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Review

Coagulase-Negative Staphylococci

Karsten Becker, Christine Heilmann, Georg Peters
Karsten Becker
Institute of Medical Microbiology, University Hospital Münster, Münster, Germany
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  • For correspondence: kbecker@uni-muenster.de
Christine Heilmann
Institute of Medical Microbiology, University Hospital Münster, Münster, Germany
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Georg Peters
Institute of Medical Microbiology, University Hospital Münster, Münster, Germany
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DOI: 10.1128/CMR.00109-13
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  • FIG 1
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    FIG 1

    Time line of the discovery of the species belonging to the genus Staphylococcus. Coagulase-negative species are shown in blue; coagulase-positive and coagulase-variable species are shown in red (note that only S. schleiferi subsp. coagulans is coagulase positive). Note that at the times of establishment of the first three species designations, S. aureus, S. epidermidis, and S. saprophyticus, these terms comprised a broader content than that accepted today. In particular, S. epidermidis and S. saprophyticus were used to describe nonpathogenic, saprophytic staphylococci (and other Gram-positive cocci occurring in clusters).

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    FIG 2

    Clinical and epidemiological schema of staphylococcal species, based on the categorization of coagulase as a major virulence factor and its resulting impact on human health.

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    FIG 3

    Phylogenetic separation of staphylococcal species and subspecies (ssp.), extended by key diagnostic characteristics as proposed by Lamers et al. (32).

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    FIG 4

    Pathogenesis of catheter-related infections and factors influencing biofilm genesis. The image shows the three-step process of biofilm formation on the surface of an intravascular catheter, with rapid initial adhesion and attachment of CoNS microorganisms to the polymer foreign body surface resulting in a monolayer (1), followed by a prolonged accumulation phase which involves cell proliferation, intercellular adhesion processes, and maturation (2 and 3). (4) Finally, microorganisms may disaggregate from the macrocolony and drift into the bloodstream, resulting in metastatic and embolic complications.

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    FIG 5

    Sections of Columbia blood agar plates showing grayish, hemolytic colonies of S. haemolyticus (the color of this photograph was modified to enhance visibility of the weak hemolysis zones [arrows] surrounding the colonies, resulting in a nonnatural reddish tinge) (A); orange, nonhemolytic colonies of S. chromogenes (B); creamy, nonhemolytic colonies of S. lugdunensis (C); and whitish, nonhemolytic colonies of S. saprophyticus subsp. saprophyticus (D).

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    FIG 6

    Columbia blood agar plate showing an isogenic S. epidermidis strain pair displaying both the normal (arrows) and SCV (dashed arrows) phenotypes. The normal phenotype (NP) on this plate was the result of a spontaneous reversion of the SCV back to the NP.

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    FIG 7

    Highly simplified schema (not true to scale) of the composition of the SCC family integrated into the S. aureus chromosome (blue). Some examples of various SCC types, including those organized in composite islands, are given. Basic structures comprise the mec gene complex (red), the ccr gene complex (yellow), and the joining regions (gray). Some SCCs additionally contain (i) resistance operons acting against antibiotic agents (violet), such as fusidic acid (fusC); (ii) resistance operons for metalloids and transition metals with toxic/bactericidal properties (green), such as arsenic (ars), cadmium (cad), copper (copB and copC), and mercury (mer); (iii) virulence genes (brown), such as the capsule polysaccharide gene (cap1); (iv) other genes (orange), such as the genes composing the arginine catabolic mobile element (arc), the copper-translocating P-type ATPase gene (copA), and the potassium-transporting ATPase genes (kdp); (v) further penicillin-binding protein 4 (PBP4) genes (pink), such as pbp4; and (vi) pseudogenes.

