Hans Mejlon

Migratory Passerine Birds as Reservoirs of Lyme Borreliosis in Europe

Birds host vector ticks and Borrelia species and vary in effectiveness as reservoirs.

Geographical distribution, host associations, and vector roles of ticks (Acari: Ixodidae, Argasidae) in Sweden

Abstract This review covers the geographic distribution and host relationships of the tick species in Sweden. Ixodes uriae White, I. caledonicus Nuttall, I. unicavatus Neumann, I. arboricola Schulze & Schlottke, and I. lividus Koch are ornithophagous species. I. trianguliceps Birula, I. canisuga Johnston, I. hexagonus Leach, and Argas vespertilionis (Latreille) are mammalophagous. I. ricinus (L.) and Haemaphysails punctata Canestrini & Fanzago feed on both birds and mammals. All these tick species may be considered to be permanently present in Sweden. I. persulcatus Schulze, Hyalomma marginatum Koch, and the brown dog tick, Rhipicephalus satiguineus (Latreille), may be regarded as not indigenous to Sweden although they may be regularly introduced by spring-migrating birds or imported dogs, respectively. The first European record of the American dog tick, Dermacentor variabilis (Say), is reported. There are several records of Hyalomma aegyptium (L.) from imported tortoises in Sweden. Excluding other ticks imported on exotic pets and zoo animals, another 13 tick species are listed that may occur, at least occasionally, in Sweden. Because of its wide geographic distribution, great abundance, and wide host range, I. ricinus is medically the most important arthropod in northern Europe. I. ricinus is common in southern and south-central Sweden and along the coast of northern Sweden and has been recorded from 29 mammal species, 56 bird species, and two species of lizards in Sweden alone. The potential introduction to Sweden of exotic pathogens with infected ticks (e.g., I. persulcatus and H. marginatum on birds or Dermacentor spp. and R. sanguineus on mammals) is evident.

Migrating Birds and Tickborne Encephalitis Virus

During spring and autumn 2001, we screened 13,260 migrating birds at Ottenby Bird Observatory, Sweden, and found 3.4% were infested with ticks. Four birds, each a different passerine species, carried tickborne encephalitis virus (TBEV)–infected ticks (Ixodes ricinus). Migrating birds may play a role in the geographic dispersal of TBEV-infected ticks.

Dissemination of Spotted Fever Rickettsia Agents in Europe by Migrating Birds

Migratory birds are known to play a role as long-distance vectors for many microorganisms. To investigate whether this is true of rickettsial agents as well, we characterized tick infestation and gathered ticks from 13,260 migratory passerine birds in Sweden. A total of 1127 Ixodes spp. ticks were removed from these birds and the extracted DNA from 957 of them was available for analyses. The DNA was assayed for detection of Rickettsia spp. using real-time PCR, followed by DNA sequencing for species identification. Rickettsia spp. organisms were detected in 108 (11.3%) of the ticks. Rickettsia helvetica, a spotted fever rickettsia associated with human infections, was predominant among the PCR-positive samples. In 9 (0.8%) of the ticks, the partial sequences of 17kDa and ompB genes showed the greatest similarity to Rickettsia monacensis, an etiologic agent of Mediterranean spotted fever-like illness, previously described in southern Europe as well as to the Rickettsia sp.IrITA3 strain. For 15 (1.4%) of the ticks, the 17kDa, ompB, gltA and ompA genes showed the greatest similarity to Rickettsia sp. strain Davousti, Rickettsia japonica and Rickettsia heilongjiangensis, all closely phylogenetically related, the former previously found in Amblyomma tholloni ticks in Africa and previously not detected in Ixodes spp. ticks. The infestation prevalence of ticks infected with rickettsial organisms was four times higher among ground foraging birds than among other bird species, but the two groups were equally competent in transmitting Rickettsia species. The birds did not seem to serve as reservoir hosts for Rickettsia spp., but in one case it seems likely that the bird was rickettsiemic and that the ticks had acquired the bacteria from the blood of the bird. In conclusion, migratory passerine birds host epidemiologically important vector ticks and Rickettsia species and contribute to the geographic distribution of spotted fever rickettsial agents and their diseases.

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.

