The biologic fate of Dacron double velour vascular prostheses —A clinicopathological study—

The Biologic Fate of Dacron Double Velour Vascular Prostheses - -A Clinicopathological Study--

Osamu SATO, Yusuke TaDA and Atsuhiko TAKAGI

ABSTRACT: Thirty-one Dacron double velour prostheses removed from 16 patients were studied microscopically in order to elucidate the changes they underwent following implantation. The process of incorporation was divided into three phases. In the initial phase, immediately following the implantation, the prostheses became surrounded by a fibrin meshwork. In the organizing phase, which sets in 10 weeks after the implantation, there was an external fibrous capsular formation around the initially fibrin- infiltrated grafts. There was also fibroblastic ingrowth and granulation formation among the interstices and the prostheses showed firm adhesion to the surrounding tissues. One year following the implantation, after most of the luminal surfaces had been covered with collagen tissues, the cellular infiltration subsided and the graft passed into the stable phase. Foreign body giant ceils and lymphocytes were seen throughout the study period. These prostheses were then compared with other prostheses which do not have velour structures. The nonvelour grafts showed less adhesion to the surrounding tissues. Microscopically, cellular reaction and collagenous ingrowth were also less. The velour surface thus seems to stimulate granulation ingrowth and to contribute to the firm adhesion of the graft to the surrounding tissues. This firm adhesion enhances resistance to infection and is considered safer in case of suture aneurysm formation.

KEY WORDS: double velour graft, healing of vascular prosthesis, graft infection, suture line aneurysm

INTRODUCTION

The first successful aortic reconstructive operations were separately reported in 1952 by Schafer and Hardin ~ and Dubost et a13 Not until after the innovative development of synthetic vascular prostheses, however, did aortic reconstruction become prevalent

The Second Department of Surgery, Faculty of Medicine, The University of Tokyo, Tokyo, Japan

Reprint requests to: Osamu Sato, MD, The Second Department of Surgery, Faculty of Medicine, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo l l 3, Japan

worldwide. The first use of cloth tubes made from Vinyon-N was reported by Voorhees et al? Thereafter, various kinds of materials were tried experimentally and clinically, but today Dacron continues to be used almost solely, in both knitted and woven vascular prostheses.* In 1967, Hall et al? proposed the use of internal velour grafts and in 1971, Sauvage et al? reported the successful fabri- cation of external velour grafts based on his trellis concept. Currently, double velour Dacron prostheses are popularly used for abdominal aortic reconstruction. Although some available reports deal with the healing. process of double velour grafts in experi-

JAPANESE JOUe.NAL OF SURGERY, VOL 19, No. 3 pp. 301-311, 1989

302 Sato et al.

mental animals, ~-1~ the gross and histologi- cal changes surrounding these grafts in man have not hitherto been elucidated. The double-velour structures have aimed to em- body several of the more ideal characteristics of vascular prostheses, however, because more than a decade has passed since their introduction, it is necessary to elucidate their clinical evaluation. Reported herein is a clinicopathological study of clinically applied double velour knitted Dacron grafts.

MATERIALS AND METHODS

Eight specimens from six patients (A2, A3, B4, C10, H18, H22, I26, and K31) were fixed in 2.5 per cent glutal aldehyde, postfixed in osmic acid, dehydrated, and coated with gold. Their flow surfaces were then examined by a scanning electron microscope (HITACHI S-800). In addition, eight specimens of nonvelour knitted Dacron graft and seven of woven Dacron graft were also recovered during the same study period. These were respectively removed from five and three cases and the total 15 specimens were examined similarly for comparison.

Dacron double velour grafts have been used in our institute since 1976, mainly for reconstructing the abdominal aorta and its branches. Since their introduction in 1976, up until the end of October, 1987, a total of 240 double velour grafts were implanted. The grafts used were either Cooley double velour grafts or Microvels | (Meadox Medi- cals, Oakland, NJ, USA), both of which are double velour knitted grafts made of Dacron. The choice of graft was made by the attend- ing surgeons.

