Zéro ischémie, la préservation parenchymateuse et l’âge sont les facteurs prédictifs de la fonction rénale après néphrectomie partielle

25 janvier 2020

Auteurs : L. Mutelica, P. Mouracadé, O. Kara, J. Dagenais, M.J. Maurice, J.H. Kaouk
Référence : Prog Urol, 2020, 1, 30, 3-11



Preoperative glomerular filtration rate, solitary kidney, age, gender, tumor size, ischemia time [1], were considered as predictors of glomerular filtration rate after partial nephrectomy (PN). A number of recent studies have found that the quality and quantity of remnant renal parenchyma after PN assume an important role in predicting future renal function.

Although preoperative evaluation and timely consultation with a nephrologist, helps optimize renal function after PN, ischemia time and parenchymal preservation are the single modifiable surgical risk factors for decreased renal function. Efforts to limit ischemic time and the extent of healthy tissue excision should be pursued when doing PN.

Minimization or reducing On-Clamp time during PN has led to alternative technical modifications [1, 2]. The concept of Off-Clamp PN which aims to avoid the ischemic injury on the healthy parenchyma of the operated kidneys has been described in the literature for open [3, 4, 5], laparoscopic, and robot assisted [2, 6, 7, 8] partial nephrectomy.

Ideally, we would like to evaluate the perioperative morbidity and functional outcome of Off-Clamp in comparison to On-Clamp, in order to assess the burden of PN and the extent of renal function preservation in this setting. Several studies tried to compare the 2 different techniques but most of these studies lack robust conclusion -no differentiation between open and laparoscopic surgery [3]. Lack of information about tumor size [6], tumor complexity [5], excisional volume loss, parenchymal preservation or late postoperative renal function [9]. Significant differences in tumor size between the groups [9] making the comparison inappropriate.

The aim of the present study was to compare, perioperative morbidity and functional outcomes of Off-Clamp, to On-Clamp approach, during robot-assisted partial nephrectomy (RAPN) in a matched groups.

Materiel and methods

Study population

We retrospectively reviewed our institutional review board-approved PN database. Data consisted of consecutive records of patients who underwent robot assisted partial nephrectomy by 8 senior surgeons in the same center between 2007 and 2015 for cT1a tumors using On-Clamp or Off-Clamp approaches. Patients with solitary kidney or multifocal tumors were excluded. Overall 940 patients were included in this study. Of this cohort, 103 patients underwent Off- Clamp approach and 837 patients underwent On-Clamp approach.

In order to reduce differences between groups due to selection bias and confounding, we performed a matched analysis using the propensity score method with a greedy matching algorithm. At all, 309 patients from the On-Clamp were matched to the 103 patients from Off- Clamp group.

Surgical technique

All RAPN procedures were performed with the da Vinci Surgical System (Intuitive Surgical, Inc., Sunnyvale, CA, USA). The renal artery was routinely localized and dissected and left unclamped in the off-clamp group and clamped in the on-clamp group. Warm Ischemia time (WIT) was defined as the time from the clamping till unclamping. No cold ischmia was used. Tumor excision was performed with parenchymal margin resection. After tumor resection, an inner parenchymal layer sutured reconstruction was performed, followed by capsular sutures for approximation of the renal defect.

Data collection

Patient demographics (age, gender, race, body mass index [BMI], Charlson comorbidity index [CCI], American Society of Anesthesiologists score [ASA], baseline estimated glomerular filtration rate [e-GFR], baseline CKD stage), and clinical tumor characteristics (R.E.N.A.L. nephrometry score: consists of [R]adius [tumor size as maximal diameter], [E]xophytic/endophytic properties of the tumour, [N]earness of tumor deepest portion to the collecting system or sinus, [A]nterior [a]/posterior [p] descriptor and the [L]ocation relative to the polar line, radiological maximum tumor diameter, hilar (h) location, laterality, malignancy, American Joint Cancer Committee staging and tumor grade) were collected.

