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Cabrera M, et al.

J Investig Allergol Clin Immunol 2019; Vol. 29(5): 371-377

© 2019 Esmon Publicidad

doi: 10.18176/jiaci.0368

ozone is the closest variable in the 2009 graph and is associated

with PM10, yet has almost no relationship with temperature

(which is distant and almost perpendicular on the graph). The

relationship between temperature and pollution variables is

even higher than in the 1996 period (ozone [R=0.53] and PM10

[R=0.34], with a positive sign in both cases). The pollution

variables (ozone and PM10) are still only slightly associated

(R=0.06), although, here, the relationship is still positive.


We found a higher symptom score in the 2009 period,

despite lower pollen counts, than in the 1996 period. However,

it is important to remember that this was a year with lower

humidity, similar temperatures, and higher ozone levels (albeit

lower than threshold). Consquently, these factors may have

affected the longer duration and intensity of the grass pollen

season that year. The specific atmospheric conditions inMadrid

in spring, where marked instability leads pollen deposited on

the ground to be lifted, may also have contributed.

In southern Spain, the grass pollen season is now longer

as a result of rising temperatures [12]; the same is true for the

Oleaceae pollen season [13]. The increase in temperature in

this geographical area seems to have a positive effect on the

intensity of flowering, with longer pollination periods that are

often more intense. In this study, the main pollen season in 2009

was 13 days longer than in 1996. The grass pollen forecast in

Madrid is always announced by March. Rainfall fromOctober

1995 to March 1996 in Madrid was twice that of the previous

period (October 1994-March 1995), thus leading to a 4-fold

higher number of grains in 1996 than in 1995. Furthermore,

the Spanish Society of Allergy and Clinical Immunology

(SEAIC) estimated that the cumulative concentrations of grass

pollen counts in 2009 exceeded 5100 grains/m


, compared

with 4000 grains/m


recorded in 2008. Nevertheless, the lower

grass pollen counts collected in 2008 were probably due to the

cleaner rain effect observed in May, which coincided with the

peak grass pollen period (Figure 1), albeit in a more polluted

atmosphere and with more allergenic activity, as shown by the

higher seasonal allergic rhinitis score.

We suggest that this finding could be associated with

the coadjuvant effect of temperature and pollution (mainly

ozone), which generates more potent allergens, as well as

with the direct relationship between the greater level of atopy

in the 2009 group than in the 1996 group. Ozone increases

allergenicity (induces larger wheals and flares in skin prick

tests) [14], and exposure of

Phleum pratense

pollen to

increasing ozone concentrations (from 100 ppb up to 5 ppm)

results in a significant increase in naturally released pollen

cytoplasmic granules, which also contain allergens [15].

Pollution is a possible cause of oxidative stress, and this

stress is responsible for the higher prevalence of seasonal

allergic rhinitis, which intensifies in activity as a defense from

environmental pollution, thus strengthening allergenicity [16].

Pollutants such as SO


, NO


, and ozone can alter the allergenic

proteins of pollen [16,17].

Ozone is a pollutant that usually reaches higher values in

areas far from the sources of emission, that is, in semiurban

and rural areas. The atmospheric conditions present in heat

waves favor the formation of tropospheric ozone from

precursors [18]. During the summer, the excessively high

temperature in Madrid (higher than the threshold of 36.5ºC)

coincides with the days on which the population must be

warned about high concentrations of ozone (higher than

the threshold of 180 μg/m


) [18]. These thresholds were

not exceeded in 2009, although mean annual values tended

to increase [19]. In Madrid in 2017, the number of times the

ozone threshold was exceeded (>25 times) was recorded in

the 2011-2017 report [20]. As ozone is a secondary pollutant,

the measures adopted were aimed at reducing the emission of

precursors, mainly NOx and volatile organic compounds [18].

In a recent report from Ecologistas en Acción (2018), 2 of

the stations measured high ozone values in winter that were

similar to those recorded in spring in the same places (San

Agustín de Guadalix and Puerto de la Morcuera), namely, 70

and 80 µg/m



With regard to photochemical pollutants or the synergistic

effect of ultraviolet radiation on pollutants, study of the effects

of UV-B rays and ozone shows that the pollen tube was

shortened considerably, more than by the stress itself, despite

low levels of ozone [22].

Differences have been found in the allergenicity of pollens

from groups of trees of the same species and grass pollen,

which, although relatively close in terms of taxonomy, are

found in areas with different pollution levels (city/countryside)

and temperatures (valley/mountain) [23]. In Spain in 2002,

Armentia et al [23] reported that the grass pollen in rural

areas of the province of Valladolid was less damaged than the

same species in urban areas, where grass pollen is subject to

a polluted environment, repeated mowing that lets very few

spikes flourish, and pesticides applied by local authorities [23].

In 2007, Feo-Brito et al [24] reported that the air pollution

levels in Puertollano (high pollution levels) were associated

with a greater risk of asthma symptoms in pollen-allergic

asthmatic patients than in a similar group from Ciudad Real

(lower pollution levels) [24]. The largest contribution was

by ozone, especially in Puertollano [24]. In 2007 and 2010,

Mur Gimeno et al [25] and Feo-Brito et al [26] reported that

pollen-allergic asthmatics in Puertollano presented poorer

clinical progress and became decompensated earlier than those

from Ciudad Real, and that this could be due to air pollution.

Consequently, urbanization and high levels of vehicle

emissions induce more symptoms of bronchial obstruction (in

particular bronchial asthma) in people living in urban areas

than in those living in rural areas.

In the eastern United States and Europe, the highest

regional ozone levels are recorded when a slow-moving, high-

pressure system develops in summer. This is when the days are

longest, when solar radiation is most direct (the solar zenith

angle is lower), and air temperatures are high. As the slow-

moving air in the shallow boundary layer passes over major

metropolitan areas, precursor concentrations rise; as the air

slowly flows around the high-pressure system, photochemical

production of ozone occurs at peak rates [27]. We suggest that

high temperatures in Madrid, even with low levels of ozone

concentrations (which was higher 13 years later), could be a

factor that has contributed to the increase in symptoms even

at lower grass pollen counts in 2009 than in 1996.