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Embryonic development of coronary vasculature in ratsCorrosion casting studies.

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Embryonic Development of Coronary
Vasculature in Rats: Corrosion
Casting Studies
Department of Pathological Anatomy, Medical University of Warsaw,
Warsaw, Poland
Department of Anatomy, Medical University of Warsaw, Warsaw, Poland
Department of Pathology, Children’s Memorial Health Institute, Warsaw, Poland
The aim of this study was to analyze the development of coronary vessels at different
stages of embryonic life in rats using corrosion casts and scanning electron microscopy (SEM).
We studied morphologic details of vessel maturation, expansion, and pattern formation from
the stage of development when the coronary system forms patent connections with the aorta
and the right atrium (embryonic day 16 (ED16)) to full-term fetus (ED21). The internal
surface morphologies of the arterial and venous vessel walls were different and were dependent on the distance from the orifice and the capillary system. They also depended on the
maturation state of a given vessel. In various branches of the coronary system we demonstrated round, fusiform or polygonal, endothelial cell imprints. The capillary network was
dense, however, at the early stages of development, it formed a thin layer over the myocardium. By ED21 capillaries assumed an orientation parallel to the long axes of the cardiac
myocytes. During all stages of development, different forms of angiogenesis by intussusceptive growth were observed. Splitting of the vessel wall occurred in two or three points along
the vessel, forming two- or three-link chains. Certain areas of vessels resembled doughnuts,
from which several sister vessels originated. The coronary arteries were situated deep within
the myocardial wall. The major coronary veins were mostly located on the surface of the
capillary plexuses of the myocardial wall. In conclusion, this method of vessel casting enables
the detection of angiogenesis by intussusceptive growth, and the visualization of a capillary’s
position to the myocardial wall, thickness of the capillary plexuses, and the internal surface
morphology of major vessels. Anat Rec Part A 270A:109 –116, 2003. © 2003 Wiley-Liss, Inc.
Key words: coronary vessel; corrosion cast; fetal rat heart; angiogenesis; scanning electron microscope
Vascularization of the rat myocardium starts relatively
late during embryonic development, on embryonic day 13
(ED13) (Heinzberger, 1983). The formation of new blood
vessels in the embryonic heart is accomplished by at least
two processes: 1) vasculogenesis (Rongish et al., 1994;
Risau, 1997), which includes in situ formation of cell clusters consisting of angioblasts and erythroblasts, which
then differentiate into endothelial cells and erythrocytes,
respectively; and 2) angiogenesis (Tomanek et al., 1996),
i.e., the sprouting of new vessels from preexisting ones.
Throughout embryonic life, both vasculogenesis and angiogenesis take part in the formation of coronary vessels.
Endothelial cells differentiate (vasculogenesis) and then
coalesce, forming a lumen. Subsequently, they arborize
(angiogenesis) to finally form a continuous, patent system
of tubes called primitive vessels, within which blood circulates (Risau, 1997).
Despite the growing number of publications in this field,
some of the morphologic details of coronary vessel angiogenesis are still undefined. The heart is a pump that
undergoes vascularization very late, considering the rat’s
Grant sponsor: KBN; Grant number: 6P05A02520; Grant sponsor: Medical University of Warsaw.
*Correspondence to: Anna Ratajska, Department of Pathological Anatomy, Medical University of Warsaw, Chałubińskiego 5,
02-004 Warsaw, Poland. Fax: ⫹48-22-629-98-92.
Received 21 December 2001; Accepted 1 October 2002
DOI 10.1002/ar.a.10011
Fig. 1. a: ED16 heart, posterior surface with the atria removed.
Surface vessels of the left ventricle were removed to demonstrate the
trabecular system of this region of the heart. The thin capillary plexus
covers the right ventricle. One vein runs along the atrioventricular sulcus
and congregates vessels coming from the direction of the apex. b:
Higher magnification of the coronary venous system of the right ventricle, with details of the capillary plexus. Round endothelial cell imprints
can be seen on the surface of venules. Bar ⫽ 100 ␮m.
short embryonic period of life (between ED13 and ED21).
Some forms of angiogenesis extend into early postnatal
life (Tomanek, 1996). During the early period of embryonic
development, the avascular heart is nourished from the
lumen by blood circulating within the trabecular system
(Ošt’ádal et al., 1975). Subsequently, the myocardial wall
thickens, and trabeculae gradually become flatter and
wider (Ošt’ádal et al., 1975). On ED16 –17, coronary arteries form patent connections with the aorta (Bogers et
al., 1988; Ratajska and Fiejka, 1999), and probably at
about the same time (based on the studies in quail heart
by Vrancken Peeters et al. (1997a) the venous system
forms a connection with the right atrium.
