Minimally Invasive Surgical Techniques for Renal Cell Carcinoma with Intravenous Tumor Thrombus: A Systematic Review of Laparoscopic and Robotic-Assisted Approaches
Abstract
:1. Introduction
2. Methods
2.1. Search Strategy
2.2. Inclusion Criteria
2.3. Systematic Review Process
2.4. Classification of IVTT
- Level 0: tumor thrombus confined to the renal vein without extension into the inferior vena cava (IVC);
- Level I: extension into the IVC less than 2 cm above the renal vein;
- Level II: extension more than 2 cm above the renal vein but below the hepatic veins;
- Level III: extension to the intrahepatic IVC, up to but not beyond the diaphragm;
- Level IV: extension above the diaphragm or into the right atrium.
2.5. Statistical Analysis
3. Results
3.1. Characteristics of Included Studies
3.2. Comparison of RA and LAP Across Different Levels of IVTT
3.2.1. Operative Time
3.2.2. Estimated Blood Loss
3.2.3. Transfusion Rate
3.2.4. Conversion Rate
3.2.5. Length of Stay
3.2.6. Minor Perioperative Complications Rate (Clavien-Dindo Grade I and II)
3.2.7. Major Perioperative Complications Rate (Clavien-Dindo Grade ≥ III)
3.2.8. Cancer Specific Mortality
3.2.9. Distant Metastasis and Local Recurrence
3.3. Techniques for Laparoscopic Management
3.3.1. Experience with Laparoscopy for Level 0–II Thrombi
3.3.2. Experience with Laparoscopy for Level III–IV Thrombi
3.3.3. Experience with Robot-Assisted Laparoscopy for Level 0–II Thrombi
3.3.4. Experience with Robot-Assisted Laparoscopy for Level III–IV Thrombi
3.4. LAP: Does Hand-Assisted Value Still Exist?
4. Discussion
4.1. Perioperative Outcomes
4.2. Technical Advancements
4.3. Imaging and Expertise
4.4. Patient Selection and Expanding Eligibility Criteria
4.5. Cost Effectiveness
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Conflicts of Interest
References
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Author/Year | Study Type | Approach | Number of Patients | Age (Median or Mean, yo) | Tumor Size (Median or Mean, cm) | RCC Histology | IVTT Level | Pathological Stage |
---|---|---|---|---|---|---|---|---|
Desai, 2003 [12] | case series | LAP | 16 | 57.8 | 3.3 ± 6.5 (3–4) | ccRCC, pRCC, sRCC, gRCC | 0: 16; invasive: 2 | T3aN0M0:13 T4N0M0:3 |
Kapoor, 2006 [13] | case series | LAP/HLAP | 12 | 62.3 | 8 (IQR = 2) | 0:12 | ||
Hammond, 2007 [14] | case series | LAP | 6 | 55.8 | 9.5 (7.5–11.5) | ccRCC, Other RCC | 0:06 | T3aNxM0:4 T3aNxM0:2 |
Steinnerd, 2007 [15] | case series | LAP | 5 | 59.8 | 5.5 (4.6–6.0) | ccRCC, pRCC | 0: 5; invasive: 1 | T3aN0M0:5 |
Martin, 2008 [16] | case series | LAP/HLAP | 14 | 65 | 7.3 ± 2.2 | ccRCC | 0: 10; I: 3; II: 1 | T3bNx |
Guzzo, 2009 [17] | case series | LAP | 37 | 65 | 6 (3.5–12) | ccRCC, pRCC, sRCC | 0:37 | T3aN0M0:32 T3aN1 + T3aNxM1:5 |
Liss, 2013 [18] | case series | LAP | 26 | 60.8 | 7.9 ± 2.2 | ccRCC, Other RCC | 0:26 | T3aNxM0 |
