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Previous Article | Next Article 
Journal of Clinical Microbiology, August 1999, p. 2598-2601, Vol. 37, No. 8
0095-1137/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
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
David F.
Welch,1,2,*
Karen C.
Carroll,3
Erik K.
Hofmeister,4
David H.
Persing,4
Denise A.
Robison,5
Arnold G.
Steigerwalt,6 and
Don
J.
Brenner6
Laboratory Corporation of America,
Dallas, Texas 752301; Department of
Pathology, University of Texas Southwestern Medical Center, Dallas,
Texas 752352; Associated and Regional
University Pathologists, Inc., and Department of Pathology, University
of Utah Medical Center, Salt Lake City, Utah
841083; Department of Laboratory
Medicine and Pathology, Mayo Foundation, Rochester, Minnesota
559054; Clinical Microbiology
Laboratory, University Hospitals, Oklahoma City, Oklahoma
731265; and Meningitis and Special
Pathogens Branch, Division of Bacterial and Mycotic Diseases, National
Center for Infectious Diseases, Centers for Disease Control and
Prevention, Atlanta, Georgia 303336
Received 8 February 1999/Returned for modification 15 March
1999/Accepted 4 May 1999
 |
ABSTRACT |
Bacteremia with fever due to a novel subspecies of Bartonella
vinsonii was found in a cattle rancher. The subspecies shared major characteristics of the genus Bartonella in terms of
most biochemical features and cellular fatty acid profile, but it was distinguishable from other subspecies of B. vinsonii by
good growth on heart infusion agar supplemented with X factor and by
its pattern of enzymatic hydrolysis of peptide substrates. DNA
relatedness studies verified that the isolate belonged to the genus
Bartonella and that it was genotypically related to
B. vinsonii. The highest level of relatedness was observed
with recently characterized strains from naturally infected mice that
were coinfected with Borrelia burgdorferi and Babesia
microti. We propose the name Bartonella vinsonii
subsp. arupensis subsp. nov. as the new subspecies to
accommodate these human and murine isolates.
| |
INTRODUCTION |
Bartonella vinsonii was
described as the Canadian vole agent in 1946 by Baker
(1). It was further characterized by Weiss and Dasch
(17), who proposed the name Rochalimaea vinsonii
in 1982. The members of the genus Rochalimaea were then
reclassified as Bartonella spp. on the basis of DNA
relatedness and 16S rRNA sequence data by Brenner and coworkers in 1993 (5). B. vinsonii has not heretofore been
implicated in human disease, although a subspecies
(Bartonella vinsonii subsp. berkhoffii) causing
canine endocarditis was recently described (3, 11).
The characterization of novel Bartonella species and
subspecies continues (2, 7, 8, 10, 11, 13). A study
originally intended to determine the prevalence of Borrelia
burgdorferi, Babesia microti, and Ehrlichia
species in Minnesota and Wisconsin mice identified, instead of any
animals infected with Ehrlichia spp., four
Bartonella-infected animals by using Ehrlichia
PCR primers (9). Analysis of the citrate synthase gene
sequence of one of the isolates showed that it was most closely related to B. vinsonii. Prior to that report, our laboratory
received an isolate from the blood culture of a Wyoming man which we
confirmed as B. vinsonii. In light of these two findings, we
were led to compare the human isolate and the isolates from nature for
DNA relatedness as well as to describe the Wyoming man's case and the
isolate itself.
| |
CASE REPORT |
Case history.
The patient is a 62-year-old Caucasian male who
was admitted in May 1994 to a community hospital in Wyoming with acute
onset of confusion, difficulty in walking, and facial numbness. The patient had been well 48 h prior to admission. He is a rancher by
occupation, and he had been very active ranching and irrigating in the
days prior to the onset of symptoms. Two days prior to admission he
developed some low-grade "warm and cold" feelings and fatigue. He
also experienced some dizziness, characterized as a feeling of
instability when walking and doing chores. A mild headache and
myalgias, but no stiffness or photophobia, were also reported. He took
aspirin and ibuprofen for these symptoms. On the day of admission, his
legs "got stiff," and he fell when trying to get up from a seated
position while branding cattle. He was noted to have slurred speech and
to be confused. There was no evidence of seizure activity. The pulse
was rapid and irregular. No other symptoms were reported.
The medical history is significant for an ill-defined rheumatologic
disease characterized by a high positive antinuclear antibody level,
elevated erythrocyte sedimentation rate, positive rheumatoid factor,
Sjögren's syndrome, and polyneuropathy, diagnosed in 1960 after
a lengthy hospitalization in California. The rheumatologic syndrome is
also characterized by variable neurological manifestations, including
aseptic meningitis. Relapses are managed by high-dose intravenous
steroids. In 1987 he was treated with prednisone for a presumed relapse
of vasculitis when he presented with vertigo, headache, and numbness of
the hands. Between exacerbations, he is relatively asymptomatic, and he
does not require long-term steroid therapy.
