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3
Journal of Environmental Health Research, Volume 4, Issue 1, 2005
Abstract
The recent introduction of new vacuum cleaning
technologies and systems is largely due to heightened
awareness of the health effects associated with particu-
late matter, bacteria and fungi on interior flooring.
Health effects and symptoms such as asthma,
respiratory illness and skin irritations have been shown
in a number of studies to be associated with airborne
particulates and microbiological concentrations in
indoor environments. This study investigates the
influence of intensive, high efficiency HEPA vacuuming
on indoor fine particulates and fungal levels and
composition in non-complaint and non-mould
contaminated Australian residential environments.
Baseline monitoring for airborne fungi and other air
quality parameters was conducted before and after the
cleaning interventions in six test and five control homes.
Monitoring was conducted with N-6 Andersen samplers
for viable airborne fungi for two minutes at a flow rate of
28.3 L/min. Cultures were then incubated, counted and
differentiated. Outdoor samples were concurrently
collected for comparison with indoor levels.
Results post-intervention show an initial increase in
indoor fungal levels in the vacuum homes. The higher
fungal levels and fungal genera isolated during the
first vacuuming period are due to the initial loadings
present in the carpet in addition to the increased
activity and intensive mechanical action (rotating
brush) of the vacuuming cleaning process, stirring up
and resuspending dust and particulates from deep
within the carpet. Subsequent vacuuming inter-
vention periods recorded reductions in indoor fungal
levels in the vacuum homes, whereas levels in the
control homes were wide-ranging. The indoor fungal
composition in the vacuum homes remained similar,
both before and during the vacuum intervention
periods with
Cladosporium
and
Penicillium,
the two
dominant fungal species isolated.
Airborne indoor fine particulates in the vacuum
homes were consistently lower following the vacuum
interventions compared to the control homes. The
study showed that regular maintenance of carpets
using high efficiency vacuuming could help in
reducing airborne fine particulate levels and maintain
a stable fungal spora within the indoor environment.
Keywords:
Activity sampling, carpet, cleaning, fine
particulates, HEPA, high efficiency, homes, indoor
fungi, residential, vacuuming.
Introduction
The management of cleaning maintenance and the
quality of indoor air are vitally important and
necessary, in order to protect both human health and
the materials and equipment in the indoor
environment. Cleaning and the management of
cleaning maintenance is the final defence in
managing indoor environmental quality (ACGIH,
1999). In the past 5-10 years, there has been
heightened public awareness and interest in the
health effects associated with particulate matter,
bacteria and fungi present in carpets and on interior
flooring of residential homes and commercial
buildings. This has led to increasing research into new
vacuum cleaning technologies and systems.
Contamination from indoor sources and the ensuing
dispersal of airborne particulates and fungi either in
the workplace or living quarters often leads to a loss of
productivity and severe health effects and symptoms.
It is estimated that of the 760 million cases of
respiratory diseases reported annually, 20-30% may be
affected by suspended particulate matter (White &
Dingle, 2002; Schwela, 2000; WHO, 1997). Strong
links between dust and health symptoms have been
found in a number of scientific studies (Gyntelberg
et
al.
, 1994; Kildeso et al., 1998 & 1999; Jones, 1999).
Short-term health effects from particulate matter
include skin, eye, nose and throat irritations and
upper respiratory infections including bronchitis and
pneumonia. Other symptoms may include headache,
nausea and allergic reactions (Hansen & Burroughs,
1999; US Institute of Medicine, 2000). Particulate
inhalation can further aggravate prevailing symptoms,
Reducing airborne indoor fungi and fine particulates in
carpeted Australian homes using intensive, high efficiency
HEPA vacuuming
Cedric D. Cheong1and Dr Heike G. Neumeister-Kemp2
1PhD Candidate, School of Environmental Science, Murdoch University, Western Australia
2Research Associate, School of Biological Sciences, Murdoch University, Western Australia
Correspondence: Cedric Cheong, School of Environmental Science, Murdoch University, South Street,
Murdoch, Western Australia, 6150. Fax: +61 8 9310 4997, Tel: +61 8 9310 2226, E-mail:
futora@wn.com.au
JEHR - vol4 iss1.qxd 8/4/05 3:49 pm Page 3
4Journal of Environmental Health Research, Volume 4, Issue 1, 2005
particularly in individuals with existing medical
conditions and are immunosuppressed (Arden, 1991;
American Lung Association, 1994; Etkin, 1994).
The degree to which indoor particulate matter
translates to short or long term health effects is dep-
endent on the size and concentration of the particles,
the duration of exposure and the pre-existing health
and condition of the exposed individual (Etkin, 1994).
Of greatest health significance are the fine particu-
lates that are small enough to be inhaled into the
deepest parts of the lungs. These fine particulates are
generally less than 2.5 microns in diameter and are
less affected by gravitational settling and can stay
suspended in the air for longer periods of time,
increasing the possibility of inhalation. These fine
particulates can cause damage at the cellular level by
bypassing the body’s respiratory system defence
mechanisms (Amman
et al.
, 1986). Increased particu-
late levels are associated with increased mortality with
ultra fine particulates being of greatest health concern
(Creason, 2001; Smith, 2000; Hansen & Burroughs,
1999; US Institute of Medicine, 2000).
Despite the increasing scientific knowledge and grow-
ing awareness of the known health consequences of
fine particulates, there are no set guidelines or
standards for fine particulate exposure for indoor air in
Australia or overseas, with little research conducted on
fine particulate levels found in Australian indoor
environments, particularly homes (White & Dingle,
2002). For outdoor air, the national (NEPM) PM10
annual ambient average standard is 50 ug m
-3
(Ayers
et
al.
, 1999). The US EPA has set ambient annual average
PM10 and PM2.5 standards at 50 ug m
-3
and 15 ug m
-3
respectively. The 24-hour PM10 and PM2.5 standard is
150 ug m
-3
and 65 ug m
-3
respectively (USEPA, 1997).
