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Groupe Européen de Recherche sur les Prothèses appliquées à la Chirurgie Vasculaire (GEPROVAS)Department of Vascular Surgery and Kidney Transplantation, Les Hôpitaux Universitaires de Strasbourg, Strasbourg, France
Groupe Européen de Recherche sur les Prothèses appliquées à la Chirurgie Vasculaire (GEPROVAS)Department of Vascular Surgery and Kidney Transplantation, Les Hôpitaux Universitaires de Strasbourg, Strasbourg, France
Groupe Européen de Recherche sur les Prothèses appliquées à la Chirurgie Vasculaire (GEPROVAS)Department of Vascular Surgery and Kidney Transplantation, Les Hôpitaux Universitaires de Strasbourg, Strasbourg, France
Groupe Européen de Recherche sur les Prothèses appliquées à la Chirurgie Vasculaire (GEPROVAS)Laboratoire de Physique et Mécanique Textiles, Mulhouse, France
Adresse of correspondence: Pr Anne LEJAY, Department of Vascular Surgery and Kidney Transplantation, Les Hôpitaux Universitaires de Strasbourg, B.P. 426, 67091 Strasbourg Cedex, France. Tél: (33) 03.69.55.09.07 Fax: (33) 03.69.55.17.83
Groupe Européen de Recherche sur les Prothèses appliquées à la Chirurgie Vasculaire (GEPROVAS)Department of Vascular Surgery and Kidney Transplantation, Les Hôpitaux Universitaires de Strasbourg, Strasbourg, France
Type of Research: Multicenter retrospective cohort study
Key Findings: The analysis of 19 explanted new generations polyethylene terephthalate grafts presenting non-anastomotic degradations allowed the identification of two main degradation phenomena: 1/ decrease in the density of the meshing and 2/ local ruptures of the polyethylene terephthalate fibers.
Take home Message: Degradation seems to result both from anatomic constraints and intrinsic textile structure phenomena, reinforcing the need to keep studying degradation mechanisms in order to develop a substitute for vascular repair that would be performant in term of both compliance and durability.
Abstract
Objectives
The aim of this study was to analyze a series of new generations of explanted knitted polyethylene terephthalate (PET) vascular grafts (VG) presenting non-anastomotic degradations according to pre-operative computed tomography angiography (CTA) when available, in order to better understand the mechanisms leading to rupture.
Methods
Knitted PET explanted vascular grafts (EVG) were collected as part of the Geprovas European collaborative Retrieval Program. VG implanted after 1990 presenting a non-anastomotic rupture of the fabric were included. Clinical data and pre-explantation CTA data when available were retrieved for each VG. The ruptures were characterized by macroscopic examination and optical microscopy according to a standardized protocol.
Results
Nineteen explants were collected across 11 European centers, 13 were implanted as infra-inguinal bypasses, 3 at the aortic level and 1 as an axillobifemoral bypass. Mean implantation duration was 9.2 years.
Pre-explantation CTA were available for 8 VG and showed false aneurysms at the adductor canal level on 4 VG, at the inguinal ligament level on 2 VG, and in the proximal or middle third thigh level on 3 VG.
Examination revealed longitudinal ruptures on 9 EVG, transversal ruptures on 15 EVG, 45°-oriented ruptures on 5 EVG, V-shaped ruptures on 7 EVG and punctiform ruptures on 2 EVG. Ruptures involved the remeshing line on 11 EVG, the guideline on 10 EVG, and the crimping valley on 15 EVG.
At microscopic level 2 main degradation phenomena could be identified: decrease in the density of the meshing and local ruptures of the PET fibers. Fourteen EVG presented a loosening of the remeshing line and 17 EVG an attenuation of the crimping.
Conclusion
New generations PET VG degradation seems to result both from anatomic constraints and intrinsic textile structure phenomena.
