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Keywords:

  • laparoscopy;
  • carcinoma;
  • transitional cell;
  • urinary tract;
  • ureter

Abstract

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. PATIENTS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. CONFLICT OF INTEREST
  8. REFERENCES

Associate Editor

Ash Tewari

Editorial Board

Ralph Clayman, USA

Inderbir Gill, USA

Roger Kirby, UK

Mani Menon, USA

OBJECTIVE

To determine the surgical feasibility and early oncological outcomes of laparoscopic distal ureterectomy in patients with low-grade upper urinary tract transitional cell carcinoma (UUT-TCC).

PATIENTS AND METHODS

We retrospectively reviewed patients treated laparoscopically with conservative management for a UUT-TCC between 2001 and 2005. We collected data on gender, age, mode of diagnosis, smoking, history of bladder cancer, complications, tumour site, size, stage, grade, hospital stay, recurrence and progression.

RESULTS

Data were analysed for six patients with a mean (range) age of 68.5 (54–76) years. Four patients had a diagnostic ureteroscopy with biopsy. The operative duration was 173.3 (120–240) min, the estimated blood loss was 75 (50–200) mL and the length of ureteric resection was 5.23 cm. Two patients required a psoas hitch. JJ stents were maintained for 25.8 (15–30) days. The hospital stay was 6 (5–8) days. There were minor complications in three patients after surgery. The follow-up was 32 (17–46) months. The tumour size was 1.7 (0.8–2.6) cm. There were low-grade tumours in four patients and pTa in five. All patients are alive and free of disease; there were no anastomotic strictures. Two patients developed a recurrence, one in the ipsilateral renal pelvis and one in the bladder.

CONCLUSION

Laparoscopic distal ureterectomy with direct re-implantation is technically feasible for low-risk UUT-TCC (i.e. low-grade, noninvasive), in the properly selected patient. Early oncological outcomes are promising but strict surveillance protocols must be followed.


Abbreviations
(U)UT

(upper) urinary tract

(O)NU

(open) nephroureterectomy

CIS

carcinoma in situ

TUR

transurethral resection.

INTRODUCTION

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. PATIENTS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. CONFLICT OF INTEREST
  8. REFERENCES

Upper urinary tract (UUT) TCCs are rare and account for only 5% of all urothelial carcinomas [1]. Tumours of the renal pelvis are 3–4 times more common than ureteric TCC [1,2]. The current standard of care in the management of such tumours is open nephroureterectomy (ONU) [1,3], but this is being superseded by less invasive surgery that spares the renal parenchyma for patients in whom renal salvage is imperative (i.e. solitary kidney, renal insufficiency) or in patients with a normal contralateral kidney and low-risk, superficial tumours (low grade and <15 mm) [4,5]. The most commonly used renal-sparing procedure is endoscopic ablation; however, open segmental ureterectomy has also been widely described [1,6–8].

Currently, laparoscopy is used to remove the prostate and kidney, with oncological outcomes similar to those for open surgery, even if the follow-up remains shorter in laparoscopic series [9,10]. Laparoscopy reduces the length of the incision, surgical morbidity, postoperative pain and decreases the duration of convalescence [9,10]. An early case report showed that an entire laparoscopic ureterectomy was feasible [11], but only two recent case reports have described partial laparoscopic ureteric resection and anastomosis for the conservative management of low-grade UUT-TCC [12,13].

We now present the first series of six patients who underwent laparoscopic distal ureterectomy with ureteric re-implantation for UUT-TCC. The aim of the study was to assess the technical feasibility of this treatment and to evaluate the intermediate oncological outcomes.

PATIENTS AND METHODS

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. PATIENTS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. CONFLICT OF INTEREST
  8. REFERENCES

Between 2001 and 2005, 28 patients had surgery for UUT-TCC at one institution. Data on the following variables were reviewed retrospectively: sex, age at diagnosis, history of bladder cancer, surgical treatment, complications, tumour characteristics (TNM stage 2002, WHO grade 2004, site, size), disease recurrence and progression. Preoperative evaluation included urinary cytology and cystoscopy with multiple systematic biopsies and/or transurethral resection (TUR) of any apparent tumour of the lower urinary tract. UUT was evaluated with either CT, IVU or retrograde pyelography. To date preoperative staging of UUT tumours by ureteroscopy and biopsy was not done routinely in our centre. For the current cases, it was only achieved at the physician’s request.

