This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Poupon, M.-A.
Right arrow Articles by Gern, L.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Poupon, M.-A.
Right arrow Articles by Gern, L.
Agricola
Right arrow Articles by Poupon, M.-A.
Right arrow Articles by Gern, L.

 Previous Article  |  Next Article 

Applied and Environmental Microbiology, January 2006, p. 976-979, Vol. 72, No. 1
0099-2240/06/$08.00+0     doi:10.1128/AEM.72.1.976-979.2006
Copyright © 2006, American Society for Microbiology. All Rights Reserved.

Prevalence of Borrelia burgdorferi Sensu Lato in Ticks Collected from Migratory Birds in Switzerland

Marie-Angèle Poupon,1 Elena Lommano,1 Pierre-François Humair,1 Véronique Douet,1 Olivier Rais,1 Michael Schaad,2 Lukas Jenni,2 and Lise Gern1*

Institute of Zoology, University of Neuchâtel, Neuchâtel, Switzerland,1 Swiss Ornithological Institute, Sempach, Switzerland2

Received 27 May 2005/ Accepted 22 September 2005


arrow
ABSTRACT
 
The prevalence of ticks infected by Borrelia burgdorferi sensu lato on birds during their migrations was studied in Switzerland. A total of 1,270 birds captured at two sites were examined for tick infestation. Ixodes ricinus was the dominant tick species. Prevalences of tick infestation were 6% and 18.2% for birds migrating northward and southward, respectively. Borrelia valaisiana was the species detected most frequently in ticks, followed by Borrelia garinii and Borrelia lusitaniae. Among birds infested by infected ticks, 23% (6/26) were infested by B. lusitaniae-infected larvae. Migratory birds appear to be reservoir hosts for B. lusitaniae.


arrow
INTRODUCTION
 
It is now clearly established that birds play a role as reservoir hosts in the ecology of Lyme borreliosis (16). In Europe, seven Borrelia species belonging to the complex B. burgdorferi sensu lato (Borrelia burgdorferi sensu stricto, Borrelia garinii, Borrelia afzelii, Borrelia valaisiana, Borrelia lusitaniae, Borrelia bissetti, and Borrelia spielmani) have been detected in the tick vector, Ixodes ricinus. The association of at least two of them, B. garinii and B. valaisiana, with birds is now well documented in Europe (12, 17, 21, 22). Birds play an important role not only in maintaining B. burgdorferi sensu lato in areas of endemicity; in fact, some of them, through their migration, also play a role by spreading ticks within and between continents (13, 19, 23-25, 30, 34, 35). In Europe, the role of migratory birds in the dispersal of B. burgdorferi sensu lato has been investigated in Scandinavia (26, 27) and on the Baltic Sea (3).

In Switzerland, studies on the infection of birds by B. burgdorferi sensu lato are scarce (17, 18). The reservoir competence of the European blackbird (Turdus merula) for B. garinii and B. valaisiana was demonstrated by Humair et al. (17). Recently, Papadopoulos et al. (28) reported the presence of I. ricinus on 51 bird species captured in this country. These authors listed 11 tick species infesting birds, with 2 (Rhipicephalus simus and Hyalomma marginatum marginatum) having been imported by migratory birds (28). Since nothing is known about the role of migratory birds in Switzerland, we investigated the tick infestation of birds during their pre- and postnuptial migrations and the prevalence of B. burgdorferi sensu lato in ticks on migratory birds.

The first survey took place at Bolle di Magadino in April and May 2002. This site is a marsh area at 194 m above sea level south of the Alps (Canton Ticino), where local birds and birds migrating further north were caught. The second survey was carried out at the Col de Bretolet (Canton Valais, at the Swiss-French border) from 6 September to 4 November 2002. At this site (1,923 m above sea level), birds were caught during their southwestward migration while crossing this Alpine pass. Birds were caught in mist nets during routine bird-catching operations of the Swiss Ornithological Institute (Sempach, Switzerland). All birds belonging to the Turdidae were examined for ticks as well as other species, such as Anthus trivalis, Anthus pratensis, Anthus spinoletta, Prunella modularis, Sylvia borin, Sylvia atricapilla, Sylvia communis, and Sturnus vulgaris. Ticks were removed from birds with forceps upon visual inspection and placed into plastic vials (one vial/bird). The species and stage of each tick were identified.

