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Application of laparoscopic ultrasound in retroperitoneal radical nephrectomy for renal cell carcinoma with Type II inferior vena cava tumor thrombectomy

1 Department of Ultrasound Medicine, Beijing Chao-Yang Hospital, Capital Medical University, Beijing, China
2 Department of Ultrasound, Fengrun People's Hospital, Tangshan, China
3 Department of Urology, Beijing Chao-Yang Hospital, Capital Medical University, Beijing, China

Date of Web Publication29-Jun-2022

Correspondence Address:
Ruijun Guo,
Department of Ultrasound Medicine, Beijing Chao-Yang Hospital, Capital Medical University, Beijing
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/ijc.IJC_153_18


Background: The aim of this study was to investigate the application value of laparoscopic ultrasound (LU) in retroperitoneal radical nephrectomy for renal cell carcinoma with Type II inferior vena cava tumor thrombectomy (RRN-RCC-TII-IVCTT).
Methods: The clinical data (operative time, length of tumor thrombus, tumor length, intraoperative bleeding, clinical stage, histological type, residual tumor tissue, and postoperative follow-up) of 6 patients who underwent LU-guided RRN-RCC-TII-IVCTT were retrospectively analyzed, and the intraoperative experience of LU was also summarized.
Results: All 6 patients recovered well with liver and kidney functions returning to normal, and no tumor recurrence, metastasis, or vena cava tumor thrombus.
Conclusions: LU-guided RRN-RCC-TII-IVCTT is a feasible treatment option, which locates the tumor accurately by retroperitoneal approach and provides the additional benefit of reduced intraoperative bleeding and shortened operative time, also achieving the much sought-after goal of precision.

Keywords: Intraoperative ultrasound, laparoscopic ultrasound, radical nephrectomy, renal cell carcinoma, retroperitoneal approach, Type II inferior vena cava tumor thrombus

How to cite this URL:
Cao W, Mi S, Yu Z, Guo D, Qu P, Liang X, Xing N, Zhang J, Zhang J, Guo R. Application of laparoscopic ultrasound in retroperitoneal radical nephrectomy for renal cell carcinoma with Type II inferior vena cava tumor thrombectomy. Indian J Cancer [Epub ahead of print] [cited 2022 Dec 5]. Available from:

  Introduction Top

Renal cell carcinoma (RCC) is a common malignant urinary tract cancer and is more prone to the involvement of the venous system, especially the inferior vena cava (IVC).[1],[2] Formation of an IVC tumor thrombosis (IVCTT) would lead to IVC obstruction, and patients might present with symptoms such as abdominal distention, varicocele, lower extremity edema, proteinuria, and Budd–Chiari syndrome, thus seriously affecting the quality of life. As an option, radical surgery can prolong survival for patients with RCC and IVC thrombus.[3] Currently, open IVCTT is the standard surgery for renal cell carcinoma inferior vena cava tumor thrombectomy (RCC-IVCTT);[4] however, during open surgery for IVCTT, the surgeon is limited by operating space and field of vision. Being minimally invasive, laparoscopy could be performed for IVCTT, which could shorten the operation time, reduce intraoperative bleeding, and shorten hospital stay.[5],[6] At present, totally trans-peritoneal laparoscopic, hand-assisted laparoscopic, single port laparoscopic, laparoscopic-assisted, and robot-assisted right nephric renal cell carcinoma (RN-RCC) have been widely performed for treating RCC-IVCTT,[7],[8],[9],[10],[11],[12],[13] but most RN- RCC-IVCTT cases use the trans-peritoneal pathway, and the totally retroperitoneal laparoscopic approach is infrequently applied.[9],[14] Due to the complex surgical procedure involved in radical nephrectomy including IVC blocking, thrombectomy, and repair, laparoscopic ultrasound (LU) is required for proper visualization.

Our hospital has completed a total of 6 LU-guided retroperitoneal radical nephrectomy for renal cell carcinoma with Type II inferior vena cava tumor thrombectomy (RRN-RCC-TII-IVCTT) cases from January 2013 to December 2015. This study summarizes the experience obtained from these 6 cases and aims to evaluate the operational skills and application value of LU in renal cell carcinoma with Type II inferior vena cava tumor thrombectomy (RRN-RCC-TII-IVCTT).

