Am. J. Trop. Med. Hyg., 60(4), 1999, pp.

593–597
Copyright q 1999 by The American Society of Tropical Medicine and Hygiene

BARTONELLA HENSELAE AND BARTONELLA CLARRIDGEIAE INFECTION IN

DOMESTIC CATS FROM THE PHILIPPINES
BRUNO B. CHOMEL, ENRIQUE T. CARLOS, RICKIE W. KASTEN, KAZUHIRO YAMAMOTO, CHAO-CHIN CHANG,
RODHORA S. CARLOS, MARIE V. ABENES, AND CAROLINE M. PAJARES
Department of Population Health and Reproduction, School of Veterinary Medicine, University of California, Davis, California;
Makati Dog and Cat Hospital, Makati City, The Philippines; Carlos Veterinary Clinic, Metro Manila, The Philippines;
Veterinary Biologics Standardization Section, Laboratory Services Division, Bureau of Animal Industry,
Quezon City, The Philippines; Regional Animal Disease Diagnostic Laboratory, Department of Agriculture,
Cebu City, The Philippines

Abstract. One hundred seven domestic cats from The Philippines were serologically tested to establish the prev-
alence of Bartonella infection. A subset of 31 of these cats also had whole blood collected to tentatively isolate
Bartonella strains. Bartonella henselae and B. clarridgeiae were isolated from 19 (61%) of these cats. Bartonella
henselae type I was isolated from 17 (89%) of the 19 culture-positive cats. Six cats (31%) were infected with B.
clarridgeiae, of which four were coinfected with B. henselae. Sixty-eight percent (73 of 107) and 65% (70 of 107)
of the cats had antibodies to B. henselae and B. clarridgeiae, respectively, detected by an immunofluorescence
antibody (IFA) test at a titer $ 1:64. When tested by enzyme immunoassay (EIA), 67 cats (62.6%) had antibodies
to B. henselae and 71 cats (66.4%) had antibodies to B. clarridgeiae. Compared with the IFA test, the B. henselae
EIA had a sensitivity of 90.4% and a specificity of 97%, with positive and negative predictive values of 98.5% and
82.5%, respectively. Similarly, the B. clarridgeiae EIA had a sensitivity of 97% and a specificity of 92% specificity,
with positive and negative predictive values of 95.8% and 94.4%, respectively. The presence of antibodies to Bar-
tonella was strongly associated with flea infestation. Domestic cats represent a large reservoir of Bartonella infection
in the Philippines.

