Nosocomial Infections with IMP-19−Producing Pseudomonas aeruginosa Linked to Contaminated Sinks, France

We isolated IMP-19–producing Pseudomonas aeruginosa from 7 patients with nosocomial infections linked to contaminated sinks in France. We showed that blaIMP-19 was located on various class 1 integrons among 8 species of gram-negative bacilli detected in sinks: P. aeruginosa, Achromobacter xylosoxidans, A. aegrifaciens, P. putida, Stenotrophomonas maltophilia, P. mendocina, Comamonas testosteroni, and Sphingomonas sp.


The Study
The hematology department of the hospital contains a 15-bed conventional unit and a 9-bed protective isolation unit. At the entrances of rooms in the conventional unit, there is a hand hygiene sink (for staff and visitors) and a bathroom in a separate area (shower stall, sink, and toilets). In the protective isolation unit, air is filtered through a laminar flow system, and a sink and toilets are located next to each bed (distance 1.5 m). The ceramic sinks have no counter space, and drains are made of stainless steel. All faucets in the department are hand-operated and provided with antibacterial filters (0.22 µm). Surfaces are cleaned daily (once in the conventional unit and twice in the protective isolation unit) with a solution containing quaternary ammonium compounds (0.25% didecyldimethylammonium chloride).
During 2009-2016, a total of 7 patients (P1-P7) in the department were infected or colonized by IMP-19-producing P. aeruginosa, which were isolated from blood samples (2 patients), urine samples (2 patients), throat swab samples (2 patients), and a central venous catheter (1 patient). All patients underwent throat, urine, and feces sampling at admission and were free of P. aeruginosa, thus indicating nosocomial acquisition. All isolates were resistant to ceftazidime, imipenem, meropenem, doripenem, ciprofloxacin, and most aminoglycosides; 4 isolates were susceptible to piperacillin and 3 to amikacin.
We conducted an environmental investigation in the hospital ( Figure 1, https://wwwnc.cdc.gov/EID/article/ 23/2/16-0649-F1.htm). More than 100 environmental samples were obtained when no patients were colonized (except for samples collected in room 32 a few hours after patient P7 had been transferred to an intensive care unit). Water samples were collected from different faucets (nursing room, medication preparation rooms, and rooms of some patients). First-catch lukewarm water (500 mL) was collected in sterile bottles containing 20 mg/L sodium thiosulfate and concentrated by filtration (0.45µm membrane filters). All sinks and shower drains were sampled by rotating a cotton swab inserted through the drain. Toilets were sampled with swabs inserted under the rim of the toilet bowl.
We plated samples from filters (for water) and swab specimens (from sinks) on Drigalski medium containing ceftazidime (32 mg/L). When a positive culture was observed after 48 hours of incubation, a PCR specific for bla  was performed for the culture mixture. For samples with a positive PCR result, we then plated a dilution of the culture mixture on Drigalski medium containing ceftazidime (32 mg/L) and imipenem (16 mg/L) to obtain isolated colonies, which we further subjected to identification and confirmation of IMP-19 production.

Nosocomial Infections with IMP-19-Producing
Pseudomonas aeruginosa Linked to Contaminated Sinks, France Many resistant organisms were detected in these environmental samples. We used mass spectrometry and nrdA gene sequencing to identify for Achromobacter isolates (6). bla  and integrons were detected as described (7,8). We used pulsed-field gel electrophoresis after XbaI digestion to genotype P. aeruginosa isolates (9). Pulsotypes were compared by calculating the Dice correlation coefficient with DendroUP-GMA software (http://genomes.urv.cat/UPGMA/).

Conclusions
The incidence of MBL producers among imipenemresistant P. aeruginosa in France is low compared with incidences for other countries (2,10). Reports of outbreaks are scarce and usually involve VIM producers (11,12). Therefore, detection of IMP-19 producers in our hospital was unusual. The long intervals without cases, the absence of any overlap between cases, and genotypic diversity of clinical isolates did not suggest a single common source of infection. These findings prompted us to conduct environmental investigations.
IMP-19 producers were detected in 9 of 15 rooms in the conventional unit and 2 of 9 rooms in the protective isolation unit. These producers were P. aeruginosa and a wide variety of gram-negative nonfermenting bacilli. Most of these producers have little clinical relevance, but they are silent reservoirs for dissemination of bla IMP-19 to major pathogens. The role of these environmental bacterial species in the spread of MBL suggested in previous studies (13,14) is confirmed by our findings.
The diversity of species found and genetic structures involved with bla IMP-19 indicated that the environmental contamination occurred a long time ago. One isolate of IMP-19-producing Aeromonas caviae was found in a patient in the same building in 2006 (7). This phenomenon is probably endemic to our hospital, in which sink drains are not accessible for removal of biofilms without complete dismantling (inappropriate sink design).
Transfer of pathogens from sinks to patients might occur in several ways. Water from faucets is directed Infections with IMP-19-Producing P. aeruginosa straight into the drain, resulting in splashing that can lead to contamination of an area <1 m from the sink (15). Therefore, patients can be contaminated when they brush their teeth, wash their hands, or take a shower. Healthcare personnel are also at risk for hand contamination, which might lead to transfer of pathogens to patients during care.
All patients had >1 stay in rooms that were positive for IMP-19-producing organisms. After patient P7 died of sepsis, all drains in the ward were changed. However, this  Infections with IMP-19-Producing P. aeruginosa measure did not eradicate biofilms found in the plumbing system. Because the building tested was 16 years old, it has been decided to completely rebuild the ward in early 2017, paying special attention to water distribution and discharge systems to minimize hospital-acquired infections. In conclusion, our findings might help other hospitals to identify potential reservoirs of carbapenemase-producing bacteria and lead to implementation of rapid control measures to contain outbreaks.