Skip to main content
Download PDF

Spatial and seasonal variation in the prevalence of Anaplasma phagocytophilum and Borrelia burgdorferi sensu lato in questing Ixodes ricinus ticks in Norway

Parasites & Vectors volume 6, Article number: 187 (2013) Cite this article

Abstract

Background

Understanding the variation in prevalence of Borrelia burgdorferi sensu lato (Lyme Borreliosis Spirochaetes, LBS) and Anaplasma phagocytophilum (causing tick-borne fever in ruminants and human granulocytic ehrlichiosis) in ticks is vital from both a human and an animal disease perspective to target the most effective mitigation measures. From the host competence hypothesis, we predicted that prevalence of LBS would decrease with red deer density, while prevalence of A. phagocytophilum would increase.

Methods

Based on a sample of 112 adult and 686 nymphal Ixodes ricinus ticks collected with flagging during questing from 31 transects (4–500 m long) corresponding to individual seasonal home ranges of 41 red deer along the west coast of Norway, we tested whether there were spatial and seasonal variations in prevalence with a special emphasis on the population density of the most common large host in this area, the red deer (Cervus elaphus). We used a multiplex real-time PCR assay for detection of A. phagocytophilum and LBS.

Results

Prevalence of LBS was higher in adult female ticks (21.6%) compared to adult male ticks (11.5%) and nymphs (10.9%), while prevalence was similar among stages for prevalence of A. phagocytophilum (8.8%). Only partly consistent with predictions, we found a lower prevalence of LBS in areas of high red deer density, while there was no relationship between red deer density and prevalence of A. phagocytophilum in ticks. Prevalence of both bacteria was much higher in ticks questing in May compared to August.

Conclusions

Our study provides support to the notion that spatial variation in host composition forms a role for prevalence of LBS in ticks also in a northern European ecosystem, while no such association was found for A. phagocytophilum. Further studies are needed to fully understand the similar seasonal pattern of prevalence of the two pathogens.

Background

There is general agreement that Ixodes ricinus ticks have expanded in Europe in the last decades, probably due to climate change and potentially other factors such as increased host density and landscape changes [1]. Among emerging infectious diseases linked to climate change in Europe, the tick-borne disease Lyme borreliosis, caused by certain genotypes of the Borrelia burgdorferi sensu lato complex, hereafter called Lyme Borreliosis Spirochaetes (LBS), is one of the ones having the highest potential of severity to human society [2]. Another important disease agent in ticks is Anaplasma phagocytophilum. Some variants of this bacterium cause tick-borne fever (TBF) in domestic ruminants [3, 4], regarded by many as the most widespread tick-borne infection in animals in Europe [5]. Some genetic variants of A.phagocytophilum also cause granulocytic anaplasmosis in humans [6], horses [7] and companion animals [3, 8].

Risk of exposure to vector-borne pathogens is, among other factors, influenced by the abundance of the vector and the prevalence of the pathogen within the vector population [9]. Knowledge about variation in both tick abundance and pathogen prevalence is, therefore, necessary to understand disease risk [10]. It is a common statement that the increase in tick-borne disease in humans is associated with an overall increase in deer populations and closer contact between humans and deer [11]. This conclusion is based on the role of deer as important hosts for adult ticks, providing enough blood to ensure production of a large number of eggs in the adult female tick, resulting in high abundance of ticks. Deer species, therefore, may play a major role in tick abundances both in Europe [12, 13] and North America [14, 15], though not in all cases [9, 16]. However, deer do not seem to be competent transmission hosts for LBS [9, 17–20]. Actually, the innate immune system of cervids may even kill LBS in infected ticks feeding on them [21, 22]. This is supported by the lower prevalence of LBS reported from ticks collected on roe deer (Capreolus capreolus) and moose (Alces alces) compared to ticks collected in the landscape [23]. A study comparing islands in Norway also documented a lower prevalence in areas of high deer density [24]. However, several studies have found either no relationship or a positive relationship between roe deer density and prevalence in continental European ecosystems [25–27]. Rather, passerine birds are the main reservoir for B. garinii[28] and rodents for B. afzelii[29]. These are the two most common genospecies of LBS circulating in ticks in Europe, followed by B. burgdorferi sensu stricto and B. valaisiana[30], while prevalence of B. burgdorferi sensu stricto is lower in Norway [31]. Both B. afzelii and B. garinii, which are the dominating genotypes found in questing ticks in Norway [30], can cause human disease and hence LBS as a group are important and are our focus here.

The prevalence of both LBS [32–34] and A. phagocytophilum[35] varies geographically, but prevalence may not follow the same pattern as tick abundance, as host species may differ largely in both abundance and in their degree of reservoir competence for the actual strains of the bacteria (LBS: [36]; A. phagocytophilum: [4, 37]). As such, it has been proposed that deer, although they are important hosts for the ticks, reduce the prevalence of LBS in ticks. However, some researchers argue that this only happens at unrealistic high densities of deer [38]. The potential dilution role of deer hosts may be counteracted by their role in vector augmentation, increasing the number of larvae feeding on reservoir-competent small mammals and some passerine birds. Knowledge about the extent to which deer density is responsible for “dilution effects” is thus one aspect necessary to understand variation in Lyme-disease risk [39]. The role of host composition for prevalence of LBS is well established in general [39, 40], but studies from northern Europe are scarce. However, direct or indirect co-feeding transmission may enable deer to transmit LBS in spite of being incompetent hosts [41–44]. If important, one would expect co-feeding transmission to be more common in areas of high abundance of ticks, due to the increased likelihood of uninfected ticks feeding temperospatially close to infected ticks. Higher prevalence in areas with higher abundance of ticks has been previously reported in Sweden [45].

A. phagocytophilum was previously regarded as a bacterium circulating between a wide range of hosts. However, recent research suggests multiple, more or less distinct subpopulations with co-existing, but more or less independent transmission cycles restricted to one or a few host species [4, 46]. The role of European cervids in the transmission cycles of A. phagocytophilum are not completely understood, but high prevalence of infection [4, 47], presence of similar genotypes, both in deer and questing ticks in the same location [46] and establishment of persistent, subclinical infection after experimental inoculation [48] suggest that deer may function as competent reservoir hosts for some of the subpopulations. Consequently, a high population density of red deer (Cervus elaphus) should be expected to be associated with high prevalence of A. phagocytophilum in questing ticks. In accordance with this, higher prevalence of A. phagocytophilum was found in islands of higher deer density in Norway [24]. Co-feeding transmission has, to our knowledge not been regarded as playing a role in the transmission cycles of A. phagocytophilum. However, infected and non-infected ticks feeding on the same animal at the same time should increase transmission rate, at least in rodents, where the level of bacteraemia is regarded to be low and life span short [3]. High infestation intensity and frequency also seem to increase the bacteraemia in ruminants [49] and may, as such, possibly facilitate transmission in these species.

