Renal perfusion with venous blood extends the permissible suprarenal clamp time in abdominal aortic surgery
Article Outline
Objective
Suprarenal clamping in abdominal aortic surgery is associated with a significant risk of postoperative renal failure, general morbidity, and mortality. Arterial access for temporary shunting in these patients is difficult, and arterial perfusion techniques are typically complex. This study evaluated if renal perfusion with venous blood using a minimal pump setup and intermediate-level heparinization prevents a decline in postoperative renal function in patients requiring suprarenal clamping for aortic reconstructive surgery.
Methods
Renal perfusion was achieved using a roller pump supplied with venous blood from a central venous catheter under medium-level heparinization to feed two perfusion balloon catheters. The calculated glomerular filtration rate was observed for 10 postoperative days and compared with the rate in patients with suprarenal clamping without renal perfusion.
Results
From 2001 to 2007, 158 patients underwent surgical reconstruction involving the pararenal aorta through a midline abdominal incision. Renal perfusion was started in 2006 and was always attempted if suprarenal clamping was anticipated preoperatively. Twenty-six patients received renal perfusion, and 132 also requiring suprarenal clamping did not. Of the latter, 109 were included in the control group. Five patients died ≤30 days (3.7%), one in the perfusion group. On average, there was a postoperative loss of renal performance in both groups. Dialysis was required postoperatively in 13 patients without renal perfusion, 4 of them long term (3.7%), but not in patients with renal perfusion. The reduction in glomerular filtration rate at 10 days in the nonperfused group was significantly higher than in the perfused group (7.24 vs 0.89 mL/min) despite a significantly longer suprarenal clamp time in the latter (25.5 vs 45.5 minutes). Multivariate analysis showed a significant reduction in the loss of glomerular filtration rate with perfusion (P = .007) if clamp time and preoperative renal function were taken into account. Patients with preoperative renal impairment showed the greatest benefit from the perfusion.
Conclusion
The setup for renal perfusion with venous blood during suprarenal clamping was simple and safe. Perfusion significantly reduced the reduction of renal function in the immediate postoperative period, suggesting that clamp time may thus be safely be extended to allow for complex reconstruction of the pararenal aortic segment. The benefit was most marked for patients with preoperative renal impairment.
Suprarenal, as opposed to infrarenal clamping in aortic surgery, is known to increase morbidity and mortality in abdominal aortic surgery.1, 2, 3 In the era of endovascular aneurysm repair (EVAR), the relative number of patients presenting for open conventional surgery with a hostile proximal anatomy and frequently pre-existing reduced renal function, increases steadily.4, 5, 6 This is because of a number of late conversions, but more important, because of the decreased reluctance to operate on severely comorbid or elderly patients despite clearly rising rates of complications with age.7, 8, 9, 10, 11 Postoperative renal failure, transitory or as a permanent loss of glomerular filtration rate (GFR), is a well established independent risk factor for survival in such patients.12, 13, 14 The incidence of renal failure after suprarenal clamping has been shown to depend on clamp time and is estimated at about 20%, with 3% to 4% requiring permanent dialysis.1, 15, 16, 17 The question of nephroprotection as a possible adjunct to improve outcome arises.
Most series define postoperative renal failure as an often-temporary increase in the serum creatinine level seen within the first postoperative week.15 The mechanisms contributing to the loss of renal function are not entirely clear. Although ischemia is the main initiating factor, the role of the acid-base balance, other buffering systems, and formation of toxins such as radicals remains less well characterized. The benefit of systemically administered protective drugs, such as diuretics, mannitol, and acetylcysteine, has not yet not been confirmed.18, 19, 20, 21 The usefulness of fenoldopam in this context also remains debatable.22, 23
On the other hand, in thoracoabdominal aneurysm surgery, the protective effect of normothermic or mildly hypothermic whole blood as the presumably perfect protective agent, or intermittent cold crystalline perfusion of the kidneys, has in many instances been confirmed, and one of the two is thus part of the routine protocol in most centers.24, 25, 26, 27 However, abdominal aortic aneurysms beginning at or just above the level of the renal artery origins, often referred to as pararenal aneurysms, are preferably approached transabdominally through a midline incision.2, 28 Therefore very little space is left to obtain an arterial blood supply from the aorta, which in addition is commonly diseased, so that passive arterial shunting is not generally a realistic option.
