Trifecta Outcomes of Laparoscopic Partial Nephrectomy for T1a and T1b Renal Tumors: A Single-Center Experience in a Tertiary Care Institution

Abstract

Objective:

To assess the effectiveness and safety of laparoscopic partial nephrectomy (LPN) in T1a and T1b renal tumors using “Trifecta” in partial nephrectomy and determine the predictive factors in respect to the criteria that constitute Trifecta.

Materials and Methods:

We retrospectively analyzed the data harvested from the patients who underwent LPN for T1a or T1b tumors. Preoperative, perioperative, and postoperative outcomes were evaluated and analyzed. Patients who had grade <2 Clavien complications, negative surgical margins, and minimal renal function deterioration (warm ischemia time [WIT] ≤25 minutes and ≤15% postoperative estimated glomerular filtration rate [eGFR] decrease) were acccepted to fit the strict Trifecta outcomes. Multivariate analysis was done using logistic regression test to determine the predictive factors affecting Trifecta.

Results:

A total of 128 patients underwent LPN. Of these, 65 (50.8%) patients had cT1a and 63 (49.2%) patients had cT1b renal tumors. The mean age was 55.8 (24–85) years. Mean operative time was 143.6 (100–200) minutes. A total of five (3.9%) patients had positive surgical margins. Mean WIT was 22.1 minutes. Ten patients (7.8%) had a >15% decrease in eGFR after surgery. Complications were observed in 11 (8.6%) patients. A total of 78 (60.9%) patients had strict trifecta outcomes. Tumor size was found to be a predictive factor affecting Trifecta at multivariate analysis.

Conclusions:

Introduction

Incidental diagnosis of renal masses has been increased due to the improvement and widespread use of imaging techniques.¹ European Association of Urology (EAU) guidelines recommend partial nephrectomy (PN) as the standard procedure for the renal masses as long as it is technically feasible.²

PN can be performed with open (OPN), laparoscopic (LPN), or robotic (RPN) approaches depending on tumor complexity and surgeon's experience. Even though OPN remains to be the gold standard technique in most centers around the globe, there is an overall sentiment to shift from open to minimally invasive PN procedures as LPN or RPN.

RPN has replaced standard laparoscopy in many high-volume centers.³ However, it is an expensive system and not all institutes have sufficient funding to own one. Mainly for this reason, LPN is continuing to be performed extensively.^3–5 LPN series have reported similar oncologic outcomes with significantly shorter hospital stay and lower analgesic requirement.^3,4 The transition from OPN to LPN is gradual, and the initial experiences with LPN were associated with relatively increased urological complications and longer warm ischemia time (WIT).^4–6 However, with increasing experience in years to come, complication rates have decreased.

Trifecta was first reported by Hung et al. and described within the terms of having no complication, negative surgical margin, and minimal renal function decrease.⁷ Since renal function preservation correlates with WIT, some authors reported a WIT ≤25 minutes to be a determinant of “Trifecta” outcomes as well. In some studies, Trifecta was simply defined as having complication-free surgery, negative surgical margins, and WIT ≤25 minutes.^8,9 In this study, to evaluate renal function preservation more precisely, both WIT and postoperative 6th month estimated glomerular filtration rate (eGFR) decrease were taken under consideration. Patients with absence of grade ≥2 Clavien-Dindo complications, WIT ≤25 minutes, ≤15% postoperative eGFR decrease, and negative surgical margins were reported to achieve strict Trifecta outcomes.

Herein, we investigate the outcomes of (strict) trifecta in cases of LPN to offer a wider range of indications and potentially expand the applicability of LPN for T1a and T1b renal tumors. To the best of our knowledge, this article reports data from one of the largest single-center LPN series, in terms of (strict) Trifecta outcomes for management of T1a and T1b renal tumors. Hence, we investigated the predictive factors affecting Trifecta outcomes.

Materials and Methods

The data of patients who underwent LPN between January 2012 and May 2017 at our institution were analyzed. The patients with T1a and T1b renal tumors and the patients we followed up for longer than 1 year at our institution were included in this study. All patients were evaluated preoperatively with renal ultrasonography (US) and a computerized tomography scan (CT) or magnetic resonance imaging (MRI). All procedures were performed by a single surgical team.

