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(Chest. 2002;121:1876-1882.)
© 2002 American College of Chest Physicians

Primary Graft Failure Following Lung Transplantation*

Predictive Factors of Mortality

Gabriel Thabut, MD; Isabelle Vinatier, MD; Jean-Baptiste Stern, MD; Guy Lesèche, MD; Philippe Loirat, MD; Michel Fournier, MD and Hervé Mal, MD

* From the Service de Pneumologie et Réanimation Respiratoire (Drs. Thabut and Stern), and Service de Chirurgie Thoracique et vasculaire (Dr. Lesèche), Beaujon, Clichy; the Groupe de Transplantation Pulmonaire (Drs. Vinatier and Loirat), Hôpital Foch, Suresnes; and Unité Inserm 408 (Drs. Fournier and Mal), Faculté de Médecine Xavier Bichat, Paris, France.

Correspondence to: Gabriel Thabut, MD, Service de Pneumologie et Réanimation, Hôpital Beaujon, 100 avenue du Général Leclerc, 92110 Clichy, France; e-mail: gabriel.thabut{at}bjn.ap-hop-paris.fr


   Abstract
TOP
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 Conclusion
 References
 
Study objectives: To assess incidence, outcome, and early predictors of mortality for patients with primary graft failure (PGF) following lung transplantation (LTx), and to develop an injury severity score able to accurately predict ICU mortality for these patients.

Design: Retrospective cohort analysis.

Setting: Two LTx centers in Paris.

Patients: Two hundred fifty-nine patients who underwent LTx over a 12-year period.

Measurements and results: One hundred thirty-one patients (50.6%) met PGF criteria: radiographic graft infiltrate within the first 3 days following LTx associated with gas exchange impairment (PaO2/fraction of inspired oxygen ratio < 300 mm Hg). This syndrome was associated with an increased duration of mechanical ventilation (9.1 ± 1 days vs 3.1 ± 0.6 days, mean ± SD; p < 0.001) and ICU mortality (29% vs 10.9%; p < 0.01). The patients with PGF were randomly assigned to developmental (n = 85) and validation (n = 46) samples. Using logistic regression analysis, four variables were found associated with ICU mortality in these patients: age, degree of gas exchange impairment, graft ischemic time, and severe early hemodynamic failure. An ischemia/reperfusion injury severity score was derived using these four variables. Model calibration was good in the developmental and validation samples, as was model discrimination (area under receiver operating characteristic curves, 0.93 and 0.85, respectively).

Conclusion: PGF following LTx is a frequent event, with significant ICU morbidity and mortality. We demonstrate that four simple factors allow prediction of ICU mortality with good accuracy.

Key Words: human • lung transplantation • outcome assessment • prognosis • reperfusion injury


   Introduction
TOP
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 Conclusion
 References
 
Lung transplantation (LTx) has gained widespread acceptance as a therapeutic option in a selected number of patients with end-stage lung disease refractory to other forms of medical treatment.1 2 However, overall mortality following LTx is still notable. According to the International Registry, the 1-year actuarial survival is approximately 70%, and most of the deaths occur within 30 days of transplantation.3 The main cause of death during the first postoperative month is nonspecific graft failure secondary to ischemia/reperfusion injury.1 3 4 5 Early graft failure after LTx has been given various names, such as reimplantation edema, reperfusion edema, primary graft failure (PGF), or allograft dysfunction.

The diagnosis of PGF rests on the occurrence of noncardiogenic pulmonary edema with gas exchange impairment associated in severe cases with early hemodynamic failure (EHF).6 Despite the clinical importance of PGF, no scoring system based on objective data to assess its severity and to accurately predict mortality in the ICU is available. Based on the retrospective analysis of the data from two LTx centers, the aims of this study were the following: (1) to assess incidence and outcome of PGF, (2) to identify early risk factors associated with ICU death in patients with PGF, and (3) to develop and validate a simple ischemia/reperfusion injury severity score (IRISS).


   Materials and Methods
TOP
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 Conclusion
 References
 
Patients
All patients who underwent single LTx (SLT) or bilateral LTx (BLT) at two centers in Paris from 1988 to 2000 were analyzed in this study. During the study period, 277 patients underwent LTx in both institutions. Data were missing for 18 patients (6.5%). The remaining 259 patients form the basis of the study (Fig 1 ). Donor selection was based on widely accepted guidelines.7 The mean ± SD age of the donors was 31.7 ± 11 years. SLT was performed using a classical technique,8 whereas BLT was a bilateral sequential operation.9 Of the 259 patients, topical cooling was used in 30 cases at the beginning of the transplant programs. In the remaining patients, flush perfusion of the pulmonary artery was used. The types of perfusion solutions were University Wisconsin (n = 30), Cambridge solution (n = 86), Euro-Collins (n = 82), and Celsior (n = 31).



