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Experimental revascularization of the entire heart
Experimental Evaluation
of epicardiectomy,
of the internal necrosis
revascularization
and
mammary death
of the entire
omental artery
graft,
and/or
in preventing
heart
implantation
myocardial
of the animal
Arthur M. Vineberg, M.D.* Yzrtaka Kato, M.D. W. J. Pirozynski, M.D. Montreal, Canada
mhe value of surgical techniques for 1 the relief of coronary artery insufficiency has been greatly doubted. This has been partly because clinical evaluation of revascularization procedures is difficult, due to the unpredictable character of the disease, and partly because basic experimental methods of evaluation of an operative procedure have been lacking. Many studies in our laboratory have made it quite clear that evaluation of a revascularization procedure by flow, backflow, ventricular fibrillation threshold, radioactive tracings, and many other such methods left a great deal to be desired and for the most part could not be relied upon. For this reason, over the years we have attempted to reproduce coronary artery occlusion by constricting the main stems at the locations at which obstructive diseaseoccurs in human patients.1-g Experiments have been carried out until a 100 per cent lethal test has been developed as a result of slow occlusion of the main stems of all three coronary arteries by Ameroid constrictors.‘“-‘” From
Besides survival of the animal from triple coronary artery occlusion, the degree of myocardial necrosis in both ventricles has been used as objective evidence of the value of a revascularization procedure. In addition, intra-arterial injection studies using Schlesinger mass13have been carried out in order to outline the extracardiac coronary pathways which may or may not develop, and which, when present, might explain any benefit that occurred as a result of a given revascularization procedure. Experimental
the Sub-Department of Cardiac Surgery, Royal Victoria and Pathology, McGill University, Montreal. Canada. Received for publication. Oct. 22, 1965. *Address: Sub-Department of Cardiac Surgery. Royal Victoria
79
study
Various methods of revascularization were tested against the 100 per cent coronary artery Ameroid occlusion test. A. Control group. In the control series of 20 animals there were 20 deaths; the spontaneous mortality was 100 per cent. The average survival time a-as 18.8 days; this was used as a base line to estimate the survival time. Survival time, therefore, becomes one of the criteria for the evaluation of various surgical procedures deHospital,
Hospital.
and the
Montreal
Departments
2, Quebec.
of Experimental
Canada.
Surgery
80
L’ineberg, Kuto, and Pirozynski
signed to relieve myocardial ischemia caused by triple coronary artery constriction. B. Treated groups. In all animals the Ameroid coronary artery constrictors were applied at the time of one of the following operative procedures: 1. EPICARDIECTOMY-10 ANIMALS. The epicardium was removed from the anterolateral and posterior surfaces of both ventricles, using specially designed epicardial scrapers which remove both layers of the epicardium without injury to the coronary vessels. 2. EPICARDIECTOMY CARDIECIOMY-10
AND ANIMALS.
SEROIIS
PERI-
The epicardium and serous layer of the pericardium were removed and the pericardium was closed. 3. EPICARDIECTOMY WITH INTERNAL MAMMARY
ARTERY
IMPLANTATION
(VINEBERG)-
10 ANIMALS. The left internal mammary artery was implanted into the anterior wall of the left ventricle. The epicardium was removed from the remainder of the left ventricle. The pericardium was left open. 4. FREE OMENTAL GRAFT OPERATION (VINEBERG)-10 ANIMALS. The entire heart was wrapped around by a graft of the greater omentum, which was completely detached from its abdominal pedicle, and the diaphragm was closed. The omentum was not sutured to the heart but to the ascending aorta. Epicardiectomy and serous pericardiectomy were not performed. The pericardium was closed over the omental graft. 5. FREE OMENTAL GRAFT OPERATION PLLS EPICARDIECTOMY AND SERO-PERICARDIECTOMY (~INEBERG)--20 ANIMALS. Extensive
epicard.iectomy of all surfaces of both ventricles was performed ; the serous layer of the pericardium was removed, as was the reflection of the pericardium over the base of the aorta. The greater omentum, after its detachment from the transverse colon, was xsrapped around the heart. It was fixed by multiple sutures to the ascending aorta and the heart. The pericardium was closed. 6. FREE OMENTAL GRAFT PLL:S EPICARDIECTOMY INTERNAL opERATION
AND
SERO-PERICARDIECTOMY
MAMMARY ARTERY (VINEBERG)-
IMPL4NTATION ANIMALS.
WITH
The
same technique as described under 2, 3, and 5 was followed. The left internal mammary artery was implanted into the anterior wall of the left ventricle. The pericardium was resected anteriorly to prevent encroachment upon the internal mammary artery implant. The omental graft was sutured to the free edges of the pericardium and to the anterior surface of the heart to avoid contact with the internal mammary artery. Postmortem
studies
All animals underwent the following investigations. A. Injection studies. The chest was opened through the fourth intercostal space; adhesions to the surface of the heart were not disturbed. The aorta was ligated above the diaphragm and at its junction with the left ventricle. Care was taken not to damage anastomotic vessels between the aorta and the omental graft. The thoracic aorta was cannulated proximal to the lower ligature. New Schlesinger mass, which does not pass through vessels that are less than 40 microns in diameter, was injected at pressures that ranged between 100 and 120 mm. of mercury, filling the aorta and its branches above the diaphragm with dye. ReAux of injection mass into the left ventricmar cavity and coronary arteries was prevented by the ligature at the aortoventricular junction. Thus, radiopaque substances appearing in the coronary arteries could only have entered them by traversing extracardiaccoronary anastomoses via the subpleural, mediastinal, and pericardial vessels. X-ray films of the heart in situ before and after injection outlined the extracardiac-coronary anastomoses when present. In the group of animals which had undergone the combined free omental graft and internal mammary artery implantation operation the internal mammary artery was ligated at the second intercostal space and cannulated distal to the ligature. The radiopaque mass injected into the thoracic aorta filled mediastinal vessels and outlined omental-coronary anastomoses as well as omental and/or mammary-coronary anastomoses. After injection and x-ray examination in situ, the internal
mammary artery was injected under q-stemic pressure and the heart was x-rayed again in situ. After removal of the heart, the ascending aorta was reinjected with Schlesinger mass so as to fill vessels leaving the root of the aorta to anastomose with those in the omental graft. The ligature around the base of the aorta \vas not removed. When the original aortic injection did not fill the entire coronary arterial tree, then both coronary ostia were cannulated with metal cannulae and injected with Schlesinger mass. Separate x-ray films were taken after injection of each coronary artery. After the injection mass had solidified, the heart was unrolled in order to study homocoronary and intercoronary anastomoses, as well as arterial channels which were formed to bypass the areas of Ameroid obstruction of the coronary’ arteries. Multiple x-ray pictures taken between the injections of radiopaque Schlesinger mass have made it possible to outline numerous arteriolar and larger vessels and to study anastomoses formed between: (a) the aorta and free omental graft, (b) the graft, coronary arteries, and myocardium, (c) mediastinal vessels, pericardium, graft, and coronary myocardial vessels, an d (d) internal mammary artery, myocardial *arterioles, and coronary arterioles. Injection studies are not so definitive as survival of animals and ventricular muscle mass. However, newly developed extracardiac channels through lvhich oxygenated blood can bypass the proximal points of coronary artery occlusion may be outlined. In this study, the injection mass was first introduced into the thoracic aorta in order to outline extracardiac coronary anastomoses. The filling of the coronary- arterial tree through the aorta via mediastinal vessels may prevent satisfactory visualization of homocoronary and intercoronary anastomoses by later individual coronary artery injections. This occurs because the injection mass hardens before there is time to remove the heart and inject the coronary arteries. Thus, the first injection should outline the important channels immediately. In this series, our attention has been focused upon the extracardiac channels reaching the heart from
the mediastinal vessels. The demonstration of homocoronary and intercoronary arteries, although desirable, was regarded to be of secondary importance. In most instances these have also been outlined satisfactorilyF. R. Pathologic studies. Each heart was examined grossly and microscopically for presence or absence and extent of ischemic myocardial damage. Jlultiple sections were taken from the right and left ventricles and the intraventricular septum. The portions of each artery included in the Ameroid constrictors were investigated microscopically to determine the extent of narrowing of the lumina of the right, anterior descending, and circumflex coronary arteries. This has been recorded as the percentage occlusion of the original cross-sectional area of the lumen. It has been expressed as an average occlusion for all three coronary arteries. The patency of the implanted internal mammary artery was determined over its entire length, including the myocardial tunnel. Results
In this study we have attempted to establish simp!e criteria for estimating the value of a revascularization procedure. The four most important criteria of value are: (1) survival time of animals; (2) extent of damage to the myocardium after triple coronary artery Ameroid constriction; (3) formation of extracardiac coronary anastomotic channels; and (4) formation of a new surface cardiac distribution system (omental graft) connecting together right and left coronary systems and arteriolar zones. 1. Survival of animals. The survival times of both the control series and the treated seriesare shown in Table I. CONTROL GKOIJP. In the control series the spontaneous mortality was 100 per cent. TKE~~TEDGKOI:PS.
