Eur J Clin Microbiol Infect Dis (2007) 26:435–437 DOI 10.1007/s10096-007-0311-7
BRIEF REPORT
Outbreak of Achromobacter xylosoxidans pseudobacteremia in a neonatal care unit related to contaminated chlorhexidine solution J. Molina-Cabrillana & C. Santana-Reyes & A. González-García & A. Bordes-Benítez & I. Horcajada
Published online: 22 May 2007 # Springer-Verlag 2007
Clusters and outbreaks of nosocomial infections occur frequently in neonatal care units (NCU). Achromobacter and Alcaligenes are emerging, infectious, gram-negative, oxidative, bacterial species that can affect immunocompromised patients and those with underlying illnesses. Epidemiological data suggest that water is the natural source of A. xylosoxidans and that most infections may be waterborne [1–3]. Holmes et al. [2] previously described clinical material as the source of this pathogen. In the literature, sporadic cases of bacteremia have appeared [3–5], but outbreaks in adults and newborns have also been reported [6–9]. Some environmental sources contaminated with A. xylosoxidans and associated with nosocomial infections include swimming pools [2], respirators, humidifiers, incubators [6], deionized water [7], tap water, and chlorhexidine solutions [2, 7, 8]. Between January 2004 and June 2005, 58 cases of Achromobacter xylosoxidans colonization or infection occurred in 52 neonates admitted to the NCU of the University Children’s Hospital in Las Palmas, Spain. This NCU is a level III neonatal reference unit that admits a mean of 1,350 newborns annually. It has 15 beds for J. Molina-Cabrillana (*) Department of Preventive Medicine, Complejo Hospitalario Universitario Insular-Materno Infantil, Avenida Marítima del sur s/n, 35016 Las Palmas de Gran Canaria, Spain e-mail:
[email protected] C. Santana-Reyes Division of Neonatology, Department of Paediatrics, Hospital Universitario Materno-Infantil de Canarias, Las Palmas de Gran Canaria, Spain A. González-García : A. Bordes-Benítez : I. Horcajada Microbiology Laboratory, Hospital General Universitario Dr. Negrín, Las Palmas de Gran Canaria, Spain
intensive care, 10 for intermediate care and 30 for minimal care. A case of nosocomial infection was defined as one culture or more that tested positive for Achromobacter xylosoxidans in samples obtained from any body site when clinical evidence of infection in the neonatal population was present. In the absence of clinical evidence of infection, patients with positive results were considered colonized. All infecting strains were considered nosocomially acquired. Medical and nursing procedures were additionally reviewed. Bacteriological cultures of environmental objects such as soaps, antiseptic solutions (chlorhexidine digluconate, aqueous and alcoholic), containers of such solutions, washbasins, incubator surfaces, and faucets were performed. The hands of 39 healthcare workers were sampled by direct fingerprinting in Petri dishes. Fluids were filtered through 0.45 μm membranes (Millipore, Bedford, MA, USA) and cultivated on sheep blood agar (bioMérieux, Marcy l’Etoile, France). For antiseptics, the membranes were rinsed three times with distilled water and cultivated on Tryptic soy agar with Tween 80 (bioMérieux). The swabs were plated onto McConkey and 5% sheep blood agar. Plates were incubated for 24 h at 36°C. Since October 2004, environmental cultures have been performed regularly, but no positive results were obtained prior to June 2005. Biochemical testing was performed using the Vitek System Gram Negative Identification Card (bioMérieux, Durham, USA). Antimicrobial susceptibility testing was performed using standard techniques and Sensititre EMIZA 9EF panels (Trek Diagnostic Systems, West Sussex, UK). Pulsed-field gel electrophoresis (PFGE) of XbaI-digested genomic DNA was performed with a Chief DR-III system (Bio-Rad Laboratories, Hercules, CA, USA). The Statistical Package for the Social Sciences (SPSS, version 11.0) was used for statistical analysis.
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Eur J Clin Microbiol Infect Dis (2007) 26:435–437
The characteristics of the affected newborns and the types of clinical specimens are shown in Table 1. Nonsterile samples (e.g. catheter and exudates) were obtained from neonates aged 10 days or older, whereas positive results for neonates aged 1 day or younger were from blood samples only. Eight of 52 affected neonates were considered infected because signs and symptoms of infection were present without another recognized source of infection. Five neonates had positive blood samples and the three others had positive cerebrospinal fluid samples. Some neonates may have had true bacteremia, as evidenced by leukopenia, a high ratio of immature PMNs to total PMNs, and a C-reactive protein level of more than 1 mg/dl. They also had difficulty breathing and feeding and demonstrated fever and irritability. All symptomatic patients recovered after an appropriate course of antibiotic therapy was instituted (i.e., a 10-day course of ceftazidime or meropenem). The three patients whose cerebrospinal fluid was affected received a 3week course of either ceftazidime (in two cases) or meropenem (in one case). All colonized patients had a favorable clinical evolution without antibiotic therapy. Four neonates died and three of them were hospitalized in the neonatal Table 1 Characteristics of 52 newborns colonized with Achromobacter xylosoxidans and types of positive samples (n=56) Characteristic
Value
Birth weight, mean±SD Gestational age, mean (range) Male/female Preterm/term Age in days, no. (%) 10 Mortality, no. (%) Diagnosis at admission, no. (%) Prematurity Digestive disorder Suspected sepsis Neurologic disorder Malformation Cardiopathy Respiratory distress Othera Location area, no. (%) ICU Non-ICU Type of sample, no. (%) Blood Catheter Cerebrospinal fluid Exudate Peritoneal liquid
2216.4±860 g 43.32 (26–42) weeks 28/24 27/25
a
11 (21.2) 11 (21.2) 30 (57.7) 4 (7.7) 21 (40.4) 5 (9.6) 5 (9.6) 4 (7.7) 4 (7.7) 4 (7.7) 2 (3.8) 7 (17.3) 26 (50) 26 (50) 29 (50.0) 11 (18.9) 9 (15.5) 5 (8.6) 2 (3.4)
Includes convulsions, meconial aspiration, mastitis.
