Rev. sci. tech. Off. int. Epiz.

, 2000,19 (1), 136-150

Cat-scratch disease
B.B. Chomel
Department of Population Health and Reproduction, School of Veterinary Medicine, University of California,
Davis, CA 95616, United States of America

This document is an update of a paper entitled 'Cat-scratch disease and bacillary angiomatosis', published In
Rev. sci tech. Off. int. Epiz., 1996,15 (3), 1061-1073.

Summary
Cat-scratch disease (CSD) w a s first described by Debré in 1950, y e t t h e causative
bacterial agent of CSD remained obscure until 1992, w h e n Bartonella (formerly
Rochaiimaea) henselae w a s implicated in CSD by serological and microbiologic
studies. Bartonella henselae had initially been linked to bacillary angiomatosis
(BA), a vascular proliferative disease most commonly associated with
long-standing human immunodeficiency virus infection or other significant
immunosuppression. Bartonella henselae has also been associated with bacillary
peliosis, relapsing bacteraemia and endocarditis in humans. Cats are healthy
carriers of B. henselae, and can be bacteraemic for months or years. Cat-to-cat
transmission of the organism by the cat flea, with no direct contact transmission,
has been demonstrated. Two n e w Bartonella species have been identified in the
cat reservoir, namely: B. clarridgeiae and B. koehlerae. The role of these species
in the aetiology of CSD still needs to be confirmed by isolation or DNA
identification from lesions in humans. The author discusses the present state of
knowledge on the aetiology, clinical features and epidemiological characteristics
of CSD/BA, in addition to diagnosis, treatment and prevention.

Keywords
Bacillary angiomatosis - Bartonella clarridgeiae - Bartonella henselae - Cats -
Cat-scratch disease - Zoonoses.

angiomatosis (BA), is associated with CSD (43, 5 4 , 1 1 6 , 118,

Introduction 119, 130, 1 3 1 , 140). Bacillary angiomatosis is a vascular
proliferative disease mainly s e e n in p e o p l e infected with
Cat-scratch disease (CSD) h a s b e e n clinically identified in
h u m a n immunodeficiency virus (HIV) (119).
h u m a n s since the 1930s, b u t was first described as a clinical
entity in 1950 b y Debré et al. (40). T h e disease is typically a
benign, subacute regional l y m p h a d e n o p a t h y resulting from
dermal inoculation of the causative agent (25). One of the
c o m m o n atypical forms of CSD is the Parinaud's
oculoglandular s y n d r o m e (25). Several other clinical
manifestations h a v e b e e n reported in i m m u n o c o m p r o m i s e d T h e cause of CSD h a s long b e e n in question. Initially it was
patients, s u c h as bacteraemia (130), peliosis hepatis ( 1 3 1 , considered to b e a possible virus, t h e n a Gram-negative
140), altered mental status (55) or dementia (129). In bacterium. However, it is only in recent years that a specific
i m m u n o c o m p e t e n t individuals, the clinical spectrum of organism h a s b e e n identified. In 1 9 8 3 , a small bacillus was
B. henselae infection h a s widely e x p a n d e d to include identified b y Warthin-Starry silver deposition stain o n l y m p h
endocarditis (70), neuroretinitis, aseptic meningitis ( 2 6 , 1 4 2 ) , n o d e biopsies of thirty-nine patients with CSD (139). In 1988,
hepatic and splenic abscesses, p n e u m o n i a and pleural a p l e o m o r p h i c , Gram-negative bacterium was isolated from
effusion, musculoskeletal manifestations, osteomyelitis, and the l y m p h n o d e of a CSD patient at the A r m e d Forces Institute
paravertebral abscesses (7). Recent evidence demonstrated of Pathology in the United States of America (USA) (48).
that Bartonella (formerly Rochaiimaea) henselae (23), a Afipia felis was then considered as the most p r o b a b l e agent of
bacterium that h a s b e e n isolated from patients with bacillary CSD. Recently, a report implicated B. henselae and A. felis,
Rev. sci. tech. Off. int Epiz., 19 (1) 137

based o n polymerase chain reaction (PCR) testing (2). A case control study to determine the risk factors associated
Isolation of A. felis was difficult and a very limited n u m b e r of with developing BA revealed that the only statistically
strains w e r e isolated in only two laboratories. T h e serology of significant risk factor w a s traumatic contact with a cat
the bacterium was not highly specific and was difficult to (scratches or bites) (134). After this study, K o e h l e r et al.
standardise. Isolation of A. felis was recently reported from a identified BA patients w h o h a d cats, and p e r f o r m e d b l o o d
patient with CSD (57), h o w e v e r , PCR testing of thirty-two cultures o n these animals (82). All seven cats o w n e d b y the
l y m p h n o d e s p e c i m e n s from CSD patients gave n o positive four patients w e r e bacteraemic with B. henselae. Furthermore,
results for A. felis, w h e r e a s all samples w e r e positive for 4 1 % of the pet cats and i m p o u n d e d cats that w e r e tested i n
B. henselae. Afipia felis was c o n c l u d e d to b e only a rare cause the San Francisco Bay area w e r e also bacteraemic. Since then,
of CSD (57). Strong evidence demonstrates that A. felis is an the d o m e s t i c cat h a s b e e n s h o w n to b e the m a i n reservoir of
environment bacterium that lives in water. It is suggested that B. henselae. K o e h l e r et al. also demonstrated that peliosis
previous isolations of A. felis from l y m p h n o d e s could b e d u e hepatis and B. henselae infection w e r e strongly associated,
to water contamination through ineffectively sterilised fluids w h e r e a s subcutaneous and lytic b o n e lesions w e r e m o r e
used for culture (94). frequently o b s e r v e d i n BA cases caused b y B. quintana (83).

In a few instances, suspected cases of CSD w e r e attributed to

The identification of B. henselae as the agent of CSD was an
B. clarridgeiae, b a s e d o n serological evidence (88, 103).
indirect result of the e p i d e m i c of acquired i m m u n e deficiency
However, B. clarridgeiae isolates or DNA h a v e not yet b e e n
syndrome (AIDS). A n e w disease k n o w n as bacillary
identified from suspect cases of CSD. Bartonella clarridgeiae
angiomatosis (BA), a type of vascular proliferative lesion in h a s b e e n isolated from domestic cats (36, 9 6 ) , w h i c h
i m m u n o c o m p r o m i s e d hosts (81), was d e s c r i b e d in constitute the m a i n reservoir of the bacterium in the USA (36,
HIV-infected patients b e t w e e n 1983 and 1988 (79, 80, 97, 89), E u r o p e (15, 65, 6 7 ) , Indonesia (104) and the Philippines
132). T h e disease was attributed to a n e w Gram-negative (34). T o date, B. koehlerae has only b e e n isolated from two
bacillus, w h i c h was subsequently n a m e d Rochaiimaea cats in the San Francisco area and has n o t yet b e e n l i n k e d to
henselae (116, 1 2 1 , 140). An indirect immunofluorescence any h u m a n case of CSD (45). T h e citrate synthase g e n e
antibody test (IFA) was d e v e l o p e d in 1 9 9 2 , at the Centers for s e q u e n c e of a fourth Bartonella species, B. weissi, isolated from
Disease Control and Prevention, to detect antibodies to this domestic cats, was p u b l i s h e d b y Marano et al. in GenBank in
organism (118). Using this test, it was n o t e d that 8 8 % of sera 1998 (100).
samples from suspected CSD patients h a d antibodies to
B. henselae, c o m p a r e d to only 3 % of control patient sera T h e genus Bartonella includes the former Rochaiimaea (25)
(118). Bartonella henselae was first isolated directly from the and Grahamella (18) genera. T h e spectrum of Bartonella
cutaneous lesions of HTV-infected patients with BA i n 1991 species that are h u m a n pathogens is still expanding. T h e
(80), and thus this organism has b e e n directly cultured from isolation of Bartonella elizabeihae from a h u m a n case of
the lesions of b o t h BA and CSD. Bacillary angiomatosis is also endocarditis (39) suggested a possible rodent reservoir,
caused b y B. quintana, the agent of trench fever (80). mainly of the genus Rattus (47). Similarly, the report of the
However, B. quintana has never b e e n directly associated with isolation of B. vinsonii subsp. arupensis from a cattle rancher
a case of CSD. Cases of BA caused b y B. quintana usually suggests transmission to h u m a n s b y ticks from a p r o b a b l e
occur in h o m e l e s s p e o p l e with a history of l o w i n c o m e and rodent reservoir (141).
alcoholism and are usually associated with exposure to lice,
not cats (83). However, two B. quintana isolates w e r e obtained
in France from two patients with chronic l y m p h a d e n o p a t h y Epidemiology and biology of the
w h o h a d contact with cats and cat fleas (95).
infection
It was only in the early 1990s that evidence clearly indicated Humans
that B. henselae was m o r e likely to b e the agent of CSD than Limited data are available regarding the prevalence or
A. felis. Bartonella are morphologically very similar to A. felis incidence of CSD world-wide. However, several reports o n
w h e n e x a m i n e d b y Warthin-Starry staining, w h i c h m a y seroprevalence of Bartonella antibodies h a v e b e e n published,
explain the previous confusion. Serological studies and mainly from western Europe (Netherlands, Germany, France,
isolation of the organism from the l y m p h n o d e s of p r o b a b l e Italy), and m o r e recently from S w e d e n (69), G r e e c e (75),
CSD cases demonstrated the major role played b y B. henselae J a p a n (144) and Australia (50). According to J a c k s o n et al, an
in the aetiology of CSD (6, 9, 3 8 , 42, 4 3 , 109, 118, 133, 145). estimated 22,000 to 24,000 h u m a n cases of CSD occurred in
Furthermore, amplification of an antigen gene of B. henselae the USA in 1992, 2,000 of w h i c h required hospitalisation
by PCR o n CSD skin-test material confirmed the presence of (71). T h e estimated total health cost of CSD was over
B. henselae but not A. felis DNA (4); and in July 1 9 9 2 , US$12 million in 1992. In the Netherlands, the incidence of
B. henselae bacteraemia was reported in a cat with a healthy CSD was estimated to b e 2,000 cases p e r year (15). In
owner (117). Connecticut, w h i c h is the only State in the USA w h e r e CSD is
138 Rev. sci. tech. Off. int. Epiz., 19 (1)

