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J Thorac Cardiovasc Surg 1994;107:450-0459
© 1994 Mosby, Inc.
Cardiac and Pulmonary Transplantation |
Middlesex, United Kingdom.
From the Cardiothoracic Surgical Unit, Harefield Hospital, Harefield, Middlesex, United Kingdom.
Address for reprints: Professor Magdi Yacoub, Harefield Hospital, Middlesex, UB9 6JH, United Kingdom.
Abstract
Obliterative bronchiolitis remains the leading cause of morbidity and mortality in long-term survivors after heart-lung transplantation. Despite enhanced immunosuppressive therapy, a significant number of patients progress to end-stage respiratory failure, leaving retransplantation as the only potential therapeutic option. Between October 1986 and August 1990, 25 heart-lung recipients (mean age 22 ± 2 years) underwent repeat heart-lung transplantation at an average of 21 months after their first procedure. Twenty-one patients (83%) were ventilator dependent at the time of retransplantation. The Kaplan-Meier survival at 1, 6, 12, and 24 months was 52%, 33%, 25%, and 25%, respectively. Post operative complications included bleeding, multisystem organ failure, and infection. Obliterative bronchiolitis resulted in death or graft failure in three patients between 12 and 36 months after the second transplantation. Five patients were currently alive at the time this article was written, with a median follow-up of 54 months. Three were in New York Heart Association class I, and two had obliterative bronchiolitis with class III symptoms. Recently, we investigated the role of single lung retransplantation in nine heart-lung recipients (mean age 23 ± 3 years). The mean interval between procedures was 36 months, and eight patients (88%) were ventilator dependent. The Kaplan-Meier survival at 1, 6, 12, and 24 months was 89%, 67%, 67%, and 50%, respectively. We observed significantly less perioperative morbidity in this group. Five patients were alive (median follow-up 20 months); four were in New York Heart Association class I or II, and one was in New York Heart Association class III with recurrent obliterative bronchiolitis. We did not have enough patients to perform multivariate survival analysis. Survival curve comparisons with the use of the Wilcoxon test did show that the absence of preformed antibodies in the recipient (panel reactive antibody frequency less than 10%) was associated with significantly improved survival after retransplantation. We also noted trends for improved survival in patients who had retransplantation at least 18 months after their original transplantation and in patients with negative preoperative sputum cultures. Retransplantation is a high-risk procedure that can result in rehabilitation in otherwise incapacitated patients. Single lung retransplantation appears to be the preferred option in carefully selected patients. (J THORAC CARDIOVASC SURG 1994;107:450-9)
Clinical heart-lung transplantation is an accepted form of therapy for patients with end-stage pulmonary vascular
1 and parenchymal lung disease. 2, 3 Between December 1983 and April 1993, 323 patients underwent primary heart-lung transplantation at Harefield Hospital for a variety of indications, including Eisengmenger's syndrome, primary pulmonary hypertension, cystic fibrosis, emphysema, and pulmonary fibrosis. Improvements in surgical techniques and immunosuppression have resulted in improved early survival, and late deterioration in lung function from obliterative bronchiolitis has now emerged as the most serious threat to long-term survival in heart-lung recipients. We have noted that the cumulative probability of obliterative bronchiolitis developing is between 30% and 40% within 3 years after heart-lung transplantation. 4 Patients typically have progressive dyspnea and a reduction in exercise capacity. Chest radiography may show hyperinflated lung fields and respiratory function studies may show air-flow obstruction manifested by a serial decrease in the measured forced expiratory volume in 1 second and forced expiratory volume in 1 second/forced vital capacity ratio. Although usually a clinical diagnosis, histologic confirmation of obliterative bronchiolitis is occasionally obtained on transbronchial lung biopsy specimens. Lung function will stabilize in approximately 50% of patients with aggressive augmentation in immunotherapy. The condition of a similar number of patients, however, progressively deteriorates into terminal respiratory failure, leaving retransplantation as the only potentially effective option. The role of surgical intervention in heart-lung recipients with obliterative bronchiolitis has not been previously defined. This report documents our experience with repeat heart-lung or single lung transplantation in patients with terminal respiratory failure after heart-lung transplantation.
