key: cord-0317721-9z3baroq
authors: Fogh, K.; Strange, J. E.; Scharff, B. F.; Eriksen, A. R.; Hasselbalch, R. B.; Bundgaard, H.; Nielsen, S. D.; Joergensen, C. S.; Erikstrup, C.; Norsk, J.; Nielsen, P. B.; Kristensen, J. H.; Oestergaard, L.; Ellermann-Eriksen, S.; Andersen, B.; Nielsen, H.; Johansen, I. S.; Wiese, L.; Simonsen, L.; Fischer, T. K.; Folke, F.; Lippert, F.; Ostrowski, S. R.; Benfield, T.; Moelbak, K.; Ethelberg, S.; Koch, A.; Sonksen, U. W.; Vangsted, A.-M.; Krause, T. G.; Formsgaard, A.; Ullum, H.; Skov, R.; Iversen, K.
title: Testing Denmark: A Danish nationwide surveillance study of COVID-19
date: 2021-08-13
journal: nan
DOI: 10.1101/2021.08.10.21261777
sha: 1db6a556e770cac2842abf0eda7ef98a5c75b583
doc_id: 317721
cord_uid: 9z3baroq

Background National data on the spread of SARS-CoV-2 infection and knowledge on associated risk factors are important for understanding the course of the pandemic. Testing Denmark is a national large-scale epidemiological surveillance study of SARS-CoV-2 in the Danish population. Methods Between September and October 2020, approximately 1.3 million of 5.8 million Danish citizens (age > 15 years) were randomly invited to fill in an electronic questionnaire covering COVID-19 exposures and symptoms. The prevalence of SARS-CoV-2 antibodies was determined by Point-of Care rapid Test (POCT) distributed to participants home addresses. Findings In total 318,552 participants (24.5% invitees) completed the questionnaire and provided the result of the POCT. Of these, 2,519 (0.79%) were seropositive (median age 55 years) and women were more often seropositive than men, interquartile range (IQR) 42-64, 40.2% males. Of participants with a prior positive Polymerase Chain Reaction (PCR) test (n=1,828), 29.1% were seropositive in the POCT. Seropositivity increased with age irrespective of sex. Elderly participants (>61 years) reported less symptoms and had less frequently been tested for SARS-CoV-2 compared to younger participants. Seropositivity was associated with physical contact with SARS-CoV-2 infected individuals (Risk ratio (RR) 7.43, 95% CI: 6.57-8.41) and in particular household members (RR 17.70, 95% CI: 15.60-20.10). Home care workers had a higher risk of seropositivity (RR 2.09 (95% CI: 1.58-2.78) as compared to office workers. Geographic population density was not associated to seropositivity. A high degree of compliance with national preventive recommendations was reported (e.g., > 80% use of face masks), but no difference was found between seropositive and seronegative participants. Interpretation This study provides insight into the immunity of the Danish population seven to eight months after the first COVID-19 case in Denmark. The seroprevalence was lower than expected probably due to a low sensitivity of the POCT used or due to challenges relating to the reading of test results. Occupation or exposure in local communities were major routes of infection. As elderly participants were more often seropositive despite fewer symptoms and less PCR tests performed, more emphasis should be placed on testing this age group.

National seroprevalence data on antibodies to SARS-CoV-2 can guide national health policies in 32 understanding transmission routes and thereby improve the management of potential new outbreaks 33 during the COVID-19 pandemic (1) (2) (3) (4) . However, a large sample size is required to describe the spread of 34 infection, risk factors, and severity of the infection across geography and demography (5) . 35 Denmark has 5.8 million inhabitants (6) and as of July 5, 2021, there have been more than 295,654 (5 %) 36 confirmed cases of SARS-CoV-2 infection and more than 2,537 COVID-19 related deaths in Denmark (7) . The 37 first confirmed case of SARS-CoV-2 infection in Denmark was reported on February 27, 2020 (8) . In 38 Denmark, the epidemic has been characterized by two infection waves; spring 2020 and autumn-winter 39 2020/2021, similar to several other European countries (9) . Two lockdowns were imposed by the 40 government, the first between March 11th to April 15th, 2020 and the second December 17th, 2020 to 41 February 8th, 2021 (10). Testing for SARS-CoV-2 in Denmark using Polymerase Chain Reaction (PCR) was 42 established in March 2020 and has been upscaled during the pandemic. From March 12 to April 21, 2020 43 individuals with moderate to severe symptoms of respiratory tract infection were offered testing. From 44 April 21, 2020 testing was available for individuals with mild symptoms and asymptomatic contacts, and 45 since May 18, 2020, nationwide high-intensity, free of charge testing for SARS-CoV-2 infection has been 46 performed using PCR (11) . Vaccination against COVID-19 began on December 27 th , 2020 with residents and 47 employees at nursing homes and frontline staff at hospitals (12) . 48

