Clampless Laparoscopic Tumor Enucleation for Exophytic Masses Greater Than 4 cm: Is Renorrhaphy Necessary?

Abstract

Objective:

To demonstrate the safety of clampless 3D laparoscopic tumor enucleation (cLTE) for exophytic T1b kidney masses, avoiding suture to achieve hemostasis.

Methods:

Between January 2010 and January 2021, 241 consecutive patients with an exophytic renal tumor underwent sutureless cLTE. Patients with predominantly endophytic growth or tumors 4 mm closer to the collecting system less were excluded. In all cases, an attempt was made to accomplish surgery without suturing kidney parenchyma. Data were obtained from a retrospective review of history and physical examinations, operative and pathology reports, anesthesia records during the hospital stay, and follow-up visits.

Results:

Among 241 patients who underwent cLTE, 148 had cT1a and 93 had cT1b renal tumor. The median tumor size was 32 mm, and the median R.E.N.A.L. (radius exophytic/endophytic nearness anterior/posterior location) score was 6. Renorrhaphy was necessary in 5 cases. The median operative time (OT) was 100 minutes, and the estimated blood loss (EBL) was 150 mL. The median 24-hour decrease in hemoglobin was 1.8 g/dL. The median length of stay was 4 days. Nineteen patients had postoperative complications: 3 cases had Clavien–Dindo (CD) 3a or more, 6 had CD2, and 10 had CD1. Comparing the T1a and T1b groups, except for the median OT and the EBL, no significant differences were observed in all the other variables analyzed. In both groups, renal function was preserved after 1 year from surgery.

Conclusion:

Our experience showed that sutureless cLTE is safe and feasible for T1b tumors leading to radical oncological outcomes and preserving renal function.

Introduction

Renal cell carcinoma accounts for 2.2% of global cancer diagnoses, and it is the seventh most common form of cancer in the developed world, with a steadily increasing incidence in recent decades.¹ The increased use of abdominal imaging has resulted in a higher frequency of incidental renal lesion <4 cm² and, therefore, attention has been paid to their optimal treatment. Over the years, nephron-sparing surgery (NSS) for localized tumors has shown excellent functional and oncological outcomes compared with radical nephrectomy³; according to the European Association of Urology (EAU), the NSS is now the gold standard for the cT1 masses.⁴

Although in the past laparoscopic partial nephrectomy (LPN) was considered more difficult and time-consuming than open partial nephrectomy, currently, each technique is considered valid.⁴

Oncologic radicality is believed to be achieved with the removal of 0.5–1 cm of healthy tissue; however, tumor enucleation has shown excellent oncological results compared with partial and radical nephrectomy.⁵

The standard NSS technique requires renal artery clamping to decrease intraoperative bleeding, but the warm ischemia time (WIT) correlates directly with hypoxia and reperfusion damage.⁶ Over the years, a progressive reduction in WIT has been obtained through the increase in surgeon's expertise and through the introduction of the clampless technique.⁷

Nowadays, the clampless technique is widely used in minimally invasive centers, and renorrhaphy is still a cornerstone in the NSS. Renorrhaphy is emerging as a negative predictor of functional outcome after NSS, as deep corticomedullary sutures can incorporate a larger amount of healthy parenchyma and cause damage to occluding important arteries.⁸

Therefore, this study aims to demonstrate the safety and feasibility of sutureless and clampless tumor enucleation for the cT1a and cT1b renal masses.

Materials and Methods

Patients

We retrospectively evaluated 287 patients who underwent clampless 3D laparoscopic tumor enucleation (cLTE) between January 2010 and June 2020. All procedures have been performed by a single skilled laparoscopic surgeon, using the same standardized technique. This study was approved by Marche Regional Ethics Committee (CERM No. 69–2021).

The exclusion criteria were predominantly endophytic growth (>50%) and proximity to the collecting system <4 mm. Therefore, 241 patients' clinical, perioperative, and follow-up data were collected. Tumor characteristics were assessed by contrast-enhanced computed tomography (CT) scan, and radius exophytic/endophytic nearness anterior/posterior location (R.E.N.A.L.) nephrometry score was calculated to estimate the surgical complexity of the masses.⁹ Every postoperative complication was recorded and ranked according to the Clavien–Dindo (CD) classification.¹⁰ Margin, ischemia, and complications (MIC) score was used to assess the cLTE safety.¹¹

Oncological follow-up has been regularly performed in all patients by full blood panel analysis within 1 month from surgery plus abdomen and chest CT or magnetic resonance imaging scan of the abdomen performed every 6 months for the first year and then yearly.

