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ORIGINAL ARTICLE
Pseudomonas aeruginosa infections due to electronic faucets in aneonatal intensive care unitjpc_2248 430..434
Hacer Yapicioglu,1 Tulin Guven Gokmen,3 Dincer Yildizdas,2 Fatih Koksal,3 Ferda Ozlu,1 Eren Kale-Cekinmez,1
Kurthan Mert,1 Birgul Mutlu,1 Mehmet Satar,1 Nejat Narli1 and Aslihan Candevir4
Department of Pediatrics, 1Divisions of Neonatology and 2Pediatric Intensive Care Unit, and 3Department of Microbiology and 4Hospital Infection Control
Committee, Cukurova University, Faculty of Medicine, Adana, Turkey
Aim: To evaluate the role of electronic faucets in a newborn intensive care unit during a Pseudomonas aeruginosa outbreak.Methods: After three patients had P. aeruginosa bacteremia, environmental cultures including those from patient rooms, incubator, venti-lators, total parenteral nutrition solutions, disinfection solutions, electronic and hand-operated faucet filters/water samples after removing filtersand staff hands were taken.Results: Only filters of electronic faucets and water samples after removing filters and one liquid hand soap showed P. aeruginosa (3–7 ¥106 cfu/mL). We have removed the electronic faucets and new elbow-operated faucets were installed. Pulsed-field gel electrophoresis analysisof outbreak-blood culture isolates from two patients and isolates from electronic water faucets/one liquid hand soap indicated the presence of90.7% genetically related subtype, probably from the same clone. Water cultures from new faucets were all clean after installation and after7 months.Conclusion: We suggest that electronic faucets may be considered a potential risk for P. aeruginosa in hospitals, especially in high-risk units.
Key words: electronic faucet; newborn; P. aeruginosa infection.
Outbreaks of Pseudomonas aeruginosa in neonatal intensive careunits (NICUs) can be life threatening, particularly in preterminfants. Specific environmental surfaces such as tap water, sinks,faucets and taps are well-known sources for infection orcontamination.1–3 In a review of prospective studies publishedbetween 1998 and 2005 by Trautmann et al.,4 9.7–68.1% ofrandomly taken water samples on different types of intensivecare units (ICUs) were reported to be positive for P. aeruginosa,and 14.2–50% of infection/colonisation episodes were due to
genotypes found in ICU water. In NICUs, long or artificialfingernails,5 contaminated multi-dose vials,6 water bath forthawing fresh frozen plasma,7 contaminated equipment,8
breastfeeding and contaminated feeding bottles9–11 are reportedrisk factors for antibiotic-resistant P. aeruginosa infections.
Electronic faucets are commonly used in public places such astoilets and restaurants mainly to prevent touching contami-nated taps. They save water and have less flushing effect thanhand-operated ones. So recontamination from the sink may beanother advantage. Due to these advantages, these devices havebeen more frequently installed in hospitals to prevent cross-contamination or recontamination, especially in ICUs. However,several studies reported that electronic faucets may be a sourceof P. aeruginosa and Legionella spp. infections,12,13 and not recom-mended in high-risk units,12,14–16 whereas one study found noP. aeruginosa growth in electronic faucets.17
Here, we report a short-term P. aeruginosa outbreak probablydue to electronic faucets in our NICU.
Correspondence: Dr Hacer Yapicioglu, Cukurova University Faculty ofMedicine, Department of Pediatrics, Division of Neonatology, Adana 01330,Turkey. Fax: +90 322 338 66 10; e-mail: [email protected]
Conflict of Interest: No conflict of interest.
Accepted for publication 02 June 2011.
What is already known on this topic
1 Outbreaks of Pseudomonas aeruginosa in neonatal intensivecare units can be life threatening, particularly in preterm infants.
2 Specific environmental surfaces such as tap water, sinks, faucetsand taps are well-known sources for infection or contamination.
3 There are a few reports about P. aeruginosa contamination inelectronic faucets. However, no outbreak was reported before.
What this paper adds
1 We have shown for the first time that electronic faucets may bean important source for P. aeruginosa outbreak in neonatalintensive care units.
