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Ann Thorac Surg 2007;84:1121-1128
© 2007 The Society of Thoracic Surgeons

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Original Articles: General Thoracic

Lung Transplantation for Idiopathic Pulmonary Fibrosis

^a Department of Thoracic and Cardiovascular Surgery, Cleveland Clinic, Cleveland, Ohio
^b Department of Quantitative Health Sciences, Cleveland Clinic, Cleveland, Ohio
^c Department of Pulmonary, Allergy, and Critical Care Medicine, Cleveland Clinic, Cleveland, Ohio

Accepted for publication April 23, 2007.

^_* Address correspondence to Dr Mason, Department of Thoracic and Cardiovascular Surgery, Cleveland Clinic, 9500 Euclid Ave, Desk F24, Cleveland, OH 44195 (Email: masond2{at}ccf.org).

Presented at the Poster Session of the Forty-third Annual Meeting of The Society of Thoracic Surgeons, San Diego, CA, Jan 29–31, 2007.

	Abstract

Top Abstract Introduction Patients and Methods Results Comment Footnotes Acknowledgments References

 
Background: Outcomes of lung transplantation for idiopathic pulmonary fibrosis (IPF) are thought to be worse than those for other indications, although the reasons are unknown. In addition, the choice of single versus double lung transplantation is unclear. To guide decision-making, we (1) compared survival of patients receiving transplantation for IPF with survival of patients receiving transplantation for non-IPF diagnoses, (2) identified risk factors for mortality after transplantation for IPF, and (3) ascertained whether double lung transplantation for IPF confers a survival advantage.

Methods: From February 1990 to November 2005, 469 patients underwent lung transplantation, 82 for IPF. Multiphase hazard modeling was used to identify risk factors, and propensity matching was used to compare survival of IPF and non-IPF patients and to assess the effect of single versus double lung transplantation.

Results: Survival estimates after transplantation for IPF were 95%, 73%, 56%, and 44% at 30 days and 1, 3, and 5 years, somewhat worse than for matched non-IPF patients (p = 0.03). Risk factors for mortality were earlier date of transplantation (p = 0.07), single lung transplantation (p = 0.03), and higher wedge pressure (p = 0.003). Survival for double versus single lung transplantation was 81% versus 67% at 1 year and 55% versus 34% at 5 years; however, among matched non-IPF patients, corresponding survivals were 88% versus 71% at 1 year and 72% versus 48% at 5 years (p = 0.3).

Conclusions: Survival after lung transplantation for IPF is worse than after other indications for transplantation when multiple clinical variables are accounted for. Survival may be improved by double lung transplant.

	Introduction

Top Abstract Introduction Patients and Methods Results Comment Footnotes Acknowledgments References

 
Idiopathic pulmonary fibrosis (IPF) is the most common adult form of diffuse parenchymal lung diseases of unknown origin and is the second most common indication for transplantation in the United States after emphysema. Transplant outcomes are thought to be worse for IPF than for other indications, although there is no explanation for this difference [1–4]. However, the largest observational studies demonstrating a high early mortality after transplantation for IPF are not well controlled for donor, recipient, and transplant variables [5]. We hypothesize that survival after transplantation for IPF might be similar to that for other indications if early death could be minimized and patients matched on important clinical variables. In addition, choice of single versus double lung transplantation for IPF remains debated [6]. We hypothesize that patients undergoing double lung transplantation for IPF might have better survival than those undergoing single lung transplantation, as seen in patients receiving lung transplants for emphysema, if similar shortcomings of early death could be minimized [7, 8]. Therefore, to guide future decision-making, we evaluated our single-center experience and (1) compared survival of IPF versus non-IPF patients using matched patient populations, (2) identified risk factors for death after transplantation for IPF, and (3) ascertained whether double lung transplantation for IPF confers a survival advantage.

