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Large amounts of airborne microorganisms are emitted from livestock production. These emitted microorganisms may associate with dust, and are suspected to pose a risk of airborne infection to humans in vicinity and to animals on other farms. However, the extent to which airborne transmission may play a role in the epidemic, and how dust acts as a carrier of microorganisms in the transmission processes is unknown. The authors present the current knowledge of the entire process of airborne transmission of microorganisms—from suspension and transportation until deposition and infection—and their relation to dust. The sampling and the mitigation techniques of airborne microorganisms and dust in livestock production systems are introduced as well.
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Airborne Microorganisms From Livestock
Production Systems and Their Relation
to Dust
Yang Zhao
, AndrÉ J. A. Aarnink
, Mart C. M. De Jong
& Peter W.
G. Groot Koerkamp
Wageningen UR Livestock Research, Lelystad, the Netherlands
Department of Agricultural and Biosystems EngineeringIowa State
University, Ames, IA, USA
Quantitative Veterinary Epidemiology, Wageningen University,
Wageningen, the Netherlands
Farm Technology Group, Wageningen University, Wageningen, the
Accepted author version posted online: 28 Aug 2013.Published
online: 16 Apr 2014.
To cite this article: Yang Zhao, AndrÉ J. A. Aarnink, Mart C. M. De Jong & Peter W. G. Groot
Koerkamp (2014) Airborne Microorganisms From Livestock Production Systems and Their Relation
to Dust, Critical Reviews in Environmental Science and Technology, 44:10, 1071-1128, DOI:
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Critical Reviews in Environmental Science and Technology, 44:1071–1128, 2014
Copyright © Taylor & Francis Group, LLC
ISSN: 1064-3389 print / 1547-6537 online
DOI: 10.1080/10643389.2012.746064
Airborne Microorganisms From Livestock
Production Systems and Their Relation to Dust
Wageningen UR Livestock Research, Lelystad, the Netherlands
Department of Agricultural and Biosystems Engineering, Iowa State University,
Ames, IA, USA
Quantitative Veterinary Epidemiology, Wageningen University, Wageningen,
the Netherlands
Farm Technology Group, Wageningen University, Wageningen, the Netherlands
Large amounts of airborne microorganisms are emitted from live-
stock production. These emitted microorganisms may associate with
dust, and are suspected to pose a risk of airborne infection to hu-
mans in vicinity and to animals on other farms. However, the
extent to which airborne transmission may play a role in the epi-
demic, and how dust acts as a carrier of microorganisms in the
transmission processes is unknown. The authors present the cur-
rent knowledge of the entire process of airborne transmission of
microorganisms—from suspension and transportation until depo-
sition and infection—and their relation to dust. The sampling and
the mitigation techniques of airborne microorganisms and dust in
livestock production systems are introduced as well.
KEY WORDS: agriculture, airborne transmission, dust, livestock,
microorganisms, production
Pathogenic microorganisms may occur in high concentrations in the air in-
side the livestock houses. Along with ventilation, they can be emitted to the
ambient environment and pose airborne infection risk to healthy animals
on other farms and to humans living in the vicinity (Seedorf et al., 1998).
Address correspondence to Andr
e J. A. Aarnink, Wageningen UR Livestock Research,
P.O. Box 65, 8200 AB Lelystad, the Netherlands. E-mail:
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1072 Y. Zhao et al.
The extent to which pathogenic microorganisms are transmitted to nearby
recipients and cause disease spreading through the airborne route remains
largely unclear. Actually, airborne transmission only has been considered as
a possible route in historical disease outbreaks in livestock production when
the outbreaks could not be attributed to other known routes such as direct
contact transmission or fecal-oral transmission (Elbers et al., 2001; Gloster
et al., 2003). Attempts to link pathogen transmission (between farms) to
prevalent wind directions—an apparent epidemiological proof of airborne
transmission—have not been always successful, and the transmission is as-
sumed to only be favored at picky atmospheric conditions (Gloster et al.,
2003; Mikkelsen et al., 2003). All these facts induce doubts on the impor-
tance of the role of airborne transmission in disease outbreaks; however, no
one can conclusively exclude this transmission route due to its potentially
extensive and intensive impacts if truly involved in epidemics.
Given the lack of knowledge on airborne transmission it is important
to stimulate relevant research in order to better understand what role it can
play. Here we define airborne transmission in livestock production as “an
entire transmission process that involves pathogenic microorganisms releas-
ing from the infected animal’s excrement or secretion to air, transporting
air, inhaled by a healthy animal, and eventually infecting the recipient.” The
airborne transmission of certain pathogenic microorganisms from animal to
animal has been demonstrated in lab-scale experiments in which healthy
animals separated physically but not aerially from infected animals became
infected (Berthelot-Herault et al., 2001; Brockmeier and Lager, 2002). Fur-
thermore, some microorganisms collected kilometers away from the source
farm were found to be capable of infecting healthy animals intramuscularly
or intratracheally (Otake et al., 2010). However, there is still uncertainty,
because of the incomplete knowledge about the entire process of airborne
transmission of microorganisms, from generation and transportation through
inhalation and finally to infection (Stark, 1999).
Dust probably plays a role as the carrier of the microorganisms in the
air. In 1987, the importance of the relationship between airborne microor-
ganisms and dust from livestock production systems was reviewed by Muller
and Wieser (1987). The authors separately described the indoor properties
(source, concentration, and constitute) of airborne microorganisms and dust,
and the dispersion in ambient air outdoors. Since then, much research has
been done on specific processes involved in the transmission of the air-
borne microorganisms and dust. However, we lack an integrated overview
of and insight into all the processes involved in the airborne transmission of
microorganisms in association with dust.
The objective of this article is to review current knowledge on air-
borne microorganisms from production systems for typical livestock species
(swine, poultry and cattle), and their relation to dust. Specifically, in section
2, we identify the sources, species, size distributions, and concentrations of
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Airborne Microorganisms and Dust in Livestock Houses 1073
airborne microorganisms and dust from livestock production systems, as well
as the factors affecting their concentrations. In section 3, the physical and
biological decay of airborne microorganisms and dust during transmission
is described. In section 4, the deposition of airborne microorganisms and
dust in respiratory tracts, and the infective dose of pathogenic microorgan-
isms to animals are introduced. In section 5, the strategies and techniques
for sampling microorganisms and dust in livestock production systems are
proposed. In section 6, the mitigation techniques are described.
2.1 Identification the Sources of Airborne Microorganisms and Dust
Identifying the source of microorganisms and dust in livestock production
systems helps to elucidate how airborne transmission is generated, and ul-
timately can help to develop and implement strategies that prevent such
transmission from beginning (Bull et al., 2006; Cambra-Lopez, 2010). Sources
of dust in livestock production systems have been identified and assessed
qualitatively and quantitatively (Aarnink et al., 1999; Donham and Gustafson,
1982). It is generally accepted that all dust sources are also sources of air-
borne microorganisms because these source materials somehow contain cer-
tain microbial species that may be generated together with dust. However,
the source identification of airborne microorganisms has not yet been exten-
sively investigated, and it is thought to be more complicated than the source
identification of dust in at least two ways. The first way is associated with
the complexity of microbial species in a source. A source material always
contains a microbial flora composed of many different microbial species.
The second way is associated with the dynamic viability of microorganisms
in the generation process (Milne et al., 1989); microorganisms may either
decay or multiply in the source material. Thus, the source identification for
microorganisms should also be dynamic.
Animals shed microorganisms mainly by means of fecal excretion, which
may contain large amount of microorganisms (Letellier et al., 1999; Pell,
1997). Consider two common zoonotic bacterial species, Salmonella and Es-
cherichia, both have been found in feces: Salmonella at a concentration of
2–7 log CFU g
feces (Gray and Fedorka-Cray, 2001; Himathongkham et al.,
1999) and E. coli at 2–6 log CFU g
feces (McGee et al., 2001; Omisakin
et al., 2003). Feces are also an important pathway for virus shedding from
infected animals (Fouchier et al., 2003). A list of viral species that may be
excreted by cattle was proposed by Pell (1997), including infectious bovine
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1074 Y. Zhao et al.
rhinotracheitis and Foot-and-mouth disease (FMD) virus. Many other viruses
have been recovered from feces of other animal species, such as avian in-
fluenza A virus (Webster et al., 1978) and Newcastle disease v irus (Spradbrow
et al., 1988) in poultry, and swine fever virus (Van Oirschot, 1979), hepati-
tis E virus (de Deus et al., 2007), and porcine reproductive and respiratory
syndrome virus (PRRSV) (Yoon et al., 1993) in pigs. The microorganisms in
feces can become airborne when dried fecal particles are disturbed by air
flow or animal activity. Some studies have managed to identify feces as the
source of airborne microorganisms. A study by Duan et al. (2009) found
the airborne E. coli strains inside and downwind from the pig houses were
closely associated with those isolated from pig feces. Water content binds
particles in feces and prevents their suspension, so, the microorganisms in
dry feces that have low water content become airborne more easily than
microorganisms in fresh feces. The water content of fresh feces (or manure,
when urine is not separated) is the range of 60–90% (Derikx et al., 1994),
depending on the animal species. Under typical livestock housing environ-
mental conditions, it may take hours or days to dry the feces to a water
content less than 20%—the water content of airborne dust in livestock pro-
duction systems (Aarnink et al., 1999; Zhao et al., 2013). This means the
microorganisms must undergo a latent period between the moment they are
excreted in the feces and the moment they become airborne.
During inhalation and exhalation the surface of the mucus in the res-
piratory tract is destabilized through an interplay between surface tension
and viscous forces (Edwards et al., 2004). This can result in mucus’s mi-
croorganisms to become airborne and expelled from the body via breathing,
coughing, and sneezing. This source of airborne microorganisms is widely
accepted in the human model of disease transmission, and pathogenic mi-
croorganisms have been frequently recovered from the exhaled aerosols
(Fabian et al., 2008; Weber and Stilianakis, 2008). Only a few studies have
been carried out to directly detect the microorganisms in exhaled air of an-
imals. By sampling exhaled air in masks placed over the heads of infected
pigs, Cho et al. (2006) recovered PRRSV and Hermann et al. (2008) recov-
ered Mycoplasma hyopneumoniae and Bordetella bronchiseptica. In contrast,
Hermann et al. (2008) failed in recovering PRRSV, Porcine circovirus 2, swine
influenza virus, and Porcine respiratory coronavirus in the exhaled air of in-
fected pigs, although they were found in the oral and nasal swabs. Similarly,
Zhao et al. (2013) could not recover infectious brusal disease virus in the
exhaled air of infected broilers. These results indicate that some microorgan-
isms in animal respiratory tracts might not readily become suspended in the
air or be expelled out of the body, which implies that this is perhaps not an
major source of airborne microorganisms as compared to animal feces (Zhao
et al., 2013). However, the reason the microorganisms may not be detected
could be because the quantities of exhaled microorganisms were below the
detection limit of the sampling devices. Therefore, animal respiratory tracts
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Airborne Microorganisms and Dust in Livestock Houses 1075
can only be excluded as a source of airborne microorganisms until it
has been incontrovertibly established that every single microorganism is
Organic materials such as feed may serve as carriers for variety of
microorganisms. The microorganisms may originate from the soil and are
transferred to standing crops by wind, rain, mechanical agitation, or insects
(Maciorowski et al., 2007). Both nonpathogenic and pathogenic microorgan-
isms have been recovered from feed; analysis has revealed concentrations
of Gram-negative bacteria in feed as high as 5 log CFU g
(Hofacre et al.,
2001). These microorganisms can be disseminated together with feed parti-
cles during feeding (Andersson et al., 1999; Chang et al., 2001); the extent
of dissemination depends greatly on how the feed is given (e.g., dry vs. wet
feed delivery and powder vs. pellet feed delivery; Pearson and Sharples,
Litter is a mixture of bedding materials (e.g., wood shavings, chopped
straw, sawdust, and rice hulls) animal feces, dander, and feed (Torok et al.,
2009). The provision of litter in livestock production systems may improve
animal welfare by increasing the incidence of natural behaviors (Appleby
and Hughes, 1991), which, however, may result in more microorganisms
being present in the air than in housing systems without litter (Madelin and
Wathes, 1989; Vucemilo et al., 2007). The microorganisms arrive in litter
during the harvesting and processing of the bedding material, and through
animal excretion and secretion. The concentrations of aerobic bacteria in
poultry litter range from 3 to 9 log CFU g
(Lu et al., 2003; Martin et al.,
1998). Most of the bacteria in the poultry litter are Gram-positive. Gram-
negative bacteria and mold account for a small fraction of the total microbial
count, but due to the high concentration of the total microorganisms, their
numbers can still be high in some cases (Martin et al., 1998). Surprisingly,
some pathogenic bacteria that are commonly recovered from animal feces
(e.g., E. coli, Salmonella,andCampylobacter) are not always detectable in
litter (Lu et al., 2003). The reason could be the less favorable microenviron-
ment for microbial survival in the feces-bedding mixture than in feces alone.