Dust particulates can be contaminated by biological,
physical and chemical sources with toxic and allergenic
properties. Physical contaminants of dust include
heavy metals, mineral particulates, synthetic and
natural fibres (Etkin, 1994). Biological contaminants of
dust include pollen, fungi, bacteria, viruses, animal
dander and epithelial cells (Leese
et al.
, 1997).
Scientific research studies have increasingly linked
indoor air quality (IAQ) problems and indoor fungi
with major respiratory health effects such as asthma,
hypersensitivity, allergies, infections, sick building
syndrome, respiratory and skin irritations (Husman
2000; Garrett et al., 1998; ACGIH, 1999; Wallace,
1996; Miller, 1992; Stetzenbach, 1997).
Fungi are ubiquitous and are transported from outdoor
sources into the building envelope and indoor
environment through a variety of means, including by
adherence to human skin, clothes, shoes, pets and
directly conveyed into the indoor environment or via
airborne transport of spores by means of ventilation or
open doors and windows. Allowing fungi to build up
indoors, particularly in bedrooms, is undesirable and
should be prevented in order to reduce potential health
effects (ACGIH, 1999; Schober, 1991; Solomon, 1976).
Studies have shown that proper cleaning and
maintenance can reduce the various components of
dust, including fungi and reduce the concentration on
surfaces including floors and the levels of airborne
dust if the cleaning is of a high standard (Frank et al.,
1997). Furthermore, the appropriate cleaning
maintenance can make a significant contribution to
healthy indoor air quality (Ragsdale
et al.
, 1995). Little
research has been conducted on the effects cleaning
has on indoor air contamination which is required to
ensure the indoor environment has a high standard of
air quality for human health (Walinder
et al.
, 1999).
A rigorous cleaning program aimed at preventing the
build up of fungi and fine particulates present in
carpets and indoor flooring is one such approach in
reducing levels. Studies investigating the effectiveness
of vacuuming have found that it can significantly
improve indoor environmental quality by reducing the
concentration of lead-containing dust, allergens, or
other hazardous particulate materials on surfaces (Lioy
et al.
, 1998; Rhoads
et al.
, 1999; Hegarty
et al.
, 1995).
This study focuses on an intensive, high efficiency HEPA
vacuuming regime as a cleaning intervention and its
effect on the level of airborne fine particulates and the
level and species range of viable airborne fungi in
residential carpeted environments in Perth, Western
Australia.
Carpets
Numerous studies have compared the benefits and
disadvantages of carpets versus hard surface flooring.
Carpets can be a reservoir for bacteria, fungi and
other microorganisms (Shaughnessy
et al.
, 2002;
Wickman et al, 1992). Studies by Warner (1999) and
Bahir
et al.
(1997) concluded that there were
significant clinical benefits for allergy sufferers in the
removal of carpets. Dybendal
et al.
(1991) found that
carpets can store vast amounts of particulate matter
and accumulate more dust, proteins and allergens per
unit area than smooth hard floors. Foarde and Berry
(2004) found that airborne biocontaminants concen-
trations were as much as three times higher over hard
surface floors than over carpeted floors. Willie (1974)
observed that it required approximately 10 times the
air velocity to resuspend a settled particle from a
carpeted surface versus a hard surface flooring.
Carpets fulfil many important health and social
functions, acting as a buffer, sink and filter for a
variety of potential pollutants from tracked in soil,
settled dust, spills and adsorbed chemicals. As a high
surface area substrate, carpets can have a positive
effect by effectively reducing the airborne levels of
many of these pollutants (Berry, 1993, 1994; Cole
et al.
,
1992). Carpets are also a low emitter of volatile organic
compounds with a relatively rapid decay (Black et al.,
1993; Hodgson
et al.
, 1992). Carpets also suppress
dust and noise, thus helping maintain a comfortable
Cedric D. Cheong and Dr Heike G. Neumeister-Kemp
JEHR - vol4 iss1.qxd 8/4/05 3:49 pm Page 4
indoor climate in buildings and homes (Berry, 1993,
1994; Schroder, 1990).
The critical factor however, is regular maintenance. It
is essential that carpets be well maintained and clean-
ed to extract and remove trapped pollutants, thus
minimising their opportunity to become resuspended
(White, et al., 2002; Hedge, 2001; Kemp
et al.
, 1998;
Berry, 1993; Dybendal et al., 1991; Hunter
et al.
, 1988).
If loadings of biocontaminants are allowed to build up
until the carpet is no longer a sink, the carpet itself
becomes a source of contamination, contributing to
various respiratory illnesses and symptoms (Cole
et al.
,
1994; Norback
et al.
, 1994).
Vacuum cleaning
Scientific studies have shown that ordinary household
activities, from dusting and vacuuming to dancing,
floor cleaning, bed making or even simply walking over
carpeted or hard floor areas, could result in an
increase in airborne particulates including fungi
(Ferro et al, 2002; Long
et al.
, 2000; CMHC, 1999;
Franke et al., 1997; Lehtonen
et al.
, 1993). The use of
vacuum cleaners for cleaning and maintenance is
synonymous with 20th century household chores. It is
estimated that in the United States, 60% of the
population utilise a vacuum cleaner for cleaning at
least once a week with 12% vacuuming twice a day
(Lioy et al, 1999). In the work place, industries such as
the hospitality industry vacuum their premises daily.
The activity of vacuum cleaning can release significant
levels of particulates including fungi into the air.
Depending on the characteristics of the vacuum
cleaner (rotating brush head and filters), its
maintenance record and age, vacuum cleaners
themselves could be a source of particles. Human
exposure to particulates from the activity of vacuum
cleaning can be significant. Studies by Dunford (1992)
and Schneider et al. (1994) demonstrated a worsening
indoor air quality following the use of conventional
vacuum cleaning equipment due to the use of bag
filters, which allowed smaller particulates to escape.
