SARS-CoV-2 antibody dynamics in blood donors and COVID-19 epidemiology in eight Brazilian state capitals: A serial cross-sectional study

  1. Carlos A Prete Jr  Is a corresponding author
  2. Lewis Fletcher Buss
  3. Charles Whittaker
  4. Tassila Salomon
  5. Marcio K Oikawa
  6. Rafael HM Pereira
  7. Isabel CG Moura
  8. Lucas Delerino
  9. Manoel Barral-Netto
  10. Natalia M Tavares
  11. Rafael FO Franca
  12. Viviane S Boaventura
  13. Fabio Miyajima
  14. Alfredo Mendrone-Junior
  15. Cesar de Almeida-Neto
  16. Nanci A Salles
  17. Suzete C Ferreira
  18. Karine A Fladzinski
  19. Luana M de Souza
  20. Luciane K Schier
  21. Patricia M Inoue
  22. Lilyane A Xabregas
  23. Myuki AE Crispim
  24. Nelson Fraiji
  25. Fernando LV Araujo
  26. Luciana MB Carlos
  27. Veridiana Pessoa
  28. Maisa A Ribeiro
  29. Rosenvaldo E de Souza
  30. Sônia MN da Silva
  31. Anna F Cavalcante
  32. Maria IB Valença
  33. Maria V da Silva
  34. Esther Lopes
  35. Luiz Amorim Filho
  36. Sheila OG Mateos
  37. Gabrielle T Nunes
  38. Alexander L Silva-Junior
  39. Michael P Busch
  40. Marcia C Castro
  41. Christopher Dye
  42. Oliver Ratmann
  43. Nuno R Faria  Is a corresponding author
  44. Vítor H Nascimento  Is a corresponding author
  45. Ester C Sabino  Is a corresponding author
  1. University of São Paulo, Brazil
  2. Imperial College London, United Kingdom
  3. Faculdade de Ciências Médicas de Minas Gerais, Brazil
  4. Universidade Federal do ABC, Brazil
  5. Institute for Applied Economic Research, Brazil
  6. Fundação Oswaldo Cruz, Brazil
  7. Fundacao Oswaldo Cruz, Brazil
  8. Fundação Pró-Sangue Hemocentro de São Paulo, Brazil
  9. Fundação Pró Sangue Hemocentro de São Paulo, Brazil
  10. Centro de Hematologia e Hemoterapia do Paraná, Brazil
  11. Fundação Hospitalar de Hematologia e Hemoterapia do Amazonas, Brazil
  12. Fundação de Hematologia e Hemoterapia da Bahia, Brazil
  13. Centro de Hematologia e Hemoterapia do Ceará, Brazil
  14. Fundação Centro de Hematologia e Hemoterapia de Minas Gerais, Brazil
  15. Fundação de Hematologia e Hemoterapia de Pernambuco, Brazil
  16. Instituto Estadual de Hematologia Arthur de Siqueira Cavalcanti, Brazil
  17. Vitalant Research Institute, United States
  18. Harvard TH Chan School of Public Health, United States
  19. University of Oxford, United Kingdom
  20. Universidade de São Paulo, Brazil

Abstract

Background: The COVID-19 situation in Brazil is complex due to large differences in the shape and size of regional epidemics. Understanding these patterns is crucial to understand future outbreaks of SARS-CoV-2 or other respiratory pathogens in the country.

Methods: We tested 97,950 blood donation samples for IgG antibodies from March 2020 to March 2021 in eight of Brazil’s most populous cities. Residential postal codes were used to obtain representative samples. Weekly age- and sex- specific seroprevalence was estimated by correcting the crude seroprevalence by test sensitivity, specificity and antibody waning.

Results: The inferred attack rate of SARS-CoV-2 in December 2020, before the Gamma VOC was dominant, ranged from 19.3% (95% CrI 17.5% - 21.2%) in Curitiba to 75.0% (95% CrI 70.8% - 80.3%) in Manaus. Seroprevalence was consistently smaller in women and donors older than 55 years. The age-specific infection fatality rate (IFR) differed between cities and consistently increased with age. The infection hospitalisation rate (IHR) increased significantly during the Gamma-dominated second wave in Manaus, suggesting increased morbidity of the Gamma VOC compared to previous variants circulating in Manaus. The higher disease penetrance associated with the health system's collapse increased the overall IFR by a minimum factor of 2.91 (95% CrI 2.43 - 3.53).

