Rodents and soricomorphs are animal hosts of fleas and associated zoonotic microbial pathogens. A total of 4,889 small mammals were collected from Gyeonggi and Gangwon Provinces, Republic of Korea, from 2008 through 2010, including: Apodemus agrarius (4,122, 84.3%), followed by Crocidura lasiura (282, 5.8%), Microtus fortis (257, 5.3%), Myodes regulus (77, 1.6%), Micromys minutus (71, 1.5%), Mus musculus (63, 1.3%), and 4 other species (17, 0.3%). A total of 1,099 fleas belonging to 10 species and 7 genera were collected. Ctenophthalmus congeneroides (724, 65.9%) was the most commonly collected flea, followed by Stenoponia sidimi (301, 27.4%), Neopsylla bidentatiformis (29, 2.6%), and Rhadinopsylla insolita (25, 2.3%). The remaining species accounted for only 1.8% (20, range 1–6) of all fleas collected. The 2 dominant flea species, C. congeneroides and S. sidimi, showed an inverse seasonal pattern, with higher populations of C. congeneroides from January–September, whereas S. sidimi was more frequently collected during October–December. The overall flea infestation rates (FIR) and flea indices (FI) were 14.1% and 0.22, respectively, and were highest during April–June (19.7% and 0.30, respectively). A total of 735 of the 1,099 fleas were assayed for the detection of Bartonella spp. by PCR using Bartonella-specific primers, of which 515 were positive for Bartonella, with an overall maximum likelihood estimate (MLE) of 700.7/1,000. The highest MLE values were observed during April–June (899.2) and July–September (936.2) trapping periods and, although lower, were similar for January–March (566.7) and October–December (574.1). C. congeneroides demonstrated high MLEs for all seasons (range 752.5–934.8), while S. sidimi was positive for Bartonella only during January–March (MLE=342.1) and October–December (MLE=497.2) collection periods. Continued long-term surveillance of small mammals and associated ectoparasites is needed to improve our understanding of the prevalence of Bartonella spp. in fleas and the role of fleas in the zoonotic maintenance and transmission of Bartonella to humans.
BoulouisHJ, ChangCC, HennJB, KastenRWet al.Factors associated with the rapid emergence of zoonotic Bartonella infections. Vet Res, 2005; 36:383–410.
3.
ChaeJS, KimCM, KimEH, HurEJet al.Molecular epidemiological study for tick-borne disease (Ehrlichia and Anaplasma spp.) surveillance at selected U.S. military training sites/installations in Korea. Ann NY Acad Sci, 2003; 990:118–125.
4.
ChaeJS, AdjemianJZ, KimHC, KoSet al.Predicting the emergence of tick-borne infections based on climatic changes in Korea. Vector-Borne Zoonot Dis, 2008; 8:265–275.
5.
ChiltonNB, AndrewsRH, BullCM. Influence of temperature and relative humidity on the moulting success of Amblyomma limbatum and Aponomma hydrosauri (Acari: Ixodidae) larvae and nymphs. Int J Parasitol, 2000; 30:973–979.
6.
ComerJA, DiazT, VlahovD, MonterrosoEet al.Evidence of rodent-associated Bartonella and Rickettsia infections among intravenous drug users from central and east Harlem, New Your City. Am J Trop Med Hyg, 2001; 65:855–860.
7.
EisenRJ, EnscoreRE, BiggerstaffBJ, ReynoldsPJet al.Human plague in the southwestern United States, 1957-2004: Spatial models of elevated risk of human exposure to Yersinia pestis. J Med Entomol, 2007; 44:530–537.
8.
FelsensteinJ. Confidence limits on phylogenies: An approach using the bootstrap. Evolution, 1985; 39:783–791.
9.
FenollarF, SireS, RaoultD. Bartonella vinsonii subsp. arupensis as an agent of blood culture-negative endocarditis in a human. J Clin Microbiol, 2005; 43:945–947.
10.
FournierPE, NdihokubwayoJB, GuidranJ, KellyPJ. Human pathogens in body and head lice. Emerg Infect Dis, 2002; 8:1515–1518.
