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Reoperation after pericardial closure with bovine pericardium
Reoperation After Pericardial Closure With Bovine Pericardium Jibah Eng, MA, MB, FRCS, P. S. Ravichandran, MB, FRCS, Cedric R. Abbott, BSC, MB, CHB, MRCPath, Philip H. Kay, MA, BM, BCH, DM, FRCS, Andrew J. Murday, MB, MS, FRCS, and Issam Shreiti, MD, RCCS Cardiothoracic Surgical Unit, Leeds General Infirmary, Leeds, England
To reduce the risk of damage to the anterior surface of the right ventricle after resternotomy, it has been recommended that the pericardium be closed with a patch after open heart operations. We have examined 4 patients undergoing resternotomy for the third time 3 to 8 years after bovine pericardium valve replacement. On each occasion the pericardium was closed with a patch of bovine pericardium. In all cases, the patch was frozen to
the inner aspect of the sternum, increasing the difficulty of resternotomy. Histological examinations of the patches confirmed dense fibrous connective tissue, patchy calcification, and foreign body giant cell reaction. Bovine pericardium appears to increase the difficulty of repeat cardiac operations. We recommend its use be discontinued. (Ann Thorac Surg 1989;48:813-5)
R
implanted bovine pericardium were removed for histological examination.
epeat cardiac operations have become increasingly common in recent years not only in valvular diseases [l, 21 but also in coronary artery operations [3]. Technical difficulties that may be encountered lead not only to increased morbidity [ l ] but also to mortality [4]. To minimize pericardial adhesions and thus ease reentry at a subsequent procedure, primary pericardial closure has been advocated [5]. However, this may not be possible in all cases due to pericardial contraction and the fear of cardiac tamponade [6]. In such cases, pericardial substitutes have been applied to shield the anterior surface of the heart from direct adhesion to the sternum. These include silicone rubber, silicone polyester, polyfluoroethylene, and heterogeneous pericardium [7]. We report our recent experience of resternotomy 3 to 8 years after the implantation of glutaraldehyde-preserved bovine pericardium as a pericardial substitute.
Patients and Methods Four patients who underwent valve replacement and closure of the pericardial cavity with glutaraldehydepreserved bovine pericardium required reoperations for valve failure 3 to 8 years later. Over the same period, 113 bovine pericardial patches were used to reconstruct the pericardium after second repeat valve replacement operations. Table 1 summarizes patients’ details and the types of operations performed. Resternotomy was performed using an oscillating saw. Dense adhesions were found not only to the posterior surface of the sternum but also to the epicardium. Patient and cautious sharp dissection enabled successful freeing of the heart in all patients. Intracardiac procedures were performed uneventfully. Specimens of the previously
Results There was no operative mortality. All patients made uneventful postoperative recovery. Histological examination of the bovine pericardium patches removed showed that although the bovine pericardium itself was well preserved structurally, the surrounding tissues demonstrated dense, poorly vascular fibrous connective tissue (Fig l), foreign body giant cell reaction (Fig 2), and chronic inflammatory cell infiltrate (Fig 3). The tissue reaction was more intense in the patch removed 8 years after implantation compared with that removed 3 years after usage.
Comment Pericardial adhesions result from serosal injury and spilled blood during cardiac operations [8]. Closure of the
Table 1. Pericardial Substitute
Patient Age No. (yr) Sex
Operation
F RedoMVR CMV,MVRx 2 M RedoAVR, AVR, MVR MVR M Redo AVR, Repair coarctation, MVR AVR, MVR M Redo AVR AVR x 2
1 2
34 46
3
46
Accepted for publication Aug 28, 1989.
4
53
Address reprint requests to Mr Eng, Cardiothoracic Surgical Unit, Leeds General Infirmary, Great George St, Leeds LSI 3EX, England.
AVR = aortic valve replacement; MVR = mitral valve replacement.
