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Ann Thorac Surg 2001;71:1839-1844
© 2001 The Society of Thoracic Surgeons

Original article: cardiovascular

Risk analysis in patients bridged to transplantation

Lawrence R. McBride, MDa, Keith S. Naunheim, MDa, Andrew C. Fiore, MDa, Robert G. Johnson, MDa, Debbie A. Moroney, RNa, Jenny A. Brannan, RN, MSNa, Marc T. Swartza

a Department of Surgery, Cardiothoracic Division, Saint Louis University School of Medicine, St. Louis, Missouri, USA

Address reprint requests to Mr Swartz, Department of Surgery, Division of Cardiothoracic Surgery, 3635 Vista Ave at Grand Blvd, St. Louis, MO 63110
e-mail: swartzmt{at}slu.edu

Presented at the Forty-seventh Annual Meeting of the Southern Thoracic Surgical Association, Marco Island, FL, Nov 9–11, 2000.


   Abstract
Top
 Abstract
Introduction
 Material and methods
 Results
 Comment
 Discussion
 References
 
Background. Efforts to predict mortality in bridge to cardiac transplant patients have concentrated on pre-ventricular assist device (VAD) status. To more fully identify factors influencing survival to transplant, we reviewed the preoperative and postoperative VAD courses of 105 bridge to transplant patients.

Methods. Sixty-four parameters (34 pre-VAD, 30 post-VAD), including hemodynamics, complications, and evaluations of major organ function were examined and analyzed.

Results. Thirty-three patients (31%) died on VADs and 72 were transplanted. There were two posttransplant operative deaths (3%). By univariate analysis 23 of 64 factors were significant. These 23 factors were entered into a stepwise logistic regression analysis to identify predictors of survival to transplant. Four factors, including pre-VAD intubation (p < 0.005), cardiopulmonary bypass (CPB) time during VAD insertion (p < 0.0001), mean pulmonary artery pressure (first postoperative day after VAD) (p < 0.0002), and highest post-VAD creatinine (p < 0.01) were independent predictors of transplantation.

Conclusions. Other than the need for intubation, pre-VAD variables were of little value in predicting survival to transplant. Problems during VAD insertion (long CPB time) and post-VAD renal insufficiency were independent predictors. Severe complications that developed during the interval of VAD support, including cerebrovascular accident, bleeding and infection, were surprisingly not predictors for transplantation.


   Introduction
Top
 Abstract
 Introduction
Material and methods
 Results
 Comment
 Discussion
 References
 
Over the last 20 years, there have been significant clinical and engineering advances made in the field of mechanical circulatory support. These have been particularly beneficial in the area of ventricular assist devices (VADs) used as bridges to cardiac transplantation. Despite these advances, there is still considerable morbidity encountered both in the immediate postoperative period and during the pretransplant interval of support. Historically, patient selection has been based on pre-VAD clinical criteria, especially hemodynamics. While some patients will die during or shortly after VAD placement, a significant percentage dies during the lengthy interval of support preceding transplantation. Patient selection criteria should consider an individual’s ability not only to survive the VAD implant, but also a period of rehabilitation before transplant.


   Material and methods
Top
 Abstract
 Introduction
 Material and methods
Results
 Comment
 Discussion
 References
 
Prospectively collected parameters from our Mechanical Circulatory Support database were reviewed focusing on patients supported as a bridge to cardiac transplantation. Those patients initially thought to be transplant candidates whose hearts recovered were weaned from support and excluded from this study (n = 3). Data were collected by cardiothoracic clinical nurses assigned exclusively to the mechanical circulatory support service. From 1982 through 1996, Investigational Device Exemption study protocols were reviewed and approved by the Food and Drug Administration (FDA) and the Institutional Review Board of Saint Louis University. All patients and/or families signed informed consents for investigation during this interval. Since 1997, the devices have been used on a noninvestigational basis in compliance with the products’ labeling.

For the most part, all patients met the standard inclusion and exclusion guidelines adopted by the National Heart, Lung and Blood Institute (NHLBI) clinical investigation group as well as the FDA [1–2]. These criteria were used in all investigational studies involving mechanical circulatory support devices. In general, patients were considered candidates for assist devices when their (1) cardiac index was less than 1.8 l/m2/min, (2) systemic vascular resistance was more than 2,100 dynes/s/cm-5, (3) systolic blood pressure was less than 90 mm Hg; (4) right or left atria pressure was more than 20 mm Hg; and (5) urine output was < 0.5 mL/kg, despite optimal preload, maximal inotropic drug support and, in the majority of cases, an intraaortic balloon pump (IABP) [3].

