Korean J Transplant 2023; 37(3): 145-154
Published online September 30, 2023
© The Korean Society for Transplantation
Si-Ho Kim1 , Yu Mi Wi1 , Chisook Moon2 , Ji-Man Kang3 , Minhwa Kim4 , Jungok Kim5 , Jong Man Kim6 , Hyeri Seok7 , Hye Jin Shi8 , Su Jin Lee9 , Ji Yeon Lee10 , Su Jin Jeong11 , Pyoeng Gyun Choe12 , Kyungmin Huh13 , Sang-Oh Lee14 , Sang Il Kim15; Transplant Infection Research Committee of the Korean Society of Infectious Diseases
1 Division of Infectious Diseases, Samsung Changwon Hospital, Sungkyunkwan University School of Medicine, Changwon, Korea
2 Division of Infectious Diseases, Department of Internal Medicine, Inje University Busan Paik Hospital, College of Medicine, Inje University, Busan, Korea
3 Department of Pediatrics, Severance Children's Hospital, Yonsei University College of Medicine, Seoul, Korea
4Korea Organ Donation Agency, Seoul, Korea
5Division of Infectious Diseases, Chungnam National University Sejong Hospital, Sejong, Korea
6Department of Surgery, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Korea
7 Division of Infectious Diseases, Department of Medicine, Korea University Ansan Hospital, Korea University College of Medicine, Ansan, Korea
8 Division of Infectious Diseases, Department of Internal Medicine, Gachon University Gil Medical Center, Gachon University College of Medicine, Incheon, Korea
9 Division of Infectious Disease, Department of Internal Medicine, Pusan National University Yangsan Hospital, Yangsan, Korea
10 Division of Infectious Diseases, Keimyung University Dongsan Hospital, Keimyung University School of Medicine, Daegu, Korea
11 Department of Internal Medicine, Yonsei University College of Medicine, Seoul, Korea
12Department of Internal Medicine, Seoul National University College of Medicine, Seoul, Korea
13 Division of Infectious Diseases, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Korea
14 Department of Infectious Diseases, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Korea
15Department of Internal Medicine, College of Medicine, The Catholic University of Korea, Seoul, Korea
Correspondence to: Chisook Moon
Division of Infectious Diseases, Department of Internal Medicine, Inje University Busan Paik Hospital, College of Medicine, Inje University, 75 Bokji-ro, Busanjin-gu, Busan 47392, Korea
Yu Mi Wi
Division of Infectious Diseases, Samsung Changwon Hospital, Sungkyunkwan University School of Medicine, 158 Paryong-ro, Masanhoewon-gu, Changwon 51353, Korea
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.
We present a summary of the evidence on testing for severe acute respiratory syndrome coronavirus-2 (SARS-CoV-2) and organ procurement from deceased donors and provide recommendations based on current clinical data and the guidelines from major transplant organizations. Because of the limited historical experience with coronavirus disease 2019 (COVID-19), certain recommendations in this document are based on theoretical rationales rather than clinical data. The recommendations in this manuscript may be subject to revision as subsequent clinical studies provide definitive evidence regarding COVID-19 in organ procurement.
Keywords: COVID-19, SARS-CoV-2, Tissue and organ procurement, Organ transplantation, Tissue donors
The coronavirus disease 2019 (COVID-19) pandemic caused significant changes in organ donation and the transplantation environment worldwide, including a decrease in the number of donors and the availability of intensive care units . With a lack of research on the transmission of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) via organs in the early stages of the pandemic, it was recommended that transplantation of organs from deceased donors who tested positive for SARS-CoV-2 be avoided . Subsequently, short-term observations showed the transmission of SARS-CoV-2 via organ transplantation in lung transplants only, accompanied by increasingly many reports of favorable outcomes in extrapulmonary organ transplantation from SARS-CoV-2-infected deceased donors [3-5]. Based on the guidelines of major transplant organizations, this study summarizes the available data for evaluating deceased donors for SARS-CoV-2 and the considerations for organ procurement from deceased donors with a history of COVID-19. Our recommendations can be revised as new data become available. A summary of the study recommendations is presented in Supplementary Material 1.
