ROSES‐S: Statement from the World Health Organization on the reporting of seroepidemiologic studies for SARS‐CoV‐2

Abstract Well‐designed population‐based seroepidemiologic studies can be used to refine estimates of infection severity and transmission, and are therefore an important component of epidemic surveillance. However, the interpretation of the results of seroepidemiologic studies for SARS‐CoV‐2 has been hampered to date principally by heterogeneity in the quality of the reporting of the results of the study and a lack of standardized methods and reporting. We provide here the ROSES‐S: Reporting of Seroepidemiologic studies—SARS‐CoV‐2. This is an updated checklist of 22 items that should be included in the reporting of all SARS‐CoV‐2 seroepidemiologic studies, irrespective of study design.

infection to time of biological sampling, 4 and the severity of disease. 6 Cross-reactive antibodies with seasonal and zoonotic coronaviruses have been observed for some assays, and their prevalence may differ depending on the population tested.
Several systematic reviews have now been conducted of the initial pre-print or peer-reviewed SARS-CoV-2 seroepidemiologic studies. [7][8][9] These reviews have found overall seroprevalence to be low, although these reviews reflect seroprevalence results before August 2020. They showed variation by country and by region, with higher seropositivity reported in high-risk groups (eg, healthcare workers) and populations that have experienced widespread community transmission. Importantly, they have also highlighted heterogeneity in the quality of many of the initial seroprevalence studies, derived principally from the quality of the reporting of the results of the study, as has been shown for other diseases. 10 Many fail to report on the validation of the immunoassay used for specific application to the study, or provide sufficient information as to how the immunoassay was validated, or report on whether seroprevalence estimates were corrected for sampling biases or immunoassay performance. In the absence TA B L E 1 Checklist for the reporting of SARS-CoV-2 seroepidemiologic studies

Item number Item ROSES-I description (Horby P, 2016) ROSES-I description for SARS-CoV-2
Title, abstract and introduction 1 Title and abstract The term "seroepidemiologic," "seroepidemiology," "seroprevalence," or "seroincidence" should be applied to the study in the title or abstract, and the medical subject heading "Seroepidemiologic Studies" be used when the report is of a population-based serological survey.
The term "seroepidemiologic," "seroepidemiology," "seroprevalence," or "seroincidence" should be applied to the study in the title and abstract, and the medical subject heading "Seroepidemiologic Studies" be used when the report is of a population-based serological survey. Provide a structured summary including, as applicable: objectives; population level (ie, national, regional, local), study design, study period, eligibility criteria of study participants, sampling dates and method, sample size, laboratory methods (assay used), results: seroprevalence and 95% CI, study limitations, conclusions and implications of key findings. For each variable of interest, give sources of data and details of methods of assessment (measurement). Describe comparability of assessment methods if there is more than one group. Give information separately for cases and controls in case-control studies and, if applicable, for exposed and unexposed groups in cohort and cross-sectional studies).

Bias
If relevant, describe efforts to control for the potential effect of immunization on estimates of outcomes.
Describe any efforts to address potential sources of bias.
10 Study size Describe the baseline estimated seroprevalence at given antibody titers or incidence of infection and cite published literature to support these estimates.
Describe the baseline estimated seroprevalence or incidence of infection and cite published literature to support these estimates. Explain the steps that led to the final sample size. Report the numbers of individuals at each stage of the study-the numbers potentially eligible, examined for eligibility, confirmed eligible, included in the study, completing follow-up, and analyzed.

Quantitative variables
Describe the serological assay's limit of detection and how this limit is defined or calculated. Describe how samples with a result below or on the borderline of the limit were handled in the analysis. Describe and justify the titer or other result used to define "seropositivity," or the antibody titer change or change in other assay result used to define "seroconversion." Avoid the term "seroconversion" unless referring to change from undetectable to detectable antibody level. Otherwise report the foldrise in titer. Avoid the term "infection" but report "seroprevalence at a titer of ….". If statements or inferences are made about protection from infection, describe what is known about the correlation between the assay results and protection from infection and illness.
Explain how quantitative variables were handled in the analyses. If applicable, describe which groupings were chosen and why. Describe the serological assay's limit of detection and how this limit is defined or calculated. Describe how samples with a result below or on the borderline of the limit were handled in the analysis. Define "seropositivity," or the antibody titer change or change in other assay result used to define "seroconversion." Avoid the term "seroconversion" unless referring to change from undetectable to detectable antibody level. Avoid the term "infection" but report "seroprevalence at a titer of ….".

