You are on page 1of 10

Ordanovich 

et al. Environmental Health (2023) 22:5 Environmental Health


https://doi.org/10.1186/s12940-022-00957-6

RESEARCH Open Access

Temporal variation
of the temperature‑mortality association
in Spain: a nationwide analysis
Dariya Ordanovich1*†, Aurelio Tobías2† and Diego Ramiro1† 

Abstract 
Background  Although adaptation to continuously rising ambient temperatures is an emerging topic and has been
widely studied at a global scale, detailed analysis of the joint indicators for long-term adaptation in Spain are scarce.
This study aims to explore temporal variations of the minimum mortality temperature and mortality burden from heat
and cold between 1979 and 2018.
Methods  We collected individual all-cause mortality and climate reanalysis data for 4 decades at a daily time step.
To estimate the temperature-mortality association for each decade, we fitted a quasi-Poisson time-series regression
model using a distributed lag non-linear model with 21 days of lag, controlling for trends and day of the week. We
also calculated attributable mortality fractions by age and sex for heat and cold, defined as temperatures above and
below the optimum temperature, which corresponds to the minimum mortality in each period.
Results  We analysed over 14 million deaths registered in Spain between 1979 and 2018. The optimum tempera-
ture estimated at a nationwide scale declined from 21 °C in 1979–1988 to 16 °C in 1999–2008, and raised to 18 °C in
2009–2018. The mortality burden from moderate cold showed a 3-fold reduction down to 2.4% in 2009–2018. Since
1988–1999, the mortality risk attributable to moderate (extreme) heat reduced from 0.9% (0.8%) to 0.6% (0.5%). The
mortality risk due to heat in women was almost 2 times larger than in men, and did not decrease over time.
Conclusion  Despite the progressively warmer temperatures in Spain, we observed a persistent flattening of the
exposure-response curves, which marked an expansion of the uncertainty range of the optimal temperatures.
Adaptation has been produced to some extent in a non-uniform manner with a substantial decrease in cold-related
mortality, while for heat it became more apparent in the most recent decade only.
Keywords  Adaptation, Temperature, Climate change, Time-series regression, Distributed lag non-linear models

Introduction
The health effects of exposure to non-optimal ambi-
ent temperatures have been extensively studied [1–3].
The interest in this topic has been expressed not only by
scientific community but also by health care profession-
*Correspondence:
Dariya Ordanovich als and policymakers. The alarming rates of the global
dariya.ordanovich@cchs.csic.es warming raise a substantial concern for adverse health
1
Institute of Economy, Geography y Demography (IEGD), Spanish outcomes to aggravate in response to the amplified expo-
National Research Council (CSIC), Madrid, Spain
2
Institute of Environmental Assessment and Water Research (IDAEA), sure to continuously changing and increasingly extreme
Spanish National Research Council (CSIC), Barcelona, Spain temperatures [4]. The southern Mediterranean region is
becoming a major hotspot due to the persistent warming

© The Author(s) 2023. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which
permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the
original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or
other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line
to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory
regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this
licence, visit http://​creat​iveco​mmons.​org/​licen​ses/​by/4.​0/. The Creative Commons Public Domain Dedication waiver (http://​creat​iveco​
mmons.​org/​publi​cdoma​in/​zero/1.​0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
Ordanovich et al. Environmental Health (2023) 22:5 Page 2 of 10

