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Urban green zones and related pollen allergy: A review. Some guidelines for designing spaces with low allergy impact

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Urban green spaces are a key element in the planning of today’s cities, since they favor the interaction between citizens and the environment, as well as promoting human health. However, lack of planning in the design of urban spaces and in the choice of ornamental species has been among the factors triggering one of the most widespread diseases in urban populations: pollen allergy. In this paper are reviewed the major causes of this extensive allergenicity, including: low species biodiversity at planting; the overabundance of given species acting as key specific pollen sources; the planting of exotic species prompting new allergies in the population; the choice of male, pollen-producing individuals in dioecious species; the presence of invasive species; inappropriate garden management and maintenance activities; the appearance of cross-reactivity between phylogenetically related species; and the interaction between pollen and air pollutants. The findings of this analysis highlight the clear need for guidelines regarding the design and planning of urban green spaces with a low allergy impact. Proposals include increased biodiversity, careful control when planting exotic species, the use of low pollen producing species, the adoption of appropriate management and maintenance strategies, and active consultation with botanists when selecting the most suitable species for a given green space.
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Landscape and Urban Planning 101 (2011) 205–214
Contents lists available at ScienceDirect
Landscape and Urban Planning
journal homepage: www.elsevier.com/locate/landurbplan
Review
Urban green zones and related pollen allergy: A review. Some guidelines for
designing spaces with low allergy impact
Paloma Cari˜
nanos, Manuel Casares-Porcel
Department of Botany, Faculty of Pharmacy, Campus de Cartuja, University of Granada, 18071 Granada, Spain
article info
Article history:
Received 13 December 2010
Received in revised form 7 March 2011
Accepted 12 March 2011
Available online 16 April 2011
Keywords:
Allergenicity
Pollinosis
Urban green spaces
Ornamental species
Aerobiology
abstract
Urban green spaces are a key element in the planning of today’s cities, since they favor the interaction
between citizens and the environment, as well as promoting human health. However, lack of planning in
the design of urban spaces and in the choice of ornamental species has been among the factors triggering
one of the most widespread diseases in urban populations: pollen allergy. In this paper are reviewed
the major causes of this extensive allergenicity, including: low species biodiversity at planting; the over-
abundance of given species acting as key specific pollen sources; the planting of exotic species prompting
new allergies in the population; the choice of male, pollen-producing individuals in dioecious species;
the presence of invasive species; inappropriate garden management and maintenance activities; the
appearance of cross-reactivity between phylogenetically related species; and the interaction between
pollen and air pollutants. The findings of this analysis highlight the clear need for guidelines regarding
the design and planning of urban green spaces with a low allergy impact. Proposals include increased
biodiversity, careful control when planting exotic species, the use of low pollen producing species, the
adoption of appropriate management and maintenance strategies, and active consultation with botanists
when selecting the most suitable species for a given green space.
© 2011 Elsevier B.V. All rights reserved.
Contents
1. Introduction .......................................................................................................................................... 205
2. Review of the causes of the growing allergenicity of ornamental species .......................................................................... 206
2.1. Biodiversity ................................................................................................................................... 206
2.2. Sources of pollen emissions .................................................................................................................. 206
2.3. Introduction of exotic species ................................................................................................................ 210
2.4. Botanical sexism .............................................................................................................................. 210
2.5. Invasive species............................................................................................................................... 210
2.6. Management and maintenance .............................................................................................................. 211
2.7. Proximity pollinosis .......................................................................................................................... 211
2.8. Establishment of cross reactions ............................................................................................................. 211
2.9. Interaction with air pollutants ............................................................................................................... 211
3. Guidelines for designing spaces with a low allergy impact ......................................................................................... 212
4. Conclusion............................................................................................................................................ 212
References ........................................................................................................................................... 213
1. Introduction
Urban green spaces are a key element in the planning of mod-
ern cities, in that they foster the interaction between citizens and
Corresponding author. Tel.: +34 958 241977; fax: +34 958 248632.
E-mail addresses: palomacg@ugr.es (P. Cari˜
nanos), mcasares@ugr.es
(M. Casares-Porcel).
the environment within an urban context, promote human health,
and provide substantial environmental and recreational benefits
to urban citizens. Matsouka and Kaplan (2008) aimed to determine
what people require from the urban landscape and highlighted two
major categories: the need for nature, reflecting the numerous ways
in which human needs are met by the natural environment, and the
need for human interaction, particularly as promoted by the urban
environment. This second need underlines the potential role of
urban design in enhancing human conditions: several studies have
0169-2046/$ – see front matter © 2011 Elsevier B.V. All rights reserved.
doi:10.1016/j.landurbplan.2011.03.006
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206 P. Cari˜
nanos, M. Casares-Porcel / Landscape and Urban Planning 101 (2011) 205–214
revealed that simply viewing nature through windows reduces the
stress of daily urban life (Jackson, 2003); hospital patients with
window views of greenery recover faster (Ulrich, 1984); and lower
levels of domestic violence are recorded among residents living in
areas with trees (Sullivan & Kuo, 1996).
Growing appreciation of the role played by green spaces in regu-
lating the local mesoclimate (Domm et al., 2008) and in the removal
of gaseous air pollutants derived from human activities (Nowak
et al., 2000) has led many cities to become immersed in a frantic
greening process, which has had a direct impact on the citizens’
quality of life (Chaphekar, 2009; Chiesura, 2004; Lewis, 1992).
However, despite the undeniable benefits of urban green spaces
for human health, they are associated with a number of problems.
Urban woodlands may reduce air quality through the emission
of biogenic volatile organic compounds involved in ozone forma-
tion, which can exacerbate smog problems (Domm et al., 2008).
