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Eur J Cardiothorac Surg 2005;28:143-148
© 2005 Elsevier Science NL

Outcome of hearts with cold ischemic time greater than 300minutes. A case-matched study

Heart Transplant Program, University of California, Los Angeles Medical Center, Los Angeles, CA, USA

Received 5 September 2004; received in revised form 3 January 2005; accepted 12 January 2005.

^* Corresponding author. Address: Division of Cardiothoracic Surgery, David Geffen School of Medicine at UCLA, 10833 Le Conte Ave., 62-266B CHS, Box 95741, Los Angeles, CA 90095-1741, USA. Tel.: +1 310 206 8232; fax: +1 310 825 7473. (Email: fmitropoulos{at}sprintmail.com).

	Abstract

Top Abstract 1. Introduction 2. Patients and methods 3. Results 4. Discussion Appendix A. Conference... References

 
Objective: Expansion of potential donor pool may be facilitated by using cardiac allografts with long ischemic time. Early graft failure and potential relation to transplant coronary artery disease remains a concern. We sought to evaluate outcomes of heart transplantation in recipients of donor allografts with prolonged ischemia time. Methods: The study group consisted of 46 (mean age, 52 years) consecutive patients at UCLA from 1994 to 2002 that underwent heart transplantation with ischemia time >300min. This group was compared to a case-matched control group of 46 (mean age, 51 years) patients identified from our database during this time frame for the following factors: UNOS status, congenital heart disease diagnosis, preop inotropes, pretransplantation creatinine>1.5 and recipient age. Primary endpoint was mortality and secondary were rejection rate and transplant coronary artery disease. Allografts were perfused and stored in cold University of Wisconsin solution. Results: Mean donor ages of the study and case-matched control group were 34±15 and 34±14 years, respectively. Mean ischemia times were 388 (range, 301–600min) and 173 (range, 96–236min), respectively. The death incidence rate per 100 transplants per year was 9% for the study group and 7.4% for the matched group (P=0.50). Thirty-day mortality for the study and case-matched groups were 4.3 and 2.1%, respectively (P=0.9). Late mortality was 16.5 and 18.5%, respectively (P=0.9). The risk of death after 30 days was 7.5 and 5.8%, respectively (P=0.5, log-rank). One-year incidence of acute cellular rejection in the study and case-matched groups were 2 and 4.5% (P=0.36), respectively. One-year incidence of transplant coronary artery disease in the study and case-matched groups were 4.3 and 5.4%, respectively (P=0.68). Conclusions: Donor hearts with ischemia time greater than 300min provide comparable early and intermediate outcomes given judicious and careful donor and recipient matching and our current techniques of myocardial preservation and modified reperfusion.

Key Words: Prolong ischemia time • Cardiac allograft • Orthotopic heart transplantation

	1. Introduction

Top Abstract 1. Introduction 2. Patients and methods 3. Results 4. Discussion Appendix A. Conference... References

 
The success of orthotopic heart transplantation (OHT) for patients with end-stage heart disease in combination with the limited donor availability has resulted in a dramatic increase of the waiting lists and waiting times. At UCLA, efforts to shorten waiting times have focused on expanding the donor pool by broadening the standard donor criteria to include: older donors, high-dose inotropic support (dopamine>10µg/kg per min), hearts with coronary artery disease (CAD), left ventricular hypertrophy (LVH), depressed ejection fraction (EF), suspected myocardial contusion, recent cardiac arrest, reused donor hearts, donors with hepatitis B or C positive and prolonged ischemia time [1,2].

The usual accepted time limit for organ preservation in human heart transplantation is up to 4–5h. Prolonged donor ischemic times (PIT) have been associated with need for higher inotropic support within the first 48h postoperatively, depressed postoperative left ventricular ejection fraction (LVEF), right ventricular dysfunction, prolong hospital stay, increased graft dysfunction, higher morbidity and early mortality [3–8].

Preservation with the University of Wisconsin solution (UW) and the improvement in myocardial reperfusion techniques have resulted in less myocardial injury as a result of ischemia and acceptance of non-standard donor hearts [9,10].

