Abstract

Objective

To describe organ donations and transplants in Ceará state, Brazil, following the declaration of the COVID-19 pandemic.

Methods

This was a descriptive study using data from the Brazilian Organ Transplantation Association. The number of donors and transplants from April to June 2020 was compared to the same period in 2019 and to the first quarter of 2020.

Results

In the first half of 2020, the state registered 72 effective donors, just 17 (23.6%) of whom related to the second quarter. Of the 352 transplants in the first half of 2020, 37 (10.7%) were performed in the second quarter. Compared with the period from April to June 2019, there was a reduction of 67.9% and 89.3% in the number of donors and transplants, respectively, in the same period of 2020.

Conclusion

The number of donors and transplants in Ceará showed an important fall in the three months following the declaration of the COVID-19 pandemic, especially for kidney, heart and cornea transplants.

Transplantation; Tissue and Organ Procurement; Tissue Donors; Pandemics; Coronavirus Infections

Introduction

At the end of 2019 the world looked on as a new disease caused by Coronavirus 2 (SARS-CoV-2) emerged. The disease was given the name COVID-19 and its signs and symptoms include fever, breathing difficulty and pulmonary infiltrates, and its outcomes can include accentuated inflammatory response, cardiopulmonary and multisystem organ failure.¹1. World Health Organization - WHO. Novel coronavirus China: disease outbreak news [Internet]. Geneva: World Health Organization; 2020 [cited 2020 Aug 18]. Available from: https://www.who.int/csr/don/12-january-2020-novel-coronavirus-china/en/
https://www.who.int/csr/don/12-january-2...

On March 11^th 2020, the World Health Organization (WHO) declared the disease to be a pandemic.⁵5. World Health Organization - WHO. WHO Director-General’s opening remarks at the media briefing on COVID-19 – 11 March 2020 [Internet]. Geneva: World Health Organization; 2020 [cited 2020 Aug 18]. Available from: https://www.who.int/dg/speeches/detail/who-director-general-s-opening-remarks-at-the-media-briefing-on-covid-19---11-march-2020
https://www.who.int/dg/speeches/detail/w... Brazil’s first COVID-19 case was confirmed in February and its first COVID-19 death in March.⁶6. Cavalcante JR, Cardoso-dos-Santos AC, Bremm JM, Lobo AP, Macário EM, Oliveira WK, et al. COVID-19 in Brazil: evolution of the epidemic up until epidemiological week 20 of 2020. Epidemiol Serv Saúde [Internet]. 2020 Aug [cited 2020 Aug 19];29(4):e2020376. Available from: http://dx.doi.org/10.5123/s1679-49742020000400010
http://dx.doi.org/10.5123/s1679-49742020... In Ceará state, as at June 29^th, there were 108,136 cases, 6,153 deaths and the lethality rate was 5.7%.⁷7. Secretaria da Saúde do Estado (Ceará). Doença pelo novo coronavírus (COVID-19). Bol Epidemiol Ceará [Internet]. 2020 jul [citado 2020 jul 31];32. Disponível em: https://drive.google.com/file/d/165L0RChieKW1WTqbaBuEv7eRj5TvjUVC/view
https://drive.google.com/file/d/165L0RCh...

The spread of COVID-19 has significantly restricted transplantation programs worldwide.⁸8. Zhang H, Dai H, Xie X. Solid organ transplantation during the COVID-19 pandemic. Front Immunol [Internet]. 2020 Jun [cited 2020 Jul 31];11:1-9. Available from: https://doi.org/10.3389/fimmu.2020.01392
https://doi.org/10.3389/fimmu.2020.01392... In Brazil, in the second quarter of 2020, there was a decrease in liver (6.9%), kidney (18.4%), heart (27.1%), lung (27.1%), pancreas (29.1%) and especially cornea (44.3%) transplants due to most transplantation services being suspended.⁹9. Associação Brasileira de Transplante de Órgãos – ABTO. Dados numéricos da doação de órgãos e transplantes realizados por estado e instituição no período: janeiro/junho – 2020 [Internet]. São Paulo: ABTO; 2020 [citado 2020 ago 25]. 22 p. Disponível em: https://site.abto.org.br/publicacao/ano-xxvi-no-2/
https://site.abto.org.br/publicacao/ano-...

