Previous Article | Next Article 
Journal of Clinical Microbiology, October 2001, p. 3548-3554, Vol. 39, No. 10
Department of Population Health and
Reproduction,1 Cardiology Unit,
Veterinary Medical Teaching Hospital and Department of Medicine and
Epidemiology,2 and Center for Companion
Animal Health,3 School of Veterinary
Medicine, University of California, Davis, California 95616
Received 20 February 2001/Returned for modification 8 May
2001/Accepted 29 May 2001
We report the first documented case of endocarditis associated with
Bartonella clarridgeiae in any species. B.
clarridgeiae was identified as a possible etiological agent of
human cat scratch disease. Infective vegetative valvular aortic
endocarditis was diagnosed in a 2.5-year-old male neutered boxer.
Historically, the dog had been diagnosed with a systolic murmur at 16 months of age and underwent balloon valvuloplasty for severe valvular aortic stenosis. Six months later, the dog was brought to a veterinary hospital with an acute third-degree atrioventricular block and was
diagnosed with infective endocarditis. The dog died of cardiopulmonary arrest prior to pacemaker implantation. Necropsy confirmed severe aortic vegetative endocarditis. Blood culture grew a fastidious, gram-negative organism 8 days after being plated. Phenotypic and genotypic characterization of the isolate, including partial sequencing of the citrate synthase (gltA) and 16S rRNA genes
indicated that this organism was B. clarridgeiae. DNA
extraction from the deformed aortic valve and the healthy pulmonic
valve revealed the presence of B. clarridgeiae DNA only
from the diseased valve. No Borrelia burgdorferi or
Ehrlichia sp. DNA could be identified. Using indirect immunofluorescence tests, the dog was seropositive for B.
clarridgeiae and had antibodies against Ehrlichia
phagocytophila but not against Ehrlichia canis,
Ehrlichia ewingii, B. burgdorferi, or
Coxiella burnetii.
Bartonella species are
emerging pathogens in humans, causing severe diseases in
immunocompromised individuals (8). Based on 16S
rRNA gene sequence comparison, the Bartonella genus has been
classified in the alpha subgroup of the Proteobacteria
(8). At least eight Bartonella species or
subspecies are known to be pathogenic for humans, including B. bacilliformis, B. quintana, B. henselae,
B. elizabethae, B. grahamii, B. vinsonii subsp. arupensis (1, 26, 52),
B. vinsonii subsp. berkhoffii (45),
and B. washoensis (8). Furthermore, based on
serological evidence, B. clarridgeiae has been associated
with cat scratch disease in humans (29, 38, 46). Among
these Bartonella species or subspecies, B. quintana, B. henselae, B. elizabethae, and
B. vinsonii subsp. berkhoffii have been
identified as causative agents of human endocarditis and B. washoensis has been identified as a cause of myocarditis (1,
5, 8, 19, 20, 45, 49).
At present, only two Bartonella species have been identified
to cause clinical diseases in dogs. B. vinsonii subsp.
berkhoffii has been shown to cause endocarditis, arrhythmia,
and myocarditis (6, 9, 31), as well as granulomatous
lymphadenitis and granulomatous rhinitis (40), and
B. henselae was recently associated with a case of peliosis
hepatis (27). During an active investigation of canine
endocarditis cases, we cultured a fastidious, gram-negative organism
that we identified to be B. clarridgeiae from the blood of a
dog with an aortic endocarditis. We describe the clinicopathologic and
histopathologic features as well as the microbiologic and genotypic
identification of the organism isolated from the dog's blood and
detected by molecular methods in the infected aortic valve.
Strain sources.
The type strains of B. vinsonii
subsp. berkhoffii (ATCC 51672) and B. clarridgeiae (ATCC 51734) were obtained from the American Type
Culture Collection (Rockville, Md.). Isolate B. henselae strain U4 was obtained from our culture collection at the University of
California, Davis (UC Davis). Isolate UCD-dog1 was cultured from the
blood of the dog described in this report.
Clinical samples.
Blood (6 ml) was collected aseptically
from the dog's external jugular vein and both lateral saphenous veins
at the time of acute third-degree atrioventricular (AV) block,
infectious endocarditis, and just prior to death. Blood samples were
submitted for aerobic and aero-anaerobic cultures, as well as for
specific Bartonella isolation on fresh blood agar (5%
defibrinated rabbit blood) (16). Serum was submitted for
determination of Bartonella antibody titers and for
detection of several tick-borne pathogens (Ehrlichia spp., Borrelia burgdorferi) and of Coxiella burnetii, a
known agent of endocarditis in humans and animals.
0095-1137/01/$04.00+0 DOI: 10.1128/JCM.39.10.3548-3554.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
Aortic Valve Endocarditis in a Dog Due to Bartonella
clarridgeiae
ABSTRACT
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
INTRODUCTION
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
MATERIALS AND METHODS
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
Tissue samples. Fragments of the aortic and pulmonic valves were frozen for PCR and electron microscopic examination and fixed in 10% buffered formalin for histology. After 24 h, formalin-fixed tissues were embedded in paraffin, sectioned, and stained with hematoxylin and eosin or silver (Warthin-Starry) stain. Slides were examined under light microscopy to characterize the lesions.
Isolation procedure.
