Difference between revisions of "Paper - Placental circulation"

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=Placental Circulation=
 
=Placental Circulation=
 
MCV QUARTERLY 8(1): 61-68, 1972
 
 
  
 
Elizabeth M. Ramsey, M.D.
 
Elizabeth M. Ramsey, M.D.
Line 24: Line 21:
 
* Presented at the 43rd Annual McGuire Lecture Series, December 3, 1971, at the Medical College of Virginia, Richmond.
 
* Presented at the 43rd Annual McGuire Lecture Series, December 3, 1971, at the Medical College of Virginia, Richmond.
  
 +
==Introduction==
  
One of the most important developments of
+
One of the most important developments of recent years in the field of uterine physiology has been the recognition that the endometrial changes occurring during the menstrual cycle and those associated with pregnancy are interlocking, sequential events in an ordered progression from the first day of the cycle to parturition—and not separate phenomena as was formerly believed. No component of the endometrium illustrates this progression more strikingly than does the vasculature.
recent years in the field of uterine physiology has
 
been the recognition that the endometrial changes
 
occurring during the menstrual cycle and those
 
associated with pregnancy are interlocking, sequential events in an ordered progression from the first
 
day of the cycle to parturition—and not separate
 
phenomena as was formerly believed. No component of the endometrium illustrates this progression more strikingly than does the vasculature.
 
 
 
 
 
Much of the story of uterine vascular pattern
 
and circulatory mechanism is based upon studies
 
in the rhesus monkey, employing in vivo techniques
 
inapplicable to clinical patients. (These studies
 
were carried out in the Department of Embryology,
 
Carnegie Institution of Washington at Baltimore.)
 
Subsequent checking of the monkey findings against
 
their human counterparts, in operative and necropsy
 
specimens, etc., has shown the monkey to be a
 
valid experimental model with reproductive system anatomy and physiology closely similar to the
 
human (Ramsey and Harris, 1966).
 
 
 
 
 
Following the menstrual slough the vasculature
 
regenerates pari passu with the endometrial stroma
 
and glands (Fig. 1). Initially a long capillary network forms between the stumps of spiral arteries in
 
the basalis and the epithelial surface. Subsequently,
 
muscular and elastic layers forming around the capillaries transform them into true arteries. It may be
 
noted parenthetically that this is a more accurate
 
description than the familiar statement that “spiral
 
arteries grow toward the endometrial surface.” A
 
rich capillary bed remains in the immediately subepithelial layer and connects the arteries with veins
 
which run perpendicularly toward the myometrium.
 
 
 
 
 
Although the follicular phase of the cycle is
 
frequently referred to as the “growth phase,” growth of spiral arteries continues unabated during
 
the corpus luteum phase and even further on, as
 
we will see. Indeed, vascular growth during the
 
lutein phase outstrips stromal growth, so that the
 
increasing length of the arteries must be accomodated within the endometrium by ever increasing
 
coiling (Fig. 1).
 
 
 
 
 
Fig. 1—Camera lucida drawings of the vascular bed at three
 
stages of the menstrual cycle in the rhesus monkey. Left.
 
postmenstrual; Center. postovulatory; Right. late secretory.
 
Myometrium stippled. (Reprinted with permission from
 
Bartelmez. Contrib. Embryol. 361153-182, 1957.)
 
 
 
 
 
The implanting ovum achieves its first contact
 
with the maternal blood supply when the penetrating
 
trophoblast both taps and engulfs capillaries of the
 
subepithelial network (Fig. 2), permitting maternal
 
blood to seep, under very low pressure, into the lacunae of the trophoblastic shell. With progressive
 
penetration by trophoblast, the terminal tips of
 
spiral arteries are opened up and maternal arterial
 
blood flows into the shell. This meanwhile has
 
itself been enlarged and transformed by the development of chorionic villi (Fig. 3). It is around the
 
villi, in the inter-villous space, that the maternal
 
blood now flows and from now on we may speak
 
of a placenta and placental circulation.
 
Reconstructions of representative uteroplacental arteries, both human and monkey, at comparable
 
stages of gestation (Fig. 4), show that there is
 
very little qualitative change in growth pattern during
 
the first weeks after implantation (Harris and Ramsey, 1966; Ramsey, 1949). The coiling of the
 
arteries continues and there is just a slight indication of a new process at the arterial tips where
 
trophoblast is beginning to replace normal wall
 
structure. Soon however a change does become
 
manifest. Arterial elongation (as determined by careful micromeasurements) is continuing, but the
 
thickness of the endometrium is being diminished
 
as the result of trophoblastic erosion combined with
 
pressure of the overlying conceptus. Thus, the
 
previously vertical arterial stems are diverted toward
 
the margins of the implantation site, an increasingly
 
sharp angulation developing. With the continuation
 
of these processes in succeeding weeks, the increased coiling of the artery is no longer suflicient
 
to effect its accomodation in the thinned endometrium, so back and forth and lateral looping is
 
added. A terminal dilatation of the artery develops proximal to its point of entry into the intervillous space.
 
 
 
 
 
 
 
 
 
 
 
Fig. 2—Photomicrograph of an early human implantation. (a) trophoblastic lacunae; (b) maternal capillaries. Carnegie Collection 8004, 7th day of pregnancy, section 11-4-4. (Reprinted with permission from Hertig and Rock. Contrib. Embryol. 31: 65-84, 1945.)
 
 
 
 
 
At about mid-pregnancy when, as Reynolds
 
has shown (Reynolds, 1947), the enlargement
 
of the uterus by growth of its parts gives place to
 
enlargement by stretching, the coils of the arteries are “paid out,” as coils of rope on the deck
 
of a ship are paid out when the space between ship and anchorage is increased. The coils are more
 
fully smoothed away in the monkey than in man,
 
probably because monkey endometrium undergoes
 
the greater stretching.
 
 
 
 
 
 
 
 
 
Fig. 3—Photomicrograph of a portion of a monkey placenta
 
in situ. Chorionic plate above; entrance of an endometrial
 
spiral artery into the intervillous space at the left. Carnegie
 
Collection C-477, 29th day of pregnancy, section 47b.
 
