Infection by multidrug-resistant Chryseobacterium indologenes in cases of obstructive uropathy: Case series with short review
Correspondence Address: Source of Support: None, Conflict of Interest: None DOI: 10.4103/MJDRDYPU.MJDRDYPU_201_16
Chryseobacterium spp. are Gram-negative, aerobic, nonfermentative, oxidase-positive and catalase-positive nonmotile bacilli that produce yellow to orange pigment. We report three cases of complicated urinary tract infections (UTIs) caused by Chryseobacterium indologenes in patients with obstructive uropathy. The first case was a known case of diabetes mellitus with right emphysematous pyelonephritis and obstructive uropathy due to prostate enlargement. The patient underwent dialysis for renal failure and subsequently developed UTI by multidrug-resistant C. indologenes. The second case was 72 years old known case of ischemic heart disease. He had acute retention of urine that was relieved after catheterization. He had obstructive uropathy due to transitional cell carcinoma of the bladder and had developed UTI due to C. indologenes. The third case was 38-year-old unmarried female admitted for difficulty in micturition and was catheterized for the same. Obstructive uropathy was due to two fibroids, first fibroid was 9.2 cm × 9.2 cm sized subserosal in the lower segment of the uterus on posterior wall (posterior cervical fibroid) and second fibroid was approximately 1.5 cm × 2.1 cm fundal fibroid; however, the patient developed UTI on the 7th day of catheterization due to C. indologenes. These cases were treated by relieving urinary obstruction and appropriate antibiotic treatment as per antibiotic susceptibility test results. Keywords: Chryseobacterium indologenes, nonfermenter, obstructive uropathy
Chryseobacterium indologenes is a nonfermentative Gram-negative bacillus that although widely distributed in nature is a rare pathogen in humans. In hospital environment, they have been recovered from water systems and humid surfaces. Most infections have been detected in hospitalized patients with severe underlying diseases having indwelling devices and implants. Formerly known as Flavobacterium indologenes, this species was once classified as a type strain of Flavobacterium species centers for disease control Group IIb. In the last decade, it has been phenotypically and genotypically differentiated from other members of this group.[1],[2] There is scarcity of data in the Indian literature regarding infections by Chryseobacterium species. We report three cases of complicated urinary tract infections (UTIs) caused by C. indologenes in patients with obstructive uropathy.
Case 1 A 52-year-old male, known case of diabetes mellitus, with right emphysematous pyelonephritis and chronic kidney disease was admitted to the hospital with urinary complaints and abdominal pain for 3 months. Abdominal examination was not significant. Laboratory investigations revealed hemoglobin as 8 g%, total differential count was 10,000/mm 3, polymorphs 78%, lymphocytes 20%, eosinophils 1%, monocytes 1%, blood urea 150 mg/dL, serum creatinine 10.8 mg/dL, serum potassium 4.9 mEq/L, and serum sodium as 138 mEq/L. Urine protein as 72 mg/L of urine. Urine microscopy showed no pus cells, no organisms, and culture was negative. The patient was put on dialysis for renal failure immediately after investigations on the day of admission and thereafter consecutively on 2nd, 3rd, and 5th day after admission. The patient was given intravenous ceftriaxone for 5 days. Ultrasonography of abdomen showed renal parenchymal disease with mild hydronephrosis on the left side along with calyceal wall thickening and irregular bladder wall. Retrograde urethrogram and micturating cystogram revealed long segmental smooth narrowing of prostate and bulbar urethra. Thus, final diagnosis of right emphysematous pyelonephritis with obstructive uropathy (due to prostate enlargement) was made. After dialysis, his blood urea reduced to 68 mg/dL and serum creatinine to 2.2 mg/dL. However, on day 10th of admission, the patient developed fever with chills and abdominal pain. The patient was empirically started on antibiotics amikacin and piperacillin-tazobactam. Urine collected from catheter was received for microscopy and culture to microbiology laboratory. Urine microscopy revealed 50–60 pus cells/HPF with abundant bacilli. On aerobic conventional urine culture by semiquantitative method, C. indologenes was isolated and identified both by conventional and automated identification system. As this isolate was multidrug resistant and sensitive to only trimethoprim-sulfamethoxazole, the patient was given trimethoprim-sulfamethoxazole for 10 days. The patient underwent double J DJ stenting on the left side to relieve urinary obstruction and recovered. Repeat urine microscopy revealed 1–2 pus cells/HPF and no growth in urine culture. Case 2 A 72-year-male patient, a known case of ischemic heart disease, was admitted to surgery ward with complaints of facial puffiness, pedal edema, acute retention of