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Eur J Cardiothorac Surg 1998;13:259-265
© 1998 Elsevier Science NL

Tissue response to biomaterials used for staple-line reinforcement in lung resection

A comparison between expanded polytetrafluoroethylene and bovine pericardium¹

^a Cardiothoracic and Vascular Surgeons, Ltd, 6036 North 19th Avenue, Suite 405, Phoenix, AZ 85015, USA
^b W.L. Gore Associates, Inc, Flagstaff, AZ 86002, USA

Received 1 October 1997; received in revised form 29 December 1997; accepted 14 January 1998.

Corresponding author. Tel.: +1 602 2421200; fax: +1 602 2420267.

	Abstract

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Objective: A study in a canine model of lung-reduction surgery evaluated the tissue response to polytetrafluoroethylene (ePTFE) and bovine pericardium (BP) used for staple-line reinforcement. Methods: In each of ten dogs, BP was placed in one lung and ePTFE in the other. The implants were retrieved at 30, 95, or 167 days after implantation and studied histologically. The connective tissue covering the implants was measured and analysis of variance was used to compare results with the two materials. Results: At 30 days, the BP specimens showed focal chronic inflammation and thin tissue coverage, whereas the ePTFE specimens had no focal inflammation and thick tissue coverage. At 95 and 167 days, the inflammation in the BP specimens had resolved, but tissue coverage remained minimal, and there was no resorption of the BP. In the ePTFE specimens, tissue coverage had increased. Analysis of variance comparing representative tissue specimens showed that the tissue encapsulating the ePTFE was significantly thicker than that surrounding the BP (P<0.0001). No air leaks, staple-line disruptions, or infections occurred in the study. Conclusions: Neither ePTFE nor BP is resorbable. Both materials have been used successfully, without resultant infections, for clinical staple-line reinforcement. The more favorable tissue response to ePTFE observed in this study may have clinical ramifications. Comparative clinical studies of the two materials are needed.

Key Words: Bovine pericardium • Expanded polytetrafluoroethylene • Lung-volume reduction • Histopathology • Surgical stapling

	Introduction

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With the renewed interest in lung-volume reduction surgery for the treatment of emphysema [1] has come recognition for a need to reinforce the staple lines inserted at excision of lung tissue in order to decrease the risk of postoperative air leaks [2]. Several materials have been used for staple-line reinforcement, including excised pleura [3], fibrin glue [2], polydioxane ribbon [4], Teflon felt [5], and polyglycolic acid fabric [6].

The most commonly used material is glutaraldehyde-fixed bovine pericardium (BP) strips (Peri-Strips or Peri-Strips Dry, Bio-Vascular, St. Paul, MN) [2]. Before use, Peri-Strips must be soaked in saline for an adequate period and rinsed to remove the propylene oxide preservative. They must then be kept from drying out before implantation. The strips are attached to the surgical stapler with a polypropylene suture, and both the suture and a polyethylene backing attached to the strips must be removed after the stapler has been fired. With Peri-Strips Dry, a gel must be applied to the BP to rehydrate it and create a temporary bond between the two BP strips and the two inner surfaces of the surgical stapler. After the gel is applied, the stapler is placed over the BP strips and locked. The plastic holder containing the BP strips is pulled away from the stapler, leaving behind the stapler clamped onto the strips and a plastic sheet between the strips. The stapler must be clamped onto the BP strips for at least 2 min to allow the gel to attach the strips to the stapler. Afterward, the stapler is unlocked and the plastic sheet between the strips is removed; the stapler, with the BP strips ‘glued’ to it, is then ready for use.

These multiple preparatory steps for use of BP strips require considerable time and effort on the part of both the surgeon and the operating room staff. In addition, although virtually no information is available on the host reaction to BP used in lung resection, the material has been associated with calcification and extensive inflammatory reactions in cardiac applications [7] [8] [9] [10] [11] [12]. Therefore, for reasons relating to both convenience and patient outcome, there has been interest among surgeons performing lung-reduction surgery in a staple-line reinforcement material that is both easy to use and biocompatible.