Once the Thoratec (Thoratec Laboratories Corporation, Pleasanton, CA) and Novacor (World Heart, Inc, Oakland, CA) VADs had received premarketing approval from the FDA, these criteria were somewhat relaxed; however, all patients manifested cardiogenic shock, the inability to maintain major organ function and/or refractory ventricular arrhythmias. Postoperative management techniques and definitions of postoperative complications have been previously described and published.[4]

Descriptions of the Thoratec, Novacor and Symbion Jarvik-7 Total Artificial Heart (TAH) (formerly Symbion, Inc, Salt Lake City, UT), as well as techniques for insertion, have been previously published.[5–7] All VADs were inserted in beating hearts during normothermic cardiopulmonary bypass. Several early Thoratec patients who received a left VAD (LVAD) underwent inflow cannulation through the left atrial appendage, the dome of the left atrium, or anterior to the entrance to the right pulmonary veins. Since 1988, all Thoratec LVAD and Novacor patients have been cannulated via the left ventricular apex. Most patients having right VADs (RVADs) implanted, had inflow cannulas placed in the right atrium (two patients had right ventricular cannulation). Ventricular assist device outflow cannulas were sutured to the ascending aorta (LVAD) and/or main pulmonary artery (RVAD). Total artificial hearts were implanted utilizing full cardiopulmonary bypass (CPB) with moderate hypothermia.

The data were analyzed using StatView for Windows (SAS Institute, Inc, Cary, NC, Version 5.01). Statistical analysis consisted of a Student’s t test for continuous variables and a {chi}2 contingency table, or Fisher’s exact test (when appropriate), for discrete variables. Means are expressed with ±1 standard deviation (SD). A p value less than 0.05 was considered significant while a p value less than 0.10 and greater than 0.05 was considered marginally significant. Both significant and marginally significant variables were then entered into a stepwise logistic regression analysis to identify significant independent predictors of pretransplant mortality. Actuarial survival was calculated using the method of Kaplan and Meier. The duration of VAD support (VAD implant to transplant or death) was used as the time component of the logistic regression analysis and the actuarial survival.


   Results
Top
 Abstract
 Introduction
 Material and methods
 Results
Comment
 Discussion
 References
 
Between April 1982 and December 1999, 105 patients had mechanical circulatory support devices inserted at Saint Louis University for the purpose of bridging to cardiac transplantation. There were 81 males and 24 females ranging in age from nine to 66 years with a mean age of 43.8 ± 14.2 years. The etiology of cardiomyopathy was ischemic in 51 patients, idiopathic in 31 patients, valvular in seven patients, postpartal in five patients, viral in four patients, posttransplant rejection in four patients (1 acute, 3 chronic) and congenital heart disease in three patients. Seventy-four patients had Thoratec VADs inserted (46 LVAD, 28 BVAD). Twenty-nine patients received Novacor LVADs; twenty-seven of these had LVADs only while two patients required Novacor LVADs plus centrifugal RVADs. Two additional patients received biventricular support with Symbion Jarvik-7–70 TAHs. The Thoratec was implanted primarily in smaller patients as well as those who were considered at risk for biventricular failure. The Novacor was used in larger patients and those believed to have isolated left ventricular failure. The Thoratec and Novacor are currently our preferred devices. The durations of support ranged from three hours to 440 days with a median of 32 days. Twenty-three patients were supported less than seven days, 26 patients were supported eight to 31 days, 36 patients were supported one to three months, and 20 patients received more than three months of support.

Seventy-two patients had orthotopic cardiac transplants. Of these, there were two posttransplant hospital deaths: one in the operating room at the time of transplant from bleeding and graft failure (prolonged ischemic time), and the second (retransplant for acute rejection) died four months posttransplant from the combination of rejection and infection. Actuarial survival curves of transplanted and nontransplanted patients are shown in Figure 1.



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  		Fig 1. Actuarial survival curves for transplanted (TX) and not transplanted (not TX) patients.

