Bartonella henselae in Ixodes ricinus ticks (Acari: Ixodida) removed from humans, Belluno Province, Italy. (Research).The potential role of ticks as vectors of Bartonella species has recently been suggested. In this study, we investigated the presence of Bartonella species in 271 ticks removed from humans in Belluno Province, Italy. By using primers derived from the 60-kDa heat shock protein heat shock protein n. Any of a group of cellular proteins that are produced under conditions of heat stress and help to stabilize other cellular proteins exposed to high temperatures. gene sequences, Bartonella DNA DNA: see nucleic acid. DNA or deoxyribonucleic acid One of two types of nucleic acid (the other is RNA); a complex organic compound found in all living cells and many viruses. It is the chemical substance of genes. was amplified and sequenced from four Ixodes ricinus ticks (1.48%). To confirm this finding, we performed amplification and partial sequencing of the pap31 protein and the cell division protein ftsZ encoding genes. This process allowed us to definitively identify B. henselae (genotype Houston-1) DNA in the four ticks. Detection of B. henselae in these ticks might represent a highly sensitive form of xenodiagnosis xenodiagnosis /xeno·di·ag·no·sis/ (-di?ag-no´sis) a method of animal inoculation using laboratory-bred bugs and animals in the diagnosis of certain parasitic infections when the infecting organism cannot be demonstrated in blood films; . B. henselae is the first human-infecting Bartonella identified from Ixodes ricinus, a common European tick and the vector of various tickborne pathogens. The role of ticks in the transmission of bartonellosis should be further investigated. ********** Bartonella species are facultative intracellular bacteria associated with a number of emerging anthropozoonoses. They have been detected in or isolated from diverse vertebrate hosts, including humans (1-3), various intradomicillary mammals (4-7), and a wide range of wild animals WILD ANIMALS. Animals in a state of nature; animals ferae naturae. Vide Animals; Ferae naturae. (8,9), which serve as natural vertebrate hosts. Various hematophagous hematophagous subsisting on blood, e.g. hematophagous flies. arthropods have been implicated im·pli·cate tr.v. im·pli·cat·ed, im·pli·cat·ing, im·pli·cates 1. To involve or connect intimately or incriminatingly: evidence that implicates others in the plot. 2. in the ecoepidemiology of Bartonella species. B. bacilliformis, the etiologic agent of Carrion disease, is transmitted by the sand fly (Lutzomyia verrucarum) in the Andes Mountains in Peru, Columbia, and Ecuador (10). B. quintana, the agent of trench fever trench fever: see rickettsia. and bacillary angiomatosis Bacillary Angiomatosis Definition A life-threatening but curable infection that causes an eruption of purple lesions on or under the skin that resemble Kaposi's sarcoma. , is found worldwide and is transmitted by the human body louse body louse n. A parasitic louse that infests the body and clothes of humans. (Pediculus humanus) (11). B. henselae is another cosmopolitan emerging human pathogen. This agent was first reported in 1990 in association with bacillary angiomatosis (12). The organism was later isolated from the blood of a febrile febrile /feb·rile/ (feb´ril) pertaining to or characterized by fever. feb·rile adj. Of, relating to, or characterized by fever; feverish. HIV-positive patient and subsequently described as a new species in 1992 (1). B. henselae is now recognized as the causative agent of cat-scratch disease (1), bacillary angiomatosis, peliosis hepatitis, oculoglandular syndrome, and endocarditis endocarditis (ĕn'dōkärdī`tĭs), bacterial or fungal infection of the endocardium (inner lining of the heart) that can be either acute or subacute. (13,14). B. henselae is associated with cats, which serve as its reservoir (13,15); the cat flea (Ctenocephalides felis) was demonstrated to be a vector (16). Other Bartonella-flea associations are apparent: for example, 61% of rat fleas (Xenopsylla cheopis) were found infected with bartonellae, including a known human pathogen, B. elizabethae (7). Polymerase chain reaction polymerase chain reaction (pŏl`ĭmərās') (PCR), laboratory process in which a particular DNA segment from a mixture of DNA chains is rapidly replicated, producing a large, readily analyzed sample of a piece of DNA; the process is (PCR PCR polymerase chain reaction. PCR abbr. polymerase chain reaction Polymerase chain reaction (PCR) ) amplification and sequence analysis of various genes are now widely used to differentiate Bartonella species. The 16S/23S rRNA intergenic spacer region (17), the heat shock protein (groEL) gene (18), the citrate synthase gene (gltA) (19), the riboflavin synthase achain gene (ribC) (20), the cell division protein (ftsZ) (21), and the pap31 (22) gene sequences were used for detecting, identifying, and classifying the phylogenetic phy·lo·ge·net·ic adj. 1. Of or relating to phylogeny or phylogenetics. 2. Relating to or based on evolutionary development or history. properties and subtyping of Bartonella isolates. Ticks are vectors of more diverse microorganisms than any other arthropod arthropod Any member of the largest phylum, Arthropoda, in the animal kingdom. Arthropoda consists of more than one million known invertebrate species in four subphyla: Uniramia (five classes, including insects), Chelicerata (three classes, including arachnids and horseshoe vector (23). The sheep tick (Ixodes ricinus) is the most common hard tick species in western Europe and has been established as the vector of tick-borne encephalitis virus tick-borne encephalitis virus n. An arbovirus of the genus Flavivirus that occurs in two subtypes, Central European and Eastern, causing two forms of encephalitis; it is transmitted by ticks. , Babesia Babesia /Ba·be·sia/ (bah-be´ze-ah) a genus of protozoa found as parasites in red blood cells and transmitted by ticks; its numerous species include B. bige´mina, B. bo´vis, and B. sp., Borrelia burgdorferi, Rickettsia rickettsia (rĭkĕt`sēə), any of a group of very small microorganisms, many disease-causing, that live in vertebrates and are transmitted by bloodsucking parasitic arthropods such as fleas, lice (see louse), and ticks. helvetica, and the agent of granulocytic granulocytic pertaining to granulocytes. granulocytic leukemia see myelocytic leukemia. granulocytic sarcoma extramedullary growth of multiple, focal granulocytic neoplasm. They may be neutrophilic or eosinophilic. ehrlichiosis, Anaplasma phagocytophila, (24). I. ricinus feeds on a large number of vertebrate hosts. The immature stages of I. ricinus are found mainly on small-size vertebrates and can readily feed on humans. Ticks have been suspected to transmit Bartonella (25). However, evidence of Bartonella infection in ticks has only recently been reported (26,27). Although these observations suggest the possibility of Bartonella transmission by ticks, more precise identification of these tick-infecting agents is required to establish their zoonotic potential. Materials and Methods Tick Collection and Identification During 2000-2001, a total of 271 ticks were removed from asymptomatic persons who visited first aid departments in Belluno Province, Italy, for assistance with tick bites. Ticks were removed with tweezers tweezers An instrument with pincers used to grasp or extract. See Optical tweezers. by grasping their mouthpart and pulling straight out from the skin. The tick-bite site was disinfected Disinfected Decreased the number of microorganisms on or in an object. Mentioned in: Isolation , and individual ticks were placed in sterile tubes and kept frozen at -70[degrees]C for further study. The ticks were stored on