Expanded PTFE Prostheses as Arterial Substitutes in Humans: Late Pathological Findings in 73 Excised Grafts

Expanded PTFE Prostheses as Arterial Substitutes in Humans: Late Pathological Findings in 73 Excised Grafts Maxime J . Formichi, MD,' Robert G. Guidoin, PhD,' Jean-Michel Jausseran, MD,2 John A . Awad, MD,3 K. Wayne Johnston, MD,4 Martin W. King, P Eng,4 Robert Courbier, MD,2 Michel Marois, MD,' Claude Rouleau, MD,' Michel Batt, MD,6 Jean-Francois Girard, MD,' and Camille Gosselin, MD,'

Through collaboration of surgeons, pathologists and bioengineers at five centers in Canada and France, this study analyzed the late pathology and structural changes in 73 expanded PTFE arterial prostheses harvested from patients at autopsies and reoperations. The degree of tissue encapsulation increased with the duration of implantation but was reduced by the presence of infection. In several cases, the fibrous tissue penetrated the wall of the prosthesis and partitioned off the thin outer layer, thus disrupting the delicate microporous structure of the wall. The presence of aneurysms was observed in models that had no external reinforcing layer and among grafts that apparently suffered from surgical trauma. Wrinkling of grafts was noted at areas of flexion and was often associated with thickening of the external capsule and reduced luminal diameters. Endothelialization was found within only a few millimeters of the anastomoses. The luminal surfaces were generally not well healed. The PTFE structure was usually readily visible under a thin covering of loosely adhering thrombotic deposits. Bacteria were observed in 46% of the cases, even though only 29% were considered clinically infected. The incidence of lipid or cholesterol deposits was high. Avoiding iatrogenic trauma to the external wall of the prosthesis during implantation is important. Those features where design improvements are required to provide longer term structural integrity and dimensional stability in future models of expanded PTFE prostheses should be identified. KEY WORDS: Expanded PTFE prostheses.

Although the autogenous saphenous vein remains the gold standard for revascularization of the extremities [ 11, the expanded PTFE prosthesis can be considered the material of choice for extranatomical bypass [2-51 and for above-knee replacement when the saphenous vein is unavailable, inadequate, or required for cardiac or distal bypass [6-191. While the clinical performance of expanded PTFE prostheses has been studied and reported extensively, the late morphological changes of this particular type of prosthesis have not been described in detail. The objective of this study was

From the Laboratoire d'Analyses Fonctionnelles, H6pital St-Frangois d'Assise 1 Laboratoire de Chirurgie Expirimentale, Universite' Laval, Quebec, PQ, Canada. zH6pital St-Joseph, Marseille, France; -'Centre Hospitalier de I'Universite' Laval, QuPbec, Canada; 4Toronto General Hospital, Toronto, Canada; 'University of Manitoba, Winnipeg, Canada; 6H6pital Annexe Republique, Nice, France. Reprint Requests: Robert Guidoin, PhD, Laboratoire d'Analyses Fonctionnelles, H6pital St-Frangois d'Assise, Quebec, GIL 3L5, Canada. 14

VOLUME

NO 1

-

2

15

ePTFE PROSTHESES IN HUMANS

1988

to follow these changes by studying the pathology and structure of 73 expanded PTFE grafts retrieved from autopsies and reoperations after periods of implantation ranging from one to 1500 days (50 months). The following characteristics were of particular interest: 1) the degree of encapsulation, 2) the shape and morphology of the external capsule, 3) the cellular elements incorporated within the capsule, 4) the extent of tissue penetration into the wall of the prosthesis, 5 ) the frequency of lesions found in the wall, and 6) the types of cellular elements deposited on the luminal surface. This work is part of an ongoing cooperative retrieval program for collecting and evaluating arterial prostheses implanted in humans [20-231.

MATERIALS AND METHODS

TABLE Ill.-State of distal runoff Patencv of distal arteries 0-blind 1 2 3 Unknown

Patients In = 731 4 23 21 12 13

Percentaae 5.5 31.5 28.8 16.4 17.8

The prostheses

Of the 73 expanded PTFE prostheses, 70 were reinforced Gore-Tex@, two ImpragraftP and one Bard [email protected] of the grafts were 8 mm in diameter; 25 had a diameter of 6 mm, and in the remaining 19 cases the size of the graft was not indicated and could not be determined in the retrieved specimens.

