Longitudinal surveillance of the tick Ixodes ricinus for borreliae

Host-seeking Ixodes ricinus (L.) (Acari: Ixodidae) were monitored for borreliae (Borrelia burgdorferi s.l.) using dark-field microscopy in South Moravia (Czech Republic) each May from 1991 to 2001 (150 nymphs, 100 females and 100 males each year). This survey revealed a mean annual percentage of infected ticks of 16.8% (range, 11.7-24.2) in nymphs, 24.9% (range, 16.5-33.6) in females and 26.1% (range, 17.1-37.3) in males. Annual incidence of Lyme borreliosis in humans of the area in the same period (range, 8.7-41.7 per 100,000) correlated significantly with the frequency (number of ticks per flag per hour) of nymphs infected with >50 borreliae or all nymphal ticks, but not with the frequency of females, infected females or the infection rate (% of ticks infected) of either nymphal or female ticks. A prediction of the annual incidence of Lyme borreliosis, based on the frequency of heavily infected or all nymphal I. ricinus ticks, is feasible. The infection rate in I. ricinus correlated significantly with the North Atlantic Oscillation winter index of the last year (in nymphs) or of the year before last (in adults).     

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.     

Borrelia burgdorferi infection in Ixodes ricinus from habitats in Denmark

A total of 2647 ticks of the genus Ixodes was sampled by flagging the vegetation in thirty-one sites in eastern Jutland, Denmark. All ticks were identified as Ixodes ricinus Linnaeus. A total of 317 ticks (202 nymphs and 115 adults) from three different sites were examined for the spirochaete Borrelia burgdorferi Johnson et al. by indirect fluorescent antibody staining; the frequency of infection varied from 7% to 22%. It is concluded that I. ricinus, known to be the most common tick in Denmark, is the vector largely responsible for the transmission of B. burgdorferi in this country.     

Borreliae in Ixodes ricinus ticks feeding on humans

A total of 298 Ixodes ricinus (L.) ticks (Acari: Ixodidae) feeding on humans in the Czech Republic were tested for borreliae (Borrelia burgdorferi sensu lato) by darkfield microscopy between 1997 and 2003. A majority (68%) of the supplied I. ricinus ticks were nymphs, 25% were females and 7% were larvae. Overall, 20% of 74 examined females and 9% of 203 examined nymphs (but none of 21 examined larvae) were infected with borreliae. The proportion of ticks with a high infection load (>100 spirochetes) was 4% in females and 2% in nymphal I. ricinus. During the year, the highest numbers and proportions of infected nymphal and female ticks were taken from humans in June. Detection of borreliae in the ticks feeding on humans might be helpful in the prophylaxis of Lyme borreliosis.     

Borrelia burgdorferi sensu lato and co‐infections with Anaplasma phagocytophilum and Rickettsia spp. in Ixodes ricinus in Hamburg,Germany

To obtain initial data on Borrelia burgdorferi sensu lato (Spirochaetales: Spirochaetaceae) in Ixodes ricinus (Ixodida: Ixodidae) ticks in Hamburg, Germany, 1400 questing ticks were collected by flagging at 10 different public recreation areas in 2011 and analysed using probe‐based quantitative real‐time polymerase chain reaction. The overall rate of infection with B. burgdorferi s.l. was 34.1%; 30.0% of adults were infected (36.7% of females and 26.0% of males), as were 34.5% of nymphs. Significant differences in tick infection rates were observed between the spring and summer/autumn months, as well as among sampling locations. Borrelia genospecies identification by reverse line blotting was successful in 43.6% of positive tick samples. The most frequent genospecies was Borrelia garinii/Borrelia bavariensis, followed by Borrelia afzelii, Borrelia valaisiana, B. burgdorferi sensu stricto, Borrelia spielmanii, Borrelia bissettii and Borrelia lusitaniae. Based on previously published data, co‐infection of Borrelia and Rickettsiales spp. was determined in 25.8% of ticks. Overall, 22.9% of ticks were co‐infected with Rickettsia spp. (Rickettsiales: Rickettsiaceae), 1.7% with Anaplasma phagocytophilum (Rickettsiales: Anaplasmataceae), and 1.2% with both pathogens. Study results show a high prevalence of Borrelia‐positive ticks in recreation areas in the northern German city of Hamburg and the potential health risk to humans in these areas should not be underestimated.     

