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Bartonella spp. infection rate and B. grahamii in ticks.
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MedLine Citation:
PMID:  23017501     Owner:  NLM     Status:  MEDLINE    
Abstract/OtherAbstract:
Authors:
Elisabeth Janecek; Andreas Mietze; Ralph Goethe; Thomas Schnieder; Christina Strube
Publication Detail:
Type:  Letter    
Journal Detail:
Title:  Emerging infectious diseases     Volume:  18     ISSN:  1080-6059     ISO Abbreviation:  Emerging Infect. Dis.     Publication Date:  2012 Oct 
Date Detail:
Created Date:  2012-09-28     Completed Date:  2013-02-19     Revised Date:  2013-07-11    
Medline Journal Info:
Nlm Unique ID:  9508155     Medline TA:  Emerg Infect Dis     Country:  United States    
Other Details:
Languages:  eng     Pagination:  1689-90     Citation Subset:  IM    
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Bank Name/Acc. No.:
GENBANK/JK758018;  JO770304
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MeSH Terms
Descriptor/Qualifier:
Animals
Bartonella / classification*,  genetics*,  isolation & purification
Bartonella henselae / classification,  genetics*,  isolation & purification
Female
Germany
Humans
Ixodes / microbiology*
Male
Molecular Sequence Data
Seasons
Sequence Analysis, DNA
Ticks / microbiology
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From MEDLINE®/PubMed®, a database of the U.S. National Library of Medicine

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Journal Information
Journal ID (nlm-ta): Emerg Infect Dis
Journal ID (iso-abbrev): Emerging Infect. Dis
Journal ID (publisher-id): EID
ISSN: 1080-6040
ISSN: 1080-6059
Publisher: Centers for Disease Control and Prevention
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Print publication date: Month: 10 Year: 2012
Volume: 18 Issue: 10
First Page: 1689 Last Page: 1690
PubMed Id: 23017501
ID: 3471628
Publisher Id: 12-0390
DOI: 10.3201/eid1810.120390

Bartonella spp. Infection Rate and B. grahamii in Ticks Alternate Title:Bartonella spp. in Ticks
Elisabeth Janecek
Andreas Mietze
Ralph Goethe
Thomas Schnieder1
Christina Strube
University of Veterinary Medicine Hannover, Hanover, Germany
Correspondence: Address for correspondence: Christina Strube, Institute for Parasitology, University of Veterinary Medicine Hannover, Buenteweg 17, 30559 Hanover, Germany; email: christina.strube@tiho-hannover.de

To the Editor: Bacteria of the genus Bartonella are transmitted by arthropods and are often implicated in human disease. Even though ticks are known to transmit a variety of pathogens, vector competences for transmission of Bartonella spp. by ticks were speculative (1) until recently, when in vivo transmission of B. birtlesii by Ixodes ricinus ticks was demonstrated in mice (2). This finding suggests that this tick species, which is common in Europe, may also transmit zoonotic Bartonella spp. Evidence of possible tick transmission of bartonellae to humans under natural conditions was provided by Eskow et al. (3) and Angelakis et al. (4), who identified Bartonella spp. in tissue samples of patients who were recently bitten by ticks. We determined the prevalence of Bartonella spp. in questing I. ricinus ticks in the city of Hanover, Germany, which is nicknamed The Green Metropolis and was selected the German Capital of Biodiversity in 2011.

During April–October 2010, we collected 2,100 questing ticks, consisting of 372 adults (177 female and 195 male), 1,698 nymphs, and 30 larvae, from 10 recreation areas in Hanover. Tick DNA was extracted by using the NucleoSpin 8 Blood kit (Macherey-Nagel, Düren, Germany). Plasmid DNA constructed from B. henselae reference strain ATCC49793 containing the 249-bp target sequence of the gltA gene was used as positive control. Bartonella spp. in ticks was detected by quantitative PCR (qPCR) by using the Mx3005 Multiplex Quantitative PCR System (Stratagene, Heidelberg, Germany) according to the protocol described by Mietze et al. (5), with minor modifications. Samples positive by qPCR were verified by gel electrophoresis. Bartonella species were differentiated by sequencing (Eurofins MWG Operon, Ebersberg, Germany), and obtained sequences underwent BLAST (http://blast.ncbi.nlm.nih.gov/Blast.cgi) comparison to published sequences.

