Skip directly to site content Skip directly to page options Skip directly to A-Z link Skip directly to A-Z link Skip directly to A-Z link
Volume 9, Number 3—March 2003
Research

Molecular Detection of Bartonella quintana, B. koehlerae, B. henselae, B. clarridgeiae, Rickettsia felis, and Wolbachia pipientis in Cat Fleas, France

On This Page
Materials and Methods
Results
Discussion
Cite This Article
Tables
Table 1
Table 2
Downloads
Article
RIS [TXT - 2 KB]
Article Metrics
Metric Details
280
citations of this article
EID Journal Metrics on Scopus
Author affiliations: *Université de la Méditerranée, Marseille, France; †Ecole Nationale Vétérinaire de Toulouse, France; ‡Conseiller Vétérinaire Régional Interarmées, Lyon Armées, France)

Cite This Article

The prevalences of Bartonella, Rickettsia, and Wolbachia were investigated in 309 cat fleas from France by polymerase chain reaction (PCR) assay and sequencing with primers derived from the gltA gene for Rickettsia, the its and pap31 genes for Bartonella, and the 16S rRNA gene for Anaplasmataceae. Positive PCR results were confirmed by using the Lightcycler and specific primers for the rOmpB of Rickettsia and gltA of Bartonella. R. felis was detected in 25 fleas (8.1%), W. pipientis, an insect symbiont, in 55 (17.8%), and Bartonella in 81 (26.2%), including B. henselae (9/81; 11.1%), B. clarridgeiae (55/81; 67.9%), B. quintana (14/81; 17.3%), and B. koehlerae (3/81; 3.7%). This is the first report of the amplification of B. quintana from fleas and the first description of B. koehlerae in fleas from an area outside the United States. Cat fleas may be more important vectors of human diseases than previously reported.

Fleas can be found worldwide and are vectors of several important zoonoses, including plague caused by Yersinia pestis (1). The classic cycle of Rickettsia typhi, the agent of murine typhus, involves rats and the rat flea, Xenopsylla cheopis, the main vector (2). The disease is transmitted by flea bites or contact with flea feces. Recently, murine typhus has been shown to exist in some endemic foci where neither rats or their fleas are found. Subsequently, in the United States, R. typhi was found to be maintained in the cat flea, Ctenocephalides felis, collected from opossums (2). R. felis is the recently recognized agent of flea-borne spotted fever, which has been reported in various countries, including the United States, Mexico, Brazil, Germany, and France (3–6). C. felis is apparently the main vector of this new rickettsial disease, and R. felis has been found in this flea in several countries, including the United States (2), Brazil (7), Spain (8), and Ethiopia (6). A reservoir of flea-borne spotted fever in the United States may be the opossum. Of major importance to the epidemiology of the above rickettsioses is the maintenance of R. typhi or R. felis in their hosts by transovarial transmission (9) and the fact that neither organism is lethal for fleas.

Bartonellae are gram-negative bacteria that cause various human diseases and have various arthropods, such as lice, ticks, and fleas, as vectors (10). Transmission to humans may also occur by scratches or bites from reservoir hosts, especially cats. Among the genus Bartonella, four species have been isolated from the blood of cats. Two of these species occur worldwide, B. henselae, the agent of cat-scratch disease, and B. clarridgeiae, which might be another agent of cat-scratch disease (11), and two have been reported only from the United States, B. koehlerae and B. bovis Bermond (B. weissii) (12–14). The main vector of B. henselae infections in cats is most likely the cat flea (2), whereas the vectors of B. koehlerae and B. weissii are unknown. Detection of B. clarridgeiae in cat fleas by polymerase chain reaction (PCR) amplification has indicated the possible role of fleas as vectors of the organism (15). Cats are the reservoirs of the bacteria, and the prevalence of cats with B. henselae and B. clarridgeiae bacteremia ranges from 4% to 70%, according to the geographic location (15).

