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Ann Thorac Surg 2002;74:1558-1567
© 2002 The Society of Thoracic Surgeons
a Heart Transplant Program, University of California, Los Angeles, Los Angeles, California, USA
* Address reprint requests to Dr Marelli, UCLA School of Medicine, 10833 Le Conte Ave, 62-266 CHS, Box 951741, Los Angeles, CA 90095-1741, USA.
e-mail: dmarelli{at}mednet.ucla.edu
Presented at the Thirty-eighth Annual Meeting of The Society of Thoracic Surgeons, Fort Lauderdale, FL, Jan 28–30, 2002.
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Abstract |
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METHODS: Adult recipients were divided into quartiles. The last 540 transplants were combined. Three eras were created from these, 1984 to 1991, 1991 to 1995, and 1995 to 2001, with three age groups: 0 to 18 years, 19 to 61 years, and 62 to 74 years. All patients have at least 1 year of follow-up time. End points were survival, rejection, and graft coronary artery disease.
RESULTS: There were 1,012 patients. Donor age, graft ischemic time, and the proportion of elderly recipients and nonstandard donor hearts have increased in the current era. Actuarial 60-month survivals of recipients after 1995 were 80.7% (0 to 18 years); 75.3% (19 to 61 years); and 76.2% (>62 years). The current era children and younger adult groups demonstrated improved results when compared with previous eras (p = 0.003 and p = 0.05). Rejection episodes equal to or greater than ISHLT grade 3A per person per year improved to 0.15 in the current era (p < 0.001). During the three eras, older recipients (>62 years) demonstrated fewer episodes of rejection when compared with other adults (0.13 versus 0.58, p = 0.03). Deaths attributed to graft coronary artery disease decreased from 11% to 5% from era 2 to era 3. Regression analysis revealed a mild effect of donor age on survival and graft coronary artery disease (hazard ratio = 1.02, p = 0.001; hazard ratio = 1.039, p < 0.001, respectively). Recipient predictors of graft coronary artery disease were diagnosis of ischemic cardiomyopathy (hazard ratio = 1.6, p = 0.014) and congenital heart disease (hazard ratio = 3.41, p = 0.02).
CONCLUSIONS: Improved survival in the current era may be attributed to better organ preservation, improved immunosuppression and control of infection, and less life-threatening graft coronary artery disease.
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Introduction |
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In the mid to late 1990s, the spotlight was shifted from surgical technique and organ preservation to management of congestive heart failure in outpatient settings and refinement in immunosuppression. More recently, the surgical arena has been the focus of intense research to develop alternatives to heart transplantation [2, 3]. In response to high demand for heart transplantation came the creation of specialized heart failure units with inpatient and outpatient branches, implantable defibrillators, and assist devices to bridge patients with cardiogenic shock to heart transplantation [4]. These advances in tertiary care have led to the stabilization of the mortality rate on the waiting list. Consequently, there has been a trend toward more patients (>60%) being listed status I, supported by inotropic agents or assist devices [5]. Although patients older than 65 years constituted approximately 5% of the total number of transplants in 1994, they currently make up approximately 10% of patients. In addition to concern regarding surgical risk, there has been some concern about diversion of organs away from younger age groups. This led the United Network for Organ Sharing to prioritize hearts from donors younger than 18 years old to similarly aged recipients since 1999.
This review outlines the University of California, Los Angeles experience with 1,083 consecutive transplants in 1,012 patients spanning 17 years. The purpose of this paper is to document trends and results from a large-volume single institution database.
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Patients and methods |
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Definition of terms
Nonstandard donor
Marginal donors were defined as any donor not meeting standard criteria (Table 1)
[7]. In general, such donors were offered to status I patients in whom the potential high risk (short or long term) of the donor was believed to be justified. For the purpose of this presentation, standard donors are defined as age younger than 45 to 55 years, normal cardiac function and anatomy, and negative viral serology.
