- Email: [email protected]
Arterialization of coronary veins in the treatment of myocardial ischemia
Arterialization of coronary veins in the treatment of myocardial ischemia Six dogs were subjected to arterialization of the left anterior descending vein (LADV). Tests showed that the predominant flow through these vessels did perfuse the myocardium: Lowering of oxygen content of the perfusing blood and myocardial uptake of macroaggregate albumin 1.11] were noted. The possibility of small atrioventricular (A-V) shunts was not excluded.
R. S. Gardner, M.D., G. J. Magovern, M.D., S. B. Park, M.D., and C. M. Dixon, Pa.
Pittsburgh,
In
1898, the possibility of retrograde perfusion of the coronary veins was suggested by the work of Pratt. 2~ He was able to sustain myocardial contractions for several hours in a eat's heart by what was essentially coronary sinus perfusion. In 1930, Batson and Beller" published a series of experiments in which they demonstrated clearly that flow in the coronary sinus is reversed in dogs that have a falling arterial pressure and an increased intra-atrial pressure. From these experiments they reached the following conclusion: With a low pressure in the capillary bed (as in cases of double coronary occlusion or as in our experiments), flow in the veins during atrial systole is probably toward the capillary bed being emptied during the ensuing ventricular systole. In arterial occlusion this would give a flow and ebb circulation for the myocardial capillaries by way of the veins. This irrigation by venous channels may explain the disappearance of pain in angina pectoris, with the inception of those complications accompanied by a fall in the coronary artery pressure. * From the Department of Surgery, Allegheny General Hospital, Pittsburgh, Pa, 15212. Received for publication April 30, 1974. "From Batson, O.V., and Bellet, S.: Am. Heart J. 6: 206, 1930, published by The C. V. Mosby Company.
The first attempts at arterialization of the coronary sinus were made by Roberts" in 1943 and Beck" in 1948. Beck' did extensive work in refining this approach to revascularization of the heart and by 1954 had performed 186 such operations on patients with coronary artery disease. He described this operation as follows: The number 2 operation consists of first shunting arterial blood into the coronary sinus. This is accomplished by placing a free vein graft between the aorta and the coronary sinus or by direct anastomosis between these structures. The second stage of this operation is done two or three weeks later and consists of partial occlusion of the coronary sinus where it enters the right auricle. This partial occlusion raises the pressure of blood in the sinus and produces retrograde flow. *
The Beck 2 procedure reduces the incidence of morbidity and death in selected cases of coronary artery disease,"- x, i r However, even in Beck's hands, the mortality rate of the operation remained high-approaching 29 per cent.' Feil" reported a 37.8 per cent mortality rate. More recent work has shown improved mortality rates." Because of the limited success, the high "From Beck, C. S., and Leighninger, D. S.: J. A. M. A. 156: 1226, 1954, published by The American Medical Association.
273
274
The Journal of Thoracic and Cardiovascular
Gardner et al.
number of deaths, and particularly the advent of direct coronary artery bypass as practiced by Favaloro and colleagues," the Beck 2 operation did not achieve wide use and was discarded. Other aspects of retrograde perfusion have gained importance in recent years, as a number of investigators"- 12, 1:1, 1"-20 have used this approach to provide myocardial perfusion during aortic valve surgery. Much information has been gained through this experience. As coronary artery bypass has progressed, a certain group of nonsurgical candidates have emerged. Angiographic studies by a number of groups have shown that 12 to 50 per cent of their patients are not candidates for surgery because of the sclerotic changes in the coronary vessels, with poor runoff in hearts with otherwise good ventricular function.': u, 22 In our own experience, the figure was approximately 20 per cent. This was a large enough group to stimulate a search for another method of cardiac revascularization. Early experiments by Magovern'" with arterialization of the left anterior descending vein (LADV) in dogs brought forth the following problems: 1. One heart scan following injection of 131 1 marcoaggregated albumin into the arterialized LADV showed only a lung scan, a fact which suggested a complete atrioventricular (A-V) shunt. 2. One angiogram of the internal mammary artery (IMA) and LADV suggested rapid filling of the coronary sinus. It was noted in all films that the flow drained into the coronary sinus after diffusion through the myocardium. 3. Studies relating electrocardiographic changes and cardiac function to induce acute infarctions were inconclusive although other investigators have shown marginal improvement in survival rates following retrograde perfusion of the LADV." 4. Changes in myocardial oxygen tension measured by oxygen tension probes were not reproducible. Because of these problems, two questions arose:
Surgery
1. Was arterialization of the LADV producing a predominant or complete A-V shunt? Other investigators had also suggested this possibility.3. x 2. Was the myocardium in fact being perfused by the retrograde perfusion of the LADV? There have been some indications to this effect in a recent investigation which showed increased myocardial oxygen tensions following arterialization of the LADV.2" The following experimental design was planned to answer these questions. The object was to compare coronary sinus oxygen content of the arterialized LADV with that of a known coronary sinus fistula under identical conditions.
Materials and methods
Six adult fasting mongrel dogs weighing 20 to 30.5 kilograms were anesthetized with intravenous sodium Pentothal (30 mg. per kilogram), and respirations were controlled with a Harvard respirator through a cuffed endotracheal tube. An incision was made in the left fourth intercostal space. The left internal mammary artery (LIMA) was dissected free, and heparin (3 mg. per kilogram) was administered intravenously. The left femoral artery was cannulated for perfusion, a single venous return cannula was inserted in the right atrial appendage, and monitoring lines for central venous pressure and arterial pressure were placed in the left femoral vein and right femoral artery, respectively. The animals were placed on cardiopulmonary bypass at flow rates of approximately 100 m!. per kilogram per minute and temperatures of 30° to 32° C. The extracorporeal circuit consisted of a roller pump and bubble oxygenator primed with 500 m!. of cross-matched dog blood and 1,000 m!. Plasma-Lyte. A vent was placed in the left ventricle through the apex. Two tourniquets were placed around the LADV at its midportion, about 1 to 2 cm. apart, to allow for anastomosis of the LIMA to the LADV (Fig. I). The anastomosis was done with running 6-0 Prolene cardiovascular sutures. The heart
Volume68 Number 2 August, 1974
Arterialization of coronary veins 275
Fig. 1. Photograph and schema of dog heart showing (A) tourniquet around the distal left anterior descending vein, (B) tourniquet around the proximal LADV, (C) left internal mammary artery, and (D) distal left anterior descending vein.
