- Email: [email protected]
Successful venous repair and reconstruction for oncologic resections
From the Society for Clinical Vascular Surgery
Successful venous repair and reconstruction for oncologic resections Yana Etkin, MD,a Paul J. Foley, MD,a Grace J. Wang, MD,a Thomas J. Guzzo, MD,b Robert E. Roses, MD,c Douglas L. Fraker, MD,c Jeffrey A. Drebin, MD,c and Benjamin M. Jackson, MD,a Philadelphia, Pa Objective: We report our institutional experience of various venous reconstruction methods during oncologic resections, especially examining the patency of venous reconstructions and the conduits used. Methods: All patients undergoing venous repair or reconstruction for oncologic resections between 2008 and 2014 were identified by a retrospective search of a prospectively maintained database at a single university hospital. Extent and manner of venous reconstruction and conduit or patch material were recorded. Need for intraoperative venovenous bypass or cardiopulmonary bypass was also recorded. Whereas no prescribed follow-up protocol has been instituted, patency and survival data as available were analyzed. Results: During the study period, 127 patients were identified. Five patients had primary ligations, without limb loss. Of the remaining 122 patients, 77 (63%) underwent primary repairs, 23 (19%) had patch repair, and 22 (18%) had bypasses. Of these, 27 (22%) were for portal vein
reconstruction during a Whipple procedure, 47 (39%) were for caval repair during caval thrombectomy in the setting of renal cell cancer, and 28 (23%) were for caval repair during resection for other abdominal malignant neoplasms. Venovenous bypass was used in 16 repairs and cardiopulmonary bypass in 10. The 1-year patency rates were 100% for primary and patch repairs and 86% for bypass graft reconstructions. Occlusions were suffered only in the prosthetic grafts group. There was no limb loss or significant long-term morbidity in patients with occluded grafts. Rate of infection was 0%, and there was no evidence of an increased infection rate in prosthetic or bioprosthetic conduits or patches. Perioperative mortality was 5.5%. Conclusions: Overall, venous reconstruction for oncologic resection can be done safely with very low complication rates and low perioperative mortality. Prosthetic grafts can be used for most reconstructions with no infections and good patency rates. (J Vasc Surg: Venous and Lym Dis 2016;4:57-63.)
A variety of malignant neoplasms, such as renal cell carcinoma (RCC), pancreatic cancer, and retroperitoneal and extremity sarcomas, have potential for venous invasion. En bloc resection and venous repair and reconstruction are often required to achieve good oncologic outcomes. Methods of reconstruction vary from primary repair to interposition grafts using autologous or prosthetic conduits. Retroperitoneal tumors commonly originate from renal parenchyma or are sarcomas and can be manifested with inferior vena cava (IVC) involvement. RCC extends into the renal vein and IVC in 5% to 10% of patients.1 Presence of tumor thrombus is not a contraindication to resection and is usually amenable to removal without major IVC reconstruction. On the contrary, retroperitoneal sarcomas
often invade the wall of the IVC or in rare cases can arise from the cava itself. Intraoperative exposure and isolation of IVC depend on the extent of the tumor. The best method of IVC reconstruction after resection remains controversial. Several authors advocate primary ligations,2,3 whereas others suggest reconstruction using autologous4,5 or prosthetic conduits.6,7 Pancreatic adenocarcinoma is another malignant neoplasm that commonly is manifested with venous invasion. Portal vein (PV) or superior mesenteric vein invasion is not always a contraindication to resection.8 Several methods of reconstruction have been described in the literature, including primary or patch repair and reconstruction with interposition graft. Grafts used in prior reports include femoral and saphenous vein,9 spiral vein,10 internal jugular vein,8 left renal vein,11 and prosthetic grafts.12 Malignant neoplasms of the extremities frequently are manifested with vascular involvement. The paradigm of management of these malignant neoplasms has shifted in recent years from primary amputation to successful limb salvage.13-15 Venous resection with negative margins and successful reconstruction play an important role in these patients’ survival, limb salvage, and preservation of function. The objective of this study was to analyze a singleinstitution experience with various venous reconstruction methods during oncologic resections involving the IVC, PV, and upper and lower extremity veins. Our analysis examined the patency of venous reconstructions and the infectious risk of various conduits.
From the Division of Vascular and Endovascular Surgery,a Department of Urology,b and Division of Endocrine and Oncologic Surgery,c Hospital of the University of Pennsylvania. Author conflict of interest: none. Presented in the rapid-paced plenary session at the Forty-third Annual Symposium of the Society for Clinical Vascular Surgery, Miami, Fla, March 29-April 2, 2015. Correspondence: Yana Etkin, MD, Surgery Department, 3400 Spruce St, Silverstein Pavilion 4th Fl, Philadelphia, PA 19104 (e-mail: yana.etkin@ uphs.upenn.edu). The editors and reviewers of this article have no relevant financial relationships to disclose per the Journal policy that requires reviewers to decline review of any manuscript for which they may have a conflict of interest. 2213-333X Copyright Ó 2016 by the Society for Vascular Surgery. Published by Elsevier Inc. http://dx.doi.org/10.1016/j.jvsv.2015.05.003
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METHODS All patients undergoing venous repair or reconstruction for oncologic resections between 2008 and 2014 were identified by a retrospective search of a prospectively maintained database at a single tertiary academic medical center. Demographic characteristics, including age, gender, type of malignant disease, and vessels involved, and procedural characteristics, including extent and technique of venous reconstruction as well as type of conduit or patch material used, were collected. Need for intraoperative venovenous bypass or cardiopulmonary bypass (CPB) as well as perioperative mortality was also recorded. The majority of patients were observed by the oncology team, who routinely performed surveillance imaging, which was used to analyze patency and rate of graft infection. Survival data were analyzed on the basis of the Social Security database and hospital records. Data collection and analysis were conducted in accordance with the University of Pennsylvania Institutional Review Board. The waiver of informed consent and Health Insurance Portability and Accountability Act waiver of authorization were approved by the Institutional Review Board committee. Statistical analysis was performed with Stata software (Stata Statistical Software: Release 13; StataCorp LP, College Station, Tex). Surgical techniques. Vena cava reconstruction. Incisions used in this series included midline laparotomy and thoracoabdominal and bilateral subcostal incisions and were selected on the basis of the extent of the tumor and the surgeon’s preference. Median sternotomy was used when tumor extended into the heart. The location of proximal and distal control of the cava also depended on the extent of the tumor. The Neves and Zincke16 classification was used to define extent of tumor invasion (Table I). For level I and level II tumors, vascular control was established by isolating the infrarenal and suprarenal IVC. For level III tumors, liver mobilization was performed to obtain suprahepatic control of the IVC. For all patients with level III tumors, venovenous bypass with an extracorporeal pump and circuit was established; 16F sheaths were percutaneously placed in the femoral veins for the inflow and right internal jugular vein for the outflow. For patients with level IV tumor extension, CPB was used in collaboration with cardiac surgery. All patients requiring Table I. The Neves and Zincke classification Level I II III IV IVC, Inferior vena cava.
