Abstract
Background
Little is known regarding the impact of donor COVID‐19 status on recipient outcomes after heart transplantation. In this study, we characterize outcomes of the first 110 heart transplants from organ donors positive for COVID‐19 (COVID‐19+) in the United States.
Methods and Results
Retrospective analysis of the United Network for Organ Sharing database was performed for single‐organ adult heart transplants from January 2020 to March 2022. Donor COVID‐19+ status was defined as a positive nucleic acid amplification, antigen, or other COVID‐19 test within 7 days of transplant. Nearest‐neighbor propensity score matching used to adjust for differences between recipients of COVID‐19+ and nonpositive donor hearts. Overall, 7251 heart transplants were included in analysis, with 110 using COVID‐19+ donor hearts. Recipients of COVID‐19+ allografts were younger (54 [interquartile range, 41–61]) versus 57 [46–64] years; P=0.02) but had similar rates of female sex and non‐White race compared with those receiving allografts from negative donors. Nearest‐neighbor propensity score matching resulted in 100 well‐matched pairs of recipients of COVID‐19+ versus nonpositive donor organs. The 2 matched groups had similar median lengths of stay (15 [11–23] days versus 15 [13–23] days; P=0.40), rates of graft failure (1% versus 0%; P=0.99), 30‐day death (3% versus 3%; P=0.99), and 3‐month survival (88% versus 94%; P=0.23) compared with recipients of nonpositive donors. No deaths occurred due to COVID‐19 infection among the 8 (7%) total deceased recipients of COVID‐19+ allografts to date.
Conclusions
Short‐term outcomes of heart transplant recipients receiving COVID‐19+ donor organs are reassuring. However, continued monitoring for long‐term survival and potential complications are warranted.
Keywords: coronavirus disease 2019, donor qualities, heart failure, heart transplantation, outcomes research, survival
Subject Categories: Heart Failure, Cardiomyopathy
Nonstandard Abbreviations and Acronyms
- UNOS
United Network for Organ Sharing
Clinical Perspective.
What Is New?
Use of COVID‐19+ donor allografts in heart transplantation has increased on a monthly basis since the start of 2021.
Recipients of COVID‐19+ donor hearts experienced similar rates of 30‐day death, acute graft failure, and respiratory causes of death as those receiving non–COVID‐19+ donor hearts.
What Are the Clinical Implications?
These findings provide preliminary evidence that heart transplantation may be performed using appropriately selected COVID‐19+ donor allografts with acceptable outcomes.
Given that organ shortages persist, the use of appropriately selected COVID‐19–positive donor allografts may help to improve access to transplantation for those on the heart transplantation wait list.
Following the onset of the COVID‐19 pandemic, several academic bodies within the organ transplantation community have discouraged the use of organ donors positive for COVID‐19 (COVID‐19+ donors). 1 , 2 Specifically within heart transplantation, the International Society for Heart and Lung Transplantation made recommendations in February 2021 discouraging the use of COVID‐19+ donor hearts for transplantation. 3 Commonly cited reasons for declining COVID‐19+ donors included the concern for donor‐to‐recipient transmission of SARS‐CoV‐2 and the theoretical possibility of cardiac injury due to viral retention within the myocardium. 4
However, since such recommendations have been made, several case series have reported the successful use of COVID‐19+ donors without evidence of viral transmission. Early institutional reports made by Lin et al 5 described 5 heart transplant operations involving the use of COVID‐19+ donors, of which all recipients survived the acute period following transplantation. More recently, Eichenberger et al presented their institution's protocol for using COVID‐19+ donor hearts and lungs for transplantation. 6 Using this protocol, they reported 12 heart transplant operations with no incidence of acute rejection and 1 death occurring 3 months following transplantation from unrelated causes. Similar findings have been reported for transplantation of other organs including liver and kidney, 5 , 7 with no reports thus far of donor‐to‐recipient viral transmission.
While several case studies have described the successful use of COVID‐19+ donors for heart transplantation, nationally representative analyses on the safety and efficacy of COVID‐19+ donor heart transplantation are lacking. In this study, we characterize short‐term outcomes of the first 110 COVID‐19+ donor heart transplants in the United States.
Methods
Study Population
All adults undergoing single‐organ heart transplantation from January 2020 to June 2022 were identified using the United Network for Organ Sharing (UNOS) database. All patients within the study period had complete data on key study variables including age, sex, and transplant date. Heart transplant recipients were primarily stratified by donor COVID‐19 status. The database was acquired from the Organ Procurement and Transplantation Network and was approved for intended use. The data that support the findings of this study are available from UNOS with research request and the data use agreement. The authors were granted an exemption for this study from the University of Pennsylvania Institutional Review Board due to deidentification of the data set. Therefore, informed consent of subjects was not required due to exemption from full review by the institutional review board.