There is paucity of clinical data in the literature evaluating the impact of prolong ischemia time (>300min) on the immediate mortality, incidence of transplant coronary artery disease (TCAD) and rejection rate in a sizeable series of adult patients with long-term follow-up. In this study, we reviewed the outcome of patients that received cardiac allografts with cold ischemia time (CIT) greater than 300min and compared with a case-matched group of patients who received allografts with CIT<240min.

	2. Patients and methods

Top Abstract 1. Introduction 2. Patients and methods 3. Results 4. Discussion Appendix A. Conference... References

 
2.1. Study population
2.1.1. Matched case-control study
Between 1994 and 2002, 48 patients who received cardiac allografts with cold ischemic time greater than 300min were identified from our database at UCLA Medical Center. Forty-six patients comprise the long ischemia time (LIT) study group (group A), since two patients were excluded (one due to the ventilator status and the other one due to the lack of sufficient follow-up data at that time). Twelve patients were transplanted during the first half of the study period and 34 over the second half.

They were matched with 46 randomly selected controls (group B) whose donor's ischemia time was less than 240min identified from our database during the same time frame for the following factors: UNOS status, congenital heart disease diagnosis, preoperative use of inotropes, pretransplantation serum creatinine>1.5 and recipient age (Table 1 ).

Congenital heart disease diagnosis: odds-ratio 2.42, P=0.0004

Ventilator: odds-ratio 2.53, P<0.0001

In hospital (including ICU): odds-ratio 2.51, P<0.0001

Intravenous inotropes: odds-ratio 0.54, P<0.0001

Dialysis: odds-ratio 2.58, P<0.0001

Since these factors are so significantly associated with mortality, elimination from the study groups or random matching of the patients for these factors would allow the identification of the other factors (such as the donor ischemia time) and their impact on outcome.

2.1.2. Exclusions
Since all the recipients in the long ischemia group were not on the ventilator, ventilated recipients were excluded from the matching process. Patients less than 16 years of age were excluded. Patients with inadequate follow-up were excluded as well.

2.2. Listing and donor allocation
Candidates for orthotopic heart transplantation are discussed on a weekly multidisciplinary conference and accepted by a consensus opinion. Donors and recipients are matched for ABO blood type compatibility and size. Panel reactive antibodies (PRA) are routinely performed. Patients with greater than 10% PRA undergo prospective crossmatching. If broadly positive (>25%) and/or previous positive prospective crossmatch, preoperative plasmapheris and/or treatment with intravenous immunoglobulin (IVIG) are performed in an effort to reduce the level of circulating antibodies.

2.3. Preservation and operative technique
Thyroid hormone infusion (T4) was started several hours prior to organ retrieval. Donor hearts were perfused with UW solution at a constant pressure of 60mmHg over a 7–10min period (8–10cm³/kg), and were transported immersed in hypothermic UW solution at 4°C. At the time of implantation, cold plasmalyte solution was infused into the left ventricle to aid in topical cooling and de-airing. Reperfusion consisted of leukocyte-depleted, aspartate/glutamate enriched, warm blood cardioplegia solution (Buckberg solution) for a total of 3–4min followed by warm blood cardioplegia for 4–10min at a pressure of 60mmHg. Bicaval anastomosis was used for the right atrium. Postoperatively patients receive inhaled nitric oxide if the mean pulmonary artery pressure was greater than 25mmHg and left atrial pressure <12mmHg [12].

An experienced cardiac surgeon with expertise in thoracic organ procurement is usually involved. Frequently, the procurement team spends considerable time in the field optimizing the donor.

2.4. Immunosuppression
Methylprednisolone (7mg/kg) is given at the time of reperfusion and again upon separation from the cardiopulmonary bypass followed by a dose of 125mg every 12h for three doses. Oral prednizone is initiated at 1mg/kg per day and tapered to 0.1mg/kg per day. For patients with few rejections at 6 months complete weaning from steroids is attempted and has been achieved in 70% of selected recipients.

Since 1998 Mycophenolate mofetil at a dose of 1000mg twice a day and since 2001 Tacrolimus at a dose of 1mg/kg have been the standard postoperative immunosuppressive regimen. Induction therapy is not utilized routinely.