Particulates from the vacuum motor, inefficient
vacuum bags, vacuum brushes releasing deeply
embedded particles from the carpet and inefficient
filters all could contribute to elevated levels (Lioy
et al.
,
1999; Franke
et al
, 1997; Dybendal
et al.
, 1991).
Vacuum cleaners principally work on using a moving
air stream to pick up dirt and debris. An internal
rotating fan creates a pressure differential between the
ambient air outside the vacuum cleaner and the air
inside the vacuum cleaner creating a suction or partial
vacuum inside the vacuum cleaner. The movement of
air particles collides against any loose dust or debris
and provided the suction is strong enough and the
debris light enough, the resultant material is carried
through the inside of the vacuum cleaner. Extra
assistance in the form of rotating brushes at the intake
port greatly assists in the removal efficiency of dust
and debris being loosened from the carpet (Dunford,
1992; Schneider
et al.
, 1994; Trakumas
et al.
, 2001).
There are two approaches when it comes to vacuum
cleaning floor surfaces in the indoor environment. The
first approach is vacuuming such that the carpeting or
flooring is free of any visible dirt or large particulates.
Often this process is relatively quick and simply
involves a once over vacuuming of the surface of the
carpet. However, heavier or smaller particulates
present deep in the fibres of carpets are often not
removed and remain so, with biocontaminant loadings
building up and available for resuspension into the air
(Gorny et al., 2001; Figley
et al.
, 1993; Dybendal
et al.
,
1991; Kemp
et al.
, 1998).
Intensive vacuuming, over a longer period of time and
with higher efficiency (stronger suction) and a
physical or mechanical action (rotating brushes)
breaking and disrupting the electrical and physical
attachments to the carpet fibres is required to
effectively remove not only the larger visible
particulates but also the smaller and attached
particulates, including fungi from deep inside the
carpet pile (Kemp
et al.
, 1998).
Vacuum cleaners and systems come in many forms and
designs, from upright and canister designs which
capture dirt and debris in a porous bag, to wet/dry
vacuum cleaners and ducted central vacuum systems,
to the more recent bagless cyclone vacuums and
systems utilising HEPA filters. Advances in vacuum
cleaner technologies in particular in the design,
suction mechanisms and collection systems, have seen
the recent high efficiency bagless cyclone vacuums
with HEPA filters being more efficient and effective in
removing the dust, fine particulates and debris, comp-
ared to conventional older model vacuum cleaners.
Scientific studies conducted by Hegarty
et al.
(1995)
and Ewers
et al.
(1994) have shown that different
vacuum cleaners remove and retain different amounts
of dust from the same surface. The choice of the
appropriate and suitably equipped vacuum cleaner is
therefore vital for efficient cleaning. An intensive, high
quality deep cleaning of carpeted floors requires a
combination of timing (vacuuming long enough to
effectively remove particles) and suitable equipment
(bagless cyclone system, rotating brush head,
sufficient suction and HEPA filters).
Materials and Methods
Eleven residential dwellings within a 15km distance
from Murdoch University, Perth, Western Australia
were selected for participation in this study. All homes
were single storey, of brick construction over a
concrete pad with their age ranging from two to more
than 30 years. Specific selection criteria required that
all homes be fully carpeted (wool or synthetic) and
that no tobacco smoking took place within the home
during the study period.
5
Journal of Environmental Health Research, Volume 4, Issue 1, 2005
Reducing airborne indoor fungi and fine particulates in carpeted homes
JEHR - vol4 iss1.qxd 8/4/05 3:49 pm Page 5
6Journal of Environmental Health Research, Volume 4, Issue 1, 2005
Of the eleven homes, six were randomly assigned in
the ‘vacuum’ intervention group whilst the other five
were assigned in the ‘control’ group. For the ‘vacuum’
intervention group, the entire area of exposed
carpeting and flooring, fabric upholstered sofas and
the participant’s bed were intensively vacuumed (4
mins m
-2
for the 1st intervention, 2 min m
-2
thereafter)
fortnightly with a vacuum cleaner (Filter Queen, HMI
Industries) meeting the Australian Standard 3733
(Standards Australia, 1995), and equipped with a
hospital grade filtration system (HEPA), to trap and
remove particulate soil and dust, for the duration of
the study period (White
et al.
, 2002).
The vacuum cleaner was equipped with a motorised
head with rotating brushes to add extra power to the
cleaning system. The process of conducting the initial
deep cleaning took place over 4-5 hours depending
on the total area of exposed carpets. Subsequent
fortnightly vacuuming interventions were carried out
over 2-3 hours. The area of exposed carpet ranged
from 4m
2
to 13m
2
, with an average of between 6m
2
and
7m
2
. The mean whole of house carpet area was
approximately 60m
2
. For the ‘control’ group, no
specific vacuum cleaning interventions were
conducted. No specific instructions were given to all
occupants with regard to the opening or closing of
windows or doors in the bedroom of the participants.
Monitoring protocol
Prior to the vacuuming intervention, baseline air
samples were obtained from the bedrooms of all eleven
homes for later comparison. The baseline air quality
parameters measured included fine particulate matter
(particles m
-3
), temperature, relative humidity and
airborne viable fungal levels. Windows and doors in the
bedrooms were kept shut during the sampling period.
Two sets of indoor measurements were taken for
comparative analysis. The first measurement was taken
prior to a simulated activity/impaction test and another
immediately after the exercise. Outdoor air quality
parameters were concurrently monitored for compar-
ison with indoor levels. The vacuum and control homes
were monitored four times during the vacuum period, at
3 weeks, 7 weeks, 11 weeks and 15 weeks.