Tables

  • Figures
  • TABLE 1

    Historic and valid designations within the Staphylococcus genus reflecting the early dualism concept of pathogenic versus nonpathogenic staphylococci

    Yr“Pathogenic” species“Nonpathogenic” speciesAuthor of description (reference)
    1884 Staphylococcus (pyogenes) aureus a Staphylococcus (pyogenes) albus b Rosenbach (8)
    1896 Micrococcus pyogenes aureus Micrococcus pyogenes albus Lehmann and Neumann (610)
    1908 Aurococcus aureus c Albococcus epidermidis d Winslow and Winslow (11)
    1916 Staphylococcus aureus Staphylococcus epidermidis Evans (611)
    1940 Staphylococcus pyogenes e Staphylococcus saprophyticus e , f Fairbrother (12)
    1980 Staphylococcus aureus Staphylococcus epidermidis Skerman et al. g (612)
    • ↵a In 1885, a lemon-colored species, designated Staphylococcus (pyogenes) citreus, was described by J. Passet (613).

    • ↵b The pus-derived “albus” variant was probably rather a less or nonpigmented S. aureus isolate, as its pathogenicity was proven by Rosenbach via animal experiments (8). Later on, “S. epidermidis albus” was described by U.S. pathologist W. H. Welch, in 1891, as a colonizer of the human epidermis found also in aseptic wounds (10).

    • ↵c Described as a “parasitic coccus, living normally on the surface of the human or animal body, or in diseased tissues” (11).

    • ↵d Described as a “parasitic coccus, living normally on the surfaces of the human or animal body” (11).

    • ↵e After the introduction of coagulase production as the major principle to differentiate staphylococcal species by Fairbrother (12).

    • ↵f S. saprophyticus was used in a broader sense to designate nonpathogenic coagulase-negative staphylococci.

    • ↵g Still valid definitions of the taxa S. aureus and S. epidermidis, together with other staphylococcal species described until this point, by the Ad Hoc Committee of the Judicial Commission of the ICSB (612).

