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Anatomy and Embryology A n a t E m b r y o l( 1 9 8 9 )1 8 0 : 5 7 7 - 5 8 2 1989 Q Springer-Verlag of humansphincterurethraemuscle The morphogenesis Miroslav Tichf 3, CS-l2800Prague2, Czechoslovakia Department olAnatomy,CharlesUniversity,MedicalFaculty,U Nemocnice Summary. The morphogenesisof the sphincter urethrae musclewas studiedin human ontogeny.Musclesof 65 em^ brvos and fetuses.7 newborns, 3 children and 3 adults of t I Uoitt sexeswere examined histologically and by means of microdissection.Three developmentalstagescan be recog'' nized in terms of morphogeneticevents,histogenesisand developmentof sexualdimorphism. In the sexuallyindifferent stage(up to approximately 50 mm crown-rump length)' the sphincter urethrae primordium is formed by a shallow arch apposedonly to the ventrolateralwall of the urethra' The primordium extends from the level of the urogenital diapliragm up to the vesicourethraltransition. It consists of a condensationof mononuclear cells.Myotubes appear in fetusesof 30 mm crown-rump length. During the second stage(until birth) sexual dimorphism developsin conjunction to the formation of the prostate and vagina. In this stage,the sphincterurethrae musclefibres gradually extend to the posterior wall of the urethra. At the sametime cranially siiuated muscle ltbres project to the lateral wall of the prostate, whereasin females caudally located muscle hbres attach to the lateral wall of the vagina. In this way the sphincterachievesthe sexuallydistinct form. The dehnitive arrangementdevelopsin the third morphogenic stage (after birth), in which a complete muscle ring is formed by encircling the urethra in the infraprostaticpart in males '' .) and in the upper, larger part of the sphincter in females. The sphincter urethrae muscle is located inside the sling of the puborectalismuscle in both sexes,but no muscle frbresconnectthem to one another.A part ofthe puborectal muscle fibres originates from the connective tissue plate lying on the ventral face of the sphincter in the level of the bladder neck.From this arrangementit can be suggested that fibres of the puborectalismuscleparticipatein the ensurenceof urinary continence. Key words: Sphincterurethrae muscle- MorphogenesisHuman pear some widely different views - even in textbooks of anatomy(Kriz 1985;Gray's Anatomy 1985). Opinions differ as to the description of the extent of this muscle both in the proximodistal direction, from the urogenital diaphragm up to the basisof the urinary bladder (Henle 1866; Young and Wesson 1921)or merely at the urogenital diaphragm level (Weigner 1934: Rolnick and Falck 1949), and with regard to the circumflerenceof the urethral wall. A complete encirclement o[ the urethra (Braus and Elze 1924),a dorsally open arch or a horseshoeshapedformation, particularly in the upper portion of the sphincter(Henle 1866; Oerlich 1980),were described. In terms of clinical urology the male m. sphincterurethrae envelops the membranous as well as a portion of the prostatic part of the urethra to form a concentric,dorsally "thinner" circle beneath the apex of the prostata gland. In the upper portion it curves in an arch adjoining the anterior side of the lower half of the prostate (Manley 1966).The upper and larger part o[ the female sphincter muscle surrounds the urethra completely while its lower part extendsto the lateral walls of the vagina (Krantz 1951). There are very few ontogenicstudiesof the m' sphincter urethrae in humans. Popowsky's study (1899) is too schematic and inadequatelytimed. Oerlich (1980)describessolely the male sphincter, and anyway only starts in fetuses 60 mm of the crown-rump length. This is too late to detect the early developmental changesof the sphincter