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Ticks - ecology, new hazards, and relevance for public health
Södertörn University, School of Natural Sciences, Technology and Environmental Studies, Environmental Science. Södertörn University, Centre for Baltic and East European Studies (CBEES), Baltic & East European Graduate School (BEEGS).ORCID iD: 0000-0002-8237-4254
2024 (English)Doctoral thesis, comprehensive summary (Other academic)Alternative title
Fästingar - ekologi, nya riskfaktorer och deras betydelse för folkhälsan (Swedish)
Abstract [en]

Ticks and tick-borne diseases are ranking second only to mosquitoes as vectors of pathogens responsible for diseases in both humans and domestic animals. In the countries around the Baltic Sea, two medically important tick species are increasing both in range and abundance, and the public health threat posed by tick-borne diseases in this area is steadily growing. The aim of this thesis was to study the eco-epidemiological dynamics and mechanisms of ticks and bacterial tick-borne pathogens along the natural-urban gradient.

Green spaces have become important intersections between humans, domestic animals, ticks, and tick-borne pathogens. Along the natural-urban gradient in Stockholm County, Sweden, we examined the impact of green space characteristics on tickabundance and pathogens prevalence. In this study all questing ticks were molecularly identified as Ixodes ricinus. Questing ticks were abundant in natural and seminatural habitats, but also present in urbanized parks. Important drivers of tickabundance included significant negative effects of local vegetation height and positiveeffects of mixed coniferous forests in the surrounding landscape.

The prevalence of Borrelia burgdorferi sensu lato was 24% and that of Anaplasma phagocytophilum 7.5%. B. miyamotoi was found at a few sites with a prevalence of 0.9%. The dominant B. burgdorferi (s.l.) genospecies was B. afzelii. Tree stem density had a significant positive effect on B. burgdorferi (s.l.) prevalence. Broadleaved forests and total forest edge had significant positive effects on A. phagocytophilum prevalence, persisting even in highly urbanized areas. The tick-borne disease equine granulocytic anaplasmosis (EGA) significant increased from 2002 to 2015, with a yearly peak in late summer and early fall.

The public health risk for tick-borne diseases in an urban green space was estimated from hazard data on tick abundances and pathogen prevalence combined with exposure data using residential population densities and green space visitor numbers. The results indicated a medium to high risk of tick-borne diseases at most sites. Structured interviews with visitors showed that even if visitors showed a high tick awareness and attempted to avoid ticks, most protective measures were only practiced during specific recreational activities.

The findings from this doctoral project show a notable risk of encountering ticks and tick-borne pathogens along the entire natural-urban gradient, even in highly urbanized areas traditionally perceived as having a low risk. The information on the eco-epidemiological drivers of EGA is important also for the medical health field since the agent causing EGA is identical to the agent causing human disease. Despite ticks and their pathogens green spaces still continue to play a vital role in public health, but the omnipresent risk of tick-borne diseases highlights the need for public health initiatives to mitigate this risk. 

Abstract [sv]

Fästingar är näst efter myggor de viktigaste vektorerna för spridning av sjukdomar både till människor och husdjur. I länderna runt Östersjön finns två medicinskt viktiga fästingarter som ökar i utbredning och antal, vilket också utgör ett ökat hot mot folkhälsan. Syftet med avhandlingen var att studera eko-epidemiologisk dynamik och viktiga mekanismer för spridningen av fästingar och fästingburna bakterier i en urban gradient.

Grönområden i och runt städer utgör mötesplatser för människor, husdjur, fästingar och fästingburna patogener. I Stockholms län undersöktes effekterna av grönområdenas egenskaper på förekomst av fästingar och deras patogener utefter den urbana gradienten. Alla insamlade fästingar artbestämdes med molekylära metoder, och samtliga tillhörde arten Ixodes ricinus. Fästingar var vanliga i rurala områden och naturliga miljöer, men förekom även i urbana parker. Viktiga faktorer för förekomst av fästingar var den signifikant negativa effekten av vegetationshöjd vid insamlingsplatsen, och den signifikant positiva effekten av barrblandskog i det omgivande landskapet.

I studien av patogener var prevalensen av Borrelia burgdorferi sensu lato 24% och för Anaplasma phagocytophilum 7.5%. Fästingar infekterade med B. miyamotoi påträffades vid några få platser med en prevalens på 0.9%. Den dominerande arten inom gruppen av B. burgdorfgeri (s.l.) var B. afzelii. Trädtäthet runt insamlingsplatsen hade en signifikant positiv effekt på prevalensen av B. burgdorferi (s.l.). Utbredningen av lövskogar och skogskanter hade signifikant positiva effekter på prevalensen av A. phagocytophilum, och fästingar infekterade med A. phagocytophilum förekom även i urbana parker. Den fästingburna sjukdomen granulocytär anaplasmos hos häst, ökade signifikant från 2002 till 2015, med flest fall på sensommar och tidig höst.