Bansal, 2014 [19] | case series | LAP | 41 | 64.4 | 9.3 (4–22) | ccRCC, pRCC, Other RCC | 0: 39; I: 3 | T3aNxM0:34 T3aNxM1:5 T3bNxM1:2 |
Wang(left), 2014 [20] | case series | LAP | 10 | 64 | 6.3 (5.0–8.5) | ccRCC(9), chRCC(1) | 0:10 | T3aN0M0:8 T3aN0M1:2 |
Xu, 2014 [21] | cohort study | LAP | 17 | 50.1 | 7.9 ± 2.6 | 0: 5; I: 12 | T3aNxM0:5 T3bNxM0:12 | |
Castillo, 2014 [22] | case series | LAP/HLAP | 11 | 66.8 | 10.5 ± 2.5 | ccRCC(10), ccRCC + sRCC(1) | 0:11 | T3aN0M0 |
Shao, 2015 [23] | case series | LAP | 11 | 53.5 | 7.8 (6.5–9.3) | ccRCC(10), pRCC(1) | II: 6; IV: 5 | T3bN0M0:9 T3bN1M0:2 |
Wang M, 2016 [24] | case series | LAP | 5 | 57 | 6.9 (3.5–9) | ccRCC | II: 5 | T3bN0M0 |
Crisan, 2018 [25] | case series | LAP | 9 | 61 | 7.6 (5.5–10.5) | ccRCC(8), sRCC(1) | 0: 3; I: 3; II: 3 | T3bN0M0:3 T3bN1M0:6 |
Cinar, 2019 [26] | case series | LAP | 13 | 61.6 | 9.5 × 7.3 (5–14) | ccRCC(11), pRCC(2) | 0/I:11; II:2; invasive: 4 | T3bN0M0:6 T3bN1M0:2 T3bN0M1:5 |
Tohi, 2019 [27] | case series | LAP/HLAP | 5 | 63 | 7.3 (3.5–11) | ccRCC | I: 1; II: 3; III:1 | T3aN0M0:1 T3bN0M0:1 T3cN0M0:3 |
Tian, 2020 [28] | case series | LAP | 78 | 59 | 8.3 (IQR: 6.9–9.5) | ccRCC(70), pRCC(7), chRCC(1) | 0: 28; I: 27; II: 23 | T3aNxM0 + T3aNxM1:28 T3bN0M0 + T3bNxM1:50 |
Zhao, 2020 [29] | cohort study | LAP | 58 | 61.2 | 7.9 ± 2.3 | ccRCC(52), Other RCC(6) | 0: 22; I:23; II: 10; III: 3 | T3a:22 T3b:33 T3c:3 |
Liu, 2021 [30] | cohort study | LAP | 17 | 52.2 | 8.1 ± 3.4 (3.5–11) | ccRCC(12), pRCC(1), chRCC(1), other(3) | II: 13; III:4 | T3bNxMx = 13; T3cNxMx = 4 |
Liu, 2021 [31] | cohort study | LAP | 41 | 60.2 | 7.98 ± 2.16 | ccRCC(37), other(4) | I: 26; II: 15 | T3aN0M0 + T3aN1M0:32 T3bN0M1 + T3bN1M1:9 |
Ma, 2021 [32] | case series | LAP | 11 | 57 | 7.20 (IQR: 6.00–10.50) | ccRCC | I: 6; II: 5 | T3bN0M0 = 9; T3bN0M1 = 2 |
Chen, 2023 [33] | cohort study | LAP | 57 | 61 | 8.0 (M; IQR = 6.1–9.9) | ccRCC(48), pRCC(4), chRCC(1), other(4) | I: 25; II: 29; III:3 | T3bN0Mx = 56; T3bNxM0 = 45 |
Scherñuk, 2023 [34] | cohort study | LAP | 15 | 61.9 | 9.00 (M; IQR = 6.50–11.90) | ccRCC(13), pRCC(1), other(1) | I: 7; II: 27; III: 6 | T3bNxMx = 15; T3bN1Mx = 3; T3bNxM1 = 4 |
Zhang, 2023 [35] | cohort study | LAP | 88 | 60 | 6.4 (M; IQR = 5.8–9.8) | ccRCC(78), pRCC(9), chRCC(1), other(6) | I: 20; II: 61; III: 7; invasive: 21 | T3a = 15; T3b = 39; T3c = 36; T4 = 4; N1 = 54; M1 = 21 |
Varkarakis, 2004 [36] | case series | HLAP | 4 | 56 | 9 (6–13) | II: 4 | T3bNx | |
Henderson, 2008 [37] | case series | HLAP | 13 | 68.8 | 8.1 (4.5–12) | 0:13 | T3aN0M0:12 T3aN1M0:1 | |
Hoang, 2010 [38] | case series | HLAP | 7 | 66 | 9.1 (5.7–12.8) | II: 6; III: 1 | T3bNxM0:5 T3bNxM1:1 T3cNxM0:1 |
Author/Year | Study Type | approach | Number of Patients | Age (Median or Mean, yo) | Tumor Size (Median or Mean, cm) | RCC Histology | IVTT Level | Pathological Stage |
---|---|---|---|---|---|---|---|---|
Ronney Abaza, 2010 [39] | case series | ROB | 5 | 64 | 10.4 (7.8–15.5) | I: 2, II: 3, | T3bN1M0:4 T3bN1M1:1 | |
