6.2 4.8 ⫾ 0.9
* Vs group 2 p ⬍0.001. † Vs groups 4 and 5 p ⬍0.0003. ‡ Vs group 3 p ⬍0.001.
to maintain continence. FPL may be shortened to almost half that of normal controls and the patient would remain continent (groups 1 and 3). 4) A minimal length of the urethral sphincter complex is essential to maintain continence, below which incontinence is inevitable (groups 2 and 4). This length is suggested to be more than 1.5 cm, as found in this and other studies.25 5) The main urinary function of the rhabdosphincter is to maintain continence during stress conditions, as shown by the results of UPP during the hold maneuver in patients in groups 1, 2 and 5. In regard to the genital function of the rhabdosphincter we have noted in a previous study in dogs that the ventral part of the bladder neck and the striated external sphincter showed a typical electromyographic pattern during artificial ejaculation.35 In fact, and as Turner-Warwick expressed the advance as a result of developing hypotheses,2 if this anatomical concept and its physiological correlate are held in the right hand and continually tested against urodynamic findings held in the left hand, and vice versa, we may achieve a more comprehensive understanding of the urethral sphincter complex and hopefully have begun to lay the questions around it at rest.
8.
9. 10. 11.
12. 13. 14. 15. 16.
17. 18. 19.
Abbreviations and Acronyms FPL MUCP MUP UPP
⫽ ⫽ ⫽ ⫽
functional profile length maximum urethral closure pressure maximum urethral pressure urethral pressure profilometry
REFERENCES 1.
Burnett AL and Mostwin JL: In situ anatomical study of the male urethral sphincteric complex: relevance to continence preservation following major pelvic surgery. J Urol 1998; 160: 1301. 2. Turner-Warwick R: Observations on the function and dysfunction of the sphincter and detrusor mechanisms. Urol Clin North Am 1979; 6: 13. 3. Kalischer O: Die Urogenitalmuskulatur des Dammes mit besonderer Berucksichtigung des Harnblasenverschlusses. Berlin: Verlag von S Karger 1900. 4. Haines RW: The striped compressor of the prostatic urethra. Br J Urol 1969; 41: 481. 5. Henle J: Handbuch der systematischen Anatomie des Menschen. Bd 2. Eingeweidelehre. Braunschweig 1866. 6. Holl M: Die Muskeln und Fascien des Beckenausganges. In: K. v. Bardeleben Handbuch der Anatomie des Menschen. Bd. 7. Jena: Gustav Fischer 1897. 7. Paulet M: Recherches sur l’anatomie compare du périnée. Paris: J l’Anat Phys 1877.
20.
21. 22.
23. 24.
25. 26.
27.
28.
29.
Cadiat M: Etude sur le muscles du périnée, en particulier sur les muscles dites de Wilson et du Guthrie. Paris: J l’Anat Phys 1877; p 29. Manley CB Jr: The striated muscle of the prostate. J Urol 1966; 95: 234. Oelrich TM: The urethral sphincter muscle in the male. Am J Anat 1980; 158: 229. Guthrie J: Ueber die Krankheiten der Harnrohre, der Prostata und des Blasenhalses. Leipzig: Deutsch von Dr Behrend 1836. Clegg EJ: The musculature of the human prostatic urethra. J Anat 1957; 91: 345. Woodburne R: Structure and function of the urinary bladder. J Urol 1960; 84: 79. Kohlrausch O: Zur Anatomie und Physiologie der Beckenorgane. Leipzig 1854. Versari RS: Annales des maladies des organs genitor-urinaires par Guyon et Lanceraux. Paris 1897; t 15, p 1089, u 1151. Brooks JD, Chao WM and Kerr J: Male pelvic anatomy reconstructed from the visible human data set. J Urol 1998; 159: 868. Eberth CJ: Die mannlichen Geschlechtsorgane. In: Bardeleben Handbuch der Anatomie. Bd. 7. Jena 1904. Elliot JS: Postoperative urinary incontinence, a revised concept of the external sphincter. J Urol 1954; 71: 49. Colapinto V and McCallum RW: Urinary continence after repair of membranous urethral stricture in prostatectomized patients. J Urol 1976; 115: 392. Gudziak MR, McGuire EJ and Gormley EA: Urodynamic assessment of urethral sphincter function in post-prostatectomy incontinence. J Urol 1996; 156: 1131. Koraitim M and Sabry A: Mechanism of continence after transpubic urethroplasty. Urology 1986; 27: 187. Koraitim MM, Atta MA, Fattah GA and Ismail HR: Mechanism of continence after repair of post-traumatic posterior urethral strictures. Urology 2003; 61: 287. Lapides J, Sweat R and Lewis L: Role of striated muscle in micturition. J Urol 1957; 77: 247. Krahn HP and Morales PA: The effect of pudendal nerve anesthesia on urinary continence after prostatectomy. J Urol 1965; 94: 282. Myers RP: Male urethral sphincteric anatomy and radical prostatectomy. Urol Clin North Am 1991; 18: 211. Lowe BA: Preservation of the anterior urethral ligamentous attachments in maintaining post-prostatectomy urinary continence: a comparative study. J Urol 1997; 158: 2137. Gosling JA, Dixon JS, Critchley HO and Thompson SA: A comparative study of the human external sphincter and periurethral levator ani muscles. Br J Urol 1981; 53: 35. Elbadawi A, Mathews R, Light JK and Wheeler TM: Immunohistochemical and ultrastructural study of rhabdosphincter component of the prostatic capsule. J Urol 1997; 158: 1819. Tokunaka S, Murakami U, Fujii H, Okamura K, Miyata M, Hashimoto H et al: Coexistence of fast and slow myosin
MALE URETHRAL SPHINCTER COMPLEX REVISITED
30. 31. 32.
isozymes in human external urethral sphincter: a preliminary report. J Urol 1987; 138: 659. Denny-Brown D and Robertson E: On the physiology of micturition. Brain 1933; 56: 149. Toldt C: Anatomischer Atlas, Bd. 2. 1. Aufl. Wien 1900. ¨ ber den Sphincter vesicae internus. Arch Anat Heiss R: U Physiol 1915: 367.
33.
1689
Wesson M: Anatomical, embryological and physiological study of the trigone and bladder neck. J Urol 1920; 4: 279. 34. Tanagho EA and Smith DR: The anatomy and function of the bladder neck. Br J Urol 1966; 38: 55. 35. Koraitim M, Schaefer W, Melchior H and Lutzeyer W: Dynamic activity of bladder neck and external sphincter in ejaculation. Urology 1977; 10: 130.