Use of a combined retroperitoneoscopic and transperitoneal laparoscopic technique for the management of renal cell carcinoma with level I tumor thrombi.

BACKGROUND: To report our initial experiences using a combined retroperitoneoscopic and transperitoneal laparoscopic technique for the management of renal cell carcinoma with level I tumor thrombi.
MATERIALS AND METHODS: Two patients underwent this technique for tumors 11- and 13-cm in diameter. After transection of the renal artery with limited mobilization of the kidney using a retroperitoneoscopic approach, additional ports were placed, and the management of the tumor thrombus was performed in the large working space provided by the transperitoneoscopic approach.
RESULTS: The technique was feasible in the present 2 cases. The total operative times were 170 and 200 min, respectively. The estimated blood loss was 450 cc in the first case and 200 cc in the second case. No complications were observed in either of the patients.
CONCLUSIONS: Based on the initial clinical experience, we have presented a feasible surgical option for the laparoscopic management of renal cell carcinoma with level I thrombi.

INTRODUCTION

It is well-established that renal cell carcinoma (RCC) has the tendency to invade the renal venous system. Despite the increasing frequency of incidentally diagnosed tumors, nearly 10% of RCC patients are diagnosed with renal vein and inferior vena cava (IVC) involvement.[1] The surgical management of these patients is challenging. Surgery remains the most effective treatment alternative, and with the exception of a small number of studies using sunitinib, no established neoadjuvant therapy is available for reducing the thrombus size in this group of patients.[23]

Since its first introduction, laparoscopic nephrectomy has come a long way.[45] Currently, laparoscopic radical nephrectomy (LRN) is the standard of care in T1-T2 RCC. With the use of LRN and the number of experienced surgeons increasing, it is now possible to perform surgery on large kidney tumors and tumors with level I or II thrombi. Worldwide, bulky lymphadenopathy and extensive inferior vena caval or perinephric visceral involvement remain contraindications for LRN.

Herein, we have presented a combined retroperitoneoscopic and transperitoneal laparoscopic technique for the management of RCC with level I tumor thrombi to decrease bleeding and to allow better visualization and management of the thrombus.

MATERIALS AND METHODS

Between January 2011 and August 2012, 5 cases of RCC were treated with a combined technique that uses both retroperitoneoscopic and transperitoneal approaches. Of these 5 cases, 2 cases with level I tumor thrombi were retrospectively evaluated for the surgical techniques and perioperative data. The other 3 patients also underwent operations using this technique, but in these cases, the patients suffered from large kidney tumors without renal vein thrombus and, therefore, fall outside of the scope of the present report.

Case 1

A 70-year-old man was referred to our department with an 11 × 10 × 8 cm stage T3b (2009 TNM classification system) right renal tumor extending into the vena and was evaluated with contrast enhanced computed tomography (CT). The radiology department reported that the tumor thrombus in the renal vein extended 2 cm into the vena cava and that there was no evidence of hilar lymphadenopathy [Figure 1]. In addition, a second tumor measuring 3 × 3 × 3 cm was detected at the upper pole of the left kidney. The patient's thorax CT and bone scan were negative. After obtaining the consent of the patient, we decided to perform a LRN using a combined retroperitoneoscopic and transperitoneal technique.

Figure 1

Right renal tumor with renal vein thrombus extending to the inferior vena cava

Surgical Technique

The operation began by using a retroperitoneoscopic approach while the patient was in a standard full flank position. A 2-cm incision was made at the Petit's triangle, and a dissector was inserted into the retroperitoneal space through the thoracolumbar fascia. The retroperitoneal space was initially created with an index finger and was then expanded using a balloon dilator. Subsequently, a 5-mm trocar was inserted at the tip of 12th rib and a 12-mm trocar was inserted 3-cm above the anterior superior iliac spine. Following, the placement of a 10-mm trocar at the Petit's incision for the camera, the operation proceeded with the opening of the Gerota's fascia and the subsequent identification of the ureter, renal hilum, and vessels. After the placement of 3 Hem-o-lok® clips on the renal artery, the vessel was transected. Meanwhile, the renal vein was identified and dissected up to the junction at the vena cava. Following this, a small incision was made in the peritoneum to produce a pneumoperitoneum. At this point, all laparoscopic equipment was transferred to the right side, and the primary (OS) and assistant surgeons moved to the patient's left side. A 10-mm trocar was introduced into the abdominal cavity lateral to the umbilicus under the vision of the camera inserted from 12-mm port used in retroperitoneoscopic approach. Meanwhile, a second 12-mm port was placed at the midclavicular line 2-cm below the costal margin and a third port 5-mm in size was inserted between the anterosuperior iliac spine and the umbilicus [Figure 2]. A transabdominal dissection began with the incision of the white line of Toldt, and the ascending colon was reflected medially to clearly expose the previously dissected retroperitoneum. The duodenum was reflected, the ureter was identified and the renal vein with the tumor thrombus was observed. With further dissection of the renal vein, which was collapsed and flattened, the vena cava was reached to reveal the distal portion of the tumor. However, the distal milking of the thrombus from the vena cava to the renal vein could not be achieved due to the inadequate elevation of the renal hilum. Therefore, the kidney was further released from the surrounding adhesions with only the upper pole attached. After this maneuver, the distal milking of the thrombus to the renal vein was achieved by further retraction of the renal hilum. Meanwhile, a Satinsky clamp was introduced from the 12-mm trocar that was used during retroperitoneal approach and was placed on the vena cava proximal to the tumor thrombus [Figure 3]. Subsequently, a Hem-o-lok clip was applied to the renal vein, and the thrombus was further milked with the aid of the jaws of a Hem-o-lok clip applier. The renal vein was transacted sharply above the Satinsky clamp. After releasing and removing the kidney from the operation site and placing the kidney in an organ bag, the vena cava was sutured with a 4-0 polypropylene suture and the Satinsky clamp was removed. After placing the suction drain and removing the kidney from the abdomen through an 8-cm Gibson incision, the operation was terminated without any complications.