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Marginal hearts were first offered to regularly listed patients. If they remained unused, they were offered to alternative recipients. For example, from 1992 to 1999, our institution accepted 182 nonstandard donor hearts. Of these, 120 went to status I regular patients and 62 were allocated to alternatives. The age for listing on the alternative list was set at 65 years in 1992. In 1998, when we observed that transplantation in selected elderly recipients was successful, the age limit was shifted to 70 years. Since 1999, selected candidates between ages 65 and 70 years have been simultaneously listed on the alternative and the regular lists to give them more access to donors while being status II. Those older than 70 years of age are alternatives only. Informed consent was obtained from all patients at the time of listing and organ acceptance. Alternative-only listed patients were not offered the possibility of status I listing so they would not compete with regularly listed patients.
Mechanical support
Mechanical support as a bridge to transplantation was defined as any ventricular assist device (VAD) used in a status I patient. External devices were extracorporeal membrane oxygenation circuits in small children and external VADs. External VADs comprised mostly the pulsatile BVS 5000 (Abiomed, Inc., Danvers, MA) and occasionally the centrifugal Biomedicus pump (Medtronic, Inc., Edenprairie, MN). Implantable VADs were the pneumatic and electrical Heartmate (ThermoCardiosystems, Inc., Woburn, MA) and the Thoratec pneumatic system (Thoratec, Inc., Berkeley, CA). Intraaortic balloon pumps were counted as part of inotropic support rather than VADs.
Listing and donor allocation
Evaluation for transplantation through our cardiomyopathy center includes cardiopulmonary exercise testing. In addition to usual Bethesda conference criteria, if maximum oxygen consumption is less than 14 mL · kg-1 · min-1, then patients are considered for transplantation [9]. If acceptable they are tested for panel reactive antibodies (PRAs). Patients with greater than 10% PRAs undergo prospective donor-specific cross-matching. If pretransplant PRAs are highly positive, then patients are treated with cyclophosphamide or plasmapheresis to reduce the PRA positivity on retesting. Considering that patients on assist devices usually received many recent blood transfusions, they underwent prospective donor-specific cross-matching if they were on support for longer than 1 week. We assumed that reactive antibodies would be present after 1 week but not before. Hearts were offered according to the United Network for Organ Sharing geographic allocation guidelines. Since 1999, hearts from donors younger than 19 years of age were prioritized to similarly aged recipients.
Organ preservation and surgical technique
Donor evaluation generally included heart rate, blood pressure, central venous pressure, need for inotropic support, and echocardiogram. Pulmonary artery catheters are rarely used. Thyroid hormone infusion is started several hours before retrieval. In 1993 our preservation solution was changed from Stanford solution to University of Wisconsin solution. Hearts were perfused at a constant pressure of 50 to 60 mm Hg more than 7 to 8 minutes, and were transported immersed in hypothermic University of Wisconsin solution. At the time of implantation, cold plasmalyte solution was infused into the left ventricle to aid in topical cooling and removal of air. Reperfusion was accomplished by means of the infusion of leukocyte-depleted, aspartate-glutamate–enriched, warm blood cardioplegia (Buckberg solution) for 3 minutes, followed by leukocyte-depleted blood for 5 minutes. Bicaval anastomosis was used for the right atrium since the early 1990s. As of the current era, postoperatively patients with pulmonary hypertension received inhaled nitric oxide if mean pulmonary artery pressure was greater than 25 mm Hg [10].
