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Urban Forestry & Urban Greening xxx (xxxx) xxx–xxx

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Urban Forestry & Urban Greening

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Combined effects of air pollution and allergens in the city of Rome

Alessandro Di Menno di Bucchianicoa, , Maria Antonia Brighettib, Giorgio Cattania,
Corrado Costac, Mariacarmela Cusanoa, Vincenzo De Gironimoa, Francesca Froiod,
Raffaela Gaddia, Simone Pelosie, Ifigenia Sfikaf, Alessandro Travaglinib, Salvatore Tripodif
ISPRA, Italian National Institute for Environmental Protection Research, Italy
Department of Biology, University of Rome Tor Vergata, Rome, Italy
Engineering and Agri-Food Processing Research Center, Monterotondo (Rm), Italy
Allergology Centre, San Pietro-Fatebenefratelli Hospital, Rome, Italy
TPS Production srl, Italy
Pediatric Department & Allergology Service, Sandro Pertini Hospital, Rome, Italy


Keywords: Urban green is an important aspect in the quality of life of citizens of modern cities. Nevertheless some orna-
PM10 mental plants cause allergic diseases in sensitive subjects that may be worsened by air pollution.
Atmospheric pollution Studies on air quality are usually addressed to the evaluation of single substances and their specific effects:
Pollen little is known about the cumulative effect that different pollutants may have on human health. Even less is
Urban areas
known about possible combined action of traditional air pollutants with pollen and spores that have huge effects,
Health effects
in terms of allergies and asthma, on citizenship of the urban areas.
In this work the synergistic effect of PM10, PM2.5, NO2, O3 and airborne pollens (belonging to 4 taxa:
Cupressaceae/Taxaceae, Graminaceae, Olea and Urticaceae) was studied in the city of Rome during six years
(from 2010 to 2015).
For air pollutants, concentration values recorded by air-quality monitoring network of Rome were used.
Pollens and spores data were detected by the Aerobiological Monitoring Centre of the University of Rome Tor
Vergata. Effects on human health were evaluated on a group of 100 patients (aged between 4 and 18) by the
Allergymonitor™ã application that records daily symptoms of hay fever, bronchial asthma and the prescribed
Data collected in the medical record were processed by 2 different Symptom Medication daily Scores and
compared with time series of air concentration of mentioned pollutants, pollen and spores.
Statistical analysis allowed highlighting when concomitant high levels of allergenic species and air pollution
occur, the influence of meteorological parameters, of the flowering calendar, of taking drugs and how these
aspects affect symptoms in patients.

1. Introduction (IG, 1988), abrogated and replaced the previous law and introduced
limit values (or air quality standards) and guide values.
Atmospheric pollution, especially in urban areas, is, nowadays, To protect human health from acute episodes of air pollution, two
generally considered an important risk factor for human health and the 1994 Ministry Decrees established attention and alert standards for the
ecosystem, but the consciousness of its importance has gradually in- same substances (IG, 1994a,b).
creased during the last decades, following the progress of scientific Specifically, the 25/11/94 Ministry Decree (IG, 1994b) introduced
research. quality objectives for the, at time so-called, unconventional pollutants
The first Italian act on air pollution was the 1966 Anti-smog law n. (PM10, Benzene, Benzo[a]pyrene).
615 (IP, 1966), followed by the 1971 executive regulation (IG, 1971) Finally, a 1996 Ministry Decree introduced specific reference levels
which provided the first concentration limits in the ambient air for for tropospheric ozone (IG, 1996).
many substances. In the late nineties was issued the European Framework Directive
The 1983 Decree (IG, 1983), updated in 1988 with the DPR n. 203 for air quality (EC, 1996) and then a number of daughter directives

Corresponding author at: ISPRA, Italian National Institute for Environmental Protection and Research, Via Vitaliano Brancati, 48, Rome, 00144, Italy.
E-mail address: (A. Di Menno di Bucchianico).
Received 31 July 2017; Received in revised form 29 January 2018; Accepted 1 April 2018
1618-8667/ © 2018 Elsevier GmbH. All rights reserved.

Please cite this article as: Di Menno di Bucchianico, A., Urban Forestry & Urban Greening (2018),
A. Di Menno di Bucchianico et al. Urban Forestry & Urban Greening xxx (xxxx) xxx–xxx

