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Ann Thorac Surg 2008;85:1193-1201. doi:10.1016/j.athoracsur.2007.12.023
© 2008 The Society of Thoracic Surgeons
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Right arrow Lung - transplantation

Original Articles: General Thoracic

Spirometry After Transplantation: How Much Better Are Two Lungs Than One?

David P. Mason, MDa,*, Jeevanantham Rajeswaran, MSb, Sudish C. Murthy, MD, PhDa, Ann M. McNeill, RNa, Marie M. Budev, DOc, Atul C. Mehta, MDc, Gösta B. Pettersson, MD, PhDa, Eugene H. Blackstone, MDa,b

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 December 4, 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).


   Abstract
Top
 Abstract
Introduction
 Patients and Methods
 Results
 Comment
 Footnotes
 Acknowledgments
 References
 
Background: The purpose of this study was to determine how much double lung transplantation improves lung function over single lung transplantation and to identify predictors of lung function after transplantation.

Methods: From February 1990 to November 2005, 463 adults underwent lung transplantation. Among 379 of these patients (82%), 6372 evaluations of postoperative normalized forced expiratory volume in 1 second (FEV1) and forced vital capacity (FVC) were analyzed using longitudinal temporal decomposition methods for repeated continuous measurements. We characterized the time course of postoperative spirometry, compared it between double and single lung transplantation, and identified its modulators.

Results: FEV1 (% of predicted) was only somewhat better after double than single lung transplantation (65%, 58%, and 59% vs 51%, 43%, and 40% at 1, 3, and 5 years, p = 0.03), as was FVC (% of predicted) (67%, 68%, and 66% vs 62%, 56%, and 51%, p < 0.0001). Both FEV1% and FVC% increased sharply to 1 year. For double lung transplantation, these values persisted, with minimal decline to 5 years; but for single lung transplantation, they continuously declined to 5 years. Values for double lung transplantation remained higher than for single lung transplantation at all time points but never approached twice the value. Patients undergoing double lung transplantation for emphysema had the highest postoperative FEV1% and FVC%, but also the lowest values for single lung transplantation; the benefit of double lung transplantation was between these values for other diagnoses.

Conclusions: Spirometry weakly favors double lung over single lung transplantation. The advantage of spirometry values alone may not justify double lung transplantation.


   Introduction
Top
 Abstract
 Introduction
Patients and Methods
 Results
 Comment
 Footnotes
 Acknowledgments
 References
 
The advantage of double lung transplantation (LTx) over single LTx remains debated [1]. Data suggest a survival advantage for patients undergoing double LTx for emphysema, although this advantage has not been well demonstrated for other transplant indications [2–4]. Although some studies have focused on predictors of postoperative lung function after LTx and the impact of single vs double LTx, they have been limited to patients who have received a transplant for emphysema or the relative impact of bronchiolitis obliterans syndrome (BOS) [5–10].

In this study, we examined spirometry of a large cohort of patients with multiple longitudinal pulmonary function tests to assess temporal trends and compare outcomes of single and double lung LTx for all transplant indications and regardless of BOS. This seems particularly important in determining the incremental value of double LTx compared with single LTx and for the purpose of organ allocation. For all patients who received a LTx at the Cleveland Clinic Lung Transplant Program, we analyzed spirometry performed uniformly in our pulmonary function laboratory. Our goal was to determine how much double LTx provides improved pulmonary function vs single LTx and to identify predictors of post-LTx pulmonary function.


   Patients and Methods
Top
 Abstract
 Introduction
 Patients and Methods
Results
 Comment
 Footnotes
 Acknowledgments
 References
 
Patients
From February 1990 to November 2005, 463 patients older than age 18 years underwent primary LTx for end-stage lung disease at Cleveland Clinic, exclusive of heart–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 (IRB), with patient consent waived.

Results of spirometry performed in the Cleveland Clinic’s certified pulmonary function laboratory, which conforms to the standards of the American Thoracic Society, were retrieved from the Pulmonary Function Test database [11]. The IRB approved supplemental review of medical records, also with patient consent waived. The mean age of patients at LTx was 48 ± 12 years (range, 18 to 71 years), and 50% were men (Table 1).