Peripheral arterial access, such as from the subclavian artery, is an option in this context; however, it requires large-bore tubing for low resistance passive shunting and surgical dissection of the artery. Perfusion techniques involving a conventional pump setup, possibly even with the addition of an oxygenator to the circuitry, have the disadvantages of both the necessary large-bore arterial or venous access and the usually required high level heparinization, with the potential consequence of bleeding diatheses. The disadvantages of cold crystalline perfusion are that it leads to loss of body temperature at an early stage of the procedure, and the monitoring of the kidney temperature from a midline incision is more difficult than in thoracoabdominal aortic surgery. Furthermore, the cooling effect is heterogeneous and not well transported to the cortex of the kidneys, which are well suspended in tissue supplied by the remaining normothermic circulation. The dorsal warming effect of heating the operating table has further far less-well-characterized influences in this context.
The aim of this study was therefore to evaluate whether renal perfusion with normothermic venous blood, using a minimal pump setup and an intermediate level of heparinization, prevents a decline in renal function during the first 10 postoperative days if suprarenal clamping is required. This article presents the results with this approach combining a less invasive access with whole blood, the potentially optimal perfusate, and an intermediate level of heparinization.
Methods
From January 2001 to September 2007, we electively treated 851 patients with abdominal aortic aneurysms (AAAs), and 157 were treated by endovascular means. In the thoracoabdominal aortic segment, 128 aneurysms were repaired in the same period. Data from all patients presenting with pararenal AAAs approached transabdominally through a midline incision (inclusion criteria) were collected prospectively. Informed consent was obtained from all patients. Whenever suprarenal clamping was anticipated, patients were scheduled for renal perfusion from 2006 onward. Exclusion criteria were emergency cases and patients presenting preoperatively with terminal renal insufficiency.
The original data collection was done to further evaluate risk factors for renal function in suprarenally clamped aortic reconstructions. The use of perfusion then evolved from the positive experience in thoracoabdominal aortic surgery and was adapted as outlined subsequently at a later stage of the studied time period.29
Instead of obtaining arterial blood from the proximal aorta for renal perfusion, venous blood was taken from a conventional high-flow central venous catheter (Arrow-Howes, Multi-Lumen-Large-Bore Catheter, 2- × 12-gauge, 1-× 16-gauge, 16-cm long; Arrow International, Diegem, Belgium), advanced into the right atrium through the right internal jugular vein. This specific catheter has been part of the routine protocol for open infrarenal aortic procedures in our unit for many years, so that no changes had to be made for the perfusion.
The operations were performed with general anesthesia with a fraction of inspired oxygen of 1.0 for the entire procedure as part of the protocol. The perfusate was applied to the renal arteries through a roller pump withn 0.25-inch tubing (SIII Double Head Pump, Stöckert, Germany) and two 9F balloon catheters (Pruitt Irrigation Occlusion Catheter, Le Maitre Vascular, Burlington, Mass) passing only through a heat exchanger. For this series, the perfusate was kept normothermic to prevent cooling the whole patient. Perfusion was started as soon as possible after suprarenal clamping and careful inspection of the renal artery ostia.
Heparin was previously administered as single injection at a dosage of about 1.5 times the conventiona1 100 IU/kg to achieve an activated clotting time (ACT) of 160 to 180 seconds. The perfusion was tailored to achieve a flow of 150 to 300 mL/min, with a maximum perfusion pressure ≤150 mm Hg measured within the distal tubing but proximal to the perfusion catheters. The flows varied considerably within the set limits amongst patients and the course of the operation. Perfusion was maintained as long as necessary to complete the proximal anastomosis and, if necessary, any renal artery reconstructions or reimplantations.