	Patients and Methods

Top Abstract Introduction Patients and Methods Results Comment Footnotes Acknowledgments References

 
Patients
From February 1990 to November 2005, 469 patients underwent primary lung transplantation for end-stage lung disease at Cleveland Clinic, exclusive of heart–lung transplantation. Eighty-two patients (17%) fulfilled the criteria for IPF as outlined by the American Thoracic Society [9]. Thirty-two (39%) of the 82 IPF patients underwent double lung transplantation.

Recipient, donor, and surgical data were extracted from the Unified Transplant Database, which has been approved for use in research by the institutional review board, with patient consent waived. The institutional review board approved supplemental review of medical records, also with patient consent waived.

End Point
The primary end point was all-cause mortality. Although most patients are followed clinically at Cleveland Clinic, formal anniversary follow-up is obtained yearly. Mean follow-up of surviving IPF patients was 3.9 ± 2.8 years (single lung transplant, 3.3 ± 1.4 years; double lung transplant, 4.5 ± 3.7 years); 18% were followed more than 5 years, and 227 patient-years of data were available for analysis. Among all patients (IPF and non-IPF), mean follow-up for surviving patients was 4.2 ± 3.0 years; 32% were followed more than 5 years, and 1,565 patient-years of data were available for analysis.

Data Analysis
Survival After Lung Transplantation for Idiopathic Pulmonary Fibrosis
Risk-unadjusted survival was estimated nonparametrically by the method of Kaplan and Meier, and parametrically by a multiphase hazard decomposition method [10]. (For additional details, see http://www.clevelandclinic.org/heartcenter/hazard.)

Nonproportional, multiphase, multivariable hazard methodology [10] was used to identify recipient, donor, and procedure variables (Appendix) associated with each hazard phase simultaneously. The process began with screening of values for variables to ensure that at least five IPF deaths were associated with each dichotomous variable. Bootstrap aggregation (bagging) was used for variable selection [11, 12] with a probability for inclusion of 0.05; variables appearing in at least 50% of bootstrap analyses were considered reliably statistically significant at a probability less than 0.05 (median rule).

Survival Comparison
Although survival may be worse after lung transplantation for IPF versus non-IPF, IPF may be simply a marker for a high-risk group of patients independent of the cause of their pulmonary disease. For example, IPF patients were more likely to be male, somewhat older, and larger than those with other etiologies (Table 1). As expected, their forced expiratory volume in 1 second was greater, but forced vital capacity less. Therefore, a propensity score for IPF was formulated, based on logistic regression of 24 donor, recipient, and transplant variables (Appendix) [13, 14]. The goal was to identify two subgroups of IPF and non-IPF patients matched as closely as possible so that comparison of survival of those patients would reflect a true difference rather than disparities in recipient and donor factors. Thus, variables were chosen that were general characteristics of patients undergoing lung transplantation, but not those that were surrogates for IPF (such as spirometry values). The C-statistic for the propensity model was 0.84. From this model, a propensity score was calculated for each patient and used for matching, yielding 70 IPF and non-IPF matched patient pairs. Twelve IPF patients were unable to be matched to similar non-IPF patients. Using the data set of matched patients, risk-adjusted comparison of survival for IPF versus non-IPF patients was performed. In addition, characteristics and survival of unmatched patients were explored (Table 2).

	Results

Top Abstract Introduction Patients and Methods Results Comment Footnotes Acknowledgments References

 
Idiopathic Pulmonary Fibrosis Versus Non–Idiopathic Pulmonary Fibrosis Survival Comparison
Risk-unadjusted survival after transplantation for IPF was 95%, 73%, 56%, 44%, and 36% at 30 days and 1, 3, 5, and 7 years, which was similar to 95%, 81%, 61%, 48%, and 38% at these same intervals after transplantation for non-IPF indications (p[early hazard phase] = 0.6, p[late hazard phase] = 0.5; Fig 1A). Instantaneous risk of death after lung transplantation for both IPF and non-IPF consisted of two hazard phases that differed early, but fell to equivalent levels after about 6 months, with risk at 2 years of 13% per year (Fig 1B). Recipient causes of death were similar in IPF and non-IPF patients.