Microorganisms, including Globicatella sulfidofaciens, Corynebacterium am-
moniagenes, Corynebacterium urealyticum, Clostridium aminovalericum,
Arthrobacter sp.,andDenitrobacter permanens, which may be involved in
degradation of wood and cycling of nitrogen and sulfur have been identified
in poultry litter (Lu et al., 2003).
Other possible sources of airborne microorganisms in livestock houses
include animal skin (Baird-Parker, 1962; Gailiunas and Cottral, 1966;
Kloos et al., 1976) and animal products (e.g., broken eggs, spoiled milk
(de Reu et al., 2008; Donaldson et al., 1983; Doyle, 1984; Doyle and
Roman, 1982), farm workers and visitors (Newell and Fearnley, 2003;
Nishiguchi et al., 2007), and ambient air (Gloster et al., 2003; Martin et al.,
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1076 Y. Zhao et al.
TABLE 1. Sources of airborne dust in animal houses
Animal Housing type Source Contribution Reference
Layers Floor housing with
Bedding material in
55–68% (Muller and
Feathers 2–12% 1987)
Excrement 2–8%
Layers Battery housing Feed 80–90% (Muller and
Wieser, 1987)
Feathers 4–12%
Excrement 2–8%
Broilers Floor housing with
Feathers >10% (Aarnink et al.,
Crystalline dust >10%
Feed, microorganisms <1%
Partially slatted
Feed >10% (Aarnink et al.,
Skin particles >10%
Feces, crystalline dust 1–3%
Sources of airborne dust include feed, animal skin and feather debris, feces,
litter, microorganisms, pollen, and insect parts (Aarnink et al., 1999; Donham
et al., 1986). The contribution of these sources to airborne dust varies, de-
pending on the animal species and the housing system. Heber et al. (1988a)
reported that the main source of airborne dust in pig houses was feed, which
is consistent with the findings of Donham et al. (1986) and Aarnink et al.
(1999). Muller and Wieser (1987) found that 55–68% of the airborne dust in
floor layer systems with litter originated from the bedding materials in litter,
while 80–90% of the airborne dust in layer systems with battery system orig-
inated from feedstuff (Table 1). In floor systems with wood shavings as litter
for three-week old broilers, Aarnink et al. (1999) found that airborne dust
mainly (>10%) originated from down feathers and urine components. The
contribution of feed to the airborne dust largely depends on its composition
and how it has been processed (Pearson and Sharples, 1995M; e.g., crumbles
or pellets). The contribution of feces is probably related to the housing sys-
tem (e.g., with or without litter [straw bedding vs. liquid manure]). Table 1
lists the main sources of dust and gives an estimation of their contributions.
2.2 Species of Airborne Microorganisms
A large fraction of the airborne microorganisms in livestock production sys-
tems are bacteria, of which the most dominant are Gram-positive bacteria,
accounting for approximately 90% of the bacterial flora (Zucker et al., 2000).
The most common species of these Gram-positive bacteria are Staphylo-
coccus, Streptococcus,andEnterococci (Clark et al., 1983; Hartung, 1992;
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Airborne Microorganisms and Dust in Livestock Houses 1077
Matkovic et al., 2007). The Gram-negative bacteria account for only a small
fraction of airborne bacteria (Zucker et al., 2000). Bakutis et al. (2004) re-
ported that in terms of the total bacterial count, the proportion of Gram-
negative bacteria was approximately 10% in cattle houses, 4.9% in pig houses,
and 2.6% in poultry houses. Zucker et al. (2000) found that the airborne
Gram-negative bacteria in pig and cattle houses were aerobic and include
Enterobacteriaceae, Pseudomonadaceae,andNeisseriaceae; no culturable
obligate anaerobic Gram-negative bacteria were isolated. Possible reasons
for the smaller proportion of airborne Gram-negative bacteria in livestock
production systems are that their excretion by animals is less than their
counterparts and these bacteria are more vulnerable to environmental stress
such as oxidation, radiation, and dehydration, probably because of their
thinner cell walls (Pal et al., 2007; Theunissen et al., 1993). The proportion
of fungi, molds, and yeasts in the airborne microbial flora in animal houses
is low (Hartung, 1992; Lee et al., 2006). The most frequently reported fungi
in poultry, pig, and dairy houses are Aspergillus sp., Alternaria sp., Cladospo-
rium sp., Penicillium sp., Fusarium sp., Scopulariopsis sp., and yeast (Chang
et al., 2001; Cormier et al., 1990; Martin et al., 1996; Matkovic et al., 2007;
Vittal and Rasool, 1995; Wilson et al., 2002).
2.3 Size Distribution of Airborne Microorganisms and Dust
The size of an airborne particle determines its transportation, sedimenta-
tion, and resuspension, as well as its deposition in the respiratory tracts
of recipients. Investigations of the size distribution of microorganisms and
dust in livestock production systems may provide a useful overview of their
quantitative importance, indicate the health risk for human and animals, and
facilitate the establishment and evaluation of control techniques.
According to interests by different scientific sectors, sizes of airborne
particles are differently categorized. For concerns in occupational health,
particle sizes are categorized into three categories: inhalable ( <100 μm),
thoracic (<10 μm), and respirable (<4 μmor5μm; Cambra-Lopez et al.,
2010; Curtis et al., 1975; Madelin and Wathes, 1989; Zhang, 2004). In en-
vironmental science, recent research is increasingly focusing on dust with
aerodynamic diameter smaller than 10 μm(PM
) and 2.5 μm(PM
). The
size distribution of airborne dust has been expressed either in mass or in
Zhao et al. (2011a) found that in three pig houses about 73–95% of the
airborne bacteria were in the nonrespirable range (Figure 1). A similar result
was reported by Curtis et al. (1975): nonrespirable bacteria accounted for
approximately 78–89% of the airborne bacteria in pig houses. The size distri-
bution of microorganisms in poultry houses depends on the type of housing
system. In broiler rooms with wood-shaving litter, most of the bacteria were
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1078 Y. Zhao et al.
FIGURE 1. Size distribution of airborne bacteria in the exhaust air from three commercial
fattening pig houses measured with an Andersen Six Stage viable bioaerosol sampler (Zhao
et al., 2011a).
nonrespirable in the full life cycle of broilers (eight weeks); a similar distri-
bution pattern was found in broiler rooms with raised netting floor only after
the birds were older than six weeks. When the birds were two to five weeks
old, the proportions of airborne respirable and nonrespirable bacteria were
similar (Madelin and Wathes, 1989).
Heber et al. (1988a) reported that nonrespirable particles (>4 μm) in
pig houses accounted for more than 80% in mass, but less than 30% in terms
of count. Expressed as percentage of total dust, Lai et al. (2010) found the
mass of PM
was 30–54% in pig houses, 41–69% in poultry houses, and 36%
in cattle houses. In all three types of house, PM
count was more than 99%
of the total dust. The equivalent figures for PM
mass were 1–3% in pig
houses, 2–8% in poultry houses (2009), and 5% in cattle houses. For PM
counts the figures were 90–99% in pig houses, 88–92% in poultry houses
and 99% in cattle houses. The difference in the mass and numeric size
distribution is caused by the fact that small dust particles contribute little to
That more microorganisms and less dust particles are found in the non-
respirable range indicates that a nonrespirable dust particle is more likely
to be loaded with microorganisms than a respirable one. This is a reason-
able hypothesis, because the larger a particle is, the greater the chance it
may contain microorganisms. Nowadays, the size distribution of airborne
microorganisms is normally determined with the Andersen stage impactor
(Andersen, 1958; Zhao et al., 2011a). This sampler actually gives the counts
of particles (in seven different size ranges) that contain microorganisms. In
some cases, for instance a biosecurity assessment for occupational health, it
is more important to quantify the individual microorganism in the collected
particles rather than the microbial-containing particles themselves, because
the former will give a better idea of the risk of infection. For this purpose,
predetachment of microorganisms from dust particles (Zhao et al., 2011b) or
visually microbiological counting techniques (Yamaguchi et al., 2012) may
be required.
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Airborne Microorganisms and Dust in Livestock Houses 1079
TABLE 2. Concentrations of airborne microorganisms and dust in livestock production
Inhalable Dust
Respirable Dust
Animal log CFU m
log CFU m
mg m
mg m
mg m
mg m
Broiler 6.4 4–5 3.8–10.4 0.42–1.14 0.9–2.4 0.04–0.09
Layer 4–5 3–4 1.0–8.8 0.03–1.26 5.9–6.1 0.25–0.29
Pig 5.1 3.7 0.6–5.1 0.09–0.46 0.2–2.0 0.01–0.07
Cattle 4.3 3.8 0.1–1.2 0.03–0.17 0.1 0.01
Data from Seedorf et al. (1998).
Data from Taikai et al.(1998).
Data from Lai et al. (2010).
2.4 Concentrations of Airborne Microorganism and Dust
Concentrations of airborne microorganisms and dust in livestock produc-
tion systems have been investigated in previous studies (Kim et al., 2008;
Radon et al., 2002; Zhao et al., 2011a). Due to the huge spatial and temporal
variations in microorganism and dust concentrations and the difference in
sampling techniques used, it is difficult to compare the data between studies.
So far, the studies by Seedorf et al. (1998) and Takai et al. (1998) still provide
the most representative concentration data on microorganisms and dust in
livestock production systems, and sampling methods were detailed in the
publications by Phillips et al. (1998) and Wathes et al. (1998). These data are
summarized in Table 2, together with the PM
and PM
concentration mea-
sured by Lai et al. (2010). For microorganisms, the highest concentrations
of airborne bacteria and fungi were found in broiler houses. The concentra-
tions found in layer, pig and cattle houses were lower than those in broiler
houses, but still much higher than those in ambient air (Wang et al., 2010).
For dust, the highest dust concentrations were found in poultry houses, and
the lowest dust concentrations were in cattle houses.
2.5 Factors Affecting Concentrations of Airborne Microorganisms
The concentrations of airborne microorganisms and dust in animal houses
are affected by animal, housing system and management. In this section,
these factors are discussed separately, but one should realize that these
factors always interactively affect the concentration because they are inter-
correlated. For instance, animal activity is associated with animal age, weight,
and light schedule, and ventilation rate is affected by outdoor and set-point
temperature, humidity, and animal species and age.
2.5.1 ANIMAL
The animal factor can be further detailed into subfactors such as age, weight,
activity, and stocking density. The concentrations of airborne microorgan-
isms and dust generally increase concomitantly with animal age and weight
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1080 Y. Zhao et al.
(Hinz and Linke, 1998; Predicala et al., 2001; Yoder and Van Wicklen, 1988).
However, an inverse relationship has also been found. Madelin and Wathes
(1989) found a decrease of microorganisms and dust concentrations in the
late fattening period of broilers. A similar result was reported by Saleh et al.
(2005). The decrease in concentration of microorganisms and dust is prob-
ably because the older broilers occupied all the floor space, which limited
their activity.
In general, higher concentrations of bacteria, fungi, and dust are mea-
sured when the animals are more active, as can be inferred from the finding
that their concentrations were higher in day time than at night (Seedorf et al.,
1998; Takai et al., 1998). Image and infrared technology allows animal activ-
ity to be automatically detected (Gloster et al., 2007; Pedersen and Pedersen,
1995). Using an infrared detector, Haeussermann et al. (2007) demonstrated
that the indoor concentrations of PM
were associated with pig activity. A
similar study by Heber et al. (2006) showed that both total dust and PM
were correlated with the pig activity. However, Gloster et al. (2007) failed to
establish the correlation between the concentration of airborne FMD virus
and pig activity quantified by taking sequential pictures. The reason is not
clear, but the authors explained that the virus production appears to be more
closely associated with other factors (e.g., physiological symptoms; Gloster
et al., 2007). Hardly any other information is available on the relation be-
tween quantified animal activity and concentrations of microorganisms.
Compared to a cage system, an aviary system contained higher concentra-
tions of microorganisms (de Reu et al., 2005) and dust (Appleby and Hughes,
1991). This is because in an aviary system, laying hens have more scopes for
moving horizontally and vertically and perform dust bathing behavior in the
litter. Housing systems with bedded floors caused more air quality problems,
although such housing systems are generally thought to be more beneficial
for animal welfare (Kim et al., 2008; Madelin and Wathes, 1989; Quarles
et al., 1970). The type of bedding material also affects the concentration of
microorganisms in the air. For instance, in broiler houses, straw bedding re-
leased less bacteria in the air than wood shavings did (Banhazi et al., 2008a).
The authors argued that this was probably because wood shavings provided
a better microenvironment for bacteria viability and multiplication.