The rates of COVID-19-related morbidity and mortality have been low in Denmark compared to other 49 European countries (13) . Nevertheless, considering the unknown proportion of asymptomatic or mildly 50 symptomatic SARS-CoV-2 infected persons who have not been PCR-tested (viral throat-and 51 nasopharyngeal swab), the population exposure to infection might be higher than reported according to 52 PCR test findings (1) . The seroprevalence has been reported for different groups in Denmark; blood donors 53 (14) , medical students (15) , health care workers (16) , a smaller national random selection of the 54 population (10), homeless persons and sex workers (17) and persons from social housing areas (18) , but 55 hitherto no national investigation of this scale has been performed in Denmark. 56 "Testing Denmark" was a nationwide surveillance study of SARS-CoV-2 infection in the Danish population, 57 launched in September 2020. The study was divided in 2 phases; phase 1 (the general population) and 58 phase 2 (subgroups). In this article, we describe the process and results of phase 1. Results from phase 2 59 have been described elsewhere (17, 18) . 60 . CC-BY-ND 4.0 International license It is made available under a perpetuity.

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The copyright holder for this this version posted August 13, 2021. ;  https://doi.org/10.1101/2021.08.10.21261777 doi: medRxiv preprint combined test sensitivity (either IgG or IgM positive) of 90.6% (95% CI: 86.6% -93.4%) and a combined 90 specificity (neither IgG nor IgM is positive) of 99.2% (95% CI: 97.6% -99.7%) (21) . An in-house validation 91 (cases=150 individuals, controls=600 individuals) showed sensitivity of 93.3% and 92.7% and specificity of 92 98.2% and 97.5% for each of the two batches respectively (see appendix Table 4 ). The case panel samples 93 were obtained from convalescent individuals within 2 months of disease onset. Sensitivity and specificity by 94 self-use has not previously been studied. 95

The POCT was sent out with a small container of isotonic saline, capillary tubes, and fingerprickers. 96

Participants were instructed by the use of the capillary tubes to add blood by fingerprick and isotonic saline 97 to each of the two test cassettes (IgG and IgM 

The primary outcome of interest was to explore the association between SARS-CoV-2 infection, defined as a 106 positive SARS-CoV-2 antibody self-test result (IgG and/or IgM), and putative risk factors for seropositivity. 107

The proportion of the study population with a positive antibody test for SARS-CoV-2 (as a proxy for 108 previous infection) was a secondary outcome of interest. 109 110

This study was performed as a national surveillance study under the authority task of the national 112 infectious disease control institute Statens Serum Institut (SSI), Copenhagen, Denmark. According to Danish 113 law national surveillance activities from SSI do not require any individual approval from an ethics 114 committee. The study was performed in agreement with the Helsinki II declaration and registered with the 115 Danish Data Protection Authorities (P-2020-901). Participation was voluntary and all data were self-116 reported. All personal data obtained in Enalyzer was kept in accordance with the general data protection 117 regulation and data protection law stated by the Danish Data Protection Agency. Invitees received 118 information about their legal rights and the use of their data in the invitation letter. 119 . CC-BY-ND 4.0 International license It is made available under a perpetuity.

is the author/funder, who has granted medRxiv a license to display the preprint in (which was not certified by peer review) preprint is the author/funder, who has granted medRxiv a license to display the preprint in (which was not certified by peer review) preprint Women were more likely to be seropositive (Table 1 Table 3 . Notably, time between positive PCR and POCT was lower for seropositive than 168 seronegative participants. 169

Supplementary figure 8 and 9 shows geographical variations between municipalities in seropositivity and 170 variations in population density. When ordering municipalities according to population density, no clear 171 association between seropositivity and population density was found. 172

