Associations between R.E.N.A.L nephrometry score and survival outcomes in renal tumors

doi:10.21203/rs.3.rs-2594683/v1

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Associations between R.E.N.A.L nephrometry score and survival outcomes in renal tumors

https://doi.org/10.21203/rs.3.rs-2594683/v1

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Objective

R.E.N.A.L. nephrometry score could be used to predict surgical outcomes and renal tumor aggressiveness. We aimed to analyze its associations with survival outcomes.

Materials and methods

We included 1368 patients with sporadic, unilateral and non-metastatic renal tumors who received curative nephrectomy in Zhongshan Hospital from January 2009 to September 2019. R.E.N.A.L. nephrometry scores (RNS) were assigned by three urologists based on preoperative CT/MRI scans. Correlations between parameters or sum of RNS, overall survival (OS) and recurrence-free survival (RFS) were analyzed by Kaplan-Meier analyses and multivariate cox regression model. We further compared survival outcomes between patients who received partial nephrectomy and patients who received radical nephrectomy.

Results

We observed statistically significant associations between all components of RNS and oncologic outcomes, including R (Radius) (OS, p < 0.001; RFS, p < 0.001), E (Exophytic/endophytic) (OS, p = 0.003; RFS, p < 0.001), N (Nearness) (OS, p = 0.063; RFS, p < 0.001), A (Anterior/posterior) (OS, p < 0.001; RFS, p = 0.005), L (Location) (OS, P = 0.008; RFS, p < 0.001) and suffix “h” (OS, p = 0.237; RFS, p = 0.034). Kaplan-Meier curves of OS and RFS rates were significantly different when stratified by RNS complexity group (OS, p < 0.001; RFS, p < 0.001). After adjusting for tumor stage and grade, RNS as continuous variables was an adverse independent risk factor for survival outcomes [p = 0.027, HR (95%CI) = 1.151 (1.016–1.303)] and RFS [p < 0.001, HR(95%CI) = 1.299 (1.125–1.501)]. For tumors with RNS score of 4 and 5, partial nephrectomy showed a survival benefit than radical nephrectomy.

Conclusion

Both components and complexity groups of R.E.N.A.L. nephrometry score associated with survival outcomes in renal tumor patients.

R.E.N.A.L nephrometry score

Renal tumors

Overall survival

Recurrence-free survival

partial nephrectomy

Partial nephrectomy demonstrates equal oncologic results [1] and better preservation of renal function [2] in comparison with radical nephrectomy, thus it has become the standard of care for localized renal tumors. Despite reduced impairment of renal functions, there was higher risk of complications in patients receiving partial nephrectomy [3]. With the common aim of standardizing anatomical complexity, estimating perioperative complications and assisting strategic surgical planning, several anatomical scoring systems have been developed [4]. Among the scoring systems, R.E.N.A.L. nephrometry score remains the most recognized and used system in the literature [5]. The R.E.N.A.L. nephrometry score is composed of five independent anatomic features, which are R, radius, the maximal diameter of tumor; E, exophytic/endophytic properties of the tumor; A, anterior or posterior of the tumor; L, location relative to the kidney’s polar line. The suffix “h” is assigned if the tumor touched the main renal artery or vein[6]. It could be a useful tool to evaluate tumors based on the difficulty to perform partial nephrectomy and aid in surgical approaches selection. Higher RNS indicates increased chance of opting for radical nephrectomy. RNS has been validated to be a predictor of surgical outcomes including warm ischemia time, estimated blood loss, length of hospital stay, complications, etc [7, 8].

On the other hand, accumulating evidence suggest a strong connection between RNS and tumor aggressiveness [9–12]. Renal lesions with low RNS are more likely to be indolent while lesions with high RNS are more likely to be aggressive. However, actual impact of anatomic features on survival outcomes remains unclear. There were few reports regarding patient survival [13–15]. This study aimed to evaluate the associations between the RNS and patient survival in renal tumors.