of the air temperatures [5]. In particular, Spain is now Methods


one of the countries most impacted by increasing tem- Mortality data
peratures and heat waves. The progressive increase in the We collected nationwide daily counts of all-cause mortal-
average annual and seasonal values of air temperatures ity. Data were provided as microdata files, including sex
in Spain is presented in all the projections used for the and age, from Vital Statistics by the Spain National Insti-
period 2081–2100 [4]. For maximum temperatures, the tute of Statistics (INE) for the study period between Janu-
rise in the annual scale is predicted to be between 2.0 and ary 1, 1979 and December 31, 2018.
3.4 °C under the RCP4.5 scenario, while for the minimum
temperatures the expected increment ranges from 1.7 to Temperature data
2.9 °C under the same intermediate pathway [6]. As the main source for ambient air temperature expo-
Adaptation can happen naturally through physiological sure, we gathered the European Centre for Medium-
or behavioral adjustment. It can also be planned through Range Weather Forecasts (ECMWF) reanalysis data,
public health initiatives like heat health warning systems, which comprises a combination of observations with past
or socioeconomic development, such as improvement short-range weather forecasts rerun with weather predic-
of living conditions [7]. Several methods have been sug- tion models. In particular, global atmospheric reanalysis
gested to quantify adaptation. The temperature-mortality ERA-Interim data set was retrieved from 1979 onward at
association has been described as a J- or U-shaped curve, a 0.125°×0.125°resolution [20, 21]. ERA-Interim uses a
with the minimum being the temperature at which the fixed version of a numerical weather prediction system to
mortality risk is the lowest [1, 2]. Therefore, absolute produce highly accurate reanalyzed data [22]. The results
or relative shifts of the minimum mortality tempera- of the multivariate atmospheric reanalysis contained in
ture (MMT) as a threshold from the epidemiological the ERA-Interim data set have passed through quality
exposure-response function is an important indicator of control and multiple bias correction compared to the
how quickly populations can adapt to climate change in preceding reanalysis data sets as noted by [20]. Moreo-
the long term [7, 8]. Similar to this, adaptation has also ver, it has been shown that ERA-5 reanalysis data allow
been measured by absolute or relative reductions in the estimating the health effects of temperature in Spain,
risk of mortality due to non-optimal temperatures [7, 9]. even in areas far or free from weather stations. Royé
However, despite the fact that adaptation might raise the et al. [23] found a similar shape of the overall cumulative
MMT to compensate for part of the mortality brought on exposure-response curves using weather station temper-
by rising temperatures, an examination of adaptation pat- ature and ERA-5 reanalysis data across the full range of
terns should take into account whether the MMT as well temperatures.
as the temperature effect have changed over time, or if To calculate the daily (24  h) average temperature,
only one has [7, 10]. we passed the data from the original spatial grid to the
Several studies have reported that MMTs could con- core study grid of 10  km×10  km, created according to
tinue to rise with increasing temperatures locally [11] the Infrastructure for Spatial Information in Europe
and nationwide [8, 12, 13], suggesting partial adaptation (INSPIRE) technical guidelines on geographical grids.
to increasing temperatures. On the other hand, there has The centroid of the core grid was assigned the hourly
been a documented decline in the risk of heat-related values from the closest spatial neighbor from the ERA-
mortality despite the observed rise in temperatures and Interim grid with an average distance between points
the increasing frequency, severity, and length of extreme estimated at 4.7 km.
heat events [14–16]. Others have also demonstrated that
the risk of cold-related mortality has recently decreased Statistical analysis
[17]. However, a thorough examination of the temporal To evaluate changes in the MMT and the mortality bur-
evolution of joint indicators for long-term adaptation, den from heat and cold, we split the study period into
such as MMT and the attributable risk related to hot and equal 10-year intervals (i.e., 1979–1988, 1989–1998,
cold temperatures, especially among susceptible groups 1999–2008, and 2009–2018). For each period, we fitted
by age and gender, is seen in the literature on a rare occa- a quasi-Poisson time-series regression model [24] using
sion [18, 19] . a distributed lag non-linear model to estimate the tem-
We aim to explore the long-term adaptation to non- perature-mortality association [25]. In particular, we con-
optimal temperatures in Spain at the national level by trolled for seasonal and long-term trends using a natural
estimating the temporal variations of the MMT and the cubic spline of time with 10 degrees of freedom per year
mortality burden from heat and cold across a 40-year and indicator variables for the day of the week. We used
period, from 1979 to 2018. a natural cubic spline with three internal knots placed at
the 10th, 75th, and 90th percentiles of the temperature
Ordanovich et al. Environmental Health (2023) 22:5 Page 3 of 10

distribution and the lag-response, up to 21 days, with In terms of the demographic strata, the change in the
a natural cubic spline with 3 internal knots placed at temperature-mortality shape was also observed by sex
equally spaced values in the log scale (Additional file 1). and age (Fig. 2). However, women had remarkably lower
The overall effects further reported in this study are com- MMT than men, with a maintained gap of approximately
puted by summing the lag-specific contributions [25]. 3.5  °C from 1989 to 1999 and a declining trend until
The entire analysis was performed in R 4.2.0, and for the the last decade (Table  2). As for the age group, the eld-
statistical modelling was used the dlnm-package [26]. est individuals (85+) had the lowest MMTs, and a more
These modelling choices are based on extensive previ- pronounced declining trend than those aged 65–85,
ous work using an overlapping data set and have been who showed a considerable MMT increase of 5  °C in
thoroughly tested by sensitivity analyses [27, 28]. We 2009–2018.
identified the MMT from each estimated curve repre- The mortality burden from moderate cold shows an
senting the overall cumulative exposure-response (the almost 3-fold reduction, from 6.1% in 1979–1988 to 2.4%
net effect across lags), together with an approximate par- in 2009–2018. Similarly, mortality burden from extreme
ametric bootstrap estimator of its confidence interval and cold reduced from 1.1 to 0.7% (Table  3). The mortality
standard error [27]. We also calculated the MMT percen- risk attributable to heat shows a smaller reduction than
tile (MMTP), defined as the percentile of the tempera- cold, but from 1988 to 1999 onward. Moderate heat is
ture distribution corresponding to the MMT. Finally, we reduced from 0.9 to 0.6%, while extreme heat from 0.8 to
estimated the attributable fractions of mortality [29] due 0.5%. The attributable fraction associated with moderate
to moderate cold and heat, defined at the 5th and 95th cold decreased more substantially in women (from 5.5%
percentiles (P5 and P95) of the temperature distribution, in 1979–1988 to 1.4% in 2009–2018) than in men (6.6–
compared to the MMT of each period. We also estimated 3.8%). The impact of extreme cold was similar for both
the attributable fractions due to extreme temperatures by sexes until 2009–2018 when it decreased more in women
comparing the 1st and 99th percentiles (P1 and P99) ver- (0.6%) than in men (0.8%). Oppositely, the mortality risk
sus the P5 and P95, respectively. attributable to moderate and extreme heat was almost 2
times larger in women and did not decrease over time
Results (Table 3). By age group, the impact of moderate cold was
We analysed 14 203 959 deaths registered in Spain reduced mainly in the elderly (7.9–1.6%) and in those
between 1979 and 2018. Table  1 shows a substantial aged 65–85 (6.5–3.6%). A similar pattern was found for
increase in the temperature by decade: mean tempera- extreme cold. Attributable fractions associated with
tures increased by 1.2 °C while the variability intensified moderate and extreme heat exposure were higher in the
by 0.3  °C. The extreme temperatures for cold (P1) and eldest individuals than in other age groups throughout
heat (P99) also increased by 0.6 and 1.4  °C, respectively the entire study period.
(Additional file 2).
The temperature-mortality association shifted from a Discussion
V-shape in 1979–1988 to a U-shape in 2009–2018, reveal- This study examined the temporal variation in the ambi-
ing a progressive flattening of the exposure-response ent temperature-mortality association across a 40-year
curve (Fig.  1). The MMT exhibited a non-uniform pat- period in Spain. We found a flattening of the exposure-
tern (Fig. 2). The maximum MMT was registered in the response curve with a considerable decrease in the
1979–1988 decade (21.0 °C), declined in 1989–1999 and cold-related mortality compared to the heat. Women
1999–2008 (18.1 °C and 16.0 °C, respectively), and raised experienced the most marked reduction in the cold-
in 2009–2018 (17.9 °C) (Table 2). related mortality, being generally less affected than
men. Oppositely, men were less impacted by the heat.

