key: cord-324918-36om8n2d
authors: Guha, Chandana; Tong, Allison; Baumgart, Amanda; Scholes‐Robertson, Nicole; Isbel, Nicole; Kanellis, John; Campbell, Scott; Coates, Toby; Chadban, Steven
title: Suspension and resumption of kidney transplant programs during the COVID‐19 pandemic: perspectives from patients, caregivers and potential living donors‐a qualitative study
date: 2020-07-08
journal: Transpl Int
DOI: 10.1111/tri.13697
sha: 
doc_id: 324918
cord_uid: 36om8n2d

BACKGROUND: Many countries have suspended kidney transplantation programs during the COVID‐19 pandemic because of concerns for patient safety and the shortage of healthcare resources. This study aimed to describe patient, family member and potential donor perspectives on the suspension and resumption of kidney transplant programs due to COVID‐19. METHODS: We conducted seven online focus groups involving 31 adult kidney transplant candidates (n=22), caregivers (n=4) and potential donors (n=5). Transcripts were analyzed thematically. RESULTS: We identified five themes: cascading disappointments and devastation (with subthemes of shattering hope, succumbing to defeat, regret and guilt); helplessness and vulnerability (fear of declining health, confronted by the threat of and change in dialysis, disconnected from healthcare, susceptibility to infective complications); stress from uncertainty (confusion from conflicting information, unable to forward plan), exacerbating burdens (incurring extra financial costs, intensifying caregiver responsibilities), and sustaining health through the delay (protecting eligibility, relying on social support, adapting to emerging modalities of care). CONCLUSIONS: During the suspension of kidney transplantation programs, patients felt medically vulnerable because of declining health, susceptibility to infection and reduced access to care. There is a need to address health vulnerabilities, disappointment, uncertainty and additional burdens arising from the suspension of kidney transplantation programs.

The COVID-19 pandemic has impacted on kidney transplant programs globally [1] [2] [3] [4] . Many countries have restricted or suspended kidney transplantation programs due to concerns for patient safety and the shortage of healthcare resources during the pandemic [2, [4] [5] [6] [7] [8] [9] . There are some data to suggest that kidney transplant recipients are at an increased risk of severe COVID-19 because of immunosuppression and comorbid conditions [7, [10] [11] [12] [13] .

Decisions to limit or suspend transplantation activity in the context of this pandemic is fraught with medical, logistical and ethical challenges [1, 7, 9] . Delays in transplantation can be detrimental for patients receiving dialysis because of deterioration in health. Additional screening, need for isolation, and protection for the transplant team (e.g. those travelling to high risk areas for donor procurement) also need to considered [5] . Challenges identified in a recent global transplantation report include hospital facilities and workforce being diverted from transplantation to manage COVID-19, uncertainties of the risks of transmission from COVID-19 positive donors, and lack of agreement about immunosuppression strategies in the context of the pandemic [7] .

Prioritization of resources is difficult as the balance between equity and utility shifts with the increased risks imposed by COVID-19 [1, 5] .

However, the impact of the suspension of transplant programs on patients, caregivers, and potential donors may be underrecognized. This study aims to describe the perspectives of kidney transplant candidates, caregivers and potential donors on the suspension and resumption of kidney transplant programs.

This article is protected by copyright. All rights reserved Kidney transplantation was classified as an elective surgery and was suspended (31 st March 2020 to 27 th April 2020) by hospital jurisdictions in a coordinated response, in consultation with State Governments and the Chief Medical Officer, following receipt of advice to do so from a peak body of transplantation and donation experts convened by the Federal Government and the Transplant Society of Australia and New Zealand as the "National Transplantation and Donation Rapid Response Taskforce -COVID 19". Kidney transplantation was suspended during the initial log-phase of incident cases of COVID-19 in Australia, at which time Australia predicted a far higher number of cases and greater burden of COVID-19 than has been experienced to date.

