Abstract
Background
Chryseobacterium indologenes is ubiquitous in nature and rarely causes infections. However, the clinical impact of C. indologenes has increased in recent years, especially in immunocompromised patients, and has resulted in high mortality rates. We aimed to investigate the clinical and microbiological characteristics of C. indologenes bacteremia.
Materials and Methods
We retrospectively reviewed medical records of a 642-bed university-affiliated hospital in Korea, dating from January 2001 to December 2020, to investigate C. indologenes bacteremia.
Results
A total of 22 C. indologenes isolates were identified from blood culture records. All patients were hospitalized at the time of bacteremia, and the most common manifestation was primary bacteremia. A sizable majority of the patients (83.3%) had underlying diseases, and all patients received intensive care unit care during their admission. The 14-day and 28-day mortality rates were 8.3% and 16.7%, respectively. Importantly, all C. indologenes isolates were 100% susceptible to trimethoprim-sulfamethoxazole.
Conclusion
In our study, most of the infections were hospital-acquired, and the susceptibility pattern of the C. indologenes isolates showed multidrug resistance. However, trimethoprim-sulfamethoxazole is a potentially useful antibiotic for C. indologenes bacteremia treatment. More attention is required to identify C. indologenes as one of the most important nosocomial bacteria with detrimental effects in immunocompromised patients.
Keywords: Chryseobacterium indologenes, Bacteremia, Nosocomial infections, Antimicrobial resistance, Immunocompromised patients
Graphical Abstract
Introduction
Chryseobacterium indologenes, formerly known as Flavobacterium indologenes is a non-motile, catalase-positive, oxidase-positive, non-glucose-fermenting Gram-negative bacillus [1]. C. indologenes is ubiquitous in nature and is frequently isolated from wet surfaces and water sources in hospital environments. C. indologenes was first isolated in 1993 from a tracheal aspirate in a patient with ventilator-associated pneumonia [2,3]. Although it rarely causes infections, manifestations such as bacteremia, pneumonia, intra-abdominal infection, skin and soft tissue infection, urinary tract infection, meningitis, keratitis, and catheter-related infections have been reported [4,5,6,7,8,9,10,11,12,13,14,15,16]. It can cause serious disease, especially in immunocompromised and critically ill patients and sometimes associated with prolonged indwelling devices (e.g., catheters) [17]. Chryseobacterium species are known to be resistant to aminoglycosides, tetracyclines, chloramphenicol, erythromycin, clindamycin, and teicoplanin [18].
Herein, we retrospectively investigated the clinical characteristics of C. indologenes bacteremia and the antibiotic susceptibility profile of each isolate from records spanning 20 years from a single university hospital.
Materials and Methods
1. Patient identification, microbiology and definitions
This was a retrospective study of medical records dating from January 2001 to December 2020, conducted in a 642-bed university-affiliated hospital in Korea wherein records of patients infected by C. indologenes were reviewed. Reports of clinical isolates of C. indologenes obtained from blood cultures in all age groups were included. These reports indicated that identification and antimicrobial susceptibility tests were performed using the Vitek 2 automated identification and antimicrobial susceptibility system (bioMérieux, Marcy-L’Etoile, France), using the broth microdilution method and susceptibility criteria as described in the Clinical and Laboratory Standards Institute (CLSI) M100 guidelines [19]. We defined significant bacteremia as having the growth of C. indologenes in one or more blood cultures with clinical signs of systemic inflammatory response syndrome (SIRS). SIRS is defined as involving two or more of the following: temperature >38°C or <36°C, heart rate >90/min, respiratory rate >20/min or PaCO2 <32 mmHg, white blood cell count >12,000/mm3 or <4,000/mm3 or >10% immature bands [20]. Immunocompromised patients were defined as having acquired secondary immunodeficiency as a result of a disease process or its therapy (e.g., human immunodeficiency virus infection, hematopoietic malignancies, radiation therapy, and treatment with immunosuppressive medication). Hospital-acquired infection was defined as bacteremia that occurs ≥48 hours after admission, or bacteremia in which the patient had been hospitalized at any time within the previous month.