a reportable disease (since January 1992), 2 4 6 p e o p l e m e t the unclear, evidence of endothelial colonisation, involving
case definition during the p e r i o d 1 9 9 2 - 1 9 9 3 . A prospective formation, engulfment and u p t a k e of a large bacterial
population-based surveillance system reported an average aggregate h a s b e e n demonstrated (41).
state-wide annual incidence of 3.7 cases of CSD p e r 100,000
persons (66). A survey of an occupational group potentially at Cats
risk for Bartonella infection found that the overall T h e domestic cat is the m a i n reservoir for the h u m a n
seroprevalence was 7 . 1 % (112). Based o n these estimates, pathogen, B. henselae. Bacteraemia in cats was first reported in
several thousand cases should occur yearly in most countries 1992, in the cat of a healthy owner, b y Regnery et al. (117). In
of Europe, including France and Germany, w h e r e a h i g h northern California, bacteraemia prevalences of 3 9 . 5 %
percentage of cats h a v e b e e n reported to b e infected (32, 67, (81/205) and 4 1 % (25/61) h a v e b e e n reported ( 3 1 , 8 2 ) . Cats
124). b e l o w the age of twelve m o n t h s and i m p o u n d e d cats w e r e
m o r e likely to b e bacteraemic, and flea infestation was also a
Cat-scratch disease occurs in i m m u n o c o m p e t e n t patients of significant risk factor (31). T h e r e was n o direct correlation
all ages, although the majority ( 5 5 % - 8 0 % ) are u n d e r twenty b e t w e e n the level of bacteraemia and the antibody litre;
years of age. In o n e study, J a c k s o n et al. reported a higher h o w e v e r , cats with serological litres of 5 1 2 or greater w e r e
p r o p o r t i o n of cases a m o n g children and teenagers than in m o r e likely to b e bacteraemic than cats with a litre of less than
adults, with 4 5 % to 5 0 % of the patients b e i n g younger than 5 1 2 (31). More recently, B. henselae h a s b e e n isolated from
15 years o l d (71). However, Sander et al. reported a rather domestic cats from m a n y parts of the world, including E u r o p e
h i g h seroprevalence in young adults in Germany (126). (e.g. the Netherlands [15], France [32, 65, 67] and Germany
Cat-scratch disease is considered to b e the m o s t c o m m o n [124]), Asia (including J a p a n [105], Indonesia [104], and the
cause of chronic, benign adenopathy in children and young Philippines [34]), Australia (20), N e w Zealand (74) and Africa
adults; m o r e cases occur in males than females (71). T h e ( Z i m b a b w e [77]). In m o s t of these studies, bacteraemia
incidence of the disease varies b y season, with most cases prevalence ranged from 1 5 % to 5 5 % , d e p e n d i n g o n w h e t h e r
being s e e n in autumn and winter. Seventy-five percent the feline population tested was m a d e u p of p e t cats or stray
(184/246) of the cases in Connecticut h a d d e v e l o p e d cats.
a d e n o p a t h y during the p e r i o d f r o m October to February (66).
In the s a m e study, the age-specific attack rate was highest In Australia, Flexman et al. reported the first isolation of
a m o n g children u n d e r ten years of age (9.3/100,000) and B. henselae from the b l o o d and fleas of a cat belonging to a
decreased with increasing age (66). T h e m e d i a n age of patient with CSD (49). T h e patient d e v e l o p e d fever, lethargy
patients with CSD was fourteen years (range: 1-64 years). and anorexia w h i c h lasted for three days, followed b y the
Eleven percent of patients w e r e hospitalised, but there w e r e appearance of axillary l y m p h a d e n o p a t h y . T h e s e s y m p t o m s
n o deaths. Risk factors highly associated with CSD include arose three w e e k s after the patient h a d r e m o v e d fleas from his
owning a cat of less than 12 m o n t h s of age, b e i n g scratched or cat. There was n o history of a bite or a scratch and n o primary
bitten b y a kitten, or owning a kitten with fleas (145). Several lesion o n the skin. Therefore, this case could also b e o n e of the
studies h a v e b e e n able to directly associate B. henselae first confirmed cases of CSD in h u m a n s transmitted b y fleas.
bacteraemia in cats, especially young kittens, with clinical
cases of CSD in h u m a n s , resulting from scratches inflicted b y In Europe, two different types of B. henselae h a v e b e e n
these animals (30, 4 2 , 85). Most cases of CSD in h u m a n s are identified b y partial sequencing of the 16S ribosomal
thought to result from inoculation of infected flea faeces at the ribonucleic acid (rRNA) gene from cases of CSD in h u m a n s
time of the scratch (51). T w o cases of B. henselae w e r e (13, 14, 4 4 , 128) and from bacteraemic cats (15, 4 4 ) . T h e
reported to b e associated with tick bites (99). serotype 'Marseille' reported in France (44) s e e m s to
correspond to the type II described b y Bergmans et al.
Bacillary angiomatosis caused b y B. henselae h a s b e e n (13, 14, 15; M. Drancourt and D. Raoult, personal
associated mainly with exposure to cats ( 8 2 , 8 3 , 1 3 4 ) . A study communication). In m o s t of western Europe, B. henselae
s h o w e d a strong link b e t w e e n the onset of neuropsychological type II is m o r e c o m m o n l y found in cats than type I (15, 65,
decline or dementia in HIV-infected p e o p l e and s e r u m 67, 124). Conversely, in h u m a n cases of CSD in the
i m m u n o g l o b u l i n M (IgM) antibodies to B. henselae (129). Cat Netherlands (14, 15) and Germany (128), B. henselae type I
ownership was associated with neuropsychological decline was identified m o s t frequently, suggesting that this type m a y
and dementia. T h e p r e s e n c e of B. henselae IgM antibodies was b e m o r e infectious for h u m a n s than type II. Distribution of
also strongly l i n k e d to cat ownership, particularly if the cat B. henselae type I and type II in domestic cats in the USA has
was acquired less than o n e year b e f o r e the measurement of not yet b e e n well d o c u m e n t e d . Bartonella henselae type II
antibody values. I m m u n o s u p p r e s s e d patients h a v e also appears to b e highly prevalent i n northern California, whereas
acquired BA after renal, liver, cardiac or b o n e m a r r o w B. henselae type II and type I are equally distributed in the cat
transplantation (37). Bartonella henselae h a s b e e n s h o w n to population of the East Coast (B.B. C h o m e l , unpublished
colonise vascular tissues and to stimulate vasoproliferative data). In the Philippines, n o n e of the cats tested carried
tumour growth. Although the molecular principle of B. henselae type II, suggesting major regional variations in the
bacterium-induced neovascularisation (angiogenesis) is still
prevalence of B. henselae types (34). Isolation of B. clarridgeiae
Rev. sci. tech. Off. int. Epiz., 19 (1) 139

from d o m e s t i c cats is u n c o m m o n in the USA; K o r d i c k et al. 64). Furthermore, l a c k of cross-protection b e t w e e n Bartonella

reported a prevalence of 10% in seventy Bartonella isolates species or B. henselae types was o b s e r v e d in
(89). In other regions s u c h as E u r o p e (15, 65, 67), the experimentally-infected and heterologously challenged cats
Philippines (34) a n d Indonesia (104), B. clarridgeiae accounts (143).
for u p to 3 6 % of Bartonella isolates.
Transmission from cat to h u m a n is p r e s u m e d to occur
Several serosurveys h a v e also b e e n c o n d u c t e d in cat predominantly b y cat scratch, b u t flea-bite transmission c o u l d
populations in the USA. In North Carolina, 2 1 % of 5 1 8 sick also b e possible. For experimental infection of cats, the
cats w e r e seropositive for B. henselae (21). Childs et al. intradermal and intravenous routes are highly effective ( 1 , 5 1 ,
reported a prevalence of 2 8 . 2 % (370/1,314) from cats in 6 2 , 8 5 , 1 1 3 ) . Experimental infection of o n e - to t w o - w e e k - o l d
various parts of the USA (29), and 14.7% in cats from kittens b y the oral route h a s also b e e n reported (63). In an
Baltimore, Maryland (28). Similarly, a s e r o e p i d e m i o l o g i e arthropod-free environment, neither direct horizontal
survey of cats from all over North America identified an transmission from cat to cat, n o r vertical transmission from
overall prevalence of 2 8 % ( 1 7 5 / 6 2 8 ) , with a l o w range of infected q u e e n s to offspring appear to occur ( 1 , 62). Zangwill
3.7% to 6.7% i n the Midwest and Great Plains region, to an et al. (145) and K o e h l e r et al. (82) suggested that fleas m a y
upper range of 6 0 % in the south-east (72). High play a role i n the transmission of the infection, as p r e s e n c e of
seroprevalence a p p e a r e d to b e correlated with w a r m , h u m i d B. henselae DNA was demonstrated b y PCR in fleas c o m b e d
climates. T h e s e w a r m , h u m i d areas with the largest from bacteraemic cats (82). Higgins et al. demonstrated that
seroprevalence w e r e also those likely to h a v e the largest cat fleas can maintain B. henselae and excrete viable organisms
in their faeces for u p to nine days after feeding o n an infected
n u m b e r of potential a r t h r o p o d vectors, including fleas. In
b l o o d m e a l (68). Cat fleas (Ctenocephalides felis), transferred
Hawaii, of thirty-one kittens involved in h u m a n cases of CSD,
from B. henselae bacteraemic cats to five specific-
twenty-one ( 6 8 % ) h a d positive b l o o d culture and elevated
pathogen-free (SPF) kittens, w e r e c a p a b l e of transmitting the
antibody titres to B. henselae (42). Only o n e (4%) out of
infection to all the SPF kittens (33). In an elegant experiment,
twenty-three adult cats h a d a positive culture, although
Foil et al. w e r e able to infect cats b y intradermal injection of
eighteen (78%) h a d elevated antibody litres. In a cluster of
flea faeces from fleas fed o n bacteraemic cats for four days
CSD e n c e p h a l o p a t h y in south Florida, 2 2 % of the 124 cats
(51).
tested w e r e found to b e bacteraemic, and 6 2 % (77/124) h a d
B. henselae antibodies (111). Bartonella henselae antibody Dogs
prevalence in e l e v e n catteries from all over the USA was
Infection of h u m a n s following contact with d o g s h a s also b e e n
35.8%, with six catteries having a l o w prevalence ( b e t w e e n
reported. In o n e study, 9 5 % of patients h a d a history of
8.3% and 3 7 . 5 % ) and five catteries showing a h i g h prevalence
contact with cats and 4 % h a d a history of contact with d o g s
(above 6 5 % ) (52). Flea infestation was the m o s t important
(102). However, a large-scale study of 1,200 cases reported
risk factor for h i g h B. henselae seroprevalence.
that 99.1 % of patients h a d a history of cat contact and was not
supportive for any other animal source (25). In Hawaii, a very
Information o n the prevalence of B. henselae antibodies in cats limited n u m b e r of seropositive d o g s h a v e b e e n reported, but
from various parts of the w o r l d is also increasing rapidly. n o bacteraemic d o g s (42). A recent report from J a p a n of a
Bartonella henselae antibodies h a v e b e e n found i n d o m e s t i c possible case of CSD caused b y contact with a d o g suggests
cats in m o s t countries of Europe, in addition to Israel (40%) that d o g s c o u l d play a role in h u m a n B. henselae infection
(8), Egypt ( 1 1 % ) (29), southern Africa (South Africa [21%] (136). However, s u c h conclusions n e e d further confirmation.
and Z i m b a b w e [23%]) (76), J a p a n (15%) ( 1 3 7 ) , and
Singapore (47.5%) (110).

