Urology Annals
About UA | Search | Ahead of print | Current Issue | Archives | Instructions | Online submissionLogin 
Urology Annals
  Editorial Board | Subscribe | Advertise | Contact
Users Online: 75   Home Print this page  Email this page Small font size Default font size Increase font size

Table of Contents
Year : 2019  |  Volume : 11  |  Issue : 4  |  Page : 353-357  

The incidence and pattern of renal cell carcinoma recurrence after robotic partial nephrectomy

Department of Urology, West Virginia University, Morgantown, West Virginia, USA

Date of Submission22-Sep-2018
Date of Acceptance08-Apr-2019
Date of Web Publication9-Oct-2019

Correspondence Address:
Dr. Mohamad W Salkini
One Medical Center Dr., P.O.Box : 9251, Morgantown, WV 26506
Login to access the Email id

DOI: 10.4103/UA.UA_134_18

PMID: 31649452

Rights and Permissions

Background: Robotic partial nephrectomy (RPN) is a rapidly growing treatment for small renal mass (SRM). In fact, RPN has shown good functional and oncologic outcome. In this manuscript, we are reporting on the incidence and pattern of recurrence of renal cell carcinoma (RCC) treated with RPN.
Patients and Methods: We reviewed prospectively collected data of patients who underwent RPN between September 2009 and March 2018. We selected patients with final pathologic diagnosis of RCC after the resection of their SRM. We described the incidence and pattern of recurrence in the patients who had it.
Results: A total of 335 patients with SRM underwent RPN. We found 269 patients to have RCC on the final pathologic evaluation of the SRM. Eight cases of recurrence were found with a recurrence rate of 2.9% after the mean follow-up period of 31 months (range 18–72). The pattern of recurrence presented as follows: two patients (0.7%) had trocar site recurrence (TSR), one patient (0.37%) had locoregional recurrence, and three patients (1.1%) had recurrence of the disease at the resection bed. Two patients (0.7%) developed second primary tumor in the other kidney. No cancer-related mortality occurred during the follow-up period.
Conclusion: TSR, locoregional recurrence, tumor bed recurrence, and contralateral tumor development are observed patterns of RCC recurrence after RPN. Recurrence was seen in up to 72 months. RPN provides great cancer control and high cure rate when utilized to treat RCC presenting as SRM.

Keywords: Nephron-sparing surgery, renal cell carcinoma, robotic partial nephrectomy, small renal mass

How to cite this article:
Salkini MW, Idris N, Lamoshi AR. The incidence and pattern of renal cell carcinoma recurrence after robotic partial nephrectomy. Urol Ann 2019;11:353-7

How to cite this URL:
Salkini MW, Idris N, Lamoshi AR. The incidence and pattern of renal cell carcinoma recurrence after robotic partial nephrectomy. Urol Ann [serial online] 2019 [cited 2020 Jul 14];11:353-7. Available from: http://www.urologyannals.com/text.asp?2019/11/4/353/266962

   Introduction and Objective Top

Renal cell carcinoma (RCC), with steadily increasing incidence, has become the third most commonly diagnosed urologic cancer in the United States.[1] This is related to the increase in the utilization of diagnostic cross-sectional imaging and detection of incidental small renal masses (SRMs), leading to stage migration of the disease.[2],[3] Surgical resection has always been the treatment of choice for localized RCC.[4],[5],[6] Nephron-sparing surgery (NSS) for RCC, when technically feasible, is proven to be of equal oncologic outcome to radical nephrectomy.[4] Multiple studies had demonstrated acceptable oncologic and improved functional outcomes when NSS was utilized to treat SRM.[5] Besides, decreased cardiovascular morbidity with preservation of renal function has become a known benefit of the NSS.[6]