The genus Bartonella is presently composed of 11 species,
of which at least four are known to be human pathogens: B.
bacilliformis, the agent of Carrion’s disease; B. quintana, the
agent of trench fever and bacillary angiomatosis (BA); B.
henselae, the agent of cat scratch disease (CSD) and BA;1
and B. elizabethae, which can cause endocarditis.2 Barton-
ella vinsonii has been recently reported to be the cause of
human endocarditis.3 Bartonella vinsonii var berkhoffii has
been found in a case of canine endocarditis as well.4 The
other species (B. clarridgeiae, B. doshiae, B. grahamii, B.
peromysci, B. talpae, and B. taylorii) have been isolated
from the blood of various mammals but are not known to
induce disease in the infected animal.5,6
Two Bartonella species (B. henselae and B. clarridgeiae)
have been isolated from the blood of domestic cats.6,7 Epi-
demiologic studies7–10 have implicated cats as a major res-
ervoir of B. henselae, and it has been demonstrated that cats
can remain asymptomatic and bacteremic for several months
to several years.9–11 Bartonella henselae DNA has been am-
plified from fleas found on bacteremic cats,9,12 and transmis-
sion of B. henselae by the cat flea Ctenocephalides felis has
been demonstrated.13 Bartonella clarridgeiae was first iso-
lated from the bloodstream of a healthy cat involved in a
human case of CSD caused by B. henselae.14 However, only
serologic evidence of a human case of CSD caused by this
organism has been documented.15
Isolation of B. henselae and/or B. clarridgeiae from do-
mestic cats has been reported from various parts of the
world, including North America, Europe, Japan, and Austra-
lia.7–9, 16–18 However, no information is available for most of
the Pacific Rim countries.
No human case of CSD from The Philippines has been
officially recognized or published in the scientific literature.
However, animal bites and scratches are certainly common
events in this part of the world, where rabies is endemic and
where an estimated 60,000 persons receive rabies postex-
posure treatment (PET) every year, and approximately
280,000 more Filipinos are bitten by dogs under circum-
stances for which PET would strictly be indicated.19 Among
the 9,495 persons seen in 1996 at the Research Institute for
Tropical Medicine in Manila for animal bites, cats accounted
for 3.3% of the exposures (Carlos E, unpublished data). Fur-
thermore, in this tropical setting, ectoparasite infestation, es-
pecially fleas, is common in pets. It was therefore of interest
to establish if the feline reservoir of Bartonella was present
in the Philippines. A serosurvey of domestic cats from the
Philippines, mainly from Metro Manila and suburbs on Lu-
zon Island, and from Cebu City on Cebu Island was con-
ducted in February 1997 to establish the prevalence of Bar-
tonella infection. A subset of 31 of these cats also had whole
blood collected to tentatively isolate Bartonella strains.
MATERIALS AND METHODS
Animals. Serum samples were conveniently collected at
specific veterinary clinics from 107 domestic cats from Met-
ro Manila and suburbs (101 cats) and Cebu City (six cats),
The Philippines. Most cats were healthy animals presented
at the clinics for vaccination or convenience surgery. For 31
of these cats (25 from Metro Manila and suburbs and six
from Cebu City), 1.5 ml of blood was also collected in a
pediatric lysis-centrifugation tube (Isolatory; Wampole Lab-
oratories, Cranbury, NJ). Most of the cats (87%) were from
a domestic breed. Thirteen percent of the cats were pure
breed (nine Persian, four Siamese, and one Tonkinese). Fif-
ty-four percent of the cats were female, with an age range
of two months to 12 years (mean 5 2.5 years, mode 5 2
years). Most of the cats (78%) were pet cats that were adopt-
ed as kittens after being found in the neighborhood, and most
were free to roam from their household. More specifically,
among the 31 cats for which a blood culture was performed,
two were reported as being stray and all other were reported

