**3. Surgical procedure**

trend in the morbidity of RCC has been increasing [1]. The hallmark of RCC is its biological characteristic of invading the renal vein and/or inferior vena cava (IVC), which occurs in 4–10% of patients [2]. Past clinical decision making mostly adopts conservative treatment, in terms of high morbidity and mortality rates during this kind of procedures. Radical nephrectomy (RN) with tumor thrombectomy is the standard approach for treating such challenging cases [3]. These patients were able to obtain, as literature reported, better long-term survival,

With the development of laparoscopy and robotic technology and the accumulation of practical experience in surgery, we noted that the height of IVC thrombus could not sufficiently guide the choice of surgical strategy, considering that only the thrombus height was assessed. Several factors, such as the effect of neoadjuvant targeted molecular therapy (TMT), invasion of the IVC wall, venous occlusion, establishment of collateral circulation, IVC thromboembolism, and primary tumor location, can determine the surgical strategy. The present comprehensive review describes how those factors influence surgical strategy

RCC tends to invade the renal venous system, forming a thrombus that invades the IVC and even involving the right atrium [2]. RN with tumor thrombectomy is the standard approach for treating such challenging cases. The grading system based on tumor thrombus height was created to determine surgical strategies. As early as 1987, the Mayo Clinic had adopted the "NEVES grading." Level I is defined as a tumor thrombus that is <2 cm apart from the orificium of the renal vein. Level II is defined as a tumor thrombus extending to the IVC >2 cm above the renal vein but below the hepatic veins. Level III is defined as a tumor thrombus that extends above the hepatic veins but below the diaphragm. Level IV is defined as a tumor thrombus located above the diaphragm. Surgical strategies are varied in corresponding levels. Traction of the liver is required in levels I to II. Turning-up the liver, blocking-up vessels located below the diaphragm, and clamping the portal vein are required in levels II to III. The establishment of an extracorporeal circulation is necessary in levels III and IV [8]. In 2002, the University of Miami divided level III tumor thrombus into four categories ulteriorly, which corresponded to diverse surgical strategies [9]. However, the most classic guideline is the "5-level classification" of a tumor thrombus, which was proposed by the Mayo Clinic in 2004 [10]. Idiographic grading standards and surgical strategies are shown

Nevertheless, these grading systems are completely based on the experience of open surgery. Since Skinner first reported the open surgery of IVC tumor thrombectomy in 1972 [11], the technique of IVC tumor thrombectomy has been improving continuously. Some scholars had attempted to accomplish these surgeries with laparoscope in 2002 [12, 13]. In 2011, Abaza first reported on robot-assisted IVC tumor thrombus extraction [14]. In recent years, several medical centers have investigated the safety and feasibility of robot-assisted laparoscopic IVC thrombectomy (RAL-IVCTE) [15–18]. Based on the anatomic characteristics of RCC, we

and the tumor-specific survival rate is in up to 50% [4–7].

**2. Technological innovations and classifications**

and patient outcomes.

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in **Table 1**.

#### **3.1. Anesthesia and patient position**

After general anesthesia induction and Foley catheter placement, the patients were positioned in a left lateral decubitus position with a 60–70° bump (**Figure 1A** and **B**). For right RCC, R-IVCTE and RN can be both completed with this position. For left RCC, R-IVCTE can be completed with this position. After R-IVCTE, the placement of patients was converted to a right lateral decubitus position with a 60–70° bump, and left RN was performed.

#### **3.2. Right RN and IVC thrombectomy**

The hepatocolic, hepatorenal, and chain ligaments were incised. The liver required to be upretracted. The anterior layer of the perirenal fascia was opened, the duodenum was dissected and retracted inside, and the IVC was exposed. Full dissection of the IVC, left renal vein, and part of the lumbar vein were required at the location of the tumor thrombus (**Figure 1C**). For level II IVC thrombus, the hepatic short vein, and even right central vein of the adrenal gland, was also clipped and divided (**Figure 1D**). Sequential clamping of the caudal IVC, left renal vein, and cephalic IVC were performed using vessel loops (**Figure 1E**). After the vessels were clamped, the IVC wall was cut, and the thrombus was removed (**Figure 1F**). After the IVC

**3.3. Left RN and IVC thrombectomy**

bypass was established (**Table 2**).

