Environmental Research 212 (2022) 113099

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

Exposure-lag response of air temperature on COVID-19 incidence in twelve

Italian cities: A meta-analysis☆,☆☆
Fang Chyi Fong a, Daniel Robert Smith b, *
a
Newcastle University Medicine Malaysia, No. 1, Jalan Sarjana 1, Kota Ilmu, EduCity@Iskandar, 79200, Iskandar Puteri, Johor, Malaysia
b
Clinical Epidemiology and Biostatistics, School of Medical Sciences, Örebro University, Örebro, Sweden

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

Keywords: The exposure-lag response of air temperature on daily COVID-19 incidence is unclear and there have been
Air temperature concerns regarding the robustness of previous studies. Here we present an analysis of high spatial and temporal
COVID-19 incidence resolution using the distributed lag non-linear modelling (DLNM) framework. Utilising nearly two years’ worth
Delayed effects
of data, we fit statistical models to twelve Italian cities to quantify the delayed effect of air temperature on daily
Italy
Time-series
COVID-19 incidence, accounting for several categories of potential confounders (meteorological, air quality and
Meta-analysis non-pharmaceutical interventions). Coefficients and covariance matrices for the temperature term were then
Distributed lag non-linear model synthesised using random effects meta-analysis to yield pooled estimates of the exposure-lag response with ef­
fects presented as the relative risk (RR) and cumulative RR (RRcum). The cumulative exposure response curve was
non-linear, with peak risk at 15.1 ◦ C and declining risk at progressively lower and higher temperatures. The
lowest RRcum at 0.2 ◦ C is 0.72 [0.56,0.91] times that of the highest risk. Due to this non-linearity, the shape of the
lag response curve necessarily varied by temperature. This work suggests that on a given day, air temperature
approximately 15 ◦ C maximises the incidence of COVID-19, with the effects distributed in the subsequent ten
days or more.

1. Introduction
As of October 2021, more than 240 million cases of COVID-19 in­
fections have been confirmed worldwide, and the global death toll has
now exceeded 4 million people (World Health Organization, 2021).
Aside from the direct impact of COVID-19, healthcare in other fields
unrelated to infectious disease have also suffered from its knock-on ef­
fects. Woolf et al. (2020) reported a higher number of deaths in the
United States than expected when comparing data to previous years and
estimated that 35% of the excess mortality is due to conditions not
directly attributed to COVID-19. Though difficulty in seeking medical
treatment due to movement restriction measures and reluctance to risk
exposure in healthcare settings are speculated reasons for the excess
mortality, an overwhelmed healthcare system likely played a significant
role, especially in the formative stages of the outbreak.
Italy was among the worst affected countries near the start of the
pandemic, with daily cases peaking at the end of March 2020. Italy
remained within the top ten countries with the highest cumulative
number of confirmed cases by June 2020, at more than 240,000 cases,
with a recorded case fatality rate exceeding 10% (Worldometer, 2020).
Over a year since the start of the pandemic, widespread lockdown was
reimposed due to transmission rates rising once more (Day, 2021).
Since the beginning of the outbreak, a number of studies have
investigated the relationship between air temperature and COVID-19
incidence, though the evidence is inconclusive (Dong et al., 2021).
Studies in Italy are no exception, with reports of both positive (Passerini
et al., 2020; Zoran et al., 2020) and negative (De Angelis et al., 2021;
Pirouz et al., 2020) associations. Several studies have also attempted to
allow for non-linear and delayed effects of meteorological predictors,
though until very recently (Nottmeyer and Sera, 2021) these have been
limited to select regions (Runkle et al., 2020), relatively narrow tem­
perature ranges (Bashir et al., 2020; Passerini et al., 2020; Tosepu et al.,
2020), relatively short time series (Shi et al., 2020) and lag periods
(Tobías and Molina, 2020), all of which may induce significant biases.
Indeed, a recent review of papers which have investigated the associa­
tion between air temperature and COVID-19 incidence identified critical

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.☆☆ This study used publicly available
☆

datasets and did not involve human subjects or experimental animals.