The blood samples were collected in
plastic 2-ml EDTA tubes (Becton Dickinson, Franklin Lakes, N.J.) and
frozen at 
70°C until plated. The blood samples were cultured on
heart infusion agar containing 5% rabbit blood and were incubated in
5% CO2 at 35°C for up to 4 weeks.
Identification of the isolates as B. clarridgeiae was
initially based on morphological and growth characteristics, as previously described (25, 29). The isolates were then
confirmed by PCR-restriction fragment length polymorphism (RFLP)
analysis and sequence analysis of the citrate synthase
(gltA) and 16S rRNA genes.
Microscopic and biochemical analysis. (i) DNA extraction. The bacterial isolate obtained from the dog's blood was heated at 95°C for 10 min in sterile water. The supernatant was used as DNA template, as previously described (13). DNA was also extracted from 26 mg of aortic valve tissue and 20 mg of pulmonic valve tissue using the DNeasy Tissue Kit (Qiagen, Valencia, Calif.) according to the manufacturer's instructions.
(ii) PCR assay. A 5-µl aliquot (diluted 1:10 in sterile water) of extracted DNA from the bacterial isolate was added to a 45-µl reaction mixture consisting of 15 mM Tris-HCl (pH 8.0), 50 mM KCl, 1.5 mM MgCl2, 200 µM concentrations of each deoxynucleoside triphosphate, 1.25 U of AmpliTaq LD (low DNA) DNA polymerase (Perkin-Elmer, Foster City, Calif.), and 0.5 µM concentrations of each primer. The primers used for the gltA gene were 5'-GGGGACCACTCATGGTGG-3' and 5'-AATGCAAAAAGAACAGTAAACA-3' (39). Thermocycling was performed in an MJ PTC-100 apparatus (Watertown, Mass.) under the following conditions: 94°C for 5 min, 45 cycles of 94°C for 0.5 min, 55°C for 1 min, and 72°C for 1 min, followed by 72°C for 10 min. For the 16S rRNA gene, the primers used were 5'-AGAGTTTGATCCTGGCTCAG-3' and 5'-AAGGAGGTGATGCAGCCGCA-3' (23), and the running cycles were as follows: 93°C for 5 min, 35 cycles of 93°C for 0.5 min, 60°C for 1 min, and 72°C for 1 min, followed by 72°C for 8 min.
For the DNA extracted from tissue, a 5-µl aliquot of extracted DNA (undiluted or a 1:5 or 1:10 dilution in sterile water) was added to a 45-µl reaction mixture as described above for the gltA and 16S rRNA genes. To determine the presence of Ehrlichia spp. and B. burgdorferi DNA, tissue-extracted DNA was evaluated by real-time PCR using protocols specific for Ehrlichia phagocytophila and B. burgdorferi as previously described (35, 42).(iii) RFLP. An approximately 400-bp fragment amplified from the gltA gene was verified by gel electrophoresis and then digested with TaqI (Promega, Madison, Wis.) and HhaI (New England Laboratories, Beverly, Mass.) restriction endonucleases (4, 44). The digestion conditions used were the ones recommended by the enzymes' manufacturers. Banding patterns of the digests were compared with a domestic dog isolate, B. vinsonii. subsp. berkhoffii (ATCC 51672), B. henselae (strain U-4; UC Davis), and B. clarridgeiae (ATCC 51734).
(iv) DNA sequencing. The extracted DNA was sequenced for the gltA and 16S rRNA genes, as previously described (15). The PCR products used for DNA sequencing were purified with Microcon centrifugal filter devices (Millipore Corp., Bedford, Mass.) and sequenced with a fluorescence-based automated sequencing system (Davis Sequencing, Davis, Calif.). The FastA program of the GCG software (version 10, Wisconsin Sequence Analysis Package; Genetics Computer Group) was applied first to determine the closest bacterial species or subspecies. Then, the GAP and PileUP programs were used for sequence alignments and determination of the percentage of DNA similarity.
IFA tests. (i) Bartonella spp.
B.
henselae, B. clarridgeiae, and B. vinsonii
subsp. berkhoffii indirect immunofluorescent antibody (IFA)
tests were performed as previously described (15, 16). The
intensity of bacillus-specific fluorescence was scored subjectively
from 1 to 4, and a fluorescence score of 
2 at a dilution of 1:64 was
reported as a positive result, as previously described
(16). The same two readers performed a double-blinded
reading of each slide. Negative and positive serum control samples were
obtained from two laboratory dogs before and after infection with
B. vinsonii subsp. berkhoffii and from cats
before and after infection with B. henselae and B. clarridgeiae.
(ii) Ehrlichia spp., B. burgdorferi, and C. burnetii Antibodies to Ehrlichia equi/Ehrlichia phagocytophila, Ehrlichia canis, and Ehrlichia ewingii were evaluated using commercially available IFA substrate slides (VMRD Inc., Pullman, Wash.) or purified E. equi-infected equine neutrophils, according to a previously described protocol (37). Known positive (a known-infected dog) and negative serum samples were run as controls on the same slide. B. burgdorferi antibodies were assessed by kinetic enzyme-linked immunosorbent assay and Western blotting at a reference laboratory (Diagnostic Laboratory, College of Veterinary Medicine, Cornell University, Ithaca, N.Y.).
