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ORIGINAL PAPER
Madeira—a tourist destination for asthma sufferers
Irene Camacho
1
&Agnieszka Grinn-Gofroń
2
&Roberto Camacho
1
&Pedro Berenguer
3
&
Magdalena Sadyś
4
Received: 10 November 2015 /Revised: 17 March 2016 /Accepted: 22 March 2016
#ISB 2016
Abstract Madeira Island is a famous tourist destination due to
its natural and climatic values. Taking into account optimal
weather conditions, flora richness and access to various sub-
strates facilitating fungal growth, we hypothesised a very high
risk of elevated fungal spore and pollen grain concentrations in
the air of Funchal, the capital of Madeira. Concentration levels
of the most allergenic taxa were measured from 2003 to 2009,
using a 7-day volumetric air sampler, followed by microscopy
analysis. Dependence of bioaerosols on the weather conditions
and land use were assessed using spatial and statistical tools.
Obtained results were re-visited by a comparison with hospital
admission data recorded at the Dr. Nélio Mendonça Hospital in
Funchal. Our results showed that despite propitious climatic
conditions, overall pollen grain and fungal spore concentra-
tions in the air were very low and did not exceed any clinically
established threshold values. Pollen and sporepeak concentra-
tions also did not match with asthma outbreaks in the winter.
Identification of places that are Bfree^from biological air pol-
lution over the summer, such as Madeira Island, is very impor-
tant from the allergic point of view.
Keywords Allergy .Aerobiology .Meteorological
parameters .Holiday .Circular statistics
Introduction
The triggering of respiratory allergic diseases is often related
with the occurrence of environmental bioaerosols. It is be-
lieved that the prevalence and severity of such disorders con-
tinue to increase. The changing environment and lifestyle are
considered significant causes for such increase. The alarming
increase in allergic disorders such as allergic rhinitis, bronchi-
al asthma and atopic dermatitis affects more than 30 % of the
population worldwide (Singh and Mathur 2012).
Asthma is a chronic disease of the airways characterised by
recurrent attacks of breathlessness and wheezing, which vary
in severity and frequency from person to person (To et al.
2012; WHO 2015). It is one of the most common chronic
diseases in the world that affects the general population.
Asthma causes a considerable burden to patients often
restricting their daily activities and quality of life, being also
an important cause of medical emergency visits and
hospitalisations (Galán et al. 2007; Héguy et al. 2008;
Masoli et al. 2004; Ruffoni et al. 2013).
A recent cross-sectional world health survey of asthma bur-
den in adults estimated that nearly 623 million individuals are
currently living with some level of asthma-related symptoms
(To et al. 2012). The prevalence of clinical asthma in the
Portuguese population is 4.8 %, and the rate of mortality is
6.9 % (Masoli et al. 2004). Comparatively to other countries,
the prevalence of asthma in childhood in Portugal is lower than
in many countries in South America or even in other former
Portuguese ex-colonies (Masoli et al. 2004). In Portugal, the
sensitisation prevalence to pollens is an important factor for
people with rhinitis and/or rhinoconjunctivitis allergic
Electronic supplementary material The online version of this article
(doi:10.1007/s00484-016-1163-6) contains supplementary material,
which is available to authorized users.
*Irene Camacho
camire@uma.pt
1
Life Science Competence Centre, Madeira University, Campus
Universitário da Penteada, 9000-390 Funchal, Portugal
2
Department of Plant Taxonomy and Phytogeography, University of
Szczecin, Wąska 13 Street, 71-415 Szczecin, Poland
3
Centro de Química da Madeira (CQM), Madeira University, Campus
Universitário da Penteada, 9000-390 Funchal, Portugal
4
Rothamsted Research, West Common, Harpenden AL5 2JQ, UK
Int J Biometeorol
DOI 10.1007/s00484-016-1163-6
aetiology. Studies of the prevalence of sensitivity to pollens
using skin prick tests revealed values ranging from 10 to
70 % (Loureiro et al. 2003). Most of the patients suffering from
hypersensitivity to pollen rhinitis are often associated with
conjunctivitis. The complaints of rhinoconjunctivitis are more
prevalent in the spring, especially from April to late June.
Although the genetic predisposition is essential for the de-
velopment of the allergic condition, the environment is impor-
tant in triggering hypersensitivity (Nunes and Ladeira 2012).
Asthma, in particular, is a heterogeneous disease caused by
multiple factors, and several studies have been focused on
environmental factors that may be associated with the risk of
developing such disease. Air pollution, pollen levels and me-
teorological variables have been the most studied parameters
(Brito et al. 2007; Héguy et al. 2008; Makra et al. 2015;Rosas
et al. 1998).
As such, there is a growing interest in the presence and
dispersion of bioaerosols in the atmosphere and their impact
on human health. Particles, such as pollen grains and fungal
spores, represent an important fraction of bioaerosol matter
being frequently implicated in allergic symptoms. Their pres-
ence in the atmosphere is directly affected by weather condi-
tions (Tormo-Molina et al. 2010), and for that reason, several
studies have emphasised the influence of meteorological pa-
rameters on airborne pollen and fungal spore concentration
and dispersion (e.g. Sadyśet al. 2015a).
Beyond the meteorological influence, the presence of these
airborne particles mainly depends on the kind of vegetation
growing in surrounding places, the season of the year and
plant phenology (D’Amato and Liccardi 1994). In addition,
pollen grains react with air pollution which in turn influences
plant allergenicity (Puc and Bosiacka 2011). Understanding
those correlations will help to prevent and manage allergic
diseases in general. Further, detailed information on the daily
and seasonal variations of bioaerosols is essential for an effec-
tive diagnosis and treatment of these ailments. A pollen dis-
tribution map throughout the Europe was described in detail in
the literature, reporting the pollen of Parietaria,olive,grass
and cypress as the most important ones for countries with the
Mediterranean climate, taking into account both their allergen-
ic properties and abundance in the air (D’Amato et al. 2007).
Fungal spores have also been considered as one of the
causes of allergic asthma (Newson et al. 2000) and for that
reason have been regularly monitored in several countries
(Abu-Dieyeh et al. 2010; Ataygul et al. 2007; Dixit et al.
2000;Gonianakisetal.2005; Sousa et al. 2015). Some studies
have included the fungal spore levels as a potential confound-
ing factor in respiratory diseases (Atkinson et al. 2006;Dales
et al. 2000;Newsonetal.2000), but few have considered the
influence of the geo-climatic features of each region in the
development and incidence of allergic disease. Madeira is
one of the most important touristic regions of Portugal. Its
natural environment is the strongest asset in attracting tourists,
accomplishing more than 1,010,000 tourists in 2005 (Oliveira
and Pereira 2008). Madeira belongs to Madeira Archipelago,
having edaphoclimatic conditions favourable to the occur-
rence of both pollen grains and fungal spores whose levels
might affect the local population and visitors.
Taking into account these considerations, we hypothesised
a very high risk of elevated fungal spore and pollen grain
concentrations in the air of Funchal, the capital of Madeira.
Fungal spores have been considered one of the causes of al-
lergic asthma (Newson et al. 2000) and a risk for emergency
hospital admissions, particularly in children (Atkinson et al.
