Disseminated Candida infection syndrome in heroin
addicts-dominance of a single Candida albicans
F. C. ODDS, AMALIA PALACIO-HERNANZ,* J. CUADRAt and J. SANCHtZt
Department of Microbiology, University of L eicester, L eicester L E 7 7RH, *Hospital 7 de Octubre, Madrid,
Spain, and t Departmento de Dermatologia, Hospital General Valhncia, Spain
Summary. Among 21 intravenous heroin abusers with cutaneous and ocular
manifestations of disseminated Candida infection, a single C. albicans strain type
(serotype A, biotype 153/7) was isolated from skin lesions in 14 cases. This suggests
that central contamination of the heroin with C. albicans is less likely to be the source
of infection than an endogenous source, and that one particular strain type is either
better adapted than others to grow in the lemon juice used as a heroin solvent, or
more likely than others to cause the specific pathology seen in these patients.
There is now an extensive literature on a specific
syndrome of disseminated Candida infections in
heroin addicts. The infections are characterised by
several features, of which chorioretinitis and follicular
and nodular skin lesions are the most common,
and associated in some instances with costochondral
arthritis (Barthelemy et al., 1981 ; Dally et al.,
1982; Mellinger et al., 1982; Badillet et al., 1983;
Collignon and Sorrell, 1983; Dally et al., 1983;
Drouhet and Dupont, 1983; Hoy and Speed, 1983;
Mackay, 1983; Tkpies Barba et al., 1983; Cuadra
et al., 1984; Dupont and Drouhet, 1985; Servant et
al., 1985). C. albicans has been isolated almost
invariably from the cutaneous lesions, but rarely
cultured from the blood or vitreous fluid. The
sources of the fungus in these cases remain
uncertain. Although some authors have suggested
that C. albicans may contaminate brown (street)
heroin (Mellinger et al., 1982; Dally et al., 1983),
attempts to culture C. albicans from the heroin
involved have been unsuccessful (Mellinger et al.,
1982; Dally et al., 1983; Dupont and Drouhet,
1985 ; Servant et al., 1985 ; Shankland et al., 1986),
and there is evidence that heroin inhibits the growth
of C. albicans in vitro (Dupont and Drouhet, 1985;
Servant et al., 1985; Shankland et al., 1986). The
lemon juice used by addicts as a heroin solvent has
frequently been postulated as a source (Hoy and
Speed, 1983; Mackay, 1983; Newton-John et al.,
1984; Servant et al., 1985; Shankland et al., 1986),
and Shankland et al. (1986) recovered C. albicans
Received 8 Jul. 1986; revised version accepted 1 Aug. 1986.
from the juice in two plastic lemons submitted by
addicts. Other postulated sources are use of unhygienic
injection techniques (Barthelemy et al., 198 1 ;
Badillet et al., 1983) and the direct spread of C.
albicans from the gut (Dupont and Drouhet, 1985).
So far, no attempt appears to have been made to
establish which biotype or biotypes of C. albicans
have been involved in the heroin-associated infections,
yet if a single biotype was responsible for all
the cases it would be strong evidence in support of
a single central source of infection. We have
therefore undertaken a survey of C. albicans
biotypes from cutaneous lesions in 21 Spanish
patients with heroin-associated Candida infections.
Patients and methods
The study group comprised 18 male and three female
heroin abusers, aged 19-33, who had presented at clinics
in Madrid or Valencia within the last 2 years. The
patients had high fever (not noted in one case only) that
within 2-7 days was followed by the development of skin
changes. All the patients hadnodular or follicular lesions,
or both, affecting the scalp. Males frequently had a
folliculitis of the beard area. In four cases there were
nodular lesions in the pubic area, and one patient had
follicular lesions on the neck, chest and arms. There were
signs of Candida endophthalmitis in 7 of the 21 patients.