was fibrillated during the anastomosis but the aorta was not cross-clamped. The two tourniquets were tightened about the LADV to provide an avascular field. Next, the heart was defibrillated and, with the animal on partial bypass, the coronary sinus was cannulated through the right atrium with a flanged No. 12 Fr. catheter. This catheter was held in place by a tourniquet encircling the orifice of the coronary sinus (Fig. 2). The animal was removed from bypass, and its condition was allowed to stabilize. Vital signs were controlled by volume replacement throughout the experiment without the use of cardiotonics, vasopressors, etc., which might have affected the flow or other characteristics of the heart vessels. When stable vital signs could not be maintained as described, the experiment was discontinued. However, if vital signs including central venous pressure were stable, the following three steps were performed at 10 to 15 minute intervals. I. The LIMA was clamped to obtain control values of the normally beating heart. Flow through the coronary sinus was measured directly. Blood gases of the arterial and
coronary sinus blood were obtained simultaneously. 2. The LIMA was opened and the tourniquet around the proximal LADV (Fig. 1, B) was tightened to allow retrograde flow into the distal branches of the LADV; this flow had shown on earlier angiographic studies to be perfusion of the myocardium (Fig. 3). Coronary sinus flow was measured directly, and LIMA flow was measured by a Model lOOI-B Micron Instruments, Inc., flowmeter. Blood gas samples were obtained simultaneously from arterial and coronary sinus blood. 3. The LIMA was opened, the tourniquet around the distal LADV (Fig. 1, A) was tightened, and that around the proximal LADV released (Fig. I, B) to allow a proximal A-V shunt into the coronary sinus. A Hoffman clamp was used to partially occlude the LIMA so that the flow into the LADVcoronary sinus would be reduced to the same as that in step 2. The methods of flow and gas measurement were identical to those used in step 2. These steps were repeated at will by simply releasing and occluding one of the three
The Journal 01
276
Gardner et al.
Thoracic and Cardiovascu lar Surgery
Fig. 2. Photograph and schema of dog heart showing (A ) coron ary sinus cannula and (B) tourniquet around the coronary sinus.
sites mentioned (Fig. I, A, B, or C). At the completion of the operation, the last 4 animals had I:l1 I macroaggregated albumin (d iameter of 10 to 60 JL) injected into the LIMA. Postoperative heart and lung scans were obtained (Fig. 4). Results
I . The most significant finding was the oxygen saturation difference between the arterialized LADV and the known fistula; blood samples were taken from the coronary sinus (Table I). Measurement of this oxygen saturation difference in all dogs tested (except second series dog No.6) showed a loss in oxygen content of the blood perfusing the LADV in a retrograde manner, as compared to that of a known shunt of the same magnitude. 2. The estimated percentage of LIMA blood reaching the coronary sinus without loss of oxygen content ranged between zero and 73 per cent (Table II) as determined in Diagram I. U is the LIMA blood flow (milliliter s) reaching the coronary sinus with no loss of oxygen content ; U % is per cent of IMA blood flow reaching the coronary sinus with no loss of oxygen content; V im"
is IMA flow (in milliliters per minute); V es is coronary sinus flow (milliliters per minute) with arterialization of the LADV; Hb is animal's hemoglobin (grams per cent) ; 1.35 is milliliters of oxygen per grams per cent of hemoglobin ; S" is per cent saturation of arterial blood; S,. is per cent saturation of coronary sinus blood during arterialization of the LADV; and SI' is per cent saturation of coronary sinus blood during normal heart perfusion with occlusion of LIMA. S,. and St. were accepted for calculations when arterial saturations (Sll) were similar. 3. Table III shows the percentage of LIMA blood perfusing myocardium as determined by: % LIMA flow to myocardium =
100 - U%.
4. Radioisotope studies on the last 4 dogs showed no fistulas larger than IOJL in 3 animals (Fig. 4). (Studies in animal No. 5 were deleted because of technical problems.) Discussion
Because of the marginal successes of retrograde perfusion of the coronary sinus as described by Beck,' and because of the more recent advent of coronary bypass surgery,
Volume 68 Number 2
Arterialization of coronary veins
277
August, J974
Fig. 4. Macroaggregate albumin
13
11 heart scan.
A, injection site, left internal mammary artery. B, Distribution of left anterior descending vein.
Small arrows approximate the cardiac border. Fig. 3. Angiogram of left internal mammary artery and left anterior descending vein showing retrograde perfu sion of the heart.
little interest has been shown in this type of myocardial revascularization. Successes with retrograde perfusion during aortic valve surgery, coupled with the difficulty of treating a relatively large group of patients with severe angina, diffuse coronary artery disease, and good ventricular function who are currently nonamenable to surgery, prompted Magovern's group 2 I to reinvestigate coronary sinus perfusion as a means to increase myocardial blood supply. Consideration of this previous work done by others suggested that more success might be obtained if a limited area of myocardium were to be perfused by retrograde venous arterialization. Two overriding facts persuaded us to take this approach. I. The mortality rate was high when complete sinus arterialization was attempted, apparently because of the inability of the heart to drain off its newly found blood supply . Some early experiments had indicated that this would be true. ' 2. In all successful cases of retrograde coronary sinus perfusion during aortic valve surgery, cardiopulmonary bypass had been
employed; bypass allowed the heart to decongest itself through the coronary arteries and Thebesian veins, since these areas were not under arterial pressure. Even in these cases caution had to be exercised so that coronary sinus perfusion pressures were kept below a safe level. It seemed feasible that a more limited perfusion of a small area of the heart would eliminate these problems. The LADV was selected because of its easy accessibility and its associated, frequently sclerotic coronary artery. The surrounding veins seemed capable of handling the new blood supply because of the limited area and particularly because the artery would be supplying marginal quantities of blood. Work by Magovern'" and others" 21i confirmed the ease with which dogs tolerated the arterialization of the LADV. After the feasibility of such an approach had been proved,": 2 1 , 21i other questions arose. The possibility of a large shunt, as mentioned, seemed likely and became a main concern. In all 6 animals , blood gas analysis of coronary sinus blood confirmed that there were no large shunts . This can be shown in Table I by comparing oxygen saturations of
The Journal of
278
Gardner et al.
Thoracic and Cardiovascular Surgery
Table I
Dog No.
Weight (Kg.)
30.5
Test
LADY Fistula LADY Control LADY Control
2
27.2
LADY Fistula Control LADY Fistula Control Fistula LADY
3
24.0
Control LADY Fistula LADY Fistula
4
28.0
Control LADY Fistula Control LADY Fistula
!
pH
Po., (mm. Hg.)