Figure 2

Port placement. Right three trocars are located for retroperitoneoscopic approach, whereas left three trocars are for transperitoneal laparoscopy. An additional trocar may be needed for placement of Satinsky clamp. Please note that three trocars placed for retroperitoneoscopy are used for liver retraction or furthermost elevation of the renal hilum

Figure 3

Satinsky clamp placed on the vena cava proximal to the tumor thrombus

Case 2

A 46-year-old man presented with right upper quadrant abdominal pain. His CT and subsequent magnetic resonance imaging (MRI) revealed a 13 × 10 × 10 cm renal mass and a renal vein thrombus extending 1.5 cm into the vena cava. The metastatic work-up using a thorax CT and bone scan was negative. After obtaining the consent of the patient, surgery using the “combination technique” was planned.

The surgical technique was performed in the same manner as the former case with the exception of the method of milking the tumor thrombus and the transection of the renal vein from its junction with the vena cava. In this case, after the furthest possible elevation of the renal hilum, milking of the thrombus was achieved with the aid of the Hem-o-lok clip applier jaws, and, subsequently, 2 Hem-o-lok® clips were applied to the renal vein. After the transection of the renal vein, the specimen was immediately removed within an organ bag through the same incision described in the first case.

RESULTS

The total operative and insufflation times for the first case were 170 and 150 min, respectively, whereas, in the second case, the operation and insufflation lasted 200 min and 165 min, respectively. The estimated blood loss was 450 cc for the first case and 200 cc for the second case. Neither patient experienced any significant complications, and they were discharged from the hospital at postoperative days 5 and 4, respectively.

The pathological examination of the tumors of both patients revealed Fuhrman Grade 3 pT3b RCC with negative surgical margins and level I tumor thrombi in the renal vein [Figure 4].

Figure 4

Gross renal specimen demonstrating renal vein thrombus

One month after the operation, the patient in the first case underwent left laparoscopic partial nephrectomy with a warm ischemia time of 15 min. After 15 months of follow-up, the disease developed a 1-cm lung metastasis and the patient is currently scheduled for surgical excision of the mass. The current serum creatinine level of this patient is 1.4 mg/dl. The second patient underwent 3 months of follow-up with contrast enhanced CT scans, and no local recurrence was detected.

DISCUSSION

The rationale for the above-described technique is to combine the major advantages, including early hilar control and a large working space, of retroperitoneoscopic and transperitoneal laparoscopic techniques, respectively. We believe that early clamping of the renal artery using the retroperitoneoscopic approach may limit the risk of dislocation of the tumor thrombus by preventing antegrade flow. The limited mobilization of the kidney may also serve to minimize the risk of tumor embolization. At the same time, a visual appreciation of the proximal extent of the tumor thrombus may be achieved. Moreover, if tumor is small in diameter, the distal milking of the thrombus from the vena cava to the renal vein may be performed with gentle retraction of the renal vein, and subsequent clipping or stapling of the renal vein may be performed. However, it is worth mentioning that, in most instances, the elevation of the hilum for milking the thrombus into the renal vein is not possible due to an increase in the size of the specimen that decreases the working space during retroperitoneoscopic surgery. This task may be more difficult in left kidneys because of the longer course of left renal vein. In addition, the placement of a Satinsky clamp or an endovascular stapler is more difficult in a retroperitoneoscopic surgery due to the limited space. Because of the inevitable need to shift the tumor for clamp or stapler placement, disturbance of the tumor may occur. In contrast, a transperitoneal approach provides a large space for determining the anatomical landmarks and allows the greatest elevation of the lower kidney pole. We believe that significant elevation of the lower pole is necessary to milk the thrombus into the renal vein, because at least 2-3 cm of extra length in renal vein is needed to milk a level I vena cava thrombus. In addition, because of the large working space provided by a transperitoneal approach, it is much easier to place an endovascular stapler, Hem-o-lok® clips or a Satinsky clamp and subsequently place intracorporeal suturing. Furthermore, the placement of hand intracorporeally may allow tactile sensation of the thrombus if needed and eases the management of associated complications such as bleeding. The use of laparoscopic ultrasound for the identification of the proximal extent of tumor thrombi is much easier in transperitoneal approach.[6] In conclusion, the use of both approaches for the extirpation of the tumor in a pure laparoscopic way is able to exploit the major advantages of both techniques.