Surgical technique

Transperitoneal and retroperitoneal approaches were respectively performed for anterior and posterior masses using a three-trocar approach. Within the retroperitoneal space, the perinephric fat is dissected, exposing Gerota's fascia. Once the latter is incised, hilar vessels are identified and, in case of a tumor greater than 4 cm, skeletonized to prevent uncontrolled intraoperative bleeding. As previously reported, renal artery clamping is avoided to reduce ischemic damage to the renal parenchyma. The tumor is exposed (Fig. 1A) and, by cold blade scissors and Ultracision^® (Harmonic Scalpel^®; Ethicon Endo-Surgery, Inc.), it is enucleated and bluntly dissected following the cleavage plane (Fig. 1B, C).

FIG. 1.

(A) Identification of the mass. (B) Dissection of tumor's margins. (C) Progressive enucleation. (D) Hemostasis with fibrin-based glue. (E) Suture to close Gerota's fascia. Color images are available online.

After resection, the hemostasis is performed with the monopolar scissor on the tumor bed in spray mode (100 W) on the bleeding spots only, and the adjunct of gelatin matrix-thrombin sealants, such as Surgiflo^® (Ethicon, New Brunswick, NJ, USA) or FloSeal^© (Baxter, Deerfield, IL, USA) (Fig. 1D). When necessary, renorrhaphy was performed using the sliding clips technique. In the case of the intraperitoneal approach, Gerota's fascia is closed through a running suture (Fig. 1E). The specimen is removed using a 10-mm ENDOPOUCH RETRIEVER^® bag (Ethicon Inc., Somerville, NJ, USA). A surgical drain is placed after surgery.

Statistical analysis

Qualitative variables are described using absolute frequencies and percentages. Quantitative variables are described using the median and interquartile ranges. Continuous normally distributed variables were compared using independent samples t-tests or one-way analysis of variance. Categorical variables were compared using chi-square tests for the independence of measures. Follow-up changes in biomarkers were also calculated and analyzed using the Wilcoxon test. IBM SPSS (V26) was used as statistical software. All statistical tests were two-tailed, and P < .05 was considered to indicate statistical significance.

Results

Baseline data are summarized in Table 1. Three patients had a solitary kidney and 1 had multiple masses. Among 241 patients who underwent cLTE, 148 had cT1a and 93 had cT1b. The median tumor size was 32 mm (26–45 mm) and the median R.E.N.A.L. score was 6 (5–7).

Table 1.

Descriptive Characteristics of Patients Related to All Clampless 3D Laparoscopic Tumor Enucleation, T1a, and T1b Groups

Variable	All-cLTE group (N = 241; 100%)	T1a group (n = 148; 61%)	T1b group (n = 93; 39%)	T1a–T1b P value
Age, years	66 (57–74)	66 (58–75)	64 (55–73)	.26
Sex
Male	157 (65)	95 (64)	62 (67)
Female	84 (35)	43 (36)	31 (33)
BMI, kg/m²	26 (24–29)	27 (24–29)	26 (24–29)	.75
ASA score	2 (2–3)	2 (2–3)	2 (2–3)	.32
Anticoagulant therapy				.29
Yes	39 (16)	21 (14)	18 (20)
No	202 (84)	127 (86)	75 (80)
Charlson Comorbidity Index	5 (3–6)	5 (4–6)	4 (3–5)	.20
Solitary kidney	3 (1)	2 (1)	1 (1)	.97
Multiple masses	1 (1)	0 (0)	1 (1)	.21
Tumor size, mm	32 (26–45)	28 (22–33)	48 (45–57)	<.001
Tumor side
Right	80 (48)	54 (47)	26 (48)
Left	88 (52)	60 (53)	28 (52)
R.E.N.A.L. score	6 (5–7)	6 (5–7)	7 (6–8)	<.001
Pre-eGFR, mL/minute	91 (71.3–115.5)	90.4 (71–116)	91.2 (71.4–110.8)	.48

Data are presented as median (interquartile ranges) and frequencies (proportions).

