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. 

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.

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.

In 2017, ticks and field data were collected from 12 different sites in Stockholm County originally chosen as random controls for another study but was never used. In 2019, we collected ticks and field data at 35 randomly selected sites along the natural-urban gradient. To calculate and urbanization index, we used the proportion of artificial surfaces surrounding each site. All sampling sites were visited once with a total of 295 sampling plots inventoried for ticks and field data. For each sampling plot, we recorded date, time, temperature, weather conditions, number of ticks, vegetation height and tree stem density surrounding the inventory plot. To retrieve large landscape characteristics, we established 10 buffer zones ranging from 100m to 1000m around each sampling site in GIS using satellite land cover maps (retrieved from: https://www.naturvardsverket.se/verktyg-och-tjanster/kartor-och-karttjanster/nationella-marktackedata/ladda-ner-nationella-marktackedata/). These maps have a spatial resolution of 10m and include the following main categories 1) Forest and seminatural areas, 2) Open areas, 3) Arable land, 4) Wetlands, 5) Artificial surfaces and 6) Inland and marine water. These main categories are further divided into subcategories with detailed information regarding the different land cover classes. In the analyses, we used the main categories, with the exception of Forest and seminatural areas where we included eight individual forest types: Pine forest, Spruce forest, Mixed coniferous forest, Mixed forest, Broadleaved forest, Broadleaved hardwood forest, Broadleaved forest with hardwood forest and Temporarily non-forest. To calculate landscape configuration metrics at each sampling site, we used land cover data from the GIS buffers with a 1000m radius, exported to GeoTIFF format and analyzed them with FRAGSTATS version 4. For landscape heterogeneity we used Shannons’ diversity index (SHDI) and to measure the aggregation of landscape attributes we used Contagion (CONTAG). As measures of forest configuration, we used percent of forest cover (PLAND) and total forest edge length (TE). All statistical analyses were performed with R version 4.0.3. To analyze the effect of possible risk factors for tick abundance in different greenspaces across the natural-urban gradient, we used generalized linear mixed models assuming Poisson distributed residuals. As the data contained a larger proportion of zeros than would be expected according to a Poisson or a negative binomial distribution causing overdispersion, we fitted zero-inflated Poisson models using the package glmmTMB (generalized linear mixed models using Template Model Builder).

För att förstå utbredningen av den vanliga fästingen Ixodes ricinus, undersökte vi hur både lokala faktorer och olika landskapsegenskaper påverkar förekomsten av fästingar i grönområden längs med urbaniseringsgradienten i Stockholms län, Sverige. Fästingar och fältdata samlades in under 2017 och 2019 och analyserades i relation till habitatdata och landskapsdata framtaget från geografiskt informationssystem (GIS). 2017 samlades fästingar och fältdata in från 12 olika platser i Stockholms län som ursprungligen hade valts som slumpmässiga kontroller till en annan studie men aldrig använts. 2019 samlades fästingar och fältdata in från 35 olika platser längs med urbaniseringsgradienten. Dessa 35 platser valdes slumpmässigt ut med hjälp av GIS. För att beräkna urbaniseringsgraden för varje plats, använde vi andelen exploaterad mark i en 1000m buffertzon. För de 12 första insamlingsplatserna under 2017 valde vi slumpmässigt ut 10 2m × 2m rutor för inventering av fästingar och fältdata. På de 35 platser som vi inventerade 2019, samlade vi in fästingar i 5 2m × 2m rutor. Vi besökte alla platser en gång och totalt inventerades 295 provtagningsrutor. För varje ruta noterade vi datum, tid, väderförhållande, antal fästingar, vegetationshöjd och trädstamstäthet runt varje ruta. För att ta fram landskapsdata skapades 10 buffertzoner från 100m till 1000m radies runt varje insamlingsplats i GIS tillsammans med Naturvårdverkets Nationella Marktäckedata. Dessa satellitkartor har en upplösning på 10m och har följande huvudkategorier 1) Skog, 2) Öppen mark, 3) Åkermark, 4) Öppen våtmark, 5) Exploaterad mark, och 6) Vatten. För att identifiera riskfaktorer valde vi att använda dessa huvudkategorier med undantag for kategorin Skog där vi valde att inkludera de åtta olika skogstyperna: Tallskog, Granskog, Barrblandskog, Lövblandad barrskog, Triviallövskog, Ädellövskog, Triviallövskog med ädellövsinslag och Temporärt ej skog. För att ta fram statistik och beräkna konfigurationen av landskapet runt varje insamlingsplats, använde vi marktäckedata från 1000m buffertzonen som exporterades till GeoTIFF-format och som sedan analyserades med FRAGSTATS version 4. Vi använde Shannons diversitetsindex (SHDI) för att uppskatta mångfalden av marktäcketyper runt varje insamlingsplats. För att mäta aggregeringen av de olika martäcketyperna i landskapet använde vi Contagion (CONTAG). Som ett mått på skogens konfiguration använde vi PLAND, som är proportionen av skog i landskapet och total edge (TE) som är den totala skogskantslängden. Alla statistiska analyser har gjorts med R, versionen 4.0.3. För att analysera effekterna av olika riskfaktorer på fästingförekomst i olika grönområden, använde vi generaliserade linjära mixade modeller med Poisson-fördelade residualer. Eftersom datasetet innehöll fler nollor än vad som förväntas enligt en Poisson eller negativ binomialfördelning som orsakar överdispersion, använde vi nollinflations-Poissonmodeller i paketet glmmTMB.

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.

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.