Keio
J. Med.
24:
159-174,
1975
SCANNING ELECTRON MICROSCOPIC OBSERVATIONS ON THE SURFACE OF THE HUMAN FALLOPIAN TUBE AND UTERINE ENDOMETRIUM TAKEO
Department
ITO
of Obstetrics and Gynecology, School of Medicine, Keio University, Tokyo, Japan (Received
for publication
February
15, 1975)
ABSTRACT The surface of the human female reproductive electron microscope and the following results
1)
tract was observed were obtained.
by scanning
The lining epithelium of the Fallopian tube was composed with two cell types: the ciliated cells and the non-ciliated cells. The ciliated cells were most abundant on the fimbrial surface and showed the tendency to de crease in the number towards the utero-tubal junction. The lining cells of the Fallopian tube would secrete through the micro and macroaprocrine secretions.
2) 3)
On the uterine endometrium, centration, especially, around be suitable to transport the
4)
The non-ciliated cells showed the bulbous surface, the macroapocrine secretion, at the secretory phase. Scanning electron microscope is a powerful weapon to investigate in the field of the reproductive biology.
5)
the ciliated cells distributed in high con the opening of the uterine gland as it would secretions from the uterine glands.
INTRODUCTION
In recent into the buted there
years,
the
scanning
field of reproductive
electron
biology
microscope
and this
has
been
new technique
widely
applied
has deeply
contri
for the understanding of the details of cellular surface topography, whereas. have been rather few studies on the human female reproductive tracts
(Psychoyos et al.1 1971; Patek et al.2-6 1972; Ludwig et al.7 1972; Johannissonn et al.8 1972; Ferenczy et al.9 1972; Suzuki et al.10-13 1972-1975; Tanaka,14 1973 Oshima,17
1973).
However,
most
of them
point of anatomical view and the results of the technical difficulties. The
purpose
of
the
present
study
were
reported
mainly
were still imcompletely is 159
to
observe
the
from approved
ultrastructures
the stand because of
the
160
Taken
surface
of the
human
female
reproductive
tracts
MATERIALS
The specimens hysterectomy, mediately mens, hyde
washed
in 0.1 M phosphate
to about
5 mm square
part of the examination. 2 hours.
ethanol
baskets
and
put
was replaced The
After
solution
for 24 hours.
under
such were
as im
taking
the speci
(pH 7.4)
to remove
was done with 2.5% glutaralde
over night.
and 2 mm thick
tissues
Then,
they
The specimens
the dissecting
were
were
microscope.
rinsed
trimmed The small
specimens were diverted for the transmission electron microscopic The post fixation was done with 1% osmium tetroxide at pH 7.4 for
The specimens
absolute
purposes.
fixation
7.4)
for
microscope.
operations
The resected
and buffered
(pH
electron
gynecological
biopsy.
and the initial
(pH 7.4)
scanning
METHODS
and divided-for
buffer
solution
by
at the various
by cold saline
and blood debris,
in the buffered
AND
and endometrial
cut in the cold saline
they were
the mucus
were obtained
adnectomy
Ito
with
specimens
(JEE-4B)
were
dehydrated
and replaced
with
into
point
critical
liquid
were
carbon
coated
and observed
amylacetate. drying
dioxide with
by ascending
were
apparatus
and critical
carbon
in a JSM-S1
They
grades
and
of ethanol
placed
in the
(JCPD-3). point
gold
at accelerating
drying
in
small
Amylacetate was performed.
a vacuum
voltage
up to
evapolator
10 KV.
RESULTS
The fimbriated cells (Fig. 1). it was difficult (Fig.
2).
end of the fallopian
tube was mostly
covered
with the ciliated
The ciliated cells had a tendency to make irregular groups and to recognize individually because of their close arrangements
The surface
of the cilia was smooth
and no deformation
could be seen
(Fig. 3). The non-ciliated cells were arranged between the groups of the ciliated cells and the border of the cells was indistinct. The surface of the non-ciliated cells were not so protruded into the lumen. In the proliferative phase, the micro villi on the surface of the non-ciliated cells were rather short and of uniform length. 5:1. apical
The ratio In the surfaces
of the ciliated
secretory (Fig.
phase,
the
cells to the non-ciliated non-ciliated
cells
cells was approximately
showed
somewhat
distended
4).
The epithelium of the ampullary portion was composed of two cell types : the ciliated cells and the non-ciliated cells. The ciliated cells formed small groups alternating with clusters of the non-ciliated cells (Fig. 5). In the proliferative phase, short and moderately thick microvilli were packed closely over the surface of the non-ciliated cells. On the apical part of the microvilli, a small number of droplets could be seen (Fig. 6). The cell boundaries of the non-ciliated cells were
SEM
Observations
on Human
Oviduct
and
Endometrium
161
indistinct.
The surface pullary lumen
of the isthmic
portion
portion except more bulging (Fig. 7). The short microvilli
covering
the
surface.
In the secretory
The
phase,
of the non-ciliated
ratio
the same
appearances
cells to non-ciliated
substance
be seen
or apparent
(Figs.
(Fig.
secretory
stones
11). phase,
surface
secretions
of the mucosal
was not observed.
was covered
cell boundaries
the non-ciliated
only microapocrine structure
and their
The
horn cavity
formed
from
the
which
with
accurate
apical
part
prevents
The ratio of ciliated
1:7-8..
protrusions
was the uterine (Fig. 10). This
cells were sparse and the hexagonal pattern short
ridges.
cells did not show secretory
plicae
am
8, 9).
place was covered with the non-ciliated cells. The ciliated hardly observed. The cells were arranged tightly forming villi
cells was
cupola-like
The utero-tubal junction which formed the uterine side of the transitional part from oviduct to the uterine
like the paving
as the
tendency of the non-ciliated cells into the over the non-ciliated cells were numerously
of ciliated
the secreted
cells could
showed
and fine micro Despite
activity,
of microvilli.
the refluence
cells to non-ciliated
in
the
but showed The
valvelike
of the uterine
fluid
cells was approximately
1:100. The ciliated
luminal
surface
of
cells and relatively
non-ciliated
cells
the increased distribution
(Fig.
number
the
endometrium
few isolated
12).