2 Mortality of P. aeruginosa infections is high in premature babies.3 If electronic faucets are in use, vigilance for a Pseudomonas
outbreak is required.
doi:10.1111/j.1440-1754.2011.02248.x
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Journal of Paediatrics and Child Health 48 (2012) 430–434© 2011 The Authors
Journal of Paediatrics and Child Health © 2011 Paediatrics and Child Health Division (Royal Australasian College of Physicians)
430
Subjects and Methods
The NICU is a tertiary centre with 25 beds in a university hospitalwith 1200 beds and cares for patients mostly with medicalproblems, with 12–14 intensive care (level III) beds. There arefour patient rooms and two sinks in each room; chlorhexidine/alcohol hand disinfectants and gloves are available in each room.Active surveillance has been performed by the Hospital InfectionControl Committee (HICC) since 2001 in NICU. In November2009, eight conventional hand-operated faucets in four patientrooms and one in a laboratory in NICU were replaced withelectronically operated faucets in order to prevent hand touch-ing. The faucets work by a non-touch technique with a sensor-operated system without a handle. Doctor rest rooms had hand-operated faucets. After a period of 6 months, in June, we had apatient infected by P. aeruginosa with ventilator-associatedpneumonia (VAP), and in the following days, three otherpatients with bloodstream infection (BSI) were infected. We havecohorted the patients, and HICC investigated the source of out-break in the beginning of July. Environmental cultures includingthose from patient rooms, incubator, ventilators, total parenteralnutrition solutions, disinfection solutions and staff hands weretaken. The unit was closed to new admissions for 4 weeks as far aspossible; however, we had four more patients infected duringinvestigation. Samples were taken from all electronic and hand-operated faucet filters. Additionally, all faucet filters were removedand after flushing water for 5 min, three times in 1 h, 2 mL ofdistilled water was inoculated into brain heart infusion (BHI) brothand incubated overnight. No turbidity of the broth was observedafter overnight incubation, and subculture on blood and Endo agarwas also negative. For identification of P. aeruginosa, samples fromfaucet filters of all patient rooms, doctor rest rooms and the labo-ratory were picked with swaps soaked in BHI broth. Samples wereenriched overnight at 37°C in BHI broth, and then incubated at37°C on blood and Endo agar plates overnight. There weregrowing in all filters and water samples from patient rooms andlaboratory where electronic faucets were in use and growth inliquid soap in a patient room. Growing colonies on Endo agarplates were identified as P. aeruginosa with the BBL Crystal Enteric/Non-fermenter Identification System (Becton Dickinson andCompany, Franklin Lakes, NJ, USA).
Results
P. aeruginosa was identified from one liquid hand soap and fromsamples of water and filters of all electronic faucets in patientrooms and laboratories (Pseudomonas spp. 3–7 ¥ 106 cfu/mL).There was no P. aeruginosa growing in hand-operated water taps.Pseudomonas stutzeri was grown in one of the doctors’ room filter,but not in water. The characteristics of the infected patients areshown in Table 1. The two blood cultures from two patients (8thand 9th patients in Table 2) and cultures from sensor-operatedwater faucets from patient rooms 1, 2, 3/laboratory and liquidsoap were genotyped by pulsed-field gel electrophoresis(PFGE).18 Potential clonal relatedness was determined at a�80% level of similarity, corresponding to maximum six banddifference. Strains that differ by no more than three bands weredetermined probably epidemiologically related.19 PFGE analysisof outbreak-blood culture isolates from the two patients Ta
ble
1C
hara
cter
istic
sof
pat
ient
sw
ithP
seud
omon
asae
rugi
nosa
infe
ctio
ns
Gen
der
Ges
tatio
nal
age
(wee
ks)
Bir
thw
eigh
t(g
)D
iagn
osis
TPN
(day
s)Li
pid
(day
s)A
CV
CV
entil
ator
trea
tmen
t
Typ
eof
Infe
ctio
n
Gro
wth
day
(day
oflif
e)
Pro
gnos
is
M24
640
PM
,RD
S16
16+
++
BSI
3Ex
itus
M24
870
PM
,RD
S9
9+
++
BSI
3Ex
itus
M35
2580
PM
2928
--
+B
SI9
Dis
char
ge
F27
935
PM
3939
-+
+B
SI19
Exitu
s
M41
3100
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ngea
lano
mal
y99
95-
++
VA
P24
Dis
char
ge
M38
3455
Con
geni
tala
nom
aly
1716
-+
+V
AP
8D
isch
arge
M37
2900
Con
geni
tala
nom
aly
2121
++
+B
