Journal of Investigative Surgery, 27, 354–359, 2014 C 2014 Informa Healthcare USA, Inc. Copyright ISSN: 0894-1939 print / 1521-0553 online DOI: 10.3109/08941939.2014.930214
SURGICAL TECHNIQUE
Total Retroperitoneal Laparoscopic Nephroureterectomy with Bladder-Cuff Resection for Upper Urinary Tract Transitional Cell Carcinoma
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Zhenqiang Fang, MD, Longkun Li, MD, Xiangwei Wang, MD, Wei Chen, MD, Weisheng Jia, MD, Fan He, MD, Chongxing Shen, MD, Gang Ye, MD Department of Urology, Center of Nephrology, The Second Affiliated Hospital of the Third Military Medical University, Chongqing, China
ABSTRACT Background: Open nephroureterectomy (ONU) and bladder cuff resection (ONU-BCR) has been the gold standard of surgical treatment for upper urinary tract transitional cell carcinoma (UUT-TCC). The aim of this study is to introduce a modified total retroperitoneal laparoscopic nephroureterectomy (LNU) with bladder-cuff resection (LNU-BCR) method for treating UUT-TCC and compare its clinical efficacy with ONU-BCR. Methods: Sixty-five patients with UUT-TCC, who underwent ONU-BCR (n = 36) or LNU-BCR (n = 29) between January 2008 and June 2012, were analyzed in this retrospective study. Perioperative data as well as incidence of disease recurrence at the primary site or distant metastasis was compared in patients with at least 6 months follow-up. Results: As compared with patients with ONU-BCR, the patients with LNU-BCR had significantly shorter operative time, lower estimated blood loss, shorter time to oral intake, lower analgesic dose, shorter duration of analgesic use, shorter duration of incision drainage tube, shorter time to ambulation out of bed and reduced postoperative hospital stay (all, p < .05). No significant difference in postoperative complications or incidence of bladder carcinoma recurrence and distant metastasis during the follow-up period was observed. Conclusions: The modified LNU-BCR represents an effective and safe alternative technique to ONU-BCR with the advantages of reduced invasiveness, bleeding and hospitalization. Keywords humans; laparoscopy; nephrectomy; transitional cell carcinoma; urinary bladder; urologic surgical procedures
INTRODUCTION
pared to the ONU as it is less invasive, safe, and effective [3–8]. However, a consensus method for excision of the ureter and bladder cuff has yet to be identified as each has their advantages and disadvantages [9]. Combined LNU and lower abdominal open surgery for removing distal ureter and bladder cuff has been commonly used due to its low surgical difficulty [7, 9–13]. To further reduce surgical trauma and achieve better clinical outcomes, we performed complete LNU and bladder cuff resection (LNU-BCR). In this retrospective study, the clinical efficacy, outcomes, and complications were compared between patients receiving ONU-BCR with those receiving LNU-BCR.
Upper urinary tract transitional cell carcinoma (UUTTCC) accounts for 5% of urinary tract tumors [1]. The standard surgical treatment for UUT-TCC consists of radical resection of the affected kidney, ureter, and bladder wall around the opening of ureter [1, 2]. Open nephroureterectomy and bladder cuff resection (ONU-BCR) has been the gold standard of surgical treatment for UUT-TCC patients. However, with the improvement of minimally invasive laparoscopic nephroureterectomy (LNU), its status as the gold standard has been challenged. LNU is now widely used for nephrectomy as a better treatment method com-
Received 14 October 2013; accepted 28 May 2014. Address correspondence to Gang Ye, Department of Urology, Center of Nephrology, The Second Affiliated Hospital of the Third Military Medical University, Chongqing 400037, China. E-mail: [email protected]
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Laparoscopic Nephroureterectomy for Urinary Carcinoma 355
MATERIALS AND METHODS
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Patients and Methods We retrospectively analyzed the clinical data of 65 patients with UUT-TCC, who were admitted to our hospital between January 2008 and June 2012. Among them, 29 patients underwent LNU-BCR, and 36 patients underwent ONU-BCR. Prior to surgery all patients received the following examinations: ultrasonography, computed tomography (CT), intravenous urography, retrograde pyelography, urine cytology, and fluorescence in situ hybridization. Ureteroscopy and biopsy were carried out for some patients. Cystoscopic examination revealed the absence of bladder tumors in all patients. The surgical procedure was randomly selected by surgeons and not necessarily based on previous experience of the open cases. Different surgeons performed both procedures within the same period. During this period, eight patients with vascular metastasis or regional lymph node metastasis (N3), who were high-risk patients, were excluded from the current study because they had to also undergo cardiopulmonary bypass surgery. At pre-anesthesia stage, all patients received an intravenous injection of hydroprednisone (40 mg; Jiangxi Medicines LLC, Nanchang, Jiangxi Province, China) and received 1.5 g cefuroxime sodium (Eli Lilly Italia Spa, Firenze, Italy) via intravenous infusion 30 min prior to surgery to prevent infection. Whole body intravenous anesthesia was applied to all patients during the surgery. Specifically, intravenous anesthesia during the induction phase consisted of bolus injections of propofol (1.5 mg/kg body weight; AstraZeneca S.P.A., Milan, Italy), sufentanil (0.4 μg/kg body weight; IDT Biologika GmbH, Dessau-Rosslau, Germany), rocuronium (0.08 mg/kg body weight; Tentai LLC, Chendu, Sichuan province, China) and midazolam (0.01 mg/kg body weight; Zenhu Pharmacy LLC, Ichan, Hubei Province, China). Maintenance phase anesthesia consisted of sufentanil (0.1–0.2 μg/h/kg body weight; IDT Biologika GmbH, Dssau-RoBlau, Germany). Patients also received intravenous infusion of fluids comprised of sodium chloride (1000 mL; Zhengzhou Yonghe Pharmaceutical Co., Ltd., Zhengzhou, Henan province China) during surgery. Morphine (Daiichi Pharmaceutical Co., Ltd Shenyang, Liaoning Province, China) was applied intramuscular injection of 5 mg each time as an analgesic following the surgery. After surgery, bladder drug infusion was routinely carried out for each patient to prevent bladder tumor recurrence. Patients received intravesical injection of pirarubicin hydrochloride (25 mg in 5% dextrose solution/ m body surface; Hisun Pharmaceutical Co., Ltd, Taizhou, Zhejiang Province, China) as regular intravesical instillation therapy. Data, including patient age, gender, initial symptom, history of transitional cell cancer, operative time, intraoperative blood loss, application time and dose of C
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pain killers, postoperative pathological type, perioperative complications, duration of urethra catheter and drainage tube use, postoperative length of stay, etc., were collected. Follow-up items included the physical examination, cystoscopic examination, urine cytology, renal function, and urinary tract ultrasound, which were examined three months after surgery in the first year and twice a year thereafter. An abdominal CT was carried out at 3, 6, and 12 months following the surgery and once per year thereafter.