Considering the impacts in this area, the objective of this article was to describe organ donations and transplants in Ceará state following the declaration of the COVID-19 pandemic.

Methods

This is a descriptive study based on the number of potential deceased donors, effective donors and transplants performed in the state of Ceará between April and June 2020. The data were retrieved in September 2020 from the Brazilian Transplant Registry,⁹9. Associação Brasileira de Transplante de Órgãos – ABTO. Dados numéricos da doação de órgãos e transplantes realizados por estado e instituição no período: janeiro/junho – 2020 [Internet]. São Paulo: ABTO; 2020 [citado 2020 ago 25]. 22 p. Disponível em: https://site.abto.org.br/publicacao/ano-xxvi-no-2/
https://site.abto.org.br/publicacao/ano-... following access provided by the Brazilian Organ Transplant Association (ABTO), which updates these indicators cumulatively on a quarterly basis.

In 2020, Ceará has an estimated population of 9,187,103 inhabitants and a Human Development Index of 0.682.¹³13. Instituto Brasileiro de Geografia e Estatística – IBGE. Cidades e estados: Ceará [Internet]. Rio de Janeiro: IBGE; 2020 [citado 2020 set 04]. Disponível em: https://www.ibge.gov.br/cidades-e-estados/ce.html
https://www.ibge.gov.br/cidades-e-estado... In 2019, the state recorded 1,454 transplants, involving kidney, liver, pancreas, heart, liver and cornea transplants. At that time, almost three months prior to the pandemic, Ceará had the largest number of liver and cornea transplants among the other Northeast Brazilian states.¹⁴14. Associação Brasileira de Transplante de Órgãos – ABTO. Dimensionamento dos transplantes no Brasil e em cada estado (2012-2019) [Internet]. São Paulo: ABTO; 2019 [citado 2020 ago 01]. 100 p. Disponível em: https://site.abto.org.br/publicacao/rbt-2019/
https://site.abto.org.br/publicacao/rbt-...

The variables taken into consideration in this analysis were the absolute frequencies of potential deceased donors and effective donors, and the number of liver, kidney, heart and cornea transplants performed. Pancreas, pancreas-kidney and lung transplants were excluded because they had not been performed in 2020, even before the pandemic was declared.

The data were organized using the Excel computer program to obtain a descriptive analysis of the frequencies. Given the declaration of the pandemic in mid March and ABTO’s forecast that its impacts would be felt with effect from the second quarter,¹¹11. Associação Brasileira de Transplante de Órgãos – ABTO. Dados numéricos da doação de órgãos e transplantes realizados por estado e instituição no período: janeiro/março – 2020 [Internet]. São Paulo: ABTO; 2020 [citado 2020 set 12]. 20 p. Disponível em: https://docs.google.com/viewerng/viewer?url=https://site.abto.org.br/wp-content/uploads/2020/06/RBT-2020-1trim-leitura-1.pdf&hl=en
https://docs.google.com/viewerng/viewer?... the results for the period April to June 2020 were compared with those for the first quarter of the year, considering the absolute and relative frequency of each variable. In this way it was possible to follow the temporal evolution of donations and transplants immediately before and following the declaration of the pandemic. In order to arrive at the data for the period April to June, the figures for the first quarter were subtracted from the cumulative total as at the end of the second quarter (January to June).

The absolute frequencies of potential deceased donors, effective donors and transplants performed in the second quarter of 2020 were also compared with the corresponding frequencies for the same period in 2019, and the percentage change for each variable were calculated.

As this study used public information, in which cases are not identified, it did not need to be submitted for appraisal by a Research Ethics Committee.

Results

In the first semester quarter of 2020, Ceará had 72 effective donors, 55 of whom were notified in the first quarter (76.4%) and 17 in the second quarter (23.6%). With regard to transplants, of the 352 procedures in the first semester, 37 (10.5%) were carried out between April and June, indicating a fall in donations and transplants immediately after the pandemic was declared. Figure 1 shows the number of potential deceased donors, effective donors and transplants performed.

