Laparoscopic Partial Nephrectomy with Precise Segmental Renal Artery Clamping for Clinical T1b Tumors

Abstract

Objective:

To assess the technique and short-term outcomes of laparoscopic partial nephrectomy (LPN) with precise segmental renal artery clamping for clinical T1b (cT1b) tumors and to analyze the possible factors affecting the glomerular filtration rate (GFR) reduction.

Materials and Methods:

This retrospective study investigated the outcomes of 72 patients with cT1b tumors who received LPN from June 2008 to May 2014. Based on three-dimensional dynamic renal vascular models built before surgery, target arteries were precisely clamped and tumors were removed under regional parenchymal ischemia. Perioperative and follow-up outcomes were analyzed.

Results:

All the LPN procedures were effectively performed using the novel technique, without converting to main renal artery clamping or open surgery. The mean operative time was 86 min, with a mean warm ischemic time of 25 min. The median estimated blood loss was 200 mL (range: 80–800). The postoperative mean GFR was 64% of the preoperative baseline, and the total complication rate was 19.4%. In multivariable analyses, the two independent factors affecting postoperative GFR were the RENAL nephrometry score (RNS) and number of intraoperative clamped segmental arteries. The median follow-up was 24 months (range: 6–72). The overall, recurrence-free, and cancer-specific survival rates were 100%, 95.8%, and 100%, respectively.

Conclusions:

For patients with cT1b tumor, LPN with precise segmental renal artery clamping is safe and feasible for removing tumors and preserving the blood supply and normal renal parenchyma. Short-term oncologic and functional outcomes were satisfactory. Postoperative GFR was related to the preoperative RNS and number of intraoperative clamped segmental arteries.

Introduction

Renal cell carcinoma (RCC) is a common malignancy and ranks among the top genitourinary cancers.^1,2 More than 70% of RCC patients have T1 stage at the time of diagnosis.^3
–5 Surgery is considered the optimal treatment for localized kidney cancer, and nephron-sparing surgery is now recommended for small renal tumors.^6,7 Although laparoscopic partial nephrectomy (LPN) has been widely adopted as a minimally invasive nephron-sparing surgery for T1a tumors,^8
–10 the application of LPN in T1b tumors remains debatable.

Compared with the T1a tumor, the larger size of the T1b requires experienced surgical skills and better technique, to decrease the greater risk of warm ischemic injury. Improvements in LPN have included new hilar control techniques to reduce ischemic/reperfusion injury.^10

–15 For LPN, we previously reported novel techniques of precise segmental renal artery clamping, performed under the guidance of dual-source computed tomography (DSCT).^10,12,15 These techniques can precisely clamp the target arteries, based on replicate three-dimensional (3D) vascular models built preoperatively, and achieve satisfactory regional parenchymal ischemia.¹⁵ The localized ischemia and optimized surgical procedures minimize intraoperative warm ischemic injury and improve early postoperative renal function, compared with main renal artery clamping.^10,12 However, for T1b tumors, there have been no published systematic studies of the outcomes of LPN using these new techniques.

This study assessed the technical feasibility and safety of LPN, with precise segmental renal artery clamping for clinical T1b (cT1b), and the short-term oncologic and functional outcomes.

Materials and Methods

Patients

From June 2008 to May 2014, 72 patients underwent LPN in our department. All these patients received a diagnosis of cT1b renal tumor (4–7 cm in diameter) and had normal contralateral renal function, which was evaluated before operation by using renal scintigraphy with a camera-based method measuring the renal uptake of technetium Tc-99m diethylenetriamine pentaacetic acid (Gate's method¹⁶). Not included in the study were tumors located in the hilum and those that could not be excised safely with LPN, based on the surgeon's judgment.