ONU-BCR Surgical Procedure After a large lower abdominal oblique incision of 10 cm was made two finger-widths above and parallel to the inguinal ligament with its lower portion close to the midline, the kidney, ureter, and bladder cuff were removed. Alternatively, the kidney and upper to middle ureter were removed from a lumbar incision, and the lower ureter and bladder cuff were removed from a lower abdominal oblique incision [14].
LNU-BCR Procedure After application of general anesthesia, the patient was placed in 90◦ lateral decubitus position, and a Foley catheter was inserted for continuous drainage of urine. Four small incisions of approximately 0.5–1.5 cm in length were made (Figure 1), and Trocars of the corresponding sizes were inserted. Carbon dioxide was pumped through port A to establish the pneumoretroperitoneum. The gas pressure was maintained at 12 mmHg. The optical fiber was inserted from the Trocar in port A, and the Trocars in the ports B and C were used for surgical manipulation (Figure 1). The psoas muscle and ureter were exposed, and the ureter inferior to the tumor was clipped using a HemR clip (Teleflex Medical, Research Triangle Park, o-lok NC, USA) to prevent tumor spillage. The lower pole and dorsal side of the kidney were dissected outside the perinephric fat. After the renal artery and vein were exposed, clipped with a HemR clip and cut, the upper pole and ventral side o-lok of the kidney were dissected. The kidney was isolated outside the perinephric fat and removed; the perirenal lymph nodes were also removed. Unless there was tumor invasion, the adrenal gland was not routinely removed. Total LNU with bladder-cuff resection through the retroperitonium was performed as described by Hattori et al. [15] with some modifications that decreased the invasiveness and reduced the difficulty of the surgery. First, modifications were made regarding the four small incisions that were used to establish the laparoscopic working channels (Figure 1). Three working channels, which are located in the posterior,
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Z. Fang et al. vent downward slippage of the kidney upon removal, which can affect lower ureter and bladder cuff removal. To shorten the operative time and simplify the procedure, we completely removed the kidney and then changed the view of surgery caudally while keeping the patient in a head-down position, and pulled the ureter and kidney through the port C to avoid the impact of downward kidney slippage for later surgery. For bladder cuff excision, the bladder wall 1.5–2 cm from the ureteral opening together with the ureter was removed.
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Data Analysis
FIGURE 1 A diamond-like distribution of port sites. Port A: Intersection of a longitudinal line 2 cm ventral to the mid-axillary line and a transverse line 3 cm superior to the iliac crest. Port B: Intersection of a longitudinal line 2 cm ventral to the anterior axillary line and a line extended from the 12th rib. Port C: Intersection of a longitudinal line 2 cm ventral to the posterior axillary line and a transverse line 2 cm inferior to the lowest point of the 12th rib. Port D: Intersection of the midclavicular line and a transverse line 3 cm inferior to the umbilicus. Line E: Posterior axillary line. Line F: Mid-axillary line. Line G: Anterior axillary line. Line H: Midclavicular line. I: Ilium. J: The 12th rib.
Continuous variables were summarized by mean ± SD or median with interquartile range (IQR, the range between the 25th and 75th percentile) based on the normality of data; categorical variables were expressed as frequencies and percentages. The differences between patients with LNU-BCR and those with ONUBCR were determined using independent t-tests or Wilcoxon rank sum tests for continuous variables and by Chi-square test or Fisher’s exact for categorical variables, respectively. The statistical analyses were all performed with SAS software version 9.2 (SAS Institute Inc., Cary, NC). A two-tailed p-value < .05 was considered statistically significant.
RESULTS Baseline Characteristics of Patients who Underwent LNU-BCR vs. ONU-BCR
mid-, and anterior axillary lines are routinely used for the laparoscopic nephrectomy; however, those in the posterior and mid-axillary lines cannot be used for lower ureter and bladder cuff removal due to obstruction by the ilium and pelvic wall. Therefore, Hattori et al. [15] added two abdominal incisions and sutured the bladder through the abdominal wall for traction. To utilize the working channels for laparoscopic nephrectomy sufficiently, reduce the surgical trauma and simplify the procedure, we made incisions that were shifted ventrally by approximately 2 cm from the incisions used in routine laparoscopic nephrectomy procedures (Figure 1). Thus, ports A and C not only can be used for nephrectomy, but also removal of the lower ureter and bladder cuff, which is less traumatic. Second, the bladder suturing step was simplified. Rather than pulling the bladder after inserting the needle through the abdominal wall and suturing it as in Hattori et al. [15] we omitted this step without extending the time for bladder suture. Third, Hattori et al. [15] did not remove the kidney after cutting the renal vessels. They first changed the view of surgery caudally and removed the lower ureter and the bladder cuff, and then changed the view cephalically to pre-
A total of 65 patients (38 males and 27 females) with UUT-TCC were included in this study; whereas 29 patients (mean age of 65.1 ± 11.3 years) underwent LNU-BCR, 36 patients (mean age of 64.3 ± 10.7 years) were treated with ONU-BCR. Analysis of the baseline characteristics between the LNU-BCR and ONU-BCR groups revealed no significant differences in age, sex, as well as tumor side, site, grade and stage (i.e., T, N, and TNM stages).
