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Occupational Exposure to Poultry Dust and Effects on

the Respiratory System in Workers
a b a a a a a
S. Viegas , V. M. Faísca , H. Dias , A. Clérigo , E. Carolino & C. Viegas
a
Higher School of Health Technology, Lisboa/Polytechnic Institute of Lisbon, Lisboa,
Portugal
b
CIESP—Centro de Investigação e Estudos em Saúde Pública, Escola Nacional de Saúde
Pública, ENSP, Universidade Nova de Lisboa, Lisboa, Portugal
Version of record first published: 20 Mar 2013.

To cite this article: S. Viegas , V. M. Faísca , H. Dias , A. Clérigo , E. Carolino & C. Viegas (2013): Occupational Exposure
to Poultry Dust and Effects on the Respiratory System in Workers, Journal of Toxicology and Environmental Health, Part A:
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 Journal of Toxicology and Environmental Health, Part A, 76:230–239, 2013
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ISSN: 1528-7394 print / 1087-2620 online
DOI: 10.1080/15287394.2013.757199

OCCUPATIONAL EXPOSURE TO POULTRY DUST AND EFFECTS

ON THE RESPIRATORY SYSTEM IN WORKERS

S. Viegas1,2, V. M. Faísca1, H. Dias1, A. Clérigo1, E. Carolino1, C. Viegas1

1
Higher School of Health Technology, Lisboa/Polytechnic Institute of Lisbon, Lisboa, Portugal
2
CIESP—Centro de Investigação e Estudos em Saúde Pública, Escola Nacional de Saúde Pública,
ENSP, Universidade Nova de Lisboa, Lisboa, Portugal
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Farmers are occupationally exposed to many respiratory hazards at work and display higher
rates of asthma and respiratory symptoms than other workers. Dust is one of the components
present in poultry production that increases risk of adverse respiratory disease occurrence.
Dust originates from poultry residues, molds, and feathers and is biologically active as it con-
tains microorganisms. Exposure to dust is known to produce a variety of clinical responses,
including asthma, chronic bronchitis, chronic airways obstructive disease (COPD), allergic
alveolitis, and organic dust toxic syndrome (ODTS). A study was developed to determine parti-
cle contamination in seven poultry farms and correlate this with prevalence rate of respiratory
defects and record by means of a questionnaire the presence of clinical symptoms associated
with asthma and other allergy diseases by European Community Respiratory Health Survey.
Poultry farm dust contamination was found to contain higher concentrations of particulate
matter (PM) PM5 and PM10 . Prevalence rate of obstructive pulmonary disorders was higher
in individuals with longer exposure regardless of smoking status. In addition, a high preva-
lence for asthmatic (42.5%) and nasal (51.1%) symptoms was noted in poultry workers. Data
thus show that poultry farm workers are more prone to suffer from respiratory ailments and
this may be attributed to higher concentrations of PM found in the dust. Intervention pro-
grams aimed at reducing exposure to dust will ameliorate occupational working conditions
and enhance the health of workers.

The first reports indicating health hazards
for workers in intensive livestock production
systems were published more than 20 years
ago (Donham et al., 1977; Hartung and Schulz,
2008). A number of syndromes have been
recognized in workers in the intensive animal
industries ranging from acute, which develops
within a few hours to days following exposure
to animal sheds, and which is accompanied
by a variety of clinical signs including lethargy,
a mild febrile reaction, headaches, joint and
muscle aches, and general malaise, to more
chronic responses. This condition is referred
to as organic dust toxic syndrome (ODTS) or
toxic alveolitis. The prevalence of ODTS ranges
from 10 to 30% in workers, depending on the
type of intensive animal production and use of
facilities (Donham, 1995; Hartung and Schulz,
2008).
Dust is one of the components present in
poultry production; it originates from poultry
residues, molds, and feathers, and is biologi-
cally active as it contains microorganisms, some
of which may be pathogens. Dust acts as a
host of biological fragments that may serve as a
sensitizer (Whyte, 2002). Exposure to dust pro-
duces a variety of clinical responses in individ-
uals. These include asthma due to sensitization
to allergens in the airspace, chronic obstructive
pulmonary disease (COPD), allergic alveolitis,
and ODTS (Iversen, 1999; Hartung and Schulz,
2008).