1. In the series of 10 animals with epirardiectomp there was one death, i.e., 90 per cent spontaneous mortality. The average survival was 16 days; there was one long-term survivor, sacrificed 266 days postoperatively. 2. In the second series of 10 animals in which the epicardium and serous layer of
Am. Heart f.
Vineberg, Kato, and Pirozynski
82
Idy,
Table I. Survival time after trifile coronary artery
1966
Ameroid constriction (control and treated) I Died
Number
___-
of
Sarrifced
I --__-
---
!
I
animals
in series
Number Of animals
Average number Of I, days
Range in days I~
spontaneous mortality (%I
235-160 I days (%i
Arwage number I, of postop. days
Control
20
20
19
(9-29)
100
Treated 1. Epica rdiectomy
10
9
16
(7-28)
90
l-10
266
10
8
30
(21-40)
80
2-20
245
10
6
26
(15-39)
60
4-40
75
10
6
20
(9-30)
60
4-40
235
20
5
26
(17-37)
25
15-75
322
32
(19-50)
21
11-79
294
2. Epicardiectomy pericardiectomy
and sero-
3. Epicardiectomy mammary artery
and internal implant
4. Free
omental
5. Epicardiectomy, cardiectomy graft
graft sero-periand free omental
6. Epicardiectomy, seri-pericard lectomy, free omental graft, and internal mammary artery implant
14
Total Average
degree
of coronary
3
37
94 artery
occlusion:
Died
spontaneously:
the pericardium were removed, there were 8 deaths, a spontaneous mortality of 80 per cent. Survival time averaged 30 days. Two long-term survivors were sacrificed after 245 days postoperatively. 3. In lthe third group of 10 animals with epicardiectomy and internal mammary artery implantation there were 6 deaths; the spontaneous mortality was 60 per cent. The average length of survival was 24 days. There were 4 (40 per cent) longterm survivors, studied approximately 75 days postoperatively. 4. In the fourth series of 10 animals in which the free omental graft was wrapped around the heart there were 6 deaths, a spontaneous mortality of 60 per cent. The average length of survival was 20 days. There were 4 long-term survivors (40 per cent), studied on an average of 235 days postoperatively.
71.3 to 76.2 per cent. Sacrificed:
82.3 to 86.2 per cent.
5. In the fifth series of 20 animals in which the epicardiectomy, sero-pericardiectomy, and free omental graft operations were performed there were 5 deaths, a spontaneous mortality of 25 per cent. The average survival was 26 days. There were 15 long-term survivors (75 per cent); these were sacrificed and studied on an average of 322 days postoperatively. 6. In the final series of 14 animals which underwent epicardiectomy, sero-pericardiectomy, free omental graft application, and internal mammary artery implantation there were 3 deaths, a spontaneous mortality of 21 per cent. The average survival was 32 days. There were 11 long-term survivors (79 per cent); these were sacrificed for study on an average of 294 days postoperatively. 2. Pathologic studies. The pathologic findings of the control animals and those
Experimental
Table II. Tabulation of myocardial nary artery constriction
revascularization
damage in ex$erimental
of entire heart
animals after triple Ameroid
A nimals
20
20
Treated 1. Epicardiectomy
10
9
1
1
10
8
2
2
3. Epicardiectomy and internal mammary artery implant
10
6
1
1
4. Free
10
6
4
3
20
15
10
14
11
4
omental
5. Epicardiectomy, pericardiectomy, free omental
coro-
sacrificed
Control
2. Epicardiectomy sero-pericardiectomy
83
and
graft seroand graft
6. Epicardiectomy, seropericardiectomy, free omental graft, and internal mammary artery implant
which have been subjected to various surgical procedures are summarized in Tables II and III. A differentiation has been made between those animals which died from myocardial ischemia and those which were sacrificed many months after surgery. For those animals which died spontaneously the average degree of coronary artery occlusion ranged from 71.3 to 76.2 per cent in all groups. In those animals which were sacrificed up to 469 days after surgery there appeared to be an increase in the degree of coronary artery occlusion as time went on, and the average degree of cross-sectional occlusion of the total coronary artery inflow tract ranged from 82.3 to 86.2 per cent for the survivors in all six treated groups (Fig. 1). The extent of myocardial damage was graded as follows: No myocardial changes, 0. Focal infarcts (not grossly visible), f.