The patients

The 73 arterial explants were harvested at five different centers in Canada and France from 64 patients (55 men and 9 women) whose mean age at implantation was 60.6 years (range: 3 3 to 83 years). The average duration of implantation was 339 days with a range from one to 1500 days. The indications for operation are given in Table I. The sites of implantation and patencies of the distal arteries prior to surgery are given in Tables I1 and 111. Four prostheses were retrieved at autopsies, and the remainder were removed at reoperation. The most frequent complications requiring removal of the graft were thrombosis and infection (Table IV). TABLE I.-Indications for surgery

Claudication Rest pain Gangrene Acute ischemia Thrombus of a previous graft False aneurysm + thrombosis Unknown

Patients (n = 73) Percentage 16 21.9 31 42.5 11 15 7 9.6 4 5.5 1 1.4 3 4.1

Analytical methods

The pathology and structural changes of the prostheses were investigated according to the following protocol [24]. After excision, the grafts were opened longitudinally, carefully rinsed with heparinized saline, fixed in a buffered solution of 1.5% glutaraldehyde and shipped immediately t o the Laboratoire d’Analyses Fonctionnelles at the Hbpital St-Francois d’Assise in Quebec City. There, the prostheses were examined macroscopically and photographed. Representative areas of the internal and external capsules were selected for pathologic studies. Each area was divided into two specimens. One part was postfixed in a Perfix@solution, dehydrated with ethanol and clarified with toluene before being mounted in paraffin. Sections four microns thick were stained in the following order for viewing by light microscopy: Hematoxyl-phloxin-safran; Weighert; Masson-Trichrome; Brenn and Brown; and Dhal stains. The second specimen was postfixed in carboxyhydrazide and osmium tetroxide for examination by scanning electron microscopy TABLE IV.-Reasons for explantation Patients Percentage

TABLE 11.-Sites of implantation Femoropopliteal above-knee (13, 17.8%) below-knee (18, 24.7%) unknown (6, 8.2%) Femorodistal Axillopopliteal lliopopliteal Aortoiliac Aortofemoral Femorofemoral (transversal) Axillofemoral Carotidohumeral Unknown

Patients Percentage 37 50.7

6 1 1 1 1 2 21 1 1

8.2 1.4 1.4 1.4 1.4 2.7 28.8 1.4 1.4

Surgical removal (94.6?70, n = 69) Thrombosis Infection Infection and thrombosis Anastomotic stenosis False aneurysm Deterioration of run-off Prosthetic aneurysm Unknown A u topsies (5.4%, n = 4) Postoperative shock Myocardial infarct Cancer of the lung SeDticemia

46 10 5 2 2 2 1 1

63.0 13.7 6.8 2.7 2.7 2.7 1.4 1.4

1 1 1 1

1.4 1.4 1.4 1.4

ePTFE PROSTHESES IN HUMANS

16

(SEM). In this case dehydration was obtained by immersion in a series of ethanol solutions of increasing concentrations, culminating in pure ethanol, followed by critical point drying using liquid CO, as the transfer medium. Specimens were then coated with gold-palladium and examined in a JSM 35CF scanning electron microscope at 15 to 20 kV of accelerating voltage. The tissue adhering to the remaining parts of the prostheses was removed by boiling in a 5 % sodium bicarbonate solution followed by immersion in a diluted commercial bleach solution at room temperature. Again the specimens were examined macroscopically and photographed. Additional specimens from the anastomotic regions were also prepared for SEM examination.

RESULTS Macroscopic observations

The external capsules of the explanted prostheses were classified according to four different degrees of encapsulation: 0) no encapsulation, 1) a thin fibrous coating, 2) an intermediate fibrous coating and 3) a thick fibrous coating (Figure 1). The frequency distribution of this ranking is presented in Table V. These data clearly demonstrate that both thickening of the capsule and progressive incorporation of fatty deposits increased with the time of implantation. In addition to time, a second major factor was observed t o affect the degree of encapsulation, namely, the presence of infection. Those prostheses explanted because of an infection showed a complete absence of encapsulation in 80% of cases, although some vestigial remains were evident, and, of the remaining 20070,none developed a thick fibrous capsule. This is in contrast with the prostheses removed because of thrombosis which revealed a more uniform distribution across the four types of capsules (Figure 2). Chi-square analysis to compare the frequencies between these two groups of prostheses confirmed that the differences for Type 0 and Type 3 capsules were statistically significant (p < 0.01) while the mean durations of implantation for the two groups were comparable (Table VI). Another interesting observation on the excised grafts was the appearance of wrinkling at areas of flexion, associated with thick external fibrous capsule and localized stenosis (Figure 3). One of the wrinkled prostheses was associated with a severe aneurysmal dilatation. Microscopic analysis

The microscopic examination of the external capsules revealed four progressive levels of adhesion between the tissue and the wall of the prosthesis. They were defined as: 0) no adherence, 1) adherent in some areas, 2) continuous and complete adher-