We describe experiments in which we used PCR amplification and DNA sequencing to detect Rickettsia, Bartonella, and Ehrlichia species in C. felis collected from various sites in France.

Materials and Methods

Source and Identification of Cat Fleas

Cat fleas (C. felis), identified according to current taxonomic keys (16), were obtained from various departments of the Veterinary School of Toulouse, located throughout France. Cat fleas were sent to our laboratory in sealed, preservative-free, plastic tubes at room temperature. To prevent contamination problems, as positive controls we used DNA from R. montanensis (ATCC VR-611) and Bartonella elizabethae F9251 (ATCC 49927), which react with the primer pairs we used in PCR but give sequences distinct from the species we were investigating. For negative controls, we used sterile water and human body lice reared in our laboratory; both negative controls were tested after every seventh cat-flea sample in our PCR.

DNA Extraction

Fleas were immersed for 5 min in a solution of 70% ethanol/0.2% iodine, washed for 5 min in sterile distilled water and crushed individually in sterile Eppendorf tubes with the tip of a sterile pipette. Their DNA was extracted by using the QIAamp Tissue Kit (QIAGEN, Hilden, Germany) according to the manufacturer’s instructions. This kit was also used to extract DNA from the human body lice reared in our laboratory under standard conditions and used as negative controls.

Detection of Bartonella spp., Rickettsia spp., and Anaplasmataceae

DNA extracts were amplified in two different runs with different target genes to confirm the results. In the first run we tested all the cat fleas by using genus-specific primers (Table 1) derived from the intergenic spacer region (its gene), the pap 31 gene for Bartonella (19,20), the citrate synthase–encoding gene for Rickettsia (17), and the 16S RNA gene for Anaplasmataceae (21,22). A total volume of 2.5 μL of the extracted DNA was amplified in a 25-μL reaction mixture containing 12.5 pmol of each primer, 200 μM of dATP, dCTP, dGTP, and dTTP, and 1 U of Elongase in 1X PCR buffer with 0.8 μL of 25 mM MgCl2 (Life Technologies, Cergy Pontoise, France). PCR was carried out in a Peltier Thermal Cycler PTC-200 (MJ Research, Inc., Watertown, MA) with an initial 3-min denaturation step at 95°C, followed by 40 cycles of denaturation at 95°C (30 s), annealing at 50°C (30 s), and extension at 72°C (1 min). Amplification was completed by holding the reaction mixture at 68°C for 3 min to allow complete extension of the PCR products. PCR products were resolved by electrophoresis in 1% agarose gels, and when appropriately sized products were found, they were purified by using Qiagen columns (QIAquick Spin PCR purification kit; QIAGEN) before sequencing.

Any positive sample was tested again by using different primers and real-time PCR technology. For Bartonella, the forward primer of the gltA gene (Table 1) was used for all samples and species-specific primers targeting B. quintana, B. henselae, B. clarridgeiae, and B. koehlerae were designed as reverse primers. For Rickettsia, we used rOmpB-specific primers targeting R. felis (Table 1) (18). A real-time PCR assay was performed on DNA extracts in a Lightcycler instrument (Roche Biochemicals, Mannheim, Germany). The amplification program began with a denaturation step of 95°C for 120 sec, followed by 40 cycles of denaturation at 95°C for 15 s, annealing at 52°C for 5 sec, and extension at 72°C for 10 s with fluorescence acquisition at 54°C in single mode. Melting curve analysis was done at 45°C to 90°C (temperature transition, 20°C/s) with stepwise fluorescence acquisition by real-time measurement of fluorescence directly in the clear glass capillary tubes. Sequence specific standard curves were generated by using 10-fold serial dilutions (105 to 106 copies) of standard bacterial concentration of Bartonella.

The positive PCR products of the two runs for Bartonella, Rickettsia, and Wolbachia were sequenced by using the d-rhodamine terminator cycle-sequencing ready reaction kit (PE Applied Biosystems, Les Ulis, France) according to the manufacturer’s protocol. Sequences obtained were compared with those in the GenBank DNA database by using the program BLAST (version 2.0, National Center for Biotechnology Information; available from URL: http://www.ncbi.nlm.nih.gov).