Live fully engorged ticks were screened for B. burgdorferi sensu lato after their molt by cultivation in BSKII medium (10, 33) either as individuals or in pools of ticks. Pools contained ticks collected from a bird at one time. Culture medium was examined by dark-field microscopy for 45 days. All tubes were investigated for Borrelia DNA detection by PCR-restriction fragment length polymorphism according to the method of Postic et al. (29).

Partially engorged ticks stored in 70% ethanol were examined for Borrelia DNA by PCR-reverse line blot (RLB) according to the method of Schouls et al. (32). Borrelia DNA was extracted using 0.7 M ammonium hydroxide. Primers used to amplify the variable spacer region between two repeated genes encoding ribosomal 23S and 5S were 5S-Bor and 23S-Bor (4). DNA amplification was performed using a Whatman (Göttingen, Germany) Biometra TGradient Thermocycler 96. Isolates of B. burgdorferi sensu stricto (B31), B. garinii (NE11), B. lusitaniae (PotiB3), B. afzelii (NE632), and B. valaisiana (VS116) were used as positive controls. Negative controls were included during extraction and PCR. For RLB, the PCR products were hybridized to seven oligonucleotide probes (75 pmol) blotted in lines on an activated Biodyne C membrane (Pall Europe Ltd., Portsmouth, United Kingdom) using a Miniblotter 45 (Immunetic, Cambridge, MA). B. burgdorferi sensu lato, B. burgdorferi sensu stricto, B. afzelii, and B. garinii probes were described by Schouls et al. (32) and Alekseev et al. (4). For this study, three new B. burgdorferi genospecies-specific oligonucleotide probes were designed: B. valaisiana (VSNE) (5' amino-TATATCTTTTGTTCAATCCATGT), B. garinii (GANE) (5' amino-CAAAAACATAAATATCTAAAAACATAA), and B. lusitaniae (LusiNE) (5' amino-TCAAGATTTGAAGTATAAAATAAAA). Hybridization was visualized after exposing the membrane to X-ray film (Hyperfilm ECL; Amersham Biosciences, Otelfingen, Switzerland).

At Bolle di Magadino, in spring, 283 birds were examined for ticks (Table 1). Seventeen birds of four species were infested by ticks, giving a prevalence of 6%. We observed a mean density (total number of ticks observed divided by total number of examined hosts [20]) of 0.12 tick per bird (33 ticks/283 birds) and an intensity of infestation (total number of ticks observed divided by the number of infested hosts [20]) of 1.94 ticks per bird (33 ticks/17 birds). Intensity of infestation varied from 2.23 to 1 according to bird species (Table 1). All 18 larvae (not identified) were found on Erithacus rubecula. Among 15 infesting nymphs, 3 were H. marginatum (2 on Phoenicurus phoenicurus and 1 on E. rubecula), 10 were Ixodes frontalis (9 on E. rubecula and 1 on Luscinia megarhynchos), and 2 were Ixodes ricinus (1 on E. rubecula and 1 on P. modularis). None of the 33 ticks was infected by Borrelia.


View this table:
[in this window]
[in a new window]
  		TABLE 1. Prevalence and intensity of tick infestation of migratory birds captured at Bolle di Magadino

In autumn, at the Col de Bretolet, 987 birds (21 species) were examined for ticks. One hundred eighty birds of 11 species were infested by 417 ticks (369 larvae and 48 nymphs), giving a prevalence of infestation of 18.2% (Table 2), a mean density of 0.42 tick per bird (417 ticks/987 birds), and an intensity of infestation of 2.32 ticks per infested bird (417 ticks/180 birds). Prevalences and intensity of infestation varied according to bird species (Table 2). The highest intensity of infestation was 7.0 ticks. The maximum number of ticks collected was 30 larvae on one European robin captured in October. The most abundant tick species was I. ricinus (n = 411). I. frontalis (n = 3) was collected from one European robin. Three additional ticks could not be identified.


