Pressure to expand the donor pool has affected all

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1 Effect of Donor Age and Ischemic Time on Intermediate Survival and Morbidity After Lung Transplantation* Dan M. Meyer, MD; Leah E. Bennett, PhD; Richard J. Novick, MD; and Jeffrey D. Hosenpud, MD Background: Pressure to expand the donor pool has required the use of lungs from older donors or from more-distant procurement areas. The long-term consequences of this policy have not yet been fully addressed. The effect of donor age and donor ischemic time on intermediate survival and important secondary end points after lung transplantation was therefore examined. Methods: A cohort of 1,800 lung transplant recipients with complete 2-year follow-up, operated on in the United States between April 1, 1993, and March 31, 1996, was studied to assess survival. For analysis of secondary end points, the cohort was limited to 1,450 patients. Results: Donor age when analyzed independently did not significantly affect intermediate survival (p 0.4). Secondary end points were also not affected by age, with the exception of the incidence of hospitalization for rejection in the univariate analysis (p 0.02) and in the multivariate analysis (p 0.04). Moreover, there was not a significant impact of donor age or ischemic time independently on survival in the multivariate analysis. Similarly, when the interaction between ischemic time and donor age was examined in all of the multivariate models, none of the secondary end points were found to be significantly influenced. However, the combined interaction between donor age and ischemia time demonstrated a significantly worse survival at 2 years (p 0.02) with donor age of > 50 years and donor ischemic time > 7h. Conclusions: Donor age and donor ischemic time did not independently influence survival or important secondary end points after lung transplantation. However, intermediate-term survival was affected by the use of older donors when combined with a prolonged ischemic time. The impact of this combination should be considered when attempting to expand the donor pool. (CHEST 2000; 118: ) Key words: donor age; ischemic time; lung transplantation Abbreviation: UNOS United Network for Organ Sharing Pressure to expand the donor pool has affected all types of organ transplantation, including lung transplantation. The procurement of adequate pulmonary grafts is even more problematic than is seen with cardiac transplantation, as only 15 to 20% of multiple organ donors have lungs acceptable for transplantation by current criteria. 1 Consequently, many centers have begun to use lungs from older *From the Division of Thoracic and Cardiovascular Surgery (Dr. Meyer), University of Texas Southwestern Medical Center at Dallas, TX; UNOS/ISHLT Registry (Dr. Bennett), Richmond, VA; London Health Sciences Centre (Dr. Novick), London, Ontario, Canada; and St. Luke s Medical Center (Dr. Hosenpud), Milwaukee, WI. Manuscript received December 9, 1999; revision accepted May 2, Correspondence to: Dan M. Meyer, MD, Department of Surgery, Division of Thoracic and Cardiovascular Surgery, University of Texas Southwestern Medical Center, 5323 Harry Hines Blvd, Dallas, TX ; dan.meyer@ .swmed.edu donors or from more-distant procurement sites. Although this strategy will certainly increase the number of available donors, the safety of this practice has not been validated. Extension of the typical donor criteria for lung procurement raises concerns based on the already suboptimal intermediate-term results in this transplant population. 2 Whether these results are related to inadequate preservation or to multiple factors present in the postoperative period remains to be determined. Clearly, less information regarding adequate preservation methods is available for lungs than for other solid organs. Moreover, the use of older donors raises concern regarding graft durability and long-term function. Additionally, the extension of donor ischemic time may increase the tendency toward development of a more significant reperfusion injury, an event that could affect both CHEST / 118 / 5/ NOVEMBER,

