Abstract
Background:
The data that exists regarding multi-organ procurement outcomes is conflicted. Given the increasing demand for pulmonary allografts, it is critical to assess the impact of dual procurement on lung transplant recipient outcomes.
Methods:
The United Network for Organ Sharing (UNOS) transplant registry was queried for all first-time adult (age ≥18) lung transplant recipients between 2006–2018 and stratified by concurrent heart donor status. Multi-organ transplant recipients and recipients with missing survival time were excluded. Donors were excluded if they were donating after circulatory death (DCD), did not consent or were not approached for heart donation, the heart was recovered for nontransplant purposes, or the heart was recovered for transplant but not transplanted. Posttransplant survival was analyzed using the Kaplan–Meier method and multivariable Cox proportional hazards regression.
Results:
A total of 18,641 recipients met inclusion criteria, including 6,230 (33.4%) in the non-heart donor group (NHD) and 12,409 (66.6%) in the heart donor group (HD). HD recipients demonstrated longer survival at 10 years posttransplant, with a median survival of 6.5 years as compared with 5.9 years in NHD recipients. On adjusted analysis, HD and NHD recipients demonstrated comparable survival (AHR 0.95, 95% CI 0.90–1.01).
Conclusions:
Concomitant heart and lung procurement was not associated with worse survival. This finding encourages maximizing the number of organs procured from each donor, particularly in the setting of urgency-driven thoracic transplantation.
Keywords: Lung, heart, transplant, outcomes
Introduction
Lung transplantation confers a survival advantage and enhanced quality of life for patients with end-stage lung disease 1. In 2019, the number of single and double lung transplants performed reached an annual peak of 2,714, exceeding 60,000 total transplants since 19882, and this growing demand for pulmonary allografts warrants continuous evaluation of ways to increase the supply of organs. Goldberg and colleagues proposed two major avenues through which organ supply can be improved: increased donation rates (percentage of possible deceased donors who become actual donors) and organs transplanted per donor3. While increasing donation rates would be challenging as donor availability is largely unpredictable, increasing the number of organs recovered from each donor is potentially a modifiable behavior within organ procurement practices.
The data that exists regarding multi-organ procurement outcomes is conflicted. A study by Farinelli and colleagues demonstrated comparable survival in recipients of hearts and lungs from multi-organ donors and recipients of organs from single-organ donors 4, while Russo and colleagues demonstrated an increased risk of primary graft dysfunction in heart transplant recipients from multi-organ donors 5. Sample sizes in these studies vary widely. Russo et al used the UNOS data base and had a sample of 16,716 recipients, while Farinelli et al only had access to 92 recipients for analysis. Differences in sample size must be taken into account when interpreting these results. Statistical methods were similar in the two studies. The International Society for Heart and Lung Transplantation (ISHLT) provides guidelines on donor quality assessment but has not published guidelines specific to concomitant procurement of heart and lung allografts 6. The current literature lacks insight into any clear associations between multi-organ procurement and factors shown to affect post-transplant survival, including prolonged ischemia time, donor age, and race 7–9. This information is much needed in light of recent studies conveying wide variability in transplant centers’ organ offer acceptance behaviors which take these highlighted factors into account 10, 11.
Given the lack of data surrounding rates of dual procurement and its impact on transplant recipient outcomes, there is a need to assess and standardize our national organ procurement practices to increase available organs. Concerns arising from dual heart and lung procurement include detriment to donor quality and subsequent recipient outcomes owing to increased ischemic time and surgical complexity of multiorgan procurement. In addition, large volume resuscitation required of brain-death donors as a result of myocardial dysfunction, which may result in pulmonary edema. 12–14 In this study, we sought to examine the rate and impact of concurrent heart and lung procurement on lung recipient outcomes using a large national registry. We tested the hypothesis that concomitant heart-lung procurement does not compromise survival in lung transplant recipients.
