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Ann Thorac Surg 1998;65:227-234
© 1998 The Society of Thoracic Surgeons

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Original Articles: General Thoracic

Pulmonary Retransplantation: Predictors of Graft Function and Survival in 230 Patients

Departments of Surgery and Epidemiology and Biostatistics, the London Health Sciences Centre, the Robarts Research Institute and the University of Western Ontario, London, Ontario, Canada;
Departments of Surgery and Epidemiology and Biostatistics, the London Health Sciences Centre, the Robarts Research Institute and the University of Western Ontario, Harefield, England, United Kingdom;
Departments of Surgery and Epidemiology and Biostatistics, the London Health Sciences Centre, the Robarts Research Institute and the University of Western Ontario, Vienna, Austria;
Departments of Surgery and Epidemiology and Biostatistics, the London Health Sciences Centre, the Robarts Research Institute and the University of Western Ontario, Hannover and Homburg, Germany;
Departments of Surgery and Epidemiology and Biostatistics, the London Health Sciences Centre, the Robarts Research Institute and the University of Western Ontario, Paris, France;
Departments of Surgery and Epidemiology and Biostatistics, the London Health Sciences Centre, the Robarts Research Institute and the University of Western Ontario, Pittsburgh, Pennsylvania, USA;
Departments of Surgery and Epidemiology and Biostatistics, the London Health Sciences Centre, the Robarts Research Institute and the University of Western Ontario, St. Louis, Missouri, and 47 participating centers in the Pulmonary Retransplant Registry, USA

Accepted for publication September 25, 1997.

Dr Novick, Department of Surgery, London Health Sciences Centre, PO Box 5339, London, Ont, Canada N6A 5A5, (e-mail: rjnovick@julian.uwo.ca).

	Abstract

Top Footnotes Abstract Introduction Patients and Methods Results Comment Acknowledgments Appendix 1 References

 
Background. Despite improving results in lung transplantation, a significant number of grafts fail early or late postoperatively. The pulmonary retransplant registry was founded in 1991 to determine the predictors of outcome after retransplantation. We hypothesized that ambulatory status of the recipient and center retransplant volume, which had been previously shown to predict survival after retransplantation, would also be associated with improved graft function postoperatively.

Methods. Two hundred thirty patients underwent retransplantation in 47 centers from 1985 to 1996. Logistic regression methods were used to determine variables associated with, and predictive of, survival and lung function after retransplantation.

Results. Kaplan-Meier survival was 47% ± 3%, 40% ± 3%, and 33% ± 4% at 1, 2, and 3 years, respectively. On multivariable analysis, the predictors of survival included ambulatory status or lack of ventilator support preoperatively (p = 0.005; odds ratio, 1.62; 95% confidence interval, 1.15 to 2.27), followed by retransplantation after 1991 (p = 0.048; odds ratio, 1.41; 95% confidence interval, 1.003 to 1.99). Ambulatory, nonventilated patients undergoing retransplantation after 1991 had a 1-year survival of 64% ± 5% versus 33% ± 4% for nonambulatory, ventilated recipients. Eighty-one percent, 70%, 62%, and 56% of survivors were free of bronchiolitis obliterans syndrome at 1, 2, 3, and 4 years after retransplantation, respectively. Factors associated with freedom from stage 3 (severe) bronchiolitis obliterans syndrome at 2 years after retransplantation included an interval between transplants greater than 2 years (p = 0.01), the lack of ventilatory support before retransplantation (p = 0.03), increasing retransplant experience within each center (fifth and higher retransplant patient, p = 0.04), and total center volume of five or more retransplant operations (p = 0.05).

Conclusions. Nonambulatory, ventilated patients should not be considered for retransplantation with the same priority as other candidates. The best intermediate-term functional results occurred in more experienced centers, in nonventilated patients, and in patients undergoing retransplantation more than 2 years after their first transplant. In view of the scarcity of lung donors, patient selection for retransplantation should remain strict and should be guided by the outcome data reviewed in this article.