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  		Table 1 Recipient, Donor, and Transplant Details: Single Versus Double Lung Transplant
 
End Points
The two primary end points were (1) National Health and Nutrition Examination Survey (NHANES)-normalized postoperative forced expiratory volume in 1 second (FEV1; %) and (2) NHANES normalized postoperative forced vital capacity (FVC; %) [12]. There were 6,372 postoperative pulmonary function tests available for 379 patients (82% of total population). Patients who died before these tests were performed or whose records could not be located (18%) were excluded. Median postoperative data collection time was 1 year from LTx (range, 3 days to 14 years; Appendix Figures 1A–C*).


Figure 1A
Figure 1A
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  		Appendix Fig 1. Number of patients with spirometry measurements available at and beyond various time points, and number of spirometry measurements available for analysis. (Black bars = patients; grey bars = spirometry measurements.) (A) All patients. (B) Double-lung transplant patients. (C) Single lung transplant patients.

 
Data Analysis
In survival-type analyses, the temporal pattern of risk underlies the entire analysis. For example, risk of death is high immediately after an operation, falls to a lower level in the weeks and months thereafter, and rises steadily after that. Decades ago, Blackstone and colleagues [13] described a method to decompose time-to-event data into biologically meaningful hazard phases—early, constant, and late—each modulated by a separate group of risk factors. More recently, our group has developed a similar temporal decomposition method for binary [14], ordinal, and continuous longitudinal outcomes with the biologic motivation of discovering factors modulating various phases of the longitudinal pattern. Thus, we explicitly model the temporal pattern of repeated-measures longitudinal data and then search for modulators of that underlying pattern. This average, and modulated pattern, can then be portrayed graphically.

Temporal pattern
We characterized the temporal pattern of postoperative FEV1(%) and FVC(%) from time of LTx by this longitudinal analysis of repeated continuous measurements. A nonlinear mixed model was used to resolve multiple time phases to form a temporal decomposition model and to estimate shaping parameters of each phase.

Risk factors
Multivariable analysis was then performed to identify risk factors modulating each temporal phase. Preoperative and intraoperative variables used in this analysis are shown in the Appendix. Nonlinear mixed-model regression [14, 15] (SAS PROC NLMIXED, SAS Institute, Cary, NC) was used to implement the temporal decomposition model. Because of limited capability of PROC NLMIXED to explore multivariable relations, we initially screened variables using ordinary multivariable linear regression with entry and stay criteria of p ≤ 0.12 and p < 0.1. This analysis identified candidates for the multiphase nonlinear model. These candidates and their transformations, as required, were entered at once into the nonlinear multiphase model and then were eliminated one by one until all variables remaining had a p ≤ 0.1.

Presentation
Simple descriptive statistics were used to summarize the data. Continuous variables are presented as mean ± standard deviation and as 15th, 50th (median), and 85th percentiles. Categoric data are described using frequencies and percentages. The bootstrap percentile method was used to obtain 68% confidence limits (equivalent to ±1 standard deviation) for longitudinal estimates [16].


   Results
Top
 Abstract
 Introduction
 Patients and Methods
 Results
Comment
 Footnotes
 Acknowledgments
 References
 
Overall Trend in FEV1 and FVC
Estimated temporal values of post-LTx FEV1 (% of predicted) were 55%, 57%, 57%, 48%, and 48% at 3 months, 6 months, 1 year, 3 years, and 5 years (Fig 1A) and 58%, 62%, 64%, 60%, and 57% for FVC (Fig 1B). The value for FEV1 sharply increased up to 6 months post-LTx, decreased gradually to 3 years, then stayed relatively constant. Forced vital capacity sharply increased up to 1 year, decreased gradually to 5 years, then stayed relatively constant.


Figure 1
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  		Fig 1. Spirometry after lung transplantation. Solid lines represent parametric estimates of the mean spirometry values across time and are enclosed within 68% bootstrapped percentile confidence intervals (clashed lines). Solid circles are actual grouped data, without regard to repeated measurements, used as a crude verification of the model. (A) Forced expiratory volume in 1 second (FEV1, % of predicted). (B) Forced vital capacity (FVC, % of predicted).

 
Single Versus Double Lung Transplant
Postoperative FEV1 values for double LTx at 3 months, 6 months, 1, 3, and 5 years were 62%, 64%, 65%, 58%, and 59%, respectively, compared with 50%, 51%, 51%, 43%, and 40% for single LTx (Fig 2A). Postoperative FVC values for double LTx were 59%, 64%, 67%, 68%, and 66% compared with 57%, 60%, 62%, 56%, and 51% for single LTx at the same time intervals (Fig 2B). The double LTx group had higher postoperative FEV1 (p = 0.03) and FVC (p < 0.0001) than the single LTx group. In addition, there was a difference in temporal pattern of FEV1 and FVC. After double LTx, FEV1 and FVC increased sharply up to 1 year, decreased slightly, and then stayed relatively constant; after single LTx, FEV1 and FVC also increased up to 1 year, but then decreased continuously, with FEV1 gradually leveling out at approximately 5 years.