593
594 CHOMEL AND OTHERS
as pets found in the neighborhood. Flea infestation was com-
mon since 54% (58 of 107) of the cats were harboring fleas
when examined at time of blood collection. For the 101 cats
from Metro Manila, 35 were from Manila, 32 from Makati,
15 from Malabon, 11 from Parañaque, and eight from Que-
zon City. All cats from Makati were owned cats that were
individually identified with a name.
Isolation of Bartonella from cat blood. The isolator
tubes were centrifuged at 1,800 3 g for 75 min at ambient
temperature and the supernatant was removed. The pellet
was then resuspended in 125 ml of inoculation media20 and
the volume was recorded. Two hundred fifty microliters of
the suspension were inoculated onto heart infusion agar (Dif-
co Laboratories, Detroit, MI) supplemented with 5% defi-
brinized rabbit blood and the remaining suspension was in-
oculated onto a second plate. The plates were incubated for
one month at 358C in 5% CO2 in a humid incubator and
checked regularly for bacterial growth. After gram stain and
microscopic examination, colonies of different morphologies
were subcultured, harvested, and frozen at 2708C in 100%
fetal calf serum. Serum tubes were centrifuged at 500 3 g
before removing and freezing the serum at 2208C.
Identification of isolates. Cat blood isolates were iden-
tified using polymerase chain reaction/restriction fragment
length polymorphism analysis (PCR-RFLP) of a fragment of
the citrate synthase gene9, 21 and a fragment of the 16S rRNA
gene.22,23
An approximately 400-basepair (bp) fragment of the cit-
rate synthase gene was amplified using previously described
primers and methods.21 The amplified products were verified
by gel electrophoresis and then enzymatically digested using
Taq I and Hha I restriction endonucleases.8 Banding patterns
were compared with type strains of B. henselae Houston-1
(ATCC 49882; American Type Culture Collection, Rock-
ville, MD) and B. clarridgeiae (ATCC 51734).
An approximately 1,500-bp fragment of the 16S rRNA
gene was amplified using previously described primers and
methods.24 The amplified products were verified by gel elec-
trophoresis and then enzymatically digested using Dde I re-
striction endonuclease to determine the B. henselae type
(type I or type II) (Kasten RW and others, unpublished data).
Serologic analysis. Immunofluorescence antibody (IFA)
test. Antibody titers against B. henselae type II and B. clar-
ridgeiae were determined using both an IFA technique as
previously described,8 and an enzyme immunoassay (EIA)
using the outer membrane proteins (OMPs) of B. henselae
and B. clarridgeiae. For the IFA test, serum was serially
diluted in phosphate-buffered saline (PBS) and incubated on
slides containing Felis catus whole fetus cells infected with
B. henselae type II (strain U4, University of California, Da-
vis) and B. clarridgeiae (ATCC 51734). The slides were
washed and probed with fluorescein isothiocyanate goat anti-
cat IgG (heavy plus light chain) conjugate (Cappel, Organon
Teknika Corp., Durham, NC), and the fluorescence was grad-
ed independently by the same two persons. Any serum with
a titer $ 64 was considered positive.8
Enzyme immunoassay (EIA). Purification of the OMPs
of Bartonella. The OMPs of two Bartonella strains (B. hen-
selae and B. clarridgeiae) were prepared as previously de-
scribed.25 Each Bartonella strain was grown on 5% rabbit
blood agar in 5% CO2 at 358C for 3–4 days. Each Bartonella
strain was harvested from 50 plates and washed by centri-
fugation three times (5 min each) in sterile PBS, pH 7.4. The
pellet was resuspended in 10 mM HEPES, pH 7.4 (Gibco
BRL, Life Technologies Inc.,y Gaithersburg, MD) buffer
solution. The whole cell bacterium suspension was then son-
icated for 1 min five times with a 1-min pause between each
sonication with a Sonifer-2 Cell Distributors (Baxter Diag-
nostics Inc., McGaw Park, IL) at 48C. The sonicated organ-
isms were then centrifuged at 1,700 3 g (4,000 rpm in an
SS-4 superspeed centrifuge; Sorvall, Newtown, CT) for 20
min to eliminate the coarse debris pellet. The supernatant
was then centrifuged by ultracentrifugation at 100,000 3 g
(32,700 rpm in a type 70-Ti rotor; Beckman, Palo Alto, CA)
for 60 min at 48C. The pellet was resuspended in 10 mM
HEPES buffer, pH 7.4, containing 1% sodium lauryl sarco-