There are currently 4 categories used by the Mayo clinic to classify macroscopic involvement of vena cava thrombus in RCC.[1] Of these categories, levels I and II (all thrombi extend into the IVC >2 cm above the junction of the renal vein, but to not extend to the hepatic veins) are suitable for laparoscopic surgery at some experienced centers. Some researchers use the laparoscopic technique for the removal of level III and IV (all tumor thrombus over hepatic veins including right atrium) tumor thrombi as well.[78910] However, despite similar oncological outcomes, we believe that the surgical management of level I tumor thrombi within the renal vein is different from surgical management of the thrombi within the IVC at <2 cm from the confluence of the renal veins. In the latter situation, extra length is required for milking the thrombus into the renal vein if the wall of vena cava has not been invaded by the tumor. Therefore, the mobilization of the entire kidney is of most importance for the maximal elevation of the renal vein. To ensure clear vision, it is necessary to transect the renal artery early and to avoid parasitic veins that may lead to severe bleeding. However, in situations where the thrombus remains within the renal vein, a limited dissection of the kidney (mobilization of only the lower pole) may be enough to control both renal artery and renal vein thrombi.

It is well-known that vena cava or renal vein thrombi can lead to parasitic veins within the tumors due to limited kidney venous outflow. These parasitic veins lack of normal organization and structure, making them susceptible to injury during dissection or retraction of the tissues.[11] One of the advantages of early ligation of the renal artery with a retroperitoneoscopic approach is the prevention of significant bleeding from these parasitic veins. The rationale for ligation in these circumstances is similar to that for the preoperative embolization of the renal artery in large kidney tumors, which have significant venous obstruction. Troxel and Das reported a case of hand-assisted left LRN with preoperative embolization on a Jehovah's Witness who refused blood transfusion.[12] The authors completed the operation with a blood loss of only 150 cc. In the present report, neither case required blood transfusion despite the large size of both tumors.

Savage and Gill reported the first planned LRN for a level I renal vein tumor thrombus.[13] In this case, the tumor thrombus in the renal vein extended up to, but not proximal to the gonadal vein. The authors performed the operation using a 3-port retroperitoneal approach and noted that the proximal renal vein appeared collapsed and flattened because of the lack of renal outflow, thereby allowing direct visualization of the intramural renal vein thrombus. Consistent with this report, we visualized the renal vein thrombi in both cases, but milking of the tumor thrombi into the renal vein was not possible because of the inadequate elevation of the renal hilum due to limited mobilization of the kidney. For this reason, a transperitoneal approach was required. Later, the same group reported 8 cases with gross renal vein thrombi and mentioned that en bloc removal of the renal vein was achieved in 7 cases.[14] Despite the fact that 1 case required open conversion due to bleeding, the mean operative time was 195 min and the mean estimated blood loss was 353 cc. In all cases, the transection of the renal vein was performed with an endovascular stapler. A report by Steinnerd et al., described 5 cases with level I thrombi and a mean tumor size of 5.5 cm.[15] The authors completed surgery in all cases with a pure transabdominal laparoscopic approach and reported favorable operative times (mean 119.6 min) and estimated blood losses (mean 150 cc) without significant complications. We believe that a pure transperitoneal approach is a valid option for small tumors, but for larger tumors in cases similar to the present report, a “combination technique” may be advantageous in terms of early ligation of the artery. Using a similar rationale, Steinnard et al., chose to use an open technique for the 3 cases in their case series of larger tumors. Similar favorable outcomes were also reported by Guzzo et al., who retrospectively evaluated a total of 37 patients with level I thrombi and a mean tumor diameter of 7.5 cm.[16] Recently, surgeries performed with robotic and laparo-endoscopic single sites (LESS) have also been reported.[1718]

To the best of our knowledge, the present report is the first to describe the use of this technique for the treatment of level I tumor thrombi. However, this technique was initially mentioned by Srivastava et al., for the treatment of T1-T2 renal tumors.[19] The authors in the study treated 10 of 72 patients with a similar technique for their large, right-sided tumors. The authors chose this technique because of the difficulty in using a transperitoneal approach to access the right renal artery in large tumors as opposed to the left-sided tumors, where the renal artery may be clipped at its aortic origin. The authors also noted that the identification of the early branches of the renal artery was technically demanding. We shared the opinion of Srivastava et al., and believed that these maneuvers may lead to tumor embolization or severe bleeding from parasitic vessels in cases with tumor thrombi.