Robotic partial nephrectomy (RPN) has an established role in the treatment of RCC with an oncologic outcome that is comparable to open approach.[7] RPN established its niche as minimally invasive approach to treat SRM since pure laparoscopic approach has been difficult to adopt due to its long, steep learning curve.[7] The da Vinci ® robotic surgical system improves the dexterity, increases visualization, and filters the tremor of the operating surgeon. It also enhances ergonomic setting to boost the surgeon's personal comfort.[8] The adoption of the robotic technique in NSS increased, leading to growth in experience with RPN to treat SRM.[7],[8] The technique and both functional and oncologic outcome of RPN were replicated by multiple authors from different centers.[9],[10] The 5-year cancer-free survival after robotic, laparoscopic, and open NSS for malignant renal masses was reported to be around 91%.[11] RPN was adopted in our institute since September 2009 as the treatment of choice for SRM. In this article, our aim is to report on the oncologic outcome and describe the recurrence pattern of RCC in patients with RCC-treated RPN at our institute.

   Patients and Methods Top

We reviewed, with IRB approval, prospectively collected data of the patients who underwent RPN for solid and cystic renal mass. We studied the medical record of patients with final diagnosis of any variant of RCC to identify patients who had recurrence of the disease. From September 2009 to March 2018, RPN was utilized routinely to treat patients with SRM (<4 cm) and selectively in the treatment in larger mass (4–7 cm) at our institute. The indication for RPN was either enhancing solid renal mass, or cystic renal mass classified as Bosniak IIF, III or IV.[12] RENAL nephrometry, first described by Kutikov and Uzzo, was used to guide our decision to perform partial nephrectomy. The score is built on five anatomical features of the renal mass [Table 1]. Four out of the five components are scored on a 1, 2, or 3. The fifth indicates whether the tumor is anterior or posterior.[13] RPN was done transperitoneally with mobilization of the colon medially. The renal hilum was isolated, and the tumor was exposed and then resected under variable warm ischemia time (WIT) ranging from 0 to 34 min. Off-clamp RPN was adopted in certain cases with the technique described by Lamoshi and Salkini.[14] Tumor resection was achieved according to the standard technique.[15] Hilar clamping, when utilized, was achieved using bulldog clamps or laparoscopic Satinsky clamp according to the situation and complexity of the hilum. After the resection, the tumor was placed in all the cases in Endo Catch™ specimen pouch. Renorrhaphy was initially performed according to the standard technique.[15] However, we modified the technique by eliminating the closure of the collecting system and that shortened the WIT in the last 225 cases utilizing the technique described by Williams et al.[16] All specimens were analyzed by dedicated uropathologists. The Fuhrman Grade (FG) was utilized for grading of the tumors.[2],[3] A positive surgical margin (PSM) was defined as the extension of tumor to the inked surface of the resected specimen on the final microscopic pathologic evaluation. Every patient was admitted to the hospital after surgery for a minimum of 24 h and had continuous vital sign monitoring during the first 2-h stay. They also had laboratory testing of basic metabolic panel and complete blood count. All patients were followed using computed tomography scan or magnetic resonance imaging of the abdomen and pelvis with contrast media. The first surveillance imaging was performed 6 months after surgery and at variable period according to the risk of recurrence.
Table 1: R.E.N.A.L nephrometry score

Click here to view

   Results Top

We studied 269 (81%) patients with a final diagnosis of RCC out of the 335 patients who underwent RPN at our institute. The mean age of the patients was 67 years (ranging from 28 to 81), and 183 were male (58%) as in [Table 2].
Table 2: Patient Demographics

Click here to view

The mean RENAL nephrometry score for the resected masses was 6.4 (ranging from 4 to 10). The pathological distribution of the tumors was as follows: 192 (71%) patients had clear cell RCC, 50 (19%) patients had papillary RCC, 16 (6%) patients had chromophobe RCC, and 11 (4%) patients had unclassified RCC. Forty-five (17%) patients had FG 1 tumor, 187 (70%) patients had Grade 2 tumors, and 37 (14%) patients had Grade 3 tumors. None of the patients had Grade 4 tumors. The tumors were distributed into 215 (80%) T1a, 42 (16%) T1b, and 12 (4%) T3a. Tumor characteristics are displayed in [Table 3].
Table 3: Tumor characteristics

Click here to view

Two patients (0.7%) with malignant tumors had positive margin in the final pathology. The first positive margin was T1a, clear cell RCC, and FG 1. The second margin was T1b, papillary RCC, and FG 2. Tumor was violated in 11 cases during the surgery (4%), 7 patients (63%) of them were cystic clear cell RCC G1, and one patient (9%) had papillary RCC, FG 2, and T1b tumor. The remaining 3 (27%) violations happened in solid clear cell RCC, FG 2, and T1a tumors.

