Robot-assisted surgical strategies for inferior vena cava thrombus with special morphology: How to balance tumor control and functional preservation?

To the Editor: Locally advanced renal cell carcinoma (RCC) with inferior vena cava (IVC) thrombus (IVCT) (RCC-IVCT) poses a significant challenge in renal cancer surgery. Traditionally, the Mayo classification system has offered invaluable guidance for the surgical treatment of IVCT in the open and robot-assisted surgical era by designing surgical strategies based on the height of the IVCT.[1] However, additional factors can influence the surgical strategy for IVCT, including thrombus morphology, bland thrombus, and IVC invasion.[2,3] In the present study, we aimed to develop a decision-making scheme for IVCT morphological grouping and report surgical strategies for IVCT with various special morphologies. This study was conducted in accordance with the Declaration of Helsinki and was approved by the Institutional Review Board of Chinese PLA General Hospital (No. S2024-279-01). All patients provided written informed consent. The detailed information on patients’ recruitment, preoperative assessment and preparation, surgical technique, postoperative treatment and follow-up, and statistical analyses is presented in the Supplementary File, https://links.lww.com/CM9/C736. We developed a decision-making scheme to guide the morphological grouping for IVCT according to three parameters: invasion of the contralateral renal vein (CRV), invasion of the caudal IVC, and shape of upward growth [Supplementary Figure 1, https://links.lww.com/CM9/C736]. All patients were divided into common or special groups based on the morphological characteristics of the IVCT. The special group included the horizontal-T (HT) (17 cases), inverted-T (IT) (four cases), and Cross (22 cases) groups. HT indicates caudal IVC invasion of the IVCT beyond the second lumbar vein. The HT group was further subdivided into HTa (bland thrombus) and HTb (tumor thrombus). IT indicates invasion of the CRV by the IVCT, which was subdivided into ITa (bland thrombus) and ITb (tumor thrombus). Considering the influence of tumor laterality on surgical strategies for IVCT, this grouping varies according to the side of the tumor. Because the right renal vein (RRV) is notably shorter than the left renal vein (LRV), IVCT invading the RRV beyond 0.5 cm is considered to indicate CRV invasion, whereas for the LRV, the invasion must extend at least above the superior mesenteric artery (SMA). Group Cross combines the characteristics of both the HT and IT groups and is further subdivided into four distinct subtypes: HTa+ITa, HTb+ITa, HTa+ITb, and HTb+ITb. The common group included the normal group (106 cases) and the Banana group (48 cases); normal is the most common, while “Banana” signifies that the IVCT is slender and curves upward in a shape reminiscent of an exponential graph or banana [Supplementary Figure 2, https://links.lww.com/CM9/C736]. The robot-assisted surgical strategy, based on the Mayo classification, for cephalic IVCT and renal tumors in the normal group, including radical nephrectomy with IVC thrombectomy (RAT-IVCT) or IVC cavectomy (RAC-IVCT);[3,4] however, additional procedures are required for IVCT with special morphology after addressing the proximal tumor thrombus [Supplementary Figure 3, https://links.lww.com/CM9/C736]. In the Banana group, the CRV was selectively not clamped to minimize damage to the healthy kidney function, making this approach especially suitable for patients with preoperative renal insufficiency. The oblique downward clamp of the supra-CRV IVC and the cephalic IVC clamp was feasible, and the CRV returned through the caudal IVC during IVC clamping. For right-sided RCC with special morphological IVCT, in the HTa group, the caudal IVC below the RRV (infra-RRV) was stapled using Endo GIA (Covidien, Minneapolis, MN, USA) to protect as much of the collateral circulation of the caudal IVC as possible. In the HTb group, we prioritized tumor control before the preservation of the collateral circulation of the IVC. The main collaterals were carefully preserved under intraoperative ultrasound guidance during caudal IVC stapling. In the ITa group, the LRV was stapled. In the ITb group, the tumor thrombus in the LRV (LRVT) was removed before stapling. Alternatively, if feasible, LRV reconstruction was performed by clamping the left renal artery (LRA). If the LRV was not completely cleared of residual thrombus, it was stapled along the left SMA margin. In the Cross HTa+ITa group, the infra-RRV IVC and LRV were stapled. In the Cross HTb+ITa group, the LRV was stapled, followed by prioritizing tumor control at the caudal IVC. In the HTa+ITb group, we performed stapling of the infra-RRV IVC and subsequently removed the LRVT. The decision to staple or reconstruct the LRV was based on the intraoperative condition. In the HTb+ITb group, we first removed the LRVT and tumor thrombus in the caudal IVC (caudal IVCT), followed by reconstruction or stapling of the LRV, and finally made efforts to preserve the collateral circulation of the caudal IVC to the greatest extent possible. For left-sided RCC with special morphological IVCT, in the HTa group, the infra-RRV IVC was stapled to preserve maximum collateral circulation of the caudal IVC. In the HTb group, we removed the caudal IVCT and preserved the RRV and collateral circulation of the caudal IVC as much as possible. In the ITa group, the bland thrombus was removed from the RRV because ligating the RRV was not feasible. In the ITb group, tumor thrombus in the RRV (RRVT) was removed, and the RRV was reconstructed to allow blood return through the caudal IVC or cephalic IVC. In the Cross HTa+ITa group, the infra-RRV IVC was stapled first, and we removed the bland thrombus in the RRV and reconstructed the RRV return through the cephalic IVC. In the HTb+ITa group, we removed the bland thrombus in the RRV and caudal IVCT and reconstructed the RRV return through the caudal IVC or cephalic IVC. In the HTa+ITb group, if the cephalic IVC was stapled, we removed the RRVT and reconstructed the caudal IVC to ensure RRV return through the IVC collaterals. If we chose to perform a thrombectomy of the cephalic IVC, we removed the RRVT and stapled the infra-RRV IVC. In the HTb+ITb group, if the IVCT could not be completely removed, we performed an oblique downward cavectomy between the