Additionally, trees may harbor hazardous diseases and insect pests
and generate fruit/leaf litter. Perhaps the most serious challenge
posed by urban green spaces, though, is related to human aller-
gic reactions to the airborne vascular plant pollen released during
pollination. Recent data suggest that people living in urban areas
are 20% more likely to suffer airborne pollen allergies than people
living in rural areas (D’Amato et al., 2007; Ogren, 2002). This situa-
tion has emerged due to several factors, chief among which are the
uniformity of green spaces, where a small number of species that
have proved highly suited to urban environmental conditions are
overwhelmingly used, and the interaction of pollen with air pol-
lutants (Cari˜
nanos, Prieto, Galán, & Dominguez, 2004; Cari˜
nanos,
Galán, Alcázar, & Dominguez, 2007), which can even prompt an
increase in pollen production by certain herbaceous species (Ziska
et al., 2003).
Continuous monitoring of airborne pollen has highlighted the
major contribution of plants growing in green spaces and urban
thoroughfares to the development of allergy symptoms in the local
populations in several parts of the world (Cardona-Dahl, 2008),
including Japan (Nakae & Baba, 2010), South Africa (Pordman,
1947), Australia (Bass, Delpech, Beard, Bass, & Walls, 2000), North
America (Ogren, 2002; White & Bernstein, 2003), South America
(Baena-Cagnani et al., 2009), and Europe (D’Amato et al., 2007).
The progressive spread of cities with associated changes in archi-
tecture and landscaping preferences has not only displaced the
ruderal species growing previously in newly urbanized areas but
also facilitated the introduction of a growing number of imported
and non-native plants (Sneller, Hayes, & Pinnas, 1993) and has also
intensified the formation of urban islands in which the city’s resi-
dents lead most of their daily lives (Cari˜
nanos et al., 2004).
In this report, we examine some of the major causes of the grow-
ing allergenicity of ornamental species, particularly trees in urban
environments, and review key features of the impact of this phe-
nomenon on local residents. Additionally, guidelines are provided
regarding the design and planning of urban green spaces with a low
allergy impact.
2. Review of the causes of the growing allergenicity of
ornamental species
2.1. Biodiversity
The need for biodiversity in urban ecosystems has become
increasingly urgent as more and more people inhabit cities (Savard,
Clergeau, & Mennecher, 2000). While species diversity is often
positively correlated with the quality of life in cities (Middleton,
1994), the overabundance of some species may have a detrimental
effect on local residents, which has been observed in association
with many urban green spaces. A study of the tree species lining
urban thoroughfares in Mediterranean areas of the Iberian Penin-
sula focused on the 12 most representative species in each town or
city sampled. The results highlighted the limited diversity present:
the total list included only 16 species, and the London plane (Pla-
tanus hyspanica) appeared in almost all of the towns sampled.
Additionally, the analysis of the species commonly used as orna-
mentals in urban areas (Table 1 ) shows that many of these are
anemophilous species producing large amounts of pollen that have
a demonstrated allergenic effect on the local population, with more
than 500,000 million grains being produced by a single tree in some
cases (Piotrowska, 2008; Tormo Molina, Mu˜
noz Rodriguez, Silva
Palacios, & Gallardo Lopez, 1996). This category includes all species
for which more than one scientific paper has reported a moder-
ate degree of allergenicity in terms of various existing scales (e.g.,
Ogren Plant-Allergy Scale (OPALSTM,Ogren, 2000), the Allergen
Index (Hruska, 2003; Hruska & Staffolani, 2010).
Two Spanish cities provide specific illustrative examples of this
phenomenon. Madrid has almost 300,000 roadside trees, which is
one of the highest figures for this parameter in the world, of which
over 60,000 are Platanus ×hispanica and P. orientalis. In Barcelona,
these species account for over a third of the 150,000 trees planted
in urban areas. Platanus species are anemophilous, with an esti-
mated pollen production of 13 ×106pollen grains per inflorescence
(Tormo Molina et al., 1996). Madrid and Barcelona are among the
highest ranking Spanish cities in terms of airborne Platanus pollen
counts during the pollen-producing season (Díaz de la Guardia
et al., 1999); not surprisingly, these trees represent one of the main
causes of pollen allergies among local people (Gabarra, Belmonte, &
Canela, 2002; Sabariego-Ruiz, Gutierrez Bustillo, Cervigon Morales,
& Cuesta, 2008).
Members of the Cupressaceae (Cupressus spp., Platycladus sp.,
Calocedrus sp., Chamaecyparis sp., Juniperus spp., and Thuja spp.) are
very common in the city of Granada (southeastern Iberian Penin-
sula), where they are a key element of the city’s famous historic
gardens (Casares, 2010) and feature prominently in various districts
of the Old Town. There are over 3000 Cupressaceae in the city. Due
to the well established allergenic capacity of these species (Charpin,
Calleja, Lahoz, Pichot, & Waisel, 2005) and to their exhibiting some
of the highest pollen production levels of all anemophilous species,
with more than 1100 ×106pollen grains being produced by each
tree (Hidalgo, Galán, & Dominguez, 1999), the incidence of allergic
sensitization is estimated at close to 30%. Additionally, Cryptomeria
japonica (Japanese cedar) is a species of Cupressaceae that is fre-
quently used as a roadside tree along Japanese city streets, and its
pollen is one of the main causes of pollen-related disease in these
areas (Okuda, 2003).
2.2. Sources of pollen emissions
The low species diversity in many towns and cities is directly
linked to the formation of large, concentrated pollen emission
sources. The large-scale use of a small number of roadside tree
species gives rise to the production of large amounts of monospe-
cific pollen that cannot always be dispersed by air currents. In many
cities with a temperate climate, urban green spaces are often char-
acterized by an overabundance of a restricted number of species,
particularly poplars (Populus spp.), willows (Salix spp.), elms (Ulmus
spp.), cypresses (Cupressus spp.), and palm trees (Phoenix spp.). All
of these species act as chimneys, simultaneously releasing large
amounts of pollen into the air during the main pollen season. A good
example of this is presented by Elche, an eastern Spanish town with
one of the largest palm groves in the Mediterranean area, where
the number of pollen-allergy sufferers is among the highest in all
of Spain (Fernandez, 1992).
