How to Select Appropriate Plants for Allergic Children

Pollen-related respiratory allergy has a significant impact on global public health, as
it involves around one-quarter of the general population. On the other hand, green areas
are of pivotal importance in improving the quality of life through a multitude of effects.
Therefore, adequately selecting plants for the urban and country landscape represents
an important preventive measure to reduce the burden of the disease. This review aims
to summarize the characteristics of the allergenic plants and the measures that can be
taken to reduce their impact on public health. The degree of allergenicity of plants can
be predicted according to various tools, e.g. the Ogren Plant Allergy Scale (OPALS) and
the criteria by the American Academy of Allergy, Asthma & Immunology. In brief, noninvasive,
non-toxic, entomophilous plants (i.e. insect-pollinated flowers) should be the
preferred ones. Interventions aimed at reducing the impact of pollen allergy should
include both a correct selection of plants and simple individual preventive measures.
In conclusion, better understanding how pollen-related respiratory allergy impacts on
global public health and defining criteria to adequately choose plants for the landscape
is of paramount importance to improve quality of life for children and adults with
respiratory allergies.


Introduction
Around 30% of the world population suffers from allergic pollen-related diseases [1], constituting an important clinical problem for affected individuals and carrying substantial costs for the healthcare system. In Europe, more than 150 million citizens have chronic allergic diseases, implying costs up to 151 billion euros per year [2] for the National Health Services. This is one of the main health issues at present, and will probably worsen exponentially in the next years, as a result of climatic change and growing urbanization, industrialization, and pollution [3]. Green areas are a qualifying element of urban environment and represent an added value, both in terms of health and economics, given its multiple effects [4]: the regulation of the microclimate through increased evaporation and perspiration, the protection from landslides and the control of river banks, and last but not least the possibility of creating a meeting and association area. The amount of green per capita is an important index to define the quality of life in a city. Green can also improve the physical and psychological well-being of people [5]. However, on the other hand, green can have negative effects, as it happens for patients with pollen allergy.
The prevention of respiratory allergic diseases is therefore an important goal and also a challenge for the scientific community.
Complex and still inconclusive studies are being carried out aimed at identifying primary and secondary preventive measures [6,7].
An example of primary prevention might be to avoid that a newborn baby with at least one parent with allergy (therefore considered at risk) becomes allergic. An example of secondary prevention might be to prevent symptoms in people who are already sensitized to an allergen. In this latter topic, the characteristics of the environment in which we live, both indoors and outdoors, play an important role. The Asthma and Allergy Foundation of America (AAFA) [8] periodically indicates which cities have the highest pollen load in the different seasons of the year, in order to adopt appropriate preventive measures and therapies. Allergies are the sixth leading cause of chronic disease in the United States according to the Center for Disease Control and Prevention [9] and represent a health cost of 18 billion dollars. The promotion of a "low allergenic charge environment" may not be easily carried on but is not unfeasible. To achieve this goal, it is important to spread the knowledge related to the pathogenetic mechanisms of allergy, as well as the life cycle of plants that are most often implied in allergic manifestations [10].