Immunosuppression and infection prophylaxis
Our program has not used induction therapy to complement three drug regimens. Methylprednisolone (7 mg/kg) was given at the time of reperfusion and on separation from cardiopulmonary bypass. Cyclosporine was administered with the aim of achieving an initial serum level of 250 to 350 ng/mL, and after 1 month, to 150 to 250 ng/mL. Azathioprine was administered at 2 mg · kg-1 · d-1. Since 1999, mycophenolate mofetil administered at 2 to 3 g/d has replaced azathioprine. Methylprednisolone was first given at a dose of 125 mg every 12 hours for three doses. Prednisone was then initiated at 1 mg · kg-1 · d-1 and tapered to 0.1 mg · kg-1 · d-1 by 6 months after transplant. For selected patients, with no or few rejections, prednisone was tapered off with an 80% success rate. For patients who developed severe or repeated episodes of rejection, cyclosporine was changed to tacrolimus and azathioprine to mycophenolate mofetil [11]. Pediatric patients with congenital heart disease and previous operation (with blood transfusions) have received tacrolimus and mycophenolate mofetil routinely since the mid-1990s. Pravastatin is currently used in all adult as well as pediatric recipients. Biopsies were performed at regular time intervals.
Postoperative antibiotic prophylaxis has been evolving. During the past 5 years, for patients with cytomegalovirus-positive serology in either the donor or recipient, ganciclovir was administered intravenously for 2 weeks at a dosage of 2.5 to 5.0 mg · kg-1 · d-1 adjusted for renal function. This was followed by oral ganciclovir for 3 months at a dose of 1 to 3 g/d. This was extended for an additional 3 months if rejection (and treatment) or chronic illness occurred. Double-strength trimethoprim-sulfamethoxazole (160 to 800 mg) tablets were administered twice daily 2 days per week for 12 months. Clotrimazole (10 mg) was used as a lozenge, three times a day for 3 months and extended in the case of and treatment for rejection. Beyond 6 months postoperatively, influenza vaccination was recommended for patients who exhibited a low risk of rejection.
Statistical analysis
Analysis was performed using Excel 97 (Microsoft Corp, Redmond, WA) and SPSS 10.0 (SPSS Inc, Chicago, IL). Averages were compared using the Student’s t test for independent samples. The 
2 test was used for proportions. Rejection rates were derived from raw data expressing the total number of rejection episodes (ISHLT 
3A) per patient per year of follow-up. Analysis of variance was used to compare means from all three eras and age groups together. Kaplan-Meier analysis with log rank test was used for survival and freedom from GCAD.
Multivariable analysis for survival was performed using a Cox logistic regression selection model (backward stepwise: enter p = 0.10, remove p = 0.15). Only eras 2 and 3 were included in these to minimize the effect of missing values. The percentage of cases dropped was 26. Indicator contrast was used for categorical variables. Continuous variables tested were donor and recipient age, graft ischemia time, and rejection episodes (ISHLT grade 3A) per person per year. Categorical variables were era, age group, occurrence of GCAD, pretransplant diagnosis of congenital heart disease, and ischemic cardiomyopathy. A similar analysis was conducted for GCAD. In this analysis, era 3 was dropped as a categorical variable because donors with preexisting coronary disease were used. Considering the possibility that graft ischemic time is not truly a patient-related preoperative variable, all regression analyses were repeated as described above with this variable removed.
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Results |
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Kaplan-Meier survival for age group 0 to 18 years improved in the most recent era but not in era 2, when it was observed to decrease (p = 0.003; Fig 6A). Survival for recipients aged 19 to 61 years old is 75.3% in the current era, which is significantly better (p = 0.05) than the previous eras (Fig 6B). For recipients aged 62 to 74 years there was a numerical improvement in survival between era 1 and era 3 (69% versus 76%, p = 0.3).
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Rejection and graft coronary artery disease
Mean (± standard deviation) number of rejection episodes equal to or greater than ISHLT grade 3A per person per year of follow-up were 0.92 (3.5), 0.75 (3.5), and 0.15 (0.84) for the three eras, respectively (p < 0.001). Adults older than 62 years of age had fewer episodes when compared with those who are 19 to 61 years (0.13 [0.64] versus 0.58 [2.9], p = 0.03) combining all three eras together. In era 3 alone, these values were 0.08 (1.0) and 0.21 (0.42), respectively (p = 0.05, equal variances not assumed, Student’s t test).