The patient position and port placement were the same as those for the right RCC. However, we suggest that left renal artery embolization must be performed 1–2 h preoperatively. The steps were similar in dissecting the IVC. Subsequently, we ligated and divided the left renal vein, which included the thrombus, with Endo-GIA (**Figure 1H**). The clamping sequence was the caudal IVC first, followed by the right renal artery, right renal vein, and cephalic IVC. After thrombus removal, the placement of the patients was converted to a right lateral

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Recently, the latest research completed by our team investigated the surgical method of robot-assisted retro- or superohepatic vena caval tumor thrombectomy and its influence factor. We found that the surgical strategy for patients with retrohepatic vena caval tumor thrombi depends on the upper extent of the tumor thrombus [20]. In addition, the first porta hepatis and hepatic veins are important anatomical boundaries. The surgical technique was described as follows. If the retrohepatic thrombus was located inferior to the first porta hepatis (**Figure 2A**), some short hepatic veins should be ligated, but the liver should not be mobilized. If the retrohepatic thrombus was located between the first porta hepatis and hepatic veins (**Figure 2B**), mobilization of the right lobe of the liver is an important step. For retrohepatic thrombus located closer or above the second porta hepatis (liver vein) but below the infra-diaphragm (**Figure 2C**), mobilization both the right and left lobes of the liver can facilitate high proximal control of the superohepatic IVC. In addition, the first porta hepatis should be clamped. For superohepatic (level IV) thrombus, thoracoscope-assisted open atriotomy was performed to cut the atrial part of the thrombus, and vena caval tumor thrombectomy was subsequently performed by clamping the superodiaphragm IVC after cardiopulmonary

**Figure 2.** The first porta hepatis and hepatic veins are important anatomical boundaries on representative images of radiography. The retrohepatic thrombus inferior to the first porta hepatis (A). The retrohepatic thrombus inferior to the first porta hepatis (B). The retrohepatic thrombus closer or above the second porta hepatis (liver vein) but blew infra-

diaphragm (C). FPH = first porta hepatis; SPH = second porta hepatis; IVC = inferior vena cava tumor.

decubitus position, with a 60–70°bump, and left RN was performed.

**3.4. Surgical technique for retro- or superohepatic IVC thrombus**

**Figure 1.** Surgical procedure for robot-assisted laparoscopic inferior vena cava thrombectomy. Patient position and port placement is shown, with three assistant ports used. (A and B). The inferior vena cava and left renal vein was exposed (C). The hepatic short vein was clipped and divided (D). Sequential clamping caudal IVC, left renal vein, and cephalic IVC were performed by vessel loops (E). The thrombus was removed (F). The IVC was closed with 5-0 polypropylene suture (G). Ligation and division of the left renal vein for the left RCC (H). Intraoperative IVC interruption in selected cases (I). IVC = inferior vena cava; RCC = renal cell carcinoma.

lumen was irrigated with heparinized saline, 5-0 polypropylene suture was used to close the IVC (**Figure 1G**). The tourniquets of the caudal IVC, left renal vein, and cephalic IVC were sequentially loosened. In the same position, right RN was completed.

#### **3.3. Left RN and IVC thrombectomy**

lumen was irrigated with heparinized saline, 5-0 polypropylene suture was used to close the IVC (**Figure 1G**). The tourniquets of the caudal IVC, left renal vein, and cephalic IVC were

**Figure 1.** Surgical procedure for robot-assisted laparoscopic inferior vena cava thrombectomy. Patient position and port placement is shown, with three assistant ports used. (A and B). The inferior vena cava and left renal vein was exposed (C). The hepatic short vein was clipped and divided (D). Sequential clamping caudal IVC, left renal vein, and cephalic IVC were performed by vessel loops (E). The thrombus was removed (F). The IVC was closed with 5-0 polypropylene suture (G). Ligation and division of the left renal vein for the left RCC (H). Intraoperative IVC interruption in selected

sequentially loosened. In the same position, right RN was completed.

cases (I). IVC = inferior vena cava; RCC = renal cell carcinoma.

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The patient position and port placement were the same as those for the right RCC. However, we suggest that left renal artery embolization must be performed 1–2 h preoperatively. The steps were similar in dissecting the IVC. Subsequently, we ligated and divided the left renal vein, which included the thrombus, with Endo-GIA (**Figure 1H**). The clamping sequence was the caudal IVC first, followed by the right renal artery, right renal vein, and cephalic IVC. After thrombus removal, the placement of the patients was converted to a right lateral decubitus position, with a 60–70°bump, and left RN was performed.