primordium; changes that have not yet been described,similar to the description of the developmentof sexualdimorphism in this muscle,are still missing. The purpose of the present study is to contribute to the existing data on the m. sphincter urethrae and its relation to the neighbouring muscles,in particular, to the m. levator ani, whose development and relation to the m. sphincterani externuswere describedin our previous study (Tichj, 1984). Another purpose is to help reconcilethe existing contradictory views in terms of developmentand to learn more about the generalprocessof the morphogenesis of the striated sphincter. Introduction Material and methods The structure of the human sphincter muscle of urethra is seeminglyunproblematic.although in reality, there aP- For this study 65 embryosand fetusesof 18-320mm crownrump length, i.e., from 6 to 30 weeks post conception, 7 neonates,3 children and 3 adults of both sexeswere used. The histological specimens(48 embryos and fetuses,2 neo- OJJprintrequeststo: M. Tich! 578 nates,2 children.2 adults)werefixedin l0% formaldehyde, dehydrated, embeddedin paraplast, cut (mostly in series) in sagittal. frontal and transversalplanes,and stainedwith hematoxylin and eosin. In the rest of the samplesthe constituents of the muscle of the pelvic tloor were dissected under a stereomicroscope in the perinealapproach. Results The smallest embryo of our series (18 mm crown-rump length, 6th week of embryonic development)had the primordium of the m. sphincter urethrae (SU) formed by a shallow arch made up of denselyclusteredcells and adjoining the anterior wall of the urogenitalsinus (Fig. 1). As early as that, the primordium is visibly distinct from the primordia of the neighbouringmuscles. A sagittal section of embryonic pelvis clearly suggests that from the early stagesof ontogeny the primordium of the SU is a relativelyhigh structure adjoining the primitive urethra (Fig. 2). The lower margin of the SU primordium is constituted of a paired condensationof cells situated on either side of the urethra. The most caudal margins of the condensations are poorly detectablein the concavity of the upper margin of the arch-like primordium of the m. bulbocavernosus(Fig. 3A). More proximally (Fig. 3 B), the condensationsof the SU are well visible. A transversesectionshows them as having a more or lesstriangular shapeand projecting in the ventral direction. Dorsally, the primordium of the m. levator ani is presentat this level. At the more cranial level both condensationsof the SU are joined by the muscleprimordium which forms an arch on the anterior side of the pelvic part of the urethra (Fig. 3C). The primordium of the puborectal part of the Ievator ani is situated lateral to and separatedfrom the SU primordium by a discerniblestreakof connectivetissue. At the level of the vesicourethraltransition (Fig.3D) the muscle layer of the SU primordium becomesthinner. At this level the SU primordium is situated inside the forkshapedpuborectalpart of the m. levator ani. Close in front of the SU there is a connective tissue plate from which a part of the puborectalmusclefibres originates. The anterior part of the SU primordium reachesthe anterior wall of the urinary bladder. The SU primordium quickly losesits original thickness,the arch becomesshorter until eventually the primordium disappearsaltogether. The situation towards the end of the indifferent period of ontogeny is summarizedin the diagram in Fig. 4, resulting from our study of serial sections of the pelvis from a fetus of 50 mm crown-rump length. The SU is shaped as an arch adjoining the urethral walls anteriorly and laterally and accompanyingthem from the level of the upper margin of the bulbocavernosus muscleprimordium to the vesicourethraltransition(Fig. aA). Most of the height of the sphincteris localizedinsidethe puborectalmusclefork with only its lower portion reachingbeyond the lower edge of this fork. A part of the levator ani muscle fibres originates in a connectivetissueplate lyin-ein front of the SU at the level of vesicourethral transition(Fig.4B). The SU primordium is situated close to the primordium of the m. bulbocavernosus and m. levator ani, though visibly separated flrom them by connectivetissue. In the subsequentperiod the SU primordium develops '!'