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Table of Contents
ORIGINAL ARTICLE
Year : 2018  |  Volume : 29  |  Issue : 1  |  Page : 33-37

Do transperitoneal and retroperitoneal hand-assisted laparoscopic nephroureterectomy have different effects on intravesical recurrence?


1 Department of Urology, National Cheng Kung University Hospital, Tainan, Taiwan
2 Department of Urology, National University Hospital, Taipei, Taiwan

Date of Web Publication23-Feb-2018

Correspondence Address:
Che-Yuan Hu
National Cheng Kung University Hospital, Tainan
Taiwan
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/UROS.UROS_14_17

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  Abstract 

Objectives: Some studies have shown that in patients with upper tract urothelial carcinoma (UTUC) who have undergone hand-assisted laparoscopic nephroureterectomy (HALNU), the narrow working space and inevitable manipulation that occurs during the retroperitoneal approach (RP-HALNU) enhances tumor cell seeding in the bladder mucosa. This study was an attempt to investigate the differences in intravesical recurrence between transperitoneal HALNU (TP-HALNU) and RP-HALNU. Patients and Methods: From 1999 to 2011, a total of 197 patients with UTUC were enrolled. After excluding those with a previous history of bladder cancer, 170 patients were analyzed. Sixty-five of these underwent RP-HALNU, and 105 of these underwent TP-HALNU. The median follow-up periods were 39.2 and 46.2 months. Tumor location was divided into three groups: In the renal pelvis, in the ureter, and in both the renal pelvis and ureter. Results: There was no significant difference in the intravesical recurrence rate in relation to the different surgical approaches (P = 0.10), but tumor location in both the renal pelvis and ureter significantly increased the risk (hazard ratio [HR] = 3.11, P = 0.01). In addition, advanced T stage (HR = 9.63, P < 0.01) was the only significant risk factor related to death. Conclusions: In patients with UTUC, tumor location in both the renal pelvis and ureter determined higher susceptibility to intravesical recurrence. However, different surgical approaches to HALNU were not a significant risk factor for intravesical recurrence.

Keywords: Hand-assisted laparoscopic nephroureterectomy, intravesical recurrence, survival rate, tumor stage, upper tract urothelial carcinoma


How to cite this article:
Hu CY, Huang CY, Huang KH, Tai HC, Lin YM, Tai TY. Do transperitoneal and retroperitoneal hand-assisted laparoscopic nephroureterectomy have different effects on intravesical recurrence?. Urol Sci 2018;29:33-7

How to cite this URL:
Hu CY, Huang CY, Huang KH, Tai HC, Lin YM, Tai TY. Do transperitoneal and retroperitoneal hand-assisted laparoscopic nephroureterectomy have different effects on intravesical recurrence?. Urol Sci [serial online] 2018 [cited 2022 Aug 13];29:33-7. Available from: https://www.e-urol-sci.com/text.asp?2018/29/1/33/226028


  Introduction Top


Laparoscopic nephroureterectomy (LNU) was introduced in 1991 by Clayman et al.[1] It is associated with lower postoperative morbidity rates and shorter hospital stays as compared with open nephroureterectomy (ONU).[2] However, a longer operating time, the need for laparoscopic experience, and a steep learning curve are the main problems encountered with this approach. Hand-assisted LNU (HALNU) has the merits of both ONU and LNU and was first introduced as the transperitoneal approach (TP) by Wolf et al.,[3] in 1998. Using this technique, the surgeon will insert one hand into the patient's body while pneumoperitoneum is still maintained. By taking advantage of tactile sensation and blunt manual dissection by hand, this method can decrease the time needed for the operation and also allows the surgeon to perform minimally invasive procedures.[4] HALNU with the retroperitoneal approach (RP) was then developed and was first described in 2000 by Igarashi et al.[5]

Recently, Kamihira et al.[6] reported the oncological outcomes of 1003 patients who underwent LNU (pure LNU, 722 cases; HALNU, 279 cases). At a median follow-up of 20 months, the use of the hand-assisted approach was found to be associated with a higher intravesical recurrence rate (P < 0.01). Furthermore, they divided these 279 HALNU patients into groups who underwent the TP or RP approaches, and the RP group had a significantly higher risk of intravesical recurrence than the TP group. They hypothesized that hand manipulation in the relatively smaller cavity in the RP group may enhance tumor cell seeding and may thus result in an increased intravesical recurrence rate. However, their paper did not present any detailed results comparing the two groups. In addition, they did not exclude those patients with a previous history of bladder cancer and did not present any information about the timing of ureter ligation in this multi-center study. Moreover, considerable variations existed in the bladder cuff resectioning methods.

To better determine if these two surgical methods (TP-HALNU vs. RP-HALNU) really affect intravesical recurrence, we compared the two surgical techniques in terms of oncological outcomes with control of the factors outlined above.