  • TABLE 2

    Main characteristics of CoNS species

    Species or subspecies a Diagnostic characteristics Site or source of detection b Clinical association (frequency) c
    Colony appearanceNovobiocin resistanceOxidaseEnvironment and/or foodAnimalsHumansFBRIOther
    S. arlettae Yellow or beige+−Textile and tannery industrial effluentsCattle, goats, pigs, poultry, sheep−−BSI (+)
    S. auricularis White−−−−External auditory canal (principle habitat), seldom on other skin regions−BSI in preterm infant (?)
    S. capitis subsp. capitis Chalk white−−−Cats, dogs, horsesPredominantly on the scalp and arms, less frequently on other skin regionsCRBI (+), PVIE (+), CAPD (+), DRBJI (++)BSI in neonates (+)
    S. capitis subsp. urealyticus d White, delayed yellow pigmentation in ∼70% of isolates−−−−Predominantly on skin (mostly from heads, primarily ears and foreheads)CRBI (+), PVIE (+)BSI in neonates (++)
    S. caprae Nonpigmented−−−GoatsSkin, anterior naresCRBI (+), CAPD (+), CFDAI (+), DRBJI (+)UTI (+)
    S. carnosus subsp. carnosus Gray-white−−Fermented food (starter cultures, soy sauce mash)Cattle−−−
    S. carnosus subsp. utilis Cream colored after 48 h−−Fermented food (soy sauce mash, fermented fish) −−−
    S. chromogenes Butyrous, orange, or creamy−−−Cattle, pigs, horses, goats, sheep−−−
    S. cohnii subsp. cohnii Unpigmented or, occasionally, tinted slightly yellowish+−−Dogs, goats, poultrySkinCRBI (++), DRBJI (++)BSI in burn patient (+)
    S. cohnii subsp. urealyticus e Translucent with concentric ring patterns c +−−Apes, clams, monkeys, horsesSkin−BSI (+), infected pressure ulcer (?)
    S. condimenti Cream colored after 48 h−−Fermented food and starter cultures−−−−
    S. devriesei Gray-yellow, yellow. or yellow-orange−−−Cattle−−−
    S. epidermidis Gray or grayish white−−Fermented sausagesCats, cattle, dogs, goats, gorillas, horses, pigs, sheepSkin (preferentially axillae and the head; also arms and legs) and mucous membranes of the nasopharynxCAPD (!), CFDAI (!), DRBJI (!), PVIE (!), and virtually all other kinds of FBRIsBSI in neonates (!)
    S. equorum subsp. equorum White+−Fermented food (starter cultures)Cattle, goats, horses, sheep−DRBJI (+)−
    S. equorum subsp. linens White+−Smear-ripened cheese (starter culture)−−−−
    S. felis Unpigmented−−−Cats, horses−−−
    S. fleurettii Unpigmented or cream colored++Milk cheeseGoats, pigs, small mammals−−−
    S. gallinarum Yellow, yellowish tint, or unpigmented+− Chickens, pheasants−CRBI (+)−
    S. haemolyticus Gray-white, white, or slight yellow tint−−Milk, fermented foodCats, cattle, dogs, horses, goats, pigs, sheepSkin (preferentially legs and arms)CAPD (+++), CFDAI (+++), DRBJI (++)BSI in neonates (+++)
    S. hominis subsp. hominis Dull, gray-white to yellowish or yellow-orange−−Goat milk, fermented foodCats, dogs, goats, pigs, sheepSkin (preferentially axillae, arms, legs, and pubic and inguinal regions)CRBI (++), DRBJI (++)BSI in neonates (+)
    S. hominis subsp. novobiosepticus Butyrous, gray-white−−−−−CRBI (++)BSI in neonates (+)
    S. jettensis Yellow (after prolonged incubation)−−−−−CRBI (+)−
    S. kloosii Opaque+−−Goats−CRBI (+)BSI (+)
    S. lentus Gray-white to white or creamy++Soy bean oil meal, meat, milkClams, goats, horses, mink, pigs, poultry, sheep−CRBI (+)BSI (+), splenic abscess (+)
    S. lugdunensis Cream-white to slightly yellow−−−Cats, chinchillas, dogs, goats, guinea pigsSkin (preferentially lower abdomen and extremities)PVIE (++), CFDAI (+), DRBJI (+)Native valve endocarditis (++), wound infection (++), SSI (++)
    S. massiliensis White−−−−Skin (?)−Brain abscess (+)
    S. microti Opalescent whitish−−−Mice−−−
    S. muscae Butyrous, grayish white−−−Flies (trapped in cattle sheds)−−−
    S. nepalensis White+−Environment (not specified)Goats, pigs, squirrel monkeys, bats (guano), dry-cured ham−−Cystitis (?; recovered from human urine)
    S. pasteuri Mostly yellow, also white−−Fermented sausagesPigs−CAPD (+), DRBJI (+), CRBI (?)BSI (+)
    S. petrasii subsp. croceilyticus Pale creamy yellow−−−−Skin (?; so far only from acoustic meatus)−−
    S. petrasii subsp. petrasii Unpigmented−−−−Skin (?)−BSI (?)
    S. pettenkoferi Mostly white, also yellow−−−−Skin (?)CRBI (++)Wound infection (?), osteomyelitis (+)
    S. piscifermentans Unpigmented, white, yellowish orange−−−Dogs (feces), fermented food and starter cultures−−−
    S. rostri White−−−Pigs, poultry, water buffalo−−−
    S. saccharolyticus f Grayish white−−−GorillasSkin, particularly on the forehead and armPVIE (?)Spondylo-discitis (+), joint infection (?), pneumonia (?)
    S. saprophyticus subsp. bovis Creamy to pale orange, also unpigmented+−−Cattle−−−
    S. saprophyticus subsp. saprophyticus Unpigmented or slight yellow tint+− Horses, goats, sheep, cats, fermented foodSkinCRBI (+)UTI (!), BSI (+), NVIE (+)
    S. schleiferi subsp. schleiferi −−−Dogs, catsSkin (particularly preaxillary)CFDAI (+), CRBI (+), DRBJI (+), PVIE (+)BSI (+), wound infection (+), UTI (?)
    S. sciuri subsp. carnaticus ++−Cattle, dolphinsSkin−BSI (?)
    S. sciuri subsp. rodentium ++−Rodents, whalesSkin−BSI (?)
    S. sciuri subsp. sciuri Gray-white with yellowish or cream-colored tint toward the center, yellowish (rare)++−Cats, cattle, clams, dogs and other carnivores, dolphins, goats, horses, insectivores, marsupials, monkeys, pigs, rodents, whalesSkinCAPD (+), CRBI (+), DRBJI (+)BSI (?), diabetic food infection (?), wound infection (?)
    S. simiae White−−−Squirrel monkeys−−−
    S. simulans Gray-white−−−Cattle, horses, sheepSkin (legs, arms, and heads of children; occasionally in adults)DRBJI (+)−
    S. stepanovicii Unpigmented++−Insectivores, rodents−−−
    S. succinus subsp. casei White+−Fermented foodInsectivores, rodents−−−
    S. succinus subsp. succinus White+−Amber, fermented food (starter cultures)Cattle, insectivores, rodents, songbirdsEye (single report)−BSI (?)
    S. vitulinus Cream to yellow, rarely unpigmented++Fermented foodHorses, poultry−−Hip infection (?)
    S. warneri Gray-white (20%), slightly yellowish colonial center to bright yellow-orange−−Fermented foodDogs, cats, goats, horses, insectivores, monkeys, pigs, prosimians, rodents, sheepSkin (preferentially nares, head, legs, and arms)CAPD (+), DRBJI (++)Septic arthritis (+)
    S. xylosus Orange-yellow, yellowish, or gray to gray-white+−Fermented food (starter cultures)Cats, clams, goats, horses, insectivores, lower primates, rodents, sheepSkin (rare)DRBJI (+)−
    • ↵a Assignment of characteristics, occurrence, and association with infections might be questionable between staphylococcal subspecies, particularly prior to their definition; in those cases, refraining from differentiation down to the subspecies level, the data were assigned to the subspecies bearing the species epithet.