ice during the identification procedure, which was done on the basis of their morphologic features by using standard taxonomic keys. Tick DNA Extraction All ticks were disinfected by immersion into a 70% ethanol solution for 5 min, rinsed with sterile water, and dried in a sterile filter paper. Ticks were then subjected to DNA extraction by using the QiaAmp tissue kit procedure (QIAGEN GmbH, Hilden, Germany). DNA was extracted from ticks according to the manufacturer's protocol. To serve as a negative control, DNA of lice from a laboratory colony that had been fed on an uninfected rabbit was extracted, along with tick DNA, to serve as control. DNA was eluted in a final volume of 200 [micro]L and stored at 4[degrees]C until studied further. PCR Screening of Ticks for the Presence of Bartonella Tick DNA was screened by PCR amplification of the heat-shock protein-encoding gene (groEL) sequences for the presence of Bartonella. Primers HSPF HSPF Hydrological Simulation Program–Fortran HSPF Heating Season Performance Factor 1d and BbHS1630.n were used as described (22) and are listed in the Table. Subtyping of Detected Bartonella with pap31 and ftsZ Partial Sequences Amplification Primers used for amplification sequencing of each gene are listed in the Table. PCR reactions were performed in a Peltier model PTC-200 thermal cycler (MJ Research, Inc., Watertown, MA). PCR was carried out in a total volume of 50 [micro]L, consisting of 10 pmol of each primer, 0.5 U of ELONGase mix enzyme (GibcoBRL, Cergy Pontoise, France), 20 mM concentration of each deoxynucleoside phosphate, and 1.8 mM of MgC12. Two negative controls were included in the reaction: DNA from uninfected lice, and the master mix with sterile water instead of the DNA template. DNA from a culture of B. elizabethae was used as the positive control. The following amplification program was used: a first denaturation denaturation, term used to describe the loss of native, higher-order structure of protein molecules in solution. Most globular proteins exhibit complicated three-dimensional folding described as secondary, tertiary, and quarternary structures. step at 94[degrees]C for 4 min was followed by 44 cycles of denaturation at 94[degrees]C for 30 s, annealing annealing (ənēl`ĭng), process in which glass, metals, and other materials are treated to render them less brittle and more workable. at temperatures corresponding to each gene (53[degrees]C for groEL and pap31 genes and 55[degrees]C for ftsZ) for 30 s, and a hybridization hybridization /hy·brid·iza·tion/ (hi?brid-i-za´shun) 1. crossbreeding; the act or process of producing hybrids. 2. molecular hybridization 3. step at 68[degrees]C for 1 min. The amplification reaction was terminated with a further extension step at 68[degrees]C for 10 min. PCR products were visualized under UV illumination after electrophoresis migration on a 1% gel agarose agarose more highly purified form of agar with similar uses to agar and widely used in the separation of nucleic acid fragments. stained with ethidium bromide. Sequencing PCR products were purified by the QIAquick PCR purification kits (QIAGEN GmbH) as recommended by the manufacturer. Primers used for the sequencing of each gene are listed in the Table. PCR products were sequenced in both directions by using the d-Rhodamine Terminator Cycle Sequencing Ready Reaction kit (PerkinElmer, Inc., Coignieres, France) according to the manufacturer's recommendations. Sequencing products were resolved in an Applied Biosystem automatic sequencer See MIDI sequencer. (music) sequencer - Any system for recording and/or playback of music via a programmable memory which stores music not as audio data, but as some representation of notes. model 3100 (PerkinElmer). Sequence Analysis Nucleotide sequences were edited with the Autoassembler (version 1.4; Perkin Elmer) package. Multiple alignment with other