|Year : 2017 | Volume
| Issue : 4 | Page : 610-616
Increased recognition of Chryseobacterium species as an emerging cause of nosocomial urinary tract infection following introduction of matrix-assisted laser desorption/ionisation-time of flight for bacterial identification
Harsimran Kaur1, Balvinder Mohan1, Vinaykumar Hallur1, Atul Raj1, Madhunarayana Basude2, Ravimohan S Mavuduru3, Neelam Taneja1
1 Department of Medical Microbiology, PGIMER, Chandigarh, India
2 Department of General Surgery, PGIMER, Chandigarh, India
3 Department of Urology, PGIMER, Chandigarh, India
|Date of Web Publication||1-Feb-2018|
Dr. Neelam Taneja
Department of Medical Microbiology, Postgraduate Institute of Medical Education and Research, Chandigarh
Source of Support: None, Conflict of Interest: None
Chryseobacterium species are rarely reported as aetiological agents of nosocomial urinary tract infection. Here, we evaluated the clinical significance of 19 isolates of Chryseobacterium species (15 Chryseobacterium indologenes and 4 Chryseobacterium gleum; identified by matrix-assisted laser desorption/ionisation-time of flight [MALDI-TOF]) obtained from urine or percutaneous nephrostomy drainage of 16 patients with urological complaints. The strains possessed drug resistance to multiple antibiotics. 14 isolates showed the presence of carbapenemases. Both MALDI-TOF and repetitive sequence-based-polymerase chain reaction grouped them into three clusters (Kappa 1.000). They may colonise the urinary tract acting as a reservoir for dissemination of drug resistance within hospital environment.
Keywords: Chryseobacterium, drug resistance, matrix-assisted laser desorption/ionisation, repetitive sequence-based polymerase chain reaction, urinary tract infection
|How to cite this article:|
Kaur H, Mohan B, Hallur V, Raj A, Basude M, Mavuduru RS, Taneja N. Increased recognition of Chryseobacterium species as an emerging cause of nosocomial urinary tract infection following introduction of matrix-assisted laser desorption/ionisation-time of flight for bacterial identification. Indian J Med Microbiol 2017;35:610-6
|How to cite this URL:|
Kaur H, Mohan B, Hallur V, Raj A, Basude M, Mavuduru RS, Taneja N. Increased recognition of Chryseobacterium species as an emerging cause of nosocomial urinary tract infection following introduction of matrix-assisted laser desorption/ionisation-time of flight for bacterial identification. Indian J Med Microbiol [serial online] 2017 [cited 2021 Jan 26];35:610-6. Available from: https://www.ijmm.org/text.asp?2017/35/4/610/224412
| ~ Introduction|| |
Chryseobacterium species is one of the emerging pathogens among the non-fermenting organisms. They are ubiquitous in nature being present in soil, plants, food and water sources, especially in hospital environment. However, they do not form a part of human microbiota. The genus Chryseobacterium was previously called as Flavobacterium.Chryseobacterium meningosepticum, known to cause meningitis and sepsis in neonates and immunosuppressed patients is considered to be the most pathogenic species of this genus. Chryseobacterium indologenes and Chryseobacterium gleum are emerging pathogenic species most commonly causing nosocomial infections. They have been isolated from patients with bacteraemia, meningitis, pneumonia, peritonitis, ocular infections and long-term indwelling devices., The frequent administration of carbapenems may help in selecting out this group, especially in health-care settings. The members of Chryseobacterium genus are known for their multidrug resistance. Hence, it is important to identify these organisms considering high mortality caused by these pathogens, especially in patients of bacteraemia and pneumonia. The conventional methods of identification are limited by being too cumbersome and time-consuming. Rapid and accurate identification of these organisms is possible by using matrix-assisted laser desorption/ionisation-time of flight (MALDI-TOF) or molecular techniques like polymerase chain reaction (PCR)., Data regarding infections caused by Chryseobacterium species is very sparse in India. Moreover, very few scattered case reports of C. indologenes' isolation form urine are available.,, Therefore, this study was planned after observing a sudden isolation of Chryseobacterium species from urine samples over a short period of duration from a single ward. The aim of the present study was to establish the clinical significance of these isolates, determine their antibiotic susceptibility, presence of carbapenemases and to compare the epidemiological typing of these isolates by MALDI-TOF and repetitive sequence-based (REP) PCR.
| ~ Methods|| |
A total of 16 patients admitted in urology ward at our tertiary care hospital were identified from August 2013 to November 2013 who grew C. indologenes or C. gleum in their urine samples. All relevant data including clinical manifestations, underlying diseases, comorbidities, date and duration of urinary catheter (if present), blood culture and outcome were recorded from the patient clinical records. Urinary tract infection in catheterised patients was considered according to standard guidelines of Centers for Disease Control and Prevention (CDC).