Monitoring was conducted in the bedroom of each
participant. Airborne viable indoor fungal spore
sampling was conducted in the morning, in the middle
of the bedroom with duplicate N-6 Andersen multi-
hole impactor samplers (Andersen Instruments Inc.,
Atlanta GA) co-located, at a height of 1 – 1.5 m above
the ground or floor surfaces, for two minutes at a flow
rate of 28.3 L min
-1
(Foarde & Berry, 2004; Kemp
et al.
,
2002; Hyvarinen et al., 1993; Lehtonen
et al.
, 1993).
Outdoor control samples were collected outside the
house (2 m away from house) to represent the air that
may enter the buildings through open windows and
doors, for comparison with indoor samples (Portnoy
et
al.
, 2004; ACGIH, 1999). Monitoring of homes
scheduled on a particular day was completed within
two hours, to maintain similar monitoring time period
constraints (Cheong
et al.
, 2004).
In order to enumerate a broad spectrum of fungi,
duplicate side-by-side sampling of airborne indoor
fungi was conducted on malt extract agar (MEA -
DIFCO) (broad spectrum medium) and Dichloran
18% Glycerol Agar (DG18 – Oxoid) (slow growing
fungi – low water activity, aw) plates. Both media were
amended with Chloramphenicol (Sigma) to limit
bacterial growth. Duplicate viable outdoor air fungal
samples were collected concurrently for comparison
with indoor levels (ACGIH, 1999; Hyvärinen
et al.
,
2001; Samson
et al.
, 1994).
In total, ten airborne viable fungal samples were taken
per house per sampling occasion. A subset of samples
were then further analysed with fungal colonies
differentiated to ascertain the fungal profile in each of
the dwellings. Due to the substantial increase in sample
numbers following the interventions, only those species
identified before the cleaning intervention were
targeted to track any changes occurring as a result of
the intervention. New species following the
interventions were not identified to species level unless
they occurred at substantial concentrations.
Temperature, relative humidity and suspended part-
iculate matter were considered as possible predictors of
indoor fungal levels and were measured in tandem with
airborne viable fungal sampling. Airborne fine
particulate matter was measured with a P-Trak Ultrafine
Particle Counter (Model 8525, TSI Inc.), capable of
detecting particles in the size range 0.02 to 1.0
micrometer. The concentration range for the P-Trak was
0 to 5 x 10
5
particles per cubic metre (particles m
-3
).
Temperature and relative humidity were measured with
an indoor humidity gauge thermometer (accuracy 618C,
65%RH) (Model 63-1013, InterTAN Inc.).
Simulated activity/impaction
The technique for simulating indoor activity as describ-
ed in Cheong
et al.
(2004) was used to determine the
influence of human activity on indoor fungal numbers
and composition in the carpeted environment. To
maintain quality control, the methodology had to be
simple, repeatable and equipment inexpensive and
readily available and accessible. A standard fully inflated
(30 psi) basketball was dropped from a height of 1.5m
in a grid-like pattern over the entire exposed carpeted
area for a period of 60 seconds. Duplicate viable
airborne fungal samples were subsequently taken
following the impaction/simulated activity for both
MEA and DG18 media. This technique was utilised to
simulate activity during the monitoring period.
Incubation and counting
The duplicate samples collected on the MEA and
DG18 plates were transported in an insulated
Cedric D. Cheong and Dr Heike G. Neumeister-Kemp
JEHR - vol4 iss1.qxd 8/4/05 3:49 pm Page 6
Yeast (Morphological group)
includes all yeast like fungi
found (except Aureobasidium)
Rhodutorula spec.,
Sporobolomyces roseus,
Candida spec.
Geomyces pannorum,
Geotricum spp.
Filamentous fungi
Cladosporium cladosporioides.,
C. herbarum,
C. sphaerospermum; Penicillium
chrysogenum,
P. commune,
P. glabrum .
P. spp.;
Aspergillus fumigatus,
A. nigar,
A. ochraceus,
A. sydowii,
A. terreus,
A. versicolor,
A. spp.;
Aternaria alternata, Alternaria spec.;
Fusarium culmorum,
F. oxisporum,
Fusarium solani,
F. sporotrichioides
F. spec;
Epicoccum nigrum,
Botrytis cinerea,
Aureobasidium pullulans,
Rizopus stolonifer.
Other fungi found
(not complete)
Mucor hiemalis,
M. racemosus,
Oidodendron griseum,
Absisdia spp.,
Acremonium spp.,
Beauveria bassiana,
Chrysonilia crassa,
Chrysosporium spp.,
Paecilomyces voriotii,
Phialophora spec.,
Phoma glomerata,
Cuvularia spec.,
Scopulariopsis brevicaulis,
Syncephalastrum racemosum,
Verticillium spec.
7
Journal of Environmental Health Research, Volume 4, Issue 1, 2005
Reducing airborne indoor fungi and fine particulates in carpeted homes
Table 1.0 Fungal taxa isolated
container, to the laboratory for incubation and analysis,
within two hours of sampling. The ten replicate culture
plates were incubated for five days at 228C (618C) and
30%RH (65%RH) in a darkened climate controlled
incubation room. Once incubated, the total
concentration of viable culturable fungal colonies was
determined with a counting loop and binocular and
compound microscopes and reported as mean colony
forming units per cubic meter of air (CFU m
-3
). Since
replicate plates were collected, the data were averaged.
After counting, a subset of the fungal samples was
identified to genus and species level to determine the
fungal composition. Subsets were taken from samples
from the pre vacuum cleaning intervention and during
the vacuum cleaning intervention periods. The
morphological characteristics of the fungi were
determined microscopically at 40x and 100x objective
magnification. Fungi were identified to genus and
species level with the aid of taxonomic texts (Domsch
and Gams, 1993; Anderson and Ellis, 1993; Samson
et
al.