Results

Overall, 309 cat fleas from 92 cats from all areas of France (north, west, east, and south) were tested. Almost two thirds (60/92; 65%) of the cats lived both outdoors and indoors, 20% lived predominantly outdoors, and 15% lived exclusively indoors. Our negative controls consistently failed to yield detectable PCR products, whereas our positive controls always gave expected PCR products. We found a total of 89 fleas (28.8%) that were infected: 25 were positive for R. felis (25/309; 8.1%) as determined by citrate synthase–gene sequencing, and 81 were positive for Bartonella species (81/309; 26.2%) as determined either by its gene or pap31 gene sequencing (Table 2). The sequences of the DNA amplicons we obtained were identical to those of R. felis (Genbank accession no. U33922), B. henselae (Genbank accession no. AF369527), B. clarridgeiae (GenBank accession no. AF312497), B. koehlerae (GenBank accession no. AF312490), or B. quintana (GenBank accession no. AF368391). The Bartonella species we identified were B. henselae (9/89; 11.1%), B. clarridgeiae (55/89; 67.9%), B. quintana (14/89; 17.3%), and B. koehlerae (3/89; 3.7%). Our results were confirmed by a second PCR with the Lightcycler and specific primers for the gltA gene for Bartonella and rOmpB for Rickettsia. Because the primers were species-specific, we were able to demonstrate that none of the fleas contained more than one Bartonella species. Seventeen fleas, however, contained R. felis and B. quintana (12 fleas) or B. clarridgeiae (5 fleas) (Table 2). Lastly, in 55 fleas (17.8%) our Anaplasmataceae-specific primers amplified DNA with a sequence identical to that of Wolbachia pipientis (Genbank accession no. U23709).

Discussion

Rickettsia and Bartonella infections occur worldwide and may cause serious diseases in people. Most of these pathogenic bacteria are transmitted to people by arthropod vectors such as ticks, fleas, and lice, which are also involved in the maintenance of the bacteria. The detection of these pathogenic bacteria in their vector arthropods can be used in epidemiologic studies and control strategies (2). We tested cat fleas from around France for the presence of Rickettsia, Bartonella, and Ehrlichia species. We found DNA of R. felis and various Bartonella species in these fleas by using PCR with primers for different specific genes and sequencing to confirm our results. All our negative controls gave no PCR products, and all fleas that tested positive were also positive with other PCRs with different target genes and different techniques.

We report for the first time the presence of R. felis in cat fleas from France. This bacteria has been detected previously in wild cat fleas from various countries, including the United States (2), Ethiopia (6), and, very recently, Spain (8), and Brazil (7). Since C. felis has a worldwide distribution and infestation with these fleas is very common, some have assumed that R. felis and flea-borne spotted fever should occur worldwide. We found that 8.1% of fleas from domestic cats were infected with R. felis, suggesting that clinical cases in humans may be prevalent in France and probably in Europe. In the United States, the infection rates of fleas, as determined by PCR amplification, have been reported to vary from 43% to 93% (2). Since bacteria are maintained transovarially, R. felis may be used as a marker to follow changes in the infection rates over time (2). In people, clinical cases of flea-borne spotted fever have been reported in the United States (Texas) (3), Mexico (4), France, and Brazil (6), and, very recently, in Germany (5). Preliminary serologic results indicate that flea-borne spotted fever might occur in France (6), and we have now shown that fleas in France are infected with R. felis. The disease is probably more prevalent than expected, even if the risk of transmission by fleas is unknown. Cross-reactions in serologic testing for R. felis are unpredictable in our experience, and thus serologic tests for R. felis should be performed in patients suffering from fever of unknown origin. Our findings of R. felis in French fleas indicate, then, that R. felis should be used, along with other spotted fever group rickettsiae, in serologic tests on patients suspected of having a spotted fever group rickettsiosis.

