Case of Staphylococcus schleiferi endocarditis and a simple scheme to identify clumping factor-positive staphylococci.
ABSTRACT Staphylococcus schleiferi is a coagulase-negative staphylococcus infrequently reported as a human pathogen. We report a case of prosthetic valve endocarditis attributed to this organism, contrast it to another Staphylococcus species that gives similar clumping factor results (S. lugdunensis), and propose a simple, effective identification scheme for identification of clumping factor-positive staphylococci.
- SourceAvailable from: François Vandenesch[show abstract] [hide abstract]
ABSTRACT: Infection remains a severe complication after pacemaker implantation. The purpose of our prospective study was to evaluate the role of the local bacteriologic flora in its occurrence. Specimens were collected at the site of implantation for culture from the skin and the pocket before and after insertion in a consecutive series of patients who underwent elective permanent pacemaker implantation. Microorganisms isolated both at the time of insertion and of any potentially infective complication were compared by using conventional speciation and ribotyping. There were 103 patients (67 men and 36 women) whose age ranged from 16 to 93 years (mean+/-SD, 67+/-15). At the time of pacemaker implantation, a total of 267 isolates were identified. The majority (85%) were staphylococci. During a mean follow-up of 16.5 months (range, 1 to 24), infection occurred in four patients (3.9%). In two of them, an isolate of Staphylococcus schleiferi was recognized by molecular method as identical to the one previously found in the pacemaker pocket. In one patient, Staphylococcus aureus, an organism that was absent at the time of pacemaker insertion, was isolated. In another patient, a Staphylococcus epidermidis was identified both at the time of pacemaker insertion and when erosion occurred; however, their antibiotic resistance profiles were different. This study strongly supports the hypothesis that pacemaker-related infections are mainly due to local contamination during implantation. S schleiferi appears to play an underestimated role in infectious colonization of implanted biomaterials and should be regarded as an important opportunistic pathogen.Circulation 06/1998; 97(18):1791-5. · 15.20 Impact Factor
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ABSTRACT: Within a 1-year period, six surgical-site infections (SSI) caused by Staphylococcus schleiferi were observed in the department of cardiac surgery of Ignatius Hospital, Breda, The Netherlands. Since outbreaks caused by this species of coagulase-negative staphylococci have not been described before, an extensive environmental survey and a case control study were performed in combination with molecular typing of the causative microorganism in order to identify potential sources of infection. Variability, as detected by four different genotyping methods (random amplification of polymorphic DNA [RAPD], conventional and PCR-mediated ribotyping, and pulsed-field gel electrophoresis [PFGE] of DNA macro restriction fragments), appeared to be limited both among the clinical isolates and among several control strains obtained from various unrelated sources. Among unrelated strains, RAPD and PCR-mediated ribotyping identified two types only, whereas seven different types were identified in a relatively concordant manner by conventional ribotyping and PFGE. The latter two procedures proved to be the most useful tools for tracking the epidemiology of S. schleiferi. Four of the outbreak-related strains were identical by both methods, and two isolates showed limited differences. In the search for a potential source of S. schleiferi infection, two slightly different PFGE types were encountered on several occasions in the nose of a single surgeon. These strains were, however, clearly different from the outbreak type. In contrast, S. schleiferi cultures remained negative for two persons identified on the basis of case control analysis. It was demonstrated that SSI caused by S. schleiferi had a clinical impact for patients comparable to that of a wound infection caused by Staphylococcus aureus. This report describes the first well-documented outbreak of S. schleiferi infection. A source of the outbreak was not detected.Journal of Clinical Microbiology 09/1998; 36(8):2214-9. · 4.07 Impact Factor
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ABSTRACT: Staphylococcus schleiferi is a new species of coagulase-negative staphylococcus first described in April 1988 (J. Freney, Y. Brun, M. Bes, H. Meugnier, F. Grimont, P. A. D. Grimont, C. Nervi, and J. Fleurette, Int. J. Syst. Bacteriol. 38:168-172, 1988). There are few data in the literature on its pathogenicity. We report two cases in which its role as an opportunistic nosocomial appears to be incontestable.Journal of Clinical Microbiology 10/1989; 27(9):2110-1. · 4.07 Impact Factor
JOURNAL OF CLINICAL MICROBIOLOGY,
Copyright © 1999, American Society for Microbiology. All Rights Reserved.
