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THE ENDOSCOPIC APPROACH TO THE DISTAL URETER IN NEPHROURETERECTOMY FOR UPPER URINARY TRACT TUMOR
0022-5347/01/1666-2017/0 THE JOURNAL OF UROLOGY® Copyright © 2001 by AMERICAN UROLOGICAL ASSOCIATION, INC.®
Vol. 166, 2017–2022, December 2001 Printed in U.S.A.
Review Article THE ENDOSCOPIC APPROACH TO THE DISTAL URETER IN NEPHROURETERECTOMY FOR UPPER URINARY TRACT TUMOR M. PILAR LAGUNA
AND
JEAN J. M. C. H.
DE LA
ROSETTE
From the Department of Urology, University Medical Center St. Radboud, Nijmegen, The Netherlands
ABSTRACT
Purpose: We reviewed the current status of the endoscopic distal ureteral approach to nephroureterectomy for transitional upper urinary tract cancer. Material and Methods: We reviewed the English, French and Spanish literature using a PubMed and MEDLINE search, and compared the stripping and pluck techniques. Statistical analysis was done using Fisher’s exact test. Individual case reports are discussed but they were not included in the statistical analysis. Results: The mean rate of bladder carcinoma recurrence after ureteral resection and detachment is 19.3% for the stripping and 24% for the pluck technique. This difference is not statistically significant. In 3.1% of cases invasive bladder cancer has been noted but only after distal ureteral resection using the pluck technique. Conclusions: The endoscopic approach to the distal ureter during nephroureterectomy is feasible. Bladder cancer recurrence was similar after each technique. However, isolated case reports illustrate the need for cautious selection of surgical candidates. KEY WORDS: carcinoma, transitional cell; neoplasm recurrence, local; bladder; urinary tract; nephrectomy
The primary diagnosis of upper urinary transitional cell carcinoma accounts for less than 5% of all urothelial tumors.1 A history of bladder carcinoma is present in 20% to 30% of patients and contralateral tumor can present synchronically in up to 2.5%.2– 6 Upper urinary transitional cell carcinoma is more common in patients treated for bladder carcinoma, probably as a result of iterative bladder resection and vesicoureteral reflux.7–9 Nephroureterectomy is the gold standard when an upper urinary tract tumor is not suitable for conservative treatment by endoscopic technique or conservative open surgery.10 –14 The specimen removed must include the complete ureter with a bladder cuff of tissue surrounding the ureteral orifice. The rationale for excising all upper urothelial tissue on the affected side is the high rate of tumoral recurrence in the remaining ureteral stump after nephrectomy only is performed.2, 4, 5, 15, 16 Although tumor grade and stage are the most important determinants of long-term outcome,2–5, 12, 17–21 others factors such as multiplicity22–24 and the type of operation can negatively influence survival.2, 22, 25 Two incisions are usually needed for nephroureterectomy, including a lumbar or subcostal incision and a pararectal or Gibson’s incision to approach the kidney and distal ureter-bladder cuff, respectively. However, an extended abdominal incision can also provide an adequate surgical field. When nephroureterectomy is indicated, a less invasive approach can be used, namely the endoscopic distal ureteral approach, at the beginning of intervention before nephrectomy or at the end of the procedure after nephrectomy, ureteral identification and ligation. Renewed interest in the endoscopic approach to the distal ureter was stimulated by the introduction of laparoscopic nephroureterectomy in clinical practice.26 –29 We reviewed the vari-
ous methods of approaching the distal ureter via endoscopy during nephroureterectomy and evaluated their feasibility and results in terms of bladder tumor recurrence. MATERIALS AND METHODS
A bibliographic PubMed and MEDLINE search was performed for this review. Our report is based on the available English, Spanish and French literature, excluding abstract presentations. Description of techniques. The most common techniques are basically ureteral stripping and the pluck technique, that is intussusception and resection of the intramural and perivesical ureter. Many modifications of the stripping technique have been reported to improve the technique by decreasing the rate of unsuccessful ureteral extractions. Ureteral Stripping: The initial description of the technique is attributed to McDonald.30, 31 Basically the ureter is catheterized at the beginning of the procedure and ligated posterior during the open flank approach. The kidney, proximal and mid ureter are removed via an open loin incision and the catheter is secured to the distal ureter. In the endoscopic approach the patient is then repositioned for ureteral intussusception and pull-through of the ureter through the urethra. After the introduction of a resectoscope ureteral detachment is performed by applying external tension to the catheter and resecting or circumcising the bladder wall.32, 33 With the aim of improving excision many variants have been described, for example traction on the adventitia through the loin incision by Allis clamps or stitches at the beginning of intussusception,34 –36 use of a venous stripper or balloon catheter to secure the ureter,37, 38 double ligation of the ureter over a kinked ureteral catheter39 and longitudinal discharge ureterectomy distal to ureteral ligation.40 The Pluck Technique or Ureteral Endoscopic De-Insertion:
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ENDOSCOPIC APPROACH TO DISTAL URETER FOR UPPER URINARY TRACT TUMOR
This technique consists of resection of the ureteral meatus and surrounding tissue. A conventional resection loop is used and resection is extended along the transmural ureteral trajectory, perforating the bladder wall until perivesical fat is visible and the ureter is completely detached from the bladder. The ureteral lumen and surrounding tissue are carefully and broadly coagulated to seal the ureter and prevent urinary spillage during the remainder of the procedure. After endoscopy is complete the patient is repositioned and nephroureterectomy is performed via a flank incision.30 Dissection of the pelvic ureter is done under direct vision until the iliac vessels are visualized. Gentle traction is then applied, helped by blunt digital dissection. Traction enables extraction of the complete ureter in all cases.41 Examination of the specimen and recognition of the coagulated tip ensure complete excision of the urothelium. In 1972 Abercrombie described a variant of this technique that involves resecting the ureteral roof with a catheter in situ.42 Others perform nephrectomy first with early distal ureteral ligation. Thus, endoscopic resection occurs at the end of the procedure.43 The most important modification of this technique is circumcision of the ureteral orifice by a hook electrode with early coagulation of the ureteral orifice before initiating the endoscopic procedure. Meatal circumcision is continued until perivesical fat is visualized, indicating that the ureter is freed of all perivesical attachments. After the procedure is complete nephroureterectomy is performed via a flank incision in the usual manner. As in the original technique, the coagulated ureteral orifice enables specimen identification.44, 45 Recently a modification of this technique was described with early trans-bladder ligation of the distal ureteral tip during laparoscopic nephroureterectomy.29 Bibliographic material. Although the technique was described almost 5 decades ago, only a small number of procedures have been reported. An even smaller number of series with long-term followup have been published. These studies mainly consist of descriptions of technique modifications or postoperative recurrence. There are no prospective comparative studies comparing open and endoscopic ureteral removal that assessed significant differences. In some series the 2 approaches were compared retrospectively32 or within the same interval.36 Information on bladder recurrence is available in 14 series, of which slightly different stripping methods were used in 532, 33, 35, 36, 46 and 9 involved the pluck technique or a variation.28, 41, 43– 45, 47–50 Survival data are available only occasionally. Followup is not available in 4 studies.28, 32, 35, 43 The site of primary upper urinary transitional cell carcinoma is not available in 1 series,41 while information on primary tumor grade and stage is available in only 2 of the stripping32, 46 and 6 of the pluck41, 43, 45, 47– 49 technique. Data on complications are available in 7 series of the pluck and in 8 of the stripping technique.28, 29, 32, 33, 35, 36, 39 – 47, 49 There are 3 isolated case reports of invasive bladder recurrence51–53 and an extensive series involving the pluck technique.27 Statistical methods. Due to the variety of techniques and reports lacking important information performing statistical analysis is difficult. For comparing bladder recurrence in the 2 techniques only tumor cases were considered and Fisher’s exact test was used with p ⬍0.05 considered significant. The lack of information in unpublished series and the weak evidence based value of the isolated case reports precluded their inclusion in statistical analysis. For calculating the complication rate tumor cases and the other series were included as well as series mentioning only a description of the technique. Only series specifically mentioning the rate and characteristics of complications were included in analysis.