, 1995) and the Hughes-Tubaki-Barron system and
Saccardo system (Barnett and Hunter, 1972). Fungal
colonies that did not produce spores or conidia were
classified as sterile mycelia. Fungal species that are not
classed as potential human pathogens (Samson et al.,
1995) and did not make up significant numbers were
grouped as ‘others’.
Statistical analysis
Analysis of indoor air quality data collected for this
study was performed using the MS Excel V5.0 Statistical
Add-ins Package. Paired t-tests assuming equal variance
(P) and a = 0.05 and ANOVA calculations were
performed for analysis of variance. Pearson product
moment correlation analysis was used to investigate
possible associations or relationships between the
mean air temperature, relative humidity, particulate
matter and total fungal colony forming units.
Results
Two hundred and forty samples of airborne viable fungi
and fine particulate readings were taken from the six
vacuum homes and the five control homes over the
study period beginning mid-May and ending mid-
October 2000.
Baseline ambient airborne viable fungal, fine
particulate and air quality parameters for Australian
conditions
The average ambient baseline indoor fungal levels of the
eleven Australian residential homes (pre-intervention)
were 467 CFU m
-3
. Corresponding outdoor fungal levels
were 443 CFU m
-3
. The average indoor fungal level
JEHR - vol4 iss1.qxd 8/4/05 3:49 pm Page 7
Indoor (n=42)
90.5
97.6
57.1
64.3
92.9
23.8
26.2
Activity (n=42)
92.9
97.6
61.9
71.4
90.5
16.7
42.9
Outdoor (n=42)
95.2
97.6
54.8
64.3
81.0
31.0
47. 6
8Journal of Environmental Health Research, Volume 4, Issue 1, 2005
Cedric D. Cheong and Dr Heike G. Neumeister-Kemp
following the simulated activity/impaction was 515 CFU
m
-3
. Ambient indoor conditions in the eleven test homes
at the start of the study period included an average
temperature of 20.78C, 61.7% relative humidity and
1.52 x 10
-2
particles m
-3
airborne fine particulates.
Corresponding outdoor conditions included an average
temperature of 19.48C, 62.2% relative humidity and
1.44 x 10
-2
particles m
-3
airborne fine particulates.
Fungal composition
Due to the substantial increase in sample numbers
following the interventions, only those species
identified before the intervention were targeted to track
any changes. New species following the interventions
were not identified to species level unless they occurred
at substantial concentrations.
In total, seventeen fungal genera were identified in the
viable airborne indoor and outdoor samples, 11 to genus
level (
Cladosporium, Penicillium, Aspergillus, Alternaria,
Fusarium, Botrytis, Aureobasidium, Rhizopus, Epicoccum,
Yeast, Nigrospora
) and 6 to species level (
Neurospora crassa,
Trichoderma viride, Chaetomium globosum, Ulocladium
chartarum, Wallemia sebi, Mucor heimialis
). The full list of
fungal taxa isolated in this study is presented in Table 1.0.
Between five and six different fungal genera were
commonly isolated in each of the indoor and outdoor
samples for the 11 residential homes.
Penicillium
(97.6%),
Yeast
(92.9%) and
Cladosporium
(90.5%) species were
the most commonly found fungi in the indoor samples,
along with
Alternaria
(64.3%) and
Aspergillus
(57.1%)
species (Table 2.0). More fungal species were isolated in
the outdoor samples with
Penicillium
(97.6%),
Cladosporium
(95.2%) and
Yeast
(81.0%) species the
most commonly isolated fungi in all outdoor samples of
the 11 test homes. Other fungi isolated outdoors
include
Alternaria
(64.3%),
Aspergillus
(54.8%),
Botrytis
(47.6%) and
Fusarium
(31.0%).
With activity/impaction resuspending dust, fungi and
particulates from deep inside the carpet pile, a greater
percentage (10.3%) and number of fungal species were
isolated, in particular
Botrytis
(16.7% increase),
Alternaria
(7.1% increase),
Aspergillus
(4.8% increase)
and
Cladosporium
species (2.4% increase). Other fungi
isolated included
Penicillium
,
Yeast
and
Fusarium
(Table
2.0).
Cladosporium
and
Penicillium
were the two
dominant fungal genera, making up 73% of the total
indoor fungal composition in the eleven residential
homes before the cleaning intervention.
Vacuum cleaning intervention
The first vacuum intervention period (Week 3) brought
about an increase in indoor fungal levels in the vacuum
homes. A 90% increase in indoor fungal levels (696 –
1323 CFU m
-3
) was recorded in the vacuum homes. This
compared to a 10% decrease (238 – 215 CFU m
-3
) in
indoor fungal levels recorded in the control homes
during the same period. Subsequent vacuuming
intervention periods recorded reductions in indoor
Table 2.0 Prevalence of fungal genera prior to the cleaning intervention in
vacuum and control homes expressed as a percentage (%).
Figure 1.0 Percentage change in indoor fungal
levels compared to baseline levels in vacuum
and control homes.
40
0
-20
-40
-100
Week 3
Week 11
20
80
60
100
-60
-80 Vacuum Control
% change
Week 7
Week 15
Fungal genera
Cladosporium
Penicillium
Aspergillus
Alternaria
Yeas t
Fusarium
Botrytis
JEHR - vol4 iss1.qxd 8/4/05 3:49 pm Page 8
fungal levels in the vacuum homes, whereas levels in the
control homes were wide-ranging (Figure 1.0).
There was a 24.5% reduction (1.67 – 1.26 x 10
-2
particles
m
-3
) in airborne fine particulate levels in the homes
following the first vacuuming intervention, compared to a
210% (1.36 – 4.22 x 10
-2
particles m
-3
) increase in
airborne fine particulate levels in the control homes. The
large increase in the control homes can be attributed to
higher fine particulates in the outdoor air infiltrating
indoors. Fine particulate levels in the vacuum homes
continued to decrease with subsequent vacuuming
interventions. Fine particulate levels in the control homes
reflected a similar pattern to that of outdoor levels (Table
3.0). There was a strong and significant correlation
between indoor particulate levels before and after
impaction/simulation (P=0.98, 0.09).