.t 'I pelvis(18 mm crown-rump Fig. l. Transvcrse scctionol'cmbr-u"onic lcngth).Thc rn. sphinctcrurcthrae(.rrr)primordium exhibits the shapcol'a shallowarch adjoiningthe sinusurogenitalis(L) anter. E. x 80 i o r l i r .R . r e c t u r r :P . p u b i cb o n cp r i m o r d i u m H F ' i g . 2 .S a g i t t a ls c c t i o no l ' c m b r v o n i cp e l i i s ( 1 8 m r n c r o w n - r u m p length) at paraurethrallcvcl. M. sphinctcrurethrae(.ru)prtmorby a high lirrrnirtionadjoininuthe urethralprimordiurn is li.lrrnccl . E, x ll0 c l i u r n( t ) a n t c r i o r l vP . . p u b i cb o n cp r i m o r d i u m H i n c o n n e c t i o n w i t h s e x u a ld i f f e r e n t i a t i o nm a r k e d b y t h e d e v e l o p m e n t o t ' t h e p r o s t a t eo r t h e v a g i n a .T h e m u s c l e p r i m o r d i u m c o n t i n u c s t o c l r a n g ci t s s h a p e .T h e s p h i n c t e r i n m a l e t ' c t u s c sr c a c h c s t h c h o r s c s h o e s h a p e ( F i g . 5 ) b e n e a t h t h e apex ol- the prostatc. and in t'emale fetuses by the upper, h i g h e r p a r t o l ' t h c s p h i n c t c r a t a s t a - s eo f a p p r o x i r n a t e l y 1 5 0 m r n c r ( ) w n - r u r n Dl c n s t h . 579 j ,.,P .,r, 'l:'.1... 'HH. ' $.*.: , d.h'' ! : l -ti:h b. I t : . t , i D I r; . i, l i $: r, Ti, primordium F i g . 3 A - D . T r i r n s r . c r s cs c c t i r - r r .9r sl ' p c l r i s o l ' f c t u s ( 4 5 m m c r o w n - r u m p l e n g t h ) m a d c i n c l i l ' l c r c n t l c i ' c l s o l ' r n . s p h i n c t c r u r e t h r a c a tlpical stellate d . " . o n r t r " t " i t s s h a p c u n t l r c l a t i 6 n i g r h c n e i _ s h b o u r i n gs t r u c t u r e s . A A s e c t i o n a t u r o g c n i t a l d i a p h r a g n r l c v c l c x h i b i t i n g (.fi/) rcprcscntcd at this level by paired shapc ol' thc ,rct5iu tt ). Thc rn6st riistal margin oi the m. sphincter urcthrac pritrtorcliutn primordium c o n d e n s a t i o n s r r l ' c c l l s i s s r t u l t c ( l l a t c r a l t o t h c u r e t h r a ( [ ) a n d p i o x i m a l t o t h c u p p c r t D a r g i n o l ' t h c b t t l b o c a v c r n o s u sm u s c l e proximally, x 8 0 M o r c 8 ( : ; a e l . p u b i c l l E . b t l t l c : R ' r c c t u l ' n : / ' . e i t e r n u s a n i (bt). dorsallr i.ining thc lrcli6tcnts ttl'thc m. sphincter ([') and projecting t h e p r r m o r t l i ' r , o l ' t h c p r . s p 5 i l c t c r u r c t l r r a e( . r a ) i s m a d e u p o f c l u s t e r so l ' c e l l s s i t u a t c c ll a t c r a l I r r t l t c t r r c t h r a ( . f u )p r i m o r d i u m vcntrally. R. rcctunr: /r. putric bonc: [r. m. lcvator ani. HE, x80. C Still rnorc prorintalll'. thc nr. sphinctcr urcthrae p a rt of m. levator p u b o r c c t a l o l ' t h c T l r c r c r r t r a l r u r s i n w a l l . i t s l b r m s a n i r r c h o r r t h c u n t c r i t r r $ u l l o l ' t h c u r c t h r a ( [ - ) i n t e g r a t e di n a n i ( 1 z r )p r i m o r d i u r l i s 6 p c i t l r c r : r d c t r l r h c u r e t h i a . R . r i c t u m l P , p u b i c b o n c . H L i . x f i 0 . D T h c p r i r n o r d i u m o f t h e m . s p h i n c t e r the arms of u r c t h r a c ( . s r r )i s c l i s c c r n i h l l t h i p n c r i r t r h c v c s l c o u r