METHODS
Patients
Previous heart-lung recipients with progressive severe respiratory failure as a result of obliterative bronchiolitis were treated by either repeat heart-lung or single lung transplantation. The original diagnoses leading to primary heart-lung transplantation are shown in Table I. Between October 1986 and August 1990, 19 female and 6 male patients underwent repeat heart-lung transplantation. The mean interval between the first and second transplantations was 21 ± 3 months, with a range of 7 to 61 months. The mean age at repeat transplantation was 22 ± 2 years, with a range of 5 to 41 years. Twenty-one patients (83%) required ventilatory support (20 conventional and 1 nasal intermittent positive-pressure ventilation 5) at the time of repeat transplantation, with time of ventilatory support ranging from 2 to 58 days. Only one patient in the group was not hospitalized and remained ambulatory at the time of repeat transplantation. Seventeen patients (72%) had positive sputum cultures at the time of repeat transplantation. Generalized poor nutrition was another characteristic feature, and 23 patients (92%) required enteral feedings at the time of retransplantation—in most instances begun several months before institution of ventilatory support.
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Donor management
Our general method for donor procurement has been previously summarized. 6 We cooled heart-lung or single lung donors until their core temperature was approximately 10° C with the use of a portable cardiopulmonary bypass machine transported to the donor hospital by our retrieval team. After cooling, the heart was arrested with potassium blood cardioplegic solution, and the excised heart-lung block was transferred back to Harefield Hospital packed in ice.
Donor-recipient matching
We attempted to match donor and recipient chest sizes. Donors were matched to recipients on the basis of ABO blood group compatibility but not for rhesus blood group. We also attempted to match cytomegalovirus (CMV)-negative donors and CMV-negative recipients. The preoperative presence of preformed lymphocytotoxic antibodies was determined prospectively in a microcytotoxic assay against a panel of random volunteer lymphocytes known as the panel reactive antibody (PRA) test. 7 We considered patients positively sensitized if the measured PRA frequency was greater than 10%. A donor specific lymphocytotoxic crossmatch was always performed retrospectively or prospectively if possible with standard techniques. 7 We did not prospectively match for human leukocyte antigens.
Recipient operation
The basic surgical techniques for repeat heart-lung transplantation are similar to those used during the primary heart-lung transplant. 8 The degree of difficulty of dissection varied from patient to patient, but in general we began the recipient procedure about 3 hours before anticipated donor arrival. The method of cannulation and excision of the heart was similar to that used for orthotopic heart transplantation. We emphasized dissection of the hilum as close as possible to the main bronchus, particularly posteriorly, to avoid injury to the vagus nerves. We always excised the previous tracheal suture line and applied Tisseal fibrin sealant (Immuno-AG, Vienna, Austria) to the posterior mediastinum and used an Argon Beam coagulator (Beacon Labs, Broomfield, Colo.) to cauterize mediastinal and pleural raw surfaces in an attempt to lessen postoperative bleeding. Monofilament absorbable PDS sutures (Ethicon, Inc., Somerville, N.J.) were used for the tracheal anastomoses and Prolene sutures (Ethicon) were used for the aortic and atrial anastomoses.
The basic surgical principles outlined previously were also used in patients undergoing single lung transplantation after heart-lung transplantation. In this group of patients, special consideration regarding the selection of the appropriate side for retransplantation was important. Occasionally patients had undergone a previous thoracotomy before or after primary heart-lung transplantation, and we transplanted via the opposite side in this setting. Preoperative bronchoscopy and coronary angiography were important adjuncts in these patients to rule out proximal bronchial airway disease or coronary arterial disease. Preoperative computed tomography was also performed, and, if possible, we transplanted the lung with the more significant radiologic features of obliterative bronchiolitis, including bronchiectasis and significant pleural thickening. In one patient, donor availability also played a necessary role in side selection.
Immunosuppression
Patients were receiving maintenance cyclosporine and azathioprine before retransplantation. Methylprednisolone 10 to 15 mg/kg was given intravenously at the time of initial reperfusion. Routine immunosuppression was achieved after the operation with cyclosporine, azathioprine, and rabbit antithymocyte globulin (RATG). Intravenous cyclosporine was converted to oral dosing with the aim to attain levels of 500 ng/ml (whole blood monoclonal antibody assay) during the first postoperative month, and after that from 250 to 350 ng/ml. If renal dysfunction with elevation of serum creatinine greater than 200 µm/L occurred, cyclosporine therapy was reduced or stopped, and patients were given azathioprine and prednisolone 0.2 mg/kg per day until renal function stabilized and cyclosporine could be readministered. Azathioprine was given at a dose of 2 mg/kg per day, provided the white blood cell count remained above 4000/ml. RATG (100 mg intravenously) was given on alternate days for the first 10 postoperative days, with the goal of maintaining a total T cell count of less than 200/ml. Patients were initially maintained on cyclosporine and azathioprine with minimal or no steriods.
