|Year : 2015 | Volume
| Issue : 1 | Page : 72-77
Comparison of surgical, functional, and oncological outcomes of open and robot-assisted partial nephrectomy
Ugur Boylu, Cem Basatac, Umit Yildirim, Fikret F Onol, Eyup Gumus
Department of Urology, Section of Uro-Oncology, Umraniye Teaching Hospital, Istanbul, Turkey
|Date of Submission||11-Aug-2014|
|Date of Acceptance||28-Sep-2014|
|Date of Web Publication||24-Dec-2014|
Department of Urology, Umraniye Teaching Hospital, Umraniye, 34766 Istanbul
Source of Support: None, Conflict of Interest: None
Background: We aimed to compare the surgical, oncological, and functional outcomes of robot-assisted partial nephrectomy (RAPN) with open partial nephrectomy (OPN) in the management of small renal masses. Materials and Methods: Between 2009 and 2013, a total of 46 RAPN patients and 20 OPN patients was included in this study. Patients' demographics, mean operative time, estimated blood loss (EBL), warm ischemia time (WIT), length of hospital stay, pre- and post-operative renal functions, complications and oncological outcomes were recorded, prospectively. Results: Mean tumor size was 4.04 cm in OPN group and 3.56 cm in RAPN group (P = 0.27). Mean R.E.N.A.L nephrometry score was 6.35 in OPN group and 5.35 in RAPN group (P = 0.02). The mean operative time was 152 min in OPN group and 225 min in RAPN group (P = 0.006). The mean EBL in OPN and RAPN groups were 417 ml and 268 ml, respectively (P = 0.001). WIT in OPN group was significantly shorter than RAPN group (18.02 min vs. 23.33 min, P = 0.003). The mean drain removal time and the length of hospital stay were longer in OPN group. There were no significant differences in terms of renal functional outcomes and postoperative complications between groups. Conclusion: Minimally invasive surgical management of renal masses with RAPN offers better outcomes in terms of EBL and length of stay. However, the mean operative time and WIT were significantly shorter in OPN group. RAPN is a safe and effective minimally invasive alternative to OPN in terms of oncological and functional outcomes.
Keywords: Kidney cancer, nephron sparing surgery, partial nephrectomy, robot
|How to cite this article:|
Boylu U, Basatac C, Yildirim U, Onol FF, Gumus E. Comparison of surgical, functional, and oncological outcomes of open and robot-assisted partial nephrectomy. J Min Access Surg 2015;11:72-7
|How to cite this URL:|
Boylu U, Basatac C, Yildirim U, Onol FF, Gumus E. Comparison of surgical, functional, and oncological outcomes of open and robot-assisted partial nephrectomy. J Min Access Surg [serial online] 2015 [cited 2019 Jun 25];11:72-7. Available from: http://www.journalofmas.com/text.asp?2015/11/1/72/147699
| ¤ Introduction|| |
Kidney cancer is the 3 rd most common urological malignancy and is expected to account for %3 of all cancer related deaths.  Historically, standard treatment for the renal masses of all sizes was radical nephrectomy.  However, radical nephrectomy is associated with increased prevalence of end-stage renal disease and cardiac events.  Instead, partial nephrectomy has similar oncological outcomes when compared with a radical approach and currently, it is the standard treatment of the small renal tumors. 
With the advancing technology, laparoscopic partial nephrectomy (LPN) has gained popularity. Reasons for wide acceptance include operative advantages such as reduced blood loss and shorter hospital stay, and decrease incisional morbidity.  However, LPN is a challenging surgical procedure due to the necessity of intracorperal suturing. Therefore, it has a steep learning curve. More recently, robot-assisted partial nephrectomy (RAPN) was introduced as a minimally invasive alternative to open and LPN. The robotic systems have significant advantages over conventional laparoscopy such as three-dimensional visualization, increased magnification, and better depth perception. Nevertheless, it requires an experienced bedside assistant who has advanced laparoscopic skills in order to assist the primary surgeon. In the current literature, several studies have shown that RAPN is an effective and a reliable treatment for the renal masses smaller than 4 cm and whenever technically feasible at any dimension. , At present, comparative analysis of RAPN and open partial nephrectomy (OPN) is lacking. In this study, we aimed to compare surgical, functional, and oncological outcomes of RAPN and OPN in order to determine the current role of these two approaches in the management of small renal masses.
