Environ Sci Pollut Res (2014) 21:3680–3685

DOI 10.1007/s11356-013-2335-0

RESEARCH ARTICLE

Biomonitoring air quality during and after a public

transportation strike in the center of Uberlândia, Minas
Gerais, Brazil by Tradescantia micronucleus bioassay
Boscolli Barbosa Pereira & Edimar Olegário de Campos Jr. &
Euclides Antônio Pereira de Lima & Marcos Antonio Souza Barrozo &
Sandra Morelli

Received: 27 August 2013 / Accepted: 4 November 2013 / Published online: 26 November 2013
# Springer-Verlag Berlin Heidelberg 2013

Abstract The aim of this study was to address the lack of
information concerning the air quality in the city of
Uberlândia, Minas Gerais, Brazil. In this study, we conducted
an unprecedented experiment involving the in situ biomoni-
toring of air genotoxicity in the city center during and after a
public transportation strike using the Tradescantia micronu-
cleus test. The frequency of micronuclei was significantly
higher in the city center compared with the reference site
(Mann–Whitney test, p <0.05), with the highest MN levels
being observed during public transport stoppage (Kruskal–
Wallis, Dunn p <0.01). In addition, the multiple linear regres-
sion analyses revealed that the low circulation of buses during
public transport stoppage and the increase in the concentration
of particulate matter from the increased flow of vehicles in the
city center during the strike positively influenced the MN
frequency. The climatic factors did not change during the
biomonitoring period, reflecting the fact that climatic factors
did not influence the MN frequency.

Responsible editor: Philippe Garrigues Keywords Biomonitoring . Urban air genotoxicity . Vehicle
B. B. Pereira (*) pollution . Tradescantia -micronuclei test
Department of Environmental Health, Laboratory of Vigilance in
Environmental Health, Federal University of Uberlandia, Santa
Monica Campus, Avenida João Naves de Ávila, 2121,
38.400-902 Uberlandia, Minas Gerais, Brazil Introduction
e-mail: boscolli86@hotmail.com