In this study, we have analyzed the variation in prevalence of B. burgdorferi sensu lato (LBS) and A. phagocytophilum using PCR in 112 questing adult and 686 nymphal ticks sampled from 31 transects corresponding to individual red deer home ranges along the west coast of Norway, with high densities of red deer in some areas. Our study area comprised of a wide range of environmental gradients (coast-inland, low-high elevation, flat-steep, low-high density of red deer; low-high density of ticks), we assessed how all of these gradients affected the prevalence of both pathogens, which has not been previously carried out. We specifically tested the following hypotheses: The host competence hypothesis (or dilution hypothesis) predicts reduced prevalence of LBS in areas of high red deer density, but a positive link to prevalence of A. phagocytophilum. The tick abundance hypothesis predicts increased prevalence of both LBS and A. phagocytophilum in areas with high abundance of ticks. This can result from higher transmission efficiency due to a higher likelihood of co-feeding transmission for LBS and a shorter time span between infected and non-infected ticks feeding on the same animal.

Methods

Study area

The study area is along the west coast of Norway (see Additional file 1). The topography is rugged with summits reaching 1000–1500 m a.s.l. just a few kilometers from the sea. The vegetation is within the boreonemoral vegetation zone. Forests are dominated by Scots pine (Pinus sylvestris) on marginal soils, with alder (Alnus incana) dominating in richer soils, and birch (Betula spp.) dominating at higher elevations. There are scattered stands of Norway spruce (Picea abies) planted by forestry mainly on better soils at low elevation. Climate is colder with increasing altitude and distance from the coast. There are dense populations of red deer in the area. The number of harvested red deer (in 2011) was 0.7-2.4 red deer per km2 in the municipalities included here, which corresponds to ~3.5-12.0 red deer per km2. The red deer populations are partially migratory [50]. Roe deer and moose were absent from our study site. There are livestocks in several of the areas, mainly free-ranging sheep (Ovis aries) during summer. Other available large hosts (>1 kg) are red fox (Vulpes vulpes), marten (Martes martes), mountain hare (Lepus timidus) and domestic cats. Densities of these are not known, but the impression is that there are low densities of hare and marten, while red fox are more common. Information regarding densities of smaller hosts such as voles, mice and birds are unavailable.

Tick collection

Questing Ixodes ricinus adult and nymphal ticks were sampled in May and August 2011 by aid of the cloth lure or “flagging” method [51] in connection with a study of variation in tick abundance in relation to red deer habitat use [50]. Sampling was based on known information on home ranges of red deer, with each transect (sampling unit) representing typically one red deer home range, but in some cases overlapping several home ranges. The spatial distribution of transects is given in Additional file 1. We used a towel (50*100 cm) attached to the end of a rod and dragged the towel over the vegetation allowing the questing ticks to attach. Each transect consisted of 12 survey plots with 20–50 m in-between, and each plot covered an approximately 10 m long and a 2 m wide belt; i.e. 20 m2. For every 2nd m after two drags on each side of the towel, ticks were counted and removed from the towel. Nymphs, adult females and adult males from each transect were pooled and killed using ethanol then dried and stored with silica beads at −20°C.

DNA extraction and pathogen detection

We analysed prevalence of A. phagocytophilum and LBS for individual ticks using real-time PCR. First, DNA extractions were performed according to Allender et al. [52]. The protocol was optimized for ticks by modifying the incubation step of the Qiagen DN easy® 96 Blood & Tissue kit; where ticks, 2 mm zirconium oxide beads, 40 μl of proteinase K solution and 4 μl Antifoam-A (Sigma) were incubated at 56°C overnight followed by 5 minutes of bead homogenization at 30 cycles per second using a Qiagen Tissue Lyser II. Some ticks were not broken and were crushed using wooden toothpicks. The remaining 160 μl of proteinase K solution was added and the homogenized mixture was incubated for 1 hour at 56°C. Centrifugation was carried out before removing seals at any step in the protocol to prevent cross-contaminating samples. The mixture was then transferred to the DN easy plates using the method described by Allender et al. [52].

Detection of A. phagocytophilum and LBS was carried out using a multiplex real-time PCR assay developed by Courtney et al. [53] on a Roche Light Cycler® 480 Real-Time PCR instrument. Roche Light Cycler® 480 Probes Master reaction mixtures was used for real-time PCR in 10 μl reactions following the cycling conditions that were described [53]. Positive controls of A. phagocytophilum and LBS DNA were used in addition to negative controls from the extraction. The results from the instrument were then scored into one of five categories: A. phagocytophilum positive, LBS positive, positive for both, unknown or negative.

Statistical analyses

The response variable was prevalence of either A. Phagocytophilum or of LBS, and we therefore used logistic regression. Our potential covariates were stage of tick (adult female, adult male or nymph), age of tick (adult vs. nymph), (log) abundance of tick in transect in May, months (May vs. August), and the spatial covariates (log) distance to main coast, (log) distance to fiord and elevation. We used two measures of red deer density. (1) The number of harvested red deer (2011) at the scale of municipalities divided by the counting area of red deer habitat, cfr. [54]. This is a coarse measure of overall population density of red deer. (2) As a more local scale measure of red deer density within a 200 m buffer from the mid-point of each transect, the habitat suitability for red deer was estimated as the ratio of use relative to availability of a given habitat, which is estimated based on a large sample of GPS-marked red deer from the same areas, cfr [55]. We considered two different random terms in our model to account for potential pseudoreplication using library “lme4”. The random term “transect” accounts for the same transect being recorded in May and August, while the random term “municipality” accounts for spatial autocorrelation among transects. We initially tested in ANOVA what random term to use. Then, we used a model selection approach aiming to find the most parsimonious model based on the Akaike Information Criterion (AIC). All analyses were performed in R v. 2.15.0.