All-cLTE, all clampless 3D laparoscopic tumor enucleation; ASA, American Society of Anesthesiologists; BMI, body mass index; pre-eGFR, preoperative estimated glomerular filtration rate; R.E.N.A.L., radius exophytic/endophytic nearness anterior/posterior location.

As shown in Table 2, the median operative time (OT) was 100 minutes (80–130 minutes) and the estimated blood loss (EBL) was 150 mL (130–188 mL). The median 24-hour decrease in hemoglobin was 1.8 g/dL (0.9–2.6 g/dL). The median length of stay was 4 days (3–5 days). None of the cLTE examined was converted to open surgery nor radical nephrectomy. Renorrhaphy was necessary in 5 cases.

Table 2.

Perioperative and Histopathological Data of Patients Related to All Clampless 3D Laparoscopic Tumor Enucleation, T1a, and T1b Groups

Variable	All-cLTE group (N = 241; 100%)	T1a group (n = 148; 61%)	T1b group (n = 93; 39%)	T1a–T1b P value
Operative time, minutes	100 (80–121)	93 (75–115)	120 (95–150)	<.001
Estimated blood loss, mL	150 (130–188)	150 (130–180)	175 (130–255)	.002
Renorrhaphy				.32
Yes	5 (2)	2 (1)	3 (3)
No	236 (98)	146 (99)	90 (97)
Conversion to radical nephrectomy				NA
Yes	0 (0)	0 (0)	0 (0)
No	241 (100)	148 (100)	93 (100)
24-Hour decrease in hemoglobin, g/dL	1,8 (0,9–2,6)	1,8 (0,9–2,5)	2,0 (0,9–2,9)	.38
Length of stay, days	4 (3–5)	4 (3–4)	4 (3–5)	.04
Clavien–Dindo classification
CD1	10 (4)	5 (3)	5 (5)	.45
CD2	6 (3)	4 (3)	2 (2)	.79
CD ≥3	3 (1)	2 (1)	1 (1)	.85
Positive surgical margins				.32
Yes	5 (2)	2 (1)	3 (3)
No	236 (98)	146 (99)	90 (97)
MIC score				.81
Yes	234 (97)	144 (97)	90 (97)
No	7 (3)	4 (3)	3 (3)

Data are presented as median (interquartile ranges) and frequencies (proportions).

All-cLTE, all clampless 3D laparoscopic tumor enucleation; CD, Clavien–Dindo; MIC, margin, ischemia, and complications; NA, not applicable.

Nineteen patients had postoperative complications, as reported in Table 3: 3 cases had major complications (CD 3a or more) and the other 16 had minor ones (10 CD1 and 6 CD2). One patient required re-surgery for hemostasis, 1 patient had renal pseudoaneurysm treated with superselective embolization, 1 patient had an episode of atrial fibrillation, which required admission to the intensive care unit. The median follow-up was 36 months, and in 1 patient with previous papillary renal cell carcinoma, abdominal CT revealed a contralateral recurrence. There were no cases of relapse. The overall survival rate at 5 years was 100%.

Table 3.

Postoperative Complications Description of Patients Related to All Clampless 3D Laparoscopic Tumor Enucleation, T1a, and T1b Groups

Complication	All-cLTE group (N = 241; 100%)	T1a group (n = 148; 61%)	T1b group (n = 93; 39%)	T1a–T1b P value
Clavien–Dindo 1	10 (4)	5 (3)	5 (5)	.45
Fever	5	3	2
Pleural injury	1	1	0
Postoperative anemia	4	1	3
Clavien–Dindo 2	6 (3)	4 (3)	2 (2)	.79
Blood transfusion	6	4	2
Clavien–Dindo 3a or more	3 (1)	2 (1)	1 (1)	.85
Re-surgery for hemostasis	1	1	0
Superselective embolization	1	1	0
Admission to ICU	1	0	1

Data are presented as frequencies (proportions).

All-cLTE, all clampless 3D laparoscopic tumor enucleation; ICU, intensive care unit.