Data on patients’ demographic characteristics; clinical variables, including the duration (in days) of hospitalization, age, sex, underlying disease, site of infection, administration of antibiotics, and outcomes; and hospital resources used were collected. Additionally, patients’ comorbidities were quantified using the Charlson Comorbidity Index. The 14-day and 28-day mortality from initial positive blood cultures were measured to evaluate patients’ outcomes.
2. Ethics statement
This study was performed in line with the principles of the Declaration of Helsinki. The study was approved by the Institutional Review Board of Inje University Ilsan Paik Hospital (IRB number: ISPAIK 2022-01-018), and the requirement for written informed consent was waived.
Results
1. Clinical characteristics and treatment outcome
During the 20-year period, a total of 22 C. indologenes isolates from 12 patients were identified from blood cultures. C. indologenes was isolated from multiple cultures incubated on the same day as that of drawing the sample in a patient, and there was no persistent or recurrent bacteremia reported. There was no polymicrobial infection. Seven (58.3%) of 12 patients were male. The mean age of patients was 63.00 ± 17.15 years (range, 18 - 79 years), and ten patients were ≥60 years. All 12 patients were hospitalized at the time of blood sample collection, and received intensive care unit (ICU) care during admission.
The demographics and characteristics of the patients are listed in Table 1. The median Charlson Comorbidity Index score was 5 (interquartile range [IQR]: 3 - 5.25). Underlying diseases were present in 83.3% of patients (10/12), and ten cases of C. indologenes bacteremia were observed in the hospital. There were five cancer patients, three of whom had distant metastasis, and one had lymphoma. All patients had indwelling catheters, including central venous catheters (n = 4), indwelling urinary catheters (n = 8), chemoports (n = 4), and ventilators (n = 6). The most common manifestation was primary bacteremia (75.0%, 9/12); the remaining patients had catheter-associated bacteremia (n = 2) and ventilator-associated pneumonia (n = 2). The 14-day and 28-day mortality rates were 8.3% (1/12) and 16.7% (2/12), respectively.
Table 1. Demographics and clinical characteristics of 12 patients with bacteremia caused by Chryseobacterium indologenes .
| Patient | Year | Age/sex | Charlson comorbidity index | Indwelling catheter | Ventilator care | Clinical syndrome | HOD | Other site of C. indologenes isolation | 14-day mortality | 28-day mortality |
|---|---|---|---|---|---|---|---|---|---|---|
| 1 | 2001 | 70/M | 3 | Chemoport | No | Primary bacteremia | 50 | – | No | No |
| 2 | 2002 | 42/M | 6 | Chemoport | No | Primary bacteremia | 5 | – | Yes | Yes |
| 3 | 2006 | 18/F | 0 | Urinary catheter | No | Primary bacteremia | 20 | – | No | No |
| 4 | 2008 | 76/M | 0 | Urinary catheter | Yes | Primary bacteremia | 7 | – | No | Yes |
| 5 | 2011 | 72/F | 3 | Urinary catheter, CVC | Yes | Primary bacteremia | 5 | – | No | No |
| 6 | 2012 | 79/M | 5 | Urinary catheter, CVC | Yes | Primary bacteremia | 89 | – | No | No |
| 7 | 2013 | 71/F | 8 | Chemoport | No | Primary bacteremia | 1 | – | No | No |
| 8 | 2014 | 60/F | 5 | Urinary catheter, CVC | Yes | Primary bacteremia | 5 | – | No | No |
| 9 | 2016 | 72/F | 6 | Urinary catheter | No | Primary bacteremia | 1 | – | No | No |
| 10 | 2016 | 60/M | 5 | Urinary catheter | Yes | Pneumonia | 8 | sputum | No | No |
| 11 | 2018 | 67/M | 4 | Urinary catheter, CVC | Yes | Catheter-related bacteremia | 267 | PICC tip | No | No |
| 12 | 2020 | 69/M | 3 | Chemoport | No | Catheter-related bacteremia | 3 | chemoport tip | No | No |
M, male; F, female; CVC, central venous catheter; HOD, hospital of day; PICC, peripherally inserted central-line catheter.
