Environmental Research 170 (2019) 243–251

Contents lists available at ScienceDirect

Environmental Research
journal homepage: www.elsevier.com/locate/envres

Incidence and mortality for respiratory cancer and traffic-related air T

pollution in São Paulo, Brazil
Adeylson Guimarães Ribeiroa, ,1, George Stanley Downwardb, ,1, Clarice Umbelino de Freitasc,3,
⁎ ⁎

Francisco Chiaravalloti Netod, Maria Regina Alves Cardosod,

Maria do Rosario Dias de Oliveira Latorred, Perry Hystade, Roel Vermeulenb,2,
Adelaide Cassia Nardoccia,2
a
Department of Environmental Health, School of Public Health, University of São Paulo, Av. Dr. Arnaldo, 715, São Paulo, SP CEP 01246-904, Brazil
b
Institute for Risk Assessment Sciences, Utrecht University, P.O. Box 80178, 3508 TD Utrecht, the Netherlands
c
Center for Epidemiological Surveillance, State Department of Health, Av. Dr. Arnaldo, 351, São Paulo, SP CEP:01246-000, Brazil
d
Department of Epidemiology, School of Public Health, University of São Paulo, Av. Dr. Arnaldo, 715, São Paulo, SP CEP 01246-904, Brazil
e
College of Public Health and Human Sciences, Oregon State University, 20C Milam Hall, Corvallis, OR 97331, USA

ARTICLE INFO ABSTRACT

Keywords: Background: Multiple lines of evidence have associated exposure to ambient air pollution with an increased risk
Air pollution of respiratory malignancies. However, there is a dearth of evidence from low-middle income countries, including
Vehicle emissions those within South America, where the social inequalities are more marked.
Respiratory cancer Objectives: To quantify the association between exposures to traffic related air pollution and respiratory cancer
Vulnerable population
incidence and mortality within São Paulo, Brazil. Further, we aim to investigate the role of socioeconomic status
Environmental justice
(SES) upon these outcomes.
Methods: Cancer incidence between 2002 and 2011 was derived from the population-based cancer registry.
Mortality data (between 2002 and 2013) was derived from the Municipal Health Department. A traffic density
database and an annual nitrogen dioxide (NO2) land use regression model were used as markers of exposure.
Age-adjusted Binomial Negative Regression models were developed, stratifying by SES and gender.
Results: We observed an increased rate of respiratory cancer incidence and mortality in association with in-
creased traffic density and NO2 concentrations, which was higher among those regions with the lowest SES. For
cancer mortality and traffic exposure, those in the most deprived region, had an incidence rate ratio (IRR) of
2.19 (95% CI: 1.70, 2.82) when comparing the highest exposure centile (top 90%) to the lowest (lowest 25%). By
contrast, in the least deprived area, the IRR for the same exposure contrast was.1.07 (95% CI: 0.95, 1.20). For
NO2 in the most deprived regions, the IRR for cancer mortality in the highest exposed group was 1.44 (95% CI:
1.10, 1.88) while in the least deprived area, the IRR for the highest exposed group was 1.11 (95% CI: 1.01, 1.23).
Conclusions: Traffic density and NO2 were associated with an increased rate of respiratory cancer incidence and
mortality in São Paulo. Residents from poor regions may suffer more from the impact of traffic air pollution.

1. Introduction associated particulate matter as a Group 1 carcinogen (IARC, 2013).

Further, diesel engine exhaust or emissions are also classified as Group
Ambient air pollution has been well established as a risk factor in 1 carcinogens based on sufficient evidence of increased risk of lung
the development of lung cancer, with the International Agency for cancer (IARC, 2012).
Research on Cancer (IARC) classifying ambient air pollution and its The bulk of the evidence investigating air pollution and lung cancer

Corresponding author.
⁎

E-mail addresses: [email protected] (A.G. Ribeiro), [email protected] (G.S. Downward), [email protected] (F. Chiaravalloti Neto),
[email protected] (M.R.A. Cardoso), [email protected] (M.d.R.D.d.O. Latorre), [email protected] (P. Hystad), [email protected] (R. Vermeulen),
[email protected] (A.C. Nardocci).
1
Co-first author.
2
Co-senior author.
3
In memorian.

https://doi.org/10.1016/j.envres.2018.12.034
Received 18 September 2018; Received in revised form 29 November 2018; Accepted 15 December 2018
Available online 18 December 2018
0013-9351/ © 2018 Elsevier Inc. All rights reserved.
A.G. Ribeiro et al. Environmental Research 170 (2019) 243–251

