JOURNAL OF ENDOUROLOGY Volume 28, Number 7, July 2014 ª Mary Ann Liebert, Inc. Pp. 819–824 DOI: 10.1089/end.2014.0066

Pure Retroperitoneal Laparoscopic Radical Nephrectomy for Right Renal Masses with Renal Vein and Inferior Vena Cava Thrombus Wenying Wang, MD,1,2 Li Wang, MD,2 Jianfeng Xu, MD, PhD,2 Tamara S. Adams, MS,2 Ye Tian, MD,1 and Wencheng Lv, MD1

Abstract

Purpose: To describe our pure retroperitoneal laparoscopic radical nephrectomy (LRN) with thrombectomy for right renal masses with renal vein (RV) and inferior vena cava (IVC) thrombus. Patients and Methods: Five patients with right renal masses with RV and IVC thrombus underwent pure retroperitoneal LRN. Three patients had a history of abdominal surgery. In one patient with a RV thrombus, the RV was ligated and dissected with Hem-o-lok clips; in four patients with IVC thrombus, the IVC was partially occluded with a laparoscopic vascular clamp and incised distal to its junction with the right RV, and the thrombus was delivered intact. The IVC was closed with a running 3-0 polypropylene suture. Results: Pure retroperitoneal LRN with thrombectomy was successfully performed for all the patients without hand-assisted or open conversion. The mean tumor size was 6.2 cm, and mean thrombus length was 2.8 cm; four thrombi extended 0.6–1.0 cm into the IVC, and the mean operative time was 127 minutes with the average estimated blood loss at 148 mL. The mean hospital stay was 5 days. Histology revealed two renal-cell carcinomas, one angiomyolipoma, one renal pelvic transitional-cell carcinoma, and one renal infarction. All the surgical margins were negative. With a mean follow-up of 35 months, metastatic diseases did not develop in any patient. Conclusions: Despite the technical challenges, pure retroperitoneal LRN for right renal masses with a RV and IVC thrombus is safe and feasible in appropriately selected patients using a retroperitoneal approach. In patients with minimal caval involvement, our surgical approach provided an alternative treatment option, especially when the patients had a history of abdominal surgery. Introduction

L

aparoscopic radical nephrectomy (LRN) has been widely used since its first description by Clayman and colleagues1 in 1990, and with the advancement of surgical skills and improvement of laparoscopic technology, the indications for LRN have greatly expanded during the past two decades. In 1996, McDougall and associates2 reported the first successful case of LRN for renal-cell carcinoma (RCC) with a renal vein (RV) thrombus. To date, pure laparoscopic, handassisted laparoscopic, laparoscopic-assisted, laparoendoscopic single-site (LESS), or robot-assisted radical nephrectomies have been successfully performed on patients with venous thrombi.3–22 Further accumulation of data and longer-term follow-up are needed, however, to confirm the ultimate validation of the safety and efficacy of these cancer treatments.

As we know, the right RV is 2–4 cm long, which is shorter than the left RV. The thrombus in the right RV is more vulnerable to extend into the inferior vena cava (IVC), so the IVC thrombus is more frequently seen in right-sided renal masses than left-sided masses at the time of diagnosis.23 Up to now, about 88 cases of right masses with venous thrombi have received LRN with thrombectomy, but most of them were performed through the transperitoneal approach; only a few cases received pure LRN with the retroperitoneal approach.3–6 To the best of our knowledge, when using the retroperitoneal approach, our study includes the largest number of right renal masses with varying lengths of venous thrombi treated with pure laparoscopic management. In this article, we describe our experience and the technique of RV and IVC thrombectomy during LRN for right renal masses using a retroperitoneal approach.

