Eur J Clin Microbiol Infect Dis (2001) 20 : 153–158 Q Springer-Verlag 2001

Article

Clinical and Microbiological Characteristics of 28 Patients

with Staphylococcus schleiferi Infection

J.L. Hernández, J. Calvo, R. Sota, J. Agüero, J.D. García-Palomo, M.C. Fariñas

Abstract The aim of this study was to analyse the clinical and microbiological char-
acteristics of a series of patients with infection by Staphylococcus schleiferi. Seventy-
one isolates were recovered from 36 patients between January 1993 and June 1999 at
a tertiary care centre in northern Spain. There were 28 patients with well-docu-
mented clinical data. Infection was more frequent in men (89.3%), and more than
half of the patients had some degree of immunosuppression, mainly malignant
neoplasms. Infection was nosocomial in 22 cases and community-acquired in the
remaining cases. Staphylococcus schleiferi was frequently associated with wound
infections, mainly surgical-site infections, although unusual types of infections were
detected. Infection-related mortality was low. This study highlights the importance
of careful identification of Staphylococcus schleiferi in the clinical microbiology labo-
ratory. Due to the documented association of Staphylococcus schleiferi with clinical
infections in humans, any isolates of this organism should be assumed to be patho-
genic, unless proven otherwise.

Introduction Some species, such as Staphylococcus epidermidis,

Coagulase-negative staphylococci (CNS) constitute the
major component of the normal human microflora,
their ecological niche being skin and mucosal surfaces.
They are among the most frequent microorganisms
recovered from clinical samples and represent one of
the most common contaminants of bacterial cultures.
The pathogenic role of several CNS species has not
been clearly elucidated. In fact, CNS have been consid-
ered historically as harmless commensals or contami-
nants with doubtful clinical significance [1]. However,
during the last two decades, they have clearly emerged
as major human pathogens, especially in hospitalised
patients [2].
J.L. Hernández (Y), J.D. García-Palomo, M.C. Fariñas
Infectious Diseases Unit, Department of Internal Medicine,
Hospital Universitario Marqués de Valdecilla,
University of Cantabria, 39008 Santander, Spain
e-mail: joselhh6teleline.es
Tel.: c34-942-202655
Fax: c34-942-202655
J. Calvo, R. Sota, J. Agüero
Department of Microbiology,
Hospital Universitario Marqués de Valdecilla,
University of Cantabria, Santander, Spain
Staphylococcus saprophyticus, Staphylococcus haemo-
lyticus and Staphylococcus lugdunensis, are more
frequently associated with definite clinical infection [3,
4]. However, distinguishing infection from contamina-
tion represents an important challenge for the clinician.
Staphylococcus schleiferi subsp. schleiferi was described
in 1988 by Freney et al. [5]. Recent studies have
suggested that this microorganism is a member of the
human preaxillary skin flora [1, 6], but it is not known if
carriage is persistent or transient. Since its first descrip-
tion, few data have been published regarding its patho-
genicity, although it has been implicated as the causa-
tive agent of several human infections [7]. In 1990, a
new subspecies, Staphylococcus schleiferi subsp. coagu-
lans, was obtained from the external auditory meatus of
dogs with external otitis [8]. The first description of the
isolation of this microorganism from humans was
reported in 1994 [9].
The unusual presence of Staphylococcus schleiferi in
human flora could explain the low frequency of infec-
tions due to this microorganism. However, we believe
that the real occurrence of these infections is underre-
ported due to the erroneous identification of Staphylo-
coccus schleiferi as Staphylococcus aureus in routine
laboratory testing, because both species produce b-
haemolysin and a heat-stable DNase [1].
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From a microbiological point of view, Staphylococcus
schleiferi subsp. schleiferi is coagulase tube-test nega-
tive and expresses clumping factor (fibrinogen affinity
factor). Conversely, Staphylococcus schleiferi subsp.
coagulans produces coagulase but not clumping factor
[1, 9]. In recent years, the pathogenic role of Staphylo-
coccus schleiferi has been well established, and viru-
lence factors such as production of DNase, lipase,
esterase, protease, b-haemolysin and adherence have
been described [10].
In the present study, we describe the patients from
whom Staphylococcus schleiferi was isolated in clinical
specimens over a 78-month period. The detailed clinical
and microbiological characteristics of 28 culture-posi-
tive patients are presented. This report includes the
largest series of infections due to Staphylococcus schlei-
feri published to date, with some clinical syndromes
never reported in previous studies.
Patients and Methods
Seventy-one isolates from 36 patients were recovered from
January 1993 to June 1999 at the University Hospital Marqués de
Valdecilla, Santander, Spain. This is a 1,100-bed tertiary centre
that serves as the reference hospital for a population of 500,000
and as the first-level hospital for an area including approximately