Figure 2
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  		Fig 2. Spirometry after single-lung (lower lines) and double-lung (top lines) transplantation (LTx). Format is as in Fig 1. Symbols are actual grouped data without regard to repeated measurements, used as a crude verification of the model. (Open circles = double LTx; diamonds = single LTx.) (A) Forced expiratory volume in 1 second (FEV1, % of predicted). (B) Forced vital capacity (FVC, % of predicted).

 
Factors Associated With Higher FEV1 and FVC After Transplantation
Patients undergoing double LTx for chronic obstructive pulmonary disease (COPD) or {alpha}-1 antitrypsin deficiency had the highest FEV1 and FVC, and those undergoing single LTx for these indications had the lowest FEV1 and FVC (Tables 2 and 3, Go Fig 3). Other diagnostic groups demonstrated benefit of double LTx that was intermediate between these extremes. Smaller age difference between recipient and donor and older recipient age were associated with higher FEV1 (Table 2).


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  		Table 2 Risk Factors Associated with Higher Postoperative Percentage of Predicted Forced Expiratory Volume in 1 Second
 

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  		Table 3 Risk Factors Associated with Higher Percentage of Predicted Postoperative Forced Vital Capacity
 

Figure 3
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  		Fig 3. Predicted mean spirometry values according to single lung vs double lung transplantation (LTx) and indication for transplant. ({alpha}-1 = {alpha}-1 antitrypsin deficiency; Bronch = bronchiectasis; CF = cystic fibrosis; COPD = chronic obstructive pulmonary disease; Eisen = Eisenmenger syndrome; IPF = idiopathic pulmonary fibrosis; PPH = primary pulmonary hypertension. (A) Forced expiratory volume in 1 second (FEV1, % of predicted). (B) Forced vital capacity (FVC, % of predicted).

 
For FVC, age difference (recipient–donor) appeared to have no effect after double LTx, whereas a smaller age difference in single LTx was associated with higher FVC. Higher preoperative FVC was associated with higher postoperative FVC (Table 3), with the influence slightly higher in the single LTx group.


   Comment
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
Footnotes
 Acknowledgments
 References
 
Postoperative pulmonary function is an important end point when transplant surgeons and physicians select single vs double LTx for a patient, but one on which only a few studies have focused [3, 17, 18]. Ideally, the benefits of double LTx should justify allocation of two lifesaving organs for a single patient from both a survival and functional perspective. However, the temporal pattern of spirometry after LTx in a large group of patients has not been well described, nor has the quantitative benefit of double LTx vs single LTx. We evaluated spirometry of patients who underwent LTx at Cleveland Clinic to determine how much improvement double LTx imparted over single LTx and what factors modulated the pattern of pulmonary function. We focused our evaluation on normalized FEV1 and FVC, the most commonly used objective measures of pulmonary function after LTx [8].

Overall Trend in FEV1 and FVC
Pulmonary function as measured by normalized FEV1 and FVC starts low but rises sharply in the initial months after transplantation, peaking between 6 months and 1 year. This early rise is likely due to multiple factors. The first is recovery from surgical trauma and chest wall pain: FEV1 and FVC may be diminished by as much as 40% after thoracotomy and take 4 months or more to recover [19]. The second is that the allograft is affected by ischemia–reperfusion injury, which may recover with time if it is not too severe [20]. Third, postoperative lung function also improves with ambulation and pulmonary rehabilitation [21]. Finally, diaphragms weakened by chronic respiratory failure before LTx dramatically recover strength starting 1 month after LTx and reach normal levels by 6 to 12 months [22]. Other studies have also demonstrated that lung function continues to improve for up to 1 year after LTx, although they were limited to patients transplanted for emphysema [3, 7].

Of interest is that FEV1 and FVC never approach 100% of predicted, but peak well below these values. Inability to achieve "normal" lung function is probably due to immune- and non-immune–mediated injury to the allograft before, during, and after implantation, from which it never completely recovers, as well as the added possibility of donor–recipient size mismatch [23, 24]. After this early peak, FEV1 and FVC decline continuously over the following 2 years before finally plateauing between years 3 and 5. This decline is also likely due to multiple factors, such as cumulative injury to the allograft from recurrent infection, aspiration, and chronic rejection [25].