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  		Figure 1. Description of the study population. PGF- = without PGD; PGF+ = with PGF; I/R = ischemia/reperfusion.

 
Immunosuppression was achieved preoperatively by IV methylprednisolone and azathioprine. Postoperative initial immunosuppression consisted of cyclosporine, azathioprine, and corticosteroids. In both centers, IV cyclosporine was administered immediately postoperatively, and the conversion to the oral route was performed when tolerated. For the first year following transplantation, the cyclosporine dose was adjusted to achieve trough whole blood level of 200 to 300 ng/mL. Azathioprine was started at a dosage of 2 mg/kg/d and subsequently adjusted to maintain WBC count > 4,000/µL. Prednisone was started at a dose of 0.2 mg/kg/d. The daily dose was progressively increased to 0.5 mg/kg/d at 1 month and then tapered to 0.2 mg/kg/d. Antilymphocyte globulin was used at the onset of transplantation program in one center (Hôpital Beaujon), whereas induction therapy is still in use in the other center (Hôpital Foch). Overall, 201 patients (93 patients in Beaujon and 108 patients in Foch) received antilymphocyte globulin. Microbiological bronchial sampling was performed routinely on a daily basis as long as the patients were receiving mechanical ventilation. Transesophageal echocardiography in order to detect pulmonary artery or vein obstruction was performed only in selected cases. When the patients died from early graft dysfunction, autopsy study was performed systematically. We retrospectively reviewed the medical records of these patients in order to assess the following: (1) the incidence of PGF, (2) the outcome of patients with PGF, and (3) the risk factors associated with poor outcome.

Definition of PGF
PGF was defined by the presence of reperfusion pulmonary edema with or without EHF. Reperfusion pulmonary edema was defined by the presence of three criteria: (1) radiographic infiltrate in the graft that develops within the first 3 days following LTx, (2) PaO2/fraction of inspired oxygen (FIO2) ratio < 300 in the first 72 h following LTx, and (3) no evidence of bacterial infection, rejection, or atelectasis.

EHF was defined as the need for catecholamine agents to maintain mean systemic arterial pressure > 60 mm Hg. EHF was classified as moderate (dopamine requirement > 5 µg/kg/min up to 20 µg/kg/min) or severe (requiring the use of epinephrine or norepinephrine when dopamine was ineffective).

Assessment of Outcome of PGF
Patients with PGF were compared to those without this complication for the following variables: duration of mechanical ventilation, duration of ICU stay, and mortality (defined as vital status at ICU discharge). In patients with PGF, information related to donor (age, sex, cause of death, gas exchange just before harvest), recipient (age, sex, indication for transplantation), graft preservation (preservation fluid, graft ischemic time), surgical procedure (SLT or BLT, use of cardiopulmonary bypass), worst PaO2/FIO2 ratio in the first 72 h following LTx, and presence and severity of EHF were retrieved in order to identify early prognostic factors associated with ICU death and to develop an IRISS.

Statistical Analysis
To develop and validate a predictive model of survival, two thirds of the patients with PGF were randomly selected to a developmental sample, and the remaining third were assigned to a validation sample. Using the developmental sample, all recorded variables were screened for association with ICU mortality by univariate analysis using {chi}2, Student t test, and analysis of variance with Newman-Keuls as the post hoc test.

Any variable for which the univariate test had a p value < 0.25 was included in a multiple logistic regression model.10 Following the fit of the multivariate model, the importance of each variable included in the model was checked by examination of its associated p value and by comparison of each estimated coefficient with the coefficient from the univariate model containing only that variable. Variables that did not contribute to the model based on these criteria were removed and a new model was fitted. We checked the assumption of linearity in the logit for continuous scaled variables using the locally weighted least-squares smoothing function.11 The cumulative probabilities of survival were assessed by Kaplan-Meier product-limit estimates, and survival curves were compared using the log-rank test.

Development and Validation of an IRISS
Development of the IRISS was made following a previously described method using the variables found to be associated with ICU mortality on multivariate analysis.12 13 14 Briefly, the coefficient of each variable was multiplied by a factor 10 and rounded to a whole number. This allows the creation of the IRISS by summing the points associated with each variable. The IRISS was used as the single variable of a logistic regression analysis, producing the following equation: logit (P) = ß0 + ß1 x IRISS. The logit was converted to a probability of death (P) at ICU discharge as P = elogit/(1 + elogit), with e indicating the mathematical constant 2.71882. To evaluate calibration of the model, we used goodness-of-fit test described by Hosmer and Lemeshow11 on both the developmental and the validation sample. The Hosmer-Lemeshow technique is based on the comparison of expected and observed mortality. A small p value would suggest a lack of fit between expected and observed mortality. A p value > 0.1 was assumed to indicate a good agreement.

