Inferior Vena Cava Reconstruction Using a Ringed Polytetrafluoroethylene Interposition Graft and Inferior Vena Cava Filter Placement Following Resection of Renal Cell Carcinoma With a Tumor Thrombus Directly Infiltrating the Inferior Vena Cava

Abstract

Background

Renal cell carcinoma (RCC) with tumor thrombus (TT) may extend into and, in rare cases, actually invade the inferior vena cava (IVC). Techniques of IVC reconstruction after removal of the RCC, TT, and infiltrated portion of the IVC have not been well documented. Methods A ringed polytetrafluoroethylene (PTFE) interposition graft along with an IVC filter placed within the graft (to prevent the development of pulmonary emboli) was used for patients who underwent surgical resection of RCC with TT extending into and directly invading the wall of the IVC. Demographic information about these patients along with their pathology reports, surgical procedures, and patency of the PTFE graft was obtained and described. Results Four male patients were identified as having RCC and TT with histologic invasion of the IVC requiring IVC dissection and replacement with a PTFE graft (as described above); their TT levels were II, IIIa, IIIc, and IV, respectively. Patient ages were 58, 65, 58, and 51 years and tumor sizes were 7.5, 7.5, 15.0, and 6.5 cm, respectively. These patients were followed for 36, 24, 32, and 48 months, respectively. At last follow-up, each patient had a patent IVC graft, and none of them developed any pulmonary emboli post-operatively. Conclusions Ringed PTFE interposition graft along with an IVC filter deployed inside the graft appears to be a safe vascular conduit for IVC reconstruction after surgical resection of RCC with TT directly invading the IVC.

Keywords

renal cell carcinoma tumor thrombus IVC reconstruction

Introduction

Renal cell carcinoma (RCC) is the most common malignant tumor of the kidney. Over 73,750 new cases were diagnosed in 2020.¹ RCC has a myriad of presentations, and although infrequently encountered, it may extend by a tumor thrombus (TT) into the inferior vena cava (IVC) and right atrium.^2-6 The TT inside the IVC can be very bulky and may directly invade the IVC, requiring dissection and/or grafting of the IVC. The surgical approach has evolved as techniques^2-6 and prosthetics have been refined.^7-9

We report our experience of RCC with a TT directly infiltrating the wall of the IVC. Replacement of the affected portion of the IVC with a ringed polytetrafluoroethylene (PTFE) interposition graft was necessary in 4 patients with partial obstruction of the IVC. The novel aspect in using this technique was the introduction of an IVC filter inside the PTFE after performing anastomosis of the PTFE to the proximal IVC and corresponding (right or left) renal vein but before performing anastomosis to the distal portions of the IVC. The IVC filter was placed below the anastomosis of the corresponding (right or left) renal vein.

Material and Methods

This study was performed after obtaining Institutional Review Board approval of the University of Miami Miller School of Medicine (# 20200791) and following the ethical principles of the Helsinki Declaration (as revised in 2013). A written informed consent was obtained from the participants in this study. A retrospective chart review was performed on 4 patients at our institution who underwent surgical treatment for large, aggressive, locally advanced RCC with direct TT infiltration of the IVC wall. None of the patients had significant lower extremity edema. Abdominal computed tomography and/or magnetic resonance imaging were used to diagnose the renal tumor, delineate the TT inside the IVC, and depict the extent of invasion of the IVC. Cardiac, renal, and respiratory status were evaluated pre-operatively. Cranial extent of the TT into the IVC was defined as Level II, III, or IV by a previous classification.¹⁰ However, 2 patients had level IIIa (retrohepatic) and level IIIC (suprahepatic, infradiaphragmatic) TT according to our further subclassification.¹¹ For pathological staging, the 2009-TNM classification was used. Tumor grade was classified according to the Furhman grading system. Informed consent was given, including the complexity of the surgery, risks associated with handling and removal of the TT, the possibility of TT pulmonary emboli occurring during IVC manipulation, and the possibility of IVC reconstrucution being required (along with placement of an IVC filter). Intermittent pneumatic compression device, early ambulation, and subcutaneous heparin (5000 U twice/day) started 72 hours after surgery were used as prophylaxis for post-operative venous thromboembolism. Before going home, patients were started on aspirin 325 mg daily.

Intraoperative transesophageal echocardiography (TEE) was used to delineate and monitor the cranieal extent of the TT during the surgical procedure. All relevant data on demographics, surgical details, pathology characteristics, postoperative complications, and major clinical outcomes were collected and analyzed.

