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Received: 12 April 2023 | Accepted: 3 May 2023

DOI: 10.1111/pai.13961

REVIEW ARTICLE

Environmental influences on childhood asthma: Climate change

Benedetta Biagioni1 | Lorenzo Cecchi2,3 | Gennaro D'Amato4 |


Isabella Annesi-­Maesano5

1
Allergy and Clinical Immunology Unit,
San Giovanni di Dio Hospital, Florence, Abstract
Italy
Climate change is a key environmental factor for allergic respiratory diseases, espe-
2
Centre of Bioclimatology, University of
Florence, Florence, Italy
cially in childhood. This review describes the influences of climate change on childhood
3
SOS Allergy and Clinical Immunology, asthma considering the factors acting directly, indirectly and with their amplifying in-
USL Toscana Centro, Prato, Italy teractions. Recent findings on the direct effects of temperature and weather changes,
4
Division of Respiratory Diseases and
as well as the influences of climate change on air pollution, allergens, biocontaminants
Allergy AORN Cardarelli and University of
Naples, Federico II, Naples, Italy and their interplays, are discussed herein. The review also focusses on the impact
5
Department of Allergic and Respiratory of climate change on biodiversity loss and on migration status as a model to study
Diseases, Montpellier University Hospital,
Institute Desbrest of Epidemiology and environmental effects on childhood asthma onset and progression. Adaptation and
Public Health, University of Montpellier mitigation strategies are urgently needed to prevent further respiratory diseases and
and INSERM, Montpellier, France
human health damage in general, especially in younger and future generations.
Correspondence
Benedetta Biagioni, Allergy and Clinical KEYWORDS
Immunology Unit, San Giovanni di Dio air pollution, allergens, asthma, biocontaminants, children, climate change, environmental
Hospital, Florence, Italy. exposure, migration, mitigation, thunderstorm asthma
Email: biagionibenedetta@gmail.com

Editor: Ömer Kalayci

1 | I NTRO D U C TI O N a direct (through heat waves, floods and other extreme weather
events), indirect (modulating allergen levels and location, augment-
Asthma is a major noncommunicable disease (NCD), affecting an esti- ing pollution damages, modifying biocontamination and microbial
mated 262 million people in 20191 and representing the most common exposure) and mixed way (effect of thunderstorm on pollen or
chronic disease among children. The incidence of asthma has risen in the moulds, of climate change on air pollution on pollen or infections) 8
last decades, and evidence for climate change perpetration is increas- (Figure 1).
ing. Earth's temperature has risen by an average of 0.08° Celsius (0.14° Climate change can also be one of the causes forcing people to
Fahrenheit) per decade since 1880 and the rate of warming since 1981 migrate, which according to the situation, can be responsible for the
is more than twice as fast, 0.18°C (0.32°F) per decade. The 2022 sur- development or the aggravation of asthma.9
face temperature was 0.86°C (1.55°F) warmer than the 20th-­century Efforts to mitigate climate change effects are urgently needed
average and 1.06°C (1.90°F) warmer than the preindustrial period.2 to protect the public's health, especially for the more vulnerable
Several epidemiological studies have pointed out that climate populations, including children. Mitigation and adaptation strategies
change is leading to an increased incidence of this respiratory dis- targeting both air pollution and climate change simultaneously are
ease, through various effects,3 largely among more vulnerable sub- necessary to improve respiratory health and beyond and to secure a
jects, such as children.4,5 Climate change impacts respiratory allergic future for younger generations.
diseases including asthma by altering the environment to which the We present here evidence of the multifaceted action of climate
6,7
subject is exposed and therefore acting on his/her exposome in change on childhood asthma.

© 2023 European Academy of Allergy and Clinical Immunology and John Wiley & Sons Ltd.

Pediatr Allergy Immunol. 2023;34:e13961.  wileyonlinelibrary.com/journal/pai | 1 of 11


https://doi.org/10.1111/pai.13961
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2 of 11 BIAGIONI et al.