RESULTS
Characteristics of primary upper urinary tract tumors. The characteristics of primary upper urinary tumors are described in 8 series (table 1). The primary tumor was invasive in 16.6% of cases treated with the stripping and in 48.6% treated with the pluck procedure. In the series of Clayman et al high grade tumors were managed by intramural ureter resection or by unroofing without ureteral detachment.33 Bladder recurrence. Of patients who underwent the stripping and pluck procedure 62 and 129 were followed, respectively (table 2). The recurrence rate varied depending on the specific approach to the distal ureter, namely 19.3% in stripping and 24% in pluck series, which was not significant (Fisher’s exact test p ⫽ 0.581). With a 95% confidence interval the odds ratio for bladder recurrence was 1.29-fold higher for the pluck than for the stripping technique but again this value was not significant. To date 9 bladder recurrences have been described at the resection site, including 5 corresponding to superficial bladder tumors and 4 (3.1%) involving invasive bladder recurrence. These recurrences developed after the pluck technique. As indicated, 3 additional invasive bladder recurrences were reported as isolated cases.51–53 All except 1 invasive tumor were diagnosed within year 1 after primary treatment (table 3). Interestingly no pelvic or trigonal invasive or superficial bladder recurrence has been described after the stripping procedure. Complications. Table 4 lists the complications of the 2 procedures. The pluck technique or resection of the distal ureter has a low complication rate and according to the reports of various groups it is feasible in all cases.41, 45, 49 The 2.7% immediate postoperative complication rate involves extravasation, which was due at least in 1 case to inadvertent intraperitoneal perforation during the endoscopic procedure.29, 41, 45 The 10% complication rate of the stripping technique is usually due to the ureteral catheter hindering endoscopic ureteral extraction. Catheter breakage, the impossibility of urethral progression and even anchorage of the pelvic ureter have led to an open conversion rate of between 9.5% and 12.5%.35, 36, 39, 40, 46 A urethral stricture was noted in a male patient after difficult extraction.46 General considerations. Mean hospital stay after endoscopic ureteral treatment varies widely between 4.6 and 11 days.32, 36, 43, 45, 49 The mean duration of bladder catheterization is 3 to 8 days.33, 39, 40, 43, 48 Only 1 series mentioned a prolonged bladder catheterization duration of 14 days. Patients who undergo the laparoscopic procedure are often discharged home within 24 hours.29 Mean endoscopic operative time is short at 22 minutes for the pluck49 and less than 45 minutes for the stripping36 technique. A modification of the pluck technique requires about 90 minutes.29 Total intervention time varies between 156 and 205 minutes, including 1 laparoscopic series.28, 33, 36, 46
TABLE 1. Characteristics of primary upper urinary transitional cell carcinoma References
No. Noninvasive
No. Invasive
Stripping procedure 16 2* Clayman et al33 14 4 Jacobsen et al46 Pluck procedure 47 2 3 Hetherington et al 10 6 Abercrombie et al48 41 12 18 Palou et al 43 2 3 Sawa et al 2 4 Kural et al49 45 10 6 Polo Peris et al * High grade, high stage tumors treated with intramural resection without ureteral detachment.
2019
ENDOSCOPIC APPROACH TO DISTAL URETER FOR UPPER URINARY TRACT TUMOR TABLE 2. Endoscopic ureteral removal in patients with tumor References
No. Pts.
Recurrence
Tumor Site
No. Bladder (%)
Stripping procedure: 18 (14 followed) Renal pelvis, 1 ureter* Clayman et al33 9 Renal pelvis, calix Valdivia et al35 46 Jacobsen 1994 18 (16 followed) Renal pelvis, ureter 32 8 Renal pelvis Zubac et al 15 Renal pelvis Angulo et al36 Followed 62 Pluck procedure: 5 Renal pelvis, ureter Hetherington et al47 50 Carr et al 19 Not available 16 Renal pelvis Abercrombie et 48 al 41 Palou et al 30 Sawa et al43 5 Renal pelvis, ureter 49 6 Renal pelvis, ureter Kural et al 45 16 Renal pelvis, ureter Polo Peris et al 19 Renal pelvis Keeley and 28 Tolley 44 Shental et al 12 Renal pelvis, calix Followed 129 * High grade tumors treated with intramural resection without ureteral detachment.
3 (21.4) 2 (22.2) 2 (12.5) 1–2 (18) 3 (20) (19.3)
No. Resection Area
Followup
No No No No No No
5 Yrs. Not available 6–60 Mos. Not available 44.6 Mos.
(60)
2
14 Mos.
6 (33.3) 6 (37.5)
1 4
23.5 Mos. 3–5 Yrs.
No 2 No No No
20 Mos. Not available 18.6 Mos. 17 Mos. Not available
3
11 (27.3) 2 (40) 1 (16.6) No No 2 (16.6) (24)
No 27 Mos. 9 (5 superficial, 4 invasive)
TABLE 3. Characteristics of invasive bladder tumor recurrence Transitional Cell Ca
No. Recurrences
References
Site
Hetherington et al47
2
Renal pelvis
Sawa et al43
1
Renal pelvis
Abercrombie et al48 Arango et al51* Jones and Moisey52*
1 1 1
Renal pelvis Renal pelvis, calix Renal pelvis, ureter, resected area Renal pelvis
Fernandez Gomez et al53* * Case report.
1
TABLE 4. Complications of endoscopic ureteral removal in all cases and series No. Procedures
References Pluck procedures: Polo Peris et al45 Kural et al49 Hetherington et al47 Sawa et al43 Palou et al41
16 12 5 5 31
Gill et al29 Keeley and Tolley28 Shental et al44
8 19 13
Totals Stripping procedure: Coulange et al40 Jacobsen et al46
109 25 18
Angulo et al36 Valdivia Uria et al35 Clayman et al33 Zubac and Kihl32 Roth et al39
21 9 18 8 8
Totals * Open conversion in 7 cases.
107
No. Complications 1 Extravasation 0 0 0 1 Extravasation due to intraperitoneal perforation 1 Extravasation 0 0 3 3 Ureteral breakage* 2 Stuck in urethra,* 1 urethral stricture 2 Retained ureters* 2 Ureteral breakage* 0 0 1 Dislodged catheter 11
DISCUSSION
To evaluate the results of a nonstandard technique in terms of efficacy, complications and costs it must be compared with a standard technique in prospective and randomized studies. Although the endoscopic approach to the distal ureter is not new in the literature, none of these techniques
Pathology Grade 3 stage pT4, grade 1, stage pT1 Grade 3
Bladder Recurrence Site
Time
Resected area
4, 9 Mos. 6 Mos.
