Impact Of The COVID-19 Pandemic On The Kidney Community: Lessons Learned And Future Directions Ⅱ

Lessons for policymakers 

Policymakers have important lessons to learn from the COVID-19 pandemic that are specific to the dialysis population28. Below, we outline key lessons learned from the USA. 

First, policymakers should strongly consider extending waivers to exempt providers from pre-existing value-based purchasing programs, including the  Quality Incentive Program52 and the End-stage Renal Disease Treatment Choices model53. These programs have laudable goals but might pose a distraction for dialysis facilities that need to remain nimble during a public health emergency. To its credit, the Centers for Medicare and Medicaid Services rapidly implemented waivers early in the pandemic, allowing facilities to focus on the emergency54.

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Second, the risk that in-center dialysis poses for patients, particularly with airborne diseases, must be addressed. Early in the pandemic, providers rightly recognized that facilities could quickly become hubs for widespread infection55. One welcome addition was the broad expansion of telehealth benefits56. However, the beginning of the COVID-19 pandemic was also fraught because of strapped supply chains that exacerbated the already limited supply of PPE. The American Society of Nephrology (ASN), the European Renal Association and the International Society of Nephrology issued calls for governments around the world to prioritize PPE for dialysis personnel and increase access to lifesaving dialysis. To prepare for the next pandemic, not only should policymakers stockpile more emergency medical equipment but they should also place a strong emphasis on distributing these supplies to providers of populations with complex medical issues, including dialysis facilities. A major concern is ongoing shortages in dialysis supplies, including dialysate.

Third, we must customize policies to address the specific needs of the dialysis population. For instance, per Centers for Medicare and Medicaid Services guidance, many hospitals deferred “non-essential” surgical procedures. However, these deferrals may have inadvertently harmed incident ESKD patients who needed dialysis access procedures27.

New therapeutics that can treat COVID-19 have shown incredible promise in reducing hospitalizations and mortality57,58. Dialysis facilities are unique in the healthcare industry because patients must return to the facility regularly. In the future, dialysis facilities should be considered a major site for the distribution of new therapeutics and vaccines.

Kidney transplant recipients 

The pandemic has created significant challenges for kidney transplantation. Transplant candidates and recipients, especially in the early post-transplant period, experienced significant excess mortality related to COVID-19, with a disproportionate impact on racial minorities and socio-economically disadvantaged individuals59,60. Both the innate and adaptive immune systems seemed profoundly altered in transplant patients, with significantly lower levels of anti-spike antibodies up to 2 months following the onset of COVID-19 symptoms compared with patients on dialysis61. As such, prime concerns have been centered around continuing kidney transplant surgeries while minimizing the risk of infection and management of post-transplant immunosuppression.

Globally, living and deceased donor transplantation has been adversely impacted to various extents and at different periods of time. This is due, in large part, to efforts to conserve resources during a COVID-19 surge and concern for the risk of newly immunocompromised individuals given their increased risk and poor outcomes, particularly during periods of high community transmission3. The mortality rate was 20–30% in kidney transplant recipients during the first wave of the pandemic, with a reduction in mortality during the second wave 47. Although there was a 16% global decrease in transplant activity, most notably during the first 3 months of the pandemic, there were substantial differences in transplant activity between countries62. Although living donation came to a nearly complete stop early on during the pandemic, it has resumed since then but does not appear to have reached pre-pandemic levels63. Notably, previously decreased donor transplantation rates have continued to increase in the US allocation system, despite a dramatic increase in organ discards, reflecting increased selectivity of organs and patients64. There are notable differences in mortality rates of waitlisted individuals compared with transplant recipients, with the USA reporting higher mortality in waitlisted individuals, and Europe and the UK reporting higher mortality in transplant recipients. The decision to continue transplants during a pandemic needs to be individualized for each country and should take into consideration the mortality risk of waitlisted individuals as well as transplant recipients and infection risk in the immediate post-transplant period. In addition, the pandemic has also impacted transplant activity owing to concerns regarding donor-derived viral transmission. A systematic review of 69 transplants from 57 donors infected with SARS-CoV-2 demonstrated that non-lung transplantation was safe, with a low risk of transmission65.

Efforts to lower the risk of transmission along with overwhelmed healthcare systems created significant challenges in the care of patients. Healthcare systems pivoted quickly towards telehealth strategies and there was increased interest in the use of non-invasive biomarkers when kidney biopsies became a challenge66–68. Although the value of monitoring strategies for allograft health remains uncertain, there does not appear to have been a dramatic uptick in acute rejection episodes69

The mainstay of treatment for COVID-19 in transplant recipients included reduction or cessation of antimetabolite therapy for 2 weeks or longer, in addition to standard adjuvant therapies used in the general population70. Although this approach also contributed to early concerns about adverse allograft consequences, recent data suggest that brief cessation of therapy was not associated with the development of donor-specific antibodies71. Additional concerns in the SARS-CoV-2-infected recipient include the abrupt increase in tacrolimus levels that has been observed at the time of presentation 72. Immunosuppressed individuals also appear to have a prolonged high viral burden with persistent positive PCR results, which may have implications for when to allow patients with previous COVID-19 infection back into the transplant clinic setting.

