Estimated glomerular filtration rate on postoperative day 7 predicts renal function preservation outcome after robot-assisted partial nephrectomy

doi:10.21203/rs.3.rs-5311045/v1

Purpose

To assess the predictive value of estimated glomerular filtration rate (eGFR) on postoperative day (POD) 7 in forecasting the post-operative renal function in patients who underwent robot-assisted partial nephrectomy (RAPN).

Methods:

We retrospectively examined data on RAPN performed from August 2016 to May 2022 at the University of Yamanashi hospital and assessed patient background, surgical outcome, and renal function. The eGFR preservation rate on POD7, and in 6 and 12 months were checked. The data were analyzed with Mann-Whitney U test and Fisher's exact test. Pearson’s product moment correlation coefficient was used to evaluate correlation between eGFR preservation rate within POD7 and in postoperative 12 months.

Results:

A total of 207 patients were included in this study. Median age was 66 and 141 male (68.1%) and 177 patients had cT1a tumor (85.5%) . The median tumor size was 25 mm. Trifecta was achieved in 162 cases (78.3%). In the group with less than 90% eGFR preservation at 12 months after surgery, both eGFR with postoperative 7 days and 6 months were significantly lower than the group with above 90%. Between these two groups, there was no significant difference in patient background and perioperative data. Logistic regression analysis also showed over 90% of eGFR preservation rate within POD7 was a factor associated with over 90% preserved at post-operative 12 months.

Conclusion:

Care should be taken to the patients with decreased eGFR at postoperative 7 days on RAPN to detect the post-operative renal function decrease and transfer to chronic renal failure treatment earlier.

Robot-assisted partial nephrectomy

renal tumor

prediction

renal function

postoperative 7-day eGFR

Robot-assisted partial nephrectomy (RAPN) was reported by Gettman et al in 2004 and is currently the standard treatment for small renal masses.[1] Compared with radical nephrectomy, RAPN for small renal mass has similar cancer-specific and overall survival and is considered to be useful in preserving renal function. [2] International guidelines recommend RAPN as the standard of care not only for cT1a tumors but also for cT1b tumors when possible. [3] [4] In Japan, RAPN has been covered by national insurance since April 2016 and spread nationwide. In our hospital, RAPN was introduced in August 2016 and indicated for the treatment of T1a and T1b renal tumors. Trifecta is a concept reported by Hung et al defined as the achievement of the following three criteria: 1) warm ischemia time (WIT) < 25 minutes, 2) no postoperative complications, and 3) negative tumor margin. [5] The distinction between WIT < 25 min and > 25 min is an important factor for the preservation of renal function: Rod et al reported that WIT < 25 min does not affect the preservation of postoperative renal function, and Thompson et al reported that WIT > 25 min is associated with new onset of stage IV chronic kidney disease (CKD) in the postoperative period. [6] [7] Other factors that have been reported to influence postoperative preservation of renal function in RAPN include age, preoperative renal function, tumor volume. In RAPN, preservation of renal function is important to prolong overall survival. [7] In this study, we evaluated the clinical outcome of RAPN and examined the factors that influence the preservation of renal function in the short-term and long-term postoperative period.

Patient selection

We retrospectively reviewed patients who underwent RAPN performed by skilled surgeons from August 2016 to May 2022 in University of Yamanashi hospital. The skilled surgeons are endoscopic and robotic surgical skill qualified surgeons admitted by the Japanese Society of Endourology and Robotics, or surgeons equally qualified by the University of Yamanashi hospital robotic surgery committee. A total of 210 patients were retrieved. Three cases were excluded because of the following reasons, 1) a patient whose surgery was transferred from RAPN to open nephrectomy for exceeded surgical time, 2) a patient whose surgery was transferred to open surgery due to difficulty in hemostasis, and 3) a patient who had two tumors removed simultaneously in a single RAPN.

Patient characteristics

Patient characteristics and surgical outcomes were extracted from their medical records. Age, gender, body mass index (BMI), preoperative estimated glomerular filtration rate (eGFR), maximum tumor size, clinical stage, approaching method, tumor location, and renal nephrometry score (RNS).