E. O. de Campos Jr. : S. Morelli

The economic development, increasing rates of urbanization,
Department of Genetics and Biochemistry, Laboratory of political and fiscal incentives for the production and purchase
Cytogenetics and Mutagenesis, Federal University of Uberlândia, of vehicles and particularly, the lack of public policies encour-
Umuarama Campus, Avenida Pará, 1720, 38.400-902 Uberlândia, aging and modernizing public transportation have all been
Minas Gerais, Brazil
cited as causal factors for the significant increase in individual
E. O. de Campos Jr. motorization in Brazil.
e-mail: edimarcampos@yahoo.com
The city of Uberlândia in southeast Brazil contained 313,950
S. Morelli vehicles in 2010, representing the second largest fleet in the state
e-mail: morelli@ufu.br
of Minas Gerais. Data from the National Traffic Department
E. A. P. de Lima (Departamento Nacional de Trânsito - DENATRAN 2010)
Department of Environmental Engineering, Sociedade Educacional show that the motorization rate in the city of Uberlândia in
Uberabense, Avenida Rondon Pacheco, 2000, 2010 was 52 vehicles per 100 inhabitants, while the national
38.408-343 Uberlândia, Minas Gerais, Brazil
average was 34 vehicles per 100 inhabitants.
e-mail: euclidesapl@yahoo.com
In Uberlândia, as in any other large urban center, increasing
M. A. S. Barrozo numbers of vehicles have intensified traffic, causing conges-
Science and Technology Center, School of Chemical Engineering, tion and inconvenience. Additionally, the combustion of fuel
Federal University of Uberlandia, Santa Monica Campus, Avenida
for automotive engines contaminates the urban atmosphere
João Naves de Ávila, 2121, 38.400-902 Uberlandia, Minas Gerais,
Brazil with ozone, sulfur and nitrogen oxides, heavy metals, organic
e-mail: masbarrozo@ufu.br compounds, and particulate matter, causing damage to the
Environ Sci Pollut Res (2014) 21:3680–3685
environment, and consequently, to human health (Kampa and
Castanas 2008).
Public transportation in Uberlândia essentially consists of
buses, as there are no trains or subways in the city. On
weekdays, approximately 240 buses pass through the city
center every hour (SETTRAN 2011). On May 17, 18, and
19 2010, the public transport workers of Uberlândia went on
strike, reducing the bus traffic to approximately 50 % of the
normal amount observed on working days. As there is a lack
of information concerning the air quality in the city, and the
occurrence of the strike presented an opportunity to conduct a
natural experiment, we attempted to biomonitor air
genotoxicity in the city center during and after the public
transportation strike using a Tradescantia micronucleus test.
According to Misík et al. (2011), many studies have used
plants to biomonitor the effects of genotoxic agents on the
environment. The simplicity, low cost, and high sensitivity of
the Tradescantia micronucleus test (TRAD-MN) has contrib-
uted to the popular use of this technique for detecting the
clastogenic effects of vehicular emissions in Brazil (Batalha
et al. 1999; Carvalho-Oliveira et al. 2005; Guimarães et al.
2000; Meireles et al. 2009; Savóia et al. 2009; Umbuzeiro
et al. 2008) and other countries (Carreras et al. 2006; Klumpp
et al. 2006; Misík et al. 2006; Prajapati and Tripathi 2008;
Villarini et al. 2009).
Therefore, the aim of this unprecedented experiment was to
provide evidence demonstrating the importance of
monitoring/controlling pollutant emissions in high-traffic
areas and of investing in public transport as an option to
reduce pollutant emissions from automobiles.
Material and methods
Monitoring and reference sites
The area outside the central transportation terminal in the city
center of Uberlândia (18° 54′47.37″S, 48°16′31.83″W) was
selected as the monitoring site because this area typically has
the highest frequency of bus traffic. To ensure the absence of
vehicular traffic, the orchard at the Institute of Biology, Fed-
eral University of Uberlândia (18°53′08.85″S, 48°15′34.64″
W) was used as a reference site (control). Although the study
sites (monitoring and reference) were relatively close, the
orchard at the Institute of Biology, Federal University of
Uberlândia is far from parking and vehicle traffic.
Both study locations (monitoring and reference) were lo-
cated near the city's Climatological Station (18°55′01.63″S,
48°15′20.60 W), which provided information concerning the
daily climatic conditions during the testing period. The Mu-
nicipal Traffic and Transportation Department (Secretaria Mu-
nicipal de Trânsito e Transportes - SETTRAN) estimated and
reported the number of buses that passed through the
3681
monitored site. The data for the particulate matter (PM10) were
obtained using a high volume sampler (Hi-Vol, Energética,
Brazil) installed in the area outside the Central Public Trans-
port Terminal.
Cultivation and exhibition of plants
The plant species Tradescantia pallida (Rose) Hunt. cv.
purpurea Boom was used for this study. The plants were
derived and propagated from the same parent and grown in a
greenhouse at the Federal University of Uberlândia under
