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Three-dimensional architecture of the myosalpinx in the mare as revealed by scanning electron microscopy.

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THE ANATOMICAL RECORD 267:235–241 (2002)
Three-Dimensional Architecture of
the Myosalpinx in the Mare
as Revealed by Scanning
Electron Microscopy
ANTONINO GERMANÀ,1 ROSA CASSATA,2 SANTO CRISTARELLA,2
AURELIO SCIRPO,2 AND UGO MUGLIA1*
1
Department of Morphology, Biochemistry, Physiology, and Animal Productions,
Morphology Section, Veterinary Faculty, University of Messina, Messina, Italy
2
Department of Surgery, Physiopathology, and Animal Reproduction Clinic,
Veterinary Faculty, University of Messina, Messina, Italy
ABSTRACT
The three-dimensional architecture of the myosalpinx in the mare was
investigated by means of scanning electron microscopy (SEM) after removal
of interstitial connective tissue with NaOH digestion. In the extramural
portion of the tubo-uterine junction (TUJ), isthmus, and ampulla, the myosalpinx architecture is represented by a unique muscular structure which
runs from the mesosalpinx to the base of the inner mucous folds. This
unique muscular structure consists mainly of bundles of muscular fibers
independent of one another, which show a multiple spatial arrangement
and form a complex network. Such a muscular architecture is likely more
suitable for stirring rather than pushing the embryos and gametes through
the Fallopian tube. Anat Rec 267:235–241, 2002. © 2002 Wiley-Liss, Inc.
Key words: salpinx; smooth muscle cells; mare; ovum transport;
scanning electron microscopy
In previous studies (Vizza et al., 1991, 1995; Muglia et
al., 1991a,b, 1992, 1996a,b, 1997a,b) we demonstrated
how direct observation of the myosalpinx structure (after
removal of the interstitial connective tissue) under a scanning electron microscope (SEM) can help resolve the problem of contradictory data in the literature, which results
from observation of bidimensional specimens. The most
recent studies based on the direct observation of myosalpinx architecture (Muglia and Motta, 2001) further emphasized the need to clarify to what extent, if any, the
musculature deriving from the mesosalpinx (namely, the
extrinsic (salpinx) musculature (EXM)) is integrated in
the salpinx musculature (intrinsic musculature) (INM)).
This could help to ascertain whether the EXM has a role in
the transport of gametes in addition to the functions it has
in the pick-up of the oocyte from the ovary surface, and in
the “tube-locking” phenomenon (Blandau, 1969, 1973).
The literature available on EXM and INM of the mare is
based on bidimensional observations under light microscopy (LM). Bignardi (1948) described in the tubo-uterine
junction (TUJ) and the isthmus an INM constituted of
isolated, loosely distributed, circular bundles that intermingle with longitudinal bundles in the innermost layer.
These intermingled bundles form an inner architecture.
©
2002 WILEY-LISS, INC.
This inner architecture is lacking in the ampulla, which
shows a unique circular orientation of bundles. Schilling
(1962) suggested that the myosalpinx (INM) of Ungulates
may be constituted by spiral fibers running deeper from
the surface toward the base of mucous folds. The variable
pitch of such spirals would account for the differences in
the architecture of the myosalpinx between the tubal segments. Finally, Sisson (1973) described an outermost longitudinal layer (continuous with the muscle present in the
mesosalpinx); an innermost intrinsic circular layer in the
TUJ, isthmus, and ampulla; and a muscular sphincter in
Grant sponsor: University of Messina; Grant number: PRA
2222/1998.
*Correspondence to: Prof. Ugo Muglia, Department of Morphology, Biochemistry, Physiology and Animal Productions, Veterinary Faculty, University of Messina, Polo Universitario Annunziata, 98168 Messina, Italy. Fax: ⫹39-90-355246.
E-mail: ugo.muglia@unime.it
Received 14 December 2001; Accepted 27 March 2002
DOI 10.1002/ar.10105
Published online 00 Month 2002 in Wiley InterScience
(www.interscience.wiley.com).
236
GERMANÀ ET AL.
the TUJ (INM). In consideration of these controversial
data, as well as of the key role that the muscular architecture of a hollow tubular organ such as the Fallopian
tube plays in the mechanism of its contraction, we investigated the three-dimensional (3D) architecture of the
myosalpinx in the mare, with the aim of settling the
controversy on this subject with definitive data.
MATERIALS AND METHODS
Sixteen pluriparous mares, aged 8 years, were used.
