Paper - The development of the cardiac-coronary circulatory system
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Goldsmith JB. and Butler HW. The development of the cardiac-coronary circulatory system. (1937) Amer. J Anat. 60(2): 186-
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The Development Of The Cardiac-Coronary Circulatory System
Joseph B. Goldsmith And H. W. Butler
Oklahoma University School of Medicine
Four Text Figures And Two Plates (Seventeen Figures)
Aided by a grant from the research appropriation of the University of Oklahoma Medical School.
Very little careful work has been done on the development of the cardiac-coronary circulation. Grant (’26), describes the origin of both arteries and Veins in the rabbit and in the same paper discusses the embryonal heart sinusoids and the probable nature of the peculiar epithelial buds observable on the younger hearts. Lewis (’04), in a paper on the major embryonal sinusoids, discusses brieﬂy the cardiac-coronary system in embryos of the Torpedo and the rabbit. Wheeldon (’16), in a description of the anatomy of a 20-mm. pig embryo, mentions the presence of a well—developed system of arteries, veins and capillaries in the heart of this age embryo. Martin (1894), gives an incomplete account of this system in the younger embryos of frogs and rabbits. Tandler (’O8), writing in ‘Keibel and Elze’ notes the beginning of the coronary arteries from the base of the aorta in a 17-mm. human embryo. Of the above-mentioned papers only Grant has attempted to describe a few age extensions of the arteries and veins and those are neither complete nor illustrated. Since the cardiac-coronary system is so important clinically, it seems worthwhile to make a complete study of its development.
Material and Methods
The material used in this study was composed exclusively of pig embryos in a closely graded series extending from the 2 mm. to over 300 mm. in length. The adult cardiac-coronary pattern is completed long before the embryo is in the 300 mm. stage. The smaller embryos were studied exclusively as serial sections, the medium—sized embryos were studied both in serial sections and injected material and the larger embryos only as injected specimens.
The material was obtained fresh from the packing plant. The smaller embryos were placed in the ﬁxative immediately, while the others were brought to the laboratory and injected with a Warm gelatin color mass before being ﬁxed. The embryos were ﬁxed in 10% formalin, Bouin’s solution or Goldsmith’s chrom-acetic—dichromate mixture, all giving equally satisfactory results. Alum cochineal counter—stained with orange G and Harris’s haematoxylin were used as stains.
At the onset of the study injections were done with a small syringe. Not being satisﬁed with the results obtained in this manner, a special manometer pressure instrument with a special needle holder was designed by the senior author. The injection mass was introduced into the embryo either through the walls of the apex of the heart or through the umbilical artery. Injections through the artery gave slightly more desirable results. Reconstruction models were made of the hearts of the younger embryos, using the blotting paper method as recommended by Mrs. Gage. The hearts of the older embryos were removed and studied as whole mounts.
The development of any portion of the circulatory system is variable in its time relationships. Because of this, the following descriptions apply to the average of the age under consideration and not to any one particular specimen. Likewise the drawings illustrating the age extensions of the various vessels are composite in nature and not speciﬁc for any one specimen.
Description of Ages
The primitive condition. It seems unnecessary to describe the primitive circulation of the mammal, however, for the sake of completeness and also as a starting point, the proximal part of this early circulation will be reviewed brieﬂy. With the heart as a single tube, looped into an open S-shaped condition, there are present eight tubes opening into it, six which carry blood toward the heart with two carrying it away. The anterior afferent tubes are the paired ventral aorta which remain separate tubes only a very short time, becoming fused very early into a single tube.
