Environmental Research 191 (2020) 110052

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

An ecological analysis of long-term exposure to PM2.5 and incidence of

COVID-19 in Canadian health regions
David M. Stieb a, b, *, Greg J. Evans c, Teresa M. To d, e, Jeffrey R. Brook c, d, Richard T. Burnett b
a
Environmental Health Science and Research Bureau, Health Canada, 420-757 West Hastings St., Federal Tower, V6C 1A1, Vancouver, BC, Canada
b
School of Epidemiology and Public Health, University of Ottawa, Room 101, 600 Peter Morand Crescent, K1G 5Z3, Ottawa, ON, Canada
c
Department of Chemical Engineering, University of Toronto, 200 College Street, M5S 3E5, Toronto, ON, Canada
d
Dalla Lana School of Public Health, University of Toronto, Health Sciences Building, 155 College Street, 6th Floor, M5T 3M7, Toronto, ON, Canada
e
Child Health Evaluative Sciences, Research Institute, The Hospital for Sick Children, M5G 1X8, Toronto, ON, Canada

A R T I C L E I N F O A B S T R A C T

Keywords: Background: Ambient fine particulate matter (PM2.5) is associated with a wide range of acute and chronic health
Fine particulate matter effects, including increased risk of respiratory infection. However, evidence specifically related to novel coro­
COVID-19 navirus disease (COVID-19) is limited.
Incidence
Methods: COVID-19 case counts for 111 Canadian health regions were obtained from the COVID-19 Canada Open
Respiratory infection
Data portal. Annual PM2.5 data for 2000–2016 were estimated from a national exposure surface based on remote
Ecological
sensing, chemical transport modelling and ground observations, and minimum and maximum temperature data
for 2000–2015 were based on a national interpolated surface derived from thin-plate smoothing splines. Pop­
ulation counts and sociodemographic data by health region were obtained from the 2016 census, and health data
(self-rated health and prevalence of smoking, obesity, and selected chronic diseases) by health region, were
obtained from the Canadian Community Health Survey. Data on total number of COVID-19 tests and changes in
mobility comparing post-vs. pre-introduction of social distancing measures were available by province. Data
were analyzed using negative binomial regression models.
Results: After controlling for province, temperature, demographic and health characteristics and days since peak
incidence by health region, long-term PM2.5 exposure exhibited a positive association with COVID-19 incidence
(incidence rate ratio 1.07, 95% confidence interval 0.97–1.18 per μg/m3). This association was larger in
magnitude and statistically significant in analyses excluding provinces that reported cases only for aggregated
health regions, excluding health regions with less than median population density, and restricted to the most
highly affected provinces (Quebec and Ontario).
Conclusions: We observed a positive association between COVID-19 incidence and long-term PM2.5 exposure in
Canadian health regions. The association was larger in magnitude and statistically significant in more highly
affected health regions and those with potentially less exposure measurement error. While our results generate
hypotheses for further testing, they should be interpreted with caution and require further examination using
study designs less prone to bias.

Abbreviations: AIC, Akaike Information Criterion; ANUSPLIN, Australian National University spline; AOD, aerosol optical depth; CANUE, Canadian urban
environmental health research consortium; CCHS, Canadian community health survey; CI, confidence interval; COPD, chronic obstructive pulmonary disease;
COVID-19, novel coronavirus disease; GEOS-Chem, Goddard earth observing system chemical transport model; IRR, incidence rate ratio; LICO, low income cutoff;
MERS, middle east respiratory syndrome; MISR, multi-angle imaging spectroradiometer; MODIS, moderate resolution imaging spectroradiometer; NASA, National
Aeronautics and Space Administration; NDVI, normalized difference vegetation index; PM2.5, fine particulate matter; SARS-CoV-1, severe acute respiratory syn­
drome; SeaWiFS, sea-viewing wide field-of-view sensor.
* Corresponding author. 420-757 West Hastings St, Vancouver, BC, V6C 1A1, Canada.
E-mail addresses: dave.stieb@canada.ca (D.M. Stieb), greg.evans@utoronto.ca (G.J. Evans), teresa.to@sickkids.ca (T.M. To), jeff.brook@utoronto.ca (J.R. Brook),
rtburnett1@gmail.com (R.T. Burnett).

