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Vascular connections between the coronary circulation and the ventricles of the rat heart.

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Vascular Connections Between the Coronary
Circulation and the Ventricles of the R a t Heart
D. A. €3. YOUNG A N D B . F . FELL
Rowett Research Institute, Bucksburn, Aberdeen, Scotland
Thebesian veins are probably remnants
in the adult heart of the sinusoidal blood
supply from the heart chambers by which
the embryonic myocardium is nourished.
Connections are formed in the embryo between the sinusoids and the developing
coronary veins (Grant, ’26; Grant and
Regnier, ’26).
Among the higher vertebrates, Thebesian veins have been demonstrated in various ways by Pratt (1898) in the ox, dog
and cat; by Grant (’26) in the rabbit; by
Grant and Viko (’29-’31) in man, the
dog and sheep; and by Wearn (’28) and
Wearn, Mettier, Klumpp and Zschiesche
(’33-’34) in man. In addition to Thebesian veins, Wearn and his collaborators
identified structures through which the
coronary arteries communicate with the
chambers of the human heart.
The purpose of this paper is to record
the presence of Thebesian veins in the
ventricles of the rat heart. Perfusate was
found to accumulate in the left ventricles
of isolated rat hearts during the course of
perfusion experiments using the method
of Bleehen and Fisher (’54). As the
hearts were not immersed in the perfusate
in these particular experiments and the
aortic valves were competent, this suggested that connections between the coronary system and the ventricles - the
Thebesian veins described in other species - must also be functional in these
circumstances. Perfusate was always present in the right ventricle as the usual exit
for coronary effluent in the perfused heart
is via the right atrium, right ventricle
and pulmonary artery.
The rat heart possess important extracoronary vessels (Halpern, ’53, ’57) and
with this retention of primitive phylogenetic characteristics it might be expected that
the Thebesian veins, representing a primitive cardiac blood supply, would be more
extensive in the rat than in many other
mammals. Foxon (’55) however, has
maintained that the evolutionary development of the vertebrate heart is not one of
progressive vascularization and that the
poor coronary system of the amphibian
heart is an adaptation.
METHODS
The hearts were obtained from male
Hooded Lister rats of 250-300 gm body
weight.
Rats were injected intravenously with
heparin (“Liquemin,” Roche Products,
Ltd.) at the rate of 250 i.u./lOO gm. The
hearts were then removed under ether
anesthesia and the aorta was temporarily
cannulated to wash the heart free of
blood with Krebs ( ’ 3 2 ) bicarbonate-saline
equilibriated with 95% 02/5% CO, at
38°C. The pulmonary artery was then
cannulated and India ink, mixed with
formalin to give a 20% formol solution,
was perfused into it at a pressure of 1015 cm water for 2-5 sec. The hearts were
then dropped into 10% formol saline.
The object of this procedure, which gave
consistent macroscopic results, was to fill
possible Thebesian vessels with ink via the
right ventricle. One heart perfused in this
way was examined histologically.
Two rats were killed under ether anesthesia by the injection into the abdominal
vena cava of 0.5 ml of 0.3 M potassium
chloride solution. The hearts, thus arrested
in diastole, were removed from the animals two hours later and were then fixed
in 10% formol saline. These hearts were
not perfused with ink.
After routine processing the hearts were
embedded in paraffin wax and serial 7 cr
thick sections were cut through the ventricles. As far as possible, all the sections
cut were mounted. The heart marked with
149
150
D. A. B. YOUNG AND B. F. FELL
ink was sectioned from the apex to the
base of the ventricles but in the other
hearts only the basal third of the ventricles was sectioned. The sections were
stained by hematoxylin and eosin. Approximately 1,000 sections were examined.
A Thebesian vein was presumed to exist
when it could be shown by continuity of
endothelium that an opening in the endocardium was in direct communication with
a blood vessel in the myocardium.
RESULTS
Macroscopically, the vasculature of the
isolated heart appeared to be completely
filled by injecting India ink via the pulmonary artery. With reduction in pressure and time of perfusion, incomplete
filling of the vasculature was obtained in
a series of 18 hearts. Such hearts showed
ink in the interventricular septum and
apex and flling of the veins draining this
area only.