To date, B. henselae is the only recognized agent of cat-scratch disease; epidemiologic studies have implicated cats, which remain bacteremic for months to years, as the major reservoirs of B. henselae (23,24). Its DNA has been amplified from fleas found on bacteremic cats, and transmission of B. henselae to cats by C. felis has been demonstrated (23,25,26). Flea infestation was found to be more common in bacteremic cats than in nonbacteremic cats. The prevalence of B. henselae in fleas in our study was 3%, whereas B. henselae has been isolated from the blood of 4% to 70% of cats, depending on location, cat population, and flea infestation rate but not depending on the infection rate of fleas on the cats or the seropositivity of the cats (15,25).

Our study has confirmed that B. clarridgeiae may be detected in fleas, and we found a 17.8% prevalence in infected fleas, that is, 67.9% of all fleas positive for Bartonella by PCR. Until now, B. henselae was the most common species isolated from cats, and the prevalence of B. clarridgeiae has ranged from 16% to 30% (25). B. clarridgeiae is more prevalent in European cats than in American cats (25). The difference of recovery rate of B. clarridgeiae in these studies may be explained by the fact that the number of bacteria in the blood of cats infected with B. clarridgeiae is low (unpub. data) and because B. clarridgeiae grows more slowly in culture (27). Also, freezing of whole blood improves the recovery rate of B. clarridgeiae since bacteria are probably localized in erythrocytes (15).

We report, for the first time, the presence of B. koehlerae in cat fleas. This recently described species has only been reported in the blood of cats in the United States (12), and our findings support the idea that this bacteria might be transmitted by cat fleas, like other Bartonella, and that it has a worldwide distribution. The prevalence of this new Bartonella species in cats remains unknown and is probably underestimated because the bacteria are extremely fastidious and only grow on chocolate agar and not on heart infusion agar with rabbit blood, Columbia, or on sheep blood agar, which are currently widely used for the isolation of Bartonella (12).

We also report for the first time that cat fleas can contain B. quintana; this is surprising because, to date, the body louse was the only known vector of this species, and people are the only known natural reservoirs. Previously, however, in two clinical reports of chronic adenopathy attributed to B. quintana infection, the only epidemiologic risk identified was the presence of infected cat fleas (28,29). The role of the cat flea as a potential vector of B. quintana and its related diseases needs to be clarified, and new investigations of patients in contact with cats and their fleas are indicated. Also, we have reported cases of endocarditis due to B. quintana for which no epidemiologic risks (alcoholism or homelessness) were found (30,31). These findings and the fact that B. quintana DNA sequences can be found in ticks (32) indicate that other arthropod vectors apart from lice may be involved in the epidemiology of B. quintana infections.

Coinfection of cats with B. clarridgeiae and B. henselae has been reported, as has infection with the two different genotypes of B. henselae, Marseille and Houston (25,33). Recent reports suggest that interspecific competition between closely related rickettsiae may control rickettsial establishment in arthropods (dual infections in arthropod vectors are rare and have not yet been observed in individual fleas) (34). Fleas, however, feed intermittently on different hosts and thus may acquire multiple bacterial strains and pass these to their progeny transovarially (2). Our finding of R. felis with either B. clarridgeiae or B. quintana in fleas suggests that dual infections may occur in humans infected by flea feces. We did not, however, find fleas infected with several species of Bartonella although cats may be bacteremic with two different species. We believe that the techniques we used should have been sensitive enough to detect such coinfections, and that competition between two Bartonella species may result in one species being eliminated and the flea becoming infected with the other Bartonella species. Further studies are indicated to confirm this possibility.

Finally, we report, for the first time, the presence of W. pipientis in fleas, which we found while seeking Ehrlichia using Anaplasmataceae-specific primers. This bacteria is known to be an endosymbiont of several arthropods, primarily insects, and it has a role in parthenogenesis (35). Any effects that it might have on fleas, however, are unknown.

