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(Chest. 2002;122:779-784.)
© 2002 American College of Chest Physicians

Predicting Survival of Lung Transplantation Candidates With Idiopathic Interstitial Pneumonia*

Does PaO2 Predict Survival?

Suzanne J. Timmer, MD; Amir M. Karamzadeh, MD; G.L. Yung, MD, FCCP; Jolene Kriett, MD; Stewart W. Jamieson, MB, FCCP and Cecilia M. Smith, DO

* From the Division of Pulmonary Medicine (Dr. Timmer), Naval Medical Center, San Diego, CA; the College of Medicine (Dr. Karamzadeh), University of California, Irvine, CA; the Divison of Pulmonary and Critical Care Medicine (Drs. Yung and Smith) and the Department of Surgery (Dr. Jamieson), Division of Cardiothoracic Surgery, University of California, San Diego Medical Center, San Diego, CA.

Correspondence to: Suzanne Timmer, MD, Naval Hospital Pensacola, Internal Medicine Department, 6000 W Highway 98, Pensacola, FL 32512; e-mail: timmersj{at}hotmail.com


   Abstract
TOP
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 Conclusion
 References
 
Objective: To find a parameter that would discriminate between the patients with idiopathic interstitial pneumonia who survived to undergo transplantation and those who died while waiting to undergo transplantation.

Methods: A retrospective review was performed of all lung transplant referrals for idiopathic interstitial pneumonia that were listed with United Network for Organ Sharing at the University of California San Diego from January 1990 to February 1999. Of the 331 patients who were listed, 48 met the eligibility criteria. Patient demographics, radiographic studies, pathology reports, and the results of resting and exercise cardiopulmonary function tests were recorded from each patient’s chart. Patients were divided into the following two groups: those patients who survived until transplantation and those still waiting were classified as "alive"; and those patients who died before undergoing transplantation were classified as "deceased." Results: Forty-three of 48 patients had a pathologic diagnosis. The cohort included 25 patients with usual interstitial pneumonitis, 3 patients with nonspecific interstitial pneumonitis, 1 patient with desquamative interstitial pneumonitis, and 14 patients with interstitial lung disease of unknown etiology. The only significant difference between the two groups was resting PaO2 (p = 0.035). A stepwise multivariate analysis demonstrated that PaO2 and FEV1/FVC ratio were significantly associated with survival (hazards ratio, 1.06; confidence interval, 0.99 to 1.13; p = 0.019).

Conclusions: A survival analysis using PaO2 and FEV1/FVC ratio values proved to be statistically significant, but a prospective trial is needed to determine the clinical relevance of these parameters for predicting survival in patients with idiopathic interstitial pneumonia.

Key Words: interstitial lung disease • lung transplantation


   Introduction
TOP
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 Conclusion
 References
 
James Hardy performed the first human lung transplant at the University of Mississippi in June 1963. Between 1963 and 1974, only 2 of the 36 patients who underwent transplantation lived longer than 1 month. After such a dismal start, the idea of lung transplantation was abandoned until the introduction of cyclosporine. In 1981, the first successful heart-lung transplantation was performed for pulmonary vascular disease at Stanford University. Lung transplantation has now been performed for a variety of diseases, including primary pulmonary hypertension, interstitial lung diseases (ILDs), COPD, and cystic fibrosis. In the United States, the demand for suitable organs has continued to rise, exceeding the annual supply.1 As a result, patients may wait up to 2 years for transplantation, and approximately 15% of those waiting for organs die before one becomes available.1 This waiting period must be taken into consideration when clinicians decide to refer a patient for a transplant evaluation.

The category of ILD includes many different diseases of known and unknown etiologies. In 1998, Katzenstein and Myers2 reported that patients in whom interstitial pulmonary fibrosis (IPF) had been diagnosed previously may have one of four distinct histopathologic entities. These include usual interstitial pneumonitis (UIP), desquamative interstitial pneumonitis (DIP), nonspecific interstitial pneumonitis (NSIP), and respiratory bronchiolitis ILD (RBILD). The failure to recognize these different histopathologic diagnoses as separate ILDs may explain the variable prognosis and response to therapy of patients with IPF. Therefore, only patients with UIP found in biopsy specimens should receive a diagnosis of IPF. The determination of optimal referral time is critical for IPF patients because their mean survival time after diagnosis is only 3 to 5 years.3 Katzenstein and Myers2 have included all four of these entities under the term idiopathic interstitial pneumonia. This report will focus on the idiopathic interstitial pneumonias. Although there is agreement among clinicians about the disease-defining criteria, the factors affecting the prognosis of patients with idiopathic interstitial pneumonia are poorly understood. The purpose of this study was to evaluate the predictors of survival for patients with idiopathic interstitial pneumonia (ie, NSIP, DIP, RBILD, and UIP) who were referred for lung transplantation.