Extent of tumor extension Involvement of IVC at the renal vein and extending into the IVC <2 cm Involvement of infrahepatic IVC >2 cm above the renal vein Involvement of the retrohepatic IVC Involvement of the supradiaphragmatic IVC (extending into right atrium)
Fig 1. Nephrectomy and renal cell carcinoma (RCC) tumor thrombus.
venovenous bypass or CPB were heparinized. Other patients were heparinized selectively on the basis of the amount of preceding intraoperative bleeding. After vascular control was established, cavotomy and tumor extraction were performed for RCC (Fig 1), and IVC resection was performed for retroperitoneal sarcomas (Fig 2). The approach to reconstruction was dependent on the degree of caval involvement, which was determined on the basis of preoperative imaging, either contrast-enhanced computed tomography or magnetic resonance imaging. If <50% of the IVC circumference was involved, primary repair with running polypropylene sutures was performed (Fig 3). If the primary repair could not be accomplished without narrowing the IVC, patch repair with bovine pericardium was preferred (Fig 4). When circumferential replacement was necessary, 20-mm ringed polytetrafluoroethylene (PTFE) graft (Fig 5) or cryopreserved aortic homograft was used, depending on the degree of intraoperative contamination with gastrointestinal contents or urine. PV reconstruction. PV reconstruction was performed in selected cases of pancreatic and biliary cancers. Primary repair was performed if the vein could be repaired without narrowing. In other cases, autologous vein or bovine pericardial patch was used to patch the PV (Fig 6). Autologous vein was preferred in cases of significant intraoperative contamination as long as the patient was hemodynamically stable and could tolerate an additional time required for a vein harvest. If a circumferential segment of the vein required replacement, autologous vein or cryopreserved homograft was used. For the autologous vein conduit, an internal jugular vein was preferred to a saphenous vein because of a better size match. RESULTS A total of 127 patients underwent venous repairs or reconstructions for oncologic resection during the study period. Patients’ demographic characteristics, type of
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Fig 2. A, Suprarenal inferior vena cava (IVC) sarcoma. B, Surgical specimen including sarcoma and circumferential resection of the portion of the IVC.
malignant neoplasms, and vessels involved are summarized in Table II. Women constituted 56% of the cohort, with an average age of 61 years. The IVC was involved in 59% of patients, and RCC was the most common malignant neoplasm in 38.6% of patients. Five patients had primary ligations: two of the IVC (both patients had chronically occluded IVCs), one splenic vein, one femoral vein, and one axillary vein. These patients had no complications of vein ligation, including no significant new limb swelling or limb loss. Of the remaining 122 patients, 77 (63%) underwent primary repairs, 23 (19%) had patch repair with vein or bovine pericardium, and 22 (18%) had bypasses with vein, homograft, or PTFE graft (Table III). Of the 122 patients undergoing venous repair or reconstruction, 27 (22%) were for PV reconstruction during a Whipple procedure, 47 (39%) were for caval repair during caval thrombectomy in the setting of RCC, and 28 (23%) were for caval repair during resection for other
abdominal malignant neoplasms. Venovenous bypass was used in 16 repairs and CPB in 10 patients. The 30-day perioperative mortality was 5.5% (n ¼ 7). Survival rate was 78.3% at 1 year and 53.6% at 3 years. The majority of patients had serial imaging (computed tomography or magnetic resonance imaging) for oncologic surveillance, which was used to assess the patency of our reconstructions. During a median follow-up of 41 months, three patients had graft occlusions. No occlusions were observed in the primary or the patch repair groups. Kaplan-Meier estimate of graft primary patency was 85.8% at 1 year (Fig 7). Occlusions occurred only in the prosthetic graft group. Three of 11 PTFE bypasses occluded: 1 vena cava, 1 axillary vein, and 1 iliac vein bypass graft. There was no limb loss or significant longterm morbidity in patients with occluded grafts. There was no evidence of infections in patients with prosthetic or bioprosthetic conduits or patches. Four patients suffered intraoperative cardiac arrest. One patient died of postoperative intra-abdominal hemorrhage. One patient suffered bowel ischemia from superior mesenteric artery embolus. One patient had sepsis and multisystem organ failure. DISCUSSION
Fig 3. Primary inferior vena cava (IVC) repair with level II tumor involvement.