A total of 19 isolates were isolated from 16 patients on cystine-lactose-electrolyte-deficient (CLED) (HiMedia) medium after overnight incubation at 37°C. The isolates were identified by both conventional standard methods and by using Bruker MALDI Biotyper 3.1 mass spectrometer. A score of 2.300–3.000 and 2.000–2.299 signifies highly probable and probable species identification, respectively.
Antimicrobial susceptibility testing
Antimicrobial susceptibility testing was done on Muller Hinton agar (HiMedia) using Kirby Bauer disc diffusion method according to the Clinical and Laboratory Standards Institute (CLSI). For interpretation, we referred to the zone diameters for Pseudomonas aeruginosa, Enterococcus (Vancomycin), and Staphylococcus (Linezolid).
Modified Hodge test
Carbapenemase production by the isolates was detected by modified Hodge test (MHT) according to CLSI. The cloverleaf-shaped zone of inhibition due to the production of carbapenemase by the test strain was considered to be positive.
Repetitive sequence-based polymerase chain reaction
All the 19 isolates were subjected to molecular typing using REP-PCR as described earlier with few modifications. In brief, single bacterial colony was suspended in 100 μl of distilled water and boiled for 15 min. It was then centrifuged at 13000 rpm for 5 min. A volume of 5 μl of supernatant was used as the DNA template. REP-PCR was performed using consensus primers (Sigma) namely REP 1 (5'-IIIGCGCCGICATCAGGC-3') and REP 2 (5'-ACGTCTTATCAGGCCTAC-3'). A no template control containing all components and 5 μl of sterile distilled H2O (which was used to prepare the master mix), was included in each PCR run, to rule out reagent contamination. The procedures for amplification by PCR were followed as described previously. Aliquots (12 μl) of each sample were subjected to electrophoresis in 1.5% agarose gels. Amplified products were detected by ethidium bromide staining. The gel picture was imported to BioNumerics 7 and dendrogram was constructed using the band based UPGMA protocol. Only those strains with ≥7 bands (between 100 and 1500 bp) were included for analysis.
Main spectra dendrogram analysis
MALDI-TOF MS profile analyses was used to construct a dendrogram by Biotyper main spectra (MSP) dendrogram creation standard method.
To see the agreement between typing methods, REP-PCR and MSP dendrogram analysis, kappa test of agreement was applied using SPSS version 17.0 software (SPSS Inc., Chicago, IL).
| ~ Results|| |
Clinical characteristics of the patients and antimicrobial therapy for the isolates with outcome of patients are given in [Table 1]. The mean age of the patients was 47.06 years and 56.25% of them were males. The most common underlying aetiologies were renal stone disease (RSD, n = 9), carcinoma urinary bladder (n = 5) or ureter (n = 1). Other comorbidities included diabetes mellitus (DM) (n = 4), hypertension (n = 2), rheumatoid arthritis (n = 1) and chronic obstructive pulmonary disease (n = 1). All of the patients were either catheterised or had indwelling nephrostomy tubes for >2 days. Significant pyuria (104/ml urine) and significant bacteriuria (103/ml of catheterised urine sample/percutaneous nephrostomy) was observed in all the patients. Symptoms of urinary tract infections (UTI) were not present in five patients (31%) which may represent colonisation (Patients 2, 7, 8, 9, 12). The mean duration of catheterisation after which pathogens were isolated was 9.14 ± 8.95 days. Blood cultures in all patients were sterile. Symptoms of all the patients improved after appropriate antimicrobial therapy according to their susceptibility pattern. The patients were numbered according to the chronological order of isolation of the pathogen from them.
