- Top of page
- Materials and methods
Arthropod species that are vectors of disease, and the pathogens they carry, are of increasing concern for public and animal health as invasive species in the context of climate and other environmental changes (Mainka & Howard 2010). A number of key invasion events have occurred in recent decades, including northward expansion of the range of Bluetongue virus in Europe (Purse et al. 2005), introduction and spread of West Nile virus in North America (Kilpatrick 2011), introduction of Chikungunya virus into Italy (Angelini et al. 2008), and emergence of Lyme disease risk in Canada (Ogden et al. 2009). Detailed knowledge of the ecology of the invader and the invasion process (Ogden et al. 2008a; Epanchin-Niell & Hastings 2010) is required to predict invasion patterns, and design key public and animal health responses of surveillance, prevention and control (Ogden et al. 2008a).
For emerging Lyme disease risk in Canada, we have extensive knowledge of the ecology of the Lyme disease system and a 20 year time series of passive surveillance data for the tick vector Ixodes scapularis Say, which comprises submissions of ticks by members of the public via medical and veterinary clinics (Ogden et al. 2006, 2010). Ticks dispersed from tick populations by hosts such as migratory birds are also detected by the system, which limits its specificity for identifying the location of established reproducing tick populations (Ogden et al. 2006, 2008b). However, by more detailed analysis of the numbers of ticks submitted per unit population (Koffi et al. 2012), or by detecting space-time clusters of ticks with low prevalence of infection with the bacterial agent of Lyme disease Borrelia burgdorferi Johnson (emergent I. scapularis populations being initially B. burgdorferi-free: Ogden et al. 2010), we can identify the spatio-temporal occurrence of emerging tick populations more precisely (Ogden et al. 2010; Leighton et al. 2012).
Lyme disease is emerging in Canada because I. scapularis is expanding its range into and across Eastern and Central Canada (Ogden et al. 2009). In the absence of an effective vaccine, public health responses involve providing information on prevention, control, diagnosis and treatment to the public and healthcare practitioners targeted to the geographic locations where first the tick, and then B. burgdorferi have invaded the local woodland/ecotone communities. We have developed a number of tools to assist in identifying likely or actual risk locations, including predictive risk maps (Ogden et al. 2008a). More recently, we have estimated the rate at which tick populations are invading, and identified environmental factors affecting that rate (Leighton et al. 2012). With these two tools, we now have a clear picture of where and when tick vector populations will establish.
An important additional piece of information required, however, is how long it takes B. burgdorferi to invade the locations where the tick populations have become established. B. burgdorferi infection prevalence within host-seeking ticks, as well as tick abundance and/or occurrence, is a key determinant of public health risk from Lyme disease. Early identification of emerging tick populations provides an early warning for Lyme disease risk emergence, but how early is that warning, and how long will it take before nymphal tick infection prevalence values reach those (>20%) associated with the high Lyme disease incidence seen in northeastern USA?
In Eastern Canada, tick populations establish free of B. burgdorferi infection because: (i) a threshold abundance of ticks in newly established populations must be reached before the basic reproduction number for B. burgdorferi can rise above unity (Norman et al. 1999); (ii), in Eastern Canada B. burgdorferi invasion may be inherently less rapid than tick invasion because of the life cycle and seasonal activity of the ticks (Fig. 1). Ticks invade northwards by being carried on migratory birds (and possibly some mammals) moving north in springtime when nymphal ticks are active but very few larval ticks are active (Ogden et al. 2008a,b). Any infected nymphal ticks engorging on migratory birds will moult into adults, which will feed mostly on reservoir-incompetent white-tailed deer Odocoileus virginianus Zimmermann (Telford et al. 1988), so this route of B. burgdorferi invasion is severely limited or a dead end. Some migratory bird species are competent reservoirs (Brinkerhoff et al. 2010), but infective northward migrating passerines in spring are uncommon, and northward migratory birds in northeastern North America carry few larval I. scapularis (Ogden et al. 2008b). However, any larvae that acquire infection from an infected bird would become infective ‘immigrant’ nymphs, which usually feed on competent reservoir hosts (e.g. rodents) and be able to introduce B. burgdorferi. Consistent with this understanding of the invasion process, B. burgdorferi is absent or occurs at low prevalence in ticks and hosts in locations where the ticks have recently become established (Bouchard et al. 2011). The infection-free ticks produced locally are detectable in passive surveillance as space-time clusters of submitted ticks with low infection prevalence because the locally produced ticks dilute the infection prevalence in ticks arriving from the USA that are also collected in passive surveillance (Ogden et al. 2010).
