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Ann Thorac Surg 2004;78:1345-1350
© 2004 The Society of Thoracic Surgeons

Original article: cardiovascular

Heterotopic Heart Transplantation: An Expanding Role in the Twenty-First Century?

Andrew E. Newcomb, MB, BSa, Donald S. Esmore, FRACS, FRCS-Edina,*, Franklin L. Rosenfeldt, FRACSa, Meroula Richardson, FRACPa, Silvana F. Marasco, FRACSa

a Heart and Lung Transplantation Service, Alfred Hospital, Melbourne, Australia

Accepted for publication March 25, 2004.

* Address reprint requests to Dr Esmore, Heart and Lung Transplant Service, Alfred Hospital, Commercial Rd, Melbourne, Victoria 3004, Australia
d.esmore{at}alfred.org.au


   Abstract
Top
 Abstract
Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
BACKGROUND: Heterotopic heart transplantation was first performed in humans in 1974, the main advantage being the continuing function of the patient's native heart, in the event of life-threatening acute rejection. The effect of cyclosporine on acute rejection saw the heterotopic transplantation technique wane. Our unit revisited heterotopic transplantation in response to a growing number of waiting list patients with high pulmonary artery pressures. We also anticipated an increased cardiac allograft utilization, and improvement of our waiting list times.

METHODS: We retrospectively analyzed 151 patients undergoing heart transplantation by our unit between August 1997 and September 2003. Twenty received allografts in the heterotopic position. This cohort was compared with the 131 contemporary orthotopic heart transplant recipients with respect to their outcomes.

RESULTS: The indication for transplantation was ischemic cardiomyopathy in 14 (70%) of the heterotopic cohort and 47 (36%) of the orthotopic cohort (p = 0.004), and dilated cardiomyopathy in 3 (15%) and 48 (37%) in the heterotopic and orthotopic groups, respectively (p = 0.06). Heterotopic recipients were significantly older than orthotopic recipients, and they had higher pulmonary artery pressures. The heterotopic donors were also older and the ischemic times were longer. A subgroup analysis was made among those patients who had high pulmonary artery pressures as these groups were better matched. Major morbidity in the heterotopic heart transplantation group consisted of reversible allograft dysfunction in 4 patients, renal dysfunction requiring hemofiltration in 3 patients, profound myopathy in 4 patients, and cerebrovascular events in 2 patients. There were two early deaths in the heterotopic transplant group and eight in the orthotopic group (p = 0.87). Kaplan-Meier survival analysis of survival was performed.

CONCLUSIONS: Heterotopic heart transplantation is a viable transplant option for selected high-risk heart transplant recipients in spite of somewhat poorer outcomes.


   Introduction
Top
 Abstract
 Introduction
Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
Barnard and Losman [1] performed the first heterotopic heart transplant in 1974 as a biologic left ventricular assist device. The main advantage was the assistance of the patient's native heart during episodes of severe acute rejection of the donor heart. The availability of cyclosporin A in 1984 with its favorable impact on acute rejection, as well as improving results with orthotopic heart transplantation and the technical challenges of the heterotopic technique, resulted in its decreased utility. Orthotopic transplantation became the configuration of choice and remains almost the exclusive cardiac transplantation option in the modern era.

In recent years a trend to falling cardiac transplant numbers has been observed worldwide [2]. Additionally, our transplantation waiting list was being inundated with a number of large patients (>80 kg) with high pulmonary artery pressures. With the previously documented under-utility of smaller cardiac allografts [3] and marginal allografts, our unit made the conscious decision to revisit the heterotopic heart transplant in an attempt to increase the utilization of available organs and to improve the waiting list times for these high-risk patients. Procurement from all over the Australian continent and often from New Zealand mandates a long ischemic time for a proportion of our donor hearts. Heterotopic heart transplant gives us the option to use these organs that would otherwise be marginal in an orthotopic configuration [2].