O. sat.
C.S. artery C.S. artery C.S. artery C.S. artery C.S. artery C.S. artery
7.25 7.89 7.65 7.65 7.53 ·7.63 7.55 7.63 7.55 7.89 7.91 7.89
20 54 26 200 28 179 26 181 20 130 18 135
24 97 70 99 61 99 55 99 39 99 65 99
C.S. artery C.S. artery C.S. artery C.S. artery C.S. artery C.S. artery C.S. artery C.S. artery
7.39 7.39 7.43 7.39 7.45 7.47 7.41 7.49 7.38 7.48 7.39 7.48 7.41
22 101 28 70 20 83 20 131 27 53 21 53 228
38 97 47 93 34 96 33 99 52 88 35 88 100
7.39 7.41
30 88
C.S. artery C.S. artery C.S. artery C.S. artery C.S. artery
7.55 7.57 7.50 7.54 7.52 7.56 7.35 7.56 7.49 7.51
C.S. artery C.S. artery C.S. artery C.S. artery C.S. artery C.S. artery
7.42 7.48 7.43 7.50 7.46 7.46 7.47 7.51 7.44 7.45 7.43 7.41
Blood sample
I
(%)
I
IMA flow (mi.)
c.s.
flow (ml./ min.)
26
72
30
80
34
74
0
70
30
90
0
75
30
87
30
100
0
73
30
97
30
124
0
111
30
160
59 96
30
112
20 205 27 198 36 230 28 190 35 225
40 99 59 99 77 99 48 93 73 99
0
38
24
56
20
58
20
56
20
58
31 350 32 230 40 325 25 475 31 450 52 451
61 99 65 99 78 99 50 99 64 99 86 99
0
70
42
68
40
86
0
70
44
76
42
75
Legend: IMA, Internal mammary artery. C.S., Coronary sinus. LADV. Left anterior descending vein.
Volume 68
Arterialization of coronary veins
Number 2
279
August, 1974
Table I-Cont'd Po,
Dog No.
Weight (Kg.)
Test LADY Fistula
5
27.0
Control LADY Fistula Control LADY Fistula
6
20.0
LADY Fistula Control LADY Fistula Control
Blood sample
(mm. Hg.)
O. sat.
pH
C.S. artery C.S. artery
7.45 7.47 7.45 7.48
36 275 85 375
73 99 96 99
C.S. artery C.S. artery C.S. artery C.S. artery C.S. artery C.S. artery
7.48 7.53 7.52 7.51 7.51 7.52 7.54 7.55 7.52 7.58 7.38 7.45
36 132 26 105 52 103 27 103 28 112 32 98
74 99 59 98 89 98 62 98 63 99 62 97
C.S. artery C.S. artery C.S. artery C.S. artery C.S. artery C.S. artery
7.21 7.20 7.23 7.26 7.27 7.28 7.27 7.30 7.26 7.30 7.27
28 208 45 208 39 250 34 211 42 201 40 202
41 99 74 99 65 99 59 99 70 99 68 99
the coronary sinus blood during arterialization of the LADV against those of the known A-V fistula. The figures show significant differences in all dogs (except in second series dog No.5, in which the cannula appears to have been pulled into the right atrium). Table II, again, confirms the absence of large shunts. In this table, the oxygen saturation of blood from the coronary sinus of a normal heart is the base line, and figures are determined from coronary sinus flow and saturation during arterialization of LADV. Calculation of these figures is based on the amount of flow by unaltered arterial blood reaching the coronary sinus that is necessary to cause the same oxygen saturation as that found in the coronary sinus during LADV
7.30
(%)
c.s.
IMA
flow
flow (ml.)
(ml./ min.)
48
73
48
103
0
75
20
70
20
74
0
70
27
74
27
72
12
80
12
100
0
94
17
85
17
92
0
80
arterialization. This figure could represent an estimation of the largest shunt that would be possible under the given laboratory data. The figure must also represent a percentage of blood unneeded by the myocardium's metabolic demand and therefore an increase in coronary sinus blood oxygen saturation (physiologic shunting). Table II then represents a combination of fistulous blood and perfused blood not used by the myocardium. Isotope scans such as the one shown in Fig. 4 suggest more of the latter. A small fistula is not considered a problem5 . " and, in fact, may be beneficial by encouraging better patency and collaterals." Fig. 4 is a scan of the heart and lungs from animal No. 3 after the injection of macroaggregated albumin (diameter of 10 to 60p.)
The Journol of
280
Gardner et al.
Thorocic and Cardiovascular Surgery
Diagram I (V"R x Vol. % O 2 : Coronary sinus blood with arterialization of LADV)
(VCR
X
Vol. % O 2 : Coronary sinus blood, normal heart perfusion)
u=----------------------------Vol. % O 2 : Coronary sinus blood, normal heart perfusion)
(Vol. % O 2 : Arterial blood
U%
=
U%=
(Ves x Hb x 1.35 x Sv) - (Ves x Hb x 1.35 x So) (Hb x 1.35 x Sa) Ves (Sv - Se) Virna (Sa - So)
U%
1
29.7 0 17.6 0 73.0 37.0 16.6 48.0 0 0 0
2 3 4 5 6
I Average U% 14.9 8.8 55.0 32.3 0 0
Legend: U%, Per cent of internal mammary artery blood flow reaching the coronary sinus with no loss of oxygen content.
Table III. Calculated IMA-LADV flow to myocardium Dog. No.
Flow (%)
1
85.1 91.2 45.0 67.7 100.0 100.0
2 3 4 5 6
X
1.35 x Se)
1
x __•
Virna
.
Table II Dog No.
(Hb
Legend: IMA, Internal mammary artery. LADY, Left anterior descending vein.
into the LADV. This scan, which is also typical of animal Nos. 4 and 6, shows capture by the myocardium of the entire injection with no loss to the lungs. It can be concluded that no A-V fistula over lOfL in size exists in these 3 animals. Table III shows the percentage of IMALADV flow that is reduced from an arterial oxygen saturation to the level of that found in the coronary sinus in the control heart.