 
The causes of death at four time intervals of the 33 patients who died on devices before cardiac transplantation are shown in Table 1. Sixteen of the 33 deaths occurred within seven days of device implantation. Despite successful VAD placement, six died of progressive multiple organ failure (MOF), two of sepsis (ischemic bowel), three from pulmonary emboli, and two who were thought to be neurologically intact preoperatively, never woke up after VAD implant. Three additional patients with LVADs died of right ventricular failure. Two of these three had very small right atria (one 64-year-old female, one 9-year-old male) which made RA cannulation difficult. The third patient suffered an acute myocardial infarction with ventricular fibrillation. Despite successful resuscitation, he developed right heart failure and died before an RVAD could be placed.


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  		Table 1. Cause of Death Nontransplanted Patients (n = 33)

 
Of the 17 deaths that occurred between eight and 263 days after device implant, six died within 31 days of implant from MOF despite being maximally supported with VADs, dialysis, ventilators, and all available measures. One female supported with an LVAD and extracorporeal membrane oxygenation (ECMO) died eight days after implant of acute respiratory distress syndrome and hypoxia. A 12-year-old who arrested pre-VAD and suffered neurologic injury, died after being supported for three weeks. Seven of the 17 deaths that occurred after one week were in patients who had severe major organ damage pre-VAD, which proved to be irreversible, and may or may not have been aggravated by the VAD implant. Two late deaths between one and three months were the result of intracranial bleeding in bacteremic patients, both of whom were receiving multiple antibiotics as well as warfarin and aspirin.

The 34 pre-VAD and 30 post-VAD, clinical parameters evaluated for this study are shown in the Appendix. There were no statistical differences between the preoperative hemodynamics of the 72 patients who survived to transplant and the 33 patients who died while being supported with devices. A comparison of the complications which developed after VAD insertion is included in Table 2. There were no differences between the two groups with regard to the incidence of the complications. The 23 parameters which were significant or marginally significant by univariate analysis are shown in Table 3.


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  		Table 2. Post-VAD Complications

 

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  		Table 3. Univariate Analysis

 
Results of the stepwise logistic regression analysis are shown in Table 4. Four parameters, pre-VAD intubation, CPB time (VAD insertion), mean pulmonary artery pressure on the first postoperative day from VAD insertion and the highest post-VAD creatinine were identified as independent predictors of survival to transplant.


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  		Table 4. Stepwise Logistic Regression Analysis

 

   Comment
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
Discussion
 References
 
Bridging to cardiac transplantation is a staged procedure in which decisions concerning patient selection must be made at two distinctly different times: the first, before VAD insertion and the second in the interval following VAD placement at the point were the patient is reaffirmed to be a transplant candidate. The criteria used to reach these two decisions are distinct and vary between centers. Initially, patient selection criteria for VADs were based on studies predicting mortality in postcardiotomy shock patients needing IABs. These hemodynamic criteria were adopted by the NHLBI and the FDA as part of the patient inclusion criteria for investigational VAD studies. During these studies in the United States, there were modifications in patient selection based on experience. After the devices received FDA clearance and were more generally available, patient selection was again modified to include groups that had been previously avoided or excluded [8, 9]. As a result of these experiences, patient selection for bridging have expanded as have the criteria for cardiac transplantation [10]. Forty-three of our last 45 referrals were accepted and had VADs inserted.

For patients who manifest acute, severe deterioration refractory to conventional therapy, the decision to place a VAD is relatively straightforward if there is reasonable expectation that myocardial recovery could occur and if no exclusions to cardiac transplantation exist. Unfortunately, it remains difficult to positively determine early in the course, whether reversible or irreversible major organ damage has occurred. Over time, significant organ damage will manifest itself, thus, accounting for the considerable percentage of patients that die from MOF during the first few weeks of support. For these patients who rapidly deteriorate, selection has remained stable over the past 15 years. The more difficult group are patients who deteriorate and improve repeatedly, those that show intermittent or slow continuous deterioration in major organ function, patients with refractory ventricular arrhythmias of increasing frequency and severity, and patients with moderate to severe pulmonary hypertension where pulmonary vascular responsiveness cannot be accurately evaluated.