   Material and Methods
Top
 Abstract
 Introduction
 Material and Methods
Results
 Comment
 Acknowledgments
 References
 
Patients
Since the inception of the heart and lung transplant program at The Alfred Hospital, Australia, in March 1989, until the end of September 2003 this unit performed 420 heart transplants. The heterotopic heart transplant program was initiated in August 1997, and 20 male patients had undergone this procedure by the end of September 2003. During the same period 131 orthotopic heart transplants were performed and will be used to provide contemporary outcome comparisons.

The inclusion criteria for heterotopic heart transplantation were as follows:

The 20 patients who received the heterotopic transplants were chosen for that surgical option on the basis of a combination of factors that included transpulmonary gradient ≥ 13 mm Hg in 12 patients, donor to recipient weight ratio less than 0.8 in 10 patients, and donor ischemic time of more than 6 hours in 13 patients. Most had more than one indication. Marginal allografts were those that had required high inotropic support, had a history of cardiac arrest or arrhythmias, had wall motion abnormalities on echocardiography, or had evidence of ischemia on electrocardiography. Many of these had been rejected for use by other transplant units within Australia and New Zealand. Fourteen of the allografts used were considered marginal.

There are two techniques of heterotopic heart transplant available for use. The original technique used left heart assist only [1]. The other alternative uses biventricular assistance. The difference between operative techniques is that a conduit needs to be anastomosed between the donor and native main pulmonary arteries when performing a biventricular assist. All except one of our heterotopic transplant recipients had the cardiac allograft implanted in the left ventricular assist configuration (Fig 1). This patient received his transplant in the biventricular assist configuration because at the time of the transplant his native right heart exhibited refractory failure.



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  		Fig 1. Heterotopic heart transplant in the left ventricular assist configuration. (LA = left atrium; LV = left ventricle; PA = pulmonary artery; RA = right atrium; RV = right ventricle; SVC = superior vena cava.)

 
The heterotopic donor allografts were prepared in the standard fashion [1]. A cardioplegic cannula was secured in the donor's ascending aorta, and the end of the aorta was oversewn or stapled. The heterotopic allograft was then positioned in the right hemithorax during the implantation procedure. The native heart was cannulated and fibrillated on cardiopulmonary bypass. Intermittent antegrade blood cardioplegia was administered regularly, thus minimizing warm ischemic time and optimizing donor heart preservation. The surgical technique for the heterotopic implantation has been previously reported [4].

Patients in both groups received standard triple-therapy immunosuppression (cyclosporine, azathioprine, and corticosteroids). Cardiac biopsies in the heterotopic recipients were normally performed by means of the right internal jugular vein crossing the superior vena caval anastomosis to enter the donor right heart. When this route could not be negotiated, the femoral vein was used. Retrograde entry from the native right atrium into the donor pulmonary artery allowed access to the donor right heart for biopsy.

Patient demographics are outlined in Table 1. Fourteen of the cardiac allografts used for heterotopic transplantation had been rejected by other cardiac transplant programs for orthotopic transplantation, or had been considered unsuitable for orthotopic transplantation in our own unit on standard exclusion criteria.


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  		Table 1. Patient Demographics for Entire Cohorta

 
A subgroup analysis was performed using the criteria of raised transpulmonary gradient or pulmonary vascular resistance as outlined previously because this is the primary indication for using the heterotopic technique. These patient demographic details are provided in Table 2. It can be seen that these groups are similar.


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  		Table 2. High Pulmonary Artery Pressure Cohorta

 
Statistical Methods
The SAS program (Statistical Analysis System; SAS Institute Inc, Cary, NC) was used for statistical analysis. Outcome variables were assessed for normal distribution and log-transformed where appropriate. Differences between groups were assessed using Student's t tests. A p value of 0.05 was considered to be statistically significant. Results are presented as means with standard errors, or geometric means with 95% confidence intervals for data found to be well approximated by a log-normal distribution. The Kaplan-Meier method was used to create survival curves, with death being defined as the end point. These were then analyzed with the log-rank test. Our survival data were also compared with contemporary International Society for Heart and Lung Transplantation data using the Cutler-Ederer life-table analysis.