On the basis of the amplicon-specific melting temperature and DNA bands representing the specific size of 249-bp after gel electrophoresis, results of qPCR showed 100 (4.76%) infected I. ricinus ticks (Table). Positive results did not vary by developmental tick stages; 4.84% (18/372) adult ticks (5.08% [9/177] female and 4.62% [9/195] male), 4.71% (80/1,698) nymphs, and 6.67% (2/30) larvae were infected (Table). Because Bartonella spp. do not seem to be transmitted transovarially (6), it is likely that larvae had interrupted blood meals and thus did not take up enough blood to develop into the nymphal stage.

Seasonal changes in Bartonella spp. infection rates resulted in a higher peak in May (38/300 [12.67%]) than in the other months (Table). For sampling locations, infection rates for grassy sampling location 6 (4/210 [1.90%] infected ticks) differed significantly (Bonferroni-Holm adjusted p<0.001; *<0.0011) from that of densely wooded sampling location 9 (22/210 [10.48%] infected ticks).

Sequencing of the gltA fragment resulted in Bartonella species identification for 56/100 positive samples; 52 of these samples (from 38 nymphs, 13 adults, and 1 larva) were identified as infected with B. henselae. In 51 samples (92.86%), maximum identity with the BLAST top hit sequence was 99% because of nucleotide substitutions in position 198 (T→C) and in position 136 (A→G) of the 249-bp fragment. The remaining sample showed 100% identity with B. henselae strains Brazil-1 and 45-00249 (GenBank accession nos. HQ012580 and GQ225709).

Four of the 56 successfully sequenced samples (7.14%; all samples from nymphs) showed the sequence pattern of B. grahamii. One sample revealed 100% identity with B. grahamii (GenBank accession no. EU014266); the remaining 3 samples showed an identity of 98% with the B. grahamii strain Hokkaido-1 (GenBank accession no. AB426652) and 99% (T→C in position 93) with a sequence described as B. grahamii–like (GenBank accession no. AY435122). Sequences obtained in this study (deposited in GenBank under accession nos. JQ770304 and JK758018) support the genetic variability of Bartonella spp., as demonstrated by others (5,7,8).

It remains unclear whether ticks are involved in transmission of pathogenic Bartonella spp. to humans under natural conditions. However, the total prevalence rate of 4.76% (100/2,100) questing I. ricinus ticks infected with B. henselae and B. grahamii highlights the need for public awareness and draws attention to the possibility of an infection with zoonotic Bartonella spp. after a tick bite (3,4). B. henselae, the predominantly identified species, has been associated with cat scratch disease, peliosis hepatis, and bacillary angiomatosis in humans. Eskow et al. (3) also connected chronic symptoms of Lyme disease to co-infections with Borrelia burgdorferi and B. henselae. B. grahamii has been associated with neuroretinitis and ocular artery thrombosis in humans (9,10). The potential risk for zoonotic Bartonella spp. infection in urban recreation areas should not be underestimated.


Notes

Suggested citation for this article: Janecek E, Mietze A, Goethe R, Schnieder T, Strube C. Bartonella spp. infection rate and B. grahamii in ticks [letter]. Emerg Infect Dis [Internet]. 2012 Oct [date cited]. http://dx.doi.org/10.3201/eid1810.120390

1Deceased.

