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Effects of air pollution on children’s pulmonary health
Afrim Tabaku
a
,
*
, Gazmend Bejtja
a
, Silvana Bala
b
, Ervin Toci
a
, Jerina Resuli
a
a
Public Health Institute, Tirana, Albania
b
University Hospital for Lung Disease, Tirana, Albania
article info
Article history:
Received 8 June 2010
Accepted 17 July 2010
Keywords:
Air pollution
Children
Particulate matter
Total suspended matter
Pulmonary function
Respiratory disease
abstract
Introduction: Many reports regarding the effects of air pollution on children’s respiratory health have
appeared in the scientific literature. Some investigators found increases in persistent cough and phlegm,
bronchitis, and early respiratory infections in communities with poor air quality. The purpose of this
survey was to compare the pulmonary function of children living in urban area of Tirana city with
children living in suburban area of the city.
Material and methods: This survey is carried out during 20 04e2005 period on 238 children living in urban
area and in 72 children living in suburban area, measuring dynamic pulmonary function. A questionnaire
was used to collect data on sex, current respiratory symptoms, allergy diagnosed by the physician, parent
education and smoking habit of parents, presence of animals, synthetic carpets and moulds in their houses.
The selection of schools, and children included in this survey was done by randomized method. Also, we
have measured and classic air pollutants.
Results: Comparing the results of values of pulmonary function of two groups of children, we have shown
that differences were significant (p0.001), whereas comparing symptoms were for cough (p0.011) and for
phlegm (p0.032). The level of particulate matter (PM10) and total suspended matter (TSP) were over the
recommended limit values, whereas the levels of other pollutants have resulted within recommended
levels of World Health Organization (WHO)
Conclusions: The results of this survey suggest that air pollution is associated with respiratory health of
children causing a slight decrease in values of pulmonary function in children of urban area compared
with those of suburban area.
Ó2010 Elsevier Ltd. All rights reserved.
1. Introduction
Outdoor air pollution is also a major problem in developing
countries. The World Health Organization found that the air quality
in large cities in many developing countries is remarkably poor and
that very large numbers of people in those countries are exposed to
ambient concentrations of air pollutants well above the World
Health Organization guidelines for air quality (WHO, 1999, 2006).
Scientific understanding of the health effects of air pollution,
including effects on children, has increased in the last decade.
Children have increased exposure to many air pollutants
compared with adults because of higher minute ventilation and
higher levels of physical activity (Plunkett et al., 1992). Because
children spend more time outdoors than do adults, they have
increased exposure to outdoor air pollution (Wiley et al., 1991a,b).
Air pollutants (ozone, sulfur dioxide, particulate matter,
nitrogen dioxide) have respiratory effects in children and adults,
including increased respiratory tract illness, asthma exacerbations,
and decreased lung function (American Thoracic Society, 1996a,b;
Ostro et al., 2001; Yu et al., 2000; Leonardi and Houthuijs, 2002;
Hajat et al., 1999; Jedruchovski et al., 2000; Oftedal et al., 2008).
In adults, particulate air pollution is associated with respiratory and
cardiovascular hospitalizations, cardiovascular mortality (Dockery,
2001) and lung cancer (Pope et al., 2002). Air pollution also has
effects on indirect health indicators such as health care utilization
and school absences (American Thoracic Society, 1996a,b; Bates,
1995; Timonen et al., 2002; Avol et al., 2001).
Tirana is a city that sustains a rapidly growing population and it
has serious air pollution problems, especially by particulate matter,
which results from motor vehicle traffic, the development of
construction industry and the dense population. The purpose of this
survey was to compare the pulmonary function of children living
and attending schools in urban area of Tirana city, with children
living and attending schools in suburban area of the city.
Studies examining associations between adverse respiratory
tract health and traffic have been reviewed (Delfino, 2002).
Increased respiratory tract complications in children (e.g., wheezing,
*Corresponding author.
E-mail address: afrimtabaku@yahoo.com (A. Tabaku).
