Surgeon’s Workshop The Use of Bovine Pericardium for Complex Urologic Venous Reconstruction Sarah Coleman, Hannah Kerr, Venkatesh Krishnamurthi, Alvin Wee, Michael Gong, Islam Ghoneim, and John C. Rabets OBJECTIVE METHODS
RESULTS
CONCLUSION
To describe the use of bovine pericardium (BP) in several scenarios for venous patching and as a tubularized graft in urologic surgery. BP was used as patch or tubularized graft in 7 patients between 2010 and 2013. Clinical scenarios and operative indications were reviewed. We used BP as a patch graft for the inferior vena cava (IVC) (N ¼ 3) and for the iliac venous system (N ¼ 1) to restore venous outflow. Tubularized grafts were used (N ¼ 2) to replace the left renal vein in oncology procedures and during renal autotransplantation (N ¼ 1). Surgical technique is reviewed in detail. We used BP as a venous patching in 4 cases and as a tubularized graft in 3 cases. There was no evidence of venous thrombosis of the replaced system with a mean of 14.8 months (range, 9-26) follow-up. The use of BP as a patch or tubularized graft is an option for complicated urologic venous reconstruction. Although the follow-up interval is relatively short and this initial series small, our initial results are promising. UROLOGY 83: 495e497, 2014. 2014 Elsevier Inc.
B
ovine pericardium (BP) has been used in cardiac and vascular surgery with success based on its biocompatibility and absence of antigenic response. The use of BP in surgical repair of congenital heart defects has been described extensively.1 The data suggest a lower infection rate, thrombus rate, and presence of aneurysmal dilation. Vascular surgeons are using BP for carotid endarterectomies extensively. Data comparing early and late complications after carotid endarterectomy with BP vs autologous vein show that BP is superior to autologous vein in terms of risk of aneurysmal dilatation and early postoperative complications. Additionally, total operating time and carotid clamping were shorter with BP supporting its ease of use.2 Given the success of using BP in cardiac and vascular reconstruction cases, our group has used BP in complex urologic procedures. Thus far in the urologic published data, the use of BP has been described for corporoplasty in penile prosthesis implantation and the surgical treatment of Peyronie’s Disease.3,4 The use of BP for inferior vena cava (IVC) reconstruction after IVC thrombectomy in the setting of recurrent renal cell carcinoma has been described in a single case report.5 We present 7 cases of novel complex venous reconstruction using BP as both patch grafts and tubularized grafts.
Financial Disclosure: The authors declare that they have no relevant financial interests. From the Glickman Urological and Kidney Institute, Cleveland Clinic Foundation, Cleveland, OH Reprint requests: Sarah Coleman, M.D., Glickman Urological and Kidney Institute, Cleveland Clinic Foundation, 9500 Euclid Avenue, Cleveland, OH 44195. E-mail: [email protected] Submitted: August 19, 2013, accepted (with revisions): October 6, 2013
ª 2014 Elsevier Inc. All Rights Reserved
PATIENTS AND METHODS Table 1 is a summary of the 7 patients in this series. Surgical technique is described in the following section. Patients A through C underwent patch venoplasty because of IVC wall invasion (Table 1). Preoperative imaging for patient B is shown in Figure 1. Venoplasty was performed if primary closure caused >50% narrowing of caval lumen. Patch vena cavoplasty was performed with BP. An elliptical patch was sewn in the defect with 4-0 polypropylene suture in continuous fashion. Patch venoplasty for patient B is shown in Figure 2. Patient D underwent living donor renal allotransplantation. Ligation of recipient hypogastric branches led to significant narrowing of the right iliac venous system. BP patch was then placed in patch fashion to narrowed segment of right common iliac and sutured in place with 5-0 polypropylene suture. Patient E is a 52-year-old woman with nutcracker syndrome who failed both endovascular stent placement of left renal vein and