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NDT Advance Access originally published online on March 23, 2006
Nephrology Dialysis Transplantation 2006 21(7):1803-1808; doi:10.1093/ndt/gfl066
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© The Author [2006]. Published by Oxford University Press on behalf of ERA-EDTA. All rights reserved. For Permissions, please email: journals.permissions@oxfordjournals.org

Original Articles: Experimental Nephrology

Primary organ function of warm ischaemically damaged porcine kidneys after retrograde oxygen persufflation*

Jürgen W. Treckmann1, Andreas Paul1, Stefano Saad2, Julia Hoffmann3, Karl-Heinz Waldmann3, Christoph E. Broelsch1 and Manfred Nagelschmidt4

1 Department for General, Visceral and Transplantation Surgery, University Hospital of Essen, Hufelandstr. 55, 45122 Essen, 2 Clinic for Visceral, Vascular and Transplantation Surgery, University of Witten Herdecke, Hospital Cologne Merheim, Ostmerheimer Str. 200, 51109 Cologne, 3 Clinic for Swine, Small Ruminants, Forensic Medicine and Ambulatory Services, Veterinary School of Hannover, Bischofsholer Damm 15, 31073 Hannover and 4 Institute of Experimental Medicine, University of Cologne, Robert-Koch-Str. 10, 50931 Cologne, Germany

Correspondence and offprint requests to: Jürgen Treckmann, MD, Klinik für Allgemein- und Transplantationschirurgie, Universitätsklinikum Essen, Hufelandstr. 55, 45122 Essen, Germany. Email: j.treckmann{at}gmx.net



   Abstract
Top
 Abstract
Introduction
 Subjects and methods
 Discussion
 References
 
Background. As warm ischaemic damage is a major reason for the loss of donor organs, an experimental study was performed in order to evaluate retrograde oxygen persufflation (ROP) as a method to extend the warm ischaemic tolerance of kidneys.

Methods. Kidneys of 32 pigs were exposed to warm ischaemia for 60, 90 or 120 min. Then, 16 kidneys were subjected to ROP for 4 h at 4°C and 16 controls were stored in cold UW-solution, followed by autotransplantation.

Results. Only in the group with 60 min warm ischaemic time and ROP did all animals survive the observation period of 7 days. In all other groups some animals died due to anuria. Short-term survivors in these groups had significantly higher creatinine levels.

Conclusions. In this setting, ROP was superior to cold storage when applied after 60 min of warm ischaemia. Clinical evaluation of ROP in the setting of marginal donors and non-heartbeating donation is recommended.

Keywords: kidney transplantation; non-heartbeating donors; retrograde oxygen persufflation; warm ischaemia



   Introduction
Top
 Abstract
 Introduction
Subjects and methods
 Discussion
 References
 
There is still a major discrepancy between cadaveric organs available for transplantation and the actual demand [1] resulting in increasing waiting times for renal transplantation by an average of 3 years in patients on dialysis in Germany and other countries. Attempts to increase the number of living donor transplantations and the use of marginal donor organs are currently the most effective strategies in order to improve this intolerable condition. Other strategies include utilization of organs from non-heartbeating donors (NHBD) [2]. The NHBD programmes have already been successfully established in several countries (e.g. USA, GB, Spain, The Netherlands) while still restricted by Federal Laws in other countries (e.g. Germany).

Preservation itself has the potential to sustain or even improve organ function. Currently, preservation is done by simple cold storage (CS) and in the setting of NHBD-programmes by machine perfusion (MP), at best performed as hypothermic pulsatile perfusion [2–4]. Our previous experiments have shown that preservation with venous systemic oxygen persufflation in combination with anti-oxidative treatment can restore viability of warm ischaemically damaged livers in an in-vitro model of isolated rat liver perfusion [5–8]. We also observed a restitution of organ function of transplanted porcine livers after 60 min of warm ischaemia, when retrograde oxygen persufflation (ROP) had been applied [9].

Already in the 1980s, ROP was performed to preserve kidneys in experimental studies, but because of the development of modern perfusion solutions, additional treatment during preservation as MP or ROP seemed to be unnecessary. Under these conditions the clinical approach of Rolles et al. [17] fell into oblivion, who at first reported a successful application of ROP in kidney transplantation. The increasing use of organs of marginal donors and the establishment of NHBD programmes prompted the prosecution of experimental work to ameliorate the quality of organs with ROP, which was optimized by the addition of the scavenger superoxid dismutase (SOD) as a result of experimental studies in animals [10,11].

