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CLINICAL OBSERVATIONS, INTERVENTIONS, AND THERAPEUTIC TRIALS
Pathogenic molds (including Aspergillus species) in hospital water distribution
systems: a 3-year prospective study and clinical implications for patients
with hematologic malignancies

Elias J. Anaissie, Shawna L. Stratton, M. Cecilia Dignani, Choon-kee Lee, Richard C. Summerbell, John H. Rex, Thomas P. Monson, and Thomas J. Walsh

The incidence of mold infections in patients with hematologic malignancies continues to increase despite the widespread use of air filtration systems, suggesting the presence of other hospital sources for these molds. Water sources are known to harbor pathogenic molds. We examined samples
from water, water surfaces, air, and other environment sources from a bone marrow transplantation unit with optimal air precautions. Molds (Aspergillus species, others) were recovered in 70% of 398 water samples, in 22% of 1311 swabs from plumbing structures and environmental surfaces, and in 83% of 274 indoor air samples. Microscopic examination of the water plumbing lines revealed hyphal forms compatible with molds. Four findings suggest that indoor airborne molds were aerosolized from the water: (1) higher mean airborne concentrations of molds in bathrooms (16.1 colony forming units [CFU]/m3) than in patient rooms (7 CFU/m3) and hallways (8.6 CFU/m3; P .00005); (2) a strong type and rank correlation between molds isolated from hospital water and those recovered from indoor hospital; (3) lack of seasonal correlation between the airborne mold concentration in outdoor and indoor air; and (4) molecular relatedness between a clinical strain and a water-related strain (previously reported). Hospital water distribution systems may serve as a potential indoor reservoir of Aspergillus and other molds leading to aerosolization of fungal spores and potential exposure for patients. (Blood. 2003;101:2542-2546) © 2003 by The American Society of Hematology

Introduction
Nosocomial opportunistic mold infections can be life-threatening in immunocompromised patients, particularly those with hematologic malignancies. These molds are thought to arise from contaminated outdoor air that infiltrates hospital ventilation systems. 1,2

Prevention of these infections is critical and has relied on air handling systems such as high-efficiency particulate air (HEPA) filters and laminar airflow (LAF).However, the incidence of mold infections continues to rise despite the widespread use of these air filtration systems, 3 suggesting that other
hospital sources for molds may exist. We have previously shown that Fusarium species colonize the water system of a hospital and causes
nosocomial fusariosis. 4 Water systems worldwide have also been shown to be colonized with pathogenic molds. 5-7

This 3-year prospective surveillance study of a hospital caring for immunocompromised patients demonstrates that opportunistic molds may colonize hospital water distribution systems and thus lead to spore aerosolization in patient care
areas and patient exposure.

