Matching donor to recipient in lung transplantation: How much does size matter?

Article Outline

• Abstract
• Patients and Methods
  • Patients
  • Total Lung Capacity
  • End Points
  • Follow-up
  • Data Analysis
    • Survival after transplant
    • Spirometry after transplant
    • Missing data
    • Data presentation
• Results
  • Effect of Donor Lung Size on Survival
  • Effect of Donor Lung Size on Spirometry
• Discussion
  • Effect of Donor Size on Survival
  • Effect of Donor Size on Spirometry
  • Limitations
• Conclusions
• Appendix A. Formulae for calculating predicted total lung capacity
• Appendix B. Variables used in multivariable analysis
  • Recipient
  • Donor
  • Transplant
• Figure E1. 
• References
• Copyright

Objective

The impact of size matching between donor and recipient is unclear in lung transplantation. Therefore, we determined the relation of donor lung size to 1) posttransplant survival and 2) pulmonary function as measured by forced expiratory volume in 1 second.

Methods

From 1990 to 2006, 469 adults underwent lung transplantation with lungs from donors aged 7 to 70 years. Donor and recipient total lung capacities were calculated using established formulae (predicted total lung capacity), and actual recipient lung size was measured in the pulmonary function laboratory. Disparity between donor and recipient lung size was expressed as a ratio of donor predicted total lung capacity to recipient predicted total lung capacity—the predicted total lung capacity ratio—and predicted donor total lung capacity to actual recipient total lung capacity—the actual total lung capacity ratio. Survival was measured by multiphase hazard methodology and repeated measures of National Health and Nutrition Examination Survey–normalized forced expiratory volume in 1 second analyzed by temporal decomposition.

Results

Predicted total lung capacity ratio and actual total lung capacity ratio ranged widely, from 0.55 to 1.59 and 0.52 to 4.20, respectively. Overall survival was unaffected by predicted total lung capacity ratio (P = .3) or actual total lung capacity ratio (P = .5). Patients with emphysema and an actual total lung capacity ratio of 0.67 or less or 1.03 or greater had higher predicted mortality (P = .01). During the first posttransplant year, forced expiratory volume in 1 second increased and then gradually declined. Predicted total lung capacity ratio and actual total lung capacity ratio had a small impact on forced expiratory volume in 1 second, primarily in the late phase after transplant in a disease-specific manner.

Conclusion

Size matching between donor and recipient using predicted total lung capacity ratio and actual total lung capacity ratio is an effective technique. Wide discrepancies in lung sizing do not affect overall posttransplant survival or pulmonary function. Therefore, a greater degree of lung size mismatch can likely be accepted, thereby improving patients' odds of undergoing transplantation.

CTSNet classification: 12

Abbreviations and Acronyms: aTLC, actual total lung capacity, aTLC_R, recipient actual total lung capacity, aTLC_Ratio, donor-to-recipient actual total lung capacity ratio, FEV1%, forced expiratory volume in 1 second, IPF, idiopathic pulmonary fibrosis, pTLC, predicted total lung capacity, pTLC_D, donor predicted total lung capacity, pTLC_Ratio, donor-to-recipient predicted total lung capacity ratio, TLC, total lung capacity

Transplant surgeons carefully evaluate donor lung size to optimize matching to a prospective recipient.¹, ², ³, ⁴ However, there is no consensus on the definition of best “size fit” or how to achieve it.⁵ Some surgeons size match using donor and recipient height values while taking into account recipient disease diagnosis.⁶, ⁷, ⁸ Our program and other transplant programs calculate donor and recipient total lung capacity (TLC) values and attempt to achieve as close a size match as possible. This technique considers the recipient's predicted TLC (pTLC) and actual TLC (aTLC), which can vary widely depending on the underlying diagnosis.⁴ To establish an optimal sizing strategy, we compared the ratio of donor-to-recipient TLC and evaluated its relation to 1) survival after lung transplantation and 2) postoperative spirometry values.

