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  Table of Contents  
Year : 2017  |  Volume : 35  |  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

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 Publication1-Feb-2018

Correspondence Address:
Dr. Neelam Taneja
Department of Medical Microbiology, Postgraduate Institute of Medical Education and Research, Chandigarh
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/ijmm.IJMM_15_413

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 ~ Abstract 

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:

 ~ Introduction Top

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.[1] However, they do not form a part of human microbiota. The genus Chryseobacterium was previously called as Flavobacterium.[2]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.[3] They have been isolated from patients with bacteraemia, meningitis, pneumonia, peritonitis, ocular infections and long-term indwelling devices.[3],[4] The frequent administration of carbapenems may help in selecting out this group, especially in health-care settings.[3] The members of Chryseobacterium genus are known for their multidrug resistance.[4] Hence, it is important to identify these organisms considering high mortality caused by these pathogens, especially in patients of bacteraemia and pneumonia.[4] 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).[4],[5] 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.[1],[6],[7] 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 Top

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).[8]

Bacterial isolates

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).[9] For interpretation, we referred to the zone diameters for Pseudomonas aeruginosa, Enterococcus (Vancomycin), and Staphylococcus (Linezolid).[9]

Modified Hodge test

Carbapenemase production by the isolates was detected by modified Hodge test (MHT) according to CLSI.[9] 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.[10] 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.[11] 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.

Statistical analysis

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 Top

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.[12] 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.
Table 1: Clinical characteristics of patients and their isolates

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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

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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

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 ~ Discussion Top

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.[13] 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.[14] In the past, these bacteria were mainly isolated from patients with polymicrobial infections which made it difficult to determine their significance.[13],[15] 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.[16],[17],[18],[19],[20] 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].[1],[6],[7],[21],[22]C. gleum is reported as a cause of pyonephrosis from our centre recently in a patient with RSD.[23] 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.[24]
Table 2: List of earlier reports of urinary tract infection caused by Chryseobacterium species

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The infections due to Chryseobacterium species have been observed usually in extremes of age.[25] 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.[1],[25]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.[8] 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.[26] 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.[26] 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.[3],[15] 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.[27]C. indologenes is known for its intrinsic resistance to carbapenems and cephalosporins due to the presence of class A and B β-lactamases.[26] Bellais et al. showed heterogeneity in metallo β-lactamases in Chryseobacterium species.[28] 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.[29]

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.[30] 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.[30] 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.

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