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J Thorac Cardiovasc Surg 2000;120:99-107
© 2000 The American Association for Thoracic Surgery
GENERAL THORACIC SURGERY |
From the Divisions of Cardiothoracic Surgery and Pulmonary and Critical Care Medicine, Washington University School of Medicine, St Louis, Mo.
Address for reprints: Bryan F. Meyers, MD, 3107 Queeny Tower, One Barnes-Jewish Hospital Plaza, St Louis, MO 63110-1013 (E-mail: meyersb{at}msnotes.wustl.edu ).
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Abstract |
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 Top Abstract IntroductionPatients and methods Results Discussion Appendix: Discussion References |
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Introduction |
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TopAbstractIntroductionPatients and methods Results Discussion Appendix: Discussion References |
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1 A subsequent report from the Toronto group described results after single lung transplantation for 20 patients with fibrotic lung diseases, including idiopathic pulmonary fibrosis (IPF), sarcoidosis, eosinophilic granuloma, and pulmonary fibrosis caused by chemotherapeutic drugs. 2 The Toronto group experienced a perioperative mortality of 20% and a 1-year survival of 45%, which at the time represented major advances. The choice of pulmonary fibrosis as the first disease to be treated with isolated lung transplantation was not random; it was selected with the thought that restrictive pulmonary function and the moderately elevated pulmonary vascular resistance would lead to selective ventilation and perfusion of the graft lung. Transplantation has subsequently been applied more broadly to other end-stage lung diseases, but IPF remains the second most frequent diagnosis leading to transplantation according to the Fifteenth Report delivered in July 1998 by the International Society of Heart and Lung Transplantation. Emphysema and 
1-antitrypsin deficiency emphysema together accounted for 55% of transplants, with IPF next at 20.9% of transplants. 3 The current report is a review of our institutional experience with lung transplantation, specifically for IPF. An effort is made to compare the results obtained with single and bilateral transplantation in patients with pulmonary fibrosis. |
Patients and methods |
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TopAbstractIntroductionPatients and methods Results Discussion Appendix: Discussion References |
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Statistical methods
All normally distributed continuous data (eg, forced expiratory volume in 1 second [FEV1] and age) are expressed as means ± SD. Two group comparisons of normally distributed continuous data are made by means of the unpaired t test. Nonnormally distributed data (ie, postoperative hospital stay) are expressed as median and interquartile (25%-75%) range. Two-group comparisons in these data sets are made with the Mann-Whitney U statistic. The combined effects of time and type of procedure on repeated measurements of physiologic function were analyzed by use of the Mixed Procedure (PROC MIXED) in SAS version 7 (SAS Institute, Inc, Cary, NC). Survival estimates were calculated with the Kaplan-Meier method. Comparison of survival of different groups of patients is done with the Mantel-Haenszel test. Tabular data are compared by the Fisher exact test. A multivariate Cox regression analysis was used to test the effect of the variables described in Table I on overall survival. With the exception of the PROC MIXED test, data analysis was performed by means of SYSTAT version 7.0 (SYSTAT, Inc, Evanston, Ill).
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4-6 In brief, patients are selected when they have disabling lung disease with a limited prognosis and no other systemic illness that would complicate or be complicated by lung transplantation and immunosuppression. In contrast to those with obstructive physiology, patients with pulmonary fibrosis whose condition has deteriorated to the point of necessitating transplantation generally have a rapid downhill course. Relative indications for early referral for transplantation include resting hypoxemia, worsening desaturation with exercise despite supplementary oxygen, failure to respond to medical therapy, and a decreasing trend in sequential measurements of vital capacity.
Procedure selection
In our earliest experience, single lung transplant was the only procedure offered, and its application was limited to patients free of pulmonary sepsis or cavitary disease. When bilateral lung transplantation became increasingly reliable, this alternative was also offered to patients with IPF. Since that time, we have been performing either single or bilateral transplants, with the decision based primarily on organ availability. Barring any specific anatomic constraints, patients will generally be listed for "either or both," indicating a willingness to accept a single graft for either the right or left lung or a bilateral graft. Single lung transplants have remained more common, despite our willingness to perform a bilateral procedure, presumably because of the increased availability of single lung grafts and the lack of any evidence for the superiority of the bilateral transplantation in this disease.