Another factor that generates pollen emission sources of con-
siderable dimensions is the development of living screens, natural
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Table 1
List of frequent plant species used as ornamental in urban environments with specification of its allergenicity (indicated as * for monoecious species and when dioecius),
as well as other observations of interest in allergy.
Family Species frequent in Mediterranean gardens Allergenicity Dioecious or female cultivars Observations
Aceraceae Acer campestre *
Acer negundo *
Acer pseudoplatanus *
Acer platanoides *
Acer opalus *
Anacardiaceae Cotinus coggygria
Schinus molle *
Schinus therebintifolius *
Pistacia atlantica Dioecious
Rhus coriaria, R. tiphyna Dioecious Female trees can cause contact allergy
Agavaceae Agave spp.
Yucca spp.
Apocynaceae Nerium oleander *
Araucariacaeae Araucaria spp. *
Arecaceae Phoenix dactylifera Dioecious
Phoenix canariensis Dioecious
Washingtonia filifera
Wasingtonia robusta
Trachycarpus fortunei Dioecious
Chamaerops humilis Dioecious
Betulaceas Alnus glutinosa *
Betula spp. *
Carpinus betulus *
Corylus spp. *
Bignoniaceae Catalpa bignonioides
Jacaranda mimosifolia
Thevetia spp.
Caprifoliaceas Sambucus nigra *
Casuarinaceae Casuarina equisetifolia *
Cupressaceae Calocedrus decurrens *
Chamaecyparis lawsoniana *
Cupressus arizonica *
Cupressus lusitanica *
Cupressus macrocarpa *
Cupressus sempervirens *
Cupressocyparis ×leilandii *
Juniperus spp. Dioecious
Platycladus orientalis *
Tetraclinis articulata *
Thuja plicata *
Cycadaceae Cycas spp. ? Dioecious
Eleagnaceae Eleagnus angustifolia *
Ericaceae Arbutus unedo
Euphorbiaceae Ricinus communis * Poisonous, avoid planting near path or
houses, may can cross allergic reaction
to latex
Fabaceae Acacia bayleyana *
Acacia cyanophylla *
Acacia dealbata *
Acacia farnesiana *
Albizia julibrissim Bahuinia sp. Ceratonia silicua
Cercis siliquastrum Polygamous
Erythrina spp.
Gleditsia triacanthos Polygamous Avoid fruitles cultivars as ‘Moraine’,
‘Skycole’ and ‘Suncole’
Robinia pseudoacacia *
Robinia hispida
Sophora japonica
Tipuana tipu
Parkinsonia aculeata
Fagaceae Castanea sativa *
Quercus ilex *
Quercus robur *
Quercus rubra *
Quercus suber *
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Table 1 (Continued)
Family Species frequent in Mediterranean gardens Allergenicity Dioecious or female cultivars Observations
Ginkgaceae Ginkgo biloba Dioecious
Hamamelidaceae Liquidambar styraciflua *
Hippocastanaceae Aesculus hippocastanum *
Aesculus ×carnea
Lauraceae Laurus nobilis Dioecious Avoid cultivars as ‘Saratoga’. It may
cause allergic reaction from contact
with the foliage.
Persea gratissima
Lythraceae Lagerstroemia indica
Magnoliaceae Magnolia grandiflora
Magnolia soulangeana *? All deciduous species may cause
allergic reaction
Liriodendron tulipifera
Malvaceaae Lagunaria patersonii Avoid planting near path or houses,
may can contact reaction with fruits
hairs.
Meliaceae Melia azederach
Menispermaceae Coculus laurifolius Dioecious Poisonous bark, frequent in some olds
gardens XIX S.
Mirtaceae Callistemon spp. *Few capacity of pollen dispersion,
avoid planting near path or houses.
Eucalyptus camaldulensis *
Eucalyptus globulus *
Eucalyptus ficifolia
Metroxyderos spp.
Myrtus communis
Moraceae Broussonetia papyrifera Dioecious
Ficus spp.
Maclura pomifera Dioecious Avoid cultivars as ‘Double O’,
‘Fand’arc’, ‘Altamont’
Morus alba Dioecious Avoid cultivars as ‘Fruitless’,
‘Mapleleaf’, ‘Urbana’
Morus nigra *
Musaceae Musa spp.
Oleaceae Fraxinus angustifolia Polygamous ‘Flame’, ‘Moraine’ an ‘Raywood’ are
cultivars
Fraxinus excelsior Polygamous Avoid cultivars as ‘Gold Cloud’,
‘Hesseri’, ‘Juglandifolia’
Fraxinus ornus Polygamous
Ligustrum lucidum * Few capacity of pollen dispersion avoid
planting near path or houses
Ligustrum japonicum * Few capacity of pollen dispersion avoid
planting near path or houses
Olea europaea * ‘Swan Hill Olive’ and ‘Monher’ are
flowerless cultivars avoid fruitless
cultivars ‘Majestic Beauty’and
‘Wilson’s’
Pinaceae Abies alba
Abies pinsapo
Cedrus atlantica *
Cedrus deodara ‘Repandens’ is a cultivar.
Picea abies
Pinus halepensis
Pinus pinaster
Pinus pinea
Pseudotsuga menziezii
Platanaceae Platanus ×hispanica *
Proteaceae Grevillea robusta * It may cause skin irritation
Pittosporaceae Pittosporum spp.