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Patients and Methods 

Patients 

From February 1990 to December 2006, 469 patients aged 18 years or older underwent primary lung transplantation 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, with patient consent waived. Results of spirometry performed in the Cleveland Clinic's certified pulmonary function laboratory, which conforms to American Thoracic Society standards, were retrieved from the Pulmonary Function Test database.⁹ The institutional review board approved supplemental review of medical records, also with patient consent waived. The mean age of patients at transplant was 48 ± 12 years (range 18–71 years), and 51% were men (Table 1).

Table 1. Recipient, donor, and transplant details (total n = 469)

Variable	n∗	No. (%) or Mean ± SD
Recipient
Demography
Female	469	232 (49)
Age at transplant (y)	469	48 ± 12
Body mass index (kg/m−2)	468	24 ± 5.3
Diagnosis
Emphysema	469	228 (49)
Bronchiectasis	469	88 (19)
IPF	469	81 (17)
PAH	469	29 (6.2)
Pulmonary function
FEV1 (% of predicted)†	345	28 ± 16
FVC (% of predicted)†	345	50 ± 16
FEV1/FVC†	345	0.6 ± 0.36
Pulmonary diffusing capacity	200	28 ± 4.02
Immunology
PRA > 10%	467	18 (3.9)
Hemodynamics
6-min walk (ft)	203	1150 ± 276
PA systolic pressure (mm Hg)	294	43 ± 20
PA diastolic pressure (mm Hg)	293	21 ± 11
PA mean pressure (mm Hg)	276	29 ± 14
Central venous pressure (mm Hg)	219	7.6 ± 4.8
Cardiac index (L/min/m2)	259	2.9 ± 0.79
Wedge pressure (mm Hg)	234	12 ± 6.0
Donor
Demography
Female	467	234 (50)
Pediatric donor age < 18 y	464	56 (12)
Age at transplant (y)	464	36 ± 15
Comorbidity
Smoking	116	62 (53)
Cause of death
Head trauma	469	197 (42)
Transplant
Double lung	469	197 (42)
Maximum ischemic time (min)	395	224 ± 70

FEV1, Forced expiratory volume in 1 second; FVC, forced vital capacity; IPF, idiopathic pulmonary fibrosis; PA, pulmonary artery; PAH, pulmonary arterial hypertension; PRA, panel reactive antibody; SD, standard deviation.

Total Lung Capacity 

aTLC is measured by plethysmography and affected by underlying pulmonary disease, whereas pTLC is calculated using a formula that incorporates age, gender, height, and weight.¹⁰, ¹¹ Formulas believed to be most accurate for pTLC were used in this analysis (Appendix A). aTLC of potential recipients was available in 309 patients (66%). It was not feasible to measure aTLC in donors.

Patients with emphysema (α-1 antitrypsin deficiency and chronic obstructive pulmonary disease) had a larger aTLC than pTLC, with idiopathic pulmonary fibrosis (IPF) smaller than predicted; for bronchiectasis and cystic fibrosis, these values were similar (Figure 1). In addition, pTLC_Ratio was calculated by dividing donor pTLC (pTLC_D) by recipient pTLC (pTLC_R) to evaluate matching to predicted lung size. Similarly, TLC_Ratio was calculated by dividing pTLC_D by recipient aTLC (aTLC_R) to evaluate matching to actual lung size.

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• Figure 1. 

  Distribution of differences in aTLC versus pTLC by diagnosis. PAH, Pulmonary arterial hypertension; IPF, idiopathic pulmonary fibrosis; aTLC, actual total lung capacity; pTLC, predicted total lung capacity.

Donor pTLC ranged from 2.37 to 8.56 L, median 5.49 L (15th and 85th percentiles 4.73–7.38), and recipient pTLC ranged from 3.49 to 8.69 L, median 5.75 L (15th and 85th percentiles 4.73–7.07). pTLC_Ratio ranged from 0.55 to 1.59, median 1.0 (15th and 85th percentiles 0.87–1.13). There was only small variation across disease diagnoses (Table 2; Figure 2, A). aTLC_Ratio ranged from 0.52 to 4.20, median 0.96 (15th and 85th percentiles 0.71–1.84). There was considerable variation of aTLC_Ratio across recipient diagnoses, with emphysema having the smallest aTLC_Ratio and IPF having the largest, and bronchiectasis again falling in between (Table 2, Figure 2, B).