A prosthetic staple-line reinforcement product made of expanded polytetrafluoroethylene (ePTFE; Seamguard Staple Line Reinforcement Material, W. L. Gore & Associates, Flagstaff, AZ) is now available for clinical open and thoracoscopic procedures [13]. The product consists of a pair of ePTFE sleeves that are slipped over the arms of the surgical stapler. The sleeves fit snugly on the stapler arms; no adhesive gel is necessary to secure them. Once the sleeves are in place, the stapler is positioned appropriately and fired. Before the stapler is released, the excess ePTFE from the three panels of the sleeves that have not been stapled through is removed by grasping it from either end and peeling it from the stapler arms along tear lines. In thoracoscopic procedures, this can be easily accomplished with grasping forceps. The stapler is then released. There is no suture or backing material to remove from the ePTFE sleeves. In addition, because the sleeves are not fixed in glutaraldehyde and contain no additives or preservatives, no presoaking or rinsing is required.

To our knowledge, no studies comparing BP and ePTFE used for staple-line reinforcement have been published. We assessed the tissue response to both these materials after pulmonary excision and stapling in a canine model of lung-reduction surgery.

	Materials and methods

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U.S. National Institutes of Health guidelines for the care and use of laboratory animals (NIH Publication no. 86-23, Rev. 1985) were observed. Ten adult mixed-breed hounds of either sex and weighing 20–25.5 kg were used. In each dog, BP staple-line reinforcement material was placed in one lung and ePTFE staple-line reinforcement material in the other. The lung in which each material was implanted was randomly determined.

The dogs were placed under general anesthesia and maintained on intermittent positive-pressure ventilation using isoflurane in 100% oxygen. A median sternotomy was performed. The basal borders of multiple lobes of one lung were identified. A linear stapling device fitted with one of the staple-line reinforcement materials was used to excise a small section of lung (2x4 cm) from the apex of each lobe. In addition, overlapping (crossed) staple lines were placed at the apex of the cranial lobe. The chest cavity was filled with warm sterile saline, the stapled portions of the lung were submerged, and the staple line was checked for air leaks during the inspiratory cycle of the ventilator. The stapler was then fitted with the other staple-line reinforcement material, and the stapling procedure was repeated in multiple locations in the opposite lung. Subsequently, air and fluid were evacuated, the chest incision was closed, a thoracostomy tube was inserted into the pleural space, and the dog was allowed to recover from the procedure. Antibiotics were administered for 14 days postoperatively. Sedatives and analgesic agents were given as needed during the immediate postoperative period.

The dogs were sacrificed approximately 30 days (five dogs), 95 days (two dogs), and 167 days (two dogs), postoperatively. One dog died of a non-implant-related pneumothorax on postoperative day 4. In all dogs, the thorax was thoroughly inspected at necropsy. The implants were identified and excised, along with several centimeters of adjacent lung tissue. The tissue was fixed in buffered formalin.

For the histologic studies, 3–6 representative tissue blocks were obtained from explants containing each prosthetic material and processed in paraffin. Multiple sections were cut from each block and stained with hematoxylin and eosin and Milligan’s trichrome. The sections were examined under light microscopy to assess overall tissue response, including foreign-body response, the presence of inflammatory cells and mineralization, and evidence of infection or periimplant pulmonary problems. The fibrovascular connective tissue covering the implants was then measured at five sites. To decrease bias, the first measurement was always taken at the proximal end of the implant strip, and the next four were obtained at 1-mm intervals from that end ( Fig. 1 ). Tissue thickness was expressed in µm. A total of 29 BP implant sections and 40 ePTFE sections were measured. Fewer BP sections were assessed because many of the specimens showed substantial deformity (curling back) of the prosthetic material. A mean capsular-tissue thickness for each implant type (BP and ePTFE) was calculated by averaging the data from all sites. Analysis of variance (ANOVA) with log transformation of the data to correct for the increased variability at greater thicknesses was used to compare tissue coverage of the two prosthetic materials.