Propensity score matching

We matched the 2 groups in terms of preoperative factors: Tumor size, Charlson comorbidity index, and R.E.N.A.L score, factors considered to be related to the decision concerning the surgical approach (On-Clamp vs. Off-Clamp). The nearest neighbor matching was used, meaning that Off-Clamp patients were matched to On-Clamp patients who have the most similar estimated propensity score. To ensure good matches, a caliper (maximum allowable difference between two patients) of 0.1 was defined. Because the sample sizes of On-Clamp and Off-Clamp groups vary greatly, 1 to 3 matching was performed in which a single Off-Clamp patient was matched to 3 On-Clamp patients [10]. Matching was done with replacement, in which a patient in the On-Clamp group had been reused to be matched to more than one patient in the Off-Clamp group, this reduces the overall imbalance between the two groups.

Primary endpoints

Our primary outcomes were decline in e-GFR [e-GFR], e-GFR preservation, and CKD upstaging. The e-GFR was calculated according to MDRD formula. Decline in e-GFR was defined as the difference between postoperative e-GFR (measured at 6 months) and baseline e- GFR. e-GFR preservation was defined as postoperative e-GFR divided by baseline e-GFR, expressed as a percentage. The CKD was defined according to the Kidney Disease Outcome Quality Initiative-Chronic Kidney Disease with stages 1, 2, 3, 4 and 5 corresponding to an e- GFR >90, 60-89, 30-59, 15-29 and <15 respectively [11].

Secondary endpoints

Secondary outcomes included, operative time, estimated blood loss [EBL], transfusion rate, postoperative Clavien complications, surgical reoperation, 30-day readmission, surgical margin status and excisional volume loss. The excisional volume loss was calculated as previously described [12]. The volume of healthy rim of renal parenchyma removed at the time of RAPN was estimated by deducting the calculated tumor volume, from the PN specimen volume. The tumor volume was measured using the ellipsoid formula: (0.523x'y'z' ), where x' , y' and z' where the three dimensions of the tumor measured on pathology assessment. The volume of PN specimen was also measured using the ellipsoid formula (0.523xyz ) [12], where x , y and z where the three dimensions of the specimen measured on pathology assessment.

Statistical analysis

Continuous variable were described as median and interquartile range. Categorical variables were described as frequency and percentage. The nonparametric Mann-Whitney U -test and the &khgr;2 test were used for comparing the continuous and categorical variables between the On- Clamp and Off-Clamp groups. Linear multiple regression was used to identify independent predictors of e-GFR decline. Variable inclusion in the multivariable model was decided using stepwise regression. Logistic regression was used to identify independent predictors of CKD upstaging. Variables with P <0.2 on Univariate analysis were introduced in the logistic multivariate model. Statistical significance was set at p<0.05. Analysis was performed using SPSS v22 software. (IBM SPSS Statistics, Armonk, NY: IBM Corp., USA). The R software and plug-in that link with the corresponding version of SPSS and propensity score matching package were installed. A propensity score module was added in the SPSS interface.


Patient demographics and tumor characteristics between the two groups were compared before matching. The Off-Clamp group had higher comorbidity burden (CCI>1, 45.6% vs. 30.1%, P <0.01), lower tumor size (median 2.0 vs. 2.5cm, P <0.01) and lower tumor complexity (R.E.N.A.L score, P <0.01). There were no difference in gender (p=0.5), age (P =0.1), race (P =0.2), BMI subclasses (P =0.9), ASA score (P =0.2) and baseline e-GFR (P =0.3), (Table 1).

After matching we found that there were no difference in gender (P =0.80, age (P =0.2), race (P =0.6), BMI subclass (P =0.9), CCI index (P =0.2), ASA score (P =0.3) and baseline e-GFR (P =0.2) between the two matched groups. The baseline patient characteristics for On-Clamp and Off-Clamp groups after matching shows in the Table 2.

Also, the characteristics of the Off-Clamp and On-Clamp tumors were compared after matching. There were no difference in tumor size (median, 2.0 vs. 2.0cm, p=0.3), laterality (P =0.1), R.E.N.A.L score (P =0.1), hilar (h) location (P =0.5) and pT stage (P =0.8) between the 2 matched groups (Table 3).

