Elizabethkingia, Chryseobacterium and Myroides species
Authors: M. Cecilia Di Pentima, M.D., MPH, FAAP
MICROBIOLOGY
The newly classified and renamed Elizabethkingia, Chryseobacterium and Myroides genera were originally included among the different species that belong to the genus Flavobacterium. The genus Flavobacterium was created in 1923 for a group of non-spore forming, aerobic gram- negative rods, with the ability to produce yellow pigmented colonies (8). Based on this broad characterization many species were added to the Flavobacterium genus including F. meningosepticum, F. indologenes and F. odoratum, well known today as human pathogens (10, 72, 119, 130). Further studies showed that many of these species were not truly related, and the genus underwent a series of reclassifications. More recently, new data on genotypic, chemotaxonomic and phenotypic analysis allowed regrouping of these species into four separate genus, Chryseobacterium spp., Flavobacterium spp., and Myroides spp. (10, 21, 71, 72,130). All belong to the family Flavobacteriaceae (66).
The genus Elizabethkingia currently includes two species: E. meningosepticum (Formerly known as C. meningosepticum, and previously as F. meningosepticum and CDC Group IIa), and E. miricola (71). Until recently, only E. meningosepticum was considered true human pathogen. In 2008, Green et al described the first case of Elizabethkingia miricola sepsis in an immunocompromised host (54). The genus Chryseobacterium includes one specie considered a human pathogen: C. indologenes (F. indologenes and CDC group IIb). The genus Flavobacterium includes species in CDC groups IIe, IIh and IIi (21). The new genusMyroides includes M. odoratus, formerly known as Chryseobacterium odoratum and F. odoratum, and M. odorimimus, formerly CDC group M-4f (21, 66). The Elizabethkingia and Chryseobacterium genus includes a group of aerobic, non-fermentative or slowly fermentative, catalase, phosphatase and indole positive, rarely encapsulated, non-motile gram-negative bacilli (9, 105). These microorganisms are long, thin, slightly curved, with rounded ends (9). E. meningosepticum and C. indologenes typically grow within 24 hours of incubation on blood and chocolate agar, but rarely on MacConkey or Salmonella-Shigella agar (74). All strains of C. indologenes produce smooth, dark yellow, pigmented colonies, clearly identifiable after 24 hours of incubation. Colonies of E. meningosepticum are weakly pigmented or not pigmented at all. However, an additional 24 to 48 hours of incubation at room temperature may increase pigmentation, allowing faster identification, and helping the clinician to choose an appropriate empiric therapy until final results become available (39, 62, 74, 105).
E. meningosepticum is the only encapsulated species and the most relevant in clinical practice. The ability to produce proteolytic enzymes may be associated with its virulence and the ability to cause severe human infections (36). Of the six serotypes described, A - F, serotype C is most commonly responsible for neonatal infections (15, 109). DNA-DNA hybridization studies on a limited number of strains have identified two main genomic groups, I and II, the latter including four subgroups, II:1 to 4 (36, 127). Eighteen of 20 strains isolated from CSF belong to subgroup II:1, leading to the hypothesis that genetic differences may play a role in pathogenicity of the different strains of E. meningosepticum (36, 127). Myroides spp. are non-saccharolytic and indole negative. Colonies produce a characteristic fruity odor.
EPIDEMIOLOGY
Elizabethkingia, Chryseobacterium and Myroides spp. are ubiquitous in the environment. They can be found in freshwater, saltwater, and soil (106, 110, 119). Strains of E. meningosepticum, sharing the same phenotypic, chemotaxonomic, and genomic characteristics of human pathogens, have been isolated from infected birds (129). However, only one human infection with Flavobacterium spp. CDC Group IIb-like organism has been reported following an animal bite (52). Although community acquired infections have been described after exposure to contaminated water, in most cases the source remains unknown (5, 17, 118).
Nosocomial outbreaks have been recognized since 1956, representing an important source of morbidity and mortality, especially in neonates and immunocompromised patients (2, 19, 20, 22, 29, 51, 56, 82, 89, 92, 101, 108, 135).
Elizabethkingia, Chryseobacterium and Myroides spp. have been isolated from numerous hospital sources, including ice machines, vials of intravenous and aerosolized drugs, nebulizers, topical disinfectants, sink traps, water taps and tube feedings (11, 18, 20, 37,43, 59, 101, 108, 124). A recent incident involving transmission of E. meningoseptica to tissue-allograph was described in two patients receiving tendon and tendon-bone allographs.
Elizabethkingia spp. and Chryseobacterium spp. have been isolated from the female genital tract, but whether this site is a source of neonatal colonization with subsequent development of early and late onset meningitis has not been studied (35, 92, 100).
CLINICAL MANIFESTATIONS
Among all Elizabethkingia spp., E. meningosepticum is the most important human pathogen. Clinical manifestations are mainly related to age, immunity and exposure to contaminated sources.
During the neonatal period, E. menigosepticum meningitis represents the most severe and common clinical presentation (15, 41, 46,56, 89, 111, 125). Onset of infection can be insidious, and may resemble the common signs and symptoms of early and late onset neonatal meningitis due to other pathogens common in this age group (32, 39, 44, 51, 69, 126, 134). Proposed risk factors associated with poor neurological outcome, mainly hydrocephalus and deafness, include prematurity, age of onset (less than 9 days of age), intrathecal antibiotics and the length of time cerebrospinal fluid (CSF) cultures remain positive (more than 10 days) (15, 39, 55). Although the overall mortality from early reports is above 60%, early diagnosis and institution of appropriate therapy is associated with a better prognosis (39). The first case of C. indologenes infection was recently described in a previously healthy 33 day-old infant who developed bacteremia without meningitis. The infant recovered following a 10 day-course of cefepime.
In older pediatric patients and adults, without underlying conditions, community acquired Elizabethkingia infections occur infrequently. Such infections are seen mainly in geriatric patients and the most common presentation is pneumonia (5, 15, 123).
Skin infections due to Elizabethkingia and Chryseobacterium spp., from recurrent cellulitis to ulcerative granulomatous lesions, are being recognized increasingly in healthy and diabetic adult patients (3, 6, 17, 50). Wound sepsis following extensive burns has been reported with E. meningosepticum and C. indologenes in children and adults (63, 70, 118). Endocarditis has been described in two patients, following dialysis and intravenous drug abuse (15).
Ophthalmologic infections, including keratitis, endophthalmitis, and corneal abscess, following trauma, surgery, or a previous infection, have been described mainly with C. indologenes (24, 40, 62, 78, 85). Recently, a case of plasma cell osteomyelitis was reported in a healthy adult, due to a mixed infection with Shigella (68). Among hospitalized adults, clinical presentation varies according to the source of exposure and risk factors. Underlying immunodeficiencies and invasive surgical procedures determine the severity and the site of infection. Bacteremia, sepsis and meningitis, peritonitis and intraabdominal abscess have been described in association with indwelling devices, infusion of contaminated solutions, head and neck surgery, peritoneal dialysis, and polypectomy among others (11, 25, 55, 57, 62, 63, 75, 78, 92, 100, 108, 114, 138). Nosocomial pneumonia, mainly among intubated, immunocompromised adults, has a mortality rate of 60% (20, 29, 124). Most frequently, Elizabethkingia spp. and Chryseobacteriumspp. are isolated from endotracheal and nasal secretions and not considered true pathogens (2, 43, 59). Bacterial load, immune status and selective antibiotic pressure may prompt invasive disease. Reported predisposing immunodeficiencies have ranged from carcinoma, tuberculosis, leukemia, aplastic anemia, asplenia, congenital immunodeficiency and corticosteroid therapy (35, 76, 77, 78,80, 91, 111, 121, 128).
The largest series of nosocomial infections due to C. indologenes have been reported from Taiwan (34, 61, 62, 63). The majority of patients had infections related to the use of indwelling devices, including surgical drains, intravascular catheters, endotracheal tubes or foley catheters. Clinical presentations included intraabdominal infection, wound sepsis, bacteremia, pneumonia, pyelonephritis, and abscess. Underlying debilitating conditions such as cancer, diabetes, and extensive burns were present in almost all patients (91%). Five deaths (14%) were attributable to overwhelming sepsis with C. indologenes. A non-fatal case of bacteremia has been reported in a patient with advanced carcinoma of the breast, where the portal of entry was assumed to be an intravenous line or an open eroded wound (123). An episode of recurrent bacteremia that cleared after removal of the Port-A-Cath was reported in a neutropenic patient (98). Peritonitis due to C. indolgenes has been reported in a patient on CAPD who was receiving treatment with ciprofloxacin to which the organism was susceptible in vitro (4). The introduction of colistin and tigecycline has been associated with increasing prevalence of C. Indologenes infections (34).
Myroides spp. are uncommonly encountered in the clinical laboratory and seldom considered true pathogens. Of 24 isolates identified over a decade at the Central Public Health Laboratory, Colindale, London, two from amputation stumps and three from urine were most likely opportunistic pathogens (58). A small number of serious infections caused by Myroides spp. have been reported in the English literature. Cases included cellulitis and bacteremia in a patient receiving prednisone, necrotizing fasciitis and bacteremia in a patient with cirrhosis due to hepatitis B virus infection, endocarditis in a patient on long term hemodialysis, and ventriculitis in a 6-week-old infant (6, 47, 65, 88).
PATHOGENESIS
Little is known about the pathogenesis of Elizabethkingia spp. and Chryseobacterium spp. infections. Early animal studies support the low virulence of these microorganisms, however, these experimental studies lack accurate information. Adult rabbits and newborn hamsters survived, without evidence of infection, after intravenous and subcutaneous inoculation, respectively. Intracerebral inoculation lead to a mortality rate of 27%, but microorganisms were not recovered at autopsy (74).
Invasive infection is usually preceded by colonization of the respiratory tract, particularly in high risk patients such as neonates and adults in intensive care units (2, 39, 41, 51, 59). Most likely, early and late onset neonatal meningitis is also preceded by colonization of the infant at the time of delivery as this has been described for other common neonatal pathogens. However, this hypothesis has not been studied.
SUSCEPTIBILITY IN VITRO AND IN VIVO
In vitro susceptibility testing for Elizabethkingia spp. and Chryseobacterium spp. have been a source of controversy and choosing appropriate empiric therapy early in the course of a severe infection can be difficult. Many factors are responsible for the lack of standardization of antibiotic management in Elizabethkingia, Chryseobacterium and Myroides infections. First, the National Committee for Clinical Laboratory Standards (NCCLS) has not established MIC breakpoints for resistance and susceptibility for either genus (97). Breakpoints used for other non-Enterobacteriaceae or for gram-positive pathogens may not correlate accurately with clinical outcome (39). Secondly, disk diffusion testing has been shown to be inaccurate (1, 23). Finally, the susceptibility pattern among Elizabethkingia, Chryseobacterium and Myroides spp. is unusual, in that they are almost always resistant to agents commonly chosen to treat aerobic gram-negative bacilli and susceptible to antibiotics used in gram-positive infections.
Elizabethkingia, Chryseobacterium and Myroides spp. are usually resistant to cephalosporins, aminoglycosides and carbapenems (33,67).
There is sufficient evidence that antibiotic resistance among Elizabethkingia, Chryseobacterium and Myroides spp. is based on production of two different classes of ß-lactamases. Classification of ß-lactamases includes four classes: three molecular families of active-site serine ß-lactamases (Class A, C and D) and one of metallo- ß-lactamases (Class B) (26, 27, 28, 94). Rossolini et al., described the ability of Elizabethkingia spp. and Chryseobacterium spp. to produce a Class A ß-lactamase, named CME-1. This enzyme is a clavulanic acid-susceptible extended-spectrum ß-lactamase active on narrow to extended spectrum cephalosporins, penicillins, and monobactams. CME-1 does not hydrolyze cephamycins and carbapenems (112). More recently, Bellais et al. described a second enzyme named CME-2, with minimal differences in the amino-acid sequence but an identical hydrolysis profile (7). Hsueh et al. reported cross-resistance between ceftazidime, cefepime and cefpirome for more than 90% of E. meningosepticumand C. indologenes strains tested (64). Similar findings have been described with P. aeruginosa, leading to the hypothesis that this pattern of resistance could be mediated by a novel ß-lactamase, OXA-1-like ß-lactamase, SHV-2 to SHV-6 and probably some extended TEM ß-lactamases (64, 133).