A variety of malignant neoplasms are associated with a particular biologic propensity for venous invasion. The current experience involves primarily RCCs with tumor thrombus extending into the IVC, retroperitoneal sarcomas, pancreatic adenocarcinoma, and extremity sarcomas. Therefore, each of these conditions is discussed briefly. RCC is one of the most common tumors associated with vascular invasion, and up to 10% of patients have tumor thrombus involving the renal vein or IVC, of which 2% to 16% have tumor thrombus extension into the right atrium.1,17 Nephrectomy and caval thrombectomy for RCC were first described by Berg in 1913.18 Since then, the surgical approach to caval thrombectomy in patients
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Fig 4. Inferior vena cava (IVC) patch repair with bovine pericardium.
with tumor thrombus extension into the IVC has been widely adopted and has been shown to improve patient outcomes, with up to 59% 5-year survival.19 Initial reports of caval thrombectomy of intrahepatic or suprahepatic IVC described the use of CPB.17,20 CPB decreases immediate blood loss during tumor removal; however, it is associated with higher overall blood loss, increased coagulopathy, and longer operative time.20-22 Subsequently, venovenous bypass techniques were described, which helped to minimize the blood loss without the need for CPB and associated coagulopathy and sternotomy.23,24 The investigators from Memorial Sloan Kettering recently described their experience with radical nephrectomy and tumor thrombus extraction offbypass.1 In our practice, if disease extends into the intrahepatic IVC or higher, mobilization of the liver to allow clamping of the diaphragmatic cava and venovenous bypass were
Fig 6. Portal vein (PV) patch repair with bovine pericardium.
performed. CPB was reserved for patients with tumor extending into the right atrium. Venovenous bypass was used in 20% of all caval thrombectomies for RCC in our series, and CPB was used in 15.5% of cases. Two of 10 patients who required CPB had intraoperative bleeding and subsequently died intraoperatively. Retroperitoneal sarcoma is another common malignant neoplasm that can involve the IVC. Sarcomas often invade the caval wall or are primary tumors arising from the wall itself. In these cases, en bloc resection and IVC reconstruction are essential for management because potent and effective chemoradiation regimens have not been established. Various methods of IVC reconstruction are described in the literature. Some authors advocate primary IVC ligation.2,3 However, significant complications have been reported after primary IVC ligation. In a series by Daylami et al,3 50% of patients developed lower extremity edema and 50% developed acute renal failure. We prefer IVC reconstruction when possible; only 2 of 75 patients in our series had IVC ligations. Both of these patients Table II. Patients’ demographics (N ¼ 127) Age, years Gender, % female Type of malignant neoplasm RCC Pancreatic malignant tumor Retroperitoneal sarcoma Other intra-abdominal malignant neoplasms Adrenal tumors or paragangliomas Primary IVC sarcoma Extremity sarcoma Breast cancer Vessels involved Vena cava PV Other intra-abdominal veins Upper and lower extremity veins
Fig 5. Inferior vena cava (IVC) reconstruction with 20-mm ringed polytetrafluoroethylene (PTFE) graft.
61.3 6 14.9 56 47 31 14 11 10 5 5 4
(37) (24.4) (11.0) (8.7) (7.9) (3.9) (3.9) (3.1)
75 27 15 10
(59.0) (21.3) (11.8) (7.9)
IVC, Inferior vena cava; PV, portal vein; RCC, renal cell carcinoma. Data are presented as number (%) unless otherwise indicated.
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Table III. Procedural characteristics Type of repair Primary repair Patch Bypass
Material used
PV
Vena cava
Other intra-abdominal
Extremity
Autologous vein Bovine Autologous vein Cryopreserved homograft Prosthetic graft
7 3 12 4 1 d
54 d 7 d 6 6
11 1 d d d 2
5 d d d d 3
1-Year patency, % 100 100 85.8
PV, Portal vein.
had chronically occluded IVCs preoperatively. In all other cases, caval primary repair or reconstruction with bovine patch or interposition graft was performed. The first report of IVC replacement with PTFE graft was published in 1970 by Sarti,25 which was followed by multiple publications of similarly successful repairs using prosthetic grafts.4,5,26 Other authors described using Dacron graft,27 superficial femoral vein,4,5 cryopreserved vena cava,28 or aortic homograft.29 In our series, 16% of patients had caval reconstruction with interposition graft. Half of the reconstructions were done with 20-mm ringed PTFE graft and the other half with cryopreserved aortic homograft. We prefer to use externally supported PTFE grafts over Dacron grafts because of the theoretical advantage of being resistant to compression by abdominal contents. In cases of possible intraoperative spillage of gastrointestinal contents, we customarily use aortic homograft. On follow-up imaging, no stenosis or IVC occlusions of primary and patch repairs were found in our series. One of 12 interposition grafts (8.3%), a PTFE graft, was found to be occluded during the follow-up; however, the patient was asymptomatic. Our graft patency rates compared favorably with the 89% to 94%4,6,26 reported in the literature. Adenocarcinoma of the pancreas not infrequently invades surrounding venous structures. Invasion of pancreatic tumor into the wall of the PV or superior mesenteric
Fig 7. Kaplan-Meier curve of graft patency. SE, Standard error.