Indications for laparoscopic segmental ureteric resection were solitary kidney, chronic renal insufficiency or a bilateral tumour. In cases of a normal contralateral kidney, it was also offered to patients with a distal, unifocal tumour of <2 cm with no evidence of invasion. In cases of concomitant bladder tumour, this was removed first to exclude any invasive (≥ pT2) or potentially aggressive tumour (i.e. carcinoma in situ, CIS). Patients who did not satisfy these criteria or who refused laparoscopic intervention were excluded.

For laparoscopic distal ureterectomy we used the transperitoneal approach. Previous abdominal surgery was not a contraindication to the procedure. Patients were placed in the full-flank position with the operating table tilted 45° laterally. A kidney rest was not used during any of the procedures. The four-port arrangement and initial dissection, including early identification of the ureter, were as previously described for routine laparoscopic nephrectomy [9]. The distal ureteric dissection was continued beyond the bifurcation of the iliac vessels. Direct contact with the tumour was avoided. Before entering the urinary tract, clips were placed on the ureter, proximal and distal to the tumour, to prevent tumour spill. For distal ureteric tumours, a wide cuff of bladder was also resected. The proximal clip was placed above the tumour. To do so, surgeons were guided either by direct extrinsic visualization of the tumour if it was bulky enough, or by imaging techniques otherwise. Proximally the ureter was then transected 1 cm above the mass. The specimen was placed in an entrapment bag and retrieved through a port incision (10 mm) without changing the patient’s position. An intraoperative frozen section was taken to verify negative surgical margins. A JJ stent was then placed through a 5-mm port before completing the ureteric re-implantation. A direct re-implantation of the ureter was then done laparoscopically using a 4/0 monofilament (interrupted) suture. No attempt was made to create an anti-refluxing anastomosis. In some patients, a psoas hitch was needed to guarantee a tension-free anastomosis. All patients were left with both a Foley catheter and a JJ stent. To describe peri-operative morbidity and report a negative surgical outcome, we used the Clavien classification (Grade I, II, III, IV or V) as already described [10,14]. Routine surveillance, including abdominal and pelvic CT, cystoscopy, urine cytology and ureteroscopy, was completed at 3 and 6 months, and yearly thereafter.

RESULTS

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. PATIENTS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. CONFLICT OF INTEREST
  8. REFERENCES

Six patients were included in the study. Before surgery, four patients had diagnostic ureteroscopy and biopsies. The patients’ characteristic are given in Table 1. The mean (range) age was 68.5 (54–76) years, the body mass index was 26.03 (23.2–29.8) kg/m2 and the preoperative creatinine level was 115  (68–176) µmol/L. Four patients had had previous abdominal surgery, and one had also previously undergone endoscopic tumour ablation of the distal ureter. Indications for conservative treatment with laparoscopic segmental ureteric resection were absolute in two cases: one solitary kidney and one preoperative renal insufficiency.

Table 1. The characteristics of the six patients (all were men), with their operative and follow-up data. All are currently free of disease
VariablePatient
123456
  1. Preop., preoperative; SP, suprapubic; (R)(L)DU, (right) (left) distal ureter; GH, gross haematuria; PVUD, primary vesico-ureteric to dome.

