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Heterogeneity in the abundance and distribution of Ixodes ricinus and Borrelia burgdorferi ( sensu lato ) in Scotland: implications for risk prediction

View Article: PubMed Central - PubMed

ABSTRACT

Background: Cases of Lyme borreliosis, a vector-borne zoonosis caused by bacteria in the Borrelia burgdorferi (sensu lato) species group, have increased in recent years in Europe. Knowledge of environmental factors associated with abundance of the tick vector Ixodes ricinus and the pathogen B. burgdorferi (s.l.) is of interest to understand responses to environmental changes, predict variation in risk and to inform management interventions.

Methods: Nineteen woodland sites across Scotland were surveyed in 2012 for B. burgdorferi (s.l.) infection in questing I. ricinus nymphs (n = 200 per site), deer abundance and vegetation. Climatic factors were extracted for each site. Six additional sites were surveyed for questing nymphs in both 2012 and 2013 (n = 200 per site and year) to test for variation in B. burgdorferi (s.l.) prevalence between years.

Results: The mean prevalence of B. burgdorferi (s.l.) across 19 sites was 1.7% (95% CI: 1.4–2.2%; range 0–6%), all four genospecies known to be present in the UK were detected: B. garinii, B. afzelii, B. burgdorferi (sensu stricto) and B. valaisiana. A higher prevalence of B. burgdorferi (s.l.), higher densities of nymphs and higher densities of infected nymphs were found at sites with warmer climates, estimated with growing degree-days. No association between infection prevalence in nymphs and woodland type (semi-natural mixed vs coniferous) or deer density was found. At six sites sampled in 2012 and 2013, there was a significant increase in B. afzelli prevalence at two sites and a decrease in B. garinii prevalence at one site.

Conclusions: This study highlights challenges for the prediction of risk of Lyme borreliosis, reflecting the sensitivity of both pathogen and vector ecology to habitat, host and climatic factors. Significant changes in the prevalence of individual genospecies at sites monitored across time are likely to be due to variability in the host community composition between years. Our results indicate the importance of monitoring dynamic variables such as reservoir host populations as well as climate and habitat factors over multiple years, to identify environmental factors associated with Lyme borreliosis risk.

Electronic supplementary material: The online version of this article (doi:10.1186/s13071-016-1875-9) contains supplementary material, which is available to authorized users.

No MeSH data available.


B. burgdorferi (s.l.) prevalence and genospecies composition in questing Ixodes ricinus nymphs at six sites in Scotland sampled in multiple years. Site locations are shown in Fig. 1. Each site has three bars which illustrate the results of sampling conducted in (from left to right for each site) 2007/2008, 2012 and 2013. Sites are categorised as ‘high’ and ‘low’ prevalence based on the initial prevalence estimate in 2007/2008
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Fig4: B. burgdorferi (s.l.) prevalence and genospecies composition in questing Ixodes ricinus nymphs at six sites in Scotland sampled in multiple years. Site locations are shown in Fig. 1. Each site has three bars which illustrate the results of sampling conducted in (from left to right for each site) 2007/2008, 2012 and 2013. Sites are categorised as ‘high’ and ‘low’ prevalence based on the initial prevalence estimate in 2007/2008

Mentions: At the six sites sampled in multiple years, (1200 nymphs tested in each year), the prevalence at ‘low’ and ‘high’ prevalence sites varied through time (Fig. 4, Additional file 2: Table S2). The best-fit model for B. burgdorferi (s.l.), B. afzelii and B. garinii prevalence at the six sites sampled in 2012 and 2013 was the intercept model, year of sampling was not supported in any of these models (Additional file 3: Table S3). There was a non-significant tendency for an increased prevalence of B. afzelii in 2013 compared to 2012 (delta AICc = 1.6, P = 0.06, Additional file 3: Table S3). At the site level, there were significant increases in B. afzelii prevalence at two of the six sites, ‘COM’ and ‘CR’ and a significant decrease in the prevalence of B. garinii at site DR between 2012 and 2013 (Fig. 4).Fig. 4