2 | D I R EC T E FFEC T S O F C LI M ATE
C H A N G E O N C H I LD H O O D A S TH M A Key message

Climate change is a key environmental factor for the rise


In the last decades, a plethora of studies demonstrated that changes
and worsening of allergic respiratory diseases, especially
in some climate variables increase respiratory morbidity and mor-
in children. Climate change influences childhood asthma
tality in adult patients with chronic respiratory diseases, such as
in direct, indirect and mixed ways and represents a global
asthma and COPD, and other serious less common lung diseases.
issue to urgently address with adaptation and mitigation
Extreme weather events, such as heatwaves and cyclones, as well as
strategies.
high humidity, can trigger asthma symptoms. Future studies with a
larger cohort are necessary to deeper examine the relationship be-
tween respiratory diseases and weather patterns, in order to predict
the onset of symptoms and diseases in various regions and weather often more frequent and severe during heatwaves. The detrimental
conditions. effects of heatwaves have been extensively described in numerous
epidemiological studies, showing that respiratory diseases increased
among children during such events and that children with respiratory
2.1 | Heatwaves and Wildfires diseases were more frequently hospitalized during these extreme
weather periods.10 Fine particulate levels can reach extreme con-
Heatwaves can be defined as a period of at least three–­five con- centrations during wildfires causing acute asthma exacerbations11
secutive days of prolonged heat, in which the daily maximum tem- and acute decrements in peak expiratory flow.12 Long-­term effect
perature is higher than the average maximum temperature by 5°C of wildfire smoke exposure is also well documented. An increase in
(9°F) or more. Wildfires, unplanned fires that burn in natural areas, physician-­dispensed short-­acting beta-­agonists for asthmatic chil-
can be caused by human activity or by natural phenomena and are dren was observed in the years following cataclysmic wildfires,13

F I G U R E 1 The multiple roles of Climate Change on childhood asthma. Climate change acts directly with weather events (in brown)
and indirectly –­through its influence on air pollution, allergens, biodiversity, biocontaminants and their interplay (in green) –­on childhood
asthma development, progression and/or exacerbation. These interconnected factors can act directly on asthma in pediatric populations
(continuous arrows) or through genetic/epigenetic modifications (dotted arrows).
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BIAGIONI et al. 3 of 11