Preoperative and postoperative monitoring of rejection
Compared with pulmonary rejection, episodes of cardiac rejection were rare. Patients were followed-up for pulmonary rejection clinically, radiographically, and by serial respiratory function tests. Dyspnea, pyrexia, leukocytosis, reduction in lung function, unexplained cough, and radiographic abnormalities were considered indicators of acute rejection. Patients were further investigated by fiberoptic bronchoscopy, bronchiolar lavage, and transbronchial lung biopsy. Patients suspected to have acute rejection were treated with intravenous methylprednisolone 1 gm/day for 3 consecutive days, occasionally supplemented with RATG. Late deterioration in lung function usually resulted from the development of obliterative bronchiolitis. Patients typically had insidious symptoms, including a dry cough and breathlessness, and daily spirometric studies revealed a gradual fall in the forced expiratory volume in 1 second and the forced expiratory volume in 1 second/forced vital capacity ratio. Bronchiolitis obliterans was a diagnosis made primarily on clinical grounds, with occasional histopathologic confirmation provided by transbronchial biopsy. Patients with this diagnosis were treated with aggressive augmentation in their immunosuppression, which generally consisted of methylprednisolone pulsing followed by the addition of high-dose steroids (1 mg/kg per day for 1 month) to the standard cyclosporine/azathioprine maintenance therapy. Respiratory function in about one half of patients with obliterative bronchiolitis stabilized, whereas the remaining patients had terminal respiratory failure. If high-dose steroid therapy failed and the decision was made to proceed with retransplantation, administration of steroids was gradually tapered to 0.2 mg/kg per day or discontinued if possible.
Infection
Patients receiving preoperative antibiotics for chronic pulmonary bacterial infections were maintained on similar doses of the same drugs after the operation for 10 days pending new culture and sensitivity data. Otherwise, patients received cefotaxime immediately before transplantation and after the operation for 10 days. They also received intravenous flucloxacillin prophylactically (unless the patient was allergic to penicillin) while chest tubes and central lines were in place. Nebulized antibiotics were also administered according to appropriate sensitivity results. Episodes of pulmonary infection were differentiated from acute rejection by a combination of clinical and radiologic findings together with studies of bronchiolar lavage specimens and transbronchial biopsy specimens. All patients received prophylactic acylovir for a period of 3 months and during episodes of augmented immunosuppression. Patients suspected of having active CMV infection (suggested by rising antibody titers, antigen staining on bronchiolar lavage specimens, histologic evidence on biopsy specimens, or any combination thereof) were treated with intravenous gancyclovir 5 mg/kg per 12 hours for 14 to 21 days.
Follow up
All patients were seen at regular intervals of 1 to 3 months when clinical evaluation, chest radiography, and respiratory function studies were performed. In addition, patients were given manual spirometers to check their respiratory function on a daily basis.
Statistical analysis of outcome predictors
Kaplan-Meier survival curves 8 were constructed for the repeat heart-lung and single lung transplantation groups, as well as for 292 first time heart-lung recipients, at Harefield Hospital. Given the small number of patients undergoing retransplantation and the even smaller numbers when subgroups are formed, we could not perform multivariate survival analysis (Cox proportional hazards modeling). We did compare Kaplan-Meier survival curves fit for different potential predictors of outcome (Table II) with the use of the Wilcoxon-Gehan test. 10 Specifically, we analyzed the influence of age, sex, original diagnosis, year of retransplantation, interval to retransplantation, ventilator status, preoperative sputum culture, CMV status of the donor and recipient, ABO status, PRA status of the recipient, donor specific crossmatch, and human leukocyte antigen (HLA-DR) compatibility on survival. Repeat heart-lung and single lung groups were analyzed separately and together, and the data presented represent analysis of the combined group of 34 patients.