Thirty-one graft materials were recovered from 16 patients on 20 occasions. The etiology of the arterial lesions that led to the aortic reconstruction was atherosclerosis in all but one case, in which the etiology of the patient's aneurysms was thought to be non- specific focal aortitis (case B). Eighteen grafts were recovered during reoperations. Two of the major reasons for reoperation were occlusion of the graft because of distal extension of the atherosclerotic process or anastomotic aneurysm formation. The remaining 13 specimens were recovered at autopsy.

After the gross findings were noted, the specimens were embedded in paraffin, sec- tioned, and stained for light microscopy. Hematoxylin-eosine, Masson's trichrome, elastica van Gieson, and phosphotungustic acid-hematoxylin stains were applied. AZAN stain was also used in several of the specimens. The stained slides were studied under light microscopy and photographed.

RESULTS

The recovered specimens were divided into three groups according to their histo- logical characteristics.

1. Initial phase: This phase characterizes the period immediately following implantation in which the graft embeds itself in the fibrin and no collagen formation is yet seen.

2. Organizing phase: This phase con- cerns the active incorporation of the graft from 10 weeks after the implantation through to 10 months. During this time, fibrous capsules are first formed at the exterior of the graft, resulting in a gradual extension into the interstices.

3. Stable phase: This phase, observed in the specimens recovered later than one year after implantation, develops after most of the luminal surface of the graft is covered with collagen. The findings of each phase are presented schematically in Fig. 1.

Findings in the initial phase: Immediate post- implantation period Only one specimen was recovered within

one week of implantation (A3) and the prosthesis had not yet adhered to the surrounding tissues in this five-day old specimen. The inner surface of the graft was covered with fresh thrombus and appeared red upon gross examination. Microscopic examination revealed the luminal surface of the graft to be covered with erythrocytes. The interstices of the graft were infiltrated with

Volume 19 Number 3 Dacron double velour vascular prostheses 303

Fig. 1. Schematic presentation of the three phases. (Top) Initial Phase

Implantation-several weeks The inner layer and the interstices are filled with fresh blood clots. No collagen fibers can be seen yet. (Middle) Organizing Phase

Two months-One year This is a podlike ingrowth of collagen fibers into the interstices. Macrophages, giant cells, fibroblasts, plasma cells, lymphocytes, and occasio- nal eosinophils can be seen in the graft. (Bottom) Stable Phase

From one year The graft has become incorporated by collagen fibers. The cells around the graft fiber are composed mainly of giant cells and lymphocytes.

fibrin, among which leukocytes with karyor- rhexis were entrapped. Erythrocytes in the interstices had already been cleared away, but nei ther fibroblasts no r collagen fibers were seen yet (Fig. 2).

Findings in the organizing phase: 10 weeks to I0 months after implantation Nine specimens f rom five patients were

studied in this group (Table 1). By this time, the double velour grafts had densely adhered to the surrounding tissues and it was

Fig. 9. (Top) Light microscopic appearance of a five day old double velour graft. The interstices are filled with a fibrin meshwork among which white cells are entrapped. HE stain. Original magnification 25X. (A3) (Bottom) SEM of the luminal surface of the same graft. The lumen is covered with erythrocytes. Original magnification 300X.

impossible to find a dissecting plane between the fabric and tissue. This firm adhesion was confirmed throughout the entire length of the graft in one autopsy case (case B). Most o f the luminal surfaces of the recovered specimens were covered with a t ransparent glistening film and some areas of red thrombus were also seen (Fig. 3). Pannus was observed in two of the specimens taken from a femoral anastomosis. Grossly, this was a white intimal extension from the host artery, conceal ing the fabric and firmly adhered to it. It consisted of fibrous intimal thickening extending in cont inuum from the host artery. The re was no obvious pannus growth from the proximal suture line in this phase.

304 Sato et al.

Table 1. Findings in the Organizing Phase (10 weeks--10 months)

Case * Implanted Luminal Capillaries Period Coverage In Out Int

Remarks

Specimens from the midportion of the grafts B 4 P 2.5/mo. None -- + B 8 P 4/mo. None -- + D 11 P 5/mo. None -- + F 14 P 10/mo. Partial -- +

Specimens from near the anastomosis B 5 P 2.5/mo. Partial - + C 10 P 3/mo. Partial -- + B 7 P 4/mo. Partial + + B 9 P 4/mo. Good - d- E 13 O 5/mo. Good -t- +

+ +

+ Foam cells +

+ + +

+ Pannus + Pannus

Foam cells

In, Inner coat; Out, Outer coat; Int, Interstices Luminal coverage means the coverage with collagen. * Graft patency at the time of recovery. P, patent; O, occluded

Fig. 3. (Top) Luminal coverage of a ten week old specimen recovered from the midportion of a graft. The luminal surface is covered with a white film. Patchy areas of red thrombi can also be seen. (B4) (Bottom) Formation of an outer fibrous capsule in the same specimen. Masson's trichrome stain. Original magnification IOX.

