Learning from Serosurveillance for SARS-CoV-2 to Inform Pandemic Preparedness and Response

The COVID-19 pandemic underlined the importance of serosurveillance as an evidence-based tool to understand population immunity, track viral transmission, and guide public health decision making.1Bergeri I Whelan MG Ware H et al.Global SARS-CoV-2 seroprevalence from January 2020 to April 2022: a systematic review and meta-analysis of standardized population-based studies.PLoS Med. 2022; 19e1004107Crossref PubMed Scopus (20) Google Scholar Since the start of the COVID-19 pandemic, more than 4200 seroprevalence studies have been done in over 145 countries by testing blood specimens from more than 34 million people.2Arora RK Joseph A Van Wyk J et al.SeroTracker: a global SARS-CoV-2 seroprevalence dashboard.Lancet Infect Dis. 2021; 21: e75-e76Summary Full Text Full Text PDF PubMed Scopus (100) Google Scholar In early 2023, the Robert Koch Institute, Germany's national public health institute, convened an online symposium about international serological studies that involved research organisations, national public health agencies, institutes, and regional public health agencies from low-income and middle-income countries. The invited participants reflected on lessons learned and drew practical conclusions on challenges, opportunities, and next steps (the participating groups are listed in the appendix). Attendees had implemented seroprevalence studies at the national or regional level since the start of the COVID-19 pandemic, and collectively addressed the questions on how to use this investment to maximise continued public health benefits and to inform future pandemic preparedness and response. Here, we discuss the primary lessons identified by the meeting attendees. First, serosurveillance data during the early phase of the COVID-19 pandemic was useful to understand national and regional outbreak dynamics, but its utility for public health decision making has now decreased with much of the world's population having been infected with or immunised against SARS-CoV-2.1Bergeri I Whelan MG Ware H et al.Global SARS-CoV-2 seroprevalence from January 2020 to April 2022: a systematic review and meta-analysis of standardized population-based studies.PLoS Med. 2022; 19e1004107Crossref PubMed Scopus (20) Google Scholar Serological studies now require a more tailored focus on vulnerable populations and also the inclusion of other pathogens. An important area of their application is to guide ongoing vaccination strategies. Here, seroprevalence studies need to focus on providing data to better understand protection of vulnerable populations, such as older people and those who are immunocompromised. This is of particular value in settings where constrained health-service provision or low vaccination uptake led to a low (continuous) vaccine coverage, that could be targeted by seroprevalence-led vaccination strategies.3Mutombo PN Fallah MP Munodawafa D et al.COVID-19 vaccine hesitancy in Africa: a call to action.Lancet Global Health. 2022; 10: e320-e321Summary Full Text Full Text PDF PubMed Scopus (0) Google Scholar To further increase our understanding of immunity to COVID-19, serological research needs to focus on quantitative antibody measurements and correlates of protection, such as the seroconversion and waning of antibodies against SARS-CoV-2. Additionally, the infrastructure developed for seroprevalence studies on SARS-CoV-2 now offers the potential to support multi-pathogen serosurveillance. Testing for different pathogens or biomakers of chronic disease would maximise the benefit of collected biosamples. Second, reflecting on the multitude of serosurveillance studies conducted during the pandemic, common methodological challenges were evident, notably the limitations of one-time assessments (eg, cross-sectional studies) and delays in study implementation and results sharing,4Donnici C Ilincic N Cao C et al.Timeliness of reporting of SARS-CoV-2 seroprevalence results and their utility for infectious disease surveillance.Epidemics. 2022; 41100645Crossref PubMed Scopus (1) Google Scholar which hampered the use of the results of seroprevalence studies in continuing surveillance and comparison of population immunity over time and across contexts. These challenges were compounded by the low comparability between studies with varied protocols and quality. This experience highlights that in any new pandemic scenario, resources need to be available immediately to enable rapid research decision making and underscores the importance of a coordinated approach as early as possible, such as that piloted by the WHO Unity Studies during the COVID-19 pandemic.5Bergeri I Lewis HC Subissi L et al.Early epidemiological investigations: World Health Organization UNITY protocols provide a standardized and timely international investigation framework during the COVID-19 pandemic.Influenza Other Respir Viruses. 