Moderate or large infarcts-(grossly noticeable-confined to one surface), ++. Massive-transmural infarcts (gross and microscopic), +++. The animals were grouped according to the operative procedure and to the mode of death (i.e., spontaneous or sacrificed). In the control group, 95 per cent of all animals showed massive to moderate myocardial damage in one or both ventricles at the time of spontaneous death. Epicardiectomy alone appears to have little beneficial effect on the prevention of massive myocardial infarction in either right or left ventricles in those animals which died spontaneously. In the second group, in which epicardiectomy was combined with serous pericardiectomy, no massive infarction was present in the animals. In the third group the implanted internal
Vineberg, Knto, nnd Pirozynski
t
+
+f + ++ + ++ + + z ++ +
I
t
+
+
+
+t+
t t
+
+
t
4
+ t
Experimentd
fevusclllarizlrtion
qf entire hectrt
85
Fig. 1. Photomicrograph of sections taken from the sites of Ameroid placement on coronary arteries in Animal No. 1.57, which was sacrificed 169 days postoperatively. .l, Photomicrograph section through the right coronary artery within the Ameroid; the degree of obstruction was 94.1 per cent. B, Photomicrograph of section taken through the anterior descending branch within the Ameroid; the degree of obstruction was 78.5 per cent. C, Photomirrograph of section taken through the circumflex coronary artery at the site of Ameroid constriction, showing 90.2 per cent occlusion of the lumen. The average degree of cross-sectional occlusion of the total coronary artery inflow tract in those animals that were sacriticed ranged from 82.3 to 86.2 per cent.
mammary artery combined with epicardiectomy prevented massive myocardial infarction in all animals. The simple omental graft without pedicle operation protected 40 per cent of the animals from massive myocardial infarction. When epicardiectomy, sero-pericardiectomy, and omental graft were performed, 5 (2.5 per cent) had no infarction and 10
(50 per cent) had scattered foci of fibrosis; none of the 75 per cent survivors had moderate to massive infarction. In the last series, in which epicardiectomy, sero-pericardiectomy, omental graft, and internal mammary artery implant \vere performed, 11 of 14 animals survived; 7 of these (50 per cent) showed no myocardial infarction in either ventricle, and 4 (36 per cent) showed only scattered
86
Am. Heart
Vineberg, Kate, and Pirozynski
high survival rate, as shown in Table I, but also a high survival rate of the ventricular muscle masses of both ventricles, as shown in Table III. Injection studies. The close correlation between animal survival after triple coronary artery occlusion and the development of extracardiac coronary anastomoses may be seen in the tabulation of coronary artery anastomoses shown in Table IV. In this table the various anastomoses which developed are shown for those animals which died spontaneously, and for those which were sacrificed for study. Anastomoses have been graded as follows: No anastomoses, 0. Slight anastomoses, +. Moderate anastomoses, ++. Extensive anastomoses, +++.
foci of fibrosis. None of the 11 surviving animals showed any evidence of moderately severe or massive myocardial infarction. All implants were patent. The average internal mammary artery patency for surviving animals was 71.8 per cent. In Table II, we have attempted to summarize our pathologic studies after triple coronary artery occlusion in all seven animal series. There is clearly a great difference in right and left ventricular muscle mass damage between the control and the treated animal in the last two groups. The last two operations, namely, epicardiectomy, sero-pericardiectomy and the free omental graft alone or combined with internal mammary artery implantation operation, were the only two procedures after which the animals had not only a
EXTRACARDIAC
Ci)RONARY
Table IV. Tabulation of coronary, extracardiac, and mammary coronary ar,lery occlz~sion and revascularization surgery Animals
coronary
dying spontaneously
Animals
Extracardiac mediastieal
in series
animals Of
+++I
++
Control
20
20
0
0
0
4
0
5
Treated 1. Epicardiectomy
10
9
0
0
0
2
2
7
1
0
10
80003442002020
3. Epicardiectomy and internal mammary artery implant
10
6
0
0 2.1112
0
1
1
5
4
4. Free omtrntal graft
10
6
1
0
0
0
0
0
5. Epicardiectomy, sero-pericardiectomy, and free omental graft
20
5
0
1
II
1
2
6. Epicardiectomy, sero-pericardiectomy, free omental graft, and internal mammary artery implant
14
3
0
1
0
0
0
Intercoronary
Homocoronary
Number
mammary
saerijced
Extracardiac
Intercoro-
Homo-
I I ~+++,++~~~~~~~~++~~~+~~~
-
-
-~
0
1
0
1
0
-
-
-
0 2.IM
0 ?.IM
3
1
4
0
4
2
2
3
1
4
0
3
15
4
11
5
9
11
4
3
11
7
4
5
6
9
2
KIM
3.IM
and sero-
1.m
Internal
after triple
_____ Number
IM:
ANASTUMOSES.
anastomoses
Number Of animals
2. Epicardiwtomy pericardhctomy
J.
July, 1966
coronary
anastomoses. +++:
Extensive
plus plus anastomoses. ++:
Moderate
anastomoss.
Experimental
Of the total of 94 animals (20 controls and 74 treated), 57 animals died spontaneously, all within an average of 24 days; 54 showed I10 extracardiac anastomoses (Fig. 2). TE lirty-seven of the 74 treated animals SUI rvived and were sacrificed for study;
Fig Am the dev
revascdarization
of entire heart
13 of these showed extensive, moderate, extracardiac coronary moses, not including mammary anastomoses. In Series 4, in which the free graft \vas simply xvrapped around
87
and 17 ana stocoron lary omenntal the hleart
. 2. Roentgenogram of the heart of Animal No. 208, which died after triple coronary artery occlusion 1by eroid constriction. The animal was studied 19 days after surgery. The only injection made was that thro wh thoracic aorta. In this animal, as in 54 of 57 animals which died spontaneously, there was no evidence of the elopment of extracardiac coronary anastomoses.
88
T’iueberg, Knto, rind Pirozyrtski
and the pericardium cIosed, it was possible to fill the coronary arteries with injection mass through the aorta via the graft (Fig. 3). In Series 5, in vf;hich only epicardiectomy and free omental graft were performed, 1.5 of 20 animals survived and 15 had moder-
ate to extensive extracardiac coronary anastomoses (Fig. 4). The anastomoses referred to are those that form between the mediastinal vessels, pericardium, omentum, and coronary arterioles. These are quite apart from the
Fig. 3. lioentgenogram of the heart of Animal So. 131, which died from a massive myocardial infarction in the right ventricle 2.5 days after placement of triple coronary artery Ameroids and a free omental graft. The onlv injection made was that through the thoraric aorta. The extracardiac radiopaque injection showed the development of omental-mammary-coronary anastomoses bringing the dye into the left coronary arterial system,
Experimenfnl
anastomoses formed between the implanted internal mammary artery and the myocardial arterioles (Fig. 5). The latter are listed as separate anastomoses in Table IV; thus, in the two implant series there are anastomoses not only from the
revmculnrization
89
of entire heart
supplementary operative procedures but from the internal mammary artery itself. INTERNAL WITH
MAMMARY
SUPPLEMENTARY
ARTERY OPERATIONS.
3, in which the internal mammary was combined with epicardiectomy,
IMPLANT In
Sel-ies
artery there
Fig. 4. Roentgenogram of the heart of Animal No. 482, which survived triple coronary artery Ameroid occlusion, epicardiectomy, and free omental graft operation. The animal was sacrificed and studied 469 days after surgery. The only injection made was that through the thoracic aorta. In this animal the injection mass filled the coronary arterial tree via the mediastinal-omental, omental-coronary, and omental-myocardial anastomoses.
90
Vineberg, Knto, and Pirozynski
Am. Hart
I.