View larger version (83K): [in this window] [in a new window]   Fig. 1. Drawing of implant site showing the sites of measurement of the thickness of tissue encapsulating the BP and ePTFE staple-line reinforcement materials. The first measurement was always made at the proximal end of the most intact implant strip in the specimen. The other four were done at 1-mm intervals (arrows), as determined with use of the ocular micrometer in the microscope.

	Results

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Gross examinations of all samples obtained at the three explantation times (30, 95, and 167 days) showed a focal, moderate fibroplasia along the pleural surface of the chest wall over the implants. These findings did not vary according to the type of staple-line reinforcement material used. In all animals and at all evaluation times, the ePTFE reinforcement material was mostly or, in some instances, entirely encapsulated with a glistening, smooth, fibrovascular connective tissue of variable thickness ( Fig. 2 ). Substantially less tissue overlaid the BP strips from the contralateral lung ( Fig. 3 ). Attachment of the ePTFE-reinforced staple line (by means of fibrinous or fibrous adhesions) to either the chest wall (thoracic inlet), pericardium, or mediastinal pleura was present in varying degrees. On the other hand, attachment of surrounding tissue to the staple line reinforced with BP was rarely observed. Occasionally, the cranial lobe (thoracic inlet) specimens in which the implants had been present for at least 90 days had fibrous tissue adhesions.

View larger version (95K): [in this window] [in a new window]   Fig. 2. Gross photograph of a freshly explanted 167-day specimen of resection site reinforced with ePTFE staple-line reinforcement material. The implant is contiguous with normal lung tissue, and large areas have lung tissue extending over the implant surface toward the free margin.

View larger version (95K): [in this window] [in a new window]   Fig. 3. Gross photograph of a freshly explanted 167-day specimen of resection site reinforced with BP staple-line reinforcement material obtained from the contralateral lung of the same dog from which the ePTFE specimen in Fig. 2 was taken. The implant is still clearly visible, with no evidence of resorption. A thin membranous tissue covers the implant, most notably at the staple heads. There is marked deformity and curling of the distal margins of the material.

The response to the ePTFE suture-line reinforcement material at 30 days was characterized by the presence of a fibrovascular connective tissue that extended up and over the proximal borders adjacent to the lung. The cells were predominately fibroblasts and macrophages in a one- to two-cell layer. There were also large areas of connective tissue alone, with no cellularity. Few multinucleated foreign-body giant cells were observed; large areas had none at all. The tissue completely encompassed the ePTFE, extending over the distal edges to form a fibrocollagenous seal of the original resection line. There was also collagen deposition along the staple tracks and in the interstices of the biomaterial.

The tissue responses in the 95- and 167-day explants were similar to each other, but as in the 30-day implants, there were considerable differences in the responses to the two prosthetic materials. The BP samples showed various degrees of deformity of the material, mild cellular infiltration, and almost no degradation of the bovine collagen fibrils. In many instances, even at 167 days after implantation, only a thin line of mesothelial cells with a minimal submesothelial connective tissue component lined the superficial surfaces of the implants ( Fig. 4 ). Along the deep surfaces of the implants, the pulmonary parenchyma was often directly adjacent to the BP collagen fibrils, with little to no fibroplasia establishing a strengthening continuity between the lung and the BP reinforcement material. The lateral borders of the material were deformed and often no longer in contact with the surface of the lung; instead, they had retracted, creating flaps that offered no support of the original staple line ( Fig. 3).

View larger version (95K): [in this window] [in a new window]   Fig. 4. Light photomicrograph of a BP explant obtained after 167 days of implantation. Milligan’s trichrome staining shows the BP as a folded, dark-green linear band at the surface of the lung. Both strips of the material are curled back on themselves. A thin, wispy layer of poorly organized fibrous tissue partly covers the upper sleeve. Much of the deep surface of the implant is in contact with the underlying pulmonary parenchyma. Original magnificationx3.25.

