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Molecular detection of Borrelia valaisiana-related spirochetes from Ixodes granulatus ticks in Taiwan

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Abstract

Borrelia valaisiana-related spirochetes were detected for the first time in Ixodes granulatus ticks collected in Taiwan. The genetic identities of these detected spirochetes were determined by analyzing the gene sequences amplified by a genospecies-specific polymerase chain reaction assay based on the outer surface protein A (OspA) gene of B. burgdorferi sensu lato. Phylogenetic relationships were analyzed by comparing the sequences of OspA gene obtained from 35 strains of Borrelia spirochetes representing six genospecies of Borrelia. Eight major clades can be easily distinguished by neighbour-joining analysis and were congruent by maximum-parsimony method. Except one strain (KH-74), all these Borrelia spirochetes of Taiwan were genetically affiliated to the same clade with highly homogeneous sequences (97.8–100% similarity), and can be discriminated from other groups of B. valaisiana and other genospecies of Borrelia spirochetes with a sequence divergence ranging from 3 to 19.6%. Moreover, intraspecific analysis also revealed that three distinct groups are evident between the same species of B. valaisiana spirochetes detected in Taiwan. Our results provide the first evidence of B. valaisiana spirochetes detected in I. granulatus ticks collected in Taiwan and demonstrate that all these B. valaisiana spirochetes of Taiwan represent three major groups distinct from the European group of B. valaisiana spirochetes.

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References

  • Aguero-Rosenfeld ME, Wang GQ, Schwartz I et al (2005) Diagnosis of Lyme borreliosis. Clin Microbiol Rev 18:484–509

    Article  CAS  PubMed  Google Scholar 

  • Ai CX, Wen YX, Zhang YG et al (1988) Clinical manifestations and epidemiological characteristics of Lyme disease in Hailin county, Heilongjiang Province, China. Annals NY Acad Sci 539:302–313

    Article  CAS  Google Scholar 

  • Bergstrom S, Bundoc VG, Barbour AG (1989) Molecular analysis of linear plasmid-encoded major surface proteins, OspA and OspB of the Lyme disease spirochete Borrelia burgdorferi. Mol Microbiol 3:479–486

    Article  CAS  PubMed  Google Scholar 

  • Burgdorfer W, Barbour AGS, Hayes FW et al (1982) Lyme disease: a tick-borne spirochetosis? Science 216:1317–1319

    Article  CAS  PubMed  Google Scholar 

  • Caporale DA, Kocher TD (1994) Sequence variation in the outer-surface-protein genes of Borrelia burgdorferi. Mol Biol Evol 11:51–64

    CAS  PubMed  Google Scholar 

  • Chao LL, Wu WJ, Shih CM (2009) Molecular analysis of Ixodes granulatus, a possible vector tick for Borrelia burgdorferi sensu lato in Taiwan. Exp Appl Acarol 48:329–344

    Article  CAS  PubMed  Google Scholar 

  • Chu CY, Liu W, Jiang BG et al (2008) Novel genospecies of Borrelia burgdorferi sensu lato from rodents and ticks in southwestern China. J Clin Microbiol 46:3130–3133

    Article  CAS  PubMed  Google Scholar 

  • Clinco M, Padovan D, Murgia R et al (1998) Rate of infection of Ixodes ricinus ticks with Borrelia burgdorferi sensu stricto, Borrelia garinii, Borrelia afzelii and group VS116 in an endemic focus of Lyme disease in Italy. Eur J Clin Microbiol Infect Dis 17:90–94

    Google Scholar 

  • Demaerschalck I, Messaoud AB, Kesel MD et al (1995) Simutaneous presence of different Borrelia burgdorferi genospecies in biological fluids of Lyme disease patients. J Clin Microbiol 33:602–608

    CAS  PubMed  Google Scholar 

  • Diza E, Papa A, Vezyri E, Tsounis S, Milonas I, Antoniadis A (2004) Borrelia valaisiana in cerebrospinal fluid. Emerg Infect Dis 10:1692–1693

    PubMed  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 52:1119–1134

    Google Scholar 

  • Jonsson M, Noppa L, Barbour AG, Bergstrom S (1992) Heterogeneity of outer surface proteins in Borrelia burgdorferi: comparison of osp operons of three isolates of different geographic origins. Infect Immun 60:1845–1853

    CAS  PubMed  Google Scholar 

  • Kawabata M, Baba S, Iguchi K et al (1987) Lyme disease in Japan and its possible incriminated tick vector, Ixodes persulcatus. J Infect Dis 156:854

    CAS  PubMed  Google Scholar 

  • Kimura M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120

    Article  CAS  PubMed  Google Scholar 

  • Kirstein F, Rijpkema SG, Molkenboer M, Gray JS (1997) The distribution and prevalence of B. burgdorferi genomospecies in Ixodes ricinus ticks in Ireland. Eur J Epidemiol 13:67–72

