Tick Surveillance for Relapsing Fever Spirochete Borrelia miyamotoi in Hokkaido, Japan

Takano, Ai; Toyomane, Kochi; Konnai, Satoru; Ohashi, Kazuhiko; Nakao, Minoru; Ito, Takuya; Andoh, Masako; Maeda, Ken; Watarai, Masahisa; Sato, Kozue; Kawabata, Hiroki

doi:10.1371/journal.pone.0104532

Cited by 84 publications

(78 citation statements)

References 28 publications

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“…persulcatus is a major tick species causing human tick bites and is an important vector of many tick-borne diseases, including human Lyme borreliosis (Borrelia afzelii and B. garinii), relapsing fever (B. miyamotoi), tick-borne encephalitis virus (TBEV; far eastern and Siberian subtypes), and neoehrlichiosis ("Candidatus Neoehrlichia mikurensis") in Russia and in northern regions of China and Japan where the tick is abundant (46)(47)(48)(49)(50). Human babesiosis caused by B. microti U.S. lineage has not been clearly documented in these areas, with the exception of China (51).…”

Section: Discussionmentioning

confidence: 99%

Ixodes persulcatus Ticks as Vectors for the Babesia microti U.S. Lineage in Japan

Zamoto-Niikura

Morikawa

Hanaki

et al. 2016

Appl Environ Microbiol

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The U.S. lineage, one of the major clades in the Babesia microti group, is known as a causal agent of human babesiosis mostly in the northeastern and upper midwestern United States. This lineage, however, also is distributed throughout the temperate zone of Eurasia with several reported human cases, although convincing evidence of the identity of the specific vector(s) in this area is lacking. Here, the goal was to demonstrate the presence of infectious parasites directly in salivary glands of Ixodes persulcatus, from which U.S. lineage genetic sequences have been detected in Asia, and to molecularly characterize the isolates. Five PCRpositive specimens were individually inoculated into hamsters, resulting in infections in four; consequently, four strains were newly established. Molecular characterization, including 18S rRNA, ␤-tubulin, and CCT7 gene sequences, as well as Western blot analysis and indirect fluorescent antibody assay, revealed that all four strains were identical to each other and to the U.S. lineage strains isolated from rodents captured in Japan. The 18S rRNA gene sequence from the isolates was identical to those from I. persulcatus in Russia and China, but the genetic and antigenic profiles of the Japanese parasites differ from those in the United States and Europe. Together with previous epidemiological and transmission studies, we conclude that I. persulcatus is likely the principal vector for the B. microti U.S. lineage in Japan and presumably in northeastern Eurasia. IMPORTANCEThe major cause of human babesiosis, the tick-borne blood parasite Babesia microti, U.S. lineage, is widely distributed in the temperate Northern Hemisphere. However, the specific tick vector(s) remains unidentified in Eurasia, where there are people with antibodies to the B. microti U.S. lineage and cases of human babesiosis. In this study, the first isolation of B. microti U.S. lineage from Ixodes persulcatus ticks, a principal vector for many tick-borne diseases, is described in Japan. Limited antigenic cross-reaction was found between the Japan and United States isolates. Thus, current serological tests based on U.S. isolates may underestimate B. microti occurrence outside the United States. This study and previous studies indicate that I. persulcatus is part of the B. microti U.S. lineage life cycle in Japan and, presumably, northeastern Eurasia. This report will be important for public health, especially since infection may occur through transfusion, and also to researchers in the field of parasitology.

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Section: Discussionmentioning

confidence: 99%

Ixodes persulcatus Ticks as Vectors for the Babesia microti U.S. Lineage in Japan

Zamoto-Niikura

Morikawa

Hanaki

et al. 2016

Appl Environ Microbiol

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“…Differences exist between B. miyamotoi isolates according to tick vector and geographic region, but so far little genetic difference has been found between isolates within a given geographic area or with the same tick vector association [4,18,29]. The overall genetic difference between a North American B. miyamotoi isolate (LB-2001) and a Japanese B. miyamotoi isolate (FR64b) is about the same as between B. turicatae and B. parkeri , two North American relapsing fever species with different host and vector associations [31], but less than between the two major genomic groups of B. hermsii strains [46] (Figure 1).…”