Nineteen isolates of Chryseobacterium species were obtained from urine samples of 16 patients on CLED medium after 18 h of incubation at 37°C. The colonies on the CLED medium were 1–2 mm in diameter, smooth, circular, glistening, moist and yellow pigmented. Four isolates obtained from 3 patients were identified as C. gleum, whereas rest 15 were identified as C. indologenes by MALDI Biotyper 3.1 mass spectrometer (Bruker) with scores ranging from 2.352 to 2.457 suggesting highly probable species identification. All isolates were oxidase and catalase positive, glucose non-fermenting Gram-negative rods. They were subcultured on 5% sheep blood agar and incubated for three days at 37°C and 42°C. The isolates identified as C. indologenes showed β haemolysis at 37°C, whereas no growth was obtained at 42°C, whereas the isolates identified as C. gleum showed α haemolysis and were able to grow at 42°C. Antimicrobial susceptibility patterns of the isolates are shown in [Figure 1]. It was observed that 100% isolates were sensitive to minocycline and linezolid, 73.6% strains were sensitive to cotrimoxazole, 63.2% were sensitive to vancomycin and 52.6% were sensitive to nitrofurantoin. All the strains (100%) were resistant to ceftazidime, cefepime, levofloxacin, ciprofloxacin and imipenem. While 94.7% were resistant to meropenem and piperacillin and tazobactam. Of the 19 isolates, 14 showed the presence of carbapenemases by MHT; although, all were resistant to imipenem and 18 were resistant to meropenem.
|Figure 1: Antimicrobial susceptibility pattern of Chryseobacterium isolates|
Click here to view
The MSP dendrogram clearly delineated C. gleum and C. indologenes isolates (distance >600) [Figure 2]a. The dendrogram showed 3 clusters of closely related strains. Cluster 1 had C. indologenes strains C3a, C6, C12, C13, C14 and C15 and cluster 2 had C. indologenes C2, C3, C4, C5, C8, C9, C11, C15a and C16. While cluster 3 had C. gleum strains C7, C7a, C10 and C1. A cluster of closely related strains was defined as strains having >90% similarity in REP-PCR. One isolate of C. gleum (C1) could not be typed using REP-PCR as it showed <7 bands (between 100 and 1500 bp). The dendrogram following REP-PCR also showed three clusters of closely related strains [Figure 2]b. Cluster 1 and 2 had C. indologenes strains C2, C3, C4, C5, C8, C9, C11, C15a and C16 and C3a, C6, C12, C13, C14 and C15. Cluster 3 had C. gleum strains C7, C7a and C10. Both the typing methods showed 100% concordance in classifying the isolates in three clusters (Kappa 1.000).
|Figure 2: (a and b) Main spectra dendrogram and repetitive sequence-based polymerase chain reaction based dendrogram showing three clusters of Chryseobacterium species|
Click here to view
| ~ Discussion|| |
Among the 21 species belonging to the genus Chryseobacterium, C. indologenes and C. gleum are most commonly isolated species from human infections. These bacteria belong to family Flavobacteriaceae. Previously considered to be of low pathogenic potential, these bacteria are gaining importance due to their ability to survive chlorination, produce protease, resistance to multiple antibiotics and to colonise inanimate objects such as sinks, indwelling catheters, nephrostomy drains as well as the patient. In the past, these bacteria were mainly isolated from patients with polymicrobial infections which made it difficult to determine their significance., However, in the past two decades, they have been isolated in patients of meningitis, bacteraemia, pneumonia, endocarditis, infections of the skin and soft tissue, ocular infections and other infections in patients with or without any predisposing factors such as indwelling catheters, immunocompromised state.,,,, Earlier studies of UTI due to members of Chryseobacterium are scanty and limited to case reports including 61-year-old male with cerebrovascular accident (1996), 19-year-old girl with RSD (2012), 86-year-old female with DM (2013) who presented with heart and renal failure and 42-year-old female with acute leukaemia (2014) [Table 2].,,,,C. gleum is reported as a cause of pyonephrosis from our centre recently in a patient with RSD. However, we did not include that case in the present series. The newer and rapid identification method, MALDI-TOF has led to increased recognition of non-fermenters as emerging cause of many nosocomial infections. Chryseobacterium species has been identified efficiently by this method in sputum samples of cystic fibrosis patients.