#### **3.4. Surgical technique for retro- or superohepatic IVC thrombus**

Recently, the latest research completed by our team investigated the surgical method of robot-assisted retro- or superohepatic vena caval tumor thrombectomy and its influence factor. We found that the surgical strategy for patients with retrohepatic vena caval tumor thrombi depends on the upper extent of the tumor thrombus [20]. In addition, the first porta hepatis and hepatic veins are important anatomical boundaries. The surgical technique was described as follows. If the retrohepatic thrombus was located inferior to the first porta hepatis (**Figure 2A**), some short hepatic veins should be ligated, but the liver should not be mobilized. If the retrohepatic thrombus was located between the first porta hepatis and hepatic veins (**Figure 2B**), mobilization of the right lobe of the liver is an important step. For retrohepatic thrombus located closer or above the second porta hepatis (liver vein) but below the infra-diaphragm (**Figure 2C**), mobilization both the right and left lobes of the liver can facilitate high proximal control of the superohepatic IVC. In addition, the first porta hepatis should be clamped. For superohepatic (level IV) thrombus, thoracoscope-assisted open atriotomy was performed to cut the atrial part of the thrombus, and vena caval tumor thrombectomy was subsequently performed by clamping the superodiaphragm IVC after cardiopulmonary bypass was established (**Table 2**).

**Figure 2.** The first porta hepatis and hepatic veins are important anatomical boundaries on representative images of radiography. The retrohepatic thrombus inferior to the first porta hepatis (A). The retrohepatic thrombus inferior to the first porta hepatis (B). The retrohepatic thrombus closer or above the second porta hepatis (liver vein) but blew infradiaphragm (C). FPH = first porta hepatis; SPH = second porta hepatis; IVC = inferior vena cava tumor.


**5. Postoperative targeted therapy in patients without metastasis**

For patients with non-metastatic RCC and tumor thrombus, the recurrence rate of the tumor is approximately 50% at 3 years preoperatively, despite performing RN [27]. Thus, for these patients, only operative treatment may not be sufficient. Adjuvant IL-2/IFN applied in prophase postoperatively, chemotherapy, and hormone therapy are all negative for high-recurrence risk RCC [28]. Small molecules targeting the vascular endothelial growth factor pathway prolong the progression-free survival of patients with advanced RCC [29, 30]. Based on these, the postoperative application of antiangiogenic medicine for patients with high-relapse risk RCC will play a positive role. Three randomized controlled trials, currently, have reported the outcomes of adopting targeted therapy for high-recurrence risk RCC. Although a study found that sunitinib treatment 1-year postoperatively prolonged relapse-free survival for 1–2 years. Two other studies did not find a survival benefit [31–33]. Therefore, the European Association of Urological Surgeons

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does not recommend targeted drugs for postoperative RCC with high risk of relapse [34].

adjuvant sorafenib or sunitinib [19].

tinely is not recommended [37, 38].

**6. Strategies and indications of IVC venography**

For patients with non-metastatic RCC and tumor thrombus, a cohort study designed by the Chinese PLA General Hospital analyzed the efficacy and safety of the postoperative administration of sorafenib or sunitinib. The results showed that no survival benefit was observed for patients with tumor thrombus or IVC tumor thrombus who were administered postoperative

Sufficient preoperative imaging data is requisite for successful thrombectomy. However, several problems in the imaging diagnosis of IVC tumor thrombus still exist: Type-B ultrasound has difficulty in accurately diagnosing abnormal changes owing to numerous interferences. Magnetic resonance imaging (MRI) and computed tomography cannot effectively reflect the collateral circulation, and cannot define the degree of occlusion [35]. Therefore, more effective means are required to supplement these three routine examinations. IVC venography can observe the thrombus occlusion through the lateral position, which enables to maximize a rich data of tumor thrombus preoperatively and to make a more accurate surgical plan.

IVC venography has been widely used in the diagnosis of Budd-Chiari syndrome and other diseases [36]. There are still more applications in renal cancer with IVC tumor thrombus yet. Some studies reported that <15% of cases of patients with cancer thrombus would use IVC venography, and some researchers previously thought that the inspection might have falsepositive or false-negative results. Meanwhile, there is a risk of emboli-induced pulmonary embolism or tumor embolus exfoliate diffusion. Therefore, performing IVC venography rou-

However, with the improvement of radiographic technique in recent years, the safety of IVC venography has been observably improved, and this method may define the formation of collateral circulation of the vena cava and help develop a thrombectomy strategy, which has unique diagnostic advantages. Hence, conducting a new study for IVC venography is necessary. Based on our experience, we speculate that the following patients may be a candidate for IVC venography: (1) RCC with IVC tumor thrombus; (2) clearance of the tumor thrombus

**Table 2.** Changes of techniques for robot-assisted retro- or supero-hepatic vena caval tumor thrombectomy in our method.