2 immediate- and long-term graft function and survival. Consequently, transplant clinicians have often demanded near optimal conditions before accepting a pulmonary donor. The problem remains, however, that in 1997, there were 4,224 patients waiting on the United Network for Organ Sharing (UNOS) lung transplantation list and only 904 adequate donors, with approximately 9.8% of patients dying while waiting for transplantation (Leah E. Bennett, PhD; personal communication; UNOS Registry; April 1998). As a result, many centers have attempted to expand the donor pool by using lungs from older donors or procured from distant sites. Although the early results of this strategy have been reported, 3 the longterm consequences of this policy have not yet been fully assessed. This study was designed to determine whether intermediate-term survival and secondary end points such as rejection, bronchiolitis obliterans, pulmonary function, airway complications, or infections were affected by donor age or donor ischemic time. Materials and Methods All adult patients undergoing lung transplantation in the United States between April 1, 1993, and March 31, 1996, recorded in the UNOS Registry were included in this study. In the United States, 2,140 lung transplantations were performed in adult recipients using organs from cadaveric donors. Cohorts were reduced to have complete data sets for both the survival and secondary end point analyses. To assess survival, a cohort of 1,800 patients was used. For analysis of secondary end points, the cohort was further limited to include only those transplants with a follow-up form submitted during either the discharge to 1-year posttransplant time period or between the 1-year and 2-year posttransplant time periods. This requirement to have complete data at one point in the follow-up period for the secondary end points reduced the cohort to 1,450 patients. The results recorded for the secondary end points were weighted to account for incomplete follow-up in an attempt to reduce the bias from incomplete observations. Specifically, if a follow-up form was submitted at 6 months and the patient had not yet been hospitalized for rejection, the outcome would be No rejection but the observation would receive a weight of only one half (6 mo/1 yr) to indicate that they had not been observed for the entire time period. Similar weights were used in the multivariate analyses. Patients were classified into groups by both donor age and donor ischemic time. The patient groups stratified by donor age were divided into three groups: 45 years, 45 to 55 years, and 55 years. Age was also analyzed separately as a continuous variable. Donor ischemic time was also separated into three intervals: 4h,4to6h,and 6 h. Similarly, ischemic time was also analyzed as a continuous variable. Patient survival was examined at 1 and 2 years after transplantation; secondary end points, including hospitalization for rejection, development of bronchiolitis obliterans, pulmonary function (FEV 1 ), bronchial stricture formation, and hospitalization for infection, were also examined at the two times. Statistical Analysis Actuarial survival was calculated using Kaplan-Meier methods. 4 Univariate comparisons between groups were made with the 2 test for categorical outcomes or Fisher s Exact Test if small sample size, the z test for survival rates, and an analysis of variance for continuous outcomes. The impact of donor age and ischemic time on survival and secondary end points was assessed using multivariate logistic regression analysis. 5 An odds ratio of each candidate variable (donor age, donor ischemic time) was calculated to evaluate differences between groups in survival and secondary end points. Interactions between donor age and ischemic time (all linear and quadratic combinations) were examined in all of the multivariate models. If a candidate variable appeared to significantly influence outcome by univariate analysis at the p 0.10 level, it was retained for the model (see Appendix). Overall outcomes were considered significantly different at the p 0.05 level. Demographics Results The analyses of survival were based on the reduced cohort (n 1,800) of adult transplant patients with complete data. For analysis of secondary end points, the cohort was limited to those transplant patients with a follow-up form submitted during either the discharge to 1-year posttransplant period or between the 1-year and 2-year posttransplant periods. This requirement reduced the cohort for the secondary end points analyses to the 1,450 patients who underwent lung transplantation between April 1, 1993, and March 31, The average recipient age was years, with the average donor age being years; 46.8% of the recipients were male, whereas 68.1% of the donors were male. The primary diagnosis of the recipient group was emphysema or COPD in 43.3%, cystic fibrosis in 13.3%, idiopathic pulmonary fibrosis in 11.7%, 1 -antitrypsin deficiency in 10.9%, primary pulmonary hypertension in 7.3%, and Eisenmenger s syndrome in 2.3%. Recipient demographics are tabulated for each of the donor age groups and ischemic time groups in Tables 1, 2, respectively. There was no relationship between donor age and type of transplant procedure performed. Further preoperative and operative categorical and continuous variables used in the multivariate analyses are listed in Tables 3, 4, respectively. Survival Neither donor age nor ischemic time, independently, had an impact on intermediate survival in either univariate (Fig 1, 2) or multivariate analyses. However, the interaction of donor age and ischemic time was significant in the multivariate logistic regression analysis at 2 years, with older donor organs 1256 Clinical Investigations