The six posterior efferent tubes are composed of three paired Vessels as follows: 1) The vitelline veins, which come from the chorion, courses along the gut and enters the heart at the posterior end. Later when the liver arises the hepatic portion of each of these veins join with the hepatic sinusoidal labyrinth, while the proximal portions continue to carry the blood to the corresponding horns of the sinus venosus. Later, according to E. G. Butler, the proximal portion of the left vitelline vein disappears and the return of blood is solely through the right vitelline Vein which is now called the posterior vena cava; 2) the umbilical veins which come from the allantois (later incorporated into the umbilical cord), courses along the right and left body walls and enters the sinus Venosus close to the entrance of the vitelline veins; 3) the precardinal veins drain the anterior part of the embryo but at this stage open into the posterior part of the heart. Later the posterior cardinal Veins develop and the proximal part of the precardinals become the right and left common cardinal veins or the ducts of Cuvier.
Embryos less than 5 mm (ﬁg. 5). In this stage the primitive plan of the tubes entering the heart is retained with the one exception of the relationship of the left common cardinal vein. Due to the unequal growth of the atrium and the sinus Venosus the opening of this vein has been shifted toward the center of the atrial region. This shifting of the opening is away from the junction of the left anterior and posterior cardinal veins thereby causing the left common cardinal vein to be longer than the right, even in this early stage. At this early age the shift is not great enough to throw the opening of the left common cardinal vein on the right side, however, this shifting has carried the sinus venosus toward the right side so that its opening into the atrium is located in the mid--dorsal region.
Embyros of 5 to 10 mm. (ﬁgs. 6 and 7). During this period the heart develops very rapidly. The shifting of the sinus venosus to the right side is practically completed. This growth elongates the left duct of Cuvier and carries it downward until it comes to lie across the posterior surface of the heart in the atrio-ventricular groove. The opening of the left duct of Cuvier into the sinus venosus is, in the older specimens of this period, slightly to the right and above the upper extent of the posterior interventricular groove. This duct becomes intimately connected with the heart by the growth of the connective tissue ﬁlling in the atrio-ventricular groove. This connective tissue furnishes a medium into which the cardiac veins arising from the coronary sinus can extend.
The ﬁrst cardiac vein arises in the 9-mm. specimen from the ventricular border of the coronary sinus, slightly to the left of the opening of the sinus into the sinus venosus (ﬁg. 1). This vein arises as an endothelial bud from the inner walls of the coronary sinus and extends through the connective tissue of the atrio-ventricular groove toward the posterior interventricular groove. This, then, is the beginning of the middle cardiac vein. There is in this stage no indication of the origin of the coronary arteries.
Embryos of 12 mm. (ﬁgs. 8 and 9). In the 12-mm. embryo all the main cardiac veins are present. The middle cardiac vein, which in the 9-mm. embryo extended only into the connective tissue of the atrio-ventricular groove, now extends through this connective tissue and is entering the posterior interventricular groove. The small cardiac vein arises to the right of the middle vein immediately distal to the opening of the coronary sinus into the sinus venosus. It extends downward into the connective tissue of the atrio-ventricular groove a very short distance and then swings to the right, remaining within the atrio-ventricular groove. At this age this vein is very short, being hardly more than an endothelial bud from the coronary sinus. The great cardiac vein arises from the left extremity of the coronary sinus and courses to the left, remaining within the connective tissue of the atrio-ventricular groove and is but a little longer than the small cardiac vein of this age (ﬁg. 2). As stated, the cardiac veins arise by endothelial budding from the coronary sinus. At no time has it been noted that the veins arise from the sinus venosus as reported by Grant in the rabbit.
Fig. 1 A section through a portion of the heart of a 9-mm. pig embryo at the level of the opening of the left common cardinal vein into the sinus venosus. This vein has shifted, by growth, into the atrio-ventricular groove thereby placing it lower on the heart than the left horn of the sinus venosus. The middle cardiac vein is budding off from the ventricular side of the left common cardinal vein. X 160.
The bulbus cordis of this stage is incompletely separated into the ascending aorta and the pulmonary artery with the proximal part of the bulbus cordis being still undivided. From this undivided proximal portion, the two coronary arteries arise (ﬁg. 3). Their points of origin are located so that with the subsequent division of this proximal part of the bulbus cordis they take their position on the right and left sides of the ascending aorta, immediately distal to the semilunal valves.