The
openings
of the ciliated
was relatively
ciliated
regular.
was
covered
mainly
cells were present
of the
uterine
cells were observed The dents
became
with
scattered
glands
surrounded
as the deep dents. indistinct
non among by Their
in the secretory
phase with increasing and bulging of the cells near the openings (Fig. 13). The ciliated cells did not show any differences with the hormonal cycle. In the pro liferative phase, the surface of the non-ciliated cells were obviously flat and the microvilli Around
crowded
numerously
the openings
served.
The ratio of ciliated
secretory
phase, uneven
were bulging
undulated
13).
thin
and
long
secretion
(Fig. were
14). ob
cells was approximately
1:4. In the
in number
of ciliated
The gross
(Fig.
to make hemispherical
were
the microapocrine
cells increased
cells was 1:10-20.
and
surface
glands,
cells to non-ciliated
the non-ciliated
cells to non-ciliated became
on the
of the uterine
The
or dome-like
and the ratio
appearances surface
of the endometrium
of the
protrusions
non-ciliated
cells
and the cell bound
aries were distinct. to fuse each other
The microvilli were thick and short. They had a tendency making larger granular protrusions (Fig. 15). The surface
of the
cells,
non-ciliated
moreover,
bulbous projection which showed cells, there were the flat surfaced villi.
The ciliated
cells were
protruded
into
the
uterine
lumen
to form
the apocrine secretions (Fig. 16). Around these non-ciliated cells with long, thin and close micro
surrounded
by increased
non-ciliated
cells and com-
162
pressed
Takeo
by
the
Ito
latter.
DISCUSSION
Scanning electron microscope has been applied to the medical fields since 1962, and the technical progress has been strikingly rapid during the recent decade.16 The author had been trying to find the best methods for preparing the :soft tissues for scanning electron microscopic specimens , and reported the several findings.10-1s There have been reported several methods for washing the speci mens17 but it is still very difficult to decide the timing to stop washing the cell. In the early years, the single fixation using ordinary formaline or glutaraldehyde have been applied, but the deformations were occurred during fixation , dehydra tion and drying process.18 Then, the double fixation method using glutaraldehyde and osmium tetroxide has been proved to be the best method . The problem of -drying is the major difficulty for the scanning electron microscopic study . The air drying method affected the sever deformations on the cell surface .16-19 The author applied the critical point drying method20 that is able to dry the materials without forming the boundary of liquid and gas in order to prevent the destruc tion of the surface structures by the tension forces of liquid , and found to be the ideal technique for drying the specimens.7,14,17. The epithelial cells of the oviducts have been classified as follows : the ciliated -cell, the non-ciliated or secretory cell and the intercalary or peg cel121 In addi tion to the specific varieties, an "indifferent" cell lying at the base of the epithelial layer had been noted. An "indifferent" cell described by Pauerstein22 was con cluded that this might be a reserve cell and formed the basis for the replication ,of the epithelium . However, by the scanning electron microscopic study, an "in different" cell could not be observed. Tanaka14 reported in detail that the peg cell could be distinguishable from other cell types by the morphological charac teristics of the apical surface. The present author has identified the peg cell and the secretory cell as non-ciliated cell, but the classification between these two cell types could be made when the methods could be improved. The findings of the ratios of ciliated to non-ciliated cells from fimbria to the utero-tubal junction were in agreement with other reports2.7,23,24 The ciliated cells were most abun dant on the fimbrial surface and diminish toward the isthmic portion up to the utero-tubal junction, but on the endometrial surface the ciliated cells occurred nearly in the ratio similiar to that of ampullary or isthmic portions. On the sur face of the plica, Patek3 noted that the ciliated cells in the ampullary portion were preferably localized to the apical part of the folds, and at the basal part mostly the non-ciliated cells were found. Ferenczy9 noted that the ciliated cells
SEM
were
more
Observations
prominent
on
study,
there
was
crease
of the
non-ciliated
different of
no
tubal
gametes
the
cells
might
from
the follicle
oviduct.
that
fimbria
on the
the
wall
In
but
plica
the
the
the
of the
of
of
163
crypts.
plica,
bottom
significance
tubal
and
present
apparent
in
wall.
on
different
61%
an average
with their
the
The
bottom
transport
of
65%
of 65%
ciliated
cells on the
microscope
deciliation tioning
part
Recently of this
part.
abrupt
change
scribed
that,
in the revealed
of the fimbria
physiological
and matted
epithelium
that,
at the
and
were
seen as microapocrine than
transmission in secretory
of ova into the
with
cells on
less
than
44%
animals
observation
showed
(Figs.
con more
1, 2). on the ampullary
there
same
was
results
Hafez
small
and
cells. short
electron
microscopic
secretion phase36
(Fig.
ostium,
No
as the parti
there
(Fig.
folds
was
or villi. and
The surface microvilli
was composed
10).
characteristics usually
epithelium.
described,
Hafez32 The
an de
present
almost
all the
of the non-ciliated
(Fig.