The personal protective equipment (PPE) requirements for COVID-19 such as masks (N95 equivalent), face shields, gloves, and gowns should follow the guidelines of the institution where the organ is recovered.
The donor’s COVID-19 history and history of close contact with COVID-19 patients should be obtained.
The major national guidelines recommend testing respiratory specimens for SARS-CoV-2 using a polymerase chain reaction (PCR) test and obtaining specimens as close as possible to the time of organ procurement (Table 1). The Organ Procurement and Transplant Network (OPTN)  in the United States recommends obtaining a respiratory specimen for SARS-CoV-2 PCR testing within 72 hours of planned organ procurement. For lung procurement, a PCR test for SARS-CoV-2 on both upper and lower respiratory tract specimens is advised. There is insufficient evidence to support a recommendation for the PCR testing of nonpulmonary organs, tissues, or body fluids .
The Transplantation Society of Australia and New Zealand (TSANZ)  recommends PCR testing for SARS-CoV-2 on nasopharyngeal specimens obtained within 24 hours (up to 48 hours) of planned organ procurement for all deceased donors. Testing for SARS-CoV-2 in the lower respiratory tract is strongly recommended for lung procurement and is also encouraged for organ donation outside of the lungs. While tracheal aspiration for specimen collection is permitted, TSANZ recommends obtaining specimens through bronchoscopy in deceased donors with a previous history of COVID-19 infection.
The National Health Service (NHS)  guidelines in the UK recommend PCR testing for SARS-CoV-2 on nasal, nasopharyngeal, and tracheal aspirate specimens obtained within 24 hours (up to 48 hours) of planned organ procurement for all deceased donors. Among the 2,469 organ recoveries (including 75 lung recoveries) performed in the UK as of January 2021, 987 deceased donors had negative PCR tests for SARS-CoV-2 in both upper and lower airway specimens, and there was no evidence of COVID-19 transmission by solid organ transplantation .
The Canadian Society of Transplantation  recommends PCR testing for SARS-CoV-2 on upper and lower respiratory tract specimens obtained within 24 hours of planned organ procurement for all deceased donors. The Centro Nazionale Trapianti (Italian Transplantation Society; CNT)  in Italy recommends PCR testing for SARS-CoV-2 in nasopharyngeal or lower respiratory tract specimens (bronchoalveolar lavage) obtained 24–48 hours prior to organ procurement in deceased donors. The Italian guidelines also suggest tissue testing for SARS-CoV-2 and histopathological evaluation for the liver and kidney, as well as PCR testing for SARS-CoV-2 in organ preservation fluid.
Higher cycle threshold (Ct) values are frequently associated with lower viral loads and negative culture results, but there may be variations in results between individuals and different respiratory specimens . Therefore, Ct values can be used as an adjunct tool to determine the potential for SARS-CoV-2 transmission, but are not recommended as an absolute criterion.
Due to a lack of research data, SARS-CoV-2 antibody testing is not recommended for assessing the safety or potential transmission risk to recipients.
Although chest computed tomography in COVID-19 patients can be helpful for early diagnosis and stratification of disease severity, its routine use for clinical decision-making regarding organ suitability or the characterization of organ donors is not recommended due to the limited sensitivity and specificity of this method [12,13].
Procuring the lungs and small bowel from deceased patients with COVID-19 and a presumed risk of respiratory transmission is not recommended due to concerns for potential SARS-CoV-2 transmission and the limited experience with transplantation cases. In lung and intestinal transplantation, there is a possibility of COVID-19 transmission for 20 days after the onset of symptoms in the infected donor. Therefore, the procurement of lungs and small bowel from patients with COVID-19 is recommended only after this period of potential transmission risk (Fig. 1).