Stage 3 Grade 2 stage pT1 Poorly differentiated
Ipsilat. squamous bladder tumor Ureteral scar Resected area Resected area
4 Yrs. 7 Mos. 3 Mos.
High grade, stage
Resected ureter
6 Mos.
has been widely used and their results have been questioned in oncological terms. In this case difficulty arises due to the retrospective design of the series as well as to the impossibility of randomization, the rarity of upper urinary transitional cell carcinoma and the selective indication for endoscopic treatment of the distal ureter, making the task extremely long and almost impossible. There are certain main questions to be answered. Do endoscopic techniques cause a major risk of bladder or pelvic recurrence? Is the rate of invasive bladder recurrence greater than when the distal ureter is approached in open fashion? Does endoscopic excision of the distal ureter result in more or fewer complications than the standard technique? After nephroureterectomy for upper urinary transitional cell carcinoma bladder recurrence is not uncommon. The rate of bladder recurrence after classic nephroureterectomy is between 23% and 30%.2–5, 16, 20, 54 Bladder recurrence is more common when there is a history of bladder cancer and recurrence is directly related to the grade of primary upper urinary transitional cell carcinoma.3, 24 In up to 80% of cases bladder recurrence appears during the initial 2 or 3 years after treatment of primary upper urinary transitional cell carcinoma.2, 4, 5, 55 Bladder tumors are of a similar grade in 89% of cases and the same stage in 72%.2 Few studies of open nephroureterectomy clearly indicate the site of bladder recurrence, which appears to be more common in the ipsilateral hemibladder adjacent to the ipsilateral ureteral orifice.56 In a morphological study of urinary tract distribution of lesions in primary upper urinary transitional cell carcinoma Kakizoe et al observed that 80% of cases of concurrent or subsequent bladder cancer had multiple lesions on the same side as primary upper urinary transitional cell carcinoma.55
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ENDOSCOPIC APPROACH TO DISTAL URETER FOR UPPER URINARY TRACT TUMOR
Although a description of bladder recurrence site is rare, even more scarce are reports of the pattern of this recurrence. The majority of reported series focus on parameters such a prognosis and survival. The rate of invasive bladder recurrence after open nephroureterectomy is 2% to 3%.2, 3, 16 To our knowledge only 1 series indicates an extremely high 25% rate of invasive concurrent or subsequent bladder tumors but patient characteristics in this series hardly reflect the natural presentation of upper urinary transitional cell carcinoma.55 No difference was noted in terms of bladder recurrence in classic open series and those of the endoscopic approach to the distal ureter. Invasive ipsilateral bladder trigonal or pelvic recurrence after endoscopic removal of the distal ureter is dramatic. In these cases perioperative seeding has been suggested and, thus, this condition has become the main contraindication to these techniques. To date 7 invasive bladder recurrences have been described, including some isolated case reports without information extending for the duration of the study, if at all.51–53 All recurrences were noted after the pluck procedure. Nevertheless, in the context of the total number of patients treated in the series only 4 invasive recurrences were described. This value corresponds to 3.1% of patients who undergo the pluck procedure and it is similar to the rate of invasive bladder recurrence after classic excision. All except 1 invasive recurrence appeared early during followup and within year 1 after treatment of primary upper urinary transitional cell carcinoma. Analysis of these invasive recurrences shows that only 4 can be directly attributed to tumor spillage.47, 51, 53 In 1 case there was a poorly differentiated tumor in the ureteral resected area and, thus, the bladder invasive tumor diagnosed 3 months later can be better considered persistence rather than recurrence.52 Moreover, tumor in the area to be resected represents a formal contraindication to any endoscopic approach. In another case bladder tumor pathology was quite different from primary tumor pathology since the latter was high grade carcinoma. Furthermore, ureteral resection was performed at the end of the surgical procedure after early ureteral ligation to prevent spillage.43 Thus, although seeding cannot be completely ruled out, the evolution is more suggestive of panurothelial disease rather than tumor spillage. Although the invasive recurrence reported by Abercrombie et al was located over the resection scar, it appeared 4 years after resection, making it unlikely that it was due to tumor seeding during primary endoscopic treatment.48 Differences in the development of subsequent invasive bladder cancer in the 2 techniques can be attributable to the technique or to differences in the pathological pattern of the primary tumor. Due to the lack of complete information in the series proper multifactorial analysis was not be performed. The possibility of tumor spillage cannot be excluded during the pluck technique, especially since no cases of recurrent invasive bladder cancer have been described after the stripping procedure. The difference in the rate of subsequent invasive bladder tumor in the stripping and pluck techniques may be due to a different pathological pattern of primary upper urinary transitional cell carcinoma. Interestingly in recent and extensive series of the pluck technique no invasive bladder or pelvic recurrence has been described,41, 44 although in some more than half of the patients presented with high grade and stage primary upper urinary transitional cell carcinoma.41 The importance of extensive and careful coagulation of the ureter lumen cannot be overemphasized. It would be interesting to identify comparative series in which the incidence of complications was compared. To our knowledge only 2 series have compared traditional nephroureterectomy with the endoscopic ureteral approach.32, 36 In the series of Angulo et al 19 and 15 patients underwent
1-incision, endoscopically assisted nephroureterectomy and the 2-incision standard technique, respectively.36 Mean operative time and mean hospital stay showed statistically significant differences in favor of endoscopically assisted nephroureterectomy. Mean estimated blood loss was less for the endoscopic approach, although no significant difference was noted when compared with the classic 2-incision procedure (240 and 392 cc, respectively). Postoperatively complications were equal in the 2 groups. Zubac and Kihl confirmed the benefits of endoscopic removal of the distal ureter in terms of mean hospital stay and survival.32 The need for less analgesia has been advocated but to our knowledge it has not been properly documented. The pluck technique and its modifications at the level of bladder resection has been shown to be feasible and easy to perform with a low rate of complications. Extravasation and pelvic abscess are also possible after open excision of the bladder cuff. Although the possibility of bladder bleeding was not described in the largest series, it must be considered, as for any bladder tumor resection.57 From the technical point of view the stripping procedure and its variations may require more learning time than endoscopic resection. The technical inconveniences of stripping accounts for approximately 10% of conversions to open surgery, which remains the gold standard and primary technique of choice for most surgeons. A discussion of the benefits or inconveniences of the endoscopic distal ureteral approach would be of little interest if we ignored the trend toward minimally invasive surgery in oncology. In the last 5 years laparoscopic nephroureterectomy for upper urinary transitional cell carcinoma has emerged as a valid alternative to open surgery even in elderly patients.58, 59 To date only 4 series have described laparoscopic nephroureterectomy for upper urinary transitional cell carcinoma,28, 60 – 62 of which 1 includes a previous report from the same group.26, 62, 63 Three techniques of bladder cuff excision have been advocated. In 2 of these series open bladder cuff excision was performed.60, 