and the exposure to wildfire smoke was also associated with a sig- NO2.12,35 The strongest impact of long-­term exposures on lung func-
nificant decline in lung function among children without bronchial tion is demonstrated on FEV1, while FVC seems to be less affected,
hyper-­reactivity.14 suggesting that air pollutants can modulate especially the airflow
obstruction rather than children's overall lung size.12
The effect of high levels of air pollution on asthma exacerbations
2.2 | Coldspells in the pediatric population has been reported in the last decades
worldwide, but mainly from developed countries.19–­24 Babin et al. re-
A cold spell is an extreme atmospheric event characterized by anom- ported in 200725 an association between pediatric asthma ED visits
alous low-­temperatures over consecutive days. Currently, there is in Washington, DC, from 2001 to 2004 and outdoor ozone concen-
not a single standard definition of a cold spell. This meteorological tration with the strongest evidence regarding children aged 5–­12. In
event consists of a rapid fall in temperature within a period of 24–­ the same year, Ko et al. 26 assessed the relationship between levels
72 h, with a variable temperature drop rate compared with a mini- of outdoor NO2, O3, PM10 and PM2.5 and hospitalization rates for
mum temperature that depends on the geographical region and time asthma in Hong Kong, demonstrating that patients from the younger
of year. It has been observed that exposure to a cold spell increases age group (0–­14 years) had a higher RR for each 10 mg/m3 increase
the risk of premature morbidity and mortality, especially for patients in air pollutants, compared with older patients, aged 15–­65 years. A
with cardiovascular and respiratory diseases.15 Studies conducted large population-­based study conducted in Atlanta between 1993
in China showed an association between cold spells and both child- and 200427 showed that, even at relatively low ambient concen-
hood asthma and allergic rhinitis. It was found that the association trations, both ozone and primary pollutants from traffic sources
between cold spells and asthma is stronger in boys and school-­age independently contributed to the burden of the daily emergency
children and that if a cold spell lasts for several days, its impact in department visits for asthma or wheeze among children aged from
later days tends to be greater than that of the previous ones.16 It 5 to 17 years. Subsequently, Silverman et al28 demonstrated a rela-
was also demonstrated that cold spells may significantly increase al- tionship between severe asthma morbidity and both PM2.5 and O3
lergic rhinitis in pediatric patients, especially in male children, aged levels in the warm season, analysing asthma admission in New York
5–­18 years and nonscattered children.17 City hospitals from 1999 to 2006. Stratification in 4 age groups (<6,
6–­18, 18–­50, >50) demonstrated that children aged 6–­18 years had
the highest risk of severe asthma exacerbations with a 26% (95%
3 | I N D I R EC T E FFEC T S O F C LI M ATE CI, 10%–­4 4%), increased rate of ICU admissions and a 19% (95% CI,
C H A N G E O N C H I LD H O O D A S TH M A 12%–­27%), increased rate of general hospitalizations for each 12-­
mg/m3 increase in PM2.5 and a 19% (95% CI, 1%–­4 0%), increased risk
Climate change plays a role on respiratory health including asthma for ICU admissions, and a 20% (95% CI, 11%–­29%) increased risk for
also in an indirect way, affecting some of the major risk factors for general hospitalizations for each 22-­ppb increase in ozone. Lastly, a
the development, progression and exacerbation of lung diseases. recently published questionnaire-­based retrospective cohort study,
Risk factors for childhood asthma that are enhanced by climate including data from 2011 to 2012 on 39,782 preschool children in
change are air pollution, aeroallergens, greenspaces and biocontami- China, explored the effects of temperature–­pollution interactions
nants (like viruses and bacteria). Climate change can act on these during pre-­and postnatal periods on asthma, 29 showing that asthma
factors alone or through their multiple interplay. prevalence in children aged 3–­6 years was significantly associated
not only with traffic-­related air pollutant (NO2) exposure but also
with exposure to an increased temperature during lifetime, preg-
3.1 | Air pollution nancy and postnatal period.
Several studies have shown that exposure to the classic air
It is well known that climate change and air pollution influence and pollutants (PM10 and/or SO2) in utero or during the first years of
enhance each other, as many of the air pollutants are greenhouse life was positively related to asthma and allergies. The first evi-
gases. It is foreseeable that in the near future global warming will dence of a significant association between childhood asthma and
lead to increasingly prolonged episodes of peak ozone concentra- early-­life exposure to ambient air pollutants was demonstrated in
tion in urban areas and that atmospheric concentrations of pollut- 2010. 30 Subsequent studies showed that not only asthma but also
ants and levels of atmospheric particulate matter (PM) will increase other childhood allergic diseases, including allergic rhinitis and ec-
in industrialized and more prone to vehicle traffic environments.8 zema, were mainly associated with exposure to traffic-­related air
Several reports showed the association of increased ambient levels pollutant, namely NO2 and especially in a specific trimester during
of air pollutants with reduced lung function,12,18 worsening asthma pregnancy. In fact, the authors showed that exposure during the
19–­23
symptoms and asthma-­related emergency department visits or first trimester of pregnancy was related to higher risk of develop-
hospitalizations in children, 24–­29 as well as asthma development.30–­34 ing eczema (1.54, 1.14–­2 .09), the second trimester with higher risk
The relationship between air pollution exposure and children's of asthma occurrence (1.72, 1.02–­2 .97), and the third trimester
lung function was shown with stronger evidence for PM2.5 and with the onset of allergic rhinitis (1.77, 1.09–­2 .89). 31 Recently, the
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4 of 11 BIAGIONI et al.