3 Table 1 Demographics Stratified by Donor Age (N 1,450)* Table 3 Patient Preoperative and Operative Categorical Variables Used in Multivariate Analyses* Donor Age Full Population Study Population Characteristics experiencing long ischemic times having the worst odds of survival (Fig 3). The strongest effect was seen in donors 55 years old with ischemic times 7h. Secondary End Points Table 2 Demographics Stratified by Donor Ischemic Time (N 1,450)* Characteristics 45 yr (n 1,258) 4h (n 627) yr (n 169) Donor Ischemic Time 4 6 h (n 578) 55 yr (n 23) Recipient age, yr Recipient sex, % male Recipient diagnosis, % Emphysema/COPD Cystic fibrosis IPF Antitrypsin PPH Retransplant/graft loss Other lung diseases Other diseases *Data are presented as mean SEM unless otherwise indicated. IPF idiopathic pulmonary fibrosis; PPH primary pulmonary hypertension. Denotes significant difference between age groups by 2 analysis, p h (n 245) Recipient age, yr Recipient sex, % male Recipient diagnosis, % Emphysema/COPD Cystic fibrosis IPF Antitrypsin PPH Retransplant/graft loss Other lung diseases Other diseases *Data are presented as mean SEM unless otherwise indicated. See Table 1 footnote for abbreviations. Denotes significant difference by analysis of variance at p Variables No. % No. % Donor sex Female Male 1, Cigarette use Unknown None History/continued Recipient sex Female Male Diagnosis Other Congenital heart disease Primary pulmonary hypertension Cystic fibrosis Other lung disease Idiopathic pulmonary fibrosis 1 -Antitrypsin deficiency COPD Prior transplant No 1, Yes Medical condition In ICU In hospital (not ICU) Not hospitalized 1, , Receiving life support No 1, , Yes Receiving mechanical ventilation No 1, , Yes Transplant type Lobar Single 1, BSL Sex mismatch Sex mismatch 1, Sex match Donor-recipient ABO match ABO identical 1, , ABO compatible ABO incompatible Patient status Alive 1, , Dead *BSL bilateral sequential lung. Univariate analyses were used to examine the impact of donor age and ischemic time on secondary end points. Overall, there did not appear to be a significant effect on the incidence of hospitalization for rejection, the incidence of bronchiolitis obliterans, the postoperative FEV 1, the incidence of bronchial stricture formation, or the incidence of hospitalization for infection (Table 5). This was confirmed at both the 1- and 2-year time points. There were two exceptions, as there was a significant difference in the incidence of hospitalization for rejection at 1 CHEST / 118 / 5/ NOVEMBER,

4 Table 4 Patient Preoperative and Operative Continuous Variables Used in Multivariate Analyses* Cohort Variables Data Full population (n 1,800) Ischemic time, h 4.49 (1.77; 0 12) Recipient age, yr (12.06; 18 70) Donor age, yr (12.36; 7 66) Study population (n 1,450) Ischemic time, h 4.44 (1.74; 0 12) Recipient age, yr ; Donor age, yr (12.04; 7 62) *Data are presented as mean (SD; range). n 1,798. year among the donor age groups, and the postoperative FEV 1 differed by donor ischemic time groups at both 1 year and 2 years (Table 6). When these secondary end points were examined in multivariate analyses, only the incidence of hospitalization for rejection at 1 year was affected by donor age or ischemic time. Patients receiving an organ from an older donor were less likely to be hospitalized for rejection by 1 year (Fig 4, p 0.04). FEV 1, which in the univariate analysis was shown to be significantly greater with increasing ischemic time, was analyzed with a multivariate model that considered the type of procedure performed (either single or bilateral sequential lung transplant). With this factor taken into account, the FEV 1 no longer achieved statistical significance. Interactions between donor age and ischemic time (all linear and quadratic combinations) were examined in all of the multivariate models, but none were determined to be significant in any of the models for secondary end points. Donor age was also shown to be a risk factor in the bronchiolitis obliterans model at 2 years, although in this model age was grouped. using older donors, even if revascularization techniques were required, with a 1-year actuarial survival of 84%. At 1 year, left ventricular function and the incidence of infection and rejection were equal between the older ( 45 years) and younger ( 45 years) age groups. Moreover, the actuarial survival and the development of transplant-associated coronary disease were similar in both groups up to 5 years after transplantation. In contrast, others have shown that transplant recipients who received hearts from donors 50 years old had an increased mortality. 