SI13
Exitu
s
M39
2430
Left
vent
ricu
lar
hyp
opla
sia
2626
--
+B
SI9
Exitu
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M29
1675
Esop
hage
alat
resi
a70
70-
-+
VA
P28
Dis
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M36
1870
PM
,RD
S13
13-
-+
BSI
5Ex
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M30
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23Ex
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2760
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geni
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aly
1615
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tion;
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ory
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H Yapicioglu et al. Infections due to electronic faucets
Journal of Paediatrics and Child Health 48 (2012) 430–434© 2011 The AuthorsJournal of Paediatrics and Child Health © 2011 Paediatrics and Child Health Division (Royal Australasian College of Physicians)
431
indicated 97.3% genetically related subtype (one-band differ-ence); isolates from electronic water faucets in patient room3/laboratory in the unit and liquid soap indicated 100%; andblood cultures and water samples of electronic faucets in patientroom 3/laboratory and liquid soap indicated the presence of90.7% genetically related subtype (five-band difference), prob-ably from the same clone (Fig. 1).19 However, microorganismsfrom patient rooms 1 and 2 were genetically different. Theantibiotic susceptibility of the microorganisms is shown inTable 2. After faucets have been suspected as the source ofinfection, additional control measures included alcoholic rubdisinfection of hands and wearing gloves after hand washing.Tap water cultures from the hospital water tank and otherelectronic faucets in the operating rooms were clean forP. aeruginosa. All electronic faucets in NICU were removed, andelbow-operated new taps were installed in the beginning ofAugust (Fig. 2). Tap water cultures from the new elbow-operated faucets were clean. There were two new cases with
P. aeruginosa infection in August, and then two VAPs in Septem-ber and November. Attack rates and additional control measuresare shown in Figure 2. Attack rates were calculated as infectedpatients/number of patients in the unit that month. Of the 12patients, eight had BSI and four had VAP. Seven of the patientswith BSIs died, two of them were due to P. aeruginosa infection.None of the patients with VAP died. After 7 months, in February2011, three patients had P. aeruginosa BSIs. HICC performed theenvironmental cultures including the tap filters and water fromnew installed faucets; they were all clean. There was P. aerugi-nosa growth in distilled water, and PFGE analysis of bloodculture isolates from the patients and the distilled water indi-cated 100% genetically related subtype.
Discussion
Although there are reports about tap water and P. aeruginosainfections,1,20,21 and about contamination and unacceptable
Table 2 Antibiotic susceptibility of microorganism
Patient no. 1st 2nd 3rd 4th 5th 6th 7th 8th 9th 10th 11th 12th
Month June June June June July July July July Aug Aug Sep Nov
(Infection type) (VAP) (VAP) (BSI) (BSI) (BSI) (BSI) (BSI) (BSI) (BSI) (BSI) (VAP) (VAP)
Amikacin S S R S S S S S S S S R
Gentamicin S S R R S S S S S S R R
Tobramycin S S R S S S S S S S R R
Colistin S S S R S S S S S S S S
Imipenem/cilastatin R R R R R S R R R S S R
Meropenem R R R R R S R R R S S R
Piperacillin R R R R R S R R R S R R
Piperacillin-tazobactam R R R R R S R R R S S R
Cefepime R R R R R S R R R S S R
Ceftazidime R R R R R S R R R S S R
Ciprofloxicillin R R R R R S S R R S S R
Ticarcillin R R R R R R R R R S R R
Levofloksasin R R R R R S S R R S S S
Dice (Opt:1.50%) (Tol 1.5%-1.5%) (H>0.0% S>0.0%) [0.0%-100.0%]
PFGE PFGE
10
0
90
80
97.3
100
90.7
79.4
78.5
75.2
Patient 1 blood culture
Patient 2 blood culture
Patient room 3
Laboratory
Liquid hand soap
Control strain from central laboratory
Patient room 2
Patient room 1
Fig. 1 Pulsed-field gel electrophoresis of the
cultures for Pseudomonas aeruginosa. Ampli-
fied fragment-length polymorphism fingerprints
of patients’ isolates in newborn unit, of isolates
from water of electronic faucets, hand soap and
of isolates from control patient from Central
Laboratory of Hospital. Levels of similarity are
expressed as percentages of similarity.
Infections due to electronic faucets H Yapicioglu et al.