The outcome measures regarding secondary endpoints were compared for Off-Clamp and On-Clamp groups. No difference found in operative time (median 172 vs. 170min, P =0.4), EBL (median 100 vs. 120ml, P =0.3), transfusion rate (5.2% vs. 10.7%, P =0.051), overall postoperative complications (17.7% vs. 22.3%, P =0.3), Clavien grade (III-IV) complications (5.5% vs. 4.8%, P =0.8), surgical reoperation (1.6% vs. 1.9%, p=1), 30-day readmission rate (4.5% vs. 3.9%, P =1), and positive surgical margins (5.5% vs. 5.8%, P =0.9) between the matched groups respectively. The excisional volume loss (median, 9.08 vs. 4.51 cm3, P <0.01) was significantly different in favor of Off-Clamp group. Regarding primary endpoints, e-GFR decline (median, −9.7 vs. −2.2ml/min/1.73m2, P <0.01), percent of e-GFR preservation (median, 87 vs. 97 percent, P <0.01), and CKD upstaging (36.5% vs. 23.3%, P =0.01) were significantly different in favor of Off-Clamp group (Table 4).

Using the linear regression model, the three predictive variables for preserving kidney function were identified. Ischemia type (P =0.01), excisional volume loss (P =0.01), and age (P =0.02),) were significant predictors of e-GFR preservation (Table 5).

The single predictor factor of upstaging was excisional volume loss (OR 1.035, CI 95% [1.015-1.06] P <0.01). Ischemia type (P =0.12), tumor size (P =0.16) and age (P =0.3) were not. The logistic regression model predicting CKD upstaging shows in the Table 6.


The potential renal functional benefit of Off-Clamp compared with renal arterial clamping remains difficult to assess, especially in retrospective comparisons. Omitting to take into consideration confounding factors and explanatory variables (preoperative glomerular filtration rate, solitary kidney, multiple tumors, age, gender, tumor size, R.E.N.A.L score, the quantity of remnant renal parenchyma) may contribute to miss the real conclusion. In order to reduce any difference between groups we excluded solitary kidney, and multiple tumor resection from our study population. Patients with solitary kidney have a lower baseline e-GFR [13] and multiple tumor excision may have higher postoperative complication rate [14]. The propensity score analysis was developed to minimize the differences in patients' covariates, which could become confounding factors in the examination of treatment effects in observational studies.

The propensity score is defined as the patient's probability for treatment selection, which is dependent on observed baseline covariates. We identify all preoperative factors that were related to the selection of On-Clamp or Off-Clamp. While age, race, BMI, ASA, laterality were not affecting the surgeon decision to select On-Clamp or Off Clamp approach, we matched on tumor size, R.E.N.A.L score and Charlson comorbidity index, factors considered as related to the selection of On-Clamp or Off-Clamp: large tumor size in one group may result in less functional kidney present following surgery by requiring an incrementally larger resection volume of adjacent normal kidney to ensure complete excision. In addition, studies using the anatomic classification nephrometry system have shown a strong correlation among higher surgical complexity of renal tumors, longer WIT, and poorer functional outcomes [15], [16, 17, 18]. Regarding perioperative outcomes, our findings were consistent with others series comparing Off-clamp to On-clamp PN in selecting cases [19]. There were no differences between groups in terms of operative time, EBL, and complication rate, with Off-Clamp PN showing a trend toward a higher transfusion rates (P =0.051).

Parenchymal volume loss is believed to occur mainly from excisional volume loss, especially in small renal tumors (loss of healthy parenchyma in the margin) [13]. Our findings support those of other authors who also reported data attesting to significantly less parenchymal loss during Off-Clamp compared with On-Clamp PN [20, 21]. We believe that in Off- Clamp approach, there is a tendency to limit parenchymal resection in order to reduce bleeding (minimal margin resection), though less volume excision did not affect the positive surgical margin in our series. This finding is consistent with the literature [2, 22].

