1. pets
2. cats

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 Cat-scratch disease - Zoonoses.
Introduction
Cat-scratch disease (CSD) h a s b e e n clinically identified in
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
patients, s u c h as bacteraemia (130), peliosis hepatis ( 1 3 1 ,
140), altered mental status (55) or dementia (129). In
i m m u n o c o m p e t e n t individuals, the clinical spectrum of
B. henselae infection h a s widely e x p a n d e d to include
endocarditis (70), neuroretinitis, aseptic meningitis ( 2 6 , 1 4 2 ) ,
hepatic and splenic abscesses, p n e u m o n i a and pleural
effusion, musculoskeletal manifestations, osteomyelitis, and
paravertebral abscesses (7). Recent evidence demonstrated
that Bartonella (formerly Rochaiimaea)
henselae (23), a
bacterium that h a s b e e n isolated from patients with bacillary
Bartonella henselae -
Cats
-
angiomatosis (BA), is associated with CSD (43, 5 4 , 1 1 6 , 118,
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
h u m a n immunodeficiency virus (HIV) (119).
T h e cause of CSD h a s long b e e n in question. Initially it was
considered to b e a possible virus, t h e n a Gram-negative
bacterium. However, it is only in recent years that a specific
organism h a s b e e n identified. In 1 9 8 3 , a small bacillus was
identified b y Warthin-Starry silver deposition stain o n l y m p h
n o d e biopsies of thirty-nine patients with CSD (139). In 1988,
a p l e o m o r p h i c , Gram-negative bacterium was isolated from
the l y m p h n o d e of a CSD patient at the A r m e d Forces Institute
of Pathology in the United States of America (USA) (48).
Afipia felis was then considered as the most p r o b a b l e agent of
CSD. Recently, a report implicated B. henselae and A. felis,
137
Rev. sci. tech. Off. int Epiz., 19 (1)
based o n polymerase chain reaction (PCR) testing (2).
Isolation of A. felis was difficult and a very limited n u m b e r of
strains w e r e isolated in only two laboratories. T h e serology of
the bacterium was not highly specific and was difficult to
standardise. Isolation of A. felis was recently reported from a
patient with CSD (57), h o w e v e r , PCR testing of thirty-two
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
results for A. felis, w h e r e a s all samples w e r e positive for
B. henselae. Afipia felis was c o n c l u d e d to b e only a rare cause
of CSD (57). Strong evidence demonstrates that A. felis is an
environment bacterium that lives in water. It is suggested that
previous isolations of A. felis from l y m p h n o d e s could b e d u e
to water contamination through ineffectively sterilised fluids
used for culture (94).
The identification of B. henselae as the agent of CSD was an
indirect result of the e p i d e m i c of acquired i m m u n e deficiency
syndrome (AIDS). A n e w disease k n o w n as bacillary
angiomatosis (BA), a type of vascular proliferative lesion in
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
HIV-infected patients b e t w e e n 1983 and 1988 (79, 80, 97,
132). T h e disease was attributed to a n e w Gram-negative
bacillus, w h i c h was subsequently n a m e d
Rochaiimaea
henselae (116, 1 2 1 , 140). An indirect immunofluorescence
antibody test (IFA) was d e v e l o p e d in 1 9 9 2 , at the Centers for
Disease Control and Prevention, to detect antibodies to this
organism (118). Using this test, it was n o t e d that 8 8 % of sera
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
(118). Bartonella henselae was first isolated directly from the
cutaneous lesions of HTV-infected patients with BA i n 1991
(80), and thus this organism has b e e n directly cultured from
the lesions of b o t h BA and CSD. Bacillary angiomatosis is also
caused b y B. quintana, the agent of trench fever (80).
However, B. quintana has never b e e n directly associated with
a case of CSD. Cases of BA caused b y B. quintana usually
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
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
w h o h a d contact with cats and cat fleas (95).
It was only in the early 1990s that evidence clearly indicated
that B. henselae was m o r e likely to b e the agent of CSD than
A. felis. Bartonella are morphologically very similar to A. felis
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
explain the previous confusion. Serological studies and
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
CSD cases demonstrated the major role played b y B. henselae
in the aetiology of CSD (6, 9, 3 8 , 42, 4 3 , 109, 118, 133, 145).