2022; 16: 7-13Crossref PubMed Scopus (0) Google Scholar The national and regional protocols for serosurveillance studies developed by public health actors globally provide an important starting point. These should be collected and retained in a global or regional operational repository of open source protocols for SARS-CoV-2 and other pathogens. Such a repository would help address a range of public health questions to be shared, adapted, and implemented in a timely manner for preparedness and response to future pandemics. Third, biobanking is widely neglected but vital for pandemic preparedness, because it allows for retention of valuable samples from seroprevalence investigations. These samples can serve as a baseline for determining existing or endemic pathogen immunity levels and as negative controls to develop serological assays for a novel pathogen, as well as an aid in chronic disease surveillance through biomarker testing.6Peeling RW Boeras D Wilder-Smith A Sall A Nkengasong J Need for sustainable biobanking networks for COVID-19 and other diseases of epidemic potential.Lancet Infect Dis. 2020; 20: e268-e273Summary Full Text Full Text PDF PubMed Scopus (24) Google Scholar Indeed, when the question about re-infection with SARS-CoV-2 emerged in 2020, the scarcity of stored respiratory samples hindered a timely answer to this question.7Abu Raddad L Chemaitelly H Malek J et al.Assessment of the risk of SARS-CoV-2 reinfection in an intense re-exposure setting.Clin Infect Dis. 2021; 73: e1830-e1840Crossref PubMed Scopus (79) Google Scholar Moderate investment in strengthening biobank infrastructure regionally and globally has the potential to yield considerable public health gains and enable more rapid responses in the future. The World Bank's Pandemic Fund could provide resources to help to retain and improve in-country biobanking capacity as part of preparedness activities. These practical lessons highlight areas for continued use of serosurveillance for preparedness and response to ongoing and future pandemics that require action now (panel). There are already initiatives under way to support this agenda and provide important steps to overcome methodological challenges and delays in study implementation and sharing of results. These initiatives include work by WHO on collaborative surveillance8WHODefining collaborative surveillance: a core concept for strengthening the global architecture for health emergency preparedness, response, and resilience (HEPR).https://apps.who.int/iris/handle/10665/367927Date: 2023Date accessed: May 24, 2023Google Scholar and to establish an international framework and network to conduct seroepidemiological investigations and studies,9Mott JA Bergeri I Lewis HC Mounts AW Briand SC Facing the future of respiratory virus surveillance: “the mosaic surveillance framework”.Influenza Other Respir Viruses. 2023; 17e13122Crossref Scopus (0) Google Scholar including an operational repository of protocols and reporting and dissemination tools that can be adapted by countries to enhance analysis.5Bergeri I Lewis HC Subissi L et al.Early epidemiological investigations: World Health Organization UNITY protocols provide a standardized and timely international investigation framework during the COVID-19 pandemic.Influenza Other Respir Viruses. 2022; 16: 7-13Crossref PubMed Scopus (0) Google Scholar There are also other for profit and non-profit efforts to visualise and analyse multi-pathogen serological investigations. Additionally, the global community can benefit from current investment in human and laboratory capacities, but should call for the availability of ready-to-use funds for coordinated and timely response following the example of the Coalition for Epidemic Preparedness Innovations, an alliance to finance and coordinate the development of new vaccines to prevent and contain infectious disease epidemics.10Coalition for Epidemic Preparedness InnovationsDelivering pandemic vaccines in 100 days.https://cepi.net/wp-content/uploads/2022/11/CEPI-100-Days-Report-Digital-Version_29-11-22.pdf?swcfpc=1Date: 2022Date accessed: April 20, 2023Google Scholar Most importantly, these funds should account for global strengthening of biobank infrastructure, including multi-pathogen serosurveillance and the storing of samples. Sustaining and building on the investments in serosurveillance made over the past 3 years will be crucial for strengthening pandemic preparedness and response and improving global public health.PanelActions to take now to improve pandemic preparedness through serosurveillanceRefine the focus of ongoing serological studies on SARS-CoV-2•Guidance for ongoing vaccination strategies•Research on COVID-19 immunity•Shift towards multi-pathogen serosurveillanceBuild an operational protocol repository•Coordinated and timely response•Designated funding for use in current (eg, outbreaks and seasonal epidemics) and future applicationsStrengthen the global infrastructure