Then, depending on tumor size, patients were categorized into T1a and T1b groups. Descriptive characteristics of patients in these two groups were similar, except for the higher R.E.N.A.L. score in the T1b group (P < .001). When comparing perioperative data in Table 2, the median OT (120 minutes versus 93 minutes, P < .01) and EBL (200 mL versus 150 mL, P < .01) were significantly higher in the T1b group, but the median 24-hour decrease in hemoglobin (1.8 g/dL versus 2 g/dL) and length of stay (4 days versus 4 days) were similar. Furthermore, no significant differences were observed for renorrhaphy necessary, major and minor complications, positive surgical margins, and MIC score rate. Also, pathological examinations show similar percentages. A comparison of preoperatory, 1 month, and 1 year from surgery renal function is reported in Table 4. In both groups, there were no significant differences in terms of medium serum creatinine and median estimated glomerular filtration rate (eGFR).

Table 4.

Preoperative, 1-Month Postoperative, and 1-Year Postoperative Renal Function Compared using Paired Wilcoxon Test

Variable	Preoperative value	1MPO value	Preoperative–1MPO P value	1YPO value	Preoperative–1YPO P value
T1a group
Serum creatinine, mg/dL	0.92 (0.75–1.09)	0.90 (0.75–1.09)	.38	0.91 (0.74–1.08)	.38
eGFR, mL/minute	90.4 (71.4–115.9)	90.2 (70.1–111.8)	.94	88.1 (71.6–109.4)	.23
eGFR change, %	—	0.3	—	–1.2	—
T1b group
Serum creatinine, mg/dL	0.92 (0.78–1.09)	0.93 (0.78–1.14)	.44	0.93 (0.78–1.12)	.28
eGFR, mL/minute	91.2 (71.4–110.8)	90.4 (67.4–111)	.74	88.3 (69–112)	.24
eGFR change, %	—	–2.8	—	–2	—

Data are presented as median (interquartile ranges) and proportions.

1MPO, 1-month postoperative; 1YPO, 1-year postoperative; eGFR, estimated glomerular filtration rate.

Discussion

Often, the diagnosis of kidney cancer occurs in the early stage, so NSS is strongly recommended. It demonstrated oncological outcomes comparable to radical nephrectomy not only for T1a but also for T1b kidney tumors.¹² Kunath et al. reported that partial nephrectomy was associated with a reduced time-to-death of any cause, whereas serious adverse event rates, cancer-specific survival, and time-to-recurrence were similar.¹³

The safety of the surgical technique is also determined by the complete removal of the tumor. In our study, only in 5 cases (2%), positive surgical margins were reported, aligned with the 0.7%–4% described by Marszalek et al. for the laparoscopic partial nephrectomy.¹⁴ As confirmed also by Minervini et al., the lack of ablation of the tumor bed does not compromise oncological radicality.¹⁵

Another noteworthy element is time to ischemia, which has to be less than 25 minutes, according to the MIC score.¹¹ Thompson et al. reported that exceeding this period increases by 5% the risk of postoperative acute renal failure and by 6% the risk of end-stage chronic kidney disease, for each additional minute.⁶ Kondo et al. also suggested that early unclamping reduces the incidence of asymptomatic renal artery pseudoaneurysm by 17.2%.¹⁶ The clampless approach is considered feasible and necessary in patients with reduced preoperative eGFR.¹⁷ However, “zero-ischemia” is not indicated at the beginning of the learning curve, as it determines a potential increased blood loss and therefore it requires the surgeon's expertise.

Furthermore, noncancer-related mortality is also greater in radical nephrectomy.¹⁸ Therefore, the preservation of renal function is fundamental and correlated directly with the amount of remaining functional parenchyma, and tumor enucleation is the best technique for this purpose. Anyway, in addition to the amount, it is important to evaluate the quality of residual renal parenchyma. Consequently, hemostatic control is in the spotlight to avoid further damage to the kidney. Nowadays, renorrhaphy has emerged as a negative predictor of functional outcome after NSS, as deep corticomedullary sutures can incorporate a larger amount of healthy parenchyma and cause damage to occluding important arteries.