   Results
Top
 Abstract
 Introduction
 Material and Methods
 Results
Comment
 Acknowledgments
 References
 
Mean follow-up for the heterotopic group was 25 months (range, 0 to 67 months) and for the orthotopic cohort 34 months (range, 0 to 75). Hospitalization and outcome data are detailed in Table 3.


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  		Table 3. Hospitalization Dataa

 
Major Morbidity
Four of the heterotopic cardiac allografts did not function adequately immediately after implantation. These organs all had ischemic times of greater than 7 hours. The patients were managed postoperatively with high-dose inotropic support, insertion of an intraaortic balloon counterpulsation device, and synchronization of donor and recipient heart pacing. In these cases of primary allograft dysfunction, full cardiac function returned, with the inotropic agents being weaned and the balloon pumps subsequently removed at a maximum of 72 hours. In each case, cardiac allograft function had normalized on echocardiographic assessment before hospital discharge. No other forms of mechanical assistance were required for these patients, which is in contrast to the 10 patients in the orthotopic cohort who required mechanical circulatory support. These patients had longer ischemic times than the rest of the orthotopic cohort, and they were older. Fifty percent of these patients died despite the intervention.

Three patients required periods of hemofiltration in the early postoperative period for durations of 3, 10, and 14 days. Cyclosporine dose was reduced or discontinued in these patients and supplemented or replaced with sirolimus or basiliximab. Renal function normalized in all three of these patients before hospital discharge.

Four patients demonstrated a moderately severe peripheral myopathy in the intensive care unit, related to the combination of inotropic agents, muscle relaxants, steroids, and protracted ventilatory support. The myopathies improved during the period of hospitalization, responding to intensive physical therapy.

Two patients sustained cerebrovascular events early perioperatively. Both patients recovered completely, one after having a 3-day course of hyperbaric oxygen therapy. The most likely cause in both patients was air embolism from either the heterotopic or native hearts that had been difficult to remove air from in the setting of early spontaneous contraction. Intraoperative transesophageal echocardiography was used in all cases to facilitate removing air from the native heart; however, the heterotopic hearts, once in situ, are difficult to visualize on transesophageal echocardiography.

Early Mortality
There were two deaths in the heterotopic group within 30 days, both occurring on day 7. Our first recipient died after a routine cardiac biopsy, which was uneventful and performed by an experienced operator. After this procedure he became hypotensive and tachycardic. A transthoracic echocardiogram was performed and showed good allograft function with a right pleural collection. His sternotomy was reopened in the ward, and there was blood in the right pleural space. He was taken to the operating room and was placed on cardiopulmonary bypass, but no obvious source of bleeding was found. Function of the native and transplanted hearts was depressed globally. The heterotopic heart transplant was converted to the biventricular assist configuration. Successful weaning and decannulation followed, but the patient deteriorated again after protamine administration. He subsequently experienced uncontrollable ventricular arrhythmias and was unable to be resuscitated.

The other early death, again on day 7, was a 54-year-old man who was in a severely compromised state preoperatively with a combination of end-stage valvular and coronary heart disease, who succumbed in the intensive care unit with progressive multiorgan failure and sepsis.

In the orthotopic group there were eight deaths within 30 days. Two had evidence of rejection in the donor organ and multiorgan failure; another had an acute infarction in the donor organ postoperatively with associated multiorgan failure. Three had primary cardiac allograft failure with no identifiable cause. Of the other early orthotopic recipient deaths on days 3 and 6, the first was from multiple bone marrow pulmonary emboli after a period of preoperative external cardiac massage, and the other had support withdrawn after no cerebral perfusion was detected in the postoperative period.