Definitions and Variables
All variables included in the study were provided by the UNOS data dictionary 8 and based on institutional data reported to UNOS on a quarterly basis. Donor COVID‐19+ status was defined as a positive nucleic acid amplification, antigen, or other COVID‐19 test within 7 days of subsequent transplantation into a recipient. This interval was selected on the basis of prior studies suggesting 7 days to be the upper limit estimate for viral incubation times. 9 Both nucleic acid amplification and antigen tests were used to determine donor COVID‐19+ status given similar specificity and low false‐positive test results per recommendations provided by the Centers for Disease Control and Prevention. 10 , 11
Statistical Analysis
Baseline characteristics and short‐term outcomes were compared between heart transplant recipients receiving a heart from a COVID‐19+ donor versus those receiving a heart from a non–COVID‐19+ donor. The number of operations using COVID‐19+ donor hearts from February 2021 to June 2022 was plotted by month. Regional differences in the use of COVID‐19+ donor hearts were mapped according to geographic boundaries determined by the Organ Procurement and Transplantation Network.
Following initial comparisons, nearest‐neighbor propensity score matching without replacement (1:1 ratio) was used to select for matching cohorts of heart transplant recipients receiving COVID‐19+ donor hearts and those receiving non–COVID‐19+ donor hearts. Factors previously associated with death following heart transplantation 12 , 13 were included in a probit regression model, which was subsequently used to determine propensity scores for each patient before matching (Table S1).
Both recipient and donor characteristics were compared between COVID‐19+ donor and non–COVID‐19+ donor groups. Baseline characteristics between groups were compared in the overall and propensity‐matched cohorts. Categorical values are displayed as frequency (proportion of the cohort), while continuous values are shown as median (interquartile range) due to the presence of skew and several outliers in the majority of continuous variables. Standardized mean differences (SMDs; COVID‐19+ donor—non–COVID‐19+ donor) were used to compare baseline characteristics between the groups. An SMD threshold of 0.25 was used to represent adequate variable balance of clinically relevant factors between groups on the basis of previously set guidelines. 14 Chi‐squared and Fisher's exact tests were used to compare categorical outcomes between cohorts where appropriate, while the Wilcoxon rank‐sum test was used to compare continuous outcomes. Multivariable logistic regression was used to determine the association of donor COVID‐19+ status on 30‐day death in the nonmatched total study population. A forward stepwise selection method (step criterion P<0.20) was used to select for covariates.
The primary study outcome was 30‐day death, while several secondary outcomes were assessed as available including postoperative stroke, postoperative dialysis, acute rejection, in‐hospital death, hospital length of stay, and survival at 3 months following transplantation. Kaplan–Meier survival estimates were used to evaluate for differences in survival between groups. Causes of death were also assessed between propensity‐matched COVID‐19+ donor and non–COVID‐19+ donor groups, defined as pulmonary, cardiovascular, graft failure, infection, cerebrovascular, malignancy, multiorgan failure, or other causes. All statistical analyses were performed using Stata/IC 14.2 (Statacorp, College Station, TX). For analytic transparency, the statistical code file used for all analyses is available online at https://github.com/iyengaramit/COVID‐OHT.
Results
Trends in COVID‐19+ Donor Heart Transplantation
Of 7251 heart transplant recipients meeting inclusion criteria, 110 (1.5%) received COVID‐19+ donor hearts. A total of 110 transplanted COVID‐19+ donor hearts were identified in the United States as of August 2022. Since February 2021, COVID‐19+ donor heart use per month has steadily risen (Pearson's r=0.67), with a peak of 20 transplants occurring in January 2022 (Figure 1). Among UNOS regions, Region 11 (Southeast+Mid‐Atlantic) performed the most COVID‐19+ donor heart transplants (n=22), followed by Region 8 (Midwest, n=17; Figure 2). Regions 7 (North Midwest + West Great Lakes) and 1 (Northeast) performed the fewest COVID‐19+ donor heart transplants (n=2, 3 respectively).
Figure 1. Trend of heart transplant donors with a positive COVID‐19 status.
Testing based on nucleic acid, antigen, or other test within 7 days of organ explant, by month. COVID‐19+ indicates positive for COVID‐19.
Figure 2. Geographic use of heart transplant donors with a positive COVID‐19 status.
Testing based on nucleic acid, antigen, or other test within 7 days of organ explant. COVID‐19+ indicates positive for coronavirus disease 2019.
Baseline Characteristics of COVID‐19+ Donor Heart Transplantation
Recipients of COVID‐19+ donor hearts were slightly younger (54 [interquartile range, 41–61] years versus 57 [46–64] years, SMD=−0.21) despite similar rates of female sex (24% versus 27%; SMD=−0.07), non‐White race (38% versus 39%; SMD=−0.02) and statuses 1 to 2 at transplant (54% versus 57%; SMD=−0.07) compared with those receiving non–COVID‐19+ donor hearts (Table 1 ). Additionally, rates of diabetes (35% versus 28%; SMD=0.15), cerebrovascular disease (6% versus 8%; SMD=−0.05), ventilator at transplant (0% versus 2%; SMD=−0.21), and prior cardiac surgery (35% versus 35%; SMD=−0.02) did not differ significantly between groups. Recipients of COVID‐19+ donors less frequently underwent immunosuppressive induction (6% versus 52%; P<0.001) or maintenance (7% versus 65%; P<0.001) therapy, with specific immunosuppressive regimens between the cohorts shown in Table S2.