Single Versus Double Lung Transplantation
Double LTx conferred some benefit over single LTx for both FEV1 and FVC at all time points. FEV1 and FVC peaked higher after double LTx than after single LTx. After this peak, FEV1 and FVC of patients undergoing double LTx decreased minimally; in contrast, spirometry of those undergoing single LTx continuously declined. More rapid decline in pulmonary function after single LTx may be explained by disease progression in the native lung through direct parenchymal destruction or mismatch of lung size and compliance between native lung and allograft.

Despite these findings favoring double LTx, the benefit of double LTx over single LTx was much smaller than expected, and at no point did spirometry approach double that of single LTx. The explanation for this is unclear. One reason may be that native lung continues to contribute to pulmonary function, as demonstrated by radiolabeled spirometry after single LTx [9]. Starobin and colleagues [26] showed that single LTx patients had 74% of perfusion to the transplanted lung and 26% to the native lung, demonstrating the native lung’s importance.

Another possible explanation for lower than expected FEV1 in double compared with single LTx might be that greater chest wall trauma caused by the double LTx impairs respiratory function, which never completely recovers. In addition, the longer ischemic time necessary to implant the second lung may cause more injury to the second lung, preventing it from reaching the same potential as the single LTx exposed to shorter ischemic time. This remains conjecture, although it is clear that the incremental value of a second lung in double LTx does not come close to doubling pulmonary function nor does it bring spirometry to normal values. In fact, this added value may not be clinically significant when focusing on spirometry as an end point.

Factors Associated with Higher FEV1 and FVC After Transplantation
Among diagnostic groups for transplantation, patients with COPD undergoing double LTx had the highest FEV1 and FVC. This may be related to chest size. Patients with emphysema have higher than predicted total lung capacity. Although donor lungs are sized to match the recipient’s predicted total lung capacity, transplanting into a hyperexpanded chest may account for the higher FEV1 and FVC in patients undergoing double LTx.

A surprising finding was that patients diagnosed with COPD who received a single lung had the lowest FEV1. This is likely accounted for by altered respiratory mechanics between allograft and native lung, which is prone to hyperexpansion [27]. Native lung and allograft inflate and empty at different rates, leading to chest wall asymmetry and mediastinal shift during respiration. Specifically, the mediastinum shifts toward the allograft during expiration, which likely accounts for the lower FEV1 and FVC measured after single LTx for emphysema [28]. In addition, asynchronous muscle force develops between the two sides of the chest after single LTx for emphysema that may exacerbate this effect [29]. Of importance was that all patients with a diagnosis of end-stage lung disease in our study had pulmonary function that was better after double than single LTx, demonstrating the value of double LTx.

For FEV1, a smaller age difference between recipient and donor demonstrated improved outcomes, as well as older recipient age, although this was not statistically significant for FVC after double LTx. The explanation is unclear and warrants further investigation. Physiologic changes occur in the lung and chest wall during aging and include costochondral calcification as well as changes in lung elastic recoil strength and distribution [30]. Optimal pulmonary function may be achieved when donor and recipient ages are matched for similarities in chest wall mechanics and pulmonary compliance. Of interest was that older patients obtained the most benefit of LTx as measured by FEV1, supporting its use in these patients.

Our study also showed that higher recipient preoperative FVC predicts higher postoperative FVC. This contrasts with Date and colleagues’ [23] study that suggested donor, rather than recipient, FVC was predictive of postoperative FVC. A combination of these two findings is likely correct, because a donor is chosen whose size most closely matches predicted size of the recipient’s chest. We are not able to explain the clinical significance of the other factors found to be associated with improved spirometry after LTx.

Limitations
A limitation of this study is that it represents the clinical experience of a single transplant center, with selection bias exercised when patients are chosen for single or double LTx. In addition, although we were able to show that patients undergoing single LTx had lower pulmonary function and a more rapid pattern of decay than patients undergoing double LTx, we can only hypothesize about the cause of this difference. Finally, we have not demonstrated that improved spirometry translates into improved survival, quality of life, or functional status, which is an important consideration. However, our study gives added insight into the post-LTx pulmonary function of a substantial cohort of patients with varied diagnoses who were studied over an extended period.

