INTRODUCTION
The first wave of the coronavirus disease 2019 (COVID-19) pandemic in spring 2020 severely impacted transplant activity worldwide.1-6 Main reasons for the dramatic decline were the sudden and unforeseen lack of resources, on the one hand, and the lack of specific recommendations for maintaining transplantation activities during a pandemic, on the other hand. Concerns about potential donor-to-recipient transmission, screening strategies, posttransplant management, ethics and legal issues, and more caused great uncertainty and even led to a temporary suspension of nonvital transplants.7 , 8
The decrease in COVID-19 cases during summer 2020 reduced the burden on healthcare systems, and guidelines emerged that outlined how to maintain transplantation activity in case of a second wave.3 , 6 , 9-11 Obviously, the question arises whether the experience gained during the first wave helped us to guide transplant activity better during the second wave. Unfortunately, the second (and third) wave in winter 2020 to 2021 lasted longer and was far more intense than the first wave, suggesting a negative influence on transplant activity.
This study aimed to illustrate the impact of COVID-19 on organ transplantation in the Eurotransplant (ET) region during the first 12 mo of the pandemic. The ET region comprises Austria, Belgium, Croatia, Germany, Hungary, Luxembourg, the Netherlands, and Slovenia and has a total population of around 137 million people. To determine whether transplant activity in ET countries adapted to this new reality, we analyzed the numbers of all organ donations and transplantations (ODTs) performed during the first 12 mo of the COVID-19 era and compared them with those of the previous 5 y.
MATERIALS AND METHODS
ODT data for all ET countries from March 1, 2015, to February 28, 2021, were obtained from the Eurotransplant International Foundation registry. The data are public and anonymous, thus eliminating the need for approval by an ethics committee. For better differentiation of donor characteristics, organ donors were divided into living and deceased donors, and deceased donors were divided into donors after brain death and donors after circulatory death. Furthermore, reported kidneys were differentiated into living and deceased donations, whereas transplanted kidneys were distinguished into standard criteria donations and extended criteria donations. To allow for a more detailed description of ODT dynamics in the period from 2020 to 2021, we divided the observation period into three 4-mo periods, ranging from March 1 to June 30 (period 1), July 1 to October 30 (period 2), and November 1 to February 28 (period 3). Hence, period 1 represents the first wave of the COVID-19 pandemic, period 3 the second wave, and period 2 the interval in between them. ODT data for the period from 2020 to 2021 were then compared with those for the respective period of the previous 5 y. COVID-19 cases for ET countries were taken from the OurWorldInData.org database, which collects the worldwide COVID-19 figures on a daily basis. To objectify the magnitude of the 2 COVID-19 waves, the area under the curve was calculated for the respective course of confirmed new COVID-19 cases.
Statistical Analysis
Statistical analysis was conducted using R, version 4.0.3. A significance level of 5% was used for all assessments. Differences in the number of ODTs between the observation period from 2020 to 2021 and the corresponding periods in the previous 5 y are given as estimated mean differences with 95% confidence intervals and assessed with the Poisson test.
RESULTS
Organ Donation
During the observation period from 2020 to 2021, the total number of organ donors in the ET region decreased by 18.3% (2960 versus 3622; P < 0.0001) compared with the average of the previous 5 y (Table 1 ). The number of living and deceased donors decreased by 32.1% (957 versus 1409; P < 0.0001) and 9.5% (2003 versus 2214; P < 0.0001), respectively. The number of donation after brain death donors decreased by 11.6% (1662 versus 1881; P < 0.0001), whereas the number of donation after circulatory death donors remained unchanged (341 versus 333; P = 0.3388; Table 1 ). The decline in organ donors is reflected in a decrease in the number of all organs reported in the ET area, including hearts, lungs, livers, pancreas, and kidneys (all P < 0.0001; Table 1 ). With respect to kidney grafts, donations from living and deceased donors decreased by 34.8% (858 versus 1315; P < 0.0001) and 12.3% (3555 versus 4052; P < 0.0001), respectively.