Bartonella sp. sequences available from GenBank was carried out by using the Clustal W program (28). Results Of the 271 ticks collected from patients, 268 were I. ricinus (98.9%); the other specimens were one female I. hexagonus (0.4%), one female Rhipicephalus sanguineus (0.4%), and one female I. ventalloi (0.4%). Most of the ticks were nymphs (142; 52.3%), followed by females (115; 42.4%); larva larva, in zoology larva, independent, immature animal that undergoes a profound change, or metamorphosis, to assume the typical adult form. Larvae occur in almost all of the animal phyla; because most are tiny or microscopic, they are rarely seen. (10; 3.6%), and males (1; 0.4%). PCR Screening of Ticks for Bartonella By using primers HSPF1d and BbHS1630.n, a single band of PCR product of approximately 1,490 bp was amplified and sequenced in four I. ricinus ticks (two females and two nymphs) (1.48%). No amplification product was yielded from the negative controls. We used the BLAST tool (available from: URL URL in full Uniform Resource Locator Address of a resource on the Internet. The resource can be any type of file stored on a server, such as a Web page, a text file, a graphics file, or an application program. : http://www.ncbi.nlm.nih.gov/BLAST/); the search of the 1,422-base sequenced fragment from all four ticks revealed a 100% homology with B. henselae Houston-1 (GenBank accession no. AF014829). Subtyping of Bartonella henselae Amplification of the pap31 and ftsZ partial sequences yielded 257-bp and 885-bp, fragments, respectively. Sequences of these products had 100% identity with those of B. henselae Houston- 1 (GenBank accession nos. AF001274 and AF061746, respectively). Discussion Recently, vector biologists and epidemiologists have suggested that ticks may have a role in Bartonella transmission (29). In 1996 Kruszewska et al. reported the preliminary finding of a Bartonella strain in I. ricinus ticks from a park in Walz, Poland (26). Unfortunately, the strain has not been further characterized. In a study conducted in the Netherlands, the 16S rRNA gene sequences of an unspecified Bartonella were amplified in >70% of I. ricinus ticks removed from roe deer (27). Such a high prevalence of Bartonella in ticks is surprising and may be because ticks were collected while they were feeding on bacteriemic hosts (30,31). According to Schouls et al., none of the Bartonella organisms detected was a known human pathogen (27). More recently, different Bartonella sp., including B. quintana, B. henselae, Bartonella strain cattle-l, B. washoensis, and B. vinsonii subsp. berkhoffii, have been detected in 19.2% of I. pacificus ticks collected in California by amplification and sequencing of a fragment of the gltA gene (32). In this study, we report the detection of B. henselae in four I. ricinus ticks (1.4%) removed from persons in Italy. Because the primers used in the screening PCR generate rather large PCR fragments (1,490 bp), this prevalence could be expected to be greater (usually, the longer the PCR product, the lower the sensitivity). DNA from positive samples was further characterized by using the groEL, the pap31, and the ftsZ genes to establish their relationship with known Bartonella sp. and subsp. On the basis of the 16S rRNA genes and immunogenic im·mu·no·gen·ic adj. Producing an immune response. immunogenic producing immunity; evoking an immune response. characteristics, Drancourt et al. (33) suggested the presence of two variants of B. henselae. Ribosomal genes such as the 16S rRNA genes are, however, highly conserved within bacteria and can pose the risk of unspecific Adj. 1. unspecific - not detailed or specific; "a broad rule"; "the broad outlines of the plan"; "felt an unspecific dread" broad general - applying to all or most members of a category or group; "the general public"; "general assistance"; "a general