Patient selection:

We included 1368 patients who underwent curative surgery for sporadic, unilateral and non-metastatic renal tumors with pathologically proved malignant renal cell carcinoma (RCC) from 2009 to 2019 in Zhongshan Hospital, Fudan University. Patients who received neoadjuvant therapy, died during perioperative period, had no preoperative CT/MRI scans or lacked follow-up information were not enrolled. The study was approved by the ethics committee of Zhongshan Hospital, Fudan University with the approval number B2021-608R.

Date Collection

Clinicopathological information such as age, gender, surgery approach, ISUP grade and TNM stage were obtained from the electronic database of Zhongshan Hospital. Tumor nucleus grade for clear cell renal cell carcinoma (ccRCC) and papillary renal cell carcinoma (pRCC) were reevaluated by pathologist Run W. and Jun H. according to 2012 ISUP consensus [16]. TNM stage were assessed based on 2017 AJCC classification of RCCs. Three experienced urologist (Yu Q, Wei X and Ying X) blinded to pathological reports evaluated the CT/MRI scans to assign the six parameters of RNS to each patient. We analyzed survival outcomes including recurrence-free survival (RFS), disease-specific survival (DSS) and overall survival (OS). RFS was defined as the time of surgery to the time of local recurrence or distant metastasis. DSS was calculated from the data of curative nephrectomy to death from renal tumors. Postoperative follow up was physician dependent, generally every 3 to 6 months in first 2 years and annually thereafter.

Statistical Analyses

Statistical analyses were carried out with SPSS Statistics 21.0. Comparisons of survival outcome in different subgroups were performed with Kaplan-Meier analyses and log-rank tests. We used the cox proportional hazards regression model for univariate and multivariate analyses. Since only ccRCC and pRCC were graded, multivariate analyses were performed in these two subtypes of RCCs. Statistical tests were two tailed and p < 0.05 was considered statistically significant.

Baseline characteristics of patients in Zhongshan cohort

In this study, a total of 1368 patients with median age of 57.7 and median tumor size of 4.0 cm were included (Table 1). Among them, 470 patients were female and 898 were male. Sixty-four percent of patients went through radical nephrectomy and the remaining sixty-four percent received partial nephrectomy. Tumor grades were only evaluated in clear cell RCCs and papillary RCCs for proved associations between tumor grades with survival in these two subtypes. Grade 1, 2, 3, 4 RCCs accounts for 5.6, 66.8, 14.1, 1.3 percent of total patients respectively. There were 83.5% stage I tumors, 6.2% stage II tumors, 10.1% stage III tumors and 0.1% stage IV tumors in Zhongshan cohort. Renal cell carcinomas represent 98.3% cases, epithelioid angiomyolipomas represent 1.3% patients and sarcomas represent 0.4% patients. There were 18.9% tumors classified as low complexity by RNS, 54.8% as intermediate complexity and the remaining 26.4% as high complexity.

Table 1

Clinical characteristics of patients in Zhongshan cohort
Characteristics	Patients
Characteristics	n	%
Age
Mean ± SD	57.7 ± 12.0
Gender
Female	470	34.4
Male	898	65.6
Surgery
Partial nephrectomy	492	36.0
Radical nephrectomy	876	64.0
Tumor size
Mean ± SD	4.0 ± 2.2 (cm)
ISUP grade
1	77	5.6
2	914	66.8
3	193	14.1
4	18	1.3
TNM Stage
I	1142	83.5
II	85	6.2
III	138	10.1
IV	2	0.1
Pathology
Clear cell RCC	1107	80.9
Papillary RCC	97	7.1
Chromophobe RCC	83	6.1
Other RCC	57	4.2
Epithelioid AML	18	1.3
Sarcomas	6	0.4
R.E.N.A.L complexity
Low	258	18.9
Intermediate	749	54.8
High	361	26.4