Corrosion casts of the coronary system can only be made
after formation of patent coronary vessel connections with
the heart’s chambers. The number of studies of heart
vascularization has dramatically increased during the last
decade due to the development of various morphological,
immunohistochemical (Poelmann et al., 1993; Vrancken
Peeters et al., 1997a, b, 1999), and India ink injection
Fig. 2. ED16 heart. a: Conal part with the pulmonary trunk (pt) in the
front and the aorta (a) behind on the left; a vessel plexus surrounding the
truncus arteriosus and the conus forms a thin layer of capillaries. b:
Higher magnification of the ascending aorta with the right coronary sinus
(the orifice of the right coronary artery marked with arrow); endothelial
cell imprints within the sinus and the proximal aorta are polygonal. c:
Higher magnification of the proximal part of the left coronary artery
coursing from the aorta (which is hidden behind the pulmonary trunk),
with longitudinally oriented endothelial cell imprints in the proximal part
(arrow) and oval or round endothelial cell imprints at a certain distance
from the orifice. Bar ⫽ 100 ␮m.
Fig. 3. ED16 heart. The anterior surface of the right ventricle with a
connection of a capillary with the ventricular chamber marked with arrow
(fistula). Bar ⫽ 100 ␮m.
techniques (Waldo et al., 1990; Vrancken Peeters et al.,
1997b), as well as retrovirus labeling methods (Mikawa
and Fischman, 1992; Mikawa and Gourdie, 1996). However, little is known about the formation and distribution
of coronary arteries, veins, and capillaries, and their three
dimensional pattern during fetal heart development in
rats. The corrosion cast technique has been successfully
utilized in studies of abnormal patterning of vessels
within the myocardium (Bockman et al., 1989; Sans-Coma
et al., 1999). In the present study we applied this technique to extend our knowledge of the normal development
of coronary vessels. We studied rat heart vascularization
during the period of embryonic life between ED16 (i.e., the
time when the coronary system makes patent connections
with the aorta) and ED21 (full-term fetus).
All procedures were performed according to the requirements of the Animal Care Ethics Committee of Poland,
and in accordance with the NIH Guidelines for the Care
and Use of Laboratory Animals.
Pregnant dams of the Wistar Albino Glasgow (WAG)
strain were used for the experiments. The animals were
kept in cages with standard laboratory food and water at
libitum (12/12-hr light/dark cycles). Day 0 of pregnancy
was estimated by the presence of spermatozoa in the
early-morning vaginal smear. Dams were anesthetized
with narcotan and chlorohydrate (100 mg/kg b.w., i.p.),
and the fetuses were removed and additionally treated
with chlorohydrate. The fetuses were then divided into six
age groups: ED16 –ED21 (full term). At least five fetuses
were used in each experimental group.
Corrosion Cast Technique
The fetuses were perfused via the umbilical artery with
3 ml of a prewarmed (37°C) heparinized saline (12.5 I.U./
ml), containing 3% dextran, M.W. 70,000 and 0.025% lidocain (Lignocain, Polfa, Poland) until a pure solution
from the umbilical vein was obtained. Subsequently, perfusion fixation was carried out with 2–3 ml of 0.08% glutaraldehyde/0.66% paraformaldehyde in 0.15 M cacody-
Fig. 4. a: ED18 heart. Maturation of the venous system. A vein
coursing horizontally (above) with its surface marked with round imprints
of endothelial cell nuclei and transverse indentations. b: ED19 heart with
“bypass vessels” (microvessels that bypass the main route of a major
vein and coalesce with this vein again at a lower level). Bar ⫽ 100 ␮m.
late buffer, pH 7.4, 37°C. Finally, a mixture consisting of
8 ml Mercox威 CL-2R (Vilene Comp., Japan) and 2 ml
methyl methacrylate (Fluka) containing 0.2 g MA initiator
per 10 ml of the casting medium was injected (in a volume
of 2 ml). Hearts were removed and placed in water overnight at 50°C to allow the resin to harden. Subsequently,
the soft tissue of the myocardium was macerated with
10% KOH and rinsed with tap water (Lametschwandtner
et al., 1990; Miodoński and Litwin, 1999). The resulting
vascular casts were dried, mounted onto specimen stubs,
coated with carbon and gold, and examined in a Jeol
JSM-35C scanning electron microscope at 25kV.