controlled temperature, humidity, and lighting conditions.
The growing conditions consisted of the use of the reference
soil type ED73, commercial liquid fertilizer NPK (10:10:10),
weekly irrigation and temperature, and relative humidity var-
iations between day and night at 26/19 °C and 64/70 %,
respectively. A photoperiod of 16 h was used for flowering
induction.
Twenty inflorescences were exposed daily from May 17 to
May 23 2010 in the city center and at the reference site. The
inflorescences were exposed each day during the same daily
public transportation circulation period in the city at each site
between 06:00 a.m. and 11:59 p.m., totaling 18 h of exposure
per day during the three-day transportation stoppage and for
4 days after the stoppage.
In accordance with the suggestions of Klumpp et al.
(2006), boxes were built to house the plants (25 × 25 ×
35 cm) and to reduce the influence of external factors on the
responses obtained. The tops and sides of the boxes were
covered with shadind fabric (50 %) to protect the plants from
excessive heat and sunlight. The plant boxes were placed on
supports at 2 m off the ground to prevent the pollutants in the
soil from reaching the plants.
Trad-MCN assay
According to the protocol of Ma et al. (1994), five young
inflorescences were collected from each site during every day
of the testing period. The inflorescences were immediately
fixed in an absolute ethyl alcohol and 45 % acetic acid (3:1)
solution. After 24 h of fixation, the inflorescences were trans-
ferred to a 70 % alcohol solution and stored at 6 °C until
further preparation.
For the slide preparation, the young inflorescences were
dissected to expose the anthers. After the disposal of the
flower bud fragments, a drop of acetic carmine dye (2 %)
was applied to the anthers, and the samples were carefully
covered and pressed underneath a coverslip. Five slides
were prepared from each site during every day of the
monitoring period. The number of micronuclei in 300
tetrads per slide was counted using an optical microscope
at 400× magnification, and the results were expressed as a
percentage (frequency of micronuclei in 100 tetrads). The
3682
slides were coded during analysis and decoded at the end
of the cytogenetic testing period.
Statistical analysis
The Mann–Whitney test was used to compare the frequency
of micronuclei between the monitored site (town center) and
the reference site (Umuarama campus). Additionally, the
Kruskal–Wallis test and multiple comparisons (Dunn test)
were used to identify the monitored events with the highest
frequency of micronuclei.
Analysis of variance, ANOVA F-tests were conducted on
the climatological data to determine if variations existed dur-
ing the study period.
A multiple linear regression analysis was used to evaluate
the relationship between the frequency of micronuclei, the
concentration of particulate matter emitted, bus traffic, and
the influence of climatic conditions (air temperature, relative
humidity, solar radiation, and precipitation) in the monitored
locations. The regression equation obtained showed only the
factors that contributed significantly to the variations in MN
frequency.
Results and discussion
According to DENATRAN (2010), Uberlândia has one of the
largest automotive fleets in Brazil. A reduction in the number
of circulating buses during the 3 days of the strike, as shown in
Fig. 1, was reflected in the intensification of traffic in the city
center due to the increased use of private cars, taxis, and vans,
thus raising the level of pollutant emissions.
According to the results of the study, which was conducted
over a 7-day evaluation period, higher levels of particulate
matter were observed on days when there was a public trans-
port stoppage and four days after the strike showed the lowest
concentrations (Fig. 2).
Fig. 1 Frequency of buses
passing in the monitored site
(town center) per hour (buses/h)
in Uberlândia, Brazil, during the
strike days, non-strike days, and
weekend (Saturday and Sunday)
Environ Sci Pollut Res (2014) 21:3680–3685
Although the PM10 levels in the city center of Uberlândia
during the evaluation period did not exceed the recommended
daily limit of 50 μg/m3 in accordance with the “Conselho
Nacional de Meio Ambiente” - CONAMA Resolution No.
003/1990 (CONAMA 2005). This study revealed that the
monitored environment (center of Uberlândia) was associated
with the occurrence of genotoxic events, as observed from the
TRAD-MN test.
As shown in Table 1, the MN frequency was significantly
higher in the city center area (monitored site) than in the reference
location, and according to the Dunn test, the highest MN levels
were observed on the public transport stoppage days.
The relationships among the MN frequency, PM10 concen-
trations, bus traffic, and climatic conditions of the monitored
events were determined using a multiple regression analysis
(Fig. 3). The mathematical model that best represents the
prediction of micronuclei frequency (Y) includes only the
variables concerning the PM10 daily concentration (X 1 ) and
bus fleet in circulation (X 2 ) and is represented with the fol-
lowing equation:
 
