key: cord-0685920-ugka473u
authors: Lentine, Krista L.; Vest, Luke; Schnitzler, Mark A.; Mannon, Roslyn B.; Kumar, Vineeta; Doshi, Mona D.; Cooper, Matthew; Mandelbrot, Didier A.; Harhay, Meera N.; Josephson, Michelle A.; Caliskan, Yasar; Sharfuddin, Asif; Kasiske, Bertram L.; Axelrod, David A.
title: Survey of U.S. Living Kidney Donation and Transplant Practices in the COVID-19 Era
date: 2020-08-25
journal: Kidney Int Rep
DOI: 10.1016/j.ekir.2020.08.017
sha: 7284a2004ba93aed639f9511000d17e5cb9b216f
doc_id: 685920
cord_uid: ugka473u

INTRODUCTION: The scope of the impact of the COVID-19 pandemic on living donor kidney transplantation (LDKT) practices is not well defined. METHODS: We surveyed U.S. transplant programs to assess practices, strategies and barriers to living LDKT during the COVID-19 pandemic. After IRB approval, the survey was distributed 5/9/20–5/30/20 by email and postings to professional society list-servs. Responses were stratified based on state COVID-19 cumulative incidence levels. RESULTS: Staff at 118 unique centers responded, representing 61% of U.S. living donor recovery programs and 75% of LKDT volume in the pre-pandemic year. Overall, 66% reported LDKT surgery was on hold (81% in “high” vs. 49% in “low” COVID-19 cumulative incidence states). Thirty-six percent reported that evaluation of new donor candidates had paused, 27% reported evaluations were very decreased (>0% to <25% typical) and 23% reported evaluations were moderately decreased (25% to <50% typical). Barriers to LDKT surgery included program concerns for donor (85%) and recipient (75%) safety, patients concerns (56%), elective case restrictions (47%) and hospital administrative restrictions (48%). Programs with higher local COVID-19 cumulative incidence reported more barriers related to staff and resource diversion. Most centers continuing donor evaluations used remote strategies (video 82%; telephone 43%). As LDKT resumes, all programs will screen for COVID-19, although timeframe and modalities vary. Recommendations for pre-surgical self-quarantine are also variable. CONCLUSION: The COVID-19 pandemic has had broad impacts on LDKT practice. Ongoing research and consensus-building are needed to reduce barriers, guide optimal practices, and support safe restoration of LDKT across centers.

The declaration of the COVID-19 pandemic in March 2020 and resulting public health emergency has had implications across the spectrum of transplant care processes, including patient evaluation, organ procurement and placement, surgery and early aftercare, and management of immunosuppressed recipients. [1] [2] [3] In the United States, transplant surgery was designated as a tier 3b essential procedure by the Centers for Medicare and Medicaid Services (CMS), establishing that transplant should not be uniformly postponed as 'elective' during the pandemic. 4 However, in practice, the feasibility of transplantation has depended on local COVID-19 disease burden and related resource considerations, as well as perceived medical urgency in balance with potential patient risks. 5 . Although programs across the United States continued lifesaving procedures (heart and high acuity liver transplantation), the numbers of deceased and living donor kidney transplants (LDKT) decreased dramatically in the early weeks of the pandemic. 5 Compared to deceased donor kidney transplantation (DDKT), the impact of the pandemic on LDKT has been particularly striking. During the week of 3/24/20, whereas 80% DDKT programs were operating with restrictions, 72% of U.S. LDKT programs reported full suspension of living donation and transplant activities. In the week ending April 11, only 11 LDKT procedures were performed in the entire United States. 6 LDKT is often considered 'elective' (i.e., distinct from 'essential' DDKT) and possible to safely delay. LDKT has added complexity related to both to the safety the recipient, as early reports suggested that transplant recipients faced substantially increased risk of mortality following SARS-CoV-2 infection, 7, 8 and of the living donor. The dramatic decrease in LDKT clinical activity has important health implications for transplant candidates seeking access to kidney transplantation.

As hospitals resume scheduling and performing elective surgeries, establishing conditions for safe conduct of LDKT activity has become a critical consideration in the transplant community. [9] [10] [11] To facilitate discussions of best practices, we designed a survey to assess the impact of the COVID-19 pandemic on comprehensive elements of living donor candidate evaluation, surgery, follow-up and education practices. Herein we report the findings based on responses at U.S. transplant programs from 5/09/20 to 5/30/20. We also compared responses according to general population COVID-19 cumulative incidence by state to assess the impact of disease burden on LDKT program practices.