The Fallopian tubes, collected immediately after slaughter, were dissected under a stereomicroscope and gently
stretched and mounted by means of thin needles on a
silicon plate in Krebs solution. This procedure was followed in order to observe the entire tube, respecting its
topography. The tubes from 12 mares (six in estrous and
six in anestrous) were processed for SEM. After dissection,
the Krebs solution was replaced by 2.5% glutaraldehyde in
0.1 M phosphate buffer for 48 hr. The following segments
were isolated from the stretched tubes, according to current anatomical and physiological classifications (Nilsson
and Reinius, 1969): TUJ, isthmus, and ampulla. The segments were incubated in 6N NaOH at 60°C, according to
Takahashi-Iwanaga and Fujita’s (1986) maceration technique, for 25 min. The digestion time was determined by
trial and error. After chemical treatment, fragments were
dehydrated in a graded series of alcohol, critical-point
dried, coated with 20 nm of gold-palladium, and examined
under a Cambridge Stereoscan 240 (SEM) at 20 kV. A
number of samples were further microdissected by ultrasonication during dehydration (Low, 1989) for 3–5 min at
20 kHz, in order to reveal the deepest muscular bundles.
The tubes from the remaining four mares (two in estrous
and two in anestrous) were processed for light microscopy
(LM). After they were dissected and stretched under the
stereomicroscope, they were fixed in 10% formaldehyde,
dehydrated in a graded series of alcohol, and embedded as
a whole in historesin. From the resin blocks, 5-␮m transverse sections were taken and stained with hematoxylineosin (H&E).
OBSERVATIONS
The stretched tubes in the mare average 25 cm in
length. Two muscular components can be distinguished
within the myosalpinx: 1) a musculature running within
the subperitoneal connective tissue (SCT) of the mesosalpinx (EXM), and 2) a musculature peculiar to the salpinx
itself (INM)) (Fig. 1). In the following sections the myosalpinx architecture is described going from the TUJ to the
ampulla, following the gradual decrease of its thickness.
Comparative observations between specimens collected
from estrous and anestrous mares did not show any difference in the described myosalpinx architecture in any
segment of the tube (TUJ, isthmus, and ampulla).
TUJ
Extrinsic musculature
SEM. The fibers are elongated, regularly outlined (in a
relaxed stage), and joined in single, thick, loosely distributed, cylindric bundles, which follow a roughly longitudinal or oblique course. These bundles originate from the
mesosalpinx, and reach and run along the surface of the
underlying INM; they often bifurcate and anastomose
along this course (Figs. 2 and 3).
LM. In the outer musculature of the salpinx, the bundles observed under SEM appear, in transverse sections
by LM, cut transversely or obliquely. These bundles are
mixed together with the musculature present within blood
vessel walls sectioned along different cutting planes
(Fig. 6).
Intrinsic musculature
SEM. At different levels, bundles of EXM musculature
of various length describe wide curves, changing their
orientation and distributing transversely with respect to
the major axis of the tube at different levels (Fig. 4). These
bundles unravel at their extremities, merging into a circular compact coat (Fig. 5). The latter, therefore, appears
mixed at different levels together with longitudinal and
oblique bundles of EXM musculature. In a relaxed stage,
the fibers of these bundles appear elongated and regularly
outlined. The blood vessels that run within the myosalpinx are enveloped by a dense coat of irregularly outlined,
roughly longitudinal muscle fibers (intrinsic vascular
musculature) independent from the surrounding INM.
This intrinsic vascular coat sometimes envelopes two parallel vessels.
LM. Observed by LM, the wide, curved bundles mixed
into the compact circular coat observed under SEM appear
in transverse sections of the tube cut longitudinally or
obliquely mixed at different levels inside a circular coat
(Fig. 6). Furthermore, the intrinsic vascular muscle coats
can be seen tangentially cut for a variable length within
the INM.
Isthmus
Extrinsic musculature
SEM. The EXM appears constituted (as in the TUJ) by
elongated, quite regularly outlined (in a relaxed stage)
muscle fibers joined in isolated, variously oriented bundles that are more densely distributed than in the TUJ.
These cylindrical bundles lean against the periphery of
the INM and anastomose (Fig. 7). The blood vessels that
run within the myosalpinx show a musculature with features similar to those of the TUJ.
LM. The myosalpinx shows the same basic structure as
in the TUJ, although it is thinner and has less obliquely
cut bundles (Fig. 9).