 
 
 
 
  
The terminal dilatations of arteries communicating with the intervillous space appear to be
 
the result of the weakening of the vessel wall
 
brought about by replacement of muscle and
 
elastic tissue by trophoblast. Appearing first as an
 
intraluminal accumulation (Fig. 5a), the trophoblastic cells gradually invade and replace the
 
vessel wall (Fig. 5b). The invasion is earlier in
 
the monkey and baboon than in the human, but it
 
is deeper and more extensive in the latter. Human
 
cytotrophoblast penetrates the endometrial stroma
 
as well as entering the arterial lumen and invasion
 
of the wall proceeds from without as well as from
 
within (Fig. 6). The more drastic elimination of
 
normal vascular wall resistance in man doubtless
 
occasions the larger and more persistent terminal
 
dilatations of human uteroplacental arteries. A
 
further result of greater trophoblastic activity in
 
the human is the erosion of arteries all the way
 
to the midendometrium where branches arise from
 
the main spiral stems. These branches then communicate with the intervillous space which explains why there is a proportionately greater number of arterial entries in humans than in monkeys.
 
Upon occasion the trophoblastic action, in contrary fashion, may cause occlusion of branches
 
or even main arterial stems.
 
  
Venous drainage, at all stages of the reproductive cycle, is a less dynamic aflair than arterial
+
Much of the story of uterine vascular pattern and circulatory mechanism is based upon studies in the rhesus monkey, employing in vivo techniques inapplicable to clinical patients. (These studies were carried out in the Department of Embryology, Carnegie Institution of Washington at Baltimore.) Subsequent checking of the monkey findings against their human counterparts, in operative and necropsy specimens, etc., has shown the monkey to be a valid experimental model with reproductive system anatomy and physiology closely similar to the human (Ramsey and Harris, 1966).
inflow. The basic venous pattern in the endometrium is a grid with dilatations into venous lakes
 
at the junction of vertical and lateral limbs. These
 
relationships continue into pregnancy with certain
 
of the vertical channels increasingly distended as
 
they are required to accommodate the ever increasing volume of placental blood. Other channels
 
are passively obliterated by external compression.
 
  
On the physiological side there is again continuity between prepregnant and pregnant states.
 
From the standpoint of circulation, this is most
 
apparent in the persistence of an intrinsic contractile potential in the spiral arteries. This is
 
manifested during the menstrual cycle by isolated
 
contractions at the myoendometrial junction which
 
produce ischemia leading to foci of endometrial
 
necrosis and slough (Bartelmez, 1957), and in
 
pregnancy by intermittency of flow through individual spiral arteries into the intervillous space
 
(Martin, McGaughey, et al, 1964).
 
  
The opposite number to uteroplacental circulation is of course fetoplacental circulation. Propelled by the vis a tergo of fetal blood pressure,
+
Following the menstrual slough the vasculature regenerates pari passu with the endometrial stroma and glands (Fig. 1). Initially a long capillary network forms between the stumps of spiral arteries in the basalis and the epithelial surface. Subsequently, muscular and elastic layers forming around the capillaries transform them into true arteries. It may be noted parenthetically that this is a more accurate description than the familiar statement that “spiral arteries grow toward the endometrial surface.” A rich capillary bed remains in the immediately subepithelial layer and connects the arteries with veins which run perpendicularly toward the myometrium.
fetal blood courses through the umbilical arteries
 
into the subdivisions which run laterally through
 
the chorionic plate. Finally, the vessels dip into the
 
substance of the placenta and travel through the
 
arborizations of the fetal villous tree. -They proceed in comparable subdivisions to the terminal
 
villi. There the fetal capillary bed, coming into its
 
closest proximity to maternal blood in the intervillous space, forms the ultimate area of matemalfetal exchange. Oxygenated blood returns via vessels running through the same villous stems to the
 
umbilical vein and thence to the fetal body (Martin
 
and Ramsey, 1970).
 
  
The mechanism of ‘circulation within the placenta, first hypothesized upon the basis of anatomical data, has been established by radioangiographic studies (Donner, et al, 1963). Especially
 
with cineradioangiography, it is possible to visualize
 
directly the inflow of arterial blood to the intervillous
 
space (Fig. 7),. its circulation through the space, and
 
finally its drainage back to uterine veins.
 
64 RAMEEY: PLACENTAL CIRCULATION
 
  
MARGIN OF INTERVILLOUS SPACE
+
Although the follicular phase of the cycle is frequently referred to as the “growth phase,” growth of spiral arteries continues unabated during the corpus luteum phase and even further on, as we will see. Indeed, vascular growth during the lutein phase outstrips stromal growth, so that the increasing length of the arteries must be accomodated within the endometrium by ever increasing coiling (Fig. 1).
  
TERMINA-L SAC
 
  
BASE or ENDOMETRIUM ; . "'E““"“"L 5“:
 
  
SPIRAL ARTERV SPNAL ARTERYI
+
Fig. 1. Camera lucida drawings of the vascular bed at three stages of the menstrual cycle in the rhesus monkey. Left. postmenstrual; Center. postovulatory; Right. late secretory. Myometrium stippled. (Reprinted with permission from Bartelmez. Contrib. Embryol. 361153-182, 1957.)
  
1 ET V
 
EIASAL ARTERY 1 (PA \f4LE.|gILED) L
 
  
ARCUATE ARTERY
+
The implanting ovum achieves its first contact with the maternal blood supply when the penetrating trophoblast both taps and engulfs capillaries of the subepithelial network (Fig. 2), permitting maternal blood to seep, under very low pressure, into the lacunae of the trophoblastic shell. With progressive penetration by trophoblast, the terminal tips of spiral arteries are opened up and maternal arterial blood flows into the shell. This meanwhile has itself been enlarged and transformed by the development of chorionic villi (Fig. 3). It is around the villi, in the inter-villous space, that the maternal blood now flows and from now on we may speak of a placenta and placental circulation. Reconstructions of representative uteroplacental arteries, both human and monkey, at comparable stages of gestation (Fig. 4), show that there is very little qualitative change in growth pattern during the first weeks after implantation (Harris and Ramsey, 1966; Ramsey, 1949). The coiling of the arteries continues and there is just a slight indication of a new process at the arterial tips where trophoblast is beginning to replace normal wall structure. Soon however a change does become manifest. Arterial elongation (as determined by careful micromeasurements) is continuing, but the thickness of the endometrium is being diminished as the result of trophoblastic erosion combined with pressure of the overlying conceptus. Thus, the previously vertical arterial stems are diverted toward the margins of the implantation site, an increasingly sharp angulation developing. With the continuation of these processes in succeeding weeks, the increased coiling of the artery is no longer suflicient to effect its accomodation in the thinned endometrium, so back and forth and lateral looping is added. A terminal dilatation of the artery develops proximal to its point of entry into the intervillous space.
  