ANNALS OF VASCULAR SURGERY

ence, and 3) penetration of the external layer of the prosthesis wall. The data presented in Table VII show that the level of adhesion between the capsule and the external layer of the prosthesis increased with the duration of implantation. Over time, fibrous tissue appeared to penetrate and separate the external layer from the rest of the prosthesis wall (Table VIII). It then filled up the gap behind the separated layer prior to further invasion of the newly exposed PTFE wall. Of the explanted prostheses studied, 46.7% had reached the fourth level of adhesion and presented a partially separated external layer of PTFE (Figure 4). The extent and location of cellular invasion of the microporous wall was studied in 32 specimens and the results are shown in Table IX using a four point scale: 0) absent or very slight, 1) external stratum invaded, 2) internal stratum invaded, or 3) full thickness of the graft wall invaded. There was no obvious relationship between the time of implantation and the level or location of invasion. In fact only a few specimens (18.7%) revealed a continuous and significant penetration by cellular elements. The degree to which fibrous tissue had penetrated and altered the microporous structure of the prosthesis was examined and recorded at one of three stages: 0) slight or absent fibrous penetration with no alteration of the structure, 1) significant penetration with some alteration of the structure, or 2) destruction of the wall. The data in Table X clearly demonstrate that both the degree of tissue penetration and damage to the microporous structure increased with longer periods of implantation (Figures 5 and 6). In two cases the lesions were particularly severe. An Impragraft implanted for 4 years (1500 days) showed a n aneurysmal dilatation. The wall of the aneurysm revealed abundant amounts of fibrous tissue incorporating isolated and dispersed PTFE nodules. In the second case, a reinforced Gore-Tex@prosthesis, implanted for only 120 days, presented a localized injury of the wall, probably consecutive to a iatrogenic trauma during surgery (Figure 7). SEM examinations of the luminal surfaces of the retrieved prostheses revealed the presence of various things including bacteremic colonization, leukocytes, lipids, cholesterol (Table XI) (Figures 8-10), adipocytes, and endothelial cells (Figure 11). Of the 67 specimens, bacteria were present in 31 grafts (46%), leukocytes were found in eight (12%), and five grafts had both (70/0). In only nine of the 31 prostheses were the bacterial colonies associated with graft infection (29%). Similarly, the presence of leukocytes was associated with an infection in only three out of eight grafts (37.5%). Lipid deposits were found in 21 grafts, cholesterol was present in 12 while groups of adipocytes were observed in two prostheses. Time is an important factor as far as these deposits are concerned. Lipids and cholesterol (Figures 8,9,10) were observed in grafts implanted for a mean of 402 days, while they were absent in grafts implanted for a mean of 249 days. Statistical analysis using a

VOWME 2

NO 1 - 1988

ePTFE PROSTHESES IN HUMANS

Fig. 1.-Explanted Gore-Tex@ arterial prostheses showing various degrees of encapsulation. (a) No encapsulation in femoropopliteal prosthesis removed from 44-year-old who died in postoperative period. (b) Second degree encapsulation in axillofemoral bypass graft in patient reoperated 300 days postimplantation because of distal stenosis. (c) Fourth degree encapsulation in axillofemoral graft removed from 65-year-old patient reoperated 730 days later because of graft thrombosis.

17

A N N A L S OF VASCULAR SURGERY

ePTFE PROSTHESES IN HUMANS

18

4

1-1

INFECTIONS :337D

THROMBOSES : 300 D

3

( p < 0.011

31.1 .4 5.6

2

80

0 -1

'

I

I

I

I

0

I

I

1

I

1

50

I 100

PERCENT ( y o )

Fig. 2.-Degree

of encapsulation of grafts explanted because of thrombosis and infection.

TABLE V.-Effect

of duration of implantation on degree of encapsulation Number of prosthesis (n = 68) 30

Yo of grafts 44.1

Mean duration of implantation (days) 176

1 = thin capsule

11

16.2

271

2 = intermediate capsule

11

16.2

423

3 = thick capsule

16

23.5

512

Degree of encapsulation 0 = no encapsulation

TABLE VI.-Comparison

Observations

-

no fatty deposits some fatty deposits extensive fatty deposits

of degree of encapsulation between grafts associated with thrombosis and infection

THROMBOSIS Mean duration of implantation = 300 days Degree of encansulation N145 O!O 31.1* 14* 0 1 10 22.2 15.6 2 7 31.1 * 3 14 *Difference significant at confidence level p ~ 0 . 0 1

INFECTION Mean duration of implantation = 332 days NI15 YO ao.o* 12* 1 6.7 2 13.3 0' o.o*

VOLUME 2 NO 1 - 1988

ePTFE PROSTHESES IN HUMANS

19

Fig. 3.-Femoropopliteal prosthesis implanted below knee in 62-year-old and removed 1080 days later because of thrombosis. Area of flexion resulted in proliferation of fibrous tissue (arrows). Enlarged external capsule compressed graft causing localized stenosis.