Surgical Technique

The organ transplant–based approach that we use includes piggy-back liver mobilization and en bloc mobilization of the spleen and pancreas which facilitates the resection of right or left large renal tumors; these techniques have been previously described.^2-6

Briefly, a modified chevron incision was used, commencing approximately 2 fingerbreadths below the right or left costal margin and extending out laterally to the mid-axillary line. Exposure was gained via the use of a Thompson retractor. Exposure of the left kidney began by mobilization of the descending colon. A left-sided tumor required that the spleen was dissected off the diaphragm and mobilized en bloc with the pancreas toward the midline. This exposes the entire upper retroperitoneal space from the diaphragm to the inferior border of the kidney. The right or left kidney was mobilized laterally and posteriorly, and the perirenal collateral circulation was ligated. The collateral circulation collapsed, making the remaining dissection easier to perform. The renal artery was identified, ligated, and divided posteriorly after a midline rotation of the kidney with the tumor.¹²

To access the retrohepatic IVC, the liver was completely mobilized off the IVC using an organ transplant–based approach, with the only remaining structural attachments being the hepatic veins and porta hepatis (piggyback liver mobilization).^2-6 Furthermore, a plane was created between the IVC and posterior abdominal wall. Small tributaries can become engorged to look like lumbar vessels, and they need to be identified and ligated. The advantage of creating this plane was to facilitate circumferential control of the IVC. Vascular isolation of the IVC was then achieved inferior and superior to the TT and to the left and right renal veins.

Of note, the patient with RCC and level II TT did not require such an extensive liver mobilization. The IVC was dissected enough to place vascular clamps at the levels of the proximal and distal IVC and at the level of the left renal vein. The vascular clamps were placed to include normal IVC for the vascular reconstruction.

For the patient with a level IIIa retrohepatic TT, the liver was fully dissected off the IVC and the small hepatic veins were ligated as described.^2-6 It was sufficient to allow removal of the TT.

For the patient with a level IIIc TT (suprahepatic, infradiaphragmatic), due to extension of the TT into the diaphragm, the central diaphragm tendon was dissected to the supra-diaphragmatic area, and the intra-pericardial IVC was identified. The dissection was circumferential so that the intra-pericardial IVC could be identified.

Use of intraoperative TEE was critical to delineate the cranial extent and mobility of the TT during dissection of either the retrohepatic or supra-diaphragmatic IVC. In addition, its use ensured that there were no pulmonary artery emboli or TT extending into the right atrium. In addition, the intraoperative TEE guided us during application of the supra-diaphragmatic IVC vascular clamp, ensuring that the clamp excluded TT.

For the patient with level IIIa TT, vascular clamps were placed in the infra-renal IVC followed by the left renal vein and below the major hepatic veins (MHVs) without the need of a Pringle maneuver.

The level IIIc TT of the third patient could not be “milked” downward out of the suprahepatic IVC, as this patient’s TT was bulky and not freely mobile. In this case, a Pringle maneuver was performed to temporarily occlude blood inflow to the liver. Vascular clamps were placed in the infra-renal vena cava, followed by the right renal and adrenal veins, and a Satinsky clamp was placed across the supra-diaphragmatic IVC (under TEE monitoring). The IVC was incised from the MHVs to the renal vein, and the TT was removed. In some areas, the TT was dissected sharply off the IVC wall. The 3 MHVs were visualized, and their orifices were inspected. Following removal of TT and closure of the upper cava, the vascular clamp was repositioned below the hepatic veins. The Pringle maneuver was discontinued, and blood flow to the liver was re-established. Clamping below the MHVs generally allows for a timewise short Pringle maneuver.

Regarding the fourth patient, the TT inside the right atrium was bulky and could not be milked downward. He required cardiopulmonary bypass (CPB).¹³ After CPB was initiated, the right atrium was opened and the TT was removed as described before.¹³ During the CBP, a Pringle maneuver was infra-renal vena cava, followed by the left renal vein. Once the opening of the right atrium was sutured and CPB removed, the rest of the procedure was similar as described for the third patient with level IIIc TT.

Following removal of the level IIIc and IV TTs and closure of the upper cava, the vascular clamp was repositioned below the MHVs. The remaining IVC below the MHVs was removed in both cases due to the infiltration/invasion of its wall at multiple sites (Figure 1A).

Figure 1.

