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International Journal of Urology (2014) 21, 1093–1096

doi: 10.1111/iju.12551

Original Article: Clinical Investigation

Long-term outcome of hand-assisted laparoscopic radical nephrectomy for T1 renal cell carcinoma Fumiya Hongo,1 Akihiro Kawauchi,2 Takashi Ueda,1 Atsuko Fujihara,1 Yasuyuki Naitoh,1 Terukazu Nakamura,1 Yoshio Naya,1 Kazumi Kamoi,1 Koji Okihara1 and Tsuneharu Miki1 1 Department of Urology, Kyoto Prefectural University of Medicine, Kyoto, and 2Department of Urology, Shiga University of Medical Science, Otsu, Japan

Abbreviations & Acronyms BMI = body mass index HALS-Nx = hand-assisted laparoscopic radical nephrectomy LAP-Nx = laparoscopic nephrectomy OPEN-Nx = open nephrectomy Correspondence: Fumiya Hongo M.D., Ph.D., Department of Urology, Kyoto Prefectural University of Medicine, 465 Kajii-cho, Kamigyo-ku, Kyoto 602-8566, Japan. Email: [email protected] Received 23 December 2013; accepted 4 June 2014. Online publication 14 July 2014

Objectives: To investigate the long-term outcomes of hand-assisted laparoscopic radical nephrectomy compared with those of open nephrectomy. Methods: Hand-assisted laparoscopic radical nephrectomy was carried out in 132 patients with T1 renal cell carcinoma (between November 1999 and November 2008). Their outcomes were compared with those of 61 patients treated with open nephrectomy. The durations of follow up were 6–121 months (median 65 months) and 7–146 months (median 84 months) in the hand-assisted laparoscopic radical nephrectomy and open nephrectomy groups, respectively. Results: The 7-year recurrence-free rates were 88.5 and 85.6% in the hand-assisted laparoscopic radical nephrectomy and open nephrectomy groups, respectively, showing no significant difference between the two groups. The 7-year cancer-specific survival rates were 92.3 and 91.4% in the hand-assisted laparoscopic radical nephrectomy and open nephrectomy groups, respectively, showing no significant difference between the two groups. Also, the 10-year recurrence-free rates were 85.4 and 78.1% in the hand-assisted laparoscopic radical nephrectomy and open nephrectomy groups, respectively. When changes in the recurrence-free rate were analyzed using the Kaplan–Meier method, no significant difference was observed between the two groups. The 10-year cancer-specific survival rates were 91.8 and 87.9% for hand-assisted laparoscopic radical nephrectomy and open nephrectomy, respectively, showing no significant difference between the groups. Conclusions: Hand-assisted laparoscopic radical nephrectomy might be comparable with open nephrectomy with regard to long-term cancer control.

Key words: hand-assisted method, laparoscopic surgery, long-term outcome, renal cell carcinoma.

Introduction Since it was reported by Clayman et al., many studies on laparoscopic nephrectomy have been carried out.1 A small intraoperative blood loss, and favorable perioperative and long-term outcomes of this surgical procedure for renal cell carcinoma, compared with those of laparotomy, have been reported, and so it can be applied as the first choice.2 There are intraperitoneal and retroperitoneal approaches for this surgical procedure with and without the hand-assisted method. Since it was initially reported in 1994,3,4 the advantages and disadvantages of the hand-assisted method have been discussed, and the method has been established.5–7 Many facilities use the hand-assisted procedure, because it is considered relatively easy to learn, but fewer studies on its anticancer effect have been reported. We have carried out hand-assisted laparoscopic nephrectomy using the retroperitoneal approach since November 1991.8,9 In the present study, we investigated the long-term outcomes by comparison with those in patients treated with laparotomy.

Methods The participants were 132 patients with renal cell carcinoma who were staged as T1 N0 M0 and underwent HALS-Nx at the Urology Department of Kyoto Prefectural University of Medicine, Kyoto, Japan, or its related hospitals between November 1999 and November 2008. After approval by the institutional review board, the data were retrospectively collected. The outcomes were compared with those of 61 patients at the same clinical stage who underwent open surgery © 2014 The Japanese Urological Association

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Table 1

Patients’ characteristics between the HALS-Nx and OPEN-Nx groups

Patients (n) Period Age (years) BMI (kg/m2) Sex (n) Male Female Laterality (n) Right Left Tumor size (mm)

