Lasers in Medical Science

, Volume 29, Issue 2, pp 621–627

Two-micron thulium laser resection of the distal ureter and bladder cuff during nephroureterectomy for upper urinary tract urothelial carcinoma

Authors

  • Kun Pang
    • Department of UrologyXuzhou Central Hospital
    • Department of Urology, School of medicineShanghai First People’s Hospital affiliated to Shanghai Jiaotong University
  • Shi-bo Liu
    • Department of UrologyLiaoning Province Tumor Hospital
  • Hai-bin Wei
    • Department of Urology, School of medicineShanghai First People’s Hospital affiliated to Shanghai Jiaotong University
  • Jian Zhuo
    • Department of Urology, School of medicineShanghai First People’s Hospital affiliated to Shanghai Jiaotong University
  • Mei-li Li
    • Department of Ophthalmology, School of medicineShanghai First People’s Hospital affiliated to Shanghai Jiaotong University
  • Shu-jie Xia
    • Department of Urology, School of medicineShanghai First People’s Hospital affiliated to Shanghai Jiaotong University
    • Department of Urology, School of medicineShanghai First People’s Hospital affiliated to Shanghai Jiaotong University
Original Article

DOI: 10.1007/s10103-013-1365-7

Cite this article as:
Pang, K., Liu, S., Wei, H. et al. Lasers Med Sci (2014) 29: 621. doi:10.1007/s10103-013-1365-7

Abstract

The thulium laser (Tm-laser) technique has been used in the management of many urologic conditions. The present study aimed to evaluate the use of this technique for distal ureter and bladder cuff (DUBC) excision during nephroureterectomy for upper urinary tract urothelial carcinoma (UUT-UC). Fifty-eight patients with UUT-UC who underwent radical nephroureterectomy were included in this retrospective study. DUBC was managed by open excision in 24 cases, by transurethral electrosurgery in 17 cases, and by transurethral Tm-laser in 17 cases. Perioperative measures and oncologic outcomes were compared among the three groups. Furthermore, 11 human ureteral segments were collected to measure the burst pressure and show physical pressure tolerance, and six ureteral segments were assessed histologically to investigate the sealing effect. Operative time and hospital stay were significantly longer, and intraoperative blood loss was significantly greater in the open excision group than in the electrosurgery and Tm-laser groups (P < 0.05 for all). There were no significant differences in these parameters between the electrosurgery and Tm-laser groups. In addition, there were no significant differences in the incidences of bladder tumors and retroperitoneal recurrence of urothelial carcinoma among the three groups. The coagulation time and resection time were significantly shorter in the Tm-laser group than in the electrosurgery group. The mean burst pressure did not differ significantly between the tissues sealed by electrosurgery and by Tm-laser. Histopathological analyses showed that distal ureters were completely sealed by both electrosurgery and Tm-laser. The Tm-laser technique is superior to open excision and comparable to transurethral electrosurgery in the management of DUBC during nephroureterectomy for UUT-UC, offering an alternative treatment option for this condition.

Keywords

Upper urinary tract urothelial carcinomaThulium laserDistal ureter and bladder cuff resectionSealing effectBurst pressure

Introduction

Upper urinary tract urothelial carcinoma (UUT-UC) is a relatively rare disease, accounting for 5–7 % of all urothelial malignancies [13]. It has a high propensity for local recurrence and the development of secondary bladder cancer. Nephroureterectomy with distal ureter and bladder cuff (DUBC) excision is the standard surgical treatment for UUT-UC [4, 5]. Adequate DUBC excision, which can be achieved by open excision, is essential for good survival outcomes and low chances of local recurrence or the development of secondary bladder cancer [46]. However, conventional open DUBC excision is associated with significant injuries and long-term recovery. Thus, it is of great clinical importance to develop new, minimally invasive techniques that offer an alternative to open DUBC excision.