1

Department of Urology, Beijing Friendship Hospital, Capital Medical University, Beijing, China. Center for Cancer Genomics, Wake Forest University School of Medicine, Winston-Salem, North Carolina. A video demonstrating this technique is available at www.liebertpub.com/end

2

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820 Patients and Methods

From November 2008 to February 2013, five patients with a diagnosis of right renal masses with RV and IVC thrombus received pure LRN using a retroperitoneal approach at our institute. A total of three women and two men with a mean age of 58 years, ranging from 26 to 79 years, were studied. The mean body mass index (BMI) was 24.2 kg/m2 (20.1– 27.3 kg/m2). Three patients had a history of abdominal open surgery—cholecystectomy in two and partial gastrectomy in one. Two patients presented with intermittent gross hematuria, and three showed renal masses during a health screening. Complete serum evaluations including hemoglobin, hematocrit, creatinine, liver function test, and electrolyte tests were within normal limits. Chest radiographs showed no metastasis, and bone scan results were negative. Cystoscopy was performed in two patients without positive findings. CT was used to define the tumor location and vascular extension in all the patients. CT revealed renal masses with RV thrombus in one patient and IVC thrombus in four patients. The thrombus was found to protrude into the IVC 0.6– 1.0 cm beyond the confluence with the IVC. No retroperitoneal lymph nodes were suspected to be involved based on abdominal or pelvic CT imaging. The CT images in four patients are shown (Fig. 1). We decided to proceed with pure retroperitoneal LRN, but hand-assisted or open conversion was ready if technical difficulty was experienced during retroperitoneoscopy. After induction with general anesthesia, the patients were placed in the 90-degree flank position. Because of suspicion of pelvic transitional-cell carcinoma (TCC) in one patient, transurethral resection of the ureteral orifice was performed with the patient in the supine lithotomy position. Then the patient was repositioned and underwent LRN. A four-port pure retroperitoneal laparoscopic approach was used with

FIG. 1. CT images. (A) Renal infarction with renal vein thrombus; (B) renal pelvic transitionalcell carcinoma with inferior vena cava (IVC) thrombus; (C) renal angiomyolipoma with IVC thrombus; (D) renal-cell carcinoma with IVC thrombus. Tip of the thrombus (arrow).

WANG ET AL.

one 12-mm port, one 10-mm port, and two 5-mm ports. The retroperitoneal space was created by finger dissection, and the pneumoretroperitoneum pressure was maintained at 12 to 15 mm Hg. The right renal artery was exposed and ligated with Hem-o-lok clips, and lack of extra renal artery should have been confirmed. For the patient with RV thrombus only, Hem-o-lok clips were used to ligate the RV. The thrombus could not be adequately excised with Hemo-lok clips or an endogastrointestinal anastomosis stapling device despite attempting to gently milk the thrombus proximal toward the kidney in four patients. Therefore, an en bloc tumor thrombectomy with IVC partial control was planned, and open surgical oncologic techniques were replicated purely laparoscopically. The mobilization of the IVC was extended cranially to the upper pole of the kidney and caudally to the lower pole of the kidney to enlarge the working space. Before the IVC was occluded, the lymphatic tissue adjacent to the IVC was removed, and the ureter was also identified and ligated. Intraoperative ultrasonography can be used to define the thrombus margin. A laparoscopic vascular clamp was applied to tangentially occlude the partial IVC through one 12-mm port with the flow preserved through the remaining lumen. The IVC was incised distal to its junction with the right RV with cold cut laparoscopic scissors. The thrombus was clearly visualized and delivered intact. We sutured the IVC contemporarily with the extraction of the IVC thrombus using uninterrupted 3-0 polypropylene sutures, which maintained more than 50% of the original luminal caliber (Fig. 2) (a supplementary video is available at www.liebertpub.com/end). No bleeding was found at the suture line after removal of the laparoscopic vascular clamp. The intact thrombus was completely removed with the en bloc specimen using an Endo catch bag without any thrombus spillage. The specimen was extracted through a suprailiac

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FIG. 2. (A) Inferior vena cava (IVC) was mobilized; (B) a laparoscopic vascular clamp was applied tangentially to occlude the partial IVC; (C) IVC was incised and the thrombus was delivered; (D) IVC was suture repaired with a 3-0 polypropylene suture.

incision, by extension of the suprailiac port site. In one patient, the mobilization of the mid and distal ureter using blunt dissection was needed, so the specimen, including the whole ureter, was extracted. The surgical field was irrigated carefully with sterile water. The retroperitoneal drainage was left in the renal fossa and was removed postoperatively after 48 to 72 hours. The thrombus was invasive to the vascular wall in two patients, and no residual thrombus was noted for all the patients. We defined the operative time from beginning at skin incision to the placing of the final sterile dressing. We calculated intraoperative blood loss based on suction volumes and swab weight. Postoperatively, all the patients were followed up with physical examination, laboratory studies, chest and abdominal imaging every 3 months for the first year, every 6 months for the second year, and then annually thereafter. Results