Microscopically, the grafts were seen to have gradually incorpora ted collagen fibers dur ing this period. At first, the fibrous capsule had fo rmed outside the prosthesis (Fig. 3), but fibrous tissues had also gradually developed in the interstices o f the graft fibers. T h e lumen was covered with a fibrin layer and red th rombi were present mainly in the valleys o f the crimps. T h e graft had b e e n infiltrated by m a n y kinds o f cells, namely, macrophages , foreign body giant cells, fibroblasts, and plasma cells (Fig. 4). Occas iona l eos inophi ls were encoun te red in two o f the specimens (cases B5 and D11) and t rans ient eos inophi l ia o f up to 16 per cent were observed in case B. O n the o the r hand, the white cell differential count was normal dur ing the patient 's postoperat ive course in case D. T h e cellular infiltration was denser at the exterior surface o f the graft where a lot of capi l la r ies were also obse rved , m a n y of which had grown into the interstices.

Differences between the midportion of the graj~ and the area near the anastomosis. Five specimens were recovered f rom nea r the anastomotic sites and c o m p a r e d with four mid- por t ion specimens (Table 1). T h e fibrous luminal coverage nea r the anastomosis was thicker and had fo rmed earlier. Capillaries


Fig. 4. Cellular infiltration of the graft at 10 weeks. Giant cells, macrophages, fibroblasts, plasma cells, and eosinophils can be seen. HE stain. Original magnification 50X. (B5)

were somet imes observed in this i nne r coverage just adjacent to the graft fibers. On the other hand, the fibrous luminal coverage was exceptional in the midportion specimens of this phase. There were no differences in the cellular infiltrations of the graft.

Findings in the stable phase: One year after implantation and thereaj2er Twenty-one specimens from 11 patients

were studied in this group (Table 2). These grafts were also found to be firmly adherent to the surrounding tissues and confirmed throughout the entire length in the autopsy cases (H, K, and M). The luminal surfaces of the recovered prostheses were covered with a glistening white film. Microscopically, very few changes had occurred over the several years in this period. Most of the luminal surfaces of the grafts were covered with collagen fibers (Fig. 5) and this covering was complete in most of the grafts near the anastomosis. In one specimen among three midportion grafts (H22), the coverage was incomplete, and the graft was covered with

Fig. 5. (Top) Appearance of a two year old graft. Good fibrous encapsulation of the graft can be seen. Masson's trichrome stain. Original magnification 10X. (H22) (Bottom) SEM view of the luminal surface of the same specimen. Original magnification 100•

thrombus in these areas. Foreign body giant cells and lymphocytes were seen throughout the period of study except in one specimen in which there was a peculiar lack of cellular reactions (I24). The fibroblasts and macrophages were much fewer when compared with the specimens recovered within one year and the giant cells were seen adjacent to the graft fibers as if engulfing them, espe- cially around the velour piles. On the other hand, the lymphocytes were noted at some distance from the fibers and arranged in a sheetlike fashion in four of the specimens: I26, K30, K31, and M35. Capillaries were ubiquitously noted in the outer coat. In eight cases, capillaries were also seen in the luminal coverage of the graft, more prominently near the anastomosis. They were just adjacent to the graft fibers, and never reached

306 Sato et aL

Table 2. Findings in the Stable Phase (One year--)

Implanted Luminal Capillaries Case * Period Coverage In Out Int

Remarks

Specimens from the midportion of the grafts H 22 P 2/yr. Partial -- + -- I 26 O 2/yr. 6/mo. Good + + + K 31 P 2/yr. 10/mo. Good -- + +

