bs_bs_banner

doi:10.1111/j.1440-1754.2011.02248.x

ORIGINAL ARTICLE

Pseudomonas aeruginosa infections due to electronic faucets in a

neonatal intensive care unit
jpc_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, ventilators, total parenteral nutrition solutions, disinfection solutions, electronic and hand-operated faucet lters/water samples after removing lters
and staff hands were taken.
Results: Only lters of electronic faucets and water samples after removing lters and one liquid hand soap showed P. aeruginosa (37
106 cfu/mL). We have removed the electronic faucets and new elbow-operated faucets were installed. Pulsed-eld gel electrophoresis analysis
of outbreak-blood culture isolates from two patients and isolates from electronic water faucets/one liquid hand soap indicated the presence of
90.7% genetically related subtype, probably from the same clone. Water cultures from new faucets were all clean after installation and after
7 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.

What is already known on this topic

What this paper adds

1 Outbreaks of Pseudomonas aeruginosa in neonatal intensive

care units can be life threatening, particularly in preterm infants.
2 Specic environmental surfaces such as tap water, sinks, faucets
and taps are well-known sources for infection or contamination.
3 There are a few reports about P. aeruginosa contamination in
electronic faucets. However, no outbreak was reported before.

1 We have shown for the rst time that electronic faucets may be
an important source for P. aeruginosa outbreak in neonatal
intensive 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.

Outbreaks of Pseudomonas aeruginosa in neonatal intensive care

units (NICUs) can be life threatening, particularly in preterm
infants. Specific environmental surfaces such as tap water, sinks,
faucets and taps are well-known sources for infection or
contamination.13 In a review of prospective studies published
between 1998 and 2005 by Trautmann et al.,4 9.768.1% of
randomly taken water samples on different types of intensive
care units (ICUs) were reported to be positive for P. aeruginosa,
and 14.250% of infection/colonisation episodes were due to

Correspondence: Dr Hacer Yapicioglu, Cukurova University Faculty of

Medicine, Department of Pediatrics, Division of Neonatology, Adana 01330,
Turkey. Fax: +90 322 338 66 10; e-mail: hyapicioglu@cu.edu.tr
Conict of Interest: No conict of interest.
Accepted for publication 02 June 2011.

430

genotypes found in ICU water. In NICUs, long or artificial

fingernails,5 contaminated multi-dose vials,6 water bath for
thawing fresh frozen plasma,7 contaminated equipment,8
breastfeeding and contaminated feeding bottles911 are reported
risk factors for antibiotic-resistant P. aeruginosa infections.
Electronic faucets are commonly used in public places such as
toilets and restaurants mainly to prevent touching contaminated taps. They save water and have less flushing effect than
hand-operated ones. So recontamination from the sink may be
another advantage. Due to these advantages, these devices have
been more frequently installed in hospitals to prevent crosscontamination or recontamination, especially in ICUs. However,
several studies reported that electronic faucets may be a source
of P. aeruginosa and Legionella spp. infections,12,13 and not recommended in high-risk units,12,1416 whereas one study found no
P. aeruginosa growth in electronic faucets.17
Here, we report a short-term P. aeruginosa outbreak probably
due to electronic faucets in our NICU.

Journal of Paediatrics and Child Health 48 (2012) 430434

2011 The Authors
Journal of Paediatrics and Child Health 2011 Paediatrics and Child Health Division (Royal Australasian College of Physicians)

3
3
9
19
24
8
13
9
28
5
23
40
BSI
BSI
BSI
BSI
VAP
VAP
BSI
BSI
VAP
BSI
BSI
VAP
+
+
+
+
+
+
-

24
24
35
27
41
38
37
39
29
36
30
37
M
M
M
F
M
M
M
M
M
M
M
M

640
870
2580
935
3100
3455
2900
2430
1675
1870
1580
2760

PM, RDS
PM, RDS
PM
PM
Laryngeal anomaly
Congenital anomaly
Congenital anomaly
Left ventricular hypoplasia
Esophageal atresia
PM, RDS
PM, RDS
Congenital anomaly

16
9
29
39
99
17
21
26
70
13
40
16

16
9
28
39
95
16
21
26
70
13
40
15

+
+
+
-

+
+
+
+
+
+
+
+
+
+
+
+

Growth day
(day of life)
Type of
Infection
Ventilator
treatment
VC
AC
Lipid (days)
TPN (days)
Diagnosis
Birthweight (g)
Gestational
age (weeks)

