EXTENSIVELY DRUG-RESISTANT PSEUDOMONAS AERUG- INOSA OUTBREAK … · 2019-06-08 · EXTENSIVELY...

EXTENSIVELY DRUG-RESISTANT PSEUDOMONAS AERUG-INOSA OUTBREAK IN A BURN UNIT: MANAGEMENT ANDSOLUTIONS

ÉPIDÉMIE À PSEUDOMONAS ÆRUGINOSA DANS UN CTB: ÉVALUATIONET ÉRADICATION

Aguilera-Sáez J.,* Andreu-Solà V., Larrosa Escartín N., Rodríguez Garrido V., Armadans Gil L.,Sánchez García J.M., Campins M., Baena Caparrós J., Barret J.P.

Vall d’Hebron University Hospital, Barcelona, Spain

SUMMARY. Infections are still the main cause of mortality in burn patients. Multidrug resistant bacteriacan cause outbreaks in critical care and burn units. We describe an outbreak of infection by extensivelydrug-resistant Pseudomonas aeruginosa in the Burn Unit of a University Hospital in Barcelona (Spain) be-tween April and July 2016. A descriptive study of all cases, a bacterial colonization screening of all admittedpatients and a microbiological environmental study were performed in order to detect a possible commonfocus. Contact isolation and cohortization of healthcare workers of all infected or colonized patients wereapplied. Environmental control measures were instituted for possible sources of infection. The outbreak wascaused by a strain of P. aeruginosa only sensitive to colistin. Ten patients were infected or colonized andtwo of them died. The same strain was detected in several taps and drains in different rooms of the Unit.After applying control measures, changing faucets and drains, carrying out thermal disinfection of the hotwater installation of the unit, disinfecting the rooms with ultraviolet radiation and placing antibacterial fil-tration devices in all the taps among other measures, an effective control of the outbreak was achieved.

Keywords: burns, Pseudomonas aeruginosa, outbreak, burn centre, extensively drug-resistant

RÉSUMÉ. Les infections sont toujours une cause majeure de mortalité chez les brûlés. Des épidémies àbactéries multirésistantes (BMR) dans les CTB sont régulièrement rapportées. Nous décrivons une épidémiedue à Pseudomonas æruginosa BMR, sensible uniquement à la colimycine, survenue dans le CTB d’un hô-pital universitaire de Barcelone entre avril et juillet 2016. Elle a touché 10 patients dont 2 sont morts. Uneétude de chaque cas, un dépistage chez tous les entrants et une étude environnementale ont été réalisées,afin de trouver d’éventuelles similitudes. Un isolement contact et un cohorting ont été mis en place. Desmesures de contrôle de l’environnement ont été implémentées. La souche incriminée a été retrouvée dansplusieurs robinets et siphons du service. Cette épidémie a été résolue après, outre les mesures précitées,changement des robinets et des siphons (avec mise en place d’ultrafiltres sur les robinets), choc thermiquedu réseau d’adduction d’eau, désinfection terminale UV des chambres.

Mots-clés : brûlure, Pseudomonas æruginosa, épidémie, CTB, BMR

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* Corresponding author: J. Aguilera-Sáez, Department of Plastic Surgery and Burn Centre, Vall d’Hebron University Hospital, c/ Passeig de la Vall d’Hebron 119-129,08035, Barcelona, Spain. Tel.: +34 934893475; email: [email protected]: submitted 14/03/2019, accepted 21/04/2019

Annals of Burns and Fire Disasters - vol. XXXII - n. 1 - March 2019

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Introduction

After the initial resuscitation of burned patients, upto 75% of patient deaths are related to an infectiousprocess.1 Several factors contribute to the high fre-quency and severity of these infections and to theirmultiple possible locations: the destruction of the skinallows easy access of microorganisms, the presence ofnecrotic tissue provides an optimal growth mediumfor them, invasive monitoring facilitates other entrypoints and, finally, nonspecific alteration of immunefunction allows microbial proliferation.1

Pseudomonas aeruginosa is a gram-negative,aerobic and non-fermenting bacterium that is widelydistributed in nature. Soil, plants or running watercan act as a reservoir, with a predilection for humid,even nutrient-deficient environments.2,3 The easewith which P. aeruginosa grows both in nature andinside hospitals, and its capacity to acquire resist-ance mechanisms to antibiotics, make it one of themost significant causes of serious nosocomial infec-tion, affecting mainly immunocompromised pa-tients.4,5 Infection between hospitalized patientsoccurs mainly through the hands of healthcare work-ers but also through contact with contaminated sur-faces and objects.3

The number of published outbreaks caused bymultidrug-resistant (MDR) bacteria in burn unitsover the last 30 years is relatively small. Of these,few come from developed countries, and diagnosticand screening techniques have changed in recentyears.6 Early detection of the outbreak can facilitateits control and limit its spread. The objective of thiswork is to describe an outbreak caused by exten-sively drug-resistant P. aeruginosa (XDR-PA)7 in theBurn Unit of the Vall d’Hebron University Hospitalin Barcelona (Spain) between April and July 2016,and the measures adopted to control it.