W h e n experimentally infected, kittens d e v e l o p a h i g h

Clinical signs
6
bacteraemia (up to 1 0 c o l o n y forming units p e r ml) within Humans
two to three w e e k s and usually clear their infection within two One to three w e e k s elapse b e t w e e n the scratch or bite and the
to three m o n t h s ( 3 3 , 59, 6 1 , 1 2 0 ) . In s o m e cases, bacteraemia appearance of clinical signs ( 5 6 , 1 0 2 ) . B e t w e e n 6 0 % and 9 3 %
can last for several m o n t h s and relapses of bacteraemia at of patients with CSD d e v e l o p a small skin lesion (3 m m to
levels m u c h l o w e r than during the initial infection can b e 5 m m ) , often resembling an insect bite, at the inoculation site
observed ( 1 , 5 3 , 6 1 , 87, 90, 9 1 ) . Cyclical bacteraemia was (usually the h a n d or forearm). This lesion appears three to ten
demonstrated, with the level of bacteraemia fluctuating b y as days after the scratch o r bite. T h e cutaneous lesion evolves
m u c h as 100-fold, and intermittent negative cultures. This from a vesicle to a pustule, and finally to a papule, or m o r e
suggests that a p r o p o r t i o n of infected cats m a y carry the frequently from a macule to a p a p u l e (102). T h e lesions
infection for years. Long-lasting bacteraemia in cats was resolve within a few days to several w e e k s . Inoculation lesions
suggested b y K o e h l e r et al. (82) a n d was well demonstrated are nonpruritic and heal without scar formation.
by K o r d i c k et al. (85, 90, 9 1 ) . Co-infection of cats w i t h Lymphadenitis is generally unilateral and c o m m o n l y appears
B. henselae and B. clarridgeiae strains h a s b e e n reported (15, i n the epitrochlear, axillary or cervical l y m p h n o d e s (25). In
 140 Rev. sci. tech. Off. int. Epiz., 19 (1)

the study in Connecticut, it was found that younger CSD In experimentally infected cats, s o m e research groups found
patients (less than 15 years old) w e r e m o r e likely to present n o clinical signs ( 1 , 120), w h e r e a s others reported fever,
with cervical a d e n o p a t h y (66). Older patients (15 years old, m o d e r a t e neurological s y m p t o m s and l y m p h a d e n o p a t h y .
or m o r e ) w e r e m o r e likely to present with inguinal K o r d i c k and Breitschwerdt reported self-limiting febrile
adenopathy and axillary adenopathy. T h e l y m p h a d e n o p a t h y illness of 4 8 h to 7 2 h duration in six of eight cats, m o d e r a t e
develops approximately three w e e k s after exposure. Swelling l y m p h a d e n o p a t h y i n all eight cats and transient neurologic
of the l y m p h n o d e is usually painful and persists for several dysfunction in two cats after experimental infection with
w e e k s to several m o n t h s . In 15% of the cases, suppuration B. henselae b y b l o o d transfusion (87). Guptill et al. (61) also
occurs (102). Approximately half of patients s h o w signs of reported m i l d clinical signs, w h i c h included m i l d fever and
systemic infection, including fever, chills, malaise, anorexia anorexia in experimentally infected cats. More recently,
and h e a d a c h e s . Less often, sore throat, rashes, conjunctivitis O'Reilly et al. (113) reported fever, lethargia, anorexia and
or e v e n arthralgia h a v e b e e n reported. In general, the disease cutaneous lesions at the inoculation site associated with
is benign and heals spontaneously without sequelae. l y m p h a d e n o p a t h y . A similar observation w a s m a d e recently
in a group of six cats experimentally-inoculated with a feline
Atypical s y m p t o m s of CSD occur in 5% to 2 5 % of cases. T h e B. henselae type I isolate, suggesting variability i n the
m o s t c o m m o n of these is Parinauds oculoglandular pathogenicity of Bartonella strains (B.B. C h o m e l , unpublished
s y n d r o m e (periauricular l y m p h a d e n o p a t h y and palpebral data). A statistical association b e t w e e n presence of B. henselae
conjunctivitis), but tonsillitis, myelitis, meningitis, antibodies and stomatitis and k i d n e y and urinary tract
encephalitis, status epilepticus, osteolytic lesions and infections was o b s e r v e d in a large serosurvey of cats in
thrombocytopenic purpura m a y also occur. Encephalopathy Switzerland ( 5 8 ) . U e n o et al. also reported a n association
is o n e of the m o s t serious complications of CSD, usually b e t w e e n B. henselae seropositivity and gingivitis and
occurring two to six w e e k s after the onset of l y m p h a d e n o p a t h y (138). Reproductive disorders (lack of
lymphadenopathy. However, patients usually m a k e c o m p l e t e pregnancy or pregnancy only after repeated breedings) h a v e
recovery with a few or n o sequelae. A cluster of five cases of b e e n o b s e r v e d in experimentally-infected q u e e n s (62).
children with acute encephalopathy associated with CSD was Similar reproductive disorders w e r e e x p e r i e n c e d during a trial
reported in south Florida (111). Bartonella henselae infection o n experimental transmission b e t w e e n a bacteraemic q u e e n
i n i m m u n o c o m p e t e n t p e o p l e h a s b e e n associated w i t h n e w and a non-bacteraemic m a l e (1); stillbirth was o b s e r v e d
clinical presentations, s u c h as neuroretinitis and bacteraemia a m o n g the kittens b o m of bacteraemic queens.
as a cause of chronic fatigue s y n d r o m e (142), as well as a case
of aggressive B. henselae endocarditis in a cat o w n e r (70). Cat-scratch disease infection is very c o m m o n in cats,
Cases of pleural effusion, p n e u m o n i a , and granulomatous especially i n y o u n g kittens. Bacteraemia usually lasts from a
hepatitis and splenitis h a v e also b e e n reported (10). One case few w e e k s to a f e w m o n t h s . T h e organisms h a v e b e e n
of paronychia was associated with a B. henselae infection in a reported to b e intra-erythrocytic (84) and pili m a y b e a
w o m a n bitten b y a cat (125). pathogenic determinant for Bartonella species (12).

In i m m u n o c o m p r o m i s e d p e o p l e , the symptomatology of BA Dogs

is rather different. Also called epithelioid angiomatosis, BA is a A survey c o n d u c t e d in Hawaii s h o w e d that n o n e of the d o g s
vascular proliferative disease of the skin, characterised b y tested w e r e B. henselae bacteraemic, a n d a very small
multiple, blood-filled, cystic n o d u l e s . Infection is usually percentage 6.4% (2 out of 3 1 dogs) h a d seroconverted (42).
characterised b y violet-coloured or colourless papular and Experimental inoculation of B. henselae b y the intra-dermal
nodular skin lesions that m a y clinically suggest Kaposi's route did not result in a bacteraemic p h a s e , although the d o g s
sarcoma, but histologically resemble epithelioid seroconverted after a few w e e k s (35). Breitschwerdt et al. (22)
h a e m a n g i o m a s ( 1 1 9 ) . W h e n visceral p a r e n c h y m a organs are and K o r d i c k et al. (86) reported the isolation of B. vinsonii
involved, the condition is referred to as bacillary peliosis subsp. berkhoffii in a case of endocarditis in a d o g . An
hepatis, splenic peliosis, or systemic BA. Koehler et al. epidemiological study of 1,920 d o g s f r o m N o r t h Carolina and
demonstrated the strong association b e t w e e n peliosis hepatis Virginia revealed a seroprevalence of 3.6%. Seropositive d o g s
and B. henselae infection (83). Fever, weight loss, malaise and w e r e m o r e likely to b e living in rural areas and h a v e h a d a
enlargement of affected organs m a y d e v e l o p in patients with history of heavy exposure to ticks (114).
disseminated BA.

Cats Diagnosis
No major clinical signs of CSD h a v e b e e n reported in cats Humans
under natural conditions. Suspicions of l y m p h a d e n o p a t h y F o r years, the diagnosis of CSD in h u m a n s w a s b a s e d o n
caused b y a CSD-like organism identified b y silver-stained clinical criteria, exposure to a cat, failure to isolate other
section h a v e b e e n reported (78), and m o r e recently, uveitis bacteria, and/or histological examination of b i o p s i e s of l y m p h
was associated with Bartonella infection (92). n o d e s . A s k i n test was d e v e l o p e d in the 1950s (102).
Rev. sci. tech. Off. int. Epiz., 19 (1) 141

However, the antigen p r e p a r e d from pasteurised exudate analysis using different restriction endonucleases or partial
from l y m p h n o d e s of patients with CSD was not standardised sequencing of the 16S rRNA or citrate syntheses genes (15,
and concerns w e r e raised about the safety of s u c h a product. 3 1 , 8 2 , 8 7 ) . A c o m m e r c i a l PCR test for detecting B. henselae
Since the identification of B. henselae as the m a i n aetiological bacteraemia in cats directly from the b l o o d is n o w available in
agent of CSD, serological tests, s u c h as the IFA ( 3 8 , 1 1 8 , 1 4 6 ) the USA (135).
or the e n z y m e - l i n k e d i m m u n o s o r b e n t assay (ELISA), using
whole b a c t e r i u m (9, 16, 98, 133) or fraction antigen (6), as Serodiagnosis of Bartonella infection in cats b y IFA or ELISA is
well as techniques to isolate the organism from h u m a n and cat of limited interest, as a large percentage of the cat p o p u l a t i o n
specimens h a v e b e e n d e v e l o p e d (82, 116). Because h a r b o u r anti-Bartonella antibodies. However, testing s h o u l d
B. henselae is an intra-erythrocytic bacterium (84), cell lysis b e c o n s i d e r e d b y cat b r e e d e r s to determine the status of
using a lysis centrifugation technique or freezing-thawing, their cat c o l o n y and for cat owners w h o m a y b e
greatly facilitates bacterial isolation from the b l o o d of i m m u n o c o m p r o m i s e d . Tests for antibodies against b o t h
bacteraemic patients. T h e technique is appropriate for B. henselae a n d B. clarridgeiae s h o u l d b e p e r f o r m e d . Further
isolation of B. quintana from BA cases or chronic carriers (95), epidemiological information is required to determine the
however there are still difficulties in isolating B. henselae from prevalence of B. koehlerae a n d the necessity for a systematic
h u m a n patients, including p e o p l e with BA. Isolation of screening against this species. In contrast to the results in
B. henselae from the b l o o d of patients with classical CSD is h u m a n s (44, 115), all the cats that w e r e experimentally-
rarely successful. In s u c h cases, DNA extraction from suspect infected with either B. henselae type I or type II, and that w e r e
l y m p h n o d e s and PCR amplification of the citrate syntheses or tested, w e r e seropositive for b o t h type I a n d type II
16S rRNA genes will allow identification of the organism (5, (K. Y a m a m o t o and B.B. C h o m e l , u n p u b l i s h e d data).
1 7 , 1 9 , 7 3 , 106, 108, 117, 1 2 2 , 123, 127).