Fig. 4.-Section of Gore-Tex@ axillofemoral prosthesis removed after 730 days of implantation in 65-yearold because of thrombosis. Inner surface is coated with unorganized coagulum (UC). Note presence of fibrin (F) in wall and very thick external fibrous capsule (EFC) which has caused partial separation of external PTFE layer (arrows) (Fibrin staining x 250).

Fig. 5.-Section of a thrombosed Gore-Tex@ femoropopliteal graft explanted after 730 da s in 74-yearold. External reinforcing layer (arrows) as been separated and disrupted by fibrous tissue which penetrated wall (FT) (Masson x 100).

Fig. 6.-Section of 6 mm femoropopliteal Gore-Tex" graft implanted for 120 days in 56-year-old and removed because of thrombosis. Wall of prosthesis has been damaged probably because of iatrogenic compression (IC). Structure has lost its integrity and shows extensive invasion of fibrous tissue (Verhoeff's x 100).

z

TABLE VIL-Effect of duration of implantation on degree of adhesion between external capsule and wall of prosthesis Mean duration Level of Patients Perof implantation adhesion (n = 30) centage (days) 0-No adherence 3 10 76 1-Adherent in 4 13.3 90 some areas 2-Complete 9 30.0 452 adherence 14 46.7 497 3-Penetration of the external layer of the prosthesis wall

TABLE VIII.-Effect of duration of implantation on level of integrity of external reinforcing layer of Gore-Tex@ prostheses Integrity of the external layer Patients PerMean duration (days) (n = 52) centage of implantation 0-intact 5 9.6 181 1-partially sepa15 28.8 325 rated 2-totally sepa8 15.4 257 rated 3-disrupted or 24 46.2 359 destroyed

ANNALS OF VASCULAR SURGERY

ePTFE PROSTHESES IN HUMANS

20

Student t-test indicated that these two distributions were significantly different (p < 0.05). Two of the prostheses showed lipid infiltration throughout the Level and Mean duration wall thickness. Even after tissue removal and cleanextent of Patients Perof implantation ing, the microporous structure appeared perma(days) cellular invasion (n = 32) centage nently altered due to the extensive lipid penetration 0-absent or very 18 56.3 279 (Figure 12). slight 1-external stra7 21.9 110 On only two occasions were endothelial-like cells tum invaded observed on the luminal surface and then only 2-internal stra1 3.1 450 within a few millimeters of the anastomoses (Figtum invaded ure 11). 3-full thickness 6 18.7 305

TABLE IX.-Extent and location of cellular invasion within the wall of prosthesis

of the graft wall invaded

DISCUSSION The expanded PTFE vascular prosthesis is the only synthetic alternative to the autologous human saphenous vein which commands widespread approval and extensive use today. However, it is still not the ideal prosthesis, and we need to recognize its various modes of failure. The appearance of wrinkling at points of flexion [25] is of particular concern. Geiger reported this phenomenon in four of nine cases [26]. It also tends to appear in the anastomotic region of end-to-side TABLE X.-Effect of duration of implantation on anastomoses when the graft is implanted at a wide degree of fibrous tissue penetration into wall of angle to the host vessel. Once formed, these wrinprosthesis kles tend to persist, even when the angle is reduced Degree of Mean duration by extending the point of the prosthesis during subfibrous tissue Patients Perof implantation sequent surgery. penetration (n = 42) centage (days) To this end we see merit in retrospective retrieval 0-slight or 32 76.2 256 programs. Such studies provide direct evidence of absent fibrous clinical experience in ill patients with their impaired penetration. No alteration physiology and elevated resistance to blood flow, of the strucwhich is not possible through animal experimentature tion. At the same time we recognize that the major 1-significant 8 19.1 438 limitation of this retrieval approach is its biased penetration, sampling. By relying mainly on grafts harvested alteration of from reoperations, this study focussed on grafts the structure that had already failed. We do not know, in most 2 4.7 810 2-destruction of instances, how long the graft functioned as a blood the wall flow conduit. It is conceivable that the changes in the grafts that failed due to infection or thrombosis might have been quite different from those observed in patent functioning grafts. We foresee that this limitation may be overcome in the future by seeking an equivalent number of patent grafts from autopsies which can serve as a more reliable control group. Cellular invasion of the prosthesis by fibrous tissue is generally considered an essential step in the healing process and long-term patency of arterial grafts [27]. It is considered to be an important criterion by many surgeons when selecting which comTABLE XI.-Frequency of various findings on lumimercial PTFE prosthesis to use [28]. Camilleri, nal surface of explanted prostheses however, has recently questioned the importance of Patients cellular invasion by observing that the walls of 26 (n = 67) Percentage patent PTFE grafts remained essentially free from Bacteremic colonization 31 46.3 adhering tissue after implantation times of one to 60 Leukocytes 8 11.9 months (29). The results of this study lend credence Lipids 21 31.3 to this alternative point of view by suggesting that Cholesterol 12 17.9 cellular invasion is responsible for alterations in the

