Abstract
Background:
Level II–III inferior vena cava (IVC) tumor thrombectomy for renal cell carcinoma is among the most challenging urologic oncologic surgeries. In 2015, we reported the initial series of robot-assisted level III caval thrombectomy.
Objective:
To describe our University of Southern California technique in a step-by-step fashion for robot-assisted IVC level II–III tumor thrombectomy.
Design, setting, and participants:
Twenty-five selected patients with renal neoplasm and level II–III IVC tumor thrombus underwent robot-assisted surgery with a minimum 1-yr follow-up (July 2011 to March 2015).
Surgical procedure:
Our standardized anatomic-based “IVC-first, kidney-last” technique for robot-assisted IVC thrombectomy focuses on minimizing the chances of an intraoperative tumor thromboembolism and major hemorrhage.
Outcome measurements and statistical analysis:
Baseline demographics, pathology data, 90-d and 1-yr complications, and oncologic outcomes at last follow-up were assessed.
Results and limitations:
Robot-assisted IVC thrombectomy was successful in 24 patients (96%) (level III: n = 11; level II: n = 13); one patient was electively converted to open surgery for failure to progress. Median data included operative time of 4.5 h, estimated blood loss was 240 ml, hospital stay 4 d; five patients (21%) received intraoperative blood transfusion. All surgical margins were negative. Complications occurred in four patients (17%): two were Clavien 2, one was Clavien 3a, and one was Clavien 3b. All patients were alive at a 16-mo median follow-up (range: 12–39 mo).
Conclusions:
Robotic IVC tumor thrombectomy is feasible for level II–III thrombi. To maximize intraoperative safety and chances of success, a thorough understanding of applied anatomy and altered vascular collateral flow channels, careful patient selection, meticulous cross-sectional imaging, and a highly experienced robotic team are essential.
Patient summary:
We present the detailed operative steps of a new minimally invasive robot-assisted surgical approach to treat patients with advanced kidney cancer. This type of surgery can be performed safely with low blood loss and excellent outcomes. Even patients with advanced kidney cancer could now benefit from robotic surgery with a quicker recovery.
Keywords: Robotics, Vena cava, inferior, Thrombectomy, Kidney cancer
1. Introduction
Surgical management of patients with level II–III inferior vena cava (IVC) tumor thrombus arising from a renal tumor requires IVC thrombectomy, radical nephrectomy (RN), and ipsilateral retroperitoneal lymphadenectomy (RPLND). This complex major open surgical operation requires a large muscle-cutting abdominal or thoracoabdominal incision to achieve the necessary surgical access for vascular control and thrombectomy. In patents without metastatic disease, complete surgical excision is the first-line treatment and provides 5-yr cancer-specific survival of up to 65% [1], a 38% complication rate, and an operative mortality rate of 4–10% [2].
Minimally invasive IVC tumor thrombectomy is a relatively recent advancement. Building on early developmental work in the laboratory [3,4], the initial experience for level 0 (renal vein) and level I–II thrombi were reported in 2003 and 2011, respectively [5,6]. Robot-assisted surgery for level III caval thrombi was first reported in 2015 [1] and 2016 [7], and laparoscopic surgery for level IV caval thrombi in 2015 [8]. Spurred by these initial publications, additional centers have recently reported early experiences attesting to the increasing interest within the field for robot-assisted caval thrombectomy surgery [9-11]. Although the literature just cited is indicative of progress, we believe that for the robotic approach to duplicate open surgery reliably and thus allow more teams to embark safely on robot-assisted caval thrombectomy surgery, a description of a uniform and reproducible technique is of value.
We carefully developed a step-by-step standardized anatomic-based robotic approach for robot-assisted IVC thrombectomy. This approach is primarily targeted towards minimizing the chances of intraoperative tumor thromboembolism and major hemorrhage, the two major complications of IVC thrombectomy surgery. This report describes our University of Southern California technique in a step-by-step fashion.
2. Patients and methods
2.1. Study population
A renal database approved by an institutional review board prospectively accrued data for all level II and III IVC thrombectomy cases. A total of 25 patients have completed a minimum follow-up of 1 yr and form the basis for this two-center series. All cases were performed by a single combined robotic team from July 2013 to March 2015.