Cases were reported during the early phase of the pandemic in which COVID-19 was transmitted via lung transplantation from deceased donors who tested positive for SARS-CoV-2. The Disease Transmission Advisory Committee in the United States plays a role in evaluating and classifying the potential for transmission of infectious diseases during organ transplantation. Between March 2020 and March 2021, a total of 27 cases of COVID-19 were reported among recipients, and nine cases were reported among donors. Three of these cases involved COVID-19 transmission via lung transplantation from donors with COVID-19. In all three cases, the upper respiratory COVID-19 PCR test conducted prior to transplantation was negative, but the lower respiratory COVID-19 PCR test performed immediately after transplantation was positive [14,15]. As a result, the OPTN issued an urgent recommendation that starting May 27, 2021, all deceased donors with the potential for lung procurement must undergo testing of lower respiratory tract specimens for SARS-CoV-2 before proceeding with organ procurement . Most countries, including the United States, currently do not recommend recovering lungs from COVID-19 patients with a presumed risk of respiratory transmission [6,8-10,17]. After this urgent recommendation, the OPTN reported that from May 27, 2021, to January 31, 2022, a total of 22 lung recoveries and transplantations had been performed from patients who tested positive for SARS-CoV-2 by PCR. In the 11 reported cases with available follow-up data, no deaths or transplant failures were observed within 30 days . In 10 of the 11 cases, the upper respiratory tract tested positive for SARS-CoV-2 while the lower respiratory tract tested negative (Table 2). Therefore, if only the upper respiratory tract PCR test is positive, lung transplantation could be considered for critically ill patients with high priority, if sufficient explanation is provided and consent is obtained from the patient and their guardians.
The potential risk of COVID-19 transmission may be higher in the small bowel than in other organs due to its abundant distribution of lymphoid tissue and the requirement for intense immunosuppression after transplantation . In the OPTN data mentioned earlier, there were only two cases of small bowel procurement and transplantation within 21 days of a positive PCR result for SARS-CoV-2, and no information regarding the outcomes of these cases was provided . Due to the lack of sufficient evidence to ensure safety, the guidelines from most countries did not recommend procurement of intestines from COVID-19 patients [6,8-10,17].
The respiratory transmission period for COVID-19 may vary according to the severity of the infection. For mild COVID-19, this period lasts approximately 10–14 days from the onset of symptoms, whereas for severe COVID-19, it can last approximately 20 days . In a study conducted during the Omicron variant phase of the pandemic, the positivity rate for the viral cultures of respiratory specimens from patients with mild COVID-19 was reported as 17% between days 6–10 after symptom onset . Another study reported that the positivity rates for the cultures of respiratory specimens were 13.5% on day 10 and 8% on day 14 after symptom onset . In addition, a positive PCR result for SARS-CoV-2 90 days or more after the initial infection was more likely to reflect a new infection caused by a different virus rather than a repeat detection of the previous infection . These data are currently being used in transplantation guidelines to manage the timing of transplantation and the potential for virus transmission. In the OPTN guidelines in the United States, even if a donor with a history of COVID-19 shows a positive PCR result for SARS-CoV-2 within 21–90 days from the diagnosis, it is considered a repeat detection of the previously resolved virus, and organ procurement and transplantation, including lungs, are recommended. In other guidelines, if it has been more than 90 days since the initial diagnosis, the likelihood of reinfection is high, and lung procurement and transplantation are not recommended . In Spain, the guidelines recommend considering standard-risk donors for transplantation procedures if 21 days have elapsed since the onset of symptoms for lung and small bowel transplants and 14 days or more for other organs . However, guidelines from the NHS in the UK, as well as the TSANZ guidelines in Australia and New Zealand, do not recommend the procurement of lungs or intestines from deceased donors in all PCR-positive cases of SARS-CoV-2, regardless of the timing of infection [8,9].
Although the data were limited, there were reported cases of lung procurement and transplantation in Korea from two adult deceased donors who tested positive for SARS-CoV-2. The time elapsed after each donors’ COVID-19 diagnosis was 24 days and 56 days. The outcomes of the recipients were not reported (Table 3).