* Corresponding author.
E-mail addresses: fang-chyi.fong@newcastle.ac.uk (F.C. Fong), daniel.smith@regionorebrolan.se (D.R. Smith).

https://doi.org/10.1016/j.envres.2022.113099
Received 15 July 2021; Received in revised form 4 March 2022; Accepted 6 March 2022
Available online 16 March 2022
0013-9351/© 2022 The Authors. Published by Elsevier Inc. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).
F.C. Fong and D.R. Smith
methodological flaws in the majority of papers studied (Dong et al.,
2021). This is perhaps unsurprising given the urgency for published
works. In addition to the limitations mentioned above, concerns high­
lighted by Dong et al. (2021) included: low spatial resolution, failure to
assess and/or account for autocorrelation, and failure to account for
various categories of confounding variables (e.g., meteorological, air
quality, non-pharmaceutical interventions (NPI)), including their
potentially delayed effects.
Here we attempt to address these concerns by performing an analysis
of high spatial and temporal resolution using almost two years’ worth of
daily data. We fit statistical models to select Italian cities to quantify the
delayed effect of air temperature on daily COVID-19 incidence, ac­
counting for confounding variables. Coefficients and covariance
matrices for the temperature term are then synthesised using random
effects meta-analysis to yield pooled estimates of the exposure-lag
response.
2. Materials and methods
2.1. Data sources
Twelve Italian cities were included in this analysis, namely: Bologna,
Brescia, Firenze, Livorno, Milano, Modena, Napoli, Parma, Prato, Roma,
Torino and Trieste, selected based on the availability of daily city level
data, between 24 February 2020 and 30 December 2021 inclusive. Daily
confirmed COVID-19 cases for each city, with respective populations at
risk, were accessed using the COVID-19 R package (Guidotti and Ardia,
2020), an interface to the COVID-19 Data Hub (https://covid19datahub.
io/). For daily city-level data, confirmed cases and populations are
sourced from Ministero della Salute (Dati COVID-19 Italia, 2021) and
Istituto Nazionale di Statistica, Italia (Istituto Nazionale di Statistica,
2018) respectively. Country-level daily values of the stringency index
(SI) are sourced from the Oxford Coronavirus Government Response
Tracker (OxCGRT) project (Hale et al., 2021). This is a composite metric
assessing the number and strictness of government policies and is
comprised of nine response indicators including travel bans, workplace
closures and school closures (https://www.bsg.ox.ac.uk/research/resea
rch-projects/covid-19-government-response-tracker).
Daily median city-level weather and air quality data were obtained
from local meteorological stations (https://aqicn.org/data-platform
/covid19/ (Air Quality Open Data Platform, 2022)) and included: (1)
air temperature, (2) relative humidity, (3) air pressure, and (4) PM2.5.
Daily city level residential mobility data was obtained from
https://www.google.com/covid19/mobility/ (COVID-19 community
mobility reports, 2020). Finally, daily COVID-19 vaccination adminis­
tration counts at regional level were obtained from https://raw.gith
ubusercontent.com/italia/covid19-opendata-vaccini/master/dati/so
mministrazioni-vaccini-latest.csv with corresponding populations from
Istituto Nazionale di Statistica, Italia (Istituto Nazionale di Statistica,
2018).
2.2. Study design
We utilised the two-stage time series design (Berhane and Thomas,
2002). In the first stage, a series of city-specific statistical models were
fitted, with terms representing the exposure-lag response with respect to
air temperature, as well as additional confounding variables. In the
second stage, coefficients and covariance matrices from the first stage
models were pooled using meta-analysis. This approach controls for
city-level confounders, relaxes the strong assumption that the
exposure-lag response is not city-specific, and has been deployed in a
recent similar study (Nottmeyer and Sera, 2021).
2.3. First stage analysis
In order to model the temporal dependency between daily temper­