Methods
Data Source
We queried the United Network for Organ Sharing (UNOS) database, which prospectively collects clinical data for all organ transplants performed in the United States. The database captures 100% of transplants performed in the US, with detailed donor, recipient, and transplant data 15, 16. This study was deemed exempt by Duke University’s Institutional Review Board.
Study Population and Design
All first-time, adult (age ≥18) recipients who underwent single or bilateral orthotopic lung transplantation between January 1, 2006 and June 30, 2018 and their associated donors were identified in the UNOS registry. Multi-organ transplant recipients and recipients with missing survival time were excluded. Donors and their associated recipients were excluded if they were donating after circulatory death (DCD), did not consent or were not approached for heart donation, their heart was recovered for nontransplant purposes, or their heart was recovered for transplant but not transplanted.
Recipients were then stratified by concurrent heart procurement status. The non-heart donor (NHD) group included recipients who received lungs from donors whose hearts were not transplanted for reasons outside of the exclusion criteria. The heart-donor (HD) group included recipients who received lungs from donors whose hearts were transplanted. The study design is summarized in Figure 1.
Figure 1:
Flow chart of cohort determination. The final cohort consisted of 12,409 heart and lung donors and 6,230 lung-only donors. UNOS: United Network for Organ Sharing; DCD: Donation after circulatory death
Outcomes and Analysis
The primary outcome of interest was post-transplant survival in HD and NHD lung transplant recipients, estimated using the Kaplan-Meier method. Cox Proportional Hazards analysis was conducted to assess risk of death in the HD group vs NHD group after adjustment for differences in baseline donor and recipient characteristics. Donor covariates included in the Cox model were selected a priori and included heart donation status, age (modeled as continuous variable using piecewise linear splines with knot at age 35 due to non-linear relationship), sex, ethnicity, cigarette use, alcohol abuse, cocaine use, history of diabetes, creatine levels, and ischemic time. Recipient covariates included age (≥ 50), sex, ethnicity, BMI, history of diabetes, creatine levels, bilirubin levels, pre-transplant status (location: outpatient, inpatient, or intensive care unit [ICU] pre-transplant), year of transplant, and lung allocation score (LAS). Interactions were tested between heart donation status and donor characteristics. A p- value of less than 0.05 was considered statistically significant.
Secondary outcomes included hospital length of stay, presence of primary graft dysfunction (grade 3), and recipient cause of death. The recipient cause of death was divided into the following categories: graft failure, acute rejection, chronic rejection, infection, cardiovascular, pulmonary, cerebrovascular or multiple-organ failure.
Results
Recipient and donor baseline characteristics
A total of 18,641 recipients met inclusion criteria. Of those, 6,230 (33.4%) were included in the NHD group and 12,409 (66.6%) were included in the HD group. Compared to the NHD recipients, the HD recipients were more likely to be male (63% vs 54%, p<0.001). NHD recipients were more likely to be in the hospital (both ICU and admitted non-ICU) before transplant (20.6% vs 18.8%, p = 0.009). Other baseline characteristics had a statistical significance, but on further inspection had a negligible clinical significance. A complete summary of recipient characteristics is reported in Table 1.