VOl UME

2

No 1 - 1988

ePTFE PROSTHESES IN HUMANS

Fig. 7.-Cleaned, external surface of thrombosed distal femoropopliteal Gore-Tex@ graft removed after 180 days in 72-year-old who was amputated. Fibrous tissue proliferation of external capsule disrupted external PTFE layer leaving internal microporous structure exposed (arrows).

Fig. 8.-Distal, luminal surface of femoropopliteal Gore-Tex@ prosthesis implanted for 540 days in 60-year-old who was subsequently amputated. Note the complete absence of inner capsule which leaves PTFE nodules and internodular fibrils exposed (arrows). In addition to red blood cells, (RBC) bacterial colonies (BC), lipid and cholesterol particles (L and C) are visible (x 2000).

21

22

ePTFE PROS THESES IN HUMANS

ANNALS OF VASCULAR SURGERY

Fig. 9.-Luminal surface of iliopopliteal Gore-Tex@ graft implanted for 780 days prior to removal from 66-year-old due to formation of false aneurysm. (a) Note presence of bacterial colonies (BC) and of lipids and cholesterol particles (C) (x 720). (b) Leukocytes are also visible (WBC) (x 2000).

VOLUME 2 - 1988

No 1

ePTFE PROSTHESES IN HUMANS

Fig. 10.-Luminal surface of a thrombosed distal femoropopliteal Gore-Tex@graft implanted for 1080 days in a 62-year-old. (a) Denuded surface reveals structure of microporous PTFE nodules (arrows) (x 200). (b) Parietal thrombi incorporating numerous cholesterol particles (C) are also evident (x 3000).

23

24

ePTFE PROSTHESES IN HUMANS

ANNALS OF VASCULAR SURGERY

Fig. 11 .-Luminal surface of thrombosed femoropopliteal Gore-Tex@ prosthesis implanted for 390 days in a 71-year-old, subsequently amputated. Note presence of thin, fragile veil of endothelial-like cells (ELC) near the anastomotic line (x 2000).

microporous structure of the wall. It is therefore not surprising that aneurysm formation has been associated with the early models of Impra@and Gore-Tex@ prostheses [30-331. In 1975, with a view to eliminating this complication, W.L. Gore and Associates added an external reinforcing layer of less porous PTFE. Since then, Reinforced Gore-Tex@ prostheses have enjoyed improved mechanical strength, have experienced less rapid and less extensive penetration of tissue, and appear to have suffered less frequently from late structural lesions [34-371. Nonetheless, we are cautious about predicting very long term stability for this improved product at this time. One of the Reinforced Gore-Tex@ prostheses retrieved in this study had experienced such a proliferation of tissue after 180 days that the external reinforcing layer had been removed, exposing the internal microporous wall (Figure 6). It is possible that this lesion may have had iatrogenic origins [38]. Nevertheless, the long term stability of those prostheses without a reinforcing layer, or those designed to favor the incorporation of fibrous tissue, must be called into question. Expanded PTFE prostheses are known to have limited resistance t o bacteremic colonization [39-421. Indeed, the frequency of bacterial colonies observed on the luminal surface of the explanted grafts in this study is considered to be high at 46% [24]. Admittedly, only 9 of these 31 grafts had clinically diagnosed infections. We cannot say whether the remaining 22 should be acclaimed “resistant to

infection” or whether their infections were merely dormant, waiting for the appropriate stimulus to activate them. Obviously the presence of bacteria in itself is a concern that points to the need for more caution in the use of aseptic techniques. Any bacteremia, however transient, has the potential to cause contamination of these grafts [43]. The near or complete absence of encapsulation in 80% of the infected prostheses suggests that the destruction of the capsule may be a consequence of the infection process. This is probably the mechanism of propagation for an infection which originally was confined to a small segment of the prostheses. The frequency and extent to which lipids and cholesterol infiltrated the walls of the explanted grafts in this study appear to be significantly greater than has been previously reported [24,44,45]. At the same time we failed to observe any arteriosclerotic changes [46] or ossification of the grafts I471 as has been reported elsewhere. This may be due to the biased sampling of our retrieval program as discussed previously. CONCLUSION Generally, PTFE has certain advantages as a material for arterial substitutes [21], but the host’s tissue reaction, even though moderate, has a tendency to compromise the integrity of the external layer of the prosthesis wall. Thus, over time, those

VOILUME

2

NO 1 - 1988

ePTFE PROSTHESES IN H U M A N S

Fig. 12.-Thrombosed axillofemoral Gore-Tex@ prosthesis removed after 300 days from a 54-year-old and cleaned. Microporous structure is not well defined, typical of the appearance of grafts containing lipid and cholesterol deposits. (a) External surface (x 200). (b) Internal surface (x 200).