saphenous vein bypass. She subsequently underwent left renal autotransplantation. BP was used in tubularized fashion to extend the left renal vein. Tubularization was completed to 30F with 5-0 polypropylene suture. An end-to-end anastomosis of the tubularized BP to the vein was performed using 6-0 polypropylene suture. The venous anastomosis to the right external iliac vein was completed with 5-0 polypropylene suture. Patient F is a 61-year-old man with recurrent left renal vein tumor thrombus after left open partial nephrectomy in a solitary kidney. Preoperative imaging for patient F is shown in Figure 3. The left renal vein was resected and venous outflow was reestablished with a tubularized bovine pericardium graft. Proximal and distal anastomoses were completed with running 5-0 polypropylene suture with in situ hypothermia using ice slush and renal arterial cannulation. Patient G is a 54-year-old man with right renal mass and level III IVC thrombus. Preoperative imaging also demonstrated 0090-4295/14/$36.00 http://dx.doi.org/10.1016/j.urology.2013.10.011
495
Table 1. Patient age, graft type, disease process, follow-up, and complications Patient Age Graft Type
Disease Process
Follow-up (mo)
Complications
IVC IVC
Leiomyosarcoma Clear cell RCC
13 18 12 14 9
None Postoperative hemorrhage (grade IIIb) None None Femoral neuropraxia (grade I)
26 12
Tumor recurrence in graft None
A B
57 66
C D E
21 Patch IVC Nonseminomatous GCT 29 Patch Common iliac vein ESRD because of ADPKD 52 Tubularized Left autotransplanted Nutcracker syndrome renal vein (bench) 61 Tubularized Left renal vein in situ Clear cell RCC 54 Tubularized Left renal vein in situ Transitional cell carcinoma
F G
Patch Patch
Vessel
ADPKD, autosomal dominant polycystic kidney disease; ESRD, end stage renal disease; GCT, germ cell tumor; IVC, inferior vena cava; RCC, renal cell carcinoma.
Figure 1. Patient B e preoperative magnetic resonance imaging showing infrahepatic inferior vena cava thrombus. Figure 2. Patient B e patch graft to inferior vena cava. (Color version available online.) thrombus in the IVC proximal to the level of the renal veins to the level of the iliac vein confluence. Intraoperatively, cavotomy revealed densely adherent tumor thrombus in the perirenal IVC and distal left renal vein. Given that preoperative venogram showed no flow in the proximal IVC and extensive collaterals, the proximal IVC was oversewn with 4-0 polypropylene suture (Fig. 4A, B). Several left adrenal and lumbar venous branches required ligation. A BP graft was then tubularized from the left renal vein to the distal IVC below the hepatic veins over 30F thoracostomy tube with 5-0 polypropylene suture.
RESULTS Patient outcomes and follow-up intervals are listed in Table 1. Imaging was performed at appropriate oncologic time points. No patients were maintained on anticoagulation. Patients D and E had dedicated imaging to rule out venous thrombosis postoperatively as described in the following section. All IVC patch venoplasties (A-C) were patent on computed tomographic imaging at last follow-up (mean 14.3 months; range, 12-18). Patient D had lower extremity duplex at postoperative day 12 showing graft patency and no clinical evidence of deep venous thrombosis at last follow-up (14 months). Patient E had normal renal transplant ultrasound on postoperative day 1 and a computed tomographic urogram showing graft patency on postoperative day 35. At last follow-up (9 months), the patient reported left 496
Figure 3. Patient F e preoperative computed tomography showing renal vein thrombus.
femoral neuropraxia, which was not present before surgery. Patient F developed nonocclusive tumor thrombus recurrence in the left renal vein and regional adenopathy 17 months postoperatively and is currently on systemic treatment. The last creatinine was 1.5. Patient G had graft patency at 10 months but passed away from metastatic transitional cell carcinoma 12 months postoperatively. UROLOGY 83 (2), 2014
Figure 4. Patient G e tubularized left renal vein replacement. (Color version available online.)
