SARS-CoV-2 antibody dynamics in blood donors and COVID-19 epidemiology in eight Brazilian state capitals: A serial cross-sectional study
- University of São Paulo, Brazil
- Imperial College London, United Kingdom
- Faculdade de Ciências Médicas de Minas Gerais, Brazil
- Universidade Federal do ABC, Brazil
- Institute for Applied Economic Research, Brazil
- Fundação Oswaldo Cruz, Brazil
- Fundacao Oswaldo Cruz, Brazil
- Fundação Pró-Sangue Hemocentro de São Paulo, Brazil
- Fundação Pró Sangue Hemocentro de São Paulo, Brazil
- Centro de Hematologia e Hemoterapia do Paraná, Brazil
- Fundação Hospitalar de Hematologia e Hemoterapia do Amazonas, Brazil
- Fundação de Hematologia e Hemoterapia da Bahia, Brazil
- Centro de Hematologia e Hemoterapia do Ceará, Brazil
- Fundação Centro de Hematologia e Hemoterapia de Minas Gerais, Brazil
- Fundação de Hematologia e Hemoterapia de Pernambuco, Brazil
- Instituto Estadual de Hematologia Arthur de Siqueira Cavalcanti, Brazil
- Vitalant Research Institute, United States
- Harvard TH Chan School of Public Health, United States
- University of Oxford, United Kingdom
- 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.
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Data from: SARS-CoV-2 antibody dynamics in blood donors and COVID-19 epidemiology in eight Brazilian state capitalsDryad Digital Repository, doi:10.5061/dryad.dz08kps08.
Article and author information
Author details
Carlos A Prete Junior Jr.
Manoel Barral-Netto
Cesar de Almeida-Neto
Vítor H Nascimento
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 Junior Jr.
Fundacao Faculdade de Medicina
- Carlos A Prete Junior Jr.
CAPES (Finance Code 001)
- Carlos A Prete Junior 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.
Reviewing Editor
- James M McCaw, The University of Melbourne, Australia
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.
Version history
- Preprint posted: February 22, 2022 (view preprint)
- Received: February 28, 2022
- Accepted: September 17, 2022
- Accepted Manuscript published: September 22, 2022 (version 1)
- Accepted Manuscript updated: September 23, 2022 (version 2)
- Version of Record published: October 7, 2022 (version 3)
Copyright
© 2022, Prete Junior 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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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
Further reading
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- Epidemiology and Global Health
Background:
The Zanzibar archipelago of Tanzania has become a low-transmission area for Plasmodium falciparum. Despite being considered an area of pre-elimination for years, achieving elimination has been difficult, likely due to a combination of imported infections from mainland Tanzania and continued local transmission.
Methods:
To shed light on these sources of transmission, we applied highly multiplexed genotyping utilizing molecular inversion probes to characterize the genetic relatedness of 282 P. falciparum isolates collected across Zanzibar and in Bagamoyo district on the coastal mainland from 2016 to 2018.
Results:
Overall, parasite populations on the coastal mainland and Zanzibar archipelago remain highly related. However, parasite isolates from Zanzibar exhibit population microstructure due to the rapid decay of parasite relatedness over very short distances. This, along with highly related pairs within shehias, suggests ongoing low-level local transmission. We also identified highly related parasites across shehias that reflect human mobility on the main island of Unguja and identified a cluster of highly related parasites, suggestive of an outbreak, in the Micheweni district on Pemba island. Parasites in asymptomatic infections demonstrated higher complexity of infection than those in symptomatic infections, but have similar core genomes.
Conclusions:
Our data support importation as a main source of genetic diversity and contribution to the parasite population in Zanzibar, but they also show local outbreak clusters where targeted interventions are essential to block local transmission. These results highlight the need for preventive measures against imported malaria and enhanced control measures in areas that remain receptive to malaria reemergence due to susceptible hosts and competent vectors.
Funding:
This research was funded by the National Institutes of Health, grants R01AI121558, R01AI137395, R01AI155730, F30AI143172, and K24AI134990. Funding was also contributed from the Swedish Research Council, Erling-Persson Family Foundation, and the Yang Fund. RV acknowledges funding from the MRC Centre for Global Infectious Disease Analysis (reference MR/R015600/1), jointly funded by the UK Medical Research Council (MRC) and the UK Foreign, Commonwealth & Development Office (FCDO), under the MRC/FCDO Concordat agreement and is also part of the EDCTP2 program supported by the European Union. RV also acknowledges funding by Community Jameel.
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- Epidemiology and Global Health
- Microbiology and Infectious Disease
Background: Few national-level studies have evaluated the impact of 'hybrid' immunity (vaccination coupled with recovery from infection) from the Omicron variants of SARS-CoV-2.
Methods: From May 2020 to December 2022, we conducted serial assessments (each of ~4000-9000 adults) examining SARS-CoV-2 antibodies within a mostly representative Canadian cohort drawn from a national online polling platform. Adults, most of whom were vaccinated, reported viral test-confirmed infections and mailed self-collected dried blood spots to a central lab. Samples underwent highly sensitive and specific antibody assays to spike and nucleocapsid protein antigens, the latter triggered only by infection. We estimated cumulative SARS-CoV-2 incidence prior to the Omicron period and during the BA.1/1.1 and BA.2/5 waves. We assessed changes in antibody levels and in age-specific active immunity levels.
Results: Spike levels were higher in infected than in uninfected adults, regardless of vaccination doses. Among adults vaccinated at least thrice and infected more than six months earlier, spike levels fell notably and continuously for the nine months post-vaccination. By contrast, among adults infected within six months, spike levels declined gradually. Declines were similar by sex, age group, and ethnicity. Recent vaccination attenuated declines in spike levels from older infections. In a convenience sample, spike antibody and cellular responses were correlated. Near the end of 2022, about 35% of adults above age 60 had their last vaccine dose more than six months ago, and about 25% remained uninfected. The cumulative incidence of SARS-CoV-2 infection rose from 13% (95% CI 11-14%) before omicron to 78% (76-80%) by December 2022, equating to 25 million infected adults cumulatively. However, the COVID-19 weekly death rate during the BA.2/5 waves was less than half of that during the BA.1/1.1 wave, implying a protective role for hybrid immunity.
Conclusions: Strategies to maintain population-level hybrid immunity require up-to-date vaccination coverage, including among those recovering from infection. Population-based, self-collected dried blood spots are a practicable biological surveillance platform.
Funding: Funding was provided by the COVID-19 Immunity Task Force, Canadian Institutes of Health Research, Pfizer Global Medical Grants, and St. Michael's Hospital Foundation. PJ and ACG are funded by the Canada Research Chairs Program.