Conclusions: These results highlight the utility of blood donor serosurveillance to track epidemic maturity and demonstrate demographic and spatial heterogeneity in SARS-CoV-2 spread.

Funding: This work was supported by Itaú Unibanco 'Todos pela Saude' program; FAPESP (grants 18/14389-0, 2019/21585-0); Wellcome Trust and Royal Society Sir Henry Dale Fellowship 204311/Z/16/Z; the Gates Foundation (INV- 034540 and INV-034652); REDS-IV-P (grant HHSN268201100007I); the UK Medical Research Council (MR/S0195/1, MR/V038109/1); CAPES; CNPq (304714/2018-6); Fundação Faculdade de Medicina; Programa Inova Fiocruz-CE/Funcap - Edital 01/2020 Number: FIO-0167-00065.01.00/20 SPU Nº06531047/2020; JBS - Fazer o bem faz bem.

Data availability

All serological data required to reproduce the analyses are available at Data Dryad (doi:10.5061/dryad.dz08kps08) and can be downloaded at https://datadryad.org/stash/dataset/doi:10.5061/dryad.dz08kps08. The codes used for the main analyses are available at https://github.com/CADDE-CENTRE/seroprevalence_eight_cities.

The following data sets were generated

Article and author information

Author details

  1. Carlos A Prete Jr

    Department of Electronic Systems Engineering, University of São Paulo, São Paulo, Brazil
    For correspondence
    carlos.prete@usp.br
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3907-423X
  2. Lewis Fletcher Buss

    Imperial College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  3. Charles Whittaker

    Imperial College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  4. Tassila Salomon

    Faculdade de Ciências Médicas de Minas Gerais, Belo Horizonte, Brazil
    Competing interests
    The authors declare that no competing interests exist.
  5. Marcio K Oikawa

    Universidade Federal do ABC, São Bernardo do Campo, Brazil
    Competing interests
    The authors declare that no competing interests exist.
  6. Rafael HM Pereira

    Institute for Applied Economic Research, Brasília, Brazil
    Competing interests
    The authors declare that no competing interests exist.
  7. Isabel CG Moura

    Faculdade de Ciências Médicas de Minas Gerais, Belo Horizonte, Brazil
    Competing interests
    The authors declare that no competing interests exist.
  8. Lucas Delerino

    Fundação Oswaldo Cruz, Manguinhos, Brazil
    Competing interests
    The authors declare that no competing interests exist.
  9. Manoel Barral-Netto

    Fundacao Oswaldo Cruz, Manguinhos, Brazil
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5823-7903
  10. Natalia M Tavares

    Fundação Oswaldo Cruz, Manguinhos, Brazil
    Competing interests
    The authors declare that no competing interests exist.
  11. Rafael FO Franca

    Fundação Oswaldo Cruz, Manguinhos, Brazil
    Competing interests
    The authors declare that no competing interests exist.
  12. Viviane S Boaventura

    Fundação Oswaldo Cruz, Manguinhos, Brazil
    Competing interests
    The authors declare that no competing interests exist.
  13. Fabio Miyajima

    Fundação Oswaldo Cruz, Manguinhos, Brazil
    Competing interests
    The authors declare that no competing interests exist.
  14. Alfredo Mendrone-Junior

    Fundação Pró-Sangue Hemocentro de São Paulo, São Paulo, Brazil
    Competing interests
    The authors declare that no competing interests exist.
  15. Cesar de Almeida-Neto

    Fundação Pró-Sangue Hemocentro de São Paulo, São Paulo, Brazil
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8490-4634
  16. Nanci A Salles

    Fundação Pró-Sangue Hemocentro de São Paulo, São Paulo, Brazil
    Competing interests
    The authors declare that no competing interests exist.
  17. Suzete C Ferreira

    Fundação Pró Sangue Hemocentro de São Paulo, São Paulo, Brazil
    Competing interests
    The authors declare that no competing interests exist.
  18. Karine A Fladzinski