The 95- and 167-day ePTFE specimens had more extensive tissue coverage (encapsulation) than the BP specimens explanted from the contralateral lung at the same time. Typically, there was a moderate amount of well-organized fibrocollagenous tissue that extended along the superficial surface, over the distal tips of the material, and into the area between the two arms of the material ( Fig. 5 ). The cellular response at the tissue-implant interface was static and bland, generally consisting of a few mononuclear cells (scattered macrophages and fibroblasts) and rare giant cells. Collagen fibril deposition occasionally extended into the interstices of the ePTFE material, thereby creating contiguity between the soft tissue and the implant. There was no cellular penetration into the structure of the prosthetic material. In some samples, the implant surface was lined with pulmonary parenchyma.

View larger version (95K): [in this window] [in a new window]   Fig. 5. Light photomicrograph of an ePTFE explant obtained after 167 days of implantation from the contralateral lung of the dog from which the specimen in Fig. 4 was taken. Normal lung tissue extends from the deep ends of the implant strips over about 40% of the superficial surface of the ePTFE. Beyond this, a well-developed fibrous capsular sheath extends over the exposed edge. The adjacent pulmonary structures (vessels, alveoli, terminal bronchioles, and pleura) are unremarkable. Milligan’s trichrome staining, original magnificationx3.25.

View larger version (10K): [in this window] [in a new window]   Fig. 6. Mean log thickness (+95% CI) of fibrous tissue capsule surrounding BP compared with that surrounding expanded polytetrafluoroethylene ePTFE staple-line reinforcement material in a canine model of lung-reduction surgery.

	Discussion

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Assessment of the 30-day explants from the dogs in which BP was implanted indicated the presence of a chronic inflammatory response. There was also some cellular penetration between the bovine collagen fibrils and evidence of collagenolysis and phagocytosis. All these observations are consistent with the early phases of cell-mediated resorption, the process that occurs in host tissue in which a resorbable suture has been placed [14]. Interestingly, however, none of the BP specimens obtained at 95 or 167 days showed any progression of resorption. The strips were structurally intact, although many were wrinkled and curled back on themselves, resulting in less contact between the implant and lung. By the later evaluation times, the chronic inflammatory responses had subsided. There was little fibroplasia surrounding and encapsulating the BP-reinforced staple line.

It is unclear why the lung tissue reacted to the BP in this manner, but cytotoxicity of residual glutaraldehyde or propylene oxide in the BP fibers may have been involved. Xenograft materials used for implantation in humans, including BP, are tanned (fixed) with glutaraldehyde to limit immunologic reactions and strengthen the prosthesis [8]. The materials are then packaged in a preservative solution and must be rinsed carefully with sterile saline before use. Numerous studies investigating the calcification and mechanical failure of glutaraldehyde-fixed BP heart valves [7] [8] [10] [12] [15] [16] [17], as well as reports on extensive inflammatory reactions to BP used as a pericardial substitute [9] [18] and to repair congenital heart defects [11], have implicated the glutaraldehyde fixation in the host reaction to these prostheses.

Depending on storage conditions (amount of light exposure and ambient temperature) and pH, glutaraldehyde can form large polymeric structures [19]. If such structures are present in a tanning solution used to process BP, they may become ‘caught’ in the pericardial fibers and not be adequately washed out during the preimplantation rinse. Under physiologic conditions, these polymers may degrade and release active, cytotoxic glutaraldehyde into the periimplant tissues. This could evoke an inflammatory response, such as that observed in the BP samples obtained 30 days after implantation in this study.

A continuous low-rate release of glutaraldehyde and residual preservative may also have been responsible for the minimal fibroplastic tissue encapsulation of the BP strips. Studies of aldehyde-treated vascular and pericardial prostheses of biologic origin [20] [21] have found that such release inhibits endothelial cell ingrowth on the surface of those devices. Any agent that inhibits the mechanics of normal granulation (for example, by impeding fibroblast and endothelial cell migration) will disrupt deposition of extracellular matrix proteins, such as type I and III collagen and thereby delay or eliminate normal processes of wound healing, including inflammation, angiogenesis, fibroplasia, and wound contraction [22] [23].

Because of concern about medical products made with bovine material, the World Health Organization (WHO) convened an international group of experts March 24–26, 1997, for a consultation on transmissible spongiform encephalopathies (TSE) in cattle [24]. The group confirmed the need for continued research on TSE. The consultation also made the following recommendation: "Whenever possible, cattle (bovine) sources should be avoided for the preparation of medicinal products and devices; other animal species naturally affected by a TSE should likewise be avoided as an alternative source."