.lzcly, 1966
Fig. 5. Roentgenogram of the heart of Animal Ko. 949, which had survived triple coronary artery occlusior 1 by Ame roids, internal mammary artery implantation, and free omental graft. The animal was studied 12 mot lths after surgery. The only injection made was that through the thoracic aorta. In this animal the injection n nass not cmly filled the coronary arterial tree via the mediastinal, omental, coronary, and myocardial vessels but filled the internal mammary artery in retrograde manner, as well.
Volw?Le
73
Nwnbsr
1
Experimentul
were 6 patent mammary-coronary anastomoses. Two of these animals died; in these, extensive intercoronary anastomoses had failed to form. In the 4 animals which survived there were extensive and moderate intercoronary anastomoses. When the omental graft was added to the internal mammary artery, 12 of 14 internal mammary arteries were patent; 11 of the animals survived, and these showed moderate to extensive mammary-coronary anastomoses. The internal mammary artery mammary-coronary anastomoses were in addition to moderate and extensive extracardiac mediastinal coronary anastomoses which had been formed as a result of the free omental graft. INTERCORONARY ANASTOMOSES. In none of the animals which died spontaneously, either the control or the treated groups, was there a single one which showed extensive intercoronary anastomoses (Fig. 6). On the right-hand side of Table IV, the findings in the animals which were sacrificed for study are recorded. Of the 37 animals which survived and were
Fig.
6. Roentgenogram of the
striction. The hear ‘t was unrolled
right coronary and x-rayed.
heart
revasculnrization
of entire heart
91
sacrificed for study, there were 19 which showed extensive, and 17 that showed moderate, intercoronary anastomoses (Fig. 7). Discussion
and
conclusion
The triple coronary artery Ameroid constriction test offers a reliable method of assaying a revascularization procedure. This simple test causes 100 per cent mortality in animals. There was massive myocardial damage in 17 of the control animals. A study of extracardiac coronary anastomoses and intercoronary anastomoses showed that nature failed to develop extracardiac coronary anastomoses. Likewise, nature failed to develop extensive intercoronary anastomoses. The most that nature was capable of doing in response to occlusion of all three coronary arteries was to develop moderate intercoronary anastomoses. Epicardiectomy and free omental graft proved to be effective in preventing death of the animal (75 per cent survival). It was likewise effective in protecting the
of Animal No. 124, which died 17 days after triple coronary artery Ameroid and then the left coronary artery were injected with Schlesinger mass. The Note the almost complete absence of intercoronary anastomoses.
92
Vj’neberg, Kate, and Pirozynski
Fig. 7. Koentgenogram of unrolled injected heart of Animal Ko. 1,000. ‘This animal underwent epicardiectomy of both ventricles and serous pericardiectomy at the same time as Ameroids were placed on the main stems of all three major coronary arteries. This animal was sacrificed 253 days after surgery. There were no extracardiac anastomoses, but there were very extensive intercoronarq. anastomoses and homocoronary anastomoses, which are shown in the injected unrolled heart. This is to be compared with the animal which died after triple coronary artery occlusion without any revascularization procedure (bee Fig. 6).
ventricular myocardium against moderate and/or massive myocardial infarction in 75 per cent of the animals. However, only 2.5 per cent of the survivors were completely free of any myocardial damage. The other 50 per cent showed focal or microscopic damage. Of the various operative procedures tested, the internal mammary artery implant combined with epicardiectomy and free omental graft proved to be best in preventing the death of the animals (79 per cent survival) and myocardial damage. In a series of 14 animals, only one showed massive myocardial infarction. Of the 11 surviving animals, 7 (50 per cent) showed no microscopic evidence of infarction, and 4 showed only scattered areas of microscopic fibrosis. The internal mammary artery implant operation combined with the free omental graft ‘was so effective in animals that it has been applied in the treatment of human coronary artery insufficiency, particularly in patients shown by tine coronary ar-
teriography to have triple coronary artery disease. At the time of the writing of this article, 78 patients have been operated upon since December, 1962. The results have been most gratifying. Summary
The Vineberg internal mammary artery implant operation combined with epicardiectomy and the Vineberg free omental graft operation is a revascularization procedure which develops new extracardiac omental, omental-coronary, mammary-coronary, and intercoronary anastomoses capable of replacing all three coronary arteries so as to maintain the health of the animal and the ventricular myocardium relatively free of damage. There would appear to be a direct relationship between the development of extracardiac omental-coronary, mammarycoronary, and inter-coronary anastomoses and the prevention of myocardial damage in the presence of triple coronary artery occlusion.
Experimental
REFERENCES 1. Vineberg, A. M., and Niloff, P. H.: The value of surgical treatment of coronary artery occlusion by implantation of the internal mammary artery into the ventricular myocardium, Surg., Gynec. & Obst. 91:551, 19.50. 2. Vineberg, A. M., and Miller, D.: Functional evaluation of an internal mammary coronary artery anastomosis, AM. HEART J. 45:873, 1953. 3. Vineberg, A. M., and Buller, W.: Technical factors which favour mammary-coronary anastomosis, J. Thoracic Surg. 30:411, 19.55. 4. Litvak, J.: Experimental production of gradual vascular occlusions. Thesis submitted in partial fulfillment of requirements for the M.Sc. degree, McGill University, Department of Neurology & Neurosurgery, Montreal Neurological Institute, 1957. 5. Litvak, J., Siderides, L. E., and Vineberg, A.: Experimental production of coronary artery insufficiency and occlusion, AX HEART J. 53:505, 1957. 6. Litvak, J., and Vineberg, A.: Experimental gradual arterial occlusion with in vitro and in vivo observations, Surgery 46:954, 19.59. 7. Vineberg, A., and Mahanti, B. C.: Evaluation of experimental myocardial revascularization operations by Ameroid coronary artery constriction, Surgery 47:748, 1960. 8. Duchesne, E. R., and Vineberg, A.: An experimental study of the effect of mechanically
9.
10.
11.
12.
13.
14.
revascularization
of entire heart
93
induced ischemia upon the mammary coronary anastomoses, Surgery 43:837, 1958. Vineberg, A., Mahanti, B. C., and I.itvak, J.: E xperimental gradual coronary artery conSurger) striction by Ameroid constrictors, 47:765, 1960. Vineberg, A.: Experimental background of myocardial revascularization by internal mammary artery implantation and supplementary technics, with its clinical application in 125 patients, Ann. Surg. 159:185, 1964. Vineberg, A.: Results of 14 years experience in the surgical treatment of human coronar) artery insufficiency, Canad. M. A. J. 92:325, 1965. Kato, Y.: Development of the triple Ameroid coronary arterial occlusion test---A 100% lethal test: Value of epicardiectomy, omental graft and/or internal mammary artery implant operation in preventing death of the animal and myocardium, Ph.D. Thesis, McGill IJniversity, May, 1965. Schlesinger, M. J., and Zoll, P. IM.: Incidence and localization of coronary artery occlusions, Arch. Path. (Chicano) 32:178. 1941. Vineberg, A:, Shanks, J., Piiarrt!, Ii., Criollos, R., Kato, Y., and Baichwal, K. S.: Myocardial revascularization by omental graft without pedicle: Experimental background and report on 25 cases followed 6-16 months, J. Thoracic & Cardiovas. Surg. 49:103, 1965.