Results

The overall prevalence of LBS was 10.9% in nymph (n = 686), 11.5% in adult male (n = 61) and 21.6% in adult female (n = 51) ticks (Table 1). The model including “municipality” as a random effect was a better model than the one with “transect” (p < 0.001). A model with both “transect” and “municipality” did not improve the model, as the estimated variance of the “transect” random effects was ~0. The most parsimonious model of LBS prevalence included stage of tick, month, distance to the coast, slope and density of red deer (see Additional file 1). There was higher prevalence in adult female ticks compared to adult male ticks and nymphs (Table 2). Prevalence in both stages was higher in May than in August and declined with increasing population density of red deer (Figure 1). Prevalence further decreased with increasing slope, but only tended to increase with distance from the coast (Table 2). Other covariates such as abundance of ticks, elevation and distance to fiord did not enter the best model (see Additional file 1).

Table 1 An overview of the prevalence (n infected) of A. phagocytophilum and Lyme Borreliosis Spirochate (LBS) positive adult male (M) and female (F) and nymphal ticks in May and August 2011 in Sogn & Fjordane, Norway
Full size table
Table 2 Estimated prevalence of Lyme Borreliosis Spirochates (LBS) in ticks collected in Sogn & Fjordane, Norway from a logistic mixed effects model. adF = adult female, adM = adult male
Full size table
Figure 1
figure 1

Prevalence of B. burgdorferi in nymph ticks as a function of the (harvest) density of red deer at the scale of municipality in Sogn og Fjordane, Norway. Average values for slope and distance to coast were used. Data points are raw proportions not adjusted for slope or distance to coast, while lines are predicated values (from GLM).

Full size image

The overall prevalence of A. phagocytophilum was 9.0% in nymphs (n = 686), 4.9% in adult male ticks (n = 61) and 9.8% in adult female ticks (n = 51). These differences were not significant, as stage of ticks did not enter the best model (see Additional file 1). The best random effect was “transect”, being a clearly better model than with “municipality” (p < 0.001). We found no evidence of a strong spatial structure in prevalence of A. phagocytophilum, as the most parsimonious model included only month as a predictor (see Additional file 1). There was markedly higher prevalence of A. phagocytophilum in May (11.3%) compared to August (5.0%) (Z = 2.799, p = 0.005).

We recorded 0.87% ticks with co-infection of LBS and A. phagocytophilum in all nymphs (Table 1). The overall correlation among transects in prevalence of LBS and A. phagocytophilum was moderate (r = 0.41).

Discussion

Ticks and tick-borne diseases have increased in Europe in recent decades with severe implications for human and animal health, understanding factors determining tick abundance and prevalence of pathogens is, therefore, of major interest. Our study reveals two main patterns; that prevalence of LBS declines as red deer density increases, while there is no apparent relationship between prevalence of A. phagocytophilum and red deer density. The first finding is consistent with predictions from the host competence hypothesis concerning LBS, also termed the dilution effect [39]. However, the host competence hypothesis predicts increases in prevalence of A. phagocytophilum with increasing deer density, but this prediction was not supported. Earlier studies in Europe found no [25, 27] or even positive relationship between roe deer [26] or red deer [56] density and prevalence of LBS. A problem for inference from these studies, as well as our own study, is that the ratio of Competent: incompetent hosts have not been determined explicitly. Variation in spatial density of deer does not automatically imply a change in ratio of competent: incompetent hosts, if the same factors driving deer abundance also drive variation in rodent abundance. However, in our case as in Scotland [56], much of the variation in red deer density is driven by harvesting management, thus likely reflecting a change in ratios of rodent: deer hosts rather than mainly habitat productivity differences.

Overall prevalence of A. phagocytophilum varies considerably across Europe. Our estimates (8.8%) are above the reported 1.6% for Italy/Slovenia [57], 1.9% in Luxembourg [58], 1.3% in Switzerland [59], and 3.2% in Hanover, Germany [60]. Estimates are close to the 8.7% reported in Leipzig, Germany [61], but lower than the 20.5% reported in Spain [62]. Our estimate of prevalence of A. phagocytophilum was higher than the 4.5% reported in an earlier study pooling various areas distributed over much of south Norway [63, 64]. However, they reported the highest values in Hitra at the west coast (up to 19.4%), with known high abundance of red deer [64]. Low prevalence in ticks may nevertheless cause high infection rates. In Belgium, the prevalence was only 3% in questing ticks, but a 21.7% in feeding ticks on cattle was reported [65]. The prevalence of LBS (10.9% in nymphs) found in our study was within the range typically reported in other studies from Europe [58]. Higher prevalence in adult females on the one hand, and lower prevalence in adult males and nymphs on the other as we found for LBS, was reported in Austria [66] and Switzerland [67], for A. phagocytophilum in Luxembourg [58] and for both pathogens in France [68]. This was attributed to an interaction between the ticks and the bacteria, with female ticks taking a larger blood meal [68], rather than to host composition. Our mean prevalence of LBS (12%) was somewhat lower than reported along the south coast of Norway (21.4%) [34], but within the wide range of prevalence (0-25%) from a study with scattered populations across southern Norway [31] and elsewhere in Europe [69]. Though with a limited sample size, only B. afzelii, some B. burgdorferi sensu stricto and no B. garinii was reported in the coastal zone of Norway, pointing to a rodent reservoir of LBS [31].

We found no correlation between spatial variation in local questing tick abundance and prevalence of LBS or A. phagocytophilum in ticks. Prevalence of both A. phagocytophilum and LBS was much higher in May than in August, consistent with a Swedish study [45] and a study from Luxembourg [58]. This may at first seem consistent with the temporal component of the tick abundance hypothesis, as the abundance of questing nymphal ticks declined markedly over the season [50]; see also [70], assuming that the development from one stage to another takes approximately one year, so that the questing tick population experienced a similar tick density back in time when they had their last blood meal. Also, further south in Norway, a peak in prevalence was observed later in the season when tick abundance peaked in that region [34]. However, in Scotland, nymphal abundance also decreased over the season while prevalence of LBS increased [56]. The relationship between prevalence of LBS, tick abundance and seasonality thus seems to differ among areas, and the tick abundance hypothesis linked to co-feeding seems, thus, not to be an overall predictor of prevalence.