Preoperative demographics and tumor characteristics, including age, body mass index (BMI), American Society of Anesthesiologists (ASA), comorbidities, hematocrit (Hct), serum creatinine (Cr) level, eGFR, tumor size, side, and R.E.N.A.L. nephrometry scores, were recorded. Intraoperative and postoperative data, including operative time, WIT, surgical margin status, estimated blood loss (EBL), intraoperative and postoperative complications, postoperative serum Cr level, Hct, and eGFR, were also scrutinized. Renal function was analyzed before the surgery and at postoperative 6th month so as to calculate eGFR through the modification of diet in renal disease (MDRD) equation.¹⁰ Postoperative 6-month eGFR was used to determine the percentage of decrease in eGFR. The R.E.N.A.L. nephrometry score was used for assessing tumor complexity.¹¹ Postoperative complications were documented based on the Clavien-Dindo grading system.¹²

Patients with an absence of grade ≥2 Clavien-Dindo complications, WIT ≤25 minutes, ≤15% postoperative eGFR decrease, and negative surgical margins were reported to achieve strict trifecta outcomes. After trifecta outcomes were determined, predictive factors affecting trifecta were assessed.

Statistical analysis

The evaluation and analysis of the data were performed using the SPSS 21.0 computer package program, Microsoft Office Excel 2010 program. The numerical values were expressed as mean ± standard deviation and median (min-max). Categorical data were expressed in terms of frequency and percentage. The chi-square test was used as the categorical variable in evaluating the difference between the groups in the analyses. Kolmogorov-Smirnov test was used as normal distribution test for numerical data. Two independent groups of continuous variables were categorized and studied in following terms: independent groups t test was used when normal distribution conditions were met, and Mann–Whitney U test was used when normal distribution conditions were not met. Paired-sample t test was used for the analysis of preoperative and postoperative changes. Predictive factors for Trifecta were examined by using backward logistic regression in multivariate analysis. There were three independent variables (age, BMI, and tumor size), which were proper for logistic regression analysis. For statistical significance, P < .05 was accepted.

Results

A total of 128 patients underwent LPN during the study period. Of these, 65 (50.8%) patients had T1a and 63 (49.2%) patients had T1b renal tumors. The mean age and BMI were 55.8 (24–85) years and 28.2 (18.7–42.4) kg/m², respectively. The tumor was on the left side in 55 (42.9%) and right side in 73 (57.1%) patients. Among the 128 patients, 88 (68.7%) had associated comorbidities with an average ASA score of 1.7 (1–3). The mean R.E.N.A.L. nephrometry score was 7.1 (4–10) (Table 1).

Table 1.

Characteristics of Patients and Cooperative Findings

Patient characteristics	N
No. of patients	128
Age (year)
Mean (range)	55.8 (24–85)
Sex
Female	35 (27.3%)
Male	93 (72.7%)
Side
Left kidney	55 (42.9%)
Right kidney	73 (57.1%)
BMI (kg/m²)
Mean (range)	28.2 (18.7–42.4)
ASA score
Mean (range)	1.7 (1–3)
R.E.N.A.L. Nephrometry score
Mean (range)	7.1 (4–10)
Operation time (min)
Mean (range)	143.6 (100–200)
Clinical tumor stage
T1a	65 (50.8%)
T1b	63 (49.2%)
Tumor size (cm)	4.2 (1–6.9)
Mean (range)
Bleeding (mL)	416 (50–1100)
Mean (range)
Perioperative complications according to Satava Classification	1 (0.8%)
Grade 3	1 (0.8%)
Postoperative complications according to Clavien Classification	11 (8.6%)
Grade 1	7 (5.5%)
Grade 2	1 (0.8%)
Grade 3b	3 (2.3%)
Hospitalization time (days)
Mean (range)	3.05 (2–11)
Positive surgical margins	5 (3.9%)
Warm ischemia time (minutes)
Mean (range)	22.1 (12–31)

BMI, body mass index.

Mean operation time was 143.6 (100–200) minutes. The mean tumor size in the surgical specimen was found to be 4.2 (1–6.9) cm. Mean WIT was 22.1 minutes and mean EBL was also noted as 416 (50–1100) mL.

Complications were observed in 11 (8.6%) patients (7 Clavien 1, 1 Clavien 2, and 3 Clavien 3b). Seven patients had postoperative bleeding that resolved with conservative managements (Clavien 1). One patient had postoperative bleeding necessitating transfusion (Clavien 2). Three patients had urinary extravasation and a double-j catheter was inserted as a preventive measure in these three patients (Clavien 3b).

