key: cord-0763967-jkfaj5wl authors: Merola, Jonathan; Schilsky, Michael L.; Mulligan, David C. title: The Impact of COVID‐19 on Organ Donation, Procurement and Liver Transplantation in the United States date: 2020-09-29 journal: Hepatol Commun DOI: 10.1002/hep4.1620 sha: b5fdbeeba529721aeb6e2c08e3625a35d12ce78b doc_id: 763967 cord_uid: jkfaj5wl The Coronavirus Disease 2019 (COVID‐19) pandemic has had an impact on all facets of our health care system, including life‐saving procedures like organ transplantation. Concerns for potential exposure to the causative severe acute respiratory syndrome coronavirus type 2 (SARS‐CoV‐2) have profoundly altered the process of organ donation and recovery that is vital to the execution of organ transplantation. Issues regarding adequate donor evaluation and consent, organ recovery, organ procurement organization (OPO) and donor hospital resources as well as the transplant center’s acceptance of organ offers for their candidates have all required new practice paradigms. Consequently, the ability to treat patients with organ failure, in particular patients with end stage liver disease where no temporizing treatments exist, and to obtain expected excellent outcomes for new liver transplant recipients has been challenged during this time. We summarize some of the negative effects of the current pandemic on organ recovery and liver transplantation as well as offer considerations and strategies for their mitigation that could have a lasting impact on the field even after COVID‐19 has waned. COVID-19 in recent months has had a substantial impact on the transplant community. The potential for viral transmission from donor to recipients or to and from healthcare workers has imposed new and significant risks, altering the ability to safely recover organs and perform transplants. Solid organ transplantation is considered as highly necessary and essential, earning the designation by the Center for Medicare Services (CMS) as a tier 3b procedure that should continue even when other elective surgical procedures are curtailed.(1) While this was a necessary condition to be able to continue the process of organ recovery and transplantation, this designation was likely too broad and did not apply to all transplants. Patients with stable disease as well as for those awaiting scheduled elective living donor transplants have in many cases been able to safely defer surgery until after the incidence peak of the pandemic subsided. The decision to proceed with transplantation was judiciously determined by each transplant center. In most cases, living donor transplantation, especially liver donation, was deferred enabling healthy donors to follow recommended stay-at-home guidelines. In contrast, deceased donor liver transplantation has been continually pursued in those with the greatest disease severity (highest Model for End-Stage Liver Disease scores). The pandemic due to SARS-CoV-2 has caused a major disruption of the process of organ donation and recovery, resulting in declining rates of overall organ recovery (Figure 1). (2) This disease process affected multiple regions in the US to varying degrees and at different time points depending on the incidence and prevalence of COVID-19. As organ recoveries and living donation have markedly diminished, liver transplantation decreased nationally by more than 25% between This article is protected by copyright. All rights reserved Donor history and COVID-19 testing have become a routine part of the process of donor evaluation. Ideally, there should be no history of exposure to SARS-CoV-2 or symptoms suggestive of coronavirus disease, rapid access to reliable diagnostics and necessary imaging studies. However, even with testing some transmission of coronavirus has occurred from asymptomatic patients through direct interaction. In addition, testing protocols are not standardized nationally, and current tests have significant false negative results. Moreover, access to sensitive imaging such as computed tomography (CT) of the chest is not always readily available, though society guidelines do not recommend its use as a routine screening strategy (4). Due to the risk of transmission to staff during recovery when teams move between centers and regions, there is now a stronger emphasis on local organ recovery for organ procurements. Moreover, the perioperative care and staffing of recovery and intensive care units required for organ recipients has become more limited due to safety from exposure to COVID-19 and staff reassignment to areas of need in hospitals. Collectively, these have forced the need for greater vigilance in organ acceptance for waitlisted registrants and in some instances has deferred the execution of transplants. The issues that have directly or This article is protected by copyright. All rights reserved indirectly resulted from the COVID-19 pandemic which have altered practices surrounding organ donation and transplantation are the subject of the following review. Guidelines from UNOS/OPTN, the American Association for the Study of Liver Disease (AASLD) and the American Society of Transplant Surgeons (ASTS) strongly recommend that donor history and rapid COVID-19 testing be a routine part of the donor and recipient evaluation. (5, 6) Assessment of exposure to SARS-CoV-2 has been challenging due to the potential for asymptomatic patients to spread disease, and there initially were great difficulties in obtaining timely testing for this virus. Many local medical centers and OPOs are only now beginning to obtain consistent access to rapid COVID-19 testing kits and machines for running the assays. Prior methodology turnaround required up to 12 hours before a negative test result was confirmed. There is also significant variability in false negative rate ranging from 2% up to 30-40% in testing for SARS-CoV-2 by nasopharyngeal (NP) swabs.