addressed to specific pollutants. All these directives were gradually membranes and greater interaction with immune system cells (D’Amato
transposed in Italy since 1999. et al., 2007). In addition, some air pollution components seem to have
The current European Directives on ambient air quality are the an adjuvant immunological effect on the synthesis of immunoglobulin E
2004/107/EC (EC, 2004) and the 2008/50/EC (EC, 2008) and these (IgE) in atopic subjects: for each increase of 10 μg/m3 of PM10 the risk
were both transposed and merged in Italy by the 2010 D. Lgs. n. 155 of hospitalization or first aid visits increases by 1.5% and to worsen
(IG, 2010). asthma increases by 3% (Pope et al., 1999). Another study has high-
The European Union adopted the 2008/50/EC Directive on ambient lighted that by crossing the data from the wastewater analysis of the
air quality and cleaner air for Europe in order to protect human health average number of daily doses consumed in the city of Milan and those
and the environment, to combat emissions of air pollutants, to identify made available by the ARPA Lombardia it was possible to find a direct
and implement the most effective emission reduction measures and set and statistically significant correlation between PM10 and PM2.5 levels
appropriate objectives for ambient air quality, taking into account and the salbutamol doses used, the active ingredient present in the
WHO standards. This Directive introduced limit values for sulphur di- drugs used to counter bronchospasm during asthma crisis. Each in-
oxide, nitrogen dioxide and oxides of nitrogen, particulate matter (PM10 crease in PM10 of 10 μg/m3 corresponds to a 6% increase in salbutamol
and PM2.5), lead, benzene, carbon monoxide and ozone in ambient air, dose employed by the Milanese population (Fattore et al., 2016).
establishing the exchange of information and data from networks and In addition, atmospheric pollution can interact both with pollen,
individual stations measuring ambient air pollution within the Member leading to an increase in release of antigens with modified allergenicity,
States. The 2008/50/EC Directive lays down measures aimed at de- both with particles carrying allergenic of plants; these particles can
fining and establishing objectives for ambient air quality designed to reach peripheral airways with inhaled air and induce asthma in sensi-
avoid, prevent or reduce harmful effects on human health and the en- tive subjects.
vironment as a whole; assessing the ambient air quality in Member
States on the basis of common methods and criteria; obtaining in- 2. Materials and methods
formation on ambient air quality in order to help combat air pollution
and nuisance and to monitor long-term trends and improvements re- In this paper, for a six-year period (2010–2015), in the city of Rome,
sulting from national and Community measures; ensuring that such the synergistic effect of airborne particulate matter, pollen, gaseous air
information on ambient air quality is made available to the public; pollutants and meteorological conditions in patient sufferers has been
maintaining air quality where it is good and improving it in other cases; studied. The aim was to evaluate if also air pollution contribute to al-
promoting increased cooperation between the Member States in redu- lergic diseases symptom manifestation in sensitive subjects and the
cing air pollution. possibility of using multivariate approach for application purpose in the
In many cases limits and threshold values set by The EU Directive do medical field.
not coincide with the World Health Organization’s reference limit va-
lues: WHO thresholds for human health protection are lower than those 2.1. Study design
foreseen by the legislation and much of the urban population is still
exposed at higher levels than these guiding values. In addition, research While it is relatively easy to demonstrate the cause and effect re-
and international regulations on air pollution are still typical today for lationship between exposure to high concentrations of certain pollen
evaluations of the individual substances and their specific effects: little species and manifestation of allergic symptoms, it is harder to highlight,
is known about the cumulative effect that more air pollutants, at high using measured data, the combined effect of some traditional pollutant
concentration levels in the same time interval, may have on human (like PM, SO2, NO2 and O3) on allergic patients.
health. Basically there is to face a difficulty linked to the intrinsic differ-
Even less has been explored the possible combined action of tradi- ences in the variables describing these airborne species and for the
tional pollutants with the granulometric particle of biological particu- difficulty in measure of symptoms.
late matter, about 10 μm or more aerodynamic diameter, consisting of Fig. 1 shows the air quality and pollen network considered in this
pollen and spores, which increases the consequences in terms of aller- study: for the evaluation of air quality in the city of Rome, time Series of
gies and asthma in the urban centres (D’Amato et al., 2007). PM10, PM2.5, NO2 and O3 concentration measured in the 14 stations of
Likewise, the absence of legal limits that directly link certain con- the AQ network of Rome (ARPA Lazio) were considered (Fig. 2). While,
centrations of pollen or aerated spores and human health does not allow for the evaluation of pollen concentrations, were considered time series
absolute assessments of air quality. of Cupressaceae/Taxaceae, Gramineae, Olea, Urticaceae and total pol-
The onset of symptoms occurs when pollen concentration, reaches a lens, measured by the Aerobiological Monitoring Centre of the Uni-
defined value, called threshold; but this threshold varies not only from versity of Rome Tor Vergata (Fig. 3), together with data from the Tor
individuals but also in the same individual during the season. Severe Vergata meteorological station (temperature, global radiation, pre-
asthma occurrence can be also triggered during thunderstorms in the cipitation, wind speed and direction).
pollen season (D’Amato et al., 2016), and thunderstorm asthma can The effects on human health were evaluated on a group of 100
affect individuals without prior asthma (Girgis et al., 2000; Lee et al., patients (between 4 and 18 years old) followed from 2010 to 2015
2017). through the Allergymonitor™© app that allows patients to record daily
Allergy sufferers respond subjectively to allergy. The severity of the symptoms of hay fever, bronchial asthma and any the therapies
symptoms depends not only on the pollen exposure, but also on specific adopted. The data collected in the clinical diary were automatically
factors of the allergic person such as lifestyle, IgE antibody level, sen- processed in various daily Symptom Medication Scores.
sitization and simultaneous exposure to other allergenic sources, the The relationship between the air quality data and pollen (unique
target organ clinical reactivity (eyes, nose, lungs). Scientific studies series for each parameter completed through the estimation of missing
show that predisposed subjects have increased respiratory reactivity data) and weather data with the selected indexes (RTSS and ACS) was
induced by air pollution and increased bronchial responsiveness to in- evaluated with a modelling approach PLSDA (Partial Least Squares
haled pollen allergens. Air pollution has been associated with hospital Discriminant Analysis).
admissions for respiratory disease in cities all over the world (Medina-
Ramòn et al., 2006). Atmospheric pollutants, particularly ozone, par- 2.2. Meteorological data
ticulate matter and sulphur dioxide, have an inflammatory effect on the
airways of susceptible subjects, causing an increase in epithelial per- The used meteorological data were recorded at the meteorological
meability, easier penetration of pollen allergen in the mucous station (SP2000, CAE Bologna, Italy) of Rome Tor Vergata, located in

