Hospital water is an important source of healthcare-associated infections, mostly caused by Pseudomonas aeruginosa. Nevertheless, other nonfermentative gram-negative bacilli (NFGNB) present in water are increasingly recognized as a cause of infection, especially in immunocompromised and critically ill patients.Reference Wang, Chen, Eason Lin, Chang and Chen 1 Chryseobacterium indologenes is an NFGNB primarily found in soil and water.Reference Lambiase, Del Pezzo, Raia, Sepe, Ferri and Rossano 2 It has intrinsic resistance to several antimicrobial classes, such as cephalosporins and carbapenems, due to the presence of metallo-β-carbapenemases.Reference Chen, Wang, Teng, Ou, Yu and Lee 3 Since 2009, Chryseobacterium has been identified in environmental samples from hospital tap water, disinfectants, and respiratory equipment. It has also been postulated to be a potential pathogen in critically ill patients.Reference Wang, Chen, Eason Lin, Chang and Chen 1 , Reference Peñasco, Duerto, González-Castro, Domínguez and Rodríguez Borregan 4 – Reference de Las Casas Cámara, Martín-Ríos, Adillo-Montero, Muñoz-Egea, Zapardiel-Ferrero and Pérez-Jorge Peremarch 6
Several healthcare-facility outbreaks of NFGNB and Enterobacteriaceae related to contaminated drainage system water have been described.Reference Trautmann, Michalsky, Wiedeck, Radosavijevic and Ruhnke 7 , Reference Bloom 8 Immunocompromised host and critically ill adults as well as neonates are the groups most commonly affected.Reference Kanamori, Weber and Rutala 9
This study describes a cluster of C. indologenes infections and colonizations, probably related to sink drainage water, in intensive care unit (ICU) patients and the measures implemented to control it.
Methods
The study was conducted in 2 adult ICUs in a 613-bed tertiary-care hospital. The hospital attends a range of patients referred from other hospitals. The medical ICU admits coronary as well as any other nonsurgical adult patients; the ICU comprises 2 units of 11 single rooms with 1 handwashing sink per bed. Patients from most surgical specialties, including heart, lung, liver, and kidney transplant, are attended in the surgical ICU, which has two 10-bed bays sharing 6 handwashing sinks per bay. A room for reprocessing and storage of respiratory devices for the surgical ICU occasionally serves both ICUs. The ICUs do not share healthcare personnel.
All patients admitted to these critical units are sampled for methicillin-resistant Staphylococcus aureus (MRSA; nasal and pharyngeal swabs) and for extended-spectrum beta-lactamase (ESBL) and/or carbapenem-resistant gram-negative bacilli (GNB; rectal and respiratory tract samples) at admission and weekly thereafter.
A case patient was defined as an ICU patient in whom C. indologenes was isolated from a clinical or surveillance culture. A patient was considered infected when (1) the patient met Centers for Disease Control and Prevention (CDC) criteria for healthcare-associated infectionReference Horan, Adrus and Dudeck 10 or (2) the patient developed changes in clinico-physiologic parameters (ie, systemic inflammatory response syndrome) concurrently with C. indologenes isolation. Colonized patients were those who did not meet any of the above criteria.
Swab samples from tap, faucet aerators, sinkholes, hemodialysis draining traps, and wash basins, as well as tap and distilled water, bronchoscope rinse water, dialysate solution, intravenous infusions, and aqueous chlorhexidine were obtained. Free residual chlorine tests of ICU tap water were performed. Air sampling was performed using an SAS-SuperISO-180 air sampler (International PBI, Milano, Italy) in a standard blood-agar media. One cubic meter of air was sampled close to the basin (within 50 cm) while flushing tap water.
All microbiological samples were seeded on blood agar. Identification of isolates from patients and environment samples was made using matrix-assisted laser desorption/ionization time-of-flight mass spectroscopy (MALDI-TOF MS), and the susceptibility tests in clinical samples were performed using a MicroScan system (Beckman Coulter, Brea, California, USA). The genetic relationship between the C. indologenes isolates was determined by pulsed-field gel electrophoresis (PFGE).
We undertook a spatiotemporal analysis of cases by associating bed occupancy of confirmed case patients against each other and possible environmental reservoirs to identify possible routes of cross transmission or point sources. This analysis was reviewed against the sequential effect of the control measures implemented. Mortality attributable to infection was determined by clinical evaluation.