Although immunosuppressed patients and those with kidney disease were excluded from the initial vaccine trials, significant real-world experience has been gained in these groups. Studies of immunogenicity after vaccination revealed poor humoral responses to  two doses of both mRNA and viral vector vaccines73,74. Older age, impaired allograft function, and use of triple maintenance immunosuppression, belatacept, steroids and anti-metabolites were associated with poor humoral response. Additionally, breakthrough infections were frequently observed in kidney transplant recipients, even before the omicron surge. An enhanced humoral response was observed after a third and fourth vaccine dose, use of heterologous vaccination, and modulation of immunosuppression75–77

Kids, kidneys and COVID-19 Outcomes in children. 

Children and adolescents are a vulnerable group and are subject to special considerations in health care, research and public policy. Although the clinical impact of COVID-19 on pediatric patients has been less profound than in adults so far, successive waves of the pandemic have led to more children being directly impacted. At the start of the pandemic in the USA, there was an initial decrease in deceased and living donor kidney transplantation; however, rates of transplantation had returned to pre-pandemic levels by May 2020 (ref.78). Unlike in adults, children taking immunosuppression for kidney disease or kidney transplant and children on dialysis have not had worse outcomes from COVID-19 infection than the general pediatric population79–82. When sick enough to be admitted, however, 12–23% of hospitalized children with COVID-19 developed AKI83–85 and AKI is more common in patients with the multisystem inflammatory syndrome in children83. Consistent with other studies of AKI in children, AKI was associated with increased levels of care, length of hospital stay and worse outcomes83,85–87.

Gaps in science and child health policy. 

Compared with adults, many gaps in science remain for the pediatric population. Long-term COVID-19 outcomes are an important area of future study, and emphasis should be placed on developing safe and effective strategies to incorporate children into such studies. Research studying long COVID is lacking in children, despite evidence that it is at least as common for children as for adults88. Furthermore, although vaccination rates are much lower for children than for adults, we need to learn more about vaccination patterns and perceptions among children with kidney disease and their caregivers89. It will take years to understand the impact of educational disruptions that affected children with CKD, who already have lower cognition than the general population90. Moreover, pediatric research addressing the impact of pandemic disruptions on access to transplants, the early detection of kidney disease and the impact on family dynamics could aid in the development of more equitable and durable pediatric care delivery models and public policy. Table 1 outlines the challenges and missed opportunities faced by the kidney community in managing patients during the pandemic.

Psychosocial aspects of COVID-19 

The COVID-19 pandemic has necessitated a change in almost every aspect of kidney care. Healthcare resources shifted to prevent, detect and manage waves of COVID-19, leading to dramatic alterations in routine kidney care in many countries. This section highlights some of the changes instituted, and their impact on patients, caregivers and healthcare providers.

As the potential severity of COVID-19 disease became clear, international efforts were made to identify people at risk. Many nations endorsed targeted public health measures to minimize both mortality and economic impact91,92. For example, in the UK, a targeted national policy of ‘shielding’ was implemented. Those considered most at-risk from COVID-19 were centrally identified using electronic records, and government letters were issued advising individuals to socially isolate themselves, restricting contact even within their household group, with the help of financial and logistical support. Many people with advanced kidney disease, kidney transplantation, and/or those requiring immunosuppressive treatment, were advised to shield93,94. Although these measures were broadly supported, the personal impact varied, with some feeling protected while others felt fearful and isolated94. In countries without such protective policies, public health messaging likely encouraged similar exposure-avoidant behaviors, particularly in at-risk groups95–97.

Additional strategies to minimize infection were implemented internationally, including reduced visitor access in hospitals98,99 and dialysis units100. End-of-life care provision was dramatically altered because of the restrictions, with limitations of social contact and rituals before and after death101. Even with technological innovations to provide human connection, the impact of reduced physical contact between patients, caregivers and clinicians was significant. Some patients experienced loneliness and depressive symptoms, and caregivers described heightened anxiety and an increased desire for information from health care professionals102. Many patient and provider groups described ethical compromise and psychological distress, as they felt unable to provide or receive care at pre-pandemic levels103,104. Furthermore, patient and provider groups have described adversity, fear, abandonment, hope and resilience105–108. A multinational mixed methods study of 251 kidney healthcare providers found that nearly one-third of respondents were at a high risk of burnout and mental health distress during the pandemic, with feelings of emotional exhaustion, depersonalization and a reduced sense of personal accomplishment109.