Antibodies against phase I and phase II of C. burnetii were evaluated using a commercially available IFA substrate slide (Fuller Laboratories, Fullerton, Calif.) at a 1:64 dilution.| |
RESULTS |
|---|
|
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
|
|---|
Case report. On 4 April 2000, a 2.5-year-old, male neutered boxer was referred to the UC Davis Veterinary Medical Teaching Hospital with the diagnosis of acute third-degree AV block. The dog was acutely weak, lethargic, and nonambulatory.
The dog had been previously diagnosed by a board-certified veterinary cardiologist with a grade IV/VI left basilar systolic heart murmur due to valvular aortic stenosis at 16 months of age. Medical treatment consisted of a selective beta-blocker, atenolol (25 mg per os [p.o.] every 12 h [q12 h]). The dog was then referred to UC Davis Veterinary Medical Teaching Hospital for possible balloon valvuloplasty of the stenotic aortic valve on 28 September 1998. Echocardiography confirmed severe valvular aortic stenosis and mild aortic insufficiency, with a left ventricular-to-aortic pressure gradient of 120 mm Hg. The left ventricular papillary muscles were hyperechogenic, indicative of myocardial fibrosis. The electrocardiogram demonstrated an increased amplitude of the R waves consistent with left ventricular hypertrophy and an ST segment depression suggestive of regional myocardial hypoxia. An aortic balloon valvuloplasty was subsequently performed on 2 October 1998 without complication. The procedure was moderately successful, producing a decrease in the left ventricular-to-aortic pressure gradient to 80 mm Hg. Subsequent echocardiograms revealed static moderate valvular aortic stenosis with no changes in the left ventricular dimensions. The dog remained free of clinical signs until March 2000, when he collapsed after exercise. An echocardiogram revealed thickened hyperechogenic aortic cusps that had restricted systolic movement and appeared calcified. The left ventricular-to-aortic pressure gradient had increased to 100 mm Hg, indicating severe progressive valvular aortic stenosis. The aortic insufficiency had increased from mild to moderate. The atenolol dose was increased from 25 mg p.o. q12 h to 50 mg p.o. q12 h. The dog was presented on 4 April 2000 as a cardiac emergency. Abnormalities on physical examination included severe weakness and depression, anisocoria, hyperthermia (39.9°C [103.5°F]), tachypnea (56 breaths/min), severely diminished femoral pulses, severe bradycardia (27 beats/min), pale mucous membranes, and a grade IV/VI left basilar systolic murmur. The electrocardiogram revealed a third-degree AV block with a ventricular rate of 28 beats/min and an atrial rate of 160 beats/min (Fig. 1). An echocardiogram again revealed severe valvular aortic stenosis (Fig. 2A and B). However, at this examination, the valvular thickening had progressed dramatically. In addition, the cusps had a shaggy, hyperechoic appearance consistent with severe infective endocarditis. The aortic insufficiency was only trivial.
|
|
Macroscopic and microscopic lesions.
Gross examination at
necropsy revealed severe infective endocarditis. Although all aortic
cusps were involved, the most severely affected one was the right
coronary cusp (Fig. 3A and B). The noncoronary cusp lesion infiltrated the atrial septum and protruded into the right atrium near the region of the AV node. No myocardial infarcts were noted. There was a mild fibrous subaortic ring present and moderate left ventricular concentric hypertrophy. Histopathology of
the aortic valve revealed chronic, active, multifocal, moderate suppurative endocarditis. The aortic valve cusps contained fibroblasts, neutrophils, and hemosiderin-laden macrophages. However, Warthin-Starry staining failed to reveal bacteria. Similarly, no bacteria were visualized by electron microscopy on a fragment of the damaged aortic
valve.
|
The dog's environment. The dog lived in central California in a household with several other pets, including three previously stray cats that were adopted 2.5 to 3 years prior to the onset of the dog's illness. The cats were 3 to 3.5 years old at the time of this study. The dog and the cats were mainly indoor pets, but they spent several hours a day outside in a fenced yard. All animals were infested with fleas. The animals lived in an area where ticks are endemic, but there was no history of tick infestation. The pet's owner is a human health care professional employed by an area hospital.
Isolation and identification of Bartonella
Three blood cultures for aerobic and anaerobic bacteria failed to grow
bacteria. However, blood collected from the dog at the same time and
cultured from the frozen-thawed EDTA tube grew a nonhemolytic
gram-negative organism after 8 days, with only a few (seven), small
(0.5 to 1 mm) white colonies. The colony growth characteristics and
morphology were suggestive of Bartonella spp., based on
time to appear, size, and color. Microscopic examination demonstrated
elongated, slightly curved, gram-negative rods. PCR amplification with
gltA primers produced a 400-bp fragment strongly suggestive of Bartonella. Digestion with
TaqI and HhaI endonucleases produced an
RFLP profile identical to that of B. clarridgeiae (ATCC
57134) and different from those of B. henselae or
B. vinsonii subsp. berkhoffii (Fig.
4). Furthermore, partial sequencing of the gltA fragment (275 bp) indicated a sequence that was
100% identical to B. clarridgeiae (Table
1). The best score for the 16S rRNA gene
fragment (741 bp) from the search by the FastA program yielded
B. clarridgeiae as the closest match (Z
score of 418.0, versus 407.7 for B. henselae). None of
the three cat blood samples yielded any organisms on blood-enriched
agar plates.
|
|
Serologic analysis. Serum antibodies to B. clarridgeiae, B. vinsonii subsp. berkhoffii, and B. henselae were detected in the dog by IFA assay at reciprocal titers of 2,048 for B. clarridgeiae and 256 for the two other Bartonella species. The dog was also seropositive for E. equi/E. phagocytophila (reciprocal titer, 100) but was seronegative for E. canis, E. ewingii, B. burgdorferi, or C. burnetii. All three cats were seronegative for B. clarridgeiae, and two of the three cats had low titers for B. henselae (reciprocal titers of 128 and 64, respectively) and for B. vinsonii subsp. berkhoffii (1:64). The dog's owner was seronegative for all three Bartonella species tested.