Gill, 2015 [40] | case series | ROB | 16 | 66.2 | 9.7 (6.5–19.5) | II: 7, III: 9, invasive: 2 | T3bN0M0: 28 T3bN1M0: 4 T3bN0M1: 4 | |
Wang, 2015 [41] | case series | ROB | 17 | 61 | 5.8 (4–10) | I: 4, II: 3 | T3bN0M0:16 T3bN1M0:2 T3bN0M1:1 | |
Abaza, 2016 [42] | case series | ROB | 32 | 63 | 9.6 (5.4–20) | I/II: 30, III: 2 | ||
Kundavaram, 2016 [43] | case series | ROB | 5 | 59.3 | 8.0 (5.5–9.5) | ccRCC(3), pRCC(1)Collecting duct CA(1) | II: 1, III: 3, invasive: 1 | T3cN1Mx:1 T3cN0Mx:2 T4N2M0 T3cN0Mx |
Chopra, 2016 [44] | case series | ROB | 24 | 64 | 8.5 (5.3–19.5) | ccRCC(23), pRCC(1) | II: 13, IV: 1 | T3b:19 T3c:3 T4:3 TxN1Mx:3 TxNxM1:5 |
Davila, 2016 [45] | case series | ROB | 10 | 55.6 | 1.9–11 | |||
Gu, 2017 [46] | cohort study | ROB | 31 | 55.7 | 7.3 (SD = 3.0) | ccRCC(26), pRCC(3), Other(2) | I: 10, II: 21 | T3bN0Mx:29 T3bN1Mx:2 |
Wang, 2017 [47] | case series | ROB | 22 | 58.5 | 7.8 (2.5–15.0) | ccRCC(16), pRCC(2), Other(4) | II: 20, III: 2, invasive: 3 | T3bN0M0:17 T3bN0M1:4 T3cN0M1:1 |
Ke, 2018 [48] | case series | ROB | 6 | 57 | 7.2 (3.2–8.4) | ccRCC(4), pRCC(1), Other(1) | 0: 3, I: 1, II: 2, | T3aN0M0:3 T3bN0M0:1 T3bN1M0:1 T3bN0M1:1 |
Fan, 2019 [49] | case series | ROB | 15 | 62 | 8.1(3–10) | ccRCC(4), pRCC(1), Collecting duct CA(1) | 0:15 | T3aN0M0:5 T3aN1Mx:1 T4NxM0:2 T3aNxM1:2 T3aN0M0:4 T3aN1M0:1 |
Rose, 2019 [50] | cohort study | ROB | 24 | ccRCC(20), Other(4) | I: 2, II: 22 | T3bNxM0:19 T3bNxM1:5 | ||
Du, 2020 [51] | case series | ROB | 7 | 58 | 9.2 (6.0–15.0) | ccRCC(5), pRCC(2) | II: 5, III: 2, invasive: 5 | T3bN0M0:2 T3cN0M0:5 |
Kishore, 2020 [52] | case series | ROB | 13 | 56.5 | 9.25 | ccRCC(12), pRCC(1) | I: 5, II: 7, III: 1, | T3aN0M0:1 T3bN0M0:8 T3bN1M0:2 T3bN0M1:2 |
Shen, 2020 [53] | case series | ROB | 27 | 60.3 | III: 14, IV: 13 | T3bNxMx:4 T3cNxMx:7 T4NxMx:1 T3bNxMx:5 T3cNxMx:8 T4NxMx:2 | ||
Shen, 2020 [54] | case series | ROB | 120 | 54.1 | 7.9 (SD = 3.1) | ccRCC(81), pRCC(14), Other(25) | I: 30, II: 74, III: 14, IV: 2 | T3b:93 T3c:23 T4:4 Nx:70 N0:35 N1:15 M0:107 M1:13 |
Shi, 2020 [55] | case series | ROB | 90 | 54 | 8.6 (2.5–19.0) | ccRCC(77), pRCC(13) | II: 90, invasive: 18 | T3b + T3c:14 T4:17 TxN1Mx:4 TxNxM1:6 T3b + T3c:59 T4:1 TxN1Mx:8 TxNxM1:6 |
Wang, 2020 [56] | case series | ROB | 13 | 57.5 | 8.2 (SD = 4.3) | ccRCC | III: 7, IV: 6 | T3bN0M0:4 T3bN1M0:1 T3cN0M0:7 T4N0M1:1 |
Ma, 2021 [57] | case series | ROB | 20 | 59 | 67 cm2 (IQR: 40–91 cm2) | ccRCC(9), other(11) | 0: 2, I: 3, II: 12, III: 3, invasive: 1 | T3aNxM0:2; T3bNxM0:13; T3cNxM0:3; T4NxM0: 2 |
Wu, 2021 [58] | cohort study | ROB | 35 | 58 | 6.9 (IQR:3.0–7.2) | ccRCC(28), other(7) | : 10, II: 25 | T3bN0M0 = 14; T3bN1M0 = 2 T3bN0M0 = 15; T3bN1M0 = 3; T3bN0M1 = 1 |
Morgan, 2022 [59] | case series | ROB | 45 | 64.9 | 4.3 (range = NA; SD = 1.3) | ccRCC(41); pRCC(2); other(2) | 0:45 | T3aN0M0 = 45 |
Zhao, 2022 [60] | cohort study | ROB | 18 | 55.3 | 8.9 (range = NA; SD = 2.9) | ccRCC(15); pRCC(1); other(2) | III: 10, IV: 8 | T3bNxMx = 10; T4NxMx = 1 or T3NxM1 = 1 T3cNxMx = 7 |