One of the major steps of vascular surgery was the introduction of synthetic vascular grafts (VG) seventy years ago. Expanded polytetrafluoroethylene (ePTFE) and polyethylene terephthalate (PET) are the main materials used to build the current generations of VG [
]. If synthetic VG provide acceptable results for the reconstructions involving middle-sized and large diameter vessels, there is still no strong recommendation concerning which synthetic material to favor in absence of suitable autologous material for small diameter vessels [
Editor's Choice - 2017 ESC Guidelines on the Diagnosis and Treatment of Peripheral Arterial Diseases, in collaboration with the European Society for Vascular Surgery (ESVS).
]. One could fall in the trap of summarizing that PET VG degradations only addressed old VG generations. Ruptures on warp-knitted PET VG have however still been observed, highlighting the need to carry on with explanted VG investigations. [
New generations of PET VG have been proposed to better mimic arterial mechanical properties to enhance their compliance by introducing the concept of thin-wall VG. We previously demonstrated that they did not fulfill expectations in terms of compliance [
] but the long-term durability of these thinner structures remains unclear. Previous reports concluded that new generations of PET VG are still subjected to long-term degradation mechanisms [
]. Accordingly, the role of material surveillance still remains essential in order to better understand the overall mechanisms of degradation and improve next generations of device.
We already know that VG degradation is multifactorial associating the design of the VG as well as post-implantation factors such as chemical and mechanical factors. Retrospective analysis is difficult but data such as imaging results provided during the life-duration of the VG could help for analysis. This is the reason we tried to get computed tomography angiography (CTA) data since it could provide objective and analyzable data allowing a better understand these phenomena of VG degradation.
The aim of this study was to analyze a series of new generations of explanted knitted PET VG presenting non-anastomotic degradations according to pre-operative CTA when available, in order to better understand the mechanisms leading to rupture.
METHODS
The explants
The explanted PET VG were collected as part of the Geprovas European collaborative Retrieval Program. The analysis focused on knitted explanted vascular grafts (EVG) presenting a rupture of the fabric. VG implanted before 1990 were excluded as they were not considered as part of the new VG generations.
Clinical data were retrieved for each explant, indexing the surgeon who explanted the VG, the model of the VG, the reason for implantation, the site and the duration of implantation, and the reason for explantation. When available, pre-explantation CTA was systematically analyzed.
Explant processing and analysis
The VG were fixed in a formalin solution right after explantation in the operating room. All specimens were studied according to our ISO 9001-certified standard protocol [
(5) After cleaning, VG were once again photographed and analyzed macroscopically to determine the area where the ruptures occurred.
-
(6) The analysis was completed by carrying out a microscopical examination using a Keyence VHX-600 digital microscope (Keyence France, Courbevoie, France).
Classification of the observed ruptures
Each rupture was classified according to its shape and localization along the tubular structure (remeshing line, guideline, crimping). Five different rupture shapes were considered in the frame of this work: longitudinal, transversal, 45° oriented, V-shaped and punctiform. When a rupture presented combined mechanisms, each observed rupture shape was classified individually. Independently of the ruptures, signs of aging degradation of each textile knitted structure was identified (local mesh opening, remeshing line loosening, loss of crimping). Two investigators performed the analysis on all the explants.
CTA analyses
When pre-explantation CTA was available, a 3D reconstruction was performed in order to understand the VG in-vivo conformation and indirectly the eventual mechanical stresses that could have been applied on the VG. For each CTA, the implantation site, the location of the false aneurysm, the presence of small dilatation along the graft and remarkable events were evaluated. Therefore, it was possible to study the observed ruptures on the VG in correlation with the in-vivo conditions.
RESULTS
Explants characteristics
From January 2011 to July 2020, 336 PET VG were collected as part of the European collaborative retrieval program. Twenty-one of them were knitted VG presenting a rupture of the fabric. Two of them were implanted before 1990 and therefore excluded. In total, 19 EVG collected from 11 European centers were analyzed.
The clinical characteristics are presented in Table 1A.
Table 1A(A) Clinical characteristics and structural properties of explanted vascular grafts. VG: vascular graft, NA: not available.