Despite variations between centers in patient selection, technology and clinical management, the survival to transplant for bridging is reported to be between 62% to 76% with overall survival rates of 40% to 67% [11–17]. Over the past decade, our survival to transplant has averaged 70% with an overall survival of 67%. We feel these relatively constant rates are the result of gradual improvements in clinical management, counterbalanced by expanding selection criteria which leads to the inclusion of "sicker" patients.

Several recent studies have examined risk factors to predict survival to transplantation and/or overall survival in patients receiving VADs. McCarthy and colleagues reviewed 100 patients receiving HeartMate (ThermocardioSystems, Inc, Woburn, MA) LVADs which identified several significant risk factors for death including preoperative ventilator ECMO, elevated blood urea nitrogen (BUN), creatinine or bilirubin and low pulmonary artery pressures [14]. Korfer and associates reviewed their experience in 114 patients who received Thoratec VADs [12]. This study identified age more than 60 years as the only independent risk factor affecting survival. Quaini and colleagues presented multicenter data in 250 patients bridged to transplant using four different types of devices [13]. Independent risk factors for overall mortality included age, indication for posttransplant graft failure, renal failure, infection, bleeding, RVADs or TAH support, and neurologic impairment. A multicenter report describing results with the Thoratec VAD by Farrar and colleagues summarized results in 186 patients and identified BUN to be significant using multivariate analysis [11]. Kawaguchi and associates identified age, total bilirubin, and body surface area as predictors of survival in patients being bridged with TAHs [18].

Surprisingly, while identified in prior reports, age, pre-VAD hemodynamics, creatinine, BUN, and ECMO were not found to be significant in our report. Ten patients in this study were older than 60 years of age, of which seven were successfully transplanted. Other risk factors were also well represented with 14 patients being supported by ECMO, 24 patients with BUNs more than 50 mg/dl, and 14 patients with a serum creatinine more than 2.5 mg/dl pre-VAD. The need for intubation and mechanical ventilation was the only pre-VAD predictor identified in our study. Clinically, this is a reflection of deteriorating hemodynamic status which often leads to irreversible major organ damage.

We also found CPB time during device implant to be significant and an independent predictor of survival to transplant. This does not appear to be accounted for solely by the need for biventricular support in certain patients. Though BVAD placement was a univariate predictor, it did not prove to be an independent predictor. Prolonged CPB time appears to be not only a reflection of the need for biventricular support, but also of clinical instability and/or technical problems (bleeding, patent foramen ovale) encountered during device implantation.

Post-VAD independent predictors included mean pulmonary artery pressure (first postop day from VAD) as well as the highest post-VAD creatinine. Elevated pulmonary vascular resistance and renal insufficiency are two known risk factors for patients being supported with VADs as well as those being considered for transplant. Of interest, post-VAD implant complications including bleeding, infection (both device and patient related), cerebrovascular accident, and device-related technical problems were not significant.

Our results suggest that the longer a patient is supported, the greater the chance of being transplanted. This seems logical and almost obvious, considering that nearly half (48%) of the patients who never reached transplant died within seven days of VAD implant. In addition, locating a donor heart is a random process requiring consistently increasing periods of time. Many of these patients never had the opportunity to be transplanted quickly (if they were candidates at the time) due to the fact that for about the last 15 years, donor hearts have rarely been offered within seven days of device implant. In this study, the patients transplanted in less than seven days were done early in our experience. In general, it has been our policy to inactivate from the transplant list bridge patients for two-four weeks post-VAD implant in order to reverse the effects of shock and provide some rehabilitation before transplant.

Some may contend that the longer the patients are maintained on devices, the more likely they are to develop complications. This may be true, however, as experience grows the development of device-related complications is being delayed and in some cases eliminated [14,19]. Twenty patients were supported longer than 90 days in this study with 18 of 20 transplanted. This 90% transplant rate came at a considerable cost. Sixteen patients developed major complications which included eight thromboembolic events (4 TIA, 4 CVA), eight device-related infections [5 episodes of bacteremia (2 device-related endocarditis)], three late anticoagulant-related bleeding episodes, and four technical complications which included changing Thoratec BVADs and performing cardiopulmonary resuscitation during a control console failure. In addition, both posttransplant deaths were in this group. This data supports what may be the most positive finding of this review. Significant problems continue to occur, but experience now supports the concept that many patients can recover from life threatening complications during mechanical circulatory support and proceed on to successful cardiac transplantation.