Sample spleen and lymph nodes are obtained from all donors at procurement and lymphocytes are tested against serum from recipients. Right heart catheterization and myocardial biopsies are performed weekly for the first month, every 2 weeks for 2 months, monthly for 3–6 months and bimonthly up to the first year post-transplant. TCAD is monitored with annual coronary angiography and intravascular ultrasound. All patients are discharged on pravastatin and aspirin as well [13].

2.5. Statistical analysis
Data analysis was performed using STATA (Stata Corporation, College Station, TX). Indicated data are reported as mean±SD. Differences in matched proportions were compared using McNemar's and Fisher exact tests. All tests were two-sided and a significant P-value was defined less than 0.05.

Survival and transplant coronary artery disease free rates were analyzed with standard Kaplan–Meier actuarial techniques along with a log-rank P-value. Early mortality was defined as death within 30 days post-transplant. Late mortality was defined as any death occurring later than 30 days post-transplant. Hospital mortality was defined as any death that occurred while the patient was still in the hospital following his original OHT procedure.

	3. Results

Top Abstract 1. Introduction 2. Patients and methods 3. Results 4. Discussion Appendix A. Conference... References

 
3.1. Donors
Mean donor ages of the study and case-matched control group were 34±15 and 34±14 years, respectively. Mean donor ischemia time was 388 (range, 301–600) and 173 (range, 96–236min), respectively. The donor causes of death in the LIT study group (n=40) and the case-matched control group (n=46) included blunt head trauma in 35 vs 30%, drug overdose in 3 vs 0%, atraumatic intracranial bleeding in 30 vs 37%, gunshot wounds in 28 vs 22%, and due to other causes in 4 vs 8%, respectively (Table 2 ). There was no statistical significance between these two groups (P=0.80 by Fischer's exact).

The mean value of the preoperative mean pulmonary artery pressure was 22.1mmHg (range, 8–49) for the study group and 23.1mmHg (range, 15–38) for the case-matched group (P=0.29).

Thirty-day mortality for groups A and B were 4.3 (2/46) and 2.1% (1/46), respectively (P=0.9). Late mortality was 16.5% (7/43) for group A and 18.5% (8/43) for group B (P=0.9).

The death incidence rate per 100 transplants per year was 9% for the study group and 7.4% for the matched group (P=0.5). The risk of death after 30 days was 7.5% for the study group and 5.8% for the matched group (P=0.5, log-rank).

The conditional 1-year incidence of biopsy-proven (Grade 3A or greater) acute cellular rejection for groups A and B was 2 and 4.5%, respectively, and was not statistically significant (P=0.35%). Kaplan–Meier estimates of actuarial rejection-free survival rates are shown in Fig. 1 .

View larger version (16K): [in this window] [in a new window]   Fig. 1. Kaplan–Meier estimates of actuarial rejection-free survival rates between the long ischemia time group and the case-matched group.

Kaplan–Meier estimates of actuarial TCAD-free survival rates are depicted in Fig. 2 .

View larger version (15K): [in this window] [in a new window]   Fig. 2. Kaplan–Meier estimates of actuarial TCAD-free survival rates.

	4. Discussion

Top Abstract 1. Introduction 2. Patients and methods 3. Results 4. Discussion Appendix A. Conference... References

Whether these improvements can allow prolongation of the ischemia time in an effort to counteract the shortage of donors remains a critical question that seeks a timely answer.

The use of allografts with ischemia times greater than 4–5h has been associated with a need for higher inotropic support within the first 48h, reduced postoperative left ventricular ejection fraction, right ventricular function, prolonged hospital stay, increased graft dysfunction, and higher morbidity and early mortality [3–8]. It is believed that although LIT could negatively affect the postoperative course the long-term outcome might not be adversely affected. Available clinical data in the literature are conflicting and limited by small number of patients without significant long-term follow-up. Endpoints that are of significant clinical relevance and pertinent to the use of are the immediate and long-term mortality, incidence of TCAD and rejection rate.