FERITONEAL SURFACE
 
6th WEEK
 
  
MARGIN or |NTEVR\/ILLOUS SPACE PERITONEAL SURHCE
 
  
|5lh WEEK
+
Fig. 2. Photomicrograph of an early human implantation. (a) trophoblastic lacunae; (b) maternal capillaries. Carnegie Collection 8004, 7th day of pregnancy, section 11-4-4. (Reprinted with permission from Hertig and Rock. Contrib. Embryol. 31: 65-84, 1945.)
  
/E, ?(4——'~ » I 5p[RA|_ ARTERY [u~:on.:o
 
  
BASE or ENDOMETRIUM , E MARGIN or INTERVILLOUS SPACE "‘
+
At about mid-pregnancy when, as Reynolds has shown (Reynolds, 1947), the enlargement of the uterus by growth of its parts gives place to enlargement by stretching, the coils of the arteries are “paid out,” as coils of rope on the deck of a ship are paid out when the space between ship and anchorage is increased. The coils are more fully smoothed away in the monkey than in man, probably because monkey endometrium undergoes the greater stretching.
3 p H _fi___,,__ ,_ , 1 ‘ BASE or ENDOMETRlUM~
 
  
PERITONEAL SURFACE
 
  
Bth WEEK
 
  
A  E Ancufls ARTERY new WEEK
+
Fig. 3. Photomicrograph of a portion of a monkey placenta in situ. Chorionic plate above; entrance of an endometrial spiral artery into the intervillous space at the left. Carnegie Collection C-477, 29th day of pregnancy, section 47b.
  
Human
 
  
I6 WEEKS 20 WEEKS
+
The terminal dilatations of arteries communicating with the intervillous space appear to be the result of the weakening of the vessel wall brought about by replacement of muscle and elastic tissue by trophoblast. Appearing first as an intraluminal accumulation (Fig. 5a), the trophoblastic cells gradually invade and replace the vessel wall (Fig. 5b). The invasion is earlier in the monkey and baboon than in the human, but it is deeper and more extensive in the latter. Human cytotrophoblast penetrates the endometrial stroma as well as entering the arterial lumen and invasion of the wall proceeds from without as well as from within (Fig. 6). The more drastic elimination of normal vascular wall resistance in man doubtless occasions the larger and more persistent terminal dilatations of human uteroplacental arteries. A further result of greater trophoblastic activity in the human is the erosion of arteries all the way to the midendometrium where branches arise from the main spiral stems. These branches then communicate with the intervillous space which explains why there is a proportionately greater number of arterial entries in humans than in monkeys. Upon occasion the trophoblastic action, in contrary fashion, may cause occlusion of branches or even main arterial stems.
  
H79)! YIIAL S0flfACE
 
  
8 WEEKS
+
Venous drainage, at all stages of the reproductive cycle, is a less dynamic aflair than arterial inflow. The basic venous pattern in the endometrium is a grid with dilatations into venous lakes at the junction of vertical and lateral limbs. These relationships continue into pregnancy with certain of the vertical channels increasingly distended as they are required to accommodate the ever increasing volume of placental blood. Other channels are passively obliterated by external compression.
  
32 WEEKS FULL TERM
 
  
nyonnnwt sunncr
+
On the physiological side there is again continuity between prepregnant and pregnant states. From the standpoint of circulation, this is most apparent in the persistence of an intrinsic contractile potential in the spiral arteries. This is manifested during the menstrual cycle by isolated contractions at the myoendometrial junction which produce ischemia leading to foci of endometrial necrosis and slough (Bartelmez, 1957), and in pregnancy by intermittency of flow through individual spiral arteries into the intervillous space (Martin, McGaughey, et al, 1964).
  
HYD;1£TEIAL sunucr
 
  
E
+
The opposite number to uteroplacental circulation is of course fetoplacental circulation. Propelled by the vis a tergo of fetal blood pressure, fetal blood courses through the umbilical arteries into the subdivisions which run laterally through the chorionic plate. Finally, the vessels dip into the substance of the placenta and travel through the arborizations of the fetal villous tree. -They proceed in comparable subdivisions to the terminal villi. There the fetal capillary bed, coming into its closest proximity to maternal blood in the intervillous space, forms the ultimate area of matemalfetal exchange. Oxygenated blood returns via vessels running through the same villous stems to the umbilical vein and thence to the fetal body (Martin and Ramsey, 1970).
  
Fig. 4—Diagrammatic representations of the course andlconfiguration of the uteroplacental arteries in the rhesus monkey and man,
 
at comparable stages of gestation. (Reprinted with permission from Harris and Ramsey. Contrib. Embryo]. 38: 43-58, 1566.)
 
  
The propulsive force throughout is the head propulsive force is reduced, in part by the, baflle
+
The mechanism of ‘circulation within the placenta, first hypothesized upon the basis of anatomical data, has been established by radioangiographic studies (Donner, et al, 1963). Especially with cineradioangiography, it is possible to visualize directly the inflow of arterial blood to the intervillous space (Fig. 7),. its circulation through the space, and finally its drainage back to uterine veins.  
of maternal blood pressure which drives blood action of the villi, the blood disperses laterally crowdinto the intervillous space in discreet, fountainlike ing the existing content of blood through the ve“spurts.” The incoming blood wafts aside the villi nous orifices in the basal plate into the uterine
 
surrounding the orifices of entry, but once the drainage channels (Fig. 8). During uterine conRAMSEY: PLACENTAL CIRCULATION
 
  
   
 
  
Fig. 5a—Photomicrograph of uteroplacental arteries in the
 
monkey illustrating early accumulation of trophoblast within
 
the lumen of the artery. Carnegie Collection C-477, 29th
 
day of pregnancy. (Reprinted with permission from Wislocki
 
and Streeter.‘ Contrib. Embryol. 27:1—66, 1933;.) >
 
  
+
Fig. 4. Diagrammatic representations of the course andlconfiguration of the uteroplacental arteries in the rhesus monkey and man, at comparable stages of gestation. (Reprinted with permission from Harris and Ramsey. Contrib. Embryo]. 38: 43-58, 1566.)
  