Surgical Technique

Surgical outcomes included operative time, console time, WIT, estimated blood loss (EBL), postoperative complications, histopathological findings, eGFR preservation rate within postoperative day (POD) 7, and Trifecta achievement. The surgical system was da Vinci Si surgical system until May 2019 and da Vinci X/Xi surgical system thereafter. Postoperative complications were classified according to the Clavien-Dindo classification. Achievement of Trifecta was defined as 1) WIT < 25 minutes, 2) no postoperative complications higher than Clavien-Dindo grade II within 4 weeks after surgery, and 3) negative surgical margin.

Assessment of renal function

The eGFR obtained from serum Creatinine and chronic kidney disease (CKD) stage (stage 1, 2, 3a, 3b, 4, 5) were used as an evaluation index of renal function. The postoperative eGFR preservation rate was defined as "postoperative eGFR/preoperative eGFR x 100". To evaluate long-term preservation of renal function, we collected eGFR value which satisfy the following criteria: 1) eGFR data available at 6 months and 12 months after surgery at our institution and 2) RAPN performed only once in the following 12 months.

Statistical analysis

Medians and interquartile range (IQR) were used to present continuous variables. The Mann-Whitney U test and Fisher's exact test were used for comparison between the two groups. Pearson’s product moment correlation coefficient was used to evaluate correlation between eGFR preservation rate within POD7 and at POM12. P < 0.05 was considered a statistically significant difference. All statistical analyses were performed using R statistical software.

In this study, 207 cases of RAPN were included. The patient background information is shown in Table 1. The median age was 66.5 years (IQR: 56–73), 143 males (68.1%), and 177 cT1a tumors (85.5%) were included. The median maximum tumor diameter was 25 mm (IQR: 20–35). The approach method was transperitoneal in 117 cases (56.5%). The median RNS was 7 (IQR: 6–8). Surgical outcomes are shown in Table 2. The median operative and console times were 216 minutes (IQR: 183–252) and 126 minutes (IQR: 97–164), respectively. The median WIT was 15 minutes (IQR: 12–21) and the median EBL was 41 ml (IQR: 20–96). Postoperative complications occurred in 14 patients (6.8%), with 6 patients (3.0%) having a Clavien-Dindo classification of 3 or higher.

Table 1

Patient characteristics
N = 207
Variables	N (%) or Median (IQR)
Age (years)	66 (56–73)
Gender (male)	141 (68.1%)
BMI (kg/m²)	23.8 (21.5–26.3)
Tumor size (mm)	25 (20–35)
Tumor side (right)	97 (46.9%)
Clinical stage
cT1a	177 (85.5%)
cT1b	30 (14.5%)
Approach
Transperitoneal	117 (56.5%)
Retroperitoneal	90 (43.5%)
Tumor location
Anterior	0 78 (37.7%)
Posterior	0 73 (35.3%)
Neither	50 (24.2%)
Anterior + Hilar location	1 (0.5%)
Posterior + Hilar location	4 (1.9%)
Neither + Hilar location	1 (0.5%)
Renal score	7 (6–8)

Table 2

Surgical outcomes
N = 207
Variables	N (%) or Median (IQR)
Surgical tool
da Vinci Si surgical system	83 (40.1%)
da Vinci X/Xi surgical system	124 (59.9%)
Operative time(min)	216 (183–252)
Console time(min)	126 (97–164)
WIT (min)	15 (12–21)
Blood loss (ml)	41 (20–96)
Postoperative complication (Clavien-Dindo classification)	14 (6.8%)
1	5 (2.4%)
2	2 (1.0%)
3a	5 (2.4%)
wound dehiscence	1
TAE for pseudoaneurysm	4
3b	2 (1.0%)
port site hernia	1
diaphragm injury	1

Histopathological findings showed that 180 tumors (87.0%) were malignant, of which 141 cases (68.1%) were clear cell renal cell carcinoma. Tumor margins were positive in 1 case (0.5%) and margins were indistinguishable in 4 cases (2.0%). Three cases (1.4%) were diagnosed pT3a postoperatively, due to renal fibrous capsular invasion with negative tumor margins.

In terms of Trifecta, 178 (86.0%) had WIT < 25 minutes, 202 (97.5%) had negative tumor margins, and 193 (93.2%) had no postoperative complications. Trifecta was achieved in 162 cases (78.3%). There were significant differences in tumor size, renal score, operative time, console time, WIT, eGFR preservation rate within POD 7, and trifecta achievement between cT1a group and cT1b group.