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Atmospheric Environment
journal homepage: www.elsevier.com/locate/atmosenv
1352-2310/$ esee front matter Ó2010 Elsevier Ltd. All rights reserved.
doi:10.1016/j.atmosenv.2010.07.033
Atmospheric Environment 45 (2011) 7540e7545

chronic productive cough, and asthma hospitalizations) have been
associated with residence near areas of high traffic density (Delfino,
2002; Edwards et al., 1994; van Vliet et al., 1997; Brunekreef et al.,
1997; Ciccone et al., 1998). Other investigators have linked various
childhood cancers to proximity to traffic(Feychting et al., 1998;
Pearson et al., 2000; Raaschou-Nielsen et al., 2001).
2. Material and methods
This survey was carried out during 2004e2005 period on 238
children living in urban area and in 72 children living in suburban
area, measuring pulmonary function, forced vital capacity (FVC),
forced expiratory volume in the first second after full inspiration
(FEV
1
), FEV
1
/FVC ratio, peak expiratory flow rate (PEF), forced expi-
ratory flow (FEF
25-75
), and vital capacity (VC). Each subject produced
at least three acceptable FVC curves based on ATS standards
(Standardization of spirometry, 1995). Testing was preceded and
followed by flow calibrations done with a 3-L volumetric syringe
(Standardization of spirometry, 1995). A questionnaire was used to
collect data on sex, current respiratory symptoms, allergy diagnosed
by the physician, parent education, parental history of atopy, envi-
ronmental tobacco smoke at home, use of gas, wood or electricity
for heating and cooking, home dampness, visible indoor moulds,
and the keeping of pets (Jedrychowski et al., 1998). The selection of
schools, and children included in thissurvey was done by randomized
method. Also, we have measured air pollutants, for particulate matter,
sulfur dioxide, nitrogen oxides, ozone and total suspended matter. Air
samples were collected in five stationary points allocated in the city
and are analyzed for total suspendedmatter (TSP), particulate matter
(PM
10
) by gravimetric cascade impact method, sulfur dioxide (SO
2
),
nitrogen oxides (NOx), and ozone (O
3
)(James and Lodge, 1988)
Statistical processing of the data was carried out using Statistical
Package for Social Science (SPSS 15). Multiples regression is used to
analyze the correlation between variables.
3. Results
A summary of 2004 average air pollution levels for PM
10
,O
3,
NO
2
,SO
2
and TSP appears in Graphs 1 and 2.
Data on urbanesuburban comparison of pulmonary function
are presented in Table 1.
4. Discussion
Air pollution in Tirana originates mostly from motor vehicle
traffic exhausts (especially diesel exhausts), road dust and
construction industry. As a result, concentrations of airborne parti-
cles are generally high, as well as some other pollutants.
The most important ambient air pollutants associated with
adverse health effects are particulate matter, ozone, oxides of
nitrogen and sulfur dioxide Motor vehicles pollute the air through
tailpipe exhaust emissions and fuel evaporation, contributing to
carbon monoxide, PM
2.5
, nitrogen oxides, hydrocarbons, other
hazardous air pollutants (HAPs), and ozone formation. Motor vehi-
cles represent the principal source of air pollution in many commu-
nities, and concentrations of traffic pollutants are greater near major
roads (Zhu et al., 2002). Recently, investigators have found increased
adverse health effects among those living near busy roads.
Particles less than 1
m
m in diameter can easily enter into the
distal portions of the lung and the systemic circulation. Moreover
they act as vehicles transporting toxic chemicals into the human
respiratory system (Zhiqiang et al., 2000).
Total airborne dust concentrations in air of urban area of city
oscillated from 146e964
m
gm
3
. Respirable dust concentration
varied from 73e445
m
gm
3
(Graph 1). The averages of these data
on air pollution exceed threshold limits values (WHO, 1999, 20 06).
Results of our survey showed that sulfur dioxide and nitrogen
oxides levels (Graph 2) are within limits of WHO (WHO, 1999,
2006), whereas the levels of ozone has the tendency to increase.