J o u r n a l P r e -p r o o f

The survey instrument was developed by the study investigators. Key topics of study interest were identified, and survey items were developed and refined by direct discussion and email between investigators. The final survey instrument comprised 34 questions (Supplementary Table S1 This study was approved as Human Subject Exempt by the Saint Louis University Institutional Review Board.

The target population was transplant program staff at all U.S. LDKT programs (N=194) active in 2020, including surgeons, nephrologists, administrators, coordinators and social workers. Potential participants at all U.S. kidney transplant programs were derived from the working group's professional connections and emailed the survey through the Qualtrics Survey Software. Opportunity for self-elected participation through a Qualtrics link was also posted to professional society list servs (e.g. American Society of Transplantation (AST) Kidney Pancreas Community of Practice (COP), Live Donor COP, and AST Outstanding Questions in Transplantation (OQiT)). COP postings were approved by COP leadership, and the OQiT posting was approved by the AST Education Committee. Data are analyzed from distribution between 05/09/20-5/30/20. The first page of the survey notes that the decision to proceed indicates consent to participate. Up to 2 reminders were provided for non-respondents.

Each program was represented only once in the analysis. For programs with multiple respondents, we selected 1 participant to represent the program using a hierarchical algorithm. First, prioritized responses with the most complete information (i.e. least unanswered items). Next, we prioritized J o u r n a l P r e -p r o o f surveys submitted by transplant surgeons, or nephrologists, over those from coordinators, social workers, administrators, or others. Finally, if any programs had more than 1 response after the above two steps, we retained the earliest submitted survey.

Responses to each survey question were described with either percentages and frequencies or means and ranges, as appropriate. To obtain percentages, we divided the number of program responses (i.e. row totals) by the total number of programs who responded to the question, such that percentages reflect proportions of respondents, as per previous methods. [12] [13] [14] [15] For questions where participants were asked to "select all that apply," the denominator for calculating percentages was the number of participants responding to that question. For these questions, column totals exceed 100%.

LDKT programs were categorized based on the COVID-19 cumulative incidence in their state using data that were published in the New York Times on 5/14/20 incorporating reports by federal, states and local county data health departments. 16 States were categorized into three levels providing approximately equivalent number of programs in each level, as: "low", <200 cases/100,000 population: "moderate", 200 to <500 per 100,000; and "high" >=500 cases per 100,000. Although the sample size of programs was too small for statistical significance (P>0.05 by Chi-square test), stratification by local COVID-19 cumulative incidence strata is presented to assess trends in the relationship of local disease cumulative incidence with living donor care practices.

All analyses were performed using R for windows version 1.2.5042 (RStudio Inc., Boston, MA).

This report describes responses from U.S. LDKT programs. We received responses from 118 unique programs (Supplementary Figure S1) . Respondents represented 61% of U.S. living donor recovery programs and 75% of LKDT volume in the year before pandemic declaration (April 2019-March 11, 2020). Participants were most often transplant nephrologists (47%) or surgeons (38%) ( Table 1 ). All UNOS regions were represented. Programs were drawn from 39 states, with 11, 17, and 11 programs located in states ranked as "low", "moderate", and "high" COVID-19 cumulative incidence, respectively.

Living donation evaluation was significantly reduced by the COVD-19 pandemic, with 36% of programs reporting pausing living donor candidate evaluation during the pandemic ( Table 2) . Among those responding programs that continued living donor evaluation, 82% used video-based evaluation and 43% used telephone-based assessment. In contrast, only 30% of programs reported using in-clinic assessment. For 87% of responding programs, telehealth reflected new technology for living donor evaluation which was driven by the COVID-19 epidemic. Centers reported using this technology predominantly for medical evaluation (76%), social work evaluation (79%), and independent living donor advocate assessments (73%). Conversely, surgical evaluation was still predominantly done in-person, with 37% reporting use of telehealth for surgical evaluation. Importantly, 83% of responding programs require at least one in-person pre-donation evaluation. As a result of impact of COVID-19, 95% of programs reported a reduction in evaluation volume, with more than 90% of programs reporting at least a 50% reduction in their average volume of donor evaluations. Trends in evaluation practices appeared similar across levels of state COVID-19 burden.