sine (Sigma Chemical Co., St. Louis, MO) and incubated for
30 min at room temperature. The ultracentrifugation process
was then repeated three times. Finally, the pellet was resus-
pended in distilled water. The protein concentrations of the
final suspension were determined by a colorimetric tech-
nique using the Bio-Rad (Hercules, CA) protein assay kit.
The OMPs were then stored at 2208C until used as an an-
tigen for the EIA.
Enzyme immunoassay. Bartonella henselae and B. clar-
ridge OMPs used as antigens for the EIA were diluted in
0.1M sodium carbonate buffer, pH 9.6, to a protein concen-
tration of 3.0 mg/ml. The EIA microtiter plates (Immulont
I; Dynatech Laboratories, Chantilly, VA) were coated with
100 ml of B. henselae or B. clarridgeiae OMP antigens on
half of the plates. After overnight incubation at room tem-
perature, the plates were washed five times with saline con-
taining 0.05% Tween 20 (Sigma Chemical Co.) and then
blocked with 250 ml of Super Blocky (Pierce, Rockford, IL)
for 1 hr at 378C. Serum samples (50 ml) to be tested and
positive (IFA test titer $ 1:1,024) and negative (specific
pathogen-free cat serum) control sera diluted at 1:100 in EIA
dilution buffer (0.15 M NaCl, 1 mM EDTA [Fisher Scien-
tific, Fair Lawn, NJ], pH 7.4, 50 mM Tris, 0.05% Tween 20,
5% skim milk [Becton Dickinson, Cockeysville, MD], and
0.1% bovine serum albumin [Sigma Chemical Co.]) were
then added in duplicate in both antigen-coated and noncoat-
ed test wells and incubated at 378C for 1 hr. The plates were
then washed five times with the same wash buffer and anti-
cat IgG (heavy plus light chain) peroxidase-labeled conju-
gate (Kirkegaard and Perry Laboratories, Gaithersburg, MD)
at a 1:3,000 dilution was added to all wells and incubated
for 1 hr at 378C. The plates were then washed five with the
wash buffer and 100 ml per well of the substrate solution
(0.005% 3,39,5,59-tetramethyl benzidine [Sigma Chemical
Co.] and 0.015% H2O2 diluted in 0.05 M citric acid, pH 4)
was added. Color development was allowed to proceed for
5–10 min at room temperature before being stopped by the
addition of 50 ml/well of 1 N H2SO4. The optical density
(OD) of each well was read with dual filters (450 nm and
570 nm) using a microplate reader (Dynatech MR 5000; Dy-
natech Laboratories). The final OD value for each sample
was determined as the average value of the antigen-coated
well OD minus the noncoated well OD. Any serum sample
with an OD $ 0.3 was considered positive (based on the
mean plus three standard deviations of serum samples [n 5
47] with negative results in the IFA test).
 BARTONELLA INFECTION IN DOMESTIC CATS FROM THE PHILIPPINES
TABLE 1
Immunofluorescence antibody titers of 107 Filipino cats for Barton-
ella henselae and B. clarridgeiae
B. henselae B. clarridgeiae
Titer No. (%) No. (%)
0 32 (30) 32 (30)
32 2 (2) 5 (5)
64 27 (25) 38 (35.5)
128 22 (20) 24 (22)
256 17 (16) 8 (7.5)
512 5 (5) 0 (0)
1,024 2 (2) 0 (0)
RESULTS
Bartonella henselae and Bartonella clarridgeiae were iso-
lated from 19 (61%) of the 31 cats tested. However, for one
of the cats, bacterial contamination did not allow identifi-
cation of Bartonella infection. Bartonella henselae was iso-
lated from 17 (89%) of the 19 culture-positive cats. All B.
henselae-bacteremic cats were infected with B. henselae
type I. Six cats (31%) were infected with B. clarridgeiae, of
which four where coinfected with B. henselae. Coinfection
was therefore observed in 21% of the bacteremic cats.
Only one of the 31 cats that had a blood culture obtained
was free of fleas at the time of blood collection. All bacter-
emic cats were flea-infested and were outdoor cats.
Sixty-eight percent (73 of 107) and 65% (70 of 107) of
the cats had antibodies to B. henselae and B. clarridgeiae,
respectively, detected by the IFA test at a titer $ 1:64. Sixty-
two cats had antibodies against both organisms, 11 cats were
B. henselae antibody positive and B. clarridgeiae antibody
negative, whereas, eight cats had antibodies only against B.
clarridgeiae. The IFA test antibody titers against B. clar-
ridgeiae were lower than those for B. henselae since as none
had a titer . 1:256 (Table 1). When tested by EIA, 67 cats
(62.6%) had antibodies to B. henselae and 71 cats (66.4%)
had antibodies to B. clarridgeiae. Fifty-seven cats were pos-