13,14 Studies assessing the effect of donor ischemic time on cardiac allograft function and survival have shown significant myocardial fibrosis 15 and worse early survival 16 with increasing donor ischemic time. Extension of the age limit criteria for lung donors has evolved much less rapidly, likely secondary to the perceived fragile nature of the pulmonary allograft. Lungs from older donors may be more sensitive to the preservation process and more significantly affected by reperfusion injury. Durability of the graft is another factor, with the long-term effects on pulmonary function, propensity for rejection (acute or chronic), or adequacy of airway healing all unknown issues. Moreover, older donors may have intrinsic lung problems such as emphysema from prior or current tobacco exposure, or occult carcinomas. As a result of the uncertainty regarding the safety of using older donors, this study was undertaken to evaluate the effect of donor age and ischemic time on intermediate survival and secondary end points. These data demonstrated no significant independent effect of donor age on survival. Although the univariate analysis comparing patient survival with donor age alone (Fig 1) appeared to show a significant difference in the early follow-up period, this did not reach statistical significance in either the univariate or multivariate analyses. This reflects the power of Discussion Attempts at expanding the donor pool have been applied to most solid organs, including the lung. In thoracic transplantation, strategies to secure more potential donors have included invasive preoperative monitoring and intervention, 6 relaxation of donor acceptance criteria, 7 revascularization of organs with significant coronary stenosis, 8 lobar lung transplantation, 9 and more recently, consideration for the use of nonbeating heart donors. 10 Few studies to date have addressed the issue of older donor use in pulmonary transplantation. 11,12 The use of older donors in cardiac transplantation has proven instructive, although controversial. Studies by Drinkwater et al 8 showed excellent results Table 5 Donor Age Group Analysis of Secondary End Points* Outcomes Time Point, yr 45 yr (n 1,258) Donor Age yr (n 169) 55 yr (n 23) Hospitalized for rejection Bronchiolitis obliterans FEV Bronchial stricture Hospitalized for infection *Data are presented as percent Clinical Investigations

5 Figure 1. Patient survival after lung transplantation stratified by donor age. multivariate analyses, as other factors may be influencing the outcomes. Perhaps a larger patient population of older donors may have changed these findings. Moreover, most of the secondary end points evaluated (incidence of infections, bronchiolitis obliterans, FEV 1, or bronchial stricture formation) were not influenced by donor age. Similarly, prolonged ischemic times did not independently affect intermediate survival or any of the selected secondary end points (with the exception of FEV 1 in the univariate analysis). Only the interaction between donor age and donor ischemic time demonstrated a negative influence on intermediate-term survival. The older donor (age 55 years) combined with a prolonged ischemic time ( 7 h) predicted decreased survival at 2 years. The only secondary end point that showed any effect from donor factors was rejection at 1 year, with decreasing odds ratio with increased donor age. The reason for this is speculative, but may be related to decreased immune response generated from an older donor. Published literature examining lung donor age is limited. A study by Sundaresan and associates 12 reviewed their results with using marginal donors. They compared results of two groups of donors: group 1, those with standard acceptable pulmonary donor criteria, and group 2, those donors who did not meet the established criteria. Acceptable criteria include age 55 years, smoking 20 pack-years, and Pao mm Hg (using inspired oxygen Figure 2. Patient survival after lung transplantation stratified by donor ischemic time. CHEST / 118 / 5/ NOVEMBER,

