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Ann Thorac Surg 1996;62:1778-1782
© 1996 The Society of Thoracic Surgeons

Original Articles: Cardiovascular

Expanded PTFE Membrane to Prevent Cardiac Injury During Resternotomy for Congenital Heart Disease

Jeffrey P. Jacobs, MD, Raju S. Iyer, MCh, Jo S. Weston, BSc, Joseph J. Amato, MD, Martin J. Elliott, FRCS, Marc R. de Leval, MD, Jaroslav Stark, MD

Great Ormond Street Hospital for Children, London, England, and Schneider Children's Hospital, New York, New York

Accepted for publication June 25, 1996.


   Abstract
Top
 Footnotes
 Abstract
Introduction
 Material and Methods
 Results
 Comment
 Appendix 1
 Acknowledgments
 References
 
Background. Resternotomy for repair of congenital cardiac defects can result in cardiac injury. Closure of the pericardium during the initial operation may prevent this, and several pericardial substitutes have been tried, with variable results, in patients in whom primary pericardial closure is not possible. We conducted a multicenter observational study of the use of the expanded polytetrafluoroethylene membrane (Preclude Pericardial Membrane, formerly called the Gore-Tex Surgical Membrane; W. L. Gore & Associates, Flagstaff, AZ) in patients likely to undergo reoperation for treatment of congenital heart disease.

Methods. Data were collected retrospectively on all patients in whom the expanded polytetrafluoroethylene membrane was inserted at the initial operation for congenital heart disease at 12 centers in 1984 to 1993.

Results. A total of 1,085 patients (mean age, 55 ± 2.5 months) received the membrane. During follow-up ranging from 1.3 to 10.5 years, 105 reoperations were performed. Injury during resternotomy occurred in only 1 patient (1% of reoperations). There were no membrane-related deaths or complications in the entire series of 1,085 patients.

Conclusions. The expanded polytetrafluoroethylene membrane was safe and effective in helping to prevent cardiac injury during resternotomy for treatment of congenital heart disease.


   Introduction
Top
 Footnotes
 Abstract
 Introduction
Material and Methods
 Results
 Comment
 Appendix 1
 Acknowledgments
 References
 
Since its popularization by Julian and associates [1] in 1957, the median sternotomy has become the most commonly used incision in cardiac surgery. Moreover, because the number of patients with congenital heart defects requiring reoperation is growing, the need for a second and even a third or fourth sternotomy is also increasing. The risks involved in reoperative sternotomy are well known [2–5]. Pericardial and mediastinal adhesions can predispose the heart to iatrogenic injury during reopening of the sternum by making it difficult for the surgeon to identify anatomic features during dissection. The sequelae of such an injury include catastrophic bleeding, decreased right ventricular function, and death. Because primary closure of the pericardium is not always possible, various materials have been suggested for use as a pericardial substitute to decrease adhesion formation and the potential for cardiac injury at reoperation. These include silicone, bovine pericardium, and expanded polytetrafluoroethylene (ePTFE) [6–10].

The 0.1-mm-thick, low-porosity ePTFE membrane (Preclude Pericardial Membrane, formerly called the Gore-Tex Surgical Membrane; W. L. Gore & Associates, Flagstaff, AZ) was initially found to reduce pericardial adhesion formation in animal models [11]. Subsequent reports described favorable results with the device in clinical series [12–14]. In addition, a survey on pericardial substitutes of members of The Society of Thoracic Surgeons found that more of the respondents were satisfied with the ePTFE membrane at reoperation than with any other substitute (p = 0.0004 by {chi}2 analysis) [15]. In the light of these findings, long-term follow-up investigations of the ePTFE membrane have been advocated [15, 16]. We therefore conducted a multicenter, cohort, observational study to assess the ability of the ePTFE membrane to minimize adhesion formation and protect the heart during subsequent reoperative sternotomy.