Furthermore, amplification of an antigen gene of B. henselae
by PCR o n CSD skin-test material confirmed the presence of
B. henselae but not A. felis DNA (4); and in July 1 9 9 2 ,
B. henselae bacteraemia was reported in a cat with a healthy
owner (117).
A case control study to determine the risk factors associated
with developing BA revealed that the only statistically
significant risk factor w a s traumatic contact with a cat
(scratches or bites) (134). After this study, K o e h l e r et al.
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
cultures o n these animals (82). All seven cats o w n e d b y the
four patients w e r e bacteraemic with B. henselae. Furthermore,
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
the San Francisco Bay area w e r e also bacteraemic. Since then,
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
B. henselae. K o e h l e r et al. also demonstrated that peliosis
hepatis and B. henselae infection w e r e strongly associated,
w h e r e a s subcutaneous and lytic b o n e lesions w e r e m o r e
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
B. clarridgeiae, b a s e d o n serological evidence (88, 103).
However, B. clarridgeiae isolates or DNA h a v e not yet b e e n
identified from suspect cases of CSD. Bartonella
clarridgeiae
h a s b e e n isolated from domestic cats (36, 9 6 ) , w h i c h
constitute the m a i n reservoir of the bacterium in the USA (36,
89), E u r o p e (15, 65, 6 7 ) , Indonesia (104) and the Philippines
(34). T o date, B. koehlerae has only b e e n isolated from two
cats in the San Francisco area and has n o t yet b e e n l i n k e d to
any h u m a n case of CSD (45). T h e citrate synthase g e n e
s e q u e n c e of a fourth Bartonella species, B. weissi, isolated from
domestic cats, was p u b l i s h e d b y Marano et al. in GenBank in
1998 (100).
T h e genus Bartonella includes the former Rochaiimaea (25)
and Grahamella (18) genera. T h e spectrum of Bartonella
species that are h u m a n pathogens is still expanding. T h e
isolation of Bartonella elizabeihae from a h u m a n case of
endocarditis (39) suggested a possible rodent reservoir,
mainly of the genus Rattus (47). Similarly, the report of the
isolation of B. vinsonii subsp. arupensis from a cattle rancher
suggests transmission to h u m a n s b y ticks from a p r o b a b l e
rodent reservoir (141).
Epidemiology and biology of the
infection
Humans
Limited data are available regarding the prevalence or
incidence of CSD world-wide. However, several reports o n
seroprevalence of Bartonella antibodies h a v e b e e n published,
mainly from western Europe (Netherlands, Germany, France,
Italy), and m o r e recently from S w e d e n (69), G r e e c e (75),
J a p a n (144) and Australia (50). According to J a c k s o n et al, an
estimated 22,000 to 24,000 h u m a n cases of CSD occurred in
the USA in 1992, 2,000 of w h i c h required hospitalisation
(71). T h e estimated total health cost of CSD was over
US$12 million in 1992. In the Netherlands, the incidence of
CSD was estimated to b e 2,000 cases p e r year (15). In
Connecticut, w h i c h is the only State in the USA w h e r e CSD is
138
a reportable disease (since January 1992), 2 4 6 p e o p l e m e t the
case definition during the p e r i o d 1 9 9 2 - 1 9 9 3 . A prospective
population-based surveillance system reported an average
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
risk for Bartonella
infection found that the overall
seroprevalence was 7 . 1 % (112). Based o n these estimates,
several thousand cases should occur yearly in most countries
of Europe, including France and Germany, w h e r e a h i g h
percentage of cats h a v e b e e n reported to b e infected (32, 67,
124).
Cat-scratch disease occurs in i m m u n o c o m p e t e n t patients of
all ages, although the majority ( 5 5 % - 8 0 % ) are u n d e r twenty
years of age. In o n e study, J a c k s o n et al. reported a higher
p r o p o r t i o n of cases a m o n g children and teenagers than in
adults, with 4 5 % to 5 0 % of the patients b e i n g younger than
15 years o l d (71). However, Sander et al. reported a rather
h i g h seroprevalence in young adults in Germany (126).
Cat-scratch disease is considered to b e the m o s t c o m m o n
cause of chronic, benign adenopathy in children and young
adults; m o r e cases occur in males than females (71). T h e
incidence of the disease varies b y season, with most cases
being s e e n in autumn and winter. Seventy-five percent
(184/246) of the cases in Connecticut h a d d e v e l o p e d
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
a m o n g children u n d e r ten years of age (9.3/100,000) and
decreased with increasing age (66). T h e m e d i a n age of
patients with CSD was fourteen years (range: 1-64 years).