Table 1  Descriptive statistics for mortality counts and temperature (°C) in Spain between 1979 and 2018
Cold Heat
Total deaths Temperature mean (sd) P1 P5 P95 P99

1979–1988 3 014 169 14.1 (5.8) 3.7 6.2 23.8 25.0


1989–1998 3 412 755 14.4 (5.7) 4.8 6.7 24.6 25.9
1999–2008 3 747 522 15.0 (6.0) 4.3 6.3 24.6 26.0
2009–2018 4 029 513 15.3 (6.1) 4.3 6.6 25.1 26.4
Ordanovich et al. Environmental Health (2023) 22:5 Page 4 of 10

Fig. 1  Overall temperature-mortality associations in Spain by decade between 1979 and 2018

The elderly also experienced the largest reduction in Vicedo-Cabrera et  al. [30], as part of a multi-country
the both cold- and heat-related mortality. The MMT assessment on potential adaptive mechanisms to cold
decreased until the most recent decade, 2009–2018, and heat, reported a decrease in the cold-related mortal-
when it increased by almost 2  °C. We observed a simi- ity for Spain and a less noticeable decrease in the heat-
lar pattern by sex, although women had much lower related mortality. Martínez-Solanas et  al. [31] compared
MMTs. The elderly also had generally lower MMTs with the temporal changes between two decades before and
a pronounced declining trend over time, while those aged after the activation of the Spanish Heat Health Preven-
65–85 showed a considerable increase of 5 °C in the last tion Plan [32], reporting greater reductions in the cold-
decade. and heat-related mortality in the elderly. Achebak et  al.
Overall, our results agree with previous studies show- [18] focused on the cause-specific mortality and showed
ing that most of the mortality burden was caused by days that the attributable fraction of cardiovascular deaths due
colder than the MMT compared to warmer days. The to the warm temperatures was higher for women, while
contribution of extreme days was comparatively lower for cold temperatures was higher in men. Vicedo-Cabrera
than moderately hot and cold temperatures [2]. How- et  al. [30] reported a consistent decrease in heat-related
ever, others have also examined temporal changes in mortality over the past decades in most of the ten coun-
the temperature-mortality association. We also found tries evaluated, but the reduction in the cold mortality
similar results to those previously reported in Spain. was only found in half of them.
Ordanovich et al. Environmental Health (2023) 22:5 Page 5 of 10

Fig. 2  Temporal evolution in the MMT and MMTP in Spain by decade between 1979 and 2018

Despite reporting similar results, the previous studies included data from the capitals of the provinces. Despite
used a two-stage design combining city-specific estimates the geographic heterogeneity, we primarily focused on
to derive a national assessment [33]. These studies mainly the national level, therefore our analysis included all daily
Ordanovich et al. Environmental Health (2023) 22:5 Page 6 of 10

Table 2  MMT,°C and MMTP,% in Spain by decade between 1979 and 2018
1979–1988 1989–1998 1999–2008 2009–2018

MMT
 Total 21.0 (19.3–21.5) 18.1 (16.8–20.5) 16.0 (14.4–18.0) 17.9 (15.5–22.0)
 Sex
  Male 21.4 (19.4–21.9) 20.5 (17.6–21.7) 18.0 (15.6–22.1) 19.7 (17.4–22.4)
  Female 20.7 (17.8–21.4) 17.1 (15.8–18.5) 14.5 (13.0-16.4) 15.1 (12.8–21.9)
 Age
  Under 65 21.9 (16.5–22.7) 17.7 (15.0-20.7) 22.5 (14.0-23.3) 19.8 (18.0-22.4)
  65–85 21.0 (19.0-21.6) 19.1 (17.6–20.9) 16.4 (14.5–19.4) 22.2 (16.2–22.9)
  Over 85 19.3 (17.1–21.2) 15.8 (14.0–21.0) 15.0 (13.2–16.9) 15.0 (12.9–17.8)
MMTP
 Total 78.9 (70.9–82.0) 66.8 (60.7–76.6) 54.8 (48.1–63.1) 61.1 (50.7–78.3)
 Sex
  Male 81.5 (71.2–84.7) 76.6 (64.3–81.3) 63.1 (52.8–81.1) 68.6 (58.9–80.3)
  Female 76.9 (65.3–81.5) 61.9 (56.4–68.5) 48.5 (42.0-56.4) 49.3 (39.1–77.8)
 Age
  Under 65 84.7 (60.9–89.3) 64.6 (52.9–77.5) 83.3 (46.6–88.1) 69.0 (61.6–80.3)
  65–85 78.9 (69.4–82.6) 71.4 (64.3–78.2) 56.4 (48.5–68.2) 79.3 (53.7–83.3)
  Over 85 70.9 (63.0-79.9) 56.4 (47.7–78.6) 50.3 (43.2–58.5) 48.9 (39.6–60.6)