risk has been derived from high-income countries, predominantly in has a population of approximately 12 million, making it the largest and
North America and Europe (Beelen et al., 2008a; Hamra et al., 2014; most populous city in Brazil (Fig. 1). It is the capital of the state of São
Hystad et al., 2013; Olsson et al., 2011; Puett et al., 2014; Raaschou- Paulo, which is considered the main national industrial center, with a
Nielsen et al., 2016, 2013; Villeneuve et al., 2014; Yorifuji et al., 2016). Gross Domestic Product (GDP) per capita of approximately 16 thousand
With the exception of several studies conducted mainly in China (Li dollars in 2014 (IBGE, 2017). It has a fleet of approximately 8.6 million
et al., 2018; Shao et al., 2019; Yue et al., 2017), there is a dearth of vehicles (of which approximately 16% are diesel operated) which cir-
evidence from low and middle income countries (LMIC). Furthermore, a culate daily on its 18,000 km of routes (DETRAN, 2017). The dis-
large number of recent studies only utilized mortality data and long- tribution of traffic routes and volume is varied, with a high density both
term exposure to conduct their risk analyses (Beelen et al., 2014; Bidoli in the central region of the city, as well as extensive corridors and
et al., 2016; Carugno et al., 2016; Crouse et al., 2015; Fischer et al., highways that cross the urban area.
2015; Hansell et al., 2016; Lepeule et al., 2012; Yorifuji et al., 2013;
Zhou et al., 2015) with relatively few studies using incidence data, with
2.2. Case ascertainment
the notable exception of the ESCAPE study which analyzed air pollution
and lung cancer incidence in European cohorts (Raaschou-Nielsen
The outcomes of interest to the present study were the incidence
et al., 2013).
and mortality of respiratory malignancies among men and women
Previous studies have established that socioeconomic status (SES)
above the age of 20. These outcomes were coded by the International
can influence the exposure and effects of air pollution (Cesaroni et al.,
Classification of Diseases (ICD-10) as follows: C32 - malignant neo-
2010; Deguen and Zmirou-Navier, 2010; Habermann et al., 2014;
plasm of the larynx, C33 - malignant neoplasm of the trachea, and C34 -
Havard et al., 2009; Pearce et al., 2006). In 2009, the Environmental
malignant neoplasm of the bronchi and lungs.
Protection Agency (EPA) initiated activities to formalize and ensure
The incidence of respiratory malignancies between 2002 and 2011
that the development of regulations, in the context of environmental
was acquired from the population-based cancer registry of São Paulo.
and health impacts, take into account environmental justice (Nweke
The mortality rate of respiratory malignancies between 2002 and 2013
et al., 2011). Thus, when evaluating the relationship between living
was acquired from the Mortality Information System (SIM) of the
near areas of high traffic density and exposure to air pollution, a so-
Municipal Health Department. The incidence registry was the result of
cioeconomic analysis should be considered. According to Galobardes
active surveillance and the mortality registry passive surveillance.
et al. (2007), socioeconomic measures on an area-level are specifically
Together they covered all cases in the city of São Paulo.
needed to investigate whether these aspects of the place where a person
A total of 15,411 incident cases (10,270 men, 5141 women) and
lives affects the person's health. Moreover, understanding the role of
19,500 deaths attributable to respiratory cancers (12,826 men, 6674
SES as an important factor of susceptibility to ambient air pollution is
women) were identified. The incident cases were geocoded by home
essential to the process of implementing air quality control programs
address and the mortality cases by residential zip code using the cen-
(Samet and White, 2004).
troid (home address information is unavailable for mortality cases –
To address the dearth of studies in LMICs and to evaluate the impact
residential zip code contains equivalent geographic information for the
of a wider contrast in SES, we performed a study in São Paulo, where a
purposes of exposure assignment). The software ArcGIS version 9.3 was
broad contrast in SES exists, to quantify the association between in-
used for the geocoding process.
cidence and mortality for respiratory cancers and traffic-related air
pollution and its interaction with SES.
2.3. Exposure assessment

2. Methods Residential exposure to traffic-related emissions was estimated for

500 m × 500 m cells. Cell size was determined based on a review study
2.1. Study area which reported that an exposure zone within a range of 300–500 m
from a major road represented the area most highly affected by traffic
The municipality of São Paulo occupies an area of 1521.11 km2 and emissions (HEI Panel on the Health Effects of Traffic-Related air

Fig. 1. Geographical location of the municipality of São Paulo, Brazil.

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A.G. Ribeiro et al. Environmental Research 170 (2019) 243–251

