Burnham, Carey-Ann D

George, Ige A

Hamad, Yasir

Yarbrough, Melanie L

English

Melanie L. Yarbrough

Yasir Hamad

Carey-Ann D. Burnham

Ige A. George

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Journal of Clinical Microbiology

The Brief Case: Bacteremia and Vertebral Osteomyelitis Due to Staphylococcus schleiferi

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Washington University School of MedicineDigital Commons@BeckerOpen Access Publications2017The Brief Case: Bacteremia and vertebralosteomyelitis due to Staphylococcus schleiferiMelanie L. YarbroughWashington University School of Medicine in St. LouisYasir HamadWashington University School of Medicine in St. LouisCarey-Ann D. BurnhamWashington University School of Medicine in St. LouisIge A. GeorgeWashington University School of Medicine in St. LouisFollow this and additional works at: https://digitalcommons.wustl.edu/open_access_pubsThis Open Access Publication is brought to you for free and open access by Digital Commons@Becker. It has been accepted for inclusion in OpenAccess Publications by an authorized administrator of Digital Commons@Becker. For more information, please contact engeszer@wustl.edu.Recommended CitationYarbrough, Melanie L.; Hamad, Yasir; Burnham, Carey-Ann D.; and George, Ige A., ,"The Brief Case: Bacteremia and vertebralosteomyelitis due to Staphylococcus schleiferi." Journal of Clinical Microbiology.55,11. 3157-3161. (2017).https://digitalcommons.wustl.edu/open_access_pubs/6304The Brief Case: Bacteremia and VertebralOsteomyelitis Due to StaphylococcusschleiferiMelanie L. Yarbrough,a Yasir Hamad,b Carey-Ann D. Burnham,a Ige A. GeorgebDepartment of Pathology & Immunology, Division of Laboratory and Genomic Medicine, WashingtonUniversity School of Medicine, St. Louis, Missouri, USAa; Department of Medicine, Division of InfectiousDiseases, Washington University School of Medicine, St. Louis, Missouri, USAbKEYWORDS Staphylococcus schleiferi, osteomyelitis, zoonotic infectionsCASEA60-year-old female was admitted to a hospital in Missouri with back pain andpathological fractures of multiple thoracic vertebrae. Four months prior to presen-tation, the patient began experiencing low back pain without inciting trauma. Over thenext 2 months, the pain continued to worsen and she experienced a 20-lb weight lossand drenching night sweats, prompting her to seek care. During the initial encounter,the patient denied experiencing fevers. She was not immunocompromised and had norisk factors for tuberculosis and no history of recent travel, hospitalization, or invasiveprocedures. Magnetic resonance imaging (MRI) revealed abnormal enhancement andedema involving the T6, T7, and T8 vertebral bodies with associated prevertebral andpostvertebral soft tissue enhancement and edema. A ﬂuoroscopy-guided T7 vertebralbody biopsy revealed acute and chronic osteomyelitis with no evidence of malignancy,prompting an infectious disease consult.Two sets of blood cultures (VersaTREK REDOX 1 and REDOX 2 media per set) wereobtained, and they signaled positive on the blood culture instrument (VersaTREK;Thermo Fisher Scientiﬁc). The aerobic bottles from both sets yielded Gram-positivecocci in clusters that were identiﬁed as Staphylococcus species by the VERIGENEGram-Positive Blood Culture Test (BC-GP) (Nanosphere/Luminex). Anaerobic mediumbottles remained negative. Subculture to sheep blood agar revealed beta-hemolyticcolonies that were subsequently identiﬁed as Staphylococcus schleiferi by matrix-assisted laser desorption ionization–time of ﬂight (MALDI-TOF) mass spectrometry (MS)with an acceptable species-level score of 2.151 (Bruker Biotyper, Reference Database5.0; Bruker Daltonics, Billerica, MA).A specimen from the T7 vertebral bone biopsy was sent for culture. Gram