Since 1992, we have used cardiac allografts with IT greater than 300min in 46 patients. Being located in Los Angeles we have traveled and procured organs from the Northeast and Southeast United States, Hawaii, and as far as Alaska. This policy has resulted on an average of six extra grafts per year.

Kawauchi et al. found that pediatric patients who received donor hearts with ischemia time greater than 4h when compared to a group with IT<4h demonstrated diminished cardiac function in the first postoperative week (primarily posterior wall diastolic movement) with functional recovery after the second week [15]. Serum cardiac myosin light chain levels were also higher during the first week in the LIT group but the difference was not evident beyond the first week in either group [16]. Of note was the fact that inotropic support was required for 5.3±3.7 days for the long ischemia time group vs 3.9±3.3 days for the short ischemia time group (not statistical significant).

In our series, the mean duration of inotropic support was 3.4 days for the study group and 3.3 days for the matched group (P=0.35). Nitric oxide was required in 4/46 and 3/46 patients, respectively.

Ischemia–reperfusion injury or extensive cytokine release could explain the temporary myocardial dysfunction [7]. Since the phenomenon of postoperative myocardial dysfunction is temporary, oversized allografts could provide a solution for this problem.

Briganti et al. compared a group of patients with IT less than 240min to a group with IT 240–300min and to a group with IT greater than 300min. They found a statistical significant decrease in left ventricular function in the greater than 300min group compared with the less than 200min group (P=0.01), which did not translate into long-term compromised functional recovery [8].

Scheule et al. compared pediatric patients with IT>8h to those with IT less than 90min. They found no difference in the length of inotropic support, rejection episodes, TCAD, hospital readmissions or late outcome. The duration of cardiopulmonary bypass was longer in the group with the long IT which they attribute to planned longer reperfusion time [17]. The Loma Linda group over the years has made a considerate effort to prolong ischemia times with significant results [15–17].

Although we included patients with congenital heart disease in our study age less than 16 years was an exclusion criterion. Our analysis included primarily adult population.

Multi-institutional studies concluded that long IT was an independent risk factor for early mortality post-transplantation (P=0.0003, relative risk 1.19), and advocate cautious extension of criteria for donor acceptance but with an anticipated greater risk in the presence of diffuse echocardiographic wall motion abnormalities and long anticipated ischemic time, particularly in older donors given inotropic support. The adverse effect of a longer ischemic time was most notable after 4h (1-month survival rate 71% for more than 4h vs 85% for less than 4h, P=0.0003) [5,6].

On the other hand, Pflugfelder et al. studied 219 transplant patients and found that long ischemia time (>3h) did not negatively affect 1-year survival [18].

Del Rizzo reports on 128 patients with IT greater than 4h and found no effect on survival. Cardiac allograft ischemia time did have an effect on survival if the donor age was >50 years and was used into urgent recipients [4]. These data illustrate that donor risk factors should be considered additive.

Mullen et al. from Canada compared two groups with IT less and greater than 4h and found no significant difference in the 30-day, 90-day or actuarial survival between these two groups (P=0.014, 0.027 and 0.27, respectively) [19].

The small number of patients and incomplete follow-up flaws single institution studies. On the other hand, multi-institutional registries compile data from centers with wide range of volume, individual institutional policy, experience and variability.

In an effort to answer these questions we design the study in such a way so that the ischemia time will be the only factor under question by comparing the study group to case-matched group and an unmatched group from the same database during the same time period [14].

In our study, the 30-day and late mortality for the study and case-matched groups were 4.3 (2/46) vs 2.1% and 16.5 vs 18.5%, respectively (P=0.9 for both variables).

The death incidence rate per 100 transplants per year was 9 and 7.4%, respectively (P=0.5). The risk of death after 30 days was 7.5 for the study group and 5.8% for the matched group (P=0.5, log-rank). None of these values reached statistical significance.

It has been hypothesized that ischemia plays a pathogenetic role in cardiac allograft vasculopathy [20]. Data from a rat cardiac allograft model showed that progression to chronic vasculopathy is principally an immunologic process accelerated by an ischemic insult to the allograft and mediated in part by T cells and macrophages [21].