Elizabethkingia spp and Chryseobacterium spp. are also known to produce a Class B metallo- ß-lactamase (13, 14, 112, 113, 137). Two major functional groups of enzymes are currently recognized. One group is capable of hydrolyzing most ß-lactams except monobactams. The second, the "true" carbapenemases, is responsible for the hydrolysis of carbapenems, and has poor activity against penicillins and cephalosporins. Neither enzyme type is inhibited by clavulanic acid (27, 28).
These broad and complex mechanisms of resistance explain the unpredictable susceptibility of Elizabethkingia spp. andChryseobacterium spp. and the limited number of antimicrobials available to treat infections due to this organism. Tables 1 through 4 list the most important published patterns of susceptibility. Among the extended spectrum penicillins, piperacillin is the most active agent. In one series of 52 isolates, all were susceptible (piperacillin MIC, 1.6-12.5µg/ml; breakpoints ≤16, ≥128µg/ml) (23). More recent studies have reported an increase in isolates resistant or of intermediate susceptibility. Bolash et al. reported that the susceptibilities of E. meningosepticum to piperacillin and ticarcillin were similar; 28% and 22% respectively (Table 2) (16). Previous reports had found none of the isolates tested susceptible to ticarcillin (45). Piperacillin is most active β-lactam against C. indologenes(Table 3) (63). Myroides spp. are particularly resistant to all extended spectrum penicillins (Table 4) (33).
The addition of a ß-lactamase inhibitor, either tazobactam or clavulanate to piperacillin, amoxicillin or ticarcillin does not confer any significant advantage (Table 1) (48, 53, 67). However, in a study of 7 distinct isolates of E. meningosepticum, addition of clavulanic acid had a significant impact lowering the MIC’s of cephalosporins, particularly ceftazidime (109). Clavulanic acid lowered ceftazidime, cefotaxime and cefoperazone MIC by 6, 3, and 2 fold, respectively. None of the strains appeared to harbor plasmids, but a broad-substrate, constitutive, chromosomal ß-lactamase was detected (109).
In general, all cephalosporins have unpredictable and usually poor activity against these pathogens. Cefoperazone, cefotaxime and ceftriaxone showed similar activity with some isolates highly susceptible and many of intermediate susceptibility. However the MIC50 for E. meningosepticum are above the NCCLS susceptibility breakpoint for almost all the strains tested. Ceftazidime, and the first and second-generation cephalosporins are generally less active (Table 2). In one study, eight of 12 isolates were reported as being susceptible to cefoperazone-sulbactam (49). Fourth generation cephalosporins, cefepime and cefpirome have also poor activity against E. meningosepticum (Table 2) (64). In the case of C. indologenes, ceftazidime, cefoperazone, and cefepime appear to be relatively active with the MIC50 for cefepime being the lowest reported among the cephalosporins, (Table 3) (64). Myroides spp. which are highly resistant to all cephalosporins, have been shown to produce a ß-lactamase distinct from that produced by E. meningosepticum (Table 4) (118).
Aztreonam has shown poor activity against the few isolates tested (16, 67, 122). Furthermore, as a result of the production of metallo- ß-lactamases, Elizabethkingia, Chryseobacterium and Myroides spp. are highly resistant to both imipenem and meropenem (13, 16,23, 67, 114, 122).
In two studies testing a total of 158 isolates, minocycline had MIC’s exceeding the susceptibility breakpoint for 50% of E. meningosepticum and C. indologenes and 90% Myroides spp. (Table 1) (48, 60). Other investigators have reported similar results forE. meningosepticum, C. indologenes and Myroides spp. (Tables 2-4) (33, 45, 60). Doxycycline and tetracycline are less active (1, 23,45, 53, 114).
Quinolones have shown good activity against E. meningosepticum, especially ofloxacin (MIC range 0.06-8µg/ml; breakpoints ≤ 2, ≥ 8), levofloxacin (1-2; ≤ 2, ≥ 8) and ciprofloxacin (0.1-8; ≤ 1, ≥ 4) (23, 30, 33, 114, 131). Resistance of C. indologenes is slightly higher to all three quinolones, (0.25-128; ≤ 2, ≥ 8), (1-2; ≤ 2, ≥ 8), (0.25-128; ≤ 1, ≥ 4), respectively, (Table 3) (30, 33, 53, 61, 131).
Myroides spp. are particularly resistant to most quinolones tested (Table 4).
Interpretation of the in vitro performance of vancomycin against E. meningosepticum can be controversial since MIC breakpoints recommended by the NCCLS are for gram-positive microorganisms. Several authors have reported MIC’s ranging from 4 µg/ml to 64 µg/ml (Table 2).
Other Agents
Other non-beta-lactam antibiotics most consistently active against E. meningosepticum are rifampin (MIC range 0.2-3.1µg/ml; breakpoints ≤ 1, ≥ 4µg/ml), trimethoprim-sulfamethoxazole (≤ 0.15- > 6.4; ≤ 2, ≥ 8), and clindamycin (0.025-16; ≤ 0.5, ≥ 4). Among the macrolides, clarithromycin (1.5-16; ≤ 0.5, ≥ 8) is more active than erythromycin (0.1-200; ≤ 0.5, ≥ 8). Activity of the newer macrolides has not been reported. However, there is no consensus on susceptibility breakpoints for any of these antimicrobials for Elizabethkingia, Chryseobacterium or Myroides spp. Although some authors have reported isolates of Elizabethkingia and points for susceptibility, e.g. an amikacin MIC of 80 µg/ml, is well above the current breakpoint of ≤ 16µg/ml (55, 97). This incorrect statement regarding susceptibility was borne out by therapeutic failure with amikacin (55). It is important to reconsider carefully susceptibility patterns reported in the older literature before applying them in clinical practice. This is particularly the case if the comment has been based on disk testing results and if the statement is at odds with the data contained in Tables 1 to 4.
Relatively few isolates of C. indologenes (Table 3) and Myroides spp. (Table 4) are reported as series tested against various antibiotics. Overall, the pattern of resistance is similar to that of E. meningosepticum. In the case of C. indologenes, ceftazidime appears to be relatively active, although the reason is not certain. Myroides spp. are exceptionally resistant to almost all antibiotics reported to have been tested, with the exceptions of minocycline and doxycycline (33, 45).
Newer antibiotics, such as linezolid and quinupristin/dalfopristin have been tested against Elizabethkingia, Chryseobacterium andMyroides spp. isolates (39, 48). Once again, interpretation of data is difficult given the lack of clinical data and breakpoint susceptibilities for gram-negative microorganisms.
Correlation Between Disk, E-test Testing and MIC Results
An early study compared disk diffusion testing with agar dilution (1). The data showed that for many agents the interpretive disk zone diameters did not accurately predict the susceptibility ofElizabethkingia and Chryseobacterium spp. as determined by the agar dilution method (1). For erythromycin, three strains tested susceptible by disk testing when MICs ranged from 32 µg/ml to 128 µg/ml, and another 11 strains showed intermediate susceptibility by disk testing but the MICs were ≥ 32 µg/ml. For gentamicin, two strains were considered susceptible and 13 of intermediate susceptibility by disk tests, however, all 28 strains had MICs above > 32 µg/ml. Vancomycin MICs ranged from 8 to 16 µg/ml, but by disk testing all strains were considered susceptible, with zones ≥ 12mm. These findings, corroborated by other authors, have lead to the recommendation that MIC testing should be performed to avoid errors in reporting Elizabethkingia and Chryseobacteriumsusceptibility results (1, 33, 136). One study has evaluated 100 isolates and compared MICs obtained by agar dilution and E-test (60). MIC50 by agar dilution for piperacillin, cefotaxime and minocycline were 1 log lower than those obtained by E-test. However, the MIC50 of ofloxacin and ciprofloxacin were exactly the opposite, 1 log higher by agar dilution than by E-test. The agreement between the two met hods (± 1 log2 dilution) was considered acceptable for cefotaxime, ceftazidime, amikacin, minocycline, ofloxacin, and ciprofloxacin (> 90%). The poorest correlation was found for piperacillin. The authors concluded that E-test results are acceptable for determining the susceptibility of Elizabethkingia and Chryseobacterium spp. except to piperacillin. The final recommendation regarding piperacillin is that any MIC by E-test between 16 µg/ml and 128 µg/ml should be further evaluated by another method (60).
Synergy Studies
In vitro synergy studies have been reported for a limited number of strains of Elizabethkingia, Chryseobacteriumand Myroides spp. using checkerboard titration techniques (39, 131). Trovafloxacin in combination with ceftazidime, amikacin and imipenem tested against 22 isolates of these genera. An additive effect was seen in all strains when trovafloxacin was combined with either ceftazidime, amikacin or imipenem. Synergy between trovafloxacin and ceftazidime was confirmed by time-kill methods for 10 strains of E. meningosepticum (131).
In a second study, the combination of vancomycin and rifampin was synergistic for 3 of four isolates tested. The interaction between meropenem in combination with ciprofloxacin, or rifampin or linezolid was additive for all four isolates. Linezolid in combination with vancomycin and ciprofloxacin also showed additive effect (39). Although these results suggests that certain combinations of antibiotics may be more useful than others, further correlation between clinical and laboratory data is needed (39).
ANTIMICROBIAL THERAPY
General
The optimal antimicrobial therapy for infections due to Elizabethkingia, Chryseobacterium and Myroides spp. is difficult to determine. Empiric therapy is based on the unusual susceptibility pattern, the availability of effective antimicrobials, the age of the patient, clinical presentation and reported experience.
Definitive therapy should rest upon the susceptibility results of the isolated organism. Important considerations to remember when managing these infections include: disk diffusion techniques are not reliable and treatment failures can occur if treatment is based on disk results, antimicrobial susceptibilities should be confirmed using a quantitative method, and acquired antimicrobial resistance can develop during therapy. Repeat cultures and susceptibility testing is recommended if the patient remains culture positive, does not improve or deteriorates.
Special Infection
Meningitis
Meningitis is not only the most common but also the most difficult E. meningosepticum infection to treat successfully. Delay in implementing appropriate therapy and the lack of effective antimicrobials commonly permits the persistence of positive CSF cultures for much longer periods than for other gram-negative pathogens causing neonatal meningitis (39).
Although vancomycin MICs are high and its indication is controversial, this drug has been the most effective agent reported in the literature for the management of meningitis, especially in combination with rifampin (39, 41, 126). Even when MICs for vancomycin are as high as 32 μg/mL, the use of this combination should be considered since the addition of rifampin lowers these values to therapeutically achievable CSF levels (39, 95). Vancomycin resistance acquired during therapy has been described, and this possibility should be considered in the event of treatment failures (56, 117). A recent report advised against using vancomycin for E. meningosepticum meningitis based on the high MICs (16 µg/ml) of this drug for this pathogen (104). Rifampin is very active againstElizabethkingia and Chryseobacterium spp., however, when used as a single agent it may rapidly induce resistance.
Susceptibility of E. meningosepticum to trimethoprim-sulfamethoxazole varies significantly in recent reports, ranging from 23 to 100% resistance (16, 45, 81). Linder et al. reported a successful outcome in eight of nine infants treated with this drug, however, none of these patients had a positive CSF culture or confirmed meningitis (84). Trimethoprim-sulfamethoxazole has excellent penetration into the CSF and anecdotal evidence for its effectiveness in E. meningosepticum meningitis is available (77, 102). Special considerations, when using trimethoprim-sulfamethoxazole during the neonatal period, is it association with hematological abnormalities and kernicterus.