stainingof the specimen revealed rare polymorphonuclear leukocytes, and no organisms wereseen. Aerobic media (sheep blood agar, chocolate agar, and MacConkey agar) wereheld for 3 days, and anaerobic media (brucella blood agar, laked blood kanamycinvancomycin agar, and phenyethyl alcohol agar) were held for 5 days and remainednegative for growth for the duration of incubation. A transesophageal echocardiogramwas negative for vegetations on the heart valves, and the patient was initiated onintravenous (i.v.) vancomycin, which was subsequently narrowed to i.v. ceftriaxoneonce susceptibility testing was available. Two follow-up blood cultures taken 24 h afterthe initiation of antimicrobial therapy were positive for the same microorganism. Thebacteremia was ultimately cleared after another 2 days, and the patient was dischargedhome on i.v. ceftriaxone for 6 weeks. Surveillance blood cultures taken 2 weeks after thecompletion of therapy were negative, and at a subsequent outpatient clinic follow-up at 3months, she reported complete resolution of her back pain and night sweats. Follow-upimaging of her spine revealed stable vertebral fractures with no disease progression.Citation Yarbrough ML, Hamad Y, BurnhamC-AD, George IA. 2017. The Brief Case:Bacteremia and vertebral osteomyelitis dueto Staphylococcus schleiferi. J Clin Microbiol55:3157–3161. https://doi.org/10.1128/JCM.00500-17.Editor Alexander J. McAdam, Boston Children'sHospitalCopyright © 2017 American Society forMicrobiology. All Rights Reserved.Address correspondence to Melanie L.Yarbrough, myarbro@wustl.edu.For answers to the self-assessment questions andtake-home points, see page 3309 in this issue(https://doi.org/10.1128/JCM.00512-17).THE BRIEF CASEcrossmNovember 2017 Volume 55 Issue 11 jcm.asm.org 3157Journal of Clinical Microbiology on November 7, 2017 by Washington University in St. Louishttp://jcm.asm.org/Downloaded from A thorough review of the patient’s social history revealed that she had a petLabrador retriever with a chronic ear infection for the past 8 months. A call to theveterinarian conﬁrmed purulent otitis, and pus from the dog’s ear was obtained forculture, which grew S. schleiferi. The patient recalled cleaning the dog’s ear with herbare hands. She was employed as a housekeeper and had intermittent skin cracks at herﬁngertips due to exposure to chemicals, which we postulated might have been theportal of entry for the microbe.DISCUSSIONSeveral bacteria that cause human infections are associated with dogs, includingPasteurella canis, Capnocytophaga canimorsus, Streptococcus canis, and Staphylococcusintermedius group (SIG). These organisms are often associated with wound infectionsfrom dog bites, as they are common inhabitants of the oral mucosa of dogs. S. schleiferibacteria are thought to be part of the normal skin ﬂora of dogs and are commonlyassociated with canine otitis externa and pyoderma (1). This species is divided into twosubspecies, S. schleiferi subsp. schleiferi and S. schleiferi subsp. coagulans. S. schleiferisubsp. schleiferi is more commonly associated with human infections, including skinand soft tissue infections, device infections, osteomyelitis, and bacteremia (2). Fewcases of human infection caused by S. schleiferi subsp. coagulans have been docu-mented, although wound infections, endocarditis, and device infections have beenreported. Immunosuppression, malignancies, and recent surgical procedures are im-portant comorbidities reported in prior case series and point toward nosocomialacquisition (3). However, the association of S. schleiferi with canine and human infec-tions supports the possibility that transmission from dogs to humans can occur, as islikely in the case presented here.S. schleiferi bacteria are facultatively