2006). In view of these concerns, this study aimed to assess
the influence of the prevailing environmental and aerobiolog-
ical conditions in Madeira in the asthma symptoms burden.
Materials and methods
Site location, land use cover and climate
Madeira Archipelago is a volcanic group of islands located in
the AtlanticOcean about 500 km north of Canary Archipelago
and southwest of Portugal (Fig. 1). With 737 km
2
and about
240,000 people, Madeira is the biggest and the main island of
the Archipelago. Funchal is the main town of Madeira, and the
most populous insular city of the mainland (Portugal).
Madeira has a climate influenced by the subtropical anti-
cyclone of the Azores, with a temperate hyperoceanic sub-
Mediterranean bioclimate influence. By this reason and geo-
graphical location, Madeira has a subtropical climate with
Funchal within the thermo-sub-Mediterranean and thermo-
Mediterranean thermo-climatic belts (Rivas-Martínez 2001).
Relative humidity varies between 55 and 75 %, rainfall be-
tween 500 and 1000 mm and temperature between 15.9 °C in
February and 22.3 °C in August with an annual average of
18.7 °C (Quintal 2007). The predominant wind direction
varies from the South-West quadrant during the winter to the
North quadrant during the summer (Santos et al. 2004).
The main island is constituted in about two thirds of a nat-
ural park that includes the Laurel forest, locally called
Laurissilva, a UNESCO world heritage site being one of the
best-preserved forests of Macaronesia (Fig. 1). Gardens and
parks of Funchal have a variety of exotic plants (e.g.
Cupressaceae, Casuarina and tree ferns). Exotic species such
as genera Acacia,Eucalyptus and Pinus can be found surround-
ing Funchal. In urban areas, land for agriculture purposes (e.g.
banana—Musa acuminata and wine grapes—Vitis vinifera)
can also be found that makes a typical landscape of Funchal
and a potential substrate for fungal growth and reproduction.
A detailed analysis of the land use at Madeira was per-
formed using Global Land Cover 2000 (GLC2000) dataset
(EC 2003) and a combination of tools available in ArcMap
(v. 10.0) software.
Int J Biometeorol
Spore and pollen sampling
The airborne spore and pollen monitoring was performed with
a Burkard 7-day volumetric trap (Hirst type), from Jan. 2003
to Dec. 2009, following the guidelines of the International
Association for Aerobiology and the recommendations pro-
posed by the Spanish Aerobiology Network (Galán et al.
2007). The air sampler was placed on the roof of Dr. João
Almada Hospital in Funchal, 10 m above the ground (32°
39′N, 16° 55′W). The identification and counting of spores
and pollen grains were performed with a light microscope
(×400), based on four longitudinal transects along the slides
that resulted in scanning 13 % of the microscope slide.
Spore (Alternaria,Cladosporium) and pollen (Betulaceae,
Olea, Poaceae, Urticaceae) counts were converted into atmo-
spheric concentrations and expressed as the number of spores
[s m
−3
]orpollengrains[gm
−3
] per cubic metre of air. In order
to verify the accuracy of calculations performed under the
microscope, most of the samples were reviewed using a digital
camera connected to a computer screen. The calculations pre-
sented in this study were made based on the daily mean con-
centration of the airborne particles and the daily mean values
of the weather parameters that were available, i.e. maximum,
minimum and mean temperature; relative humidity; precipita-
tion; and wind direction. Meteorological data were provided
by the Portuguese Sea and Atmosphere Institute (IPMA),
Funchal, and covered the period from Jan. 2003 to Dec. 2009.
Emergency visits
The database containing patient history was produced since
Jun. 2005, and therefore, only the period overlapping with the
spore and pollen measurements was selected for a detailed
examination (Jun. 2005–Dec. 2009). Initially, patients who
reported symptoms similar to asthma during the registration
at the emergency room (ER) were selected. This group was
then narrowed down to patients who were located either at
pneumology, ENT (eyes, nose, throat), paediatrics, special
care unit and multipurpose intensive care unit departments;
who were sent back home; or who have died during the visit
at the hospital. All patients were then divided into three age
groups, i.e. children (0–15 years), adults (16–59 years) and
seniors (60–98 years) after Rosas et al. (1998).
Statistical testing
Seasonality of bioaerosol occurrence at Funchal was assessed
by calculating 90 % (spore) and 95 % (pollen) accumulative
daily mean concentration following Nilsson and Persson
(1981). Upon the preliminary pollen, spore, weather and asth-
ma admission rates through data screening with the aid of
descriptive statistics, Shapiro-Wilk test and matrix scatter
plots, it was necessary to apply non-parametric statistics for
further testing. All dependencies, i.e. (1) pollen and spore
concentration vs. weather, (2) number of emergency visits
vs. pollen and spore concentration, and (3) number of emer-
gency visits vs. meteorological parameters were examined
using Spearman’s rank test, while annual variations in
bioaerosol occurrence in the air and hospital admission rates
were studied using ANOVA Kruskal-Wallis test. All calcula-
tions were performed in GenStat (v. 17) software.
In addition to above, circular statistics was applied since
measurements of the local wind distribution represent a direc-
tional type of data (Aradóttir et al. 1997; Kasprzyk 2008).
Initial data screening was limited to descriptive statistical
tools, such as mean direction, circular standard deviation,
mean resultant length, skewness, kappa estimate, probability
test of randomness, probability Rayleigh test of uniformity,
Fig. 1 The maps show an elevation of Madeira Island (http://srtm.csi.
cgiar.org) with a location of sampling site (left) and land use (right)based
on the Global Land Cover 2000 (EC 2003). The following classes were
found: (1) mosaic—cropland, tree cover, and other natural vegetation
(light yellow); (2) tree cover, broadleaved, deciduous, open (dark green)
; (3) shrub cover, closed-open, evergreen (light green); (4) bare areas
(dark brown); (5) sparse herbaceous or sparse shrub cover (dark grey);
and (6) herbaceous cover, closed-open (beige). More details regarding
each land use class can be found at http://www.fao.org/docrep/003/
X0596E/x0596e01f.htm#p381_40252
Int J Biometeorol
chi-square von Mises and probability chi-square von Mises,
all available in Bcdescribe^package of the GenStat (v.17)
software (Fisher 1993). Subsequently, the annual variations
in local wind direction were investigated using Bccompare^
module containing tests for comparing circular distributions,
test for a common mean direction and test of homogeneity,
which jointly constitute an equivalent for the ANOVA
Kruskal-Wallis test for circular data (Fisher 1993). The
Bcassociation^module (Fisher 1993), which includes tests
for linear-circular association, was then used in order to study
the relationship between local wind direction and bioaerosol
distribution.
Results
Land use analysis
An analysis of the Madeira land use showed that the biggest
territory of the island was occupied by a mosaic consisted of
croplands, trees and other natural vegetation (62.93 %), while
the second most dominant land use class turned out to be
forest areas made of broadleaved, deciduous and open trees
15.82 % (Table 1,Fig.1).
Bioaerosol levels and their dependence on the weather
Overall, concentrations of all examined fungal spore and pol-
len grain genera, in the air of Funchal were very low (Table 2).