https://doi.org/10.1016/j.envres.2020.110052
Received 28 May 2020; Received in revised form 16 July 2020; Accepted 5 August 2020
Available online 26 August 2020
0013-9351/Crown Copyright © 2020 Published by Elsevier Inc. This is an open access article under the CC BY-NC-ND license
(http://creativecommons.org/licenses/by-nc-nd/4.0/).
D.M. Stieb et al.
1. Introduction
There is considerable evidence from multiple lines of research
including toxicology, human clinical studies and epidemiological
studies that air pollution in general and fine particulate matter (PM2.5)
more specifically are associated with a wide range of acute and chronic
health effects (Thurston et al., 2017). Based on estimates from the Global
Burden of Disease initiative, PM2.5 accounts for the greatest burden of
mortality of any environmental exposure, accounting for approximately
3 million worldwide deaths annually (GBD, 2017 Risk Factor Collabo­
rators, 2018). It is well established that acute exposure increases the risk
of emergency visits and hospital admissions for respiratory infections
including pneumonia (Atkinson et al., 2014; Domingo and Rovira, 2020;
Nhung et al., 2017). There is also a growing body of evidence that long
term exposure increases the risk of morbidity and mortality from res­
piratory infection (Mehta et al., 2013; Neupane et al., 2010).
Evidence specifically related to PM2.5 and novel coronaviruses such
as severe acute respiratory syndrome coronavirus (SARS-CoV-1) and
middle east respiratory syndrome (MERS) is limited. Studies based on
the SARS-CoV-1 outbreak suggest that meteorology and exposure to air
pollution increased transmission (Cai et al., 2007) and worsened patient
prognosis (Kan et al., 2005). Notably SARS-CoV-1 patients from more
polluted regions were twice as likely to die as those in less polluted
places (Cui et al., 2003). There is also evidence that air pollution
exposure more generally adversely affects respiratory immune defences
(Domingo and Rovira, 2020; Yang et al., 2020), and emerging evidence
suggesting that novel coronavirus disease (COVID-19) incidence and
mortality may be increased in relation to both acute (Zhu et al., 2020)
and chronic exposure (Andree, 2020; Liang et al., 2020; Ogen, 2020; Wu
et al., 2020). This evidence implies that deterioration in air quality over
short time periods (e.g. from wildfire smoke, other local burning, spe­
cific meteorological events such as temperature inversions) may lead to
more cases of severe COVID-19 infections, adding further demand to the
healthcare system. Conversely, improving air quality by reducing both
the occurrence of acute events and long term average concentrations,
may help to protect communities from COVID-19 and reduce the burden
on hospitals.
In this study, we conduct an ecological analysis of COVID-19 cases
and 17 year average PM2.5 concentrations among Canadian health re­
gions. While ecological analyses have many limitations which preclude
attribution of cause and effect, they can be readily conducted once data
are available and permit the generation of hypotheses to be more
rigorously examined in subsequent studies.
2. Materials and methods
COVID-19 case counts compiled from publicly available reports for
111 health regions were obtained from the COVID-19 Canada Open Data
portal (Berry et al., 2020). Health regions are defined by provincial
ministries of health; in some jurisdictions, they correspond to areas
served by local public health departments or authorities (Statistics
Canada, 2018a). The provinces of British Columbia and Saskatchewan
reported counts for groups of health regions (up to four per group),
which we distributed to individual health regions in proportion to
population. Similarly, health region was not reported for many cases in
Nova Scotia. These were distributed among four health regions in pro­
portion to population. In an attempt to account for stage of outbreak,
response to distancing measures, and correlation between case counts
and deaths, we also obtained data on days elapsed since the first case,
days since peak daily incidence of new cases, and deaths at the health
region level (Berry et al., 2020), as well as date of declaration of public
health emergency or state of emergency at the provincial level (Boir­
e-Schwab et al., 2020). Total number of COVID-19 tests was only
available by province. Annual PM2.5 data for 2000–2016 were derived
from a surface combining a 0.01◦ × 0.01◦ (approximately 1 km × 1 km)
resolution Aerosol Optical Depth (AOD) retrieval from the National
2
Environmental Research 191 (2020) 110052
Aeronautics and Space Administration (NASA) Moderate Resolution
Imaging Spectroradiometer (MODIS), Multi-angle Imaging SpectroR­
adiometer (MISR), and Sea-Viewing Wide Field-of-View Sensor (Sea­
WiFS) instruments, Goddard Earth Observing System chemical transport
model (GEOS-Chem) simulations, and ground observations (van Don­
kelaar et al., 2019). Values prior to 2004 were temporally adjusted (Boys
et al., 2014). These data have been used extensively in air pollution
epidemiology studies in Canada (Pappin et al., 2019). Greenness data for
2000–2019 were based on growing season maximum normalized dif­
ference vegetation index (NDVI) data from the MODIS onboard the
Terra satellites (Didan, 2015; Gorelick et al., 2017). NDVI values vary
from − 1 to 1, negative values indicating features such as water and
positive values indicating vegetation. We employed positive values only
in calculating average greenness by health region. Temperature data for
2000–2015 (annual minimum of lowest monthly maximum temperature
– henceforth referred to as “minimum temperature,” and annual
maximum of highest monthly minimum temperature – henceforth
referred to as “maximum temperature”) were based on a national
interpolated surface of available observations derived using thin-plate
smoothing splines, implemented in Australian National University
Spline (ANUSPLIN) climate modeling software (Wang et al., 2018). All
exposure data were available by 6 character postal codes (CANMAP
2015), which were mapped to 2018 health region boundaries in R
(GISTools (Brunsdon and Chen, 2014), rgdal (Bivand et al., 2019) and
raster (Hijmans, 2020) packages). Postal codes are used by Canada Post
corporation for mail delivery, and are analogous to American zip codes –
there are currently approximately 875,000 postal codes in Canada; as
they are point locations, they do not have a specified surface area
(CANUE, 2018). Maps were generated using the ggplot2 (Wickham,
2016) and broom (Robinson and Hayes, 2020) packages. Population
counts and sociodemographic data by health region on percent of pop­
ulation 65 or older, with income less than the low income cutoff (LICO),
and Black (Adams et al., 2020; Dyer, 2020; Yancy, 2020), were obtained
from the 2016 census (Statistics Canada, 2018b). LICOs are defined as
income levels below which families spend a disproportionate share of
their income on necessities, and are family-size and community-size
specific (Statistics Canada, 2016). Health data by health region on fac­
tors thought to increase susceptibility to COVID-19 (Adams et al., 2020)
(percent of population who rate health as fair or poor, are daily or oc­