Area under the receiver operating characteristic (ROC) curve was used to evaluate discrimination power of the IRISS on both developmental and validation sample. A value > 0.8 was accepted to indicate good discrimination.15 Analysis was performed using software (STATA 6.0 for Windows; Stata Corporation; College Station, TX).


   Results
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 Conclusion
 References
 
Of the 259 patients, 131 patients (50.6%) met the criteria for PGF, and 70 of them had EHF. The main characteristics of the 259 patients are summarized in Table 1 and indications for LTx are given in Table 2 . Apart from the 39 patients with cystic fibrosis, the indications for BLT were emphysema (n = 23), bronchiectasis (n = 7), pulmonary fibrosis (n = 5), and pulmonary hypertension (n = 4). Ten of the 259 patients required mechanical ventilation prior to allograft implantation. Retransplantation was performed in 13 patients: 9 patients had PGF, whereas 4 patients did not. The indications for retransplantation in the nine patients with PGF was occurrence of bronchiolitis obliterans syndrome in all cases. Only data concerning 48 of 70 EHF patients were available. As previously described,6 the hemodynamic profile mimicked septic shock: cardiac index of 3.5 ± 1.1 L/min/m2 and systemic vascular resistance of 1,493 ± 458 dyne·s·cm-5·m2 (hemodynamic data collected with the patient receiving vasopressive and inotropic drugs, and obtained at the time of full-blown EHF).


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  		Table 1. Clinical Characteristics of Patients Included in the Study (n = 259)*

 

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  		Table 2. Indications for LTx*

 
The overall ICU mortality of the 131 patients with PGF was 29%, compared to 10.9% in those without PGF (p < 0.01). ICU mortality was 12% for patients without EHF, 18% for patients with moderate EHF, and 63% for patients with severe EHF (p < 0.01). PGF occurred within the first 24 h following LTx in > 90% of cases, and was associated with moderate-to-severe EHF in 53.4% of cases. A close relationship between severity of oxygenation impairment and severity of EHF was found (Table 3 ). Duration of mechanical ventilation was 9.1 ± 1 days in the PGF group vs 3.1 ± 0.6 days in the remaining patients (p < 0.001). Length of ICU stay was 22.7 ± 2 days in the PGF group vs 19.7 ± 1.5 days in the patients without PGF (p = 0.15). No difference in outcome was observed when the early-transplant and late-transplant experiences were compared. Similarly, no difference in outcome according to the institution was observed. The long-term survival of patients with and without PGF did not significantly differ (Fig 2 ).


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  		Table 3. Relationship Between Severity of Hemodynamic Failure and Gas Exchange*

 


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  		Figure 2. Long-term survival of patients with and without PGF. Overall survival in patients with and without PGF was not significantly different (p = 0.20). See Figure 1 legend for expansion of abbreviations.

 
On univariate analysis, of the variables described in "Materials and Methods," only five variables were found associated with ICU mortality: graft ischemic time, severe EHF, BLT, PaO2/FIO2 ratio, and age. Since the hemodynamic data were not available in all EHF patients, they were not incorporated into the final model. Using multivariate analysis, increasing age, graft ischemic time, degree of gas exchange impairment, and severe EHF were independently associated with ICU mortality in the developmental sample (Table 4 ). In this model, age, graft ischemic time, and PaO2/FIO2 ratio were modeled as continuous variables.


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  		Table 4. Multiple Logistic Regression Model With OR for ICU Mortality*

 
The IRISS was derived taking into account the four variables independently associated with ICU mortality. The patients from the different institutions were equally allocated to the developmental and validation models (n = 46 and n = 26 at Hôpital Beaujon, respectively; n = 39 and n = 20 at Hôpital Foch, respectively). Based on characteristics listed in Table 1 , no significant difference was found between developmental and validation samples. The IRISS points are shown in Table 5 . As indicated above, the IRISS, obtained by summing IRISS points, was used as the only term of a new logistic regression. This analysis yields the following results: logit (P) = 0.0833 x (IRISS) - 9.25. Figure 3 indicates the relationship between IRISS and predicted ICU mortality. The p value of the Hosmer-Lemeshow goodness-of-fit test was 0.75 in the developmental sample and 0.45 in the validation sample indicating a good fit between expected and observed mortality. The area under the ROC curve was 0.93 for the developmental sample and 0.85 in the validation sample.


