Environmental Research 144 (2016) 6065

Contents lists available at ScienceDirect

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

The association between lung cancer incidence and ambient air

pollution in China: A spatiotemporal analysis
Yuming Guo a,n,1, Hongmei Zeng b,1, Rongshou Zheng b, Shanshan Li a, Adrian G. Barnett c,
Siwei Zhang b, Xiaonong Zou b, Rachel Huxley d, Wanqing Chen b,nn, Gail Williams a
a

Division of Epidemiology and Biostatistics, School of Public Health, University of Queensland, Brisbane, Australia
National Ofce for Cancer Prevention and Control, National Cancer Center, Chinese Academy of Medical Sciences, Cancer Hospital, Beijing, China
c
School of Public Health and Social Work & Institute of Health and Biomedical Innovation, Queensland University of Technology, Brisbane, Australia
d
School of Public Health, Curtin University, Perth, Australia
b

art ic l e i nf o

a b s t r a c t

Article history:
Received 11 September 2015
Received in revised form
2 November 2015
Accepted 3 November 2015

Background: China is experiencing more and more days of serious air pollution recently, and has the
highest lung cancer burden in the world.
Objectives: To examine the associations between lung cancer incidence and ne particles (PM2.5) and
ozone in China.
Methods: We used 75 communities data of lung cancer incidence from the National Cancer Registration
of China from 1990 to 2009. The annual concentrations of ne particles (PM2.5) and ozone at 0.1
0.1
spatial resolution were generated by combing remote sensing, global chemical transport models, and
improvements in coverage of surface measurements. A spatial age-period-cohort model was used to
examine the relative risks of lung cancer incidence associated with the air pollutants, after adjusting for
impacts of age, period, and birth cohort, sex, and community type (rural and urban) as well as the spatial
variation on lung cancer incidence.
Results: The relative risks of lung cancer incidence related to a 10 mg/m3 increase in 2-year average PM2.5
were 1.055 (95% condence interval (CI): 1.038, 1.072) for men, 1.149 (1.120, 1.178) for women, 1.060
(1.044, 1.075) for an urban communities, 1.037 (0.998, 1.078) for a rural population, 1.074 (1.052, 1.096) for
people aged 3065 years, and 1.111 (1.077, 1.146) for those aged over 75 years. Ozone also had a signicant association with lung cancer incidence.
Conclusions: The increased risks of lung cancer incidence were associated with PM2.5 and ozone air
pollution. Control measures to reduce air pollution would likely lower the future incidence of lung
cancer.
& 2015 Elsevier Inc. All rights reserved.

Keywords:
Air pollution
Lung cancer incidence
Fine particles
Ozone
Spatial age-period-cohort study

1. Introduction
Lung cancer is now the most common cancer in the world, with
the majority of the cases in developing countries (Ferlay et al.,
2010; Jemal et al., 2011). China has the highest lung cancer burden
in the world (Zhao et al., 2010). According to the latest Chinese
cancer registration annual report, the world age-standardized incidence rate of lung cancer was 47.5 per 100,000 for men and 22.2
per 100,000 for women in 2009 (Chen et al., 2013), and these
incidences are expected to rise (Chen et al., 2011).
Determining the risk factors associated with this high burden is
crucial for cancer prevention and control. The established risk
n

Corresponding author.
Corresponding author.
E-mail addresses: y.guo1@uq.edu.au (Y. Guo), chenwq@cicams.ac.cn (W. Chen).
1
These authors contributed equally to the study.

nn

http://dx.doi.org/10.1016/j.envres.2015.11.004
0013-9351/& 2015 Elsevier Inc. All rights reserved.

factors for lung cancer include smoking (Correa et al., 1983;

Hackshaw et al., 1997; Hecht, 2002; Janerich et al., 1990) and air
pollution (Cohen, 2000; Mumford et al., 1987; Pope et al., 2002;
Vineis et al., 2004). In particular, ambient air pollution is the most
widespread environmental carcinogen (Cohen, 2000; Vineis et al.,
2004). Globally, it is estimated that 12.8% of lung cancer death can
be attributed to exposure of the ne particulate matter air pollution alone (Evans et al., 2013; Fajersztajn et al., 2013). In 2010, an
estimated 223,000 deaths from lung cancer worldwide were attributed to air pollution (Straif et al., 2013).
With the rapid economic growth and increased urbanization of
rural areas, China is experiencing very high concentrations of air
pollutants (Brauer et al., 2012). The average concentration of ne
particulate matter in densely populated regions of China can exceed 100 g/m3 (Guo et al., 2013). However, studies on ambient air
pollution and lung cancer have never been performed at the national level. In the present study, we investigated lung cancer

Y. Guo et al. / Environmental Research 144 (2016) 6065

incidence in relation to long-term exposure to two ambient air

pollutants, ne particulate matter (PM2.5) and ozone (O3), using
population-based national cancer registration data of China.