Ablative therapies, such as electrocoagulation and laser ablation, have been investigated as minimally invasive alternatives to open excision over the past several decades [7]. Among many laser ablative techniques, thulium laser (Tm-laser) ablation was first introduced into clinical use in 2004 and has many advantages over other techniques. The central wavelength of the Tm-laser can vary between 1.75 and 2.22 mm, matching the 1.92-mm water absorption peak in tissue [8, 9]. Compared to Diode-laser and Nd:YAG laser, the Tm-laser is associated with a higher absorption of radiation by tissue and therefore more efficient and rapid tissue ablation [10], causes a smaller zone of thermally damaged tissue (as small as approximately 50 μm) [11], and provides smoother cutting, more efficient incision, less deep-tissue coagulation, and minimal blood loss due to the continuous wave mode, rapid absorption in water, short penetration depth (∼200 nm), and hemostatic properties [12]. In recent years, the Tm-laser technique has been used for the management of many urologic conditions, including benign prostatic hyperplasia [13, 14], bladder tumors [11], stones [15, 16], urethral or ureteral strictures [17], and even partial nephrectomy [18, 19]. However, there have been no reports on the Tm-laser technique for DUBC resection during nephroureterectomy for UUT-UC.

The Tm-laser technique has been used for treatment of UUT-UC at Shanghai First People’s Hospital since 2005. The aim of the present retrospective study was to evaluate the feasibility of the Tm-laser technique in the management of DUBC during nephroureterectomy for UUT-UC by comparing with open excision and electrosurgery.

Methods

Patients

This study was approved by the Institutional Review Board and Ethics Committee of Shanghai First People’s Hospital (Shanghai, China). From January 2005 to January 2011, 74 patients were diagnosed with UUT-UC and underwent radical nephroureterectomy at Shanghai First People’s Hospital. Among them, 16 were excluded from this study because of previous or concomitant urinary bladder tumors (nine cases), lymph node, or distant metastasis at diagnosis (three cases), or incomplete data (four cases). The remaining 58 patients were included in the study. None of these patients received preoperative chemotherapy or radiotherapy. Among the 58 patients, 24 underwent open surgery for DUBC resection, 17 underwent transurethral DUBC resection by electrosurgery, and 17 underwent transurethral resection by Tm-laser. There were no significant differences in age, gender, smoking status, history of gross hematuria, tumor side, location, stage, or grade among the three groups (Table 1). Nephroureterectomy was performed openly, and the method for managing DUBC was decided by surgeons. All operations were performed by the same team consisting of well-experienced urologic surgeons.
Table 1

Patient and tumor characteristics

 

Total n (%)

Open n (%)

Electrosurgery n (%)

TmL n (%)

P values

Patient number

58 (100)

24 (41.4)

17 (29.3)

17 (29.3)

 

Age (years)

0.8289

  ≤65

23 (39.7)

9 (15.5)

7 (12.1)

7 (12.1)

  >65

35 (60.3)

15 (25.9)

10 (17.2)

10 (17.2)

Sex

0.7694

  Male

33 (56.9)

15 (25.9)

9 (15.5)

10 (17.2)

  Female

25 (43.1)

9 (15.5)

8 (13.6)

7 (12.1)

Smoke

0.9546

  Yes

11 (19.0)

5 (8.6)

3 (5.2)

3 (5.2)

  No

47 (81.0)

19 (32.8)

14 (24.1)

14 (24.1)

Gross hematuria

0.9140

  Yes

46 (79.3)

19 (32.8)

13 (22.4)

14 (24.1)

  No

12 (20.7)

5 (8.6)

4 (6.9)

3 (5.2)

Tumor side

0.5730

  Left

33 (56.9)

14 (24.1)

8 (13.6)

11 (19.0)

  Right

25 (43.1)

10 (17.2)

9 (15.5)

6 (10.3)

Tumor location

0.1221

  Renal pelvis or calyx

26 (44.8)

5 (8.6)

11 (19.0)

10 (17.2)

  Upper ureter

11 (19.0)

5 (8.6)

2 (3.4)

4 (6.9)

  Middle ureter

3 (5.2)

2 (3.4)

1 (1.7)

0 (0.0)

  Lower ureter

14 (24.1)

10 (17.2)

2 (3.4)

2 (3.4)

  Multiple

4 (6.9)

2 (3.4)

1 (1.7)

1 (1.7)

Pathologic stage

0.7279

  Ta/Tis/T1

29 (50.0)

11 (19.0)

7 (12.1)

11 (19.0)

  T2

9 (15.5)

5 (8.6)

2 (3.4)

2 (3.4)

  T3

16 (27.6)

7 (12.1)

6 (10.3)

3 (5.2)

  T4

4 (6.9)

1 (1.7)

2 (3.4)

1 (1.7)