COMMENT The initial use of bovine pericardium graft in complex urologic venous reconstruction has promising initial results. The use of BP in venous grafting for urologic procedures provides a novel alternative to Dacron (polyethylene terephthalate) and Gore-Tex (polytetrafluoroethylene). The safety of BP has been demonstrated extensively in cardiac and vascular procedures for arterial patching. Carotid endarterectomy is performed routinely with BP, and literature supports its use when compared with other grafts. A retrospective analysis from Brigham and Women’s Hospital compared outcomes in 1331 patients undergoing carotid endarterectomy by primary closure, Dacron patch angioplasty, and bovine pericardial patch angioplasty. Their data show a lower rate of restenosis with BP and equivalent rates of postoperative bleeding, infection, and pseudoaneurym formation.6 A prospective randomized trial compared suture line bleeding in BP vs Dacron and showed improved hemostasis with BP.7 Cardiothoracic surgery literature describes the use of BP for repair of complex congenital cardiac defects, ventricular septal defects, and repair of diaphragmatic defects. Retrospective review comparing BP and polytetrafluoroethylene for ventricular septal defect repair showed similar rates of mortality, aneurysm formation, and calcification but surgeons preferred BP because of its easy handling, elasticity, and lower risk of endocarditis.8 A prospective review of 30 pediatric patients undergoing surgery for repair of complex congenital cardiac anomalies using BP showed no evidence of calcification, infection, thromboembolic events, or device failure at 18-36 months.9 Descriptions of BP for venous patching and venous replacement are scant. BP has been demonstrated to be a suitable graft material in infected fields.10 Data show that BP can be used effectively for arterial reconstruction after removal of infected grafts in vascular surgery literature.11 BP is biocompatible, derived from a biologic material fixed in glutaraldehyde, allowing for easy handling and low antigenicity. BP has comparable texture to a large vein such that suturing is not technically challenging. Routine anticoagulation is also not required after the use of BP. None of our patients was maintained on warfarin therapy. This initial series is small, but our data show no major graft-related complications. Patient B developed postoperative hemorrhage, but this was unrelated to the graft UROLOGY 83 (2), 2014
site. One mortality in our series was related to underlying malignancy. Further studies are necessary to support our findings that BP is a suitable graft material for venous patching in complex urologic procedures.
CONCLUSION In our experience, the use of BP as patch or tubularized graft is successful when venous reconstruction is required during urologic surgery. A prospective randomized trial comparing graft materials would be very difficult to perform given the unique scenarios requiring BP grafting in urologic surgery. Our series highlights a novel approach to venous reconstruction in complex urologic surgery. References 1. David TE. The use of pericardium in acquired heart disease: a review article. J Heart Valve Dis. 1998 Jan;7:13-18. 2. Kim JH, Cho YP, Kwon TW, et al. Ten-year comparative analysis of bovine pericardium and autogenous vein for patch angioplasty in patients undergoing carotid endarterectomy. Ann Vasc Surg. 2012; 26:353-358. 3. Lopes EJ, Kuwano AY, Guimaraes AN, et al. Corporoplasty using bovine pericardium grafts in complex penile prosthesis implantation surgery. International Braz J Urol. 2009;35:49-55. 4. Egydio PH, Lucon AM, Arap S. Treatment of Peyronie’s disease by incomplete circumferential incision of the tunica albuginea and plaque with bovine pericardium graft. Urology. 2002;59:570-574. 5. Smaldone MC, Cannon GM Jr, Hrebink RL. Resection of recurrent inferior vena cava tumor after radical nephrectomy for renal cell carcinoma. Urology. 2006;67:1084e5-1084e7. 6. Ho KJ, Nguyen LL, Menard MT. Intermediate-term outcome of carotid endarterectomy with bovine pericardial patch closure compared with Dacron patch and primary closure. J Vasc Surg. 2012; 55:708-714. 7. Marien BJ, Raffetto JD, Seidman CS, et al. Bovine pericardium vs Dacron for patch angioplasty after carotid endarterectomy: a prospective randomized study. Arch Surg. 2002;137:785-788. 8. Us MH, Sungun M, Sanioglu S, et al. A retrospective comparison of bovine pericardium and polytetrafluoroethylene patch for closure of ventricular septal defects. J Int Med Res. 2004;32:218-221. 9. Neethling WM, Strange G, Firth L, et al. Evaluation of a tissueengineered bovine pericardial patch in paediatric patients with congenital cardiac anomalies: initial experience with ADAPTtreated CardioCel patch. Interact Cardiovasc Thorac Surg. 2013; 17:698-702. 10. D’Ambra L, Berti S, Feleppa C, et al. Use of bovine pericardium graft for abdominal wall reconstruction in contaminated field. World J Gastrointestinal Surg. 2012;4:171-176. 11. McMillan WD, Leville CD, Hile CN. Bovine pericardial patch repair in infected fields. J Vasc Surg. 2012;55:1712-1715.