Eleven percent of patients w e r e hospitalised, but there w e r e
n o deaths. Risk factors highly associated with CSD include
owning a cat of less than 12 m o n t h s of age, b e i n g scratched or
bitten b y a kitten, or owning a kitten with fleas (145). Several
studies h a v e b e e n able to directly associate B. henselae
bacteraemia in cats, especially young kittens, with clinical
cases of CSD in h u m a n s , resulting from scratches inflicted b y
these animals (30, 4 2 , 85). Most cases of CSD in h u m a n s are
thought to result from inoculation of infected flea faeces at the
time of the scratch (51). T w o cases of B. henselae w e r e
reported to b e associated with tick bites (99).
Bacillary angiomatosis caused b y B. henselae h a s b e e n
associated mainly with exposure to cats ( 8 2 , 8 3 , 1 3 4 ) . A study
s h o w e d a strong link b e t w e e n the onset of neuropsychological
decline or dementia in HIV-infected p e o p l e and s e r u m
i m m u n o g l o b u l i n M (IgM) antibodies to B. henselae (129). Cat
ownership was associated with neuropsychological decline
and dementia. T h e p r e s e n c e of B. henselae IgM antibodies was
also strongly l i n k e d to cat ownership, particularly if the cat
was acquired less than o n e year b e f o r e the measurement of
antibody values. I m m u n o s u p p r e s s e d patients h a v e also
acquired BA after renal, liver, cardiac or b o n e m a r r o w
transplantation (37). Bartonella henselae h a s b e e n s h o w n to
colonise vascular tissues and to stimulate vasoproliferative
tumour growth. Although the molecular principle of
bacterium-induced neovascularisation (angiogenesis) is still
Rev. sci. tech. Off. int. Epiz., 19 (1)
unclear, evidence of endothelial colonisation, involving
formation, engulfment and u p t a k e of a large bacterial
aggregate h a s b e e n demonstrated (41).
Cats
T h e domestic cat is the m a i n reservoir for the h u m a n
pathogen, B. henselae. Bacteraemia in cats was first reported in
1992, in the cat of a healthy owner, b y Regnery et al. (117). In
northern California, bacteraemia prevalences of 3 9 . 5 %
(81/205) and 4 1 % (25/61) h a v e b e e n reported ( 3 1 , 8 2 ) . Cats
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
significant risk factor (31). T h e r e was n o direct correlation
b e t w e e n the level of bacteraemia and the antibody litre;
h o w e v e r , cats with serological litres of 5 1 2 or greater w e r e
m o r e likely to b e bacteraemic than cats with a litre of less than
5 1 2 (31). More recently, B. henselae h a s b e e n isolated from
domestic cats from m a n y parts of the world, including E u r o p e
(e.g. the Netherlands [15], France [32, 65, 67] and Germany
[124]), Asia (including J a p a n [105], Indonesia [104], and the
Philippines [34]), Australia (20), N e w Zealand (74) and Africa
( Z i m b a b w e [77]). In m o s t of these studies, bacteraemia
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
the feline population tested was m a d e u p of p e t cats or stray
cats.
In Australia, Flexman et al. reported the first isolation of
B. henselae from the b l o o d and fleas of a cat belonging to a
patient with CSD (49). T h e patient d e v e l o p e d fever, lethargy
and anorexia w h i c h lasted for three days, followed b y the
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
arose three w e e k s after the patient h a d r e m o v e d fleas from his
cat. There was n o history of a bite or a scratch and n o primary
lesion o n the skin. Therefore, this case could also b e o n e of the
first confirmed cases of CSD in h u m a n s transmitted b y fleas.
In Europe, two different types of B. henselae h a v e b e e n
identified b y partial sequencing of the 16S ribosomal
ribonucleic acid (rRNA) gene from cases of CSD in h u m a n s
(13, 14, 4 4 , 128) and from bacteraemic cats (15, 4 4 ) . T h e
serotype 'Marseille' reported in France (44) s e e m s to
correspond to the type II described b y Bergmans et al.