The left coronary artery arises from the left posterior quadrant of the proximal undivided portion of the bulbus cordis and courses downward on the bulbus between it and the ventral horn of the left atrium. Shortly after its origin, it divides into two primary branches. The longer branch is the left interventricular artery which continues downward over the bulbus to enter the upper portion of the anterior interventricular groove. The shorter branch is the left circumﬂex artery which extends a very short distance to the left in the atrio—ventricular groove.
Fig. 2 A section through a portion of the heart of a 12-mm. pig embryo showing the origin of the great cardiac vein from the coronary sinus. X 160.
The right coronary artery arises from the right side of the bulbus cordis between it and the ventral horn of the right atrium and extends only a very short distance down the right side of the bulbus cordis.
The above description of the 12-mm. embryo heart applies to the average of this stage. In some cases the coronary arteries did not appear until in later stages. In one 11-mm. specimen the heart was much farther developed than the length of the embryo would indicate. In this specimen the cardiac-coronary circulation was comparable to the average of the 18-mm. embryo, however, in the average of the 11-mm. embryo there were no coronary arteries present.
Fig. 3 A section of the bulbus cordis of a. 12-mm. pig embryo. This shows the origin of both the right and left coronary arteries. This section is slightly oblique to the bulbus cordi so that the complete lumen is not present. X 160.
Embryo of 15 mm. (ﬁgs. 10 and 11). The advance of the cardiac-coronary system of the 15-mm. stage over that of the 12-mm. stage is purely of elongation of the veins already present. The great cardiac vein extends about one-half the distance from its origin at the left extremity of the coronary sinus, to the left border of the heart and remains Within the atrio-ventricular groove. The middle cardiac vein now extends about one-third of the way to the apex of the heart in the interventricular groove. The small cardiac vein extends about one-third of the distance from the right border of the heart, remaining within the atrio-ventricular groove.
The coronary sinus has shifted downward until it now is placed transversely on the posterior surface of the heart. The distal portion of the left duct of Cuvier is becoming reduced in size. This distal portion remains, in the pig, as the hemiazygos vein, while in the human it completely disappears. The coronary sinus and the umbilical vein (posterior vena cava) still open into the sinus venosus. The right duct of Cuvier (anterior vena cava) opens directly into the right atrium.
The division of the bulbus cordis into the descending aorta and the pulmonary artery is completed in this stage and takes place in such a manner as to cause the coronary arteries to arise from the descending aorta. The only change in the arteries of this stage is that of increased length. The right coronary artery extends about one-half the distance toward the right margin of the heart. The left interventricular branch of the left coronary artery extends about one-half the distance toward the apex. The left circumﬂex branch of the left coronary artery extends about one-half the distance across the top of the left ventricle.
Embryos of 20 mm. (ﬁgs. 12 and 13). The cardiaccoronary system of this stage is much advanced over that of the previous stage. The small branches of both the arterial and venosus channels are developing, and, in this stage, occur as very short twigs.
The great cardiac vein has grown around the left margin. of the heart, extending across the top of theleft ventricle, and has turned down the anterior interventricular groove. It extends down this sulcus to about one-fourth the distance to the apex. The left marginal vein, a branch of the great cardiac vein, is a very short twig on the left margin of the left ventricle. The middle cardiac vein, coursing down the posterior interventricular groove, reaches about one-half the distance to the apex. The small cardiac vein extends around the right margin of the heart and reaches about one—third the distance across the top of the right ventricle.