2. Methods
2.1. Study design and participants
The National Cancer Registration Center of China is responsible
for the collection, evaluation and publication of cancer statistics
from population-based cancer registries in China each year since
1970s. All data on cancer incidence are reported to populationbased cancer registries from hospitals, community health centers
or other departments, including centers of township medical insurance and the New-type Rural Cooperative Medical System.
Based on the integrity and quality of lung cancer data, a total of 75
cancer registries out of 104 (72%) from the national cancer database were selected from 1990 to 2009 in this study (Fig. 1). ICD10
(International Classication of Disease for Oncology, version 10)
was used to classify lung cancer cases. The detailed information on
each case including year and age at diagnosis, gender and community type (rural or urban area) was used. Population data was
collected for each community and year from local statistics bureaus. We limited analyses to persons at least 30 years old, because
few cases occurred below this age. We stratied the lung cancer
incidence into 12 age groups (3034 years, 3539 years, 4044
years, 8084 years, and 85 years) for each community.
2.2. Exposure assessment
We used data on annual mean PM2.5 and O3 for the years 1990
and 2005 from a previous study (Brauer et al., 2012), which estimated the concentration of global air pollution to assess the global
burden of disease attributable to outdoor air pollution. In brief,
Ambient PM2.5 and O3 exposures for the Earths entire human

61

population were estimated, which allowed the inclusion of populations in smaller cities and rural areas to examine the disease
burden related to air pollution. Remote sensing, global chemicaltransport models, and improvements in coverage of surface measurements were combined to estimate the global estimates of
annual average ambient concentrations of PM2.5 and O3 at
0.1
0.1 spatial resolution for the years 1990 and 2005.
We spatially matched our study communities with the global
air pollution data using latitude and longitude for the years 1990
and 2005. We then predicted the annual concentrations of PM2.5
and O3 during the years 19902009 for each community using a
linear regression model, because the data for air pollution is only
available for the years 1990 and 2005.
Lastly we linked the lung cancer incidence data and predicted
annual concentrations of PM2.5 and O3 during the years 1990
2009 for each of the 75 communities.
2.3. Statistical analysis
Age-period-cohort models can separate the effects of age from
the effects of risk factors in relation to calendar time and birth
cohort effects (Robertson and Boyle, 1998). The incidence of lung
cancer increases with age, and there were substantial birth cohort
effect and period effect (Eilstein et al., 2008; Mdzinarishvili et al.,
2009). In this study, we therefore included separate variables for
age, period, and cohort effects, and gradually extended the model
to include information on air pollution. Thus we examined the
association between air pollution and lung cancer incidence after
controlling for the effects of age, period, and birth cohort. As there
might be spatial cluster in lung cancer incidence, we also included
a spatial term in the analyses to control for the spatial distribution
of lung cancer incidence (Mdzinarishvili et al., 2010).
We used an over-dispersed Poisson regression model to t the
spatial age-period-cohort model:

Lung cancer
rate/100,000

500

1000 1500 km

32.171.1
71.1110
110148
148187
187225
225264
264303
303380
380419

Fig. 1. The location of the 75 study communities and standardized lung cancer incidence rate for people aged 4 30 years in urban (red colour) and rural (purple colour)
China, during 19902009. The rate was standardized by world Segi's population 1985. (For interpretation of the references to colour in this gure legend, the reader is
referred to the web version of this article.)

62

Y. Guo et al. / Environmental Research 144 (2016) 6065

Log (t, i ) = + Age + S(Period) + Cohort + Gender

+ Location + S(latitude, longitude)
+ offset(log(population))

(1)

where t is the year of the observation; i is the community of the

lung cancer incidence; Yt,i is the observed yearly incidence counts
on year t at community i; is the intercept; Age is a categorical
variable of age group for lung cancer incidence,and is vector of
coefcients for Age. S(.) is a natural cubic spline and Period is the
year of lung cancer incidence. Cohort is a categorical variable representing birth cohort (year of birth), and is vector of coefcients. Gender represents the gender category and is the vector

of corresponding coefcients. Location is a binary variable that is

1 for urban areas and 0 for rural areas. A exible spatial term
latitude, longitude smoothed using a natural cubic spline was
used to control for spatial variation in lung cancer incidence. The
degrees of freedom for spline functions were chosen using the
Akaike information criterion for quasi-Poisson models (Q-AIC). The
log of the population size for each age group for each community
was modelled as the offset.
Model (1) was used to control for the effects of age, period,
birth cohort, and gender, as well as the spatial variation on lung
cancer incidence. To examine the association between air pollutants and lung cancer incidence, we added 2-year average PM2.5
and 2-year average O3 separately to Model (1). We used a linear

PM2.5
350

PM2.5 (ug/m3)

300
250
200
150
100
50

O3

O3 (ppb)

70
60
50
40

Fig. 2. The spatial distribution of mean concentrations of modelled PM2.5 (mg/m3) and O3 (ppb) in China during the study period.