Tumor grade

0.8402

  Low

24 (41.4)

9 (15.5)

7 (12.1)

8 (13.6)

  High

34 (58.6)

15 (25.9)

10 (17.2)

9 (15.5)

Electrosurgery procedure

Electrosurgery began with the placement of a 26 F continuous flow resectoscope and introduction of an electrosurgical loop into the bladder. The ureteral orifice was identified and sealed by coagulation completely. A circular diathermal incision, 1.0 to 1.6 cm in diameter, was made around the ureteral meatus. The ureteral orifice was circumferentially incised through the full thickness of the bladder to detach the DUBC from the bladder. Meticulous coagulation of the excised area was then carried out. Subsequently, a Foley catheter was placed and conventional nephrectomy [14] was performed via a lumbar incision. The ureteral and periureteral tissues were dissected visually.

Tm-laser equipment and procedure

All the patients were placed in the lithotomy position, and epidural anesthesia was achieved. A Tm-laser system (Lisa Laser products OHG, Katlenburg-Lindau, Germany) with an average power of 70 W and the highest power of 110 W operated in continuous-wave mode was used for this procedure. The wavelength of Tm-laser used in this experiment was 2.01 μm. The energy was delivered via 550-μm end-firing PercuFib fibers (Lisa Laser products, Katlenburg, Germany). The laser fiber can be handled in a non-contact manner mainly to coagulate the tissue or in a contact manner mainly to resect the tissue. Our procedure consists of both the sealing and the incision for removing the tissue and the sealing. The laser fibers were introduced via a Karl Storz 26 F continuous flow resectoscope. The speed of fiber movement depended on surgical needs. For example, the fiber was not moved for coagulating the tissue to achieve a higher temperature. Saline irrigation was used in all cases. The laser power was set at 70 W. The laser fiber tip was kept 1–2 mm away from the ipsilateral ureter orifice (Fig. 1a) to seal the ureter orifice carefully to prevent cellular implantation. The seal time was about 2 s (Fig. 1b). A circular incision, 1.0 to 1.6 cm in diameter, was made around the ureteral meatus. The tissue vaporized during the resection (Fig. 1c). The ipsilateral ureteral orifice was circumferentially incised through the full thickness of the bladder (Fig. 1d). The incision time was about 30 s. The DUBC was then pushed out and detached from the bladder. Conventional nephrectomy and dissection of the ureteral and periureteral tissues were then conducted as described above.
https://static-content.springer.com/image/art%3A10.1007%2Fs10103-013-1365-7/MediaObjects/10103_2013_1365_Fig1_HTML.gif
Fig. 1

The Tm-laser procedure. a Placement of the laser fiber near the ureteral orifice. b Sealing the ureter orifice by Tm-laser before resection. c Tissue coagulation and vaporization during Tm-laser resection. d Continuous cutting to expose perivesical fat and detachment of DUBC from the bladder

Tumor staging and follow-up

Clinicopathological data were collected retrospectively for each patient by reviewing available medical records. Pathologic staging of tumors was performed based on the 2002 TNM staging system, and tumors were graded according to the 1998 World Health Organization classification [20].

All patients were followed for at least 1 year postoperatively. Postoperative follow-up consisted of physical examination, urinalysis, chest X-ray, abdominal ultrasound, computed tomography urography, and cystoscopy. Cystoscopy was performed every 3 months for the first 2 years, every 6 months for the next 2 years, and annually thereafter.

Perioperative measures and oncologic outcomes

Perioperative measures included operative time, energy for coagulation, coagulation time, energy for resection, resection time, postoperative hospital stay, intraoperative blood loss, duration of drainage, and duration of catheterization. Oncologic outcomes included the occurrence of subsequent bladder tumors and retroperitoneal recurrence of urothelial carcinoma.