Five-year actuarial freedom from GCAD is currently 86%, 76%, and 78% for the three age groups, respectively, in era 3. This has not changed significantly compared with the previous era. Further analysis of the current era revealed that there were proportionately fewer deaths attributable to GCAD (of all deaths, 11% in era 2 versus 5% currently, p < 0.05). The multivariable selection model for GCAD revealed that independent predictors of GCAD were donor age (HR = 1.039; 95% CI, 1.025 to 1.053; p < 0.001), ischemic time (HR = 1.003; 95% CI, 1.0 to 1.006; p = 0.05). Categorical predictors were recipient diagnosis of ischemic cardiomyopathy (HR = 1.6; 95% CI, 1.09 to 2.40; p = 0.015), and congenital heart disease (HR = 3.2; 95% CI, 0.96 to 10.5; p = 0.05). Removing ischemic time from the model did not affect these results.
Use of an alternative recipient list
In 1997, when all patients older than 65 years of age were transplanted as alternatives, they constituted 10% of the total recipients, receiving 2% of the standard donor hearts used. In 1998, when patients between 65 and 70 years old were taken off the alternative list and placed on the regular list, there was a sharp rise in the distribution (17.8% of total transplants) of standard donors to recipients between 65 and 70 years old, who made up approximately 20% of total recipients that year. When patients 65 to 70 years of age were dually listed in 1999, they comprised 20% of total transplants but received only 10% of standard donors. A series of 62 consecutive alternatives (median age = 67 years) who underwent heart transplantation between 1992 and 1999 after a median wait of 107 days was reviewed. Median donor age was 45 years. Survival at 90 days was 82%. These patients were analyzed together with 401 contemporaneous recipients on the regular list. Recipient predictors of early mortality were prior cardiac operation and renal dysfunction. Only atraumatic intracranial bleed as a cause of donor death was identified as a significant donor risk factor. Late death rate per 1,000 person-months was 4.3 versus 3.6 (relative risk = 1.2; 95% CI, 0.62 to 2.36).
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Comment |
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TopAbstractIntroductionPatients and methodsResultsCommentAcknowledgmentsDiscussionReferences |
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In response to increasing recipient demand and longer wait times, our institution has expanded its program using nonstandard donor hearts. Expansion of the donor pool has been facilitated by improvement of our preservation protocol and the initiation of an alternative recipient waiting list. The multivariable analysis showed that longer graft ischemia time and older age influenced both survival (independent of GCAD) and GCAD. This effect was statistically significant but the hazard ratio was small. This suggests a low clinical significance and that with adequate precaution, long ischemia time and older age should not preclude donor heart retrieval.
The use of marginal donors has limits, particularly in the younger age groups who require hearts with greater expected longevity, and who are likely to better tolerate assist device operations. Such younger adults have dilated cardiomyopathy more often and have had previous operation less commonly. Therefore, these younger patients would appear to benefit most from standard donor hearts. In our experience, certain elderly recipients had a higher surgical risk when compared with younger adults. Our use of nonstandard donor hearts for status I patients and alternative elderly recipients has followed the model of matching donor and recipient risk [12].
Heart transplantation in well-selected elderly recipients yielded clinical results similar to those of younger patients. The elderly did not show an improvement in 5-year survival despite having fewer episodes of rejection. This is possibly explained by the higher prevalence of ischemic cardiomyopathy in this group (translating to a greater risk of GCAD), increased surgical risk, and other medical risk factors (such as renal failure). This also justified the use of nonstandard donors in this age group; both the donor heart and recipient variables had potentially increased long-term risk. The alternative list for elderly recipients may prove itself useful to prevent diversion of standard donors away from younger recipients. Such a two-list strategy for adult recipients permitted expansion of the donor pool with organs that were not being used. It is important to note that two thirds of the marginal donor hearts were allocated to younger patients who were status I. We also demonstrated that the age for alternative listing could be adjusted according to allocation trends and ongoing experience in 1999, when we increased the age from 65 to 70 years for alternative listing. A formal alternative list facilitates the use of nonstandard organs in status II patients because consent can be obtained from them ahead of time.