Surgical procedures

All the LPNs were performed through a retroperitoneal approach and used the precise segmental renal artery clamping technique under the guidance of DSCT that was described in our previous work.^10,12,15 Briefly, all the patients underwent computed tomography (CT) and DSCT before surgery to establish 3D dynamic renal vascular models. Information regarding tumor size, position, growth pattern, RENAL nephrometry score (RNS),¹⁷ and renal arterial segmentation and its anatomic relationship with the tumor was obtained. Thus, the segmental arteries feeding the tumor could be precisely identified preoperatively and the clamping branches chosen. The selected target for precise clamping was the segmental artery feeding the tumor, with no further branches before entering the parenchyma.

Patients were administered general anesthesia and placed in the lateral decubitus position. Four ports in the lumbar region were applied. The targeted segmental renal arteries were isolated at the pulsatile position and clamped with the bulldog before removing the tumor. The parenchyma was incised and the tumor was excised closely around its capsule. Transected vessels in the tumor bed and incised calices were sutured and repaired. Then, the parenchymal defect was closed using hem-o-lok clips to tighten and secure the sutures at each exit point. Finally, the bulldogs were unclamped after the completion of renorrhaphy.

Follow-up

A study of glomerular filtration rate (GFR) was performed to evaluate the split renal function before (baseline) and 3 months after the surgery, using renal scintigraphy with a camera-based method measuring the renal uptake of technetium Tc-99m diethylenetriamine pentaacetic acid (Gate's method¹⁶). A CT scan was performed to determine the recurrence or metastasis of the renal tumor every 6 months for the first 3 years and then annually thereafter.^6,7

Clinical data

Patient demographic data, including age, gender, and body mass index, were collected, and the following clinicopathologic characteristics—tumor size, location, and growth pattern; RNS¹⁷; perioperative data on operative and clamping time, estimated blood loss (EBL), pathology, number of intraoperative clamped segmental arteries (clamped arteries), positive surgical margin; and GFR and complications, were also carefully collected. Complications were classified based on the Clavien grading system.¹⁸ The follow-up outcomes noted were follow-up time and overall, recurrence-free, and cancer-specific survival.

Statistical analyses

All the data collected were analyzed by STATA 12.0 software. Univariable and multivariable linear regression analyses were utilized to investigate associations between tumor characteristics, perioperative outcomes, and postoperative GFR reduction from baseline. Overall, recurrence-free, and cancer-specific survival rates were calculated using the Kaplan–Meier method. p<0.05 was considered statistically significant.

Results

Patient and tumor characteristics

The 72 patients consisted of 48 men and 24 women (Table 1). The median tumor diameter was 5.4 cm (range: 4.1–7.0). Regarding tumor location, approximately half of the tumors were polar (48.6%), followed by posterior (27.8%), striding (striding tumor was defined as the lesion located on both anterior and posterior sides of the kidney) (13.9%), and anterior (9.7%). Tumor pathology was 84.7% clear-cell carcinoma, with chromophobe cell carcinoma and papillary carcinoma making up the balance.

Table 1.

Patient Demographics and Tumor Characteristics

Age, years	53±12.1
Gender, n (%)
Male	48 (66.7)
Female	24 (33.3)
Body mass index	23.6±1.38
Tumor size, cm	5.8±0.87
RNS, median (range)	8 (5–10)
Tumor location, n (%)
Polar	35 (48.6)
Anterior	7 (9.7)
Posterior	20 (27.8)
Striding	10 (13.9)
Growth pattern, n (%)
Exophytic	35 (48.6)
Mesophytic	30 (41.7)
Endophytic	7 (9.7)
Pathology, n (%)
Clear-cell carcinoma	61 (84.7)
Chromophobe cell carcinoma	6 (8.3)
Papillary carcinoma	5 (6.9)

RNS=RENAL nephrometry score.

Perioperative outcomes

The median operative time was 86 min with mean segmental clamping time 25 min (the median segmental clamping time was 25.5 min with a range of 14–40 min), and the median EBL was 200 mL (range: 80–800; Table 2). In most cases, a satisfactory ischemic area was achieved by clamping 1 (47.2%), 2 (41.7%), or 3 (11.1%) branches, consistent with DSCT before surgery. All the clamping arteries were effectively isolated and clamped during the surgeries. None of the patients required conversion to main renal artery clamping or radical nephrectomy. The mean preoperative GFR was 48.42 mL/min, and the postoperative mean GFR (affected side) was 64% that of the preoperative baseline.