Host composition and host reservoir competence may potentially play a role in the seasonal pattern. Throughout the questing season, the composition of the questing tick population varies according to the relative amount of tick stages that either emerge from moulting after a blood meal, some months earlier in the same season or emerge after behavioural diapause from the unfed stage or after developmental diapause from engorged and non-moulted stage [71]. The specific composition of the questing tick population and the time of their last blood meal may, therefore, influence the seasonal pattern of prevalence. During spring, densities of rodents are low, while high reproduction from spring onwards substantially increases population sizes towards fall. Also birds such as thrushes have large clutches increasing the population size from spring to autumn, and migratory stress can reactivate latent Borrelia infection and hence increase the reservoir competence of these species [72]. In contrast, red deer populations in Norway may increase by only some 15% from spring to fall due to females producing a single offspring each year. The ratio of rodent: deer and thrush: deer hosts, therefore, is likely much higher during fall. Given a certain mortality rate of ticks through the summer, a larger proportion of the ticks questing in May have likely had their last meal during the previous late summer or early fall compared to ticks questing in August. The same seasonal decline was, however, found for prevalence of A. phagocytophilum in Ixodes ricinus ticks, though there are indications of rodent A. phagocytophilum ecotypes not being transmitted by this tick species [46] while deer is considered as being a competent reservoir host for at least some subpopulations [37]. That we found co-infection of both pathogens in nymphs might suggest rodents or birds also play a role for transmission of A. phagocytophilum as indicated by a North American study [73], or that individual larvae have fed on multiple hosts.

A number of other processes may potentially explain seasonal variation in prevalence, such as effects of infection on tick behavior and survival [74, 75] and possibly the survival of the pathogen within the ticks over the season [76]. Firstly, ticks with infestation of LBS have larger fat stores and are more active than uninfected ticks [74, 75, 77]. It has also been suggested that infected ticks have a higher probability to undergo quiescence in order to avoid dry periods [58]. It may be speculated that the prevalence of infected ticks increases after environmental bottlenecks due to higher survival [77, 78]. In the study area, having moist summers, but a relatively harsh winter, the prevalence of both pathogens may increase over the winter. Secondly, it may be speculated that the survival of the bacteriae within the ticks is negatively affected when moulting and activity occurs in the warmest period of the year when the immune system of the tick is likely to be more effective at killing pathogens. If so, prevalence would also be lower in fall. Lastly, differences between areas may then arise if newly emerged ticks in some areas (e.g. Scotland) are more likely to start questing in fall, while they in other areas (e.g. Norway) go into diapause if they have more energy stores.

Conclusion

In conclusion, our study provides further support to a dilution effect of high deer density on LBS in a northern ecosystem in Europe, similar to what has been reported elsewhere [9, 18–20]. Clearly, the overall disease risk might nevertheless increase even with reduced prevalence; due to deer possibly increasing tick abundance [13, 79]. There was no clear association between deer density and prevalence of A. phagocytophilum. We cannot yet fully explain the seasonal decline in prevalence of both LBS and A. phagocytophilum from May to August, though several theories seem plausible. This may require further studies of the transmission cycle of the pathogens, host and tick dynamics, in particular the survival rates of the pathogens within the ticks and the influence of infection on tick questing behavior and life history.

References

  1. Jaenson TGT, Lindgren E: The range of Ixodes ricinus and the risk of contracting Lyme borreliosis will increase northwards when the vegetation period becomes longer. Ticks Tick Borne Dis. 2011, 2: 44-49. 10.1016/j.ttbdis.2010.10.006.

    Article  PubMed  Google Scholar 

  2. Lindgren E, Andersson Y, Suk JE, Sudre B, Semenza JC: Monitoring EU emerging infectious disease risk due to climate change. Science. 2012, 336: 418-419. 10.1126/science.1215735.

    CAS  Article  PubMed  Google Scholar 

  3. Woldehiwet Z: Anaplasma phagocytophilum in ruminants in Europe. Ann N Y Acad Sci. 2006, 1078: 446-460. 10.1196/annals.1374.084.

    CAS  Article  PubMed  Google Scholar 

  4. Scharf W, Schauer S, Freyburger F, Petrovec M, Schaarschimdt-Kiener D, Liebisch G, Runge M, Ganter M, Kehl A, Dumler JS, Garcia-Perez AL, Jensen J, Fingerle V, Meli ML, Ensser A, Stuen S, Von Loewenich FD: Distinct host species correlate with Anaplasma phagocytophilum ankA gene clusters. J Clin Microbiol. 2011, 49: 790-10.1128/JCM.02051-10.

    PubMed Central  Article  PubMed  Google Scholar 

  5. Stuen S: Anaplasma phagocytophilium - the most widespread tick-borne infection in animals in Europe. Vet Res Commun. 2007, 31: 79-84. 10.1007/s11259-007-0071-y.

    Article  PubMed  Google Scholar 

  6. Dumler JS, Choi KS, Garcia-Garcia JC, Barat NS, Scorpio DG, Garyu JW, Grab DJ, Bakken JS: Human granulocytic anaplasmosis and Anaplasma phagocytophilum. Emerg Infect Dis. 2005, 11: 1828-1834. 10.3201/eid1112.050898.

    PubMed Central  Article  PubMed  Google Scholar 

  7. Silaghi C, Liebisch G, Pfister K:Genetic variants ofAnaplasma phagocytophilumfrom 14 equine granulocytic anaplasmosis cases. ParasitVectors. 2011, 4: 161-

    CAS  Google Scholar 

  8. Carrade DD, Foley JE, Borjesson DL, Sykes JE: Canine granulocytic anaplasmosis: a review. J Vet Intern Med. 2009, 23: 1129-1141. 10.1111/j.1939-1676.2009.0384.x.

    CAS  Article  PubMed  Google Scholar 

  9. Ostfeld RS, Canham CD, Oggenfuss K, Winchcombe RJ, Keesing F: Climate, deer, rodents, and acorns as determinants of variation in Lyme-disease risk. PLoS Biol. 2006, 4: 1058-1068.

    CAS  Article  Google Scholar 

  10. Eisen RJ, Piesman J, Zielinski-Gutierrez E, Eisen L: What do we need to know about disease ecology to prevent Lyme disease in the northeastern United States?. J Med Entomol. 2012, 49: 11-22. 10.1603/ME11138.