View this table:
[in this window]
[in a new window]
  		TABLE 2. Prevalence and intensity of tick infestation of migratory birds captured at the Col de Bretolet

I. ricinus larvae and nymphs collected from 95 birds (76 E. rubecula, 2 P. phoenicurus, 1 Oenanthe oenanthe, 12 T. philomelos, 3 T. merula, and 1 P. ochruros bird) were examined for Borrelia infection. Among these birds, 26/95 (27.4%) harbored infected ticks: 14/76 (18.4%) of E. rubecula, 7/12 (58.3%) of T. philomelos, 2/3 (66.7%) of T. merula, 2/2 (100%) of P. phoenicurus, and 1/1 (100%) of P. ochruros. Most birds (15/26, 57.7%) were infested by larvae only (11 of E. rubecula, 2 of T. merula, 1 of P. phoenicurus, and 1 of P. ochruros), 7 (26.9%) were infested by larvae and nymphs (3 of E. rubecula, 1 of P. phoenicurus, and 3 of T. philomelos), and 4 (15.4%) were infested by nymphs only (T. philomelos).

Borrelia was observed in 21/127 (16.5%) larvae and 9/26 (34.6%) nymphs examined individually (chi-square = 4.475; P < 0.05). Five Borrelia species were detected in ticks. Mixed infections were observed in six larvae (B. lusitaniae and B. garinii; B. lusitaniae and B. burgdorferi sensu stricto; B. garinii and B. valaisiana [n = 2]; B. lusitaniae, B. valaisiana, and B. garinii; and B. lusitaniae, B. valaisiana, and B. burgdorferi) and one nymph (B. garinii and B. valaisiana). In addition to these individually examined ticks, 68 larvae and 2 nymphs collected on 9 E. rubecula, 2 T. merula, and 1 T. philomelos bird were examined as 12 pools (1 for each bird). B. valaisiana and B. afzelii were detected in one pool of two larvae collected from one E. rubecula bird, B. valaisiana and B. lusitaniae in one pool of two larvae collected from one T. merula bird, and B. valaisiana in 1 pool of 3 larvae collected from one T. merula bird.

B. valaisiana was the most frequent species in ticks (n = 14), followed by B. garinii (n = 8), B. lusitaniae (n = 7), B. afzelii (n = 5), B. burgdorferi sensu stricto (n = 5), and unidentified species (n = 5) (Table 3). Five Borrelia species were detected in ticks feeding on E. rubecula and T. philomelos, whereas T. merula and P. phoenicurus were infested by ticks infected by B. garinii, B. valaisiana, and B. lusitaniae. Ticks collected from P. ochruros were infected by B. valaisiana and B. burgdorferi sensu stricto only. E. rubecula birds harboring infected ticks were infested in 11 cases by larvae only and by larvae and nymphs in 3 cases. Five isolates were obtained from ticks: NE3928 (B. afzelii), NE3929 (B. garinii), NE3930 (B. valaisiana and B. lusitaniae), and NE3931 and NE3032 (B. valaisiana).


View this table:
[in this window]
[in a new window]
  		TABLE 3. B. burgdorferi sensu lato infection in I. ricinus feeding on the different bird species (including mixed infections and infections of pooled ticks)

I. ricinus, I. frontalis, and H. marginatum were infesting migratory birds during the northward and southward migrations. I. ricinus clearly dominated on birds captured during the southward autumn migration, whereas I. frontalis dominated among ticks identified from local or northward spring-migrating birds. I. ricinus is very frequently found on birds in Switzerland (2, 17, 18, 28). In this country, I. ricinus is known as the vector of B. burgdorferi sensu lato, the tick-borne encephalitis virus, Rickettsia helvetica, Babesia divergens, Babesia microti, Dipetalonema rugosicauda, and a trypanosome related to Trypanosoma theileri (1, 5, 8, 28).

I. frontalis is widely distributed in Europe and is rather rare in Switzerland compared to regions with a milder climate, such as Spain (28). Robins appear to be its most common hosts (28), as confirmed here. Papadopoulos et al. (28) also described its presence on a song thrush, and we observed I. frontalis for the first time in Switzerland on L. megarhynchos.

All H. marginatum ticks were collected from northward spring-migrating birds, as reported by Papadopoulos et al. (28). All individuals of this Mediterranean Hyalomma species were fully engorged, showing that they had been attached for a few days and were ready to drop off. This suggests that exotic ticks are imported into Switzerland by birds coming from the south. This tick species is considered the main vector of Crimean-Congo hemorrhagic fever virus in Eastern Europe, the Balkan countries, and Transcaucasia (14) and has been found infected by the West Nile virus (6).

