Seropositivity of borrelia burgdorferi s. L. In germany—an analysis across four german national cohort (nako) study sites

ABSTRACT Lyme borreliosis (LB) is caused by the transmission of _Borrelia burgdorferi_ s.l. from ticks to humans. Climate affects tick abundance, and climate change is projected to promote

shifts in abundance in Europe, potentially increasing human exposure. We analyzed serum samples collected between the years 2014–2019 from German National Cohort (NAKO) participants at four

study sites (Augsburg, Berlin, Hanover, Münster) for immunoglobulin G (IgG) and immunoglobulin M (IgM) antibodies using an enzyme‐linked immunosorbent assay (ELISA) and line blot immunoassay

as confirmatory test for positive and equivocal ELISA samples. We reported crude and weighted seropositivity proportions for local estimates. We used mixed model analysis to investigate

associated factors, such as age, sex, migration background, or animal contacts. We determined the serostatus of 14,207 participants. The weighted seropositivity proportions were 3.4% (IgG)

and 0.4% (IgM) in Augsburg, 4.1% (IgG) and 0.6% (IgM) in northern Berlin, 3.0% (IgG) and 0.9% (IgM) in Hanover, and 2.7% (IgG) and 0.6% (IgM) in Münster. We found higher odds for IgG

seropositivity with advancing age (_p_ < 0.001), among males compared to females (_p_ < 0.001) and reduced odds among participants with migration background compared to those without

(_p_ = 0.001). We did not find evidence for an association between serostatus and depression, children within the household, or animal contact, respectively. We found low seropositivity

proportions and indications of differences across the study locations, although between-group comparisons did not yield significant results. Comparisons to earlier research are subject to

important limitations; however, our results indicate no major increases in seropositivity over time. Nevertheless, monitoring of seropositivity remains critical in light of potential

climate-related _Borrelia_ exposure. SIMILAR CONTENT BEING VIEWED BY OTHERS DETECTION OF _BORRELIA BURGDORFERI_ ANTIGENS IN TISSUES AND PLASMA DURING EARLY INFECTION IN A MOUSE MODEL Article

Open access 30 August 2021 TICK-BORNE ENCEPHALITIS VIRUS SEROPREVALENCE AND INFECTION INCIDENCE IN SWITZERLAND, 2020–2021 Article Open access 11 March 2025 CORRELATION BETWEEN COVID-19

SEVERITY AND PREVIOUS EXPOSURE OF PATIENTS TO _BORRELIA_ SPP. Article Open access 24 September 2022 INTRODUCTION In Europe, Lyme borreliosis (LB) is the most frequent tick-borne disease

caused by _Borrelia burgdorferi_ sensu lato (_B. burgdorferi_ s.l.). Climatic factors affect the geographical spread of _Ixodes ricinus (I. ricinus)_, the primary vector of _B. burgdorferi_

s.l. in Europe1. Due to climate change-related temperature increases and humidity alterations, _I. ricinus_ expanded its territory while also showing prolonged seasonal activity2, implying

an increased potential risk for human exposure to ticks. Especially in central and northern Europe, reported LB cases have increased within the past two decades3. However, LB is a notifiable

disease in selected, but not all European countries4. In Germany, LB is partially notifiable in nine of sixteen federal states; notification data from these states indicate a varying but

steady incidence by region for the years 2013–2017, ranging from 26 to 41 cases per 100,000 persons5, while nation-wide health insurance data from 2019 indicated an incidence of 179 cases of

LB per 100,000 insured persons in Germany6. Two recent local serological surveys conducted in Hanover, Northern Germany (2014–2018)7, and in Bonn in Western Germany (2018–2020)8,

respectively, found no increases in seropositivity proportions compared to earlier investigations (1997–1999 and 2008–2011, respectively)9, despite increases in tick density in at least one

German region (Siebengebirge near Bonn). The data for Hanover is included in this work with a different research focus. Our work aims (1) to estimate the local seropositivity proportion of

antibodies against _B. burgdorferi_ s.l. among the general population of four different regions in Germany based on a nation-wide population-based cohort study (Augsburg in southern, Berlin