Y. Guo et al. / Environmental Research 144 (2016) 6065

term for PM2.5 and O3, as our initial analyses showed the associations between PM2.5 and O3 and lung cancer incidence were
linear. We also examined the effects of air pollutants on lung
cancer incidence separately for men, women, rural residents, urban residents, people aged 3065 years, people aged 6575 years,
and those aged over 75 years.
A series of sensitivity analyses were conducted to check the
robustness of our results. We removed the period and spatial term
respectively from the spatial age-period-cohort model, to examine
whether we underestimated the associations between air pollutants and the lung cancer incidence. To consider the uncertainties
of the predicted annual concentrations of air pollutants, for each
community we simulated 10,000 data set for PM2.5 and O3 respectively by adding random residuals (mean 0 with standard
deviation 5). We rerun the spatial age-period-cohort model
10,000 times for PM2.5 and O3 respectively using the simulated
data set. We calculated the mean of the effect estimates and
condence intervals.

3. Results

Table 1
The relative risks of lung cancer incidence associated with an increase of 10 mg/m3
in PM2.5 and an increase of 10 ppb in O3 in difference groups in China, during 1990
2009.
Group

PM2.5

All
Male
Female
Urban
Rural
Age 3065
Age 6575
Age475

1.074
1.055
1.149
1.060
1.037
1.074
1.101
1.111

0.0

0.12

0.5

0.04

0.12

2.0

0.2
60

80

PM2.5 (ug/m3)

100

(1.079, 1.095)
(1.082, 1.102)
(1.065, 1.094)
(1.075, 1.092)
(0.980, 1.028)
(1.071, 1.096)
(1.105, 1.133)
(1.081, 1.115)

0.04

1.5

40

1.087
1.092
1.080
1.083
1.004
1.083
1.119
1.098

To the best of our knowledge, this study is the rst to assess the

0.2

20

(1.060, 1.089)
(1.038, 1.072)
(1.120, 1.178)
(1.044, 1.075)
(0.998, 1.078)
(1.052, 1.096)
(1.076, 1.126)
(1.077, 1.146)

4. Discussion

0.5

1.0

O3

increase of 10 mg/m3 in PM2.5 and an increase of 10 ppb in O3 were

associated with relative risks of 1.074 (95% condence interval
(CI): 1.060, 1.089) and 1.087 (1.079, 1.095) in lung cancer incidence,
respectively. Women, urban residents, and the elderly had higher
relative risks of lung cancer associated with exposure to PM2.5
than men, rural residents, and the young, respectively. Urban residents and the elderly had higher relative risks of lung cancer
associated with exposure to O3 than rural residents and the young,
respectively.
Within both men and women, urban residents had a higher
risk of lung cancer associated with exposure to PM2.5 and O3 than
those living in rural areas (Table 2). Women had similar raised
relative risks of lung cancer related to exposure to PM2.5 across all
ages, but elderly men had higher risks than young men. We found
similar patterns for O3.
We further examined the relative risks of lung cancer incidence
associated with PM2.5 and O3 by geographical area (Table 3). In
general, the effects estimates of lung cancer associated with air
pollutants were higher in urban area than those in rural area,
except for people aged 3065 years with exposure to PM2.5. The
elderly urban resident had a greater risk of lung cancer related to
exposure to PM2.5 and O3 than the young urban resident.
When we removed the period and spatial terms from the
models, respectively, the effect estimates were slightly increased
but not signicantly. When rerun the models using the simulated
data set with random residuals, the mean effect estimates were
not changed, but the condence intervals were slightly wide.