Oct. 1999, p. 3353–3356Vol. 37, No. 10
Case of Staphylococcus schleiferi Endocarditis and a Simple Scheme
To Identify Clumping Factor-Positive Staphylococci
MICHAEL J. LEUNG,1* NICHALAS NUTTALL,2MARGARET MAZUR,3TANIA L. TADDEI,1
MICHAEL MCCOMISH,3AND JOHN W. PEARMAN1
Division of Microbiology and Infectious Diseases1and Division of Internal Medicine,3Royal Perth Hospital, Perth,
Western Australia 6000, and Division of Microbiology, Queensland Health Pathology and Scientific Services,
Royal Brisbane Hospital, Herston 4029, and Gold Coast Hospital, Southport 4215, Queensland,2Australia
Received 14 December 1998/Returned for modification 27 February 1999/Accepted 17 July 1999
Staphylococcus schleiferi is a coagulase-negative staphylococcus infrequently reported as a human pathogen.
We report a case of prosthetic valve endocarditis attributed to this organism, contrast it to another Staphy-
lococcus species that gives similar clumping factor results (S. lugdunensis), and propose a simple, effective
identification scheme for identification of clumping factor-positive staphylococci.
Staphylococcus schleiferi is a recently described (6) coagu-
lase-negative staphylococcus (CoNS) that has rarely been re-
ported in human infections. We report what we believe is the
first described case of S. schleiferi endocarditis.
A 78-year-old man presented with a 2-day history of inter-
mittent rigors, night sweats, urinary and fecal incontinence on
one occasion, and urinary retention at presentation. There was
no history of dysuria, frequent urination, or abdominal pain.
He reported an influenza-like illness with rhinorrhea, cough,
myalgia, and vertigo 3 weeks prior to presentation.
His medical history included a Starr-Edwards mitral valve
replacement for myxomatous valve degeneration and coronary
artery bypass grafting to three vessels 4 years previously,
chronic atrial fibrillation, hypertension, and one transient isch-
emic attack. His regular oral medication included digoxin (250
?g per day [q.d.]), amiodarone (100 mg q.d.), warfarin (2 mg
q.d.), and captopril (50 mg/12 h). He was an ex-smoker.
On examination, he had a temperature of 38.5°C, a heart
rate of 90 to 100 in atrial fibrillation, and a blood pressure of
115/74 mm Hg. The prosthetic valve sounds were normal; no
murmurs or added sounds were heard. The rest of the clinical
examination was unremarkable; in particular, there were no
peripheral signs of endocarditis.