PCR heart valve analysis. Bartonella DNA was amplified from the aortic valve but not from the pulmonic valve. After digestion of the gltA fragment, the PCR-RFLP profile observed was characteristic of B. clarridgeiae (Fig. 4) and the partial sequence was identical to B. clarridgeiae (Table 1). Although a fragment was amplified using the primers for the Bartonella 16S rRNA gene, the product was not clean enough for sequence analysis. No Ehrlichia or Borrelia DNA was amplified from the damaged aortic valve and the pulmonic valve.
| |
DISCUSSION |
|---|
|
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
|
|---|
We report here the first isolation of B. clarridgeiae
outside of its natural feline reservoir, as well as the first case of endocarditis associated with B. clarridgeiae. It is also the
first clinical case associated with the isolation of the infectious agent, as human cases of cat scratch disease caused by B. clarridgeiae have only been established serologically (29,
38, 46). In this dog, several factors support causation,
including (i) isolation of the organism from blood, (ii) failure to
isolate other bacteria by conventional blood culture, and (iii) PCR
amplification of B. clarridgeiae DNA from the abnormal
aortic valve but not the normal pulmonic valve. Unfortunately, we were
not able to confirm microscopically the presence of bacilli in
the damaged valve. More likely, this negative result could be
associated with the paucity of bacilli in the lesion as well as the
testing of a very limited amount of the damaged tissue, most of it
being used for PCR testing. The valvular lesion was located mainly on
the aortic valve, as previously reported for Bartonella
endocarditis cases in dogs (6, 9). As reported by those
authors, endocarditis associated with Bartonella and other
-Proteobacteria mainly involves the aortic valve (70%),
in contrast to a review of five studies of bacterial endocarditis in
which the mitral valve was involved more often than the aortic valve
(67% versus 23%). Increased predilection for aortic valve involvement
could be explained by preexisting valvular disease, such as subaortic
stenosis, for which boxers are congenitally predisposed. Similarly, in
humans, in a series of 33 patients with Bartonella
endocarditis, 29 (88%) had involvement of the aortic valve, including
2 with concurrent aortic and mitral valvular involvement, compared to
only 4 patients with involvement only of the mitral valve
(43). In a cohort of 15 patients with Bartonella endocarditis, more than half of the patients
(53%) had preexisting valvular disease (34). Furthermore,
the human case of endocarditis caused by B. vinsonii subsp.
berkhoffii had a bicuspid aortic valve with thickened cusps
and significant regurgitation (45), and the patient from
whom B. elizabethae was isolated had large vegetations on
the aortic valve (19). In humans, blood culture-negative
endocarditis comprises between 5 and 30% of all cases of infective
endocarditis (5, 50, 51). Bartonella endocarditis accounts for 3 to 10% of human endocarditis cases (10, 33). In one series, Bartonella infection
accounted for 10 (3.3%) of 299 cases of endocarditis (10,
43), and in another series of 369 patients with endocarditis, 38 (10.3%) were diagnosed with Bartonella sp. endocarditis
(33). Although the clinical incidence of infective
endocarditis in dogs is unknown, reported prevalences at necropsy vary
from 0.06 to 6.6% (48). However, as in human beings
(43), negative blood cultures are obtained from a high
number (24 to 75%) of canine endocarditis cases (11, 12,
47). Unfortunately, no data are available yet to determine the
prevalence of Bartonella endocarditis among all infective canine endocarditis cases.
B. clarridgeiae has been reported as a potential zoonotic agent causing cat scratch disease, based on serologic evidence (29, 38). Recently, Sander et al. (46) indicated that 3.9% of 724 patients suffering from lymphadenopathy had antibodies specific for the FlaA protein of B. clarridgeiae. Human cases of endocarditis caused by B. clarridgeiae will likely be diagnosed in the near future, just as B. vinsonii subsp. berkhoffii was initially diagnosed in dogs and later in a human endocarditis case. It is noteworthy that in the present case the dog's owner was Bartonella seronegative and therefore unlikely to have been infected by Bartonella spp.