Perioperative Characteristics of Patients who Underwent LNU-BCR vs. ONU-BCR The perioperative characteristics between the two groups were compared in Table 1. Patients that underwent LNU-BCR had significantly lower operative time as compared to those with ONU-BCR [median (IQR): 205.0 (180.0, 240.0) min vs. 240.0 (210.0, 290.0) min, p = .045] if repositioning time was not included in the operative time as the LNU-BCR does not require patient repositioning. Inclusion of the repositioning time further increased the difference in operative time Journal of Investigative Surgery
Laparoscopic Nephroureterectomy for Urinary Carcinoma 357 TABLE 1 Peri-operative data for the LNU-BCR and ONU-BCR groups LNU-BCR Group (n = 29)
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Operative time (min)a Without repositioning time With repositioning time∗ Estimated blood loss (mL)a Time to oral intake (days)a Analgesics (mg morphine sulfate equivalent)b Duration of analgesics (h)a Duration of incision drainage tube (days)a Duration of catheterization (days)a Time to ambulation out of bed (days)a Postoperative hospital stay (days)a Complicationc No Yes Wound infection Urinary tract infection Wound hematoma Prolonged ileus Lymphatic fistula Urinary retention Subcutaneous emphysema
205.0 (180.0, 240.0) 205.0 (180.0, 240.0) 120.0 (100.0, 200.0) 2.0 (2.0, 3.0) 31.6 ± 21.7 14.0 (6.0, 25.0) 3.0 (2.0, 4.0) 7.0 (6.0, 8.0) 2.0 (2.0, 3.0) 8.0 (7.0, 8.0) 19 (65.5) 10 (34.5) 1 2 1 0 0 1 5
ONU-BCR Group (n = 36)
P-value
240.0 (210.0, 290.0) 284.5 (251.0, 332.5) 300.0 (200.0, 500.0) 4.0 (3.5, 5.0) 180.1 ± 80.4 48.5 (28.0, 66.5) 3.0 (3.0, 4.0) 7.0 (6.0, 8.0) 5.5 (5.0, 6.0) 12.0 (10.0, 13.0)
0.045‡ < 0.0001‡ 0.001‡ < 0.0001‡ < 0.0001† < 0.0001‡ 0.039‡ 0.763‡ < 0.0001‡ < 0.0001‡
26 (72.2) 10 (27.8) 2 1 1 1 3 2 0
0.560§
∗
Only ONU-BCR group had repositioning time. Median (IQR); b Mean ± SD; c n(%). † Independent test; ‡ Wilcoxon rank sum test; § Chi-square test. a
between the LNU-BCR and ONU-BCR groups [205.0 (180.0, 240.0) min vs. 284.5 (251.0, 332.5) min, p < .0001; Table 1]. Moreover, as compared with the ONU-BCR group, the LNU-BCR group had significantly lower estimated blood loss (p = .001), shorter time to oral intake (p < .0001), lower analgesic dose (p < .0001), shorter duration of analgesic use (p < .0001), shorter duration of incision drainage tube (p = .039), shorter time to ambulation out of bed (p < .0001) and reduced postoperative hospital stay (p < .0001). The duration of catheterization and proportion of complications were similar between the two groups (p = .763 and p = .560, respectively; Table 1).
Follow-up Outcomes in Patients who Underwent LNU-BCR vs. ONU-BCR Of the 65 patients included in this study, 62 had at least 6-months follow-up and complete follow-up data. As shown in Table 2, the duration of follow-up did not differ significantly between the LNU-BCR and ONUBCR groups [22.4 (13.0, 43.2) months vs. 30.8 (21.2, 43.6) months, p = .381]. Next, follow-up outcomes were compared between the two treatment groups. The disease recurrence rates (i.e., in the bladder or and metastasis to another organ) were similar (37.9% in the LNU-BCR group vs. 41.7% in the ONU-BCR group, p = .760; Table 2). In addition, no differences were observed in the disease recurrence site (i.e., in the bladder or metastasis to another organ) or the median time to C
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recurrence (Table 2). Furthermore, for patients with bladder tumor recurrence, recurrence site (i.e., at the resection site or another area of the bladder) and tumor stage were also comparable (Table 2). Finally, as of July 2013, no patient had died in the LNU-BCR group; one patient died as a result of metastasis in the ONU-BCR group.
DISCUSSION In this retrospective study, the clinical efficacy of a modified LNU-BCR approach was compared with ONU-BCR in 65 patients with UUT-TCC. No differences in patient baseline characteristics, complications or disease recurrence were observed between the treatment groups. In the LNU-BCR group, the operative time was shorter with less blood loss and analgesic use and reduced time to ambulation and length of hospital stay. Our procedure was based on that previously described by Hattori et al. [15] with three major modifications that decreased the invasiveness and simplified the procedure. First, we modified the surgical incisions using four working channels as compared to the five channels described by Hattori et al. [15], thereby inducing less surgical trauma. In addition, we simplified the bladder suturing step. Finally, to shorten the operative time and simplify the procedure, we completely removed the kidney, changed the view of surgery caudally while keeping the patient in a head-down
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TABLE 2 Follow-up data for the LNU-BCR and ONU-BCR groups
Follow-up duration (months)a Recurrence metastasisb No Yes For patients with recurrence and metastasis (N = 26) Recurrence metastasis siteb Bladder tumor Other metastasis Time to bladder tumor and other metastasis (months)a For patients with recurrence in bladder tumor (N = 19) Bladder tumorb
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Resection site Other bladder Bladder tumor stageb Less than T2 T2 or greater a †
LNU-BCR Group (n = 28)
ONU-BCR Group (n = 34)
p-value
22.4 (13.0, 43.2)
30.8 (21.2, 43.6)
0.381† 0.760‡
18 (62.1) 11 (37.9)
21 (58.3) 15 (41.7)
8 (72.7) 3 (27.3) 8.7 (6.0, 18.5)
11 (73.3) 4 (26.7) 9.4 (5.0, 32.0)
2 (25.0) 6 (75.0)
3 (27.3) 8 (72.7)
5 (62.5) 3 (37.5)
7 (63.6) 4 (36.4)
1.000§ 1.000† 1.000§ 1.000§
Median (IQR); b n (%). Wilcoxon rank sum test; ‡ Chi-square test; § Fisher’s exact test.