    Article  PubMed  Google Scholar 

  11. Barbour AG: Fall and rise of Lyme disease and other Ixodes tick-borne infections in North America and Europe. Brit Med Bull. 1998, 54: 647-658. 10.1093/oxfordjournals.bmb.a011717.

    CAS  Article  PubMed  Google Scholar 

  12. Gray JS, Kahl O, Janetzki C, Stein J: Studies on the ecology of Lyme disease in a deer forest in County Galway, Ireland. J Med Entomol. 1992, 29: 915-920.

    CAS  Article  PubMed  Google Scholar 

  13. Gilbert L, Maffey GL, Ramsay SL, Hester AJ: The effect of deer management on the abundance of Ixodes ricinus in Scotland. Ecol Appl. 2012, 22: 658-667. 10.1890/11-0458.1.

    CAS  Article  PubMed  Google Scholar 

  14. Daniels TJ, Fish D, Schwartz I: Reduced abundance of Ixodes scapularis (Acari, Ixodidae) and Lyme disease risk by deer exclusion. J Med Entomol. 1993, 30: 1043-1049.

    CAS  Article  PubMed  Google Scholar 

  15. Stafford KC, DeNicola AJ, Kilpatrick HJ: Reduced abundances of Ixodes scapularis (Acari: Ixodidae) and the tick parasitoid Ixodiphagus hookeri(Hymenoptera: Encyrtidae) with reduction of white-tailed deer. J Med Entomol. 2003, 40: 642-652. 10.1603/0022-2585-40.5.642.

    Article  PubMed  Google Scholar 

  16. Jordan RA, Schulze TL, Jahn MB: Effects of reduced deer density on the abundance of Ixodes scapulatis (Acari: ixodidae) and Lyme disease incidence in a northern New Jersey endemic area. J Med Entomol. 2007, 44: 752-757. 10.1603/0022-2585(2007)44[752:EORDDO]2.0.CO;2.

    Article  PubMed  Google Scholar 

  17. Tälleklint L, Jaenson TGT: Transmission of Borrelia burgdorferi s.l. from mammal reservoirs to the primary vector of Lyme borreliosis, Ixodes ricinus (Acari, Ixodidae), in Sweden. J Med Entomol. 1994, 31: 880-886.

    Article  PubMed  Google Scholar 

  18. Piesman J, Gern L: Lyme borreliosis in Europe and North America. Parasitology. 2004, 129: S191-S220. 10.1017/S0031182003004694.

    Article  PubMed  Google Scholar 

  19. LoGiudice K, Duerr STK, Newhouse MJ, Schmidt KA, Killilea ME, Ostfeld RS: Impact of host community composition on Lyme disease risk. Ecology. 2008, 89: 2841-2849. 10.1890/07-1047.1.

    Article  PubMed  Google Scholar 

  20. Keesing F, Brunner J, Duerr S, Killilea M, LoGiudice K, Schmidt K, Vuong H, Ostfeld RS: Hosts as ecological traps for the vector of Lyme disease. Proc R Soc Lond Ser B. 2009, 276: 3911-3919. 10.1098/rspb.2009.1159.

    CAS  Article  Google Scholar 

  21. Kurtenbach K, De Michelis S, Etti S, Schaefer SM, Sewell HS, Brade V, Kraiczy P: Host association of Borrelia burgdorferi sensu lato - the key role of host complement. Trends Microbiol. 2002, 10: 74-79. 10.1016/S0966-842X(01)02298-3.

    CAS  Article  PubMed  Google Scholar 

  22. Bhide MR, Travnicek M, Levkutova M, Curlik J, Revajova V, Levkut M: Sensitivity of Borrelia genospecies to serum complement from different animals and humans: a host-pathogen relationship. FEMS Immunol Med Microbiol. 2005, 43: 165-172. 10.1016/j.femsim.2004.07.012.

    CAS  Article  PubMed  Google Scholar 

  23. Kjelland V, Ytrehus B, Stuen S, Skarpaas T, Slettan A: Prevalence of Borrelia burgdorferi in Ixodes ricinus ticks collected from moose (Alces alces) and roe deer (Capreolus capreolus) in southern Norway. Ticks Tick Borne Dis. 2011, 2: 99-103. 10.1016/j.ttbdis.2010.12.002.

    Article  PubMed  Google Scholar 

  24. Rosef O, Paulauskas A, Radzijevskaja J: Prevalence of Borrelia burgdorferi sensu lato and Anaplasma phagocytophilum in questing Ixodes ricinus ticks in relation to the density of wild cervids. Acta Vet Scand. 2009, 51: 47-10.1186/1751-0147-51-47.

    PubMed Central  Article  PubMed  Google Scholar 

  25. Pichon B, Mousson L, Figureau C, Rodhain F, Perez-Eid, C: Density of deer in relation to the prevalence of Borrelia burgdorferi sl in Ixodes ricinus nymphs in Rambouillet forest, France. Exp Appl Acarol. 1999, 23: 267-275. 10.1023/A:1006023115617.

    CAS  Article  PubMed  Google Scholar 

  26. Rizzoli A, Merler S, Furlanello C, Gench C: Geographical information systems and bootstrap aggregation (Baggin) of tree-based classifiers for Lyme disease risk prediction in Trentino, Italian Alps. J Med Entomol. 2002, 39: 485-492. 10.1603/0022-2585-39.3.485.

    Article  PubMed  Google Scholar 

  27. Jensen PM, Hansen H, Frandsen F: Spatial risk assessment for lyme borreliosis Denmark. Scand J Infect Dis. 2000, 32: 545-550. 10.1080/003655400458857.

    CAS  Article  PubMed  Google Scholar 

  28. Comstedt P, Bergström S, Olsen B, Garpmo U, Marjavaara L, Mejlon H, Barbour AG, Bunikis J: Migratory passerine birds as reservoirs of lyme borreliosis in Europe. Emerg Infect Dis. 2006, 12: 1087-1095. 10.3201/eid1207.060127.

    PubMed Central  Article  PubMed  Google Scholar 

  29. Hanincova K, Schafer SM, Etti S, Sewell HS, Taragelova V, Ziak D, Labuda M, Kurtenbach K: Association of Borrelia afzelii with rodents in Europe. Parasitology. 2003, 126: 11-20. 10.1017/S0031182002002548.