Histological Examination
Some fetal hearts of 21-day-old rats were fixed in 4%
buffered formalin, dehydrated in a series of increasing
alcohol concentrations, and embedded in paraffin. Serial
sections were cut and stained with hematoxylin-eosin.
Morphometry and Statistical Analysis
Scanning electron microscopy (SEM) images were used
for measurements of proximal diameters of both coronary
Fig. 5. Different forms of angiogenesis by intussusceptive growth
demonstrated in embryonic hearts. a: ED18 heart: angiogenesis is visible
as a chain of three consecutive splitting loops along the same capillary
(arrow). b: ED19 heart: angiogenesis within a vein representing a doughnut-like structure (arrow); there are three or four vessels branching off in
various directions. Bar ⫽ 100 ␮m.
arteries and distal branches of two major veins running on
the posterior surface of the ventricles. The same respective vessels were measured at the earliest and the latest
stages of development (ED16 and ED21). At least three
measurements were taken of every vessel by the use of an
image analysis program (Multiscan). The results were
presented as the mean value ⫾ standard deviation.
In ED16 hearts the outer surface of the myocardial wall
was covered with vascular plexuses, which appeared to be
discontinuous over the whole myocardium. The trabecular
system of the ventricles was visible under the thin capillary surface (Fig. 1a and b). Capillaries and primordial
veins and arteries were distinguished. Morphologically,
these vessels were very similar at this stage of development. However, the veins and arteries had larger diameters than the capillaries (44 ␮m for veins, 36.6 ⫾ 2.9 ␮m
for arteries, and 15.4 ⫾ 3.84 for capillaries). Capillaries
over the surface of the heart close to the apex were oriented haphazardly (not shown). The surface of veins was
Fig. 6. a: The conus of an ED21 heart with capillaries running obliquely in the proximal part (upstream) and transversely in the distal part
(downstream). b: Higher magnification of the distal part of the heart
conus with capillaries arranged transversely; arrow points to the cranial
direction; pt, pulmonary trunk. Bar ⫽ 100 ␮m.
marked with round endothelial cell imprints. The major
veins were located on the posterior surface of the ventricles. The veins at this stage of heart development were
short. Thus, the proximal end of these vessels was situated not far from the base of the heart. The course of some
veins overlapped the atrioventricular sulcus. The conus of
the heart was covered with a thin capillary plexus forming
a wreath around this part of the heart (Fig. 2a). The vessel
plexus in this area consisted of one layer of capillaries,
under which the surface of the conotruncus was seen. The
coronary sinuses were imprinted with polygonal nuclei of
endothelial cells. Imprints of the same shape were also
found in the wall of the aortic and pulmonary trunk roots
(Fig. 2b). The proximal part of the coronary artery had
fusiform endothelial cell imprints oriented longitudinally
to the direction of the blood flow, whereas at a certain
distance from the coronary sinus the imprints on the coronary artery surface were round (Fig. 2c). In one case we
observed a coronary vessel fistula (a connection of a capillary with the ventricular chamber) (Fig. 3, arrow).
On ED17, the thickness of the capillary plexus increased within the myocardial wall. The major veins were
Fig. 7. a: ED19 heart. Parallel orientation of the capillary plexus on
the posterior surface of the left ventricle. b: ED21 heart, right-posterior
surface: superficial capillaries run in a vertical orientation (long arrow);
beneath. Capillaries run in a horizontal orientation (short arrow). Bar ⫽
100 ␮m.
located on the posterior surface of the left and right ventricles, and their proximal ends were located closer to the
apex of the heart compared with the respective veins of
ED16 hearts (not shown). Both veins merged with their
minor tributaries into the coronary sinus, or the right vein
went directly into the right atrium, independently of the
coronary sinus. Some veins were situated on the lateral
and anterior surfaces of the outflow tract. Coronary arteries and their branches coursed deep within the myocardial
wall, except for their very proximal portion, which ran
subepicardially. Starting from ED17 and later during development, the capillaries within the myocardial wall
tended to be oriented parallel to the long axes of the
cardiac myocytes.