0 1989 by The Society of Thoracic Surgeons
Previous Operations
Length of Imp1antation (Yr) 3 4
5 8
CMV = closed mitral valvotomy;
O003-4975/89/$3.50
814
ENGETAL BOVINE PERICARDIAL SUBSTITUTE
Ann Thorac Surg 1989;48:81>5
Fig 1 . Bovine pericardium (arrows) with dense substernal (A) and epicardial (B)scars. (Hemutoxylin and eosin, x l W before 43% reduction.)
pericardium, if feasible, reduces such adhesions and aids reoperations (5, 61. This has not been found to affect graft patency after coronary artery bypass grafting [9], postoperative blood loss, or the requirement for reexplorations [101. Conversely, pericardial closure prevented cardiac tamponade as most postoperative bleeding appeared to originate from extrapericardial sources [6]. The pericardium may shrink substantially within one to two hours of exposure during cardiac operations (61. This may make it impossible to effect primary pericardial closure without compressing the heart, with harmful hemodynamic consequences. Many pericardial substitutes have been advocated to allow closure without tension and to ease resternotomy by preventing direct adhesion of the heart to the posterior surface of the sternum. These include bovine and equine glutaraldehyde-preserved xenografts [ll, 121, expanded polytetrafluoroethylene [13], siliconized Dacron [14], Silastic [15], and autologous fascia lata [16]. Of these, polytetrafluoroethylene Fig 2 . Substernal foreign body giant cell reaction adjacent to bovine pericardiul patch (arrow). (Hemutoxylin and eosin, X265 before 43% reduction.)
appears to be a satisfactory substitute [7], especially in children requiring multiple corrective procedures [131. Since the initial reports of favorable results in experimental animals [171, bovine pericardium has become increasingly used in achieving pericardial closure. It soon emerged both in experimental animals [ l l ] and in clinical application that pericardial adhesions still occurred from intense inflammatory reaction [18, 191. Calcification can result [ll]. This may be the result of mechanical distortion [20] or the use of preservatives [19]. Our experience with glutaraldehyde-preserved bovine pericardium as a pericardial substitute as presented here confirms these observations. These adhesions not only complicate resternotomy but also make identification of coronary anatomy difficult [ E l . Use of autogenous tissues, including fascia lata [16], may reduce the intensity of such inflammatory response. In our institution, bovine pericardium is no longer used for such a purpose. A controlled study is thus not feasible. No other pericardial substitutes have been
ENGETAL BOVINE PERKARDIAL SUBSTITUTE
Ann Thorac Surg 1989:48:81>5
815
Fig 3 . Chronic inflammatory cell infiltrate in scar adjacent to pericardial patch (arrow). (Hematoxylin and eosin, X265 before 43% reduction.)
used in our unit. However, our experiences of reoperating on patients who previously had bovine pericardial substitute place us in a favorable position to describe the difficulties encountered, as we appear to have a higher frequency of repeat valve operations than other groups [l]. Although technically more demanding, resternotomy after a previous cardiac operation with the pericardium left open may not be associated with a higher operative mortality provided a careful technique is adopted [2]. When reoperation appears likely at the first procedure, primary pericardial closure should be attempted. This may be aided by methods of traction to prevent pericardial contraction after its incision [6]. The use of pericardial substitutes in cardiac surgery remains doubtful, and caution is advised in their wider application [7].
7. Heydorn WH, Ferraris VA, Berry WR. Pericardial substitutes: a survey. Ann Thorac Surg 1988;46:567-9.
8. Cliff WJ, Grobety J, Ryan GB. Postoperative pericardial adhesions. The role of mild serosal injury and spilled blood. J Thorac Cardiovasc Surg 1973;65:74&50. 9. Bahn CH. Pericardial closure. J Thorac Cardiovasc Surg 1987;93317-8. 10. Bahn CH, Annest LS, Miyamoato M. Pericardial closure. Am J Surg 1986;151:612-5. 11. Mathisen SR, Wu H, Sauvage LR, Walker MW. Prevention of
12.
13.
References 1. Mary DS, Elmufti ME, Pakrashi BC, Fayoumi SM, Ionescu
MI. Analysis of risk factors involved in reoperation for mitral and tricuspid valve disease. J Thorac Cardiovasc Surg 1974; 6733342.
14. 15.