Materials and methods
The hospital
The hospital is located in Little Rock, AR, and has 2 bone marrow
transplantation (BMT) units. One unit (A) is housed in a newly constructed
patient care tower (built in 1997), whereas the second unit (B) is in the old
hospital building (built in 1955). Both units are equipped with central
HEPA filtration. Unit A also has 3 LAF rooms. All HEPA and LAF filters are
monitored and maintained per industry standards.
The hospital water is supplied by the Little Rock Municipal Water
Works and meets water industry standards.
8
The municipal water enters the
hospital from 2 separate substations. One serves the new patient care tower
(unit A), and the other serves the old hospital (unit B). After entry into the
new building, cold water is pumped immediately to all patient wards. Cold
water is also distributed to 2 instantaneous water heaters and then sent to all
floors. After entry into the old hospital building, cold water is pumped to 2
large water storage tanks housed on the hospital roof and then gravity-fed to
unit B. Cold water is also sent to 4 large heating tanks and pumped to all
floors of the old building.
Environmental sampling
Environmental sampling was performed prospectively during a 3-year
period (1997-2000). Samples were obtained according to room availability.
A total of 416 water samples (1 L each) was collected from municipal
mains, cold- and hot-water storage tanks, and showers and sinks in patient
rooms. All water samples were collected in sterile polystyrene bottles
containing 0.8 mL 3% sodium thiosulfate and passed through sterile
0.45- m filters (Millipore, Bedford, MA) using a filtration apparatus
(Millipore). Using sterile forceps, the filters were placed directly on
Sabouraud dextrose agar plates.
From the Myeloma Institute for Research and Treatment, University of
Arkansas for Medical Sciences, Little Rock; Centraalbureau voor
Schimmelcultures, Baarn, The Netherlands; Center for Infectious Diseases,
University of Texas Medical School, Houston; John L. McClellan Memorial
Veterans Hospital and University of Arkansas for Medical Sciences, Little Rock;
and Immunocompromised Host Section, National Cancer Institute, National
Institutes of Health, Bethesda, MD.
Submitted May 2, 2002; accepted October 5, 2002. Prepublished online as Blood
First Edition Paper, December 5, 2002; DOI 10.1182/blood-2002-02-0530.
This work was presented in part at the 42nd Annual Meeting of the American
Society of Hematology, San Francisco, CA, December 1-5, 2000.
Reprints: Elias J. Anaissie, Professor of Medicine, Clinical Director, Myeloma and
Transplantation Research Center, Arkansas Cancer Research Center, University of
Arkansas for Medical Sciences 4301 West Markham, Mail Slot 776, Little Rock, AR
72205; e-mail: elias114@aol.com or anaissieeliasj@exchange.uams.edu.
The publication costs of this article were defrayed in part by page charge
payment. Therefore, and solely to indicate this fact, this article is hereby
marked ‘‘advertisement’’ in accordance with 18 U.S.C. section 1734.
© 2003 by The American Society of Hematology
2542 BLOOD, 1 APRIL 2003 VOLUME 101, NUMBER 7A total of 1311 swab cultures from the water distribution system and
environmental surfaces was obtained using sterile Culturette swabs (Becton
Dickinson, Franklin Lakes, NJ). Sites that were sampled included the inner
walls of storage tanks and plumbing lines of shower heads and sinks, sink
and shower drains, surfaces of sinks and showers, and internal and external
components of disassembled shower heads and faucet aerators. Other
surfaces that were swabbed included door and windowsills, floors, walls,
HEPA filter surfaces, stethoscope pads, thermometers, curtains, light
fixtures, and toilet seats and bowls. Plumbing lines and drains were
swabbed by ringing the inner surface of the line once. Flat surfaces were
swabbed over an area of approximately 25 cm2
.
A total of 283 air samples was collected using a 6-stage Andersen
Bioaerosol Sampler (Andersen Instruments, Atlanta, GA) as previously
described.
9
Air samples were recovered from outdoor air; patient shower
facilities, bathrooms, and rooms; and adjoining hallways of HEPA-filtered
and LAF rooms.
All samples (water, swabs, and air) were placed on Sabouraud dextrose
agar with chloramphenicol and gentamicin, incubated at 30°C, and checked
daily for growth for at least 28 days. All fungi were identified according to
established methods.
10
Colony counts were enumerated as colony-forming
units per liter (CFU/L) for water and CFU/m3
for air.
9
Ten swabs of plumbing structures and lines were mounted on slides and
stained with lactophenol cotton blue. The slides were then examined by
gross microscopy. The free chlorine levels of municipal, cold-water tank,
and cold end-use product at patient taps were tested using test strips
(Daigger, Lincolnshire, IL).
Statistical analysis
The number of positive samples from each source was compared by 2 2
table analysis, with 2
statistics or 2-tailed Fisher exact test depending on
the number of cases. The Mann-Whitney U test was used for 2-group
comparison between independent concentrations of molds from each
source. For comparison among more than 2 groups, the Kruskal-Wallis
analysis of variance test was used.