Diagnosis of CSD in h u m a n s usually e m p l o y s serological tests Treatment

to detect anti-Bartonella IgM or IgG. G o o d sensitivity and
specificity was reported for B. henselae in suspected cases of Humans
CSD b o t h in the USA and Europe (3, 13, 3 8 , 1 3 3 ) . However, Antimicrobial treatment is indicated for patients with BA,
the correct source of Bartonella antigen must b e u s e d to bacillary peliosis or relapsing bacteraemia. Treatment with
reduce false negative results, as reported with serotype erythromycin (2 g p e r day p e r o s ) , rifampin, or doxycycline
'Marseille' (44), or in a series of s u s p e c t e d CSD cases (46). In for at least six w e e k s , and m o r e likely for t w o to three m o n t h s
terms of specificity, cross-reactions h a v e b e e n o b s e r v e d is r e c o m m e n d e d for i m m u n o c o m p r o m i s e d p e o p l e , but
b e t w e e n B. henselae and Coxiella burnetii (93). It is also relapses can occur (119). In case of peliosis hepatis, treatment
important to n o t e that AIDS patients suffering from BA or b y the parenteral route is initially necessary (81).
peliosis hepatis are often seronegative for Bartonella
antibodies ( 1 1 5 ) . For CSD, antimicrobial treatment is not generally indicated, as
m o s t typical cases d o not r e s p o n d to antimicrobial
Cats administration (101). A retrospective study of 2 0 2 CSD
In cats, w h e r e bacteraemia is c o m m o n , isolation of feline patients demonstrated that the m o s t effective antibiotics w e r e
Bartonella is p e r f o r m e d b y b l o o d culture. A sample of 1.5 m l rifampin, ciprofloxacin, trimethoprim-sulphamethoxazole,
of b l o o d is d r a w n into lysis-centrifugation tubes (82), or and gentamicin, but that a m i n i m u m of four w e e k s of
plastic ethylenediamine tetra-acetic acid (EDTA) tubes. T h e treatment was required (101). More recently, treatment of
tubes are k e p t frozen for a few days to a few w e e k s at - 3 0 ° C , typical CSD patients with oral azithromycin for five days
or preferably at - 7 0 ° C (24). Brenner et al. demonstrated that afforded significant clinical benefit as m e a s u r e d b y total
collection of cat b l o o d in EDTA tubes and subsequent freezing decrease i n l y m p h n o d e v o l u m e within the first m o n t h of
improves the sensitivity of detection of B. henselae (24). T h e treatment ( 1 1 , 27). Intravenous administration of gentamicin
tubes are centrifuged and the pellet spread onto heart infusion and doxycycline and oral administration of erythromycin
agar plates containing 5% fresh rabbit b l o o d . T h e s e plates are h a v e b e e n u s e d successfully i n the treatment of disseminated
maintained at 35°C in a h i g h humidity c h a m b e r with 5% C 0 2 CSD (60, 107). According to W o n g et al, therapy with
for three or four w e e k s . Colonies usually d e v e l o p in a few days doxycycline and rifampin appears to b e helpful in the
from cat b l o o d , although s o m e strains m a y require a few treatment of patients with neuroretinitis (142).
weeks. Isolation of B. clarridgeiae and B. koehlerae is often
fastidious, as these species are m o r e likely to take two w e e k s Cats
or m o r e b e f o r e appearing o n agar plates. Furthermore, Attempts to clear Bartonella bacteraemia in cats using
B. koehlerae requires c h o c o l a t e agar plates, since it d o e s not antibiotics have h a d m i x e d results, m o s t of w h i c h w e r e
replicate o n fresh rabbit b l o o d m e d i u m for primary isolation disappointing. Greene et al. reported that antibiotic treatment
(45). Identification of isolates of B. henselae, B. clarridgeiae or with doxycycline for o n e w e e k was effective in suppressing
B. koehlerae is confirmed b y DNA amplification using PCR- bacteraemia in all eight cats u n d e r study, but was effective in
restriction fragment length p o l y m o r p h i s m (PCR-RFLP) clearing infection from only four cats (59). H o w e v e r , this
142 Rev. sci. tech. Off. int. Epiz., 19 (1)

uncontrolled observation h a s not b e e n corroborated. Regnery is n o correlation b e t w e e n seropositivity and bacteraemia.

et al. reported that antibiotic therapy was incompletely Bacteraemia can also b e transient, with relapses.
efficacious in terminating cat bacteraemia, as tetracycline
h y d r o c h l o r i d e (HCL) and erythromycin d e p r e s s e d B. henselae Declawing cats h a s also b e e n suggested, but this w o u l d h a v e
bacteraemia, but the duration of bacteraemia remained similar limited value, as infection can b e transmitted from cat to cat
to that of untreated cats (120). Furthermore, K o r d i c k et al. b y fleas (30). Therefore, flea control appears to b e o n e of the
tested the efficacy of enrofloxacin and doxycycline for the major control measures n e e d e d to prevent cats from
treatment of B. henselae and B. clarridgeiae infection in cats b e c o m i n g infected and infection b e i n g spread from cat to cat.
(89). Bacteraemia was not eliminated from all the cats treated
and a long treatment was required to eliminate infection. T h e T h e m o s t effective m e a n s of preventing infection b y
authors stated that they would reserve r e c o m m e n d a t i o n for B. henselae are c o m m o n sense, hygiene and, possibly,
treatment to cats o w n e d b y an i m m u n o c o m p r o m i s e d changing the behaviour of cat owners themselves. People
individual or as an alternative to euthanasia of a pet'. should w a s h their h a n d s after handling pets, and clean any
cuts, bites or scratches promptly with soap and water.

Prevention D e v e l o p m e n t of a feline vaccine to prevent the spread of

infection in cat populations and to r e d u c e the risk of infection
Cat ownership h a s b e e n increasing i n m o s t industrialised of h u m a n s , will b e difficult, given the diversity of Bartonella
countries over the 1980s and 1990s, and n o w surpasses d o g species and types h a r b o u r e d b y cats, and the l a c k of
ownership. A large reservoir of B. henselae exists a m o n g the cross-protection b e t w e e n species and types (143).
60 million pet cats residing in one-third of h o m e s in the
USA (56), the 8.4 million pet cats in France, of
w h i c h approximately 1.5 million could b e bacteraemic
Acknowledgements
(B.B. C h o m e l , unpublished data) or the 2 million pet cats in T h e author w o u l d like to thank Drs R.C. Abbott, C.-C. Chang,
the Netherlands, of w h i c h 4 0 0 , 0 0 0 (22%) are estimated to b e T.E. Honadel, R.W. Kasten, Y. Kikuchi and K. Y a m a m o t o ,
bacteraemic (15). As the possibility of B. henselae infection and the several students, especially C. H e w and A. Ziedins,
b e c o m e s m o r e widely recognised, there is likely to b e negative w h o h a v e b e e n working over the last six years to understand
publicity about the perceived hazards of cat ownership, the e p i d e m i o l o g y and pathogenesis of CSD in its feline
especially for i m m u n o c o m p r o m i s e d p e o p l e . However, cats reservoir and of other Bartonella infections in domestic and
can b e very comforting to the chronically and terminally ill. wild m a m m a l s . T h a n k s are also e x t e n d e d to D. W e b e r ,
A. Poland, K. Floyd-Hawkins and to Drs J. F o l e y and
Selecting an appropriate c o m p a n i o n animal is important. N.C. Pedersen from the Center for C o m p a n i o n Animal Health
Seronegative cats are m o r e likely not to b e bacteraemic and to (CCAH), S c h o o l of Veterinary Medicine, University of
b e safe for ownership, h o w e v e r , 2 % of seronegative cats can California, Davis. Research h a s b e e n funded through grants
b e bacteraemic (15, 31). Young kittens, especially i m p o u n d e d from the CCAH, and Mortal Laboratories.
kittens and flea-infested kittens, are m o r e likely to b e
bacteraemic. People w h o o w n kittens are fifteen times m o r e
likely to d e v e l o p CSD than owners of older cats (145).
Therefore, to minimise the risk of infection w h e n acquiring
a pet cat, especially if the prospective owner is
i m m u n o c o m p r o m i s e d , a cat raised in a 'clean', flea-controlled
cattery should b e c h o s e n (52). If possible, the cat s h o u l d b e an
adult and should c o m e from a flea-controlled environment.
Cats could b e serologically tested so that prospective owners
could adopt only a seronegative animal. Unfortunately, there
Rev. sci. tech. Off. int. Epiz., 19(1) 143

Maladie des griffes du chat

B.B. Chomel

Résumé
La maladie des griffes du chat fut décrite cliniquement en 1950 par Debré, mais
son étiologie est restée obscure jusqu'en 1992, date à laquelle les méthodes
sérologiques et la biologie moléculaire ont permis d'incriminer une nouvelle
bactérie, Bartonella (connue auparavant comme Rochaiimaea) henselae, comme
l'agent de la maladie des griffes du chat. Bartonella henselae avait déjà été
reconnue comme l'agent de l'angiomatose bacillaire, une maladie
vasculo-proliférative sévissant principalement chez les sujets infectés par le
virus de l'immunodéficience humaine ou atteints d'autres troubles
immunodéficitaires majeurs. Bartonella henselae est également responsable du
purpura hépatique ainsi que de formes récidivantes de bactériémie et
d'endocardite chez l'homme. Les chats sont porteurs sains de l'agent infectieux et
peuvent présenter une bactériémie pendant des mois, voire des années.
L'infection se transmet de chat à chat sans contact direct, essentiellement par
l'intermédiaire des puces. Deux nouvelles espèces de Bartonella ont été isolées
chez le chat, à savoir B. clarridgeiae et B. koehlerae. Il reste à démontrer, par
isolement ou analyse de l'ADN présent dans les lésions, que ces espèces sont
bien à l'origine de cas humains de maladie des griffes du chat. L'auteur présente
les connaissances actuelles concernant l'étiologie, les manifestations cliniques
et I'épidémiologie de la maladie des griffes du chat et de l'angiomatose bacillaire,
ainsi que sur le diagnostic, le traitement et la prévention de ces maladies.