  Materials and methods Top


From January 2013 to December 2015, six patients with a diagnosis of right renal cell cancer (Neves stage II) and IVC infrahepatic thrombus underwent RRN-RCC-TII-IVCTT using a retroperitoneal approach in our hospital. In total, 5 men and 1 woman with mean age of 58 years, ranging from 43 to 69 years, were studied. Mean body mass index (BMI) was 24.0 kg/m2, ranging from 21.0 kg/m2 to 27.0 kg/m2. Cardiac and pulmonary functions were normal. Complete serum evaluation including hemoglobin, hematocrit, creatinine, liver function tests, and electrolyte levels was within normal limits. Abdominal ultrasound, computed tomography (CT), and magnetic resonance imaging (MR) were used to define tumor location and vascular extension in all patients. CT and MR showed no metastasis. Deep vein thrombus of lower limbs was ruled out by a presurgical ultrasound.

Surgical method and application of LU

All patients underwent LU-guided RRN-RCC-TII-IVCTT under general anesthesia: after entering the retroperitoneal cavity, four sleeves were inserted: point A was located at the junction of the 12th sub-rib and the posterior axillary line; point B was located under the costal margin of the anterior axillary line; point C was located two-fingers above the iliac crest; point D was located two-fingers away from the inner side of the anterior superior iliac crest below point B. CO2 was used to maintain the pneumoperitoneum at a pressure of 15 mmHg, and one laparoscope was placed at point C; after separation and ligation of the right renal artery, the IVC was separated from the anteroinferior site of the renal artery, extending from the lower renal pole to the inferior border of the liver, so that the contralateral renal vein could be separated and exposed; all the lumbar vein branches were then blocked behind the vena cava. The ALOKA 4000 ultrasound (Aloka Co. Ltd, Tokyo, Japan) equipped with a laparoscopic probe (UST-5536, 7.5 MHz) was used intraoperatively to delineate the relation of the tumor thrombus and IVC [Figure 1], as well as to precisely mark the proximal and distal ends of the tumor thrombus [Figure 2] and [Figure 3]. As an indicator of IVC and dual protection, homemade elastic tourniquets ligated loop at both ends of the IVC tumor thrombus to prevent falling off and bleeding. The distal end of the IVC tumor thrombus was first ligated, followed by blocking of the left renal vein using bulldog forceps, and the proximal end of the IVC was finally blocked. After this procedure, the systemic circulation exhibited no obvious abnormalities, and LU was also performed to explore the blocking effect, which was considered successful if no color flow signals and spectrum signals were seen in the involved kidney. The vena cava wall was then cut to remove the tumor thrombus and tumor containing right renal vein, followed by vascular anastomosis using three-point continuous suture method with absorbable 4-0 suture material. During above procedure, we monitored the left renal perfusion by using LU every 30 min. The distal IVC end, left renal vein, and proximal loop of IVC end were then opened consecutively; LU was performed to determine the blood flow and thrombus condition in the IVC to decide whether the proximal IVC end should be opened and thrombolysis should be performed [Figure 4]. The kidney and suspicious lymph nodes were then freed and completely removed outside Gerota's fascia. Meanwhile, we monitored vital signs to prevent pulmonary embolism during surgery and used the low molecular heparin to prevent the microthrombi from low limbs and pelvic vein.
Figure 1: Relation of tumor thrombus and inferior vena cava confirmed by laparoscopic ultrasound. Thrombus: tumor thrombus; IVC: residual lumen of inferior vena cava

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Figure 2: Upper boundary of tumor thrombus involving inferior vena cava. Thrombus: tumor thrombus; IVC: residual lumen of inferior vena cava; Liver: liver; arrow: IVC wall invaded by thrombus

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Figure 3: Lower boundary of tumor thrombus involving inferior vena cava. Thrombus: tumor thrombus; IVC: residual lumen of inferior vena cava; arrow: clear boundary of IVC wall

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Figure 4: Color Doppler demonstrated the patency of inferior vena cava after thrombectomy. IVC: residual lumen of inferior vena cava; arrows showed the narrow lumen after reconstruction of IVC

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The surgical and postoperative pathological conditions of these 6 patients are shown in [Table 1].
Table 1: Surgical conditions of the 6 RCC-IVCTT patients

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  Results Top

All patients exhibited good postoperative recovery and recovered well after removal of the peritoneal drainage tubes; liver and kidney function recovered to normal, and there was no tumor recurrence, metastasis, or vena cava tumor thrombus. The 6-month follow-up also demonstrated the above recovery conditions. Three cases had no tumor recurrence after a 24-month follow-up. Two cases developed liver metastasis after a 12-month follow-up. One case was lost to follow-up after 6 months. These 6 cases proved that LU-guided RRN-RCC-TII-IVCTT is a feasible treatment option and can lead to good surgical outcomes.

