Bacteremia Caused by Pseudomonas Luteola in Pediatric Patients

Jpn. J. Infect. Dis., 68, 50–54, 2015

Original Article Bacteremia Caused by Pseudomonas luteola in Pediatric Patients

Gulsum Iclal Bayhan1*, Saliha Senel2,4, Gonul Tanir1, and Sengul Ozkan3 1Department of Pediatric Infectious Disease, 2Department of Pediatrics, and 3Department of Clinical Microbiology and Infectious Disease, Dr. Sami Ulus Maternity and Children's Health Education and Research Hospital; and 4Department of Pediatrics, Yƒldƒrƒm Beyazit University, Ankara, Turkey

SUMMARY: Pseudomonas luteola has rarely been reported as a human pathogen. The clinical mani- festations of P. luteola bacteremia and its susceptibility to antibiotics have not been characterized. This retrospective study was conducted at a 382-bed tertiary care center in Turkey. During the 9-year study period, 7 patients (5 females and 2 males) were diagnosed with P. luteola bacteremia. Six of these patients had hospital-acquired bacteremia, whereas 1 patient had community-acquired P. luteola infection. All patients had monomicrobial bacteremia. Antimicrobial susceptibility testing revealed that all strains of P. luteola were sensitive to amikacin, gentamicin, trimethoprim-sulfamethoxazole, and meropenem, and that all strains were resistant to piperacillin-tazobactam, aztreonam, and colistin. In conclusion, we believe that P. luteola can cause both community- and hospital-acquired bacteremia. Amikacin, gentamicin, trimethoprim-sulfamethoxazole, and meropenem were effective against P. luteola in the present study.

tion of antibiotic treatment because of clinical deterio- INTRODUCTION ration or antibiogram results, duration of antibiotic Pseudomonas luteola, which is also called Chryseo- treatment, and treatment outcome. monas luteola, is a nonfermenting gram-negative bac- P. luteola bacteremia was diagnosed based on the iso- terium that was previously classified in US Centers for lation of bacterium in 1 peripheral blood cultures. Disease Control and Prevention group Ve-1. P. luteola Bacteremia was considered hospital-acquired if it oc- is rarely reported as human pathogen, and the literature curred 48 h after hospital admission. Community- includes only a few cases of infection by this bacterium acquired infection was defined as bacteremia that oc- (1,2). The present study aimed to determine the clinical curred within the first 48 h after hospital admission characteristics, antibiotic susceptibility, treatment regi- without exposure to a healthcare facility. Bacterial mens, and outcomes in 7 pediatric patients with P. lu- growth was detected in blood cultures using a teola bacteremia. BacT/Alert3D automated system (bioMerieux,Á Marcy l'Etoile, France). The organism with slow growth and the presence of small yellow-orange colonies on eosin MATERIALS AND METHODS methylene blue agar and blood agar after 48 h incuba- This study was conducted at Dr. Sami Ulus Maternity tion were considered in the identification process. It was and Children's Health and Diseases Research and Edu- identified as catalase-positive and oxidase-negative in cation Hospital, a 382-bed tertiary care center in standard biochemical tests. It utilized glucose, man- Ankara, Turkey. The study included patients aged 1 nitol, and maltose oxidatively; hydrolyzed esculin; and month–18 years who developed P. luteola bacteremia reduced nitrates to nitrites. It did not decarboxylate ly- between January 2005 and November 2013. The sine, did not hydrolyze urea, and did not produce in- patients' medical records were reviewed. The following doles. Identification of P. luteola was performed using variables were analyzed patients' age and gender, pri- the Vitek 2 (bioMerieux) automated system. The suscep- mary diagnosis, peripheral blood leukocyte count and tibility of bacterial isolates to antimicrobial agents was serum C-reactive protein (CRP) level at the time blood initially determined via the routine disk diffusion culture was obtained, use of total parenteral nutrition, method, according to the guidelines of the Clinical and central vascular access and mechanical ventilation for Laboratory Standards Institute's guideline for other ＞48 h, duration of hospitalization prior to bacteremia, non-Enterobacteriaceae (3). Bacterial isolates were test- number of positive blood cultures, antimicrobial sus- ed using the following antimicrobials: amikacin; gen- ceptibility profile, empirical antibiotic regimen, altera- tamicin; aztreonam; ceftriaxone; ceftazidime; cefoper- azone-sulbactam; ciprofloxacin; imipenem; piperacil- Received February 3, 2014. Accepted June 16, 2014. lin; piperacillin-tazobactam; and trimethoprim-sul- J-STAGE Advance Publication November 25, 2014. famethoxazole. Statistical analysis was performed using DOI: 10.7883/yoken.JJID.2014.051 SPSS v.15.0 for Windows (SPSS, Inc., Chicago, IL, *Corresponding author: Mailing address: Department of USA). Pediatric Infectious Disease, Dr. Sami Ulus Maternity and Children's Health Education and Research Hospital, RESULTS Babur caddesi, No: 44 (06080), Altindag, Ankara, Turkey. Tel: ＋90 312 305 65 45, Fax: ＋90 312 317 03 53, E-mail: During the 9-year study period, 7 patients (5 females gibayhan＠gmail.com and 2 males) were diagnosed with P. luteola bacteremia.

