Original Research
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JOURNAL OF ENDOUROLOGY Volume XX, Number XX, XXXXXX 2014 ª Mary Ann Liebert, Inc. Pp. ---–--DOI: 10.1089/end.2014.0517
Comparison of Hand-Assisted Laparoscopic Versus Robot-Assisted Laparoscopic Versus Open Partial Nephrectomy in Patients with T1 Renal Masses Kyung-sik Han, MD, Gee Hyun Song, MD, PhD, Dalsan You, MD, PhD, Cheryn Song, MD, PhD, In Gab Jeong, MD, PhD, Jun Hyuk Hong, MD, PhD, Hanjong Ahn, MD, PhD, Choung-Soo Kim, MD, PhD, and Bumsik Hong, MD, PhD
Abstract
Purpose: To evaluate the validity of hand-assisted laparoscopic partial nephrectomy (HALPN) for small renal masses, patients who underwent HALPN, robot-assisted laparoscopic partial nephrectomy (RALPN), or open partial nephrectomy (OPN) at a single medical institution were compared in terms of perioperative outcomes. Patients and Methods: In this retrospective cohort study, all 590 consecutive patients who underwent HALPN (n = 89), RALPN (n = 147), or OPN (n = 354) between July 2011 and April 2014 in a single institute were compared in terms of perioperative outcomes, including the mean operative time, warm ischemia time (WIT), length of the hospital stay, change in the estimated glomerulofiltration rate (eGFR), duration of analgesic use, surgical margins, and adverse events. The patient groups were compared by a multivariate regression model, in which adjustments were made for differences in baseline demographic and tumor characteristics. Results: OPN associated with a significantly longer mean operative time (187 minutes) than RALPN (162 minutes; p < 0.001) or HALPN (172 minutes; p = 0.013), a longer hospital stay (7.3, 5.3, and 5.9 days, respectively; p < 0.001 and < 0.001, respectively), and a longer duration of analgesic use (6.6, 4.6, and 5.4 days, respectively; p < 0.001 and < 0.001, respectively). HALPN and RALPN were equivalent in terms of operative time. RALPN had a significantly longer WIT than HALPN and OPN ( p < 0.001 and < 0.001, respectively). HALPN had a significantly longer hospital stay than RALPN ( p = 0.026). The three methods differed in terms of eGFR change ( p = 0.028), but multivariate analysis found that the surgical method was not a significant factor for eGFR. The three methods did not differ in terms of complication rates. Conclusions: HALPN associated with shorter operative and convalescence times compared with OPN. HALPN was generally not inferior to RALPN in terms of perioperative outcomes, although it associated with a longer convalescence. A number of minimally invasive technologies have been made recently. There are two different endoscopic approaches for PN, namely, the laparoscopic transperitoneal and retroperitoneoscopic approaches. For both approaches, handassisted and robotic-assisted techniques are available. Since the principal advantage of the retroperitoneoscopic approach is the absence of intra-abdominal manipulation, this technique is favored mostly in patients who have undergone previous abdominal surgery or who have a posteriorly located tumor.6 Therefore, at present, there are three different laparoscopic PN (LPN) techniques, namely, pure LPN, hand-assisted LPN (HALPN), and robot-assisted LPN (RALPN). HALPN has one marked advantage over LPN and RALPN; it allows the surgeon to perform laparoscopic procedures with his or her hand inside the patient’s abdominal cavity, thus maintaining tactile feedback.7
Introduction
T
he American Urological Association (AUA) guidelines recommend partial nephrectomy (PN), when feasible, as a standard treatment for patients presenting with T1 renal cell carcinoma.1 However, whether this approach really is the best method for treating a small renal mass was initially thrown in doubt when a prospective randomized study comparing the oncologic outcomes of elective nephron-sparing surgery and radical nephrectomy for low-stage renal cell carcinoma suggested that nephron-sparing surgery may not confer overall survival benefits.2 Nevertheless, subsequent evidence indicated that compared with radical nephrectomy, PN indeed associates with a lower renal function impairment, better overall patient survival, and equivalent oncologic survival.3–5
Department of Urology, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Korea.
1
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Moreover, since RALPN has largely overcome the technical difficulties of LPN, it is increasingly being performed instead of LPN.8 Despite these advances in minimally invasive PN, open PN (OPN) is still predominantly used at present to treat small renal masses.9 All this technical diversity has spawned debate about which of the three PN techniques (OPN, HALPN, and RALPN) yields the best outcomes in terms of warm ischemia times (WIT), positive surgical margins, perioperative complications, and renal functional outcomes. To address these issues, the contemporary PN series between 2011 and 2014 at a single medical center was analyzed to compare the perioperative outcomes of HALPN, RALPN, and OPN for T1 renal tumor. Patients and Methods Study population
This retrospective cohort study was based on all consecutive patients with T1 renal tumor who underwent HALPN, OPN, or RALPN between July 2011 and April 2014 in a single medical institute. Thus, the medical charts of 590 consecutive patients who underwent HALPN (n = 89), RALPN (n = 147), or OPN (n = 354) were reviewed. All patient data were obtained from our Institutional Review Board-approved database, which prospectively registers all baseline patient characteristics.
