Questing Ixodes ricinus ticks and Borrelia spp. in urban green space across Europe: A review

Abstract

For more than three decades, it has been recognized that Ixodes ricinus ticks occur in urban green space in Europe and that they harbour multiple pathogens linked to both human and animal diseases. Urban green space use for health and well-being, climate mitigation or biodiversity goals is promoted, often without consideration for the potential impact on tick encounters or tick-borne disease outcomes. This review synthesizes the results of over 100 publications on questing I. ricinus and Borrelia spp. infections in ticks in urban green space in 24 European countries. It presents data on several risk indicators for Lyme borreliosis and highlights key research gaps and recommendations for future studies. Across Europe, mean density of I. ricinus in urban green space was 6.9 (range; 0.1-28.8) per 100 m² and mean Borrelia prevalence was 17.3% (range; 3.1%-38.1%). Similar density estimates were obtained for nymphs, which had a Borrelia prevalence of 14.2% (range; 0.5%-86.7%). Few studies provided data on both questing nymph density and Borrelia prevalence, but those that did found an average of 1.7 (range; 0-5.6) Borrelia-infected nymphs per 100 m² of urban green space. Although a wide range of genospecies were reported, Borrelia afzelii was the most common in most parts of Europe, except for England where B. garinii was more common. The emerging pathogen Borrelia miyamotoi was also found in several countries, but with a much lower prevalence (1.5%). Our review highlights that I. ricinus and tick-borne Borrelia pathogens are found in a wide range of urban green space habitats and across several seasons. The impact of human exposure to I. ricinus and subsequent Lyme borreliosis incidence in urban green space has not been quantified. There is also a need to standardize sampling protocols to generate better baseline data for the density of ticks and Borrelia prevalence in urban areas.

Keywords: Borrelia miyamotoi; Lyme disease; global change; public health; ticks; urban ecology; urbanization.

FIGURE 1

Total number of publications per country contributing to the assessment of risk posed by questing Ixodes ricinus in peri/urban areas of Europe, during the period 1990–2021

FIGURE 2

Total number of publications per year contributing to the assessment of risk posed by questing Ixodes ricinus in peri/urban areas of Europe, during the period 1990–2021

FIGURE 3

Mean tick density of Ixodes ricinus per 100 m² from studies in peri/urban green space across Europe (ordered West to East) during the period 1990–2021; 1 (Hansford et al., 2017); 2 (Greenfield, 2011); 3 (Hansford et al., 2021); 4 (Mathews‐Martin et al., 2020); 5 (Heylen et al., 2019); 6 (Reye et al., ; Junttila et al., 1999); 7 (Maetzel et al., 2005); 8 (Hauck et al., 2020); 9 (Chvostáč et al., 2018); 10 (Minichová et al., 2017); 11 (Svitálková et al., 2015); 12 (Bukowska et al., 2003); 13 (Kubiak & Dziekońska‐Rynko, 2006); 14 (Kubiak et al., 2019); 15 (Pet’ko et al., 1997); 16 (Kowalec et al., 2017); 17 (Borşan et al., 2020); 18 (Klemola et al., 2019); 19 (Mäkinen et al., 2003); 20 (Junttila et al., 1999); 21 (Sormunen et al., 2020); 22 (Cayol et al., 2017); 23 (Makenov et al., 2019)

FIGURE 4

Mean nymph density of Ixodes ricinus per 100 m² from studies in peri/urban green space across Europe (ordered West to East) during the period 1990–2021; 1 (Hansford et al., 2017); 2 (Greenfield, 2011); 3 (Hansford et al., 2021); 4 (Marchant et al., 2017); 5 (Vourc’h et al., 2016); 6 (Heylen et al., 2019); 7 (Maetzel et al., 2005); 8 (Hauck et al., 2020); 9 (Chvostáč et al., 2018); 10 (Svitálková et al., 2015); 11 (Minichová et al., 2017); 12 (Bukowska et al., 2003); 13 (Pet’ko et al., 1997); 14 (Kowalec et al., 2017); 15 (Borşan et al., 2020); 16 (Klemola et al., 2019); 17 (Sormunen et al., 2020); 18 (Makenov et al., 2019)

FIGURE 5

Mean Borrelia burgdorferi sensu lato prevalence in Ixodes ricinus adults and nymphs collected from peri/urban green space across Europe (ordered West to East), during the period 1990–2021. Error bars show 95% confidence intervals. Number of analysed ticks per country; Czech Republic (n = 2083); England (n = 1739); Finland (n = 441); France (n = 6199); Germany (n = 9755); Ireland (n = 103); Italy (n = 115); Poland (n = 1434); Romania (n = 95); Russia (n = 227); Slovakia (n = 2145); Switzerland (n = 1798); Ukraine (n = 976)

FIGURE 6

Mean Borrelia burgdorferi sensu lato prevalence in Ixodes ricinus adult ticks collected from peri/urban green space across Europe (ordered West to East), during the period 1990–2021. Error bars show 95% confidence intervals. Number of analysed adults per country; Czech Republic (n = 1485); England (n = 252); Finland (n = 53); France (n = 1676); Germany (n = 2854); Hungary (n = 240); Ireland (n = 24); Italy (n = 42); Lithuania (n = 36); Moldova (n = 198); Poland (n = 571); Romania (n = 65); Russia (n = 172); Slovakia (n = 475); Turkey (n = 75); Ukraine (n = 679)

FIGURE 7

Mean Borrelia burgdorferi sensu lato prevalence in Ixodes ricinus nymphs collected from peri/urban green space across Europe (ordered West to East), during the period 1990–2021. Error bars show 95% confidence intervals. Number of analysed nymphs per country; Czech Republic (n = 1079); England (n = 2400); Finland (n = 1774); France (n = 9874); Germany (n = 5429); Ireland (n = 79); Italy (n = 106); Poland (n = 56); Romania (n = 30); Russia (n = 55); Slovakia (n = 1000); Ukraine (n = 297)

FIGURE 8

Mean density of Borrelia burgdorferi sensu lato infected Ixodes ricinus nymphs per 100 m² from studies in peri/urban green space across Europe (ordered West to East), during the period 1990–2021; 1 (Hansford et al., 2017); 2 (Hansford et al., 2021); 3 (Nelson et al., 2015); 4 (Marchant et al., 2017); 5 (Vourc’h et al., 2016); 6 (Maetzel et al., 2005); 7 (Chvostáč et al., 2018); 8 (Klemola et al., 2019); 9 (Sormunen et al., 2020); 10 (Makenov et al., 2019)

FIGURE 9

Proportion of Borrelia burgdorferi sensu lato genospecies per country in Ixodes ricinus ticks collected from peri/urban green space across Europe (ordered West to East), during the period 1990–2021