Sex-biased genetic structure in the vector of Lyme disease,Ixodes ricinus

Abstract.— We analyzed 725 Ixodes ricinus ticks (the principal vector of Lyme disease in Europe) collected in Switzerland in 1995 and 1996 (three and eight samples, respectively) and in Tunisia in 1996 (one sample) with five microsatellite markers. We found highly significant genetic differentiation between Swiss and Tunisian samples but detected almost no differentiation within Switzerland, even between those samples separated by the Alps. Interestingly, we found that I. ricinus females were more genetically related to one another than were males at a local scale, which would indicate a higher dispersal rate of immature males. Possible explanations for these findings in terms of sex-specific association of ticks with certain hosts (e.g., birds) and their epidemiological consequences are discussed.     

Effect of forest clearing on the abundance of Ixodes ricinus ticks and the prevalence of Borrelia burgdorferi s.l

Questing Ixodes ricinus L. (Acari: Ixodidae) ticks were collected on a forest trail that had been completely cleared of shrubs and ground vegetation in winter 2002 and on a nearby control uncleared forest transect in South Moravia (Czech Republic). Samples were collected each May in 2003, 2004 and 2005. Nymphal ticks were 3.4 times, 1.9 times and 1.2 times less frequent on cleared forest than on uncleared forest trails in the three respective years, whereas adult tick abundance was 27.2 times, 4.0 times and 2.2 times lower, respectively. The ticks were examined for borreliae by dark-field microscopy: prevalence of nymphal ticks infected with Borrelia burgdorferi sensu lato (12.6% to 20.0%) did not differ significantly between the cleared and uncleared trail during the 3 years. In conclusion, the habitat modification appeared to result in a decreased abundance of I. ricinus as well as a reduced frequency of infected ticks (and thus indirectly a lower potential risk of Lyme borreliosis), which lasted, however, for only 2 years. Eight cultures of borreliae isolated from the ticks were all identified as the 'ornithophilic' genomic species Borrelia garinii, possibly indicating a greater role of forest birds than that of forest rodents as the hosts of immature I. ricinus in the tick (and borrelial) colonization of the cleared part of the forest.     

Tick infection rates with Borrelia Ixodes ricinus versus Haemaphysalis concinna and Dermacentor reticulatus in two locations in eastern Germany

Unfed nymphal Ixodes ricinus, Haemaphysalis concinna, and adult Dermacentor reticulatus were collected in two locations of Saxony in July and September 1991 by flagging. In July, the abundance of nymphal I. ricinus was about 2-3 times higher than that of nymphal H. concinna, a time of the year when nymphs of both species are reported to have a seasonal peak of activity. No D. reticulatus were flagged concurrently. In September, host-seeking activity of nymphal I. ricinus was again quite high as was that of adult D. reticulatus but only low numbers of nymphal H. concinna were collected. The flagged ticks were individually examined for Borrelia by an indirect immunofluorescence assay (I. ricinus: n = 414; H. concinna: n = 96; D. reticulatus: n = 116). The prevalence of Borrelia (probably B. burgdorferi) in I. ricinus varied from 12.1% to 21.0%. No borreliae were found in H. concinna. Of the examined D. reticulatus from one site (n = 97) 11.3% contained either B. burgdorferi or a related Borrelia. This may be the first finding of Borrelia in an Eurasian Dermacentor species.     

Density of deer in relation to the prevalence of Borrelia burgdorferi s.1. in Ixodes ricinus nymphs in Rambouillet forest, France

The Rambouillet Forest, a Lyme disease-endemic area near Paris, France, was surveyed from September 1994 to October 1995 to determine the risk periods and zones for humans. Firstly, during the period of Ixodes ricinus activity, abundance of nymphs is greater in spring than in autumn. Secondly, we observed significant variation in nymphal abundance between zones according to the density of cervids. The polymerase chain reaction (PCR) was used to detect DNA of Borrelia burgdorferi sensu lato in 461 unfed nymphs. DNA was detected in 38 nymphs (8.2%). By genospecific PCR based on the OspA gene, we detected the three pathogenic spirochetes with occurrences of 10.3, 31.1 and 58.6 for B. burgdorferi s.s., Borrelia garinii and Borrelia afzelii, respectively, indicating that B. afzelii is probably the main Borrelia species in the Rambouillet Forest. Finally, 11.5% of positive nymphs exhibited a double infection. Infection rates of I. ricinus nymphs by B. burgdorferi s.l. were not significantly different throughout the year for a given area, indicating that the risk periods of acquiring Lyme disease are mainly linked to nymph activity and correspond to spring and autumn. Likewise infection rates of nymphs were not significantly different between zones with a high density of deer (more than 100 animals per 100 ha) and zones with lower deer density (less than 20 animals per 100 ha). In addition to the role of deer as an amplifier of tick populations, these data indicate that zones with a high density of cervids should be considered as higher risk areas. © Rapid Science Ltd. 1998     