Official American Thoracic Society Workshop Report stated that by urbanization and desertification.39,40 Climate conditions leading
long-­term exposure to air pollution is associated with the onset of to the increase in airborne pollen concentration influence the preva-
childhood asthma, especially traffic-­related air pollution (NO2 and lence and severity of ARD. In particular, high temperatures, low
black carbon). 32 A subsequent meta-­analysis by Han K. et al. 33 fo- atmospheric humidity and sunny meteorological conditions have
cussed on the effect of early childhood exposure to traffic-­related all been associated with increased pollen count and augmented al-
air pollution (TRAP) on asthma development. The causative role lergic rhinitis prevalence in children.37 Climate factors are probably
of fine particulate matter (PM2.5), nitrogen dioxide (NO2), benzene able to directly influence pollen potency too: preliminary data from
and total volatile organic pollutants (TVOCs) exposures was anal- HIALINE project showed that the content of group five grass aller-
ysed in the 27 studies included in this meta-­analysis, demonstrat- gens is positively associated with outdoor humidity.41 We published
ing that TRAP increases the risk of asthma among children with a systematic review and meta-­analysis, showing that in the last dec-
the following odd ratios and confidence intervals: meta-­O R = 1.07, ades a large number of studies reported the evidence of a significant
95% CI: 1.00–­1.13 for PM2.5, meta-­O R = 1.11, 95% 23 CI: 1.06–­ positive association between total pollen concentrations and asthma
1.17 for NO2 , meta-­O R: 1.21, 95% CI: 1.13–­1.29 for Benzene and exacerbations in the pediatric population, requiring ED visits or hos-
meta-­O R: 1.06, 95% CI: 24 1.03–­1.10 for TVOC. The most recent pital admission.42 Among them, in the last decade an association
and extensive review on this topic, performed by Moreira and between children asthma-­related ED admissions or hospitalizations
coll., 34 focussed on the relationship between childhood asthma and total pollen counts was reported in Australia in a case-­crossover
and air pollution—­specifically industrial pollutants, traffic-­related, study43 and in a time-­series analysis,44 the latter reporting a positive
due to disinfection products and tobacco smoke—­underlying the association with a 10 unit increase in total pollen count. As we sum-
role of environmental inequality at the basis of an unequal dis- marized,42 the strongest evidence of this association was observed
tribution of the risks and benefits of different living settings and in patients under 18 years of age, especially regarding grass pollen
conditions. concentration increase in the 2 days before the asthma exacerbation
All this evidence points to the urgent need to designate accept- reports.43,45–­48 Similar results were described for pollen of various
able thresholds for air pollutants, in order to prevent severe or life-­ tree species: several studies showed a positive association between
threatening asthma episodes, especially in more vulnerable subjects, severe asthma exacerbations in patients younger than 18 years old
such as the pediatric population. and an increase in pollen concentration from different tree species in
the previous 2–­4 days.42,43,46,48 Positive associations were found for
birch pollen concentration increase in patients of this age group.42,49
3.2 | Allergens A positive association between the increase in pollen concentration
and an augmented risk of reduced lung function was also observed
Climate change influences aeroallergens too, increasing their pro- in a recent meta-­analysis by Idrose et al.,50 considering the obtain-
duction, their atmospheric concentration and their geographical dis- able data on the effect of outdoor pollen exposure on both lung
tribution as well as we will see below their allergenicity.36 Climate function parameters and airway inflammation markers.
change impacts the quantity and quality of aeroallergens. These
can trigger or enhance the production of pro-­
inflammatory and
immunomodulatory mediators necessary to the occurrence of IgE-­ 3.2.2 | Dust mites
mediated sensitization, thus accelerating the onset of allergic res-
piratory diseases and causing their exacerbations.3,6,7 Dust mites are a major source of allergens inside homes,
Dermatophagoides pteronyssinus and Dermatophagoides farinae
being the most common species of dust mite reported in Western
3.2.1 | Pollen Countries.51 Global warming affects dust mite proliferation and sur-
vival because both temperature and relative humidity are important
Airborne pollen are one of the most common causative agents of adjuvating factors for the natural life cycle of these invisible arthro-
allergic respiratory disease. Climate change influences not only the podes. Older homes, increased population density, lower income,
quantity but also the quality of pollen allergens; in fact, seasonal var- presence of cockroaches and mould, presence of carpeting and lack
iations in pollens due to weather events have occurred worldwide, of air conditioning are all factors involved in the increase of dust
along with an increased sensitization rate to pollen both in pediat- mite exposure.52 House dust mite allergens have a high allergenic
9
ric and adult population. Weather conditions may influence pollen potency, activating both the innate and adaptive immune response
concentrations altering the biogeographic distribution of plants and towards a Th2-­polarization and thus causing the onset and aggrava-
affecting the vegetal life cycle.37 An increased pollen production and tion of allergic respiratory diseases.53 Early exposure to house dust
an augmented duration of pollen season with anticipation of the pol- mite allergens has been associated with asthma development long
len season was demonstrated for grass,37 birch, oak and olive tree ago, and to date the suggested threshold level for sensitization to
pollen.38 Moreover, allergenic plants, such as ragweed, are spread- Dermatophagoides pteronyssinus major allergen, Der p 1 is >2 μg/g
ing, finding favourable conditions in a soil more and more damaged while a level of 10 μg/g of Der p 1 represents a significant risk
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BIAGIONI et al. 5 of 11