Figure 1. A diagram of the Ixodes scapularis life cycle (solid lines) and Borrelia burgdorferi transmission cycle (broken lines). Stages that are carried into Canada by hosts in spring are indicated by bird symbols. The inset shows stylized annual seasonal activity patterns of immature I. scapularis in northeastern (NE – upper panel) and Midwestern (MW – lower panel) USA.
Download figure to PowerPoint
Here, we analysed infection prevalence in ticks collected in passive surveillance in southern Canada to identify the invasion of tick populations by detecting spatial clusters of ticks with low infection prevalence (Ogden et al. 2010). We then assessed the time it takes for these clusters to disappear as B. burgdorferi invades where the ticks have become established. We then used an existing simulation model of B. burgdorferi transmission to explore possible processes in the ecology of the system that may affect the speed at which B. burgdorferi invades following tick invasion. Specifically, we investigated the relative importance of the numbers of immigrating infected and uninfected ticks, compared to the ecological conditions (host density and biodiversity) at the point of invasion.
- Top of page
- Materials and methods
In this study, we used spatio-temporal analysis of a long-term data set on infection prevalence in the tick population to provide the first quantitative estimate of the time gap between tick invasion and the subsequent increase in Lyme disease risk associated with invasion of B. burgdorferi. We then used a mechanistic model of B. burgdorferi transmission to explore ecological factors that determine the speed B. burgdorferi invades after tick populations become established. This allowed us to produce a framework for predicting how fast significant Lyme disease risk will emerge in locations into which the tick vectors are spreading.
Analysis of recent passive surveillance data allowed us to confirm and further characterize a space-time cluster of ticks of low infection prevalence associated with the emergence of newly established I. scapularis populations in southern Quebec. Field studies here have identified that emergent tick populations are initially B. burgdorferi-free (Ogden et al. 2008a, 2010), which is consistent with modelling studies that identify that a threshold abundance of vector ticks must be reached for B. burgdorferi transmission to be maintained (e.g. Norman et al. 1999; Ogden et al. 2007). These ticks initially dilute the prevalence of infection in ticks arriving from the USA causing location-specific declines in the infection prevalence in ticks collected in passive surveillance that detect where the tick populations are becoming established (Ogden et al. 2010). However, here we have continued our longitudinal analysis of passive surveillance data and identified that the cluster disappeared after 5 years, suggesting that under the environmental conditions in this location, the gap between I. scapularis becoming established (indicated by declining infection prevalence) and B. burgdorferi becoming established (indicated by increasing infection prevalence) was 5 years.
When our simulation model was parameterized with host abundances expected for the region, the timing of changes in infection prevalence simulated for ticks collected in passive surveillance was that observed in southern Quebec: that is, a gap of 5 years between the first sign of tick establishment and the first sign of establishment of efficient B. burgdorferi transmission cycles. The range of values for numbers of immigrating infectious nymphal and adult ticks that produced this gap was very limited: one immigrating infected engorged larva that survives the moult to become a questing infective nymph, and between 5 and 250 engorged nymphal ticks that survive to become questing adults per km2. A ratio of 10–25 immigrating engorged nymphs to one engorged larvae would be particularly consistent with the ratio expected of ticks carried north by migratory birds in spring when nymphal ticks are active and when larval ticks are found at low abundance on hosts due to the typical spring seasonality of nymphal and late summer activity for larval I. scapularis in northeastern North America (reviewed in Ogden et al. 2007). A total number of 100–250 immigrating engorged nymphal ticks that survive to become questing adults may provide an estimate of the numbers of immigrating ticks per km2 in southeastern Canada. The simulated decline in prevalence was lower than that observed, but this result was not surprising. Our simulation is for one establishing tick population whereas in the zone of tick population emergence in southern Quebec, tick establishment is likely occurring in <50% of the land surface (Ogden et al. 2010). Therefore, within the observed cluster in our surveillance data, the numerator for the observed prevalence would be the sum of locally produced infected ticks (which are few) plus immigrating infected ticks in the emerging tick populations and in all areas in between these tick populations. The prevalence of infected adult ticks at the end of the simulation was similar to that observed in locations where B. burgdorferi transmission has become established in Canada (Lindsay et al. 1997).
