A Modified and Practical Surgical Technique for Pure Transperitoneal Laparoscopic Radical Nephroureterectomy in a Single Position and Research Outcomes

Abstract

Purpose:

To explore the surgical techniques and clinical value of pure transperitoneal laparoscopic nephroureterectomy (LNU) plus bladder cuff excision (BCE) conducted without changing the patient's position in the treatment of upper tract urothelial carcinoma (UTUC).

Methods:

From August 2018 to July 2021, we retrospectively reviewed 66 patients who underwent LNU + BCE in a single position. Then, their demographic characteristics, perioperative and pathological outcomes, and postoperative follow-up data were evaluated.

Results:

All 66 operations in this group were successfully completed without conversion to open surgery. The mean operative time was 125 ± 47 minutes, whereas the estimated blood loss was 10 (10, 15) mL. The median postoperative drainage time was 4 (3.8, 6.0) days, the time to catheter extraction after the operation was 4.5 (3.0, 6.0) days, and the median postoperative hospital stay was 6 (5, 7) days. Pathological results showed urothelial carcinoma in 65 cases, including 56 high-grade and 9 low-grade cases. Lymph node metastasis was found in 8 cases of high-grade urothelial carcinoma. All the surgical margins were negative. The median follow-up was 16.5 (11.0–25.6) months, and there was neither tumor recurrence nor distant metastasis.

Conclusions:

Pure transperitoneal LNU + BCE in a single position is a safe and effective minimally invasive technique for UTUC and is worthy of clinical application and promotion. It takes advantage of a programmed procedure, short operation time, less blood loss, less trauma, and quick recovery after the operation. However, multicenter randomized controlled studies with large samples are needed to further confirm these findings.

Trial Registration:

The study was registered at Cancer Hospital, Chinese Academy of Medical Sciences (No. 22/054-3255) and the registration date is August 2018.

Introduction

Radical nephroureterectomy (RNU) with bladder cuff excision (BCE) is considered the gold standard for treating patients with high-risk upper tract urothelial carcinoma (UTUC).¹ At present, the most commonly used surgical method is to perform laparoscopic nephrectomy and proximal ureterectomy first. Then, the surgical position is changed, and a lower abdominal oblique incision is made to complete the distal ureteral and bladder cuff (DUBC) excision by open surgery.² Consequently, the operation time is prolonged owing to the change in surgical position, and postoperative pain and incision-related complications are increased due to larger surgical incisions.

Laparoscopic nephroureterectomy (LNU) can be performed through transperitoneal or retroperitoneal approaches. Many surgeons choose the retroperitoneal approach owing to easy access to the renal pedicle and avoidance of bowel mobilization but ignore the potential surgical value of the operation space and identifiable surgical anatomical marks through the transperitoneal approach.³ In recent years, some scholars at home and abroad have explored single-position LNU and BCE through transperitoneal or retroperitoneal approaches, but the operation time is relatively long, and the surgical techniques and tips have not been elaborated in detail.^4,5 Therefore, we creatively developed a new transperitoneal LNU and BCE procedure conducted in a single position and reported our surgical techniques and satisfactory findings in detail to solve the problems mentioned earlier and further improve the clinical application and promotion.

Patients and Methods

Study population

From August 2018 to July 2021, a total of 66 patients who underwent LNU performed in our department by 1 surgeon were enrolled in this study. Among them, there were 31 males and 35 females. The mean age was 66 ± 10 years, the body mass index (BMI) was 24.26 ± 3.25 kg/m², the Charlson comorbidity index was 2 (2, 3), and the American Society of Anesthesiologists score was 2 (2, 3). There were 30 UTUCs on the right and 36 UTUCs on the left. The average tumor size was 3 (2.3, 4.5) cm. There were 41 cases of renal pelvic cancer, 22 cases of ureteral cancer, and 3 cases of kidney and ureter cancer. See Table 1 for details. In addition, perioperative and pathological outcomes and postoperative follow-up data were collected and evaluated.

Table 1.

Patient Demographics

Variables	Value
Age, years ( $\bar{x} \pm s$ )	66 ± 10
Gender (F/M, n)	31/35
BMI, kg/m² ( $\bar{x} \pm s$ )	24.26 ± 3.25
Tumor side (R/L, n)	30/36
Tumor side, cm [median (IQR)]	3.0 (2.3, 4.5)
CCI score [median (IQR)]	2 (2, 3)
ASA score [median (IQR)]	2 (2, 3)
Location of tumor (n)
Renal pelvis	41
Ureter	22
Renal pelvis and ureter	3
Clinical T stage, n (%)
Tx	2
<T2	21
≥T2	43

ASA, American Society of Anesthesiologists; BMI, body mass index; CCI, Charlson comorbidity index; F, female; IQR, interquartile range; L, left; M, male; R, right.