Preoperative eGFR, CKD stage before surgery, postoperative 7 days, and downgrade of CKD stage within POD 7 of the 207 patients were shown in Table 3. Median preoperative eGFR was 67(ml/min/1.73m2). The preservation rate of eGFR within POD 7 was 97.1%, and downgrade of CKD stage within POD7 was confirmed in 38 patients (18.4%).

Logistic regression analysis of factors associated with short term renal function were analyzed univariable and multivariable. With the univariable analysis, operative time, console time, WIT, and trifecta achievement were associated with the short-term renal function preservation, there was no factor associated. Male gender and WIT had a trend in preserving the short-term renal function.(Table 4)

Table3: Preoperative and short term postoperative Renal function in 207 patients

Table 4

Logistic regression analysis of factors associated with short term renal function.
	Univariable analysis		Multivariable analysis
	OR (95% CI)	P	OR (95% CI)	P
Age (years)	0.98 (0.96–1.01)	0.22	0.98 (0.95–1.01)	0.13
Gender (Male)	0.37 (0.17–0.79)	0.01	0.32 (0.13–0.76)	0.01
BMI (kg/m²)	1.07(0.98^1.16)	0.12	1.03(0.93–1.13)	0.60
Tumor size (mm)	1.03 (1.01–1.06)	0.02	1.00 (0.97–1.04)	0.83
R.E.N.A.L. score	1.13 (0.94–1.35)	0.94	1.07 (0.86–1.32)	0.54
Operative time (min)	1.01 (1.00-1.01)	< 0.01	0.99 (0.99–1.01)	0.79
Console time (min)	1.01 (1.00-1.02)	< 0.01	1.01 (0.99–1.02)	0.20
WIT (min)	1.07 (1.03–1.12)	< 0.01	1.07 (0.99-1.00)	0.02
Blood loss (ml)	1.00 (0.99-1.00)	0.69	1.00 (0.14–0.78)	0.93
Trifecta achievement	2.18 (1.08–4.37)	< 0.01	0.87 (0.31–2.40)	0.79

Renal function follow-up in 120 patients who were chased for 12 months and were shown in Table 8. The median preoperative eGFR was 67 (IQR: 56–79) and the preoperative CKD stage was Stage 2 in 72 cases (60.0%). Postoperative eGFR declined to 66.5, and 63, 61.5 on POD7, and in postoperative month (POM) 6 and 12, respectively. The preservation rate of eGFR declined to 98.1% (IQR: 50.8-105.4), 94.4%(IQR: 64.3-100.4), and 92.4% (IQR: 64.1–100.0), in POD7, POM 6 and 12, respectively. Downgrade of CKD stage was 14.2%, 21.7%, and 25.8%, in POD7, POM 6 and 12, respectively. (Table 5)

Table 5

Long term renal function in 120 patients
N = 120
Variables	N (%) or Median (IQR)
	Preoperative	within POD7	At POM6	At POM12
eGFR (ml/min/1.73cm2)	67 (56–79)	66.5 (55–74)	63 (54–71)	61.5 (52–70)
eGFR preservation rate (%)	―	98.1 (50.8–105.4)	94.4 (64.3-100.4)	92.4 (64.1–100.0)
CKD stage
Stage 1 (eGFR 90-)	11 (9.2%)	10 (8.3%)	9 (7.5%)	6 (5.0%)
Stage 2 (eGFR 60–89)	72 (60.0%)	64 (53.3%)	60 (50.0%)	61 (50.8%)
Stage 3a (eGFR 45–59)	26 (21.7%)	32 (26.7%)	36 (30.0%)	36 (30.0%)
Stage 3b (eGFR 30–44)	8 (6.7%)	12 (10.0%)	12 (10.0%)	13 (10.8%)
Stage 4 (eGFR 15–29)	3 (2.5%)	2 (1.7%)	2 (1.7%)	3 (2.5%)
Stage G5 (eGFR < 15)	0 (0%)	0 (0%)	1 (0.8%)	1 (0.8%)
Downgrade of CKD stage from preoperative stage	―	17 (14.2%)	26 (21.7%)	31 (25.8%)

We have compared the long-term follow-up for the preoperative eGFR, tumor size, operative time, console time, the eGFR preservation rate between the WIT of within or over 25 minutes groups. The preservation rates of eGFR between these two groups have no significant difference, however, there were trends of decrease in POM6 (p value = 0.12) and POM12 (p value = 0.28). (Data not shown)

The comparison of eGFR preservation rates of over and below 90% groups at POM 12 was shown in Table 6. There was no significant difference in the preoperative eGFR, tumor size, operative time, console time, WIT, and blood loss, however, the eGFR preservation rate below 90% group was significantly lower in POD 7 (100.0 vs. 93.8% p = 0.01) and in POM6 (98.5 vs. 88.6% p < 0.01). Comparison of the eGFR preservation rate in POD7 between the two groups of over and below 90% showed a similar significant decrease at POM6 (98.5 vs 88.6% p < 0.01)and POM 12(93.5 vs 88.1% p < 0.01).

