Lyme disease ecology in a changing world: consensus, uncertainty and critical gaps for improving control

Abstract

Lyme disease is the most common tick-borne disease in temperate regions of North America, Europe and Asia, and the number of reported cases has increased in many regions as landscapes have been altered. Although there has been extensive work on the ecology and epidemiology of this disease in both Europe and North America, substantial uncertainty exists about fundamental aspects that determine spatial and temporal variation in both disease risk and human incidence, which hamper effective and efficient prevention and control. Here we describe areas of consensus that can be built on, identify areas of uncertainty and outline research needed to fill these gaps to facilitate predictive models of disease risk and the development of novel disease control strategies. Key areas of uncertainty include: (i) the precise influence of deer abundance on tick abundance, (ii) how tick populations are regulated, (iii) assembly of host communities and tick-feeding patterns across different habitats, (iv) reservoir competence of host species, and (v) pathogenicity for humans of different genotypes of Borrelia burgdorferi Filling these knowledge gaps will improve Lyme disease prevention and control and provide general insights into the drivers and dynamics of this emblematic multi-host-vector-borne zoonotic disease.This article is part of the themed issue 'Conservation, biodiversity and infectious disease: scientific evidence and policy implications'.

Keywords: Borrelia burgdorferi; Ixodes; dilution effect; emerging infectious disease; epidemiology.

Figure 1.

Schematic of the ecology of Lyme disease. The tick vector has three stages, larvae, nymphs and adults, which each take one blood meal (except adult males) before moulting into the next stage or reproducing and dying (adult females). Adult female ticks feed primarily on deer, whereas the other two stages feed from a wide range of vertebrates including mammals, birds and reptiles with widely varying probabilities of infecting ticks as described in the main text, figure 4 and the electronic supplementary material. Host species are eaten by a suite of interacting predators, and their populations are influenced by fluctuations in food availability. Original illustrations by Yiwei Wang and Taal Levi.

Figure 2.

Data illustrating the correlations between deer density and nymphal tick density at two sites in Connecticut (Redrawn from [63]). The top row of panels shows the relationship between deer density (deer km⁻²) and larval tick density (ticks 100 m⁻²) 1 year later that result from adult ticks (density not reported) feeding on deer in the previous year. The second row shows the relationship between larval tick density and nymphal tick density that fed larvae would moult into 1 year later. Finally, the bottom row shows the relationship between deer density and nymphal tick density 2 years later. Simple Pearson's correlation statistics are shown for each relationship, and where relationships appeared to be nonlinear and potentially asymptotic, a simple nonlinear function was fit to the data (with the p-value corresponding to the slope coefficient).

Figure 3.

Microclimate and density-dependent factors influencing tick development, survival, activity and feeding success. (a) Inter-stage development rates of l. ricinus (blue) and l. scapularis (orange) at different temperatures (redrawn from [75] and [76]). (b) Survival of nymphal l. scapularis ticks after 4–24 h exposure to four different humidity treatments (redrawn from [77]). (c) Proportion of ticks questing plotted against vapour pressure deficit, a measure of dessication stress (redrawn from [78] after correcting for mortality [68]). (d) Per cent of larval Ixodes trianguliceps ticks successfully engorging when feeding on Clethrionomys glareolus (now Myodes glareolus) that had been fed on by variable number of ticks 14 days previously (redrawn from [79]).

Figure 4.

Role of hosts in contributing to the population of infected nymphal ticks at sites in North America and Europe. The first column in each plot shows the fraction of ticks that fed on each host. The second column shows the relative reservoir competence (duration and probability of infecting feeding ticks) of each host (for the actual reservoir competence, see the electronic supplemental material), and the third column shows the estimated fraction of infected nymphal ticks arising from feeding on each species. See the electronic supplemental material for detailed data, calculations and sources. Map of tick distributions reprinted from [2].

Figure 5.

Summary of patterns of Lyme disease risk (density of infected nymphal ticks) and human incidence across a fragmentation gradient from highly urban areas (far left) to large forested areas (right) based on the available literature (see text). The mechanisms underlying the trends in both risk and incidence are given above the graph. The two blue and three red curves ending with question marks illustrate the variability and uncertainty in the pattern of incidence and disease risk in large forested areas. (Online version in colour.)