Piperacillin should be use cautiously in CNS infections, even when the isolates are inhibited by ≤ 8 μg/ml since the achievable concentration of this drug in the CSF could be sub-therapeutic (38, 39, 107). Furthermore, of the 8 reported cases who received piperacillin, five developed hydrocephalus and one died (2, 83, 110).
The use of intraventricular antibiotics has been associated with an increased risk of hydrocephalus, and should not be considered unless intravenous therapy has failed to eradicate infection (39). In older patients, empiric treatment with minocycline and quinolones can also be considered. Minocycline has good in vitro activity against the great majority of isolates, good penetration into CSF and is available as a parenteral formulation (15). Given that tetracyclines are primarily bacteriostatic, combination with another active agent such as rifampin is advisable.
The pharmacodynamics of quinolones in bacterial meningitis have shown that in order to achieve bactericidal effectiveness, the concentration of antibiotics in the CSF needs to exceed the MBC for the entire dosing interval (87). Quinolones are lipophilic agents and peak CSF concentrations, up to 26% of the serum concentration are reached rapidly (87). Although there are discrepancies in the literature, in general the MIC50 of ciprofloxacin is below the NCCLS susceptibility breakpoint for the majority of the isolates tested (Table 2) (15, 16). Ciprofloxacin is currently FDA approved for neonatal treatment of multidrug-resistant Gram-negative infections. Nevertheless, clinical experience with quinolones in E. meningosepticum neonatal meningitis is not widely available in the English literature. Sakuma et al, recently reported the successful treatment of a 5-day-old infant with E. meningosepticum meningitis treated with intravenous ciprofloxacin and trimethoprim-sulfamethoxazole (115). The use of trimethoprim-sulfamethoxazole has to be cautiously in this age group.
Most strains of E. meningosepticum are highly resistant to all cephalosporins (Table 2). Based on in vitro susceptibilities, it has been proposed that ceftizoxime might be effective treatment, however, there is not enough clinical experience reported in the English literature to support the use of this agent in neonatal meningitis (12, 15). A single case of E. meningosepticum meningitis treated with cefepime was reported in the Literature. Lu et al described a 21 year-old women with insulin-dependent diabetes and E. meningosepticummeningitis, successfully treated with a 21-day-course of cefepime. The recovered strain was sensitive to third generation cephalosporins, cefepime, meropenem, imipenem/cilastatin, and moxalactam.
As with other gram-negative meningitis it is recommended that therapy continue for two to three weeks after sterilization of the CSF is accomplished. Recommendations for treatment of other E. meningosepticum infections follow those for meningitis and are modified by the age of the patient. Minocycline or a quinolone, in combination with rifampin, seems appropriate empiric therapy in patients older than 8 years. For C. indologenes, piperacillin, ceftazidime, cefoperazone, and fourth generation cephalosporins may be considered drugs of choice (33, 64). As previously mentioned, trimethoprim-sulfamethoxazole has excellent penetration into the CSF and anecdotal evidence suggest that in combination with ceftazidime, this drug can be efficient in patients with C. indologenesmeningitis (99). Although minocycline has good activity, in severe infections piperacillin is recommended since tetracyclines are bacteriostatic agents. Management of catheter related infections should follow the general considerations indicated for other gram-negative pathogens (96). It has been reported, however, that intravascular catheter associated bacteremia due to C. indologenes can be cleared without removal of the catheter (63).
Myroides spp. are exceptionally resistant. Of the antibiotics tested in vitro minocycline appears most active (15). There is insufficient clinical experience of the treatment of infections due to M. odoratum to justify any particular recommendation.
ENDPOINTS FOR MONITORING THERAPY
In gram-negative neonatal meningitis, systemic antibiotics are given for approximately 2 weeks after bacteriologic cure. Repeat CSF examinations and cultures are usually required 48 to 72 hours after initiation of therapy, until negative cultures are achieved and at the end of therapy. Because sterilization of CSF is commonly delayed in E. meningosepticum meningitis, antibiotic therapy is generally prolonged for three or more weeks. Endpoint criteria to make this final decision are based on the clinical course and CSF findings before stopping antimicrobial therapy.
Management of catheter related infections should follow the general recommendations for other gram-negative pathogens (96). In general, if the patient remains clinically stable and bacteremia resolves within 48-72 hours after institution of therapy, removal of the catheter may not be mandatory. Blood cultures should be obtained daily from each catheter port and peripherally until all cultures remain negative for 48 to 72 hours. Length of therapy is based on the duration of bacteremia and the immunologic status of the patient. Intravenous therapy should be continued for 7 to10 sterile days in immunocompetent patients and for 10 to 14 sterile days in immunocompromised patients. Successful treatment of C. indologenes bacteremia without removal of the catheter has been reported (63).
VACCINES
No vaccines are currently available for Chryseobacterium and Myroides species.
INFECTION CONTROL MEASURES
Patients known to be infected or colonized with Elizabethkingia, Chryseobacterium or Myroides spp. should be placed in isolation following the institutional guidelines for multiple antibiotic-resistant organisms. Particular attention should be placed when handling respiratory equipment, especially nebulizers with a reservoir. These species can multiply to substantial concentrations in nebulizer fluid and increase the risk of spreading nosocomial pneumonia.
REFERENCES
1. Aber RC, Wennersten C, Moellering RC, Jr. Antimicrobial susceptibility of flavobacteria. Antimicrob Ag Chemother 1978;14:483-487. [PubMed]
2. Abrahamsen TG, Finne PH, Lingaas E. Flavobacterium meningosepticum infections in a neonatal intensive care unit. Acta Paediatr Scand 1989;78:51-55. [PubMed]
3. Abter EI, Lutwick LI, Torrey MJ, Mann R. Cellulitis associated with bacteremia due to Flavobacterium meningosepticum [Letter]. Clin Infect Dis 1993;17:929-930. [PubMed]
4. Akl ZA, Stern L, Romagnoli MF, Della-Latta P. Flavobacterium group IIb peritonitis in a patient on chronic ambulatory peritoneal dialysis [Letter]. Perit Dial Int 1996;16:331-332. [PubMed]
5. Ashdown LR, Previtera S. Community acquired Flavobacterium meningosepticum pneumonia and septicaemia [Letter]. Med J Aust 1992;156:69-70. [PubMed]
6. Bachman KH, Sewell DL, Strausbaugh LJ. Recurrent cellulitis and bacteremia caused by Flavobacterium odoratum. Clin Infect Dis 1996;22:1112-1113. [PubMed]
7. Bellais S, Poirel L, Naas T, Girlich D, Nordmann P. Genetic-biochemical analysis and distribution of the Ambler class A beta-lactamase CME-2, responsible for extended-spectrum cephalosporin resistance in Chryseobacterium (Flavobacterium) meningosepticum. Antimicrob Agents Chemother 2000;44:1-9. [PubMed]
8. Bergey DH, Harrison FC, Breed R, Hammer B, Huntoon F. Bergey's Manual of Determantive Bacteriology. Baltimore: Williams and Wilkins Co; 1923.
9. Bergey's Manual of Determinative Bacteriology. Ninth Edition ed. Philadelphia: Lippincott Williams & Wilkins; 2000.
10. Bernardet JF, Segers P, Vancanneyt M, Berthe F, Kersters K, Vandamme P. Cutting a gordian knot: Emended classification and description of the genus Flavobacterium, and proposal of Flavobacterium hydatis nom. nov. (Basonym, Cytophaga aquatilis Strohl and Tait 1978). Int J Syst Bacteriol 1996;46:128-148.
11. Berry WB, Morrow AG, Harrison DC, Hochstein HD, Himmelsbach CK. Flavobacterium septicemia following intracardiac operations: clinical observations and identification of the source of infection. J Thorac Cardiovasc Surg 1963;45:476-481.
12. Bhutta ZA, Naqvi SH. Successful eradication of Flavobacterium meningosepticum neonatal meningitis with ceftizoxime. J Pak Med Assoc 1991;41:141-142. [PubMed]
13. Blahova J, Hupkova M, Krcmery V, Kubonova K. Resistance to and hydrolysis of imipenem in nosocomial strains of Flavobacterium meningosepticum [Letter]. Eur J Clin Microbiol Infect Dis 1994;13:833. [PubMed]
14. Blahova J, Kralikova K, Krcmery V, Sr., Kubonova K. Hydrolysis of imipenem, meropenem, ceftazidime, and cefepime by multiresistant nosocomial strains of Sphingobacterium multivorum. Eur J Clin Microbiol Infect Dis 1997;16:178-180. [PubMed]
15. Bloch KC, Nadarajah R, Jacobs R. Chryseobacterium meningosepticum: an emerging pathogen among immunocompromised adults. Report of 6 cases and literature review. Medicine (Baltimore) 1997;76:30-41.[PubMed]
16. Bolash NK, Liu HH. Quinolone susceptibility of multiply-resistant Flavobacterium meningosepticum clinical isolates in one urban hospital. Drugs 1995;49 (Suppl 2):168-170. [PubMed]
17. Bolivar R, Abramovits W. Cutaneous infection caused by Flavobacterium meningosepticum [Letter]. J Infect Dis 1989;159:150-151. [PubMed]
18. Botzenhart K, Heizmann W, Sedaghat S, Heeg P, Hahn T. Bacterial colonization and occurrence of Legionella pneumophila in warm and cold water, in faucet aerators, and in drains of hospitals. Zentralbl Bakteriol Mikrobiol Hyg [B] 1986;183:79-85. [PubMed]
19. Brody JA. MH, King E. Meningitis caused by an unclassified gram-negative bacterium in newborn infants. J Dis Child 1958;96:1-5. [PubMed]
20. Brown RB, Phillips D, Barker MJ, Pieczarka R, Sands M, Teres D. Outbreak of nosocomial Flavobacterium meningosepticum respiratory infections associated with use of aerosolized polymyxin B. Am J Infect Control 1989;17:121-125. [PubMed]