The supposition is that this blood perfused the myocardium and lost this volume of oxygen to the cells. Previous angiograms (Fig. 3) had demonstrated the diffusion of the flow through the myocardium, a fact that was also confirmed by isotope scan. It seems fair to conclude that the myocardium does, in fact, receive direct perfusion from the arterialized LADV. Long-term studies in dogs indicate the patency of the vessels. 21 The coronary venous system in man has fewer variations than that of dogs1 8 , 2 1 and will be a better recipient of retrograde perfusions. It would appear from these tests that LADV arterialization might be of value for patients with diffuse coronary artery disease, incapacitating angina, and good ventricular function who are not currently candidates for coronary bypass surgery. Summary
Arterialization of the LADV increased myocardial uptake of oxygen from the perfusing blood. This we determined by comparing retrograde arterial flow against flow of a known fistula. Second, the amount of oxygen lost to cardiac muscle during arterialization of the LADV was compared with that of the normal heart. These studies showed loss of oxygen content from a good portion of the new source of cardiac blood as it perfused the myocardium. These same calculations did not rule out the possibility of a small fistula and in fact did strongly suggest that one exists. The heart scans done with macro aggregate 131 1, on the other hand,
Volume 68 Number 2
Arterialization of coronary veins
28 I
August, 1974
indicated that the fistulas, if present, were small and that arterialization of the LADY perfused evenly the distribution of the LADY. Conclusion
I. Arterialization of the LADY does cause increased myocardial perfusion. 2. Arterialization of the LADY does not cause a large A-Y shunt, although the presence of a small shunt cannot be ruled out. 3. The next step is the clinical application of arterialization of the LADY in selected cases. LADV revascularization has been done in 7 patients who fit the previously discussed criteria. The results although still early are encouraging. REFERENCES I Arealis, E. G., Voider, J. G. R., and Kolff, W. J.: Communications to the Editor: Arterialization of the Coronary Vein Coming From an Ischemic Area. Chest 63: 462, 1973. 2 Bakst, A. A., Adam, A., Goldberg, H., and Bailey, C. P.: Arterialization of the Coronary Sinus in Occlusive Coronary Artery Disease, J. THORAC. SURG. 29: 188, 1954. 3 Batson, O. V., and Bellet, S.: The Reversal of Flow in the Cardiac Veins, Am. Heart 1. 6: 206, 1930. 4 Beck, C. S.; The Development of a New Blood Supply to the Heart by Operation, Ann. Surg. 102: 801, 1935. 5 Beck, C. S.: Revascularization of the Heart, Ann. Surg. 128: 854, 1948. 6 Beck, C. S.: Surgical Operations for Coronary Artery Disease, in Encyclopedia of Thoracic Surgery, vol. II, Berlin, 1959, Springer-Verlag, p. 779. 7 Beck, C. S., and Leighninger, D. S.: Operations for Coronary Artery Disease, J. A. M. A. 156: 1226, 1954. 8 Beck, C. S., Stanton, E., Batiuchok, W., and Leiter, E.: Revascularization of Heart by Graft of Systemic Artery Into Coronary Sinus, J. A. M. A. 137: 436, 1948. 9 Bhayana, J. N., Olsen, D. 8., Byrne, J. P., and Kolff, W. J.: Reversal of Myocardial Ischemia by Arterialization of the Coronary Vein, J. THORAC. CARDIOVASC. SURG. 67: 125, 1974. 10 Blanco, G., Adam, A., and Fernandez, A.: A Direct Experimental Approach to the Aortic Valve. II. Acute Retroperfusion of the
Coronary Sinus, J. THORAC. SURG. 32: 171, 1956. 11 Brown, A. H., Braimbridge, M. V., Niles, N. R., Gerbode, F., and Aguilar, M. J.: The Effect of Excessively High Perfusion Pressures on the Histology, Histochemistry, Birefringence, and Function of the Myocardium, J. THORAC. CARDIOVASC. SURG. 58: 655, 1969. 12 Brown, A. H., Niles, N. R., Braimbridge, M. V., and Austen, W. G.: Retrograde Insufflation of Gaseous Oxygen Into the Coronary Sinus as a Means of Myocardial Maintenance, Arch. Surg. 105: 622, 1972. 13 Camishion, R. C., Davies, A. L., Tokunaga, K., and Solit, R. W.: Retrograde Perfusion of the Coronary Arteries With Gaseous Oxygen During Cardiopulmonary Bypass, Surgery 59: 145, 1966. 14 Eckstein, R. W., Smith, G., Eleff, M., and Demming, J.: The Effect of Arterialization of the Coronary Sinus in Dogs on Mortality Following Acute Coronary Occlusion, Circulation 6: 16, 1952. 15 Eckstein, W. R., and Leighninger, D. S.: Chronic Effects of Aorta-Coronary Sinus Anastomosis of Beck Dogs, Circ, Res. 2: 60, 1954. 16 Favaloro, R. G., Effler, D. 8., Groves, L. K., Sheldon, W. C., Shirey, E. K., and Sones, F. M., Jr.: Severe Segmental Obstruction of the Left Coronary Artery and Its Divisions, J. THORAC. CARDIOVASC. SURG. 60: 469, 1970. 17 Feil, H.: Clinical Appraisal of the Beck Operation, Ann. Surg, 118: 807, 1943. 18 Gott, V. L., Gonzalez, J. L., Zuhdi, M. N., Varco, R. L., and Lillehei, C. W.: Retrograde Perfusion of the Coronary Sinus for Direct Vision Aortic Surgery, Surg, GynecoJ. Obstet. 104: 319, 1957. 19 Hammond, G. L., Davies, A. L., and Austen, W. G.: Retrograde Coronary Sinus Perfusion: A Method of Myocardial Protection in the Dog During Left Coronary Artery Occlusion, Ann. Surg. 166: 39, 1967. 20 Lillehei, C. W., DeWall, R. A., Gott, V. L., and Varco, R. L.: The Direct Vision Correction of Calcific Aortic Stenosis by Means of a Pump-Oxygenator and Retrograde Coronary Sinus Perfusion, Chest 30: 123, 1956. 21 Magovern, G. J., Park, S. B., Liebler, G. A., Dixon, C. M., Begg, F. R., Dosios, T., and Fisher, D. L.: Unpublished work, 1972-1973. 22 Moll, J. W., Dziatkowiak, A., Rybinski, K., Edelman, M., and Ratajczak-Pakalska, E.: Arterialisierung des sinus coronarius-s-indikationen, technik, ergebnisse, Thoraxchirurgie 21: 295, 1973. 23 Neidorf, B. S., Brest, A. N., Kasparian, H., Wiener, L., and Rafter, J. J.: Angiocardio-
The Journal of
282
Gardner et al.
graphic Assessment for Coronary Bypass Surgrey, Pa. Med. 76: 43, 1973. 24 Pratt, F. H.: The Nutrition of the Heart Through the Vessels of Thebesius and Coronary Veins, Am. 1. PhysioI. 1: 86, 1898. 25 Roberts, 1. T., Browne, H. S., and Roberts, G.: Nourishment of the Myocardium by Way
Thoracic and Cardiovascular Surgery
of the Coronary Veins, Fed. Proc. 2: 90, 1943. 26 Wiener, L.: Reversal of Acute Myocardial Ischemia by Retrograde Intercoronary Venoarterial Perfusion (abstr.), Am. J. CardioI. 33: 178, 1974.
