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(Chest. 2005;127:161-165.)
© 2005 American College of Chest Physicians

Impact of Primary Graft Failure on Outcomes Following Lung Transplantation*

Jason D. Christie, MD, MS, FCCP; Jeffrey S. Sager, MD; Stephen E. Kimmel, MD, MS; Vivek N. Ahya, MD; Christina Gaughan, MS; Nancy P. Blumenthal, MSN, CRNP and Robert M. Kotloff, MD, FCCP

* From the Divisions of Pulmonary and Critical Care Medicine (Drs. Christie, Sager, Ahya, and Kotloff, Ms. Gaughan, and Ms. Blumenthal) and Cardiovascular Medicine (Dr. Kimmel), Department of Medicine, University of Pennsylvania School of Medicine, Philadelphia, PA.

Correspondence to: Jason D. Christie, MD, MS, FCCP, Assistant Professor of Medicine and Epidemiology, Division of Pulmonary, Allergy and Critical Care Medicine, Center for Clinical Epidemiology and Biostatistics, University of Pennsylvania School of Medicine, 423 Guardian Dr, 719 Blockley Hall, Philadelphia, PA 19104; e-mail: jchristi{at}cceb.med.upenn.edu


   Abstract
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 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Study objectives: Primary graft failure (PGF) is a severe acute lung injury syndrome that occurs following lung transplantation. We compared the clinical outcomes of patients who developed PGF with those who did not.

Methods: We conducted a retrospective cohort study including 255 consecutive lung transplant procedures. PGF was defined as (1) diffuse alveolar opacities developing within 72 h of transplantation, (2) an arterial partial pressure of oxygen/fraction of inspired oxygen (PaO2/FIO2) ratio of < 200 beyond 48 h postoperatively, and (3) no other secondary cause of graft dysfunction. PGF was tested for acceptance with 30-day and all-cause hospital mortality rates, overall survival, hospital length of stay (HLOS), duration of mechanical ventilation, and best 6-min walk test (6MWT) distance achieved within 12 months.

Setting: Academic medical center.

Results: The overall incidence of PGF was 11.8% (95% confidence interval [CI], 7.9 to 15.9%). The all-cause mortality rate at 30 days was 63.3% in patients with PGF and 8.8% in patients without PGF (relative risk [RR], 7.15; 95% CI, 4.34 to 11.80%; p < 0.001). A total of 73.3% of patients with PGF died during hospitalization vs 14.2% of patients without PGF (RR, 5.18%; 95% CI, 3.51 to 7.63; p < 0.001). The median HLOS in 30-day survivors was 47 days in patients with PGF vs 15 days in those without PGF (p < 0.001), and the mean duration of mechanical ventilation was 15 days in patients with PGF vs 1 day in those without PGF (p < 0.001). By 12 months, a total of 28.5% of survivors with PGF achieved a normal age-appropriate 6MWT distance vs 71.4% of survivors without PGF at 12 months (p = 0.014). The median best 6MWT distance achieved within the first 12 months was 1,196 feet in patients with PGF vs 1,546 feet in those without PGF (p = 0.009).

Conclusions: PGF has a significant impact on mortality, HLOS, and duration of mechanical ventilation following lung transplantation. Survivors of PGF have a protracted recovery with impaired physical function up to 1 year following transplantation.

Key Words: acute lung injury • complications • lung transplantation • outcomes • reperfusion injury


   Introduction
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 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
Primary graft failure (PGF) represents a severe form of ischemia-reperfusion lung injury to the lung allograft occurring in the early posttransplant period.12 The radiographic and histologic features are most similar to those of ARDS.134 The incidence of PGF has been reported to be in the range of 12 to 25%, and it has been reported as the leading cause of early death following transplantation.12567 However, some studies8 have suggested that severe ischemia-reperfusion injury does not adversely impact mortality.

Outside the lung transplant population, survivors of severe acute lung injury have impaired functional status and quality of life extending far beyond the initial hospitalization.91011 However, the longer term functional outcomes in survivors of PGF have not been systematically studied. The purpose of this study was to test the association of PGF with both short-term and long-term clinical outcomes following lung transplantation.


