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European Urology
Volume 58, issue 3, pages e29-e38, September 2010Kidney Cancer
Every Minute Counts When the Renal Hilum Is Clamped During Partial Nephrectomy
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R. Houston Thompson a 
1 
, Brian R. Lane b 1, Christine M. Lohse a, Bradley C. Leibovich a, Amr Fergany b, Igor Frank a, Inderbir S. Gill c, Michael L. Blute a and Steven C. Campbell b
Accepted 31 May 2010, Published online 9 June 2010, pages 340 - 345
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Abstract
Background
The safe duration of warm ischemia during partial nephrectomy remains controversial.
Objective
Our aim was to evaluate the short- and long-term renal effects of warm ischemia in patients with a solitary kidney.
Design, setting, and participants
Using the Cleveland Clinic and Mayo Clinic databases, we identified 362 patients with a solitary kidney who underwent open (n = 319) or laparoscopic (n = 43) partial nephrectomy using warm ischemia with hilar clamping.
Measurements
Associations of warm ischemia time with renal function were evaluated using logistic or Cox regression models first as a continuous variable and then in 5-min increments.
Results and limitations
Median tumor size was 3.4 cm (range: 0.7–18.0 cm), and median ischemia time was 21 min (range: 4–55 min). Postoperative acute renal failure (ARF) occurred in 70 patients (19%) including 58 (16%) who had a glomerular filtration rate (GFR) <15 ml/min per 1.73 m2 within 30 d of surgery. Among the 226 patients with a preoperative GFR ≥ 30 ml/min per 1.73 m2 and followed ≥30 d, 38 (17%) developed new-onset stage IV chronic kidney disease during follow-up. As a continuous variable, longer warm ischemia time was associated with ARF (odds ratio: 1.05 for each 1-min increase; p < 0.001) and a GFR < 15 (odds ratio: 1.06; p < 0.001) in the postoperative period, and it was associated with new-onset stage IV chronic kidney disease (hazard ratio: 1.06; p < 0.001) during follow-up. Similar results were obtained adjusting for preoperative GFR, tumor size, and type of partial nephrectomy in a multivariable analysis. Evaluating warm ischemia in 5-min increments, a cut point of 25 min provided the best distinction between patients with and without all three of the previously mentioned end points. Limitations include the retrospective nature of the study.
Conclusions
Longer warm ischemia time is associated with short- and long-term renal consequences. These results suggest that every minute counts when the renal hilum is clamped.
Keywords: Ischemia, Kidney neoplasms, Postoperative complications, Nephrectomy, Warm ischemia.
Article Outline
1. Introduction
Interruption of renal blood flow via pedicle clamping is often necessary during partial nephrectomy, especially for hilar tumors or those with deep parenchymal invasion. Vascular clamping aids in hemostasis and allows precise surgical closure of the collecting system and reapproximation of the parenchymal defect. However, the most important factor governing the return of renal function remains the duration of ischemia time. The historically safe duration of warm ischemia time, where full recovery of renal function is expected, was commonly thought to be 30 min [1] and [2]. More recently, we have observed that warm ischemia should be limited to 20 min whenever feasible [3], [4], and [5], a notion that was recently supported by an international collaborative review of the literature [6].
Others have challenged the maximal safe duration of warm ischemia, suggesting that renal pedicle clamping for 90 min is safe in the porcine model [7] and [8]. Furthermore, clinical observations have suggested that warm ischemia for 40–55 min is safe and effective [9] and [10]. However, these studies included patients with normal contralateral kidneys, potentially masking the effects of ischemia on a solitary renal unit because serum creatinine and estimated glomerular filtration rate (GFR; which relies on serum creatinine) were used to assess renal function. In the largest study evaluating the effects of warm ischemia in 174 patients with a solitary kidney, we previously reported that warm ischemia >20 min was associated with an increased risk of acute renal failure (ARF) and chronic renal insufficiency (defined as serum creatinine >2.0 ng/dl) [5]. Limitations of this work included the fact that renal function was crudely estimated with serum creatinine alone, and adjustments for tumor complexity were not originally accounted for [11]. In this report, we update our collaboration to evaluate the short- and long-term renal effects of warm ischemia in a large cohort of patients with a solitary kidney.