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Repeat heart-lung transplantation
Kaplan-Meier survival for patients undergoing repeat heart-lung transplantation was 52%, 33%, 25%, and 25% at 1, 6, 12, and 24 months, respectively, which was significantly worse (p < 0.05) than the 75%, 59%, 57%, and 51% survival at similar time intervals observed in 292 patients undergoing primary heart-lung transplantation at our institution (Fig. 1). Bleeding was the most significant early complication in patients in the repeat heart-lung group (Table III). Two patients (8%) died on the operating room table because of uncontrollable bleeding. Nine patients (36%) required reoperation (seven thoracotomy, two resternotomy) for bleeding after graft implantation. Most significantly, excessive bleeding was associated with early death in eight patients (32%) (48-hour mean blood transfusion requirement 38 ± 4 U). Nerve injuries occurred in two patients (one phrenic nerve, one recurrent laryngeal nerve) during the second transplant procedure. The causes of early (<90 days) and late (>90 days) mortality are summarized in Table IV. There were 15 early deaths in the repeat heart-lung group. Seven patients died of multisystem organ failure, and excessive bleeding was thought to be a contributing factor in five patients, possibly with bacterial sepsis as an underlying component in the other two. Two patients died of primary cardiac graft failure, and one of these patients also experienced early excessive bleeding. One patient died from Aspergillus aortitis involving the proximal aortic suture line. The remaining infections resulting in death involved Pseudomonas, Aspergillus, CMV, or combinations thereof. There were two late deaths resulting from the development of terminal obliterative bronchiolitis in the second graft 12 months and 17 months after retransplantation. A third patient with obliterative bronchiolitis underwent successful single lung transplantation 36 months after repeat heart-lung transplantation (considered death a result of obliterative bronchiolitis at 36 months for statistical purposes).
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Single lung retransplantation
Kaplan-Meier survival for heart-lung recipients undergoing single lung transplantation was 89%, 67%, 67%, and 50% at 1, 6, 12, and 24 months compared with 52%, 33%, 25%, and 25% at similar time intervals in the repeat heart-lung group (Fig. 2). Bleeding was not a significant complication in patients in the single lung group (
Table III). There were no intraoperative or postoperative deaths associated with excessive bleeding, and only one patient (11%) required reoperation for bleeding. Three of nine patients required cardiopulmonary bypass, and the single reoperation for bleeding occurred in one of these patients. No nerve injuries occurred in this group. There were two early deaths (Table IV). One patient died of multisystem organ failure triggered by a low output state and the other from Pseudomonas sepsis. One late death resulted from CMV sepsis, whereas another patient had recurrent obliterative bronchiolitis 17 months after single lung retransplantation
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Analysis of outcome predictors
Multivariant analysis was not suitable for this study. Survival curve comparisons using the Wilcoxon test showed that age, sex, original diagnosis, year of transplantation, ventilator status, CMV status of the recipient, ABO identical versus compatible matching, and HLA-DR compatibility did not have an impact on outcome. The absence of preformed antibodies in the recipient (negative PRA status) was significantly associated with improved survival (p < 0.05) (Fig. 3). A trend was noted toward improved survival in patients with an interval between first and second transplants greater than 18 months (the median time for all patients) (Fig. 4). A trend for improved survival was also seen in patients with negative preoperative sputum cultures (Fig. 5). Finally, possible trends for improved survival were noted in crossmatch-negative recipients and in recipients receiving CMV-negative donor organs, although p values reflect the small numbers represented at the various times of analysis (Figs. 6 and 7).
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Obliterative bronchiolitis is the major cause of death of long-term survivors after heart-lung transplantation. 4, 11 Although augmented immunosuppression stabilizes lung function in some patients, 12 a similar number experience progressive deterioration, leaving terminal ventilation or retransplantation as the only remaining effective treatment options. This study has shown that repeat heart-lung transplantation can result in a satisfactory quality of life in a small percentage of patients. The significant prevalence of perioperative bleeding and early multisystem organ failure, however, results in a 30-day mortality rate of approximately 50%, compared with 25% in patients undergoing first time heart-lung transplantation. Our data would suggest single lung transplantation for obliterative bronchiolitis is preferable to repeat heart-lung transplantation. The single lung procedure is less complex technically and does not require cardiopulmonary bypass in the majority of patients, and the absence of cardiopulmonary bypass diminishes the impact of excessive bleeding on early survival; this is reflected in the 30-day mortality rate of only 11% in the single-lung group. It should also be pointed out that, in general, the majority of single lung transplantations occurred later in our overall experience, and this tendency might also be anticipated to translate into improved survival in the later group. Although we were initially concerned about the healing of the bronchial anastomosis between the new lung graft and the original graft's mainstem bronchus, this has not been a problem. Recently, we used the internal mammary artery to directly revascularize an intercostal-bronchial artery in two patients in the single lung group to optimize early healing. Single lung transplantation appears to be suitable for the majority of heart-lung recipients who require retransplantation because the presence of bronchial complications or significant coronary disease is rare in our experience.