Table 2.

Perioperative Outcomes

Operative time, min	86.25±10.80
Clamping time, min	24.82±6.52
Estimated blood loss, mL	200 (80–800)
Clamped arteries, n (%)
1	35 (48.6)
2	28 (38.9)
3	9 (12.5)
Distribution of target arteries, n (%)
Anterior	25 (34.7)
Posterior	30 (41.6)
Combined	17 (23.6)
Preoperative GFR level (affected side), mL/min	48.42±8.14
GFR reduction, %	35.97±10.86
Complications, n (%)
Grade 1^a	6 (8.33)
Grade 2^b	5 (6.94)
Grade 3a^c	3 (4.17)
Positive surgical margin, n	0

Hematuria.

Major hemorrhage requiring transfusion.

Postoperative hemorrhage requiring intervention.

GFR=glomerular filtration rate.

The total complication rate was 19.4% (Table 2). Six patients were found with hematuria (grade 1) postoperation, with no intervention taken. Five cases required blood transfusion due to a major hemorrhage (grade 2). Three patients received superselective branch embolization intervention 2 days after surgery with the guidance of digital subtraction angiography, because of postoperative hemorrhage (grade 3a).

Associations between tumor/operative features and postoperative GFR

Univariable and multivariable linear regression analyses were performed for the tumor characteristics and intraoperative variables that may influence GFR after surgery (Table 3). In the univariable analyses, the four independent factors affecting postoperative GFR reduction were RNS, clamping time, EBL, preoperative GFR, and number of clamped arteries. The multivariable analyses showed that only RNS and the number of clamped arteries were independent factors that may decrease renal function.

Table 3.

Associations of Tumor Characteristics and Intraoperative Variables with GFR Reduction

	Univariable			Multivariable
	β (95% CI)	t	p	β (95% CI)	t	p
Gender	−0.15 (−0.089 to 0.019)	−1.30	0.197	−0.18 (−0.086 to 0.0049)	−1.78	0.08
Age	0.0066 (−0.0021 to 0.0022)	0.06	0.956	0.0032 (−0.0015 to 0.0016)	0.04	0.970
Body mass index	0.053 (−0.014 to 0.023)	0.45	0.654	0.060 (−0.0087 to 0.018)	0.73	0.469
RNS	0.63 (0.032 to 0.059)	6.73	0.000	0.39 (0.0099 to 0.048)	3.05	0.003
Tumor size	0.028 (−0.026 to 0.033)	0.24	0.812	0.058 (−0.016 to 0.032)	0.65	0.520
Operative time	0.036 (−0.0020 to 0.0027)	0.30	0.761	−0.091 (−0.0027 to 0.0008)	−1.08	0.285
Clamping time	0.31 (0.0014 to 0.0090)	2.76	0.007	−0.035 (−0.0049 to 0.0036)	−0.31	0.760
Estimated blood loss	0.30 (0.00006 to 0.0005)	2.60	0.011	0.029 (−0.0002 to 0.0002)	0.24	0.813
Preoperative GFR	0.12 (−0.0015 to 0.0048)	1.05	0.298	0.031 (−0.0018 to 0.0026)	0.37	0.713
Number clamped arteries	0.67 (0.076 to 0.13)	7.49	0.000	0.51 (0.048 to 0.11)	5.13	0.000

CI=confidence interval.

We further analyzed each individual RENAL factor and the number of clamped arteries for their effect on postoperative GFR (Table 4). The R score (i.e., regarding the radius of the tumor at maximum diameter) for the cT1b tumor was the same, and the A score was anterior or posterior descriptor, hence these two factors were excluded from the analysis.

Table 4.

