Fatal Pseudomonas aeruginosa pneumonia in a previously healthy woman was most likely associated with a contaminated hot tub

Article (PDF Available)inInfection 39(3):265-9 · April 2011with25 Reads
DOI: 10.1007/s15010-011-0096-6 · Source: PubMed
Abstract
Community-acquired pneumonia due to Pseudomonas aeruginosa in previously healthy individuals is a rare disease that is associated with high fatality. On 14 February 2010 a previously healthy 49-year-old woman presented to an emergency room with signs and symptoms of pneumonia, 2 days after returning from a spa holiday in a wellness hotel. Blood cultures and respiratory specimens grew P. aeruginosa. Despite adequate antimicrobial therapy, the patient died of septic multiorgan failure on day nine of hospitalization. On February 26, nine water samples were taken from the hotel facilities used by the patient: In the hot tub sample 37,000 colony-forming units of P. aeruginosa/100 ml were detected. Two of five individual colonies from the primary plate used for this hot tub water sample were found to be genetically closely related to the patient's isolates. Results from PFGE, AFLP and MLST analysis allowed the two lung isolates gained at autopsy and the whirlpool bathtub isolates to be allocated into one cluster. The patient most likely acquired P. aeruginosa from the contaminated water in the hotel's hot tub. The detection of P. aeruginosa in high numbers in a hot tub indicates massive biofilm formation in the bath circulation and severe deficiencies in hygienic maintenance. The increasing popularity of hot tubs in hotels and private homes demands increased awareness about potential health risks associated with deficient hygienic maintenance.

Figures

CASE REPORT
Fatal Pseudomonas aeruginosa pneumonia in a previously healthy
woman was most likely associated with a contaminated hot tub
S. Huhulescu
M. Simon
M. Lubnow
M. Kaase
G. Wewalka
A. T. Pietzka
A. Sto
¨
ger
W. Ruppitsch
F. Allerberger
Received: 28 November 2010 / Accepted: 28 February 2011 / Published online: 1 April 2011
Ó The Author(s) 2011. This article is published with open access at Springerlink.com
Abstract Community-acquired pneumonia due to Pseu-
domonas aeruginosa in previously healthy individuals is a
rare disease that is associated with high fatality. On 14
February 2010 a previously healthy 49-year-old woman
presented to an emergency room with signs and symptoms
of pneumonia, 2 days after returning from a spa holiday in
a wellness hotel. Blood cultures and respiratory specimens
grew P. aeruginosa. Despite adequate antimicrobial ther-
apy, the patient died of septic multiorgan failure on day
nine of hospitalization. On February 26, nine water sam-
ples were taken from the hotel facilities used by the patient:
In the hot tub sample 37,000 colony-forming units of
P. aeruginosa/100 ml were detected. Two of five individ-
ual colonies from the primary plate used for this hot tub
water sample were found to be genetically closely related
to the patients’ isolates. Results from PFGE, AFLP and
MLST analysis allowed the two lung isolates gained at
autopsy and the whirlpool bathtub isolates to be allocated
into one cluster. The patient most likely acquired P. aeru-
ginosa from the contaminated water in the hotel’s hot tub.
The detection of P. aeruginosa in high numbers in a hot tub
indicates massive biofilm formation in the bath circulation
and severe deficiencies in hygienic maintenance. The
increasing popularity of hot tubs in hotels and private homes
demands increased awareness about potential health risks
associated with deficient hygienic maintenance.
Keywords Pseudomonas aeruginosa Pneumonia
Community acquired Whirlpool Hot tub Jacuzzi
PFGE AFLP MLST
Introduction
Pseudomonas aeruginosa is widespread in soil, water and
other moist environments. It is extremely adaptable, has
low nutrient requirements and can live at variable pH and
temperature conditions [1]. It is also an important oppor-
tunistic pathogen, especially in the hospital setting, and the
respiratory tract is the most frequent site of such infections
[1]. The typical patient presenting with nosocomial
P. aeruginosa infection is ventilated mechanically, has
slowly progressive lung infiltrates and has been colonized
with this pathogen for days [1]. However, acute pneumonia
due to P. aeruginosa has also been seen in the community,
for example, among individuals who have inhaled con-
taminated hot tub steam [2].
