Borrelia miyamotoi Infections among Wild Rodents Show Age and Month Independence and Correlation with Ixodes persulcatus Larval Attachment in Hokkaido,Japan

Abstract

To clarify how Borrelia miyamotoi is maintained in the environment in Hokkaido, we examined Ixodes persulcatus for its prevalence among wild rodents and its tick vector by detecting a portion of the borrelial flaB gene in rodent urinary bladder and blood samples, and from whole ticks. We compared B. miyamotoi infection rates to Borrelia garinii and Borrelia afzelii, which are human Lyme disease pathogens also carried by wild rodents, and which are transmitted by the same vector tick. Whereas B. garinii and B. afzelii showed age dependence of infection rates among wild rodents (18.4% and 9.9% among adults and 6.0% and 3.4% among sub-adults, respectively) when looking at urinary bladder samples, B. miyamotoi infection rates were not age dependent for either blood (4.2% among adults, and 7.9% among sub-adults) or urinary bladder samples (1.0% among adults, and 1.7% among sub-adults). Moreover, while B. garinii and B. afzelii infection rates showed increases across months (June, July [p<0.05] and August [p<0.01] had higher rates than in May for adult rodents with B. garinii, and July and August had higher rates than in May [p<0.01] for adult rodents with B. afzelii), B. miyamotoi infection rates did not show significant month dependence. These differences in month and age dependence led us to suspect that B. miyamotoi may not develop persistent infections in wild rodents, as B. garinii and B. afzelii are thought to. Furthermore, we examined the extent of rodent exposure to I. persulcatus nymphs and larvae throughout most of the tick's active season (May through September), and determined that B. miyamotoi infection rates in sub-adult rodents were correlated with larval burden (p<0.01), suggesting that larvae may be very important in transmission of B. miyamotoi to wild rodents.

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References

Abe

. Age determination of Clethrionomys rufocanus bedforidiae (Thomas) Jpn J Ecol, 1976; 26:221–227.

Abe

. A Pictoral Guide to the Mammals of Japan. Tokyo: Tokai University Press, 1994; 90–109171–183.

Barbour AG Bunikis J Travinsky B Hoen AG et al. Niche partitioning of Borrelia burgdorferi and Borrelia miyamotoi in the same tick vector and mammalian reservoir species. Am J Trop Med Hyg, 2009; 81:112–1131.

Fomenko NV Livanova NN Borgoyakov VY Kozlova IV et al. Detection of Borrelia miyamotoi in Ixodes persulcatus ticks in Russia. Parazitologiia, 2010; 44:201–211.

Forestry Research Institute [Internet]. Hokkaido: Local Independent Administrative Agency Hokkaido Research Organization. c2010(cited March 8, 2011)www.fri.hro.or.jp/nezumi/shicho.htm/.

Fraenkel

, Garpmo

, Berglund

. Determination of novel Borrelia genospecies in Swedish Ixodes ricinus ticks. J Clin Microbiol, 2002; 40:3308–3312.

Fukunaga M Takahashi Y Tsuruta Y Matsushita O et al. Genetic and phenotypic analysis of Borrelia miyamotoi sp. nov., isolated from the ixodid tick Ixodes persulcatus, the vector for Lyme disease in Japan. Int J Syst Bacteriol, 1995; 45:804–810.

Hikida

, Murakami

. Age determination of the Japanese wood mouse, Apodemus speciosus. Jpn J Ecol, 1980; 30:109–116.

Kanai

, Fujii

, Saito

, Toyama

. Rapid and simple method for preparation of genomic DNA from easily obtainable clotted blood. J Clin Pathol, 1994; 47:1043–1044.

10.

Larsson C Andersson M Pelkonen J Guo BP et al. Persistent brain infection and disease reactivation in relapsing fever borreliosis. Microbes Infect, 2006; 8:2213–2219.

11.

Masuzawa T Beppu Y Kawabata H Yanagihara Y et al. Experimental Borrelia burgdorferi infection of outbred mice. J Clin Microbiol, 1992; 30:3016–3018.

12.

Mun

, Eisen

, Lane

. Detection of a Borrelia miyamotoi sensu lato relapsing-fever group spirochete from Ixodes pacificus in California. J Med Entomol, 2006; 43:120–123.

13.

Nakao

, Miyamoto

. Reservoir competence of the wood mouse, Apodemus speciosus ainu, for the Lyme disease spirochete, Borrelia burgdorferi, in Hokkaido, Japan. Jpn J Sanit Zool, 1993; 44:69–84.

14.

Nakao M Miyamoto K Fukunaga M Hashimoto Y et al. Comparative studies on Borrelia afzelii isolated from a patient of Lyme disease, Ixodes persulcatus ticks, and Apodemus speciosus rodents in Japan. Microbiol Immunol, 1994; 38:413–420.

15.

Ohdachi

, Ishibashi

, Iwasa

, Saitoh

. The Wild Mammals of Japan. Kyoto: Mammalogical Society of Japan, 2009; 141–181.

16.

Platonov AE Karan LS Kolyasnikova NM Makhneva NA et al. Humans infected with relapsing fever spirochete Borrelia miyamotoi, Russia. Emerg Infect Dis, 2011; 17:1816–1823.

17.

Richter

, Debski

, Hubalek

, Muatuschka

. Absence of Lyme disease spirochetes in larval Ixodes ricinus ticks. Vector Borne Zoonot Dis, 2012; 12:21–27.

18.

Rodent anesthesia using open-drop exposure to isoflurane [Internet]. Milwaukee: University of Wisconsin-Milwaukee, Animal Care Program. c2010(cited February 29, 2011)http://www4.uwm.edu/usa/acp/anesthesia/open-drop.cfm/.

19.

Sato Y Konishi T Hashimoto Y Takahashi H et al. Rapid diagnosis of Lyme disease: Flagellin gene-based nested polymerase chain reaction for identification of causative Borrelia species. Int J Infect Dis, 1997; 2:64–73.

20.

Schwan

, Karstens

, Schrumpf

, Simpson

. Changes in antigenic reactivity of Borrelia burgdorferi, the Lyme disease spirochete, during persistent infection in mice. Can J Microbiol, 1991; 37:450–454.

21.

Scoles

, Papero

, Beati

, Durland

. A relapsing fever group spirochete transmitted by Ixodes scapularis ticks. Vector Borne Zoonot Dis, 2001; 1:21–34.

22.

Takano A Goka K Une Y Shimada Y et al. Isolation and characterization of a novel Borrelia group of tick-borne borreliae from imported reptiles and their associated ticks. Environ Microbiol, 2010; 12:134–146.

23.

Takano A Nakao M Masuzawa T Takada N et al. Multilocus sequence typing implicates rodents as the main reservoir host of human-pathogenic Borrelia garinii in Japan. J Clin Microbiol, 2011; 49:2035–2039.

24.

Yamaguti

, Tipton

, Keegan

, Toshioka

. Ticks of Japan, Korea, and the Ryukyu Islands. Provo, Utah: Brigham Young University Science Bulletin, 1971.

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