Comparisons of dust concentrations between natural and mechanical
ventilation systems showed that with mechanical ventilation, less respirable
(Phillips, 1986) and total dust was found in pig houses (Chiba et al., 1985) and
there was less total dust in turkey houses (Janni and Redig, 1986). By contrast,
concentrations of total bacteria and fungi were lower in naturally ventilated
pig houses without bedding materials (deep-pit manure system with slats,
and manure removal system by scraper) than in mechanically ventilated
houses. The contradictory results found for the effect of type of ventilation
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Airborne Microorganisms and Dust in Livestock Houses 1081
(natural or mechanical) on microorganisms and dust are not fully understood,
but it seems likely that the situations (including the management) of the
ventilation systems vary between the different studies, making the data less
Feed management may play an important role in dust concentration in live-
stock production systems. Previous studies have shown that dust concentra-
tions were reduced by giving pelleted feed rather than powdered feed, wet
feed rather than dry feed, and coated feed rather than uncoated feed (Clark
and McQuitty, 1988; Pearson and Sharples, 1995; Zeitler et al., 1987). The
effect of feeding management on airborne microorganism concentration has
not been extensively studied.
Maintaining good hygiene in livestock production systems may help to
improve the air quality with respect to microorganisms and dust. For in-
stance, cleaning (e.g., removing litter, scrubbing surfaces, and disinfecting
the house) between two production circles may reduce both airborne mi-
croorganisms and dust (Banhazi et al., 2008a). Investigations of the relation
between hygiene and air quality have found they are not always positively
correlated. Duchaine et al. (2000) reported that a housing system that ap-
peared cleaner contained more airborne bacteria than one that appeared
dirtier. The probable explanation is that houses with more settled dust on
the surfaces are more readily ranked as dirtier, but dust accumulated on
surfaces is not an appropriate indicator of the concentration of bacteria in
the air.
Ventilation management (e.g., adjusting the rate at which indoor air is
exchanged with outdoor air by mechanical ventilation systems) is to control
the temperature and other aerial variables such as humidity and gas con-
centrations inside livestock houses. Previous studies have shown that lower
concentrations of microorganisms and dust can be achieved by increasing
the ventilation rate in livestock production systems (Duchaine et al., 2000;
Hinz and Linke, 1998; Kim et al., 2007b). However, a nonsignificant correla-
tion between these variables has also been reported in livestock production
systems (Banhazi et al., 2008b; Seedorf et al., 1998). The probable reason for
these contradictory findings is that ventilation affects the concentration of mi-
croorganisms and dust in two ways: by exhausting airborne microorganisms
and dust to outdoors through air exchange, thereby reducing their indoor
concentrations, and by producing airflow turbulence above surfaces, agitat-
ing the particles and causing them to suspend in the air, thus compromising
the removal effect. Smaller airborne particles seem to be more effectively
removed from livestock houses by ventilation than bigger particles (Kuehn,
1988) because they are readily transported in the air streams.
A high relative humidity in the air reduced the dust concentration in
livestock production systems (Guarino et al., 1999). In humid environments,
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1082 Y. Zhao et al.
the dust particles bind to the surface and are not easily suspended, and
those in the air aggregate and to settle faster (Heber et al., 1988b; Takai
et al., 1998). In contrast, humidity seems not to affect the concentrations
of total and Gram-negative bacteria (Attwood et al., 1987; Banhazi et al.,
2008b; Nicks et al., 1993). A high humidity favors survival and/or multiplica-
tion of dehydration-sensitive microbial species in the sources (de Rezende
et al., 2001), which might trade off the physical settlement of airborne mi-
croorganisms. Experimental validation of this hypothesis is of importance,
because it may strengthen the understanding of the interaction between
airborne microorganism concentration and air humidity. This will help to
formulate effective air humidification strategies for reducing both, dust and
microorganisms, instead of achieving one by compromising the other. This
information will also be valuable for understanding the bioenvironment in
livestock houses where air humidification (e.g., water spray and evapora-
tion cooling pad) is used to ameliorate animal heat stress in summer time
(Brown-Brandl et al., 2010; Tao and Xin, 2003).
Indoor temperature management is well regulated for the poultry and
pig industries, to optimize productivity. Al Homidan et al. (1997) reported
that the total dust in broiler rooms increased when the temperature was
set 2
C above the recommended level. The correlation between dust con-
centration and temperature reverses from positive to negative when the
temperature is extremely high, apparently because animal activity decreases
at high temperature and thus fewer particles from surfaces are disturbed
and suspended (Donkoh, 1989; Guarino et al., 1999; Wylie et al., 2001). As
well, a high temperature triggers a series of events that may affect the dust
concentrations in livestock production systems, such as increasing the ven-
tilation rate and activating wet cooling systems (Simmons and Lott, 1996).
Although some researchers (Banhazi et al., 2008a) have suggested there is
a relation between the concentration of microorganisms and temperature,
little information is available so far.
The decay of microorganisms and dust is a parameter that cannot be ignored
in empirical and theoretical models of airborne transmission (Lighthart and
Frisch, 1976; Yu et al., 2004); it may help when assessing health impacts
from exposure. The term “decay” encompasses both physical and biological
means. Physical decay is the physical elimination of a particle from the air
by means of a series of processes such as gravitational sedimentation, im-
paction and electrostatic precipitation; biological decay is the loss of biolog-
ical activity of an airborne microorganism owing to loss of enzyme activities
or denaturing of membrane phospholipids, proteins or nucleic acids (Cox,
1989). For biological decay, the situation may be more complicated in some
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Airborne Microorganisms and Dust in Livestock Houses 1083
cases when the microorganisms go into a viable but nonculturable (McKay,
1992; Oliver, 2010; Trevors, 2011) or dormancy state (Locey, 2010). It is clear
that physical decay applies to the elimination of dust particles, whereas both
physical and biological decay apply to airborne microorganisms.
3.1 Physical Decay
Mechanisms affecting physical decay of particles are listed in Table 3. In
reality, these mechanisms may have collective effect on a particle, but the
dominant mechanism varies mainly with particle size (e.g., decay of larger
particles is prone to drive by gravimetric sedimentation whereas decay of
smaller particles is mainly determined by diffusion (Abadie et al., 2001; He
et al., 2005). Physical decay can be quantified by the rate of deposition
(deposition rate loss coefficient or deposition velocity; Deshpande et al.,
2009). Lai (2002) reviewed the deposition rate for particles ranging from
0.01 to 10 μm and found it had a U-shaped pattern. The lowest deposition
rate was found for particles ranging from 0.1 to 1 μm because particles
in this range were less affected by either sedimentation or diffusion than
TABLE 3. Mechanisms associating physical decay of microorganisms and dust
Mechanism Definition
Advection The mean transport of a particle by
the mean motion of the
atmosphere, and occurs when the
spatial gradient is nonzero and the
particle is transported along the
mean wind
(Baldocchi et al., 1988)
Brownian diffusion The process of mass transfer of
particles brought about by a
random molecular motion
(Brownian motion) and associated
with a concentration gradient
(Vaithiyalingam et al., 2002)
Thermophoresis The motion of a particle under the
influence of a temperature gradient
(Langer and Holcombe, 1999)
The separation of dispersed particles
from gaseous phase under action of
(Wunsch, 1994)
Impaction The deposition of particles due to
their momentum causing them to
deviate from airflow streamlines
and impacting at bifurcations
(Katz et al., 2001)
The use of an electrostatic field for
precipitating or removing charged
particles from a gas flow in which
the particles are carried
(Shen and Pereira, 1979)
Some definitions in this table that were originally for gases or molecules in nonaerial environments
have been modified to make them suitable for describing the associating mechanisms of microorganisms
and dust in the air.
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1084 Y. Zhao et al.
their counterparts do. Besides particle size, deposition rate is affected by
other factors such as room furnishing and air speed. Thatcher et al. (2002)
found increasing surface area (provide more furniture) and air speed (by
means of elevating ventilation rate) increased the deposition rate of particles
(0.5–10 μm) in an experimental room.
3.2 Biological Decay
The biological decay of airborne microorganisms has been expressed in
different ways (e.g., decay rate [or death rate], survival, or half-life). The
decay rate is the decrease in concentration of viable microorganisms over
time. A proportionality constant (k) indicates the extent of decay rate, and
is shown in equation 1, where C
is the initial concentration of airborne
microorganisms, C
is the concentration of microorganisms at time t after
initial (Phillips et al., 1964). The survival represents the percentage of viable
microorganisms left at a certain moment vis-
a-vis the initial microbial count
(Wu, 2009). The half-life, t
, is the time taken for the concentration of viable
microorganisms in the air to decrease by half (see equation 2). Previous
studies showed that the biological decay of airborne microorganisms was
species-dependent and was determined by many external factors, such as
humidity, oxygen concentration, temperature, ozone concentration, radiation
(UV, γ -ray, X-ray), air ions, and air pollutants (CO, SO
; Benbough,
1971; Lighthart, 1973).
k =
log 2
× t
3.3 Environmental Factors Affecting Biological Decay
For long distance airborne transmission between farms, microorganisms may
be exposed to unfavorable environmental conditions that induce death or
dormancy of microorganisms (Lennon and Jones, 2011; Locey, 2010; Wu
et al., 2012). In this section we present an introduction of several envi-
ronmental factors and their working mechanisms on biological decay of
The effect of humidity on the biological decay of airborne microorgan-
isms has been investigated since the 1950s. In the early studies, the measure
most used for humidity was relative humidity (RH; the ratio o f the actual
water vapor pressure of the air to the water vapor pressure of saturated air
at a certain temperature). The results of these studies showed that different
microorganisms were prone to decay either at low RH (Lighthart, 1973), at
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Airborne Microorganisms and Dust in Livestock Houses 1085
median RH (Wright et al., 1968b), or at higher RH (Songer, 1967; Theunis-
sen et al., 1993). More recently, a few studies have used absolute humidity
(AH; the actual water content of the air) as another measure of humidity.
For instance, Shaman and Kohn (2009) reported that the survival of airborne
influenza virus was more significantly constrained by AH than by RH. The
authors argued that RH is a meaningful physical quantity and for certain or-
ganisms may affect biological response; however, the AH can be of greater
biological significance for many organisms. Some studies reported significant
effects of other measures of humidity, such as evaporation potential (EP; the
difference between actual water vapor content in the air and the water va-
por content in saturated air at the same temperature), on microbial survival
(Zhao et al., 2012). Although a bunch of studies have been carried out, it is
not yet fully understood how humidity influences microbial decay.
Temperature profoundly affects the biological decay of airborne mi-
croorganisms. In general, the higher the ambient temperature is, the faster
the microorganisms decay. For instance, the decay rate of Flavobacterium sp.
is 0.007 log min
at –2 to 24
C, but increases to 0.017 log min
at 29 to 49
(Ehrlich et al., 1970a). A faster decay at higher temperature has also been
reported for other microbial species, such as E. coli, S. marcescens (Ehrlich
et al., 1970b), and Newcastle disease virus (Kournikakis et al., 1988). Prescott
et al. (2005) have stated that high temperature may damage microorganisms
either by denaturing the enzymes, transport carriers, and other proteins, or
by melting and disintegrating the lipid bilayer, or both.
The ambient environment is full of various types of radiation, including
UV (10–400 nm) and visible light (400–750 nm), which may inactivate the
microorganisms. The wavelength of UV between 10 nm and 120 nm has the
highest energy, but this type of UV is blocked by normal dioxygen in air
and cannot reach the ground. The rest of UV radiation, from low to high
energy, is categorized as UV-A (320–400 nm), UV-B (280–320 nm), and UV-C
(100–280 nm), of which UV-C is considered to be the most germicidal. The
UV-C wavelength between 250–270 nm can be effectively absorbed by mi-
crobial genetic material, and is the UV wavelength most lethal to microor-
ganisms (Keyser et al., 2008). The germicidal effect of UV-C light on bacteria
and viruses is primarily due to the formation of pyrimidine (thymine and
cytosine) dimers that inhibit the replication and function of genetic material
(Giese and Darby, 2000; Prescott et al., 2005). Bacteria decay more readily
under UV radiation than RNA viruses (Harris et al., 1987; Hijnen et al., 2006).
The probable reason for this is that the thymine of bacterial DNA is more
vulnerable to dimerization induced by UV than the uracil of viral RNA. The
mechanism whereby UV-A and UV-B (also called near-UV) inactivates mi-
croorganisms is suspected to be the breaks in strands of genetic materials that
are induced by the UV itself and toxic tryptophan photoproducts (Prescott
et al., 2005). Visible light may also damage microorganisms. Microbial pig-
ments become excited when they absorb light energy, and are transferred
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1086 Y. Zhao et al.
to O
, generating singlet oxygen (
), which is a highly reactive oxidant
(Valduga et al., 1993). As a self-protecting mechanism, some microorganisms
may possess carotenoids that can absorb the excitation energy and reduce
the formation of singlet oxygen, thus preventing cells from being damaged
by light radiation (McCambridge and McMeekin, 1981).
Oxygen may accept electrons forming other toxic derivatives such as
superoxide radical, hydrogen peroxide, and hydroxyl radical, which may
easily destroy the cellular constituents. Many aerobic microorganisms contain
enzymes such as superoxide dismutase and catalase, which protect the cell
against oxidation by the derivatives; all the strictly anaerobic microorganisms
lack these enzymes (Prescott et al., 2005). The effect of oxygen level on decay
of airborne Serratia marcescens 8UK and E. coli B was studied by Cox (1989),
who reported that oxygen was toxic for these microorganisms only when RH
was lower than 70%. The toxicity increased with oxygen concentrations up
to 30%; higher concentrations produced no additional toxicity. This finding
was generally in agreement with other similar studies (Benbough, 1967;
Hess, 1965). Viruses seem to be less sensitive to oxygen than bacteria. The
decay of airborne viruses that included Semliki Forest virus, Langat virus,
T7 coliphage, Poliovirus, and Encephalomyocarditis virus was no different
whether they were aerosolized in the air or in nitrogen (Benbough, 1971;
de Jong et al., 1975).