e t h r a jl u n c t i o n l c v c l . T h c p r i n r t t r t l i u t n o l ' t h c s p h i n c t c r l i c s b c t w c c n of t h c p r i m o r d i u m o l ' t h c p i r b o r c c t a l p 6 r t i 6 n o f t h c m . l e v i t o r a n i ( l u ) . P : r l o l ' t h c l c v u t o l ' l i b r c s p r o . i c c t sl ' r o m t h c c o n d e n s a t i o n x h o r l c . l l 0 p u b i c I I I : ( L ) . P . r e c t u m ; ( ( / / ' , / / r . \ ) o u t s i d e R . p l u t c t i s s u c u r e t h r a the L h cc o n n c c t i v c 580 CTP sae Pr B Fig.4A, B. Schematicrepresentationof the m. sphincter urethrae primordium and its relation to neighbouring muscles, based on the studiesof a fetusof 50 mm crown-rump length; sa,m. sphincterurethrae;pr, puborectalpart of the m. levator ani ; Dc,m. bulbocavernosus; .rae,m. sphincterani externus:C?"P,connectivetissueplate; SI, symphysis In male fetuses,the superior part of the SU continues to retain the shapeofan arch anteriorly coveringthe prostatic part of the urethra and the prostate itself. In female fetuses,the upper part of the primordium is almost closed dorsally to the urethra, while in the lower part the complete encircling of the urethra is preventedby the vagina, which is in close contact with the dorsal urethral wall. The SU muscle bundles merge there with the lateral walls of the vagina. This SU relationship with the prostate and the lower part of the vagina remains unchanged even after birth. First in childhood the SU of both sexesacquires its definite shape. The lower, infraprostatic part of the SU in boys and the upper part of this sphincterin girls gradually grow to complete the ring-like muscular structure (Fig. 6). This pattern was seen in girls at 10, in boys at about 13 years of age. In the subsequentperiods of life the shapeofthe sphincterremainsunchangedin both sexes. Our histological study of SU developmentwas supplementedwith microdissectionof this and neighbouringmuscles in fetusesof both sexesof 190-320 mm crown-rump length.The fetal SU in both sexesis a relativelylargemuscle (Figs. 7-9). In male fetuses(Fig. 7) the SU covers the prostate and the infraprostatic part of the urethra. Betweenthe inferior margin of the sphincter and the bulbus corporis cavernosi the urethra is merely envelopedin a thin connectivetissue. In femalefetuses(Fig. 8) the substantiallylarger superior part of the SU adjoins the urethra alone. The smaller, inferior part of the sphinctercoversthe lateral vaginal walls. In both sexes,the SU is situated inside the puborectal muscle fork with only the lower part reaching beyond its lower margin (Fig. 9). On the anterior surface of the SU at the level of the vesicourethraltransition there is a plate of connective tissue from which part of the fibres of m. puborectalistake their origin. Discussion The coursd of morphogenesis,histogenesisand development of sexualdimorphism of the m. sphincterurethrae can be divided into three phases: 1. Indifferent phaseof development(up to 50 mm crownrump length, 10th week of gestation).SU muscle primordium forms a shallow arch adjoining the urethra from the urogenital diaphragm up to the vesicourethraltransition in both sexes.At first it is representedby condensation of myoblasts only (up to 30 mm crown-rump length); later on myotubes and muscularfibres are seen. 2. The phaseof sexualdimorphic development(until birth). This phase is related to the development of the prostate and vagina. The SU primordium spreadsout along the urethral wall gradually reachingits posterior wall in the infraprostatic part of the male and in the upper, larger part of the female sphincter.In the prostatic region it exhibits the shape of an arch anteriorly adjoining the urethra and the prostate. In female fetuses the lower part of the sphincter (about one-sixth) adjoins the anterior and lateral walls of the urethra and projects to the lateral walls of the vagina. 