A. Di Menno di Bucchianico et al. Urban Forestry & Urban Greening xxx (xxxx) xxx–xxx

Fig. 1. Map of Rome with air quality and pollen stations.

Fig. 3. Aerobiological Monitoring Centre − Rome, Tor Vergata.

Fig. 2. Urban Background station of the air quality monitoring network of
pollen grains per cubic meter, p/m3 (Mandrioli et al., 1998), of the 4
the Laboratory of Experimental Ecology and Aquaculture (LESA) of the taxa, Cupressaceae, Olea, Poaceae, Urticaceae and total pollen.
Department of Biology, currently managed by the Hydrographic Service Cupressaceae pollen belong to an great and important family. We
of the Lazio Region. consider as Cupressaceae pollen all pollen belonging to following
The following variables were considered: rain rate (mm), tempera- genera: Cupressus, Calocedrus, Chamaecyparis, Hesperocyparis, Juniperus,
ture (maximum, minimum and mean; °C), wind speed mean (Km h−1), Sequoia, Sequoiadendron, Taxodium, Thuja and although belonging to
global radiation mean (Watt m−2). another family, Taxus. Normally these genera blossoms during winter,
Cupressus and Hesperocyparis during spring other genera while Juniperus
can blossom in spring and sometimes in autumn. All these species have
2.3. Pollen counts not flowers, but produce high quantity of pollen. These species were
normally used in our cities for ornamental use. For this reason, it is
The aerobiological monitoring shows the qualitative and quantita- possible to see them in parks, garden, parking, along avenue, in ce-
tive variations of pollen of allergy interest. The instrument used is a meteries. These genera have evergreen leaves, opposite or whorled and
volumetric sampler type Hirst; and the data are set with a standardized usually paired or in threes. Adult leaves are narrow, scalelike, and
sampling method (UNI, 2004; Travaglini et al., 2009). Pollen counts pressed against the branchlets, which themselves are often flattened.
were recorded at the aerobiological station of the University of Rome The male reproductive structures are borne at the ends of short twigs;
Tor Vergata. the female structures (cones) are terminal, with opposite or whorled
The pollen data used refer to the daily concentration, expressed in