urine, abdominal distension, and hematuria. On examination, he was afebrile with pulse rate 100/min and blood pressure 180/90 mmHg. His abdominal examination did not reveal any significant finding. Laboratory investigations revealed hemoglobin as 8.9 g%, total lymphocyte count 10,500/mm 3, blood urea 45 mg/dL, and serum creatinine marginally elevated as 1.7 mg/dL. The patient had acute retention of urine that was relieved after catheterization. Urine microscopy revealed abundant pus cells and red blood cells. On ultrasonography, abdomen revealed mild hydronephrosis with hydroureter on the right side and 3.1 cm × 4.1 cm heterogeneous predominantly hyperechoic wall-based lesion in urinary bladder suggestive of neoplastic etiology. Urine cytology showed round to oval degenerated cells in clusters and sheets with mild anisocytosis suggestive of neoplastic etiology. Thus, provisional diagnosis of transitional cell carcinoma of the urinary bladder was made. Urine was sent for culture and sensitivity. On aerobic conventional urine culture by semiquantitative method, C. indologenes was isolated. However, follow-up of the patient was not possible as he took discharge against medical advice. Case 3 A 38-year-old unmarried female was admitted to surgical ward for difficulty in micturition since last 15 days and was catheterized for the same 10 days back before admission. On examination, all vitals were normal. On per abdomen examination, firm to hard mass approximately 6 cm × 6 cm, smooth edged, mobile, nontender was found. The patient was catheterized again on the day of admission (day 1) and investigated. On ultrasonography, two fibroids were seen, first fibroid was 9.2 cm × 9.2 cm sized subserosal in the lower segment of the uterus on posterior wall (posterior cervical fibroid) and second fibroid was approximately 1.5 cm × 2.1 cm fundal fibroid. The patient was transferred to gynecology department and continued to be on catheter for 7 days. However, the patient complained of burning micturition and pain in lower abdomen on the 6th day of catheterization and urine was sent for culture and sensitivity. Urine microscopy revealed abundant pus cells and bacilli on microscopy. Culture grew C. indologenes. Automated antimicrobial susceptibility testing by Phoenix (BD Diagnostics) determined minimal inhibitory concentrations (MICs). The patient underwent myomectomy on the 8th day of admission to relieve obstruction before treating UTIs. Posterior cervical fibroid of size 10 cm × 10 cm and another fundal fibroid of 2 cm × 2 cm were removed. The patient was put on ciprofloxacin as per antibiotic sensitivity testing results of C. indologenes for the next 8 days. Repeat urine culture and sensitivity sample at postoperative day 5 and after 5 days of antibiotics showed no growth. Thus, infection by C. indologenes was cleared after urinary obstruction (uterine fibroids) was removed and after appropriate antibiotic treatment. Identification and antimicrobial susceptibility testing Colonies of C. indologenes that grew on nutrient agar were dark yellow colored, 1–2 mm, low convex, circular with regular margins [Figure 1] showing colonies on nutrient agar]. No growth was observed on MacConkey agar. The organisms grown were nonmotile Gram-negative bacilli that were catalase and oxidase positive. The oxidative-fermentative (glucose) test of Hugh and Leifson yielded oxidative reaction. Indole was produced in tryptophan broth, methyl red, urease production and citrate utilization were negative. Yellow-pigmented colonies were better observed on nutrient agar. The flexirubin type of pigment was confirmed by adding 1 drop of 10% KOH solution to a bit of cell paste. The color of the colonies changed from yellow to red [Figure 2]. The organism was identified as C. indologenes by both conventional biochemical reactions and automated Phoenix identification system.[2] In our study, automated antimicrobial susceptibility testing by Phoenix (BD Diagnostics) determined MICs and results were interpreted. The above mentioned C. indologenes isolates from all the three cases were multidrug resistant. They all showed resistance to second and third generation cephalosporins (cefoxitin, ceftazidime, cefotaxime), carbapenems (imipenem and meropenem), β-lactam + β-lactam inhibitor combinations (piperacillin-tazobactam, amoxicillin-clavulanate, ticarcillin-clavulanate) and colistin. C. indologenes isolates from Case no. 1 and 2 showed additional resistance to fluoroquinolones (levofloxacin, ciprofloxacin) and were intermittently sensitive to tetracycline. C. indologenes isolated from Case no. 3 was sensitive to ciprofloxacin, levofloxacin but resistant to tetracycline. All three isolates were sensitive to trimethoprim-sulfamethoxazole (cotrimoxazole) and were resistant to colistin. MICs for colistin was >256 mcg/ml by E-test in all the three isolates. Minimum inhibitory concentrations of Chryseobacterium indologenes isolated from above three cases by Phoenix automated susceptibility testing illustrated in [Table 1].
