Lars Eisen

Changes in the geographical distribution and abundance of the tick Ixodes ricinus during the past 30 years in Sweden

BackgroundIxodes ricinus is the main vector in Europe of human-pathogenic Lyme borreliosis (LB) spirochaetes, the tick-borne encephalitis virus (TBEV) and other pathogens of humans and domesticated mammals. The results of a previous 1994 questionnaire, directed at people living in Central and North Sweden (Svealand and Norrland) and aiming to gather information about tick exposure for humans and domestic animals, suggested that Ixodes ricinus ticks had become more widespread in Central Sweden and the southern part of North Sweden from the early 1980s to the early 1990s. To investigate whether the expansion of the ticks northern geographical range and the increasing abundance of ticks in Sweden were still occurring, in 2009 we performed a follow-up survey 16 years after the initial study.MethodsA questionnaire similar to the one used in the 1994 study was published in Swedish magazines aimed at dog owners, home owners, and hunters. The questionnaire was published together with a popular science article about the ticks biology and role as a pathogen vector in Sweden. The magazines were selected to get information from people familiar with ticks and who spend time in areas where ticks might be present.ResultsAnalyses of data from both surveys revealed that during the near 30-year period from the early 1980s to 2008, I. ricinus has expanded its distribution range northwards. In the early 1990s ticks were found in new areas along the northern coastline of the Baltic Sea, while in the 2009 study, ticks were reported for the first time from many locations in North Sweden. This included locations as far north as 66°N and places in the interior part of North Sweden. During this 16-year period the ticks range in Sweden was estimated to have increased by 9.9%. Most of the range expansion occurred in North Sweden (north of 60°N) where the ticks coverage area doubled from 12.5% in the early 1990s to 26.8% in 2008. Moreover, according to the respondents, the abundance of ticks had increased markedly in LB- and TBE-endemic areas in South (Götaland) and Central Sweden.ConclusionsThe results suggest that I. ricinus has expanded its range in North Sweden and has become distinctly more abundant in Central and South Sweden during the last three decades. However, in the northern mountain region I. ricinus is still absent. The increased abundance of the tick can be explained by two main factors: First, the high availability of large numbers of important tick maintenance hosts, i.e., cervids, particularly roe deer (Capreolus capreolus) during the last three decades. Second, a warmer climate with milder winters and a prolonged growing season that permits greater survival and proliferation over a larger geographical area of both the tick itself and deer. High reproductive potential of roe deer, high tick infestation rate and the tendency of roe deer to disperse great distances may explain the range expansion of I. ricinus and particularly the appearance of new TBEV foci far away from old TBEV-endemic localities. The geographical presence of LB in Sweden corresponds to the distribution of I. ricinus. Thus, LB is now an emerging disease risk in many parts of North Sweden. Unless countermeasures are undertaken to keep the deer populations, particularly C. capreolus and Dama dama, at the relatively low levels that prevailed before the late 1970s - especially in and around urban areas where human population density is high - by e.g. reduced hunting of red fox (Vulpes vulpes) and lynx (Lynx lynx), the incidences of human LB and TBE are expected to continue to be high or even to increase in Sweden in coming decades.

Using Geographic Information Systems and Decision Support Systems for the Prediction, Prevention, and Control of Vector-Borne Diseases

Emerging and resurging vector-borne diseases cause significant morbidity and mortality, especially in the developing world. We focus on how advances in mapping, Geographic Information System, and Decision Support System technologies, and progress in spatial and space-time modeling, can be harnessed to prevent and control these diseases. Major themes, which are addressed using examples from tick-borne Lyme borreliosis; flea-borne plague; and mosquito-borne dengue, malaria, and West Nile virus disease, include (a) selection of spatial and space-time modeling techniques, (b) importance of using high-quality and biologically or epidemiologically relevant data, (c) incorporation of new technologies into operational vector and disease control programs, (d) transfer of map-based information to stakeholders, and (e) adaptation of technology solutions for use in resource-poor environments. We see great potential for the use of new technologies and approaches to more effectively target limited surveillance, prevention, and control resources and to reduce vector-borne and other infectious diseases.