All the operations were performed successfully without hand-assisted or open conversion. There were no intraoperative and postoperative complications, including pulmonary embolism, postoperative bleeding, pneumonia, or wound infection. The mean thrombus length for all the five patients was 2.8 cm (range 1.8–3.7 cm). The mean operative time was 127 minutes (range 75–160 min). The operative time for transurethral resection of the ureteral orifice and reposition was not included for the patient with suspected pelvic TCC. The mean estimated blood loss was 148 mL (range 20–240 mL). No patients needed blood transfusion. The mean tumor size was 6.2 cm (range 3.5–9.5 cm). The average hospital stay was 5 days (range 4–6 days). In one patient who was 79 years old, the drainage tube was removed postoperatively after 72 hours; the patient was in good condition on postoperative day 5 and discharged on postoperative day 6.

Pathologically, tumors were confirmed to be RCC in two patients with a Fuhrman grade 2 for both, angiomyolipoma (AML) in one, renal pelvic TCC with high histologic grade in one, and renal infarction in one patient. No patients had histologic evidence of lymph node involvement. Renal masses with evidence of perirenal fat invasion were not observed. Three thrombi were floating intraluminally, and two thrombi invaded the vascular wall. All the patients had negative margins. With a mean follow-up of 35 months (10–55 mos), no tumor recurrence or metastasis occurred for all the patients. Patient clinical characteristics, perioperative variables, and outcomes are listed in Table 1. Discussion

LRN has been considered a less invasive alternative to open nephrectomy, and with continuous advances in laparoscopy, it has been proven to be a reliable surgical approach in some complex and challenging surgical cases. LRN for right renal masses in selected patients with RV and IVC thrombus has been reported in 20 studies (Table 2), most of them case report or case series.3–22 To the best of our knowledge, despite having only five patients in our study, when using the retroperitoneal approach, we reported the largest series of right renal masses with RV and IVC thrombus in patients undergoing pure LRN. Both retro- and transperitoneal approaches can be used, although the selection of the approach usually depends on surgeon training and preference. Most cases of LRN with thrombectomy were performed using the transperitoneal approach; only a few small series of patients were reported using the retroperitoneal approach in the literature to date.3–6 The retroperitoneal approach to LRN has been well established as safe and efficacious even for large renal masses and some complex cases.24 The recent published meta-analysis on comparison between retroperitoneal and transperitoneal LRN concluded that the retroperitoneal approach may be faster and equally

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Table 1. Clinical Characteristics, Perioperative Variables, and Postoperative Outcomes of the Patients Variables Sex/age (y) BMI (kg/m2) History of surgery Tumor size (cm) RV or IVC thrombus Thrombus length (cm) Thrombus type Operative time (min) Estimated blood loss (mL) Pathology Fuhrman tumor grade Hospital stay (days) Follow-up (months) Recurrence or metastasis

Patient 1

Patient 2

Patient 3

Patient 4

Patient 5

F/57 25.2 Cholecystectomy 3.5 RV 1.8 Invasive 75 20 Renal infarction N/A 4 10 N/A

F/79 25.7 No 5.5 IVC 2.8 Invasive 130 160 TCC High grade* 6 24 No

F/26 21.1 No 4.2 IVC 2.5 Floating 160 120 AML N/A 4 50 No

M/56 24.6 Gastrectomy 8.1 IVC 3 Floating 130 200 RCC 2 5 38 No

M/73 27.3 Cholecystectomy 9.5 IVC 3.7 Floating 140 240 RCC 2 5 55 No

*According to grading of World Health Organization 2004 for urothelial carcinoma. BMI = body mass index; RV = renal vein; IVC = inferior vena cava; TCC = transitional cell carcinoma; AML = angiomyolipoma; RCC = renal cell carcinoma; N/A = not applicable.