2. Materials and methods
2.1. Patient selection
Following approval from the institutional review boards, we identified 362 patients with a solitary kidney who had warm ischemia used during partial nephrectomy for renal cortical tumors between 1990 and 2008. Patients treated with no ischemia or cold ischemia were excluded. The surgical technique employed at the Mayo Clinic and Cleveland Clinic was summarized in 2007 [5]. It was common practice at both institutions to clamp both the artery and vein during hilar compression for warm ischemia, and enucleations (as opposed to wedge resections) were predominantly used in these patients with solitary kidneys. During the study time period, it was routine at both participating institutions to use cold ischemia if it was anticipated that vascular clamping would be required for >30 min. Otherwise, warm ischemia was used if clamp time was anticipated to be <20–30 min.
2.2. Features studied and complications
The clinical and pathologic features studied included age, gender, pathologic tumor size, histology (malignant vs benign), and preoperative GFR as estimated by the abbreviated Modification of Diet in Renal Disease (MDRD) equation [12]. The complications studied included hemorrhage, urine leak in the postoperative period, ARF diagnosed clinically as documented in the medical record, development of a GFR <15 ml/min per 1.73 m2 within 30 d of surgery, and need for temporary or permanent dialysis.
2.3. Statistical methods
The associations of warm ischemia with a clinical diagnosis of ARF and the development of a GFR <15 ml/min per 1.73 m2 within 30 d of surgery were evaluated using logistic regression models and summarized with odds ratios and 95% confidence intervals (CIs); patients with a preoperative GFR <15 ml/min per 1.73 m2 were excluded for the latter analysis. The new-onset development of stage IV chronic kidney disease (GFR <30 ml/min per 1.73 m2) after the acute postoperative period was estimated using the Kaplan-Meier method; patients with a preoperative GFR <30 ml/min per 1.73 m2 were excluded from this analysis. The associations of warm ischemia time with this end point were evaluated using Cox proportional hazards regression models and summarized with hazard ratios and 95% CIs. We evaluated warm ischemia time as a continuous variable and in 5-min increments for the end points just cited and used concordance indexes to determine the best cut point for each end point. Statistical analyses were performed using the SAS software package (SAS, Cary, NC, USA). All tests were two sided, and p values <0.05 were considered statistically significant.
3. Results
Baseline clinical and pathologic features and complications among all 362 patients are detailed in Table 1. Median age was 62 yr, and median tumor size was 3.4 cm. Median preoperative GFR was 61 ml/min per 1.73 m2, and 20 patients (6%) had a preoperative GFR < 30 ml/min per 1.73 m2. Median (range) preoperative serum creatinine was 1.2 (0.6–4.1) mg/dl. Hemorrhage and a postoperative urine leak were observed in 5% of patients each. Five patients (1%) had a positive margin after pathologic analysis. A clinical diagnosis of ARF and a GFR <15 within 30 d of surgery were noted in 70 patients (19%) and 56 patients (16%), respectively. Temporary and permanent dialysis was needed in only 2% of patients each.
Table 1 Clinical and pathologic features and complications for 362 patients with a solitary kidney treated with partial nephrectomy
| Feature | Median (range) |
|---|---|
| Age at surgery, yr | 62 (19–93) |
| Preoperative GFR (n = 358) | 61 (11–33) |
| Pathologic tumor size, cm (n = 360) | 3.4 (0.7–8.0) |
| No. (%) | |
|---|---|
| Male gender | 246 (68) |
| Preoperative GFR <30 (n = 358) | 20 (6) |
| Type of partial nephrectomy | |
| Open | 319 (88) |
| Laparoscopic | 43 (12) |
| Malignant histology | 319 (88) |
| Hemorrhage (n = 330) | 15 (5) |
| Urine leak (n = 330) | 17 (5) |
| ARF (clinical diagnosis) | 70 (19) |
| ARF (GFR <15; n = 356) | 56 (16) |
| Temporary dialysis | 7 (2) |
| Permanent dialysis | 8 (2) |
ARF = acute renal failure; GFR = glomerular filtration rate.