Ixodes (Pholeoixodes) hexagonus, an efficient vector of Borrelia burgdorferi in the laboratory

Borrelia burgdorferi Johnson et al. was first isolated from the midgut of Ixodes dammini Spielman et al. in the U.S.A. and from the midgut of I.ricinus (L.) in Europe. I.ricinus was considered to be the only tick vector of this borrelia, in Europe, until I.hexagonus Leach, the hedgehog tick, was found to harbour spirochaetes. This paper reports an evaluation of the vector competence of I.hexagonus for the spirochaete B.burgdorferi. Transovarial and trans-stadial survival were demonstrated and the spirochaete was transmitted to laboratory mice via the bites of trans-stadially infected I.hexagonus females.     

Problems of isolating Borrelia burgdorferi from ticks collected in United Kingdom foci of Lyme disease

Abstract. Many isolates of Borrelia burgdorferi have been obtained from ticks and vertebrate tissues collected in North America and continental Europe but only one established culture of United Kingdom Borrelia burgdorferi has been recorded. In this paper we report the isolation of B.burgdorferi from one of 108 tick pools representing 733 ticks and eighty-four tissue samples from twenty-six rodents collected in the U.K., and the subsequent failure to establish the isolate (from ticks collected in Fordingbridge) in culture. In contrast, using identical techniques and culture medium, B.burgdorferi was isolated from one of seven tick pools collected in Switzerland, and from a single pool of ticks collected in Slovakia, and both isolates were successfully passaged. Analysis of questing I.ricinus collected from Fordingbridge by direct immunofluorescence showed 6/32 (19%) of adults and 8/108 (7%) of nymphs were positive for B. burgdorferi , although only one nymph contained ≥ 1000 spirochaetes. To examine further the problem of isolating U.K. B.burgdorferi , twelve Ixodes ricinus tick samples from Fordingbridge, a recognized focus of Lyme disease, were subjected to isolation and culturing techniques, and the procedures monitored by use of the polymerase chain reaction (PCR). Whereas 11/12 samples were PCR positive after 2 weeks in culture, only one was PCR positive after 4 weeks. Motile spirochaetes were not visible by dark-field microscopy in any of the cultures. The results indicate that the standard BSK II medium routinely used to isolate and culture B. burgdorferi does not readily support the replication of the Borrelia species endemic to the U.K.     

Borrelia Burgdorferi Sensu Lato in Ixodes Ricinus Ticks and Rodents in a Recreational Park in South-Western Ireland

Ixodes ricinus ticks infected with Borrelia burgdorferi sensu lato were numerous on the edges of paths and roads in a recreational park in south-western Ireland. The abundance of ticks at different sites was related to the presence of deer, but a negative relationship was shown between tick abundance and tick infection rates. This is thought to be due to the deposition of large numbers of uninfected ticks by deer, which are apparently not good reservoir hosts of B. burgdorferi s.l. Blood meal analysis only detected deer DNA in uninfected nymphs. Reservoir competent rodents, Apodemus sylvaticus and Clethrionomys glareolus, were abundant at all sites and a high proportion of captured specimens were infested with larval ticks. However, very few rodents were infected with B. burgdorferi s.l. and none of the unfed infected nymphs analysed for the identity of their larval blood meal had fed on rodents. The spirochaetes detected in I. ricinus in the study area may be poorly adapted to rodents or are not transmitted readily because of the absence of nymphal infestation. The majority of spirochaetes in these ticks were apparently acquired from non-rodent hosts, such as birds.     

First report of Anaplasma phagocytophilum and its co-infections with Borrelia burgdorferi sensu lato in Ixodes ricinus ticks (Acari: Ixodidae) from Republic of Moldova

We examined 198 questing Ixodes ricinus ticks collected in Chisinau City, Republic of Moldova by PCR assays for Anaplasma phagocytophilum, Borrelia burgdorferi sensu lato and co-infection of both pathogens, which were detected in 9%, 25.2% and 2.5% of tested ticks, respectively. B. burgdorferi s.l. genotyping revealed the presence of five genospecies with dominance of B. garinii. Our preliminary study provides evidence about occurrence of both pathogens in this populated area, which represent a potential health risk for inhabitants.     