Because of the small numbers resulting from subgrouping of our 34 patients, we lack the statistical power to clearly define predictors of outcome. For instance, 29 of 34 recipients had CMV-positive diagnoses, and, similarly, 27 of 34 recipients required conventional ventilatory support at the time of the second transplantation; we therefore cannot comment on the influence of these variables on overall survival. Our findings of a significant correlation between PRA status and poor graft survival mimics our findings in 283 first-time heart-lung recipients, where patients with a positive PRA frequency (greater than 10%) had a 1-year actual survival of 39% compared with 64% in recipients with a PRA-negative diagnosis (p = 0.008). We also observed a trend toward improved survival in patients with longer intervals between the first and second transplantation, suggesting patients who aggressively reject their first graft are more likely to do the same after undergoing retransplantation. The data also suggest that patients with negative preoperative sputum cultures fare better, although airway colonization is probably inevitable in many patients, considering over 80% required ventilatory support before their second transplantation.
Previous literature regarding retransplantation in heart-lung recipients with chronic rejection is anecdotal. 11 Similarly, many centers have published limited experiences with repeat lung transplantation for obliterative brochiolitis after primary lung transplantation. 11, 13-15 Recently, Novick and colleagues 15 published their results of an international survey involving 20 centers in North America and Europe in which the result of 63 single or double lung retransplantation procedures in 61 single lung, double lung, or heart-lung recipients with obliterative bronchiolitis (32 patients), graft failure (14 patients), intractable airway disease (8 patients), severe acute lung rejection (5 patients), and miscellaneous complications (4 patients) were described. They noted actuarial survival after lung retransplantation to be 65%, 42%, 35%, and 32% at 1, 6, 12, and 18 months, respectively, and noted survival did not differ according to indication for the second transplant. They also noted trends toward improved survival in patients ambulatory before retransplantation and in patients receiving ABO identical grafts. They also noted significantly improved survival (p < 0.05) in patients receiving CMV-negative organs. Analysis of the group undergoing retransplantation for obliterative bronchiolitis showed a trend for improved survival in patients undergoing ipsilateral retransplantation. In contrast to our results, the subset of patients undergoing single lung transplantation for obliterative bronchiolitis after previous double lung or heart-lung transplantation had actuarial survival of 32% and 21% at 3 and 12 months, respectively. On the basis of these data, it was suggested that leaving a damaged, frequently colonized lung graft in situ was detrimental to overall survival after retransplantation. It is difficult to make comparisons between these data involving patients from multiple centers with differing experience and protocols and our data from a single institution. It is possible that our improved survival in the group undergoing single lung transplantation compared with the multicenter survey is due to our larger cumulative experience with retransplantation in general. Our practice of steroid-free maintenance immunotherapy perhaps also decreases the prevalence of sepsis-related complications arising from the remaining contralateral lung graft, assuming at least some of the patients in the multicenter survey received maintainance long-term steroid therapy.
In light of the limited availability of suitable thoracic organ donors, the value of retransplantation of incapacitated heart-lung recipients can be appropriately questioned on the basis of the overall poorer survival of these patients compared with that of patients undergoing primary heart transplantation, lung transplantation, or both. The question of whether it is reasonable to provide patients with a second graft and thereby perhaps deny another patient a possible first transplant presents another ethical quandary. Despite the high risks, retransplantation can nevertheless result in full rehabilitation in otherwise terminally ill patients, and we believe it must therefore be considered as a therapeutic option on an individual basis. Furthermore, as the experience with these procedures increases, one can expect a decline in the early morbidity and mortality associated with retransplantation. Although the prevalence of obliterative bronchiolitis in the second graft does not appear to be increased, this disease process continues to represent a major risk to survival in patients undergoing heart-lung retransplantation.