The control group was recruited from the prospectively collected data set starting in 2001, as outlined. Those who had presented with perforated aneurysms and those approached retroperitoneally, as well as the patients who died early postoperatively without completing the 10 days surveillance period, were excluded from the analysis in both groups.
The GFR as calculated using the Cockcroft-Gault equation was monitored on a 24-hour basis for 10 postoperative days, and the changes over time were compared between the groups of patients with and without renal perfusion.30 Intraoperative details that entered into the evaluation were total operating time, suprarenal clamp time, reconstructions of renal arteries, division of the left renal vein for access, and the type of aortic reconstruction performed. Postoperative variables included in the analysis were hemoglobin, creatinine kinase, and C-reactive protein (CRP) levels on postoperative days 0, 1, 2, 3, 5, 7, and 10.
Statistical analysis
The patient baseline characteristics were compared using the t test to identify potentially relevant cofactors for the multifactorial univariate and multivariate analyses. The primary outcome measure was the cumulative change of GFR during a 10-day period, as determined from the area under the curve (AUC) of GFR plotted against time (GFRarea). Furthermore, we analyzed the maximum change in GFR observed ≤10 days after surgery to also address the size of a temporary change of renal function (GFRDmax). Third, the absolute difference between preoperative GFR and GFR on day 10 was used to characterize the overall change in renal function. These three variables were then directly compared between the groups using the t test.
Multifactorial univariate and multivariate analyses were used to examine the influence of perfusion on GFR with respect to total operating time, suprarenal clamp time, temporary division of the left renal vein, postoperative load of creatinine kinase (AUC creatinine kinase vs time), rise of CRP, and the presence of preoperative renal impairment. The latter was defined as a preoperative starting GFR <60 mL/min. Logistic regression analysis was used to describe the effect of perfusion on renal function in dependence of suprarenal clamp time. A significance level of P < .05 was used for statistical analysis.
Results
From January 2006, 26 of 28 patients scheduled for renal perfusion received this during suprarenal clamping for abdominal aortic surgery. Four patients during that period had suprarenal clamping where this was not expected preoperatively so that they did not receive perfusion and were included in the control group. Cannulation of the renal arteries was not possible in one patient, and the central venous access did not allow sufficient drainage for perfusion in a further patient. In the other 26 patients, perfusion was uneventful. No detectable injuries occurred to the renal arteries by the perfusion catheters or their introduction. The space taken up by the catheters within the operating field did in no case led to the necessity to stop perfusion to perform the proximal anastomosis or any renal artery reconstruction. It was possible to maintain flow >150 mL/min in all cases. Advantageous aspects of cannulating the renal arteries were the lack of back bleeding and thus the benefit of not having to clamp the vessels separately. Arterial blood gas analysis showed a mean partial pressure of oxygen of 287 mm Hg (range, 181.2-400.2 mm Hg) during the operations, thus confirming adequate oxygenation.
From 2001 to 2007, 132 patients principally eligible to be included in the control group were identified and 109 eventually qualified for the retrospective analysis according to the inclusion and exclusion criteria. Baseline characteristics and intraoperative variables are summarized in Table I. Suprarenal clamp time was significantly longer in the perfusion group (45.5 vs 25.5 minutes). The groups were statistically similar in mortality rate, total operating time, incidence of temporary left renal vein division (reconstructed in all but 3 patients), incidence of concomitant renal artery surgery, extent of aortic reconstruction (tube vs bifurcated graft), preoperative renal insufficiency, and levels of creatinine kinase and CRP as expression of operative trauma (Table I). Intraoperative transfusion requirement of packed red blood cells but not fresh frozen plasma was higher in the perfused group (2.9 ± 3.7 vs 5.1 ± 3.9 U, P = .021) and this was statistically significant.