When analyzing each kind of transplant individually, it can be seen that the kidney and heart transplant programs were practically interrupted, with just one transplant of these two organs in the second quarter of 2020. Of the 71 liver transplants in the first semester, 16 (22.5%) were performed between April and June. Cornea transplants also fell considerably, with 190 (91%) procedures in the first quarter and 19 (9%) in the second quarter (Figure 1).

Table 1 shows the number of potential deceased donors, effective donors and transplants performed between April and June 2020. In comparison with the same period in 2019, there was a 38.8% reduction in the number of potential donors and a 67.9% reduction in the number of effective donors. In all, 37 transplants were recorded, this being 89.3% less than in the same period in 2019, when 348 procedures were performed. Kidney, heart and cornea transplants decreased most.

Discussion

The results point to a considerable reduction in the number of potential deceased donors and effective donors immediately after the COVID-19 pandemic was declared. All types of transplantation included in this study were affected, especially the kidney, heart and cornea transplantation programs.

When the first COVID-19 cases were confirmed in Ceará in March, the state government introduced social isolation measures,¹⁵15. Aquino EML, Silveira IH, Pescarini JM, Aquino R, Souza-Filho JA, Rocha AS, et al. Social distancing measures to control the COVID-19 pandemic: potential impacts and challenges in Brazil. Ciênc Saúde Coletiva [Internet]. 2020 Jun [cited 2020 Aug 21];25(Suppl 1):2423-46. Available from: https://doi.org/10.1590/1413-81232020256.1.10502020
https://doi.org/10.1590/1413-81232020256... with the aim of reducing infection and ensuring availability of hospital beds for people with severe COVID-19 symptoms. In the first fortnight, road traffic accidents fell by 61%.¹⁶16. Secretaria da Saúde do Estado (Ceará). Isolamento social aponta para redução de acidentes nas rodovias estaduais – 05/04/2020 [Internet]. Fortaleza: Secretaria da Saúde do Estado do Ceará; 2020 [citado 2020 ago 25]. Disponível em: https://www.saude.ce.gov.br/2020/04/05/isolamento-social-aponta-para-reducao-de acidentes-nas-rodovias-estaduais
https://www.saude.ce.gov.br/2020/04/05/i... However, in April and May there was an increase of almost 500% in occupation of hospital beds reserved for treatment of COVID-19. ICU beds at several hospitals became 100% occupied.¹⁷17. Secretaria da Saúde do Estado (Ceará). Doença pelo novo coronavírus (COVID-19). Bol Epidemiol Ceará [Internet]. 2020 maio [citado 2020 jul 31];26. Disponível em: https://coronavirus.ceara.gov.br/wp-content/uploads/2020/05/boletim_covid_n26_19_05_2020_v2.pdf
https://coronavirus.ceara.gov.br/wp-cont...

The reduction in notifications of potential donors may be related to the drop in road traffic accidents and the consequent impact on brain death cases. In addition, potential donors being infected with SARS-CoV-2 contributed to an even greater reduction in effective donors. Organ donation is absolutely contraindicated in the case of potential donors with active COVID-19, positive SARS-CoV-2 RT-PCR results for severe acute respiratory syndrome, with undefined etiology or undefined laboratory test results.²2. Ministério da Saúde (BR). Nota Técnica nº 25/2020 - Critérios técnicos para triagem clínica do coronavírus (SARS, MERS, SARS-CoV-2) nos candidatos à doação de órgãos e tecidos [Internet]. Brasília: Ministério da Saúde; 2020 [citado 2020 jul 31]. 10 p. Disponível em: https://portalarquivos.saude.gov.br/images/pdf/2020/May/07/Nota-t--cnica-N---25-2020-CGSNT-DAET-SAES-MS.pdf
https://portalarquivos.saude.gov.br/imag...