Responding programs identified a number of key barriers to proceeding with donor evaluation and testing. Restrictions caused by local stay at home orders (71%) was the most common issue reported, followed by limited access to evaluation testing (63%), donor concern/refusal (61%), and reduced donor inquires (38%). Patterns appear to be generally similar across COVID-19 cumulative incidence groups (Table 3) . Although the majority of responding programs continued laboratory testing (56%); of those continuing lab testing, many incorporated local testing in community labs (74%) and some are using home-based phlebotomy (17%). Testing appeared to decline more in high COVID-19 burden areas, where 52% of responding programs reported stopping testing compared with 35% of program in low cumulative incidence states. In contrast, 61% of responding programs reported halting other types of testing (e.g. radiology and cardiac testing), with minimal differences by local burden of COVID-19 infection.

Living donation/transplant surgery practices and pre-surgical screening LDKT surgery has been largely curtailed during the epidemic (Figure 2 ). Volume was decreased by at least 50% of pre-pandemic levels at 93% of responding programs, with 66% of programs halting LDKT completely. Programs in the highest COVID-19 cumulative incidence states were more likely to have paused LDKT (81%) compared with programs in low cumulative incidence states (49%). Among the barriers cited to proceeding with LDKT, program concern for donor safety (85%), concern for recipient safety (75%), and patient reluctance (56%,) were the most common reasons (Figure 3) . Government restrictions on 'elective' cases was cited in 60% of programs in high cumulative incidence areas and 27% of low cumulative incidence areas. The majority of programs that reported interruptions also reported plans to restart LDKT within the next month. Overall, 72% of programs elected to pause kidney paired donation (KPD) programs with minimal variation by disease burden.

To ensure safe practice, all programs plan to implement predonation testing for COVID-19 by polymerase chain reaction (PCR). In addition, 19% of programs reported use of serum IgG testing, which varied from 16% in low cumulative incidence areas to 26% in high cumulative incidence areas (Table 5) .

COVID-19 testing was performed at the hospital lab in 93% of programs, while 13% reported using community labs and 4% are using a public health lab. Timing of testing varies by center with 25% requiring testing within 24 hours, 48% within 48 hours, and the remainder within 72 hours of donation surgery. Program practice regarding self-quarantining prior to donation varied significantly. At 27% of responding programs, no quarantine is requested, 39% require 7-14 days, while the remainder require a variety of shorter lengths. Recommendation for longer self-quarantine trended higher in high COVID-19 J o u r n a l P r e -p r o o f cumulative incidence states at 45%, compared to 32% in low cumulative incidence states. For patients who travel to the living donor recovery center, 28% of responding programs require no additional quarantine while 36% require 7-14 days. Notably, 8% of programs in high COVID-19 cumulative incidence states stated a preference for remote donation (i.e., organ travel, compared to patient travel for a distant donor), while no center in low and moderate cumulative incidence states expressed such preference. To further protect patients during hospitalization, 90% of responding programs have separate COVID-19 wards and 86% require personal protective equipment (PPE) for all staff.

With regards to variation in counseling, 44% of programs counsel donors that the risk of contracting COVID-19 is not impacted by donation, 31% counsel that the risk of complications is not impacted by donation, and 57% educate donors that COVID-19 has been associated with acute kidney injury (AKI).

These practices appear similar across state cumulative incidence levels.

Living donor follow-up Safe living donation requires programs to carefully follow donors. However, operationalizing this followup has changed in the pandemic ( Table 6) . Overall, 28% of responding programs have stopped followup completely during the pandemic, and this frequency was similar across state COVID-19 cumulative incidence levels. A majority (52%) reported continuing follow-up without change while 20% have continued follow-up without lab testing. Importantly, only 21% of programs that continued follow-up used in-person evaluation, while the majority of centers performing follow-up report using video-based telehealth (73%) and telephone-based telehealth (66%) strategies. Among programs continuing laboratory follow-up testing for donors during the study period, 80% used community labs and 19% used home-based phlebotomy. The most common barriers to living donor follow-up reported were hospital restrictions on elective visits (54%) and patients' unwillingness to come for lab tests (42%) and on-site visits (39%) (Figure 4) . Following the COVID-19 pandemic, 93% of responding programs plan to increase the use of telehealth for donor follow-up compared to pre-pandemic levels.