deaths nationwide, regardless of the size of the city (i.e. year) [17] and the Netherlands (0.15  °C/year), although
including the areas with less than 10 000 inhabitants). these countries showed a sustained increase in the MMT
We also accurately calculated a national average daily in 1972–2012 and 1995–2017, respectively. In France the
temperature using the ERA-interim data set, which pro- MMT increased by 0.027 °C/year for adults over 65 years
vided a similar exposure to the Spain National Meteorol- in 1968–2009 [13] while in our study this parameter was
ogy Agency calculated using 42 reference stations [34]. A estimated at 0.037 °C/year for the population aged 65–85
recent study on the long-term adaptation to heat stress in in 1979–2018. Although the MMT decreased since 1979
the Netherlands also used the same nationwide approach and increased in the last decade, the shape of the tem-
as the one implemented in our study [12]. Nevertheless, perature-morality association changed substantially from
we conducted a sensitivity analysis comparing the expo- a V-shape in the first decade to a U-shape in the last dec-
sure-response curves for the temperature mortality asso- ade. The continuous flattening of the exposure-response
ciation from our nationwide analysis and the city-specific curve across the decades implies a more extensive range
estimates from the 52 provincial capital cities (Additional of optimal temperatures for both cold and heat, taking
file 3) using a two-stage approach (Additional file 4). into account the MMTs’ confidence intervals. Therefore,
The MMT has also been used as a threshold for climate we could consider that adaptation to non-optimal tem-
adaptation. If populations become less susceptible to peratures in Spain has been produced progressively since
heat, an increase in the MMT can be expected over time 1989 for cold and since 2009 for heat. It is, however, of
[11, 13, 35], similar to higher MMT values in warmer cit- great importance to highlight the fact that the analysis
ies due to geographic differences [27]. If the MMTP is based on all-cause mortality data might conceal some
fixed at a certain percentile of temperature distribution patterns otherwise discernible when working with spe-
and all other factors are held constant, warmer climates cific causes of death. Thus, the MMTs estimated for the
would tend to increase the MMT. Similarly, if the MMT same period of time in Spain using cardiovascular and
is fixed, higher temperatures would shift the MMTP to respiratory mortality data exhibited a multidirectional
a lower percentile of the temperature distribution. Sev- trend over time [18, 19, 36]. In case of the cardiovascu-
eral studies have reported that MMT could continue ris- lar diseases, the optimum temperatures were monotoni-
ing with increasing temperatures at the local level and cally increasing with time, which attributed to the fact
nationwide, suggesting partial adaptation to warmer tem- that for this group of diseases the risks for both hot and
peratures. The observed increase of the MMT by 1.9 °C cold temperatures were persistently reducing while the
in the last decade (0.1 °C/year) seen in our study is similar rate of reduction for hotter temperatures was higher. On
to the estimates previously reported for Japan (0.12  °C/ the contrary, the MMTs for respiratory diseases were
Ordanovich et al. Environmental Health (2023) 22:5 Page 7 of 10

Table 3  Mortality attributable fractions (%) due to heat and cold in Spain between 1979 and 2018
Total Sex Age
Female Male Under 65 65–85 Over 85