Appendix: DISCUSSION
Dr. Richard J. Novick (London, Ontario, Canada).
Last year we presented and published a North American–European series of 63 cases of pulmonary retransplantations (J Heart Lung Transplant 1993;12:5-16). Thirty-two of these patients underwent reoperation for end-stage obliterative bronchiolitis. Recently I presented the intermediate-term results in these 32 patients, with complete follow-up averaging 2 years.
Our results differed from those of the Harefield group, especially when actuarial survival after reoperation was analyzed according to the type of retransplant procedure. In our experience, patients undergoing double lung transplantation as a second operation and those receiving an ipsilateral single lung retransplant tended to fare better than those undergoing a redo single lung transplantation on the contralateral side and patients in whom a single lung transplantation was performed after a previous double lung or heart-lung transplantation. After the second transplant operation, 59% of patients had an old retained contralateral graft, whereas 41% did not. Actuarial survival was significantly better in those patients without an old contralateral graft as compared with those patients with an old contralateral graft; at 1 year, survival was 62% in the former, as opposed to 26% in the latter group. As assessed by Wilcoxon analysis, the difference between curves was statistically significant. Finally, a Cox multiple hazard analysis of 17 covariates indicated that one of the two most significant variables predictive of survival was the absence of an old contralateral graft after retransplantation.
I have two questions and one comment for Dr. Adams. First, in the single lung group, how long did it take in the postoperative period for the new graft to become colonized by microorganisms originating from the retained, chronically rejected (and probably infected) allograft? Second, what antibiotic and immunosuppressive regimen did the Harefield group use in the perioperative period in retransplant recipients? Was it different from that used for first-time lung transplant recipients, particularly vis-à-vis steroid maintenance therapy?
My final comment relates to the fact that the two procedures described by Dr. Adams were performed in different time frames: redo heart-lung transplantation was carried out from 1986 to 1990 and single lung transplantation after heart-lung transplantation was usually performed from 1990 to 1992. The superior results in the second group may very well have been due to increasing experience in the operative and postoperative treatment of lung retransplant patients rather than due to a true difference between the two procedures. In fact, in our series, second independent predictor of survival was reoperation in a more recent time frame (i.e., after 1990). Did you subject your data to a Cox hazard analysis to determine whether the year of retransplantation influenced survival?
Dr. Adams.
Your first question related to our antibiotic prophylaxis. If patients were receiving antibiotic therapy before the operation and sensitivities were available, we would continue the same antibiotics after the operation for 10 days as a routine. If patients were not receiving antibiotic therapy before the operation, they were given a third-generation cephalosporin for the first 10 days, and we would obviously tailor these antibiotics according to available culture and sensitivity results.
With regard to your question about colonization in the new graft, I cannot answer that; I do not have the data. With regard to immunosuppression, we did not alter therapy for our second-time transplant recipients. They were given methylprednisolone (Solu-Medrol) and antithymocite globulin initially and received maintainance cyclosporine intravenously and then orally in combination with azathioprine. At Harefield we use a steroid-free maintenance protocol, and we continued that practice in this group with the use of steroid pulsing and steroid therapy for either acute rejection or more long-term steroid therapy in patients with evidence of recurrent obliterative bronchiolitis.
Finally, you commented about the year of retransplantation and improved results. We did look at that by the Wilcoxon test and we did not see a difference. Our confidence interval has improved with time, however, and we believe one of the reasons the single lung group has fared better is because of the experience we gained in the repeat heart-lung group. If we had larger numbers, I think that point would certainly be borne out, but that does not change the fact that the single lung procedure is less complex; if it continues to result in significant rehabilitation, it will probably be the preferred option in affected heart-lung recipients, except in patients with significant bilateral obliterative bronchiolitis or disseminated infection in both lungs.
Acknowledgments
We thank Drs. Rosemary Radley-Smith and Brendan Madden for their review of patient follow-up data and Elizabeth Allred, MS, for performing the statistical analysis. We also thank Helen Garlic and Jacqueline Smith for their help with data retrieval and Teresa Kearns for manuscript preparation.
Footnotes
Read at the Seventy-third Annual meeting of The American Association for Thoracic Surgery, Chicago, Ill., April 25-28, 1993. 
*Dr. Adams is the 1992-1994 Alton Ochsner Research Scholar of the American Association for Thoracic Surgery.
References
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