Material and methods

The Vall d’Hebron University Hospital ofBarcelona (Spain) is a health centre with more than1100 beds. The Burn Unit is an integral unit that hassix beds for critical patients, 16 beds for semi-criticalor non-critical patients and four beds for pediatric pa-

tients. It also has its own operating room, a room foroutpatient treatment, an emergency room, a rehabili-tation area, a room for hydrotherapy and a gamesroom, along with other rooms for storage and workareas for healthcare workers. It forms part of the Cen-tres, Services and Reference Units (CSUR) of theSpanish National Health System for critically burnedpatients, and its direct area of influence includes Cat-alonia, the Balearic Islands and Andorra, covering apopulation of more than 8,000,000 people.

Epidemiological investigationA case was defined as any patient admitted to the

Burn Unit who, as of April 2016, presented infectionor colonization by P. aeruginosa with “in vitro” re-sistance to all the antibiotics evaluated except col-istin. Weekly screening by rectal smear wasperformed on all patients admitted to the Unit to de-tect possible colonization, in addition to the culturesthat were performed in case of suspected infection.This screening was extended to patients who wentto the outpatient and rehabilitation treatment roomsand who had been admitted as of April 2016.

Microbiological studyIn order to detect possible reservoirs and environ-

mental sources from which the pathogen could havebeen transmitted, seven rounds of environmental sam-pling were performed in which samples were takenwith a swab, and on three occasions, water sampleswere taken. A total of 290 samples were collected,which included hot and cold water, moisturizers, soapsand antiseptic solutions, the aerators from all taps, theinternal surfaces of the tap pipes and all of the draingrates, the surfaces of containers and other environ-mental surfaces (Table I). The surfaces were sampledusing wet sponges with neutralizing buffer (3MTM

Sponge-Stick, USA). Likewise, samples of hot andcold water were obtained from all of the taps in theUnit. The samples of hot water were obtained follow-ing the recommendations published in “Health Tech-nical Memorandum 04-01: Safe water in healthcarepremises: Part C - Pseudomonas aeruginosa - advicefor augmented care units”. In the hot water taps, a 2-Lwater sample was obtained after 2 hours of not usingthe tap, and another 2-L sample was obtained after 2min of letting the water circulate.


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The sponges were incubated overnight at 37ºC andwere then planted in selective and differential media toinvestigate the presence of P. aeruginosa and mul-tidrug-resistant gram-negative bacilli. The water sam-ples were filtered through a 0.45-µm Millipore filterand cultured in the appropriate selective media.

The clinical samples were seeded in selective anddifferential culture media, some of which specific forthe search for resistant microorganisms. In the case ofurine and respiratory samples, quantitative cultureswere inoculated. All media were incubated at 35ºC insuitable atmospheres, with reading and interpretationafter at least 24 hours had elapsed.

As regards monitoring samples (stool samples takenby rectal swab) for colonization, active searches formultidrug-resistant gram-negative bacilli were madewith specific selective media.

Antimicrobial susceptibility to beta-lactam antibi-otics with antipseudomonal activity (piperacillin-tazobactam, aztreonam, ceftazidime, cefepime,imipenem and meropenem), aminoglycosides (gentam-icin, tobramicin and amikacin), quinolones(ciprofloxacin), fosfomycin and colistin was deter-mined by disk diffusion in Mueller-Hinton agar and an-tibiotic gradient strip test, following the EUCASTguidelines (www.eucast.org). The presence of metallo-beta-lactamase production (MBL) was screened by themodified Hodges test and double-disk synergy testusing imipenem and imipenem+EDTA and confirmedby Polymerase Chain Reaction (PCR). In this case spe-cific primers for the detection of the MBL-encodinggenes blaVIM, blaIMP and blaNDM were used.8