vein is not a contraindication to resection but represents an additional technical challenge to pancreaticoduodenectomy. Several methods of PV reconstruction have been reported in the literature.8-12 Some authors describe PV resection and primary end-to-end anastomosis with good results8,12; however, we think that accomplishing a tension-free anastomosis is difficult by that technique. Other reports suggest using a prosthetic graft for reconstruction12,30,31; however, we think that this carries an increased risk of infection and has lower patency compared with vein grafts.9,12,30 In our series, if a circumferential segment of the vein required replacement, autologous vein or cryopreserved homograft was used. Malignant neoplasms involving major veins in the upper and lower extremities were also analyzed in this series. In recent years, progress in surgical techniques and advances in neoadjuvant therapies have facilitated successful limb salvage in these patients. In the current experience, 10 patients had extremity sarcomas or breast cancer involving veins of the upper or lower extremities. In two patients, primary ligation was performed because the involved veins were occluded preoperatively. Venous ligation does not preclude successful limb salvage and has been described in the literature.32 However, limb swelling is a significant complication of venous ligation and can cause significant disability, so we prefer to perform venous repair and reconstructions when possible. Various venous conduits for venous resections in the extremities have been described in the literature, including saphenous vein, PTFE, and Dacron.33 These have demonstrated variable patency rates of 14% to 100%.33 In our series, three of eight patients had reconstruction with PTFE, one of which occluded during the follow-up. The other five patients had primary repair. In this series, 11 reconstructions were performed with PTFE and 19 reconstructions were performed with bovine pericardium. It is a small sample size and represents only 25% of patients in our series. However, none of these patients had a graft or patch infection during the followup. This is consistent with negligible rates of graft infection reported in the literature.4,34 This study is a retrospective review of a singleinstitution experience and carries certain biases and limitations. The complication data were difficult to obtain and were limited by the information available in patients’ charts. This study was also limited by small sample size
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and heterogeneity of the study population and type of malignant neoplasms included. We are a tertiary referral center for complicated RCCs and retroperitoneal sarcomas, possibly explaining the relative predominance of caval involvement in our series. Patients were observed primarily by an oncologist, and most patients did not have dedicated follow-up by a vascular surgeon. Therefore, graft patency was largely determined on the basis of follow-up imaging done to monitor oncologic recurrence.
10.
11.
12.
CONCLUSIONS
13.
Overall, venous reconstruction for oncologic resection can be done safely by various reconstruction techniques with very low complication rates, excellent patency, and low perioperative mortality. Prosthetic grafts can be used for most reconstructions when there is no intestinal or urinary contamination. Bovine pericardium can be safely used even in cases of abdominal contamination.
14.
15.
16. 17.
AUTHOR CONTRIBUTIONS Conception and design: YE, RR, BJ Analysis and interpretation: YE, PF, GW, TG, RR, DF, JD Data collection: YE Writing the article: YE Critical revision of the article: YE, PF, GW, TG, RR, DF, JD, BJ Final approval of the article: YE, PF, GW, TG, RR, DF, JD, BJ Statistical analysis: YE, BJ Obtained funding: Not applicable Overall responsibility: BJ
18.
19.
20.
21.
22.
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reconstruction using femoral and saphenous vein during pancreaticoduodenectomy. J Vasc Surg 2010;51:662-6. Chiu KM, Chu SH, Chen JS, Li SJ, Chan CY, Chen KS. Spiral saphenous vein graft for portal vein reconstruction in pancreatic cancer. Vasc Endovascular Surg 2007;41:149-52. Smoot RL, Christein JD, Farnell MB. An innovative option for venous reconstruction after pancreaticoduodenectomy: the left renal vein. J Gastrointest Surg 2007;11:425-31. Liao K, Wang H, Chen Q, Wu Z, Zhang L. Prosthetic graft for superior mesenteric-portal vein reconstruction in pancreaticoduodenectomy: a retrospective, multicenter study. J Gastrointest Surg 2014;18: 1452-61. Fortner JG, Kim DK, Shiu MH. Limb-preserving vascular surgery for malignant tumors of the lower extremity. Arch Surg 1977;112:391-4. Imparato AM, Roses DF, Francis KC, Lewis MM. Major vascular reconstruction for limb salvage in patients with soft tissue and skeletal sarcomas of the extremities. Surg Gynecol Obstet 1978;147:892-6. Eilber FR, Mirra JJ, Grant TT, Weisenburger T, Morton DL. Is amputation necessary for sarcomas? A seven-year experience with limb salvage. Ann Surg 1980;192:431-8. Neves RJ, Zincke H. Surgical treatment of renal caner with vena cava extension. Br J Urol 1987;59:390-5. Nesbitt JC, Soltero ER, Dinney CPN, Walsh GL, Schrump DS, Swanson DA, et al. Surgical management of renal cell carcinoma with inferior vena cava tumor thrombus. Ann Thorac Surg 1997;63: 1592-600. Berg AA. Malignant hypernephroma of the kidney, its clinical course and diagnosis, with a description of the author’s method of radical operative cure. Surg Gynecol Obstet 1913;17:463-71. Blute ML, Leibovich BC, Lohse CM, Cheville JC, Zincke H. The Mayo Clinic experience with surgical management, complications and outcome for patients with renal cell carcinoma and venous tumour thrombus. BJU Int 2004;94:33-41. Novick AC, Kaye MC, Cosgrove DM, Angermeier K, Pontes JE, Montie JE, et al. Experience with cardiopulmonary bypass and deep hypothermic circulatory arrest in the management of retroperitoneal tumors with large vena cava thrombi. Ann Surg 1990;212:476-7. Klein EA, Kaye MC, Novick AC. Management of renal cell carcinoma with vena caval thrombi via cardiopulmonary bypass and deep hypothermic circulatory arrest. Urol Oncol 1991;18:445-7. Stewart JA, Carey JA, McDougal WS, Merrill WH, Koch MO, Bender HW Jr. Cavoatrial tumor thrombectomy using cardiopulmonary bypass without circulatory arrest. Ann Thorac Surg 1991;51: 717-22. Granberg CF, Boorjian SA, Schaff HV, Orszulak TA, Leibovich BC, Lohse CM, et al. Surgical management, complications, and outcome of radical nephrectomy with inferior vena cava tumor thrombectomy facilitated by vascular bypass. Urology 2008;72:148-52. Browning AJ, Eardley I, Joyce AD, Minhas S, Bellamy MC. Percutaneous veno-venous bypass in surgery for renal cell carcinoma with associated vena caval tumour thrombus. BJU Int 1999;83: 850-2. Sarti L. Total prosthetic transplantation of the inferior vena cava, with venous drainage restoration of the one remaining kidney on the graft, successfully performed on a child with Wilms’ tumor. Surgery 1970;67: 851-5. Quinones-Baldrich W, Alktaifi A, Eilber F, Eilber F. Inferior vena cava resection and reconstruction for retroperitoneal tumor excision. J Vasc Surg 2012;55:1386-93. Hyams ES, Pierorazio PM, Shah A, Lum YW, Black J, Allaf ME. Graft reconstruction of inferior vena cava for renal cell carcinoma stage pT3b or greater. Urology 2011;78:838-43. Lim JH, Sohn SH, Sung YW, Moon HJ, Choi JS, Oh SJ. Banked vena caval homograft replacement of the inferior vena cava for primary leiomyosarcoma. Korean J Thorac Cardiovasc Surg 2014;47: 473-7. Praseedom RK, Dhar P, Jamieson NV, Wallwork J, Bergman I, Lomas DJ. Leiomyosarcoma of the retrohepatic vena cava treated by excision and reconstruction with an aortic homograft: a case repot and review of literature. Surg Innov 2007;14:287-91.