	Introduction

Top Footnotes Abstract Introduction Patients and Methods Results Comment Acknowledgments Appendix 1 References

 
Although the results of lung transplantation are improving [1][2], a significant number of grafts fail because of severe early graft dysfunction [3], intractable airway healing problems [4], or, especially, obliterative bronchiolitis (OB) [5][6]. In recent years, an increasing number of pulmonary retransplantations have been performed because of acute or chronic graft failure [7][8][9][10][11][12][13][14]. The results and predictors of outcome after retransplantation have been determined in a series of publications from the international pulmonary retransplant registry [10][11][12][13][14]. In 1996 a multivariable analysis of registry data revealed that the preoperative ambulatory status of retransplant recipients predicted 3-month survival and the total center volume of retransplant procedures predicted 2-year survival postoperatively [14]. In the past year 70 new patients were recruited to the registry and the number of intermediate-term survivors of retransplantation increased substantially. New analyses were therefore planned to determine the predictors of graft function in the intermediate-term after retransplantation, in addition to survival. We hypothesized that the ambulatory status of the recipient and center experience with retransplantation would be associated not only with survival but also with graft function at 2 years after retransplantation.

	Patients and Methods

Top Footnotes Abstract Introduction Patients and Methods Results Comment Acknowledgments Appendix 1 References

 
Patient Population
Since mid-1991 patients undergoing retransplantation have been recruited to the retransplant registry by means of a standardized study questionnaire. Patients who had undergone repeat heart-lung transplantation or a heart-lung transplantation after a previous pulmonary transplantation have been excluded, in view of the possible confounding effect of a cardiac graft [10]. All patients have been followed up prospectively, with yearly updates of clinical status and pulmonary function. For the purposes of this report, the status of all study patients was determined in October 1996. Patients who underwent retransplantation for any indication were included in the study cohort.

Variables Studied
Recipient variables included age, sex, original diagnosis before the first transplant procedure, indication for retransplantation, ambulatory status of the recipient before retransplantation, requirement for ventilator support, ABO blood group, cytomegalovirus (CMV) status, official waiting time for retransplantation, and interval between transplant procedures. An ambulatory recipient was defined as a patient who was able to walk at least 50 m, with or without assistance, immediately before retransplantation. In view of the close interaction between ambulatory status and the need for ventilator support before retransplantation, composite variables of "both ambulatory and not ventilator dependent" and "either ambulatory or not ventilator dependent" were also studied. Donor and operative variables included year of retransplantation, retransplant center, type of retransplant procedure, total center volume and individual center experience with retransplantation, donor ABO blood group, and CMV status.

Statistical Analysis of Survival
Data were incorporated into the pulmonary retransplant database with the use of the FoxPro database management system (Microsoft Corporation, Redmond, WA) on a Pentium/100 MHz computer. Statistical analysis was performed with the SAS statistical package, version 6.11 (SAS Institute Inc, Cary, NC). All data were expressed as mean ± standard error of the mean. Survival was calculated using the Kaplan-Meier method [15] and survival curves were contrasted using the log-rank test. Cox regression methods [16] were then used to determine which variables were associated with survival after retransplantation. Variables exhibiting a p value less than 0.10 on univariable analysis were considered for entry into a multivariable model to determine the independent predictors of survival after retransplantation. Furthermore, the odds ratio of each variable was expressed as a comparison of survival between groups, with a value of 1.0 indicating no survival difference, a value greater than 1.0 indicating increased survival, and a value less than 1.0 indicating decreased survival after retransplantation.

Because the data in this study were collected from 47 North American, European, and Australian centers, there was a possibility that these data might be clustered by center. We therefore adjusted for between-center effects, so that our analyses would more clearly show significant recipient, donor, and operative characteristics [14]. A variable for center was therefore created in which centers with five or more retransplantations were assigned unique levels, whereas centers with fewer than five retransplantations were grouped together as a single level. This variable for center, in addition to the recipient, donor, and operative characteristics, was included in the Cox regression analyses to adjust for possible between-center differences.