Table 1.
Baseline Characteristics of COVID‐19+ Donor Heart Transplantation
| Variable | COVID‐19+ donor (n=110) | Non–COVID‐19+ donor (n=7141) | SMD |
|---|---|---|---|
| Recipient characteristics | |||
| Age, y | 54 (41–61) | 57 (46–64) | −0.21 |
| Sex, female | 26 (24) | 1913 (27) | −0.07 |
| BMI, kg/m2 | 28 (25–32) | 28 (24–31) | 0.09 |
| Race or ethnicity | |||
| White | 68 (62) | 4337 (61) | 0.02 |
| Black | 26 (24) | 1728 (24) | −0.01 |
| Hispanic | 15 (14) | 729 (10) | 0.11 |
| Asian | 1 (1) | 266 (4) | −0.19 |
| Other | 0 (0) | 81 (1) | −0.15 |
| MCS modality at transplant | |||
| ECMO | 4 (4) | 412 (6) | −0.10 |
| IABP | 31 (28) | 1930 (27) | 0.03 |
| tVAD | 2 (2) | 322 (5) | −0.15 |
| LVAD | 35 (32) | 2402 (34) | −0.04 |
| UNOS status | |||
| Status 1 | 7 (6) | 663 (9.3) | −0.11 |
| Status 2 | 52 (47) | 3429 (48) | −0.01 |
| Status 3 | 17 (15) | 1112 (16) | −0.003 |
| Status 4 | 27 (25) | 1490 (21) | 0.09 |
| Status 5 | N/A | N/A | |
| Status 6 | 7 (6) | 447 (6) | −0.01 |
| Ventilator at transplant | 0 (0) | 154 (2.2) | −0.21 |
| Days on wait list | 24 (8–142) | 31 (9–154) | −0.10 |
| Diabetes | 38 (35) | 1981 (28) | 0.15 |
| Pulmonary hypertension* | 64 (58.2) | 4383 (61) | −0.07 |
| Cerebrovascular disease | 7 (6) | 541 (8) | −0.05 |
| Prior cardiac surgery | 38 (35) | 2520 (35) | −0.02 |
| Systolic PA pressure, mm Hg | 39 (29–52) | 40 (30–51) | −0.01 |
| Mean PA pressure, mm Hg | 27 (20–35) | 27 (19–36) | −0.01 |
| Cardiac output, L/min | 3.9 (3.2–5.1) | 4.1 (3.3–5.0) | −0.09 |
| Donor characteristics | |||
| Age, y | 28 (21–34) | 32 (25–39) | 0.45 |
| Hypertension | 46 (42) | 3137 (44) | −0.04 |
| Diabetes | 3 (3) | 300 (4) | −0.08 |
| BMI, kg/m2 | 25 (23–31) | 27 (24–31) | −0.06 |
| Female donor | 21 (19) | 1979 (28) | −0.20 |
| Female‐to‐male | 7 (6) | 775 (11) | −0.16 |
| Ischemic time, h | 3.6 (3.1–4.1) | 3.5 (2.9–4.0) | 0.03 |
| Size mismatch† | 30 (27) | 1442 (20) | 0.17 |
| +COVID‐19 test to transplant, d | 3.5 (2–5) | N/A | |
Values are expressed as frequency (%) or median (interquartile range). COVID‐19+ donor: heart transplant recipients receiving an allograft from a donor positive for COVID‐19. Non‐COVID‐19+ donor: those receiving an allograft from a donor who did not test positive for COVID‐19. BMI indicates body mass index; ECMO, extracorporeal membrane oxygenation; IABP, intra‐aortic balloon pump; LVAD, left ventricular assist device; MCS, mechanical circulatory support; N/A, not applicable; PA, pulmonary artery; SMD, standardized mean difference; tVAD, temporary ventricular assist device; and UNOS, United Network for Organ Sharing. Other races include: American Indian or Alaska Native, Native Hawaiian or Other Pacific Islander, Multiracial.
Pulmonary hypertension defined as mean PA pressure ≥25 mm Hg.
Donor predicted heart mass ≤80% recipient predicted heart mass.
Donors who were COVID‐19+ were younger (28 [21–34] years versus 32 [25–39] years; SMD=−0.45) and slightly less commonly women (19% versus 28%; SMD=−0.20) but had similar rates of hypertension (42% versus 44%; SMD=−0.04), diabetes (3% versus 4%; SMD=−0.08), and size mismatch by predicted heart mass (27% versus 20%; SMD=0.17). Similarly, donor body mass index (25 [23–31] kg/m2 versus 27 [25–39] kg/m2; SMD=−0.06) and ischemic times (3.6 [3.1–4.1] hours versus 3.5 [2.9–4.0] hours; SMD=0.17) did not differ significantly between groups. Causes of death between COVID‐19+ donors and nonpositive donors were not significantly different between groups (P=0.08), with the most common causes of death for COVID‐19+ donors being anoxia (51%) and head trauma (44%; Figure 3).