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30. Stauffer JA, Dougherty MK, Kim GP, Nguyen JH. Interposition graft with polytetrafluoroethylene for mesenteric and portal vein reconstruction after pancreaticoduodenectomy. Br J Surg 2009;96:247-52. 31. Siriwardana HP, Siriwardena AK. Systematic review of outcome of synchronous portal-superior mesenteric vein resection during pancreatectomy for cancer. Br J Surg 2006;93:662-73. 32. Matsushita M, Kuzuya A, Mano N, Nishikimi N, Sakurai T, Nimura Y, et al. Sequelae after limb-sparing surgery with major vascular resection for tumor of the lower extremity. J Vasc Surg 2001;33:694-9.
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33. Nishinari K, Wolosker N, Yazbek G, Zerati AE, Nishimoto IN. Venous reconstructions in lower limbs associated with resection of malignancies. J Vasc Surg 2006;44:1046-50. 34. Hemming AW, Reed AI, Langham MR Jr, Fujita S, Howard RJ. Combined resection of the liver and inferior vena cava for hepatic malignancy. Ann Surg 2004;239:712-9.
Submitted Mar 31, 2015; accepted May 12, 2015.
Successful venous repair and reconstruction for oncologic resections Yana Etkin, MD,a Paul J. Foley, MD,a Grace J. Wang, MD,a Thomas J. Guzzo, MD,b Robert E. Roses, MD,c Douglas L. Fraker, MD,c Jeffrey A. Drebin, MD,c and Benjamin M. Jackson, MD,a Philadelphia, Pa Objective: We report our institutional experience of various venous reconstruction methods during oncologic resections, especially examining the patency of venous reconstructions and the conduits used. Methods: All patients undergoing venous repair or reconstruction for oncologic resections between 2008 and 2014 were identified by a retrospective search of a prospectively maintained database at a single university hospital. Extent and manner of venous reconstruction and conduit or patch material were recorded. Need for intraoperative venovenous bypass or cardiopulmonary bypass was also recorded. Whereas no prescribed follow-up protocol has been instituted, patency and survival data as available were analyzed. Results: During the study period, 127 patients were identified. Five patients had primary ligations, without limb loss. Of the remaining 122 patients, 77 (63%) underwent primary repairs, 23 (19%) had patch repair, and 22 (18%) had bypasses. Of these, 27 (22%) were for portal vein
reconstruction during a Whipple procedure, 47 (39%) were for caval repair during caval thrombectomy in the setting of renal cell cancer, and 28 (23%) were for caval repair during resection for other abdominal malignant neoplasms. Venovenous bypass was used in 16 repairs and cardiopulmonary bypass in 10. The 1-year patency rates were 100% for primary and patch repairs and 86% for bypass graft reconstructions. Occlusions were suffered only in the prosthetic grafts group. There was no limb loss or significant long-term morbidity in patients with occluded grafts. Rate of infection was 0%, and there was no evidence of an increased infection rate in prosthetic or bioprosthetic conduits or patches. Perioperative mortality was 5.5%. Conclusions: Overall, venous reconstruction for oncologic resection can be done safely with very low complication rates and low perioperative mortality. Prosthetic grafts can be used for most reconstructions with no infections and good patency rates. (J Vasc Surg: Venous and Lym Dis 2016;4:57-63.)
A variety of malignant neoplasms, such as renal cell carcinoma (RCC), pancreatic cancer, and retroperitoneal and extremity sarcomas, have potential for venous invasion. En bloc resection and venous repair and reconstruction are often required to achieve good oncologic outcomes. Methods of reconstruction vary from primary repair to interposition grafts using autologous or prosthetic conduits. Retroperitoneal tumors commonly originate from renal parenchyma or are sarcomas and can be manifested with inferior vena cava (IVC) involvement. RCC extends into the renal vein and IVC in 5% to 10% of patients.1 Presence of tumor thrombus is not a contraindication to resection and is usually amenable to removal without major IVC reconstruction. On the contrary, retroperitoneal sarcomas
often invade the wall of the IVC or in rare cases can arise from the cava itself. Intraoperative exposure and isolation of IVC depend on the extent of the tumor. The best method of IVC reconstruction after resection remains controversial. Several authors advocate primary ligations,2,3 whereas others suggest reconstruction using autologous4,5 or prosthetic conduits.6,7 Pancreatic adenocarcinoma is another malignant neoplasm that commonly is manifested with venous invasion. Portal vein (PV) or superior mesenteric vein invasion is not always a contraindication to resection.8 Several methods of reconstruction have been described in the literature, including primary or patch repair and reconstruction with interposition graft. Grafts used in prior reports include femoral and saphenous vein,9 spiral vein,10 internal jugular vein,8 left renal vein,11 and prosthetic grafts.12 Malignant neoplasms of the extremities frequently are manifested with vascular involvement. The paradigm of management of these malignant neoplasms has shifted in recent years from primary amputation to successful limb salvage.13-15 Venous resection with negative margins and successful reconstruction play an important role in these patients’ survival, limb salvage, and preservation of function. The objective of this study was to analyze a singleinstitution experience with various venous reconstruction methods during oncologic resections involving the IVC, PV, and upper and lower extremity veins. Our analysis examined the patency of venous reconstructions and the infectious risk of various conduits.