350,000 inhabitants in northern Spain. The specimens were
submitted to the clinical laboratory of the hospital for routine
bacteriological culture.
Presumptive identification was based on growth and haemolytic
characteristics on Columbia agar with 5% (v/v) sheep blood agar
at 37 7C; catalase production; and latex slide agglutination for
clumping factor, protein A and capsular polysaccharides of
Staphylococcus aureus (Pastorex Staph-Plus; Sanofi Diagnostics
Pasteur, France). Biochemical identification and antibiogram
profiles were performed with MicroScan system panels (Dade
International, USA) according to the procedures recommended
by the manufacturer. The results were read by MicroScan equip-
ment, the Walkaway-96 or the autoScan-4. The resulting
biochemical profiles were expressed as six-digit numbers.
After the first identification of Staphylococcus schleiferi in our
laboratory (January 1996), we changed the diagnostic strategy
when penicillin susceptibility or positive pyrrolidonyl-b-naphthy-
lamide hydrolysis was reported for Staphylococcus aureus isolates
by the MicroScan System. In these cases we read the tests manu-
ally on MicroScan Combo Pos 4I panels, and definitive identifica-
tion was confirmed using additional tests such as coagulase
activity in the tube with rabbit plasma (Difco Laboratories,
USA), production of ornithine decarboxylase in decarboxylase
basal medium with 1% (w/v) L-ornithine dihydrochloride (Difco
Laboratories, USA) and DNase activity on DNase test agar
(Merck Laboratories, Germany). In December 1998, new panels
were introduced in our laboratory (MicroScan Combo Pos 1S),
and Staphylococcus schleiferi was then correctly diagnosed by
new MicroScan system software. A total of 49 isolates from 26
patients were recovered after the first isolation, and four distinct
biochemical profile codes were defined: 307343, 317343, 307341
and 317341. Additionally, a retrospective search was started to
find Staphylococcus schleiferi reported as Staphylococcus aureus,
which showed the mentioned code profiles that had actually fit
with Staphylococcus schleiferi. Using this approach, ten additional
isolates from nine patients were recovered.
The medical records of patients with positive cultures were
reviewed according to a standardised protocol. The following
data were collected for each patient: age, sex, clinical presenta-
tion, acquisition (nosocomial or community-acquired), underlying
conditions, treatment and outcome. Nosocomial infection was
defined according to the Centers for Disease Control and Preven-
tion (CDC) criteria [11]. Infections of surgically implanted
devices were considered of nosocomial origin when diagnosed
during the first year after the procedure [12]. Furthermore, we
analysed the relationship between isolation and infection,
according to the following definitions [13]: definite infection was
defined as symptoms or signs consistent with bacterial infection in
the area in which Staphylococcus schleiferi was isolated, in the
absence of other microorganisms in the clinical samples; probable
infection was defined as infection that was neither definite nor
unlikely; unlikely infection or colonisation was defined as infec-
tion that produced clinical or microbiological data that were
inconclusive due to the absence of clinical manifestations or the
presence of another clinical alternative diagnosis.
Results
Microbiological Findings. Staphylococcus schleiferi was
isolated from a variety of sources, including wound
exudates (18 patients, 50% of total), blood cultures (7
patients, 19.4%), catheter tip (5 patients, 13.8%), ear
exudate (3 patients, 8.3%) and cerebrospinal fluid (2
patients, 5.5%). Other specimens submitted were
pleural fluid, corneal exudate, biliary drainage and
urine (1 patient each).
All isolates were b-haemolytic on blood agar and
showed agglutination with Pastorex Staph-Plus. When
coagulase and DNase activity and production of orni-
thine decarboxylase were tested (January 1996–
December 1998), all of the isolates were negative for
coagulase and ornithine decarboxylase, and positive for
desoxyribonuclease activity. Results of the MicroScan
panels are summarised in Table 1. All isolates except
two were susceptible to all antibiotics present in the
standard panels (Table 2). Two isolates were resistant
to fosfomycin (MIC 1 32 mg/ml), and none of the
isolates produced b-lactamase.
Clinical Features. The main characteristics of the
patients in this series are detailed in Table 3. There
were 28 patients with well-documented clinical data.
Eight (5 with wound infections, 2 with otitis and 1 with
urinary tract infection) were excluded due to incom-
plete chart data.
Twenty-five of the 28 (89.3%) patients with Staphylo-
coccus schleiferi infections were men and three were
women. The mean age was 64 years (range, 19–85
years). Two patients became infected after orthotopic
liver transplantation. Neoplasms were the most
frequent underlying disease (46.4%), especially solid
tumours, followed by cardiovascular and neurological
disorders. Infection was nosocomial in 22 (78.6%) cases
and community-acquired in the remaining. Two-thirds
of patients underwent some type of surgical procedure,