Comparison of Kidney Function in the Early Postoperative Period in Transperitoneal Robot-Assisted Laparoscopic Partial Nephrectomy Between Anterior and Posterior Renal Tumors: A Propensity Score-Matched Study

Abstract

Objective:

To compare early postoperative renal function in transperitoneal robot-assisted laparoscopic partial nephrectomy (RAPN) for anterior and posterior renal tumors.

Patients and Methods:

This study included 227 patients who underwent transperitoneal RAPN for anterior or posterior renal tumors. Tumor position was defined by RENAL nephrometry score. To minimize selection bias between anterior and posterior tumors, patient variables were adjusted using 1:1 propensity score matching.

Results:

Of the 227 patients, 125 were classified as having anterior tumors and 102 as having posterior tumors. After matching, 82 patients were included in each group. The mean preoperative estimated glomerular filtration rate (eGFR) was 66 mL/min/1.73 m². The mean tumor size was 28 to 29 mm. The decrease in early postoperative nadir eGFR (−10% vs −4.0%, p = 0.0103) was significantly higher for posterior tumors than for anterior tumors. However, the difference improved 6 to 12 months after surgery (−6.0% vs −6.2%, p = 0.9564). The other surgical outcomes, including operative time, warm ischemia time (WIT), complications, surgical margin status, and length of hospital stay, were not significantly different between the two groups. In multivariate analysis of the entire cohort, posterior tumors (vs anterior tumor, odds ratio [OR]: 2.30, p = 0.0051), longer WIT (OR: 3.10, p = 0.0019), and high tumor complexity (vs low complexity, OR: 3.46, p = 0.0264) were independent predictors for development of a 10% decrease in early postoperative eGFR.

Conclusions:

Posterior tumors had a greater decrease in early postoperative nadir eGFR than anterior tumors, with equivalent surgical outcomes, including similar renal function, 6 to 12 months after surgery in the setting of transperitoneal RAPN.

Introduction

Robot-assisted laparoscopic partial nephrectomy (RAPN) is widely utilized for small renal tumors, and the indication is expanding to more challenging cases. Two surgical approaches, transperitoneal and retroperitoneal, are used in RAPN and the selection depends on tumor position or surgeon preference. At our institution, a transperitoneal approach is mainly used for RAPN except for tumors located posteriorly and at the renal hilum.

We encountered several patients with posterior tumors who developed acute kidney injury (AKI) after RAPN, despite small renal mass size and short ischemic time. In the case of kidney tumors located in a posterior position, the kidney is mobilized to expose the tumor surface in transperitoneal RAPN, and there is a possibility of compression of the renal hilum, especially in patients without adequate abdominal space or with a kidney covered with abundant fat. In such cases, ischemic kidney injury during mobilization may occur in addition to during renal hilum clamping.

There are several reports describing the association of ischemic kidney injury with acute and late postoperative renal function; however, the association is stronger in the acute phase than in the late phase, given the conditions of limited warm ischemia or hypothermal ischemia.I.^1,2 There are few reports analyzing the impact of kidney function in the acute postoperative period according to tumor position, such as anterior or posterior, specifically in transperitoneal RAPN.^3,4

In the present study, we compared surgical outcomes, including early postoperative renal function after transperitoneal RAPN between anterior and posterior tumors, using propensity score matched analyses.

Patients and Methods

Patient population

We obtained study approval from the Institutional Review Board of our hospital. A total of 417 patients who underwent RAPN between January 2014 and August 2016 participated in this study. Patients with a solitary kidney, lateral tumors, or whose surgery was performed using a retroperitoneal approach were excluded. Patients were divided into two groups according to their tumor position, anterior and posterior. The tumor position was determined according to the RENAL nephrometry score (RENAL-NS).⁵ The following patient background characteristics were considered to be adjusted by 1:1 propensity score matching to minimize selection bias between the two groups: age, sex, body mass index, Charlson comorbidity index,⁶ tumor size, tumor complexity (RENAL-NS), and preoperative estimated glomerular filtration rate (eGFR). Perioperative surgical outcomes were defined as follows: a decrease in early postoperative nadir eGFR, decrease in postoperative eGFR, incident rate of AKI stratified by risk, injury, failure, loss and ESKD (RIFLE) criteria,⁷ operation time, warm ischemia time (WIT), estimated blood loss (EBL), transfusion, surgical margin status, perioperative complications defined by the Clavien–Dindo classification system,⁸ and postoperative length of hospital stay (PLOS).