Moral distress in health care during the COVID-19 pandemic has been extensively described and may explain some of the negative psychological consequences described above104. Moral distress can occur when an individual perceives that they are unable to act according to their ethical values owing to external barriers110. If individuals perceive that their ethical duties are compromised in settings of severe resource constraints — where institutional, health policy or financial barriers limit access to optimal treatments that are clinically indicated — moral distress can occur111,112. Notably, it occurs in both patients and caregivers and has been described in relation to the intentional separation between loved ones during end-of-life care and hospital visitation restrictions103,108. The consequences of moral distress include experiences of anger, guilt, depersonalization and, for healthcare professionals, a desire to leave the workforce entirely113. If persistent, moral distress can result in moral injury, resulting in long-term social and psychological trauma114,115.

Table 1 | Challenges in managing patients with kidney disease during the COVID-19 pandemic

Children and young adults with kidney disease face unique and pervasive mental and behavioral health challenges, with higher rates of depression, anxiety and neurocognitive disorders than their peers90. One survey reported that children felt that they were missing out on work-related and educational opportunities, missing family and friends, and compared with their peers, they lived with more COVID-related restrictions90. Health-related quality of life and physical activity decreased significantly for both children and adolescents during the pandemic owing to school closures, social distancing, and home confinement116. Although these strategies were employed to reduce virus transmission, their prolonged use requires assessment to mitigate the adverse psychological effects, especially in populations at a high risk of COVID-19. Furthermore, parents and caregivers of children with kidney disease experience significant psychosocial stressors that leave many families dysfunctional and disempowered. During the pandemic, this often-unseen care burden has been experienced disproportionately by families struggling with adverse social determinants of health and health disparities. Caregivers of children with kidney disease reported feelings of stress, anxiety, depression and insomnia during the pandemic, mirroring findings in parents of children with other chronic conditions117,118. Children with medical complexities have lost access to therapies, educational services and peer interactions, all while parents and caregivers have taken on additional responsibilities to navigate changes in employment and keep their families healthy119.

A global health perspective 

With its rapid spread across the globe, the COVID-19 pandemic revealed that most health systems were unprepared for, or at least underestimated, the challenge it would pose. Initially, the lack of readiness, combined with an almost lack of belief that such a pandemic could occur in the current day and age, resulted in acute shortages of many items needed for an effective response. A pertinent example is the scarcity of PPE early on in the pandemic, which sometimes resulted in hoarding by countries and by individuals. This “catastrophic breakdown in global cooperation”120 highlighted the need to develop global strategies to improve equity and access equipment, treatment and vaccines to treat COVID-19 (refs.120,121). Unfortunately, a lack of equity and empathy persists, with booster doses of vaccines being administered to most adults and children in some countries before adults at risk of poor outcomes even receive their first vaccine in others122. Hoarding, pricing, protection of intellectual property and dissemination of misinformation regarding vaccines have exacerbated inequities and contributed to deaths123. These persistent and pervasive inequities, which impact how individuals and nations have been (un)able to tackle the challenges posed by the pandemic have coined the term “political determinants of health”124.

Political and social determinants of health exist within as well as between countries, and the same populations who have experienced centuries of structural violence (such as African Americans and Indigenous populations) are those at the highest risk of serious illness from COVID-19 and most at risk of poor outcomes125–131. People living with chronic diseases, and especially kidney disease, are at the highest risk132. These facts have finally raised global awareness that we cannot continue to overlook non-communicable diseases, including when looking beyond the pandemic133,134. As the demand for hospital beds and health care services outstripped availability at various stages, triage guidance had to be urgently drawn up to allocate scarce intensive care unit beds, raising debates around which criteria would be morally acceptable135,136. Rationing of health care services became a reality, faced by many for whom the concept had been merely theoretical before then137–140.

The nephrology community was rapidly drawn into the eye of the storm. The capacity to provide dialysis became strained in some settings, leading to complex triage algorithms and in some cases deaths, even in high-income countries (HICs) because of a lack of access to dialysis140,141. People living with kidney disease are an at-risk population, tend to have lower socio-economic status, belong to minority populations and live with multiple co-morbidities142.

The pandemic has had a significant global impact on healthcare delivery in general, with consequences being particularly evident in low- and lower-middle-income countries (LLMICs)43. Notably, there were gross inequities in the provision of dialysis services143. Many guidelines were developed and disseminated for the management of patients with kidney disease, including those on dialysis, but most of these guidelines could not be adhered to because of the lack of resources in most LLMICs144. Surveys conducted by the International Society of Nephrology in partnership with the Dialysis Outcomes and Practice Patterns group were aimed at understanding how clinical practice was being impacted by the pandemic, and if and how people living with kidney disease were being prioritized across the globe43,145. Challenges affecting both staff and patients were common in LLMICs. The patient-level impact reported by survey respondents included challenges in access to diagnostic testing, interruptions in hemodialysis delivery, restricted access to intensive care, mechanical ventilation and in-hospital hemodialysis, affecting patients in LLMICs more frequently than those in upper-middle-income countries and HICs. Staff in dialysis units in LLMICs had less access to COVID-19 testing, PPE (Fig. 1) and training in infection control, and suffered a greater psychological impact43.