If sufficient explanation is provided and consent is obtained, nonlung and non-small bowel solid organ procurement can be considered from deceased donors with COVID-19. The risk of COVID-19 transmission through nonlung and non-small bowel solid organs is very low. For organs other than the lungs and small bowels, if 14–90 days have passed since the onset of COVID-19 symptoms, they can be considered to have the same risk level as donors who are PCR-negative for COVID-19, even if the PCR test for SARS-CoV-2 is positive at the time of transplantation (considered reinfection if positive after 90 days) (Fig. 1).
The procurement of nonlung and non-small intestine solid organs from patients diagnosed with COVID-19 has been consistently performed even if they had active SARS-CoV-2 infection or were diagnosed during the pretransplantation evaluation process. Italy, one of the countries that experienced the COVID-19 pandemic earliest, allowed the acquisition and transplantation of organs from COVID-19 deceased donors for patients in need of emergency transplantation as authorized by the CNT from November 2020. In the following 3 months, a total of 10 liver transplantations from patients with COVID-19 were performed at five institutions. Among the 10 donors, three were diagnosed with COVID-19 at the time of organ acquisition, while the remaining seven were diagnosed within 10 days before transplantation. Tissue examinations were conducted on the livers obtained from nine patients, and no SARS-CoV-2 was detected in the tissue samples. As for the recipients, there were no suspected cases of COVID-19 transmission through transplantation, and (except for one patient who died due to sepsis) all recipients survived for more than 5 months . A study evaluating SARS-CoV-2 in the plasma and renal tissue of 24 kidney transplant recipients with COVID-19 reported that the virus was not detected in either the donors’ plasma or renal tissue . Based on this evidence, the organ procurement and transplantation of nonlung and non-small bowel organs from COVID-19 patients has increased worldwide. Data from the OPTN in the United States, from May 2021 to January 2022, show that 617 organs were recovered from donors who were positive for COVID-19 (within 21 days of initial diagnosis), and 1,241 organ recipients were identified. Among these recipients, which included 776 kidney, 316 liver, and 106 heart transplant cases, the 30-day graft failure and mortality rates were like those of recipients who received organs from donors who were negative for COVID-19. Furthermore, there were no confirmed or probable cases of COVID-19 transmission through transplanted organs, except for one possible case . Another study using OPTN data, limited to COVID-19-positive donors within 14 days of the initial diagnosis, found that the outcomes of transplant recipients were like those of recipients who received organs from COVID-19-negative donors . Although the reported cases were limited in number, both the UK and Spain reported organ transplantations from donors who were positive for COVID-19 with no transmission to the recipients. Furthermore, the outcomes of the recipients were favorable [3,4] (Table 2). Thus, although patients with COVID-19 are generally considered to be a risk for transmission through the respiratory route, it can be inferred that: (1) SARS-CoV-2 is not detected in nonlung organs, (2) transplantation of organs from donors who are positive for COVID does not result in the transmission of COVID-19, and (3) the short-term posttransplant outcomes for recipients appear not to be affected. According to the OPTN guidelines, procurement of nonlung organs can proceed from donors who are 10–21 days past a mild COVID-19 infection, since the risk of transmitting COVID-19 to the recipient is considered very low. Even if the donor is diagnosed with COVID-19 for the first time during the evaluation process for organ procurement, the transplantation of nonlung organs can be considered . According to the NHS and TSANZ guidelines, if a sufficient explanation is provided and consent is obtained, the procurement and transplantation of nonlung organs from COVID-19-positive donors can be considered. These guidelines do not differentiate recommendations based on the specific timing of the COVID-19 diagnosis. However, it is explicitly stated that COVID-19 should not be the cause of death in the case of deceased donors [8,9]. In Spain, even if the donor is diagnosed with COVID-19 at the time of organ recovery or within 14 days of diagnosis, the donor can be evaluated as a nonstandard-risk donor and considered for transplantation in cases where emergency transplantation is necessary for the recipient. This can be done with patient consent after sufficient explanation that they have not been evaluated as being at the standard level of risk . According to the guidelines in Spain, if COVID-19 is the cause of death, transplantation is contraindicated. However, cases have been reported in the United States of organ procurement and transplantation from donors who died from COVID-19, but there are no reports of COVID-19 transmission or transplant failure associated with the organs transplanted from such donors . Therefore, there is insufficient evidence to universally prohibit organ procurement and transplantation based solely on donor death from COVID-19. More studies are needed to further evaluate this issue.