Regarding the recommencement of transplant programs, the Communique released by the COVID-19 National Transplantation and Donation Rapid Taskforce (13 May 2020) stated that "Deceased donor transplantation has resumed cautiously and any changes in community infection rates and transmission will be followed closely before a decision is made to resume full transplant activity. Processes need to be in place to ensure that patients can be safely managed through the operative and post-operative periods with as little time spent in hospitals and waiting rooms as possible, acknowledging that the safest place for immunosuppressed people being at home with no visitors. Units need to be as well prepared as possible for potential further outbreaks and clusters of infection." [14] According to the Australian and New Zealand Dialysis and Transplant Registry (ANZDATA), for patients receiving dialysis and waitlisted for kidney transplant, survival from time of waitlisting (censored at transplantation) is 99% and 94% at one and three years, respectively [15] . The mortality rate is 1.9 deaths per 100 patient-years (95% CI: 1.5 -2.5) [15] . The average waiting time for a kidney transplantation is 2 to 3 years, but can be up to 7 years." [1] . As of 17 th June 2020, there were eight cases of COVID-19 in transplant recipients, and 4 cases in patients receiving dialysis in Australia [16] .

We used the Consolidated Criteria for Reporting Qualitative Studies (COREQ) to report this study [17] .

This article is protected by copyright. All rights reserved Kidney transplant candidates age 18 years and over, their family members, and potential donors who had commenced workup were eligible to participate. All participants had to be Englishspeaking and able to give informed and voluntary consent. We took an inclusive approach and invited participants through Transplantation Society of Australia and New Zealand (TSANZ) Patient Network (this was open to all with registration available on the TSANZ website), social media and news media. This also enabled the inclusion of a wide diversity of demographic and clinical characteristics. Ethics approval was provided by The University of Sydney (2020-217).

Due to the multi-pronged method of recruitment, we could not apply a purposive sampling strategy.

The one-hour focus groups were convened from April to May 2020 using ZOOM videoconferencing. To maximize attendance rates (participants could select their preferred session) and to support diverse discussion, focus groups were mixed and included transplant candidates, family members and potential donors. The question guide was developed from the literature and discussion with the investigator team. We asked questions about: the impact of the suspension programs (including on health, treatment, emotional and mental wellbeing, family, finances, and access to care, self-management), access to care, resumption of transplant activity (knowledge, expectations, decision-making, information and communication) (Supplementary File). An investigator (CG, AB, NSW, AT) facilitated each group, and a co-facilitator took field notes. We convened groups until we reached data saturation, when little or no new concepts were arising. All groups were recorded and transcribed.

All transcripts were imported into HyperRESEARCH software (version 3.7.5 ResearchWare Inc) to facilitate data analysis. Using thematic analysis, author CG inductively identified initial concepts related to the participant perspectives on the suspension and resumption of kidney transplantation programs. Similar concepts were grouped into preliminary themes and subthemes, which were discussed with the facilitator team, and sent to participants for comment. This ensures Accepted Article that the final analysis reflects the full range and depth of the data obtained. A thematic schema was developed to summarize and depict conceptual links among the themes.

In total, 22 kidney transplant candidates, four caregivers, and five potential donors participated across seven focus groups (N=31). Of the 49 participants confirmed to attend, 31 (63%) participated in the focus groups. Participant characteristics are shown in Table 1 . Of the 22 patients, three had chronic kidney disease not yet requiring kidney replacement therapy, 12 were receiving hemodialysis, and seven were receiving peritoneal dialysis; 17 were female. Fourteen participants had their transplant cancelled during the time of the suspension.

We identified five themes, which are described in the following section. Concepts specific to those on the waiting list or with a living donor are detailed accordingly. Selected quotations to support each theme are provided in Table 2 . The thematic schema is provided in Figure 1 .

Shattering hope: Patients were "traumatized" when the program was stalled because a transplant was their hope. The suspension was "one more event" on top of every other disappointment (including previous cancellation of transplant). Those who had their transplant cancelled felt like the "rug was pulled out from under them." Some were frustrated as they feared having to start the workup over again. Regret and guilt: Some potential donors had an initial transplant date prior to the suspension and felt guilty and that they had let the patient down when the rescheduled surgery had to be cancelled.

One patient who "estimated" that he had about "20 years" of life left said "I just could see my

This article is protected by copyright. All rights reserved prime whittling away" due to the suspension. He felt he "owed to himself and his wife [a potential donor]" to be well and now "there's the sort of sense of disappointment this possibly may not come about."

Fear of declining health: Some patients were concerned about their health deteriorating in terms of disease progression or because of dialysis. The stress related to COVID-19 was thought to "accelerate the loss of their kidney function". Some questioned, "will I even make it to survive to get to this transplant. Because it keeps being pushed later and later."

Confronted by the threat and change in dialysis: Some patients who were preparing for preemptive transplantation now faced the dreaded possibility of needing dialysis because of the delay.

