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Right arrow Transplantation - heart

Ann Thorac Surg 2001;71:278-283
© 2001 The Society of Thoracic Surgeons

Original article: cardiovascular

Posttransplant function of a nonbeating heart is predictable by an ex vivo perfusion method

Kotaro Suehiro, MDa, Makoto Mohri, MDa, Hiroki Yamaguchi, MDa, Masami Takagaki, MDa, Kunikazu Hisamochi, MDa, Toru Morimoto, MDa, Shunji Sano, MD, PhDa

a Department of Cardiovascular Surgery, Okayama University Medical School, Okayama, Japan

Accepted for publication April 25, 2000.

Address reprint request to Dr Sano, Department of Cardiovascular Surgery, Okayama University Medical School, 2-5-1 Shikata-cho Okayama 700-8558, Japan
e-mail: s_sano{at}cc.okayama-u.ac.jp


   Abstract
Top
 Abstract
Introduction
 Material and methods
 Results
 Comment
 Acknowledgments
 References
 
Background. We attempted to predict the posttransplant cardiac function of nonbeating donor hearts.

Methods. A total of 13 dogs were studied. Hearts were left in situ for 45 minutes after cardiac arrest caused by exsanguination. Hearts were then excised and reperfused in an ex vivo perfusion apparatus after 60 minutes of warm ischemia to test whether they could eject against an 80 mm Hg afterload from a preload of 10 mm Hg. Thereafter, all hearts were transplanted orthotopically.

Results. Four of 13 hearts were able to eject in the apparatus (group A). However, the other nine hearts could not eject under the defined conditions (group B). All four hearts in group A showed good posttransplant hemodynamics (systolic arterial pressure > 80 mm Hg with mean left atrial pressure < 10 mm Hg) without dopamine. However, none of nine hearts in group B could support the circulation without dopamine.

Conclusions. Nonbeating donor heart function evaluated in the perfusion apparatus predicts posttransplant heart function. This method may be applicable for selection of transplantable hearts from nonbeating heart donors.


   Introduction
Top
 Abstract
 Introduction
Material and methods
 Results
 Comment
 Acknowledgments
 References
 
Cardiac transplantation is accepted as a standard treatment for patients with end-stage cardiac disease. However, the number of heart transplantation has achieved a plateau since 1990, despite the practice of using marginal donors to expand the donor pool. Some reports suggest that there has even been a decline in the number of donors recently [1]. A shortage of donor organs remains a worldwide problem.

Non-heart-beating donors (NHBDs) could be an important potential source of donor organs. Experimental studies of the use of hearts from NHBDs have been performed since the 1960s [2]. However, clinical application of these methods is still difficult, mainly because of the uncertainty of contractile function of the nonbeating hearts. Because these hearts undergo prolonged normothermic ischemia during cardiac arrest and reperfusion injury during resuscitation, they likely have completely different quality and function from those they had before cardiac arrest. However, if heart function can be evaluated before transplantation, the use of NHBDs for heart transplants could become feasible.

In the present study, we reperfused hearts that had undergone 60-minutes of normothermic arrest and evaluated their function under controlled preload and afterload conditions using an ex vivo perfusion apparatus before orthotopic transplantation. Cardiac function was then assessed in vivo after transplantation. We tested the hypothesis that good outcome after transplantation was correlated with good performance on the ex vivo perfusion apparatus.


   Material and methods
Top
 Abstract
 Introduction
 Material and methods
Results
 Comment
 Acknowledgments
 References
 
All animals used in this study received humane care in compliance with the "Guide for the Care and Use of Laboratory Animals" (NIH publication 85–23, revised 1985).

Overview of study
Thirteen dogs were exsanguinated to induce cardiac arrest. The hearts were left in situ for 45 minutes. The hearts were then excised and reperfused after a total of 60 minutes of warm ischemia in an ex vivo perfusion apparatus, which allowed for control of preload and afterload (see below). The hearts that could eject against 80 mm Hg of afterload from a preload of 10 mm Hg in the apparatus were assigned to group A, whereas hearts that could not eject under these conditions were assigned to group B. All hearts were transplanted orthotopically, and the posttransplantation cardiac function was evaluated and correlated with pretransplantation function.

Ex vivo perfusion apparatus
In the present study, we used an ex vivo perfusion apparatus to reperfuse and evaluate donor heart function (Fig 1). This apparatus consisted of a reservoir, two roller pumps, an oxygenator with a heat exchanger, two arterial ultrafilters, an air cushion, a preload chamber, a Starling resistor, and polyvinyl chloride tubing. Preload can be set by changing the height of the chamber. Afterload can be controlled by applying air pressure into the Starling resistor. In this study, we set the pressure of the Starling resistor at 80 mm Hg, which has frequently been used in physiologic experiments of dog hearts [3] to simulate conditions after orthotopic heart transplantation.