Table I. Comparison of means by t test and χ2 test between the groups to identify relevant parameters for the multivariate analysis
| Variable | No perfusion | Perfusion | P |
|---|---|---|---|
| Patients, No. | 109 | 26 | |
| Age, years | 68.3 | 71.1 | .147 |
| Female, No. (%) | 14 (12.8) | 5(19.2) | .338 |
| Pre-op renal failure, No. (%) | 38(34.9) | 8(30.8) | .692 |
| Operating time, min | 238.9 | 244.62 | .788 |
| Suprarenal clamp time, mean (range) min | 25.5(10-86) | 45.5(17-100) | <.001 |
| Renal vein division, No. (%) | 27(25.0) | 11(42.3) | .739 |
| Renal artery surgery, No. (%) | 25(23.1) | 7(26.9) | .764 |
| Tube graft, No. (%) | 40(35.4) | 13(50) | .228 |
| RBC transfusion, mean ± SD U | 2.9 ± 3.7 | 5.1 ± 3.9 | .021 |
| Ventilation, mean (range) h | 39.16(0-823) | 33.96(0-432) | |
| Post-op ICU, mean (range) days | 3.7(0-37) | 2.6(0-20) | .335 |
| Post-op renal failure, No. (%) | 56(51.9) | 14(53.8) | .821 |
No patients required dialysis postoperatively in the perfused group; but dialysis was required in 13 patients (11.1%) in the nonperfused group, and 4 (3.7%) remained on dialysis long-term. A deterioration of GFR was noted in both groups, as determined by the t test looking at the AUC GFR against time (GFRarea) and the maximum change in GFR (GFRDmax) in the postoperative period. In patients with renal perfusion, the GFR decreased on average 1.7 ± 27.4 mL/min (GFRDmax) and 4.1 ± 17.1 mL/min (GFRarea), whereas the group without perfusion lost 14.0 ± 30.6 mL/min (GFRDmax) and 9.4 ± 23.6 mL/min (GFRarea). Neither the change in GFRarea nor that in GFRDmax reached statistical significance in the unpaired t test because the variation of individual results was large in both groups. A t test for paired samples, however, showed a highly significant drop of 7.24 mL/min (P = .002) of GFR from before the operation to day 10 in the group without perfusion, whereas no significant change occurred in the perfused group (0.89 mL/min, P = .823).
Furthermore, the multivariate analysis with the outcome parameters GFRarea and GFRDmax proved perfusion to be highly statistically significant for the preservation of renal function (GFRarea, P = .007; GFRDmax, P = .002) when suprarenal clamp time and preoperative renal impairment were taken into account as covariables (Table II). These two factors had previously been identified as relevant variables for renal function in the univariate analysis. Expressed in another way: The clamp time did, as expected, have a relationship with postoperative loss of renal function in the nonperfused group (P < .001), but this relationship was lost in the perfused group (Fig 1).
Table II. Multivariate analysis of variables indicating postoperative deterioration of renal function
| Variable | Renal function loss due to clamping | P |
|---|---|---|
| Suprarenal clamp time | Increased | <.001 |
| Perfusion | Decreased | .007 |
| Pre-op renal function | Increased | .021 |
Fig 1.
The change in renal function with the operation is shown as a function of suprarenal clamp time and renal perfusion in patients (A) with no perfusion and (B) those with perfusion. A, Renal function deteriorates with clamp time if there has been no perfusion, and this is highly significant. B, This relationship, however, is lost if perfusion is performed. GFR, glomerular filtration rate.
Table III reports the other variables that were tested for their influence on postoperative renal function in the multivariate analysis but did not prove to be significant. Thus, creatinine kinase as a marker for operative trauma, total operating time, and temporary left renal vein division did not show a correlation with renal function. Subgroup analysis revealed CRP and preoperative renal insufficiency independently correlated with the loss of renal function only in the nonperfused group (Fig 2). Therefore, the effect of perfusion was tested for its influence on renal outcome dependent on the presence or absence of preoperative renal insufficiency and perfusion was shown to be strongly advantageous in the patients with preoperative renal impairment (P = .008, Table IV).