We collected 7 different models of VG from Perouse Medical (Ivry Le Temple, France), InterVascular (La Ciotat, France), Vascutek (Inchinnan, Scotland), C.R.Bard (Murray Hill, New Jersey, USA), and Baxter International (Deerfield, Illinois, USA). Graft models were anonymized and substituted with numbers 1 through 7 in the table.
Nine of them were thin-wall VG (wall thickness < 0,4mm). Eighteen VG were coated (4 with gelatin and 14 with bovine collagen). Eight VG had an external velour surface only with a non-velour inner surface, and one VG was double velour. Nine VG were glutaraldehyde and formaldehyde free.
The mean duration of implantation was 9.2 years (range: 2.3 – 22.8 years).
Thirteen VG were implanted as infra-inguinal bypasses (11 above-the-knee femoral-popliteal bypasses, 1 femoro-femoral bypass, 1 crossed femoro-femoral bypass); 3 VG were implanted at the aortic level (1 aortobifemoral bypass, 1 aortobiiliac bypass and 1 aorto-femoral bypass); 1 VG was implanted as an axillobifemoral bypass.
The main reason for explantation was a non-anastomotic rupture with false aneurysm (n=16), infection (n=1) and thrombosis requiring redo procedure (n=1). Reason for explantation was missing in one case. When VG were explanted for non-anastomotic rupture or thrombosis requiring redo procedure, infection was excluded based on the clinical reports provided by the surgeon as well as the CTA data when available.
CTA reconstructions
Pre-explantation CTA images were available for 8 VG: 6 femoral-popliteal bypasses, 1 aorto-femoral bypass, 1 cross femoro-femoral bypass. The results of CTA analysis are listed in Table 1B.
Table 1B(B) Conclusions drawn from analysis of pre-explantation computed tomography angiography of the vascular grafts. VG: vascular graft.
VG
Site of implantation
False aneurysm location
Presence of small dilatation along the bypass
Remarkable event
VG2
above-the-knee femoral-popliteal
adductor canal
no
no
VG3
above-the-knee femoral-popliteal
adductor canal
no
the distal anastomosis seemed to pull on the popliteal artery
False aneurysms were observed at the adductor canal level on 4 EVG (Figure 1A), at the inguinal ligament level on 2 EVG (Figure 1B), and in the proximal or middle third thigh level on 3 EVG. We observed on 3 CTA more than one false aneurysm along the EVG.
Figure 1(A) Reconstruction of the pre-explantation computed tomography angiography of VG3: femoral popliteal above the knee bypass presenting a false aneurysm at middle third thigh level, in the adductor canal. The distal anastomosis seems to pull on the popliteal artery. Duration of implantation: 6,8 years.(B) Reconstruction of the pre-explantation computed tomography angiography of VG11: cross femoro-femoral bypass presenting a left false aneurysm, a smaller right femoral false-aneurysm and a kinking in the middle of the prosthesis. Side-by-side comparison of the explanted graft before cleaning. Duration of implantation: 3,5 years.
On one CTA it seemed that the distal anastomosis of the VG exerted a traction on the native artery (Figure 1A). One CTA displays a kinking on the VG that was also observed on the corresponding EVG (Figure 1B).
Type of degradations
After cleaning, all EVG revealed one or several non-anastomotic ruptures. Observations on degradations are presented in Table 2.
Table 2
Table 2
The mean length of the collected EVG was 115mm. Fifteen EVG presented more than one rupture. Fourteen EVG presented additional initiations of ruptures outside of the ruptured areas. The macroscopic analysis revealed longitudinal ruptures on 9 EVG, transversal ruptures on 15 EVG, 45°-oriented ruptures on 5 EVG, V-shaped ruptures on 7 EVG and punctiform ruptures on 2 EVG. Ruptures with multiple mechanisms were observed on 11 EVG. Six EVG presented ruptures due to the explantation process. One EVG presented ruptures due to the insertion of an endoprosthesis inside the graft.