Ceará was the first state to implement testing of potential donors. Between March and June 2020, 23% of potential donors notified in the state tested positive for SARS-CoV-2,¹⁹19. Diário do Nordeste. Transplantes de órgãos caem pela metade durante pandemia e 23% dos potenciais doadores tiveram Covid [Internet]. Fortaleza: Diário do Nordeste; 2020 [atualizado 2020 ago 12; citado 2020 set 12]. Disponível em: https://diariodonordeste.verdesmares.com.br/metro/transplantes-de-orgaos-caem-pela-metade-durante-pandemia-e-23-dos-potenciais-doadores-tiveram-covid-1.2976817
https://diariodonordeste.verdesmares.com... which may have contributed to raising the rate of medical contraindication in relation to organ donation. In 2019, this rate was 17% in Ceará, while it jumped to 28% in the first semester of 2020.⁹9. Associação Brasileira de Transplante de Órgãos – ABTO. Dados numéricos da doação de órgãos e transplantes realizados por estado e instituição no período: janeiro/junho – 2020 [Internet]. São Paulo: ABTO; 2020 [citado 2020 ago 25]. 22 p. Disponível em: https://site.abto.org.br/publicacao/ano-xxvi-no-2/
https://site.abto.org.br/publicacao/ano-...

Ceará does not have hospitals that exclusively perform transplants, so that these procedures are carried out at large general hospitals which are also now caring for COVID-19 cases. As such, it is not possible to ensure areas totally free from risk of exposure to the virus for transplant patients. The transplantation centers have therefore reserved transplantation procedures for severe and urgent situations and have adopted more conservative measures in relation to using borderline donors.

In accordance with Ministry of Health guidelines, active tracing of circulatory death donors for cornea donation has been suspended, although donation of ocular tissues from brain death donors has been maintained.²2. Ministério da Saúde (BR). Nota Técnica nº 25/2020 - Critérios técnicos para triagem clínica do coronavírus (SARS, MERS, SARS-CoV-2) nos candidatos à doação de órgãos e tecidos [Internet]. Brasília: Ministério da Saúde; 2020 [citado 2020 jul 31]. 10 p. Disponível em: https://portalarquivos.saude.gov.br/images/pdf/2020/May/07/Nota-t--cnica-N---25-2020-CGSNT-DAET-SAES-MS.pdf
https://portalarquivos.saude.gov.br/imag... Liver transplants have continued, since for many diseases this is the only and immediate therapy. Ceará does not perform living-donor liver transplants.

With regard to kidney transplantation, substitute therapies such as dialysis have been considered. Living-donor kidney transplants have been suspended, in accordance with Ministry of Health recommendations to assess suspension of elective living-donor transplants during the period of SARS-CoV-2 community transmission.²2. Ministério da Saúde (BR). Nota Técnica nº 25/2020 - Critérios técnicos para triagem clínica do coronavírus (SARS, MERS, SARS-CoV-2) nos candidatos à doação de órgãos e tecidos [Internet]. Brasília: Ministério da Saúde; 2020 [citado 2020 jul 31]. 10 p. Disponível em: https://portalarquivos.saude.gov.br/images/pdf/2020/May/07/Nota-t--cnica-N---25-2020-CGSNT-DAET-SAES-MS.pdf
https://portalarquivos.saude.gov.br/imag... In the first semester of 2019, Ceará performed eight living-donor kidney transplants, while only one was performed in the same period in 2020.⁹9. Associação Brasileira de Transplante de Órgãos – ABTO. Dados numéricos da doação de órgãos e transplantes realizados por estado e instituição no período: janeiro/junho – 2020 [Internet]. São Paulo: ABTO; 2020 [citado 2020 ago 25]. 22 p. Disponível em: https://site.abto.org.br/publicacao/ano-xxvi-no-2/
https://site.abto.org.br/publicacao/ano-...