    Centro de Hematologia e Hemoterapia do Paraná, Curitiba, Brazil
    Competing interests
    The authors declare that no competing interests exist.
  19. Luana M de Souza

    Centro de Hematologia e Hemoterapia do Paraná, Curitiba, Brazil
    Competing interests
    The authors declare that no competing interests exist.
  20. Luciane K Schier

    Centro de Hematologia e Hemoterapia do Paraná, Curitiba, Brazil
    Competing interests
    The authors declare that no competing interests exist.
  21. Patricia M Inoue

    Centro de Hematologia e Hemoterapia do Paraná, Curitiba, Brazil
    Competing interests
    The authors declare that no competing interests exist.
  22. Lilyane A Xabregas

    Fundação Hospitalar de Hematologia e Hemoterapia do Amazonas, Manaus, Brazil
    Competing interests
    The authors declare that no competing interests exist.
  23. Myuki AE Crispim

    Fundação Hospitalar de Hematologia e Hemoterapia do Amazonas, Manaus, Brazil
    Competing interests
    The authors declare that no competing interests exist.
  24. Nelson Fraiji

    Fundação Hospitalar de Hematologia e Hemoterapia do Amazonas, Manaus, Brazil
    Competing interests
    The authors declare that no competing interests exist.
  25. Fernando LV Araujo

    Fundação de Hematologia e Hemoterapia da Bahia, Salvador, Brazil
    Competing interests
    The authors declare that no competing interests exist.
  26. Luciana MB Carlos

    Centro de Hematologia e Hemoterapia do Ceará, Fortaleza, Brazil
    Competing interests
    The authors declare that no competing interests exist.
  27. Veridiana Pessoa

    Centro de Hematologia e Hemoterapia do Ceará, Fortaleza, Brazil
    Competing interests
    The authors declare that no competing interests exist.
  28. Maisa A Ribeiro

    Fundação Centro de Hematologia e Hemoterapia de Minas Gerais, Belo Horizotne, Brazil
    Competing interests
    The authors declare that no competing interests exist.
  29. Rosenvaldo E de Souza

    Fundação Centro de Hematologia e Hemoterapia de Minas Gerais, Belo Horizotne, Brazil
    Competing interests
    The authors declare that no competing interests exist.
  30. Sônia MN da Silva

    Fundação Centro de Hematologia e Hemoterapia de Minas Gerais, Belo Horizotne, Brazil
    Competing interests
    The authors declare that no competing interests exist.
  31. Anna F Cavalcante

    Fundação de Hematologia e Hemoterapia de Pernambuco, Recife, Brazil
    Competing interests
    The authors declare that no competing interests exist.
  32. Maria IB Valença

    Fundação de Hematologia e Hemoterapia de Pernambuco, Recife, Brazil
    Competing interests
    The authors declare that no competing interests exist.
  33. Maria V da Silva

    Fundação de Hematologia e Hemoterapia de Pernambuco, Recife, Brazil
    Competing interests
    The authors declare that no competing interests exist.
  34. Esther Lopes

    Instituto Estadual de Hematologia Arthur de Siqueira Cavalcanti, Rio de Janeiro, Brazil
    Competing interests
    The authors declare that no competing interests exist.
  35. Luiz Amorim Filho

    Instituto Estadual de Hematologia Arthur de Siqueira Cavalcanti, Rio de Janeiro, Brazil
    Competing interests
    The authors declare that no competing interests exist.
  36. Sheila OG Mateos

    Instituto Estadual de Hematologia Arthur de Siqueira Cavalcanti, Rio de Janeiro, Brazil
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5416-2724
  37. Gabrielle T Nunes

    Instituto Estadual de Hematologia Arthur de Siqueira Cavalcanti, Rio de Janeiro, Brazil
    Competing interests
    The authors declare that no competing interests exist.
  38. Alexander L Silva-Junior

    Fundação Hospitalar de Hematologia e Hemoterapia do Amazonas, Manaus, Brazil
    Competing interests
    The authors declare that no competing interests exist.
  39. Michael P Busch