Kaplan-meier Analyses Of Each Parameter In Renal Nephrometry Score

We first analyzed the associations between each components of RNS and survival outcomes based on Kaplan-Meier analyses and log rank tests. For R score, tumor lager than 7cm (R = 3) predicted worse OS compared with tumors less than 4cm (R = 1) (p < 0.001) or tumors between 4cm and 7cm (R = 2) (p < 0.001) (A). For E score, entirely endophytic tumors (E = 3) showed better survival outcomes than tumors with exophytic properties > 50% (E = 1) (p = 0.009) (Fig. 1B). For parameter A, we found that tumors grew from the tips of the renal poles or arises from the kidney (x) correlated with shorter OS compared with anterior tumors (a) (p < 0.001) or posterior tumors (p) (p = 0.004) (Fig. 1D). For L score, patients with L = 3 tumors had poorer OS than L = 1 (p = 0.006) or L = 2 (p = 0.05) tumors (Fig. 1E). N and h parameter did not show statistical correlation with OS in Zhongshan cohort (Fig. 1C, Fig. 1F). We observed similar trend in analyses of recurrence free survival, except that N (p < 0.001) and h (p = 0.034) parameters reached statistical significance in RFS. Tumors with nearness of the tumor to the collecting system or sinus ≤ 4mm (N = 3) had a more dismal survival compared with tumors with nearness > 4 but < 7 (N = 2) (p = 0.095) and nearness ≥ 7 (N = 1) (p < 0.001) (Figure S1C). Patients with non-hilar tumors had longer RFS than patients with hilar tumors (p = 0.034) (Figure S1F). In short, we found that both OS rates and RFS rates were significantly stratified by R, E, A and L components of RNS (Fig. 1, Figure S1).

Correlation Between Renal Nephrometry Score Sum And Oncologic Outcomes

We then explored whether R.E.N.A.L. complexity group associated oncologic outcomes in patients with renal tumors. Kaplan-Meier curves of both the OS rate and RFS rate were significantly different when stratified by R.E.N.A.L. complexity group (OS, p < 0.001, RFS, p < 0.001) (Fig. 2). Patients with high complexity tumors had the worst OS and RFS in comparison with low (OS: p < 0.001, RFS: p < 0.001) or intermediate (OS: p = 0.001, RFS: p < 0.001) complexity tumors. A significant survival benefit was observed in low complexity tumors versus intermediate complexity tumors in terms of RFS (p = 0.014, Fig. 2B) but not OS (p = 0.135, Fig. 2A). We further explored the prognostic value of RNS as continuous variable, and found that after adjusting for tumor stage and grade, RNS remained an independent

adverse risk factor for both OS [p = 0.027, HR(95%CI) = 1.151 (1.016–1.303)] and RFS [p < 0.001, HR(95%CI) = 1.299 (1.125–1.501)] (Table 2).

Table 2

Multivariate cox regression analyses of survival based on R.E.N.A.L. nephrometry score
Variables	Overall survival		Recurrence-free survival
Variables	HR (95%CI)	P-value†	HR (95%CI)	P-value†
TNM stage		< 0.001		< 0.001
I	Reference		Reference
II	1.677 (0.888–3.167)	0.111	1.730 (0.862–3.470)	0.123
III	3.696 (2.440–5.598)	< 0.001	5.605 (3.703–8.485)	< 0.001
IV	9.080 (2.099–39.280)	0.003	8.885 (2.085–37.870)	0.003
ISUP grade		< 0.001		< 0.001
1	Reference		Reference
2	1.203 (0.485–2.985)	0.690	1.555 (0.486–4.978)	0.451
3	3.070 (1.210–7.789)	0.018	4.929 (1.529–15.885)	0.008
4	10.274 (3.353–31.484)	< 0.001	10.166 (2.661–38.834)	0.001
RNS	1.151 (1.016–1.303)	0.027	1.299 (1.125–1.501)	< 0.001
RNS = R.E.N.A.L. nephrometry score ; HR = hazard ratio; CI = confidence interval; OS = overall survival; RFS = recurrence free survival; †Data obtained from the Cox proportional hazards model, P-value < 0.05 was regarded as statistically significant

Survival Analyses Of Radical Versus Partial Nephrectomy Stratified By Renla Nephrometry Score