2. English TAH, Milstein BB. Repeat open intracardiac opera-
tion. Analysis of fifty operations. J Thorac Cardiovasc Surg 1978;765640. 3. Schaff HV, Orszulak TA, Gersh BJ, et al. The morbidity and
mortality of reoperation for coronary artery disease and analysis of late results with use of actuarial estimate of event-free interval. J Thorac Cardiovasc Surg 1983;85:508-15. 4. Dobell ARC, lain AK. Catastrophic hemorrhage during redo sternotomy. Ann Thorac Surg 1984;3727?-8. 5. Nandi P, Leung ISM, Cheung KL. Closure of pericardium after heart surgery. A way to prevent postoperative cardiac tamponade. Br Heart J 1976;38:1319-23. 6. Cunningham JN, Spencer FC, Zeff R, William CD, Cullingnan R, Mullin M. Influence of primary closure of the pericardium after open heart surgery on the frequency of tamponade, postcardiotomy syndrome and pulmonary complications. J Thorac Cardiovasc Surg 1975;70:11%2.!5.
16.
17.
retrosternal adhesions after pericardiotomy. J Thorac Cardiovasc Surg 1986;92:92-8. Gallo I, Artinano E, Duran CG. Late clinical results with the use of heterologous pericardium for closure of the pericardial cavity. J Thorac Cardiovasc Surg 1985;89:709-12. Harada Y, Imai Y, Kurosawa H, Hoshino S, Nakano K. Long-term results of the clinical use of an expanded polytetrafluoroethylene surgical membrane as a pericardial substitute. J Thorac Cardiovasc Surg 1988;96:811-5. Mazuji MK, Let JC. Siliconized Dacron as a pericardial patch. Arch Surg 1963;87:446-9. Youmans CR, White J, Demck JR. The prevention of pleural and pericardial adhesions with Silastic. J Thorac Cardiovasc Surg 1968;55:383-8. Kohanna FH, Adams PX, Cunningham JN, Spencer FC. Use of autologous fascia lata as a pericardial substitute following open heart surgery. J Thorac Cardiovasc Surg 1977;74:14-9. Meus PJ, WernIy JA, Campbell CD, et al. Long-term evaluation of pericardial substitutes. J Thorac Cardiovasc Surg
1983;85:544. 18. Gallo I, Nistal F, Artinano E. Pericardial substitute: animal versus clinical results. J Thorac Cardiovasc Surg 1988; 96:488-91. 19. Opie JC, Larrien SJ, Cornell IS. Pericardial substitute: delayed reexploration and findings. Ann Thorac Surg 1987; 43:383-5. 20. Revuelta JM, Garcia-Rinaldi R, Johnston RH, Vaughan GD
111. Implantation of pericardial substitute. Ann Thorac Surg 1985;39:190-1.
To reduce the risk of damage to the anterior surface of the right ventricle after resternotomy, it has been recommended that the pericardium be closed with a patch after open heart operations. We have examined 4 patients undergoing resternotomy for the third time 3 to 8 years after bovine pericardium valve replacement. On each occasion the pericardium was closed with a patch of bovine pericardium. In all cases, the patch was frozen to
the inner aspect of the sternum, increasing the difficulty of resternotomy. Histological examinations of the patches confirmed dense fibrous connective tissue, patchy calcification, and foreign body giant cell reaction. Bovine pericardium appears to increase the difficulty of repeat cardiac operations. We recommend its use be discontinued. (Ann Thorac Surg 1989;48:813-5)
R
implanted bovine pericardium were removed for histological examination.
epeat cardiac operations have become increasingly common in recent years not only in valvular diseases [l, 21 but also in coronary artery operations [3]. Technical difficulties that may be encountered lead not only to increased morbidity [ l ] but also to mortality [4]. To minimize pericardial adhesions and thus ease reentry at a subsequent procedure, primary pericardial closure has been advocated [5]. However, this may not be possible in all cases due to pericardial contraction and the fear of cardiac tamponade [6]. In such cases, pericardial substitutes have been applied to shield the anterior surface of the heart from direct adhesion to the sternum. These include silicone rubber, silicone polyester, polyfluoroethylene, and heterogeneous pericardium [7]. We report our recent experience of resternotomy 3 to 8 years after the implantation of glutaraldehyde-preserved bovine pericardium as a pericardial substitute.