   Materials and Methods
TOP
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 Conclusion
 References
 
A retrospective review was performed of all lung transplant referrals for idiopathic interstitial pneumonia listed with the United Network for Organ Sharing (UNOS) at the University of California San Diego from January 1990 to February 1999. Forty-eight transplant candidates met the inclusion criteria, which included the following: (1) a diagnosis of idiopathic interstitial pneumonia, as determined by clinical history, serology, chest radiograph, and/or high-resolution CT (HRCT) scan, and pathology specimen, if obtained; and (2) age > 18 years. Patients with diffuse ILD that was caused by occupational exposures, sarcoidosis, collagen vascular diseases, prior radiation, or infection were excluded from the study. In addition, UCSD pathology reports, pulmonary function laboratory charts, and inpatient hospital records also were reviewed. All patients had diffuse interstitial opacities found on chest radiographs and restrictive pulmonary physiology.

Data collected from the charts included patient demographics, results of pulmonary function tests, cardiopulmonary exercise studies, radiographic reports, pathology findings, and dates of symptom onset, diagnosis, referral, UNOS listing, transplantation, and death. Cardiopulmonary exercise testing included maximum oxygen consumption (O2max) and steady-state exercise. The pulmonary function and cardiopulmonary exercise tests were performed at the University of California San Diego or the referring institution. Based on this review, patients were divided into the following two groups: those who survived until undergoing transplantation and those still waiting for transplantation were classified as "alive"; and those who died before undergoing transplantation were classified as "deceased." The patients who died after undergoing transplantation were included in the alive group for the purpose of this study.

Statistical analyses were performed using a statistical software package (Stata Corp; College Station, TX). Descriptive statistics were used to describe patient characteristics. Continuous data were expressed as means, and categoric data were expressed as counts and proportions. Two-group comparisons were contrasted using two-tailed t tests for means if the data were normally distributed or with a rank-sum test if the data were not normally distributed. Categoric data were analyzed using either the {chi}2 test or Fisher exact test. Kaplan-Meier graphs were used to demonstrate survival over time, and the log rank test was used to determine the significance between the graphs. Patients who underwent lung transplantation were censored at the time of transplantation, and patients who were alive awaiting transplantation were censored on a fixed date for data collection. Variables that were statistically significant by univariate analysis were entered into a multiple logistic regression model. A p value of > 0.10 was used as the criterion for removal of the covariates from the model.


   Results
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 Conclusion
 References
 
Of 331 patients listed with UNOS from January 1990 to February 1999, 48 met the study eligibility criteria. Twenty-eight patients were classified as alive, and 20 were classified as deceased. At the end of the data collection period, 19 patients had undergone lung transplantation, and 9 patients were alive and waiting for a transplant. Forty-three of 48 patients in the study had a pathologic diagnosis. Twenty-five of the 48 patients had pathologic findings of UIP. The remainder of diagnoses included 3 patients with NSIP, 1 patients with DIP, and 14 patients with interstitial fibrosis of unknown etiology (Table 1 ). Eight of 48 patients lacked a pathologic diagnosis prior to undergoing transplantation, and their conditions were diagnosed clinically as idiopathic interstitial pneumonia. Three of the eight patients underwent transplantation and had a pathologic examination of the explanted lung that revealed UIP. Five of 48 patients lacked a lung biopsy and did not undergo transplantation.


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  		Table 1. Histopathology Findings on Biopsy Specimens of Patients With Idiopathic Interstitial Pneumonia

 
There was not a statistically significant difference in age at the time of referral, sex, race, or body mass index (BMI) between those in the alive or deceased groups (Table 2 ). The mean time from symptom onset to diagnosis was 20.07 months in the alive group and 23 months in the deceased group (p = 0.62). The mean time from diagnosis to referral for transplantation evaluation was 43.2 months in the alive group and 20.9 months in the deceased group. However, the median value for the interval was 22.4 months in the alive group and 14 months in the deceased group, demonstrating the presence of a non-normal distribution. There was no statistically significant difference in the time from diagnosis to referral in the two groups (p = 0.43). The number of patients with a pathologic diagnosis of UIP was 18 of 28 patients (64%) in the alive group and 7 of 20 patients (35%) in the deceased group. The time from diagnosis to referral in the UIP subgroup was 40.3 months in the alive group and 23.0 months in the deceased group. The three patients with NSIP were in the alive group.