Pollution, 2010). Therefore, the definition of cell size considered both The Municipal Human Development Index (MHDI) was used as an
that the greatest exposure occurs at a distance of up to 500 m of high- indicator of SES. This indicator considered three dimensions: longevity,
traffic roads and that the cell could not be smaller than 100 m × 100 m income and education grouped by a geometric mean, according to the
(which is the usual size of the blocks). methodology of the United Nations Development Programme (UNDP
The volume and density of traffic were assigned for the year 2008, Brazil, 2013), which ranges on a scale from 0 to 1, by census tract. For
and the annual estimates of nitrogen dioxide (NO2) averaged between longevity, the dimension used an average of mortality data from the
1997 and 2011, at the home street of incident and mortality cases. The years 2009, 2010 and 2011, which was obtained from the Municipal
development of the traffic density dataset has been described elsewhere Health Department. The use of an average avoided an atypical mor-
(Cardoso et al., 2010). Briefly, the Traffic Engineering Company of São tality event in a single year producing a bias. For the income and
Paulo (CET) conducts vehicular counts in streets throughout the city, education dimensions, data from the most recent Demographic Census,
which are classified according to their function in traffic distribution as: performed in 2010 by the Brazilian Institute of Geography and Statistics
expressway, arterial-1, arterial-2, arterial-3, collector-1, collector-2, (which aggregated individual-level measures by census tract) were used
and local. These categories correlate well with their traffic volumes. (IBGE, 2010). The income dimension was measured by the per capita
The number of cars, motorcycles, buses and trucks were counted, from income, defined as the sum of the income of all residents, divided by the
Monday to Friday, during the peak hours of the morning (7–10 a.m.) or number of residents. In the calculation of the education dimension the
afternoon (5–8 p.m.). The number of vehicles were counted in 15 min educational level of adults and children were treated and weighted
intervals and multiplied by four to convert into hourly volumes. Mea- separately. The educational level of the adult population was measured
surements were never performed near traffic lights nor when traffic was by the percentage of people 18 years and older who had completed
stagnant. grade school. This metric was given a weighting of 1. For children, the
The current study complemented this routine data with additional percentages of children attending schools and completing specific years
traffic counts, performed using the same method used by the CET in at school were given a weighting of 2. The education dimension was
additional streets which were evenly distributed throughout the city. In calculated as the geometric mean of these components. In these ana-
total, 681 streets were measured, corresponding to 21% of the total lyses, population data and MHDI were converted to grid cells. The
number of expressways; 16% of arterial-1; 21% of arterial-2; 14% of values of the intercept census tract in each grid cell, weighted by the
arterial-3; 9% of collector-1; 6% of collector-2; and 0.5% of the local proportion of the area occupied by each of them, were summed to
streets of the city. The mean volume for each street category was at- calculate populations and obtain an average to calculate the MHDI. This
tributed to the other streets of the same category without any mea- conversion was done with the software ArcGIS ArcInfo 9.3
surement. All traffic information was entered into a geo-coded street (Environmental Systems Research Institute ESRI, 2008).
database. The urban area was subsequently divided into a grid with The population was categorized in five groups according to age:
500 m x 500 m cells. The software ET Geowizards 9.9 for ArcGIS 9.2 21–40, 41–60, 61–70, 71–80 and ≥ 81 years old. The grid cells were
was used for constructing the vectorial grid of the units of analysis. The classified by MHDI in four categories: low (quartile ≤ 25), medium
traffic density was calculated for each cell by: (quartile 26–50), medium-high (quartile 51–75) and high (quartile >
n
75) (Table 1). The level of exposure was measured by traffic density
VL
i=1 i i and NO2 measurements categorization into five centile groups: 0–25,
TD =
A 26–50, 51–75, 76–90 and > 90% (Fig. 2). Grid cells with a total po-
pulation less than 20 inhabitants were excluded from analysis, (1876
Where TD is the traffic density of each cell (vehicles/hour/meter), Vi is
cells out of a total of 6384 were excluded).
the number of vehicles (vehicles/hour), Li is the length of the i-th
segment of the street (meters), A is the area (meters2) of the cell (500 m
2.4. Statistical analyses
x 500 m) and n is the number of segments of streets inside the cell.
Using this approach, the total traffic density (TTD), the traffic density of
The effect of traffic density and NO2 exposure on the rate of in-
vehicles powered by gasoline and ethanol (TDG) (cars + motorcycles)4
cidence and mortality from respiratory cancers was quantified by
and vehicles powered by diesel (buses + trucks) (TDD) were calcu-
means of incidence rate ratios (IRRs) and corresponding 95% con-
lated. Traffic density was calculated using the software ArcGIS ArcInfo
fidence intervals (CI), calculated using Binomial Negative Regression
9.3 (Environmental Systems Research Institute ESRI, 2008).
models. The dependent variable was the number of incident respiratory
Annual estimates of NO2 were obtained from a global NO2 land use
cancer cases and the number of deaths from all respiratory cancers,
regression (LUR) model, which included satellite observations and
offset by population above the age of 20. All IRRs were adjusted for
geographic predictor variables. The detailed description of the NO2 LUR
MHDI, age and gender. To further investigate the role of SES, models
model has been described elsewhere (Larkin et al., 2017). Briefly, 5220
were also stratified by MHDI category. Further, the interaction between
ground-based monitors from 57 nations were used to develop the LUR
exposure and MHDI was also tested. In interaction analysis, MHDI was
model. Satellite estimates of NO2, developed by combining tropospheric
kept as a categorical variable and exposure as a continuous one.
NO2 column retrievals from the SCIAMACHY and GOME-2 satellites
Analyses were performed using Stata version 12 (StataCorp, 2011).
with output from the global GEOS-Chem model (from 1997 to 2011),
captured regional NO2 concentrations at a 10 × 10 km resolution.
3. Results
Multiple land use predictor variables (e.g. length of roads, population
density, green spaces etc.) were included in the final LUR models
Of the incident cases, 21% were laryngeal malignancies (C32), 78%
(variable selection was performed via Lasso), which predicted NO2 at a
were bronchial and lung malignancies (C34) and less than 1% were
100 × 100 m resolution, thus capturing fine-scale within-city variation
tracheal malignancies (C33). Of the mortalities, 15% were related to
in traffic related air pollutants. The final LUR predicted 54% of the
laryngeal malignancies, 85% bronchial and lung malignancies, and less
global NO2 variation with a mean absolute error of 3.7 ppb. We aver-
than 1% tracheal malignancies.
aged NO2 predictions to the 500 m x 500 m analytics cells, where each
Fig. 2a and b show the traffic density and annual NO2 estimates for
cell had a predicted annual NO2 that was used to assign exposure to
São Paulo respectively. In general, traffic density and NO2 were higher
residential locations located within this area unit.
in the central regions than the peripheral regions and were moderately
correlated with each other (correlation coefficient of 0.56), likely re-
4
16% of the vehicles run only on ethanol and the others run on a mixture of presenting traffic-related generation of NO2. Traffic density ranged
75% of gasoline and 25% of ethanol. from 0 to 163 m.vehicles.hour/m2 (the number of vehicles for each