Table 6

Comparison of 90% and over eGFR preservation group and under 90% eGFR preservation group
N = 120
Variables	N (%) or Median (IQR)		P value
% eGFR preservation rate at POM12	90% and over preservation (n = 71)	Under 90% preservation (n = 49)
Preoperative eGFR(ml/min/1.73cm2)	65 (54–75)	70 (60–76)	0,28
Tumor size(mm)	25 (20–34)	29 (20–37)	0,29
Operative time (min)	217 (182–242)	228 (191–260)	0.25
Console time (min)	135 (103–164)	124 (104–150)	0.47
WIT (min)	15 (11–22)	15 (12–21)	0.45
Blood loss (ml)	43 (20–89)	33 (18–72)	0.49
eGFR preservation rate
Within POD7	100.0 (92.8-107.7)	93.8 (88.6-101.4)	0.01
At POM 6	98.5 (88.6-125.9)	88.6 (82.9–94.4)	< 0.01
At POM 12

The Pearson’s correlation value between eGFR preservation rate within POD7 and at POM12 was 0.363 (95%CI 0.197–1.509, P value < 0.01). (Fig. 1)

In this study, we examined the initial outcomes of RAPN at our institution, comparing surgical outcomes for cT1a/cT1b tumors and investigated factors influencing long-term renal function preservation. Partial nephrectomy is considered the standard treatment for small renal tumors in various guidelines such as NCCN, EAU guidelines. [3] [4] Partial nephrectomy for small renal tumors is considered to have equivalent cancer control to radical nephrectomy while preserving renal function, and it is associated with significantly higher overall survival rates. [8] RAPN, reported by Gettman and colleagues in 2004, offers advantages over laparoscopic surgery. [1] It provides a 3D expanded field of view and the use of the versatile EndoWrist, allowing for more delicate and high-degree-of-freedom surgery compared to laparoscopic procedures. [1] Due to these advantages, it has become possible to safely approach challenging cases with tumors larger than 4 cm or tumors located at the renal hilum, and to reduce WIT compared with the laparoscopic procedures. In the 2020 multicenter study by Furukawa et al involving 804 Japanese cases, WIT of 21 minutes, a Trifecta achievement rate of 62.1%, and a complication rate (Clavien-Dindo classification 3 or higher) of 5.8% were reported. [9] The outcome in our study is comparable to these previous studies. In our study of 207 cases, WIT of 15 minutes, a Trifecta achievement rate of 78.3%, and a complication rate of 3.4% were observed. When comparing the data of 96 cT1b tumors from Furukawa et al. with 30 cT1b tumors from our institution, the results showed WIT 20 vs. 20 minutes, EBL 70 vs. 30 ml, postoperative complications 14.7 vs. 13.3%, positive surgical margins 3.2 vs. 0%, and Trifecta achievement rates 48.4 vs. 56.7%, respectively. [9] Our institution yielded results with minimal blood loss, few postoperative complications, and a Trifecta achievement rate comparable to previous studies. From the above results, we believe that RAPN can be safely performed for both cT1a and cT1b tumors at our institution. Factors influencing the preservation of renal function after partial nephrectomy have been examined in previous studies. Thompson et al. reported that for every 1-minute increase in WIT, the risk of developing stage IV chronic kidney disease (CKD) increases by 5%. [8] They also reported a cutoff value for WIT influencing renal function decline as 25 minutes. [8] [10] Dagenais et al. stated that the excised tumor volume was correlated with eGFR preservation six months later, while WIT and tumor complexity did not show a clear correlation with eGFR preservation. [7] Regarding ischemia, discussions have been held not only about the duration of WIT but also about the method of vascular clamping. [11] [12] [13] In renal artery clamping methods during RAPN, complete renal artery clamping, which temporarily obstructs the entire renal blood flow, was predominant. [1] [14] However, considering the impact of WIT on renal function, alternative approaches such as selective clamping, which selectively occludes arterial branches nourishing the tumor, and off-clamp techniques, where tumor resection is performed without vascular occlusion, have been employed. [15] Several reports suggest their utility in preserving renal function. [16] [17] [18] Selective clamping may be challenging in cases where vascular identification is difficult or when it becomes impractical to perform actual selective occlusion due to certain difficulties. The off-clamp technique is applicable only to small tumors and may require a skilled operator; however, it carries the risk of increased bleeding and the need for blood transfusion. [19] [20] Due to the above reasons, it cannot be applied in all cases. It has been reported that if WIT is 25 minutes or less, it does not have a long-term impact on renal function. [5] In our institution's RAPN cases, complete renal artery clamping method is employed in all cases, and hemostasis is achieved by suturing the renal parenchyma. With these firmed methods, the median eGFR preservation rate at 12 months postoperatively exceeds 90%, leading us to believe that renal function is well-preserved. In the short-term assessment of this study, it was found that WIT had an impact on eGFR preservation of 90% within one week after surgery. However, in the long-term evaluation, no significant difference was observed with a WIT cutoff value of 25 minutes. On the other hand, in the group with 90% eGFR preservation at 12 months, significant differences were observed in eGFR preservation within one week and at six months after surgery. It is suggested that the early decrease in eGFR within one week is a predictor for subsequent eGFR decline. Based on the above results, patients with a low eGFR preservation rate within one week after surgery may suggest a potential for long-term renal function decline. Therefore, long-term monitoring of renal function should be conducted for such cases. Factors associating the renal function preservation after partial nephrectomy are reported to be age, hypertension, RNS, preoperative eGFR, WIT, preservation of normal parenchyma volume and others. We identified gender (male) and WIT as predictive risk factors of short-term renal function.