All patients underwent ultrasound, magnetic resonance imaging, urine cytology, and cystoscopy before surgery. All patients and surgical protocols were approved by the Medical Ethics Committee of Cancer Hospital, Chinese Academy of Medical Sciences, and informed consent was obtained from the patients and their families before the operation. All methods were carried out in accordance with relevant guidelines and regulations.

Surgical technique

All 66 patients underwent pure transperitoneal LNU + BCE in a single position. Among them, 2 patients with bladder tumors were treated with transurethral resection of bladder tumor at the lithotomy position, followed by laparoscopic operation for UTUC. Retroperitoneal lymph node dissection (LND) was performed in 17 patients.

Patient positioning and trocar configuration

The patient's position was usually in a 50°–70° flank position on the healthy side. The catheter was indwelling, and chemotherapeutic drugs were injected into the bladder through the catheter for 30 minutes to prevent intravesical recurrence after LNU + BCE. Figure 1 shows the location of the trocar.

FIG. 1.

Patient trocar configuration. (A) For left UTUC, a 5-mm trocar A is located 1 cm below the costal edge of the middle line of the left clavicle; a 10-mm trocar B is located 2 cm on the left side of the umbilicus; a 10-mm trocar C is located at the midpoint between the left anterior superior iliac spine and the umbilicus; a 5-mm trocar D is located at the level of the navel in the anterior axillary line; and a 12-mm trocar E is located at the midpoint of the umbilicus and symphysis pubis. (B) For right UTUC, the 5-mm trocar A is located 1 cm below the costal edge of the middle line of the right clavicle; the 10-mm trocar B is located 2 cm on the right side of the umbilicus; the 10-mm trocar C is located at the midpoint between the right anterior superior iliac spine and the umbilicus; the 5-mm trocar D is located ∼5–8 cm above trocar B; the 12-mm trocar E is located at the midpoint of the umbilicus and symphysis pubis; and the 5-mm trocar F is located ∼2 cm under the xiphoid process. UTUC, upper tract urothelial carcinoma.

Laparoscopic nephroureterectomy

The peritoneum in the paracolic sulcus of the ascending (descending) colon was cut off with an ultrasonic scalpel and dissociated downward to the iliac vessels and pelvic peritoneum. The affected ureter was exposed in front of the psoas major muscle of the lower pole of the kidney and was clamped with Hem-O-Lok at the distal ureter, which is beneficial to prevent the implantation and metastasis of tumors (Fig. 2A). For the left UTUC, the left posterior peritoneum was cut off at the lower edge of the spleen, and the spleen kidney ligament was cut off.

FIG. 2.

The surgical procedure of laparoscopic nephroureterectomy. (A) The affected ureter was exposed in front of the psoas major muscle of the lower pole of the kidney and was clamped with Hem-O-Lok at the distal ureter. (B) Exposed retroperitoneal perirenal fascia and kidney after cutting off the posterior peritoneum and the spleen kidney ligament. (C) Exposed left renal artery and vein. (D) The renal vein was cut off and closed by an Endo-GIA stapler. (E) Exposure of the inferior vena cava and renal vein after dissociating the hepatic flexure and ascending colon and the rear of the duodenum. (F) The right renal artery and vein were clamped with Hem-O-Loks.

Then, the relaxed colon, colonic splenic flexure and partial sigmoid colon were pushed to the healthy side to expose the perirenal fascia and kidney behind the peritoneum (Fig. 2B). The ureters and reproductive vessels were exposed in the middle of the surface of the psoas major at the level of the lower pole of the left kidney. The renal vein was then exposed by proximal dissociation along the left reproductive vessel. Then, the renal artery was clamped with Hem-O-Lok, the renal vein was clamped with two Hem-O-Lok clips at the proximal end and one at the distal end, and the renal artery was treated in the same way (Fig. 2C). The renal vein was also handled with an Endo-GIA stapler (Fig. 2D).