   Materials and Methods
TOP
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
Study Population
A retrospective cohort study was performed including all 255 consecutive lung transplant procedures performed at our institution between October 1991 and July 2000. One heart-lung transplant and two lung-liver transplants were excluded as it was thought that they would not be representative of outcomes in the population at whole. The follow-up period for survival analysis and clinical outcomes extended to July 2002. We chose this time frame to ensure at least 2 years of follow-up time for all subjects. In addition, 250 patients would provide 80% power at an {alpha} level of 0.05 to detect a 5% absolute difference in 30-day mortality above an estimated 30-day mortality rate of 8% in the non-PGF group.

Standard Transplant Protocol
Donor selection, graft procurement, immunologic evaluation, surgical technique, postoperative management, and immunosuppression therapy all proceeded according to our standard transplant protocol, which has been previously published.17 Of note, we used antilymphocyte induction therapy in all but 40 of our patients (sequentially between patient 60 and 100) during the time period of study. Other immunosuppression therapy consisted of treatment with cyclosporine, azathioprine, and prednisone, and this was the same in all subjects over the period of the study.

Definition of PGF
The definition of PGF represents an adaptation of the American European Consensus Conference definition of ARDS.12 Although there is a spectrum of reperfusion injury following lung transplantation,4813 we chose criteria that select the patients with the most severe form of clinical graft dysfunction, which is most similar to ARDS. To be defined as having PGF, study subjects had to meet all of the following criteria: (1) the presence within 72 h of transplantation of a diffuse alveolar infiltrate involving the lung allograft and, in the case of single-lung transplant, sparing the native lung; (2) a ratio of arterial partial pressure of oxygen/fraction of inspired oxygen (PaO2/FIO2) of < 200 persisting beyond the initial 48 h postoperatively; (3) no other secondary cause of graft dysfunction identified, including cardiogenic pulmonary edema (defined as a pulmonary artery occlusion pressure of > 18 cm or the resolution of infiltrates with effective diuresis), pathologic evidence of rejection, pneumonia (as evidenced by the presence of fever, leukocytosis, and purulent secretions with positive cultures on bronchoscopy during the first 3 postoperative days), and pulmonary venous outflow obstruction by clot or kinking (as demonstrated by transesophageal echocardiogram or direct inspection on surgical reexploration or postmortem examination); and, (4) in the event of death prior to day 3, the patient must fulfill the above criteria at the time of death and must demonstrate diffuse alveolar damage as the predominant process on histologic examination of the lung (available on all patients with death within 72 h).

Definition of Outcomes
Study outcomes were all-cause mortality rate at day 30 following transplantation, all-cause hospital mortality rate, overall survival rate, hospital length of stay (HLOS), duration of mechanical ventilation, number of ventilator-free days during the first 30 postoperative days,14 and 6-min walk test (6MWT) distance within 12 months following transplantation. Due to biases potentially introduced by early death in the postoperative period, HLOS and duration of mechanical ventilation were assessed only among 30-day survivors. To be considered "extubated," subjects needed to be free of mechanical ventilation for 48 h. Reintubation following this 48-h period was not considered part of the duration of mechanical ventilation attributable to PGF, because of the likelihood of other contributing causes. To further evaluate the contribution of PGF to the length of intubation when accounting for the effects of early deaths and reintubation, we calculated the number of 30-day ventilator-free days in all patients.14

The 6MWT was performed in a standard fashion.15 We compared the best distance achieved within the first 12 months of the date of transplantation as a measure of peak function achieved during this time period. A "normal" 6MWT distance was defined as the minimum age-appropriate distance using standard criteria for population norms.15 Subjects who were alive but unable to perform the test due to physical disability were scored as a zero value. Subjects who were dead were excluded from analysis.

Data Collection and Management
All of the data prior to July 2000 were collected from a review of preexisting medical records. After this time point, the follow-up mortality and 6MWT data were recorded prospectively as part of a prospective cohort study. Data extraction was conducted separately and by persons who were blinded to knowledge of PGF.