In this national survey of U.S. transplant programs on LDKT program practices during the COVID-19 pandemic, we found evidence of marked reductions in all phases of living donor care and surgery nationwide. In high cumulative incidence areas, LDKT activity was curtailed not only in response to concerns for donor safety but also as a result of administrative restrictions and resource availability for cases perceived to be elective. These findings resonate with data from the Organ Procurement and Transplantation Network (OPTN)/United Network for Organ Sharing (UNOS) data which documented a substantial decline in LDKT surgery during the initial pandemic, 5 but add knowledge in terms of underlying evaluation, testing and care processes. While LDKT rates are slowly recovering, the practice constraints described in this survey identify potential barriers that may recur in the context of local infection resurgences.

Living donor safety is the central priority for all healthcare professionals involved in LDKT. Although national guidance from CMS has been to continue organ transplantation as an essential procedure where local resources allow, living donation practice should be considered in light of both donor and recipient risks, and the potential to safely delay surgery. Initially, donation was reduced due to profound shortages in medically necessary supplies and high hospital occupancy in areas with significant COVID-19 disease cumulative incidence as well as patient safety concerns. As these limitations have eased, programs have begun to resume elective surgeries with appropriate safety steps. Our survey shows that 80% of programs planned to resume LDKT by early summer 2020. However, this resumption in activity has not replaced the lost transplants, as 27% fewer living donor transplants have been performed as of August 11 in 2020 compared to 2019. 5 This survey demonstrates a decline in living donor candidate evaluations due to donor/recipient safety concerns and fewer donor inquiries. Donors and recipients should be educated and reassured that their donor's safety is of paramount importance to every transplant program. Many programs have changed their practice significantly to protect the donor during all phases of donor care, including increased use of telehealth and obtaining labs locally before and after donation to minimize SARS-CoV-2 exposure.

These practices should help to alleviate the anxiety experienced potential donors.

Asymptomatic infected patients undergoing surgical procedures in a series from Wuhan China experienced significantly higher morbidity and mortality rates, 17 Transplantation Society recommends a two-week quarantine for donors. 11 The current survey shows wide variation in adoption of these recommendations, with most programs requiring no or a few days of quarantine prior to surgery. Programs generally did not require longer durations of quarantine for donors traveling a distance, who may be at higher risk of COVID due to travel related contact with several individuals. While the use of telehealth and local testing has minimized donor inconvenience, the need for up to 2 weeks of self-quarantine prior to surgery could add burden and potentially financial hardship for employed donors without work-from-home options. In response to feasibility concerns, in July 2020, the AST modified recommendations to suggest that while self-quarantine is recommended as a preventive strategy, it should not be mandatory. 9 In our practice, while we highly recommend that the living donor candidate, recipient, and their support system self-quarantine for 7-14 days prior to the scheduled surgery, we consider exposure risk at a case-by-case level and review the exposure prevention plan at multidisciplinary selection committee. We concur with the AST that living donors who travel by air to the transplant center for surgery should be strongly encouraged to self-quarantine for 14 days prior to donation. 9 In April 2020, the OPTN/UNOS suspended data collection & submission requirements for living donor follow-up (along with recipient follow-up and recipient malignancy forms), retroactive to 3/17/2020 and currently effective through 9/30/20. 18, 19 The purpose is to reduce patient exposure to COVID-19 driven by testing, as well as to reduce administrative burden on centers. We found that a third of the programs suspended living donor follow-up during the survey period. Those programs that continued follow-up have used telehealth or phone visits to minimize risk of COVID-19 exposure to the donor. The use of remote technologies should allow programs to continue vital post donation surveillance and maintain best practices regardless of temporary relaxation in OPTN/UNOS reporting requirements.

With regards to variation in counseling, less than half of programs counsel donors that the risk of contracting COVID-19 is not impacted by donation, less than a third counsel that the risk of complications from infection is not impacted by donation, while 57% educate donors about associations of COVID-19 and AKI. 20, 21 In our opinion, while status as a donor should not impact susceptibility to contracting COVID-19 in the community setting or confer an immunosuppressed state, reduced renal reserve due to surgical nephrectomy could increase susceptibility to severe AKI in the context of severe infection, due to lower baseline renal reserve. To date, there have been no reports in which a recent living donor has acquired COVID-19 and suffered AKI or required dialysis, although monitoring is warranted as donation and LKDT resume during the pandemic. Postdonation precautions to reduce risk of infection, such as social distancing and use of masks, and further consensus on data-driven education and counseling for living donors, are advisable until effective disease prevention strategies (e.g.