The group from Columbia in a very elegant study compared four groups based on their donor ischemia time and found that prolong IT did not adversely affect long-term outcome and that there was no significant difference in freedom from TCAD among the four groups [14]. Although the group of patients with IT>300 was small (17 patients) they conclude that it can be safely extended to 5h [14].

In our series, 1-year conditional incidence of biopsy-proven (Grade 3A or greater) acute cellular rejection in the groups A and B were 2 and 4.5%, respectively (P=0.36). The 1-year incidence of TCAD was 4.3 and 5.4%, respectively (P=0.68). These data support the hypothesis that in the current era long ischemia time does not affect the incidence of rejection or TCAD.

In summary, we can conclude that donor hearts with ischemia time greater than 300min provide comparable early and intermediate outcomes given judicious and careful donor and recipient matching and our current techniques of myocardial preservation and modified reperfusion. We believe that donor hearts with prolong ischemia time should not be a contraindication for OHT. Careful evaluation of these allografts should be undertaken, taking into consideration the left ventricular ejection function, presence of LV hypertrophy, coronary anatomy, donor age, stability of the donor, UNOS status and co-morbidities of the recipient since the presence of more than one donor or recipient risk factors appear to have an additive effect.

	Appendix A. Conference discussion

Top Abstract 1. Introduction 2. Patients and methods 3. Results 4. Discussion Appendix A. Conference... References

 
Dr A. Pavie (Paris, France): We know everything of the UCLA transplantation program, but we are a little frustrated after your presentation because you didn't give us any data on the acute choice of such donor. You increase the ischemia time, but probably you choose an excellent donor using other criteria. We were also pleased to know how you weaned the patient from extracorporeal circulation, with which drugs and at which doses do you need sometimes cardiac assistance.

No time for reply.

	Acknowledgments

 
The authors would like to acknowledge the contribution of all the members of the UCLA Heart Transplant team. In particular, we would like to express our deepest appreciation to the transplant coordinators for their hard work.

	Footnotes

 
Presented at the joint 18th Annual Meeting of the European Association for Cardio-thoracic Surgery and the 12th Annual Meeting of the European Society of Thoracic Surgeons, Leipzig, Germany, September 12–15, 2004.

	References

Top Abstract 1. Introduction 2. Patients and methods 3. Results 4. Discussion Appendix A. Conference... References

 