    CAS  Article  PubMed  Google Scholar 

  30. Jenkins A, Hvidsten D, Matussek A, Lindgren PE, Stuen S, Kristiansen BE: Borrelia burgdorferi sensu lato in Ixodes ricinus ticks from Norway: evaluation of a PCR test targeting the chromosomal flaB gene. Exp Appl Acarol. 2012, 58: 431-439. 10.1007/s10493-012-9585-2.

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  31. Paulauskas A, Ambrasiene D, Radzijevskaja J, Rosef O, Turcinaviciene J: Diversity in prevalence and genospecies of Borrelia burgdorferi sensu lato in Ixodes ricinus ticks and rodents in Lithuania and Norway. Int J Med Microbiol. 2008, 298 (S1): 180-187.

    CAS  Article  Google Scholar 

  32. Rauter C, Hartung T: Prevalence of Borrelia burgdorferi sensu lato genospecies in Ixodes ricinus ticks in Europe: a metanalysis. Appl Environ Microbiol. 2005, 71: 7203-7216. 10.1128/AEM.71.11.7203-7216.2005.

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  33. Horobik V, Keesing F, Ostfeld RS: Abundance and Borrelia burgdorferi-infection prevalence of nymphal Ixodes scapularis ticks along forest-field edges. Ecohealth. 2006, 3: 262-268.

    Article  Google Scholar 

  34. Kjelland V, Stuen S, Skarpaas T, Slettan A: Prevalence and genotypes of Borrelia burgdorferi sensu lato infection in Ixodes ricinus ticks in southern Norway. Scand J Infect Dis. 2010, 42: 579-585. 10.3109/00365541003716526.

    CAS  Article  PubMed  Google Scholar 

  35. Wallménius K, Pettersson JHO, Jaenson TGT, Nilsson K: Prevalence of Rickettsia spp., Anaplasma phagocytophilum, and Coxiella burnetii in adult Ixodes ricinus ticks from 29 study areas in central and southern Sweden. Ticks Tick Borne Dis. 2012, 3: 100-106. 10.1016/j.ttbdis.2011.11.003.

    Article  PubMed  Google Scholar 

  36. Ytrehus B, Vikøren T: Borrelia infections. Infectious diseases of wild mammals and birds in Europe. Edited by: Gavier-Widén D, Duff JP, Meredith A. 2012, Oxford, U.K: Blackwell, 345-362.

    Chapter  Google Scholar 

  37. Silaghi C, Hamel D, Thiel C, Pfister K, Passos LMF, Rehbein S: Genetic variants of Anaplasma phagocytophilum in wild Caprine and Cervid ungulates from the Alps in Tyrol, Austria. Vector Borne Zoonotic Dis. 2011, 11: 355-362. 10.1089/vbz.2010.0051.

    Article  PubMed  Google Scholar 

  38. Randolph SE: Tick-borne disease systems emerge from the shadows: the beauty lies in molecular detail, the message in epidemiology. Parasitology. 2009, 136: 1403-1413. 10.1017/S0031182009005782.

    CAS  Article  PubMed  Google Scholar 

  39. Randolph SE, Dobson ADM: Pangloss revisisted: a critique of the dilution effect and the biodiversity-buffers-disease paradigm. Parasitology. 2012, 139: 847-863. 10.1017/S0031182012000200.

    CAS  Article  PubMed  Google Scholar 

  40. Keesing F, Belden LK, Daszak P, Dobson A, Harvell CD, Holt RD, Hudson P, Jolles A, Jones KE, Mitchell CE, Myers SS, Bogich T, Ostfeld RS: Impacts of biodiversity on the emergence and transmission of infectious diseases. Nature. 2010, 468: 647-652. 10.1038/nature09575.

    CAS  Article  PubMed  Google Scholar 

  41. Cadenas FM, Rais O, Humair PF, Douet V, Moret J, Gern L: Identification of host bloodmeal source and Borrelia burgdorferi sensu lato in field-collected Ixodes ricinus ticks in Chaumont (Switzerland). J Med Entomol. 2007, 44: 1109-1117. 10.1603/0022-2585(2007)44[1109:IOHBSA]2.0.CO;2.

    CAS  Article  Google Scholar 

  42. Pichon B, Gilot B, Perez-Eid C: Detection of spirochaetes of Borrelia burgdorferi complex in the skin of cervids by PCR and culture. Eur J Epidemiol. 2000, 16: 869-873. 10.1023/A:1007646216035.

    CAS  Article  PubMed  Google Scholar 

  43. Kimura K, Isogai E, Isogai H, Kamewaka Y, Nishikawa T, Ishii N, Fujii N: Detection of Lyme disease spirochetes in the skin of naturally infected wild sika deer (Cervus nippon yesoensis) by PCR. Appl Environ Microbiol. 1995, 61: 1641-1642.

    PubMed Central  CAS  PubMed  Google Scholar 

  44. Ogden NH, Nuttall PA, Randolph SE: Natural lyme disease cycles maintained via sheep by co-feeding ticks. Parasitology. 1997, 115: 591-599. 10.1017/S0031182097001868.

    Article  PubMed  Google Scholar 

  45. Tälleklint L, Jaenson TGT: Relationship between Ixodes ricinus density and prevalence of infection with Borrelia-like spirochetes and density of infected ticks. J Med Entomol. 1996, 33: 805-811.

    Article  PubMed  Google Scholar 

  46. Bown KJ, Lambin X, Ogden NH, Begon M, Telford G, Woldehiwet Z, Birtles RJ: Delineating Anaplasma phagocytophilum ecotypes in coexisting, discrete enzootic cyles. Emerg Infect Dis. 2009, 15: 1948-1954. 10.3201/eid1512.090178.

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  47. Stuen S, Pettersen KS, Granquist EG, Bergström K, Bown KJ, Birtles RJ: Anaplasma phagocytophilum variants in sympatric red deer (Cervus elaphus) and sheep in southern Norway. Ticks Tick Borne Dis. 2013, 4: 197-201. 10.1016/j.ttbdis.2012.11.014.

    Article  PubMed  Google Scholar 

  48. Stuen S, Handeland K, Frammarsvik T, Bergstrom K: Experimental Ehrlichia phagocytophilia infection in red deer (Cervus elaphus). Vet Rec. 2001, 149: 390-392. 10.1136/vr.149.13.390.