Table 2. Estimated donor-to-recipient total lung capacity by diagnosis

Diagnosis	No.	Mean ± SD	Range
pTLCRatio
Emphysema	226	1.01 ± 0.14	0.56–1.59
Bronchiectasis	86	1.01 ± 0.13	0.59–1.27
PAH	28	1.06 ± 0.19	0.72–1.53
IPF	80	0.95 ± 0.14	0.55–1.25
Other	42	0.98 ± 0.19	0.56–1.56
aTLCRatio
Emphysema	152	0.84 ± 0.17	0.52–1.41
Bronchiectasis	52	1.13 ± 0.35	0.62–2.24
PAH	13	1.23 ± 0.27	0.84–1.77
IPF	57	1.93 ± 0.70	0.73–4.20
Other	29	1.53 ± 0.69	0.64–2.97

aTLC_Ratio, Donor-to-recipient actual total lung capacity ratio; IPF, idiopathic pulmonary fibrosis; PAH, pulmonary arterial hypertension; pTLC_Ratio, donor-to-recipient predicted total lung capacity ratio; SD, standard deviation.

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• Figure 2. 

  Cumulative distribution of donor-to-recipient TLC according to diagnosis. A, Donor-to-recipient pTLC_Ratio. B, Donor-to-recipient aTLC_Ratio. IPF, Idiopathic pulmonary fibrosis; pTLC_Ratio, donor-to-recipient predicted total lung capacity ratio; aTLC_Ratio, donor-to-recipient actual total lung capacity ratio.

End Points 

The 3 primary end points were 1) overall and 2) disease-specific survival and 3) National Health and Nutrition Examination Survey–normalized postoperative forced expiratory volume in 1 second (FEV1%).¹² Postoperative spirometry became available electronically in 1994. Thus, among 382 of 469 patients (81%), 7673 FEV1% values were retrieved. Median postoperative data collection time was 16 months from transplant (range 3 days to 15 years; Figure E1). These data were considered reliable for estimating temporal pattern of FEV1% to at least 6 years.

Follow-up 

Anniversary follow-up as of April 24, 2007, was used for the analyses. Fourteen patients (3%) were transferred at various times to outside institutions and lost to follow-up. All patients had at least 1 year of follow-up, with 1605 patient-years of data available for analysis. Median follow-up among survivors was 3.5 years (mean 4.5 ± 3.1 years); 25% were followed at least 5.9 years, and 10% were followed at least 8.8 years.

Data Analysis 

Survival was estimated nonparametrically by the Kaplan–Meier method and parametrically by hazard function methodology.¹³ Bagging was used to identify reliable risk factors from among those listed in Appendix B on the basis of 1000 bootstrap samples and automated stepwise selection, with a variable-retention criterion of P ≤ .05.¹⁴ Then, the factor of interest, pTLC_Ratio or aTLC_Ratio, was entered into the model to analyze its effect. In the multivariable analysis, sporadic missing values for variables were imputed with the mean value.

Repeated measurements of FEV1% were analyzed longitudinally across time for temporal trends after transplantation. A nonlinear mixed model with decomposition of time phases was used to model the temporal trend. A temporal trend was separately identified for the 3 largest diagnostic groups: emphysema, bronchiectasis, and IPF. To assess the effect of pTLC_Ratio and aTLC_Ratio, the rate was incorporated first into a model with only double versus single lung transplantation and then into a model containing other patient factors previously found to affect postoperative spirometry values.¹⁵

Data fields missing more than 30% of values were excluded from the analysis, except pulmonary artery pressures and 6-minute walk, despite more than 30% of values being missing. In addition, because patients were sometimes unable to breathhold, aTLC was unmeasured. Therefore, multiple imputation was used in multivariable analyses to maximize the number of patients available in each analysis. Bootstrapping was performed on the first imputation, and the final model underwent 5 imputation cycles before aggregating results.