| ¤ Materials and methods|| |
Following the institutional review board approval, a total of 46 patients who underwent RAPN and 20 patients who underwent OPN was included in this study between 2009 and 2013. Preoperative evaluation included medical history, physical examination, routine laboratory studies, including serum creatinine and urinalysis, chest X-ray, and abdominal computerized tomography (CT). Tumor size was reported as the largest single dimension of the lesion as measured on the CT. Pathological staging was performed according to the 2009 IUCC/American Joint Committee on Cancer tumor-node-metastasis staging system.  All tumors were graded according to R.E.N.A.L. nephrometry score.  Patients' demographics, mean operative time, estimated blood loss (EBL), warm ischemia time (WIT), length of hospital stay, pre- and post-operative renal functions, complications, and oncological outcomes were recorded prospectively. Preoperative creatinine levels and estimated glomerular filtration rates (eGFR) calculated with the Modification of Diet and Renal Disease  formula were compared with the postoperative creatinine and eGFR levels. Tumors that were excised under cold ischemia using ice slush, patients with a solitary kidney, multifocal tumors, patients with radiological evidence of locally advanced disease, patients with incomplete records or follow-up <12 months were excluded. All complications within 30 days of the procedure were recorded prospectively and graded based on the modified Clavien-Dindo classification system. 
All statistical analyses were performed using SPSS Statistics version 20 (IBM, Armonk, NY, USA) software. Descriptive statistics were analyzed using 2-sample t-test, and Chi-square test was applied for categorical variables. When normality assumptions are not satisfied for any one or both of groups, the equivalent nonparametric Mann-Whitney U or Wilcoxon Rank Sum Test were used as appropriate. Before and after responses of an outcome within group comparison was analyzed using with paired sample t-test. The confidence interval was taken 95%, and a P < 0.05 was considered statistically significant.
Robotic Partial Nephrectomy
A five-port transperitoneal approach was used in all patients. Following the endotracheal intubation under general anesthesia, the patient was placed in a 60° modified flank position, and the pneumoperitoneum was achieved with a veress needle. The colon was reflected medially, followed by isolation of the gonadal vein, which was dissected up to the renal vein/vena cava. The renal hilum was skeletonized. Intraoperative laparoscopic ultrasound was used to identify the tumor margins and its depth. After the hilar preparation, renal capsule was scored using monopolar shears. Two 15-cm long 3-0 polyglyconate barbed sutures on a 26 mm 1/2 circle needle (V-loc, Covidien, Ireland) were placed in the abdominal cavity for renal parenchymal repair. Two laparoscopic bulldog clamps were placed on the renal artery. Afterward, cold excision of the tumor was performed with robotic scissors. Tumor bed was sutured continuously with a V-loc suture to stop the bleeders and approximate the renal parenchyma. The defect was then covered with hemostatic agent (Floseal, Baxter, Inc., Irvine, CA, USA) and renal parenchyma was further approximated using 0-0 polyglactin sutures on CT-1 needle with sliding-clip renorrhaphy technique.  The bulldog clamps were removed, and a final inspection for homeostasis was performed. A Jackson-Pratt drain was placed in all patients.
Open partial nephrectomy
Flank incision for retroperitoneal approach or chevron incision for transperitoneal approach based on the location of the renal mass was utilized for all patients. After full renal mobilization was achieved, renal vessels were skeletonized. Intraoperative ultrasound was available to assess the tumor margins. Renal artery was then clamped with two bulldog clamps. Renal tumor was excised with adequate surgical margin of the renal parenchyma using cold scissors. Tumor bed was sutured continuously with a V-loc suture to stop the bleeders and approximate the renal parenchyma. The defect was then covered with hemostatic agent (Floseal, Baxter, Inc., Irvine, CA, USA) and renal parenchyma was further approximated using a 0-0 polyglactin suture on a CT-1 needle with sliding-clip renorrhaphy technique. 
All patients received comprehensive metabolic panel every 6 months for 2 years and then yearly. An abdominal ultrasound and chest radiography were done at 3 rd month. Abdominal and thorax CT were performed at 6 th month and yearly thereafter.
| ¤ Results|| |
[Table 1] summarizes the demographics of the patients. The mean age was 56 years in OPN group and 54 years in RAPN group (P = 0.63). The mean body mass index, American Society of Anesthesiologists score and age-adjusted Charlson comorbidity indices in OPN and RAPN groups were 27.5 kg/m 2 and 28.7 kg/m 2 (P = 0.19), 1.45 and 1.85 (P = 0.03), 1.55 and 1.91 (P = 0.25), respectively. Mean tumor size was 4.04 (range = 2-12) cm in OPN group and 3.56 (range = 1.7-7) cm in RAPN group (P = 0.27). Mean R.E.N.A.L nephrometry score was 6.35 (±1.7, range = 4-10) in OPN group and 5.35 (±1.6, range = 4-10) in RAPN group. R.E.N.A.L nephrometry score was significantly higher in OPN group (P = 0.02). There were no statistically differences in preoperative serum creatinine, eGFR, and hematocrit values between two groups.