Median warm ischemia time (interquartile range: 16–31 min; range: 4–55 min) was 21 min. As a continuous variable, longer warm ischemia was associated with ARF (odds ratio: 1.05 for each 1-min increase; 95% CI, 1.02–1.08; p < 0.001) and a GFR < 15 ml/min per 1.73 m2 (odds ratio: 1.06 for each 1-min increase; 95% CI, 1.02–1.09; p < 0.001) in the postoperative period. Adjusting for preoperative GFR, tumor size, and type of partial nephrectomy (open vs laparoscopic) in a multivariable analysis, longer warm ischemia remained significantly associated with ARF (p = 0.001) and a GFR < 15 ml/min per 1.73 m2 (p = 0.001) in the postoperative period (Table 2).
Table 2 Univariate and multivariable associations of warm ischemia time (continuous) with clinical end points
| Feature | ARF | |||
|---|---|---|---|---|
| Univariate | Multivariable | |||
| OR (95% CI) | p value | OR (95% CI) | p value | |
| Warm ischemia time (1-min increase) | 1.05 (1.02–1.08) | <0.001 | 1.06 (1.03–1.10) | 0.001 |
| Preoperative GFR (10-unit increase) | 0.67 (0.58–0.79) | <0.001 | 0.66 (0.56–0.78) | <0.001 |
| Tumor size (1-cm increase) | 1.12 (1.02–1.24) | 0.023 | 1.06 (0.94–1.19) | 0.369 |
| Laparoscopic vs open | 0.39 (0.14–1.14) | 0.086 | 0.32 (0.10–1.05) | 0.060 |
| Acute-onset GFR <15 | ||||
|---|---|---|---|---|
| Univariate | Multivariable | |||
| OR (95% CI) | p value | OR (95% CI) | p value | |
| Warm ischemia time (1-min increase) | 1.06 (1.02–1.09) | <0.001 | 1.07 (1.03–1.11) | 0.001 |
| Preoperative GFR (10-unit increase) | 0.65 (0.55–0.78) | <0.001 | 0.63 (0.52–0.76) | <0.001 |
| Tumor size (1-cm increase) | 1.13 (1.01–1.26) | 0.027 | 1.05 (0.93–1.19) | 0.446 |
| Laparoscopic vs open | 0.53 (0.18–1.55) | 0.246 | 0.42 (0.13–1.37) | 0.149 |
| New-onset GFR <30 | ||||
|---|---|---|---|---|
| Univariate | Multivariable | |||
| HR (95% CI) | p value | HR (95% CI) | p value | |
| Warm ischemia time (1-min increase) | 1.06 (1.03–1.09) | <0.001 | 1.04 (1.00–1.08) | 0.033 |
| Preoperative GFR (10-unit increase) | 0.61 (0.48–0.77) | <0.001 | 0.59 (0.46–0.76) | <0.001 |
| Tumor size (1-cm increase) | 1.18 (1.08–1.28) | <0.001 | 1.09 (0.96–1.23) | 0.173 |
| Laparoscopic vs open | 0.65 (0.20–2.14) | 0.483 | 0.59 (0.17–2.06) | 0.410 |
ARF = acute renal failure; CI = confidence interval; GFR = glomerular filtration rate; HR = hazard ratio; OR = odds ratio.
Among the 362 patients, 226 patients had a preoperative GFR ≥ 30 ml/min per 1.73 m2 and were followed for ≥30 d. Median (range) follow-up for this subset was 1.6 (0.1–19.0) yr. Among these 226 patients, 38 (17%) developed new-onset stage IV chronic kidney disease during follow-up. Longer warm ischemia was significantly associated with new-onset stage IV chronic kidney disease (hazard ratio: 1.06 for each 1-min increase; p < 0.001; Table 2). Adjusting for preoperative GFR, tumor size, and type of partial nephrectomy (open vs laparoscopic) in a multivariable analysis, longer warm ischemia remained significantly associated with new-onset stage IV chronic kidney disease (p = 0.033; Table 2).