Conclusions
Double LTx provides better lung function, as measured by spirometry, than single LTx. The benefit of double LTx appears to endure and become more pronounced over time. We found the improvement in spirometry with double LTx to be surprisingly small, however, which calls into question its added clinical value. Although double LTx appears to be the procedure of choice to optimize spirometry, single LTx may be an appropriate option to maximize the number of patients who receive a transplant and to minimize deaths of patients on waiting lists. This seems particularly salient given that the survival benefit of double over single LTx, particularly for the diagnosis of idiopathic pulmonary fibrosis, has been difficult to demonstrate when controlling for other important clinical variables [31]. Further investigation into quality-of-life outcomes of patients undergoing double vs single LTx may help in making this decision. However, at this time, choosing two lungs over one on the basis of postoperative spirometry is not obvious, and a decision must be made while taking into consideration the need to derive maximal benefit from a scarce and lifesaving resource.


   Appendix
 
Variables Used in the Analyses

Recipient Variables

• Demographic: Age (years), sex, weight (kg), height (cm), body surface area (m2), body mass index (kg/m2), race
• Diagnosis: Idiopathic pulmonary fibrosis, chronic obstructive pulmonary disease, cystic fibrosis, {alpha}-1 antitrypsin deficiency, primary pulmonary hypertension, sarcoidosis, bronchiectasis, Eisenmenger syndrome, silicosis, lymphangioleiomyomatosis, bronchiolitis obliterans syndrome, scleroderma, retransplant
• Pulmonary function: Forced expiratory volume in 1 second (FEV1), forced vital capacity (FVC), FEV1 (% of predicted, National Health and Nutrition Examination Survey [NHANES] normalized), FVC (% of predicted, NHANES normalized); ratio: FEV1/FVC
• Comorbidities: Diabetes (insulin-dependent, non-insulin–dependent), hypertension, history of smoking, serum creatinine
• Serology, immunology: Blood type (A, AB, B, O, Rh+), panel reactive antibody exceeding 10%, cytomegalovirus serology, Epstein-Barr virus serology

Donor Variables

• Demographic: Age (years), sex, weight (kg), height (cm), body surface area (m2), body mass index (kg/m2), race
• Comorbidities: Hypertension, history of smoking, serum creatinine
• Serology, immunology: Blood type (A, AB, B, O, Rh+), cytomegalovirus serology, Epstein-Barr virus serology
• Cause of death: Anoxia, cerebral bleed, central nervous system tumor, cerebrovascular accident/stroke, head trauma, other
• Mismatch variables: Cytomegalovirus: donor–recipient mismatch; Epstein-Barr virus: donor–recipient mismatch; Rh: donor–recipient mismatch, ABO compatibility
• Procedure: Maximum ischemic time (minutes), single or double lung transplant


   Acknowledgments
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Footnotes
 Acknowledgments
References
 
We thank Kevin McCarthy, R-CPT, for providing pulmonary function data, Peter Kisuule, MS, for data management, Lucy Thuita, MS, for statistical programing, and Tess Parry, BS, for editorial assistance and manuscript preparation. This study was supported in part by the Peter and Elizabeth C. Tower and Family Endowed Chair in Cardiothoracic Research, James and Sharon Kennedy, the Slosburg Family Charitable Trust, and Stephen and Saundra Spencer (Dr Pettersson) and by the Kenneth Gee and Paula Shaw, PhD, Chair in Heart Research (Dr Blackstone).


   Footnotes
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Footnotes
Acknowledgments
 References
 
* The Appendix Figures 1A–C are available only online. To access them, please visit: http://ats.ctsnetjournals.org and search for the article by Mason, Vol. 85, pages 1193–1201.e1–2. Back


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

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  17. Meyers BF, Lynch JP, Trulock EP, Guthrie T, Cooper JD, Patterson GA. Single versus bilateral lung transplantation for idiopathic pulmonary fibrosis: a ten-year institutional experience J Thorac Cardiovasc Surg 2000;120:99-107.[Abstract/Free Full Text]
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  23. Date H, Aoe M, Nagahiro I, et al. How to predict forced vital capacity after living-donor lobar-lung transplantation J Heart Lung Transplant 2004;23:547-551.[Medline]
  24. Egan TM, Thompson JT, Detterbeck FC, et al. Effect of size (mis)matching in clinical double-lung transplantation Transplantation 1995;59:707-713.[Medline]
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