21. Bruckner D, Colonna P, Bearson B. Nomenclature for aerobic and facultative bacteria. Clin Infect Dis 1999;29:713-723. [PubMed]
22. Bruun B, Jensen ET, Lundstrom K, Andersen GE. Flavobacterium meningosepticum infection in a neonatal ward. Eur J Clin Microbiol Infect Dis 1989;8:509-514. [PubMed]
23. Bruun B. Antimicrobial susceptibility of Flavobacterium meningosepticum strains identified by DNA-DNA hybridization. Acta Pathol Microbiol Immunol Scand (B) 1987;95:95-101. [PubMed]
24. Bucci FA, Jr., Holland EJ. Flavobacterium meningosepticum keratitis successfully treated with topical trimethoprim-sulfamethoxazole. Am J Ophthalmol 1991;111:116-118. [PubMed]
25. Burnakis TG, Mioduch HJ, LeBar WD, Yalamanchi RR. Sepsis from Flavobacterium meningosepticum, an uncommon pathogen with unusual susceptibility patterns. South Med J 1986;79:518-519. [PubMed]
26. Bush K, Mobashery S. How beta-lactamases have driven pharmaceutical drug discovery. From mechanistic knowledge to clinical circumvention. Adv Exp Med Biol 1998;456:71-98. [PubMed]
27. Bush K. Metallo-beta-lactamases: a class apart. Clin Infect Dis 1998;27 Suppl 1:S48-53. [PubMed]
28. Bush K. New beta-lactamases in gram-negative bacteria: diversity and impact on the selection of antimicrobial therapy. Clin Infect Dis 2001;32:1085-1089. [PubMed]
29. Cabrera HA, Davis GH. Epidemic meningitis of the newborn caused by flavobacteria. I. Epidemiology and bacteriology. Am J Dis Child 1961;101:289-291. [PubMed]
30. Canton E, Peman J, Jimenez MT, Ramon MS, Gobernado M. In vitro activity of sparfloxacin compared with those of five other quinolones. Antimicrob Agents Chemother 1992;36:558-565. [PubMed]
31. Cartwright EJ, Prabhu RM, Zinderman CE, Schobert W, Jensen B, Noble-Wang J, Church K, Welsh C, Kuehnert M, Burke TL, Srinivasan A, and the Food and Drug Administration Tissue Safety Team Investigators. J bone Joint Surg Am 2010;92:1501-6. [PubMed]
32. Chandrika T, Adler SP. A case of neonatal meningitis due to Flavobacterium meningosepticum successfully treated with rifampin. Pediatr Infect Dis 1982;1:40-41. [PubMed]
33. Chang JC, Hsueh PR, Wu JJ, Ho SW, Hsieh WC, Luh KT. Antimicrobial susceptibility of flavobacteria as determined by agar dilution and disk diffusion methods. Antimicrob Agents Chemother 1997;41:1301-1306.[PubMed]
34. Chen FL, Wang GC, Teng SO, Ou TY, Yu FL, Lee WS. Clinical and epidemiological features of Chryseobacterium indologenes infections: Analysis of 215 cases. J Microbiol Immunol Infect 2013;46:425-32. [PubMed]
35. Chiu CH, Waddingdon M, Greenberg D, Schreckenberger PC, Carnahan AM. Atypical Chryseobacterium meningosepticum and meningitis and sepsis in newborns and the immunocompromised, Taiwan. Emerg Infect Dis 2000;6:481-486. [PubMed]
36. Colding H, Bangsborg J, Fiehn NE, Bennekov T, Bruun B. Ribotyping for differentiating Flavobacterium meningosepticum isolates from clinical and environmental sources. J Clin Microbiol 1994;32:501-505. [PubMed]
37. Coyle-Gilchrist MM, Crewe P, Roberts G. Flavobacterium meningosepticum in the hospital environment. J Clin Pathol 1976;29:824-826. [PubMed]
38. Decazes JM, Meulemans A, Bure A, Laisne MJ, Modai J. [Penetration of piperacillin into the cerebrospinal fluid of patients with purulent meningitis]. Presse Med 1984;13:261-264. [PubMed]
39. Di Pentima MC, Mason EO Jr., Kaplan SL. In vitro antibiotic synergy against Flavobacterium meningosepticum: implications for therapeutic options. Clin Infect Dis 1998;26:1169-1176. [PubMed]
40. Doiz O, Llorente MT, Mateo A, Seral C, Garcia C, Rubio MC. [Corneal abscess by Flavobacterium indologenes. A case report]. Enferm Infecc Microbiol Clin 1999;17:149-150. [PubMed]
41. Dooley JR, Nims LJ, Lipp VH, Beard A, Delaney LT. Meningitis of infants caused by Flavobacterium meningosepticum: report of a patient and analysis of 63 infections. J Trop Pediatr 1980;26:24-30. [PubMed]
42. Douvoyiannis M, Kalyoussef S, Phillip G, Mayers MM. Chryseobacterium indologenes bacteremia in an infant. Int J Infect Dis 2010;44:e531-e532. [PubMed]
43. Du Moulin GC. Airway colonization by Flavobacterium in an intensive care unit. J Clin Microbiol 1979;10:155-160. [PubMed]
44. Eykens A, Eggermont E, Eeckels R, Vandepitte J, Spaepen J. Neonatal meningitis caused by Flavobacterium meningosepticum. Helv Paediatr Acta 1973;28:421-425. [PubMed]
45. Fass RJ, Barnishan J. In vitro susceptibilities of nonfermentative gram-negative bacilli other than Pseudomonas aeruginosa to 32 antimicrobial agents. Rev Infect Dis 1980;2:841-853. [PubMed]
46. Ferlauto JJ, Wells DH. Flavobacterium meningosepticum in the neonatal period. South Med J 1981;74:757-759.[PubMed]
47. Ferrer C, Jakob E, Pastorino G, Juncos LI. Right-sided bacterial endocarditis due to Flavobacterium odoratum in a patient on chronic hemodialysis. Am J Nephrol 1995;15:82-84. [PubMed]
48. Fraser SL, Jorgensen JH. Reappraisal of the antimicrobial susceptibilities of Chryseobacterium andFlavobacterium species and methods for reliable susceptibility testing. Antimicrob Agents Chemother 1997;41:2738-2741. [PubMed]
49. Fujita J, Hata Y, Irino S. Respiratory infection caused by Flavobacterium meningosepticum [Letter]. Lancet 1990;335:544. [PubMed]
50. Ge Y, MacDonald D, Henry MM, Hait HI, Nelson KA, Lipsky BA, Zasloff MA, Holroyd KJ. In vitro susceptibility to pexiganan of bacteria isolated from infected diabetic foot ulcers. Diagn Microbiol Infect Dis 1999;35:45-53.[PubMed]
51. George RM, Cochran CP, Wheeler WE. Epidemic meningitis of the newborn caused by flavobacteria. II. Clinical manifestations and treatment. Am J Dis Child 1961;101:296-304. [PubMed]
52. Goldstein EJ, Citron DM, Merkin TE, Pickett MJ. Recovery of an unusual Flavobacterium group IIb-like isolate from a hand infection following pig bite. J Clin Microbiol 1990;28:1079-1081. [PubMed]
53. Goldstein EJ, Citron DM. Comparative activities of cefuroxime, amoxicillin-clavulanic acid, ciprofloxacin, enoxacin, and ofloxacin against aerobic and anaerobic bacteria isolated from bite wounds. Antimicrob Agents Chemother 1988;32:1143-1148. [PubMed]
54. Green O, Murray P, Gea-Banacloche JC. Sepsis caused by Elizabethkingia miricola successfully treated with tigecycline and levofloxacin. Diagn Microbiol Infect Dis 2008;62:430-432. [PubMed]
55. Harrington SP, Perlino CA. Flavobacterium meningosepticum sepsis: disease due to bacteria with unusual antibiotic susceptibility. South Med J 1981;74:764-766. [PubMed]
56. Hazuka BT, Dajani AS, Talbot K, Keen BM. Two outbreaks of Flavobacterium meningosepticum type E in a neonatal intensive care unit. J Clin Microbiol 1977;6:450-455. [PubMed]
57. Hirsh BE, Wong B, Kiehn TE, Gee T, Armstrong D. Flavobacterium meningosepticum bacteremia in an adult with acute leukemia. Use of rifampin to clear persistent infection. Diagn Microbiol Infect Dis 1986;4:65-69. [PubMed]
58. Holmes B, Snell JJ, Lapage SP. Flavobacterium odoratum: a species resistant to a wide range of antimicrobial agents. J Clin Pathol 1979;32:73-77. [PubMed]
59. Hoque SN, Graham J, Kaufmann ME, Tabaqchali S. Chryseobacterium (Flavobacterium) meningosepticumoutbreak associated with colonization of water taps in a neonatal intensive care unit. J Hosp Infect 2001;47:188-192. [PubMed]
60. Hsueh PR, Chang JC, Teng LJ, Yang PC, Ho SW, Hsieh WC, Luh KT. Comparison of Etest and agar dilution method for antimicrobial susceptibility testing of Flavobacterium isolates. J Clin Microbiol 1997;35:1021-1023.[PubMed]
61. Hsueh PR, Hsiue TR, Wu JJ, Teng LJ, Ho SW, Hsieh WC, Luh KT. Flavobacterium indologenes bacteremia: clinical and microbiological characteristics. Clin Infect Dis 1996;23:550-555. [PubMed]
62. Hsueh PR, Teng LJ, Ho SW, Hsieh WC, Luh KT. Clinical and microbiological characteristics of Flavobacterium indologenes infections associated with indwelling devices. J Clin Microbiol 1996;34:1908-1913. [PubMed]
63. Hsueh PR, Teng LJ, Yang PC, Ho SW, Hsieh WC, Luh KT. Increasing incidence of nosocomial Chryseobacterium indologenes infections in Taiwan. Eur J Clin Microbiol Infect Dis 1997;16:568-574. [PubMed]
64. Hsueh PR, Teng LJ, Yang PC, Ho SW, Luh KT. Susceptibilities of Chryseobacterium indologenes andChryseobacterium meningosepticum to cefepime and cefpirome. J Clin Microbiol 1997;35:3323-3324. [PubMed]
65. Hsueh PR, Wu JJ, Hsiue TR, Hsieh WC. Bacteremic necrotizing fasciitis due to Flavobacterium odoratum. Clin Infect Dis 1995;21:1337-1338. [PubMed]
66. Jooste PJ, Hugo CJ. The taxonomy, ecology and cultivation of bacterial genera belonging to the family Flavobacteriaceae. Int J Food Microbiol 1999;53:81-94. [PubMed]
67. Jorgensen JH, Maher LA, Howell AW. Activity of meropenem against antibiotic-resistant or infrequently encountered gram-negative bacilli. Antimicrob Agents Chemother 1991;35:2410-2414. [PubMed]
68. Kang L, Millett PJ, Mezera K, Weiland AJ. Chronic plasma cell osteomyelitis of the humerus associated with Shigella and Flavobacterium. J Shoulder Elbow Surg 2001;10:292-294. [PubMed]
69. Kaplan M, Goldberg MD, Tauber Z, Solomon F, Sompolinsky D. Successful treatment of neonatalFlavobacterium meningosepticum infection. Eur J Pediatr 1983;140:337-338. [PubMed]
70. Kienzle N, Muller M, Pegg S. Chryseobacterium in burn wounds. Burns 2001;27:179-182. [PubMed]
71. Kim KK, Park HY, Park W, Kim IS, Lee ST. Microbacterium xylanilyticum sp. nov., a xylan-degrading bacterium isolated from a biofilm. Int J Syst Evol Microbiol. 2005;55:2075-9. [PubMed]
72. King E. Studies on a group of previously unclassified bacteria associated with meningitis in infants. Am J Clin Pathol 1959;31:241-247. [PubMed]
73. Kirby JT, Sader HS, Walsh TR, Jones RN. JT. Antimicrobial Susceptibility and Epidemiology of a Worldwide Collection of of Chryseobacterium spp.: Report from the SENTRY Antimicrobial Surveillance Program (1997–2001). J Clin Microbiol 2004;42:445–448. [PubMed]
74. Koneman EW, Allen SD, Janda WM, Schreckenberger PC, Winn WC. Color Atlas and Texbook of Diagnostic Microbiology. Fourth ed. Philadelphia: J. B. Lippincott Co; 1992.