Operative and early postoperative findings of two groups are listed on [Table 2]. The mean operative time was 152 (±18) min in OPN group and 225 (±58) min in RAPN group. The mean EBL in OPN and RAPN groups was 417 (±202) ml and 268 (±303) ml, respectively. The mean operative time was significantly longer in RAPN group (P = 0.006), whereas the mean EBL was higher in OPN group (P = 0.001). WIT was significantly longer in RAPN group when compared with OPN group (18.02 min vs. 23.33 min, P = 0.003). The mean decline in hematocrit was 5.83% (±4.4) in OPN group and 5.82% (±7.1) in RAPN group (P = 0.17). Mean drain removal time and length of hospital stay were longer in OPN group (3.85 vs. 3.13 days, P = 0.046 and 5.45 vs. 4.11 days P = 0.005, respectively).
[Table 3] lists renal functional outcomes of the two groups. The creatinine levels at postoperative day 1 compared to preoperative serum creatinine were significantly higher in both open (P < 0.001) and robotic groups (P < 0.001). Nevertheless, mean pre- and post-operative 3 rd month eGFR values (ml/min/1.73 m 2 ) were 88 and 79.8 in open group (P = 0.17) and 90.8 and 84.5 in robotic group (P = 0.34). The differences were not significant.
No significant intraoperative complication has occurred in both groups. The complications recorded as Clavien grade one or two included blood transfusion in 2 patients, one prolonged drainage >6 days (no further intervention was required), and one wound infection in the open group. In robotic group, blood transfusion was required in 5 patients, 2 patients had sub-ileus which resolved spontaneously, and 1 patient had transient elevation of serum creatinine. There was no significant difference in postoperative complication rate (P = 0.80) and blood transfusion requirement (P = 0.91) between groups. No open conversion was required in any patient, and there were no robotic malfunctions, system failures or complications related to the robotic surgical system.
Pathological characteristics of patients are listed on [Table 4]. The final pathological examination of 66 resected tumors revealed 14 malignant tumors (%70) in open group and 37 malignant tumors (%80.4) in robotic group. Pathological examination revealed clear cell renal cell carcinoma (RCC) in 36 patients, papillary RCC in 11 patients, and chromophobe RCC in 4 patients. Fuhrman nuclear grading was Grade 1 in 12 patients, Grade 2 in 30 patients, Grade 3 in 7 patients, and Grade 4 in 2 patients. One patient in a robotic group had a positive surgical margin. However, no tumor recurrence has occurred in any group in the follow-up.
| ¤ Discussion|| |
Surgical excision is still the standard treatment modality of the clinically localized renal tumors, and OPN is the most widely performed approach at worldwide.  Minimally invasive nephron-sparing surgical modalities, such as LPN and RAPN, have gained popularity in the last 2 decades. Several studies have compared OPN and LPN and concluded that LPN has acceptable surgical and oncologic outcomes when compared to OPN. , Nevertheless, LPN requires advanced laparoscopic skills with a very steep learning curve. As a result, LPN remains limited to experienced laparoscopic centers. Conversely, robotic surgical system has been introduced in order to reduce limitations associated with conventional laparoscopy.
In this study, mean operation time was significantly longer in patients who underwent RAPN. On the contrary, RAPN has better outcomes in terms of EBL when compared with an open group. However, the mean postoperative decline of hematocrit was not statistically different between groups. In addition to this, length of hospital stay and drain removal time were significantly shorter in RAPN group. Our findings suggest that RAPN provided rapid convalescence, decreased hospital stay and less blood loss. Recently, Simhan et al. compared RAPN and OPN in patients with moderately and highly complex renal tumors according to R.E.N.A.L. nephrometry score. They noticed that, in open surgery, mean operation time was significantly shorter (189 vs. 296 min, P < 0.001) while EBL (256 vs. 131 ml, P < 0.001) and length of stay (5.6 vs. 3.7 days, P < 0.001) were greater than RAPN. They concluded that RAPN offered acceptable perioperative outcomes compared to open surgery.  In another study, Lee et al. reported to comparative analyses of RAPN versus OPN. In this study, the mean operation time was longer in a robotic group (192 vs. 142 min, P = 0.001) while there was no significant difference in EBL. Nonetheless, the length of hospital stay (6.2 vs. 8.9 days, P < 0.001) and postoperative analgesic requirement (ketoprofen, 0.26 vs. 0.88 ampules, P < 0.001) were favorable in robotic group. Eventually, the authors concluded that RAPN is a viable option as a nephron-sparing procedure with acceptable clinical outcomes when compared with open surgery.  Moreover, Lucas et al. compared three nephron-sparing surgical modalities in patients who have similar tumor size, age, gender, and nephrometry score. In this comparison, EBL was observed higher (250 ml vs. 100 ml vs. 100 ml, P < 0.001) and the mean operation time was shorter (147 min vs. 190 min vs. 195 min, P < 0.01) for OPN versus RAPN versus LPN. However, length of stay was significantly shorter in RAPN and LPN when compared with OPN (2 days vs. 2 days vs. 3 days, P < 0.01). In conclusion, the authors emphasized that OPN provided shorter operation time while hospital stay and blood loss were lower in RAPN and LPN. 