R. S. Gardner, M.D., G. J. Magovern, M.D., S. B. Park, M.D., and C. M. Dixon, Pa.
Pittsburgh,
In
1898, the possibility of retrograde perfusion of the coronary veins was suggested by the work of Pratt. 2~ He was able to sustain myocardial contractions for several hours in a eat's heart by what was essentially coronary sinus perfusion. In 1930, Batson and Beller" published a series of experiments in which they demonstrated clearly that flow in the coronary sinus is reversed in dogs that have a falling arterial pressure and an increased intra-atrial pressure. From these experiments they reached the following conclusion: With a low pressure in the capillary bed (as in cases of double coronary occlusion or as in our experiments), flow in the veins during atrial systole is probably toward the capillary bed being emptied during the ensuing ventricular systole. In arterial occlusion this would give a flow and ebb circulation for the myocardial capillaries by way of the veins. This irrigation by venous channels may explain the disappearance of pain in angina pectoris, with the inception of those complications accompanied by a fall in the coronary artery pressure. * From the Department of Surgery, Allegheny General Hospital, Pittsburgh, Pa, 15212. Received for publication April 30, 1974. "From Batson, O.V., and Bellet, S.: Am. Heart J. 6: 206, 1930, published by The C. V. Mosby Company.
The first attempts at arterialization of the coronary sinus were made by Roberts" in 1943 and Beck" in 1948. Beck' did extensive work in refining this approach to revascularization of the heart and by 1954 had performed 186 such operations on patients with coronary artery disease. He described this operation as follows: The number 2 operation consists of first shunting arterial blood into the coronary sinus. This is accomplished by placing a free vein graft between the aorta and the coronary sinus or by direct anastomosis between these structures. The second stage of this operation is done two or three weeks later and consists of partial occlusion of the coronary sinus where it enters the right auricle. This partial occlusion raises the pressure of blood in the sinus and produces retrograde flow. *
The Beck 2 procedure reduces the incidence of morbidity and death in selected cases of coronary artery disease,"- x, i r However, even in Beck's hands, the mortality rate of the operation remained high-approaching 29 per cent.' Feil" reported a 37.8 per cent mortality rate. More recent work has shown improved mortality rates." Because of the limited success, the high "From Beck, C. S., and Leighninger, D. S.: J. A. M. A. 156: 1226, 1954, published by The American Medical Association.
273
274
The Journal of Thoracic and Cardiovascular
Gardner et al.
number of deaths, and particularly the advent of direct coronary artery bypass as practiced by Favaloro and colleagues," the Beck 2 operation did not achieve wide use and was discarded. Other aspects of retrograde perfusion have gained importance in recent years, as a number of investigators"- 12, 1:1, 1"-20 have used this approach to provide myocardial perfusion during aortic valve surgery. Much information has been gained through this experience. As coronary artery bypass has progressed, a certain group of nonsurgical candidates have emerged. Angiographic studies by a number of groups have shown that 12 to 50 per cent of their patients are not candidates for surgery because of the sclerotic changes in the coronary vessels, with poor runoff in hearts with otherwise good ventricular function.': u, 22 In our own experience, the figure was approximately 20 per cent. This was a large enough group to stimulate a search for another method of cardiac revascularization. Early experiments by Magovern'" with arterialization of the left anterior descending vein (LADV) in dogs brought forth the following problems: 1. One heart scan following injection of 131 1 marcoaggregated albumin into the arterialized LADV showed only a lung scan, a fact which suggested a complete atrioventricular (A-V) shunt. 2. One angiogram of the internal mammary artery (IMA) and LADV suggested rapid filling of the coronary sinus. It was noted in all films that the flow drained into the coronary sinus after diffusion through the myocardium. 3. Studies relating electrocardiographic changes and cardiac function to induce acute infarctions were inconclusive although other investigators have shown marginal improvement in survival rates following retrograde perfusion of the LADV." 4. Changes in myocardial oxygen tension measured by oxygen tension probes were not reproducible. Because of these problems, two questions arose:
Surgery
1. Was arterialization of the LADV producing a predominant or complete A-V shunt? Other investigators had also suggested this possibility.3. x 2. Was the myocardium in fact being perfused by the retrograde perfusion of the LADV? There have been some indications to this effect in a recent investigation which showed increased myocardial oxygen tensions following arterialization of the LADV.2" The following experimental design was planned to answer these questions. The object was to compare coronary sinus oxygen content of the arterialized LADV with that of a known coronary sinus fistula under identical conditions.
Materials and methods
Six adult fasting mongrel dogs weighing 20 to 30.5 kilograms were anesthetized with intravenous sodium Pentothal (30 mg. per kilogram), and respirations were controlled with a Harvard respirator through a cuffed endotracheal tube. An incision was made in the left fourth intercostal space. The left internal mammary artery (LIMA) was dissected free, and heparin (3 mg. per kilogram) was administered intravenously. The left femoral artery was cannulated for perfusion, a single venous return cannula was inserted in the right atrial appendage, and monitoring lines for central venous pressure and arterial pressure were placed in the left femoral vein and right femoral artery, respectively. The animals were placed on cardiopulmonary bypass at flow rates of approximately 100 m!. per kilogram per minute and temperatures of 30° to 32° C. The extracorporeal circuit consisted of a roller pump and bubble oxygenator primed with 500 m!. of cross-matched dog blood and 1,000 m!. Plasma-Lyte. A vent was placed in the left ventricle through the apex. Two tourniquets were placed around the LADV at its midportion, about 1 to 2 cm. apart, to allow for anastomosis of the LIMA to the LADV (Fig. I). The anastomosis was done with running 6-0 Prolene cardiovascular sutures. The heart
Volume68 Number 2 August, 1974
Arterialization of coronary veins 275
Fig. 1. Photograph and schema of dog heart showing (A) tourniquet around the distal left anterior descending vein, (B) tourniquet around the proximal LADV, (C) left internal mammary artery, and (D) distal left anterior descending vein.