The source of infection and mode of transmission of B. clarridgeiae for this dog will most likely remain unexplained. The presence of several formerly stray cats in the household could be the source of infection, as domestic cats have been shown to be the main reservoir for B. clarridgeiae (17, 24, 28, 30). Although two of the three cats were B. henselae seropositive, none had B. clarridgeiae-specific antibodies and all three cats were Bartonella negative by blood culture, making it unlikely that they were the origin of the dog's infection. Bartonella infections have been shown to be vector borne, and cat fleas (Ctenocephalides felis) are the main vectors for cat-to-cat transmission of B. henselae (18, 22). Cat fleas are also considered to be the vector for B. clarridgeiae infection among cats (8). Fleas and flea dirt were observed on the household cats and therefore could have been potential vectors for the dog's Bartonella infection, as cat fleas are also the main flea species that infests dogs (3, 21). The dog was found to be not only Bartonella seropositive but also seropositive for E. phagocytophila/E. equi, an infectious agent known to be transmitted by ticks. The observation of past tick exposure in this dog raises the possibility of acquisition of the infection through a tick bite. Ticks have been suspected as the possible vector of B. vinsonii subsp. berkhoffii in dogs, based on epidemiological (41) and serological (2, 7, 32) evidence, as most B. vinsonii subsp. berkhoffii-seropositive dogs were also seropositive for E. canis or Babesia canis. Similarly, Davoust et al. reported that B. vinsonii subsp. berkhoffii-positive dogs were more likely to be infested by Rhipicephalus sanguineus ticks (P < 0.001) (B. Davoust, M. Drancourt, M. Boni, J. Signot, V. Roux, and D. Raoult, Eur. Working Group on Rickettsia-Am. Soc. Rickettsiol. Joint Meeting, Marseille, France, abstr. 232B, 1999). Tick transmission was also highly suspected in two human cases of B. henselae infection (36). Finally, we have been able to identify Bartonella DNA in Ixodes pacificus questing adult ticks from coastal northern California (14). However, more investigations are needed to better understand how B. clarridgeiae is transmitted among cats and dogs, the respective roles of fleas and ticks as vectors for this bacterium, and the potential risk for humans to acquire this infection.
| |
ACKNOWLEDGMENTS |
|---|
This project was supported in part by a grant from the Center for Companion Animal Health, School of Veterinary Medicine, UC Davis.
We thank Robert Munn, Amy Poland, Courtney Rand, and Christian Leutenegger for technical assistance. We also thank M. A. Greeley and R. J Higgins for performing the histopathology analysis.
| |
FOOTNOTES |
|---|
* Corresponding author. Mailing address: Department of Population Health and Reproduction, School of Veterinary Medicine, University of California, Davis, CA 95616. Phone: (530) 752-8112. Fax: (530) 752-2377. E-mail: bbchomel{at}ucdavis.edu.
| |
REFERENCES |
|---|
|
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
|
|---|
| 1. | Anderson, B. E., and M. A. Neuman. 1997. Bartonella spp. as emerging human pathogens. Clin. Microbiol. Rev. 10:203-219[Abstract]. |
| 2. | Baneth, G., E. B. Breitschwerdt, B. C. Hegarty, B. Pappalardo, and J. Ryan. 1998. A survey of tick-borne bacteria and protozoa in naturally exposed dogs from Israel. Vet. Parasitol. 74:133-142[CrossRef][Medline]. |
| 3. | Beresford-Jones, W. P. 1981. Prevalence of fleas on dogs and cats in an area of central London. J. Small Anim. Pract. 22:27-29[Medline]. |
| 4. |
Birtles, R. J., and D. Raoult.
1996.
Comparison of partial citrate synthase gene (gltA) sequences for phylogenetic analysis of Bartonella species.
Int. J. Syst. Bacteriol.
46:891-897 |
| 5. |
Breathnach, A. S.,
J. M. Hoare, and S. J. Eykyn.
1997.
Culture-negative endocarditis: contribution of Bartonella infections.
Heart
77:474-476 |
| 6. |
Breitschwerdt, E. B.,
C. E. Atkins,
T. T. Brown,
D. L. Kordick, and P. S. Snyder.
1999.
Bartonella vinsonii subsp. berkhoffii and related members of the alpha subdivision of the Proteobacteria in dogs with cardiac arrhythmias, endocarditis or myocarditis.
J. Clin. Microbiol.
37:3618-3626 |
| 7. |
Breitschwerdt, E. B.,
B. C. Hegarty, and S. I. Hancock.
1998.
Sequential evaluation of dogs naturally infected with Ehrlichia canis, Ehrlichia chaffeensis, Ehrlichia equi, Ehrlichia ewingii, or Bartonella vinsonii.
J. Clin. Microbiol.
36:2645-2651 |
| 8. |
Breitschwerdt, E. B., and D. L. Kordick.
2000.
Bartonella infection in animals: carriership, reservoir potential, pathogenicity, and zoonotic potential for human infection.
Clin. Microbiol. Rev.
13:428-438 |
| 9. | Breitschwerdt, E. B., D. L. Kordick, D. E. Malarkey, B. Keene, T. L. Hadfield, and K. Wilson. 1995. Endocarditis in a dog due to infection with a novel Bartonella subspecies. J. Clin. Microbiol. 33:154-160[Abstract]. |
| 10. |
Brouqui, P., and D. Raoult.
2001.
Endocarditis due to rare and fastidious bacteria.
Clin. Microbiol. Rev.
14:177-207 |
| 11. | Calvert, C. A. 1982. Valvular bacterial endocarditis in the dog. J. Am. Vet. Med. Assoc. 180:1080-1084[Medline]. |
| 12. | Calvert, C. A., C. E. Greene, and E. M. Hardie. 1985. Cardiovascular infections in dogs: epizootiology, clinical manifestations, and prognosis. J. Am. Vet. Med. Assoc. 187:612-616[Medline]. |
| 13. | Chang, C. C., B. B. Chomel, R. W. Kasten, R. Heller, K. M. Kocan, H. Ueno, K. Yamamoto, C. Elmi, V. C. Bleich, B. M. Pierce, B. J. Gonzales, P. K. Swift, W. M. Boyce, S. S. Jang, H. Boulouis, and Y. Piemont. 2000. Isolation of Bartonella spp. from wild cervids, bovids, and domestic cattle in North America. Emerg. Infect. Dis. 6:306-311[Medline]. |
| 14. |
Chang, C. C.,
B. B. Chomel,
R. W. Kasten,
V. Romano, and N. Tietze.
2001.