Late Deaths
There were seven late deaths in the heterotopic group. One patient died at home on day 33 from a cerebral event. A sudden death occurred on day 142 in a patient with multiple system problems, who was discharged from hospital the previous day after an admission for surgical management of pressure ulcers. One patient deteriorated and died on day 222 from a pulmonary embolus. Another patient died after presentation to the emergency department on day 294 with sternal sepsis and associated septic shock. One patient was admitted to the intensive care unit with febrile neutropenia and a newly diagnosed lymphoid malignancy and died of respiratory failure on day 505. The final late death was a patient who was admitted to the hospital with community-acquired pneumonia, had cardiogenic shock, and died on day 679.

Kaplan-Meier survival curves are shown in Figure 2 comparing our contemporary heterotopic heart transplant and orthotopic heart transplant cohorts. The outcomes for these two groups are statistically different (p = 0.003) as measured by the log-rank test. This difference is diminished when comparing the subgroups of patients who had a high transpulmonary gradient (Fig 3). A comparison with the International Society for Heart and Lung Transplantation heterotopic heart transplant 4-year actuarial survival (Cutler-Ederer) of 48% (unpublished data, L Edwards, UNOS Registry) is similar to the 51% for our heterotopic heart transplant group, both being significantly inferior to the 76% 4-year survival of our orthotopic heart transplant cohort (p = 0.0026).



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  		Fig 2. Survival comparison for entire cohort (p = 0.003).

 


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  		Fig 3. Survival of high transpulmonary gradient subgroups (p = 0.54).

 
Of the 11 intermediate-term heterotopic heart transplant survivors, all are New York Heart Association functional class I. There has been little morbidity or mortality related to the presence of the native heart. More specifically, there have been no further neurologic events and no angina pectoris. There has been only one episode of recurrent ventricular tachycardia in the native heart (day 202), which responded to antiarrhythmic therapy with amiodarone.


   Comment
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
Acknowledgments
 References
 
The main benefits of using the heterotopic heart transplant are the ability to transplant patients with a high pulmonary vascular resistance and the ability to use organs that would otherwise be wasted. The predominant indication for heterotopic heart transplant is high pulmonary artery pressures in the recipient. This is because of the previously documented poor survival in these patients who undergo orthotopic transplantation [2, 5]. Nakatani and associates [5] showed good intermediate-term survival for their 8 heterotopic heart transplant recipients with raised pulmonary vascular resistance when compared with contemporary orthotopic transplant counterparts. They also reported a trend toward normalization of pulmonary artery pressures within 12 months postoperatively. Similar results have been realized by other groups [6, 7]. Others, however, have questioned the validity of performing heterotopic heart transplantation in patients with high pulmonary artery pressures.

Ridley and colleagues [8] suggest that better options are available for dealing with recipients with high pulmonary artery pressure, namely orthotopic heart transplantation with a large donor or a preconditioned cardiac allograft from a domino heart-lung transplant procedure. The other options available to these patients are the heart-lung transplant, or ventricular assist device as a bridge to orthotopic transplant [9]. The 5-year survival for our heterotopic cohort was 51%. This compares favorably to that reported for heart-lung transplants [2] with a cumulative 40% 5-year survival. We also believe in this era of organ shortages that it reflects poor organ utilization to be offering this option to these patients.

The analysis of ventricular assist devices in the setting of cardiac failure was performed by the REMATCH study group [10], who realized a 2-year survival of 23%, which was more than twice as good as optimal medical management, but less than half the survival conferred to those receiving a heterotopic heart transplant by our unit.

Many of the heterotopic transplant patients with a high transpulmonary gradient weighed more than 80 kg. Potential recipients of larger body weight have been shown to wait longer for a size-matched donor organ [11], whereas up to 32% of patients die while awaiting a donor organ [12]. During the last decade we think the heterotopic heart transplantation has found a new indication in addressing these issues. By facilitating the utilization of small and marginal donor cardiac allografts, heterotopic transplantation effectively increases the donor pool. In accepting these organs, larger higher-risk patients may be offered heart transplantation sooner. This decreases their waiting list time, and at the same time gives them a definitive transplant option that is the best available for their situation. In this study, we have shown that patients undergoing heterotopic heart transplantation have similar waiting list times to those patients undergoing orthotopic heart transplantation.