During the mean follow-up period of 39 months (ranging 6–96), we identified 8 (2.9%) cases of RCC recurrence, as in [Table 2]. The average lag time from the RPN and recurrence was 31 months (18–72). The pattern of recurrence presented as follows [Table 4]: two patients (0.7%) had trocar site recurrence (TSR) [Figure 1], one patient (0.37%) had locoregional recurrence with infiltration of the disease in the perinephric fat and/or lymph nodes [Figure 2] and [Figure 3], and three patients (1.1%) had recurrence of the disease at the resection bed [Figure 4]. Two patients (0.7%) developed second primary tumor in the other kidney. No cancer-related mortality occurred during the follow-up period.
Table 4: Patient who had RCC recurrence after RPN and the type of recurrence

Click here to view
Figure 1: (a and b) Trocar site recurrence

Click here to view
Figure 2: Locoregional recurrence

Click here to view
Figure 3: Locoregional recurrence

Click here to view
Figure 4: Recurrence at the tumor bed

Click here to view

   Discussion Top

RPN using the da Vinci ® Robotic Surgical System (Intuitive Surgical ®, Sunnyvale, Calif) is one of the fastest growing forms of MIS in the US Despite safety concerns. RPN has become the treatment of choice for SRM as it is continuously showing outstanding oncologic outcome, and at the same time, maintaining good renal function.[15] In fact, the feasibility and safety of the technique have been demonstrated by many authors.[15],[16] It was proven that the required skills for robotic approach may be gained faster than what is needed in the classical laparoscopic skills.[17],[18]

This study describes the nature and locations of recurrence of clinically T1, RCC treated with RPN. Peyronnet et al. proved in his multicenter analysis of 1800 partial nephrectomies that RPN has superior oncologic outcome compared to open and laparoscopic approach.[19] However, most of the other studies were unable to show any oncologic difference.[10],[18] We were able to demonstrate comparable oncologic outcome to what has been published in the literature about RPN.[10],[18],[19] The recurrence rate was 2.9% in our study with statistically acceptable sample size of 269. The tumor variants, stage, and grade was found to be similar to what has been published in the literature.[10],[18],[19] We, in this study, report on a single-center solo surgeon (MWS) experience with RPN in the treatment of RCC. That, in fact, enabled us to avoid variability in technique and instrumentation and account for the learning curve. However, it makes it fall into the trap of reporting and selection bias. We had a similar period of follow-up compared to other RPN series with almost similar rate of recurrence when compared to other studies as eight patients developed recurrence out of 269 patients with RCC treated with RPN (2.9%). Peyronnet et al. reported a recurrence rate of 5.5% in his multi-institutional data.[19] The main difference is that our data are derived from single-surgeon performance that may explain the lower rate of positive margin and recurrence. Cleveland clinic group reported 11% of recurrence in their hybrid cases of robotic, laparoscopic, and open partial nephrectomy.[11] In this study, we described neglected pattern of RCC recurrence after RPN, that is, TSR with an incidence rate of 0.7%. TSR is underreported in both RPN and laparoscopic partial nephrectomy. We found few reports of TSR in laparoscopic radical nephrectomy and hand-assisted laparoscopic radical nephrectomy.[20],[21] In 2008, Masterson and Russo from Memorial Sloan Kettering Cancer Center reported on a case of combined locoregional and trocar site seeding after laparoscopic partial nephrectomy.[22] However, we found both types of recurrences in different patients. The etiology of TSR is likely to be multifactorial, involving tumor biology, local wound and general host immune processes, gas ambiance, and surgical factors. Similar factors are likely to be involved in the etiology of intraperitoneal dissemination, which can occur during both laparoscopic and open surgery.[20],[21],[22] In fact, Song et al. reported for the first TSR involving the camera trocar in robotic surgery after partial nephrectomy.[23] We reported in our series two cases. The first case of TSR was involving the robotic 8-mm metal trocar and the second was involving the assistant trocar. Interestingly, our second case presented 7 years after the surgery. None of the TSR was the camera trocar or tumor excision site. The risk of locoregional recurrence after laparoscopic and open surgery is well known in cancer literature, and it is well reported in Gynecology and Surgical Oncology.[24] Our findings showed that high grade, larger tumor, and papillary types are the surrogate with recurrence. This was compatible with what has been reported in the literature.[11],[20],[21],[22],[23]