casional smokers, overweight, obese, have asthma, chronic obstructive
pulmonary disease (COPD), hypertension or diabetes), were based on
data from the 2017 and 2018 Canadian Community Health Survey
(CCHS) (Statistics Canada, 2020), which is an annual national
cross-sectional survey of individuals 12 years of age and over. Changes
in mobility by province comparing post- vs. pre-introduction of social
distancing measures were based on aggregated data from Google Ac­
count users who opted-in to location history for their account (Google
LLC, 2020). Correlations among variables were examined using a cor­
relogram based on Spearman correlations (Harrell et al., 2020; Wei and
Simko, 2017).
Data were analyzed using negative binomial regression models,
specifying PM2.5 and covariates (including province) as fixed effects. Log
population was included as an offset. PM2.5 and covariates were first
regressed individually vs. case counts, then those exhibiting statistically
significant associations were included in multivariate models. Preva­
lence of asthma, COPD, hypertension and diabetes were excluded from
multivariate models with PM2.5, since they could be intermediate in a
putative causal pathway with COVID-19 incidence. The most parsimo­
nious model was selected based on the Akaike Information Criterion
(AIC) (Akaike, 1974). Presence of residual spatial autocorrelation was
examined by mapping model residuals and computing Moran’s I (Bivand
and Wong, 2018). Sensitivity analyses were conducted by excluding
Montréal (which accounted for 27.5% of cases but only 5.5% of popu­
lation); excluding British Columbia, Saskatchewan and Nova Scotia
(which reported cases counts only for aggregated health regions);
excluding health regions with less than median population density (with
D.M. Stieb et al.
presumably greater exposure measurement error over larger, more
sparsely populated health regions); restricting the analysis to Ontario
and Quebec, the two provinces with the highest incidence, attributed in
part to provincial level policies on testing (Weeks, 2020), and timing of
school vacation periods (Perreaux, 2020) respectively; and specifying
province as a random rather than fixed effect. Analysis was conducted in
R (R Core Team, 2019) using the lme4 package (Bates et al., 2015).
Research ethics board approval was not required because all data were
publicly available and aggregated at health region level. The work
described here has been carried out in accordance with the Uniform
Requirements for manuscripts submitted to Biomedical journals.
3. Results
There were 73,390 cases up to May 13, 2020 and overall incidence
was 208.8 cases/100,000 (2016 population). Incidence was highest in
Quebec (489.0/100,000) and Ontario (166.5/100,000) and lowest in
Nunavut (0/100,000) and the Northwest Territories (12.0/100,000)
(Fig. 1). The ten health regions with the highest incidence were
distributed among multiple provinces, and included three large cities
(Montréal, Toronto, Calgary), regions surrounding Montréal (Laval,
Lanaudière, Montérégie, Laurentides, Mauricie/Centre-du-Québec), and
one remote northern area (Far North, Saskatchewan) (Supplementary
Table S1). Deaths were very strongly correlated with case counts by
health region (R2 = 0.95). PM2.5 concentrations averaged 6.1 (standard
deviation 2.1) and were highest in urban areas as well as more generally
in southern Ontario and Quebec (Fig. 2). Variability in other exposures,
sociodemographic and health characteristics by health region are sum­
marized in Table 1. There was little variability in days since declaration
of emergency. A correlogram is provided in Fig. S2. PM2.5 was strongly
positively correlated with percent Black, minimum and maximum
temperature. Population density exhibited strong positive correlations
with percent Black and low income, PM2.5, minimum and maximum
temperature, as well as strong negative correlations with prevalence of
obesity and smoking. Prevalence of obesity was strongly positively
correlated with prevalence of diabetes, hypertension and smoking,
while percent age 65 and older was strongly positively correlated with
prevalence of hypertension and COPD. Changes in mobility during the
period March 13 (the date after which social distancing recommenda­
tions were introduced in most provinces)-April 26 vs. January 3-
Fig. 1. COVID-19 incidence by health region. (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of
this article.)
3
Environmental Research 191 (2020) 110052
February 6, were generally comparable among provinces (Supplemen­
tary Table S3). Notably, changes in visits/length of stay were somewhat
more modest in Nunavut, which had no cases, and visits/length of stay
in parks increased substantially in British Columbia, the most populous
regions of which typically experience milder weather during the March/
April period compared to elsewhere in Canada.
Results of regression models are summarized in Table 2. In bivariate
models, PM2.5, minimum and maximum temperature, percent Black
population, percent of population < LICO, population density, and days
since first case were significantly positively associated with COVID-19
counts, while days since peak incidence, percent of population 65 or
older, and prevalence of asthma, COPD, hypertension, overweight and
obesity exhibited significant negative associations. COVID-19 counts
were not significantly associated with total number of tests or percent
change in mobility to work locations by province (not shown). In the
best fitting multivariate model, minimum temperature exhibited a sig­
nificant positive association, and percent age 65 and older and days
since peak incidence exhibited a significant negative association with
COVID-19 counts. PM2.5 and percent low income remained positively
associated with COVID-19 counts, and prevalence of overweight and
obesity remained negatively associated, but the associations were no
longer significant. Additional multivariate models are summarized in
Table S4. The association of PM2.5 with COVID-19 counts was not sen­
sitive to the sequential addition to the best-fitting model of population
density, percent Black population, or days since first case; the PM2.5
coefficient changed by <10% and additional covariates were not
significantly associated with COVID-19 counts. However, the associa­
tion of PM2.5 with COVID-19 counts was sensitive to the removal of
minimum temperature from the best-fitting model (IRR increased to
1.10, 95% CI 1.00–1.21, p < 0.05). Mapping of model residuals and
Moran’s I did not indicate presence of residual spatial autocorrelation.
In sensitivity analyses (Table 3), the association of PM2.5 with
COVID-19 incidence was unchanged when Montréal was excluded or
when province was included as a random effect rather than a fixed ef­
fect. In models excluding British Columbia, Saskatchewan and Nova
Scotia, excluding health regions with less than median population
density, and restricted to Ontario and Quebec, the association of PM2.5
with COVID-19 incidence was larger in magnitude than the national
analysis, and statistically significant. These analyses accounted for
85–95% of cases and 62–82% of population. Notably, in the subset of
D.M. Stieb et al. Environmental Research 191 (2020) 110052