position, and pulled the ureter and kidney through port C to avoid kidney slippage, which may affect the subsequent surgery. The modified bladder suturing procedure described in the present study also has advantages over the “pluck” technique for transurethral resection under rigid cystoscope, which is often used for open resection of the kidney and ureter as well as following laparoscopic nephrectomy [16]. However, this method increases the risk of implantation metastases via the bladder incision or the exposed ureteral opening [17–19]. Moreover, the incision used for bladder resection cannot be closed with this method, thereby extending the duration of postoperative drainage tube placement, which increases urine leakage and risk of infection and extends the duration of urinary catheter placement [17–20]. However, our modified procedure closes the bladder, shortening the time to bladder healing and duration of drainage tube and urinary catheter placement and reducing the rate of infection. Previous studies have removed the distal ureter and bladder cuff using a laparoscopic technique together with an Endo-GIA stapler or large Hem-o-lok clips [21, 22]. Although this method can prevent the occurrence of local tumor cell implantation, it does not accurately control the site of resection and may result in insufficient resection or injury to the contralateral ureter. Moreover, accurate histological evaluation of the surgical margin is impossible with this method, resulting in a rate of positive margins up to 25% and a rate of local tumor recurrence as high as 15% [22, 23]. In addition, staplers or large Hem-o-lok clips may easily induce stone formation [9, 22, 23]. In our modified procedure, the ureter and part of the bladder wall (1–1.5 cm from the junction) can be removed under direct vi-
sion, ensuring complete tumor resection without leaving any remnant tumor tissues. Manipulation under direct vision can also avoid injury to the contralateral ureteral opening and significantly increase the safety of the surgery. Indeed, the surgical margins of all patients undergoing LNU-BCR were negative, and there was no injury to the contralateral opening of ureter. Furthermore, the rate of local tumor recurrence in the surgical margin of the bladder was only 8.3%, which was comparable to that in patients receiving ONU-BCR. Also, no differences in tumor stage were observed between the two treatment groups. Moreover, we used absorbable sutures for closing the bladder to avoid the risk of stone formation due to remnant foreign bodies [9, 23]. Thus, the method described in this study can overcome these shortcomings, including the high rate of positive margins; it can also reduce stone formation and had a comparable safety profile with that observed for the open surgery procedure [9, 22, 23]. Although patient repositioning for the open bladder cuff resection may be simplified by rolling the table until the patient is nearly flat for the Gibson incision, this modified LNU-BCR approach has the potential to save at least 40 min operative time for position change that is required for open and transurethral surgeries. In addition, this approach is less invasive and simpler with comparable efficacy. The ureter can be blocked at the beginning of the surgery, thereby preventing tumor spill and subsequent metastasis. Moreover, this modified LNU-BCR approach avoids interference with the rectum and colon, prevents the abdominal implantation metastasis, and bypasses the unfavorable impact on the intestinal function [15, 24]. There are several limitations of this study should be mentioned. This study is limited by its Journal of Investigative Surgery
Laparoscopic Nephroureterectomy for Urinary Carcinoma 359
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retrospective nature and relatively small sample size. The results may be affected if surgeons with the laparoscopic cases were performed after the experience of the open cases. The selection criteria between ONU-BCR and LNU-BCR are not randomized. Patients’ health conditions will be the primary concerns of selection criteria. ONU-BCR will be selected for patients who had prior ipsilateral lower abdominal surgery history, patients with poor lung function who cannot tolerate general anesthesia, and patients who had lower-segment ureter cancer. LNU-BCR was chosen for patients with early-stage renal pelvic cancer and upper-segment ureter cancer as well as obese patients. Additionally, patients’ own choices also affected the selection criteria. Further analyses with more patients and in other settings are necessary to fully elucidate the benefits of this modified LNU-BCR.
CONCLUSION In conclusion, we report a modified approach for total retroperitoneal LNU with bladder-cuff resection that is less invasive and simpler and has comparable clinical efficacy to ONU-BCR. Additional long-term comparative studies are necessary to fully evaluate the benefits of this modified approach. Declaration of interest: The authors report no conflict of interest. The authors alone are responsible for the content and writing of the article. This study is supported by National Natural Science Foundation of China Project No. 81200500; Natural Science Foundation Project of CQ-CSTC (No. 2009BB5154, CSTC).
REFERENCES [1] Flanigan RC. Urothelial tumors of the upper urinary tract. In: Campbell Urology. Walsh PC, ed. Philadelphia, PA: WB Saunders; 2007. [2] Murphy DM, Zincke H, Furlow WL. Management of high grade transitional cell cancer of the upper urinary tract. J Urol. 1981;125:25–29. [3] Laguna MP, de la Rosette JJ. The endoscopic approach to the distal ureter in nephroureterectomy for upper urinary tract tumor. J Urol. 2001;166:2017–2022. [4] Abercrombie GF. Nephro-ureterectomy. Proc R Soc Med. 1972;65:1021–1022. [5] Oosterlinck W, Solsona E, van der Meijden AP, et al. EAU guidelines on diagnosis and treatment of upper urinary tract transitional cell carcinoma. Eur Urol. 2004;46:147–154. [6] Az´emar MD, Comperat E, Richard F, et al. Bladder recurrence after surgery for upper urinary tract urothelial cell carcinoma: frequency, risk factors, and surveillance. Urol Oncol. 2011;29:130–136.