View larger version (17K): [in this window] [in a new window]   Fig 1. Death after lung transplantation for idiopathic pulmonary fibrosis (IPF; red symbols and lines) versus other indications (non-IPF; blue symbols and lines). (A) Survival. Each symbol represents a death, vertical bars are 68% confidence limits equivalent to ± 1 standard error, and numbers in parentheses indicate patients remaining at risk. Solid lines enclosed within dashed 68% confidence limits represent parametric estimates. (B) Instantaneous risk of death (hazard function). Solid lines enclosed within dashed confidence limits represent parametric estimates. Note expanded horizontal scale.

View larger version (12K): [in this window] [in a new window]   Fig 2. Survival after lung transplantation in idiopathic pulmonary fibrosis (IPF; red symbols and lines) patients and patients undergoing transplantation for other indications (non-IPF; blue symbols and lines). Solid lines are propensity-matched patients, and dotted lines are unmatched patients. Vertical bars represent 68% confidence limits equivalent to ± 1 standard error, and numbers in parentheses indicate patients remaining at risk.

View larger version (6K): [in this window] [in a new window]   Fig 3. Percent of patients undergoing double lung transplantation for idiopathic pulmonary fibrosis. Numbers above bars represent patients undergoing transplantation.

View larger version (6K): [in this window] [in a new window]   Fig 4. Percent of patients undergoing lung transplantation for idiopathic pulmonary fibrosis who received double versus single lungs according to recipient age at transplantation. Dots indicate actual grouped percentage; solid line is trend line.

View larger version (13K): [in this window] [in a new window]   Fig 5. Survival after transplantation for idiopathic pulmonary fibrosis according to single (red lines) or double (blue lines) lung transplantation. Solid lines are 10 matched pairs, and dashed lines are unmatched patients. Format is as in Figure 2.

	Comment

Top Abstract Introduction Patients and Methods Results Comment Footnotes Acknowledgments References

Principal Findings
Survival After Lung Transplantation for Idiopathic Pulmonary Fibrosis
Patients undergoing transplantation for IPF had somewhat worse survival than patients undergoing transplantation for other indications, when matched on multiple variables. The reasons for this difference are unclear. It does not appear to be related to size of the transplanted organ. There was no difference in donor total lung capacity in patients undergoing transplantation for IPF and non-IPF indications. This surprising lack of size difference is attributable to our sizing strategy that uses donor organs whose predicted total lung capacity lies between the actual and predicted total lung capacity of the recipient. This "oversizes" donor lungs for IPF chests and "undersizes" lungs for patients with emphysema. However, the difference in survival may be related to the smaller chest size of IPF patients. Shrinking lung volume may have caused irreversible damage to pulmonary mechanics by contracting the chest wall (remodeling). Matching patients with different disease states by pretransplant pulmonary function tests is unfeasible because each disease has its own characteristic alteration in pulmonary function. For example, patients with IPF have smaller-than-predicted total lung capacity, and emphysema patients have larger-than-predicted total lung capacity; IPF patients have a restrictive pattern of pulmonary disease, and patients with emphysema have an obstructive pattern [16].

By definition, the underlying cause of IPF is unknown [17]. Antiinflammatory treatments such as corticosteroids and azathioprine have been shown to be useful [9, 18]; however, disease progression usually occurs. These agents are part of essential immunosuppressive therapy after lung transplantation. Idiopathic pulmonary fibrosis may carry a progressive course that is inhibited, but not eliminated, by transplantation and its immunosuppression regimen. Our data suggest that the driving force behind progression of pulmonary dysfunction may continue to affect the patient even after transplantation. Indirect evidence for this exists in patients with single lung transplantation for IPF: radiographic evidence has shown that the native lung usually demonstrates disease progression [19, 20]. Nevertheless, at this point, the reason for a survival disadvantage after transplantation for IPF remains elusive and warrants focused investigation. Causes of death in our patients undergoing transplantation for IPF were no different from those undergoing transplantation for other indications.