Protective effect of authority recommendations 174

Most participants followed multiple recommended public health measures to prevent infection, e.g. >80% 175

reported use of face masks. However, when examining serostatus according to behavior, no difference in 176 serostatus was found between individual protective health measures, e.g. 82.5% of seronegative and 84% 177 of seropositive reported use of face masks. (Figure 2) . 178

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The copyright holder for this this version posted August 13, 2021. ; https://doi.org/10.1101/2021.08.10.21261777 doi: medRxiv preprint Participants who had physical contact or lived in a household with a SARS-CoV-2 infected person had the 180 highest risk of being seropositive compared to participants who reported not to have been exposed to a 181 SARS-CoV-2 infected person; RR of 7.43 (95% CI: 6.57 to 8.41) and 17.70 (95% CI: 15.60 to 20.10), 182 respectively ( Figure 3 ). Among participants exposed to a SARS-CoV-2 infected person within the household, 183 the proportion of seropositive participants was higher in smaller household sizes (see Supplementary figure  184 10). However, when adjusting for sex, age, and household size, there was no significant increased risk for 185 lower household size and risk of seropositivity (Table 2) . 186

Occupation 187

Among professionals (full-time, part-time, and self-employed), working in the healthcare sector or with 188 home care was associated with a higher risk of seropositivity compared to office work; healthcare sector: 189 RR 2.02 (95%CI: 1.75 to 2.33), home care: RR 2.09 (95%CI: 1.58 to 2.78), see Figure 4 . findings can be summarized as follows; females were found to have a higher seroprevalence than males. 202

Elderly participants were more often seropositive despite fewer symptoms and less often PCR tests. The 203 geographical variation in seroprevalence was limited and did not seem to be related to population density. 204

A prevalence of SARS-CoV-2 antibodies of only 0.79% was reported. Only 29% of PCR positive were POCT 205 seropositive in our study. The study showed a high degree of adherence with national recommendation but 206 there was no clear difference in reported compliance between seropositive and seronegative participants 207 . CC-BY-ND 4.0 International license It is made available under a perpetuity.

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The copyright holder for this this version posted August 13, 2021. ; https://doi.org/10.1101/2021.08.10.21261777 doi: medRxiv preprint in the study period which covered the interval between the first infectious wave in spring 2020 and the 208 second in autumn/winter. 209

Until October 2020, 2.4 million people in Denmark had been tested with PCR at least once and up to 211 multiple times, and 27,998 people were confirmed PCR positive (0.5% of the total population) (24). A 212 population-based study in Denmark with 7,015 participants from August 2020 found a seroprevalence of 213 2.0% (age > 12 years) measured by Wantai SARS-CoV-2 Ab ELISA (10), the point estimates tended to be 214 higher in the age group 18-39 years and lower in the age group >65 years, with no difference observed by 215 sex. Also, a convenience sample of blood donors tested in October 2020 with ELISA found a seroprevalence 216 of 2.1% (adults aged 18-70) (25) . In contrast, we found a seroprevalence of only 0.79%, higher proportions 217 of seropositivity in younger age groups and females being seropositive more often. 218

A Danish study of household transmission, with individual level register data on all national PCR test for 219 SARS-CoV-2 for the period February-July 2020, suggested that susceptibility to infection increases with the 220 age of the susceptible person (26) . Other international studies tends to show trends in line with our results 221 with an increase in seropositivity with age (9) and females having increased IgG positivity (27) . By sending 222 our test material to participants at home, we may have been able to include vulnerable and elderly 223 susceptible to infection who otherwise would not have had the opportunity to participate. This is 224 supported by our findings that participation in POCT was high in all age groups except the younger age 225 group. This could partially explain the difference in seroprevalence between our study and aforementioned 226

Danish studies, which included healthy blood donors as well as a population that should attend a venous 227 blood sample. 228

In Denmark, one of the measures to contain the epidemic has been to offer easy-access, free of charge 230 testing. The Danish Health authorities have encouraged the population to have test performed in case of 231 symptoms of COVID-19 or after close contact with infected persons. Elderly participants reported fewer 232 previous tests. When compared to younger participants, elderly participants might have fewer social 233 contacts and/or could have isolated themselves to a higher degree thus avoiding potential close contact 234 with infected persons. Further, younger participants may be more exposed to infection by having more 235 social contacts or via their employment. However, in a recent report by the HOPE project (How 236

Democracies Cope with COVID19), elderly people in Denmark were not found to report higher levels of self-237 . CC-BY-ND 4.0 International license It is made available under a perpetuity.