Regarding renal function preservation, the relative importance of ischemia type is still debatable. In a multi-institutional study of 886 robot-assisted PN cases, Kaczmarek et al. [6] performed an analysis involving propensity score matching between 49 patients who underwent Off-Clamp and 283 who underwent On-Clamp PN. The Off-Clamp group had significantly higher renal function preservation at last follow-up compared with On-Clamp (e-GFR 2% vs. -6%, P =0.008).

This study had several limitations. One of these limitations was the absence of information on parenchymal volume preservation. A retrospective comparison of superselective clamping PN and On-Clamp PN by Desai et al. [22] showed that superselective clamping PN was associated with a lower decrease in e-GFR (P =0.03). Porpiglia et al. [7] evaluate postoperative renal function after On-Clamp (WIT<25min) and Off-Clamp PN. Postoperative functional parameters at 3 months after surgery were similar in the two groups.

In our study, the Off-Clamp group had a better renal function preservation in comparison to On-Clamp group, though the median ischemia time in the On-Clamp group was less than 20min (acceptable threshold for WIT). This advantage on e-GFR preservation was not only related to Off-Clamp approach. Indeed, the trend to resect less parenchyma during Off-Clamp partial nephrectomy explains part of the renal function preservation in Off-Clamp group as shown by the multivariate analysis.

Our multivariate analysis showed that ischemia type, volume loss, and age were predictors of renal function preservation. These results validated that parenchymal preservation, and no ischemia technique are the most important determinants of renal function after PN.

Our study validates previous publications reporting the feasibility of RAPN Off-Clamp approach in selected patients with acceptable morbidity in comparison to On-Clamp approach. Identifying the relative benefits and risks associated with Off-Clamp can help with appropriate selection of patients for this approach.

We acknowledge some limitations in our study; most are inherent problems of retrospective studies, even though data were collected prospectively by chart review, on the basis of a predetermined registration grid. Propensity score (PS) analyses have the limitation that remaining unmeasured confounding may still be present. In addition, matching using the PS do not overcome initial selection bias.


RAPN for selected renal mass using Off-Clamp approach offered renal functional advantage over On-Clamp, without adding morbidities. While no ischemia technique was associated with less excisional volume loss then On-Clamp; excisional volume loss, Off-Clamp approach, and age were independent predictors of renal function preservation. Clinical significance of these findings in various clinical settings will require further investigation.

Disclosure of interest

The authors declare that they have no competing interest.

Table 1 - Baseline characteristics for patients in the study group.
Variable  On-clamp  Off-clamp  P  
N (%)  837 (100%)  103 (100%)   
Gender n (%)      0,5 
Male  490 (58,5)  57 (55,3%)   
Female  347 (41,5)  46 (44,7)   
Age (year)      0,1 
Median [IQR]  59 [51-67]  63 [53-69]   
Race n (%)      0,2 
White  734 (87,7)  86 (83,5)   
Other  103 (12,3)  17 (16,5)   
BMI (kg/m2) n (%)      0,9 
[<25]  153 (18,3)  21 (20,4)   
[25-29,9]  304 (36,3)  35 (34,0)   
[30-34,9]  210 (25,1)  25 (24,3)   
[>35]  170 (20,3)  22 (21,4)   
CC index n (%)      <0,01 
CC index <= 585 (69,9)  56 (54,4)   
CC index> 252 (30,1)  47 (45,6)   
ASA score n (%)      0,2 
ASA<= 287 (34,3)  28 (27,2)   
ASA> 550 (65,7)  75 (72,8)   
Baseline e-GFR ml/min      0,3 
Median [IQR]  82 [69-99]  83 [64-94]   
Tumor size (cm)      <0,01 
Median [IQR]  2,5 [2,0-3,1]  2,0 [1,4-2,5]   
Side n (%)      0,1 
Left  414 (49,4)  59 (57,3)   
Right  423 (50,6)  44 (42,7)   
R.E.N.A.L. score      <0,01 
< 327 (39,1)  78 (75,7)   
>= 510 (60,9)  25 (24,3)   
Location: Hilar (h) n (%)      0,3 
Yes  111 (13,3)  10 (9,7)   
No  726 (86,7)  93 (90,3)   