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  		Fig 1. Perfusion apparatus.

 
Donor heart preparation
Thirteen dogs, weighing 17 to 24 kg (21.7 ± 2.5 kg), served as donors. The dog was anesthetized with intramuscular ketamine hydrochloride (0.3 mg/kg) and intravenous sodium pentobarbital (5 mg/kg), and then mechanically ventilated. The right femoral artery and vein were cannulated for systemic arterial pressure monitoring and fluid infusion, respectively. Arterial blood gas was analyzed at 30-minute intervals using a blood gas analyzer (OMNI-5, AVL List GmbH Medizintechnik, Austria).

The chest was entered through a midline sternotomy. A microtip manometer (model SPC-350, Millar Instruments, Houston, TX) and a conductance catheter (Cordis Europa, Roden, The Netherlands) were introduced into the left ventricle (LV) through the apex to record instantaneous pressure-volume loops with a signal conditioner (Sigma 5, Leycom/CardioDynamics, Zoetermeer, The Netherlands). A catheter was inserted into the left atrium (LA) to measure LA pressure. A length of umbilical tape was placed around the inferior vena cava for gradual occlusion during pressure-volume loop recordings.

A 14F cannula was then inserted into the left femoral artery. Without any pretreatment or heparinization, exsanguination was initiated. Blood pressure dropped, and cardiac arrest (defined as standstill or ventricular fibrillation on electrocardiogram) was achieved. The heart was left in situ for 45 minutes after cardiac arrest. The heart was then excised, and the ascending aorta and the LA appendage were connected to the ex vivo perfusion apparatus as shown in Figure 1, to perfuse the coronary arteries and infuse blood into the LA as preload. These procedures for ex vivo preparation required approximately 15 minutes, so that the total duration of warm ischemia was 60 minutes. The microtip manometer and the conductance catheter were reinserted into the LV.

The heart was carefully reperfused, as we reported previously [4], using substrate-enriched warm-blood cardioplegic solution containing 0.5 µg/mL of EPC [5, 6], a hydroxyl radical scavenger, and 120,000 U of urokinase. After 15 minutes of reperfusion with warm-blood cardioplegic solution, the heart was perfused with oxygenated autologous blood, which was obtained during exsanguination. When ventricular fibrillation occurred, the heart was immediately defibrillated. The heart rate was maintained at more than 130 beats/min using atrial pacing. Initially, the heart was perfused at a pressure of 40 mm Hg. The perfusion pressure was then gradually increased to 80 mm Hg over the course of 1 minute. After 30 minutes of coronary perfusion with oxygenated blood, 10 mm Hg of preload was applied, and retrograde coronary perfusion was carefully withdrawn over the course of 1 to 2 minutes. When the heart could eject against 80 mm Hg of afterload, LV function was evaluated. Thereafter, the ascending aorta was clamped, and 15 mL/kg of cold (4°C) St. Thomas’s solution was infused into the coronary arteries. The heart was then preserved in cold (4°C) University of Wisconsin solution.

When the hearts could not eject against 80 mm Hg of afterload in the perfusion apparatus, blood infusion into the LA was stopped immediately. Retrograde coronary perfusion was continued for an additional 15 minutes, and the heart was then preserved in the same fashion.

Recipient preparation
Thirteen size-matched dogs served as recipients. The induction of anesthesia was performed in the same way as for the donors. After a median sternotomy, each recipient was systemically anticoagulated with heparin (250 U/kg). An arterial cannula was inserted into the left femoral artery, and venous cannulas were inserted into the superior vena cava and the inferior vena cava. Cardiopulmonary bypass (CPB) was initiated, and the dog was cooled to a rectal temperature of 28°C. The recipient’s heart was excised, and the donor heart was transplanted orthotopically as described by Lower and coworkers [7]. Catheters were inserted into the heart in the same fashion described above for the donors to measure cardiac function. After the terminal warm-blood cardioplegia, the aortic cross-clamp was released. Heart rate was maintained by atrial pacing at a rate greater than 130 beats/min and posttransplantation cardiac function was evaluated.

At the end of the experiment, the hearts were excised, and the coronary arteries and veins were incised as far as possible to evaluate for the presence of thrombi.