Zhang, 2023 [35] | case series | ROB | 30 | 60 | 7.3 (M; range = NA; IQR = 6.1–8.7) | ccRCC(23), pRCC(3), other(4) | II: 28, III: 2, invasive: 13 | T3bNxMx = 8; T3cNxMx = 7; T3N1Mx = 3; T3NxM1 = 4 T3bNxMx = 8; T3cNxMx = 7; T3N1Mx = 3; T3NxM1 = 7 |
Zhang, 2023 [61] | cohort study | ROB | 22 | 58 | 6.5 (M; range = NA; IQR = 5.8–9.6) | ccRCC(21), pRCC(1) | I: 5, II: 15, III: 2, invasive: 4 | T3a = 5; T3b = 10; T3c = 7; N1 = 13; M1 = 6 |
Category | Technique | Description |
---|---|---|
Laparoscopy for Level 0–II Thrombi | Hand-assisted Laparoscopic Surgery | First reported for right-sided RCC with level I IVTT using Satinsky clamps for en bloc thrombus removal |
Thrombus Milking Technique | Removal of intraluminal thrombi using an endoscopic stapler | |
Intraoperative Ultrasound | Utilized to define thrombus margins, addressing limited tactile feedback | |
Early Renal Artery Ligation | Facilitates thrombus retraction and control in both pure and hand-assisted techniques | |
DeBakey Graspers/Satinsky Clamps | Ensures thrombus-free renal vein transection | |
Laparoendoscopic Single-Site Surgery | Pioneered for selected patients | |
Early Renal Artery Ligation | Reduces tumor vascularity and thrombus retraction | |
GelPort Device | Enhances tactile feedback in complex cases | |
Pure Retroperitoneal Approach | Introduced for left-sided RCC, enabling early renal hilar control | |
Partial IVC Clamping | Used for incomplete thrombus milking, preserving over 50% of the IVC lumen | |
Bulldog Clamps/Modified Rummel Tourniquets | Provides precise IVC control and partial wall resection | |
Combined Retroperitoneal and Transperitoneal Approaches | Applied for complex cases | |
Suction Irrigation Cannulas | Used for thrombus milking | |
Modified Vein Clamping Technique | Developed for Level I-II thrombi | |
Delayed Occlusion of the Proximal Inferior Vena Cava (DOPI) | Utilizes pneumoperitoneum pressure to delay IVC clamping | |
Pure Retroperitoneal Laparoscopic Peritoneum Incision Technique (PREP-IT) | Improves IVC access in right-sided RCC | |
Laparoscopy for Level III-IV Thrombi | Hand-assisted Laparoscopic Nephrectomy and Thrombectomy | Pioneered for Level III thrombi using intraoperative ultrasonography and IVC clamping |
Thoracoscope-assisted Open Atriotomy | First reported for Level IV thrombi under cardiopulmonary bypass | |
Liver Rotation and Pringle Maneuver | Described for Level III thrombi | |
DOPI Technique | Applied to avoid immediate IVC clamping | |
PREP-IT Technique | Extended to Level III thrombi | |
Adjustable IVC and Hepatic Vein Control Technique | Developed for cases without hepatic vein involvement |
Category | Technique | Description |
---|---|---|
Robot-Assisted Laparoscopy for Level 0–II Thrombi | Robotic Radical Nephrectomy (RN) and IVC Thrombectomy (IVTTx). | First case series for right-sided RCC with Level I-II thrombi using modified Rummel tourniquet and percutaneous Satinsky clamp |