Continuous variables are summarized by mean ± standard deviation, and categoric variables are summarized by frequencies and percentages. All analyses were performed with SAS statistical software (SAS v9.1; SAS Inc, Cary, NC).

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Results 

Effect of Donor Lung Size on Survival 

Unadjusted survival at 6 months and 1, 3, and 5 years was 87%, 79%, 62%, and 45%, respectively. The hazard function resolved into 2 phases; 47 deaths occurred in the early phase, and 207 deaths occurred in the longer late phase. In multivariable analysis, pTLC_Ratio did not reliably predict overall survival (Figure 3) or survival when analyzed for each separate disease diagnosis (Table 3). aTLC_Ratio also was not associated with overall survival. However, when the 3 most common disease diagnoses were analyzed separately, only patients with emphysema receiving lungs from donors at either extreme of lung size (aTLC_Ratio < 0.67 and > 1.03, representing the top and bottom 15% of values) had poorer survival than the 70% within the range 0.67 to 1.03 (Figure 4).

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• Figure 3. 

  Overall unadjusted survival by terciles of donor-to-recipient pTLC_Ratio. Symbols represent deaths. Vertical bars represent 68% confidence limits equivalent to ± 1 standard error. Numbers in parentheses represent patients remaining at risk (P [log-rank] = .4). o = patients with largest 15% of pTLC_Ratio. • = patients with the middle 70% of pTLC_Ratio. □ = patients with the smallest 15% of pTLC_Ratio.

Table 3. Risk factors for mortality

Risk factor	Estimate ± SE	P	Reliability (%)∗
Early hazard phase
Higher PA diastolic pressure†	0.11 ± 0.03	.002	63
Earlier date of operation	−0.25 ± 0.06	<.0001	93
Late hazard phase
PRA >10 %	0.98 ± 0.32	.002	73
Recipient blood type A	0.30 ± 0.15	.04	52
CPB not used	0.45 ± 0.21	.03	53
pTLCRatio‡	1.50 ± 1.37	.3	11
Emphysema	1.86 ± 1.60	.3	22
IPF	2.62 ± 1.87	.2	22
Bronchiectasis	2.12 ± 1.65	.2	22
Interaction: emphysema · TLCRatio‡	−1.19 ± 1.50	.4	22
Interaction: IPF · pTLCRatio‡	−1.92 ± 1.73	.3	23
Interaction: bronchiectasis · pTLCRatio‡	−1.27 ± 1.55	.4	53

CPB, Cardiopulmonary bypass; IPF, idiopathic pulmonary fibrosis; PA, pulmonary artery; PRA, panel reactive antibody; pTLC_Ratio, donor-to-recipient predicted total lung capacity ratio; SE, standard error.

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• Figure 4. 

  Unadjusted survival in patients with emphysema stratified by donor-to-recipient aTLC_Ratio. o = patients with extreme values of aTLC_Ratio (n = 44). □ = the 70% of patients with more typical values (n = 108). Format is as in Figure 3. P (Wilcoxon) = .01.

Effect of Donor Lung Size on Spirometry 

The temporal trend of FEV1% after transplantation demonstrated an early peaking phase followed by a slowly rising late phase. FEV1% remained relatively constant thereafter, with some slow decline over time.

Neither pTLC_Ratio nor aTLC_Ratio had an overall effect on postoperative FEV1%. However, when analyzed by specific disease diagnoses (Table 4), 1) a larger pTLC_Ratio and smaller aTLC_Ratio predicted a slightly higher FEV1% early after transplantation for emphysema, but had no late effect (Figure 5, A and B); 2) a smaller pTLC_Ratio and smaller aTLC_Ratio predicted higher FEV1% in the late phase after transplantation for IPF (Figure 6, A and B); and 3) a larger pTLC_Ratio predicted higher FEV1% in the early phase but lower FEV1% in the late phase in patients undergoing transplantation for bronchiectasis, and a smaller aTLC_Ratio predicted higher FEV1% in the late phase (Figure 7, A and B).