Studies indicate that there is still uncertainty about the risk of transmission of this disease, the immune response of recipients and exposure of healthy living donors.³3. Woolley AE, Mehra MR. Dilemma of organ donation in transplantation and the COVID-19 pandemic. J Heart Lung Transplant [Internet]. 2020 Mar [cited 2020 Jul 31];39(5):410-1. Available from: https://doi.org/10.1016/j.healun.2020.03.017
https://doi.org/10.1016/j.healun.2020.03... A systematic review indicated that the clinical presentation of COVID-19 in kidney transplant recipients can be different in the general population in view of a higher rate of the more severe form of the disease. Based on 24 studies and reports of 129 people who had had kidney transplants and became infected with SARS-CoV-2, the systematic review showed that, on average, 20% of infected recipients needed to be admitted to an ICU and 34.1% had acute kidney injury; the COVID-19 mortality rate was 18.8%, whereas among the general population it was 3.4%.²²22. Iman A, Abukhalaf SA, Imam R, Abu-Gazala S, Merhav H, Khalaileh A. Kidney transplantation in the times of COVID-19 – a literature review. Ann Transplant [Internet]. 2020 Jul [cited 2020 Oct 13];25:e925755. Available from: http://pesquisa.bvsalud.org/portal/resource/pt/mdl-32703929
http://pesquisa.bvsalud.org/portal/resou... With regard to liver transplantation, a prospective multi-center study conducted with COVID-19-infected recipients identified 12% lethality. This increased to 17% when taking only hospitalized recipients into consideration.²³23. Becchetti C, Zambelli MF, Pasulo L, Donato MF, Invernizzi F, Detry O, et al. COVID-19 in an international European liver transplant recipient cohort. Gut [Internet]. 2020 Jun [cited 2020 Oct 13];69:1832-40. Available from: https://gut.bmj.com/content/gutjnl/69/10/1832.full.pdf
https://gut.bmj.com/content/gutjnl/69/10...

In Spain there was a drastic reduction in the number of donors and transplants even in the first month of the pandemic.⁴4. Domínguez-Gil B, Coll E, Ferrer-Fábrega J, Briceño J, Ríos A. Drástico impacto de la epidemia de COVID-19 sobre la actividad de donación y trasplante en España. Cir Esp [Internet]. 2020 ago-set [citado 2020 jul 20];98(7):412-4. Disponible en: https://doi.org/10.1016/j.ciresp.2020.04.012
https://doi.org/10.1016/j.ciresp.2020.04... In Ceará, April and May were the most critical months and no kidney or heart transplants were performed then.²⁴24. Diário do Nordeste. Número de transplantes cai 48,4% durante pandemia no Ceará, aponta Associação [Internet]. Fortaleza: Diário do Nordeste; 2020 [atualizado 2020 ago 12; citado 2020 set 9]. Disponível em: https://diariodonordeste.verdesmares.com.br/metro/numero-de-transplantes-cai-484-durante-pandemia-no-ceara-aponta-associacao-1.2976687
https://diariodonordeste.verdesmares.com... In that period, kidneys continued to be removed from deceased donors with undetectable COVID-19 RT-PCR test results and with no clinical signs of the disease. Those kidneys were sent to the National Organ Transplantation Bank.

Multiple factors affect the reduction in donors and transplants, and it is related to social distancing, hospital capacity, reallocation of hospital beds and mechanical ventilators, reduced availability of health workers and uncertainty about results, which has led the transplantation centers to indicate the procedure only in severe situations.³3. Woolley AE, Mehra MR. Dilemma of organ donation in transplantation and the COVID-19 pandemic. J Heart Lung Transplant [Internet]. 2020 Mar [cited 2020 Jul 31];39(5):410-1. Available from: https://doi.org/10.1016/j.healun.2020.03.017
https://doi.org/10.1016/j.healun.2020.03...

This study analyzed a single scenario and only the single three-month period following the declaration of the pandemic. No comparisons were made with other Brazilian states. As no lung, pancreas or pancreas-kidney transplants were performed in Ceará in 2020, even before the pandemic was declared, this study only examined liver, kidney, heart and cornea transplants. Further studies are needed to monitor the impact on donations and transplants in the long term and in other scenarios.

We conclude that the numbers of donors and transplants in Ceará fell considerably in the three months following the declaration of the COVID-19 pandemic. This reduction may restrict patients being included on waiting lists and, consequently, increase the waiting time of recipients already on waiting lists, in addition to favoring complications. We therefore hope that the results of this study will inform the implementation of strategies that contribute to the safe return of transplantations in the state of Ceará.

References

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History