Figure 3. Donor causes of death by COVID‐19 status.
Positive COVID‐19 (COVID‐19+ donor) defined as a positive nucleic acid, antigen, or other test within 7 days of organ explant. COVID‐19+ indicates positive for COVID‐19; and CNS, central nervous system.
Association of COVID‐19+ Donors and 30‐Day Death
A multivariable model was developed to identify donor and recipient factors associated with 30‐day death following heart transplantation (Table 2 ). After adjustment, donor COVID‐19+ status was not associated with increased death (adjusted odds ratio [AOR], 0.85 [95% CI, 0.21–3.53]; P=0.83). Recipient factors associated with increased 30‐day death included increasing age (AOR, 1.03/year [95% CI, 1.01–1.04]; P<0.001), extracorporeal membrane oxygenation at transplant (AOR, 2.83 [95% CI, 1.64–4.91]; P<0.001), left ventricular assist device at transplant (AOR, 1.66 [95% CI, 1.16–2.36]; P<0.01), and prior cardiac surgery (AOR, 1.62 [95% CI, 1.18–2.21]; P<0.01). Increasing donor ischemic time (AOR, 1.12/hour [95% CI, 1.00–1.27]; P=0.06) trended toward association with increased 30‐day death following transplantation.
Table 2.
Logistic Regression for 30‐day Mortality Following Heart Transplantation
| Recipient variable | Adjusted odds ratio | 95% CI | P value |
|---|---|---|---|
| COVID‐19+ donor | 0.85 | 0.21–3.53 | 0.83 |
| Age, increasing, per y | 1.03 | 1.01–1.04 | <0.001 |
| Sex, female | 0.96 | 0.66–1.40 | 0.85 |
| Body mass index, increasing, per kg/m2 | 1.02 | 0.99–1.06 | 0.14 |
| Race or ethnicity | |||
| White | Reference | Reference | Reference |
| Black | 0.71 | 0.48–1.06 | 0.09 |
| Hispanic | 0.99 | 0.59–1.66 | 0.96 |
| Asian | 1.07 | 0.48–2.35 | 0.87 |
| Other | 2.04 | 0.72–5.76 | 0.18 |
| MCS modality at transplant | |||
| ECMO | 2.83 | 1.64–4.91 | <0.001 |
| IABP | 0.94 | 0.62–1.42 | 0.76 |
| tVAD | 0.08 | 0.01–0.58 | 0.01 |
| LVAD at transplant | 1.66 | 1.16–2.36 | <0.01 |
| Mean PA pressure, increasing, per mm Hg | 1.00 | 0.97–1.02 | 0.84 |
| Pulmonary hypertension* | 0.97 | 0.59–1.58 | 0.89 |
| Prior cardiac surgery | 1.62 | 1.18–2.21 | <0.01 |
| Duration on wait list, increasing, per d | .00 | 1.00–1.00 | 0.46 |
| Donor age, increasing, per y | 1.01 | 0.99–1.02 | 0.45 |
| Female donor to male recipient | 1.15 | 0.73–1.81 | 0.55 |
| Donor ischemic time, increasing, per h | 1.12 | 1.00–1.27 | 0.06 |
COVID‐19+ donor: heart transplant recipients receiving an allograft from a donor positive for COVID‐19. Non–COVID‐19+ donor: those receiving an allograft from a donor who did not test positive for COVID‐19. BMI indicates body mass index; ECMO, extracorporeal mechanical oxygenation; IABP, intra‐aortic balloon pump; LVAD, left ventricular assist device; MCS, mechanical circulatory support; PA, pulmonary artery; and VAD, temporary ventricular assist device. Other races include: American Indian or Alaska Native, Native Hawaiian or Other Pacific Islander, Multiracial.
Pulmonary hypertension defined as mean PA pressure ≥25 mm Hg.
Outcomes of COVID‐19+ Donor Heart Transplantation
Outcomes of COVID‐19+ donor heart transplantation are displayed in Table 3 . Recipients of COVID‐19+ donor hearts experienced similar 30‐day (3% versus 3%; P=0.99) and in‐hospital (5% versus 5%; P=0.63) death as those receiving non–COVID‐19+ donor organs. Rates of postoperative stroke (2% versus 4%; P=0.44) and dialysis (15% versus 14%; P=0.58) as well as total hospital length of stay (15 [11–23] days versus 17 [12–25] days; P=0.27) were also not significantly different between groups. Recipients of COVID‐19+ donor hearts had slightly lower rates of acute rejection (10% versus 17%; P=0.04) compared with others.
Table 3.