Phytolaccaceae Phytolacca dioica Dioecius
Punicaecae Punica granatum
Rhamanaceae Rhamnus spp. *
Zizyphus jujuba The fruits may cause food allergic
reaction
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Table 1 (Continued)
Family Species frequent in Mediterranean gardens Allergenicity Dioecious or female cultivars Observations
Rosaceae Chaenomeles speciosa
Malus spp.
Mespilus germanica
Eriobotrya japonica
Photinia serrulata
Prunus cerasifera
Prunus domestica
Prunus dulcis *
Prunus laurocerassus *
Prunus serrulata * The flore pleno varieties are less
allergenic
Pyrus spp.
Sorbus spp
Rutaceae Citrus aurantium
Salicaceae Populus alba Dioecious Avoid var pyramidalis know as bolleana
is . ‘Siberia Extreme˜
na’ and ‘Nivea’
are
Populus ×canescens Dioecious
Populus ×euroamericana Dioecious ‘Regenerata’ is a . Planting
individuals may contaminate the
natural populations of P. nigra
Populus nigra Dioecious Avoid ‘Italica’ is a . In landscapping
may be replaced by “Gigantea”, female,
or female individuals of P. ×canescens
Populus simoni Dioecious
Populus tremula Dioecious Avoid ‘Pendula’ is a
Salix alba Dioecious ‘Cardinalis’ and ‘Caerulea’ are , avoid
‘Crisostela’, ‘Brizensis’, ‘Liempde’ and
‘Tristis’ (=S. ×sepulcralis)
Salix babylonica Dioecious ‘Crispa’(=‘Annularis’) is
Salix caprea Dioecious ‘Pendula’ is ‘Kilmarnock’ is
Salix matsudana Dioecious ‘Torulosa’ and ‘Navajo’ are
Simaroubacee Ailanthus alisssima Polygamous ‘Erytrocarpa’ is
Sterculiaceae Brachychiton acerifolium
Brachychiton discolor The fruits hairs may produce allergic
reaction.
Brachychiton populneum
Firmiana simplex
Strelitziaceae Strelitzia spp.
Tamaricaceae Tamarix spp. *
Taxaceae Taxus baccata Dioecious ‘Adpresa’, ‘Cheshuntensis’, ‘Fastigiata’,
‘Fructu-luteo’, ‘Repandens’ and
‘Washingtonii’ are . Poisonous plant.
Taxodiaceae Cryptomeria japonica *
Metasequoia glyptostroboides
Sequoiadendron giganteum
Sequoia sempervirens *
Taxodium distichum *
Tiliaceae (or Malvaceae) Tilia spp. *Few capacity of pollen dispersion avoid
planting near path or houses
Ulmaceae Celtis Australis *?
Ulmus minor * ‘Gracilis’ is a flowerless cultivar
Ulmus pumila *
Ulmus glabra * ‘Horizontalis’ is a flowerless cultivar
Zelkova serrata *
edges and hedges. In many areas, it is a common practice to
use a single constituent species for numerous purposes, such
as acting as property boundary walls, lining avenues and open
spaces, and the construction of anti-noise barriers. The species
that are most used for these purposes include many members
of the Cupressaceae and other species that successfully support
the development of topiaries, such as privet (Ligustrum spp.), box-
wood (Buxus sempervirens), holly (Ilex spp.), yew (Taxus baccata)
and myrtle (Myrtus communis). Although continuous pruning usu-
ally diminishes flower production, the high economic cost of this
process encourages poor maintenance, which can allow flowers
and, consequently, pollen to be produced. This can also be linked
to proximity pollinosis, as some of these species can produce flow-
ers almost down to their base (Seitz & Escobedo, 2009), and pollen
will, thus, be emitted at human height (Alcázar, Galán, Cari˜
nanos,
& Dominguez, 1999).
The microenvironmental conditions found in a given urban dis-
trict can affect the quality of life of its residents. Comparison of
pollen counts in areas with different degrees of urbanization reveals
differences in terms of the quantity and number of pollen types
recorded (Cari˜
nanos, Sánchez-Mesa, Prieto, López, & Guerra, 2002),
daily pollen cycles (Kasprzyk, 2006; Sikoparija, Radisik, Pejak, &
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210 P. Cari˜
nanos, M. Casares-Porcel / Landscape and Urban Planning 101 (2011) 205–214
Simié, 2006) and plant growth and productivity (Ziska, Bunce, &
Goins, 2004). In a study by Sanchez-Mesa et al. (2005) that related
the sale of antihistamines in different districts of a city to the pollen
content in each of these urban areas, it was observed that the high-
est sales figures occurred in the areas where there was also a large
presence of ornamental trees.
2.3. Introduction of exotic species
Grouped together under this heading are all of the species
growing outside their natural distribution range that have been
introduced principally by man. In this section, we consider those
species with a primarily ornamental function for which expansion
is controlled in urban environments. The introduction of exotic
flora for ornamental purposes has been found to have occurred
in all ancient societies. The discovery of America and the great
explorations of the 18th century gave rise to an unprecedented
flow, leading to allergic responses among both New and Old World
inhabitants (Selvaggio, 1992). Although some authors have recom-
mended the introduction of exotic plants as a preventive measure
to avoid sensitization (Chiesura, 2004), there is evidence showing
that the use of some exotic species as ornamentals in towns and
cities has eventually given rise to new sources of pollinosis for local
residents. The genus Casuarina (Australian pine) comprises approx-
imately 60 species that are mainly native to Australia and southern
Asia. Some of these species have been used as ornamentals, mainly
in coastal cities (Trigo et al., 1999). These wind-pollinated trees
produce large amounts of pollen during the main pollen season,
which generally occurs during late summer and autumn. As a result,
Casuarina has become a cause of autumn pollinosis, thus extending
the period of symptoms for polysensitized patients (Garcia et al.,
1997).