Ruptures involved the remeshing line on 11 EVG, the guideline on 10 EVG and the crimping valley on 15 EVG. An anastomotic rupture was observed on one EVG.
All the transversal ruptures observed occurred on the crimping (Figure 2).
Figure 2(A) Microscopic examination (x20) of a transversal rupture on the crimping of VG6 (above-the knee femoral-popliteal bypass with a duration of implantation of 8,2 years) with schematic representation of potential traction forces exerted on the damaged area.(B) Microscopic examination (x50) of VG3 (above-the-knee femoral-popliteal bypass with a duration of implantation of 6,8 years) showing broken filaments along the guideline.(C) Microscopic examination (x30) of VG4 (above-the-knee femoral-popliteal bypass with a duration of implantation of 4,8 years) showing broken filaments forming a transversal rupture following the crimping valleys.
At microscopic level 2 main degradations phenomena could be identified: (1) decrease in the density of the meshing (Figure 2A); (2) local ruptures of the PET fibers (Figure 2B). Aging degradations were seen in majority on the crimping valleys and the remeshing line, with 14 EVG presenting a loosening of the remeshing line (Figure 3) and 17 EVG presenting an attenuation of the crimping. One EVG also presented loosed meshes outside of those areas.
Figure 3(A) A V-shaped rupture on VG7 (femoro-femoral bypass with a duration of implantation of 7,9 years) with simulation of the graft aspect before rupture and schematization of the combination of potential traction, flexion and torsion forces exerted on the textile.(B) Macroscopic examination (x30 and x50) showing loosened meshes on the edges of the rupture, mostly on the remeshing line
One explant (VG9) presented only one punctiform rupture with clean edges (Figure 4). The rupture was circular. Its diameter included 5 rows of meshes and the center of the hole was located on top of the crimping. After cleaning, the borders were characterized by yarn fuzzing. Broken filaments appeared as pulled out through the external surface. The tongue like pattern of some broken filaments suggested local ruptures due to fatigue.
Figure 4(A) Macroscopic observation of VG9 (above-the-knee femoral-popliteal bypass with a duration of implantation of 3,2 years) after cleaning, presenting a single circular rupture with clean regular edges. (B) Microscopic examination (x50) showing broken filament in a tongue-like pattern all around the edges of the rupture.
One explant (VG12) presented an endoprosthesis implanted inside the graft (Supplemental Figure 1). The ruptures observed on the graft’s textile were attributed to the stents of the endoprosthesis.
DISCUSSION
The main findings presented in the frame of this study point out that new generations of VG can still undergo degradations despite improvement efforts performed in the manufacturing technology. Previous reports of graft degradations led to modifications in textile design such as the selection of warp-knitted and woven structures [
]. Newer polyester knitted VG implanted after 1990 in this study are all warp-knitted prostheses. They introduce the concept of thin-wall VG, that are supposed to offer better compliance and conformability with a better resemblance to native arteries. Other new-generations characteristics are the absence of velour structure or the limitation to external velour-structure; and a coating agent (either bovine collagen or hydrolyzable gelatin).
Previous VG generations failures have been described as a limited number of longitudinal failures. [
]. Observed degradations in this study ranged from a majority of transversal ruptures, to transversal, V-shaped and 45° ruptures, and two punctiform ruptures. Frequent areas of degradations were identified as remeshing lines, guidelines and crimping valleys. The mechanisms of degradation at microscopic level were either decrease in density of the meshing or local rupture of textile fibers. As several models have been included in the analysis, one can conclude that this issue can concern all the currently available models.
One key finding here is that the degradation tends to occur preferentially in some graft zones where the textile VG was already weakened at manufacturing level like remeshing lines, or crimping peak or valley. A remeshing line is a zone which presents a discontinuity regarding the way yarns are crossed in the knitted construction. While the line is necessary in order to obtain a tubular knitted shape, the local structural change induces stress concentration.