75. Korzets Z, Maayan MC, Bernheim J. Flavobacterial peritonitis in patients treated by peritoneal dialysis. Nephrol Dial Transplant 1995;10:280-283. [PubMed]
76. Krebs S, Blanche P, Bouscary D, Gauther E, Dreyfus F, Sicard D, Blanchard H. Flavobacterium meningosepticum meningitis in an adult with acute leukaemia [Letter]. Postgrad Med J 1996;72:187-188. [PubMed]
77. Lapage SP, Owen RJ. Flavobacterium meningosepticum from cases of meningitis in Botswana and England. J Clin Pathol 1973;26:747-749. [PubMed]
78. Lee M, Munoz J. Septicemia occurring after colonoscopic polypectomy in a splenectomized patient taking corticosteroids. Am J Gastroenterol 1994;89:2245-2246. [PubMed]
79. LeFrancois M, Baum JL. Flavobacterium endophthalmitis following keratoplasty. Use of a tissue culture medium-stored cornea. Arch Ophthalmol 1976;94:1907-1909. [PubMed]
80. Lim LC, Low JA, Chan KM. Chryseobacterium meningosepticum (Flavobacterium meningosepticum): a report of five cases in a local hospital. Ann Acad Med Singapore 1999;28:858-860. [PubMed]
81. Lin YT, Jeng YY, Lin ML, Yu KW, Wang FD, Liu CY. Clinical and microbiological characteristics of Chryseobacterium indologenes bacteremia. J Microbiol Immunol Infect 2010;43:498-505. [PubMed]
82. Lin YT, Chiu CH, chan YJ, Lin ML, Yu KW, Wang FD, Liu CY. Clinical and microbiological analysis ofElizabethkingia meningoseptica bacteremia in adult patients in Taiwan. Scand J Infect Dis 2009;41:628-634.[PubMed]
83. Lin CH, Huang FY. [Clinical observation of neonatal meningitis caused by Flavobacterium meningosepticum]. Zhonghua Min Guo Xiao Er Ke Yi Xue Hui Za Zhi 1991;32:171-176. [PubMed]
84. Linder N, Korman SH, Eyal F, Michel J. Trimethoprim sulphamethoxazole in neonatal Flavobacterium meningosepticum infection. Arch Dis Child 1984;59:582-584. [PubMed]
85. Lu CH, Huang CR, Tsai NW, Chang CS, Chuang YC, Lee PY, Lei CB, Wang CB, Wang KW, Chang WN. An adult case of Chryseobacterium meningosepticum meningitis. Jpn J Infect Dis 2007;57:214-15. [PubMed]
86. Lu PC, Chan JC. Flavobacterium indologenes keratitis. Ophthalmologica 1997;211:98-100. [PubMed]
87. Lutsar I, McCracken GH Jr., Friedland IR. Antibiotic pharmacodynamics in cerebrospinal fluid. Clin Infect Dis 1998;27:1117-1127, quiz 1128-1129. [PubMed]
88. Macfarlane DE, Baum-Thureen P, Crandon I. Flavobacterium odoratum ventriculitis treated with intraventricular cefotaxime. J Infect 1985;11:233-238. [PubMed]
89. Madruga M, Zanon U, Pereira GM, Galvao AC. Meningitis caused by Flavobacterium meningosepticum. The first epidemic outbreak of meningitis in the newborn in South America. J Infect Dis 1970;121:328-330. [PubMed]
90. Manfredi R, Nanetti A, Ferri M, Mastroianni A, Coronado OV, Chiodo F. Flavobacterium spp. organisms as opportunistic bacterial pathogens during advanced HIV disease. J Infect 1999;39:146-152. [PubMed]
91. Mani RM, Kuruvila KC, Batliwala PM, Damle PN, Shirgaonkar GV, Soni RP, Vyas PR. Flavobacterium meningosepticum as an opportunist. J Clin Pathol 1978;31:220-222. [PubMed]
92. Maraki S, Scoulica E, et al. A Chryseobacterium meningosepticum colonization outbreak in a neonatal intensive care unit. Eur J Clin Microbiol Infect Dis. 2009;28:1415-1419. [PubMed]
93. Marnejon T, Watanakunakorn C. Flavobacterium meningosepticum septicemia and peritonitis complicating CAPD. Clin Nephrol 1992;38:176-177. [PubMed]
94. Matsumoto T, Nagata M, Ishimine N, Kawasaki K, Yamauchi K, Hidaka E, Kasuga E, Horiuchi K, Oana K, Kawakami Y, Honda T. Chacterization of CIA-1, an Ambler Class A Extended-Spectrum-Lactamase from Chryseobacterium indologenes. Antimicrob Agents Chemother 2012;56:588-90. [PubMed]
95. McGee SM, Kaplan SL, Mason EO Jr.. Ventricular fluid concentrations of vancomycin in children after intravenous and intraventricular administration. Pediatr Infect Dis J 1990;9:138-139. [PubMed]
96. Mermel LA, Farr BM, Sherertz RJ, Raad II, O'Grady N, Harris JS, Craven DE. Guidelines for the management of intravascular catheter-related infections. Clin Infect Dis 2001;32:1249-1272. [PubMed]
97. NCCLS. Performance Standards for Antimicrobial Susceptibility Testing: Eleventh Informational Supplement. Wayne, PA: National Committee for Clinical Laboratory Standards; 2001.
98. Nulens E, Bussels B, Bols A, Gordts B, Van Landuyt HW. Recurrent bacteremia by Chryseobacterium indologenes in an oncology patient with a totally implanted intravascular device. Clin Microbiol Infect 2001;7:391-393. [PubMed]
99. Olbrich P, Rivero-Garvia M, Falcon-Nevra MD, Lepe JA, Cisneros JM, Marquez-Rivas J, Neth O. Chryseobacterium indologenes central nervous system infection in infancy: an emergent pathogen? Infection 2014;42:179-183. [PubMed]
100. Olsen H, Ravn T. Flavobacterium meningosepticum isolated from the genitals. Acta Pathol Microbiol Scand [B] Microbiol Immunol 1971;79:102-106. [PubMed]
101. Olsen H, Frederiksen W, Siboni K. Flavobacterium meningosepticum in 8 non-fatal cases of postoperative bacteremia. Lancet 1965;1:1294-1296. [PubMed]
102. Overturf GD. Use of trimethoprim-sulfamethoxazole in pediatric infections: relative merits of intravenous administration. Rev Infect Dis 1987;9 Suppl 2:S168-176. [PubMed]
103. Ozkalay N, Anil M, Agus N, Helvaci M, Sirti S. Community-acquired meningitis and sepsis caused by Chryseobacterium meningosepticum in a patient diagnosed with thalasemia major. J Clin Microbiol 2006;44:3037-9. [PubMed]
104. Pen-Yi L, Chishih Chu, Lin-Hui Su, Chung-Tsui Huang, Wen-Ya Chang, and Cheng-Hsun Chiu. Clinical and Microbiological Analysis of Bloodstream Infections Caused by Chryseobacterium meningosepticum in Nonneonatal Patients. J Clin Micrbiol 2004;42:3353-3355.[PubMed]
105. Pickett MJ. Methods for identification of flavobacteria. J Clin Microbiol 1989;27:2309-2315. [PubMed]
106. Pitlik S, Berger SA, Huminer D. Nonenteric infections acquired through contact with water. Rev Infect Dis 1987;9:54-63. [PubMed]
107. Placzek M, Whitelaw A, Want S, Sahathevan M, Darrell J. Piperacillin in early neonatal infection. Arch Dis Child 1983;58:1006-1009. [PubMed]
108. Pokrywka M, Viazanko K, Medvick J, Knabe S, McCool S, Pasculle AW, Dowling JN. A Flavobacterium meningosepticum outbreak among intensive care patients. Am J Infect Control 1993;21:139-145. [PubMed]
109. Raimondi A, Moosdeen F, Williams JD. Antibiotic resistance pattern of Flavobacterium meningosepticum. Eur J Clin Microbiol 1986;5:461-463. [PubMed]
110. Ratner H. Flavobacterium meningosepticum. Infect Control 1984;5:237-239. [PubMed]
111. Rios I, Klimek JJ, Maderazo E, Quintiliani R. Flavobacterium meningosepticum meningitis: report of selected aspects. Antimicrob Agents Chemother 1978;14:444-447. [PubMed]
112. Rossolini GM, Franceschini N, Lauretti L, Caravelli B, Riccio ML, Galleni M, Frere J-M, Amicosante G. Cloning of a Chryseobacterium (Flavobacterium) meningosepticum chromosomal gene (blaA(CME)) encoding an extended-spectrum class A beta-lactamase related to the Bacteroides cephalosporinases and the VEB-1 and PER beta-lactamases. Antimicrob Agents Chemother 1999;43:2193-2199. [PubMed]
113. Rossolini GM, Franceschini N, Riccio ML, Mercuri PS, Perilli M, Galleni M, Frere JM, Amicosante G. Characterization and sequence of the Chryseobacterium (Flavobacterium) meningosepticum carbapenemase: a new molecular class B beta-lactamase showing a broad substrate profile. Biochem J 1998;332( Pt 1):145-52.[PubMed]
114. Sader HS, Jones RN, Pfaller MA. Relapse of catheter-related Flavobacterium meningosepticum bacteremia demonstrated by DNA macrorestriction analysis. Clin Infect Dis 1995;21:997-1000. [PubMed]
115. Sakuma, et al. Successful Treatment of Neonatal Meningitis Caused by Chryseobacterium meningosepticumWith Intravenous Ciprofloxacin and Trimethoprim-Sulfamethoxazole. Infectious Diseases in Clinical Practice. 2008;16:137-138.
116. Sato K, Fujii T, Okamoto R, Inoue M, Mitsuhashi S. Biochemical properties of beta-lactamase produced byFlavobacterium odoratum. Antimicrob Agents Chemother 1985;27:612-614. [PubMed]
117. Senquiz AL. Neonatal meningitis by Flavobacterium meningosepticum. Bol Asoc Med P R 1987;79:464-466.[PubMed]
118. Sheridan RL, Ryan CM, Pasternack MS, Weber JM, Tompkins RG. Flavobacterial sepsis in massively burned pediatric patients. Clin Infect Dis 1993;17:185-187. [PubMed]
119. Shewan JM, McMeekin TA. Taxonomy (and ecology) of Flavobacterium and related genera. Annu Rev Microbiol 1983;37:233-252. [PubMed]
120. Siegman-Igra Y, Schwartz D, Soferman G, Konforti N. Flavobacterium group IIb bacteremia: report of a case and review of Flavobacterium infections. Med Microbiol Immunol (Berl) 1987;176:103-111. [PubMed]
121. Skapek SX, Jones WS, Hoffman KM, Kuskie MR. Sinusitis and bacteremia caused by Flavobacterium meningosepticum in a sixteen-year-old with Shwachman Diamond syndrome. Pediatr Infect Dis J 1992;11:411-413.[PubMed]
122. Strandberg DA, Jorgensen JH, Drutz DJ. Activities of aztreonam and new cephalosporins against infrequently isolated gram-negative bacilli. Antimicrob Agents Chemother 1983;24:282-286. [PubMed]
123. Sztajnbok J, Troster EJ. Chryseobacterium meningosepticum pneumonia and sepsis in a previously healthy child. J Infect 1998;37:310-312. [PubMed]
124. Teres D. ICU-acquired pneumonia due to Flavobacterium meningosepticum. JAMA 1974;228:732. [PubMed]
125. Thong ML, Puthucheary SD, Lee EL. Flavobacterium meningosepticum infection: an epidemiological study in a newborn nursery. J Clin Pathol 1981;34:429-433. [PubMed]
126. Tizer KB, Cervia JS, Dunn AM, Stavola JJ, Noel GJ. Successful combination vancomycin and rifampin therapy in a newborn with community-acquired Flavobacterium meningosepticum neonatal meningitis. Pediatr Infect Dis J 1995;14:916-121. [PubMed]
127. Ursing J, Bruun B. Genetic heterogeneity of Flavobacterium meningosepticum demonstrated by DNA-DNA hybridization. Acta Pathol Microbiol Immunol Scand (B) 1987;95:33-39. [PubMed]
128. Valerga M, Armesto G, Gil Deza J, Gilabert G, Grandval S. [Post-splenectomy sepsis caused by Flavobacterium meningosepticum]. Enferm Infecc Microbiol Clin 2000;18:483-484. [PubMed]
129. Vancanneyt M, Segers P, Hauben L, Hommez J, Devriese LA, Hoste B, Vandamme P, Kersters K. Flavobacterium meningosepticum, a pathogen in birds. J Clin Microbiol 1994;32:2398-2403. [PubMed]
130. Vandamme P, Bernardet JF, Segers P, Kersters K, Holmes B. New perspectives in the classification of the Flavobacteria: description of Chryseobacterium gen. Nov., Bergeyella gen. Nov., and Empedobacter nom. Rev. Int J Syst Bacteriol 1994;44:827-831.