Specimens from near the anastomosis G 16 O 1/yr. 1/mo. G 15 O 1/yr. l l / m o . H 21 O 2/yr. H 23 O 2/yr. I 24 O 2/yr. 5/mo. I 25 O 2/yr. 6/mo. I 28 O 2/yr. 6/too. J 29 P 2/yr. 10/mo. K 30 P 2/yr. 10/mo. E 12 O 3/yr. 3/mo. L 32 P 4/yr. 2/mo. M 33 P 4/yr. 10/mo. M 34 P 4/yr. 10/mo. M 35 P 4/yr. 10/mo. N 36 P 5/yr. 6/mo. N 37 P 5/yr. 6/mo. O 38 P 5/yr. 6/mo. P 39 P 9/yr.

Good + + + Good + + - Good -- + - Good -- + -- Good -- + - Good + + - Only fragments recovered Good -- + -- Good -- + + Good -- + -- Good + + + Partial + - + Good - + - Good -- + - Good + + + Good + + + Good + + + Good - + --

Foam cells

Lipid depo.

Foam cells Foam cells

Foam cells

Foam cells

In, Inner coat; Out, Outer coat; Int, Interstices Luminal coverage means the coverage with collagen. * Graft patency at the time of recovery. P, patent; O, occluded

the lumen . I n seven spec imens , they were visible in t he graf t interst ices. Endo the l i a l coverage was no t found.

Differences between the midportion of the graft and the area near the anastomosis. T h e lumina l cove rage with co l l agen f ibers was th i cke r n e a r the a n a s t o m o s e s a n d was par t ia l ly defective in t he m i d p o r t i o n o f t he graft. More - ove r the cap i l l a r i es in the l umina l s ide o f the graft were m o r e p r o m i n e n t n e a r the anastomoses.

Early sclerotic changes in the prostheses F o a m cells were seen in seven o f the

spec imens (Tables 1 a n d 2), s i tuated in the valleys o f t he c r imps ly ing ad j acen t to the graft f ibers (Fig. 6). In a n o t h e r spec imen (G15), a layer o f a lcoho l - so lub le mate r ia l e x t e n d i n g to the d e p t h o f the i n n e r coa t was seen (Fig. 6). Bo th these obse rva t ions were

c o n s i d e r e d to b e ear ly sclerot ic changes . The ear l ies t sign o f l ip id depos i t i on was seen on two grafts i m p l a n t e d for five m o n t h s ( D l l a n d El3) . H ype rc ho l e s t e ro l e mia , up to 262 m g / d l , was o b s e r v e d in on ly o n e o f these e igh t pa t ien ts (case M).

Comparison with other types of prostheses T h e f irm a d h e s i o n o f v e l o u r grafts strik-

ingly con t ras t s with the a d h e s i o n o f o ther types o f grafts. Eight spec imens o f nonve lou r kn i t t ed grafts f rom four pa t ien ts a n d seven spec imens o f woven grafts f rom th ree pa- t ients were s tud ied for c o m p a r i s o n (Tables 3 a n d 4). O n e n o n v e l o u r kn i t ted D a c r o n graft was tes ted in t e rms o f its adhes ive s t rength to the pe r ig ra f t t issues (A2). Th is graft h a d a poros i ty o f 1,150 m l / m i n a n d h a d been i m p l a n t e d as an aor to i l iac bypass 11 years ear l ier . T h e r e c o v e r e d s p e c i m e n a p p e a r e d to


Fig. 6. (Top) Foam cells observed in a 2 year and 10 month old graft (arrows). HE stain. Original magnification 50X. (]29) (Bottom) Deposition of alcohol-soluble material adjacent to the graft fibers (arrows). HE stain. Original magnification 10X. (G15)

be well incorporated by fibrous tissue, however, the fabric was easily peeled away from

Fig. 7. Macroscopic appearance of an 11 year old nonvelour knitted Dacron graft. (A2) (Top) The graft appears well incorporated by the surrounding tissues. (Bottom) It was easily peeled away by gentle pulling.

the surrounding tissue by gentle pulling with forceps (Fig. 7). Two cases (B and H) implanted with a woven Dacron graft having a porosity of less than 200 m l / m i n were similarly studied. In case B, the four month old prosthesis had detached itself f rom the surrounding tissues except at the suture lines. In case H, the two year old graf t had largely detached itself f rom the surrounding tissues

Table 3. Findings from the Nonvelour Knitted Grafts

Case * Implanted Luminal Interstitial Remarks Period Coverage Ingrowth

Specimens from the midportion of the grafts A 2 P 11/yr. 2/mo. A 42 P ll /yr. 2/mo.