(A) Resected inferior vena cava (IVC) with adherent tumor thrombus (white arrow), (B) drawing showing the deployed IVC filter inside the ringed PTFE graft (black arrow), (C) intraoperative ringed PTFE graft anastomosed to the proximal (P) and distal (D) IVC and left renal vein (LRV), (D) Coronal computed tomography scan demonstrating open-ringed PTFE graft (dotted white arrow) with IVC filter (white arrow) 2 years after en bloc resection of renal cell carcinoma with tumor thrombus and IVC.

The IVC was replaced with a vascular conduit of ringed PTFE graft. The PTFE graft was anastomosed to the proximal IVC with 4-0 Prolene and to the left or right renal vein with 5-0 Prolene. Then, a vascular clamp was placed below the right or left renal vein, and the rest of vascular clamps were released. A Trapease^® permanent IVC filter was deployed inside the ringed PTFE graft before finishing the distal anastomosis with 4-0 Prolene (Figure 1B). Three patients had the left renal vein anastomosed to the PTFE graft (Figure 1C), and the third patient with left RCC and level IIIc TT, a patch of tumor-free IVC with right adrenal and renal veins, was anastomosed to the ringed PTFE graft.

For each patient, at the end of surgery, a TEE was re-performed to rule out any pulmonary artery emboli or piece of TT being left behind.

Results

All relevant data on demographics, surgical details, pathology characteristics, postoperative complications, and subsequent clinical outcomes were collected and included in Table 1 (patients were ordered according to their TT level. All the patients were male, and their ages at surgery were 58, 65, 58, and 51, respectively. The tumor was right-sided in 3 patients; tumor sizes were 7.5, 7.5, 15.0, and 6.5 cm, respectively. Each of these tumors was removed via a trans-abdominal approach, and only one patient with a level IV, bulky right atrium TT required CPB. For the first 3 patients, estimated blood loss was 1500, 500, and 1500cc, and transfusions of packed red blood cells were 2, 0, and 4U, respectively. Blood loss in the fourth patient who required CPB was 2150cc; this patient was transfused with 5U of packed red blood cells and also received 600cc of cell saver. The operative time for the first 3 patients was 345, 348, and 449 minutes, respectively. The last patient who required CPB had an operative time of 664 minutes.

Table 1.

Main Characteristics of the Patients.

Patient	#1	#2	#3	#4
Demographic variable
Age (years)	58	65	58	51
Gender	M	M	M	M
Pre-operative diagnostic variables
Laterality	R	R	L	R
Tumor size (cm)	7.5	7.5	15	6.5
Tumor thrombus level (N&Z)	II	III	III	IV
Tumor thrombus level (UM)		IIIa	IIIc
Intraoperative variables
EBL (cc)	1500	500	1500	2150
Transfusion rate (PRBC units)	2 U	0 U	4 U	5 U, 600cc of cellsaver
Size of the PTFE graft (mm)	20	16	16	20
Main outcomes
Complications (30 days)	None	None	None	None
CPB	No	No	No	Yes
OR Time (min)	345	348	449	664
LOS (days)	6	7	6	22
pTNM (2009)	pT3cN0M0	pT3cN0M0	pT3cN0M0	pT3cN0M0
Pathology-variant	RCC—clear type	RCC—clear type, sarcomatoid, rhabdoid features (30% of the specimen)	RCC—papillary type	RCC—clear type
Furhman grade	III	IV	IV	IV
Lymph nodes (+/total)	0/10	0/7	0/3	0/5
Pre-operative Cr (mg/dl)	1.0	1.37	1.65	.94
Post-operative Cr^a(mg/dl)	1.1	1.5	1.15	1.2
Follow-up (months)	36	24	32	48
Status at last follow-up	Alive	Alive	Alive	Alive (multiple metastases)
Anticoagulation	ASA 325 mg	ASA 325 mg	ASA 325 mg	ASA 325 mg
Patency of IVC graft at last follow-up	Yes	Yes	Yes	Yes

N&Z, Neves and Zincke Classification system; UM, University of Miami Classification System; M, male; R, right; L, left; EBL, estimated blood loss; PRBC, packed red blood cells; PTFE, polytetrafluroethylene; CPB, cardiopulmonary bypass; OR, operative time; LOS, length of stay; Cr, creatinine; ASA, aspirin.

^aPost-operative value was determined at post-operative day 7.

The post-operative courses for each of the 4 patients were uneventful.