This survey suggested that the COVID-19 pandemic is likely to have long-lasting impacts on living kidney donation and LDKT practices. CMS and insurance companies were responsive in permitting use of telehealth in new donor evaluation and even those across state-lines, and transplant programs adapted quickly in incorporating telehealth in their practice. However, most programs remain unwilling to use telehealth for the surgical evaluation and require at least one in-person visit prior to donation. We concur that telehealth cannot replace an in-person physical examination by at least one provider; further, an in-person assessment may not only be a key component of surgical assessment but also of medical evaluation and psychosocial evaluation. In response to the success of telehealth platforms, most programs report a willingness to use this technology both prior to and following donation. 6 Although most programs reported continuing some form of post-donation follow-up, a minority deferred laboratory follow-up. Although early postdonation complications rates are very low in general, recent data demonstrate the prognostic importance of early post-donation renal function, 22 There is a need for research to define optimal living donation testing strategy and timing, to maintain donor and recipient safety, and inform counseling. As the pandemic evolves there is a need to define best practices for safe KPD, and optimal logistical procedures for donors who live far from the donor recovery center.

Our study has the limitations inherent to the survey study design, such as potential for recall bias. The findings represent practices as they are reported; we cannot verify how accurately the reports represent actual practice at each LDKT program. Respondents were identified by online outreach to U.S. transplant professionals, and not all programs are represented. However, the 61% response rate is higher than many contemporary studies of transplant program practices (where response rates in 30%-range are common), 14,26,27 likely reflecting the strong community interest in the topic, and the responding centers represent 75% of LDKT volume in the period. Per prior methods, [26] [27] [28] we applied an a priori methodology to select one representative survey per program favoring completeness and clinical role that was blind J o u r n a l P r e -p r o o f to the responses, but results may have varied somewhat with other methodologies. These survey data reflect the opinions and experiences of the respondents at the time of completion, and given the rapidly dynamic nature of the COVID-19 pandemic, may not be reflective of subsequent practice. However, these data provide the most comprehensive assessment of living donor practice in the United States currently available and offer a benchmark for comparing future practices as the pandemic and related guidance evolve over time. The number of transplant programs provides limited power for statistical comparison of differences across local COVID-19 cumulative incidence levels; nonetheless, we included the trends to address a question of interest frequently raised in the community.

In conclusion, the COVID-19 pandemic has had profound impacts on all aspects of transplantation, and this impact is particularly notable for living kidney donation and LKDT. Living donation practice carries additional responsibilities for transplant programs given potential risks to healthy donors undergoing a surgical procedure for the benefit of another person, and the risks of disease transmission to an immunosuppressed recipient. However, pausing LDKT may have a lasting impact on the organ supply and transplant candidate outcomes. While the pandemic continues, outcomes of donors and recipients alike must be closely monitored, especially in areas experiencing local disease resurgences. Additional study and consensus building are needed to determine whether individuals who have recovered from COVID-19 may safely donate, to define guidance for safe KPD, and to inform optimal logistical procedures for donors who live distant from the donor recovery center. Careful development of guidance and protocols to minimize risk, balanced for feasibility and practicality for donors, is vital to enabling programs to reopen safely and to continue LDKT while COVID-19 persists in our communities.

As donor centers embrace the challenge of allowing LDKT to recover, efforts to develop, update and follow best practices must be sustained throughout the pandemic to ensure that living donation and LDKT remain as safe as possible, and serve and support the best outcomes of donors and their recipients. Table S1 . Survey instrument (PDF) Figure S1 . Flowchart of representative survey response selection (PDF) Supplementary information is available at KI Report's website. (3) 10% (4) 12% (5) If a donor has to travel to your center for surgery (i.e., residence is not local), how long will you require them to quarantine prior to surgery (in addition to negative COVID-19 testing)? (N=113) % (n) % (n) % (n) % (n) 

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The authors thank survey respondents, including members of the American Society of Transplantation 

The authors of this manuscript have no conflicts of interest to disclose.

Data availability is limited to aggregate summaries as reported, based on IRB requirements.

Patient concern / reluctance to proceed Program concern for recipient safety Program concern for donor safety