itive for both species, 10 cats were positive only for B. hen-
selae, and 14 cats were positive only for B. clarridgeiae.
The OMP EIA for B. henselae antibody performed well
compared with the IFA test since it had an agreement of
93.4%, a sensitivity of 90.4%, and a specificity of 97%. The
positive predictive value was 98.5% and the negative pre-
dictive value was 82.5%. Similarly, when compared with the
IFA test, the B. clarridgeiae EIA had an agreement of
92.5%, a sensitivity of 97%, and a specificity of 92%. The
positive and negative predictive values were 95.8% and
94.4%, respectively.
The prevalence of antibodies to B. henselae and B. clar-
ridgeiae increased with age and ranged from 48% to 52%
in cats , 1 year of age, from 67% to 78% in one-year-old
cats, from 73% to 80% in young adults (2–3 years old), and
then moderately decreased (from 62% to 69%) in cats great-
er than or equal to four years of age (Table 2).
The presence of antibodies to Bartonella detected by the
IFA test was strongly associated with flea infestation, breed
of cat, and city of origin (Table 3). Domestic cats were more
likely than pure breed cats to be seropositive and cats from
Makati, a wealthy district of Metro Manila, were less likely
than the cats from other cities to be seropositive. Similar
595
TABLE 2
Prevalence of antibodies to Bartonella henselae and B. clarridgeiae
by age for 107 Filipino cats*
B. henselae B. clarridgeiae
IFA EIA IFA EIA
Age
(years) N No. (%) No. (%) No. (%) No. (%)
0 29 15 (52) 14 (48) 15 (52) 15 (52)
1 9 7 (78) 7 (78) 6 (67) 6 (67)
2–3 30 24 (80) 22 (73) 24 (80) 23 (77)
$4 39 27 (69) 24 (62) 25 (64) 27 (69)
* IFA 5 immunofluorescence antibody; EIA 5 enzyme immunoassay.
results were observed for antibodies detected by the EIA.
However, when statistically controlled for the presence of
fleas, breed of cat and city of origin were no longer signif-
icant risk factors.
DISCUSSION
This is the first report of isolation of the agent of CSD
and bacillary angiomatosis from its animal reservoir in the
Philippines. A high percentage of the cats analyzed by blood
cultures were bacteremic, which may be explained by the
fact that all but one of the cats that had a blood culture
obtained were flea-infested. A positive association between
both seropositivity and bacteremia and flea infestation has
been previously reported.8,9,26 Furthermore, experimental
transmission of B. henselae by the cat flea has been dem-
onstrated.13 It is the first time that flea infestation was found
to be associated with seropositivity for B. clarridgeiae, sug-
gesting a similar mode of transmission from cat to cat. The
percentage of bacteremic cats harboring B. clarridgeiae is
very similar to what has been observed in France by Heller
and others27 or in The Netherlands by Bergmans and others.28
It is much higher that the 10% (7 of 70) reported in the
United States29 or the lack of isolation of B. clarridgeiae in
Japanese cats, despite the isolation of many B. henselae
strains (Maruyama S, unpublished data). We found several
cats coinfected with the two feline Bartonella species, con-
firming that coinfection occurs also in The Philippines, as
previously demonstrated in Dutch28 and French cats.24 How-
ever, the most striking finding was the absence of any B.
henselae type II isolates, whereas it is the most common
isolate from European cats,24,27,28,30 and is also common in
the United States (Chomel BB, unpublished data). Distri-
bution of the various species and types of Bartonella isolated
from cats appears to vary widely. Knowledge of the respec-
tive distribution of these types or species is of major impor-
tance since it appears that humans may be more likely to be
infected by one type or species than another, as shown by
Bergmans and others in The Netherlands.31 Such observa-
tions still need to be validated with human isolates from
other parts of the world. Similarly, if a vaccine strategy is
to be developed in domestic cats to prevent human infection,
it appears essential to adapt the composition of the vaccines
to the local strain characteristics. It has been recently shown
that under experimental conditions, there is very limited
cross-protection against reinfection in cats infected by het-
erologous types or species.32
Several studies have determined the sensitivity and spec-
596 CHOMEL AND OTHERS