We report here on a fatal case of community-acquired
P. aeruginosa pneumonia in a previously healthy 49-year-old
German woman following a vacation at a wellness resort
in Austria. Water samples from the whirlpool bathtub (hot
S. Huhulescu G. Wewalka A. T. Pietzka A. Sto
¨
ger
W. Ruppitsch F. Allerberger
Austrian Agency for Health and Food Safety, Vienna, Austria
M. Simon
Institute of Microbiology and Hygiene,
University of Regensburg, Regensburg, Germany
M. Lubnow
Department of Internal Medicine II,
University Hospital of Regensburg, Regensburg, Germany
M. Kaase
Institute of Hygiene and Microbiology, National Reference
Centre for Gram-Negative Pathogens, Bochum, Germany
F. Allerberger (&)
Institute for Medical Microbiology,
Hygiene and Infectious Diseases, Paracelsus Medical University,
Muellner Hauptstrasse 48, 5020 Salzburg, Austria
e-mail: franz.allerberger@ages.at
Infection (2011) 39:265–269
DOI 10.1007/s15010-011-0096-6
tub) in the implicated apartment yielded high numbers of
P. aeruginosa genetically closely related to isolates that
had grown in lung samples obtained post mortem.
Case report
On 14 February 2010 a previously healthy 49-year-old
woman presented to the emergency room of a German
hospital, 2 days after returning from a spa holiday in a
wellness hotel in Austria. She complained of severe chest
pain with productive cough, supposedly without fever or
chills. With the exception of smoking (at least 25 pack-
years), there were no underlying risk factors. Initial phys-
ical examination revealed normal body temperature, blood
pressure 60/40 mmHg, pulse 120/min and a respiratory
frequency of 20/min. Laboratory examinations demon-
strated elevated C-reactive protein (38.1 mg/dl, normal
\0.5 mg/dl) and a white blood cell count of 3.94/nl (nor-
mal 4–11/nl). Antibiotic treatment was initiated with
piperacillin/sulbactam [piperacillin 4 g three times daily
plus sulbactam 1 g twice daily, intravenous (IV)] and
moxifloxacin (400 mg once daily, IV). Blood cultures and
respiratory specimens were taken and grew P. aeruginosa
susceptible to piperacillin, piperacillin/sulbactam, cipro-
floxacin and gentamicin when tested according to Clinical
and Laboratory Standards Institute criteria [3]. PCR tests
for influenza A virus, influenza B virus, cytomegalovirus,
Epstein–Barr virus, herpes simplex virus and adenovirus
were negative. A chest X-ray and computed tomography
scan showed subtotal infiltration of the left lung. Due to
rising partial pressure of carbon dioxide in the blood
(pCO
2
) and respiratory acidosis the patient was transferred
to a university hospital several hours after initial admission
and extra-corporal membrane oxygenation (ECMO) was
initiated. Blood cultures and respiratory specimens again
grew P. aeruginosa. On February 22, day 9 of hospital-
ization, the patient died of septic multiorgan failure. Two
lung specimens gained at autopsy grew P. aeruginosa.
Environmental investigation
The patient fell ill 2 days after returning from a 6-day
vacation at an Austrian wellness resort. According to her
companion, she had repeatedly used the apartment’s hot
tub. On February 26, 1 day after receiving a request issued
by a German court to investigate a possible causative role
of the spa, nine water samples were taken by health officers
from the hotel facilities used by the patient: (1) in the
apartment, from the shower, the sink and the hot tub
(usually with a working water temperature of 35°C); (2) in
the hotel’s wellness area, from a sauna basin, two showers,
a shower in a rest room (toilet area), a small outdoor pond
(created for swimming) and a knee-deep pine bath. In the
hot tub sample (water temperature at the time of sampling:
18°C) 37,000 colony-forming units (CFU) of P. aerugin-
osa/100 ml were detected. Another strain of P. aeruginosa
was isolated at 5 CFU/100 ml from the shower in the
patient’s room. All other samples were negative for P.
aeruginosa.
Typing of isolates
Two P. aeruginosa isolates were available for typing from
the patient. The isolates originated from the two lung
samples taken at autopsy. Six water isolates comprising
five individual colonies from the primary plate used for the
hot tub water sample and one colony from the primary
plate used for the water sample of the shower were arbi-
trarily selected for comparative analysis. Species identity
was confirmed by biochemical testing (API 20 NE; Bio-
Merieux, Marcy-l’Etoile, France) and by use of mass
spectrometry (MALDI-TOF Biotyper; Bruker Daltonics,
Bremen, Germany).
At the German reference centre for Gram-negative
pathogens (Bochum, Germany), the eight isolates were typed
by pulsed-field gel electrophoresis (PFGE), as described by
Johnson et al. [4]. The patient’s two post-mortem lung iso-
lates showed a PFGE band pattern indistinguishable from
each other and were considered genetically indistinguishable
according to the criteria by Tenover et al. [5]. From the six
water isolates, four isolates (three from the hot tub and one
from the shower) yielded PFGE patterns clearly distin-
guishable from those of the patient’s isolates and considered
to be unrelated according to the criteria by Tenover et al. [5]
The two remaining isolates (both from the tub) showed
PFGE patterns highly similar to the lung isolates (Fig. 1).