Mots-clés
Angiomatose bacillaire - Bartonella clarridgeiae - Bartonella henselae - Chats - Maladie
des griffes du chat-Zoonoses.

Fiebre de rasguño del gato

B.B. Chomel

Resumen
La fiebre de rasguño del gato fue descrita por primera vez por Debré en 1950, pero
su agente causal permaneció en la sombra hasta 1992, cuando estudios
serológicos y microbiológicos establecieron un nexo entre la bacteria Bartonella
(anteriormente Rochaiimaea) henselae y esta enfermedad. En un principio,
B. henselae había sido relacionada con la angiomatosis bacilar, una enfermedad
vascular proliferante ligada en general a la infección prolongada por el virus de la
inmunodeficiencia humana u otras importantes inmunosupresiones. Bartonella
henselae también ha sido relacionada con la púrpura hepática, bacteriemia
recurrente y endocarditis en el hombre. El gato es un portador sano de
B. henselae, el cual puede permanecer presente en su sangre durante meses o
años. Bartonella henselae se transmite de gato a gato mediante las pulgas, pero
no por contacto directo. Dos nuevas especies de Bartonella han sido aisladas en
el gato, a saber B. clarridgeiae y B. koehlerae. Sin embargo, queda por confirmar,
mediante aislamiento y análisis del ADN presente en las lesiones, si estas
especies juegan un papel en la etiología humana de la fiebre de rasguño del gato.
El autor examina el estado actual de los conocimientos sobre la etiología, los
 Rev. sci. tech. Off. int Epiz., 19(1)
144

rasgos clínicos y las características epidemiológicas de la fiebre de rasguño del

gato y de la angiomatosis bacilar, y discute del diagnóstico, tratamiento y
prevención de estas enfermedades.

Palabras clave
Angiomatosis bacilar-Bartonella clarridgeiae-Bartonella henselae - Fiebre de rasguño
del gato - Gatos - Zoonosis.

References

1. Abbott R.C., Chomel B.B., Kasten R.W., Floyd- 10. Bass J.W., Vincent J.M. & Person D.A. (1997). - The
Hawkins K.A., Kikuchi Y., Koehler J.E. & Perdersen N.C. expanding spectrum of Bartonella infections. II. Cat-scratch
(1997). - Experimental and natural infection with Bartonella disease. Pediatr. infect. Dis.J., 16, 163-179.
henselae in domestic cats. Comp. Immunol. Microbiol., infect.
11. Bass J.W., Freitas B.C., Freitas A.D., Sisler C.L., Chan D.S.,
Dis., 20, 41-51.
Vincent J.M., Person D.A., Claybaugh J.R., Wittler R.R.,
2. Alkan S., Morgan M.B., Sandin R.L., Moscinski L.C. & Ross Weisse M.E., Regnery R.L. & Slater L.N. (1998). -
C.W. (1995). - Dual role for Afipia felis and Rochalimaea Prospective randomized double blind placebo-controlled
henselae in cat-scratch disease. Lancet, 345, 385. evaluation of azithromycin for treatment of cat-scratch
3. Amerein M.P., De Briel D., Jaulhac B., Meyer P., Monteil H. disease. Pediatr. infect. Dis.]., 17, 447-452.
& Piemont Y. (1996). - Diagnostic value of the indirect
12. Batterman H.J., Peek J.A., Loutit J.S., Falkow S. &
immunofluorescence assay in cat scratch disease with
Tompkins L.S. (1995). - Bartonella henselae and Bartonella
Bartonella henselae and Afipia felis antigens. Clin. diagn. Lab.
quintana adherence to and entry into cultured human
Immunol., 3, 200-204.
epithelial cells. Infect. Immun., 63 (11), 4553-4556.
4. Anderson B., Kelly C , Threlkel R. & Edwards K. (1993). -
Detection of Rochalimaea henselae in cat scratch disease skin 13. Bergmans A.M.C., Groothedde J.W., Schellekens J.F.P., Van
test antigens. J. infect. Dis., 168, 1034-1036. Embden J.D.A., Ossewaarde J.M. & Schouls L.M. (1995). -
Etiology of cat scratch disease: comparison of polymerase
5. Anderson B., Sims K. Regnery R., Robinson L.,
chain reaction detection of Bartonella (formerly Rochalimaea)
Schmidt M.J., Goral S., Hager C. & Edwards K. (1994). -
and Afipia felis DNA with serology and skin tests. J. infect.
Detection of Rochalimaea henselae DNA in specimens from
Dis., 171,916-923.
cat scratch patients by PCR. J. clin. Microbiol, 3 2 , 942-948.
6. Anderson B., Lu E., Jones D. & Regnery R. (1995). - 14. Bergmans A.M.C., Schellekens J.F.P., Van Embden J.D.A. &
Characterization of a 17-kilodalton antigen of Bartonella Schouls L.M. (1996). - Predominance of two Bartonella
henselae reactive with sera from patients with cat scratch henselae variants among cat-scratch disease patients in the
disease. J. clin. Microbiol. 3 3 , 2358-2365. Netherlands. J. clin. Microbiol, 34, 254-260.

7. Anderson B.E. & Neuman M. (1997). - Bartonella spp. as 15. Bergmans A.M.C., De Jong C.M.A., Van Amerongen G.,
emerging pathogens. Clin. Microbiol. Rev., 10, 203-219. Schot C.S. & Schouls L.M. (1997). - Prevalence of Bartonella
species in domestic cats in the Netherlands. J. clin. Microbiol,
8. Baneth G., Kordick D.L., Hegarty C. & Breitschwerdt E.B.
35, 2256-2261.
(1996). - Comparative seroreactivity to Bartonella henselae
and Bartonella quintana among cats from Israel and North 16. Bergmans A.M.C., Peeters M.F., Schellekens J.F.P.,
Carolina. Ve£. Microbiol, 50, 95-103. Vos M.C., Sabbe L.J.M., Ossewaarde J.M., Verbakel H.,
9. Barka N.E., Hadfield T., Patnaik M., Schwartzman W.A. & Hooft H.J. & Schouls L.M. (1997). - Pitfalls and fallacies of
Peter J.B. (1993). - EIA for detection of Rochalimaea cat scratch disease serology: evaluation of Bartonella
henselae-reactive IgG, IgM, and IgA antibodies in patients henseïae-based indirect fluorescence assay and
with suspected cat-scratch disease (letter). J. infect. Dis., 16, enzyme-linked immunoassay. J. din. Microbiol., 35,
1503-1504. 1931-1937.
Rev. sci. tech. Off. int Epiz., 19 (1) 145

17. Birtles R.J. (1995). - Differentiation of Bartonella species 31. Chomel B.B., Abbott R.C., Kasten R.W., Floyd-
using restriction endonuclease analysis of PCR-amplified 16S Hawkins K.A., Kass P.H., Glaser C.A., Pedersen N.C &
rRNA genes. FEMS Microbiol. Lett, 129, 261-266. Koehler J.E. (1995). - Bartonella henselae prevalence in
domestic cats in California: risk factors and association
18. Birtles R.J., Harrison T.G., Saunders N.A. & Molyneux D.H.
between bacteremia and antibody titers. J. din. Microbiol, 33,
(1995). - Proposals to unify the genera Grahamella and
2445-2450.
Bartonella, with descriptions of Bartonella talpae comb, nov.,
Bartonella peromysci c o m b . nov., and three new species,
32. Chomel B.B., Gurfield A.N., Boulouis H.J., Kasten R.W. &
Bartonella grahamii sp. nov., Bartonella taylorii sp. nov., and
Piémont Y. (1995). - Réservoir félin de l'agent de la maladie
Bartonella doshiae sp. nov. Int.J. syst. Bacteriol., 45 (1), 1-8.
des griffes du chat, Bartonella henselae, en région parisienne :
19. Birtles R.J. & Raoult D. (1996). - Comparison of partial résultats préliminaires. Rec. Méd. vét, 171, 841-845.
synthase gene (gltA) sequences for phylogenetic analysis of
Bartonella species. Int. J. syst. Bacteriol., 46, 91-897. 33. Chomel B.B., Kasten R.W., Floyd-Hawkins K.A., Chi B.,
Yamamoto K., Roberts-Wilson J., Gurfield A.N., Abbott R.C,
20. Branley J., Wolfson C., Waters P., Gottlieb T. & Bradbury R. Pedersen N.C & Koehler J.E. (1996). - Experimental
(1996). - Prevalence of Bartonella henselae bacteremia, the transmission of Bartonella henselae by the cat flea. J. clin.
causative agent of cat scratch disease, in an Australian cat Microbiol. 34, 1952-1956.
population. Pathology, 28, 262-265.
34. Chomel B.B., Carlos E.T., Kasten R.W., Yamamoto K.,
21. Breitschwerdt E.B. & Kordick D.L. (1995). - Bartonellosis.
Chang C - C , Carlos R.S., Abenes M.V. & Pajares CM.
J. Am. vet. med. Assoc., 206, 1928-1931.
(1999). - Bartonella henselae and Bartonella darridgäae
22. Breitschwerdt E.B., Kordick D.L., Malarkey D.E., Keene B., infection in domestic cats from the Philippines. Am. J. trop.
Hadfield T.L. & Wilson K. (1995). - Endocarditis in a dog Med. Hyg., 60, 593-597.
due to infection with a novel Bartonella subspecies. J. clin.
Microbiol, 33, 154-160. 35. Chomel B.B., Ermel R.W., Kasten R.W., Yamamoto K.,
Chang C.-C, Heller R., Weber D., Poland A., Piemont Y.,
23. Brenner D.J., O'Connor S.P., Winkler H.H. & Boulouis H.J. & Pedersen N.C. (1999). - Experimental
Steigerwalt A.G. (1993). - Proposals to unify the genera infection of cats and dogs with Bartonella isolated from
Bartonella and Rochaiimaea, with descriptions of Bartonella domestic and wild carnivores. In Programme and Abstracts:
quintana c o m b . nov., Bartonella vinsonii comb. nov., International Conference on Rickettsiae and Rickettsial
Bartonella henselae comb. nov., and Bartonella elizabeihae Disease and American Society for Rickettsiology, 14th
comb. nov., and to remove the family Bartonellaceae from the Sesquiannual Joint Meeting (P. Brouqui, ed.), 13-16 June,
order Rickettsiales. Int.J. syst. Bacteriol., 43, 777-786. Marseilles, France. Reprographie Crillon, Marseilles, 103 pp.
24. Brenner S.A., Rooney J.A., Manzewitsch P. & Regnery R.L.
(1997). - Isolation of Bartonella (Rochaiimaea) henselae: 36. Clarridge J.E. III, Raich T.J., Pirwani D., Simon B., Tsai L.,
effects of methods of b l o o d collection and handling. J. clin. Rodríguez-Barradas M.C., Regnery R.L., Zollo A., Jones D.C.
Microbiol. 35, 544-547. & Rambo C. (1995). - Strategy to detect and identify
Bartonella species in routine clinical laboratory yields
25. Carithers H.A. (1985). - Cat scratch disease. An overview Bartonella henselae from human immunodeficiency
based on a study of 1,200 patients. Am. J. Dis. Child., 139, virus-positive patient and unique Bartonella strain from his
1124-1133. cat. J. clin. Microbiol, 33, 2107-2113.