(13, 14, 15; M. Drancourt and D. Raoult, personal
communication). In m o s t of western Europe, B. henselae
type II is m o r e c o m m o n l y found in cats than type I (15, 65,
67, 124). Conversely, in h u m a n cases of CSD in the
Netherlands (14, 15) and Germany (128), B. henselae type I
was identified m o s t frequently, suggesting that this type m a y
b e m o r e infectious for h u m a n s than type II. Distribution of
B. henselae type I and type II in domestic cats in the USA has
not yet b e e n well d o c u m e n t e d . Bartonella henselae type II
appears to b e highly prevalent i n northern California, whereas
B. henselae type II and type I are equally distributed in the cat
population of the East Coast (B.B. C h o m e l , unpublished
data). In the Philippines, n o n e of the cats tested carried
B. henselae type II, suggesting major regional variations in the
prevalence of B. henselae types (34). Isolation of B. clarridgeiae
139
Rev. sci. tech. Off. int. Epiz., 19 (1)
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.
reported a prevalence of 10% in seventy Bartonella isolates
(89). In other regions s u c h as E u r o p e (15, 65, 67), the
Philippines (34) a n d Indonesia (104), B. clarridgeiae accounts
for u p to 3 6 % of Bartonella isolates.
Several serosurveys h a v e also b e e n c o n d u c t e d in cat
populations in the USA. In North Carolina, 2 1 % of 5 1 8 sick
cats w e r e seropositive for B. henselae (21). Childs et al.
reported a prevalence of 2 8 . 2 % (370/1,314) from cats in
various parts of the USA (29), and 14.7% in cats from
Baltimore, Maryland (28). Similarly, a s e r o e p i d e m i o l o g i e
survey of cats from all over North America identified an
overall prevalence of 2 8 % ( 1 7 5 / 6 2 8 ) , with a l o w range of
3.7% to 6.7% i n the Midwest and Great Plains region, to an
upper range of 6 0 % in the south-east (72). High
seroprevalence a p p e a r e d to b e correlated with w a r m , h u m i d
climates. T h e s e w a r m , h u m i d areas with the largest
seroprevalence w e r e also those likely to h a v e the largest
n u m b e r of potential a r t h r o p o d vectors, including fleas. In
Hawaii, of thirty-one kittens involved in h u m a n cases of CSD,
twenty-one ( 6 8 % ) h a d positive b l o o d culture and elevated
antibody titres to B. henselae (42). Only o n e (4%) out of
twenty-three adult cats h a d a positive culture, although
eighteen (78%) h a d elevated antibody litres. In a cluster of
CSD e n c e p h a l o p a t h y in south Florida, 2 2 % of the 124 cats
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
prevalence in e l e v e n catteries from all over the USA was
35.8%, with six catteries having a l o w prevalence ( b e t w e e n
8.3% and 3 7 . 5 % ) and five catteries showing a h i g h prevalence
(above 6 5 % ) (52). Flea infestation was the m o s t important
risk factor for h i g h B. henselae seroprevalence.
Information o n the prevalence of B. henselae antibodies in cats
from various parts of the w o r l d is also increasing rapidly.
Bartonella henselae antibodies h a v e b e e n found i n d o m e s t i c
cats in m o s t countries of Europe, in addition to Israel (40%)
(8), Egypt ( 1 1 % ) (29), southern Africa (South Africa [21%]
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
bacteraemia (up to 1 0 c o l o n y forming units p e r ml) within
two to three w e e k s and usually clear their infection within two
to three m o n t h s ( 3 3 , 59, 6 1 , 1 2 0 ) . In s o m e cases, bacteraemia
can last for several m o n t h s and relapses of bacteraemia at
levels m u c h l o w e r than during the initial infection can b e
observed ( 1 , 5 3 , 6 1 , 87, 90, 9 1 ) . Cyclical bacteraemia was
demonstrated, with the level of bacteraemia fluctuating b y as
m u c h as 100-fold, and intermittent negative cultures. This
suggests that a p r o p o r t i o n of infected cats m a y carry the
infection for years. Long-lasting bacteraemia in cats was
suggested b y K o e h l e r et al. (82) a n d was well demonstrated
by K o r d i c k et al. (85, 90, 9 1 ) . Co-infection of cats w i t h
B. henselae and B. clarridgeiae strains h a s b e e n reported (15,
6
64). Furthermore, l a c k of cross-protection b e t w e e n Bartonella
species
or
B. henselae
types
was
o b s e r v e d in
experimentally-infected and heterologously challenged cats
(143).