Intrinsic musculature
SEM. The elongated fibers form cylindrical bundles. As
in the TUJ, these show an outer roughly longitudinal
course and change to an inner direction. They follow a
wide curve, distributing transversely or obliquely with
respect to the major axis of the tube (Fig. 8), and unravel
at their extremities, forming a roughly circular coat. The
fiber bundles can often be seen leaving from the main
bundles to form small plexuses. The blood vessels that run
within the myosalpinx show an INM with features similar
to that in the TUJ.
LM. The myosalpinx appears less thick with respect to
the TUJ. The bundles described by SEM appear constituted, in transverse sections, by segments of oblique bundles immersed in a coat of circular fibers.
Fig. 1. General view of the intramural (i) and extramural (e) portions of
the myosalpinx of the TUJ: uterine horn (u), peritoneum (p), and subperitoneal connective tissue (s). SEM, 20⫻.
Fig. 2. Extramural portion of the TUJ. EXM: longitudinal and oblique
muscle bundles (asterisks). SEM, 120⫻.
Fig. 3. Extramural portion of the TUJ. EXM: bundles of SMC fibers
bifurcate and anastomose repeatedly (asterisk), merging into the underlying INM (arrows). SEM, 310⫻.
Fig. 4. Extramural portion of the TUJ. EXM bundles (arrow) of SMC
fibers describe wide curves, change their orientation, and merge into the
underlying musculature. SEM, 210⫻.
Fig. 5. Extramural portion of the TUJ. INM: SMC fibers of the circular
coat. SEM, 1430⫻.
Fig. 6. Comparative histology of the Fallopian tube. Transverse
section of the extramural portion of the TUJ: longitudinal and oblique
muscle bundles (arrows), wide curves of muscle bundles (twin arrow),
and circular muscular coat (asterisks). LM, H&E, 140⫻.
238
GERMANÀ ET AL.
Fig. 7. Isthmus. Extrinsic musculature: oblique muscle fiber bundles
(asterisks), peritoneum (p), and subperitoneal connective tissue (s). SEM,
380⫻.
Fig. 8. Isthmus. Intrinsic musculature: SMC fiber bundles change
their orientation from outer, roughly longitudinal to inner circular (double
arrow). SEM, 90⫻.
Fig. 9. Comparative histology of the tube. Transverse section of the
isthmus. Extrinsic musculature: isolated, oblique muscle bundles (arrows).
Intrinsic musculature: circular coat (double arrow) mixed with oblique bundles (asterisks). Subperitoneal connective tissue (SCT). LM, H&E, 340⫻.
Fig. 10. Ampulla. Plexiform architecture of the intrinsic musculature.
SEM, 530⫻.
3D ARCHITECTURE OF THE MYOSALPINX IN THE MARE
239
Fig. 11. Comparative histology of the tube. Transverse section of the ampulla. Loose SCT; intrinsic musculature: muscle fiber bundles cut along different planes; mucous epithelium (asterisk). LM, H&E, 160⫻. The diagram
summarizes the 3D architecture of the myosalpinx as revealed by SEM after maceration. J, extramural segment
of the TUJ; I, isthmus; A, ampulla. Extrinsic musculature (arrows); intrinsic musculature (i).
Ampulla
Extrinsic musculature
SEM and LM. Only rare, isolated muscle fibers are
observed.
Intrinsic musculature
SEM. The bundle and fiber shapes are similar to those
observed in the isthmus. These loosely distributed bun-
dles run across multiple planes and intersect, giving rise
to a plexiform architecture (Fig. 10). The blood vessels are
enveloped by the muscular coat, as previously described in
the isthmus.
LM. The musculature is considerably decreased in
thickness compared to the previously described segments.
The bundles of fibers observed under SEM as plexiform
structures appear to be constituted by oblique segment
fibers under LM (transversal section) (Fig. 11).
240
GERMANÀ ET AL.
DISCUSSION
The myosalpinx is generally constituted by an EXM
originating from the broad ligament, and by a more conspicuous component that is peculiar to the myosalpinx
(INM) (Muglia and Motta, 2001). In the mare, these two
components are represented by a unique muscular structure that runs from the mesosalpinx to the base of the
inner mucous folds (see diagram, Fig. 11). In this mammal, therefore, the terms EXM and INM have exclusively
a topographic meaning. In this muscular complex our
results show an EXM composed of single, thick, oblique
and/or rather longitudinal bundles of fibers (described by
Bignardi (1948) as plexiform, and by Sisson (1973) as
longitudinal), which gradually lose their individuality as
they reach the ampulla. Here the EXM consists of rare,
isolated fibers. The INM consists of plexiform, loosely distributed bundles in both the isthmus and ampulla, which
form an inner, compact, circular coat in the TUJ and
isthmus. These bundles have been described as circular,
or circular and longitudinal (Sisson, 1973), or (in Ungulates) as spirals (Schilling, 1962). However, the results of
the present SEM study support our previous observations
in the cow, sheep, and sow (Muglia et al., 1996b, 1997a,b),
suggesting that the architecture of the IXM and EXM
myosalpinx in the mare is mainly plexiform.