2
Environmental Research 212 (2022) 113099
ature and COVID-19 incidence, we adopted the Distributed Lag Non-
linear Model (DLNM) framework (Gasparrini et al., 2010). For each
city, we fitted a Generalized Additive Model (GAM) (Wood, 2011) of the
form:
Yt ∼ negative binomial (μt ),
∑
K
(1)
log(μt ) = β0 + log(P) + β1 Tt , l + β2 DOWt + fk (utk )
k=1
where Yt denotes the number of COVID-19 cases on day t and β0 the
model intercept. The logarithm of the population at risk (P) is fitted as a
model offset. Tt , l denotes a cross-basis term for air temperature on day t
considering lag l, constructed using natural splines with β1 the corre­
sponding vector of coefficients. For the exposure dimension, internal
knots were placed at the 27.5th and 72.5th percentiles, corresponding to
10.4 and 21.9 ◦ C respectively (informed by minimising the AIC over a
range of knot placement settings; see R code in the SI). For the lag basis,
we pre-specified 3 degrees of freedom, with knots placed at the 33.3rd
and 66.7th percentiles (Nottmeyer and Sera, 2021 found that larger
values for the degrees of freedom incurred a loss of precision for the
estimates). We considered lag range 0 through 10 days inclusive as in
recent studies (Lauer et al., 2020; Nottmeyer and Sera, 2021). DOW
denotes the day of week fitted as dummy variables, with β2 the corre­
sponding vector of coefficients. utk denotes additional predictors fitted
as penalised smoothing splines, with the degree of smoothing estimated
from the data. Time, t, was fitted as a highly flexible penalised natural
spline with 20 knots to allow for seasonal and long-term trends, as well
as sudden changes such as testing policy. We fitted cross-basis terms for
additional confounders using penalised natural splines with 3 degrees of
freedom for the exposure and lag dimensions and lag effects up to 10
days. This included: (1) log(daily cases + 1) in order to allow for auto­
correlation (Imai et al., 2015; Nottmeyer and Sera, 2021); residential
mobility, cumulative percentage of vaccines administered; stringency
index, relative humidity, air pressure and PM2.5 (time series plots of
these variables are provided in the SI). By fitting these as penalised
terms, corresponding parameter estimates can shrink to simple linear
effects to avoid over-parameterization (Benedetti and Abrahamowicz,
2004; Chen et al., 2016).
Heteroscedasticity and Autocorrelation Consistent (HAC) estimation
of the covariance matrix was performed using the sandwich estimator
(Zeileis, 2004, 2006). Parameters were estimated using restricted
maximum likelihood (REML). Simulated Quantile-Quantile (Figure SI9)
(Hartig, 2021) and partial autocorrelation (Figure SI10) plots are pro­
vided as supplementary information. We performed a sensitivity anal­
ysis by adjusting the parameterization of the cross-basis term for
temperature since this was the predominant term of interest. Accord­
ingly, we assessed the impact of changing the lag period to 5 and 15
days, as well as increasing the degrees of freedom for the lag basis to 4
and 5 respectively.
2.4. Second stage analysis
For each of the city-specific GAM’s, the cross-basis term for air
temperature, Tt , l , was reduced to simpler sets of one-dimensional co­
efficients and corresponding covariance matrices for the exposure- and
lag-dimensions respectively (Gasparrini and Armstrong, 2013). These
were then pooled using random effects meta-analysis with REML esti­
mation (Sera et al., 2019). We assessed for heterogeneity using the
multivariate Cochran’s Q test (using pre-specified α = 0.05) and the I2
statistic. The pooled exposure (i.e., air temperature) response summed
over the lag period was presented as the cumulative relative risk
(RRcum), centred on the temperature of the maximal RRcum. The pooled
lag response at select temperatures (i.e., “exposure specific”) was pre­
sented as the relative risk (RR) centred on the current day (i.e. lag day
0). We computed 95% confidence intervals for both RR and RRcum to
quantify uncertainty in these point estimates.
F.C. Fong and D.R. Smith Environmental Research 212 (2022) 113099