Space-time clusters of ticks with low infection prevalence were identified in other areas of Eastern Canada: eastern Ontario and the Maritimes (Nova Scotia and New Brunswick), where tick populations are establishing (http://www.phac-aspc.gc.ca/id-mi/tickinfo-eng.php). The cluster in the Maritime provinces spanned 7 years, which is likely to reflect a less temporally synchronous, and more spatially patchy, emergence of tick populations than in southern Quebec (L.R. Lindsay unpublished data). These findings support our assumptions on the tick and B. burgdorferi immigration mechanisms and the parameterization of our model. There was no significant space-time cluster among ticks collected in western Ontario and Manitoba (although there was a nonsignificant short 3-year decline in prevalence from 2003–2005) even though I. scapularis and B. burgdorferi have become established in a number of locations in the region (http://www.gov.mb.ca/health/lyme/surveillance.html). This supports our simulation results of only a very short gap, which may not be detectable in passive surveillance, between I. scapularis and B. burgdorferi establishment in locations where there are high numbers of immigrating infected engorged larvae as would be expected where immigrating ticks come from locations where larval and nymphal ticks are seasonally synchronous such as the Midwest USA (Brinkerhoff et al. 2011). In our simulations when the number of infected questing nymphs that immigrated as engorged larvae reached 100 (equalling the numbers of adult ticks that immigrated), there was no observable gap between I. scapularis and B. burgdorferi establishment (Fig. 4a). In nature, questing larval ticks outnumber questing nymphal ticks by an order of magnitude when the activity of these instars is seasonally synchronous in spring (Gatewood et al. 2009), so for every questing adult tick that immigrated in our model into Manitoba and western Ontario, it would be expected that there would be 10 questing nymphal ticks. For there to be no detectable gap between I. scapularis and B. burgdorferi establishment, the infection prevalence would have to be in the order of 10%. This level of prevalence was not be seen in engorged larval ticks collected from northward migrating birds in Eastern Canada (Ogden et al. 2008a,b) but may be more likely in engorged larval ticks immigrating into western Ontario and Manitoba from populations in Midwestern USA (Brinkerhoff et al. 2011).
Sensitivity analyses indicated that the main factors determining the interval between I. scapularis and B. burgdorferi establishment are the actual and relative rates of immigration of infected engorged larvae and engorged nymphs. We created a virtual community of tick hosts that is realistic for the situation in southeastern Canada, but in sensitivity analysis variations in reservoir host abundance and community had a relatively limited impact on the gap between I. scapularis and B. burgdorferi establishment. This means that while the abundance of deer, P. leucopus mice and other mammalian and avian species that form the community of hosts for ticks and pathogens determines the final equilibrium prevalence of B. burgdorferi infection in host-seeking ticks, any ‘dilution effect’ may have a limited effect on the gap between tick and B. burgdorferi invasion. Clearly, the model could be parameterized to have more profound effects on tick survival and B. burgdorferi transmission (Ogden et al. 2007; Ogden & Tsao 2009), so while our assumptions in setting model parameters may be appropriate in most cases, there may be some specific locations where establishment of B. burgdorferi is more rapid or slow.
Here, we have identified the speed at which B. burgdorferi invades following I. scapularis establishment in Canada by analysis of surveillance data, and explored the factors that may determine the duration of the interval between these events using a simulation model. Our results suggest that under current conditions of tick invasion in Eastern Canada, early identification of I. scapularis populations (Koffi et al. 2012) gives a window of c. 5 years before significant Lyme disease risk emerges. Using this time window, there may be imminent increased risk of Lyme disease in southeastern Ontario: the start of the space-time cluster identified in this region was 2007, suggesting that in 2012 infection prevalence in questing ticks will rise increasing the risk of Lyme disease to the public. In contrast, our study suggests that in regions receiving immigrating ticks that originate in locations where larval and nymphal activity is seasonally synchronous (such as western Ontario and Manitoba), B. burgdorferi transmission cycles would become established, and risk to the public from Lyme disease would rise, much more rapidly with the early identification of newly established tick populations providing little or no early warning of significant risk to the public. Similar effects of seasonal tick synchrony on tickborne pathogen invasion would be expected in other parts of the world where ticks and tickborne pathogens are expanding their range, and where seasonal activity of larval and nymphal ticks in source populations may vary depending on their location (e.g. I. ricinus in Europe: Randolph et al. 1999, 2002; Estrada-Peña et al. 2004). Invasion from locations where ticks and B. burgdorferi are established into immediate surrounding areas would also probably be free of detectable gaps between tick and pathogen establishment as local host dispersion would occur throughout the activity seasons of all instars of the ticks.