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A.G. Ribeiro et al. Environmental Research 170 (2019) 243–251

Table 1 cancer showed a statistically significant exposure-response gradient for

Distribution of the study populationa stratified by age group, gender both traffic density (IRR: 1.03, 95% CI: 1.02, 1.05 per 10 m.vehicle-
and category of MHDI – 2010b (São Paulo, Brazil). s.hour/m2 increase) and NO2 (IRR: 1.14, 95% CI: 1.11, 1.18 per 5 µg/
Total people in study population 7,846,441 m3 increase). Individuals in the highest 2 centile groups for traffic
density had approximately 2-fold increases in cancer incidence (IRR for
Age group (%) highest vs. lowest centile (1.63, 95% CI: 1.46, 1.81). For NO2 exposure,
21–40 50.2
individuals in the highest centile had an IRR of 1.34 (95% CI: 1.22,
41–60 34.1
61–70 8.6 1.47) compared to the lowest centile. Similar incidence rates between
71–0 4.9 men and women were observed in relation to traffic exposure while
≥ 80 2.2 lower rates were observed for NO2 in women.
Gender (%)
For cancer mortality, a significant exposure-response gradient was
Men 46.0
Women 54.0
seen for ambient NO2 (IRR: 1.05, 95% CI: 1.02, 1.08 per 5 µg/m3 in-
MHDI category (%) crease). The rate of death was approximately 30% higher in NO2 ex-
1 (lowest) 19.7 posure groups higher than the reference centile (e.g. IRR among the
2 28.6 highest centile: 1.18, 95% CI: 1.09, 1.29). When stratifying by gender,
3 25.8
men generally had a higher rate of death, except for the highest exposed
4 (highest) 25.9
group where findings were equivalent – men had an IRR of 1.19 (95%
a
Grid cells with a total population less than 20 inhabitants were CI: 1.07, 1.32) and women an IRR of 1.20 (95% CI: 1.04, 1.39). The IRR
excluded. for mortality in relation to traffic density was generally higher for men
b
MHDI – 2010: Municipal Human Development Index. than women. For example, in the highest centile men had an IRR of
1.56. (95% CI: 1.38, 1.76) and women an IRR of 1.27 (95% CI: 1.08,
street segment within one hour divided by the area in square meters) 1.49).
and ambient NO2 concentrations ranged from 3 to 32 µg/m3. The The IRRs of incidence and mortality in relation to traffic density,
geographic distribution of MHDI is shown in Fig. 2c. Areas with the stratified by MHDI category are shown in Table 3. Overall, an excess in
highest index were typically concentrated in the central regions with incidence and mortality rates within MHDI 1 (the lowest) is observed
the index declining towards the peripheral regions. compared to the other MHDI categories. The exposure-response gra-
The IRRs for cancer incidence and mortality for all individuals, men, dient between traffic density and both incidence and mortality is no-
and women are shown in Table 2. Overall, the incidence of respiratory tably higher in the lowest MHDI strata (1.26, 95% CI: 1.14, 1.40 and

Fig. 2. (a) Total traffic density (2008), (b) mean annual NO2 concentrations (1997–2011) and (c) Municipal Human Development Index (MHDI) − 2010, by grid cells
(500 m × 500 m), in São Paulo, Brazil.

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Table 2
Incidence rate ratio (IRR) (and 95% CI) for incidence and mortality for respiratory cancer by proximity to traffic density and NO2 concentrations (São Paulo, Brazil).
All Men Women

a b
IRR (95% CI) IRR (95% CI) IRRb (95% CI)

Incidence (2002–2011)
Traffic Density (%)
0–25 1 1 1
26–50 1.36 (1.24–1.50) 1.41 (1.25–1.59) 1.46 (1.22–1.74)
51–75 1.58 (1.43–1.73) 1.66 (1.47–1.87) 1.62 (1.35–1.93)
76–90 1.69 (1.53–1.87) 1.76 (1.55–1.99) 1.78 (1.48–2.14)
> 90 1.63 (1.46–1.81) 1.75 (1.53–2.00) 1.65 (1.36–2.01)
10-unit increase 1.03 (1.02–1.05) 1.04 (1.03–1.06) 1.02 (1.00–1.05)
NO2 (%)
0 − 25 1 1 1
26 − 50 0.98 (0.91–1.06) 0.99 (0.90–1.09) 0.97 (0.84–1.11)
51 − 75 1.07 (0.99–1.16) 1.13 (1.02–1.25) 0.98 (0.85–1.13)
76 − 90 1.13 (1.04–1.24) 1.21 (1.09–1.35) 1.00 (0.86–1.16)
> 90 1.34 (1.22–1.47) 1.40 (1.25–1.58) 1.24 (1.06–1.45)
5-µg/m3 increase 1.14 (1.11–1.18) 1.16 (1.12–1.20) 1.12 (1.06–1.17)
Mortality (2002–2013)
Traffic Density (%)
0–25 1 1 1
26–50 1.36 (1.25–1.47) 1.45 (1.30–1.61) 1.25 (1.08–1.43)
51–75 1.44 (1.32–1.56) 1.61 (1.45–1.79) 1.24 (1.07–1.43)
76–90 1.47 (1.35–1.61) 1.60 (1.43–1.80) 1.30 (1.12–1.51)
> 90 1.42 (1.29–1.56) 1.56 (1.38–1.76) 1.27 (1.08–1.49)
10-unit increase 1.00 (0.99–1.02) 1.01 (0.99–1.02) 1.00 (0.98–1.02)
NO2 (%)
0–25 1 1 1
26–50 1.06 (0.99–1.13) 1.06 (0.97–1.15) 1.11 (0.99–1.25)
51–75 1.10 (1.02–1.18) 1.14 (1.04–1.25) 1.08 (0.95–1.22)
76–90 1.06 (0.98–1.15) 1.13 (1.02–1.24) 1.01 (0.88–1.16)
> 90 1.18 (1.09–1.29) 1.19 (1.07–1.32) 1.20 (1.04–1.39)
5-µg/m3 increase 1.05 (1.02–1.08) 1.05 (1.01–1.08) 1.05 (1.00–1.10)