They encountered additional barriers in accessing the preferred mode of dialysis, for example having to do in-center hemodialysis rather than home hemodialysis because of the costs -"because I'm down on the transplant list, the costs for setting up a home dialysis for short-term, they didn't want to do, so they just told me to stick with hospital dialysis."

Disconnected from healthcare: Patients appreciated being contacted about the suspension personally by phone or email, rather than a generic mailed letter, which was regarded as perfunctory. Some felt neglected when appointments with their nephrologists were cancelled.

Others were still waiting for a follow up call after the initial news of cancellation. Some did receive general information from their specialist but also sought information from other sources including news media -"I didn't hear very much about it. My specialist did ring me to let me know that they were going to start redoing it. I think I got most of my information from the news." Susceptibility to infective complications: Some patients understood the decision to suspend transplantation was for their own safety -"I understand the reasons why the transplant program was suspended for these patients going on immunosuppressants. It's just not worth the risk. But it doesn't take the trauma away from being on hold". They also considered the increased risk of infection in hospital settings -"I was disappointed that elective surgeries were cancelled, [I saw] on our Facebook groups, before I got official letter. It's to stay on the safe side I guess, the risk of Accepted Article infection in hospital maybe outweighs it, or leaving the team to be available to the COVID patients." Another patient expressed, "I was very scared to catch it (COVID) so I was happy that it was postponed." Some patients felt conflicted about whether to proceed with transplant once programmes resumed because of the potential risks of severe COVID-19 infection after surgery while on immunosuppressants. Potential donors worried about being carriers of the virus.

Participants questioned if deceased and living donors would be screened for COVID-19. However, others wanted to proceed with transplantation immediately because they trusted the decision of their medical team and their efforts to minimize such risks. Unable to forward plan: Being on standby was difficult for donors who wanted to "donate, and get on with their lives," and some worried about being able to remain healthy enough to donate.

Without "having a clear direction of a time frame" patients were unable to plan for the transplant -"we've [patient and donor] got to organize people to look after the house, sit in the house and live there for a month…..the lots of unknowns puts a lot of pressure on you". One patient reported they were contacted by their transplant unit who could not give them a timeframe for the suspension -

This article is protected by copyright. All rights reserved "He rang and said that due to the number of ICU beds, they couldn't continue with doing the transplants. It was on hold indefinitely."

Incurring extra financial costs: One patient who had hoped to return to work after transplant was concerned about the delay because they were unemployed and had no income. For some patients, the transplant workup had cost "an absolute fortune" and some worried about costs of repeating the screening tests after transplant programs resumed. One patient who had their transplant cancelled had purchased AU$400 (US$250) worth of immunosuppressants that could not be returned.

Intensifying caregiver responsibilities: With the postponement of transplants, caregivers had to keep up their duties in supporting the patient receiving dialysis. Some changed the way they lived to protect patients during the suspension. A family member who was a healthcare worker had to "leave home" and make separate arrangements to socially distance themselves from the patient during the suspension period.

Protecting eligibility: Potential donors felt added pressure to keep fit during the suspension because they "didn't want to be the reason" for jeopardizing the patient's chance for the transplant.

Those enrolled in paired kidney exchange programs felt they were in a precarious predicament because everyone in program had to remain healthy -"it just takes one person in the program to get sick or if something happens we would be all out of whack".

Relying on social support: Patients relied on family support to cope with the increased waiting period due to transplant suspension -"family support … everyone just ganging together and pushing and encouraging and each day is just a massive battle".

This article is protected by copyright. All rights reserved Adapting to emerging modalities of care: During the suspension, some patients had to use telehealth. They took more responsibility for self-monitoring and checked their blood pressure and blood glucose levels at home. They felt that telehealth used during the suspension period would help them self-monitor and minimize visits to the hospital if they received a transplant during the COVID-19 period.

The suspension of kidney transplantation programs due to COVID-19 was devastating for patients who felt medically vulnerable because of declining health, and susceptibility to infection and having to miss in-person appointments and monitoring. The uncertainty in the duration of the delay and conflicting information exacerbated stress in patients, family members and donors. They were conscious and vigilant about protecting their eligibility for transplant/donation. Some patients experienced added financial burden in paying for immunosuppression that could not be refunded, having to take leave on their employer's advice, and needing to pay for extra tests. The responsibilities on caregivers were also intensified. Decisions to proceed with transplantation after the resumption of programs were difficult for some because of concerns about increased risks of severe COVID-19, while others believed it was safe to undergo transplant immediately.