Fig. 5b—Photomicrograph of uteroplacental arteries in
+
The propulsive force throughout is the head propulsive force is reduced, in part by the, baflle of maternal blood pressure which drives blood action of the villi, the blood disperses laterally crowdinto the intervillous space in discreet, fountainlike ing the existing content of blood through the ve“spurts.” The incoming blood wafts aside the villi nous orifices in the basal plate into the uterine surrounding the orifices of entry, but once the drainage channels (Fig. 8). During uterine contractions both inflow and outflow cease, in whole or in part, depending upon the strength of the contraction (Ramsey, Martin, McGaughey, et al, 1966). The volume of the placental pool, however, is maintained. That is to say, the old concept that “contractions squeeze the placenta like a sponge” is incorrect; rather blood is trapped in the placenta during contractions.
monkey illustrating subsequent replacement of the" arterial
 
wall without trophoblastic penetration of stroma. Carnegie
 
Collection C-629, 53rd day of pregnancy. (Reprinted with
 
permission from Ramsey. Contrib. Embryol. 33:l13—147,
 
1949.) '
 
  
tractions both inflow and outflow cease, in whole
 
or in part, depending upon the strength of the contraction (Ramsey, Martin, McGaughey, et al, 1966).
 
The volume of the placental pool, however, is maintained. That is to say, the old concept that “contractions squeeze the placenta like a sponge” is incorrect; rather blood is trapped in the placenta during
 
contractions.
 
  
Radioangiography of the fetal side of placental
+
Fig. 5a. Photomicrograph of uteroplacental arteries in the monkey illustrating early accumulation of trophoblast within the lumen of the artery. Carnegie Collection C-477, 29th day of pregnancy. (Reprinted with permission from Wislocki and Streeter.‘ Contrib. Embryol. 27:1—66, 1933;.)
circulation (Martin, Ramsey, and Donner, 1966)
 
  
65
 
  
fie
+
Fig. 5b. Photomicrograph of uteroplacental arteries in monkey illustrating subsequent replacement of the" arterial wall without trophoblastic penetration of stroma. Carnegie Collection C-629, 53rd day of pregnancy. (Reprinted with permission from Ramsey. Contrib. Embryol. 33:l13—147, 1949.)
  
Fig. 6——Photomicrograph of a human uteroplacental artery
 
showing replacement of wall and penetration of stroma by
 
trophoblast. Carnegie Collection 10117, 85th day of pregnancy. (Reprinted with permission from Ramsey. Prenatal
 
Life. Wayne State University Press, 1970, pp. 37-53.)
 
  
shows the progress of blood from the fetal body into
 
the capillary network of the fetal cotyledons and
 
back via the umbilical vein. Double injection of a
 
radiopaque medium (Ramsey, Martin, and Donner, 1967 ), that is, into fetal and maternal circulations in rapid succession, permits visualization of the
 
1:1 relationship" between maternal spiral arteries
 
and fetal cotyledons (Fig. 9).
 
  
Two points of clinical interest emerge from the
+
Radioangiography of the fetal side of placental circulation (Martin, Ramsey, and Donner, 1966) shows the progress of blood from the fetal body into the capillary network of the fetal cotyledons and back via the umbilical vein. Double injection of a radiopaque medium (Ramsey, Martin, and Donner, 1967 ), that is, into fetal and maternal circulations in rapid succession, permits visualization of the 1:1 relationship" between maternal spiral arteries and fetal cotyledons (Fig. 9).
foregoing. The first is that placental circulation
 
ceases during strong contractions. That this may
 
present the fetus with periods of anoxia is clear and
 
should contractions be unduly prolonged, as the
 
result of pathology or medication, it could indeed
 
be critical. Second, and somewhat mitigating the
 
implied threat of the cessation of flow, is the fact
 
  
that the pool of placental blood is preserved
 
  
throughout. Thus, under normal conditions, continued maternal-fetal exchange is made possible.
 
  
And that exchange, of course, is the whole
+
Fig. 6. Photomicrograph of a human uteroplacental artery showing replacement of wall and penetration of stroma by trophoblast. Carnegie Collection 10117, 85th day of pregnancy. (Reprinted with permission from Ramsey. Prenatal Life. Wayne State University Press, 1970, pp. 37-53.)
purpose of the long and elaborate procession of
 
vascular changes from Day 1 of the menstrual cycle
 
to parturition.
 
66 RAMSEY: PLACENTAL CIRCULATION
 
  
Fig. 7—Photographs of X rays made at 2, 3, and 7% seconds respectively after injection of contrast material into a femoral artery
 
of a monkey. (R.a.) renal artery; (S.a.) endometrial spiral artery;—>“spurts” into intervillous space. Carnegie Collection Monkey
 
60/14, 100th day of pregnancy. (Reprinted with permission from Ramsey, er al. Montanino Editore, Napoli. ll: 1779-1784, 1962.)
 
  
Fig. 8—Composite drawing of the primate placenta to show its structure and circulation. (Drawing by Ranice Davis Crosby for
+
Two points of clinical interest emerge from the foregoing. The first is that placental circulation ceases during strong contractions. That this may present the fetus with periods of anoxia is clear and should contractions be unduly prolonged, as the result of pathology or medication, it could indeed be critical. Second, and somewhat mitigating the implied threat of the cessation of flow, is the fact that the pool of placental blood is preserved throughout. Thus, under normal conditions, continued maternal-fetal exchange is made possible.
E. M. Ramsey. Courtesy of the Carnegie Institution of Washington.) ‘
 
RAMSEY: PLACENTAL CIRCULATION
 
  
67
 
  
Fig. 9—Spot films made during a combined fetal and maternal injection study. (A) taken 3 seconds after injection of contrast
+
And that exchange, of course, is the whole purpose of the long and elaborate procession of vascular changes from Day 1 of the menstrual cycle to parturition.  
material into the fetal circulation; (B) taken 2 seconds after immediately subsequent maternal injection. (FC) fetal cotyledon;
 
(SA) endometrial spiral artery;—>“spurts” into the intervillous space. Carnegie Collection Monkey 65/80, 152nd day of pregnancy.
 
(Reprinted with permission from Ramsey, et al. Am. J. Obstet. Gyrtec. 98: 419-423, 1967.)
 