Address correspondence to S. Viegas, Higher School of Health Technology, Av. D. João II 4.69.01, 1990-096 Lisboa, Polytechnic
Institute of Lisbon. E-mail: susana.viegas@estesl.ipl.pt

230
 OCCUPATIONAL EXPOSURE TO POULTRY DUST
Farmers are exposed occupationally to
many respiratory hazards and have high rates of
asthma, inflammatory manifestations, and res-
piratory symptoms (Dosman et al., 1988; Toren
et al., 1991; Schenker et al., 1991; Fishwick
et al., 1997; Karjalainen et al., 2000; Willson
et al., 2008; Burch, 2010). Individuals involved
in animal production, especially pig and poul-
try farmers, display a higher prevalence of
adverse respiratory symptoms than other farm-
ers and other rural residents (Kogevinas et al.,
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1999; Senthilselvan et al., 1997; Novak, 1994;
Radon et al., 2001; Rimac et al., 2010).
Increased adverse respiratory symptoms and
decreased lung function have been observed
among swine and poultry workers (Novak,
1994; Senthilselvan et al., 1997; Radon et al.,
2001; Burch et al., 2010; Kogevinas et al.,
2009; Rimac et al., 2010) and among veteri-
nary surgeons (Karjalainen et al., 2000).
The suggestion that the primary clinical pro-
blem is an obstruction of the airways is suppor-
ted by various studies in which workers were
subjected to lung function tests. Although the
forced expiratory volume-in-one-second (FEV1)
was not changed in most individuals examined,
decreases in the FEV1/forced vital capacity (FVC)
ratio and flow rates were noted (Brouwer et al.,
1986; Haglind and Rylander, 1987; Dosman
et al., 1988, Hartung and Schulz, 2008). The
decrease in pulmonary airflow was correlated
to the dose of swine barn dust and a thresh-
old of susceptibility occurred after low, chronic
exposure to the dust (Cleave et al., 2010).
Poultry dust may also produce immune
responses against pathogenic biological agents.
The response may be acute, recurrent, or chronic
in the lungs, depending mainly on the frequency
and level of exposure (Alencar et al., 2004).
Several inflammatory agents are also present;
among them is bacterial endotoxin, which was
found to be related to the presence of decrease
in respiratory airflow and subjective symptoms
(Cleave et al., 2010; Burch et al., 2010). Another
biologically potent agent is (1/3)-b-D-glucan,
present in the cell wall of molds, which exerts a
suppressive effect on the immune system and is
correlated with a higher risk for atopic sensitiza-
tion against allergens (Rylander, 1986; Schuyler
231
et al., 1998; Rylander and Carvalheiro, 2006).
In addition, this organic dust is composed of feed
particles, dander, and gases (Whyte, 2002). The
particulate matter (PM) in poultry dust varies in
composition size and density, and these physical
parameters may influence the health of workers
due to aerosolization and bioaerosol contami-
nation (Just et al., 2009). In addition, dust may
be combined with ammonia, a common con-
taminant in this occupational setting that acts as
a respiratory insult and may result in acute or
chronic respiratory disease. In this case, respi-
ratory impairment includes chronic bronchitis,
hypersensitivity pneumonitis (allergic alveolitis),
occupational asthma, and toxin fever (Rylander,
1986; Whyte, 2002).
There are several tasks in the case of poul-
try work that give rise to dust, including laying
down litter; handling and inspection of birds;
vaccination; routine maintenance and cleaning
of houses during growth or production peri-
ods; catching or removing birds; removing litter
and/or manure; and other related or simi-
lar activities. However, there are some tasks
that normally involve higher exposure to dust,
namely, brushing down surfaces and sweeping,
and spreading litter (Whyte, 2002). The mate-
rial used for poultry litter (wood shavings) varies
but normally is constituted with pine shavings,
sawdust or eucalyptus, or other various types
of wood. In some regions rice hulls, peanut,
coffee, sugar cane, straw, hay, grass, and paper
processed are also used (Fernandes, 2004).
The aim of this study was to determine PM
contamination in seven poultry farms located
in Lisbon district, Portugal. In addition, it
was of interest to examine prevalence rate
of pulmonary disorders in workers and the
presence of clinical symptoms associated with