50 Bacteremia Caused by Pseudomonas luteola

The mean age of the patients was 44 ± 40.8 months pies and alterations to the treatment regimens based on (median: 24 months; range: 11–105 months). All the results of drug susceptibility testing of P. luteola iso- patients were febrile when blood was obtained for cul- lates are presented in Table 2. ture. Two patients had a central vascular catheter at the Recurrent P. luteola bacteremia occurred in 1 patient time of bacteremia, and 1 patient was receiving mechan- (case no. 4). Although this patient was being followed- ical ventilation before P. luteola bacteremia developed. up in the hospital for a diagnosis of Miller-Dieker syn- Three patients (42.8z) had leukocytosis (＞15,000 leu- drome, fever and respiratory distress developed, and kocytes/mL), and 5 patients (71.4z) had an elevated respiratory support with mechanical ventilation was re- CRP level (＞10 mg/dL) at the time of obtain blood cul- quired. His CRP level and leukocyte count were ex- ture. All patients had monomicrobial bacteremia, as tremely elevated, and chest radiography revealed there were no cases of concomitant microorganism in- bilateral infiltration. Colistin was added to the initial fection. The clinical characteristics of 7 patients with P. antibiotic treatment following a diagnosis of nosocomi- luteola bacteremia are shown in Table 1. al pneumonia. P. luteola was cultured in blood that was Six patients had hospital-acquired bacteremia, with a obtained at the beginning of the patient's febrile period. median interval from hospitalization to the develop- After 48 h, P. luteola was again isolated in the second ment of bacteremia of 13 days, whereas 1 patient had blood culture while the patient was receiving colistin community-acquired P. luteola infection; she had pro- treatment. As colistin-resistant P. luteola was identified tein-losing enteropathy and presented with a fever of in both blood cultures, colistin was withdrawn, and the 38.39C, vomiting, and diarrhea. Initial empirical thera- patient was treated with imipenem.

Table 1. Summary of demographic data, comorbidities, clinical characteristics, and length of hospital stay of 7 patients with Pseudomonas luteola bacteremia Age Hospitalization Single/multiple Acquired Clinical positive blood Case (mo)/ Year Primary disease source TPN/CVL/MV situation day on positive Gender culture obtained culture

1 105/F 2011 Miller Fisher syndrome Hospital －/－/－ Bacteremia 13 Single 2 11/F 2011 Congenital hypophospatasia, Hospital / / Bacteremia 126 Single malnutrition －－＋ 3 14/F 2011 Protein-losing enteropathy Community －/－/－ Bacteremia 0 Single 4 72/M 2011 Miller-Dieker syndrome Hospital / / Pneumonia, 49 2 ＋＋－ bacteremia 5 19/F 2010 Infantile spasm Hospital －/－/－ Bacteremia 7 Single 6 29/M 2010 Tetralogy of Fallot Hospital －/＋/－ Bacteremia 10 Single 7 86/F 2007 Meningomyelocele Hospital －/－/－ Bacteremia 24 Single TPN, total parenteral nutrition; CVL, central vascular line; MV, mechanic ventilation.