11).
the secretory
Although activity
of two cell types : the
non-ciliated cells showed the most cycle, as was seen previously by studies23.34,35
in the microvilli 14).
portion
anatomical
cells did not show
of endometrium
cell.
environment
the tubal
no mucosal as
of this
study.
on the
internal
by the non-ciliated with
significance
the tubal
and
cells and the non-ciliated cells. The changes during the normal hormonal
light
would
and normal
important
from
endometrium
human, the
which
the ciliated
frequently
in this
published
in the secretory phase, the non-ciliated -lore than the microapocrine secretion. The lining
The present
environment
the
cells were composed was flat
the
have been
between
transfer
and fimbria
is a physiologically
Lisa31 reported
observation
cells.
could be observed
reports
Mastroi
5, 6). The meaning of this cell is not yet known investigation using transmission and scanning
junction
of the uterine
several
cells
cilium7,14,30 was visible
clarify
or ciliogenesis
The utero-tubal
cleaner
between
of ovum masses,
surface
thick
will
relations
ovum.
an ovum as it was released
cilia insured
on the
ciliated
ciliated
surface of the oviduct (Figs. well, but further comparative electron
released
and ovum transport using the experimental ovariec transport of egg masses occurred on the surface of
or more
The cell with single
the
did not work as a vacuum
to the report2S
with
is to pick-up
cells did not effect movement
tained
rather
the
Endometrium
lumen ; nor did they grasp
but the fimbria
According
ciliated
ciliated notable
in
of at the
cells
some
the fimbria
the surface of the fimbria tomized rabbits, the rapid
cells
observed
and
than
surface
of the fimbria
suck an ovum into the tubal
lining
summits the
ciliated
have
function
anni27,28 described
than
was
Oviduct
24,25,26
The main
the
on
of the
wall
Human
plical
difference
distribution
the
on
The surface
Some
apical
droplets
in the proliferative of the non-ciliated
phase cells
164
Takeo
was
somewhat
liferative other
flat and the
phase.
after
the
protrusions
microvilli
In the secretory cell surface
might
were
phase,
bulged
contain
Ito
the
thin
and relatively
the microvilli
like
a dome
substances
of
long in the
pro
and fused
each
were short
(Fig.
15).
various
These
cytoplasmic
mucoproteins
and
muco
polysaccarides which were supposed to constitute important nutrients for the blastocyst.1 After the apocrine secretion, the surface of the non-ciliated cells became
flat again
with
cell, Johannisson8 liferative
phase
blistered
during
and
the
phase.
in
The
uterine
the
will
the
concentration
results electron
more
be investigated
by
in the
the
detailed
but
with
morphological
in our
did
not
did
occur
the
occur,
the pro
rugged
but
and
cells could dif
around
of
secretory
the
the
the
investigators8,11,15,37
decrease
the
surrounding
cells
the
during
distributions
plateaus
ciliated glandular
openings
and
the
of
author
the ob
study. observations
the
were
be due to the technical
cells
ciliated
many
microscopic
cell,
the ciliated
during
of the ciliated
cells
geographical in
present
As for cilia
method.
the
of
reported
16)? erect structure
and it might
of ciliated
concentration
were
superficial
non-ciliated
that
(Fig.
of cilia,
The cyclic changes
study,
number
reported
of the
their
phase.
cells,to
greater
same
Scanning morphology scope,
ciliated
high
glands
and
and the drying
of the
of
were
ostia.
tained
decrease ratio
long microvilli
in the present
Ferenezy37
cells
drooping
at the fixation
The of
and
the cyclic changes
the secretory
not be observed ferences
thin
reported
ocmbination and
inform
us
only
of transmission
functional
characteristics
the
electron of
surface micro the
cell
laboratory.
ACKNOWLEDGEMENT
The author gratfully thanks to Associate Professor Shuetu Suzuki for his consistent instruction and suggestion in this work. The author thanks to Dr. Tatsushi Fujiwara and Dr. Mitsuma Hamada for their outstanding as sistance and also thanks to the staffs of the gynecological ward of the Keio University Hospital for their kindly cooperations. This work was partly sup ported by Grant M 67-79, M 69-144 and M 72-08c from the Population Coun cil, Rockefeller University and Scientific Research Grant from Japanese Min istry of Education 1974 to Dr. Shuetu Suzuki. This work was partly presented at the 60th Tokyo Regional Meeting of the Japanese Fertility Society in Tokyo, Japan (1972), the 18th Annual Meeting of the Japanese Fertility Society in Nagoya, Japan (1973), the 19th Annual Meeting of the Japanese Fertility Society in Kanazawa, Japan (1974) and at the 8th World Congress of Fertility and Sterility in Buenos Aires, Argentina (1974). REFERENCES 1.
Psychoyos, A. and Mandon, P.: the rat uterine epithelium during
Scanning delayed
electron microscopy of implantation. J. Reprod.
the surface of Fert. 26: 137
SEM
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139, 1971 Patek, E., Nilsson, L. and Johannisson, E.: Scanning electron microscopic study of the human fallopian tube. Report I. The proliferative and secretory stages. Fertil. & Steril. 23: 459-465, 1972 Patek, E., Nilsson, L. and Johannisson, E.: Scanning electron microscopic study of the human fallopian tube. Report ‡U. Fetal life, Reproductive life, and Post menopause. Fertil. & Steril. 23: 719-733, 1972 Patek, E., Nilsson, L., Johannisson, E., Hellema, M. and Bout, J.: Scanning elec tron microscopic study of the human fallopian tube. Report ‡V. The effect of midpregnancy and of various steroids. Fertil. & Steril. 24: 31-43, 1973 Patek, the
6.
Observations
E., human
The
effect
24:
832-843,
Nilsson,
L.
fallopian of
a
synthetic
and tube.
Hellema,
M.:
Report ‡W. progestin
Scanning
At on
the
term
electron gestation
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in
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the
study
of
puerperium.
Fertil.