None of the patients presented with distant metastasis (all were M0), and none of the patients had positive lymph nodes (all were N0). For patients #1, #2, and #4, the RCC was clear cell type; patient #3 had a papillary cell type. Length of hospital stay (LOS) was 6, 7, and 6 days for patients #1–#3, respectively, and 22 days for patient #4. Each patient was discharged with stable renal function (Table 1). Post-surgical follow-up for the 4 patients have been through 36, 24, 32, and 48 months, respectively. The ringed PTFE graft with the IVC filter remained patent throughout each patient’s follow-up period and without any evidence of disease recurrence at the IVC resection site (Figure 1.D). None of the patients experienced a post-operative pulmonary embolic event. Overall survival at 2 years following surgery was 100%. At last follow-up, the fourth patient was being followed by oncology due to the development of multiple bone metastasis; the other 3 patients remained disease-free at last follow-up.

Discussion

RCC with TT extension into the IVC, and sometimes even into the right atrium, continues to be a technically challenging and complex urological surgery to perform successfully.^2-7 One of the more stressful surgical problems occurs when the IVC is partially or completely obstructed by the TT. The TT may directly invade the wall of the IVC, and it is almost impossible to determine before surgery whether the TT has invaded the IVC wall. During surgery, the IVC should be carefully inspected to determine where and to what extent the infiltration/invasion by the TT has occurred. In certain circumstances, the TT, while bulky, is not attached to the wall of the IVC, and the IVC can be surgically resected and repaired where needed; otherwise, its continuity can be restored with the use of a synthetic or homologous venous graft.^7-9,14

Here, we reported our experience in surgically removing RCC with TT that has directly infiltrated the IVC. The most important aspect of this report is the reconstruction of the IVC with a ringed PTFE graft and an IVC filter inserted into the tubal graft before the vascular anastomoses to the remnant distal IVC was performed. The IVC filter was used in these 4 patients because of the possibility of an existing distal bland thrombus, which could not be determined before or during the surgery.¹⁵ The concept of including an IVC filter has not been previously described in the literature for surgical resection of RCC with TT. The interposition grafts remained patent throughout each patient’s follow-up period, and there was no evidence of disease recurrence at the surgical resection site. None of the patients had a post-operative pulmonary embolic event.

In all 4 patients, abdominal computed tomography and/or magnetic resonance imaging did not show chronic IVC obstruction, but in each case, there was a possibility that IVC infiltration had occurred. After performing an en bloc radical nephrectomy, tumor thrombectomy, and IVC resection, PTFE grafting was necessary in the absence (or poor development) of collateral circulation. The PTFE graft is a synthetic material which is often used as IVC replacement.^7-9 The ringed PTFE graft has a low thrombogenic potential and a comfortable patency rate for low flow vessels like the IVC.^8,9,14

In 1998, Sarkar et al. reported that only 1 of 10 patients with a prosthetic IVC replacement had graft thrombosis at a mean follow-up of 19 months.¹⁶ Caso et al reported their outcomes in 5 asymptomatic patients with incomplete IVC obstruction who underwent reconstruction of the IVC with PTFE (4 cases) and Dacron (1 case) grafts for different urologic malignancies. Only one of these 5 patients had RCC with TT, and reconstruction of the IVC was performed with the Dacron graft which subsequently occluded at 9 months of follow-up.¹⁴ Recently, Benkirane et al reported that graft thrombosis developed in 5 out of 26 (19.2%) RCC patients with caval thrombus during the first year of follow-up. Patency of the IVC graft at 6 and 12 months was 88% and 79%, respectively.⁸

We described in our early experience the routine use of a PTFE interposition graft to replace the IVC gap after extensive surgical resection.¹⁵ It was subsequently observed that patients with complete IVC obstruction caused by the TT did not necessarily need IVC replacement, as most of such patients did not have preoperative lower extremity edema (indicating that sufficient collateral circulation had already developed). Those patients tolerated total IVC interruption or removal.^15,17,18

Conclusions

To conclude, when RCC included direct IVC infiltration by the TT, the IVC can be replaced by a ringed PTFE and the novelty of this approach is that an IVC filter can be deployed before completing the distal IVC anastomosis. None of the patients experienced a post-operative pulmonary emboli event, and the PTFE graft in each patient was patent at last follow-up. Nevertheless, there are 2 questions still to be answered when dealing with RCC extending into the IVC and the TT invading/infiltrating the IVC wall. First, does resection of the IVC invaded by TT increase cancer-specific survival? That is, by removing the cava, will the probability of a local recurrence developing at the IVC resection site be reduced?¹⁹ Second, when primarily removing the TT from the IVC without IVC resection or replacement and leaving behind areas of severe endothelial damage, is it sufficient to reasonably conclude that a negative surgical margin has been achieved?