Plants and Pollen
Pollens in the atmosphere are the key element (male gametophyte) for the reproduction of seed plants. The pollen grain has a protective layer made up of two walls: an external (hexin) and an internal (intin) wall. When the pollen is mature, it is released for pollination and can reach the female part of the flower, carried by the wind (anemophilous plants) or through insects (entomophilous plants), water, birds and other animals [11]. Pollens that can cause allergies in general have some common characteristics [12]: a. They belong to anemophilous plants, b. They contain allergenic components that stimulate the immune system of the allergic subject genetically predisposed to produce specific antibodies, c. They have to be produced in large quantities from plants widespread in the area, and d. They have to be small and light in order to be carried by the wind at a great distance [13].
The wall of the pollen grains has numerous proteins that allow the recognition of the granule by the female part of the flower.
These same proteins are responsible for allergic reactions in genetically predisposed sensitive subjects, acting as antigens and stimulating the immune system to produce antibodies (IgE). When antibodies and antigens meet, chemical mediators are produced, including histamine, triggering the inflammatory process underlying allergic symptoms, e.g. rhinitis, conjunctivitis, asthma [11]. Some plants (monoecious) have male and female flowers on the same plant, others (dioecious) are male or female: the latter, i.e. the dioecious, are the most allergenic. Mosses and ferns produce pollens that propagate in the surrounding environment, unlike conifers (which belong to gymnosperms) and other plants with flowers (angiosperms); the latter produce large quantities of pollen which spread at considerable distances. Plants with flowers or angiosperms can have different morphologies: ancestral magnoliatype flowers, inconspicuous flowers such as Grasses and Ambrosia, complex flowers such as orchids and sunflowers.
A "perfect" plant for allergic people is the one that has male and female parts in the same flower as tulip, poppy, orchid and magnolia [13]. In the anemophilous angiosperm plants often petals and sepals of the flower are absent or vestige only, and the male part is separated from the female; the flowers constitute inflorescences, that is groups of flowers together like oaks, birches and mulberries.
A list of main anemophilus plants that cause allergies is shown in Table 1. Finally, it must be remembered that pollution, especially the particles derived from diesel combustion, increases the allergenicity of pollen. A particular mention is deserved by the Grasses, Ambrosia, and the Parietaria as they produce the highest quantity of clinically relevant allergens. The concentration of the various types of pollen in the atmosphere depends above all on the presence and diffusion of the plants on the territory, as well as on some environmental parameters such as wind, humidity, temperature and atmospheric turbulence. Climate change also affects pollen: the increase in temperatures is associated with lengthening and anticipation of the pollen season, the distribution and establishment of pests and contributes with high concentrations of CO 2 to the increase in pollen production [14,15].

Grasses
This family includes about 9,000 species spread all over the world; some are annual because they produce seeds over a year, others are perennial because they live for several years and produce seeds several times. In unfavourable situations, perennials have the aerial part that emerges from the completely dry soil,

Parietaria
The genus Parietaria belongs to the Urticaceae family and is typical of temperate and tropical regions. They are annual or perennial herbaceous plants reaching 20-80cm of height. The leaves are alternate, simple, entire, often with a cluster of small leaves in their axils. Flowers are produced in clusters of three to many in the leaf axils, and can either be bisexual or both male and female. The fruit is a small dry achene. The term Parietaria stems from the Latin paries, i.e. wall, as it tends to grow onto old walls. Parietaria pollen is the most important cause of pollen allergies in the Mediterranean area, as the plant is common in this region [16]. The Parietaria pollen mean diameter is measured in micrometres and is larger than 10mm. Thus, the grains generally induce inflammation in the upper airways and bronchi, whereas they cannot reach the terminal bronchioles. A recent study addressing the seasonality of Parietaria pollination found that it lasts 6-7 months on average, with two main peaks during mid-spring and early fall, respectively [17].

Impact of Climate Change on Pollens
Human activities and industrialization have led to an increase in atmospheric greenhouse gases and climate change. Indeed, CO 2 atmospheric concentration has risen from 280 p.p.m. in 1750 to more than 370 p.p.m. in 2002, whereas global average surface temperature has turned up by 0.6 °C [18]. Projections estimate that CO 2 concentration and temperature increase will top at around 541-970 p.p.m. and 1.4-5.8 °C by 2100 [18]. This epochal climate change is exerting a significant impact on aeroallergen-mediated allergy by a multitude of effects, i.e. pollen amount, pollen allergenicity, pollen season, and plant and pollen distribution [19,20]. Two studies found a significant increase in the production of pollen by Ambrosia, paralleled by the rise in CO 2 atmospheric concentration [21,22]. Ahlholm, et al. [23] examined the amount of the pollen allergen Bet v 1 produced by mountain birch (Betula pubescens) grown at two different temperatures and found significantly higher allergenicity for the trees at higher temperature [23]. Two Italian studies reported an earlier start of the pollen season related to a warming in temperature over the years 1981-2000 [24,25]. Last, Kelly, et al. [26] found that the average altitude of the allergenic plants in Southern California increased by 65m between 1976 and 2006, thus augmenting pollen production; this shift was attributed to an increase in average surface temperature [26].