Minimal-Touch Technique | Emphasizes “midline-first, lateral-last” strategy for Level II thrombi to minimize peri-caval tissue manipulation | |
Side-Specific Techniques | Preoperative renal artery embolization for left-sided RCC; left renal vein clamping for right-sided RCC | |
Satinsky Clamps | Refined techniques for low-level thrombi | |
Fogarty Balloon Catheters | Proximal IVC occlusion without liver mobilization | |
IVC Tributaries Management | Hem-o-lok clips and sutures for secure vascular control | |
Dual-Positioning Strategies | For left-sided RCC with thrombi extending beyond the SMA | |
Pure Robotic RN and IVTTx | Reported in 24 cases | |
3D Reconstruction | Precise IVC resection in left-sided RCC with Level II thrombi | |
Selective Robotic Cavectomy/Thrombectomy | Based on IVC wall invasion, using tailored vascular stapling techniques | |
Cephalic IVC Non-Clamping Technique | Increased pneumoperitoneum pressure to control blood flow | |
Robot-Assisted Laparoscopy for Level III-IV Thrombi | IVC-First, Kidney-Last Strategy | Prioritizes thrombus extraction and IVC repair before renal manipulation |
Intracaval Balloon Occlusion and Robotic Biologic Patch Cavoplasty | For complex Level III thrombi | |
Liver Mobilization and SHV Ligation | Based on thrombus location relative to FPH and SPH | |
Cardiopulmonary Bypass (CPB) and Thoracoscopy-Assisted Thrombectomy | For Level IV cases and intra-atrial thrombi | |
Modified Sequential Vascular Control Strategy | Enables early CPB cessation | |
Rubber Vascular Bands | Sequential IVC clamping | |
Stepwise Thrombus-Lowering Technique | Reduces CPB duration by transitioning vascular control |
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Wu, Y.; Feng, S.; Fu, P. Minimally Invasive Surgical Techniques for Renal Cell Carcinoma with Intravenous Tumor Thrombus: A Systematic Review of Laparoscopic and Robotic-Assisted Approaches. Curr. Oncol. 2025, 32, 256. https://doi.org/10.3390/curroncol32050256
Wu Y, Feng S, Fu P. Minimally Invasive Surgical Techniques for Renal Cell Carcinoma with Intravenous Tumor Thrombus: A Systematic Review of Laparoscopic and Robotic-Assisted Approaches. Current Oncology. 2025; 32(5):256. https://doi.org/10.3390/curroncol32050256
Chicago/Turabian StyleWu, Yiting, Shuyang Feng, and Ping Fu. 2025. "Minimally Invasive Surgical Techniques for Renal Cell Carcinoma with Intravenous Tumor Thrombus: A Systematic Review of Laparoscopic and Robotic-Assisted Approaches" Current Oncology 32, no. 5: 256. https://doi.org/10.3390/curroncol32050256
APA StyleWu, Y., Feng, S., & Fu, P. (2025). Minimally Invasive Surgical Techniques for Renal Cell Carcinoma with Intravenous Tumor Thrombus: A Systematic Review of Laparoscopic and Robotic-Assisted Approaches. Current Oncology, 32(5), 256. https://doi.org/10.3390/curroncol32050256