Similar characteristics are reported for a number of Eucalyp-
tus species. This highly adaptable Australian genus has been used
widely for reforestation, and the pollen counts of these trees are
sufficient to cause allergy symptoms (Galdi, Perfetti, Calcagno,
Marcotulli, & Moscato, 2003).
Finally, the potential allergenic capacity of Ginkgo biloba pollen
in the near future should be noted. Ginkgo biloba is considered the
oldest tree species surviving on earth. It is native to eastern China
and was introduced into Europe from China around 1730 and to the
USA in 1784 (Cothran, 2004). This living fossil adapts well to urban
conditions, and its use to line urban thoroughfares has become
fashionable among the Parks and Gardens Departments of many
European and American towns and cities. Gingko biloba is a dioe-
cious gymnosperm with spectacular fan-shaped leaves that turn
gold in autumn. Because its seeds give off an odor of butyric acid,
most of the trees planted are male, and on reaching reproductive
maturity (at approximately 10 years), they release large amounts
of pollen with a demonstrated allergenic capacity (Yun, Si-Hwan,
Jung-Won, & Chein-Soo, 2000).
2.4. Botanical sexism
Ogren (2000) attributed the increasing incidence of pollen aller-
gies in the urban environment to botanical sexism in the process
of selecting ornamental species for many towns and cities. He
correctly noted that “for reasons of convenience, more and more
shrubs, trees and other plants are selected for their ‘litter-free’ char-
acteristics, that is, they are male types and generate few or no seeds
or fruits”. Some of the species that are commonly used in urban
green spaces are dioecious, i.e., individual trees are either wholly
male or wholly female. Fruit production (sometimes partheno-
carpic) in female plants is associated with a number of problems,
including litter, undesirable odor, and slippery ground surfaces. As
a result, there has been a marked increase in the use of male trees,
which are often selected from asexually propagated clones that
are pollen intensive (Ogren, 2002). The dioecious species that are
widely planted in warm areas and exhibit pollen with a demon-
strated allergenic capacity include Salix (Reqi, Xie, & Wei, 2001),
Schinus (Vargas Correa et al., 1991), Acer (Eriksson, 1978), Morus
(Navarro et al., 1997), Ginkgo (Yun et al., 2000), Juniperus (Hrabina,
Dumur, Sicard, Viatte, & Andre, 2003) and some palms of the genus
Phoenix (Blanco et al., 1995). Similar problems are also posed by
certain polygamous species (Table 1), in which hermaphrodite and
monoecious flowers occur on the same tree; some cultivars pro-
duce mostly masculine flowers and, thus, behave in practice like
dioecious species in terms of pollen output. These include certain
species of the genus Fraxinus. As this genus belongs to the Oleaceae
family, it has a high allergic potential related both to compounds
unique to its member (Guerra et al., 1995) and to the presence of
allergens common to other Oleaceae (Pajarón et al., 1997). Addi-
tionally, a problem is posed by the fact that some commercial
varieties are sold as seedless, when in reality they are male or polyg-
amous species. Depending on the sex of the individuals chosen for
planting and on the species, the Allergen Index can reach a max-
imum (Fraxinus americana,F. excelsior,F. nigra,F. pennsylvanica,F.
uhdei,F. velutina) or, if only female varieties exist, a minimum (F.
angustifolia,F. burgeana,F. dipetala)(Ogren, 2000).
2.5. Invasive species
Invaders are non-native plant species introduced by humans,
either accidentally or deliberately, into a given area where they
have effectively become naturalized, i.e., populations are main-
tained and reproduce unaided. The entrance routes for these
allochthonous species are numerous, changing over time according
to the characteristics of each society. Since the 19th century, two
routes have existed that have propitiated the introduction of the
vast majority of naturalized species: accidental introduction (such
as arvenses in crops) and the utilization of species for ornamen-
tal and recreational purposes. This can be illustrated by the case
of Ailanthus altissima (tree of heaven), which has become popular
as a roadside tree in many cities and for which rapid propagation
has been observed. Its abundance in some areas has been found to
generate pollen sensitization reactions in some patients (Ballero,
Ariu, Falagiani, & Piu, 2003). Among the most common invaders
are also species belonging to two of the families with the great-
est allergenic potential, Poaceae and Asteraceae, which represent
an additional source of sensitization for an already overexposed
population (Campos Prieto, Herrero Gallastegui, Biurrum, & Loidi,
2004; Mandal, Roy, Chatterjee, & Gupta-Bhattacharya, 2008).
Other less common invaders have also been linked to aller-
genic potential, including members of the Fabaceae (Radauer &
Breiteneder, 2006), Myrtaceae (Boral & Bhattacharya, 2008), Ama-
ranthaceae (Galan et al., 1989), Polygonaceae (Spieksma, Charpin,
Nolard, & Stix, 1980) and Zygophyllaceae (Belchí-Hernandez et al.,
2001). Some of these species are now used as urban ornamentals,
such as Acacia dealbata,Acacia saligna,Acer negundo,Gleditsia tria-
canthos,Robinia pseudoacacia and Parkinsonia aculeata (Dirr, 1990;
Griffith, 1994).
Of more global note is that, in the list of 100 of the World’s
Worst Invasive Alien Species, published by the IUCN/SSC Invasive
Species Specialist Group, a number of species with a high aller-
genic potential according to some of the existing scales are found
in the section on terrestrial plants (Ogren, 2000). These species
include Acacia mearnsii,Schinus terebinthifolius (the most allergenic
species of the genus Schinus, introduced for its tolerance to drought
in many cities with harsh summers), Cecropia peltata,Arundo donax,
Ligustrum robustum,Chromolaena odorata and Tamarix ramosissima
(Sellers, Simpson, & Curd-Hetrick, 2010).