Transmission from cat to h u m a n is p r e s u m e d to occur
predominantly b y cat scratch, b u t flea-bite transmission c o u l d
also b e possible. For experimental infection of cats, the
intradermal and intravenous routes are highly effective ( 1 , 5 1 ,
6 2 , 8 5 , 1 1 3 ) . Experimental infection of o n e - to t w o - w e e k - o l d
kittens b y the oral route h a s also b e e n reported (63). In an
arthropod-free environment, neither direct horizontal
transmission from cat to cat, n o r vertical transmission from
infected q u e e n s to offspring appear to occur ( 1 , 62). Zangwill
et al. (145) and K o e h l e r et al. (82) suggested that fleas m a y
play a role i n the transmission of the infection, as p r e s e n c e of
B. henselae DNA was demonstrated b y PCR in fleas c o m b e d
from bacteraemic cats (82). Higgins et al. demonstrated that
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
b l o o d m e a l (68). Cat fleas (Ctenocephalides felis), transferred
from B. henselae
bacteraemic cats to five specificpathogen-free (SPF) kittens, w e r e c a p a b l e of transmitting the
infection to all the SPF kittens (33). In an elegant experiment,
Foil et al. w e r e able to infect cats b y intradermal injection of
flea faeces from fleas fed o n bacteraemic cats for four days
(51).
Dogs
Infection of h u m a n s following contact with d o g s h a s also b e e n
reported. In o n e study, 9 5 % of patients h a d a history of
contact with cats and 4 % h a d a history of contact with d o g s
(102). However, a large-scale study of 1,200 cases reported
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
limited n u m b e r of seropositive d o g s h a v e b e e n reported, but
n o bacteraemic d o g s (42). A recent report from J a p a n of a
possible case of CSD caused b y contact with a d o g suggests
that d o g s c o u l d play a role in h u m a n B. henselae infection
(136). However, s u c h conclusions n e e d further confirmation.
Clinical signs
Humans
One to three w e e k s elapse b e t w e e n the scratch or bite and the
appearance of clinical signs ( 5 6 , 1 0 2 ) . B e t w e e n 6 0 % and 9 3 %
of patients with CSD d e v e l o p a small skin lesion (3 m m to
5 m m ) , often resembling an insect bite, at the inoculation site
(usually the h a n d or forearm). This lesion appears three to ten
days after the scratch o r bite. T h e cutaneous lesion evolves
from a vesicle to a pustule, and finally to a papule, or m o r e
frequently from a macule to a p a p u l e (102). T h e lesions
resolve within a few days to several w e e k s . Inoculation lesions
are nonpruritic and heal without scar formation.
Lymphadenitis is generally unilateral and c o m m o n l y appears
i n the epitrochlear, axillary or cervical l y m p h n o d e s (25). In
140
the study in Connecticut, it was found that younger CSD
patients (less than 15 years old) w e r e m o r e likely to present
with cervical a d e n o p a t h y (66). Older patients (15 years old,
or m o r e ) w e r e m o r e likely to present with inguinal
adenopathy and axillary adenopathy. T h e l y m p h a d e n o p a t h y
develops approximately three w e e k s after exposure. Swelling
of the l y m p h n o d e is usually painful and persists for several
w e e k s to several m o n t h s . In 15% of the cases, suppuration
occurs (102). Approximately half of patients s h o w signs of
systemic infection, including fever, chills, malaise, anorexia
and h e a d a c h e s . Less often, sore throat, rashes, conjunctivitis
or e v e n arthralgia h a v e b e e n reported. In general, the disease
is benign and heals spontaneously without sequelae.
Atypical s y m p t o m s of CSD occur in 5% to 2 5 % of cases. T h e
m o s t c o m m o n of these is Parinauds oculoglandular
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
conjunctivitis),
but
tonsillitis,
myelitis,
meningitis,
encephalitis, status epilepticus, osteolytic lesions and
thrombocytopenic purpura m a y also occur. Encephalopathy
is o n e of the m o s t serious complications of CSD, usually
occurring two to six w e e k s after the onset of
lymphadenopathy. However, patients usually m a k e c o m p l e t e
recovery with a few or n o sequelae. A cluster of five cases of
children with acute encephalopathy associated with CSD was
reported in south Florida (111). Bartonella henselae infection
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
clinical presentations, s u c h as neuroretinitis and bacteraemia
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).