26. Carithers H.A. & Margileth A.M. (1991). - Cat scratch

37. Cline M.S., Cummings O.W., Goldman M., Filo R.S. &
disease. Acute encephalopathy and other neurologic
Pescovitz M.D. (1999). - Bacillary angiomatosis in a renal
manifestations. Am. J. Dis. Child., 145, 98-101.
transplant recipient. Transplantation, 67, 296-298.
27. Chia J.K.S., Nakata M.M., LamiJ.L.M., Park S.S. & Ding J.C.
(1998). - Azithromycin for the treatment of cat-scratch 38. Dalton M.J., Robinson L.E., Cooper J., Regnery R.L.,
disease. Clin. infect Dis., 26, 193-194. Olson J.G. & Childs J.E. (1995). - U s e of Bartonella antigens
for serologic diagnosis of cat-scratch disease at a national
28. Childs J.E., Rooney J.A., Cooper J.L., Olson J.G. & referral center. Arch. internal Med., 155, 1670-1676.
Regnery R.L. (1994). - Epidemiologic observations on
infection with Rochaiimaea species among cats living in 39. Daly J.S., Worthington M.G., Brenner D.J., Moss C.W.,
Baltimore, Md. J. Am. vet. med. Assoc., 204, 1775-1778. Hollis D.G., Weyant R.S., Steigerwalt A.G., Weaver R.E.,
Daneshvar M.I. & O'Connor S.P. (1993). - Rochaiimaea
29. Childs J.E., Olson J.G., Wolf A., Cohen N . , F a k i l e Y.,
elizabethae sp. nov. isolated from a patient with endocarditis.
Rooney J.A., Bacellar F. & Regnery R.L. (1995). - Prevalence
J. clin. Microbiol. , 3 1 , 8 7 2 - 8 8 1 .
of antibodies to Rochaiimaea species (cat scratch disease
agent) in cats. Vet. Rec., 136, 519-520.
40. Debré R., Lamy M., Jammet M.L., Costil L. & Mozziconacci
30. Chomel B.B. (1996). - Cat-scratch disease and bacillary P. (1950). - La maladie des griffes de chat. Bull. Membres Soc.
angiomatosis. Rev. sci. tech. Off. int. Epiz., 15 (3), 1061-1073. méd. Hôp. Paris, 66, 76-79.
146 Rev. sci. tech. Off. int. Epiz., 19(1)

41. Dehio C , Meyer M., Berger J., Schwarz H. & Lanz C. (1997). 53. Freeland R.L., Scholl D.T., Rohde K.R., Shelton L.J. &
- Interaction of Bartonella henselae with endothelial cells O'Reilly K.L. (1999). - Identification of BartoneHa-specific
results in bacterial aggregation on the cell surface and the immunodominant antigens recognized by the feline humoral
subsequent engulfment and internalisation of the bacterial immune system. Clin. diagn. Lab. Immunol, 6, 558-566.
aggregate by a unique structure, the invasome. J. Cell Sri.,
54. Gasquet S., Maurin M., Brouqui P., Lepidi H. & Raoult D.
110, 2141-2154.
(1998). - Bacillary angiomatosis in immunocompromised
42. Demers D.M., Bass J.W., Vincent J.M., Person D.A., patients. AIDS, 12, 1793-1803.
Noyes D.K., Staege C.M., Samlaska C.P., Lockwood N.H., 55. George T.I., Manley G., Koehler J.E., Hung V.S.,
Regnery R.L. & Anderson B.E. (1995). - Cat-scratch disease McDermott M. & Bollen A. (1998). - Detection of Bartonella
in Hawaii: etiology and seroepidemiology. J. Pediatr., 127, henselae by polymerase chain reaction in brain tissue of an
23-26. immunocompromised patient with multiple enhancing
lesions. J. neurosurg. Anaesthesiol., 89, 640-644.
43. Dolan M.J., Wong M.T., Regnery R.L., Jorgensen J.H.,
Garcia M., Peters J. & Drehner D. (1993). - Syndrome of 56. Gieger T.L., Taboada J. & Groves M.G. (1998). - Cat scratch
Rochalimaea henselae adenitis suggesting cat scratch disease. disease and other Bartonella infections. Compend. cont. Educ.
Ann. internal Med., 118, 331-336. pract. Vet., 20, 1308-1312, 1314-1317.

44. Drancourt M., Birtles R., Chaumentin G., Vandenesch F., 57. Guadi M., Avidor B., Kletter Y., Abulafia S., Slater L.N.,
Etienne J. & Raoult D. (1996). - New serotype of Bartonella Welch D.F., Brenner D.J., Steigerwalt A.G., Whitney A.M. &
henselae in endocarditis and cat-scratch disease. Lancet, 347, Ephros M. (1998). - Cat scratch disease: the rare role of
441-443. Afipia felis. J. clin. Microbiol, 36, 2499-2502.

45. Droz S., Chi B., Horn E., Steigerwalt A.G., Whitney A.M. & 58. Glaus T., Hofmann-Lehmann R., Greene C , Glaus B.,
Brenner D.J. (1999). - Bartonella koehlerae sp. nov., isolated Wolfensberger C. & Lutz H. (1997). - Seroprevalence of
from cats. J. clin. Microbiol, 37, 1117-1122. Bartonella henselae infection and correlation with disease
status in cats in Switzerland. J. din. Microbiol, 35,
46. Dupon M., Savin De Larclause A.-M., Brouqui P., 2883-2885.
Drancourt M., Raoult D., De Mascarel A. & Lacut J.Y.
(1996). - Evaluation of serological response to Bartonella 59. Greene C.E., McDermott M., Jameson P.H., Atkins C.L. &
henselae, Bartonella quintana, and Afipia felis antigens in Marks A.M. (1996). - Bartonella henselae infection in cats:
64 patients with suspected cat-scratch disease. Scand. f. evaluation during primary infection, treatment and
infect. Dis., 28, 361-366. rechallenge infection. J. din. Microbiol, 34, 1682-1685.

47. Ellis B.A., Regnery R.L., Beati L., Bacellar F., Rood M., 60. Groves M.G. & Harrington K.S. (1994). - Rochalimaea
Glass G.G., Marston E., Ksiazek T.G., Jones D. & Childs J.E. henselae infections: newly recognized zoonoses transmitted
(1999). - Rats of the genus Rattus are reservoir hosts for by domestic cats. J. Am. vet. med. Assoc., 204, 267-271.
pathogenic Bartonella species: an old world origin for a new 61. Guptill L., Slater L , W u C.-C, Lin T.-L., Glickman L.T.,
world disease? J. infect. Dis., 180, 220-224. Welch D.F. & Hogenesch H. (1997). - Experimental
infection of young specific pathogen-free cats with Bartonella
48. English C.K., Wear D.J., Margileth A.M., Lissner C.R. &
henselae.J. infect. Dis., 176, 206-216.
Walsh G.P. (1988). - Cat scratch disease. Isolation and
culture of the bacterial agent. JAMA, 259, 1347-1352. 62. Guptill L. Slater L.N., Wu C.-C, Lin T.-L., Glickman LT.,
Welch D.F., Tobolski J. & Hogenesch H. (1998). - Evidence
49. Flexman J.P., Lavis N.J., Kay I.D., Watson M., Metcalf C. & of reproductive failure and lack of perinatal transmission of
Pearman J.W. (1995). - Bartonella henselae is a causative Bartonella henselae in experimentally infected cats. Vet.
agent of cat scratch disease in Australia. J. Infection, 3 1 , Immunol. Immunopathol., 65, 177-189.
241-245.
63. Guptill L., Slater L., Wu C.-C., Lin T.-L., Glickman L.T.,
50. Flexman J.P., Chen S.C.A., Dickeson D.J., Pearman J.W. & Welch D.F., Tobolski J. & Hogenesch H. (1999). - Immune
Gilbert G.L. (1997). - Detection of antibodies to Bartonella response of neonatal specific pathogen-free cats to
henselae in clinically diagnosed cat scratch disease. Med. J. experimental infection with Bartonella henselae. Vet. Immunol.
Aust., 166, 532-535. Immunopathol., 71, 233-243.
51. Foil L., Andress E., Freeland R.L., Roy A.F., Rutledge R., 64. Gurfield N., Boulouis H.J., Chomel B., Heller R., Kasten R.,
Triche P.C. & O'Reilly K.L. (1998). - Experimental infection Yamamoto K. & Piemont Y. (1997). - Coinfection with
of domestic cats with Bartonella henselae by inoculation of Bartonella clarridgeiae and Bartonella henselae and with
Ctenocephalides felis (Siphonaptera: Pulicidae) feces, f. med. different Bartonella henselae strains in domestic cats. J. din.
Entomol. 35, 625-628. Microbiol, 35, 2120-2123.