A. Di Menno di Bucchianico et al. Urban Forestry & Urban Greening xxx (xxxx) xxx–xxx

scales, consisting of both a fused bract (modified leaf) and a scale. The monitoring centre of Tor Vergata, for its statistically good spatial and
cones, usually woody, have erect ovules. Pollen size is about 20–30 μm, temporal representativeness of the air quality status of the whole city
at optical microscope pollen of these genera is very similar. For this and for the simultaneous presence of the needed monitoring equipment
reason we count all Cupressaceae pollen as unique type (Pignatti, 1982; (not always, in an AQ network PM10, PM2.5, NO2 and O3 are sampled
Travaglini et al., 2014). and measured in the same site).
Olea belongs to Oleaceae or olive family. It is a woody plant native In addition, the 5 data time series were completed through a mul-
to forested regions in Mediterranean basin. The leaves are opposite each tiple linear regression with the other stations records for the estimation
other on the branch. Flowers in most members of the family have four of missing data.
sepals, four petals, the fruit is the fleshy olive. In recent years, olive Airborne particulate matter (PM) consists in a mixture of solid and
trees are used in our cities as ornamental plant, determining an increase liquid atmospheric particles with an aerodynamic diameter (da) be-
of Olea pollen in the town. Pollen size is about 20–25 μm (Pignatti, tween 0.01 and 100 μm. Particles larger than 10 μm are generally dust
1982; Travaglini et al., 2014). resulting from erosion or industrial processes, they settle to the ground
Poaceae, formerly called Gramineae or Graminaceae, are grass fa- in a short time and are responsible for pollution phenomena on a small
mily of monocotyledonous flowering plants. Grasses are perennial or spatial scale. Particles with an aerodynamic diameter less than or equal
annual and usually terrestrial and free-standing. Their flowers are very to 10 μm and aerodynamic diameters less than or equal to 2.5 μm are
simple, without tepals. From the anthers high quantity of pollen is the subject of most air pollution studies and are commonly identified in
widespread. Poaceae live everywhere in the world, in all continents, in the PM10 and PM2.5 fractions. They are characterized by long periods of
desert, in forest, in town and so on being most important source of food. stay in the atmosphere and can be transported at very large distances
They can form a typical ecosystem, the prairie. In Rome more than 150 from the emission source, they have a particularly complex and variable
species are known. Poaceae pollen is very important from allergological chemical nature and are able to penetrate the human respiratory tree
point view, some species such timothy grass or Bermuda grass are very and thus have negative effects on health.
dangerous. Poaceae pollen is monoporate, spheroidal, about 20–45 μm Part of these substances are directly emitted into the atmosphere as
size (Pignatti, 1982; Travaglini et al., 2014). particulates (primary aerosols), others are generated in atmosphere by
Urticaceae: to this family belong several herbaceous and shrubs chemical-physical processes that occur among gaseous pollutants (sec-
genera such as: Urtica (nettle), Parietaria (pellittory), Ramié (Boehmeria ondary aerosols).
nivea). Many species, especially the nettles (Urtica) have stinging hairs The particulate matter can have both a natural (erosion of rocks,
on the stems and leaves. The leaves are varied and the sap is usually volcanic eruptions, forest combustion and pollens) and anthropic origin
watery. Small, greenish flowers often form clusters in the leaf axils. (for example, car emissions, tyre and road abrasion and various kinds of
Both male and female flowers may be borne on the same or different combustion).
plant. The curled stamens of the male flowers straighten quickly as the Nitrogen dioxide (NO2) is a toxic gas part of the nitrogen oxides. In
flowers open, releasing pollen. From allergological point of view the polluted atmosphere its presence is associated with the nitrogen
Pellittory is the most important specie, living everywhere in towns on monoxide (NO) and the mixture of the two gases is indicated as ni-
wall, ruins, pavements and similar environment with high quantity of trogen oxides (NOX).
nitrates. Nowadays Pellittory in Rome flourishes all the year. Pollen size In the atmosphere nitrogen dioxide is mainly a secondary pollutant,
in very small, about 10–18 μm. at optical microscope pollen of these which results from the oxidation of nitrogen monoxide. It plays an
three genera is very similar, almost indistinguishable (Pignatti, 1982; important role in the photochemical reactions of ozone; its high con-
Travaglini et al., 2014). centration, coupled with the presence of volatile hydrocarbons and
The instrument used for pollen monitoring is a volumetric sampler- particular atmospheric conditions, such as strong solar radiation, it
type Hirst (1952), recommended in 1972 by the International Biolo- produces high concentrations of tropospheric ozone.
gical Program (Benninghoff and Edmonds, 1972), Model 2000 VPPS The sources of nitrogen oxide emissions are mainly related to
Lanzoni (Mandrioli, 1994); the data acquisition was carried out as re- human activity and to a lesser extent to natural phenomena. Anthropic
ported in Standard UNI (2004) and next updates, the protocol that sources can be associated with combustion processes (vehicular traffic,
describes the procedure for measuring of the concentration of pollen industry, electricity generation, domestic heating) and processes
grains and fungal spores dispersed into the atmosphere and reported in without combustion (nitric acid production, use of nitrogen fertilizers,
the Manuale di gestione e qualità della R.I.M.A. – Rete Italiana di Mon- etc.). Natural sources of nitrogen dioxide are represented by: volcanic
itoraggio in Aerobiologia (Travaglini et al., 2009). The pollen data used eruptions, electric shock caused by lightning and biological activity of
refer to the daily concentration, expressed in p/m3 (Mandrioli et al., some bacterial species in the soil.
1998), of the pollen of the considered families registered from January Nitrogen dioxide is a strong oxidant, highly reactive and corrosive.
1st, 2010 to December 31th, 2015. The main toxic effects on human health, which can be acute and
chronic, are due to the respiratory system, the mucous membranes and
2.4. Air pollutants the eyes. Extremely high concentrations can cause death.
Environmental damage is mainly related to acidification of rainfall,
For the evaluation of the air quality in the city of Rome the daily deposition in general (in the presence of water nitrogen dioxide is
levels of particulate matter, nitrogen dioxide and ozone were con- converted into nitric acid) and the eutrophic effect that nitrogen com-
sidered: these are the most critical air pollutants and they were selected pounds exert on the vegetation and the water.
based on their past and recent average levels and for their interactive Tropospheric ozone is a secondary pollutant formed through pho-
effect with pollens grains on human health (D’Amato et al., 2007). tochemical processes in the presence of primary pollutants such as ni-
Specifically, 5 parameters that better describe the air quality status trogen oxides (NOx) and volatile organic compounds (VOCs). Following
were calculated: the daily average mass concentration of PM10 parti- the photochemical processes, a complex mixture of substances called
culate matter; the daily average mass concentration of PM2.5 particulate photochemical smog forms in the low layers of the atmosphere. Ozone,
matter; the daily average concentration of nitrogen dioxide, NO2; the which is the main representative, can cause serious problems to human
daily average concentration of ozone, O3, and the ozone daily max- health and the ecosystem, as well as to agriculture and materials.
imum 8-h mean. All data were collected from the Cinecittà Urban Photochemical pollution, is a transboundary phenomenon: in par-
Background station, chosen within the ARPA air quality network after a ticular conditions photochemical pollutants can be transported for long
complete intercomparison among the air pollutants and pollen time distances. Ozone pollution is, therefore, a phenomenon that is spread
series from the whole network, for the proximity to the Aerobiological over large spatial scales and the high concentration levels found in a