25

26

ePTFE PROSTHESES IN HUMANS

models that are unsupported tend t o form aneurysms. O n t h e other h a n d , those models that have been augmented with an external reinforcing layer appear t o have sufficient protection against damaging tissue infiltration. It is therefore important f o r surgeons to preserve this external protective layer during implantation, since any damage f r o m clamps o r needles might diminish t h e structural integrity a n d long term stability of the graft. Further improvements in the design o f these prostheses a r e still required, b u t this will only be achieved by first obtaining a clearer understanding of how t h e structure and properties of t h e outer layer influence the nature a n d degree of fibrous incorporation, how to control t h e incidence of infection, a n d how t o control t h e deposition of lipids.

ACKNOWLEDGMENTS This work has been supported in part by the HBpital St-Franqois d’Assise, Quebec a n d t h e Medical Research Council of Canada. The following hospitals collaborated in this study: HBpital St-Joseph in Marseille, France. HBpital Annexe-RCpublique in Nice, France. HBpital St-Franqois d’Assise a n d t h e Centre Hospitalier d e I’Universite Lava1 in Quebec City, Canada; a n d t h e T o r o n t o General Hospital in Toronto, C a n a d a . The exchanges with the French investigators were supported by t h e Echanges France-Quibec. The authors would like t o extend their gratitude t o Daniel Marceau, Royston Paynter, a n d Yves Marois for help a n d guidance. The technical assistance of Suzanne Bourassa, Marielle Corriveau, H u g u e t t e Desbiens, Claire Kingston, Denise Lafrenikre-Gagnon, Nicole Massicotte a n d Gilles Mongrain is gratefully acknowledged. We a r e also indebted to t h e attending staffs o f the operating r o o m a n d the pathology laboratories who participated in harvesting t h e grafts. Finally, the collaboration o f W.L. G o r e and Associates is also greatly appreciated.

REFERENCES 1. REICHLE FA. Criteria for evaluation of new arterial

prosthesis by comparing vein with Dacron femoropopliteal bypass. Surg Gynecol Obstet 1978; 146:7 14-720. 2. CAMPBELL CD, BROOKS DH, SIEWERS RD, PEEL RL, BAHNSON HT. Extra-anatomic bypass with expanded PTFE. Surg Gynecol Obstet 1979; 148:525-530. 3 . FLETCHER JP, LITTLE JM, LOEWENTHAL J. Initial experience with PTFE extraanatomic bypass. A m J Surg 1980; 139:696-699. 4. COURBIER R, JAUSSERAN JM, BERGERON P. Axillo-femoral bypass material of choice. In GREENHALGH RM (ed). Extraanatomic and secondary arterial reconstruction. Pitman Press, 1982: 122- 130.