Table 2. Summary of treatment regimen, treatment duration, and outcome Empirical antibiotic Appropriate/ Antibiotic Treatment Case First-line antibiotic treatment during Inappropriate treatment after Outcome treatment bacteremia therapy culture result duration

1 CTX, CD IMP App IMP 23 Survived 2 CAZ, COLI, LZD IMP App IMP 24 Died 3 CTR, AK IMP App IMP 10 Survived 4 PTZ, VA COLI Inapp IMP 34 Survived 5 CEF MERZ App MERZ 14 Survived 6 AS IMP App IMP 7 Survived 7 VA, AK MERZ App MERZ 21 Discharge

App/Inapp, appropriate/inappropriate; CTRX, ceftriaxone; CD, clindamycin; CAZ, ceftazidime; COLI, colistin; LZD, linezolid; AK, amikacin; PTZ, piperacillin-tazobactam; VA, vancomycin; AS, ampicillin-sulbactam; MERZ, meropenem; IMP, imipenem.

Table 3. Antimicrobial susceptibility of Pseudomonas luteola isolates

Case PI AZT CAZ CTX CP IMP STX AK PTZ GM CPZ COLI 1RRRSSSSSRSRR 2RRRNSSSSRSNN 3NRRNRSSSRSRR 4RRRSSSSSRSNR 5SRRNSSSSRSSR 6NRRSSSSSNSNN 7SNSSSSSSNSNN PI, piperacillin; AZT, aztreonam; SXT, trimethoprim-sulfamethoxazole; CP, ciprofloxacin; GM, gentamicin; CPZ, cephoperazon-sulbactam; N, not performed; R, resistant; S, susceptible.

51 Antimicrobial susceptibility testing illustrated that all oped P. luteola bacteremia on the 126th day of hospi- strains of P. luteola were sensitive to amikacin, gen- talization died. Although this patient was treated with tamicin, trimethoprim-sulfamethoxazole, and meropen- effective antibiotic against to P. luteola and mechanical em and resistant to piperacillin-tazobactam, aztreonam, ventilation, the patient died 24 days after a positive and colistin. In total, 15 and 85z of the isolates were re- blood culture. sistant to ciprofloxacin and ceftazidime, respectively. Antimicrobial susceptibility test results of all 7 identi- DISCUSSION fied strains are presented in Table 3. The duration of antibiotic treatment based on anti- P. luteola is a member of the nonflorescent group of biograms of P. luteola was 19 ± 9.3 days. In all, 6 the family Pseudomonadaceae. It is a catalase-positive, patients recovered, whereas 1 patient with congenital oxidase-negative, motile gram-negative bacillus that hypophosphatasia and severe malnutrition who devel- forms yellow-pigmented colonies in blood cultured on

Table 4. Summary of reported cases of infection by Pseudomonas luteola

Acquired Y Antibiotic Author Country source Age /Sex Site of infection Predisposing factor Outcome treatment