Data on mortality outcomes were complete in all subjects. No patients were lost to follow-up during the period of the cohort study. 6MWT data were complete in the survivors who had PGF. However, 6MWT data were not uniformly complete in the group of survivors without PGF. Missing data were mostly due to death within 1 year of lung transplantation and the inability to perform the test due to disability. Of the 214 subjects who were alive at 30 days following transplantation, 194 had performed a 6MWT within the first year. Of the 20 remaining subjects, 16 died prior to completing a test, 2 were alive but too disabled to perform the test, and 1 was performing a home exercise regimen that equated to a normal 6MWT distance. Only one patient was lost to follow-up during the period of observation.

Statistical Analysis
Relative risks (RRs) with 95% confidence intervals (CIs) were calculated as the incidence of outcome (such as 30-day mortality rate) in patients with PGF divided by the incidence of outcome in patients without PGF. Due to the expected skewed distribution of HLOS, duration of mechanical ventilation, and 6MWT distance, these continuous variables were compared using nonparametric methods, using the rank sum test. To assess the potential confounding effects of variables on the relationship of PGF with mortality, we used multivariable logistic regression. Given the small number of subjects with PGF (30 subjects), we only included one potential confounder in the model at a time. Potential confounding variables included the following: recipient age, race, and diagnosis; donor age, race, and gender; type of transplant; and ischemic time. In addition, we adjusted for the potential effects of changes in therapy over time by including the calendar year of the transplant in the model. Overall survival between subjects with PGF and those without was compared using the Kaplan-Meier method and log-rank test.16 All statistical comparisons were performed using a statistical software package (STATA, version 8.0; STATA Corp; College Station, TX). This research protocol was approved by the Institutional Review Board of the Office of Regulatory Affairs at the University of Pennsylvania.


   Results
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 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
Thirty of the 252 patients met the criteria for PGF (incidence, 0.118; 95% CI, 0.079 to 0.159). The all-cause mortality rate at 30 days was 63.3% in patients with PGF and 8.8% in patients without PGF (RR, 7.15; 95% CI, 4.34 to 11.80; p < 0.001). Likewise, there was a significant difference in the hospital mortality rates between the groups, with 73.3% of patients with PGF dying during hospitalization and 14.2% of patients without PGF dying (RR, 5.18; 95% CI, 3.51 to 7.63; p < 0.001). Patients with PGF accounted for 48.7% of the total number of deaths at 30 days, and 40.7% of hospital deaths in the entire cohort. The all-cause mortality rate at 1 year was 70.0% in patients with PGF vs 24.7% in patients without PGF (RR, 2.83; 95% CI, 2.04 to 3.91; p < 0.001), indicating that the majority of the mortality in PGF patients occurred in the first 30 days. Among patients with PGF, the all-cause mortality rate at 1 year (70.0%) was lower than the in-hospital mortality rate (73.3%), as one patient remained alive in the hospital for > 1 year prior to expiring. The results of these mortality measures are summarized in Figure 1 . In the multivariable analysis, none of the variables diminished the point estimate of the odds ratio (OR) when added individually to a logistic regression equation containing PGF and any of the three dichotomous mortality measures. The overall survival rate was significantly worse in patients with PGF (hazard ratio, 3.97; 95% CI, 2.54 to 6.21; p < 0.001). The Kaplan-Meier curves for this comparison are illustrated in Figure 2 (p < 0.001 [log-rank test]).



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  		Figure 1. The mortality rate at 30 days, at hospital discharge, and at 1 year following transplantation in patients with PGF and those without PGF. For each comparison, the number of subjects with PGF was 30 and the number without PGF was 222. p < 0.001 for each comparison between patients with PGF and those without PGF.

 


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  		Figure 2. Kaplan-Meier survival by PGF, with analysis time in years. The p value was derived from the log-rank test between subjects with PGF and those without PGF. The number of subjects at risk per interval is reported along the x-axis. Hash marks indicate censoring events.