Surgery

RAPN was performed using the techniques previously described.⁹ All surgeries were performed by three specific surgeons. All RAPN procedures were performed under warm ischemia. Renal arteries were clamped with a bulldog clamp in most cases. The renal vein was also clamped when tumors were in close contact with the main branches of the renal vein. After completing the incision, an inner running suture was placed using a barbed suture (15 cm 3-0 V-Loc^® 180 with a half-circle 17-mm needle; Covidien, New Haven, CT). After the inner suture, the arterial clamp was removed and the absence of arterial bleeding confirmed. Renorrhaphy was performed using a barbed suture (30 cm 2-0 V-Loc 180 with a half-circle 37-mm needle; Covidien) and a TachoSil^® bolster was placed in the defect.

Renal function evaluation

All serum creatinine measurements were analyzed at a single clinical reference laboratory and eGFR values were estimated using the Modification of Diet in Renal Disease 2 equation recently modified for Japanese patients, as stipulated by the Japanese Society of Nephrology (eGFR = 194 × serum creatinine [mg/dL]^−1.094 × age^−0.287 × 0.739 [if female]).¹⁰ Early postoperative nadir eGFR was evaluated on postoperative day 1 to 7. AKI was evaluated using nadir eGFR. Postoperative renal function was evaluated between 6 and 12 months after surgery.

Statistical analysis

Continuous variables were analyzed using the Mann–Whitney U-test, and categorical variables were analyzed using the χ ² test. Multivariate logistic regression analyses were used to calculate the propensity scores and to analyze factors associated with development of a 10% decrease in eGFR. All analyses were performed using JMP 11.2.0 software (SAS Institute, Cary, NC), and p-values less than 0.05 were considered statistically significant.

Results

Table 1 presents a comparison of patient backgrounds. A total of 227 patients, including 125 patients with anterior tumors (Ant group) and 102 patients with posterior tumors (Post group), were included in this study. Before matching, there were no differences in patient characteristics between the two groups. After matching, 82 patients were assigned to each group. The mean tumor size was 28 to 29 mm in diameter, and the mean preoperative eGFR was 66 mL/min/1.73 m². Almost 50% of patients had intermediate complex tumors, and 10% of those had high-complex tumors.

Table 1.

Patient Characteristics

	Prematching			Postmatching
	Ant (125)	Post (102)	p	Ant (82)	Post (82)	p
Age (years), mean ± SD	57 ± 13	58 ± 13	0.5566	58 ± 12	57 ± 13	0.3921
Sex, male, n (%)	94 (75)	67 (66)	0.1419	55 (67)	59 (72)	0.4975
BMI (kg/m²), mean ± SD	24 ± 3.7	24 ± 3.2	0.5527	24 ± 3.9	24 ± 3.3	0.8699
Preop eGFR (mL/min/1.73 m²), mean ± SD	68 ± 16	67 ± 19	0.7002	66 ± 16	66 ± 19	0.9604
CCI, mean ± SD
1	0.9 ± 1.5	0.9 ± 1.3	0.8553	0.9 ± 1.4	0.9 ± 1.4	0.8674
Tumor complexity, n (%)
Low (4–6)	46 (37)	35 (34)	0.1829	28 (34)	32 (39)	0.8007
Intermediate (7–9)	62 (50)	60 (59)		47 (57)	43 (52)
High (10–12)	17 (14)	7 (7)		7 (9)	7 (9)
Tumor size (mm), mean ± SD	27 ± 11	29 ± 11	0.2038	28 ± 11	29 ± 11	0.5943
R, n (%)
1	106 (85)	84 (82)	0.8833	72 (88)	68 (83)	0.471
2	18 (14)	17 (17)		10 (12)	13 (16)
3	1 (1)	1 (1)		0	1 (1)
E, n (%)
1	36 (29)	27 (26)	0.762	19 (23)	25 (30)	0.5713
2	74 (59)	65 (64)		54 (66)	49 (60)
3	15 (12)	10 (10)		9 (11)	8 (10)
N, n (%)
1	46 (37)	25 (25)	0.1336	22 (27)	24 (29)	0.9364
2	16 (13)	17 (17)		14 (17)	14 (17)
3	63 (50)	60 (59)		46 (56)	44 (54)
L, n (%)
1	49 (39)	41 (40)	0.063	35 (43)	35 (43)	0.9754
2	17 (14)	25 (25)		14 (17)	15 (18)
3	59 (47)	36 (35)		33 (40)	32 (39)

