The role of the sand lizard (Lacerta agilis) in the transmission cycle of Borrelia burgdorferi sensu lato

Abstract

In order to examine the role of Lacerta agilis in the transmission cycle of Borrelia burgdorferi sensu lato, lizards were captured in three different localities in Slovakia, Poland, and Romania. Skin biopsy specimens from collar scales and ticks feeding on the lizards at the time of capture were collected. In total, 87 individuals (11 in Slovakia, 48 in Poland, 28 in Romania) of L. agilis were captured. Altogether, 245 (74, 74, 97) larvae and 191 (78, 113, 0) nymphs were removed from captured lizards. Borrelial infection was detected by PCR amplifying a fragment of the 5S–23S rDNA intergenic spacer and genotyping by restriction fragment length polymorphism (RFLP). When examining the presence of borreliae in biopsy specimens, striking differences between separate populations were observed. Whilst none of the biopsy specimens from L. agilis from Poland were positive for B. burgdorferi s.l., 45% of the sand lizards from Slovakia and 57% from Romania were positive. B. lusitaniae was confirmed in all positive biopsy specimens. The prevalence of borreliae in ticks that had fed on lizards was 6% in Poland, 21% in Slovakia, and 13% in Romania. While B. lusitaniae was the only genospecies in ticks from Slovakia (except for 2 larvae infected with B. afzelii) and Romania, it represented 64% and B. valaisiana 27% of the borrelia infections in ticks from lizards captured in Poland. The highest probability of ticks to get infected expressed as specific infectivity of lizards was recorded in Slovakia (0.102) and the lowest in Poland (0.003). Our findings underline the importance of the sand lizard in the transmission cycle of B. lusitaniae.

Introduction

Lyme borreliosis (LB) is the most widespread vector-borne disease in the northern hemisphere. The causative agents of LB are spirochetes from the Borrelia burgdorferi sensu lato (s.l.) complex which currently comprises at least 12 genospecies. The main European vector of LB is Ixodes ricinus, the most common tick in Europe. Currently, B. burgdorferi s.s., B. garinii, B. afzelii, and B. spielmanii are clearly established as pathogenic to humans (van Dam et al., 1993; Wang et al., 1999; Földvári et al., 2005). B. valaisiana and B. lusitaniae previously considered as non-pathogenic might cause disease as well (Collares-Pereira et al., 2004; Diza et al., 2004). The geographic distribution of B. burgdorferi s.l. genospecies in Europe is very variable and can vary even in relatively small areas as well as over time in a given area (Derdáková and Lenčáková, 2005). In endemic areas of Europe, at least 6 Borrelia genospecies may circulate between vertebrate hosts and ticks. B. afzelii and B. garinii are the most frequent and the most widely distributed genospecies and occur over the whole of Europe (Hubálek and Halouzka, 1997) followed by B. valaisiana and B. burgdorferi s.s. (Derdáková et al., 2003). B. spielmanii and B. lusitaniae belong to the less abundant genospecies in Europe. Records of B. spielmanii in I. ricinus, in reservoir hosts, and in human patients come from the Netherlands (Wang et al., 1999), the Czech Republic (Derdáková et al., 2003), Germany (Richter et al., 2004), and Hungary (Földvári et al., 2005). The prevalence of B. lusitaniae varies in different parts of Europe. While in the Mediterranean basin it represents the dominant or the only genospecies present in I. ricinus ticks, reports from other parts of Europe are rather rare (Postic et al., 1997; Gern et al., 1999; De Michelis et al., 2000; Younsi et al., 2001; Sarih et al., 2003; Wodecka and Skotarczak, 2005; Poupon et al., 2006; Amore et al., 2007). Particular Borrelia genospecies differ in their transmission cycles with different vertebrate taxons as reservoir hosts. Birds are competent reservoir hosts of B. garinii and B. valaisiana (Humair et al., 1998; Hanincová et al., 2003b). Rodents serve as reservoir hosts for B. afzelii (Humair et al., 1999; Hanincová et al., 2003a) and B. garinii belonging to the OspA type 4 (Postic et al., 1997). The newly described genospecies B. spielmanii is maintained in natural foci by the edible dormouse (Eliomys quercinus) and the fat dormouse (Glis glis) (Matuschka et al., 1994; Richter et al., 2004). Several lizard species were proved to possess a complement with borreliacidal activity (Lane and Loye, 1989; Wright et al., 1998), and therefore the role of lizards in the circulation of B. burgdorferi s.l. has been underestimated. Recent studies suggest associations of lizards with B. lusitaniae circulation. The reservoir competence of Psammodromus algirus was proven recently (Dsouli et al., 2006). B. lusitaniae was detected in skin biopsy specimens and blood samples and in larvae and nymphs of I. ricinus removed from green lizards (Lacerta viridis) (Majláthová et al., 2006) and wall lizards (Podarcis muralis) (Amore et al., 2007). Richter and Matuschka (2006) detected a high prevalence of B. lusitaniae in ticks feeding on L. agilis and Podarcis muralis.

The aim of this study was to demonstrate that the sand lizard (L. agilis) contributes to the maintenance cycle of B. burgdorferi s.l. and to compare 3 distinct populations of L. agilis in Europe.