1979–1988
 P1vs. P5 1.12 1.12 1.11 0.52 1.20 1.78
(0.93–1.31) (0.90–1.36) (0.86–1.36) (0.19–0.82) (0.99–1.43) (1.43–2.11)
 P5vs. MMT 6.06 5.51 6.62 4.03 6.54 7.85
(3.92–7.96) (3.10–7.82) (4.03–9.04) (0.07–7.37) (4.10–8.87) (4.81–10.54)
  MMT vs. P95 0.34 0.52 0.20 0.08 0.37 0.79
(0.23–0.46) (0.32–0.70) (0.11–0.31) (-0.01-0.17) (0.23–0.50) (0.22–1.33)
 P95vs. P99 0.49 0.67 0.32 0.17 0.52 0.88
(0.41–0.56) (0.57–0.78) (0.23–0.42) (0.04–0.29) (0.43–0.62) (0.69–1.06)
1989–1998
 P1vs. P5 0.97 1.07 0.90 0.51 1.07 1.20
(0.86–1.09) (0.93–1.22) (0.73–1.05) (0.30–0.72) (0.92–1.21) (1.02–1.38)
 P5vs. MMT 3.87 3.98 4.12 2.59 4.98 3.24
(2.84–4.87) (2.73–5.15) (2.20–5.92) (0.70–4.41) (3.51–6.37) (1.94–4.59)
  MMT vs. P95 0.89 1.56 0.40 0.92 0.71 1.42
(0.52–1.26) (0.97–2.15) (0.17–0.63) (0.07–1.77) (0.33–1.08) (0.52–2.26)
 P95vs. P99 0.75 1.10 0.45 0.50 0.63 1.20
(0.62–0.87) (0.91–1.26) (0.32–0.58) (0.24–0.76) (0.48–0.78) (0.98–1.42)
1999–2008
 P1vs. P5 0.76 0.76 0.79 0.64 0.80 0.88
(0.65–0.88) (0.62–0.90) (0.63–0.95) (0.32–1.01) (0.64–0.95) (0.71–1.06)
 P5vs. MMT 2.21 1.78 2.92 3.97 2.47 2.24
(1.41–2.94) (0.94–2.54) (1.64–4.22) (-0.64-8.10) (1.36–3.52) (1.16–3.29)
  MMT vs. P95 1.10 1.94 0.53 0.12 1.03 2.22
(0.39–1.77) (0.97–3.02) (-0.12-1.16) (-0.01-0.25) (0.15–1.82) (1.05–3.31)
 P95vs. P99 0.59 0.89 0.34 0.24 0.48 1.01
(0.47–0.71) (0.71–1.06) (0.20–0.49) (0.10–0.37) (0.33–0.63) (0.82–1.21)
2009–2018
 P1vs. P5 0.68 0.57 0.81 0.50 0.83 0.66
(0.54–0.82) (0.44–0.71) (0.62–1.01) (0.16–0.79) (0.60–1.05) (0.50–0.82)
 P5vs. MMT 2.38 1.37 3.76 4.56 3.57 1.62
(1.23–3.48) (0.54–2.27) (1.99–5.49) (1.65–7.28) (1.37–6.02) (0.64–2.54)
  MMT vs. P95 0.64 1.12 0.43 0.62 0.25 1.63
(0.19–1.09) (0.14–2.01) (0.00-0.84) (-0.12-1.44) (0.11–0.39) (0.67–2.58)
 P95vs. P99 0.49 0.69 0.33 0.25 0.33 0.82
(0.39–0.59) (0.53–0.84) (0.21–0.44) (0.05–0.44) (0.25–0.41) (0.65–0.99)
Cold: moderate cold (P5vs. MMT) and extreme cold (P1vs. P5)
Heat: moderate heat (MMT vs. P95) and extreme heat (P95vs. P99)

cooling down until 2000–2010, driven by a higher rate present analysis tackles the topic of the adaptation to
of decrease of risk of death for cold temperatures, and warming environment from a wider perspective, which
remained constant from then onwards. These results are might affect the flexibility of the selected model to repro-
in line with the findings presented in our study, which is duce the monotonically decreasing trends in the risks at
based on the individual level mortality data scaled up to all temperatures.
the national level. The disaggregation of these individual Gosling et al. [7] suggested to model the adaptation by
data by cause of death, sex and age in barely populated threshold shifts and reductions in the exposure-response
rural areas (municipalities with less than 10 000 inhab- association. In our study, we quantified the temporal
itants) is not available since the provider cannot release variation in impact estimates such as MMTs and attrib-
these data due to the risk of the disclosure of personal utable fractions, giving a comprehensive picture of how
information, in this way complying with the confiden- non-optimal temperatures have affected the population
tiality and data protection regulations. Moreover, the over the past 40 years in Spain. Days with exceptionally
Ordanovich et al. Environmental Health (2023) 22:5 Page 8 of 10

high temperatures have become more common, and this society-based and technology-driven adjustments.
trend is expected to continue. Therefore, it is reasonable This is a standard limitation in epidemiological studies
to assume that, to some extent, people and societies can of long-term adaptation to climate and weather. How-
adapt to gradual increases in average temperatures. The ever, as previously stated, we summarized the trends
decrease in the cold-related mortality could be explained of non-climate driven factors changing over 40 years,
by a possible biological adaptation to extreme ambient such as demographic changes and economic growth,
temperatures [37] or a possible modification in suscepti- which could influence long-term adaptation to climate
bility to temperature [30]. (Table  4). Third, we did not include data on air pollu-
The decrease in the heat-related mortality since 1999 tion and influenza epidemics. Nevertheless, Buckley
occurred despite the progressive shift of the tempera- et al. [38] stated that air pollution should not confound
tures towards warmer ranges. It has been attributed the effects of temperature. Others also showed no
to the implementation the Heat Health Prevention changes in the temperature-mortality association when
Plan [31]. Moreover, other factors may contribute to fitting influenza epidemics in sensitivity analyses [39].
changes in susceptibility to non-optimal tempera- Finally, we accounted for short-term mortality displace-
tures, such as the ageing population, improvements ment of up to three weeks. Mortality displacement at a
in healthcare and health interventions, living condi- longer scale was not considered. However, Armstrong
tions and urban built environment, and social progress et al. [40] reported that the effects of having low winter
(Table  4). The proportion of population aged over 65 mortality in the following summer were low in Spain.
years increased by 6.2% between 1979 and 1989 and
2009–2018, life expectancy 6.5 years, GDP 67.5% and Conclusion
health expenditure was doubled. In addition, the use of Our study provides nationwide quantitative estimates
air conditioning has increased in the last decades from for long-term adaptation to non-optimal temperatures
9 to 43.7%, which can also explain part of the decline in Spain over the past 40 years. Despite the progressively
in the heat-related mortality [33]. We acknowledge warmer temperatures in Spain, we observed a persis-
some limitations in our study. First, we considered tent flattening of the exposure-response curves, which
all causes of death, including ones that might not be marked an expansion of the optimal temperature ranges
related to ambient temperatures, rather than just natu- for cold and heat. Adaptation has been produced to
ral causes. However, this has allowed us to include all some extent in a non-uniform manner with a substantial
deaths in locations with less than 10,000 inhabitants decrease in cold-related mortality, while for heat became
that have been rarely considered in previous studies in more apparent in the most recent decade only. Since the
Spain. Likewise, our study did not consider geographic climate change projections indicate a substantial increase
variability since the main objective was to address in temperatures in Spain [4, 6] and more than a third of
the long-term adaptation to non-optimal tempera- all deaths caused by heat may be attributable to global
tures at the national level. Second, we could not dif- warming [41], Spain must set as a priority to develop an
ferentiate between physiological, behavioral, cultural, adaptation strategy to climate change.