P. aeruginosa was identified from one liquid hand soap and from
samples of water and filters of all electronic faucets in patient
rooms and laboratories (Pseudomonas spp. 37 106 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 are
shown in Table 1. The two blood cultures from two patients (8th
and 9th patients in Table 2) and cultures from sensor-operated
water faucets from patient rooms 1, 2, 3/laboratory and liquid
soap were genotyped by pulsed-field gel electrophoresis
(PFGE).18 Potential clonal relatedness was determined at a
80% level of similarity, corresponding to maximum six band
difference. Strains that differ by no more than three bands were
determined probably epidemiologically related.19 PFGE analysis
of outbreak-blood culture isolates from the two patients

Gender

Results

Table 1 Characteristics of patients with Pseudomonas aeruginosa infections

The NICU is a tertiary centre with 25 beds in a university hospital

with 1200 beds and cares for patients mostly with medical
problems, with 1214 intensive care (level III) beds. There are
four 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 Infection
Control Committee (HICC) since 2001 in NICU. In November
2009, eight conventional hand-operated faucets in four patient
rooms and one in a laboratory in NICU were replaced with
electronically operated faucets in order to prevent hand touching. The faucets work by a non-touch technique with a sensoroperated system without a handle. Doctor rest rooms had handoperated faucets. After a period of 6 months, in June, we had a
patient infected by P. aeruginosa with ventilator-associated
pneumonia (VAP), and in the following days, three other
patients with bloodstream infection (BSI) were infected. We have
cohorted the patients, and HICC investigated the source of outbreak in the beginning of July. Environmental cultures including
those from patient rooms, incubator, ventilators, total parenteral
nutrition solutions, disinfection solutions and staff hands were
taken. The unit was closed to new admissions for 4 weeks as far as
possible; however, we had four more patients infected during
investigation. Samples were taken from all electronic and handoperated faucet filters. Additionally, all faucet filters were removed
and after flushing water for 5 min, three times in 1 h, 2 mL of
distilled water was inoculated into brain heart infusion (BHI) broth
and incubated overnight. No turbidity of the broth was observed
after overnight incubation, and subculture on blood and Endo agar
was also negative. For identification of P. aeruginosa, samples from
faucet filters of all patient rooms, doctor rest rooms and the laboratory were picked with swaps soaked in BHI broth. Samples were
enriched overnight at 37C in BHI broth, and then incubated at
37C on blood and Endo agar plates overnight. There were
growing in all filters and water samples from patient rooms and
laboratory where electronic faucets were in use and growth in
liquid soap in a patient room. Growing colonies on Endo agar
plates were identified as P. aeruginosa with the BBL Crystal Enteric/
Non-fermenter Identification System (Becton Dickinson and
Company, Franklin Lakes, NJ, USA).

Prognosis

Subjects and Methods

Journal of Paediatrics and Child Health 48 (2012) 430434

2011 The Authors
Journal of Paediatrics and Child Health 2011 Paediatrics and Child Health Division (Royal Australasian College of Physicians)

AC, arterial catheterisation; BSI, bloodstream infection; PM, prematurity; RDS, respiratory distress syndrome; TPN, total parenteral nutrition; VAP, ventilator associated infection; VC, umbilical/central venous
catheterisation.

Infections due to electronic faucets

Exitus
Exitus
Discharge
Exitus
Discharge
Discharge
Exitus
Exitus
Discharge
Exitus
Exitus
Exitus

H Yapicioglu et al.

431

Infections due to electronic faucets

H Yapicioglu et al.

Table 2 Antibiotic susceptibility of microorganism

Patient no.
Month
(Infection type)

1st
June
(VAP)

2nd
June
(VAP)

3rd
June
(BSI)

4th
June
(BSI)

5th
July
(BSI)

6th
July
(BSI)

7th
July
(BSI)

8th
July
(BSI)

9th
Aug
(BSI)

10th
Aug
(BSI)

11th
Sep
(VAP)

12th
Nov
(VAP)

Amikacin
Gentamicin
Tobramycin
Colistin
Imipenem/cilastatin
Meropenem
Piperacillin
Piperacillin-tazobactam
Cefepime
Ceftazidime
Ciprooxicillin
Ticarcillin
Levooksasin