  Patients and Methods Top


From 1999 to 2011, a total of 197 patients with upper tract urothelial carcinoma (UTUC) were enrolled from a single medical center. After excluding those with a previous history of bladder cancer, 170 patients were finally analyzed. Sixty-five of these patients underwent RP-HALNU, and 105 underwent TP-HALNU. In the TP-HALNU group, we made a 7 cm Gibson's incision as a site for the hand port before entering the peritoneal cavity. Ureter identification and ligation were done in the RP space, and then, we opened the peritoneum and inserted a hand into the peritoneal cavity. Pneumoperitoneum was created, and air tightness was ensured using a GelPort laparoscopic system. One camera port was inserted near the paraumbilical region, and one working port was inserted near the subcostal region. Radical nephrectomy and residual ureter dissection were done with hand manipulation and the use of a laparoscopic device. The remaining ureter connection to the bladder and ureteral orifice were identified through gentle traction on the ureter, and a transaction was done. Suturing of the bladder cuff and specimen extraction was completed through the open Gibson's wound. In the RP-HALNU group, we made a Gibson's incision and did the ureter identification and ligation in the RP space. Then, we set up the GelPort laparoscopic system without opening the peritoneum. We created the retroperitoneal space by manual dissection. Pneumoretroperitoneum was done after that. The camera and working ports were inserted near the subcostal region. The remaining radical nephrectomy, ureter dissection, and bladder cuff resection were similar to those used in the TP-HALNU procedures. Ureter ligation was regularly done before any manipulation of the kidney, and we did not give prophylactic intravesical chemotherapy after HALNU in either group.

The patients were classified as “with previous bladder cancer history” if they had suffered from bladder cancer before the nephroureterectomy, and if not, they were classified as “without previous bladder cancer history.” Tumor location was divided into three groups for statistical analysis: The renal pelvis, ureter, and both the renal pelvis and ureter. Techniques were divided into two groups: TP or RP approaches with hand assistance. The UTUC grading and staging were performed according to the 1999 World Health Organization grade classification and the 2002 tumor, node, metastasis staging system.[7] If carcinoma in situ was noted along with Ta (noninvasive urothelial carcinoma), it was categorized into “Tis.” Otherwise, if carcinoma in situ was noted along with T1~T4 (invasive urothelial carcinoma), it was categorized into T1 to T4 in relation to the most severe stage of the specimen. The follow-up schedule was as follows: Computed tomography examinations were performed at 6-month intervals in the 1st year, and then every year thereafter. Evaluation of bladder recurrence was performed first with cystoscopy at the 3rd month, at the sixth and 12th month in the 1st year, and then, every 6 months or when there were clinically-indicated symptoms such as hematuria, suprapubic pain, or persistent irritable bladder. The clinical data included patient survival rates and bladder recurrence-free survival rates. “Recurrence-free survival time” was defined as the period between the date of the first operation for the original disease and the date of the first bladder recurrence. In addition, we also defined “overall survival time” as the period between the date of the first operation for the original disease and the patient's date of death.

The Kaplan–Meier curve was used to compare the intravesical recurrence-free survival rates between patients with and without a previous history of bladder cancer. Clinicopathologic factors in each group were compared using the Mann–Whitney U-test, Chi-square, and Fisher's exact test. Intravesical recurrence-free survival and overall survival were analyzed using the Cox proportional hazard ratio (HR) model. P < 0.05 was considered statistically significant.


  Results Top


Of the 197 patients with UTUC, a significantly higher intravesical recurrence rate (P < 0.001) was noted in the 27 patients with a previous history of bladder cancer [Figure 1]. To avoid its effect on intravesical recurrence after HALNU, patients with a previous history of bladder cancer were excluded from the subsequent statistical analysis. Of the remaining 170 patients, 65 underwent RP-HALNU, and 105 underwent TP-HALNU. The median follow-up periods were 39.2 and 46.2 months, respectively. The clinicopathological data of “patients without previous history of bladder cancer” is shown in [Table 1], with no significant differences in age, gender, body mass index, smoking, or previous history of the end-stage renal disease (ESRD) before HALNU. The pathological results were also comparable between the two groups. There were no significant differences in tumor location, grade, T stage, or N stage.
Figure 1: Kaplan–Meier curve to demonstrate the intravesical recurrence-free survival rate with/without a previous history of bladder cancer in the total of 197 upper tract urothelial carcinoma patients

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Table 1: Comparison of clinicopathological data in the 170 patients without a previous history of bladder cancer after being divided into retroperitoneal- and transperitoneal-hand-assisted laparoscopic nephroureterectomy groups