There were some differences between candidates on the transplant waiting list and those with a living donor. Patients with a living donor felt a responsibility to remain as health as possible to protect their eligibility for living donor kidney transplant, including in the context of paired kidney exchange. Those who were preparing for pre-emptive transplant feared the possibility of having to commence dialysis due to the delay. Some felt unable to forward plan with their donor because of the uncertainty of timing as to when transplant would recommence.

The COVID-19 pandemic has had detrimental impacts on physical, mental and social health in the general population, with fears of infection, frustration, boredom, inadequate information, financial loss and stigma identified as stressors [18] . While these were also identified in our study, additional unique medical and psychosocial challenges faced by patients, caregivers and potential donors were identified that were directly attributed to the suspension of transplant programs. COVID-19

infection was feared to jeopardize opportunities for transplantation or transplant outcomes. Whilst

published data is emerging [10] [11] [12] , limited and conflicting information available to patients exacerbated stress amidst the disappointment and uncertainty about remaining eligible, or even alive, for transplantation following resumption.

We generated novel and detailed evidence on patient, family and potential donor perspectives on the suspension and resumption of kidney transplant programs during COVID-19. To our knowledge, their priorities and concerns regarding the impacts of the suspension have not been systematically assessed and documented and may also not always expressed to clinicians involved in their care. We achieved data saturation and the findings were send back to participants to ensure that the analysis reflected the full range and depth of data. However, there are some potential limitations. The study did not include participants who were non-English speaking and would preclude those without access to the internet. Given our multipronged method of recruitment, we were unable to use a purposive sampling. However, there was reasonable diversity in the demographic and clinical characteristics among the participants.

We suggest changes to transplant programs, in particular any cessation of transplant activity, warrant a well-coordinated and consistent approach in communicating this to patients and potential living kidney donors, including the rationale for suspension. This includes the potential risks to kidney transplant recipient and healthcare system, and resource implications. We suggest that centers could provide periodic updates about the pandemic, as available, that includes information about potential plans to restart kidney transplantation programs. Where feasible, transplant coordinators and other staff could personally inform transplant candidates about the suspension and resumption of transplant programs." The potential psychological sequalae indicates that access to counselling to manage disappointment, stress and anxiety is needed. We also recommend programs that support patients in self-monitoring and managing their health to remain fit for transplantation or donation. In considering the resumption of transplant programs, informed-decision making with patients and their caregivers should include discussion of the potential risks of remaining on dialysis or delaying transplantations versus risks of COVID-19 infection in immunosuppressed recipients. We suggest that further efforts are needed to assess for any changes in how patients are educated and counselled.

This article is protected by copyright. All rights reserved Addressing health and emotional vulnerabilities, disappointment, uncertainty and additional burdens arising may help to mitigate the some of the direct consequences of suspending transplant programs on the lives of patients, caregivers, and potential donors.`À ccepted Article 

Total may not sum to 31 as multiple responses were possible; were not reported, or were not applicable. For patient characteristics, donor and caregivers could provide a response regard the characteristics of the patient *Other, Middle Eastern, Indian, Chinese; ** Other included Alport Syndrome n=2, FSGS n=1, Reflux nephropathy n=1, immune-related m=1, genetic n= 2, scleroderma n=1 (3%), lupus n=1; ***Other, brother/sister in law, paired kidney program 

This article is protected by copyright. All rights reserved "Also, mention of the risks of why the suspension has occurred and that's one of the points because I think more information of why it has happened will make people go "Oh, they're looking after my health before doing the transplant." (P, 

This article is protected by copyright. All rights reserved 

This article is protected by copyright. All rights reserved 

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Accepted Article This article is protected by copyright. All rights reserved 12

A single center observational study of the clinical characteristics and short-term outcome of 20 kidney transplant patients admitted for SARS-CoV2 pneumonia

Australian Government Department of Health. Australian Health Protection Principal Committee (AHPPC) coronavirus (COVID-19) statements on 24

COVID-19 -National Transplantation and Donation Rapid Response Taskforce Weekly Communique No.12 -17

Consolidated criteria for reporting qualitative research (COREQ): a 32-item checklist for interviews and focus groups

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Accepted Article

We thank all the patients, caregivers and potential donors who gave their time to participate in the study.

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