Table 4. Effect of total lung capacity ratio on mean postoperative forced expiratory volume in 1 second after controlling for other patient factors,^∗ according to diagnosis

aTLC_Ratio, Donor-to-recipient actual total lung capacity ratio; IPF, idiopathic pulmonary fibrosis; pTLC_Ratio, donor-to-recipient predicted total lung capacity ratio; SE, standard error.

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• Figure 5. 

  Predicted mean FEV1% after lung transplantation for emphysema from multivariable model of Table 4. A, Individual curves represent specific values of donor-to-recipient pTLC_Ratio. B, Individual curves represent specific values of donor-to-recipient aTLC_Ratio. FEV1%, Forced expiratory volume in 1 second; pTLC_Ratio, donor-to-recipient predicted total lung capacity ratio; aTLC_Ratio, donor-to-recipient actual total lung capacity ratio.

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• Figure 6. 

  Predicted mean FEV1% after lung transplantation for IPF from multivariable model of Table 4. A, Individual curves represent specific values of donor-to-recipient pTLC_Ratio. B, Individual curves represent specific values of donor-to-recipient aTLC_Ratio. FEV1%, Forced expiratory volume in 1 second; pTLC_Ratio, donor-to-recipient predicted total lung capacity ratio; aTLC_Ratio, donor-to-recipient actual total lung capacity ratio.

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• Figure 7. 

  Predicted mean FEV1% after lung transplantation for bronchiectasis from multivariable model of Table 4. A, Individual curves represent specific values of donor-to-recipient pTLC_Ratio. B, Individual curves represent specific values of donor-to-recipient aTLC_Ratio. FEV1%, Forced expiratory volume in 1 second; pTLC_Ratio, donor-to-recipient predicted total lung capacity ratio; aTLC_Ratio, donor-to-recipient actual total lung capacity ratio.

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Discussion 

Effect of Donor Size on Survival 

The Cleveland Clinic sizing strategy is universal across diseases and factors in 2 sequential components related to TLC when sizing donor to recipient. The first component attempts to closely match pTLC of donor and recipient. Although this was achieved, a few patients in all disease categories received lungs that were markedly oversized and undersized, as shown by the wide range of pTLC_Ratio. However, there was minimal survival impact of pTLC_Ratio, suggesting that wider size discrepancies can be accepted.

The second aspect of the sizing strategy comes into play when exact matching by pTLC_Ratio is not possible. Donor size is then targeted to achieve a pTLC_D that is between aTLC_R and pTLC_R. This approach factors in disease-specific chest remodeling. Interestingly, the aTLC_Ratio was found to have no effect overall on survival. However, when considered according to underlying disease, patients with emphysema who received organs at the extremes of aTLC_Ratio had worse survival: aTLC is larger than pTLC in patients with emphysema.¹⁶ When selecting an allograft for a patient with emphysema, lung size should be smaller than aTLC to improve respiratory mechanics, similar to what is achieved with lung volume reduction surgery.¹⁷, ¹⁸, ¹⁹ Transplanting a lung that is so large that it approximates the size of the hyperinflated lung likely produces inefficient respiratory mechanics and contributes to diminished long-term survival.⁴ Downsizing of donor lungs has been described for smaller recipients.²⁰, ²¹ However, the amount of size mismatch that mandates downsizing and the amount of size reduction that should be performed are not clear. For this reason, downsizing has not been practiced at Cleveland Clinic. Our data suggest that wide discrepancies in size matching can be accepted without downsizing and that this practice should be rare. However, a patient with emphysema would be the best candidate for an oversized lung (greater than the aTLC).

At the other extreme, mechanisms of chest remodeling for an undersized allograft, such as diaphragmatic elevation, alterations in the bony thorax, and mediastinal shift, may have a maximal range of compensation.¹⁸ At this point, residual space problems, such as persistent pneumothorax, intractable pleural effusions, and empyema, may negatively affect survival.²², ²³, ²⁴

Effect of Donor Size on Spirometry 

Neither pTLC_Ratio nor aTLC_Ratio affected overall postoperative FEV1%, supporting previous findings that donor lung size has minimal effect on lung function after transplantation.¹, ⁸, ²⁵ However, there were disease-specific differences. For emphysema, early effects favored a larger pTLC_Ratio, but long-term spirometry was minimally affected. For IPF, a smaller pTLC_Ratio produced better long-term spirometry, and for bronchiectasis, a larger pTLC_Ratio predicted better early spirometry but worse late spirometry. Similar trends were noted for the aTLC_Ratio. Although statistically significant, it seems unlikely that the small differences in spirometry within differing donor-to-recipient size ratios are clinically important.