a
Estimates from negative binomial regression models adjusted by Municipal Human Development Index – MHDI (2010), age and gender.
b
Adjusted by MHDI 2010 and age.

1.21, 95% CI: 1.11, 1.32 per 10 units respectively) than the highest The excess incidence and mortality rates among the lowest MHDI is
(1.04, 95% CI: 1.02, 1.05 and 1.01, 95% CI: 1.00, 1.03 per 10 units). also seen when examining ambient NO2 concentrations (Table 4). As
Further, individuals in the lowest MHDI strata who experienced the with traffic density, those in the lowest MHDI category who experience
highest traffic density centile had incidence and mortality IRRs up to 2 the highest levels of ambient NO2 have higher IRRs for both incidence
times higher than those experiencing similar density in the highest (1.45, 95% CI: 1.04, 2.00) and mortality (1.44, 95% CI: 1.10, 1.88) than
MHDI group (incidence IRR for lowest MHDI: 2.72, 95% CI: 1.98, 3.73 those in the highest MHDI category (IRR for incidence: 1.42, 95% CI:
and for the highest: 1.30, 95% CI: 1.16, 1.46). 1.29, 1.57; for mortality: 1.11, 95% CI: 1.01, 1.23). However, the

Table 3
Incidence rate ratio (IRR)a (and 95% CI) for incidence and mortality for respiratory cancer by proximity to traffic density, stratified by category of MHDI – 2010b (São
Paulo, Brazil).
Incidence Mortality Incidence Mortality

(2002–2011) (2002–2013) (2002–2011) (2002–2013)

IRR (95% CI) IRR (95% CI) IRR (95% CI) IRR (95% CI)

MHDI 1 (lowest) MHDI 2

Traffic Density (%) Traffic Density (%)
0–25 1 1 0–25 1 1
26–50 1.95 (1.39–2.73) 1.49 (1.13–1.96) 26–50 1.26 (1.08–1.47) 1.20 (1.05–1.38)
51–75 2.27 (1.67–3.10) 2.03 (1.58–2.60) 51–75 1.35 (1.16–1.57) 1.22 (1.07–1.40)
76–90 2.45 (1.80–3.34) 2.26 (1.77–2.88) 76–90 1.45 (1.23–1.70) 1.34 (1.16–1.55)
> 90 2.72 (1.98–3.73) 2.19 (1.70–2.82) > 90 1.41 (1.17–1.69) 1.18 (1.00–1.40)
10-unit increase 1.26 (1.14–1.40) 1.21 (1.11–1.32) 10-unit increase 1.05 (1.01–1.08) 1.01 (0.98–1.05)
MHDI 3 MHDI 4 (highest)
Traffic Density (%) Traffic Density (%)
0–25 1 1 0–25 1 1
26–50 1.14 (1.03–1.26) 1.15 (1.05–1.26) 26–50 1.25 (1.15–1.36) 1.11 (1.02–1.20)
51–75 1.31 (1.19–1.45) 1.19 (1.09–1.30) 51–75 1.30 (1.19–1.41) 1.13 (1.04–1.23)
76–90 1.25 (1.12–1.41) 1.10 (0.99–1.22) 76–90 1.36 (1.23–1.50) 1.23 (1.12–1.35)
> 90 1.14 (0.97–1.33) 0.98 (0.85–1.13) > 90 1.30 (1.16–1.46) 1.07 (0.95–1.20)
10-unit increase 1.02 (0.99–1.04) 0.98 (0.96–1.00) 10-unit increase 1.04 (1.02–1.05) 1.01 (1.00–1.03)

a
Estimates from negative binomial regression models adjusted by age and gender.
b
MHDI-2010: Municipal Human Development Index.