Connor et al. United States Hospital 41/M Recurrent Continuous ambulatory Cured TOB, CFZ (1987) (23) of America peritonitis peritoneal dialysis Freney et al. Belgium Hospital 5 months/M Sepsis Atrial reconstruction surgery Cured CTX, NET (1988) (22) Kostman et al. United States Hospital 32/F Meningitis Neurosurgery Cured CAZ (1991) (24) of America Kostman et al. United States Hospital 59/M Surgical site Neurosurgery Cured CAZ (1991) (24) of America infection Rahav et al. Israel Community 26/M Femur NR Cured CP (1995) (18) osteomyelitis Rahav et al. Israel Community 26/F Peritonitis Perforation of the stump Cured GM, AMP, (1995) (18) of appendix MTZ Rahav et al. Israel Community 83/M Peritonitis Colon carcinoma Died GM, AMP, (1995) (18) MTZ Rahav et al. Israel Hospital 26/F Bacteremia Neurosurgery, central line Cured CP (1995) (18) Rastogi et al. United States Community 59/M Facial cellulitis NR Cured CTX (1998) (14) of America and bacteremia Ghosh et al. United Community 28/F Facial erosive Human immunodeficiency Cured CP (2000) (13) Kingdom ulcer virus (HIV) Tsakris et al. Greece Community 38/F Leg ulcer Sickle cell disease Lesion was No antibiotic (2002) (15) deteriorated was given Dalamaga et al. Greece Community 65/M Bacteremia and Intramuscular Cured CAZ, AK (2004) (6) cutaneous abscess acetaminophen injections Jayagopal et al. United Community 49/M Hand Working in tree clearing Cured OXT, CP (2004) (17) Kingdom osteomyelitis industry Chihab et al. Morocco Community Newborn/M Sepsis NR Died CTX, GEN (2004) (9) Chihab et al. Morocco Hospital 13/M Infective Mitral valve replacement Died CTX (2004) (9 endocarditis surgery Sabir et al. Pakistan Hospital 52/M Catheter-related Recurrent meningiomas, Cured OFX, AZT, (2004) (19) bacteremia diabetes, asthma AK Yetkin et al. Turkey Community 21/M Infective Ventricular septal defect Cured CAZ, GEN (2005) (10) endocarditis Casalta et al. France Community 53/M Infective Prosthetic valve Cured TIM (2005) (11) endocarditis Uy et al. Philippines Hospital 61/F Endophthalmitis Cataract surgery Cured PTZ, STX (2007) (21) Gaschetetal. France Community 3/M Brain abscesses NR Cured MTZ, CP, (2009) (5) MERZ Ramana et al. India Community 50/M Bacteremia Pyocele of the scrotum and Cured AMC, CP (2010) (7) Fournier's scrotal gangrene Goteri et al. Italy Community 16/F Mediastinal High-dose steroid therapy Cured MERZ, CP (2010) (12) abscess De et al. India Hospital 60/M Biliary infection Cholecystectomy Cured CTX, GM (2010) (16) Ngoh et al. Morocco Hospital 60/M Sepsis Diabetes, asthma, Died IMP, AK, (2011) (20) hypertension TEC, FLC Wen et al. United States Community 14/M Bacteremia Pulmonary arterial hyperten- Cured PTZ, VA (2013) (8) of America sion, receiving intravenous treprostinil therapy

Y,year;M,male;F,female;NR,notreported;CTRX,cefotaxime;NET,netilmicin;TOB,tobramycin;CFZ,cefazolin;TEC,teicoplanin; AMP, ampicillin; AMC, amoxicillin-clavulanic acid; FLC, fluconazole; OXT, oxytetracyclin; OFX, ofloxacin; MTZ, metronidazole; TIM, ticarcillin-clavulanic acid.

52 Bacteremia Caused by Pseudomonas luteola

MacConkey agar. P. luteola is an environmental organ- genetic analysis, as a facility for this analysis is not ism that is also found in healthcare environments (1,2). available at our institution. The diagnostic sensitivities P. luteola rarely causes community- or hospital- and specificities of these tests for the investigation of acquired infection in humans, and the literature in- most positive blood cultures are extremely high, but cludes only few case reports. In a study from Tanzania some PCR assays could fail to identify gram-negative that investigated extended spectrum beta-lactamases rods including P. luteola andnospecificPCRassayfor among gram-negative bacteria of nosocomial origin, P. P. luteola had been developed (25). luteola was reported as a nosocomial pathogen in 1 In conclusion, we believe that P. luteola may be more patient in an intensive care unit of a tertiary hospital (4). common in children than previously reported. P. luteola In this study, we reviewed all cases of infection related can cause both community- and hospital-acquired to P. luteola from 1988 to date (Table 4) (5–24). Of the bacteremia. Amikacin, gentamicin, trimethoprim-sul- reported cases of P. luteola, bacteremia was the most famethoxazole, and meropenem were effective against common infection. Community-acquired infections P. luteola in the present study. Empirical treatment of were more commonly reported than hospital-acquired nosocomial infections, including P. luteola infections, infections. Only 6 pediatric patients with P. luteola in- with carbapenem antibiotics is considered the appropri- fection have been reported. P. luteola infections have ate regimen at our hospital. been reported from the United States of America, Eu- rope, Africa, and Western and Southern Asia (4–24). Conflict of interest None to declare. 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