Primary vascular anastomosis in growing pigs

J THoRAc CARDIOVASC SURG 81:921-927, 1981

Primary vascular anastomosis in growing pigs Comparison of polypropylene and polygiycolic acid sutures Stenosis remains a significant problem in vascular anastomoses performed in the growing patient. This study compares the growth of' vascular anastomoses performed with either polypropylene or polyglycolic acid sutures. End-to-end infrarenal aortic anastomoses were performed in 18 piglets. Twelve were performed with polypropylene; in six all sutures were placed in a continuous fashion (Group IA), and in the other six the posterior sutures were continuous and the anterior were interrupted (Group IB). Six anastomoses were performed with polyglycolic acid sutures placed in a continuous fashion (Group 2). The animals were killed 6 months [ollowing operation. The abdominal aorta was removed, measured, burst tested, and subjected to histologic studies. All anastomoses were patent. There were no burst failures at 300 mm Hg mean pressure. All polypropylene sutures in Group IA and the continuous portion in Group I B had straightened without breaking. Straightening without polypropylene suture breakage resulted in stricture in three Group IA anastomoses and one Group I B anastomosis; there was intraluminal polypropylene suture material in two Group IA and jive Group I B anastomoses. Bowstring formation of the straightened, continuous portion of the polypropylene suture in two Group I A anastomoses and one Group I B anastomosis resulted in adherent thrombus. Group 2 anastomoses were without stricture and were grossly indistinguishable from adjacent normal vessel. Histologic examination showed varying degrees o] chronic inflammation in the polypropylene anastomoses but negligible inflammation in the polyglvcolic acid anastomoses. These results suggest that continuous suture techniques with polypropylene in growing vessels may result in stenosis and/or thrombosis. Moreover, synthetic absorbable polyglycolic acid sutures will be (Jf' use in vascular anastomoses in growing patients and in cases in which exacting technique with minimal postsurgical inflammation may be crucial to patency.

Walter E. Pae, Jr., M.D., John A. Waldhausen, M.D., G. Allen Prophet, B.S., and William S. Pierce, M.D., Hershey, Pa.

Although the growth of a primary vascular anastomosis is influenced by the technique of anastomosis as well as by the suture material, stenosis remains a significant problem in the growing patient. With early operative repair of coarctation of the aorta, the incidence of signs of significant recoarctation varies from 7% to 35% following different surgical techniques .':" In fact, the most widely utilized method, consisting of resection of the coarctation and end-to-end anasFrom the Department of Surgery. The Milton S. Hershey Medical Center. The Pennsylvania State University, College of Medicine, Hershey, Pa. Supported in part by U.S. Public Health Service Grant F32HL05994. Received for publication Oct. 6, 1980. Accepted for publication Dec. 2, 1980. Address for reprints: John A. Waldhausen, M.D., The Milton S. Hershey Medical Center, The Pennsylvania State University, College of Medicine, 500 University Dr., Hershey, Pa. 17033.

tomosis, has been associated with an incidence of recoarctation varying from 20% to 35%.2, 4. 6-H The present study was undertaken to compare the effects of polypropylene and polyglycolic acid sutures and two standard anastomotic techniques performed with polypropylene sutures on the subsequent growth of the infrarenal aorta in piglets.

Materials and methods Eighteen piglets (body weight 13.6 ± 3.1 kg SO) were anesthetized with a mixture of halothane and oxygen. Following endotracheal intubation, an incision was made in the left retroperitoneal flank, the infrarenal abdominal aorta was exposed, and its external diameter was measured. The animals were anticoagulated with heparin, and an end-to-end anastomosis of the infrarenal abdominal aorta was performed. The site of anastomosis was then marked by a nonabsorbable suture in order for precise identification of the anastomosis to be

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Reservoir (saline)

Fig. 1. Apparatus utilized for burst testing the aorta. The flow was kept constant via the roller pump and resistance was increased with the variable clamp until 300 mm Hg pressure was applied or the vessel burst.

Fig. 3. Photomicrograph of a hematoxylin and eosin stained specimen removed from pig No. 58. Nonabsorbable polypropylene suture is seen with minimal surrounding inflammation. This is the least reaction seen with polypropylene in our study. (Original magnification x 225.)