Until the morbidity associated with VADs is reduced, it is unlikely that implants will become more widespread or be performed on a more elective basis. In addition to the significant morbidity, bridging to transplantation is an expensive, labor-intensive procedure. In order to justify the use of significant resources and the donor organ, clinicians must assure that bridge patients who are transplanted survive as long and with a comparable quality of life as those patients transplanted without bridging. The overall survival with bridging could be improved with patient selection criteria that excluded some of the sicker patients. It is clear that the high-risk groups can be identified, however, more objective measurements of organ damage reversibility need to be determined. Clinicians will be hesitant to exclude anyone with a "reasonable" chance of survival (67% survival for this study) with a VAD from receiving support, since the alternative is almost certain death. Ventricular assist devices are now commercially available and should be considered conventional therapy at not only transplant centers, but also at many institutions performing cardiac surgery. This greatly expands the potential bridge population which may further complicate patient selection.

This report could be criticized for describing a small patient population undergoing VAD placement more than 18 years in retrospective fashion. Unfortunately, the low frequency of VAD placement means that an extended period is required to accumulate a significant volume of patients. While it is true that many changes occurred over this period, many factors remained constant. Although our data has been retrospectively analyzed, it was collected prospectively.

Despite many shortcomings, current techniques allow not only for reversals of cardiogenic shock but also significant rehabilitation in a majority of the patients supported. Those who avoid or recover from complications during the period of support can enjoy posttransplant survival in excess of 90% [4,14].

Although great progress has been made, bridging to cardiac transplantation continues to be associated with significant morbidity and mortality. However, our experience demonstrates that even those patients suffering major complications can, with time and effort, recover to near normal and undergo eventual transplantation. Our ability to successfully manage and reverse serious complications leads us to hold great hope as we proceed towards permanent implantable ventricular support devices.


   Appendix
 

Pre-VAD
Post-VAD
Age
 Total operating room time (VAD implant)
Gender
 Cardiopulmonary bypass time
Body surface area
 Type of support
Etiology of cardiomyopathy
 LVAD
Ischemic Postpartal BVAD (TAH included)
Idiopathic Congenital Device (Thoratec, Novacor or Symbion TAH)
Valvular Chronic rejection Late RVAD
Viral Acute rejection Implantable device
Cardiac index
 Days intubated
MAP
 Postoperative bleeding (VAD)
RAP
 Units blood products transfused
Mean PAP
 Hematocrit (first postop day)
Heart rate
 Platelet count (first postop day)
Intra-aortic balloon pump
 VAD flow (first postop day)
ECMO
 MAP (first postop day)
Ventricular tachyarrhythmias
 RAP (first postop day)
Cardiac arrest
 Mean PAP (first postop day)
Intubated
 VAD flow index (mean of total support time)
Prothrombin time INR
 Highest creatinine
Partial thromboplastin time
 Highest blood urea nitrogen (BUN)
Hemoglobin
 Dialysis
Hematocrit
 Ventricular tachyarrhythmias
Platelet count
 Infection (patient or device related)
White blood cell count
 Bacteremia
Fibrinogen
 Highest white blood cell count
Albumin
 Days IV antibiotics
Total bilirubin
 Late bleeding
Creatinine
 Cerebrovascular accident
Blood urea nitrogen (BUN)
 Hemolysis
Listed for cardiac transplantation
 Elevated circulating antibody levels
Diabetes mellitus
 Technical problems
Cerebrovascular accident
 Duration of support
History of congestive heart failure
Previous cardiac operation
Anticoagulants/platelet inhibitors
Infection
Number of days hospitalized
Experience


   Discussion
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 Discussion
References
 
DR ROBERT GUYTON (Atlanta, GA): It is a beautiful series. Your experience with ECMO looks fairly dismal, and my question would be whether or not that has led to a change in institutional policy with regard to the use of ECMO in these patients.

DR McBRIDE: No, it has not. We had eight patients that ultimately came to transplantation, so we will resuscitate apatient with ECMO and try to bridge them through.

DR FREDERICK L. GROVER (Denver, CO): Very nice paper and nice data. In the LVAD group, was there any difference between the two devices?

DR McBRIDE: No, there was no difference.