Short‐Term Outcomes of COVID‐19+ Donor Heart Transplantation
| Variable | COVID‐19+ donor (n=110) | Non‐COVID‐19+ donor (n=7141) | P value |
|---|---|---|---|
| 30‐d death | 3 (3) | 204 (3) | 0.99 |
| In‐hospital death | 6 (5) | 321 (5) | 0.63 |
| Cumulative death | 8 (7) | 657 (9) | 0.62 |
| COVID‐19 infection | 0 (0) | 42 (1) | 0.99 |
| Pulmonary | 0 (0) | 47 (1) | 0.99 |
| Cardiovascular | 2 (2) | 85 (1) | 0.38 |
| Graft failure | 1 (1) | 95 (1) | 0.99 |
| Infection (non–COVID‐19) | 1 (1) | 124 (2) | 0.99 |
| Cerebrovascular | 1 (1) | 58 (1) | 0.60 |
| Malignancy | 0 (0) | 14 (0.2) | 0.99 |
| Multiorgan failure | 0 (0) | 69 (1) | 0.63 |
| Other | 3 (3) | 123 (2) | 0.99 |
| Acute rejection | 11 (10) | 1236 (17) | 0.04 |
| Postoperative complications | |||
| Pacemaker | 1 (1) | 110 (1) | 0.59 |
| Stroke | 2 (2) | 258 (4) | 0.44 |
| Dialysis | 17 (15) | 982 (14) | 0.61 |
| Hospital length of stay, d | 15 (11–23) | 17 (12–25) | 0.26 |
Values are expressed as frequency (%) or median (interquartile range). COVID‐19+ donor: heart transplant recipient receiving an allograft from a donor positive for COVID‐19. Non–COVID‐19+ donor: those receiving an allograft from a donor who did not test positive for COVID‐19.
A total of 8 (7%) patients receiving COVID‐19+ donor organs have died to date. Unadjusted survival at 3 months following transplantation was similar between groups (86% versus 95%; P=0.06), though recipients of COVID‐19+ donors trended toward lower survival (Figure 4). Causes of death were also similar between groups, with no recipients of COVID‐19+ donor allografts dying due to COVID‐19 infection (0% versus 1%; P=0.99) or other pulmonary causes of death (0% versus 0.6%; P=0.99) and only 1 patient dying due to infectious causes (Table 3 ). Other causes of death including cardiovascular (2% versus 1%; P=0.38), graft failure (1% versus 1%; P=0.99), cerebrovascular (1% versus 1%; P=0.60), malignancy (0% versus 0.2%; P=0.99), and multiorgan failure (0% versus 1%; P=0.63) were rare and not significantly different between groups.
Figure 4. Survival in heart transplant recipients, by donor COVID‐19 status.
Overall population in the left panel, nearest‐neighbor propensity score–matched cohorts in the right panel. Positive COVID‐19 (COVID‐19+) defined as a positive nucleic acid, antigen, or other test within 7 days of organ explant. COVID‐19+ donor: heart transplant recipient receiving an allograft from a donor positive for COVID‐19. Non–COVID‐19+ donor: those receiving an allograft from a donor who did not test positive for COVID‐19.
Outcomes of Propensity Score–Matched COVID‐19+ Donor Heart Transplantation
Propensity score matching resulted in 100 well‐matched pairs of COVID‐19+ donor and non–COVID‐19+ donor, with SMD <0.25 for all clinically relevant variables (Table 4 ). A total of 74 different transplant centers were represented across the 2 propensity score–matched cohorts, with no obvious clustering of patients at any given center. Acute outcomes of COVID‐19+ donor heart transplant recipients following propensity score matching are shown in Table 5 . Among matched cohorts, there were again no significant differences in 30‐day (3% versus 3%; P=0.99) and in‐hospital (5% versus 4%; P=0.99) death, postoperative stroke (1% versus 1%; P=0.99), postoperative dialysis (14% versus 11%; P=0.52), and total hospital length of stay (15 [11–23] days versus 15 [13–23] days; P=0.40). Acute rejection remained slightly more prevalent in the non–COVID‐19+ donor group (9% versus 19%; P=0.07).
Table 4.
