Distribution of tick-borne microorganisms in human-biting ticks in France collected through a Citizen-science program

Abstract Ticks occupy diverse habitats, increasing the risk of human exposure. Assessing the public health threat posed by ticks requires rigorous monitoring of their distribution and of the prevalence of tick-borne pathogens. In France since 2017, the citizen science program CiTIQUE monitors human tick bites through multiple complementary approaches. Citizens can report bites and submit biting ticks to a national tick bank for research and surveillance. This study aimed to investigate human exposure to tick-borne microorganisms including pathogens across France, using ticks submitted through the CiTIQUE program. In total, 2,009 ticks were selected from the CiTIQUE tick bank, identified, and screened for microorganisms using a real-time microfluidic PCR method. Most bites involved Ixodes ricinus nymphs except in Mediterranean regions where Dermacentor and Rhipicephalus ticks were more common. Twenty-six microorganisms were detected, eighteen of which are potentially pathogenic to humans. These pathogens were widely distributed across the country. Borrelia spp. were the most frequently detected pathogens with spatial variation among regions. Anaplasma phagocytophilum infection rates varied from region to region. Neoehrlichia mikurensis was found in seven out of twelve French regions. Rickettsia species diversity was highest in the southeast, associated with a greater diversity of vectors. Five percent of ticks were infected with more than one pathogen. Although spatial heterogeneity was observed, no region was free of infected ticks. This study demonstrates the power of citizen science for nationwide surveillance of tick-borne pathogens, providing a large-scale overview of pathogen diversity and distribution across France from crowdsourced tick data. Competing Interest Statement The authors have declared no competing interest. Funding Statement This project was made possible through significant funding from different sources, including from the Ministry of Health and Access to Care, the Laboratory of Excellence ARBRE (ANR-11-LABX-0002-01), the Grand Est Region, the European Regional Development Fund, the ‘Des Hommes et Des Arbres’ investment program (Territoire d’Innovation), the Groupama Foundation, and the Fondation de France. This project was also carried out with own funding from ANSES and INRAE. Author Declarations I confirm all relevant ethical guidelines have been followed, and any necessary IRB and/or ethics committee approvals have been obtained. Yes I confirm that all necessary patient/participant consent has been obtained and the appropriate institutional forms have been archived, and that any patient/participant/sample identifiers included were not known to anyone (e.g., hospital staff, patients or participants themselves) outside the research group so cannot be used to identify individuals. Yes I understand that all clinical trials and any other prospective interventional studies must be registered with an ICMJE-approved registry, such as ClinicalTrials.gov. I confirm that any such study reported in the manuscript has been registered and the trial registration ID is provided (note: if posting a prospective study registered retrospectively, please provide a statement in the trial ID field explaining why the study was not registered in advance). Yes I have followed all appropriate research reporting guidelines, such as any relevant EQUATOR Network research reporting checklist(s) and other pertinent material, if applicable. Yes Footnotes ↵# co-first authors We added statistical analysis to support differences observed between different regions of France, and we clarified the human pathogenic status of the different microorganisms found in this study. The manuscript and supplemental files were updated accordingly and all figures were updated to increase their readability. We also added a discussion on the finding of nymphal Dermacentor ticks biting humans. Data Availability All data produced in the present study are available upon reasonable request to the authors. Data will be available from the Recherche Data Gouv Repository when accepted.