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  		Table 2. Demographic and Clinical Characteristics of Idiopathic Interstitial Pneumonia Patients*

 
There were no significant differences in the percent of predicted values for FEV1, FVC, total lung capacity (TLC), or diffusing capacity of the lung for carbon monoxide (DLCO) [Table 3 ]. The FEV1/FVC ratio was higher in the deceased group but did not reach statistical significance (p = 0.06). The changes in values for exercise PaO2, resting PCO2, exercise PCO2, and O2max, expressed as a volume per the weight of each patient, were not statistically significant. Fourteen of 48 patients had arterial blood gas levels measured during exercise, and 27 of 48 patients had results of cardiopulmonary exercise testing. All of the hemodynamic measurements were recorded during right heart catheterization. There was no significant difference in the systolic pulmonary artery pressure, diastolic pulmonary artery pressure, mean pulmonary artery pressure, or cardiac output between the two groups. The mean PaO2 in the alive group was 62.4 mm Hg, and in the deceased group it was 53.9 mm Hg (p = 0.04). The only statistically significant gas exchange abnormality between the two groups was resting PaO2. In order to determine the clinical relevance of the parameters that were statistically significant between the two groups, a survival analysis was performed. Because the FEV1/FVC ratio approached statistical significance, it was included in the survival analysis. A univariate Cox regression analysis demonstrated that the FEV1/FVC ratio was a significant predictor of survival (hazards ratio, 1.07; 95% confidence interval [CI], 1.00 to 1.14; p = 0.04). In stepwise multivariate analysis, PaO2 and FEV1/FVC ratio were significantly associated with survival (hazards ratio, 1.07; 95% CI, 1.00 to 1.14; p = 0.03).


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  		Table 3. Resting and Exercise Cardiopulmonary Function Tests*

 

   Discussion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
Conclusion
 References
 
Although there have been other articles advocating a better prognosis for patients with NSIP, predicting survival in patients having the other subgroups of idiopathic interstitial pneumonia remains difficult.3 DIP has a reported 10-year survival rate of 70%.3 The clinical course of patients with RBILD is unknown, but appears to be substantially better than those with IPF.3 A handful of studies in the literature have identified predictors of survival in IPF patients.

Schwartz et al4 performed a survival analysis of 74 IPF patients. A Cox regression analysis demonstrated that decreased survival was associated with male gender, a higher FEV1/FVC ratio, and the enhanced release of prostaglandin E2 by cultured alveolar macrophages. Hanson et al5 evaluated post-therapy changes in pulmonary function tests as predictors of survival in 58 IPF patients. He noted that patients with a >= 10% reduction in FVC or a >= 20% reduction in DLCO after treatment had decreased survival times compared with patients whose test results improved or were unchanged. Erbes et al6 also evaluated the utility of pulmonary function and steady-state exercise tests in predicting survival in patients with IPF. They measured lung volumes, spirometry, DLCO, and arterial oxygen saturation at rest and with steady-state exercise. The results demonstrated diminished survival times of patients with age > 50 years, and a reduction in either TLC and/or vital capacity (VC) of > 2 SDs below the predicted values. Gay et al7 prospectively studied 38 IPF patients to identify pretreatment features, including clinical factors, HRCT findings, and pathologic characteristics that could be used to predict short-term improvement in pulmonary function and long-term survival. Thirty-seven of 38 patients had a pathologic diagnosis of UIP. Patients were assigned a clinical-radiographic-physiologic score based on the degree of dyspnea, radiographic features, spirometry, DLCO, lung volumes, and exercise testing results. HRCT scans were reviewed and graded for the degree of ground glass and reticular opacities. Patients’ biopsy specimens also were scored for the amount of fibrosis, cellularity, desquamation, and granulation or connective tissue. HRCT imaging and pathologic fibrosis scores were able to reliably predict long-term survival. Among these reports, clinicians have been unable to find any combination of parameters that will uniformly predict survival time and that may be used as a criterion to decide a patient’s optimal referral time.