North in Eastern-, Hanover in Northern-, and Münster in Western Germany) with—for the first time—high accuracy due to large sample size; (2) to compare seropositivity using identical age-

and sex population weights; and (3) to investigate risk factors for seropositivity across regions. The data create a base for future comparisons regarding potentially increasing human _B.

burgdorferi_ s.l. exposure and enable investigations of seroconversion and –reversion within a large and ongoing cohort. METHODS The German National Cohort (NAKO) is a prospective

population-based cohort study with 205,415 baseline participants examined across 18 study sites10. All potential NAKO-participants were randomly drawn from population registries. Subjects

were eligible for participation when aged between 20 and 69 years at sampling date, provided written informed consent, had their primary residence within a regionally limited catchment area

corresponding to the responsible NAKO study site, and were of sufficient health for study participation on site. Participants aged 40 years and above were oversampled. Detailed information

is provided by Peters et al.10. All participants provided written informed consent. In our investigation, we randomly selected baseline serological samples from the urbanized sites Augsburg,

Berlin North, Münster, and used all eligible samples from Hanover. The Hanover data were reported before7 with a different research focus. We performed stratified random sampling for the

three other study sites after restricting to those with: available data for risk factor evaluation (if possible), focusing on a target distribution of 50% males and a distribution of age

groups corresponding to the original NAKO recruitment, i.e., an oversampling of the age groups ≥ 40 years. A laboratory (DIN EN ISO accredited, ISO 9001 certified) screened all samples for

immunoglobulin G (IgG) and immunoglobulin M (IgM) _B. burgdorferi_ s.l. antibodies using an enzyme‐linked immunosorbent assay (ELISA). Positive and equivocal ELISA samples underwent line

blot immunoassay for confirmation (test kit information: Table S1). In the primary analysis, we considered a sample with positive or equivocal ELISA and positive line blot result as a

seropositive (classification according to the microbiologic-infectiologic quality standard MIQ12). For the secondary analysis to allow comparability with two previous studies, we considered

a positive ELISA sample with subsequent positive or equivocal line blot or an equivocal ELISA with a positive line blot as positive 9. We classified each sample for IgG and IgM serostatus

based on these two schemes. To estimate general population seropositivity, we weighted our sample with the respective local age and sex distribution based on the 2020 update of the 2011

census (www.destatis.de). For comparison with earlier estimates, we additionally weighted by the age- and sex distributions of the underlying study populations of the German National Health

Interview and Examination Survey 1998 (BGS98, 1997–1999) and the German Health Interview and Examination Survey for Adults (DEGS, 2008–2011)9. Due to low total number of IgM-positive

samples, we restricted further analyses to IgG antibodies. We used the χ2-test for trend in proportions to investigate a potential seropositivity trend with age, and with increasing

education level. Then, we used the χ2-test (two-sided) to test for differences in German standard-population-weighted (2020 update of the 2011 census) seropositivity proportions between the

study sites, and used post-hoc pairwise comparisons between the individual centers using the Fisher’s exact test (two-sided) with Bonferroni correction. To evaluate potential risk factors

for seropositivity, we used logistic mixed model analysis, with study centers as the clusters. We constructed models to estimate odds ratios (OR) for IgG seropositivity; in model 1, as a

function of sex, age, education level, migration background, depression (score ≥ 10 of the 9-question Patient Health Questionnaire, PHQ-9), children within the household; in model 2, as a

function of all variables from model 1 and additionally animal-related variables (having a particular pet vs. no pet) due to their restricted availability by NAKO design. We controlled for

education level and migration background in our models to add additional evidence to recent conflicting findings concerning the role of socioeconomic factors concerning seropositivity7, 8.

Due to the indication of a potential association of seropositivity with depressive symptomatology 7, we also added depression as control variable to obtain further insight. To provide

insights into potentially altered tick exposure with children living in the same household, e.g., by altered outdoor activities8, we added this variable to our models as control variable. We

considered a significance level of 5% to determine statistical significance. All analysis and visualization was conducted in R version 4.1.2. We used the package “survey” to apply weights,

“gtsummary” to support table creation, “ggplot” for visualization, and the glmer()-function from “lme4” to fit the mixed model. Finally, we used the “DHARMa”-package for further inspection

of the model, e.g., residual analysis. ETHICS APPROVAL The Bavarian Medical Association (“Bayerische Landesärztekammer”) approved all NAKO-related human examinations as the central ethics

committee [13023, 13031]. Local medical associations additionally approved the examinations. Our study respects all national laws and the 1975 Declaration of Helsinki in the current version.