Surgical technique
The HALPN procedure that is performed in our institution is similar to the method described by Strup et al.10 Thus, an 8cm vertical incision is made for a hand port and the Gel Port system (Applied Medical, Rancho Santa Margarita, CA) is applied. An additional two 12-mm trocars are then placed. Occasionally, a third (5-mm) trocar is used. For dissection, the Harmonic Ace scalpel (Endo Surgery; Ethicon, Cincinnati, OH) is generally used instead of electrocautery laparoscopic scissors. The RALPN procedure that is used in our institution is similar to the method described by Gettman et al.11 Thus, the da Vinci S robot (Intuitive Surgical Systems, Sunnyvale, CA) with a four-arm technique and a transperitoneal approach is employed. Hilar control is obtained through bulldog clamping. OPN is performed using a subcostal or flank approach. Most of the present cases involved the retroperitoneal approach. The renal pedicle is generally clamped by using a bulldog clamp. Occasionally, when tumor is superficial and peripheral, the pedicle is not clamped. Depending on the operator’s preference, ice is used during pedicle clamping. Opened calices and bleeding sites are always carefully repaired. Statistical considerations
For all patients, the tumor localization was determined by reviewing the radiographic images and the RENAL
Table 1. Demographic and Tumor Characteristics of Entire Cohort HALPN (n = 89) Patient age, year, mean (SD) Male gender, n (%) BMI (SD) ASA score (SD) Baseline eGFR (SD, mL/minute/1.73 m2) Prior abdominal surgery, n (%) Solitary kidney, n (%) Right/left (R) Tumor size (SD, cm) (E) Exophytic/endophytic properties ‡ 50% < 50% Entirely endophytic (N) Nearness of tumor to the collecting system ‡7 > 4 but < 7 £4 (A) Anterior/posterior Anterior Posterior Neither (L) Location relative to polar lines Upper and lower pole Cross polar line Entirely between polar line RENAL nephrometry score (SD)
53.6 (9.7) 62 (69.7) 25.8 (3.1) 1.66 (0.5) 82.1 (10.4) 4 (4.5) 1 (1.1) 53/36 2.39 (0.95) 24 (27%) 48 (53.9%) 17 (19.1%)
RALPN (n = 147) 52.5 (11.9) 108 (73.5) 25.56 (3.2) 1.51 (0.52) 82.3 (9.9) 16 (10.9) 1 (0.6) 79/68 2.58 (1.13) 68 (46.3%) 60 (40.8%) 19 (12.9%)
OPN (n = 354)
Total (n = 590)
55.3 (12.4) 270 (76.3) 24.5 (3.0) 1.40 (0.49) 80.1 (13.3) 33 (9.3) 10 (1.1) 177/177 2.80 (1.35)
54.4 (11.9) 440 (74.6) 24.9 (4.1) 1.47 (0.51) 80.9 (12.1) 53 (9.0) 12 (2.8) 309/281 2.68 (1.25)
143 (40.4%) 134 (37.9%) 77 (21.8%)
235 (39.8%) 242 (41.0%) 113 (19.2%)
p-Value 0.05 0.41 0.02 < 0.001 0.12 0.24 0.24 0.25 0.08 0.007
0.13 44 (49.4%) 16 (18%) 29 (32.6%)
74 (50.3%) 37 (25.2%) 36 (24.5%)
205 (57.9%) 64 (18.1%) 85 (24%)
323 (54.7%) 117 (19.8%) 150 (25.4%)
31 (34.8%) 41 (46.1%) 17 (19.1%)
71 (48.3%) 52 (35.4%) 24 (16.3%)
149 (42.1%) 130 (36.7%) 75 (21.2%)
251 (42.5%) 223 (37.8%) 116 (19.7%)
112 134 108 6.72
221 201 168 6.51
0.23
0.002 34 28 27 6.21
(38.2%) (31.5%) (30.3%) (1.61)
75 39 33 6.58
(51.0%) (26.5%) (22.5%) (1.80)
(31.6%) (37.9%) (30.5%) (1.63)
(37.4%) (34.1%) (28.5%) (1.73)
0.07
ANOVA, chi-square test, Kruscal–Wallis test. ASA score = American Society of Anesthesiologists score; BMI = body–mass index; eGFR = estimated glomerulofiltration rate; HALPN = hand-assisted laparoscopic partial nephrectomy; OPN = open partial nephrectomy; RALPN = robot-assisted laparoscopic partial nephrectomy; SD = standard deviation.
WHICH IS THE BEST IN PARTIAL NEPHRECTOMY
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Table 2. Perioperative Outcomes in the Three Cohorts
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HALPN (n = 89) Operative time (SD, minute) WIT (SD, minute) Length of hospitalization (SD, day) Decrease in eGFR (SD, mL/minute/1.73 m2) Resection margin (SD, cm) Duration of analgesic (SD, day) Postoperative complications (%)
172.9 19.4 5.9 3.20 0.35 5.40 4
(42.3) (6.7) (1.66) (5.44) (0.24) (1.24) (4.49)
RALPN (n = 147) 162.3 24.7 5.3 2.40 0.36 4.65 5
(32.2) (7.3) (1.41) (6.70) (0.26) (1.26) (3.4)
OPN (n = 354) 187.2 19.6 7.3 4.34 0.46 6.61 28
(43.8) (6.7) (2.06) (8.34) (0.36) (1.66) (7.91)
p-Value < 0.0001 < 0.0001 < 0.0001 0.028 0.0007 < 0.0001 0.13
ANOVA, chi-square test. WIT = warm ischemia time.
nephrometry scores were calculated. The three groups were compared in terms of perioperative outcomes by using a multivariate regression model, in which adjustments were made for potential confounders, namely, baseline demographic and tumor characteristics. Comparisons involving categorical and continuous variables were made by using the chi-square test and ANOVA, respectively. All reported pvalues were two sided, and a value of p < 0.05 was considered to indicate statistical significance. SPSS version 18.0 (IBM Corp., Armonk, NY) was used for statistical analyses.
Table 3. Linear Regression Model of Perioperative Outcomes Multivariate analysis Variable
Estimate (95% CI)
Operative time RALPN/HALPN - 8.91 ( - 19.5, 1.70) OPN/HALPN 15.11 (5.67, 24.56) Gender M/F 15.05 (7.66, 22.45) BMI 1.66 (0.60, 2.72) RENAL 3.24 (1.38, 5.09) nephrometry score WIT RALPN/HALPN 6.01 (4.21, 7.81) OPN/HALPN 0.42 ( - 1.17, 2.01) RENAL 0.88 (0.56, 1.20) nephrometry score Length of hospitalization (log) RALPN/HALPN - 0.11 ( - 0.17, - 0.05) OPN/HALPN 0.20 (0.14, 0.25) Duration of analgesic (log) RALPN/HALPN - 0.15 ( - 0.21,0.10) OPN/HALPN 0.20 (0.15, 0.24) Decrease in eGFR RALPN/HALPN - 0.11 ( - 2.05, 1.82) OPN/HALPN 1.13 ( - 0.60, 2.87) Age 0.11 (0.06, 0.16) ASA score 1.87 (0.59, 3.14) Solitary kidney 5.13 (0.91, 9.35) RENAL 0.72 (0.38, 1.06) nephrometry score CI = confidence intervals.