Statistical Analysis of Graft Function
A major focus of this study was postoperative graft function in the intermediate term and the recurrence of bronchiolitis obliterans syndrome (BOS) after retransplantation. Complete pulmonary function test data were therefore obtained prospectively from every survivor of retransplantation at 12-month intervals. Bronchiolitis obliterans syndrome stages were assigned according to previously published criteria on the basis of postoperative values of forced expiratory volume in one second (FEV₁) [17]. The changes in absolute FEV₁ values at 1, 2, and 3 years after retransplantation were calculated for the entire study cohort and for patients who underwent retransplantation because of obliterative bronchiolitis versus those who underwent retransplantation because of other conditions. Unpaired, two-tailed t tests were employed to compare FEV₁ values between patient groups. In addition, logistic regression methods [16] were used to determine the factors associated with freedom from BOS (ie, BOS stage 0) and the absence of severe BOS (ie, BOS stage 3) 2 years after retransplantation. For all statistical analyses, a p value less than 0.05 was considered significant.

	Results

Top Footnotes Abstract Introduction Patients and Methods Results Comment Acknowledgments Appendix 1 References

 
Forty-seven lung transplantation programs participated in the study, including 26 from North America, 20 from Europe, and 1 from Australia (see Appendix 1). The study cohort comprised 230 retransplant recipients, including 130 female and 100 male patients, with a median age of 41 years (range, 6 months to 62 years). Before undergoing the first transplantation, 31% of patients had emphysema, 22% primary pulmonary hypertension or Eisenmenger’s Syndrome, 19% cystic fibrosis, 17% restrictive lung disease, and 11% miscellaneous conditions. The indications for retransplantation (and median interval between transplant procedures) included OB in 146 patients (639 days), acute graft failure in 52 (15 days), intractable airway complications in 14 (119 days), histologically confirmed severe acute rejection in 9 (13 days), and miscellaneous conditions in 9 (243 days). Forty-six patients (20%) underwent ipsilateral single-lung retransplantation, 55 patients (24%) contralateral single-lung retransplantation, 44 patients (19%) repeat double-lung transplantation, 30 patients (13%) double-lung transplantation after a previous single-lung transplantation, and 55 patients (24%) single-lung transplantation after a previous double-lung or heart-lung transplantation. Patient follow-up was 100% complete, with current survival and pulmonary function test data available for every patient.

Survival
Of the 230 retransplant recipients, 146 have died and 84 are still living. Kaplan-Meier survival was 47% ± 3% at 1 year (versus 35% ± 5% 4 years ago), 40% ± 3% at 2 years, and 33% ± 4% at 3 years. The median follow-up in current survivors is 26 months (mean, 30.5 ± 2.2 months; range, 1 to 79 months). Ninety-five patients have reached the first anniversary, 59 the second anniversary, 37 the third anniversary, 21 the fourth anniversary, and 11 the fifth anniversary of retransplantation.

Association of Recipient, Donor, and Operative Variables With Survival
Variables that were significantly associated with survival on univariable analysis are shown in Table 1. Survival was not significantly different according to the age, sex, original diagnosis, official waiting time, or CMV status of the recipient. The actuarial survival of patients undergoing retransplantation because of OB was significantly greater than in patients undergoing retransplantation because of other indications when a center-adjusted analysis was performed (Table 1), but not when the data were unadjusted for a possible center effect (Table 1; Fig 1). These data are provocative, as patients surviving a retransplantation that was performed because of OB exhibited more pulmonary dysfunction postoperatively in a previous study from the registry than patients surviving a retransplantation performed because of acute graft failure or an intractable airway complication [14].

View larger version (13K): [in this window] [in a new window]   Actuarial survival of patients undergoing retransplantation because of obliterative bronchiolitis versus those undergoing retransplantation because of other indications (log-rank p value = 0.07).

View larger version (13K): [in this window] [in a new window]   Actuarial survival according to the interval between transplantation procedures (log-rank p value = 0.002).

View larger version (14K): [in this window] [in a new window]   Actuarial survival according to the requirement for ventilator support before retransplantation (log-rank p value = 0.002).

View larger version (18K): [in this window] [in a new window]   Actuarial survival according to the recipient’s ambulatory status and requirement for ventilator support preoperatively (log-rank p value = 0.003).