S
S
S
S
R
R
R
R
R
R
R
R
R

S
S
S
S
R
R
R
R
R
R
R
R
R

R
R
R
S
R
R
R
R
R
R
R
R
R

S
R
S
R
R
R
R
R
R
R
R
R
R

S
S
S
S
R
R
R
R
R
R
R
R
R

S
S
S
S
S
S
S
S
S
S
S
R
S

S
S
S
S
R
R
R
R
R
R
S
R
S

S
S
S
S
R
R
R
R
R
R
R
R
R

S
S
S
S
R
R
R
R
R
R
R
R
R

S
S
S
S
S
S
S
S
S
S
S
S
S

S
R
R
S
S
S
R
S
S
S
S
R
S

R
R
R
S
R
R
R
R
R
R
R
R
S

Dice (Opt:1.50%) (Tol 1.5%-1.5%) (H>0.0% S>0.0%) [0.0%-100.0%]

100

PFGE

90

80

PFGE

97.3
90.7

79.4
78.5

100

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

75.2

indicated 97.3% genetically related subtype (one-band difference); isolates from electronic water faucets in patient room
3/laboratory in the unit and liquid soap indicated 100%; and
blood cultures and water samples of electronic faucets in patient
room 3/laboratory and liquid soap indicated the presence of
90.7% genetically related subtype (five-band difference), probably from the same clone (Fig. 1).19 However, microorganisms
from patient rooms 1 and 2 were genetically different. The
antibiotic susceptibility of the microorganisms is shown in
Table 2. After faucets have been suspected as the source of
infection, additional control measures included alcoholic rub
disinfection of hands and wearing gloves after hand washing.
Tap water cultures from the hospital water tank and other
electronic faucets in the operating rooms were clean for
P. aeruginosa. All electronic faucets in NICU were removed, and
elbow-operated new taps were installed in the beginning of
August (Fig. 2). Tap water cultures from the new elbowoperated faucets were clean. There were two new cases with
432

Fig. 1 Pulsed-eld gel electrophoresis of the

cultures for Pseudomonas aeruginosa. Amplied fragment-length polymorphism ngerprints
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.

P. aeruginosa infection in August, and then two VAPs in September and November. Attack rates and additional control measures
are shown in Figure 2. Attack rates were calculated as infected
patients/number of patients in the unit that month. Of the 12
patients, eight had BSI and four had VAP. Seven of the patients
with BSIs died, two of them were due to P. aeruginosa infection.
None of the patients with VAP died. After 7 months, in February
2011, three patients had P. aeruginosa BSIs. HICC performed the
environmental cultures including the tap filters and water from
new installed faucets; they were all clean. There was P. aeruginosa growth in distilled water, and PFGE analysis of blood
culture isolates from the patients and the distilled water indicated 100% genetically related subtype.

Discussion
Although there are reports about tap water and P. aeruginosa
infections,1,20,21 and about contamination and unacceptable

Journal of Paediatrics and Child Health 48 (2012) 430434

2011 The Authors
Journal of Paediatrics and Child Health 2011 Paediatrics and Child Health Division (Royal Australasian College of Physicians)

H Yapicioglu et al.

Infections due to electronic faucets

Attack rates

b
11,4%

c
8,3%

8,1%

4,3%
3,6%

3,4%
1,8%

0,0%

3,1%
2,4%

2,3%

0,0% 0,0% 0,0%

0,0%

0,0%

0,0%

0,0%

1
.1
ar

1
b.
Fe

11
n.
Ja

0
.1

ec
D

0
.1

0
.1

ov
N

ec
D

.1
pt
Se

0
.1
ar

10
g.
Au
10
ly
Ju
10
ne
Ju
0
.1
ay
M
0
r.1
Ap

1
b.
Fe

10
n.
Ja

9
.0

9
.0

ec
D

9
.0
ct

ov
N

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.