ED18 and ED19 hearts were completely covered with
dense capillary plexuses that ran within the thickened
myocardial wall. Distal branches of the coronary arteries
were completely covered with thick capillary plexuses.
Venules and their minor tributaries could be distinguished by the presence of round or oval endothelial cell
imprints on their surface, and by transversely oriented
indentations (Fig. 4a; compare with the ED16 heart in Fig.
1a, in which the veins are devoid of indentations). Some
Fig. 8. a: ED20 heart viewed from the front; the pulmonary trunk has
been removed. The aorta with the coronary sinuses and the proximal
coronary arteries can be seen. b: Proximal part of the left coronary artery
at the level of branching (close to the aortic sinus), with longitudinally
oriented endothelial cell imprints. Bar ⫽ 100 ␮m.
veins on the posterior wall of the ventricle formed an
unusual pattern with “bypassing” capillaries (Fig. 4b). In
the latter case, these vessels were highly convoluted and
formed structures, bypassing the main route of the great
vein and then coalescing with the same vein again at a
lower level.
Intussusceptive angiogenesis was distinguishable on
the surface of the ventricular wall at all stages (Fig. 5a
and b). Various forms of intussusceptive angiogenesis
were identified by the presence of small pits and holes,
and capillaries splitting into two sister vessels (not
shown). In some areas capillary splitting occurred in two
or three adjacent places along the capillary wall, creating
two- or three-link chain structures, respectively (Fig. 5a).
In another case a fragment of a small vein formed a
structure resembling a doughnut, from which several descendent vessels originated (Fig. 5b).
On ED20 –21 the right ventricular conus was covered
with a thick, dense capillary plexus, within which capillaries took on a specific orientation along cardiac myocytes
traversing obliquely within the conal wall (Fig. 6a). Distally (upstream), at the origin of the pulmonary trunk (at
Fig. 9. ED19 heart with the atria removed. The right-posterior surface
of the ventricles with major veins coursing superficially. The veins on the
heart conus are short, whereas the proximal ends of the veins running on
the posterior part of the ventricles are close to the apex. Bar ⫽ 100 ␮m.
the arterio-myocardial border) the capillaries were oriented circularly (Fig. 6b). In the fetal myocardium at these
stages of development, the capillary system imitated the
orientation of cardiac myocytes. In certain parts of the
myocardial wall, the capillary system formed strata with a
different orientation of capillaries. In the posterior part of
the left ventricle, capillaries were oriented parallel to the
tributaries of the major vein, i.e., transversely to the long
axis of the heart (Fig. 7a). The posterior wall of the right
ventricular myocardium (close to the interventricular septum) contained vertically and horizontally oriented capillaries in different strata (Fig. 7b). Both coronary arteries
and their branches (Fig. 8a and b) together with the venous system (Fig. 9) could be distinguished. The mean
diameter of coronary arteries at their proximal courses
was 90.9 ⫾ 13 ␮m, whereas the mean diameter of veins
measured at their distal courses was 81.3 ⫾ 9.7 ␮m. The
arteries and veins took an analogous position and course
to the respective vessels in adult rat heart. Some veins
coursing within the subepicardium of the proximal interventricular sulcus accompanied the superficial branches
of the left coronary artery (Fig. 10). The veins coursing
within the conal and lateral parts of the heart were short:
their proximal ends were situated in the middle of the
ventricular length (Fig. 9). The veins of the right ventricular epicardium did not accompany the respective
branches of the right coronary artery. The same was true
for the veins running on the posterior surface of both
ventricles (Fig. 10).
On ED20 –21, the coronary artery sinuses within the
aortic wall were entirely developed (Fig. 8a and b). Fusiform endothelial cell imprints within the proximal portion
of the coronary artery were oriented longitudinally to the
blood stream, whereas endothelial cell imprints within the
sinuses of Valsalva did not have such a regular orientation, and assumed polygonal shapes.