&
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Patek, E. and Nilsson, L.: Scanning electron microscopic observations on the ciliogenesis of the infundibulum of the human fetal and adult fallopian tube epithelium. Fertil. & Steril. 24: 819-831, 1973 Ludwig, H., Wolf, H. and Metzger, H.: Zur Ultrastruktur der Tubeninnenfl?che im Rasterelektronenmikroskop. Arch. Gynak. 212: 380-396, 1972 Johannisson, E. and Nilsson, L.: Scanning electron microscopic study of the human endometrium. Fertil. & Steril. 23: 613-625, 1972 Ferenczy, A., Richard, R. M., Agate, Jr. F. J., Purkerson, M. L. and Dempsy, E. D.: Scanning electron microscopy of the human fallopian tube. Science 175: 783-784. 1972
Suzuki, S., Ito, T., Seki, K., Hamada, M. and Fujiwara, T.: World of scanning electron microscope. Reproductive tract, as the environments of fertilization and implantation. Igakunoayumi. 83: A319-A330, 1972 (in Japanese) Suzuki, S., Ito, T., Seki, K., Hamada, M. and Fujiwara, T.: Scanning electron microscopic observations of the surface ultrastructure of the reproductive tracts and the gametes. Obst. Gyne. Thera. 27: 337-346, 1973 (in Japanese) Suzuki, S., Ito, T., Seki, K., Fujiwara, T. and Hamada, M.: The oviduct. The surface ultrastructure of the human and rabbit endosalpinx. Obst. & Gyne. 41: 22-29, 1974 (in Japanese) Suzuki, S., Ito, T., Seki, K., Oyama, T., Tojo, R., Kobayashi, Y., Hamada, M. and Fujiwara, T.: Morphological characteristics of the surface of the human oocyte and the genital tracts. The cell. 7: 75-85, 1975 (in Japanese) Tanaka, M.: Scanning Electron Microscopic Study on the Human Endosalpinx. Adv. Obst. Gyne. 26: 213-256, 1973 (in Japanese) Oshima, M.: A scanning electron microscopic study on ultrastructure of the sur face of human endometrium. Adv. Obst. Gyne. 25: 163-180, 1973 (in Japanese) Tokunaga, J. and Hataba, Y.: The some problems in the preparation of biological specimens for SEM and interpretation of the SEM image. The cell. 3: 17-31, 1971 (in Japanese)
17.
Gould, K.: Preparation of mammalian scanning electron microscopy. Fertil.
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Tokunaga, J., Fujita, T. and lnoue, H.: Atlas of Scanning in Medicine. Igaku shoin, Tokyo, 1970 (in Japanese)
19.
Kanagawa, H., Hafez, E. S. E., Baechler, C. A. and Pitchford, W. C.: Improved Methodology for Scanning Electron Microscopy of the Female Reproductive Tract. Int. J. Fertil. 17: 75-80, 1972
20.
Tanaka, K.: A simple type of apparatus for critical point drying method. Micro. 21: 153-154, 1972 (in Japanese) Novak, E. R. and Woodruff, J. D.: Histology of Fallopian Tubes. In:
21.
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Gynecologic and Obstetric Pathology with Clinical and Endocrine Relations. Edited by Novak, E. R. and Woodruff, J. D. W. B. Saunders Company, Philadelphia and London, 1967, 250-258 Pauerstein, J. C. and Woodruff, J. D.: The role of the "indifferent" cell of the tubal epithelium. Am. J. Obst. & Gynec. 98: 121-125, 1967 Clyman, M. J.: Electron Microscopy of the Human Fallopian Tube. Ferti. & Steril. 17: 281-301, 1966 Gaddum-Rosse, human
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33.
34. 35. 36.
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Ito
P.,
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B.: Zoo.
Ciliary 188:
activity 269-275,
in
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Blandau, R. J.: Gamate Transport-Comparative Aspects. In: The Mammalian Oviduct. Edited by Hafez, E. S. E. and Blandau, R. J. The University of 'Chicago Press, Chicago and London, 1969, 126-162 Hafez, E. S. E.: Transport of spermatozoa in the female reproductive tract. Am. J. Obst. Gyne. 115: 705-717, 1973 Mastroianni, Jr., L.: The structure and function of the fallopian tube. Clini. Obste. Gynec. 5 : 781-790, 1962 Mastroianni; Jr., L.: The tube. In: Scientific Foundations of Obstetrics and Gynecology. Edited by Philipp, E. E., Barnes, J. and Newton, M. William Heine mann Medical Book LTD. London, 1970, 81-87 Odor, D. L. and Blandau, R. J.: Egg transport over the fimbrial surface of the rabbit oviduct under experimental conditions. Fertil. & Steril. 24: 292-300, 1973 Rumery, R. E. and Eddy, E.: Scanning Electron Microscopy of the Fimbriae and Ampullae of Rabbit Oviducts. Anat. Rec. 178: 83-102, 1973 Lisa, J. R., Gioia, J. D. and Rubib, I. C.: Observations on the interstitial portion of the fallopian tube. Surg. Gynec. & Obst. 99: 159-169, 1954 Hafez, E. S. E. and Black, D. L.: The mammalian Uterotubal Junction. In: The Mammalian Oviduct. Edited by Hafez, E. S. E. and Blandau, R. J. The Univer sity of Chicago Press, Chicago and London, 1969, 85-126 Nilsson, 0.: Electron Microscopy of the Glandular Epithelium in the Human Uterus. I. Follicular Phase. J. Ultra. Res. 6: 413-421, 1962. ‡U. Early and Late Luteal Phase. J. Ultra. Res. 6: 422-432, 1962 Wynn, R. M. and Harris, L. A.: Ultrastructural Cyclic Changes in the Human Endometrium. I Normal Preovulatory Phase. Fertil. & Steril. 18: 632-648, 1967 Wynn, R. M. Woolley, R. S.: Ultrastructural Cyclic Changes in the Human Endo metrium. ‡U Normal Postovulatory Phase. Fertil. & Steril. 18: 721-738, 1967 Hayashi, K., Hamanishi, S. and Ri, H.: Ultrastructural changes of the endo metrial surface at the implantation stage and it's hormonal control. Folia Endo. Tan 50: 813-827. 1974 (in Japanese) Ferenczy, Scanning & Steril.
A., Richart, R. M., Agate, electron microscopy of the 23: 515-521, 1972
F. J., Purkerson, human endometrial
M. L. and Dempsy, surface epithelium.
E. W.: Fertil.
SEM
Fig.
Fig.
1
2
The
Observations
crowded
ciliated
on Human
cells
Oviduct
and
Endometrium
are seen on the fimbrial
The strands or group arrangement on the fimbrial surface. (•~1000)
of the
ciliated
surface. (•~
and
167
1000)
non-ciliated
cells
168
Fig.
Takeo
3
Fig. 4
High magnification be seen. (•~ 10000)
of the
ciliated
Ito
cell.