Results of ANOVA Kruskal-Wallis test showed that there was
a statistically significant difference (p<0.001) in annual dis-
tributions of spores, i.e. Alternaria (H= 29.78) and
Cladosporium (H= 74.56), as well as pollen, i.e. Betulaceae
(H=22.72), Olea (H= 9.88), Poaceae (H= 41.56 ) and
Urticaceae (H= 77.34). The Spearman ’s correlation coeffi-
cient value between both studied spore types was equal to
r
s
=0.446 (p<0.001).
The length of fungal spore seasons ranged from 199 to
321 days (Alternaria) and from 203 to 319 days
(Cladosporium)(Table2). Cladosporium spores were mainly
present in the air between January and November while
Alternaria from February to November. Commonly accepted
threshold values for triggering the asthma attacks at sensitised
individuals, i.e. 100 s m
−3
for Alternaria and 3000 s m
−3
for
Cladosporium (Table 3), within 7 years of study were not
exceeded at all. The maximum concentration of Alternaria
sporeswasobservedon14Nov.2009(60sm
−3
) while
Cladosporium spores peaked on 8 Oct. 2009 reaching
217 s m
−3
(Table 2).
Regarding the pollen grain genera, the pollen seasons
usually began in February–March and lasted till October–
November (Table 2). In general, Olea showed the shortest
pollen season (lasted on average 205 days), while
Urticaceae pollen seasons revealed the longest seasons
(on average 215 days). The first pollen peak concentra-
tions appeared with Urticaceae in March. Then,
Betulaceae pollen prevailed between April and May,
along with Urticaceae. The pollen of Poaceae reached
peaks intermittently, revealing maximum concentration
in April and June.
The maximum Urticaceae pollen concentrations were ob-
served in 2008 and 2009 on 7 April (45 g m
−3
) and on 28
March(44gm
−3
), respectively (Table 2). The second highest
maximum pollen concentrations were found for Betulaceae on
10April2009(31gm
−3
). Similarly, a clinically established
threshold value of 35 g m
−3
for grass pollen in Spain was
never exceeded (Tables 2and 3).
The presence of spores in the air was not directly dependent
on the changes of the weather conditions (Table 4). The cor-
relation coefficient values of the statistically significant rela-
tionships between Alternaria and meteorological parameters
was 0.072–0.075 (p≤0.05), while for Cladosporium −0.074–
0.095 (p≤0.05). In both cases, the most influencing factor was
found to be temperature while for Cladosporium,anequally
important factor was also rainfall. Furthermore, the correlation
analysis showed statistically significant values (p≤0.05) be-
tween most pollen types and meteorological parameters
(Table 4). The strongest correlation coefficient value between
meteorological parameters and Betulaceae was −0.040, for
Poaceae, it was varying from −0.047to0.039(p≤0.05),
whereas for Urticaceae, it ranged between −0.066 and
−0.049 (p≤0.05).
Emergency visits and their associations with weather
and bioaerosols
In the analysed period of time (Jun. 2005–Dec. 2009), 5143
patients with asthma symptoms were admitted to the hospital,
what constituted merely 3.04 % of the total number of regis-
tered patients in the emergency room at that time (Table 5,
Tabl e 1 Land use statistics for Madeira island based on the GLC2000
dataset
Land cover class Class no. Area (ha) Area (%)
Tree cover, broadleaved, deciduous,
open
3 2071 15.82
Shrub cover, closed-open, deciduous 12 831 6.35
Herbaceous cover, closed-open 13 71 0.54
Sparse herbaceous or sparse shrub
cover
14 641 4.90
Cropland/tree cover/other natural
vegetation
17 8236 62.93
Bare areas 19 1238 9.46
Total 13,088 100
Int J Biometeorol
Fig. 2). Results of ANOVA Kruskal-Wallis test showed that
there was a statistically significant difference in annual distri-
butions of a number of patients admitted to the hospital with
symptoms related to asthma, regardless whether year 2005
was included (H= 32.74, p<0.001)ornot(H= 10.81,
p< 0.01). The greatest number of cases was found in adults
group (49.19 %) and the lowest at children (16.92 %). Seven
death cases caused by asthma were found during analysed
period of time, and this concerned three women and four
men (Fig. 2).
In relation to the sex and age of all admitted patients, then
women at the age between 16 and 59 years old were more
frequently exhibiting asthma symptoms comparing to men
while this situation was reversed as men were found to be
more susceptible at child age and senior age. However, overall
there was not much difference between the gender ratio of all
Tabl e 2 Characteristics of fungal spore and pollen grain seasons at Funchal, Madeira (Jan. 2003–Dec. 2009)
Year 2003 2004
a
2005 2006 2007 2008
a
2009
Alternaria Start of season 25 Apr. 26 Feb. 12 Jan. 9 Mar. 1 Mar. 27 Feb. 11 Feb.
End of season 18 Nov. 11 Sep. 28 Nov. 18 Nov. 19 Dec. 8 Dec. 14 Nov.
Duration [ndays] 208 199 321 255 294 286 277
Peak value 8 23 8 5 42 30 60
Date of peak 27 Apr. 25 Mar. 16 Apr. 7 Aug. 15 Jul. 27 Apr. 14 Nov.
SFI 117 113 97 39 370 165 395
Cladosporium Start of season 25 Apr. 13 Jan. 8 Feb. 27 Apr. 19 Jan. 28 Jan. 19 Jan.
End of season 17 Nov. 19 Sep. 22 Nov. 15 Nov. 3 Dec. 22 Nov. 11 Nov.
Duration [ndays] 207 251 288 203 319 300 297
Peak value 190 43 117 122 104 183 217
Date of peak 26 Apr. 10 Mar. 11 Apr. 24 Jul. 28 Mar. 23 Apr. 8 Oct.
SFI 3829 1171 1821 1727 2270 2896 2155
Betulaceae Start of season 2 May 5 Feb. 5 Feb. 31 Mar. 5 Feb. 9 Mar. 12 Mar.
End of season 30 Nov. 22 Oct. 15 Oct. 1 Jul. 19 Aug. 26 Nov. 4 Oct.
Duration [ndays] 213 261 253 93 196 263 207
Peakvalue523841831
Date of peak 8 May 7 Apr. 27 Apr. 9 May 13 Jun. 14 May 10 Apr.
SPI 5630247842121511
Olea Start of season –11 Jan. 11 Jan. 6 Mar. 17 May 11 Jan. 4 Mar.
End of season –17 Jun. 17 Jun. 6 Nov. 26 Sep. 21 Oct. 6 Nov.
Duration [ndays] –159 158 246 133 285 248
Peak value –2232114
Date of peak –22 May 22 May 21 Jun. 17 May 11 Jan.
21 Oct.
07 Oct.
SPI 0761172 82
Poaceae Start of season 9 Jan. 11 Jan. 11 Jan. 6 May 12 Feb. 5 Apr. 16 Mar.
End of season 18 Dec. 12 Nov. 29 Nov. 2 Nov. 27 Dec. 7 Nov. 9 Nov.
Duration [ndays] 343 307 323 181 319 217 239
Peak value 5 9 9 39 9 31 28
Date of peak 30 Jun. 25 Jun. 25 Jun. 1 Sep. 28 Jun. 5 Apr. 4 Apr.
SPI 46 53 53 347 84 231 558
Urticaceae Start of season 24 Apr. 21 Jan. 23 Jan. 10 Mar. 27 Jan. 4 Mar. 15 Jan.