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A.G. Ribeiro et al. Environmental Research 170 (2019) 243–251

Table 4
Incidence rate ratio (IRR)a (and 95% CI) for incidence and mortality for respiratory cancer by NO2 concentrations, stratified by category of MHDI – 2010b (São Paulo,
Brazil).
Incidence Mortality Incidence Mortality

(2002–2011) (2002–2013) (2002–2011) (2002–2013)

IRR (95% CI) IRR (95% CI) IRR (95% CI) IRR (95% CI)

MHDI 1 (lowest) MHDI 2

NO2 (%) NO2 (%)
0–25 1 1 0–25 1 1
26–50 1.50 (1.08–2.10) 1.19 (0.90–1.57) 26–50 0.99 (0.86–1.13) 0.96 (0.86–1.09)
51–75 1.45 (1.05–2.00) 1.48 (1.14–1.93) 51–75 1.09 (0.96–1.24) 1.02 (0.91–1.14)
76–90 1.45 (1.05–2.01) 1.41 (1.08–1.84) 76–90 1.12 (0.98–1.29) 0.99 (0.87–1.11)
> 90 1.45 (1.04–2.00) 1.44 (1.10–1.88) > 90 1.24 (1.07–1.44) 1.06 (0.93–1.21)
5-µg/m3 increase 1.06 (0.97–1.14) 1.12 (1.05–1.20) 5-µg/m3 increase 1.13 (1.06–1.20) 1.05 (0.99–1.11)
MHDI 3 MHDI 4 (highest)
NO2 (%) NO2 (%)
0–25 1 1 0–25 1 1
26–50 1.01 (0.92–1.11) 1.03 (0.96–1.13) 26–50 1.10 (1.00–1.20) 1.03 (0.95–1.12)
51–75 1.05 (0.96–1.15) 1.00 (0.92–1.08) 51–75 1.14 (1.05–1.24) 1.00 (0.92–1.08)
76–90 1.18 (1.06–1.31) 1.01 (0.91–1.11) 76–90 1.25 (1.14–1.37) 1.17 (1.07–1.27)
> 90 1.23 (1.07–1.40) 0.93 (0.82–1.06) > 90 1.42 (1.29–1.57) 1.11 (1.01–1.23)
5-µg/m3 increase 1.09 (1.03–1.16) 0.96 (0.91–1.01) 5-µg/m3 increase 1.23 (1.17–1.29) 1.09 (1.04–1.14)

a
Estimates from negative binomial regression models adjusted by age and gender.
b
MHDI-2010: Municipal Human Development Index.

exposure-response gradient between NO2 and mortality is only slightly comparing the highest quartile of residential nitrogen oxides
higher between the lowest MHDI strata (1.12, 95% CI: 1.05, 1.20 per (> 29.7 µg/m3), to the lowest concentrations (< 17.2 µg/m3). Studies
5 µg/m3) and the highest (1.09, 95% CI: 1.04, 1.14 per 5 µg/m3) and conducted in The Netherlands showed an association between exposure
the difference was not statistically significant considering the overlap of to NO2 and an elevated risk of incident lung cancer (HR: 1.29, 95% CI:
CI values. 1.08, 1.54, per 30 µg/m3) and lung cancer mortality (HR: 1.10, 95% CI:
The interaction of MHDI as a categorical variable and exposure as a 1.09, 1.11, per 10-µg/m3 increase) (Fischer et al., 2015; Hart et al.,
continuous variable was examined. This yielded similar results to the 2015). A systematic review and meta-analysis found that a 10-µg/m3
stratified results, finding differing IRRs for the varying MHDI cate- increase in exposure to NO2 was associated with a meta-estimate for
gories. For example, the lung cancer mortality IRR for traffic density lung cancer of 1.04 (95% CI: 1.01, 1.08) (Hamra et al., 2015). In an
and MHDI category 1 was 1.22 (95% CI: 1.12, 1.33) while for MHDI Italian study, Bidoli et al. (2016) reported elevated of risks of death
category 4 it was 1.01 (95% CI: 1.00, 1.03). For NO2 and cancer mor- from lung cancer among those residing within 25 m of a major road,
tality, the IRR for MHDI category 1 was 1.13 (95% 1.05, 1.21) and for adjusting for urban and rural environments, in both men (1.10, 95% CI:
MHDI category 4 it was 1.09 (95% CI: 1.04, 1.15). Full results are 1.06, 1.14) and women (1.25, 95% CI: 1.10, 1.44). Long-term exposure
available in the supplement. to NO2 was also associated with lung cancer mortality in Italy (HR:
1.04, 95% CI: 1.02, 1.07) and Japan (HR: 1.20, 95% CI: 1.03, 1.40), per
4. Discussion 10 µg/m3 increase (Cesaroni et al., 2013; Yorifuji et al., 2013). How-
ever, the ESCAPE study has not found any significant association be-
This study found an increased rate of respiratory cancer incidence tween lung cancer and nitrogen oxides concentration or traffic intensity
and mortality in association with an increase in traffic density and NO2 on the nearest street in Europe (Raaschou-Nielsen et al., 2013).
concentrations within São Paulo. Stratifying by categories of MHDI The present paper investigated the relationship between traffic
showed that the degree of this relationship was even more pronounced densities, NO2 concentrations, and cancer incidence/mortality in the
in the lowest, indicating that residents of these regions may suffer more context of MHDI categories. The traffic density and NO2 concentrations
from the effects of traffic-related air pollution. in São Paulo were higher in the central regions, which was character-
Our results are generally consistent with previous work, although ized by a better MHDI, indicating that the residents of these central
the larger IRRs observed here may reflect differences in tailpipe emis- regions are probably exposed to higher levels of air pollution than those
sions since most studies have been conducted in North America and who live in the most deprived regions. However, we found a higher rate
Europe which have more stringent emission controls. Chen et al. (2009) of respiratory cancer mortality among residents from regions with the
showed an increased risk of lung cancer in areas with high traffic lowest MHDI, regardless of local traffic intensity and NO2 concentra-
density in the United States, reporting risks 136% and 68% higher for tions, indicating that SES plays an important role in the relationship
adenocarcinoma and squamous cells carcinomas, respectively, for the between air pollution and disease (however we note that this difference
highest (937 motor vehicles per square mile) vs. lowest (one motor is less pronounced for disease incidence and ambient NO2 as seen when
vehicle per square mile) exposed groups. Hystad et al. (2013), in a comparing the exposure-response gradient between the lowest MHDI
Canadian case-control study, found elevated risks for lung cancer in- and the highest). These findings are consistent with a study conducted
cidence associated with living within 100 m of highways for a period of in South Carolina, USA, which found a strong association between SES
10 years (OR: 1.10, 95% CI: 0.83, 1.46) and per 10 ppb increase for NO2 metrics and estimated cancer risks associated with air pollutants, while
(OR: 1.34; 95% CI: 1.07, 1.69). Another Canadian study, with a large also highlighting that on-road source risk was significantly related to all
national-level cohort, found positive associations (HR: 1.07; 95% CI: sociodemographic factors (Wilson et al., 2015). A partial explanation
1.05, 1.10) between trachea, bronchus, and lung cancer deaths and for this phenomenon may be that poorer people living in the peripheries
cumulative exposure to an increment of 8.1ppb for NO2 (Crouse et al., of São Paulo have longer commuting hours, and thus using their re-
2015). Raaschou-Nielsen et al. (2011), in a Danish cohort study, re- sidential address alone to assign traffic exposure may result in an un-
ported an IRR for lung cancer of 1.30 (95% CI: 1.05, 1.61) when derestimation of their true exposures. However, various vulnerability