Statistical methods
If relevant, state how the non-independence of data was managed. If relevant, report methods used to account for the probability of seropositivity or seroconversion if infected, and to account for decay in antibody titers over time.
Describe all statistical methods, including those used to control for confounding. Describe any methods used to examine subgroups and interactions. Describe all methods used to address sampling and selection biases (eg, weighting results, multilevel regression and post-stratification). Explain how missing data were addressed. For a cohort study, explain how loss to follow-up was addressed, if applicable. For a case-control study, explain how variables on which cases and controls were matched, if applicable. For a cross-sectional study, describe analytical methods taking account of sampling strategy, if applicable. Describe any sensitivity analyses. If relevant, report methods used to account for adjustment for assay performance (sensitivity and specificity), the probability of seropositivity or seroconversion if infected, and to account for decay in antibody titers over time. . Report if antigen(s) from potentially crossreactive pathogens/strains were used in order to identify cross-reactivity, and specify which antigen was used, including virus name, subtype, strain, lineage and clade, with standardized nomenclature and reference. If red blood cells were used for a hemagglutinin inhibition assay, specify the animal species from which they were obtained and concentration (v/v) used. Describe positive and negative controls used. Describe starting and end dilutions. Specify laboratory biosafety conditions. Specify whether replication was performed, and if so, the acceptable replication parameters. Specify whether a confirmatory assay was performed and all specifics of this assay, at the same level of detail. Specify international standards used, if appropriate Wherever possible, use defined and standardized methods that have been established in more than one laboratory, and that ideally are commercially available in more than one country. Avoid laboratorylevel formulations if standardized formulations are available for the same analytical targets. Specify the testing algorithm (if more than one test used) and assay type (eg, virus neutralization/ microneutralization/surrogate neutralization; ELISA; LFIA; CLIA; other) and readout used to determine the endpoint titer. Reference a previously published protocol, if used, and any modifications of the protocol. If a previously published protocol was not used, provide full details in supplementary materials. For in-house assays, include a description of the assay format (e.g., direct or indirect immunoassay) as well as description of cutoff determination and which antibody isotype is targeted, and reference previously published validation data. State what is known about the determinants of the variability of the antibody detection assay being used. Specify the antigen(s) and antibody isotope target used, with standardized nomenclature and reference; specify whether live virus or pseudo virus was used (where applicable). Describe how the cutoff was established. If viral antigen produced in-house is used, specify sequence, expression system (bacteria or mammalian cells). Specify reactivity with other coronavirus antigens (MERS-CoV, SARS-CoV, seasonal CoVs) in the same population. Describe positive and negative controls used. Specify international standards used, if appropriate. Describe starting and end dilutions. Specify laboratory biosafety conditions. Specify whether replication was performed, and if so, the acceptable replication parameters. Specify whether a confirmatory assay was performed and all specifics of this assay, at the same level of detail.

13
Participants Report the numbers of individuals at each stage of the study-the numbers potentially eligible, examined for eligibility, confirmed eligible, included in the study, completing follow-up, and analyzed. Give reasons for non-participation at each stage. Consider use of a flow diagram.
Report the numbers of individuals at each stage of the study-the numbers potentially eligible, examined for eligibility, confirmed eligible, included in the study, completing follow-up, and analyzed. Give reasons for non-participation at each stage.
Consider use of a flow diagram.
14 Descriptive data Give characteristics of study participants (eg, demographic, clinical, social) and information on exposures and potential risk factors. Indicate the number of participants with missing data for each variable of interest. Cohort study-summarize follow-up time (eg, average and total amount).
Give characteristics of study participants (eg, demographic, clinical, social) and information on exposures and potential risk factors for all participants, not solely stratified by outcome status. Indicate the number of participants with missing data for each variable of interest. For a cohort study, detail follow-up time (eg, average and total amount).

TA B L E 1 (Continued)
(Continues) of the use of the same assay used with standardized cutoffs and confirmatory testing algorithms, these factors hamper the interpretation of the study results, as well as efforts to pool study results to understand population seroprevalence at a country, regional, or global level. Here, we provide in Table 1  . This forum allows the sharing of well-characterized panels of sera to enable standardization of serologic assays worldwide and access to high-quality antigen specifically for assays to conduct serologic surveys. Solidarity II is also developing a standardized serology assay for collaborators who wish to use a global standard assay and methodologies for laboratories around the world to develop their own serologic assays. It facilitates the sharing of laboratory protocols for serologic assays for the purposes of serology surveys and study protocols, such as the Unity studies.

Item number Item ROSES-I description (Horby P, 2016) ROSES-I description for SARS-CoV-2
15 Outcome data Cohort study-report the numbers of outcome events or summary measures over time. Case-control study-report the numbers in each exposure category, or summary measures of exposure. Cross-sectional study-report the numbers of outcome events or summary measures.
For a cohort study, report the numbers of outcome events or summary measures over time. For a case-control study, report the numbers in each exposure category, or summary measures of exposure. For a cross-sectional study, report the numbers of outcome events or summary measures.

16
Main result Report unadjusted estimates of distribution of titers by age group. Report methods to standardize the results from the study sample to the target population.
Report unadjusted estimates of distribution of seropositivity by age group. Report methods to standardize the results from the study sample to the target population.

17
Other analyses Report other analyses performed-analyses of subgroups and interactions, and sensitivity analyses.
Report other analyses performed-analyses of subgroups and interactions, and sensitivity analyses.

Key results
Summarize key results with reference to study objectives.
Summarize key results with reference to study objectives.

19
Limitations Discuss limitations and strengths of the study. Discuss limitations and strengths of the study.

20
Interpretation Discuss the interpretation of the results in the context of known or potential cross-reactivity.
Discuss the interpretation of the results in the context of known or potential cross-reactivity, assay performance and other sources of bias. Understanding population seroprevalence over time is important for informing public health decisions made by health authorities and policy makers. Conducting and reporting studies that are aligned with this ROSES-S checklist will allow for more refined epidemic modeling, outbreak responses, and public health and social measures, as well as more complete secondary data analyses.

CO N FLI C T O F I NTE R E S T
The authors have no conflict of interest to declare.

PATI E NT CO N S E NT S TATE M E NT
Patient consent was not applicable to this article as no patients were involved in the current study.

PE R M I SS I O N TO R E PRO D U CE M ATE R I A L FRO M OTH E R S O U RCE S
Permission to reproduce material from other sources is not applicable to this article.

E TH I C S S TATEM ENT
Ethics approval was not applicable to this article.

PE E R R E V I E W
The peer review history for this article is available at https://publo ns.com/publo n/10.1111/irv.12870.

DATA AVA I L A B I L I T Y S TAT E M E N T
Data sharing is not applicable to this article as no datasets were generated or analyzed during the current study.