  
REFERENCES
 
  
BARTELMEZ, G. W. The form and the functions of the uterine
+
Fig. 7. Photographs of X rays made at 2, 3, and 7% seconds respectively after injection of contrast material into a femoral artery of a monkey. (R.a.) renal artery; (S.a.) endometrial spiral artery;—>“spurts” into intervillous space. Carnegie Collection Monkey 60/14, 100th day of pregnancy. (Reprinted with permission from Ramsey, er al. Montanino Editore, Napoli. ll: 1779-1784, 1962.)
  
blood vessels in the rhesus monkey. Carnegie Inst. Wash.,
+
Fig. 8. Composite drawing of the primate placenta to show its structure and circulation. (Drawing by Ranice Davis Crosby for E. M. Ramsey. Courtesy of the Carnegie Institution of Washington.)
Contrib. Embryol. 36:153—182, 1957.
 
  
DONNER, M. W., RAMSEY, E. M., AND CORNER, G. W., JR.
 
Maternal circulation in the placenta of the rhesus monkey;
 
A radioangiographic study. Amer. J. Radiol. and Roentgen.
 
Therapy. 901638-649, 1963.
 
  
HARRIS, J. W. S. AND RAMSEY, E. M. The morphology of
 
human uteroplacental vasculature. Carnegie Inst. Wash.,
 
Corztrib. Embryol. 38:43-58, 1966.
 
  
HERTIG, A. T. AND ROCK, J. Two human ova of the previllous stage, having a developmental age of about seven
+
Fig. 9. Spot films made during a combined fetal and maternal injection study. (A) taken 3 seconds after injection of contrast material into the fetal circulation; (B) taken 2 seconds after immediately subsequent maternal injection. (FC) fetal cotyledon; (SA) endometrial spiral artery;—>“spurts” into the intervillous space. Carnegie Collection Monkey 65/80, 152nd day of pregnancy. (Reprinted with permission from Ramsey, et al. Am. J. Obstet. Gyrtec. 98: 419-423, 1967.)
and nine days respectively. Carnegie Inst. Wash., Contrib.
 
Embryol. 31:65-84, 1945.
 
  
MARTIN, C. B., JR., MCGAUGHEY, H. S., JR., KAISER, I. H.,
+
==References==
DONNER, M. W., AND RAMSEY, E. M. Intermittent functioning of the uteroplacental arteries. Am. J. Obstet, Gynec.
 
  
90:8l9—823, 1964.
+
BARTELMEZ, G. W. The form and the functions of the uterine blood vessels in the rhesus monkey. Carnegie Inst. Wash., Contrib. Embryol. 36:153—182, 1957.
  
MARTIN, C. B., JR. AND RAMSEY, E. M. Gross anatomy of
+
DONNER, M. W., RAMSEY, E. M., AND CORNER, G. W., JR. Maternal circulation in the placenta of the rhesus monkey; A radioangiographic study. Amer. J. Radiol. and Roentgen. Therapy. 901638-649, 1963.
the placenta of rhesus monkeys. Obstet. Gynecol 36:167
 
177, 1970.
 
  
MARTIN, C. B., JR., RAMSEY, E. M., AND DONNER, M. W.
+
HARRIS, J. W. S. AND RAMSEY, E. M. The morphology of human uteroplacental vasculature. Carnegie Inst. Wash., Corztrib. Embryol. 38:43-58, 1966.
The fetal placental circulation in rhesus monkeys demonstrated by radioangiography. Am. J. Obstet. Gynec. 95:943947, 1966.
 
  
RAMSEY, E. M. The vascular pattern of the endometrium of
+
HERTIG, A. T. AND ROCK, J. Two human ova of the previllous stage, having a developmental age of about seven and nine days respectively. Carnegie Inst. Wash., Contrib. Embryol. 31:65-84, 1945.
the pregnant rhesus monkey (Macaca mulatta). Carnegie
 
Inst. Wash., Contrib. Embryol. 33:113—147, 1949‘.
 
  
RAMSEY, E. M. Placental circulation in rhesus and man.
+
MARTIN, C. B., JR., MCGAUGHEY, H. S., JR., KAISER, I. H., DONNER, M. W., AND RAMSEY, E. M. Intermittent functioning of the uteroplacental arteries. Am. J. Obstet, Gynec. 90:8l9—823, 1964.
Prenatal Life. Proceedings of the Third Annual Symposium
 
on the Physiology and Pathology of Human Reproduction.
 
Harold C. Mack (ed.). Detroit: Wayne State University
 
  
Press. 1970, pp. 37-53.
+
MARTIN, C. B., JR. AND RAMSEY, E. M. Gross anatomy of the placenta of rhesus monkeys. Obstet. Gynecol 36:167 177, 1970.
  
RAMSEY, E. M., CORNER, G. W., JR., DONNER, M. W., AND
+
MARTIN, C. B., JR., RAMSEY, E. M., AND DONNER, M. W. The fetal placental circulation in rhesus monkeys demonstrated by radioangiography. Am. J. Obstet. Gynec. 95:943947, 1966.
STRAN, H. M. Visualization of maternal circulation in the
 
monkey placenta by radioangiography. Scritti in onore del
 
Prof. Giuseppe Tesauro nel XXV anno del Suo insegnamento. Montanino Editore, Napoli. II:1779—1784, 1962.
 
68
 
  
RAMSEY, E. M. AND HARRIS, J. W. S. Comparison of uteroplacental vasculature and circulation in the rhesus monkey
+
RAMSEY, E. M. The vascular pattern of the endometrium of the pregnant rhesus monkey (Macaca mulatta). Carnegie Inst. Wash., Contrib. Embryol. 33:113—147, 1949.
and man. Carnegie Inst. Wash., Contrib. Embryol. 38:59
 
70, 1966.
 
  
RAMSEY, E. M., MARTIN, C. B., JR., AND DoNNER, M. W.
+
RAMSEY, E. M. Placental circulation in rhesus and man. Prenatal Life. Proceedings of the Third Annual Symposium on the Physiology and Pathology of Human Reproduction. Harold C. Mack (ed.). Detroit: Wayne State University Press. 1970, pp. 37-53.
Fetal and maternal placental circulations. Am. J. Obstet.
 
Gynec. 981419-423, 1967.
 