During the southward migration in autumn, the prevalence of tick infestation was higher in birds (18.2%) than during the northward migration in spring (6.0%). In autumn, E. rubecula and T. merula had a tick infestation prevalence of 22% and 28%, respectively. For E. rubecula, this prevalence is much higher than that reported by Olsen et al. (26) in Scandinavia (2.2%). The mean density of ticks on birds was also higher in autumn (0.45 tick per bird) than in spring (0.12 tick per bird). A previous study in Egypt (15) also showed a higher infestation of birds in autumn than in spring. In contrast, other studies have shown a higher prevalence of tick infestation and mean density in spring than in autumn (3, 26). In our study, considering bird species, the rate of infestation of E. rubecula by I. ricinus was almost five times higher in autumn than in spring, while the sample size was too small with the other species for comparisons between seasons. The higher proportion of birds carrying ticks and the higher mean density in autumn than in spring or vice versa reflect the activity of ticks at these times of the year at stopover sites used by birds. It is clear that the lower the latitude (as with Switzerland compared to Sweden, Denmark, and Baltic Sea), the higher the infestation in autumn, since birds captured during the southward autumn migration over the Alps traveled through areas where I. ricinus biotopes are widespread and where I. ricinus may show a second peak of questing activity at this period of the year. At the opposite, in spring, birds traveled through the southern part of Europe before arriving in Switzerland and therefore had few contacts with I. ricinus. This explains why birds migrating to the south were three times more infested by ticks than those migrating northwards.

Most of the migrants caught in autumn originate from areas of the northeast of Switzerland, up to Fennoscandia and Russia. Among the species with a sample size >20 and which carried infected ticks, E. rubecula, T. philomelos, T. merula, and P. ochruros are wintering in southern France, Italy, the Iberian peninsula, Morocco, and Algeria, whereas P. phoenicurus is wintering in sub-Saharan Africa.

Among birds migrating southward, five species (E. rubecula, T. philomelos, T. merula, P. ochruros, and P. phoenicurus) carried B. burgdorferi sensu lato-infected ticks. Infection rates of examined I. ricinus ticks were 16.5% for larvae and 34.6% for nymphs. These results are similar to those observed in Scandinavia (26).

In Europe, B. garinii, B. burgdorferi sensu stricto, and B. afzelii were reported in ticks from migrating birds (3, 26). In our study, B. valaisiana, B. garinii, and B. lusitaniae were the most frequently found species, followed by B. afzelii and B. burgdorferi sensu stricto. Interestingly, robins and song thrushes were harboring ticks infected by five Borrelia species. Most robins (78.6%) were infested by larvae alone, suggesting that birds transmitted these Borrelia species to feeding larvae. The origin of the Borrelia species found in ticks feeding on song thrushes is less clear; larvae may have been infected through cofeeding transmission (9). The role played in our results by the reactivation of Borrelia infection in migrating birds (11) is unknown.

The most surprising part of our results is the abundance of B. lusitaniae in ticks feeding on birds. Not only was this Borrelia species identified in larvae in most cases, but it was above all present in larvae feeding on birds (6/7) infested by larvae only. This strongly suggests that birds are reservoir hosts for B. lusitaniae. This Borrelia species appears to be infrequent in I. ricinus in most areas of Europe (10), but B. lusitaniae has been described as the dominant species in southwest Europe (7) and in North Africa (31, 36, 37). Since some bird species, such as E. rubecula and T. philomelos, are migrating between southwestern Europe/North Africa and northern Europe, their role in the dispersal of B. lusitaniae, according to our results, is highly suspected.


arrow
ACKNOWLEDGMENTS
 
This work was partially supported by the Swiss National Science Foundation (no. 3200B0-100657). P.-F.H. was supported by the Roche Research Foundation and the Novartis Foundation for Medicine and Biology.

We warmly thank R. Lardelli, F. Moran-Cadenas, C. Burri, and H. Schneider for their precious help. We also acknowledge L. Schouls and I. van de Pol for introducing us to the RLB technique.