A. Di Menno di Bucchianico et al. Urban Forestry & Urban Greening xxx (xxxx) xxx–xxx

certain area are not always attributable to emission sources located (RTSS/6 + RMS)/2.
close to the sampling point. Inclusion criteria were the following: A) allergy sufferers children
The higher ozone concentrations are recorded in the warm months between 4 and 18 years old; B) a diagnosis of pollen-AR (Bousquet
of the year and during the hours of maximum solar irradiation. In urban et al., 2007, 2008); C) IgE sensitization to one or more of the following
areas, ozone is formed and transformed rapidly, with a very different four pollen sources: cypress, grass, olive, pellitory, i.e. the most relevant
behaviour than that observed for other pollutants. ones in Rome between April and June (Travaglini et al., 2002) and for
The main sources of emissions of ozone precursors are road trans- their principal molecular allergens; D) positive skin prick test (SPT) four
port, industrial activities, civil sector and energy production. pollen sources: cypress, grass, olive, pellitory, i.e. the most relevant
ones in Rome between April and June (Travaglini et al., 2002); E) the
2.5. Clinical data intention to stay in Rome for the whole study period; F) a number of
symptoms and medications recordings per patient ≥20 consecutive
The methods for assessing and monitoring allergic symptoms are days at least during 2 years. IgE sensitization was also considered by
based on online diaries compiled by patients. This practice begins to be introducing IgE correction – IgE-pc, an index obtained by multiplying
widespread in some European states such as Germany, Switzerland, the pollen concentration with the specific activity was also created and
Austria (Berger et al., 2013; de Weger et al., 2013; Voukantsis et al., defined “IgE-pc” (Pollen concentration multiplied by the Specific Ac-
2013). In Italy, since 2010, the Allergymonitor™© app can be down- tivity, SA), considered positive values are > 0.35 (Di Lorenzo et al.,
loaded, accessible for free for mobile device, with Android or iOS op- 2009). The SA correction values of IgE were calculated using the ratio
erating system. This tool is an easy-to-use and well-accepted web between the values of molecular IgE and total IgE for each patient. IgE
platform for patients because it is very useful for improving their ad- molecules considered are: T222 (Cupressaceae), g205 + g215 (Grami-
herence to therapy (Tripodi et al., 2012; Pizzulli et al., 2014). This is an neae), t224 (Oleaceae), w211 (Urticaceae). The value of IgE against
online diary, in which every patient, upon informed written consent of rCup a1, rPhlp1 and rPhlp 5b, nOle e1, and rPar j2 has been multiplied
the parents, is invited to record daily, generally in the evening, any by the value of the daily pollen concentration of the corresponding
medications taken and allergic symptoms through the smile symbolism, pollen type (Cupressaceae for rCup a1, Poaceae for rPhl p1 + rPhl p5b,
answering questions about the quality of life Inherent in Allergic pa- Olea for nOle e1, Urticaceae for rPar j2) (Costa et al., 2014).
thology, evaluating their state of mind or daily malaise with an Ana-
logic Visual Scale, whose score ranges from 0 (very good) to 10 (bad). 2.6. The multivariate time lag modelling
The severity of the symptoms is recorded with the use of four different
emoticons, each of which represents a degree of severity (absent, mild, A multivariate predictive modelling approach was used. This ap-
moderate and severe). The innovative aspect of the system is in the proach is based on PLSDA (Partial Least Squares Discriminant Analysis)
possibility of bi-directional interaction between physician and patient (Swierenga et al., 1998) and statistical modelling libraries were written
via e-mail, chat and SMS (text message). Patients (or their parents) not in the MATLAB 7.1 R14 environment by the Research Centre for en-
entering their data for two consecutive days received an automatic alert gineering and agro-food processing at CREA (Italy). The PLSDA ap-
SMS on their mobile phone or by e-mail. In this way, it establishes a proach (Sjöström et al., 1986; Sabatier et al., 2003; Costa et al.,
direct and constant relationship between patient and physician, while 2013a,b,2014; Taiti et al., 2015) was used in order to predict the pre-
improving both the medical management of the disease and the ad- sence or the absence of symptoms; the Y variable is represented by
herence of the patient to the doctor’s prescriptions. threshold 6 for the scores RTSS (RTSS ≥ 6), and threshold 1 for ACS
The full process followed local, national and European laws on (ACS ≥ 1). The partitioning design consists, for each patient, in using
protection of privacy and sensitive personal data. the data from the year with the larger number of records to build and
Allergymonitor™© transforms patient data and automatically calcu- cross-validate the dataset (hereafter labelled as the “model year”), and
lates SMS indices, generating a database that can be used for statistical the other year as independent test (hereafter labelled as the “test year”).
analysis. The study population consisted of 100 children patients The prediction ability of PLSDA and the different number of models also
seeking care for pollen-AR at the paediatric allergy outpatient Unit of depends on the number of latent vectors (LV, used up to 19) used in the
the Sandro Pertini Hospital in Rome. model. The x-block (25 variables) was pre-processed using a first au-
Patients registered ocular (itching, tear flow, and redness), nasal toscale algorithm (centres columns to zero mean and scales to unit
(sneezing, itching, running, and blockage), and bronchial (cough, variance). Followed by a second pre-processing step applying seven
wheezing, and dyspnea) symptoms. The allergic responses are set different algorithms: none, baseline (Weighted Least Squares), detrend
considering RTSS (Rhinoconjuntivitis Symptom Total Score). The RTSS (remove a linear trend), mean centring, MSC (multiplicative scatter
includes six individual symptoms: four nasals (sneezing, rhinorrhoea, correction with offset), normalize (normalization of the rows) and snv
itching, and congestion) and two ocular (itching and tearing). The in- (Standard Normal Deviate). The best models were extracted at 5 dif-
tensity of each symptom can be expressed with a value from 0 to 3: ferent forecast levels (time lag) ranging from 0 to 4 days (Brighetti
0 = absent (no sign/symptom evident); 1 = mild (sign/symptom et al., 2014). A summary of the relative importance of the X-variables is
clearly present, but minimal awareness; easily tolerated); 2 = moderate given by Variable Importance in the Projection (VIP) (Febbi et al., 2015;
(definite awareness of sign/symptom that is bothersome, but tolerable); Infantino et al., 2015; Taiti et al., 2015). VIP scores estimate the im-
3 = severe (sign/symptom that is hard to tolerate; causes interference portance of each variable in the PLS-based models. VIP scores were
with activities of daily living and/or sleeping). The daily total of six calculated according to Chong and Jun (2005).
symptoms combined can reach a score between 0 and 18 (6 symptoms The forecast model is constructed by considering two sets of data:
×3 point scale). data for all years of available recordings, except for one, 2015, are used
The use of drug is an additional variable. For this reason, Symptom in the calibration phase, while data for the year 2015 are used for the
Medication Scores – SMS (Grouin et al., 2011; Häfner et al., 2011) will be test and validation of the model.
introduced to modulate the value of the RTSS. The SMS considered in
this study is: ACS – Average Combined Score, an index derived from the 3. Results and discussion
combination of the RTSS and the RMS (Rescue Medication Score adopts a
scale based on the type of drug taken); RMS:0 = no rescue medication; 3.1. Air quality and pollen allergens in Rome
1 = antihistamines; 2 = nasal corticosteroids; 3 = oral corticosteroids
(the RMS for a given day is equal to the highest score recorded for that The first step of this study was the evaluation of the average levels
day). The ACS score varies between 0 and 3) according to the formula: of air pollutants and pollens in the city of Rome: what is the current