Molecular evidence of Bartonella spp. in questing adult Ixodes pacificus ticks in California.
J. Clin. Microbiol.
39:1221-1226 |
| 15. |
Chang, C. C.,
R. W. Kasten,
B. B. Chomel,
D. C. Simpson,
C. M. Hew,
D. L. Kordick,
R. Heller,
Y. Piemont, and E. B. Breitschwerdt.
2000.
Coyotes (Canis latrans) as the reservoir for a human pathogenic Bartonella sp.: Molecular epidemiology of Bartonella vinsonii subsp. berkhoffii infection in coyotes from central coastal California.
J. Clin. Microbiol.
38:4193-4200 |
| 16. | Chomel, B. B., R. C. Abbott, R. W. Kasten, K. A. Floyd-Hawkins, P. H. Kass, C. A. Glaser, N. C. Pedersen, and J. E. Koehler. 1995. Bartonella henselae prevalence in domestic cats in California: risk factors and association between bacteremia and antibody titers. J. Clin. Microbiol. 33:2445-2450[Abstract]. |
| 17. | Chomel, B. B., E. T. Carlos, R. W. Kasten, K. Yamamoto, C. C. Chang, R. S. Carlos, M. V. Abenes, and C. M. Pajares. 1999. Bartonella henselae and Bartonella clarridgeiae infection in domestic cats from The Philippines. Am. J. Trop. Med. Hyg. 60:593-597[Abstract]. |
| 18. | Chomel, B. B., R. W. Kasten, K. Floyd-Hawkins, B. Chi, K. Yamamoto, J. Roberts-Wilson, A. N. Gurfield, R. C. Abbott, N. C. Pedersen, and J. E. Koehler. 1996. Experimental transmission of Bartonella henselae by the cat flea. J. Clin. Microbiol. 34:1952-1956[Abstract]. |
| 19. |
Daly, J. S.,
M. G. Worthington,
D. J. Brenner,
C. W. Moss,
D. G. Hollis,
R. S. Weyant,
A. G. Steigerwalt,
R. E. Weaver,
M. I. Daneshvar, and S. P. O'Connor.
1993.
Rochalimaea elizabethae sp. nov. isolated from a patient with endocarditis.
J. Clin. Microbiol.
31:872-881 |
| 20. |
Drancourt, M.,
J. L. Mainardi,
P. Brouqui,
F. Vandenesch,
A. Carta,
F. Lehnert,
J. Etienne,
F. Goldstein,
J. Acar, and D. Raoult.
1995.
Bartonella (Rochalimaea) quintana endocarditis in three homeless men.
N. Engl. J. Med.
332:419-423 |
| 21. | Dryden, M. W., and M. K. Rust. 1994. The cat flea: biology, ecology and control. Vet. Parasitol. 52:1-19[CrossRef][Medline]. |
| 22. | Foil, L., E. Andress, R. L. Freeland, A. F. Roy, R. Rutledge, P. C. Triche, and K. L. O'Reilly. 1998. Experimental infection of domestic cats with Bartonella henselae by inoculation of Ctenocephalides felis (Siphonaptera: Pulicidae) feces. J. Med. Entomol. 35:625-628[Medline]. |
| 23. | Gurfield, A. N., H. J. Boulouis, B. B. Chomel, R. Heller, R. W. Kasten, K. Yamamoto, and Y. Piemont. 1997. Coinfection with Bartonella clarridgeiae and Bartonella henselae and with different Bartonella henselae strains in domestic cats. J. Clin. Microbiol. 35:2120-2123[Abstract]. |
| 24. | Heller, R., M. Artois, V. Xemar, D. De Briel, H. Gehin, B. Jaulhac, H. Monteil, and Y. Piemont. 1997. Prevalence of Bartonella henselae and Bartonella clarridgeiae in stray cats. J. Clin. Microbiol. 35:1327-1331[Abstract]. |
| 25. |
Heller, R.,
M. Kubina,
P. Mariet,
P. Riegel,
G. Delacour,
C. Dehio,
F. Lamarque,
R. Kasten,
H. J. Boulouis,
H. Monteil,
B. Chomel, and Y. Piemont.
1999.
Bartonella alsatica sp. nov., a new Bartonella species isolated from the blood of wild rabbits.
Int. J. Syst. Bacteriol.
49:283-288 |
| 26. |
Kerkhoff, F. T.,
A. M. C. Bergmans,
A. Van Der Zee, and A. Rothova.
1999.
Demonstration of Bartonella grahamii DNA in ocular fluids of a patient with neuroretinitis.