In the past decade, there have been considerable improvements, such as the introduction of barbed suture and single-layer closure, thus reducing the operative time and WIT.¹⁹ To maximize the preservation of renal function, the sutureless technique represents a further step for the preservation of the eGFR. In a randomized study on the porcine model, the suture resulted in both longer operative time and a greater area of necrosis in postoperative surveillance.²⁰ Furthermore, renorrhaphy has a significantly higher rate of acute kidney injury than the sutureless approach.²¹

As alternatives, microwave tissue coagulator and an ultrasonic coagulating device may be used to decrease perioperative hemorrhagic complication, involving only the cleavage plane and not the surrounding kidney tissue. Porcine (Surgiflo)- and bovine (FloSeal)-derived gelatin matrix-thrombin sealants can assist in achieving hemostasis. These agents have shown efficacy in laparoscopic partial nephrectomy with a low overall hemorrhage and urine leakage rate.²²

In our study, 2 (1%) cases of major complications associated with failure to control hemostasis occurred, including a case of renal artery pseudoaneurysm. In a meta-analysis including 5229 patients, the incidence of the latter is higher after minimally invasive partial nephrectomy than after an open approach (1.96% versus 1%).²³ Jain et al. also reported that the suture of the renal bed may lacerate arterioles, favoring the onset of pseudoaneurysm, as previously described for ischemia. Therefore, our clampless and sutureless technique reduces the risk of this complication, as demonstrated in comparison with our percentage.

Table 5 compares the studies found on PubMed regarding sutureless laparoscopic partial nephrectomy.^24–29 Variables such as the percentage of cases with renorrhaphy, major complications, positive surgical margins, and changes in renal function during follow-up are similar. According to the literature, it was already evident that this procedure was effective for cT1a kidney tumors. To the best of our knowledge, the present study is the first report focusing on clampless LPN without renorrhaphy for cT1b tumors.

Table 5.

Perioperative Outcomes of Sutureless Laparoscopic Partial Nephrectomy Series for Renal Tumors

Variable	Minervini et al.²⁴	Kihara et al.²⁵	Simone et al.²⁶	Introini et al.²⁷	Zhang et al.²⁸	Dell'Atti et al.²⁹	Present study
Patients	32	103	101	62	142	143	241
Tumor size, mm	M 19	23	24	M 27	M 32	27	32
Cases cT1b or higher	0 (0)	9 (9)	0 (0)	—	—	—	93 (39)
Estimated blood loss, mL	M 107	244	100	M 165	M 100	110	150
Warm ischemia time, minutes	M 16	0	0	0	0	0	0
Hemostatic renorrhaphy rate	0	2 (2)	4 (4)	0 (0)	0 (0)	3 (2)	5 (2)
Clavien–Dindo 3a or more	0	3 (3)	0 (0)	0 (0)	—	1 (1)	3 (1)
Positive surgical margins	—	4 (4)	0 (0)	2 (3)	2 (1)	4 (3)	5 (2)
Change in eGFR, %	—	–2.4 (3MPO)	1.6 (1YPO)	0.1 (3MPO)	—	–1 (6MPO)	−1.4 (1YPO)

Data are presented as median, and frequencies (proportions).

1YPO, 1-year postoperative; 3MPO, 3-month postoperative; 6MPO, 6-month postoperative; eGFR, estimated glomerular filtration rate; M, mean.

However, this article has clear limitations. First, it is a retrospective study. We used nephrometry scoring and selected appropriate patients, which is a selection bias. Besides, the follow-up of patients' renal function is limited to 1 year after surgery, and therefore, it is not possible to evaluate the long-term outcome. Finally, a single experienced laparoscopic surgeon was involved, so our findings need to be confirmed in multicentric studies.

Conclusions

Sutureless cLTE using soft coagulation and gelatin matrix-thrombin sealants appears to be feasible also for cT1b tumors, despite this resulting in greater operative time and intraoperative blood loss. This procedure may reduce the incidence of chronic renal failure while maintaining oncological safety. Nevertheless, further prospective studies with a bigger sample size are needed to ensure the safety of this procedure for kidney tumors greater than 4 cm.

Footnotes

Authors' Contributions

M.D.B. and V.I. conceived of the presented idea. C.G. developed the theory and performed the computations. A.M. and M.D. verified the analytical methods. V.F. encouraged W.G. and G.S. to compare the present study with the literature and supervised the findings of this work. All authors discussed the results and contributed to the final article.

Ethics Approval

Data collection followed the principles of the Declaration of Helsinki and its amendments. This study was approved by Marche Regional Ethics Committee (CERM No. 69–2021).

Disclosure Statement

No competing financial interests exist.

Funding Information

No funding was received for this article.

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