The left interventricular branch of the left coronary artery reaches three-fourths of the way down the anterior interventricular sulcus. The circumﬂex branch of the left coronary artery continues around the left margin of the heart and extends almost to the root of the great cardiac vein on the posterior surface of the heart. The left marginal artery is a branch of the left circumﬂex and in this stage, is a very short twig on the left margin of the left ventricle. The right coronary artery extends around the right margin of the heart over the top of the right ventricle to the posterior interventricular sulcus where it turns downward in this sulcus as the posterior interventricular artery. It extends about threefourths the distance to the apex on the posterior surface of the heart. The right anterior ventricular artery is, in this stage, a very short branch from the right coronary, arising about midway between the root of the right coronary and the right margin of the heart. The right marginal artery is another branch of the right coronary, somewhat longer than the right anterior ventricular artery, arising near the right margin of the heart and extending downward on the right ventricle.
Embryos of 25 mm. (ﬁgs. 14 and 15). The advance of the cardiac-coronary system of this age is one of extension only. This growth is in size as well as in length, so that the arteries and veins are not only larger than those of the previous stage but they also extend farther along their lines of growth.
The rapid enlargement of the right atrium has practically absorbed the sinus venosus. The right valve of the sinus venosus is changing to form the cristae terminalis, the valves of the posterior vena cava and the valves of the coronary sinus. The coronary sinus now empties directly into the right atrium.
Embryos of 30 mm. (ﬁgs. 16 and 17). The cardiac-coronary system has continued the steady growth of the parts present so that by this stage the system is quite extensive although it is not complete.
The one outstanding feature of this stage is the origin of one of the branches which supplies the septum. In the human this branch is relatively unimportant, however, in the pig it becomes much larger than the other branches to the septum and is of importance enough to warrant description. It arises by budding at the point where the right coronary artery turns downward to continue as the right interventricular artery. This artery branches near its point of origin. The left, smaller branch crosses the interventricular sulcus at the atrial end and extends onto the upper right portion of the posterior wall of the left ventricle. The right, more important branch burrows directly into the heart. In this stage the branches are very short. The artery might appropriately be called the ‘intercardial artery.’ The name septal was discarded because of the possibility of confusing it with the septal artery of the internasal septum.
Embryos of 35 mm. (ﬁgs. 18 and 19). In this stage the vessels are still being extended in length and size by their steady growth. The intercardial artery extends into the septum of the heart at the point where the interatrial septum joins the interventricular septum. The other arteries and veins continue elongating in their respective paths of growth.
Embryos of 45 mm. (ﬁgs. 20 and 21). At this stage the cardiac-coronary circulation is to all purposes completed. A description of this is unnecessary with the exception of the intercardial artery. This artery extends through the septum as previously mentioned and gives off branches downward into the interventricular septum and upward into the interatrial septum. It continues through the septum until it reaches the posterior wall of the basal part of the ascending aorta where it breaks up into smaller vessels and ﬁnally ends in a capillary bed at that place.
Throughout this study there has been observed no evidence of the formation of intercellular spaces in the locations which will be occupied by the cardiac-coronary system after its development. As far as has been observed all the vessels of this system arise by endothelial budding. They ﬁrst appear as sprouts from the pre-existing endothelium of the ascending aorta or the coronary sinus along with that small portion found in the few Thebesian vessels incorporated into the cardiac-coronary system. The endothelial lining of the Thebesian vessels arise from the endothelium of the heart cavities.
It is, of course, realized that the vessels of the cardiaccoronary system belong, in spite of their importance to the individual, to the category of smaller vessels. It is also realized that these vessels arise long after the embryo has a workable circulation. Since these are small vessels which arise relatively late, it should be expected that they would develop by budding rather than by the coalescence of intercellular spaces.