Results: Water samples
Molds were recovered from the municipal water, hospital water storage tanks, and hospital water from patient care areas (total of 416 water samples; Table 1). The mean levels of free chlorine in
municipal water, cold-water storage tanks, and cold tap water were
within standard guidelines at 0.2, 0.1 to 0.2, and 0.05 ppm,
respectively (data not shown).
A total of 109 water samples yielded Aspergillus species. The
species of Aspergillus found were all recognized opportunistic
pathogens, and included A niger (77%), A fumigatus (11%), A
terreus (9%), and A flavus (3%). All the Paecilomyces species
found in 44 water samples were P lilacinus. Three of 14 Fusarium
species recovered from water samples were identified to species
level. All 3 were F solani (known pathogens). The mean concentration SD of molds was 9-fold higher in the water tanks than in the
municipal water: mean 11.4 14.0 versus. 1.3 1.7 CFU/L,
respectively (P .01). With the exception of Chaetomium species,
all molds recovered from municipal water were also present in the
water tank. Penicillium species and Aspergillus species were the 2
most common molds recovered from municipal water and from
hospital water. Penicillium species were present in 33%, 42%, and
43% of the samples of municipal water, water storage tanks, and
water from patient care areas, respectively, whereas Aspergillus
species were recovered in 33%, 55%, and 21%, respectively, of
water samples obtained from these same sites.
Samples of the first liter of water from taps yielded a higher rate
of molds (190 of 250, 70%, mean 5.2 CFU/L) than sampling the
second liter (58 of 108, 54%, mean 4.4 CFU/L; P .001).
Microscopic examination of lactophenol cotton blue stains of
swabs taken from internal plumbing lines revealed hyphal elements
compatible with molds (data not shown).

Surface swabs
Molds were recovered on the interior surfaces of water lines, sink
drains, and sink plumbing lines, shower drains, shower head
surfaces, shower head plumbing lines, and toilet bowls (total of
1311 swabs; Table 2). A total of 58 surface swab samples yielded
Aspergillus species including A niger (50%), A fumigatus (19%), A
terreus (14%), A flavus (9%), A nidulans (7%), and A sydowi (1%).
All Paecilomyces species recovered from swab samples were P
lilacinus. Twelve of 37 Fusarium species isolated from 34 swab
samples could be identified to species level. Eight (67%) were F
solani and 4 (33%) were F oxysporum. Cultures of doors, furniture,
and personal objects did not yield molds. All molds that were
identified are known to cause infections in patients with cancer.
Environmental objects (HEPA filter surfaces, walls, floors, and
windowsills) harbored molds less frequently than did hospital
water samples (38 of 174, 32% versus 248 of 358, 67%, respectively; P .001).
Molds were more frequently recovered from the plumbing and
the environmental samples of the old building (149 of 436, 34%
and 89 of 444, 20%, respectively) than those from the new building
(29 of 139, 20% and 43 of 328, 13%, respectively; P .002 and
.012, respectively).