497
RESULTS
CONCLUSION
To describe the use of bovine pericardium (BP) in several scenarios for venous patching and as a tubularized graft in urologic surgery. BP was used as patch or tubularized graft in 7 patients between 2010 and 2013. Clinical scenarios and operative indications were reviewed. We used BP as a patch graft for the inferior vena cava (IVC) (N ¼ 3) and for the iliac venous system (N ¼ 1) to restore venous outflow. Tubularized grafts were used (N ¼ 2) to replace the left renal vein in oncology procedures and during renal autotransplantation (N ¼ 1). Surgical technique is reviewed in detail. We used BP as a venous patching in 4 cases and as a tubularized graft in 3 cases. There was no evidence of venous thrombosis of the replaced system with a mean of 14.8 months (range, 9-26) follow-up. The use of BP as a patch or tubularized graft is an option for complicated urologic venous reconstruction. Although the follow-up interval is relatively short and this initial series small, our initial results are promising. UROLOGY 83: 495e497, 2014. 2014 Elsevier Inc.
B
ovine pericardium (BP) has been used in cardiac and vascular surgery with success based on its biocompatibility and absence of antigenic response. The use of BP in surgical repair of congenital heart defects has been described extensively.1 The data suggest a lower infection rate, thrombus rate, and presence of aneurysmal dilation. Vascular surgeons are using BP for carotid endarterectomies extensively. Data comparing early and late complications after carotid endarterectomy with BP vs autologous vein show that BP is superior to autologous vein in terms of risk of aneurysmal dilatation and early postoperative complications. Additionally, total operating time and carotid clamping were shorter with BP supporting its ease of use.2 Given the success of using BP in cardiac and vascular reconstruction cases, our group has used BP in complex urologic procedures. Thus far in the urologic published data, the use of BP has been described for corporoplasty in penile prosthesis implantation and the surgical treatment of Peyronie’s Disease.3,4 The use of BP for inferior vena cava (IVC) reconstruction after IVC thrombectomy in the setting of recurrent renal cell carcinoma has been described in a single case report.5 We present 7 cases of novel complex venous reconstruction using BP as both patch grafts and tubularized grafts.
Financial Disclosure: The authors declare that they have no relevant financial interests. From the Glickman Urological and Kidney Institute, Cleveland Clinic Foundation, Cleveland, OH Reprint requests: Sarah Coleman, M.D., Glickman Urological and Kidney Institute, Cleveland Clinic Foundation, 9500 Euclid Avenue, Cleveland, OH 44195. E-mail: [email protected] Submitted: August 19, 2013, accepted (with revisions): October 6, 2013
ª 2014 Elsevier Inc. All Rights Reserved
PATIENTS AND METHODS Table 1 is a summary of the 7 patients in this series. Surgical technique is described in the following section. Patients A through C underwent patch venoplasty because of IVC wall invasion (Table 1). Preoperative imaging for patient B is shown in Figure 1. Venoplasty was performed if primary closure caused >50% narrowing of caval lumen. Patch vena cavoplasty was performed with BP. An elliptical patch was sewn in the defect with 4-0 polypropylene suture in continuous fashion. Patch venoplasty for patient B is shown in Figure 2. Patient D underwent living donor renal allotransplantation. Ligation of recipient hypogastric branches led to significant narrowing of the right iliac venous system. BP patch was then placed in patch fashion to narrowed segment of right common iliac and sutured in place with 5-0 polypropylene suture. Patient E is a 52-year-old woman with nutcracker syndrome who failed both endovascular stent placement of left renal vein and saphenous vein bypass. She subsequently underwent left renal autotransplantation. BP was used in tubularized