Two studies in the literature have addressed predictors of survival in lung transplant candidates. The first was a retrospective analysis comparing the survival of patients with IPF, histocytosis X, and lymphangioleiomyomatosis. Harari et al8 evaluated the prognostic value of pulmonary hypertension in patients with chronic lung disease who were referred for lung or heart-lung transplantation. The results of spirometry, resting arterial blood gas measurements, and hemodynamic measurements made during right heart catheterization were reviewed. Of the 67 patients in the study, 43 had diagnoses of IPF, 18 had diagnoses of histocytosis X, and 6 patients had diagnoses of lymphangioleiomyomatosis. Four of the IPF patients lacked a pathologic diagnosis. Eight IPF patients who received a transplant were not included in the statistical analysis. Harari et al8 found that hemodynamics and respiratory function were not related to survival time in patients with IPF and histocytosis X. Histocytosis X patients actually survived longer than those with IPF despite having more severe pulmonary hypertension. The second study, by Vizza et al,9 was a retrospective review of 146 lung transplant candidates with cystic fibrosis. Decreased survival time was associated with shorter 6-min walk distance, elevated systolic pulmonary artery pressure, and the presence of diabetes mellitus.

The evolution of lung transplantation has been the greatest hope for improving the quality of life for patients with IPF, but the optimal time for patient referral to a lung transplant center is not well-defined. Currently, it is recommended that patients be referred who have TLC or VC values that are < 60 to 65% of predicted values, have resting or exercise hypoxemia PaO2 values of < 55 mm Hg, and/or have failed to respond to corticosteroids or immunosuppressive therapy.2 10 Because IPF patients with a histologic diagnosis of UIP have a worse prognosis than patients with other lung diseases requiring transplantation, UNOS has developed a policy to provide patients with a diagnosis of IPF a 90-day credit on the waiting list.3 Our finding that a larger percentage of patients in the alive group had a pathologic diagnosis of UIP reflects that fact that 14 patients had ILD of unknown etiology found in biopsy specimens. If most of those patients had IPF, it would explain the disparity between our findings and those in the literature. The outcomes of transplant candidates with other histopathologic variants of idiopathic interstitial pneumonitis have not been reported. The discovery of a parameter that would discriminate between the patients who survived and were to be transplanted and those who died while waiting to undergo transplantation could optimize the timing of patient referral for transplant evaluation. This study was designed to determine whether pulmonary function tests, exercise studies, or hemodynamic measurements would reliably predict the survival of transplant candidates with idiopathic interstitial pneumonia. The fact that the two groups did not differ in age, sex, race, BMI, time to diagnosis or referral, and results of pulmonary or cardiac physiologic studies refutes the claim that those who died simply had more advanced disease at the time of referral.

Although it has been postulated that patients with idiopathic interstitial pneumonia die from sequelae of progressive pulmonary hypertension, we found that the values for pulmonary artery pressure and cardiac output of those patients who survived to transplantation were not significantly different from those who died.11 Other authors6 have reported that patients with a lower VC (2 SDs below that predicted) and/or TLC (2 SDs below that predicted) have a worse prognosis. Our data did not show any significant differences in FEV1, FVC, or TLC between the patients in the two groups. The log rank test demonstrated that the FEV1/FVC ratio approached statistical significance between the two groups (p = 0.06). A univariate Cox regression analysis demonstrated the PaO2 values of patients in the alive group were significantly higher than those in the deceased group and correlated with an improved survival time (hazard ratio, 0.96; 95% CI, 0.92 to 1.0; p = 0.04). Figure 1 demonstrates that a PaO2 >= 50 mm Hg was correlated with an improved survival time. After adjusting for a critical change of 5 mm Hg, the difference in PaO2 values between the two groups did not show any clinically significant correlation with survival (hazards ratio, 0.82; 95% CI, 0.67 to 1.00). Multivariate logistic regression showed that PaO2 and FEV1/FVC ratio were correlated with an improved survival time (hazard ratio, 1.07; 95% CI, 1.00 to 1.14; p = 0.04]). Although the difference in PaO2 between the two groups was statistically significant, a prospective trial to replicate this finding would be important to determine whether it is clinically significant. One of the limitations of the study is the small number of patients with exercise data. Determining the utility of exercise PaO2, PCO2, and O2max values in predicting the survival time of this population will require a greater number of patients with these measurements.



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  		Figure 1. Kaplan-Meier survival plots by PaO2.