was fibrillated during the anastomosis but the aorta was not cross-clamped. The two tourniquets were tightened about the LADV to provide an avascular field. Next, the heart was defibrillated and, with the animal on partial bypass, the coronary sinus was cannulated through the right atrium with a flanged No. 12 Fr. catheter. This catheter was held in place by a tourniquet encircling the orifice of the coronary sinus (Fig. 2). The animal was removed from bypass, and its condition was allowed to stabilize. Vital signs were controlled by volume replacement throughout the experiment without the use of cardiotonics, vasopressors, etc., which might have affected the flow or other characteristics of the heart vessels. When stable vital signs could not be maintained as described, the experiment was discontinued. However, if vital signs including central venous pressure were stable, the following three steps were performed at 10 to 15 minute intervals. I. The LIMA was clamped to obtain control values of the normally beating heart. Flow through the coronary sinus was measured directly. Blood gases of the arterial and
coronary sinus blood were obtained simultaneously. 2. The LIMA was opened and the tourniquet around the proximal LADV (Fig. 1, B) was tightened to allow retrograde flow into the distal branches of the LADV; this flow had shown on earlier angiographic studies to be perfusion of the myocardium (Fig. 3). Coronary sinus flow was measured directly, and LIMA flow was measured by a Model lOOI-B Micron Instruments, Inc., flowmeter. Blood gas samples were obtained simultaneously from arterial and coronary sinus blood. 3. The LIMA was opened, the tourniquet around the distal LADV (Fig. 1, A) was tightened, and that around the proximal LADV released (Fig. I, B) to allow a proximal A-V shunt into the coronary sinus. A Hoffman clamp was used to partially occlude the LIMA so that the flow into the LADVcoronary sinus would be reduced to the same as that in step 2. The methods of flow and gas measurement were identical to those used in step 2. These steps were repeated at will by simply releasing and occluding one of the three
The Journal 01
276
Gardner et al.
Thoracic and Cardiovascu lar Surgery
Fig. 2. Photograph and schema of dog heart showing (A ) coron ary sinus cannula and (B) tourniquet around the coronary sinus.
sites mentioned (Fig. I, A, B, or C). At the completion of the operation, the last 4 animals had I:l1 I macroaggregated albumin (d iameter of 10 to 60 JL) injected into the LIMA. Postoperative heart and lung scans were obtained (Fig. 4). Results
I . The most significant finding was the oxygen saturation difference between the arterialized LADV and the known fistula; blood samples were taken from the coronary sinus (Table I). Measurement of this oxygen saturation difference in all dogs tested (except second series dog No.6) showed a loss in oxygen content of the blood perfusing the LADV in a retrograde manner, as compared to that of a known shunt of the same magnitude. 2. The estimated percentage of LIMA blood reaching the coronary sinus without loss of oxygen content ranged between zero and 73 per cent (Table II) as determined in Diagram I. U is the LIMA blood flow (milliliter s) reaching the coronary sinus with no loss of oxygen content ; U % is per cent of IMA blood flow reaching the coronary sinus with no loss of oxygen content; V im"
is IMA flow (in milliliters per minute); V es is coronary sinus flow (milliliters per minute) with arterialization of the LADV; Hb is animal's hemoglobin (grams per cent) ; 1.35 is milliliters of oxygen per grams per cent of hemoglobin ; S" is per cent saturation of arterial blood; S,. is per cent saturation of coronary sinus blood during arterialization of the LADV; and SI' is per cent saturation of coronary sinus blood during normal heart perfusion with occlusion of LIMA. S,. and St. were accepted for calculations when arterial saturations (Sll) were similar. 3. Table III shows the percentage of LIMA blood perfusing myocardium as determined by: % LIMA flow to myocardium =
100 - U%.
4. Radioisotope studies on the last 4 dogs showed no fistulas larger than IOJL in 3 animals (Fig. 4). (Studies in animal No. 5 were deleted because of technical problems.) Discussion
Because of the marginal successes of retrograde perfusion of the coronary sinus as described by Beck,' and because of the more recent advent of coronary bypass surgery,
Volume 68 Number 2
Arterialization of coronary veins
277
August, J974
Fig. 4. Macroaggregate albumin
13
11 heart scan.
A, injection site, left internal mammary artery. B, Distribution of left anterior descending vein.
Small arrows approximate the cardiac border. Fig. 3. Angiogram of left internal mammary artery and left anterior descending vein showing retrograde perfu sion of the heart.
little interest has been shown in this type of myocardial revascularization. Successes with retrograde perfusion during aortic valve surgery, coupled with the difficulty of treating a relatively large group of patients with severe angina, diffuse coronary artery disease, and good ventricular function who are currently nonamenable to surgery, prompted Magovern's group 2 I to reinvestigate coronary sinus perfusion as a means to increase myocardial blood supply. Consideration of this previous work done by others suggested that more success might be obtained if a limited area of myocardium were to be perfused by retrograde venous arterialization. Two overriding facts persuaded us to take this approach. I. The mortality rate was high when complete sinus arterialization was attempted, apparently because of the inability of the heart to drain off its newly found blood supply . Some early experiments had indicated that this would be true. ' 2. In all successful cases of retrograde coronary sinus perfusion during aortic valve surgery, cardiopulmonary bypass had been
employed; bypass allowed the heart to decongest itself through the coronary arteries and Thebesian veins, since these areas were not under arterial pressure. Even in these cases caution had to be exercised so that coronary sinus perfusion pressures were kept below a safe level. It seemed feasible that a more limited perfusion of a small area of the heart would eliminate these problems. The LADV was selected because of its easy accessibility and its associated, frequently sclerotic coronary artery. The surrounding veins seemed capable of handling the new blood supply because of the limited area and particularly because the artery would be supplying marginal quantities of blood. Work by Magovern'" and others" 21i confirmed the ease with which dogs tolerated the arterialization of the LADV. After the feasibility of such an approach had been proved,": 2 1 , 21i other questions arose. The possibility of a large shunt, as mentioned, seemed likely and became a main concern. In all 6 animals , blood gas analysis of coronary sinus blood confirmed that there were no large shunts . This can be shown in Table I by comparing oxygen saturations of
The Journal of
278
Gardner et al.
Thoracic and Cardiovascular Surgery
Table I
Dog No.
Weight (Kg.)
30.5
Test
LADY Fistula LADY Control LADY Control
2
27.2
LADY Fistula Control LADY Fistula Control Fistula LADY
3
24.0
Control LADY Fistula LADY Fistula
4
28.0
Control LADY Fistula Control LADY Fistula
!
pH
Po., (mm. Hg.)
