J
THORAC CARDIOVASC SURG
82:922-927, 1981
Subclavian flap angioplasty Experimental study in growing piglets Persistent stenosis or recoarctation remains the major long-term complication of repair of coarctation of the aorta in infancy. This present study was undertaken to observe the growth of the thoracic aorta in piglets following subclavian flap angioplasty across normal and abnormal retained aortic segments utilizing two conventional suturing techniques. Subclavian flap angioplasty was performed with 6-0 monofilament polypropylene in 12 piglets (body weight 13.3 ± 2.3 kg SD) after measuring the aortic diameter and excising 50% of the aortic wall to simulate an aortic coarctation. In six piglets the medial and lateral sides of the subclavian flap were sewn into the aorta by means of a continuous suture technique (Group /); in the remaining animals suture lines were completed with an interrupted technique (Group II). In three animals in each group the remaining aortic isthmus was injected circumferentially and intramurally with a 10% neutral buffered formalin solution to simulate an abnormal aortic wall. The animals were killed 6 months following operation when their weight had increased eightfold. The thoracic aorta was excised, aortography was performed under high pressure, and the vessel diameters were measured. Burst testing for strength was carried out and photographs were made. There were no postoperative complications or deaths. All anastomoses were patent, and all vessels withstood burst testing at 300 mm Hg mean pressure. No hemodynamically significant strictures were seen in either group. with the greatest reduction and in diameter being 36%. However, in Group I animals intraluminal suture material was associated with adherent thrombus in one animal. These results indicate that. regardless of the suture technique or the growth potential of the retained aortic segment after subclavian flap angioplasty , subsequent satisfactory growth of the aortic area will occur. A strong. nonstenotic vessel results. However, the use of continuous suture technique in fashioning the subclavian flap angioplasty should be avoided. since suture material may erode into the lumen and may form a nidus for thrombus generation.
Walter E. Pae, Jr., M.D., John L. Myers, M.D., John A. Waldhausen, M.D., G. Allen Prophet, B.S., and William S. Pierce, M.D., Hershey, Pa.
Infants with medically refractory congestive heart failure and coarctation of the aorta require prompt operative intervention. Unfortunately, persistent stenosis or recoarctation remains the major long-term complication of the aortic reconstruction in infancy. In the past, the most widely utilized method of repair, consisting of resection of the coarctation and 'end-to-end anastomosis, has been associated with a reported incidence
From the Division of Cardiothoracic Surgery, Department of Surgery, The Milton S. Hershey Medical Center, The Pennsylvania State University, Hershey, Pa. Received for publication April 6, 1981. Accepted for publication April 29, 1981. Address for reprints: John A. Waldhausen, M.D., Department of Surgery, College of Medicine, The Milton S. Hershey Medical Center, The Pennsylvania State University, Hershey, Pa. 17033.
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of recoarctation varying from 20% to 35%.1-5 To reduce this complication Waldhausen and Nahrwold" described in 1966 the technique of aortoplasty with a viable left subclavian artery flap. With this method of repair aortic growth is not dependent on the growth of the anastomoses in an area of possibly abnormal tissue. Thus the incidence of recoarctation should be reduced or eliminated. Several retrospective clinical studies of infant coarctation repair utilizing the subclavian flap technique appear to have confirmed this, but basic animal experimental data have been produced only sparingly.?"? This present study was undertaken to observe the luminal growth of the thoracic aorta in piglets after partial excision of the aortic wall and repair using the subclavian flap technique and to determine whether the use of a continuous or interrupted suture technique affects this growth.
0022-5223/81/120922+06$00.60/0 © 1981 The C. V. Mosby Co.
Volume 82 Number 6 December, 1981
A.
Fig. 1. A, Position of proposed thoracotomy incision in left third intercostal space. B, Vascular clamps have been placed proximally and distally on the aorta. The subclavian artery has been ligated; the proposed line of incision of the subclavian artery and aorta is indicated by the dashed line. C, Incison of the subclavian artery and aorta has been completed. The hatched area within the dashed lines indicates the proposed amount of aorta to be excised to simulate aortic coarctation and accommodate the subclavian flap.
Materials and methods Twelve piglets (body weight 13.3 ± 2.3 kg SD) were anesthetized with a mixture of halothane and oxygen. Following endotracheal intubation, a thoracotomy was performed in the left third intercostal space (Fig. 1, A). After incision of the pleura the left subclavian artery and adjacent aorta were exposed and the aortic diameter at the level of the isthmus was measured. Tapes were placed around the left subclavian artery, distal aortic arch, and descending thoracic aorta. The subclavian artery was then ligated at the origin of the vertebral artery, the ligature also including the latter artery to prevent the subclavian steal phenomenon (Fig. 1, B). Vascular clamps were placed across the aorta just distal to the brachiocephalic trunk and just below the ligamentum arteriosum. The distal end of the subclavian artery was divided and incised in line with the anterolateral aspect of the aorta (Fig. 1,B). This incision was then carried into the aorta a distance equal to the length of the left subclavian artery segment. Fifty percent of the aortic wall was excised to simulate an aortic coarctation (Fig.