After evaluating warm ischemia as a continuous variable, we investigated warm ischemia time in 5-min intervals to find a cutoff that best discriminated between the three end points previously evaluated. The highest concordance index that best distinguished between patients with and without ARF, with and without an acute GFR <15 in the postoperative period, and with and without new-onset stage IV chronic kidney disease during follow-up was observed at 25 min of warm ischemia for each of the three end points. For example, for patients treated with >25 min (vs ≤25) of warm ischemia, the odds of developing ARF was 2.72 (95% CI, 1.58–4.67; p < 0.001), and the odds of having a GFR <15 ml/min per 1.73 m2 in the postoperative period was 2.58 (95% CI, 1.43–4.63; p = 0.002; Table 3). Furthermore, patients treated with >25 min of warm ischemia were greater than four times more likely to develop stage IV chronic kidney disease during follow-up (hazard ratio: 4.11; 95% CI, 2.09–8.10; p < 0.001; Fig. 1). Baseline clinical and pathologic features and complications among patients treated with ≤25 min and >25 min of warm ischemia are detailed in Table 4. In a multivariable analysis, adjusting for preoperative GFR, tumor size, and type of partial nephrectomy, patients treated with >25 min of warm ischemia remained at significant risk of ARF (p = 0.001) and a GFR < 15 ml/min per 1.73 m2 (p = 0.006) in the postoperative period and new-onset stage IV chronic kidney disease (p = 0.004) during follow-up (Table 2). When these analyses were repeated on the subset of patients treated with open partial nephrectomy only, a 25-min cut point of warm ischemia continued to best discriminate between patients with and without the three end points evaluated. In addition, warm ischemia time remained significantly associated with these end points after multivariable adjustment for preoperative GFR and tumor size among the subset of patients treated with open partial nephrectomy only (data not shown).
Table 3 Univariate and multivariable associations of warm ischemia time (>25 vs ≤25 min) with clinical end points
| Warm ischemia time | ARF | |||
|---|---|---|---|---|
| Univariate | Multivariable* | |||
| OR (95% CI) | p value | OR (95% CI) | p value | |
| >25 min (vs ≤25) | 2.72 (1.58–4.67) | <0.001 | 2.71 (1.49–4.94) | 0.001 |
| Acute-onset GFR < 15 | ||||
|---|---|---|---|---|
| Univariate | Multivariable* | |||
| OR (95% CI) | p value | OR (95% CI) | p value | |
| >25 min (vs ≤25) | 2.58 (1.43–4.63) | 0.002 | 2.47 (1.30–4.69) | 0.006 |
| New-onset GFR < 30 | ||||
|---|---|---|---|---|
| Univariate | Multivariable* | |||
| HR (95% CI) | p value | HR (95% CI) | p value | |
| >25 min (vs ≤25) | 4.11 (2.09–8.10) | <0.001 | 3.01 (1.44–6.30) | 0.004 |
* Adjusted for preoperative GFR, tumor size, and type of partial nephrectomy (laparoscopic vs open).
ARF = acute renal failure; CI = confidence interval; GFR = glomerular filtration rate; HR = hazard ratio; OR = odds ratio.
00531-2/assets/gr1.jpg)
Fig. 1 Risk of developing new-onset stage IV chronic kidney disease for patients treated with >25 min versus ≤25 min of warm ischemia.GFR = glomerular filtration rate.