|Table 2: List of earlier reports of urinary tract infection caused by Chryseobacterium species|
Click here to view
The infections due to Chryseobacterium species have been observed usually in extremes of age. However, the patients in our study had a mean age of 47.06 years. It is noteworthy that all the patients were hospitalised on presentation and were catheterised or had a nephrostomy tube in situ for an average of 9 days and 94.1% (n = 16) of had an abnormality of the urinary tract. The finding that all patients were hospitalised and were subsequently catheterised or had a nephrostomy drain in situ is in agreement older reports of nosocomial infection and colonisation of indwelling devices. The indwelling urinary catheter may act as a predisposing factor for colonisation of these organisms by biofilm formation.,C. gleum isolated from patient 1 showed in vivo response to piperacillin tazobactam despite its in vitro resistance to the drug. The patients in the present study were mainly having two underlying diseases, i.e., RSD with or without ureteric calculi and carcinoma urinary bladder or ureter. This may highlight some kind of association between RSD or malignancy and isolation of chryseobacteria which have the ability to survive in such environment and are resistant to many antibiotics. The patients with predisposing factors like RSD or carcinoma of the urinary tract and history of catheterisation for >2 days, fever, suprapubic tenderness/costovertebral pain or tenderness and positive culture of ≥105 cfu/ml of C. indologenes or C. gleum fulfilled the CDC criteria 1a for diagnosis of catheter-associated UTI. Five patients did not have any complaints of UTI and were, therefore, cases of asymptomatic bacteriuria due to Chryseobacterium species. Only six of our patients were immunocompromised, in contrast to previous reports where a vast majority of the patients were immunocompromised. The present study had three cases where repeat isolation occurred, two of which had recurrent episodes with the same organism 2 and 9 days later, respectively. Among the repeat isolates, 7 and 7a were identical thereby showing its persistence in the urinary tract as a colonizer as the patient did not show any symptoms of UTI. However, 3, 3a and 15, 15a showed a certain variation which placed them apart, thereby showing that these isolates attained some difference in the spectra which may be due to exposure to antibiotics. Therefore, hospitalisation, catheterisation or presence of nephrostomy tube or an abnormality of the urinary tract and exposure to multiple antibiotics are considered to be a risk factor for colonisation and subsequent development of UTI due to Chryseobacterium species.
The observation that clinical strains of Chryseobacterium are resistant to multiple antibiotics was confirmed in the present study. It was found that all the strains in this study were resistant to ceftazidime, cefepime, levofloxacin, ciprofloxacin and imipenem and a majority (94.7%) of them were resistant to piperacillin-tazobactam using disk diffusion method. Earlier reports have shown ciprofloxacin resistance in 85% of C. indologenes isolates and ineffectiveness of piperacillin-tazobactam. These findings are in contrast to the SENTRY study in 2004 where >85% of the strains were susceptible to piperacillin-tazobactam, cefepime and ceftazidime and similar to findings of the study by Chen et al. who found that only 7.7% strains were sensitive ceftazidime, cefepime, imipenem and meropenem, both of which used the MIC testing for determining the susceptibility., However, the high resistance to fluoroquinolones found in the present study is alarming preventing the use of these drugs in our scenario. We found that 100% strains were susceptible to minocycline and linezolid, 73.7% were sensitive to cotrimoxazole, and 63.2% were sensitive to nitrofurantoin and vancomycin by using disk diffusion method. These drugs may be considered as an alternative for management of UTI by Chryseobacterium species. Some of the isolates showed in vivo response to the antibiotics to which they were resistant in vitro. However, further studies are required to validate the results of disk diffusion method.
Phenotypic screening of carbapenemases by MHT has shown good results in many non-fermenters including Pseudomonas and Acinetobacter species.C. indologenes is known for its intrinsic resistance to carbapenems and cephalosporins due to the presence of class A and B β-lactamases. Bellais et al. showed heterogeneity in metallo β-lactamases in Chryseobacterium species. We found all except five isolates showing the presence of carbapenemases although in vitro resistance was shown to carbapenems by them which may show other mechanisms such as increased efflux pump expression, decreased porin expression and increased chromosomal cephalosporinases may play a role in carbapenem resistance; although, we did not perform the genotypic screening.