Recent Rapid Rise of a Permethrin Knock Down Resistance Allele in Aedes aegypti in México

Background Aedes aegypti, the ‘yellow fever mosquito’, is the primary vector to humans of dengue and yellow fever flaviviruses (DENV, YFV), and is a known vector of the chikungunya alphavirus (CV). Because vaccines are not yet available for DENV or CV or are inadequately distributed in developing countries (YFV), management of Ae. aegypti remains the primary option to prevent and control outbreaks of the diseases caused by these arboviruses. Permethrin is one of the most widely used active ingredients in insecticides for suppression of adult Ae. aegypti. In 2007, we documented a replacement mutation in codon 1,016 of the voltage-gated sodium channel gene (para) of Ae. aegypti that encodes an isoleucine rather than a valine and confers resistance to permethrin. Ile1,016 segregates as a recessive allele conferring knockdown resistance to homozygous mosquitoes at 5–10 µg of permethrin in bottle bioassays. Methods and Findings A total of 81 field collections containing 3,951 Ae. aegypti were made throughout México from 1996 to 2009. These mosquitoes were analyzed for the frequency of the Ile1,016 mutation using a melting-curve PCR assay. Dramatic increases in frequencies of Ile1,016 were recorded from the late 1990s to 2006–2009 in several states including Nuevo León in the north, Veracruz on the central Atlantic coast, and Yucatán, Quintana Roo and Chiapas in the south. From 1996 to 2000, the overall frequency of Ile1,016 was 0.04% (95% confidence interval (CI95) = 0.12%; n = 1,359 mosquitoes examined). The earliest detection of Ile1,016 was in Nuevo Laredo on the U.S. border in 1997. By 2003–2004 the overall frequency of Ile1,016 had increased ∼100-fold to 2.7% (±0.80% CI95; n = 808). When checked again in 2006, the frequency had increased slightly to 3.9% (±1.15% CI95; n = 473). This was followed in 2007–2009 by a sudden jump in Ile1,016 frequency to 33.2% (±1.99% CI95; n = 1,074 mosquitoes). There was spatial heterogeneity in Ile1,016 frequencies among 2007–2008 collections, which ranged from 45.7% (±2.00% CI95) in the state of Veracruz to 51.2% (±4.36% CI95) in the Yucatán peninsula and 14.5% (±2.23% CI95) in and around Tapachula in the state of Chiapas. Spatial heterogeneity was also evident at smaller geographic scales. For example within the city of Chetumal, Quintana Roo, Ile1,016 frequencies varied from 38.3%–88.3%. A linear regression analysis based on seven collections from 2007 revealed that the frequency of Ile1,016 homozygotes accurately predicted knockdown rate for mosquitoes exposed to permethrin in a bioassay (R2 = 0.98). Conclusions We have recorded a dramatic increase in the frequency of the Ile1,016 mutation in the voltage-gated sodium channel gene of Ae. aegypti in México from 1996 to 2009. This may be related to heavy use of permethrin-based insecticides in mosquito control programs. Spatial heterogeneity in Ile1,016 frequencies in 2007 and 2008 collections may reflect differences in selection pressure or in the initial frequency of Ile1,016. The rapid recent increase in Ile1,016 is predicted by a simple model of positive directional selection on a recessive allele. Unfortunately this model also predicts rapid fixation of Ile1,016 unless there is negative fitness associated with Ile1,016 in the absence of permethrin. If so, then spatial refugia of susceptible Ae. aegypti or rotational schedules of different classes of adulticides could be established to slow or prevent fixation of Ile1,016.

Transmission dynamics of an insect-specific flavivirus in a naturally infected Culex pipiens laboratory colony and effects of co-infection on vector competence for West Nile virus.

We established a laboratory colony of Culex pipiens mosquitoes from eggs collected in Colorado and discovered that mosquitoes in the colony are naturally infected with Culex flavivirus (CxFV), an insect-specific flavivirus. In this study we examined transmission dynamics of CxFV and effects of persistent CxFV infection on vector competence for West Nile virus (WNV). We found that vertical transmission is the primary mechanism for persistence of CxFV in Cx. pipiens, with venereal transmission potentially playing a minor role. Vector competence experiments indicated possible early suppression of WNV replication by persistent CxFV infection in Cx. pipiens. This is the first description of insect-specific flavivirus transmission dynamics in a naturally infected mosquito colony and the observation of delayed dissemination of superinfecting WNV suggests that the presence of CxFV may impact the intensity of enzootic transmission of WNV and the risk of human exposure to this important pathogen.