Table 1. Detection of molds in hospital water using water-filtration
sampling methods
Source of water
Total positive
sites/total
tested sites (%)
Molds
recovered*
Positive
sites by
mold
Mean (range)
concentration,
CFU/L†
Municipal water 12/18 (67) Penicillium 6 7.4 (1-20)
Aspergillus 6 1.9 (1-4)
Chaetomium 2 1 (1-1)
Chrysonilia 2 1 (1-1)
Water tanks 33/40 (82) Aspergillus 30 5.2 (1-24)
Penicillium 17 7.1 (1-20)
Alternaria 10 2.7 (1-10)
Trichoderma 8 2.2 (1-5)
Fusarium 8 2.6 (1-9)
Paecilomyces 7 9.9 (1-30)
Mucor 4 1.8 (1-4)
Acremonium 4 2.3 (1-5)
Chrysonilia 3 2.7 (1-4)
Sinks 104/162 (64) Penicillium 71 5.5 (1-20)
Aspergillus 30 2.3 (1-20)
Showers 144/196 (73) Penicillium 86 7.4 (1-20)
Aspergillus 46 2.1 (1-20)
Paecilomyces 27 10.3 (1-23)
Aspergillus species included A niger (77%), A fumigatus (11%), A terreus (9%),
and A flavus (3%). All the Paecilomyces species were P lilacinus. Three of 14
Fusarium species could be identified; all 3 were F solani.
*Molds shown are those that accounted for 10% of positive water samples.
Other molds recovered include Acremonium, Alternaria, Bipolaris, Chrysonilia,
Cladosporium, Chrysosporium, Curvularia, Epicoccum, Mucor, Nigrospora, and
Ulocladium species.
†Represents the mean concentration of the positive cultures from the specified
site.
BLOOD, 1 APRIL 2003 VOLUME 101, NUMBER 7 MOLDS IN HOSPITAL WATER SYSTEM 2543Air samples
A total of 137 indoor air samples yielded Aspergillus species
including A niger (66%), A fumigatus (17%), A nidulans (7%), A
terreus (5%), A flavus (3%), A versicolor (1.5%), and A clavatus
(0.7%). The great majority of the Paecilomyces species recovered
from 42 indoor air samples were P lilacinus (98%) followed by P
variotti (2%). Ten of 12 Fusarium species recovered from indoor
air samples could be identified to species level. All 10 were F
solani. Indoor air samples (n 274) from bathrooms (n 142;
mean, 16.1; SEM, 1.5), rooms (n 82; mean, 7; SEM, 1.1), and
hallways (n 50; mean, 8.6; SEM, 2.3) yielded significantly lower
concentrations of molds than outdoor samples (n 9; mean 123;
SEM, 26.2 CFU/m3
; P .001), indicating that the air precautions on these units (sealed windows, HEPA filtration, others) were
adequate. The highest mean concentrations of molds in outdoor air
were noted during the summer (n 9 total; 173 CFU/m3
) and fall
(168 CFU/m3
) and the lowest during winter (46 CFU/m3
). By
contrast the highest concentration of molds in indoor samples was
seen during fall (21 CFU/m3
) and the lowest during spring (7.1
CFU/m3
). A significantly higher mean concentration of airborne
molds was present in the bathroom (16.1 CFU m3
) than in rooms (7
CFU/m3
) or hallways (8.6 CFU/m3
; P 0.00004; Figure 1).
Rank order distribution of molds in hospital water
and air samples
The most common molds recovered from hospital water were also
the most common ones recovered from air samples. In addition, the
distribution of molds by genera and species was comparable in
water samples and the bioaerosols from bathrooms, rooms, and
hallways (Figure 2).
Discussion
The results of this 3-year prospective surveillance study that was
conducted in a hospital with adequate air filtration precautions and
water chlorination show that (1) Aspergillus species and other
pathogenic molds inhabit the hospital water distribution system; (2)
the same genera and species of molds are recovered from municipal
water and hospital water structures; (3) these molds become part of
the hospital water system biofilm; (4) a concentration differential of
airborne molds exists between areas of water usage such as
bathrooms (highest) and other areas such as patient rooms and
hallways (lowest); (5) a strong correlation exists between the type
and rank orders of molds isolated from hospital water and those
Figure 1. Indoor airborne concentrations of molds by site. A significantly higher
concentration of airborne molds was observed in bathrooms (areas of major water
use) compared with patient rooms and hallways.
Figure 2. Frequency and distribution of pathogenic molds in hospital water and
in air of patients’ rooms, bathrooms, and BMT ward hallways. A similar rank order
distribution of molds was observed in water and air at different sites. A significantly