of epicardiectomy,
of the internal necrosis
revascularization
and
mammary death
of the entire
omental artery
graft,
and/or
in preventing
heart
implantation
myocardial
of the animal
Arthur M. Vineberg, M.D.* Yzrtaka Kato, M.D. W. J. Pirozynski, M.D. Montreal, Canada
mhe value of surgical techniques for 1 the relief of coronary artery insufficiency has been greatly doubted. This has been partly because clinical evaluation of revascularization procedures is difficult, due to the unpredictable character of the disease, and partly because basic experimental methods of evaluation of an operative procedure have been lacking. Many studies in our laboratory have made it quite clear that evaluation of a revascularization procedure by flow, backflow, ventricular fibrillation threshold, radioactive tracings, and many other such methods left a great deal to be desired and for the most part could not be relied upon. For this reason, over the years we have attempted to reproduce coronary artery occlusion by constricting the main stems at the locations at which obstructive diseaseoccurs in human patients.1-g Experiments have been carried out until a 100 per cent lethal test has been developed as a result of slow occlusion of the main stems of all three coronary arteries by Ameroid constrictors.‘“-‘” From
Besides survival of the animal from triple coronary artery occlusion, the degree of myocardial necrosis in both ventricles has been used as objective evidence of the value of a revascularization procedure. In addition, intra-arterial injection studies using Schlesinger mass13have been carried out in order to outline the extracardiac coronary pathways which may or may not develop, and which, when present, might explain any benefit that occurred as a result of a given revascularization procedure. Experimental
the Sub-Department of Cardiac Surgery, Royal Victoria and Pathology, McGill University, Montreal. Canada. Received for publication. Oct. 22, 1965. *Address: Sub-Department of Cardiac Surgery. Royal Victoria
79
study
Various methods of revascularization were tested against the 100 per cent coronary artery Ameroid occlusion test. A. Control group. In the control series of 20 animals there were 20 deaths; the spontaneous mortality was 100 per cent. The average survival time a-as 18.8 days; this was used as a base line to estimate the survival time. Survival time, therefore, becomes one of the criteria for the evaluation of various surgical procedures deHospital,
Hospital.
and the
Montreal
Departments
2, Quebec.
of Experimental
Canada.
Surgery
80
L’ineberg, Kuto, and Pirozynski
signed to relieve myocardial ischemia caused by triple coronary artery constriction. B. Treated groups. In all animals the Ameroid coronary artery constrictors were applied at the time of one of the following operative procedures: 1. EPICARDIECTOMY-10 ANIMALS. The epicardium was removed from the anterolateral and posterior surfaces of both ventricles, using specially designed epicardial scrapers which remove both layers of the epicardium without injury to the coronary vessels. 2. EPICARDIECTOMY CARDIECIOMY-10
AND ANIMALS.
SEROIIS
PERI-
The epicardium and serous layer of the pericardium were removed and the pericardium was closed. 3. EPICARDIECTOMY WITH INTERNAL MAMMARY
ARTERY
IMPLANTATION
(VINEBERG)-
10 ANIMALS. The left internal mammary artery was implanted into the anterior wall of the left ventricle. The epicardium was removed from the remainder of the left ventricle. The pericardium was left open. 4. FREE OMENTAL GRAFT OPERATION (VINEBERG)-10 ANIMALS. The entire heart was wrapped around by a graft of the greater omentum, which was completely detached from its abdominal pedicle, and the diaphragm was closed. The omentum was not sutured to the heart but to the ascending aorta. Epicardiectomy and serous pericardiectomy were not performed. The pericardium was closed over the omental graft. 5. FREE OMENTAL GRAFT OPERATION PLLS EPICARDIECTOMY AND SERO-PERICARDIECTOMY (~INEBERG)--20 ANIMALS. Extensive
epicard.iectomy of all surfaces of both ventricles was performed ; the serous layer of the pericardium was removed, as was the reflection of the pericardium over the base of the aorta. The greater omentum, after its detachment from the transverse colon, was xsrapped around the heart. It was fixed by multiple sutures to the ascending aorta and the heart. The pericardium was closed. 6. FREE OMENTAL GRAFT PLL:S EPICARDIECTOMY INTERNAL opERATION
AND
SERO-PERICARDIECTOMY
MAMMARY ARTERY (VINEBERG)-
IMPL4NTATION ANIMALS.
WITH
The
same technique as described under 2, 3, and 5 was followed. The left internal mammary artery was implanted into the anterior wall of the left ventricle. The pericardium was resected anteriorly to prevent encroachment upon the internal mammary artery implant. The omental graft was sutured to the free edges of the pericardium and to the anterior surface of the heart to avoid contact with the internal mammary artery. Postmortem
studies
All animals underwent the following investigations. A. Injection studies. The chest was opened through the fourth intercostal space; adhesions to the surface of the heart were not disturbed. The aorta was ligated above the diaphragm and at its junction with the left ventricle. Care was taken not to damage anastomotic vessels between the aorta and the omental graft. The thoracic aorta was cannulated proximal to the lower ligature. New Schlesinger mass, which does not pass through vessels that are less than 40 microns in diameter, was injected at pressures that ranged between 100 and 120 mm. of mercury, filling the aorta and its branches above the diaphragm with dye. ReAux of injection mass into the left ventricmar cavity and coronary arteries was prevented by the ligature at the aortoventricular junction. Thus, radiopaque substances appearing in the coronary arteries could only have entered them by traversing extracardiaccoronary anastomoses via the subpleural, mediastinal, and pericardial vessels. X-ray films of the heart in situ before and after injection outlined the extracardiac-coronary anastomoses when present. In the group of animals which had undergone the combined free omental graft and internal mammary artery implantation operation the internal mammary artery was ligated at the second intercostal space and cannulated distal to the ligature. The radiopaque mass injected into the thoracic aorta filled mediastinal vessels and outlined omental-coronary anastomoses as well as omental and/or mammary-coronary anastomoses. After injection and x-ray examination in situ, the internal
mammary artery was injected under q-stemic pressure and the heart was x-rayed again in situ. After removal of the heart, the ascending aorta was reinjected with Schlesinger mass so as to fill vessels leaving the root of the aorta to anastomose with those in the omental graft. The ligature around the base of the aorta \vas not removed. When the original aortic injection did not fill the entire coronary arterial tree, then both coronary ostia were cannulated with metal cannulae and injected with Schlesinger mass. Separate x-ray films were taken after injection of each coronary artery. After the injection mass had solidified, the heart was unrolled in order to study homocoronary and intercoronary anastomoses, as well as arterial channels which were formed to bypass the areas of Ameroid obstruction of the coronary’ arteries. Multiple x-ray pictures taken between the injections of radiopaque Schlesinger mass have made it possible to outline numerous arteriolar and larger vessels and to study anastomoses formed between: (a) the aorta and free omental graft, (b) the graft, coronary arteries, and myocardium, (c) mediastinal vessels, pericardium, graft, and coronary myocardial vessels, an d (d) internal mammary artery, myocardial *arterioles, and coronary arterioles. Injection studies are not so definitive as survival of animals and ventricular muscle mass. However, newly developed extracardiac channels through lvhich oxygenated blood can bypass the proximal points of coronary artery occlusion may be outlined. In this study, the injection mass was first introduced into the thoracic aorta in order to outline extracardiac coronary anastomoses. The filling of the coronary- arterial tree through the aorta via mediastinal vessels may prevent satisfactory visualization of homocoronary and intercoronary anastomoses by later individual coronary artery injections. This occurs because the injection mass hardens before there is time to remove the heart and inject the coronary arteries. Thus, the first injection should outline the important channels immediately. In this series, our attention has been focused upon the extracardiac channels reaching the heart from
the mediastinal vessels. The demonstration of homocoronary and intercoronary arteries, although desirable, was regarded to be of secondary importance. In most instances these have also been outlined satisfactorilyF. R. Pathologic studies. Each heart was examined grossly and microscopically for presence or absence and extent of ischemic myocardial damage. Jlultiple sections were taken from the right and left ventricles and the intraventricular septum. The portions of each artery included in the Ameroid constrictors were investigated microscopically to determine the extent of narrowing of the lumina of the right, anterior descending, and circumflex coronary arteries. This has been recorded as the percentage occlusion of the original cross-sectional area of the lumen. It has been expressed as an average occlusion for all three coronary arteries. The patency of the implanted internal mammary artery was determined over its entire length, including the myocardial tunnel. Results
In this study we have attempted to establish simp!e criteria for estimating the value of a revascularization procedure. The four most important criteria of value are: (1) survival time of animals; (2) extent of damage to the myocardium after triple coronary artery Ameroid constriction; (3) formation of extracardiac coronary anastomotic channels; and (4) formation of a new surface cardiac distribution system (omental graft) connecting together right and left coronary systems and arteriolar zones. 1. Survival of animals. The survival times of both the control series and the treated seriesare shown in Table I. CONTROL GKOIJP. In the control series the spontaneous mortality was 100 per cent. TKE~~TEDGKOI:PS.