Légende :
CC index: Charlson Comorbidities Index; ASA score: American Society of anesthesiologists score; BMI: Body mass index; e-GFR: estimated glomerular filtration rate definite by the Modification of Diet in Renal Disease (MDRD); R.E.N.A.L. nephrometry score consist of radius (R) (tumor size as maximal diameter), exophytic/endophytic (E) properties of the tumor, nearness (N) of tumor deepest portion to the collector system or sinus, anterior (A)/posterior (a/p) descriptor and the location(L) relative to the polar line.

Table 2 - Baseline characteristics for patients in the matched group.
Variable  On-clamp  Off-clamp  P  
N (%)  309 (100%)  103 (100%)   
Gender n (%)      0,8 
Male  174 (58,0)  57 (55,3)   
Female  135 (42,0)  46 (44,7)   
Age (year)      0,2 
Median [IQR]  60 [52-67]  63 [53-69]   
Race n (%)      0,6 
White  264 (85,4)  86 (83,5)   
Other  45 (14,6)  17 (16,5)   
BMI (kg/m2) n (%)      0,9 
[<25]  58 (18,8)  21 (20,4)   
[25-29,9]  115 (37,2)  35 (34,0)   
[30-34,9]  72 (23,3)  25 (24,3)   
[>35]  64 (20,7)  22 (21,4)   
CC index n (%)      0,2 
CC index <=  193 (62,5)  56 (54,4)   
CC index> 116 (37,5)  47 (45,6)   
ASA score n (%)      0,3 
ASA<= 99 (32,0)  28 (27,2)   
ASA> 210 (68,0)  75 (72,8)   
Baseline e-GFR ml/min      0,2 
Median [IQR]  84 [69-98]  83 [64-94]   

Légende :
CC index: Charlson Comorbidities Index; ASA score: American Society of anesthesiologists score; BMI: Body mass index; e-GFR: estimated glomerular filtration rate definite by the Modification of Diet in Renal Disease (MDRD). Continuous variable was described as median and interquartile range. Categorical variables were described as number and frequency. Mann-Whitney U-test was used for continuous and chi-squared test was used for categorical variables All test used 5% as a significant threshold.

Table 3 - Tumor's characteristics for patients in the matched groups.
Variable  On-clamp  Off-clamp  P  
N (%)  309 (100%)  103 (100%)   
Tumor size (cm)      0,3 
Median [IQR]  2,0 [1,5-2,5]  2,0 [1,4-2,5]   
Side n (%)      0,1 
Left  149 (48,2)  59 (57,3)   
Right  160 (51,8)  44 (42,7)   
R.E.N.A.L. score      0,3 
<7  216 (69,9)  78 (75,7)   
>= 93 (30,1)  25 (24,3)   
Location: Hilar (h) n (%)      0,5 
Yes  37 (12)  10 (9,7)   
No  272 (88)  93 (90,3)   
Tumor histology n (%)      0,03 
Clear cell  159 (51,5)  34 (33,0)   
Papilary  59 (19,1)  27 (26,2)   
Chromophobe  11 (3,6)  4 (3,9)   
Other malignant  18 (5,8)  8 (7,8)   
Benign  62 (20,1)  30 (29,1)   
pT stage n (%)      0,8 
pT1a  230 (74,4)  69 (67)   
pT3a  17 (5,5)  4 (3,9)   
Grade n (%)      0,9 
Low (I-II)  141 (45,6)  38 (36,9)   
High (III-IV)  78 (25,3)  23 (22,3)   
NCa  90 (29,1)  42 (40,8)   

Légende :
R.E.N.A.L. nephrometry score consist of radius (R) (tumor size as maximal diameter), exophytic/endophytic (E) properties of the tumor, nearness (N) of tumor deepest portion to the collector system or sinus, anterior (A)/posterior (a/p) descriptor and the location(L) relative to the polar line. Continuous variable was described as median and interquartile range. Categorical variables were described as number and frequency. Mann-Whitney U-test was used for continuous and Chi2 test was used for categorical variables All test used 5% as a significant threshold.