Fig. 2. Macrophotograph of the aorta removed from pig No. 57 shows intimal roughening and intraluminal polypropylene suture material. Although no stricture was found. wellorganized thrombus is seen adherent to the intraluminal suture, which was bowstrung across the lumen. made at future necropsy. All anastomoses were performed with 6-0 diameter suture materials (polypropylene or polyglycolic acid) with the aid of 2.5 power magnification loupes. Twelve anastomoses were performed with monofilament polypropylene suture; in six all sutures were placed in a continuous fashion (Group IA), whereas in the other six the posterior sutures were continuous and the anterior ones were interrupted (Group IB). For the other six anastomoses, polyglycolic acid sutures, placed in a continuous fashion,

were employed (Group 2). The animals were returned to cages until skin wounds were healed and then they were placed in free range pens. Approximately 6 months following operation they were put to death (body weight 108.7 ± 13.2 kg SD). The abdominal aorta was carefully excised and the branches were ligated. The vessels were then filled with a water-soluble roentgenographic contrast material at a mean pressure of 100 mm Hg. At this pressure the external diameters were determined proximal (I ern) to the anastomotic site, at the site, and distal (1 em) to the site. Roentgenography was then performed. Following this, burst testing was carried out with a roller pump (Fig. 1). Intraluminal pressure was raised until either the vessel burst or a mean pressure of 300 mm Hg was reached. Photographs of the gross specimens were taken. The specimens were fixed in formalin for light microscopy and were stained with hematoxylin and eosin and standard elastin stains.

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Fig. 4. Photomicrograph of an elastin stained specimen from pig No. 58. Disruption of the architecture of the tunica media is seen at the area of the anastomosis. The intima overlying the suture is heaped up. (Original magnification x 100.)

Table I. Group JA: Polypropylene suture-continuous technique At operation

Pig No.

Weight (kg)

Aortic external diameter * (mm)

52 81 51 57 88 58

10.0 13.6 18.2 14.1 17.3 10.5

6.0 8.0 7.0 7.0 8.0 6.0

* Measurement

At sacrifice External aortic diameter

Aortic area * (mmi)

Weight (kg)

28.3 50.3 38.5 38.5 50.3 28.3

104.5 122.7 128.2 118.2 105.9 113.6

1 em prox- I Anastomoimal (mm) sis (mm)

15.0 17.0 15.5 15.0 14.0 15.0

12.5 16.0 12.5 15.0 14.0 15.0

Aortic area

1 1 em dis-

tal (mm)

Average areat (mm')

15.0 17.0 15.5 15.0 14.0 15.0

176.7 226.9 188.7 176.7 153.9 176.7

I

Anastomosis (mm')

122.7 201. I 122.7 176.7 153.9 176.7

I

Stricture" (%)

30.6 11.4 34.9 0.0 0.0 0.0

taken at anastomotic site.

t Average area = (area I em proximal + I em distal to anastomosis) -;- 2.

Results Approximately 6 months following operation the weight of the animals had increased to a mean of 800% of the operative weight (13.6 ± 3.1 kg SO to 108.7 ± 13.2 kg SO). There were no postoperative complications or deaths. All anastomoses were patent and no vessel failed burst testing at 300 mm Hg pressure. However, certain important differences were seen among the groups and these will be discussed individually. Group lA: Monofilament polypropylene suturecontinuous technique. Stricture was evident in three (pig Nos. 51, 52, and 81) of the six anastomoses (Table

I). Intraluminal polypropylene suture material was seen and the intimal surface was noted to be grossly roughened in two of six anastomoses (Fig. 2). Bowstring formation of a portion of the continuous polypropylene suture in these two anastomoses (pig Nos. 52 and 57) resulted in adherent thrombus (Fig. 2). Notably, the continuous polypropylene suture had straightened in all six anastomoses in this group. Light microscopy of the specimens demonstrated varying degrees of chronic inflammation about the polypropylene material and anastomotic site (Fig. 3). Some narrowing of the tunica media was present and architectural disruption appeared severe (Fig. 4).

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Fig. 5. A. Macrophotograph of specimen removed from pig No. 67. The continuous portion of the suture on the left is straightened and intraluminal. Roughening of the intima as well as gross evidence of inflammation surrounding the interrupted portion of the anastomosis is apparent. B. Macrophotograph of specimen removed from pig No. 68. The continuous portion of the polypropylene suture is bowstrung across the lumen. Wellorganized thrombus adherent to the suture is seen.

Table II. Group JB: Polypropylene suture -anterior interrupted and posterior continuous technique At operation

Pig No.

Weight (kg)

Aortic external diameter* (mm)

66

10.0 10.9 15.5 10.9 13.6 12.8

7.0 6.0 7.0 6.0 8.0 6.0

64

67 65 68 60

At sacrifice External aortic diameter

Aortic area * (mm'}

Weight (kg)

1 cm proximal (mm)

38.5 28.3 38.5 28.3 50.3 28.3

90.0 121.8 95.5 107.7 107.3 92.3

18.0 15.0 13.0 14.0 14.0 14.0

I Anastomosis (mm)

Aortic area

11 cm distal (mm)

Average areat (mm']

18.0 15.0 13.0 14.0 14.0 14.0

254.5 176.7 132.7 153.9 153.9 153.9

13.5 15.0 13.0 14.0 14.0 14.0

I

Anastomosis (mmi)

StricI ture*

(%)

143.1 176.7 132.7 153.9 153.9 153.9

43.8 0.0 0.0 0.0 0.0 0.0

• Measurement taken at anastomotic site.

t Average area = (area 1 em proximal + I em distal to anastomosis) + 2.