Fig. 2. Long term average PM2.5 concentrations by health region. (For interpretation of the references to colour in this figure legend, the reader is referred to the Web
version of this article.)

Table 1
Summary of sociodemographic characteristics, health measures and exposures by health region.
Minimum 25th %ile Median Mean 75th %ile Maximum

Population (n) 2632 76,626 169,244 316,682 421,538 2,731,571

Population density per km2 0.0 2.2 10.6 212.4 39.0 4848.3
Population density per km2a 10.6 23.2 39.0 418.4 227.9 4848.3
Incidence/100,000 0.0 20.4 54.5 114.0 118.8 1041.8
Days since first case 24 54 59 61 63 109
Days since emergency declared 52 56 57 57. 57 61
Days since peak incidence 4 23 39 35 44 109
Age ≥65 (%) 3.8 15.2 18.0 17.8 21.6 26.4
Black (%) 0.0 0.5 0.7 1.5 1.7 9.5
< Low Income Cut-off (%) 2.5 4.9 6.3 6.9 7.6 18.1
Poor or fair self-rated health (%) 7.0 11.1 12.6 12.9 14.3 21.9
Overweight (%) 28.5 33.7 35.5 35.8 38.0 46.1
Obese (%) 12.1 28.1 32.3 31.9 36.7 47.2
Asthma (%) 4.5 7.2 8.5 8.4 9.5 14.1
COPD (%) 0.0 3.4 4.8 4.8 6.3 9.1
Hypertension (%) 12.1 17.1 19.0 19.4 21.6 29.8
Diabetes (%) 2.7 6.4 7.8 8.0 9.4 14.4
Daily or occasional smoker (%) 8.8 15.7 18.3 18.9 20.6 63.1
Physically active (%) 38.0 50.1 55.0 54.7 58.6 71.9
PM2.5 (μg/m3) 2.0 4.2 6.0 6.1 7.5 11.5
Minimum temperature − 34.9 − 24.6 − 18.0 − 17.8 − 12.4 − 0.9
Maximum temperature 10.3 17.5 19.4 19.2 21.4 23.8
NDVIb>0a 0.54 0.59 0.62 0.62 0.65 0.66
a
For health regions with population density ≥ median.
b
Normalized Difference Vegetation Index.

health regions with population density greater than the median,
greenness exhibited a significant negative association with case counts
on its own, but was no longer significant in a multivariate model which
had a larger AIC than the final model. Results were also similar when
based on data from earlier in the course of the pandemic when there
were 35,986 cases (April 19).
4. Discussion
We found that after controlling for province, temperature, health and
demographic characteristics, and time since peak incidence by health
region, long-term PM2.5 exposure exhibited a non-statistically signifi­
cant positive association with COVID-19 incidence among 111 Canadian
health regions. This association was larger in magnitude and statistically
significant in models excluding provinces which reported cases only for
aggregated health regions, excluding health regions with less than me­
dian population density, and restricted to Ontario and Quebec, in each
case accounting for a majority of COVID-19 cases. The association we
observed parallels that reported in an analysis of PM2.5 and COVID-19
mortality in approximately 3000 US counties (Wu et al., 2020). While
this is striking, especially given the lower COVID-19 incidence and
narrower range of PM2.5 exposure in Canada compared to the US,
findings should be interpreted with caution; the analyses examined
different outcomes (incidence vs. mortality) and associations with PM2.5
in both studies could result from similar biases related to ecologic ana­
lyses. PM2.5 exposures and other risk factors for COVID-19 incidence can
vary over a smaller scale than health region, particularly for large health
regions. Greenness in particular varies at a much smaller scale than
health region, even in predominantly urban health regions. Our analysis
entailed coarser spatial resolution and a much smaller number of health