Limitations 

The primary limitation of this study is its retrospective nature. In addition, the mechanisms behind the findings can only be postulated. End points were limited to survival and spirometry. Finally, the sizing strategy used during the time frame of this study focused on minimizing size mismatch and was not designed to address extremes of tolerable size discrepancy. Exceptions made to the standard sizing strategy that resulted in mismatch extremes were surgeon specific, and the rationale was impossible to ascertain retrospectively.

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Conclusions 

Transplant surgeons turn down organs that are believed to be too large or too small for a recipient. Some even “downsize” lungs that they believe are too large in an effort to increase organ use.¹, ², ³, ²⁶ It is not clear when this is necessary or to what extent this strategy is helpful, and underlying disease diagnosis compounds the uncertainty.¹⁰ Should a donor lung be selected that is similar in size to the diseased lung or more closely approximates the nondiseased condition? The sizing strategy that has been analyzed considers these factors and seems effective. The results suggest that wide size discrepancies can be accepted without adverse effect, which may improve a patient's odds of undergoing transplantation.

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Appendix A. Formulae for calculating predicted total lung capacity 

Male patients aged < 18 y

(38.1842 · age + 23.0973 · height + 44.5411 · weight−2236.7774) ÷ 1000

Female patients aged < 18 y

(13.0601 · age + 40.4346 · height + 14.526 · weight−3495.2291) ÷ 1000

Male patients aged > 18 y

0.08 · height + 0.003 · age−7.333

Female patients aged > 18 y

0.059 · height−4.537

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Appendix B. Variables used in multivariable analysis 

Recipient 

Demography: Female, Caucasian, African-American, age, body mass index, body surface area, weight · height

Diagnosis: Idiopathic pulmonary fibrosis, emphysema, bronchiectasis

Comorbidity: Diabetes, hypertension, creatinine

Pulmonary function: FEV1%, NHANES normalized; FVC%, NHANES normalized; FEV1%/FVC% ratio, actual total lung capacity, predicted total lung capacity, donor-to-recipient actual total lung capacity ratio, donor-to-recipient predicted total lung capacity ratio

Serology/immunology: Blood type A, blood type AB, blood type B, blood type O, Rh+, panel reactive antibody >10%, CMV serology

Hemodynamics: 6-minute walk, systolic blood pressure, diastolic blood pressure, mean blood pressure, pulmonary artery systolic pressure, pulmonary artery diastolic pressure, pulmonary artery mean pressure

Donor 

Demography: Female, Caucasian, African-American, pediatric donor, age at transplant, body mass index, body surface area, weight · height

Comorbidity: History of hypertension, creatinine

Pulmonary function: Estimated total lung capacity

Serology/immunology: Blood type A, blood type B, blood type O, Rh+, CMV

Cause of death: Anoxia, cerebral bleeding, stroke, head trauma

Mechanism of death: Blunt injury, gunshot wound, ischemic/stroke

Transplant 

Procedure: Double lung transplantation, right lung transplantation only, left lung transplantation only, cardiopulmonary bypass, time from January 1, 1990, to index operation, maximum ischemic time

Donor–recipient mismatch: Donor male and recipient male; donor female and recipient female; donor male and recipient female; donor female and recipient male; CMV: donor–recipient mismatch; RH: donor–recipient mismatch; ratio of donor-to-recipient age

FEV1%, Forced expiratory volume in 1 second; FVC%, forced vital capacity; NHANES, National Health and Nutrition Examination Survey; CMV, cytomegalovirus.

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Figure E1. 

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• Number of patients with spirometry measurements available at and beyond various time points, and number of spirometry measurements available for analysis (black bars, spirometry measurements; grey bars, patients).

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