Table 4  Changes in the demographic and socioeconomic indicators in Spain between 1979 and 2018
Population older than 65 Life expectancy at birth GDP, constant 2015 Health expenditure as % Air conditioning
years (%) (a) (years) (b) US$ (c) of GDP (d) prevalence (%)
(e)

1979–1988 11.7 76.1 15389.6 4.5


1989–1998 14.5 77.8 19842.1 5.5 9.0
1999–2008 16.7 80.1 25463.8 7.5 27.2
2009–2018 17.9 82.6 25784.7 9.1 43.7
Indicators estimated as average value for each decade according to the data availability
a
Population structure indicators by National Institute of Statistics of Spain. Available at www.​ine.​es
b
Demographic indicators by National Institute of Statistics of Spain. Available at www.​ine.​es
c
GDP per capita by World Bank. Available at data.​world​bank.​org
d
Public health spending in Spain: 10 years of national health system by Ministry of Economy and Finance. Global Health Expenditure by World Health Organization.
Available at apps.​who.​int
e
Population and Housing Census, Life Conditions Survey, Households and Environment Survey by National Institute of Statistics of Spain. Available at www.​ine.​es.
Housing survey by the Center for Sociological Studies. Available at www.​cis.​es
Ordanovich et al. Environmental Health (2023) 22:5 Page 9 of 10

Abbreviations Competing interests


RCP Representative Concentration Pathway The authors declare that they have no competing interests.
MMT Minimum Mortality Temperature
MMTP Minimum Mortality Temperature Percentile Consent for publication
IPCC Intergovernmental Panel on Climate Change The informed consent for publication was obtained from all the authors.
ECMWF Centre for Medium-Range Weather Forecasts
INSPIRE Infrastructure for Spatial Information in Europe
Received: 30 September 2022 Accepted: 30 December 2022