   Material and Methods
Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
Results
 Comment
 Appendix 1
 Acknowledgments
 References
 
Demographic, medical status, operative, and postoperative data were collected on all patients with congenital heart disease in whom the ePTFE membrane was inserted at the initial cardiac operation at 12 centers (Appendix 1) participating in the study in 1984 to 1993. The indication for insertion of the membrane was a judgment by the surgeon that reoperation was likely. Early in the study, several surgeons chose to insert the membrane almost routinely to gain more experience with the device.

The pericardial membrane was inserted with one of two techniques. With the first, the membrane was attached to the pericardium on both sides and inferiorly to ensure that, at reoperation, the saw or scissors would stay above the implant. With the second technique, it was sutured to one side of the pericardium and along the inferior border of the pericardium. On the other side of the pericardium, the membrane was attached to the pleural fat. With both techniques, either both sides were attached with interrupted sutures or one side was attached with interrupted sutures and one side with running sutures. Inferiorly, a small gap was left for a pericardial drain on one side of the midline. Superiorly, an opening of at least 2 cm was left above the aorta to allow communication between the pericardial and mediastinal drains.


   Results
Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
Comment
 Appendix 1
 Acknowledgments
 References
 
An ePTFE membrane was inserted in 1,085 patients in 1984 to 1993 at the 12 centers in the study. The mean (± standard error of the mean) age of the patients at membrane insertion was 55 ± 2.5 months; the mean weight was 14.5 kg. The initial operations performed most often and information on postoperative complications are shown in Table 1Go. Overall, there were 54 deaths (5.0% of total patients). Early mortality at initial operation occurred in 37 patients (3.4% of all patients). Late mortality after initial operation occurred in 17 patients (1.6% of all patients): 12 patients (1.1% of all patients) died late without undergoing resternotomy and 5 patients (0.5% of all patients) died after undergoing resternotomy. There were no perioperative complications or deaths attributable to the membrane. There were no membrane-related infections; the 9 patients with sepsis (see Table 1Go) did not have mediastinitis.


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  		Table 1. . Most Common Operative Procedures and Postoperative Complications in 1,085 Patients in Whom an Expanded Polytetrafluoroethylene Membrane Was Useda
 
Follow-up time varied from 1.3 to 10.5 years; overall, the study included 4,769 patient-years of follow-up. During that time, there were no infections or other complications related to the use of the ePTFE membrane. Reoperation was performed in 105 patients (9.7% of the total number) (Table 2Go) at a mean of 13.3 ± 1.3 months after the initial operation. The mean age of the patients at reoperation was 67.9 ± 6.4 months. The most commonly performed reoperative procedures, the cannulation sites used, and postoperative complications are listed in Table 2Go. Early mortality after reoperation occurred in 5 patients (4.8% of those undergoing resternotomy). No late mortality after reoperation was reported. Only 1 patient (0.1% of all patients, 1% of those undergoing resternotomy) sustained an injury at resternotomy: a laceration of the innominate vein that occurred during sternal transection. This was repaired immediately, and there were no sequelae.


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  		Table 2. . Most Common Operative Procedures, Cannulation Site, and Postoperative Complications in 105 Patients Who Underwent Resternotomy After Implantation of an Membranea,b
 
At reoperation, the ePTFE membrane was clearly separate from the sternum and resembled a sheet of clear plastic overlying the heart. The underlying epicardium and coronary vessels were sometimes obscured by a film of fine adhesions. However, no problematic adhesions were observed between the membrane and the heart or between the membrane and the chest wall. An explanted gross specimen of the membrane is shown in Figure 1Go. Histologic studies after long-term implantation of the device characteristically showed no tissue ingrowth into the prosthesis and only focal areas of collagen attachment (Fig 2Go). Where tissue was attached, there was an easily discerned plane of dissection at the interface between the membrane and tissue (Fig 3Go), a result of the small pore size in the ePTFE material, which prohibits cellular penetration. Typically, when tissue was present, it consisted of bland fibrocollagenous/fibrofatty connective material. Frequently, large areas of the implant had no tissue attached along either the epicardial or chest wall surface. Figure 3Go depicts a transmission electron micrograph of specimen of ePTFE pericardial membrane explanted after 4 years of clinical use. Fibroblasts are present at the surface of the microporous ePTFE material. The spindle-shaped cells are in a collagenous, pericellular stroma. The implant appears as electron-lucent nodules of various sizes, reflecting the node-and-interconnecting-fibril structure of ePTFE. There is a clear plane of separation at the tissue/implant boundary, and the restrictive internodal pore size (too small to allow entry of fibroblasts) can be appreciated.