The results of our study indicate that spirometric lung-function
measurements of urban children were consistently lower than
those of suburban children. Application of Levine’s test, as is pre-
sented in Table 1 revealed that this difference was significant
P<0.001 level for FVC, FEV
1
and PEF. The average percentage
predicted FVC and FEV
1
in the urban area were 12.2% and 8.1% less
than those of the suburban area, respectively. This difference could
not be explained by urban-suburban variations in (a) anthropo-
metric measurements of the children; (b) exposures to potential
sources of indoor air pollutants (e.g., cooking and heating fuels);
(c) parental smoking patterns; or (d) socioeconomic status.
The decrements in lung function were, however, associated with
differences in ambient levels of PM
10
between areas.
To assess whether other variables contributed to the lower
lung function of the urban children, we explored nutritional status
(Table 2) indoor air quality (Table 3), and socioeconomic status
(Table 4). We examined three potential sources of indoor pollut-
ants: cooking and heating sources, and tobacco smoke.
We categorized cooking and heating sources (e.g., fuel oil,
kerosene, wood) on the basis of their fume-generating capability as
0 200 400 600 800 1000
μ
g
/m3
Tirana 1
Tirana 2
Tirana 3
Tirana 4
Tirana 5
CONCENTRATIONS OF TSP AND PM 10
IN URBAN AIR OF TIRANA
PM 10
TSP
Graph 1.
0
20
40
60
80
100
120
3m/gμ
anariT 1
ri
Taan2
Tari na3
Tari na4
5anariT
CONCENTRATIONS OF SO2, NOx AND O3
IN URBAN AIR OF TIRANA
Suffur dioxide
Nitrogen oxide s
Ozone
Graph 2.
Table 1
Urbanesuburban comparison of pulmonary function.
Urban group Suburban group P
FVC 2085.294 668.3199 2412.708 761.3831 0.0010
FEV
1
2073.197 657.828 2412.861 761.3831 0.0007
PEF 4823.227 1274.764 5518.167 1500.794 0.0001
A. Tabaku et al. / Atmospheric Environment 45 (2011) 7540e7545 7541

fume-generating sources, Suburban households used more fume-
generating cooking and heating sources, (p0.032) than urban
homes. Regarding smoking habits of parents, we did not obtain
significant differences between two groups (p0.093).
Socioeconomic status is a risk factor for respiratory disease. The
indices we used to assess socioeconomic status in this study
were size of household, rooms in the house, and education level of
parents. The number of rooms per household and the number
of people in the household did not differ significantly between the
suburban and urban areas (p0.329). Regarding parental educations,
according this survey there are significant differences in maternal
educations between two groups (p0.045), whereas for paternal
education no significant differences were observed (p0.234).
The respiratory symptoms we investigated in the questionnaire
were coughing, phlegm, and wheezing. In addition, we assessed
the prevalence of physician-diagnosed asthma. A summary of the
frequency of reported respiratory symptoms is presented inTable 5.
Regarding the symptoms we found significant differences
between two groups of children for wheezing during physical
activity (p0.022), cough with cold (p0.011) and phlegm with cold
(p0.036), whereas for asthma diagnosed by physician we didn’t
notice any significant difference (p0.208). Also, for other symptoms
like cough for three consecutive months and phlegm for three
consecutive months we didn’t ascertain any significant differences,
(p0. 45 and p0.0650) respectively.
The most significant air pollutant in Tirana that has consistently
exceeded established air-quality guidelines are TSP and PM
10
.The
findings of lower FEV
1
and FVC in the more polluted urban envi-
ronment are in agreement with the current literature, and recently,
results of several studies have pointed to particulates as the main
factor in morbidity and mortality associated with air-pollution
episodes (Edwards et al.,1994; van Vliet et al.,1997; Brunekreef et al.,
1997; Ciccone et al.,1998; Feychtinget al., 1998; Pearson et al., 2000;
Raaschou-Nielsen et al., 2001), as well as for decrements in pulmo-
nary function associated with air pollution. The association between
decrements in pulmonary function and TSP/PM
10
levels suggested
in this study has also been documented in other international
studies (American Thoracic Society, 1996a,b; Ostro et al., 2001; Yu
et al., 2000; Leonardi and Houthuijs, 2002; Hajat et al., 1999;
Jedruchovski et al., 2000; Oftedal et al., 2008).