61 In the most recent comparative series most distal ureters were approached by transurethral unroofing and electrocoagulation or resection to the ureterovesical junction but without penetration of the bladder wall.62 Laparoscopic tenting and ureteral stapling were then performed, following the previously described technique of high grade upper urinary transitional cell carcinoma.32 At 24 months of followup the rate of bladder recurrence was 23%, equal to the rate of the open procedure in the same series. Importantly there was a lower rate of major complications in the laparoscopic group (8% versus 29%), emphasizing the future potential impact of laparoscopic nephroureterectomy.62 As early as 1993, the pluck technique was mentioned by Rassweiler et al as a natural complement to laparoscopic nephroureterectomy.27 They based the choice on the excellent results achieved when they applied the technique in open surgery. This preliminary report was followed by the series of Keeley and Tolley of 19 cases of laparoscopic nephroureterectomy complemented by resection of the distal ureter until detachment with no bladder recurrence.28 They limited this technique to patients with pyelic or caliceal tumors and used other methods when a ureter tumor was present. No complications or open conversions were attributable to the pluck technique. This series compares the open and laparoscopic approaches. The rate of postoperative complications was similar for laparoscopic and open surgery (27% and 35%, respectively). When other factors are compared, the rate appears more favorable in the laparoscopic group since the rate of pulmonary complications was lower (4.5% versus 19%), hospital stay was shorter (5.5 versus 10.8 days) and the transfusion requirement was less (0.3 versus 0.9 units). Using the pluck technique Keeley and Tolley
ENDOSCOPIC APPROACH TO DISTAL URETER FOR UPPER URINARY TRACT TUMOR
achieved an operative time that was equal to that of open surgery. More recently Gill et al presented 8 cases of laparoscopy using a modification of the pluck procedure with early transbladder ligation of the ureteral distal tip, and circumcision of the intramural and perivesical ureter until detachment.29 Although procedure time was longer than that of the original technique, there may be a hypothetical advantage to early ureteral ligation. CASE SELECTION
Case selection is probably the most important factor when deciding to use the endoscope to remove the ureter during nephroureterectomy. Because of the major disadvantage of possible tumor cell seeding, surgical boundaries must be far from the tumor. Therefore, a known ureteral tumor seems to be a formal contraindication to the endoscopic technique. Technically the pluck technique can be used even when a proximal ureter tumor is present as long as some safeguards are met, namely early sealing of the ureteral ostium or ureteral ligation. This maneuver may at least theoretically prevent the flow of urine in the pelvic field. Nevertheless, this technique must be used with care when a ureteral tumor is suspected. For some groups that advocate ureteral stripping a synchronous bladder tumor is a contraindication to the pluck technique due to the danger of perivesical tumor implantation. In reports of directly attributable tumor spillage no bladder tumor resection was performed at the time of the pluck procedure. To our knowledge the question remains unresolved. In addition, preoperative assessment of any cause causing periureteral fibrosis must be considered. Since pelvic ureteral detachment is performed in blind fashion in all endoscopic techniques, an anchored distal ureter would hinder ureteral removal, leaving the possibility of ureteral breakage and urothelial remnants remaining in place. Consequently previous surgery or irradiation of the pelvic field, distal aortic or iliac aneurysm and inflammatory pelvic diseases as well as retroperitoneal fibrosis represent a formal contraindication to these techniques. We can state that the case for these methods involves low grade and stage upper urinary transitional cell carcinoma at a pyelic and/or caliceal site and as part of laparoscopic nephroureterectomy, making this procedure entirely endoscopic and minimally invasive. The case against these techniques involves high disease grade and stage, and/or a ureteral tumor or multiplicity and suspected pelvic fibrosis/adhesions. CONCLUSIONS
Although endoscopic removal of the distal ureter is not yet widely done, most techniques have already proved their feasibility. Whether invasive bladder or pelvic recurrence should be attributed to spillage during performance of the technique remains unanswered but concerns about a higher rate of invasive bladder cancer have not been confirmed in larger current series. The pluck technique has a lower complication rate than the stripping technique but after the latter no invasive bladder recurrence has been described. When deciding on the endoscopic distal ureteral approach, careful patient selection is necessary. When a distal ureteral tumor is suspected during surgery, the procedure should be converted to open excision. The pluck technique or a modification with early ureteral sealing, and circumcision of the intramural and perivesical ureter until detachment may be the ideal supplement to laparoscopic nephroureterectomy. REFERENCES
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32. 33. 34. 35. 36. 37. 38. 39. 40. 41. 42. 43. 44. 45. 46. 47.
ENDOSCOPIC APPROACH TO DISTAL URETER FOR UPPER URINARY TRACT TUMOR
carcinoma entirely minimally invasive. J Endourol, 12: 139, 1998 Gill, I. S., Soble, J. J., Miller, S. D. et al: A novel technique for management of the en bloc bladder cuff and distal ureter during laparoscopic nephroureterectomy. J Urol, 161: 430, 1999 Mc Donald H. P., Upchurch, W. E. and Sturdevant, C. E.: Nephro-ureterectomy: a new technique. J Urol, 67: 804, 1952 Mc Donald, D. F.: Intussusception ureterectomy: a method of removal of the ureteral stump at time of nephroureterectomy without an additional incision. Surg Gynecol Obstet, 97: 565, 1953 Zubac, D. P. and Kihl, B.: One or two incisions for nephroureterectomy in transitional cell renal pelvis tumours. Scand J Urol Nephrol, 31: 431, 1997 Clayman, R. V., Garske, G. L. and Lange, P. H.: Total nephroureterectomy with ureteral intussusception and transurethral ureteral detachment and pull-through. Urology, 21: 482, 1983 Dell’Adami, G. and Breda, G.: Transurethral or endoscopic ureterectomy. Eur Urol, 2: 156, 1976 Valdivia Uria, J. G., Lopez Lopez, J. A., Bayo Ochoa, A. et al: [Endoscopic ureterectomy.] Arch Esp Urol, 44: 573, 1991 Angulo, J. C., Hontoria, J. and Sanchez-Chapado, M.: Oneincision nephroureterectomy endoscopically assisted by transurethral ureteral stripping. Urology, 52: 203, 1998 Miskowiak, J.: Stripping of the distal ureter after nephrectomy for pelvis papilloma. Scand J Urol Nephrol, 20: 285, 1986 Kaye, K. W.: Ureteral intussusception catheter for one-incision nephroureterectomy. Urology, 27: 358, 1986 Roth, S., van Ahlen, H., Semjonow, A. et al: Modified ureteral stripping as an alternative to open surgical ureterectomy. J Urol, 155: 1568, 1996 Coulange, C., Leremboure, H., Albert, P. et al: [Our experience using ureteral stripping in nephroureterectomy.] Ann Urol, 22: 355, 1988 Palou, J., Caparros, J., Orsola, A. et al: Transurethral resection of the intramural ureter as the first step of nephroureterectomy. J Urol, 154: 43, 1995 Abercrombie, G. F.: Nephroureterectomy. Proc R Soc Med, 65: 1021, 1972 Sawa, T. E., Lendorf, A. and Kvist, E.: Single incision, endoscopically assisted nephroureterectomy for tumors of the upper urinary tract. Scand J Urol Nephrol, 30: 273, 1996 Shental, J., Rozenman, J., Chaimowitch, G. et al: Nephroureterectomy through a single lumbar incision combined with endoscopic incision of a bladder cuff. Urol Int, 62: 147, 1999 Polo Peris, A. C., Gonzalvo Perez, V., Navarro Anton, J. A. et al: [Endoscopic removal of the ureter prior to nephroureterectomy. Preliminary analysis.] Actas Urol Esp, 22: 595, 1998 Jacobsen, J. D., Raffnsoe, B., Olesen, E. et al: Stripping of the distal ureter in association with nephroureterectomy. Evaluation of the method. Scand J Urol Nephrol, 28: 45, 1994 Hetherington, J. W., Ewing, R. and Philp, N. H.: Modified
48. 49.