Clonal relatednessPulsed-field gel electrophoresis (PFGE) of the re-

striction fragments of total bacterial DNA, obtainedby means of the restriction enzyme Spel (Roche,USA) was performed to confirm the clonal relation-ships of the P. aeruginosa isolates. All of the isolatesfrom the culture of the clinical samples, along withthose from the previously mentioned colonizationand environmental samples, were studied using thistechnique. DNA separation was performed in theCHEF-DRII pulsed field electrophoresis system(Bio-Rad, USA) according to the conditions de-scribed previously.9 The gel images were capturedusing the Gel DocTM XR system (Bio-Rad, USA),

and the analysis of the macro-restriction profiles wasperformed with the GelCompar II program (AppliedMaths, Belgium) using the Dice similarity index,which is based on UPGMA (unweighted pair groupmethod using arithmetic averages). For the genera-tion of the dendrograms, a position tolerance valueof 1.0% was accepted. The clonal relationship wasdetermined by comparisons of the macrorestrictionprofiles of each of the isolates studied. Thus, twoisolates belonging to the same clone were definedbased on a similarity higher than 85%.10

Control measures takenAll infected or colonized patients were sub-1jected to contact precautions. Isolation pre-cautions were adopted by the healthcareworkers (personnel dedicated exclusively toinfected or non-infected patients). Compliance with basic infection prevention2measures (hand hygiene, aseptic measures,cleaning and disinfection of surfaces andmaterials) was reinforced through trainingsessions with the professionals of the unit.A review of the antimicrobial treatment pro-3tocols and antibiotic policy of the unit wasconducted, with the aim of reducing antibi-otic pressure and limiting the developmentof multidrug-resistance. We do not performempirical systemic antibiotic treatment in ageneralized way on admission. In caseswhere infection is suspected in the first 72hours of admission, in patients who have hadno previous relationship with the health sys-tem and no colonization by Pseudomonasaeruginosa is suspected, amoxycillin/clavu-lanic acid is preferentially administered, afterobtaining samples for microbiological cul-ture. In contrast, in patients with criteria ofpossible colonization or infection byPseudomonas aeruginosa or with more than72 hours of admission, broad-spectrum an-tibiotic therapy is initiated, preferablypiperacillin-tazobactam. The use of car-bapenems, aminoglycosides, glycopeptidesor other antimicrobials is reserved for pa-tients with septic shock or prolonged admis-


4

Fig. 1

Results

8P. aeruginosa

8

TableII

Table II Fig. 1

P. aeruginosa

Fig. 1


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progressed to multi-organ failure and death; in oneof them, the septic shock was secondary to a respi-ratory infection by XDR-PA, and in the other, it wassecondary to an infection of the burns by XDR-PA.

The results of the environmental study are shownin Table I. The strain of XDR-PA that caused theoutbreak was detected in the tap aerator and the tapplumbing of four rooms occupied with patients col-onized or infected by said bacteria. This strain wasalso detected in the grates of the basin drains of tworooms occupied by infected patients (in one of theserooms, two consecutive patients acquired XDR-PA;in the drain of the basin in the other room, XDR-PAwas detected only in the second sampling), in theaerator of the tap of the hydrotherapy room and inthe grate of the basin drain of the nurses’ station(Fig. 2).

The molecular epidemiology study using thePFGE technique showed that all the isolates ofXDR-PA obtained from clinical and environmentalsamples were identical.

With the progressive application of the controlmeasures mentioned above, no more cases were de-tected, and all of the environmental samples were

negative for XDR-PA (Fig. 1); therefore, the out-break was considered controlled in September 2016.Patient no. 8 remained hospitalized and colonizedby XDR-PA until October 2016. For the early detec-tion of a possible recontamination, a protocol wasestablished that includes the monthly sampling ofthe Unit’s water and the taps and plumbing. On 1st

November 2018, no new episodes of XDR-PA infec-tion had been detected, nor were positive environ-mental samples detected.

Discussion

P. aeruginosa is an opportunistic bacterium witha large environmental reservoir that can cause seri-ous systemic infections of any type (respiratory, uri-nary, cutaneous or soft-tissue infections, orbacteremia, among others) in patients with severecomorbidities or some type of immunosuppression,such as occurs with extensive burns. Its multiplestructural (capsular exopolysaccharides, adhesins,pili, diffusible pigments, endotoxins), toxigenic (ex-otoxins A, S and T) and enzymatic (elastase, alkaline

Environmental study

Date Objects investigated (n samples) Pseudomonas aeruginosa positive samples (n samples)

MDR Pseudomonas aeruginosa positive objects

1 14/06/2016 Faucet aerators (7) Sink drain grilles (7)

4 faucet aerators

1 sink drain grille

4 faucet aerators

1 sink drain grille

2 21/06/2016 Tap pipes (6) 4 tap pipes 4 tap pipes

3 27/06/2016 Hot water (12 samples) 0 0

4 12/07/2016 Faucet aerators (5) Sink drain grilles (3)