One water isolate differed from the patient’s isolates by an
additional band explainable by a single insertion; the other
differed by two additional bands, which could be explained
either by a single insertion containing a SpeI restriction site
or by two insertions. Both isolates can be regarded as being
closely related based on the criteria of Tenover et al. [5].
Similar PFGE band patterns were not found among 60 P.
aeruginosa isolates (49 clinical isolates, 11 environmental
isolates) investigated in the laboratory performing the PFGE.
Natural diversity of PFGE patterns
In order to assess the epidemiological relevance of the
minor differences observed among the PFGE patterns of
P. aeruginosa from the two patient isolates and these two
tub isolates, we prospectively collected 78 clinical isolates
266 S. Huhulescu et al.
(from June 20 to July 10, 2010, provided by 11 hospital
laboratories from 5 different provinces) to compare with
the eight case-related isolates (two lung isolates, six water
isolates) and two epidemiologically unrelated water iso-
lates. The clinical isolates originated from wound swabs
(n = 34), tracheal secretions (n = 14), ear swabs (n = 8),
urine (n = 7), blood cultures (n = 4), sputum (n = 4), eye
swabs (n = 2), tongue swab (n = 1), stool specimen
(n = 1), drain (n = 1) and a percutaneous endoscopic
gastrostomy (PEG) tube (n = 1); for one clinical isolate no
specific information was available (n = 1).
The Austrian Agency for Health and Food Safety typed
the 88 isolates by PFGE pattern analysis, as described above,
by amplified fragment length polymorphism (AFLP) anal-
ysis and by multi-locus sequence typing (MLST). Genomic
bacterial DNA (gDNA) for the AFLP and MLST analysis
was extracted with the Quick Extract Bacterial DNA
Extraction kit according to the manufacturer’s instructions
(Epicentre Biotechnologies, Madison, WI). The AFLP
analysis was performed using an AFLP Core Reagent kit
(Life Technologies, Carlsbad, CA) for gDNA restriction,
adaptor ligation and prePCR according to the manufacturer’s
protocol [6]. MLST analysis was performed on all 88 isolates
as described by Mansfeld et al. [7]. The sequences obtained
were submitted to the P. aeruginosa PubMLST database
(http://pubmlst.org/paeruginosa)[8]. Novel alleles and
sequence types (STs) were submitted for allele and ST and
clonal complex (CC) designations.
The 88 P. aeruginosa isolates were attributable to 56
sequence types as determined by MLST, to 80 PFGE types
and to 74 AFLP types. Nine new alleles and 22 new STs,
previously not available in the P. aeruginosa MLST
database, were found [8]. Twelve STs comprised at least
two different isolates. Twenty-two STs were assignable to
ST groups within the MLST database using eBURST v3
(http://eburst.mlst.net) cluster analysis. The remaining 34
STs represented singletons.
The two lung isolates #74 and #75, the two hot tub water
isolates #76 and #78 and an epidemiologically unrelated
clinical isolate derived from tracheal secretions of a patient
from the province Upper Austria (#27) belonged to ST-313
and could clearly be differentiated from the remaining 83
isolates (Fig. 2).
The AFLP pattern analysis of these five isolates revealed
three different patterns (Fig. 2). One band of the epide-
miologically unrelated isolate #27 had a lower molecular
weight than the respective band of the two lung isolates
#74 and #75 and the water isolate #78. The water isolate
#76 lacked this band completely. The AFLP patterns of
these five isolates were clearly different from those of the
remaining 83 isolates, similar to the PFGE patterns being
clearly different from those of the 83 isolates. PFGE pat-
tern analysis revealed three different patterns (Fig. 2). The
epidemiologically unrelated isolate #27 lacked one band
present in the two lung isolates. One band of the water
isolate #76 had a higher molecular weight than that of the
respective band of the two lung isolates. The PFGE pattern
of water isolate #78 was indistinguishable from that of the
epidemiologically unrelated isolate #27. According to the
Fig. 1 Pulsed-field gel electrophoresis patterns of Pseudomonas
aeruginosa: Lanes: 136, 137 lung isolates, 138–143 water isolates.
x The two additional bands (lane 138), o the one additional band (lane
140). MRSA (methicillin-resistant Staphylococcus aureus), PAO1
(Pseudomonas aeruginosa PAO1 strain) Internal controls
Fig. 2 PFGE patterns (left column), amplified fragment length
polymorphism patterns (AFLP, middle column) and multi-locus
sequence typing (right column)ofP. aeruginosa: isolate #27 from
an epidemiologically unrelated patient, lung isolates #74 and #75 and
water isolates #76 and #78. ST Sequence type
Fatal Pseudomonas aeruginosa pneumonia in a previously healthy woman 267
criteria of Tenover et al. [5], the lung isolates and the water
isolates from the tub can therefore to be considered as
genetically closely related and as standing in an epidemi-
ological context.