Bacteria exposed to ozone (O
) may be inactivated due to damage
to the cell surface (Giese and Christensen, 1954; Scott and Lesher, 1963)
and destruction of the intracellular enzymes, protein and genetic material
(Barron, 1954; Ingram and Haines, 1949; Kim et al., 1999). Ozone may dam-
age the viral nucleic acids of viruses and alter the polypeptide chains of
the viral protein coat (de Mik and de Groot, 1977; Kim et al., 1999; Roy
et al., 1981). Investigations of the ozone effect on decay of airborne microor-
ganisms showed that fungi seemed more resistant to ozone than bacteria;
Gram-positive bacteria were more resistant than Gram-negative ones (Hein-
del et al., 1993; Kowalski et al., 1998). Ozone alone can be toxic to airborne
microorganisms; however, its toxicity is enhanced when ozone reacts with
compounds in the ambient air, known as open air factors (OAF). Studies
have shown that mixture of ozone with olefins (de Mik et al., 1977; Druett
and Packman, 1972) and ozone with negative air ions (Fan et al., 2002) are
more toxic to airborne microorganisms than ozone alone.
The dust particles to which microorganisms adhere may protect them
from biological decay. When microorganisms are carried by the dust, they
may suffer less radiation and exposure to toxic gas, and less fluctuation in
micro-climate (Milling et al., 2005). It has been found that individual bac-
teria are effectively inactivated by ozone; however, when these bacteria
were covered with a coating of organic matter, as a bio aerosols, ozone in
permissible concentration had no effect (Elford and van den Ende, 1942).
As well as providing physical protection, the composition of dust particles
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Airborne Microorganisms and Dust in Livestock Houses 1087
might give bio-chemical support to microorganisms. In order to metabolize,
microorganisms require carbon, oxygen, nitrogen, phosphorus, sulfur, and
other elements (Maus et al., 2001). Compounds containing these elements
are abundant in airborne dust from livestock production systems (Aarnink
et al., 1999; Muller and Wieser, 1987). An interesting hypothesis is that micro-
bial decay in particles differs, depending on the composition of the particles.
Actually, in some laboratory experiments, it appears that decay of microor-
ganisms differs as they are aerosolized from liquid suspensions with different
chemical compounds. (Benbough, 1971; Hess, 1965).
3.4 Studies on Biological Decay
There have been extensive studies on the biological decay of microorganisms
at different temperature and RH levels, using aerosol experiments. In these
experiments, microorganisms were aerosolized in airspace that was sampled
at certain intervals. The biological decay was indicated by the amounts of
collected microorganisms at different sampling moments. The results of se-
lected studies are summarized in Tables 4 and 5. The selection of references
follows the procedures and screening criteria as below: first, all references
related to biological decay of any species of airborne microorganisms were
searched in literature databases (Web of Science, Scopus, Google Scholar);
second, only references in which biological decay was investigated by ex-
cluding confounding effect of physical decay (e.g., using inert tracers or
labeled microorganisms) were selected; third, due to the fact that some mi-
croorganisms showed a biphase biological decay (with a fast initial decay
rate in the first few seconds or minutes after aerosolization, followed by
a slow secondary decay) and the airborne transmission concerned is long
distance and time (Brankston et al., 2007; Cox, 1971; Songer, 1967; Webb,
1959), only the secondary biological decay is presented in the tables. The ta-
bles show the highest biological decay at the least favorable temperature/RH,
and the lowest biological decay at the most favorable temperature/RH. The
values of biological decay have been presented in three ways: decay rate,
survival and half-life. By reviewing the results in Tables 4 and 5, it proofs
that the biological decay largely varies between the microbial species and is
profoundly affected by temperature and RH.
Most of the previous studies have used wet aerosolization in which mi-
crobial suspensions were aerosolized. Wet aerosolization does mimic the fate
of microorganisms expelled from animal respiratory tracts in wet aerosols.
However, after they have been generated, the large wet aerosols containing
microorganisms settle on surfaces and the small ones shrink into dry nu-
clei; both processes are very fast, taking only seconds to minutes (Kincaid
and Longley, 1989; Sun and Ji, 2007; Wells, 1934). Therefore, the microor-
ganisms in wet aerosols can only be transported over short distances and
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TABLE 4. Biological decay of bacteria under different relative humidity (RH) and temperature (Temp)
Bacteria RH levels involved (%)
Temp levels
involved (
C) H/L
Extreme RH for
decay (%)
Extreme Temp
for decay (
C) Decay Survival
Half-life Reference
5, 50, 95 8.5, 15, 25, 35 H 50 35 0% (1.5) (Theunissen et al., 1993)
L 95 15, 25 >10%
32–87 15, 30 H <50% 30 3 min (Wathes et al., 1986)
L High RH 15 83 min
E. coli
26.5 H 50
26.5 0.9
% (30) (Cox, 1970)
26.5 20
% (30)
Flavobacterium 25, 45, 65, 85, 99 24 H 99 24 2.6% min
(Ehrlich et al., 1970a)
L 85 24 1.3% min
85, 100 –40,–18, –2, 24,
29, 38, 49
H85 49 <0.01%
(Ehrlich et al., 1970a)
L 100 40,–18 4.7% min
strain 74/81
30, 60, 90 20 H 60 20 - <1% (120) (Dennis and Lee, 1988)
L90 20 >10
% (120)
10, 25, 40, 50, 60, 75, 90 27 H 40 27 <1% (300) (Wright et al., 1968b)
L 10, 90 27 10
% (60)
10, 25, 40, 50, 60, 75, 90 27 H 50, 60 27 0% (300) (Wright et al., 1968b)
L 10 27 100%
10, 25, 30, 40, 50, 60, 75, 80, 90 27 H 60, 80 27 0% (240) (Wright et al., 1968a)
L 10 27 50% (240)
28, 40, 59, 79 22.6 H 79 22.6 2.1% (45) (Thomson et al., 1992)
L 40 22.6 8.9% (45)
26.8 H 50
% (15) (Cox and Goldberg, 1972)
H 55 0.2
% (15) (Cox, 1971)
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26.8 H 81 0.4
% (15) (Cox and Goldberg, 1972)
% (15)
H 75 0.01
(Cox, 1971)
% (15)
23, 39, 60, 79 H 79 0.01
(Handley and Webster,
L 39, 60 1
% (60)
30, 50, 70, 95 20 H 30 20 0.1
% (300) (Won and Ross, 1969)
L 50, 70, 95 20 >10
% (300)
Sarcina lutea 1/3, 23/27, 45/52, 73/76, 88/96 15 H 1/3 15 0.346 log%
(Lighthart, 1973)
L 45/52 15 0.001 log%
40, 97 25 H 40 25 2% (32) (Hess, 1965)
L 97 100% (32)
45/52, 73/76, 88/96 15 H 45/52 15 0.368 log%
(Lighthart, 1973)
L 73.0/75.5 15 0.057 log%
no. 1600
39, 75 H 75 0.0189 log
(Strasters and Winkler,
L 39 0.0037 log
20, 40, 60, 80 27 H 40 27 0% (30) (Stewart and Wright, 1970)
L20 27 >10
% (240)
Estimated readings from figures.
H = highest biological decay of airborne microorganisms (i.e., worst survival and shortest half-life time). L = lowest biological
decay of airborne microorganisms (i.e., optimal survival and longest half-life time).
In brackets is the time span (in minutes) between which survival rate
corresponds to.
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TABLE 5. Biological decay of viruses under different relative humidity (RH) and temperature (Temp)
RH levels
Temp levels
C) H/L
Extreme RH for
decay (%)
Extreme Temp
for decay (
C) Decay Survival
Half-life Reference
Bacteriaphage S-13 20, 50, 80 21 H 50 21 0.1
% (120) (Dubovi and Akers,
L80 21 >10
% (120)
Bacteriaphage MS-2 20, 50, 80 21 H 50 21 0.01
% (120) (Dubovi and Akers,
L20 21 1
% (120)
type 3
30, 90 6, 32 H 90 32 0% (180) (Elazhary and
Derbyshire, 1979)
L 90 6 1.6–4.0% (180)
Newcastle disease
10, 35, 90 23 H 35 23 0.1
% (90) (Songer, 1967)
L10 23 >10
% (90)
Infectious bovine
10, 35, 90 23 H 35 23 0.1
% (90) (Songer, 1967)
L90 23 >10
% (90)
Vesicular stomatitis
10, 35, 90 23 H 35 23 1
% (90) (Songer, 1967)
L10 23 >10
% (90)
E. coli B T3
10, 35, 90 23 H 35 23 0% (90) (Songer, 1967)
L90 23 >10
% (90)
Bovine rotavirus UK 30, 50, 80 20 H 80 20 3 h (Ijaz et al., 1994)
L50 20 18h
Mouse rotavirus 30, 50, 80 20 H 80 20 2 h (Ijaz et al., 1994)
L50 20 24h
Poliovirus type 1
30, 50, 80 20 H 30, 50 20 n.r. (Ijaz et al., 1985b)
L80 20 9hs
Human corona virus
30, 50, 80 6, 20 H 80 20 3.3 h (Ijaz et al., 1985a)
L 50 6 102.5 h
Human rotavirus 30, 50, 80 6, 20 H 80 6 1.7 h (Ijaz et al., 1985c)
L 50 6 57.4 h
Bovine rotavirus 20, 50, 80 10, 20, 30 H 50 30 2.39 log h
(Moe and Harper,
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L90 100.03logh
E. coli B T3
8, 30, 50,
80, 95
21 H 8 21 0% (240) (Hatch and Warren,
L95 21 >10
% (240)
Pasteurella pestis
20, 40, 50,
60, 72, 95
21 H 40, 50, 60 21 0.1
% (240) (Hatch and Warren,
L 20, 72, 95 21 >10
% (240)
rditis Virus
10, 20, 30,
37 0.001
(de Jong et al.,
20 100
% (30–35)
Foot and Mouth
disease virus O
BFS 1860
20, 30, 40,
50, 60, 70
19–22 H 20 19–22 0.01
% (5) (Barlow and
Donaldson, 1973)
L 50, 60, 70 19–22 0.01
55, 70 18–23 H 55 18–23 n.c. (Donaldson, 1972)
L 70 18–23 3.15 log h
Foot and Mouth
disease virus O
55, 70 18–23 H 55 18–23 n.c. (Donaldson, 1972)
L 70 18–23 2.60 log h
Foot and Mouth
disease virus O
55, 70 18–23 H 55 18–23 n.c. (Donaldson, 1972)
L 70 18–23 2.38 log h
Foot and Mouth
disease virus C
55, 70 18–23 H 55 18–23 2.90 log h
(Donaldson, 1972)
L 70 18–23 1.88 log h
Foot and Mouth
disease virus A5
55, 70 18–23 H 55 18–23 2.60 log h
(Donaldson, 1972)
L 70 18–23 1.78 log h
Foot and Mouth
disease virus C
55, 70 18–23 H 55 18–23 2.40 log h
(Donaldson, 1972)
L 70 18–23 1.43 log h
Foot and Mouth
disease virus A22
55, 70 18–23 H 55 18–23 3.28 log h
(Donaldson, 1972)
(Continued on next page)
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TABLE 5. Biological decay of viruses under different relative humidity (RH) and temperature (Temp) (Continued )
RH levels
Temp levels
C) H/L
Extreme RH for
decay (%)
Extreme Temp
for decay (
C) Decay Survival
Half-life Reference
L 70 18–23 1.25 log h
Foot and Mouth
disease virus O1
55, 70 18–23 H 55 18–23 2.05 log h
(Donaldson, 1972)
L 70 18–23 1.06 log h
Influenza virus 20/25,
H 81 32.0 0% (240) (Harper, 1961)
L 23/25 7.0/8.0 61% (1380)
Vaccinia virus 17/20,
H 80/83 31.5/33.5 0% (1380) (Harper, 1961)
L 20 10.5/11.5 66% (1380)
Venezuelan equine
32.0/ 33.0
H 81/85 32.0/33.0 0% (360) (Harper, 1961)
L 19 9.0/9.5 26% (1380)
Poliomyelitis virus 18/23,
20.5/23.5 H 49/51 20.5/23.5 0% (360) (Harper, 1961)
L 80/81 20.5/23.5 85% (1380)
20, 80 H 20 2.5% (60) (Benbough, 1971)
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L 80 53% (60)
Japanese B
Encephalitis Virus
30, 55, 80 24 H 80 24 28 min (Larson et al., 1980)
L30 24 62min
Langat virus 20, 80 H 80 10% (60) (Benbough, 1971)
L 20 52% (60)
Semliki Forest virus 20, 80 H 80 51% (60) (Benbough, 1971)
L 20 67% (60)
E. coli B T7
20, 80 H 20 0.05% (60) (Benbough, 1971)
L 80 57% (60)
Lassa virus Josiah 30, 55, 80 24, 32, 38 H 80 32 6.9% min
0.3% (60) 10.1 min (Stephenson et al.,
L 30 24 1.3% min
16.9% (60) 54.6 min
Pseudorabies virus 55, 85 4, 22 H 85 22 17.4 min (Schoenbaum et al.,
L 55 4 43.6 min
Newcastle disease
20/30, 50,
10, 15, 20,
25, 30
H 80 25, 30 8% (360) (Kournikakis et al.,
L 20/30 10 56% (360)
reproductive and
syndrome virus
5–90 5–41 H 63.8 30 3.3 min (Hermann et al.,
L 17.1 5 192.7 min
(Continued on next page)
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TABLE 5. Biological decay of viruses under different relative humidity (RH) and temperature (Temp) (Continued)
RH levels
Temp levels
C) H/L
Extreme RH for
decay (%)
Extreme Temp
for decay (
C) Decay Survival
Half-life Reference
Psittacosis agent 30, 50, 80 26.7 H 80 26.7 6.73%
(Mayhew and
Hahon, 1970)
L 30 26.7 0.64%
Reovirus type 1
21/24 H 65/75, 25/35 21/24 3.2–3.3%
(Adams et al., 1982)
L 85/95 21/24 1.5–2.5%
Yellow fever virus 30, 50, 80 26.7 H 50 26.7 7.04%
(Mayhew and
Hahon, 1970)
L 30 26.7 3.26%
Variola virus 30, 50, 80 26.7 H 30 26.7 0.86%
(Mayhew and
Hahon, 1970)
L 80 26.7 0.56%
Syncytial Virus
20, 30, 40,
50, 60, 70,
80, 90
20.5 H 80 20.5 1.49 log h
(Rechsteiner and
Winkler, 1969)
L 20 20.5 0.47 log h
Rift Valley fever
virus ZH-501
30, 55, 80 24 H 80 24 10.1%
6.9 min (Brown et al., 1982)
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L 30 24 0.9% min
77.0 min
Rift Valley fever
virus SA-51
30, 55, 80 24 H 80 24 6.1% min
11.4 min (Brown et al., 1982)
L 30 24 1.3% min
53.3 min
Rotavirus SA11 25, 50, 80 20 H 80 20 <2 h (Sattar et al., 1984)
L50 20 40h
St. Louis
encephalitis (SLE)
29, 46, 60,
21 H 80 21 14
% (360) (Rabey et al., 1969)
L29 21 79
% (360)
Venezuelan equine
30, 60 22 H 60 22 0.006–77.3% (60) (Berendt and
Dorsey, 1971)
L 30 22 0.02–88.7% (60)
Rhinovirus-14 30, 50, 80 20 H 30, 50 20 <0.25% (15) (Karim et al., 1985)
L 80 20 30% (1440) 13.7 hs
Estimated readings from the figures. n.c. = not calculated due to no infectious virus was recovered.