All statistical analyses were performed in R studio version 2021.09.0, Table 2

using R version 4.1.2 (R Core Team, 2013) and relying heavily on the Cochran’s multivariate Q test and I2 statistic to assess heterogeneity in the meta-
packages ‘dlnm’ (Gasparrini, 2011), ‘mgcv’ (Wood, 2011) and ‘mix­ analytic models.
meta’ (Sera et al., 2019). R code and datasets are included in the sup­ Meta-analytic model Q df P I2 (%)
plementary material to fully reproduce the analysis. Overall cumulative response 18.2 33 0.983 <.05
Lag response 1 ◦C 10.06 33 1.000 <.05
3. Results 10 ◦ C 8.36 33 1.000 <.05
20 ◦ C 9.09 33 1.000 <.05
30 ◦ C 18.42 33 0.981
Across all city-specific time series, daily median air temperature
<.05

ranged from − 2.2 to 33.6 ◦ C (Table 1). Model checking plots indicated
good fit of the first stage models to the observed data (Figures SI9, SI10).
Estimates of parameters from the meta-analytic models are provided in
SI Table 1. There appeared to be low heterogeneity in meta-analytic
models for the exposure and lag responses respectively with all P
values for the Multivariate Cochran’s Q test non-significant (P > 0.05)
and I2 < 0.05% (Table 2). This indicated there was very little variation in
effects between studies beyond sampling error.
The cumulative exposure response curve was non-linear with peak
risk at 15.1 ◦ C, and declining risk at lower and higher temperatures
(Fig. 1). Cumulative risk at 0.2 ◦ C is 0.72 [0.56,0.91] times that at
15.1 ◦ C. The decline in RRcum at temperature >15.1 ◦ C exhibited slightly
more uncertainty than the corresponding effect at temperatures
<15.1 ◦ C. The reductions in risk are statistically significant (P < 0.05) at
temperatures below approx. 7 ◦ C and above approx. 26 ◦ C.
The lag response curves were centred at lag = 0 days and tempera­
ture = 15.1 ◦ C (Fig. 2). The shape of the lag response necessarily varied
by temperature due to the non-linear cumulative exposure response
curve (Fig. 2). The magnitude of the effect becomes greater for
increasing or decreasing temperatures compared with the reference
temperature. Accordingly the lag response curves are relatively flat at
temperatures 10 and 20 ◦ C compared with 1 and 30 ◦ C (Fig. 2). At 1 ◦ C
(top left Fig. 2) the decline in RRcum is statistically significant (P < 0.05)
from day 0 to approx. lag 5.5 days with peak reduction at approx. 3 days
Fig. 1. Overall cumulative exposure-response association. Cumulative RR is
lag. In contrast, for 30 ◦ C the reduction in RRcum is delayed, with point computed by summing the log RR over the lag period (0 through 10 days in­
estimates <1 only occurring beyond a lag of 2 days, and is significant clusive) before exponentiating. The effects are centred at the reference level
between approx. 7 and 9.5 days lag. Aside from very high temperatures, (solid diamond = 15.1 ◦ C). Grey shaded area represents 95% confi­
the curves retract to the null at the end of the modelled lag (10 days). dence intervals.
Changing the lag period of the cross-basis term for temperature from
10 to either 5 or 15 days in the sensitivity analysis incurred a loss of 4. Discussion
precision. For lag 5 days, the decline in RRcum above the reference
temperature was less certain with confidence intervals that include the In this contribution, we quantified the exposure-lag response of air
null and becoming wider with increasing temperature (Figures SI11). temperature on daily COVID-19 incidence in Italy. We fitted city-specific
Upon increasing the lag to 15 days, the temperature of the maximum statistical models to extended time series accounting for numerous
RRcum reduced slightly to approx. 11 ◦ C (Figure SI12). Under this sce­ confounders, before pooling the temperature effects using meta-
nario point estimates hint of a possible upward trend at high tempera­ analysis, which was justified by low heterogeneity. We show that the
tures, though again confidence intervals are too wide to conclude with cumulative exposure response curve is non-linear with peak risk at
any degree of certainty. 15.1 ◦ C, and declining risk at progressively lower and higher
The shape and precision of the RRcum curve was relatively robust to temperatures.
increasing the degrees of freedom allocated to the lag basis from 3, to 4 The decline in RRcum at temperature >12.9 ◦ C was slightly shallower
and 5 respectively (Figures SI13, SI14).

Table 1
Summary statistics by city for the modelling period.
City Total number of confirmed COVID-19 cases Population at risk Mean temperature (◦ C) Minimum temperature (◦ C) Maximum temperature (◦ C)

Bologna 123,736 1,011,291 15.3 − 1 30.5

Brescia 139,145 1,262,402 15 − 1.6 30
Firenze 102,974 1,013,260 16.2 1 31.4
Livorno 27,461 336,215 15.8 1.2 28.1
Milano 397,922 3,234,658 15.2 − 0.4 30.4
Modena 84,624 701,896 14.7 − 2.2 29.7
Napoli 337,124 3,101,002 17.8 2.1 31
Parma 37,439 450,256 15.6 − 1.1 30.4
Prato 31,503 256,071 15.8 1.1 31
Roma 365,339 4,355,725 17.9 3.3 31.5
Torino 255,154 2,269,120 15.3 − 0.5 30.1
Trieste 37,576 234,638 16.3 − 0.5 33.6

*Mean, minimum and maximum temperature are computed using daily median temperatures over the time series’.

