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THE MUSCULATURE OF THE HUMAN PROSTATIC BY E. J. CLEGG Department of Anatomy, the University of Liverpool

INTRODUCTION Henle (1866) described two distinct sphincters in the wall of the . The proximal, composed entirely of smooth muscle, was continuous above with the circular muscle layer of the bladder and formed a complete ring around the internal . He named it the 'sphincter vesicae internus'. Distally, and over- lapping the lower fibres of the internal sphincter on their outer surface, he described a ' sphincter vesicae externus', which lay mainly anterior to the urethra, and which near the apex of the gland blended with the deep transverse muscle of the perineum, completely surrounding the urethra. The fibres of the external sphincter were mainly striped, and originated in the stroma of the anterior parts of the gland. Subsequent workers have generally agreed with the above findings, although there is disagreement on the more detailed anatomy of the muscles (Walker, 1906; Young & Wesson, 1921; Graning, 1936; Macleod, 1942; and others). During a previous study of the blood vessels of the prostate gland (Clegg, 1956) it was noted incidentally that, contrary to Henle's view, comparatively few trans- verse fibres, either of muscle or connective tissue, were seen anterior to the urethra, although posteriorly a thick band of transversely running fibres was observed. In addition, the number of longitudinally directed fibres, especially in the anterior and lateral urethral walls, was much greater than Henle's description warranted. It seemed desirable therefore to re-investigate this problem.

MATERIALS AND METHODS Prostate glands were removed from fresh post-mortem material. The ages of the subjects, seven in number, ranged from 53 to 82 years. None of the glands showed significant pathological changes, other than small adenomata; these did not affect the findings. The glands, together with adjoining portions of the bladder, were fixed for periods from 2 to 6 months in 10 % formol saline. In six, transverse sections 50 , thick were cut on the freezing microtome, and one section in ten was stained by Masson's trichrome method. The remaining gland was sectioned longitudinally and treated in the same way. In a few instances, sections were stained by Mallory's method, but this proved unsatisfactory. RESULTS Striped muscle In no case is striped muscle seen to enter into close relationship with the urethra except near the apex of the gland, where bands of fibres infiltrate the smooth muscle anterior, lateral and sometimes posterior to the urethra. Striped muscle fibres make 346 E. J. Clegg their appearance in the anterior region of the gland at the level of the termination of the ejaculatory ducts and progressively increase in number towards the apex.

Smooth muscle With regard to the arrangement of its smooth muscle, it is convenient to consider the prostatic urethra in three parts, a proximal immediately below the internal urinary meatus, an intermediate, comprising that part above the opening of the ejaculatory ducts, and a distal part extending to the apex of the gland.