factor for the development of asthma in already dust mite-­sensitized Furthermore, several experimental studies have demonstrated that
51
individuals. the permeability of the respiratory epithelium and the mucociliary
clearance are subject to modification by atmospheric pollutants,
O3, NO2 and diesel particulate emissions in particular.7 The increase
3.2.3 | Mould in permeability and the reduction of mucociliary clearance due to
these pollutants facilitate the permanence of allergens and irritating
Global warming affects the quantity, intensity and frequency of pre- products on the epithelium surface and allow its entry at the level
cipitation type as well as the frequency of extreme weather events of the submucosa, favouring pathogenic immunological pathways.
such as flood and intensive precipitation, which can result in damp-
ness, leading to mould proliferation, causing asthma exacerbations
in sensitized subjects.54 Recent reviews about indoor mould expo- 4.2 | Thunderstorm asthma
sure and respiratory allergic diseases have established the causal re-
lationship between the presence of visible mould and mould odour The peculiar interaction between extreme weather events due to
55
with the development and exacerbations of asthma in children. climate change, aeroallergens and respiratory epithelia of sensitized
Mould-­sensitized children affected by asthma and living in inner-­city subjects can lead to acute and dangerous asthma epidemics, such as
environments are exposed to airborne fungi in both indoor and out- in the case of thunderstorm asthma, detailed below.
door air,56 and it has been demonstrated that the exposure to higher Thunderstorms are weather events characterized by striking
levels of indoor fungi causes a significant increase in unscheduled electrical activity and strong convective updraft in early phases,
visits for asthma in urban children, even after controlling for outdoor followed by a strong downdraft in a column of precipitation in dis-
fungal levels.57 Studies have also focussed on the relevance of mould sipating stages. Thunderstorm asthma (TA) can be defined as the
in the school environment and its impact on respiratory health in occurrence of acute asthma attacks immediately following a thun-
58
students. Chen et al. demonstrated the association between derstorm.36 These events are due to the combination of meteoro-
Aspergillus/Penicillium and basidiospores presence in classroom logical and aerobiological factors and can lead to asthma epidemics
and childhood asthma during school attendance,59 while Holst et al. affecting predisposed atopic patients. Thunderstorm outflows cause
showed that high levels of dampness in Danish classroom correlated the concentration of aeroallergens (mainly pollen or mould allergens)
60
with increased wheezing and decreased lung function in students. at ground level, releasing respirable allergenic particles after their
The importance of fungi exposure and sensitization in children has rupture by osmotic shock caused by humidity and rainfall. The inhala-
been demonstrated also during extreme weather conditions, such as tion of high concentrations of these aeroallergens by sensitized indi-
thunderstorm asthma episodes, discussed below. viduals can induce an early asthmatic response, eventually followed
by a late inflammatory phase.61 In the last decades, these extreme
weather events became a global health concern, because of the im-
4 | CO M B I N ATI O N O F D I R EC T A N D portant and seldom fatal clinical consequences in patients affected
I N D I R EC T E FFEC T S O F C LI M ATE C H A N G E by respiratory allergies. Climate change acceleration has the poten-
O N C H I LD H O O D A S TH M A tial of causing more frequent and unpredictable extreme weather
events such as TA; consequently, the health system has to be pre-
The combination of direct and indirect effects of climate change pared to face more severe epidemics worldwide.57 Previous data on
can result in a synergic action on respiratory health. The interac- thunderstorm asthma pandemics62–­6 4 suggested that asthma symp-
tion between climate change, air pollutants, aeroallergens, epithelial toms during thunderstorms aggravated predominantly in the adult
barrier and biocontaminants has a favourable knock-­on effect on population, affecting just 15% or less of children. Nevertheless, in
atopic sensitization as well as respiratory disease exacerbations and 2020 Y.-­Y. Xu et al. described the effect on pediatric patients of
development.7 the thunderstorm asthma that happened on 11 September 2018 in
Yulin, China.65 This study showed that thunderstorm asthma can se-
riously affect children, especially if suffering from allergic rhinitis or
4.1 | Air pollution and pollen untreated asthma and that mugwort pollen can be a relevant aeroal-
lergen in thunderstorm asthma epidemics. An increase of 2.7 and
Throughout the increase in greenhouse gases (GHGs), to date CO2, 16 times, respectively, in the mean number of daily visits to emer-
NO2 and O3 are the air pollutants that have shown the most relevant gency/outpatient department and of daily admission to hospital was
impact on aeroallergen production and potency. A number of stud- observed, with a gender prominence of males between children.
ies have shown the influence of air pollutants level, especially CO2, Among the hospitalized children, 56% of them had never experi-
not only in augmenting the rise of pollen concentrations but also enced asthma symptoms while 25% had a confirmed diagnosis of
leading to a higher expression of allergenic proteins in the pollen asthma. The vast majority of the hospitalized children (94%) showed
itself. This increased ‘allergenicity’ is responsible for the aggravation positive IgE against mugwort pollen, 78% of them being monosensi-
or development of allergic diseases in already sensitized subjects.9 tized to this pollen species.
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4.3 | Climate variables and infections severe pneumonia in immunocompromised hosts. Changes in animal
behaviour and geographic distribution due to global warming likely
Extreme weather events, such as heat waves, floods, major storms, have had an impact on the diffusion of this disease.77 Not only fungal