    Article  CAS  PubMed  Google Scholar 

  • Kurtenbach K, Peacey M, Rijpkema SG, Hoodless AN, Nuttall PA, Randolph SE (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

    CAS  PubMed  Google Scholar 

  • Kurtenbach K, Michelis SDe, Etti S et al (2002) Host associations of Borrelia burgdorferi sensu lato-the key role of host complement. Trends Microbiol 10:74–79

    Article  CAS  PubMed  Google Scholar 

  • Liebisch G, Sohns B, Bautsch W (1998) Detection and typing of Borrelia burgdorferi sensu lato in Ixodes ricinus ticks attached to human skin by PCR. J Clin Microbiol 36:3355–3358

    CAS  PubMed  Google Scholar 

  • Masuzawa T, Fukui T, Miyake M et al (1999) Determination of members of a Borrelia afzelii-related group isolated from Ixodes nipponensis in Korea as Borrelia valaisiana. Int J Syst Bacterial 49:1409–1415

    Article  CAS  Google Scholar 

  • Masuzawa T, Takada N, Kudeken M et al (2001) Borrelia sinica sp. nov., a Lyme disease-related Borrelia species isolated in China. Int J Syst Evol Microbiol 51:1817–1824

    CAS  PubMed  Google Scholar 

  • Masuzawa T, Hashimoto N, Kudeken M et al (2004) New genomospecies related to Borrelia valaisiana, isolated from mammals in Okinawa archipelago, Japan. J Med Microbiol 53:421–426

    Article  CAS  PubMed  Google Scholar 

  • Matuschka FR, Richter D, Fischer P et al (1990) Subadult Ixodes ricinus (Acari: Ixodidae) on rodents in Berlin, West Germany. J Med Entomol 27:385–390

    CAS  PubMed  Google Scholar 

  • Maupin GO, Gage KL, Piesman J et al (1994) Discovery of an enzootic cycle of Borrelia burgdorferi in Neotoma mexicana and Ixodes spinipalpis from northern Colorado, an area where Lyme disease is nonendemic. J Infect Dis 170:636–643

    CAS  PubMed  Google Scholar 

  • Nakao M, Miyamoto K, Uchikawa K et al (1992) Characterization of Borrelia burgdorferi isolated from Ixodes persulcatus and Ixodes ovatus ticks in Japan. Am J Trop Med Hyg 47:505–511

    CAS  PubMed  Google Scholar 

  • Park KH, Chang WH, Schwan TG (1993) Identification and characterization of Lyme disease spirochetes, Borrelia burgdorferi sensu lato, isolated in Korea. J Clin Microbiol 31:1831–1837

    CAS  PubMed  Google Scholar 

  • Peavey CA, Lane RS, Damrow T (2000) Vector competence of Ixodes angustus (Acari: Ixodidae) for Borrelia burgdorferi sensu stricto. Exp Appl Acarol 24:77–84

    Article  CAS  PubMed  Google Scholar 

  • Postic D, Korenberg E, Gorelova N, Kovalevski YV, Bellenger E, Baranton G (1997) Borrelia burgdorferi sensu lato in Russia and neighbouring countries: high incidence of mixed isolates. Res Microbiol 148:691–702

    Article  CAS  PubMed  Google Scholar 

  • Postic D, Garnier M, Baranton G (2007) Multilocus sequence analysis of atypical Borrelia burgdorferi sensu lato isolates: description of Borrelia californiensis sp. nov., and genomospecies 1 and 2. Int J Med Microbiol 297:263–271

    Article  CAS  PubMed  Google Scholar 

  • Richter D, Postic D, Sertour N et al (2006) Delineation of Borrelia burgdorferi sensu lato species by multilocus sequence analysis and confirmation of the delineation of Borrelia spielmanii sp. nov. Int J Syst Evol Microbiol 56:873–881

    Article  CAS  PubMed  Google Scholar 

  • Rijpkema SG, Golubic D, Molkenboer M, Verbeek-De Kruif N, Schellekens JF (1996) Identification of four genomic groups of Borrelia burgdorferi sensu lato in Ixodes ricinus ticks collected in a Lyme borreliosis endemic region of northern Croatia. Exp Appl Acarol 20:23–30

    Article  CAS  PubMed  Google Scholar 

  • Saito K, Ito T, Asashima N et al (2007) Case report: Borrelia valaisiana infection in a Japanese man associated with traveling to foreign countries. Am J Trop Med Hyg 77:1124–1127

    CAS  PubMed  Google Scholar 

  • Shih CM, Chao LL (1998) Lyme disease in Taiwan: primary isolation of Borrelia burgdorferi-like spirochetes from rodents in Taiwan area. Am J Trop Med Hyg 59:687–692

    CAS  PubMed  Google Scholar 

  • Shih CM, Chao LL (2002) An OspA-based genospecies identification of Lyme disease spirochetes (Borrelia burgdorferi sensu lato) isolated in Taiwan. Am J Trop Med Hyg 66:611–615