higher rate of recovery of airborne molds was noted in bathrooms. Only pathogenic
molds were included in this figure. Hospital water includes water samples from
storage tanks and taps of patient care areas. Other molds recovered from water and
air samples include Acremonium species, Basidiomycota, Bipolaris species, Curvularia species, Dreschlera, Fusarium species, and Mucor and Penicillium species.
Table 2. Detection of molds in hospital plumbing and on environmental
surfaces using the swab culture sampling method
Source
Total positive
sites/total
tested sites (%)
Molds
recovered*
Positive sites
by molds
Water tanks, inner
walls/draining ports 13/48 (27) Alternaria 7
Bipolaris 4
Penicillium 4
Cladosporium 3
Acremonium 2
Sinks† 78/334 (23) Paecilomyces 38
Acremonium 23
Penicillium 6
Showers‡ 147/721 (20) Paecilomyces 63
Aspergillus 30
Penicillium 30
Fusarium 25
Acremonium 20
Toilets§ 8/34 (23) Aspergillus 4
Penicillium 5
Paecilomyces 1
Cladosporium 1
Patient rooms¶ 38/174 (22) Penicillium 19
Aspergillus 12
Alternaria 10
Cladosporium 6
Aspergillus species recovered in surface swab samples included A niger (50 %),
A fumigatus (19 %), A terreus (14 %), A flavus (9 %), A nidulans (7%), and A sydowi
(1%). All the Paecilomyces species were P lilacinus. Twelve of 37 Fusarium species
could be identified; 8 (67%) were F solani and 4 (33%) were F oxysporum.
*Molds shown are those that accounted for 10% of positive swab samples.
Other molds recovered include Bipolaris, Chaetomium, Chrysonilia, Curvularia,
Epicoccum, Mucor, Nigrospora, Oospora, Phialophora, and Trichoderma species.
†Includes drains and drain covers (n 119), surfaces (n 88), plumbing and
faucet aerators (n 65), and O-ring seals (n 62).
‡Includes drain and drain covers (n 154), floors (n 154), walls (n 176),
shower heads (n 158), and plumbing (n 79).
§Includes seats (n 16) and bowls (n 18).
¶Includes HEPA filter surfaces (n 17), walls (n 31), floors (n 34),
windowsills (n 17), room surfaces (n 51), objects related to patient care
(mattress, thermometer case, stethoscope pad, oxygen nozzle; n 24).
2544 ANAISSIE et al BLOOD, 1 APRIL 2003 VOLUME 101, NUMBER 7recovered from indoor hospital air; and (6) no seasonal correlation
in airborne molds exists between the indoor and outdoor air.
These findings suggest that waterborne molds enter the hospital
via municipal water and are subsequently integrated in the water
distribution system biofilm. The higher recovery of molds in the
initial water samples (compared with the subsequent ones) and
from the plumbing structures of the older building further support
the role of the water biofilm. A higher rate of dislodging of biofilm
particles in the initial sample is known to occur with other
biofilm-related microbes,
11
and the extent of biofilm formation
increases with aging of the water structures.
12
Taken together, our findings suggest that, in hospitals with
adequate air precautions, airborne molds originate from hospital
water and not contaminated outside air. Further support for this
hypothesis is given by the molecular studies showing relatedness
between clinical and water-associated environmental samples of A
fumigatus
13
This patient with refractory lymphoma died of A
fumigatus pneumonia. Isolates from the patient’s room shower
wall showed the same genotype as the isolate obtained by
bronchoscopy, whereas repeated testing of room air failed to yield
A fumigatus.
The increasing incidence of aspergillosis reported despite the
widespread implementation of air precautions,
3
the lack of correlation between the air spore counts of Aspergillus species and rate of
nosocomial aspergillosis or colonization by aspergilli,
14
and the
increase in airborne molds in a HEPA-filtered cancer unit in which
the source of these molds was ultimately traced to leaking
plumbing lines are also suggestive of a water source for these
airborne molds.
15
In support of possible water-relatedness of at least some mold
infections, infections with Aspergillus and other molds have been
reported and include pneumonias in near-drowning accidents
involving healthy individuals,
16-20
nosocomial A niger cutaneous
infection in a BMT unit,
21
disseminated infections by F solani
4
and
Exophiala jeanselmei,
22
and endophthalmitis by Acremonium species.
23