Investigation demonstrated a subtherapeutic international
normalized ratio of 1.2 (recommended therapeutic range, 3.0
to 4.5), and urinalysis was positive for blood. Full blood count,
creatinine, electrolyte, and liver function tests were all within
reference ranges. The chest X-ray was reported as normal. The
C-reactive protein level was 150 mg/liter (normal, ?10 mg/
liter). Despite the lack of clinical signs to support a diagnosis of
endocarditis, the occurrence of fevers in a patient with a mitral
valve prosthesis in situ necessitated antimicrobial therapy. He
was given gentamicin (180 mg, stat) and amoxicillin (1 g/6 h)
intravenously (i.v.). A transthoracic echocardiogram did not
demonstrate any vegetations. Blood cultures yielded staphylo-
cocci after 48 h, and flucloxacillin (1 g/4 h given i.v.) was
substituted for the amoxicillin. A transesophageal echocardio-
gram (TOE) showed a small (5 by 3 by 4 mm) vegetation on the
prosthetic mitral valve, with independent mobility and differ-
ent echodensity. Valve function was normal, and there was no
evidence of paravalvular regurgitation or abscess, so conserva-
tive therapy with antimicrobials was continued in lieu of urgent
All four sets of blood cultures (BacT/Alert FAN; Organon
Teknika Corporation, Durham, N.C.) yielded gram-positive
cocci in clusters that were catalase positive, consistent with
staphylococci. Growth on solid media (chocolate agar [Oxoid
GC agar base with growth supplement; Unipath Ltd., Basing-
stoke, United Kingdom] and horse blood agar) produced col-
ony variation consisting of large and small morphotypes; pure
subcultures of both colonial morphologies also produced col-
ony variation with identical biochemical reactions. The clump-
ing factor (coagulase rabbit plasma with EDTA; BBL Becton
Dickinson, Cockeysville, Md.), STAPH-A-LEX latex aggluti-
nation (Trinity Laboratories Inc., Raleigh, N.C.), and tube
coagulase tests were all negative. The clumping factor test
using human plasma was positive. The isolate produced a heat-
stable nuclease when commercial media were used (10). The
RBH-STAPH system that utilizes Rosco diagnostic tablets, the
Murex PYR (1-pyrrolidonyl-?-naphthylamide) reagent (Murex
Biotech Ltd., Dartford, United Kingdom), and antibiotic sus-
ceptibility testing for identification of staphylococci (15)
showed the isolate to be furazolidone susceptible, to be des-
ferrioxamine resistant, to be novobiocin susceptible, to be PYR
positive, to be beta-hemolytic on horse blood agar after 18 h of
incubation at 37°C, to be polymyxin susceptible, to be resistant
to 0.04 U of bacitracin but susceptible to 10 U of bacitracin, to
exhibit a zone of inhibition greater than 30 mm in diameter
(susceptible) around a fosfomycin tablet, to be ornithine de-
carboxylase (ODC) negative, to be alkaline phosphatase
(ALP) positive, and to be urease negative. These results were
consistent with those for S. schleiferi. The ID32 STAPH iden-
tification system (bioMe ´rieux Vitek Inc., Hazelwood, Mo.)