Discussion
Community-acquired P. aeruginosa infections are rare and
tend to be mild and superficial. Examples include otitis
externa, varicose ulcers, and folliculitis associated with
jacuzzis [9]. There are only a few published reports of
severe P. aeruginosa infections occurring in previously
healthy persons without underlying diseases [2, 1015].
However, community-acquired pneumonia due to P.
aeruginosa in previously healthy individuals is associated
with high fatality (over 30%) [12]. In the English literature
from 1966 to 2000, there are 11 publications on 11 cases of
community-acquired P. aeruginosa pneumonia in previ-
ously healthy persons, with a total of four fatalities [12].
The disease was associated with exposure to contaminated
water aerosols in at least two of the 11 cases published:
Alan et al. [13] reported on a case of community-acquired
P. aeruginosa pneumonia associated with the use of a
home humidifier, and Rose et al. [10] reported on P.
aeruginosa pneumonia occurring following a single
extended (90 min) exposure to contaminated water aero-
sols in a private home whirlpool. In 2003, Crnich et al. [2]
reported on another case of community-acquired hot tub-
associated necrotizing pneumonia in a previously healthy
40-year-old with a smoking history.
The patient described in our report most likely acquired
P. aeruginosa from the contaminated water in the hotel’s
hot tub. PFGE, AFLP and MLST analysis allowed the two
lung isolates and the whirlpool bathtub isolates to be
allocated into one cluster. The fact that the PFGE patterns
of the lung isolates and the water isolates did not show
100% homology must not be misinterpreted as proof of
non-clonality. P. aeruginosa is known to be highly muta-
tional and, therefore, molecular typing methods are prone
to over-discriminate. Smith et al. [16] have shown that
DNA sequence mutations occur frequently during a
patient’s infection. Most of these mutations are single base-
pair changes, which can result in a different restriction
pattern based on PFGE and AFLP analysis [17].
The increasing popularity of hot tubs in hotels and pri-
vate homes demands increased awareness about the
potential health risks associated with deficient hygienic
maintenance. The occurrence of P. aeruginosa pneumonia
in the community should always prompt proper environ-
mental investigations in order to elucidate possible sources
of infection. Using PFGE, a case of P. aeruginosa uro-
sepsis and prostatitis in a previously healthy 38-year-old
was recently linked to contaminated water in the patient’s
hot tub; this underlines the considerable potential of
today’s molecular subtyping methods as a tool to elucidate
sources of infection [18].
The detection of 37,000 CFU of P. aeruginosa in a hot
tub indicates massive biofilm formation in the bath circu-
lation and severe deficiencies in hygienic maintenance. P.
aeruginosa is able to multiply in biofilms that form on the
surfaces of pipes filled with stagnant water, and it can grow
at temperatures up to 42°
C[1, 18]. There are a number of
regulations governing the microbiological quality of water
in hot tubs in commercial premises, such as wellness hotels
or health spas; however, in Austria this has been regulated
by law only since July 2009 [19]. The microbiological
requirements are based on the Austrian standard O
¨
NORM
M 6222-1, which stipulates ‘Requirements for the char-
acteristics of bath water in hot tubs: operations, mainte-
nance and inspection’ [20]. This standard requires that the
hot tub water circuit system be disinfected during or after
each filling to prevent the formation of biofilms. According
to this regulation, there must be no E. coli, P. aeruginosa
and Legionella spp. in a 100 ml sample of water (taken
after 5 min of running idle).
Acknowledgments We gratefully acknowledge the support
received from So
¨
ren Gaterman (Bochum, Germany), Hannes Pohla
(Salzburg, Austria) and Thomas Holzmann (Regensburg, Germany)
in this investigation. We are also indebted to our colleagues who
provided clinical P. aeruginosa isolates for comparison.
Conflict of interest The authors declare that they have no com-
peting interests.
Open Access This article is distributed under the terms of the
Creative Commons Attribution Noncommercial License which per-
mits any noncommercial use, distribution, and reproduction in any
medium, provided the original author(s) and source are credited.
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Fatal Pseudomonas aeruginosa pneumonia in a previously healthy woman 269
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