Table 1:
Recipient baseline characteristics
| Heart donor | |||
|---|---|---|---|
| Variable | No | Yes | p-value |
| (n=6,230) | (n=12,409) | ||
| Male gender | 54.3% (3,383) | 63.0% (7,822) | < 0.001 |
| Age (median, IQR) | 60 (14) | 60 (15) | 0.001 |
| BMI (median, IQR) | 25.4 (6.9) | 25.5 (7.0) | 0.631 |
| Ethnicity | 0.499 | ||
| White | 81.8% (5,099) | 82.8% (10,269) | |
| Black | 9.2% (572) | 8.7% (1,085) | |
| Hispanic | 6.5% (404) | 6.1% (762) | |
| Other | 2.5% (155) | 2.4% (293) | |
| Diabetes | 18.6% (1,160) | 18.5% (2,297) | 0.875 |
| Malignancy | 7.7% (478) | 7.7% (959) | 0.916 |
| Creatinine (median, IQR) | 0.8 (0.3) | 0.8 (0.3) | < 0.001 |
| Bilirubin (median, IQR) | 0.5 (0.4) | 0.5 (0.4) | 0.008 |
| Pre-transplant status | 0.009 | ||
| Intensive care unit | 11.2% (697) | 9.9% (1,232) | |
| Hospitalized (non-ICU) | 9.4% (584) | 8.8% (1,095) | |
| Not hospitalized | 79.4% (4,949) | 81.2% (10,082) | |
| Medical therapy | |||
| IV antibiotics in two weeks before transplant | 10.3% (639) | 10.4% (1,289) | 0.802 |
| Ventilator support at transplant | 6.3% (395) | 5.7% (702) | 0.066 |
| ECMO support at transplant | 3.6% (227) | 3.0% (378) | 0.033 |
| ABO blood type | < 0.001 | ||
| A | 40.3% (2,511) | 39.9% (4,954) | |
| B | 12.2% (760) | 10.3% (1,272) | |
| AB | 5.0% (309) | 3.0% (378) | |
| O | 42.5% (2,650) | 46.8% (5,805) | |
| Days on waitlist (median, IQR) | 59 (168) | 62 (169) | 0.070 |
| Lung allocation score at match (median, IQR) | 40.9 (17.4) | 40.3 (16.3) | 0.002 |
| Year of transplant (median, IQR) | 2013 (7) | 2013 (6) | 0.036 |
Compared with heart donors, non-heart donors were more likely to have a history of tobacco use (7% vs 12.4%, p < 0.001), hypertension (11.9% vs 40.9%, p< 0.001), cerebrovascular accident (CVA) as the cause of death than NHD (20.4% vs 51.7%, p < 0.001), head trauma as the cause of death (24.3% vs 58.2%, p< 0.001). Other donor characteristics are reported in Table 2.
Table 2:
Donor/graft characteristics
| Heart donor | |||
|---|---|---|---|
| Variable | No | Yes | p-value |
| (n=6,230) | (n=12,409) | ||
| Donor male gender | 48.4% (3,013) | 68.9% (8,552) | < 0.001 |
| Donor age (median, IQR) | 45 (23) | 26 (17) | < 0.001 |
| Donor BMI (median, IQR) | 25.4 (6.8) | 25.1 (6.1) | < 0.001 |
| Donor ethnicity | < 0.001 | ||
| White | 59.8% (3,725) | 61.5% (7,627) | |
| Black | 21.1% (1,316) | 18.8% (2,334) | |
| Hispanic | 13.5% (839) | 16.4% (2,033) | |
| Other | 5.6% (350) | 3.3% (415) | |
| Donor history | |||
| Cigarette use | 12.4% (771) | 7.0% (874) | < 0.001 |
| Cocaine use | 13.6% (845) | 14.3% (1,772) | 0.192 |
| Alcohol abuse | 15.2% (946) | 13.0% (1,617) | < 0.001 |
| Diabetes | 13.9% (868) | 2.8% (345) | < 0.001 |
| Hypertension | 40.9% (2,549) | 11.9% (1,474) | < 0.001 |
| Cancer | 2.7% (171) | 1.1% (133) | < 0.001 |
| Donor creatinine (median, IQR) | 1.1 (0.8) | 1.0 (0.6) | < 0.001 |
| Donor bilirubin (median, IQR) | 0.7 (0.7) | 0.7 (0.7) | < 0.001 |
| Donor cause of death | < 0.001 | ||
| Anoxia | 20.7% (1,292) | 18.6% (2,304) | |
| Cerebrovascular/stroke | 51.7% (3,224) | 20.4% (2,530) | |
| Head trauma | 24.3% (1,517) | 58.2% (7,217) | |
| CNS tumor | 0.4% (28) | 0.6% (79) | |
| Other | 2.7% (169) | 2.2% (279) | |
| ABO blood type | < 0.001 | ||
| A | 36.7% (2,284) | 35.7% (4,431) | |
| B | 12.1% (751) | 9.9% (1,228) | |
| AB | 3.1% (193) | 1.5% (185) | |
| O | 48.2% (3,002) | 52.9% (6,565) | |
| Graft ischemic time (hours, median, IQR) | 5.1 (2.2) | 5.0 (2.1) | < 0.001 |
Survival outcomes
On unadjusted analysis HD recipients demonstrated improved survival, with a median survival of 6.5 years (95% CI 6.3–6.7) as compared with 5.9 years (95% CI 5.6–6.1) in NHD recipients (Figure 1).