On admission, the patient had a temperature of 100.9°F (38.3°C).
Blood pressure was 150/90 mm Hg, the pulse was 120/min, and the
respiratory rate was 16/min. He appeared encephalopathic but in no
acute distress. A skin examination revealed no stigmata of vasculitis.
Examination of the head, eyes, ears, nose, and throat was normal. The
neck was supple, and there was no adenopathy. The heart rate was
irregularly irregular without murmurs, rubs, or gallops. The lungs were
clear to percussion and auscultation. There was no hepatosplenomegaly
or mass found on abdominal examination. The neurological examination
was significant for decreased sensation in the area innervated by the
right-fifth-cranial nerve. There was a palsy of the right fourth
cranial-nerve, and the gag reflex was absent. He had bilateral diplopia
and slurred speech. There was no visual-field defect. He had
hyperreflexia with bilateral clonus. He exhibited decreased
concentration and emotional lability on mental-status examination but
was otherwise fully oriented.
The peripheral leukocyte count was 8,700/µl with 81% neutrophils,
8% band forms, and 10% lymphocytes; platelet count was 166,000/µl and the hematocrit was 41.3%. A cerebrospinal fluid (CSF) analysis was
performed, and there were three leukocytes, undifferentiated. CSF
protein was 49 mg/dl, and glucose was 45 mg/dl (peripheral glucose, 120 mg/dl). Other CSF study results included a serum-to-CSF immunoglobulin
G ratio of 0.31, positive oligoclonal bands, but a normal
immunoglobulin G index. The erythrocyte sedimentation rate was 45 mm/h.
A chemistry screen was normal except for a serum glutamic oxalacetic
transaminase level of 53 µ/liter and a lactate dehydrogenase level of
190 µ/liter. An antinuclear antibody test was positive, showing a
1:2,560 titer with a speckled pattern. Magnetic resonance imaging of
the head showed an area of increased signal in T2-weighted images in
the middle and superior portions of the pons. A computerized axial
tomography scan of the head was normal. An echocardiogram showed
moderate mitral and tricuspid insufficiency and mild aortic
insufficiency but no evidence of endocarditis. An electrocardiogram
revealed atrial flutter. Blood cultures were obtained on admission,
including one set in BACTEC bottles and one in an Isolator, which grew
five colonies of a gram-negative bacillus at day 7 on chocolate agar.
The organism was sent to the microbiology laboratory of Associated and
Regional University Pathologists, Inc., for identification. The
organism was identified as a Bartonella species, but not
B. henselae or B. quintana. The organism was then
sent to D. F. Welch for further characterization.
The patient initially had 24 to 36 h of temperatures as high as
39°C; he received a single 1-g dose of ceftriaxone, after which he
defervesced. Prednisone (40 mg) was administered for presumptive
cerebral vasculitis related to Sjögren's syndrome. Anticoagulation was begun because of the atrial flutter. He was discharged after 7 days of hospitalization with a significant improvement in neurologic symptoms. He has gradually been tapered off
steroids; persistent neurologic deficits include mild dizziness, slight
difficulty in swallowing, and mild ophthalmoplegia. He has not required
hospital admission since 1994, and he continues an active lifestyle as
a rancher in rural Montana.
| |
MATERIALS AND METHODS |
Strains.
The following type strains were obtained from the
American Type Culture Collection: Bartonella henselae ATCC
49793, Bartonella quintana ATCC 51694, Bartonella
vinsonii subsp. vinsonii ATCC VR-152, B. vinsonii subsp. berkhoffii ATCC 51672, and
Bartonella elizabethae ATCC 49927. The isolate described in
"Case history" was designated OK 94-513. Cultures were maintained
on Columbia agar supplemented with 5% defibrinated sheep blood.
DNA relatedness studies.
The strains used in DNA relatedness
determinations are listed in Table 1. The
methods used for isolation and purification of bacterial DNA and the
hydroxyapatite method used for DNA relatedness determinations have been
described previously (4). Divergence (D) was calculated to
the nearest 0.5%. All reactions were done at least twice.
Phenotypic studies.
Conventional biochemical tests and
commercial panels of biochemicals were used as described elsewhere
(15, 18). Briefly, inocula were obtained from cultures
growing on Columbia blood agar that were incubated for 5 to 7 days at
35°C in 5 to 10% CO2. For determining biochemical
reactivity based on preformed enzymes, suspensions equivalent to a
McFarland no. 2 turbidity standard were prepared in sterile water. A
dehydrated panel containing 24 substrates (Rapid Anaerobe Panel; Dade
International, Inc., West Sacramento, Calif.) was inoculated and
incubated at 35°C for 4 h, after which the results were
interpreted according to the manufacturer's directions. Suspensions
equivalent to a 0.5 McFarland turbidity standard were prepared in
saline for determining X-factor growth requirements, with strips
(Difco, Detroit, Mich.) applied to heart infusion agar, or in
Trypticase soy broth for susceptibility testing by the E-test technique
(AB Biodisk, Culver City, Calif.) on Columbia blood agar. Cellular
fatty acid compositions were analyzed by gas-liquid chromatography, and
immunofluorescence tests were performed as previously described
(15, 19).
| |
RESULTS |
DNA relatedness studies.