safe compared with the transperitoneal approach.24 Disanto and coworkers3 also regarded the retroperitoneal approach as the ideal approach for treating patients with right renal masses with IVC thrombus. When using the retroperitoneal approach, we thought it yielded more direct and quicker access to the hilum and control of the renal artery early; it afforded easier access to the IVC with no need to mobilize the colon or duodenum or retract the liver or bowel. In addition, when the patient had a history of abdominal surgery, the retroperitoneal approach would be more appropriate. Three patients had a history of abdominal surgery in our study, so we chose to perform LRN based on our experience of pure LRN for left RCC with differential extensions of the RV thrombus using the retroperitoneal approach.25

To date, different laparoscopic techniques have been reported in patients with RV thrombi. Pure or hand-assisted LRN can usually be successfully performed in most of the cases, and the right RV can be ligated and dissected by milking the thrombus back to the kidney.5–13Although there is widespread use of LESS technology, only two reports of LESS radical nephrectomy with RV thrombectomy have been reported,14,15 and it was safe and feasible for right tumors with RV thrombus in selected patients. Liss colleagues15 also compared LESS with multiport laparoscopic for radical nephrectomy and RV thrombus. Some benefits with less pain and hospital stay for LESS were demonstrated. Tumor thrombi at the level of the IVC represents a technical challenge, especially for higher levels of IVC thrombi, which

Table 2. Reports of Laparoscopic Radical Nephrectomy for Right Masses with Renal Vein and Inferior Vena Cava Thrombus Investigator 12

Henderson et al. Sundaram et al.8 Kovac et al.17 Kapoor et al.9 Varkarakis et al.18 Hoang et al.19 Kopp et al.14 Liss et al.15 Abaza20 Lee et al.21 Guzzo et al.11 Steinnerd et al.10 Fernandez-Pello et al.22 Martin et al.7 Romero et al.16 Hammond et al.13 Desai et al.5 Xu et al.6 S1ojewski et al.4 Disanto et al.3

No. patients

Treatment

Approach

RV or IVC

Pathology

9 1 1 6 4 7 1 12 5 1 16 3 1 6 1 6 5 1 1 1

Hand-assisted Hand-assisted Hand-assisted Hand-assisted Lap-assisted Lap-assisted LESS LESS Robotic Robotic Pure Pure Pure Pure Pure Pure Pure Pure Pure Pure

Trans Trans Trans Trans Trans Trans Trans Trans Trans Trans Trans Trans Trans Trans Trans N/A Trans and retro Retro Retro Retro

RV IVC IVC RV IVC IVC RV RV IVC IVC RV RV IVC RV(4), IVC(2) IVC RV RV RV IVC IVC

RCC RCC RCC RCC RCC RCC RCC RCC RCC RCC with rhabdoid cell-type RCC, sarcomatoid RCC AML RCC PNET RCC, rhabdoid cell-type RCC, sarcomatoid Wilms tumor RCC Poorly differentiated RCC

RV = renal vein; IVC = inferior vena cava; RCC = renal-cell carcinoma; LESS = laparoendoscopic single-site; AML = angiomyolipoma; PNET = primitive neuroectodermal tumor; N/A = not available; trans = transperitoneal; retro = retroperitoneal.