How to Define the Allergenicity of a Plant
Despite all the limitations of a relatively refined stratification, a book published by the botanist Thomas Ogren entitled "The allergy-fighting garden" ranks the potential allergenicity of plants (OPALS Allergy Index Scale) [27]. Plants are categorized from slightly allergenic (1 or 2) to highly allergenic (9 or 10)  The selection of plants for the landscape can be a difficult task.

How to Select Low Allergenic Plants for the Landscape
There are many recommendations on the least allergenic species to choose, depending on whether the climate is dry or wet (13,30). Tables 1-3 show a list of grass and plants to be avoided and chosen, respectively. In case of doubts on a plant which is not mentioned, a simple algorithm can be adopted (Figure 1 [13,28].

Species Family Short Features
Ilex opaca Aquifoliaceae It is an evergreen tree, belongs to the agrifolio family. The winter buds are brown, short, dull or sharp.

Cornus florida Cornaceae
It includes shrubs or trees, with deciduous leaves. It is a fairly rustic plant and is used in isolation, in groups or to form hedges.

Cornus sanguinea Cornaceae
The species spreads by seeds and stolons. Its natural range covers most of Europe and western Asia. It is especially abundant in riversides, especially in shady areas and ravines.

Diospyros kaki Ebenaceae
It is among the oldest cultivated plants, having been in use in China for more than 2000 years.

Diospyros virginiana Ebenaceae
The tree grows wild but has been cultivated for its fruits and wood since prehistoric times by Native Americans. Its fruit is a kind of persimmon.

Kalmia latifolia Ericaceae
Native to North America, where it grows spontaneously in fresh woods, under the foliage of large trees; it is a magnificent evergreen shrub.

Baptisia australis Fabaceae
It is a perennial, attractive green-blue foliage; the flower is blue-lilac, its flowering period is June -August.

Sophora japonica Fabaceae
Deciduous tree with erect bearing, vaguely resembling Robinia, slowly reaches 20 m in height.

Cercis canadensis Fabaceae
It reaches 11 meters in height, the width is greater than 8 meters, has considerable resistance to cold.

Sassafras albidum Lauraceae
Sassafras is a shrubby plant common in North America; from the root an essential orange-yellow oil is obtained.

Liriodendron tulipifera Magnoliaceae
It is an often multi-stemmed, deciduous tree with a wide spreading, flat topped, rounded, or even spike shaped open habit. The tree is a popular nesting shrub for songbirds.

Magnolia grandiflora Magnoliaceae
Although endemic to the lowland subtropical forests on the Gulf and south Atlantic coastal plain, magnolia grandiflora is widely cultivated in warmer areas around the world. The timber is hard and heavy, and has been used commercially to make furniture, pallets, and veneer.

Liriodendron tulipifera Magnoliaceae
The liriodendro or Tulip tree sometimes exceeds 30 m in height with cupped flowers similar to those of the tulip.

Magnolia soulangeana
Magnoliaceae It is a cultivation hybrid obtained from the French agronomist Soulange-Bodin.

Magnolia soulangiana
Magnoliaceae It is a hybrid plant. Its flowers emerge dramatically on a bare tree in early spring, with the deciduous leaves expanding shortly thereafter, lasting through summer until autumn.

Magnolia stellata Magnoliaceae
The tree blooms at a young age, with the slightly fragran flowers covering the bare plant in late winter or early spring before the leaves appear. The flowers are star-shaped.

Forsythia viridissima Oleaceae
It is a deciduous Shrub growing to 2.5 m.

Chionanthus virginicus Oleaceae
Its name is evocative: it means from the Greek "flower of snow", rustic tree. It does not fear the most intense frosts, it does not suffer from particular diseases, it is almost never attacked by parasites.
Amelanchier arborea Rosaceae Native to North American. The fruit is a berry similar to blueberry, with a sweet taste reminiscent of gooseberries.

Crataegus monogyna Rosaceae
It is a species of hawthorn native to Europe, northwest Africa and western Asia. It has been introduced in many other parts of the world. It can be an invasive weed.