Use of Mapping and Spatial and Space-Time Modeling Approaches in Operational Control of Aedes aegypti and Dengue

The aims of this review paper are to 1) provide an overview of how mapping and spatial and space-time modeling approaches have been used to date to visualize and analyze mosquito vector and epidemiologic data for dengue; and 2) discuss the potential for these approaches to be included as routine activities in operational vector and dengue control programs. Geographical information system (GIS) software are becoming more user-friendly and now are complemented by free mapping software that provide access to satellite imagery and basic feature-making tools and have the capacity to generate static maps as well as dynamic time-series maps. Our challenge is now to move beyond the research arena by transferring mapping and GIS technologies and spatial statistical analysis techniques in user-friendly packages to operational vector and dengue control programs. This will enable control programs to, for example, generate risk maps for exposure to dengue virus, develop Priority Area Classifications for vector control, and explore socioeconomic associations with dengue risk.

County-Scale Distribution of Ixodes scapularis and Ixodes pacificus (Acari: Ixodidae) in the Continental United States.

Abstract The blacklegged tick, Ixodes scapularis Say, is the primary vector to humans in the eastern United States of the Lyme disease spirochete Borrelia burgdorferi, as well as causative agents of anaplasmosis and babesiosis. Its close relative in the far western United States, the western blacklegged tick Ixodes pacificus Cooley and Kohls, is the primary vector to humans in that region of the Lyme disease and anaplasmosis agents. Since 1991, when standardized surveillance and reporting began, Lyme disease case counts have increased steadily in number and in geographical distribution in the eastern United States. Similar trends have been observed for anaplasmosis and babesiosis. To better understand the changing landscape of risk of human exposure to disease agents transmitted by I. scapularis and I. pacificus, and to document changes in their recorded distribution over the past two decades, we updated the distribution of these species from a map published in 1998. The presence of I. scapularis has now been documented from 1,420 (45.7%) of the 3,110 continental United States counties, as compared with 111 (3.6%) counties for I. pacificus. Combined, these vectors of B. burgdorferi and other disease agents now have been identified in a total of 1,531 (49.2%) counties spread across 43 states. This marks a 44.7% increase in the number of counties that have recorded the presence of these ticks since the previous map was presented in 1998, when 1,058 counties in 41 states reported the ticks to be present. Notably, the number of counties in which I. scapularis is considered established (six or more individuals or one or more life stages identified in a single year) has more than doubled since the previous national distribution map was published nearly two decades ago. The majority of county status changes occurred in the North-Central and Northeastern states, whereas the distribution in the South remained fairly stable. Two previously distinct foci for I. scapularis in the Northeast and North-Central states appear to be merging in the Ohio River Valley to form a single contiguous focus. Here we document a shifting landscape of risk for human exposure to medically important ticks and point to areas of re-emergence where enhanced vector surveillance and control may be warranted.

Risk indicators for the tick Ixodes ricinus and Borrelia burgdorferi sensu lato in Sweden

The distributional area of the tick Ixodes ricinus (L.), the primary European vector to humans of Lyme borreliosis spirochaetes (Borrelia burgdorferi sensu lato) and tick‐borne encephalitis virus, appears to be increasing in Sweden. It is therefore important to determine which environmental factors are most useful to assess risk of human exposure to this tick and its associated pathogens. The geographical distribution of I. ricinus in Sweden was analysed with respect to vegetation zones and climate. The northern limit of I. ricinus and B. burgdorferi s.l. in Sweden corresponds roughly to the northern limit of the southern boreal vegetation zone, and is characterized climatically by snow cover for a mean duration of 150 days and a vegetation period averaging 170 days. The zoogeographical distribution of I. ricinus in Sweden can be classified as southerly–central, with the centre of the distribution south of the Limes Norrlandicus. Ixodes ricinus nymphs from 13 localities in different parts of Sweden were examined for the presence of B. burgdorferi s.l. and found to be infected with Borrelia afzelii and Borrelia garinii. Tick sampling localities were characterized on the basis of the density of Borrelia‐infected I. ricinus nymphs, presence of specific mammals, dominant vegetation and climate. Densities of I. ricinus nymphs and Borrelia‐infected nymphs were significantly correlated, and nymphal density can thus serve as a general indicator of risk for exposure to Lyme borreliosis spirochaetes. Analysis of data from this and other studies suggests that high densities of Borrelia‐infected nymphs typically occur in coastal, broadleaf vegetation and in mixed deciduous/spruce vegetation in southern Sweden. Ixodes ricinus populations consistently infected with B. burgdorferi s.l. can occur in: (a) biotopes with shrews, rodents, hares and birds; (b) biotopes with shrews, rodents, hares, deer and birds, and (c) island locations where the varying hare (Lepus timidus) is the only mammalian tick host.