Patients and Methods Four patients who underwent valve replacement and closure of the pericardial cavity with glutaraldehydepreserved bovine pericardium required reoperations for valve failure 3 to 8 years later. Over the same period, 113 bovine pericardial patches were used to reconstruct the pericardium after second repeat valve replacement operations. Table 1 summarizes patients’ details and the types of operations performed. Resternotomy was performed using an oscillating saw. Dense adhesions were found not only to the posterior surface of the sternum but also to the epicardium. Patient and cautious sharp dissection enabled successful freeing of the heart in all patients. Intracardiac procedures were performed uneventfully. Specimens of the previously
Results There was no operative mortality. All patients made uneventful postoperative recovery. Histological examination of the bovine pericardium patches removed showed that although the bovine pericardium itself was well preserved structurally, the surrounding tissues demonstrated dense, poorly vascular fibrous connective tissue (Fig l), foreign body giant cell reaction (Fig 2), and chronic inflammatory cell infiltrate (Fig 3). The tissue reaction was more intense in the patch removed 8 years after implantation compared with that removed 3 years after usage.
Comment Pericardial adhesions result from serosal injury and spilled blood during cardiac operations [8]. Closure of the
Table 1. Pericardial Substitute
Patient Age No. (yr) Sex
Operation
F RedoMVR CMV,MVRx 2 M RedoAVR, AVR, MVR MVR M Redo AVR, Repair coarctation, MVR AVR, MVR M Redo AVR AVR x 2
1 2
34 46
3
46
Accepted for publication Aug 28, 1989.
4
53
Address reprint requests to Mr Eng, Cardiothoracic Surgical Unit, Leeds General Infirmary, Great George St, Leeds LSI 3EX, England.
AVR = aortic valve replacement; MVR = mitral valve replacement.
0 1989 by The Society of Thoracic Surgeons
Previous Operations
Length of Imp1antation (Yr) 3 4
5 8
CMV = closed mitral valvotomy;
O003-4975/89/$3.50
814
ENGETAL BOVINE PERICARDIAL SUBSTITUTE
Ann Thorac Surg 1989;48:81>5
Fig 1 . Bovine pericardium (arrows) with dense substernal (A) and epicardial (B)scars. (Hemutoxylin and eosin, x l W before 43% reduction.)
pericardium, if feasible, reduces such adhesions and aids reoperations (5, 61. This has not been found to affect graft patency after coronary artery bypass grafting [9], postoperative blood loss, or the requirement for reexplorations [101. Conversely, pericardial closure prevented cardiac tamponade as most postoperative bleeding appeared to originate from extrapericardial sources [6]. The pericardium may shrink substantially within one to two hours of exposure during cardiac operations (61. This may make it impossible to effect primary pericardial closure without compressing the heart, with harmful hemodynamic consequences. Many pericardial substitutes have been advocated to allow closure without tension and to ease resternotomy by preventing direct adhesion of the heart to the posterior surface of the sternum. These include bovine and equine glutaraldehyde-preserved xenografts [ll, 121, expanded polytetrafluoroethylene [13], siliconized Dacron [14], Silastic [15], and autologous fascia lata [16]. Of these, polytetrafluoroethylene Fig 2 . Substernal foreign body giant cell reaction adjacent to bovine pericardiul patch (arrow). (Hemutoxylin and eosin, X265 before 43% reduction.)
appears to be a satisfactory substitute [7], especially in children requiring multiple corrective procedures [131. Since the initial reports of favorable results in experimental animals [171, bovine pericardium has become increasingly used in achieving pericardial closure. It soon emerged both in experimental animals [ l l ] and in clinical application that pericardial adhesions still occurred from intense inflammatory reaction [18, 191. Calcification can result [ll]. This may be the result of mechanical distortion [20] or the use of preservatives [19]. Our experience with glutaraldehyde-preserved bovine pericardium as a pericardial substitute as presented here confirms these observations. These adhesions not only complicate resternotomy but also make identification of coronary anatomy difficult [ E l . Use of autogenous tissues, including fascia lata [16], may reduce the intensity of such inflammatory response. In our institution, bovine pericardium is no longer used for such a purpose. A controlled study is thus not feasible. No other pericardial substitutes have been
ENGETAL BOVINE PERKARDIAL SUBSTITUTE
Ann Thorac Surg 1989:48:81>5
815
Fig 3 . Chronic inflammatory cell infiltrate in scar adjacent to pericardial patch (arrow). (Hematoxylin and eosin, X265 before 43% reduction.)
used in our unit. However, our experiences of reoperating on patients who previously had bovine pericardial substitute place us in a favorable position to describe the difficulties encountered, as we appear to have a higher frequency of repeat valve operations than other groups [l]. Although technically more demanding, resternotomy after a previous cardiac operation with the pericardium left open may not be associated with a higher operative mortality provided a careful technique is adopted [2]. When reoperation appears likely at the first procedure, primary pericardial closure should be attempted. This may be aided by methods of traction to prevent pericardial contraction after its incision [6]. The use of pericardial substitutes in cardiac surgery remains doubtful, and caution is advised in their wider application [7].
