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Copyright © 1999, American Society for Microbiology. All Rights Reserved.

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,3ANDJOHN 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 schleiferiis 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-lococcusspecies 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 ofS. schleiferiendocarditis.

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 valve replacement.

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 forS. 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: michael.leung@hcoa.maynick.com.au.

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not identified by Vitek GPI cards, asS. schleiferiis not in that gram-positive database.

A nested PCR using primers specific for theS. 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 Becton Dickinson).

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 toS. schleiferihas been previ-ously reported. The references given were two that reported blood culture isolates ofS. schleiferi. Fleurette et al. (5) briefly mentioned one patient with a single blood culture positive for S. schleiferiand 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 forS. schleiferi; again, the possibility of endocarditis was not mentioned. Ce´lard et al. (1) described four pacemaker infections withS. 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 withS. schleiferibacteremia resulting from pacemaker infec-tion. Endocarditis was not listed as a complication in these patients.

A recent paper described biochemical tests that helped to differentiateS. schleiferisubsp.schleiferiandS. schleiferisubsp. coagulans(18). Only seven differentS. 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.coagulansis tube coagulase and urease positive) and there is only a single report ofS. schleiferi subsp.coagulansbeing isolated from humans (18).

NineS. schleiferiisolates 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 isolates a Geographic origin Source Tube coagulase test result

Human clumping factor Rabbit clumping factor Thermo- nuclease PYR ALP Urease Mannose Maltose ID32 profile Staph-Zym profile Southeastern Queensland Blood culture Neg Pos Neg Pos Pos Pos Neg Neg Neg 26103640 2071-3 Southeastern Queensland Peritoneal dialysate Neg Pos Pos Pos Pos Pos Neg Neg Neg 26113640 2171-3 Melbourne, Victoria Eye swab Neg Pos Pos Pos Pos Pos Neg Neg Neg 26113640 2171-3 Far northern Queensland Blood culture Neg Pos Pos Pos Pos Pos Neg Neg Neg 26112640 2171-3 Far northern Queensland Catheter tip Neg Pos Pos Pos Pos Pos Neg Neg Neg 26102600 2071-3 Sydney, New South Wales Blood culture Neg Pos Pos Pos Neg b Pos Neg Neg Neg 26113240 2171-3 b Northern Queensland Catheter tip Neg Pos Pos Pos Pos Pos Neg Neg Neg 26113640 2171-3 Perth, Western Australia Pacemaker Neg Pos Pos Pos Pos Pos Neg Neg Neg 26112640 2171-3 Perth, Western Australia Blood culture Neg Pos Neg Pos Pos Pos Neg Neg Neg 26112640 2171-3 aNeg, negative; Pos, positive. bPYR positive by the Staph-Zym kit.

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the isolates were tube coagulase negative, clumping factor pos-itive (using human plasma), heat-stable nuclease pospos-itive, 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 were performed.

S. schleiferiandS. lugdunensisare 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 ofS. haemolyticusgave a weak positive ODC reaction although this

phenomenon has been reported previously (16). Three of 37 isolates ofS. epidermidisdid yield a weak positive ODC reac-tion, but allS. epidermidis isolates were clumping factor and PYR negative. We believe that this screening strategy will accurately identifyS. schleiferiandS. lugdunensisand differen-tiate them from other tube coagulase-negative staphylococci.

S. lugdunensishas increasingly been reported in endocardi-tis, characteristically an aggressive form with poor clinical out-come similar to that ofS. aureus rather than the better out-come generally associated with other CoNS species (13, 17). The more aggressive endocarditis associated withS. lugdunen-sishas 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. schleiferiseem to be underrepresented compared to infections caused byS. lugdunensis. Moreover,S. schleiferihas not previ-ously been reported to cause endocarditis.S. schleiferisubsp. schleiferiis 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. schleiferiwas isolated from preaxillary skin in a similar number of patients undergoing pacemaker insertion (3 of 104) (3).