Questing behaviour of Ixodes ricinus ticks (Acari: Ixodidae)

The vertical distribution in the vegetation of questing Ixodes ricinus ticks was investigated in two different vegetation types (‘high’ and ‘low’ vegetation) at two localities in south-central Sweden during 1992-1993 (Toro) and 1995 (Bogesund). Significant correlations were found between the vertical distribution of immature ticks and the height of the vegetation. The greatest mean availabilities of the larvae and nymphs in low vegetation were in the intervals 0-9 and 30-39 cm, respectively. The larval numbers were greatest close to the ground (0-29 cm) in both high and low vegetation. The larval : nymphal ratio, at ground level at localities free of ground vegetation, varied between 8 : 1 and 32 : 1. In high vegetation, the greatest mean numbers of nymphal and adult ticks were at height intervals of 50-59 and 60-79 cm, respectively. These ranges are within the estimated height interval (40-100 cm) of the main part of the body surface of their ‘preferred’ host, the roe deer (Capreolus capreolus). The presence of most questing I. ricinus larvae at ground level would favour the transmission of Borrelia burgdorferi s.l., since this is where the highly reservoir-competent rodents and shrews usually occur.

Seasonal prevalence of Borrelia burgdorferi in Ixodes ricinus in different vegetation types in Sweden

The aim of this investigation was to estimate the seasonal risk of contracting human Lyme disease in different vegetation types in southern Sweden. Host-seeking Ixodes ricinus ticks (Acari: Ixodidae) were collected with standardized methods during May-September 1988 and March-October 1989 at 10 different sampling sites. Tick abundance was greatest during May-June and August-September. Prevalence of Borrelia burgdorferi infection of the ticks was assessed by phase-contrast microscopy complemented by immunology. Spirochetal infection of tick larvae was not detected. The prevalence of infection among nymphal ticks differed significantly between years and between sampling sites. Infection prevalence was greater in adult females than in nymphs, but was similar in female and male ticks. Among all vegetation types studied, the greatest Lyme disease risk was deemed to be from I. ricinus nymphs during May and September in mixed forest vegetation.

Prevalence of Borrelia burgdorferi sensu lato infection in Ixodes ricinus in Sweden

Between 1988-1991, a total of 3,141 Ixodes ricinus ticks, 2,740 adults and 401 nymphs, was collected from different localities in 23 of the 25 provinces of Sweden. The ticks were identified, dissected and examined for the presence of Borrelia spirochetes. Indirect immunofluorescence was performed, using an antiserum obtained from rabbits, immunized with sonicated, whole Borrelia burgdorferi spirochetes isolated from Swedish Ixodes ricinus ticks. Borrelia-positive I. ricinus were found in all 23 provinces. The prevalence of infection in adults ranged from 3% in Jämtland to 23% in Södermanland. In nymphs, the infection prevalence ranged from 0% in 9 provinces to 15% in Södermanland. A significantly greater proportion of the adult ticks were found to be positive for Borrelia in the southern and central parts of Sweden as compared to the northern part (Norrland). No significant difference in prevalence could be demonstrated between the western and eastern parts of Sweden. On average, 10% of the nymphs and 15% of the adult I. ricinus were positive for Borrelia. Of 41 non-I. ricinus ticks, none was positive for Borrelia. This study shows that Borrelia burgdorferi sensu lato is present throughout the distributional area of I. ricinus in Sweden. This should lead to increased awareness of signs and symptoms compatible with Lyme borreliosis in persons living in or visiting areas where I. ricinus is present.

Diel activity of Ixodes ricinus Acari:ixodidae at two locations near Stockholm, Sweden.

The diel ‘activity’, i.e. availability, of Ixodes ricinus larvae, nymphs and adults was investigated in a meadow and a forest habitat near Stockholm during 1991–1993. Generally, the immature ticks were more prevalent in the forest than in the meadow. In the meadow, the mean larval and adult numbers varied significantly between 4 h time intervals with the peak activity from 2300 to 0300 h. In the forest, the tick numbers did not differ significantly between the time intervals. The association of the tick activity with certain meteorological variables was strongest in the meadow, where the mean numbers of all tick stages were negatively correlated with the temperature. The relative humidity was positively correlated only with the mean numbers of larvae. In contrast, the larval activity in the forest was positively and negatively correlated with the temperature and relative humidity, respectively, while the nymphal and adult activity showed no association with these climatic variables. The impact of the host activity on the tick diel activity is also discussed.

Evaluation of host‐targeted applications of permethrin for control of Borrelia‐infected Ixodes ricinus (Acari: Ixodidae)

Evaluation of host-targeted applications of permethrin for control of Borrelia-infected Ixodes ricinus (Acari: Ixodidae)