A. Di Menno di Bucchianico et al. Urban Forestry & Urban Greening xxx (xxxx) xxx–xxx

Fig. 4. PM10, PM2.5, NO2 and O3 2010–2015 time series from the Cinecittà Urban Background station, Rome.

status and the time trend of these two different forms of air pollution? 3.2. The multivariate time lag modelling
There are periods in which emissions and dispersion episodes lead them
to be present together in the air or the total diversity of sources makes A total number of 100 patients were recruited, but only 65 com-
them out of phase? pleted the study (Table 3). Reason for drop-out are too short period of
In the period of study, the considered air quality pollutants (PM10, registration (< 20 days of registration).
PM2.5, NO2 and O3) showed their typical seasonal pattern (higher levels The Table 4 shows the registration years number per patients
during the cold months for PM10, PM2.5, NO2, higher levels during the number.
warm months for O3) and a general decrease, except for the ozone, in Some of the 65 patients had no variability in the allergic response:
the number of exceedances of limit values (Fig. 4) the recorded values were all lower or higher than the threshold value.
On the other side, the pollen families considered as representative of Therefore, the number of patients included in PLSDA was 45 for ACS
pollen emission in the city of Rome (Cupressaceae/Taxaceae, and 59 for RTSS.
Gramineae, Olea and Urticaceae) showed concentration picks strictly The system has generated 68,181 models in total: 39,960 models for
related with their blooming season (Fig. 5, please note that in other ACS and 28,221 models for RTSS (Table 5).
periods of the year concentration go to zero). Therefore, for best model selection the following modelling para-
During the period of study, the pollen families showed generally meters were considered: time lag (from 0 to 4), number of LVs (from 1
stationary levels, except for the Urticaceae and this is probably caused up to 19) and x-block second pre-processing (7).
by a reduced care of public green areas in recent years. For each patient, the best models obtained for ACS (222 models)
A clear difference between PM10 (the thoracic fraction) and pollen and for RTSS (278 models) at different time lag (from 0 to 4 days) and
aerosol time patterns is well showed considering specific threshold up to 19 LVs, have been selected.
values (Table 1) to extract PM10 exceedances and pollen events (ex- RTSS models generally resulted better than ACS models (Tables 6
ceedances is the legal term referred to the European Directive on air and 7) in terms of percentage of correct classification.
quality). PM10 daily exceedances of EU limit value 50 μg/m3 follow the The best results are observed at time lag 1 for RTSS (Table 8) and at
typical seasonal pattern, even as pollen events (Travaglini et al., 2009) time lag 4 for ACS (Table 9). This delay may be due to the drug: the ACS
that are strictly linked to the blooming period, because of the short index also includes drug use, which results in an improvement in per-
permanence in the atmosphere of pollen grains (Fig. 6). ception of the symptoms. It is possible to observe high performances of
To investigate the potential cumulative effect that these different mean correct classification about 70% (from 69,09% to 79,76%). These
pollutants may have on human health it is fundamental to point out the values indicate a relative high accuracy in predicting symptoms when
number and the period of possible common events. During the period of present.
study, based on the abovementioned threshold values, the worst The Table 10 shows the percentage VIP scores of patients in order to
months for the contemporary presence of high levels of air pollutants evaluate the impact of x-block variables.
and pollen, in the city of Rome, were February and March. (Table 2). Fig. 7 shows the VIP scores of 4 patients taken as cases for example
among the 68 analyzed, for the two SMS, ACS and RTSS: the values of