Specimens from near the anastomosis

None None Partial Partial

Q 44 P 2/yr. 5/too. Partial None R 46 O 3/yr. 3/mo. Good Partial Q 45 P 4/yr. 10/too. Partial Partial A 1 P 11/yr. 2/too. Good Partial A 43 P l l /yr. 2/too. Partial Partial S 47 P l l /yr. 7/mo. Partial Partial

Foam cells

Luminal coverage means the coverage with collagen. Interstitial ingrowth means that by collagen. * Graft patency at the time of recovery. P, patent; O, occluded

308 Sato et al.

Table 4. Findings from the Woven Grafts

Case �9 Implanted Luminal Period Coverage Outer Coverage Remarks

Specimens from the midportion of the grafts H 18 P 2/yr. Partial Blood clot H 19 P 2/yr. Partial Blood clot

Specimens from near the anastomosis T 40 P 6 days Graft embedded in a blood clot T 41 P 6 days Graft embedded in a blood clot B 6 P 4/mo. None Blood clot H 17 P 2/yr. None Blood clot H 20 P 2/yr. Good Blood clot

Foam cells

Luminal coverage means the coverage with collagen.

Fig. 8. (Top) Separation of a woven graft two years after implantation. An old blood clot can be seen between the fabric and surrounding tissues. (H19) (Bottom) SEM view of the flow surface of the same graft. The fabric is largely exposed to the lumen. Original magnification 100X.

and an old b lood clot was seen between them (Fig. 8).

Microscopically, the col lagenous coverage o f the lumen was of ten f o u n d to be defective in the n o n v e l o u r knit ted grafts, with the flow surface be ing covered by th rombus in these areas. An interstitial ingrowth o f collagen was also incomple te in these grafts, and two

Fig. 9. (Top) Two sharply demarcated layers in a 11 year old nonvelour knitted graft. The graft and outer layers are clearly distinguishable. Masson's trichrome stain. Original magnification 10X. (A2) (Bottom) SEM view of the same graft. The lumen is largely covered with what is thought to be fibrin. Original magnification 100X.


Fig. 10. Less cellular infiltration in a 2 year and 5 month old nonvelour knitted graft. HE stain. Original magnification 25• (Q44)

sharply demarcated layers were observed in the specimens, namely, the graft layer and the outer collagen layer (Fig. 9). Foreign body giant cells were seen around the grafts, but were fewer when compared with those around the double velour grafts. Round cell infiltrations were also seen less frequently in these grafts (Fig. 10).

The salient features of woven grafts are that they are hardly incorporated, if ever, and luminal coverage is often defective (Fig. 8). The grafts did not adhere to the surrounding tissues and old blood accumulation was seen around them.

The following case involves a patient in whom bacteremia from a remote focus resulted in graft infection of a poorly incorporated woven graft, whereas his double velour graft was apparently insulated from this infection.

Presentation of a case: Case B. A 74 year old Japanese male was referred to our hos- pital with a two-month history of hemateme- sis and melena. Under the diagnosis of primary aortoduodenal fistula, he was immediately operated upon. An infrarenal aneurysm was resected, and an axillobi- femoral bypass was established. Ten weeks later, another supraceliac aneurysm was resected and a woven Dacron graft was implanted. At the same time, anatomic reconstruction from the aortic stump to both

femoral arteries was done using a bifurcated Dacron double velour graft No organism grew from the culture of the aortic stump at that time. Two months after the second operation, he was readmitted because of a left groin infection and the culture of the wound exhibited Staphylococcus aureus growth. Debridement and sartorius muscle coverage of the graft apparently cured the infection. Eight weeks after that operation, however, he was again admitted with a spike fever. His blood culture produced Staphylo- coccus aureus and he died three days after the onset of the fever.