The present work describes for the first time the sequence of events taking place during embryonic coronary
Fig. 10. ED21 heart, H&E staining. a: The proximal part of the left
coronary artery (large arrowhead) branching off the aorta with an accompanying vein (small arrowhead); the vein courses subepicardially
within the conal part of the heart. b: At the level of the artioventricular
junction the subepicardially coursing veins (small arrowheads) accompany two branches of the left coronary artery, whereas two branches of
the right coronary artery (large arrowhead) do not have their venous
counterparts subepicardially; bar ⫽ 200 ␮m. c: Major veins run subepicardially (small arrowheads) on the posterior surface of the ventricles,
whereas the respective arteries (or their branches) course at a certain
distance within the myocardial wall (large arrowheads). d: Higher magnification of the area shown in b, representing the anterior interventricular septum with four branches of the left coronary artery (two of them
marked with large arrowheads) and accompanying veins (small arrowheads). Bar ⫽ 100 ␮m.
angiogenesis by means of the corrosion cast method. Since
the first steps of the angiogenic process involve interactions between cell clusters that do not form continuous
channels within the myocardium (Bogers et al., 1989;
Poelmann et al., 1993; Rongish et al., 1994), it is not
possible to study these stages (vasculogenesis) by the corrosion cast technique. The corrosion cast technique can be
very useful in demonstrating those angiogenic events that
occur after the formation of a patent system of vessels
continuous with the fetal circulation.
Studies by van Groningen et al. (1991) have dealt with
rat heart vascularization in the prenatal and early postnatal periods of life by corrosion cast and quantitative
methods. We focused only on the embryonic period, and
extended the study by adding some important data to this
topic. First, we have described in detail for the first time
the coronary system at the very early stages of development (ED16), when coronary arteries first form patent
connections with the aorta. Second, we found that in ED16
hearts the coronary system consists of a very thin layer of
capillary plexuses and larger vessels (primordial arteries
and veins). The larger vessels on the posterior side of the
heart have the surface morphology of veins with typical
round endothelial cell imprints. As the process of vein
maturation proceeds, additional marks on their internal
surface can be seen in the form of transverse indentations.
During later stages of development this system of vessels
thickens as the myocardium enlarges, and the trabeculae
gradually become flatter. Third, we confirmed previous
observations from corrosion casts made on ED16 and
ED21 (van Groningen et al., 1991) that angiogenesis is
characterized by certain morphological signs, such as the
formation of “splitting vessels” which divide into sister
vessels. These events correspond to the time sequence of
new vessel formation by intussusceptive growth (Burton
and Palmer, 1989; Burri and Tarek, 1990; Patan et al.,
1993; Miodoński et al., 1998). In addition we demonstrated the existence of other forms of angiogenesis by
intussusceptive growth, during which new vessels start to
develop from veins, creating structures similar to doughnuts. In the case of “bypass” vessels, the newly formed
vessels could originate either from a large vein that gives
off capillaries, or from a single capillary that further splits
into two vessels (one remaining a capillary, and the other
differentiating into a large vein). We have also shown with
this method that coronary vessel maturation and differentiation involves certain changes on their internal surface by characteristic nuclear imprints of endothelial cells.
These imprints occur first when coronary circulation becomes patent and connects with the whole-body circulation. The shapes of these imprints may depend on the
velocity of blood flow within the vessel, and may be related
to the vessel shape. For example, within the sinuses of the
aorta and the pulmonary trunk (with wall shapes similar
to hemispheres) the imprints are polygonal; in the ascending aorta and the proximal part of the coronary arteries
(cylinder-like shapes) the imprints are fusiform, with the
long axes oriented longitudinally to the direction of the
blood flow. Interestingly, in very young fetuses the endothelial cell imprints are oval on the surface of coronary
arteries at a certain distance from the orifice, as in veins
(low blood flow velocity). The surface of postarterial capillaries within the capillary plexuses is smooth.
Our present study indicates that the early system
(ED16) of venules tends to be localized close to the atrioventricular sulcus, leaving the rest of the myocardial wall
void of larger coronary vessels. The venules (precursors of
major veins) are very short at this stage of development.
The same tendency was demonstrated in our previous
study with regard to the arterial system: the length of the
coronary artery is small compared with ventricular length
on ED16 –17, and increases rapidly at later stages of development (Ratajska et al., 2000). Other studies of quail
hearts (Vrancken Peeters et al., 1997b), in which the India
ink injection technique was used, also suggest the existence of very short coronary arteries and veins just after
the formation of patent connections with the aortic lumen.
These studies indicate that the expansion of the venous
and arterial systems during embryonic life proceeds toward the heart apex.
The capillary plexus of the myocardial wall is very thin
at this stage and appears to be discontinuous. The demonstration of capillaries throughout the myocardium with
other techniques (Ratajska and Fiejka, 1999) may indicate
a lack of patency between the respective groups of capillary plexuses at these early stages.