The present findings do not invalidate the available
data on the myosalpinx architecture in the mare; rather,
they complete the data by providing a clear, topographical,
3D view of these features. In fact, the circular coat, the
outer circular and inner longitudinal layers, and the spiral
architecture reported by Sisson (1973), Bignardi (1948),
and Schilling (1962), respectively, in the TUJ, isthmus,
and ampulla correspond (according to our SEM results) to
those oblique bundles of variable length and direction that
run across multiple cellular planes and form a plexiform
structure. Therefore, the disagreement in the literature
about the structure of the mare myosalpinx may very
likely arise from different interpretations of histological
data. In fact, the observation of bidimensional sections by
LM may be misleading when a 3D plexiform structure
such as that of myosalpinx has to be described exactly.
The muscle fiber bundles may appear obliquely, longitudinally, or unevenly circularly arranged depending on the
plane of the sections, which only rarely are perfectly
transverse. Moreover, the relative proportion of fibers and
bundles following different spatial directions within a
transverse section of a plexiform structure (such as the
myosalpinx) may vary greatly, further affecting interpretation of the data.
On the basis of our observations, and in relation to the
morpho-physiological classification by Muglia and Motta
(2001), the mare has a sphincter-like, type-b TUJ (plexiform and with a unique, complex EXM-INM) like that in
the woman and cow, and a type-2 isthmus (plexiform and
with a unique, complex EXM-INM) like that in the rabbit,
ewe, and sow, as well as in the woman and cow. The
sphincter-like TUJ is characteristic of species that have
an intravaginal deposition (in the horse the penis does not
intrude beyond the vagina (Day, 1942; Parker et al.,
1975)) so that the uterus and the uterine horns are not
directly subjected to the pressure of semen during mating.
Therefore, a first selection of sperm is performed by the
uterine cervix (Mann et al., 1956; Hunter, 1973; Polge,
1978). Thus, the TUJ, rather than functioning as a barrier
against the flow of seminal plasma (as in the sow, which
has a barrier-like TUJ) may have a more active role in
modulating the seminal flow, as evidenced by its complex
muscular architecture. In the type-2 isthmus the close
fusion of the EXM with the INM is in accord with the
existence of a unique mesosalpinx contractile system.
Therefore, one may reasonably assume a direct control of
the EXM over the INM in type-2 salpinxes (as in the
rabbit, ewe, sow, cow, and woman). This supports the
theory (Blandau, 1969, 1973) that the EXM has a primary
role in the transport of gametes, in addition to its role in
the “tube-locking” phenomenon.
It is widely accepted that myosalpinx contractions propagate randomly, producing a backward–forward egg motion (Daniel et al., 1975a,b; Talo and Hodgson, 1978), and
are transmitted, usually over short distances, from different pace-maker sites (Talo and Pulkkinen, 1982). These
data were also confirmed by studies that recorded the
random myoelectrical activity of the tube (Daniel et al.,
1975a; Hodgson et al., 1977; Hodgson and Talo, 1978; Talo
and Hodgson, 1978). Our observations show that the myosalpinx architecture of the mare (unlike that of hollow
organs with geometrically arranged musculature (e.g.,
gut) in which the orthogonal disposition of the smooth
muscle cells (SMC) is suitable to generate and coordinate
peristaltic movements in an antagonistic manner) is similar to that of other hollow organs with plexiform musculature (e.g., the gall bladder) (see Uehara et al., 1990, for
review). The contraction of such a plexiform SMC structure (Hodgson et al., 1977) may deform the tube wall,
generating a stirring process within the tubal lumen. As a
result of this stirring movement, the contact between the
hormones and nutrients contained in the tubal lumen, on
the one hand, and the gametes, zygotes, and embryos, on
the other hand, is intensified, resulting in correct fertilization and early embryo development (Motta et al.,
1994a,b, 1995, 1998, 1999). Finally, these mechanisms
may explain why a decrease in tube length can cause a
decrease in the percentage of pregnancies (McComb and
Gomel, 1979; Silber and Cohen, 1980; McComb et al.,
1981).
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