Ideal WIT is still under debate in the current literature. Based on anecdotal data, WIT <30 min is recommended in order to reduce renal ischemic injury.  A more recently published multicenter study suggest that the optimal WIT should be <20 min in order to preserve optimal renal functions.  The WIT in OPN has been reported shorter than LPN within the range of 14-20 min in the large series.  Similarly, comparative results revealed that RAPN helps achieving a shorter WIT (within the range of 21-32 min) when compared with traditional laparoscopy. , Our study demonstrated a shorter WIT in OPN group. More recently, Ficarra et al. reported multicenter comparison of RAPN versus OPN. The WIT was shorter in the open group compared to RAPN group (15.4 ± 5.9 vs. 19.2 ± 7.3 min; P < 0.001).  Conversely, Serni et al. compared 392 patients who underwent RAPN or OPN in a single center. No significant difference was observed regarding WIT (18.5 min vs. 16.4 min, P = 0.5). Furthermore, according to results of multivariable analyses, the surgical approach wasn't independently associated with WIT >25 min. In this study, the authors concluded that RAPN has similar outcomes in terms of WIT and eGFR when compared with open surgery.  In our study, WIT was 18.02 min in OPN and 23.3 min in RAPN (P = 0.003). Despite the significantly longer WIT in RAPN group, no difference was observed in postoperative 3 rd month eGFR levels between groups.
According to published series, complication rates were slightly higher in open procedures than RAPN. Vittori carried out multicenter comparison of RAPN and OPN. In this study, postoperative complication rate was higher in OPN (%5.7 vs. %21.2, P < 0.001). In addition, Clavien 3-4 complications were reported 9.1% in the open group and 1% in RAPN group. According to these results, the authors concluded that the surgical approach was one of the independent predictor of postoperative complications on multivariate analyses.  Spana et al. retrospectively reviewed the records of 450 consecutive RAPN patients and reported overall complication rate of %15.8. The authors concluded that RAPN is a reliable nephron-sparing technique, and the complications of this approach could, usually, be managed conservatively.  In the present study, there was no intraoperative complication in both groups. Four postoperative complications (%20) in the open group and 8 complications (%17) in RAPN group had occurred. All complications were graded 1 and 2 based on Clavien-Dindo classification system. There were no significant differences in complication rates between groups.
There are no available contemporary studies in order to compare oncologic outcomes of OPN and RPN. In published series, positive surgical margin rates were reported %0.8-6.8 in OPN series. The largest study with 1390 patients reported PSM rate as %5.8 while the largest RAPN series have reported PSM rates from %0 to %10. ,, In our study, malignant pathology was found in %70 of OPN patients and %80.4 in RAPN patients. One patient in RAPN group has PSM but, no local recurrence occurred in both groups in the follow-up.
Data analysis in a retrospective fashion and small patient number were the drawbacks of the current study. Nevertheless, this single-center study suggests that RAPN is a reliable and effective alternative minimally invasive technique compared with traditional open surgery. Multicentric, prospective, and randomized controlled studies are still required to determine the most valuable approach among these nephron-sparing surgical modalities.
| ¤ Conclusion|| |
Minimally invasive surgical management of renal masses with RAPN offers better outcomes in terms of EBL and length of stay. However, the mean operative time and WIT were significantly shorter in OPN group. RAPN is a safe and effective minimally invasive alternative to OPN in terms of oncological and functional outcomes.
| ¤ References|| |
Siegel R, Naishadham D, Jemal A. Cancer statistics, 2013. CA Cancer J Clin 2013;63:11-30.
Vander Eeckt K, Joniau S, Van Poppel H. Open surgery for localized RCC. ScientificWorldJournal 2007;7:742-52.
