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| [[File:Mark_Hill.jpg|90px|left]] This historic 1972 paper by Ramsey describes development of the placental circulation. The paper uses human and monkey embryos from the [[Carnegie Collection]].
| [[File:Mark_Hill.jpg|90px|left]] This historic 1972 paper by Ramsey (17 February 1906 - 2 July 1993)  describes development of the placental circulation. She published extensively on placental and embryonic development and this paper uses both human and monkey placentas from the [[Carnegie Collection]]. Dr. Ramsey discovered the "Yale" embryo and was a member of the Carnegie Institute's [[Carnegie Collection|embryology department]] research group from 1932 to 1971 when she retired. In addition to her research articles she published 2 books "The Placenta of Laboratory Animals and Man" (1975) and "Placental Vasculature and Circulation" (1982).  
<br>
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See the links below for the current placenta notes pages.
Search PubMed: [https://www.ncbi.nlm.nih.gov/pubmed/?term=Ramsey%20EM%5BAuthor%5D&cauthor=true&cauthor_uid=11616343 Author - Ramsey EM]
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See also {{#pmid:10825630}}
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'''Modern Notes:''' {{monkey}}
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{{Placenta Links}}
{{Placenta Links}}
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{{Historic Disclaimer}}
{{Historic Disclaimer}}
=Placental Circulation=
=Placental Circulation=
[[File:Elizabeth M. Ramsey.jpg|thumb|alt=Elizabeth M. Ramsey|Link=Embryology History - Elizabeth Ramsey|Elizabeth M. Ramsey,  M.D. (1906-1993)]]


MCV QUARTERLY 8(1): 61-68, 1972
[[Embryology History - Elizabeth Ramsey|Elizabeth M. Ramsey, M.D.]]




Elizabeth M. Ramsey, M.D.
Visiting Professor of Obstetrics and Gynecology, University of Virginia


Visiting Professor of Obstetrics and Gynecology, University of Virginia


School of Medicine, Charlottesville, Virginia
School of Medicine, Charlottesville, Virginia


* 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
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 [[Carnegie Collection|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).
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
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.
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
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).
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).


[[File:Ramsey1972 fig01.jpg|600px]]


Fig. 1—Camera lucida drawings of the vascular bed at three
'''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.)
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
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.
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.


[[File:Ramsey1972 fig02.jpg|600px]]


'''Fig. 2.''' Photomicrograph of an early human implantation. (a) trophoblastic lacunae; (b) maternal capillaries. [[Carnegie Collection]] {{CE8004}}, 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. 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.)
[[File:Ramsey1972 fig03.jpg|600px]]


'''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.


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.


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.


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.


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 terminal dilatations of arteries communicating with the intervillous space appear to be
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 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.
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.  
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,
[[File:Ramsey1972 fig04.jpg|600px]]
fetal blood courses through the umbilical arteries
<br>
into the subdivisions which run laterally through
{|
the chorionic plate. Finally, the vessels dip into the
! colspan=4|Maternal Placental Artery Remodelling
substance of the placenta and travel through the
|-
arborizations of the fetal villous tree. -They proceed in comparable subdivisions to the terminal
| [[File:Ramsey1972 fig04-16a.jpg|200px]]
villi. There the fetal capillary bed, coming into its
| [[File:Ramsey1972 fig04-16b.jpg|200px]]
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
| [[File:Ramsey1972 fig04-16c.jpg|200px]]
umbilical vein and thence to the fetal body (Martin
| [[File:Ramsey1972 fig04-16d.jpg|200px]]
and Ramsey, 1970).
| [[File:Ramsey1972 fig04-16e.jpg|200px]]
|-
| {{GA}} 8 weeks
| {{GA}} 16 weeks
| {{GA}} 20 weeks
| {{GA}} 32 weeks
| term
|}


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
<br>
with cineradioangiography, it is possible to visualize
'''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. Embryol. 38: 43-58, 1566.)
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
 
TERMINA-L SAC
 
BASE or ENDOMETRIUM ; . "'E““"“"L 5“:
 
SPIRAL ARTERV SPNAL ARTERYI
 
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EIASAL ARTERY 1 (PA \f4LE.|gILED) L
 
ARCUATE ARTERY
 
FERITONEAL SURFACE
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MARGIN or |NTEVR\/ILLOUS SPACE PERITONEAL SURHCE
 
|5lh WEEK
 
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BASE or ENDOMETRIUM , E MARGIN or INTERVILLOUS SPACE "‘
3 p H _fi___,,__ ,_ , 1 ‘ BASE or ENDOMETRlUM~
 
PERITONEAL SURFACE
 
Bth WEEK
 
A  E Ancufls ARTERY new WEEK
 
Human
 
I6 WEEKS 20 WEEKS
 
H79)! YIIAL S0flfACE
 
8 WEEKS
 
32 WEEKS FULL TERM
 
nyonnnwt sunncr
 
HYD;1£TEIAL sunucr
 
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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 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;.) >


   
The propulsive force throughout is the head of maternal blood pressure which drives blood into the intervillous space in discreet, fountain-like “spurts.” The incoming blood wafts aside the villi surrounding the orifices of entry, but once the propulsive force is reduced, in part by the, baffle action of the villi, the blood disperses laterally crowding the existing content of blood through the venous orifices in the basal plate into the uterine 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. 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.) '


tractions both inflow and outflow cease, in whole
[[File:Ramsey1972 fig05a.jpg|600px]]
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
[[File:Ramsey1972 fig05b.jpg|600px]]


Fig. 6——Photomicrograph of a human uteroplacental artery
'''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.)
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
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
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).


throughout. Thus, under normal conditions, continued maternal-fetal exchange is made possible.
[[File:Ramsey1972 fig06.jpg|600px]]


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
[[File:Ramsey1972 fig07.jpg|600px]]


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.,
[[File:Ramsey1972 fig08.jpg|600px]]
Contrib. Embryol. 36:153—182, 1957.