LRN FOR RIGHT RENAL MASSES WITH RV AND IVC THROMBUS

needs duplication of some measures practiced in open surgery. The first case of pure LRN and IVC thrombectomy was reported in 2006 by Romero and associates16 using a transperitoneal approach, with the thrombus extended 3 cm above the RV. Series of hand-assisted LRN and entirely LRN for right masses with IVC thrombi have also been reported.7,17,18 Some investigators performed the clinical cases with the thrombus projecting 1cm to 2 cm into the IVC using a hand-assisted laparoscopic approach, and this approach decreased the operative time and increased intraoperative blood loss, but it also facilitated rapid control of major venous hemorrhage.17,18 Hoang et al19 also successfully performed laparoscopic-assisted radical nephrectomy in patients with higher IVC tumor thrombi. When using the retroperitoneal approach, only two cases of LRN with IVC thrombectomy were reported by Disanto and colleagues3 and S1ojewski and coworkers,4 respectively. With the expanding use of robotic technology, two reports have demonstrated that robot-assisted radical nephrectomy can be safe and effective for right tumors with IVC thrombi in well-selected patients, but it necessitated skilled laparoscopists with extensive experiences of robotic renal surgery. The authors also thought that robotic IVC thrombectomy remained technical challenging and should not be embarked on lightly.20,21 In our study, the right RV can be controlled by Hem-o-lok clips in one patient with a RV thrombus. For the four patients with IVC thrombus, the thrombus could not be milked back into the right RV completely despite attempting to gently milk the thrombus toward the kidney. We had to use the laparoscopic vascular clamp to occlude the IVC partially, but crossclamping of the IVC and control of all the lumbar veins was not necessary. We used the split style of vascular clamp. No trocar needed to be occupied after the clamp was applied on the IVC, which was different from the clamp used in the literature.7,8 Safety should be ensured for these high-risk patients. Significant bleeding will occur if the clamp becomes dislodged during LRN, so we sutured the IVC contemporarily with the extraction of the IVC thrombus. Overall mean estimated blood loss was less than 150 mL, and no blood transfusion was needed in our patients, which provided a potential advantage for pure LRN and thrombectomy. The advantage of pure LRN included less operative time, less blood loss, and less hospital stay. The operative time, intraoperative blood loss, and hospital stay in our study were similar or even less than that in some reports in the literature.15–17 Pulmonary embolisms with thrombosis and carbon dioxide embolism are a critical concern, but to date no such cases were reported as a result of LRN with thrombectomy.3–22 To perform pure LRN safely, optimized exposure with careful dissection and identification of the distal extent of the thrombus margin will ensure the accurate application of the laparoscopic vascular clamp. The atraumatic bowel grasper and laparoscopic forceps are both helpful for determining the margin for venous ligation. In addition, laparoscopic ultrasonography can be used to confirm the location of the tip of the thrombus, 9,17 which was used in three of our patients. Surgery will be more difficult for patients with larger tumors and higher levels of thrombi. Steinnerd and colleagues10 excluded more than 10 cm of the primary renal tumor to ensure that LRN can be safely performed for patients with a RV thrombus. Hoang and coworkers19 reported that the patients

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with smaller right renal tumors (< 8 cm) and BMI < 30 were ideal candidates for laparoscopic-assisted radical nephrectomy and IVC thrombectomy. Based on our experience, the transperitoneal approach is more appropriate for a larger tumor and higher BMI, but for patients with a history of abdominal surgery, abdominal adhesion would be serious and affect the surgery, so the retroperitoneal approach would be an alternative. Early hand-assisted or open conversion should be strongly considered in case of intraoperative uncontrolled hemorrhage, hilar adenopathy, positive margin, or failure to progress; the rate for open conversion was 2.7% to 16% in some reports.9,11 Despite the technical challenges, no hand-assisted or open conversion was needed in our study. The long-term cancer control outcome is another major concern for LRN with thrombectomy. Only 88 patients with a right renal mass and a venous thrombus (23 cases with IVC thrombus) underwent LRN in the literature, however; longterm cancer control outcomes were not shown in most of the patients.3–22 The study of Martin and associates7 showed that two patients had pulmonary and brain metastasis 2 months postoperatively and six patients had no evidence of disease with a mean follow-up of 32 months. Recurrence or metastatic diseases did not develop in any patient with a mean follow-up of 35 months for our patients with renal tumors. Long-term oncologic outcomes should be demonstrated in a pooling of patients from multiple collaborative centers, and randomized studies are needed. RCC is the most frequently reported cause of venous thrombi. Compared with the extension of RCC into the venous system, extensions of AML and TCC into the venous system are rare. There were 48 cases and fewer than 30 cases reported, respectively.22,26 In addition, a renal infarction with the RV thrombus is extremely rare. We reported the first case of such an occurrence. To the best of our knowledge, we first performed pure LRN and thrombectomy for patients with RV and IVC thrombus caused by TCC, AML, and renal infarction using the retroperitoneal approach. In most patients with RCC, the thrombus extending into the IVC will not invade the venous wall,10 which was true in our patients with RCC. The thrombus in patients with TCC and renal infarction, however, invaded the vascular wall in our cases. Admittedly, there are some limitations for our study. First, we only performed LRN with thrombectomy in well-selected patients, in which the length of the thrombus extending into IVC did not exceed 1 cm. Second, although the results are encouraging, only five patients received LRN with this technique; a much larger series of patients is needed to confirm the safety and efficiency with our technique. Finally, different tumors were included in our study, but we proved that our technique can be applied in patients with different kinds of renal tumors and diseases with venous thrombus. Despite the limitations of this study, a pure retroperitoneal approach may enable us include a minimal IVC thrombus as the relative indications for LRN. Conclusions