52. Foley J., Chomel B., Kikuchi Y., Yamamoto K. & 65. Gurfield N., Boulouis H.J., Chomel B., Heller R., Kasten R.,
Pedersen N.C (1998). - Seroprevalence of Bartonella Yamamoto K. & Piemont Y. (1997). - Epidemiology of
henselae in cattery cats: association with cattery hygiene and Bartonella infection in domestic French cats. Epidémiol. Santé
flea infestation. Vet. Q., 20, 1-5. anim., 31-32, 04.03.1-3.
Rev. sci. tech. Off.intEpiz., 19 (1) 147

66. Hamilton D.H., Zangwill K.M., Hadler J.L. & Cartter M.L. 79. Koehler J.E., Leboit P.E., Egbert B.M. & Berger T.G. (1988).
(1995). - Cat-scratch disease - Connecticut, 1992-1993. - Cutaneous vascular lesions and disseminated cat scratch
J. infect. Dis., 172 (2), 570-573. disease in patients with acquired immunodeficiency
syndrome (AIDS) and AIDS-related complex. Ann. internal
67. Heller R., Artois M., Xemar V., De Briel D., Gehin H , Med., 109, 449-455.
Jaulhac B., Monteil H. & Piemont Y. (1997). - Prevalence of
Bartonella henselae and Bartonella clarridgeiae in stray cats. 80. Koehler J.E., Quinn F.D., Berger T.G., Leboit P.E. &
J. clin. Microbiol., 35, 1327-1331. Tappero J.W. (1992). - Isolation of Rochalimaea species from
cutaneous and osseous lesions of bacillary angiomatosis. New
68. Higgins J.A., Radulovic S., Jaworski D.C. & Azad A.F. Engl. J. Med., 327, 1625-1631.
(1996). - Acquisition of the cat scratch disease agent
Bartonella henselae b y cat fleas (Siphonaptera: Pulicidae). 81. Koehler J.E. & Tappero J.W. (1993). - AIDS commentary:
J. med. Entomol, 3 3 , 490-495. bacillary angiomatosis and bacillary peliosis in patients
infected with human immunodeficiency virus. Clin. infect.
69. Holmberg M., McGill S., Ehrenborg C , Wesslen L., Dis., 17, 612-624.
Hjelm E., Darelid J., Blad L., Engstrand L., Regnery R. &
Friman G. (1999). - Evaluation of human seroreactivity to 82. Koehler J.E., Glaser C.A. & Tappero J.T. (1994). -
Bartonella species in Sweden. J. clin. Microbiol, 37, Rochalimaea henselae infection: a n e w zoonosis with the
1381-1384. domestic cat as reservoir. ]AMA, 2 7 1 , 531-535.

83. Koehler J.E., Sanchez M.A., Garrido C.S., Whitfeld M.J.,

70. Holmes A.H., Greenough T.C., Balady G.J., Regnery R.L.,
Chen F.M., Berger T.G., Rodriguez-Barradas M.C.,
Anderson B.E., Conor O'Keane J., Fonger J.D. &
Leboit P.E. & Tappero J.W. (1997). - Molecular
McCrone E.L. (1995). - Bartonella henselae endocarditis in an
epidemiology of Bartonella infections in patients with
immunocompetent adult. Clin. infect. Dis., 2 1 , 1004-1007.
bacillary angiomatosis-peliosis. New Engl. J. Med., 337,
1876-1883.
71. Jackson L.A., Perkins B.A. & Wenger J.D. (1993). - Cat
scratch disease in the United States: an analysis of three
84. Kordick D.L. & Breitschwerdt E.B. (1995). -
national data bases. Am. J. public Hlth, 83, 1707-1711.
Intraerythrocytic presence of Bartonella henselae. J. clin.
Microbiol, 33, 1655-1656.
72. Jameson P., Green C , Regnery R., Dryden M., Marks A.,
Brown J., Cooper J., Glaus B. & Greene R. (1995). - 85. Kordick D.L., Wilson K.H., Sexton D.J., Hadfield T.L.,
Prevalence of Bartonella henselae antibodies in pet cats Berkhoff H.A. & Breitschwerdt E.B. (1995). - Prolonged
throughout regions of North America. J. infect. Dis., 1 7 2 , Bartonella bacteremia in cats associated with cat-scratch
1145-1149. disease patients. J. clin. Microbiol., 33, 3245-3251.

73. Joblet C , Roux V., Drancourt M., Gouvernet J. & Raoult D. 86. Kordick D.L., Swaminathan B., Greene C.E., Wilson K.H.,
(1995). - Identification of Bartonella (Rochalimaea) species Whitney A.M., O'Connor S., Hollis D.G., Matar G.M.,
among fastidious gram-negative bacteria o n the basis of the Steigerwalt A.G., Malcolm G.B., Hayes P.S., Hadfield T.L.,
partial sequence of the citrate-synthase gene. J. din. Breitschwerdt E.B. & Brenner D.J. (1996). - Bartonella
Microbiol., 3 3 , 1879-1883. vinsonii subsp. berkhoffii subsp. nov., isolated from dogs;
Bartonella vinsonii subsp. vinsonii; and emended description
74. Joseph A.K., W o o d C.W., Robson J.M., Paul S.L. & of Bartonella vinsonii int. J. syst. Bacteriol.,46 (3), 704-709.
Morris A.J. (1997). - Bartonella henselae bacteraemia in
domestic cats from Auckland. N.Z. vet. J., 4 5 , 185-187. 87. Kordick D.L. & Breitschwerdt E.B. (1997). - Relapsing
bacteremia after blood transmission of Bartonella henselae to
75. Karpathios T., Golphinos C , Psychou P., Garoufi A., cats. Am. J. vet. Res., 58, 492-497.
Papadimitriou A. & Nicolaidou P. (1998). - Cat scratch
disease in Greece. Arch. Dis. Child., 78, 64-66. 88. Kordick D.L., Hilyard E.J., Hadfield T.L., Wilson. K.H.,
Steigerwalt A.G., Brenner D.J. & Breitschwerdt. E.B. (1997).
76. Kelly P.J., Matthewman L.A., Hayter D., Downey S., — Bartonella darridgeiae, a newly r e c o g n i z e d zoonotic
Wray K., Bryson N.R. & Raoult D. (1996). - Bartonella pathogen causing inoculation papules, fever, and
(Rochalimaea) henselae in Southern Africa - evidence for lymphadenopathy (cat scratch disease). J. clin. Microbiol., 35,
infections in domestic cats and implications for 18134818.
veterinarians. J. S. Afr. vet. Assoc., 67, 182-187.
89. Kordick D.L., Papich M.G. & Breitschwerdt E.B. (1997). -
77. Kelly P.J., Rooney J.J.A., Marston E.L., Jones D.C. & Efficacy of enrofloxacin and doxycycline tot treatment of
Regnery R.L. (1998). - Bartonella henselae isolated from cats Bartonella henselae or Bartonella clarridgeiae infection in cats.
in Zimbabwe. Lancet, 3 5 1 , 1 7 0 6 . Antimicrob. AgentsChemother.,4 1 , 2448-2455.

78. Kirkpatrick C.E. & Whiteley H.E. (1987). - Argyrophilic, 90. Kordick D.L. & Breitschwerdt E.B. (1998). - Persistent
intracellular bacteria in the lymph node of a cat: cat scratch infection of pets within a household with three Bartonella
disease bacilli? J. infect. Dis., 156, 690-691. species, Emerg. infect. Dis., 4 , 325-328.
148 Rev. sci. tech. Off.int.Epiz., 19 (1)

91. Kordick D.L., Brown T.T., Shin K. & Breitschwerdt E.B. 104. Marston E.L., Finkel B., Regnery R.L., Winoto I.L.,
(1999). - Clinical and pathologic evaluation of chronic Graham R.R., Wignal S., Simanjuntak G. & Olson J.G.
Bartonella henselae or Bartonella clarridgeiae infection in cats. (1999). – Prevalence of Bartonella henselae and Bartonella
J. clin. Microbiol, 37, 1536-1547. clarridgeiae in an urban Indonesian cat population. Clin.
diagn. Lab. Immunol, 6, 41-44.
92. Lappin M.R. & Black J.C. (1999). - Bartonella spp. infection
as a possible cause of uveitis in a cat. J. Am. vet. med. Assoc. 105. Maruyama S., Nogami S., Namba S., Asanome K. &
214, 1205-1207. Katsube Y. (1996). - Isolation of Bartonella henselae from
domestic cats in Japan. J. vet. med. Sci., 58, 81-83.
93. La Scola B. & Raoult D. (1996). - Serological cross-reaction
between Bartonella quintana, Bartonella henselae and Coxiella 106. Matar G.M., Swaminathan B., Hunter S.B., Slater L.N. &
burnetii. J. clin. Microbiol., 34, 2270-2274. Welch D.F. (1993). - Polymerase chain reaction-based
restriction fragment length polymorphism analysis of a
94. La Scola B. & Raoult D. (1999). - Afipia felis in hospital water fragment of the ribosomal operon from Rochalimaea species
supply in association with free-living amoeba. Lancet, 353, for subtyping. J. clin. Microbiol, 3 1 , 1730-1734.
1330.
107. Maurin M. & Raoult D. (1993). - Antimicrobial
95. La Scola B. & Raoult D. (1999). - Culture of Bartonella susceptibility of Rochalimaea quintana, R. vinsonii, and the
quintana and Bartonella henselae from human samples: a newly recognized Rochalimaea henselae. J. antimicr.
5-year experience (1993 to 1998). J. clin. Microbiol, 37, Chemother., 3 2 , 587-594.
1899-1905.
108. Minnick M.F. & Barbian K.D. (1997). - Identification of
96. Lawson P.A. & Collins M.D. (1996). - Description of Bartonella using PCR; genus- and species-specific primer
Bartonella clarridgeiae sp. nov. isolated from the cat of a sets. J. microbiol Meth., 3 1 , 51-57.
patient with Bartonella henselae septicemia. Med. Microbiol.
Lett., 5, 64-73. 109. Nadal D. & Zbinden R. (1995). - Serology to Bartonella
(Rochalimaea) henselae may replace traditional diagnostic
97. Leboit P.E., Berger T.G., Egbert B.M., Yen T.S., Stoler M.H., criteria for cat-scratch disease. Eur. J. Pediatr., 154, 906-908.
Bonfiglio T.A., Strauchen J.A., English C.K. & Wear D.J.
(1988). - Epithelioid haemangioma-like vascular 110. Nasirudeen A.M.A. & Thong M.L. (1999). - Prevalence of
proliferation in AIDS: manifestation of cat scratch disease Bartonella henselae immunoglobulin G antibodies in
bacillus infection? Lancet, 1, 960-963. Singaporean cats. Pediatr. infect. Dis. f., 18, 276-278.

98. Litwin C.M., Martins T.B. & Hill H.R. (1997). - 111. Noah D.L., Bresee J.S., Gorensek M.J., Rooney J.A.,
Immunologic response to Bartonella henselae as determined Cresanta J.L., Regnery R.L., Wong J., Del Toro J., Olson J.G.
by enzyme immunoassay and western blot analysis. Am. J. & Childs J.E. (1995). - Cluster of five children with acute
clin. Pathol, 108, 202-209. encephalopathy associated with cat-scratch disease in South
Florida. Pediatr. infect. Dis. J., 14, 866-869.
99. Lucey D., Dolan M.J., Moss C.W., Garcia M., Hollis D.G.,
Wegner S., Morgan G., Almeida R., Leong D., Greisen K.S., 112. Noah D.L., Kramer C.M., Verbsky M.P., Rooney J.A.,
Welch D.F. & Slater L.N. (1992). - Relapsing illness due to Smith K.A. & Childs J.E. (1997). - Survey of veterinary
Rochalimaea henselae in immunocompetent hosts: professionals and other veterinary conference attendees for
implication for therapy and new epidemiological antibodies to Bartonella henselae and B. quintana. J. Am. vet.
associations. Clin. infect. Dis., 14, 683-688. med. Assoc., 210, 342-344.