    CAS  Article  PubMed  Google Scholar 

  49. Ogden NH, Casey ANJ, French NP, Adams JDW, Woldehiwet Z: Field evidence for density-dependent facilitation amongst Ixodes ricinus ticks feeding on sheep. Parasitology. 2002, 124: 117-125.

    CAS  PubMed  Google Scholar 

  50. Qviller L, Risnes-Olsen N, Bærum KM, Meisingset EL, Loe LE, Ytrehus B, Viljugrein H, Mysterud A: Landscape level variation in tick abundance relative to seasonal migration pattern of red deer. PLoS One. 2013, in press

    Google Scholar 

  51. Vassallo M, Pichon B, Cabaret J, Figureau C, Pérez-Eid C: Methodology for sampling questing nymphs of Ixodes ricinus (Acari: Ixodidae), the principal vector of Lyme disease in Europe. J Med Entomol. 2000, 37: 335-339. 10.1603/0022-2585(2000)037[0335:MFSQNO]2.0.CO;2.

    CAS  Article  PubMed  Google Scholar 

  52. Allender CJ, Easterday WJ, Van Ert MN, Wagner DM, Keim P: High-throughput extraction of arthropod vector and pathogen DNA using bead milling. Biotechniques. 2004, 37: 730-734.

    CAS  PubMed  Google Scholar 

  53. Courtney JW, Kostelnik LM, Zeidner NS, Massung RF: Multiplex real-time PCR for detection of Anaplasma phagocytophilum and Borrelia burgdorferi. J Clin Microbiol. 2004, 42: 3164-3168. 10.1128/JCM.42.7.3164-3168.2004.

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  54. Mysterud A, Meisingset EL, Veiberg V, Langvatn R, Solberg EJ, Loe LE, Stenseth NC: Monitoring population size of red deer: an evaluation of two types of census data from Norway. Wildl Biol. 2007, 13: 285-298. 10.2981/0909-6396(2007)13[285:MPSORD]2.0.CO;2.

    Article  Google Scholar 

  55. Loe LE, Bonenfant C, Meisingset EL, Mysterud A: Effects of spatial scale and sample size in GPS-based species distribution models: are the best models trivial for red deer management?. Eur J Wildl Res. 2012, 58: 195-203. 10.1007/s10344-011-0563-5.

    Article  Google Scholar 

  56. James MC, Bowman AS, Forbes KJ, Lewis F, McLeod JE, Gilbert L: Environmental determinants of Ixodes ricinus ticks and the incidence of Borrelia burgdorferi sensu lato, the agent of Lyme borreliosis, in Scotland. Parasitology. 2013, 140: 237-246. 10.1017/S003118201200145X.

    CAS  Article  PubMed  Google Scholar 

  57. Cinco M, Floris R, Menardi G, Boemo B, Mignozzi K, Altobelli A: Spatial pattern of risk exposure to pathogens transmitted by Ixodes ricinus in north-eastern Italy and the Italy/Slovenia transborder territory. Int J Med Microbiol. 2008, 298 (S1): 211-217.

    Article  Google Scholar 

  58. Reye AL, Hubschen JM, Sausy A, Muller CP: Prevalence and seasonality of tick-borne pathogens in questing Ixodes ricinus ticks from Luxembourg. Appl Environ Microbiol. 2010, 76: 2923-2931. 10.1128/AEM.03061-09.

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  59. Lommano E, Bertaiola L, Dupasquier C, Gern L: Infections and coinfections of questing Ixodes ricinus ticks by emerging zoonotic pathogens in western Switzerland. Appl Environ Microbiol. 2012, 78: 4606-4612. 10.1128/AEM.07961-11.

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  60. Schicht S, Junge S, Schnieder T, Strube C: Prevalence of Anaplasma phagocytophilum and coinfection with Borrelia burgdorferi senso lato in the hard tick Ixodes ricinus in the city of Hanover (Germany). Vector Borne Zoonotic Dis. 2011, 11: 1595-1597. 10.1089/vbz.2011.0699.

    Article  PubMed  Google Scholar 

  61. Silaghi C, Woll D, Hamel D, Pfister K, Mahling M, Pfeffer M: Babesia spp. and Anaplasma phagocytophilum in questing ticks, ticks parasitizing rodents and the parasitized rodents - analyzing the host-pathogen-vector interface in a metropolitan area. Parasit Vectors. 2012, 5: 191-10.1186/1756-3305-5-191.

    PubMed Central  Article  PubMed  Google Scholar 

  62. Ruiz-Fons F, Fernandez-de-Mera IG, Acevedo P, Gortázar C, de la Fuente J: Factors driving the abundances of Ixodes ricinus ticks and the prevalence of Zoonotic I. ricinus-borne pathogens in natural foci. Appl Environ Microbiol. 2012, 78: 2669-2676. 10.1128/AEM.06564-11.

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  63. Radzijevskaja J, Paulauskas A, Rosef O: Prevalence of Anaplasma phagocytophilum and Babesia divergens in Ixodes ricinus ticks from Lithuania and Norway. Int J Med Microbiol. 2008, 298 (S1): 218-221.

    Article  Google Scholar 

  64. Rosef O, Radzijevskaja J, Paulauskas A, Haslekås C: The prevalence of Anaplasma phagocytophilum in host-seeking Ixodes ricinus ticks in Norway. Clin Microbiol Infec. 2009, 15: 43-45.

    Article  Google Scholar 

  65. Lempereur L, Lebrun M, Cuvelier P, Sepult G, Caron Y, Saegerman C, Shiels B, Losson B: Longitudinal field study on bovine Babesia spp. and Anaplasma phagocytophilum infections during a grazing season in Belgium. Parasitol Res. 2012, 110: 1515-1530.

    Article  Google Scholar 

  66. Blaschitz M, Narodoslavsky-Gföller M, Kanzler M, Walochnik J, Stanek G: Borrelia burgdorferi sensu lato genospecies in questing Ixodes ricinus ticks in Austria. Int J Med Microbiol. 2008, 298 (S1): 168-176.

    Article  Google Scholar 

  67. Jouda F, Perret J-L, Gern L: Ixodes ricinus density, and distribution and prevalence of Borrelia burgdorferi sensu lato infection along an altitudinal gradient. J Med Entomol. 2004, 41: 162-169. 10.1603/0022-2585-41.2.162.