50. 51. 52. 53.
54. 55. 56.
57. 58.
59. 60. 61.
62. 63.
Nephroureterectomy: a risk of tumor implantation. Br J Urol, 58: 368, 1986 Abercrombie, G. F., Eardley, I., Payne, S. R. et al: Modified nephro-ureterectomy. Long-term follow-up with particular reference to subsequent bladder tumors. Br J Urol, 61: 198, 1988 Kural, A. R., Demirkesen, O., Arar, O. et al: Modified “pluck” nephroureterectomy for upper urinary tract disorders: combined endourologic and open approach. J Endourol, 11: 131, 1997 Carr, T., Powell, P. H., Ramsden, P. D. et al: Nephroureterectomy [letter to the editor]. Br J Urol, 59: 99, 1987 Arango, O., Bielsa, O., Carles, J. et al: Massive tumor implantation in the endoscopic resected area in modified nephroureterectomy. J Urol, 157: 1839, 1997 Jones, D. R. and Moisey, C. U.: A cautionary tale of the modified “pluck” nephroureterectomy. Br J Urol, 71: 486, 1993 Fernandez Gomez, J. M., Barmadah, S. E., Perez Garcia, J. et al: [Risk of tumor seeding after nephroureterectomy combined with endoscopic resection of the ureteral meatus.] Arch Esp Urol, 51: 829, 1998 Racioppi, M., D’Addessi, A., Alcini, A. et al: Clinical review of 100 consecutive surgically treated patients with upper urinary tract transitional tumours. Br J Urol, 80: 707, 1997 Kakizoe, T., Fujita, J., Murase, T. et al: Transitional cell carcinoma of the bladder in patients with renal, pelvic and ureteral cancer. J Urol, 124: 17, 1980 Droller, M. J.: Transitional cell cancer: upper tracts and bladder. In: Campbell’s Urology, 5th ed. Edited by P. C. Walsh, R. F. Gittes, A. D. Perlmutter et al. Philadelphia: W. B. Saunders, p. 1343, 1986 Palou Redorta, J., Caparros Sariol, J., Salvador Bayarri, J. et al: [Simplified technique of nephroureterectomy.] Arch Esp Urol, 44: 809, 1991 Hsu, T. H., Gill, I. S., Fazeli-Matin, S. et al: Radical nephrectomy and nephroureterectomy in the octogenarian and nonagenarian: comparison of laparoscopic and open approaches. Urology, 53: 1121, 1999 McDougall, E. M. and Clayman, R. V.: Laparoscopic nephrectomy and nephroureterectomy in the octogenarian with a renal tumor. J Laparoendosc Surg, 4: 233, 1994 Salomon, L., Hoznek, A., Cicco, A. et al: Retroperitoneoscopic nephroureterectomy for renal pelvic tumors with a single iliac incision. J Urol, 161: 541, 1999 Chung, H. J., Chiu, A. W., Chen, K. K. et al: Retroperitoneoscopy-assisted nephroureterectomy for the management of upper tract urothelial cancer. MIT, 5: 266, 1996 Shalhav, A. L., Dunn, M. D., Portis, A. J. et al: Laparoscopic nephroureterectomy for upper tract transitional cell cancer: the Washington University experience. J Urol, 163: 1100, 2000 Kerbl, K., Clayman, R. V., McDougall, E. M. et al: Laparoscopic nephro-ureterectomy: evaluation of first clinical series. Eur Urol, 23: 431, 1993.
Vol. 166, 2017–2022, December 2001 Printed in U.S.A.
Review Article THE ENDOSCOPIC APPROACH TO THE DISTAL URETER IN NEPHROURETERECTOMY FOR UPPER URINARY TRACT TUMOR M. PILAR LAGUNA
AND
JEAN J. M. C. H.
DE LA
ROSETTE
From the Department of Urology, University Medical Center St. Radboud, Nijmegen, The Netherlands
ABSTRACT
Purpose: We reviewed the current status of the endoscopic distal ureteral approach to nephroureterectomy for transitional upper urinary tract cancer. Material and Methods: We reviewed the English, French and Spanish literature using a PubMed and MEDLINE search, and compared the stripping and pluck techniques. Statistical analysis was done using Fisher’s exact test. Individual case reports are discussed but they were not included in the statistical analysis. Results: The mean rate of bladder carcinoma recurrence after ureteral resection and detachment is 19.3% for the stripping and 24% for the pluck technique. This difference is not statistically significant. In 3.1% of cases invasive bladder cancer has been noted but only after distal ureteral resection using the pluck technique. Conclusions: The endoscopic approach to the distal ureter during nephroureterectomy is feasible. Bladder cancer recurrence was similar after each technique. However, isolated case reports illustrate the need for cautious selection of surgical candidates. KEY WORDS: carcinoma, transitional cell; neoplasm recurrence, local; bladder; urinary tract; nephrectomy
The primary diagnosis of upper urinary transitional cell carcinoma accounts for less than 5% of all urothelial tumors.1 A history of bladder carcinoma is present in 20% to 30% of patients and contralateral tumor can present synchronically in up to 2.5%.2– 6 Upper urinary transitional cell carcinoma is more common in patients treated for bladder carcinoma, probably as a result of iterative bladder resection and vesicoureteral reflux.7–9 Nephroureterectomy is the gold standard when an upper urinary tract tumor is not suitable for conservative treatment by endoscopic technique or conservative open surgery.10 –14 The specimen removed must include the complete ureter with a bladder cuff of tissue surrounding the ureteral orifice. The rationale for excising all upper urothelial tissue on the affected side is the high rate of tumoral recurrence in the remaining ureteral stump after nephrectomy only is performed.2, 4, 5, 15, 16 Although tumor grade and stage are the most important determinants of long-term outcome,2–5, 12, 17–21 others factors such as multiplicity22–24 and the type of operation can negatively influence survival.2, 22, 25 Two incisions are usually needed for nephroureterectomy, including a lumbar or subcostal incision and a pararectal or Gibson’s incision to approach the kidney and distal ureter-bladder cuff, respectively. However, an extended abdominal incision can also provide an adequate surgical field. When nephroureterectomy is indicated, a less invasive approach can be used, namely the endoscopic distal ureteral approach, at the beginning of intervention before nephrectomy or at the end of the procedure after nephrectomy, ureteral identification and ligation. Renewed interest in the endoscopic approach to the distal ureter was stimulated by the introduction of laparoscopic nephroureterectomy in clinical practice.26 –29 We reviewed the vari-
ous methods of approaching the distal ureter via endoscopy during nephroureterectomy and evaluated their feasibility and results in terms of bladder tumor recurrence. MATERIALS AND METHODS
A bibliographic PubMed and MEDLINE search was performed for this review. Our report is based on the available English, Spanish and French literature, excluding abstract presentations. Description of techniques. The most common techniques are basically ureteral stripping and the pluck technique, that is intussusception and resection of the intramural and perivesical ureter. Many modifications of the stripping technique have been reported to improve the technique by decreasing the rate of unsuccessful ureteral extractions. Ureteral Stripping: The initial description of the technique is attributed to McDonald.30, 31 Basically the ureter is catheterized at the beginning of the procedure and ligated posterior during the open flank approach. The kidney, proximal and mid ureter are removed via an open loin incision and the catheter is secured to the distal ureter. In the endoscopic approach the patient is then repositioned for ureteral intussusception and pull-through of the ureter through the urethra. After the introduction of a resectoscope ureteral detachment is performed by applying external tension to the catheter and resecting or circumcising the bladder wall.32, 33 With the aim of improving excision many variants have been described, for example traction on the adventitia through the loin incision by Allis clamps or stitches at the beginning of intussusception,34 –36 use of a venous stripper or balloon catheter to secure the ureter,37, 38 double ligation of the ureter over a kinked ureteral catheter39 and longitudinal discharge ureterectomy distal to ureteral ligation.40 The Pluck Technique or Ureteral Endoscopic De-Insertion:
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ENDOSCOPIC APPROACH TO DISTAL URETER FOR UPPER URINARY TRACT TUMOR
This technique consists of resection of the ureteral meatus and surrounding tissue. A conventional resection loop is used and resection is extended along the transmural ureteral trajectory, perforating the bladder wall until perivesical fat is visible and the ureter is completely detached from the bladder. The ureteral lumen and surrounding tissue are carefully and broadly coagulated to seal the ureter and prevent urinary spillage during the remainder of the procedure. After endoscopy is complete the patient is repositioned and nephroureterectomy is performed via a flank incision.30 Dissection of the pelvic ureter is done under direct vision until the iliac vessels are visualized. Gentle traction is then applied, helped by blunt digital dissection. Traction enables extraction of the complete ureter in all cases.41 Examination of the specimen and recognition of the coagulated tip ensure complete excision of the urothelium. In 1972 Abercrombie described a variant of this technique that involves resecting the ureteral roof with a catheter in situ.42 Others perform nephrectomy first with early distal ureteral ligation. Thus, endoscopic resection occurs at the end of the procedure.43 The most important modification of this technique is circumcision of the ureteral orifice by a hook electrode with early coagulation of the ureteral orifice before initiating the endoscopic procedure. Meatal circumcision is continued until perivesical fat is visualized, indicating that the ureter is freed of all perivesical attachments. After the procedure is complete nephroureterectomy is performed via a flank incision in the usual manner. As in the original technique, the coagulated ureteral orifice enables specimen identification.44, 45 Recently a modification of this technique was described with early trans-bladder ligation of the distal ureteral tip during laparoscopic nephroureterectomy.29 Bibliographic material. Although the technique was described almost 5 decades ago, only a small number of procedures have been reported. An even smaller number of series with long-term followup have been published. These studies mainly consist of descriptions of technique modifications or postoperative recurrence. There are no prospective comparative studies comparing open and endoscopic ureteral removal that assessed significant differences. In some series the 2 approaches were compared retrospectively32 or within the same interval.36 Information on bladder recurrence is available in 14 series, of which slightly different stripping methods were used in 532, 33, 35, 36, 46 and 9 involved the pluck technique or a variation.28, 41, 43– 45, 47–50 Survival data are available only occasionally. Followup is not available in 4 studies.28, 32, 35, 43 The site of primary upper urinary transitional cell carcinoma is not available in 1 series,41 while information on primary tumor grade and stage is available in only 2 of the stripping32, 46 and 6 of the pluck41, 43, 45, 47– 49 technique. Data on complications are available in 7 series of the pluck and in 8 of the stripping technique.28, 29, 32, 33, 35, 36, 39 – 47, 49 There are 3 isolated case reports of invasive bladder recurrence51–53 and an extensive series involving the pluck technique.27 Statistical methods. Due to the variety of techniques and reports lacking important information performing statistical analysis is difficult. For comparing bladder recurrence in the 2 techniques only tumor cases were considered and Fisher’s exact test was used with p ⬍0.05 considered significant. The lack of information in unpublished series and the weak evidence based value of the isolated case reports precluded their inclusion in statistical analysis. For calculating the complication rate tumor cases and the other series were included as well as series mentioning only a description of the technique. Only series specifically mentioning the rate and characteristics of complications were included in analysis.
RESULTS
Characteristics of primary upper urinary tract tumors. The characteristics of primary upper urinary tumors are described in 8 series (table 1). The primary tumor was invasive in 16.6% of cases treated with the stripping and in 48.6% treated with the pluck procedure. In the series of Clayman et al high grade tumors were managed by intramural ureter resection or by unroofing without ureteral detachment.33 Bladder recurrence. Of patients who underwent the stripping and pluck procedure 62 and 129 were followed, respectively (table 2). The recurrence rate varied depending on the specific approach to the distal ureter, namely 19.3% in stripping and 24% in pluck series, which was not significant (Fisher’s exact test p ⫽ 0.581). With a 95% confidence interval the odds ratio for bladder recurrence was 1.29-fold higher for the pluck than for the stripping technique but again this value was not significant. To date 9 bladder recurrences have been described at the resection site, including 5 corresponding to superficial bladder tumors and 4 (3.1%) involving invasive bladder recurrence. These recurrences developed after the pluck technique. As indicated, 3 additional invasive bladder recurrences were reported as isolated cases.51–53 All except 1 invasive tumor were diagnosed within year 1 after primary treatment (table 3). Interestingly no pelvic or trigonal invasive or superficial bladder recurrence has been described after the stripping procedure. Complications. Table 4 lists the complications of the 2 procedures. The pluck technique or resection of the distal ureter has a low complication rate and according to the reports of various groups it is feasible in all cases.41, 45, 49 The 2.7% immediate postoperative complication rate involves extravasation, which was due at least in 1 case to inadvertent intraperitoneal perforation during the endoscopic procedure.29, 41, 45 The 10% complication rate of the stripping technique is usually due to the ureteral catheter hindering endoscopic ureteral extraction. Catheter breakage, the impossibility of urethral progression and even anchorage of the pelvic ureter have led to an open conversion rate of between 9.5% and 12.5%.35, 36, 39, 40, 46 A urethral stricture was noted in a male patient after difficult extraction.46 General considerations. Mean hospital stay after endoscopic ureteral treatment varies widely between 4.6 and 11 days.32, 36, 43, 45, 49 The mean duration of bladder catheterization is 3 to 8 days.33, 39, 40, 43, 48 Only 1 series mentioned a prolonged bladder catheterization duration of 14 days. Patients who undergo the laparoscopic procedure are often discharged home within 24 hours.29 Mean endoscopic operative time is short at 22 minutes for the pluck49 and less than 45 minutes for the stripping36 technique. A modification of the pluck technique requires about 90 minutes.29 Total intervention time varies between 156 and 205 minutes, including 1 laparoscopic series.28, 33, 36, 46
TABLE 1. Characteristics of primary upper urinary transitional cell carcinoma References
No. Noninvasive
No. Invasive
Stripping procedure 16 2* Clayman et al33 14 4 Jacobsen et al46 Pluck procedure 47 2 3 Hetherington et al 10 6 Abercrombie et al48 41 12 18 Palou et al 43 2 3 Sawa et al 2 4 Kural et al49 45 10 6 Polo Peris et al * High grade, high stage tumors treated with intramural resection without ureteral detachment.