Burst pressure measurement

Eleven nephroureterectomy specimens were obtained to test the sealing effect, including five from patients treated by Tm-laser and six from those treated by electrosurgery. When the specimens were harvested, the ureter was cut 5 cm distally and the stump was connected to a three-way pipe (Fig. 2a). The other two ends of the pipe were connected to a piezometer, a device that could show the real-time pressure inside the specimen through the three-way pipe, and a 50-ml syringe, respectively. The tissue was continuously flooded with saline containing methylene blue using the syringe via the pipe. The burst pressure was recorded at the point of visible leakage of saline through the ablated dome.
https://static-content.springer.com/image/art%3A10.1007%2Fs10103-013-1365-7/MediaObjects/10103_2013_1365_Fig2_HTML.gif
Fig. 2

Burst pressure measurement and histological analyses. a Photograph of the three-way pipe. b Comparison of the mean burst pressure between the Tm-laser and electrosurgery groups (P > 0.05). c, d Histological analyses of tissues treated by c electrocoagulation and d Tm-laser (H&E, magnification ×40). Arrows show the coagulated necrotic areas. The areas affected by Tm-laser and electrocoagulation were boxed

Histology

Histological analyses were carried out under a light microscope (Nikon, Tokyo, Japan) to observe structural changes (×40). Six ablated ureteral segments sealed by electrocoagulation or Tm-laser were taken and assessed histologically by a dedicated pathologist to examine the sealing effect. The samples were taken 5 cm away from the ureter orifice. Before histological examination, the samples were fixed in 4 % neutral-buffered formalin for 12 h, embedded in paraffin, cut into 5-μm-thick serial sections in the transverse plane, and stained with hematoxylin and eosin (H&E).

Statistical analysis

Statistical analyses were performed using SAS v8.02 software (SAS Institute Inc., Cary, NC, USA). Numerical data are expressed as mean ± standard deviation, and categorical data are presented as a percentage. Comparisons of numerical data among the three groups were performed using the Student–Newman–Keuls test. The burst pressure between two groups was compared using the t test. The incidence of bladder cancer was compared using the Fisher's exact test. Categorical data were compared using the chi-square test. A P < 0.05 was considered statistically significant.

Results

Operative time and postoperative hospital stay were significantly longer, and intraoperative blood loss was significantly greater in the open excision group than in both the electrosurgery and Tm-laser groups (P < 0.05; Table 2). However, these parameters showed no significant differences between the electrosurgery group and the Tm-laser group (P > 0.05). In addition, although the durations of drainage and catheterization showed no significant differences between the three groups (P > 0.05), the coagulation time and resection time were significantly shorter in the Tm-laser group than in the electrosurgery group (P < 0.05).
Table 2

Perioperative and outcome measures between the three groups

 

Open excision

Electrosurgery

Tm-laser

Operative time, min*

233.0 ± 51.4

148.1 ± 47.2

126.5 ± 48.8

Energy for coagulation, J

153.53 ± 10.64

153.18 ± 6.42

Coagulation time, s**

3.07 ± 0.21

2.19 ± 0.13

Energy for resection, J

1744.4 ± 152.0

1704.7 ± 122.9

Resection time, s**

34.89 ± 3.04

24.34 ± 1.76

Intraoperative blood loss, mL*

352.0 ± 85.2

136.5 ± 74.4

141.0 ± 69.5

Duration of drainage, days

6.5 ± 3.1

7.1 ± 2.9

7.5 ± 3.5

Durations of catheterization, days

8.7 ± 3.3

8.2 ± 3.2

8.2 ± 3.8

Postoperative hospital stay, days*

12.7 ± 3.4

9.8 ± 2.7

9.9 ± 3.1

*P < 0.05 between the open excision group and the two ablation therapy groups; **P < 0.05 between the electrosurgery and Tm-laser groups

Of the 58 patients enrolled in this study, 11 developed subsequent bladder tumors and one developed retroperitoneal occurrence of urothelial carcinoma. Bladder tumors occurred in five, four, and two patients in the open surgery group, electrocoagulation, and Tm-laser group, respectively, and there were no significant differences in the incidence of bladder tumors among the three groups (P = 0.060). Retroperitoneal recurrence of urothelial carcinoma occurred only in the open surgery group. The incidence of retroperitoneal recurrence of urothelial carcinoma was not compared among the three groups due to low statistical power.

The mean burst pressure showed no significant difference between the electrosurgery group and the Tm-laser group (139.32 ± 31.47 cmH2O vs. 115.85 ± 20.92 cmH2O, P > 0.05; Fig. 2b). Histopathological analyses of the terminal ureteral segments showed that the distal ureters were completely sealed by both electrocoagulation and Tm-laser (Fig. 2c and d).