Supplementary Information
The online version contains supplementary material available at https://​doi.​
org/​10.​1186/​s12940-​022-​00957-6.
References
Additional file 1. Sensitivity analysis results. Figure 6. Sensitivity analysis 1. Guo Y, Gasparrini A, Armstrong B, Li S, Tawatsupa B, Tobias A, et al. Global
performed for degrees of freedom for seasonal trend (top row), for the lag variation in the effects of ambient temperature on mortality: a systematic
period (middle row) and for the number of knots for exposure-response evaluation. Epidemiology. 2014;25(6):781–9.
function (bottow row). 2. Gasparrini A, Guo Y, Hashizume M, Lavigne E, Zanobetti A,
Schwartz J, et al. Mortality risk attributable to high and low ambi-
Additional file 2. Distribution of the mean temperature in Spain by ent temperature: a multicountry observational study. Lancet.
decades between 1979 and 2018 in Spain. Figure 3. Variations in the mean 2015;25(9991):369–75.
temperature between 1979 and 2018 in Spain (including archipelagos). 3. Song X, Wang S, Hu Y, Yue M, Zhang T, Liu Y, et al. Impact of ambient
Additional file 3. Overall temperature-mortality associations estimated temperature on morbidity and mortality: an overview of reviews. Sci Total
for Spanish provincial capital cities between 1979 and 2018. Figure 4. Environ. 2017;15:241–54.
Overall temperature-mortality associations estimated for Spanish provin- 4. IPCC. Climate Change 2021 the physical science basis, Working Group 1
cial capital cities between 1979 and 2018. (WG1) contribution to the Sixth Assessment Report of the Intergovern-
mental Panel on Climate Change. Cambridge University Press Cambridge,
Additional file 4. Comparison of the overall temperature-mortality
UK; 2021.
association estimated nationwide and using a two-stage design pooling
5. Vicedo-Cabrera AM, Guo Y, Sera F, Huber V, Schleussner CF, Mitchell
provincial capital cities exposure-response curves. Figure 5. Temperature-
D, et al. Temperature-related mortality impacts under and beyond
mortality associations estimated nationwide and using a two-stage design
Paris Agreement climate change scenarios. Climatic Change.
pooling provincial capital cities exposure-response curves.
2018;150(3):391–402.
6. Amblar Francés P, Casado Calle MJ, Pastor Saavedra A, Ramos Calzado
P, Rodríguez Camino E. Guía de escenarios regionalizados de cambio
Acknowledgements
climático sobre España a partir de los resultados del IPCC-AR5. Agencia
The analysis conducted in this study was made possible thanks to the National
Estatal de Meteorología; 2017. Available from: http://​www.​aemet.​es/​es/​
Institute of Statistics of Spain (INE) which provided the mortality data.
conoc​ermas/​recur​sos_​en_​linea/​publi​cacio​nes_y_​estud​ios/​publi​cacio​
nes/​detal​les/​Guia_​escen​arios_​AR5. Cited 2022 Aug 16.
Authors’ contributions
7. Gosling SN, Hondula DM, Bunker A, Ibarreta D, Liu J, Zhang X, et al.
Dariya Ordanovich designed the study, did the statistical analysis and draft the
Adaptation to Climate Change: a comparative analysis of mod-
manuscript. Aurelio Tobías contributed to the statistical analysis and drafting
eling methods for heat-related mortality. Environ Health Perspect.
of the manuscript. Diego Ramiro contributed to the drafting of the manu-
2017;16(8):087008.
script. All authors contributed to the submitted version of the manuscript and
8. Honda Y, Kabuto M, Ono M, Uchiyama I. Determination of optimum daily
approved the final version.
maximum temperature using climate data. Environ Health Prev Med.
2007;12(5):209–16.
Funding
9. Huynen MMTE, Martens P. Climate change effects on heat- and cold-
Open Access funding provided thanks to the CRUE-CSIC agreement with
related mortality in the Netherlands: a scenario-based integrated
Springer Nature. Dariya Ordanovich was supported by LONGPOP H2020 ITN
environmental health impact assessment. Int J Environ Res Public Health.
Marie Sklodowska-Curie grant (agreement Nº 676060) and ERC Advanced
2015;12(10):13295–320.
ECHO H2020 grant (agreement Nº 788582).
10. Huang C, Barnett AG, Wang X, Vaneckova P, FitzGerald G, Tong S. Project-
Aurelio Tobías was supported by Grant CEX2018–000794-S funded by MCIN/
ing future heat-related mortality under climate change scenarios: a
AEI/https://​doi.​org/​10.​13039/​50110​00110​33.
systematic review. Environ Health Perspect. 2011;119(12):1681–90.
Diego Ramiro was supported by PTI Salud Global CSIC WP3 Modelling (BDC
11. Åström C, Tornevi A, Ebi K, Rocklöv J, Forsberg B. Evolution of minimum
SGL2103000) and Proyectos I + D + i Retos Investigación (RTI2018-097812-B-I00).
mortality temperature in Stockholm, Sweden, 1901–2009. Environ Health
Perspect. 2016;124(6). Available from: https://​pubmed.​ncbi.​nlm.​nih.​gov/​
Availability of data and materials
26566​270/. Cited 2022 Feb 21.
Mortality data cannot be made publicly available under the Spain National Insti-
12. Folkerts MA, Bröde P, Botzen WJW, Martinius ML, Gerrett N, Harmsen CN,
tute of Statistics (INE) sharing agreement. Temperature data can be downloaded
et al. Long Term Adaptation to heat stress: shifts in the minimum mortal-
from the European Centre for Medium-Range Weather Forecasts (ECMWF).
ity temperature in the Netherlands. Front Physiol. 2020;11:225.
13. Todd N, Valleron AJ. Space-time covariation of mortality with tempera-
Declarations ture: a systematic study of deaths in France, 1968–2009. Environ Health
Perspect. 2015;123(7):659–64.
Ethics approval and consent to participate 14. Bobb JF, Peng RD, Bell ML, Dominici F. Heat-related mortality and
This study is based on the individual mortality data provided to the authors in adaptation to heat in the United States. Environ Health Perspect.
the anonymized form by the National Institute of Statistics of Spain (INE). The 2014;122(8):811–6.
reference information on the municipality of the residence of the deceased 15. Gasparrini A, Guo Y, Hashizume M, Kinney PL, Petkova EP, Lavigne E, et al.
was available only in case where the municipality had more than 10 000 of Temporal variation in Heat-Mortality Associations: a Multicountry Study.
inhabitants, otherwise only the reference data on the province and autono- Environ Health Perspect. 2015;123(11):1200–7.
mous community was available. For the purposes of this study these data 16. Ng CFS, Boeckmann M, Ueda K, Zeeb H, Nitta H, Watanabe C, et al. Heat-
were aggregated to large spatial units. The data comply with the Data Protec- related mortality: effect modification and adaptation in Japan from 1972
tion Act and do not require any ethical approval or special permission. to 2010. Glob Environ Change. 2016;1:234–43.
Ordanovich et al. Environmental Health (2023) 22:5 Page 10 of 10