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ENDOSCOPIC APPROACH TO DISTAL URETER FOR UPPER URINARY TRACT TUMOR TABLE 2. Endoscopic ureteral removal in patients with tumor References
No. Pts.
Recurrence
Tumor Site
No. Bladder (%)
Stripping procedure: 18 (14 followed) Renal pelvis, 1 ureter* Clayman et al33 9 Renal pelvis, calix Valdivia et al35 46 Jacobsen 1994 18 (16 followed) Renal pelvis, ureter 32 8 Renal pelvis Zubac et al 15 Renal pelvis Angulo et al36 Followed 62 Pluck procedure: 5 Renal pelvis, ureter Hetherington et al47 50 Carr et al 19 Not available 16 Renal pelvis Abercrombie et 48 al 41 Palou et al 30 Sawa et al43 5 Renal pelvis, ureter 49 6 Renal pelvis, ureter Kural et al 45 16 Renal pelvis, ureter Polo Peris et al 19 Renal pelvis Keeley and 28 Tolley 44 Shental et al 12 Renal pelvis, calix Followed 129 * High grade tumors treated with intramural resection without ureteral detachment.
3 (21.4) 2 (22.2) 2 (12.5) 1–2 (18) 3 (20) (19.3)
No. Resection Area
Followup
No No No No No No
5 Yrs. Not available 6–60 Mos. Not available 44.6 Mos.
(60)
2
14 Mos.
6 (33.3) 6 (37.5)
1 4
23.5 Mos. 3–5 Yrs.
No 2 No No No
20 Mos. Not available 18.6 Mos. 17 Mos. Not available
3
11 (27.3) 2 (40) 1 (16.6) No No 2 (16.6) (24)
No 27 Mos. 9 (5 superficial, 4 invasive)
TABLE 3. Characteristics of invasive bladder tumor recurrence Transitional Cell Ca
No. Recurrences
References
Site
Hetherington et al47
2
Renal pelvis
Sawa et al43
1
Renal pelvis
Abercrombie et al48 Arango et al51* Jones and Moisey52*
1 1 1
Renal pelvis Renal pelvis, calix Renal pelvis, ureter, resected area Renal pelvis
Fernandez Gomez et al53* * Case report.
1
TABLE 4. Complications of endoscopic ureteral removal in all cases and series No. Procedures
References Pluck procedures: Polo Peris et al45 Kural et al49 Hetherington et al47 Sawa et al43 Palou et al41
16 12 5 5 31
Gill et al29 Keeley and Tolley28 Shental et al44
8 19 13
Totals Stripping procedure: Coulange et al40 Jacobsen et al46
109 25 18
Angulo et al36 Valdivia Uria et al35 Clayman et al33 Zubac and Kihl32 Roth et al39
21 9 18 8 8
Totals * Open conversion in 7 cases.
107
No. Complications 1 Extravasation 0 0 0 1 Extravasation due to intraperitoneal perforation 1 Extravasation 0 0 3 3 Ureteral breakage* 2 Stuck in urethra,* 1 urethral stricture 2 Retained ureters* 2 Ureteral breakage* 0 0 1 Dislodged catheter 11
DISCUSSION
To evaluate the results of a nonstandard technique in terms of efficacy, complications and costs it must be compared with a standard technique in prospective and randomized studies. Although the endoscopic approach to the distal ureter is not new in the literature, none of these techniques
Pathology Grade 3 stage pT4, grade 1, stage pT1 Grade 3
Bladder Recurrence Site
Time
Resected area
4, 9 Mos. 6 Mos.
Stage 3 Grade 2 stage pT1 Poorly differentiated
Ipsilat. squamous bladder tumor Ureteral scar Resected area Resected area
4 Yrs. 7 Mos. 3 Mos.
High grade, stage
Resected ureter
6 Mos.
has been widely used and their results have been questioned in oncological terms. In this case difficulty arises due to the retrospective design of the series as well as to the impossibility of randomization, the rarity of upper urinary transitional cell carcinoma and the selective indication for endoscopic treatment of the distal ureter, making the task extremely long and almost impossible. There are certain main questions to be answered. Do endoscopic techniques cause a major risk of bladder or pelvic recurrence? Is the rate of invasive bladder recurrence greater than when the distal ureter is approached in open fashion? Does endoscopic excision of the distal ureter result in more or fewer complications than the standard technique? After nephroureterectomy for upper urinary transitional cell carcinoma bladder recurrence is not uncommon. The rate of bladder recurrence after classic nephroureterectomy is between 23% and 30%.2–5, 16, 20, 54 Bladder recurrence is more common when there is a history of bladder cancer and recurrence is directly related to the grade of primary upper urinary transitional cell carcinoma.3, 24 In up to 80% of cases bladder recurrence appears during the initial 2 or 3 years after treatment of primary upper urinary transitional cell carcinoma.2, 4, 5, 55 Bladder tumors are of a similar grade in 89% of cases and the same stage in 72%.2 Few studies of open nephroureterectomy clearly indicate the site of bladder recurrence, which appears to be more common in the ipsilateral hemibladder adjacent to the ipsilateral ureteral orifice.56 In a morphological study of urinary tract distribution of lesions in primary upper urinary transitional cell carcinoma Kakizoe et al observed that 80% of cases of concurrent or subsequent bladder cancer had multiple lesions on the same side as primary upper urinary transitional cell carcinoma.55
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ENDOSCOPIC APPROACH TO DISTAL URETER FOR UPPER URINARY TRACT TUMOR
Although a description of bladder recurrence site is rare, even more scarce are reports of the pattern of this recurrence. The majority of reported series focus on parameters such a prognosis and survival. The rate of invasive bladder recurrence after open nephroureterectomy is 2% to 3%.2, 3, 16 To our knowledge only 1 series indicates an extremely high 25% rate of invasive concurrent or subsequent bladder tumors but patient characteristics in this series hardly reflect the natural presentation of upper urinary transitional cell carcinoma.55 No difference was noted in terms of bladder recurrence in classic open series and those of the endoscopic approach to the distal ureter. Invasive ipsilateral bladder trigonal or pelvic recurrence after endoscopic removal of the distal ureter is dramatic. In these cases perioperative seeding has been suggested and, thus, this condition has become the main contraindication to these techniques. To date 7 invasive bladder recurrences have been described, including some isolated case reports without information extending for the duration of the study, if at all.51–53 All recurrences were noted after the pluck procedure. Nevertheless, in the context of the total number of patients treated in the series only 4 invasive recurrences were described. This value corresponds to 3.1% of patients who undergo the pluck procedure and it is similar to the rate of invasive bladder recurrence after classic excision. All except 1 invasive recurrence appeared early during followup and within year 1 after treatment of primary upper urinary transitional cell carcinoma. Analysis of these invasive recurrences shows that only 4 can be directly attributed to tumor spillage.47, 51, 53 In 1 case there was a poorly differentiated tumor in the ureteral resected area and, thus, the bladder invasive tumor diagnosed 3 months later can be better considered persistence rather than recurrence.52 Moreover, tumor in the area to be resected represents a formal contraindication to any endoscopic approach. In another case bladder tumor pathology was quite different from primary tumor pathology since the latter was high grade carcinoma. Furthermore, ureteral resection was performed at the end of the surgical procedure after early ureteral ligation to prevent spillage.43 Thus, although seeding cannot be completely ruled out, the evolution is more suggestive of panurothelial disease rather than tumor spillage. Although the invasive recurrence reported by Abercrombie et al was located over the resection scar, it appeared 4 years after resection, making it unlikely that it was due to tumor seeding during primary endoscopic treatment.48 Differences in the development of subsequent invasive bladder cancer in the 2 techniques can be attributable to the technique or to differences in the pathological pattern of the primary tumor. Due to the lack of complete information in the series proper multifactorial analysis was not be performed. The possibility of tumor spillage cannot be excluded during the pluck technique, especially since no cases of recurrent invasive bladder cancer have been described after the stripping procedure. The difference in the rate of subsequent invasive bladder tumor in the stripping and pluck techniques may be due to a different pathological pattern of primary upper urinary transitional cell carcinoma. Interestingly in recent and extensive series of the pluck technique no invasive bladder or pelvic recurrence has been described,41, 44 although in some more than half of the patients presented with high grade and stage primary upper urinary transitional cell carcinoma.41 The importance of extensive and careful coagulation of the ureter lumen cannot be overemphasized. It would be interesting to identify comparative series in which the incidence of complications was compared. To our knowledge only 2 series have compared traditional nephroureterectomy with the endoscopic ureteral approach.32, 36 In the series of Angulo et al 19 and 15 patients underwent