In summary, our study has provided evidence that cat fleas are commonly infected by R. felis and Bartonella species in France. Further, we have shown for the first time that B. quintana may infect fleas. The description of B. quintana-related diseases in patients with histories of contact with fleas indicates the possibility that fleas may be vectors of the organism. Finally, we reported for the first time the presence of B. koehlerae outside the United States.

Dr. Rolain is a microbiologist at the Unité des Rickettsies, the national reference center for rickettsiosis and World Health Organization collaborative center. The laboratory is primarily involved in the study of emerging and reemerging bacteria and arthropod-borne diseases.

Top

Acknowledgment

We thank Patrick Kelly for reviewing the manuscript.

Top

References

  1. Perry  RD, Fetherston  JD. Yersinia pestis—etiologic agent of plague. Clin Microbiol Rev. 1997;10:35–66.PubMedGoogle Scholar
  2. Azad  AF, Radulovic  S, Higgins  JA, Noden  BH, Troyer  JM. Flea-borne rickettsioses: ecologic considerations. Emerg Infect Dis. 1997;3:319–27. DOIPubMedGoogle Scholar
  3. Schriefer  ME, Sacci  JB Jr, Dumler  JS, Bullen  MG, Azad  AF. Identification of a novel rickettsial infection in a patient diagnosed with murine typhus. J Clin Microbiol. 1994;32:949–54.PubMedGoogle Scholar
  4. Zavala-Velazquez  JE, Ruiz-Sosa  JA, Sanchez-Elias  RA, Becerra-Carmona  G, Walker  DH. Rickettsia felis rickettsiosis in Yucatan. Lancet. 2000;356:1079–80.PubMedGoogle Scholar
  5. Richter  J, Fournier  PE, Petridou  J, Haussinger  D, Raoult  D. Rickettsia felis infection acquired in Europe and documented by polymerase chain reaction. Emerg Infect Dis. 2002;8:207–8. DOIPubMedGoogle Scholar
  6. Raoult  D, La Scola  B, Enea  M, Fournier  PE, Roux  V, Fenollar  F, A flea-associated Rickettsia pathogenic for humans. Emerg Infect Dis. 2001;7:73–81. DOIPubMedGoogle Scholar
  7. Oliveira  RP, Galvao  MAM, Mafra  CL, Chamone  CB, Calic  SB, Silva  SU, Rickettsia felis in Ctenocephalides spp. fleas, Brazil. Emerg Infect Dis. 2002;8:317–9. DOIPubMedGoogle Scholar
  8. Marquez  FJ, Muniain  MA, Perez  JM, Pachon  J. Presence of Rickettsia felis in the cat flea from southwestern Europe. Emerg Infect Dis. 2002;8:89–91. DOIPubMedGoogle Scholar
  9. Azad  AF, Sacci  JB, Nelson  WM, Dasch  GA, Schmidtmann  ET, Carl  M. Genetic characterization and transovarial transmission of a typhus-like rickettsia found in cat fleas. Proc Natl Acad Sci U S A. 1992;89:43–6. DOIPubMedGoogle Scholar
  10. Jacomo  V, Kelly  PJ, Raoult  D. Natural history of Bartonella infections (an exception to Koch’s postulate). Clin Diagn Lab Immunol. 2002;9:8–18.PubMedGoogle Scholar
  11. Kordick  DL, Hilyard  EJ, Hadfield  TL, Wilson  KH, Steigerwalt  AG, Brenner  DJ, Bartonella clarridgeiae, a newly recognized zoonotic pathogen causing inoculation papules, fever, and lymphadenopathy (cat scratch disease). J Clin Microbiol. 1997;35:1813–8.PubMedGoogle Scholar
  12. Droz  S, Chi  B, Horn  E, Steigerwalt  AG, Whitney  AM, Brenner  DJ. Bartonella koehlerae sp. nov., isolated from cats. J Clin Microbiol. 1999;37:1117–22.PubMedGoogle Scholar