(7) (8) This limits reliance on these tests, particularly in the setting of high clinical suspicion. In settings with high suspicion for COVID-19 exposure, bronchoalveolar lavage (BAL) is the most effective method for viral detection and has a very low false negative rate. However, performing BAL carries the risk of aerosolization of respiratory secretions and is often challenging to obtain in a short time window. Further, BAL has the greatest sensitivity later in the course of the infection whereas NP swab testing has greatest sensitivity during the early period. There is recent evidence that sputum testing for SARS-CoV-2 is even more reliable and sensitive during both the early and late periods of the disease. (9) Development of newer, more accurate and rapid testing will hopefully improve in the near future. This article is protected by copyright. All rights reserved Procurement of deceased donor organs for transplantation has traditionally relied on surgical teams from the recipient centers traveling sometimes significant distances to execute recovery procedures at the donor medical centers, many of which do not have sufficient protective equipment requiring the donor surgical teams to bring their own for the travel and the operations. The current epidemic has imposed greater risks to donor recovery teams. An incident of a team from a high prevalence region with an asymptomatic but COVID-19 positive healthcare worker exposing healthcare workers in the organ recovery operating room who later became infected with COVID-19 has been reported. This led to strong recommendations by UNOS/OPTN and later the ASTS for greater collaboration and reliance on local donor recovery teams. (5) This move to local donor recovery necessitates improved communications between teams and OPOs as well as the use of technology for digital imaging, digital microscopy, and even video sharing across secure platforms like DonorNet, which are actively being implemented. Successful organ donation relies on donor hospitals for the timely relocation of potential donors to non-COVID-19 intensive care units (ICUs) and to obtain the necessary testing as screening measures to exclude SARS-CoV-2 and pneumonitis caused by the virus respectively. In the face of the COVID-19 pandemic, it was not uncommon for patients meeting brain death criteria to take an additional 36 to 48 hours of ICU bed and ventilator time in order that appropriate testing and history taking can be done. Moreover, family consent and organ placement processes are often initiated before recovery operating room times can be set. Under the constraints of COVID-19, hospital bed and ventilator shortages as well as staffing shortages made demands for a potential organ donor evaluation that were often unable to be accommodated. Additionally, availability of blood products at times was limited due to This article is protected by copyright. All rights reserved decreased donation rates in areas affected by COVID-19. Further, hospital visitor restrictions of family members or next-of-kin posed a barrier to obtaining timely donation consent. The performance of donation after circulatory death (DCD) donation was made even more difficult as that required the ICU physician to be removed from the clinical unit so that the prospective donor can be removed from mechanical ventilatory support and allowed to expire. This required time away from clinical care for the ICU physician who was needed for the care of other critical patients in the ICU. Due to staffing shortages, many hospitals declined opportunities for organ donation. Overall, UNOS data revealed a 25% decrease in the number of deceased donor livers recovered between February and April 2020. (2) Moving forward, establishment of neutral recovery sites run by organ procurement organizations (OPOs) may minimize exposure to both donor and recipient teams and enable consistent recovery and testing practices within individual regions. One current impediment in moving this forward has been the lack of financial reimbursement for transplant centers sending deceased donor organs to centralized recovery facilities for procurement, which are not counted in the hospital's usable organ count as "organs sent to OPOs." (10) Altering the language for the CMS protocol which allows transplant centers to count donors as in-house among those who were "consented" rather than only if organs are "recovered" would mitigate financial burdens on already strained healthcare systems who opt to utilize centralized procurement facilities. Organ recovery centers, whether off site or on site at the transplant centers have the potential to allow more efficient, expeditious and timely recoveries of solid organs that could also mitigate many of the issues created by COVID-19 to protect OPO and hospital staff, allowing better communication with families, and liberating demands faced by transplant centers to focus on recipient patients.(11) Doing so would limit transportation to package movements rather than staffed teams, which are much less costly and easier to obtain. This article is protected by copyright. All rights reserved This article is protected by copyright. All rights reserved COVID-19 pandemic such that centers should not fear of being penalized for low volumes while practicing in a manner to protect their patients during the critical phases. (2) As our community has learned to co-exist with COVID-19 and the incidence has diminished, we have seen that liver transplant volumes have begun to increase, approaching the rates prior to the pandemic. Lessons learned from this COVID-19 pandemic for liver transplantation as we evolve into a new normal are many. We have learned to rapidly improve communication with our teams and the hospital resource managers, between transplant centers and OPOs, across our