Exclusion criteria for this study comprised Mayo level 0–I thrombi (extending <2 cm into the IVC), level IV thrombi (supradiaphragmatic), and widespread metastatic disease (more than one metastatic site). Also, to maintain consistency in the reported technique, we excluded four patients in whom intra- or retro-hepatic IVC control was obtained via an intracaval Fogarty balloon [12]. All patients underwent surgery with curative or cytoreductive intent.
2.2. Preoperative assessment and surgical indication
All patients included in the study presented with a renal mass and a level II or III IVC tumor thrombus and had good performance status (Eastern Cooperative Oncology Group performance status 0 or 1). Five patients (20%) had preexisting small-volume metastasis.
Patients underwent a standard preoperative work-up including cross-sectional abdominal imaging (computed tomography and/or magnetic resonance imaging). Angioembolization of the tumor-bearing kidney was performed in a majority of cases (80%).
2.3. Surgical technique
2.3.1. Robotic instrumentation
The four-arm Si or Xi da Vinci Surgical System (Intuitive Surgical Inc, Sunnyvale, CA, USA) with a six- to seven-port approach was used including two assistant ports. Bariatric-length robotic ports help minimize external robotic arm clashing, and standard robotic instruments were used. A double-fenestrated grasper is used to pass posterior to the vena cava to establish Rummel tourniquet control of the retrohepatic/intrahepatic IVC.
2.3.2. Patient positioning, port placement, and robot docking
The patient is secured in a 75° lateral decubitus position with the table fully flexed. For both right- or left-sided tumors, the patient is initially secured right side up to facilitate IVC exposure and control. For right-sided tumors, the procedure proceeds directly to a right RN following IVC thrombectomy; for left-sided tumors, the patient is repositioned left side up and the robot’s redocked following IVC thrombectomy (Fig. 1a-1d).
Fig. 1 –
Patient positioning and port placement. Veress needle pneumoperitoneum is achieved, and the 12-mm camera port is placed at the level of the 12th rib in a somewhat more medial location than regular renal robotic surgery, where this port is closer to the right lateral rectus border. The rest of the bariatric robotic ports are inserted, the most caudal located cephalad to the pubic symphysis and slightly lateral to the medial umbilical ligament. One robotic port is placed three fingerbreadths cephalad and medial to the anterosuperior iliac spine; of note, an equilateral triangle configuration is the goal of these three ports (including the camera port). The uppermost bariatric robotic port is placed one fingerbreadth from the costal margin, 8–10 cm cephalad to the camera port. A 5-mm port is placed below the xiphisternum for liver retraction; a 12-mm assistant port is placed medially between the camera and uppermost robotic port; and a 15-mm assistant port is placed distal to the umbilicus, closer to the midline. The robot is docked over the patient’s shoulder. (a) Schematic demonstrating port placement for vena caval control (laterality nonspecific) and right-sided caval thrombectomy; (b) operative photograph demonstrating port placement for vena caval control (laterality nonspecific) and right-sided caval thrombectomy; (c) schematic demonstrating port placement for left radical nephrectomy following caval thrombectomy; (d) operative photograph demonstrating port placement for left radical nephrectomy following vena caval thrombectomy.
As = assistant port; Cam = camera; Liv = liver.
2.3.3. Vena cava control (for right- or left-sided tumors)
The primary concept we developed in this regard is the “IVC-first, kidney-last” approach in a minimal IVC touch manner, to minimize chances of tumor embolism and major hemorrhage. The right colon and duodenum are reflected medially to expose the vena cava. Retroperitoneal dissection begins infrarenally in the midline to expose the interaortocaval region (Fig. 2a-2b). The laparoscopic fan retractor facilitates the medial retraction of bowel for increased exposure.
Fig. 2 –
Vena caval control. (a) Dissection occurs to expose the vena cava; (b) the interaortocaval region is exposed; (c) the infrarenal inferior vena cava (IVC) is dissected and lumbar veins are controlled; (d) the gonadal vein is controlled; (e) the infrarenal IVC is encircled with a double-loop tourniquet (Rummel) using a vessel loop; (f) the left renal vein is encircled with a double-loop tourniquet (Rummel) using a vessel loop; (g) the suprarenal IVC is dissected intrahepatically and short hepatic veins are controlled with Hem-o-lok clips; (h) the right adrenal vein is controlled with Hem-o-lok clips; (i) the IVC proximal to the thrombus and in the high intrahepatic location is encircled with a double-loop tourniquet (Rummel) using a vessel loop. All tourniquets are secured in place with a Hem-o-lok clip.