Log (RR)

Log (RR)

There were 368,762 lung cancer cases, including 247,533 (67%)

men and 312678 (85%) cases living in urban area. Table S1 shows
the rates of lung cancer incidence in China from 1990 to 2009. The
crude rates of lung cancer incidence increased signicantly from
1990 to 2009 for all groups. However, the standardized rates
changed slightly during the study period for all groups. Men had
higher crude and standardized rates than women. There was
spatial variation in the standardized lung cancer incidence rate
across China (Fig. 1). Lung cancer rates increased with age across
different periods and birth cohorts, while the rates unchanged
along the period (Supplemental material, Fig. S1). However, lung
cancer cases increased along the period, and early birth cohorts
had high lung cancer cases (Supplemental material, Fig. S2)
The spatial distribution of PM2.5 and O3 in China is shown in
Fig. 2. For PM2.5, the central-east and northwest of China were
highly polluted. O3 levels were high in the north and southwest of
China. Concentrations of both PM2.5 and O3 were higher in urban
areas than in rural areas (Supplemental material, Table S2).
Fig. 3 shows the associations between lung cancer incidence
and exposure to 2-year average of PM2.5 and O3 in China during
19902009. Generally, both PM2.5 and O3 had linear effects on lung
cancer incidence, which means the higher concentrations of PM2.5
and O3, the higher risk of lung cancer incidence in China.
The associations between PM2.5 and O3 and lung cancer incidence in different groups are shown in Table 1. A two-year

63

40

50

60

70

O3 (ppb)

Fig. 3. : The associations between PM2.5, O3 and lung cancer incidence in China during 19902009, using spatial age-period-cohort design. A natural cubic spline with
4 degrees of freedom was used for PM2.5 and O3, respectively.

64

Y. Guo et al. / Environmental Research 144 (2016) 6065

Table 2
The relative risks of lung cancer incidence associated with an increase of 10 mg/m3 in PM2.5 and an increase of 10 ppb in O3 in the subgroups of women and men in China,
during 19902009.
Group

Urban
Rural
Age 3065
Age 6575
Age4 75

O3

PM2.5
Women

Men

1.128
1.061
1.176
1.175
1.163

1.042
1.033
1.038
1.102
1.084

(1.097, 1.159)
(0.985, 1.143)
(1.132, 1.222)
(1.125, 1.226)
(1.101, 1.228)

(1.024, 1.061)
(0.988, 1.080)
(1.013, 1.063)
(1.073, 1.132)
(1.044, 1.126)

associations between ambient PM2.5 and O3 and lung cancer in

China. A large data set of 75 communities spread across the
country during 19902009 was used in present study. We developed the spatial age-period-cohort mode which tted the data
very well (Supplemental material, Fig. S3). There were statistically
signicant associations between PM2.5 and O3 and lung cancer in
China. In general, the effects of air pollution on lung cancer were
greater in women, elderly and urban people than those in men, the
young, and rural people, respectively.
The present study found signicant associations between ambient air pollution and lung cancer in China. Many studies in USA
and Europe have reported that ambient air pollutants including
particulate matter and ozone were associated with the risk for
lung cancer incidence or deaths (Cohen, 2000; Pope et al., 2002;
Raaschou-Nielsen et al., 2013; Vineis et al., 2004). Studies showed
signicant associations between risk for lung cancer incidence and
PM2.5 with relative risks of 1.18 (95% CI 0.96, 1.46) per 5 g/m3 in
Europe (Raaschou-Nielsen et al., 2013) and in Italy 1.05 (1.01, 1.10)
per 10 g/m3 (Cesaroni et al., 2013).
Recently, the International Agency for Research on Cancer
(IARC) has concluded that outdoor air pollution causes lung cancer
(Straif et al., 2013). However, no study has reported the relationship between ambient PM2.5 and O3 and lung cancer in China. A
cohort study showed that an increase of 10 g/m3 of total suspended particle, sulphur dioxide, and nitrogen oxides corresponded to 1.1% (95% CI:  0.1%, 2.3%), 4.2% (95% CI: 2.3%, 6.2%),
and 2.7% (95% CI:  0.9%, 6.5%) increase of lung cancer mortality in
China (Cao et al., 2011).
One interesting nding is that the relative risks of lung cancer
incidence associated with PM2.5 were higher in women than in
men, but not signicant for O3. Importantly, in China, smoking was
more prevalent among men (63%) than women (4%) (Yang et al.,
1999). Several epidemiological studies have reported that the
signicant association of air pollution and lung cancer mainly exist
in non-smokers (Raaschou-Nielsen et al., 2011) and never-smokers
(Beelen et al., 2008; Raaschou-Nielsen et al., 2010). The potential
biological mechanism for women being more sensitive to outdoor
air pollution than men might be that women have smaller lung
size and airway diameter. This might increase women's airway
reactivity and exacerbate particulate deposition (Bennett et al.,
1996). However, further individual level studies collecting clinic,
behavioural, and demographic data may help elucidate why

Women

Men

1.076
0.963
1.094
1.093
1.095

1.089
1.015
1.080
1.135
1.096

(1.061, 1.092)
(0.919, 1.009)
(1.071, 1.117)
(1.068, 1.118)
(1.067, 1.125)

(1.078, 1.099)
(0.986, 1.044)
(1.065, 1.096)
(1.118, 1.153)
(1.075, 1.117)

women are likely to be the more vulnerable than men.