End of season 3 Aug. 10 Jul. 19 Nov. 2 Aug. 28 Nov. 27 Aug. 10 Nov.
Duration [ndays] 102 172 301 146 306 177 300
Peak value 12 6 8 33 24 45 44
Date of peak 24 Apr. 27 May 21 Apr. 10 Mar. 4 Mar. 7 Apr. 28 Mar.
SPI 158 171 237 225 159 361 828
SFI Seasonal Fungal Index (sum of the daily mean spore concentration within a season), SPI Seasonal Pollen Index (sum of the daily mean pollen grain
concentration within a season)
a
Leap year
Int J Biometeorol
registered patients, as women and men showed almost identi-
cal morbidity ratio (51:49).
A maximum daily number of emergency visits varied be-
tween six patients (at children group) and eight patients (at
adults group). On average, the greatest number of patients
with asthma-related symptoms were registered during the
winter period, i.e. in November (children, n=26), in
December (adults, n= 54) and in February (seniors, n=44),
(Fig. 3).
Figures 4,5, and 6show the annual distribution of the
number of emergency visits together with annual changes in
the total sum of daily mean pollen and spore concentrations
plotted against the annual mean air temperature, annual mean
relative humidity and annual sum of rainfall. These dependen-
cies were then further examined using Spearman’sranktest,
which showed that a number of hospital admissions related to
asthma symptoms were positively correlated with the pres-
ence of rainfall and negatively correlated with air temperature
(Table 4). None of the relationships between a number of
emergency visits and pollen and spore concentrations
(Table 6) was found to be statistically significant (p≤0.05).
Wind direction analysis
Table S1 shows results of the descriptive circular statistics
performed for the local wind direction that was measured at
Funchal, Madeira (Jan. 2003–Dec. 2009). The annual mean
wind direction remained constant throughout the period of the
first 6 years and oscillated from the SW to SE bearing
(Fig. S1). In 2009, the final year under investigation, the mean
wind direction was found to originate from the NNE direction
(Fig. S1). This discrepancy in annual wind direction pattern
was also confirmed by the Rayleigh’s test of uniformity
(Table S1). Similar findings were obtained by looking at other
circular parameters, for example, the circular dispersion; in
years 2003–2008, the circular dispersion was found to be
<27°, while in 2009, this value rose to 113°, thus it was >4
times higher than in the previous years.
Discussion and conclusion
The knowledge of the potentially allergenic pollen and spore
counts and their changes throughout the year in a given area is
of great importance for allergic persons and for the determi-
nation of the origins of the disease and recommendation of an
effective therapy. The production and distribution of such
bioaerosols are highly influenced by weather phenomena.
Taking into account the climatic conditions and land use of
Madeira Island (Table 1,Fig.S2), we hypothesised very high
levels of both fungal spores (Alternaria,Cladosporium)and
pollen grains (Betulaceae, Olea, Poaceae, Urticaceae) in the
air of Funchal. However, the overall concentration levels of all
selected bioaerosols throughout the period under investigation
Tabl e 3 Concentration levels of bioaerosol that trigger symptoms of
asthma
Bioaerosol Threshold
a
Country References
Alternaria 50 UK Frankland and Davies (1965)
80 Poland Rapiejko et al. (2007)
100 Finland Ranta and Pessi (2006)
Cladosporium 2800 Poland Rapiejko et al. (2007)
3000 UK Frankland and Davies (1965)
4000 Finland Ranta and Pessi (2006)
Betulaceae 70 France Caillaud et al. (2014)
75 Poland Rapiejko et al. (2007)
Olea 162 Spain Brito et al. (2011)
400 Spain Florido et al. (1999)
Poaceae 35 Spain Brito et al. (2010)
50 Poland Rapiejko et al. (2007)
50 Sweden Kiotseridis et al. (2013)
Urticaceae 80 Italy Negrini et al. (1992)
a
Expressed as number of fungal spores or pollen grains per cubic
metre of air
Tabl e 4 Results of Spearman’s
rank correlation test between
environmental factors and daily
number of emergency visits and
bioaerosol concentrations
measured at Funchal, Madeira
(2003–2009)
Bioaerosol TMAX TMIN TME RAIN RH WIND
a
Alternaria 0.075*0.072* 0.075* −0.015 0.033 0.000
Cladosporium 0.088* 0.084* 0.095* −0.074* 0.031 0.002
Betulaceae −0.033 −0.030 −0.020 −0.040* −0.022 0.000
Olea 0.008 0.009 0.011 0.018 0.038 0.000
Poaceae 0.173*0.187* 0.190* −0.047* 0.039* 0.000
Urticaceae −0.060* −0.066*−0.049* −0.034 0.022 0.000
Emergency visits −0.106* −0.093* −0.100* 0.015* −0.028 0.000
Abbreviations:TMAX maximum temperature (°C), TMIN minimum temperature (°C), TME mean temperature
(°C), RAIN rainfall (mm), RH relative humidity (%), WIND wind direction (°)
*Statistical significance at p≤0.05
a
Circular association test was used
Int J Biometeorol
were found to be very low (Table 2), and therefore, we had to
reject this hypothesis. None of them exceeded the threshold
values established clinically by several independent research
groups (Table 3), nor was statistically significantly correlated
with a number of patients admitted to the hospital (Table 6).
Given the timing when aeroallergenswere present inthe air of
sampling site (Table 2), as well as an increased frequency of
the hospital admissions during the winter period (Figs. 2and
3), it must be concluded that analysed aeroallergens were not
responsible for triggering the asthma attacks. Asthma is a
multifactorial disease, and for that reason, other factors be-
yond outdoor allergens, such as viral infections and exposure
to house dust mites, can cause asthma exacerbation and sub-
sequent hospital admissions (Ghosh et al. 2012;Global
Initiative for Asthma 2010; Hodder et al. 2010).
Furthermore, it was shown that a cold and dry weather in
autumn corresponded to increased asthma admissions and
peak days in admissions, in particularly at school-aged popu-
lation, whereas hot and dry weather in summer corresponded
to peak days in asthma admissions (Lee et al. 2012). Other
reports focusing on the relationshipbetween weather and asth-
ma revealed that increase in the asthma-related symptoms, as
well as the need for hospital admission, was associated with
dropping temperatures (May et al. 2011;D’Amato et al. 2015;
Royé et al. 2015). Breathing cold air can trigger
bronchoconstriction in asthmatics because physiological
mechanisms linked to the cooling of the airways can trigger
asthma symptoms (Koskela 2007;D’Amato et al. 2015).
These reports are in agreement with our findings presented
in Table 4.