3. The phase of definite structuring (after birth). The SU relationship with the prostate and the lower part of the vagina reveals no further change. The infraprostatic part of the male sphincter and the upper, larger part of the female sphincter grow to complete a ring of muscle. These three phases correspond to the second, third and fourth phasesof muscle morphogenesis(separationof individual muscle primordia, their rebuilding and definite arrangement) as stated in the study of limb musculature (eihek 1972).Wedo not seecommon muscleprimordia (first phase according to einat; in the region of the pelvic outlet. In the smallestembryos of our series(18 mm crown-rump length) the muscleprimordia were alreadyindependentand well discerniblefrom neighbouringmuscleprimordia. Our observationof the SU structurein a 10-year-old girl correspondswith the descriptionof this musclein women as reportedby Krantz (1951),especiallyconcerningthe muscular ring in the upper portion, while on the lower part the sphincter musclebundles also surround the lateral walls of the vagina. On the gther hand, our hndings are at variance with classicaltextbooks(Gray's Anatomy 1985;Kriz 1985)describing the m. sphincterurethraeas a part of the urogenital diaphragm, as well as with classicalstudies.According to 581 ) ) Fig.5. Transverses,#tion of female fetus (190mm crown-rump length) at the level of the superior portion of the m. sphincterurethrae (sz). The sphincter shows.theshapeof a dorsally open horseshoewith a connectivetissue raphe (.1')dorsal to the ureihra (L). Arrows, connectivetissueplate giving rise to a part of the fibres of the m. levator ani; v, vagina-HE, i 41 Fig.6. Transversesection of the upper portion of m. sphincter urethrae (szi)in a lO-year-old girl. The sphincterforms a concentric circle around urethra (U). I/, vagina. HE Fig. 7' Anterolateral view of the m. sphincterurethrae (sr) in a male fetus (200 mm crown-rump length) after transsectionand openrng up of symphysis (^9).The sphincteriovers the anterior and lateral surfaces of the prostate ana itre pelvic parr of urethra (tn. i, connectivetissue plate covering the vesicourethraljunction anteriorly and giving rise io some of the fibres @)roxsSof the puborectal part of levator ani (/c). VIJ, urinary bladder; B, bulbus corporis cavernosi { r t1 trl lr lr (: Fig' 8' Anterolateral view of the microdissectionof the sphincter urethrae (.ra) in a female letus (210 mm crown-rump length) after transsectionand.opening up of symphysis(S). Most of ihe sphincter adjoins the urethra alone except lor the distal portion -bladder height (arrows)which joins the lateral walls of vagina |n. VU, urinary dies of EMG records from the m. sphincter urethrae as reviewed by Basmajian (1978). Studies describing the SU as being totally devoid of function (Elliot 1954; Tanagho and Smith 1966) are not supported by the above facts. Our discovery of the connective tissue plate which adjoins the anterior surface of the SU and which gives rise to some of the backward oriented muscle fibres of the m. levator ani provides a morphological basis for a possible role of the puborectal muscle in closing the urethra. This view is also supported by EMG examinations of the pelvic floor muscles (Basmajian 1978), as there is a simultaneously increased activity both in the m. sphincter urethrae and m. levator ani. Even though the m. levator ani adjoins the m. sphincter urethrae very closely, Gil Vernet (1968) and Krantz (1951) rule out any muscle fibre junction between the two muscles in both sexes. This view is supported by our findings, particularly related to the study of histological sections. References BasmajianJV (1978) Muscle alive. 