Protocol
Baseline cardiac function was measured before exsanguination (preexsanguination).

After reperfusion of the heart in the perfusion apparatus, the second evaluation of heart function was performed. If the heart could maintain ejection for 15 minutes after withdrawal of retrograde coronary perfusion, the hearts were considered to be weaned from retrograde coronary perfusion, and cardiac function was assessed (postreperfusion).

The third assessment was performed after transplantation. The hearts were assisted with CPB for 1 hour after aortic unclamping and then gradually weaned from CPB with 5 µg · kg-1 · min-1 dopamine infusion. At 1 hour after weaning from CPB, with systolic arterial pressure maintained greater than 80 mm Hg with LA pressure less than 10 mm Hg, the heart was considered to be successfully weaned from CPB, and cardiac function was assessed (posttransplantation with dopamine).

Finally, dopamine infusion was stopped. If the hemodynamics as indicated above were maintained 30 minutes after stopping dopamine infusion, the heart was considered to be successfully weaned from dopamine, and the last measurements were performed (posttransplantation without dopamine).

Systolic LV pressure, LV end-diastolic pressure, the positive and negative first derivatives of LV pressure (LV max +dp/dt, LV max -dp/dt), and LV end-systolic pressure-volume relation were measured as indices of LV function. The slope of the LV end-systolic pressure-volume relation was calculated using the software package provided by Taisho Biomedical Instruments Co (Osaka, Japan). The physiologic signals were recorded on a polygraph (EP-1200, NEC, Tokyo, Japan).

Statistical analysis
Results are expressed as mean ± standard deviation, unless otherwise indicated. An analysis was performed by the Mann-Whitney test to compare the data between the groups. A p value of less than 0.05 was considered statistically significant.


   Results
Top
 Abstract
 Introduction
 Material and methods
 Results
Comment
 Acknowledgments
 References
 
Ex vivo studies
The outcomes after reperfusion and transplantation were summarized in Figure 2. Four of 13 hearts could eject against 80 mm Hg of afterload for more than 15 minutes in the perfusion apparatus after weaning from coronary perfusion (group A). The other nine hearts could not eject against 80 mm Hg of afterload (group B).



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  		Fig 2. The outcomes after reperfusion and transplantation. (CPB = cardiopulmonary bypass.)

 
The weight of donor dogs was not significantly different between two groups (group A, 22.0 ± 1.8 kg; group B, 21.6 ± 2.8 kg). The condition of cardiac arrest (standstill or ventricular fibrillation), the exsanguination period (time from initiation of exsanguination to reaching zero blood pressure), the agonal period (time from initiation of exsanguination to cardiac arrest), the ischemic period (time from the initiation of preservation to aortic unclamping), the CPB time (time from initiation to termination of CPB), and the aortic cross-clamp time (time from aortic cross-clamping to unclamping) were not significantly different between two groups (Table 1).


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  		Table 1. Procedure Variablesa

 
Outcomes after transplantation
After transplantation, all four hearts in group A and six of nine hearts in group B were successfully weaned from CPB with 5 µg · kg-1 · min-1 dopamine. All hearts in group A could maintain a systolic arterial pressure more than 80 mm Hg with an LA pressure less than 10 mm Hg without inotropic support. On the other hand, none of the six hearts in group B that were successfully weaned from CPB with dopamine could maintain the same hemodynamics without dopamine (Fig 2).

Three of four hearts in group A and seven of nine hearts in group B needed atrial pacing to maintain the heart rate greater than 130 beats/min. Complete atrioventricular block was found in one heart in group B.

Cardiac function
The changes in hemodynamics and LV function are summarized in Tables 2 and 3, respectively. The hemodynamics and indices of cardiac function at baseline were not significantly different between the two groups. The hearts in group A showed significantly higher systolic pressure (86 ± 6 versus 70 ± 7 mm Hg; p < 0.05) with lower LA pressure (9 ± 1 versus 12 ± 2 mm Hg; p < 0.05) than the hearts in group B at posttransplantation without dopamine. At posttransplantation without dopamine, the hearts in group A showed significantly higher systolic LV pressure (90 ± 10 versus 71 ± 7 mm Hg; p < 0.05) and tended to have better slope of the LV end-systolic pressure-volume relation (4.1 ± 2.6 versus 2.7 ± 1.3 mm Hg/mL; p = 0.08) than those in hearts in group B (Table 3). However, LV end-diastolic pressure, LV max +dp/dt, and LV max -dp/dt were not significantly different between the two groups.