anaerobic, Gram-positive cocci. Colonies areround and nonpigmented and are beta-hemolytic on sheep blood agar (Fig. 1). Severalbiochemical reactions differentiate S. schleiferi from other Staphylococcus species thatcause human infections. S. schleiferi is characteristically pyrrolidonyl arylamidase (PYR)positive, ornithine decarboxylase negative, alkaline phosphatase positive, and suscep-tible to novobiocin and polymyxin B (4).Identiﬁcation systems vary in their performance characteristics for S. schleiferi iden-tiﬁcation. One study found that 22 isolates of S. schleiferi were identiﬁed 100% of thetime by MALDI-TOF with both the Bruker Biotyper and the Vitek2 system (GP no. 21342;FIG 1 (A and B) S. schleiferi growth on sheep blood agar after 24 h of incubation of the human (A) andcanine (B) isolates. Hemolysis is visible in the smaller image. (C) Christensen’s medium for the detectionof urease production. () and () indicate positive and negative controls, respectively. (D) Latexagglutination (StaphTEX) of the human and canine isolates.The Brief Case Journal of Clinical MicrobiologyNovember 2017 Volume 55 Issue 11 jcm.asm.org 3158 on November 7, 2017 by Washington University in St. Louishttp://jcm.asm.org/Downloaded from bioMérieux) (5). In our case, the Bruker Biotyper MALDI-TOF identiﬁed both the humanand canine isolates to the species level with acceptable scores of 2.143 and 2.245,respectively. Both isolates were also assayed on the Vitek MS and identiﬁed as S.schleiferi with a score of 99.9%. Neither system identiﬁed the isolates to the subspecieslevel. This species is also included in the database of MicroScan systems and the APIStaph biochemical proﬁling system (bioMérieux); however, little is known about theperformance of these systems for the identiﬁcation of S. schleiferi. Notably, identi-ﬁcation systems often recommend additional testing such as sugar fermentation toconﬁrm an identiﬁcation of S. schleiferi.Differentiation of the two subspecies is possible through biochemical testing withthe tube coagulase and urease reactions. S. schleiferi subsp. schleiferi is slide coagulase(clumping factor) positive, tube coagulase (free coagulase) negative, and urease neg-ative, while S. schleiferi subsp. coagulans is negative by slide coagulase testing andpositive by urease and tube coagulase testing. Interestingly, recent genetic analysis ofseveral clinically relevant Staphylococcus species found that, unlike Staphylococcusaureus, S. schleiferi does not possess the coa gene that encodes the staphylocoagulaseprotein. Thus, the coagulase activity of S. schleiferi is likely mediated by other mecha-nisms (6). The patient and canine isolates described in the case presentation exhibitedthe same morphological and biochemical characteristics, further supporting a zoonoticsource for the patient’s infection (Fig. 1). Both isolates were positive by tube coagulaseand for PYR and urease production. Although we did not report the human isolateto the subspecies level, these characteristics supported the idea that both the humanand canine isolates were likely S. schleiferi subsp. coagulans because of the positiveurease and tube coagulase reactions. Latex agglutination testing (StaphTEX; HardyDiagnostics) produced a questionable weakly positive result with both the human andcanine isolates in our case (Fig. 1). Similar to another clumping factor-positive species,Staphylococcus lugdunensis, S. schleiferi lacks protein A and may produce a rough or“stringy” reaction if tested by latex agglutination.Because of the microbiological and pathological characteristics of S. schleiferi, theincidence of infections caused by this organism may be underrecognized and under-reported. Gram-positive cocci in clusters with a positive tube coagulase (S. schleiferisubsp. coagulans) or slide agglutination (S. schleiferi subsp. schleiferi) reaction may bemisidentiﬁed as S. aureus. Unlike S. aureus, S. schleiferi does not acidify maltose,mannitol, or sucrose. In addition, a positive reaction for PYR should raise suspicion thatan isolate is not S. aureus. Coagulase-positive staphylococcal isolates that are PYRpositive ﬁt the description of S. schleiferi subsp. coagulans or SIG. These species can beseparated biochemically by fermentation of sucrose and mannose, which is positive forSIG. Importantly, MALDI-TOF MS can accurately separate S. schleiferi from other coagulase-positive staphylococcal organisms.Beta-lactam resistance mediated by mecA (PBP2a) in staphylococcal isolates is amajor concern in human and veterinary infections. In one study, 57% of the clinicalisolates of S. schleiferi from dogs were methicillin resistant (1). While cefoxitin is used asthe surrogate for methicillin resistance in S. aureus, there is evidence that it is not asensitive predictor of methicillin resistance in S. schleiferi and SIG. Instead, oxacillin diskdiffusion is more effective at predicting methicillin resistance in SIG and S. schleiferi (7).The performance of an alternative method of mecA detection, rapid detection of themecA gene product PBP2a, has been assessed for S. schleiferi. An evaluation of the AlerePBP2a immunochromatographic assay found that it was 100% sensitive and speciﬁc forthe differentiation of mecA-positive and -negative clinical isolates of S. schleiferi subsp.coagulans with mecA PCR as a gold standard (8). The human and canine isolates in ourcase were tested by disk diffusion. Both isolates were pansusceptible to all of theantibiotics tested in our panel, providing supporting evidence that the human andcanine isolates were from the same source (Table 1). While there are no interpretivecriteria for oxacillin disk diffusion, the oxacillin result would be interpreted as suscep-tible when using the SIG criterion of 18 mm as susceptible (Table 1) (9).In summary, S. schleiferi is an uncommon but important cause of human infectionThe Brief Case Journal of Clinical MicrobiologyNovember 2017 Volume 55 Issue 11 jcm.asm.org 3159 on November 7, 2017 by Washington University in St. Louishttp://jcm.asm.org/Downloaded from that may be mistaken for S. aureus or other Staphylococcus species. While MALDI-TOFMS analysis can differentiate most Staphylococcus species, additional biochemicaltesting may be necessary for clinical laboratories that do not use these systems.Differentiation of the species is important, as the presence of mecA is common in S.schleiferi, but methods for detection of methicillin resistance differ between staphylo-coccal species. Last, a thorough history of exposures, including animal contact, isimportant for interpreting microbiological results in a clinical context.SELF-ASSESSMENT QUESTIONS1. What is detected by a tube coagulase test using rabbit plasma?A. Free coagulaseB. Bound coagulaseC. Protein AD. Hemolysin2. A Gram-positive coccus in clusters tests positive for catalase and PYR butnegative for urease and ornithine decarboxylase. What is the most likely identityof this organism?A. S. aureusB. S. schleiferi subsp. schleiferiC. S. schleiferi subsp. coagulansD. S. lugdunensis3. Which of the following methods is a rapid test that could be used to predictmethicillin resistance in S. schleiferi?A. PBP2a testing by immunochromatographic assayB. Ceﬁnase testC. Cefoxitin disk diffusionD. Oxacillin disk diffusionACKNOWLEDGMENTWe thank William Fales (Veterinary Medical Diagnostic Laboratory at the College ofVeterinary Medicine, University of Missouri, Columbia, MO) for providing the canine S.schleiferi isolate for comparison and additional analysis.REFERENCES1. Cain CL, Morris DO, Rankin