Microscopically, numerous Thebesian
veins were present in each of the three
hearts in the right ventricles and less frequently in the left. The openings were
found at three main sites (fig. 1 ) . These
were in the right ventricle on the face of
the interventricular septum and at the
intersection of the wall of the right ventricle and the interventricular septum.
The distribution in the left ventricle
was irregular but the vessels were most
R. V,
common at the junction of papillary muscles and ventricular wall.
The connections were of four main
types.
1. Vessels of capillary size or small
venules opened into recesses on the right
ventricular face of the interventricular
septum; often several small vessels opened
into one recess (fig. 2 ) .
2. At the junction of interventricular
septum and right ventricular wall deep
sinuses occurred. Small Thebesian veins
discharged into these sinuses which in
addition were commonly in connection
with large veins deeper in the myocardium
(figs. 3 , 4). At this site relatively large
veins were found also to discharge directly
into the ventricle (figs. 5-7).
3 . In the left ventricle at the base of
the papillary muscles, the Thebesian openings consisted of small sinuses into which
discharged numerous capillaries (fig. 8).
4. In the wall of the left ventricle a
more specialized type of structure was also
present. This was seen only in the rats
killed by potassium chloride injection and
it may be that here the state of myocardial
contraction or vascular Wing was particularly favorable for the demonstration
of Thebesian vessels.
This type consisted of anastomosing
veins which opened into the chamber of
the heart and which received numerous
tributaries throughout their length, thus
V.
Fig. 1 Diagram of rat heart in cross-section through the ventricles. The main sites of
Thebesian vessels are indicated by crosses. LV, Left Ventricle, RV, Right Ventricle,
S, Sinusoids.
THEBESIAN VEINS IN THE RAT HEART
draining a considerable volume of muscle
(fig. 9). Myocardial fibers were disposed
longitudinally along and between the main
veins. The curving vessel which enters
near the mouth of the main duct in figure 9 is thin-walled and was shown by
serial sections to be a looping branch between two veins, entering at either end as
a “T” junction.
In the other examples of similar venous
plexuses there was no main collecting
vein but the plexus communicated with
the chamber of the ventricle by several
small orifices.
In the marked heart there was widespread filling of the coronary veins with
India ink. Occasionally, small quantities
of ink appeared in the coronary arteries
close to the base of the heart.
151
the ventricular cavities, but when the
coronary arteries are partially occluded
such a transfer is theoretically possible
(Wiggers, ’36). Local pressure gradients
may occur, however, for Bohning, Jochim
and Katz (’33), using a modified heartlung preparation, found that particulate
matter could pass from the chambers of
the dog’s heart to the coronary venous
sinus.
SUMMARY
The blood vessels of the isolated, beating rat heart can be filled with India ink
by perfusion of the right ventricle. When
the duration and pressure of perfusion are
suitably reduced it is possible to restrict
the perfusion of the vasculature to the
interventricular septum and the veins
draining this area. Microscopic examination of stained serial sections of the
DISCUSSION
ventricles of one such heart, and also of
The Thebesian veins demonstrated in unperfused specimens, showed that Thebethe ventricles of the rat heart by this work sian veins were present in both left and
are similar to those described in other right ventricles. They were most numermammalian species. The existence of ous in the latter. The most common site
connections between the coronary arteries was the wall of the interventricular sepand the chambers of the heart is less cer- tum, where Thebesian veins communitain. Wearn (’28) and Wearn et al. (’33- cated with the chamber of the right ven’34) show that in man such connections tricle by capillaries and venules which
exist in the form of relatively large ves- discharged into recesses in the ventricular
sels which they classify as “arterio-lum- wall or into sinuses situated at the juncinal” and “arterio-sinusoidal,” whereas tion of the right ventricular wall and inother investigators believe that such con- terventricular septum. In addition to these
nections are limited to vessels of capillary communications, a small number of large
size (Pratt, 1898; Grant and Viko, ’29-’31; Thebesian veins discharged directly into
the ventricle. In the left ventricle the
Stella, ’31).