11.
GageKL. Fleas, the Siphonaptera. MarquardtWC. Biology of Disease Vectors, 2nd. San Diego, CA: Elsevier Academic, 2005; 77–92.
12.
HallTA. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser, 1999; 41:95–98.
13.
HanTH, ChungJY, SeongHK, KimSW. Molecular detection of Bartonella henselae DNA from fleas obtained from dog, Korea. Korean J Pediatr, 2006; 49:983–986.
14.
HongHK. Key to the species of Korean fleas (Siphonaptera) and their host relationship. Thesis Collection of Basic Science Institute, Incheon University, 1994; 5:183–200.
15.
HopkinsGHE, RothschildM. An Illustrated Catalogue of the Rothschild Collection of Fleas (Siphonaptera) in the British Museum. Cambridge, UK: Cambridge University Press, 1953; I:1–361.
16.
HopkinsGHE, RothschildM. An Illustrated Catalogue of the Rothschild Xollection of Fleas (Siphonaptera) in the British Museum. Cambridge, UK: Cambridge University Press, 1956; I:1–445.
17.
IraluJ, BaiY, CrookL, TempestBet al.Rodent-associated Bartonella illness, southwestern United States. Emerg Infect Dis, 2006; 5:402–409.
18.
JacomoV, KellyPJ, RaoultD. Natural history of Bartonella infections (an exception to Koch's postulate)Clin Diagn Lab Immunol, 2002; 9:8–18.
19.
JardineC, WaldnerC, WobeserG, LeightonFA. Effect of experimental ectoparasite control on Bartonella infections in wild Richardson's ground squirrels. J Wildl Dis, 2006; 42:750–758.
20.
KaremKL. Immune aspects of Bartonella. Crit Rev Microbiol, 2000; 26:133–145.
21.
KeeS, HwangKJ, OhHB, KimMBet al.Isolation and identification of Borrelia burgdorferi in Korea. J Korean Soc Microbiol, 1994; 29:301–310.
22.
KerkhoffFT, BergmansAMC, Van Der ZeeA, RothovaA. Demonstration of Bartonella grahamii DNA in ocular fluids of a patient with neuroretinitis. J Clin Microbiol, 1999; 37:4034–4038.
23.
KimCM, KimJY, YiYH, LeeMJet al.Detection of Bartonella species from ticks, mites and small mammals in Korea. J Vet Sci, 2005; 6:327–334.
24.
KimHC, YangYC, ChongST, KoSet al.Detection of Rickettsia typhi and seasonal prevalence of fleas collected from small mammals in the Republic of Korea. J Wildl Dis, 2010; 46:165–172.
25.
KimHC, KleinTA, KangHJ, GuSHet al.Ecological surveillance of small mammals at Dagmar North Training Area, Geyonggi Province, Republic of Korea, 2001–2005. J Vector Ecol, 2011; 36:42–54.
26.
KimYS, SeoKW, LeeJH, ChoiEWet al.Prevalence of Bartonella henselae and Bartonella clarridgeiae in cats and dogs in Korea. J Vet Sci, 2009; 10:85–87.
27.
KimuraM. A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide seqeuences. J Mol Evol, 1980; 16:111–120.
28.
KoS, KimHC, YangYC, ChongSTet al.Detection of Rickettsia felis and Rickettsia typhi and seasonal prevalence of fleas collected from small mammals at Gyeonggi Province in the Republic of Korea. Vector-Borne Zoonot Dis, 2011; 11:1243–1251.
29.
KobayashiH. Rat-fleas in Chosen. J Manchuria-Chosen Med Assoc, 1931; 129:1–2.
30.
KosoyM, MurrayM, GilmoreRDJr., BaiYet al.Bartonella strains from ground squirrels are identical to Bartonella washoensis isolated from a human patient. J Clin Microbiol, 2003; 41:645–650.
31.
LeeDK, LeeYK. Roles of Saemaul Undong in reforestation and NGO activities for sustainable forest management in Korea. Paper presented at the IUFRO Science/Policy Interface Task Force regional meeting held at the M.S. Swaminathan Research Foundation, Chennai, India, July 16–19, 2002, 1–13.