p-Value 0.09 0.002 < 0.001 0.002 0.001
< 0.001 0.60 < 0.001
0.001 < 0.001 < 0.001 < 0.001 0.90 0.20 < 0.001 0.004 0.01 < 0.001
Results
The demographic data are summarized in Table 1. Regarding the perioperative outcomes, the average operative times of the HALPN, RALPN, and OPN groups were 173, 162, and 187 minutes, respectively ( p < 0.001). The HALPN and RALPN groups did not differ significantly in terms of this variable ( p = 0.18). The RALPN group had the longest mean WIT (24.7 minutes). However, the HALPN and OPN groups did not differ significantly in terms of WIT (19.4 vs19.6 minutes, p = 0.85). The OPN group had the longest average hospitalization stay (7.3 days). Moreover, the HALPN group stayed significantly longer in hospital than the RALPN group (5.9 vs 5.3 days, p = 0.026). The OPN group also had a significantly longer duration of analgesic use (6.6 days) than the RALPN (4.6 days) or HALPN (5.4 days) group ( p < 0.001). The three groups differed significantly in terms of estimated glomerular filtration rate (eGFR) decrease; it was 3.20, 2.40, and 4.34 mL/minute/1.73 m2 for the HALPN, RALPN, and OPN groups, respectively ( p = 0.028) (Table 2). However, multivariate regression model analysis did not find that the operation type associated significantly with the eGFR decrease. By contrast, age, American Society of Anesthesiologists score (ASA score), solitary kidney status, and the RENAL nephrometry score all associated significantly with the eGFR decrease. However, multivariate regression model analysis showed that OPN associated significantly with a long operation time. Gender also associated significantly regardless of the operation type; PN took about 15 minutes longer in men than in women. Body–mass index also associated significantly with operative time; the higher the body– mass index (BMI), the longer the operation time (Table 3). The complications included hematuria, urine leak, hypoxia, transfusion, pesudoaneurysm, and wound dehiscence. The overall complication rates for the HALPN, RALPN, and OPN groups were 4.5%, 3.4%, and 7.9%, respectively (Tables 2 and 4). The three groups did not differ in terms of complication rates ( p = 0.13). Multivariate regression analysis revealed that only the RENAL nephrometry score was a significant factor for complication rate (odds ratio 1.49, 95% confidence intervals 1.22, 1.81) (Table 5). The surgical margins in all patients were negative. Discussion
HALPN was introduced by Jordan and Winslow in 1993 and is a practical option for small ( < 4 cm) renal masses.12,13 While two studies have compared HALPN with RALPN or OPN,14,15 they are disadvantaged by a small sample size or
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Table 4. Complications
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HALPN 4 (4.5%)
RALPN 5 (3.4%)
Clavien grade I
Hematuria (1)
Clavien grade II Clavien grade III-IV
— Pseudoaneurysm (1), urine leak (1), wound dehiscence (1)
by differences between the groups in terms of tumor characteristics. Therefore, to determine whether these three methods differ in terms of perioperative outcomes and complications, we designed the present study, which was reasonably sized and involved covariant-adjusted group comparisons. Although the retroperitoneal approach has several advantages that allow direct access to the renal artery, thus reducing the chance of organ injury, this approach is complicated by the small working space and relative paucity of distinct anatomical landmarks.6,16 Therefore, unless patients are not eligible for the transperitoneal approach, we prefer to employ the transperitoneal approach rather than the retroperitoneal approach. By contrast, most of the OPN surgeries in the present study involved the retroperitoneal approach. Moreover, there was variability in terms of whether ice was used when the pedicle was clamped in OPN; 22.8% of the OPN cases involved the use of ice. There was also some variability in terms of whether the nonclamp technique was used, if the tumor was superficial and peripheral clamping was not performed. This applied in four HALPN cases, one RALPN case, and 21 OPN cases. OPN is considered to be the gold standard treatment for small renal tumors as its renal functional outcomes and disease-specific survival are superior and equivalent to those of radical nephrectomy, respectively.17,18 However, compared with LPN, OPN associates with an increased convalescence time because it involves a large incision that produces intense pain. By contrast, LPN reduces recovery time while yielding similar oncologic and nephrologic outcomes. Indeed, one study of 1800 consecutive patients who underwent either
OPN 28 (7.9%)
Hypoxia (1), hematuria (1) Blood transfusion (1) Pseudoaneurysm (1), urine leak (1)
Ileus (4) Blood transfusion (17) Pseudoaneurysm (2), urine leak (2), wound dehiscence (3)
OPN or LPN reported that the LPN group had shorter operative times, less intraoperative blood loss, and a shorter length of hospital stay. However, it should be noted that the patients who underwent LPN were more likely than the patients undergoing OPN to have more peripheral and smaller tumors. Moreover, due to the greater number of surgical steps involved in LPN compared with OPN, LPN associated with longer WITs and a significant increase in the postoperative complication rate.19 To reduce the problems associated with such a difficult laparoscopic technique, RALPN was developed. It reduces surgeon fatigue and shortens the learning curve of LPN and has as a result largely replaced LPN.20 HALPN is also another traditional minimally invasive approach for PN. Thus, the three most commonly used PN techniques in our medical institution in the study period were HALPN, RALPN, and OPN. A previous study showed that HALPN associates with a shorter mean operation time than OPN (161 vs 191 minutes; p = 0.027). It also associates with less blood loss (120 vs 353 cc; p = 0.0003), a shorter WIT (27.0 vs 33.0 minutes; p = 0.035), and a smaller overall complication rate (18.3% vs 32.5%, p = 0.10).14 The present study also showed that HALPN associated with better outcomes than OPN in terms of most perioperative variables. This may reflect the fact that although HALPN is still a minimally invasive approach, it also allows tactile feedback that aids tumor perception and dissection and specimen extraction and reduces the WIT.21 The present study showed that HALPN associated with a shorter convalescence time than OPN. However, HALPN did not differ from OPN in terms of complication rates or eGFR decrease. Moreover, the WITs of these groups did not differ (19.4 vs 19.6 minutes,
Table 5. Independent Predictor of Complication Univariate OR (95% CI) Group RALPN/HALPN OPN/HALPN Age Gender M/F BMI ASA score Prior abdominal surgery Solitary kidney Right/left RENAL nephrometry score OR = odds ratio.