asthma and other allergy diseases using a ques-
tionnaire formulated by European Community
Respiratory Health Survey.
MATERIALS AND METHODS
Environmental Monitoring
Environment evaluations were performed
with portable direct-reading equipment
 232
(Lighthouse, model 3016 IAQ). Particles con-
centration measurement was performed in
five different sizes (PM0.5 ; PM1 ; PM2.5 ; PM5 ;
PM10 ). This technique was selected because
differentiation between particle size fractions is
important in order to quantify penetration of
dust within the respiratory system. Vincent and
Mark (1981) demonstrated that respirable dust
is the fraction of airborne dust that reaches the
gas exchange regions of the lung and is less
than 7 µm aerodynamic diameter in size from
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PM.5 to PM5 .
The measurements were conducted in the
vicinity of the nasal area of the workers and dur-
ing performance of different tasks in pavilions.
In most poultry farms, three measurements
were undertaken and the mean value obtained
for each particle size considered. In some cases
the number of measurements was reduced
because it was only pavilions with animals at
the time of measurements were examined. All
measurements were done continuously and
with 5 min duration. In all poultry farms stud-
ied, workers did not use respiratory protection
devices or other kind of protective equipment.
Subjects and Study Protocol
The study included 46 workers from the
7 poultry farms. An individual questionnaire
was applied to obtain data on (1) smok-
ing habits, (2) history of known lung disease,
(3) presence of respiratory symptoms, and
(4) exposure history. All workers gave written
informed consent.
Spirometries were performed using a
MK8 Microlab spirometer. The spirometer was
always calibrated prior to data collection, with
a 3-L syringe to a total of 12 L. Values from
calibration were accepted if there was not an
error greater than 3%. The spirometer used
meets the international standards with respect
to flow rate and duration of the test. The
test was done a minimum of three acceptable
times and repeatability was verified on the two
tests with largest forced vital capacity (FVC)
and forced expiratory volume in 1 s (FEV1 ),
according to ATS/ERS 2005 guidelines (Miller
et al., 2005). Respiratory function parameters
S. VIEGAS ET AL.
evaluated included FVC, FEV1 , FEV1 /FVC%,
and forced expiratory flow at different FVC vol-
umes (FEF 25, FEF50; FEF75, and FEF25-75).
A control group was not examined, as the
aim was to identify the prevalence rate of pul-
monary airway disturbances in exposed work-
ers. Taking this in consideration, the method-
ology normally used in lung function labs was
considered suitable. Therefore, results were
compared with reference values from European
Community for Coal and Steel (ECCS) (Quanjer
et al., 1993).
For interpretation purposes the fixed cut-
off of 80% of predicted was used. Pulmonary
airway disturbances were classified as fol-
lows: (1) obstructive—FEV1 /FVC% below 80%;
(2) restrictive—FEV1 and FVC below 80% with
a FEV1 /FVC % equal or above 80%; and
(3) nonspecific—FEV1 , FVC, and FEV1 /FVC%
below 80% or FEF below 60%.
Questionnaire of Clinical Symptoms
Epidemiological data were analyzed by
the validated questionnaire of Portugal of
the European Community Respiratory Health
Survey (ECRHS, 2007). This enables evalua-
tion of the prevalence of asthma and other
allergic disease, the characterization of respira-
tory, skin, and eye symptoms, and estimation
of the work related symptoms. Clinical data
were obtained by cross-sectional study. The
ECRHS questionnaire was completed by all
subjects from case and control sample groups,
in the form of an interview. The case sample
group included 47 poultry workers and con-
trols included 69 subjects without any type of
agricultural activities.
Statistical Analyses
Statistical analysis of all data was performed
using the Statistical Package for Social Sciences
(SPSS), version 20.0. Given the reduced sam-
ple size obtained in ventilatory capacity mea-
surements, frequency analysis and calcula-
tion of means and standard deviations were
used. The Mann–Whitney U-test was applied
to detect statistically significant differences
between genders, between smoking habits
 OCCUPATIONAL EXPOSURE TO POULTRY DUST 233