3
F.C. Fong and D.R. Smith
Fig. 2. Exposure-specific lag-response associations. The effects are centred at lag = 0 days and temperature = 15.1 ◦ C. Grey shaded area represents 95% confi­
dence intervals.
and exhibited more uncertainty than the corresponding effect at tem­
peratures <12.9 ◦ C. The air temperature yielding minimum RRcum was
0.2 ◦ C, i.e., the minimum temperature used in the pooled analysis.
Due to the non-linear cumulative exposure response curve, the shape
of the lag response curves necessarily vary by temperature. RR falls
below 1 within the lag period, which is consistent with delayed effects of
an increase or decrease in temperature (relative to reference) on a given
day. Whilst the lag response for low temperatures declines and then
returns to the null by day lag 10, this was not observed at high tem­
peratures where the effects seemed further delayed with RR < 1 at lag
day 10 (though the effect is not statistically significant). Moreover, our
sensitivity analysis suggests effects may be distributed beyond 10 days.
It is possible that, at the population level, temperature changes on a
given day may affect daily incidence up to and beyond 15 days hence,
and further work might consider investigating longer lag periods.
Nottmeyer and Sera (2021) performed a similar study on cities in
England. The shape of the non-linear exposure-response relationship
reported herein shows a similar trend to their study (though note the
4
Environmental Research 212 (2022) 113099
different centering temperature), suggesting progressively lower and
higher temperatures beyond that at the maximum RRcum, are associated
with reduced COVID-19 incidence. However, it appeared as though the
temperature at which peak risk occurred was approximately 3.2 ◦ C
higher in our study (15.1 ◦ C) compared to theirs (11.9 ◦ C). Moreover,
the largest absolute RRcum reported herein (1.39 [95% CI: 1.10; 1.79]) is
also slightly smaller than that of the above study, at 1.62 [95% CI: 1.44;
1.81]). The temperature for which risk is minimised was 0.2 ◦ C in the
current study compared with 21.8 ◦ C in their study (though confidence
intervals widened at higher temperatures in their study).
Experiments on SARS-CoV-2 have demonstrated a temperature-
dependent effect on the stability of virus particles on smooth surfaces
(Chin et al., 2020). Since SARS-CoV-2 is shown to be capable of sur­
viving in aerosols for at least 3 hours, airborne transmission is highly
plausible (Van Doremalen et al., 2020). Aerosol dynamics, and subse­
quently disease transmission, appear to be affected by air temperature
and humidity. Low humidity and low temperature result in smaller
infected droplet nuclei that can travel further, remain airborne for a
F.C. Fong and D.R. Smith
longer duration, and cause delayed virus inactivation (Chen, 2020;
Moriyama et al., 2020). Experimental evidence for the effects of climate
on transmission dynamics using influenza virus in a guinea pig model
lends credence to this hypothesis (Lowen et al., 2007). Low temperature
and high humidity favour contact transmission (Lowen et al., 2007;
Zhao et al., 2020), whilst high temperature and low humidity promote
the accumulation of aerosol particles, increasing the likelihood of
inhalation (Moriyama et al., 2020). As highlighted in the above refer­
ence, this ambiguity makes non-linear associations plausible. However,
not all experimental studies agree that stability of SARS-CoV-2 is greatly
affected by temperature (Kratzel et al., 2020). More recent evidence
showed that outdoor airborne transmission is unlikely in non-crowded
areas (Belosi et al., 2021; Chirizzi et al., 2021; Pivato et al., 2021).
Though outdoor air temperature likely has limited direct impact on
transmission via virus stability in non-crowded outdoor settings, host
factors, such as human behaviour influenced by meteorological vari­
ables, may underlie the observed trend. Several studies have suggested
an association of human mobility with warmer temperatures (Shao
et al., 2021; Xi et al., 2020). An exploratory study in Italy found that
mobility correlated with increased spread of COVID-19 (Carta et al.,
2021). Although we attempt to control for this confounder by including
city level residential mobility, omitted variable bias may have occurred
if other mobility indices are confounded with temperature. Further­
more, the stringency index we included is only available on a national
level, while restrictions enforced by the Italian government varied
across regions depending on the evolving situation of the pandemic. As
such, we acknowledge this as a major limitation of our analysis, and,
increased human mobility as influenced by temperature remains one