1. In the series of 10 animals with epirardiectomp there was one death, i.e., 90 per cent spontaneous mortality. The average survival was 16 days; there was one long-term survivor, sacrificed 266 days postoperatively. 2. In the second series of 10 animals in which the epicardium and serous layer of
Am. Heart f.
Vineberg, Kato, and Pirozynski
82
Idy,
Table I. Survival time after trifile coronary artery
1966
Ameroid constriction (control and treated) I Died
Number
___-
of
Sarrifced
I --__-
---
!
I
animals
in series
Number Of animals
Average number Of I, days
Range in days I~
spontaneous mortality (%I
235-160 I days (%i
Arwage number I, of postop. days
Control
20
20
19
(9-29)
100
Treated 1. Epica rdiectomy
10
9
16
(7-28)
90
l-10
266
10
8
30
(21-40)
80
2-20
245
10
6
26
(15-39)
60
4-40
75
10
6
20
(9-30)
60
4-40
235
20
5
26
(17-37)
25
15-75
322
32
(19-50)
21
11-79
294
2. Epicardiectomy pericardiectomy
and sero-
3. Epicardiectomy mammary artery
and internal implant
4. Free
omental
5. Epicardiectomy, cardiectomy graft
graft sero-periand free omental
6. Epicardiectomy, seri-pericard lectomy, free omental graft, and internal mammary artery implant
14
Total Average
degree
of coronary
3
37
94 artery
occlusion:
Died
spontaneously:
the pericardium were removed, there were 8 deaths, a spontaneous mortality of 80 per cent. Survival time averaged 30 days. Two long-term survivors were sacrificed after 245 days postoperatively. 3. In lthe third group of 10 animals with epicardiectomy and internal mammary artery implantation there were 6 deaths; the spontaneous mortality was 60 per cent. The average length of survival was 24 days. There were 4 (40 per cent) longterm survivors, studied approximately 75 days postoperatively. 4. In the fourth series of 10 animals in which the free omental graft was wrapped around the heart there were 6 deaths, a spontaneous mortality of 60 per cent. The average length of survival was 20 days. There were 4 long-term survivors (40 per cent), studied on an average of 235 days postoperatively.
71.3 to 76.2 per cent. Sacrificed:
82.3 to 86.2 per cent.
5. In the fifth series of 20 animals in which the epicardiectomy, sero-pericardiectomy, and free omental graft operations were performed there were 5 deaths, a spontaneous mortality of 25 per cent. The average survival was 26 days. There were 15 long-term survivors (75 per cent); these were sacrificed and studied on an average of 322 days postoperatively. 6. In the final series of 14 animals which underwent epicardiectomy, sero-pericardiectomy, free omental graft application, and internal mammary artery implantation there were 3 deaths, a spontaneous mortality of 21 per cent. The average survival was 32 days. There were 11 long-term survivors (79 per cent); these were sacrificed for study on an average of 294 days postoperatively. 2. Pathologic studies. The pathologic findings of the control animals and those
Experimental
Table II. Tabulation of myocardial nary artery constriction
revascularization
damage in ex$erimental
of entire heart
animals after triple Ameroid
A nimals
20
20
Treated 1. Epicardiectomy
10
9
1
1
10
8
2
2
3. Epicardiectomy and internal mammary artery implant
10
6
1
1
4. Free
10
6
4
3
20
15
10
14
11
4
omental
5. Epicardiectomy, pericardiectomy, free omental
coro-
sacrificed
Control
2. Epicardiectomy sero-pericardiectomy
83
and
graft seroand graft
6. Epicardiectomy, seropericardiectomy, free omental graft, and internal mammary artery implant
which have been subjected to various surgical procedures are summarized in Tables II and III. A differentiation has been made between those animals which died from myocardial ischemia and those which were sacrificed many months after surgery. For those animals which died spontaneously the average degree of coronary artery occlusion ranged from 71.3 to 76.2 per cent in all groups. In those animals which were sacrificed up to 469 days after surgery there appeared to be an increase in the degree of coronary artery occlusion as time went on, and the average degree of cross-sectional occlusion of the total coronary artery inflow tract ranged from 82.3 to 86.2 per cent for the survivors in all six treated groups (Fig. 1). The extent of myocardial damage was graded as follows: No myocardial changes, 0. Focal infarcts (not grossly visible), f.