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  		Table 5. IRISS Points

 


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  		Figure 3. Relationship between IRISS and probability of mortality at ICU discharge.

 

   Discussion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
Conclusion
 References
 
The key findings of this study are that: (1) PGF is a frequent event, occurring in approximately 50% of patients who underwent LTx; (2) PGF is associated with an increased ICU morbidity and mortality; (3) the presence of a moderate or severe EHF is a frequent event, associated with severe oxygenation impairment and poor outcome; (4) graft ischemic time, degree of gas exchange impairment, recipient age and presence of severe EHF are independently associated with outcome in patients with PGF; and (5) the knowledge of these four parameters allows prediction of ICU mortality with a good accuracy.

PGF is the major complication following LTx and is the main cause of death in the early postoperative period.1 2 3 The main clinical manifestation of PGF is noncardiogenic reperfusion edema. Its severity ranges from a mild form (allograft edema on chest radiograph without gas exchange impairment) to severe dysfunction leading to prolonged mechanical ventilatory support with high fatality rate.4 5 16 EHF may occur in association with reperfusion edema mimicking septic shock.6 17 18 The pathogenesis of PGF includes release of large amounts of reactive oxygen species and graft neutrophil accumulation.1 19 In the presence of EHF, local production and release of proinflammatory cytokines into the systemic circulation have also been described.6 Since the onset of PGF may be delayed after the procedure, we chose to take into account the first 3 postoperative days.20 21 In our series, the diagnosis of reimplantation edema was made using previously established criteria.16

Due to the lack of an homogeneous definition for PGF, its incidence varies markedly in published series. Using only a radiographic definition, Anderson et al20 found pulmonary infiltrates compatible with reperfusion edema in 97% of LTx recipients. Similar results were observed by Kundu et al,21 who studied 44 LTx procedures. Among them, the number of patients who presented radiographic manifestations of reperfusion edema at day 1 and at day 4 was 39 patients and 43 patients, respectively. These authors failed to detect a good correlation between radiographic features and oxygenation parameters. This lack of correlation was also reported in other studies.22 When the definition of reperfusion edema associated radiographic and oxygenation criteria, Sleiman et al16 and Khan et al,4 reported reperfusion edema in 60% and 57% of cases, respectively. In these series, reperfusion edema was associated with an increased morbidity and mortality. Christie et al,5 using very restrictive criteria, reported an incidence of this syndrome of about 15% with a 1-year mortality of 60%. We think that the lack of a standard definition accounts for the conflicting results of the studies analyzing the incidence and risk factors of this frequent event.

Several authors4 23 previously used severity scores to assess the severity of PGF. However, these scores were based on clinical judgment alone without prognostic relevance. The development of a scoring system based on mortality allows a more objective assessment of the severity of PGF. For this purpose, logistic regression permitted the selection of variables associated with mortality, to obtain the IRISS and convert this score to a probability of ICU death. This statistical approach has already been used to develop general scoring systems in ICU setting.12 13 24 The final multiple logistic regression model included four variables (age, ischemic time, presence of severe EHF, degree of gas exchange impairment) capable of accurately predicting mortality in patients with PGF following LTx. In our patients with PGF, age was closely associated with ICU death. In the general population, age has been found to predict mortality in ICU patients.25 In LTx recipients, age has also been identified as a predictor of 1-year mortality.3 Gas exchange impairment defined by the worst PaO2/FIO2 ratio within the first 3 postoperative days was part of our scoring system. Early postoperative gas exchange impairment has already been described as a major independent indicator of length of ICU stay after LTx,26 and was found to be predictive of 2-month mortality in a recent multicenter French study (unpublished data). Ischemic time was found to be independently associated with outcome in our study. The influence of graft ischemic time on reimplantation edema has already been demonstrated in a rat model of lung transplantation,27 where edema formation increased in proportion to the duration of graft ischemia. Controversial results have been observed in clinical transplantation. A negative influence of graft ischemic time on early graft function was found by several groups including ours,16 28 but others have not reported similar results.4 5 The deleterious effect of a long graft ischemia on survival was recently pointed out by Snell and coworkers29 and another study by Novick et al30 showed that the interaction of graft ischemic time and donor age was a significant predictor of 1-year mortality, whereas ischemic time per se was not a risk factor.30 Severe EHF requiring major vasoactive drugs such as epinephrine or norepinephrine was part of the IRISS. Since this complication mimics septic shock with hemodynamic collapse,6 vasoactive drugs are required. The gradation of EHF severity was based on the use of different catecholamine agents. In case of EHF, the first-line therapy is dopamine up to 20 µg/kg/min, with epinephrine or norepinephrine being used when the first-line treatment fails. The use of epinephrine or norepinephrine thus reflects the severity of hemodynamic failure. The difficulty of scoring cardiovascular variables has been highlighted by several authors.31 In these studies, the use and the type of vasoactive drugs administered were proposed for scoring severity of hemodynamic impairment. In our series, EHF was associated with the highest mortality odds ratio (OR) of 6.1, demonstrating its major role on ICU mortality. Similar findings were observed in patients with ARDS.32 To our knowledge, only one study6 focused on EHF in the setting of LTx. In this study,6 7 patients had EHF among 26 consecutive LTx recipients. All of them were severely hypoxemic and subsequently died within 3 weeks following LTx.