log10 MN ¼ 0:8145 þ 0:0685X 1 þ ð−0:0032X 2 Þ; R2 ¼ 0:72; F ¼ 18:01; p < 0:001 :
According to the data obtained from the multiple linear
regression analysis, the variables X 1 and X 2 accounted for
73.27 and 3.33 % of the coefficient of determination (R 2 ),
respectively. The air temperature (X 3 ), relative humidity (X 4 ),
sunshine (X 5 ), and rainfall (X 6 ) variables were not considered
in the regression curve analysis because they were accounted
for only 3.2 % of the R 2 .
As observed in Table 2 the temperature means and relative
humidity means had no significant variations during this study
(ANOVA, p =0.74 and p =0.65, respectively). Because the
weather conditions in the city of Uberlândia were generally
constant, it was possible to attribute the main cause of the
genotoxic events of the present study to increased vehicular
traffic (and increased air pollution), according to the multiple
linear regression analysis. However, the long-term
Environ Sci Pollut Res (2014) 21:3680–3685 3683

Fig. 2 Concentrations of
particulate material (PM10) at the
monitored site (town center) in
Uberlândia, Brazil, during the
strike days, non-strike days, and
weekend (Saturday and Sunday)

biomonitoring performed during different seasons using the
TRAD-MN test has shown the direct influence of environ-
mental factors, particularly those derived from changes in the
relative humidity. Low relative air humidity promotes stoma-
tal opening and thereby increases the absorption and transport
of mutagenic substances in these cells (Klumpp et al. 2006).
The data provided of the Kruskal–Wallis test and multiple
linear regression analysis revealed that the low bus circulation
during the public transport stoppage and the increase in partic-
ulate matter concentration (a consequence of the increased flow
of vehicles in the city center during the strike) were factors that
positively influenced MN frequency in the T. pallida tetrads.
Although the results obtained from monitoring the urban
environment in a specific situation are difficult to reproduce,
other studies in Brazil and other countries corroborate these
results, reinforcing the idea that the air in regions with intense
vehicular traffic show the greatest genotoxic potential (Isidori
et al. 2003; Meireles et al. 2009; Crispim et al. 2012; Pereira
et al. 2013), even in situations with PM10 concentrations of
less than 50 μg/m3 (Isidori et al. 2003; Guimarães et al. 2000).
Ten years ago, it would have been reasonable to argue that
during a citywide public transport stoppage, there would be a
reduction in the overall levels of vehicle emissions. However,
the current trend in urban mobility in Brazil is characterized
by the growth of individual motorized transport and a reduc-
tion in the use of public transportation (IPEA 2011).
From an environmental standpoint, the increase in the
numbers of individual vehicles leads to an increase in air
pollution levels in large cities (Carvalho-Oliveira et al.
2005). Solutions to this problem might include changes in
automotive technologies, such as the use of hybrid or electric
cars, the investment in public policies that prioritize the use of
public transport, and the adoption of air quality monitoring
programs in major cities.
Thus, the development of parameters to estimate the effects
of air pollution on human health and the environment has
become a global challenge. Given the impact that particulate
matter can have on the health of an individual, the World
Health Organization (WHO) has established standards for
monitoring air pollution (WHO 2006).
Despite the existence of these recommendations, the
CONAMA Resolution No. 003/1990 has established Brazil's
current air quality standards, which only include standards for
inhalable particulate matter (PM10).

Table 1 Daily average percentage of micronucleus (AV), expressed in the average frequencies of micronucleus daily estimated in inflorescences
percent symbol and respective standard errors (SE) in inflorescences of from monitored site (town center) relative to those from Umuarama
Tradescantia pallida cv. Purpurea and percentage of alteration (%A) in Campus (reference site)

Day Umuarama campus (reference site) Town center (monitored site)

AV SE AV SE %A

05-17-2010 0.8 0.1 2.4 0.2 201*†

05-18-2010 1.0 0.2 4.4 0.5 361*†
05-19-2010 0.7 0.1 2.5 0.3 278*†
05-20-2010 0.9 0.1 1.9 0.2 109*
05-21-2010 0.9 0.1 2.0 0.1 127*
05-22-2010 0.8 0.1 1.5 0.1 80*
05-23-2010 0.8 0.1 1.3 0.1 62*

*Significant increase (Mann–Whitney rank sum - test; p <0.05)