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  		Table 2. Hemodynamicsa

 

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  		Table 3. Left Ventricular Functiona

 
Thrombi in coronary arteries and veins
After completing the protocol, the hearts were excised, and the coronary arteries and veins were incised as far as possible to look for evidence of thrombi. No thrombi were found in the major coronary arteries and veins after transplantation in any hearts.


   Comment
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
Acknowledgments
 References
 
We demonstrated that prediction of posttransplantation function of nonbeating hearts may be feasible using ex vivo perfusion techniques.

Dead on arrival patients as heart donors
In 1995, the First International Workshop on NHBDs was held. Although the workshop focused on renal transplantation, the importance of the use of NHBD organs were reconfirmed in this workshop [8], and "dead on arrival" patients were thought to be a potentially large source of donor organs [9].

Trauma deaths, the most common cause of death for individuals younger than 44 years of age, are estimated to occur at a rate of approximately 140,000/y in the United States [10]. Many of these patients would meet criteria for dead on arrival, although only a small number of them underwent tissue retrieval [11]. These patients might have the possibility of being organ donors. However, there is currently no method to evaluate and use the hearts of these subjects.

Several investigators have reported successful transplantations of NHBD hearts in animal models [12–16]. Most of these studies simulated conditions that would occur during retrieval of nonbeating hearts from the patients whose treatment was being withdrawn in the intensive care unit. This setting may be reasonable for the clinical application. However, to enlarge the donor pool further, we focused on establishing a method to use another kind of NHBDs, dead on arrival patients.

Superiority of ex vivo perfusion system
The results of the present study suggested that the hearts harvested from NHBDs should be evaluated and selected for use based on an assessment of cardiac function before transplantation. To assess function of these hearts, they must be perfused either in vivo or ex vivo. We used a Langendorff-type perfusion apparatus in the present study to reperfuse and evaluate the donor heart before transplantation because of some advantages over an in vivo setting.

One of the advantages of this system is feasibility of controlled reperfusion and complete LV unloading, which are difficult with in situ resuscitation techniques using CPB [12]. In addition, control of hyperkalemia, which inevitably occurs in the cadaver body after prolonged cardiac arrest, was easily controlled using an ex vivo system.

Another advantage of using the isolated heart approach is related to exclusion of thrombi. Although thrombus formation after prolonged cardiac arrest is one of the major concerns, the amount and distribution of thrombi in cadaver hearts is not clear. Therefore, we performed three separate preliminary studies concerning this issue.

In all dogs, massive thrombi were found in the inferior vena cava after 60 minutes of cardiac arrest caused by exsanguination without anticoagulation. One heart had thrombi in both ventricles. Two of three dogs had small amounts of thrombi in the right atrium. However, interestingly, no thrombi were found in the major coronary arteries and veins.

Kloner and colleagues [17] reported that thrombi were infrequently seen by electron microscopy and were not seen by light microscopy in sections of tissue obtained 10 to 12 seconds after release of a 90-minute occlusion of the coronary artery or in the tissue made ischemic for 90 minutes.

Based on these findings, and because Gundry and associates [18] reported successful transplantation of cadaver hearts from exsanguination using streptokinase, we concluded that all the visible thrombi in the cardiac chambers could be removed directly and all microthrombi could be excluded with urokinase. These procedures could be accomplished easier using an excised heart.

Cardiac function
The outcomes obtained in the perfusion apparatus were closely correlated to the outcomes after transplantation. Namely, all the hearts that were weaned from coronary perfusion in the perfusion apparatus could maintain good hemodynamics after transplantation. Moreover, the hearts in group A showed systolic function comparable to the baseline function after transplantation without inotropic support. Therefore, it is suggested that donor heart selection using this kind of ex vivo perfusion system may be feasible.

Regarding the diastolic function, LV max -dp/dt was decreased after transplantation in both groups, whereas systolic function was relatively maintained. This tendency was also observed in our previous report [4]. Myocardial edema, myocardial contracture, and vascular dysfunction are considered to contribute to this abnormality [19].

Limitation
In the present study, dogs were exsanguinated as a model of a trauma death. However, in the clinical setting, there are not many fatalities from pure exsanguination. In addition, most trauma victims or victims of other types of exsanguinating hemorrhage receive massive resuscitative efforts, eg, transfusions, vasoactive drugs, inotropic agents, and cardiac massage, which may further attenuate cardiac function. Therefore, for the clinical application of this technique, all these factors should be included and assessed, although simulation of these factors in an experimental model may be a challenge.