arrow
FOOTNOTES
 
* Corresponding author. Mailing address: Institute of Zoology, Emile Argand 11, 2007 Neuchâtel 7, Switzerland. Phone: 41-32-718-3000. Fax: 41-32-718-3001. E-mail: lise.gern{at}unine.ch Back


arrow
REFERENCES
 
    1
  1. Aeschlimann, A., W. Burgdorfer, H. Matile, O. Péter, and R. Wyler. 1979. Aspects nouveaux du rôle de vecteur joué par Ixodes ricinus L. en Suisse. Note préliminaire. Acta Trop. 36:181-191.[Medline]
    2. 2
  2. Aeschlimann, A., C. Vaucher, and C. Mermod. 1974. The role of birds in the life cycle of Ixodes ricinus (L.) in a low marsh forest of Switzerland, p. 949-950. Proceedings of the Third International Congress of Parasitology, vol. 2. Facta Publication, Verlag H. Egermann, Vienna, Austria.
    3. 3
  3. Alekseev, A. N., H. V. Dubinina, A. V. Semenov, and C. V. Bolshakov. 2001. Evidence of ehrlichiosis agents found in ticks (Acari: Ixodidae) collected from migratory birds. J. Med. Entomol. 38:471-474.[Medline]
    4. 4
  4. Alekseev, A. N., A. V. Dubinina, I. van de Pol, and L. M. Schouls. 2001. Identification of Ehrlichia spp. and Borrelia burgdorferi in Ixodes ticks in the Baltic regions of Russia. J. Clin. Microbiol. 39:2237-2242.[Abstract/Free Full Text]
    5. 5
  5. Beati, L., O. Péter, W. Burgdorfer, A. Aeschlimann, and D. Raoult. 1993. Confirmation that Rickettsia helvetica sp. nov. is a distinct species of the spotted fever group of rickettsiae. Int. J. Syst. Bacteriol. 43:521-526.[Abstract/Free Full Text]
    6. 6
  6. Chevalier, V., S. de la Rocque, T. Baldet, L. Vial, and F. Roger. 2004. Epidemiological processes involved in the emergence of vector-borne diseases: West Nile fever, Rift Valley fever, Japanese encephalitis and Crimean haemorrhagic fever. Rev. Sci. Tech. (Off. Int. Epizoot.) 23:535-555.
    7. 7
  7. de Michelis, S., H.-S. Sewell, M. Collares-Pereira, M. Santos-Reis, L. M. Schouls, V. Benes, E. C. Holmes, and K. Kurtenbach. 2000. Genetic diversity of Borrelia burgdorferi sensu lato in ticks from mainland Portugal. J. Clin. Microbiol. 38:2128-2133.[Abstract/Free Full Text]
    8. 8
  8. Foppa, I. M., P. J. Krause, A. Spielman, H. Goethert, L. Gern, B. Brand, and S. R. Telford. 2002. Entomologic and serologic evidence of zoonotic transmission of Babesia microti in Eastern Switzerland. Emerg. Infect. Dis. 8:722-726.[Medline]
    9. 9
  9. Gern, L., and O. Rais. 1996. Efficient transmission of Borrelia burgdorferi between cofeeding Ixodes ricinus ticks (Acari: Ixodidae). J. Med. Entomol. 33:189-192.[Medline]
    10. 10
  10. Gern, L., C. M. Hu, E. Kocianova, V. Vyrostekova, and J. Rehacek. 1999. Genetic diversity of Borrelia burgdorferi sensu lato isolates obtained from Ixodes ricinus ticks collected in Slovakia. Eur. J. Epidemiol. 15:665-669.[CrossRef][Medline]
    11. 11
  11. Gylfe, A., S. Bergström, J. Lundström, and B. Olsen. 2000. Reactivation of Borrelia infection in birds. Nature 403:724-725.[CrossRef][Medline]
    12. 12
  12. Hanincova, K., V. Taragelova, J. Koci, S. M. Schäfer, R. Hails, A. J. Ullmann, J. Piesman, M. Labuda, and K. Kurtenbach. 2003. Association of Borrelia garinii and B. valaisiana with songbirds in Slovakia. Appl. Environ. Microbiol. 69:2825-2830.[Abstract/Free Full Text]
    13. 13
  13. Hoogstraal, H. 1972. Birds as tick hosts and as reservoirs and disseminators of tickborne infectious agents. Wiad. Parazytol. 18:702-706.
    14. 14
  14. Hoosgtraal, H. 1979. The epidemiology of Crimean-Congo hemorrhagic fever in Asia, Europe and Africa. J. Med. Entomol. 15:307-415.[Medline]
    15. 15
  15. Hoogstraal, H., M. N. Kaiser, M. A. Traylor, E. Guindy, and S. Gaber. 1963. Ticks (Ixodidae) on birds migrating from Europe and Asia to Africa, 1959-1961. Bull. W. H. O. 28:235-262.[Medline]
    16. 16
  16. Humair, P. F. 2002. Birds and Borrelia. Int. J. Med. Microbiol. 291:70-74.
    17. 17
  17. Humair, P. F., D. Postic, R. Wallich, and L. Gern. 1998. An avian reservoir (Turdus merula) of the Lyme borreliosis spirochetes. Zentbl. Bakteriol. 287:521-538.
    18. 18
  18. Humair, P. F., N. Turrian, A. Aeschlimann, and L. Gern. 1993. Ixodes ricinus immatures on birds in a focus of Lyme borreliosis. Folia Parasitol. 40:237-242.
    19. 19
  19. Ishiguro, F., N. Takada, T. Masuzawa, and T. Fukui. 2000. Prevalence of Lyme disease Borrelia spp. in ticks from migratory birds on the Japanese mainland. Appl. Environ. Microbiol. 66:982-986.[Abstract/Free Full Text]