Baseline Characteristics of COVID‐19+ Donor Heart Transplantation—Matched
| Variable | COVID‐19+ donor (n=100) | Non–COVID‐19+ donor (n=100) | SMD |
|---|---|---|---|
| Recipient characteristics | |||
| Age, y | 54 (42–61.5) | 52.5 (41–60.5) | 0.09 |
| Sex, female | 25 | 23 | 0.05 |
| BMI, kg/m2 | 28 (25–32) | 28 (25–32) | −0.04 |
| Race or ethnicity | |||
| White | 61 | 53 | 0.16 |
| Black | 25 | 27 | −0.05 |
| Hispanic | 13 | 12 | 0.03 |
| Asian | 1 | 6 | −0.27 |
| Other | 0 | 2 | −0.20 |
| MCS modality at transplant | |||
| ECMO | 2 | 0 | 0.20 |
| IABP | 29 | 30 | −0.02 |
| tVAD | 2 | 3 | −0.06 |
| LVAD | 32 | 37 | −0.10 |
| UNOS status | |||
| Status 1 | 5 | 6 | 0.04 |
| Status 2 | 46 | 52 | −0.12 |
| Status 3 | 16 | 11 | 0.15 |
| Status 4 | 27 | 26 | 0.02 |
| Status 5 | N/A | N/A | |
| Status 6 | 7 | 447 | 0.04 |
| Ventilator at transplant | 0 | 1 | −0.14 |
| Days on waitlist | 25 (8–144) | 31 (11.5–129) | −0.02 |
| Diabetes | 36 | 37 | −0.02 |
| Pulmonary hypertension* | 58 | 62 | −0.08 |
| Cerebrovascular disease | 6 | 7 | −0.04 |
| Prior cardiac surgery | 36 | 43 | 0.14 |
| Systolic PA pressure, mm Hg | 39.5 (28.5–53) | 42 (31–54) | −0.14 |
| Mean PA pressure, mm Hg | 30 (21–37) | 27 (19–36.5) | −0.11 |
| Cardiac output, L/min | 3.9 (3.2–5.1) | 4.1 (3.2–5.0) | −0.10 |
| Donor characteristics | |||
| Age, y | 27 (20.5–35) | 29 (22.5–35) | −0.12 |
| Hypertension | 44 | 44 | 0 |
| Diabetes | 2 | 0 | 0.20 |
| BMI, kg/m2 | 25 (23–31) | 26 (24–31) | −0.01 |
| Female donor | 19 | 19 | 0 |
| Female‐to‐male | 6 | 7 | −0.04 |
| Ischemic time, h | 3.6 (3.1–4.1) | 3.6 (3.1–4.3) | −0.16 |
| Size mismatch† | 28 | 30 | −0.04 |
| +COVID‐19 test to transplant, d | 3 (2–5) | N/A | |
Values are expressed as frequency (%) or median (interquartile range). COVID‐19+ donor: heart transplant recipient receiving an allograft from a donor positive for COVID‐19. Non–COVID‐19+ donor: those receiving an allograft from a donor who did not test positive for COVID‐19. BMI indicates body mass index; ECMO, extracorporeal membrane oxygenation; IABP, intraaortic balloon pump; LVAD, left ventricular assist device; MCS, mechanical circulatory support; N/A, not applicable; PA, pulmonary artery; SMD, standardized mean difference; tVAD, temporary ventricular assist device; and UNOS, United Network for Organ Sharing. Other races include: American Indian or Alaska Native, Native Hawaiian or Other Pacific Islander, Multiracial.
Pulmonary hypertension defined as mean PA pressure ≥25 mm Hg.
Donor predicted heart mass ≤80% recipient predicted heart mass.
Table 5.
Short‐Term Outcomes of COVID‐19+ Donor Heart Transplantation—Matched
| Variable | COVID‐19+ donor (n=100) | Non‐COVID‐19+ donor (n=100) | P value |
|---|---|---|---|
| 30‐d death | 3 | 3 | 0.99 |
| In‐hospital death | 5 | 4 | 0.99 |
| Cumulative death | 7 | 10 | 0.61 |
| COVID‐19 infection | 0 | 0 | … |
| Pulmonary | 0 | 1 | 0.99 |
| Cardiovascular | 1 | 1 | 0.99 |
| Graft failure | 1 | 0 | 0.99 |
| Infection (non–COVID‐19) | 1 | 2 | 0.99 |
| Cerebrovascular | 1 | 0 | 0.99 |
| Malignancy | 0 | 1 | 0.99 |
| Multiorgan failure | 0 | 2 | 0.50 |
| Other cause of death | 3 | 3 | 0.99 |
| Acute rejection | 9 | 19 | 0.07 |
| Postoperative complications | |||
| Pacemaker | 1 | 3 | 0.31 |
| Stroke | 1 | 1 | 0.99 |
| Dialysis | 14 | 11 | 0.52 |
| Hospital length of stay, d | 15 (11–23) | 15 (13–23) | 0.40 |
Values are expressed frequency or median (interquartile range). COVID‐19+ donor: heart transplant recipient receiving an allograft from a donor positive for COVID‐19. Non–COVID‐19+ donor: those receiving an allograft from a donor who did not test positive for COVID‐19.
In the propensity score–matched cohorts, 7 (7%) of COVID‐19+ donor heart transplant recipients died during the study period, with similar 3‐month survival (88% versus 94%; P=0.23) between groups (Figure 4). Causes of death among propensity score–matched heart transplant recipients of COVID‐19+ versus non–COVID‐19+ donor hearts are shown in Table 5 .
Discussion
In this study, we report national trends in the use and outcomes of COVID‐19+ donor heart transplantation. Since February 2021, use of COVID‐19+ donor allografts in heart transplantation has increased on a monthly basis, with UNOS Region 11 (Southeast+Mid‐Atlantic) performing the most COVID‐19+ donor heart transplants. Notably, we found recipients of COVID‐19+ donor hearts to experience similar rates of 30‐day death, acute graft failure, and respiratory causes of death as those receiving non‐COVID‐19+ donor allografts.