O. sat.
C.S. artery C.S. artery C.S. artery C.S. artery C.S. artery C.S. artery
7.25 7.89 7.65 7.65 7.53 ·7.63 7.55 7.63 7.55 7.89 7.91 7.89
20 54 26 200 28 179 26 181 20 130 18 135
24 97 70 99 61 99 55 99 39 99 65 99
C.S. artery C.S. artery C.S. artery C.S. artery C.S. artery C.S. artery C.S. artery C.S. artery
7.39 7.39 7.43 7.39 7.45 7.47 7.41 7.49 7.38 7.48 7.39 7.48 7.41
22 101 28 70 20 83 20 131 27 53 21 53 228
38 97 47 93 34 96 33 99 52 88 35 88 100
7.39 7.41
30 88
C.S. artery C.S. artery C.S. artery C.S. artery C.S. artery
7.55 7.57 7.50 7.54 7.52 7.56 7.35 7.56 7.49 7.51
C.S. artery C.S. artery C.S. artery C.S. artery C.S. artery C.S. artery
7.42 7.48 7.43 7.50 7.46 7.46 7.47 7.51 7.44 7.45 7.43 7.41
Blood sample
I
(%)
I
IMA flow (mi.)
c.s.
flow (ml./ min.)
26
72
30
80
34
74
0
70
30
90
0
75
30
87
30
100
0
73
30
97
30
124
0
111
30
160
59 96
30
112
20 205 27 198 36 230 28 190 35 225
40 99 59 99 77 99 48 93 73 99
0
38
24
56
20
58
20
56
20
58
31 350 32 230 40 325 25 475 31 450 52 451
61 99 65 99 78 99 50 99 64 99 86 99
0
70
42
68
40
86
0
70
44
76
42
75
Legend: IMA, Internal mammary artery. C.S., Coronary sinus. LADV. Left anterior descending vein.
Volume 68
Arterialization of coronary veins
Number 2
279
August, 1974
Table I-Cont'd Po,
Dog No.
Weight (Kg.)
Test LADY Fistula
5
27.0
Control LADY Fistula Control LADY Fistula
6
20.0
LADY Fistula Control LADY Fistula Control
Blood sample
(mm. Hg.)
O. sat.
pH
C.S. artery C.S. artery
7.45 7.47 7.45 7.48
36 275 85 375
73 99 96 99
C.S. artery C.S. artery C.S. artery C.S. artery C.S. artery C.S. artery
7.48 7.53 7.52 7.51 7.51 7.52 7.54 7.55 7.52 7.58 7.38 7.45
36 132 26 105 52 103 27 103 28 112 32 98
74 99 59 98 89 98 62 98 63 99 62 97
C.S. artery C.S. artery C.S. artery C.S. artery C.S. artery C.S. artery
7.21 7.20 7.23 7.26 7.27 7.28 7.27 7.30 7.26 7.30 7.27
28 208 45 208 39 250 34 211 42 201 40 202
41 99 74 99 65 99 59 99 70 99 68 99
the coronary sinus blood during arterialization of the LADV against those of the known A-V fistula. The figures show significant differences in all dogs (except in second series dog No.5, in which the cannula appears to have been pulled into the right atrium). Table II, again, confirms the absence of large shunts. In this table, the oxygen saturation of blood from the coronary sinus of a normal heart is the base line, and figures are determined from coronary sinus flow and saturation during arterialization of LADV. Calculation of these figures is based on the amount of flow by unaltered arterial blood reaching the coronary sinus that is necessary to cause the same oxygen saturation as that found in the coronary sinus during LADV
7.30
(%)
c.s.
IMA
flow
flow (ml.)
(ml./ min.)
48
73
48
103
0
75
20
70
20
74
0
70
27
74
27
72
12
80
12
100
0
94
17
85
17
92
0
80
arterialization. This figure could represent an estimation of the largest shunt that would be possible under the given laboratory data. The figure must also represent a percentage of blood unneeded by the myocardium's metabolic demand and therefore an increase in coronary sinus blood oxygen saturation (physiologic shunting). Table II then represents a combination of fistulous blood and perfused blood not used by the myocardium. Isotope scans such as the one shown in Fig. 4 suggest more of the latter. A small fistula is not considered a problem5 . " and, in fact, may be beneficial by encouraging better patency and collaterals." Fig. 4 is a scan of the heart and lungs from animal No. 3 after the injection of macroaggregated albumin (diameter of 10 to 60p.)
The Journol of
280
Gardner et al.
Thorocic and Cardiovascular Surgery
Diagram I (V"R x Vol. % O 2 : Coronary sinus blood with arterialization of LADV)
(VCR
X
Vol. % O 2 : Coronary sinus blood, normal heart perfusion)
u=----------------------------Vol. % O 2 : Coronary sinus blood, normal heart perfusion)
(Vol. % O 2 : Arterial blood
U%
=
U%=
(Ves x Hb x 1.35 x Sv) - (Ves x Hb x 1.35 x So) (Hb x 1.35 x Sa) Ves (Sv - Se) Virna (Sa - So)
U%
1
29.7 0 17.6 0 73.0 37.0 16.6 48.0 0 0 0
2 3 4 5 6
I Average U% 14.9 8.8 55.0 32.3 0 0
Legend: U%, Per cent of internal mammary artery blood flow reaching the coronary sinus with no loss of oxygen content.
Table III. Calculated IMA-LADV flow to myocardium Dog. No.
Flow (%)
1
85.1 91.2 45.0 67.7 100.0 100.0
2 3 4 5 6
X
1.35 x Se)
1
x __•
Virna
.
Table II Dog No.
(Hb
Legend: IMA, Internal mammary artery. LADY, Left anterior descending vein.
into the LADV. This scan, which is also typical of animal Nos. 4 and 6, shows capture by the myocardium of the entire injection with no loss to the lungs. It can be concluded that no A-V fistula over lOfL in size exists in these 3 animals. Table III shows the percentage of IMALADV flow that is reduced from an arterial oxygen saturation to the level of that found in the coronary sinus in the control heart.