RESULTS Blood samples of 14,207 participants were available for our analysis. The participants were aged 20–74 years, with a median age of 50; 50.0% were male, 55.6% reported high education

according to ISCED97, and 18.0% had a migration background. The overall crude IgG-seropositivity proportion was 3.4%. Generally, we found an increasing trend concerning crude seropositivity

with advancing age (_p_ < 0.001); however, differences were only significant when comparing the older age group 60–69 (5.2%; 95% confidence interval (CI) 4.5–5.9%) to the younger age

group 20–29 (2.6%; 95%-CI 1.8–3.5%) (Table 1). Overall, males had higher seropositivity (4.8%; 95%-CI 4.3–5.3%) than females (2.0%; 95%-CI 1.6–2.3%). Seropositivity increased with education:

1.3% (95%-CI 0.0–2.2%) in the lowest group and 3.9% (95%-CI 3.4–4.3) in the highest education group across all sites (p < 0.001). Participants without a migration background had higher

seropositivity (3.7%; 95%-CI 3.4–4.0%) than those with a migration background (2.0%; 95%-CI 1.5—2.6). We did not observe differences in seropositivity between participants with depression

(3.0%; 95%-CI 2.2–3.8%) or without depression (3.5%; 95%-CI 3.1–3.8%) and between participants with pets (dogs: 2.3%; 95%-CI 0.8–3.8%) compared to those without pets (3.9%; 95%-CI 3.1–4.8%).

Local population-weighted point seropositivity varied by location (Fig. 1, Table S2). Participants from Berlin had the highest weighted IgG seropositivity proportion (4.1%, 95%-CI

3.0–5.2%), while those from Münster had the lowest weighted proportion (2.7%, 95%-CI 2.1–3.4). The CI of seropositivity proportions overlapped between the four sites. However, the χ2-test

indicated overall differences in proportions for estimates weighted by nation-wide age and sex population proportions from 2020 (_p_ = 0.04). The pairwise comparisons with Fisher's

exact test did not yield significant results at the 95% significance level. Table S3 reports weighted seropositivity using the age- and sex distribution of earlier studies9. From logistic

mixed-model analysis, we found that every 10-year increase in age was associated with 1.26-fold (95%-CI 1.16–1.38) the odds for IgG-seropositivity (Table 2). Men had 2.54 times (95%-CI

2.05–3.13) the odds of being IgG-seropositive compared to females. Participants with a migration background had 0.56 (95%-CI 0.41–0.78) times the odds for a positive IgG-serostatus compared

to participants with no migration background. We did not find evidence for an association of IgG serostatus with education level, depression on a binary scale (PHQ-9), children within the

household (any versus none), or any current or previous animal contacts, respectively. DISCUSSION We conducted the largest-ever German multi-center serological survey for _B. burgdorferi_

s.l. in Germany. We compared seropositivity estimates of four German regions representing the four cardinal directions. The crude proportion of seropositive participants slightly varied by

study location. We estimated the local seropositivity to lie between 4.1% in Berlin (95%-CI 3.0–5.2%) and 2.7% in Münster (95%-CI 2.1–3.4). The comparison of our findings to earlier studies

is subject to critical limitations due to differences in the sampling methodology. We could not account for factors such as the degree of rurality or other living conditions. However, when

classifying our samples like in9 and weighting them by age and sex for comparability to two earlier studies9 based on BGS98 and DEGS, we did not find any indication for relevant increases in

seropositivity. Seropositivity in Augsburg was lower in our study when compared to BGS98 (6.1%, 95%-CI 5.1–7.0% vs. 10.4%, 95%-CI 7.5–13.4%) and DEGS estimates (6.5%, 95%-CI 5.5–7.4% vs.