Blood cultures for bacteria and fungi gave negative
results in all 21 cases; however, all the patients yielded
high numbers of C. aZbicans in cultures from the skin
276 F. C. ODDS ET AL.
C. albicans biotyping
The C. albicans isolates were biotyped according to the
methods of Odds and Abbott (1980,1983). The biotyping
tests were repeated on three occasions to ensure consistency
of results. From 16 of the patients a single isolate
was tested; from the other five, isolates from at least two
anatomical sites were tested.
A control group of 45 C. albicans isolates was obtained
from the same Madrid clinic that was attended by 12 of
the patients with the heroin-associated Candida infection.
Clearly, these control isolates could not be obtained from
lesions similar to those of the heroin addicts; 43 were
from patients with Candida vulvovaginitis, one each from
skin and nail lesions.
Fourteen (67%) of the 21 patients with heroinassociated
disease were infected with C. albicans
biotype 153/7.T he other seven were types 075, 135,
137, 175, 253, 557 and one indeterminate type. All
the isolates were serotype A and all could use citrate
as a carbon source. In the three cases where isolates
were obtained from different anatomical sites, all
the isolates were type 153/7. The prevalence of
biotype 153/7, serotype A strains in the control
isolates was 11.1% (5 out of 45). Thirteen (28.9%)
of the control isolates were serotype B; these did
not include any examples of biotype 1 53/7.
These results indicate a greatly heightened
prevalence of C. albicans biotype 15 /7 in patients
with heroin-associated Candida infection that may
be accounted for in two ways. First, the source of
the fungus could be the heroin itself or its acid
solvent; second, type 153/7, serotype A, whatever
its source, may have a higher predilection for
causing infection than other biotypes of C. albicans.
If the heroin were the source, it is difficult to
understand why some of the isolates were not
biotype 153/7. The idea of contamination of the
lemon juice solvent, either for individuals injecting
their heroin alone or for small groups sharing lemon
Badillet G, Pietrini P, Puissant A 1983 Pustuloses chez des
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Burnie J P, Odds F C, Lee W, Webster C, Williams J D 1985
juice, is entirely compatible with our results and
with the observations that C. albicans grows well in
fresh lemon juice (Newton-John et al., 1984) and
can sometimes be recovered from lemon juice used
by addicts (Shankland et al., 1986). It is notable
that all the isolates from the addicts gave positive
results in the citrate biotyping test, indicating their
ability to grow on citrate at a low pH value (Odds
and Abbott, 1980).
C. albicans type 153/7 is closely related to a type
(0/155/7p)r eviously found to be responsible for an
outbreak of systemic Candida infection in a hospital
intensive care unit and to possess an enhanced
ability to adhere to epithelial cells (Burnie et al.,
1985). Its isolation in the majority of cases of the
Candida-heroin addiction syndrome is, therefore,
compatible with the possibility of endogenous
infection of the addicts. C. albicans is a ubiquitous
member of the normal human microflora, and it is
evident from the control isolates in this study that
type 153/7 is a common biotype amongst vaginal
isolates. A previous survey showed that the frequencies
of different C. albicans biotypes are similar
regardless of their anatomical site of isolation, and
that types 153 and 157 belong to the most numerous
group of C. albicans biotypes (Odds et al., 1983).
The 1 1 % prevalence of type 1 53/7 in vaginal isolates
is, therefore, likely to indicate the normal prevalence
of this type in other sites, including the gutnormally
held to be the major human reservoir of
In the absence of prospectively gathered data
concerning Candida colonisation of heroin addicts
with and without the systemic Candida infection
syndrome we conclude that candidaemia may be a
common sequel to intravenous heroin usage, either
directly or indirectly (via lemon juice) from a
reservoir, presumably endogenous to the user(s)
and that C. albicans serotype A, biotype 153/7 is
more likely to be involved in invasive disease in
addicts than are other strain types of the fungus.
We thank Miss B. K. Gill for technical assistance. This work
was supported by a grant from the Wellcome Trust.
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