Eryobrotrya japonica Rosaceae
It is a large evergreen shrub or tree, grown commercially for its yellow fruit, and also cultivated as an ornamental plant.

Malus domestica Rosaceae
It is a deciduous tree that produces apples.

Mespilus germanica Rosaceae
It is a large shrub or small tree, and the name of the fruit of this tree.

Prunus laurocerasus Rosaceae
It is an evergreen species of cherry, native to regions bordering the Black Sea in southwestern Asia and southeastern Europe, from Albania and Bulgaria east through Turkey to the Caucasus Mountains and northern Iran.

Crataegus phaenopyrum Rosaceae
It is a species of hawthorn commonly known as Washington hawthorn. It is widely cultivated as an ornamental plant and can reach 10 m in height. The red berried fruits have a delicate flavor, eaten raw or cooked.

Pyrus communis Rosaceae
It is a species of pear native to central and eastern Europe and southwest Asia. It is one of the most important fruits of temperate regions.

Spiraea vanhuttei Rosaceae
It is a vase-shaped, deciduous shrub with branching that arches toward the ground. It is a hybrid.  [13,28].

Species Family Short Features
Ilex opaca Aquifoliaceae It is an evergreen tree, belongs to the agrifolio family. The winter buds are brown, short, dull or sharp.
Polygonatum odoratum var Asparagaceae Perennial herbaceous plant, also called Solomon's seal; present in the woods.

Aster tataricus Asteraceae
Perennial plant, erect bearing, the flower is light blue purple with a yellow center, its flowering period is October -November.

Boltonia asteroides Asteraceae
It is a perennial, elongated greyish-green foliage, the flower is white; its flowering period is July -September.

Coreopsis verticillata Asteraceae
It is a plant with bush development, which can reach 90 cm in height, slowly expanding through underground rhizomes. The flower head is yellow Echinacea purpura Asteraceae Perennial plant native to North America with ornamental and herbal interest.
Berberis julianae Berberidacee Native to Central Chine. It is an compact evergreen shrub with rigid, glossy elliptic leaves and racemes of yellow flowers, tinged with red, in late spring. Bloomy black berries in autumn

Mahonia acquifolium Berberidacee
Native to Western North America. It is an evergreen shrub with pinnate leaves consisting of spiny leaflets, and dense clusters of yellow flowers in early spring, followed by dark bluish-black berries

Radicans tecoma Bignoniacee
It is commonly called trumpet vine or trumpet creeper, is a dense, vigorous, multi-stemmed, deciduous, woody, clinging vine that attaches itself to structures and climbs by aerial rootlets. It is native to the Southeastern America including Missouri, but has naturalized in many northern states.

Lobelia cardinalis Campanulaceae
Perennial plant typical of humid places and with beautiful scarlet flowers, it adapts very well to living in the waters of temperate aquariums.

Chimonanthus praecox Calycanthaceae
It is a vigorous deciduous shrub with strongly scented pendent flowers.

Viburnum opulus Caprifoliaceae
The common name 'guelder rose' relates to the Dutch province of Gelderland, where a popular cultivar, the snowball tree, supposedly originated. It is a deciduous shrub.

Viburnum rhytidophyllum Caprifoliaceae
It is an evergreen shrub. Produces flat cymes of creamy white flowers in the spring and berries in early fall which first appear red and then change to a glossy black.

Viburnum tinus Caprifoliaceae
It is a dense, evergreen shrub with dark and oval, glossy leaves, which contrast beautifully with fragrant pinkish-white flowers, followed by dark black fruit.

Sedum ternatum Crassulaceae
Perennial plant with round foliage; the flower is white.

Ginkgo biloba Ginkgoaceae
Native to China, the tree is widely cultivated, and was cultivated early in human history.

Lavandula angustifolia Labiatae
It is popular for its colourful flowers, its fragrance, and its ability to survive with low water consumption.

Rosmarinus officinalis
Labiatae It is an aromatic evergreen shrub with leaves similar to hemlock needles. It is native to the Mediterranean and Asia, but is reasonably hardy in cool climates.
Caratonia siliqua Leguminosae Native to the Mediterranean region and the Middle Easts, it is widely cultivated for its edible pods, and as an ornamental tree in gardens and landscapes.
Cercis siliquastrum Leguminosae It is commonly known as the Judas tree or Judas-tree,is a small deciduous tree from Southern Europe and Western Asia which is noted for its prolific display of deep pink flowers in spring.