Our successful studies in porcine livers encouraged us to evaluate ROP systematically in a model of experimental kidney transplantation, also because clinical implementation of this method should be possible in this setting than in liver transplantation.

So we performed a controlled study in a porcine model of autotransplantation followed by contralateral nephrectomy in order to compare standard treatment (CS) with the effect of ROP on primary function of warm ischaemically damaged kidneys.



   Subjects and methods
Top
 Abstract
 Introduction
 Subjects and methods
Discussion
 References
 
Study design
Thirty-four female German landrace pigs with a mean body weight of 27 kg were used for the trial. The maximal warm ischaemic time (WIT), which allowed restitution of primary renal function by oxygen persufflation was evaluated creating six experimental groups. The WIT was 60 min in the groups 1 and 2, 90 min in the groups 3 and 4 and 120 min in the groups 5 and 6. Oxygen persufflation was administered to the groups 1, 3 and 5. The experimental groups 2, 4 and 6 received only CS without additional oxygen and were used as control (Table 1). The experiment was started with the shortest WIT, thus allowing to stop the study when the WIT became too extended to restore organ function.


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  		Table 1. Survival in the different treatment groups

 
Therefore, randomization of the animals was only performed between the groups with identical WIT. Usually two different teams performed explantation and implantation of the kidneys. In these cases, the second team was blinded with respect to the type of preservation of the organs.

Operation and treatment of the kidneys
Under general anaesthesia with ketamine, fentanyl, pancuronium bromide, oxygen and nitrous oxide, the blood vessels and the ureter of the left kidney were clamped and the organ was subjected to complete in-situ warm ischaemia with the abdomen covered. Then the kidney was removed and flushed anterograde with cold Ringer's solution containing 10.000 IU heparin followed by UW-solution (Viaspan®). In the ROP groups, 12.500 IU of superoxid dismutase (SOD, Sigma Chemicals, St Louis, MO) were infused with the last 20 ml of the UW-solution. All explanted organs were stored for 4 h in UW solution at 4°C. During this time, the ROP to the kidneys was administered as described [5].

Briefly, filtered and humidified pure gaseous oxygen was given through the renal vein with a pressure of 18 mmHg. About 15–20 small pinpricks with a depth of about 1 cm were set with a fine acupuncture needle into the surface of the organ to allow the gas to leave the microvasculature. When the oxygen flow was installed, it was checked whether there was persufflation of all areas. Otherwise additional pinpricks were added. The control kidneys were stored in cold UW-solution without further treatment with the exception that they also received pinpricks in order to mask their treatment.

After 4 h of treatment, the explanted kidneys were flushed anterograde with cold Ringer's solution and autotransplanted into the pigs which were still under anaesthesia. The right kidney was removed leaving the clamped vessels as long as possible. Then the left kidney was implanted contralaterally constructing an end to end anastomosis of the vein and of the artery (7/0 Prolene). After removal of the clamps and correction for possible leakages, the ureter was connected (5/0 PDS) and checked for free passage with the aid of a canula. Finally, the kidney was placed into the retroperitoneal pocket which was closed with four sutures (3/0 Vicryl). A suprapubic catheter was inserted into the bladder and fixed, before the abdomen was closed. The catheters of the vena jugularis interna and the arteria carotis communis were left in place and protected by an adhesive tape. At the end of the operation, the animals received a subcutaneous injection of 50 mg tramadol and an intravenous injection of 40 mg furosemide. Post-operatively 500 mg ampicillin and 50 mg tramadol were administered daily. In most cases, the animals were able to drink on the day of the operation and eat on the first post-operative day. If not, they received infusions of 20% glucose and 0.9% NaCl.

Post-operative management and data collection
Animals without primary renal function were sacrificed, if they developed a very bad general status (unable to move, apathic, plasma potassium >9 mmol/l). Animals with post-operative complications, which were not specifically related to the transplantation such as sepsis and ileus, were excluded.