Subclavian flap angioplasty
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Brach iocephal ic arte ry
Fig. 2. The completed subclavian flap utilizingan interrupted technique of 6-0 monofilament polypropylene is depicted (Group II). In Group I the subclavianflap was fashioned with a continuous 6-0 monofilament polypropylene (not shown). 1, C). The midpoint of the divided end of the left subclavian flap was sutured to the caudal point of the aortic incision with a 6-0 polypropylene monofilament suture. In six piglets the medial and lateral sides of the subclavian flap were sewn into the aorta with a continuous suture technique (Group I); in the remaining six piglets the medial and lateral suture lines were completed with an interrupted technique (Group II) (Fig. 2). All anastomoses were performed with the aid of 2.5 power magnification loupes. Additionally, randomly in one half of the animals in each group the remaining aortic isthmus was injected circumferentially and intramurally with a 10% neutral buffered formalin (colored with methylene blue for visibility) to simulate an abnormal aortic wall that may be seen in coarctation of the aorta. The animals were returned to cages until the skin wounds were healed, and then placed in pens until approximately 6 months following operation. When their weight had generally increased eightfold they were killed. The entire thoracic aorta was carefully excised and all the side branches were ligated. The vessels were then filled with a water-soluble roentgenographic contrast material and pressurized to 100 mm Hg mean pressure; roentgenography was performed and internal diameters were determined at the midpoint of the subclavian flap
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924 Pae et al.
Fig. 3. Radiograph of specimen removed from Pig No. 23 (formalin injected). The vessel was fiIled with water-soluble roentgenographic contrast material and pressurized to 100 mm Hg mean pressure. The approximate midpoint of the subclavian flap is indicated by the arrow. The angioplastic segment is not strictured and in fact is relatively larger than the aorta distaIly. repair as well as 1 em proximal and distal to this midpoint. Roentgenographic measurements were corrected for magnification. Following this, burst testing was performed with a pressure testing apparatus previously described. 10 Intraluminal pressure was raised until burst failure occurred or a mean pressure of 300 mm Hg was reached. Photographs of the gross specimens were taken. Results All piglets survived operation and grew normally. At approximately 6 months postoperatively the mean weight had increased 835% from an operative weight of 13.3 ± 2.3 kg (SD) to 124.4 ± 15.0 kg (SD). There were no postoperative complications or deaths. All anastomoses were patent, and all vessels withstood burst testing at 300 mm Hg mean pressure. Group I: Subclavian flap repair; continuous suture technique. The results after 6 months are summarized in Table I. In four ofthe six pigs (nos. 28,23,24,
Thoracic and Cardiovascular Surgery
FIg. 4. Gross specimen removed from Pig No. 24. The specimen has been opened in a manner to best illustrate bowstringing of the monofilment polypropylene. A smaIl thrombus is adherent to the intraluminal suture material and the intima is roughened. The arrow marks the apex of the subclavian flap with the proximal aorta at the top of the photograph.
and 19) there were no strictures; in these pigs the angioplastic segments were relatively larger than the aorta I em distally (Fig. 3). This occurred despite formalin injection in three of the pigs (Nos. 28,23, and 24), as well as in one pig not injected with formalin (No. 19). In the remaining two pigs in this group (Nos. 26 and 25), neither of which had been formalin injected, reduction in the cross-sectional area of 46% and 42% occurred, respectively. These stenoses were not sufficiently severe enough to produce pressure gradients but were obvious angiographically. Interestingly, intraluminal suture material was seen in two of six pigs (Nos. 24 and 26), and in Pig No. 24 a small thrombus was adherent to the intraluminal suture material (Fig. 4). Group II: Subclavian flap repair; interrupted suture technique. Table II summarizes the results in this group. In four of the six pigs (Nos. 30, 32,20, and 21)
Volume 82 Number 6 December, 1981
Subclavian flap angioplasty
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Table I. Group I: Subclavian flap; polypropylene suture; continuous suture technique At death
Pig No. 28§ 23§ 24§ 26 25 19
I
At operation
Weight Aortic external* (kg) diameter (mm) 10.0 10.0 15.5 12.2 16.8 12.3
I
12.0 12.0 12.0 11.0 11.0 11.0
Aortic area* (mmt}
Weight (kg)
113.0 113.0 113.0 95.0 95.0 95.0
143.2 92.7 132.7 125.0 121.8 120.0
I
Internal aortic diameter
Proximal I em (mm)
I
Anastomo-I Distal sis* (mm) 1 em (mm)
23.5 30.0 33.0 23.5 22.0 17.5
21.5 30.0 33.0 17.5 18.0 17.5
16.5 27.5 32.5 24.0 25.0 14.0
I
Aortic area
Averaget Anastomo./ Change at anas(mm 2) sis* (mmi} tomosisx (%) 323.6 650.1 842.0 442.8 435.2 197.1
362.9 706.5 854.9 240.4 254.3 240.4
+12 +9 +2 -46 -42 +22
• Measurement taken at the midpoint of subclavian flap. = (area I cm proximal + 1 cm distal to midpoint of subclavian flap) + 2. Percent relative enlargement (+) or percent relative reduction (-) in cross-sectional area compared to average aortic area. § Ten percent formalin injection of aortic remnant.