17. Chung Y, Yang D, Gasparrini A, Vicedo-Cabrera AM, Fook Sheng Ng C, Kim 40. Armstrong B, Bell ML, de Sousa Zanotti Stagliorio Coelho M, Leon Guo YL,
Y, et al. Changing susceptibility to non-optimum temperatures in Japan, Guo Y, Goodman P, et al. Longer-term impact of high and low tempera-
1972–2012: the role of climate, demographic, and socioeconomic factors. ture on mortality: an International Study to clarify length of Mortality
Environ Health Perspect. 2018;126(5):057002. Displacement. Environ Health Perspect. 2017;27(10):107009.
18. Achebak H, Devolder D, Ballester J. Trends in temperature-related age- 41. Vicedo-Cabrera AM, Scovronick N, Sera F, Royé D, Schneider R, Tobias A,
specific and sex-specific mortality from cardiovascular diseases in Spain: a et al. The burden of heat-related mortality attributable to recent human-
national time-series analysis. Lancet Planet Health. 2019;3(7):e297-306. induced climate change. Nat Clim Chang. 2021;11(6):492–500.
19. Achebak H, Devolder D, Ingole V, Ballester J. Reversal of the seasonality of
temperature-attributable mortality from respiratory diseases in Spain. Nat
Commun. 2020;20(1):2457. Publisher’s Note
20. Dee DP, Uppala SM, Simmons AJ, Berrisford P, Poli P, Kobayashi S, et al. Springer Nature remains neutral with regard to jurisdictional claims in pub-
The ERA-Interim reanalysis: configuration and performance of the data lished maps and institutional affiliations.
assimilation system. Q J R Meteorol Soc. 2011;137(656):553–97.
21. Hoffmann L, Günther G, Li D, Stein O, Wu X, Griessbach S, et al. From ERA-
Interim to ERA5: the considerable impact of ECMWF’s next-generation
reanalysis on Lagrangian transport simulations. Atmos Chem Phys.
2019;19(11):3097–124.
22. Zhao P, Gao L, Wei J, Ma M, Deng H, Gao J, et al. Evaluation of ERA-interim
air temperature data over the Qilian Mountains of China. Adv Meteorol.
2020;10(2020):e7353482.
23. Royé D, Íñiguez C, Tobías A. Comparison of temperature–mortality asso-
ciations using observed weather station and reanalysis data in 52 Spanish
cities. Environ Res. 2020;1(183):109237.
24. Bhaskaran K, Gasparrini A, Hajat S, Smeeth L, Armstrong B. Time series
regression studies in environmental epidemiology. Int J Epidemiol.
2013;42(4):1187–95.
25. Gasparrini A, Armstrong B, Kenward MG. Distributed lag non-linear mod-
els. Stat Med. 2010;29(21):2224–34.
26. Gasparrini A. Distributed lag linear and non-linear models in R: the pack-
age dlnm. J Stat Softw. 2011;25(43):1–20.
27. Tobías A, Hashizume M, Honda Y, Sera F, Ng CFS, Kim Y, et al. Geographi-
cal variations of the Minimum Mortality temperature at a global scale: a
Multicountry Study. Environ Epidemiol. 2021;5(5):e169.
28. Iñiguez C, Royé D, Tobías A. Contrasting patterns of temperature related
mortality and hospitalization by cardiovascular and respiratory diseases
in 52 Spanish cities. Environ Res. 2021;1(192):110191.
29. Gasparrini A, Leone M. Attributable risk from distributed lag models. BMC
Med Res Methodol. 2014;14(1):55.
30. Vicedo-Cabrera AM, Sera F, Guo Y, Chung Y, Arbuthnott K, Tong S, et al.
A multi-country analysis on potential adaptive mechanisms to cold and
heat in a changing climate. Environ Int. 2018;111:239–46.
31. Martínez-Solanas È, Basagaña X. Temporal changes in temperature-
related mortality in Spain and effect of the implementation of a Heat
Health Prevention Plan. Environ Res. 2019;169:102–13.
32. de Sanidad M. Consumo y Bienestar Social. Plan Nacional de Actuaciones
Preventivas de los Efectos del Exceso de Temperaturas sobre la Salud.
2004. Available from: https://​www.​sanid​ad.​gob.​es/​exces​oTemp​eratu​ras20​
22/​consu​ltar.​do.
33. Sera F, Gasparrini A. Extended two-stage designs for environmental
research. Environ Health. 2022;21(1):41.
34. Chazarra A, Lorenzo B, Rodriguez C, Botey R. Análisis de las temperaturas
en España en el periodo 1961–2018. Volumen 2 series de temperaturas
medias en España a partir de estaciones de referencia (nota técnica 31.2
de AEMET). Agencia Estatal de Meteorología; 2020. Available from: http://​
www.​aemet.​es/​es/​conoc​ermas/​recur​sos_​en_​linea/​publi​cacio​nes_y_​
estud​ios/​publi​cacio​nes/​detal​les/​NT31_​AEMET.
35. Barrett JR. Increased Minimum Mortality temperature in France: data sug-
Ready to submit your research ? Choose BMC and benefit from:
gest humans are adapting to Climate Change. Environ Health Perspect.
2015;123(7):A184.
• fast, convenient online submission
36. Achebak H, Devolder D, Ballester J. Heat-related mortality trends under
recent climate warming in Spain: a 36-year observational study. PLoS • thorough peer review by experienced researchers in your field
Med. 2018;15(7):e1002617. • rapid publication on acceptance
37. Boeckmann M, Rohn I. Is planned adaptation to heat reducing heat-
• support for research data, including large and complex data types
related mortality and illness? A systematic review. BMC Public Health.
2014;14(1):1112. • gold Open Access which fosters wider collaboration and increased citations
38. Buckley JP, Samet JM, Richardson DB. Commentary. Does air pollution • maximum visibility for your research: over 100M website views per year
confound studies of temperature? Epidemiology. 2014;25(2):242–5.
39. Lee WH, Lim YH, Dang TN, Seposo X, Honda Y, Guo YLL, et al. An investiga- At BMC, research is always in progress.
tion on attributes of ambient temperature and diurnal temperature
range on mortality in five East-Asian Countries. Sci Rep. 2017;31(1):10207. Learn more biomedcentral.com/submissions

You might also like