of national and regional biobanks to harness the potential of samples collected•Baseline immunity to emerging or endemic pathogens•Development of tests for novel pathogens•Surveillance through testing for biomarkers Refine the focus of ongoing serological studies on SARS-CoV-2 •Guidance for ongoing vaccination strategies•Research on COVID-19 immunity•Shift towards multi-pathogen serosurveillance Build an operational protocol repository •Coordinated and timely response•Designated funding for use in current (eg, outbreaks and seasonal epidemics) and future applications Strengthen the global infrastructure of national and regional biobanks to harness the potential of samples collected •Baseline immunity to emerging or endemic pathogens•Development of tests for novel pathogens•Surveillance through testing for biomarkers SAM reports grants from the Germany Ministry of Health via the Global Health Protection Programme. AA reports grants from the UK Department of Health and Social Care, Foreign, Commonwealth and Development Office, the Medical Research Council, the Wellcome Trust, the EDCTP2 programme supported by the European Union, and the Bill & Melinda Gates Foundation. RKA reports funding from the Public Health Agency of Canada through Canada's COVID-19 Immunity Task Force, the WHO Health Emergencies Programme, the Robert Koch Institute, the Canadian Medical Association, and Open Philanthropy; consulting fees from the Bill & Melinda Gates Foundation Strategic Investment Fund; and he was previously employed as a Senior Policy Advisor at Health Canada. AC reports funding from the Bill & Melinda Gates Foundation through Oxford University. EWK reports funding from the Bill & Melinda Gates Foundation and the UK Foreign, Commonwealth and Development Office. RO reports funding from the Ministry of Health, Government of Germany. SS reports funding from the Public Health Agency of Canada through Canada's COVID-19 Immunity Task Force, the WHO Health Emergencies Programme, and the Robert Koch Institute. KAS reports funding from WHO and the Robert Koch Institute and travel support from the Bill & Melinda Gates Foundation. MW reports funding from Canada's COVID-19 Immunity Task Force via the Public Health Agency of Canada, WHO, the Canadian Medical Association Joule Innovation Fund, and the Robert Koch Institute. AKZ reports funding from the Bill & Melinda Gates Foundation through Oxford University. All the other authors declare no competing interests. The findings and conclusions in this Comment are those of the authors and do not necessarily represent the views of the US Centers for Disease Control and Prevention/Agency for Toxic Substances and Disease Registry. The members of the Public Health Collaborators on Serosurveillance for Pandemic Preparedness and Response PHSeroPPR are Sophie A Müller, Ambrose Agweyu, Olusola A Akanbi, Mary A Alex-Wele, Kokou N Alinon, Rahul K Arora, Saidou Balam, Bernard Barekye, Amen Ben Hamida, Isabel Bergeri, Nicki Boddington, Lena Böff, Idesbald Boone, Andelé Conradie, Anahit Demirchyan, Sandra Dudareva, Charbel El Bcheraoui, Megan Evans, Elise Farley, Iris Hunger, Jefferson M Jones, E Wangeci Kagucia, Makobu Kimani, Hannah C Lewis, Festo Mazuguni, Solomon Mwakasungula, Jason M Mwenda, Olena Nesterova, Emmanuel Nepolo, Natasha Nghitukwa, James Nyagwange, Ruth Offergeld, Tochi J Okwor, Felix Reichert, Serine Sahakyan, Sabah Shaikh, Kaveto A Sikuvi, Sabrina Weiss, Mairead Whelan, Christian H Winter, Abdhalah K Ziraba, and Johanna Hanefeld. Robert Koch Institute, 13353 Berlin, Germany (SAM, LB, IBo, AC, SD, CEB, ME, IH, RO, FR, SW, CHW, JH); KEMRI-Wellcome Trust Research Programme, Kilifi, Kenya (AA, EWK, MK, JN); London School of Hygiene & Tropical Medicine, London, UK (AA, JH); Nigeria Centre for Disease Control and Prevention, Abuja, Nigeria (OAA, TJO); University of Port Harcourt and University of Port Harcourt Teaching Hospital, Port Harcourt, Nigeria (MAA-W); Africa Centres for Disease Control and Prevention, Addis Ababa, Ethiopia (KNA, BB, FM); SeroTracker, Centre for Health Informatics, University of Calgary, Calgary, AB, Canada (RKA, SSh, MW); University of Sciences of Techniques and Technologies of Bamako, Bamako, Mali (SB); WHO Unity Studies, WHO, Geneva, Switzerland (IBe, NB, HCL); Turpanjian College of Health Sciences, American University of Armenia, Yerevan, Armenia (AD, SSa); WHO Regional Office for Africa, Brazzaville, Republic of Congo (EF, JMM); US Centers for Disease Control and Prevention, Atlanta, GA, USA (ABH, JMJ); Ifakara Health Institute, Ifakara, Tanzania (SM); State Institution Public Health Center of the Ministry of Health of Ukraine, Kyiv, Ukraine (ON); School of Medicine, University of Namibia, Windhoek, Namibia (EN); Namibian Ministry of Health and Social Services, Windhoek, Namibia (NN, KAS, CHW); African Population and Health Research Center, Nairobi, Kenia (AKZ) Download .pdf (.06 MB) Help with pdf files Supplementary appendix