1 sink drain grille 1 sink drain grille

5 22/07/2016 Hot water (92 samples) Faucet aerators (48) Sink drain grilles (45) Environmental surfaces (18) Body milks, soaps & antiseptics (9)

Container surfaces (6)

Hot water (1 sample) Faucet aerators (5) Sink drain grilles (19) Environmental surfaces (3) Body milks, soaps & antiseptics (1)

1 faucet aerator

1 sink drain grille

6 29/07/2016 Cold water (5) 0 0

7 23/08/2016 Faucet aerators (3)

Sink drain grilles (26)

Environmental surfaces (1)

4 sink drain grilles 1 sink drain grille

Table I - Summary of environmental studies, and objects from which the outbreak strain was isolated


P. aeruginosa

Fig. 2

Table II

Case Age Date of

admission First positive culture date

Sample TBSA (%) Mechanical ventilation

Urinary catheter

Total admission

days Evolution

1 80-90 23/03/2016 25/04/2016 Urine 15% No Yes 43 Discharged

2 30-40 28/04/2016 05/05/2016 Urine 30% Yes Yes 63 Discharged

3 50-60 16/04/2016 09/05/2016 Rectal swab 21% No Yes 38 Discharged

4 40-50 02/05/2016 09/05/2016 Rectal swab 28% No Yes 7 Discharged

5 70-80 11/04/2016 17/05/2016 Urine Sequels of

scleroderma

No No 50 Discharged

6 40-50 10/05/2016 27/05/2016 Rectal swab 5.5 % No No 23 Discharged

7 50-60 24/04/2016 28/05/2016 Tracheal aspirate 40% Yes Yes 57 Dead

8 20-30 12/05/2016 02/06/2016 Wound swab 70% Yes Yes .. Admitted

9 30-40 29/06/2016 06/07/2016 Tracheal aspirate 80% Yes Yes 39 Dead

10 40-50 08/07/2016 18/07/2016 Tracheal aspirate 88% Yes Yes 62 Discharged


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strated to be one of the most frequent causes of ac-quiring P. aeruginosa in Intensive Care Units (ICU)since only between 20% and 33% of patients are col-onized at admission.3 In addition, cross-transmissionbetween patients has been identified in between 8%and 50% of infections or colonizations acquired dur-ing admission.3 In these cases, healthcare workerswould be the most likely vector. Reinforcing handhygiene of healthcare workers is one of the most es-sential measures to prevent cross-transmission of in-fections. An educational program to promote handhygiene among healthcare workers is well estab-lished in our centre following the World Health Or-ganization (WHO) multimodal hand hygienestrategy12 and annual monitoring of hand hygienecompliance is performed by direct observationalmethod. Alcohol-based handrub is the most usedmethod for routine hand antisepsis in our setting,using soap and water when hands are visibly dirty orsoiled with blood or body fluids. In 2016, the ob-served adherence of hand hygiene in the burn unit ofour hospital was about 70.4%.

However, for 30% to 60% of the remaining cases,there is plausible evidence from previous studies thatstrains of P. aeruginosa found in washbasins, hy-drotherapy tanks, taps and water from these taps canbe a source for colonization and infection of patients,especially in ICUs.3,13-15 The persistence of P. aerug-inosa in adverse media is due to its capacity to formbiofilms.5 Transmission might be caused by splash-ing of water droplets from contaminated sinks tohealthcare personnel’s hands, which may becometransiently colonized;16 then these hands might comeinto contact with the patient or with invasive devicessuch as an orotracheal tube, a vascular catheter or aurinary catheter. Although in outbreaks related towater environment the routes of transmission havebeen difficult to characterize, in most of them the re-inforcement of hand hygiene and contact precautionshas been associated with a significant reduction intransmission.17 In the present outbreak, XDR-PA wasfound in the tap aerators of four rooms and in thegrates of the basin drains of two additional roomswhere patients colonized or infected by XDR-PAwere admitted. To relate the possible sources with thecases, an epidemiological study is required, and cur-rently only genotypic methods are considered ade-

quate to relate the isolates,3 such as PFGE, as usedin the present outbreak.