With respect to crimp peaks and valleys, the yarns located in these zones have been pressed against the crimp molding device and heated above vitreous transition temperature. This has locally fragilized the structure. These observations have already been made in the past. We previously demonstrated that ruptures observed on explanted knitted PET VG occurred on these areas that could be qualified as areas of weakness [
]. The guideline and the remeshing line have therefore been identified as weak spots potentially leading to longitudinal ruptures. Further chemical and mechanical analyses concluded that these areas of weakness could stem from the manufacturing steps, inducing alterations in the PET yarns and resulting in premature ageing of the VG structure. [
No difference was seen between the grafts that could explain the tendency of graft degradation according to the duration of implantation. However, it is always difficult to identify the precise cause of the degradation, as several factors can be involved like VG deformation stress (extension, flexure, torsion), biodegradation by tissue fluids and enzymes, or textile wear when the VG is in contact with an abrasive zone, or locally compressed by a neighbor vessel or outgrowing body part. [
] However, imaging can help interpreting the degradation cause. It can help to establish a correlation between the degradations observed and the position of the degraded zone in the body. This information is of great interest for VG manufacturers and clinicians, in order to improve the quality of the devices at manufacturing level and the way they are used in clinical practice.
The rupture patterns observed in the frame of this work pointed out several rupture mechanisms, which can be partly explained by the stress applied to the VG in vivo. The main stress patterns applied to a prosthesis are extension, flexure and torsion.
First, the transverse ruptures can be typically caused and explained by the involvement of a flexure stress. Actually, when the VG is bent, fibers located at the level of the VG external curvature undergo locally high extension stress. As the loading is cyclic under pulsed cardiac flow, the mesh starts to become loose and the fibers tend to break presenting a tongue shaped fatigue rupture facies. The rupture initiated at the top of the curvature tends then to propagate radially along the fragilized crimp valleys or peaks as can be seen in Figure 2. Second, if some additional stress like extension is applied to the VG, the direction of the initial radially oriented rupture is modified and becomes inclined. At last, the V-shaped ruptures can suggest the involvement of torsion stress since these are not symmetrically shaped, as seen in Figure 3.
One key finding of this work is that this combination of stress applied to the VG can be partly explained from the CTA images. As shown in the analysis of pre-explantation CTA, a recurrent location for false-aneurysms of femoral-popliteal bypasses tends to be the adductor canal. The adductor canal is an anatomic area known for the strong mechanical constraints it applies on the superficial femoral artery. [
In vivo MR angiographic quantification of axial and twisting deformations of the superficial femoral artery resulting from maximum hip and knee flexion.
Journal of Vascular and Interventional Radiology.2006; 17: 979-987
] There, the VG could undergo axial compression and extension, radial compression, flexion and torsion. Unlike the natural superficial femoral artery, VG are lacking elastic fibers, thus resisting less efficiently to mechanical forces. The same process can be hypothesized for the inguinal ligament area [
]. Moreover, some of the VG presented a local creasing that could have been present before explantation as can be seen in some CTA reconstruction. If the VG was bent in vivo because of anatomic disposition, the blood flow inside the VG would circulate in a curved line, producing a pulsed traction at both extremities of the curve. The knitted textile would have been strongly solicited in these areas (especially on the outward of the curve where the traction constraint is the most prominent), creating a fatigue of the PET fibers and inter-filament friction leading to rupture. The curved flow would also create a cyclic flexion inside the creasing that would generate more flexion forces in the fibers.
Understanding the mechanisms of VG degradation and therefore avoid late VG rupture requires investigating each step that could be the cause of later degradation, together with textile engineers, manufacturing engineers and physicians. First, carrying out mechanical strength tests on virgin VG of different models, before and after compaction process and thermic treatment, would allow a better understanding of the mechanisms of rupture related to the weaknesses induced by the manufacturing steps of VG. Another prospect would be to carry out histological analysis on these types of EVG in order to assess in-vivo interactions with biological tissues, the graft encapsulation and healing [
], the interaction with the coating and with the textured fibers, especially in the area of the textile rupture. Although experience allows us to rule out degradations induced by explantation techniques and surgical handling of the VG, some lesions can be of difficult interpretation. In the case of the punctiform rupture on VG9 however, macroscopic and microscopic analysis alone do not allow us to conclude towards a specific mechanism of degradation.