Gleditsia triacanthos Leguminosae
It is a deciduous tree, native to central North America where it is mostly found in the moist soil of river valleys.

Sophora japonica Leguminosae
It is native to China; despite the name, it was introduced in Japan. It is a popular ornamental tree in Europe, North America and South Africa, grown for its white flowers, borne in late summer after most other flowering trees have long finished flowering.

Lagerstroemia indica Lythraceae
It is a very popular flowering shrub/small tree in mild-winter states.

Hibiscus syriacus Malvaceae
It is a hardy deciduous shrub. It is upright and vase-shaped, bearing large trumpet-shaped flowers with prominent yellow-tipped white stamens.

Ficus carica Moraceae
It is an Asian species of flowering plant in the mulberry family, known as the common fig.

Maclura pomifera Moraceae
It is a small deciduous tree or large shrub, The fruits secrete a sticky white latex when cut or damaged.

Musa basjoo Musaceae
It is a herbaceous perennial. The species produces male and female flowers on the same inflorescence which may extend for over 1 m.

Trachycarpusa fortunei Palmae
It is a species of hardy evergreen palm tree.

Penstemon digitalis Plantaginaceae
Evergreen perennial plant, beautiful large foliage, slightly wavy; the flower is white.

Phlox divaricate Polemoniaceae
Plants native to America and Asia. The herbaceous stem ends with numerous tubular flowers, variously colored and speckled, of great decorative effect.

Punica granatum Punicaceae
It is a fruit-bearing deciduous shrub. It is grown for its fruit crop, and as ornamental trees and shrubs in parks and gardens. Mature specimens can develop sculptural twisted-bark multiple trunks and a distinctive overall form.

Helleborus orientalis Ranuncolaceae
It is also called Christmas Rose, because it blooms between December and February, as soon as warm days occur during the winter.

Heuchera micrantha Saxifragaceae
Evergreen with beautiful lobed leaves and erect racemes of small tubular flowers. It is mainly cultivated for highly ornamental foliage throughout the whole year.
Paulownia tomentosa Scrophulariaceae It is an extremely fast-growing deciduous tree, and is a persistent exotic invasive in North America.

Tamarix gallica Tamaricaceae
It is a deciduous, herbaceous, twiggy shrub or small tree reaching up to about 5 meters high.

Conclusion
Allergic diseases are constantly increasing so all the possible measures must be implemented to reduce their clinical potential, intervening at every level [3,13,30]. When addressing the issue of environmental green, both private and public, one must first think of creating a collective culture. It is therefore necessary to integrate information: a. You need to know which plants are present in the territory with a listing of the existing species.
b. You must consult the Bulletin of pollen and allergenic spores.
c. It is necessary to inform and train those who deal with the management of public green spaces, but also to transmit information to private individuals who still manage a relevant aspect. In this sense, botanical and biological, but also clinical knowledge can help change some habit and some landscape habitats without giving up on having a pleasant and soothing green environment.
The adoption of simple methods to choose the type of plants to be planted can significantly help block the increase in allergic diseases or at least contain its symptoms. The planning of these interventions must be the task of the public structure which must coordinate the measures and favour a culture where the private sector must and can be an important force.

Key Messages
• Allergic pollen-related diseases have a high worldwide prevalence and imply substantial healthcare costs.
• Air pollution and climate change related to industrialization and urbanization contribute to increase pollen allergenicity and sensitization. • A list of species with the highest and least allergenic potential is provided in order to better choose plants for the landscape.
• Hints to reduce pollen spread in the atmosphere are:

a.
Choose entomophilous species or the female gender of anemophilous dioecious plant.

b.
Plant female plants near the male ones, in order to capture pollens.

c.
Periodically prune male trees such as birches and alders.

d.
Create a hedge on the borders with female plants.
• Pollen calendars are useful tools showing the peak pollen times for various plants in different areas.