 
The median HLOS in 30-day survivors was 47 days among patients with PGF vs 15 days among those without PGF (p < 0.001). The median duration of mechanical ventilation was 15 days in PGF patients and 1 day in non-PGF patients among 30-day survivors (p < 0.001). The median number of 30-day ventilator-free days was 0 in PGF patients as opposed to 29 ventilator-free days in non-PGF patients (p < 0.001), indicating that the majority of patients with PGF died or continued to receive mechanical ventilation for the entire 30 days (ie, 0 ventilator-free days), and the majority of patients without PGF spent ≤ 1 day receiving mechanical ventilation and lived at least 30 days. A total of 28.5% of survivors in the PGF group achieved a normal age-appropriate 6MWT distance vs 71.4% of those without PGF within 12 months (RR for poorer performance in the PGF group, 2.52; 95% CI, 1.50 to 4.24; p = 0.014). As illustrated in Figure 3 , the median best 6MWT distance achieved within the first 12 months was 1,196 feet (8 patients; range, 600 to 1,223 feet) in PGF patients vs 1,546 feet (185 patients; range, 100 to 2645 feet) in non-PGF patients (p = 0.009 [rank sum test]).



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  		Figure 3. Comparison of median best 6MWT distance achieved during the first 12 months. The p value for the comparison was 0.009 (rank sum test).

 

   Discussion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
In this study, we have illustrated the profound impact of PGF on clinical course following lung transplantation. Our study shows that PGF is associated with a high mortality risk, as patients with PGF have a greater than fivefold increase in the risk of death during hospitalization. Further, the attributable mortality is high, as PGF is the major cause of early death following lung transplantation, contributing to almost half of deaths at 30 days. There is a protracted recovery of functional status, as evidenced by impaired 6MWT distance up to 1 year following hospital discharge.

In patients with PGF, the majority of deaths occur during hospitalization, with almost three of every four patients with PGF not surviving to hospital discharge. In addition, the finding of prolonged disability in survivors far beyond discharge from the hospital highlights the importance of PGF to overall transplant outcomes. The striking 6MWT distance difference highlights the protracted recovery in PGF patients, which is similar to findings in patients following prolonged critical illness and/or ARDS.910 The reasons for this observed long-term functional limitation are likely the same factors that contribute to the deficits in survivors of ARDS and other critical illnesses, as follows: muscle wasting; malnutrition; deconditioning; and other complications of prolonged hospitalization. In our cohort study, we did not have enough survivors past hospital discharge to examine the impact of PGF on chronic rejection, however, none of the eight patients who survived past hospital discharge developed clinical bronchiolitis obliterans syndrome during the duration of the follow-up.

The chosen definition of PGF contributes to the differences in observed mortality and other outcomes between published studies.17 King and colleagues2 employed a definition that was similar to ours, and found a comparable incidence of PGF (22%) with similar differences in hospital mortality and duration of mechanical ventilation. Our study adds to these findings by illustrating the relationship of PGF with impaired longer term functional outcomes. Using a more liberal PaO2/FIO2 ratio threshold to define PGF (ie, < 300), Thabut and colleagues8 reported an incidence of > 50%. Consequently, in their study, the differences in mortality and mechanical ventilation were not as striking. In contrast, using a compilation of data from many centers, the most recent International Society for Heart and Lung Transplantation registry report18 describes PGF as a significant and increasing contributor to mortality within the first 30 days following transplantation, accounting for > 30% of deaths in the first 30 days. However, the definition of PGF in this registry is not standardized. Recently, Chatilla and colleagues13 suggested that the major cause of early mortality is ischemia-reperfusion lung injury. In contrast, in our study other causes of postoperative respiratory failure (eg, less severe ischemia-reperfusion injury, pneumonia, and heart failure) were grouped for comparison against PGF. Even with these subjects included in the comparison group, the impact of PGF on outcomes was striking.

In a prior publication on this same cohort, we reported that a recipient diagnosis of primary pulmonary hypertension, donor age, donor female gender, and donor African-American race were associated with the development of PGF.7 We did not have enough subjects in the current study to evaluate the specific risk factors for mortality among subjects with PGF (30 patients with 8 survivors). However, we were able to assess whether any of these variables were responsible for the observed effect of PGF on mortality by serving as confounding variables. In a multivariable logistic regression model, no variables diminished the unadjusted OR of PGF for mortality.

The most important limitation in any cohort study is loss to follow-up.1920 Notably, in our mortality estimates no subjects were lost to follow-up. Our data on 6MWT distance were not rigorously collected at exactly the 12-month point but were complete in almost all patients within the period of observation. In addition, our cohort study design had the benefit of the calculation of a true RR of mortality from PGF, which is an important feature given that calculated ORs may be an inaccurate estimation of RR as the mortality rates following PGF were > 15% in the exposed (ie, PGF) group.