Change in fungal composition
Cladosporium
and
Penicillium
were the two dominant
Average airborne
fine particulates
(n=195)
Pre vacuum
1st vacuum
intervention
final vacuum
intervention
Indoor
1.67 (0.97)
1.26 (0.67)
1.30 (1.5)
Outdoor
1.83 (1.43)
2.54 (1.35)
0.77 (0.83)
Activity
1.49 (1.50)
1.31 (4.43)
1.18 (1.46)
Indoor
1.36 (1.33)
4.22 (1.74)
1.55 (1.24)
Outdoor
1.06 (0.91)
5.83 (3.69)
1.46 (1.34)
Activity
1.50 (1.24)
4.43 (1.58)
1.46 (1.09)
Vacuum homes
x 10-2 particles m-3
(SD)
Control homes
x 10-2 particles m-3
(SD)
9
Journal of Environmental Health Research, Volume 4, Issue 1, 2005
Reducing airborne indoor fungi and fine particulates in carpeted homes
Table 3.0 Average airborne fine particulate levels in the vacuum and control homes
Time period
Pre vacuum
Vacuum
intervention
Indoor
species*
41% Clad
34% Pen
6% Asp
3% Alt
1% Fus
15% Yeast
40% Clad
30% Pen
5% Asp
2% Alt
1% Fus
2% Epic
14% Yeast
5% Sterile
Outdoor
species*
51% Clad
25% Pen
8% Asp
3% Alt
1% Fus
1% Bot
7% Yeast
3% Sterile
23% Clad
51% Pen
5% Asp
3% Alt
2% Fus
4% Bot
2% Aur
1% Rhiz
9% Yeast
Activity
species*
41% Clad
35% Pen
3% Asp
4% Alt
1% Bot
1% Aur
14% Yeast
39% Clad
34% Pen
3% Asp
11% Alt
1% Bot
1% Aur
1% Rhiz
6% Yeast
3% Sterile
Indoor
species*
39% Clad
33% Pen
5% Asp
7% Alt
1% Rhiz
2% Epic
11% Yeast
2% Sterile
28% Clad
37% Pen
10% Asp
5% Alt
2% Fus
3% Epic
15% Yeast
Outdoor
species*
52% Clad
28% Pen
5% Asp
7% Alt
4% Fus
1% Bot
2% Epic
7% Yeast
29% Clad
46% Pen
5% Asp
3% Alt
1% Fus
2% Bot
2% Epic
11% Yeast
Activity
species*
44% Clad
32% Pen
6% Asp
7% Alt
1% Bot
1% Rhiz
10% Yeast
32% Clad
28% Pen
11% Asp
13% Alt
1% Epic
13% Yeast
Vacuum homes (n=6) Control homes (n=5)
Table 4.0 Average fungal species distribution in vacuum and control homes pre vacuum and
during the vacuum cleaning intervention period
* Clad = Cladosporium, Pen = Penicillium, Asp = Aspergillus, Alt = Alternaria, Fus = Fusarium, Epic = Epicoccum,
Bot = Botrytis, Aur = Aureobasidium, Rhiz = Rhizopus
JEHR - vol4 iss1.qxd 8/4/05 3:49 pm Page 9
Cedric D. Cheong and Dr Heike G. Neumeister-Kemp
10 Journal of Environmental Health Research, Volume 4, Issue 1, 2005
fungal species. A change in fungal composition can be
seen in the outdoor samples over time with fungal
dominance changing from
Cladosporium
dominance in
the beginning of the study (Clad 51-52% Pen 25-28%)
to
Penicillium
dominance at the end of the study (Clad
23-29% Pen 51-46%) in the vacuum and control homes
(Table 4.0).
The indoor fungal composition in the vacuum homes
remained similar, both before and during the vacuum
intervention periods. When subjected to
impaction/activity, more species of fungi were isolated
overall in the vacuum homes during the vacuum
intervention, with
Alternaria
species increasing from 4%
to 11%, whilst
yeast
species decreased from 14% to 6%
(Table 4.0).
Discussion
Baseline culturable indoor fungal levels
The baseline culturable indoor fungal levels reported in
this Australian study (mean = 467 CFU m
-3
) were in the
same range as those reported in studies of airborne
indoor fungi levels in residential Australian houses
(median = 443 CFU m
-3
, 421 CFU m
-3
, 495 CFU m
-3
, &
812 CFU m
-3
(rural area)) (Cheong
et al.
, 2004;
Dharmage
et al.
, 2002; Godhish
et al.
, 1996; Garett
et
al.
, 1997). As a comparison with international
conditions, levels reported in this study were in a
similar range to that of Californian houses (mean = 480
CFU m
-3
) which have a similar climatic condition to that
of Perth, and complaint houses in Scotland (median =
624 CFU m
-3
), but higher than those reported in Finland
(generally under 100 CFU m
-3
, colder conditions) and
lower than those reported in non complaint houses in
Iowa (1200 CFU m
-3
, farming environment) (Reponen et
al., 1992; Flannigan
et al.
, 1993; DeKoster & Thorne,
1995; Kozak
et al.
, 1979). The comparison of our results
and those internationally supports the hypothesis of
higher levels of airborne viable fungi homes in farming,
or rural areas compared to those in urban residential
areas (Dharmage
et al.
, 2002; Pasanen, 1992).
Fungal composition
Penicillium, Cladosporium, Aspergillus, Alternaria
and
yeasts were the most common and widespread fungal
taxa recovered indoors and outdoors, reflecting similar
findings in fungal composition recovered in residential
environments in other Australian, US and European
studies (Dharmage
et al.