Labeled DNAs from the patient strain,
OK 94-513, and from three separate passages of mouse strain 95 0726 14a
were reacted with unlabeled DNAs from each other and from type strains
of Bartonella species (Table 1). Relatedness of the patient
strain and the passages of the mouse strain was 72 to 82% at 55°C
(optimal criterion for DNA reassociation), with a D of 2.0 to 3.5%.
Relatedness at the stringent (70°C) reaction temperature was 77 to
80%. Reciprocal DNA relatedness of the human and mouse strains to
B. vinsonii subsp. vinsonii and B. vinsonii subsp. berkhoffii was 65 to 85% at 55°C,
with a D of 4.5 to 7%; relatedness in 70°C reactions was 57 to 71%.
Relatedness of the human and mouse strains to all other
Bartonella species for which strains are available (there are no strains for Bartonella talpae, Bartonella
peromysci, and Bartonella taylorii) was 23 to 68% at
55°C, with a D of 10 to 13.5%. Similar results were obtained when
labeled DNAs from the type strains of B. vinsonii subsp.
vinsonii (Table 1) and B. vinsonii subsp.
berkhoffii were used.
Phenotypic characterization of isolate.
The organism was
initially recognized as a fastidious, small, gram-negative rod, based
on its Gram staining properties and its recovery on chocolate agar
after 7 days of incubation in an Isolator-processed blood culture. It
was catalase and oxidase negative, and it was unreactive with
immunodiagnostic reagents specific for Brucella,
Francisella, B. henselae, and B. quintana. The cellular fatty acid profile was consistent with
Bartonella spp., however, characterized by a large amount
(~50%) of C18:1
7C and only four other cellular
fatty acids in significant amounts: C16:0, 13%;
C17:0, 9%; C17:16C, 3%; and
C18:0, 16%.
Biochemical analysis with preformed enzyme-dependent
substrate utilization assays revealed reactivity with substrates
bis p-nitrophenyl-phosphate,
L-leucine-
-naphthylamide,
L-lysine--naphthylamide (alkaline),
glycylglycine--naphthylamide, glycine--naphthylamide, L-arginine--naphthylamide,
L-tryptophan--naphthylamide, and DL-methionine--naphthylamide (weakly
positive); there was no reactivity with substrates
p-nitrophenyl--D-galactopyranoside, p-nitrophenyl-
-D-galac-topyranoside, p-nitrophenyl-N-actelyl--D-glucosaminide, p-nitrophenyl--D-glucopyranoside,
p-nitrophenyl--D-glu-copyranoside, p-nitrophenyl-phosphate, p-nitrophenyl--L-fucopyranoside, p-nitrophenyl--D-mannopyranoside, L-lysine--naphthylamide (acid), L-prolyl--naphthylamide, L-pyrrolindonyl--naphthylamide,
3-indoxyl phosphate, trehalose, urea, indole, and nitrate. A comparison
of these results with those which could help distinguish other
Bartonella species or subspecies is shown in Table
2. Also shown in Table 2 are the results
of motility testing by wet mount and growth tests on heart infusion
agar plus X factor, which also distinguish the isolate from B. henselae and from B. quintana, although the latter grew weakly in the presence of the X factor.
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|
TABLE 2.
Differential phenotypic characteristics of the case
isolate compared to those of representative strains of other
Bartonella species
or subspeciesa
|
|
The isolate displayed in vitro susceptibility (MIC < 0.5 µg/ml)
to ampicillin, penicillin, cefotaxime, ciprofloxacin, chloramphenicol, erythromycin, clarithromycin, and tetracycline. The MIC of gentamicin was 3.0 µg/ml.
| |
DISCUSSION |
The exact contribution of the Bartonella isolate to
this patient's illness is unclear. He clearly was bacteremic, and he
clearly had very high fever. The infection may have prompted a relapse of the vasculitis and the associated neurologic manifestations of his
ill-defined rheumatologic syndrome. Occupational exposure seems to have
been the likely means of acquiring the infection. There is anecdotal
evidence of an abundance of voles in the locales of Montana in which
this man worked. Ample opportunity probably existed for ectoparasitic
exposure (ticks, fleas, and biting flies), but none was documented.