131. Visalli MA, Bajaksouzian S, Jacobs MR, Appelbaum PC. Comparative activity of trovafloxacin, alone and in combination with other agents, against gram-negative nonfermentative rods. Antimicrob Agents Chemother 1997;41:1475-1481. [PubMed]
132. Watanabe N, Katsu K, Moriyama M, Kitoh K. In vitro evaluation of E1040, a new cephalosporin with potent antipseudomonal activity. Antimicrob Agents Chemother 1988;32:693-701. [PubMed]
133. Watanabe NA. Newer antipseudomonal cephalosporins. J Chemother 1996;8 Suppl 2:48-56. [PubMed]
134. Watson KC, Krogh JG, Jones DT. Neonatal meningitis caused by Flavobacterium meningosepticum type F. J Clin Pathol 1966;19:79-80. [PubMed]
135. Weaver KN, Jones RC, Albright R, Thomas Y, Zambrano CH, Costello M, Havel J, Price J, Gerber S. Acute emergence of Elizabethkingia meningoseptica infection among mechanically ventilated patients in a long-term acute care facility. Infect Cont Hosp Epidemiol 2010;31:54-58. [PubMed]
136. Winslow DL, Pankey GA. Successful therapy with rifampin-Flavobacterium meningosepticum meningitis developing while on erythromycin therapy. Del Med J 1982;54:575-579. [PubMed]
137. Woodford N, Palepou MF, Babini GS, Holmes B, Livermore DM. Carbapenemases of Chryseobacterium (Flavobacterium) meningosepticum: distribution of blaB and characterization of a novel metallo-beta-lactamase gene, blaB3, in the type strain, NCTC 10016. Antimicrob Agents Chemother 2000;44:1448-1452. [PubMed]
138. Yannelli B, Koj IG, Cunha BA. Chryseobacterium meningosepticum bacteremia secondary to central intravenous line-related infection. Am J Infect Control 1999;27:533-535. [PubMed]
Tables
Table 1. In Vitro Susceptibilities of Elizabethkingia and Chryseobacterium Species a
| Antibiotic | n | Range | MIC50 | MIC90 | Breakpoint b | % Susceptible | Reference | |
|---|---|---|---|---|---|---|---|---|
| Minocycline | 58 | <0.25-4 | 1 | 2 | <4 | 100 | (48) c | |
| Levofloxacin | 58 | <0.5-8 | 1 | 2 | <2 | 98 | (48) | |
| Gentamicin | 19 | 4->64 | >64 | >64 | <4 | (67) d | ||
| Gentamicin | 28 | 32->128 | 64 | >128 | <4 | 0 | (1) e | |
| Cefazolin | 28 | 128->128 | 128 | >128 | <8 | 0 | (1) | |
| Cefepime | 58 | <1->64 | 64 | >64 | <4 | 10 | (48) | |
| Cefotaxime | 19 | 4->64 | 64 | >64 | <8 | (67) | ||
| Cefoxitin | 28 | 4-64 | 8 | 16 | <8 | (1) | ||
| Ceftazidime | 19 | 1->64 | >64 | >64 | <8 | (67) | ||
| Cephalothin | 28 | 128->128 | >128 | >128 | <8 | 0 | (1) | |
| Aztreonam | 19 | >64 | >64 | >64 | <8 | (67) | ||
| Imipenem | 19 | 2->16 | >16 | >16 | <4 | (67) | ||
| Imipenem | 58 | 2->16 | >16 | >16 | <4 | 17 | (48) | |
| Meropenem | 19 | 2->16 | 16 | >16 | (67) | |||
| Meropenem | 58 | 2->16 | >16 | >16 | <4 | 7 | (48) | |
| Tetracycline | 28 | 16-64 | 32 | 64 | <4 | 0 | (1) | |
| Ampicillin | 28 | 64->128 | >128 | >128 | (1) | |||
| Ampicillin | 18 | 1->128 | >128 | >128 | (53) | |||
| Amoxicillin-clavulinic acid | 18 | 1-32 | >32 | >32 | (53) | |||
| Piperacillin | 19 | <2-256 | 64 | 128 | <16 | (67) | ||
| Piperacillin-tazobactam | 58 | <2->128 | 64 | >128 | <16/4 | 29 | (48) | |
| Ticarcillin | 19 | 32->256 | 256 | >256 | <16 | (67) | ||
| Ticarcillin-clavulinic acid | 19 | 8->256 | 128 | >256 | <16/2 | (67) | ||
| Ticarcillin-clavulinic acid | 58 | 16->128 | >128 | >128 | <16/2 | 2 | (48) | |
| Cefclidin | 22 | 0.78->100 | 50 | >100 | (132) | |||
| Ciprofloxacin | 19 | 0.25->8 | 1 | 4 | <1 | (67) | ||
| Ciprofloxacin | 58 | 0.5-16 | 2 | 8 | <1 | 48 | (48) | |
| Clinafloxacin | 58 | <0.12-2 | 0.25 | 1 | (48) | |||
| Rifampicin | 28 | 0.25-2 | 1 | 2 | <1 | (1) | ||
| Rifampin | 58 | <0.12-4 | 1 | 2 | <2 | 88 | (48) | |
| Erythromycin | 28 | 32->128 | 128 | >128 | <0.5 | 0 | (1) | |
| Erythromycin | 58 | 2->32 | >32 | >32 | <0.5 | 0 | (48) | |
| Chloramphenicol | 28 | 64-128 | 128 | 128 | <8 | 0 | (1) | |
| Chloramphenicol | 58 | 16->64 | 64 | >64 | <8 | 0 | (48) | |
| Clindamycin | 28 | 0.5-8 | 4 | 8 | <0.5 | (1) | ||
| Clindamycin | 58 | 0.5->32 | 8 | 16 | <0.5 | 2 | (48) | |
| Trimethoprim- sulfamethoxazoleg | 28 | 0.15-1.25 | 0.62 | 1.25 | <2/38 | 100 | (1) | |
| Trimethoprim- sulfamethoxazoleg | 58 | 0.5->32 | 4 | 8 | <2/38 | 33 | (48) | |
| Sulfamethoxazole | 28 | 32-128 | 128 | 128 | (1) | |||
| Linezolid | 58 | 8->16 | >16 | >16 | (48) | |||
| Vancomycin | 58 | 16->64 | 32 | >64 | <4 | 0 | (48) | |
| Vancomycin | 28 | 8-16 | 16 | 16 | <4 | 0 | (1) | |
a Modified from (1, 48, 67, 136 )
b Current NCCLS interpretive standards for susceptibility (µg/ml) (96).
c The 58 isolates tested included: E. meningosepticum (38), C. indologenes (11), C. gleum (3), M. odoratum (4), and 4 unspeciated.
d The 19 isolates tested included: E. meningosepticum (10), C. indologenes (8), and one unspeciated.
e The 28 isolates tested included: E. meningosepticum (6) and other species (22)
f No information provided on the species tested
g Trimethoprim-sulfamethoxazole tested in a ratio of 1:19. Concentration refers to the trimethoprim component
Table 2. In Vitro Susceptibilities of Elizabethkingia Meningosepticum a
| Antibiotic | n | Range | MIC50 | MIC90 | Breakpoint b | % Susceptible | Reference |
|---|---|---|---|---|---|---|---|
| Amikacin | 9 | ≤2->64 | 64 | >64 | ≤16 | 22 | (114) |
| Amikacin | 18 | ≥64 | NS c | NS | ≤16 | 0 | (16) |
| Amikacin | 10 | ≥64 | >64 | NS | ≤16 | 0 | (45) |
| Amikacin | 8 | 8-64 | 32 | 32 | ≤16 | (119) | |
| Amikacin | 41 | 16->128 | 64 | >128 | ≤16 | (33) | |
| Gentamicin | 9 | 1->16 | >16 | >16 | ≤4 | 11 | (114) |
| Gentamicin | 18 | 2-≥16 | NS | NS | ≤4 | 6 | (16) |
| Gentamicin | 10 | 16->64 | >64 | NS | ≤4 | 0 | (45) |
| Gentamicin | 8 | 16-32 | 16 | 16 | ≤4 | 0 | (122) |
| Gentamicin | 41 | 8->128 | 64 | >128 | ≤4 | 0 | (33) |
| Kanamycin | 10 | >64 | >64 | NS | ≤16 | 0 | (45) |
| Netilmicin | 52 | 6.25->200 | 200 | >200 | ≤8 | (23) | |
| Netilmicin | 10 | >64 | >64 | NS | ≤8 | 0 | (45) |
| Netilmicin | 41 | 32->128 | >128 | >128 | ≤8 | 0 | (33) |
| Streptomycin | 10 | ≥64 | >64 | NS | (45) | ||
| Tobramycin | 18 | 8-≥16 | NS | NS | ≤4 | 0 | (16) |
| Tobramycin | 10 | >64 | >64 | NS | ≤4 | 0 | (45) |
| Ampicillin | 18 | 16-≥32 | NS | NS | (16) | ||
| Ampicillin | 52 | 2->200 | 100 | 200 | (23) | ||
| Ampicillin | 10 | 64->128 | 128 | NS | (45) | ||
| Mecillinam | 10 | >128 | >128 | NS | (45) | ||
| Penicillin | 52 | 6.25-100 | 50 | 50 | (23) | ||
| Penicillin | 10 | 16->128 | 64 | NS | (45) | ||
| Apalcillin d | 9 | 8-128 | 32 | 32 | (114) | ||
| Azlocillin | 10 | 32-64 | 64 | NS | (45) | ||
| Carbenicillin | 10 | >128 | >128 | NS | ≤16 | 0 | (45) |
| Mezlocillin | 18 | ≤16-≥256 | NS | NS | ≤16 | 67 | (16) |
| Mezlocillin | 10 | 8->128 | 32 | NS | ≤16 | (45) | |
| Piperacillin | 18 | ≤8-≥256 | NS | NS | ≤16 | 28 | (16) |
| Piperacillin | 52 | 1.6-12.5 | 6.25 | 12.5 | ≤16 | 100 | (23) |
| Piperacillin | 10 | 8-128 | 16 | NS | ≤16 | (45) | |
| Piperacillin | 41 | 1-32 | 4 | 8 | ≤16 | (33) | |
| Piperacillin-tazobactam | 9 | 2->128 | 64 | 64 | ≤16/4 | 22 | (114) |
| Ticarcillin | 18 | ≤16-≥256 | NS | NS | ≤16 | 22 | (16) |
| Ticarcillin | 10 | >128 | >128 | NS | ≤16 | 0 | (45) |
| Cefamandole | 10 | 32-128 | 64 | NS | ≤8 | 0 | (45) |
| Cefazolin | 18 | ≥32 | NS | NS | ≤8 | 0 | (16) |
| Cefazolin | 10 | ≥128 | >128 | NS | ≤8 | 0 | (45) |
| Cefepime | 21 | 0.5->256 | 64 | >256 | ≤8 | 19 | (64) |
| Cefoperazone | 8 | 16-32 | 32 | 32 | ≤16 | (122) | |
| Cefoperazone | 41 | 16->128 | 32 | 64 | ≤16 | (33) | |
| Cefpirome | 21 | 1->256 | 128 | >256 | 19 | (64) | |
| Cefotaxime | 52 | 1.6-50 | 12.5 | 25 | ≤8 | (23) | |