Table 4 Clinical and pathologic features and complications stratified by warm ischemia time
| Feature | Median (range) | p value | |
|---|---|---|---|
| ≤25 min | >25 min | ||
| (n = 230) | (n = 118) | ||
| Age at surgery, yr | 63 (19–93) | 61 (24–83) | 0.20 |
| Preoperative GFR (n = 344) | 62 (18–133) | 59 (14–109) | 0.18 |
| Pathologic tumor size, cm (n = 346) | 3.0 (0.7–15.0) | 4.0 (1.4–18.0) | <0.001 |
| Ischemia time | 18 (4–25) | 31 (25–55) | – |
| No. (%) | |||
|---|---|---|---|
| ≤25 min | >25 min | ||
| (n = 230) | (n = 118) | ||
| Male gender | 156 (68) | 82 (69) | 0.75 |
| Preoperative GFR <30 (n = 344) | 13 (6) | 5 (4) | 0.57 |
| Type of partial nephrectomy | |||
| Open | 209 (91) | 100 (85) | 0.09 |
| Laparoscopic | 21 (9) | 18 (15) | |
| Malignant histology | 202 (88) | 105 (89) | 0.75 |
| Hemorrhage (n = 316) | 7 (3) | 6 (5) | 0.39 |
| Urine leak (n = 316) | 8 (4) | 8 (7) | 0.19 |
| ARF (clinical diagnosis) | 32 (14) | 36 (31) | <0.001 |
| ARF (GFR <15; n = 343) | 26 (11) | 29 (25) | 0.001 |
| Temporary dialysis | 4 (2) | 3 (3) | 0.69 |
| Permanent dialysis | 4 (2) | 4 (3) | 0.45 |
ARF = acute renal failure; GFR = glomerular filtration rate.
4. Discussion
To our knowledge, this is the largest report evaluating the renal consequences of warm ischemia time in patients undergoing partial nephrectomy in the setting of a solitary kidney. Compared with our previous results [5], we include more than twice as many patients (362 vs 174 treated with warm ischemia), we better assess renal function with estimated GFR according to the MDRD equation (as opposed to serum creatinine alone), and we include patients treated with both open and laparoscopic approaches. Our results demonstrate that longer warm ischemia time during partial nephrectomy is associated with an increased risk of short- and long-term renal consequences, including ARF in the postoperative period and new-onset development of stage IV chronic kidney disease during follow-up. For example, each additional minute of warm ischemia was associated with a 5% and 6% increased odds of developing ARF or a GFR < 15 ml/min per 1.73 m2 in the postoperative period, respectively, and was associated with a 6% increased risk of new-onset stage IV chronic kidney disease during follow-up. These observations suggest that every minute counts when the renal hilum is clamped without hypothermic techniques, and efforts to minimize ischemia time should be entertained when planning a surgical approach, especially during imperative situations such as a tumor in a solitary kidney.
In an attempt to identify a potential ischemic time cut point, we evaluated time in 5-min increments to determine the threshold that best distinguishes between ARF, acute GFR < 15, and new-onset stage IV chronic kidney disease individually. Somewhat surprisingly, the cut point that best distinguished between each of these three end points was 25 min. This is in agreement with our previous collaboration, where we found >20 min of warm ischemia to be an important predictor of adverse renal outcomes [5], and a limit of 20 min of warm ischemia was recently supported by an international collaborative review of the literature [6]. With the current results, we submit that although 20 or 25 min of warm ischemia may represent the best cutoff for predicting adverse renal consequences, the observation that warm ischemia as a continuous variable is significantly associated with short- and long-term renal functional decline suggests that each increasing minute of warm ischemia invites additional risk of renal consequences. This also confirms our previous finding that the duration of renal ischemia is the largest modifiable risk factor during partial nephrectomy in the solitary or two-kidney setting [4]. Thus clamp time should be minimized whenever possible, and if longer ischemic times are anticipated, techniques such as ice slush should be considered. If a laparoscopic approach is employed, an early unclamping technique can be used with shorter warm ischemia times [13]. Furthermore, robotic assistance has recently shown promise for maintaining within 25–30 min [14]. Collectively, these observations support the use of shorter warm ischemic times, which must be obtained regardless of surgical approach.