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The copyright holder for this this version posted August 13, 2021. ; https://doi.org/10.1101/2021.08.10.21261777 doi: medRxiv preprint quarantine when experiencing symptoms or when testing positive by PCR compared to younger people 238 (28). 239

The strongest correlation to seropositivity was ageusia and anosmia (loss of taste and smell), consistent 240 with previous findings (15, 16, 18) . In general, we found that seropositive participants more frequently 241 recalled having had symptoms when compared to seronegative participants. 242

When stratifying for age groups, elderly participants reported symptoms less frequently. It may be that only 243 the healthiest elderly participated, however, this outcome could also be a bias resulting from comorbidity 244 disorders and long recall period. Our results are surprising because aging itself has been associated with 245 more severe COVID-19 symptoms due to increased comorbidities with age and more aggressive clinical 246 behavior (29) . Nevertheless, the level of antibodies (comparable levels of IgG and IgM) was highest among 247 elderly participants although they reported fewer symptoms and had fewer tests. As such, elderly 248 participants may more often be subject to asymptomatic infections, thereby constituting an important 249 subgroup that may warrant further attention. However, it should also be noted that individuals in the 250 working age who were unable to work from home may attend PCR testing more often than people who 251 have retired, and this could contribute to our observations. 252

Occupation 253

As previously reported, working in the health care sector was associated with a higher risk of seropositivity 254 (16, 30) . Working in home care or at nursing homes also increased the risk. These occupations often 255 involves working with patients and being in close physical contact to other persons, thus increasing the risk 256 of infection (30) . The proportion of females working in the health care sector is typically higher than males 257 (31), possibly explaining the higher proportion of seropositive females. Conversely, those who have office 258 jobs, and therefor possibly better opportunities to work from home, have been at less risk of infection 259 during the first infectious surge. 260

We observed a high proportion of participants following the authority's recommendations to reduce the 262 risk of SARS-CoV-2 infection. Remarkably, seropositive participants were slightly more compliant with these 263 recommendations compared to seronegative participants on almost all the preventive measures. However, 264 participants who are more attentive to recommendations, e.g. health care professionals are more exposed 265 to SARS-CoV-2 infection. As such, the effect of the authority's recommendations could be underestimated. is the author/funder, who has granted medRxiv a license to display the preprint in (which was not certified by peer review) preprint

The copyright holder for this this version posted August 13, 2021. The low seroprevalence at 0.79% in our study may be due to low sensitivity of the POCT used or due to 296 challenges relating to the reading of the test results, since 2.9% were inconclusive. POCT in general have a 297 lower diagnostic performance compared to laboratory testing (35) . Test results also depend on the 298 prevalence of infection in the population which will be low when screening asymptomatic and higher for 299 those with suggestive symptoms. In low prevalence settings, true positive test results are uncommon. As 300 . CC-BY-ND 4.0 International license It is made available under a perpetuity.

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The copyright holder for this this version posted August 13, 2021. ; https://doi.org/10.1101/2021.08.10.21261777 doi: medRxiv preprint such, the predictive value of a positive test will be lower in individuals with a low background risk of 301 infection (36) . Only 0.5% of the Danish population were confirmed PCR positive during the study period. 302

The diagnostic testing window is also of importance as the study was performed seven to eight months 303 after the first COVID-19 case in Denmark. The antibody response of IgM and IgG is found to be highest 304 about 2-3 weeks and 3-4 weeks, respectively after symptom onset and decrease afterwards (35) . 37% of 305 our study participants had a positive POCT 20-30 days after a positive PCR. In addition, we found that for 306 seronegative, longer time had passed from a previously positive PCR test than for seropositive. As 307 participants performed the POCT at home, incorrect testing procedure or misinterpreted POCT results 308 could lead to false negative POCT results. Importantly, inconclusive tests were treated as negative in our 309 study, and weak lines suggesting a positive test result, could be misinterpreted as a negative test result. In 310 other Danish studies, the tests (POCT and ELISA) have been performed and read or analyzed by professional 311 staff which increases the performance of the test. Consequently, the seroprevalence is likely 312 underestimated in our study. However, seropositivity was low among participants who did not have a 313 previous positive PCR test, indicating a high specificity of the POCT, thus the associations found are reliable. 314