4
D.M. Stieb et al. Environmental Research 191 (2020) 110052

Table 2 incidence in more highly urban areas with potentially better access and
Summary of regression model results. generally higher PM2.5 concentrations, potentially resulting in a
Variable Bivariatea Multivariatea spurious association between PM2.5 exposure and COVID-19 incidence.
While COVID-19-related hospitalizations and deaths may be less
IRR 95% CI IRR 95% CI
affected by artefacts introduced by differential eligibility for and/or
PM2.5 (per μg/m3) 1.25 1.13–1.38 1.07 0.97–1.18 access to testing by health region, the number of hospitalizations and
Minimum temperatureb 1.64 1.23–2.19 1.42 1.05–1.93
Maximum temperatureb 1.42 1.08–1.86
deaths in Canada is relatively small. At the health region level, a large
Population densityb 1.40 1.19–1.63 number of small or zero counts would be expected, which introduces
Percent age 65+b 0.57 0.48–0.69 0.72 0.59–0.88 other limitations in the analysis. In any case, hospitalization data were
Percent < LICOb 1.57 1.33–1.84 1.12 0.91–1.38 not available nationally at the health region (or smaller) level. Our
Percent Blackb 1.49 1.27–1.75
observation that deaths were very strongly correlated with case counts
Percent asthmab 0.81 0.68–0.97
Percent COPDb 0.61 0.52–0.72 by health region provides evidence that differences in case numbers by
Percent hypertensionb 0.64 0.52–0.79 health region were not driven by differences in testing, which would be
Percent diabetesb 1.03 0.84–1.27 expected to introduce more scatter in the relationship between deaths
Percent physically activeb 0.92 0.70–1.19 and cases. Finally, associations observed based solely on area level
Percent overweightb 0.78 0.65–0.93 0.86 0.71–1.03
Percent obeseb 0.71 0.57–0.87 0.90 0.68–1.20
measures may not exist at the individual level (ecological fallacy).
Percent smokersb 0.97 0.72–1.30 The magnitude of the association both in our study and the US study
Days since first caseb 1.52 1.24–1.86 was several fold larger per unit PM2.5 than hazard ratios typically
Days since peak incidenceb 0.60 0.50–0.72 0.71 0.59–0.84 observed in cohort studies of mortality (Crouse et al., 2015). It is pre­
NDVIc 0.58 0.44–0.77
mature to speculate on pathophysiological mechanistic explanations for
a
Includes log(population) as offset and province as factor. this observation. While there is existing evidence that PM2.5 increases
b
scaled. the risk of respiratory infections, including the SARS virus, the most
c
only health regions with population density greater ≥ median. likely explanation for the large magnitude association is residual con­
founding by unmeasured factors.
In addition to the Wu et al. (2020) study, another American
Table 3
ecological study based on approximately 3000 counties found that ni­
Summary of sensitivity analyses of association of PM2.5 and COVID-19
trogen dioxide (NO2) was significantly associated with COVID-19 mor­
incidence.
tality and case-fatality rates, while PM2.5 exhibited a marginally
Model IRR 95% CI % %
significant association with mortality (Liang et al., 2020). A significant
cases population
positive association of PM2.5 with COVID-19 incidence and hospital
Best fitting multivariate model 1.07 0.97–1.18 99.9a 99.6a admissions was also reported in the Netherlands (Andree, 2020). Ogen
(province as fixed effect)
(2020) reported co-location of high NO2 concentrations estimated from
Exclude Montréal 1.07 0.96–1.18 72.4 94.5
Exclude 3 provinces with 1.15 1.00–1.32b 94.6 81 remote sensing and high COVID-19 mortality counts in northern Italy
aggregated health regions and Madrid. However, the analysis did not account for the underlying
Exclude health regions with 1.16 1.00–1.34b 94.8 82 population at risk, population density, timing of onset of cases or
population density < median
introduction of control measures, or sociodemographic or health char­
Ontario and Quebec only 1.21 1.03–1.40 84.9 61.5
April 19 data (35,986 cases) 1.10 1.01–1.19 99.9 99.6
acteristics. In a time-series study in 120 Chinese cities, significant pos­
Best fitting multivariate model 1.09 0.98–1.21c 99.9a 99.6a itive associations were observed between short term (two week)
(province as random effect) exposure to PM2.5, NO2 and ozone and COVID-19 incidence (Zhu et al.,
a
Five health regions excluded due to missing data. 2020).
b
Lower bound >1 with additional decimal places. We also found that percent Black population was positively associ­
c
Corrected for overdispersion by multiplying standard error by square root of ated with COVID-19 incidence (although it was not included in the final
dispersion factor (Bolker, 2020). multivariate model). This is consistent with reports from the US of
disproportionately high COVID-19 incidence and mortality among Black
regions than US counties. However, analyses excluding provinces that Americans (Dyer, 2020; Yancy, 2020). Percent of population less than
reported cases only for aggregated health regions, excluding health re­ LICO was also positively associated with COVID-19 incidence. Those
gions with less than median population density, and restricted to Quebec with lower income have more barriers to self isolating and social
and Ontario resulted in a larger magnitude and statistically significant distancing. Inequality in access to care affecting access to COVID-19
association, which could reflect reduced exposure measurement error testing and outcome following infection would be expected to be less
for these generally smaller, more densely populated health regions. The in Canada with universal healthcare. Negative associations of percent of
US study also found that the mortality risk ratio was elevated in an population age 65 and older, prevalence of asthma, COPD, hyperten­
analysis restricted to urban areas, but it was no longer significant (Wu sion, overweight and obesity with COVID-19 incidence may reflect a
et al., 2020). Owing to the smaller sample, we were also constrained in higher prevalence in predominantly rural health regions with few cases.
the number of covariates that could be included in multi-variate models. Subsequent studies should examine effects of both acute and chronic
Still, we did account for unmeasured confounders by province by exposure to PM2.5, and air pollution more generally, on COVID-19
specifying it as a fixed or random effect, and found that the magnitude of morbidity and mortality using more highly spatially resolved area
the association was larger in more highly urban and more highly level data, as well as individual level data to determine whether results
affected areas. Mobility data indicated that effects of social distancing from ecological analysis are borne out.
restrictions were generally similar among provinces. We employed
publicly available laboratory confirmed case counts, thus our results are 5. Conclusions
not generalizable to milder or asymptomatic cases which did not un­
dergo laboratory confirmation, and case criteria may differ by province We report an analysis of COVID-19 incidence by Canadian health
and change over time. Data on COVID-19 testing were only available at region. After controlling for temperature, demographic and health
the provincial level. Although criteria for testing are standardized, ac­ characteristics and days from peak incidence by health region, long-term
cess may differ by health region, which could increase the observed PM2.5 exposure exhibited a positive association with COVID-19 inci­
dence, paralleling results of a recent American analysis of mortality. The