No deformation
or no coagulation
Fimbrial surface in the secretory phase. The cell boundaries in the proliferative phase. (•~3000)
can
are not clear as
SEM
Fig.
Fig.
5
6
Lining
Luminal microapocrine
Observations
cells
cells
on
the
on
the
secretion
on
Human
ampullary
portion
ampullary can
Oviduct
portion be
seen. (•~3000)
in
and
the
in
Endometrium
proliferative
the
proliferative
169
phase. (•~1000)
phase.
Several
170
Takeo
Fig.
7
Lining surface
cells on the isthmic of the non-ciliated
Fig.
8
Isthmic portion 3000)
in the
Ito
portion in the proliferative cells. (•~3000)
secretory
phase.
Several
secretory
phase.
Note
activity
the bulging
can
be seen. (•~
SEM
Fig.
Fig.
9
10
High
Observations
magnification
on
Human
of the isthmic
Tubal ostia, the view ciliated cells. (•~300)
from
the
Oviduct
portion
uterine
and
Endometrium
in the secretory
lumen.
Note
the
171
phase. (•~10000)
sparseness
of the
172
Takeo
Fig.
Fig.
11
12
Ito
He(•~agonal cells in the utero tubal and small and the few microapocrine
Gross appearance Note the sharrow
of the corporal funnel-shaped
junction. The microvilli are short secretion can be seen. (•~3000)
endometrium in the proliferative gland openings. (•~200)
phase.
SEM
Fig.
13
Gross the
Observations
appearance
of
narrowing
Fig.
of
14
the
on Human
the
uterine
gland
and
endometrium Note
cells. (•~3000)
and
endometrium
openings
Fundal phase.
Oviduct
the
in the
in flat
Endometrium
the
surfaced
the
secretory
undulating
proliferative non-ciliated
173
phase.
surface. (•~300)
Note
174
Fig.
Takeo
15
Fig.
Ito
Luminal epithelium of the corporal endometrium in the secretory the granular microvilli bearing the apical surface. (•~3000)
16
phase.
Note
Luminal epithelium of the corporal endometrium in the secretory phase. Note the bulbously protruded cells and flat surfaced cell with long and vigorous microvilli. (•~3000)
J. Med.
24:
159-174,
1975
SCANNING ELECTRON MICROSCOPIC OBSERVATIONS ON THE SURFACE OF THE HUMAN FALLOPIAN TUBE AND UTERINE ENDOMETRIUM TAKEO
Department
ITO
of Obstetrics and Gynecology, School of Medicine, Keio University, Tokyo, Japan (Received
for publication
February
15, 1975)
ABSTRACT The surface of the human female reproductive electron microscope and the following results
1)
tract was observed were obtained.
by scanning
The lining epithelium of the Fallopian tube was composed with two cell types: the ciliated cells and the non-ciliated cells. The ciliated cells were most abundant on the fimbrial surface and showed the tendency to de crease in the number towards the utero-tubal junction. The lining cells of the Fallopian tube would secrete through the micro and macroaprocrine secretions.
2) 3)
On the uterine endometrium, centration, especially, around be suitable to transport the
4)
The non-ciliated cells showed the bulbous surface, the macroapocrine secretion, at the secretory phase. Scanning electron microscope is a powerful weapon to investigate in the field of the reproductive biology.
5)
the ciliated cells distributed in high con the opening of the uterine gland as it would secretions from the uterine glands.
INTRODUCTION
In recent into the buted there
years,
the
scanning
field of reproductive
electron
biology
microscope
and this
has
been
new technique
widely
applied
has deeply
contri
for the understanding of the details of cellular surface topography, whereas. have been rather few studies on the human female reproductive tracts
(Psychoyos et al.1 1971; Patek et al.2-6 1972; Ludwig et al.7 1972; Johannissonn et al.8 1972; Ferenczy et al.9 1972; Suzuki et al.10-13 1972-1975; Tanaka,14 1973 Oshima,17
1973).
However,
most
of them
point of anatomical view and the results of the technical difficulties. The
purpose
of
the
present
study
were
reported
mainly
were still imcompletely is 159
to
observe
the
from approved
ultrastructures
the stand because of
the
160
Taken
surface
of the
human
female
reproductive
tracts
MATERIALS
The specimens hysterectomy, mediately mens, hyde
washed
in 0.1 M phosphate
to about
5 mm square
part of the examination. 2 hours.
ethanol
baskets
and
put
was replaced The
After
solution
for 24 hours.
under
such were
as im
taking
the speci
(pH 7.4)
to remove
was done with 2.5% glutaralde
over night.
and 2 mm thick
tissues
Then,
they
The specimens
the dissecting
were
were
microscope.
rinsed
trimmed The small
specimens were diverted for the transmission electron microscopic The post fixation was done with 1% osmium tetroxide at pH 7.4 for
The specimens
absolute
purposes.
fixation
7.4)
for
microscope.
operations
The resected
and buffered
(pH
electron
gynecological
biopsy.
and the initial
(pH 7.4)
scanning
METHODS
and divided-for
buffer
solution
by
at the various
by cold saline
and blood debris,
in the buffered
AND
and endometrial
cut in the cold saline
they were
the mucus
were obtained
adnectomy
Ito
with
specimens
(JEE-4B)
were
dehydrated
and replaced
with
into
point
critical
liquid
were
carbon
coated
and observed
amylacetate. drying
dioxide with
by ascending
were
apparatus
and critical
carbon
in a JSM-S1
They
grades
and
of ethanol
placed
in the
(JCPD-3). point
gold
at accelerating
drying
in
small
Amylacetate was performed.
a vacuum
voltage
up to
evapolator
10 KV.
RESULTS
The fimbriated cells (Fig. 1). it was difficult (Fig.