plausible explanation for our results.
Our study has several strengths which we believe make it a valuable
contribution to the literature, particularly in the light of criticisms raised
by Dong et al. (2021). First, we employ the DLNM framework to
simultaneously assess non-linear and delayed dependencies of air tem­
perature in the exposure and lag dimensions (Gasparrini et al., 2010).
Second, we used city-level daily data for COVID-19 incidence and
several confounders providing high spatial resolution. Third, we used
the powerful two-stage design; this allows for both the background risk
and the exposure-lag response functions to vary by city which would
otherwise incur ecologic bias. Forth, we account for many confounders,
including meteorological, air quality and NPI variables, and allow for
delayed dependencies in these effects. Fifth, analysing data from a single
country, Italy, which has coordinated nationwide COVID-19 in­
terventions, as compared to analysis using data from different countries,
allows for better control over confounding variables. This is especially
significant, because confounders, such as government interventions,
likely have a greater influence over an immunologically naïve popula­
tion more than meteorological factors (Baker et al., 2020). For the later
period of the study, we have also accounted for vaccination efforts by
including the cumulative percentage of vaccine doses administered in
each region. Sixth, we have accounted for and assessed autocorrelation
and model fit in each of the city level models. Finally, we controlled for
potential overfitting using shrinkage estimators for confounding vari­
ables. In sum, we have addressed the major concerns highlighted in a
recent review of the relationship between air temperature and
COVID-19 incidence (Dong et al., 2021).
Our work has several limitations. The first concerns the accuracy of
the estimated daily counts of COVID-19. In addition to varying rates of
testing, it is postulated that estimates are biased low due to undocu­
mented infections (Li et al., 2020) or other reporting errors (De Natale
et al., 2020). Secondly, our study is limited to the lag effects of median
daily temperature. It has been reported that extremes of daily temper­
ature might be a better predictor of COVID-19 incidence (Babin, 2020);
this would be a worthy avenue for future research. Third, our analysis
was based on a smaller number of cities (albeit longer time series and
more confounders considered) than similar work (Nottmeyer and Sera,
2021; Shi et al., 2020); this was a direct consequence of the availability
5
Environmental Research 212 (2022) 113099
of good quality city-level data for confounders which we considered a
key feature of our analysis. Although meta-analysing 12 cities in this
framework is valid (the example in Gasparini and Armstrong (Gasparrini
and Armstrong, 2013) used 10 regions), further work might consider a
larger sample size of cities, increasing statistical power and yielding
more precise effect estimates. Forth, although meteorological, air
quality and residential mobility data were city level, vaccine data was
regional, whilst SI data was country level policy; this may incur some
aggregation bias and presents a limitation for our analysis. Fifth, we also
had not considered the possible change in virus infectivity throughout
the course of the study period.
In conclusion, our results support recent works of a non-linear cu­
mulative exposure-response of air temperature on COVID-19 incidence.
Peak risk for daily incidence is 15.1 ◦ C, with the effects seen over the
subsequent 10 days or more due to the delayed response. It should be
stressed that risks presented herein are population level risks since the
statistical units analysed are population groups. This information is
particularly useful for policy makers assessing population level trends,
though might not necessarily correspond to individual level risk due to
the ecological fallacy.
Credits
Fang Chyi Fong: Conceptualization; Data curation; Investigation;
Methodology; Writing – original draft; Writing – review & editing.
Daniel Robert Smith: Conceptualization; Data curation; Formal analysis;
Investigation; Methodology; Software; Supervision; Validation; Visual­
ization; 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.
Appendix A. Supplementary data
Supplementary data to this article can be found online at https://doi.
org/10.1016/j.envres.2022.113099.
References
Air Quality Open Data Platform [Internet], 2021 [cited 31 Dec 2021]. World Air Quality
Index project. Available from: https://aqicn.org/data-platform/covid19/.
Babin, S., 2020. Use of weather variables in SARS-CoV-2 transmission studies. Int. J.
