We investigated the prevalence of Bartonella washoensis in California ground squirrels (Otospermophilus beecheyi) and their fleas from parks and campgrounds located in seven counties of California. Ninety-seven of 140 (69.3%) ground squirrels were culture positive and the infection prevalence by location ranged from 25% to 100%. In fleas, 60 of 194 (30.9%) Oropsylla montana were found to harbor Bartonella spp. when screened using citrate synthase (gltA) specific primers, whereas Bartonella DNA was not found in two other flea species, Hoplopsyllus anomalus (n = 86) and Echidnophaga gallinacea (n = 6). The prevalence of B. washoensis in O. montana by location ranged from 0% to 58.8%. A majority of the gltA sequences (92.0%) recovered from ground squirrels and fleas were closely related (similarity 99.4–100%) to one of two previously described strains isolated from human patients, B. washoensis NVH1 (myocarditis case in Nevada) and B. washoensis 08S-0475 (meningitis case in California). The results from this study support the supposition that O. beecheyi and the flea, O. montana, serve as a vertebrate reservoir and a vector, respectively, of zoonotic B. washoensis in California.
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References
1.
AngelakkisE, LepidiH, CanelA, RispalP, et al.Human case of Bartonella alsatica lymphadenitis. Emerg Infect Dis, 2008; 14:1951–1952.
2.
BaiY, KosoyM, MartinA, RayC, et al.Characterization of Bartonella strains isolated from black-tailed prairie dogs (Cynomys ludovicianus). Vector Borne Zoonotic Dis, 2008; 4:1–5.
3.
BilleterS, GundiVA, RoodMP, KosoyMY. Molecular detection and identification of Bartonella species in Xenopsylla cheopis fleas (Siphonaptera: Pulicidae) collected from Rattus norvegicus rats in Los Angeles, California. Appl Environ Microbiol, 2011; 77:7850–7852.
4.
BownKJ, EllisBA, BirtlesRJ, DurdenLA, et al.New world origins for haemoparasites infecting United Kingdom grey squirrels (Sciurus carolinensis), as revealed by phylogenetic analysis of Bartonella infecting squirrel populations in England and the United States. Epidemiol Infect, 2002; 129:647–653.
5.
BreitschwerdtEB. Bartonellosis: One health perspective for an emerging infectious disease. ILAR J, 2014; 55:46–58.
6.
BuffetJP, KosoyM, Vayssier-TaussatM. Natural history of Bartonella infecting rodents in light of new knowledge on genomics, diversity, and evolution. Future Microbiol, 2013; 8:1117–1128.
7.
ChangCC, ChomelBB, KastenRW, RomanoV, et al.Molecular evidence of Bartonella spp. in questing adult Ixodes pacificus ticks in California. J Clin Microbiol, 2001; 39:1221–1226.
8.
ChomelBB, KastenRW, WilliamC, WeyAC, et al.Bartonella endocarditis: A pathology shared by animal reservoirs and Patients. Ann N Y Acad Sci, 2009; 1166:120–126.
9.
ChomelBB, WeyAC, KastenRW. Isolation of Bartonella washoensis from a dog with mitral valve endocarditis. J Clin Microbiol, 2003; 41:5327–5332.
10.
DalyJS, WorthingtonMG, BrennerDJ, MossCW, et al.Rochalimae elizabethae sp. nov. isolated from a patient with endocarditis. J Clin Microbiol, 1993; 31:872–881.
11.
DavisRM, SmithRT, MadonMB, Sitko-CleughE. Flea, rodent, and plague ecology at Chuchupate Campground, Ventura County, California. J Vector Ecol, 2002; 27:107–125.
12.
DengH, Le RhunD, BuffetJ, CottéV, et al.Strategies of exploitation of mammalian reservoirs by Bartonella species. Vet Res, 2012; 43:15.
13.
DinizPP, MaggiRG, SchwartzDS, CadenasMB, et al.Canine bartonellosis: Serological and molecular prevalence in Brazil and evidence of co-infection with Bartonella henselae and Bartonella vinsonii subsp. berkhoffii. Vet Res, 2007; 38:697–710.
14.
FurmanD, CattsEP. Manual of Medical Entomology, 4th edition. United Kingdom: Cambridge University Press, 1982:138–157.
15.
GundiVA, BilleterS, RoodMP, KosoyMY. Bartonella spp. in rats and zoonoses, Los Angeles, California, USA. Emerg Infect Dis, 2012; 18:631–633.