For the right UTUC, the hepatic flexure and ascending colon were separated, the rear portion of the duodenum was freed, and the ascending colon and descending duodenum were pushed to the healthy side. Then, the confluence of the right renal vein and inferior vena cava was exposed by dissociating the anterior wall of the inferior vena cava (Fig. 2E). The treatment of the right renal artery and vein was the same as that on the left (Fig. 2F). The perirenal fat was separated from the Gerota fascia and peritoneum to the upper pole of the kidney, and the affected adrenal gland was preserved. The lower pole of the kidney was freed, followed by complete freeing of the affected kidney and distal ureter.

Bladder cuff excision

The peritoneum beside the iliac vessels was incised downward to the outside of the bladder; the upper ureter was lifted and separated from the surrounding tissue until reaching the opening of the ureter and bladder. The end of the ureter was fully dissociated, followed by exposure and excision of part of the bladder detrusor muscle; the ureter was pulled toward the head, and the terminal ureter and bladder mucosa were further separated into a “trumpet” shape and then dissociated 1–2 cm to the distal end of the bladder to ensure complete sleeve excision (Fig. 3A).

FIG. 3.

The surgical procedure of bladder cuff excision. (A) The “trumpet”-shaped terminal ureter is exposed by dissociating the distal ureter and bladder mucosa. (B) The bladder mucosa and muscle layer were sutured with 3-0 barbed thread. (C) The distal ureteral and bladder cuff excision was performed by an Endo-GIA stapler. (D) Transvaginal natural orifice specimen extraction surgery. (E) The peritoneum of the paracolic sulcus area was sutured. (F) Surgical specimens after the operation.

The whole layer of the normal bladder wall at the ureteral opening was sutured with a 3-0 barbed thread for traction, and then the bladder mucosa and muscle layer were sutured after excision (Fig. 3B). DUBC excision was also performed by an Endo-GIA stapler (Fig. 3C). The resected kidney, ureter, and part of the bladder wall were put into the specimen bag, and in males specimens were taken from the median incision of the inferior abdomen. In females, specimens were removed through the vagina (Fig. 3D). The peritoneum of the paracolic sulcus area was sutured (Fig. 3E). Figure 3F presents the surgical specimens after the operation.

Results

All 66 cases were performed successfully, with no conversion to open surgery and no intraoperative complications. The mean total operation time was 125 ± 47 minutes, the intraoperative bleeding volume was 10 (10, 15) mL, the time to flatus was 1 (1, 1) days, the time to resume eating was 1 (1, 1) days, the time to ambulation was 1 (1, 1) days, the drainage tube extraction time was 4.0 (3.8, 6.0) days, the time to catheter extraction was 4.5 (3.0, 6.0) days, and the length of postoperative hospital stay was 6.0 (5.0, 7.0) days. Pathological results showed urothelial carcinoma in 65 cases; among them, there were 56 cases of high-grade invasive urothelial carcinoma, 20 cases high-grade urothelial carcinoma with vascular tumor thrombus and 9 cases of low-grade urothelial carcinoma.

Beyond that, in 1 case, tumor cells were not found by postoperative pathology, and the grading could not be evaluated because of preoperative chemotherapy combined with immunotherapy. The pathological stages were as follows: 1 case in stage Tx, 5 cases in stage Ta, 1 case in stage Tis, 14 cases in stage T1, 8 cases in stage T2, 36 cases in stage T3, and 1 case in stage T4. Lymph node metastasis was found in 8 cases of high-grade urothelial carcinoma. All the surgical margins were negative. The median follow-up was 16.5 (11.0–25.6) months, and there was neither tumor recurrence nor distant metastasis. Detailed information can be found in Table 2.

Table 2.

Perioperative and Pathological Outcomes

Variables	Value
Operative time, minutes ( $\bar{x} \pm s$ )	125 ± 47
Mean blood loss, mL [median (IQR)]	10 (10, 15)
Time to flatus, days [median (IQR)]	1 (1, 1)
Time to resume eating, days [median (IQR)]	1 (1, 1)
Time to ambulation, days [median (IQR)]	1 (1, 1)
Time to drainage tube extraction, days [median (IQR)]	4 (3.8, 6.0)
Time to catheter extraction, days [median (IQR)]	4.5 (3, 6)
Postoperative hospital stays, days [median (IQR)]	6 (5, 7)
Intra/postoperative complications, n (%)	Not
Pathological stage, n (%)
pTx	1
pTa	5
pTis	1
pT1	14
pT2	8
pT3	36
pT4	1
Tumor grade, n (%)
Low grade	9
High grade	56
Associated vascular tumor thrombus, n (%)	20 (30.3)
Lymph node dissection, n (%)	17 (25.8)
Lymph node metastasis, n (%)	8 (12.1)
Positive surgical margin, n (%)	0
Tumor recurrence, n (%)
Intravesical tumor recurrence	0
Extra-bladder recurrence	0
Follow-up, months [median (IQR)]	16.5 (11.0–25.6)

IQR, interquartile range.