2).
end of the fallopian
tube was mostly
covered
with the ciliated
The ciliated cells had a tendency to make irregular groups and to recognize individually because of their close arrangements
The surface
of the cilia was smooth
and no deformation
could be seen
(Fig. 3). The non-ciliated cells were arranged between the groups of the ciliated cells and the border of the cells was indistinct. The surface of the non-ciliated cells were not so protruded into the lumen. In the proliferative phase, the micro villi on the surface of the non-ciliated cells were rather short and of uniform length. 5:1. apical
The ratio In the surfaces
of the ciliated
secretory (Fig.
phase,
the
cells to the non-ciliated non-ciliated
cells
cells was approximately
showed
somewhat
distended
4).
The epithelium of the ampullary portion was composed of two cell types : the ciliated cells and the non-ciliated cells. The ciliated cells formed small groups alternating with clusters of the non-ciliated cells (Fig. 5). In the proliferative phase, short and moderately thick microvilli were packed closely over the surface of the non-ciliated cells. On the apical part of the microvilli, a small number of droplets could be seen (Fig. 6). The cell boundaries of the non-ciliated cells were
SEM
Observations
on Human
Oviduct
and
Endometrium
161
indistinct.
The surface pullary lumen
of the isthmic
portion
portion except more bulging (Fig. 7). The short microvilli
covering
the
surface.
In the secretory
The
phase,
of the non-ciliated
ratio
the same
appearances
cells to non-ciliated
substance
be seen
or apparent
(Figs.
(Fig.
secretory
stones
11). phase,
surface
secretions
of the mucosal
was not observed.
was covered
cell boundaries
the non-ciliated
only microapocrine structure
and their
The
horn cavity
formed
from
the
which
with
accurate
apical
part
prevents
The ratio of ciliated
1:7-8..
protrusions
was the uterine (Fig. 10). This
cells were sparse and the hexagonal pattern short
ridges.
cells did not show secretory
plicae
am
8, 9).
place was covered with the non-ciliated cells. The ciliated hardly observed. The cells were arranged tightly forming villi
cells was
cupola-like
The utero-tubal junction which formed the uterine side of the transitional part from oviduct to the uterine
like the paving
as the
tendency of the non-ciliated cells into the over the non-ciliated cells were numerously
of ciliated
the secreted
cells could
showed
and fine micro Despite
activity,
of microvilli.
the refluence
cells to non-ciliated
in
the
but showed The
valvelike
of the uterine
fluid
cells was approximately
1:100. The ciliated
luminal
surface
of
cells and relatively
non-ciliated
cells
the increased distribution
(Fig.
number
the
endometrium
few isolated
12).
The
openings
of the ciliated
was relatively
ciliated
regular.
was
covered
mainly
cells were present
of the
uterine
cells were observed The dents
became
with
scattered
glands
surrounded
as the deep dents. indistinct
non among by Their
in the secretory
phase with increasing and bulging of the cells near the openings (Fig. 13). The ciliated cells did not show any differences with the hormonal cycle. In the pro liferative phase, the surface of the non-ciliated cells were obviously flat and the microvilli Around
crowded
numerously
the openings
served.
The ratio of ciliated
secretory
phase, uneven
were bulging
undulated
13).
thin
and
long
secretion
(Fig. were
14). ob
cells was approximately
1:4. In the
in number
of ciliated
The gross
(Fig.
to make hemispherical
were
the microapocrine
cells increased
cells was 1:10-20.
and
surface
glands,
cells to non-ciliated
the non-ciliated
cells to non-ciliated became
on the
of the uterine
The
or dome-like
and the ratio
appearances surface
of the endometrium
of the
protrusions
non-ciliated
cells
and the cell bound
aries were distinct. to fuse each other
The microvilli were thick and short. They had a tendency making larger granular protrusions (Fig. 15). The surface
of the
cells,
non-ciliated
moreover,
bulbous projection which showed cells, there were the flat surfaced villi.
The ciliated
cells were
protruded
into
the
uterine
lumen
to form
the apocrine secretions (Fig. 16). Around these non-ciliated cells with long, thin and close micro
surrounded
by increased
non-ciliated
cells and com-
162
pressed
Takeo
by
the
Ito
latter.
DISCUSSION
Scanning electron microscope has been applied to the medical fields since 1962, and the technical progress has been strikingly rapid during the recent decade.16 The author had been trying to find the best methods for preparing the :soft tissues for scanning electron microscopic specimens , and reported the several findings.10-1s There have been reported several methods for washing the speci mens17 but it is still very difficult to decide the timing to stop washing the cell. In the early years, the single fixation using ordinary formaline or glutaraldehyde have been applied, but the deformations were occurred during fixation , dehydra tion and drying process.18 Then, the double fixation method using glutaraldehyde and osmium tetroxide has been proved to be the best method . The problem of -drying is the major difficulty for the scanning electron microscopic study . The air drying method affected the sever deformations on the cell surface .16-19 The author applied the critical point drying method20 that is able to dry the materials without forming the boundary of liquid and gas in order to prevent the destruc tion of the surface structures by the tension forces of liquid , and found to be the ideal technique for drying the specimens.7,14,17. The epithelial cells of the oviducts have been classified as follows : the ciliated -cell, the non-ciliated or secretory cell and the intercalary or peg cel121 In addi tion to the specific varieties, an "indifferent" cell lying at the base of the epithelial layer had been noted. An "indifferent" cell described by Pauerstein22 was con cluded that this might be a reserve cell and formed the basis for the replication ,of the epithelium . However, by the scanning electron microscopic study, an "in different" cell could not be observed. Tanaka14 reported in detail that the peg cell could be distinguishable from other cell types by the morphological charac teristics of the apical surface. The present author has identified the peg cell and the secretory cell as non-ciliated cell, but the classification between these two cell types could be made when the methods could be improved. The findings of the ratios of ciliated to non-ciliated cells from fimbria to the utero-tubal junction were in agreement with other reports2.7,23,24 The ciliated cells were most abun dant on the fimbrial surface and diminish toward the isthmic portion up to the utero-tubal junction, but on the endometrial surface the ciliated cells occurred nearly in the ratio similiar to that of ampullary or isthmic portions. On the sur face of the plica, Patek3 noted that the ciliated cells in the ampullary portion were preferably localized to the apical part of the folds, and at the basal part mostly the non-ciliated cells were found. Ferenczy9 noted that the ciliated cells
SEM
were
more
Observations
prominent
on
study,
there
was
crease
of the
non-ciliated
different of
no
tubal
gametes
the
cells
might
from
the follicle
oviduct.