, 2002; Godhish et al., 1993;
Chew
et al.
, 2003; Kozak
et al.
, 1979; Li & Kendrick,
1995; Consentino
et al.
, 2002; De Lara
et al.
, 1990).
The change in fungal species composition from
Cladosporium
dominance in the beginning of the study
(Autumn season) to
Penicillium
dominance at the end of
the study (wetter Winter/Spring season) is supported by
studies by Cheong
et al.
(2004), Chew
et al.
(2003),
Koch
et al.
(2000), Solomon & Platts-Mills (1998) and
Hirsch & Sosman (1976), who similarly found
significant decreases in occurrence of
Cladosporium
and
Alternaria
in the winter period, but is contrary to studies
by Takatori
et al.
(2001) and Solomon (1976), which
show
Cladosporium
species dominating wetter time
periods/seasons (Table 4.0). As a direct comparison,
the Australian study by Godish
et al.
(1993) found much
higher levels of
Penicillium
species indoors (85.8%)
rather than outdoors (65%), whereas in this study
Penicillium
species indoors were only slightly higher
(35%) than outdoors (25%) during the pre vacuum
intervention period (Table 4.0). This difference can be
attributed to the cooler and wetter climate experienced
in the east coast of Australia (where the study by Godish
et al.
was conducted) compared to the milder and drier
climate of Perth, Western Australia.
It must be noted that not all
Penicillium
species prefer
dry conditions. It is possible that a shift to wet loving
Penicillium
species could have occurred in our study.
However, isolates were only identified to genera level,
and therefore meaningful analysis of any species shift
within the
Penicillium
species is not possible.
Effect of intensive, high efficiency vacuum
cleaning
In the short term, there was an overall increase in fungal
genera/biodiversity following the first vacuum cleaning
intervention, which is consistent with higher recorded
fungal spore counts. The higher fungal levels and fungal
genera isolated during the first vacuuming period are
due to the initial increased activity and intensive
mechanical action (rotating brush) of the vacuuming
cleaning process, stirring up and resuspending dust and
particulates from deep within the carpet (Gorny
et al.
,
2001; Figley
et al
, 1993; Dybendal
et al.
, 1991; Kemp
et al
,
1998). Studies by the Canadian Mortgage and Housing
Corporation (CMHC) (2003) and Fugler (2004) found
that regardless of whether HEPA filtration was available,
simply operating the vacuum cleaner resulted in
significantly raised dust levels during the start up phase
of a clean up. We suggest that the initial increase in
fungal biodiversity and numbers was due to the initial
high loadings contained within the carpet. As the
loadings contained in the carpet were reduced, so too
does the amount available for resuspension is reduced.
Prior to the intensive vacuuming intervention, the
carpet fibres are flat and horizontal, trapping dust,
particulates and fungi deep in the carpet pile.
Conventional vacuum cleaners, which rely on moving
air alone, do not effectively remove deeply embedded
dirt and particulates due to the difficulty in creating
sufficient velocity and air flow required to motivate and
agitate the particulates. Cleaning with a vacuum not
equipped with a rotating brush head, HEPA filters,
sufficient suction and dwell time (surface vacuuming
time) results in only superficial and visible dust and
particulates being removed from the surface of the
carpet pile. This still leaves a significant amount of
heavier and fine particulates, including fungi, trapped
deep within the carpet pile.
These smaller particles are difficult to dislodge from the
carpet pile due to the electrical attraction
JEHR - vol4 iss1.qxd 8/4/05 3:49 pm Page 10
11
Journal of Environmental Health Research, Volume 4, Issue 1, 2005
Reducing airborne indoor fungi and fine particulates in carpeted homes
(electrostatic, van der Waals, geometric factors)
between the fibres of the carpets and the adhesive
forces of these particles (Braun
et al.
, 2002). Vincent
(1995) and Hinds (1982) put forward that the adhesive
forces are proportional to the particle diameter (
d
);
while the removal forces are proportional to the particle
mass (
d3
) for vibration and detachment by air currents
is proportional to the exposed surface area of the
particle (
d2
). As the size of the particles decreases, the
more difficult it is to detach them from surfaces. Hinds
(1982) determined that about 10 times as much force is
required to remove 98% of the particles as that required
to remove 50%, which explains why it is easier to remove
larger particles from a surface than smaller ones. This
was similarly observed in studies by Nishioka et al.
(1999) and Braun et al. (2002).
Further to this discussion, Varekhov (1994) and Jenning
& Lysek (2001) found that under certain external
conditions, certain fungal spores are able to adhere to
surfaces and create a unique microclimate via the
growth of fungal hyphae and the expansion of fungal
mycelium. To enhance their ability to survive and
compete with other species, fungi are able to create
unique microhabitats within their immediate settled
surroundings, and establish the ideal moisture content
and pH levels around the fungal hyphae tip (apical
growth zone), creating an ‘encrusted’ area, thereby
maximising their growth potential and competitiveness.
Sheltered and attached within the carpet fibres, fungal
spores have an ideal environment for growth, with
readily available nutrients from dust and debris. The
combination of the electrical attraction and physical
attachments creates a situation whereby the removal of
fungi from carpet fibres is particularly difficult. The
physical and mechanical action of the rotating vacuum
cleaner brushes (or similar type devices) is therefore
vital in breaking the adherence forces and physical
attachments of the hyphae and mycelium, and
effectively removing fungi and particulates from the
carpet fibres.