gave an identification profile of 26112640, consistent with
99.99% certainty of identification as S. schleiferi. The Mi-
croScan WalkAway Rapid Pos Breakpoint 1 Panel (Dade-
Behring, West Sacramento, Calif.) gave an identification pro-
file of 040075762000-110, consistent with 99.9% certainty of
identification as S. schleiferi. The Staph-Zym identification
method (Rosco Diagnostica, Taastrup, Denmark) gave an
identification profile of 2171-3, consistent with unequivocal
identification as S. schleiferi, after additional tests recom-
mended by the manufacturer (acetoin production and lactose
and sucrose fermentation) were performed. The isolate was
* Corresponding author. Present address: Western Diagnostic Pa-
thology, 74 McCoy St., Myaree, WA 6154, Australia. Phone: 61-8-9317
0959. Fax: 61-8-9317 1536. E-mail: firstname.lastname@example.org.
not identified by Vitek GPI cards, as S. schleiferi is not in that
A nested PCR using primers specific for the S. aureus ther-
monuclease gene (nuc) and primers for the gene encoding
penicillin-binding protein 2a and conferring methicillin resis-
tance (mecA) (2) produced no amplicons. Susceptibility testing
using the Kirby-Bauer disc diffusion method (14), the Vitek
GPS-IX card (bioMe ´rieux Vitek Inc.), and the MicroScan
WalkAway Rapid Pos Breakpoint 1 Panel (Dade-Behring)
showed the isolate to be susceptible to benzylpenicillin, oxacil-
lin, ciprofloxacin, rifampin, tetracycline, erythromycin, and
vancomycin. The ?-lactamase tests in the Vitek GPS-IX card
(bioMe ´rieux Vitek Inc.) and the MicroScan panel (Dade-Be-
hring) were negative and were confirmed negative by using
growth at the margin of the zone of inhibition around a 0.5-U
penicillin disk to inoculate a nitrocefin disk (Cefinase; BBL
After confirmation of the isolate’s identity, the patient was
treated with benzylpenicillin (1.8 g/4 h) i.v. and rifampin (300
mg/8 h) orally with cessation of flucloxacillin. Gentamicin (80
mg/8 h) was given i.v. for the first 2 weeks of treatment. He
received benzylpenicillin and rifampin for a total of 6 weeks. A
follow-up TOE showed resolution of the vegetation. The pa-
tient made a complete recovery with a C-reactive protein level
of ?4 mg/liter at follow-up 6 weeks after presentation.
We believe that this case represents the first report of S.
schleiferi endocarditis. Blood samples collected by four sepa-
rate percutaneous venipunctures (eight bottles) all grew the
organism, and TOE evidence was consistent with a vegetation
on the prosthetic mitral valve. These findings fulfilled the Duke
clinical criteria for definite endocarditis (4). A recent paper (9)
suggested that endocarditis due to S. schleiferi has been previ-
ously reported. The references given were two that reported
blood culture isolates of S. schleiferi. Fleurette et al. (5) briefly
mentioned one patient with a single blood culture positive for
S. schleiferi and possible vertebral osteomyelitis; the possibility
of endocarditis was not raised. Jean-Pierre et al. (7) described
a patient with eight blood cultures positive for S. schleiferi;
echocardiography excluded endocarditis, and the probable
source of the organism was extensive venous thrombophlebitis.
At least three other papers have reported the isolation of S.
schleiferi from blood cultures, but none reported associated
endocarditis. Latorre et al. (12) described a patient with three
blood cultures positive for S. schleiferi; again, the possibility of
endocarditis was not mentioned. Ce ´lard et al. (1) described
four pacemaker infections with S. schleiferi, including one in a
patient with six positive blood cultures, without mentioning
endocarditis. Da Costa et al. (3) examined the role of preax-
illary flora in pacemaker infections and described two patients
with S. schleiferi bacteremia resulting from pacemaker infec-
tion. Endocarditis was not listed as a complication in these
A recent paper described biochemical tests that helped to
differentiate S. schleiferi subsp. schleiferi and S. schleiferi subsp.
coagulans (18). Only seven different S. schleiferi strains were
tested, making it difficult to attribute defining characteristics to
individual subspecies, and the isolates were not correlated with
human infections. We did not identify our isolate to the sub-
species level, but it was considered most likely to belong to the
subspecies schleiferi since it was tube coagulase and urease
negative (S. schleiferi subsp. coagulans is tube coagulase and
urease positive) and there is only a single report of S. schleiferi
subsp. coagulans being isolated from humans (18).
Nine S. schleiferi isolates from six distinct geographical re-
gions of Australia were tested for common phenotypic char-
acteristics. This data is presented in Table 1. In summary, all of
TABLE 1. Geographical origins, sites of isolation, and phenotypic characteristics of nine Australian S. schleiferi isolatesa
Far northern Queensland
Far northern Queensland
Sydney, New South Wales
Perth, Western Australia
Perth, Western Australia
aNeg, negative; Pos, positive.
bPYR positive by the Staph-Zym kit.