Phenology of the tick, Ixodes ricinus, in its southern distribution range (central Spain)

The abundance, seasonal activity patterns and development rates of the tick Ixodes ricinus (L.) (Acari: Ixodidae), as well as microclimate features of the site of study, are described for a 9-year-long study (1994-2002) in north-central Spain. According to drag captures, larvae had a unimodal activity pattern, with a maximum observed around July-August, whereas nymphs displayed a bimodal pattern (May-June and August-September) with strong dominance of spring activity. An inversion of this pattern, with larger autumn peak, was observed in years with humid summers. Adults showed a small spring peak and a large autumn one. In the later years of the study, a small increase in the adult spring peak of activity was noticed, correlated with mild winters. Over the entire period of study, a clear increase in the total tick abundance was detected. Statistically significant differences between years were observed for some climate variables (saturation deficit, winter temperatures and number of days with temperatures above 6 degrees C), but a consistent and constant pattern of change was not observed in any climate variable. Temperature requirements for developing stages showed a sharp decrease in weeks 35-51 (eggs) and 38-50 (larvae and nymphs), a feature attributed to the presence of the morphogenetic diapause, beginning around September. Development rates obtained under quasi-natural conditions were almost twice those reported for other sites, suggesting an adaptation of this local, largely isolated I. ricinus population. According to drag captures and field-obtained development rates, interchange of nymphs between the two cohorts is common in this site, and seems to be influenced by the winter temperature and the date of larval engorgement.     

Detection of Lyme disease spirochete,Borrelia burgdorferi sensu lato,including three novel genotypes in ticks (Acari: Ixodidae) collected from songbirds (Passeriformes) across Canada

Lyme disease is reported across Canada, but pinpointing the source of infection has been problematic. In this three‐year, bird‐tick‐pathogen study (2004–2006), 366 ticks representing 12 species were collected from 151 songbirds (31 passerine species/subspecies) at 16 locations Canada‐wide. Of the 167 ticks/pools tested, 19 (11.4%) were infected with Borrelia burgdorferi sensu lato (s.l.). Sequencing of the rrf‐rrl intergenic spacer gene revealed four Borrelia genotypes: B. burgdorferi sensu stricto (s.s.) and three novel genotypes (BC genotype 1, BC genotype 2, BC genotype 3). All four genotypes were detected in spirochete‐infected Ixodes auritulus (females, nymphs, larvae) suggesting this tick species is a vector for B. burgdorferi s.l. We provide first‐time records for: ticks in the Yukon (north of 60° latitude), northernmost collection of Amblyomma americanum in North America, and Amblyomma imitator in Canada. First reports of bird‐derived ticks infected with B. burgdorferi s.l. include: live culture of spirochetes from Ixodes pacificus (nymph) plus detection in I. auritulus nymphs, Ixodes scapularis in New Brunswick, and an I. scapularis larva in Canada. We provide the first account of B. burgdorferi s. l. in an Ixodes muris tick collected from a songbird anywhere. Congruent with previous data for the American Robin, we suggest that the Common Yellowthroat, Golden‐crowned Sparrow, Song Sparrow, and Swainson's Thrush are reservoir‐competent hosts. Song Sparrows, the predominant hosts, were parasitized by I. auritulus harboring all four Borrelia genotypes. Our results show that songbirds import B. burgdorferi s.l.‐infected ticks into Canada. Bird‐feeding I. scapularis subadults were infected with Lyme spirochetes during both spring and fall migration in eastern Canada. Because songbirds disperse millions of infected ticks across Canada, people and domestic animals contract Lyme disease outside of the known and expected range.     

Mosaic Pattern of Borrelia Infection in a Continuous Population of the Tick Ixodes Ricinus (Acari: Ixodidae)

An array of 12 20 × 20 m quadrats in a mixed forest near Poteply, Central Bohemia, Czech Republic, was investigated for the abundance and spatial distribution of host-questing Ixodes ricinus nymphs and their infection with borreliae. Tick densities were estimated by flagging and their borrelia infection status was determined by direct immunofluorescence. While the tick population appeared to be continuous and homogeneous based on quadrat counts, their infection with borreliae evinced a mosaic pattern. The nymphal infection rates ranged between 1.6 and 10.5% (mean = 6.0%) with significant differences between adjacent quadrats. Home ranging of small rodents (Apodemus flavicollis and Clethrionomys glareolus) inhabiting the forest seems to be responsible for the spatial pattern of borrelial infection.     