    20. 20
  20. Kahl, O., L. Gern, L. Eisen, and R. S. Lane. 2002. Ecological research on Borrelia burgdorferi sensu lato: terminology and some methodological pitfalls, p. 29-46. In J. Gray, O. Kahl, R. S. Lane, and G. Stanek (ed.), Lyme borreliosis: biology, epidemiology and control. CAB International, Oxon, United Kingdom.
    21. 21
  21. Kurtenbach, K., M. Peacey, S. G. T Rijpkema, A. Hoodless, P. A. Nuttall, and S. E. Randolph. 1998. Differential transmission of the genospecies of Borrelia burgdorferi sensu lato by game birds and small rodents in England. Appl. Environ. Microbiol. 64:1169-1174.[Abstract/Free Full Text]
    22. 22
  22. Kurtenbach, K., S. M. Schäfer, H. S. Sewell, M. Peacey, A. N. Hoodless, P. A. Nuttall, and S. E. Randolph. 2002. Differential survival of Lyme borreliosis spirochetes in ticks that feed on birds. Infect. Immun. 70:5893-5895.[Abstract/Free Full Text]
    23. 23
  23. Miyamoto, K., M. Nakao, H. Fujita, and F. Sato. 1993. The Ixodid ticks on migratory birds in Japan and the isolation of Lyme disease spirochetes from bird-feeding ticks. Jpn. J. Sanit. Zool. 44:315-326.
    24. 24
  24. Miyamoto, K., Y. Sato, K. Okada, M. Fukunaga, and F. Sato. 1997. Competence of a migratory bird, red-bellied thrush (Turdus chrysolaus), as an avian reservoir for the Lyme disease spirochetes in Japan. Acta Trop. 65:43-51.[CrossRef][Medline]
    25. 25
  25. Nakao, M., K. Miyamoto, and M. Fukunaga. 1994. Lyme disease spirochetes in Japan: enzootic transmission cycles in birds, rodents, and Ixodes persulcatus ticks. J. Infect. Dis. 170:878-882.[Medline]
    26. 26
  26. Olsen, B., T. G. T. Jaenson, and S. Bergström. 1995. Prevalence of Borrelia burgdorferi sensu lato-infected ticks on migrating birds. Appl. Environ. Microbiol. 61:3082-3087.[Abstract]
    27. 27
  27. Olsen, B., T. G. T. Jaenson, L. Noppa, J. Bunikis, and S. Bergström. 1993. A Lyme borreliosis cycle in seabirds and Ixodes uriae ticks. Nature 362:340-342.[CrossRef][Medline]
    28. 28
  28. Papadopoulos. B., P. F. Humair, A. Aeschlimann, C. Vaucher, and W. Büttiker. 2002. Ticks on birds in Switzerland. Acarologia 42:3-19.
    29. 29
  29. Postic, D., M. V. Assous, P. A. D. Grimont, and G. Baranton. 1994. Diversity of Borrelia burgdorferi sensu lato evidenced by restriction fragment length polymorphism of rrf (5S)-rrl (23S) intergenic spacer amplicons. Int. J. Syst. Bacteriol. 44:743-752.[Abstract/Free Full Text]
    30. 30
  30. Rand, P. W., E. H. Lacombe, R. P. Smith, Jr., and J. Ficker. 1998. Participation of birds (Aves) in the emergence of Lyme disease in southern Maine. J. Med. Entomol. 35:270-276.[Medline]
    31. 31
  31. Sarih, M., F. Jouda, L. Gern, and D. Postic. 2003. First isolation of Borrelia burgdorferi sensu lato from Ixodes ricinus ticks in Morocco. Vector borne Zoonotic Dis. 3:133-141.[CrossRef][Medline]
    32. 32
  32. Schouls, L. M., I. van de Pol, S. G. T. Rijpkema, and C. S. Schot. 1999. Detection and identification of Ehrlichia, Borrelia burgdorferi sensu lato, and Bartonella species in Dutch Ixodes ricinus ticks. J. Clin. Microbiol. 37:2215-2222.[Abstract/Free Full Text]
    33. 33
  33. Sinsky, R. J., and J. Piesman. 1989. Ear punch biopsy method for detection of Borrelia burgdorferi from rodents. J. Clin. Microbiol. 27:1723-1727.[Abstract/Free Full Text]
    34. 34
  34. Smith, R. P., Jr., P. W. Rand, E. H. Lacombe, S. R. Morris, D. W. Holmes, and D. A. Caporale. 1996. Role of bird migration in the long-distance dispersal of Ixodes dammini, the vector of Lyme disease. J. Infect. Dis. 174:221-224.[Medline]
    35. 35
  35. Weisbrod, A. R., and R. C. Johnson. 1989. Lyme disease and migrating birds in the Saint Croix River Valley. Appl. Environ. Microbiol. 55:1921-1924.[Abstract/Free Full Text]
    36. 36
  36. Younsi, H., D. Postic, G. Baranton, and A. Bouattour. 2001. High prevalence of Borrelia lusitaniae in Ixodes ricinus ticks in Tunisia. Eur. J. Epidemiol. 17:53-56.[CrossRef][Medline]
    37. 37
  37. Younsi, H., D. M. Sarih, F. Jouda, E. Godfroid, L. Gern, A. Bouattour, G. Baranton, and D. Postic. 2005. Characterization of Borrelia lusitaniae isolates collected in Tunisia and Morocco. J. Clin. Microbiol. 43:1587-1593.[Abstract/Free Full Text]