J. Clin. Microbiol.
37:4034-4038 |
| 27. | Kitchell, B. E., T. M. Fan, D. L. Kordick, E. B. Breitschwerdt, G. Wollenberg, and C. A. Lichtensteiger. 2000. Peliosis hepatis in a dog infected with Bartonella henselae. J. Am. Vet. Med. 216:519-523. |
| 28. | Kordick, D. L., and E. B. Breitschwerdt. 1998. Persistent infection of pets within a household with three Bartonella species. Emerg. Infect. Dis. 4:325-328[Medline]. |
| 29. | Kordick, D. L., E. J. Hilyard, T. L. Hadfield, K. H. Wilson, A. G. Steigerwalt, D. J. Brenner, and E. B. Breitschwerdt. 1997. Bartonella clarridgeiae, a newly recognized zoonotic pathogen causing inoculation papules, fever, and lymphadenopathy (cat scratch disease). J. Clin. Microbiol. 35:1813-1818[Abstract]. |
| 30. | Kordick, D. L., M. G. Papich, and E. B. Breitschwerdt. 1997. Efficacy of enrofloxacin or doxycycline for treatment of Bartonella henselae or Bartonella clarridgeiae infection in cats. Antimicrob. Agents Chemother. 41:2448-2455[Abstract]. |
| 31. |
Kordick, D. L.,
B. Swaminathan,
C. E. Greene,
K. H. Wilson,
A. M. Whitney,
S. O'Connor,
D. G. Hollis,
G. M. Matar,
A. G. Steigerwalt,
G. B. Malcolm,
P. S. Hayes,
T. L. Hadfield,
E. B. Breitschwerdt, and D. J. Brenner.
1996.
Bartonella vinsonii subsp. berkhoffii subsp. nov., isolated from dogs; Bartonella vinsonii subsp. vinsonii; and emended description of Bartonella vinsonii.
Int. J. Syst. Bacteriol.
46:704-709 |
| 32. |
Kordick, S. K.,
E. B. Breitschwerdt,
B. C. Hegarty,
K. L. Southwick,
C. M. Colitz,
S. I. Hancock,
J. M. Bradley,
R. Rumbough,
J. T. McPherson, and J. N. MacCormack.
1999.
Coinfection with multiple tick-borne pathogens in a Walker Hound kennel in North Carolina.
J. Clin. Microbiol.
37:2631-2638 |
| 33. |
La Scola, B., and D. Raoult.
1999.
Culture of Bartonella quintana and Bartonella henselae from human samples: a 5-year experience (1993 to 1998).
J. Clin. Microbiol.
37:1899-1905 |
| 34. |
Lepidi, H.,
P. E. Fournier, and D. Raoult.
2000.
Quantitative analysis of valvular lesions during Bartonella endocarditis.
Am. J. Clin. Pathol.
114:880-889 |
| 35. |
Leutenegger, C. M.,
N. Pusterla,
C. N. Mislin,
R. Weber, and H. Lutz.
1999.
Molecular evidence of coinfection of ticks with Borrelia burgdorferi sensu lato and the human granulocytic ehrlichiosis agent in Switzerland.
J. Clin. Microbiol.
37:3390-3391 |
| 36. | Lucey, D., M. J. Dolan, C. W. Moss, M. Garcia, D. G. Hollis, and S. Wegner. 1992. Relapsing illness due to Rochalimaea henselae in immunocompetent host: implication for therapy and new epidemiological associations. Clin. Infect. Dis. 14:683-688[Medline]. |
| 37. | Madigan, J. E., S. Hietala, S. Chambers, and E. DeRock. 1990. Seroepidemiologic survey of antibodies to Ehrlichia equi in horses in northern California. J. Am. Vet. Med. Assoc. 196:1962-1964[Medline]. |
| 38. | Margileth, A. M., and D. F. Baehren. 1998. Chest-wall abscess due to cat-scratch disease (CSD) in an adult with antibodies to Bartonella clarridgeiae: case report and review of the thoracopulmonary manifestations of CSD. Clin. Infect. Dis. 27:353-357[Medline]. |
| 39. | Norman, A. F., R. Regnery, P. Jameson, C. Greene, and D. C. Krause. 1995. Differentiation of Bartonella-like isolates at the species level by PCR-restriction fragment length polymorphism in the citrate synthase gene. J. Clin. Microbiol. 33:1797-1803[Abstract]. |
| 40. | Pappalardo, B. L., T. Brown, J. L. Gookin, C. L. Morrill, and E. B. Breitschwerdt. 2000. Granulomatous disease associated with Bartonella infection in 2 dogs. J. Vet. Intern. Med. 14:37-42[CrossRef][Medline]. |
| 41. | Pappalardo, B. L., M. T. Correa, C. C. York, C. Y. Peat, and E. B. Breitschwerdt. 1997. Epidemiologic evaluation of the risk factors associated with exposure and seroreactivity to Bartonella vinsonii in dogs. Am. J. Vet. Res. 58:467-471[Medline]. |
| 42. |
Pusterla, N.,
J. B. Huder,
C. M. Leutenegger,
U. Braun,
J. E. Madigan, and H. Lutz.
1999.
Quantitative real-time PCR for detection of members of the Ehrlichia phagocytophila genogroup in host animals and Ixodes ricinus ticks.
J. Clin. Microbiol.
37:1329-1331 |
| 43. |
Raoult, D.,
P. E. Fournier,
M. Drancourt,
T. J. Marrie,
J. Etienne,
J. Cosserat,
P. Cacoub,
Y. Poinsignon,
P. Leclercq, and A. M. Sefton.
1996.
Diagnosis of 22 new cases of Bartonella endocarditis.
Ann. Intern. Med.
125:646-652 |
| 44. |
Regnery, R. L.,
B. E. Anderson,
J. E. Clarridge III,
M. C. Rodriguez-Barradas,
D. C. Jones, and J. H. Carr.
1992.
