The impact of COVID-19 on kidney transplant activities in Brazil: a descriptive study

ABSTRACT BACKGROUND: The coronavirus 19 (COVID-19) pandemic has reached services, systems, and world society. Despite its certified efficiency, the Brazilian National Transplant System is not exempt from the side effects of COVID-19. OBJECTIVE: To compare kidney transplantation activity registered in Brazil between the pandemic (2020) and pre-pandemic (2019) periods. DESIGN AND SETTING: A descriptive study was conducted in March 2021. The annual reports of the Brazilian Transplantation Registry for 2019 and 2020 were included in this study. METHODS: We conducted a descriptive study of kidney transplant activity in Brazil in 2019 and 2020. RESULTS: A 23.9% decrease in kidney transplants per million population was observed during the pandemic period (22.9 in 2020 versus 30.1 in 2019). Kidney transplants with a living donor (-58.8%) and in the North Region (-79.5%) experienced the greatest declines. The pandemic waiting list increased by 6.8%, and deaths during the waiting period increased by 36.8%. The number of patients on the waiting list and transplant teams decreased by 31.3% and 9.5%, respectively. CONCLUSION: The COVID-19 pandemic drastically affected Brazil and had a significant negative impact on KT activities in the country.


INTRODUCTION
After the outbreak in China, severe acute respiratory syndrome coronavirus 2 (SARS-  infection has rapidly spread to other countries and continents. The pandemic of coronavirus disease  has reached services, systems, and global society. The first case of COVID-19 in Brazil was confirmed in mid-February 2020, and within days the number of cases increased dramatically. 1 The Brazilian epicenter of COVID-19 was in the southern region, in the city of São Paulo. However, several cities in the north and northeast of the country also experienced alarmingly high numbers of cases and deaths in the first months of the disease's registration. 1 the side effects of COVID-19 go beyond devastating damage to human health and undermine the structure, processes, and outcomes of a nation's services and systems. Despite its certified efficiency, the Brazilian National Transplant System was not exempt from the side effects of COVID-19, and the first negative impact of the pandemic on the organ donationtransplant process in Brazil was observed in the first quarter of 2020. 2 Compared with the same period in 2019, there was a 9.5% decrease in heart transplants and a 30% and 22.2% decrease in the number of living kidney and liver donors, respectively, in the first quarter of 2020. Of the 27 Brazilian states, only six (22.2%) performed pancreas transplants, and one state in the Northeast saw a 27% decrease in liver transplants. Additionally, there was a significant decrease in the number of transplants for all solid organs in March 2020 compared with January and February 2 which corresponds to the period when records of COVID-19 infections began in the country, resulting in an exponential increase in the number of confirmed cases. Alternatively, we observed an increase in the rate of effective donors compared to the same period in 2019, especially due to the sharp decrease in the family rejection rate, which was below 40% for the first time. 2 Analysis of pre-pandemic data showed that between 1995

OBJECTIVE
To compare the kidney transplantation activities registered in Brazil between the pandemic (2020) and pre-pandemic

Statistical analysis
All statistical analyzes were performed in the Microsoft Excel, version 2010, and we present descriptive data for all variables of interest. Data from the pandemic (2020) and pre-pandemic (2019) periods were compared by calculating the percentage difference between the years of interest.

Ethical approval
We analyzed data from the Brazilian Transplantation Registry, which was made publicly available by the Brazilian Organ Transplantation Society. since we used publicly available data, it was not necessary to obtain formal consent for developing the study because the data were publicly available, patients were not identified, and sources were accurately cited.

Kidney transplantation activities
During the pandemic and pre-pandemic periods, 22.9 and 30.1 kidney transplants per million population were performed, respectively, a 23.9% decrease from the COVID-19 era. The largest decreases occurred in living donor kidney transplants (-58.8%) and in the Northern region (-79.5%) ( Table 1). The percentage difference between kidney transplant volume and estimated demand was higher in the pandemic period (61.8%) than in the pre-pandemic period (49.8%) ( Table 2). Analyzing data from each Brazilian state, we found that the decrease in kidney transplantation procedures was consonant with the increase in the incidence of COVID-19 (Figure 1).

Waiting list and transplant teams
During the pandemic period (2020), there were 26,862 patients on the kidney transplant waiting list, compared with 25,163 during the pre-pandemic period, an increase of 6.8% ( Figure 2A). The number of patients newly added to the waiting list decreased by 31.3% and was 9,064 in the pandemic period and 13,194 in the pre-pandemic period ( Figure 2B).
The number of patients who died on the waiting list before receiving a kidney transplant increased by 36.8% and to 1,780 in the pandemic period and 1,301 in the pre-pandemic period ( Figure 2C). The number of transplant teams was 133 during the pandemic period and 147 in the pre-pandemic period, a decrease of 9.5% ( Figure 2D).  This negative outlook has also been observed in other countries, 7   As shown in Table 2, the COVID-19 pandemic increased the percentage difference between the demand and supply of kidneys for transplantation. However, being a country with a large geographic area, the decline in kidney transplantation in Brazil shows considerable variation among the different regions of the country ( Table 1). The decline in kidney transplantation rates showed a geographic distribution related to the increase in COVID-19

DISCUSSION
contamination rates (Figure 1). The availability of resources in a region directly impacts kidney transplantation rates, as this is a factor that has contributed to the suspension or reduction in activity. 7 in a particular hospital, it is recommended to refer patients or even organs to the nearest service that can perform the procedure. 16 The recommendations of the Brazilian Organ Transplantation Society for Brazilian programs to maintain kidney transplantation activity are plausible and defensible.
During the pandemic period, the number of patients on the waiting list increased (Figure 2A), but the number of new patients added to the waiting list decreased ( Figure 2B). These data are consistent with other studies conducted worldwide, and several countries have implemented strategies to minimize the impact of COVID-19 on kidney transplant program activity. 7,14 The inactivity of the waiting list may have an impact on the congestion of Brazilian dialysis centers in the period after COVID-19, as is likely to be the case in other countries. 7 Despite global concern about infection of kidney transplant recipients with the SARS Cov-2 virus, a study conducted in the United States has shown that patients on the waiting list are at significantly higher risk of hospitalization and death compared with kidney transplant recipients. 17 In the United Kingdom, 10% of patients on the waiting list and with COVID-19 died. 18 In France, 42% of deaths of patients on the waiting list were attributable to COVID-19. 19 We cannot retrieve specific Brazilian data; however, we verified that the number of deaths on the waiting list increased during the pandemic period cleared for transplant 28 days after infection). 22 As in Brazil, the United States, 10 Canada, 23 Spain, 13 Italy, 11 the United Kingdom, 9 and the Netherlands 24 implemented good organ donation and transplantation practices during the COVID-19 pandemic.

Future perspectives
The Brazilian Transplant System is an international reference, mainly because of the financial subsidy of almost all transplants by the public health system. 25 However, looking to the post-COVID-19 era, we believe that Brazil will have a gradual, slow, and regionalized recovery, both in terms of the good kidney transplant rates that the country had in the pre-pandemic period and in several other areas. The inequality of income and resources among Brazilian regions was even greater during COVID-19, and integration among the system, health services, and society will be essential for the country's recovery.

CONCLUSION
The COVID-19 pandemic has drastically affected Brazil and had a significant negative impact on kidney transplant activity in the country. This is the first study to analyze national data on kid-