| Cefotaxime | 10 | 16-64 | 32 | NS | ≤8 | 0 | (45) |
| Cefotaxime | 8 | 16-64 | 16 | 32 | ≤8 | 0 | (122) |
| Cefotaxime | 41 | 16->128 | 32 | 128 | ≤8 | 0 | (33) |
| Cefoxitin | 18 | 8-≥32 | NS | NS | ≤8 | 11 | (16) |
| Cefoxitin | 10 | 4-64 | 8 | NS | ≤8 | (45) | |
| Cefsulodin | 8 | ≥128 | ≥128 | ≥128 | (122) | ||
| Ceftazidime | 18 | ≤8-≥32 | NS | NS | ≤8 | 6 | (16) |
| Ceftazidime | 52 | 6.25-200 | 50 | 100 | ≤8 | (23) | |
| Ceftazidime | 8 | ≥128 | ≥128 | ≥128 | ≤8 | 0 | (122) |
| Ceftazidime | 41 | 2->128 | >128 | >128 | ≤8 | (33) | |
| Ceftazidime | 10 | 4-256 | 128 | 256 | ≤8 | (122) | |
| Ceftizoxime | 8 | 2-32 | 4 | 16 | ≤8 | (122) | |
| Ceftriaxone | 18 | 16-≥64 | NS | NS | ≤8 | 0 | (16) |
| Ceftriaxone | 41 | 16->128 | 64 | 128 | ≤8 | 0 | (33) |
| Cefuroxime | 52 | 25->200 | 200 | >200 | ≤8 | 0 | (23) |
| Cefuroxime | 10 | ≥128 | ≥128 | NS | ≤8 | 0 | (45) |
| Cephalothin | 52 | 25->200 | 200 | >200 | ≤8 | 0 | (23) |
| Cephalothin | 10 | 64->128 | 128 | NS | ≤8 | 0 | (45) |
| Cephalothin | 41 | >128->128 | >128 | >128 | ≤8 | 0 | (33) |
| Moxalactam | 10 | 16->128 | 64 | NS | ≤8 | 0 | (45) |
| Moxalactam | 8 | 16-64 | 16 | 32 | ≤8 | 0 | (119) |
| Moxalactam | 41 | 8->128 | 64 | 128 | ≤8 | (33) | |
| Aztreonam | 18 | ≤8-≥32 | NS | NS | ≤8 | 11 | (16) |
| Aztreonam | 8 | ≥128 | ≥128 | ≥128 | ≤8 | 0 | (122) |
| Aztreonam | 41 | 128->128 | >128 | >128 | ≤8 | 0 | (33) |
| Biapenem | 9 | 4-8 | 8 | 8 | (114) | ||
| Imipenem | 18 | ≥16 | NS | NS | ≤4 | 0 | (16) |
| Imipenem | 8 | 16-32 | 16 | 32 | ≤4 | 0 | (122) |
| Imipenem | 41 | 1-128 | 64 | 64 | ≤4 | (33) | |
| Imipenem | 10 | 1-64 | 8 | 64 | ≤4 | (131) | |
| Meropenem | 9 | 8->8 | 8 | >8 | (114) | ||
| Thienamycin | 52 | 1.6-50 | 25 | 50 | (23) | ||
| Chloramphenicol | 52 | 6.25->200 | 50 | 100 | ≤8 | (23) | |
| Chloramphenicol | 10 | 32>64 | 64 | NS | ≤8 | 0 | (45) |
| Clindamycin | 9 | 0.5-8 | 4 | 8 | ≤0.5 | 11 | (114) |
| Clindamycin | 52 | 0.025-3.1 | 0.8 | 3.1 | ≤0.5 | (23) | |
| Clindamycin | 10 | 0.5-16 | 1 | NS | ≤0.5 | (45) | |
| Ciprofloxacin | 9 | 0.5-2 | 1 | 2 | ≤1 | 67 | (114) |
| Ciprofloxacin | 18 | <0.5-2 | NS | NS | ≤1 | 94 | (16) |
| Ciprofloxacin | 52 | 0.1-6.25 | 0.8 | 3.1 | ≤1 | (23) | |
| Ciprofloxacin | 41 | 0.5-16 | 1 | 8 | ≤1 | (33) | |
| Ciprofloxacin | 10 | 0.5-8 | 2 | 8 | ≤1 | (131) | |
| Clinafloxacin | 9 | 0.12-1 | 0.25 | 0.5 | (114) | ||
| Clinafloxacin | 10 | 0.25-4 | 1 | 4 | (131) | ||
| Levofloxacin | 10 | 1-2 | 2 | 2 | ≤2 | (131) | |
| DU-6859a | 9 | 1->4 | 2 | >4 | (114) | ||
| Ofloxacin | 9 | 0.06-0.25 | 0.25 | 0.25 | ≤2 | 100 | (114) |
| Ofloxacin | 18 | ≤1-4 | NS | NS | ≤2 | 83 | (16) |
| Ofloxacin | 41 | 1-8 | 2 | 4 | v2 | (33) | |
| Ofloxacin | 10 | 1-4 | 4 | 4 | v2 | (131) | |
| Sparfloxacin | 10 | 0.016-4 | 0.5 | 4 | (131) | ||
| Trovafloxacin | 10 | 0.03-4 | 1 | 4 | (131) | ||
| Colistin | 10 | >64 | >64 | NS | (45) | ||
| Trimethoprim-sulfamethoxazole e | 18 | ≤0.5-4 | NS | NS | ≤2/38 | 72 | (16) |
| Trimethoprim-sulfamethoxazole | 10 | 3.2->6.4 | >6.4 | NS | ≤2/38 | 0 | (45) |
| Trimethoprim | 41 | 1->16 | 8 | >16 | (33) | ||
| Erythromycin | 52 | 0.1-200 | 0.8 | 3.1 | ≤0.5 | (23) | |
| Erythromycin | 10 | 4-32 | 8 | NS | v0.5 | 0 | (45) |
| Erythromycin | 41 | 8->128 | 16 | >128 | ≤0.5 | 0 | (33) |
| Clarithromycin | 9 | 1.5-16 | 6 | 8 | v2 | 11 | (114) |
| Everninomicin | 9 | 2-8 | 2 | 2 | (114) | ||
| Fusidic acid | 52 | 3.1->200 | 100 | >200 | (23) | ||
| Rifampin | 52 | 0.2-3.1 | 0.8 | 3.1 | ≤1 | (23) | |
| Rifampin | 9 | 0.5-1 | 1 | 1 | ≤1 | 100 | (114) |
| Doxycycline | 9 | 1-16 | 2 | 4 | ≤4 | 89 | (114) |
| Doxycycline | 10 | 1-32 | 4 | NS | ≤4 | (45) | |
| Minocycline | 10 | 0.5-4 | 1 | NS | ≤4 | 100 | (45) |
| Minocycline | 41 | 1-8 | 2 | 4 | ≤4 | (33) | |
| Tetracycline | 52 | 25-200 | 100 | 100 | ≤4 | (23) | |
| Tetracycline | 10 | 32->64 | 64 | NS | £4 | 0 | (45) |
| Vancomycin | 9 | 8-32 | 16 | 16 | v4 | 0 | (114) |
| Vancomycin | 52 | 3.1-50 | 12.5 | 50 | £4 | (23) | |
| Vancomycin | 10 | 8-32 | 16 | NS | v4 | 0 | (45) |
| Vancomycin | 41 | 4-32 | 16 | 16 | v4 | (33) | |
| Teicoplanin | 9 | 8-32 | 8 | 16 | ≤8 | 56 | (114) |
| Teicoplanin | 41 | 8-64 | 16 | 32 | ≤8 | (33) |
a Modified from (16, 23, 33, 45, 64, 115, 119, 128).
b Current NCCLS interpretive standards for susceptibility (µg/ml) (95)
c NS = not stated.
d Apalcillin in combinations with a ß-lactamase inhibitor, Ro48-1220 (4µg/ml).
e Trimethoprim-sulfamethoxazole tested in a ratio of 1:19. Concentration refers to the trimethoprim component.
Table 3. In Vitro Susceptibilities of Chryseobacterium Indologenes a
| Antibiotic | n | Range | MIC50 | MIC90 | Breakpoint b | % Susceptible | Reference | ||
|---|---|---|---|---|---|---|---|---|---|
| Amikacin | 12 | 32->128 | 64 | >128 | ≤16 | 0 | (61) | ||
| Amikacin | 10 | 8-64 | 16 | NS c | ≤16 | (45) | |||
| Amikacin | 4 | 2-32 | 8 | 32 | ≤16 | (119) | |||
| Amikacin | 59 | 32-128 | 128 | >128 | ≤16 | 0 | (33) | ||
| Gentamicin | 12 | 8->128 | 64 | >128 | ≤4 | 0 | (61) | ||
| Gentamicin | 10 | 2-16 | 8 | NS | ≤4 | (45) | |||
| Gentamicin | 4 | 1-16 | 4 | 16 | ≤4 | (119) | |||
| Gentamicin | 59 | 8->128 | 128 | >128 | ≤4 | 0 | (33) | ||
| Kanamycin | 10 | ≥64 | ≥64 | NS | ≤16 | 0 | (45) | ||
| Netilmicin | 12 | 64->128 | >128 | >128 | ≤8 | 0 | (61) | ||
| Netilmicin | 10 | 8-64 | 16 | NS | ≤8 | (45) | |||
| Netilmicin | 59 | 16->128 | >128 | >128 | ≤8 | 0 | (33) | ||
| Streptomycin | 10 | 2->64 | 8 | NS | (45) | ||||
| Tobramycin | 10 | ≥64 | ≥64 | NS | ≤4 | 0 | (45) | ||
| Penicillin | 18 | 2->128 | >128 | >128 | (53) | ||||
| Penicillin | 10 | 4-128 | 8 | NS | (45) | ||||
| Ampicillin | 10 | 8->128 | 16 | NS | (45) | ||||
| Ampicillin | 18 | 1->128 | >128 | >128 | (53) | ||||
| Amoxicillin-clavulinic acid | 18 | 1-32 | 32 | 32 | ≤8/4 | 11 | (53) | ||
| Mecillinam | 10 | 64->128 | 128 | NS | (45) | ||||
| Azlocillin | 10 | 0.5-16 | 2 | NS | (45) | ||||
| Carbenicillin | 10 | 32->128 | 32 | NS | ≤16 | 0 | (45) | ||
| Mezlocillin | 10 | 1-8 | 4 | NS | ≤16 | 100 | (45) | ||
| Piperacillin | 12 | 1-8 | 2 | 4 | ≤16 | 100 | (61) | ||
| Piperacillin | 10 | 0.25-4 | 1 | NS | ≤16 | 100 | (45) | ||
| Piperacillin | 59 | 1->128 | 4 | 128 | ≤16 | (33) | |||
| Ticarcillin | 10 | 16->128 | 32 | NS | ≤16 | (45) | |||
| Cefadroxyl | 18 | 8->128 | >128 | >128 | (53) | ||||
| Cefamandole | 10 | 64->128 | 128 | NS | ≤8 | 0 | (45) | ||
| Cefazolin | 10 | 32->128 | 64 | NS | ≤8 | 0 | (45) | ||
| Cefoperazone | 12 | 4->128 | 8 | 16 | ≤16 | 92 | (61) | ||
| Cefoperazone | 4 | 2-8 | 4 | 8 | ≤16 | 100 | (119) | ||
| Cefoperazone | 59 | 2->128 | 16 | >128 | ≤16 | (33) | |||
| Cefotaxime | 12 | 16->128 | 32 | 64 | ≤8 | 0 | (61) | ||
| Cefotaxime | 10 | 2-32 | 8 | NS | ≤8 | (45) | |||
| Cefotaxime | 4 | 1-32 | 16 | 32 | ≤8 | (119) | |||
| Cefotaxime | 59 | 4->128 | 64 | >128 | ≤8 | (33) | |||
| Cefoxitin | 10 | 4-64 | 8 | NS | ≤8 | (45) | |||
| Cefsulodin | 4 | ≥128 | ≥128 | ≥128 | (119) | ||||
| Ceftazidime | 12 | 2->128 | 8 | 8 | ≤8 | 92 | (61) | ||
| Ceftazidime | 4 | 0.5-4 | 2 | 4 | ≤8 | 100 | (119) | ||
| Ceftazidime | 59 | 2->128 | 8 | 32 | ≤8 | (33) | |||
| Ceftazidime | 9 | 2->256 | 16 | NS | ≤8 | (128)d | |||
| Cefepime | 96 | 0.25->256 | 4 | 16 | ≤8 | 73 | (64) | ||
| Cefpirome | 96 | 0.25->256 | 8 | 128 | 64 | (64) | |||
| Ceftizoxime | 4 | 4-32 | 16 | 32 | ≤8 | (119) | |||
| Ceftriaxone | 12 | 16->128 | 32 | 64 | ≤8 | 0 | (61) | ||
| Ceftriaxone | 59 | 16->128 | 32 | >128 | ≤8 | 0 | (33) | ||
| Cefuroxime | 18 | 1->128 | >128 | >128 | ≤8 | 6 | (53) | ||