  
RAMSEY, E. M., MARTIN, C. B., JR., MCGAUGHEY, H. S., JR.,
+
RAMSEY, E. M., CORNER, G. W., JR., DONNER, M. W., AND STRAN, H. M. Visualization of maternal circulation in the monkey placenta by radioangiography. Scritti in onore del Prof. Giuseppe Tesauro nel XXV anno del Suo insegnamento. Montanino Editore, Napoli. II:1779—1784, 1962. 68
KAISER, I. H., AND DONNER, M. W. Venous drainage of the
 
  
RAMSEY: PLACENTAL CIRCULATION
+
RAMSEY, E. M. AND HARRIS, J. W. S. Comparison of uteroplacental vasculature and circulation in the rhesus monkey and man. Carnegie Inst. Wash., Contrib. Embryol. 38:59 70, 1966.
  
placenta in rhesus monkeys: radiographic studies. Am. J.
+
RAMSEY, E. M., MARTIN, C. B., JR., AND DoNNER, M. W. Fetal and maternal placental circulations. Am. J. Obstet. Gynec. 981419-423, 1967.
Obstet. Gynec. 95:948—955, 1966.
 
  
REYNOLDS, S. R. M. Uterine accommodation of the products
+
RAMSEY, E. M., MARTIN, C. B., JR., MCGAUGHEY, H. S., JR., KAISER, I. H., AND DONNER, M. W. Venous drainage of the placenta in rhesus monkeys: radiographic studies. Am. J. Obstet. Gynec. 95:948—955, 1966.
of conception: physiologic considerations. Am. J. Obstet.
 
Gynec. 532901-913, 1947.
 
  
WISLOCKI, G. B. AND STREETER, G. L. On the placentation
+
REYNOLDS, S. R. M. Uterine accommodation of the products of conception: physiologic considerations. Am. J. Obstet. Gynec. 532901-913, 1947.
of the macaque (Macaca mulatta), from the time of implantation until the formation of the definitive placenta.
 
Carnegie Inst. Wash., Contrib. Embryol. 2721-66, 1938.
 
  
 +
WISLOCKI, G. B. AND STREETER, G. L. On the placentation of the macaque (Macaca mulatta), from the time of implantation until the formation of the definitive placenta. Carnegie Inst. Wash., Contrib. Embryol. 2721-66, 1938.
  
Rights © VCU. Licensed under a Creative Commons Attribution-Noncommercial-Share Alike 3.0 Unported License. http://creativecommons.org/licenses/by-nc-sa/3.0 Acknowledgement of the Virginia Commonwealth University Libraries as a source is required.
 
  
 
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Ramsey EM. Placental Circulation. (1972) MCV Quarterly, 8(1): 61-68.

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This historic 1972 paper by Ramsey describes development of the placental circulation. The paper uses human and monkey embryos from the Carnegie Collection.


See the links below for the current placenta notes pages.

Placenta Links: placenta | Lecture - Placenta | Lecture Movie | Practical - Placenta | implantation | placental villi | trophoblast | maternal decidua | uterus | endocrine placenta | placental cord | placental membranes | placenta abnormalities | ectopic pregnancy | Stage 13 | Stage 22 | placenta histology | placenta vascular | blood vessel | cord stem cells | 2013 Meeting Presentation | Placenta Terms | Category:Placenta
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Pages where the terms "Historic Textbook" and "Historic Embryology" appear on this site, and sections within pages where this disclaimer appears, indicate that the content and scientific understanding are specific to the time of publication. This means that while some scientific descriptions are still accurate, the terminology and interpretation of the developmental mechanisms reflect the understanding at the time of original publication and those of the preceding periods, these terms and interpretations may not reflect our current scientific understanding.     (More? Embryology History | Historic Embryology Papers)

Placental Circulation

Elizabeth M. Ramsey, M.D.

Visiting Professor of Obstetrics and Gynecology, University of Virginia

School of Medicine, Charlottesville, Virginia

  • Presented at the 43rd Annual McGuire Lecture Series, December 3, 1971, at the Medical College of Virginia, Richmond.

Introduction

One of the most important developments of recent years in the field of uterine physiology has been the recognition that the endometrial changes occurring during the menstrual cycle and those associated with pregnancy are interlocking, sequential events in an ordered progression from the first day of the cycle to parturition—and not separate phenomena as was formerly believed. No component of the endometrium illustrates this progression more strikingly than does the vasculature.


Much of the story of uterine vascular pattern and circulatory mechanism is based upon studies in the rhesus monkey, employing in vivo techniques inapplicable to clinical patients. (These studies were carried out in the Department of Embryology, Carnegie Institution of Washington at Baltimore.) Subsequent checking of the monkey findings against their human counterparts, in operative and necropsy specimens, etc., has shown the monkey to be a valid experimental model with reproductive system anatomy and physiology closely similar to the human (Ramsey and Harris, 1966).


Following the menstrual slough the vasculature regenerates pari passu with the endometrial stroma and glands (Fig. 1). Initially a long capillary network forms between the stumps of spiral arteries in the basalis and the epithelial surface. Subsequently, muscular and elastic layers forming around the capillaries transform them into true arteries. It may be noted parenthetically that this is a more accurate description than the familiar statement that “spiral arteries grow toward the endometrial surface.” A rich capillary bed remains in the immediately subepithelial layer and connects the arteries with veins which run perpendicularly toward the myometrium.


Although the follicular phase of the cycle is frequently referred to as the “growth phase,” growth of spiral arteries continues unabated during the corpus luteum phase and even further on, as we will see. Indeed, vascular growth during the lutein phase outstrips stromal growth, so that the increasing length of the arteries must be accomodated within the endometrium by ever increasing coiling (Fig. 1).


Fig. 1. Camera lucida drawings of the vascular bed at three stages of the menstrual cycle in the rhesus monkey. Left. postmenstrual; Center. postovulatory; Right. late secretory. Myometrium stippled. (Reprinted with permission from Bartelmez. Contrib. Embryol. 361153-182, 1957.)