ANNALS OF VASCULAR SURGERY

5 . ASCER E, VEITH FJ, GUPTA SK, SCHER LA, SAMSON RM, WHITE-FLORES SA, SPRAYRECAN S. Comparison of axillounifemoral and axillobifemoral bypass operations. Surgery 1985; 97: 169-175. 6. CAMPBELL CD, BROOKS DH, WEBSTER MW, DIAMOND DL, PEEL RL, BAHNSON HT. Expanded microporous polytetrafluoroethylene as a vascular substitute: a two year follow-up. Surgery 1 979; 85: 177- 1 83 . 7. HAIMOV M, GIRON F, JACOBSON I1 JH. The expanded polytetra- fluoroethylene graft. Three years’ expeiience with 362 grafts. Arch Surg 1979; 114~613-677. 8. SUY R, NEVELSTEEN A, DELEERSNLJDER D, DEWAELE G, SEGHERS K, HENDRICKS J, STALPAERT G. The expanded polytetrafluoroethylene (PTFE) graft as a vascular substitute. J Curdiovasc surgi98o; 21:321-328. 9 . CRANLEY J J , HAFNER CD. Newer prosthetic material compared with autologous saphenous vein for occlusive arterial disease of the lower extremity. Surgery 1981; 89:2-7. 10. SIMONE JR ST, DUBNER B, SAFI AR, DELGUERCIA P, SHAH MA, ZAGOUN L, REICHLE FA. Comparative review of early and intermediate patency rates of PTFE and autolonous saphenous iein &afts for lower extremity ischemia. -Surgery 1981: 90~991-999. 1 1 . WEI’SEL RD, JOHNSTON KW, BAIRD R J , DREZNER AD, OATES TK, LIPTON IH. Comparison of conduits for leg revascularization. Surgery 1981; 89:8-15. 12. O’DONNELL JR. TF, FARBER SP, RICHMOND DM, DETERLING RA, CALLOW AD. Above-knee PTFE femoropopliteal bypass graft: is it a reasonable alternative to the below-knee reversed autologous vein graft? Surgery 1982; 94:26-31. 13. YEAGER RA, HOBSON I1 RW, LYNCH TG, JAMIL Z, LEE BC, JAIN K, KEYS R. Analysis of factors influencing patency of polytetrafluoroethylene Drostheses for limb salvage. - J Sura Res 1982: 32:499-506. 14. JULIAN TB, LOUBEAU J , STREMPLE FJ. POlytetrafluoroethylene or saphenous vein as a femoropopliteal bypass graft? J Surg Res 1982; 32:l-6. 15. QUINONES-BALDRICH WJ, MARTINPAREDERO V, BAKER JD, BUSUTTIL RW, MACHLEDER HI, MOORE WS. Polytetrafluoroethylene grafts as the first choice arterial substitute in femoropopliteal revascularization. Arch Surg 1984; 119: 1238-1243. 16. BENNION RS, WILLIAMS RA, STABILE BE, FOX MA, OWENS ML, WILSON SE. Patency of autologous saphenous vein versus polytetrafluoroethylene grafts in femoro-popliteal bypass for advanced ischemia of the extremity. Surg Gynecol Obstet 1985; 160:239-242. 17. CHRISTENSON JT, BROOME A, NORGREN L, EKLOF B. Revascularization of popliteal and belowknee arteries with polytetrafluoroethylene. Surgery 1985; 97: 141- 149. 18. ASCER E, VEITH FJ, GUPTA SK, KRASOWSKI G, SAMSON RM, SCHER LA, WHITE-FLORES SA, SPRAYREGEN S. Six-year experience with expanded polytetrafluoroethylene arterial grafts for limb salvage. J Curdiovusc Surg 1985; 26:468-472. 19. VEITH FJ, GUPTA SK, ASCER E, WHITEFLORES S, SAMSON RM, SCHER LA, TOWNE JB, BERNHARD VM, BONIER P, FLINN WR, ASTELFORD P, YAO JST, BERGAN JJ. Six-years prospective multicenter randomized comparison of I

VOLUME 2 - 1988

No 1

ePTFE PROSTHESES IN HUMANS

autologous saphenous vein and expanded polytetrafluoroethylene grafts in infrainguinal arterial reconstructions. J Vasc Surg 1986; 3:104-114. 20. GUIDOIN R, KING M, BLAIS P, MAROIS M, GOSSELIN C , ROY P, COURBIER R, DAVID M, NOEL HP. A biological and structural evaluation of retrieved dacron arterial prostheses. NBS Special Report 1981; 601:29-129. 21. COUTURE J , GUIDOIN R , KING M, MAROIS M. Textile Teflon arterial prostheses: how successful are they? Canad J Surg 1984; 27575-582. 22. GUIDOIN R, GAGNON Y, ROY P, MAROIS M, JOHNSTON KW, BATT M. Pathologic features of surgically excised human umbilical vein grafts. J Vasc Surg 1986; 3~146-154. 23. GUIDOIN R , THEVENET #, MARY H , NOEL HP, MAROIS M, GOSSELIN C , KING M. Le sparksmandril comme prothese arterielle. Un concept ingenieux. un echec comdet. Oue faut-il en retenir? JMal Vasc i984; 9:277-283. . 24. FORMICHI M, JAUSSERAN J M , GUIDOIN R, MAROIS M. BERGERON P. GOSSELIN C. COURBIER R . Analyse de prothises arterielles en teflon microporeux apres exerkse chirurgicale. J Ma1 Vasc 1986; I 1 :248-255. 25. KEMPCZINSKI RF. Physical characteristics of implanted polytetrafluoroethylene grafts. A preliminary report. Arch Surg 1979; 114:917-919. 26. GEIGER G , HOEVELS J , STORZ L, BAYER HP. Vascular grafts in below-knee femoro-popliteal bypass. A- comparative study. J Cardiovasc Surg 1974: 25~523-539. 27. HANEL KC, MCCABE c , ABBOTT WM, FALLON J , MEGERMAN J . Current PTFE grafts. A biomechanical, scanning electron and light microscopy evaluation. Ann Surg 1982; 195:456-463. 28. ANSEL AL, JOHNSON JM. Prevention and management of polytetrafluoroethylene grafts. Complications in DeriDheral vascular reconstruction. A m J Surg 1982;*144:228-230. 29. CAMILLERI JP, PHAT VN, BRUNEVAL P, TRICOTTET V. BALATON A. FISSINGER JN. CORMIER JM. Surface healing and histologic maturation of patent polytetrafluoroethylene grafts implanted in patients for up to 60 months. Arch Pathol Lab Med 1985; 1091833-837. 30. CAMPBELL C D , BROOKS D H , WEBSTER MW, BOND1 RP, LLOYD JC, HYBES MF, BAHNSON HT. Aneurysm formation in expanded polytetrafluoroethylene prostheses. Surgery 1976; 79:491-493. 3 1. ROBERTS AK, JOHNSON N. Aneurysm formation in an expanded microporous polytetrafluoroethylene graft. Arch Surg 1978; 113:211-213. 32. COURBIER R, JAUSSERAN J M , REGGI M, C H I C H E G . Les protheses artkrielles en polytetrafluoroethylene. Premiers resultats cliniques. J M a l Vasc 1979; 4:151-155. 33. MOHR LL, SMITH LL. Polytetrafluoroethylene grafts aneurvsm. A reDort of five aneurysms. Arch 5urg 1980; i15:1457-1;170. 34. MARCEAU D, GUIDOIN R, CARDOU A, GOSSELIN C , KING M. Etude de la deformation circon-