    Article  PubMed  Google Scholar 

  68. Halos L, Bord S, Cotte V, Gasqui P, Abrial D, Barnouin J, Boulouis HJ, Vayssier-Taussat M, Vourc’h G: Ecological factors characterizing the prevalence of bacterial tick-borne pathogens in Ixodes ricinus ticks in pastures and woodlands. Appl Environ Microbiol. 2010, 76: 4413-4420. 10.1128/AEM.00610-10.

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  69. Rizzoli A, Hauffe HC, Carpi G, Vourc’h GI, Neteler M, Rosà R: Lyme borreliosis in Europe. Euro Surveill. 2011, 16: 19906-

    PubMed  Google Scholar 

  70. Mannelli A, Boggiatto G, Grego E, Cinco M, Murgia R, Stefanelli S, De Meneghi D: Acarological risk to exposure to agents of tick-borne zoonoses in the first recognized Italian focus of Lyme borreliosis. Epidemiol Infect. 2003, 131: 1139-1147. 10.1017/S0950268803001328.

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  71. Randolph SE: Tick ecology: processes and patterns behind the epidemiological risk posed by ixodid ticks as vectors. Parasitology. 2004, 129: S37-S65. 10.1017/S0031182004004925.

    Article  PubMed  Google Scholar 

  72. Gylfe A, Bergström S, Lundström J, Olsen B: Epidemiology - reactivation of Borrelia infection in birds. Nature. 2000, 403: 724-725. 10.1038/35001663.

    CAS  Article  PubMed  Google Scholar 

  73. Keesing F, Hersh MH, Tibbetts M, McHenry DJ, Duerr S, Brunner J, Killilea M, LoGiudice K, Schmidt KA, Ostfeld RS: Reservoir competence of vertebrate hosts for Anaplasma phagocytophilum. Emerg Infect Dis. 2012, 18: 2013-2016. 10.3201/eid1812.120919.

    PubMed Central  Article  PubMed  Google Scholar 

  74. Herrmann C, Gern L: Do the level of energy reserves, hydration status and Borrelia infection influence walking by Ixodes ricinus (Acari: Ixodidae) ticks?. Parasitology. 2012, 139: 330-337. 10.1017/S0031182011002095.

    CAS  Article  PubMed  Google Scholar 

  75. Herrmann C, Voordouw MJ, Gern L: Ixodes ricinus ticks infected with the causative agent of Lyme disease, Borrelia burgdorferi sensu lato, have higher energy reserves. Int J Parasitol. 2013, 43: 477-483. 10.1016/j.ijpara.2012.12.010.

    CAS  Article  PubMed  Google Scholar 

  76. Piesman J, Oliver JR, Sinsky RJ: Growth kinetics of the Lyme disease spirochete (Borrelia burgdorferi) in vector ticks (Ixodes dammini). AmJ Trop Med Hyg. 1990, 42: 352-357.

    CAS  Google Scholar 

  77. Herrmann C, Gern L: Survival of Ixodes ricinus (Acari: Ixodidae) under challenging conditions of temperature and humidity is influenced by Borrelia burgdorferi sensu lato infection. J Med Entomol. 2010, 47: 1196-1204. 10.1603/ME10111.

    Article  PubMed  Google Scholar 

  78. Neelakanta G, Sultana H, Fish D, Anderson JF, Fikrig E: Anaplasma phagocytophilum induces Ixodes scapularis ticks to express an antifreeze glycoprotein gene that enhances their survival in the cold. J Clin Invest. 2010, 120: 3179-3190. 10.1172/JCI42868.

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  79. Mannelli A, Bertolotti L, Gern L, Gray J: Ecology of Borrelia burgdorferi sensu lato in Europe: transmission dynamics in multi-host systems. FEMS Microbiol Rev. 2012, 36: 837-861. 10.1111/j.1574-6976.2011.00312.x.

    CAS  Article  PubMed  Google Scholar 

Download references

Acknowledgements

We are grateful for the financial support of the Research Council of Norway (TickDeer project; 203786/E40) and the Directorate for nature management. We would also like to thank Ania Paziewska for her expertise and assistance in the lab.

Author information

Authors and Affiliations

  1. Centre for Ecological and Evolutionary Synthesis (CEES), Department of Biosciences, University of Oslo, P.O. Box1066, Oslo, NO-0316, Norway

    Atle Mysterud, William Ryan Easterday, Lars Qviller & Hildegunn Viljugrein

  2. Norwegian Veterinary Institute, P.O. Box 750, Sentrum, Oslo, NO-0106, Norway

    Hildegunn Viljugrein & Bjørnar Ytrehus

Authors
  1. Atle Mysterud
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. William Ryan Easterday
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Lars Qviller
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hildegunn Viljugrein
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Bjørnar Ytrehus
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Atle Mysterud.

Additional information

Competing interests

The authors affirm that they have no competing interests.

Authors’ contributions

AM, HV and BY designed the study. LQ performed field work. WRE performed laboratory work. AM and HV carried out data analysis. AM drafted the manuscript. All authors read and approved the final version of the manuscript.

Electronic supplementary material

13071_2013_973_MOESM1_ESM.docx

Additional file 1: Table A1: Results from model selection of the prevalence of B. burgdorferi in Sogn & Fjordane, Norway. 1 = variable included in model. AIC = Akaike Information Criterion. ΔAIC = difference in AIC relative to the best model. “Municipality” was fitted as a random term. (DOCX 2 MB)

Authors’ original submitted files for images

Below are the links to the authors’ original submitted files for images.

Authors’ original file for figure 1

Rights and permissions

This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Reprints and Permissions

About this article

Cite this article

Mysterud, A., Easterday, W.R., Qviller, L. et al. Spatial and seasonal variation in the prevalence of Anaplasma phagocytophilum and Borrelia burgdorferi sensu lato in questing Ixodes ricinus ticks in Norway. Parasites Vectors 6, 187 (2013). https://doi.org/10.1186/1756-3305-6-187

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1186/1756-3305-6-187

Keywords

  • Anaplasma
  • Borrelia
  • Dilution effects
  • Host competence hypothesis
  • Ixodes ricinus
  • Lyme Borreliosis Spirochaetes
  • Prevalence
  • Red deer
  • Rodents
  • Ticks

Parasites & Vectors

ISSN: 1756-3305

Contact us