16.
GutiérrezR, KrasnovB, MorickD, GottliebY, et al.Bartonella infection in rodents and their flea ectoparasites: An overview. Vector-Borne Zoonot, 2015; 15:27–39.
17.
HubbartJA, JachowskiDS, EadsDA. Seasonal and among-site variation in the occurrence and abundance of fleas on California ground squirrels (Otospermophilus beecheyi). J Vector Ecol, 2011; 36:117–123.
18.
InoueK, KabeyaH, HagiyaK, KosoyMY, et al.Multi-locus sequence analysis reveals host specific association between Bartonella washoensis and squirrels. Vet Microbiol, 2011; 148:60–65.
19.
InoueK, MaruyamaS, KabeyaH, HagiyaK, et al.Exotic small mammals as potential reservoirs of zoonotic Bartonella spp. Emerg Infect Dis, 2009; 15:526–532.
20.
JardineC, AppleyardG, KosoyMY, McCollD, et al.Rodent-associated Bartonella in Saskatchewan, Canada. Vector-Borne Zoonot, 2005; 5:402–409.
KerkhoffFT, BergmansAM, van Der ZeeA, RothovaA. Demonstration of Bartonella grahamii DNA in ocular fluid of a patient with neuroretinitis. J Clin Microbiol, 1999; 37:4034–4038.
23.
KosoyM, MurrayM, GilmoreRDJr, BaiY, et al.Bartonella strains from ground squirrels are identical to Bartonella washoensis isolated from a human patient. J Clin Microbiol, 2003; 41:645–650.
24.
MetzgerME, RustME. Abiotic factors affecting the development of fleas (Siphonaptera) of California Ground Squirrels (Rodentia: Sciuridae) in southern California, USA. Proceedings of the 3rd International Conference on Urban Pests, Prague, Czech Republic, 1999.
25.
NormanAF, RegneryR, JamesonP, GreeneC, et al.Differentiation of Bartonella-like isolates at the species level by PCR restriction fragment length polymorphism in the citrate synthase gene. J Clin Microbiol, 1995; 33:1797–1803.
26.
ProbertW, LouieJK, TuckerJR, LongoriaR, et al.Meningitis due to a “Bartonella washoensis”—like human pathogen. J Clin Microbiol, 2009; 47:2332–2335.
27.
RenestoP, GouvernetJ, DrancourtM, RouxV, et al.Use of rpoB gene analysis for detection and identification of Bartonella species. J Clin Microbiol, 2001; 39:430–437.
28.
RizzoMF, BilleterSA, OsikowiczL, Luna-CaipoDV, et al.Fleas and flea-associated Bartonella species in dogs and cats from Peru. J Med Entomol, 2015; 52:1374–1376.
29.
RubioAV, Ávila-FloresR, OsikowiczLM, BaiY, et al.Prevalence and genetic diversity of Bartonella strains in rodents from northwestern Mexico. Vector-Borne Zoonot, 2014; 14:838–845.
30.
SatoS, KabeyaH, MiuraT, SuzukiK, et al.Isolation and phylogenetic analysis of Bartonella species from wild carnivores of the suborder Caniformia in Japan. Vet Microbiol, 2012; 161:130–136.
31.
StarkHE, HudsonBW, PittmanB. Plague Epidemiology. Atlanta, GA: U.S. Department of Health and Human Services, Centers for Disease Control and Prevention, 1966.
32.
U.S. Department of Health. Pictorial Keys to Arthropods, Reptiles, Birds and Mammals of Public Health Significance. Atlanta, GA: U.S. Department of Health, Education and Welfare Public Health Service Communicable Disease Center, 1966.
33.
WelchDF, CarrollKC, HofmeisterEK, PersingDH, et al.Isolation of a new subspecies, Bartonella vinsonii subsp. arupensis, from a cattle rancher: Identity with isolates found in conjunction with Borelia burgdoferi and Babesia microti among naturally infected mice. J Clin Microbio, 1999; 37:2598–2601.
34.
ZeaiterZ, FournierPE, OgataH, RaoultD. Phylogenetic classification of Bartonella species by comparing groEL sequences. Int J Syst Eco Microbiol, 2002a; 52:165–171.
35.
ZeaiterZ, LiangZ, RaoultD. Genetic classification and differentiation of Bartonella species based on comparison of partial ftsZ gene sequences. J Clin Microbiol, 2002b; 40:3641–3647.