(smoker, nonsmoker), and in exposure time
(<10 years, ≥10 years). The criterion for sig-
nificance was set at p < .05.
RESULTS
Particle Assessment
With respect to PM contamination, the
ones with the larger dimension were detected
at higher concentrations, particularly PM5 and
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lung disease. From the 41 workers considered,
60.6% were males and 30.4% were females.
Mean age was 44.5 ± 12.4 years and mean
duration of exposure was 18.3 ± 11 years.
Concerning smoking habits, 43.9% were smok-
ers and 56.1% were nonsmokers. Data from
nonsmokers and smokers were analyzed sepa-
rately. Prevalence rate of obstructive pulmonary
ventilatory disturbances was higher in individ-
uals with longer exposure (31.7%) whether
they were smokers (17.1%) or nonsmokers

PM10 (Table 1). The distribution of particles size

(14.6%). No significant differences were found
showed the same tendency in all poultry farms;
with respect to duration of exposure, and with
however, farms A, C, and E presented higher
respect to spirometric parameters in both smok-
levels of contamination, particularly in PM10
ers and nonsmokers.
(Figure 1).

Spirometry Clinical Symptoms Obtained by

Table 2 shows the pulmonary ventilatory Questionnaire
capacity data of poultry workers. Five workers Forty-seven workers were analyzed, 16
(10.9%) were excluded because of previous (34%) women and 31 (66%) men. The

TABLE 1. Results Obtained in Each Poultry Farm (Mean Value, mg m−3 )

Poultry Number of
farms measurements PM0.5 PM1.0 PM2.5 PM5.0 PM10.0

A 4 4.7 × 10−3 8.2 × 10−3 6.1 × 10−2 1.1 6.5

B 3 1.1 × 10−2 2.4 × 10−2 1.1 × 10−1 1.0 4.0
C 1 2.9 × 10−3 8.9 × 10−3 1.2 × 10−1 2.0 15.2
D 3 2.8 × 10−3 4.7 × 10−3 2.0 × 10−2 3.4 × 10−1 2.1
E 3 1.4 × 10−2 3.2 × 10−2 2.4 × 10−1 2.4 6.5
F 3 2.5 × 10−2 3.1 × 10−2 8.4 × 10−2 8.0 × 10−1 3.6
G 2 5.0 × 10−3 7.5 × 10−3 2.4 × 10−2 2.2 × 10−1 1.4

20,0000

15,0000
PM0.5
PM1.0
PM ( mg/m3)

PM2.5
10,0000 PM5.0
PM10.0

5,0000

0,0000
A B C D E F G
Poultry units

FIGURE 1. Distribution by size of particle matter in each poultry farm (color figure available online).
 234 S. VIEGAS ET AL.

TABLE 2. Spirometry Data of Poultry Workers

Exposure
<10 ≥10
Count Min Max Mean SD Count Min Max Mean SD

Smoking
FEF25 % 8 80 131 101 15 12 57 148 87 24
Predicted
FEF50 % 8 56 92 79 11 12 41 102 67 23
Predicted
FEF75 % 8 26 95 70 22 12 18 87 54 25
Predicted
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FEF25/75 % 8 42 87 74 14 12 31 91 64 24
Predicted
FEV1 % 8 70 109 96 13 12 67 108 93 12
Predicted
FVC % 8 65 121 100 19 12 79 118 102 11
Predicted
Measured 8 71 93 82 7 12 62 85 74 8
FEV1/FVC
PEF % 8 71 123 100 17 12 70 136 103 19
Predicted
Nonsmoking
FEF25 % 6 82 119 100 15 20 43 131 95 25
Predicted
FEF50 % 6 58 155 99 33 20 24 149 89 33
Predicted
FEF75 % 6 55 153 97 44 20 15 140 77 35
Predicted
FEF25/75 % 6 57 147 96 34 20 22 137 82 30
Predicted
FEV1 % 6 88 132 105 15 20 54 130 100 22
Predicted
FVC % 6 87 122 104 12 20 65 141 103 20
Predicted
Measured 6 77 93 85 6 20 58 92 81 9
FEV1/FVC
PEF % 6 83 130 98 17 20 65 118 98 15
Predicted

Note. Min, minimum; max, maximum; SD, standard deviation.