Paecilomyces lilacinus was the fourth most frequently
recovered molds from air and water samples in our study. The same
pathogen was responsible for an outbreak of serious infections and
death in a hematology and BMT unit.
24
The organism is phylogenetically related to Fusarium species
25
and, importantly, tends to
shares their resistance to treatment with polyene drugs.
The rank order of the fungal genera recovered is maintained
across all sampling areas (water, bath air, room air, and hall air;
Figure 2) for Aspergillus species. Indeed, Aspergillus species was
one of the most frequently isolated organisms in our environmental
samples and is also the most common mold infection in this patient
population.
1 We also frequently recovered other molds such as
Penicillium species and Paecilomyces species, organisms that are
rarely associated with infections. This lack of correlation between
high patient exposure to the latter organisms and the well-known
very low rate of infection are best explained by the lower virulence
of these organisms compared with Aspergillus species.
1
The magnitude of the problem of waterborne molds cannot be
fully appreciated until prospective studies correlate the concentration of molds in various hospital water systems with the rate of
infection in patients cared for at these hospitals and until a genetic
identity between the clinical and the environmental isolates is
proven. These studies are currently under way.
Our findings that hospital water can be an important source of
opportunistic molds have clinically significant implications. An
effective and inexpensive approach to prevent patient exposure to
waterborne molds in the hospital setting is to provide high-risk
patients with sterile (boiled) water for drinking and sterile sponges
for bathing (to avoid the aerosolization associated with showering).
Such precautions could also be extended to the community, after
hospital discharge, as dictated by the net state of immunosuppression of individual patients. Because the recovery of molds in water
systems has been reported worldwide in the community and
hospital settings as early as in 1982,
5,6,26-28
it is likely that our
recommendations may be applicable to various communities and
hospitals. In addition, we have recently shown that cleaning the
floors of patient shower facilities in a BMT unit reduced the mean
air concentration of Aspergillus species (from 22 CFU/m3
to 4
CFU/m3
; P .0047) and other airborne pathogenic molds.
29 We
strongly recommend this approach for patients at high risk for
developing serious infections with these fungi.
In conclusion, hospital water distribution systems may be
a potential indoor reservoir of Aspergillus species and other
molds leading to aerosolization of fungal spores and potential
patient exposure.
Acknowledgments
We thank the University of Arkansas for Medical Sciences Office
of Grants and Scientific Publications for their editorial assistance
during the preparation of this manuscript and Dr Kieren Marr, from
the Fred Hutchinson Cancer Center, Seattle, WA, for her critical
review of the manuscript.
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2546 ANAISSIE et al BLOOD, 1 APRIL 2003 VOLUME 101, NUMBER 7

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 as well as Kill Cockroaches
 

Important Herbal Remedy
&
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Hong Kong Sex Pills http://www.hongkongsexpills.com


 
Environmental Health Websites

Mold Health Information:  http://www.moldinspector.com
Mold Inspector Directory http://www.certifiedmoldinspectors.com
Mold Removal http://www.moldmart.net 
Mold Training http://www.ecology-college.com
Environmental Hygienists http://www.certifiedhygienists.com
Allergy, Asthma, & Sinusitis http://www.allergy-asthma-sinusitis.com
Hong Kong Mould http://www.envirohongkong.com
Singapore Mould http://www.envirosingapore.com
Malaysia Mould http://www.enviromalaysia.net
Indonesia Mould http://www.enviroindonesia.com
Thailand Mould http://www.envirothai.com
Taiwan Mould http://www.envirotaiwan.com
Germany Mould http://www.envirogermany.com
Canada Mould: http://www.envirocanada.net
Mold Test Kits  Ozone Generator  Workplace Mold  Air Conditioning Mold
Mold Lawyer  Home Repair  Home Remodeling