Cases of pleural effusion, p n e u m o n i a , and granulomatous
hepatitis and splenitis h a v e also b e e n reported (10). One case
of paronychia was associated with a B. henselae infection in a
w o m a n bitten b y a cat (125).
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
is rather different. Also called epithelioid angiomatosis, BA is a
vascular proliferative disease of the skin, characterised b y
multiple, blood-filled, cystic n o d u l e s . Infection is usually
characterised b y violet-coloured or colourless papular and
nodular skin lesions that m a y clinically suggest Kaposi's
sarcoma,
but
histologically
resemble
epithelioid
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
involved, the condition is referred to as bacillary peliosis
hepatis, splenic peliosis, or systemic BA. Koehler et al.
demonstrated the strong association b e t w e e n peliosis hepatis
and B. henselae infection (83). Fever, weight loss, malaise and
enlargement of affected organs m a y d e v e l o p in patients with
disseminated BA.
Cats
No major clinical signs of CSD h a v e b e e n reported in cats
under natural conditions. Suspicions of l y m p h a d e n o p a t h y
caused b y a CSD-like organism identified b y silver-stained
section h a v e b e e n reported (78), and m o r e recently, uveitis
was associated with Bartonella infection (92).
Rev. sci. tech. Off. int. Epiz., 19 (1)
In experimentally infected cats, s o m e research groups found
n o clinical signs ( 1 , 120), w h e r e a s others reported fever,
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 .
K o r d i c k and Breitschwerdt reported self-limiting febrile
illness of 4 8 h to 7 2 h duration in six of eight cats, m o d e r a t e
l y m p h a d e n o p a t h y i n all eight cats and transient neurologic
dysfunction in two cats after experimental infection with
B. henselae b y b l o o d transfusion (87). Guptill et al. (61) also
reported m i l d clinical signs, w h i c h included m i l d fever and
anorexia in experimentally infected cats. More recently,
O'Reilly et al. (113) reported fever, lethargia, anorexia and
cutaneous lesions at the inoculation site associated with
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
B. henselae type I isolate, suggesting variability i n the
pathogenicity of Bartonella strains (B.B. C h o m e l , unpublished
data). A statistical association b e t w e e n presence of B. henselae
antibodies and stomatitis and k i d n e y and urinary tract
infections was o b s e r v e d in a large serosurvey of cats in
Switzerland ( 5 8 ) . U e n o et al. also reported a n association
b e t w e e n B. henselae seropositivity and gingivitis and
l y m p h a d e n o p a t h y (138). Reproductive disorders (lack of
pregnancy or pregnancy only after repeated breedings) h a v e
b e e n o b s e r v e d in experimentally-infected q u e e n s (62).
Similar reproductive disorders w e r e e x p e r i e n c e d during a trial
o n experimental transmission b e t w e e n a bacteraemic q u e e n
and a non-bacteraemic m a l e (1); stillbirth was o b s e r v e d
a m o n g the kittens b o m of bacteraemic queens.
Cat-scratch disease infection is very c o m m o n in cats,
especially i n y o u n g kittens. Bacteraemia usually lasts from a
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
reported to b e intra-erythrocytic (84) and pili m a y b e a
pathogenic determinant for Bartonella species (12).
Dogs
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
tested w e r e B. henselae bacteraemic, a n d a very small
percentage 6.4% (2 out of 3 1 dogs) h a d seroconverted (42).
Experimental inoculation of B. henselae b y the intra-dermal
route did not result in a bacteraemic p h a s e , although the d o g s
seroconverted after a few w e e k s (35). Breitschwerdt et al. (22)
and K o r d i c k et al. (86) reported the isolation of B. vinsonii
subsp. berkhoffii in a case of endocarditis in a d o g . An
epidemiological study of 1,920 d o g s f r o m N o r t h Carolina and
Virginia revealed a seroprevalence of 3.6%. Seropositive d o g s
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
history of heavy exposure to ticks (114).
Diagnosis
Humans
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
clinical criteria, exposure to a cat, failure to isolate other
bacteria, and/or histological examination of b i o p s i e s of l y m p h
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).