Examination of the variables not included in the final model also merits comments. Although these variables may be important in a univariate sense, they are not necessary components of our scoring system when other variables are included. For example, BLT was associated with mortality at ICU discharge on univariate analysis, but when included in the final model, this parameter did not increase the accuracy of the IRISS to predict mortality. The fact that a longer ischemic time is observed in cases of BLT could explain the increased ICU mortality in the latter group. From a statistical standpoint, the discrimination power of the model assessed by area under ROC curve seems good. Moreover, Hosmer-Lemeshow goodness-of-fit test indicates good agreement between expected and observed mortality in both the developmental and the validation sample, indicating the reliability of the scoring system employed. We feel that model validation using an external sample is mandatory especially when assessing predictive scores.11

What is the overall interest of such a score? This is not to estimate the risk of death in one patient but the percentage of patients with the same probabilities who are likely to die. Such a score may be useful to better assess the comparability of two groups in randomized studies, since it is the first scoring system, to our knowledge, to have survival prediction capabilities.


   Conclusion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Conclusion
References
 
PGF is a common clinical manifestation following LTx. This complication is associated with significant ICU mortality, especially when EHF coexists with PGF. The development of a simple and reliable scoring system allows better assessment of severity in this setting. We advocate the use of our definition of PGF together with this scoring system to ensure comparability of further studies.


   Footnotes
 
Abbreviations: BLT = bilateral lung transplantation; EHF = early hemodynamic failure; FIO2 = fraction of inspired oxygen; IRISS = ischemia/reperfusion injury severity score; LTx = lung transplantation; OR = odds ratio; PGF = primary graft failure; ROC = receiver operating characteristic; SLT = single lung transplantation

Received for publication June 8, 2001. Accepted for publication December 24, 2001.


   References
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Conclusion
 References
 

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T. Shimoyama, N. Tabuchi, K. Kojima, H. Akamatsu, H. Arai, H. Tanaka, and M. Sunamori
Aprotinin attenuated ischemia-reperfusion injury in an isolated rat lung model after 18-hours preservation
Eur. J. Cardiothorac. Surg., October 1, 2005; 28(4): 581 - 587.
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T. Oto, B. J. Levvey, D. V. Pilcher, M. J. Bailey, and G. I. Snell
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J. Thorac. Cardiovasc. Surg., July 1, 2005; 130(1): 180 - 186.
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D.V. Pilcher, C.D. Scheinkestel, G.I. Snell, A. Davey-Quinn, M.J. Bailey, and T.J. Williams
High central venous pressure is associated with prolonged mechanical ventilation and increased mortality after lung transplantation
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 Am. J. Respir. Crit. Care Med.Home page
G. Thabut, H. Mal, J. Cerrina, P. Dartevelle, C. Dromer, J.-F. Velly, M. Stern, P. Loirat, G. Leseche, M. Bertocchi, et al.
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J. D. Christie, J. S. Sager, S. E. Kimmel, V. N. Ahya, C. Gaughan, N. P. Blumenthal, and R. M. Kotloff
Impact of Primary Graft Failure on Outcomes Following Lung Transplantation
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 Am. J. Respir. Crit. Care Med.Home page
T. Goto, A. Ishizaka, F. Kobayashi, M. Kohno, M. Sawafuji, S. Tasaka, E. Ikeda, Y. Okada, I. Maruyama, and K. Kobayashi
Importance of Tumor Necrosis Factor-{alpha} Cleavage Process in Post-Transplantation Lung Injury in Rats
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 PerfusionHome page
G. Cattaneo, A. Strauss, and H. Reul
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 Am. J. Respir. Crit. Care Med.Home page
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Pulmonary Complications of Solid Organ and Hematopoietic Stem Cell Transplantation
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S. M. Levine and L. F. Angel
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Clinical Risk Factors for Primary Graft Failure Following Lung Transplantation
Chest, October 1, 2003; 124(4): 1232 - 1241.
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