12.1, 95%-CI 8.8–15.4%) for Bavaria. Seropositivity for Hanover was comparable with Lower-Saxony estimates in BGS98 (4.9%, 95%-CI 4.5–5.4% vs. 7.4%, 95%-CI 5.1–9.6%), but lower when compared

to DEGS (5.3%, 95%-CI 4.8–5.8% vs. 9.1%, 95%-CI 6.7–11.4%). For northern Berlin, seropositivity was comparable to BGS98 jointly reported estimates for Brandenburg, Mecklenburg-Vorpommern,

and Saxony-Anhalt (5.0%, 95%-CI 3.8–6.3% vs. 7.2%, 95%-CI 5.8–8.7%). Similarly, seropositivity was comparable when comparing northern Berlin seropositivity estimates to DEGS estimates (5.6%,

95%-CI 4.3–6.9% vs. 9.3%, 95%-CI 6.8–11.9). When considering the seropositivity proportions for Münster, we found a similar seropositivity proportion compared to earlier BGS98-estimates for

North Rhine-Westphalia (5.2%, 95%-CI 4.3–6.1% vs. 7.4%, 95%-CI 5.1–9.6). However, seropositivity was lower than DEGS estimates (5.5%, 95%-CI 4.5–6.4 vs. 9.1%, 95%-CI 6.7–11.4). All four

study sites recruited participants from predominantly urban areas, which may have resulted in reduced seropositivity proportion compared to earlier investigations, which included a higher

proportion of rural participants. Within DEGS, participants living in municipalities with less than 5000 inhabitants had twice the chance for being seropositive compared with those with more

than 100,000 inhabitants11, potentially due to higher exposure to green-space areas and, therefore, ticks. Notification data from Bavaria and Berlin supports this by showing that, compared

to the surrounding region, Berlin and Augsburg had lower incidences5. Our results confirm advancing age and male sex as risk factors for positive antibody detection. As found in earlier

studies, adults with a migration background were less likely to be seropositive11, 12. We did not find conclusive evidence for an association between educational level, current depression

(PHQ-9 score ≥ 10), or previous or current animal contact with serostatus, respectively. Our results from multivariable modelling concerning educational level are in line with previous

studies, which also found no association between socio-economic status and serostatus9, but opposes recent findings from a population-based cohort in central Bonn, in which highly educated

individuals had higher chances for positive serostatus compared to individuals with medium-level education8. The conflicting findings might be explainable by the availability or use of

different outdoor spare time activities in different urban regions. Additional investigations including higher proportions of participants with lower and intermediate education are required

to complement this discussion. In contrast to a previous study using the original PHQ-9-scores as a proxy for depression diagnosis7, we did not find evidence for an association between

serostatus and depression on a binary scale. Our findings did not support an association between animal contacts and seropositivity, which is in line with earlier findings among adults11,

but contrasts a previous finding12, which found higher chances for seropositivity among children living in households with any pet vs. no pet or with a cat vs. no cat, respectively. Our work

has several limitations. Most samples considered in our regression analysis originate from the study center in Hanover. Hence, our analysis is predominantly driven by this single-site data.

Furthermore, the use of test kits with differing specificity, sensitivity, and considered _Borrelia_ strains between the studies hamper the comparability of seropositivity proportions of

our study with previous analyses. A long-term cohort like NAKO can overcome this in the future by providing the basis for a harmonized longitudinal seropositivity analysis. The small number

of seropositive individuals in the low education group and the groups of individuals with animals in the household may have resulted in low statistical power and, thus, the inability to

identify a potential association in the regression models. In conclusion, we found low seropositivity across four study locations across Germany, with minor indications of differences

between sites. Our seropositivity estimates of the years 2014–2019 for four predominantly urban regions correspond to previous estimates for 1997–1999 and 2008–2011, respectively, indicating

no considerable increases of seropositivity over time. However, comparisons to earlier estimates suffer from limitations. Even in urbanized regions, potential climate-change-related shifts

in tick exposure may increase infections and, therefore, non-urgent follow-up may be conducted in future waves of the NAKO cohort study. Our findings underpin previously suggested risk

factors for seropositivity, with advancing age and male sex as the most critical risk factors. Migration status appears as an additional factor of lower seropositivity since many persons

migrating to Germany may come from countries with little or no _Borrelia_ exposure. DATA AVAILABILITY The German National Cohort (NAKO) data is not openly available due to data protection

measures. However, scientists can apply for data access following the official usage regulations and upon formal request to the NAKO use and access committee (https://transfer.nako.de/).