Preoperative treatment
Once patients are listed for lung transplantation, efforts are made to optimize their medical care to enhance survival and function while on the organ waiting list. For all patients, this involves enrollment and active participation in pulmonary rehabilitation. Adjustment of medications may include weaning of steroids to minimize the complications of corticosteroids during the time spent on the waiting list for donor lungs. Preoperative therapy ranges from ensuring continued compliance with pulmonary rehabilitation to acute management, including intubation and intensive care when deterioration occurs during the waiting period. Although patients will generally not be listed if they are intubated, patients who decline after listing for transplantation are still considered if their general health is otherwise compatible with postoperative recovery from a transplant operation.
Donor selection
The criteria for lung donors are well established and are applied to pulmonary fibrotic recipients, just as they are to patients with other diagnoses. Our donor lung selection criteria and our operative techniques for lung procurement have recently been reviewed. 7 Specific modifications for recipients with pulmonary fibrosis occur mainly with regard to the size of acceptable donor lungs. For example, when planning a lung transplantation for obstructive lung disease, we attempt to place allografts with 15% to 20% greater volume than the recipient’s predicted lung volume. Implantation of such a large allograft is easily achieved in a patient with obstructive lung disease because the recipient pleural space may be two or more times the predicted volume. The restrictive nature of pulmonary fibrosis causes the lungs and pleural spaces to be markedly reduced in size. It is therefore inadvisable to oversize these patients to an excessive degree. For bilateral lung replacement, we prefer to match the donor lung volumes to the predicted normal lung volume. A bilateral transplant with oversized donor lungs for a recipient with pulmonary fibrosis may produce hemodynamic difficulties at the termination of the procedure.
Operative techniques
Our current operative technique has been described in previous publications. 8 Single lung transplantation is generally performed through a posterolateral thoracotomy, and the technique has varied little over the time span of this report. The lung chosen for replacement is resected, and the donor lung is implanted, generally without the need for cardiopulmonary bypass. Bilateral lung transplantation has been typically performed through a clamshell incision consisting of bilateral anterolateral thoracotomies with transverse division of the sternum to allow maximal exposure. 9 For the past 3 years, we have been omitting the sternal division in an effort to avoid the major and minor complications commonly encountered with sternal division and subsequent closure. 10 The use of omentum to wrap the bronchial anastomosis was limited to the earliest fraction of the patients described in this report. Cardiopulmonary bypass was used on an individualized basis in cases of concomitant pulmonary hypertension or when hypoxemia or hypercarbia would not allow single lung ventilation during the implantation of the first lung. The IPF recipients pose challenges on implantation because of their diminished chest volumes and the difficulty in maintaining adequate topical hypothermia with iced saline slush during surgery. The use of malleable retractors to depress the diaphragm during implantation has partially overcome this problem.
Postoperative care
Early postoperative care occurs in the intensive care unit, with mechanical ventilation and invasive cardiac monitoring. We routinely extubate patients as soon as standard weaning criteria are met. A flexible bronchoscope is used at the time of extubation and again 7 to 10 days after transplantation. Immunosuppression consists initially of cyclosporine (INN: ciclosporin), corticosteroids, and azathioprine, with the addition of antithymocyte globulin during the first several postoperative days. 5 As might be expected, the management of acute rejection has changed dramatically over the period of these observations. The early experience was marked by frequent empiric boluses of intravenous corticosteroids based on clinical parameters, such as fever, hypoxemia, and pulmonary infiltrates. The recent practice is more objective and guided by transbronchial biopsies to accurately diagnose rejection before intensifying the immunosuppression. Similarly, prevention and treatment of cytomegalovirus (CMV) infection has been streamlined in the 10 years that constitute this experience. It is our current practice that recipients negative for CMV receiving CMV-positive grafts receive prophylactic ganciclovir intravenously for 6 weeks postoperatively.
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Results |
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TopAbstractIntroductionPatients and methods Results Discussion Appendix: Discussion References |
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. There was no significant preoperative difference between patients given single lung transplants and patients given bilateral lung transplants when compared according to sex distribution, age, or functional status as described by oxygen use, FEV1, forced vital capacity, and 6-minute walk distance.