0.75 1.83 1.01 1.50 0.97 1.12 0.89 1.37 0.85 1.52
(0.20, (0.62, (0.98, (0.64, (0.95, (0.58, (0.26, (0.17, (0.44, (1.25,
2.86) 5.35) 1.04) 3.48) 0.99) 2.19) 2.99) 10.9) 1.66) 1.85)
Multivariable p-Value
OR (95% CI)
p-Value
0.67 0.27 0.47 0.35 0.64 0.73 0.85 0.76 0.64 < 0.001
0.96 (0.25, 3.77) 1.74 (0.58, 5.21)
0.95 0.32
1.49 (1.22, 1.81)
< 0.001
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WHICH IS THE BEST IN PARTIAL NEPHRECTOMY
p = 0.85). However, this contrasts with a previous study, which showed that HALPN has superior WIT compared with OPN.14 The present study also compared HALPN with RALPN. Unlike the equivalence of HALPN and OPN in terms of WIT, HALPN is associated with a shorter WIT (19.4 minutes) than RALPN (24.7 minutes; p < 0.001). This is significant because Thompson et al.22 showed that a high WIT associates with an acute risk of postoperative renal failure and an increased risk of postoperative stage IV chronic kidney disease (CKD). Thus, WIT is an important predictor of renal function preservation. However, the present study could not demonstrate a relationship between WIT and postoperative renal failure. Another study also found that RALPN does not yield remarkable benefits in terms of perioperative outcomes relative to HALPN; moreover, RALPN is associated with increased cost.15 Most of the advantages of HALPN over other laparoscopic techniques stem from the surgeon being able to use his or her hand during the surgery. When resecting a tumor after positioning a hilar clamp, a fingertip can bluntly dissect a mass, similar to what is achieved by using a blade handle in open surgery. Moreover, using the hand to enclose a defect can be both effective and prompt. Grasping and folding a kidney by hand is also helpful for approximating the defect surface. Moreover, unlike OPN, HALPN is performed in our institute by using a high-definition laparoscopic monitor that facilitates the meticulousness of the technique. It should, however, be noted that HALPN is more invasive than LPN or RALPN and can lead to wound problems and hernias. Furthermore, the hand can hinder laparoscopic vision during surgery. However, these problems are compensated by the great advantages yielded by the tactile feedback in HALPN. Moreover, although the open surgical technique is still considered to be the gold standard treatment in terms of renal function outcomes and disease-specific survival relative to radical nephrectomy,17,18 HALPN is also amenable to oncologic principles. The present study suggested that HALPN may achieve the superior outcomes of OPN relative to radical nephrectomy, while tending to reduce complications. This study has some limitations. First, there was a selection bias due to the use of different surgeons. Only HALPN was performed by one surgeon. Furthermore, although a multivariate regression model was employed, the study was not a randomized prospective study and thus it is subject to the inherent limitations of a retrospective analysis of observational data. Conclusions
Compared to OPN, HALPN associated with a shorter operative time and convalescence period. Compared to RALPN, HALPN generally did not have inferior perioperative outcomes; however, it did associate with a significantly longer convalescence period. The three approaches did not differ in terms of the complication rate. Disclosure Statement
The authors have no conflicts of interest to disclose. References
1. Campbell SC, et al. Guideline for management of the clinical T1 renal mass. J Urol 2009;182:1271–1279.
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2. Van Poppel H, et al. A prospective, randomised EORTC intergroup phase 3 study comparing the oncologic outcome of elective nephron-sparing surgery and radical nephrectomy for low-stage renal cell carcinoma. Eur Urol 2011;59: 543–552. 3. MacLennan S, et al. Systematic review of oncological outcomes following surgical management of localised renal cancer. Eur Urol 2012;61:972–993. 4. Antonelli A, et al. Elective partial nephrectomy is equivalent to radical nephrectomy in patients with clinical T1 renal cell carcinoma: Results of a retrospective, comparative, multi-institutional study. BJU Int 2012;109:1013–1018. 5. Ficarra V, et al. A multicentre matched-pair analysis comparing robot-assisted versus open partial nephrectomy. BJU Int 2014;113:936–941. 6. Ren T, et al. Transperitoneal approach versus retroperitoneal approach: A meta-analysis of laparoscopic partial nephrectomy for renal cell carcinoma. PLoS One 2014;9: e91978. 7. Wolf JS, Jr. Hand-assisted laparoscopy: Pro. Urology 2001; 58:310–312. 8. Benway BM, et al. Robot assisted partial nephrectomy versus laparoscopic partial nephrectomy for renal tumors: A multi-institutional analysis of perioperative outcomes. J Urol 2009;182:866–872. 9. Kowalczyk KJ, et al. Comparative effectiveness, costs and trends in treatment of small renal masses from 2005 to 2007. BJU Int 2013;112:E273–E280. 10. Strup S, et al. Laparoscopic partial nephrectomy: Handassisted technique. J Endourol 2005;19:456–459; discussion 459–460. 11. Gettman MT, et al. Robotic-assisted laparoscopic partial nephrectomy: Technique and initial clinical experience with DaVinci robotic system. Urology 2004;64:914–918. 12. Jordan GH, Winslow BH. Laparoendoscopic upper pole partial nephrectomy with ureterectomy. J Urol 1993;150: 940–943. 13. Wu Z, et al. A propensity-score matched comparison of perioperative and early renal functional outcomes of robotic versus open partial nephrectomy. PLoS One 2014;9: e94195. 14. DeVoe WB, et al. Hand-assisted laparoscopic partial nephrectomy after 60 cases: Comparison with open partial nephrectomy. Surg Endosc 2009;23:1075–1080. 15. Elsamra SE, et al. Hand-assisted laparoscopic versus robotassisted laparoscopic partial nephrectomy: Comparison of short-term outcomes and cost. J Endourol 2013;27:182– 188. 16. Marszalek M, et al. Laparoscopic partial nephrectomy: A matched-pair comparison of the transperitoneal versus the retroperitoneal approach. Urology 2011;77:109–113. 17. Mabjeesh NJ, Avidor Y, Matzkin H. Emerging nephron sparing treatments for kidney tumors: A continuum of modalities from energy ablation to laparoscopic partial nephrectomy. J Urol 2004;171(2 Pt 1):553–560. 18. Fergany AF, Hafez KS, Novick AC. Long-term results of nephron sparing surgery for localized renal cell carcinoma: 10-year followup. J Urol 2000;163:442–445. 19. Gill IS, et al. Comparison of 1,800 laparoscopic and open partial nephrectomies for single renal tumors. J Urol 2007; 178:41–46. 20. Haber GP, et al. Robotic versus laparoscopic partial nephrectomy: Single-surgeon matched cohort study of 150 patients. Urology 2010;76:754–758.
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21. Wolf JS, Jr., Seifman BD, Montie JE. Nephron sparing surgery for suspected malignancy: Open surgery compared to laparoscopy with selective use of hand assistance. J Urol 2000;163:1659–1664. 22. Thompson RH, et al. Every minute counts when the renal hilum is clamped during partial nephrectomy. Eur Urol 2010;58:340–345.