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Bladder recurrence developed in 26 (40.0%) patients in the RP-HALNU group and 30 (28.6%) patients in the TP-HALNU group. The median time to bladder recurrence was 29.5 months in the RP-HALNU group and 34.6 months in the TP-HALNU group. [Table 2] shows the results of the univariate and multivariate analyses of oncological outcomes with regard to intravesical recurrence. In the univariate analysis, there were no significant differences in intravesical recurrence among risk factors such as age, gender, smoking, and previous history of ESRD. Neither advanced T stage (T3-4) nor N stage (N1-3) were significantly different between the two groups. However, a significantly increased risk of intravesical recurrence was observed in groups where tumors were located in both the renal pelvis and ureter, as compared with groups where tumors were located in the renal pelvis only (HR = 2.64, P = 0.01). There was no significant difference in intravesical recurrence between the two surgical approaches of HALNU (HR = 1.50, P = 0.11). When age, gender, tumor grade, tumor location, T stage, N stage, and surgical approaches were adjusted, tumor in both the renal pelvis and ureter still remained as the only significant risk factor for intravesical recurrence (HR = 3.11, P = 0.01). Surgery carried out using the RP approach did not increase the risk of intravesical recurrence (HR = 1.73, P = 0.10). The results of the univariate and multivariate analyses for the overall death rate are shown in [Table 3]. Tumor in both the renal pelvis and ureter was not the risk factor for overall death (HR = 1.71, P = 0.40), and neither was the method of surgical approach (HR = 1.53, P = 0.27). Age, gender, smoking, previous history of ESRD, and N stage also did not significantly impact the overall death rate. In contrast, advanced T stage (T3, T4) had a significant impact on overall survival in the univariate analysis (HR = 5.36, P < 0.01). After adjustment for age, sex, tumor grade, T stage, N stage, and surgical approaches, the advanced T stage still increased the risk of overall death (HR = 9.63, P < 0.01).
Table 2: Univariate and multivariate analyses of the risk of intravesical recurrence in the 170 patients without a previous history of bladder cancer

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Table 3: Univariate and multivariate analyses of the risk of overall death in the 170 patients without a history of previous bladder cancer

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  Discussion Top


To the best of our knowledge, this is the first study to compare the long-term intravesical recurrence rate for TP and RP approaches to HALNU, with control of previous bladder cancer history. Since bladder cancer history had a key impact on intravesical recurrence [Figure 1], we excluded those patients with previous bladder cancer from our study to provide more accurate results than other similar studies. The oncological outcomes revealed no significant difference in the intravesical recurrence rate between these two kinds of surgical approaches. Tumor location in both the renal pelvis and ureter and advanced T stage were determined to be the only risk factors for intravesical recurrence and overall death, respectively.

The study from Kamihira et al.[6] revealed that HALNU was associated with a higher intravesical recurrence rate than pure LNU. When they divided patients into groups that underwent TP-HALNU or RP-HALNU, they found the latter had a significantly higher intravesical recurrence rate. However, they did not exclude those patients with a history of previous bladder cancer. In addition, a lack of consistency in the timing of ureter ligation and the methods of bladder cuff resection are also major concerns with this earlier work. In our study, both groups of patients underwent ureter ligation before the manipulation of the kidney. The bladder cuff was also resected by traditional open excision from the Gibson wound. This is similar to the technique used during the ONU, the gold standard of nephroureterectomy. The advantages of the open technique are its minimized risk of tumor spillage and the lower probability of incomplete bladder cuff excision under direct vision.[8]

Matsui et al.[9] compared 68 patients who underwent ONU with 21 patients who underwent RP-LNU. At a median follow-up period of 39.7 months, RP-LNU was found to increase the risk of intravesical recurrence (HR = 2.24, P = 0.04). Due to no early ligation of the ureter before kidney manipulation, tumor violation was thought to be responsible for the cancer cells seeding in the bladder cavity. Surgeons now try to clip the ureter distal to the tumor site immediately after controlling the renal artery. In a series of 47 patients who underwent ONU and 18 patients who underwent RP-LNU, Kume et al.[10] inferred that prolonged operating time, and not the laparoscopic approach, was a significant factor for a higher intravesical recurrence rate (HR = 5.56; P = 0.03). However, they did not ligate the ureter during the surgery in any patient. This result indicated that intraoperative renal manipulation for an extensive time has a strong correlation with intravesical recurrence. Earlier ureteral ligation may thus be a key step in prevention.