H = highest biological decay of airborne microorganisms
(i.e., worst survival and shortest half-life time); L = lowest biological decay of airborne microorganisms (i.e., optimal survival and longest half-life time).
by dividing the amount of virus collected in the last air sample (360 min) by that in the first air sample (15 min).
In brackets is the time span (in minutes) between
which survival rate corresponds to.
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1096 Y. Zhao et al.
induce infections in limited areas (Brankston et al., 2007). For microorgan-
isms released from dry sources such as feces and litter, which may be more
closely associated with long distance transmission, dry aerosolization i s rec-
ommended. Dry aerosolization may give a picture of the biological decay
of microorganisms that differs from the decay in wet aerosolization because
the microorganisms may suffer either dehydration stress at low ambient RH
or rehydration at high ambient RH (Cox, 1971).
4.1 Particle Deposition in Respiratory Tract of Humans and Animals
According to Heyder et al. (1986), the probability of deposition will be
different for each particle even if all the particles in the air inhaled in one
breath are identical, because the inhaled air with particles penetrates the
respiratory tract to different depths where it remains for different periods of
time, and because of the stochastic nature of particle transport. Therefore,
particle deposition (in the respiratory tract) refers to the “mean probability”
of an inspired particle being collected on airway surfaces. Particle deposition
in the respiratory tract depends on particle characteristics (e.g., size, shape,
density) and breathing pattern (e.g., nasal/oral breath, respiratory flow rate,
cycle period), and is commonly expressed as a function of particle size.
Particle deposition in the human respiratory tract has been well doc-
umented (Brown et al., 2002; James et al., 1991; Lippmann et al., 1980).
In principle, the deposition of particles is governed by the mechanisms
of diffusion for particles <0.1 μm, or by diffusion and sedimentation for
0.1–1 μm particles, or by sedimentation and impaction for particles >1 μm
(Heyder, 2004). On the basis of previous experimental studies, Heyder et al.
(1986) developed a semiempirical deposition model for particles ranging
from 0.005 μmto15μm. The model-simulated deposition pattern for slow
inspiration over a long period for both oral and nasal breathing is shown in
Figure 2. The deposition has been shown for three regions of the respiratory
tract—extra-thoracic, bronchial, and alveolar—based on how far down the
tract particles may be deposited. In addition, total deposition is given (the
sum of the deposition in the three regions). It can be seen that the total de-
position is least for particles of 0.1–1 μm, and that the deposition increases
as the size of small particles (<0.1 μm) decreases, and the size of the larger
particles (>1 μm) increases. Particles larger than 10 μm are mainly deposited
in the extrathoracic region, and cannot penetrate the alveolar region during
slow and fast oral and nasal inspiration.
The deposition in the human respiratory tract cannot be extrapolated to
livestock because of the discrepancy in morphology of human and animal
respiratory systems (Corbanie et al., 2006). Particle deposition in guinea pig
head, trachea, and lungs was investigated by Harper and Morton (1953).
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Airborne Microorganisms and Dust in Livestock Houses 1097
FIGURE 2. Deposition of unit density spherical particles in human respiratory tract at a mean
flow rate of 250 cm
and a breathing cycle period of 8 s. Solid curves show the deposition
curve for steady oral breathing, and dashed curves for steady nasal breathing. Deposition =
1 indicates all particles deposit, and deposition = 0 means no particle deposit at a certain
region. Adapted from Heyder et al. (1986).
They found an increasing regional deposition in guinea pig head for larger
particles: 35.7% of the 1 μm particles were deposited in the guinea pig
head region, compared with 98.1% of the 10 μm particles. The reverse was
true for lung deposition: 55.2% of 1 μm particles and 0.6% of 10 μmwere
deposited in this region. The particle size most deposited in the trachea
was 2.5 μm. A model of particle deposition in the guinea pig respiratory
tract was established by Schreider and Hutchens (1979), w ho found that
99% of unit density particles of 10 μm or more could be deposited in the
nasopharyngeal-tracheobronchial region (Figure 3). The lowest deposition
was 10% for a particle size of 0.8 μm. About 17% of particles ranging from
0.08 to 4 μm could be deposited in the pulmonary region. However, this
model was compromised by several assumptions that were made by the
authors (e.g., laminar airflow in the respiratory tract, equal expansion of all
lobes and alveoli, and complete mixing of the particles in the alveoli.
Hayter and Besch (1974) investigated the regional deposition of five
particle sizes (0.091, 0.176, 0.312, 1.1, and 3.7 to 7 μm) in chicken. The
particles deposited in the head and anterior trachea were in the 3.7–7 μm
size range, those deposited in the lung and posterior air sacs were 1.1 μm
size, and those deposited in the caudal regions of the birds were in the size
classes 0.091 and 0.176 μm. Those of size 0.312 μm were deposited mainly
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1098 Y. Zhao et al.
FIGURE 3. Deposition of unit density spherical particles in the respiratory tract of guinea
pig at a tidal volume of 4.44 cm
and a respiratory rate of 60 breaths min
. NP-TB:
nasopharyngeal-tracheobronchial region. P = pulmonary region. Adapted from Schreider
and Hutchens (1979).
in upper airways. These early data of particle deposition in chicken airways
are suspected to be compromised by the use of anesthetized chickens, be-
cause anesthesia alters the animals’ breathing pattern. Corbanie et al. (2006)
investigated the deposition of particles in a wider range (1, 3, 5, 10, and
20 μm) in unanaesthetized chickens of three ages. Unlike the definition of
deposition that was proposed by Heyder et al. (1986), Corbanie et al. (2006)
defined deposition as the percentage of particles deposited in a particular
region of the respiratory tract among those in the entire tract. They found
that particles larger than 5 μm were too large to be deposited in the lungs
and air sacs in 2- and 4-week-old chickens, as low percentages of particles
were recovered in these regions (Figure 4). For 1-day-old chicks, however,
the particle deposition in lungs and air sacs was independent of particle size
and even particles of 20 μm were deposited in the lower airway, possibly
due to the chicks having a different breathing pattern than older chickens.
The deposition pattern of monodispersed particles (3.3 μm) in calf air-
ways was studied by Jones et al. (1987). They found those particles were
preferentially deposited in the trachea and major bronchi.
4.2 Infective Dose
Inhalation of pathogens may result in infection of recipients. Infection is
likely to fit a single-hit model, which means that one pathogenic microor-
ganism may trigger an infection in a recipient. From this point of view, the
infective dose (ID; or occurrence of infection) is therefore related to the
probability that a recipient becomes infected after taking in a certain dose
of pathogenic microorganisms, following a Poisson distribution. The ID of
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Airborne Microorganisms and Dust in Livestock Houses 1099
FIGURE 4. Deposition of fluorescent particles in the respiratory tract of 1-day-old (), 2-
week-old (), and 4-week-old () broilers. NELTS = nose, eyes, larynx, trachea and syrinx.
LT = lungs and thoracic air sacs. LTOC = lower beak, tongue, esophagus and crop. Adapted
from Corbanie et al. (2006).
pathogenic microorganisms to human and animals has generally been ex-
pressed in two ways. In one way, ID is expressed as the number of infected
recipients out of a population after a dose of microorganisms has been
administered. The other way is to determine the microbial concentrations
required to infect 50% of a population (ID
Table 6 lists the ID of several pathogenic microorganisms. The ID of
the same microorganism varies, depending on the recipient animal species.
For instance, a lower ID of FMD virus is needed to infect sheep and cattle
than to infect a pigs (Alexandersen and Donaldson, 2002; Donaldson et al.,
1987; Gibson and Donaldson, 1986). It can be also seen that a certain dose
of a microorganism is not always capable of infecting all recipients, probably
because of a difference in the resistance of individual recipients (due to e.g.,
age, breed; Roy, 1980). Furthermore, the route by which the microorgan-
isms are administered may also be responsible for variation in ID (Cafruny
and Hovinen, 1988; Zimmerman et al., 1993). In previous studies, the ad-
ministration routes were either nasally or orally, or via aerosols, and these
reflect different deposition situations and regions for microorganisms in the
respiratory tract. Nasal administration simulates infection because larger mi-
crobial particles are deposited in the upper airways, the oral ministration
may simulate oral breathing, and the aerosol administration simulates infec-
tion because smaller microbial particles are deposited in deeper airways. It
was reported that the microorganisms had preferential sites for multiplication
and i nfection because of the complex vulnerability of regions in respiratory
tracts (Cafruny and Hovinen, 1988; Druett et al., 1953; Druett et al., 1956).
This being so, infection occurs more readily when the microorganisms are
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TABLE 6. Infective dose (ID) of some pathogenic microorganisms
Microorganism ID Recipient Administration
(or% infected) Reference
Campylobacter jejuni 90 CFU 3-day chickens Orally 9/10 (Ruiz-Palacios et al., 1981)
E. coli (O157:H7) 6000 CFU 3-month pigs 6/8 (Cornick and Helgerson, 2004)
E. coli (O157:H7) <300 CFU 10-week calves Orally 2/17 (Besser et al., 2001)
E. coli (O157:H7) 10
CFU 3-year steer Stomach tube 2/5 (Cray and Moon, 1995)
Salmonella typhimurium 1000 CFU 10–14-day pigs Intranasal 1/5 (Loynachan and Harris, 2005)
Salmonella enteritides <10 CFU >52-week molted layers Orally 50% (Holt, 1993)
Salmonella enteritides 6500–56000 CFU >52-week unmolted layers Orally 50% (Holt, 1993)
FMD virus (strain O1
1700 TCID
20–30 kg pigs Aerosol 5/8 (Alexandersen and Donaldson,
FMD virus (strain O
13–398 TCID
43–166 kg calves Aerosol 10/12 (Donaldson et al., 1987)
FMD virus (strain O
10–50 TCID
26–82 kg sheep Aerosol 7/12 (Gibson and Donaldson, 1986)
FMD virus (strain SAT 2 SAR
25–251 TCID
118–150 kg calves Aerosol 11/15 (Donaldson et al., 1987)
4–5-week pigs Intranasal 2/3 (Yoon et al., 1999)
Porcine rotavirus 1 PFU 2-hr piglets Pharynx 2/2 (Graham et al., 1987)
Encephalomyocarditis virus 10
4–6-week pigs Intranasal 2/5 (Zimmerman et al., 1993)
Influenza A/Texas/91 (H1N1)
100000 TCID
18–33-year-old humans Intronasal 24/33 (Hayden et al., 1996)
Influenza A2/Bethesda/10/63 1–5 TCID
21–40-year-old man Aerosol 4/14 (Alford et al., 1966)
Rotavirus 0.9 FFU 18–45-year-old man Orally 1/7 (Ward et al., 1986)
Salmonella newport 150000 CFU Human Orally 1/6 (McCullough and Eisele, 1951)
Salmonella derby 1.5×10
CFU Human Orally 3/6 (McCullough and Eisele, 1951)
Salmonella bareilly 13000 CFU Human Orally 1/6 (McCullough and Eisele, 1951)
CFU = colony forming unit; TCID
= 50% tissue culture infective dose; PFU = plaque forming unit; FFU = focus forming unit.