35.

36.

37.

38.

39.

40.

41.

42.

43.

44.

45.

46.

47.

27

ferentielle des protheses arterielles en polytetrafluoroethylkne. Rev Europ Biotech Med 1982; 4~114-117. GRAHAM LM, BERGAN J J . Expanded PTFE vascular grafts. Clinical and experimental observations. In: Biologic and synthetic vascular prostheses. Stanley JC, Burke1 WE, Lindenauer SM, Bartlett RH, Turcotte JG, eds. New York: Grune and Stratton, 1982; 563-586. BERGAN J J , HARRIS JP, RUDO ND, YAO JST, VEITH F J , (eds). Update of PTFE grafts. In: Current critical problems in vascular surgery. New York: Appleton-Century Crofts, 1982; 105-122. VAUGHAN GD, MATTOX KL, FELICIANO DV, BEALL JR AC, DeBAKEY ME. Surgical experience with expanded PTFE as a replacement graft for traumatized vessels. J Trauma 1979; 19:403-408. GUIDOIN R, DOYON B, BLAIS P, DOMURADO D, BOYCE B, MAROIS M, MARTIN L, ROY J , GOSSELIN C. Effects of traumatic manipulations of graft sutures and host arteries during vascular surgery procedures. Res Exp Med 1981; 179:l-21. S H A H P M , I T 0 K, CLAUSS R H , BABU SC, REYNOLDS BM, STAHL WM. Expanded microporous polytetrafluoroethylene (PTFE) grafts in contaminated wounds: experimental and clinical study. J Trauma 1983; 23: 1030-1033. SHAH DM, LEATHER RP, CORSON JD, KARMODY AM. Polvtetrafluoroethvlene grafts in the rapid reconstructibn of acute contamiiated peripheral vascular injuries. A m J Surg 1984; 148:229-233. MOORE WS, MALONE J M , KEOWN K . Prosthetic actual graft material. Influence on neointimal healing and bicteremic infectability. Arch Surg 1980; 115: 1379-1383. GOEAU-BRISSONNIERE 0, PECHERE JC, GUIDOIN R, NOEL HP, COUTURE J . Experimental colonization of vascular grafts with staphylococcus aureus. Canad J Surg 1983; 26:540-545. MOORE WS, ROSSON CT, HALL AD, THOMAS AN. Transient bacteremia. A cause of infection in prosthetic vascular grafts. A m J Surg 1969; 117342-343, MOORE WS, ROSSON CT, HALL AD. Effect of prophylactic antibiotics in preventing bacteremic 1971; infection of vascular Drostheses. Surgery ~. 69:825-828. CHIGNIER E. GUIDOLLET J . HEYNEN Y. SERRES M, CLENDINNEN G, LOUISOT P, ELOY R. Macromolecular, histological, ultrastructural and immunocytochemical characteristics of the neointima developed within PTFE vascular grafts. Experimental study in dogs. J Biomed Mat Res 1983; 17:623-636. SELMAN SH, RHODES RS, ANDERSON JM, DePALMA RG, CLOWES AW. Atheromatous changes in expanded polytetrafluoroethylene grafts. Surgery 1980; 87:630-637. EGGLETON SPH, PALMER Y, STAMP G , BAlN JR, SETTLAGE RA, NEWCOMBE JF. Heterotopic ossification of an expanded polytetrafluoroethylene vascular graft. Brit J Surg 1986; 73: 159-160.

...