The findings of phylogenetic relatedness of MALDI-TOF were confirmed by REP-PCR. Both the methods satisfactorily differentiated between the two species. Further, the clustering pattern in both the methods was similar (Kappa 1.000). Infections due to Chryseobacterium species have been reported from hospital settings in the form of sporadic cases or outbreaks. It was interesting to note that all the strains in the present study were isolated during a span of 4 months from patients admitted in the same ward. We tried to trace the possible environmental source of these pathogens by performing surveillance cultures from the ward including trolleys, refrigerator handles, bed railings, operation theatre tables, disinfectants, taps and washbasins but no culture yielded positive results. We postulate that the sudden recognition of these isolates should have been due to the newly introduced MALDI-TOF for identification in routine diagnostics. We then looked vigilantly for the endemicity of this MDR pathogen in our hospital. The routine identification of significant urine isolates by MALDI-TOF revealed no isolation of Chryseobacterium species in the next 2 months, i.e., December 2013 and January 2014. Interestingly, the isolates started to appear regularly thereafter reaching a count of 66 (excluding 19 of first recognition) Chryseobacterium species till April, 2015 with maximum isolation in months of July, 2014 (n = 9), August, 2014 (n = 6), September, 2014 (n = 10) and March, 2015 (n = 10). Although the seasonal variation of these multidrug-resistant pathogens is yet not known, it appears from our observation that the increased temperature during July, August and September at our place may allow the survival of these organisms in the environment as they are known to thrive at higher temperatures. The isolates of this genus seem to have been missed earlier due to the limitations of the conventional methods of identification which may have misidentified them.
Multiple strains of Chryseobacterium species circulating in the hospital could cause urinary tract infection or colonisation in hospitalised individuals with abnormalities in the urinary tract or indwelling devices. These organisms are well-known for their multidrug resistance; therefore, early and accurate identification by MALDI-TOF plays an important role in guiding appropriate antimicrobial therapy.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
| ~ References|| |
Bhuyar G, Jain S, Shah H, Mehta VK. Urinary tract infection by Chryseobacterium indologenes
. Indian J Med Microbiol 2012;30:370-2. [Full text]
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.
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.
Chang YC, Lo HH, Hsieh HY, Chang SM. Identification, epidemiological relatedness, and biofilm formation of clinical Chryseobacterium indologenes
isolates from central Taiwan. J Microbiol Immunol Infect 2015;48:559-64.
Lo HH, Chang SM. Identification, characterization, and biofilm formation of clinical Chryseobacterium gleum
isolates. Diagn Microbiol Infect Dis 2014;79:298-302.
Acosta-Ochoa MI, Rodrigo-Parra A, Rodríguez-Martín F, Molina-Miguel A. Urinary infection due to Chryseobacterium indologenes
. Nefrologia 2013;33:620.
Omar A, Camara M, Fall S, Ngom-Cisse S, Fall B, Ba-Diallo A, et al.
Chryseobacterium indologenes in a woman with acute leukemia in Senegal: A case report. J Med Case Rep 2014;8:138.
Urinary Tract Infection (Catheter-Associated Urinary Tract Infection [CAUTI] and Non-Catheter-Associated Urinary Tract Infection [UTI]) and Other Urinary System Infection [USI]) Events. Device associated module CAUTI. CDC; 2017. Available from: http://www.cdc.gov/nhsn/pdfs/pscManual/7pscCAUTIcurrent.pdf
. [Last accessed on 2017 Feb 8].
Clinical and Laboratory Standards Institute. Performance Standards for Antimicrobial Susceptibility Testing: Twenty Second Informational Supplement M100-S22. Wayne, Pa, USA: Clinical and Laboratory Standards Institute; 2012.
Chang HL, Tang CH, Hsu YM, Wan L, Chang YF, Lin CT, et al.
Nosocomial outbreak of infection with multidrug-resistant Acinetobacter baumannii
in a medical center in Taiwan. Infect Control Hosp Epidemiol 2009;30:34-8.
Snelling AM, Gerner-Smidt P, Hawkey PM, Heritage J, Parnell P, Porter C, et al.
Validation of use of whole-cell repetitive extragenic palindromic sequence-based PCR (REP-PCR) for typing strains belonging to the Acinetobacter calcoaceticus
complex and application of the method to the investigation of a hospital outbreak. J Clin Microbiol 1996;34:1193-202.
Hooton TM, Bradley SF, Cardenas DD, Colgan R, Geerlings SE, Rice JC, et al.
Diagnosis, prevention, and treatment of catheter-associated urinary tract infection in adults: 2009 International Clinical Practice Guidelines from the Infectious Diseases Society of America. Clin Infect Dis 2010;50:625-63.