Discussion

Standard radical nephroureterectomy involves two distinct procedures, nephroureterectomy and DUBC excision [21]. Nephroureterectomy can be achieved either by an open or a laparoscopic approach [22, 23], and cancer-related outcomes seem similar between both modalities [15, 22, 23]. However, there is still controversy over the optimal technique for DUBC excision, and the method for managing DUBC has not been standardized yet. In the present study, the feasibility of the Tm-laser technique was evaluated versus open excision and electrosurgery in the management of DUBC during nephroureterectomy for UUT-UC. It was found that open excision was associated with longer operative time and postoperative hospital stay and more intraoperative blood loss than electrosurgery and the Tm-laser technique. Furthermore, although the latter two techniques were comparable in terms of most perioperative parameters, oncologic outcomes, and sealing effect, Tm-laser was associated with shorter coagulation time and resection time than electrosurgery.

There are currently at least five different approaches for the management of DUBC, and each has its inherent advantages and disadvantages [5, 24]. The open excision technique ensures adequate exposure and complete excision, but it is associated with longer hospital stay and operative time compared with endoscopic approaches [7]. In agreement, it was found that the operative time and postoperative hospital stay were significantly longer and intraoperative blood loss was significantly more in the open excision group than in the two transurethral resection groups. The reason might be that transurethral surgeries do not require an extra-incision, which shortens the operative time and reduces injury to patients.

Due to the risk of tumor seeding as a result of fluid extravasation with potential tumor cell exfoliation, all the ‘pluck’ technique approaches are associated with a common problem, oncological safety [5, 7, 25]. Many studies have shown that local recurrence results from fluid extravasation-related tumor seeding [26, 27]. A retrospective study performed by Li et al. [7] showed that the recurrence rate of retroperitoneal urothelial tumors was 7 %. However, they found that there was no significant difference between open surgery and by electrosurgery with respect to local recurrence, suggesting that the ‘pluck’ technique can achieve the same effect as open excision in terms of local tumor control and long-term outcome [24]. This is consistent with the finding of this study that there were no significant differences in the incidences of bladder tumors among the three groups. The occurrence of bladder tumors may arise from microscopic tumor seeding or chronic carcinogen stimulation [7].

Local recurrence after bladder cuff resection may be associated with urinary spillage resulting from a surgical procedure. In this series, the patients underwent rigid cystoscopy with aggressive resection of DUBC into the perivesical fat. Once the proximal specimen was mobilized, the previous transurethral resection eased the subsequent DUBC excision. The ureteric lumen was completely coagulated to prevent urinary spillage [24].

Transurethral electrosurgery has been demonstrated to be a simple and efficient method for the management of DUBC during nephroureterectomy [5, 25]. In this study, perioperative and oncologic outcomes showed no significant differences between the Tm-laser and electrosurgery groups. Histological analysis showed that distal ureters were sealed completely both by electrocoagulation and Tm-laser. In addition, Tm-laser could generate the same seal structure as electrocoagulation via a high-temperature thermal injury. Besides, the physical pressure tolerance was similar between the tissues treated by Tm-laser and electrocoagulation. These findings suggest that the Tm-laser technique is comparable to electrosurgery in the management of DUBC during nephroureterectomy for UUT-UC.

Endoscopic management of upper urinary tract tumors has gained wide acceptance, and the use of lasers has provided urologists with an excellent tool for endoscopic treatment [28]. Many types of lasers, such as carbon dioxide and holmium-yttrium aluminum garnet (YAG), have been used in urology [29]. Holmium-YAG and/or neodymium-YAG laser ablation has been used as the primary treatment for UUT-UC and demonstrates satisfactory performance in patients with relatively small tumors (<4 cm) [30]. Tm-laser is a new type of laser for surgery that holds many advantages over traditional lasers, such as improved vaporization ability, less damage, more smooth tissue incision, and more versatility [11]. These advantages enable Tm-laser to accurately remove lesions [29]. Consistent with these findings, it was found that the Tm-laser technique was associated with shorter operative time and postoperative hospital stay and less intraoperative blood loss in this study. The results demonstrate that the Tm-laser technique is a feasible option for the management of DUBC.

In conclusion, it was demonstrate that the Tm-laser technique is superior to open excision and comparable to transurethral electrosurgery in terms of perioperative parameters, oncologic outcomes, and sealing effect in the management of DUBC during nephroureterectomy for UUT-UC, offering an alternative treatment option.

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