At the time of the survey, conducted during the first year of the pandemic, diagnostic tests for SARS-CoV-2 were unavailable or of limited availability, with longer turnaround times for test results in the majority of LLMICs43. Patients in LICs frequently had to pay out-of-pocket for diagnostic (PCR) testing. Owing to multiple factors including lockdowns, curfews and delays awaiting COVID-19 test results, patients in LLMICs missed dialysis with a greater frequency than pre-pandemic and these delays cost lives145.

Fig. 1 | Shortage of personal protective equipment across countries by income status. Data on country income derived from World Bank data. The graphs show the results of a global online survey of hemodialysis units, which was aimed at determining patterns and access to resources associated with hemodialysis care during the COVID-19 pandemic. As shown, LICs had the greatest shortage of personal protective equipment (PPE) at the peak of the pandemic (a) and the greatest use of PPE beyond the manufacturer’s shelf life (b), the latter representing a need to continue using out-of-date PPE owing to a shortage of supply. HIC, high-income countries; LIC, low-income countries; LMIC, lower-middle-income countries; UMIC, upper-middle-income countries.

A subsequent survey focused on access to vaccination for people living with advanced kidney disease. At least one COVID-19 vaccine was available in 97% of respondent countries. Over 90% of the respondent countries reported prioritization of health care workers within the first two phases of vaccine rollout, whereas patients living with stage 4/5 CKD, dialysis, or kidney transplants were prioritized within the first two phases in 51%, 71%, and 62% of countries respectively. Overall, at least 50% of patients receiving in-center hemodialysis, peritoneal dialysis or living with a kidney transplant were reported to have completed vaccination in around half of respondent countries, with the lowest rates reported in Africa and the highest rates in Western Europe. Vaccine hesitancy, vaccine shortages, and difficulties in mass distribution of vaccines were common and reported more frequently in LLMICs than in HICs. Although the vaccination rate in the dialysis population may appear relatively high in lower-income settings, indicating that the vulnerability of this group has been acknowledged globally, the global disparities echo the call by the World Health Organization for more equitable access to vaccines, having set a global target of 40% of the population of every country to have completed vaccination by the end of 2021 and 70% by mid-2022. Two major global efforts, COVAX and ACT-Accelerator, where richer countries should contribute to supplying and distributing vaccines to poorer countries, have been launched to facilitate global vaccination120,121,146. These schemes, however, have not yet translated into action in terms of global solidarity, although equity gaps may be beginning to narrow147,148

Children are an inherently vulnerable population that modern society has a duty to protect. However, the unique social status of children places them at an equally unique risk of health inequities. Current research and pharmaceutical development processes are designed to protect children by studying drugs and diseases in adults first; however, the lack of interventions and immunizations that are available in a timely manner for children, including those with underlying chronic diseases during the pandemic, has raised concern for age-based health inequity that should be re-evaluated. Protection of children is paramount; however, equipoise with the timely availability of emerging therapies and robust safety information are critical to this endeavor for the ethical management of COVID-19 vaccines. At a national level, the prevalence of childhood poverty, specifically its relationship to health and its disproportionality across sociodemographic groups most at risk during the pandemic, highlights another important pediatric kidney health risk119. Evidence of social deprivation along racial, ethnic, and class divisions has been shown to have adverse consequences in both children and adults with kidney disease, but the specific effect of the pandemic on this population is yet to be studied149,150. The almost miraculous rapidity with which the scientific community tackled the COVID-19 pandemic has been a simultaneous triumph and a failure. The rapid development of tests, vaccines, and therapeutics has been life-saving for many but has left many behind. The early, robust efforts to identify and publish potential management strategies led to great advances in clinical understanding and rapid knowledge sharing but also led to the dissemination of pseudoscience and misinformation. This has severely impacted trust in health systems globally and has led to the loss of life. The COVID-19 pandemic has revealed how necessary solidarity is at all levels, beginning with global governance and trickling down to the individual in the dialysis chair in a remote dialysis unit123,151,152 (Fig. 2). This requires attention be paid to justice and ethics at all levels. Global collaboration and cooperation are needed between countries, institutions, industry, and academia. Collaborative focus on “building back better” is required such that health systems and societies emerge from the pandemic stronger, more resilient, and fairer.

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