  13. Breitschwerdt  EB, Sontakke  S, Cannedy  A, Hancock  SI, Bradley  JM. Infection with Bartonella weissii and detection of Nanobacterium antigens in a North Carolina beef herd. J Clin Microbiol. 2001;39:879–82. DOIPubMedGoogle Scholar
  14. Bermond  D, Boulouis  HJ, Heller  R, Van  LG, Monteil  H, Chomel  BB, Bartonella bovis Bermond et al. sp. nov. and Bartonella capreoli sp. nov., isolated from European ruminants. Int J Syst Evol Microbiol. 2002;52:383–90.PubMedGoogle Scholar
  15. La Scola  B, Davoust  B, Boni  M, Raoult  D. Lack of correlation between serology, Bartonella DNA detection within fleas and results of blood culture in a Bartonella-infected stray cat population. Clin Microbiol Infect. 2002;8:345–51. DOIPubMedGoogle Scholar
  16. Ménier  K, Beaucournu  JC. Taxonomic study of the genus Ctenocephalides Stiles & Collins, 1930 (Insecta: Siphonaptera:Pulicidae) by using Aedeagus characters. J Med Entomol. 1998;35:883–90.PubMedGoogle Scholar
  17. Roux  V, Rydkina  E, Eremeeva  M, Raoult  D. Citrate synthase gene comparison, a new tool for phylogenetic analysis, and its application for the rickettsiae. Int J Syst Bact. 1997;47:252–61. DOIPubMedGoogle Scholar
  18. Roux  V, Raoult  D. Phylogenetic analysis of members of the genus Rickettsia using the gene encoding the outer-membrane protein rOmpB (ompB). Int J Syst Evol Microbiol. 2000;50:1449–55.PubMedGoogle Scholar
  19. Roux  V, Raoult  D. The 16S-23S rRNA intergenic spacer region of Bartonella (Rochalimaea) species is longer than usually described in other bacteria. Gene. 1995;156:107–11. DOIPubMedGoogle Scholar
  20. Zeaiter  Z, Fournier  PE, Ogata  H, Raoult  D. Phylogenetic classification of Bartonella species by comparing groEL sequences. Int J Syst Evol Microbiol. 2002;52:165–71.PubMedGoogle Scholar
  21. Brouqui  P, Fournier  PE, Raoult  D. Doxycycline and eradication of microfilaremia in patients with loiasis. Emerg Infect Dis. 2001;7:604–5. DOIPubMedGoogle Scholar
  22. Dumler  JS, Barbet  AF, Bekker  CP, Dasch  GA, Palmer  GH, Ray  SC, Reorganization of genera in the families Rickettsiaceae and Anaplasmataceae in the order Rickettsiales: unification of some species of Ehrlichia with Anaplasma, Cowdria with Ehrlichia and Ehrlichia with Neorickettsia, descriptions of six new species combinations and designation of Ehrlichia equi and ‘HGE agent’ as subjective synonyms of Ehrlichia phagocytophila. Int J Syst Evol Microbiol. 2001;51:2145–65.PubMedGoogle Scholar
  23. Abbott  RC, Chomel  BB, Kasten  RW, Floyd-Hawkins  KA, Kikuchi  Y, Koehler  JE, Experimental and natural infection with Bartonella henselae in domestic cats. Comp Immunol Microbiol Infect Dis. 1997;20:41–51. DOIPubMedGoogle Scholar
  24. Kordick  DL, Wilson  KH, Sexton  DJ, Hadfield  TL, Berkhoff  HA, Breitschwerdt  EB. Prolonged Bartonella bacteremia in cats associated with cat-scratch disease patients. J Clin Microbiol. 1995;33:3245–51.PubMedGoogle Scholar
  25. Gurfield  AN, Boulouis  HJ, Chomel  BB, Kasten  RW, Heller  R, Bouillin  C, Epidemiology of Bartonella infection in domestic cats in France. Vet Microbiol. 2001;80:185–98. DOIPubMedGoogle Scholar