Associations Between RNS and Clamped Number of Arteries and Postoperative GFR

	Univariable			Multivariable
	β (95% CI)	t	p	β (95% CI)	t	p
RNS
E	0.18 (−0.020 to 0.061)	1.02	0.31	0.18 (0.0022 to 0.058)	2.15	0.035
1	Reference	—	—	Reference	—	—
2	0.089 (−0.036 to 0.074)	0.69	0.49	0.080 (−0.022 to 0.057)	0.87	0.387
3	0.12 (−0.049 to 0.14)	0.94	0.35	0.20 (0.010 to 0.14)	2.33	0.023
N	0.58 (0.050 to 0.099)	5.99	0.000	0.35 (0.020 to 0.071)	3.95	0.001
1	Reference	—	—	Reference	—	—
2	0.53 (0.075 to 0.18)	4.91	0.000	0.36 (0.034 to 0.14)	3.32	0.002
3	0.67 (0.10 to 0.20)	6.18	0.000	0.45 (0.047 to 0.16)	3.70	0.000
L	0.45 (0.033 to 0.090)	4.26	0.000	0.11 (−0.0092 to 0.040)	1.25	0.214
1	Reference	—	—	Reference	—	—
2	0.26 (0.0061 to 0.11)	2.22	0.029	0.054 (−0.033 to 0.057)	0.55	0.583
3	0.48 (0.064 to 0.18)	4.17	0.000	0.098 (−0.028 to 0.078)	0.94	0.353
Clamped number
1	Reference	—	—	Reference	—	—
2	0.47 (0.062 to 0.15)	4.97	0.000	0.23 (0.0077 to 0.093)	2.36	0.021
3	0.64 (0.15 to 0.27)	6.78	0.000	0.46 (0.089 to 0.21)	4.93	0.000

According to the multivariable analyses, the only factors related to postoperative GFR were the RNS scores for E (exophytic/endophytic properties of the tumor) and N (nearness of tumor's deepest portion to the collecting system or sinus), and the number of clamped arteries. Regarding the E score, the difference between a score of 3 (entirely endophytic) and 1 (≥50% exophytic) was significant (p=0.023), but scores of 2 (<50% exophytic) and 1 (≥50% exophytic) were statistically comparable (p=0.387). Differences in the N score indicated that the closer the tumor was to the collecting system or sinus, the greater the postoperative GFR reduction from baseline (2 cf. 1 point: β=0.36, p=0.002; 3 cf. 1 point: β=0.45, p<0.001).

As the number of clamped arteries increased, the reduction in postoperative GFR from baseline increased (2 cf. 1 branch: β=0.23, p=0.021; 3 cf. 1 branch: β=0.46, p<0.001).

Follow-up outcomes

The median follow-up time was 24 months (range: 6–72). The overall, recurrence-free, and cancer-specific survival rates were 100%, 95.8%, and 100%, respectively.

Local recurrence was found in two patients, at postoperative 12 and 14 months, and radical nephrectomy was performed for both. These two patients are still alive. In another one patient, lung metastasis from RCC was diagnosed by biopsy at postoperative 12 months and the patient received targeted therapy. This patient is also alive at this writing. All three of these patients had initially received diagnoses of clear-cell carcinoma with negative surgical margins. No other recurrence or metastasis was found among these patients, whose follow-up time was longer than 14 months.

Discussion

To the best of our knowledge, this is the first study that focused on the outcomes of LPN for cT1b tumors using precise segmental renal artery clamping techniques. We found the outcomes to be satisfactory, indicated by short warm ischemic time, acceptable blood loss, and reliable GFR reduction, as well as high rates of overall, recurrence-free, and cancer-specific survival (100%, 95.8%, and 100%, respectively). We also showed that RNS and the number of clamped arteries were independent factors affecting GFR reduction after surgery.

Warm ischemia during LPN remains a problem, and prolonged ischemic time may cause renal dysfunction after surgery.^10,19 A number of techniques have been devised to diminish ischemic time and ischemia/reperfusion injury, including renal hypothermia²⁰ and off-clamping.^21,22 However, the limitations associated with these methods have narrowed their applications. For example, renal hypothermia to decrease warm ischemic time resulted in intraoperative hypothermia, and a reliable and consistent method has not been established.²⁰ Off-clamping to avoid renal ischemia increases blood loss when compared with main artery clamping.²² In contrast, our novel segmental clamping techniques precisely block the feeding arteries to the tumor, thus avoiding whole renal ischemia and protecting residual renal function.

