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date: 18 October 2019

Pollen, Allergens, and Human Health

Summary and Keywords

Allergenic pollen is produced by the flowers of a number of trees, grasses, and weeds found throughout the world. Human exposure to such pollen grains can exacerbate pollen-related asthma and allergenic conditions such as allergic rhinitis (hay fever). While allergenic pollen comes from three main groups of plants—certain trees, grasses, and weeds—many people are sensitive to pollen from one or a few taxa only. Weather, climate, and environmental conditions have a significant impact on the levels and varieties of pollen grains present in the air. These allergenic conditions significantly reduce the quality of life of affected individuals and have been shown to have a major economic impact.

Pollen production depends on both the current meteorological conditions (including day length, temperature, irradiation, precipitation, and wind speed/direction), and the water availability and other environmental and meteorological conditions experienced in the previous year. The climate affects the types of vegetation and taxa that can grow in a particular location through availability of different habitats. Land-use or land management is also crucial, and so this field of study has implications for vegetation management practices and policy.

Given the influential effects of weather and climate on pollen, and the significant health impacts globally, the total effect of any future environmental and climatic changes on aeroallergen production and spread will be significant. The overall impact of climate change on pollen production and spread remains highly uncertain, and there is a need for further understanding of pollen-related health impact information. There are a number of ways air quality interacts with the impact of pollen. Further understanding of the risks of co-exposure to both pollen and air pollutants is needed to better inform public health policy. Furthermore, thunderstorms have been linked to asthma epidemics, especially during the grass pollen seasons. It is thought that allergenic pollen plays a role in this “thunderstorm asthma.”

To reduce the exposure to, or impact from, pollen grains in the air, a number of adaptation and mitigation options may be adopted. Many of these would need to be done either through policy changes, or at a local or regional level, although some can be done by individuals to minimize their exposure to pollen they are sensitive to. Improved aeroallergen forecast models could be developed to provide detailed taxon-specific, localized information to the public. One challenge will be combining the many different sources of aeroallergen data that are likely to become available in future into numerical forecast systems. Examples of these potential inputs are automated observations of aeroallergens, real-time phenological observations and remote sensing of vegetation, social sensing, DNA analysis of specific aeroallergens, and data from symptom trackers or personal monitors. All of these have the potential to improve the forecasts and information available to the public.

Keywords: aeroallergen, air quality, allergenic pollen, climate, climate change, human health, land cover, pollen forecast, public health, species distribution

Introduction

The study of pollen is a truly cross-disciplinary area of research, which includes the fields of biodiversity, ecology, molecular genetics, botany, climate science, physics, atmospheric science, epidemiology, toxicology, geospatial analysis, and health and environmental policy.

Pollen grains contain the male reproductive cells of seed plants, and during pollination the pollen grains transfer these reproductive cells to the female reproductive organs. Pollination can occur through the grains being transferred by air, animals, or water (anemophilous, entomophilous, or hygrophilous). Allergenic pollen is produced by a number of trees, grasses, and weeds found throughout the world. Pollen grains are around 0.006–100µm in size and as such can be breathed in by humans through the nose, mouth, and into the respiratory tract and the lungs (bronchioles).

Weather, climate, and environmental conditions have a significant impact on the levels and varieties of pollen grains present in the air. The amount and the timing of production and release of pollen grains varies depending on environmental conditions, particularly meteorology, as well as past and current conditions (Emberlin et al., 2007). Land-use or land management is also crucial, and so this field of study has implications for vegetation management practices and policy, which will be discussed later.

Human exposure to allergenic pollen is associated with a range of health effects, including the exacerbation of pollen-related asthma in susceptible individuals, as well as allergenic conditions such as allergic rhinitis (also known as hay fever or pollinosis) and atopic dermatitis (eczema). These allergenic conditions have a significant health effect on populations. Both allergic rhinitis and asthma significantly reduce the quality of life of affected individuals and have been shown to have a major economic impact (Bousquet et al., 2001). Many people’s asthma or hay fever can be well managed, but sometimes these conditions can lead to hospitalization.

Given the influential effects of weather and climate on pollen (and other aeroallergens), and the serious health impacts globally, the total effect of any future environmental and climatic changes on aeroallergen production and spread will be significant. The overall impact of climate change on pollen production and spread remains highly uncertain (Osborne & Eggen, 2014), and there is a need for further understanding of aeroallergen-related health impact information.