Table III. Indicators found to be without significant influence on postoperative renal function on multivariate analysis
| Variable | Outcome measure | P |
|---|---|---|
| Renal vein division | GFRarea | .297 |
| GFRDmax | .161 | |
| Operating time | GFRarea | .380 |
| GFRDmax | .368 | |
| Creatinine kinase load | GFRarea | .539 |
| GFRDmax | .605 | |
| C-creative protein load | GRFarea | .159 |
| GFRDmax | .569 |
Fig 2.
The rise in C-reactive protein (CRP) after the operation is shown as function of suprarenal clamp time and renal perfusion in patients (A) with no perfusion and (B) those with perfusion. There is interdependence of CRP and suprarenal clamp time, but only for the patients without renal perfusion.
Table IV. Relative significance of perfusion on renal outcome depicted as glomerular filtration rate area under the curve dependent on preoperative renal insufficiency (correlation analysis)
| Variable | No Perfusion | Perfusion | 95% CI | P |
|---|---|---|---|---|
| Pre-op renal function | ||||
| Poor | −4.315 | 9.029 | −32to−6 | .006 |
| Good | −12.068 | −9.914 | −15to−11 | .764 |
Discussion
Postoperative deterioration of renal function after infrarenal aortic surgery has been described.14, 31 Whereas for infrarenal clamping this is attributed to the impact of the surgery as such and the handling of the aorta near the renal artery origins,32 in cases of suprarenal clamping, ischemia additionally endangers renal function and has been well linked to morbidity, mortality, and long-term survival.33, 34, 35 For suprarenal clamping, the role of inadvertent visceral flow obstruction by the exposure as such, the clamp position between the superior mesenteric artery and the renal arteries, and the distortion of the aortic wall by the clamp cannot be clearly defined. Published reports, however, show a distinct difference in outcome between suprarenal and supraceliac clamping that clearly justifies the attempt to achieve the most distal clamp level.10 Provided that suprarenal clamp times are kept to <30 to 45 minutes, the loss of renal function in patients with normal preoperative renal function is considered small.1, 6, 10, 17 With pre-existing renal impairment or longer clamp times, or with the increase in age and comorbidity of the patients, however, renal protection becomes an important issue. Of the various protective adjuncts propagated over the years, only cold and warm perfusion with crystalline solution and blood, respectively, have been secured for their nephroprotective action.27, 34, 36, 37, 38
The method for renal artery perfusion with venous blood advocated here avoids the need to gain arterial access for passive shunting or the expensive, complex, and thrombogenic setup of a complete heart–lung machine. A scaled down version using a heparin-coated oxygenator also allowing a moderate heparinization would be an option, but the issue of cost and complexity remains.
In this series of 26 perfused and 109 nonperfused aortic repairs requiring suprarenal clamping, no patients in the perfused group needed postoperative dialysis, but 13 patients (11.1%) in the nonperfused did, and 4 (3.7%) required long-term dialysis. The preoperative incidence of reduced renal function was statistically not significantly different between the two groups. The results show, furthermore, an average loss of GFR within the 10 postoperative days in both the perfused and the nonperfused group but this was clearly reduced, if perfusion is applied. Because of the spread of the measured values, the difference did not reach statistical significance on direct comparison of the means with an unpaired t test. When a paired t test is applied to the GFR before and 10 days after the operation, however, a highly significant loss of GFR (7.24 mL/min, P = .002) occurred in the nonperfused group, but this is not the case in the perfused group (0.89 mL/min, P = .823).
Clamp times were significantly longer in the perfused group, and this as well as preoperative renal impairment, turned out to be significant determinants of loss of renal function in the univariate testing. They were thus included as cofactors in the further analysis. Perfusion then turned out to have a highly statistically significant and independent protective effect on renal function in the multivariate analysis. As suggested by the paired t test within the groups, postoperative GFR deterioration determined by changes in GFRarea and GFRDmax in the multivariate analysis is now independent of clamp time if perfusion is used.
In a subgroup analysis, the effect of perfusion was statistically especially beneficial in patients presenting with preoperative renal impairment.