t Average area
*
Table II. Group II: Subclavian flap; polypropylene suture; interrupted suture technique At death
Pig No. 27§ 30§ 32§ 20 21 22
I
At operation
Weight Aortic external* (kg) diameter (mm) 13.6 12.5 12.3 16.4 12.7 13.8
* Measurement
12.0 12.0 10.0 12.0 12.0 12.0
I
Aortic area* (mm 2)
Weight (kg)
113.0 113.0 100.1 113.0 113.0 113.0
133.2 140.0 105.5 117.7 131.8 129.5
I
Internal aortic diameter
Proximal I em (mm) 17.5 14.0 26.0 19.5 20.0 18.0
I
Anastomo-I Distal sis* (mm) I em (mm) 11.0 14.0 25.0 19.0 20.0 15.0
17.0 11.0 22.0 15.0 16.0 15.0
I
Aortic area
Averaget Anastomo./ Change at anas(mmi] sis* (mm') tomosist (%) 233.6 124.4 455.3 237.6 257.5 215.5
95.0 153.9 490.6 283.4 314.0 176.6
-59 +24 +8 +19 +22 -18
taken at the midpoint of subclavian flap.
t Average area = (area I cm proximal + I cm distal to midpoint of subclavian flap) + 2.
*
Percent relative enlargement (+) or percent relative reduction (-) in cross-sectional area compared to average aortic area. § Ten percent formalin injection of aortic remnant.
there were no strictures, and again the angioplastic segments were larger than the aorta 1 ern distally (Fig. 5). Again, this occurred despite formalin injection in two of the three pigs (Nos. 30 and 32). In the remaining two pigs in this group (Nos. 27 and 22) reduction in the cross-sectional area of 59% and 18% occurred, respectively. The severest reduction in cross-sectional area occurred in Pig No. 27, which had been formalin injected. In contrast to Group I, intraluminal suture material was seen in only one of six pigs (No 32), and no adherent thrombus was observed. Discussion
The mechanism of recoarctation following successful repair of coarctation in infancy is unclear. Possible causes that have been implicated include incomplete relief of the coarctation, failure of the anastomosis to grow, as well as tension on the suture line. 1, 6 Previous experiments in circumferential anastomosis in piglets
with the use of nonabsorbable sutures showed the failure of the anastomosis to groW. I O- 14 The subclavian flap angioplasty represents the one surgical technique that theoretically should completely eliminate residual stenosis. Future growth should not depend entirely on the growth of the retained aortic segment since the pedicled subclavian flap is a viable angioplastic tissue. Furthermore, since the sutures are longitudinally rather than circumferentially oriented, lack of suture line growth should have little influence on circumferential growth. 6. 7 Clinical results with this technique have been excellent, but animal data have not been complete. Erath and associates" did show that the subclavian flap technique did allow for growth in the puppy. However, aortic growth in the dog is far less than that of the pig. 12 • 14 The growth of the pig aorta between the ages of 6 weeks and 6 months is comparable to the increase in the size of the aorta in the growing child. 14. 15 Furthermore, the histology of the pig's aorta closely
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The Journal of
Pae et at.
Thoracic and Cardiovascular Surgery
whether formalin was injected or not. Indeed, the severest reduction in cross-sectional area in our series was 59% and represents only a 36% reduction in diameter of the lumen. Furthermore, the technique of suturing, whether interrupted or continuous, did not affect the outcome since no hemodynamically significant stenoses were evident in either group. The incidence of insignificant stenoses (Group I, two out of six; Group II, three out of six) was not statistically different and can readily be explained by difference in the surgeon's technique. Precise attention must be given to suture placement to ensure the most favorable result. The most important difference between Group I and Group II was in the occurrence of intraluminal suture material in two of six versus one of six animals, respectively, and the observation of adherent thrombus to a loop of straightened continuous suture material in one animal in Group I. This phenomenon has been observed in end-to-end aortic anastomoses in growing piglets when a continuous monofilament suture material was utilized for anastomoses.I" This might be expected where growth of the suture line exceeds the length of the straightened suture material. 3 This represents a potential hazard in utilizing the continuous suture technique in any form of anastomoses subject to growth. Last, the use of a subclavian flap angioplasty results in a strong vessel as evidenced by no burst failures in this series. Fig. 5. Photograph of gross specimen removed from Pig No. 21 (no formalin injection). The subclavian flap was constructed with a simple interrupted technique of 6-0 polypropylene. The proximal aorta is at the top. Note that the subclavian flap makes up approximately50% of the aortic width. The intima is relatively smooth.