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nanos, M. Casares-Porcel / Landscape and Urban Planning 101 (2011) 205–214 211
2.6. Management and maintenance
The presence of wasteland and neglected garden areas, with
sizes that often surpass the conservation capacity of local author-
ities, provides opportunist species with a chance to make use of
the available resources; space, water, and fertilizer thus cease to
be limiting factors and encourage the spread of plants with severe
pollen-allergy implications. Urticaceae are the main offenders in
this respect, particularly Parietaria in terms of allergenic poten-
tial (Trigo, Fernandez-Gonzalez, Jato, Galan, 2008). This species is
also known as lichwort or pellitory-of-the-wall, and its preferred
habitat is the walls of old or derelict buildings on highly disturbed,
nitrified soil. It responds rapidly to even a minimal water supply
and spreads faster than it can be eradicated using routine manage-
ment and maintenance strategies. Due to its rapid spread and the
small size of its pollen grains, Parietaria is among the major aller-
genic pollen types found in the Mediterranean region (D’Amato &
Spieksma, 1992).
These problems are exacerbated when species cover the walls
of buildings designated as having Cultural Heritage status. In a
study carried out on periodic changes detected in the spontaneous
flora of the Coliseum in Rome from 1643 until 2001, among more
than 200 species inventoried over this period, members of the
Asteraceae, Chenopodiaceae/Amaranthaceae, Poaceae, Urticaceae,
Plantaginaceae and Poligonaceae families stood out as being among
the most abundant. In addition to being indicative of the extraor-
dinary capacity of these plants for colonization and of the difficulty
of eradicating them, the abundance of these species can also repre-
sent a problem for visitors suffering from allergies who are forced
to leave the monument each year (Caneva, Ceschiu, Pacini, & Vinci,
2004).
Intensive urban development has not only changed the land-
scape and the skyline in many cities, but has also created urban
wastelands in the form of building sites that have remained unde-
veloped, especially in times of crisis, providing marginal plants
with a niche that meets their requirements. Species associated
with these sites include numerous members of the Amaranthaceae
family, some of which are considered among the most detrimen-
tal widespread weeds with proven allergenicity (Cari˜
nanos, Galan,
Alcazar, & Dominguez, 2000). These sites can be included in the
so-called “third landscape” (Clément, 2007), which are residual
spaces generated by town planning, agriculture or other anthropic
uses of territory and which constitute important refuges of diver-
sity. Rather than seeking to eliminate this spontaneously growing
vegetation, management of these sites should be characterized
by selective maintenance, encouraging colonization by diverse
naturally occurring species and avoiding the establishment of
monospecific populations of allergenic species.
2.7. Proximity pollinosis
This term refers to all allergic processes in which proximity to
the pollen source plays a decisive role, either through close physical
contact with a given plant species or in workplaces or homes close
to such sources.
Privets (Ligustrum spp.) are a good example of this phenomenon.
They are members of the Oleaceae, and therefore, they are closely
related to Olea, which is the main allergy-causing species found
in Mediterranean countries. However, unlike Olea, privets are
insect-pollinated. Their pollen grains are large and heavy and their
dispersal from the tree after being released is quite limited (Trigo
et al., 2008). Another important characteristic of these species is
that their flowering period overlaps with the last stages of the flow-
ering period of olive trees. The fact that the two pollen types share
common allergens means that there are cross-reactions between
them, but, whereas olive pollen can travel long distances from its
source (Galan et al., 2008), the allergic reactions prompted by Ligus-
trum appear only close to the source (Cari˜
nanos, Alcázar, Galán, &
Dominguez, 2002). Similar findings have been reported for Phyto-
lacca dioica, also known as “ombú” or “bella sombra”, which is a
tree native to the South American Pampas that is widely cultivated
in temperate cities throughout the world. Despite being dioecious
exhibiting entomophilous pollination (Table 1), cases of patients
with rhinoconjunctivitis and wheezing caused by the pollen of this
species have been reported (Drago, Pineda de la Losa, & Guspi-Bori,
2007). This characteristic has also been noted for Pyrus pirifolia
(Karamloo et al., 2001) and Tilia (Mur et al., 2001).
2.8. Establishment of cross reactions
The response of the immune system to the inhalation of pollen
grains is due to the presence of allergens, usually proteins, which
are mostly located on the pollen wall, and these are generally spe-
cific (Barber, 2003). The pollen wall also harbors a number of minor
allergens that act as panallergens, i.e., that are present in vari-
ous species and responsible for the appearance of pollen–pollen
cross-reactions (Weber, 2003). Knowledge about the patterns of
cross-allergenicity between different pollen types is essential for
the identification of many allergic symptoms for which there is no
apparent cause. Weber (2003) noted that pollen cross-allergenicity
is due to interrelationships at two levels: taxonomical and phylo-
genic; i.e., more closely related plants will have a greater number
of shared antigens. This has been clearly demonstrated in numer-
ous plant groups. Studies involving up to 12 different species of
Cupressaceae, which include the genera Juniperus,Thuja,Cupressus
and Chamaecyparys, have found cross-reactivity among all 12, as
well as between these species and Pinaceae species, such as Cedrus
deodara (Schwietz, Goetz, Whisman, & Reid, 2000).
Certain proteins present in Pinaceae pollen grains (Pinus spp.,
Picea spp., Abies spp., and Pseudotsuga spp.) display cross-reactivity
with ryegrass (Lolium perenne, Poaceae) proteins (Conford,
Fountain, & Burr, 1990). A number of studies on grasses, which
are species that produce pollen that is a major cause of allergies,
have revealed strong cross-reactivity between members of a par-
ticular subfamily (Martin, Mansfield, & Nelson, 1985), as well as
between members of different subfamilies (Smith, Xu, Swoboda,
& Singh, 1997). The most surprising finding with respect to cross-
reactivity is an elevated percentage of reaction with oilseed rape,
Brassica napus (Smith et al., 1997), and almost 44% homology with
the major olive allergen Olee1(Asturias et al., 1997).