TABLE 3
Risk factors associated with Bartonella immunofluorescence antibody (IFA) seropositivity in 107 Filipino cats

B. henselae IFA1 B. henselae IFA2

Risk factors Odds ratio 95% CI*

Fleas Flea 1 Flea 2 Flea 1 Flea 2

52 21 6 28 11.56 3.86, 38.24
B. clarridgeiae IFA1 B. clarridgeiae IFA2

Flea 1 Flea 2 Flea 1 Flea 2

46 24 12 25 3.99 1.59, 10.25
B. henselae IFA1 B. henselae IFA2
Odds ratio 95% CI*

Breed Domestic Pure breed Domestic Pure breed

68 5 25 9 4.9 1.32, 20.14
B. clarridgeiae IFA1 B. clarridgeiae IFA2

Domestic Pure breed Domestic Pure breed

66 4 27 10 6.11 1.56, 28.51
B. henselae IFA1 B. henselae IFA2
Odds ratio 95% CI*

City Makati Other Makati Other

11 62 21 13 0.11 0.04, 0.31
B. clarridgeiae IFA1 B. clarridgeiae IFA2

Makati Other Makati Other

12 58 20 17 0.18 0.06, 0.47
* CI 5 confidence interval.

ificity of Bartonella EIA tests compared with IFA tests in
clinical cases in humans.33,34 Monitoring of feline Bartonella
infections have been recently done by EIAs,35 but no eval-
uation of their sensitivity and specificity has been conducted
in naturally infected cats. Our data indicate a strong agree-
ment between the IFA and OMP-EIA in detecting IgG an-
tibodies to B. henselae and B. clarridgeiae in domestic cats,
and the titers were in the same ranges as those reported by
Litwin and others34 in humans. Based on these results, the
EIA could easily be substituted for the more cumbersome
and expensive IFA test, which is subject to reader bias and
is often limited by the quality of the antigen preparations.
The prevalence of antibody to Bartonella was much high-
er than in most previous studies.8,36 It increased with age for
the few first years of life, and then declined for cats $ four
years old. The high percentage of cats either seropositive
and/or bacteremic indicates a large animal reservoir from
which the human population is at risk for exposure. It is
surprising that no clinical case of CSD has ever been re-
ported in The Philippines since it may be a rather common
but under-diagnosed condition. An epidemiologic study in
humans, particularly in Filipino children, seems warranted
to establish the public health importance of this infection.
Acknowledgments: We thank J. N. Hufano (Makati Dog and Cat
Hospital, Metro Manila) for collecting the cat blood samples and
Dr. R. de la Pena, Dr. A. Gonzales, and J. Vargas (Veterinary Bio-
logics Standardization Section, Laboratory Services Division, Bu-
reau of Animal Industry, Quezon City) for technical assistance.
Authors’ addresses: Bruno B. Chomel, Rickie W. Kasten, Kazuhiro
Yamamoto, and Chao-chin Chang, Department of Population Health
and Reproduction, School of Veterinary Medicine, University of
California, Davis, CA 95616. Enrique T. Carlos, Makati Dog and
Cat Hospital, Gen. Luna cor. Algier Street Poblacion, Makati City
1210, Philippines. Rodhora S. Carlos, Carlos Veterinary Clinic, Su-
cat, Parañaque 1700, Metro Manila, The Philippines. Marie V. Abe-
nes, Veterinary Biologics Standardization Section, Laboratory Ser-
vices Division, Bureau of Animal Industry, Visayas Avenue, Dili-
man, Quezon City, The Philippines. Caroline M. Pajares, Regional
Animal Disease Diagnostic Laboratory, Department of Agriculture,
RFU VII, M. Velez Street, 6000 Cebu City, Philippines.
Reprint requests: Bruno B. Chomel, Department of Population
Health and Reproduction, School of Veterinary Medicine, University
of California, Davis, CA 95616.
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