fashion to extend the left renal vein. Tubularization was completed to 30F with 5-0 polypropylene suture. An end-to-end anastomosis of the tubularized BP to the vein was performed using 6-0 polypropylene suture. The venous anastomosis to the right external iliac vein was completed with 5-0 polypropylene suture. Patient F is a 61-year-old man with recurrent left renal vein tumor thrombus after left open partial nephrectomy in a solitary kidney. Preoperative imaging for patient F is shown in Figure 3. The left renal vein was resected and venous outflow was reestablished with a tubularized bovine pericardium graft. Proximal and distal anastomoses were completed with running 5-0 polypropylene suture with in situ hypothermia using ice slush and renal arterial cannulation. Patient G is a 54-year-old man with right renal mass and level III IVC thrombus. Preoperative imaging also demonstrated 0090-4295/14/$36.00 http://dx.doi.org/10.1016/j.urology.2013.10.011
495
Table 1. Patient age, graft type, disease process, follow-up, and complications Patient Age Graft Type
Disease Process
Follow-up (mo)
Complications
IVC IVC
Leiomyosarcoma Clear cell RCC
13 18 12 14 9
None Postoperative hemorrhage (grade IIIb) None None Femoral neuropraxia (grade I)
26 12
Tumor recurrence in graft None
A B
57 66
C D E
21 Patch IVC Nonseminomatous GCT 29 Patch Common iliac vein ESRD because of ADPKD 52 Tubularized Left autotransplanted Nutcracker syndrome renal vein (bench) 61 Tubularized Left renal vein in situ Clear cell RCC 54 Tubularized Left renal vein in situ Transitional cell carcinoma
F G
Patch Patch
Vessel
ADPKD, autosomal dominant polycystic kidney disease; ESRD, end stage renal disease; GCT, germ cell tumor; IVC, inferior vena cava; RCC, renal cell carcinoma.
Figure 1. Patient B e preoperative magnetic resonance imaging showing infrahepatic inferior vena cava thrombus. Figure 2. Patient B e patch graft to inferior vena cava. (Color version available online.) thrombus in the IVC proximal to the level of the renal veins to the level of the iliac vein confluence. Intraoperatively, cavotomy revealed densely adherent tumor thrombus in the perirenal IVC and distal left renal vein. Given that preoperative venogram showed no flow in the proximal IVC and extensive collaterals, the proximal IVC was oversewn with 4-0 polypropylene suture (Fig. 4A, B). Several left adrenal and lumbar venous branches required ligation. A BP graft was then tubularized from the left renal vein to the distal IVC below the hepatic veins over 30F thoracostomy tube with 5-0 polypropylene suture.
RESULTS Patient outcomes and follow-up intervals are listed in Table 1. Imaging was performed at appropriate oncologic time points. No patients were maintained on anticoagulation. Patients D and E had dedicated imaging to rule out venous thrombosis postoperatively as described in the following section. All IVC patch venoplasties (A-C) were patent on computed tomographic imaging at last follow-up (mean 14.3 months; range, 12-18). Patient D had lower extremity duplex at postoperative day 12 showing graft patency and no clinical evidence of deep venous thrombosis at last follow-up (14 months). Patient E had normal renal transplant ultrasound on postoperative day 1 and a computed tomographic urogram showing graft patency on postoperative day 35. At last follow-up (9 months), the patient reported left 496
Figure 3. Patient F e preoperative computed tomography showing renal vein thrombus.
femoral neuropraxia, which was not present before surgery. Patient F developed nonocclusive tumor thrombus recurrence in the left renal vein and regional adenopathy 17 months postoperatively and is currently on systemic treatment. The last creatinine was 1.5. Patient G had graft patency at 10 months but passed away from metastatic transitional cell carcinoma 12 months postoperatively. UROLOGY 83 (2), 2014
Figure 4. Patient G e tubularized left renal vein replacement. (Color version available online.)