Age at diagnosis, years687276546959
Smoking, >20/day for 5 yearsYesNoYesYesYesYes
Previous abdominal surgeryCholecystectomyHemicolectomyR prostatectomyAppendectomyNoneNone
History of bladder tumourNoNoYesNoYesNo
Clinical presentationGHFlank pain in solitary kidneyGHUTIHaematuriaGH
Preop. cytology−ve+veAtypicalAtypical+ve+ve
Diagnostic ureteroscopy and biopsyYesNoYesYesYesNo
Preop. creatinine, µmol/L176138901007168
Primary tumour locationRDULDURDURDULDURDU
Concomitant bladder tumourYesNoYesNoNoNo
Operative and follow-up data
Operative duration, min120180240120180200
Type of re-implantPVUDPVUDPVUD + psoas hitchPVUDPVUD + psoas hitchPVUD
Blood loss, mL200501005050120
Complication (grade)NoneNoneUTI (II)NoneAzotaemia (II)Urinoma (III)
Tumour diameter, cm1.92.62.20.81.21.5
Hospital stay, days768556
GradeHighLowLowLowLowHigh
Tumour stagepTa + CISpTapTapTapTa + CISpT2
Recurrence siteBladderRenal pelvisNoneNoneNoneNone
Other treatmentBCG and cystectomyPercutaneous ablationMitomycin CMitomycin CNoneNU
Follow-up, months464240212517

Detailed data and tumour staging are also shown in Table 1. The mean operative duration was 173.3 min and the mean estimated blood loss was 75 mL. The mean length of the ureteric resection was 5.23 cm. Two patients required a psoas hitch. One patient had a tumour in and around the ureteric orifice and had TUR, revealing T2a bladder cancer with ureteric involvement. One patient underwent partial cystectomy (large bladder cuff) along with distal ureterectomy because of a procident tumour. Another patient also had TUR of his ureteric orifice at the time of re-implantation. The Foley catheter was left in situ for 8.2 (6–15) days and the JJ stents were maintained for 25.8 (15–30) days. After surgery minor complications occurred in three patients, including a UTI in one that was treated with antibiotics (Grade II), an obstructed Foley catheter in another, resulting in azotaemia that subsequently resolved after replacing the catheter (Grade II), and one required temporary stent replacement for residual anastomotic oedema and obstruction (Grade III).

All patients are currently alive and free of disease (Table 1). The mean follow-up was 32 months. There were low-grade tumours with no infiltration in four of the six patients. The patient who had initial partial cystectomy and distal ureterectomy had a high-grade lesion associated with CIS within the ureteric specimen. He had progression in the bladder, requiring cystectomy and ileal loop diversion after failing BCG therapy; he is currently free of disease. One patient with a solitary kidney had a recurrence in the treated UUT, and had percutaneous tumour ablation of a renal pelvic recurrence 16 months after the initial surgery. Currently his cytology remains positive, but there are no visible tumours on ureteroscopy or imaging studies. The last patient with an invasive pT2 tumour in the final specimen elected to undergo complete NU for oncological safety. At the last follow-up no patients had had an anastomotic stricture.

DISCUSSION

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. PATIENTS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. CONFLICT OF INTEREST
  8. REFERENCES

Although the ‘gold standard’ for urothelial tumours involving the UUT has been complete excision of the entire kidney and ureter, equivalent oncological outcomes after conservative endoscopic management of low-grade superficial UUT-TCC have been widely reported, suggesting that the removal of the entire ipsilateral UT is not always necessary [5–7]. Proponents of conservative management (i.e. endoscopic ablation and segmental resection) argue that the grade and stage of the primary ureteric tumours are more significant prognostic factors than the extent of surgical resection [4,5,15]. Endoscopic ablation of low-risk, superficial tumours allows the preservation of a portion of the UUT and renal unit while avoiding the morbidity associated with open surgery [3,6]. However, one drawback of endoscopic approaches is the paucity of specimen for pathological evaluation when devices such as the laser are used to treat the tumour [4–6]. However, segmental ureteric resection with wide margins provides an adequate pathological specimen for definitive staging and grade analysis, while preserving the ipsilateral kidney [12,13]. In fact, open segmental ureteric resection results in equivalent oncological outcomes to more extensive resection (i.e. radical NU) in patients with low-grade tumours, but is associated with the same morbidities as open surgery [1,8,13]. Therefore, although absolute indications for each surgical approach are not clearly defined, tumour risk factors such as stage, grade, location and size, as well as existing comorbidities, should all be factors in determining the optimal intervention [15].

To our knowledge, no published series has evaluated outcomes of patients treated with laparoscopic distal ureterectomy and there are only two case reports of laparoscopic segmental ureterectomy [12,13]. In the present short series, we report intermediate-term recurrence and cancer-specific survival results equivalent to those reported following either ONU or endoscopic ablation in highly selected patients with low-grade UUT tumours [3,5].