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Airborne Microorganisms and Dust in Livestock Houses 1101
TABLE 7. Initial infection region of microorganisms (Baskerville, 1981)
Microorganism Animal Infection region
Bordetella bronchiseptica Pig URT
Haemophilus spp. Pig URT
Pasteurella spp. Pig URT
Cattle URT
Sheep URT
Mycoplasma Poultry URT
Cattle URT
Bovine herpesvirus-1 Cattle URT
Parainfluenza-3 Cattle URT
Sheep URT
Infectious laryngo-tracheitis virus Poultry URT
Infectious bronchitis virus Poultry URT
Aujeszky’s disease virus Pig URT
Aspergillus fumigatus and other fungi Poultry LRT
Respiratory syncytial virus Cattle LRT
Adenoviruses Cattle LRT
Note. URT = upper respiratory tract (including nose, pharynx, and tonsil); LRT = lower respiratory tract
(including trachea, bronchi and bronchioles, and alveoli).
administered to the more vulnerable region. Baskerville (1981) summarized
the preferred infection regions of some microorganisms to animals by cat-
egorizing nose, pharynx, and tonsils as the upper respiratory tract, and the
trachea, bronchi and bronchioles, and alveoli as the lower respiratory tract
(Table 7).
Sampling protocols for dust in ambient air have been legislated by the U.S.
Environmental Protection Agency (2006) and the European Committee for
Standardization (European Commission, 1998, 2005). Nowadays, the offi-
cial sampling protocols focus increasingly on small particles (e.g., PM
) because these have the potential to be suspended for longer time,
transported for longer distance, and deposited in the lower respiratory tract,
thus are more hazardous to human and animal health. To ensure unbiased
sampling, these protocols specify many details, such as sampling duration,
type of sampler, and sample handling.
The protocols for ambient air may not be directly applicable for dust
sampling in livestock production systems where the dust concentrations are
much higher than those in ambient air. In addition, to date there is no gold
standard for sampling airborne microorganisms. Given that the sampling
of microorganisms and dust in livestock production systems is increasingly
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1102 Y. Zhao et al.
being performed for assessing the biosecurity of air environments and for
evaluating mitigation techniques, the sampling protocol must be well de-
signed in order to assure reliable data. Subsequently, sampling strategies
and samplers for airborne microorganisms and dust are highlighted, taking
into consideration their sampling in livestock production systems.
5.1 Sampling Strategy
Isokinetic sampling is the ideal sampling method, because it has been de-
vised to sample the true numbers of particles in the air. Such sampling can be
achieved if the sampler inlet is in alignment with and facing the direction of
air flow and if the air velocity within the sampler is the same as the ambient
air velocity (Zhang, 2004). However, true isokinetic sampling is impossible
in practice due to variations in the surrounding air flow pattern (air direction
and velocity) and the limitations of some samplers (Liu and Pui, 1981). As
a concession, the current legislation aims to reduce the sampling bias in
nonisokinetic samplings by stipulating the range of conditions under which
the samplings may be performed.
The sampling location should be chosen bearing in mind the research
purpose. When human health is of concern, sampling should be carried out
near the human breathing zone. One option is to fit a portable sampler on
a worker’s body at a height of 150–170 cm above floor level and within a
radius of 30 cm around the mouth (Aarnink et al., 2011b; Ouellette et al.,
1999). There are difficulties in doing the same with animals, therefore station-
ary samplers in their breathing zones are recommended. The recommended
level of the breathing zone is 30–40 cm above floor level for pigs, 10–25 cm
for poultry, and shoulder height for cattle (Kim et al., 2007a; Topisirovic,
2003; Zhao et al., 2011d). For growing animals these figures should be ad-
justed according to the animal height at a certain age. When emissions of
microorganisms and dust are of interest, the best sampling location is in or
near the air outlet. Care should be taken not to place the samplers at a loca-
tion where the air speed is too high, because the efficiency of the sampler
(the ratio of the aerial pollutant concentration calculated from the air sam-
ples to the true concentration in the air) may drift far from 100% (Grinshpun
et al., 1994; Hofschreuder et al., 2007).
For ambient air, the daily and annual thresholds for PM
have been set
at 50 and 40 μgm
, respectively (European Commission, 1999); the annual
threshold for PM
has been set at 25 μgm
(European Commission, 2008).
To assess the dust concentration, the sampling period is generally 24 hr. The
sampling duration for ambient air may also be applied when sampling dust
in animal houses to obtain daily mean concentrations. For studies collecting
information on dust fluctuations during the day, continuous samplings for
short periods should be performed. This kind of sampling can be achieved
by interval sampling or sampling with real-time optical samplers.
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Airborne Microorganisms and Dust in Livestock Houses 1103
Due to the lack of a standard, the sampling duration for airborne mi-
croorganisms in different studies varies, but is normally less than 1 hr. The
duration is determined by taking account of the estimated concentrations of
microorganisms and the characteristics of the sampler in use. The sampling
duration can be set at a short period (a few minutes) when the total microor-
ganism is abundant in livestock houses. When the microorganism of interest
is sporadically present, the period should be set long enough to collect
enough microorganisms for further quantification analysis. Some samplers
have not been designed to be used for long sampling duration. For instance,
severe evaporation of liquid medium in All Glass Impinger (AGI-30) occurs
when the sampling period is long and this may affect its sampling efficiency.
The recommended maximum duration of the sampling period for the AGI-
30 is 30 min. Impactors may easily become overloaded when samples are
taken in livestock houses (Thorne et al., 1992), therefore, the sampling du-
ration is limited to minutes or even to seconds. Filtration method would not
encounter the problems (evaporation of sampling liquid and overloading)
of impingers and impactors; however, long sampling duration by filtration
may not benefit in microorganism collection because of the biological decay
of microorganisms owing to dehydration (Griffin et al., 2011; Wang et al.,
2001). In order to collect detectable amounts of microorganisms and to get
representative samples over a longer period, some high-volume and durable
samplers that can be continuously operated over hours have been developed
and applied, including OMNI-3000 and high-volume impinger (Griffin et al.,
2011; Kesavan and Schepers, 2006).
Other aspects in sampling and detection strategies include practical and
economic considerations. The portability of the instrument and its ancillaries
(e.g., weight and dimensions) are factors that should be considered. A high-
quality pump is required for dust filtration sampling, and it should be able
to provide a constant airflow when ambient temperature changes or when
pressure differences increases because of dust accumulation on the filter.
The culture-dependent techniques for microorganism numeration are time
consuming and particularly expensive; culture-independent techniques such
as quantitative PCR provide possibilities for rapid and accurate analysis which
is critical for biological emergency (Postollec et al., 2011; St
ahl et al., 2011),
but its incapability to distinguish between viable and dead microorganisms
needs to be considered (Y
nez et al., 2011).
5.2 Samplers for Microorganisms
Current samplers for airborne microorganisms are generally based on one of
three main principles (i.e., impaction, impingement, or filtration; Table 8).
These different sampling principles have their advantages and disadvantages.
Samplers using the impaction principle (e.g., Andersen Six Stage Impactor)
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1104 Y. Zhao et al.
TABLE 8. Common samplers for airborne microorganisms
Sampling principle Collection medium Example samplers
Impaction Agar plate Andersen One/Two/Six Stage Impactor
(Andersen Instruments Incorporated,
Atlanta, GA, USA)
Casella Slit Sampler (Casella Ltd,
Bedford, England)
Surface Air Systems (Cherwell
Laboratories, Bicester, England)
Burkard air sampler (Burkard
Manufacturing Co. Ltd., Rickman
Worth, England)
Impingement Liquid medium AGI-30 (Ace Glass, Vineland, USA)
Multistage May Liquid Impinger (AW
Dixon, Beckenham, Kent, England)
Filtration Filter Sartorius MD8 AirPort/AirScan with
gelatin or polytetrafluoroethylene filter
(Sartorius, G
ottingen, Germany)
Button Personal Inhalable Sampler (SKC,
Inc., Pennsylvania, USA)
can be used to distinguish the microorganisms according to their sizes (An-
dersen, 1958). In addition, the bacteria impacted on agar plates may be di-
rectly incubated for viable counts. However, its susceptibility to overloading
limits its sampling in livestock houses to short periods, which may result in
nonrepresentative samples. The problem of overloading can be overcome by
using samplers with the impingement principle, because the liquid samples
may be decimally diluted and analyzed after sampling. A disadvantage of
this sampler is that it may not be able to sample for a long time due to evap-
oration of the collection liquid (Lin et al., 1997). Filtration is a user-friendly
method in a practical situation, but not suitable for sampling microorganisms
that are vulnerable to dehydration stress.
A sampler with known efficiency is a prerequisite for a reliable evalu-
ation of the microbial concentration. The efficiency of a bioaerosol sampler
includes physical and biological efficiency. The physical efficiency describes
how well nonviable airborne particles are aspirated by the device’s inlet and
transported to the collection medium, referred to as inlet sampling efficiency,
and how well the bioaerosol sampler retains these particles in its medium,
referred to as collection efficiency (Griffiths and Stewart, 1999; Nevalainen
et al., 1992). For particles in the range from 1 to 10 μm and an airflow rate
between 0 and 500 cm s
, the inlet sampling efficiency of the Andersen
Six Stage Impactor is 90–150% when the opening faces in direction of the
air flow and 8–100% when it is oriented perpendicularly to the horizontal
aerosol flow (Grinshpun et al., 1994). The inlet efficiency of the AGI-30 for
particles of 1 μm is close to 100%, but it is reduced to 70–90% for 5 μmpar-
ticles and to 20–30% for 10 μm particles (Grinshpun et al., 1994). When the
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Airborne Microorganisms and Dust in Livestock Houses 1105
50% collection efficiency of the Andersen Six Stage Impactor and AGI-30 was
investigated it was found that the Andersen Six Stage Impactor has 50% col-
lection efficiency for 6.6–7.0 μm particles at the first stage and 0.57–0.65 μm
particles for the last stage (Andersen, 1958; Nevalainen et al., 1992). The
50% collection efficiency of AGI-30 was for particles of 0.31 μm (Nevalainen
et al., 1992).
Filters vary in their physical efficiency. Some are highly effective. By
measuring the particle concentration upstream and downstream of filters
with an optical particle counter, polytetrafluoroethylene (PTFE) filters and
gelatin filters were confirmed to collect more than 93% of particles, even
down to 80 nm (Burton et al., 2007).
If the particles are living organisms, they may be inactivated during sam-
pling due to impaction stress (Stewart et al., 1995), impingement stress (Shipe
et al., 1959; Tyler and Shipe, 1959; Tyler et al., 1959), and/or dehydration
stress (Li et al., 1999). Therefore, in order to indicate how well a bioaerosol
sampler maintains the microbial viability and prevents cell damage during
sampling, the concept of biological efficiency has been introduced (Griffiths
and Stewart, 1999).
In some studies, the efficiency has been evaluated by comparing sam-
plers side by side in an environment with unknown microbial concentration
(Engelhart et al., 2007; Henningson et al., 1982; Thorne et al., 1992). This
method easily ranks the performance of different samplers; however, it nei-
ther reveals whether the amount of microorganisms collected in the samples
accurately represents the microorganism content of the air nor distinguishes
between the physical and biological efficiency. Other studies separately in-
vestigated the physical and biological efficiency of bioaerosol samplers in
aerosol experiments, in which a known amount of microorganisms together
with an indicator (either labeled microorganisms, or inert tracer compound)
were nebulized in an isolator. The physical efficiency can be determined by
comparing the amount of tracer collected by a bioaerosol sampler with that
collected by the reference sampler (a sampler that has a high physical effi-
ciency); the biological efficiency is subsequently indicated by the change in
the ratio of microorganisms/indicator. Using this method, Zhao et al. (2011b;
2011c) reported the efficiency of the Andersen Six Stage Impactor, AGI-
30, OMNI-3000, and gelatin filter in sampling Enterococcus faecalis, E. coli,
Campylobacter jejuni, Mycoplasma synoviae , and Gumboro vaccine virus.