Journal of Paediatrics and Child Health 48 (2012) 430–434© 2011 The Authors
Journal of Paediatrics and Child Health © 2011 Paediatrics and Child Health Division (Royal Australasian College of Physicians)
432
levels of microbial growth in water with electronic faucets,12,14,22
to date, no P. aeruginosa outbreak has been related to electronicfaucets. The present study demonstrated that electronic faucetswere related with P. aeruginosa outbreak in NICU, while therewas no growing in hand-operated faucets; and also, attack ratefell markedly after replacement of the electronic faucets.
Electronic faucets work in a manner to prevent hand touch ofstaff and prevent recontamination. However, the outlet, themagnetic valve and the mixing device were found to be the mostcontaminated parts of these faucets (Fig. 3).12 The reasons forcontamination mentioned in previous studies are: as the faucetssave water, there is not enough water to sufficiently flush andclean the faucet; the faucets have water at a temperature of 35°C,a temperature ideal for P. aeruginosa growth, until released fromthe tap and, also, the magnetic valve in these faucets is made ofrubber, plastic and polyvinylchloride membranes which are suit-able for P. aeruginosa biofilms.12,14,15 It is very difficult to decon-taminate the faucets despite hyperchlorination,15,16 and for thisreason, the faucets had to be removed in other studies.12,16
In our study, the HICC evaluated the central water tank.However, there was no P. aeruginosa growing, and the microbio-logical examinations of water were suitable according to theTurkish drinking water regulations. HICC has also investigatedthe other electronic faucets in other parts of the hospital;however, there was no P. aeruginosa growth. In our unit, afteronly 6 months of installation, we had an outbreak. In Chaberny
et al.’s study,15 98% of water samples from new electronic faucetsin a renovated hospital kitchen showed bacteria counts greaterthan the reference values in 6 months after installation, butalthough they did not investigate prospectively, it was not asso-ciated with an infection or outbreak. The reason we had anoutbreak may be due to immunocompromised patient group innewborn ICUs. The patients in the present study were mostlypremature babies and patients with underlying diseases such as
0,0%
3,6%
1,8%
0,0% 0,0% 0,0% 0,0%
2,3%
11,4%
8,3%
4,3%
3,4%
0,0%
2,4%
0,0%
3,1%
8,1%
0,0%
Oct.09
Nov.09
Dec.09
Jan.10
Feb.10
Mar.10
Apr.10
May.10
June10
July10
Aug.10
Sept.10
Dec.10
Nov.10
Dec.10
Jan.11
Feb.11
Mar.11
Attack rates
b
c
ad
Fig. 2 The attack rate of Pseudomonas aeruginosa and interventions to stop outbreak. (a) Electronic faucets installation, November; (b) P. aeruginosa
outbreak, June; (c) electronic faucets were detected as source of outbreak, additional control measures included alcoholic rub disinfection of hands and
wearing gloves, July; (d) Removal of electronic faucets and installation of elbow-operated ones, in the beginning of August.
Fig. 3 Diagram of an electronic faucet.
H Yapicioglu et al. Infections due to electronic faucets
Journal of Paediatrics and Child Health 48 (2012) 430–434© 2011 The AuthorsJournal of Paediatrics and Child Health © 2011 Paediatrics and Child Health Division (Royal Australasian College of Physicians)
433
congenital heart defects or abnormalities. The first two extremelypremature patients died; probably, the microorganism was resis-tant to imipenem and meropenem. These are two of the mostlyused first-line antibiotics for health care-associated infections inour unit, as we have mostly gram-negative infections.23,24 Thelimitation of this study is that we could not study the genotypingof all the grown microorganisms of the patients. The bloodcultures of the two patients are genetically related with some ofthe environmental cultures; however, cultures from watersamples of electronic faucets in patient rooms 1 and 2 seem to begenetically different. So this outbreak is probably polyclonal.
In conclusion, as the attack rate has markedly decreased afterinstallation of new faucets, this study shows that electronicfaucets may be an important source for P. aeruginosa outbreak inNICUs and should be in mind in case of a P. aeruginosa outbreakin high-risk units in hospitals. If these faucets are in use, vigi-lance for an unusually high or increasing rate of Pseudomonasinfections is required.
Acknowledgements
There is no financial support in this study.
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Infections due to electronic faucets H Yapicioglu et al.
Journal of Paediatrics and Child Health 48 (2012) 430–434© 2011 The Authors
Journal of Paediatrics and Child Health © 2011 Paediatrics and Child Health Division (Royal Australasian College of Physicians)
434
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