A. Di Menno di Bucchianico et al. Urban Forestry & Urban Greening xxx (xxxx) xxx–xxx

Fig. 5. Main Pollen allergens 2010–2015 time series from the Aerobiological monitoring Centre of Tor Vergata, Rome.

Table 1 total IgE are higher than 300 kU/L for 2 patients (patient #27: IgE
2008/50/EC PM10 daily limit value and A.I.A. – Aerobiology Italian Association – tot = 847 kU/L, patient #31: IgE tot = 381 kU/L) and less than
pollen standards. 300 kU/L in the case of other two patients (patient #92: IgE tot = 294
Adopted threshold values kU/L, patient #127: IgE tot = 168 kU/L). The results of percentage of
correct classification in the model are high for patients #27 and #31
PM10 50 μg/m3 (respectively 96.9% and 100.0%), lower for patient #92 and #127
Cupressaceae/Taxaceae 90 p/m3 (respectively 46.7% and 63,1%); same result for the test: patient
Graminae 30 p/m3
Olea 25 p/m3
#27 = 81.0%, patient #31 = 96.4%; patient #92 = 12.1%, patient
Urticaceae 70 p/m3 #127 = 12.2% (Table 11). The 2 pie plots shows the values of IgE SA
sensitization of each of the 4 patients: Patient #27 is sensitive to rPhl

80 160
PM10 - exceedance days per year Pollens - events per year
70 140

60 120
N. of exceedance days

50 100
N. of events

40 80

30 60

20 40

10 20

0 0
2010 2011 2012 2013 2014 2015 2010 2011 2012 2013 2014 2015

20 30
PM10 - average number of exceedance days Pollens - average number of events
N. of exceedance days

N. of events

10 15
0 0

Fig. 6. PM10 and pollen concentrations in Rome: comparing time patterns.

A. Di Menno di Bucchianico et al. Urban Forestry & Urban Greening xxx (xxxx) xxx–xxx

Table 2 Table 7
PM10 and pollen concentrations in Rome: 2010–2015 common events. Mean of percentages of correct classification: comparison between ACS and
RTSS models.
Month/year 2010 2011 2012 2013 2014 2015 Tot
SMS % Correct Classification
January 0 1 0 1 1 0 3
February 2 9 5 2 2 1 21 mean test mean models
March 9 4 5 3 7 5 33
April 0 0 0 0 1 1 2 ACS 66.46 76.23
May 0 0 0 0 0 0 0 RTSS 73.85 79.32
June 0 0 1 0 0 0 1
July 0 0 0 0 0 0 0
August 0 0 0 0 0 0 0
Table 8
September 0 0 0 0 0 0 0
October 0 0 0 0 0 0 0
RTSS: influence of the time lag on the algorithm prediction performance in the
November 0 0 0 0 0 0 0 patients. In bold the best values at time lag 1.
December 0 0 0 0 0 0 0
Time lag Mean%
Tot 11 14 11 6 11 7 60
Correct Classification Correct Mean Mean Test
Model Classification Test Model
Table 3
Characteristics of the population samples. 0 79.11 70.64 72.24 76.92
1 80.91 74.97 72.51 77.02
n. of patients 2 78.62 75.69 70.78 77.60
100 3 79.17 73.70 71.53 77.99
n. of selected patients 4 78.75 74.36 69.09 78.48
Males Females
35 30
Average age (2010)
Table 9
12 y ACS: influence of the time lag on the algorithm prediction performance in the
min age max age patients. In bold the best values at time lag 4.
6y 18 y
Time lag Mean%

Correct Classification Correct Mean Mean Test

Table 4 Model Classification Test Model
Patients number vs observation years.
0 77.99 70.20 76.37 75.05
N. of years N. of patients 1 79.04 72.35 76.34 75.23
2 76.60 68.43 76.02 75.35
2 27 3 77.34 71.77 71.18 74.59
3 12 4 79.76 71.91 76.75 76.26
4 20
5 5
6 1
Table 10
Percentage VIP scores. xn = number X-block variables.
Table 5 pollen meteoclimatic pollutant
Total models for ACS and RTSS. (xn = 13) (xn = 6) (xn = 5)

Models ACS RTSS ACS 63.1 19.1 17.8

RTSS 64.3 12.9 22.8
TOTAL 39960 28221
selected 222 278
n. of patients 45 59
are due: for patient #27 to Graminaceae; for patient #31 to Olea; for
patient #92 to Olea; for patient #127 to Olea without IgE correction.
Table 6 The patients #27, #31 and #127 show also an important variables
Number of models (m) with different percentages of correct classification (pcc). pollutant contribute (in order NO2, O3max and PM10).