   References
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 Discussion
 References
 

  1. Pennington D.G., Joyce L.D., Pae W.E., Burkholder J.A. Patient selection. Ann Thorac Surg 1989;47:77-81.[Medline]
  2. Pennington D.G., Samuels L.D., Williams G., et al. Experience with the Pierce-Donachy ventricular assist device in postcardiotomy patients with cardiogenic shock. World J Surg 1985;9:37-46.[Medline]
  3. Norman J.C., Cooley D.A., Igo S.R., et al. Prognostic indices for survival during postcardiotomy intraaortic balloon pumping. J Thorac Cardiovasc Surg 1977;74:709.[Abstract]
  4. Pennington D.G., McBride L.R., Peigh P.S., et al. Eight years experience with bridging to cardiac transplantation. J Thorac Cardiovasc Surg 1994;107:472-480.[Abstract/Free Full Text]
  5. Ganzel B.L., Gray L.A., Jr, Slater A.D., Mavroudis C. Surgical techniques for the implantation of heterotopic prosthetic ventricles. Ann Thorac Surg 1989;47:113-120.[Abstract]
  6. Pennington D.G., McBride L.R., Swartz M.T. Implantation technique for the Novacor left ventricular assist system. J Thorac Cardiovasc Surg 1994;108:604-608.[Abstract/Free Full Text]
  7. DeVries W.C. Surgical technique for implantation of the Jarvik7–100 Total Artificial Heart. JAMA 1988;259:875-880.[Abstract/Free Full Text]
  8. Swartz M.T., Lowdermilk G.A., Moroney D.A., McBride L.R. Ventricular assist device support in patients with mechanical heart valves. Ann Thorac Surg 1999;68:2248-2251.[Abstract/Free Full Text]
  9. Holman W.L., Roye G.D., Bourge R.C., et al. Circulatory support for myocardial infarction with ventricular arrhythmias. Ann Thorac Surg 1995;59:1230-1231.[Abstract/Free Full Text]
  10. John R., Rajasinghe H., Chen J.M., et al. Impact of current management practices on early and late death in more than 500 consecutive cardiac transplant recipients. Ann Surg 2000;232:302-311.[Medline]
  11. Farrar D.J. Preoperative predictors of survival in patients with Thoratec ventricular assist devices as a bridge to heart transplantation. J Heart Lung Transplant 1994;13:93-101.[Medline]
  12. Korfer R., El-Banayosy A., Arusoglu L., et al. Single center experience with the Thoratec ventricular assist device. J Thorac Cardiovasc Surg 2000;19:596-600.
  13. Quaini E., Pavie A., Chieco S., Mambrito B. The concerted action "heart" European registry on clinical application of mechanical circulatory support systems: bridge to transplant. The Registry Scientific Committee. Eur J Cardiothorac Surg 1997;11:182-188.[Abstract]
  14. McCarthy P.M., Smedira N.O., Vargo R.L., et al. One hundred patients with the HeartMate left ventricular assist device: evolving concepts and technology. J Thorac Cardiovasc Surg 1998;115:904-912.[Abstract/Free Full Text]
  15. Frazier O.H., Rose E.A., McCarthy P.M., et al. Improved mortality and rehabilitation of transplant candidates treated with a long-term implantable left ventricular assist system. Ann Surg 1995;222:327-336.[Medline]
  16. Minami K., El-Banayosy A., Sezai A., et al. Morbidity and outcome after mechanical ventricular support using Thoratec, Novacor and HeartMate for bridging to heart transplantation. J Artificial Organs 2000;24:421-426.
  17. El-Banayosy A., Arusoglu L., Kizner L. Novacor left ventricular assist system vs. HeartMate vented electric left ventricular assist system as a long-term mechanical circulatory support device in bridging patients: a prospective study. J Thorac Cardiovasc Surg 2000;119:581-587.[Abstract/Free Full Text]
  18. Kawaguchi A.T., Cabrol C., Pavie A., et al. Survival prediction in staged heart transplantation using Jarvik-7 artificial heart. Circulation 1992;86(Suppl 2):311-315.[Abstract/Free Full Text]
  19. McBride L.R., Naunheim K.S., Fiore A.C., et al. Clinical experience with 111 Thoratec ventricular assist devices. Ann Thorac Surg 1999;67:1233-1239.[Abstract/Free Full Text]



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