    Vitalant Research Institute, San Franscico, United States
    Competing interests
    The authors declare that no competing interests exist.
  40. Marcia C Castro

    Harvard TH Chan School of Public Health, Boston, United States
    Competing interests
    The authors declare that no competing interests exist.
  41. Christopher Dye

    Department of Zoology, University of Oxford, Oxford, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  42. Oliver Ratmann

    Imperial College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8667-4118
  43. Nuno R Faria

    Imperial College London, London, United Kingdom
    For correspondence
    nfaria@ic.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
  44. Vítor H Nascimento

    Department of Electronic Systems Engine, Universidade de São Paulo, São Paulo, Brazil
    For correspondence
    vitnasci@usp.br
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0543-4735
  45. Ester C Sabino

    Instituto de Medicina Tropical, University of São Paulo, São Paulo, Brazil
    For correspondence
    sabinoec@gmail.com
    Competing interests
    The authors declare that no competing interests exist.

Funding

Itau Unibanco (Todos pela Saúde)

  • Nuno R Faria
  • Ester C Sabino

CNPq (304714/2018-6)

  • Vítor H Nascimento

FAPESP

  • Suzete C Ferreira

Programa Inova FIOCRUZ-CE/Funcap (Edital 01/2020 Number: FIO-0167-00065.01.00/20 SPU Nº 06531047/2020)

  • Fabio Miyajima

CNPq

  • Manoel Barral-Netto

JBS - Fazer o bem faz bem

  • Rafael FO Franca

Medical Research Council (MR/V038109/1)

  • Oliver Ratmann

FAPESP (18/14389-0)

  • Nuno R Faria
  • Ester C Sabino

Medical Research Council (MR/S0195/1)

  • Nuno R Faria
  • Ester C Sabino

Wellcome Trust and Royal Society (Sir Henry Dale Fellowship 204311/Z/16/Z)

  • Nuno R Faria

Gates Foundation (INV- 034540 and INV-034652)

  • Nuno R Faria
  • Ester C Sabino

National Heart, Lung, and Blood Institute Recipient Epidemiology and Donor Evaluation Study (HHSN268201100007I)

  • Nuno R Faria
  • Ester C Sabino

FAPESP (2019/21858-0)

  • Carlos A Prete Jr

Fundacao Faculdade de Medicina

  • Carlos A Prete Jr

CAPES (Finance Code 001)

  • Carlos A Prete Jr
  • Vítor H Nascimento

The National Heart, Lung, and Blood Institute Recipient Epidemiology and Donor Evaluation Study (REDS-IV-P) provided blood donor demographic and zip code data for analysis. The other funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Human subjects: This project was approved by the Brazilian national research ethics committee, CONEP CAAE - 30178220.3.1001.0068. The Brazilian national research committee (CONEP) waived for informed consent. All methods were performed in accordance with relevant guidelines and regulations.

Reviewing Editor

  1. James M McCaw, The University of Melbourne, Australia

Publication history

  1. Received: February 28, 2022
  2. Accepted: September 17, 2022
  3. Accepted Manuscript published: September 22, 2022 (version 1)
  4. Accepted Manuscript updated: September 23, 2022 (version 2)

Copyright

© 2022, Prete et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Carlos A Prete Jr
  2. Lewis Fletcher Buss
  3. Charles Whittaker
  4. Tassila Salomon
  5. Marcio K Oikawa
  6. Rafael HM Pereira
  7. Isabel CG Moura
  8. Lucas Delerino
  9. Manoel Barral-Netto
  10. Natalia M Tavares
  11. Rafael FO Franca
  12. Viviane S Boaventura
  13. Fabio Miyajima
  14. Alfredo Mendrone-Junior
  15. Cesar de Almeida-Neto
  16. Nanci A Salles
  17. Suzete C Ferreira
  18. Karine A Fladzinski
  19. Luana M de Souza
  20. Luciane K Schier
  21. Patricia M Inoue
  22. Lilyane A Xabregas
  23. Myuki AE Crispim
  24. Nelson Fraiji
  25. Fernando LV Araujo
  26. Luciana MB Carlos
  27. Veridiana Pessoa
  28. Maisa A Ribeiro
  29. Rosenvaldo E de Souza
  30. Sônia MN da Silva
  31. Anna F Cavalcante
  32. Maria IB Valença
  33. Maria V da Silva
  34. Esther Lopes
  35. Luiz Amorim Filho
  36. Sheila OG Mateos
  37. Gabrielle T Nunes
  38. Alexander L Silva-Junior
  39. Michael P Busch
  40. Marcia C Castro
  41. Christopher Dye
  42. Oliver Ratmann
  43. Nuno R Faria
  44. Vítor H Nascimento
  45. Ester C Sabino
(2022)
SARS-CoV-2 antibody dynamics in blood donors and COVID-19 epidemiology in eight Brazilian state capitals: A serial cross-sectional study
eLife 11:e78233.
https://doi.org/10.7554/eLife.78233
  1. Further reading