Perspectives 315

To date, this is the largest population-based Danish study where test material has been sent to participants 316 and performed at home with broad national participation. Nationwide information can be difficult to 317 gather and the study design in question presents a novel way for conducting future studies. Additionally, 318 this setup can be used as a model for ongoing monitoring of COVID-19 immunity in the population, both 319 from past infection and from vaccination against SARS-CoV-2. 320 321

This study provides insight into the immunity of the Danish population seven to eight months after the first 323 COVID-19 case in Denmark. The seroprevalence was lower than expected probably due to low sensitivity of 324 the POCT used or due to challenges relating to the reading of test results. Future studies could be improved 325 with an easier POCT test to perform and a shorter questionnaire. A high degree of compliance with national 326 preventive recommendations was seen, but no clinically significant protective effect was identified. is the author/funder, who has granted medRxiv a license to display the preprint in (which was not certified by peer review) preprint is the author/funder, who has granted medRxiv a license to display the preprint in (which was not certified by peer review) preprint is the author/funder, who has granted medRxiv a license to display the preprint in (which was not certified by peer review) preprint is the author/funder, who has granted medRxiv a license to display the preprint in (which was not certified by peer review) preprint

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The copyright holder for this this version posted August 13, 2021. ; https://doi.org/10.1101/2021.08.10.21261777 doi: medRxiv preprint : Risk ratio for seropositivity in a subset of 32,812 participants exposed to COVID-19 infected persons in various settings. For each setting, participants exposed to COVID-19 infected persons was compared to participants not exposed in this setting (reference group). is the author/funder, who has granted medRxiv a license to display the preprint in (which was not certified by peer review) preprint

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The copyright holder for this this version posted August 13, 2021. ; https://doi.org/10.1101/2021.08.10.21261777 doi: medRxiv preprint Figure 3 : Risk ratio for seropositivity in a subset of 32,812 participants exposed to COVID-19 infected persons in various settings. For each setting, participants exposed to COVID-19 infected persons was compared to participants not exposed in this setting (reference group).

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The copyright holder for this this version posted August 13, 2021. ; https://doi.org/10.1101/2021.08.10.21261777 doi: medRxiv preprint Supplementary figure 2: Distribution of SARS-CoV-2 antibodies according to age groups. Numbers above bars represent percentage of total number of participants in groups.

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The copyright holder for this this version posted August 13, 2021. ; https://doi.org/10.1101/2021.08.10.21261777 doi: medRxiv preprint Supplementary figure 4: SARS-CoV-2 seropositive % according to smoking habits, weekly alcohol consumption, and BMI stratified for sex. Red bar represents females, blue bar represents males. Numbers above bars represent number of participants in each group.

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The copyright holder for this this version posted August 13, 2021. ; https://doi.org/10.1101/2021.08.10.21261777 doi: medRxiv preprint Supplementary figure 9: Scatterplot of seropositive % according to population density for all municipalities. Each x-axis tick represents a municipality with the corresponding population density. Dots, triangles, squares, and crosses represent population density quartiles from lowest to highest quartile, respectively.

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The copyright holder for this this version posted August 13, 2021. ; https://doi.org/10.1101/2021.08.10.21261777 doi: medRxiv preprint Supplementary figure 10: SARS-CoV-2 seropositive % in households with a COVID-19 infected person stratified by household size. Numbers above bars represent number of seropositive and seronegative participants in each household size.

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The copyright holder for this this version posted August 13, 2021. ; https://doi.org/10.1101/2021.08.10.21261777 doi: medRxiv preprint Supplementary figure 11: Proportion of persons who experienced symptoms stratified for age groups. Numbers next to bars represent percentages.

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The copyright holder for this this version posted August 13, 2021. ; https://doi.org/10.1101/2021.08.10.21261777 doi: medRxiv preprint Supplementary figure 12: Number of previous tests for 318,552 participants stratified for age groups and sex.

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The questionnaire:

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Supplementary table 1: Sex and age group distribution and place of living for responders and nonresponders among population invited to participate in the questionnaire. Missing data represents invited persons who requested to be removed. Also shown are sex and age group distribution and place of living for participants who provided POCT results versus participants who did not provide the POCT results.