SC. 2011. Clinical characterization of Staphy-lococcus schleiferi infections and identiﬁcation of risk factors for acquisi-tion of oxacillin-resistant strains in dogs: 225 cases (2003–2009). J Am VetMed Assoc 239:1566–1573. https://doi.org/10.2460/javma.239.12.1566.2. Davis MF, Cain CL, Brazil AM, Rankin SC. 2013. Two coagulase-negativestaphylococci emerging as potential zoonotic pathogens: wolves insheep’s clothing? Front Microbiol 4:123. https://doi.org/10.3389/fmicb.2013.00123.3. Hernández JL, Calvo J, Sota R, Agüero J, García-Palomo JD, Fariñas MC.2001. Clinical and microbiological characteristics of 28 patients withTABLE 1 Antimicrobial susceptibility results of S. schleiferi isolatesAntibioticHuman CanineZone size (mm)or MIC InterpretationZone size (mm)or MIC InterpretationCefoxitin 30 Susceptible 32 SusceptibleOxacillin 23 —a 22 —aErythromycin 27 Susceptible 28 SusceptibleClindamycin 26 Susceptible 27 SusceptibleTrimethoprim-sulfamethoxazole20 Susceptible 19 SusceptibleRifampin 32 Susceptible 32 SusceptibleDoxycycline 29 Susceptible 29 SusceptibleLinezolid 30 Susceptible 31 SusceptibleDaptomycin 0.064b Susceptible 0.064b SusceptibleaNo CLSI disk diffusion breakpoints are available for oxacillin.bEtest MIC (g/ml).The Brief Case Journal of Clinical MicrobiologyNovember 2017 Volume 55 Issue 11 jcm.asm.org 3160 on November 7, 2017 by Washington University in St. Louishttp://jcm.asm.org/Downloaded from Staphylococcus schleiferi infection. Eur J Clin Microbiol Infect Dis 20:153–158. https://doi.org/10.1007/s100960100467.4. Becker K, Skov RL, Von Eiff C. 2015. Staphylococcus,Micrococcus, and othercatalase-positive cocci, p 354–382. In Jorgensen JH, Pfaller MA, Carroll KC,Funke G, Landry ML, Richter SS, Warnock DW (ed), Manual of clinicalmicrobiology, 11th ed, vol 1. ASM Press, Washington, DC.5. Delport JA, Peters G, Diagre D, Lannigan R, John M. 2015. Identiﬁcation ofcoagulase-negative staphylococci by the Bruker MALDI-TOF Biotypercompared to the Vitek 2 and MIS gas liquid chromatography. J BacteriolMycol Open Access 1(1):00003. https://doi.org/10.15406/jbmoa.2015.01.00003.6. Misic AM, Cain CL, Morris DO, Rankin SC, Beiting DP. 2016. Divergentisoprenoid biosynthesis pathways in Staphylococcus species constitutea drug target for treating infections in companion animals. mSphere1:e00258-16. https://doi.org/10.1128/mSphere.00258-16.7. Bemis DA, Jones RD, Hiatt LE, Ofori ED, Rohrbach BW, Frank LA, Kania SA.2006. Comparison of tests to detect oxacillin resistance in Staphylococcusintermedius, Staphylococcus schleiferi, and Staphylococcus aureus isolatesfrom canine hosts. J Clin Microbiol 44:3374–3376. https://doi.org/10.1128/JCM.01336-06.8. Arnold AR, Burnham CA, Ford BA, Lawhon SD, McAllister SK, Lonsway D,Albrecht V, Jerris RC, Rasheed JK, Limbago B, Burd EM, Westblade LF.2016. Evaluation of an immunochromatographic assay for rapid detectionof penicillin-binding protein 2a in human and animal Staphylococcusintermedius group, Staphylococcus lugdunensis, and Staphylococcusschleiferi clinical isolates. J Clin Microbiol 54:745–748. https://doi.org/10.1128/JCM.02869-15.9. CLSI. 2016. Performance standards for antimicrobial susceptibility testing;twenty-sixth informational supplement. CLSI document M100-S26. Clini-cal and Laboratory Standards Institute, Wayne, PA.The Brief Case Journal of Clinical MicrobiologyNovember 2017 Volume 55 Issue 11 jcm.asm.org 3161 on November 7, 2017 by Washington University in St. Louishttp://jcm.asm.org/Downloaded from 

The Brief Case: Bacteremia and vertebral osteomyelitis due to Staphylococcus schleiferi

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The Brief Case: Bacteremia and vertebral osteomyelitis due to Staphylococcus schleiferi

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