 
The mean survival time, defined as the period from UNOS listing to death, transplant, or time of this chart review (February 1999), was 10.2 months (range, 0.3 to 74.3 months). The mean survival time for patients with a pathologic diagnosis of UIP was 9.6 months compared with the remainder of patients whose mean survival time was 10.6 months. The mean time from diagnosis to death, transplant, or the chart review was 48.7 months in the patients with a pathologic diagnosis of UIP and 44.8 months in the remainder. The literature contains many reports of decreased survival time of patients with the pathologic variant of UIP compared to NSIP or DIP.2 All three patients with a histologic diagnosis of NSIP were in the alive group. There were an insufficient number of patients with DIP, RBILD, and NSIP to warrant any interpretation.


   Conclusion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Conclusion
References
 
The only statistically significant parameter separating those who were alive from those who had died was resting PaO2. This finding has not been previously reported. A survival analysis using FEV1/FVC ratio and PaO2 values proved to be statistically significant, but a prospective trial is needed to determine the clinical relevance of these parameters for predicting survival time in patients with idiopathic interstitial pneumonia. Lung transplantation remains the best hope for an improved quality of life for many patients with chronic lung disease. As clinicians learn more about the correlation between a clinical course and the pathologic variants of idiopathic interstitial pneumonia, the uncertainty surrounding the optimal time for transplantation referral may be resolved. The logical solution for improving survival times in IPF patients is the early referral for transplantation of those patients with UIP found in lung biopsy specimens. We must continue to look for disease parameters that will predict survival in order to decrease the number of patients dying while waiting to undergo lung transplantation.


   Footnotes
 
Abbreviations: BMI = body mass index; CI = confidence interval; DIP = desquamative interstitial pneumonitis; DLCO = diffusing capacity of the lung for carbon monoxide; HRCT = high-resolution CT; ILD = interstitial lung disease; IPF = interstitial pulmonary fibrosis; NSIP = nonspecific interstitial pneumonitis; RBILD = respiratory bronchiolitis interstitial lung disease; TLC = total lung capacity; UIP = usual interstitial pneumonitis; UNOS = United Network for Organ Sharing; VC = vital capacity; O2max = maximum oxygen consumption

The views expressed in this article are those of the authors and do not reflect the official policy or position of the Department of the Navy, Department of Defense, or the United States Government.

Received for publication June 12, 2001. Accepted for publication February 14, 2002.


   References
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Conclusion
 References
 

  1. Trulock, EP (1997) State of the art: lung transplantation. Am J Respir Crit Care Med 155,798-818
  2. Katzenstein, AA, Myers, JL State of the art: idiopathic pulmonary fibrosis clinical relevance of pathologic classification. Am J Respir Crit Care Med 1998;157,1301-1315[Free Full Text]
  3. American Thoracic Society. Consensus statement on idiopathic pulmonary fibrosis: diagnosis and treatment. Am J Respir Crit Care Med 2000;161,646-664[Free Full Text]
  4. Schwartz, DA, Helmers, RA, Galvin, JR, et al Determinants of survival in idiopathic pulmonary fibrosis. Am J Respir Crit Care Med 1994;149,450-454[Abstract]
  5. Hanson, D, Winterbauer, RH, Kirtland, SH, et al Changes in pulmonary function test results after one year of therapy as predictors of survival in patients with idiopathic pulmonary fibrosis. Chest 1995;108,305-310[Abstract/Free Full Text]
  6. Erbes, R, Schaberg, T, Loddenkemper, R Lung function tests in patients with idiopathic pulmonary fibrosis: are they helpful for predicting outcome? Chest 1997;111,51-57[Abstract/Free Full Text]
  7. Gay, SE, Kazerooni, EA, Toews, GB, et al Idiopathic pulmonary fibrosis: predicting response to therapy and survival. Am J Respir Crit Care Med 1998;157,1063-1072[Abstract/Free Full Text]
  8. Harari, S, Simonneau, G, DeJuli, E, et al Prognostic value of pulmonary hypertension in patients with chronic interstitial lung disease referred for lung or heart-lung transplantation. J Heart Lung Transplant 1997;16,460-463[ISI][Medline]
  9. Vizza, CD, Yusen, RD, Lynch, JP, et al Outcome of patients with cystic fibrosis awaiting lung transplantation. Am J Respir Crit Care Med 2000;162,819-825[Abstract/Free Full Text]
  10. Smith, CM Patient selection, evaluation, and preoperative management for lung transplant candidates. Clin Chest Med 1997;18,183-197[CrossRef][ISI][Medline]
  11. Jezek, V The prognosis and development of pulmonary hypertension in idiopathic diffuse interstitial lung fibrosis. G Ital Cardiol 1984;14(suppl),39-45



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