    • ↵b In particular for livestock and animal food products, as well as for companion animals, contamination by the human CoNS microbiota should be considered and, vice versa, observations of primarily animal-associated CoNS species on human skin could be caused by professional and domestic animal contacts.

    • ↵c Abbreviations: BSI, bloodstream infection; CAPD, continuous ambulatory peritoneal dialysis-related infection; CFDAI, cerebrospinal fluid device-associated infection; CRBI, catheter-related bloodstream infection; FBRI, foreign body-related infection; DRBJI, device-related bone and joint infection; NVIE, native valve infectious endocarditis; PVIE, prosthetic valve infectious endocarditis; SSI, skin and soft tissue infection; UTI, urinary tract infection; −, unknown, not described; ?, questionable or unconfirmed; +, single cases; ++, occasional detection; +++, frequent detection; !, most common origin.

    • ↵d For literature search, note that this subspecies was originally described in 1991 as S. capitis subsp. ureolyticus.

    • ↵e For literature search, note that this subspecies was originally described in 1991 as S. cohnii subsp. urealyticum. While strains isolated from humans are usually unpigmented and their colonies have gray and gray-white rings, strains isolated from nonhuman primates are (i) usually pigmented with brilliantly colored colonies, with alternating yellow-orange, gray, gray-white, orange, and gray rings or bands; or (ii) show colonies with a yellow-green tint and only a subtle ring pattern.

    • ↵f For literature search, note that this species, originally described in 1948 as belonging to the Micrococcus genus, was transferred from the Peptococcus genus into the Staphylococcus genus in 1984.

  • TABLE 3

    Species distribution of CoNS in human clinical samples in recent studies (published since 2000)

    ParameterValue or description in study b
    Petinaki et al., 2001 (614)Cuevas et al., 2004 c (615)Sivadon et al., 2005 d (616)Arciola et al., 2006 e (130)Gatermann et al., 2007 (617)Koksal et al., 2009 (618)Jain et al., 2011 f (619)Shin et al., 2011 (91)
    Study design parameters
        CountryGreeceSpainFranceItalyGermanyTurkeyIndiaSouth Korea
        No. of CoNS isolates4503692126014942009851
        Underlying infectionNot specified g Not specified c BJIPJI, surgical wound revisionBSI, CRBIBSICRBICAPD peritonitis
        Method of identificationAPI ID 32 Staph, BBL Crystal GP ID kitSPSP, sodA API Staph, API ID 32 StaphSP, sodA API ID 32 StaphSP16S rRNA, tuf, sodA
    % Identified staphylococci
        S. auricularis 1.0
        S. capitis 3.536.11.91.07.512.23.9
        S. caprae 1.90.31.4 5.9
        S. chromogenes 0.5 0.21.5
        S. cohnii 1.2<1.00.51.21.01.08.2
        S. equorum 0.2
        S. epidermidis 50.05671.236.167.443.523.566.7
        S. haemolyticus 14.852.42.811.911.536.711.8
        S. hominis a 11.1184.23.27.5/1.09.53.0
        S. lentus 2.5
        S. lugdunensis 2.0 2.80.53.09.0
        S. pasteuri 1.90.1 2.0
        S. saprophyticus 5.719 0.10.42.5
        S. schleiferi 0.10.61.0
        S. sciuri 1.2 0.10.6
        S. simulans 2.011.40.11.22.01.0
        S. warneri 4.047.12.11.84.0 7.8
        S. xylosis 4.0<1.0 0.10.85.013.3
    • ↵a If data for subspecies were provided, the percentages are separated by a slash, as follows: S. hominis subsp. hominis/S. hominis subsp. novobiosepticus. Differences from 100% are due to ambiguously and nonidentified isolates.