141
Rev. sci. tech. Off. int. Epiz., 19 (1)
However, the antigen p r e p a r e d from pasteurised exudate
from l y m p h n o d e s of patients with CSD was not standardised
and concerns w e r e raised about the safety of s u c h a product.
Since the identification of B. henselae as the m a i n aetiological
agent of CSD, serological tests, s u c h as the IFA ( 3 8 , 1 1 8 , 1 4 6 )
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
well as techniques to isolate the organism from h u m a n and cat
specimens h a v e b e e n d e v e l o p e d (82, 116). Because
B. henselae is an intra-erythrocytic bacterium (84), cell lysis
using a lysis centrifugation technique or freezing-thawing,
greatly facilitates bacterial isolation from the b l o o d of
bacteraemic patients. T h e technique is appropriate for
isolation of B. quintana from BA cases or chronic carriers (95),
however there are still difficulties in isolating B. henselae from
h u m a n patients, including p e o p l e with BA. Isolation of
B. henselae from the b l o o d of patients with classical CSD is
rarely successful. In s u c h cases, DNA extraction from suspect
l y m p h n o d e s and PCR amplification of the citrate syntheses or
16S rRNA genes will allow identification of the organism (5,
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
to detect anti-Bartonella IgM or IgG. G o o d sensitivity and
specificity was reported for B. henselae in suspected cases of
CSD b o t h in the USA and Europe (3, 13, 3 8 , 1 3 3 ) . However,
the correct source of Bartonella antigen must b e u s e d to
reduce false negative results, as reported with serotype
'Marseille' (44), or in a series of s u s p e c t e d CSD cases (46). In
terms of specificity, cross-reactions h a v e b e e n o b s e r v e d
b e t w e e n B. henselae and Coxiella burnetii (93). It is also
important to n o t e that AIDS patients suffering from BA or
peliosis hepatis are often seronegative for
Bartonella
antibodies ( 1 1 5 ) .
Cats
In cats, w h e r e bacteraemia is c o m m o n , isolation of feline
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
of b l o o d is d r a w n into lysis-centrifugation tubes (82), or
plastic ethylenediamine tetra-acetic acid (EDTA) tubes. T h e
tubes are k e p t frozen for a few days to a few w e e k s at - 3 0 ° C ,
or preferably at - 7 0 ° C (24). Brenner et al. demonstrated that
collection of cat b l o o d in EDTA tubes and subsequent freezing
improves the sensitivity of detection of B. henselae (24). T h e
tubes are centrifuged and the pellet spread onto heart infusion
agar plates containing 5% fresh rabbit b l o o d . T h e s e plates are
maintained at 35°C in a h i g h humidity c h a m b e r with 5% C 0
for three or four w e e k s . Colonies usually d e v e l o p in a few days
from cat b l o o d , although s o m e strains m a y require a few
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
or m o r e b e f o r e appearing o n agar plates. Furthermore,
B. koehlerae requires c h o c o l a t e agar plates, since it d o e s not
replicate o n fresh rabbit b l o o d m e d i u m for primary isolation
(45). Identification of isolates of B. henselae, B. clarridgeiae or
B. koehlerae is confirmed b y DNA amplification using PCRrestriction fragment length p o l y m o r p h i s m (PCR-RFLP)
2
analysis using different restriction endonucleases or partial
sequencing of the 16S rRNA or citrate syntheses genes (15,
3 1 , 8 2 , 8 7 ) . A c o m m e r c i a l PCR test for detecting B. henselae
bacteraemia in cats directly from the b l o o d is n o w available in
the USA (135).
Serodiagnosis of Bartonella infection in cats b y IFA or ELISA is
of limited interest, as a large percentage of the cat p o p u l a t i o n
h a r b o u r anti-Bartonella antibodies. However, testing s h o u l d
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
their cat c o l o n y and for cat owners w h o m a y b e
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
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
epidemiological information is required to determine the
prevalence of B. koehlerae a n d the necessity for a systematic
screening against this species. In contrast to the results in
h u m a n s (44, 115), all the cats that w e r e experimentallyinfected with either B. henselae type I or type II, and that w e r e
tested, w e r e seropositive for b o t h type I a n d type II
(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).
Treatment
Humans
Antimicrobial treatment is indicated for patients with BA,
bacillary peliosis or relapsing bacteraemia. Treatment with
erythromycin (2 g p e r day p e r o s ) , rifampin, or doxycycline
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
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
relapses can occur (119). In case of peliosis hepatis, treatment
b y the parenteral route is initially necessary (81).