rule"; amplification. Protein-coding genes exhibit a higher degree of sequence variation and thus can be targeted as tools for differentiating strains of the same species. Although the two genogroups of B. henselae, Marseille and Houston-1, are closely related, and the respective pathogenicity spectrum of the two serotypes has not been established, the serotypes could be differentiated on the basis of sequences of the groEL, C-terminal region of the ftsz gene and the pap31 gene (21,22). In northwestern Italy, about 89% of the ticks found to parasitize par·a·sit·ize v. To live on or in a host as a parasite. parasitize to live on or within a host as a parasite. people were I. ricinus (34). In our study, four different species of ticks were recorded from humans, and I. ricinus was recorded most frequently (98.9%). All the active life stages of I. ricinus were represented. Experimental studies and epidemiologic observations have suggested that ticks may play a role in the transmission of Bartonella sp. Dermacentor andersoni was proven to be a competent vector of B. bacilliformis in the experimental infection of nonhuman primates many years ago (35). B. vinsonii subsp. berkhoffii infection was correlated with heavy tick infestation infestation /in·fes·ta·tion/ (-fes-ta´shun) parasitic attack or subsistence on the skin and/or its appendages, as by insects, mites, or ticks; sometimes used to denote parasitic invasion of the organs and tissues, as by helminths. of dogs (36). The cat flea (Ctenocephalides felis) is the main arthropod vector of B. henselae with cats serving as the main vertebrate reservoirs. Although finding B. henselae in ticks might suggest another possible reservoir, I. ricinus-like ticks have a very broad host range and are known to infest in·fest v. 1. To live as a parasite in or on tissues or organs or on the skin and its appendages. 2. To inhabit or overrun in numbers large enough to be harmful, threatening, or obnoxious. cats. In our study, none of the persons from whom the positive ticks were collected exhibited symptoms associated with B. henselae infection. However, serum specimens from these patients have not been tested. Because bacteremia bacteremia: see septicemia. bacteremia Presence of bacteria in the blood. Short-term bacteremia follows dental or surgical procedures, especially if local infection or very high-risk surgery releases bacteria from isolated sites. levels in cat-scratch disease patients have never been consistently demonstrated (37), the tick was unlikely to have acquired B. henselae from feeding on patients with asymptomatic cat-scratch disease. Nevertheless, a number of wild animals, including the preferred hosts of both adults and immature stages of I. ricinus (38) have been found to be infected with Bartonella sp. (8,39). Questing ticks have been found infected with Bartonella, including B. henselae (32). Furthermore, ticks were suspected of being vectors of B. henselae in an epidemiologic study conducted by Lucey et al. in 1992 (25). These authors reported B. henselae bacteremia levels in patients who recalled a tick bite but had no history of contact with cats. Ticks were also reported as possible source of infection in some human cases of concurrent infection of the central nervous system by Borrelia burgdorferi and Bartonella henselae (40). The evidence that ticks may serve as Bartonella vectors appears to be rapidly accumulating. In conclusion, we have confirmed that ticks feeding on humans were infected with the agent of cat-scratch disease, B. henselae (Houston-1). The source of infection of the ticks was not determined. No case of transmission to humans was observed. However, our findings suggest that the ticks were naturally infected. These results support the argument that ticks are involved in the transmission of Bartonella organisms and represent a potential source of infection for persons