Risk factors in habitats of the tick Ixodes ricinus influencing human exposure to Ehrlichia phagocytophila bacteria

Ixodes ricinus L. (Acari: Ixodida) were sampled during 1996-99 in southern Scotland, on vegetation using cloth drags, on humans by removal from clothing and on roe deer (Capreolus capreolus L.) by searching legs of culled deer. Developmental microclimate was recorded by automatic recorders and questing microclimate by portable instruments during tick collections. Ticks and deer were examined for infection with Ehrlichia phagocytophila bacteria (Rickettsiales) using microscopy and polymerase chain reaction. This pathogen causes tick-borne fever of sheep in Europe and human granulocytic ehrlichiosis in North America, but in Europe human clinical ehrlichiosis due to E. phagocytophila has not been recorded despite serological evidence of exposure. Among three types of habitat, coniferous woodland was most infested with questing ticks (560 ticks/km of drag; mean numbers collected on long trousers: 24.3 larvae, 13.5 nymphs and 0.8 adult ticks/km walked), deciduous woodland had slightly lower infestation (426 ticks/km drag) and upland sheep pasture had much lower infestation (220 ticks/km drag). Of the three main vegetation types, bracken was least infested (360 ticks/km drag), ericas most (430 ticks/km drag) and grassland had intermediate infestation density (413 ticks/km drag). Questing and developmental microclimates were poor predictors of exposure within these habitats, except lower infestation of pastures was attributed to greater illumination there. Collectors who walked a total of 300 km through all habitats (taking 360 h in all seasons), wearing cotton trousers hanging outside rubber boots, were bitten by only four nymphs and 11 larvae of I. ricinus (but no adult ticks). There was a negative correlation between densities of deer and ticks collected, although presence of deer remains a major indicator of exposure. The proportion of infected ticks was fairly uniform at four sites studied. Overall prevalence of E. phagocytophila in I. ricinus was 3.3% in nymphs (40/1203) but only approximately 1.5% in adults of both sexes (although males do not bite). It was estimated that nymphs of I. ricinus gave 4.4% probability of one infected bite/person/year (for occupational exposure during this research) due to presence in all seasons and habitats, their human biting rate of 0.011 nymphs/h or 0.013 nymphs/km and widespread infection with E. phagocytophila. The frequency distribution of intensity of infection in ticks was approximately normal (mean 98 morulae/nymph infected), thus there is a high risk of receiving a high dose from any one infected tick bite.     

Acquired resistance in dogs to repeated infestation with Ixodes scapularis (Acari: Ixodidae) reduces tick viability and reproductive success

The purpose of this study was to determine whether dogs develop acquired resistance to adult Ixodes scapularis infestation in an experimental model. Five dogs were each infested with ten mating pairs of ticks every week for 7 consecutive weeks, another five dogs were each infested with ten mating pairs once every 2 weeks for 10 weeks and four dogs served as controls not exposed to ticks. All ticks were allowed to feed to repletion and were collected only after dropping from the host. Several variables were measured to determine the extent of blood feeding success. Regression analysis indicated that the engorgement success, survival and mean tick engorgement weight declined with repeated infestation in both groups of dogs (p<0.05). Tick oviposition as well as the F1 viability declined with each successive infestation in both groups. These results suggest that repeated infestation with I. scapularis elicits a protective immune response against tick feeding and could serve as a limiting factor in the spread and transmission of Borrelia burgdorferi.     

Mapping and monitoring tick (Acari,Ixodida) distribution,seasonality, and host associations in the United Kingdom between 2017 and 2020

Tick-borne disease risk is intrinsically linked to the distribution of tick vector species. To assess risk and anticipate disease emergence, an understanding of tick distribution, host associations, and seasonality is needed. This can be achieved, to some extent, using passive surveillance supported by engagement with the public, animal health, and public health experts. The Tick Surveillance Scheme (TSS) collects data and maps tick distribution across the United Kingdom (UK). Between 2017 and 2020, 3720 tick records were received and 39 tick species were detected. Most records were acquired in the UK, with a subset associated with recent overseas travel. The dominant UK acquired species was Ixodes ricinus (Ixodida: Ixodidae, Linnaeus), the main vector of Lyme borreliosis. Records peaked during May and June, highlighting a key risk period for tick bites. Other key UK species were detected, including Dermacentor reticulatus (Ixodida: Ixodidae, Fabricius) and Haemaphysalis punctata (Ixodida: Ixodidae, Canestrini & Fanzago) as well as several rarer species that may present novel tick-borne disease risk to humans and other animals. Updated tick distribution maps highlight areas in the UK where tick exposure has occurred. There is evidence of increasing human tick exposure over time, including during the COVID-19 pandemic, but seasonal patterns remain unchanged.