Folkhälsorisker för fästingburna sjukdomar i ett urbant grönområde uppskattades med hjälp av information om fästingförekomst, patogenprevalens, befolkningstäthet och besöksantal. Resultatet visade en måttlig till hög risk för fästingburna sjukdomar i hela det undersökta grönområdet. Vid intervjuer med besökare påvisades en hög medvetenhet om fästingar och fästingspridda sjukdomar, men att skyddsåtgärder endast tillämpades vid specifika fritidsaktiviteter såsom bärplockning.

Resultatet från avhandlingen visar på en betydande risk för spridning av fästingburna sjukdomar längs med hela den urbana gradienten, inklusive områden som traditionellt ansetts ha en låg risk. Resultaten som visar på eko-epidemiologiska mekanismer för spridning av granulocytär anaplasmos hos häst är relevanta också ur ett folkhälsoperspektiv eftersom bakterierna orsakar sjukdom även hos människor. Trots risker med fästingar och deras sjukdomar är grönområden ytterst viktiga för folkhälsan utifrån andra hälsoaspekter, men det behövs initiativ och medvetenhet för att motverka riskerna.

Place, publisher, year, edition, pages
Huddinge: Södertörns högskola, 2024. , p. 196
Series
Södertörn Doctoral Dissertations, ISSN 1652-7399 ; 226
Keywords [en]
Baltic Sea region, eco-epidemiology, habitat, Ixodes persulcatus, Ixodes ricinus, landscape, risk, urbanization
National Category
Ecology
Research subject
Environmental Studies; Baltic and East European studies
Identifiers
URN: urn:nbn:se:sh:diva-53598ISBN: 978-91-89504-70-7 (print)ISBN: 978-91-89504-71-4 (electronic)OAI: oai:DiVA.org:sh-53598DiVA, id: diva2:1840903
Public defence
2024-03-22, MB505, Alfred Nobels allé 7, Huddinge, 10:00 (English)
Opponent
Supervisors
Part of project
Human – environment interactions and the epidemiological periurban landscape of tick-borne diseases, The Foundation for Baltic and East European Studies
Funder
The Foundation for Baltic and East European Studies, 52/12Available from: 2024-02-29 Created: 2024-02-27 Last updated: 2024-03-01Bibliographically approved
List of papers
1. Factors responsible for Ixodes ricinus presence and abundance across a natural-urban gradient
Open this publication in new window or tab >>Factors responsible for Ixodes ricinus presence and abundance across a natural-urban gradient
2023 (English)In: PLOS ONE, E-ISSN 1932-6203, Vol. 18, no 5, article id e0285841Article in journal (Refereed) Published
Abstract [en]

To better understand the spatial distribution of the common tick Ixodes ricinus, we investigated how local site factors and landscape characteristics influence tick presence and abundance in different greenspaces along the natural-urban gradient in Stockholm County, Sweden. Ticks and field data were collected in 2017 and 2019 and analyzed in relation to habitat type distributions estimated from land cover maps using geographical information system (GIS). A total of 1378 (992 larvae, 370 nymphs, 13 females, and 3 males) questing ticks were collected from 295 sampling plots in 47 different greenspaces. Ticks were present in 41 of the 47 greenspaces and our results show that both local site features such as vegetation height, and landscape characteristics like the amount of mixed coniferous forest, significantly affect tick abundance. Tick abundance was highest in rural areas with large natural and seminatural habitats, but ticks were also present in parks and gardens in highly urbanized areas. Greenspaces along the natural-urban gradient should be included in surveillance for ticks and tick-borne diseases, including highly urbanized sites that may be perceived by the public as areas with low risk for tick encounters.

Place, publisher, year, edition, pages
Public Library of Science (PLoS), 2023
Keywords
Forests, Ricinus, Larvae, Nymphs, Urbanization, Ticks, Ixodes, Forest ecology
National Category
Environmental Sciences
Research subject
Environmental Studies; Baltic and East European studies
Identifiers
urn:nbn:se:sh:diva-51517 (URN)10.1371/journal.pone.0285841 (DOI)000993290400020 ()37195993 (PubMedID)2-s2.0-85159760656 (Scopus ID)
Funder
The Foundation for Baltic and East European Studies, 52/2018
Available from: 2023-05-23 Created: 2023-05-23 Last updated: 2024-02-27Bibliographically approved
2. Ixodes-borne bacterial pathogen distribution across a natural-urban gradient
Open this publication in new window or tab >>Ixodes-borne bacterial pathogen distribution across a natural-urban gradient
Show others...
(English)Manuscript (preprint) (Other academic)
National Category
Natural Sciences
Research subject
Environmental Studies; Baltic and East European studies
Identifiers
urn:nbn:se:sh:diva-53600 (URN)
Funder
The Foundation for Baltic and East European Studies, 52/12
Note

As manuscript in dissertation

Available from: 2024-02-27 Created: 2024-02-27 Last updated: 2024-02-28Bibliographically approved
3. Equine Granulocytic Anaplasmosis in Southern Sweden: Associations with coniferous forest, water bodies and landscape heterogeneity
Open this publication in new window or tab >>Equine Granulocytic Anaplasmosis in Southern Sweden: Associations with coniferous forest, water bodies and landscape heterogeneity
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2019 (English)In: Agriculture, Ecosystems & Environment, ISSN 0167-8809, E-ISSN 1873-2305, Vol. 285, article id 106626Article in journal (Refereed) Published
Abstract [en]