Daily blood samples were taken from the arterial and venous catheters and—if possible—samples of urine were collected. At the end of the observation period (maximally 7 days) the animals were anaesthetized and a relaparotomy was performed in order to examine the kidney in situ. The kidney was adjudged concerning colour, perfusion defects and arterial or venous thrombosis. The anastomotic sites of both vessels were excised and inspected for technical problems. Then the organ was removed and the animal sacrificed for autopsy.

Tissue samples of the kidney were freeze-dried for determination of lipid peroxidation according to Ohkawa et al. [12] or transferred into formalin for histological examination (PAS-staining, according to Leonhardt [13]). Histological criteria of kidney damage were hydropic swelling of epithelium, loss of brush border, denatured basal membrane, tubular effusions, dilated tubuli, reduced epithelium, necrosis of single cells with loss of nucleus.

The main endpoint of the study was the primary function of the transplanted kidneys, which was characterized by urine production and survival and quantitated by the determination of plasma creatinine (Merckotest Creatinin, Merck, Darmstadt, Germany), urea (Merckotest Harnstoff, Merck, Darmstadt, Germany), potassium (Blood Gas Analyzer, Gem Premier 5300, Mallinckrodt, Hennef, Germany) and protein in urine (BIO-RAD Protein Assay, BIO-RAD Laboratories, Munich, Germany). Additionally, a blood cell count was done.

Statistics
The data presented are expressed as mean±SD. Differences between the groups were detected with one way ANOVA and post hoc least significant difference (LSD) tests. For evaluation of the primary endpoints, the maximum levels during the observation period and the final values obtained immediately before the death of the animals were used. P ≤ 0.05 was considered significant.

Results
Two animals had to be excluded from the study. One with 60 min WIT and ROP and one with 90 min WIT and CS developed an ileus and had to be sacrificed on post-operative days 4 and 6.

Following warm ischaemia, anterograde flushing of the kidneys was easy in all cases. No clots could be observed. No bleeding occurred from the pinpricks on the kidney surface.

In the group with 60 min WIT and ROP (group 1), all six animals survived, whereas in all other groups some animals were lost due to uraemia (Table 1).

The animals of group 1 produced urine over the complete observation period and their maximum creatinine levels in plasma were significantly lower than in the other groups (Figure 1). They all reached normal creatinine levels with a very small variance after 7 days. Concerning the final values, group 1 showed a significant advantage when compared with the groups 2, 3, 5 and 6 (Figure 2). However, even in the groups with 90 min WIT and ROP (group 3) and with 90 min WIT and CS (group 4), there were 2/5 and 3/5 animals with nearly normal plasma creatinine. After 120 min WIT and ROP (group 5) or CS (group 6), there was one animal out of three in each group with highly elevated plasma creatinine, but with urine production and already slightly decreasing creatinine levels at the end of the observation period.


Figure 1
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  		Fig. 1. Plasma creatinine maximum levels (mean±SD). aSignificantly different from all other groups.

 

Figure 2
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  		Fig. 2. Plasma creatinine at the end of trial (day 7 or death of animal) (mean±SD). bSignificantly different from group 60 CS, 90 ROP, 120 ROP, 120 CS.

 
Comparing only the animals which produced urine supported the aforementioned findings. In spite of the reduced number of the surviving pigs, the maximum creatinine levels were significantly lower in group 1 when compared with the groups 3 and 6.

Determination of urea and potassium in plasma of all animals resulted in patterns similar to creatinine. In group 1, the maximum urea values were significantly lower than in groups 4 and 6 (Figure 3), and the maximum values of potassium showed a significant lower level when compared with the groups 2, 3, 5 and 6 (data not shown). Evaluation of the final values of urea in plasma showed a significant advantage of group 1 compared with group 2–6 (Figure 4). Evaluation of the final values of potassium did not result in significant differences.


Figure 3
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  		Fig. 3. Plasma urea maximum levels (mean±SD). cSignificantly different from group 90 CS, 120 CS.

 

Figure 4
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  		Fig. 4. Plasma urea at the end of trial (day 7 or death of animal) (mean±SD). dSignificantly different from all other groups.

 
All the animals with urine production exhibited some degree of proteinuria. When comparing the maximum levels, group 1 showed no difference to the groups 2 through 6. At the end of the trial only one pig still had protein >2 g/l in its urine (90 min WIT, CS: 19 g/l). Even the two pigs surviving in groups 5 and 6 no longer had proteinuria (Figure 5).