The heterotopic heart transplantation option has been particularly useful in allowing us to retrieve donor hearts from all over the Australian continent. With a population of just 20 million, and a multiorgan donation rate of 10 donors per million population per annum [13], the donor pool in Australia is less than 10% that of the United States. As such, donor offers are not restricted geographically to states or regions but are offered on a national rotation. Clearly, procurement of organs over such a large continent presents logistical problems. The most pertinent of these is the long ischemic times that are almost inevitable when traversing a country that is 3,800 km from north to south, and 4,000 km from east to west. Organ procurement from New Zealand enlarges our donor pool by a small percentage, but with the attendant problem of long travel and ischemic times. As can be seen in Table 1, the mean ischemic time of 362 minutes in our heterotopic heart transplant cohort is much longer than many other reported series [14–16].

Another significant advantage gained by use of the heterotopic technique is that of the added support given by the recipient organ in the setting of allograft dysfunction. Barnard and Losman [1] recognized this when they discussed the advantages of heterotopic heart transplantation because the patient's cardiac output is not solely dependent on that of the donor allograft. This benefit was confirmed in four of our patients, in whom there was depressed activity from the allograft for up to 72 hours after transplantation.

Our results show a lower survival associated with heterotopic heart transplantation compared with orthotopic heart transplantation for the same period. This survival benefit was lost when the subgroup analysis was performed for those patients with high pulmonary artery pressures. Our heterotopic survival results are similar to those reported by the international registry and compare favorably with those reported by others [5–8, 15, 17].

One of the supposed disadvantages of using the heterotopic configuration is the added complexity and prolonged duration of the operation [5], and some centers consider previous surgery a contraindication for this procedure [14]. Fourteen of our 20 heterotopic heart transplant recipients had undergone previous surgery for ischemic heart disease. The heterotopic option was believed to offer an advantage over the orthotopic configuration in the redo setting because only the right side of the heart and aorta needed to be dissected of adhesions to allow for cannulation for cardiopulmonary bypass and completion of the anastomoses required for the left ventricular assist configuration as favored by our institution.

It has been suggested by some authors that it is harder to perform endomyocardial biopsies in the heterotopic patients [17, 18]. This is probably true; however, if we were unable to biopsy the right ventricle through the internal jugular vein, the donor heart was accessed retrograde through the femoral vein using a modification of the technique described by Boffa and associates [19]. Using a combination of these approaches, our cardiologists were able to retrieve adequate samples from each of our heterotopic heart transplant patients.

Other authors have raised concerns regarding the ongoing risk of complications from the native heart, namely recurrence of angina, thromboembolic events, ventricular arrhythmias, and progression of native valvular disease [20]. We have observed only one episode of ventricular tachycardia in our heterotopic heart transplantation cohort and have experienced no other complications related to the retention of the native heart during the period of follow-up.

Heterotopic heart transplantation is a viable alternative for selected high-risk patients who may be denied heart transplantation. It has also allowed us to use marginal donor hearts that may otherwise have been wasted. There are some pitfalls with this technique, of which surgeons need to be cognizant. However, we believe this is an invaluable option that should be used when appropriate by all high-volume transplant centers.


   Acknowledgments
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
References
 
We acknowledge the statistical assistance of Michael Bailey in the Department of Epidemiology and Preventative Medicine, Monash University, Melbourne; the assistance of Anne Griffiths, Julie Johns, and Sharon Daly for data collection for the manuscript; and Leah B. Edwards, Associate Director of Data Analysis for the International Society for Heart and Lung Transplantation, for the data used in our comparative analyses.