2. Antimicrobial susceptibility and appropriateness of antibiotics
The results of antimicrobial susceptibility testing for each patient are presented in Table 2. The antibiotic susceptibility profile of the isolates showed that 100, 67, 63.6, 50, and 41.7% of the isolates were susceptible to trimethoprim-sulfamethoxazole, levofloxacin, ciprofloxacin, cefepime, and piperacillin-tazobactam, respectively.
Table 2. In-vitro susceptibility results of 12 Chryseobacterium indologenes isolates from blood samples.
| Drugs | Patient number (number of bacterial isolations) | |||||||||||
|---|---|---|---|---|---|---|---|---|---|---|---|---|
| # 1 (2) | # 2 (2) | # 3 (2) | # 4 (2) | # 5 (2) | # 6 (1) | # 7 (1) | # 8 (2) | # 9 (1) | # 10 (1) | # 11 (4) | # 12 (2) | |
| Ampicillin | >16 (R) | 16 (I) | >16 (R) | >16 (R) | >16 (R) | >16 (R) | >16 (R) | >16 (R) | >16 (R) | >16 (R) | ||
| Amoxicillin/clavulanate | >16 (R) | >16 (R) | >16 (R) | >16 (R) | >16 (R) | >16 (R) | 4 (S) | >16 (R) | ||||
| Cafazolin | >32 (R) | >32 (R) | >32 (R) | >32 (R) | >32 (R) | >32 (R) | >32 (R) | |||||
| Cefalotin | >32 (R) | >32 (R) | >32 (R) | |||||||||
| Cefotaxime | >32 (R) | 16 (I) | >32 (R) | >32 (R) | >32 (R) | >32 (R) | >32 (R) | >32 (R) | 32 (I) | >32 (R) | >32 (R) | >32 (R) |
| Ceftazidime | >32 (R) | >32 (R) | >32 (R) | >32 (R) | >32 (R) | >32 (R) | ≤1 (S) | 32 (R) | 16 (I) | 4 (S) | ||
| Cefepime | >32 (R) | >32 (R) | >32 (R) | 32 (R) | >32 (R) | 8 (S) | ≤1 (S) | 4 (S) | 4 (S) | ≤1 (S) | ||
| Piperacillin | >64 (R) | >64 (R) | >64 (R) | >64 (R) | 64 (I) | |||||||
| Piperacillin/tazobactam | 8/4 (S) | ≤4/4 (S) | 32/4 (I) | 16/4 (S) | ≥128/4 (R) | ≥128/4 (R) | ≥128/4 (R) | ≥128/4 (R) | ≤4/4 (S) | 64/4 (I) | ≥128/4 (R) | ≥128/4 (R) |
| Aztreonam | >32 (R) | >32 (R) | ||||||||||
| Meropenem | 8 (I) | >8 (R) | >8 (R) | >8 (R) | ||||||||
| Imipenem | >8 (R) | ≤0.5 (S) | >8 (R) | >8 (R) | >8 (R) | >8 (R) | >8 (R) | >8 (R) | ≤0.25 (S) | >8 (R) | >8 (R) | >8 (R) |
| Gentamicin | >8 (R) | >8 (R) | >8 (R) | >8 (R) | >8 (R) | >8 (R) | >8 (R) | 8 (I) | ≤1 (S) | >8 (R) | >8 (R) | >8 (R) |
| Amikacin | >32 (R) | >32 (R) | >32 (R) | >32 (R) | >32 (R) | >32 (R) | >32 (R) | >32 (R) | ≤2 (S) | >32 (R) | >32 (R) | >32 (R) |
| Ciprofloxacin | 1 (S) | 0.5 (S) | 1 (S) | 1 (S) | >2 (R) | 2 (I) | >2 (R) | ≤0.25 (S) | 0.5 (S) | 2 (I) | 0.5 (S) | |
| Levofloxacin | >4 (R) | 1 (S) | 0.5 (S) | |||||||||
| Trimethoprim-sulfamethoxazole | ≤1 (S) | ≤1 (S) | ≤1 (S) | ≤1 (S) | ≤1 (S) | ≤1 (S) | ≤1 (S) | ≤1 (S) | ≤1 (S) | ≤1 (S) | 2 (S) | ≤1 (S) |
| Tigecycline | 1 (S) | >4 (R) | 4 (I) | ≤0.5 (S) | 4 (I) | >4 (R) | >4 (R) | |||||
| Tetracycline | >8 (R) | >8 (R) | ||||||||||
| Colistin | >8 (R) | >8 (R) | ||||||||||
R, resistant; I, intermediate; S, susceptible.