Proximal part In this section of the urethra the main feature is the thick band of muscle running obliquely downwards and medially behind the lumen (P1. 1, fig. 1). The considerable amount of connective tissue which separates its individual fibres gives it an 'onion- skin' appearance, and it will subsequently be referred to as the 'concentric muscle'. Its fibres are derived from two sources. Peripherally they have their origin in the muscular stroma of the antero-lateral part of the prostate gland and its capsule. Centrally they are continuous with the transverse fibres of the trigone and with the anterior longitudinal of the bladder. Some of these latter fibres pass directly backwards lateral to the internal urinary meatus. Others pass downwards in the anterior urethral wall (P1. 1, figs. 2, 3) for varying distances before passing obliquely downwards and backwards to the posterior aspect of the urethra. From the trigone a number of longitudinally directed fibres pass downwards immediately deep to the of the posterior urethral wall (P1. 1, fig. 3). They are of smaller diameter than the fibres of the concentric muscle. In the lower part of this segment of the urethra a few transverse fibres, again of small diameter, may be seen in the of the anterior urethral wall. Some of these are continuous with the innermost concentric fibres, and thus a complete although very thin ring of smooth muscle passes around the urethra a short distance above the crest. There is no anatomical sphincter immediately below the bladder neck, except in the sense that the peripheral part of the concentric muscle is in continuity with the capsular fibres of the prostate, some of which cross the midline anterior to the urethra. These anterior transverse fibres, however, are not in such intimate relationship with the urethra as are the concentric fibres, as they are separated from it by the fibres derived from the anterior longitudinal layer of the bladder. Intermediate part The is a fibromuscular structure containing the ducts of prostatic glands which open on its sides. The musculature consists of bundles of fibres sepa- rated by connective tissue, which run downwards in the line of the urethra. They are in the main continuous with the posterior longitudinal fibres of the proximal part of the urethra, but in addition longitudinal fibres anterior to the urethra, which run obliquely round to its posterior aspect, and a few fibres from the concentric muscle contribute to the muscle of the crest. As the height of the crest increases, the ejaculatory ducts and pass forwards and downwards through the substance of the prostate towards the base of The musculature of the human prostatic urethra 347 the crest. The ducts and utricle are contained in a sheath, the composition of which changes proximo-distally. Above, it consists mainly of connective tissue with a small number of smooth muscle fibres (PI. 1, fig. 4). The walls of the ejaculatory ducts contain smooth muscle, but the utricle in five of the six glands sectioned trans- versely contains no muscle. In the remaining gland, the utricle wall contains well- defined bands of circular muscle (P1. 2, fig. 5). Below the point where the ducts and utricle turn almost directly forwards the sheath contains considerable amounts of muscle, in which longitudinal, circular, and oblique fibres may be seen, although separate layers cannot be distinguished (P1. 2, figs. 6-8). This muscle is quite distinct from that of the walls of the ejaculatory ducts. As the ducts pass forwards into the crest, there lies behind them in the median plane a thick bar of muscular tissue which blends anteriorly with the posterior part of the sheath and which posteriorly appears to be continuous with the concentric muscle. In the crest, this bar, together with the posterior half of the sheath, assumes a 'Y' shape (P1. 3, fig. 9). The limbs of the 'Y' extend to the urethral submucosa, and the crest is thus divided into an anterior part, containing the terminations of the ejaculatory ducts and utricle, and a posterior, divided by the stem of the ' Y' into two halves, each containing the ducts of the prostatic glands. At this level the amount of smooth muscle in the submucosa of the anterior urethral wall increases. Both longitudinal and transverse fibres are present, the latter being especially prominent opposite the openings of the ejaculatory ducts and prostatic utricle (PI. 3, fig. 9). They are continuous with the transverse fibres noted in the proximal segment. The concentric fibres in the upper part of this segment form a thick mass behind the urethra. As the ejaculatory ducts and prostatic utricle pass forward to their terminations thev traverse this muscle. That part anterior to the ducts terminates at or above the level of their entrance into the urethra (P1. 3, fig. 10). The much thinner posterior part generally persists, although in an attenuated form, into the next segment of the urethra. Distal part Immediately below the level of entrance of the ejaculatory ducts and prostatic utricle into the urethra the muscle of the crest still retains its 'Y' shape. With the gradual disappearance of the utricle and ducts, the limbs of the 'Y' approach one another and fuse in the midline, the anterior end of the bar so formed being immedi- ately deep to the urethral submucosa (P1. 3, fig. 11). This bar persists, although of diminishing height, to the lowest part of the prostatic urethra (PI. 3, fig. 12). In this part, the amount of circular muscle surrounding the urethra increases considerably (P1. 3, figs. 11, 12). In five cases out of seven it is directly continuous with the concentric muscle referred to above, although the connexion immediately below the openings of the ejaculatory ducts is but a tenuous one. The fibres of the muscle arise entirely in the stroma of the prostate in the antero-lateral region, generally a short distance from the mid-line. As noted previously, striped fibres are present in this segment of the urethra. They are most numerous anteriorly, but a few pass backwards to the lateral and occasionally the posterior aspects of the urethra.