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[7] Waldert M, Remzi M, Klingler HC, et al. The oncological results of laparoscopic nephroureterectomy for upper urinary tract transitional cell cancer are equal to those of open nephroureterectomy. BJU Int. 2009;103:66–70. [8] Simone G, Papalia R, Guaglianone S, et al. Laparoscopic versus open nephroureterectomy: perioperative and oncologic outcomes from a randomised prospective study. Eur Urol. 2009;56:520–526. [9] Ph´e V, Cussenot O, Bitker MO, Roupret M. Does the surgical technique for management of the distal ureter influence the outcome after nephroureterectomy? BJU Int. 2011;108:130–138. [10] Tsujihata M, Nonomura N, Tsujimura A, et al. Laparoscopic nephroureterectomy for upper tract transitional cell carcinoma: comparison of laparoscopic and open surgery. Eur Urol. 2006;49:332–336. [11] Salomon L, Hoznek A, Cicco A, et al. Retroperitoneoscopic nephroureterectomy for renal pelvic tumors with a single iliac incision. J Urol. 1999;161:541. [12] Klingler HC, Lodde M, Pycha A, et al. Modified laparoscopic nephroureterectomy for treatment of upper urinary tract transitional cell cancer is not associated with an increased risk of tumour recurrence. Eur Urol. 2003;44:442–447. [13] Taweemonkongsap T, Nualyong C, Amornvesukit T, et al. Outcomes of surgical treatment for upper urinary tract transitional cell carcinoma: comparison of retroperitoneoscopic and open nephroureterectomy. World J Surg Oncol. 2008;6:3–10. [14] Margulis V, Shariat SF, Matin SF, et al. Outcomes of radical nephroureterectomy: a series from the Upper Tract Urothelial Carcinoma Collaboration. Cancer. 2009;115:1224–1233. [15] Hattori R, Yoshino Y, Komatsu T, et al. Pure laparoscopic complete excision of distal ureter with a bladder cuff for upper tract urothelial carcinoma. World J Urol. 2009;27:253–258. [16] Keeley FX Jr, Tolley DA. Laparoscopic nephroureterectomy: making management of upper-tract transitionalcell carcinoma entirely minimally invasive. J Endourol. 1998;12:139–141. [17] Arango O, Bielsa O, Carles J, Gelabert-Mas A. Massive tumor implantation in the endoscopic resected area in modified nephroureterectomy. J Urol. 1997;157:1839. [18] Jones DR, Moisey CU. A cautionary tale for the modified “pluck” nephroureterectomy. Br J Urol. 1993;71:486–487. [19] Hetherington JW, Ewing R, Philip NH. Modified nephroureterectomy: a risk of tumor implantation. Br J Urol. 1986;58:368–370. [20] Mueller TJ, DaJusta DG, Cha DY, et al. Ureteral fibrin sealant injection of the distal ureter during laparoscopic nephroureterectomy—a novel and simple modification of the pluck technique. Urology. 2010;75:187–192. [21] Tan BJ, Ost MC, Lee BR. Laparoscopic nephroureterectomy with bladder cuff resection: techniques and outcomes. J Endourol. 2005;19:664–676. [22] Shalhav AL, Dunn MD, Portis AJ, et al. Laparoscopic nephroureterectomy for upper tract transitional cell cancer: the Washington University experience. J Urol. 2000;163:1100–1104. [23] Matin SF, Gill IS. Recurrence and survival following laparoscopic radical nephroureterectomy with various forms of bladder cuff control. J Urol. 2005;173:395–400. [24] Gill IS, Sung GT, Hobart MG, et al. Laparoscopic radical nephroureterectomy for upper tract transitional cell carcinoma: the Cleveland Clinic experience. J Urol. 2000;164:1513–1522.
SURGICAL TECHNIQUE
Total Retroperitoneal Laparoscopic Nephroureterectomy with Bladder-Cuff Resection for Upper Urinary Tract Transitional Cell Carcinoma
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Zhenqiang Fang, MD, Longkun Li, MD, Xiangwei Wang, MD, Wei Chen, MD, Weisheng Jia, MD, Fan He, MD, Chongxing Shen, MD, Gang Ye, MD Department of Urology, Center of Nephrology, The Second Affiliated Hospital of the Third Military Medical University, Chongqing, China
ABSTRACT Background: Open nephroureterectomy (ONU) and bladder cuff resection (ONU-BCR) has been the gold standard of surgical treatment for upper urinary tract transitional cell carcinoma (UUT-TCC). The aim of this study is to introduce a modified total retroperitoneal laparoscopic nephroureterectomy (LNU) with bladder-cuff resection (LNU-BCR) method for treating UUT-TCC and compare its clinical efficacy with ONU-BCR. Methods: Sixty-five patients with UUT-TCC, who underwent ONU-BCR (n = 36) or LNU-BCR (n = 29) between January 2008 and June 2012, were analyzed in this retrospective study. Perioperative data as well as incidence of disease recurrence at the primary site or distant metastasis was compared in patients with at least 6 months follow-up. Results: As compared with patients with ONU-BCR, the patients with LNU-BCR had significantly shorter operative time, lower estimated blood loss, shorter time to oral intake, lower analgesic dose, shorter duration of analgesic use, shorter duration of incision drainage tube, shorter time to ambulation out of bed and reduced postoperative hospital stay (all, p < .05). No significant difference in postoperative complications or incidence of bladder carcinoma recurrence and distant metastasis during the follow-up period was observed. Conclusions: The modified LNU-BCR represents an effective and safe alternative technique to ONU-BCR with the advantages of reduced invasiveness, bleeding and hospitalization. Keywords humans; laparoscopy; nephrectomy; transitional cell carcinoma; urinary bladder; urologic surgical procedures
INTRODUCTION
pared to the ONU as it is less invasive, safe, and effective [3–8]. However, a consensus method for excision of the ureter and bladder cuff has yet to be identified as each has their advantages and disadvantages [9]. Combined LNU and lower abdominal open surgery for removing distal ureter and bladder cuff has been commonly used due to its low surgical difficulty [7, 9–13]. To further reduce surgical trauma and achieve better clinical outcomes, we performed complete LNU and bladder cuff resection (LNU-BCR). In this retrospective study, the clinical efficacy, outcomes, and complications were compared between patients receiving ONU-BCR with those receiving LNU-BCR.