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  		Fig 1. . Expanded polytetrafluoroethylene pericardial membrane explanted after 4 years of use as a pericardial substitute in a patient undergoing a modified Fontan procedure. The implant is transparent and mechanically intact. Some fibrofatty tissue is attached to it along mostly one border.

 


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  		Fig 2. . Microscopical study of specimen of expanded polytetrafluoroethylene pericardial membrane explanted after 4 years of clinical use. The membrane (arrows) is devoid of cells and has focal collagen (green) attachments at discrete points along the interface with the tissue (arrowheads). (Milligan's trichrome; x105 before 67% reduction.)

 


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  		Fig 3. . Transmission electron micrograph of specimen of expanded polytetrafluoroethylene (ePTFE) pericardial membrane explanted after 4 years of clinical use. Fibroblasts (arrows) are present at the surface of the ePTFE. The ePTFE (bottom) appears as electron-lucent (white) nodules. A clear plane of separation (arrowheads) exists at the tissue/implant boundary. (Uranyl acetate/lead citrate; x4,000 before 65% reduction; bar = 2 µm.)

 
Twenty-two of the 105 patients (21%) who underwent reoperation had non-membrane-related postoperative complications (see Table 2Go). There were no cases of membrane-related cardiac tamponade, infection, or any other membrane-related complication. The patients with sepsis (see Table 2Go) did not have mediastinitis.


   Comment
Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
Appendix 1
 Acknowledgments
 References
 
Reoperative median sternotomy can result in cardiac injury [2–5] and serious bleeding, with the rate of hemorrhage at resternotomy ranging from 2% to 6% in historical controls [2, 4, 5, 16, 17]. Unfortunately, among patients who have massive bleeding at resternotomy, the reported mortality rate ranges from 37% to 50% [5, 16, 17]. Despite numerous improvements in medical care and surgical technique, bleeding at resternotomy can still represent a substantial cause of morbidity and even mortality. The goal of research on alternative methods for closing the pericardium after cardiac operations is to develop a safe way to protect the heart in the event of reoperation by providing a clear plane of dissection and minimization of clinically important adhesions. The barrier materials for protecting the myocardium that have been studied most extensively include autologous pleura and fascia lata [18, 19], heterologous bovine pericardium [7, 20], silicone rubber or elastomer [8, 10], and Dacron [9]. For various reasons, however, none of these materials has achieved widespread acceptance. Bovine pericardium has been associated with infection, sterile abscess formation, persistent reactive fever, reactive pericarditis, and adhesion formation [7, 20]. Many synthetic materials have been found to produce severe scarring and adhesion formation [20].

In contrast, in a study in dogs [11], evaluation of explanted specimens of 0.1-mm ePTFE pericardial membranes showed no adhesions between the prosthesis and tissue. All membranes were observed to be acellular and to have maintained their original mechanical characteristics. The membranes were covered by a thin fibrous membrane in the external aspect, but the epicardium showed no inflammatory reaction. The coronary arteries were visible beneath the membranes.

Previous clinical series in which the ePTFE membrane was used were described by Harada and co-workers [12], Minale and colleagues [13], and Amato and co-workers [14]. Harada and co-workers [12] used the device as a pericardial substitute in 61 children with congenital heart disease, 23 of whom underwent reoperation. No cardiac injuries occurred on resternotomy. The ePTFE membranes could be removed easily, and underneath them, the anterior surface of the heart was covered with a thin layer of fibrous tissue that obscured fine surface features but allowed visualization of the principal cardiac structures. Occasionally, dense adhesions were observed along the margin of a membrane. Within a follow-up period of 1 to 87 months, three complications possibly resulting from the use of the membrane were observed: a pericardial effusion and two abscesses. Harada and co-workers [12] concluded that the ePTFE membrane is safe and provides definite advantages during sternotomy and dissection of the pericardial space at reoperation.