In conclusion, we have illustrated that PGF has a significant impact on mortality, HLOS, and duration of mechanical ventilation following lung transplantation. Survivors of PGF have a protracted recovery with impaired 6MWT distance at 12 months. Given the important impact of PGF on morbidity and mortality as well as on long-term function, studies aimed at a better understanding of the mechanism and modifiable risks of PGF are important directions for future research.


   Acknowledgements
 
The authors acknowledge M. Annette Hill for her administrative help in preparing this manuscript, Ejigayehu DeMissie, MSN, for her assistance with obtaining the data, and Dr. Gregory Tino for his insightful comments regarding the intellectual content.


   Footnotes
 
Abbreviations: CI = confidence interval; HLOS = hospital length of stay; OR = odds ratio; PaO2/FIO2 = arterial partial pressure of oxygen/fraction of inspired oxygen; PGF = primary graft failure; RR = relative risk; 6MWT = 6-min walk test

This research was supported by National Heart, Lung, and Blood Institute grant K23 HL04243, and by the Craig and Elaine Dobbin Pulmonary Research Fund.

Presented in part at the American Thoracic Society International Conference, May 2001, San Francisco, CA.

Received for publication February 5, 2004. Accepted for publication August 11, 2004.


   References
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 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

  1. Christie, JD, Bavaria, JE, Palevsky, HI, et al (1998) Primary graft failure following lung transplantation. Chest 114,51-60[Abstract/Free Full Text]
  2. King, RC, Binns, OA, Rodriguez, F, et al Reperfusion injury significantly impacts clinical outcome after pulmonary transplantation. Ann Thorac Surg 2000;69,1681-1685[Abstract/Free Full Text]
  3. Fisher, AJ, Wardle, J, Dark, JH, et al Non-immune acute graft injury after lung transplantation and the risk of subsequent bronchiolitis obliterans syndrome (BOS). J Heart Lung Transplant 2002;21,1206-1212[CrossRef][ISI][Medline]
  4. Khan, SU, Salloum, J, O’Donovan, PB, et al Acute pulmonary edema after lung transplantation: the pulmonary reimplantation response. Chest 1999;116,187-194[Abstract/Free Full Text]
  5. Arcasoy, SM, Kotloff, RM Lung transplantation. N Engl J Med 1999;340,1081-1091[Free Full Text]
  6. De Perrot, M, Sekine, Y, Fischer, S, et al Interleukin-8 release during early reperfusion predicts graft function in human lung transplantation. Am J Respir Crit Care Med 2002;165,211-215[Abstract/Free Full Text]
  7. Christie, JD, Kotloff, RM, Pochettino, A, et al Clinical risk factors for primary graft failure following lung transplantation. Chest 2003;124,1232-1241[Abstract/Free Full Text]
  8. Thabut, G, Vinatier, I, Stern, JB, et al Primary graft failure following lung transplantation: predictive factors of mortality. Chest 2002;121,1876-1882[Abstract/Free Full Text]
  9. Davidson, T, Caldwell, E, Curtis, J, et al Reduced quality of life in survivors of acute respiratory distress syndrome compared with critically ill control patients. JAMA 1999;281,354-360[Abstract/Free Full Text]
  10. Angus, DC, Musthafa, AA, Clermont, G, et al Quality-adjusted survival in the first year after the acute respiratory distress syndrome. Am J Respir Crit Care Med 2001;163,1389-1394[Abstract/Free Full Text]
  11. Herridge, MS, Cheung, AM, Tansey, CM, et al One-year outcomes in survivors of the acute respiratory distress syndrome. N Engl J Med 2003;348,683-693[Abstract/Free Full Text]
  12. Bernard, GR, Reines, HD, Brigham, KL, et al The American European consensus conference on ARDS: definitions, mechanisms, relevant outcomes and clinical trials coordination. Am J Respir Crit Care Med 1994;149,818-824[Abstract]
  13. Chatilla, WM, Furukawa, S, Gaughan, JP, et al Respiratory failure after lung transplantation. Chest 2003;123,165-173[Abstract/Free Full Text]
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Novel approaches to preventing PGF.
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