Other studies conducted in countries with a similar climate
showed from at least twofold higher levels of pollen such as
Parietaria, which is one of the most important taxon of the
Urticaceae family (Negrini et al. 1992), to 18–33-fold higher
for Olea pollen (Tosunoglu and Bicakci 2015). These plants
are found only in specific regions: Parietaria and olive trees
are found mainly in the Mediterranean area. In turn, ragweed
grows predominantly in North America, birch occurs mainly
Tabl e 5 Asthma attacks at
different age groups of patients
at Funchal, Madeira
(Jun. 2005–Dec. 2009)
Group Year Total number
of cases
FMA
F
M
F
A
M
M
M
Children (0–15 years) 2005 89 29 60 8 9 8 9
2006 220 79 141 8 6 7 7
2007 212 77 135 8 7 8 7
2008 181 64 117 9 8 8 8
2009 168 70 98 8 8 8 8
Adults (16–59 years) 2005 235 154 81 38 39 39 41
2006 574 390 184 39 41 40 42
2007 595 345 250 40 41 39 38
2008 563 330 233 40 42 38 40
2009 563 287 276 38 38 39 43
Seniors (60–98 years) 2005 171 63 108 71 70 71 70
2006 447 198 249 74 73 73 72
2007 405 187 218 73 73 72 72
2008 361 164 197 72 72 72 72
2009 359 176 183 71 70 71 71
Abbreviations:Ffemale, Mmale, A
F
female average age, M
F
female median age, A
M
male average age, M
M
male
median age
0
10000
20000
30000
40000
50000
2005 2006 2007 2008 2009
[n]
Year
Admissions with asthma symptoms All admissions
86%
88%
90%
92%
94%
96%
98%
100%
2005 2006 2007 2008 2009
Yea r
Return to home Hospitalisation Death
Fig. 2 Relation between the total number of hospital admissions and emergency visits with asthma symptoms (left) and further consequences of the
latter group (right) recorded at Funchal, Madeira (Jun. 2005–Dec. 2009)
Int J Biometeorol
in the NW Europe (Emberlin et al. 2002) and the Japanese
cedar is restricted to Japan (D’Amato 2007). Despite the oc-
currence of some of these allergenic taxa in Madeira Island,
their concentration levels in the atmosphere are considered as
low (Camacho 2015). Poaceae pollen also occurs in Madeira,
which is considered as an important causal agent of asthma in
Europe and a dominant element in the herbaceous vegetation
of the Mediterranean landscape (Rodríguez-Rajo et al. 2010).
Grasses are both annual and perennial herbs and most species
are anemophilous (León-Ruiz et al. 2010) producing large
amounts of pollen grains during a short period of time
(Knox et al. 1993). Beyond these features, Poaceae pollen
season is quite long; however, this pollen type occurs in the
atmosphere of Madeira in low levels (Table 2).
In contrast, the spore counts of Alternaria and
Cladosporium recorded at Funchal were similar to those re-
ported for the Trent region (Newson et al. 2000). However, the
annual average of Alternaria (185.30) and Cladosporium
(2266.92) in the atmosphere of Funchal is easily surpassed
by fungal spore counts detected in Thessaloniki (Greece)
(Gioulekas et al. 2004)orinMadrid(Spain),wherethe
monthly concentrations were always above 3000 s m
−3
during
every month of the year (Sabariego et al. 2007). The coastal
proximity of Funchal city, as well as the insular condition of
Madeira, might explain the low fungal spore levels, a phe-
nomenon also observed in other regions (Aira et al. 2008;
Belmonte et al. 2008). In fact, the geographical position of a
given region along with the meteorological elements is an
important factor that drives bioaerosol dispersal (Veriankaitė
et al. 2010).
In Fig. 2, annual fluctuations in hospital admission num-
bers were presented. In Jun. 2005, the patient database was
created, and therefore, this particular year represented only 6-
month observation in contrast to the following years. Hence,
the real lowest number of registered patients exhibiting asth-
ma symptoms occurred in 2009, and it was equal to n=1090
(Fig. 2). The highest number of admitted patients with signs of
asthma was found in 2006. The data did not show a visible
upward or downward trend with regard to the overall number
of emergency visits while specifically admissions in relation
to the asthma outbreaks showed a gradual decrease of 14 %
from 2006 to 2009. Similar results were reported by the
Global Asthma Network (2014) for Portugal, where 2000–
2004 data was compared with 2008–2012. In contrast to
Portugal, in many European countries, like Netherlands,
Croatia, Germany or Lithuania, it has been observed a signif-
icant increase in hospital admission rates between 2008 and
2012 (Global Asthma Network (2014). Other countries of a
Mediterranean climate also exhibited a decrease in numbers of
registered asthma sufferers. In such type of surveys, special
attention has been given to the child population. The rates of
asthma attacks involving children are normally higher than in
the adults (Atkinson et al. 2006; Dales et al. 2000; Galán et al.
2003). Nevertheless, in Madeira, during the period of study, a
0
10
20
30
40
50
60
Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec
[n]
Month
Children Adults Seniors
0
10
20
30
40
50
60
70
80
06/2005
08/2005
10/2005
12/2005
02/2006
04/2006
06/2006
08/2006
10/2006
12/2006
02/2007
04/2007
06/2007
08/2007
10/2007
12/2007
02/2008
04/2008
06/2008
08/2008
10/2008
12/2008
02/2009
04/2009
06/2009
08/2009
[n]
Month and year
Children Adults Seniors
Fig. 3 Mean monthly sums of
the emergency visits of patients
with asthma-related symptoms
(top) and actual numbers of the
emergency visits recorded at
Funchal, Madeira between Jun.
2005 and Dec. 2009 (bottom)
Int J Biometeorol
maximum daily number of emergency visits of six children
and eight adults were reported contrasting with rates ranging
from 0 to 36 visits per day, 8.8 % of which caused by fungal
spores (Dales et al. 2000).
Another common feature isthe seasonal pattern in the num-
ber of asthma events. In a survey conducted by Leblanc et al.
(2013) in an emergency hospital department at Lisbon
(Portugal), it was shown that months with the highest visits
of asthmatic patients occurred at the end of spring time. The
authors explained that some exacerbations episodes could be
due to exposure to environmental allergens, as in the case of
patients sensitised to pollens. A similar scenario was observed
inPortocity(Ribeiroetal.2009) where tree pollen and hos-
pital admissions for asthma or dyspnea were positively corre-
lated. In the particular case of our survey, we have not found
an association between daily emergency visits from asthma
and the periods when pollen or fungal spore allergens
prevailed in the atmosphere. Further, we did not observe a
periodical pattern in asthma hospital admissions, suggesting
that the onset of asthma symptoms could be linked to other
variables, namely the genetic background and lifestyle of the
population, as suggested by Rosado-Pinto et al. (2006).