22 Anat. 91 348 E. J. Clegg

DISCUSSION The smooth muscle of the prostatic urethra Apart from Griffiths (1891) and Scher (1950) who considered that there was no sphincter at the bladder neck (although the latter author considered that the fibro- muscular tissue of the prostate as a whole could act as one), all previous authors are agreed that some type of sphincter muscle exists in this position. Most workers agree with Henle (1866) that the bladder neck sphincter is continu- ous above with the circular muscle of the bladder and that its fibres pass obliquely downwards and forwards on either side of the internal urinary meatus to become continuous with one another anterior to the urethra. Pettigrew (1867), von Ebner (1902), Eberth (1904) and Young & Wesson (1921) were of this opinion, and Griffiths (1889) stated that circular muscle fibres from the bladder could be traced into the urethra, but Walker (1899) and McCrea (1926) considered that these fibres ended at the internal urinary meatus. Testut & Latarjet (1949) regarded the 'smooth sphincter' at the bladder neck as resembling an inverted cone, continuous with the bladder musculature, and traversed from base to apex by the urethra. They con- sidered it to be histologically distinct from the bladder musculature. Lowsley (1930) and Graning (1936) found that fibres from the anterior longi- tudinal muscle layer of the bladder pass round the urethra in a postero-inferior direction; these fibres were continuous with those of the opposite side behind the urethra. The present findings agree with the last two authors in that the main musculature ofthe upper part ofthe prostatic urethra lies behind the urethra, and is partly derived from the anterior longitudinal muscle of the bladder. Its continuity with the trans- verse muscle of the trigone is also in agreement with Graning (1936). Thus there appears to be no anatomical sphincter at the bladder neck. From the functional point of view, however, such a muscle as the one described would have the effect of approximating the posterior to the anterior urethral wall, not only at the bladder neck but throughout the extent of the prostatic urethra, and it could therefore close the latter. The description of the structure of the urethral crest differs from that of Henle (1866) and Testut & Latarjet (1949). These authors described a mass of cavernous tissue lying immediately lateral to the fibromuscular 'skeleton' of the crest. The present findings do not substantiate this. The striped muscle of the prostatic urethra The extent to which voluntary fibres are concerned in the formation of the urethral musculature is in some dispute. It is agreed that the amount of striped muscle increases towards the apex of the prostate, but some authors consider that it is present in the upper part of the prostatic urethra. McCrea (1926) maintained that striped fibres were present in the trigone, Henle (1866), Walker (1906) and Young & Wesson (1921) found that the sphincter muscles at the bladder neck had a striped component, while Testut & Latarjet (1949) found fibres of their 'striped sphincter' as high as the neck of the bladder. In the present investigation no striped muscle fibres were present in the urethra The musculature of the human prostatic urethra 349 above the level of entrance of the ejaculatory ducts and prostatic utricle. The whole extent of the trigone of the bladder was never examined, but in no case were striped fibres seen in this situation. However, below the level of the entrance into the urethra of the ejaculatory ducts and prostatic utricle the number of striped muscle fibres progressively increases. Henle and most of the subsequent writers on the subject consider that a distinction can be made between the internal and external vesical sphincters both in their constitution and in their anatomical identity. The present findings do not completely substantiate this view. Although the muscle near the apex of the gland which corresponds to Henle's 'sphincter vesicae externus' contains striped fibres, its smooth component is similar in origin and distribution to the smooth muscle fibres in the upper part of the urethra (the fibres corresponding to Henle's 'internal sphincter') and the two groups of fibres are usually contiguous, although the muscle is always thinner below the openings of the ejaculatory ducts, and in a minority of cases an actual gap is present. In addition, the striped fibres are comparatively small in number and probably have little sphincteric action. It would seem more accurate, therefore, to regard the urethral sphincter as a single muscle which has a striped component below the openings of the ejaculatory ducts and prostatic utricle. The muscle in relation to the terminations of the ejaculatory ducts and prostatic utricle Little attention has been paid to the muscular arrangements in this situation. The presence or absence of muscle in the wall of the utricle has caused controversy; thus Walker (1899), von Ebner (1902), Eberth (1904) and Testut & Latarjet (1949) consider that it is present, while Stieve (1930) denies its existence. The present findings indicate that the muscle is more often absent; it may be that previous workers confused muscle in the common sheath of the duct and utricle with muscle in the wall of the utricle. With regard to the ejaculatory ducts, all authors except Eberth agree that muscle is present in the duct walls, but the presence of extra-mural muscle has received little attention. The suggestion that a sphincter may exist at the termina- tions of the ducts has been made by Finger (quoted by Walker, 1899); Eberth also noted the existence of circular and oblique fibres around the ducts. The present findings indicate that in the lower part of the sheath of the ducts there are both longitudinal and transverse muscle fibres, although proximally the sheath is com- posed of connective tissue with few, if any, muscle fibres. It could be contended that these fibres are concerned with the expulsion of the ejaculate, but their localization around the ends of the ducts and their extra-mural situation lead one to the hypothesis that they exert a sphincteric action on the ducts and utricle. Obviously some means of preventing the passage of into the ejaculatory ducts is necessary; Lowsley (1912) believed that a valve was present at their mouths. Indirect evidence for the presence of a closure mechanism has been provided by Macmillan (1952), who showed that in the rat ligation of the did not affect the rate of disintegration of spermatozoa in the tail of the .