Address correspondence to: Bumsik Hong, MD, PhD Department of Urology Asan Medical Center University of Ulsan College of Medicine 88, Olympic-ro 43-gil Songpa-gu Seoul 138-736 Korea E-mail: [email protected]
Abbreviations Used ASA score ¼ American Society of Anesthesiologists score BMI ¼ body–mass index CI ¼ confidence intervals eGFR ¼ estimated glomerulofiltration rate HALPN ¼ hand-assisted laparoscopic partial nephrectomy OPN ¼ open partial nephrectomy OR ¼ odds ratio PN ¼ partial nephrectomy RALPN ¼ robot-assisted laparoscopic partial nephrectomy WIT ¼ warm ischemia time
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JOURNAL OF ENDOUROLOGY Volume XX, Number XX, XXXXXX 2014 ª Mary Ann Liebert, Inc. Pp. ---–--DOI: 10.1089/end.2014.0517
Comparison of Hand-Assisted Laparoscopic Versus Robot-Assisted Laparoscopic Versus Open Partial Nephrectomy in Patients with T1 Renal Masses Kyung-sik Han, MD, Gee Hyun Song, MD, PhD, Dalsan You, MD, PhD, Cheryn Song, MD, PhD, In Gab Jeong, MD, PhD, Jun Hyuk Hong, MD, PhD, Hanjong Ahn, MD, PhD, Choung-Soo Kim, MD, PhD, and Bumsik Hong, MD, PhD
Abstract
Purpose: To evaluate the validity of hand-assisted laparoscopic partial nephrectomy (HALPN) for small renal masses, patients who underwent HALPN, robot-assisted laparoscopic partial nephrectomy (RALPN), or open partial nephrectomy (OPN) at a single medical institution were compared in terms of perioperative outcomes. Patients and Methods: In this retrospective cohort study, all 590 consecutive patients who underwent HALPN (n = 89), RALPN (n = 147), or OPN (n = 354) between July 2011 and April 2014 in a single institute were compared in terms of perioperative outcomes, including the mean operative time, warm ischemia time (WIT), length of the hospital stay, change in the estimated glomerulofiltration rate (eGFR), duration of analgesic use, surgical margins, and adverse events. The patient groups were compared by a multivariate regression model, in which adjustments were made for differences in baseline demographic and tumor characteristics. Results: OPN associated with a significantly longer mean operative time (187 minutes) than RALPN (162 minutes; p < 0.001) or HALPN (172 minutes; p = 0.013), a longer hospital stay (7.3, 5.3, and 5.9 days, respectively; p < 0.001 and < 0.001, respectively), and a longer duration of analgesic use (6.6, 4.6, and 5.4 days, respectively; p < 0.001 and < 0.001, respectively). HALPN and RALPN were equivalent in terms of operative time. RALPN had a significantly longer WIT than HALPN and OPN ( p < 0.001 and < 0.001, respectively). HALPN had a significantly longer hospital stay than RALPN ( p = 0.026). The three methods differed in terms of eGFR change ( p = 0.028), but multivariate analysis found that the surgical method was not a significant factor for eGFR. The three methods did not differ in terms of complication rates. Conclusions: HALPN associated with shorter operative and convalescence times compared with OPN. HALPN was generally not inferior to RALPN in terms of perioperative outcomes, although it associated with a longer convalescence. A number of minimally invasive technologies have been made recently. There are two different endoscopic approaches for PN, namely, the laparoscopic transperitoneal and retroperitoneoscopic approaches. For both approaches, handassisted and robotic-assisted techniques are available. Since the principal advantage of the retroperitoneoscopic approach is the absence of intra-abdominal manipulation, this technique is favored mostly in patients who have undergone previous abdominal surgery or who have a posteriorly located tumor.6 Therefore, at present, there are three different laparoscopic PN (LPN) techniques, namely, pure LPN, hand-assisted LPN (HALPN), and robot-assisted LPN (RALPN). HALPN has one marked advantage over LPN and RALPN; it allows the surgeon to perform laparoscopic procedures with his or her hand inside the patient’s abdominal cavity, thus maintaining tactile feedback.7
Introduction
T
he American Urological Association (AUA) guidelines recommend partial nephrectomy (PN), when feasible, as a standard treatment for patients presenting with T1 renal cell carcinoma.1 However, whether this approach really is the best method for treating a small renal mass was initially thrown in doubt when a prospective randomized study comparing the oncologic outcomes of elective nephron-sparing surgery and radical nephrectomy for low-stage renal cell carcinoma suggested that nephron-sparing surgery may not confer overall survival benefits.2 Nevertheless, subsequent evidence indicated that compared with radical nephrectomy, PN indeed associates with a lower renal function impairment, better overall patient survival, and equivalent oncologic survival.3–5
Department of Urology, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Korea.
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Moreover, since RALPN has largely overcome the technical difficulties of LPN, it is increasingly being performed instead of LPN.8 Despite these advances in minimally invasive PN, open PN (OPN) is still predominantly used at present to treat small renal masses.9 All this technical diversity has spawned debate about which of the three PN techniques (OPN, HALPN, and RALPN) yields the best outcomes in terms of warm ischemia times (WIT), positive surgical margins, perioperative complications, and renal functional outcomes. To address these issues, the contemporary PN series between 2011 and 2014 at a single medical center was analyzed to compare the perioperative outcomes of HALPN, RALPN, and OPN for T1 renal tumor. Patients and Methods Study population
This retrospective cohort study was based on all consecutive patients with T1 renal tumor who underwent HALPN, OPN, or RALPN between July 2011 and April 2014 in a single medical institute. Thus, the medical charts of 590 consecutive patients who underwent HALPN (n = 89), RALPN (n = 147), or OPN (n = 354) were reviewed. All patient data were obtained from our Institutional Review Board-approved database, which prospectively registers all baseline patient characteristics.