6 Figure 3. Patient mortality at 2 years: adjusted odds ratio for interaction between donor age and donor ischemic time. Odds ratios 1.0 equate to an increased 2-year mortality after transplantation, whereas odds ratios 1.0 indicate decreased 2-year posttransplant mortality. fraction of 1.0 and positive end-expiratory pressure of5cmh 2 O). A donor with an age 55 years was considered marginal. Although there was a tendency toward older donors in group 2 ( years vs years, p 0.057), only two donors exceeded this age limit. Nevertheless, 30-day mortality was not significantly different between the two groups. Sommers and colleagues 17 found that older donor age correlated with early graft dysfunction within the first hours after transplantation but not at 1 year. Older lung donors were shown to provide acceptable results in other studies as well. 11 Previous publications assessing the effect of lung donor ischemic time on survival have reported varied results. 18,19 Kshettry et al 18 reviewed their series of 83 patients, examining three intervals of ischemia ( 4h,4to6h,and 6 h). Actuarial survival was not significantly different among their groups. They proposed that the lung is the only solid organ that does not rely on perfusion for cellular respiration, Figure 4. Patient hospitalization for rejection by 1-year adjusted odds ratio for donor age. The dotted lines represent 95% confidence intervals Clinical Investigations

7 Table 6 Results of Univariate Analyses of Secondary End Points (p Values) Comparisons Time Point, yr Donor Age p Values Donor Ischemic Time Hospitalized for rejection Bronchiolitis obliterans FEV Bronchial stricture Hospitalized for infection leading to speculation that the process of irreversible ischemia may be delayed in the lung. This information, along with previous studies related to the use of nonbeating heart donors, has caused some investigators to propose the use of cadaveric lungs, again implying the greater ischemic tolerance of the lung. In contrast, Snell and colleagues 19 reviewed their experience with prolonged pulmonary allograft ischemic time in 106 lung or heart-lung transplant patients. These authors found that donor ischemic time 5 h led to reduced survival. The survival difference appeared early, with significant differences noted between 1 and 6 months after transplantation. As in our study, both Kshettry et al 18 and Snell et al 19 reported no detrimental effect of prolonged ischemic time on secondary end points. This includes outcomes such as acute or chronic rejection, duration of ICU or total hospital stay, and FEV 1 at 1 month after transplantation. The incidence of airway complications was also not affected by duration of graft ischemia. Prolonged ischemic time was actually found to be associated with a lower perioperative morbidity from acute rejection and infection in a report by Glanville and associates, 20 although 1-year outcome did not differ from those patients with a shorter ischemic time. In addition to donor age and ischemic time, the present analysis looked at other variables to assess their influence on survival and secondary end points. Among these were tobacco use by the donor, donorrecipient sex mismatches, and ABO blood group incompatibility. An expanded survey of donor and recipient variables identified no factors that independently influenced survival. One secondary end point, hospitalization for rejection, was less likely if the donor was a woman. The explanation for this finding is uncertain at this time. Study Limitations As in any large retrospective, multi-institutional study, this report has several limitations. Pooling data from multiple centers means that management of the patients in terms of immunosuppressive therapy, surgical technique, or preservation strategy was not standardized. This may affect survival data as well as secondary end points. Similarly, voluntary reporting of complete and accurate data in large databases such as the UNOS Registry may be biased toward favorable results. Regarding secondary end points, rejection and infection episodes were reported as such when they were treated in the standard manner. Data were not available as to the type and location of infecting organisms. The definitions of stricture formation and bronchiolitis obliterans were based on clinical criteria from individual transplant centers, and therefore subject to interpretation. Furthermore, important data may not have been available because of limitations of the database. Specifically, indicators of pulmonary function such as the alveolar-arterial oxygen pressure difference, the 6-min walk test, and more in-depth pulmonary spirometry data were not available in the registry. Information regarding the duration of ventilatory support, duration of ICU stay, and the total hospital length of stay would have also strengthened this analysis. Similarly, size mismatch between the donor and the recipient also could have been useful data. Finally, and importantly, the conclusions made from the statistical analysis stating that the strongest effect on survival was seen in donors 55 years of age and ischemic times 7 h must be made with the knowledge of small subgroup sizes available for analysis. Modeled