The Effect of Climate and Weather on Allergenic Pollen

This article will discuss the impact of weather (meteorology) and climate on pollen and on health. Weather is day-to-day changes in, for example, temperature, wind, and rain. Climate describes the average, the variations, and the extremes of weather in a region over long periods.

The process of a plant making and releasing pollen is extremely complicated, and this article gives an overview of how weather and climate plays a role in it. The production of pollen by a plant is dependent on the current meteorological conditions (including day length, temperature, precipitation, and wind speed/direction), and, importantly, also on the weather and environmental conditions and water availability experienced in the prior year. It is during this time that pollen is formed (Emberlin et al., 2007). Some key weather and climate conditions are shown in Table 1 to illustrate the interplay of these with pollen production, release, and spread.

Table 1. Some Key Weather and Climate Conditions, Illustrating Their Interplay With Pollen, Production, Release, and Spread

Readiness to Flower

Pollen Release

Pollen Spread

water availability

light intensity (irradiation)

rainfall

habitat availability and land use

humidity

wind direction/strength

temperature (often need period of low, above freezing temperatures)

day length

light intensity (irradiation)

The section “Pollen Production, Release, and Dispersal” describes the environmental conditions, including weather and climate, that affect pollen production, release, and spread. Weather also has a direct impact on the health effects of pollen, and this will be explored in the section “Health Impacts of Allergenic Pollen.”

Brief History of Pollen Research

The invention of the optical microscope at the end of 15th century allowed detailed study of pollen grains (among other biological particles). A thorough history of experimental pollen research is given in Scheifinger et al. (2012), and some key highlights are presented in this article.

The timing of the production or release of pollen is included in an area of study called phenology, which looks at any changes in this seasonal cycle. Carolus Linnaeus started the first observational phenological network (monitoring the timing of flowering by species and location) in Sweden and Finland from 1750–1752 (Nekovar et al., 2008).

Since then, many global phenological networks have been operated (Scheifinger et al., 2012), and a detailed overview is given in Schwartz (2003), Nekovar et al. (2008), and Koch (2010).

Charles Blackley (b. 1820–d. 1900) was the first to show that pollen affected human health. He used himself as a test case and applied different pollen types to his eyes, nose, and mouth. He also showed that the amount of pollen present in the air correlated with the strength of his symptoms (Scheifinger et al., 2012). He published his paper “Experimental Researches on the Causes and Nature of Catarrhus Aestivus” in 1873.

Hans Molisch (b. 1856–d. 1937) used the term “aeroplankton” to describe biological particles, including pollen and fungal spores. Pashley, Fairs, Free, and Wardlaw (2012) stated that aerobiology was a term that was first used in the 1930s and defined as the study of biological particles present in the air. Aerobiology includes the study of airborne pollen grains and fungal spores.

Dr. Ruby Hirose (b. 1904–d. 1960) was a chemist and microbiologist who developed a way to improve pollen extracts used to develop a desensitization treatment for hay fever sufferers. She is pictured in Figure 1 working in the William. S. Merrell biological laboratories while isolating pollen for a potential hay fever treatment.

Pollen, Allergens, and Human HealthClick to view larger

Figure 1. Dr. Ruby Hirose (b. 1904–d. 1960) was a chemist and microbiologist. She found a way to improve the pollen extracts used to desensitize hay fever sufferers (and also laid the groundwork for the polio vaccine). She is pictured here at the lab bench, isolating pollen for a potential hay fever treatment while a researcher at the William S. Merrell biological laboratories.

Image credit: Smithsonian Institution Archives. Image # SIA2008-3224.

In terms of historical observing techniques used to collect pollen grains, this also began with Charles Blackley. Blackley carried out many observational experiments using kites to collect airborne particles (Comtois, 1995). Early samplers were used in the late 1800s and early 1900s. Later types of pollen samplers included the gravimetrically standardized sampler, which was frequently used after it was introduced in 1946 (Durham, 1946). In 1952 Jim Hirst designed a sampler with a suction pump, and most present-day samplers (the Burkard and Lanzoni traps) are based on the Hirst-type volumetric sampler. In 1967 the “Rotoslide” sampler was invented, which was a rotary sampler. “Passive sampling” was devised by Cour (1974), did not require a power supply (an advantage for siting these traps), and was used alongside a weather vane to orientate the collector. The first pollen monitoring carried out on a national scale was in the United States in 1928, in a study of Ambrosia pollen and its impact. This network sparked a number of other similar networks in Canada, Mexico, and Cuba.