prevalence of diagnosed asthma was 6.4%. All
asthmatic workers were previously diagnosed
with asthma, of which 66.7% reported the first
attack after 45 yr of age. Clinical data on res-
piratory symptoms demonstrated a trend to
high prevalence for asthmatic (42.5%) and nasal
(51.1%) symptoms in poultry workers. In con-
trast, skin and eye symptoms displayed a low
prevalence.
A high prevalence of respiratory symptoms
in workers without asthma was also observed,
including wheezing (n = 9; 19.1%) and cough-
ing (n = 14; 29.8%). Further, 12.8% (n = 6) of
the workers reported problems with sneezing,
runny nose, or stuffy nose without having a
cold or flu and also without medical diagno-
sis of rhinitis. In this study, six workers (12.8%)
reported having chest tightness or wheezing at
work, which was reported to be directly associ-
ated with their involvement in specific activities
in the workplace. Further, 13 (27.7%) of all the
enquired workers referred to an improvement
of their respiratory ability during the resting
days and holidays, suggesting an association of
respiratory disturbances with working activities.
However, these results were not found to be
statistically significant differences between indi-
viduals that displayed symptoms and those who
 OCCUPATIONAL EXPOSURE TO POULTRY DUST
did not. Nevertheless, it is important to note
that there was a trend for increased frequency
of upper and lower respiratory symptoms in
subjects exposed to higher concentration of
PM.
DISCUSSION
Our particle contamination results showed
higher density in PM5 and, predominantly
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in PM10 . These PM in the respirable range
(<5–7 µm) indicate that poultry dust PM pen-
etrate into the gas exchange region of the
lung (Vincent and Mark, 1981). Exposure to
PM10 may also produce disease by impacting
in the upper and larger airways below the vocal
cords. In addition, it is important to bear in
mind that organic poultry dust may serve as a
favorable medium for the persistence of numer-
ous species of bacteria and microscopic fungi,
which may release allergens and toxins that
exert different health effects in workers respira-
tory system (Millner et al., 2008). Tsapko et al.
(2011) in a recent review found a direct positive
correlation between the concentrations of dust
and microorganisms in the air of the working
zone. Ellen and colleagues (2000) observed in
poultry farms the same tendency with respect
to PM size distribution, namely, dust concen-
trations ranging from 0.02 to 81.33 mg m−3
for inhalable dust and 0.01 to 6.5 mg m−3 for
respirable dust.
Another aspect that is important to take
into account is the type of poultry produc-
tion farm: floor-housed operations and cage-
housed facilities, being the first ones correlated
with higher concentrations of dust because of
the use of litter (Just et al., 2009; Kirychuk
et al., 2010). In our investigation only farms
with floor-housed operations were considered.
Differences found between farms related
with PM size distribution may be due to many
factors such as environmental variables, venti-
lation rate, presence or absence of air cleaning
technologies, animal stocking density, type of
bird, bird age, and manure management meth-
ods (Banhazi et al., 2000; Oppliger et al.,
2008; HSE, 2008). In this particular case, it is
235
important to note that farms with only natural
ventilation showed higher levels of PM10 .
Concomitant with environmental monitor-
ing, the adverse health effects in exposed work-
ers were evaluated due to the fact that organic
dust is one of the most recognized respira-
tory hazards associated with animal production
(Rimac et al., 2010). Considering lung func-
tion, both smokers and nonsmokers with longer
exposure showed a higher prevalence rate of
obstructive pulmonary ventilatory disturbances.
This finding is in agreement with other studies
(Ávila, 1971; Kirychuk et al., 2003; Szczyrek
et al., 2011). However, prevalence cannot be
compared because criteria used to identify lung
function abnormalities were not always avail-
able. Rimac and colleagues (2010) found no
pulmonary ventilatory disturbances but only a
70% cutoff for FEV1/FVC was used instead of
the 80% or the 5th percentile proposed by
ATS/ERS (Zuskin et al., 1995).
No other lung function abnormalities were
found. These results may be related to the sam-
ple size, since restrictive and mixed defects are
also described in this type of workers (Alencar,
2004; Omland, 2011). However, findings need
to be based on reliable quality spirometries and
the presence of an FEV1% higher than FVC%,
observed in some studies, suggests poor subject
cooperation which may lead to confounding
conclusions (Steltner et al., 2004). In fact, if FVC
is not complete it is not possible to find airways
obstruction.
Radon and colleagues (2001) showed that
poultry workers are exposed to high concen-
trations of dust and have lower mean lung