    • ↵b Differences from 100% are due to ambiguously and nonidentified isolates or nongiven coagulase-positive isolates. Abbreviations: BJI, bone and joint infection; BSI, bloodstream infection; CAPD, continuous ambulatory peritoneal dialysis; CRBI, catheter-related bloodstream infection; IVD, intravenous device; PJI, (peri)prosthetic joint infection; SP, standard procedures (based on the work of Kloos and Schleifer [407] and subsequent modifications and supplementations).

    • ↵c Data are from the fifth study period, carried out in 2002. The most frequent sources of isolation of CoNS were blood (32%), catheter tips (20%), wounds and abscesses (21%), and urine (12%); 8% were represented by other CoNS species.

    • ↵d Data comprise about 60% BJIs related to revision arthroplasty surgery and 40% due to fracture nonunions, contiguous osteitis, and other entities.

    • ↵e Data are percentages of overall prevalence among all 1,490 clinical isolates, including 530 (46.9%) S. aureus isolates.

    • ↵f Data are given for IVD tip examination (see the respective publication for results of examination of blood samples and skin swabs from the site of IVD insertion).

    • ↵g Comprising blood cultures (41.1%), wounds (22%), vascular catheters (11.1%), urine cultures (6.2%), and tissue culture foci (19.6%).

  • TABLE 4

    Species distribution of CoNS b in animal- and food-derived samples in recent studies (published since 2000)

    ParameterValue or description in study a
    Faria et al., 2009 (55)Gillespie et al., 2009 (620)Coton et al., 2010 (621)Hauschild et al., 2010 (622)Leroy et al., 2010 (623)Huber et al., 2011 (624)Waller et al., 2011 (625)
    Study design parameters
        CountryPortugalUSAFrancePolandFranceSwitzerlandSweden
        Animal or food source (no. of samples)Drinking water (172)Cow (618)Food-related samples (431)Free-living insectivores and rodents (NG)Meat products (27)Food-related samples (1,639)Cow (NG)
        Sample originDistribution networkMammary quarter milkFrench cheese, dry sausage typesNGProcessing units (n = 9)Farms (>800)Milk
        No. of isolates242383431197388275 (only MR-CoNS)154
        Identification method16S rRNA gene PCRAPI StaphSeveral PCR and hybridization strategies rpoB and dnaJ PCR-RFLP analysis sodA gene PCRMALDI-TOF MS, sodA gene PCR tuf gene PCR
    % Identified staphylococci
        S. arlettae 0.3 1
        (S. aureus) b 1.5
        S. auricularis 0.5
        S. capitis 1.7 0.2 0.0
        S. carnosus 1.9 3.6
        S. caprae
        S. chromogenes 480.5 24
        S. cohnii 0.00.4
        S. epidermidis 28.5104.44.12.11.422
        S. equorum 28.52.058.2
        S. fleurettii 0.50.50.035.6
        S. gallinarum 1
        S. haemolyticus <14.41.0 2.214
        S. hominis 21.21.00.0
        (S. hyicus) b 26 5
        (S. intermedius) b <1
        S. lentus 2.61.0 10.9<1
        S. lugdunensis 1.2
        S. microti 0.5
        S. pasteuri 65.7 0.22.02.3
        (S. pseudintermedius) b <1
        S. saprophyticus 2.3112.50.511.9 5
        S. sciuri 0.6<11.47.60.348.7
        S. simulans 71.2 18
        S. stepanovicii 18.3
        S. succinus 7.727.9 c 7.7
        S. vitulinus 1.22.52.1
        S. warneri 22.85.60.30.7
        S. xylosus 128.320.811.3 4
    • ↵a Differences from 100% are due to ambiguously and nonidentified isolates or nongiven coagulase-positive isolates. Abbreviations: NG, not given; SP, standard procedures (based on the work of Kloos and Schleifer [407] and subsequent modifications and supplementations).