Allergenic Vegetation

In this section we will discuss either species (e.g., Acer pseudoplatanus [sycamore]) or genera (e.g., Alnus [alder]), and so for clarity we refer to all as “taxa” (singular form “taxon”).

The climate affects the types of vegetation and taxa that can grow in a location through availability of different habitats.

Grasses, Trees, and Weeds

Certain taxa are considered to be more important aeroallergens than others. The taxa in Table 2 have been found to be highly allergenic (those most commonly causing allergy) (Okuda, 2003; de Weger et al., 2012; Matricardi et al., 2016).

Grasses (Poaceae), are highly allergenic and found worldwide. Some species of grass are much more allergenic than others, but more research is needed in this area to provide a confident list of the species most commonly causing allergies—or indeed those causing the most severe symptoms. This is because the individual species of grasses cannot be distinguished by their pollen grains using an optical microscope (conventionally used in much pollen monitoring worldwide). This is in contrast to tree species whose pollen grains look quite different under an optical microscope, and so more has been learned about the allergenicity (also known as the allergen content, or the potency) and spread of these pollen grains.

Trees with allergenic pollen belong to the orders Fagales (alder, beech, birch, hazel, oak), Lamiales (ash, privet, olive, lilac), Pinales (cypress, Japanese cedar, juniper), and Proteales (plane tree, sycamore) (Matricardi et al., 2016). In the Mediterranean, Africa, America, and Australia, trees belonging to the order Lamiales (i.e., olive tree) or Pinales (i.e., cypress tree) are the main allergen-producing trees (Matricardi et al., 2016).

Most allergenic tree pollen in Europe is produced by Betula (birch) and in Mediterranean regions by Olea europaea (olive) and Cupressus (cypress) (D’Amato et al., 2007a). Despite its allergenicity, Betula is planted widely in cities (Spellerberg, Eriksson, & Crump, 2006). In Europe, the largest proportion of the population with a positive skin prick test to Betula allergens was 54%, recorded in Switzerland (D’Amato et al., 2007a). Cupressaceae pollen was found to account for 30% of the total pollen count during winter (in Spain) and is responsible for allergic rhinitis at a time when no other allergenic plants are flowering (Alcázar et al., 2004; D’Amato et al., 2007a). Cryptomeria japonica (Sugi, or Japanese cedars) are widespread in Japan, Asia, and North America. These are highly allergenic trees that have had serious health effects on local populations (Okuda, 2003; Yamada, Saito, & Fujieda, 2014). Jianan, Zhiyun, Hua, and Xiaoke, (2007) offered a review of allergenic planting in urban areas, with a focus on species planted in China. Ligustrum (privet) is frequently used in the Mediterranean in ornamental settings as well as for hedges in parks or gardens and can potentially cause local allergy problems (Cariñanos, Alcázar, Galán, & Dominguez, 2002).

Table 2. Certain Taxa Are Considered to Be More Important Aeroallergens Than Others; the Taxa in This Table Have Been Found to Be Highly Allergenic (Okuda, 2003; de Weger et al., 2012; Matricardi et al., 2016)

Taxa

Common Name

Grasses

Poaceae

Trees

Alnus

alder

Betula

birch

Carpinus

hornbeam

Castanea

chestnut

Casuarina

Australian pine

Corylus

hazel

Cryptomeria japonica

sugi, or Japanese cedars

Cupressaceae

cypress, juniper and cedar

Fagus

beech

Fraxinus

ash

Ligustrum

privet

Olea europaea

olive

Ostrya

hop hornbeam

Platanus

plane

Syringa vulgaris

lilac

Quercus

oak

Weeds

Ambrosia

ragweed

Artemisia

mugwort

Parietaria

pellitory

Weeds from the following plant families produce allergenic pollen: Asteraceae, Urticaceae, Plantaginaceae, Euphorbiaceae, and Amaranthaceae (Matricardi et al., 2016, ch. B03). Pollen from 35 weed taxa have been identified as allergens (Stemeseder, Hemmer, Hawrnanek, & Gadermaier, 2014). Parietaria (pellitory) is an allergenic pollen producing plant in the Mediterranean. Urtica (nettle) is not an important aeroallergen, but it has pollen grains that cannot be distinguished microscopically from Parietaria judaica. Thus, care needs to be taken if using observational pollen counts that Parietaria judaica pollen grains have not been misclassified as Urtica.