functions. In our study, abnormal lung function
was not present in poultry workers. This differ-
ence may in part be explained by the known
“healthy worker effect” (HWE), a term applied
to the deficit of both morbidity and mortality
ascribed to various employment-associated fac-
tors when workers and the general population
are compared (Li and Sung, 1999; McMichael
et al., 1986; Burns et al., 2011, Burch et al.,
2010), which was previously noted in pop-
ulation occupationally exposed to allergens
(Rimac et al., 2010). This phenomenon occurs
because relatively healthy individuals are likely
 236
to gain employment and remain employed,
while severely ill and chronically disabled indi-
viduals are ordinarily excluded from employ-
ment (Moual et al., 2008; Thygesen et al.,
2011). In our study, the admission policy was
not known and data for workers that left their
jobs due to health problems related with poul-
try production work were not obtained. All
these data may contribute to a better explana-
tion of the results obtained.
Considering clinical symptoms, prevalence
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of asthma was found in 6.4%, which is numer-
ically lower than previously reported data
for the prevalence of asthma in the gen-
eral population (10%) and farmer workers
(7.7%) (Kogevinas et al., 1999; Bardana, 2003).
In addition, the prevalence of self-reported
work-related symptoms including eye, nose,
dermal, and asthma symptoms was quite similar
in poultry workers and controls. However, the
occurrence of nose and asthma symptoms in
poultry workers presented a higher prevalence
in comparison to eye and dermal symptoms,
which was expected due to continuous expo-
sure to poultry dust. Aerosol particles with a
mean aerodynamic diameter below 10 µm
are able to deeply penetrate the human air-
ways and can promote asthma manifestations
(Lauriere et al., 2008). It is of interest that 2 of
the workers reported that the first asthma attack
occurred after 45 yr of age, suggesting an influ-
ence of working activities in the development
of disease. This fact supports the possibility
that activities undertaken by poultry workers
may exert a negative effect in development of
respiratory disease, indicating the prevalence
of occupational asthma of 4.3% is consistent
with others European studies (Kogevinas et al.,
1999; Bardana, 2003). Further, a high preva-
lence of respiratory symptoms was observed in
professionals without asthma, directly related
with different farming activities, since it is espe-
cially aggravated during performance of those
activities.
Studies previously showed that poultry
workers may develop health problems pro-
vided by air contaminants present in the
workplace (Radon et al., 2001; Rylander and
Carvalheiro, 2006; Burch et al., 2010). Zuskin
S. VIEGAS ET AL.
and colleagues (1995) compared poultry work-
ers with a control group and noted a signif-
icantly higher prevalence of chronic cough,
chronic phlegm, chronic bronchitis, and chest
tightness in the former group.
Regarding preventive measures applied to
avoid exposure to poultry dust, one needs to
consider that some of these measures may
decrease the exposure but might increase
exposure to other contaminants. Associations
between respiratory findings and the use of
individual protection equipment were not stud-
ied because data from observations were
not consistent and the majority of workers
stated that they did not use this equipment.
Application of water mists reduces particles
suspension or resuspension during operations
but elevates relative humidity, which facilitates
ammonia production and microbial growth.
Therefore, occupational health interventions
may be complex and need to consider all
risk factors present in this occupational setting
(Whyte, 2002). Radon et al. (2001) demon-
strated that workers in animal houses that were
equipped with humidity sensors and auto-
matic ventilation achieved significantly higher
lung function results than those in buildings
with poor ventilation. The use of tractors and
combine harvesters that have enclosed cabs
equipped with air filtration also reduce inhal-
able grain dust levels (Linaker and Smedley,
2002).
CONCLUSIONS
Poultry dust is a complex mixture of organic
and inorganic materials as well as microbio-
logical and invertebrate contaminants. There
is evidence that inhalation exposure to these
materials at the levels likely to be encoun-
tered in poultry production may produce aller-
gic respiratory diseases and exacerbate exist-
ing respiratory allergies. However, the sever-
ity of the health problems might be more
affected by the composition of bio-aerosols
than just by PM contamination. Further stud-
ies are needed to improve understanding of
the poultry house environment and develop
 OCCUPATIONAL EXPOSURE TO POULTRY DUST
intervention programs aimed at improvement
and protection of respiratory health of poultry
workers.
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