HALS-Nx

OPEN-Nx

132 Nov/1999–Nov/2008 62.3 ± 11.1 23.6 ± 3.4

61 Oct/1996–Apr/2008 62.0 ± 12.9 22.8 ± 3.0

94 38

P = 0.8754 P = 0.1014 P = 0.5732

41 20 P = 0.5529

67 64 39.83 ± 13.36

34 27 39.13 ± 12.8

P = 0.7276

during the same period. HALS-Nx was carried out as previously reported.8,9 Briefly, the patient was placed in the complete lateral position with the affected side up. A skin incision was made and a trocar was positioned as previously reported: a 7-cm pararectal incision was made at the navel level, and the posterior sheath of the rectus abdominis muscle was separated from the peritoneum through this incision, reaching the retroperitoneum, and the retroperitoneal procedure was macroscopically initiated. LAP DISC (Hakko, Nagano, Japan) was attached, and a 12-mm trocar was inserted into it. The assistant inserted his/her left and right hands through the LAP DISC when the affected side was present on the right and left sides, respectively. Hand assistance was carried out mainly for palpation to rapidly identify the great blood vessels and renal artery or dissection of the perirenal tissue and excision of a free organ through the wound. The Clavien Classification of Surgical Complications was used for surgical-related complications.10

Statistical methods For statistical analysis, the χ2-test and t-test were used. Survival was analyzed using the Kaplan–Meier method, followed by the log–rank test. All analyses were carried out using JMP 10.0.2 (SAS Institute, Cary, NC, USA).

Results The patient background and surgical outcomes are shown in Table 1. There were no significant differences in the age (62.3 ± 11.1 years vs 62.0 ± 12.9 years), body mass index (23.6 ± 3.4 vs 22.8 ± 3.0) or tumor size (39.83 ± 13.36 mm vs 39.13 ± 12.8 mm) between the HALS-Nx and OPEN-Nx groups. Regarding the surgical outcomes, the operation times were 213 ± 68.7 and 212 ± 69.6 min in the HALS-Nx and OPEN-Nx groups, respectively, showing no significant difference. The blood losses were 188 ± 216 and 212 ± 69.6 cc, respectively, showing a favorable result in the HALS-Nx group. Complications occurred in four patients in the HALS-Nx group and in three patients in the OPEN-Nx group. In the HALS-Nx group, surgery was switched to open surgery in one patient, and the cause was bleeding from the renal vein. A blood transfusion was carried out in another patient. An intestinal perforation was found when abdominal pain developed in a patient after surgery, and this was repaired by laparotomy (grade III). Pan1094

Table 2

Histological findings between the HALS-Nx and OPEN-Nx groups

Stage pT1 pT2 pT3a pT3b Grade 1 2 3 Subtype Clear Non-clear Microvascular invasion V (+) V (−)

HALS-Nx (%)

OPEN-Nx (%)

125 (94.7) 0 6 (4.5) 1 (0.8)

57 (93.4) 0 2 (3.3) 2 (3.3)

45 (34.1) 84 (63.6) 3 (2.3)

23 (37.7) 34 (55.7) 4 (6.6)

116 (87.9) 16 (12.1)

51 (83.6) 10 (16.4)

19 (14.4) 113 (85.6)

12 (19.7) 49 (80.3)

P = 0.5989

P = 0.2603

P = 0.4190

P = 0.3535

creatic injury occurred in one patient, and it was healed by conservative treatment (grade I), such as drain placement. In the OPEN-Nx group, small injury of the spleen occurred in one patient (grade I), and transfusion was carried out to two patients. No significant difference was noted in the incidence of complications between the two groups. The histopathological findings are shown in Table 2. Seven and four cases were pT3a-b in the HALS-Nx and OPEN-Nx groups, respectively. Regarding atypia, the HALS-Nx and OPEN-Nx groups included nine and four G3 cases, respectively. There were no significant differences between the HALS-Nx and OPEN-Nx groups. Also, regarding subtype type and microscopic invasion, there were no significant differences between the two groups. The duration of follow up was 6–121 months (median 65 months) in the HALS-Nx group, and no port site or local recurrence was observed. In the OPEN-Nx group, the duration of follow up was 7–146 months (median 84 months). The 5-year recurrence-free rates were 93.9 and 93.4% in the HALS-Nx and OPEN-Nx groups, respectively. The 7-year recurrence-free rates were 88.5 and 85.6% in the HALS-Nx and OPEN-Nx groups, respectively. The 10-year recurrence-free rates were 85.4 and 78.1% in the HALS-Nx and OPEN-Nx groups, respectively. Changes in the recurrence-free rate were analyzed using the Kaplan–Meier method, but no significant difference was noted between the two groups (Fig. 1), nor was there a significant difference in the cancer-specific 5-year survival rate between the two groups (95.5 vs 94.3%, respectively) and 7-year survival rate between the two groups (92.3 vs 91.4%, respectively; Fig. 2). The 10-year survival rate between the two groups was 91.8 versus 87.9%, respectively.