Table III. Group 2: Polyglycolic acid sutures-continuous technique At operation

Pig No.

Weight (kg)

Aortic external diameter * (mm)

59 61 53 62 55 63

20.0 13.2 16.8 15.0 14.1 9.0

7.0 7.0 8.0 7.0 7.0 7.5

At sacrifice External aortic diameter

Aortic area * (mmi)

Weight (kg)

1 em proximal (mm)

38.5 38.5 50.3 38.5 38.5 44.2

128.2 99.1 128.2 103.2 91.8 99.1

16.0 14.0 17.0 14.0 14.0 16.0

* Measurement taken at anastomotic site. t Average area = (area 1 em proximal + I em distal to anastomosis) + 2.

I Anastomosis (mm) 16.0 14.0 17.0 14.0 14.0 16.0

Aortic area

11 em distal (mm)

Average areat (mm']

16.0 14.0 17.0 14.0 14.0 16.0

201.1 153.9 226.9 153.9 153.9 201.1

I

Anastomosis (mmi) 201.1 153.9 226.9 153.9 153.9 201.1

I

Stric-

ture" (%) 0.0 0.0 0.0 0.0 0.0 0.0

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Fig. 6. Macrophotograph of the aorta removed from pig No. 57 demonstrates the smooth intimal lining seen with polyglycolic suture anastomoses. No suturematerial is visible and the anastomosis is difficult to distinguish from adjacent normal vessel. Group IB: Monofilament polypropylene sutureposterior row continuous and anterior row interrupted technique. Stricture was apparent in one of the six anastomoses (pig No. 66) (Table II). Intraluminal polypropylene suture material and intimal roughening was evident in five of six anastomoses, a more frequent phenomenon than seen with the pure continuous technique of Group lA (Fig. 5A). Bowstring formation of the continuous portion of the polypropylene suture resulted in adherent thrombus in one of the six anastomoses (pig No. 68) (Fig. 5B). Additionally, the posterior continuous row of polypropylene suture had straightened in all six anastomoses (Fig. 5A). Light microscopy demonstrated findings similar to those in Group lA, although inflammation seemed more intense, presumably secondary to the greater amount of suture material present. Group 2: Polyglycolic acid suture-continuous technique. No strictures were found in anastomoses in this group (Table III). Suture material was not visible and the intimal surface about the suture line appeared grossly nearly identical to the normal adjacent vessel (Fig. 6). Light microscopy failed to demonstrate residual suture material and, in contrast to Groups lA and lB, chronic inflammation was negligible and architectural disarray was less marked (Figs. 7A and 7B). Discussion For many years, nonabsorbable sutures have been the standard material for vascular anastomoses. In the

Fig. 7A. Photomicrograph of a hematoxylin and eosin stained specimen from pig No. 63. The only evidence of previous suturingis this ovoid fibrous reaction. (Original magnification

x 100.)

early 1950s, several groups suggested that continuous sutures be used for the posterior row and interrupted sutures for the anterior row when a vascular anastomosis is performed in a growing patient. 9-11 Such a technique permits a hemostatic posterior row with the potential for enlargement of the anterior row as the child grows. However, this technique has serious shortcomings, perhaps most apparent in the results following repair of coarctation in infants, wherein the recoarctation rate has been as high as 35% in certain series.": 7. 8 Our study documents some of the complications that may result from the use of nonabsorbable suture material for vascular anastomoses where growth is required. The studies were performed with the monofilament polypropylene suture, a nonabsorbable material which is widely used at present because of its low drag and freedom from interstices. Use of a continuous technique with the polypropylene suture resulted in stenosis in three of six animals and intraluminal suture material with adherent thrombus in two of six animals. Use of the more commonly accepted technique with a continuous posterior row and an interrupted anterior row was associated with stenosis in only one of six animals, but again, intraluminal suture and adherent thrombus were

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Fig. 7B. Photomicrograph of the same specimen stained for elastin illustrates the smooth intima and minimal architectural disarray in the area of the anastomosis. (Original magnification x 100.)