Donor lung characteristics
Using criteria described in a previous publication, 11 we classified donor lungs as either ideal or marginal. The lungs implanted in this series were deemed ideal in 37 cases and marginal in 10 cases. Marginal lungs were only used when the transplant was bilateral. Thirty-six lung grafts were procured at a distance from St Louis, which required air travel to allow timely procurement and return, whereas 11 donors were local. In 32 cases the procurement was performed by a member of our operative team, whereas the other 15 procurements were performed by other teams in the course of retrieving the contralateral lung or the heart. The mean ischemic times were 263 minutes for right lungs and 290 minutes for left lungs.
Recipient operation
There were no intraoperative deaths. The mean length of operation was 5.4 hours. Eight patients required cardiopulmonary bypass, and one patient had such severe immediate reperfusion injury that weaning from bypass proved impossible, and the patient was maintained on extracorporeal membrane oxygenation postoperatively. Operative times and ischemic times were similar for the patients receiving single and bilateral transplants. There was a statistically significant difference in the frequency of use of cardiopulmonary bypass, with bypass being used in 6 (46%) of 13 of the bilateral transplants and only 2 (6%) of 32 of the single lung transplants. The number of transplants per year and the ratio of single/bilateral transplants have remained stable throughout the studied time period.
Postoperative results
The summary of early hemodynamic measurements appears in Table II. There was an immediate fall in the pulmonary vascular resistance, but all hemodynamic changes were mild in magnitude and failed to reach statistical significance. This analysis is prone to bias because the typical patient doing well postoperatively will have a low pulmonary artery pressure, low pulmonary vascular resistance, and high cardiac output. This good function will lead to removal of the pulmonary artery catheter and cause later observations to be weighted in the direction of the poorly performing patients. Four patients, all male subjects, were considered operative deaths. Causes of death included an anastomotic dehiscence leading to death on postoperative day 37, primary graft failure and rejection causing death on postoperative day 33, sepsis and ischemic bowel with death on postoperative day 37, and primary graft failure and renal failure with death on postoperative day 9 despite retransplantation. The frequency of adverse events in single and bilateral transplant recipients are displayed in Table III. Forty-one patients survived the operation and were discharged from the hospital. Some details regarding the length of hospitalization are recorded in Table IV. When single lung transplantation and bilateral lung transplantation for IPF were compared, there was no significant difference in the length of hospitalization or in the prevalence of adverse events encountered postoperatively.
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, the FEV1 data show a statistically significant time effect over the period of observation (P < .0001). There is no significant difference when the patients are compared according to type of transplant (P = .088) and no interaction between time and type of transplant (P = .7). Similarly, Fig 2 shows the distances traveled in a 6-minute walk over various intervals from the time of transplantation. The 6-minute walk distances show a statistically significant change over time (P < .0001) after transplantation, which is not significantly different between single and bilateral recipients (P = .37). When individual intervals between evaluation and follow-up measurement were assessed with the same statistical tool (ie, evaluation to 3 months and evaluation to 12 months), none of the specific interval changes for either FEV1 or 6-minute walk distance were statistically significant. Similar findings were noted in other measured indicators of function, including forced vital capacity and room air arterial blood gasses.
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. None of the variables were statistically significant predictors of survival. Late deaths have occurred in 17 patients, and the causes for these deaths are listed in Table V. Bronchiolitis obliterans syndrome is the leading cause of late mortality. There has been no recurrence of pulmonary fibrosis in any allograft.
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Discussion |
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TopAbstractIntroductionPatients and methods Results Discussion Appendix: Discussion References |
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12 Such a restriction will describe a relatively uniform group of patients with a progressive and generally fatal disease with a median survival between 2 and 3 years. Less-precise diagnostic classification will include patients with other similar disorders with better prognoses and less-predictable downward courses.
The poor prognosis of patients with IPF is well established. Harari and colleagues 13 reported on the actuarial survival of 43 patients with IPF referred for transplantation who were comparable in many criteria with the patients described in our report. By censoring patients actually undergoing transplantation (treating them as lost to follow-up at the time of transplantation), they observed a median survival of less than 10 months and a 2-year survival of 25% compared with the median post-transplantation survival of 5 years and a 2-year survival of 73% described in this report. Such a comparison is hazardous; the medically treated patients included all patients with IPF listed for transplantation, whereas the surgically treated patients are the result of selection bias, which has removed all patients too sick to survive on the waiting list until donor lungs became available. Still, the high mortality of medically treated patients at least provides a benchmark that makes the post-transplantation median survival more meaningful.