Colony variation was noted in the strain ofS. schleiferiin 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 inS. schleiferi isolates. We reported a similar observation inS. lugdunensis strains and question whether colony variation is also underre-ported inS. schleiferi, although all three of the otherS. schle-iferistrains in our previous report did not show colony varia-tion (13).

S. schleiferiappears 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 ofS. schleiferiendocarditis. 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 thatS. schleiferiwas 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

[image:3.612.52.552.85.191.2]

en-FIG. 1. Screening scheme for the identification of clumping factor (CF)-positive staphylococci. Symbols: NEG *, some strains of S. lugdunensisare clumping factor negative; #, tested by using human plasma; NEG, negative reaction;⫹, positive reaction.

TABLE 2. Key reactions for differentiation ofS. schleiferiandS. lugdunensisfrom other staphylococci

Species isolates testedNo. of

% Positivity

Tube coagulase

Human clumping

factor

Rabbit clumping

factor

Thermo-nuclease PYR ALP ODC Urease Maltose

S. aureus 20 100 100 100 100 0 95 0 95 90

S. schleiferi 9 0 100 78 100 89 100 0 0 0

S. lugdunensis 15 0 87 73 0 100 100 100 81 100

S. haemolyticus 25 0 0 0 NTa 100 0 0 3 96

S. epidermidis 37 0 0 0 NT 0 92 11b 86 100

Other CoNS spp. 40 0 0 0 NT 40 23 0 70 63

aNT, not tested. bWeak reaction.

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hance the identification ofS. schleiferi. We expect more reports of human infections caused byS. schleiferiin the future.

REFERENCES

1.Ce´lard, M., F. Vandenesch, H. Darbas, J. Grando, H. Jean-Pierre, G. Kir-korian, and J. Etienne.1997. Pacemaker infection caused byStaphylococcus

schleiferi, a member of the human preaxillary flora: four case reports. Clin.

Infect. Dis.24:1014–1015.

2.Coombs, G. W., I. D. Kay, J. W. Pearman, and K. J. Christiansen.1997. The role of multiplex mecA/nuc PCR for routine detection of methicillin resis-tance in staphylococci, abstr. 2292, p. 38.InProgramme and abstracts of the 20th International Congress of Chemotherapy. International Congress of Chemotherapy, Sydney, Australia.

3.Da Costa, A., H. Lelie`vre, G. Kirkorian, M. Ce´lard, P. Chevalier, F. Vanden-esch, J. Etienne, and P. Touboul.1998. Role of the preaxillary flora in pacemaker infections. Circulation97:1791–1795.

4.Durack, D. T., A. S. Lukes, D. K. Bright, and The Duke Endocarditis Service.

1994. New criteria for diagnosis of infective endocarditis: utilization of spe-cific echocardiographic findings. Am. J. Med.96:200–209.

5.Fleurette, J., M. Be`s, Y. Brun, J. Freney, F. Forey, M. Coulet, M. E. Reverdy, and J. Etienne.1989. Clinical isolates ofStaphylococcus lugdunensisandS.

schleiferi: bacteriological characteristics and susceptibility to antimicrobial

agents. Res. Microbiol.140:107–118.

6.Freney, J., Y. Brun, M. Bes, H. Meugnier, F. Grimont, P. A. Grimont, C. Nervi, and J. Fleurette.1988.Staphylococcus lugdunensissp. nov. and

Staph-ylococcus schleiferisp. nov., two species from human clinical specimens. Int.

J. Syst. Bacteriol.38:168–172.

7.Jean-Pierre, H., H. Darbas, A. Jean-Roussenq, and G. Boyer.1989. Patho-genicity in two cases ofStaphylococcus schleiferi, a recently described species. J. Clin. Microbiol.27:2110–2111.

8.Kloos, W.1997. Taxonomy and systematics of staphylococci indigenous to humans, p. 113–137.InK. B. Crossley and G. L. Archer (ed.), The staphy-lococci in human disease. Churchill Livingstone, New York, N.Y. 9.Kluytmans, J., H. Berg, P. Steegh, F. Vandenesch, J. Etienne, and A. Van

Belkum.1998. Outbreak ofStaphylococcus schleiferiwound infections: strain characterization by randomly amplified polymorphic DNA analysis, PCR ribotyping, conventional ribotyping, and pulsed-field gel electrophoresis. J. Clin. Microbiol.36:2214–2219.