oversight organizations and professional societies, and most importantly with our patients. We have navigated assimilation of Telehealth into our practices and learned how often we actually need physical visits and labs compared to what we had become accustomed to utilizing. Incorporation of Telehealth has required weighing the advantages of mitigating exposure risks, increasing patient convenience and decreasing care costs with the challenges of incorporating new technology platforms and reducing the ability to perform clinical physical exams. We learned how to connect with technology between donor teams and transplant centers and what other forms of transportation could work effectively to transport organs rather than entire organ recovery teams and will realize the financial impacts of that change in practice. Utilization of DCD livers and living donors will continue to serve an unmet need for access to transplant but may be variable in the current environment given uneven regional trends in viral mitigation and the potential resurgence of new infections. The postponement of DCD organ utilization for fear of organ quality compromise and poor transplant outcomes, not to mention the admissions and exposures in the hospitals of the candidates hoping the donor will progress in time with minimal ischemic injury, will certainly lead to a total decrease in deceased liver transplantation in the US. In addition, the delay in living donor liver transplantation for caution against exposing a normal healthy donor to COVID-19 as they This article is protected by copyright. All rights reserved recover from major surgery, will also contribute to a decline in total liver transplantation. If ever a donor becomes infected with significant sequelae of SARS-CoV-2, it will have serious ramifications and impact living donation all across the country. Therefore, we will need to This article is protected by copyright. All rights reserved Perhaps more widespread and reliable testing, vaccination, and more successful treatments will restore patient and healthcare personnel confidence in our medical systems. The future may bring a workforce of organ recovery surgeons managed by the OPOs with streamlined technologies to share images and micrographs and better point to point transportation of organs which is less expensive due to less need to transport organ recovery teams. There will likely be regional centers for organ regeneration/resuscitation which will have multiple organ perfusion devices to assess and improve organ function before sending them to the recipient centers for transplantation. This would enhance the use of potentially marginal livers and livers obtained by deceased cardiac donation as well as improve timing of the transplant operation to ensure optimal resources and personnel are available at the transplanting center. Successful liver transplantation is a complex process that is reliant on many factors that have been challenged in the COVID-19 pandemic. These factors include adequate donor evaluation, organ recovery, the availability OPO and donor hospital resources, as well as the transplant center's acceptance of organ offers for their candidates and their own resources for performing transplants (ICU beds, ventilator availability, blood product availability, staff, etc.), all of which have been significantly altered by the COVID-19 pandemic. To successfully improve organ donation in the era of COVID, we must facilitate reliable and timely testing that is widespread, limit travel for personnel from transplant centers and promote local or centralized organ recoveries. To balance risks and benefits, we must also re-prioritize waitlisted registrants and determine the relative resources and risks of performing transplantation at a given transplant center depending on the geographic constraints and local information regarding the incidence of COVID-19 in the hospital and community at a given time. Navigating these hurdles can help the transplant community educate staff and the public about challenges facing organ donation and hopefully improve and maximize the availability of needed resources to ensure that patients with end stage This article is protected by copyright. All rights reserved liver disease continue to receive timely and safe liver transplantation. There are many lessons that will be learned during this pandemic which will change transplantation as a whole for the better and allow more patients to receive life-saving organs with excellent longterm outcomes. United Network for Organ Sharing. Current state of donation and transplantation United Network for Organ Sharing. COVID-19 refusal codes for transplant hospitals implemented ACR Recommendations for the use of Chest Radiography and Computed Tomography (CT) for Suspected COVID-19 Infection Economics/ACR-Position-Statements/Recommendations-for-Chest-Radiography-and-CTfor-Suspected-COVID19-Infection American Association for the Study of Liver Disease. Clinical Best Practice Advice for Hepatology and Liver Transplant Providers During the COVID-19 Pandemic: AASLD Expert Panel Consensus Statement 2020 Detection of SARS-CoV-2 in Different Types of Clinical Specimens Comparison of SARS-CoV-2 detection in nasopharyngeal swab and saliva Saliva is more sensitive for SARS-CoV-2 detection in COVID-19 patients than nasopharyngeal swabs 2020 The First 2 Years of Activity of a Specialized Organ Procurement Center: Report of an Innovative Approach to Improve Organ Donation Changes in liver transplant center practice in response to COVID-19: Unmasking dramatic center-level variability Determining risk factors for mortality in liver transplant patients with COVID-19 This article is protected by copyright. All rights reserved This article is protected by copyright. All rights reserved This article is protected by copyright. All rights reserved