Olive pollen, which is considered one of the main allergenic
pollen types in the Mediterranean region, not only shares com-
mon allergens with other Oleaceae species, such as ash, privet and
syringa (Martin Orozco et al., 1994) but also shares panallergens
with numerous species present in green spaces, including Eleag-
nus angustifolia (Kernerman, McCullough, Green, & Ownby, 1992),
castor bean (Ricinus)(Vallverdi et al., 1998) and Plantago (Castro,
Alché, Calabozo, Rodriguez, & Polo, 2007). Some authors have
reported homology between Oleaceae, Fagaceae and Betulaceae
allergens, thus expanding the potential range of species exhibiting
cross-reactivity to include a number of commonly planted genera,
such as Quercus,Castanea,Juglans,Carya,Betula,Alnus and Corylus
(Eriksson, 1978; Niederberger et al., 2002; Valenta et al., 1991). A
number of proteins isolated from Betulaceae species harbor aller-
gens similar to those found in other trees, grasses and herbs (Hayek
et al., 1998), which indicates the potential scope of allergic sensiti-
zation linked to urban ornamental flora.
2.9. Interaction with air pollutants
One environmental factor that clearly distinguishes towns and
cities from the rural environment is the considerable presence
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212 P. Cari˜
nanos, M. Casares-Porcel / Landscape and Urban Planning 101 (2011) 205–214
of air pollutants. Human activities, especially automobile traffic,
have created sources of pollution posing a serious threat to health
(Kim, Back, Koh, & Cho, 2001). Many authors have reported that
urban air pollution is one of the main reasons why there are more
allergy sufferers in cities than in rural areas (D’Amato, Liccardi,
& D’Amato, 2000). There are also experimental and epidemiologi-
cal data supporting the association between residential proximity
to fine particles and sources of emissions with allergic sensitiza-
tion and asthma in primary school children (Annesi-Maesano et al.,
2007).
Some authors have noted that the allergenic potential of pollen
grains may be enhanced by the presence of other air pollutants
and that pollen production in species with considerable allergenic
potential has actually increased due to the action of gases such as
CO2(Rodriguez-Rajo, Fernandez-Sevilla, Stach, & Jato, 2010; Ziska
et al., 2004). The exposure of pollen grains to agitation by air and
air pollutants generates paucimicronic allergen particles measur-
ing less than 2.5 m, which are capable of penetrating into the
lower regions of the respiratory tract (Rantio-Lehtimaki, Viander, &
Koivikko, 1994; Spieksma, Nikkels, & Dijkman, 1995). Pollen grains
are considered the major biological cause of air quality deterio-
ration because they behave in a similar manner to non-biological
airborne contaminants, are associated with high counts, and are
damaging to human health (Cari˜
nanos et al., 2004).
A number of reports have highlighted the coadjuvant effect of air
pollution on pollen-allergy sufferers: air pollutants lead to a wors-
ening of allergy symptoms (D’Amato, Liccardi, D’Amato, & Cazorla,
2001) and appear to have implications for airborne allergen activity,
especially in recent times. In certain situations, pollen grains may
carry micrometer-sized particles into the respiratory tract, thus
increasing their allergenic potential (Bartra et al., 2007; Kalbande,
Dhadse, Chaudhari, & Wate, 2008).
3. Guidelines for designing spaces with a low allergy impact
The effects of the ornamental flora in urban green spaces on the
development of pollinosis by city inhabitants is extensively docu-
mented in the bibliography, and many of the recommendations that
have been put forth for reducing its impact on health are directed
toward reducing exposure to pollen, limiting outdoor activities dur-
ing the pollen season, staying inside during peak pollen periods or
wearing a dust mask (Seitz & Escobedo, 2009). The establishment of
prevention strategies aimed at the general public is also promoted
in the literature, including the dissemination of local aerobiological
information, avoidance of contact with allergens, hygiene and pro-
phylaxis measures and relocation away from primary residences
to areas with different vegetation at times of maximum pollina-
tion (Spanish Aerobiology Network (REA) web page). Only recently
have initiatives begun to be implemented with the aim of reduc-
ing the impact of transmission sources, e.g., Allergy-free Gardening
(Ogren, 2000), and these are most often focused on selecting species
with a low or moderate allergenic potential and using females of
species with separate sexes, resulting in the so-called “female gar-
dens” (Ogren, 2002). Here, we list some of the key measures that we
have concluded should be adopted to reduce the impacts of aller-
genic plant pollen and alleviate its harmful effects on urban allergy
sufferers, as well as provide recommendations on the planning and
design of healthy green spaces, as follows (Table 2):
(a) Increase urban biodiversity. This measure has been strongly
urged as a priority by a number of specialist groups, including
biologists, ecologists, landscape gardeners, and conservation-
ists. Increased biodiversity would reduce the planting of
traditional species for which allergenic capacity has been clearly
demonstrated; at the same time, it would disperse current large,
Table 2
Guidelines to design green spaces of low-allergy impact.
(a) Increase plant biodiversity
(b) Ensure moderate, controlled introduction of exotic flora
(c) Control of invasive species
(d) Avoid massive use of male individuals of dioecious species (avoid
botanical sexism)
(e) Choose species with low-to-moderate pollen production
(f) Adopt appropriate management, maintenance and gardening
strategies to ensure removal of opportunist and spontaneous species
(g) Avoid forming large focal pollen sources and screens by respecting
planting distances
(h) Obtain expert advice when selecting suitable species for each green
area, and avoid fostering cross-reactivity between panallergens
(i) Establish specific local authority by-laws ensuring that sufficient time
is available for the design and planning of urban green spaces
concentrated monospecific pollen sources, potentially reducing
the release of allergenic pollen by up to 30%.