In a few parts of the United States where rodent populations have been
studied, Bartonella spp. have been found to be prevalent among mice and rats. Kosoy et al. (12) detected
Bartonella in roughly 50% of the rodent populations in the
southeastern United States, and Hofmeister et al. (9)
detected a novel Bartonella species in the blood of mice in
Minnesota and Wisconsin in the course of studies on the reservoirs of
tick-borne pathogens. The new Bartonella species was
detected incidentally, along with Borrelia burgdorferi and
Babesia microti, when PCR primers targeting
Ehrlichia spp. resulted in the amplification of
Bartonella-like 16S ribosomal DNA segments. These findings,
as well as those of this case, suggest that Bartonella spp.
may occasionally be transmitted by ticks. Prior to the current
understanding of the epidemiology of cat scratch disease, Lucey et al.
(14) reported two cases of bacteremia due to B. henselae in immunocompetent men who had sustained tick bites prior
to their illnesses. In addition to the well-documented role of fleas in
the transmission of B. henselae (6) and the classic examples of louse-borne trench fever due to B. quintana and oroya fever due to Bartonella
bacilliformis acquired from sand flies, it is possible that more
than one arthropod vector of Bartonella-associated diseases exists.
The Bartonella strains isolated from mice by Hofmeister et
al. (9) were most closely related to Bartonella
grahamii (2) on the basis of 16S rRNA sequence analysis
and were most closely related to B. vinsonii subsp.
vinsonii on the basis of citrate synthase gene sequence
analysis. Our DNA relatedness studies indicated that mouse isolate 95 0726 14a from the study of Hofmeister et al. and human strain OK 94-513 fulfilled the molecular definition of a species as strains with 70% or
more DNA relatedness (at an optimal reassociation criterion) and a D of
5% or less within related sequences (16). On the basis of
this definition, the human and mouse strains were easily differentiated
from all Bartonella species other than B. vinsonii. The relatedness to B. vinsonii subsp.
vinsonii and B. vinsonii subsp.
berkhoffii was at the species level, except that D was
almost always 5 to 7%. These data left us with the choice of creating
a new species for these strains or creating a third subspecies for them
within B. vinsonii. We chose the second alternative because
of the similarity of relatedness of the new strains to that previously
seen within existing B. vinsonii subspecies (11).
We therefore now describe Bartonella vinsonii subsp.
arupensis subsp. nov.
Description of B. vinsonii subsp. arupensis
subsp. nov.
Bartonella vinsonii subsp. arupensis
(a.rup.en.'sis. N.L. fem.adj. arupensis, from Associated and
Regional University Pathologists, Inc., the laboratory where the type
strain was initially characterized). Exhibits characteristics of the
species B. vinsonii. Grows on heart infusion agar in the
presence of X factor. Catalase, oxidase, and motility negative. Does
not react with monospecific antisera to B. henselae or
B. quintana. Biochemical characteristics that may be used to
distinguish it from other Bartonella spp. are shown in Table
2. Isolated from a human and mice (Peromyscus leucopus). Presumptively pathogenic for humans.
The type strain is OK 94-513 (= ATCC 700727), isolated from a
62-year-old bacteremic man.
| |
ACKNOWLEDGMENTS |
The details for the case report were kindly furnished by William
T. Close. The technologist responsible for the initial characterization of the isolate and whose curiosity led to conclusive findings is Ann Croft.
| |
FOOTNOTES |
*
Corresponding author. Mailing address: Laboratory
Corporation of America, 7777 Forest Ln., Suite C-350, Dallas, TX 75230. Phone: (972) 566-3268. Fax: (972) 566-6639. E-mail:
da_welchd{at}rodeo.biomed.com.
| |
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Journal of Clinical Microbiology, August 1999, p. 2598-2601, Vol. 37, No. 8
0095-1137/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
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(2006). EFFECT OF EXPERIMENTAL ECTOPARASITE CONTROL ON BARTONELLA INFECTIONS IN WILD RICHARDSON'S GROUND SQUIRRELS. J Wildl Dis
42: 750-758
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Reeves, W. K., Nelder, M. P., Cobb, K. D., Dasch, G. A.
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Maggi, R. G., Breitschwerdt, E. B.
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CASTLE, K. T., KOSOY, M., LERDTHUSNEE, K., PHELAN, L., BAI, Y., GAGE, K. L., LEEPITAKRAT, W., MONKANNA, T., KHLAIMANEE, N., CHANDRANOI, K., JONES, J. W., COLEMAN, R. E.
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Breitschwerdt, E. B., Blann, K. R., Stebbins, M. E., Munana, K. R., Davidson, M. G., Jackson, H. A., Willard, M. D.
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Gilmore, R. D. Jr., Carpio, A. M., Kosoy, M. Y., Gage, K. L.
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Johnson, G., Ayers, M., McClure, S. C. C., Richardson, S. E., Tellier, R.
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Abstract
Introduction