| Cefuroxime | 10 | 16->128 | 32 | NS | ≤8 | 0 | (45) | ||
| Cephalexin | 18 | 8->128 | >128 | >128 | (53) | ||||
| Cephalothin | 12 | 32->128 | >128 | >128 | ≤8 | 0 | (61) | ||
| Cephalothin | 10 | 16->128 | 64 | NS | ≤8 | 0 | (45) | ||
| Cephalothin | 59 | 32->128 | >128 | >128 | ≤8 | 0 | (33) | ||
| Moxalactam | 12 | 32->128 | 64 | >128 | ≤8 | 0 | (61) | ||
| Moxalactam | 10 | 16-64 | 16 | NS | ≤8 | 0 | (45) | ||
| Moxalactam | 4 | 8-32 | 8 | 32 | ≤8 | (119) | |||
| Moxalactam | 59 | 32->128 | 64 | 128 | ≤8 | 0 | (33) | ||
| Aztreonam | 12 | >128 | >128 | >128 | ≤8 | 0 | (61) | ||
| Aztreonam | 4 | ≥128 | ≥128 | ≥128 | ≤8 | 0 | (119) | ||
| Aztreonam | 59 | >128->128 | >128 | >128 | ≤8 | 0 | (33) | ||
| Imipenem | 12 | 32->128 | 64 | 64 | ≤4 | 0 | (61) | ||
| Imipenem | 4 | 4-32 | 4 | 32 | ≤4 | (119) | |||
| Imipenem | 59 | 1->128 | 64 | >128 | ≤4 | (33) | |||
| Imipenem | 9 | 1-64 | 32 | NS | ≤4 | (128)d | |||
| Chloramphenicol | 10 | 32->64 | 32 | NS | ≤8 | 0 | (45) | ||
| Clindamycin | 12 | 4 | 4 | 4 | ≤0.5 | 0 | (61) | ||
| Clindamycin | 10 | 0.13->64 | 0.5 | NS | ≤0.5 | (45) | |||
| Ciprofloxacin | 12 | 0.5-128 | 1 | 32 | ≤1 | 67 | (61) | ||
| Ciprofloxacin | 18 | 0.5-1 | 0.5 | 0.5 | ≤1 | 100 | (53) | ||
| Ciprofloxacin | 59 | 0.25-128 | 2 | 128 | ≤1 | (33) | |||
| Ciprofloxacin | 9 | 0.25-8 | 1 | NS | ≤1 | (128)d | |||
| Clinafloxacin | 9 | 0.125-2 | 0.5 | (128)d | |||||
| Enoxacin | 18 | 0.5-4 | 1 | 2 | ≤2 | 94 | (53) | ||
| Levofloxacin | 9 | 0.25-4 | 1 | NS | ≤2 | (131)d | |||
| Ofloxacin | 12 | 2-64 | 2 | 32 | ≤2 | 50 | (61) | ||
| Ofloxacin | 18 | 0.25-2 | 0.25 | 1 | ≤2 | 100 | (53) | ||
| Gatifloxacin | 20 | 0.25- | 0.25 | 1 | 95 | (73) | |||
| Garenoxacinb | 20 | 0.12- | 2 | ≤2 | 95 | (73) | |||
| Ofloxacin | 59 | 0.5-64 | 8 | 64 | ≤2 | (33) | |||
| Ofloxacin | 9 | 0.5-8 | 2 | NS | ≤2 | (131)d | |||
| Sparfloxacin | 9 | 0.016-2 | 0.25 | NS | (131)d | ||||
| Trovofloxacin | 9 | 0.016-2 | 0.125 | NS | (131)d | ||||
| Trimethoprim-sulfamethoxazole e | 12 | 0.5-16 | 2 | 16 | ≤2/38 | 50 | (61) | ||
| Trimethoprim-sulfamethoxazole | 10 | 0.2-1.6 | 0.4 | NS | ≤2/38 | 100 | (45) | ||
| Trimethoprim | 59 | 0.25-16 | 4 | 16 | (33) | ||||
| Erythromycin | 12 | 64->128 | >128 | >128 | ≤0.5 | 0 | (61) | ||
| Erythromycin | 10 | 1-16 | 2 | NS | ≤0.5 | 0 | (45) | ||
| Erythromycin | 59 | 8->128 | 128 | >128 | ≤0.5 | 0 | (33) | ||
| Doxycycline | 10 | 1-8 | 4 | NS | ≤4 | (45) | |||
| Minocycline | 12 | 2-16 | 4 | 4 | ≤4 | 92 | (61) | ||
| Minocycline | 10 | 1-4 | 1 | NS | ≤4 | 100 | (45) | ||
| Minocycline | 59 | 1-16 | 4 | 8 | ≤4 | (33) | |||
| Tetracycline | 18 | 4-32 | 16 | 32 | ≤4 | 29 | (53) | ||
| Tetracycline | 10 | 4-32 | 16 | NS | ≤4 | (45) | |||
| Vancomycin | 12 | 2-128 | 16 | 16 | ≤4 | 8 | (61) | ||
| Vancomycin | 10 | 16->64 | 16 | NS | ≤4 | 0 | (45) | ||
| Vancomycin | 59 | 2->128 | 16 | 16 | ≤4 | (33) | |||
| Teicoplanin | 12 | 32-64 | 32 | 64 | ≤8 | 0 | (61) | ||
| Teicoplanin | 59 | 16->128 | 32 | 32 | ≤8 | 0 | (33) | ||
| Colistin | 10 | >64 | >64 | NS | (45) | ||||
a Modified from (33, 44, 53, 61, 119, 131).
b Current NCCLS interpretive standards for susceptibility (µg/ml) (98)
c NS = not stated.
d Includes Chryseobacterium gleum strains
e Trimethoprim-sulfamethoxazole tested in a combination of 1:19. Concentration refers to the trimethoprim component.
Table 4. In Vitro Susceptibilities of Myroides Species a
| Antibiotic | n | Range | MIC50 | MIC90 | Breakpoint b | % Susceptible | Reference |
|---|---|---|---|---|---|---|---|
| Amikacin | 5 | >64 | >64 | NS c | ≤16 | 0 | (45) |
| Amikacin | 17 | 64->128 | >128 | >128 | ≤16 | 0 | (58) |
| Amikacin | 6 | >128->128 | >128 | NS | ≤16 | 0 | (45) |
| Gentamicin | 5 | >64 | >64 | NS | ≤4 | 0 | (45) |
| Gentamicin | 26 | 64->128 | >128 | >128 | ≤4 | 0 | (58) |
| Gentamicin | 6 | >128->128 | >128 | NS | ≤4 | 0 | (45) |
| Kanamycin | 5 | >64 | >64 | NS | ≤16 | 0 | (45) |
| Kanamycin | 26 | >128 | >128 | >128 | ≤16 | 0 | (58) |
| Netilmicin | 5 | >64 | >64 | NS | ≤8 | 0 | (45) |
| Netilmicin | 6 | >128->128 | >128 | NS | ≤8 | 0 | (45) |
| Streptomycin | 5 | >64 | >64 | NS | (45) | ||
| Streptomycin | 26 | 64->128 | >128 | >128 | (58) | ||
| Tobramycin | 5 | >64 | >64 | NS | ≤4 | 0 | (45) |
| Tobramycin | 17 | >128 | >128 | >128 | ≤4 | 0 | (58) |
| Ampicillin | 5 | 1->128 | 16 | NS | (45) | ||
| Ampicillin | 26 | 4->128 | 32 | 128 | (58) | ||
| Penicillin | 5 | 1->128 | 4 | NS | (45) | ||
| Mecillinam | 5 | >128 | >128 | NS | (45) | ||
| Azlocillin | 5 | 16->128 | 16 | NS | (45) | ||
| Carbenicillin | 5 | 8->128 | 128 | NS | ≤16 | (45) | |
| Carbenicillin | 26 | 32->128 | 128 | >128 | ≤16 | 0 | (58) |
| Mezlocillin | 5 | 8->128 | 16 | NS | ≤16 | (45) | |
| Piperacillin | 5 | 16->128 | 16 | NS | ≤16 | (45) | |
| Piperacillin | 6 | 4->128 | >128 | NS | ≤16 | (33) | |
| Ticarcillin | 5 | 1->128 | 64 | NS | ≤16 | (45) | |
| Cefamandole | 5 | ≥128 | ≥128 | NS | ≤8 | 0 | (45) |
| Cefuroxime | 5 | 128 | 128 | NS | ≤8 | 0 | (45) |
| Cefazolin | 5 | ≥128 | ≥128 | NS | ≤8 | 0 | (45) |
| Cefoperazone | 6 | 16->128 | >128 | NS | ≤16 | (33) | |
| Cefotaxime | 5 | 64-128 | 64 | NS | ≤8 | 0 | (45) |
| Cefotaxime | 6 | 64->128 | >128 | NS | ≤8 | 0 | (33) |
| Ceftazidime | 6 | 4->128 | >128 | NS | ≤8 | (33) | |
| Ceftriaxone | 6 | 128->128 | >128 | NS | ≤8 | 0 | (33) |
| Cephaloridine | 26 | 1-128 | 8 | 16 | (58) | ||
| Cephalothin | 5 | 64->128 | 64 | NS | ≤8 | 0 | (45) |
| Cephalothin | 6 | 128->128 | >128 | NS | ≤8 | 0 | (33) |
| Moxalactam | 5 | 8-128 | 32 | NS | ≤8 | (45) | |
| Moxalactam | 6 | 16-64 | 64 | NS | ≤8 | 0 | (33) |
| Aztreonam | 6 | 32->128 | >128 | NS | ≤8 | 0 | (33) |
| Imipenem | 6 | 8-32 | 16 | NS | ≤4 | 0 | (33) |
| Chloramphenicol | 5 | 4-32 | 32 | NS | ≤8 | (45) | |
| Chloramphenicol | 26 | 4->128 | 16 | 32 | ≤8 | (58) | |
| Clindamycin | 5 | 0.13-1 | 0.5 | NS | ≤0.5 | (45) | |
| Ciprofloxacin | 6 | 1-64 | 32 | NS | ≤1 | (33) | |
| Ofloxacin | 6 | 2-64 | 32 | NS | ≤2 | (33) | |
| Colistin | 5 | >64 | >64 | NS | (45) | ||
| Trimethoprim-sulfamethoxazole d | 5 | 0.4->6.4 | >6.4 | NS | ≤2/38 | (45) | |
| Trimethoprim- sulfamethoxazole | 26 | 0.2->6.4 | 3.2 | 6.4 | ≤2/38 | (58) | |
| Sulfamethoxazole | 26 | 1->128 | >128 | >128 | (58) | ||
| Trimethoprim | 6 | 4->16 | >16 | NS | (33) | ||
| Erythromycin | 5 | 4 | 4 | NS | ≤0.5 | 0 | (45) |
| Erythromycin | 26 | <1->128 | 2 | 4 | ≤0.5 | (58) | |
| Erythromycin | 6 | 64->128 | >128 | NS | ≤0.5 | 0 | (33) |
| Minocycline | 5 | 0.5-2 | 0.5 | NS | ≤4 | 100 | (45) |
| Minocycline | 6 | 2-8 | 2 | NS | ≤4 | (33) | |
| Doxycycline | 5 | 0.5-8 | 1 | NS | ≤4 | (45) | |
| Tetracycline | 5 | 4->64 | 64 | NS | ≤4 | (45) | |
| Tetracycline | 26 | 4-128 | 64 | 128 | ≤4 | (58) | |
| Vancomycin | 5 | 32->64 | >64 | NS | ≤4 | 0 | (45) |
| Vancomycin | 6 | 16-64 | 64 | NS | ≤4 | 0 | (33) |
| Teicoplanin | 6 | 16->128 | >128 | NS | ≤8 | 0 | (33) |
| Polymyxin B | 26 | 64->128 | >128 | >128 | (58) | ||
| Nalidixic acid | 26 | 8-32 | 8 | 16 | (58) |
a Modified from, (33, 45, 58, 131).
b Current NCCLS interpretive standards for susceptibility (µg/ml) (97)
c NS = not stated.
d Trimethoprim-sulfamethoxazole tested in a ratio of 1:19. Concentration refers to the trimethoprim component.
What's New
Sakuma, et al. Successful Treatment of Neonatal Meningitis Caused by Chryseobacterium meningosepticum With Intravenous Ciprofloxacin and Trimethoprim-Sulfamethoxazole. Infectious Diseases in Clinical Practice; 16(2):137-138, March 2008.