In their study of adult pulmonary function in relation to TSP and
SO
2
levels (Xu et al., 1991), also proposed that FVC may be a better
indicator than FEV
1
for the assessment of effects of long-term
cumulative exposure to air pollutants. In our survey, comparison of
the spirometric lung function of urban children with suburban
children revealed a similar trend (i.e., a larger decrement of FVC
12.2% than FEV
1
8.1%). This trend is consistent with the hypothesis
(Xu et al., 1991; He et al., 1993) that changes in FVC may be more
reflective of long-term, cumulative exposures than changes in FEV
1.
High levels of ambient air pollutants are associated with
increased incidence or worsening of asthma and increased risk of
developing allergic diseases, respiratory symptoms and respiratory
tract infections. The underlying mechanism for the harmful effects is
the generation of oxidative stress which induces a strong respiratory
as well as systemic inflammatory response. Individuals with genetic
defects in enzymes associated with antioxidant defenses seem to be
particularly vulnerable to the harmful effects of air pollutants.
Children seem to be particularly susceptible to the harmful
effects of ambient air pollution because their lungs are growing.
Lung growth is guided by a complex and precisely timed sequence
of chemical messages. Many ambient air pollutants are chemicals
that have the potential to interfere with these signaling pathways
(Trasande and Thurston, 2005).
Compared with adults, children have poor defenses against PM
and gaseous air pollutants, have a differential ability to metabolize
and detoxify environmental agents and have an airway epithelium
that is more permeable to inhaled air pollutants (Schwartz, 2004).
Also, children have a greater level of physical activity than adults
(an average physical activity duration of 124 versus 21 min per day)
(Salvi, 2007), hence the intake of air into the lungs is much greater
than adults per day. Children spend more time outdoors than
adults, particularly in the summer and in the late afternoon. Some
of that time is spent in activities that increase ventilation rates.
Table 2
Urbanesuburban comparison of anthropomorphic data.
Urban Suburban Urban vs. Suburban
Arit. mean SD Arit. mean SD P
Age 13.76 0.67 13.54 0.62 0.014
Height 160.18 11.31 162.27 27.83 0.529
Weight 51.80 9.78 50.59 9.82 0.362
BMI 20.23 4.65 19.23 5.02 0.184
Table 3
Urban eSuburban Comparison of Home Environmental Exposure
Source Urban Suburban Urban vs. suburban
P
Fume generating heating and cooking sources (gas liquid petrol þwood)
No 78 (33.1) 15 (20.0) 0.032
Yes 158 (66.9) 60 (80.0)
Smoking in home
No 129 (54.2) 46 (63.89) 0.121
Yes 109 (45.8) 26 (36.11)
Table 4
Urbanesuburban comparison of socioeconomic status.
Urban Suburban Urban vs. suburban
P
Paternal education
Primary school 42 (17.8) 20 (26.7) 0.234
High school 135 (57.2) 37 (49.3)
College 59 (25.0) 18 (24.0)
Maternal education
Primary school 46 (19.5) 25 (33.3) 0.045
High school 145 (61.4) 38 (50.7)
College 45 (19.1) 12 (16.0)
Parent’s allergy
No 193 (81.43) 65 (91.55) 0.043
Yes 44 (18.57) 6 (8.45)
People/room
1.33 1.21 0.329
Table 5
Urbanesuburban comparison of respiratory symptoms.
Number of children with
respiratory symptoms
Urban Suburban P(urban vs
suburban)
Wheezing during physical activity 28 (11.9) 15 (20.8) 0.022
Cough apart the cold 52 (22.0) 20 (27.8) 0.376
Cough with cold 41 (17.4) 23 (31.9) 0.011
Cough for 3 consecutive months 8 (3.4) 4 (5.3) 0.45
Phlegm apart the cold 13 (5.5) 8 (11.1) 0.128
Phlegm with cold 66 (28.0) 28 (38.9) 0.036
Phlegm for 3 consecutive months 5 (2.1) 5 (6.7) 0.065
Asthma 4 (1.7) 3 (4.16) 0.205
A. Tabaku et al. / Atmospheric Environment 45 (2011) 7540e75457542

A recent study from Japan has demonstrated that intrauterine
exposure to high levels of traffic-related air pollutants and/or such
exposure soon after birth increases the risk of developing allergic
disorders in infants (Miyake et al., 2010).