Further reading

    1. Epidemiology and Global Health
    Catherine Meh, Prabhat Jha
    Research Article

    Preference for sons and smaller families and, in the case of China, a one-child policy, have contributed to missing girl births in India and China over the last few decades due to sex-selective abortions. Selective abortion occurs also among Indian and Chinese diaspora, but their variability and trends over time are unknown. We examined conditional sex ratio (CSR) of girl births per 1000 boy births among second or third births following earlier daughters or sons in India, China, and their diaspora in Australia, Canada, United Kingdom (UK), and United States (US) drawing upon 18.4 million birth records from census and nationally representative surveys from 1999 to 2019. Among Indian women, the CSR in 2016 for second births following a first daughter favoured boys in India (866), similar to those in diaspora in Australia (888) and Canada (882). For third births following two earlier daughters in 2016, CSRs favoured sons in Canada (520) and Australia (653) even more than in India (769). Among women in China outside the one-child restriction, CSRs in 2015 for second order births somewhat favoured more girls after a first son (1154) but more heavily favoured boys after a first daughter (561). Third-birth CSRs generally fell over time among diaspora, except among Chinese diaspora in the UK and US. In the UK, third-birth CSRs fell among Indian but not among other South Asian diasporas. Selective abortion of girls is notable among Indian diaspora, particularly at higher-order births.

    1. Epidemiology and Global Health
    Yupeng Liu, Siyu Le ... Shuran Wang
    Research Article

    Background:

    The effect of calcium supplementation on bone mineral accretion in people under 35 years old is inconclusive. To comprehensively summarize the evidence for the effect of calcium supplementation on bone mineral accretion in young populations (≤35 years).

    Methods:

    This is a systematic review and meta-analysis. The Pubmed, Embase, ProQuest, CENTRAL, WHO Global Index Medicus, Clinical Trials.gov, WHO ICTRP, China National Knowledge Infrastructure (CNKI), and Wanfang Data databases were systematically searched from database inception to April 25, 2021. Randomized clinical trials assessing the effects of calcium supplementation on bone mineral density (BMD) or bone mineral content (BMC) in people under 35 years old.

    Results:

    This systematic review and meta-analysis identified 43 studies involving 7,382 subjects. Moderate certainty of evidence showed that calcium supplementation was associated with the accretion of BMD and BMC, especially on femoral neck (standardized mean difference [SMD] 0.627, 95% confidence interval [CI] 0.338–0.915; SMD 0.364, 95% CI 0.134–0.595; respectively) and total body (SMD 0.330, 95% CI 0.163–0.496; SMD 0.149, 95% CI 0.006–0.291), also with a slight improvement effect on lumbar spine BMC (SMD 0.163, 95% CI 0.008–0.317), no effects on total hip BMD and BMC and lumbar spine BMD were observed. Very interestingly, subgroup analyses suggested that the improvement of bone at femoral neck was more pronounced in the peripeak bone mass (PBM) population (20–35 years) than the pre-PBM population (<20 years).

    Conclusions:

    Our findings provided novel insights and evidence in calcium supplementation, which showed that calcium supplementation significantly improves bone mass, implying that preventive calcium supplementation before or around achieving PBM may be a shift in the window of intervention for osteoporosis.

    Funding:

    This work was supported by Wenzhou Medical University grant [89219029].