On adjusted analysis heart donation was not related with increased survival (Hazard Ratio [HR] 0.97, 95% Confidence Interval [CI] 0.91–1.02). Several donor factors were associated with an increased risk of death in the adjusted analysis, including black race (HR 1.23, CI 1.16–1.30), cigarette use (HR 1.14, CI 1.05–1.23), and diabetes (HR 1.15, CI 1.04–1.26). Notably, prolonged ischemic time beyond 6 hours was not associated with increased hazard of death (HR 0.97, CI 0.92–1.03; Table 4). Interactions between donor factors and heart donation were tested (supplemental table 1), with a significant interaction demonstrated between heart donation and donor age ≥ 35 (interaction p-value = 0.028).
Table 4:
Cox Proportional Hazards
| 95% Confidence Interval | ||||
|---|---|---|---|---|
| Predictor | Hazard Ratio | Lower | Upper | p-value |
| Donor/graft characteristics | ||||
| Heart donor | 0.97 | 0.91 | 1.02 | 0.215 |
| Age | ||||
| < 35 (per 5 years) | 0.98 | 0.96 | 1.00 | 0.030 |
| >= 35 (per 5 years) | 1.03 | 1.01 | 1.05 | 0.001 |
| Male sex (vs female) | 0.95 | 0.90 | 1.00 | 0.058 |
| Ethnicity | ||||
| White | Ref | Ref | Ref | Ref |
| Black | 1.23 | 1.16 | 1.30 | < 0.001 |
| Hispanic | 1.10 | 1.03 | 1.18 | 0.004 |
| Other | 1.05 | 0.93 | 1.19 | 0.441 |
| Cigarette use | 1.14 | 1.05 | 1.23 | 0.001 |
| Cocaine use | 1.09 | 1.02 | 1.17 | 0.010 |
| Diabetes | 1.15 | 1.04 | 1.26 | 0.005 |
| Creatinine | ||||
| < 1 | Ref | Ref | Ref | Ref |
| 1.0–2.0 | 1.03 | 0.98 | 1.08 | 0.279 |
| 2.0–4.0 | 1.13 | 1.03 | 1.24 | 0.007 |
| > 4.0 | 1.09 | 0.97 | 1.23 | 0.153 |
| Ischemic time | ||||
| < 6 hours | Ref | Ref | Ref | Ref |
| >= 6 hours | 0.97 | 0.92 | 1.03 | 0.314 |
| Recipient characteristics | ||||
| Age >= 50 | 1.45 | 1.36 | 1.54 | < 0.001 |
| Male gender (vs female) | 1.07 | 1.01 | 1.13 | 0.017 |
| Ethnicity | ||||
| White | Ref | Ref | Ref | Ref |
| Black | 0.99 | 0.91 | 1.07 | 0.770 |
| Hispanic | 0.91 | 0.82 | 1.01 | 0.062 |
| Other | 0.89 | 0.76 | 1.05 | 0.176 |
| BMI | 1.01 | 1.00 | 1.01 | 0.028 |
| Diabetes | 1.07 | 1.01 | 1.14 | 0.028 |
| Creatinine | ||||
| < 1 | Ref | Ref | Ref | Ref |
| 1.0–2.0 | 1.13 | 1.08 | 1.20 | < 0.001 |