This study has several limitations. First, this is a retrospective study conducted in a single institute with small sample size. The data does reflect skilled surgeons in a tertiary academic center, however, a broad mix of demographic groups with a complex patient population should be included to assess the true predictive value of eGFR at POD7. Secondly, patients treated at our institution with favorable postoperative outcomes are often referred to other hospitals, so there is a possibility that renal function decline or recurrence may be overlooked at other institutions. Thirdly, in the patients from whom eGFR data were acquired at postoperative one year, some of them had comorbidities other than renal cancer and they had to continue follow-up at the university hospital. It is suggested that factors other than RAPN might be involved in renal function decline. These factors can account for the contradiction between the results of logistic regression analysis for short-term renal function preservation and long-term renal function preservation rates based on WIT less than 25 minutes versus 25 minutes or more. To improve the above issues, it is necessary to increase the number of follow-up cases and collaborate with other hospitals to conduct precise tracking of renal function. This is the first study to our knowledge to evaluate the utility of eGFR at POD 7 in RAPN. Recently quite a few institutes have lessened the length of hospital stay as 1 day or less, however, the average length of hospital stay is longer in Japan due to the national public health insurance system. We have utilized the eGFR at POD7 as a milestone to forecast the postoperative renal function in the longer period.

RAPN was effectively and safely performed at our institution. Patients with a decrease in eGFR on POD7 following RAPN should be followed carefully for renal function because of the possibility of a long-term decline in renal function.

RAPN

Robot-assisted Partial Nephrectomy

RNS

renal nephrometry score

WIT

warm ischemia time

eGFR

estimated glomerular filtration rate

CKD

chronic kidney disease

POD

postoperative day

POM

postoperative month

IQR

interquartile range

Author Contribution

All authors contributed to the study conception and design. Manuscript writing. M.K.: Data collection. M.K.: Statistical analysis. M.K., N.S.: Manuscript revision and editing. M.K., N.S Manuscript revision and editing. All authors read and approved the final manuscript.

Data Availability

Data is provided within the manuscript.

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No competing interests reported.

Estimated glomerular filtration rate on postoperative day 7 predicts renal function preservation outcome after robot-assisted partial nephrectomy

Status:

Version 1

Abstract

Figures

Introduction

Methods

Patient selection

Patient characteristics

Surgical Technique

Assessment of renal function

Statistical analysis

Results

Discussion

Conclusion

Abbreviations

Declarations

Author Contribution

Data Availability

References

Additional Declarations

Status:

Version 1