Proactive Vector Control Strategies and Improved Monitoring and Evaluation Practices for Dengue Prevention

ABSTRACT Despite tremendous efforts by public health organizations in dengue-endemic countries, it has proven difficult to achieve effective and sustainable control of the primary dengue virus vector Aedes aegypti (L.) and to effectively disrupt dengue outbreaks. This problem has multiple root causes, including uncontrolled urbanization, increased global spread of dengue viruses, and vector and dengue control programs not being provided adequate resources. In this forum article, we give an overview of the basic elements of a vector and dengue control program and describe a continuous improvement cyclical model to systematically and incrementally improve control program performance by regular efforts to identify ineffective methods and inferior technology, and then replacing them with better performing alternatives. The first step includes assessments of the overall resource allocation among vector/dengue control program activities, the efficacy of currently used vector control methods, and the appropriateness of technology used to support the program. We expect this will reveal that 1) some currently used vector control methods are not effective, 2) resource allocations often are skewed toward reactive vector control measures, and 3) proactive approaches commonly are underfunded and therefore poorly executed. Next steps are to conceptualize desired changes to vector control methods or technologies used and then to operationally determine in pilot studies whether these changes are likely to improve control program performance. This should be followed by a shift in resource allocation to replace ineffective methods and inferior technology with more effective and operationally tested alternatives. The cyclical and self-improving nature of the continuous improvement model will produce locally appropriate management strategies that continually are adapted to counter changes in vector population or dengue virus transmission dynamics. We discuss promising proactive vector control approaches and the continued need for the vector and dengue control community to incorporate emerging technologies and to partner with academia, business and the community-at-large to identify new solutions that reduce dengue.

Environmentally Related Variability in Risk of Exposure to Lyme Disease Spirochetes in Northern California: Effect of Climatic Conditions and Habitat Type

Abstract Risk of exposure to Borrelia burgdorferi sensu lato (s.l.) spirochetes, which include the causative agents of Lyme disease, is, in part, determined by the density of questing infected vector ticks. We sought to clarify the temporal patterns of nymphal activity, and the extent of variation in peak and cumulative densities of B. burgdorferi s.l.-infected Ixodes pacificus Cooley & Kohls nymphs, at 12 sites within the ecologically diverse Mendocino County in northwestern California. Also, we assessed the impact of various environmental characteristics (e.g., climatologic variables, habitat type, deer usage) on the aforementioned tick-related traits. The average durations of total and peak (nymphal density > 75% of absolute peak) questing activity were 31% and 82% longer, respectively, in areas with conifers present than in oak woodlands, which represented the warmest and driest habitat type examined. Peak and cumulative densities of infected nymphs varied > 400-fold between sites. Both traits were positively associated with the presence of Quercus spp. oaks or deer, and lower in redwood/tanoak versus oak and oak/Douglas fir habitats. However, a prolonged duration of nymphal activity in redwood habitats, relative to oak woodlands, resulted in a shift from peak nymphal densities occurring in oak woodlands in spring to redwood/tanoak habitats in summer. In conclusion, our data clearly show significant variability in seasonal as well as spatial risk of exposure to Lyme disease spirochetes within a small but ecologically, diverse geographic area. Hence, temporally dynamic and spatially explicit models are needed to assess the risk of exposure to tick-borne pathogens at spatial scales encompassing diverse climatologic or ecological conditions.

Use of Google Earth to strengthen public health capacity and facilitate management of vector-borne diseases in resource-poor environments.

OBJECTIVE Novel, inexpensive solutions are needed for improved management of vector-borne and other diseases in resource-poor environments. Emerging free software providing access to satellite imagery and simple editing tools (e.g. Google Earth) complement existing geographic information system (GIS) software and provide new opportunities for: (i) strengthening overall public health capacity through development of information for city infrastructures; and (ii) display of public health data directly on an image of the physical environment. METHODS We used freely accessible satellite imagery and a set of feature-making tools included in the software (allowing for production of polygons, lines and points) to generate information for city infrastructure and to display disease data in a dengue decision support system (DDSS) framework. FINDINGS Two cities in Mexico (Chetumal and Merida) were used to demonstrate that a basic representation of city infrastructure useful as a spatial backbone in a DDSS can be rapidly developed at minimal cost. Data layers generated included labelled polygons representing city blocks, lines representing streets, and points showing the locations of schools and health clinics. City blocks were colour-coded to show presence of dengue cases. The data layers were successfully imported in a format known as shapefile into a GIS software. CONCLUSION The combination of Google Earth and free GIS software (e.g. HealthMapper, developed by WHO, and SIGEpi, developed by PAHO) has tremendous potential to strengthen overall public health capacity and facilitate decision support system approaches to prevention and control of vector-borne diseases in resource-poor environments.