5
D.M. Stieb et al.
association was larger in magnitude and statistically significant in more
highly affected health regions and those with potentially less exposure
measurement error. While parallels with US findings are noteworthy,
and generate hypotheses for further testing, results should be inter­
preted with caution and require further examination using study designs
less prone to bias.
Credit author statement
David M. Stieb: Conceptualization, Methodology, Formal analysis,
Data curation, Writing - original draft, Writing - review & editing; Greg
J. Evans: Conceptualization, Methodology, Writing - original draft,
Writing - review & editing, Teresa M. To: Conceptualization, Method­
ology, Writing - original draft, Writing - review & editing, Jeffrey R.
Brook: Conceptualization, Methodology, Data curation, Writing - orig­
inal draft, Writing - review & editing, Richard T. Burnet: Conceptuali­
zation, Methodology, Writing - original draft, Writing - review & editing
Declaration of competing interest
The authors declare that they have no known competing financial
interests or personal relationships that could have appeared to influence
the work reported in this paper.
Acknowledgement
PM2.5 and NDVI metrics, as well as weather-related indicators, based
on custom data from Natural Resources Canada, indexed to DMTI
Spatial Inc. postal codes, were provided by CANUE (Canadian Urban
Environmental Health Research Consortium). The authors thank Dr.
Francesca Dominici and colleagues (Harvard University), for posting
their analysis and mapping code, and providing comments on the draft
manuscript, and Marc Smith-Doiron (Health Canada), for assistance
with mapping PM2.5 exposure. Dr. Eric Lavigne (Health Canada, Uni­
versity of Ottawa), Dr. Markey Johnson (Health Canada), and Mr. Gary
Mallach (Health Canada) provided helpful suggestions on the analysis
and draft manuscript. This research did not receive any specific grant
from funding agencies in the public, commercial, or not-for-profit
sectors.
Appendix A. Supplementary data
Supplementary data to this article can be found online at https://doi.
org/10.1016/j.envres.2020.110052.
References
Adams, M.L., Katz, D.L., Grandpre, J., 2020. Population-based estimates of chronic
conditions affecting risk for complications from coronavirus disease, United States.
Emerg. Infect. Dis. 26 https://doi.org/10.3201/eid2608.200679.
Akaike, H., 1974. A new look at the statistical model identification. IEEE Trans. Automat.
Contr. 19, 716–723. https://doi.org/10.1109/TAC.1974.1100705.
Andree, B.P.J., 2020. Incidence of COVID-19 and connections with air pollution
exposure: evidence from The Netherlands (preprint). medRxiv
2020.04.27.20081562. https://doi.org/10.1101/2020.04.27.20081562.
Atkinson, R.W., Kang, S., Anderson, H.R., Mills, I.C., Walton, H.A., 2014.
Epidemiological time series studies of PM2.5 and daily mortality and hospital
admissions: a systematic review and meta-analysis. Thorax 69, 660–665. https://doi.
org/10.1136/thoraxjnl-2013-204492.
Bates, D., Maechler, M., Bolker, B., Walker, S., 2015. Fitting linear mixed-effects models
using lme4. J. Stat. Software 67, 1–48.
Berry, I., Soucy, J.-P.R., Tuite, A., Fisman, D., 2020. Open access epidemiologic data and
an interactive dashboard to monitor the COVID-19 outbreak in Canada. Can. Med.
Assoc. J. 192, E420. https://doi.org/10.1503/cmaj.75262. https://art-bd.shinyapps.
io/covid19canada/.
Bivand, R., Kitt, T., Rowlington, B., 2019. rgdal: Bindings for the “Geospatial” Data
Abstraction Library. R package version 1.4-8.
Bivand, R, Wong, D, 2018. Comparing implementations of global and local indicators of
spatial association. TEST 27, 716–748.
Boire-Schwab, D., Goldenberg, A., Castonguay, J.-S., Hillstrom, M., Landry-Plouffe, L.,
Demeo, M., Fimiani, M., Lee, C., Naglie, N., Soubolsky, L., Fitz-Simon, N., 2020.
COVID-19 emergency measures tracker [WWW document] (accessed 4.26.20).
6
Environmental Research 191 (2020) 110052
https://www.mccarthy.ca/en/insights/articles/covid-19-emergency-measures-trac
ker.
Bolker, B., 2020. GLMM FAQ [WWW document] (accessed 4.26.20). https://bbolker.gith
ub.io/mixedmodels-misc/glmmFAQ.html#testing-for-overdispersioncomputing-ov
erdispersion-factor.