We found only two cases of recurrence at the resection bed, and that echoes what has been published in the literature.[11] Positive resection margin, tumor violation during surgery was not associated with recurrence, contrary to what has been reported by Petros et al. in their large group long-term follow-up.[25] We had low number of PSM making it difficult to draw statistical conclusion. This study represents one large single center and surgeon experience with RPN, with acceptable length of follow-up. We still recommend longer follow-up and encourage more reporting on the outcome of RPN.

   Conclusion Top

RPN yielded low rate of RCC recurrence at our institute. Tumors with Fuhrman histologic Grade ≥3, larger tumors ≥4 cm, and tumors with local invasion T3 tumors are more likely to recur. Papillary type RCC was found to be surrogate with recurrence. Positive margin and violation of the tumor during resection did not translate into recurrence in our series.

Financial support and sponsorship


Conflicts of interest

There are no conflicts of interest.

   References Top

Hollingsworth JM, Miller DC, Daignault S, Hollenbeck BK. Rising incidence of small renal masses: A need to reassess treatment effect. J Natl Cancer Inst 2006;98:1331-4.  Back to cited text no. 1
Lipworth L, Tarone RE, McLaughlin JK. The epidemiology of renal cell carcinoma. J Urol 2006;176:2353-8.  Back to cited text no. 2
Chow WH, Linehan WM, Devesa SS. Re: Rising incidence of small renal masses: A need to reassess treatment effect. J Natl Cancer Inst 2007;99:569-70.  Back to cited text no. 3
Campbell SC, Novick AC, Belldegrun A, Blute ML, Chow GK, Derweesh IH, et al. Guideline for management of the clinical T1 renal mass. J Urol 2009;182:1271-9.  Back to cited text no. 4
Liss MA, Wang S, Palazzi K, Jabaji R, Patel N, Lee HJ, et al. Evaluation of national trends in the utilization of partial nephrectomy in relation to the publication of the American urologic association guidelines for the management of clinical T1 renal masses. BMC Urol 2014;14:101.  Back to cited text no. 5
Miller DC, Schonlau M, Litwin MS, Lai J, Saigal CS; Urologic Diseases in America Project. Renal and cardiovascular morbidity after partial or radical nephrectomy. Cancer 2008;112:511-20.  Back to cited text no. 6
Gohil R, Ahmed K, Kooiman G, Khan MS, Dasgupta P, Challacombe B. Current status of robot-assisted partial nephrectomy. BJU Int 2012;110:1602-6.  Back to cited text no. 7
Wang L, Lee BR. Robotic partial nephrectomy: Current technique and outcomes. Int J Urol 2013;20:848-59.  Back to cited text no. 8
Chang KD, Abdel Raheem A, Kim KH, Oh CK, Park SY, Kim YS, et al. Functional and oncological outcomes of open, laparoscopic and robot-assisted partial nephrectomy: A multicentre comparative matched-pair analyses with a median of 5 years' follow-up. BJU Int 2018;122:618-26.  Back to cited text no. 9
Omidele OO, Davoudzadeh N, Palese M. Trifecta outcomes to assess learning curve of robotic partial nephrectomy. JSLS 2018;22. pii: e2017.00064.  Back to cited text no. 10
Mouracade P, Kara O, Maurice MJ, Dagenais J, Malkoc E, Nelson RJ, et al. Patterns and predictors of recurrence after partial nephrectomy for kidney tumors. J Urol 2017;197:1403-9.  Back to cited text no. 11