The levels of Cr and eGFR were significantly lower in the postoperative period than in the preoperative period. Functional outcomes are given in Table 2.

Table 2.

Preoperarive and Postoperative Changes in Serum Hematocrit, Creatinine, and Estimated Glomerular Filtration Rate

Variables	Preoperative	Postoperative (6th Months)	Relative change (%)	P value
Creatinine
Mean (range)	0.90 (0.5–2.8)	1.00 (0.5–3.0)	+5.22	.049^a
Hct	41.1 (29–49)	34.8 (17–45)	−14.8	<.001^a
eGFR
Mean (range)	88.7 (24.2–176.2)	84.9 (21.7–171.9)	−3.6	<.001^a

Paired t test.

eGFR, estimated glomerular filtration rate; Hct, hematocrit.

A total of 104 (81.2%) patients had a WIT ≤25 minutes. Of these, five patients had positive surgical margins (PSM). Ten patients (7.8%) had >15% decrease in eGFR after surgery. A total of 78 (60.9%) patients had trifecta outcomes. Age, BMI, side of tumor, previous abdominal surgery, ischemia, stage of tumor, or nephrometry score was not found to be a predictive factor for Trifecta at univariate analysis (Table 3). However, size of tumor was found to be a risk factor for Trifecta, in univariate analysis. In addition, the size of tumor was found to be a statistically significant risk factor regarding trifecta outcomes in multivariate analysis (Table 4).

Table 3.

Predictive Factors for Trifecta at Univariate Analysis

Variables	Trifecta (+)	Trifecta (−)	P value
Age	57.0 (26–85)	53.9 (24–76)	.166
BMI	27.6 (18.7–42.4)	29.2 (21.2–42.4)	.075
Side			.279
Left	31 (56.4%)	24 (43.6%)
Right	48 (65.8%)	25 (34.2%)
Previous abdominal surgery			.631
Yes	18 (58.1%)	13 (41.9%)
No	61 (62.9%)	36 (37.1%)
Ischemia			.410
Yes	16 (55.2%)	13 (44.8%)
No	63 (63.6%)	36 (36.4%)
Clinical tumor stage			.493
T1a	42 (64.6%)	23 (35.4%)
T1b	37 (58.7%)	26 (41.3%)
Nephrometry score	7.1 (4–10)	7 (4–10)	.828
Size (cm)	3.6 (1.0–6.8)	4.8 (2.2–6.9)	<.001

Table 4.

Logistic Regression Analysis for Trifecta

Variables	P	Exp (B)	95% CI for lower	95% CI for upper
Age	.837	0.996	0.963	1.031
BMI	.174	0.941	0.863	1.027
Size	.000	0.416	0.282	0.615

Discussion

Currently, PN is the “gold standard” treatment for organ-restricted renal tumors when it is technically feasible. Its oncological outcomes are similar as radical nephrectomy for small renal tumors (<4 cm).¹³ The upper bound for the diameter of a resectable tumor for PN is usually considered 7 cm whenever feasible.¹⁴ After the introduction of the minimally invasive approaches such as laparoscopy and robot-assisted laparoscopy, there is a trend toward performing nephron-sparing surgeries by using these modalities. Nephron-sparing techniques within the introduction of the robotic platform are gaining widespread popularity among many centers across the world, and indications for it are continuously expanding. Unfortunately it is an expensive system; every center cannot afford to have it. Specifically for this reason, LPN continues to be performed at relatively higher rates in health centers across the globe, especially in developing countries. Therefore, when making the decision that partial nephrectomy is indicated as a treatment modality in a patient, the level of experience of the surgeon, the characteristics of the patient, the diameter of the tumor, the complexity of the tumor, the technological equipment of the hospital, and financial factors should be taken under consideration. The Trifecta is often used to assess the success of PN.^7–9 In this study, a total of 128 patients underwent LPN. There were 65 (50.8%) patients who had T1a and 63 (49.2%) patients T1b renal tumors. We achieved strict trifecta outcomes in 78 (60.9%) of the patients.