Surgical technique
The HALPN procedure that is performed in our institution is similar to the method described by Strup et al.10 Thus, an 8cm vertical incision is made for a hand port and the Gel Port system (Applied Medical, Rancho Santa Margarita, CA) is applied. An additional two 12-mm trocars are then placed. Occasionally, a third (5-mm) trocar is used. For dissection, the Harmonic Ace scalpel (Endo Surgery; Ethicon, Cincinnati, OH) is generally used instead of electrocautery laparoscopic scissors. The RALPN procedure that is used in our institution is similar to the method described by Gettman et al.11 Thus, the da Vinci S robot (Intuitive Surgical Systems, Sunnyvale, CA) with a four-arm technique and a transperitoneal approach is employed. Hilar control is obtained through bulldog clamping. OPN is performed using a subcostal or flank approach. Most of the present cases involved the retroperitoneal approach. The renal pedicle is generally clamped by using a bulldog clamp. Occasionally, when tumor is superficial and peripheral, the pedicle is not clamped. Depending on the operator’s preference, ice is used during pedicle clamping. Opened calices and bleeding sites are always carefully repaired. Statistical considerations
For all patients, the tumor localization was determined by reviewing the radiographic images and the RENAL
Table 1. Demographic and Tumor Characteristics of Entire Cohort HALPN (n = 89) Patient age, year, mean (SD) Male gender, n (%) BMI (SD) ASA score (SD) Baseline eGFR (SD, mL/minute/1.73 m2) Prior abdominal surgery, n (%) Solitary kidney, n (%) Right/left (R) Tumor size (SD, cm) (E) Exophytic/endophytic properties ‡ 50% < 50% Entirely endophytic (N) Nearness of tumor to the collecting system ‡7 > 4 but < 7 £4 (A) Anterior/posterior Anterior Posterior Neither (L) Location relative to polar lines Upper and lower pole Cross polar line Entirely between polar line RENAL nephrometry score (SD)
53.6 (9.7) 62 (69.7) 25.8 (3.1) 1.66 (0.5) 82.1 (10.4) 4 (4.5) 1 (1.1) 53/36 2.39 (0.95) 24 (27%) 48 (53.9%) 17 (19.1%)
RALPN (n = 147) 52.5 (11.9) 108 (73.5) 25.56 (3.2) 1.51 (0.52) 82.3 (9.9) 16 (10.9) 1 (0.6) 79/68 2.58 (1.13) 68 (46.3%) 60 (40.8%) 19 (12.9%)
OPN (n = 354)
Total (n = 590)
55.3 (12.4) 270 (76.3) 24.5 (3.0) 1.40 (0.49) 80.1 (13.3) 33 (9.3) 10 (1.1) 177/177 2.80 (1.35)
54.4 (11.9) 440 (74.6) 24.9 (4.1) 1.47 (0.51) 80.9 (12.1) 53 (9.0) 12 (2.8) 309/281 2.68 (1.25)
143 (40.4%) 134 (37.9%) 77 (21.8%)
235 (39.8%) 242 (41.0%) 113 (19.2%)
p-Value 0.05 0.41 0.02 < 0.001 0.12 0.24 0.24 0.25 0.08 0.007
0.13 44 (49.4%) 16 (18%) 29 (32.6%)
74 (50.3%) 37 (25.2%) 36 (24.5%)
205 (57.9%) 64 (18.1%) 85 (24%)
323 (54.7%) 117 (19.8%) 150 (25.4%)
31 (34.8%) 41 (46.1%) 17 (19.1%)
71 (48.3%) 52 (35.4%) 24 (16.3%)
149 (42.1%) 130 (36.7%) 75 (21.2%)
251 (42.5%) 223 (37.8%) 116 (19.7%)
112 134 108 6.72
221 201 168 6.51
0.23
0.002 34 28 27 6.21
(38.2%) (31.5%) (30.3%) (1.61)
75 39 33 6.58
(51.0%) (26.5%) (22.5%) (1.80)
(31.6%) (37.9%) (30.5%) (1.63)
(37.4%) (34.1%) (28.5%) (1.73)
0.07
ANOVA, chi-square test, Kruscal–Wallis test. ASA score = American Society of Anesthesiologists score; BMI = body–mass index; eGFR = estimated glomerulofiltration rate; HALPN = hand-assisted laparoscopic partial nephrectomy; OPN = open partial nephrectomy; RALPN = robot-assisted laparoscopic partial nephrectomy; SD = standard deviation.
WHICH IS THE BEST IN PARTIAL NEPHRECTOMY
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Table 2. Perioperative Outcomes in the Three Cohorts
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HALPN (n = 89) Operative time (SD, minute) WIT (SD, minute) Length of hospitalization (SD, day) Decrease in eGFR (SD, mL/minute/1.73 m2) Resection margin (SD, cm) Duration of analgesic (SD, day) Postoperative complications (%)
172.9 19.4 5.9 3.20 0.35 5.40 4
(42.3) (6.7) (1.66) (5.44) (0.24) (1.24) (4.49)
RALPN (n = 147) 162.3 24.7 5.3 2.40 0.36 4.65 5
(32.2) (7.3) (1.41) (6.70) (0.26) (1.26) (3.4)
OPN (n = 354) 187.2 19.6 7.3 4.34 0.46 6.61 28
(43.8) (6.7) (2.06) (8.34) (0.36) (1.66) (7.91)
p-Value < 0.0001 < 0.0001 < 0.0001 0.028 0.0007 < 0.0001 0.13
ANOVA, chi-square test. WIT = warm ischemia time.
nephrometry scores were calculated. The three groups were compared in terms of perioperative outcomes by using a multivariate regression model, in which adjustments were made for potential confounders, namely, baseline demographic and tumor characteristics. Comparisons involving categorical and continuous variables were made by using the chi-square test and ANOVA, respectively. All reported pvalues were two sided, and a value of p < 0.05 was considered to indicate statistical significance. SPSS version 18.0 (IBM Corp., Armonk, NY) was used for statistical analyses.
Table 3. Linear Regression Model of Perioperative Outcomes Multivariate analysis Variable
Estimate (95% CI)
Operative time RALPN/HALPN - 8.91 ( - 19.5, 1.70) OPN/HALPN 15.11 (5.67, 24.56) Gender M/F 15.05 (7.66, 22.45) BMI 1.66 (0.60, 2.72) RENAL 3.24 (1.38, 5.09) nephrometry score WIT RALPN/HALPN 6.01 (4.21, 7.81) OPN/HALPN 0.42 ( - 1.17, 2.01) RENAL 0.88 (0.56, 1.20) nephrometry score Length of hospitalization (log) RALPN/HALPN - 0.11 ( - 0.17, - 0.05) OPN/HALPN 0.20 (0.14, 0.25) Duration of analgesic (log) RALPN/HALPN - 0.15 ( - 0.21,0.10) OPN/HALPN 0.20 (0.15, 0.24) Decrease in eGFR RALPN/HALPN - 0.11 ( - 2.05, 1.82) OPN/HALPN 1.13 ( - 0.60, 2.87) Age 0.11 (0.06, 0.16) ASA score 1.87 (0.59, 3.14) Solitary kidney 5.13 (0.91, 9.35) RENAL 0.72 (0.38, 1.06) nephrometry score CI = confidence intervals.