| 2.0–4.0 | 1.65 | 1.26 | 2.15 | < 0.001 |
| > 4.0 | 1.18 | 0.59 | 2.38 | 0.633 |
| Total bilirubin | ||||
| < 1 | Ref | Ref | Ref | Ref |
| 1.0–2.0 | 1.10 | 1.02 | 1.19 | 0.019 |
| 2.0–4.0 | 1.24 | 1.05 | 1.48 | 0.014 |
| > 4.0 | 1.19 | 0.93 | 1.51 | 0.164 |
| Pre-transplant recipient status | ||||
| Intensive care unit | Ref | Ref | Ref | Ref |
| Hospitalized (non-ICU) | 0.83 | 0.74 | 0.92 | < 0.001 |
| Not hospitalized | 0.72 | 0.66 | 0.79 | < 0.001 |
| Year of transplant (per year) | 0.99 | 0.98 | 0.99 | 0.001 |
| Lung allocation score (LAS) | ||||
| < 30 | Ref | Ref | Ref | Ref |
| 30–40 | 1.30 | 0.79 | 2.12 | 0.300 |
| 40–50 | 1.27 | 0.78 | 2.08 | 0.339 |
| >= 50 | 1.32 | 0.80 | 2.16 | 0.273 |
Among recipient factors, age of 50 years or greater (HR 1.45, CI 1.36–1.54) was associated with an increased risk of mortality, while hospitalization outside of the ICU (HR 0.83, CI 0.74–0.92) and no hospitalization (HR 0.72, CI 0.66–0.79) before transplant were associated with reduced risks of death (Table 4).
Secondary outcomes
Among all secondary outcomes (Table 3), only length of hospital stay was significantly different between HD and NHD recipients, with the HD group demonstrating shorter stays (median (IQR): 16 (15) vs 16 (17), p< 0.001].
Table 3:
Unadjusted outcomes stratified by concurrent heart donation status
| Heart donor | |||
|---|---|---|---|
| Variable | No | Yes | p-value |
| (n=6,230) | (n=12,409) | ||
| Length of stay (days, median, IQR) | 16 (17) | 16 (15) | < 0.001 |
| Primary graft dysfunction, grade 3* | 30.5% (333) | 31.3% (705) | 0.646 |
| Recipient cause of death** | |||
| Primary failure | 2.7% (65) | 2.5% (108) | 0.555 |
| Acute rejection | 1.2% (28) | 1.4% (60) | 0.582 |
| Chronic rejection | 15.2% (359) | 15.0% (652) | 0.833 |
| Infection | 20.3% (480) | 19.0% (826) | 0.192 |
| Cardiovascular | 7.4% (174) | 7.9% (344) | 0.463 |
| Pulmonary | 20.4% (482) | 20.2% (881) | 0.891 |
| Cerebrovascular | 3.4% (80) | 3.4% (149) | 0.996 |
| Multiple-organ failure | 5.9% (140) | 4.7% (205) | 0.035 |
Unadjusted outcomes stratified by concurrent heart donation status. IQR: Interquartile range.