Upper urinary tract transitional cell carcinoma (UUTTCC) accounts for 5% of urinary tract tumors [1]. The standard surgical treatment for UUT-TCC consists of radical resection of the affected kidney, ureter, and bladder wall around the opening of ureter [1, 2]. Open nephroureterectomy and bladder cuff resection (ONU-BCR) has been the gold standard of surgical treatment for UUT-TCC patients. However, with the improvement of minimally invasive laparoscopic nephroureterectomy (LNU), its status as the gold standard has been challenged. LNU is now widely used for nephrectomy as a better treatment method com-
Received 14 October 2013; accepted 28 May 2014. Address correspondence to Gang Ye, Department of Urology, Center of Nephrology, The Second Affiliated Hospital of the Third Military Medical University, Chongqing 400037, China. E-mail: [email protected]
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Laparoscopic Nephroureterectomy for Urinary Carcinoma 355
MATERIALS AND METHODS
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Patients and Methods We retrospectively analyzed the clinical data of 65 patients with UUT-TCC, who were admitted to our hospital between January 2008 and June 2012. Among them, 29 patients underwent LNU-BCR, and 36 patients underwent ONU-BCR. Prior to surgery all patients received the following examinations: ultrasonography, computed tomography (CT), intravenous urography, retrograde pyelography, urine cytology, and fluorescence in situ hybridization. Ureteroscopy and biopsy were carried out for some patients. Cystoscopic examination revealed the absence of bladder tumors in all patients. The surgical procedure was randomly selected by surgeons and not necessarily based on previous experience of the open cases. Different surgeons performed both procedures within the same period. During this period, eight patients with vascular metastasis or regional lymph node metastasis (N3), who were high-risk patients, were excluded from the current study because they had to also undergo cardiopulmonary bypass surgery. At pre-anesthesia stage, all patients received an intravenous injection of hydroprednisone (40 mg; Jiangxi Medicines LLC, Nanchang, Jiangxi Province, China) and received 1.5 g cefuroxime sodium (Eli Lilly Italia Spa, Firenze, Italy) via intravenous infusion 30 min prior to surgery to prevent infection. Whole body intravenous anesthesia was applied to all patients during the surgery. Specifically, intravenous anesthesia during the induction phase consisted of bolus injections of propofol (1.5 mg/kg body weight; AstraZeneca S.P.A., Milan, Italy), sufentanil (0.4 μg/kg body weight; IDT Biologika GmbH, Dessau-Rosslau, Germany), rocuronium (0.08 mg/kg body weight; Tentai LLC, Chendu, Sichuan province, China) and midazolam (0.01 mg/kg body weight; Zenhu Pharmacy LLC, Ichan, Hubei Province, China). Maintenance phase anesthesia consisted of sufentanil (0.1–0.2 μg/h/kg body weight; IDT Biologika GmbH, Dssau-RoBlau, Germany). Patients also received intravenous infusion of fluids comprised of sodium chloride (1000 mL; Zhengzhou Yonghe Pharmaceutical Co., Ltd., Zhengzhou, Henan province China) during surgery. Morphine (Daiichi Pharmaceutical Co., Ltd Shenyang, Liaoning Province, China) was applied intramuscular injection of 5 mg each time as an analgesic following the surgery. After surgery, bladder drug infusion was routinely carried out for each patient to prevent bladder tumor recurrence. Patients received intravesical injection of pirarubicin hydrochloride (25 mg in 5% dextrose solution/ m body surface; Hisun Pharmaceutical Co., Ltd, Taizhou, Zhejiang Province, China) as regular intravesical instillation therapy. Data, including patient age, gender, initial symptom, history of transitional cell cancer, operative time, intraoperative blood loss, application time and dose of C
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pain killers, postoperative pathological type, perioperative complications, duration of urethra catheter and drainage tube use, postoperative length of stay, etc., were collected. Follow-up items included the physical examination, cystoscopic examination, urine cytology, renal function, and urinary tract ultrasound, which were examined three months after surgery in the first year and twice a year thereafter. An abdominal CT was carried out at 3, 6, and 12 months following the surgery and once per year thereafter.
ONU-BCR Surgical Procedure After a large lower abdominal oblique incision of 10 cm was made two finger-widths above and parallel to the inguinal ligament with its lower portion close to the midline, the kidney, ureter, and bladder cuff were removed. Alternatively, the kidney and upper to middle ureter were removed from a lumbar incision, and the lower ureter and bladder cuff were removed from a lower abdominal oblique incision [14].
LNU-BCR Procedure After application of general anesthesia, the patient was placed in 90◦ lateral decubitus position, and a Foley catheter was inserted for continuous drainage of urine. Four small incisions of approximately 0.5–1.5 cm in length were made (Figure 1), and Trocars of the corresponding sizes were inserted. Carbon dioxide was pumped through port A to establish the pneumoretroperitoneum. The gas pressure was maintained at 12 mmHg. The optical fiber was inserted from the Trocar in port A, and the Trocars in the ports B and C were used for surgical manipulation (Figure 1). The psoas muscle and ureter were exposed, and the ureter inferior to the tumor was clipped using a HemR clip (Teleflex Medical, Research Triangle Park, o-lok NC, USA) to prevent tumor spillage. The lower pole and dorsal side of the kidney were dissected outside the perinephric fat. After the renal artery and vein were exposed, clipped with a HemR clip and cut, the upper pole and ventral side o-lok of the kidney were dissected. The kidney was isolated outside the perinephric fat and removed; the perirenal lymph nodes were also removed. Unless there was tumor invasion, the adrenal gland was not routinely removed. Total LNU with bladder-cuff resection through the retroperitonium was performed as described by Hattori et al. [15] with some modifications that decreased the invasiveness and reduced the difficulty of the surgery. First, modifications were made regarding the four small incisions that were used to establish the laparoscopic working channels (Figure 1). Three working channels, which are located in the posterior,
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Z. Fang et al. vent downward slippage of the kidney upon removal, which can affect lower ureter and bladder cuff removal. To shorten the operative time and simplify the procedure, we completely removed the kidney and then changed the view of surgery caudally while keeping the patient in a head-down position, and pulled the ureter and kidney through the port C to avoid the impact of downward kidney slippage for later surgery. For bladder cuff excision, the bladder wall 1.5–2 cm from the ureteral opening together with the ureter was removed.
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Data Analysis
FIGURE 1 A diamond-like distribution of port sites. Port A: Intersection of a longitudinal line 2 cm ventral to the mid-axillary line and a transverse line 3 cm superior to the iliac crest. Port B: Intersection of a longitudinal line 2 cm ventral to the anterior axillary line and a line extended from the 12th rib. Port C: Intersection of a longitudinal line 2 cm ventral to the posterior axillary line and a transverse line 2 cm inferior to the lowest point of the 12th rib. Port D: Intersection of the midclavicular line and a transverse line 3 cm inferior to the umbilicus. Line E: Posterior axillary line. Line F: Mid-axillary line. Line G: Anterior axillary line. Line H: Midclavicular line. I: Ilium. J: The 12th rib.
Continuous variables were summarized by mean ± SD or median with interquartile range (IQR, the range between the 25th and 75th percentile) based on the normality of data; categorical variables were expressed as frequencies and percentages. The differences between patients with LNU-BCR and those with ONUBCR were determined using independent t-tests or Wilcoxon rank sum tests for continuous variables and by Chi-square test or Fisher’s exact for categorical variables, respectively. The statistical analyses were all performed with SAS software version 9.2 (SAS Institute Inc., Cary, NC). A two-tailed p-value < .05 was considered statistically significant.