drought and wildfires, affect respiratory infections, and there- respiratory infections but also the spread of mycobacteriosis is in-
fore respiratory health, by affecting vectors and host immune re- tertwined with climate change. It has been demonstrated that hurri-
35
sponses. Climate change can also play a role in the new onset, canes, which have lately increased due to climate change, contribute
spreading and/or modification of infectious respiratory disease, to an increase in nontuberculous mycobacteria (NTM) disease.78,79
some of them representing known risk factors for respiratory dis- Differently from TB, NTM lung diseases are typically conveyed
ease onset and/or exacerbation, especially in children, as discussed through environmental sources, such as municipal water and soil,
further. At the same time, cold weather increases the occurrence and environment cross-­contamination by NTM is greatly favoured
of respiratory infections in individuals with underlying respiratory by hurricanes.80,81 It is evident to all how public health and safety are
3
disease. threatened and damaged by emerging viral diseases such as Ebola,
It is well known that respiratory virus infections, particularly severe acute respiratory syndrome (SARS), the avian flu and novel vi-
respiratory syncytial virus (RSV) and rhinovirus, are important risk ruses in the coronavirus family. Climate change must be considered
factors for the onset of wheezing in infants and children.66 The an important cofactor in their outbreak and spreading. Notably, both
pathogenic role of respiratory viruses as triggers for exacerbations in biodiversity decrease and air pollution increase, caused by climate
asthmatic patients is also established, even if not fully characterized. change, probably favoured the onset and diffusion of the COVID-­19
However, respiratory infections are common causes of asthma exac- pandemic.
erbation in children. Climate change can play a role in the new onset,
spreading and/or modification of infectious respiratory disease too.
An extensive body of literature shows climate change's impact on 5 | B I O D I V E R S IT Y LOS S
incidence and severity of infectious respiratory diseases through
the modifications of host immune response, exposure to fungal Climate change and urbanization are both involved in the reduction
and mycobacterial species, vectors' vitality and the spread of novel of green spaces, depletion of biodiversity and impoverishment of
viruses.67 Climate change influences respiratory viral transmission microbiota, with relevant consequences on respiratory diseases and
such as influenza epidemics by modifying its ecology and geograph- more.82 Although biodiversity is a difficult parameter to measure on
ical distribution. In fact, changes in temperature, precipitation and a global scale, in recent years there has been a unanimous scientific
relative humidity influence viral activity and transmission contrib- consensus that the planet's biodiversity is declining, and one of the
uting to the size and severity of epidemics.68 Recently, studies on most important causes of this decline is climate change. The vari-
climate change have also considered its influence on the outbreak ety and quality of the ‘internal’ microbiota, present in human skin,
of pandemics of novel pathogenic species such as COVID-­19 caused respiratory and intestinal tract is deeply influenced by the ‘external’
by the emergence of the new coronavirus SARS-­CoV-­2. Dramatic microbiota biodiversity, being continuously colonized by the micro-
temperature shifts can lead to an increased exposure to environ- biome present in water, soil, plants and animals. The ‘Biodiversity
ments where vector-­borne pathogens thrive. Rise in temperatures Hypothesis’ connected the reduction in biodiversity to chronic in-
is able to increase vectors' vitality and therefore the risk of disease flammatory and allergic diseases, stipulating that the contact with
spread.68 This has been shown, for example, in rodents that are res- nature promotes the proper functioning of the immune system and
ervoirs for Hantaviruses, a virus known for regional outbreaks man- enables immunological tolerance by enriching the human microbi-
69
ifesting as pneumonia and diffuse systemic disease. Furthermore, ome.82 According to this largely accepted theory, the reduction of
desertification, expansion of drylands and dust storms have con- external biodiversity results in a progressive depletion of the micro-
tributed to the release and diffusion of fungal dust-­borne spores bial variety with which the human body comes into contact, deter-
commonly found on soil that can cause respiratory infections, as mining an insufficient activation of the immunoregulatory pathways
70–­73
observed in Southwestern USA with Coccidiomycosis. Another and a consequent state of immunodysregulation. This hypothesis is
example is the geographic spread of Cryptococcus gattii, causal agent now supported by consistent data of subsequent studies; in fact,
of Cryptococcosis, a disease that most commonly affects immuno- many cohorts have shown that alterations in the gut microbiota
compromised human hosts. This respiratory disease, originally only during infancy and early childhood are associated with respiratory
present in subtropical areas, is expanding in Mediterranean regions diseases.83
of Europe and in Pacific Northwest regions of the USA, and it has
been hypothesized that trees and livestock trading, flocks of mi-
gratory birds, anomalous atmospheric events (e.g. tsunamis) and 6 | M I G R ATI O N S T U D I E S
human interactions have substantially contributed to the diffusion
of this pathogen.74–­76 A similar case is Histoplasma capsulatum, an Finally, climate change is directly or indirectly responsible for migra-
endemic fungus transmitted through inhalation in areas with bird tion, causing an augmented risk in migrant people, and migrant chil-
or bat droppings in northern parts of the USA and known to cause dren in particular, for the development and severity of presentation
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BIAGIONI et al. 7 of 11