levels of microbial growth in water with electronic faucets,12,14,22

to date, no P. aeruginosa outbreak has been related to electronic
faucets. The present study demonstrated that electronic faucets
were related with P. aeruginosa outbreak in NICU, while there
was no growing in hand-operated faucets; and also, attack rate
fell markedly after replacement of the electronic faucets.
Electronic faucets work in a manner to prevent hand touch of
staff and prevent recontamination. However, the outlet, the
magnetic valve and the mixing device were found to be the most
contaminated parts of these faucets (Fig. 3).12 The reasons for
contamination mentioned in previous studies are: as the faucets
save water, there is not enough water to sufficiently flush and
clean the faucet; the faucets have water at a temperature of 35C,
a temperature ideal for P. aeruginosa growth, until released from
the tap and, also, the magnetic valve in these faucets is made of
rubber, plastic and polyvinylchloride membranes which are suitable for P. aeruginosa biofilms.12,14,15 It is very difficult to decontaminate the faucets despite hyperchlorination,15,16 and for this
reason, 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 microbiological examinations of water were suitable according to the
Turkish drinking water regulations. HICC has also investigated
the other electronic faucets in other parts of the hospital;
however, there was no P. aeruginosa growth. In our unit, after
only 6 months of installation, we had an outbreak. In Chaberny

Fig. 3

Diagram of an electronic faucet.

et al.s study,15 98% of water samples from new electronic faucets

in a renovated hospital kitchen showed bacteria counts greater
than the reference values in 6 months after installation, but
although they did not investigate prospectively, it was not associated with an infection or outbreak. The reason we had an
outbreak may be due to immunocompromised patient group in
newborn ICUs. The patients in the present study were mostly
premature babies and patients with underlying diseases such as

Journal of Paediatrics and Child Health 48 (2012) 430434

2011 The Authors
Journal of Paediatrics and Child Health 2011 Paediatrics and Child Health Division (Royal Australasian College of Physicians)

433

Infections due to electronic faucets

H Yapicioglu et al.

congenital heart defects or abnormalities. The first two extremely

premature patients died; probably, the microorganism was resistant to imipenem and meropenem. These are two of the mostly
used first-line antibiotics for health care-associated infections in
our unit, as we have mostly gram-negative infections.23,24 The
limitation of this study is that we could not study the genotyping
of all the grown microorganisms of the patients. The blood
cultures of the two patients are genetically related with some of
the environmental cultures; however, cultures from water
samples of electronic faucets in patient rooms 1 and 2 seem to be
genetically different. So this outbreak is probably polyclonal.
In conclusion, as the attack rate has markedly decreased after
installation of new faucets, this study shows that electronic
faucets may be an important source for P. aeruginosa outbreak in
NICUs and should be in mind in case of a P. aeruginosa outbreak
in high-risk units in hospitals. If these faucets are in use, vigilance for an unusually high or increasing rate of Pseudomonas
infections is required.

Acknowledgements
There is no financial support in this study.

References
1 Bert F, Maubec E, Bruneau B et al. Multi-resistant Pseudomonas
aeruginosa outbreak associated with contaminated tap water in a
neurosurgery intensive care unit. J. Hosp. Infect. 1998; 39: 5362.
2 Berthelot P, Grattard F, Mahul P et al. Prospective study of
nosocomial colonization and infection due to Pseudomonas
aeruginosa in mechanically ventilated patients. Intensive Care Med.
2001; 27: 50312.
3 Lawrence FM. Contribution of tap water and environmental surfaces
to nosocomial transmission of antibiotic-resistant Pseudomonas
aeruginosa. Infect. Control Hosp. Epidemiol. 2004; 25: 3425.
4 Trautmann M, Michalsky T, Wiedeck H, Radosavljevic V, Ruhnke M.
Tap water colonization with Pseudomonas aeruginosa in a surgical
intensive care unit (ICU) and relation to Pseudomonas infections of
ICU patients. Infect. Control Hosp. Epidemiol. 2001; 22: 4952.
5 Moolenaar RL, Crutcher JM, San Joaquin VH et al. A prolonged
outbreak of Pseudomonas aeruginosa in a neonatal intensive care
unit: did staff ngernails play a role in disease transmission? Infect.
Control Hosp. Epidemiol. 2000; 21: 805.
6 Archibald LK, Ramos A, Arduino MJ et al. Enterobacter cloacae and
Pseudomonas aeruginosa polymicrobial bloodstream infections
traced to extrinsic contamination of a dextrose multidose vial. J.
Pediatr. 1998; 133: 6404.
7 Muyldermans G, de Smet F, Pierard D et al. Neonatal infections due to
Pseudomonas aeruginosa associated with a water-bath used to thaw
fresh frozen plasma. J. Hosp. Infect. 1998; 39: 30914.
8 Garland SM, Mackay J, Tabrizi S, Jacobs S. Pseudomonas aeruginosa
outbreak associated with a contaminated blood-gas analyser in a
neonatal intensive care unit. Hosp. Infect. 1996; 33: 14551.