Heterogeneity in the abundance and distribution of Ixodes ricinus and Borrelia burgdorferi ( sensu lato ) in Scotland: implications for risk prediction
B. burgdorferi (s.l.) prevalence and genospecies composition in questing Ixodes ricinus nymphs at six sites in Scotland sampled in multiple years. Site locations are shown in Fig. 1. Each site has three bars which illustrate the results of sampling conducted in (from left to right for each site) 2007/2008, 2012 and 2013. Sites are categorised as ‘high’ and ‘low’ prevalence based on the initial prevalence estimate in 2007/2008
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC5120507&req=5

Fig4: B. burgdorferi (s.l.) prevalence and genospecies composition in questing Ixodes ricinus nymphs at six sites in Scotland sampled in multiple years. Site locations are shown in Fig. 1. Each site has three bars which illustrate the results of sampling conducted in (from left to right for each site) 2007/2008, 2012 and 2013. Sites are categorised as ‘high’ and ‘low’ prevalence based on the initial prevalence estimate in 2007/2008
Mentions: At the six sites sampled in multiple years, (1200 nymphs tested in each year), the prevalence at ‘low’ and ‘high’ prevalence sites varied through time (Fig. 4, Additional file 2: Table S2). The best-fit model for B. burgdorferi (s.l.), B. afzelii and B. garinii prevalence at the six sites sampled in 2012 and 2013 was the intercept model, year of sampling was not supported in any of these models (Additional file 3: Table S3). There was a non-significant tendency for an increased prevalence of B. afzelii in 2013 compared to 2012 (delta AICc = 1.6, P = 0.06, Additional file 3: Table S3). At the site level, there were significant increases in B. afzelii prevalence at two of the six sites, ‘COM’ and ‘CR’ and a significant decrease in the prevalence of B. garinii at site DR between 2012 and 2013 (Fig. 4).Fig. 4

View Article: PubMed Central - PubMed

ABSTRACT

Background: Cases of Lyme borreliosis, a vector-borne zoonosis caused by bacteria in the Borrelia burgdorferi (sensu lato) species group, have increased in recent years in Europe. Knowledge of environmental factors associated with abundance of the tick vector Ixodes ricinus and the pathogen B. burgdorferi (s.l.) is of interest to understand responses to environmental changes, predict variation in risk and to inform management interventions.

Methods: Nineteen woodland sites across Scotland were surveyed in 2012 for B. burgdorferi (s.l.) infection in questing I. ricinus nymphs (n = 200 per site), deer abundance and vegetation. Climatic factors were extracted for each site. Six additional sites were surveyed for questing nymphs in both 2012 and 2013 (n = 200 per site and year) to test for variation in B. burgdorferi (s.l.) prevalence between years.

Results: The mean prevalence of B. burgdorferi (s.l.) across 19 sites was 1.7% (95% CI: 1.4–2.2%; range 0–6%), all four genospecies known to be present in the UK were detected: B. garinii, B. afzelii, B. burgdorferi (sensu stricto) and B. valaisiana. A higher prevalence of B. burgdorferi (s.l.), higher densities of nymphs and higher densities of infected nymphs were found at sites with warmer climates, estimated with growing degree-days. No association between infection prevalence in nymphs and woodland type (semi-natural mixed vs coniferous) or deer density was found. At six sites sampled in 2012 and 2013, there was a significant increase in B. afzelli prevalence at two sites and a decrease in B. garinii prevalence at one site.

Conclusions: This study highlights challenges for the prediction of risk of Lyme borreliosis, reflecting the sensitivity of both pathogen and vector ecology to habitat, host and climatic factors. Significant changes in the prevalence of individual genospecies at sites monitored across time are likely to be due to variability in the host community composition between years. Our results indicate the importance of monitoring dynamic variables such as reservoir host populations as well as climate and habitat factors over multiple years, to identify environmental factors associated with Lyme borreliosis risk.

Electronic supplementary material: The online version of this article (doi:10.1186/s13071-016-1875-9) contains supplementary material, which is available to authorized users.

No MeSH data available.