View larger version (19K): [in this window] [in a new window]   Actuarial survival according to the year of retransplantation and the recipient’s requirement for ventilator support preoperatively (log-rank p value = 0.001).

Functional Status After Retransplantation
After a median follow-up of 26 months, 58% of patients were in New York Heart Association functional class I, 28% in class II, 11% in class III, and 3% in class IV. Seventy-seven of the 84 survivors did not require supplemental oxygen whereas 7 patients were oxygen-dependent.

Pulmonary Function and Bronchiolitis Obliterans Syndrome Stages in Retransplant Survivors
Complete, up-to-date FEV₁ data were available from every retransplant patient who survived at least 1 year after operation. Fig 6 shows the prevalence of BOS stages in these patients at 1, 3, and 5 years after retransplantation. Eighty-one percent of patients were free of BOS (stages 1 to 3) at 1 year, 62% at 3 years, and 50% at 5 years. The prevalence of stage 3 (severe) BOS was 12% at 1 year, 24% at 3 years, and 27% at 5 years, which is similar to that reported after primary lung transplantation [6][9][18].

View larger version (14K): [in this window] [in a new window]   Prevalence of stages 0, 1, 2, and 3 bronchiolitis obliterans syndrome (BOS) at 1, 3, and 5 years after retransplantation.

View larger version (12K): [in this window] [in a new window]   Forced expiratory volume in 1 second (FEV1) values in 3-year survivors who underwent retransplantation because of obliterative bronchiolitis (OB) versus non-OB conditions (see text for p values). (SEM = standard error of the mean.)

	Comment

Top Footnotes Abstract Introduction Patients and Methods Results Comment Acknowledgments Appendix 1 References

The practice of retransplantation has raised ethical dilemmas, which reflect the inalienable conflict between rights-based moral theories and utilitarianism [19][20][21]. Some authors have gone so far as to advocate an outright ban on retransplantation [19], whereas others believe that waiting lists should be altered so that primary transplant candidates have a better chance of receiving organs than retransplant candidates [20]. Our current study indicated that careful selection of pulmonary retransplant candidates can result in a 1-year survival that is nearly identical to that of primary lung transplant recipients (Table 3). Furthermore, this study demonstrated that BOS does not recur in a more accelerated manner after retransplantation than after first-time lung transplantation. The argument that pulmonary retransplantation should be banned because it invariably results in lower survival rates or worse graft function can therefore not be supported by the available evidence. We believe that lung retransplantation should be conducted only by programs that are accountable and willing to share their results with the international lung transplant community.

Compared with previous reports, there were several additional findings in this study that resulted from increased patient accrual to the retransplant registry and from the increased survival of previously registered patients. In addition, by adjusting for center effects, variability in our survival model was reduced, thus yielding higher odds ratios (and lower p values) for the other prognostic factors. Although a long interval between transplant procedures and the absence of ventilator support before retransplantation were not significant predictors of survival in our previous reports [13][14], they were significantly associated with survival in the current study. The interval between transplant procedures did not, however, enter the multivariable models predicting survival, probably because of the confounding effect of other variables such as ambulatory status and ventilator support. The group of patients with the strongest survival advantage on multivariable analysis were those who were either ambulatory or not on the ventilator before retransplantation and patients undergoing retransplantation after 1991 (Table 2). The interaction between ambulatory status and ventilator support was strong, and the favorable survival of patients who were not ambulatory but free of ventilator support was noteworthy (Fig 4). Interestingly, our initial hypothesis was only partially validated, in that the ambulatory status of retransplant candidates was not significantly associated with graft function in the intermediate term postoperatively. On the other hand, center experience with retransplantation, in concert with an interval between transplants of greater than 2 years and the lack of ventilatory support before retransplantation, was an important variable correlating with BOS stage postoperatively.