p-Value 0.09 0.002 < 0.001 0.002 0.001
< 0.001 0.60 < 0.001
0.001 < 0.001 < 0.001 < 0.001 0.90 0.20 < 0.001 0.004 0.01 < 0.001
Results
The demographic data are summarized in Table 1. Regarding the perioperative outcomes, the average operative times of the HALPN, RALPN, and OPN groups were 173, 162, and 187 minutes, respectively ( p < 0.001). The HALPN and RALPN groups did not differ significantly in terms of this variable ( p = 0.18). The RALPN group had the longest mean WIT (24.7 minutes). However, the HALPN and OPN groups did not differ significantly in terms of WIT (19.4 vs19.6 minutes, p = 0.85). The OPN group had the longest average hospitalization stay (7.3 days). Moreover, the HALPN group stayed significantly longer in hospital than the RALPN group (5.9 vs 5.3 days, p = 0.026). The OPN group also had a significantly longer duration of analgesic use (6.6 days) than the RALPN (4.6 days) or HALPN (5.4 days) group ( p < 0.001). The three groups differed significantly in terms of estimated glomerular filtration rate (eGFR) decrease; it was 3.20, 2.40, and 4.34 mL/minute/1.73 m2 for the HALPN, RALPN, and OPN groups, respectively ( p = 0.028) (Table 2). However, multivariate regression model analysis did not find that the operation type associated significantly with the eGFR decrease. By contrast, age, American Society of Anesthesiologists score (ASA score), solitary kidney status, and the RENAL nephrometry score all associated significantly with the eGFR decrease. However, multivariate regression model analysis showed that OPN associated significantly with a long operation time. Gender also associated significantly regardless of the operation type; PN took about 15 minutes longer in men than in women. Body–mass index also associated significantly with operative time; the higher the body– mass index (BMI), the longer the operation time (Table 3). The complications included hematuria, urine leak, hypoxia, transfusion, pesudoaneurysm, and wound dehiscence. The overall complication rates for the HALPN, RALPN, and OPN groups were 4.5%, 3.4%, and 7.9%, respectively (Tables 2 and 4). The three groups did not differ in terms of complication rates ( p = 0.13). Multivariate regression analysis revealed that only the RENAL nephrometry score was a significant factor for complication rate (odds ratio 1.49, 95% confidence intervals 1.22, 1.81) (Table 5). The surgical margins in all patients were negative. Discussion
HALPN was introduced by Jordan and Winslow in 1993 and is a practical option for small ( < 4 cm) renal masses.12,13 While two studies have compared HALPN with RALPN or OPN,14,15 they are disadvantaged by a small sample size or
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Table 4. Complications
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HALPN 4 (4.5%)
RALPN 5 (3.4%)
Clavien grade I
Hematuria (1)
Clavien grade II Clavien grade III-IV
— Pseudoaneurysm (1), urine leak (1), wound dehiscence (1)
by differences between the groups in terms of tumor characteristics. Therefore, to determine whether these three methods differ in terms of perioperative outcomes and complications, we designed the present study, which was reasonably sized and involved covariant-adjusted group comparisons. Although the retroperitoneal approach has several advantages that allow direct access to the renal artery, thus reducing the chance of organ injury, this approach is complicated by the small working space and relative paucity of distinct anatomical landmarks.6,16 Therefore, unless patients are not eligible for the transperitoneal approach, we prefer to employ the transperitoneal approach rather than the retroperitoneal approach. By contrast, most of the OPN surgeries in the present study involved the retroperitoneal approach. Moreover, there was variability in terms of whether ice was used when the pedicle was clamped in OPN; 22.8% of the OPN cases involved the use of ice. There was also some variability in terms of whether the nonclamp technique was used, if the tumor was superficial and peripheral clamping was not performed. This applied in four HALPN cases, one RALPN case, and 21 OPN cases. OPN is considered to be the gold standard treatment for small renal tumors as its renal functional outcomes and disease-specific survival are superior and equivalent to those of radical nephrectomy, respectively.17,18 However, compared with LPN, OPN associates with an increased convalescence time because it involves a large incision that produces intense pain. By contrast, LPN reduces recovery time while yielding similar oncologic and nephrologic outcomes. Indeed, one study of 1800 consecutive patients who underwent either
OPN 28 (7.9%)
Hypoxia (1), hematuria (1) Blood transfusion (1) Pseudoaneurysm (1), urine leak (1)
Ileus (4) Blood transfusion (17) Pseudoaneurysm (2), urine leak (2), wound dehiscence (3)
OPN or LPN reported that the LPN group had shorter operative times, less intraoperative blood loss, and a shorter length of hospital stay. However, it should be noted that the patients who underwent LPN were more likely than the patients undergoing OPN to have more peripheral and smaller tumors. Moreover, due to the greater number of surgical steps involved in LPN compared with OPN, LPN associated with longer WITs and a significant increase in the postoperative complication rate.19 To reduce the problems associated with such a difficult laparoscopic technique, RALPN was developed. It reduces surgeon fatigue and shortens the learning curve of LPN and has as a result largely replaced LPN.20 HALPN is also another traditional minimally invasive approach for PN. Thus, the three most commonly used PN techniques in our medical institution in the study period were HALPN, RALPN, and OPN. A previous study showed that HALPN associates with a shorter mean operation time than OPN (161 vs 191 minutes; p = 0.027). It also associates with less blood loss (120 vs 353 cc; p = 0.0003), a shorter WIT (27.0 vs 33.0 minutes; p = 0.035), and a smaller overall complication rate (18.3% vs 32.5%, p = 0.10).14 The present study also showed that HALPN associated with better outcomes than OPN in terms of most perioperative variables. This may reflect the fact that although HALPN is still a minimally invasive approach, it also allows tactile feedback that aids tumor perception and dissection and specimen extraction and reduces the WIT.21 The present study showed that HALPN associated with a shorter convalescence time than OPN. However, HALPN did not differ from OPN in terms of complication rates or eGFR decrease. Moreover, the WITs of these groups did not differ (19.4 vs 19.6 minutes,
Table 5. Independent Predictor of Complication Univariate OR (95% CI) Group RALPN/HALPN OPN/HALPN Age Gender M/F BMI ASA score Prior abdominal surgery Solitary kidney Right/left RENAL nephrometry score OR = odds ratio.