Infect. Dis. 100, 333–336.
Baker, R.E., Yang, W., Vecchi, G.A., Metcalf, C.J.E., Grenfell, B.T., 2020. Susceptible
supply limits the role of climate in the early SARS-CoV-2 pandemic. Science 369,
315–319.
Bashir, M.F., Ma, B., Bilal Komal, B., Bashir, M.A., Tan, D., Bashir, M., 2020. Correlation
between climate indicators and COVID-19 pandemic in New York, USA. Sci. Total
Environ. 728, 138835.
Belosi, F., Conte, M., Gianelle, V., Santachiara, G., Contini, D., 2021. On the
concentration of SARS-CoV-2 in outdoor air and the interaction with pre-existing
atmospheric particles. Environ. Res. 193, 110603.
Benedetti, A., Abrahamowicz, M., 2004. Using generalized additive models to reduce
residual confounding. Stat. Med. 23, 3781–3801.
Berhane, K., Thomas, D.C., 2002. A two-stage model for multiple time series data of
counts. Biostatistics 3, 21–32.
Carta, M.G., Minerba, L., Demontis, R., Orrù, G., Romano, F., Scano, A., Restivo, A., Del
Giacco, S., Deidda, S., Firnu, D., Campagna, M., Meloni, F., Cossu, G., Sancassiani, F.,
Chessa, L., Kalcev, G., Littera, R., Zorcolo, L., Aviles-Gonzale, C.I., Usai, P., 2021. The
COVID-19 incidence in Italian regions correlates with low temperature, mobility and
PM10 pollution but lethality only with low temperature. J. Publ. Health Res.
Chen, L.D., 2020. Effects of ambient temperature and humidity on droplet lifetime - a
perspective of exhalation sneeze droplets with COVID-19 virus transmission. Int. J.
Hyg Environ. Health 229, 113568.
Chen, Q., Nian, H., Zhu, Y., Talbot, H.K., Griffin, M.R., Harrell Jr., F.E., 2016. Too many
covariates and too few cases? - a comparative study. Stat. Med. 35, 4546–4558.
Chin, A.W.H., Chu, J.T.S., Perera, M.R.A., Hui, K.P.Y., Yen, H.L., Chan, M.C.W.,
Peiris, M., Poon, L.L.M., 2020. Stability of SARS-CoV-2 in different environmental
conditions. Lancet Microb. 1, e10.
F.C. Fong and D.R. Smith
Chirizzi, D., Conte, M., Feltracco, M., Dinoi, A., Gregoris, E., Barbaro, E., La Bella, G.,
Ciccarese, G., La Salandra, G., Gambaro, A., Contini, D., 2021. SARS-CoV-2
concentrations and virus-laden aerosol size distributions in outdoor air in north and
south of Italy. Environ. Int. 146, 106255.
Google LLC, 2020. Google COVID-19 Community Mobility Reports. https://www.google.co
m/covid19/mobility/. (Accessed 30 December 2021).
Dati COVID-19 Italia, 2021 [30 Dec 2021]. Dipartimento della Protezione Civile.
Available from: https://github.com/pcm-dpc/COVID-19.
Day, M., 2021. Covid-19: Italy reimposes widespread lockdown as transmission rate rises
again. Bmj 372, n726.
De Angelis, E., Renzetti, S., Volta, M., Donato, F., Calza, S., Placidi, D., Lucchini, R.G.,
Rota, M., 2021. COVID-19 incidence and mortality in Lombardy, Italy: an ecological
study on the role of air pollution, meteorological factors, demographic and
socioeconomic variables. Environ. Res. 195, 110777.
De Natale, G., Ricciardi, V., De Luca, G., De Natale, D., Di Meglio, G., Ferragamo, A.,
Marchitelli, V., Piccolo, A., Scala, A., Somma, R., Spina, E., Troise, C., 2020. The
COVID-19 infection in Italy: a statistical study of an abnormally severe disease.
J. Clin. Med. 9.
Dong, Z., Fan, X., Wang, J., Mao, Y., Luo, Y., Tang, S., 2021. Data-related and
methodological obstacles to determining associations between temperature and
COVID-19 transmission. Environ. Res. Lett. 16, 034016.
Gasparrini, A., 2011. Distributed lag linear and non-linear models in R: the package
dlnm. J. Stat. Software 43, 1–20.
Gasparrini, A., Armstrong, B., 2013. Reducing and meta-analysing estimates from
distributed lag non-linear models. BMC Med. Res. Methodol. 13, 1.
Gasparrini, A., Armstrong, B., Kenward, M.G., 2010. Distributed lag non-linear models.
Stat. Med. 29, 2224–2234.
Guidotti, E., Ardia, D., 2020. COVID-19 data Hub. J. Open Sour. Software 5, 2376.
Hale, T., Angrist, N., Goldszmidt, R., Kira, B., Petherick, A., Phillips, T., Webster, S.,
Cameron-Blake, E., Hallas, L., Majumdar, S., Tatlow, H., 2021. A global panel
database of pandemic policies (Oxford COVID-19 Government Response Tracker).
Nat. Hum. Behav. 5, 529–538.
Hartig, F., 2021. DHARMa: Residual Diagnostics for Hierarchical (Multi-Level/Mixed)
Regression Models. R package version 0.4.4.
Imai, C., Armstrong, B., Chalabi, Z., Mangtani, P., Hashizume, M., 2015. Time series
regression model for infectious disease and weather. Environ Res. 142, 319–327.
Istituto Nazionale Di Statistica, I., 2018. Population and Household: Data and Microdata
[Online]. Available, 2021. https://www.istat.it/en/population-and-households?data
-and-indicators.
Kratzel, A., Steiner, S., Todt, D., V’kovski, P., Brueggemann, Y., Steinmann, J.,
Steinmann, E., Thiel, V., Pfaender, S., 2020. Temperature-dependent surface stability