intensive care area; since other clinical conditions explained these deaths, the mortality ratio during the epidemic period was not modified. Achromobacter xylosoxidans was isolated as the sole pathogen from 24 neonates throughout the total NCU stay. A polymicrobial isolate (Achromobacter xylosoxidans plus Proteus mirabilis) was detected in the umbilical exudate of one patient. Environmental sampling detected Achromobacter xylosoxidans on a faucet and in all aqueous chlorhexidine solutions containing a concentration of 0.5 g/100 ml in the NCU. No other organisms were isolated. Microbiological studies showed that the organism was susceptible to trimethoprim–sulfamethoxazole, ceftazidime, imipenem, meropenem, piperacillin, tazobactam, ticarcillin, azlocillin, colistin and cefoperazone. Antimicrobial resistance was demonstrated for gentamicin, netilmicin, cefotaxime, cefepime and ciprofloxacin. Pulsed-field gel electrophoresis (PFGE) with restriction endonuclease XbaI (40 U) showed identical PFGE patterns for the strains obtained from neonates and environmental samples. Hand carriage of A. xylosoxidans was not demonstrated, since the results of repeat cultures were all negative. Our daily observations revealed that hand washing, isolating affected neonates in the same area and other preventive control measures were consistent among staff. Chlorhexidine solution was prepared in the hospital pharmacy and placed in 1-l containers. In the NCU, 100-ml reusable containers had been used for a very long time. Repeat sampling of multiple environmental sites was consistently negative, but on 1 June 2005 microbiological cultures yielded A. xylosoxidans from all aqueous chlorhexidine samples and from a faucet. Samples of the solution obtained from the pharmacy were negative. Apart from two patients who had positive cultures following discharge from the NCU, no cases were detected in any other hospital setting. An explanation for this finding is that aqueous chlorhexidine is mainly used in the NCU area, and reusable containers were used there for the antiseptic solution. It is likely that the containers were contaminated when healthcare workers manipulated and rinsed them with tap water. Neonates were subsequently affected when antiseptic treatment of the skin was required. No further cases occurred following removal of the containers in June 2005. Nevertheless, this outbreak was not identified promptly. In a similar outbreak in India, Kumar et al. [10] were also unable to determine the source. In the outbreak presented here, the identical results of molecular typing of the environmental and patient samples in addition to the immediate and sustained eradication of A. xylosoxidans after control measures were implemented, strongly suggest that the aqueous chlorhexidine containers were the source of the outbreak. This report highlights the
Eur J Clin Microbiol Infect Dis (2007) 26:435–437
importance of hospital surveillance and investigation of unusual clusters of A. xylosoxidans infection and colonization. Prompt identification of unexpected sources of these opportunistic pathogens and implementation of prevention and control measures should curtail outbreaks and protect other patients at risk. References 1. Schoch PE, Cunha BA (1988) Nosocomial Achromobacter xylosoxidans infections. Infect Control Hosp Epidemiol 9:84–87 2. Holmes B, Snell JS, Lapage SP (1977) Strains of Achromobacter xylosoxidans from clinical material. J Clin Pathol 30:595–601 3. Duggan JM, Goldstein SJ, Chenoweth CE, Kauffman CA, Bradley SF (1996) Achromobacter xylosoxidans bacteremia: report of four cases and review of the literature. Clin Infect Dis 23:569–576 4. Gómez-Cerezo J, Suárez I, Ríos JJ, Peña P, García de Miguel MJ, de José M et al (2003) Achromobacter xylosoxidans bacteremia: a 10year analysis of 54 cases. Eur J Clin Microbiol Infect Dis 22:360–363
437 5. Ramos JM, Domine M, Ponte MC, Soriano F (1996) Bacteremia caused by Alcaligenes (Achromobacter) xylosoxidans. Description of 3 cases and review of the literature. Enferm Infecc Microbiol Clin 14:436–440 6. Foley JF, Gravella CR, Englehard WE, Chin TD (1961) Achromobacter septicemia—fatalities in prematures. I. Clinical and epidemiological study. Am J Dis Child 101:279–288 7. Vu-Thien H, Darbord JC, Moissenet D, Dulot C, Dufourcq JB, Marsol P, Garbarg-Chenon A (1998) Investigation of an outbreak of wound infections due to Alcaligenes xylosoxidans transmitted by chlorhexidine in a burns unit. Eur J Clin Microbiol Infect Dis 17:724–726 8. Tena D, Carranza R, Barbera JR, Valdezate S, Garrancho JM, Arranz M, Saez-Nieto JA (2005) Outbreak of long-term intravascular catheter-related bacteremia due to Achromobacter xylosoxidans subspecies xylosoxidans in a hemodialysis unit. Eur J Clin Microbiol Infect Dis 24:727–732 9. Hearn YR, Gander RM (1991) Achromobacter xylosoxidans. An unusual neonatal pathogen. Am J Clin Pathol 96:211–214 10. Kumar A, Ray P, Kanwar M, Sethi S, Narang A (2006) Investigation of hospital-acquired infections due to Achromobacter xylosoxidans in a tertiary care hospital in India. J Hosp Infect 62:248–250