The vacuum cleaning intervention conducted in the
vacuum homes utilised a combination of high efficiency
HEPA vacuums, mechanical rotating brush head and
sufficient dwell time (2-4 mins m
-2
) to effectively remove
not only visible surface particulates but also those
deeply imbedded in the carpet pile. Except for central
vacuum systems with external exhausts, the same air
being vacuumed into the vacuum cleaner is recirculated
back into the environment. HEPA filters have an
efficiency rating of 99.97% and effectively remove fine
particulates, which would normally have passed
through conventional bag, cloth, and paper filters. The
mechanical rotating brush heads revolve at very high
speeds, agitating the carpet fibres, effectively loosening
dirt deeply embedded in the carpet pile and aiding in
its removal. A sufficient dwell time is also important as
the increased time spent on the surface of the carpet
aids the suction from the motor, pulling the carpet
under the nozzle and bowing it backward slightly.
Studies by Fugler (2004) and CHMC (2003) yielded a
90% recovery of deposited dust if the vacuum cleaner
was passed over an area 10 times the normal number of
passes. The increased number of passes and the
accumulated dwell time, aids in the separation of the
nap of the carpet and enhances airflow through the
carpet fibres (Ristenbatt, 2004).
Continual maintenance of the carpet with intensive,
high efficiency HEPA vacuum cleaning in the long term
results in more and more of the deeply imbedded dust,
particulates and fungi being removed from the
environment. These are therefore not available for
resuspension into the air and therefore decreased
exposure by occupants in the indoor environment, as
the loadings in the carpet pile were reduced. In our
study, both airborne particulate and indoor fungi levels
eventually showed reductions in the long term as
previous dust and fungi available for resuspension, was
effectively reduced, reflecting results similarly found by
Fugler (2004) and CHMC (2003). A well-maintained
carpet (low loadings) could serve as a filter for incoming
particulates, trapping and holding particulates and
fungi within the carpet fibres until they are removed
during the next vacuuming occasion.
Activity vs non-activity sampling (I:A ratios)
Although many studies recognise outdoor air as a major
contributor to indoor levels of fungi, not all indoor
fungi found indoors can be attributed to outdoor air
(Verhoeff et al., 1992; Fradkin
et al.
, 1987; Solomon,
1975). In cases where the outdoor air is not the source
of indoor fungi, other fungal sources inside the
building need to be investigated. However, in many
situations, there are often no obvious indoor fungal
colonisation (visible/hidden mould) and no obvious
indoor sources (Lehtonen, 1993).
Settled spores present on hard and soft surfaces in the
indoor environment may become resuspended by air
movement caused by various activities including human
disturbance (walking, cleaning, foot traffic, etc.), or by
environmental changes such as changes in air humidity
and wind gusts (Ferro et al, 2002; Long
et al.
, 2000;
CMHC, 1999; Flannigan & Hunter, 1998; Lehtonen
et al
,
1993; Pasanen
et al.
, 1991; Hunter
et al.
, 1988; Hirsch &
Kozak
et al.
, 1979; Hirsch & Sosman, 1976). Fungal spores
and fine particulates can remain airborne for long
periods and are subject to drift throughout the home.
They can adhere to vertical surfaces (walls) and settle on
horizontal surfaces (finished furniture and smooth
floors). In addition, these spores and particulates can be
transferred on clothing to other places within and
between homes and to schools or workplaces where they
can be inhaled, thereby contributing to respiratory
symptoms (Lioy
et al.
, 1999; Ferro, 2000).
Several studies have since shown that human activity has
a significant effect on the concentrations of micro-
organisms isolated during sampling (Buttner &
Stetzenbach, 1993; Greene
et al.
, 1962). The methodology
used in this study to simulate activity/impaction was a
simple, cheap and readily accessible technique that
consistently produced higher concentrations of airborne
viable spores (Cheong
et al.
, 2004).
JEHR - vol4 iss1.qxd 8/4/05 3:49 pm Page 11
12 Journal of Environmental Health Research, Volume 4, Issue 1, 2005
Cedric D. Cheong and Dr Heike G. Neumeister-Kemp
Direct comparison of the control and vacuum homes
suggests that the vacuum cleaning intervention
although initially resulting in increased exposure to
fungi, in the long term resulted in reduced levels of
fungi indoors. Whereas fungal composition in the
control homes varied with outdoor air and infiltration,
in the vacuum homes fungal composition remained the
same. Continual maintenance of the carpet ensures
incoming outdoor fungal sources are continually
removed, therefore maintaining a stable fungal spora
within the indoor environment.
Conclusion
The intensive, high efficiency HEPA vacuum cleaning
intervention was effective in keeping levels of indoor
fine particulates at a stable and lower level than
outdoors. There was an initial increase in fungal levels,
due to the initial loadings present in the carpets. After
the first vacuum cleaning intervention, consistent
reductions in airborne fungal and particulate levels
were observed. Penicillium, Cladosporium and yeasts were
the most common and widespread fungi recovered
indoors and outdoors. Fungal range increased in the
vacuum homes whereas it remained the same in the
control homes. It is suggested that fungal sampling be
undertaken under ambient no activity and simulated
activity/impaction conditions to give a better
indication of the influence indoor sources have on
fungal levels.
Intensive high efficiency HEPA vacuuming benefits the
indoor environment by maintaining not only
established fungal levels indoors but also a stable
indoor fungal spora. A well maintained carpet could
serve as a filter for incoming particulates, trapping and
holding particulates and fungi within the carpet fibres
until they are removed during the next vacuuming
occasion. Continual maintenance of the carpet ensures
incoming fungal sources are continually removed
(loadings kept low), therefore maintaining a stable
fungal spora within the indoor environment, in terms of
numbers and composition.
It is suggested that in future studies, a physical and
biological comparison of dust loadings extracted
from within the carpet, with that of airborne levels,
should be conducted to further investigate the
relationship between the carpet loadings and
cleaning activity.
Acknowledgments
The authors would like to thank Kevin White, Jane
Jones, Scott Smith, Rita Tan and Joanne Nastov for their
assistance in the field. In particular, the authors are
indebted to Dr Peter Dingle for his valuable support
and academic contributions in the editing of this
manuscript and encouragement throughout this study.
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