The history of antibiotic use and the appropriateness of antibiotics for each patient are presented in Table 3. Empirical antibiotics are defined as antibiotics used prior to the results of culture studies, and definite antibiotics are defined as those used after the results of culture studies. According to the susceptibility results, the empirical use of antibiotics was appropriate in only one patient (8.3%). After confirming the culture results and adjusting the antibiotics, 41.7% (5/12) of the patients received appropriate antibiotic treatment.
Table 3. History of antibiotics use and appropriateness of empirical and definite antibiotics.
| Patient | Date of specimen | Duration of antibiotics use (days) | Total duration (days)a | Appropriateness of antibiotics | |
|---|---|---|---|---|---|
| Empirical | Definite | ||||
| 1 | 2001-SEP-12 | Ciprofloxacin (8), piperacillin/tazobactam (5), trimethoprim/sulfamethoxazole (4) | 13 | Appropriate | Appropriate |
| 2 | 2002-NOV-24 | Aztreonam (5), teicoplanin (9) | 9 | – | – |
| 3 | 2006-AUG-10 | Aztreonam (7), vancomycin (7), ciprofloxacin (6) | 12 | – | Appropriate |
| 4 | 2008-NOV-13 | Ceftriaxone (7), metronidazole (7), piperacillin/tazobactam (15) | 22 | – | Appropriate |
| 5 | 2011-APR-03 | Ceftriaxone (2), aztreonam (14), metronidazole (14) | 30 | – | – |
| 6 | 2012-MAY-14 | Piperacillin/tazobactam (13), meropenem (10) | 22 | Inappropriate | Inappropriate |
| 7 | 2013-MAR-18 | Ceftriaxone (26) | 26 | Inappropriate | Inappropriate |
| 8 | 2014-AUG-24 | Ceftriaxone (2), piperacillin/tazobactam (7), ciprofloxacin (7), meropenem (7) | 13 | Inappropriate | Inappropriate |
| 9 | 2016-JUN-29 | Ceftriaxone (6), metronidazole (6), piperacillin/tazobactam (12) | 17 | Inappropriate | Appropriate |
| 10 | 2016-JUL-14 | Piperacillin/tazobactam (5), vancomycin (5), metronidazole (5), meropenem (18), teicoplanin (13) | 22 | Inappropriate | Inappropriate |
| 11 | 2019-SEP-18 | Colistimethate sodium (6), piperacillin/tazobactam (6), vancomycin (6), levofloxacin (23) | 29 | Inappropriate | Appropriate |
| 12 | 2020-SEP-30 | Aztreonam (3), cefaclor (7) | 9 | Inappropriate | – |
aTotal duration of antibiotics use excluding duplication.