From the Division of Vascular and Endovascular Surgery,a Department of Urology,b and Division of Endocrine and Oncologic Surgery,c Hospital of the University of Pennsylvania. Author conflict of interest: none. Presented in the rapid-paced plenary session at the Forty-third Annual Symposium of the Society for Clinical Vascular Surgery, Miami, Fla, March 29-April 2, 2015. Correspondence: Yana Etkin, MD, Surgery Department, 3400 Spruce St, Silverstein Pavilion 4th Fl, Philadelphia, PA 19104 (e-mail: yana.etkin@ uphs.upenn.edu). The editors and reviewers of this article have no relevant financial relationships to disclose per the Journal policy that requires reviewers to decline review of any manuscript for which they may have a conflict of interest. 2213-333X Copyright Ó 2016 by the Society for Vascular Surgery. Published by Elsevier Inc. http://dx.doi.org/10.1016/j.jvsv.2015.05.003
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METHODS All patients undergoing venous repair or reconstruction for oncologic resections between 2008 and 2014 were identified by a retrospective search of a prospectively maintained database at a single tertiary academic medical center. Demographic characteristics, including age, gender, type of malignant disease, and vessels involved, and procedural characteristics, including extent and technique of venous reconstruction as well as type of conduit or patch material used, were collected. Need for intraoperative venovenous bypass or cardiopulmonary bypass (CPB) as well as perioperative mortality was also recorded. The majority of patients were observed by the oncology team, who routinely performed surveillance imaging, which was used to analyze patency and rate of graft infection. Survival data were analyzed on the basis of the Social Security database and hospital records. Data collection and analysis were conducted in accordance with the University of Pennsylvania Institutional Review Board. The waiver of informed consent and Health Insurance Portability and Accountability Act waiver of authorization were approved by the Institutional Review Board committee. Statistical analysis was performed with Stata software (Stata Statistical Software: Release 13; StataCorp LP, College Station, Tex). Surgical techniques. Vena cava reconstruction. Incisions used in this series included midline laparotomy and thoracoabdominal and bilateral subcostal incisions and were selected on the basis of the extent of the tumor and the surgeon’s preference. Median sternotomy was used when tumor extended into the heart. The location of proximal and distal control of the cava also depended on the extent of the tumor. The Neves and Zincke16 classification was used to define extent of tumor invasion (Table I). For level I and level II tumors, vascular control was established by isolating the infrarenal and suprarenal IVC. For level III tumors, liver mobilization was performed to obtain suprahepatic control of the IVC. For all patients with level III tumors, venovenous bypass with an extracorporeal pump and circuit was established; 16F sheaths were percutaneously placed in the femoral veins for the inflow and right internal jugular vein for the outflow. For patients with level IV tumor extension, CPB was used in collaboration with cardiac surgery. All patients requiring Table I. The Neves and Zincke classification Level I II III IV IVC, Inferior vena cava.
Extent of tumor extension Involvement of IVC at the renal vein and extending into the IVC <2 cm Involvement of infrahepatic IVC >2 cm above the renal vein Involvement of the retrohepatic IVC Involvement of the supradiaphragmatic IVC (extending into right atrium)
Fig 1. Nephrectomy and renal cell carcinoma (RCC) tumor thrombus.
venovenous bypass or CPB were heparinized. Other patients were heparinized selectively on the basis of the amount of preceding intraoperative bleeding. After vascular control was established, cavotomy and tumor extraction were performed for RCC (Fig 1), and IVC resection was performed for retroperitoneal sarcomas (Fig 2). The approach to reconstruction was dependent on the degree of caval involvement, which was determined on the basis of preoperative imaging, either contrast-enhanced computed tomography or magnetic resonance imaging. If <50% of the IVC circumference was involved, primary repair with running polypropylene sutures was performed (Fig 3). If the primary repair could not be accomplished without narrowing the IVC, patch repair with bovine pericardium was preferred (Fig 4). When circumferential replacement was necessary, 20-mm ringed polytetrafluoroethylene (PTFE) graft (Fig 5) or cryopreserved aortic homograft was used, depending on the degree of intraoperative contamination with gastrointestinal contents or urine. PV reconstruction. PV reconstruction was performed in selected cases of pancreatic and biliary cancers. Primary repair was performed if the vein could be repaired without narrowing. In other cases, autologous vein or bovine pericardial patch was used to patch the PV (Fig 6). Autologous vein was preferred in cases of significant intraoperative contamination as long as the patient was hemodynamically stable and could tolerate an additional time required for a vein harvest. If a circumferential segment of the vein required replacement, autologous vein or cryopreserved homograft was used. For the autologous vein conduit, an internal jugular vein was preferred to a saphenous vein because of a better size match. RESULTS A total of 127 patients underwent venous repairs or reconstructions for oncologic resection during the study period. Patients’ demographic characteristics, type of
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Fig 2. A, Suprarenal inferior vena cava (IVC) sarcoma. B, Surgical specimen including sarcoma and circumferential resection of the portion of the IVC.