Kaplan-Meier analyses revealed that patients who received partial nephrectomy had better overall survival compared with patients who received radical nephrectomy in all complexity subgroups, but reached statistical significance in intermediate complexity tumors only (low complexity: p = 0.095, Fig. 3A; intermediate complexity: p = 0.001, Fig. 3B; high complexity: p = 0.130, Fig. 3C). Although we analyzed the survival difference between two surgical approaches in the same complexity group, partial or radical nephrectomy may still correlated with different levels of complexity. The survival benefit may result from different complexity. Thus we analyzed the RNS score for partial and radical nephrectomy, and found that in intermediate complexity group, RNS for radical nephrectomy was significantly higher than RNS for partial nephrectomy (p < 0.001, Fig. 3D). To avoid the bias caused by different level of RNS, we next compared the survival outcomes between the two types of surgeries in each RNS subgroup. We found that partial nephrectomy associated with prolonged overall survival in RNS = 4 or 5 renal tumors with statistical significance (R = 4, p = 0.025; R = 5, p = 0.023, Fig. 3E). When RNS = 7 ~ 9, partial nephrectomy showed borderline significant OS benefit compared with radical nephrectomy (RNS = 7, p = 0.081; RNS = 8, p = 0.059; RNS = 9, p = 0.095, Fig. 3E). When RNS = 10 ~ 12, no differences in survival were observed (RNS = 10, p = 0.401; RNS = 11, p = 0.152; RNS = 12, p = 0.564, Fig. 3E).

The Radius-Exophytic/Endophytic-Nearness-Anterior/Posterior-Location R.E.N.A.L. nephrometry score proposed by Kutikov et al. with the aim to facilitate preoperative planning and surgical decision making[6]. Surgical approach selection between radical nephrectomy and partial nephrectomy for localized RCC are influenced profoundly by anatomical features of renal tumors. Previous studies have proved that RNS is an independent predictor of warm ischemia time[17], perioperative complications[5], conversion to radical nephrectomy[18], pelvicalyceal system entry/repair[19], urine leak[20] and postoperative repair function[21].

Interestingly, researchers also found that RNS correlates with tumor aggressiveness. Kutikov and colleagues postulated the predictive value of RNS for tumor grade. The authors revealed that R score, E score and L score were predictors of high-grade histology and construct a nomogram evaluating renal mass being high-grade based on sex, R score, E score, N score, L score and H score [5]. The nomogram was externally validated in two independent cohorts of 391 Chinses patients and 1129 Korean patients, with AUC of 0.73 and 0.574 respectively [10, 22]. In an Australian cohort of 111 patients, Prassannah et al further confirmed the correlation between high RNS and an increased risk of clear cell histology, stage ≥ pT3 and grade 4 tumors [11]. In addition, Michael et al identified high RNS was a preoperative risk factor associated with cT1 to pT3a tumor upstaging. Patients with pT3a tumors had worse recurrence-free survival in this study, in accordance with higher stage designation for tumors invading perinephric, pelvic fat or renal vein [23].

These findings suggested more aggressive biological behavior for RCCs with higher RNS score, while whether such aggressive nature finally translated to a more dismal prognosis remains unclear, with few studies of very limited number of patients who had received curative nephrectomy enrolled. Previous studies only focused on specific subgroups of patients, such as cT2 and pT1b-2b renal tumors [13, 14]. In a study of 202 cT2 patients, patients with RNS scores > 10 were more likely to die from the disease or any cause[11]. Akira and colleagues found that RNS sum was independent predictors of postoperative recurrence in 91 patients with pT1b-2b RCC who underwent radical nephrectomy [13].

Herein, we found that component R (Radius), E (exophytic), A (anterior), L (location) were all associated with both OS and RFS. N (nearness) and suffix “h” (Hilar) correlated with RFS with statistical significance only. Radius refers to tumor size, a well-established adverse risk factor for prognosis [24]. In our study, we also found that R score adversely associated with prognosis. The total score of RNS as continuous variable correlated to both RFS and OS in Zhongshan cohort, which was in accordance with previous studies. Multivariate regression analyses confirmed the role of RNS sum as an independent adverse risk factor for prognosis, indicating that anatomic features can be used as an easily obtainable complementary markers for prognosis prediction in addition to tumor stage and grade. On the other hand, Akira et al. did not find the associations between parameters of E, N and A in a cohort of 91 patients [13]. The limited sample size may explain the different results compared with Zhongshan cohort, in which 1368 patients were analyzed. Kaplan-Meier analyses revealed that RNS risk group stratified patients with different OS and RFS. In RNS = 4 and RNS = 5 tumors, partial nephrectomy showed significantly longer OS and demonstrated survival benefit in RNS = 7, RNS = 8 and RNS = 9 tumors with borderline statistical significance compared with radical nephrectomy. Our findings may also provide more evidence for treatment selection. When surgically feasible, in terms of long term survival outcomes, partial nephrectomy was more likely to be a better choice.