Results
We identified a total of 12 cases from April 4 through May 18 (a rate of 2.72 per 1,000 patient days). All patients had positive samples from the respiratory tract (1 patient also had a positive blood sample). Of these cases, 4 developed pneumonia, and 3 infected patients died. One of these deaths was attributable to the infection. Other clinical and demographical characteristics are displayed in Table 1.
Table 1 Characteristics of Patients Infected and Colonized by Chryseobacterium indologenes
Note. ICU, intensive care unit.
a Unless otherwise specified.
b Cardiac valvular disease (n=3), aortic aneurysm (n=1).
c Lung transplant (n=2), cardiopulmonary transplant (n=1), kidney transplant (n=1).
d Traumatic brain injury (n=1), idiopathic pulmonary fibrosis (n=1).
Most case patients had been previously receiving 3 or more broad-spectrum antibiotics. The previous mean lengths of stay in the hospital and in the ICU were 37 and 17 days, respectively (Table 1). This outbreak was controlled after a third tier of control measures (Figure 1).
Figure 1 Epidemic curve and timing of control measures.
In total, 232 environmental samples were collected. All tap and distilled water, aqueous chlorhexidine, dialysate solution, and intravenous infusions samples were negative for microorganisms. Tap water free residual chlorine levels were above 0.2 ppm.
In addition to the isolates derived from the patients, C. indologenes was recovered from 8 sinkholes of handwashing sinks in patient boxes; 5 of these related to patient cases. Also, C. indologenes was recovered from 3 air samples taken close to the sinks: 1 from the reprocessing room and 2 near handwashing stations in patient boxes. Only 5 of these environmental samples could be analyzed by PFGE typing due to overgrowth of other microorganisms.
The PFGE results from all 12 patients showed a unique pattern indistinguishable from the isolate recovered from the air close to the reprocessing room sink (pattern 1). The other 4 environmental isolates had distinct PFGE patterns, except for a couple of samples from the same box (sinkhole and air close to the basin) sharing the same pattern (pattern 2).
Furthermore, many other species of bacteria, mainly NFGNB but also Enterobacteriaceae and fungi, were recovered from the water drainage system (ie, sinkholes and the hemodialysis draining trap). Most of these microorganisms where also recovered from air samples close to the sinks (Supplementary Table 1).
Discussion
We describe an outbreak of C. indologenes infections and colonizations that resulted in important morbidity and mortality in a critically ill population. In total, 12 patients acquired the microorganism during a 6-week period; 33% of them developed serious infections, and 3 infected patients died (75%). We were able to control the outbreak after 6 weeks.
Interventions to contain the outbreak started shortly after identification of the first cases. They included reeducation of staff on standard and contact precautions, implementation of contact precautions, removal of aerators, provision of bottled water for patients, and point-of-use water filtration for clinical care and respiratory devices reprocessing, but new cases occurred. After closing patient-care handwashing stations, sealing hemodialysis drain connections, establishing waterless patient hygiene, redesigning the reprocessing and storage of material, and training in reprocessing, no new cases appeared for the next 5 months (Figure 1).
We were unable to assure the real mode of transmission. The recovery of the same PFGE of C. indologenes, as well as other microorganisms, from drainage sinks and air in its vicinity, demonstrates that contamination of devices close to the sinks is possible by aerosolization of drainage water, which potentially played a role in this outbreak. Also, contamination of respiratory devices during reprocessing could have played an important role because the same PFGE pattern was shared by patients and the air sample close to the sink in the reprocessing room that occasionally serves both ICUs. Unfortunately, only 5 of the 11 environmental specimens could be analyzed by PFGE; thus, we were not able to prove the contamination of handwashing sinks as the cause of the outbreak. The immediate control of the outbreak after implementation of the third tier of measures would support both hypotheses. Other hypotheses, such as lapses in hand hygiene between patients, also cannot be ruled out.
In conclusion, sinkholes and drains are potentially contaminated and can act as a reservoir for NFGNB and other microorganisms. Tap water flushing may spread them to surrounding areas. Susceptible patients and their equipment should be protected from these splashes because contamination can occur.
Supplementary materials
To view supplementary material for this article, please visit https://doi.org/10.1017/ice.2018.126
Acknowledgments
Financial support
No financial support was provided relevant to this article.
Conflicts of interest
All authors report no conflicts of interest relevant to this article.