    CAS  PubMed  Google Scholar 

  • Shih CM, Chao LL (2004) Current status of Lyme disease in Taiwan with description of its vector ticks and reservoir hosts. In: Lu KH et al (eds) Proceedings, Symposium on rodent damage and control strategy. The Plant Protection Society of the Republic of China, Taichung, pp 79–92 (in Chinese)

  • Shih CM, Liu LP, Chung WC et al (1997) Human babesiosis in Taiwan: asymptomatic infection with a Babesia microti-like organism in a Taiwanese woman. J Clin Microbiol 35:450–454

    CAS  PubMed  Google Scholar 

  • Shih CM, Chang HM, Chen SL et al (1998a) Genospecies identification and characterization of Lyme disease spirochetes of genospecies Borrelia burgdorferi sensu lato isolated from rodents in Taiwan. J Clin Microbiol 36:3127–3132

    CAS  PubMed  Google Scholar 

  • Shih CM, Wang JC, Chao LL et al (1998b) Lyme disease in Taiwan: first human patient with characteristic erythema chronicum migrans skin lesion. J Clin Microbiol 36:807–808

    CAS  PubMed  Google Scholar 

  • Spielman A (1988) Lyme disease and human babesiosis: evidence incriminating vector and reservoir hosts. In: Englund PT, Sher AR (eds) The biology of parasitism. Liss, New York, pp 147–165

    Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  CAS  PubMed  Google Scholar 

  • Teng KF, Jiang ZJ (1991) Economic insect fauna of China Fasc 39 Acari: Ixodidae. Science Press, Beijing (in Chinese)

    Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nuc Acids Res 22:4673–4680

    Article  CAS  Google Scholar 

  • Wan KL, Zhang ZF, Dou GL et al (1998) Investigation on primary vectors of Borrelia burgdorferi in China. Chinese J Epidemiol 19:263–266 (in Chinese)

    CAS  Google Scholar 

  • Wang G, van Dam AP, Le Fleche A et al (1997) Genetic and phenotypic analysis of Borrelia valaisiana sp. nov. (Borrelia genomic groups VS116 and M19). Int J Syst Bacteriol 47:926–932

    Article  CAS  PubMed  Google Scholar 

  • Wang G, van Dam AP, Schwartz I, Dankert J (1999) Molecular typing of Borrelia burgdorferi sensu lato: taxonomic, epidemiological, and clinical implications. Clin Microbiol Rev 12:633–653

    CAS  PubMed  Google Scholar 

  • Wang G, van Dam AP, Dankert J (2000) Two distinct ospA genes among Borrelia valaisiana strains. Res Microbiol 151:325–331

    Article  CAS  PubMed  Google Scholar 

  • Will G, Jauris-Heipke S, Schwab E et al (1995) Sequence analysis of OspA genes shows homogeneity within Borrelia burgdorferi sensu stricto and Borrelia afzelii strains but reveals major subgroups within the Borrelia garinii species. Med Microbiol Immunol 184:73–80

    Article  CAS  PubMed  Google Scholar 

  • Wilske B, Preac-Mursic V, Gobal UB et al (1993) An OspA serotyping system for Borrelia burgdorferi based on reactivity with monoclonal antibodies and OspA sequence analysis. J Clin Microbiol 31:340–350

    CAS  PubMed  Google Scholar 

  • Wilson N (1970) New distributional records of ticks from Southeast Asia and the Pacific (Metastigmata: Argasidae, Ixodidae). Oriental Insects 4:37–46

    Google Scholar 

  • Zhang ZF, Wan KL, Zhang JS et al (1997) Studies on epidemiology and etiology of Lyme disease in China. Chinese J Epidemiol 18:8–11 (in Chinese)

    Google Scholar 

  • Zumstein G, Fuchs R, Hofmann A, Preac-Mursic V, Soutschek E, Wilske B (1992) Genetic polymorphism of the gene encoding the outer surface protein A (OspA) of Borrelia burgdorferi. Med Microbiol Immunol 181:57–70

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This work was supported in part by grants from the Department of Defense (DOD98-34) and National Science Council (NSC96-2314-B-016-025-MY3), Taipei, Taiwan, Republic of China.

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Authors and Affiliations

  1. Department of Parasitology and Tropical Medicine, National Defense Medical Center, Taipei, 114, Taiwan, ROC

    Li-Lian Chao & Chien-Ming Shih

  2. Department of Entomology, National Taiwan University, Taipei, Taiwan, ROC

    Li-Lian Chao & Wen-Jer Wu

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  1. Li-Lian Chao
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  2. Wen-Jer Wu
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Correspondence to Chien-Ming Shih.

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Chao, LL., Wu, WJ. & Shih, CM. Molecular detection of Borrelia valaisiana-related spirochetes from Ixodes granulatus ticks in Taiwan. Exp Appl Acarol 52, 393–407 (2010). https://doi.org/10.1007/s10493-010-9372-x

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