Ludwig W, Euzeby J, Whitman WB. Road map of the phyla Bacteroidetes, Spirochaetes, Tenericutes (Mollicutes), Acidobacteria, Fibrobacteres, Fusobacteria, Dictyoglomi, Gemmatimonadetes, Lentisphaerae, Verrucomicrobia, Chlamydiae, and Planctomycetes. In: Krieg N, Parte A, Ludwig W, Whitman W, Hedlund B, Paster B, et al
., editors. Bergey's Manual of Systematic Bacteriology. Vol. 4. New York: Springer Science & Business Media; 2011. p. 1-19.
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;16:568-74.
Kirby JT, Sader HS, Walsh TR, Jones RN. Antimicrobial susceptibility and epidemiology of a worldwide collection of Chryseobacterium spp: Report from the SENTRY antimicrobial surveillance program (1997-2001). J Clin Microbiol 2004;42:445-8.
Lin JT, Wang WS, Yen CC, Liu JH, Chiou TJ, Yang MH, et al.
Chryseobacterium indologenes bacteremia in a bone marrow transplant recipient with chronic graft-versus-host disease. Scand J Infect Dis 2003;35:882-3.
Douvoyiannis M, Kalyoussef S, Philip G, Mayers MM. Chryseobacterium indologenes
bacteremia in an infant. Int J Infect Dis 2010;14:e531-2.
Calderón G, García E, Rojas P, García E, Rosso M, Losada A.Chryseobacterium indologenes
infection in a newborn: A case report. J Med Case Rep 2011;5:10.
Cascio A, Stassi G, Costa GB, Crisafulli G, Rulli I, Ruggeri C, et al. Chryseobacterium indologenes
bacteraemia in a diabetic child. J Med Microbiol 2005;54:677-80.
Sudharani V, Asiya, Saxena NK. Chryseobacterium indologenes
bacteraemia in a preterm baby. Indian J Med Microbiol 2011;29:196-8.
] [Full text]
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;34:1908-13.
Zeba B, De Luca F, Dubus A, Delmarcelle M, Simporé J, Nacoulma OG, et al.
IND-6, a highly divergent IND-type metallo-beta-lactamase from Chryseobacterium indologene
s strain 597 isolated in Burkina Faso. Antimicrob Agents Chemother 2009;53:4320-6.
Garg S, Appannanavar SB, Mohan B, Taneja N. Pyonephrosis due to Chryseobacterium gleum
: A first case report. Indian J Med Microbiol 2015;33:311-3.
] [Full text]
Fernández-Olmos A, García-Castillo M, Morosini MI, Lamas A, Máiz L, Cantón R. MALDI-TOF MS improves routine identification of non-fermenting gram negative isolates from cystic fibrosis patients. J Cyst Fibros 2012;11:59-62.
Nemli SA, Demirdal T, Ural S. A case of healthcare associated pneumonia caused by Chryseobacterium indologenes
in an immunocompetent patient. Case Rep Infect Dis 2015;2015:483923.
Cunha V, Ferreira M, Fonseca AG, Diogo J. Community-acquired Chryseobacterium indologenes
in an immunocompetent patient. JMM Case Rep 2014;2014:1. [doi: 10.1099/jmmcr.0.000588].
Noyal MJ, Menezes GA, Harish BN, Sujatha S, Parija SC. Simple screening tests for detection of carbapenemases in clinical isolates of nonfermentative Gram-negative bacteria. Indian J Med Res 2009;129:707-12.
] [Full text]
Bellais S, Léotard S, Poirel L, Naas T, Nordmann P. Molecular characterization of a carbapenem-hydrolyzing beta-lactamase from Chryseobacterium (Flavobacterium) indologenes
. FEMS Microbiol Lett 1999;171:127-32.
Meletis G, Exindari M, Vavatsi N, Sofianou D, Diza E. Mechanisms responsible for the emergence of carbapenem resistance in Pseudomonas aeruginosa
. Hippokratia 2012;16:303-7.
Alfouzan W, Dhar R, Al-Hashemi H, Al-Sweih N, Albert MJ. Clinical and microbiological characteristics of Chryseobacterium spp. Isolated from neonates in Kuwait. JMM Case Rep 2014;2014:1. [doi: 10.1099/jmmcr.0.001008].
[Figure 1], [Figure 2]
[Table 1], [Table 2]