Among recipients with documented 72-hour oxygenation data
among recipients who died during follow-up
Comment
In the present study, we examined the impact of donor heart procurement on lung transplant recipient outcomes. In our unadjusted analysis, the HD lung transplant recipients showed improved survival as compared with the NHD recipients. However, this difference was no longer significant after adjustment for factors known to influence recipient survival, such as increased ischemia time, including donor age, race, and tobacco use 7–9. This suggests that HD donors were healthier at baseline than NHD donors, which negates some of the historical concerns that dual procurement may be associated with several surgeons vying for anatomic territory and operating room space12. In addition, dual procurement was not associated with prolonged ischemic time. Our findings are corroborated by a study conducted in heart transplantation by Xia and colleagues, which showed noninferior survival in heart transplant recipients of concomitant lung donors 12. Taken together, these studies complement each other in informing the national practice in dual heart and lung procurement: which is to use all possible organs that are deemed acceptable for transplant. Importantly, it is possible that the NHD cohort is a surrogate for extended criteria donors (ECD), similar to the results by Mulligan et al.17 In their study ECD are defined as “one or more or the following: donor age 65 years or more, history of smoking 20 pack-years or more, diabetes, and African American race”17. These donor characteristics all showed reduced outcomes for the recipient in our analysis. Overlap between HND and ECD is evident.
Several donor characteristics were associated with an increased risk of mortality in lung transplant recipients after controlling for multi-organ donation, including black race, cigarette use, and diabetes. The association between black race donor and poor recipient survival post-transplant has been well studied across various solid organ transplants 18. Cigarette use by donors is known to cause damage to the lung tissue 19, including cellular damage to the pulmonary parenchyma, and is a known risk factor of rejection regardless of multiorgan procurement. Similarly, cocaine use by donors was associated with poor survival in recipients, likely due to vasoconstriction of blood supply to the lungs resulting in ischemia and tissue damage 20. However, this finding is also not unique to multiorgan procurement recipients. Finally, donor history of diabetes was associated with poor survival in HD recipients. This is another donor factor implicated in poor recipient outcomes regardless of multiorgan donation as increased plasma glucose is shown to induce inflammation in the lung parenchyma 21. Historic concerns about ischemic time were proven to be insignificant in the setting of survival after transplant from dual organ procurement. Our interaction analysis showed that age ≥ 35 had significant interaction with heart donor status. This finding suggests that older donor age is more detrimental for NHD recipients compared with HD recipients.
There are several limitations that warrant discussion. Retrospective reviews using large registry data are unfortunately intrinsically limited by unknown confounders that cannot be measured within the analysis. One significant limitation is that our dataset does not provide insight on why some hearts were deemed suitable for transplantation and others were not. There are certainly unmeasured confounders that influence why certain hearts were not accepted for transplant that affect recipient outcomes. In addition, large databases require manual entry of data and are prone to coding errors and missing data. Some of these concerns are mitigated by the large sample size of the national transplant registry. Importantly, because this retrospective observational data causality cannot be determined.
Conclusion
Concomitant heart procurement of donors was not associated with worse survival in lung transplant recipients. Future efforts to increase the donor pool should include maximizing the number of organs procured from each donor. Donor age appears to have a greater impact on NHD than ND.
Supplementary Material
Supplemental table 1: Summary of tests of interactions between heart donor and other donor variables
Figure 2:
Kaplan-Meier analysis of unadjusted survival over 10 years post-transplant. Median survival in the HD group was 6.5 years and 5.9 years in the NHD group. HD: Lung recipient from a donor who also donated a heart; NHD: Lung recipient from a donor that did not donate a heart.
Acknowledgements
This study was supported by a NIH T-32 grant 5T32HL069749 in clinical cardiovascular research. This work was supported in part by Health Resources and Services Administration contract 234–2005-37011C.
The content is the responsibility of the authors alone and does not necessarily reflect the views or policies of the Department of Health and Human Services, nor does mention of trade names, commercial products, or organizations imply endorsement by the U.S. Government.
Sources of Funding: Institutional funding was used for this study. In addition, OKJ and VR are supported by the NIH T32 grants 5T32HL069749 and 5T32CA093245, respectively, and AYC is supported by the National Center for Advancing Translational Sciences of the NIH under award number TL1TR002555.
Footnotes
Conflict of Interest: The authors report no relevant conflicts of interests as described by ICMJE.
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Supplementary Materials
Supplemental table 1: Summary of tests of interactions between heart donor and other donor variables