Israel GM, Bosniak MA. An update of the bosniak renal cyst classification system. Urology 2005;66:484-8.  Back to cited text no. 12
Kutikov A, Uzzo RG. The R.E.N.A.L. Nephrometry score: A comprehensive standardized system for quantitating renal tumor size, location and depth. J Urol 2009;182:844-53.  Back to cited text no. 13
Lamoshi AY, Salkini MW. Off-clamp robotic partial nephrectomy: Technique and outcome. Urol Ann 2015;7:226-30.  Back to cited text no. 14
[PUBMED]  [Full text]  
Rogers CG, Singh A, Blatt AM, Linehan WM, Pinto PA. Robotic partial nephrectomy for complex renal tumors: Surgical technique. Eur Urol 2008;53:514-21.  Back to cited text no. 15
Williams RD, Snowden C, Frank R, Thiel DD. Has sliding-clip renorrhaphy eliminated the need for collecting system repair during robot-assisted partial nephrectomy? J Endourol 2017;31:289-94.  Back to cited text no. 16
Caruso RP, Phillips CK, Kau E, Taneja SS, Stifelman MD. Robot assisted laparoscopic partial nephrectomy: Initial experience. J Urol 2006;176:36-9.  Back to cited text no. 17
Phillips CK, Taneja SS, Stifelman MD. Robot-assisted laparoscopic partial nephrectomy: The NYU technique. J Endourol 2005;19:441-5.  Back to cited text no. 18
Peyronnet B, Seisen T, Oger E, Vaessen C, Grassano Y, Benoit T, et al. Comparison of 1800 robotic and open partial nephrectomies for renal tumors. Ann Surg Oncol 2016;23:4277-83.  Back to cited text no. 19
Chen YT, Yang SS, Hsieh CH, Wang CC. Hand port-site metastasis of renal-cell carcinoma following hand-assisted laparoscopic radical nephrectomy: Case report. J Endourol 2003;17:771-5.  Back to cited text no. 20
Dhobada S, Patankar S, Gorde V. Case report: Port-site metastasis after laparoscopic radical nephrectomy for renal-cell carcinoma. J Endourol 2006;20:119-22.  Back to cited text no. 21
Masterson TA, Russo P. A case of port-site recurrence and locoregional metastasis after laparoscopic partial nephrectomy. Nat Clin Pract Urol 2008;5:345-9.  Back to cited text no. 22
Song JB, Tanagho YS, Kim EH, Abbosh PH, Vemana G, Figenshau RS. Camera-port site metastasis of a renal-cell carcinoma after robot-assisted partial nephrectomy. J Endourol 2013;27:732-9.  Back to cited text no. 23
Paolucci V, Schaeff B, Schneider M, Gutt C. Tumor seeding following laparoscopy: International survey. World J Surg 1999;23:989-95.  Back to cited text no. 24
Petros FG, Metcalfe MJ, Yu KJ, Keskin SK, Fellman BM, Chang CM, et al. Oncologic outcomes of patients with positive surgical margin after partial nephrectomy: A 25-year single institution experience. World J Urol 2018;36:1093-101.  Back to cited text no. 25


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

  [Table 1], [Table 2], [Table 3], [Table 4]


    Similar in PUBMED
   Search Pubmed for
   Search in Google Scholar for
 Related articles
    Access Statistics
    Email Alert *
    Add to My List *
* Registration required (free)  

  In this article
   Introduction and...
     Patients and Methods
    Article Figures
    Article Tables

 Article Access Statistics
    PDF Downloaded108    
    Comments [Add]    

Recommend this journal