7. Heydorn WH, Ferraris VA, Berry WR. Pericardial substitutes: a survey. Ann Thorac Surg 1988;46:567-9.
8. Cliff WJ, Grobety J, Ryan GB. Postoperative pericardial adhesions. The role of mild serosal injury and spilled blood. J Thorac Cardiovasc Surg 1973;65:74&50. 9. Bahn CH. Pericardial closure. J Thorac Cardiovasc Surg 1987;93317-8. 10. Bahn CH, Annest LS, Miyamoato M. Pericardial closure. Am J Surg 1986;151:612-5. 11. Mathisen SR, Wu H, Sauvage LR, Walker MW. Prevention of
12.
13.
References 1. Mary DS, Elmufti ME, Pakrashi BC, Fayoumi SM, Ionescu
MI. Analysis of risk factors involved in reoperation for mitral and tricuspid valve disease. J Thorac Cardiovasc Surg 1974; 6733342.
14. 15.
2. English TAH, Milstein BB. Repeat open intracardiac opera-
tion. Analysis of fifty operations. J Thorac Cardiovasc Surg 1978;765640. 3. Schaff HV, Orszulak TA, Gersh BJ, et al. The morbidity and
mortality of reoperation for coronary artery disease and analysis of late results with use of actuarial estimate of event-free interval. J Thorac Cardiovasc Surg 1983;85:508-15. 4. Dobell ARC, lain AK. Catastrophic hemorrhage during redo sternotomy. Ann Thorac Surg 1984;3727?-8. 5. Nandi P, Leung ISM, Cheung KL. Closure of pericardium after heart surgery. A way to prevent postoperative cardiac tamponade. Br Heart J 1976;38:1319-23. 6. Cunningham JN, Spencer FC, Zeff R, William CD, Cullingnan R, Mullin M. Influence of primary closure of the pericardium after open heart surgery on the frequency of tamponade, postcardiotomy syndrome and pulmonary complications. J Thorac Cardiovasc Surg 1975;70:11%2.!5.
16.
17.
retrosternal adhesions after pericardiotomy. J Thorac Cardiovasc Surg 1986;92:92-8. Gallo I, Artinano E, Duran CG. Late clinical results with the use of heterologous pericardium for closure of the pericardial cavity. J Thorac Cardiovasc Surg 1985;89:709-12. Harada Y, Imai Y, Kurosawa H, Hoshino S, Nakano K. Long-term results of the clinical use of an expanded polytetrafluoroethylene surgical membrane as a pericardial substitute. J Thorac Cardiovasc Surg 1988;96:811-5. Mazuji MK, Let JC. Siliconized Dacron as a pericardial patch. Arch Surg 1963;87:446-9. Youmans CR, White J, Demck JR. The prevention of pleural and pericardial adhesions with Silastic. J Thorac Cardiovasc Surg 1968;55:383-8. Kohanna FH, Adams PX, Cunningham JN, Spencer FC. Use of autologous fascia lata as a pericardial substitute following open heart surgery. J Thorac Cardiovasc Surg 1977;74:14-9. Meus PJ, WernIy JA, Campbell CD, et al. Long-term evaluation of pericardial substitutes. J Thorac Cardiovasc Surg
1983;85:544. 18. Gallo I, Nistal F, Artinano E. Pericardial substitute: animal versus clinical results. J Thorac Cardiovasc Surg 1988; 96:488-91. 19. Opie JC, Larrien SJ, Cornell IS. Pericardial substitute: delayed reexploration and findings. Ann Thorac Surg 1987; 43:383-5. 20. Revuelta JM, Garcia-Rinaldi R, Johnston RH, Vaughan GD
111. Implantation of pericardial substitute. Ann Thorac Surg 1985;39:190-1.