22-2 350 E. J. Clegg

SUMMARY 1. The results of the examination of sections from seven prostate glands, stained by Masson's technique, are described. 2. Striped muscle fibres are found in that part of the prostatic urethra below the level of opening of the ejaculatory ducts and prostatic utricle. They increase in number towards the apex of the prostate, but never form a true sphincter within the gland itself. 3. Behind the urethra is a layer of transversely arranged smooth muscle which is thickest above and in front of the ejaculatory ducts. This muscle is continuous with the anterior longitudinal layer of the bladder, with the transverse muscle of the trigone and with the stroma of the prostate. Although not a true sphincter, it is considered that it may act as one. 4. The ejaculatory ducts and prostatic utricle are enclosed in a sheath which near their terminations contains much smooth muscle. It is considered that this muscle may exert a sphincteric effect on the ejaculatory ducts.

I am indebted to Prof. R. G. Harrison for his interest and advice. The sections were prepared by Miss B. Birkett, and the photomicrographs by Messrs L. G. Cooper and A. F. Taunton.

REFERENCES CLEGG, E. J. (1956). The vascular arrangements within the human prostate gland. Brit. J. Urol. 28, 428-435. EBERTH, C. J. (1904). Die mannlichen Geschlechtsorgane. In von Bardeleben: Handbuch der Anatomie des Menschen, 7. Band, 2. Abt., 2. Teil, pp. 65-71. Jena: Gustav Fischer Verlag. EBNER, V. VON (1902). In Koliker: Handbuch der Geweblehre des Menschen, 6. umgearb. Aufl., 3. Band, 402-505. Leipzig: W. Engelmann. GRANING, W. (1936). Beitrag zur vergleichenden Anatomie der Muskulatur von Harnblase und Harnrohre. Z. ges. Anat. 1. EntwGesch. 106, 226-250. GRIFFITHS, J. (1889). Observations on the anatomy of the prostate. J. Anat., Lond., 23, 374-386. GRIFFITHS. J. (1891). Observations on the and urethra. J. Anat., Lond., 25, 535-549. HENLE, J. (1866). Handbuch der systematischen Anatomie des Menschen, 2. Teil. Braunschweig: F. Viewig u. Sohn. LOWSLEY, 0. S. (1912). The development ofthe human prostate gland with reference to the develop- ment of other structures at the neck of the urinary bladder. Amer. J. Anat. 13, 299-350. LOWSLEY, 0. S. (1930). Embryology, anatomy and surgery of the prostate gland. Amer. J. Surg. 8, 35-43. MCCREA, E. D. (1926). The musculature of the bladder. Proc. R. Soc. Med. (Section of Urology), 19, 35-43. MACLEOD, D. (1942). The posterior wall of the prostate gland. Brit. J. Urol. 14, 153-171. MACMILLAN, E. W. (1952). Observations on the isolated vaso-epididymal loop and on the effects of experimental subeapital epididymal obstructions. Studies on Fertility, 6, 57-64. PETTIGREW, J. B. (1867). On the muscular arrangements of the bladder and prostate, and the manner in which the and urethra are closed. Phil. Trans. 157, 17-48. SCHER, S. (1950). Some observations on the anatomy of the bladder neck and posterior urethra with reference to prostatic obstruction. Brit. J. Urol. 22, 116-124. STIEVE, H. (1930). Der Vorsteherdruse. In von Mollendorf:Handbuch der mikroskopischen Anatomie des Menschen, 2. Teil, pp. 246-272. Berlin: Springer Verlag. TESTUT, L. & LATARJET, A. (1949). Traite d'anatomie humaine, Tome 5. Paris: G. Doin et Cie. Journal of Anatomy, Vol. 91, Part 3 Plate 1