Historically, 30 min was considered the maximum safe duration of warm ischemia during partial nephrectomy. Within the past 5 yr, this notion has been challenged. Observations in the porcine model have suggested that renal pedicle clamping for 90 min is safe [7] and [8]. Additionally, retrospective clinical observations have suggested that warm ischemia for 40–55 min is safe and effective [9] and [10]. However, these studies included patients with normal contralateral kidneys, potentially masking the effects of ischemia on a solitary renal unit because serum creatinine and estimated GFR were used to assess renal function. It has previously been reported that a study involving the effect of warm ischemia in solitary kidneys is needed. The current results, which stem from an updated collaboration between the Mayo Clinic and the Cleveland Clinic, strongly support that longer warm ischemic times are associated with adverse renal consequences, even after multivariable analysis adjusting for preoperative GFR, tumor size, and type of partial nephrectomy. To our knowledge, this is the first report to evaluate warm ischemia time as a continuous variable with short- and long-term renal disease in patients with a solitary kidney. Although external validation on patients with a solitary kidney is needed, our results support the notion that every minute counts when the renal hilum is clamped under warm ischemia conditions. However, the results of this work do not have any implications for patients treated with cold ischemia. These patients were omitted during the planning phases of this work for the sole purpose that only the most challenging tumors at the Mayo Clinic and Cleveland Clinic were treated with hypothermic techniques during the study time frame. In fact, one could argue that because approximately 25% of patients in this study with a preoperative estimated ischemia time <30 min actually endured >30 min of warm ischemia, perhaps cold ischemia should be used more often in patients with a solitary kidney.
This study is not without limitations. The data were collected in a retrospective fashion and are subject to the many inherent biases associated with this approach. In our multivariable analyses, we adjusted for tumor size, preoperative GFR, and surgical approach; however, we were unable to factor in recently reported scores that predict for surgical complexity [15] and [16]. Additionally, all patients had a solitary kidney with imperative indications for partial nephrectomy. Previous observations have suggested that a solitary kidney is more resistant to ischemic damage compared with paired kidneys [17], [18], and [19]. Therefore, our results may overestimate the maximal renal tolerance to ischemia in patients with a normal contralateral kidney. Furthermore, only patients treated with warm ischemia were included in this study. Because the more challenging cases were treated with hypothermic techniques, our results may not apply to all patients with a renal mass. Nevertheless, our results support the recommendation that warm ischemia should be limited to 20–25 min during partial nephrectomy.
5. Conclusions
Longer warm ischemia time is associated with short- and long-term renal consequences, including ARF and new-onset stage IV chronic kidney disease. Given the importance of preserving renal function, particularly in patients with a solitary kidney, every effort should be made to minimize warm ischemic intervals during partial nephrectomy, and research priority should be given to methods to improve renal surgical paradigms to minimize ischemic parenchymal damage.
Author contributions: R. Houston Thompson had full access to all the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis.
Study concept and design: Thompson, Lane, Campbell, Blute.
Acquisition of data: Thompson, Lane, Lohse.
Analysis and interpretation of data: Thompson, Lane, Campbell, Blute, Lohse.
Drafting of the manuscript: Thompson, Lane.
Critical revision of the manuscript for important intellectual content: Thompson, Lane, Campbell, Blute, Fergany, Gill, Leibovich, Frank.
Statistical analysis: Lohse.
Obtaining funding: None.
Administrative, technical, or material support: None.
Supervision: Campbell, Blute.
Other (specify): None.
Financial disclosures: I certify that all conflicts of interest, including specific financial interests and relationships and affiliations relevant to the subject matter or materials discussed in the manuscript (eg, employment/affiliation, grants or funding, consultancies, honoraria, stock ownership or options, expert testimony, royalties, or patents filed, received, or pending), are the following: None.
Funding/Support and role of the sponsor: None.
Acknowledgment statement: The authors are indebted to the late Dr. Andrew C. Novick, who operated on most of the patients included in this study.
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Footnotes
a Mayo Medical School and Mayo Clinic, Rochester, MN, USA
b Glickman Urological Institute; Cleveland Clinic Foundation, Cleveland, OH, USA
c Keck School of Medicine, University of Southern California, Los Angeles, CA, USA
Corresponding author. Department of Urology, Mayo Clinic, 200 First Street SW, Rochester, MN 55905, USA. Tel. +1 507 284 3981; Fax: +1 507 284 4951.
1
Contributed equally to this work.
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Article information
PII: S0302-2838(10)00531-2
DOI: 10.1016/j.eururo.2010.05.047
© 2010 European Association of Urology, Published by Elsevier B.V.
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