(b) Ensure the moderate, controlled introduction of exotic species.
Large-scale planting of exotics has sometimes given rise to new
pollinoses; the overuse of exotics and their use as exclusive
roadside species should, therefore, be avoided. However, the
controlled incorporation of some exotic species can be a valid
strategy for increasing floral diversification.
(c) The incorporation of new species must also involve an exhaus-
tive verification that they are not referred to as invasive species
in localities of similar ecological characteristics to the intended
sites of their planting.
(d) Encourage botanical “gender equality”. Replace male individuals
of dioecious species with females; this does not alter esthetics
and does not always entail fruit-litter problems; for example this
could be carried out for Salix,Juniperus,Acer,Schinus or Fraxinus.
(e) Choose species associated with low-to-moderate pollen produc-
tion. Not all anemophilous species produce the same amount of
pollen. More frequent use of entomophilous species would also
help to reduce pollen counts.
(f) Ensure proper management and maintenance of green areas and
encourage the presence of “third landscape” sites facilitating the
selective colonization of diverse and vagrant species to limit the
presence of spontaneous low-diversity populations producing
allergenic pollen.
(g) Respect minimum planting distances between trees and min-
imum distances between trees and buildings, thus limiting
the screen effect and the likelihood of proximity pollinosis.
Greater knowledge of pollen types will help ensure that aller-
genic species with a low dispersal capacity (Ligustrum,Tilia) are
planted in areas further away from thoroughfares, homes and
offices.
(h) To reduce cross-reactivity between different pollen types, the
principle of “resemblance and relatedness” underlying phyloge-
netic classifications, i.e., members of the same genus and family
are very likely to share major allergens and panallergens, should
be considered. Species that are not particularly closely related,
but that share common phylogenetic ancestors may also share
common panallergens.
(i) Ensure that local by-laws establish guidelines for the design
of urban green spaces with a low allergy impact; this would
improve advanced planning efforts when choosing the species
best suited to every green space. It is also essential to involve
expert advisers at the planning stage.
4. Conclusion
The analysis carried out in this review of the principal factors
that have contributed to the allergenic characteristics of ornamen-
tal flora makes it clear that there is a need to implement planning
Author's personal copy
P. Cari˜
nanos, M. Casares-Porcel / Landscape and Urban Planning 101 (2011) 205–214 213
of low impact green zones based on the principles of biodiversity,
the prevalence of female varieties and the use of autochthonous
species. Only in this way will we be able to achieve sustainable
and healthy spaces for all urban inhabitants who suffer from pollen
allergies. Additionally, expert participation in the teams involved
in the design and planning of green zones is of equal importance.
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... Thus, the allergenic capacity for a given species was established using allergenicity lists and indices for common urban plant species (Cariñanos et al., 2011(Cariñanos et al., , 2014Hruska, 2003;Ogren, 2000;. This value ranges from 0 for non-allergenic species to 4 for species with a very high referenced allergenic potency (for example, olive pollen in the Mediterranean region). ...
... In terms of the tree species composition, 17% of the most abundant species are highly allergenic and corresponding to only two species, while moderate allergenic potential corresponds to 28% of the most abundant trees comprised of three species (Table 3). The distribution, abundance, and composition of tree species across a city influences the pollen emissions and concentrations in specific areas, given that species composition is one of the main strategies in minimizing the allergenic impact and ecosystem disservices of green areas (Cariñanos & Casares-Porcel, 2011). Species distribution is not only important at the city scale but also at finer scale, where distribution should also be accounted for, since higher socioeconomic strata tend to show greater tree diversity than lower socioeconomic strata (Escobedo et al., 2015). ...
... and Ligustrum spp. (Cariñanos et al., 2002) and other native and exotic species (e.g., Chionanthus spp.) needs to be considered in long term urban forest planning (Cariñanos & Casares-Porcel, 2011). The trade-offs between short term (e.g., increase canopy cover, reforestation and aesthetics) versus long-term objectives (biodiversity and allergies) Fig. 3. Percent public tree cover for the most abundant species (i.e., 50-55% of the localities' tree population) with high, moderate, low, and unclassified allergenicity (NA) Allergenicity Potential Values (APV) in localities with a high occurrence of low-income Strata 1 and 2 neighborhoods in Bogota Colombia. ...
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... ▪ Allergenic pollen can undermine health (Smith 1981;Beckett et al. 1998;Cariñanos and Casares-Porcel 2011;Säumel et al. 2016;Eisenman et al. 2019;Hewitt et al. 2020). Climate change and air pollution have led to the increased production of pollen in some tree species (Cariñanos and Casares-Porcel 2011). Allergies due to pollen can decrease the quality of life of urban dwellers, and allergen exposure has been linked to ill health conditions such as cardiovascular disease, pneumonia, and asthma (Curtis et al. 2006). ...
... When pollen grains (as airborne PM) interact with other air pollutants, they can be modified, enhancing their allergic potential as well as their penetration potential into the respiratory tract . Exposure to air pollutants can also exacerbate allergy symptoms ( Jianan et al. 2007;Cariñanos and Casares-Porcel 2011). ...
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... If necessary precautions are not taken, it can turn into diseases such as sinusitis, bronchitis, otitis media and asthma. Plant species that are commonly used in cities due to poor landscaping methods cause a variety of issues, including allergic rhinitis, colds, asthma, and even heart disease (Cariñanos & Casares-Porcel, 2011). ...
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Originally released in April, 2004. Updated again in July, 2010. Now maintained as a "living document" or database online at: http://www.gisin.org/GISINList.htm
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