DONNER, M. W., RAMSEY, E. M., AND CORNER, G. W., JR.
'''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.)
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
[[File:Ramsey1972 fig09.jpg|600px]]
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.
{{Ref-Bartelmez1957}}


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.
{{Ref-HarrisRamsey1966}}
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
{{Ref-Hertig1945a}}
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.
{{#pmid:4986963}}
Obstet. Gynec. 95:948—955, 1966.


REYNOLDS, S. R. M. Uterine accommodation of the products
{{#pmid:4958128}}
of conception: physiologic considerations. Am. J. Obstet.
Gynec. 532901-913, 1947.


WISLOCKI, G. B. AND STREETER, G. L. On the placentation
{{#pmid:20247845}}
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.


{{Ref-WislockiStreeter1938}}


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Ramsey EM. Placental Circulation. (1972) MCV Quarterly, 8(1): 61-68.

Online Editor  
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This historic 1972 paper by Ramsey (17 February 1906 - 2 July 1993) describes development of the placental circulation. She published extensively on placental and embryonic development and this paper uses both human and monkey placentas from the Carnegie Collection. Dr. Ramsey discovered the "Yale" embryo and was a member of the Carnegie Institute's embryology department research group from 1932 to 1971 when she retired. In addition to her research articles she published 2 books "The Placenta of Laboratory Animals and Man" (1975) and "Placental Vasculature and Circulation" (1982).


Search PubMed: Author - Ramsey EM
See also Longo LD & Meschia G. (2000). Elizabeth M. Ramsey and the evolution of ideas of uteroplacental blood flow and placental gas exchange. Eur. J. Obstet. Gynecol. Reprod. Biol. , 90, 129-33. PMID: 10825630

Modern Notes: monkey

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Placental Circulation

Elizabeth M. Ramsey
Elizabeth M. Ramsey, M.D. (1906-1993)

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).

Ramsey1972 fig01.jpg

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.

Ramsey1972 fig02.jpg

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.

Ramsey1972 fig03.jpg

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.

Ramsey1972 fig04.jpg

Maternal Placental Artery Remodelling
Ramsey1972 fig04-16a.jpg Ramsey1972 fig04-16b.jpg Ramsey1972 fig04-16c.jpg Ramsey1972 fig04-16d.jpg Ramsey1972 fig04-16e.jpg
GA 8 weeks GA 16 weeks GA 20 weeks GA 32 weeks term


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. Embryol. 38: 43-58, 1566.)

The propulsive force throughout is the head of maternal blood pressure which drives blood into the intervillous space in discreet, fountain-like “spurts.” The incoming blood wafts aside the villi surrounding the orifices of entry, but once the propulsive force is reduced, in part by the, baffle action of the villi, the blood disperses laterally crowding the existing content of blood through the venous orifices in the basal plate into the uterine 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.


Ramsey1972 fig05a.jpg

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;.)


Ramsey1972 fig05b.jpg

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).

Ramsey1972 fig06.jpg

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.

Ramsey1972 fig07.jpg

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.)

Ramsey1972 fig08.jpg

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.)

Ramsey1972 fig09.jpg

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

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 JWS. and Ramsey EM. The morphology of human uteroplacental vasculature. (1966) Contrib. Embryol., Carnegie Inst. Wash. Publ. 625, 38: 43-58.

Hertig AT. and Rock J. Two human ova of the pre-villous stage, having a developmental age of about seven and nine days respectively. (1945) Contrib. Embryol., Carnegie Inst. Wash. Publ. 557, 31: 65-84.

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 EM, Martin CB & Donner MW. (1967). Fetal and maternal placental circulations. Simultaneous visualization in monkeys by radiography. Am. J. Obstet. Gynecol. , 98, 419-23. PMID: 4986963

Ramsey EM, Martin CB, McGaughey HS, Kaiser IH & Donner MW. (1966). Venous drainage of the placenta in rhesus monkeys: radiographic studies. Am. J. Obstet. Gynecol. , 95, 948-55. PMID: 4958128

REYNOLDS SR. (1947). Uterine accommodation of the products of conception; physiologic considerations. Am. J. Obstet. Gynecol. , 53, 901-13. PMID: 20247845

Wislocki GB. and Streeter GL. On the placentation of the macaque (Macaca mulatta), from the time of implantation until the formation of the definitive placenta.. (1938) Contrib. Embryol., Carnegie Inst. Wash. 721-66.

© 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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