RESULTS Baseline Characteristics of Patients who Underwent LNU-BCR vs. ONU-BCR
mid-, and anterior axillary lines are routinely used for the laparoscopic nephrectomy; however, those in the posterior and mid-axillary lines cannot be used for lower ureter and bladder cuff removal due to obstruction by the ilium and pelvic wall. Therefore, Hattori et al. [15] added two abdominal incisions and sutured the bladder through the abdominal wall for traction. To utilize the working channels for laparoscopic nephrectomy sufficiently, reduce the surgical trauma and simplify the procedure, we made incisions that were shifted ventrally by approximately 2 cm from the incisions used in routine laparoscopic nephrectomy procedures (Figure 1). Thus, ports A and C not only can be used for nephrectomy, but also removal of the lower ureter and bladder cuff, which is less traumatic. Second, the bladder suturing step was simplified. Rather than pulling the bladder after inserting the needle through the abdominal wall and suturing it as in Hattori et al. [15] we omitted this step without extending the time for bladder suture. Third, Hattori et al. [15] did not remove the kidney after cutting the renal vessels. They first changed the view of surgery caudally and removed the lower ureter and the bladder cuff, and then changed the view cephalically to pre-
A total of 65 patients (38 males and 27 females) with UUT-TCC were included in this study; whereas 29 patients (mean age of 65.1 ± 11.3 years) underwent LNU-BCR, 36 patients (mean age of 64.3 ± 10.7 years) were treated with ONU-BCR. Analysis of the baseline characteristics between the LNU-BCR and ONU-BCR groups revealed no significant differences in age, sex, as well as tumor side, site, grade and stage (i.e., T, N, and TNM stages).
Perioperative Characteristics of Patients who Underwent LNU-BCR vs. ONU-BCR The perioperative characteristics between the two groups were compared in Table 1. Patients that underwent LNU-BCR had significantly lower operative time as compared to those with ONU-BCR [median (IQR): 205.0 (180.0, 240.0) min vs. 240.0 (210.0, 290.0) min, p = .045] if repositioning time was not included in the operative time as the LNU-BCR does not require patient repositioning. Inclusion of the repositioning time further increased the difference in operative time Journal of Investigative Surgery
Laparoscopic Nephroureterectomy for Urinary Carcinoma 357 TABLE 1 Peri-operative data for the LNU-BCR and ONU-BCR groups LNU-BCR Group (n = 29)
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Operative time (min)a Without repositioning time With repositioning time∗ Estimated blood loss (mL)a Time to oral intake (days)a Analgesics (mg morphine sulfate equivalent)b Duration of analgesics (h)a Duration of incision drainage tube (days)a Duration of catheterization (days)a Time to ambulation out of bed (days)a Postoperative hospital stay (days)a Complicationc No Yes Wound infection Urinary tract infection Wound hematoma Prolonged ileus Lymphatic fistula Urinary retention Subcutaneous emphysema
205.0 (180.0, 240.0) 205.0 (180.0, 240.0) 120.0 (100.0, 200.0) 2.0 (2.0, 3.0) 31.6 ± 21.7 14.0 (6.0, 25.0) 3.0 (2.0, 4.0) 7.0 (6.0, 8.0) 2.0 (2.0, 3.0) 8.0 (7.0, 8.0) 19 (65.5) 10 (34.5) 1 2 1 0 0 1 5
ONU-BCR Group (n = 36)
P-value
240.0 (210.0, 290.0) 284.5 (251.0, 332.5) 300.0 (200.0, 500.0) 4.0 (3.5, 5.0) 180.1 ± 80.4 48.5 (28.0, 66.5) 3.0 (3.0, 4.0) 7.0 (6.0, 8.0) 5.5 (5.0, 6.0) 12.0 (10.0, 13.0)
0.045‡ < 0.0001‡ 0.001‡ < 0.0001‡ < 0.0001† < 0.0001‡ 0.039‡ 0.763‡ < 0.0001‡ < 0.0001‡
26 (72.2) 10 (27.8) 2 1 1 1 3 2 0
0.560§
∗
Only ONU-BCR group had repositioning time. Median (IQR); b Mean ± SD; c n(%). † Independent test; ‡ Wilcoxon rank sum test; § Chi-square test. a
between the LNU-BCR and ONU-BCR groups [205.0 (180.0, 240.0) min vs. 284.5 (251.0, 332.5) min, p < .0001; Table 1]. Moreover, as compared with the ONU-BCR group, the LNU-BCR group had significantly lower estimated blood loss (p = .001), shorter time to oral intake (p < .0001), lower analgesic dose (p < .0001), shorter duration of analgesic use (p < .0001), shorter duration of incision drainage tube (p = .039), shorter time to ambulation out of bed (p < .0001) and reduced postoperative hospital stay (p < .0001). The duration of catheterization and proportion of complications were similar between the two groups (p = .763 and p = .560, respectively; Table 1).
Follow-up Outcomes in Patients who Underwent LNU-BCR vs. ONU-BCR Of the 65 patients included in this study, 62 had at least 6-months follow-up and complete follow-up data. As shown in Table 2, the duration of follow-up did not differ significantly between the LNU-BCR and ONUBCR groups [22.4 (13.0, 43.2) months vs. 30.8 (21.2, 43.6) months, p = .381]. Next, follow-up outcomes were compared between the two treatment groups. The disease recurrence rates (i.e., in the bladder or and metastasis to another organ) were similar (37.9% in the LNU-BCR group vs. 41.7% in the ONU-BCR group, p = .760; Table 2). In addition, no differences were observed in the disease recurrence site (i.e., in the bladder or metastasis to another organ) or the median time to C
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recurrence (Table 2). Furthermore, for patients with bladder tumor recurrence, recurrence site (i.e., at the resection site or another area of the bladder) and tumor stage were also comparable (Table 2). Finally, as of July 2013, no patient had died in the LNU-BCR group; one patient died as a result of metastasis in the ONU-BCR group.