Risk Factors for Death After Lung Transplantation for Idiopathic Pulmonary Fibrosis
Factors associated with mortality were earlier date of transplantation for IPF, elevated wedge pressure, and single lung transplantation. Earlier date of transplantation as a risk factor reflects improvement in critical care management, antibiotic prophylaxis, immunosuppressive regimens, and our own experience in caring for patients after lung transplantation that has occurred over time.

Another risk factor identified for death after transplantation for IPF was higher cardiac wedge pressure. This finding was independent of elevated pulmonary artery pressures, which have been suggested as a risk factor for mortality after transplantation for IPF [5]. Elevated wedge pressures as a risk factor for transplantation for IPF may represent the effects of cardiac remodeling. Kroft and colleagues [21] used magnetic resonance imaging to examine cardiac function in patients with IPF and found impaired right ventricular diastolic function compared with control subjects. These patients also had lower cardiac output, although the study population was small and numbers did not reach statistical significance. Recent studies in patients with pulmonary arterial hypertension have shown that in the presence of a low cardiac index, lower, not higher, pulmonary pressures portend a worse prognosis [22–24]. A higher wedge pressure in our patients may reflect compensation occurring to maintain cardiac output. Finally, single lung transplantation was at least a marker for higher mortality after transplantation for IPF.

Single Versus Double Lung Transplantation for Idiopathic Pulmonary Fibrosis
Choice of single versus double lung transplantation in nonsuppurative lung disease remains a hotly debated topic. However, most of the debate has focused on transplantation for emphysema. Results appear to support a survival advantage for double lung transplantation, although this is confounded by increased risk with older recipient age and higher perioperative mortality [7, 8, 25–27]. Despite this, most transplant physicians advocate double lung transplantation for younger patients with emphysema.

Choice of single versus double lung transplantation for IPF is far less clear. One study comparing the two techniques demonstrated a survival advantage for single lung transplantation in patients with IPF [6]. However, perioperative mortality was higher for double lung transplantation, and follow-up was limited to 3 years. One-month mortality was 10% for single lung transplantation and 21% for double lung transplantation, compared with 6% for both single and double lung transplantation in our study. Increased perioperative mortality for double lung transplantation in that experience may have negated any survival benefit, with potential benefits not realized even by intermediate-term follow-up.

Another study comparing single versus double lung transplantation for IPF failed to demonstrate any survival advantage of double lung transplantation, although the study was small, with 32 single lung and 13 double lung transplantations [28]. The largest study evaluating lung transplantation for IPF used the International Society for Heart and Lung Transplant Registry for a cohort study of 830 patients, focusing on the effect of preoperative pulmonary artery pressure [5]. It excluded 667 patients because of incomplete data, was multi-institutional, had high 90-day mortality, and limited follow-up to 90 days. Results showed that double lung transplantation carried greater risk for early mortality, and elevated pulmonary artery pressures increased risk of death after single lung transplantation. The authors were unable to recommend one procedure over the other.

In our study, patients receiving double lung transplantation for IPF had better risk-unadjusted survival than those receiving a single lung. In fact, survival after double lung transplantation for IPF closely approximated survival for double lung transplantation for non-IPF indications. Reasons for improved survival with double lung transplantation are likely related to enhanced pulmonary reserve and improved respiratory mechanics. Improved survival with double lung transplantation for IPF was not true for matched patients. However, we were able to match only 10 pairs of sicker patients in our analysis. This small number of matched patients reflects a strong selection bias that was practiced at our program when choosing patients for single versus double lung transplantation for IPF and makes comparison difficult. The strongest discriminator was age, with younger patients receiving double lung transplantation and older patients receiving single. Although advanced age has been considered as a risk factor for double lung transplantation, we did not find it to be associated with increased mortality in our multivariable analysis, supporting emerging literature that double lung transplantation can be safely performed in older patients [29].

Interestingly, survival was worse for matched than unmatched patients in both the single and double lung groups. This provides some clues about contributors to worse outcomes in patients undergoing transplantation for IPF. Matched single lung transplantation patients were younger and received lungs from older donors than did unmatched single lung transplantation patients. Matched double lung transplantation patients were older and more likely to be smokers than were unmatched double lung transplantation patients.