Since the intertrabecular or Thebesian circulation is the primitive one, as shown by the facts of comparative anatomy, it is to be expected that this type would develop in the higher vertebrates prior to the cardiac-coronary system. Such, of course, is the case. In the younger stages studied in this series the vasation of the heart wall is taken care of by wideopen extensions of the internal sinusoidal spaces of the heart. With the increase in age of the embryo the myocardium develops. Concomittant with the myocardial development and because of it these wide-open extensions become reduced in size so that they are slender tubes quite like capillaries. These Thebesian vessels are very numerous (ﬁg. 4). Careful reading of serial sections show that some of these vessels are continuous with the cardiac-coronary system in the stages in which the arteries and veins are developing. In the majority of cases it is equally clear that all Thebesian vessels do not anastomose with the cardiac-coronary system. Indeed, only a small portion of these vessels do join the permanent system. At least a portion of these are incorporated into the permanent system, some few remain as connections between the cardiac-coronary system and the internal cavities of the heart, While the remaining majority become reduced in size and gradually disappear due to the pressure of the developing musculature of the myocardium.
Fig.4 A section through the atrial wall of a 30-mm. pig embryo showing 3. Thebesian vessel extending from the atrial cavity. This specimen had been injected with a color mass previous to ﬁxing. X 160.
- The ﬁrst part of the cardiac-coronary system to appear is the middle cardiac vein which is first seen in the 9-mm. embryo.
- All the main vessels are present as short sprouts in the 12-mm. stage.
- By the time the embryo reaches the 20- to 25-mm. stage the cardiac-coronary system is quite extensive.
- The cardiac-coronary system is, to all purposes, completed in the 45-mm. stage.
- All vessels arise by endothelial budding from pre-existing endothelium.
- The intercardial artery is one of the branches from the right coronary which supplies the septum. This branch warrants description since it is much larger than the other branches supplying the septum and does not end in the septum but continues through the septum to end on the posterior Wall of the basal part of the ascending aorta.
Butler EG. The relative role played by the embryonic veins in the development of the mammalian vena cava posterior. (1927) Amer. J Anat. 39(2): 267-.
GOLDSMITH, J. B. 1927 A new ﬁxative of general value. Trans. Am. Micro. Soc., vol. 48, pp. 216-217. 1936 An injecting apparatus suitable for injecting embryos and organs. Trans. Am. Micro. Soc., vol. 55.
GRANT, R. T. 1926 Development of the cardiac-coronary vessels in the rabbit. Heart, vol. 13, pp. 261-271.
LEWIS, T. F. 1904 The questions cf sinusoids. Anat. Anz., vol. 25, pp. 261-279.
MAn'r1N, G. 1894 Recherches anatomique ct embryologique sur les Arteres coronaires du Cour. Paris.
TANDLER, J. 1908 In ‘Keibel and Elze’ Normentaf. z. Entwickl. d. Menschen. Jena.
WHEELDON, T. F. 1916 The coronary vessels of the 20-mm. pig embryo. Anat. Rec., vol. 11, pp. 430-431.
Figures 5 to 9 inclusive are drawings of models made by the method recommended by Mrs. Gage. The remainder of the drawings were made from injected specimens. The atria of all ages have been lifted slightly to expose the underlying vessels. All measurements refer to the crown-rump length.
The models were made from a series selected from a group of the same developmental stage as being the average for that particular group. The drawings of the injected specimens are composite in nature, being the average of all speci mens of that group studied.
A.A., ascending aorta
A.V.C., anterior vena cava.
C.A., coronary arteries
C.S., coronary sinus
D.A., ductus arteriosus
G.C.V., great cardiac vein
H.V., hemiazygos vein
I.A., intercardial artery
L.A., left atrium
L.O.A., left coronary artery L.C.C. left common cardinal vein L.Ci., left circumﬂex artery L.I., left interventricular artery L.M.A., left marginal artery L.M.V., left marginal vein
L.V., left ventricle
L.V.V., left vitelline vein
M.C.V., middle cardiac vein
P.T., pulmonary twig
P.V., pulmonary vein
P.V.C., posterior vena cava
R.A., right atrium
R.A.V., right anterior ventricular artery R.C.A., right coronary artery R.C.C., right common cardinal vein R.I.A., right interventricular artery R.M.A., right marginal artery
R.V., right ventricle
R-.V.V., right vitelline vein
S.C.V., small cardiac vein
S.V., sinus venosus
T.V., Thebesian vessel
W.L.V., wall of left ventricle
5 A drawing of a model of the heart of a 2.7-mm. pig embryo. This is a view of the dorsal aspect of the heart showing the change in the relative sizes of the two common cardinal veins even at this early stage. The left common cardinal vein is elongated. X 15.