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factors, such as smoking prevalence and biological, nutritional, and assume that the traffic-related exposures remained stable over pre-
educational status, the regular practice of physical activities and ac- ceding decades. There are some limitations to this assumption as while
cessibility to health care services are also likely to have contributed to the number of cars in use was lower in previous years, the car fleet was
the increased rates in areas with the worst index. Differences in ac- less technologically advanced and the policies on the emissions of
cessibility to health centers, health insurances, preventive care services pollutants were less rigorous. Furthermore, the historical air quality
and effective treatment options for population from regions with high data reported pollutants level higher in previous years in related to the
MHDI in comparison those who live in peripheral regions are likely to year of the traffic density and estimates of NO2 used in this study. For
impact disease prevention, treatment, and prognosis. Arcaya et al. example, the PM10 and NO2 concentrations decreased by around 60 µg/
(2015) affirms that an unequal distribution of physical health risks and m3 to 40 µg/m3 and 80 µg/m3 to 50 µg/m3, respectively, from 1987 to
resources across geographies and social groups contributes to social 2008 (Andrade et al., 2017) meaning that the exposures assigned here
inequalities in health via material pathways. likely under-estimate historical exposures.
The relationship between exposure to ambient air pollution and SES Previous studies have investigated the impact of air pollution on the
was discussed by Deguen and Zmirou-Navier (2010) who, in their health of São Paulo's population (Marcilio and Gouveia, 2007; Pereira
analysis of European studies, concluded that deprived populations, al- et al., 2005; Toledo and de, Nardocci, 2011; Yanagi et al., 2012) but no
though not always more exposed, suffer more from air pollution effects analyses to date were conducted to evaluate cancer risks in relation to
because of vulnerability factors. A comprehensive assessment of risk residential proximity to traffic and exposure to NO2 concentrations and
factor exposure and attributable burden of disease, from 1990 to 2016, its interaction with SES. São Paulo is characterized by great social in-
estimated that air pollution was the second highest risk factor in terms equalities and the use of small area units improved the SES evaluation.
of attributable disability-adjusted life-years (DALYs) in low Socio-de- Although air quality reports have indicated a general improvement in
mographic Index countries (Abajobir et al., 2017). This injustice in air pollution rates in São Paulo over recent decades (Andrade et al.,
traffic-related air pollution exposure was discussed by Jerrett (2009) 2017), the population still coexists with high exposures to toxic pollu-
who stated that even in economically advanced countries air pollution tants. For example, PM10 in the metropolitan region, according the
and other environmental risks remain unequally distributed, dis- Environmental Company of the State of São Paulo (CETESB), presented
proportionately affecting disadvantaged populations. an average concentration of 39 μg/m3 over the last 17 years (CETESB -
Despite our findings, the current study has several limitations, in- Companhia Ambiental do Estado de São Paulo, 2017), which is higher
cluding a lack of individual information. We assumed that all in- than the value recommended by the World Health Organization (WHO)
dividuals within the 500 m x 500 m cells had the same exposure as it of 20 μg/m3 (WHO - World Health Organization, 2006). São Paulo has a
was not possible to assess the variation of individual exposures during pollutant monitoring network that includes 17 fixed stations with reg-
daily movements within the city, potentially leading to exposure mis- ular measurements for: PM10, SO2, NOX, CO, O3 and PM2.5 but the
classification. Mortality cases were geocoded by the centroid of their number and geographical distribution of the stations are insufficient to
residential zip code, which was less precise than the address level in- measure exposures to these pollutants on a fine spatial scale. Further-
formation available for incident cases. However, zip code information more, CETESB reported that the data from their monitoring networks
in São Paulo is highly detailed, and relative to the cell size we used in are more representative of background pollution and do not have a
analysis, postal code remains a valid method of assigning residential good correlation with surrounding traffic. Therefore, despite the lack of
location. Another consideration is that information on individual other sources of air pollution data, a major strength of our study was
smoking habits was not available. Smoking is a well-known major risk the use of the global NO2 land use regression model that allowed esti-
factor for respiratory cancers, and historically was more prevalent in mating NO2 concentrations at a relatively fine spatial scale (100 m re-
men. The population level smoking rates, by gender, reported in 2008, solution). Other strengths include the use of a complete incidence and
that women were more likely to report being never smokers (65%) than mortality database, the ability to estimate traffic density at a fine spatial
men (55%). Consequently, a lower proportion of women reported being scale, that might be used as a proxy for traffic exposure in São Paulo
current smokers (20% versus 24% for men) and ex-smokers (16% (Silva et al., 2006), and detailed information on socio-economic factors.
versus 21%) (São Paulo SP, 2010). However, despite these different Further, this study represents only one of a few studies investigating
smoking patterns, we observed comparable cancer rates for men and proxies of ambient air pollution on health within Latin American
women by proximity to traffic density and exposure to higher ambient countries and represents the first time that the relationship between
NO2 concentrations, further strengthening our finding of an association traffic density and NO2 with respiratory cancers in Sao Paulo has been
between air pollution and respiratory cancers. To further investigate investigated.
any potential bias by smoking, we accessed a periodic health survey,
conducted by the Municipal Health Department and University of São 5. Conclusions
Paulo, using a representative São Paulo sample for the years 2003, 2008
and 2015 (São Paulo SP, 2018). Using this information, we tested the The results of this study show that traffic density and ambient NO2
associations between smoking status (never smoker, current smoker concentrations were associated with an increased rate of incidence and
and ex-smoker) and per capita income (≤ 2 and > 2 minimum wages, death for respiratory cancers in São Paulo. This study also indicates that
being the smallest amount of money that employers are legally allowed those with lower SES were more vulnerable to the development of re-
to pay someone who works for them), finding no statistically significant spiratory cancers due to traffic pollution. While the reasons for this are
results in 2003 (p = 0.18), 2008 (p = 0.34) and 2015 (p = 0.93). not completely clear, it indicates an important at-risk group that war-
Smoking rates in the low income group were 19.61%, 19.46% and rants additional focus by policy makers and health providers.
16.48%, and in the high were 17.58%, 17.05% and 17.25%, in 2003,
2008 and 2015, respectively. Therefore, this slight (and non-statisti- Acknowledgments
cally significant) difference in smoking rates between the two groups
would not be sufficient to explain the disparity in IRRs. Moreover, We thank the National Council for Scientific and Technological
previous western studies have found associations between air pollution Development (CNPq) – Process number 475362/2012-8, and the State
and lung cancer in non-smoking groups (Beelen et al., 2008b; Hamra of São Paulo Research Foundation (FAPESP) – FAPESP/PPP-SUS 2006/
et al., 2014; Raaschou-Nielsen et al., 2011; Turner et al., 2011). 61616-5.
An additional limitation is that as respiratory cancers have long We also acknowledge the São Paulo Municipal Population-Based
latency periods, and the specific exposures responsible for the measured Cancer Registry and the São Paulo Municipal Health Department for the
outcomes likely occurred before the period in this study, requiring us to availability of the databases and the Institute for Risk Assessment