Making a study with trifecta to describe the clinical successes and outcomes of LPN is a relatively new trend. Trifecta stands in as a measure of surgical quality and has been increasingly used as a standardized tool to compare outcomes. Trifecta criteria differ in the literature, but principally consist of absence of complications, negative surgical margins, and minimal renal function decrease. There is a large alteration of the rates on achievement of Trifecta, varying from 32% to 81%.^15–17 The wide range of alteration is caused by many factors such as the used surgical techniques, surgeon's experience, and differing definitions of Trifecta on PN cases. Khalifeh et al. reported a 31.6% achievement of the trifecta outcome in a large single-surgeon LPN series; according to the group doing the study, the low rate of achievement was due to their inexperience with LPN on earlier cases at the beginning of their study and manipulation of some of the trifecta inclusion criteria.¹⁷ There are studies in literature that examine the risk factors for trifecta. Osaka et al. found that tumor size and the experience of the surgeon were significant risk factors in multivariate studies, in which the predictive factors for LPN were studied.¹⁸ They also achieved a trifecta rate of 62%, similar to ours. On the contrary, they did not include a risk scoring for other parameters elaborating tumor complexity, such as the nephrometry score we used in our study. Likewise, only the tumor size was found to be statistically significant to predict trifecta outcomes with multivariate analysis, in this study (P < .001).

Without distinction in the literature, through open or laparoscopic nephrectomy case-based studies, the number of studies with long-term follow-up and adequate number of patients focusing on oncological outcomes on a comparative basis is very rare. However, PSM effect on recurrence rate and overall survival in renal cancer is still argumentative. PSM is reported between 0.7% and 4.4% for LPN, in the literature.^19,20 Predictive risk factors for PSM are not fully known. However, some studies showed that PSM affects tumor recurrence rate, but does not appear to have an effect on cancer-specific survival.^21,22 While other studies have not demonstrated a clear interrelation,^23,24 PSM rate has been reported to be in the range of 4.9%–8.1% for the open and laparoscopic nephron-sparing techniques.²⁵ In our study, 3.9% of the patients had PSM in the pathological specimens obtained during surgery.

An important feature and also a scaling parameter for all nephron-sparing surgeries is the grade of preservation of renal function. Inevitably, most studies described a decrease in eGFRs and an increase in serum Cr levels. In recent studies, it is noteworthy that there is a significant relationship between prolonged WIT and development of de novo renal dysfunction.^26,27 WIT is also a predictor of the postoperative eGFR. In the study of Thompson et al., 362 patients who underwent OPN or LPN due to a mass in the solitary kidney were enrolled, and it is reported that every 1-minute increase in WIT increased the risk of acute renal failure by 1.05 times.²⁷ In addition, they found a significant relationship between the duration of warm ischemia and the development of postoperative de novo stage 4 chronic kidney disease. Other important results of the study can be listed as follows: these findings are valid when a controlled analysis is performed according to preoperative factors (GFR, tumor diameter, and surgical technique), there is also a report in the study stating that the duration of critical WIT as 25 minutes can be considered a threshold for acute renal failure and de novo stage 4 chronic renal failure to develop. Some authors have speculated that whatever surgical approach is preferred, the duration of warm ischemia should not be longer than 20 minutes, and the duration of cold ischemia longer than 30–35 minutes.^6,28

In a recent study evaluating the long-term (10-year) functional outcomes of laparoscopic and open partial nephrectomy, Lane et al. found that median GFR decreased by 16.9% in the laparoscopic group and by 14% in the open group.²⁹ Although the difference is not significant, as the duration of warm ischemia increased, the decline in GFR was also reported to be more evident. Several studies have investigated the renal deterioration rate using eGFR by far and it averages between 5.6% and 14.7% throughout the literature.^30–33 In our study, a WIT of 25 minutes and >15% postoperative eGFR decrease were set as a cutoff point regarding strict Trifecta criteria to ensure optimal renal function preservation. The mean WIT was found to be 22.1 minutes in our study. The result is compatible with most of the recent comparative studies between LPN and OPN, where LPN results constantly associated with a longer WIT. Marszalek et al., Gill et al., and Lane et al. reported a mean of 23, 30, and 20 minutes WIT, respectively, in their series.^3,4,29 Hence, decline rate of eGFR in our study was 3.6% and found to be in concord with the aforementioned outcomes in the literature supporting good functional outcomes of LPN at postoperative 6th month.