5.3 Samplers for Dust
European reference samplers use the filtration principle to collect dust from
the air (European Commission, 1998; European Commission, 2005); while in
US, a list of reference and equivalent samplers, including tapered element
oscillating microbalance (TEOM), filter, and optical sampler, have been pro-
posed by the U.S. Environmental Protction Agency (1997).
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1106 Y. Zhao et al.
For sampling dust in certain size fractions (e.g., PM
and PM
), a pre-
separator for separating the coarse dust from the target dust particle sizes
has to be installed in front of the filter/sensor/dust collector. Sampling sys-
tems with pre-separators using the impaction principle have been legislated
as reference methods for measuring dust in ambient air in the United States
(U.S. Environmental Protction Agency, 1997) and European countries (Euro-
pean Commission, 1998, 2005). These systems show steep collection curves
for sampling fine dust in ambient air where dust load is low (Kenny et al.,
2000). However, the preseparator with impaction principle may become
overloaded when sampling in dusty livestock production systems, thereby
resulting in overestimated concentrations of fine dust (Zhao et al., 2009). In
contrast, a preseparator with cyclone principle has been found to be less
vulnerable to overloading in dusty environments than preseparators based
on impaction (Zhao et al., 2009).
Optical dust samplers are now commercially available. These dust sam-
plers can monitor the real-time dust concentrations, and no further process is
needed after sampling (unlike the gravimetric method, in which filters must
be weighed). Moreover, some optical samplers may separately record the
concentrations of dust in different size ranges. However, the optical sam-
plers have limitations in humid environments, because it cannot distinguish
between droplets and dry dust. Another limitation of using optical sam-
plers lies to the difficulty in converting count to mass concentrations without
knowing the true density of the particles in concern.
Many techniques have been applied in practice to reduce the concentrations
and emissions of airborne microorganisms and dust in the livestock industry.
They vary in their utility, but can be grouped into two main principles. The
first principle, to control particles at source, includes techniques such as feed
coating and oil spraying, which has been stated to be “the most effective
means” of controlling airborne particles in the space (Pearson and Sharples,
1995). The second principle is air purification. Ionization (electrostatic) and
air scrubbers are examples.
6.1 Control at Source
The fatty substances often added to feed to increase metabolizable energy
content may reduce the airborne microorganisms and dust in animal houses
(Pearson and Sharples, 1995). Gore et al. (1986) reported that concentrations
of airborne bacteria were reduced by 27%, and settled dust by 45–47%, when
5% soybean oil was added to the pig diet. This result is consistent with the
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Airborne Microorganisms and Dust in Livestock Houses 1107
study by Welford et al. (1992), who found a 31% reduction of inhalable dust
with 2% oil addition to the feed. Other substances, such as tallow, lecithin
and lignin have also been used as effective feed additives for the purpose
of particle control in animal houses (Dawson, 1990; Pearson and Sharples,
Spraying techniques reduce the particle concentrations mainly by coat-
ing the surfaces, thereby, preventing particles from being suspended or re-
suspended from their sources (Takai, 2007). Kim et al. (2006) reported that
spraying 60 ml m
of tap water, salt water, treated manure, microbial addi-
tive, soybean oil, artificial spice, and essential oil may all reduce particles in
pig houses. These authors found an average reduction of 53% for airborne
bacteria, 51% for fungi, and 30% for total dust. The substance for spraying
found to be the most effective additive for reducing dust was soybean oil. In
broiler rooms, Aarnink et al. (2009) reported that PM
reduction increased
linearly from 55 to 85% when daily rapeseed oil application rates increased
. The PM
reduction was not related to application rate
and was about 80%. In aviary systems for layers, a 34% reduction for PM
and 50% reduction for PM
were achieved by daily spraying with 20 ml m
(Aarnink et al., 2009). Although a high oil application rate achieves high PM
reduction in broiler rooms, it may adversely affect animal health (Aarnink
et al., 2011b). When spraying 24 ml m
daily, there was a tendency for statis-
tically higher footpad lesion in broilers. Aarnink et al. (2009) recommended
limiting oil application to 16 ml m
6.2 Air Purification
The ionization (also referred to as electrostatic) technique produces nega-
tive ions in the air, which causes airborne particles to become negatively
charged. The negatively charged particles are attracted to earthed or pos-
itively charged surfaces. Previous studies have shown promising reduction
effects on dust in animal houses using ionization techniques, total dust was
reduced by 13–61% in poultry houses (Lyngtveit and Eduard, 1997; Mitchell
et al., 2000; Mitchell et al., 2004; Richardson et al., 2003), and by 45–58%
in pig houses (Rosentrater, 2003; Tanaka and Zhang, 1996). Cambra-Lopez
et al. (2009) reported that the technique produced average reductions of
36% for PM
and 10% for PM
. The disparity is probably caused by the
different charging mechanisms to particles. The small particles (<0.1 μm)
are charged by the thermal charging mechanism, which is proportional to
the diameter; large particles (>0.5 μm) are charged by field charging mech-
anism, which is proportional to the square of the diameter (Bundy, 1984).
Ionization has the potential to prevent airborne transmission of microor-
ganisms (Gast et al., 1999; Holt et al., 1999), however, no reduction of
airborne bacteria, fungi and mold was found in broiler houses by this tech-
nique (Cambra-Lopez et al., 2009). Knowledge of ionization on reduction of
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1108 Y. Zhao et al.
airborne microorganisms in animal houses is still limited and needs to be
End-of-pipe techniques, such as dedusters, air filters, and scrubbers have
been installed at air outlets of animal houses to minimize emissions of air
pollutants. Zhang et al. (2001) found a deduster removed 90% total dust
from the air exhausted from a pig house. Because dedusters are based on
the centrifuge principle, they are more effective at removing larger particles
than smaller ones. The deduster studied by Zhang et al. (2001) had a removal
efficiency of 90% for particles larger than 10 μm, 77% for 7 μm particles,
and 50% for 4 μm particles. The low removal efficiency for small particles
was assumed to be particle re-entrainment due to high air turbulence. Acid
and biological air scrubbers were originally developed to reduce ammonia
and odor emissions, and they also appear to be effective in reducing parti-
cle emissions. An acid scrubber that uses sulfuric acid may achieve a 70%
reduction of total bacteria (Aarnink et al., 2011a). In a lab-scale experiment,
Aarnink et al. (2011a) found that E. faecalis and Gumboro virus could be re-
duced by 100% when per-acetic acid was used as the circulation solution in
a scrubber. The biological scrubbers are not consistent in reducing microor-
ganisms (Seedorf and Hartung, 1999), probably because the microorganisms
for digesting odorous compounds can also be emitted to the ambient air.
The removal of total dust by biological scrubbers was found to be 22–96%
(Seedorf and Hartung, 1999).
Combined techniques have been applied in practice: for instance, oil
spraying combined with feed coating (Takai and Pedersen, 2000) and multi-
stage air scrubbers (Zhao et al., 2011a). These techniques are more consistent
and effective in reducing emissions of airborne microorganisms and dust,
as well as other gaseous pollutants (Ogink and Bosma, 2007; Zhao et al.,
2008). A disadvantage of combined scrubbing techniques is the relatively
high energy use and the complexity for use on practical farms. Therefore,
further research is needed to develop energy-saving and simple-to-operate
combined scrubbing techniques.
The most important source of airborne microorganisms is the animals
themselves by means of excretion. The sources of dust include excrement,
litter, feed, skin, and feathers.
Airborne microorganisms in animal houses are mostly bacteria, with Gram-
positive bacteria predominating; fungi account for only a small proportion
of microorganisms.
Concentrations of both microorganisms and dust are high in animal
houses. They are affected by animal type, housing system, management,
and environmental factors. Because these factors play an interrelated role
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Airborne Microorganisms and Dust in Livestock Houses 1109
on the concentrations of microorganisms and dust, integrated research on
the effects is required.
The microorganisms transmitted i n the air suffer physical and biological
decay. The physical decay largely depends on their size, and the biological
decay is mainly determined by environmental factors, such as humidity,
temperature, radiation, and toxic gases. In airborne transmission, microor-
ganisms may be carried by dust particles that may protect microorganisms
from biological decay. Knowledge of the role of dust in the transportation
of microorganisms is still lacking, and needs to be expanded.
Microorganisms are deposited on different regions in the respiratory tract,
mainly depending on their size. They have different preferred infection
regions in the respiratory tract. The amount of microorganisms needed to
induce an infection varies with microorganism species and animal species.
Reference methods for microorganism and dust sampling in animal houses
need to be legislated. These methods should be resistant to highly micro-
bial and dusty environments, and the efficiency of the sampling devices
needs to be investigated.
Different techniques have been applied to reduce airborne microorgan-
isms and dust in and from animal houses. Combining several abatement
techniques may achieve higher and more consistent reduction. Energy-
saving and simple-to-operate combined techniques are of interest for
further development.
Huynh, T. T. T. (2011a). Scrubber capabilities to remove airborne microorgan-
isms and other aerial pollutants from exhaust air of animal houses. Transactions
of the ASABE, 54, 1921–1930.
Aarnink, A. J. A., Mosquera, J., Winkel, A., Cambra-Lopez, M., Van Harn, J., Buisonje,
F. E. D., Van Hattum, T., and Ogink, N. W. M. (2009). Options for dust reduc-
tion from poultry houses. Proc. CIGR International Symposium on ‘Agricultural
Technologies in a Changing Climate’, Brisbane, Australia.
Aarnink, A. J. A., Roelofs, R. F. M. M., Ellen, H., and Gunnink, H. (1999). Dust sources
in animal houses. Proc. Proceedings on Dust Control in Animal Production
Facilities, Horsens, Denmark.
Aarnink, A. J. A., van Harn, J., van Hattum, T. G., Zhao, Y., and Ogink, N. W. M.
(2011b). Dust reduction in broiler houses by spraying rapeseed oil. Transactions
of the ASABE, 54, 1479–1489.
Abadie, M., Limam, K., and Allard, F. (2001). Indoor particle pollution: effect of wall
textures on particle deposition. Building and Environment, 36, 821–827.
Adams, D. J., Spendlove, J. C., Spendlove, R. S., and Barnett, B. B. (1982). Aerosol
stability of infectious and potentially infectious reovirus particles. Applied and
Environmental Microbiology, 44, 903–908.
Downloaded by [Wageningen UR Library] at 04:52 05 June 2015
1110 Y. Zhao et al.
Al Homidan, A., Robertson, J. F., and Petchey, A. M. (1997). Effect of temperature,
litter and light intensity on ammonia and dust production and broiler perfor-
mance. British Poultry Science, 38, S5–S17.
Alexandersen, S., and Donaldson, A. I. (2002). Further studies to quantify the dose
of natural aerosols of foot-and-mouth disease virus for pigs. Epidemiology and
Infection, 128, 313–323.
Alford, R. H., Kasel, J. A., Gerone, P. J., and Knight, V. (1966). Human influenza
resulting from aerosol inhalation. Proceedings of the Society for Experimental
Biology and Medicine, 122, 800–804.
Andersen, A. A. (1958). New sampler for the collection, sizing, and enumeration o f
viable airborne particles. Journal of Bacteriology, 76, 471–484.
Andersson, A. M., Weiss, N., Rainey, F., and Salkinoja Salonen, M. S. (1999). Dust
borne bacteria in animal sheds, schools and children’s day care centres. Journal
of Applied Microbiology, 86, 622–634.
Appleby, M. C., and Hughes, B. O. (1991). Welfare of laying hens in cages and
alternative systems: Environmental, physical and behavioural aspects. World’s
Poultry Science Journal, 47, 109–128.
Attwood, P., Brouwer, R., Ruigewaard, P., Versloot, P., De Wit, R., Heederik, D., and
Boleij, J. S. M. (1987). A study of the relationship between airborne contaminants
and environmental factors in dutch swine confinement buildings. American
Industrial Hygiene Association Journal, 48, 745–751.
Baird-Parker, A. C. (1962). The occurrence and enumeration, according to a new
classification, of micrococci and staphylococci in bacon and on human and pig
skin. Journal of Applied Microbiology, 25, 352–361.
Bakutis, B., Monstviliene, E., and Januskeviciene, G. (2004). Analyses of airborne
contamination with bacteria, endotoxins and dust in livestock barns and poultry
houses. Acta Veterinaria Brno, 73, 283–289.
Baldocchi, D. D., Hincks, B. B., and Meyers, T. P. (1988). Measuring biosphere-
atmosphere exchanges of biologically related gases with micrometeorological
methods. Ecology, 69, 1331–1340.
Banhazi, T. M., Seedorf, J., Laffrique, M., and Rutley, D. L. (2008a). Identification
of the risk factors for high airborne particle concentrations in broiler buildings
using statistical modelling. Biosystems Engineering, 101, 100–110.
Banhazi, T. M., Seedorf, J., Rutley, D. L., and Pitchford, W. S. (2008b). Identification
of risk factors for sub-optimal housing conditions in Australian piggeries: Part
2. Airborne pollutants. Journal of Agricultural Safety and Health, 14, 21–39.
Barlow, D. F., and Donaldson, A. I. (1973). Comparison of the aerosol stabilities of
foot-and-mouth disease virus suspended in cell culture fluid or natural fluids.