1. Laks H, Marelli D, Fazio D, Kobashigawa J. Expanding the heart donor base. Curr Opin Organ Transplant 2000;5:134.
2. Marelli D, Laks H, Kobashigawa JA, Bresson J, Ardehali A, Esmailian F, Plunkett MD, Kubak B. Seventeen-year experience with 1,083 heart transplants at a single institution. Ann Thorac Surg 2002;74(5):1558-1566.[Abstract/Free Full Text]
3. Wahlers T, Cremer J, Fieguth HG, Dammenhayn L, Albes J, Schafers HJ, Haverich A, Borst HG. Donor related variables and 30-day mortality after heart transplantation. J Heart Lung Transplant 1991;10:22-27.[Medline]
4. Del Rizzo DF, Menkis AH, Pfungfelder PW, Novick RJ, McKenzie FN, Boyd WD, Kostuk WJ. The role of donor age and ischemic time on survival following orthotopic heart transplantation. J Heart Lung Transplant 1999;18(4):310-319.[CrossRef][Medline]
5. Young JB, Naftel DC, Bourge RC, Kirklin JK, Clemson BS, Porter CB, Rodeheffer RJ, Kenzora JL. Matching the heart donor and heart transplant recipient. Clues for successful expansion of the donor pool: a multivariable, multiinstitutional report. The transplant cardiologists research Database Group. J Heart Lung Transplant 1994;13:353-365.[Medline]
6. Bourge RC, Naftel DC, Costanzo-Nordin MR, Kirklin JK, Young JB, Kubo SH, Olivari MT, Kasper EK. Pretransplantation risk factors for death after heart transplantation: a multi-institutional study. The transplant cardiologists research Database Group. J Heart Lung Transplant 1993;12:549-562.[Medline]
7. Fernandez J, Aranda J, Mabbot S, Weston M, Cintron G. Overseas procurement of donor hearts: ischemic time effect on postoperative outcomes. Transplant Proc 2001;33:3803-3804.[CrossRef][Medline]
8. Briganti EM, Bergin PJ, Rosenfelt FL, Esmore DS, Rabinov M. Successful long-term outcome with prolonged ischemic time in cardiac allografts. J Heart Lung Transplant 1995;14:845-940.
9. Jeevanandam V, Barr ML, Auteri JS, Sanchez JA, Fong J, Schenkel RN, Marboe CC, Michler RE, Smith CR, Rose EA. University of Wisconsin solution versus crystalloid cardioplegia for human donor heart preservation. J Thorac Cardiovasc Surg 1992;103:194-199.[Abstract]
10. Stringham JC, Love RB, Welter D, Canver CC, Menter Jr RM. Does University of Wisconsin solution harm the transplanted heart?. J Heart Lung Transplant 1999;18(6):587-596.[Medline]
11. Kaye MP. The registry of the international society for heart and lung transplantation: tenth official report-1993. J Heart Lung Transplant 1993;12:541-548.[Medline]
12. Ardehali A, Hughes K, Sadeghi A. Inhaled nitric oxide for pulmonary hypertension after heart transplantation. Transplantation 2001;72(4):638-641.[CrossRef][Medline]
13. Kobashigawa JA, Katznelson S, Laks H. Effect of pravastatin on outcomes after cardiac transplantation. N Engl J Med 1995;333:621.[Abstract/Free Full Text]
14. Morgan J, John R, Weinberg A, Kherani A, Colletti N, Vigilance D, Cheema FH, Bisleri G, Cosola T, Mancini DM, Oz MC, Edwards NM. Prolonged donor ischemia time does not adversely affect long-term survival in adult patients undergoing cardiac transplantation. J Thorac Cardiovasc Surg 2003;1126:1624-1633.[CrossRef]
15. Kawauchi M, Gundry SR, de Begona JA, Fullerton DA, Razzouk AJ, Boucek M, Kanakriyeh M, Bailey LL. Prolonged preservation of human pediatric hearts for transplantation: correlation of ischemic time and subsequent function. J Heart Lung Transplant 1993;12(1 Pt 1):55-58.[Medline]
16. Kawauchi M, Gundry SR, Beierle F, Alonso de Begona J, Bailey LL. Myosin light chain efflux after heart transplantation in infants and children and its correlation with ischemic preservation time. J Thorac Cardiovasc Surg 1993;106(3):458-462.[Abstract]
17. Scheule A, Zimmerman G, Johnston J, Razzouk A, Gundry S, Bailey L. Duration of graft cold ischemia does not affect outcomes in pediatric heart transplant recipients. Circulation 2002;106(Suppl. I):I-163-I-167.[Medline]
18. Pflugfelder PW, Singh NR, Mckenzie FN, Menkis AH, Novic RJ, Kostuk WJ. Extending cardiac allograft ischemic time and donor age: effect on survival and long-term cardiac function. J Heart Lung Transplant 1991;10(3):394-400.[Medline]
19. Mullen JC, Bentley MJ, Modry DL, Koshal A. Extended donor ischemic times and recipient outcome after orthotopic cardiac transplantation. Can J Cardiol 2001;17(4):421-426.[Medline]
20. Weiss M, von Scheidt W. Cardiac allograft vasculopathy: a review. Circulation 1997;96:2069-2077.[Abstract/Free Full Text]
21. Knight RJ, Dikman S, Liu H, Martinelli GP. Cold ischemic injury accelerates the progression to chronic rejection in a rat cardiac allograft model. Transplantation 1997;64(8):1102-1107.[CrossRef][Medline]

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This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Personal Folders Download to citation manager Author home page(s): Fotios A. Mitropoulos Jonah Odim Daniel Marelli Abbas Ardehali Hillel Laks Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Mitropoulos, F. A. Articles by Laks, H. Search for Related Content PubMed PubMed Citation Articles by Mitropoulos, F. A. Articles by Laks, H. Related Collections Transplantation - heart