resembles that of a human being. 16 The use of a 10% formalin injection of the retained aortic segment, randomly in one half of the animals in each group of experimental animals, further allows observation of aortic growth should the retained segment not grow at the expected rate." Since it has been previously documented that the growth of anastomoses is also dependent on suture technique, it was important to evaluate two clinical suture techniques (continuous and interrupted) in order to eliminate variants based on technical factors. 10-14 Our study confirms in this animal model that the subclavian flap angioplasty used clinically will bridge the tissue at the aortic coarctation and continue to grow regardless of the growth potential (normal or abnormal) of the retained aorta. This was clear in that no hemodynamically significant strictures (cross-sectional area reduction of 75% or more) were present in either group
2 3 4 5
6 7
8
REFERENCES Hartmann AF Jr, Goldring D, HernandezA, Behrer MR, Schad N, Ferguson T, Burford T, Crawford C: Recurrent coarctation of the aorta after successful repair in infancy. Am J Cardiol 25:405-410, 1970 Ibarra-Perez C, Castaneda AR, Yarco RL, Lillehei CW: Recoarctation of the aorta. Nineteen year clinical experience. Am J Cardiol 23:778-784, 1969 Lindesmith GG, Stanton RE, Stiles QR, Meyer BW, Jones JC: Coarctation of the thoracic aorta. Ann Thorac Surg 11:482-497, 1971 Pelletier C, Davignon A, Ethier MF, Stanley P: Coarctation of the aorta in infancy. Postoperative follow-up. J THoRAc CARDIOVASC SURG 57:171-179, 1969 Shinebourne EA, Tam ASY, Elseed AM, Paneth M, Lennox SC, Cleland WP, Lincoln C, Joseph MC, Anderson RH: Coarctation of the aorta in infancy and childhood. Br Heart J 38:375-380, 1976 Waldhausen JA, Nahrwold DL: Repair of coarctation of the aorta with a subclavian flap. J THORAC CARDIOVASC SURG 51:532-533, 1966 Pierce WS, WaldhausenJA, BermanWB Jr, Whitman Y: Late results of the subclavian flap procedure in infants with coarctation of the thoracic aorta. Circulation 58:Suppl 1:78-82, 1978 Hamilton 01, DiEvsanio G, Sandrasagra FA, Donnelly
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RJ: Early and late results of aortoplasty with a left subclavian flap for coarctation of the aorta in infancy. J THORAC CARDIOVASC SURG 75:699-704, 1978 Erath HG, Jr, Starnes VA, Davidson IT, Bender HW Jr, Hammon JW Jr: Comparison of anastomotic growth with subclavian artery flap angioplasty and end-to-end aortic anastomosis. Surg Forum 33:245-247, 1980 Pae WE Jr, Waldhausen JA, Prophet GA, Pierce WS: Primary vascular anastomosis in growing pigs. A comparison of polypropylene and polyglycolic acid sutures. J THORAC CARDIOVASC SURG 81:921-927, 1981 Sako Y, Chisholm TC, Merindino KA, Varco RL: An experimental evaluation of certain methods of suturing of the thoracic aorta. Ann Surg 130:363-383, 1949 Johnson J, Kirby CK; The relationship of the method of suture to the growth of end-to-end arterial anastomoses. Surgery 27:17-25, 1950
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13 Sauvage LR, Harkins HN, Growth of vascular anastomoses. An experimental study of the influence of suture type and suture method with a note on certain mechanical factors involved. Johns Hopkins Med J 91:276-297, 1952 14 Tawes RL Jr, Aberdeen E, Berry CL: The growth of an aortic anastomosis. An experimental study in piglets. Surgery 64: 1122-1132, 1968 15 Moss AJ, Adams FH, O'Loughlin BJ, Dixon WJz;The growth of the normal aorta and of the anastomotic site in infants following surgical resection of coarctation of the aorta. Circulation 19:338-349, 1959 16 Detweiler DK: Swine in Biomedical Research, LK Bustad, RO McClellan, eds., Richland, Washington, 1966, Battelle Memorial Institute, Pacifica Northwest Laboratories, p 301