Discussion The retroperitoneal approach is advantageous in that a past medical history of intra-abdominal surgery is not problematic, the abdominal organs, such as the intestine, are less influenced, and the hilum of the kidney can be readily reached, but the working space is narrow, which is disadvantageous.24 At present, our hospital uses the intraperitoneal or retroperitoneal © 2014 The Japanese Urological Association

Long-term outcome of HALS nephrectomy

Disease-free survival rate

100 80

P = 0.6276

60 40 20 0

0

20

40

HALS-Nx 122 OPEN-Nx 55

102 45

60 80 100 120 Follow-up time (months) No. patients at review 69 36 16 39 32 26

140

160

1 16

Fig. 1 Disease-free survival rate by surgical procedure. The 7-year recurrencefree rates were 88.5% and 85.6% in the HALS-Nx and OPEN-Nx groups, respectively. Also, the 10-year recurrence-free rates were 85.4% and 78.1% in the HALS-Nx and OPEN-Nx groups, respectively. Changes in the recurrence-free rate were analyzed using the Kaplan–Meier method, but no significant difference was , HALS-Nx; , OPEN-Nx. noted between the two groups.

Cancer-specific survival rate

100 80

P = 0.6481

60 40 20 0

0

20

HALS-Nx 124 OPEN-Nx 55

40

103 46

60 80 100 120 Follow-up time (months) No. patients at review 71 37 18 39 33 27

140

160

1 17

Fig. 2 Cancer-specific survival rate curve by surgical procedure. The 7-year cancer-specific survival rates were 92.3% and 91.4% in the HALS-Nx and OPEN-Nx groups, respectively, showing no significant difference between the two groups. The 10-year cancer-specific survival rates were 91.8% and 87.9% in the HALS-Nx and OPEN-Nx groups, respectively, showing no significant difference between , HALS-Nx; , OPEN-Nx. the two groups.

approach without hand-assisted for nephrectomy. In 1999, we started laparoscopic nephrectomy with the hand-assisted method, because the hand-assisted method is considered useful as the working space preparation, search for the great vessels and renal artery by palpation, assistance for dissection of the perirenal tissue, and excision of a free organ out of the wound can be carried out by hand.12 The learning curve is short, compared with that of LAP-Nx, which might also be advantageous.13 Studies on the comparison of HALS-Nx and LAP-Nx reported that, although the operation time (of HALS-Nx) was short, postoperative recovery after LAP-Nx was more favorable.14,15 Regarding cancer control, the kidney is elevated through the posterior side to access the renal stem in the retroperitoneal © 2014 The Japanese Urological Association

lateral approach, in which cancer dissemination by compression is of concern. This problem can be overcome by the present procedure in which the kidney can be elevated atraumatically while the assistant manually moves the tumor region away, and the palpation of blood vessels might shorten the time to reach the processing of renal blood vessels. In previous reports on the outcome, the 5-year recurrencefree rate after LAP-Nx for T1-T2 renal cell carcinoma was 91–94%, and the 5-year cancer-specific survival rate was 94–98%.16–19 In HALS-Nx, the 5-year recurrence-free rate and the 5-year cancer-specific survival rate for T1-T2 renal cell carcinoma was 90.7 and 94.4%, respectively.20 In other reports, the 4-year disease-free and overall survival rates after HALS-Nx for T1-T2 renal cell carcinoma were 88% and 100%, respectively.21 Also, the intraperitoneal approach was mainly taken in both previous reports.20,21 In a previous study, a comparison of the 5- and 10-year recurrence-free survival rates of the laparoscopic and open groups showed no significant differences, as the cancer-specific survival rate in T1-2 patients treated with LAP-Nx was 97% at year 5 and year 10.17 In addition, the 5- and 10-year cancer-specific survival rates of the laparoscopic and open groups showed no significant differences.17,22 Also, the cancer-specific survival rate for >7 cm renal tumor after laparoscopic nephrectomy was 89.5% at year 5 and year 10.21 We previously investigated the usefulness of HALS-Nx for T1-2N0M0 carcinoma, and observed that the incidence of complications was comparable with that in OPEN-Nx,23 and so were the 5-year recurrence-free rate (HALS-Nx 92% vs OPEN-Nx 91%) and 5-year cancer-specific survival rate (HALS-Nx 92% vs OPEN-Nx 94%).24 In the present study, the long-term outcome after HALS-Nx was investigated in T1 cases, but no significant differences were noted in the recurrence-free or cancer-specific survival rate from those after OPEN-Nx. At present, our hospital uses the transabdominal or retroperitoneal approach, or laparoscopic partial nephrectomy depending on the tumor size and location, but HALS-Nx might also be useful as a procedure complementing the disadvantages of the retroperitoneal approach. The present study suggested that the long-term safety and curability of HALS-Nx are comparable with those of OPENNx. Unlike other cancer types, the recurrence and metastasis of renal cell carcinoma occur over a prolonged period. To discuss the safety and curability of this procedure, a longer follow-up period is necessary.