The current technique of resuscitation allowed only 4 of 13 hearts to be resuscitated. Although this poor outcome must be improved using better reperfusion and preservation techniques, the rate of recovery after prolonged ischemia includes potential limitations. Probably most of the hearts from dead on arrival patients may have similar problems. However, emergency room staff encounter that some patients who are dead on arrival show incredible recovery for some reason. Therefore, we hypothesized that this may be seen even after declaration of death. Although the numbers of viable grafts found among these nonbeating hearts may be limited, abolition of all the hearts in dead on arrival patients can be avoided.

Conclusion
We demonstrated that pretransplant donor heart function evaluated in our perfusion apparatus correlated well with the outcomes after orthotopic heart transplantation. Many dead on arrival patients die without evaluation for cardiac transplantation. However, some of them have the potential to be organ donors. We propose an approach for evaluating hearts from such patients, which has the potential to substantially increase the donor pool.


   Acknowledgments
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 Acknowledgments
References
 
The authors thank Dr Atsushi Aoki for his suggestions and encouragement. This study was supported in part by Senju Pharmaceutical Company Co, Ltd, Osaka, Japan. The volumetric conductance catheter and the model Sigma 5 were provided by Taisho Biomedical Instruments Co, Ltd, Osaka, Japan. The blood gas analyzer (OMNI 5) was generously provided by AVL List GmbH, Medizintechnik, Austria.


   References
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 Acknowledgments
 References
 

  1. Hosenpud J.D., Bennett L.E., Keck B.M., Fiol B., Boucek M.M., Novick R.J. The Registry of the International Society of Heart and Lung Transplantation: Sixteenth Official Report—1999. J Heart Lung Transplant 1999;18:611-626.
  2. Wuerflein R.D., Shumway N.E. Resuscitation and function of the cadaver heart. Circulation 1967;35:I92-I95.
  3. Patterson S.W., Starling E.H. On the mechanical factors which determine the output of the ventricles. J Physiol (Lond) 1914;48:357-379.
  4. Suehiro K., Mohri M., Takagaki M., Hisamochi K., Morimoto T., Sano S. The effect of graft perfusion with warm blood cardioplegia for cadaver heart transplantation. Surg Today 1999;29:890-896.
  5. Mori A., Edamatsu R., Kohno M., Ohmori S. A new hydroxyl radical scavenger: EPC-K1. Neuroscience 1989;15:371-376.
  6. Inoue M. [Effect of phosphate diester linkage of vitamin E, and vitamin C (EPC-K1) on myocardial ischemia reperfusion injury in the isolated working rat heart. Nippon Kyobu Geka Gakkai Zasshi 1997;45:742-749.
  7. Lower R.R., Stofer R.C., Shumway N.E. Homovital transplantation of the heart. J Thorac Cardiovasc Surg 1961;41:196-204.
  8. Kootstra G. Statement on non-heart-beating donor programs. Transplant Proc 1995;27:2965.
  9. Kootstra G., Daemen J.H., Oomen A.P. Categories of non-heart-beating donors. Transplant Proc 1995;27:2893-2894.
  10. Papadopoulos I.N., Bukis D., Karalas E., et al. Preventable prehospital trauma deaths in a Hellenic urban health region: an audit of prehospital trauma care. J Trauma 1996;41:864-869.
  11. Pasquale M.D., Rhodes M., Cipolle M.D., Hanley T., Wasser T. Defining "dead on arrival:" impact on a level I trauma center. J Trauma 1996;41:726-730.
  12. Takagaki M., Hisamochi K., Morimoto T., Bando K., Sano S., Shimizu N. Successful transplantation of cadaver hearts harvested one hour after hypoxic cardiac arrest. J Heart Lung Transplant 1996;15:527-531.
  13. Morimoto T., Hisamochi K., Teramoto S. Transplantation of the canine cadaver heart using a core-cooling technique. Acta Med Okayama 1993;47:199-207.
  14. Hisamochi K., Morimoto T., Bando K., Senoo Y., Teramoto S. A new hydroxyl radical scavenger "EPC" on cadaver heart transplantation in a canine model. Surg Today 1997;27:930-935.
  15. Gundry S.R., Fukushima N., Eke C.C., Hill A.C., Zuppan C., Bailey L.L. Successful survival of primates receiving transplantation with "dead," nonbeating donor hearts. J Thorac Cardiovasc Surg 1995;109:1097-1112.
  16. Shirakura R., Matsuda H., Nakano S., et al. Cardiac function and myocardial performance of 24-hour-preserved asphyxiated canine hearts. Ann Thorac Surg 1992;53:440-444.
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