that
fimbria
on the
the
wall
In
but
plica
the
the
the
of the
of
of
163
crypts.
plica,
bottom
significance
tubal
and
present
apparent
in
wall.
on
different
61%
an average
with their
the
The
bottom
transport
of
65%
of 65%
ciliated
cells on the
microscope
deciliation tioning
part
Recently of this
part.
abrupt
change
scribed
that,
in the revealed
of the fimbria
physiological
and matted
epithelium
that,
at the
and
were
seen as microapocrine than
transmission in secretory
of ova into the
with
cells on
less
than
44%
animals
observation
showed
(Figs.
con more
1, 2). on the ampullary
there
same
was
results
Hafez
small
and
cells. short
electron
microscopic
secretion phase36
(Fig.
ostium,
No
as the parti
there
(Fig.
folds
was
or villi. and
The surface microvilli
was composed
10).
characteristics usually
epithelium.
described,
Hafez32 The
an de
present
almost
all the
of the non-ciliated
(Fig.
11).
the secretory
Although activity
of two cell types : the
non-ciliated cells showed the most cycle, as was seen previously by studies23.34,35
in the microvilli 14).
portion
anatomical
cells did not show
of endometrium
cell.
environment
the tubal
no mucosal as
of this
study.
on the
internal
by the non-ciliated with
significance
the tubal
and
cells and the non-ciliated cells. The changes during the normal hormonal
light
would
and normal
important
from
endometrium
human, the
which
the ciliated
frequently
in this
published
in the secretory phase, the non-ciliated -lore than the microapocrine secretion. The lining
The present
environment
the
cells were composed was flat
the
have been
between
transfer
and fimbria
is a physiologically
Lisa31 reported
observation
cells.
could be observed
reports
Mastroi
5, 6). The meaning of this cell is not yet known investigation using transmission and scanning
junction
of the uterine
several
cells
cilium7,14,30 was visible
clarify
or ciliogenesis
The utero-tubal
cleaner
between
of ovum masses,
surface
thick
will
relations
ovum.
an ovum as it was released
cilia insured
on the
ciliated
ciliated
surface of the oviduct (Figs. well, but further comparative electron
released
and ovum transport using the experimental ovariec transport of egg masses occurred on the surface of
or more
The cell with single
the
did not work as a vacuum
to the report2S
with
is to pick-up
cells did not effect movement
tained
rather
the
Endometrium
lumen ; nor did they grasp
but the fimbria
According
ciliated
ciliated notable
in
of at the
cells
some
the fimbria
the surface of the fimbria tomized rabbits, the rapid
cells
observed
and
than
surface
of the fimbria
suck an ovum into the tubal
lining
summits the
ciliated
have
function
anni27,28 described
than
was
Oviduct
24,25,26
The main
the
on
of the
wall
Human
plical
difference
distribution
the
on
The surface
Some
apical
droplets
in the proliferative of the non-ciliated
phase cells
164
Takeo
was
somewhat
liferative other
flat and the
phase.
after
the
protrusions
microvilli
In the secretory cell surface
might
were
phase,
bulged
contain
Ito
the
thin
and relatively
the microvilli
like
a dome
substances
of
long in the
pro
and fused
each
were short
(Fig.
15).
various
These
cytoplasmic
mucoproteins
and
muco
polysaccarides which were supposed to constitute important nutrients for the blastocyst.1 After the apocrine secretion, the surface of the non-ciliated cells became
flat again
with
cell, Johannisson8 liferative
phase
blistered
during
and
the
phase.
in
The
uterine
the
will
the
concentration
results electron
more
be investigated
by
in the
the
detailed
but
with
morphological
in our
did
not
did
occur
the
occur,
the pro
rugged
but
and
cells could dif
around
of
secretory
the
the
the
investigators8,11,15,37
decrease
the
surrounding
cells
the
during
distributions
plateaus
ciliated glandular
openings
and
the
of
author
the ob
study. observations
the
were
be due to the technical
cells
ciliated
many
microscopic
cell,
the ciliated
during
of the ciliated
cells
geographical in
present
As for cilia
method.
the
of
reported
16)? erect structure
and it might
of ciliated
concentration
were
superficial
non-ciliated
that
(Fig.
of cilia,
The cyclic changes
study,
number
reported
of the
their
phase.
cells,to
greater
same
Scanning morphology scope,
ciliated
high
glands
and
and the drying
of the
of
were
ostia.
tained
decrease ratio
long microvilli
in the present
Ferenezy37
cells
drooping
at the fixation
The of
and
the cyclic changes
the secretory
not be observed ferences
thin
reported
ocmbination and
inform
us
only
of transmission
functional
characteristics
the
electron of
surface micro the
cell
laboratory.
ACKNOWLEDGEMENT
The author gratfully thanks to Associate Professor Shuetu Suzuki for his consistent instruction and suggestion in this work. The author thanks to Dr. Tatsushi Fujiwara and Dr. Mitsuma Hamada for their outstanding as sistance and also thanks to the staffs of the gynecological ward of the Keio University Hospital for their kindly cooperations. This work was partly sup ported by Grant M 67-79, M 69-144 and M 72-08c from the Population Coun cil, Rockefeller University and Scientific Research Grant from Japanese Min istry of Education 1974 to Dr. Shuetu Suzuki. This work was partly presented at the 60th Tokyo Regional Meeting of the Japanese Fertility Society in Tokyo, Japan (1972), the 18th Annual Meeting of the Japanese Fertility Society in Nagoya, Japan (1973), the 19th Annual Meeting of the Japanese Fertility Society in Kanazawa, Japan (1974) and at the 8th World Congress of Fertility and Sterility in Buenos Aires, Argentina (1974). REFERENCES 1.