Weight CJ, Lieser G, Larson BT, Gao T, Lane BR, Campbell SC, et al.
Partial nephrectomy is associated with improved overall survival compared to radical nephrectomy in patients with unanticipated benign renal tumours. Eur Urol 2010;58:293-8.
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.
Gill IS, Kavoussi LR, Lane BR, Blute ML, Babineau D, Colombo JR Jr, et al.
Comparison of 1,800 laparoscopic and open partial nephrectomies for single renal tumors. J Urol 2007;178:41-6.
Borghesi M, Schiavina R, Gan M, Novara G, Mottrie A, Ficarra V. Expanding utilization of robotic partial nephrectomy for clinical T1b and complex T1a renal masses. World J Urol 2013;31:499-504.
Patel MN, Krane LS, Bhandari A, Laungani RG, Shrivastava A, Siddiqui SA, et al.
Robotic partial nephrectomy for renal tumors larger than 4 cm. Eur Urol 2010;57:310-6.
Edge SB, Compton CC. The American Joint Committee on Cancer: The 7 th
edition of the AJCC cancer staging manual and the future of TNM. Ann Surg Oncol 2010;17:1471-4.
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.
Levey AS, Bosch JP, Lewis JB, Greene T, Rogers N, Roth D. A more accurate method to estimate glomerular filtration rate from serum creatinine: A new prediction equation. Modification of diet in renal disease study group. Ann Intern Med 1999;130:461-70.
Dindo D, Demartines N, Clavien PA. Classification of surgical complications: A new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg 2004;240:205-13.
Benway BM, Wang AJ, Cabello JM, Bhayani SB. Robotic partial nephrectomy with sliding-clip renorrhaphy: Technique and outcomes. Eur Urol 2009;55:592-9.
Porpiglia F, Volpe A, Billia M, Scarpa RM. Laparoscopic versus open partial nephrectomy: Analysis of the current literature. Eur Urol 2008;53:732-42.
Simhan J, Smaldone MC, Tsai KJ, Li T, Reyes JM, Canter D, et al.
Perioperative outcomes of robotic and open partial nephrectomy for moderately and highly complex renal lesions. J Urol 2012;187:2000-4.
Lee S, Oh J, Hong SK, Lee SE, Byun SS. Open versus robot-assisted partial nephrectomy: Effect on clinical outcome. J Endourol 2011;25:1181-5.
Lucas SM, Mellon MJ, Erntsberger L, Sundaram CP. A comparison of robotic, laparoscopic and open partial nephrectomy. JSLS 2012;16:581-7.
Novick AC. Renal hypothermia: In vivo
and ex vivo
. Urol Clin North Am 1983;10:637-44.
Ficarra V, Bhayani S, Porter J, Buffi N, Lee R, Cestari A, et al.
Predictors of warm ischemia time and perioperative complications in a multicenter, international series of robot-assisted partial nephrectomy. Eur Urol 2012;61:395-402.
Benway BM, Bhayani SB, Rogers CG, Dulabon LM, Patel MN, Lipkin M, et al.
Robot assisted partial nephrectomy versus laparoscopic partial nephrectomy for renal tumors: A multi-institutional analysis of perioperative outcomes. J Urol 2009;182:866-72.
Scoll BJ, Uzzo RG, Chen DY, Boorjian SA, Kutikov A, Manley BJ, et al.
Robot-assisted partial nephrectomy: A large single-institutional experience. Urology 2010;75:1328-34.
Ficarra V, Minervini A, Antonelli A, Bhayani S, Guazzoni G, Longo N, et al.
A multicentre matched-pair analysis comparing robot-assisted versus open partial nephrectomy. BJU Int 2014;113:936-41.
Serni S, Vittori G, Masieri L, Gacci M, Lapini A, Siena G, et al.
Robotic vs open simple enucleation for the treatment of T1a-T1b renal cell carcinoma: A single center matched-pair comparison. Urology 2014;83:331-7.
Vittori G. Open versus robotic-assisted partial nephrectomy: A multicenter comparison study of perioperative results and complications. World J Urol 2014;32:287-93.
Spana G, Haber GP, Dulabon LM, Petros F, Rogers CG, Bhayani SB, et al.
Complications after robotic partial nephrectomy at centers of excellence: Multi-institutional analysis of 450 cases. J Urol 2011;186:417-21.
Yossepowitch O, Thompson RH, Leibovich BC, Eggener SE, Pettus JA, Kwon ED, et al.
Positive surgical margins at partial nephrectomy: Predictors and oncological outcomes. J Urol 2008;179:2158-63.
[Table 1], [Table 2], [Table 3], [Table 4]