VG failures prevalence is still under-estimated to this day and difficult to truly evaluate as only few cases are reported, highlighting de need to keep studying vascular explants. The main interest of our retrieval program is to allow the analysis of a significant number of VG to be able to point out mechanisms of ageing of different models of devices and to learn about the concept itself. However, a study based on a retrieval program has unavoidable limitations that must be taken in consideration when interpreting the results since one may consider that the probability to find structural lesions onto VG for a complication is higher than on uncomplicated VG. Moreover, the analysis must considered that lesions could have been created during the explantation of the VG. However, our expertise and the fact that all analyses of EVG are performed using a multistep standardized protocol systematically associating clinicians and engineers can exclude the risk of mis-interpretation.
CONCLUSION
Explant analysis tends towards the conclusion that VG degradation results both from anatomic constraints and intrinsic textile structure. The combination of stress in traction, flexion and torsion with the cyclic arterial flow exerts strong pressures on the warp-knitted textile in localized area of weaknesses, producing a global loosening of the mesh and the loss of the crimping, then leading to rupture. These degradations still exist in today’s generation of VG, reinforcing the need to keep studying their mechanisms in order to develop a substitute for vascular repair that would be performant in term of both compliance and durability. Pre-operative imaging can become a great tool in both the manufacturing and clinical process as it is shown to help in the interpretation of degradation mechanisms.
Funding
Financial support provided by Eurometropole de Strasbourg and the Région Grand’Est.
Acknowledgements
We acknowledge the European Society of Vascular Surgery and the Société Française de Chirurgie Vasculaire et Endovasculaire, who support our explant analysis program.
Editor's Choice - 2017 ESC Guidelines on the Diagnosis and Treatment of Peripheral Arterial Diseases, in collaboration with the European Society for Vascular Surgery (ESVS).
In vivo MR angiographic quantification of axial and twisting deformations of the superficial femoral artery resulting from maximum hip and knee flexion.
Journal of Vascular and Interventional Radiology.2006; 17: 979-987
Collaborators: Samuel BOUTTIER (Clinique Claude Bernard, Ermont, France), Pierre CARLIER (Centre Médico-Chirurgical Floréal, Bagnolet, France), Jacques CHEVALIER, (Hôpital Saint-Philibert, Lomme, France), Sébastien DEGLISE, (Centre Hospitalier Universitaire Vaudois, Lausanne, Switzerland), Denis GARNIER (Clinique générale d'Annecy, France), Adrien HERTAULT (Centre Hospitalier de Valenciennes, France), Rémi LAURENT (Hôpital Saint-Philibert, Lomme, France), Boris POSTAIRE (Centre Hospitalier Universitaire de Nantes, France), Pascal VERNON (Centre Hospitalier de Saint-Quentin, France), Renaud VIDAL (Hôpital La Casamance, Aubagne, France).
This multicenter retrospective analysis of 19 explanted new generations polyethylene terephthalate grafts identified two main degradation phenomena: decrease in the density of the meshing and local ruptures of the fibers. These findings reinforce the need to keep studying degradation mechanisms in order to develop an ideal vascular substitute.
Clinical relevance
In this study, the analysis of explanted new generations polyethylene terephthalate grafts presenting non-anastomotic lesions allowed the identification of two main degradation phenomena: a decrease in the density of the meshing and local ruptures of the polyethylene terephthalate fibers. This highlights that both anatomic constraints and intrinsic textile structure phenomena are involved in degradation phenomena.
This study highlights the need to keep studying the degradation mechanisms in order to develop compliant and durable vascular substitutes.
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