The possible limitations of studies involving multiinstitutional databases have been recently reviewed [22]. In summary, the caliber of all multiinstitutional studies is heavily dependent on the quality of the data and the completeness of follow-up. Furthermore, variables used in statistical analyses in multiinstitutional studies must be well defined a priori and the definition should not differ among contributing institutions. In this study, although the practice of primary and repeat lung transplantation differed among contributing programs, the data were of high quality, variables were clearly defined a priori, and follow-up was 100% complete. Nonetheless, the odds ratios depicted in Table 1Table 2 Table 4 were relatively low (1.5 to 2.5) and the 95% confidence intervals for some variables were relatively wide, indicating suboptimal precision despite the low p values. It is likely that more precise multivariable models predicting survival and graft function after pulmonary retransplantation could be obtained if additional relevant variables were analyzed. Data on the immunosuppressive protocol employed in each patient after retransplantation are therefore currently being entered prospectively into the pulmonary retransplant database. We anticipate that these additional data, further patient accrual to the retransplant registry, and an increasing duration of follow-up of retransplant recipients will increase our statistical power to determine the independent predictors of long-term survival and lung graft function after retransplantation. In the final analysis, however, predictive data from multivariable analyses must be validated prospectively before these models can be definitively relied upon to optimize clinical decision making in retransplant candidates [23].

In summary, although the early results of pulmonary retransplantation are improving, patient selection should remain strict because of the scarcity of lung donors. Nonambulatory, ventilated patients should not be considered for retransplantation with the same priority as other candidates. The strongest predictors of survival were ambulatory status or lack of ventilator support preoperatively, followed by retransplantation after 1991. The most favorable intermediate-term functional results occurred in more experienced centers, in nonventilated patients, and in patients undergoing retransplantation more than 2 years after their first transplant. Data on immunosuppression protocols after retransplantation are being prospectively entered into the pulmonary retransplant database to determine the ability of these agents to prevent progressive graft dysfunction after pulmonary retransplantation.

	Acknowledgments

Top Footnotes Abstract Introduction Patients and Methods Results Comment Acknowledgments Appendix 1 References

 
Supported by grants from the Multi-Organ Transplant Service, London Health Sciences Centre and Sandoz Canada, Inc. We thank the contributing thoracic surgeons, pulmonary medicine physicians, and recipient coordinators who have participated in the pulmonary retransplant registry. We also acknowledge the assistance of Heather Motloch in manuscript preparation and of Theresa Novick, MSc, in data collection and analysis.

	Footnotes

Top Footnotes Abstract Introduction Patients and Methods Results Comment Acknowledgments Appendix 1 References

 
See Appendix 1 for a list of the 47 participating centers.

	Appendix 1

Top Footnotes Abstract Introduction Patients and Methods Results Comment Acknowledgments Appendix 1 References