  Discussion Top

The key of RRN-RCC-IVCTT lies in opening the IVC for the thrombectomy, with the technique of dissection, the cutting range and site being related to the tumor thrombus length and degree of violation. Therefore, tumor thrombus and RCC typing are essential for guiding in the selection of surgical approach. Currently, the four main recommended staging systems in RRN-RCC-IVCTT are TNM staging,[14] Neves staging,[15] Novick staging,[16] and Hinman staging.[17] TNM, Novick, and Hinman staging methods are less detailed than Neves when the tumor thrombus invades the IVC. The difficulties of this surgery lie in cutting, suturing, and protecting the IVC, additionally ensuring complete resection of the tumor thrombus. Therefore, in our study, the Neves system, based on the level of invasion of the tumor thrombus into the IVC, was used to perform surgical typing, as well as to determine the surgical plan. Besides, we only included right RRN-RCC-IVCTT in this study considering the higher bleeding and clamping risk of left side. However, based on the satisfactory clinical results, we wish to apply this approach on the left side after complete evaluation. Although the preoperative Neves staging system would clarify the position of tumor thrombus based on CT and MRI results, these two methods would not clearly display the blood supply of the tumor thrombus and the relationship between the tumor thrombus and the venous wall; therefore, they could not provide a reference to determine whether the venous wall should be retained after the vena cava thrombus is removed. However, due to its high frequency, the probe of LU could be directly placed on the surface of an organ intraoperatively, thus clearly displaying the relationship between the IVC wall and tumor thrombus, as well as the blood supply of the tumor thrombus [Figure 1]. LU could also distinguish the tumor thrombus from a thrombus, as well as whether the vena cava wall was involved [Figure 2] and [Figure 3], based on the blood flow conditions; hence, we could decide whether or how much the vena cava wall should be retained based on the LU results and the IVC incision condition. LU did not only compensate the surgical plan limitations faced by the Neves staging, refined the surgical procedure, protected the IVC as far as possible, and prevented postoperative risks but also significantly improved the diagnostic accuracy; furthermore, LU was reported indispensable in RRN-RCC-IVCTT.[18]

LU is one of the methods of interventional ultrasound, and its linear- or convex-array probe could enter the abdominal cavity via the Trocar to explore the condition directly on the organ surface. The technique requires certain spatial orientation abilities among surgeons, who should be quite familiar with the anatomical structures and laparoscopic surgeries. Meanwhile, during pneumoperitoneum, in order to obtain high-quality images, the probe matching layer should closely contact the target organ. However, when used for vascular exploration, especially veins, excessive force might be applied for better organ contact, thus flattening the vascular lumen and affecting the display of venous blood flow. Therefore, while operating the probe, appropriate force should be applied, or the target vessel could be explored using other organs as acoustic windows. As the linear-array probe has high resolution but a small exploring angle, the contact range with the target tissue needs to be increased to obtain high-quality images. However, the retroperitoneal space is small, so occasionally it might be inconvenient to use the linear probe. Although the near-field exploration ability of the end-scanning convex-array probe is limited, it has a bigger scanning angle and smaller fit surface, resulting in satisfactory images using other organs as the acoustic window and increasing the distance between the probe and target; furthermore, it has relatively smaller operating space requirements. Therefore, these two probes should be alternately used during surgeries to achieve the best display effect. IVCTT is also involved in partial resection and repair of venous walls, and LU could accurately pinpoint the tumor thrombus intraoperatively, thus reducing the damage to the IVC and ensuring complete resection of the tumor thrombus. LU-guided IVCTT performed by Chinese and foreign surgeons was usually combined with laparotomy, or the retroperitoneal LU and trans-peritoneal approach were combined, and the patient's position or surgical procedures changed intraoperatively.[19],[20] However, the 6 cases performed in our hospital were completed for the first time using the retroperitoneal approach, which reduced the risk of anesthesia, and achieved the purpose of avoiding damage to the retroperitoneal and intraperitoneal organs by using LU.