Section: The Organismmentioning

confidence: 99%

Borrelia miyamotoi infection in nature and in humans

Krause

Fish

Narasimhan

et al. 2015

Clinical Microbiology and Infection

217

189

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Borrelia miyamotoi is a relapsing fever Borrelia group spirochete that is transmitted by the same hard-bodied (ixodid) tick species that transmit the agents of Lyme disease. It was discovered in 1994 in Ixodes persulcatus ticks in Japan. B. miyamotoi species phylogenetically cluster with the relapsing fever group spirochetes, which usually are transmitted by soft-bodied (argasid) ticks or lice. B. miyamotoi infects at least six Ixodes tick species in North America and Eurasia that transmit Lyme disease group spirochetes and may use small rodents and birds as reservoirs. Human cases of B. miyamotoi infection were first reported in 2011 in Russia and subsequently in the United States, Europe, and Japan. These reports document the public health importance of B. miyamotoi, as human B. miyamotoi infection appears to be comparable in frequency to babesiosis or human granulocytic anaplasmosis in some areas and may cause severe disease, including meningoencephalitis. The most common clinical manifestations of B. miyamotoi infection are fever, fatigue, headache, chills, myalgia, arthralgia, and nausea. Symptoms of B. miyamotoi infection generally resolve within a week of the start of antibiotic therapy. B. miyamotoi infection should be considered in patients with acute febrile illness who have been exposed to Ixodes ticks in a region where Lyme disease occurs. Because clinical manifestations are non-specific, etiologic diagnosis requires confirmation by blood smear examination, PCR, antibody assay, in vitro cultivation, and/or isolation by animal inoculation. Antibiotics that have been used effectively include doxycycline for uncomplicated B. miyamotoi infection in adults and ceftriaxone or penicillin G for meningoencephalitis.

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“…Ixodes ticks concomitantly transmit spirochetes belonging to the Borrelia burgdorferi sensu lato group, which are known to cause Lyme borreliosis (3). The incidence of B. miyamotoi in Ixodes ticks is lower than that of B. burgdorferi sensu lato, with infection rates ranging from 0 to 15.4% in the United States and as high as 4% in Europe and Japan (2,4,5). RF Borrelia spirochetes cause a variety of diseases, which are characterized by episodes of high fever separated by periods of relative well-being.…”

mentioning

confidence: 99%

In Vitro Susceptibility of the Relapsing-Fever Spirochete Borrelia miyamotoi to Antimicrobial Agents

Koetsveld

Draga

Wagemakers

et al. 2017

Antimicrob Agents Chemother

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Hard-tick-borne relapsing fever (HTBRF) is an emerging infectious disease throughout the temperate zone caused by the relapsing-fever spirochete Borrelia miyamotoi. Antibiotic treatment of HTBRF is empirically based on the treatment of Lyme borreliosis; however, the antibiotic susceptibility of B. miyamotoi has not been studied to date. Thus, we set out to determine the in vitro antimicrobial susceptibility of B. miyamotoi. A microdilution method with 96-well microtiter plates was used to determine the antibiotic susceptibilities of two B. miyamotoi strains isolated on two different continents (Asia and North America), two Borrelia burgdorferi sensu lato strains, and one Borrelia hermsii isolate for purposes of comparison. The MIC and minimal bactericidal concentration (MBC) were determined by both microscopy and colorimetric assays. We were able to show that relative to the B. burgdorferi sensu lato isolates, both B. miyamotoi strains and B. hermsii demonstrated greater susceptibility to doxycycline and azithromycin, equal susceptibility to ceftriaxone, and resistance to amoxicillin in vitro. The MIC and MBC of amoxicillin for B. miyamotoi evaluated by microscopy were 16 to 32 mg/liter and 32 to 128 mg/liter, respectively. Since B. miyamotoi is susceptible to doxycycline, azithromycin, and ceftriaxone in vitro, our data suggest that these antibiotics can be used for the treatment of HTBRF. Oral amoxicillin is currently used as an alternative for the treatment of HTBRF; however, since we found that the B. miyamotoi strains tested were resistant to amoxicillin in vitro, this issue warrants further study. KEYWORDS hard-tick-borne relapsing fever, relapsing-fever borrelia, Borrelia miyamotoi, Borrelia miyamotoi disease, antibiotic susceptibility, antimicrobials T he relapsing-fever spirochete Borrelia miyamotoi was first described in Japan in 1995 (1). While it is phylogenetically closely related to other relapsing-fever (RF) spirochetes, such as Borrelia hermsii, Borrelia turicatae (transmitted by soft ticks), and Borrelia recurrentis (transmitted by body lice), it is transmitted by hard-bodied Ixodes ticks across the temperate zone (2). Ixodes ticks concomitantly transmit spirochetes belonging to the Borrelia burgdorferi sensu lato group, which are known to cause Lyme borreliosis (3). The incidence of B. miyamotoi in Ixodes ticks is lower than that of B. burgdorferi sensu lato, with infection rates ranging from 0 to 15.4% in the United States and as high as 4% in Europe and Japan (2, 4, 5). RF Borrelia spirochetes cause a variety of diseases, which are characterized by episodes of high fever separated by periods of relative well-being. The clinical presentation of disease caused by B. miyamotoi, however, appears to differ from that of classical RF, since relapsing-fever episodes have been observed only in 10% of patients infected with B. miyamotoi, and their levels of spirochetemia are calculated to be low (6, 7). Since most patients with B. miyamotoi infection are usually treated with antibiotics, this ...

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Tick Surveillance for Relapsing Fever Spirochete Borrelia miyamotoi in Hokkaido, Japan

Cited by 84 publications

References 28 publications

Ixodes persulcatus Ticks as Vectors for the Babesia microti U.S. Lineage in Japan

Ixodes persulcatus Ticks as Vectors for the Babesia microti U.S. Lineage in Japan

Borrelia miyamotoi infection in nature and in humans

In Vitro Susceptibility of the Relapsing-Fever Spirochete Borrelia miyamotoi to Antimicrobial Agents

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