Boys, B.L., Martin, R.V., van Donkelaar, A., MacDonell, R.J., Hsu, N.C., Cooper, M.J.,
Yantosca, R.M., Lu, Z., Streets, D.G., Zhang, Q., Wang, S.W., 2014. Fifteen-year
global time series of satellite-derived fine particulate matter. Environ. Sci. Technol.
48, 11109–11118. https://doi.org/10.1021/es502113p.
Brunsdon, C., Chen, H., 2014. GISTools: Some Further GIS Capabilities for R. R Package
Version 0, 7-4.
Cai, Q.-C., Lu, J., Xu, Q.-F., Guo, Q., Xu, D.-Z., Sun, Q.-W., Yang, H., Zhao, G.-M.,
Jiang, Q.-W., 2007. Influence of meteorological factors and air pollution on the
outbreak of severe acute respiratory syndrome. Publ. Health 121, 258–265. https://
doi.org/10.1016/j.puhe.2006.09.023.
CanMap Postal Code Suite v2015.3. [computer File] Markham, 2015. DMTI Spatial Inc.
CANUE, 2018. Postal Code User Guide. Canadian Urban Environmental Health Research
Consortium.
Crouse, D.L., Peters, P.A., Hystad, P., Brook, J.R., van Donkelaar, A., Martin, R.V.,
Villeneuve, P.J., Jerrett, M., Goldberg, M.S., Arden Pope, C., Brauer, M., Brook, R.D.,
Robichaud, A., Menard, R., Burnett, R.T., 2015. Ambient PM2.5, O3, and NO2
exposures and associations with mortality over 16 years of follow-up in the Canadian
census health and environment cohort (CanCHEC). Environ. Health Perspect. 123,
1180–1186. https://doi.org/10.1289/ehp.1409276.
Cui, Y., Zhang, Z.-F., Froines, J., Zhao, J., Wang, H., Yu, S.-Z., Detels, R., 2003. Air
pollution and case fatality of SARS in the People’s Republic of China: an ecologic
study. Environ. Health Glob. Access Sci. Source 2, 15. https://doi.org/10.1186/
1476-069X-2-15.
Didan, K., 2015. MOD13Q1 MODIS/Terra Vegetation Indices 16-Day L3 Global 250m
SIN Grid V006 [Data Set], NASA EOSDIS Land Processes DAAC.
Domingo, J.L., Rovira, J., 2020. Effects of air pollutants on the transmission and severity
of respiratory viral infections. Environ. Res. 187, 109650. https://doi.org/10.1016/
j.envres.2020.109650.
Dyer, O., 2020. Covid-19: Black people and other minorities are hardest hit in US. BMJ
369, m1483. https://doi.org/10.1136/bmj.m1483.
GBD 2017 Risk Factor Collaborators, 2018. Global, regional, and national comparative
risk assessment of 84 behavioural, environmental and occupational, and metabolic
risks or clusters of risks for 195 countries and territories, 1990-2017: a systematic
analysis for the Global Burden of Disease Study 2017. Lancet Lond. Engl. 392,
1923–1994. https://doi.org/10.1016/S0140-6736(18)32225-6.
Google LLC, 2020. Google COVID-19 Community Mobility Reports [WWW Document].
https://www.google.com/covid19/mobility/ (accessed 5.4.20).
Gorelick, N., Hancher, M., Dixon, M., Ilyushchenko, S., Thau, D., Moore, R., 2017.
Google Earth engine: planetary-scale geospatial analysis for everyone. Big Remote.
Sensed Data Tools Appl. Exp. 202, 18–27. https://doi.org/10.1016/j.
rse.2017.06.031.
Harrell, F., Dupont, C., others, 2020. Hmisc: Harrell Miscellaneous. R Package Version
4.4-0 (accessed 5.17.20). https://CRAN.R-project.org/package=Hmisc.
Hijmans, R., 2020. Raster: Geographic Data Analysis and Modeling. R Package Version 3,
0-12.
Kan, H.-D., Chen, B.-H., Fu, C.-W., Yu, S.-Z., Mu, L.-N., 2005. Relationship between
ambient air pollution and daily mortality of SARS in Beijing. Biomed. Environ. Sci.
BES 18, 1–4.
Liang, D., Shi, L., Zhao, J., Liu, P., Schwartz, J., Gao, S., Sarnat, J.A., Liu, Y., Ebelt, S.T.,
Scovronick, N.C., Chang, H., 2020. Urban air pollution may enhance COVID-19 case-
fatality and mortality rates in the United States (preprint). medRxiv
2020.05.04.20090746. doi: 10.1101/2020.05.04.20090746.
Mehta, S., Shin, H., Burnett, R., North, T., Cohen, A.J., 2013. Ambient particulate air
pollution and acute lower respiratory infections: a systematic review and
implications for estimating the global burden of disease. Air Qual. Atmosphere
Health 6, 69–83. https://doi.org/10.1007/s11869-011-0146-3.
Neupane, B., Jerrett, M., Burnett, R.T., Marrie, T., Arain, A., Loeb, M., 2010. Long-term
exposure to ambient air pollution and risk of hospitalization with community-
acquired pneumonia in older adults. Am. J. Respir. Crit. Care Med. 181, 47–53.
https://doi.org/10.1164/rccm.200901-0160OC.
Nhung, N.T.T., Amini, H., Schindler, C., Kutlar Joss, M., Dien, T.M., Probst-Hensch, N.,