Dissection of the infrarenal IVC involves control of all relevant lumbar veins (Fig. 2c) and the gonadal vein (Fig. 2d), which are taken with Hem-o-lok clips (Teleflex, Wayne, PA, USA). The infrarenal IVC is encircled with a double-loop tourniquet (Rummel) using a vessel loop (part no. KDL311456694, Devon Surgical Vessel Loops [Covidien, Dublin, Ireland]; dimensions: 12.5 × 4.9 × 5.8 in; volume: 0.206 ft3) passed through a half-inch piece of 20F red rubber urethral catheter and secured in place with a Hem-o-lok clip (Fig. 2e). Dissection is carried cephalad within the interaortocaval region. The left renal vein is mobilized and encircled with a Rummel tourniquet (Fig. 2f).
For proximal IVC control, careful interaortocaval dissection is performed towards the liver. For level III thrombi, the relevant number of short hepatic veins is controlled with robotic Hem-o-lok clips and/or suture-ligation (Fig. 2g). Releasing the short hepatic veins is essential to retract the caudate lobe; this maneuver exposes an additional 3–4 cm of the IVC allowing high intrahepatic access to the retrohepatic IVC. The right main adrenal vein is controlled with Hem-o-lok clips (Fig. 2h), and the right lateral border of the suprarenal IVC is dissected. Retrocaval dissection of the intrahepatic IVC is performed. A double-fenestrated grasper is used to encircle the IVC with a Rummel tourniquet in this high retrohepatic location (Fig. 2i). The right renal hilum is dissected and the right renal vein is exposed.
2.3.4. Right-sided caval thrombectomy
All Rummel tourniquets are reconfirmed to be in the appropriate position, with a sufficient margin around the thrombus. This is achieved with visual confirmation (appropriate narrowing of the cava on cinching the Rummel tourniquet) and/or a drop-in ultrasound probe.
The right renal artery is dissected and clipped in the interaortocaval region (Fig. 3a). Anesthesia is alerted that caval blood flow will be temporarily halted. The initial maneuver is to cinch the distal (infrarenal) IVC tourniquet. Once assured that the patient is able to tolerate caval cross-clamping, the left renal vein and proximal IVC Rummel tourniquets are cinched sequentially, thus excluding the thrombus-bearing caval segment. The thrombus-bearing right renal vein is transected with an Endo GIA stapler (vascular load; Covidien) (Fig. 3b and 3c). The excluded caval segment is now rotated and circumferentially inspected 360° to reconfirm visually that all feeding lumbar veins have been secured. An appropriately situated cavotomy is created toward the right edge of the IVC, adjacent to the right renal vein ostium (Fig. 3d and 3e); the cavotomy should be well planned so that subsequent caval reconstruction does not overly narrow its lumen.
Fig. 3 –
Right-sided caval thrombectomy. (a) The right renal artery is clipped and transected; (b, c) the thrombus-bearing right renal vein is transected with an Endo GIA stapler; (d–f) a cavotomy is performed and the thrombus is removed; (g) the thrombus is dissected free without local spillage; (h) a 5-0 Gore-Tex suture is used for inferior vena cava reconstruction; (i) the tourniquets are released and caval flow is restored.
The thrombus is carefully dissected free from the IVC lumen without local spillage (Fig. 3f and 3g). The right renal vein ostium, along with its staple line, and any infiltrated or densely adherent IVC wall are excised en bloc with the thombus; the tumor thrombus specimen is immediately placed in a 10-mm Endo Catch bag (Covidien), precluding local seeding. The IVC lumen is copiously irrigated and flushed with heparinized water. Caval reconstruction is performed with a 5-0 Gore-Tex (W. L. Gore & Associates, Newark, DE, USA) suture with a single-layer running stitch (Fig. 3h). Tourniquets are released sequentially (left renal vein, suprarenal IVC, infrarenal IVC) and caval flow restored (Fig. 3i). Right RN and ipsilateral RPLND are then completed in the standard fashion.