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
administration (101). A retrospective study of 2 0 2 CSD
patients demonstrated that the m o s t effective antibiotics w e r e
rifampin,
ciprofloxacin, trimethoprim-sulphamethoxazole,
and gentamicin, but that a m i n i m u m of four w e e k s of
treatment was required (101). More recently, treatment of
typical CSD patients with oral azithromycin for five days
afforded significant clinical benefit as m e a s u r e d b y total
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
treatment ( 1 1 , 27). Intravenous administration of gentamicin
and doxycycline and oral administration of erythromycin
h a v e b e e n u s e d successfully i n the treatment of disseminated
CSD (60, 107). According to W o n g et al, therapy with
doxycycline and rifampin appears to b e helpful in the
treatment of patients with neuroretinitis (142).
Cats
Attempts to clear Bartonella bacteraemia in cats using
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
disappointing. Greene et al. reported that antibiotic treatment
with doxycycline for o n e w e e k was effective in suppressing
bacteraemia in all eight cats u n d e r study, but was effective in
clearing infection from only four cats (59). H o w e v e r , this
Rev. sci. tech. Off. int. Epiz., 19 (1)
142
uncontrolled observation h a s not b e e n corroborated. Regnery
et al. reported that antibiotic therapy was incompletely
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
bacteraemia, but the duration of bacteraemia remained similar
to that of untreated cats (120). Furthermore, K o r d i c k et al.
tested the efficacy of enrofloxacin and doxycycline for the
treatment of B. henselae and B. clarridgeiae infection in cats
(89). Bacteraemia was not eliminated from all the cats treated
and a long treatment was required to eliminate infection. T h e
authors stated that they would reserve r e c o m m e n d a t i o n for
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
individual or as an alternative to euthanasia of a pet'.
Prevention
Cat ownership h a s b e e n increasing i n m o s t industrialised
countries over the 1980s and 1990s, and n o w surpasses d o g
ownership. A large reservoir of B. henselae exists a m o n g the
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
(B.B. C h o m e l , unpublished data) or the 2 million pet cats in
the Netherlands, of w h i c h 4 0 0 , 0 0 0 (22%) are estimated to b e
bacteraemic (15). As the possibility of B. henselae infection
b e c o m e s m o r e widely recognised, there is likely to b e negative
publicity about the perceived hazards of cat ownership,
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
can b e very comforting to the chronically and terminally ill.
Selecting an appropriate c o m p a n i o n animal is important.
Seronegative cats are m o r e likely not to b e bacteraemic and to
b e safe for ownership, h o w e v e r , 2 % of seronegative cats can
b e bacteraemic (15, 31). Young kittens, especially i m p o u n d e d
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
is n o correlation b e t w e e n seropositivity and bacteraemia.
Bacteraemia can also b e transient, with relapses.
Declawing cats h a s also b e e n suggested, but this w o u l d h a v e
limited value, as infection can b e transmitted from cat to cat
b y fleas (30). Therefore, flea control appears to b e o n e of the
major control measures n e e d e d to prevent cats from
b e c o m i n g infected and infection b e i n g spread from cat to cat.
T h e m o s t effective m e a n s of preventing infection b y
B. henselae are c o m m o n sense, hygiene and, possibly,
changing the behaviour of cat owners themselves. People
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.
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
of h u m a n s , will b e difficult, given the diversity of Bartonella
species and types h a r b o u r e d b y cats, and the l a c k of
cross-protection b e t w e e n species and types (143).
Acknowledgements
T h e author w o u l d like to thank Drs R.C. Abbott, C.-C. Chang,
T.E. Honadel, R.W. Kasten, Y. Kikuchi and K. Y a m a m o t o ,
and the several students, especially C. H e w and A. Ziedins,
w h o h a v e b e e n working over the last six years to understand
the e p i d e m i o l o g y and pathogenesis of CSD in its feline
reservoir and of other Bartonella infections in domestic and
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
N.C. Pedersen from the Center for C o m p a n i o n Animal Health
(CCAH), S c h o o l of Veterinary Medicine, University of
California, Davis. Research h a s b e e n funded through grants
from the CCAH, and Mortal Laboratories.
143
Rev. sci. tech. Off. int. Epiz., 19(1)
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.
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