Autopsy findings: The distal anastomosis between the woven graft and the abdominal aorta had been disrupted, which was the cause of his death. The blood clot in the abdominal cavity was foul smelling, and the aortic wall near the disrupted anastomosis was fragile. The four month old woven graft had completely detached from the surrounding tissues. Histologically, an old blood clot was found around the woven graft. Con- versely, the double velour graft in the infrarenal position showed good incorporation and firm adherence to the surrounding tissue. Moreover, no sign of infection was found around the latter graft.

DISCUSSION

As stated above, double velour grafts were constructed to actualize some of the ideal characteristics of vascular prostheses. Al- though several successes have been reported in animal experiments, s,n,12 not all are necessarily applicable to man.

It has been reported that there is a broad range of interspecies differences of the host reaction toward t h e implanted prosthesis? 3 As mentioned before, the incorporating process in man is divided into three phases: the initial phase, the organizing phase, and the stable phase.

In experimental studies using dogs, velour Dacron grafts have been reported to be covered with an endothelial lining. 12 In one

310 Sato et al. 1989

a n e c d o t a l r epor t , TM in which a h u m a n autopsy case was studied after an in situ fixation of the prosthesis, endothelial coverage was found in the midportion of the graft. In the present study, however, no endothelia on the prostheses were demonstrated. The fragility of the endothelial layer 15 may have resulted in a failure to recognize it, but it is more prudent to conclude that endothelial coverage of grafts in man is exceptional, if in fact it occurs at all.

The cellular reaction is more marked in velour grafts than in nonvelour grafts but is not necessarily detrimental to the incorporation process? ~ Rather, it contributes to, or results in, the granulation ingrowth, thus promoting firm adhesion of the prosthesis.

The double velour graft's good interstitial ingrowth and luminal coverage with collagen, though the latter is sometimes partially defective in the midportion, directly contrasts with what was observed in the nonvelour knitted specimens? 5 Luminal coverage is reported to enhance resistance to infection ~7,~8 and it is also reported that infection of the graft is usually associated with graft separation from the surrounding tissues) 9 The presented case shows that poorly incorporated vascular grafts seem to be more vulnerable to infection when bacteremia is present.

Poor adhesion is thought to result in grave sequelae in the case of anastomotic aneurysm formation. Extravasated blood could readily dissect the graft from the surrounding tissues. Flap occlusion of the aorta and sudden death of the padent could therefore ensue. The woven Teflon grafts, which are also known to show poor adherence to the surrounding tissues, have been reported to form this type of suture aneurysm? ~ The flap occlusion of the aorta by a woven Dacron graft has not been encountered in our institute; the risk is, however, inherent in this poorly incorporated graft. The rate of free rupturing is high with woven Teflon grafts ~~ and poor incorporation of the woven Dacron graft also presents the risk of free

bleeding into the body cavity rather than pseudoaneurysm formation, as clarified in the above case report. Suture line aneurysms do occur with double velour grafts despite their good incorporation. In contrast to nonvelour prostheses, however, they are con- fined to femoral anastomoses. Free rupture or flap occlusion has not been encountered.

In the reconstruction of larger-caliber arteries, such as the thoracic aorta, it is com- monplace to use a woven graft in order to reduce interstitial bleeding from the wide surface area. When feasible, however, it is better to use a double velour graft after meticulous preclotting.

Another observation that deserves atten- tion is the appearance of foam cells in the inner layer of the graft. DeBakey reported the formation of an atherosclerotic plaque in a nonvelour knitted graft observed after five years, 22 however, sclerotic changes have been proven to take place much earlier. In this study, foam cells were observed near the graft fibers where thickening of the inner layer was observed. The clearance of ac- cumulated substances is thought to be defective in the depths of the inner layer and it is quite possible that the defective transport mechanism results in this characteristic loca- tion of the foam cells. It also supports the speculation as to why these cells were not found around the capillaries, which were also characteristically located only to the depth of the inner coat.

ACKNOWLEDGMENTS

The authors would like to thank Itsuo Katagiri, Atsuko Takeuchi, and Rokurou Miyazawa for their technical assistance and Toru Sato for preparing the illustrations.

(Received for publication on May 20, 1988)

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The biologic fate of Dacron double velour vascular prostheses —A clinicopathological study—