2.3.5. Left-sided caval thrombectomy
The following maneuvers are different for left-sided tumors. Temporary cessation of blood flow to the right kidney is necessary to properly exclude the caval segment for controlled thrombectomy. The right renal artery and vein are controlled with individual bulldog clamps, prior to cinching the infra- and suprarenal IVC tourniquets (Fig. 4a). The thrombus-bearing left renal vein is transected with an Endo GIA stapler (left-sided tumors routinely undergo preoperative angioinfarction) (Fig. 4b and 4c). After caval thrombectomy and reconstruction, caval flow is restored and the right kidney revascularized. The patient is repositioned left side up for left RN (Fig. 4d) and ipsilateral RPLND.
Fig. 4 –
Left-sided caval thrombectomy. (a) The infrarenal inferior vena cava (IVC), suprarenal IVC, left and right renal veins are encircled with a double-loop tourniquet and secured with a Hem-o-lok clip. Then the right renal artery and right renal vein are controlled using individual bull-dog clamps. (Note: In this operative picture, the patient had a solitary kidney. The previous kidney was emergently removed during a previous motor vehicle accident). (b, c) The thrombus-bearing left renal veins is transected with an Endo GIA stapler after have already undergone preoperative angioembolization. (d) The left renal artery is ligated following patient repositioning.
2.4. Postoperative care and follow-up
Routine postoperative care, deep vein thrombosis prophylaxis, and early ambulation are performed. Postoperatively, subcutaneous heparin is prescribed at a dose of 5000 U every 8 hours. Upon discharge, prophylactic anticoagulation with 40 mg enoxaparin sodium daily is continued for 1 mo. Follow-up includes a routine postoperative clinic visit within 1–2 weeks of discharge that includes wound care check, vital sign assessment, complication and functional assessment, and medical oncology consultation as indicated. Follow-up then continues at 1 month, 3 months, and then annually. Cross-sectional imaging, chest x-ray, and laboratory investigations are done at 3 and 6 months and per surgeon discretion thereafter.
2.5. Data collection and statistical methods
Data were prospectively accrued in our renal database approved by a institutional review board. Demographic data included age, gender, body mass index, and American Society of Anesthesiologists score. Preoperative tumor characteristics included renal tumor size and side, thrombus length, and thrombus level (Mayo classification [13]). Preoperative embolization status, any preexisting metastasis, and neoadjuvant treatment status are noted. Operative and postoperative data were collected as per our database protocol. Median, range, and statistical significance were used to report continuous and categorical data.
3. Results
Table 1 presents the demographic and perioperative data. Of the cases, 24 (96%) were successfully completed robotically without intraoperative complications. One patient (4%) was electively converted to open surgery within 30–45 minutes of starting because of failure to progress due to insurmountable bowel loops. Because the entire IVC surgery in this case was performed open surgically for >8 h, this case was censured from postoperative analysis.
Table 1 –
Demographic and perioperative data
Variable | Results |
---|---|
Patients, n | 24 |
Age, yr, median (range) | 64 (36–88) |
Male, n (%) | 21 (87.5) |
BMI, kg/m2, median (range) | 28 (22–41.9) |
ASA score, median (range) | 3 (2–4) |
Charlson Comorbidity Index, median (range) | 2 (0–6) |
Renal tumor | |
CT size, cm, median (range) | 8.5 (5.3–19.5) |
Left side, n (%) | 7 (29.2) |
IVC thrombus length, cm, median (range) | 4 (2–7) |
Mayo IVC thrombus classification level, n (%) | |
II | 13 (54.2) |
III | 11 (45.8) |
Preexisting metastasis, n (%) | 5 (20.8) |
Neoadjuvant therapy, n (%) | 2 (8.3) * |
Preoperative embolization, n (%) | 20 (80.3) |
Operative time, h, median (range) | 4.5 (3–8) |
Thrombectomy time, h | 2.6 (1.3–5) |
IVC clamp time, h | 0.4 (0.3–1.7) |
Nephrectomy time, h | 1 (0.3–3) |
RPLND time, h | 0.5 (0.3–1.5) |
Hepatic veins taken, median (range) | 1.5 (0–5) |
Proximal caval control | |
Suprarenal IVC | |
Intrahepatic, n (%) | 9 (37.5) |
EBL, ml, median (range) | 240 (100–7000) |
Patients receiving intraoperative transfusions, n (%) | 5 (20.8) |
Patients receiving intraoperative bovine pericardial patch, n (%) | 1 (4.2) |
Lymph nodes removed, median (range) | 7 (1–22) |
Lymph nodes positive, median (range) | 0 (0–22) |
Intraoperative complications, n | 0 |
Positive surgical margins, n | 0 |
Length of hospital stay, d, median (range) | 4 (1–22) |
ASA = American Society of Anesthesiologists; BMI = body mass index; CT = computed tomography; EBL = estimated blood loss; IVC = inferior vena cava; RPLND = retroperitoneal lymph node dissection.