Although it is not a universally accepted standard procedure, during the maximum tolerable WIT, it is technically possible to complete the surgery without clamping the pedicle, to avoid chronic kidney disease that may emerge after partial nephrectomy. However, since the aforementioned technique is not always possible, some technical modifications [continuous suture technique, pedicle clamping, early clamp administration, sliding clamps, renografi, segmental arterial clamping, and zero-ischemic technique] have been innovated to minimize the duration of warm ischemia in the minimally invasive partial nephrectomy procedure for optimization of renal function.^6,28,34–36 Morphometric scoring systems (R.E.N.A.L. nephrometry score, P.A.D.U.A. score, and C-index) used to express tumor complex in a standard and objective manner, they can also be used to predict the duration of warm ischemia.^11,37,38 The surgeon might be more inclined to perform an open surgical technique for nephron-sparing surgery under warm ischemia if tumor complexity is higher. In a prospective study, Porpiglia et al. have documented that low renal functions occurred within 3 months after LPN procedure and remained stable until the 12th month subsequently.³² In another study, the author stated that a clampless nephrectomy should be performed whenever feasible, particularly in patients with poor baseline renal functions.¹⁴ In the our study, 30 of the patients underwent clampless LPN. The mean R.E.N.A.L. nephrometry score was 7.1 (4–10) and it did not alter the trifecta outcomes (P = .828). We also recorded eGFRs of the patients 6 months after the operation to monitor the long-term kidney functions and viability. Clamping procedure was not found to be statistically significant for predicting trifecta outcomes (P = .410).

One of the patient groups we find challenging for LPN procedure is the obese patient group. Romero et al. compared 56 obese and 56 nonobese patients on an LPN-based study.³⁹ As a result, there was no difference in terms of operation time, ischemia time, and complication rates. However, they reported higher bleeding rates in the obese group compared to the nonobese patient group (300 vs. 200 mL, P > .05). It is emphasized that the most important factors for LPN success in obese patients are proper positioning and port placement. Similarly, BMI was not found to have a statistically significant effect to predict trifecta outcomes in our study. (P = .075).

Currently, there are no prospective randomized trials comparing open and minimally invasive partial nephrectomy techniques within the parameters of perioperative morbidity, oncological outcomes, and functional outcomes. Although the robotic approach is a newer technique, it shows similar performance for perioperative outcomes and complication rates compared to laparoscopic and open approaches. However, it can be stated that open and minimally invasive approaches do not have a remarkable advantage on one another, given the perioperative results and complications. Comparison of 118 consecutive LPNs and 129 consecutive RPNs performed by three experienced surgeons in minimally invasive surgery, a retrospective study with no difference in terms of BMI, age, sex, and tumor size, the mean operative time (RPN: 189 minutes and LPN: 174 minutes), pathologic tumor size (RPN: 2.8 cm and LPN: 2.5 cm), and surgical margin positivity (RPN: 3.9% and LPN: 1%) recorded in laparoscopic and robotic partial nephrectomy were similar.⁴⁰ In this study, there were no significant differences between the groups in terms of major and minor complications. It was reported that urine extravasation developed in three patients in the RPN group and four in the LPN group. The most frequent complications in LPN are bleeding (5%) and urinary leakage (4.2%). In our study, complications were observed in 11 patients (8.3%). Seven patients had postoperative bleeding that resolved with conservative management (Clavien I). One patient had postoperative bleeding necessitating transfusion (Clavien II). Three patients had urinary extravasation and a double-J catheter was inserted for these three patients (Clavien IIIB). All patients recovered without complications.

This study has some limitations. First and foremost, this is a retrospective study. Second, although the number of patients is sufficient for a study of that kind, it is not a comparative study interrelating open or robotic partial nephrectomy. It should not be forgotten that under normal practice, many surgeons make the clinical decision for the patient to undergo LPN; we used nephrometry scoring and selected appropriate patients. This constitutes a selection bias. In addition, due to the short-term follow-up and limited time span we could have achieved, postoperative renal functions could have been evaluated only 6 months after the surgery; long-term follow-up is required to asses more elaborate oncological data and renal function prognosis. However, we believe that this study, which reports the results of consecutive LPN operations in patients with T1a and T1b renal tumors in a certain time span in our clinic, including trifecta outcomes, is noteworthy. The results of our study suggest that LPN has acceptable trifecta outcomes. Only the tumor size was found to be a predictive factor regarding the Trifecta criteria. However, there is a necessity for prospective, randomized controlled trials involving larger patient series.

Conclusion

LPN procedure has been shown to demonstrate improved strict Trifecta outcomes in patients with T1a and T1b renal tumors. Only the tumor size was found to be a predictive factor regarding the Trifecta criteria. Further prospective and randomized controlled studies, including large series of patients, are needed.

Footnotes

Disclosure Statement

No competing financial interests exist.

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