    • ↵b If part of the study, percentages of coagulase-positive or coagulase-variable species (species names in parentheses) are also given.

    • ↵c Comprises S. succinus subsp. succinus (9%) and S. succinus subsp. casei (91%).

  • TABLE 5

    Percentages of clinical CoNS isolates categorized as antibiotic resistant toward various antibiotic agents

    ParameterValue or description in study for given species a
    Hellmark et al., 2009 (499) Mendes et al., 2010 (497) b Putnam et al., 2010 (543) Kresken et al., 2011 (75) c Mendes et al., 2012 (64) Gordon et al., 2012 (65) d Barros et al., 2012 (573) Flamm et al., 2013 (534) e Zhanel et al., 2013 (496)
    S. epidermidisMS-CoNSMR-CoNSCoNSS. epidermidisS. haemolyticusS. epidermidisS. epidermidisS. haemolyticusMS-CoNSMR-CoNSMS-SEMR-SE
    Study design parameters
        No. of isolates334201,3882,510148102711006427848347585
        CountrySwedenEuropeEuropeWorldwideGermanyGermanyUSAUSABrazilUSAUSACanadaCanada
        SourcePJIDiverseDiverseMainly BSI, also cSSSIDiverseDiverseMainly BSIDiverseMainly BSIDiverseDiverseDiverseDiverse
    % Resistant isolates
        PenicillinNDNDNDND91.1/88.0/94.695.9/93.9/93.1ND98.095.3NDNDNDND
        Oxacillin840.0100.076.482.7/83.1/85.590.4/90.9/89.273.279.087.50.0100.00.0100.0
        Gentamicin795.558.8ND65.5/56.3/60.880.8/84.8/87.340.846.073.43.624.634.778.8
        Erythromycin6735.772.366.1NDND69.086.064.139.968.3NDND
        Clindamycin675.537.333.4NDND40.974.046.913.034.637.686.7
        Q/DND0.01.60.5NDNDNDNDNDNDNDNDND
        ClarithromycinNDNDNDNDNDNDNDNDNDNDND64.484.7
        Ciprofloxacin79NDNDNDNDND70.4ND71.923.061.147.296.5
        LevofloxacinND8.667.954.1NDNDND77.0ND21.959.647.095.6
        Moxifloxacin64NDNDND42.3/52.1/47.357.5/51.5/60.8NDNDNDNDND39.094.1
        SXT829.148.6NDNDND47.973.053.120.144.733.980.0
        ChloramphenicolNDNDNDNDNDNDNDND25.0NDNDNDND
        Fusidic acid39NDNDNDNDNDNDNDNDNDNDNDND
        Rifampin39NDNDNDNDNDND35.010.9NDNDNDND
        DoxycyclineNDNDNDND10.1/9.2/6.112.3/12.1/5.9NDNDNDNDNDNDND
        TetracyclineND10.519.9NDNDND11.318.018.77.618.6NDND
        Tigecycline0NDNDND0.0/0.0/0.71.4/4.5/0.0NDNDNDNDND0.00.0
        Daptomycin30.00.10.0NDNDNDNDNDNDND0.00.0
        Linezolid00.20.40.80.0/0.0/0.00.0/0.0/0.018.32.0ND0.41.70.00.0
        Vancomycin00.00.00.00.0/0.0/0.00.0/0.0/0.00.0NDND0.00.00.00.0
        TeicoplaninND3.3 (0.0) f 12.2 (0.5) f 0.4NDNDNDNDND0.00.0NDND
        MupirocinNDNDNDNDNDNDNDND7.8NDNDNDND
    • ↵a Abbreviations: ND, not done; Q/D, quinupristin-dalfopristin; SXT, trimethoprim-sulfamethoxazole; SE, S. epidermidis; MS, methicillin susceptible; MR, methicillin resistant; BSI, bloodstream-related infection; cSSSI, complicated skin and skin structure infection; PJI, prosthetic joint infection.