We demonstrate the safety and feasibility of patients with right renal masses with minimal IVC thrombi undergoing pure LRN through the retroperitoneal approach in detail. It is safe and efficacious for well-selected patients. In patients with minimal caval involvement, especially when the patient has a

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history of abdominal surgery, our surgical approach provided an alternative treatment option. Early hand-assisted and open conversion should be performed whenever necessary, however. Safety, efficacy, and longer-term cancer control are requisite to be confirmed in further accumulations of data. Disclosure Statement

No competing financial interests exist. References

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17. Kovac JR, Luke PP. Hand-assisted laparoscopic radical nephrectomy in the treatment of a renal cell carcinoma with a level II vena cava thrombus. Int Braz J Urol 2010;36: 327–331. 18. Varkarakis IM, Bhayani SB, Allaf ME, et al. Laparoscopicassisted nephrectomy with inferior vena cava tumor thrombectomy: Preliminary results. Urology 2004;64:925– 929. 19. Hoang AN, Vaporcyian AA, Matin SF. Laparoscopy-assisted radical nephrectomy with inferior vena caval thrombectomy for level II to III tumor thrombus: A single-institution experience and review of the literature. J Endourol 2010;24: 1005–1112. 20. Abaza R. Initial series of robotic radical nephrectomy with vena caval tumor thrombectomy. Eur Urol 2011;59: 652–656. 21. Lee JY, Mucksavage P. Robotic radical nephrectomy with vena caval tumor thrombectomy: Experience of novice robotic surgeons. Korean J Urol 2012;53:879–882. 22. Fernandez-Pello S, Gonzalez Rodriguez I, Villamil LR, et al. Laparoscopic management of right renal angiomyolipoma with involvement of the inferior vena cava: Case report and review of the literature. Scand J Urol 2013;47:340–344. 23. Katkoori D, Murugesan M, Ciancio G, Soloway MS. Tumor thrombus involving the inferior vena cava in renal malignancy: Is there a difference in clinical presentation and outcome among right and left side tumors? Int Braz J Urol 2009;35:652–657. 24. Fan X, Xu K, Lin T, et al. Comparison of transperitoneal and retroperitoneal laparoscopic nephrectomy for renal cell carcinoma: A systematic review and meta-analysis. BJU Int 2013;111:611–621. 25. Wang W, Xu J, Adams TS, et al. Pure retroperitoneal laparoscopic radical nephrectomy for left renal cell carcinoma with differential extensions of level I renal vein tumor thrombus. J Endourol 2014;28:312–317. 26. Tseng YS, Chen KH, Chiu B, et al. Renal urothelial carcinoma with extended venous thrombus. South Med J 2010;103:813–814.

Address correspondence to: Wencheng Lv, MD Department of Urology Beijing Friendship Hospital Capital Medical University 95 YongAn Road, Xicheng District Beijing 100050 China E-mail: [email protected]

Abbreviations Used AML ¼ angiomyolipoma BMI ¼ body mass index CT ¼ computed tomography IVC ¼ inferior vena cava LESS ¼ laparoendoscopic single-site LRN ¼ laparoscopic radical nephrectomy RCC ¼ renal-cell carcinoma RV ¼ renal vein TCC ¼ transitional-cell carcinoma

Pure retroperitoneal laparoscopic radical nephrectomy for right renal masses with renal vein and inferior vena cava thrombus.

To describe our pure retroperitoneal laparoscopic radical nephrectomy (LRN) with thrombectomy for right renal masses with renal vein (RV) and inferior...
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