A number of epidemiological studies have reported associations
between residential and school proximity to busy roads as a surro-
gate for high levels of ambient air pollution, and a variety of adverse
respiratory health outcomes in children, including presence of
respiratory symptoms and worsening of asthma exacerbations
(Wjst et al., 1993; Behrens et al., 2004; Gilliland, 2009; Sucharew
et al., 2010; Brauer et al., 2007, 2002; Gehring et al., 2010).
A recent study from Cincinnati, OH, USA, revealed that children
exposed to the highest tertile of traffic exhaust had a 45% increased
risk of recurrent dry cough at night compared with children
who were less exposed (Gauderman et al., 2004). In literature
(Gauderman et al., 2000, 2002) are reported positive associations
between markers of traffic-related air pollution and respiratory
health outcomes, including asthma onset, incidence of wheeze, ear-
enoseethroat infections and serious colds or flu in a large cohort of
children4 yrs of age, effects that were first noted at the age of 2 years .
A growing number of studies also showed that children living in
homes that are situated near roads with heavy truck traffichavean
increased risk of new-onset asthma and asthma exacerbations
accompanied by increased school absenteeism and asthma-related
hospitalizations (Kinney et al., 1996; White et al., 1994).
More recently, a Dutch study has reported that ambient PM air
pollution mainly arising from motor vehicular exhausts was
significantly associated with increased incidence of asthma among
schoolchildren (Gehring et al., 2010). The authors of a study that
investigated the association between the prevalence of wheeze and
allergic symptoms and truck traffic density in 13 and 14 yr old
school children from Munster, Germany (Behrens et al., 2004),
reported that compared with children who lived in ‘never exposed
to truck traffic areas’, those children who lived in areas with rare,
frequent and constant flow of truck traffic had a 29%, 58% and 57%
increased prevalence of wheeze, respectively.
In a prospective study of 10-yr-old children that started with
1759 children and lasted for 8 yrs, (Gauderman et al., 2004)was
found a significant association between lung function parameters
FEV
1
and ambient levels of NO
2
, acid vapor, PM
2.5
and elemental
carbon, even after controlling for known confounding factors.
Children who lived in areas with relatively higher ambient PM air
pollution had a significant decrease in FEV1 values compared with
children who lived in areas with lower PM air pollution levels. These
effects were similar in males and females and remained significant
even among children with no history of asthma. The magnitude of
these effects was similarto those observed due to effects of maternal
smoking reported in earlier studies (Gilliland, 2009; Sucharew et al.,
2010; Brauer et al., 2007, 2002; Gehring et al., 2010).
Children in communities with higher levels of urban air pollu-
tion (acid vapor, nitrogen dioxide, particulate matter with a median
aerodynamic diameter less than 2.5
m
m (PM
2.5
), and elemental
carbon which is a component of diesel exhaust had decreased lung
function growth, and children who spent more time outdoors had
larger deficits in the growth rate of lung function (Gauderman et al.,
2000, 2002).
Ozone is a powerful oxidant and respiratory tract irritant in
adults and children, causing shortness of breath, chest pain when
inhaling deeply, wheezing, and cough (Gauderman et al., 2000).
Children have decreases in lung function, increased respiratory
tract symptoms, and asthma exacerbations on days with higher
levels of ambient ozone (Gauderman et al., 2002; Kinney et al.,
1996; White et al., 1994; Thurston et al., 1997, 1994; Ostro et al.,
1995; Tolbert et al., 2000). Increases in ambient ozone have been
associated with respiratory or asthma hospitalizations, emergency
department visits for asthma (McCreanor et al., 2007) and school
absences for respiratory tract illness (Gilliland et al., 2001).
PM
10
is small enough to reach the lower respiratory tract and
has been associated with a wide range of serious health effects.