Discussion
Although it is a rare human pathogen, C. indologenes is known to cause serious infections in immunosuppressed patients from various parts of the globe [21]. In our study, the 14-day and 28-day mortality rates were relatively low (8.3% and 16.7%, respectively). Data on mortality are scarce, but according to one study analyzing C. indologenes bacteremia in 22 patients, the 14-day and 28-day mortalities were 36.4% and 50.0%, respectively [22], which were higher than the rates in our study. In the same study, in-hospital mortality was significantly higher in the bacteremia group (63.6%) than in the pneumonia group (35.2%) (P = 0.015).
Furthermore, in our study, ten cases of C. indologenes bacteremia were acquired in the hospital. In two patients (patients 7 and 9), samples were collected 1 day after admission. However, one patient received chemotherapy for one month and was discharged 10 days before next admission. In a previous report, Lin et al. found that all bacteremia cases were hospital-acquired, and most bacteremia developed at least 10 days after admission [23]. C. indologenes colonization through contaminated medical devices, such as endotracheal tubes, humidifiers, and syringes has been reported [4]. In addition, this bacterium produces a biofilm on indwelling catheters and has protease activity, which mirrors the virulence of invasive infections. In this study, the source of infection was unknown in 75.0% (9/12) of the patients. Similar to our study, the primary site of infection was unknown in 80.0% (8/10) of ICU-acquired C. indologenes bacteremia in a study conducted by Chou et al. [24]. However, in our study, as all patients had indwelling catheters, such as central venous catheters, chemoports or urinary catheters, catheter-related infections may have been underestimated. Considering the high mortality rate associated with bacteremia in patients with indwelling catheters, C. indologenes should be seriously considered as an important nosocomial pathogen.
According to previous studies, C. indologenes isolates showed variable susceptibility to various antibiotics [7,22,23,24,25,26] and resulted in life-threatening infections because of their multidrug resistance [27]. A study by Chang et al. reported high resistance to most drugs examined in C. indologenes isolates obtained between 2007 and 2011. All isolates were completely resistant to gentamicin, amikacin, ceftriaxone, chloramphenicol, colistin, and imipenem [26]. In our study, the isolates only had 100% susceptibility to trimethoprim-sulfamethoxazole; they were also variably susceptible to quinolones (63.6% for levofloxacin and 50.0% for ciprofloxacin). Contrastingly, several studies reported 30.6 - 87.0% susceptibility to trimethoprim-sulfamethoxazole [16,22,25,26,27,28]. Chen et al. showed a trend of increasing prevalence of C. indologenes infection after the introduction of colistin and tigecycline usage [22]. Because of the limited spectrum of antimicrobial susceptibility of C. indologenes, it is difficult to choose appropriated antibiotics [28].
Our study has several limitations. First, there could have been missing data due its retrospective design, and there could have been an error in determining whether there was a true infection or not. Second, it was difficult to establish a definite correlation between antibiotic appropriateness and mortality because most of the patients were using two or more antibiotics and were in a severe condition, and the number of cases was small. Despite these limitations, our study is meaningful in that we analyzed data of C. indologenes bacteremia from records covering 20 years.
In conclusion, this study demonstrated the clinical characteristics and outcomes of patients with C. indologenes bacteremia and antimicrobial susceptibility of each isolate. Most of the C. indologenes bacteremia were hospital-acquired, and the susceptibility pattern showed multidrug resistance. According to the in vitro susceptibility results, trimethoprim-sulfamethoxazole can be a potential antibiotic for C. indologenes infections. As the number of immunocompromised and nosocomial infections is increasing, more attention needs to be paid to C. indologenes as an important nosocomial pathogenic bacterium.
Footnotes
Funding: None.
Conflict of Interest: No conflict of interest.
- Conceptualization: JES, JC.
- Data curation: THU, CRC, SK.
- Formal analysis: JC.
- Investigation: JC, CRC.
- Methodology: JC, JES.
- Supervision: JES.
- Validation: UTH.
- Writing - original draft: JC, JES.
- Writing - review & editing: JC, JES, SK, THU, CRC, YGK.
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