10. Lachica, R. V., P. D. Hoeprich, and C. Genigeorgis.1972. Metachromatic agar-diffusion microslide technique for detecting staphylococcal nuclease in foods. Appl. Microbiol.23:168–169.

11. Lambe, D. W., K. P. Ferguson, J. L. Keplinger, C. G. Gemmell, and J. H. Kalbfleisch.1991. Pathogenicity ofStaphylococcus lugdunensis,

Staphylococ-cus schleiferiand three other coagulase-negative staphylococci in a mouse

model and possible virulence factors. Can. J. Microbiol.36:455–463. 12. Latorre, M., P. M. Rojo, M. J. Unzaga, and R. Cisterna.1993.Staphylococcus

schleiferi: a new opportunistic pathogen. Clin. Infect. Dis.16:589–590.

13. Leung, M. J., N. Nuttall, T. M. Pryce, G. W. Coombs, and J. W. Pearman.

1998. Colony variation inStaphylococcus lugdunensis. J. Clin. Microbiol.

36:3096–3098.

14. National Committee for Clinical Laboratory Standards.1998. Performance standards for antimicrobial susceptibility testing. Sixth informational supple-ment. NCCLS document M100-S8. National Committee for Clinical Labo-ratory Standards, Villanova, Pa.

15. Nuttall, N.1996. RBH-STAPH: a simple, effective method to identify coag-ulase negative staphylococci of clinical significance, abstr. O-18, p. 67.In

Programme and abstracts of the 8th International Symposium on Staphylo-cocci and Staphylococcal Infections.

16. Schnitzler, N., R. Meilicke, G. Conrads, D. Frank, and G. Haase.1998.

Staphylococcus lugdunensis: report of a case of peritonitis and an

easy-to-perform screening strategy. J. Clin. Microbiol.36:812–813.

17. Vandenesch, F., J. Etienne, M. E. Reverdy, and S. J. Eykyn.1993. Endocar-ditis due toStaphylococcus lugdunensis: report of 11 cases and review. Clin. Infect. Dis.17:871–876.

18. Vandenesch, F., C. Lebeau, M. Bes, G. Lina, B. Lina, T. Greenland, Y. Benito, Y. Brun, J. Fleurette, and J. Etienne. 1994. Clotting activity in

Staphylococcus schleiferisubspecies from human patients. J. Clin. Microbiol.

32:388–392.

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ERRATA

Differentiation of

Campylobacter jejuni

Serotype O19 Strains

from Non-O19 Strains by PCR

NAOAKI MISAWA, BAN MISHU ALLOS,ANDMARTIN J. BLASER

Division of Infectious Diseases, Vanderbilt University School of Medicine, Nashville, Tennessee 37232-2605, and Department of Veterans Affairs Medical Center, Nashville, Tennessee 37212

Volume 36, no. 12, p. 3567–3573, 1998. Page 3568, column 1, line 14 from bottom: “160 pM” should read “160 nM.” Page 3569, column 1, line 5: “80 pM” should read “80 nM.”

Case of

Staphylococcus schleiferi

Endocarditis and a Simple Scheme

To Identify Clumping Factor-Positive Staphylococci

MICHAEL J. LEUNG, NICHALAS NUTTALL, MARGARET MAZUR, TANIA L. TADDEI, MICHAEL MCCOMISH,ANDJOHN W. PEARMAN

Division of Microbiology and Infectious Diseases and Division of Internal Medicine, Royal 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, Australia

Volume 37, no. 10, p. 3353–3356, 1999. Page 3355, Table 2, column 8, row 3: “100” should read “0.”

Figure

TABLE 2. Key reactions for differentiation of S. schleiferi and S. lugdunensis from other staphylococci

References

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