We have failed to find direct connections Thebesian veins were concentrated at the
between arteries and the chambers of the bases of the papillary muscles. Usually
ventricles in these few rats. Examples these were capillaries, several of which
were found of Thebesian veins originating communicated with the lumen of the venin a vascular network composed of vessels tricle by means of a common sinus-like
slightly larger than capillaries. The or- opening, but anastomosing veins were also
ganization of these vessels suggests a pres- present. No connections were found between arterial vessels and the chambers of
sure-buffering or valvular mechanism.
the
left or right ventricles.
The functional significance of Thebesian connections in the normal or diseased
ACKNOWLEDGMENT
heart is uncertain (Gregg, ’46), but it has
been frequently suggested that Thebesian
We thank Miss K. A. Smith for techveins have a nutritive function in that nical assistance.
through them blood can pass from the venLITERATURE CITED
tricles into the capillary bed. This view
is not supported by studies on the dynamic Bleehen, N. M., a n d R. B. Fisher 1954 The
pressure gradients found in the normal
action of insulin in the isolated rat heart. J.
Physiol., 123: 260-276.
heart between the coronary arteries and
152
D. A. B. YOUNG AND B. F. FELL
Bohning, Anne, K. Jochim and L. N. Katz
1933 The Thebesian vessels as a source of
nourishment for the myocardium. Am. J.
Physiol., 106: 183-200.
Foxon, G. E. H. 1955 Problems of the double
circulation in vertebrates. Biol. Rev., 30: 196228.
Grant, R. T. 1926 Development of the cardiac
coronary vessels in the rabbit. Heart, 13: 261271.
Grant, R. T., and M. Regnier 1926 The comparative anatomy of the cardiac coronary veins.
Heart, 13: 285-310.
Grant, R. T., and L. E. Viko 1929-31 Observations on the anatomy of the Thebesian vessels
of the heart. Heart, 15: 103-123.
Gregg, D. E. 1946 The coronary circulation.
Physiol. Rev., 26: 2 8 4 6 .
Halpern, M. H. 1953 Extra-coronary cardiac
veins in the rat. Am. J. Anat., 92: 307-327.
1957 The dual blood supply of the
rat heart. Am. J. Anat., 101: 1-16.
Krebs, H. A., and K. Henseleit 1932 Untersuchungen uber die Harnstoffbildung im Tierkorper. Hoppe-Seyl Z., 21 0: 33-66.
Pratt, F. H. 1898 The nutrition of the heart
through the vessels of Thebesius and the coronary veins. Am. J. Physiol., 1: 86-103.
Stella, G. 1931 The part played by the Thebesian vessels in the blood supply to the heart.
J. Physiol., 73: 3 6 4 4 .
Wearn, J. T. 1928 The role of the Thebesian
vessels in the circulation of the heart. J. Exp.
Med., 47: 293-316.
Wearn, J. T., S. R. Mettier, T. G. Klumpp and
Louise J. Zschiesche 1933-34 The nature of
the vascular communication between the coronary arteries and the chambers of the heart.
Amer. Heart J., 9: 143-164.
Wiggers, C . J. 1936 The physiology of the
coronary circulation. In: Diseases of the
coronary arteries and cardiac pain. R. L. Levy.
New York. pp. 89-95.
PLATE 1
E X P L A N A T I O N OF FIGURES
2
Thebesian veins containing India ink, opening onto the right
ventricular face of the interventricular septum of a perfused
heart. Hematoxylin and eosin. X 150.
3 and 4
Two of a set of serial sections of a heart perfused with ink to
show a large Thebesian connection with a sinus-like opening of
the right ventricle. H.
E. X 150.
5-7
Serial sections of a heart perfused with ink to show a large
Thebesian vein communicating with the right ventricle. H. + E.
x 150.
8
Thebesian capillaries opening into the left ventricle of a n unperfused heart. H.
E. X 150.
9
Anastomosing Thebesian vessels in the wall of the left ventricle
of an unperfused heart. H.
E. x 150.
+
+
+
THEBESIAN VEINS I N THE RAT HEART
D. A. B. Young and B . F. Fell
PLATE 1
153
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