The supposition is that this blood perfused the myocardium and lost this volume of oxygen to the cells. Previous angiograms (Fig. 3) had demonstrated the diffusion of the flow through the myocardium, a fact that was also confirmed by isotope scan. It seems fair to conclude that the myocardium does, in fact, receive direct perfusion from the arterialized LADV. Long-term studies in dogs indicate the patency of the vessels. 21 The coronary venous system in man has fewer variations than that of dogs1 8 , 2 1 and will be a better recipient of retrograde perfusions. It would appear from these tests that LADV arterialization might be of value for patients with diffuse coronary artery disease, incapacitating angina, and good ventricular function who are not currently candidates for coronary bypass surgery. Summary
Arterialization of the LADV increased myocardial uptake of oxygen from the perfusing blood. This we determined by comparing retrograde arterial flow against flow of a known fistula. Second, the amount of oxygen lost to cardiac muscle during arterialization of the LADV was compared with that of the normal heart. These studies showed loss of oxygen content from a good portion of the new source of cardiac blood as it perfused the myocardium. These same calculations did not rule out the possibility of a small fistula and in fact did strongly suggest that one exists. The heart scans done with macro aggregate 131 1, on the other hand,
Volume 68 Number 2
Arterialization of coronary veins
28 I
August, 1974
indicated that the fistulas, if present, were small and that arterialization of the LADY perfused evenly the distribution of the LADY. Conclusion
I. Arterialization of the LADY does cause increased myocardial perfusion. 2. Arterialization of the LADY does not cause a large A-Y shunt, although the presence of a small shunt cannot be ruled out. 3. The next step is the clinical application of arterialization of the LADY in selected cases. LADV revascularization has been done in 7 patients who fit the previously discussed criteria. The results although still early are encouraging. REFERENCES I Arealis, E. G., Voider, J. G. R., and Kolff, W. J.: Communications to the Editor: Arterialization of the Coronary Vein Coming From an Ischemic Area. Chest 63: 462, 1973. 2 Bakst, A. A., Adam, A., Goldberg, H., and Bailey, C. P.: Arterialization of the Coronary Sinus in Occlusive Coronary Artery Disease, J. THORAC. SURG. 29: 188, 1954. 3 Batson, O. V., and Bellet, S.: The Reversal of Flow in the Cardiac Veins, Am. Heart 1. 6: 206, 1930. 4 Beck, C. S.; The Development of a New Blood Supply to the Heart by Operation, Ann. Surg. 102: 801, 1935. 5 Beck, C. S.: Revascularization of the Heart, Ann. Surg. 128: 854, 1948. 6 Beck, C. S.: Surgical Operations for Coronary Artery Disease, in Encyclopedia of Thoracic Surgery, vol. II, Berlin, 1959, Springer-Verlag, p. 779. 7 Beck, C. S., and Leighninger, D. S.: Operations for Coronary Artery Disease, J. A. M. A. 156: 1226, 1954. 8 Beck, C. S., Stanton, E., Batiuchok, W., and Leiter, E.: Revascularization of Heart by Graft of Systemic Artery Into Coronary Sinus, J. A. M. A. 137: 436, 1948. 9 Bhayana, J. N., Olsen, D. 8., Byrne, J. P., and Kolff, W. J.: Reversal of Myocardial Ischemia by Arterialization of the Coronary Vein, J. THORAC. CARDIOVASC. SURG. 67: 125, 1974. 10 Blanco, G., Adam, A., and Fernandez, A.: A Direct Experimental Approach to the Aortic Valve. II. Acute Retroperfusion of the
Coronary Sinus, J. THORAC. SURG. 32: 171, 1956. 11 Brown, A. H., Braimbridge, M. V., Niles, N. R., Gerbode, F., and Aguilar, M. J.: The Effect of Excessively High Perfusion Pressures on the Histology, Histochemistry, Birefringence, and Function of the Myocardium, J. THORAC. CARDIOVASC. SURG. 58: 655, 1969. 12 Brown, A. H., Niles, N. R., Braimbridge, M. V., and Austen, W. G.: Retrograde Insufflation of Gaseous Oxygen Into the Coronary Sinus as a Means of Myocardial Maintenance, Arch. Surg. 105: 622, 1972. 13 Camishion, R. C., Davies, A. L., Tokunaga, K., and Solit, R. W.: Retrograde Perfusion of the Coronary Arteries With Gaseous Oxygen During Cardiopulmonary Bypass, Surgery 59: 145, 1966. 14 Eckstein, R. W., Smith, G., Eleff, M., and Demming, J.: The Effect of Arterialization of the Coronary Sinus in Dogs on Mortality Following Acute Coronary Occlusion, Circulation 6: 16, 1952. 15 Eckstein, W. R., and Leighninger, D. S.: Chronic Effects of Aorta-Coronary Sinus Anastomosis of Beck Dogs, Circ, Res. 2: 60, 1954. 16 Favaloro, R. G., Effler, D. 8., Groves, L. K., Sheldon, W. C., Shirey, E. K., and Sones, F. M., Jr.: Severe Segmental Obstruction of the Left Coronary Artery and Its Divisions, J. THORAC. CARDIOVASC. SURG. 60: 469, 1970. 17 Feil, H.: Clinical Appraisal of the Beck Operation, Ann. Surg, 118: 807, 1943. 18 Gott, V. L., Gonzalez, J. L., Zuhdi, M. N., Varco, R. L., and Lillehei, C. W.: Retrograde Perfusion of the Coronary Sinus for Direct Vision Aortic Surgery, Surg, GynecoJ. Obstet. 104: 319, 1957. 19 Hammond, G. L., Davies, A. L., and Austen, W. G.: Retrograde Coronary Sinus Perfusion: A Method of Myocardial Protection in the Dog During Left Coronary Artery Occlusion, Ann. Surg. 166: 39, 1967. 20 Lillehei, C. W., DeWall, R. A., Gott, V. L., and Varco, R. L.: The Direct Vision Correction of Calcific Aortic Stenosis by Means of a Pump-Oxygenator and Retrograde Coronary Sinus Perfusion, Chest 30: 123, 1956. 21 Magovern, G. J., Park, S. B., Liebler, G. A., Dixon, C. M., Begg, F. R., Dosios, T., and Fisher, D. L.: Unpublished work, 1972-1973. 22 Moll, J. W., Dziatkowiak, A., Rybinski, K., Edelman, M., and Ratajczak-Pakalska, E.: Arterialisierung des sinus coronarius-s-indikationen, technik, ergebnisse, Thoraxchirurgie 21: 295, 1973. 23 Neidorf, B. S., Brest, A. N., Kasparian, H., Wiener, L., and Rafter, J. J.: Angiocardio-
The Journal of
282
Gardner et al.
graphic Assessment for Coronary Bypass Surgrey, Pa. Med. 76: 43, 1973. 24 Pratt, F. H.: The Nutrition of the Heart Through the Vessels of Thebesius and Coronary Veins, Am. 1. PhysioI. 1: 86, 1898. 25 Roberts, 1. T., Browne, H. S., and Roberts, G.: Nourishment of the Myocardium by Way
Thoracic and Cardiovascular Surgery
of the Coronary Veins, Fed. Proc. 2: 90, 1943. 26 Wiener, L.: Reversal of Acute Myocardial Ischemia by Retrograde Intercoronary Venoarterial Perfusion (abstr.), Am. J. CardioI. 33: 178, 1974.