4th ed., Williams and Wilkonis Co, Baltimore Fig.9. Perinealleft sideview of m. sphincterurethrae(sa) in a Braus H, Elze C (1924)Anatomie des Menschen.2. Band, Springer malefetus(320mmcrown-rump length)afterremovalof cavernose - Verlag, Berlin and spongiousbodiesof penisand resection of urethra(ti). The R (1972) Ontogenesisof skeleton and intrinsic musclesof Cihek sphincterliesinsidethe bifurcationof m. levatorani (la) reaching the human hand and foot. Erg Anat Entw-Gesch461:1-149 beyondit distally.Closeto m. sphincter urethraeliestheconnective Elliot JS (1954)Postoperative urinary incontinence. a revisedcontissueplate (arrov)givingrise to somemusclehbresof the m. ceptofexternal sphincter.J Urol"ll:49-57 levatorani Gegenbaur C (1883) Lehrbuch der Anatomie des Menschen.W EngelmannVerlag,Leipzig Gil Vernet S (1968) Morphology and function of vesico-prostatourethral musculature.Edizioni Canova Trevisco thesestudiespart of the musclesof the pelvic outlet, includCray's Anatomy (1985)ed. by Williams and Warwick, Churchill ing the urogenital diaphragm, should arise from the m. Livingstone,Edinbourgh-Melbourne-NewYork sphincter cloacae(Gegenbauer1883)and the m. sphincter Henle J (1866) Handbuch der systematischen Anatomie des Menurethrae should develop from the common blastema "m. schen.F Vieweg, Braunschweig sphincterurogenitalis" (Popowsky1899),which should-eive Krantz KE (1951)The anatomyof the urethraand anteriorvaginal rise to the urogenitaldiaphragm.According to our observawall. Am J Obstet Gynecol 62:374-386 tions, the m. sphincterurethrae is, from the early stages Kriz W (1985) Die harnableitenden Organe.In: FleischhauerK of ontogeny, an entirely independentprimordium with me(ed) Benninghoff: Makroskopischeund mikroskopischeAnatosenchyma visibly separatingit from the primordia of the mie des Menschen.2. Band, Urban und Schrvarzenberg, Miinchen-Wien-Baltimore,pp 45 l-460 neighbouring muscles.Throughout the period of ontogeny, Manley CB Jr (1966) The striated muscleof the prostate.J Urol only the m. bublocavernosus and m. levator ani are situated 95:234-240 in the vicinity o[ the m. sphincter urethrae. We observed Oerlich TM (1980) The urethral sphinctermusclein male. Am no muscle bundles which could be identified as those of J Anat 158:229-246 the m. transversusperinei superhcialisand profundus and Popowsky J (1899) Entwicklungsgeschichte der Dammuskulatur which would be in contact with the sphincter muscle. If beim Menschen.Anat Hefte 12:.1446 the m. sphincter urethrae, m. sphincter ani externus and Rolnick HC, Falk KA (1949)Anatomic study of the externalureother human muscles are. indeed. derived from the m. thral sphincter in relation to prostatic surgery. J Urol sphinctercloacae,then the processofsplitting oftheir indi61:591-603 Tanagho EA, Smith DR (1966)The anatomy and function of the vidual muscleprimordia from this common premusclemass bladderneck. Br J Urol 38:54-71 is no longer repeatedin human ontogeny. Moreover, the Tichj, M (1984)The developmentand organizationofthe sphincter sphinctersof the urethra and the anusdevelop at a different ani externus and the adjacent part of the levator ani muscle topographic levelsincethe lower margin of the m. sphincter in man. Folia Morphol Prague32:113-120 urethrae is situated at the level of the upper margin of Weigner K (1934) Topografick6 anatomie. III Topografie biicha. the m. sphincterani externus. Vesmir. Praha As shown by microdissection in the fetal phase,the m. Young HH, WessonMB (1921)The anatomyand surgeryol the sphincterurethraeis a powerful and well identifiablemuscle trigone.Arch Surg 3:1-37 designedto play a prominent role in the compressionof the anterior urethral wall. Our review is supported by stu- AcceptedAugust l, 1989