exposed to tick bites. Therefore, we encourage further investigation of ticks as vectors of human pathogenic Bartonella strains. Table. Primers used for polymerase chain reaction or sequencing Primer Bartonella species HSPF1d (a,b) All BbHS1630.n (a,b) All HSP1 (b) All HSP2 (b) All HSPS1 (b) All HSPS2 (b) All HSPF2d (b) All HSPR2d (b) All PAPn1 (a,b) B. henselae and B. quintana PAPn2 (a,b) B. henselae and B. quintana PAPns2 (a,b) B. henselae and B. quintana PAPns1 (b) B. henselae and B. quintana BaftsZF B. henselae BaftsZR B. henselae BhftsZ 1393.n B. henselae Bh ftsZ 1247.p B. henselae Primer Primer sequence HSPF1d (a,b) 5'-GAACTNGAAGATAAGTTNGAA-3' BbHS1630.n (a,b) 5'-AATCCATTCCGCCCATTC-3' HSP1 (b) 5'-GGAAAAAGTNGGCAATGAAG-3' HSP2 (b) 5'-GCNGCTTCTTCACCNGCATT-3' HSPS1 (b) 5'-AAGCNCCNGGNTTTGGTGA-3' HSPS2 (b) 5'-TCACCAAANCCNGGNGCTT-3' HSPF2d (b) 5'-GAAAGANCGNGTNGATGAT-3' HSPR2d (b) 5'-GTNATNAGAAGNCTNGCAAT-3' PAPn1 (a,b) 5'-TTCTAGGAGTTGAAACCGAT-3' PAPn2 (a,b) 5'-GAAACACCACCAGCAACATA-3' PAPns2 (a,b) 5'-GCACCAGACCATTTTTCCTT-3' PAPns1 (b) 5'-CAGAGAAGACGCAAAAACCT-3' BaftsZF 5'-GCTAATCGTATTCGCGAAGAA-3' BaftsZR 5'-GCTGGTATTTCCAAYTGATCT-3' BhftsZ 1393.n 5'-GCGAACTACGGCTTACTTGC-3' Bh ftsZ 1247.p 5'-CGGTTGGAGAGCAGTTTCGTC-3' Primer Target gene References HSPF1d (a,b) groEL 22 BbHS1630.n (a,b) groEL 18 HSP1 (b) groEL 22 HSP2 (b) groEL 22 HSPS1 (b ) groEL 22 HSPS2 (b) groEL 22 HSPF2d (b) groEL 22 HSPR2d (b) groEL 22 PAPn1 (a,b) pap31 22 PAPn2 (a,b) pap31 22 PAPns2 (a,b) pap31 22 PAPns1 (b) pap31 22 BaftsZF fisZ This study BaftsZR fisZ This study BhftsZ 1393.n fisZ 21 Bh ftsZ 1247.p fisZ 21 (a) Amplification primer. (b) Sequencing primer. Acknowledgments We acknowledge P. Parola and J.L. Camicas for helping with tick identification and S. Telford III for English review and comments. This research was made possible by the European Network on Surveillance of Tick-Borne Diseases funded by the European Community QLRT-2001-01293. Y.O. Sanogo is a recipient of the Amis des Sciences (Paris) fellowship. References (1.) Regnery RL, Anderson BE, Clarridge JE III, Rodriguez-Barradas MC, Jones DC, Carr JH. Characterization of a novel Rochalimaea species, R. henselae sp. nov., isolated from blood of a febrile, human immunodeficiency virus-positive patient. J Clin Microbiol 1992;30:265-74. (2.) La Scola B, Raoult D. Culture of Bartonella quintana and Bartonella henselae from human samples: a 5-year experience (1993 to 1998). J Clin Microbiol 1999;37:1899-1905. (3.) Brouqui P, Lascola B, Roux Roux , Pierre Paul Émile 1853-1933. French bacteriologist. His work with the diphtheria bacillus led to the development of antitoxins to neutralize pathogenic toxins. V, Raoult D. Chronic Bartonella quintana bacteremia in homeless patients. N Engl J Med 1999;340:184-9. (4.) Kordick DL, Swaminathan B, Greene CE, Wilson KH, Whitney AM, O'Connor S, et al. Bartonella vinsonii subsp. berkhoffii subsp. nov., isolated from dogs; Bartonella vinsonii subsp. vinsonii; and emended e·mend tr.v. e·mend·ed, e·mend·ing, e·mends To improve by critical editing: emend a faulty text. description of Bartonella vinsonii, Int J Syst Bacteriol 1996;46:704-9. (5.) Kelly PJ, Rooney JJ, Marston EL, Jones DC, Regnery RL. Bartonella henselae isolated from cats in Zimbabwe. Lancet 1998;351:1706. (6.) Birtles RJ, Canales J, Ventosilla P, Alvarez E, Guerra H, Llanos-Cuentas A, et al. Survey of Bartonella species infecting intradomicillary animals in the Huayllacallan Valley, Ancash, Peru, a region endemic for human bartonellosis. Am J Trop Med Hyg 1999;60:799-805. (7.) 