Perez, L., Kunzli, N., 2017. Short-term association between ambient air pollution and
pneumonia in children: a systematic review and meta-analysis of time-series and
case-crossover studies. Environ. Pollut. Barking Essex 230, 1000–1008. https://doi.
org/10.1016/j.envpol.2017.07.063, 1987.
Ogen, Y., 2020. Assessing nitrogen dioxide (NO2) levels as a contributing factor to
coronavirus (COVID-19) fatality. Sci. Total Environ. 726, 138605. https://doi.org/
10.1016/j.scitotenv.2020.138605.
Pappin, A.J., Christidis, T., Pinault, L.L., Crouse, D.L., Brook, J.R., Erickson, A.,
Hystad, P., Li, C., Martin, R.V., Meng, J., Weichenthal, S., van Donkelaar, A.,
Tjepkema, M., Brauer, M., Burnett, R.T., 2019. Examining the shape of the
association between low levels of fine particulate matter and mortality across three
cycles of the Canadian census health and environment cohort. Environ. Health
Perspect. 127, 107008. https://doi.org/10.1289/EHP5204.
Perreaux, L., 2020. Why Quebec’s Coronavirus Cases Have Skyrocketed. Globe and Mail.
R Core Team, 2019. R: a language and environment for statistical computing [WWW
Document]. R Found. Stat. Comput (accessed 10.28.19). https://www.R-project.org/
.
Robinson, D., Hayes, A., 2020. Broom: Convert Statistical Analysis Objects into Tidy
Tibbles. R package version 0.5.5.
D.M. Stieb et al.
Statistics Canada, 2020. Table 13-10-0113-01 Health characteristics, two-year period
estimates [WWW Document] (accessed 4.26.20). https://www150.statcan.gc.
ca/t1/tbl1/en/tv.action?pid=1310011301.
Statistics Canada, 2016. Low Income Lines: What they are and how they are created.
Income Research Paper Series. Catalogue no. 75F0002M — No. 002.
Statistics Canada, 2018a. Health Regions: Boundaries and Correspondence with Census
Geography [WWW Document]. Health Reg. Peer Groups. https://www150.statcan.
gc.ca/n1/pub/82-402-x/2018001/hrpg-rsgh-eng.htm (accessed 5.13.20).
Statistics Canada, 2018b. Age, Sex, Type of Dwelling, Families, Households, Marital
Status, Language, Income, Immigration and Ethnocultural Diversity, Housing,
Aboriginal Peoples, Education, Labour, Journey to Work, Mobility and Migration,
and Language of Work for Canada, Provinces and Territories, and Health Regions,
2016 Census Catalogue number: 98-401-X2016058 [WWW Document]. https:
//www12.statcan.gc.ca/census-recensement/2016/dp-pd/prof/details/download-t
elecharger/comp/page_dl-tc.cfm?Lang=E (accessed 4.26.20).
Thurston, G.D., Kipen, H., Annesi-Maesano, I., Balmes, J., Brook, R.D., Cromar, K., De
Matteis, S., Forastiere, F., Forsberg, B., Frampton, M.W., 2017. A joint ERS/ATS
policy statement: what constitutes an adverse health effect of air pollution? An
analytical framework. Eur. Respir. J. 49, 1600419.
van Donkelaar, A., Martin, R.V., Li, C., Burnett, R.T., 2019. Regional estimates of
chemical composition of fine particulate matter using a combined geoscience-
Environmental Research 191 (2020) 110052
statistical method with information from satellites, models, and monitors. Environ.
Sci. Technol. 53, 2595–2611. https://doi.org/10.1021/acs.est.8b06392.
Wang, P.L., Feddema, J., Shooshtari, M., 2018. Water Balance Model for Canadian Urban
Environment (CANUE) and Health Research Consortium. Please Contact CANUE
(info@canue.Ca) for Additional Information.
Weeks, C., 2020. Ottawa to Intervene in Lagging Regions amid COVID-19 Test Backlog.
Globe and Mail.
Wei, T., Simko, V., 2017. R Package “Corrplot”: Visualization of a Correlation Matrix
(Version 0.84).
Wickham, H., 2016. ggplot2: Elegant Graphics for Data Analysis. Springer-Verlag, New
York.
Wu, X., Nethery, R.C., Sabath, B.M., Braun, D., Dominici, F., 2020. Exposure to air
pollution and COVID-19 mortality in the United States (preprint). medRxiv
2020.04.05.20054502. https://doi.org/10.1101/2020.04.05.20054502.
Yancy, C.W., 2020. COVID-19 and african Americans. J. Am. Med. Assoc. https://doi.
org/10.1001/jama.2020.6548.
Yang, L., Li, C., Tang, X., 2020. The impact of PM2.5 on the host defense of respiratory
system. Front. Cell Dev. Biol. 8, 91. https://doi.org/10.3389/fcell.2020.00091.
Zhu, Y., Xie, J., Huang, F., Cao, L., 2020. Association between short-term exposure to air
pollution and COVID-19 infection: evidence from China. Sci. Total Environ. 727,
138704. https://doi.org/10.1016/j.scitotenv.2020.138704.