TABLE 1. -
Number of organ donors, organs reported, organs transplanted, and patients on waiting lists during the first 12 mo of COVID-19 (defined as March 1, 2020, to February 28, 2021) compared with the mean values of the respective periods during the previous 5 y
Count (2020–2021)
Mean count (2015–2019)
Decrease (%)
P
Donors reported
Total
2960
3622 (3570-3676)
18.3
<0.0001
Living
957
1409 (1376-1442)
32.1
<0.0001
Deceased
2003
2214 (2173-2255)
9.5
<0.0001
DBD
1662
1881 (1843-1919)
11.6
<0.0001
DCD
341
333 (317-349)
–2.4
0.3388
Organs reported
Heart
724
834 (809-860)
13.2
<0.0001
Lung
2000
2145 (2105-2186)
6.8
<0.0001
Liver
2089
2219 (2178-2260)
5.8
<0.0001
Pancreas
732
882 (857-909)
17.0
<0.0001
Kidney
4413
5367 (5303-5432)
17.8
<0.0001
Living
858
1315 (1284-1347)
34.8
<0.0001
Deceased
3555
4052 (3997-4108)
12.3
<0.0001
Organs transplanted
Total
6160
7044 (6970-7118)
12.5
<0.0001
Heart
571
607 (585-629)
5.9
0.001
Lung
1257
1293 (1262-1325)
2.8
0.0228
Liver
1439
1620 (1585-1655)
11.2
<0.0001
Pancreas
152
203 (190-215)
25.0
<0.0001
Kidney
2741
3321 (3271-3372)
17.5
<0.0001
SCD
1583
1866 (1828-1904)
15.2
<0.0001
ECD
1158
1456 (1422-1489)
20.5
<0.0001
Waiting list
Total
14 260
14 835 (14 728-14 942)
3.9
<0.0001
Heart
1108
1147 (1118-1177)
3.4
0.0091
Lung
623
767 (743-791)
18.7
<0.0001
Liver
1459
1661 (1626-1697)
12.2
<0.0001
Pancreas
397
433 (415-452)
8.3
0.0001
Kidney
10 673
10 827 (10 736-10 919)
1.4
0.0009
Data are presented as mean (95% CI).
CI, confidence interval; COVID-19, coronavirus disease 2019; DBD, donation after brain death; DCD, donation after circulatory death; ECD, extended criteria donation; SCD, standard criteria donation.
The mean number of actively listed patients waiting for a heart, lung, liver, pancreas, and kidney transplantation significantly decreased during the first 12 mo of the pandemic compared with the previous 5 y (Table 1 ).
Organ Transplantation
The number of transplantations performed decreased significantly for all organ entities in the ET region, with abdominal organs being more affected than thoracic organs (Table 1 ). No single ET country was able to prevent a decline in the total number of organ transplantations (all P < 0.001); however, stable rates for heart transplantation could be maintained in Austria (minus 8.7%; P = 0.103), the Netherlands (minus 3.0%; P = 0.6673), and Slovenia (minus 14.7%; P = 0.0774); stable rates for lung transplantation in Germany (minus 0.5%; P = 0.7764), Hungary (plus 16.6%; P = 0.0501), and the Netherlands (plus 3.7%; P = 0.3087); stable rates for liver transplantation in Austria (minus 5.9%; P = 0.0897) and the Netherlands (minus 4.3%; P = 0.2101); and stable rates for pancreas transplantation in Germany (minus 6.3%; P = 0.1619) and Hungary (minus 9.1%; P = 0.5828). Kidney transplantations decreased significantly in all countries (all <0.05). Standard criteria donation and extended criteria donation kidney transplantations decreased by 15.2% (1583 versus 1866; P < 0.0001) and 20.5% (1158 versus 1456; P < 0.0001), respectively (Table 1 ).
Temporal Analysis
The total number of organ donors decreased by 26.2% in period 1, by 5.5% in period 2, and by 23.1% in period 3 (all P < 0.0001) compared with the mean number of the corresponding periods of the preceding 5 y (Table 2 ). As a result, the number of performed transplantations decreased by 16.5% in period 1, by 4.9% in period 2, and by 16.4% in period 3 (all P < 0.0001). Details on the temporal development of the ODT numbers during the observation period are presented in Table 2 . A graphical presentation of ODT numbers in relation to cumulative COVID-19 cases in the ET countries is shown in Figure 1 . Calculation of the area under the curve of cumulative COVID-19 cases found that the magnitude of the second COVID-19 wave was 12-fold higher than that of the first wave (Figure 1 ).