of SARS-CoV-2. J. Infect. 81, 452–482.
Lauer, S.A., Grantz, K.H., Bi, Q., Jones, F.K., Zheng, Q., Meredith, H.R., Azman, A.S.,
Reich, N.G., Lessler, J., 2020. The incubation period of coronavirus disease 2019
(COVID-19) from publicly reported confirmed cases: estimation and application.
Ann. Intern. Med. 172, 577–582.
Li, R., Pei, S., Chen, B., Song, Y., Zhang, T., Yang, W., Shaman, J., 2020. Substantial
undocumented infection facilitates the rapid dissemination of novel coronavirus
(SARS-CoV-2). Science 368, 489–493.
Lowen, A.C., Mubareka, S., Steel, J., Palese, P., 2007. Influenza virus transmission is
dependent on relative humidity and temperature. PLoS Pathog. 3, 1470–1476.
Moriyama, M., Hugentobler, W.J., Iwasaki, A., 2020. Seasonality of respiratory viral
infections. Annu. Rev. Virol. 7, 83–101.
Nottmeyer, L.N., Sera, F., 2021. Influence of temperature, and of relative and absolute
humidity on COVID-19 incidence in England - a multi-city time-series study.
Environ. Res. 196, 110977.
Environmental Research 212 (2022) 113099
Passerini, G., Mancinelli, E., Morichetti, M., Virgili, S., Rizza, U., 2020. A preliminary
investigation on the statistical correlations between SARS-CoV-2 spread and local
meteorology. Int. J. Environ. Res. Publ. Health 17.
Pirouz, B., Shaffiee Haghshenas, S., Pirouz, B., Shaffiee Haghshenas, S., Piro, P., 2020.
Development of an assessment method for investigating the impact of climate and
urban parameters in confirmed cases of COVID-19: a new challenge in sustainable
development. Int. J. Environ. Res. Publ. Health 17.
Pivato, A., Amoruso, I., Formenton, G., Di Maria, F., Bonato, T., Vanin, S., Marion, A.,
Baldovin, T., 2021. Evaluating the presence of SARS-CoV-2 RNA in the particulate
matters during the peak of COVID-19 in Padua, northern Italy. Sci. Total Environ.
784, 147129.
Runkle, J.D., Sugg, M.M., Leeper, R.D., Rao, Y., Matthews, J.L., Rennie, J.J., 2020. Short-
term effects of specific humidity and temperature on COVID-19 morbidity in select
US cities. Sci. Total Environ. 740, 140093.
Sera, F., Armstrong, B., Blangiardo, M., Gasparrini, A., 2019. An extended mixed-effects
framework for meta-analysis. Stat. Med. 38, 5429–5444.
Shao, W., Xie, J., Zhu, Y., 2021. Mediation by human mobility of the association between
temperature and COVID-19 transmission rate. Environ. Res. 194, 110608.
Shi, P., Dong, Y., Yan, H., Zhao, C., Li, X., Liu, W., He, M., Tang, S., Xi, S., 2020. Impact of
temperature on the dynamics of the COVID-19 outbreak in China. Sci. Total Environ.
728, 138890.
Tobías, A., Molina, T., 2020. Is temperature reducing the transmission of COVID-19.
Environ. Res. 186, 109553.
Tosepu, R., Gunawan, J., Effendy, D.S., Ahmad, O.A.I., Lestari, H., Bahar, H., Asfian, P.,
2020. Correlation between weather and covid-19 pandemic in Jakarta, Indonesia.
Sci. Total Environ. 725, 138436.
Van Doremalen, N., Bushmaker, T., Morris, D.H., Holbrook, M.G., Gamble, A.,
Williamson, B.N., Tamin, A., Harcourt, J.L., Thornburg, N.J., Gerber, S.I., Lloyd-
Smith, J.O., De Wit, E., Munster, V.J., 2020. Aerosol and surface stability of SARS-
CoV-2 as compared with SARS-CoV-1. N. Engl. J. Med. 382, 1564–1567.
Wood, S.N., 2011. Fast stable restricted maximum likelihood and marginal likelihood
estimation of semiparametric generalized linear models. J. Roy. Stat. Soc. B 73,
3–36.
Woolf, S.H., Chapman, D.A., Sabo, R.T., Weinberger, D.M., Hill, L., 2020. Excess deaths
from COVID-19 and other causes, march-april 2020. JAMA 324, 510–513.
World Health Organization, 2021. WHO Coronavirus (COVID-19) Dashboard [Online].
Available: https://covid19.who.int/. (Accessed 20 October 2021).
Worldometer, 2020. Italy Coronavirus [Online]. Available. https://www.worldometers.
info/coronavirus/country/italy/. (Accessed 4 July 2020).
Xi, T., Wang, Q., Qin, H., Jin, H., 2020. Influence of outdoor thermal environment on
clothing and activity of tourists and local people in a severely cold climate city.
Build. Environ. 173, 106757.
Zeileis, A., 2004. Econometric computing with HC and HAC covariance matrix
estimators. J. Stat. Software 1 (Issue 10), 2004.
Zeileis, A., 2006. Object-oriented Computation of Sandwich Estimators, vol. 16, p. 16,
2006.
Zhao, L., Qi, Y., Luzzatto-Fegiz, P., Cui, Y., Zhu, Y., 2020. COVID-19: effects of
environmental conditions on the propagation of respiratory droplets. Nano Lett. 20,
7744–7750.
Zoran, M.A., Savastru, R.S., Savastru, D.M., Tautan, M.N., 2020. Assessing the
relationship between surface levels of PM2.5 and PM10 particulate matter impact on
COVID-19 in Milan, Italy. Sci. Total Environ. 738, 139825.
Further reading
Hartig, F., 2020. DHARMa: Residual Diagnostics for Hierarchical (Multi-level/mixed)
Regression Models.