Figure 5
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  		Fig. 5. Proteine in urine at end of trial (day 7 or death of animal) (mean±SD).

 
As high concentrations of oxygen may damage cellular membranes by oxygen-free radicals, lipid peroxidation was measured in kidney samples of the surviving animals and in some of the removed right kidneys as a control. The results are presented in Table 2.


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  		Table 2. Lipid peroxidation of kidney tissue determined on day 7 after transplantation (nmol malondialdehyde/g dry weight)

 
Up to 90 min WIT there were no differences between fresh untreated kidneys and the treated kidneys whether cold stored or persufflated. According to these data, treatment with oxygen did not induce increased lipid peroxidation in these groups. Both animals surviving 120 min WIT of the kidney showed increased levels of malondialdehyde, with the persufflated kidney far exceeding the level of the cold stored kidney.

Judged by the macroscopic aspect, the urine producing kidneys did not differ significantly. They all showed a reddish-brown colour and a soft-elastic consistency. The kidneys of the anuric animals (n = 10) appeared less or more necrotic depending on the time elapsed since transplantation. In these animals, we found four kidneys with arterial or venous thrombosis and one with clots in both vessels. Concerning the anastomoses no technical problems could be observed.

The remaining five necrotic kidneys were completely free of thrombotic vessel obstruction.

Histologically, the urine producing kidneys exhibited only minimal signs of tissue damage. Group 1 seemed nearly completely regenerated within the observation period however, in general group specific differences could not be ascertained.



   Discussion
Top
 Abstract
 Introduction
 Subjects and methods
 Discussion
References
 
The method of retrograde oxygen persufflation, primarily discovered because of an experimental mistake, was utilized successfully in different approaches in animal experiments to restore organ function of heart, kidney and liver [11]. It has been shown that the energy status of the organs can be maintained under persufflation and that the treated organs can restore their function following transplantation [11]. Ventilation of warm ischaemic damaged lungs led to comparable good results [14].

In this study, the effects of ROP on the restitution of the kidney in a large animal experiment in different WITs were examined.

In our experimental setting, ROP in combination with SOD was beneficial for functional restitution of warm ischaemically damaged kidneys. There was a significant positive effect after 60 min of warm ischaemia when compared with the appropriate groups with CS. However, with the extension of the WIT to 90 and 120 min, we could find no advantage of our ROP method.

For human NHBD, the maximum acceptable WIT is considered to be less than 30–40 min [2]. In our set of experiments, ischaemic tolerance was surprisingly much higher than expected. After 90 min of warm ischaemia without in situ anticoagulation, 10 of 13 kidneys had moderate or good initial function regardless of the conservation method applied. Even after 120 min of WIT, 2/6 kidneys functioned primarily. Nevertheless, we had to stop further evaluation in these groups because of missing approval of the animal rights committee, since it was not expected that ROP had a relevant positive effect after 120 min of warm ischaemia.

There are several explanations for the extended ischaemic tolerance we observed, at least in some of the kidneys. Ischaemic tolerance of porcine kidneys per se might be higher or acute. Ischaemic tolerance of porcine kidneys per se might be higher or acute complete ischemia has different effects when compared with the situation of NHBD with a preceding depression of circulation including activation of a cascade of cytokine release. Another explanation could be that the effects of warm ischaemia injury of the kidney so far described are simply overestimated.

Consistent with our results, canine kidneys have been transplanted successfully by others after 60 min WIT and 24 h of ROP [15], and in an experimental study of Leone et al. [16], a maximum time of 50 min of WIT was described for porcine kidneys in an NHBD situation without additional treatment. Rolles et al. [17] transplanted kidneys in 1984 in 10 patients with a maximum WIT of 55 min and a median time of ROP of 21.5 h. Although several experimental studies [18,19] and the clinical pilot trial of Rolles et al. [17] have demonstrated beneficial effects of ROP, this method has not yet reached the status of routine clinical application.