References
1. . BilleterSA, LevyMG, ChomelBB, BreitschwerdtEBVector transmission of Bartonella species with emphasis on the potential for tick transmission.Med Vet Entomol. Year: 2008;22:1–1510.1111/j.1365-2915.2008.00713.x18380649
2. . ReisC, CoteM, Le RhunD, LecuelleB, LevinML, Vayssier-TaussatM, et al. Vector competence of the tick Ixodes ricinus for transmission of Bartonella birtlesii.PLoS Negl Trop Dis. Year: 2011;5:e118610.1371/journal.pntd.000118621655306
3. . EskowE, RaoRV, MordechaiEConcurrent infection of the central nervous system by Borrelia burgdorferi and Bartonella henselae: evidence for a novel tick-borne disease complex.Arch Neurol. Year: 2001;58:1357–6310.1001/archneur.58.9.135711559306
4. . AngelakisE, BilleterSA, BreitschwerdtEB, ChomelBB, RaoultDPotential for tick-borne bartonelloses.Emerg Infect Dis. Year: 2010;16:385–9110.3201/eid1603.09168520202411
5. . MietzeA, MorickD, KohlerH, HarrusS, DehioC, NolteI, et al. Combined MLST and AFLP typing of Bartonella henselae isolated from cats reveals new sequence types and suggests clonal evolution.Vet Microbiol. Year: 2011;148:238–4510.1016/j.vetmic.2010.08.01220863631
6. . CottéV, BonnetS, Le RhunD, Le NaourE, ChauvinA, BoulouisHJ, et al. Transmission of Bartonella henselae by Ixodes ricinus.Emerg Infect Dis. Year: 2008;14:1074–8010.3201/eid1407.07111018598628
7. . ArvandM, SchubertH, ViezensJEmergence of distinct genetic variants in the population of primary Bartonella henselae isolates.Microbes Infect. Year: 2006;8:1315–2010.1016/j.micinf.2005.12.01516697237
8. . EhrenborgC, HandleyS, EllisB, MillsJ, HolmbergMBartonella grahamii infecting rodents display high genetic diversity over short geographic distances.Ann N Y Acad Sci. Year: 2003;990:233–510.1111/j.1749-6632.2003.tb07369.x12860632
9. . SerratriceJ, RolainJM, GranelB, EneN, ConrathJ, AvierinosJF, et al. Bilateral retinal artery branch occlusions revealing Bartonella grahamii infection.Rev Med Interne. Year: 2003;24:629–3010.1016/S0248-8663(03)00224-812951187
10. . KerkhoffFT, BergmansAM, van Der ZeeA, RothovaADemonstration of Bartonella grahamii DNA in ocular fluids of a patient with neuroretinitis.J Clin Microbiol. Year: 1999;37:4034–810565926

Tables
[TableWrap ID: T1] Table  Seasonal distribution of Ixodes ricinus ticks infected with Bartonella spp., Hanover, Germany, 2010*
Ticks April May June July August September October Total
No. infected ticks/no. tested (%) 5/300 (1.67) 38/300 (12.67) 7/300 (2.33) 10/300 (3.33) 5/300 (1.67) 17/300 (5.67) 18/300 (6.00) 100/2,100 (4.76)
No. (%) adults positive 1/88 (1.14) 8/48 (16.67) 0/39 0/41 2/56
(3.57) 3/53
(5.66) 4/47
(8.51) 18/372
(4.84)
No. (%) females 1/32 (3.13) 3/19
(15.79) 0/20 0/17 1/32
(3.13) 2/28
(7.14) 2/29
(6.90) 9/177
(5.08)
No. (%) males 0/56 5/29
(17.24) 0/19 0/24 1/24
(4.17) 1/25
(4.00) 2/18
(11.11) 9/195
(4.62)
No. (%) nymphs 3/203 (1.48) 30/248 (12.10) 7/261 (2.68) 10/259 (3.86) 3/244 (1.23) 14/240 (5.83) 13/243 (5.35) 80/1,698 (4.71)
No. (%) larvae 1/9 (11.11) 0/4 ND ND ND 0/7 1/10 (10.00) 2/30
(6.67)

*ND, testing not done.



Article Categories:
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Article Categories:
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Keywords: Keywords: Bartonella henselae, Bartonella grahamii, Ixodes ricinus, tickborne diseases, vector-borne infections, bacteria, Germany, zoonoses.

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