Applied and Environmental Microbiology, January 2006, p. 976-979, Vol. 72, No. 1
0099-2240/06/$08.00+0     doi:10.1128/AEM.72.1.976-979.2006
Copyright © 2006, American Society for Microbiology. All Rights Reserved.



This article has been cited by other articles:

  • Staszewski, V, McCoy, K.D, Boulinier, T (2008). Variable exposure and immunological response to Lyme disease Borrelia among North Atlantic seabird species. Proc R Soc B 275: 2101-2109 [Abstract] [Full Text]  
  • Taragel'ova, V., Koci, J., Hanincova, K., Kurtenbach, K., Derdakova, M., Ogden, N. H., Literak, I., Kocianova, E., Labuda, M. (2008). Blackbirds and Song Thrushes Constitute a Key Reservoir of Borrelia garinii, the Causative Agent of Borreliosis in Central Europe. Appl. Environ. Microbiol. 74: 1289-1293 [Abstract] [Full Text]  
  • Wielinga, P. R., Gaasenbeek, C., Fonville, M., de Boer, A., de Vries, A., Dimmers, W., Akkerhuis Op Jagers, G., Schouls, L. M., Borgsteede, F., van der Giessen, J. W. B. (2006). Longitudinal Analysis of Tick Densities and Borrelia, Anaplasma, and Ehrlichia Infections of Ixodes ricinus Ticks in Different Habitat Areas in The Netherlands. Appl. Environ. Microbiol. 72: 7594-7601 [Abstract] [Full Text]  
  • Richter, D., Matuschka, F.-R. (2006). Perpetuation of the Lyme Disease Spirochete Borrelia lusitaniae by Lizards.. Appl. Environ. Microbiol. 72: 4627-4632 [Abstract] [Full Text]  

This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Poupon, M.-A.
Right arrow Articles by Gern, L.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Poupon, M.-A.
Right arrow Articles by Gern, L.
Agricola
Right arrow Articles by Poupon, M.-A.
Right arrow Articles by Gern, L.

Copyright © 2009 by the American Society for Microbiology.   For an alternate route to Journals.ASM.org, visit: http://intl-journals.asm.org | More Info»