Once the patient with IPF receives a transplant, there is much evidence to suggest that the early post-transplant course is more difficult than that seen for patients with other underlying diagnoses. The first-year survival of our patients with IPF is 75.5%, which is not statistically different from the 1-year survival of 85.5% seen in our entire cohort of transplant recipients, excluding patients with IPF. Similarly, the data reported to the United Network for Organ Sharing (UNOS) describes a 1-year survival of 74% for IPF recipients compared with 82% for emphysema and 80.3% for cystic fibrosis. 14 This difference in early outcome of our recipients has been previously described by Davis and colleagues. 15 In that report, 16 patients with IPF were compared with 43 patients with emphysema and 24 patients with pulmonary hypertension. The patients with IPF had the worst initial gas exchange, the highest initial pulmonary artery pressures, the highest peak airway pressures, the longest ventilatory times, the longest intensive care unit stays, and the highest tracheostomy rates. Thus, it appears the conclusion of one author that "no underlying disease in transplantation poses the dramatic difficulties faced in association with advanced pulmonary fibrosis" is an accurate observation. 16 It is interesting to note, however, that the data collected by the International Society for Heart and Lung Transplantation (ISHLT) failed to single out IPF as a risk factor for increased mortality at 1 year, and our own data from the current report did not show a statistical difference in survival between patients with and without IPF. The ISHLT multivariate analysis of risk factors for 1-year mortality after lung transplant showed only primary pulmonary hypertension to have an odds ratio for mortality greater than 1 (1.31). At the other end of the spectrum, emphysema (0.48) and 1-antitrypsin deficiency (0.74) had odds ratios of less than 1. IPF did, however, fall out as having a greater risk for 5-year mortality, with an odds ratio of 1.68 (confidence intervals, 1.16-2.43) and a P value of .01. 3
Our data cannot support any claim of superiority for bilateral transplantation over single lung transplantation. There was no functional difference as measured by 6-minute walk distance and FEV1, and the differences in survival between the groups did not reach statistical significance. This can be added to other reports with similar conclusions regarding the single-versus-bilateral debate for emphysema 17-19 and for pulmonary hypertension. 20 Such a simple comparison can be misleading, though. For instance, in transplants performed for diagnoses that allow either single or bilateral grafts, the preoperative plan to perform a bilateral transplant may be altered intraoperatively on the basis of the difficulty of the dissection or the discovery of severe reperfusion injury on unclamping the hilum of the first graft. Such a decision may be lifesaving for the patient, leaving behind a native lung that acts as a buffer for the poor initial function of the graft lung, yet the practice will bias retrospective analysis against single lung transplantation by including all such complicated patients in the single lung transplantation group. With respect to our data, the preponderance of left single lung transplants in this report (24 left vs 8 right) raises some questions and is not easily explained.
In summary, our data show that patients with IPF can undergo successful transplantation with an operative mortality of less than 10%. Median survival in excess of 5 years is possible, and functional improvement, as measured by spirometry, diffusing capacity, and 6-minute walk distance, is immediate and sustained. The timing of referral becomes increasing crucial for patients with IPF as the waiting times for donor lungs lengthen because many cohorts of patients with IPF reported in the literature have median survivals that are similar to the current mean waiting times experienced on the transplant list. Even with existing waiting lists, nearly 33% of patients with IPF die on the waiting list, whereas another 10% are removed from the list, many because of deterioration to a state no longer considered amenable to transplantation. 21 International guidelines for referral for transplantation include "symptomatic, progressive disease with failure to improve or maintain on medical therapy." 6 Because it is estimated that 70% to 90% of patients with true IPF will fail to respond to medical treatment, 12,22,23 early referral for transplantation is urged when patients with IPF become symptomatic. Finally, the question of whether a single or bilateral transplant is most appropriate for IPF remains incompletely answered. The full answer to this question will likely require pooled data from the UNOS or the ISHLT to answer.