One patient underwent tyrosine kinase inhibitor treatment for 3 mo; one patient underwent partial nephrectomy.
Of the cases, 11 (46%) were Mayo level III thrombi and 13 were Mayo level II (54%). Primary renal tumors were right sided (n = 16) or left sided (n = 7), with median size 8.5 cm (range: 5.3–19.5 cm) on radiologic imaging. Median thrombus length was 4 cm (range: 2–7 cm). Five patients (21%) had low-volume preexisting metastasis at the time of surgery: pulmonary (n = 1), paracaval 2.2-cm node (n = 1), lumbar vertebra (n = 1), and adrenal gland with two lymph nodes (n = 1). Two patients (8.3%) received neoadjuvant therapy, with one a prior partial nephrectomy. Twenty patients (80%) underwent preoperative renal artery embolization. The median number of hepatic veins taken was 1.5 (range: 0–5), median operating time was 4.5 hours (range: 3–8 hours), and estimated blood loss was 240 ml (range: 100–7000 ml). Table 1 summarizes the operative time breakdown of the procedure steps. Five patients (21%) required blood transfusion(s). Median hospital stay was 4 days (range: 1–22 days).
Four patients (16.7%) had a complication within 1 year postoperatively. These included deep vein thrombosis (n = 1) or pulmonary embolus (n = 1), both treated with anticoagulation (Clavien 2), chylous ascites (n = 1) treated with paracentesis (Clavien 3a), and subphrenic abscess (n = 1) treated with percutaneous drainage (Clavien 3b). Table 2 presents the pathology and follow-up data. Final pathologic stage was T3a (n = 5), T3b (n = 14), T3c (n = 2), and T4a (n = 3). Three patients (12.5%) were found to have positive lymph nodes. Median follow-up for the cohort was 16 months (range: 12–39 months). All patients were alive at last follow-up. Eleven patients (46%) developed new-onset metastatic disease; at last follow-up, 10 patients (42%) had received adjuvant therapy.
Table 2–
Pathology and follow-up data
Variable | Results |
---|---|
Patients, n | 24 |
Histology, n (%) | |
Renal cell carcinoma | 23 (95.8) |
Papillary type II | 1 (4.2) |
Tumor grade, n (%) | |
2 | 7 (29.2) |
3 | 11 (45.8) |
4 | 6 (25.0) |
Stage, n (%) | |
T3a | 5 (20.9) |
T3b | 14 (58.3) |
T3c | 2 (8.3) |
T4a | 3 (12.5) |
Positive lymph nodes, n (%) | 3 (12.5) |
No. of patients with 1-yr Clavien complications, n (%) | 4 (16.7) |
2 | 2 (8.3) * |
3a | 1 (4.2) † |
3b | 1 (4.2) ‡ |
Cancer status | |
Disease free | 13 (54.2) |
Recurrence | 11 (45.8) |
Patient status, n (%) | |
Alive | 24 (100) |
Dead | 0 |
Adjuvant therapy, n (%) | 10 (41.7) |
Follow-up, mo, median (range) | 16 (12–39) |
Pulmonary embolism or deep vein thrombosis (treated with nadroparin; occurred within 90 d after surgery).
Chylous ascites.
Percutaneous drainage of subphrenic abscess.