estimates such as used in this analysis were more precise for some of the other combinations tested (donor age 45 years and ischemia time 4 h), for which more patients were available for analysis. Advantages of expanding the donor age criteria and ischemic duration guidelines are clear. Both changes would lead to the potential procurement of more organs and treatment of a greater number of patients. With the safety of an extended ischemic time, more-distant geographic regions could be accessed for organ retrieval. Moreover, prospective human leukocyte antigen cross-matching could be performed. This latter issue would yield additive benefit, as the frequency of rejection might be reduced with a prospective cross-match, potentially extending survival. Further studies will be required to evaluate the many variables associated with adverse outcomes in pulmonary transplantation. How- CHEST / 118 / 5/ NOVEMBER,

8 ever, on the basis of these data, clinicians might use caution in accepting donors at the extremes of both age and ischemic time. Appendix 1 Preoperative and Operative Variables Considered for the Multivariate Analyses Donor Demographics Donor sex Donor age Donor ischemic time Donor tobacco use Recipient Demographics Recipient sex Recipient age Recipient Medical Factors Recipient diagnosis Order of transplant (primary or repeat) In ICU before transplant Hospitalized before transplant Receiving life support before transplant Receiving ventilation before transplant Procedure type (only for FEV 1 analysis) Mismatch Variables Sex mismatch ABO blood group incompatibility References 1 Sundaresan S, Trachiotis GD, Aoe M, et al. Donor lung procurement: assessment and operative technique. Ann Thorac Surg 1993; 56: Hosenpud JD, Bennett LE, Keck BM, et al. The registry of the international society for heart and lung transplantation: fourteenth official report; J Heart Lung Transplant 1997; 16: Novick RJ, Bennett LE, Meyer DM, et al. Influence of graft ischemic time and donor age on survival after lung transplantation. J Heart Lung Transplant 1999; 18: Kaplan EL, Meier P. Nonparametric estimation form incomplete observations. J Am Stat Assoc 1957; 53: Cox DR. Analysis of binary data. London: Methuen, Wheeldon DR, Potter CDO, Oduro A, et al. Transforming the unacceptable donor: outcomes from the adoption of a standardized donor management technique. J Heart Lung Transplant 1995; 14: Ott GY, Herschberger RE, Ratkovec RR, et al. Cardiac allografts from high-risk donors: excellent clinical results. Ann Thorac Surg 1994; 57: Drinkwater DC, Laks H, Blitz A, et al. Outcomes of patients undergoing transplantation with older donor hearts. J Heart Lung Transplant 1996; 15: Starnes VA, Barr ML, Cohen RG. Lobar transplantation: indications, technique, and outcome. J Thorac Cardiovasc Surg 1994; 108: Mauney MC, Cope JT, Binns OAR, et al. Non-heart beating donors: a model of thoracic allograft injury. Ann Thorac Surg 1996; 62: Shumway SJ, Hertz MI, Petty MG, et al. Liberalization of donor criteria in lung and heart-lung transplantation. Ann Thorac Surg 1994; 57: Sundaresan S, Semenkovich J, Ochoa L, et al. Successful outcome of lung transplantation is not compromised by the use of marginal donor lungs. J Thorac Cardiovasc Surg 1995; 109: Young JB, Naftel DC, Bourge RC, et al. Matching the heart donor and heart transplant recipient: clues for successful expansion of the donor pool: a multivariable, multiinstitutional report. J Heart Lung Transplant 1994; 13: Pierson RN III, Reed GW, Bennett LE, et al. Short- and intermediate-term implications of using older donors for heart transplantation. Transplant Proc 1997; 29: Pickering JG, Boughner DR. Fibrosis in the transplanted heart and its relation to donor ischemic time: assessment with polarized light microscopy and digital image analysis. Circulation 1990; 81: Bourge RC, Naftel DC, Constanzo-Nordin MR, et al. Pretransplantation risk factors for death after heart transplantation: a multiinstitutional study. J Heart Lung Transplant 1993; 12: Sommers KE, Griffith BP, Hardesty RL, et al. Early lung allograft function in twin recipients from the same donor: risk factor analysis. Ann Thorac Surg 1996; 62: Kshettry VR, Kroshus TJ, Burdine J, et al. Does donor organ ischemia over four hours affect long-term survival after lung transplantation? J Heart Lung Transplant 1996; 15: Snell GI, Rabinov M, Griffiths A, et al. Pulmonary allograft ischemic time: an important predictor of survival after lung transplantation. J Heart Lung Transplant 1996; 15: Glanville AR, Marshman D, Keogh A, et al. Outcome in paired recipients of single lung transplants from the same donor. J Heart Lung Transplant 1995; 14: Clinical Investigations

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