% Correct mean total mean test mean models

Classification test + models
4. Summary and conclusions

ACS RTSS ACS RTSS ACS RTSS Millions of people worldwide, particularly children, suffer from al-
lergic rhino-conjunctivitis (AR) induced by pollens (pollen-AR) (Asher
m < 60 pcc 25 39 57 62 26 26
60 ≤ m < 70 pcc 60 49 50 48 40 61
et al., 2006; Brozek et al., 2010). AR negatively affects patients’ per-
m ≥ 70 pcc 137 190 115 168 156 191 formance of daily activities, sleep patterns, cognitive function, work
and school productivity and quality of life (Peden and Reed, 2010).
Allergies are increasing despite, in Rome, the analysis of trends shows a
p1 + rPhl p5b (59.29 kU/L) and to rPar j2 (243,00 kU/L) and to a lesser statistically significant decrease of important atmospheric pollutants
extent nOle e1 (0,54 kU/L,); patient #31 is sensitive to rPhl p1 + rPhl such as PM10, PM2.5 and NO2, all related o anthropogenic emissions
p5b (111.78 kU/L) and to rPar j2 (23,70 kU/L) and to a lesser extent such as the road traffic (Cattani et al., 2010, 2014). Pollen concentra-
nOle e1 (0,47 kU/L); the patient #92 is sensitive to nOle e1 (9,38 kU/L) tions in Rome, on the other hand, appear stable, with the only exception
and to rPhl p1 + rPhl p5b (2,59 kU/L); patient #127 is sensitive to nOle of Urticaceae that are increasing in the last years. In general the higher
e1 (0,69 kU/L) and to rPar j2 (0,10 kU/L). The same figures (bar plots) levels of concentrations in the atmosphere of pollens and air pollutants
show the contribution of VIP score for each of the 25 variables used in occur in different seasons, this is due to the big differences in natural
the x-block; regarding pollen concentrations, the major contributions and anthropogenic sources of these substances. In the city of Rome the

A. Di Menno di Bucchianico et al. Urban Forestry & Urban Greening xxx (xxxx) xxx–xxx

Fig. 7. Variable Importance in Projection (VIP) scores: factors that contribute to the prediction of allergic symptoms. From top to left in clockwise direction: pz #27,
pz #31, pz #92, pz #127.

Table 11
Molecular profile of 4 patients: pz #27, pz #31, pz #92, pz #127.
patient IgE kU/L pcc


E TOT E CYP E PHL E OLI E PAR E Cup a 1 E Phl p 1 + E Phl p 5 E Ole e 1 E Par j 2 SA model test

#27 847.18 4.48 32.72 NR 110.90 NR 59.29 0.54 243.00 0.36 96.88 80.95
#31 381.00 0.39 60.32 NR 14.30 NR 111.78 0.47 23.70 0.36 100.00 96.43
#92 294.00 26.52 2.64 13.03 NR NR 2.59 9.38 NR 0.04 46.67 12.12
#127 168.00 NR 0.27 NR 0.66 NR NR 0.10 0.69 0.05 63.11 12.16

greatest overlap period is between February and March, when high prevention, and this is a topic of particular interest in applied research
levels of pollens occur together with high levels of air pollutants. in various fields.
Less than half of the patients regularly follow medical advice, drug The PLSDA, based on air concentrations of atmospheric pollutants,
therapies generally achieve only partial control of symptoms, and pa- pollens and weather data, showed a good accuracy in the prediction of
tient’s adherence to therapy is often poor (Canonica et al., 2007); in allergic symptoms. Comparing the results with a previous study (Costa
addition, allergic responses are subjective. The development of pre- et al., 2014), we confirm that: 1) a multivariate modelling approach can
dictive models represents an important contribution to symptomatology accurately predict the presence or absence of symptoms up to 4 days

A. Di Menno di Bucchianico et al. Urban Forestry & Urban Greening xxx (xxxx) xxx–xxx

before the event; 2) the models’ predictive performance tended to im- external shape analysis. Aquacult. Eng. 52, 58–64.
prove when the degree of individual allergic susceptibility was also Costa, C., Antonucci, F., Menesatti, P., Pallottino, F., Boglione, C., Cataudella, S., 2013b.
An advanced colour calibration method for fish freshness assessment: a comparison
taken into account. Results confirm that the models performance is between standard and passive refrigeration modalities. Food Bioprocess Technol. 6,
highly dependent from patients: the forecast models are reliable for 2190–2195.
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