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PubMed  PubMed Central  Google Scholar  Download references FUNDING Open Access funding enabled and organized by Projekt DEAL. This project used German National Cohort (NAKO) data

(www.nako.de). NAKO is funded by the German Federal Ministry of Education and Research (BMBF), the Helmholtz Association, and federal states. Participating universities and institutes of the

Leibniz Association provided additional funding. Funding references: 01ER1301A/B/C and 01ER1511D. MJH receives a scholarship from the Life Science Stiftung (LSS) to promote science and

research. AUTHOR INFORMATION AUTHORS AND AFFILIATIONS * Department for Epidemiology, Helmholtz Centre for Infection Research (HZI), Braunschweig, Germany Max J. Hassenstein, Yvonne Kemmling 

& Stefanie Castell * PhD Programme “Epidemiology”, Braunschweig-Hannover, Germany Max J. Hassenstein * Max-Delbrueck-Center for Molecular Medicine in the Helmholtz Association (MDC),

Molecular Epidemiology Research Group, Berlin, Germany Tobias Pischon, Ilais Moreno Velásquez & Jürgen Janke * Max-Delbrueck-Center for Molecular Medicine in the Helmholtz Association

(MDC), Biobank Technology Platform, Berlin, Germany Tobias Pischon & Jürgen Janke * Berlin Institute of Health at Charité-Universitätsmedizin Berlin, Core Facility Biobank, Berlin,

Germany Tobias Pischon * Charité-Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität Zu Berlin, Berlin, Germany Tobias Pischon * Institute of

Epidemiology and Social Medicine, University of Münster, Münster, Germany André Karch & Henning Teismann * Institute of Epidemiology, Helmholtz Zentrum München–German Research Center for

Environmental Health (GmbH), Neuherberg, Germany Annette Peters, Alexandra Schneider & Sigrid Thierry * Chair of Epidemiology, Institute for Medical Information Processing, Biometry and

Epidemiology, Medical Faculty, Ludwig-Maximilians-Universität München, Munich, Germany Annette Peters * Department of RNA-Biology of Bacterial Infections, Helmholtz Institute for RNA-Based

Infection Research, Würzburg, Germany Tobias Kerrinnes * NAKO Studienzentrum, Klinik für Diagnostische und Interventionelle Radiologie und Neuroradiologie, Universitätsklinikum Augsburg,

Augsburg, Germany Sigrid Thierry * TWINCORE, Centre for Experimental and Clinical Infection Research, a Joint Venture of the Hannover Medical School and Helmholtz Centre for Infection

Research, 30625, Hannover, Germany Stefanie Castell Authors * Max J. Hassenstein View author publications You can also search for this author inPubMed Google Scholar * Tobias Pischon View

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Conceptualization: SC, MJH; Methodology: M.J.H., S.C., T.P.; Formal analysis: M.J.H.; Investigation: S.C., Y.K., A.K., T.P., A.P., H.T., S.T., J.J.; Data Curation: M.J.H.; Writing—Original

Draft: M.J.H.; Writing—Review & Editing: M.J.H., S.C., T.P., A.P., A.K., H.T., A.S., I.M.V., T.K.; Visualization: M.J.H.; Supervision: S.C.; Project administration: S.C.; Funding

acquisition: S.C., T.K. All authors reviewed the manuscript. CORRESPONDING AUTHOR Correspondence to Stefanie Castell. ETHICS DECLARATIONS COMPETING INTERESTS The authors declare no competing

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permissions ABOUT THIS ARTICLE CITE THIS ARTICLE Hassenstein, M.J., Pischon, T., Karch, A. _et al._ Seropositivity of _Borrelia burgdorferi_ s.l. in Germany—an analysis across four German

National Cohort (NAKO) study sites. _Sci Rep_ 13, 21087 (2023). https://doi.org/10.1038/s41598-023-47766-6 Download citation * Received: 20 February 2023 * Accepted: 17 November 2023 *

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