superior border of the RRV and the inferior border of the LRV, removed the RRVT and caudal IVCT, and reconstructed the RRV-caudal IVC return to avoid the potential risk of pulmonary embolism after the recurrence of tumor thrombus. Conversely, if thrombectomy was performed on the cephalic IVC, the RRVT and caudal IVCT were removed. The decision to staple or reconstruct the caudal IVC was based on the intraoperative situation. Patients in the special group had longer IVCT, higher Mayo classification levels, a larger maximum diameter of the tumor thrombus, and higher IVC blocking rates. No significant differences were noted in demographic characteristics, tumor location, size, grade, type, or lymph node and distant metastasis [Supplementary Table 1, https://links.lww.com/CM9/C736]. Supplementary Table 2, https://links.lww.com/CM9/C736 presents the perioperative outcomes and complications. The median operative time was significantly longer in the special group than in the common group (310 vs. 230 min; P = 0.001). Surgery for left-sided RCC took longer with higher blood loss than for right-sided RCC in both groups. The median estimated blood loss was 1200 mL (interquartile range [IQR]: 700–2000 mL) in the special group, which was significantly greater than the 700 mL (IQR: 300–1025 mL) in the common group (P <0.001). In the common group, most of the complications were mild (grades I and II); however, more severe complications were observed in the special group (P <0.05). Except for one death due to irreversible multiple organ failure in the special group, all patients with complications recovered within 1 month of symptomatic treatment without reoperation. The special group exhibited poorer preoperative liver and kidney function, potentially associated with higher IVC blocking rates. A statistically significant difference was observed only in the preoperative serum creatinine (SCR) [Supplementary Table 3, https://links.lww.com/CM9/C736]. Notably, postoperative SCR, alanine aminotransferase (ALT), and aspartate aminotransferase (AST) levels increased significantly compared to preoperative values, with a more pronounced increase in the special group. A marked disparity in ALT and AST levels emerged on the first postoperative day, along with notable differences in the peak SCR levels from postoperatively to discharge [Supplementary Figure 4, https://links.lww.com/CM9/C736]. Interestingly, no significant difference was observed in the incidence of postoperative acute kidney injury (AKI) between groups. Four patients in the common group and three in the special group received continuous renal replacement therapy. The postoperative elevations in the indicators of liver and kidney injury were transient, with no statistically significant differences in liver and kidney function between the groups on the day of discharge [Supplementary Figure 4, https://links.lww.com/CM9/C736]. During the median follow-up of 34 months, no patients developed contralateral kidney metastases. Survival analysis revealed that patients in the special group had poorer overall survival (OS) and progression-free survival (PFS); however, no statistically significant differences were found between the two groups. Given that radical surgery for RCC-IVCT is inherently highly invasive, the presence of high-grade IVCT may impact survival outcomes. Furthermore, after restricting the patient population to those with Mayo grades I–II, survival analysis demonstrated statistically significant differences in OS between the two groups (P <0.05) [Supplementary Figure 5, https://links.lww.com/CM9/C736]. Robot-assisted surgeries have gradually achieved various breakthroughs in surgical strategies for IVCT. As the oncological control of the tumor thrombus during surgery is reaching the point of perfection, even in those with higher Mayo grades, we should start considering better functional preservation for these patients after surgery. Balancing tumor control and functional preservation has always been a challenge in the field of RTs, especially for IVCT with special morphology. We designed a decision-making process based on the morphological grouping of IVCT. This grouping mainly focuses on the invasion of the contralateral renal vein and the caudal IVC, which differs from the previous grading method based on the height of the IVCT and anatomical landmarks of the cephalic IVC. This morphological grouping system can also complement existing robot-assisted surgical systems. We classified IVCT into two subtypes based on the nature of the thrombus: bland thrombus and tumor thrombus. In general, for patients with IVCT with special morphology, the priority for those with tumor thrombus will be tumor control, while for those with bland thrombus, it will be functional preservation. For mixed-type thrombus (Cross group), the strategy focuses more on postoperative functional preservation while ensuring adequate tumor control, including contralateral renal function, cardiopulmonary function, and reducing the risk of severe lower extremity edema and decreased cardiac output. The special group had more blood loss and longer operation time. This is due to the higher complexities involved in trying to achieve the desired oncological and functional outcome during the surgery. Although IVCT with special morphologies poses a greater surgical challenge, our cohort demonstrated that robot-assisted surgical strategies based on morphological grouping can effectively balance tumor control and functional preservation. In conclusion, we described the surgical strategies and oncological outcomes associated with various morphological groups of IVCT. The robot-assisted surgical strategies based on the morphological grouping are feasible and safe, striking a balance between tumor control and functional preservation. Despite the complexities of the surgery, a minimally invasive approach remained a viable option for selected RCC patients with special morphology IVCT. Further validation of the grouping system through multicenter and long-term follow-up studies is crucial to comprehensively assess the feasibility and advantage of the surgical strategies. Funding The project was supported by grants from the National Natural Science Foundation of China (No. 82273412 and 82373169) and the Research and Development Program of Ministry of Science and Technology of China (No. 2023YFB4706000). Conflicts of Interest None.