of asthma and other allergic respiratory diseases,9 as discussed


below. Studies in migrant populations provide a unique opportunity
to investigate the role of environmental factors in the pathogen-
esis of asthma and other respiratory noncommunicable diseases.
Overall, these studies highlight the predominant role of environment
in driving the allergic sensitization and respiratory disease initiation
and development in migrant populations. Migrant people may ex-
perience an abrupt exposure to different environmental factors in
the host country, dealing all at once with different climate condi-
tions and new allergens, due to their relocation to areas with differ-
ent weather, flora and fauna, as well as the sudden and prolonged
exposure to high level of new air pollutants. Migrants, and children
in particular may adopt a different lifestyle after moving, including
changes in diet, physical activity and stress levels, all of those im-
pacting their immune system and increasing their risk of developing
atopic diseases. Finally, migrants may experience social and eco-
nomic disadvantages in the host country, including lower income,
limited access to healthcare and discrimination. These factors can
increase their risk of developing noncommunicable disease such as
allergic respiratory diseases and also the risk of poorer disease out-
comes.9,84 Current knowledge suggests that immigrants coming from
less affluent countries with low allergic diseases prevalence tend to
have a lower prevalence of asthma and allergic diseases compared
with native-­born population of the affluent host country, in line with
the so-­called ‘healthy immigrant effect’ observed for other noncom-
municable diseases. Nonetheless, the protective role of migrant sta-
tus towards allergic disease declines with the increasing duration of
residence in the host country and migrant people, especially in more
fragile conditions, can experience higher prevalence and severity of
respiratory diseases.
The main factors influencing the risk of developing atopic dis-
ease in migrant populations compared with autochthonous popula-
tion can be resumed as follows (9; Figure 2):

1. the burden of allergic diseases is lower in immigrants compared


with autochthonous population when the migration occurred
from a less affluent country to a high-­
income host country
(healthy immigrant effect).
2. the prevalence of allergic disorders in immigrants reaches the
prevalence of the local population in a time-­dependent process
(assimilation effect).
3. the age at migration influences the risk of ARD development.
F I G U R E 2 Main factors influencing ARDs risk in immigrant
4. there is a risk gradient between first-­and second-­generation im- people. Adapted from figure 4 Biagioni B, et al. The rising of allergic
migrants and within the second generation. respiratory diseases in a changing world: from climate change to
migration. Expert Rev Respir Med. 2020;14(10):973–­986. Ref.9
Many studies have demonstrated the role of environmental
exposures, such as air pollution and allergen levels, in augmenting
the risk of asthma and allergic respiratory disease in migrant chil- prevalence of asthma than local residents and recently Cacciani
dren. For example, Leung et al.85 found that migrant status was as- et al.87 investigated potentially avoidable hospitalizations for asthma
sociated with an increased risk of hospitalizations for asthma and in children and adolescents by migrant status in Italy and found
other wheezing disorders in Hong Kong children, afterwards Li that children with migrant backgrounds had a higher risk of hospi-
et al.86 investigating the prevalence of asthma and allergic symp- talization. Similar observations have been reported in 2021 by the
toms in Suzhou, China, found that domestic migrants had a higher group of Gallo Marin,88 with a scoping review of noncommunicable
|