TCC recurs within the bladder in 20–40% of patients after ONU, reinforcing the importance of close surveillance in the management of urothelial tumours [16–18]. After segmental resection and UUT conservation for UUT-TCC, this is particularly crucial [19]. In the present series, there were two recurrences that required a secondary intervention, including one patient who developed invasive TCC of bladder and went on to have a radical cystectomy. The second patient developed a renal pelvic recurrence in his solitary kidney and had percutaneous ablation. Published data advocate repeat conservative surgery whenever possible for local recurrence [5,6]. At the last follow-up, all patients were free of tumour recurrence.

Accurate preoperative staging is essential to determine the most appropriate surgical procedure [20,21]. It is recommended that all patients with a defect filling the UUT are diagnosed by ureteroscopic biopsy, because staging errors are common with contrast imaging, which does not always evaluate wall infiltration by a UUT-TCC [21,22]. If biopsy had been routine in our centre, the patient with a pT2 tumour understaged by imaging could have benefited from earlier radical ONU and more candidates might have been identified for conservative management [22,23]. For invasive tumours, segmental resection by either open or laparoscopic procedures is not recommended and complete ONU remains the standard of care [1,3]. Several groups suggested that the laparoscopic procedure is questionable whenever the ureteric tumour invades the muscle wall [24,25]. UUT-TCCs are very susceptible to dissemination and recurrence after tumour spill [26,27], and there is a risk of tumour spill whenever the UT is entered during surgical resection of a urothelial tumour. It was postulated that the high-pressure environment of the pneumoperitoneum might exacerbate tumour dissemination and result in a higher recurrence rate [25,26]. To reduce the risk of tumour spill, we strongly advocate strict adherence to techniques aimed at isolating the tumour and preventing the flow of urine from the affected ureter into the peritoneal cavity [25,26]. During the ureteric dissection, direct contact with the tumour should be rigorously avoided. Second, ligation of the ureter proximal and distal to the tumour before transection of the ureteric wall is essential [25,26]. Third, intraoperative frozen sections are imperative for oncological safety, to check surgical margins before opening the bladder to perform any re-implantation. Moreover, lymph node status is becoming increasingly important in patients with UUT-TCCs [28]. We think that such a dissection could also be achieved easily during the laparoscopic procedure.

Technically, one important point is that laparoscopic segmental resection and direct ureteric re-implantation, as described here, do not preclude future surveillance ureteroscopy. The refluxing re-implantation technique allows for ureteroscopic access to the UUT with minimal risk of obstruction or stenosis at the vesico-ureteric anastomosis [12]. For surgical teams accustomed to the laparoscopic techniques used in nephrectomy and PUJ reconstruction, segmental ureteric resection and re-implantation are readily accessible. However, an anti-refluxive ureteric re-implantation could also be considered for improved oncological safety. Although ureteroscopic surveillance could thereafter be more difficult, reflux of tumour cells in the bladder would be theoretically diminished. In the present series, there were no major complications during or after surgery, according to Clavien’s classification [10,14]. Previous abdominal surgery and body habitus did not significantly affect operative duration or blood loss but this might be attributable to the extensive experience in laparoscopic pelvic and UUT surgery at our institution. Apart from technical feasibility, it would also be interesting to see whether the laparoscopic procedure could enhance functional outcomes (i.e. access trauma, stricture formation, anastomosis quality) compared to ureteroscopy.

In conclusion, conservative laparoscopic ureteric resection for treating of superficial, low-grade UUT-TCCs is feasible and early outcomes are encouraging. Precautionary measures to reduce tumour spill are essential. As for all patients with urothelial tumours, patients require close surveillance of the entire urinary tract. However, based upon the present series, laparoscopy could soon be an acceptable alternative to ureteroscopy for treating low-risk distal ureteric tumours. Long-term outcomes with larger series of patients are required before any generalizations can be made.

REFERENCES

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. PATIENTS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. CONFLICT OF INTEREST
  8. REFERENCES