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Appendix: Discussion |
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TopAbstractIntroductionPatients and methods Results Discussion Appendix: Discussion References |
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Several important points are made. First, at the authors’ institution, transplantation for IPF can offer improved survival compared with the best current medical therapy, with a median survival of 5 years in the authors’ study compared with 10 months with current medical therapy at an acceptable operative risk of under 9%. These are outstanding data.
Second, there seems to be no advantage to bilateral over single lung transplantation for these patients, and this confirms the common practice of single lung transplantation for IPF around the world.
Our own experience, very briefly, in lung transplantation at the University of Minnesota over the past 10 years is slightly less encouraging than the data of the Washington University group. We have performed transplantation in 300 patients, of whom 27 had IPF. Similar to the authors’ experience, survival at 1 year was indistinguishable from that of patients undergoing transplantation for other diagnoses; however, at 2 years and beyond, survival for IPF was statistically less than that for other diagnoses, and 55% of our patients currently are dead. Median survival is only 34 months compared with the 5 years in your study.
Your report is very encouraging; however, survival in your own study for IPF is less at 1 year, and in the data from the ISHLT survival is less for patients with IPF, although not statistically so. A previous report from your own institution details the difficulties of transplantation in these patients. In light of this information, and also recent data from the registry of the ISHLT demonstrating that IPF is indeed a risk factor for 5-year mortality, I have two questions for you.
Given the acknowledged lower survival, at least in UNOS data and in data from our centers and others, can we justify giving these patients 90 days of extra advantage on the waiting list when they are placed on the list for transplantation? Is this truly in the best interest of achieving the best overall outcomes from a limited resource, namely scarce donor lungs?
Second, tracheostomy was required in roughly 15% of your patients. Can you comment on this and compare it with your incidence in patients without IPF? Also, could you tell us when to recommend tracheostomy after lung transplantation and describe your indications?
Again, I would like to congratulate you on a truly fine presentation and another important contribution from the Washington University group to the field of lung transplantation.
Dr Meyers. Thank you for your comments. With regard to the first question: Can we justify adding 90 days to the waiting time for patients with IPF in light of their lower survival overall? I would turn it around and answer that you might want to add more time because my impression is that the patients with pulmonary fibrosis who actually reach the end of the pipeline and are eligible for donor lung allocation are more depleted and are less fit candidates for transplantation than patients with other diagnoses who are far more stable on the waiting list. Therefore, I think that from my observations, justification is there for the additional 90 days, and one could even consider adding time to this group of patients who experience a more rapid decline than patients with chronic obstructive pulmonary disease.
With regard to the tracheostomy question, I do not have data for comparison on the rate of tracheostomy insertion in patients with IPF versus our other patients. Our general philosophy is that if patients cannot be extubated in the first 6 or 7 days after transplantation, a tracheostomy will assist with a more gradual and controlled wean from the ventilator. Therefore, usually, if we can extubate them within the first week, then they avoid a tracheostomy.
We have had some patients, particularly patients with IPF, who have deteriorated on the waiting list and who were not intubated by the time of listing but were intubated at the time of transplantation, and those patients are at more risk for long-term failure to wean and have a higher rate of tracheostomy.
Dr Scott J. Swanson (Boston, Mass). Given your results, can you tell us now when you consider a double lung transplant for IPF versus a single lung transplant?
Dr Meyers. In our program the consideration between a single lung transplant or a bilateral lung transplant goes beyond the recipient diagnosis. We have tried to cultivate a reputation in our Organ Procurement Organization of our willingness to accept lung grafts that might not be suitable for single lung transplantation but would be reasonable for a bilateral operation. In those situations we will often get a pair of lungs and perform a bilateral transplantation in patients who could accept either a single or a bilateral transplant. Basically, except in unusual circumstances, the type of operation is determined by the availability of the bilateral or single lung grafts.
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Acknowledgments |
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Footnotes |
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References |
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TopAbstractIntroductionPatients and methods Results Discussion Appendix: Discussion References |
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  E. S. Weiss, J. G. Allen, C. A. Merlo, J. V. Conte, and A. S. Shah Survival after single versus bilateral lung transplantation for high-risk patients with pulmonary fibrosis. Ann. Thorac. Surg., November 1, 2009; 88(5): 1616 - 1626. [Abstract] [Full Text] [PDF]
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