18.00
18.50
19.00
19.50
20.00
20.50
0
300
600
900
1200
2005 2006 2007 2008 2009
[°C]
[s m
-3
] / [n]
Asthma emergency visits Alternaria Mean temperature
18.00
18.50
19.00
19.50
20.00
20.50
0
500
1000
1500
2000
2500
3000
3500
2005 2006 2007 2008 2009
[°C]
[s m
-3
] / [n]
Asthma emergency visits Cladosporium Mean temperature
18.00
18.50
19.00
19.50
20.00
20.50
0
300
600
900
1200
2005 2006 2007 2008 2009
[°C]
[s m
-3
] / [n]
Asthma emergency visits Betulaceae Mean temperature
18.00
18.50
19.00
19.50
20.00
20.50
0
300
600
900
1200
2005 2006 2007 2008 2009
[°C]
[s m
-3
] / [n]
Asthma emergency visits Olea Mean temperature
18.00
18.50
19.00
19.50
20.00
20.50
0
300
600
900
1200
2005 2006 2007 2008 2009
[°C]
[s m-3] / [n]
Asthma emergency visits Parietaria Mean temperature
18.00
18.50
19.00
19.50
20.00
20.50
0
300
600
900
1200
2005 2006 2007 2008 2009
[°C]
[s m
-3
] / [n]
Asthma emergency visits Poaceae Mean temperature
18.00
18.50
19.00
19.50
20.00
20.50
0
300
600
900
1200
2005 2006 2007 2008 2009
[°C]
[s m
-3
] / [n]
Asthma emergency visits Urticaceae Mean temperature
Fig. 4 Associations between examined fungal spores (Seasonal Fungal Indices) and pollen grains (Seasonal Pollen Indices), annual mean air
temperature and number of asthma-related emergency visits recorded at Funchal, Madeira Island (Jun. 2005–Dec 2009)
Int J Biometeorol
An overview of the weather changes was given in Fig. S2
and Tables 4and 6. Air temperature and relative humidity are
the major factors that governfungal spore production and their
release mechanisms; for instance, the optimal temperature for
Alternaria brassicae and A. brassicicola sporulation require
18–24 °C and 20–30 °C, respectively, and 87–92 % of relative
humidity (Humperson-Jones and Phelps 1989). Although
these conditions matched, the Alternaria spore counts were
rarely observed in the air of Funchal (Table 3). However, the
impact of climate change on bioaerosol concentrations is not
yet fully understood; some authors suggest a decline in future
spore concentration and hence a decreasing number of emer-
gency visits caused by asthma (Damialis et al. 2015; Sadyś
et al. 2015b). Graphs presented in Fig. S2 uniformly showed a
gradual increase in mean air temperature, relative humidity
and precipitation at Madeira Island.
Although the climate change must be partly responsible for
low bioaerosol concentrations in the air of Funchal, it does not
entirely explain the observed phenomenon. Noteworthy is the
fact that major wind directions observed throughout the year
were coming from the SWand SE directions (Fig. S2). The air
masses blowing from the south originated over the Atlantic
50.00
55.00
60.00
65.00
70.00
0
300
600
900
1200
2005 2006 2007 2008 2009
[%]
[s m
-3
] / [n]
Asthma emergency visits Alternaria RH
50.00
55.00
60.00
65.00
70.00
0
500
1000
1500
2000
2500
3000
3500
2005 2006 2007 2008 2009
[%]
[s m
-3
] / [n]
Asthma emergency visits Cladosporium RH
50.00
55.00
60.00
65.00
70.00
0
300
600
900
1200
2005 2006 2007 2008 2009
[%]
[s m
-3
] / [n]
Asthma emergency visits Betulaceae RH
50.00
55.00
60.00
65.00
70.00
0
300
600
900
1200
2005 2006 2007 2008 2009
[%]
[s m
-3
] / [n]
Asthma emergency visits Olea RH
50.00
55.00
60.00
65.00
70.00
0
300
600
900
1200
2005 2006 2007 2008 2009
[%]
[s m
-3
] / [n]
Asthma emergency visits Parietaria RH
50.00
55.00
60.00
65.00
70.00
0
300
600
900
1200
2005 2006 2007 2008 2009
[%]
[s m
-3
] / [n]
Asthma emergency visits Poaceae RH
50.00
55.00
60.00
65.00
70.00
0
300
600
900
1200
2005 2006 2007 2008 2009
[%]
[s m
-3
] / [n]
Asthma emergency visits Urticaceae RH
Fig. 5 Associations between examined fungal spores (Seasonal Fungal Indices) and pollen grains (Seasonal Pollen Indices), annual mean relative
humidity (RH) and number of asthma-related emergency visits recorded at Funchal, Madeira Island (Jun 2005–Dec 2009)
Int J Biometeorol
Ocean and, therefore, must be free from any biological mate-
rial, as suggested by Urbano et al. (2011). A previous survey
performed by McGregor et al. (1999) revealed that cold and
maritime air masses could be used as a predictor for a decrease
in the number of emergency visits related to the respiratory
tract infections since they were associated with a decline in air
pollution. In contrast, the air masses arriving from the NNE
bearing in 2009, although they originated on the African con-
tinent, they did not contribute significantly towards the pollen
and spore counts trapped in Funchal due tothe lack of suitable
sources (Table 2, Fig. S1).
450.00
550.00
650.00
750.00
0
300
600
900
1200
2005 2006 2007 2008 2009
[mm]
[s m
-3
] / [n]
Asthma emergency visits Alternaria Rain
450.00
550.00
650.00
750.00
0
500
1000
1500
2000
2500
3000
3500
2005 2006 2007 2008 2009
[mm]
[s m
-3
] / [n]
Asthma emergency visits Cladosporium Ra in
450.00
550.00
650.00
750.00
0
300
600
900
1200
2005 2006 2007 2008 2009
[mm]
[s m
-3
] / [n]
Asthma emergency visits Betulaceae Rain
450.00
550.00
650.00
750.00
0
300
600
900
1200
2005 2006 2007 2008 2009
[mm]
[s m
-3
] / [n]
Asthma emergency visits Olea Rain
450.00
550.00
650.00
750.00
0
300
600
900
1200
2005 2006 2007 2008 2009
[mm]
[s m
-3
] / [n]
Asthma emergency visits Parietaria Rain
450.00
550.00
650.00
750.00
0
300
600
900
1200
2005 2006 2007 2008 2009
[mm]
[s m
-3
] / [n]
Asthma emergency visits Poaceae Rain
450.00
550.00
650.00
750.00
0
300
600
900
1200
2005 2006 2007 2008 2009
[mm]
[s m
-3
] / [n]
Asthma emergency visits Urticaceae Rain
Fig. 6 Associations between the examined fungal spores (Seasonal Fungal Indices) and pollen grains(Seasonal Pollen Indices), annual precipitation and
number of asthma-related emergency visits recorded at Funchal, Madeira Island (Jun. 2005–Dec. 2009)
Tabl e 6 Results of
Spearman’srank
correlation test between
daily emergency visits
and bioaerosol
concentrations measured
at Funchal, Madeira
(Jun 2005–Dec 2009)
Bioaerosol Emergency visits
Alternaria 0.014
Cladosporium −0.047
Betulaceae −0.029
Olea −0.011
Poaceae −0.041
Urticaceae −0.036
*Statistical significance at p≤0.05
Int J Biometeorol
In the end, a very low numbers of the pollen grain and
fungal spore concentrations with allergenic properties record-
ed in Funchal from spring to autumn suggest that Madeira
Island can be considered as a safe touristic destination for
allergic sufferers.
Acknowledgments We would like to thank the Unit of Management of
Patients and Statistic of Hospital Central of Funchal, the Portuguese
Society of Allergology and Clinical Immunology (SPAIC) and the
Meteorological Observatory of Funchal for their help and support in the
aerobiological study.