249
A.G. Ribeiro et al. Environmental Research 170 (2019) 243–251

Sciences – IRAS, Utrecht University, The Netherlands, as an important Fischer, P.H., Marra, M., Ameling, C.B., Hoek, G., Beelen, R., de Hoogh, K., Breugelmans,
partner in this work. O., Kruize, H., Janssen, N.A.H., Houthuijs, D., 2015. Air Pollution and Mortality in
Seven Million Adults: the Dutch Environmental Longitudinal Study (DUELS).
Environ. Health Perspect. 123, 697–704. https://doi.org/10.1289/ehp.1408254.
Funding Galobardes, B., Lynch, J., Smith, G.D., 2007. Measuring socioeconomic position in health
research. Br. Med. Bull. 81–82, 21–37. https://doi.org/10.1093/bmb/ldm001.
Habermann, M., Souza, M., Prado, R., Gouveia, N., 2014. Socioeconomic inequalities and
This work was supported by the Brazilian Ministry of Education – exposure to traffic-related air pollution in the city of Sao Paulo, Brazil. Cad Saude
Coordination for the Improvement of Higher Education Personnel Publica 119–125.
(CAPES), Adeylson G. Ribeiro/PDSE Program/Process number Hamra, G.B., Guha, N., Cohen, A., Laden, F., Raaschou-Nielsen, O., Samet, J.M., Vineis,
P., Forastiere, F., Saldiva, P., Yorifuji, T., Loomis, D., 2014. Outdoor particulate
88881.134281/2016-01. matter exposure and lung cancer: a systematic review and meta-analysis. Environ.
Health Perspect. 122. https://doi.org/10.1289/ehp.1408092.
Appendix A. Supporting information Hamra, G.B., Laden, F., Cohen, A.J., Raaschou-Nielsen, O., Brauer, M., Loomis, D., 2015.
Lung cancer and exposure to nitrogen dioxide and traffic: a systematic review and
meta-analysis. Environ. Health Perspect. 123, 1107–1112. https://doi.org/10.1289/
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