Conflict of interest None declared.

References 1 Clayman RV, Kavoussi LR, Soper N et al. Laparoscopic nephrectomy: initial case report. J. Urol. 1991; 146: 278–82. 2 Dunn MD, Portis AJ, Shalhav AL et al. Laparoscopic versus open radical nephrectomy: a 9-yearexperience. J. Urol. 2000; 164: 1153–9. 3 Tierney JP, Oliver SR, Kusminsky RE, Tiley EH, Bolan JP. Laparoscopic radical nephrectomy with intra-abdominal manipulation. Min. Invas. Ther. 1994; 3: 303–5. 4 Nakada SY, Moon TD, Gist M et al. Use of the PneumoSleeve as an adjunct in laparoscopic nephrectomy: comparison to standard laparoscopic nephrectomy. Urology 1997; 49: 612–13.

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5 Wolf JS Jr, Moon TD, Nakada SY et al. Hand assisted laparoscopic nephrectomy: comparison to standard laparoscopic nephrectomy. J. Urol. 1998; 160: 22–7. 6 Wolf JSJ. Hand-assisted laparoscopy: pro. Urology 2001; 58: 310–12. 7 Gill IS. Hand-assisted laparoscopy: con. Urology 2001; 58: 313–17. 8 Kawauchi A, Fujito A, Miki T. Hand assisted retroperitoneoscopic radical nephrectomy. Jpn. J. Endourol. ESWL 2003; 16: 24–9. 9 Kawauchi A, Fujito A, Ukimura O et al. Hand assisted retroperitoneoscopic radical nephrectomy: initial experience. Int. J. Urol. 2002; 9: 480–4. 10 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. 11 Gill IS, Schweizer D, Hobart MG et al. Retroperitoneal laparoscopic nephrectomy: the Cleveland Clinic experience. J. Urol. 2000; 163: 1665–70. 12 Tanaka M, Tokuda N, Koga H et al. Hand assisted laparoscopic radical nephrectomy for renal cell carcinoma using new abdominal wall sealing device. J. Urol. 2000; 164: 314–18. 13 Kawauchi A, Fujito A, Soh J et al. Lerning curve of hand-assisted retroperitoneoscopic nephrectomy in less-experienced laparoscopic surgeons. Int. J. Urol. 2005; 12: 1–5. 14 Nelson CP, Wolf JSJ. Comparison of hand-assisted laparoscopic radical nephrectomy for suspected renal cell carcinoma. J. Urol. 2002; 167: 1989–94.