Ambrosia (ragweed) pollen is a major aeroallergen, and it appears to induce asthma about twice as often as other pollen (Dahl, Stranhede, & Wihl, 1999). There is a risk it will spread to new areas in the future with changes to the climate and land use (Ziska et al., 2011; Smith, Cecchi, Skjøth, Karrer, & Šikoparija, 2013; Hamaoui-Laguel et al., 2015; Pashley, Satchwell, & Edwards, 2015). Ragweed pollen has been shown to be transported hundreds of kilometers in the wind; high concentrations of ragweed pollen can be found in the air far from the areas where most ragweed plants are located (Prank et al., 2013; Grewling et al., 2016; de Weger et al., 2016).

Allergenic pollen is also produced by Helianthus anuus (sunflower), Parthenium hysterophorus (feverfew), mercurialis annua (Annual mercury), chenopodium album (goosefoot), salsola kali (Russian thistle) and amaranthus retroflexus (amaranth), although it is unclear how important these aeroallergens are for health impacts (Matricardi et al., 2016, ch. B03).

Other pollen-producing plants likely to be less important aeroallergens include Castanea (chestnut); it is unclear how allergenic this plant is. Similarly, Pinus (pine) is not considered to be allergenic. Plantago (plantain) is thought to be only a minor cause of hay fever in Europe and has some cross-reactivity with grass pollen (de Weger et al., 2012). Similarly, Rumex (dock, sorrels) is not considered to be an important aeroallergen. Salix (willow) can be both wind pollinated and insect pollinated; it has minimal importance as an aeroallergen, and the airborne pollen loads are often low.

Pollen Production, Release, and Dispersal

Many environmental conditions, particularly meteorology (Emberlin et al., 2007), affect the timing of the development and release of pollen from a plant. This also varies by taxon. Pollen production depends on both the current meteorological conditions (including day length, temperature, irradiation, precipitation, and wind speed/direction) and the water availability and other environmental and meteorological conditions experienced in the previous year (Emberlin et al., 2007). This is because it is during this previous year that pollen grains begin to form.

Any changes to these environmental conditions or meteorological conditions, such as changes to temperature, rainfall, humidity, or light levels, affect the phenology of the tree or plant. These have an effect on the timing of the onset of pollen release, the total volume of pollen produced, and the length of the flowering season (Dahl et al., 2012). (See the section “Changing Allergenicity” for a discussion on how the allergenicity [potency] of pollen may also be affected.) How land is used and managed by humans is also critical, for example if fields are cut or grazed by animals, then the potential to release pollen is significantly affected.

Pollen grains contain the male reproductive cells of seed plants. After pollen grains have been released from a plant, they can be spread (dispersed). Depending on the taxon, pollen grains are dispersed by wind, animals, or water. Allergenic pollen is predominantly that dispersed by the wind, and so here we focus on this allergenic pollen. This dispersion of allergenic pollen grains is dependent on many environmental factors, particularly meteorological ones. Pollen can travel large distances from its original source (Sofiev et al., 2012). Most pollen grains are deposited within a few hundred meters of the plant. However, the concentration of pollen (particles per m3) is not just a localized phenomenon; pollen counts have been found to correlate across distances of 20 km (Erbas et al., 2007) and 41 km (Pashley et al., 2009), with the potential for pollen to travel much further (Skjøth, Sommer, Stach, Smith, & Brandt, 2007), indeed across the globe (Sofiev et al., 2012). Some people suffer allergic symptoms when exposed to very low concentrations of pollen grains, and so even if a small fraction of the total pollen grains travel further (tens to hundreds of kilometers), then these pollen grains can have an impact on health far from their original source. The main factors affecting the dispersion of pollen grains are wind speed and direction, as well as precipitation (which brings the pollen to the ground). Pollen grains from different taxa can travel different distances, as each of the pollen grains are different sizes and shapes and so have different aerodynamic properties. Tree pollen is more likely to be transported long distances. This is because the release height of the grain is higher from the ground than, for example, grass pollen, and so they are more likely to be carried higher into the atmosphere and so can be transported large distances. Pollen can travel long distances (Skjøth et al., 2007) (this phenomenon is known as “long range transport”) and indeed across the globe (Sofiev et al., 2012). Regional, continental or global scale atmospheric conditions affect the transport of such grains, much like the transport of Saharan dust or other particles around the globe. As with other pollen, ragweed pollen has been shown to be transported hundreds of kilometers in the wind, and so areas with high concentrations of ragweed pollen in the air are more extensive than those where most ragweed plants are located (Prank et al., 2013; Grewling et al., 2016; de Weger et al., 2016).