32.
LeeJH, ParkHS, JungKD, JangWJet al.Identification of the spotted fever group rickettsiae detected from Haemaphysalis longicornis in Korea. Microbiol Immunol, 2003; 47:301–304.
33.
MorwayC, KosoyM, EisenR, MontenieriJet al.A longitudinal study of Bartonella infection in populations of wood rats and their fleas. J Vector Ecol, 2008; 33:353–364.
34.
NagahanaM. Rat-flea survey in Chosen (Korea). I. Species and distribution of rat-flea in Chosen. J Chosen Med Assoc, 1937; 27:1637–1644.
35.
NagahanaM. Rat-flea survey in Chosen (Korea). III. Rat-flea survey of the Port of Busan. J Chosen Med Assoc, 1938; 28:964–970.
36.
NagahanaM. Studies on rat-fleas of Korea. Jap J Sanit Zool(special edition of Dr. Harujiro Kobayashi Jubilee Publication)1954; 4:260–290.
37.
NietoNC, DabritzH, FoleyP, DrazenovichNet al.Ecotoparasite diversity and exposure to vector-borne disease agents in wild rodents in central coastal California. J Med Entomol, 2007; 44:328–335.
38.
O'GuinnML, KleinTA, LeeJS, RichardsALet al.Serological surveillance of scrub typhus, murine typhus, and leptospirosis in small mammals captured at firing points 10 and 60, Gyeonggi Province, Republic of Korea, 2001–2005. Vector-Borne Zoonot Dis, 2010; 10:125–133.
39.
ParkKH, LeeSH, WonWJ, JangWJet al.Isolation of Borrelia burgdorferi, the causative agent of Lyme disease, from Ixodes ticks in Korea. J Korean Soc Microbiol, 1992; 27:307–312.
40.
RenestoP, GouvernetJ, DrancourtM, RouxVet al.Use of rpoB gene analysis for detection and identification of Bartonella species. J Clin Microbiol, 2001; 39:430–437.
41.
RichardsAL, SoeatmadjiDW, WidodoMA, SardjonoTWet al.Seroepidemiologic evidence for murine and scrub typhus in Malang, Indonesia. Am J Trop Med Hyg, 1997; 57:91–95.
42.
SaitouN, NeiM. The neighbor-joining method: A new method for reconstructing phylogenetic trees. Mol Biol Evol, 1987; 4:406–425.
43.
SmithHM, ReporterR, RoodMP, LinscottAJet al.Prevalence study of antibody to rat-borne pathogens and other agents among patients using a free clinic in downtown Los Angeles. J Infect Dis, 2002; 186:1673–1678.
44.
SongJW, MoonSS, GuSH, SongKJet al.Hemorrhagic fever with renal syndrome in 4 US soldiers, South Korea, 2005. Emerg Infect Dis, 2009; 15:1833–1836.
TapperoJW, KoehlerJE, BergerTG, CockerellCJet al.Bacillary angiomatosis and bacillary splenitis in immunocompetent adults. Ann Intern Med, 1993; 118:363–365.
47.
TiptonVJ, SouthwickW, AhHS, YuHS. Fleas of Korea. Korean J Parsitol, 1972; 10:52–63.
48.
TsukaharaM, TsuneokaH, IinoH, MuranoIet al.Bartonella henselae infection as a cause of fever of unknown origin. J Clin Microbiol, 2000; 38:1990–1991.
49.
WelchDF, CarrollKC, HofmeisterEK, PersingDHet al.Isolation of a new subspecies, Bartonella vinsonii subsp. arupenis, from a cattle rancher: Identity with isolates found in conjunction with Borrelia burgdorferi and Babesia microti among naturally infected mice. J Clin Microbiol, 1999; 37:2598–2601.
50.
WaltonDW, HongHK. Fleas of small mammals from the endemic hemorrhagic fever zones of Kyonggi and Kangwon province of the Republic of Korea. Korean J Parsitol, 1976; 14:17–24.