15 Matin SF, Dhanani N, Acosta M et al. Conventional and hand-assisted laparoscopic radical nephrectomy: comparative analysis of 271 cases. J. Endourol. 2006; 20: 891–4. 16 Permpongkosol S, Chan DY, Link RE et al. Long-term survival analysis after laparoscopic radical nephrectomy. J. Urol. 2005; 174: 1222–5. 17 Borin JF. Laparoscopic radical nephrectomy: long-term outcomes. Curr. Opon. Urol. 2008; 18: 139–44. 18 Saika T, Ono Y, Hattori R et al. Long-term outcome of laparoscopic radical nephrectomy for pathologic T1 renal cell carcinoma. Urology 2003; 62: 1018–23. 19 Portis AJ, Yan Y, Landman J et al. Long-term followup after laparoscopic radical nephrectomy. J. Urol. 2002; 167: 1257–62. 20 Chung SD, Huang KH, Lai MK et al. Long-term follow-up of hand-assisted laparoscopic radical nephrectomy for organ-confined renal cell carcinoma. Urology 2007; 69: 652–5. 21 Harano M, Eto M, Omoto K et al. Long-term outcome of hand-assisted laparoscopic radical nephrectomy for localized stage T1/T2 renal-cell carcinoma. J. Endourol. 2005; 19: 803–7. 22 Hattori R, Osamu K, Yoshino Y et al. Laparoscopic radical nephrectomy for large renal-cell carcinomas. J. Endourol. 2009; 23: 1523–6. 23 Okihara K, Kawauchi A, Yoneda K et al. Hand assisted retroperitoneoscopic radical nephrectomy. Jpn. J. Endourol. ESWL 2005; 18: 48–52. 24 Kawauchi A, Yoneda K, Fujito A et al. Oncological outcome of hand-assisted laparoscopic radical nephrectomy. Urology 2007; 69: 53–6.

Editorial Comment Editorial Comment from Dr Golebiewski to Long-term outcome of hand-assisted laparoscopic radical nephrectomy for T1 renal cell carcinoma In this issue of the journal, Hongo et al. retrospectively evaluated the long-term outcomes of hand-assisted laparoscopic radical nephrectomy (HALS-Nx) versus open nephrectomy (OPEN-Nx) in patients with T1 renal cell carcinoma (RCC).1 The median duration of the follow up was 65 and 84 months in the HALS-Nx and OPEN-Nx groups, respectively. Regarding the surgical outcomes, the operation times and complication rates showed no significant difference between the two groups. However, the blood loss was significantly lower in the HALS-Nx group. During the follow-up period, no significant differences were noted in either the 7- and 10-year recurrencefree rates or the cancer-specific 7- and 10-year survival rates between the two groups. The authors conclude that the longterm safety and curability of HALS-Nx is comparable with that of OPEN-Nx. The hand-assisted laparoscopic surgical technique has not compromised oncological outcomes in the RCC patients. Furthermore, the complication rates have been shown to be comparable with the open technique. Their findings were in agreement with those of other reports.2,3 The limitations of the present study included its retrospective nature and selection bias. A prospective, randomized trial of HALS-Nx and OPEN-Nx should be considered as a more objective and informative assessment of the outcomes of those surgical techniques in RCC patients. Laparoscopic radical nephrectomy (LRN) has become a standard treatment modality for patients with localized RCC. In long-term follow up, LRN has shown excellent oncological outcome, equal to open surgery for both stage T1 and T2 renal tumors.3,4 However, no consensus has yet been established regarding the best laparoscopic access for LRN. Each technique offers advantages and disadvantages. Hand-assisted 1096

LRN offers morbidity and recovery that are comparable with those of standard laparoscopy. The benefits of hand-assisted LRN include shorter learning curve, direct manual control of operative field, easier intact specimen removal and shorter operative time. In the analysis presented by Silberstein, handassisted nephrectomy was associated with significantly less operative blood loss and risk of open conversion than was pure laparoscopic nephrectomy.5 The data presented support the role of hand-assisted laparoscopic nephrectomy as one of the treatment options for renal cancer when nephron-sparing surgery is not suitable. To assess the true oncological efficacy of the procedure, a longer follow-up period (>10 years) is necessary. Based on the current knowledge, one could anticipate the same excellent results of hand-assisted LRN that have been shown in conventional radical laparoscopic nephrectomy. Surgeons’ experience and personal preference remain the most important factors that guide their choice of laparoscopic technique, but it has to be acknowledged that the treatment for the patient with localized RCC needs to be highly individualized. Therefore, it is crucial for surgeons to access unbiased information regarding the outcome of different laparoscopic techniques to help them make the choice that best suits the individual patient. Andrzej Golebiewski M.D., Ph.D. Department of Surgery and Urology for Children and Adolescents, Medical University of Gdansk, Gdansk, Poland [email protected] DOI: 10.1111/iju.12567 © 2014 The Japanese Urological Association

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Long-term outcome of hand-assisted laparoscopic radical nephrectomy for T1 renal cell carcinoma.

To investigate the long-term outcomes of hand-assisted laparoscopic radical nephrectomy compared with those of open nephrectomy...
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