malignant neoplasms, and vessels involved are summarized in Table II. Women constituted 56% of the cohort, with an average age of 61 years. The IVC was involved in 59% of patients, and RCC was the most common malignant neoplasm in 38.6% of patients. Five patients had primary ligations: two of the IVC (both patients had chronically occluded IVCs), one splenic vein, one femoral vein, and one axillary vein. These patients had no complications of vein ligation, including no significant new limb swelling or limb loss. Of the remaining 122 patients, 77 (63%) underwent primary repairs, 23 (19%) had patch repair with vein or bovine pericardium, and 22 (18%) had bypasses with vein, homograft, or PTFE graft (Table III). Of the 122 patients undergoing venous repair or reconstruction, 27 (22%) were for PV reconstruction during a Whipple procedure, 47 (39%) were for caval repair during caval thrombectomy in the setting of RCC, and 28 (23%) were for caval repair during resection for other
abdominal malignant neoplasms. Venovenous bypass was used in 16 repairs and CPB in 10 patients. The 30-day perioperative mortality was 5.5% (n ¼ 7). Survival rate was 78.3% at 1 year and 53.6% at 3 years. The majority of patients had serial imaging (computed tomography or magnetic resonance imaging) for oncologic surveillance, which was used to assess the patency of our reconstructions. During a median follow-up of 41 months, three patients had graft occlusions. No occlusions were observed in the primary or the patch repair groups. Kaplan-Meier estimate of graft primary patency was 85.8% at 1 year (Fig 7). Occlusions occurred only in the prosthetic graft group. Three of 11 PTFE bypasses occluded: 1 vena cava, 1 axillary vein, and 1 iliac vein bypass graft. There was no limb loss or significant longterm morbidity in patients with occluded grafts. There was no evidence of infections in patients with prosthetic or bioprosthetic conduits or patches. Four patients suffered intraoperative cardiac arrest. One patient died of postoperative intra-abdominal hemorrhage. One patient suffered bowel ischemia from superior mesenteric artery embolus. One patient had sepsis and multisystem organ failure. DISCUSSION
Fig 3. Primary inferior vena cava (IVC) repair with level II tumor involvement.
A variety of malignant neoplasms are associated with a particular biologic propensity for venous invasion. The current experience involves primarily RCCs with tumor thrombus extending into the IVC, retroperitoneal sarcomas, pancreatic adenocarcinoma, and extremity sarcomas. Therefore, each of these conditions is discussed briefly. RCC is one of the most common tumors associated with vascular invasion, and up to 10% of patients have tumor thrombus involving the renal vein or IVC, of which 2% to 16% have tumor thrombus extension into the right atrium.1,17 Nephrectomy and caval thrombectomy for RCC were first described by Berg in 1913.18 Since then, the surgical approach to caval thrombectomy in patients
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Fig 4. Inferior vena cava (IVC) patch repair with bovine pericardium.
with tumor thrombus extension into the IVC has been widely adopted and has been shown to improve patient outcomes, with up to 59% 5-year survival.19 Initial reports of caval thrombectomy of intrahepatic or suprahepatic IVC described the use of CPB.17,20 CPB decreases immediate blood loss during tumor removal; however, it is associated with higher overall blood loss, increased coagulopathy, and longer operative time.20-22 Subsequently, venovenous bypass techniques were described, which helped to minimize the blood loss without the need for CPB and associated coagulopathy and sternotomy.23,24 The investigators from Memorial Sloan Kettering recently described their experience with radical nephrectomy and tumor thrombus extraction offbypass.1 In our practice, if disease extends into the intrahepatic IVC or higher, mobilization of the liver to allow clamping of the diaphragmatic cava and venovenous bypass were
Fig 6. Portal vein (PV) patch repair with bovine pericardium.
performed. CPB was reserved for patients with tumor extending into the right atrium. Venovenous bypass was used in 20% of all caval thrombectomies for RCC in our series, and CPB was used in 15.5% of cases. Two of 10 patients who required CPB had intraoperative bleeding and subsequently died intraoperatively. Retroperitoneal sarcoma is another common malignant neoplasm that can involve the IVC. Sarcomas often invade the caval wall or are primary tumors arising from the wall itself. In these cases, en bloc resection and IVC reconstruction are essential for management because potent and effective chemoradiation regimens have not been established. Various methods of IVC reconstruction are described in the literature. Some authors advocate primary IVC ligation.2,3 However, significant complications have been reported after primary IVC ligation. In a series by Daylami et al,3 50% of patients developed lower extremity edema and 50% developed acute renal failure. We prefer IVC reconstruction when possible; only 2 of 75 patients in our series had IVC ligations. Both of these patients Table II. Patients’ demographics (N ¼ 127) Age, years Gender, % female Type of malignant neoplasm RCC Pancreatic malignant tumor Retroperitoneal sarcoma Other intra-abdominal malignant neoplasms Adrenal tumors or paragangliomas Primary IVC sarcoma Extremity sarcoma Breast cancer Vessels involved Vena cava PV Other intra-abdominal veins Upper and lower extremity veins
Fig 5. Inferior vena cava (IVC) reconstruction with 20-mm ringed polytetrafluoroethylene (PTFE) graft.
61.3 6 14.9 56 47 31 14 11 10 5 5 4
(37) (24.4) (11.0) (8.7) (7.9) (3.9) (3.9) (3.1)
75 27 15 10
(59.0) (21.3) (11.8) (7.9)
IVC, Inferior vena cava; PV, portal vein; RCC, renal cell carcinoma. Data are presented as number (%) unless otherwise indicated.