   References
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 

  1. Barnard CN, Losman JG. Left ventricular bypass. SA Med J. 1975;49:303–312
  2. Hosenpud JD, Bennett LE, Keck BM, et al. The Registry of the International Society for Heart and Lung Transplantation: Eighteenth Official Report—2001. J Heart Lung Transplant. 2001;20:805–815[Medline]
  3. Jeevanandam V, Furukawa S, Prendergast TW, Todd BA, Eisen HJ, McClurken JB. Standard criteria for an acceptable donor heart are restricting heart transplantation. Ann Thorac Surg. 1996;62:1268–1275[Abstract/Free Full Text]
  4. Novitzky D, Cooper DK, Barnard CN. The surgical technique of heterotopic heart transplantation. Ann Thorac Surg. 1983;36:476–482[Abstract]
  5. Nakatani T, Frazier OH, Lammermeier DE, Macris MP, Radovancevic B. Heterotopic heart transplantation: a reliable option for a select group of high-risk patients. J Heart Transplant. 1989;8:40–47[Medline]
  6. Livi U, Faggian G, Chiominto B, Mazzucco A, Bortolotti U, Gallucci V. Heterotopic heart transplantation—a means to increase donor availability. Eur J Cardiothorac Surg. 1990;4:202–206[Abstract]
  7. Reichenspurner H, Hildebrandt A, Boehm D, et al. Heterotopic heart transplantation in 1988: recent selective indications and outcome. J Heart Transplant. 1989;8:381–386[Medline]
  8. Ridley PD, Khaghani A, Musumeci F, et al. Heterotopic heart transplantation and recipient heart operation in ischemic heart disease. Ann Thorac Surg. 1992;54:333–337[Abstract]
  9. Adamson RM, Dembitsky WP, Jaski BE, et al. Left ventricular assist device support of medically unresponsive pulmonary hypertension and aortic insufficiency. ASAIO J. 1997;43:365–369[Medline]
  10. Rose EA, Gelijns AC, Moskowitz AJ, et al. Long- term use of a left ventricular assist device for end stage heart failure. N Engl J Med. 2001;345:1435–1443[Abstract/Free Full Text]
  11. Sharples LD, Roberts M, Parameshwar J, et al. Heart transplantation in the United Kingdom: who waits longest and why. J Heart Lung Transplant. 1995;14:236–243[Medline]
  12. Deng MC, DeMeester MJ, Smits JM, et al. Effect of receiving a heart transplant: analysis of a national cohort entered onto a waiting list, stratified by heart failure severity. BMJ. 2000;321:540–545[Abstract/Free Full Text]
  13. Herbert K, Russ GR, eds. ANZOD Registry Report 2002. Australia and New Zealand Organ Donation Registry, Adelaide, Australia
  14. Sekela ME, Smart FW, Noon GP, Young JB. Attenuation of waiting time mortality with heterotopic heart transplantation. Ann Thorac Surg. 1992;54:547–551[Abstract]
  15. Bleasdale RA, Banner NR, Anyanwu AC, et al. Determinants of outcome after heterotopic heart transplantation. J Heart Lung Transplant. 2002;21:867–873[Medline]
  16. Anyanwu AC, Rogers CA, Murday AJ. Variations in cardiac transplantation: comparisons between the United Kingdom and the United States. J Heart Lung Transplant. 1999;18:297–303[Medline]
  17. Desreunnes M, Muneretto C, Gandjbakhch I, et al. Heterotopic heart transplantation: current status in 1988. J Heart Transplant. 1989;8:479–485[Medline]
  18. Arzouman DA, Arabia FA, Sethi GK, Copeland JG. Endomyocardial biopsy in the heterotopic heart transplant patient. Ann Thorac Surg. 1998;65:857–858[Abstract/Free Full Text]
  19. Boffa GM, Grassi G, Cocco P, et al. Endomyocardial biopsy in heterotopic heart transplant recipients via the femoral vein. Cathet Cardiovasc Diagn. 1993;28:18–21[Medline]
  20. Tagasuri O, Kormos RL, Kawai A, et al. Native heart complications after heterotopic heart transplantation: insight into the potential risk of left ventricular assist device. J Heart Lung Transplant. 1999;18:1111–1119[Medline]

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