Ant = anterior; BMI = body mass index; CCI = Charlson comorbidity index; eGFR = estimated glomerular filtration rate; Post = posterior; Preop = preoperative; RAPN = robot-assisted laparoscopic partial nephrectomy; SD = standard deviation.

Table 2 shows a comparison of the surgical outcomes between the two groups. After matching, when compared with preoperative eGFR, the early postoperative nadir eGFR showed a mean 4.0% decrease in the Ant group and a mean 10% decrease in the Post group, which was significantly different (p = 0.0103). However, the difference was not significant 6 to 12 months after surgery (Ant: −6.2%, Post: −6.0%, p = 0.9564). The incidence rate of AKI was 9% in the Ant group and 18% in the Post group, which was not significantly different (p = 0.0668). The mean WIT was 19 minute in both groups. The other surgical outcomes of surgical margin status, perioperative complications, and PLOS were not significantly different.

Table 2.

Surgical Outcomes

	Prematching			Postmatching
	Ant (125)	Post (102)	p	Ant (82)	Post (82)	p
Preop eGFR (mL/min/1.73 m²), mean ± SD	68 ± 16	67 ± 19	0.7002	66 ± 16	66 ± 19	0.9604
Early postop eGFR (mL/min/1.73 m²), mean ± SD	64 ± 17	60 ± 18	0.1179	63 ± 17	60 ± 19	0.1875
Change in early postop eGFR (%), mean ± SD	−5.1 ± 15	−9.5 ± 14	0.026	−4.0 ± 14	−10 ± 15	0.0103
AKI risk, n (%)	12 (10)	16 (16)	0.1654	7 (9)	15 (18)	0.0668
Postop at 6–12 m eGFR (mL/min/1.73 m²), mean ± SD	64 ± 17	64 ± 18	0.9194	62 ± 2.0	63 ± 2.0	0.7998
Change in postop at 6–12 m eGFR (%), mean ± SD	−5.7 ± 11	−4.9 ± 15	0.6005	−6.2 ± 1.4	−6.0 ± 1.4	0.9564
OT (min), mean ± SD	196 ± 40	187 ± 46	0.0743	194 ± 37	190 ± 46	0.3682
Console time (min), mean ± SD	127 ± 38	136 ± 36	0.0225	127 ± 39	137 ± 36	0.1019
Ischemia time (min), mean ± SD	19 ± 8.4	20 ± 7.5	0.5963	19 ± 8.1	19 ± 7.9	0.7998
EBL (mL), mean ± SD	65 ± 169	101 ± 191	0.1313	74 ± 204	107 ± 210	0.3013
Transfusion, n (%)	1 (1)	2 (2)	0.4462	1 (1)	2 (2)	0.5601
SM positive, n (%)	0	1 (1)	0.2672	0	0	1
Perioperative complications, n (%)
Overall	22 (18)	21 (21)	0.5676	9 (11)	16 (20)	0.1283
Clavien 1–2	(6%)	(11%)		(2%)	8 (10)
Clavien 3	15 (12)	10 (10)		7 (9)	8 (10)
PLOS (day), mean ± SD	4.7 ± 2.5	4.3 ± 1.7	0.2418	4.5 ± 2.4	4.3 ± 1.7	0.7689

AKI = acute kidney injury; Ant = anterior; EBL = estimated blood loss; OT = operation time; PLOS = postoperative length of hospital stay; SM = surgical margin.