  26. Chomel  BB, Kasten  RW, Floyd-Hawkins  K, Chi  B, Yamamoto  K, Roberts-Wilson  J, Experimental transmission of Bartonella henselae by the cat flea. J Clin Microbiol. 1996;34:1952–6.PubMedGoogle Scholar
  27. Marston  EL, Finkel  B, Regnery  RL, Winoto  IL, Graham  RR, Wignal  S, Prevalence of Bartonella henselae and Bartonella clarridgeiae in an urban Indonesian cat population. Clin Diagn Lab Immunol. 1999;6:41–4.PubMedGoogle Scholar
  28. Drancourt  M, Moal  V, Brunet  P, Dussol  B, Berland  Y, Raoult  D. Bartonella (Rochalimaea) quintana infection in a seronegative hemodialyzed patient. J Clin Microbiol. 1996;34:1158–60.PubMedGoogle Scholar
  29. Raoult  D, Drancourt  M, Carta  A, Gastaut  JA. Bartonella (Rochalimaea) quintana isolation in patient with chronic adenopathy, lymphopenia, and a cat. Lancet. 1994;343:977. DOIPubMedGoogle Scholar
  30. Fournier  PE, Lelievre  H, Eykyn  SJ, Mainardi  JL, Marrie  TJ, Bruneel  F, Epidemiologic and clinical characteristics of Bartonella quintana and Bartonella henselae endocarditis: a study of 48 patients. Medicine (Baltimore). 2001;80:245–51. DOIPubMedGoogle Scholar
  31. Raoult  D, Fournier  PE, Drancourt  M, Marrie  TJ, Etienne  J, Cosserat  J, Diagnosis of 22 new cases of Bartonella endocarditis. Ann Intern Med. 1996;125:646–52.PubMedGoogle Scholar
  32. Chang  CC, Chomel  BB, Kasten  RW, Romano  V, Tietze  N. Molecular evidence of Bartonella spp. in questing adult Ixodes pacificus ticks in California. J Clin Microbiol. 2001;39:1221–6. DOIPubMedGoogle Scholar
  33. La Scola  B, Liang  Z, Zeaiter  Z, Houpikian  P, Grimont  PAD, Raoult  D. Genotypic characteristics of two serotypes of Bartonella henselae. J Clin Microbiol. 2002;40:2002–8. DOIPubMedGoogle Scholar
  34. Azad  AF, Beard  CB. Rickettsial pathogens and their arthropod vectors. Emerg Infect Dis. 1998;4:179–86. DOIPubMedGoogle Scholar
  35. McGraw  EA, O'Neill  SL. Evolution of Wolbachia pipientis transmission dynamics in insects. Trends Microbiol. 1999;7:297–302. DOIPubMedGoogle Scholar

Top

Tables

Top

Cite This Article

DOI: 10.3201/eid0903.020278

Table of Contents – Volume 9, Number 3—March 2003

EID Search Options
presentation_01 Advanced Article Search – Search articles by author and/or keyword.
presentation_01 Articles by Country Search – Search articles by the topic country.
presentation_01 Article Type Search – Search articles by article type and issue.

Top

Comments

Please use the form below to submit correspondence to the authors or contact them at the following address:

Didier Raoult, Unité des Rickettsies, Faculté de Médecine, 27, Boulevard Jean Moulin, 13385 Marseille Cedex 5, France; fax: 33.04.91.38.77.72

Send To

10000 character(s) remaining.

Top

Page created: December 07, 2010
Page updated: December 07, 2010
Page reviewed: December 07, 2010
The conclusions, findings, and opinions expressed by authors contributing to this journal do not necessarily reflect the official position of the U.S. Department of Health and Human Services, the Public Health Service, the Centers for Disease Control and Prevention, or the authors' affiliated institutions. Use of trade names is for identification only and does not imply endorsement by any of the groups named above.
file_external