Interestingly, GCAD occurred with equal frequency but was less lethal in the most recent era. This is probably, in part, because of the use of pravastatin and improved immunosuppression. This lower cause of mortality may also be an underreporting owing to patients with sudden death and no autopsy. The high potassium content of University of Wisconsin solution did not appear to have a clinically negative impact on GCAD as freedom from GCAD in the current era was 76% to 86% depending on the age group.
Results for patients between 0 and 18 years of age were the lowest in era 2. This may be a result of liberalizing patient selection before the current era during which most of the refinement in preservation and immunosuppression became routine. The second era, which was before the introduction of tacrolimus, also had more congenital diagnosis patients. Such patients often present increased bronchial collateral blood flow and unique anatomy, increasing surgical difficulty. They also may have higher levels of preformed antibodies from previous operations and associated blood transfusions. This last possibility may explain the increased risk of GCAD observed on multivariable regression analysis in patients with congenital heart disease.
By combining short-term external mechanical cardiac assist with an aggressive donor retrieval strategy our institution has in the past minimized the use of long-term implantable devices [5]. Such devices usually require more complex procedures, which require cardiopulmonary bypass possibly resulting in longer hospital stays. Previously, mean waiting time for status I patients in our institution has been 22 days. For patients with blood type O or more than 2 m2 body surface area, waiting time has been 33 days (unpublished data). As a result of more-severely ill patients being listed, current waiting times for status I patients in our program now average approximately 40 days. This trend indicates that the use of an implantable device may be more common at our institution in the future.
On the horizon are smaller implantable left-sided VADs and the possibility of heart replacement therapy with a total artificial heart. Future studies will identify certain patients for destination therapy with left-sided VADs and those who may require total artificial heart replacement. It is anticipated that such therapies, as well as advances in medical treatment, will complement heart transplantation, which has achieved excellent and predictable results in the most recent era. The improved survival rates for the current era, as reported in this study, may change in the future as longer follow-ups are obtained for the patients in era 3. Half of these patients have less than a 5-year follow-up; this is a limitation of the data presented. Nevertheless, the present study documents results against which other newer surgical therapies for heart failure may be compared.
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Acknowledgments |
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Discussion |
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TopAbstractIntroductionPatients and methodsResultsCommentAcknowledgmentsDiscussionReferences |
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The results presented, that of a 5-year survival in the most recent period of 76% across the adult population, despite a high percentage of status I patients, using sicker donor hearts, longer ischemic times, and the increased use of marginal donors, have certainly raised the bar for those of us performing heart transplantation. You and your team are certainly to be congratulated.
I think you are to be congratulated as well for the pioneering efforts in the use of pravastatin, which has significantly decreased the incidence of posttransplant coronary artery disease and has changed the way all of us treat posttransplant patients. This has reduced but unfortunately not eliminated the problem.
I agree with your conclusion that improvements in preservation and immunosuppression have significantly contributed to the excellent results that you have presented, and in that regard I have a few questions.
The use of thyroid hormone is controversial in the literature; there are proponents and detractors. In your manuscript, you implied that thyroid hormone is used in all patients. I would like to ask you to expand on that and tell us whether in fact it is used in all donors and elucidate your rationale and philosophy for using thyroid hormone.
Second, related to your immunosuppression protocol, in the manuscript you report that you deliver steroids at two times, once before release of the cross-clamp prior to reperfusion and once you separate from bypass. Can you also elucidate that for us?
Third, the use of University of Wisconsin solution is credited with improvements as a result of the preservation effect you talked about. Have you any thoughts about the new extracellular low-potassium solutions that have come out in the last few years which may further decrease the incidence of transplant coronary disease while reducing the effects of high-potassium solutions on the endothelium?