0.75 1.83 1.01 1.50 0.97 1.12 0.89 1.37 0.85 1.52
(0.20, (0.62, (0.98, (0.64, (0.95, (0.58, (0.26, (0.17, (0.44, (1.25,
2.86) 5.35) 1.04) 3.48) 0.99) 2.19) 2.99) 10.9) 1.66) 1.85)
Multivariable p-Value
OR (95% CI)
p-Value
0.67 0.27 0.47 0.35 0.64 0.73 0.85 0.76 0.64 < 0.001
0.96 (0.25, 3.77) 1.74 (0.58, 5.21)
0.95 0.32
1.49 (1.22, 1.81)
< 0.001
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WHICH IS THE BEST IN PARTIAL NEPHRECTOMY
p = 0.85). However, this contrasts with a previous study, which showed that HALPN has superior WIT compared with OPN.14 The present study also compared HALPN with RALPN. Unlike the equivalence of HALPN and OPN in terms of WIT, HALPN is associated with a shorter WIT (19.4 minutes) than RALPN (24.7 minutes; p < 0.001). This is significant because Thompson et al.22 showed that a high WIT associates with an acute risk of postoperative renal failure and an increased risk of postoperative stage IV chronic kidney disease (CKD). Thus, WIT is an important predictor of renal function preservation. However, the present study could not demonstrate a relationship between WIT and postoperative renal failure. Another study also found that RALPN does not yield remarkable benefits in terms of perioperative outcomes relative to HALPN; moreover, RALPN is associated with increased cost.15 Most of the advantages of HALPN over other laparoscopic techniques stem from the surgeon being able to use his or her hand during the surgery. When resecting a tumor after positioning a hilar clamp, a fingertip can bluntly dissect a mass, similar to what is achieved by using a blade handle in open surgery. Moreover, using the hand to enclose a defect can be both effective and prompt. Grasping and folding a kidney by hand is also helpful for approximating the defect surface. Moreover, unlike OPN, HALPN is performed in our institute by using a high-definition laparoscopic monitor that facilitates the meticulousness of the technique. It should, however, be noted that HALPN is more invasive than LPN or RALPN and can lead to wound problems and hernias. Furthermore, the hand can hinder laparoscopic vision during surgery. However, these problems are compensated by the great advantages yielded by the tactile feedback in HALPN. Moreover, although the open surgical technique is still considered to be the gold standard treatment in terms of renal function outcomes and disease-specific survival relative to radical nephrectomy,17,18 HALPN is also amenable to oncologic principles. The present study suggested that HALPN may achieve the superior outcomes of OPN relative to radical nephrectomy, while tending to reduce complications. This study has some limitations. First, there was a selection bias due to the use of different surgeons. Only HALPN was performed by one surgeon. Furthermore, although a multivariate regression model was employed, the study was not a randomized prospective study and thus it is subject to the inherent limitations of a retrospective analysis of observational data. Conclusions
Compared to OPN, HALPN associated with a shorter operative time and convalescence period. Compared to RALPN, HALPN generally did not have inferior perioperative outcomes; however, it did associate with a significantly longer convalescence period. The three approaches did not differ in terms of the complication rate. Disclosure Statement
The authors have no conflicts of interest to disclose. References
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2. Van Poppel H, et al. A prospective, randomised EORTC intergroup phase 3 study comparing the oncologic outcome of elective nephron-sparing surgery and radical nephrectomy for low-stage renal cell carcinoma. Eur Urol 2011;59: 543–552. 3. MacLennan S, et al. Systematic review of oncological outcomes following surgical management of localised renal cancer. Eur Urol 2012;61:972–993. 4. Antonelli A, et al. Elective partial nephrectomy is equivalent to radical nephrectomy in patients with clinical T1 renal cell carcinoma: Results of a retrospective, comparative, multi-institutional study. BJU Int 2012;109:1013–1018. 5. Ficarra V, et al. A multicentre matched-pair analysis comparing robot-assisted versus open partial nephrectomy. BJU Int 2014;113:936–941. 6. Ren T, et al. Transperitoneal approach versus retroperitoneal approach: A meta-analysis of laparoscopic partial nephrectomy for renal cell carcinoma. PLoS One 2014;9: e91978. 7. Wolf JS, Jr. Hand-assisted laparoscopy: Pro. Urology 2001; 58:310–312. 8. Benway BM, et al. Robot assisted partial nephrectomy versus laparoscopic partial nephrectomy for renal tumors: A multi-institutional analysis of perioperative outcomes. J Urol 2009;182:866–872. 9. Kowalczyk KJ, et al. Comparative effectiveness, costs and trends in treatment of small renal masses from 2005 to 2007. BJU Int 2013;112:E273–E280. 10. Strup S, et al. Laparoscopic partial nephrectomy: Handassisted technique. J Endourol 2005;19:456–459; discussion 459–460. 11. Gettman MT, et al. Robotic-assisted laparoscopic partial nephrectomy: Technique and initial clinical experience with DaVinci robotic system. Urology 2004;64:914–918. 12. Jordan GH, Winslow BH. Laparoendoscopic upper pole partial nephrectomy with ureterectomy. J Urol 1993;150: 940–943. 13. Wu Z, et al. A propensity-score matched comparison of perioperative and early renal functional outcomes of robotic versus open partial nephrectomy. PLoS One 2014;9: e94195. 14. DeVoe WB, et al. Hand-assisted laparoscopic partial nephrectomy after 60 cases: Comparison with open partial nephrectomy. Surg Endosc 2009;23:1075–1080. 15. Elsamra SE, et al. Hand-assisted laparoscopic versus robotassisted laparoscopic partial nephrectomy: Comparison of short-term outcomes and cost. J Endourol 2013;27:182– 188. 16. Marszalek M, et al. Laparoscopic partial nephrectomy: A matched-pair comparison of the transperitoneal versus the retroperitoneal approach. Urology 2011;77:109–113. 17. Mabjeesh NJ, Avidor Y, Matzkin H. Emerging nephron sparing treatments for kidney tumors: A continuum of modalities from energy ablation to laparoscopic partial nephrectomy. J Urol 2004;171(2 Pt 1):553–560. 18. Fergany AF, Hafez KS, Novick AC. Long-term results of nephron sparing surgery for localized renal cell carcinoma: 10-year followup. J Urol 2000;163:442–445. 19. Gill IS, et al. Comparison of 1,800 laparoscopic and open partial nephrectomies for single renal tumors. J Urol 2007; 178:41–46. 20. Haber GP, et al. Robotic versus laparoscopic partial nephrectomy: Single-surgeon matched cohort study of 150 patients. Urology 2010;76:754–758.
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21. Wolf JS, Jr., Seifman BD, Montie JE. Nephron sparing surgery for suspected malignancy: Open surgery compared to laparoscopy with selective use of hand assistance. J Urol 2000;163:1659–1664. 22. Thompson RH, et al. Every minute counts when the renal hilum is clamped during partial nephrectomy. Eur Urol 2010;58:340–345.
Address correspondence to: Bumsik Hong, MD, PhD Department of Urology Asan Medical Center University of Ulsan College of Medicine 88, Olympic-ro 43-gil Songpa-gu Seoul 138-736 Korea E-mail: [email protected]
Abbreviations Used ASA score ¼ American Society of Anesthesiologists score BMI ¼ body–mass index CI ¼ confidence intervals eGFR ¼ estimated glomerulofiltration rate HALPN ¼ hand-assisted laparoscopic partial nephrectomy OPN ¼ open partial nephrectomy OR ¼ odds ratio PN ¼ partial nephrectomy RALPN ¼ robot-assisted laparoscopic partial nephrectomy WIT ¼ warm ischemia time