References
Abu-Dieyeh MH, Barham R, Abu-Elteen K, Al-Rashidi R, Shaheen I
(2010) Seasonal variation of fungal spore populations in the atmo-
sphere of Zarqa area, Jordan. Aerobiologia 26:263–276
Aira MJ, Rodríguez-Rajo FJ, Jato V (2008) 47 annual records of aller-
genic fungi spore: predictive models from the NW Iberian
Peninsula. Ann Agric Environ Med 15:91–98
Aradóttir AL, Robertson A, Moore E (1997) Circular statistical anal-
ysis of birch colonization and the directional growth response of
birch and black cottonwood in south Iceland. Agric For
Meteorol 84:179–186
Asthma GIf (2010) Global strategy for asthma prevention. National
Institutes of Health, National Heart, Lung, and Blood Institute,
Bethesda
Ataygul E, Celenk S, Canitez Y, Bicakci A, Malyer H, Sapan N (2007)
Allergenic fungal spore concentrations in the atmosphere of Bursa,
Turkey. J Biol Environ Sci 1:73–79
Atkinson RW, Strachan DP, Anderson HR, Hajat S, Emberlin J (2006)
Temporal associations between daily counts of fungal spores and
asthma exacerbations. Occup Environ Med 63:580–590
Belmonte J, Puigdemunt R, Cuevas E, Alonso S, González R, Poza P et al
(2008) Eolo-PAT project: aerobiology and respiratory allergies in
Santa Cruz de Tenerife since 2004. Allergy 63:58–611
Brito FF, Gimeno PM, Martínez C, Tobías A, Suárez L, Guerra F et al
(2007) Air pollution and seasonal asthma during the pollen season.
A cohort study in Puertollano and Ciudad Real (Spain). Allergy 62:
1152–1157
Brito FF, Mur Gimeno P, Carnés J, Fernández-Caldas E, Lara P,
Alonso AM et al (2010) Grass pollen, aeroallergens, and clinical
symptoms in Ciudad Real, Spain. J Investig Allergol Clin
Immunol 20:295–302
Brito FF, Gimeno PM, Carnés J, Martín R, Fernández-Caldas E, Lara P
et al (2011) Olea europaea pollen counts and aeroallergen levels
predict clinical symptoms in patients allergic to olive pollen. Ann
Allergy Asthma Immunol 106:146–152
Caillaud D, Martin S, Segala C, Besancenot JP, Clot B, Thibaudon M
(2014) Effects of airborne birch pollen levels on clinical symptoms
of seasonal allergic rhinoconjunctivitis. Int Arch Allergy Immunol
163:43–50
Camacho IC (2015) Airborne pollen in Funchal city, (Madeira Island,
Portugal)—first pollinic calendar and allergic risk assessment. Ann
Agric Environ Med 22(4):608–613
D’Amato G (2007) Pollen allergy in Europe. The UCB Institute of
Allergy 1–12
D’Amato G, Liccardi G (1994) Pollen related allergy in the European
Mediterranean area. Clin Exp Allergy 24:210–219
D’Amato G, Cecchi L, Bonini S, Nunes C, Annesi-Maesano I, Behrendt
H et al (2007) Allergenic pollen and pollen allergy in Europe.
Allergy 62:976–990
D’Amato G, Holgate ST, Pawankar R, Ledford DK, Cecchi L, Al-Ahmad
M et al (2015) Meteorological conditions, climate change, new
emerging factors, and asthma and related allergic disorders. A state-
ment of the world allergy organization. World Allergy Organ J 8:25
Dales RE, Cakmak S, Burnett RT, Judek S, Coates F (2000) Influence of
ambient fungal spores on emergency visits for asthma to a regional
children’s hospital. Am J Respir Crit Care Med 162:2087–2090
Damialis A, Mohammad AB, Halley JM, Gange AC (2015) Fungi in a
changing world: growth rates will be elevated, but spore production
may decrease in future climates. Int J Biometeorol 59:1157–1167
Dixit A, Lewis W, Baty J, Crozier W, Wedner J (2000) Deuteromycete
aerobiology and skin-reactivity patterns. Grana 39:209–218
EC (2003) Global land cover 2000 database. In: Joint Research Centre
EC, editor, Ispra
Emberlin J, Detandt M, Gehrig R, Jaeger S, Nolard N, Rantio-Lehtimäki
A (2002) Responses in the start of Betula (birch) pollen seasons to
recent changes in spring temperatures across Europe. Int J
Biometeorol 46:159–170
Fisher NI (1993) Statistical analysis of circular data. University Press,
Cambridge
Florido JF, Delgado PG, de San Pedro BS, Quiralte J, de Saavedra JM,
Peralta V et al (1999) High levels of Olea europaea pollen and
relation with clinical findings. Int Arch Allergy Immunol 119:
133–137
Frankland AW, Davies RR (1965) Allergy to mold spores in England.
Poumon Coeur 21:11–31
Galán C, Tobías A, Banegas JR, Aránguez E (2003) Short-term effects of
air pollution on daily asthma emergency room admissions. Eur
Respir J 22:802–808
Galán C, Cariñanos P, Alcázar P, Dominguez E (2007) Spanish aerobiol-
ogy network (REA): management and quality manual. Universidad
de Córdoba, Córdoba
Ghosh D, Chakraborty P, Gupta J, Biwas A, Roy I, Das S et al (2012)
Associations between pollen counts, pollutants, and asthma-related
hospital admissions in a high-density Indian metropolis. J Asthma
49:792–799
Gioulekas D,Damialis A, Papakosta D, Spieksma F, Giouleka P, Patakas
D (2004) Allergenic fungi spore records (15 years) and sensitization
in patients with respiratory allergy in Thessaloniki-Greece. J Invest
Allerg Clin 14:225–231
Global Asthma Network. The global asthma report 2014. 2014 [cited;
Ava ilable fr om : http://www.globalasthmareport.org/resources/
Global_Asthma_Report_2014.pdf
Gonianakis M, Neonakis I, Darivianaki E, Gonianakis I, Bouros D,
Kontou-Fili K (2005) Airborne Ascomycotina on the island of
Crete: seasonal patterns based on an 8-year volumetric survey.
Aerobiologia 21:69–74
Héguy L, Garneau M, Goldberg MS, Raphoz M, Guay F, Valois M-F
(2008) Associations between grass and weed pollen and emergency
department visits for asthma among children in Montreal. Environ
Res 106:203–211
Hodder R, Lougheed MD, Rowe BH, Fitzgerald JM, Kaplan AG, McIvor
RA (2010) Management of acute asthma in adults in the emergency
department: nonventilatory management. CMAJ 182:E55–E67
Humperson-Jones FM, Phelps K (1989) Climatic factors influencing
spore production in Alternaria brassicae and Alternaria
brassicicola. Ann Appl Biol 114:449–458
Kasprzyk I (2008) Non-native Ambrosia pollen in the atmosphere of
Rzeszow (SE Poland). Evaluation of the effect of weather conditions
on daily concentrations and starting dates of the pollen season. Int J
Biometeorol 52:341–351
Kiotseridis H, Cilio CM, Bjermer L, Tunsäter A, Jacobsson H, Dahl Å
(2013) Grass pollen allergy in children and adolescents symptoms,
health related quality of life and the value of pollen prognosis. Clin
Transl Allergy 3:19
Int J Biometeorol
Knox RB, Taylor P, Smith P, Hough T, Ong EK, Suphioglu C et al (1993)
Pollen allergens, botanical aspects. In: Kraft D, Sehon A (eds)
Molecular biology and immunology of allergens. CRC Press,
Boca Raton, pp 31–34
Koskela HO (2007) Cold air-provoked respiratory symptoms: the mech-
anisms and management. Int J Circumpolar Health 66(2):91–100
Leblanc A, Silva R, Dias de Castro E (2013) Asthmatic admissions in a
central hospital emergency department. Rev Port Imunoalergologia
21:275–282
Lee CC, Sheridan SC, Lin S (2012) Relating weather types to
asthma-related hospital admissions in New York State.