6 A drawing of a model of a heart of a 7-mm. pig embryo. This is a dorsal view and shows the further elongation of the left common cardinal vein. No cardiac veins are present in this age. X 15.
7 A drawing of a model of the heart of a 9-mm. pig embryo. This is a view of the dorsal aspect and shows the origin of the ﬁrst cardiac vein to appear. This is the middle cardiac vein. Note the downward shift of the left common cardinal vein toward the atrio-ventricular groove. X 15.
8 A drawing of a model of the heart of a 12-mm. pig embryo. The left. atrium has been displaced upward exposing the great cardiac vein. This is a dorsal view of the heart and shows the origin of all three of the main cardiac veins. These veins are the great, middle and small cardiac veins. X 15.
9 A drawing of the same model as ﬁgure 8 showing the ventral side of the heart. Both atria have been displaced upward to expose the origin of the coronary arteries. Both coronary arteries are present in this stage. The left is already branched to form the left circumﬂex and the left interventricular arteries. X 15.
10 A dorsal view of an injected heart of a 15—mm. pig embryo showing the increase in length of the three cardiac veins. Note also the further shifting of the left common cardinal vein into the atrio-ventricular sulcus to form the coronary sinus. The distal part of this vein becomes the hemiazygos vein. X 10.
11 A ventral view of a heart the same as ﬁgure 10. This shows the extensions of the coronary arteries. The pulmonary portion of the bulbus cordis has been removed to expose the origin of the arterie. X 10.
12 A dorsal view of the heart of an injected 20-mm. pig embryo. This shows the growth extensions of the arteries to the dorsum of the heart. The right coronary artery has reached the mid-line of the dorsum and turned downward to form the right interventricular artery. The left circumﬂex artery has also extended to the dorsal aspect of the heart and branches are extending downward over the basal portion of the left ventricle. X 10.
13 A ventral view of a heart of the same stage as ﬁgure 12, showing the origin of the right marginal, right anterior ventricular and left marginal arteries. The great cardiac vein ha extended to the ventral aspect of the heart and turned downward in the interventricular groove to form the left interventricular vein. The small cardiac vein ha extended around the right margin of the heart to the dorsal surface. X 10.
14 A dorsal view of an injected heart of a 25 mm pig embryo showing the further extension of the vessels of the basic cardiac—coron:xry pattern. X 10.
15 A ventral View of a heart of the same stage as ﬁgure 14, showing the extensions of the vessels on this side of the heart. X 10.
16 A dorsal view of an injected heart of a 30-mm. pig embryo. This shows the origin of the intercardiac artery from a point where the right coronary artery turns downward to continue as the right interventricular artery. A branch of the intereardiac artery extends to the right side of the basal part of the left ventricle. X 7%.
17 A ventral view of an injected heart of the same stage as ﬁgure 16. Con« tinued growth has carried the left interventricular artery to the apex of the heart. x 7% 18 A dorsal View of an injected heart of a 35-min. pig embryo. This shows growth extensions of all the arteries and veins. X 7%.
19 A ventral View of an injected heart of the same stage as ﬁgure 18, showing the growth extensions on this surface. X 7-}.
20 A dorsal View of an injected heart from a 45-mm. pig embryo showing the adult cardiac-coronary pattern practically completed. X 721;.
21 A ventral view of an injected heart of the same stage as ﬁgure 20, showing the branching of the anterior vessels. X 7%.
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