NC: Not Concerned (benign tumors, chromophobe tumors, unclassified).

Table 4 - Outcomes variables in the matched groups.
Variable  On-Clamp  Off-Clamp 
N (%)  309 (100%)  103 (100%)   
Operation time (min)      0,4 
Median [IQR]  172 [126-208]  170 [118-200]   
Warm ischemia time (min)       
Median [IQR]  19 [14-23]  NC   
EBL (ml)      0,28 
Median [IQR]  100 [50-200)]  120 [50-300]   
Margin status n (%)      0,9 
Positive  17 (5,5)  6 (5,8)   
Negative  292 (94,5)  97 (94,2)   
Excisional volume (cm3 7,08 [3,59-12,9]  3,5 [1-5,5,6]  <0,01 
Surgeon assessment of volume preservation (%)       
Median [IQR]  95 [86-95]  95 [89-95]  0,9 
Postoperative renal scan (relative function %)       
Median [IQR]       
Right  48,3 [41-57]  48,7 [44-55,3]  0,9 
Transfusion n (%)  16 (5,2)  11 (10,7)  0,051 
G 3-5 postoperative complications n (%)  17 (5,5)  5 (4,8)  0,8 
Overall postoperative complications n (%)  55 (17,7)  23 (22,3)  0,3 
Surgical Reoperation n (%)  5 (1,6)  2 (1,9) 
30-day Readmission n (%)  14 (4,5)  4 (3,9) 
Postoperative e-GFR (ml/min)      0,6 
Median [IQR]  73 [58-87]  74 [57-90]   
Delta e-GFR (ml/min)       
Median [IQR]  −9,7 [-19-0,05]  −2,2 [-12-0,0]  <0,01 
e-GFR preservation       
Median [IQR]  87 [76-100]  97 [83-100]  <0,01 
CKD upstaging  113 (36,5%)  24 (23,3%)  0,01 

Légende :
EBL: Estimated Blood loss; Delta e-GFR: postoperative e-GFR- baseline e-GFR; e-GFR: estimated glomerular filtration rate definite by the Modification of Diet in Renal Disease (MDRD). E-GFR preservation was defined as postoperative e-GFR divided by baseline e-GFR. The CKD was defined according to the Kidney Disease Outcome Quality Initiative-Chronic Kidney Disease with stages 1,2,3,4 and 5 corresponding to an e-GFR>=90, 60-89,30-59,15-30 and <15ml/min respectively.

Table 5 - Multiple linear regression predicting the e-GFR preservation rate.
  e-GFR preservation 
Variables  Coefficient (SE)  P  
Age (per 1 year)  −0,154 (0,065)  0,02 
Baseline e-GFR (per 1ml/min/1,73M2)  −0,05 (0,032)  0,09 
Ischemia type (Zero=0, Warm=1)  −4,2 (1,7)  0,011 
Excisional volume loss (per 1 cm3 −0,14 (0,06)  0,015 
F ratio=29
P <0,01
Adjusted R squared=22%
Multicollinearity tested: correlation matrix-Tolerance-Variance inflation factor 

Légende :
The dependent variable (e-GFR preservation rate) is a continuous variable. A linear regression model was used to predict this variable. The overall F-test determines whether the relationship is statistically significant. In this model, the p of the overall F-test was <0,05. We conclude that the R-squared value is significantly different from zero. R-squared provides an estimate of the strength of the relationship between the model and the response variable.

Table 6 - shows the logistic regression model predicting CKD upstaging.
  CKD upstaging 
Variables  OR (95%CI)  P  
Age (years)  1,01 [0,99-1,030]  0,3 
Tumor size (cm)  1,22 [0,92-1,61]  0,16 
Ischemia type (Zero=0, Warm=1)  0,652 [0,4-1,2]  0,12 
Excisional volume loss (per 1cm3)  1,035 [1,15]  <0,01 

Légende :
OR: Odd ratio; CI Confidence interval.


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