434

9 Crivaro V, Di Popolo A, Caprio A et al. Pseudomonas aeruginosa in a

neonatal intensive care unit: molecular epidemiology and infection
control measures. BMC Infect. Dis. 2009; 9: 70.
10 Sanchez-Carrillo C, Padilla B, Marrin M et al. Contaminated feeding
bottles: the source of an outbreak of Pseudomonas aeruginosa
infections in a neonatal intensive care unit. Am. J. Infect. Control
2009; 37: 1504.
11 Mammina C, Di Carlo P, Cipolla D et al. Nosocomial colonization due
to imipenem-resistant Pseudomonas aeruginosa epidemiology linked
to breast milk feeding in a neonatal intensive care unit. Acta
Pharmacol. Sin. 2008; 29: 148692.
12 Halabi M, Wiesholzer-Pittl M, Schberl J, Mittermayer H. Non-touch
ttings in hospitals: a possible source of Pseudomonas aeruginosa
and Legionella spp. J. Hosp. Infect. 2001; 49: 11721.
13 Leprat R, Denizot V, Bertrand X, Talon D. Non-touch ttings in
hospitals: a possible source of Pseudomonas aeruginosa and
Legionella spp. J. Hosp. Infect. 2003; 53: 77.
14 Hargreaves J, Shireley MS, Hansen S et al. Bacterial contamination
associated with electronic faucets: a new risk for healthcare facilities.
Infect. Control Hosp. Epidemiol. 2001; 22: 2025.
15 Chaberny IF, Gastmeier P. Should electronic faucets be recommended
in hospitals? Infect. Control Hosp. Epidemiol. 2004; 25: 9971000.
16 Merrer J, Girou E, Ducellier D et al. Should electronic faucets be used
in intensive care and hematology units? Intensive Care Med. 2005; 31:
17158.
17 Assadian O, El-Madani N, Seper E et al. Sensor-operated faucets: a
possible source of nosocomial infection? Infect. Control Hosp.
Epidemiol. 2002; 23: 446.
18 Tenover FC, Arbeit RD, Goering RV et al. Interpreting chromosomal
DNA restriction patterns produced by pulsed-eld electrophoresis:
criteria for bacterial strain typing. J. Clin. Microbiol. 1995; 33:
22339.
19 Speijer H, Svaelkoul PHM, Bonten MJ, Stobberingh EE, Tjhie JHT.
Application of different genotyping methods for Pseudomonas
aeruginosa in a setting of endemicity in an intensive care unit. J. Clin.
Microbiol. 1999; 37: 365461.
20 Reuter S, Sigge A, Wiedeck H, Trautmann M. Analysis of transmission
pathways of Pseudomonas aeruginosa between patients and tap
water outlets. Crit. Care Med. 2002; 30: 22228.
21 Grundmann H, Kropec A, Hartung D, Berner R, Daschner F.
Pseudomonas aeruginosa in a neonatal intensive care unit: reservoirs
and ecology of the nosocomial pathogen. J. Infect. Dis. 1993; 168:
9437.
22 van der Mee-Marquet N, Bloc D, Briand L, Besnier JM, Quentin R.
Non-touch ttings in hospitals: a procedure to eradicate
Pseudomonas aeruginosa contamination. J. Hosp. Infect. 2005; 60:
2359.
23 Yapicioglu H, Satar M, Ozcan K et al. A 6-year prospective surveillance
of healthcare-associated infections in a neonatal intensive care unit
from southern part of Turkey. J. Paediatr. Child Health 2010; 46:
33742.
24 Yapicioglu H, Ozcan K, Sertdemir Y et al. Healthcare-associated
infections in a neonatal intensive care unit in Turkey in 2008:
incidence and risk factors, a prospective study. J. Trop. Pediatr. 2011;
57: 15764.

Journal of Paediatrics and Child Health 48 (2012) 430434

2011 The Authors
Journal of Paediatrics and Child Health 2011 Paediatrics and Child Health Division (Royal Australasian College of Physicians)

Copyright of Journal of Paediatrics & Child Health is the property of Wiley-Blackwell and its content may not
be copied or emailed to multiple sites or posted to a listserv without the copyright holder's express written
permission. However, users may print, download, or email articles for individual use.