The genus Chryseobacterium belongs to the family Flavobacteriaceae, six species of Chryseobacterium are more commonly isolated from clinical species: Chryseobacterium meningosepticum, Chryseobacterium odoratum, Chryseobacterium multivorum, Chryseobacterium breve, and Group IIb Chryseobacterium spp., which includes C. indologenes and C. gleum.[1] C. indologenes is found naturally in soil, water, plants, and foodstuffs. In the hospital environment, they exist in water systems and on wet surfaces which serve as potential reservoirs of infection. Chryseobacterium spp. are Gram-negative, aerobic, nonfermentative, oxidase-positive and catalase-positive nonmotile bacilli that produce yellow to orange pigment. They are readily distinguished from other nonfermenters by their ability to produce indole in tryptophan broth. Nosocomial infections due to C. indologenes have been linked to the use of indwelling devices during hospital stay.[2] Colonization of patients through contaminated medical devices, involving fluids such as respirators, intubation tubes, mist tents, humidifiers, incubators for newborns, ice chests, and syringes, has been documented.[3] The clinical significance of C. indologenes has not been fully established yet because this bacterium has not been frequently recovered from clinical specimens. In 1993, Bonten et al. first isolated a strain of C. indologenes from a tracheal aspirate in a patient with ventilator-associated pneumonia.[4] In 1996, Hsueh et al. found increasing incidence of healthcare-associated infection due to Chryseobacterium species other than C. meningosepticum (Elizabethkingia meningoseptica).[5] Reported infections include bacteremia, pneumonia, meningitis, pyomyositis, keratitis, also indwelling device-associated infection such as UTI, surgical and burn wound infections.[2],[4],[5],[6],[7],[8],[9] Chryseobacteria represent only 0.27% of the processed nonfermentative Gram-negative bacilli and 0.03% of all bacterial isolates collected by the SENTRY Program during the 5 year period 1997–2001.[10] With increasing clinical usage of colistin and tigecycline against emerging carbapenem-resistant pathogens, such as Acinetobacter baumannii, extended-spectrum β-lactamases-producing Escherichia coli and Klebsiella pneumoniae, Chryseobacterium species have caused significant problems in critical healthcare setting.[11] Appropriate choice of effective antimicrobial agents for the treatment of infections by C. indologenes is difficult because of the unpredictability and breadth of antimicrobial resistance of this organism, which often involves resistance to many of the antibiotics chosen empirically for serious Gram-negative infections. C. indologenes has intrinsic resistance to aminoglycosides, first generation cephalosporins, aminopenicillins, and aztreonam. C. indologenes is intrinsically resistant to carbapenems and cephalosporins due to its production of molecular Class A β-lactamase and Class B carbapenem-hydrolyzing β-lactamase (IND1-IND7).[11] Results for nitrofurantoin and amoxicillin-clavulanate are always reported as resistant because they are not indicated for or are not clinically effective for treatment of glucose-nonfermenting Gram-negative rods. According to the results of the SENTRY antimicrobial surveillance program, the most active agents against C. indologenes are the quinolones (gatifloxacin and levofloxacin) and trimethoprim-sulfamethoxazole (>95% susceptibility). Ciprofloxacin, cefepime, ceftazidime, piperacillin, and rifampin showed reasonable activity (85% susceptibility). Furthermore, as per report from the SENTRY antimicrobial surveillance program (1997–2001), vancomycin, chloramphenicol, linezolid, and glycopeptides are not appropriate for treating infections due to this organism.[10] Clinical microbiologists have additional problems to resolve: (1) results of susceptibility testing for Chryseobacterium vary when different methods are used and (2) results from disk diffusion methods are not reliable, so broth reference quality microdilution tests should be performed when possible.[10]
C. indologenes, although uncommon, is an important pathogen causing UTI especially in obstructive uropathy cases with indwelling catheters or instrumentation in hospitalized patients. Furthermore, identification of C. indologenes is easy and simple even by conventional methods such as its ability to produce deep yellow-colored colonies on blood agar, failure to grow on MacConkey, being oxidase positive, nonmotile, and being a nonfermenter. Proper management by relieving urinary obstruction and appropriate antibiotic treatment of infection for this relatively resistant organism warrants correct identification and antimicrobial susceptibility testing. Financial support and sponsorship Nil. Conflicts of interest There are no conflicts of interest.
[Figure 1], [Figure 2]
[Table 1]
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