Table 3 provides multivariate analysis of factors that were associated with the 10% decrease in early postoperative nadir eGFR. In all, 89 (39%) patients had a 10% decrease in eGFR in this study. Tumors located in a posterior position (vs anterior position, odds ratio [OR]: 2.30, p = 0.0051), high-complex tumors (vs low complexity, OR: 3.46, p = 0.0264), and longer WIT (≥25 minutes vs <25 minutes, OR: 3.10, p = 0.0019) were the independently significant factors.

Table 3.

Factors Associated with Development of 10% Decrease in Early Postoperative Nadir Estimated Glomerular Filtration Rate

Factors	OR (95% CI)	p
Tumor position
Anterior	Reference
Posterior	2.30 (1.28–4.19)	0.0051
Tumor complexity
Low	Reference
Intermediate	1.43 (0.76–2.75)	0.2706
High	3.46 (1.16–10.8)	0.0264
WIT
<25 min	Reference
≥25 min	3.10 (1.51–6.42)	0.0019
Age
<70 years	Reference
≥70 years	0.89 (0.38–2.05)	0.7918
Tumor size
≤4 cm	Reference
>4 cm	1.01 (0.44–2.30)	0.9711
Preop eGFR
>60 mL/min/1.75 m²	Reference
≤60 mL/min/1.75 m²	1.04 (0.54–2.01)	0.8954
CCI
<2	Reference
≥2	0.74 (0.35–1.51)	0.4057
BMI
≤25	Reference
>25	1.69 (0.93–3.11)	0.0865

CI = confidential interval; OR = odds ratio; WIT = warm ischemia time.

Discussion

The choice of a retroperitoneal or transperitoneal approach in RAPN for renal masses depends on tumor position, surgeon preference, and abdominal surgical history. At our institution, a retroperitoneal approach is used in patients with posterior and hilum tumors. Therefore, more than 90% of RAPNs were performed using a transperitoneal approach. A transperitoneal approach for posterior renal tumors requires mobilization of the kidney to expose the renal tumor, which is not required for anterior renal tumors. In addition, the surgical field tends to be limited in cases of large tumors or tumors with abundant adhesive perirenal fat in transperitoneal RAPN for posterior tumors. Therefore, there are more concerns about inferior surgical outcomes such as a longer operative time or more perioperative complications in tumors located in a posterior position than for those in an anterior position.

The present study showed no significant differences in the surgical outcomes of operative time, EBL, surgical margin status, PLOS, or perioperative complications between posterior and anterior renal masses. However, we demonstrated that posterior tumors had a significantly greater decline in early postoperative nadir eGFR than anterior tumors (Ant: −4.0%, Post: −10%, p = 0.0103). In addition, multivariate analysis of the overall cohort demonstrated that posterior position of the tumor is an independent predictor for a 10% decrease in nadir eGFR (OR: 2.30, p = 0.0051) along with tumor complexity (OR: 3.46, p = 0.0264) and WIT (OR: 3.10, p = 0.0019). The reason for our result is unclear, but ischemic injury during mobilization of the kidney in posterior tumors could explain this finding. In addition, perirenal fat around the tumor is removed to determine an incision line. During this procedure, renal vessels in the renal hilum could be inflected or compressed, which may damage renal parenchyma by ischemic injury if the procedure requires a comparatively long duration in cases of abundant and adhesive perirenal fat or a small abdominal cavity.