According to data from the Korean Network for Organ Sharing, a total of 14 kidney, 6 liver, 4 heart, and 1 pancreas transplant cases were reported from seven deceased donors who were positive for SARS-CoV-2. Among the cases, one deceased donor was a pediatric patient. The time interval between organ procurement and COVID-19 diagnosis ranged from 3 to 56 days. One liver transplant recipient experienced graft loss and death, while the outcomes of the remaining patients were not reported (Table 3).
If the upper and lower respiratory tract samples from deceased donors with a history of COVID-19 yield negative SARS-CoV-2 test results, the likelihood of SARS-CoV-2 transmission via the transplanted organs is expected to be significantly low.
As previously mentioned, according to the NHS, in cases in which both upper and lower respiratory tract samples yield confirmed negative PCR results for SARS-CoV-2, there has been no evidence of COVID-19 transmission through organ procurement and transplantation . However, in lung transplantation, there have been reported cases of COVID-19 transmission via the lungs of donors with negative upper respiratory tract samples but positive lower respiratory tract samples. Therefore, it is necessary to confirm negative SARS-CoV-2 test results in lower respiratory tract samples before lung transplantation [6,8,9,14,16]. When deciding on organ transplantation from a deceased donor with a history of COVID-19, if the respiratory tract samples show a negative PCR test for SARS-CoV-2, the possibility of transmission through the transplanted organs is expected to be very low. However, it is important to obtain informed consent from the recipient after sufficient explanation of the theoretical possibility of transmission .
Based on previous research on the long-term outcomes of COVID-19 infection, it cannot be completely ruled out that deceased donors with a history of COVID-19 may experience end-organ dysfunction associated with COVID-19. Therefore, a thorough evaluation of the organs should be conducted prior to transplantation to assess for the possibility of such complications [25-28]. There is a lack of research on the long-term outcomes for the recipients of organs from deceased donors with a history of COVID-19. Therefore, when deciding on organ transplantation, it is important to consider the potential risks of delaying transplantation and thereby aggravating underlying diseases and complications in the recipient versus the possibility of late complications due to the functional deterioration of the transplanted organ related to the donor’s past COVID-19 infection .
It remains unclear whether there is a possibility of SARS-CoV-2 transmission via organs transplanted from deceased donors with a history of close contact with COVID-19 patients (within 7 or 10 days) but who tested negative for SARS-CoV-2. From the current reports, there have been no documented cases of COVID-19 transmission through organ transplantation from deceased donors who had close contact with COVID-19 patients but tested negative for SARS-CoV-2 [6,8,9,29].
If test results are negative during the evaluation process for organ procurement, there is a possibility that the deceased donor who had close contact with a COVID-19 patient might have been tested during the eclipse period (time between infection and test positivity), but it is difficult to clearly distinguish such situations in clinical practice. Previous studies have shown the eclipse period of the SARS-CoV-2 virus to be 7–8 hours or 12–36 hours . While the theoretical possibility is low, the transmission of SARS-CoV-2 to the recipient through lung transplantation cannot be completely ruled out. A case-by-case evaluation and plan are necessary for lung transplantation. However, in nonpulmonary organ transplantation, the transmission risk is considered to be very low or nonexistent .
Conflict of Interest
Jong Man Kim is an editorial board member of the journal but was not involved in the peer reviewer selection, evaluation, or decision process of this article. No other potential conflict of interest relevant to this article was reported.
Conceptualization: CM, YMW. Data curation: SHK, CM, YMW. Validation: JMK. Investigation: all authors. Writing–original draft: all authors. Writing–review & editing: all authors. All authors read and approved the final manuscript.
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