Journal of General Virology, 20, 311–318.
Barron, E. S. G. (1954). The role of free radicals and oxygen in reactions produced
by ionizing radiations. Radiation Research, 1, 109–124.
Baskerville, A. (1981). Mechanisms of infection in the respiratory tract. New Zealand
Veterinary Journal, 29, 235–238.
Benbough, J. E. (1967). Death mechanisms in airborne Escherichia coli. Microbiology,
47, 325–333.
Benbough, J. E. (1971). Some factors affecting the survival of airborne viruses.
Journal of General Virology, 10, 209–220.
Downloaded by [Wageningen UR Library] at 04:52 05 June 2015
Airborne Microorganisms and Dust in Livestock Houses 1111
Berendt, R. F., and Dorsey, E. L. (1971). Effect of simulated solar radiation and
sodium fluorescein on the recovery of Venezuelan equine encephalomyelitis
virus from aerosols. Applied and Environmental Microbiology, 21, 447–450.
Berthelot-Herault, F., Gottschalk, M., Labbe, A., Cariolet, R., and Kobisch, M. (2001).
Experimental airborne transmission of Streptococcus suis capsular type 2 in pigs.
Veterinary Microbiology, 82, 69–80.
Besser, T. E., Richards, B. L., Rice, D. H., and Hancock, D. D. (2001). Escherichia
coli O157:H7 infection of calves: Infectious dose and direct contact transmission.
Epidemiology and Infection, 127, 555–560.
Brankston, G., Gitterman, L., Hirji, Z., Lemieux, C., and Gardam, M. (2007).
Transmission of influenza A in human beings. Lancet Infectious Diseases,7,
Brockmeier, S. L., and Lager, K. M. (2002). Experimental airborne transmission of
porcine reproductive and respiratory syndrome virus and Bordetella bronchisep-
tica. Veterinary Microbiology, 89, 267–275.
Brown, J. L., Dominik, J. W., and Larson, E. W. (1982). Airborne survival of Rift Valley
fever virus. Army Medical Research Institute of Infectious Diseases, Maryland,
Brown, J. S., Zeman, K. L., and Bennett, W. D. (2002). Ultrafine particle deposi-
tion and clearance in the healthy and obstructed lung. American Journal of
Respiratory and Critical Care Medicine, 166, 1240–1247.
Brown-Brandl, T., Eigenberg, R., and Nienaber, J. (2010). Water spray cooling during
handling of feedlot cattle. International Journal of Biometeorology, 54, 609–616.
Bull, S. A., Allen, V. M., Domingue, G., Jorgensen, F., Frost, J. A., Ure, R., Whyte, R.,
Tinker, D., Corry, J. E. L., Gillard-King, J., and Humphrey, T. J. (2006). Sources
of Campylobacter spp. colonizing housed broiler flocks during rearing. Applied
and Environmental Microbiology, 72, 645–652.
Bundy, D. S. (1984). Rate of dust decay as affected by relative humidity, ionization
and air movement. Transactions of the ASAE, 27, 865–870.
Burton, N. C., Grinshpun, S. A., and Reponen, T. (2007). Physical collection efficiency
of filter materials for bacteria and viruses. Annals of Occupational Hygiene, 51,
Cafruny, W. A., and Hovinen, D. E. (1988). The relationship between route of
infection and minimum infectious dose: Studies with lactate dehydrogenase-
elevating virus. Journal of Virological Methods, 20, 265–268.
Cambra-Lopez, M. (2010). Control of particulate matter emissions from poultry and
pig houses. PhD, Universidad Polit
ecnica de Valencia, Valencia, Spain.
Cambra-Lopez, M., Aarnink, A. J. A., Zhao, Y., Calvet, S., and Torres, A. G. (2010).
Airborne particulate matter from livestock production systems: A review of an
air pollution problem. Environmental Pollution, 158, 1–17.
Cambra-Lopez, M., Winkel, A., Van Harn, J., Ogink, N. W. M., and Aarnink, A.
(2009). Ionization for reducing particulate matter emissions from poultry houses.
Transactions of the ASABE, 52, 1757–1771.
Chang, C. W., Chung, H., Huang, C. F., and Su, H. J. J. (2001). Exposure of workers to
airborne microorganisms in open-air swine houses. Applied and Environmental
Microbiology, 67, 155–161.
Downloaded by [Wageningen UR Library] at 04:52 05 June 2015
1112 Y. Zhao et al.
Chiba, L. I., Peo, E. R. Jr., Lewis, A. J., Brumm, M. C., Fritschen, R. D., and Crenshaw,
J. B. (1985). Effect of dietary fat on pig performance and dust levels in modified
open-front and environmentally regulated confinement buildings. Journal of
Animal Science, 61, 763–781.
Cho, J. G., Dee, S. A., Deen, J., Trincado, C., Fano, E., Jiang, Y., Faaberg, K.,
Murtaugh, M. P., Guedes, A., and Collins, J. E. (2006). The impact of animal
age, bacterial coinfection, and isolate pathogenicity on the shedding of Porcine
reproductive and respiratory syndrome virus in aerosols from experimentally
infected pigs. Canadian Journal of Veterinary Research, 70, 297–301.
Clark, P. C., and McQuitty, J. B. (1988). Air quality in farrowing barns. Canadian
Agricultural Engineering, 30, 173–178.
Clark, S., Rylander, R., and Larsson, L. (1983). Airborne bacteria, endotoxin and
fungi in dust in poultry and swine confinement buildings. American Industrial
Hygiene Association Journal, 44, 537–541.
Corbanie, E. A., Matthijs, M. G., van Eck, J. H., Remon, J. P., Landman, W. J., and
Vervaet, C. (2006). Deposition of differently sized airborne microspheres in the
respiratory tract of chickens. Avian Pathology, 35, 475–485.
Cormier, Y., Tremblay, G., Meriaux, A., Brochu, G., and Lavoie, J. (1990).
Airborne microbial contents in two types of swine confinement build-
ings in Quebec. American Industrial Hygiene Association Journal, 51,
Cornick, N. A., and Helgerson, A. F. (2004). Transmission and infectious dose of
Escherichia coli O157:H7 in swine. Applied and Environmental Microbiology,
70, 5331–5335.
Cox, C. S. (1970). Aerosol survival of Escherichia coli B disseminated from the dry
state. Applied and Environmental Microbiology, 19, 604–607.
Cox, C. S. (1971). Aerosol survival of Pasteurella tularensis disseminated from the
wet and dry states. Applied and Environmental Microbiology, 21, 482–486.
Cox, C. S. (1989). Airborne bacteria and viruses. Science Progress, 73, 469–499.
Cox, C. S., and Goldberg, L. J. (1972). Aerosol survival of Pasteurella tularensis and
the influence of relative humidity. Applied and Environmental Microbiology, 23,
Cray, W. C., and Moon, H. W. (1995). Experimental infection of calves and adult
cattle with Escherichia coli O157:H7. Applied and Environmental Microbiology,
61, 1586–1590.
Curtis, S. E., Drummond, J. G., Grunloh, D. J., Lynch, P. B., and Jensen, A. H. (1975).
Relative and qualitative aspects of aerial bacteria and dust in swine houses.
Journal of Animal Science, 41, 1512–1520.
Dawson, J. R. (1990). Minimizing dust in livestock buildings: Possible alternatives
to mechanical separation. Journal of Agricultural Engineering Research, 47,
de Deus, N., Seminati, C., Pina, S., Mateu, E., Mart
ın, M., and Segales, J. (2007).
Detection of hepatitis E virus in liver, mesenteric lymph node, serum, bile and
faeces of naturally infected pigs affected by different pathological conditions.
Veterinary Microbiology, 119, 105–114.
Downloaded by [Wageningen UR Library] at 04:52 05 June 2015
Airborne Microorganisms and Dust in Livestock Houses 1113
de Jong, J. C., Harmsen, M., and Trouwborst, T. (1975). Factors in the inactiva-
tion of Encephalomyocarditis virus in aerosols. Infection and Immunity, 12,
de Mik, G., and de Groot, I. (1977). Mechanisms of inactivation of Bacteriophage
phiX174 and its DNA in aerosols by ozone and ozonized cyclohexene. The
Journal of Hygiene, 78, 199–211.
de Mik, G., de Groot, I., and Gerbrandy, J. L. F. (1977). Survival of aerosolized
bacteriophage X174 in air containing ozone–olefin mixtures. Epidemiology and
Infection, 78, 189–198.
de Reu, K., Grijspeerdt, K., Heyndrickx, M., Zoons, J., de Baere, K., Uyttendaele,
M., Debevere, J., and Herman, L. (2005). Bacterial eggshell contamination in
conventional cages, furnished cages and aviary housing systems for laying hens.
British Poultry Science, 46, 149–155.
de Reu, K., Messens, W., Heyndrickx, M., Rodenburg, T. B., Uyttendaele, M., and
Herman, L. (2008). Bacterial contamination of table eggs and the influence of
housing systems. World’s Poultry Science Journal, 64, 5–19.
de Rezende, C. L., Mallinson, E. T., Tablante, N. L., Morales, R., Park, A., Carr, L. E.,
and Joseph, S. W. (2001). Effect of dry litter and airflow in reducing Salmonella
and Escherichia coli populations in the broiler production environment. Journal
of Applied Poultry Research, 10, 245–251.
Dennis, P. J., and Lee, J. V. (1988). Differences in aerosol survival between
pathogenic and non-pathogenic strains of Legionella pneumophila serogroup
1. Journal of Applied Microbiology, 65, 135–141.
Derikx, P. J. L., Willers, H. C., and ten Have, P. J. W. (1994). Effect of pH on
the behaviour of volatile compounds in organic manures during dry-matter
determination. Bioresource Technology, 49, 41–45.
Deshpande, B. K., Frey, H. C., Cao, Y., and Liu, X. (2009). Modeling of the penetration
of ambient PM
to indoor residential microenvironment. Proc. 102nd Annual
Conference and Exhibition, Air & Waste Management Association, Detroit, USA.
Donaldson, A. I. (1972). The influence of relative humidity on the aerosol stability
of different strains of foot-and-mouth disease virus suspended in saliva. Journal
of General Virology, 15, 25–33.
Donaldson, A. I., Gibson, C. F., Oliver, R., Hamblin, C., and Kitching, R. P. (1987).
Infection of cattle by airborne foot-and-mouth disease virus: Minimal doses with
O1 and SAT 2 strains. Research in Veterinary Science, 43, 339–346.
Donaldson, A. I., Sellers, R. F., and Lacey, J. (1983). Quantitative data on airborne
foot-and-mouth disease virus: Its production, carriage and deposition [and dis-
cussion]. Philosophical Transactions of the Royal Society of London. Series B,
Biological Sciences, 302, 529–534.
Donham, K. J., and Gustafson, K. E. (1982). Human occupational hazards from swine
confinement. Annals of the American Conference of Governmental Industrial
Hygienists, 2, 137–142.
Donham, K. J., Scallon, L. J., Popendorf, W., Treuhaft, M. W., and Roberts, R. C.
(1986). Characterization of dusts collected from swine confinement buildings.
American Industrial Hygiene Association Journal, 47, 404–410.
Downloaded by [Wageningen UR Library] at 04:52 05 June 2015
1114 Y. Zhao et al.
Donkoh, A. (1989). Ambient temperature: A factor affecting performance and phys-
iological response of broiler chickens. International Journal of Biometeorology,
33, 259–265.
Doyle, M. P. (1984). Association of Campylobacter jejuni with laying hens and eggs.
Applied and Environmental Microbiology, 47, 533–536.
Doyle, M. P., and Roman, D. J. (1982). Prevalence and survival of Campylobac-
ter jejuni in unpasteurized milk. Applied and Environmental Microbiology, 44,
Druett, H. A., Henderson, D. W., Packman, L., and Peacock, S. (1953). Studies on
respiratory infection. I. The influence of particle size on respiratory infection
with anthrax spores. The Journal of Hygiene, 51, 359–371.
Druett, H. A., and Packman, L. P. (1972). The germicidal properties of ozone—olefin
mixtures. Journal of Applied Microbiology, 35, 323–329.
Druett, H. A., Robinson, J. M., Henderson, D. W., Packman, L., and Peacock, S.
(1956). Studies on respiratory infection. II. The influence of aerosol particle size
on infection of the guinea-pig with Pasteurella pestis. The Journal of Hygiene,
54, 37–48.
Dubovi, E. J., and Akers, T. G. (1970). Airborne stability of tailless bacte-
rial viruses S-13 and MS-2. Applied and Environmental Microbiology, 19,
Duchaine, C., Grimard, Y., and Cormier, Y. (2000). Influence of building mainte-
nance, environmental factors, and seasons on airborne contaminants of swine
confinement buildings. American Industrial Hygiene Association Journal, 61,
Edwards, D. A., Man, J. C., Brand, P., Katstra, J. P., Sommerer, K., Stone, H. A.,
Nardell, E., and Scheuch, G. (2004). Inhaling