People living in urban areas are more likely to develop lung
cancer than those living in rural area. This might be caused by the
more serious air pollution in urban area than rural area (Li et al.,
2014). Our data shows that people living urban cities have higher
exposures to air pollution than those living in rural areas (Table
S2). In addition, urban air pollution combines toxic effects from
many constituents, leading to more severe effects on human
health (Yue et al., 2013).
The elderly were more vulnerable to air pollution associated
with lung cancer than the young. The elderly are more sensitive
than younger people to the air pollution both in terms of physiology and behaviour. It is acknowledged that many physiological
regulatory functions weaken with age (Collins, 1987). This means
their bodies are less able to compensate for the impacts of air
pollutants, which might increase risks of health events. In addition, the elderly usually spends more time outdoors than the
young because of work necessities, which many result in that the
elderly experiences greater exposure to the outdoor air pollution
than the young (Tong et al., 2015). Many studies have found that
the relative risks of morality or morbidity associated with air
pollutants were higher in elderly than the young in China (Chen
et al., 2012a, 2012b).
This study has several strengths. To the best of our knowledge,
this is the rst study to examine the associations between PM2.5
and O3 and lung cancer incidence in China. We used national lung
cancer registration data at 75 communities with varying air pollution exposure levels. The exposure assessment of air pollution
used a standardized protocol from the global burden disease study
(Brauer et al., 2012). The spatial age-period-cohort model was
used, which produced a high predictive ability. Our study overcomes several limitations of previous cohort studies, for example,
broad national coverage and lung cancer incidence as the
outcome.
There are also some limitations. We did not control for the
trend of smoking rate, as smoking data at this detailed spatial level
were not available. We only had air pollution data for the years
1990 and 2005, and interpolated the data to 19902009. This
might underestimate the effect estimates of air pollution on lung
cancer, because random measurement error in exposure will bias
the effect estimates towards the null (Hutcheon et al., 2010).
However, our sensitivity analyses showed that the effect estimates

Table 3
The relative risks of lung cancer incidence associated with an increase of 10 mg/m3 in PM2.5 and an increase of 10 ppb in O3 in the subgroups of rural and urban areas in China,
during 19902009.
Group

Age 3065
Age 6575
Age4 75

PM2.5

O3

Rural

Urban

Rural

Urban

1.042 (0.986, 1.102)

0.992 (0.929, 1.058)
1.071 (0.976, 1.176)

1.042 (0.974, 1.115)

1.037 (0.965, 1.116)
1.148 (1.039, 1.267)

1.001 (0.961, 1.043)

0.967 (0.923, 1.012)
0.879 (0.826, 0.934)

1.049 (1.032, 1.067)

1.071 (1.054, 1.088)
1.079 (1.060, 1.098)

Y. Guo et al. / Environmental Research 144 (2016) 6065

did not change when we added random residuals to the annual

concentrations. This study used community-level incidence and
air pollution exposure, but not individual level information on
exposure and outcome. community-level exposure may introduce
exposure bias which might make the our effect estimates smaller
than the real associations (Hutcheon et al., 2010). However, this
study is still useful and important, especially in the context that
China has dearth of studies evaluating long-term exposure effects
of air pollution on lung cancer.

5. Conclusions
The ndings suggest that lung cancer is associated with ambient air pollution in China. Air pollution is a serious problem in
China, and on the basis of our ndings, decrease in concentrations
of air pollution can be expected to greatly reduce the future
number of lung cancer cases in China.

Conict of interests
The authors have declared that no competing interests exist.

Ethical approval
This study was approved by the University of Queenslands
behavior and social sciences ethical review committee
(#2013000739).

Acknowledgements
We gratefully acknowledged the cooperation of all the population-based cancer registries in providing cancer statistics, data
collection, sorting, verication and database creation. YG is supported by the University of Queensland Research Fellowship. The
study was funded by Hope Run Malathon Fund (Cancer Institute &
Hospital, Chinese Academy of Medical Sciences, LC2011Y41), and
the Australia National Health and Medical Research Council
(#APP1030259). No funding bodies had any role in study design,
data collection and analysis, decision to publish, or preparation of
the manuscript.

Appendix A. Supplementary material

Supplementary data associated with this article can be found in
the online version at http://dx.doi.org/10.1016/j.envres.2015.11.
004.

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