Compared with open surgery, laparoscopy enlarges the hilar anatomy and provides a clearer surgical field. This makes it possible to isolate the renal artery and its branches in the renal hilum. What is more, we apply DSCT before surgery to obtain a 3D representation of the kidney, mass, vessels, and ureter, as well as the details of the arteries feeding the tumor.¹⁵ Based on the DSCT image, we can precisely clamp the targeted branch(es) without blocking the entire renal blood flow, so that the normal parenchyma can be maximally preserved (which reportedly correlates with renal function^23,24).

Our results revealed satisfactory outcomes, which are consistent with some other studies.^25

–30 The present study reports the greatest number of LPNs performed for cT1b tumors, achieving similar clamping times but shorter operative time. The EBL and perioperative complication rate are in accord with the other reported studies. However, two recurrence cases and one metastasis case were found during follow-up. All the patients had diagnoses of clear-cell carcinoma with negative surgical margins. The EBL of these three patients was 200, 300, and 200 mL, respectively. Thus, the segmental artery clamping technique not only minimized the ischemic region but also provided sufficient ischemic status of surgical parenchyma. Moreover, it also revealed reliable postoperative GFR and outcomes without compromising the oncologic outcomes.

In linear regression analyses and univariable analyses, the RNS, clamping time, EBL, and number of clamped arteries were the independent factors affecting GFR reduction. In multivariable analyses, only RNS and the number of clamped arteries were independent factors. Further analyses were performed to determine which of the individual scores of RENAL and the actual number of clamped arteries correlated with GFR reduction. Multivariable analyses showed that only E and N of the RNS and the number of clamped arteries were factors that correlated with GFR reduction.

Regarding the E score of the RNS, a significant difference existed only between scores 3 and 1 (p=0.023). This indicates that entirely endophytic tumors are significantly more likely to result in more postoperative change in GFR than tumors that are more than 50% exophytic. This may be because entirely endophytic tumors are difficult to identify intraoperatively and require more excising and suturing than nonendophytic tumors, and the extended surgical area may cause decreased renal function.

The differences in the N scores of the RNS suggest that the nearer the tumor is to the collecting system or sinus, the greater the postoperative GFR reduction. This is in logical accord with the E score, since tumors nearer to the collecting system or sinus are more likely to involve a greater surgical area and less normal parenchyma; they are also complicated to handle and demand more experienced surgical skills due to possible damage to the collecting system. The number of clamped arteries was another factor affecting renal function; both two and three clamped branches were associated with a significantly greater postoperative GFR reduction (β=0.23, p=0.021 and β=0.46, p<0.001, respectively). The need for more clamped branches suggests larger ischemic and surgical areas and less residual normal parenchyma, limiting the recovery of renal function after surgery. The combination of these three factors together implies more excising and suturing area and less remaining normal parenchyma that may prevent postoperative reduction of the GFR. Therefore, we conclude that the RNS and number of clamped arteries may be predictors of the degree of postoperative GFR reduction.

The results of this study are limited in that it is a retrospective analysis from a single center and long-term outcomes of this novel technique are still required.

Conclusions

LPN with precise segmental renal artery clamping for cT1b tumor patients is a safe and reliable approach to remove tumors and preserve normal renal parenchyma. It is also an efficacious procedure with satisfactory short-term outcomes. The RNS and number of intraoperative clamped arteries may be predictors of postoperative GFR reduction.

Footnotes

Acknowledgments

The study was approved by the Local Ethics Committees of the First Affiliated Hospital with Nanjing Medical University, Nanjing, China. Written informed consent was obtained from all participants involved in this study.

Author Disclosure Statement

No competing financial interests exist.

Abbreviations Used

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