Minale and colleagues [13] inserted an ePTFE membrane in 110 patients (53 with congenital heart lesions and 57 with acquired heart disease), 5 of whom underwent reoperation. The mean follow-up time was 15 months. No postoperative infections occurred; there was one episode of cardiac tamponade and one mediastinal hematoma. At reoperation, the membranes were transparent and could be removed easily from the underlying surface of the heart. Electron microscopic studies of membrane specimens showed some fibrinous debris, a few erythrocytes on the internal surface, and a loose protein layer on the external surface. Minale and colleagues [13] recommended that the ePTFE membrane be used routinely in cardiac surgery patients who were likely to require reoperation.

Amato and co-workers [20] used an ePTFE membrane for pericardial closure in 96 patients who underwent repair of congenital heart defects during a 4-year period. Seven reoperations were done. There were no infections and no deaths or complications attributable to the membrane. In vivo evaluations of the ePTFE membranes at reoperation showed that they had become transparent and loosely attached to the epicardium. There were no adhesions between the membranes and the chest wall. The membranes could be lifted easily off the epicardial surface, except at the points of suture placement at the periphery, where a fibrous reaction had occurred with the suture material. Under the membranes was a thin epicardial reaction that did not prevent visualization of the coronary vessels and was found on microscopic examination to be collagenous fibrous tissue.

The results of our multicenter, nonrandomized observational study of the ePTFE membrane provide solid support of those of previous clinical and laboratory investigations of the use of the membrane as a pericardial substitute. We found the ePTFE to be safe and effective. No membrane-related deaths or complications, including infections, occurred. Our rate of injury at resternotomy (1%) was low compared with rates that have previously been reported in the literature. Although insertion of the ePTFE membrane in patients who will possibly require resternotomy is not a substitute for meticulous surgical technique [21], its use can reduce the rate of cardiac injury at resternotomy without causing additional morbidity.


   Appendix 1
Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Appendix 1
Acknowledgments
 References
 
The following surgeons provided data for this study: Joseph J. Amato, MD, Schneider Children's Hospital, New York, NY, (current institution: Rush-Presbyterian-St. Luke's Medical Center, Chicago, IL); William J. Brawn, FRCS, Birmingham Children's Hospital, Birmingham, England; Adriano Carotti, MD, Ospedale Pediatrico Bambino Gesù, Rome, Italy; Sabine Däbritz, MD, Klinik für Thorax-, Herz- und Gefäßchirurgie, Aachen, Germany; Marc R. de Leval, MD, Great Ormond Street Hospital for Children, London, England, and Harley Street Clinic, London, England; Martin J. Elliott, FRCS, Great Ormond Street Hospital for Children, London, England; Tom R. Karl, MD, Royal Children's Hospital, Melbourne, Australia; Carlo Marcelletti, MD, Ospedale Pediatrico Bambino Gesù, Rome, Italy; Roger B. B. Mee, FRACS, Royal Children's Hospital, Melbourne, Australia (current institution: The Cleveland Clinic Foundation, Cleveland, OH); Dominique Metras, MD, Unite de Chirurgie Thoracique et Cardiaque, Children's Hospital "La Timone," Marseille, France; Patricia A. Penkoske, MD, University of Alberta Hospitals, Edmonton, Alberta, Canada; James C. S. Pollock, FRCS, Royal Hospital for Sick Children, Glasgow, Scotland; Jaroslav Stark, MD, Great Ormond Street Hospital for Children, London, England, and Harley Street Clinic, London, England; George A. Trusler, MD, Hospital for Sick Children, Toronto, Ontario, Canada; and Yuguo Weng, MD, Deutsches Herzzentrum, Berlin, Germany.