During later stages of development (starting from
ED18) the diameter of both coronary arteries and veins
increases markedly. The maturation of veins during all
stages of development is demonstrated by a change of
their internal surface morphology: in ED16 hearts endothelial cell imprints are weak, and later (ED18 –21) the
imprints on the internal surface of veins are more prominent and accompanied by transverse indentations. The
shape of aortic sinuses changes during development (com-
pare Figs. 2b and 8a). There are also some differences
among species. Compared with chicken embryonic hearts
at the same developmental stage (Aikawa and Kawano,
1982), in which the aortic sinuses are oval and flat in
shape, in the rat the sinuses are round and bulgy.
Since corrosion casting samples are very fragile, we
were unable to use this technique to analyze the surface
morphology of deeply located coronary arteries, branches,
and vessels covered by dense capillaries. Thus, to localize
the arterial system we performed histological analysis of
serial sections of ED21 hearts. The arteries and their
branches are located deep within the myocardial wall.
Interestingly, the veins in most areas of the heart usually
do not accompany the respective arteries within the rat
myocardium, with the exception of veins running on the
left surface of the outflow tract, which are situated close to
the respective arteries (namely, the superior branches of
the left coronary artery). Major veins have a tendency to
run on the posterior surface of the ventricles and on the
lateral surfaces of the outflow tract. The veins of the
outflow tract are short. By the end of fetal life, the pattern
of major vessel distribution reaches a final shape and
position equivalent to those seen in the adult rat heart
(Jons and Olson, 1954; Dbalý et al., 1968; Beighley et al.,
1997). The course and branching system of the major
vessels, however, appear to depend on the rat strain.
The morphological pattern of the capillary plexuses at
the beginning of their formation is irregular, except for the
conal part of the heart, where they become oriented circularly around the conus in the early stages of development.
At later developmental stages the capillaries are usually
oriented parallel to the long axes of the myocytes. Thus,
during the earlier stages of development, which are characterized by immature shapes of cardiac cells, myocardial
capillaries also show an irregular orientation.
In this study we presented one example of a connection
between the coronary system and the ventricular chamber. We suspect that these connections (fistulas) are rare
during normal heart development, because in our other
studies (performed by serial section analysis) we found
few of them (data not published).
Interestingly, at the bases of the major vessels extending from the heart (the pulmonary trunk and the aorta),
the capillary system is oriented in a very regular way and
tends to encircle the roots of the great vessels. This pattern of distribution may reflect the direction of cardiac
myocytes in this region of the heart.
The authors are thankful to Prof. B. Woźniewicz, the
head of the Department of Pediatric Pathology, Children’s
Memorial Health Institute in Warsaw, for access to the
scanning electron microscope. We are also grateful to Prof.
A. Miodoński, Collegium Medicum of the Jagiellonian
University of Kraków, for his expert suggestions and discussion. The technical photographic assistance of Piotr
Gawdzis is greatly appreciated.
Aikawa E, Kawano J. 1982. Formation of coronary arteries sprouting
from the primitive sinus wall of the chick embryo. Experientia
38:816 – 818.
Beighley PE, Thomas PJ, Jorgensen SM, Ritman EL. 1997. 3D architecture of myocardial microcirculation in intact rat heart: a study
with micro-CT. Adv Exp Med Biol 430:165–175.
Bockman DE, Redmond ME, Kirby ML. 1989. Alterations of early
vascular development after ablation of cranial neural crest. Anat
Rec 225:209 –217.
Bogers AJJC, Gittenberger-de Groot AC, Dubbeldam JA, Huysmans
HA 1988. The inadequacy of existing theories on development of the
proximal coronary arteries and their connections with the arterial
trunks. Int J Cardiol 20:117–123.
Bogers AJJC, Gittenberger de Groot AC, Poelmann RE, Peault BM,
Huysmans HA. 1989. Development of the origin of the coronary
arteries, a matter of ingrowth or outgrowth? Anat Embryol 180:
437– 441.
Burri PH, Tarek MR. 1990. A novel mechanism of capillary growth in
the rat pulmonary microcirculation. Anat Rec 228:35– 45.
Burton GJ, Palmer ME. 1989. The chorio-allantoic capillary plexus of
the chicken egg: a microvascular corrosion casting study. Scanning
Microsc 3:549 –559.
Dbalý J, Ošt’ádal B, Rychter Z. 1968. Development of the coronary
arteries in rat embryos. Acta Anat 71:209 –222.