EcoHealth 9:427–439
León-Ruiz E, Alcázar P, Domínguez-Vilches E, Galán C (2010) Study of
Poaceae phenology in a Mediterranean climate. Which species con-
tribute most to airborne pollen counts? Aerobiologia 27:37–50
Loureiro G, Blanco B, São Braz M, Pereira C (2003) Reactividade
cruzada a aeroalergénios numa população alérgica da Cova da
Beira. Rev Port Imunoalergologia 11:107–116
Makra L, Puskás J, Matyasovszky I, Csépe Z, Lelovics E, Bálint B,
Tusnády G (2015) Weather elements, chemical air pollutants and
airborne pollen influencing asthma emergency room visits in
Szeged, Hungary: performance of two objective weather classifica-
tions. Int J Biometeorol 59(9):1269–1289
Masoli M, Fabian D, Holt S, Beasley R (2004) The global burden of
asthma: executive summary of the GINA Dissemination
Committee Report. Allergy 59:469–478
May L, Carim M, Yadav K (2011) Adult asthma exacerbations and envi-
ronmental triggers; a retrospective review of ED visits using an
electronic medical record. Am J Emerg Med 29:1074–1082
McGregor G, Walters S, Wordley J (1999) Daily hospital respiratory
admissions and winter air-mass types, Birmingham UK. Int J
Biometeorol 43:21–30
Negrini AC, Voltolini S, Troise C, Arobba D (1992) Comparison between
Urticaceae (Parietaria) pollen count and hay fever symptoms: as-
sessment of a «threshold-value». Aerobiologia 8:325–329
Newson R, Strachan D, Corden J, Millington W (2000) Fungal and other
spore counts as predictors of admissions for asthma in the Trent
region. Occup Environ Med 57:786–792
Nilsson S, Persson S (1981) Tree pollen spectra in the Stockholm region
(Sweden), 1973–1980. Grana 20:179–182
Nunes C, Ladeira S (2012) Long-term efficacy of specific immunothera-
py in rhino-conjunctivitis to pollens. Rev Port Imunoalergologia 20:
253–261
Oliveira P, Pereira PT (2008) Who values what in a tourism destination?
The case of Madeira Island. Tour Econ 14:155–168
Puc M, Bosiacka B (2011) Effects of meteorological factors and air
pollution on urban pollen concentrations. Pol J Environ Stud 20:
611–618
Quintal R (2007) Quintas, Parques e Jardins do Funchal - Estudo
fitogeográfico. Lisboa: Esfera do Caos Editores
Ranta H, Pessi A-M (2006) Pollen bulletin summary 2005. Finn Pollen
Bull 30:1–12
Rapiejko P, Stankiewicz W, Szczygielski K, Jurkiewicz D (2007)
Threshold pollen count necessary to evoke allergic symptoms.
Otolaryngol Pol 61:591–594
Ribeiro H, Oliveira M, Ribeiro N, Cruz A, Ferreira A, Machado H,
Reis A, Abreu I (2009) Pollen allergenic potential nature of
some trees species: a multidisciplinary approach using aerobio-
logical, immunochemical and hospital admissions data. Environ
Res 109(3):328–333
Rivas-Martínez S (2001) Bioclimatic map of Europe—thermotypes.
University of Léon, Léon
Rodríguez-Rajo FJ, Astray G, Ferreiro-Lage JA, Aira MJ, Jato-Rodríguez
MV, Mejuto JC (2010) Evaluation of atmospheric Poaceae pollen
concentration using a neural network applied to a coastal Atlantic
climate region. Neural Netw 23:419–425
Rosado-Pinto J, Gaspar A, Morais-Almeida M (2006) Épidémiologie de
l’asthme et des allergies dans les pays de langue portugaise. Revue
Française d’allergologie et d’immunologie Clinique 46:305–308
Rosas I, McCartney HA, Payne RW, Calderón C, Lacey J, Chapela R et al
(1998) Analysis of the relationships between environmental factors
(aeroallergens, air pollution, ad weather) and asthma emergency to a
hospital in Mexico City. Allergy 53:394–401
Royé D, Taboada JJ, Martín A, Lorenzo MN (2015) Winter circulation
weather types and hospital admissions for respiratory diseases in
Galicia, Spain. Int J Biometeorol. doi:10.1007/s00484-015-1047-1
Ruffoni G, Passalacqua G, Ricciardolo F, Furgani A, Corrado Negrini A,
De Amici M et al (2013) A 10-year survey on asthma exacerbations:
relationships among emergency medicine calls, pollens, weather,
and air pollution. Rev Fr Allergol 53:569–575
SabariegoS, Díez A, Gutiérrez M (2007) Monitoring of airborne fungi in
Madrid (Spain). Acta Bot Croat 66:117–126
SadyśM, Kennedy R, Skjoth CA (2015a) An analysis of local wind and
air mass directions and their impact on Cladosporium distribution
using HYSPLIT and circular statistics. Fungal Ecol 18:56–66
SadyśM, Kennedy R, West JS (2015b) Potential impact of climate
change on fungal distributions: analysis of 2 years of contrasting
weather in the UK. Aerobiologia
Santos FD, Valente MA, Miranda PMA, Aguiar A, Azevedo EB, Tomé
AR et al (2004) Climate change scenarios in the Azores and Madeira
islands. WRR 16:473–491
Singh AB, Mathur C (2012) An aerobiological perspective in allergy and
asthma. Asia Pac Allergy 2:210–222
Sousa L, Camacho I, Grinn-GofrońA, Camacho R (2015) Monitoring of
anamorphic fungal spores in Madeira region (Portugal), 2003–2008.
Aerobiologia 31:1–13
To T, Stanojevic S, Moores G, Gershon AS, Bateman ED, Cruz AA et al
(2012) Global asthma prevalence in adults: findings from the cross-
sectional world health survey. BMC Public Health 12:1–8
Tormo-Molina R, Gonzalo-Garijo MA, Silva-Palacios I, Muñoz-
Rodríguez AF (2010) General trends in airborne pollen production
and pollination periods at a Mediterranean site (Badajoz, Southwest
Spain). J Investig Allergol Clin Immunol 20:567–574
Tosunoglu A, Bicakci A (2015) Seasonal and intradiurnal variation of
airborne pollen concentrations in Bodrum, SW Turkey. Environ
Monit Assess 187:167
Urbano R, Palenik B, Gaston CJ, Prather KA (2011) Detection and phy-
logenetic analysis of coastal bioaerosols using culture dependent
and independent techniques. Biogeosciences 8:301–309
VeriankaitėL, Siljamo P, Sofiev M, ŠaulienėI, Kukkonen J (2010)
Modelling analysis of source regions of long-range transported birch
pollen that influences allergenic seasons in Lithuania. Aerobiologia
26:47–62
WHO. Asthma, http://www.who.int/topics/asthma/en/,2015
Int J Biometeorol