PM
10
is a heterogeneous mixture of small solid or liquid particles
of varying composition found in the atmosphere. Fine particles
(PM
2.5
) are emitted from combustion processes (especially diesel-
powered engines, power generation, and wood burning) and from
some industrial activities. Coarse particles (diameter between 2.5
and 10 m) include windblown dust from dirt roads or soil and dust
particles created by crushing and grinding operations. Toxicity of
particles may vary with composition (Ghio et al., 2002; Pandya
et al., 2002).
In children, particulate pollution affects lung function and lung
growth (Oftedal et al., 2008; Brunekreef et al.,1997;Gauderman et al.,
2004, 2000, 2002). In a prospective cohort of children living in
southern California,children with asthma living incommunities with
increased levels of air pollution (especially particulates, nitrogen
dioxide, and acid vapor) were more likely to have bronchitis symp-
toms. In thisstudy, bronchitis symptoms refers toa parental report of
“one or more episodes of ‘bronchitis’inthe past 12 months”or report
that, “apart from colds, the child usually seems to be congested in the
chest or able to bring up phlegm (Gauderman et al., 2004). The same
mix of air pollutants was also associated with deficits in lung growth
(as measured by lung function tests) (Gauderman et al., 2004).
The relative contribution of fine versus coarse particles to
adverse health effects is being investigated. In studies of cities on the
East Coast, fine particles seem to be important (Ostro et al., 2000).
In other areas, coarse particles have a stronger or similar effect
(Laden et al., 2000; Ozkaynak and Thurston, 1987). Several studies
have found that fine particles from powerplants and motor vehicles
or industrial sources may be more closely associated with mortality
(Woodruff et al., 1997).
Epidemiologic studies have reported relationships between
increased ambient nitrogen dioxide and risks of respiratory tract
symptoms) and asthma exacerbations (Ostro et al., 2001; Yu et al.,
2000; Leonardi and Houthuijs, 2002; Hajat et al., 1999; Jedruchovski
et al., 2000; Oftedal et al., 2008).
The epidemiologic studies of health effects associated with
nitrogen dioxide should be interpreted with caution. Increased levels
of ambient nitrogen dioxide may be a marker for exposure to traffic
emissions or other combustion-related pollution. An independent
role of nitrogen dioxide cannot be clearly established because of
the high covariation between ambient nitrogen dioxide and other
pollutants. Nonetheless, these studies illustrate that adverse respi-
ratory tract effectsare seen in urban areas where traffic is a dominant
source of air pollution.
Public health interventions to improve air quality can improve
health at the population level. A decrease in levels of air pollution
in former East Germany after reunification was associated with
improved lung function (Frye et al., 2003).
This survey has several strengths; it is the only published study
of the effects of ambient air pollution on children’s lung function in
Albania. Other strengths is significant difference in pulmonary
function between urban versus suburban group, good exposure
data, a well-selected control group, and an extensive search for
possible confounding variables.
We would like to mention and some weaknesses of our survey, as
although, for the purposes of this analysis, the highest value of
three efforts was defined as the child’speakflow value, there was
wide variability withinsubjects. In contrast, there wasfar less within-
subject variability in the lung-volume measurements. Another
concern is that not all of the spirograms met the ATS criteria for
reproducibility, indicating variable effort. Also, some of the total
measured lung volumes were lower than expected for height and
A. Tabaku et al. / Atmospheric Environment 45 (2011) 7540e7545 7543

weight, indicating sub maximal effort; however, because this effort
was observed in both urban and suburban spirograms and with
similar frequency, there wasno bias in urban-suburban comparisons.
As a conclusion, in an urban-suburban comparison of lung
function and symptoms in Tirana, higher pollutant levels in the
urban area were associated with lower lung function among chil-
dren aged 14e15 years. This difference was not explained by indoor
air quality, environmental tobacco smoke, differences in socioeco-
nomic status, or by nutritional status. We believe that further
research is needed because the pollutant levels and health effects
measured are consistent with those in studies in other parts of the
world and the levels and effects could indicate an important and
potentially irreversible response to ambient pollutants.
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