Discussion

LNU and DUBC excision by open surgery are commonly used in clinical practice. Although this operation is much improved compared with the traditional open operation, it still requires the surgeon to change the patient's body position and redisinfect the operation area, which prolongs the time of anesthesia and operation and increases the risk of postoperative infection. In addition, the trauma caused by an open incision in the lower abdomen is also extensive, which partially negates the advantages of minimally invasive surgery.⁶

In recent years, the LNU + BCE procedure in a single position has become a research hotspot due to the potential advantages of not having to change surgical positions. The most important prerequisite for the realization of single-position surgery is the layout and distribution of the trocar. In general, three trocar puncture points were selected in many studies,^7,8 including the subcostal midline of the collarbone, the lateral border of the flat navel rectus muscle, and the midpoint of the symphysis pubis and umbilicus. On this basis, some scholars use another two trocar puncture points,⁹ and some scholars use another one trocar puncture point.¹⁰ In this study, we used five trocar puncture cannulas.

When performing laparoscopic nephrectomy, the operator used cannulas A and C, and the assistant used cannula D to make the surgical field exposure clearer; when performing bladder cuff resection, the operator used cannulas C and E, which made it easier for the operator to dissect, cut, and suture. In addition, in males, the specimens can be removed through the incision of the extended cannula E. In females, transvaginal natural orifice specimen extraction surgery can be performed,¹¹ which is more in line with the concept of minimal invasiveness. In our study, we performed pure transperitoneal LNU + BCE in a single position. There was no need to change the body position during the operation, and the procedure was reasonable and standard, which reduced the operation and anesthesia time, with less trauma, a faster postoperative recovery, and a shorter hospital stay.

There has always been intense debate about whether to perform retroperitoneal or transperitoneal LNU. Liu et al¹² retrospectively analyzed 34 cases of retroperitoneal LNU and 34 cases of transperitoneal LNU. The results indicated that both methods were safe and feasible, and the perioperative and oncological outcomes were similar. Some surgeons consider that compared with the transperitoneal approach, the retroperitoneal approach can enable direct access to the renal artery and kidney.¹³ However, as long as we master the programmed method of finding the renal pedicle, the transperitoneal approach is also very effortless.

Based on our experience, the programmed method of finding the renal pedicle through a transperitoneal approach was summarized. For the left renal pedicle, generally at the lower pole of the left kidney, the reproductive vessels and ureter are exposed in the middle of the surface of the psoas major muscle, and then the renal pedicle can be exposed by dissociating it to the proximal end. For the right renal pedicle, on the one hand, dissociating the anterior wall of the inferior vena cava can expose the confluence of the right renal vein and the inferior vena cava, further exposing the renal pedicle. On the other hand, the ureter was identified in front of the right inferior psoas major muscle and the lateral side of the inferior vena cava and then dissociated upward to expose the renal pedicle.

Some researchers believe¹⁴ that the transperitoneal approach can interfere with bowel mobilization, thus affecting the postoperative first oral intake. However, as long as we restore the normal position of the abdominal organs and close the peritoneum, there is no effect on the recovery of intestinal function. In our study, patients received oral administration on the 1st day after surgery, and none had significant gastrointestinal-related complications.

We believe the transperitoneal approach has many advantages: (1) The readily identifiable surgical anatomical landmarks and wide field of surgical vision are more beneficial to larger tumor resection, bladder suture, and LND. (2) The large operating space for the operator is more in line with ergonomics, which can effectively reduce the operator's fatigue. (3) The approach is more suitable for patients who are obese, have a history of retroperitoneal surgery, and have a tumor involving the perirenal fascia.

The DUBC can be treated with a variety of methods, such as open excision through a lower abdominal Gibson incision or an endoscopic, transvesical, and pure laparoscopic extravesical excision.^15,16 Distal ureter management is an important factor for intravesical recurrence.¹⁷ Xylinas et al¹⁸ retrospectively compared the oncology and prognosis of transvesical (n = 1811), extravesical (n = 785), and endoscopic (n = 85) surgical approaches for UTUC. They found no difference between the three methods in terms of nonbladder recurrence and survival, whereas the endoscopic approach led to higher intravesical recurrence. Gill et al¹⁹ described laparoscopic transvesical treatment for DUBC.