 
List of Participating Centers in the Pulmonary Retransplant Registry
Australia

1. Alfred Hospital, Melbourne
   

Canada

1. Centre for Health Sciences, Winnipeg, Manitoba
   
2. Montreal General Hospital, Montreal, Quebec
   
3. London Health Sciences Centre, London, Ontario
   
4. Toronto Hospital, Toronto, Ontario
   
5. Vancouver General Hospital, Vancouver, British Columbia
   

Europe

1. Allegemeine Krankenhaus, Vienna, Austria
   
2. Hôpital Erasme, Brussels, Belgium
   
3. Rigshospitalet, Copenhagen, Denmark
   
4. Freeman Hospital, Newcastle-upon-Tyne, England
   
5. Harefield Hospital, Harefield, England
   
6. Papworth Hospital, Cambridge, England
   
7. Wythenshawe Hospital, Manchester, England
   
8. Helsinki University Central Hospital, Helsinki, Finland
   
9. Hôpital Beaujon, Clichy, France
   
10. Centre Hospitalier Universitaire de Grenoble, Grenoble, France
    
11. Hôpital d’Enfants de la Timone, Marseille, France
    
12. Hôpital Marie Lannelongue, Paris, France
    
13. Hôpital Xavier-Arnozan, Pessac, France
    
14. Centre Medico-Chirurgical Foch, Suresnes, France
    
15. Medizinische Hochschule Hannover, Hannover, Germany
    
16. Klinikum Großhadern, Munich, Germany
    
17. Academisch Ziekenhuis Groningen, Groningen, Holland
    
18. Ospedale San Giovanni Battista, Torino, Italy
    
19. Rikshospitalet, Oslo, Norway
    
20. Universitätsspital Zürich, Zürich, Switzerland
    

United States

1. Cedars-Sinai Medical Center, Los Angeles, California
   
2. Stanford University Medical Center, Stanford, California
   
3. Loyola University Medical Center, Maywood, Illinois
   
4. University of Iowa Hospital, Iowa City, Iowa
   
5. University of Kentucky, Chandler Medical Center, Lexington, Kentucky
   
6. Ochsner Clinic, New Orleans, Louisiana
   
7. Brigham and Women’s Hospital, Boston, Massachusetts
   
8. University of Michigan Medical Center, Ann Arbor, Michigan
   
9. University of Minnesota Health Center, Minneapolis, Minnesota
   
10. St. Louis Children’s Hospital, St. Louis, Missouri
    
11. Washington University, Barnes-Jewish Hospital, St. Louis, Missouri
    
12. Duke University Medical Center, Durham, North Carolina
    
13. University of North Carolina Medical Center, Chapel Hill, North Carolina
    
14. University of Pennsylvania Hospital, Philadelphia, Pennsylvania
    
15. University of Pittsburgh, Presbyterian Hospital, Pittsburgh, Pennsylvania
    
16. Vanderbilt University Medical Center, Nashville, Tennessee
    
17. Baylor-Methodist Hospital, Houston, Texas
    
18. University of Texas Medical Center, San Antonio, Texas
    
19. University of Virginia Health Sciences Center, Charlottesville, Virginia
    
20. University of Washington School of Medicine, Seattle, Washington
    
21. University of Wisconsin Medical Center, Madison, Wisconsin
    

	References

Top Footnotes Abstract Introduction Patients and Methods Results Comment Acknowledgments Appendix 1 References

 