The demonstrated prolongation of suprarenal clamp time in the perfused group could be explained with the installation and handling of the perfusion. This, however, takes about 3 to 5 minutes, even if catheters need to be repositioned for flow optimization. The obstruction within the operating field due to the presence of the catheters is minimal. The surgeons involved were experienced in infrarenal and thoracoabdominal aortic surgery, and there was no obvious learning curve or difference in patient characteristics demonstrated. It is therefore currently assumed that the anticipated protection by perfusion led the surgeons to leave themselves more time for the completion of the proximal aortic and renal reconstructions. Given the well-accepted limits for safe, unprotected suprarenal clamping of 30 to possibly 45 minutes, the mean clamp time of 45.5 minutes in the group of perfused patients with no significant loss of renal function can, however, be seen as supportive for the technique.3, 17
Two factors that were unexpectedly unrelated to the postoperative renal function were creatinine kinase load, thought to represent a measure of the impact of the operation as such (tissue damage), and the temporary division of the left renal vein. The latter cannot be further commented on, as this work did not include a differential measure of left and right renal function. Suprarenal clamp time and CRP level did show a correlation (P = .003), but only for the nonperfused group, possibly pointing to a more general effect of perfusion on the effect of the operation on the patient.
The increase in red blood cell transfusion with perfusion is an unfavorable result. It reached statistical significance, and this presumably reflects the blood volume required to fill the tubing for the perfusion and a slight increase in blood loss due to the additional heparin. Supporting this is that the first postoperative hemoglobin level in the intensive care unit was not different between the groups. Optimization of the handling of blood losses may help to reduce this observed difference in transfusion requirements in the future.
The study has some limitations. The analysis and definition of the control group was retrospective, although involving a prospectively collected data set. A long-term benefit of renal protection by this method of renal perfusion cannot be concluded from these data, but may be assumed. This is because results from thoracoabdominal aortic surgery and long-term follow-up studies relating renal function to survival are very clear in this respect. This may also be seen as supportive for our principal aim to preserve renal function. This work was not aimed to elucidate the mechanism of renal protection by venous blood and this thus remains speculative. The partial pressure of oxygen was not determined in the venous perfusate. The potential benefit of oxygenation and possibly cooling, in addition to the other protective functions of whole blood, will thus have to be determined in a larger comparative study. Because there are no follow-up data on renal artery pathology after surgery, a small possibility exists that some of the effects seen might have occurred by chance and were independent of the perfusion. The perfused group was small, however, so that a subgroup analysis addressing this problem cannot presently be performed.
Conclusion
Our data confirm that suprarenal clamp time is strongly linked to postoperative loss of renal function if no protective adjuncts are applied. Renal perfusion with venous blood as the proposed protective adjunct proved effective in reducing the postoperative deterioration of renal function significantly and therefore prolongs the permissible clamp time. This effect is most marked in patients with preoperative renal impairment. The technique is simple, safe, and not very expensive, and may thus lend itself to be used in various settings of the health care system.
C-reactive protein seems to function as a marker for suprarenal clamp time, which has previously only been linked to other procedure-related details such as the operative approach.39, 40
It may be suggested, that dependent on preoperative computed tomography evaluation, patients with likely suprarenal clamp levels should optionally and with additional pre-existing renal impairment be facultatively scheduled for renal perfusion. An additional preoperative evaluation of the suitability of the renal arteries for perfusion may be helpful. In this series, no definitive indicators concerning this topic were specifically evaluated. However, experience shows that similarly to the situation with thoracoabdominal aortic surgery, heavy calcification along the course of the renal arteries, duplicatures or proximal stenoses at the ostia, may pose a problem for catheter insertion or cause embolization.
Author contributions
References
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Competition of interest: none.
CME article
PII: S0741-5214(08)00074-8
doi:10.1016/j.jvs.2008.01.020
© 2008 The Society for Vascular Surgery. Published by Elsevier Inc. All rights reserved.