The present study showed that patients whose tumors were located in both the renal pelvis and the ureter were significantly more likely to develop intravesical recurrence. However, the intravesical recurrence rate did not significantly differ when the tumor was only in one place, either the renal pelvis or ureter. This result is inconsistent with the findings of Muntener et al.[11] They examined 39 patients who underwent LNU for UTUC and found that those with ureteral tumors were more likely to experience intravesical recurrence than those with renal pelvic tumors (P = 0.03). However, the number of patients in their study was rather limited, and they only performed univariate analysis for the intravesical recurrence. With regard to overall survival, the present study showed that advanced tumor stage remained the main risk factor for patient death, and other series support this finding.[11],[12],[13]

One of the limitations of our research is its retrospective design. In addition, we lacked some important covariables such as tumor size or lymphovascular invasion, the detailed stage distribution of intravesical recurrence, and the operation time in different surgical approaches. However, most of the intravesical recurrence was noninvasive bladder cancer due to the close follow-up schedule. The total operation time was also around 2 h in either TP approach or RP approach. The method of surgical approach was decided by surgeon preference, not by randomized control. Therefore, a prospective study that compares oncological results between early and delayed ureteral ligation and between RP-HALNU and TP-HALNU may help to clarify these issues.


  Conclusions Top


Different surgical approaches to HALNU did not have any significantly different effects on intravesical recurrence. Tumor location in both the renal pelvis and ureter was the only significant risk factor for intravesical recurrence after controlling for the previous history of bladder cancer and the timing of ureter ligation. In addition, advanced tumor stage was the only deciding factor for survival rate.

Acknowledgments

The authors would like to thank the National Cheng Kung Hospital Clinical Research Center for funding this project. Protocol number/IRB number: CKUH-1U5U3UI2/B-ER-IU4-276.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

 
  References Top

1.
Clayman RV, Kavoussi LR, Figenshau RS, Chandhoke PS, Albala DM. Laparoscopic nephroureterectomy: Initial clinical case report. J Laparoendosc Surg 1991;1:343-9.  Back to cited text no. 1
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Rassweiler JJ, Schulze M, Marrero R, Frede T, Palou Redorta J, Bassi P, et al. Laparoscopic nephroureterectomy for upper urinary tract transitional cell carcinoma: Is it better than open surgery? Eur Urol 2004;46:690-7.  Back to cited text no. 2
    
3.
Wolf JS Jr., Moon TD, Nakada SY. Hand assisted laparoscopic nephrectomy: Comparison to standard laparoscopic nephrectomy. J Urol 1998;160:22-7.  Back to cited text no. 3
    
4.
Landman J, Lev RY, Bhayani S, Alberts G, Rehman J, Pattaras JG, et al. Comparison of hand assisted and standard laparoscopic radical nephroureterectomy for the management of localized transitional cell carcinoma. J Urol 2002;167:2387-91.  Back to cited text no. 4
    
5.
Igarashi T, Tobe T, Mikami K, Suzuki H, Ichikawa T, Ito H, et al. Gasless, hand-assisted retroperitoneoscopic nephroureterectomy for urothelial cancer of the upper urinary tract. Urology 2000;56:851-3.  Back to cited text no. 5
    
6.
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Rouprêt M, Babjuk M, Compérat E, Zigeuner R, Sylvester R, Burger M, et al. European guidelines on upper tract urothelial carcinomas: 2013 update. Eur Urol 2013;63:1059-71.  Back to cited text no. 7
    
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Macejko AM, Pazona JF, Loeb S, Kimm S, Nadler RB. Management of distal ureter in laparoscopic nephroureterectomy – A comprehensive review of techniques. Urology 2008;72:974-81.  Back to cited text no. 8
    
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Matsui Y, Utsunomiya N, Ichioka K, Ueda N, Yoshimura K, Terai A, et al. Risk factors for subsequent development of bladder cancer after primary transitional cell carcinoma of the upper urinary tract. Urology 2005;65:279-83.  Back to cited text no. 9
    
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Kume H, Teramoto S, Tomita K, Nishimatsu H, Takahashi S, Takeuchi T, et al. Bladder recurrence of upper urinary tract cancer after laparoscopic surgery. J Surg Oncol 2006;93:318-22.  Back to cited text no. 10
    
11.
Muntener M, Nielsen ME, Romero FR, Schaeffer EM, Allaf ME, Brito FA, et al. Long-term oncologic outcome after laparoscopic radical nephroureterectomy for upper tract transitional cell carcinoma. Eur Urol 2007;51:1639-44.  Back to cited text no. 11
    
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Berger A, Haber GP, Kamoi K, Aron M, Desai MM, Kaouk JH, et al. Laparoscopic radical nephroureterectomy for upper tract transitional cell carcinoma: Oncological outcomes at 7 years. J Urol 2008;180:849-54.  Back to cited text no. 12
    
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Rouprêt M, Hupertan V, Sanderson KM, Harmon JD, Cathelineau X, Barret E, et al. Oncologic control after open or laparoscopic nephroureterectomy for upper urinary tract transitional cell carcinoma: A single center experience. Urology 2007;69:656-61.  Back to cited text no. 13
    


    Figures

  [Figure 1]
 
 
    Tables

  [Table 1], [Table 2], [Table 3]


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