Characterization of a novel Rochalimaea species, R. henselae sp. nov., isolated from blood of a febrile, human immunodeficiency virus-positive patient.
J. Clin. Microbiol.
30:265-274 |
| 45. |
Roux, V.,
S. J. Eykyn,
S. Wyllie, and D. Raoult.
2000.
Report of Bartonella vinsonii subspecies berkhoffii as an agent of afebrile blood culture negative endocarditis in man.
J. Clin. Microbiol.
38:1698-1700 |
| 46. |
Sander, A.,
A. Zagrosek,
W. Bredt,
E. Schiltz,
Y. Piemont,
C. Lanz, and C. Dehio.
2000.
Characterization of Bartonella clarridgeiae flagellin (FlaA) and detection of antiflagellin antibodies in patients with lymphadenopathy.
J. Clin. Microbiol.
38:2943-2948 |
| 47. | Sisson, D., and W. P. Thomas. 1984. Endocarditis of the aortic valve in the dog. J. Am. Vet. Med. Assoc. 184:570-577[Medline]. |
| 48. | Sisson, D., and W. P. Thomas. 1986. Current veterinary therapy IX, p. 402-406. W.B. Saunders Company, Philadelphia, Pa. |
| 49. |
Spach, D. H.,
K. P. Callis,
D. S. Paauw,
Y. B. Houze,
F. D. Schoenknecht,
D. F. Welch,
H. Rosen, and D. J. Brenner.
1993.
Endocarditis caused by Rochalimaea quintana in a patient infected with human immunodeficiency virus.
J. Clin. Microbiol.
31:692-694 |
| 50. | Tunkel, A. R., and D. Kaye. 1992. Endocarditis with negative blood cultures. N. Engl. J. Med. 326:1215-1217[Medline]. |
| 51. | Watanakunakorn, C., and T. Burkert. 1993. Infective endocarditis at a large community teaching hospital, 1980-1990: a review of 210 episodes. Medicine 72:90-102[Medline]. |
| 52. |
Welch, D. F.,
K. C. Carroll,
E. K. Hofmeister,
D. H. Persing,
D. A. Robison,
A. G. Steigerwalt, and D. J. Brenner.
1999.
Isolation of a new subspecies, Bartonella vinsonii subsp. arupensis, from a cattle rancher: identity with isolates found in conjunction with Borrelia burgdorferi and Babesia microti among naturally infected mice.
J. Clin. Microbiol.
37:2598-2601 |
Journal of Clinical Microbiology, October 2001, p. 3548-3554, Vol. 39, No. 10
0095-1137/01/$04.00+0 DOI: 10.1128/JCM.39.10.3548-3554.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
This article has been cited by other articles:
-
Henn, J. B., Gabriel, M. W., Kasten, R. W., Brown, R. N., Koehler, J. E., MacDonald, K. A., Kittleson, M. D., Thomas, W. P., Chomel, B. B.
(2009). Infective Endocarditis in a Dog and the Phylogenetic Relationship of the Associated "Bartonella rochalimae" Strain with Isolates from Dogs, Gray Foxes, and a Human. J. Clin. Microbiol.
47: 787-790
[Abstract] [Full Text] -
Henn, J. B., Gabriel, M. W., Kasten, R. W., Brown, R. N., Theis, J. H., Foley, J. E., Chomel, B. B.
(2007). Gray Foxes (Urocyon cinereoargenteus) as a Potential Reservoir of a Bartonella clarridgeiae-Like Bacterium and Domestic Dogs as Part of a Sentinel System for Surveillance of Zoonotic Arthropod-Borne Pathogens in Northern California. J. Clin. Microbiol.
45: 2411-2418
[Abstract] [Full Text] -
Pesavento, P. A., Chomel, B. B., Kasten, R. W., McDonald, K. A., Mohr, F. C.
(2005). Pathology of Bartonella Endocarditis in Six Dogs. Vet Pathol
42: 370-373
[Abstract] [Full Text] -
Breitschwerdt, E. B., Blann, K. R., Stebbins, M. E., Munana, K. R., Davidson, M. G., Jackson, H. A., Willard, M. D.
(2004). Clinicopathological Abnormalities and Treatment Response in 24 Dogs Seroreactive to Bartonella vinsonii (berkhoffii) Antigens. Journal of the American Animal Hospital Association
40: 92-101
[Abstract] [Full Text] -
Chomel, B. B., Wey, A. C., Kasten, R. W.
(2003). Isolation of Bartonella washoensis from a Dog with Mitral Valve Endocarditis. J. Clin. Microbiol.
41: 5327-5332
[Abstract] [Full Text] -
Chomel, B. B., Wey, A. C., Kasten, R. W., Stacy, B. A., Labelle, P.
(2003). Fatal Case of Endocarditis Associated with Bartonella henselae Type I Infection in a Domestic Cat. J. Clin. Microbiol.
41: 5337-5339
[Abstract] [Full Text] -
Mexas, A. M., Hancock, S. I., Breitschwerdt, E. B.
(2002). Bartonella henselae and Bartonella elizabethae as Potential Canine Pathogens. J. Clin. Microbiol.
40: 4670-4674
[Abstract] [Full Text]
| |||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
Copyright © 2009 by the American Society for Microbiology. For an alternate route to Journals.ASM.org, visit: http://intl-journals.asm.org | More Info»