Landscape characteristics influence both vector and host habitats affecting the spatial and temporal distribution of vector-borne diseases. Anaplasma phagocytophilum is one of the most widespread tick-borne diseases in Europe causing tick-borne fever (TBF) in domestic ruminants, and granulocytic anaplasmosis in humans, horses and companion animals. The aim of this study was to identify landscape factors associated with Equine Granulocytic Anaplasmosis (EGA) cases in a refined temporal and spatial analysis by combining land cover data and presence/absence disease data, using a geographical information system (GIS). This study is a retrospective analysis utilizing 1030 EGA diagnostic test results extracted from the National Veterinary Institute (SVA, Sweden). The association between EGA and different land cover types was analyzed with generalized linear models. To analyze the relation between landscape heterogeneity and EGA, we calculated the Gini-Simpson index. Our results showed a significant increase in the proportion positive EGA cases from 2002 to 2015 and marked differences in the seasonal within year distribution of EGA cases. The association with landscape configuration is shown by the positive relationship between A. phagocytophilum and coniferous forest, water bodies, and landscape heterogeneity, respectively. The information on the eco-epidemiological drivers for EGA can be central for disease control and prevention. Our method of linking land cover to disease risk may be applied to other vector-borne diseases and to other study regions.

Place, publisher, year, edition, pages
Elsevier, 2019
Keywords
Epidemiology, Landscape ecology, Vector-borne diseases
National Category
Environmental Sciences
Research subject
Environmental Studies; Baltic and East European studies
Identifiers
urn:nbn:se:sh:diva-38735 (URN)10.1016/j.agee.2019.106626 (DOI)000500213400016 ()2-s2.0-85070302032 (Scopus ID)
Funder
The Foundation for Baltic and East European Studies, 52/2018
Available from: 2019-08-15 Created: 2019-08-15 Last updated: 2024-02-27Bibliographically approved
4. Ticks: public health risks in urban green spaces
Open this publication in new window or tab >>Ticks: public health risks in urban green spaces
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2024 (English)In: BMC Public Health, E-ISSN 1471-2458, Vol. 24, no 1, article id 1031Article in journal (Refereed) Published
Abstract [en]

Background: Urban green spaces are important for human health, but they may expose visitors to tick-borne diseases. This not only presents a potential public health challenge but also undermines the expected public health gains from urban green spaces. The aim of this study is to assess the public health risk of tick-borne diseases in an urban green space used for recreation in Stockholm, Sweden.

Methods: We used a mixed method approach identifying both the magnitude of the tick hazard and the extent of the human exposure to tick-borne diseases. At six entry points to an urban green space, we sampled ticks and documented microhabitat conditions from five randomly assigned 2 m × 2 m plots. Surrounding habitat data was analyzed using geographical information system (GIS). Nymphs and adult ticks were tested for Borrelia burgdorferi sensu lato and Anaplasma phagocytophilum using TaqMan qPCR. Positive B. burgdorferi (s.l.) ticks were further analyzed by nested PCR amplification and sequence analysis. Population census data and visitor count data were used to estimate the degree of human exposure to tick-borne diseases. To further understand the degree to which visitors get in contact with infected ticks we also conducted interviews with visitors to green spaces.

Results: High tick densities were commonly found in humid broadleaved forest with low field vegetation. High pathogen prevalence was significantly correlated with increasing proportions of artificial areas. Integrating the tick hazard with human exposure we found that the public health risk of tick-borne diseases was moderate to high at most of the studied entry points. Many of the visitors frequently used urban green spaces. Walking was the most common activity, but visitors also engaged in activities with higher risk for tick encounters. Individual protective measures were connected to specific recreational activities such as picking berries or mushrooms.

Conclusions: The number of visitors can be combined with tick inventory data and molecular analyses of pathogen prevalence to make crude estimations of the public health risk of tick-borne diseases in urban green spaces. The risk of encountering infected ticks is omnipresent during recreational activities in urban green spaces, highlighting the need for public health campaigns to reduce the risk of tick-borne diseases.

Place, publisher, year, edition, pages
Springer Nature, 2024
Keywords
Ixodes persulcatus, Ixodes ricinus, Exposure, Habitat; Hazard, Human activity, Microhabitat, Recreation, Tick-borne diseases
National Category
Natural Sciences
Research subject
Environmental Studies; Baltic and East European studies
Identifiers
urn:nbn:se:sh:diva-53599 (URN)10.1186/s12889-024-18540-8 (DOI)001201501900004 ()38614967 (PubMedID)2-s2.0-85190373009 (Scopus ID)
Funder
The Foundation for Baltic and East European Studies, 52/12
Note

As manuscript in dissertation

Available from: 2024-02-27 Created: 2024-02-27 Last updated: 2024-04-29Bibliographically approved

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