DISCUSSION In this retrospective study, the clinical efficacy of a modified LNU-BCR approach was compared with ONU-BCR in 65 patients with UUT-TCC. No differences in patient baseline characteristics, complications or disease recurrence were observed between the treatment groups. In the LNU-BCR group, the operative time was shorter with less blood loss and analgesic use and reduced time to ambulation and length of hospital stay. Our procedure was based on that previously described by Hattori et al. [15] with three major modifications that decreased the invasiveness and simplified the procedure. First, we modified the surgical incisions using four working channels as compared to the five channels described by Hattori et al. [15], thereby inducing less surgical trauma. In addition, we simplified the bladder suturing step. Finally, to shorten the operative time and simplify the procedure, we completely removed the kidney, changed the view of surgery caudally while keeping the patient in a head-down
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TABLE 2 Follow-up data for the LNU-BCR and ONU-BCR groups
Follow-up duration (months)a Recurrence metastasisb No Yes For patients with recurrence and metastasis (N = 26) Recurrence metastasis siteb Bladder tumor Other metastasis Time to bladder tumor and other metastasis (months)a For patients with recurrence in bladder tumor (N = 19) Bladder tumorb
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Resection site Other bladder Bladder tumor stageb Less than T2 T2 or greater a †
LNU-BCR Group (n = 28)
ONU-BCR Group (n = 34)
p-value
22.4 (13.0, 43.2)
30.8 (21.2, 43.6)
0.381† 0.760‡
18 (62.1) 11 (37.9)
21 (58.3) 15 (41.7)
8 (72.7) 3 (27.3) 8.7 (6.0, 18.5)
11 (73.3) 4 (26.7) 9.4 (5.0, 32.0)
2 (25.0) 6 (75.0)
3 (27.3) 8 (72.7)
5 (62.5) 3 (37.5)
7 (63.6) 4 (36.4)
1.000§ 1.000† 1.000§ 1.000§
Median (IQR); b n (%). Wilcoxon rank sum test; ‡ Chi-square test; § Fisher’s exact test.
position, and pulled the ureter and kidney through port C to avoid kidney slippage, which may affect the subsequent surgery. The modified bladder suturing procedure described in the present study also has advantages over the “pluck” technique for transurethral resection under rigid cystoscope, which is often used for open resection of the kidney and ureter as well as following laparoscopic nephrectomy [16]. However, this method increases the risk of implantation metastases via the bladder incision or the exposed ureteral opening [17–19]. Moreover, the incision used for bladder resection cannot be closed with this method, thereby extending the duration of postoperative drainage tube placement, which increases urine leakage and risk of infection and extends the duration of urinary catheter placement [17–20]. However, our modified procedure closes the bladder, shortening the time to bladder healing and duration of drainage tube and urinary catheter placement and reducing the rate of infection. Previous studies have removed the distal ureter and bladder cuff using a laparoscopic technique together with an Endo-GIA stapler or large Hem-o-lok clips [21, 22]. Although this method can prevent the occurrence of local tumor cell implantation, it does not accurately control the site of resection and may result in insufficient resection or injury to the contralateral ureter. Moreover, accurate histological evaluation of the surgical margin is impossible with this method, resulting in a rate of positive margins up to 25% and a rate of local tumor recurrence as high as 15% [22, 23]. In addition, staplers or large Hem-o-lok clips may easily induce stone formation [9, 22, 23]. In our modified procedure, the ureter and part of the bladder wall (1–1.5 cm from the junction) can be removed under direct vi-
sion, ensuring complete tumor resection without leaving any remnant tumor tissues. Manipulation under direct vision can also avoid injury to the contralateral ureteral opening and significantly increase the safety of the surgery. Indeed, the surgical margins of all patients undergoing LNU-BCR were negative, and there was no injury to the contralateral opening of ureter. Furthermore, the rate of local tumor recurrence in the surgical margin of the bladder was only 8.3%, which was comparable to that in patients receiving ONU-BCR. Also, no differences in tumor stage were observed between the two treatment groups. Moreover, we used absorbable sutures for closing the bladder to avoid the risk of stone formation due to remnant foreign bodies [9, 23]. Thus, the method described in this study can overcome these shortcomings, including the high rate of positive margins; it can also reduce stone formation and had a comparable safety profile with that observed for the open surgery procedure [9, 22, 23]. Although patient repositioning for the open bladder cuff resection may be simplified by rolling the table until the patient is nearly flat for the Gibson incision, this modified LNU-BCR approach has the potential to save at least 40 min operative time for position change that is required for open and transurethral surgeries. In addition, this approach is less invasive and simpler with comparable efficacy. The ureter can be blocked at the beginning of the surgery, thereby preventing tumor spill and subsequent metastasis. Moreover, this modified LNU-BCR approach avoids interference with the rectum and colon, prevents the abdominal implantation metastasis, and bypasses the unfavorable impact on the intestinal function [15, 24]. There are several limitations of this study should be mentioned. This study is limited by its Journal of Investigative Surgery
Laparoscopic Nephroureterectomy for Urinary Carcinoma 359
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retrospective nature and relatively small sample size. The results may be affected if surgeons with the laparoscopic cases were performed after the experience of the open cases. The selection criteria between ONU-BCR and LNU-BCR are not randomized. Patients’ health conditions will be the primary concerns of selection criteria. ONU-BCR will be selected for patients who had prior ipsilateral lower abdominal surgery history, patients with poor lung function who cannot tolerate general anesthesia, and patients who had lower-segment ureter cancer. LNU-BCR was chosen for patients with early-stage renal pelvic cancer and upper-segment ureter cancer as well as obese patients. Additionally, patients’ own choices also affected the selection criteria. Further analyses with more patients and in other settings are necessary to fully elucidate the benefits of this modified LNU-BCR.
CONCLUSION In conclusion, we report a modified approach for total retroperitoneal LNU with bladder-cuff resection that is less invasive and simpler and has comparable clinical efficacy to ONU-BCR. Additional long-term comparative studies are necessary to fully evaluate the benefits of this modified approach. Declaration of interest: The authors report no conflict of interest. The authors alone are responsible for the content and writing of the article. This study is supported by National Natural Science Foundation of China Project No. 81200500; Natural Science Foundation Project of CQ-CSTC (No. 2009BB5154, CSTC).
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