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8 of 11 BIAGIONI et al.

diseases and maternal and child health needs of Venezuelan mi- and known decarbonization technologies and techniques that re-
grants in South America, and the study observed that environmental duce fossil-­based CO2 emissions, including renewable energy, nu-
factors, such as poor housing conditions and exposure to air pollu- clear power, carbon capture and storage (CCS) as well as utilization
tion, may contribute to the development of asthma and allergies in (CCU), fuel switching and efficiency gains. The second one is nega-
this population. The role of farm environment was analysed by Timm tive emissions, represented by new technologies and methods that
89
et al. in a three-­generation cohort study in Denmark founding that have been recently proposed, aiming to capture and sequester at-
selective migration from farming environments was associated with mospheric carbon to reduce carbon dioxide levels. The third and
an increased risk of asthma, suggesting that changes in environmen- last one is radiative forcing geo-­engineering, and these techniques
tal exposures, such as decreased exposure to endotoxins and farm aim to alter the earth's radiative energy budget to stabilize or re-
animals, may contribute to this increased risk. Finally, the impor- duce global temperatures.93 Urbanization, industrialization, trans-
tance of life condition of migrant children has been observed; for portation, deforestation, livestock and fossil fuel burning are the
example, Richter et al.90 investigated the burden of atopy in immi- main drivers of anthropogenic climate change, which has irrevers-
grant families living in substandard apartments in Sweden and found ible impacts on human health with present and future generations
a high prevalence of atopy in this population, suggesting that poor of children bearing unacceptably high disease burden caused by cli-
housing conditions, such as dampness and mould, may contribute to mate change. Conserving and implementing biodiversity is critical
this increased risk. to address climate change94; therefore, protecting natural elements,
Overall, these studies confirm that environmental exposures, revegetating urban areas, reforestation and improvement of public
such as climate conditions, air pollution, allergen levels and poor transport, walking and bicycling also represent important strategies
housing conditions, play a massive role in the development of asthma to both climate change mitigation and adaptation. UNHCR promotes
and allergies. Improving environmental setting may be an important protection and assistance to people displaced by the effects of cli-
strategy for preventing and managing these conditions in more frag- mate change as well as helps to increase their resilience to future dis-
ile populations such as children and migrant children in particular. asters. Mitigation of climate change can only be reached with global
and public health policy action. Media, political and public support
is therefore necessary and urgent for the development of efficient
7 | M ITI G ATI O N S TR ATEG I E S climate change mitigation and adaptation strategies.

As discussed above, climate change has a huge impact on respira- AU T H O R C O N T R I B U T I O N S


tory health and beyond, acting directly and through the complex Benedetta Biagioni contributed to writing—­
original draft and
interplay between patient genetic factors, airborne allergens and writing—­review and editing; Isabella Annesi-­Maesano and Lorenzo
pollutants. Anthropogenic climate change is a severe and press- Cecchi contributed to writing—­review and editing and conceptual-
ing global issue we must address now and tackling both air pollu- ization; Gennaro D'Amato contributed to review and editing.
tion and climate change simultaneously is of striking importance to
achieve a mitigation of climate-­related health events in general and PEER REVIEW
respiratory diseases in children in particular. Suffice to say that it The peer review history for this article is available at https://
has been estimated that meeting the minimum air pollution levels www.webof​s cien​ce.com/api/gatew​ay/wos/peer-­revie​w/10.1111/
for NO2 (1.5 μg·m−3), PM2.5 (0.4 μg·m−3) and BC (0.4 × 10−5 m−1) can pai.13961.
prevent 135,257 (23%), 191,883 (33%) and 89,191 (15%) cases of
asthma in children, respectively.91 It is also known that exposure ORCID
to high temperatures and pollution, as direct effects of climate Isabella Annesi-­Maesano https://orcid.
change, can affect the host immune system. Therefore, the fight org/0000-0002-6340-9300
against fossil fuel emissions and air pollution can prevent the out-
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