TABLE 2. -
Number of organ donors, organs reported, and organs transplanted during the observation periods 1–3 during 2020–2021 compared with the average numbers of the corresponding periods of the previous 5 y
Period 1
Period 2
Period 3
Count (2020–2021)
Mean count (2015–2019)a
Decrease (%)
P
Count (2020–2021)
Mean count (2015–2019)a
Decrease (%)
P
Count (2020–2021)
Mean count (2015–2019)
Decrease (%)
P
Donors reported
Total
881
1193 (1163-1224)
26.2
<0.0001
1130
451 (433-470)
5.5
0.0091
949
1234 (1203-1265)
23.1
<0.0001
Living
243
478 (459-497)
49.1
<0.0001
406
451 (433-470)
10.0
<0.0001
308
480 (461-499)
35.8
<0.0001
Deceased
638
715 (692-739)
10.8
<0.0001
724
745 (721-769)
2.8
0.0869
641
754 (730-778)
15.0
<0.0001
DBD
544
609 (587- 631)
10.6
<0.0001
590
632 (610-654)
6.7
0.0001
528
640 (618-662)
17.5
<0.0001
DCD
94
106 (98-116)
11.7
0.0049
134
113 (103-122)
–19.0
<0.0001
113
114 (105-124)
0.9
0.8334
Organs reported
Heart
237
273 (259-288)
13.3
<0.0001
261
280 (266-295)
6.9
0.0085
226
281 (266-296)
19.5
<0.0001
Lung
634
699 (676-723)
9.3
<0.0001
710
731 (707-755)
2.8
0.0839
656
715 (692-739)
8.3
<0.0001
Liver
664
713 (690-737)
6.9
<0.0001
757
744 (721-769)
–1.7
0.3097
668
761 (737-786)
12.2
<0.0001
Pancreas
216
290 (275-305)
25.4
<0.0001
276
296 (282-312)
6.9
0.0065
240
296 (282-312)
19.0
<0.0001
Kidney
1327
1759 (1723-1797)
24.6
<0.0001
1695
1782 (1745-1819)
4.9
<0.0001
1391
1826 (1789-1864)
23.8
<0.0001
Living
207
446 (427-465)
53.6
<0.0001
375
421 (404-440)
11.0
<0.0001
276
448 (430-467)
38.4
<0.0001
Deceased
1120
1314 (1282-1346)
14.7
<0.0001
1320
1361 (1328-1393)
3.0
0.0129
1115
1378 (1346-1411)
19.1
<0.0001
Organs transplanted
Total
1923
2304 (2262-2346)
16.5
<0.0001
2266
2381 (2339-2425)
4.9
<0.0001
1971
2358 (2316-2401)
16.4
<0.0001
Heart
191
197 (185-210)
3.1
0.3316
202
206 (193-219)
1.8
0.5711
178
204 (192-217)
12.8
<0.0001
Lung
369
436 (418-455)
15.4
<0.0001
469
442 (424-461)
–6.2
0.0048
419
415 (397-433)
–1.0
0.6701
Liver
462
527 (507-548)
12.3
<0.0001
512
545 (525-566)
6.1
0.0011
465
548 (572-569)
15.1
<0.0001
Pancreas
50
70 (63-78)
28.8
<0.0001
66
69 (62-76)
3.8
0.4741
36
64 (57-71)
43.6
<0.0001
Kidney
851
1073 (1045-1102)
20.7
<0.0001
1017
1120 (1091-1150)
9.2
<0.0001
873
1128 (1099-1158)
22.6
<0.0001
SCD
505
611 (590-633)
17.4
<0.0001
609
651 (629-674)
6.5
0.0002
469
603 (582-625)
22.3
<0.0001
ECD
346
462 (443-481)
25.1
<0.0001
408
469 (450-488)
13.0
<0.0001
404
525 (505-545)
23.0
<0.0001
a Data are presented as mean (95% CI).
CI, confidence interval; DBD, donation after brain death; DCD, donation after circulatory death; ECD, extended criteria donation; SCD, standard criteria donation.
FIGURE 1.: The light gray and dark gray lines (solid for the period 2020–2021 and dashed for the period 2015–2019 averages) represent organs reported and organs transplanted, respectively. The solid black line represents the 14-d moving average of daily new COVID-19 cases in the Eurotransplant region. COVID-19, coronavirus disease 2019.
DISCUSSION
This retrospective analysis shows that the first 12 mo of the COVID-19 pandemic caused a significant drop in organ donation and transplantation activities in the ET region, with all ET countries being similarly affected. The decrease in ODTs during the second wave was comparable with that during the first one, although the incidence of COVID-19 cases was unequally higher during the second wave.