   Acknowledgments
Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Appendix 1
 Acknowledgments
References
 
We thank Thomas J. Herbst, PhD, for performing the histologic studies.


   Footnotes
Top
 Footnotes
Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Appendix 1
 Acknowledgments
 References
 
Address reprint requests to Dr Elliott, Cardiothoracic Unit, Great Ormond Street Hospital for Children, Great Ormond St, London, England WC1N 3JH.


   References
Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Appendix 1
 Acknowledgments
 References
 

  1. Julian OC, Lopez-Belio M, Dye WS, et al. The median sternotomy in intracardiac surgery with extracorporeal circulation: a general evaluation of its use in heart surgery. Surgery 1957;42:753–61.[Medline]
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  6. Vander Salm TJ, Okike ON, Marsicano TH, Compton C, Espinoza E. Prevention of postoperative pericardial adhesions: an animal study. Arch Surg 1986;121:462–7.[Abstract]
  7. Mills SA. Complications associated with the use of heterologous bovine pericardium for pericardial closure. J Thorac Cardiovasc Surg 1986;92:446–54.[Abstract]
  8. Laks H, Hammond G, Geha AS. Use of silicone rubber as a pericardial substitute to facilitate reoperation in cardiac surgery. J Thorac Cardiovasc Surg 1981;82:88–92.[Abstract]
  9. Mazuji MK, Lett JC. Siliconized Dacron as a pericardial patch. Arch Surg 1963;87:446–9.[Medline]
  10. Youmans CR Jr, White J, Derrick JR. The prevention of pleural and pericardial adhesions with Silastic. J Thorac Cardiovasc Surg 1968;55:383–8.[Medline]
  11. Revuelta JM, Garcia-Rinaldi P, Val F, Crego R, Duran CMG. Expanded polytetrafluoroethylene surgical membrane for pericardial closures. J Thorac Cardiovasc Surg 1985;89:451–5.[Abstract]
  12. Harada Y, Imai Y, Kurosawa H, Hoshino S, Nakano K. Long-term results of the clinical use of expanded polytetrafluoroethylene surgical membrane as a pericardial substitute. J Thorac Cardiovasc Surg 1988;96:811–5.
  13. Minale C, Nikol S, Hollweg G, Mittermayer C, Messmer BJ. Clinical experience with expanded polytetrafluoroethylene Gore-TexTM surgical membrane for pericardial closure: a study of 110 cases. J Card Surg 1988;3:193–201.[Medline]
  14. Amato JJ, Cotroneo JV, Galdieri RJ, Alboliras E, Antillon J, Vogel RL. Experience with the polytetrafluoroethylene surgical membrane for pericardial closure in operations for congenital cardiac defects. J Thorac Cardiovasc Surg 1989;97:929–34.[Abstract]
  15. Heydorn WH, Ferraris VA, Berry WE. Pericardial substitutes: a survey. Ann Thorac Surg 1988;46:567–9.[Abstract]
  16. Loop FD. Catastrophic hemorrhage during sternal reentry. Ann Thorac Surg 1984;37:271–2.[Medline]
  17. Wideman FE, Blackstone EH, Kirklin JW, Karp RB, Kouchoukos NT, Pacifico AD. Hospital mortality of re-replacement of the aortic valve: incremental risk factors. J Thorac Cardiovasc Surg 1981;82:692–8.[Abstract]
  18. Kohanna FH, Adams PX, Cunningham JN Jr, Spencer FC. Use of autologous fascia lata as a pericardial substitute following open-heart surgery. J Thorac Cardiovasc Surg 1977;74:14–9.[Abstract]
  19. Schechter FG, Owens RR, Bryant LR. Pleural flap closure of pericardial defects following intraperitoneal pneumonectomy. Ann Thorac Surg 1976;21:67–9.[Abstract]
  20. Minale C, Hollweg G, Nikol S, Mettermayer D, Messmer BJ. Closure of the pericardium using expanded polytetrafluoroethylene Gore-TexTM-surgical membrane: clinical experience. Thorac Cardiovasc Surg 1987;35:312–5.[Medline]
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