The findings of this study expand on previous institutional case series and earlier national reports documenting the use of COVID‐19+ donor allografts in heart transplantation. 15 The earliest reports on COVID‐19+ donors by Lin et al noted 5 cases using donors testing positive on polymerase chain reaction testing with no active symptoms of an upper respiratory tract infection. 5 Despite perioperative complications occurring in 3 of 5 cases, no complications could plausibly be linked to the donor's COVID‐19+ status. Similarly, a more recent report by Eichenberger et al 6 described an institutional protocol on the use of COVID‐19+ donors in thoracic transplantation, noting that none of the 13 recipients of COVID‐19+ donor organs experienced signs or symptoms of COVID‐19 infection following transplantation. Of note, in the report by Eichenberger and colleagues, the transplants largely occurred in 2021, when the delta strain of SARS‐CoV‐2 was the predominant strain. Based on data from Centers for Disease Control and Prevention, 16 the most prevalent strain of SARS‐CoV‐2 in the United States was the delta variant through November 2021, with the omicron variant overtaking delta as the dominant strain in late December 2021. Therefore, it may be reasonable to infer that delta was the predominant strain in COVID‐19+ donors in our study before December 2021 and omicron for those donors infected after this date.
Initial apprehension surrounding the use of COVID‐19+ donors can largely be attributed to the potential for donor organ‐to‐recipient viral transmission and subsequent inflammatory damage within the transplanted organ. 3 Symptomatic COVID‐19 has been associated with increased risk for myocarditis due to the notable cardiac tropism of SARS‐CoV‐2 compared with other human coronaviruses. Specifically, the SARS‐CoV‐2 virus maintains structural properties that enhance its targeting for the angiotensin‐converting enzyme 2 receptor, found in high density within the heart, kidney, and liver outside of its predominant presence in the lungs. 17 , 18 However, practically, such cases of transmission have proven to be extremely rare 19 , 20 and confined to the transplantation of lungs, in which the SARS‐CoV‐2 load may be sufficiently high to survive organ ischemia and the known inflammatory insult associated with organ procurement.
Organ mapping of SARS‐CoV‐2 RNA in symptomatic patients with COVID‐19 has previously shown the that the virus is retained predominantly within the upper and lower respiratory tracts and, to a lesser extent, within the distal pulmonary artery branches and surrounding lymph nodes. 21 In contrast, viral load has been shown to be exceedingly low within the heart and aorta, central nervous system, gastrointestinal tract, and urinary tract, among several other organ systems. 21 Such studies were conducted post mortem on individuals dying due to respiratory complications of COVID‐19. Given the association between viral load and disease severity, 22 asymptomatic donors testing positive for COVID‐19 may be even less likely to pass on symptomatic disease to the recipient via organ transplantation. Studies by Yao et al further contribute to this notion, showing SARS‐CoV‐2 to be undetectable within the myocardium of individuals dying due to complications of COVID‐19. 17 , 18 Given that mostly asymptomatic donors were used in the institutional protocols previously published, 5 , 6 , 23 the equivocal findings shown in our study between recipients of COVID‐19+ and non–COVID‐19+ donors may reflect the low likelihood of viral transmission from a potentially asymptomatic donor population. This notion is supported by the lack of recipient deaths occurring due to COVID‐19 infection in the COVID‐19+ donor cohort. Furthermore, the most serious complications of SARS‐CoV‐2, such as respiratory failure and myocarditis, were likely not major contributors of death in the COVID‐19+ donor recipient pool given relatively low rates of death from pulmonary and cardiovascular causes, respectively. These data are supported by prior institutional protocols that have shown the successful transplantation of COVID‐19+ donor hearts without subsequent COVID‐19 infection in the recipients. 5 , 6
The reassuring short‐term outcomes of COVID‐19+ donor heart transplantation found in our study may help to inform decision making for physicians and patients on the heart transplant wait list. These findings, however, may not capture a selection bias for COVID‐19+ donors who are potentially healthier than the typical donor pool and otherwise likely to yield successful outcomes upon transplantation in a recipient. Conversely, the 3‐month survival of 86% in the COVID‐19+ donor group was lower than expected, though this finding did not reach significance. This may be indicative of a potentially sicker recipient population receiving allografts from COVID‐19+ donors that is not reflected within the baseline characteristics captured by UNOS. Recipients of allografts from COVID‐19+ donors may have had extenuating circumstances such as initial difficulty finding a donor match, in which case the patient and physician were willing to accept a COVID‐19+ donor offer despite the relative paucity of data to date on the use of COVID‐19+ donor organs. Such data warrant further monitoring in future studies to determine whether the survival curves continue to diverge over time. Though the preliminary data provided in this study did not show significant differences between the cohorts, it is important to consider the retrospective nature of this study, with long‐term outcomes yet to be studied.