100. Marano N., Jameson P., Marston E., Jones D., Greene C. & 113. O'Reilly K.L., Bauer R.W., Freeland R.L., Foil L.D.,
Regnery R. (1998). - A third Bartonella species isolated from Hughes K.J., Rohde K.R., Roy A.F., Stout R.W. & Triche P.C.
domestic cats, Bartonella weissi, sp. nov. National Center for (1999). - Acute clinical disease in cats following infection
Biotechnology Information, GenBank, Accession No. with a pathogenic strain of Bartonella henselae (LSU 16).
AF071190 (http://www.ncbi.nlm.nih.gov). Infect. Immun., 67, 3066-3072.

101. Margileth A.M. (1992). - Antibiotic therapy for cat scratch 114. Pappalardo B.L., Correa M.T., York C.C., Peat C.Y. &
disease: clinical study of therapeutic outcome in 268 patients Breitschwerdt E.B. (1997). - Epidemiologic evaluation of the
and a review of the literature. Pediatr. infect. Dis. f., 11, risk factors associated with exposure and seroreactivity to
474-478. Bartonella vinsonii in dogs. Am. J. vet. Res., 58, 467-471.

102. Margileth A.M. (1993). - Cat scratch disease. Adv. Pediatr. 115. Raoult D. (1999). - Infections humaines à Bartonella. Presse
Infect. Dis., 8, 1-21. méd., 28, 429-434.

103. Margileth A.M. & Baehren D.F. (1998). - Chest-wall abscess 116. Regnery R.L., Anderson B.E., Clarridge J.E. III,
due to cat-scratch disease (CSD) in an adult with antibodies Rodriguez-Barradas M.C., Jones D.C. & Carr J.H. (1992). -
to Bartonella clarridgeiae: case report and review of the Characterization of a novel Rochalimaea species, R. henselae,
thoracopulmonary manifestations of CSD. Clin. infect. Dis., sp. nov., isolated from blood of a febrile, HIV-positive
27, 353-357. patient. J. din. Microbiol, 30, 265-274.
Rev. sci. tech. Off. int. Epiz., 19 (1) 149

117. Regnery R.L., Martin M. & Olson J.G. (1992). - Naturally 130. Slater L.N., Welch D.F., Hensel D. & Coody D.W. (1990). -
occurring Rochalimaea henselae infection in domestic cat. A newly recognized fastidious gram-negative pathogen as a
Lancet, 340, 557-558. cause of fever and bacteremia. New Engl. J. Med., 323,
1587-1593.
118. Regnery R.L., Olson J.G., Perkins B.A. & Bibb W. (1992). -
Serological response to Rochalimaea henselae antigen in 131. Slater L.N., Welch D.F. & Min K.W. (1992). - Rochalimaea
suspected cat scratch disease. Lancet, 339, 1443-1445. henselae causes bacillary angiomatosis and peliosis hepatis.
Arch. internal Med., 152, 602-606.
119. Regnery R.L., Childs J.E. & Koehler J.E. (1995). - Infections
132. Stoler M.H., Bonfiglio T.A., Steigbigel R.T. & Pereira M.
associated with Bartonella species in persons infected with
(1983). - An atypical subcutaneous infection associated with
human immunodeficiency virus. Clin. infect. Dis., 21
acquired immune deficiency syndrome. Am. J. din. Pathol,
(Suppl. 1), 94-98.
80, 714-718.
120. Regnery R.L., Rooney J.A., Johnson A.M., Nesby S.L., 133. Szelc-Kelly C.M., Goral S., Perez-Perez G.I., Perkins B.A.,
Manzewisch P., Beaver K. & Olson J.G. (1996). - Regnery R.L. & Edwards K.M. (1995). - Serologic responses
Experimentally induced Bartonella henselae infections to Bartonella and Afipia antigens in patients with cat scratch
followed by challenge exposure and antimicrobial therapy in disease. Pediatrics, 96, 1137-1142.
cats. Am. J. vet. Res., 57, 1714-1719.
134. Tappero J.W., Mohle-Boetani J., Koehler J.E.,
121. Reiman D.A., Loutit J.S., Schmidt T.M., Falkow S. & Swaminathan B., Berger T.G., Leboit P.E., Smith L.L.,
Thompkins L.S. (1990). - The agent of bacillary Wenger J.D., Pinner R.W., Kemper C A . & Reingold A.L.
angiomatosis: an approach to the identification of (1993). - The epidemiology of bacillary angiomatosis and
uncultured pathogens. New Engl. J. Med., 323, 1573-1580. bacillary peliosis. JAMA, 269, 770-775.
135. Tobias E.J., Noone K.E. & Garvey M.S. (1998). - Managing
122. Rodriguez-Barradas M.C., Hamill R.J., Houston E.D.,
Bartonella henselae infection in cats. Vet. Med., 93, 745-749.
Georghiou P.R., Clarridge J.E., Regnery R.L. & Koehler J.E.
(1995). - Genomic fingerprinting of Bartonella species by 136. Tsukahara M., Tsuneoka H., Lino H., Ohno K. & Murano I.
repetitive element PCR for distinguishing species and (1998). - Bartonella henselae infection from a dog. Lancet,
isolates. J. clin. Microbiol, 3 3 , 1089-1093. 352, 1682.
137. Ueno H., Muramatsu Y., Chomel B.B., Hohdatsu T.,
123. Roux V. & Raoult D. (1995). - Inter- and intraspecies
Koyama H. & Morita C. (1995). - Seroepidemiological
identification of Bartonella (Rochalimaea) species. J. clin.
survey of Bartonella (Rochalimaea) henselae in domestic cats
Microbiol, 3 3 , 1573-1579.
in Japan. Microbiol. Immunol, 39, 339-341.
124. Sander A., Buhler C , Pelz K , Von Cramm E. & Bredt W. 138. Ueno H., Hohdatsu T., Muramatsu Y., Koyama H. &
(1997). - Detection and identification of two Bartonella Morita C. (1996). - Does coinfection of Bartonella henselae
henselae variants in domestic cats in Germany. J. clin. and FIV induce clinical disorders in cats? Microbiol.
Microbiol, 35, 584-587. Immunol, 40, 617-620.

125. Sander A. & Frank B. (1997). - Paronychia caused by 139. Wear D.J., Margileth A.M., Hadfield T.L., Fisher G.W.,
Bartonella henselae. Lancet, 350, 1078. Schlagel C.J. & King F.M. (1983). - Cat scratch disease: a
bacterial infection. Science, 2 2 1 , 1403-1405.
126. Sander A., Posselt M., Oberle K. & Bredt W. (1998). -
140. Welch D.F., Pickett D.A., Slater L.N., Steigerwalt A.G. &
Seroprevalence of antibodies to Bartonella henselae in patients
Brenner D.J. (1992). - Rochalimaea henselae sp. nov., a cause
with cat scratch disease and in healthy controls: evaluation
of septicemia, bacillary angiomatosis, and parenchymal
and comparison of two commercial serological tests. Clin.
bacillary peliosis. J. clin. Microbiol, 30, 275-280.
diagn. Lab. Immunol, 5, 486-490.
141. Welch D.F., Carroll K.A., Hofmeister E.K., Persing D.H.,
127. Sander A., Ruess M., Bereswill S., Schuppler M. & Robison D.A., Steigerwalt A.G. & Brenner D.J. (1999). -
Steinbrueckner B. (1998). - Comparison of different DNA Isolation of a new subspecies, Bartonella vinsonii subsp.
fingerprinting techniques for molecular typing of Bartonella arupensis, from a cattle rancher: identity with isolates found
henselae isolates. J. din. Microbiol, 36, 2973-2981. in conjunction with Borrelia burgdorferi and Babesia microti
among naturally infected mice. J. din. Microbiol., 37,
128. Sander A., Posselt M., Bohm N., Ruess M. & Altwegg M. 2598-2601.
(1999). - Detection of Bartonella henselae DNA by two
different PCR assays and determination of the genotypes of 142. Wong M.T., Dolan M.J., Lattuada C.P., Regnery R.L.,
strains involved in histologically defined cat scratch disease. Garcia M.L., Mokulis E.C., Labarre R.C, Ascher D.P.,
J. clin. Microbiol, 37, 993-997. Delmar J.A., Kelly J.W., Leigh D.R., McRae A.C., Reed J.B.,
Smith R.E. & Melcher G.P. (1995). - Neuroritinitis, aseptic
129. Schwartzman W.A., Patnaik M., Angulo F.J., Vissher B.J., meningitis, and lymphadenitis associated with Bartonella
Miller E.M. & Peter J.B. (1995). - Bartonella (Rochalimaea) (Rochalimaea) henselae infection in immunocompetent
antibodies, dementia, and cat ownership among m e n patients and patients infected with human
infected with human deficiency virus. Clin. infect. Dis., 2 1 , immunodeficiency virus type I. Clin. infect. Dis., 2 1 ,
954-959. 352-360.
150 Rev. sci. tech. Off. int Epiz., 19 (1)

143. Yamamoto K., Chomel B.B., Kasten R.W., Chang C.C., 146. Zbinden R., Michael N., Sekulovski M., Von Graevenitz A. &
Tseggai T., Decker P.R., Mackowiak M., Floyd-Hawkins K.A. Nadal D. (1997). - Evaluation of commercial slides for
& Pedersen N.C. (1998). - Homologous protection but lack detection of immunoglobulin G against Bartonella henselae by
of heterologous-protection by various species and types of indirect immunofluorescence. Eur. J. clin. Microbiol. infect.
Bartonella in specific pathogen-free cats. Vet. Immunol. Dis., 16, 648-652.
Immunopathol., 65, 191-204.

144. Yoshida H., Kusaba N., Omachi K., Miyazaki N.,

Yamawaki M., Tsuji Y., Nakahara K., Sumito M.,
Noudomi M., Shimokawa Y. & Tanikawa K. (1996). -
Serological study of Bartonella henselae in cat scratch disease
in Japan. Microbiol. Immunol., 40, 671-673.

145. Zangwill K.M., Hamilton D.H., Perkins B.A., Regnery R.L.,

Plikayüs B.D., Hadler J.L., Cartter M.L. & Wengler J.D.
(1993). - Cat scratch disease in Connecticut: epidemiology,
risk factors, and evaluation of a new diagnostic test. New
Engl.J. Med., 329, 8-13.