Moderate or large infarcts-(grossly noticeable-confined to one surface), ++. Massive-transmural infarcts (gross and microscopic), +++. The animals were grouped according to the operative procedure and to the mode of death (i.e., spontaneous or sacrificed). In the control group, 95 per cent of all animals showed massive to moderate myocardial damage in one or both ventricles at the time of spontaneous death. Epicardiectomy alone appears to have little beneficial effect on the prevention of massive myocardial infarction in either right or left ventricles in those animals which died spontaneously. In the second group, in which epicardiectomy was combined with serous pericardiectomy, no massive infarction was present in the animals. In the third group the implanted internal
Vineberg, Knto, nnd Pirozynski
t
+
+f + ++ + ++ + + z ++ +
I
t
+
+
+
+t+
t t
+
+
t
4
+ t
Experimentd
fevusclllarizlrtion
qf entire hectrt
85
Fig. 1. Photomicrograph of sections taken from the sites of Ameroid placement on coronary arteries in Animal No. 1.57, which was sacrificed 169 days postoperatively. .l, Photomicrograph section through the right coronary artery within the Ameroid; the degree of obstruction was 94.1 per cent. B, Photomicrograph of section taken through the anterior descending branch within the Ameroid; the degree of obstruction was 78.5 per cent. C, Photomirrograph of section taken through the circumflex coronary artery at the site of Ameroid constriction, showing 90.2 per cent occlusion of the lumen. The average degree of cross-sectional occlusion of the total coronary artery inflow tract in those animals that were sacriticed ranged from 82.3 to 86.2 per cent.
mammary artery combined with epicardiectomy prevented massive myocardial infarction in all animals. The simple omental graft without pedicle operation protected 40 per cent of the animals from massive myocardial infarction. When epicardiectomy, sero-pericardiectomy, and omental graft were performed, 5 (2.5 per cent) had no infarction and 10
(50 per cent) had scattered foci of fibrosis; none of the 75 per cent survivors had moderate to massive infarction. In the last series, in which epicardiectomy, sero-pericardiectomy, omental graft, and internal mammary artery implant \vere performed, 11 of 14 animals survived; 7 of these (50 per cent) showed no myocardial infarction in either ventricle, and 4 (36 per cent) showed only scattered
86
Am. Heart
Vineberg, Kate, and Pirozynski
high survival rate, as shown in Table I, but also a high survival rate of the ventricular muscle masses of both ventricles, as shown in Table III. Injection studies. The close correlation between animal survival after triple coronary artery occlusion and the development of extracardiac coronary anastomoses may be seen in the tabulation of coronary artery anastomoses shown in Table IV. In this table the various anastomoses which developed are shown for those animals which died spontaneously, and for those which were sacrificed for study. Anastomoses have been graded as follows: No anastomoses, 0. Slight anastomoses, +. Moderate anastomoses, ++. Extensive anastomoses, +++.
foci of fibrosis. None of the 11 surviving animals showed any evidence of moderately severe or massive myocardial infarction. All implants were patent. The average internal mammary artery patency for surviving animals was 71.8 per cent. In Table II, we have attempted to summarize our pathologic studies after triple coronary artery occlusion in all seven animal series. There is clearly a great difference in right and left ventricular muscle mass damage between the control and the treated animal in the last two groups. The last two operations, namely, epicardiectomy, sero-pericardiectomy and the free omental graft alone or combined with internal mammary artery implantation operation, were the only two procedures after which the animals had not only a
EXTRACARDIAC
Ci)RONARY
Table IV. Tabulation of coronary, extracardiac, and mammary coronary ar,lery occlz~sion and revascularization surgery Animals
coronary
dying spontaneously
Animals
Extracardiac mediastieal
in series
animals Of
+++I
++
Control
20
20
0
0
0
4
0
5
Treated 1. Epicardiectomy
10
9
0
0
0
2
2
7
1
0
10
80003442002020
3. Epicardiectomy and internal mammary artery implant
10
6
0
0 2.1112
0
1
1
5
4
4. Free omtrntal graft
10
6
1
0
0
0
0
0
5. Epicardiectomy, sero-pericardiectomy, and free omental graft
20
5
0
1
II
1
2
6. Epicardiectomy, sero-pericardiectomy, free omental graft, and internal mammary artery implant
14
3
0
1
0
0
0
Intercoronary
Homocoronary
Number
mammary
saerijced
Extracardiac
Intercoro-
Homo-
I I ~+++,++~~~~~~~~++~~~+~~~
-
-
-~
0
1
0
1
0
-
-
-
0 2.IM
0 ?.IM
3
1
4
0
4
2
2
3
1
4
0
3
15
4
11
5
9
11
4
3
11
7
4
5
6
9
2
KIM
3.IM
and sero-
1.m
Internal
after triple
_____ Number
IM:
ANASTUMOSES.
anastomoses
Number Of animals
2. Epicardiwtomy pericardhctomy
J.
July, 1966
coronary
anastomoses. +++:
Extensive
plus plus anastomoses. ++:
Moderate
anastomoss.
Experimental
Of the total of 94 animals (20 controls and 74 treated), 57 animals died spontaneously, all within an average of 24 days; 54 showed I10 extracardiac anastomoses (Fig. 2). TE lirty-seven of the 74 treated animals SUI rvived and were sacrificed for study;
Fig Am the dev
revascdarization
of entire heart
13 of these showed extensive, moderate, extracardiac coronary moses, not including mammary anastomoses. In Series 4, in which the free graft \vas simply xvrapped around
87
and 17 ana stocoron lary omenntal the hleart
. 2. Roentgenogram of the heart of Animal No. 208, which died after triple coronary artery occlusion 1by eroid constriction. The animal was studied 19 days after surgery. The only injection made was that thro wh thoracic aorta. In this animal, as in 54 of 57 animals which died spontaneously, there was no evidence of the elopment of extracardiac coronary anastomoses.
88
T’iueberg, Knto, rind Pirozyrtski
and the pericardium cIosed, it was possible to fill the coronary arteries with injection mass through the aorta via the graft (Fig. 3). In Series 5, in vf;hich only epicardiectomy and free omental graft were performed, 1.5 of 20 animals survived and 15 had moder-
ate to extensive extracardiac coronary anastomoses (Fig. 4). The anastomoses referred to are those that form between the mediastinal vessels, pericardium, omentum, and coronary arterioles. These are quite apart from the
Fig. 3. lioentgenogram of the heart of Animal So. 131, which died from a massive myocardial infarction in the right ventricle 2.5 days after placement of triple coronary artery Ameroids and a free omental graft. The onlv injection made was that through the thoraric aorta. The extracardiac radiopaque injection showed the development of omental-mammary-coronary anastomoses bringing the dye into the left coronary arterial system,
Experimenfnl
anastomoses formed between the implanted internal mammary artery and the myocardial arterioles (Fig. 5). The latter are listed as separate anastomoses in Table IV; thus, in the two implant series there are anastomoses not only from the
revmculnrization
89
of entire heart
supplementary operative procedures but from the internal mammary artery itself. INTERNAL WITH
MAMMARY
SUPPLEMENTARY
ARTERY OPERATIONS.
3, in which the internal mammary was combined with epicardiectomy,
IMPLANT In
Sel-ies
artery there
Fig. 4. Roentgenogram of the heart of Animal No. 482, which survived triple coronary artery Ameroid occlusion, epicardiectomy, and free omental graft operation. The animal was sacrificed and studied 469 days after surgery. The only injection made was that through the thoracic aorta. In this animal the injection mass filled the coronary arterial tree via the mediastinal-omental, omental-coronary, and omental-myocardial anastomoses.
90
Vineberg, Knto, and Pirozynski
Am. Hart
I.