†
Monitored events (days) with significantly higher average frequencies of micronucleus (Dunn test; p <0.01).
3684 Environ Sci Pollut Res (2014) 21:3680–3685

Fig. 3 Surface graphic

representation of the multiple
regression analysis between the
concentration of particulate
matter emitted, bus traffic, and the
frequency of micronuclei (MN) in
inflorescences of Tradescantia
pallida obtained during the bio-
monitoring study

As this resolution was established in 1990, the Brazilian
standard regarding PM10 requires discussion and update. In
comparison, other countries have adopted more stringent
standards. While daily emissions of PM10 are limited to
50 μg/m3 in Brazil, the WHO and the European Commission
of Environment (ECE) have recommended maximum daily
emissions of 20 and 40 μg/m3, respectively (ECE 2004).
According to SETTRAN (2011), the city of Uberlândia
has one of the newest and most modern transportation
systems in the country, which satisfies the requirements
for reducing pollutant emissions in accordance with the
Air Pollution Control Program for Motor Vehicles of the
Brazilian Institute for the Environment and Renewable
Natural Resources (Instituto Brasileiro do Meio Ambiente
e dos Recursos Naturais Renováveis - (IBAMA 2011).
While the age and engine technology of the buses are pre-
determined during the bidding process for the provision of
public transport in the city, the only air quality monitoring
parameter is a high volume sampler at the city's Central
Public Transport Terminal, which provides data on
inhalable particulate matter (PM10).
According to Monarca et al. (1999); Isidori et al. (2003),
and Misík et al. (2006), air pollution results from a complex
mixture of metals, organic compounds, and secondary com-
pounds generated from photochemical reactions. Only certain
substances are detected in towns where there are air quality
chemical monitoring stations, and although the components
have been identified, this analysis alone cannot establish the
genotoxic potential of air (Villarini et al. 2009).
This study is therefore important because the chemical
standard for the particulate matter (PM10) is integrated with
in situ biomonitoring using the TRAD-MN test as a biological

Table 2 The weather conditions during the 18 h/day of plant exposure in Uberlândia, Minas Gerais, Brazil. The study period lasted from 05-17-2010 to
05-23-2010

Day Weather conditions

Temperature (min-max °C) *Temperature (mean±SD) *Relative humidity (mean±SD) Insolation (h) Rainfall (mm)

05-17-2010 23.0-31.2 25.5±3.4 64.8±12.7 9.9 0

05-18-2010 23.0-26.9 25.0±1.5 66.0±4.8 6.3 0
05-19-2010 18.0-26.2 21.5±3.0 75.0±12.2 5.0 2.7
05-20-2010 17.0-24.8 20.4±3.1 81.6±0.9 9.8 0.5
05-21-2010 16.8-25.0 21.2±3.3 67.2±7.0 9.7 0
05-22-2010 20.2-26.4 22.5±3.0 60.4±5.8 9.6 0
05-23-2010 21.0-30.0 24.0±3.5 64.4±11.5 6.4 0

* Variations on temperature means and relative humidity means are statistically analyzed using analysis of variance (ANOVA). There was no significant
variations (p =ANOVA, p =0.74, and p =0.65, respectively)
Environ Sci Pollut Res (2014) 21:3680–3685
parameter to analyze the air genotoxicity of central Uberlândia
during and after a public transportation stoppage.
Thus, we propose that our results not only demonstrate that
vehicle emissions contain mutagenic substances but also pro-
vide substantiated evidence that investments in public trans-
port contribute directly to air quality through reductions in the
flow of vehicles, thereby reducing the mutagenic potential of
the air in large cities.
Acknowledgments The authors are grateful to SETTRAN for provid-
ing the information associated with traffic at the monitored site and to
Prof. Dr. Luiz Antônio de Oliveira of the Laboratory of Climatology and
Water Resources (Laboratório de Climatologia e Recursos Hídricos) for
sharing the climatological data used in this study.
Conflict of Interest The authors declare that there are no conflicts of
interest.
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