1-incision, endoscopically assisted nephroureterectomy and the 2-incision standard technique, respectively.36 Mean operative time and mean hospital stay showed statistically significant differences in favor of endoscopically assisted nephroureterectomy. Mean estimated blood loss was less for the endoscopic approach, although no significant difference was noted when compared with the classic 2-incision procedure (240 and 392 cc, respectively). Postoperatively complications were equal in the 2 groups. Zubac and Kihl confirmed the benefits of endoscopic removal of the distal ureter in terms of mean hospital stay and survival.32 The need for less analgesia has been advocated but to our knowledge it has not been properly documented. The pluck technique and its modifications at the level of bladder resection has been shown to be feasible and easy to perform with a low rate of complications. Extravasation and pelvic abscess are also possible after open excision of the bladder cuff. Although the possibility of bladder bleeding was not described in the largest series, it must be considered, as for any bladder tumor resection.57 From the technical point of view the stripping procedure and its variations may require more learning time than endoscopic resection. The technical inconveniences of stripping accounts for approximately 10% of conversions to open surgery, which remains the gold standard and primary technique of choice for most surgeons. A discussion of the benefits or inconveniences of the endoscopic distal ureteral approach would be of little interest if we ignored the trend toward minimally invasive surgery in oncology. In the last 5 years laparoscopic nephroureterectomy for upper urinary transitional cell carcinoma has emerged as a valid alternative to open surgery even in elderly patients.58, 59 To date only 4 series have described laparoscopic nephroureterectomy for upper urinary transitional cell carcinoma,28, 60 – 62 of which 1 includes a previous report from the same group.26, 62, 63 Three techniques of bladder cuff excision have been advocated. In 2 of these series open bladder cuff excision was performed.60, 61 In the most recent comparative series most distal ureters were approached by transurethral unroofing and electrocoagulation or resection to the ureterovesical junction but without penetration of the bladder wall.62 Laparoscopic tenting and ureteral stapling were then performed, following the previously described technique of high grade upper urinary transitional cell carcinoma.32 At 24 months of followup the rate of bladder recurrence was 23%, equal to the rate of the open procedure in the same series. Importantly there was a lower rate of major complications in the laparoscopic group (8% versus 29%), emphasizing the future potential impact of laparoscopic nephroureterectomy.62 As early as 1993, the pluck technique was mentioned by Rassweiler et al as a natural complement to laparoscopic nephroureterectomy.27 They based the choice on the excellent results achieved when they applied the technique in open surgery. This preliminary report was followed by the series of Keeley and Tolley of 19 cases of laparoscopic nephroureterectomy complemented by resection of the distal ureter until detachment with no bladder recurrence.28 They limited this technique to patients with pyelic or caliceal tumors and used other methods when a ureter tumor was present. No complications or open conversions were attributable to the pluck technique. This series compares the open and laparoscopic approaches. The rate of postoperative complications was similar for laparoscopic and open surgery (27% and 35%, respectively). When other factors are compared, the rate appears more favorable in the laparoscopic group since the rate of pulmonary complications was lower (4.5% versus 19%), hospital stay was shorter (5.5 versus 10.8 days) and the transfusion requirement was less (0.3 versus 0.9 units). Using the pluck technique Keeley and Tolley
ENDOSCOPIC APPROACH TO DISTAL URETER FOR UPPER URINARY TRACT TUMOR
achieved an operative time that was equal to that of open surgery. More recently Gill et al presented 8 cases of laparoscopy using a modification of the pluck procedure with early transbladder ligation of the ureteral distal tip, and circumcision of the intramural and perivesical ureter until detachment.29 Although procedure time was longer than that of the original technique, there may be a hypothetical advantage to early ureteral ligation. CASE SELECTION
Case selection is probably the most important factor when deciding to use the endoscope to remove the ureter during nephroureterectomy. Because of the major disadvantage of possible tumor cell seeding, surgical boundaries must be far from the tumor. Therefore, a known ureteral tumor seems to be a formal contraindication to the endoscopic technique. Technically the pluck technique can be used even when a proximal ureter tumor is present as long as some safeguards are met, namely early sealing of the ureteral ostium or ureteral ligation. This maneuver may at least theoretically prevent the flow of urine in the pelvic field. Nevertheless, this technique must be used with care when a ureteral tumor is suspected. For some groups that advocate ureteral stripping a synchronous bladder tumor is a contraindication to the pluck technique due to the danger of perivesical tumor implantation. In reports of directly attributable tumor spillage no bladder tumor resection was performed at the time of the pluck procedure. To our knowledge the question remains unresolved. In addition, preoperative assessment of any cause causing periureteral fibrosis must be considered. Since pelvic ureteral detachment is performed in blind fashion in all endoscopic techniques, an anchored distal ureter would hinder ureteral removal, leaving the possibility of ureteral breakage and urothelial remnants remaining in place. Consequently previous surgery or irradiation of the pelvic field, distal aortic or iliac aneurysm and inflammatory pelvic diseases as well as retroperitoneal fibrosis represent a formal contraindication to these techniques. We can state that the case for these methods involves low grade and stage upper urinary transitional cell carcinoma at a pyelic and/or caliceal site and as part of laparoscopic nephroureterectomy, making this procedure entirely endoscopic and minimally invasive. The case against these techniques involves high disease grade and stage, and/or a ureteral tumor or multiplicity and suspected pelvic fibrosis/adhesions. CONCLUSIONS
Although endoscopic removal of the distal ureter is not yet widely done, most techniques have already proved their feasibility. Whether invasive bladder or pelvic recurrence should be attributed to spillage during performance of the technique remains unanswered but concerns about a higher rate of invasive bladder cancer have not been confirmed in larger current series. The pluck technique has a lower complication rate than the stripping technique but after the latter no invasive bladder recurrence has been described. When deciding on the endoscopic distal ureteral approach, careful patient selection is necessary. When a distal ureteral tumor is suspected during surgery, the procedure should be converted to open excision. The pluck technique or a modification with early ureteral sealing, and circumcision of the intramural and perivesical ureter until detachment may be the ideal supplement to laparoscopic nephroureterectomy. REFERENCES
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