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Having complex nutritional requirements. Used of microorganisms. gram-negative pathogen as a cause of fever and bacteremia. N Engl J Med 1990;323:1587-93. (13.) Regnery R, Martin M, Olson J. Naturally occurring "Rochalimaea henselae" infection in domestic cat. Lancet 1992; 340:557-8. (14.) Wong MT, Dolan MJ, Lattuada CP Jr, Regnery RL, Garcia ML, Mokulis EC, et al. Neuroretinitis, aseptic meningitis, and lymphadenitis Lymphadenitis Definition Lymphadenitis is the inflammation of a lymph node. It is often a complication of a bacterial infection of a wound, although it can also be caused by viruses or other disease agents. associated with Bartonella (Rochalimaea) henselae infection in immunocompetent im·mu·no·com·pe·tent adj. Having the normal bodily capacity to develop an immune response following exposure to an antigen. im patients and patients infected with human immunodeficiency virus human immunodeficiency virus n. HIV. 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Arising or occurring within a species: intraspecific competition. Adj. 1. genetic variation within the 60 kDa heat-shock protein gene (groEL) of Bartonella species. Int J Syst Bacteriol 1999;49:1015-23. (19.) Birtles RJ, Raoult D. Comparison of partial citrate synthase gene (gltA) sequences for phylogenetic analysis of Bartonella species. Int J Syst Bacteriol 1996;46:891-7. (20.) Bereswill S, Hinkelmann S, Kist kist n. Variant of cist2. kist Noun Scot & S African a large wooden chest Kist a chest of money, hence, a store or cache of money, 1619. M, Sander A. Molecular analysis of riboflavin riboflavin: see coenzyme; vitamin. riboflavin or vitamin B2 Yellow, water-soluble organic compound, abundant in whey and egg white. It has a complex structure incorporating three rings. synthesis genes in Bartonella henselae and use of the ribC gene for differentiation of Bartonella species by PCR. J Clin Microbiol 1999;37:3159-66. (21.) Ehrenborg C, Wesslen L, Jakobson A, Friman G, Holmberg M. 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J Clin Microbiol 2001;39:1221-6. (33.) Drancourt M, Birtles R, Chaumentin G, Vandenesch F, Etienne J, Raoult D. New serotype serotype /se·ro·type/ (ser´o-tip) the type of a microorganism determined by its constituent antigens; a taxonomic subdivision based thereon. se·ro·type n. See serovar. v. of Bartonella henselae in endocarditis and cat-scratch disease. Lancet 1996;347:441-3. (34.) Manfredi MT, Dini V, Piacenza S, Genchi C. Tick species parasitizing people in an area endemic for tick-borne diseases in north-western Italy. Parassitologia 1999;41:555-60. (35.) Noguchi H. Etiology of Oroya fever. V. The experimental transmission of Bartonella bacilliformis by ticks (Dermacentor andersoni). J Exp Med 1926;44:729-34. (36.) Pappalardo BL, Correa MT, York CC, Peat CY, Breitschwerdt EB. Epidemiologic evaluation of the risk factors associated with exposure and seroreactivity to Bartonella vinsonii in dogs. Am J Vet Res 1997;58:467-71. (37.) 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Address for correspondence: Didier Raoult, Unite des Rickettsies, CNRS CNRS Centre National de la Recherche Scientifique (National Center for Scientific Research, France) CNRS Centro Nacional de Referencia Para El Sida (Argentinean National Reference Center for Aids) UMR UMR Unite Mixte de Recherche (French: Mixed Unit of Research ) UMR University of Missouri - Rolla UMR Upper Mississippi River UMR Uniform Methods and Rules (US Department of Agriculture) UMR Unit Manning Report 6020, Faculte de Medecine, 27 Boulevard Jean Moulin, 13385 Marseille Cedex 5, France; fax: (33) 4 9183 03 90; e-mail: Didier. Raoult@medecine.univ-mrs.fr Yibayiri O. Sanogo, * Zaher Zeaiter, * Giuseppe Caruso, ([dagger]) Francesco Merola, ([dagger]) Stanislav Shpynov, * Philippe Brouqui, * and Didier Raoult * * Faculte de Medecine, Marseille, France; and ([dagger]) Ospedale San Martino Belluno, Italy. Dr. Sanogo is a postdoctoral researcher in microbiology and medical entomology at the Faculte de Medecine, Marseille, France. His work focuses on the relationship between arthropods and bacteria. |
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