Although the positive surgical margin and tumor recurrence rate are small, the procedure is difficult to perform, especially for patients with a high BMI. Therefore, pure laparoscopic extravesical excision is currently considered to be the most effective surgical method for the treatment of DUBCs. DUBCs can be removed by the Hem-O-Lok clamp, Endo-GIA stapler, or arterial forceps.²⁰ The arterial clamp suture technique is difficult to perform and not easy for beginners to master; Hem-O-Lok poses the risk of urine leakage and bladder wound bleeding secondary to exfoliation.

In our study, we adopted two methods to deal with DUBC. For the “cutting and suturing” method, the bladder mucosa at the end of the ureter is presutured with an inverted thorn before opening the bladder to prevent the mucosa from retracting after being cut open and leaving a loose suture. Then, with “cutting and suturing,” the entire excision process was accurate, and suture was conducted accurately. For the Endo-GIA stapler method, 1 cm of the bladder wall around the ureter was completely removed with an Endo-GIA stapler to prevent urine overflow and incision implantation. Then, the peritoneum was sutured around it with 3-0 barbed thread to prevent the formation of bladder stones.

In our study, none of the 66 included patients had postoperative urinary leakage from urine-containing tumors, which reduced the possibility of tumor planting. It should be noted that when the terminal distal ureter is fully dissociated from thin to thick portions, it is necessary to further dissociate at least 2 cm from the distal end of the bladder to ensure complete sleeve excision. In addition, the bladder wall should be resected at least 1 cm away from the surrounding mucosa of the ureter.

At present, whether to perform retroperitoneal LND is still controversial. LND can determine the stage, but whether it can improve the patients' prognosis is controversial. Studies have shown that template-based LND improves cancer-specific survival (CSS) in patients with muscle-invasive UTUC and reduces the risk of local recurrence.²¹ However, there are also multicenter studies showing that LND has no effect on CSS.²² In our study, 17 patients who were suspected of having muscle-invasive UTUC underwent LND according to preoperative imaging and other comprehensive considerations. According to the 2021 European Association of Urology guidelines, experts recommend LND for muscle-invasive UTUC (≥T2). Therefore, we intend to perform regular LND for patients with locally advanced UTUC in a follow-up clinical study.

Inevitably, there are some limitations in this study. First, there is a lack of comparison with transperitoneal laparoscopic RNU, which will be improved in future studies. Second, this study was a retrospective investigation with a single center and small sample size.

Conclusions

In summary, pure transperitoneal LNU plus BCE in a single position is a safe and effective minimally invasive technique for UTUC and is worthy of clinical application and promotion. It provides the advantages of a simple operation, short operation time, less blood loss, less trauma, and quick recovery after surgery. However, multicenter randomized controlled studies with large samples are needed to further confirm these findings.

Footnotes

Acknowledgments

The authors thank all the 66 patients who agreed to this study and completed the follow-up survey.

Authors' Contributions

Q.Z. contributed to the data collection and management, data analysis, and article writing. L.W. contributed to the data collection and article writing. F.Y. contributed to the interpretation of results. D.C. contributed to data management and analysis. N.X. contributed to the project development and article editing. All authors read and approved the final article.

Ethics Approval and Consent to Participate

The study was approved by Research Ethics Committee of Cancer Hospital, Chinese Academy of Medical Sciences (Project No. 22/054-3255). All the patients in this study provided written informed consent. All information was handled following relevant ethical and legal standards.

Consent for Publication

All participants have given their written informed consent to the publication of their personal or clinical data and details.

Availability of Data and Materials

Data used and/or analyzed in the current research can be obtained from the corresponding author on reasonable request.

Disclosure Statement

The authors declare that they have no competing interests.

Funding Information

This study was financially supported by The Capital Health Research and Development of Special Funding (Grant No. 2022-1-4021), the CAMS Initiative for Innovative Medicine (Grant Nos. 2022-I2M-2-002 and 2021-I2M-1-015), the National Natural Science Foundation of China (Grant No. 81972400), Beijing Hope Run Special Fund of Cancer Foundation of China (Grant No. LC2019B02), and National Key R&D Program of China (Grant No. 2022YFE0200800).

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