An additional advantage of our ROP treatment consists in the administration of SOD as a scavenger for radicals. It is known that reperfusion or reoxygenation after a period of ischaemia affects the vascular system by generation of oxygen free radicals. This can be counteracted by treatment with oxygen radical scavengers such as SOD or allopurinol. In a study on rat livers, our group has shown that addition of SOD before ROP reduces reperfusion injuries as indicated by decreased lipid peroxidation without affecting the positive effects of oxygen persufflation on the energy status [10,20]. For this reason, we have integrated these two principles of organ protection in our concept of ROP. The groups which underwent CS did not receive SOD because we aimed to compare our method with the standard procedures currently used in organ preservation.

In this trial, the animals in the groups 1–4 showed normal levels of lipid peroxidation, meaning that in these groups gaseous oxygen did not cause damage. The results of the animals in group 5 and 6 raise the impression that SOD may not be able to prevent oxidative damages when the WIT is extended beyond 90 min, but there was just one animal in each group. Concerning these results, it has to be considered that malondialdehyde was measured on day 7 after transplantation and therefore, no conclusions on the status directly after transplantation can be drawn. Answers to this question require examination of kidneys directly after preservation.

The cold ischaemic time (CIT) of 4–5 h with 4 h treatment as applied in this study is rarely achieved in clinical practice with a mean CIT of about 18 h for kidneys of deceased donors in Germany. So, it has to be questioned whether the beneficial effects of ROP demonstrated in this study might be transferred to the average clinical situation. Additional studies with longer CIT should be performed. For canine kidneys, and rat livers, it has already been shown that treatment with ROP has comparable beneficial effects whether applied for 2 h or for 24 h [11]. So clinical approaches with short-term ROP followed by a long cold preservation seem possible.

Concerning the groups with 60 min WIT, our results agree with previously published reports [5–9,11,15,17–19,21,22], demonstrating that ROP is an appropriate method to optimize kidney function in cases where delayed or no function is expected. In addition to the good functional parameters, the histological features of group 1 point to an accelerated regeneration after WIT possibly as a result of a better energy status. However, extension of the WIT to 90 and 120 min could not be successfully compensated for by this method. Even worse, group 4 with 90 min WIT followed by CS without ROP is almost as effective as the 60 min WIT followed by CS with ROP, where five out of six animals survived. Nevertheless, the maximum level of plasma creatinine and the level of plasma creatinine at the end of the trial in group 4 were significantly higher than in group 1 with 60 min WIT and ROP. From these findings, we have to conclude that for the pig kidney, ROP is only beneficial after the short WIT. As outlined earlier, porcine kidneys might have a higher ischaemic tolerance than human kidneys, which might be responsible for the fact that the advantage of ROP could only partially be assured after 90 min WIT.

Thus we have to draw further conclusions carefully.

In conclusion of our present results and those obtained from the liver model [9], we suggest that ROP is superior to CS at least for the limited WIT. Organ quality is significantly improved as shown by the functional parameters. Therefore, ROP seems an appropriate method to be used in cases of kidneys which are expected to develop delayed graft function. Whether ROP might be able to overcome longer WIT has to be studied with human kidneys preferentialy in comparison with MP. If ROP is also benefical for the human kidneys, then it would represent a simple, low-cost measure for organ restitution after severe warm ischaemic damage and perhaps other forms of damage, which might extend our possibilities to recruit organs of extended criteria donors or NHBD for transplantation [2,4].



   Acknowledgments
 
The authors gratefully acknowledge the valuable practical help of Simone Hess and Monika Strünker during the perioperative setting. The work is supported by the Deutsche Forschungsgemeinschaft (grant no. Pa 776/1-1) and by the Köln Fortune Program (Faculty of Medicine, University of Cologne, Germany).

*Results have been in part presented at the annual ATS meeting, 3 June 2003, Washington DC and at the Surgical Forum of the annual meeting of the German Society of Surgery, 30 April 2003.

Conflict of interest statement. None declared.



   References
Top
 Abstract
 Introduction
 Subjects and methods
 Discussion
 References
 

  1. Cumulative Data Eurotransplant Centers (ET, ONT), 1 January–31 December 1999
  2. Wijnen RMH, Booster MH, Stubenitsky BM, de Boer J, Heineman E, Kootstra G. Outcome of transplantation of non-heart-beating donor kidneys. Lancet 1995; 345: 1067–1070[CrossRef][Web of Science][Medline]
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Received for publication: 11. 6.05
Accepted in revised form: 3. 2.06


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