Limitations
The primary limitation of this study is that it represents a clinical experience at a single center with a small number of patients undergoing transplantation for IPF. In addition, although we were able to show that patients undergoing transplantation for IPF had worse outcomes than those undergoing transplantation for other indications, we were not able to identify the reasons for this difference. Finally, choice of single versus double lung transplantation in our group was influenced by selection bias. Our lung transplant committee chooses patients based on objective as well as subjective criteria that made propensity matching in our analysis difficult. This highlights the need for a prospective, randomized trial of single versus double lung transplantation for IPF.

Conclusions
Survival after lung transplantation for IPF is worse than after other indications for lung transplantation. However, survival of these patients is better if they receive two lungs and approaches survival of patients undergoing transplantation for non-IPF indications. Our numbers were small, however, and this advantage could not be demonstrated in our matched analysis. Choice of procedure must be balanced against allocating a scarce resource with the potential to save two lives rather than one. However, given the national trend of decreasing waiting times, as well as decreasing waiting list mortality in the face of an increasing proportion of double lung transplantations being performed [4], the primary focus should be on improving individual patient outcome. Therefore, we cautiously recommend double lung transplantation for patients with IPF, although a prospective, randomized trial will be necessary to resolve this issue definitively.

	Appendix

 
Variables Used in Analyses
Recipient
Demographic: Sex,^_* age,^_* race (Caucasian,^_* African-American), height, weight,^_* weight-to-height ratio, body surface area, body mass index

Cardiac and pulmonary: Blood pressure (systolic,^_* diastolic, mean), cardiac index,^_* cardiac output, central venous pressure,_^* pulmonary artery pressure (systolic,^_* diastolic, mean), pulmonary vascular resistance,^_* wedge pressure, forced expiratory volume in 1 second (actual and percent of predicted), forced vital capacity (actual and percent of predicted), ratio of forced expiratory volume in 1 second percent of predicted to forced vital capacity percent of predicted

Comorbidities: History of hypertension,^_* history of smoking

Serology/immunology: Blood type (A, B, AB,^_* O, Rh positive), pretransplantation serum creatinine,^_* pretransplantation panel-reactive antibody, cytomegalovirus (immunoglobulin G), Epstein-Barr virus (immunoglobulin G)

Donor
Demographic: Sex,^_* age,^_* race (Caucasian,^_* African-American), height, weight,^_* weight-to-height ratio, body surface area, body mass index

Comorbidities: History of hypertension^_*

Serology: Blood type (A,^_* B, O, Rh positive), serum creatinine, cytomegalovirus (immunoglobulin G)

Lung size: Total lung capacity^_*

Cause of death: Cerebral bleed, stroke, head trauma^_*

Donor/Recipient: Rh-factor mismatch, cytomegalovirus (CMV) mismatch (CMV⁺ donor to CMV^– recipient)

Transplantation: Years from January 1, 1990, to transplantation,^_* double lung transplantation,^_* right side transplantation, left side transplantation,^_* cold ischemic time^_*

____________________

	Acknowledgments

Top Abstract Introduction Patients and Methods Results Comment Footnotes Acknowledgments References

 
We acknowledge and appreciate the expert editing and manuscript preparation by Tess Parry.

	Footnotes

Top Abstract Introduction Patients and Methods Results Comment Footnotes Acknowledgments References

 
^_* Indicates variables used in propensity matching IPF to non-IPF patients.

Indicates variables used in propensity matching single to double lung transplantation in IPF patients.

	References

Top Abstract Introduction Patients and Methods Results Comment Footnotes Acknowledgments References

 

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This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Personal Folders Download to citation manager Author home page(s): David P. Mason Mariano E. Brizzio Sudish C. Murthy Gösta B. Pettersson Eugene H. Blackstone Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Mason, D. P. Articles by Blackstone, E. H. Search for Related Content PubMed PubMed Citation Articles by Mason, D. P. Articles by Blackstone, E. H. Related Collections Lung - transplantation