COMMENT The initial use of bovine pericardium graft in complex urologic venous reconstruction has promising initial results. The use of BP in venous grafting for urologic procedures provides a novel alternative to Dacron (polyethylene terephthalate) and Gore-Tex (polytetrafluoroethylene). The safety of BP has been demonstrated extensively in cardiac and vascular procedures for arterial patching. Carotid endarterectomy is performed routinely with BP, and literature supports its use when compared with other grafts. A retrospective analysis from Brigham and Women’s Hospital compared outcomes in 1331 patients undergoing carotid endarterectomy by primary closure, Dacron patch angioplasty, and bovine pericardial patch angioplasty. Their data show a lower rate of restenosis with BP and equivalent rates of postoperative bleeding, infection, and pseudoaneurym formation.6 A prospective randomized trial compared suture line bleeding in BP vs Dacron and showed improved hemostasis with BP.7 Cardiothoracic surgery literature describes the use of BP for repair of complex congenital cardiac defects, ventricular septal defects, and repair of diaphragmatic defects. Retrospective review comparing BP and polytetrafluoroethylene for ventricular septal defect repair showed similar rates of mortality, aneurysm formation, and calcification but surgeons preferred BP because of its easy handling, elasticity, and lower risk of endocarditis.8 A prospective review of 30 pediatric patients undergoing surgery for repair of complex congenital cardiac anomalies using BP showed no evidence of calcification, infection, thromboembolic events, or device failure at 18-36 months.9 Descriptions of BP for venous patching and venous replacement are scant. BP has been demonstrated to be a suitable graft material in infected fields.10 Data show that BP can be used effectively for arterial reconstruction after removal of infected grafts in vascular surgery literature.11 BP is biocompatible, derived from a biologic material fixed in glutaraldehyde, allowing for easy handling and low antigenicity. BP has comparable texture to a large vein such that suturing is not technically challenging. Routine anticoagulation is also not required after the use of BP. None of our patients was maintained on warfarin therapy. This initial series is small, but our data show no major graft-related complications. Patient B developed postoperative hemorrhage, but this was unrelated to the graft UROLOGY 83 (2), 2014
site. One mortality in our series was related to underlying malignancy. Further studies are necessary to support our findings that BP is a suitable graft material for venous patching in complex urologic procedures.
CONCLUSION In our experience, the use of BP as patch or tubularized graft is successful when venous reconstruction is required during urologic surgery. A prospective randomized trial comparing graft materials would be very difficult to perform given the unique scenarios requiring BP grafting in urologic surgery. Our series highlights a novel approach to venous reconstruction in complex urologic surgery. References 1. David TE. The use of pericardium in acquired heart disease: a review article. J Heart Valve Dis. 1998 Jan;7:13-18. 2. Kim JH, Cho YP, Kwon TW, et al. Ten-year comparative analysis of bovine pericardium and autogenous vein for patch angioplasty in patients undergoing carotid endarterectomy. Ann Vasc Surg. 2012; 26:353-358. 3. Lopes EJ, Kuwano AY, Guimaraes AN, et al. Corporoplasty using bovine pericardium grafts in complex penile prosthesis implantation surgery. International Braz J Urol. 2009;35:49-55. 4. Egydio PH, Lucon AM, Arap S. Treatment of Peyronie’s disease by incomplete circumferential incision of the tunica albuginea and plaque with bovine pericardium graft. Urology. 2002;59:570-574. 5. Smaldone MC, Cannon GM Jr, Hrebink RL. Resection of recurrent inferior vena cava tumor after radical nephrectomy for renal cell carcinoma. Urology. 2006;67:1084e5-1084e7. 6. Ho KJ, Nguyen LL, Menard MT. Intermediate-term outcome of carotid endarterectomy with bovine pericardial patch closure compared with Dacron patch and primary closure. J Vasc Surg. 2012; 55:708-714. 7. Marien BJ, Raffetto JD, Seidman CS, et al. Bovine pericardium vs Dacron for patch angioplasty after carotid endarterectomy: a prospective randomized study. Arch Surg. 2002;137:785-788. 8. Us MH, Sungun M, Sanioglu S, et al. A retrospective comparison of bovine pericardium and polytetrafluoroethylene patch for closure of ventricular septal defects. J Int Med Res. 2004;32:218-221. 9. Neethling WM, Strange G, Firth L, et al. Evaluation of a tissueengineered bovine pericardial patch in paediatric patients with congenital cardiac anomalies: initial experience with ADAPTtreated CardioCel patch. Interact Cardiovasc Thorac Surg. 2013; 17:698-702. 10. D’Ambra L, Berti S, Feleppa C, et al. Use of bovine pericardium graft for abdominal wall reconstruction in contaminated field. World J Gastrointestinal Surg. 2012;4:171-176. 11. McMillan WD, Leville CD, Hile CN. Bovine pericardial patch repair in infected fields. J Vasc Surg. 2012;55:1712-1715.
497