Acute functional decline after PN is the result of parenchymal mass reduction or ischemic kidney injury. Parenchymal mass reduction is irreversible kidney injury. By contrast, ischemic kidney injury can recover under limited conditions. Several articles demonstrated that patients with AKI after PN recovered their kidney function 3 to 12 months after surgery, given the conditions of cold ischemia or limited warm ischemia were applied.^1,2,11 Zhang and colleagues evaluated the etiologies of AKI after PN and their prognostic significance in a solitary kidney. They demonstrated that acute decline in function after PN was associated with more prolonged ischemic time and appeared to impact subsequent functional recovery. However, most kidneys eventually recovered strongly.¹ The present study showed greater deterioration in eGFR during the early postoperative period in tumors located in a posterior position (−10%) than in the anterior position (−4%). However, the difference improved within 3 to 6 months postoperatively (Post: −6.0%, Ant: −6.2%, p = 0.9564). As mentioned above, parenchymal mass reduction is an irreversible kidney insult. The functional recovery seen in the present study may indicate that acute kidney functional decline in posterior tumors is a result of ischemic injury.

Several studies have addressed the surgical feasibility of RAPN for anterior or posterior renal masses, as we did.^3,4 Harris and colleagues analyzed 260 patients who underwent transperitoneal RAPN with 92 cases of posterior tumors and 168 cases of anterior tumors. They demonstrated no significant difference in operative time, WIT, EBL, PLOS, positive surgical margins, reduction in eGFR, and postoperative complications according to tumor position. Paulucci et al. reported a similar study of 123 patients, including 46 patients with anterior tumor and 77 patients with posterior tumor, and showed no significant differences in surgical outcomes. In addition, they analyzed postoperative renal function at discharge (mean PLOS, 1.4–1.5 days) and demonstrated no significant differences according to tumor position, which differs from our study. The reason for this difference is unclear; however, patient characteristics such as better preoperative renal function, shorter WIT, or shorter operative time in their study might account for the difference.

According to our results, some posterior tumors, including larger tumors or tumors with abundant perirenal fat, which may require long operative time or WIT, may be appropriate for a retroperitoneal approach. There are several benefits of a retroperitoneal approach in RAPN for posterior tumors such as easier exposure of the renal artery or tumor position without kidney mobilization, which may prevent acute kidney damage. The feasibility of a retroperitoneal approach in RAPN has been evaluated in several studies.^12,13 Choo and colleagues compared surgical outcomes between transperitoneal RAPN and retroperitoneal RAPN with matched-pair comparisons by nephrometry score and demonstrated that retroperitoneal RAPN had a shorter operative time, but perioperative results were generally equivalent to those of transperitoneal RAPN.¹² Stroup and colleagues reported similar result of a shorter operative time using a retroperitoneal approach and better utility in posterior tumors.¹³

Our study has several limitations. First, this study was retrospective in nature, was conducted at a single institution, and included a population of tertiary care patients. Second, the decrease in eGFR of the operated kidney could not be estimated because pre- and postoperative renal scans were not performed, which might not correctly reflect ischemic kidney injury. However, patients with a solitary kidney were excluded from this study; therefore, we believe that global renal function can be an alternative to that of operative kidney function. Third, lack of renal mass preservation analyses, which is the most important factor for postoperative renal function, might influence the renal function 6 to 12 months after surgery. The strengths of this study include a relatively large cohort and matching of patient characteristics between those with anterior and those with posterior tumors by propensity scoring; thus, the surgical and functional outcomes were well balanced and comparable between the two groups.

Conclusions

This study showed a greater deterioration in early postoperative nadir eGFR in posterior tumors than in anterior tumors in transperitoneal RAPN with surgical outcomes being similar. Although the difference in the deterioration had improved 6 to 12 months after surgery, some posterior tumors, which require long WIT and operative time, may be good candidates for a retroperitoneal approach.

Footnotes

Acknowledgment

We thank Ms. Nobuko Hata for her secretarial work.

Author Disclosure Statement

No competing financial interests exist.

Abbreviations Used

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