1. Hosenpud JD, Novick RJ, Bennett LE, Keck BM, Fiol B, Daily OP The registry of the International Society for Heart and Lung Transplantation: 13th official report—1996. J Heart Lung Transplant 1996;15:655-674.[Medline]
2. Cooper JD, Patterson GA, Trulock EP, Washington University Lung Transplant Group. Results of single and bilateral lung transplantation in 131 consecutive recipients. J Thorac Cardiovasc Surg 1994;107:460-471.[Abstract/Free Full Text]
3. Novick RJ, Gehman KE, Ali IS, Lee J Lung preservation: the importance of endothelial and alveolar type II cell integrity. Ann Thorac Surg 1996;62:302-314.[Abstract/Free Full Text]
4. Date H, Trulock EP, Arcidi JM, Sundareasan S, Cooper JD, Patterson GA Improved airway healing after lung transplantation: an analysis of 348 bronchial anastomoses. J Thorac Cardiovasc Surg 1995;110:1424-1433.[Abstract/Free Full Text]
5. Sundaresan S, Trulock EP, Mohanakumar T, Cooper JD, Patterson GA Prevalence and outcome of bronchiolitis obliterans syndrome after lung transplantation. Ann Thorac Surg 1995;60:1341-1347.[Abstract/Free Full Text]
6. Reichenspurner H, Girgis RE, Robbins RC, et al. Obliterative bronchiolitis after lung and heart-lung transplantation. Ann Thorac Surg 1995;60:1845-1853.[Abstract/Free Full Text]
7. Fournier M, Sleiman C, Mal H, et al. Single-lung retransplantation for late graft failure. Eur Respir J 1993;6:1202-1206.[Abstract]
8. Adams DH, Cochrane AD, Khaghani A, Smith JD, Yacoub MH Retransplantation in heart-lung recipients with obliterative bronchiolitis. J Thorac Cardiovasc Surg 1994;107:450-459.[Abstract/Free Full Text]
9. Schäfers HJ, Hausen B, Wahlers T, Fieguth HG, Jurmann M, Borst HG Retransplantation of the lung: a single center experience. Eur J Cardiothorac Surg 1995;9:291-296.[Abstract]
10. Novick RJ, Kaye MP, Patterson GA, et al. Redo lung transplantation: a North American–European experience. J Heart Lung Transplant 1993;12:5-16.[Medline]
11. Novick RJ, Andréassian B, Schäfers HJ, et al. Pulmonary retransplantation for obliterative bronchiolitis: intermediate-term results of a North American–European series. J Thorac Cardiovasc Surg 1994;107:755-763.[Abstract/Free Full Text]
12. Novick RJ, Schäfers HJ, Stitt L, et al. Seventy-two pulmonary retransplantations for obliterative bronchiolitis: predictors of survival. Ann Thorac Surg 1995;60:111-116.[Abstract/Free Full Text]
13. Novick RJ, Schäfers HJ, Stitt L, et al. Recurrence of obliterative bronchiolitis and determinants of outcome in 139 pulmonary retransplant recipients. J Thorac Cardiovasc Surg 1995;110:1402-1414.[Abstract/Free Full Text]
14. Novick RJ, Stitt L, Schäfers HJ, et al. Pulmonary retransplantation: does the indication for operation influence postoperative lung function?. J Thorac Cardiovasc Surg 1996;112:1504-1514.[Abstract/Free Full Text]
15. Harris EK, Albert A Survivorship analysis for clinical studies. New York: Marcel Dekker, 1991:12-15.
16. Hosmer DW, Lemeshow S Applied logistic regression. New York: John Wiley & Sons, 1989:1-134.
17. Cooper JD, Billingham M, Egan T, et al. A working formulation for the standardization of nomenclature and for clinical staging of chronic dysfunction in lung allografts. J Heart Lung Transplant 1993;12:713-716.[Medline]
18. Egan TM, Detterbeck FC, Mill MR, et al. Improved results of lung transplantation for patients with cystic fibrosis. J Thorac Cardiovasc Surg 1995;109:224-235.[Abstract/Free Full Text]
19. Collins EG, Mozdzierz GJ Cardiac retransplantation: determining limits. Heart Lung 1993;22:206-212.[Medline]
20. Ubel PA, Arnold RM, Caplan AL Rationing failure: the ethical lessons of the retransplantation of scarce vital organs. JAMA 1993;270:2469-2474.[Abstract/Free Full Text]
21. Mentzer SJ, Reilly JJ, Caplan AL, Sugarbaker DJ Ethical considerations in lung retransplantation. J Heart Lung Transplant 1994;13:56-58.[Medline]
22. Huston P, Naylor CD Health services research: reporting on studies using secondary data sources. Canad Med Assoc J 1996;155:1697-1702.[Medline]
23. Thorogood J, Houwelingen JC, Persijn GG, Zantvoort FA, Schreuder GMTh, van Rood JJ Prognostic indices to predict survival of first and second renal allografts. Transplantation 1991;52:831-836.[Medline]

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				R. M. Kotloff Lung Retransplantation: All for One or One for All? Chest, June 1, 2003; 123(6): 1781 - 1782. [Full Text] [PDF]

				O. Brugiere, G. Thabut, Y. Castier, H. Mal, G. Dauriat, A. Marceau, and G. Leseche Lung Retransplantation for Bronchiolitis Obliterans Syndrome: Long-term Follow-up in a Series of 15 Recipients Chest, June 1, 2003; 123(6): 1832 - 1837. [Abstract] [Full Text] [PDF]

				L. B. Balsam, D. D. Yuh, R. C. Robbins, and B. A. Reitz Heart-Lung and Lung Transplantation Card. Surg. Adult, January 1, 2003; 2(2003): 1461 - 1490. [Full Text]

				M. Estenne and M. I. Hertz Bronchiolitis Obliterans after Human Lung Transplantation Am. J. Respir. Crit. Care Med., August 15, 2002; 166(4): 440 - 444. [Full Text] [PDF]

				S. M. Arcasoy and R. M. Kotloff Lung Transplantation N. Engl. J. Med., April 8, 1999; 340(14): 1081 - 1091. [Full Text] [PDF]

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