CLEGG-THE MUSCULATURE OF THE HUMAN PROSTATIC URETHRA (Facing p. 350) Journal of Anatomy, Vol. 91, Part 3 Plate 2

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CLEGG-THE MUSCULATURE OF THE HUMAN PROSTATIC URETHRA The musculature of the human prostatic urethra 351 WALKER, G. (1899). Beitrag zur Kenntniss der Anatomie und Physiologie der Prostata nebst Bemerkungen uber den Vorgang der Ejaculation. Arch. Anat. Physiol., Lpz., PP. 313-352. WALKER, J. W. T. (1906). On the surgical anatomy of the prostate. J. Anat., Lond., 40, 188-209. YOUNG, H. H. & WEssoN, M. B. (1921). The anatomy and surgery of the trigon. Arch. Surg. 3, 1-37.

EXPLANATION OF PLATES All histological sections shown in the plates were stained with Masson's trichrome stain. PLATE 1 Fig. 1. Transverse section through a prostate just below the internal urinary meatus. The con- centric fibres passing behind the urethral lumen can be seen. x 12. Fig. 2. Transverse section through a prostate a short distance above the urethral crest. The thick bundle of vertically directed fibres anterior to the urethra can be seen. x 10. Fig. 3 Longitudinal section through the internal urinary meatus. Both anteriorly and posteriorly bundles of longitudinal fibres descend from the bladder into the urethra. They are very thick in front; behind they are much less well developed. The concentric muscle is seen posteriorly. The transversely directed fibres seen anteriorly are part of the prostatic capsule. x 12. Fig. 4. Transverse section through the ejaculatory ducts in the upper part ofthe prostate. Although their walls contain muscle, the sheath in which they lie is composed almost entirely of con- nective tissue. x 17. PLATE 2 Fig. 5. At a lower level in the same gland the lumen of the prostatic utricle can be seen to be surounded by darkly staining muscle fibres. The sheath now contains numbers of muscle fibres, which are distinct from the muscle in the duct walls. x 11. Fig. 6. In this section the ducts and utricle lie behind the urethral crest. Well-defined muscle fibres, in this case mainly circular, may be seen in the sheath. x 12. Fig. 7. The ducts and utricle have entered the urethral crest, and one of the ducts is opening into the urethra. On either side of the ducts numbers of longitudinally directed fibres may be seen. x9. Fig. 8. Longitudinal section through a prostate near the midline. The (ED.) can be seen passing towards the urethra (U.). Near its termination it is surrounded by a mass of muscle fibres (M.), the direction of which is oblique. x 12. PLATE 3 Fig. 9. Transverse section through a prostate at the point of opening of the prostatic utricle into the urethra. The 'Y'-shaped bar of muscle can be seen. A well-defined layer of circular muscle fibres lies immediately deep to the mucous membrane of the anterior urethral wall. x 10. Fig. 10. Longitudinal section through a prostate above the level of entrance of the ejaculatory ducts into the urethra. The concentric muscle can be seen to thin out inferiorly while the posterior longitudinal muscle continues into the urethral crest. x 14. Fig. 11. Transverse section through a prostate a short distance below the point of entry of the ejaculatory ducts into the urethra. The median bar of muscle is seen. The circular muscle deep to the mucous membrane of the anterior urethral wall is well developed. x 10. Fig. 12. Transverse section through the apex of the prostate. The median bar is still present, and the concentric muscle forms an almost complete ring around the urethra. x 7.