.lzcly, 1966
Fig. 5. Roentgenogram of the heart of Animal Ko. 949, which had survived triple coronary artery occlusior 1 by Ame roids, internal mammary artery implantation, and free omental graft. The animal was studied 12 mot lths after surgery. The only injection made was that through the thoracic aorta. In this animal the injection n nass not cmly filled the coronary arterial tree via the mediastinal, omental, coronary, and myocardial vessels but filled the internal mammary artery in retrograde manner, as well.
Volw?Le
73
Nwnbsr
1
Experimentul
were 6 patent mammary-coronary anastomoses. Two of these animals died; in these, extensive intercoronary anastomoses had failed to form. In the 4 animals which survived there were extensive and moderate intercoronary anastomoses. When the omental graft was added to the internal mammary artery, 12 of 14 internal mammary arteries were patent; 11 of the animals survived, and these showed moderate to extensive mammary-coronary anastomoses. The internal mammary artery mammary-coronary anastomoses were in addition to moderate and extensive extracardiac mediastinal coronary anastomoses which had been formed as a result of the free omental graft. INTERCORONARY ANASTOMOSES. In none of the animals which died spontaneously, either the control or the treated groups, was there a single one which showed extensive intercoronary anastomoses (Fig. 6). On the right-hand side of Table IV, the findings in the animals which were sacrificed for study are recorded. Of the 37 animals which survived and were
Fig.
6. Roentgenogram of the
striction. The hear ‘t was unrolled
right coronary and x-rayed.
heart
revasculnrization
of entire heart
91
sacrificed for study, there were 19 which showed extensive, and 17 that showed moderate, intercoronary anastomoses (Fig. 7). Discussion
and
conclusion
The triple coronary artery Ameroid constriction test offers a reliable method of assaying a revascularization procedure. This simple test causes 100 per cent mortality in animals. There was massive myocardial damage in 17 of the control animals. A study of extracardiac coronary anastomoses and intercoronary anastomoses showed that nature failed to develop extracardiac coronary anastomoses. Likewise, nature failed to develop extensive intercoronary anastomoses. The most that nature was capable of doing in response to occlusion of all three coronary arteries was to develop moderate intercoronary anastomoses. Epicardiectomy and free omental graft proved to be effective in preventing death of the animal (75 per cent survival). It was likewise effective in protecting the
of Animal No. 124, which died 17 days after triple coronary artery Ameroid and then the left coronary artery were injected with Schlesinger mass. The Note the almost complete absence of intercoronary anastomoses.
92
Vj’neberg, Kate, and Pirozynski
Fig. 7. Koentgenogram of unrolled injected heart of Animal Ko. 1,000. ‘This animal underwent epicardiectomy of both ventricles and serous pericardiectomy at the same time as Ameroids were placed on the main stems of all three major coronary arteries. This animal was sacrificed 253 days after surgery. There were no extracardiac anastomoses, but there were very extensive intercoronarq. anastomoses and homocoronary anastomoses, which are shown in the injected unrolled heart. This is to be compared with the animal which died after triple coronary artery occlusion without any revascularization procedure (bee Fig. 6).
ventricular myocardium against moderate and/or massive myocardial infarction in 75 per cent of the animals. However, only 2.5 per cent of the survivors were completely free of any myocardial damage. The other 50 per cent showed focal or microscopic damage. Of the various operative procedures tested, the internal mammary artery implant combined with epicardiectomy and free omental graft proved to be best in preventing the death of the animals (79 per cent survival) and myocardial damage. In a series of 14 animals, only one showed massive myocardial infarction. Of the 11 surviving animals, 7 (50 per cent) showed no microscopic evidence of infarction, and 4 showed only scattered areas of microscopic fibrosis. The internal mammary artery implant operation combined with the free omental graft ‘was so effective in animals that it has been applied in the treatment of human coronary artery insufficiency, particularly in patients shown by tine coronary ar-
teriography to have triple coronary artery disease. At the time of the writing of this article, 78 patients have been operated upon since December, 1962. The results have been most gratifying. Summary
The Vineberg internal mammary artery implant operation combined with epicardiectomy and the Vineberg free omental graft operation is a revascularization procedure which develops new extracardiac omental, omental-coronary, mammary-coronary, and intercoronary anastomoses capable of replacing all three coronary arteries so as to maintain the health of the animal and the ventricular myocardium relatively free of damage. There would appear to be a direct relationship between the development of extracardiac omental-coronary, mammarycoronary, and inter-coronary anastomoses and the prevention of myocardial damage in the presence of triple coronary artery occlusion.
Experimental
REFERENCES 1. Vineberg, A. M., and Niloff, P. H.: The value of surgical treatment of coronary artery occlusion by implantation of the internal mammary artery into the ventricular myocardium, Surg., Gynec. & Obst. 91:551, 19.50. 2. Vineberg, A. M., and Miller, D.: Functional evaluation of an internal mammary coronary artery anastomosis, AM. HEART J. 45:873, 1953. 3. Vineberg, A. M., and Buller, W.: Technical factors which favour mammary-coronary anastomosis, J. Thoracic Surg. 30:411, 19.55. 4. Litvak, J.: Experimental production of gradual vascular occlusions. Thesis submitted in partial fulfillment of requirements for the M.Sc. degree, McGill University, Department of Neurology & Neurosurgery, Montreal Neurological Institute, 1957. 5. Litvak, J., Siderides, L. E., and Vineberg, A.: Experimental production of coronary artery insufficiency and occlusion, AX HEART J. 53:505, 1957. 6. Litvak, J., and Vineberg, A.: Experimental gradual arterial occlusion with in vitro and in vivo observations, Surgery 46:954, 19.59. 7. Vineberg, A., and Mahanti, B. C.: Evaluation of experimental myocardial revascularization operations by Ameroid coronary artery constriction, Surgery 47:748, 1960. 8. Duchesne, E. R., and Vineberg, A.: An experimental study of the effect of mechanically
9.
10.
11.
12.
13.
14.
revascularization
of entire heart
93
induced ischemia upon the mammary coronary anastomoses, Surgery 43:837, 1958. Vineberg, A., Mahanti, B. C., and I.itvak, J.: E xperimental gradual coronary artery conSurger) striction by Ameroid constrictors, 47:765, 1960. Vineberg, A.: Experimental background of myocardial revascularization by internal mammary artery implantation and supplementary technics, with its clinical application in 125 patients, Ann. Surg. 159:185, 1964. Vineberg, A.: Results of 14 years experience in the surgical treatment of human coronar) artery insufficiency, Canad. M. A. J. 92:325, 1965. Kato, Y.: Development of the triple Ameroid coronary arterial occlusion test---A 100% lethal test: Value of epicardiectomy, omental graft and/or internal mammary artery implant operation in preventing death of the animal and myocardium, Ph.D. Thesis, McGill IJniversity, May, 1965. Schlesinger, M. J., and Zoll, P. IM.: Incidence and localization of coronary artery occlusions, Arch. Path. (Chicano) 32:178. 1941. Vineberg, A:, Shanks, J., Piiarrt!, Ii., Criollos, R., Kato, Y., and Baichwal, K. S.: Myocardial revascularization by omental graft without pedicle: Experimental background and report on 25 cases followed 6-16 months, J. Thoracic & Cardiovas. Surg. 49:103, 1965.