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Table III. Procedural characteristics Type of repair Primary repair Patch Bypass
Material used
PV
Vena cava
Other intra-abdominal
Extremity
Autologous vein Bovine Autologous vein Cryopreserved homograft Prosthetic graft
7 3 12 4 1 d
54 d 7 d 6 6
11 1 d d d 2
5 d d d d 3
1-Year patency, % 100 100 85.8
PV, Portal vein.
had chronically occluded IVCs preoperatively. In all other cases, caval primary repair or reconstruction with bovine patch or interposition graft was performed. The first report of IVC replacement with PTFE graft was published in 1970 by Sarti,25 which was followed by multiple publications of similarly successful repairs using prosthetic grafts.4,5,26 Other authors described using Dacron graft,27 superficial femoral vein,4,5 cryopreserved vena cava,28 or aortic homograft.29 In our series, 16% of patients had caval reconstruction with interposition graft. Half of the reconstructions were done with 20-mm ringed PTFE graft and the other half with cryopreserved aortic homograft. We prefer to use externally supported PTFE grafts over Dacron grafts because of the theoretical advantage of being resistant to compression by abdominal contents. In cases of possible intraoperative spillage of gastrointestinal contents, we customarily use aortic homograft. On follow-up imaging, no stenosis or IVC occlusions of primary and patch repairs were found in our series. One of 12 interposition grafts (8.3%), a PTFE graft, was found to be occluded during the follow-up; however, the patient was asymptomatic. Our graft patency rates compared favorably with the 89% to 94%4,6,26 reported in the literature. Adenocarcinoma of the pancreas not infrequently invades surrounding venous structures. Invasion of pancreatic tumor into the wall of the PV or superior mesenteric
Fig 7. Kaplan-Meier curve of graft patency. SE, Standard error.
vein is not a contraindication to resection but represents an additional technical challenge to pancreaticoduodenectomy. Several methods of PV reconstruction have been reported in the literature.8-12 Some authors describe PV resection and primary end-to-end anastomosis with good results8,12; however, we think that accomplishing a tension-free anastomosis is difficult by that technique. Other reports suggest using a prosthetic graft for reconstruction12,30,31; however, we think that this carries an increased risk of infection and has lower patency compared with vein grafts.9,12,30 In our series, if a circumferential segment of the vein required replacement, autologous vein or cryopreserved homograft was used. Malignant neoplasms involving major veins in the upper and lower extremities were also analyzed in this series. In recent years, progress in surgical techniques and advances in neoadjuvant therapies have facilitated successful limb salvage in these patients. In the current experience, 10 patients had extremity sarcomas or breast cancer involving veins of the upper or lower extremities. In two patients, primary ligation was performed because the involved veins were occluded preoperatively. Venous ligation does not preclude successful limb salvage and has been described in the literature.32 However, limb swelling is a significant complication of venous ligation and can cause significant disability, so we prefer to perform venous repair and reconstructions when possible. Various venous conduits for venous resections in the extremities have been described in the literature, including saphenous vein, PTFE, and Dacron.33 These have demonstrated variable patency rates of 14% to 100%.33 In our series, three of eight patients had reconstruction with PTFE, one of which occluded during the follow-up. The other five patients had primary repair. In this series, 11 reconstructions were performed with PTFE and 19 reconstructions were performed with bovine pericardium. It is a small sample size and represents only 25% of patients in our series. However, none of these patients had a graft or patch infection during the followup. This is consistent with negligible rates of graft infection reported in the literature.4,34 This study is a retrospective review of a singleinstitution experience and carries certain biases and limitations. The complication data were difficult to obtain and were limited by the information available in patients’ charts. This study was also limited by small sample size
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and heterogeneity of the study population and type of malignant neoplasms included. We are a tertiary referral center for complicated RCCs and retroperitoneal sarcomas, possibly explaining the relative predominance of caval involvement in our series. Patients were observed primarily by an oncologist, and most patients did not have dedicated follow-up by a vascular surgeon. Therefore, graft patency was largely determined on the basis of follow-up imaging done to monitor oncologic recurrence.
10.
11.
12.
CONCLUSIONS
13.
Overall, venous reconstruction for oncologic resection can be done safely by various reconstruction techniques with very low complication rates, excellent patency, and low perioperative mortality. Prosthetic grafts can be used for most reconstructions when there is no intestinal or urinary contamination. Bovine pericardium can be safely used even in cases of abdominal contamination.
14.
15.
16. 17.
AUTHOR CONTRIBUTIONS Conception and design: YE, RR, BJ Analysis and interpretation: YE, PF, GW, TG, RR, DF, JD Data collection: YE Writing the article: YE Critical revision of the article: YE, PF, GW, TG, RR, DF, JD, BJ Final approval of the article: YE, PF, GW, TG, RR, DF, JD, BJ Statistical analysis: YE, BJ Obtained funding: Not applicable Overall responsibility: BJ
18.
19.
20.
21.
22.
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30. Stauffer JA, Dougherty MK, Kim GP, Nguyen JH. Interposition graft with polytetrafluoroethylene for mesenteric and portal vein reconstruction after pancreaticoduodenectomy. Br J Surg 2009;96:247-52. 31. Siriwardana HP, Siriwardena AK. Systematic review of outcome of synchronous portal-superior mesenteric vein resection during pancreatectomy for cancer. Br J Surg 2006;93:662-73. 32. Matsushita M, Kuzuya A, Mano N, Nishikimi N, Sakurai T, Nimura Y, et al. Sequelae after limb-sparing surgery with major vascular resection for tumor of the lower extremity. J Vasc Surg 2001;33:694-9.
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Submitted Mar 31, 2015; accepted May 12, 2015.