Download The morphogenesis of human sphincter urethrae muscle

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