Heinzberger CFM. 1983. Development of myocardial vascularization
in the rat. Acta Morphol Neerl-Scand 21:267–284.
Jons TNP, Olson BJ. 1954. Experimental myocardial infarction. Ann
Surg 140:675– 682.
Lametschwandtner A, Lametschwandtner U, Weiger T. 1990. Scanning electron microscopy of vascular corrosion casts—technique and
applications: updated review. Scanning Microsc 4:889 –941.
Mikawa T, Fischman DA. 1992. Retroviral analysis of cardiac
morphogenesis: discontinuous formation of coronary vessels. Proc
Natl Acad Sci USA 89:9504 –9508.
Mikawa T, Gourdie RG. 1996. Pericardial mesoderm generates a
population of coronary smooth muscle cells migrating into the heart
along with ingrowth of the epicardial organ. Dev Biol 174:221–232.
Miodoński AJ, Bugajski A, Litwin JA. 1998. Vascular architecture of
human urinary bladder carcinoma: a SEM study of corrosion cast.
Virchows Arch 433:145–151.
Miodoński AJ, Litwin JA. 1999. Microvascular architecture of the
human urinary bladder wall: a corrosion casting study. Anat Rec
Ošt’ádal B, Schiebler TH, Rychter Z. 1975. Relations between the
development of the capillary wall and the myoarchitecture of the rat
heart. Adv Exp Med Biol 53:375–388.
Patan S, Haenni B, Burri PH. 1993. Evidence for intussusceptive
capillary growth in the chicken chorio-allantoic membrane. Anat
Embryol 187:121–130.
Poelmann RE, Gittenberger-de Groot AC, Mentink MMT, Bökenkamp
R, Hogers B. 1993. Development of the cardiac coronary vascular
endothelium, studied with antiendothelial antibodies, in chickenquail chimeras. Circ Res 73:559 –568.
Risau W. 1997. Mechanisms of angiogenesis. Nature 386:671– 674.
Ratajska A, Fiejka E. 1999. Prenatal development of coronary arteries
in the rat: morphologic pattern. Anat Embryol 200:533–540.
Ratajska A, Fiejka E, Siemińska J. 2000. Prenatal development of
coronary arteries in the rat: morphometric pattern. Folia Morphol
Rongish BJ, Torry RJ, Tucker DC, Tomanek RJ. 1994. Neovascularization of embryonic rat hearts cultured in oculo closely mimics in
utero coronary vessel development. J Vasc Res 31:205–215.
Sans-Coma V, Durán AC, Fernández B, Fernández MC, López D,
Arqué JM. 1999. Coronary artery anomalies and bicuspid aortic
valve. In: Angelini P, editor. Coronary artery anomalies: a comprehensive approach. Philadelphia: Lippincott Williams & Wilkins. p.
Tomanek RJ. 1996. Formation of the coronary vasculature: a brief
review. Cardiovascular Res 31:E46 –E51.
Tomanek RJ, Haung L, Suvarna PR, O’Brien LC, Ratajska A, Sandra
A. 1996. Coronary vascularization during development in the rat
and its relationship to basic fibroblast growth factor. Cardiovasc
Res 31:E116 –E126.
Van Groningen JP, Wenink ACG, Testers LHM. 1991. Myocardial
capillaries: increase in number by splitting of existing vessels. Anat
Embryol 184:65–70.
Vrancken Peeters MPFM, Gittenberger-de Groot AC, Mentink MMT,
Hungerford JE, Little CD, Poelmann RE. 1997a. Differences in
development of coronary arteries and veins. Cardiovasc Res 36:101–
Vrancken Peeters MPFM, Gittenberger-de Groot AC, Mentink MMT,
Hungerford JE, Little CD, Poelmann RE. 1997b. The development
of the coronary vessels and their differentiation into arteries and
veins in the embryonic quail heart. Dev Dyn 208:338 –348.
Vrancken Peeters MPFM, Gittenberger-de Groot AC, Mentink MMT,
Poelmann RE. 1999. Smooth muscle cells and fibroblasts of the
coronary arteries derive from epithelial-mesenchymal transformation of the epicardium. Anat Embryol 199:367–378.
Waldo KL, Willner W, Kirby ML. 1990. Origin of the proximal coronary artery stems and a review of ventricular vascularization in the
chick embryo. Am J Anat 188:109 –120.
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development, vasculature, ratscorrosion, embryonic, coronary, casting, studies
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