    • ↵b Besides those for other and unidentified CoNS species, mainly S. epidermidis (n = 953), S. haemolyticus (n = 114), S. hominis (n = 176), S. lugdunensis (n = 25), S. saprophyticus (n = 30), S. warneri (n = 36), and S. xylosus (n = 24) data have been included. Only EUCAST interpretative criteria-based data are given; for CLSI criteria-based data, see the relevant publication.

    • ↵c Data are shown for three collection periods, as follows: 2005/2007/2009.

    • ↵d Data are shown only for isolates characterized as most disseminated.

    • ↵e For methicillin-susceptible CoNS, besides those for other and unidentified CoNS species (n = 188), mainly S. capitis (n = 15), S. epidermidis (n = 57), S. haemolyticus (n = 5), S. hominis (n = 6), and S. warneri (n = 5) data are shown; for methicillin-resistant CoNS, besides those for other and unidentified CoNS species (n = 330), mainly S. epidermidis (n = 102), S. haemolyticus (n = 5), S. hominis (n = 10), S. lugdunensis (n = 18), and S. saprophyticus (n = 6) data are shown.

    • ↵f Percentages given in parentheses show prevalences according to CLSI interpretative criteria.

  • TABLE 6

    In vitro activities of clinical CoNS isolates toward newer antibiotic agents

    ParameterValue or description in study for given species a
    von Eiff et al., 2005 (500) Kratzer et al., 2007 (525) Hellmark et al., 2009 (499) Karlowsky et al., 2011 (501, 526)
    MS-SEMR-SEMS-SHMR-SHMS-SEMR-SES. epidermidisMS-SEMR-SE
    Study design parameters
        No. of isolates1421171515873383 (501), 202 (526)19 (501), 34 (526)
        CountryGermanyGermanyGermanyGermanyAustriaAustriaSwedenCanadaCanada
        SourceDiverseDiverseDiverseDiverseBSI of BMTRsBSI of BMTRsPJIDiverseDiverse
    MIC90, MIC range
        CeftarolineNDNDNDNDNDNDND0.25, ≤0.12–0.50.5, 0.25–1
        Ceftobiprole0.5, 0.13–12, 0.5–40.5, 0.13–14, 1–4NDND1.5, 0.094–1.51.0, ≤0.06–22, 1–4
        Linezolid1.0, 0.5–11, 0.5–11, 0.5–11, 0.5–1NDND0.25, 0.047–0.381, ≤0.12–2 (501), and 1, ≤0.12–2 (526)1, 0.5–1 (501), and 1, 0.25–1 (526)
        DaptomycinNDNDNDND0.25, <0.01–0.250.25, <0.01–0.5ND0.25, ≤0.03–0.25 (501), and 0.25, ≤0.03–1 (526)0.25, 0.12–0.25 (501), and 0.25, 0.12–0.5 (526)
        TigecyclineNDNDNDND0.5, 0.06–0.50.5, <0.01–0.50.25, 0.047–0.50.5, ≤0.03–0.5 (501), and 0.5, ≤0.03–0.5 (526)0.25, 0.06–0.25 (501), and 0.25, 0.06–0.5 (526)
        DalbavancinNDNDNDNDNDND0.047, 0.003–0.0470.06, ≤0.03–10.06, ≤0.03–0.06
        TelavancinNDNDNDNDNDNDND0.5, ≤0.06–10.5, 0.12–1
    • ↵a Abbreviations: ND, not done; SE, S. epidermidis; SH, S. haemolyticus; MS, methicillin susceptible; MR, methicillin resistant; PJI, prosthetic joint infection; BMTRs, bone marrow transplant recipients; BSI, bloodstream-related infection.