According to the institutional protocol published by Eichenberger et al, 6 COVID‐19+ donors with a terminal illness complicated by hypercoagulability or hyperinflammatory syndrome are excluded from use in transplantation. Additionally, the protocol endorses a potentially more conservative threshold for other donor factors that may be predictive of poor organ performance upon transplantation that may be reasonably applied in COVID‐19+ donors. 24 , 25 , 26 , 27 Other donor exclusionary criteria in a protocol recently reported by Madgula et al 23 include radiographic evidence of pneumonia or active symptoms of COVID‐19 at presentation. Furthermore, all protocols highlighting the use of COVID‐19+ donors to date have excluded those with moderate to severe symptoms at the time of testing. Further, given that vaccination rates are known to decrease transmission rates of SARS‐CoV‐2 within the community, 28 vaccination status of the donor and recipient may also aid in decision making in the use of a COVID‐19+ donor. Though this information was not available in our study, use of COVID‐19+ donor hearts may reasonably be more heavily favored in cases in which both the donor and recipient are vaccinated. All available protocols documenting the successful use of COVID‐19+ donors have performed heart transplantation in vaccinated recipients. 5 , 6 , 23 Such reports provide preliminary evidence that other institutions performing COVID‐19+ donor heart transplantation may be adopting similar practices regarding recipient vaccination status. However, it is important to consider that vaccination may elicit a poor immune response in solid‐organ transplant recipients, with immunosuppressed patients experiencing more severe complications of COVID‐19 infection compared with the immunocompetent patient population. 29 Nevertheless, these criteria serve as a potential framework if the decision is made to use a COVID‐19+ donor, though the validity of such protocols cannot be affirmed by the findings of this study and the long‐term implications remain unknown.
Given the paucity of data on COVID‐19+ donor heart transplantation, there is also no guidance on the management and posttransplant surveillance of recipients of COVID‐19+ donor organs. Certainly, extra caution may be exercised in regard to monitoring for respiratory symptoms associated with SARS‐CoV‐2 infection at follow‐up, but the role of and potential need for increased surveillance for myocardial complications is debatable. No alterations to a standard rejection surveillance protocol have been specified by institutional protocols reported thus far, and there must be diligence for cardiac‐specific complications moving forward. Therefore, we recommend postoperative surveillance of COVID‐19+ donor heart recipients via weekly nasopharyngeal COVID‐19 reverse transcription polymerase chain reaction testing for at least the first month following transplantation. This time period is a conservative approach to testing given prior literature showing the time to peak viral load after shedding of SARS‐CoV‐2 to be <1 week. 9 However, it is important to note that the standard postoperative protocols for recipients of COVID‐19+ donor hearts must be optimized as further data on this cohort become available.
We acknowledge the limitations in our study, several of which are inherent to a retrospective cohort study with limited sample size. The UNOS database lacks granular clinical data, and thus several donor and recipient factors were unable to be accounted for in analysis, including echocardiographic abnormalities, radiographic findings, certain preoperative laboratory values such as cardiac enzymes, and both recipient and donor vaccination statuses. The strain of COVID‐19 and mode of viral transmission (community‐acquired or nosocomial), viral strain, and presence of symptoms in COVID‐19+ donors were also not available in the UNOS database. Therefore, data informing further donor selection criteria was not fully available and should be considered for future investigation. Though our study encompasses the national cohort of COVID‐19+ donors used in heart transplantation through to June 2022, our sample size and study power were limited given the relatively slow growth and acceptance of COVID‐19+ donor use in the country. It should be cautioned that the data set may be underpowered to detect small differences in short‐term death and survival; however, this represents the largest sample size to date on COVID‐19+ donor heart recipients. Data on donor offers, including COVID‐19+ donors ultimately not used for transplantation, were not available in the UNOS database and should be examined in future studies. While the Organ Procurement and Transplantation Network in conjunction with UNOS receives death data from a wide range of sources, including institutional reporting and the social security death master file, it is important to note that these data may be incomplete given the recency of the data in this study. 30 , 31 Finally, longer‐term data such as remote survival and rates of cardiac allograft vasculopathy were unavailable based on the limited follow‐up data due to recency of COVID‐19+ donor use. Future studies should continue to monitor for the development of long‐term complications associated with latent viral infection or late manifestations of SARS‐CoV‐2 infection.
This study is the most comprehensive report to date on the national outcomes of COVID‐19+ donor heart transplantation. We found that 30‐day death and rates of graft failure did not significantly differ between recipients of COVID‐19+ and non–COVID‐19+ donor hearts, despite a nonsignificant decrease in 3‐month survival in the COVID‐19+ donor cohort. While the impact of the COVID‐19 pandemic on organ transplantation continues to wane, 32 organ shortages persist and the use of COVID‐19+ donor organs may eventually help to improve access to transplantation as more data become available. However, continued monitoring of COVID‐19+ donor heart recipients for long‐term outcomes and potential complications is warranted.
Sources of Funding
This study was supported by the Division of Cardiovascular Surgery, Department of Surgery at the University of Pennsylvania.
Disclosures
None.
Supporting information
Tables S1–S2
This manuscript was sent to Sakima A. Smith, MD, MPH, Associate Editor, for review by expert referees, editorial decision, and final disposition.
This work was presented in part at the American Heart Association Scientific Sessions, November 5–7, 2022.
Supplemental Material is available at https://www.ahajournals.org/doi/suppl/10.1161/JAHA.122.029178
For Sources of Funding and Disclosures, see page 11.
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Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Supplementary Materials
Tables S1–S2