3354NOTESJ. CLIN. MICROBIOL.
the isolates were tube coagulase negative, clumping factor pos-
itive (using human plasma), heat-stable nuclease positive, ALP
positive, and urease and maltose fermentation negative. Eight
of the nine isolates were PYR positive. All of the isolates could
be definitively identified with the ID32 STAPH (bioMe ´rieux
Vitek Inc.) and RBH-STAPH systems. The Staph-Zym (Rosco
Diagnostica) system gave unequivocal identification of all iso-
lates after additional tests (acetoin production and lactose and
sucrose fermentation) recommended by the manufacturer
S. schleiferi and S. lugdunensis are the only two CoNS species
that frequently give positive clumping factor reactions. We
tested 146 staphylococcal strains with a variety of phenotypic
and biochemical tests (using Rosco diagnostic tablets and the
Murex PYR reagent). Results are presented in Table 2. From
these results, a 4-h screening scheme (Fig. 1) was derived for
the identification of staphylococci that yield positive clumping
factor results (using human plasma). None of 25 strains of S.
haemolyticus gave a weak positive ODC reaction although this
phenomenon has been reported previously (16). Three of 37
isolates of S. epidermidis did yield a weak positive ODC reac-
tion, but all S. epidermidis isolates were clumping factor and
PYR negative. We believe that this screening strategy will
accurately identify S. schleiferi and S. lugdunensis and differen-
tiate them from other tube coagulase-negative staphylococci.
S. lugdunensis has increasingly been reported in endocardi-
tis, characteristically an aggressive form with poor clinical out-
come similar to that of S. aureus rather than the better out-
come generally associated with other CoNS species (13, 17).
The more aggressive endocarditis associated with S. lugdunen-
sis has been attributed to the expression by the organism of
virulence factors similar to those of S. aureus (11). It is of
interest that the same group reported similar virulence factors
in strains of S. schleiferi, yet severe infections caused by S.
schleiferi seem to be underrepresented compared to infections
caused by S. lugdunensis. Moreover, S. schleiferi has not previ-
ously been reported to cause endocarditis. S. schleiferi subsp.
schleiferi is indigenous to carnivores but may be transferred
from carnivore pets to their owners or handlers (8). An earlier
article that reviewed a large number of S. schleiferi isolates
reported that almost all were considered to be part of the skin
flora of some humans (5). One report suggested that the pre-
axillary skin is a preferred site, although prospective cultures
yielded only five strains from 104 patients (1). In a more recent
study, S. schleiferi was isolated from preaxillary skin in a similar
number of patients undergoing pacemaker insertion (3 of 104)
Colony variation was noted in the strain of S. schleiferi in this
report and also in another isolate from a patient at one of our
institutions with an infected pacemaker. The feature of colony
variation has not been previously documented in S. schleiferi
isolates. We reported a similar observation in S. lugdunensis
strains and question whether colony variation is also underre-
ported in S. schleiferi, although all three of the other S. schle-
iferi strains in our previous report did not show colony varia-
S. schleiferi appears to have a propensity to cause infection
associated with implanted foreign material and should be con-
sidered when a CoNS is isolated from implants. We believe
that this is the first report of S. schleiferi endocarditis. Because
S. schleiferi has virulence factors similar to those of S. lug-
dunensis, a CoNS isolated from blood cultures from a patient
with suspected endocarditis needs to be accurately identified.
It is possible that S. schleiferi was previously incorrectly iden-
tified due to overlap of phenotypic characteristics with those of
S. aureus and other CoNS species. Application of a simple
identification method as presented in this report should en-
FIG. 1. Screening scheme for the identification of clumping factor (CF)-
positive staphylococci. Symbols: NEG *, some strains of S. lugdunensis are
clumping factor negative; #, tested by using human plasma; NEG, negative
reaction; ?, positive reaction.
TABLE 2. Key reactions for differentiation of S. schleiferi and S. lugdunensis from other staphylococci
Other CoNS spp.
aNT, not tested.
VOL. 37, 1999NOTES 3355
hance the identification of S. schleiferi. We expect more reports
of human infections caused by S. schleiferi in the future.
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korian, and J. Etienne. 1997. Pacemaker infection caused by Staphylococcus
schleiferi, a member of the human preaxillary flora: four case reports. Clin.
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2. Coombs, G. W., I. D. Kay, J. W. Pearman, and K. J. Christiansen. 1997. The
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3356NOTESJ. CLIN. MICROBIOL.