  • TABLE 7

    Overview of mecA homologues and prototype strains according to the classification of the IWG-SCC

    Proposed new designation a Reported gene name (reference)Prototype strainStrain originSize (bp)% Identity b
    mecA mecA (477) S. aureus N315Human (Japan)2,007100
    mecA Staphylococcal strains that carry mecA Diverse hosts and sources2,00798.3–100
    mecASf (465) S. fleurettii SFMP01 (CCUG 43834T)Goat (goat milk cheese)ND c 99.8
    mecA1 mecA (mecA1) (463) S. sciuri subsp. carnaticum K11 d Cattle (veal leg, sliced)2,00179.1
    mecAs, mecASs (465, 466) S. sciuri subsp. rodentium ATCC 700061Norway rat2,00180.2
    mecA2 mecA (464) S. vitulinus CSBO8 c Horse2,00791
    mecB mecAm (626) M. caseolyticus JCSC5402 c Domestic chicken (skin swab)2,02561.6
    mecC mecA LGA251 (470) S. aureus LGA251 c Cattle (bulk milk sample)1,99868.7
    mecC1 mecC1 (474) S. xylosus S04009Bovine mastitis1,99769.9 d
    mecC2 mecC2 (475) S. saprophyticus subsp. saprophyticus 210Common shrew1,99892.9 e
    • ↵a According to the proposed nomenclature for reporting novel mecA gene homologues (461), as follows: mec gene type, ≥70% nucleotide sequence identity with the respective prototype (hitherto described genes are mecA, mecB, and mecC); and mec gene allotypes, ≥70% to <95% nucleotide sequence identity to the respective mec gene prototype strains, designated with a numeral based on the chronological order of discovery (e.g., mecA1, mecA2, and mecC1).

    • ↵b Unless otherwise stated, percent identity with the mecA gene in S. aureus N315.

    • ↵ND, no data given.

    • ↵d Percent identity with the mecA gene of S. aureus MRSA252. The gene has 93.5% nucleotide identity to mecC in S. aureus LGA251.

    • ↵e Percent identity with the mecC sequence of S. aureus LGA251. The gene has 94.5% identity to the mecC1 sequence of S. xylosus S04009.

  • TABLE 8

    Occurrence of SCC elements in a selection of CoNS species

    CoNS speciesSource(s)SCCmec (sub)type(s) a [reference(s)]
    S. capitis Humans, dogsI, IA, II, III, IV, IVa, V, NT (627 – 630)
    S. cohnii Humans, dogsNT (629, 630)
    S. chromogenes HumansIV (630)
    S. epidermidis Humans, cats, dogs, horses, pigs, poultryI, IIa, IIb, III, III (variant), IV, IVa, IVb, IVc, IVd, IVe, IVg, V, VI, NT (63, 70, 627 – 635)
    S. haemolyticus Humans, cats, horses, pigsI, II, II.1, III, III (variant), IV, V, NT (70, 627 – 630, 632, 634 – 637)
    S. hominis Humans, dogs, pigsI, III, IV, NT (627 – 630, 633 – 635)
    S. lentus Cattle, goats, sheepIII (631)
    S. pasteuri PigsIVc (634)
    S. rostri PigsIII, IVa, NT (634)
    S. saprophyticus HumansIII, NT (498, 638)
    S. sciuri Humans, cattle, goats, pigs, sheepI, III, IIIA, V, VII, NT (468, 627, 631, 634)
    S. warneri Humans, dogs, pigs, fish foodIV, IV.1, IVb, IVE, NT (629, 632 – 634, 637)
    S. xylosus CattleIII, XI b (474, 631)
    • ↵NT, nontypeable and/or novel nondesignated types.

    • ↵b Harbors the mecC gene or its allotype (mecC1).

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Coagulase-Negative Staphylococci
Karsten Becker, Christine Heilmann, Georg Peters
Clinical Microbiology Reviews Oct 2014, 27 (4) 870-926; DOI: 10.1128/CMR.00109-13

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Coagulase-Negative Staphylococci
Karsten Becker, Christine Heilmann, Georg Peters
Clinical Microbiology Reviews Oct 2014, 27 (4) 870-926; DOI: 10.1128/CMR.00109-13
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