The implanting ovum achieves its first contact with the maternal blood supply when the penetrating trophoblast both taps and engulfs capillaries of the subepithelial network (Fig. 2), permitting maternal blood to seep, under very low pressure, into the lacunae of the trophoblastic shell. With progressive penetration by trophoblast, the terminal tips of spiral arteries are opened up and maternal arterial blood flows into the shell. This meanwhile has itself been enlarged and transformed by the development of chorionic villi (Fig. 3). It is around the villi, in the inter-villous space, that the maternal blood now flows and from now on we may speak of a placenta and placental circulation. Reconstructions of representative uteroplacental arteries, both human and monkey, at comparable stages of gestation (Fig. 4), show that there is very little qualitative change in growth pattern during the first weeks after implantation (Harris and Ramsey, 1966; Ramsey, 1949). The coiling of the arteries continues and there is just a slight indication of a new process at the arterial tips where trophoblast is beginning to replace normal wall structure. Soon however a change does become manifest. Arterial elongation (as determined by careful micromeasurements) is continuing, but the thickness of the endometrium is being diminished as the result of trophoblastic erosion combined with pressure of the overlying conceptus. Thus, the previously vertical arterial stems are diverted toward the margins of the implantation site, an increasingly sharp angulation developing. With the continuation of these processes in succeeding weeks, the increased coiling of the artery is no longer suflicient to effect its accomodation in the thinned endometrium, so back and forth and lateral looping is added. A terminal dilatation of the artery develops proximal to its point of entry into the intervillous space.


Fig. 2. Photomicrograph of an early human implantation. (a) trophoblastic lacunae; (b) maternal capillaries. Carnegie Collection 8004, 7th day of pregnancy, section 11-4-4. (Reprinted with permission from Hertig and Rock. Contrib. Embryol. 31: 65-84, 1945.)


At about mid-pregnancy when, as Reynolds has shown (Reynolds, 1947), the enlargement of the uterus by growth of its parts gives place to enlargement by stretching, the coils of the arteries are “paid out,” as coils of rope on the deck of a ship are paid out when the space between ship and anchorage is increased. The coils are more fully smoothed away in the monkey than in man, probably because monkey endometrium undergoes the greater stretching.


Fig. 3. Photomicrograph of a portion of a monkey placenta in situ. Chorionic plate above; entrance of an endometrial spiral artery into the intervillous space at the left. Carnegie Collection C-477, 29th day of pregnancy, section 47b.


The terminal dilatations of arteries communicating with the intervillous space appear to be the result of the weakening of the vessel wall brought about by replacement of muscle and elastic tissue by trophoblast. Appearing first as an intraluminal accumulation (Fig. 5a), the trophoblastic cells gradually invade and replace the vessel wall (Fig. 5b). The invasion is earlier in the monkey and baboon than in the human, but it is deeper and more extensive in the latter. Human cytotrophoblast penetrates the endometrial stroma as well as entering the arterial lumen and invasion of the wall proceeds from without as well as from within (Fig. 6). The more drastic elimination of normal vascular wall resistance in man doubtless occasions the larger and more persistent terminal dilatations of human uteroplacental arteries. A further result of greater trophoblastic activity in the human is the erosion of arteries all the way to the midendometrium where branches arise from the main spiral stems. These branches then communicate with the intervillous space which explains why there is a proportionately greater number of arterial entries in humans than in monkeys. Upon occasion the trophoblastic action, in contrary fashion, may cause occlusion of branches or even main arterial stems.


Venous drainage, at all stages of the reproductive cycle, is a less dynamic aflair than arterial inflow. The basic venous pattern in the endometrium is a grid with dilatations into venous lakes at the junction of vertical and lateral limbs. These relationships continue into pregnancy with certain of the vertical channels increasingly distended as they are required to accommodate the ever increasing volume of placental blood. Other channels are passively obliterated by external compression.


On the physiological side there is again continuity between prepregnant and pregnant states. From the standpoint of circulation, this is most apparent in the persistence of an intrinsic contractile potential in the spiral arteries. This is manifested during the menstrual cycle by isolated contractions at the myoendometrial junction which produce ischemia leading to foci of endometrial necrosis and slough (Bartelmez, 1957), and in pregnancy by intermittency of flow through individual spiral arteries into the intervillous space (Martin, McGaughey, et al, 1964).


The opposite number to uteroplacental circulation is of course fetoplacental circulation. Propelled by the vis a tergo of fetal blood pressure, fetal blood courses through the umbilical arteries into the subdivisions which run laterally through the chorionic plate. Finally, the vessels dip into the substance of the placenta and travel through the arborizations of the fetal villous tree. -They proceed in comparable subdivisions to the terminal villi. There the fetal capillary bed, coming into its closest proximity to maternal blood in the intervillous space, forms the ultimate area of matemalfetal exchange. Oxygenated blood returns via vessels running through the same villous stems to the umbilical vein and thence to the fetal body (Martin and Ramsey, 1970).


The mechanism of ‘circulation within the placenta, first hypothesized upon the basis of anatomical data, has been established by radioangiographic studies (Donner, et al, 1963). Especially with cineradioangiography, it is possible to visualize directly the inflow of arterial blood to the intervillous space (Fig. 7),. its circulation through the space, and finally its drainage back to uterine veins.


Fig. 4. Diagrammatic representations of the course andlconfiguration of the uteroplacental arteries in the rhesus monkey and man, at comparable stages of gestation. (Reprinted with permission from Harris and Ramsey. Contrib. Embryo]. 38: 43-58, 1566.)

The propulsive force throughout is the head propulsive force is reduced, in part by the, baflle of maternal blood pressure which drives blood action of the villi, the blood disperses laterally crowdinto the intervillous space in discreet, fountainlike ing the existing content of blood through the ve“spurts.” The incoming blood wafts aside the villi nous orifices in the basal plate into the uterine surrounding the orifices of entry, but once the drainage channels (Fig. 8). During uterine contractions both inflow and outflow cease, in whole or in part, depending upon the strength of the contraction (Ramsey, Martin, McGaughey, et al, 1966). The volume of the placental pool, however, is maintained. That is to say, the old concept that “contractions squeeze the placenta like a sponge” is incorrect; rather blood is trapped in the placenta during contractions.


Fig. 5a. Photomicrograph of uteroplacental arteries in the monkey illustrating early accumulation of trophoblast within the lumen of the artery. Carnegie Collection C-477, 29th day of pregnancy. (Reprinted with permission from Wislocki and Streeter.‘ Contrib. Embryol. 27:1—66, 1933;.)


