Prevalence of Borrelia burgdorferi sensu lato genospecies in Ixodes ricinus ticks in Europe: a metaanalysis

Abstract

In Europe, Borrelia burgdorferi genospecies causing Lyme borreliosis are mainly transmitted by the tick Ixodes ricinus. Since its discovery, B. burgdorferi has been the subject of many epidemiological studies to determine its prevalence and the distribution of the different genospecies in ticks. In the current study we systematically reviewed the literature on epidemiological studies of I. ricinus ticks infected with B. burgdorferi sensu lato. A total of 1,186 abstracts in English published from 1984 to 2003 were identified by a PubMed keyword search and from the compiled article references. A multistep filter process was used to select relevant articles; 110 articles from 24 countries contained data on the rates of infection of I. ricinus with Borrelia in Europe (112,579 ticks), and 44 articles from 21 countries included species-specific analyses (3,273 positive ticks). These data were used to evaluate the overall rate of infection of I. ricinus with Borrelia genospecies, regional distributions within Europe, and changes over time, as well as the influence of different detection methods on the infection rate. While the infection rate was significantly higher in adults (18.6%) than in nymphs (10.1%), no effect of detection method, tick gender, or collection period (1986 to 1993 versus 1994 to 2002) was found. The highest rates of infection of I. ricinus were found in countries in central Europe. B. afzelii and B. garinii are the most common Borrelia species, but the distribution of genospecies seems to vary in different regions in Europe. The most frequent coinfection by Borrelia species was found for B. garinii and B. valaisiana.

FIG. 1.

Regression of mean rates of infection of Borrelia in nymphs and adults. Only studies in which both nymphs and adults and at least 100 individuals of each stage were examined were included. Each data point represents one record.

FIG. 2.

Influence of detection method on infection rates. DFM, dark-field microscopy; IFA, immunofluorescence assay.

FIG. 3.

Regression analysis of the mean rates of infection in adults with the corresponding longitude (P < 0.05; r² = 0.102) (a) or latitude (P > 0.05; r² = 0.031) (b).

FIG. 4.

(a) Map of the defined regions. Areas with low infection rates (nymphs, ≤11%; adults, ≤20%) are indicated by light gray; areas with higher infection rates are indicated by dark gray. (b) Regions and means of the rates of infection of nymphs (Inf. N) and adults (Inf. A). The number of records used for every region is indicated. A section sign indicates that the infection rates were extremely high (>30%).

FIG. 5.

Comparison of rates of infection of nymphs and adults in two collecting periods. Each data point represents one record. To obtain a similar proportion of areas with high and low infection rates in both periods, data for extremely high infection rates (>30%) were excluded. n.s., not significant.

FIG. 6.

Overall ratio of the Borrelia species B. afzelii (B.a.), B. garinii (B.g.), B. burgdorferi sensu stricto (B.b.), B. valaisiana (B.v.), and B. lusitaniae (B.l.) in I. ricinus ticks in Europe. Fifty records with 3,273 positive ticks were included. The percentages of positive ticks per species for every single study are given. n.t., nontypeable; n.s., not significant; one asterisk, P < 0.05; two asterisks, P < 0.01; three asterisks, P < 0.001.

FIG. 7.

Distribution of the Borrelia genospecies B. afzelii (B.a.), B. garinii (B.g.), B. burgdorferi sensu stricto (B.b.), B. valaisiana (B.v.), and B. lusitaniae (B.l.) and nontypeable Borrelia (n.t.) in nymphs (N) and adults (A). The average of the percentages of positive ticks per species for every single study is given. The numbers of infected ticks examined are indicated above the bars, and the numbers of records are indicated in parentheses.

FIG. 8.

Distribution of mixed infections in ticks. Only records in which B. afzelii (Ba), B. garinii (Bg), B. burgdorferi sensu stricto (Bb), and B. valaisiana (Bv) were examined were included (21 records). The average of the percentages of positive ticks per species combination for every single study is given. Three asterisks, P < 0.001.