And finally, you do not mention, either in your presentation or in the manuscript, the role that the large volume and the extensive experience that you and your colleagues have on these outstanding results. Although I think you are being modest, a lot of the credit for these outstanding results should go to you and your colleagues owing to your considerable medical and surgical expertise. In light of that, do you think there are minimum volume requirements for transplant programs in this day and age? Contrary to what we heard yesterday by Dr Khuri in his lecture, who said that there is not significant volume impact on survival in thoracic surgical procedures, I contend that there is in transplantation. Do you think that a system such as the one that exists currently in Great Britain, in which there are smaller numbers of high-volume centers, would improve the overall results of the US centers to more like those of your own center?
I enjoyed the paper very much, I appreciated the opportunity to review it, and I would like to thank the Society again for the opportunity to review this paper.
DR O. H. FRAZIER (Houston, TX): I was very pleased to see this presentation and very pleased with the early good results in this older patient population. We reported a series of cardiac transplants for patients over the age of 60 in 1988. We have not used the specific alternative listing because we often have "unused" donors for our older patients. Only 40% of the organ donors in the United States who have consented to donate their heart and kidneys will, ultimately, have the heart placed under the current organ allocation system. Therefore, potentially, 60% of cardiac donors could be matched to suitable recipients; however, for various reasons (usually logistic), they are not used. We believe that a suitable recipient should not be denied a donor even if the recipient is older, particularly if the donor would not be used under any circumstance.
DR MARELLI: I want to thank Drs Frazier and Conte for their comments. With regards to Dr Frazier’s question, we currently try to match as much as possible donor risk to recipient risk. The donor selection in our program is complex: sometimes we select donors without consultation with the referring cardiologist and sometimes there is intense consultation with referring cardiologists. There has been somewhat of a reluctance to use the very old donors, meaning older than 40 or 50 years old, in the status II young patients from our pediatric cardiology colleagues. The data shown do reflect this somewhat. We consider them in the case of status I listing versus an assist device.
To answer Dr Conte, we use thyroid hormone almost routinely whenever possible. We do not use the T3 infusion, as previously reported by other groups, but rather the more economical T4 infusion. This is done whenever possible and we ask it routinely on all donors. This has allowed us to decrease the dose of inotropic support in many donors in many instances and has in other times allowed us to repeat the echocardiogram and find an improved ejection fraction and allowed us to accept a donor that nobody else would use.
We use two doses of steroids during the operation, one during the reperfusion to prevent the initial possibility of rejection. This is in association with leukocyte depletion. This also decreases myocardial edema. After separation from cardiopulmonary bypass, because there is often bleeding, we also give an additional dose as a precaution. We have rarely seen acute graft rejection in the operating room, but it does occur approximately once a year or once every 2 years.
The question of high potassium is an interesting one. Experimental evidence shows that the high potassium in University of Wisconsin solution can damage endothelium. The question remains whether this damage is recoverable or not, as endothelium is a live organ. Our data analysis shown in this manuscript does not specifically address that question. We would have had to do a multivariate analysis using donors with coronary artery disease and era both in the same analysis, and we are in the process of doing that. We have other data in which we specifically examined the use of University of Wisconsin solution, and we were not able to prove that the high-potassium content leads to graft coronary artery disease. I do think that some of the newer solutions will be safer from that respect. The University of Wisconsin solution has been excellent for us. We have routinely achieved preservation times of 8 to 9 hours without any significant graft failure postoperatively.
The high volume of our institution comes with a price. There is a large infrastructure, and our residents and fellows can attest to that. It is very time-consuming and taxing to perform two heart transplants per week. There are many donor calls. This experience allows us to push the barrier and the cutting edge on a daily basis. Other smaller programs may be reluctant to push the barrier because of the fear of the report card. In that respect, a higher volume program is necessary to push these barriers constantly. The expertise is no doubt an asset, and if we were asked to set a minimum number, one could argue for 15 to 20.
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