Renal blood supply varies, and tumor blood supply is complex; therefore, blocking the main renal artery often could not completely cut off the tumor blood supply. Exploring the effects of renal artery occlusion by LU in this study has an important implication for reducing bleeding and preventing tumor thrombus shedding. Second, fully blocking the lumbar vein is the key in the retroperitoneal approach. If lumbar vein occlusion is not complete, hastily cutting the IVC would cause a lot of bleeding. Although the retroperitoneal approach could benefit renal artery occlusion, due to its limited operation space, it is not conducive for blocking the contralateral renal vein. If the contralateral renal vein cannot be completely blocked during surgery, it would also cause heavy bleeding. Therefore, applying LU to determine the blocking effects of major blood vessels would prove to be of great significance and could shorten the operation time and reduce blood loss to a great extent. At the same time, too large a tumor (Case 6) meant that the dissection range between the tumor and normal tissue would be large, the operating requirements would be complex, and the intraoperative blood loss will increase; long tumor thrombus in IVC (Case 5) would also require a larger IVC dissection range, so the lumbar vein and peri-IVC vessels that need to be blocked will be more, and this also would cause more bleeding. Based on our experience, the IVC tumor thrombus less than 5 cm in diameter will present relatively easy operation technique and minimal blood loss.

During the IVCTT procedure, the IVC should be first ligated by a tourniquet to block the blood flow; second, because a partial tumor thrombus would violate the venous wall, a part of the IVC wall would require removal and repair, thus activating the clotting mechanisms, and these would all become risk factors for IVC thrombosis. If these risks of thrombosis are not paid enough attention and pulmonary embolism develops, they could lead to surgical failure. Furthermore, due to surgical stretch, the tumor thrombus might also shed, thus causing a pulmonary embolism. Therefore, real-time intraoperative LU monitoring of the IVC must be performed. First, before blocking the IVC, LU should be used to reconfirm the location of the tumor thrombus in the proximal segment of the ligation. After completing thrombectomy and repair of the IVC, as well as before and after releasing the tourniquet, LU should be performed again to determine the presence of thrombosis and evaluate hemodynamic conditions after IVC recanalization to prevent a large number of thrombi, and this would be extremely important for the success of surgery. Once acute thrombosis was found during surgery, the surgeons could inject heparin or place a filter to reduce the risk of pulmonary embolism. In addition, repairing or partially resecting the IVC wall would inevitably affect the IVC reflux; hence, intraoperative LU can be used to observe the hemodynamic changes in the IVC to decide whether postoperative anticoagulants, such as heparin, should be initiated based on the changes in order to prevent pulmonary embolism.

Although preoperative CT and MRI could locate the position of the tumor thrombus, the operative space of retroperitoneal approach is small, and the field of vision would be limited; therefore, it is impossible to find the beginning and the end of the tumor thrombus with clear anatomical landmarks. In addition, due to the limited touch sensation of the operators, it is impossible to pinpoint the start and end points of the tumor thrombus by palpation during laparoscopy. The application of LU in IVC thrombectomy could help surgeons to accurately locate borders of the tumor thrombus and accurately select the level of the IVC block according to location of the tumor thrombus; furthermore, on ensuring complete resection of the tumor thrombus, the IVC incision could also be reduced as much as possible. To some extent, LU could shorten the operation time, ensure surgical safety, and reduce chances of tumor recurrence due to incomplete incision. The postoperative pathology and inspection of the 6 patients in this study revealed that the desired surgical results had been achieved.

The limitation of this study was the short term of follow-up. The application of LU needs more training and costs valuable clamping time, which would increase the risk of renal insufficient and pulmonary embolism after surgery.

  Conclusions Top

In summary, with continuous developments in surgical techniques, LU would be gradually applied for the treatment of RCC-IVCTT. The surgical approach of LU-guided RRN-RCC-TII-IVCTT first proposed in our study is safe and feasible, and this surgical approach fully combines the advantages of retroperitoneal approach and LU. Therefore, it can effectively reduce trauma, avoid the risk of intraoperatively changing patient position, and ensures surgical safety, thus achieving the goal of precision.

Ethical approval

This study was conducted in accordance with the declaration of Helsinki. This study was conducted with approval from the Ethics Committee of Beijing Chao-Yang Hospital of Capital Medical University. Written informed consent was obtained from all participants.

Declaration of patient consent

The authors certify that they have obtained all appropriate patient consent forms. In the form, the patients have given their consent for their images and other clinical information to be reported in the journal. The patients understand that their names and initials will not be published and due efforts will be made to conceal their identity, but anonymity cannot be guaranteed.

Financial support and sponsorship


Conflicts of interest

There are no conflicts of interest.

  References Top

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  [Figure 1], [Figure 2], [Figure 3], [Figure 4]

  [Table 1]


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