Limited knowledge of the new infectious disease caused by severe acute respiratory syndrome coronavirus 2, the unknown impact of infection in immunosuppressed organ recipients, and possible severe acute respiratory syndrome coronavirus 2 donor-to-recipient transmission moved several transplantation societies to the recommended postponement of nonurgent kidney and pancreas transplantations in March 2020.7 As the rapid progression of the pandemic demanded that substantial healthcare resources be made available quickly,12 many surgical intensive care units (ICUs) were converted to COVID-19 ICU facilities, and medical staff was relocated to prevent critical healthcare areas from collapse.7 These measures most likely caused an additional reduction in ODTs during the first trimester of our observation period compared with the previous 5 y, which is in line with reports from various countries describing a similar development during the first wave (spring 2020) of the COVID-19 crisis.1 , 2 , 4 , 7 , 13-15 In addition, societal and habitual changes during lockdown periods may have contributed to the decrease in potential organ donors. One example could be the decrease in the number of traumatic brain injuries because of falls and road traffic accidents.16
As the numbers of COVID-19–infected patients began to decline toward the end of spring and early summer 2020, transplant activities in the ET region recovered slightly, although they remained below the level of the previous 5 y. With the emergence of the second wave by the end of summer 2020 (third period in our observation), ODT activities again significantly declined, comparable with period 1. This finding cannot be attributed to recommendations to postpone organ transplantations but probably reflects the need to again convert surgical units and ICUs to COVID-19 units. Although it may seem that our experience from the first wave was of little help in sustaining ODT activity during the second wave, it is important to acknowledge that the daily incidence of COVID-19 infections was disproportionately higher in winter 2020 to 2021 than in spring 2020 (Figure 1 ). The fact that ODT activity remained comparable suggests that efforts to maintain transplant volume during the second wave of the pandemic were partially successful. These include, for example, coordinated interdisciplinary management of surgical volume and intensive care capacity.15 Also, the increasing availability of tests and protective equipment may have contributed to the stabilization of ODT activity in the third trimester.
In conclusion, despite the lessons learned from the first wave and the significant efforts made during the second wave to stabilize transplant activity, the number of ODTs dramatically decreased also during the second wave compared with the same period in previous years; however, it must be emphasized that, despite the severity of the second COVID-19 wave, the decline was not greater than that of the first wave.
ACKNOWLEDGMENT
We are indebted to the Eurotransplant International Foundation for providing the data.
REFERENCES
1. Giovinazzo F, Avolio AW, Galiandro F, et al. Solid organ transplantation during COVID-19 pandemic: an international web-based survey on resources’ allocation. Transplant Direct. 2021;7:e669.
2. Putzer G, Martini J, Gasteiger L, et al. Liver transplantation activity in the Eurotransplant area is recovering slowly during the COVID-19 crisis. Transplant Direct. 2020;6:e611.
3. Domínguez-Gil B, Fernández-Ruiz M, Hernández D, et al. Organ donation and transplantation during the COVID-19 pandemic: a summary of the Spanish experience. Transplantation. 2021;105:29–36.
4. Cholankeril G, Podboy A, Alshuwaykh OS, et al. Early impact of COVID-19 on solid organ transplantation in the United States. Transplantation. 2020;104:2221–2224.
5. Reddy MS, Hakeem AR, Klair T, et al. Trinational study exploring the early impact of the COVID-19 pandemic on organ donation and liver transplantation at national and unit levels. Transplantation. 2020;104:2234–2243.
6. Heldman MR, Kates OS, Safa K, et al.; UW COVID-19 SOT Study Team. Changing trends in mortality among solid organ transplant recipients hospitalized for COVID-19 during the course of the pandemic. Am J Transplant. 2022;22:279–288.
7. Zaidan M, Legendre C. Solid organ transplantation in the era of COVID-19: lessons from France. Transplantation. 2021;105:61–66.
8. Contributors to the C4 article. C4 article: implications of COVID-19 in transplantation. Am J Transplant. 2021;21:1801–1815.
9. Chang SH, Wang M, Lentine KL, et al. Solid organ transplantation during the COVID-19 pandemic in the United States. Transpl Int. 2021;34:1319–1321.
10. Weiss MJ, Hornby L, Foroutan F, et al. Clinical practice guideline for solid organ donation and transplantation during the COVID-19 pandemic. Transplant Direct. 2021;7:e755.
11. Weiss MJ, Lalani J, Patriquin-Stoner C, et al. Summary of international recommendations for donation and transplantation programs during the coronavirus disease pandemic. Transplantation. 2021;105:14–17.
12. Klein SJ, Bellmann R, Dejaco H, et al. Structured ICU resource management in a pandemic is associated with favorable outcome in critically ill COVID-19 patients. Wien Klin Wochenschr. 2020;132:653–663.
13. Loupy A, Aubert O, Reese PP, et al. Organ procurement and transplantation during the COVID-19 pandemic. Lancet. 2020;395:e95–e96.
14. Aubert O, Yoo D, Zielinski D, et al. COVID-19 pandemic and worldwide organ transplantation: a population-based study. Lancet Public Health. 2021;6:e709–e719.
15. Chan EG, Chan PG, Harano T, et al. Trends in lung transplantation practices across the United States during the COVID-19 pandemic. Transplantation. 2021;105:187–192.
16. Lester A, Leach P, Zaben M. The impact of the COVID-19 pandemic on traumatic brain injury management: lessons learned over the first year. World Neurosurg. 2021;156:28–32.