observed. These results with nonabsorbable polypropylene sutures illustrate that stenosis and/or bowstring formation with subsequent thrombosis may occur during growth if the diameter of the vessel exceeds the maximum length of the straightened suture material. 11 Moreover, considerable inflammatory reaction and intimal roughening will occur. It appears at present that all nonabsorbable sutures, including monofilament polypropylene as employed in this study, inevitably cause some degree of chronic inflammation that may contribute to restenosis or thrombus formation. 12 Thus the results of vascular anastomosis performed by standard "clinical" techniques in the growing pig indicate considerable room for improvement. Our study did not include vascular anastomoses performed solely with an interrupted suture technique because this method is not often employed to suture growing arteries. Absorbable suture such as chromic catgut has been employed for vascular anastomoses in growing animals with good results." 11-13 The absorbable nature of the gut suture eliminates any restraining bands or intraluminal material. Moreover, the inflammatory response has been less marked than that generally seen with nonabsorbable sutures.?: II, 13, 14 However, absorbable chromic catgut has not been accepted for use in clinical vascular operations because of concern that the material would disintegrate before the anastomosis had become strong enough. 14 Nonetheless, several case reports describing satisfactory use of chromic catgut in the repair of coarctation of the aorta and in construction of splenorenal shunts in the growing patient have appeared which verified the animal data. 12 The introduction of polyglycolic acid suture has provided an absorbable material with greater tensile strength and a slower, more controlled absorption rate

than chromic catgut. The only technical disadvantage of the polyglycolic acid suture as compared to synthetic nonabsorbable materials is the higher tissue drag. In our study, the use of polyglycolic acid suture for vascular anastomosis in the growing pig resulted in no stricture formation, a smooth intimal lining without residual intraluminal material, minimal inflammation, and a strong vessel as evidenced by no burst failures. Polyglycolic acid suture provides excellent results in anastomoses where vascular growth is required. Moreover, the results are considerably better than are those obtained with monofilament polypropylene suture. Similar conclusions have been drawn by several other groups in comparing polyglycolic acid suture with braided silk or Dacron suture.P""? Interestingly, although we are not aware of the clinical use of polyglycolic acid suture for vascular anastomosis in this country, it has been employed abroad with satisfactory results." REFERENCES Fishman NH, Bronstein MH, Berman W Jr, Roe BB, Edmunds LH Jr, Robinson SJ, Rudolph AM: Surgical management of severe aortic coarctation and interrupted aortic arch in neonates. J THORAC CARD10VASC SURG 71:35-48, 1976 2 Hartmann AF Jr, Goldring D, Hernandez A, 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 3 Rue1 GJ Jr, Kabbani SS, Sandiford FM, Wukasch DC, Cooley DA: Repair of coarctation of the thoracic aorta by patch graft aortoplasty. J THORAC CARDIOVASC SURG 68: 696-704, 1974 4 Shinebourne EA, Tam ASY, Elseed AM, Paneth M, Lennox SC, Cleland WP, Lincoln C, Joseph MC, Ander-

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son RH: Coarctation of the aorta in infancy and childhood. Br Heart J 38:375-380, 1976 Tawes RL Jr, Aberdeen E, Waterson DJ, Bonham-Carter RE: Coarctation of the aorta in infants and children. A review of 333 operative cases, including 179 infants. Circulation 39, 40:Suppl I: 173-184, 1969 Ibarra-Perez C, Castaneda AR, Varco 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 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 Johnson J, Kirby CK, Allam MW, Hagan W: The growth of vascular anastomoses with continuous posterior and interrupted anterior silk sutures. Surgery 29:721-725, 1951 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

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factors involved. Bull Johns Hopkins Hosp 91:276-297, 1952 Deterling RA Jr, Coleman CC Jr, Kee J, Humphreys GH: An experimental evaluation of catgut as a vascular suture material and a report on its clinical use. J THORAC SURG 23:303-326, 1952 Tawes RL Jr, Aberdeen E, Berry CL: The growth of an aortic anastomosis. An experimental study in piglets. Surgery 64:1122-1132,1968 Sako Y, Chisholm TC, Merendino KA, Varco RL: An experimental evaluation of certain methods of suturing of the thoracic aorta. Ann Surg 130:363-383, 1949 Alvarez-Cordero R, Reyes EI, Alcazar MG, HernandezJauregui P: Evaluation of polyglycolic acid sutures in vascular surgery. J Surg Research 15:35-44, 1973 Dardik H, Dardik I, Katz AR, Smith RB, Schwibner BH, Laufman H: A new absorbable synthetic suture in growing and adult primary vascular anastomoses. Morphologic study. Surgery 68:1112-1121,1970 Watts DR, Carr SH, Hohf RP: Poly(Glycolic acid) sutures in canine vascular anastomoses. J Biomed Mater Res 10:867-877, 1976 Kuo TP, Huang TJ, Howng SL: The clinical use of synthetic absorbable suture in vascular surgery. J Formosan Med Assoc 73:45-52, 1974