The transmission of strains from patients to drainshas also been described in the literature.13 This ob-servation emphasizes the importance of minimizingroom changes of patients infected or colonized byXDR-PA as much as possible to avoid the spread ofthese microorganisms. For all of these reasons, thedisinfection of the taps, basins and drains of the ICUsand Burn Units is of vital importance. However, Gar-vey et al.15 demonstrated that following the nationalguidelines of the British Department of Health on theuse and maintenance of the water supply system wasnot sufficient since transmission persisted. This as-sessment has led to the description of alternativemethods for cleaning and disinfecting the surfaces ofthe basins, grates and drains.18,19 Finally, it has beendescribed that the use of point-of-use tap filters is as-sociated with a decrease in number of colonizationsand infections,3,20 with a lower cost than a strategyinvolving the use of sterile bottled water.20

However, in our outbreak, after having identifiedthe facility that supplies sanitary hot water as a po-tential source and having adopted corrective meas-ures (replacement of taps and aerators, disinfection),two more cases of XDR-PA infection were detected.In addition, the times between admission and acqui-sition of XDR-PA were shorter in these two casescompared with the others. These two cases corre-sponded to patients who were admitted to rooms inwhich other infected patients had been admitted. Ina previous prospective observational study,21 it wasfound that admission to an ICU room previously oc-cupied by a patient with MDR-PA increases the riskof acquisition of this bacterium in subsequent pa-tients, and the time to acquire the bacterium was alsoshorter. This has been related to the fact that disin-fection and cleaning of these rooms does not com-pletely eliminate these pathogens22 and suggests thatthe contamination of surfaces of the rooms, and ofthe basins and drains, can play a role in the transmis-sion of MDR-PA.21 Interestingly, in the present study,XDR-PA was detected in the drain grate of a basinfrom one of the two rooms where two patients werepositive for XDR-PA. Another recent study23 associ-ated a more intense terminal disinfection of therooms with a decrease in the risk of infection of the


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organisms studied (methicillin-resistant Staphylo-coccus aureus, vancomycin-resistant Enterococcus,and multidrug-resistant Clostridium difficile andAcinetobacter spp.); however, this work did not in-clude MDR-PA as an object of study. This observa-tion suggests that objects and surfaces may play arole in the spread of certain microorganisms and,therefore, that the use of the ultraviolet radiation dis-infection system used in the present outbreak mayhave played an important role in their control.

The investigation of the survival mechanisms ofinanimate environments and the dispersion mecha-nisms of these microorganisms is fundamental to un-derstanding and stopping these outbreaks. Forexample, it would be useful to investigate the de-signs of taps and drains to reduce their contamina-tion and to avoid spreading, since one of thepostulated forms of transmission is related to splash-ing from the drains, possibly due to basins designedin such a way that the stream of water directly hitsthe drain.19

Several studies have been published on the im-pact that multidrug-resistant P. aeruginosa has onthe increase in mortality rates, the hospitalization pe-riod and, to a lesser extent, the economics. In gen-eral, it is estimated that infections caused bymultidrug-resistant P. aeruginosa are associated witha higher mortality rate, a prolonged period of hospi-talization and increased costs compared with infec-tions caused by antibiotic-susceptible bacteria,especially in terms of increased pharmaceuticalcosts.24-27 The secondary expense of the implemen-tation of the different control measures (replacementof contaminated taps and drains, bacterial filtrationsystems in taps, ultraviolet irradiation, among other

measures) could be justified if the eradication of theoutbreak and a decrease in the number of baselinecases with multidrug-resistant microorganisms areachieved.

On February 27, 2017, WHO published a list ofthe 12 bacteria that require priority research for thedevelopment of new antibiotics.28 P. aeruginosa re-sistant to carbapenems is one of the critical prioritygroup. These multidrug-resistant bacteria constitutea serious public health problem.

Conclusions

In April 2016, there was an outbreak of infectionby extensively drug-resistant P. aeruginosa in theBurn Unit of a university hospital in Barcelona(Spain), with 10 patients affected. The epidemiolog-ical investigation revealed the existence of environ-mental reservoirs in the taps and drains of the Unit.The application of strict control measures againsttransmission, the strict adherence by healthcareworkers to infection control policy, the use of an an-tibiotic protocol, along with the replacement of tapsand drains and the installation of bacterial filterswere associated with an effective control of the out-break.

P. aeruginosa infections continue to be a majorconcern among burn patients because they drasti-cally worsen the prognosis of these patients, and out-breaks are not uncommon in burn units. We believethat research should be promoted in this field, asshould the exchange of experiences to control oneof the greatest threats to modern medicine: microor-ganisms resistant to multiple antibiotics.

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E R R A T A C O R R I G E

As an author of the article "TWELVE YEARS OF LYELL'S SYNDROME IN THE BURN UNIT OF SÃO JOÃO HO-SPITAL CENTER" I declare that Pedro Reis, affiliated to the Department of Plastic Surgery and Burn Unit ofSão João Hospital Center (Porto, Portugal) is a co-author and contributed for this work.

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