Psychoyos, A. and Mandon, P.: the rat uterine epithelium during
Scanning delayed
electron microscopy of implantation. J. Reprod.
the surface of Fert. 26: 137
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Gould, K.: Preparation of mammalian scanning electron microscopy. Fertil.
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Tokunaga, J., Fujita, T. and lnoue, H.: Atlas of Scanning in Medicine. Igaku shoin, Tokyo, 1970 (in Japanese)
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Kanagawa, H., Hafez, E. S. E., Baechler, C. A. and Pitchford, W. C.: Improved Methodology for Scanning Electron Microscopy of the Female Reproductive Tract. Int. J. Fertil. 17: 75-80, 1972
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Blandau, R. J.: Gamate Transport-Comparative Aspects. In: The Mammalian Oviduct. Edited by Hafez, E. S. E. and Blandau, R. J. The University of 'Chicago Press, Chicago and London, 1969, 126-162 Hafez, E. S. E.: Transport of spermatozoa in the female reproductive tract. Am. J. Obst. Gyne. 115: 705-717, 1973 Mastroianni, Jr., L.: The structure and function of the fallopian tube. Clini. Obste. Gynec. 5 : 781-790, 1962 Mastroianni; Jr., L.: The tube. In: Scientific Foundations of Obstetrics and Gynecology. Edited by Philipp, E. E., Barnes, J. and Newton, M. William Heine mann Medical Book LTD. London, 1970, 81-87 Odor, D. L. and Blandau, R. J.: Egg transport over the fimbrial surface of the rabbit oviduct under experimental conditions. Fertil. & Steril. 24: 292-300, 1973 Rumery, R. E. and Eddy, E.: Scanning Electron Microscopy of the Fimbriae and Ampullae of Rabbit Oviducts. Anat. Rec. 178: 83-102, 1973 Lisa, J. R., Gioia, J. D. and Rubib, I. C.: Observations on the interstitial portion of the fallopian tube. Surg. Gynec. & Obst. 99: 159-169, 1954 Hafez, E. S. E. and Black, D. L.: The mammalian Uterotubal Junction. In: The Mammalian Oviduct. Edited by Hafez, E. S. E. and Blandau, R. J. The Univer sity of Chicago Press, Chicago and London, 1969, 85-126 Nilsson, 0.: Electron Microscopy of the Glandular Epithelium in the Human Uterus. I. Follicular Phase. J. Ultra. Res. 6: 413-421, 1962. ‡U. Early and Late Luteal Phase. J. Ultra. Res. 6: 422-432, 1962 Wynn, R. M. and Harris, L. A.: Ultrastructural Cyclic Changes in the Human Endometrium. I Normal Preovulatory Phase. Fertil. & Steril. 18: 632-648, 1967 Wynn, R. M. Woolley, R. S.: Ultrastructural Cyclic Changes in the Human Endo metrium. ‡U Normal Postovulatory Phase. Fertil. & Steril. 18: 721-738, 1967 Hayashi, K., Hamanishi, S. and Ri, H.: Ultrastructural changes of the endo metrial surface at the implantation stage and it's hormonal control. Folia Endo. Tan 50: 813-827. 1974 (in Japanese) Ferenczy, Scanning & Steril.
A., Richart, R. M., Agate, electron microscopy of the 23: 515-521, 1972
F. J., Purkerson, human endometrial
M. L. and Dempsy, surface epithelium.
E. W.: Fertil.
SEM
Fig.
Fig.
1
2
The
Observations
crowded
ciliated
on Human
cells
Oviduct
and
Endometrium
are seen on the fimbrial
The strands or group arrangement on the fimbrial surface. (•~1000)
of the
ciliated
surface. (•~
and
167
1000)
non-ciliated
cells
168
Fig.
Takeo
3
Fig. 4
High magnification be seen. (•~ 10000)
of the
ciliated
Ito
cell.
No deformation
or no coagulation
Fimbrial surface in the secretory phase. The cell boundaries in the proliferative phase. (•~3000)
can
are not clear as
SEM
Fig.
Fig.
5
6
Lining
Luminal microapocrine
Observations
cells
cells
on
the
on
the
secretion
on
Human
ampullary
portion
ampullary can
Oviduct
portion be
seen. (•~3000)
in
and
the
in
Endometrium
proliferative
the
proliferative
169
phase. (•~1000)
phase.
Several
170
Takeo
Fig.
7
Lining surface
cells on the isthmic of the non-ciliated
Fig.
8
Isthmic portion 3000)
in the
Ito
portion in the proliferative cells. (•~3000)
secretory
phase.
Several
secretory
phase.
Note
activity
the bulging
can
be seen. (•~
SEM
Fig.
Fig.
9
10
High
Observations
magnification
on
Human
of the isthmic
Tubal ostia, the view ciliated cells. (•~300)
from
the
Oviduct
portion
uterine
and
Endometrium
in the secretory
lumen.
Note
the
171
phase. (•~10000)
sparseness
of the
172
Takeo
Fig.
Fig.
11
12
Ito
He(•~agonal cells in the utero tubal and small and the few microapocrine
Gross appearance Note the sharrow
of the corporal funnel-shaped
junction. The microvilli are short secretion can be seen. (•~3000)
endometrium in the proliferative gland openings. (•~200)
phase.
SEM
Fig.
13
Gross the
Observations
appearance
of
narrowing
Fig.
of
14
the
on Human
the
uterine
gland
and
endometrium Note
cells. (•~3000)
and
endometrium
openings
Fundal phase.
Oviduct
the
in the
in flat
Endometrium
the
surfaced
the
secretory
undulating
proliferative non-ciliated
173
phase.
surface. (•~300)
Note
174
Fig.
Takeo
15
Fig.
Ito
Luminal epithelium of the corporal endometrium in the secretory the granular microvilli bearing the apical surface. (•~3000)
16
phase.
Note
Luminal epithelium of the corporal endometrium in the secretory phase. Note the bulbously protruded cells and flat surfaced cell with long and vigorous microvilli. (•~3000)