The wound-healing response in the periimplant lung tissues in which the ePTFE material had been implanted in this study was similar to what has been observed, experimentally and clinically, in other ePTFE implantation sites [25] and was substantially different from the response in the tissues surrounding the BP strips. In the ePTFE samples, there was a static mononuclear cell response that resulted in an interfascial cellular layer of 2–4 cell diameters. By 30 days after implantation, a variably thick fibrocollagenous stroma had encapsulated most of the ePTFE-reinforced staple line. Examination of specimens obtained at 95 and 167 days showed that this capsule continued to thicken so that the staple line became integrated into the surrounding tissue. A statistical analysis showed that the capsule around the ePTFE implants was significantly thicker than that around the BP implants. This fibroplasia probably added strength to the original resection line and considerably decreased the amount of material exposed along the pleural surface. There was no evidence of a chronic inflammatory response in the tissue adjacent to the ePTFE implants, and the foreign-body response was minimal.

No air leaks, staple-line disruptions, or infections occurred in either the BP- or the ePTFE-implanted healthy lungs in this experimental study. In the long-term clinical setting, however, the nature of the tissue response to BP strips used for staple-line reinforcement in lung surgery, which we found to be characterized by early chronic inflammation, minimal fibroplasia and encapsulation, and little to no resorption-even at 6 months after implantation-may have several ramifications. For example, patients in whom these strips have been used may be at an increased risk of separation of the staple line and resultant pneumothorax or of bacterial colonization of the exposed prosthesis, especially in the presence of a chest infection. Additional laboratory and clinical studies comparing BP and ePTFE suture-line reinforcement materials are needed, with special attention paid to the varying tissue reactions to the two prostheses.

	Footnotes

 
Presented at the 11th Annual Meeting of the European Association for Cardio-Thoracic Surgery, Copenhagen, Denmark, 28 September–1 October, 1997.

	Appendix A. Conference discussion

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Dr L. Von Segesser (Lausanne, Switzerland): I have two questions for you, one concerning the PTFE that was used. As you know, there are different pore sizes available for PTFE sheaths. Do you know something about the pore size for this specific application? And the other question concerns the bovine pericardium; one can assume that the tanning of this pericardium provides some antimicrobial activity which might be useful in this application. Can you comment on this?

Dr C. Vaughn: In response to the pTFE used in Seanguard Staple Line reinforcement Material. W.L. Gore does not refer to the pore size but rather to the inter nodal fibril length which is 5–10 µm. With regard to the anti-microbial activity of bovine pericardium—I suppose that glutaraldehyde used in the tanning process could have an anti-microbial effect, however the glutaraldehyde is rinsed away before use of the bovine pericardium to reinforce staple lines. Both PTFE and bovine pericardium represent the introduction of a foreign body in a potentially infected space; however with the widespread use of both materials worldwide we simply have not seen infection, certainly not in the PTFE group. We feel that the initial inflammatory response in bovine pericardium sections was related to residual glutaraldehyde.

Dr E. Wolner (Austria, Vienna): We have used this material in some patients. We have no histological data but we have had no air leaks. I have only one recommendation for this material: you should offer this PTFE together with a special type of stapler so that this material is incorporated, more or less, in the stapler. This would very much facilitate the use of PTFE sleeves. But from our clinical experience, this is an excellent option for preventing air leaks.

Dr L. Von Segesser: The way this was presented for you, was that as a combination of staples and sleeves?

Dr Vaughn: No. The PTFE is presented as a quadrangular sleeve that slides onto the jaws of the stapler. Dr Wolner is modest. The first implants were done in this unit in Vienna. The endoscopic application of the PTFE was initially a little more difficult; the people at Gore are very interested in developing a device where it is included in the stapler that would facilitate the thorascope application as well as the open procedure.

	References

Top Abstract Introduction Materials and methods Results Discussion Appendix A. Conference... References

 

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