4. Discussion
Level III IVC tumor thrombectomy is one of the most challenging open surgical urologic oncologic procedures, with major complication rates of up to 38% and perioperative mortality rates of 4–10% [8]. Given the potential for these major intraoperative complications, it is essential that the perioperative safety, oncologic efficacy, and technical reproducibility of the robotic approach be carefully documented before integration and eventual adoption at other centers of robotic expertise. At our institution, a backup open surgical team is on standby in the event of an intraoperative complication. We also preprepare so-called rescue stitches [14], made of a 6-inch long suture of 2–0 Vicryl (Ethicon, Somerville, NJ, USA) on a CT-1 needle with a Hem-o-lok tied to the end of the stitch, which can be used expeditiously to control a bleeding vessel. Finally, a competent bedside assistant, facile in laparoscopic suction irrigation, also adds further expertise in securing vascular control. Most important, careful and meticulous vascular dissection with precise control of all feeding blood vessels is paramount for successful outcomes.
To guard against tumor embolism, a minimal IVC touch strategy is adopted. To the extent possible, tissues are dissected away from the IVC, rather than the IVC away from the tissues. Immediately after securing the thrombus-bearing IVC segment by tightening the Rummel tourniquets (thus eliminating any chance of embolization), we staple-transect the thrombus-bearing renal vein. This key step delivers three major advantages: (1) The thrombus-bearing caval segment can now be easily rotated and inspected 360° to ensure all feeding lumbar veins are clipped; (2) back bleeding from the tumorous kidney into the IVC is eliminated; and (3) the excised thrombus and stapled renal vein ostium are immediately placed in the Endo Catch bag, precluding local spillage.
Essential aspects of left-sided thrombectomy include starting with the patient in the right-side-up position to address the caval thrombus first, transient vascular control of the right renal artery and vein while preserving the right adrenal gland, followed by thrombectomy, caval reconstruction, and right renal revascularization. We performed angioembolization 24 hours preoperatively in 80% of our patients, especially in those with left-sided or larger tumors. Preoperative renal embolization has been controversial prior to open surgical IVC thrombectomy, correlated with increased transfusions, operative time, and postoperative complications, leading to longer intensive care unit stay and higher perioperative mortality [15]. However, we did not notice any such downside; rather, it is our impression that angioinfarction decompressed the venous collaterals, decreasing blood loss and enhancing robotic efficacy. Due to our limited sample size, we are unable to compare outcomes between those who did and did not undergo angioembolization.
Our study has limitations. To our knowledge, reported here is the largest number of robot-assisted level III IVC thrombectomy cases (n = 11) in the literature; nevertheless it still is a relatively small patient cohort. Also, our median follow-up of 16 mo is short. We are therefore unable to report on the long-term oncologic efficacy of robotic surgery; however, to date the oncologic outcomes have been sanguine. Given the lack of a comparator open surgical cohort, we are unable to comment definitively on the relative merits and demerits of a matched comparison with open surgery. In this regard, we are currently in the midst of a retrospective comparison of open and robot-assisted level II–III IVC thrombectomy.
5. Conclusions
Our report demonstrates the University of Southern California technique and clinical outcomes data for robotic level II–III inferior vena cava tumor thrombectomy. Our encouraging early experience provides confidence that the requisite vascular, reconstructive, and oncologic surgical principles and technical nuances can be reliably and reproducibly addressed robotically with good clinical outcomes.
Supplementary Material
Footnotes
Conflicts of interest
Mihir M. Desai declares conflict of interest for Hansen Medical; Auris Robotics; Procept Biorobotics; Baxter.
Inderbir S. Gill declares conflict of interest for EDAP, Mimic, Hansen Medical.
Financial disclosures: Inderbir Singh Gill certifies that all conflicts of interest, including specific financial interests and relationships and affiliations relevant to the subject matter or materials discussed in the manuscript (eg, employment/ affiliation, grants or funding, consultancies, honoraria, stock ownership or options, expert testimony, royalties, or patents filed, received, or pending), are the following: None.
Appendix A. Supplementary data
The Surgery in Motion video accompanying this article can be found in the online version at http://dx.doi.org/10.1016/j.eururo.2016.08.066 and via www.europeanurology.com.
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