This study is not deprived of limitations. First, the RNS was assigned by three different urologists which may lead to potential bias. The reproducibility among urologists and radiologists were not very good either. Second, we enrolled patients from a very long time range, surgical approaches and survival outcomes may be influenced by the date when the surgery was performed. In earlier years, due to limitations of surgical techniques, physicians tend to choose radical nephrectomy more. Third, the findings need to be validated prospectively and externally in the future.

In conclusion, we demonstrated the associations between patient survival and parameters/sum of RNS in a large cohort. We found for the first time that all components R, E N, A, L and H of RNS were significantly associated with oncologic outcomes. RNS sum was an independent adverse risk factor for RF and OS as continuous variables. Patients in different RNS complexity group had varied survival outcomes. Partial nephrectomy correlated with longer OS compared with radical nephrectomy in RNS = 4 and RNS = 5 tumors.

Ethics approval and consent to participate:

The study was approved by the ethic committee of Zhongshan Hospital with the approval number of B2021-608R. All methods were carried out in accordance with relevant guidelines and regulations. Informed consent was obtained from each patient.

Consent for publication:

All authors have read the manuscript and give consent to publication. No identifying information is present. Consent for publication on part of participants was not applicable.

Availability of data and materials:

The datasets generated and/or analysed during the current study are not publicly available because the hospital did not authorize us to do so but are available from the corresponding author on reasonable request.

Conflict of interest

The authors declare no conflict of interest.

Funding

This work was supported by grants from National Natural Science Foundation of China (81902563), Zhongshan Hospital Science Foundation (2020ZSXMYS17, 2021ZSQ15), Medical Project of Xiamen (3502Z20214ZD1080) and Shanghai Sailing Program (19YF1408000). All these study sponsors have no roles in the study design, in the collection, analysis, and in the interpretation of data.

Author contributions

X. Zhang, J. Lin, Y. Qi and Y. Xiong for acquisition of data, analysis and interpretation of data, statistical analysis and drafting of the manuscript; W. Xi and Y. Qi for technical and material support; X. Li, C. Miao, X. Quan and Q. Sun for study concept and design, analysis and interpretation of data, drafting of the manuscript, obtained funding and study supervision. All authors read and approved the final manuscript.

Acknowledgements

Not applicable.

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No competing interests reported.

FigureS1.tif
Figure S1: Kaplan-Meier analyses of recurrence-free survival according to R.E.N.A.L. nephrometry score parameters A. Kaplan-Meier analysis of RFS based on R score B. Kaplan-Meier analysis of RFS based on E score C. Kaplan-Meier analysis of RFS based on N score D. Kaplan-Meier analysis of RFS based on A parameter E. Kaplan-Meier analysis of RFS based on L score F. Kaplan-Meier analysis of RFS based on h suffix

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Version 1

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You are reading this latest preprint version

Associations between R.E.N.A.L nephrometry score and survival outcomes in renal tumors

Status:

Version 1

Abstract

Objective

Materials and methods

Results

Conclusion

Figures

Introduction

Materials And Methods

Patient selection:

Date Collection

Statistical Analyses

Results

Baseline characteristics of patients in Zhongshan cohort

Kaplan-meier Analyses Of Each Parameter In Renal Nephrometry Score

Correlation Between Renal Nephrometry Score Sum And Oncologic Outcomes

Survival Analyses Of Radical Versus Partial Nephrectomy Stratified By Renla Nephrometry Score

Discussion

Declarations

References

Additional Declarations

Supplementary Files

Status:

Version 1