Footnotes

Author Contributions

Gaetano Ciancio: Conceptualization, methodology, investigation, writing—original draft, visualization, supervision, and formal analysis.

Declaration of Conflicting Interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) received no financial support for the research, authorship, and/or publication of this article.

ORCID iD

Gaetano Ciancio

References

Siegel

Miller

Jemal

. Cancer statistics, 2020. CA Cancer J Clin. 2020;70:7-30.

Ciancio

Gonzalez

Shirodkar

, et al. Liver transplantation techniques for the surgical management of renal cell carcinoma with tumor thrombus in the inferior vena cava: Step-by-step description. Eur Urol 2011;59(3):401-406.

Ciancio

Livingstone

Soloway

. Surgical management of renal cell carcinoma with tumor thrombus in the renal and inferior vena cava: The University of Miami experience in using liver transplantation techniques. Eur Urol 2007;51(4):988-994; discussion 94-5.

Ciancio

Hawke

Soloway

. The use of liver transplant techniques to aid in the surgical management of urological tumors. J Urol 2000;164:665-672.

Ciancio

Vaidya

Shirodkar

, et al. En bloc mobilization of the pancreas and spleen to facilitate resection of large tumors, primarily renal and adrenal, in the left upper quadrant of the abdomen: Techniques derived from multivisceral transplantation. Eur Urol 2009; 55:1106-1111.

González

Gaynor

Martínez-Salamanca

, et al. Association of an organ transplant-based approach with a dramatic reduction in postoperative complications following radical nephrectomy and tumor thrombectomy in renal cell carcinoma. Eur J Surg Oncol. 2019;45:1983-1992.

González

Gorin

Garcia-Roig

, et al. Inferior vena cava resection and reconstruction: Technical considerations in the surgical management of renal cell carcinoma with tumor thrombus. Urol Oncol. 2014;32:34.e19-26.

Benkirane

Khodari

Yakoubi

, et al. Polytetrafluoroethylene expanded prosthesis as replacement of the inferior vena cava in renal cell carcinoma with caval thrombus. Int J Urol. 2014;21:448-452.

Okada

Kumada

Terachi

, et al. Long-term followup of patients with tumor thrombi from renal cell carcinoma and total replacement of the inferior vena cava using an expanded polytetrafluoroethylene tubular graft. J Urol. 1996;155:444-446; discussion 447.

10.

Neves

Zincke

. Surgical treatment of renal cancer with vena cava extension. BJU Int 1987;59(5):390-395.

11.

Ciancio

Vaidya

Savoie

, et al. Management of renal cell carcinoma with level III thrombus in the inferior vena cava. J Urol 2002;168(4 Pt 1):1374-1377.

12.

Ciancio

Vaidya

Soloway

. Early ligation of the renal artery using the posterior approach: A basic surgical concept reinforced during resection of large hypervascular renal cell carcinoma with or without inferior vena cava thrombus. BJU Int 2003;92:488-489.

13.

Serena

Gonzalez

Gaynor

, et al. Pulmonary tumor embolization as early manifestation in patients with renal cell carcinoma and tumor thrombus: Perioperative management and outcomes. J Card Surg. 2019;34:1018-1023.

14.

Caso

Seigne

Back

, et al. Circumferential resection of the inferior vena cava for primary and recurrent malignant tumors. J Urol. 2009;182:887-893.

15.

Ayyathurai

Garcia-Roig

Gorin

, et al. Bland thrombus association with tumour thrombus in renal cell carcinoma: Analysis of surgical significance and role of inferior vena caval interruption. BJU Int. 2012;110:E449-E455.

16.

Sarkar

Eilber

Gelabert

, et al. Prosthetic replacement of the inferior vena cava for malignancy. J Vasc Surg. 1998;28:75-81;discussion 82-3.

17.

Shirodkar

Ciancio

Soloway

. Vascular stapling of the inferior vena cava: Further refinement of techniques for the excision of extensive renal cell carcinoma with unresectable vena caval involvement. Urology 2009;4:8446-8850.

18.

Ciancio

Soloway

. Resection of the abdominal inferior vena cava for complicated renal cell carcinoma with tumor thrombus. Br J Urol Int 2005;96:815-818.

19.

Ciancio

González

. Tumor thrombus into the inferior vena cava after resection of renal cell carcinoma: Recurrence or tumor thrombus left behind? Urology. 2021;148:e17-e22.