Fig. 5b. Photomicrograph of uteroplacental arteries in monkey illustrating subsequent replacement of the" arterial wall without trophoblastic penetration of stroma. Carnegie Collection C-629, 53rd day of pregnancy. (Reprinted with permission from Ramsey. Contrib. Embryol. 33:l13—147, 1949.)


Radioangiography of the fetal side of placental circulation (Martin, Ramsey, and Donner, 1966) shows the progress of blood from the fetal body into the capillary network of the fetal cotyledons and back via the umbilical vein. Double injection of a radiopaque medium (Ramsey, Martin, and Donner, 1967 ), that is, into fetal and maternal circulations in rapid succession, permits visualization of the 1:1 relationship" between maternal spiral arteries and fetal cotyledons (Fig. 9).


Fig. 6. Photomicrograph of a human uteroplacental artery showing replacement of wall and penetration of stroma by trophoblast. Carnegie Collection 10117, 85th day of pregnancy. (Reprinted with permission from Ramsey. Prenatal Life. Wayne State University Press, 1970, pp. 37-53.)


Two points of clinical interest emerge from the foregoing. The first is that placental circulation ceases during strong contractions. That this may present the fetus with periods of anoxia is clear and should contractions be unduly prolonged, as the result of pathology or medication, it could indeed be critical. Second, and somewhat mitigating the implied threat of the cessation of flow, is the fact that the pool of placental blood is preserved throughout. Thus, under normal conditions, continued maternal-fetal exchange is made possible.


And that exchange, of course, is the whole purpose of the long and elaborate procession of vascular changes from Day 1 of the menstrual cycle to parturition.


Fig. 7. Photographs of X rays made at 2, 3, and 7% seconds respectively after injection of contrast material into a femoral artery of a monkey. (R.a.) renal artery; (S.a.) endometrial spiral artery;—>“spurts” into intervillous space. Carnegie Collection Monkey 60/14, 100th day of pregnancy. (Reprinted with permission from Ramsey, er al. Montanino Editore, Napoli. ll: 1779-1784, 1962.)

Fig. 8. Composite drawing of the primate placenta to show its structure and circulation. (Drawing by Ranice Davis Crosby for E. M. Ramsey. Courtesy of the Carnegie Institution of Washington.)


Fig. 9. Spot films made during a combined fetal and maternal injection study. (A) taken 3 seconds after injection of contrast material into the fetal circulation; (B) taken 2 seconds after immediately subsequent maternal injection. (FC) fetal cotyledon; (SA) endometrial spiral artery;—>“spurts” into the intervillous space. Carnegie Collection Monkey 65/80, 152nd day of pregnancy. (Reprinted with permission from Ramsey, et al. Am. J. Obstet. Gyrtec. 98: 419-423, 1967.)

References

BARTELMEZ, G. W. The form and the functions of the uterine blood vessels in the rhesus monkey. Carnegie Inst. Wash., Contrib. Embryol. 36:153—182, 1957.

DONNER, M. W., RAMSEY, E. M., AND CORNER, G. W., JR. Maternal circulation in the placenta of the rhesus monkey; A radioangiographic study. Amer. J. Radiol. and Roentgen. Therapy. 901638-649, 1963.

HARRIS, J. W. S. AND RAMSEY, E. M. The morphology of human uteroplacental vasculature. Carnegie Inst. Wash., Corztrib. Embryol. 38:43-58, 1966.

HERTIG, A. T. AND ROCK, J. Two human ova of the previllous stage, having a developmental age of about seven and nine days respectively. Carnegie Inst. Wash., Contrib. Embryol. 31:65-84, 1945.

MARTIN, C. B., JR., MCGAUGHEY, H. S., JR., KAISER, I. H., DONNER, M. W., AND RAMSEY, E. M. Intermittent functioning of the uteroplacental arteries. Am. J. Obstet, Gynec. 90:8l9—823, 1964.

MARTIN, C. B., JR. AND RAMSEY, E. M. Gross anatomy of the placenta of rhesus monkeys. Obstet. Gynecol 36:167 177, 1970.

MARTIN, C. B., JR., RAMSEY, E. M., AND DONNER, M. W. The fetal placental circulation in rhesus monkeys demonstrated by radioangiography. Am. J. Obstet. Gynec. 95:943947, 1966.

RAMSEY, E. M. The vascular pattern of the endometrium of the pregnant rhesus monkey (Macaca mulatta). Carnegie Inst. Wash., Contrib. Embryol. 33:113—147, 1949.

RAMSEY, E. M. Placental circulation in rhesus and man. Prenatal Life. Proceedings of the Third Annual Symposium on the Physiology and Pathology of Human Reproduction. Harold C. Mack (ed.). Detroit: Wayne State University Press. 1970, pp. 37-53.

RAMSEY, E. M., CORNER, G. W., JR., DONNER, M. W., AND STRAN, H. M. Visualization of maternal circulation in the monkey placenta by radioangiography. Scritti in onore del Prof. Giuseppe Tesauro nel XXV anno del Suo insegnamento. Montanino Editore, Napoli. II:1779—1784, 1962. 68

RAMSEY, E. M. AND HARRIS, J. W. S. Comparison of uteroplacental vasculature and circulation in the rhesus monkey and man. Carnegie Inst. Wash., Contrib. Embryol. 38:59 70, 1966.

RAMSEY, E. M., MARTIN, C. B., JR., AND DoNNER, M. W. Fetal and maternal placental circulations. Am. J. Obstet. Gynec. 981419-423, 1967.

RAMSEY, E. M., MARTIN, C. B., JR., MCGAUGHEY, H. S., JR., KAISER, I. H., AND DONNER, M. W. Venous drainage of the placenta in rhesus monkeys: radiographic studies. Am. J. Obstet. Gynec. 95:948—955, 1966.

REYNOLDS, S. R. M. Uterine accommodation of the products of conception: physiologic considerations. Am. J. Obstet. Gynec. 532901-913, 1947.

WISLOCKI, G. B. AND STREETER, G. L. On the placentation of the macaque (Macaca mulatta), from the time of implantation until the formation of the definitive placenta. Carnegie Inst. Wash., Contrib. Embryol. 2721-66, 1938.



Cite this page: Hill, M.A. (2019, November 13) Embryology Paper - Placental circulation. Retrieved from https://embryology.med.unsw.edu.au/embryology/index.php/Paper_-_Placental_circulation

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