Daily and Seasonal Cycles of Pollen

The time in the season that different allergenic taxa release pollen into the atmosphere is known as the pollen calendar. The exact timings of the pollen calendar will of course be dependent on many of the factors we have already discussed (meteorological, climatological, day length, geographical location, etc.); however, general trends can be summarized by classifying the pollen season into three main parts: the tree season, grass season, and weed season. Within this, the pollen calendar will give more details of different taxa—when emissions are most likely and when they peak.

Generally, the tree pollen season marks the start of the overall pollen season, occurring in late winter to spring, although this is dependent on latitude and local climate. The tree pollen season is followed by the grass season, which lasts for a few months over the summer. Finally, the weed season continues from here, starting in late summer and going into autumn. As the seasonal cycles of the allergenic pollen released from different plants depends so much on the climate, environmental conditions, latitude, northern or southern hemisphere, and on the taxon of plant, it is difficult to illustrate these for the many different countries/areas here. Typically, however, the seasonal pattern of which species tend to release pollen in which month is described or displayed as a pollen calendar. See Figure 2 for an illustration of this pollen calendar for the United Kingdom, which is shown as an example. In different countries the same general pattern will follow, but the exact timings and months will vary across the world.

Pollen, Allergens, and Human HealthClick to view larger

Figure 2. Pollen calendar showing timings of release of pollen in a typical season for the United Kingdom. Note that the seasonal cycles of the allergenic pollen released from different plants depends on the climate, environmental conditions, latitude, northern/southern hemisphere, and so timings will vary across different countries and areas.

Image: Crown copyright 2018, courtesy of The Met Office.

Typically in the United Kingdom, the pollen season for tree taxa ranges from January to April for early flowering taxa such as alder and hazel, to mid-March to end of July for the later taxa, including oak and pine. Grass flowering occurs generally between May and early September, coincident with many taxa of weeds with allergenic pollen, see Worcester University (2017a) and Figure 2.

As well as a seasonal cycle of peak pollen levels, during each day there is a daily (diurnal) cycle of pollen levels in the air. The daily profile of concentrations of pollen in the air can vary greatly. However, when looking over an entire season, the mean diurnal cycle of pollen can be established. Several studies have measured the diurnal cycle of tree pollen and have found that different species exhibit different daily cycles. Tree pollen has been observed to peak in the afternoon, with lowest levels observed throughout the night (Ščevková, Dušička, Mičieta, & Somorčík, 2015). However, Latałowa, Uruska, Pe˛dziszewska, Góra, and Dawidowska (2005) found that Betula resulted in peaks throughout the day and night.

Much of the daily variation in pollen loads comes directly from the emission of the pollen from the plant. Many different species of grass are known to flower (and therefore emit pollen) at different times of the day (Peel et al., 2014). The same study found three different daily profiles at different phases in the grass pollen season in Denmark—a twin peak profile during the early season, a single evening profile during the middle of the season, and a single midday peak during the late season. They hypothesize that these different diurnal flowering patterns come from different species of grasses that flower at different periods in the pollen season. Subba Reddi, Reddi, and Atluri Janaki (1988) studied the daily pollen emissions of 54 species of grass in India. They found that 52 of the species exhibited a characteristic diurnal emission pattern: each species with their own characteristic pattern throughout the day and/or night. They found two species, Imperata cylindrica and Pennisetum americanum, shed pollen constantly throughout a 24 hour period, even if it was raining. In the other 52 grasses, the duration and intensity of pollen emission were inversely related. They found that the pollen release times of any species were the same on all “fine weather” days. Weather did affect the normal pattern, and each species responded differently to variations in weather factors.Both the flowering processes and the dispersion of the grains are driven by weather, and both of these factors affect the daily cycle of pollen concentrations.

Current Approaches to Pollen Monitoring

Measurements, or observations, of aeroallergen concentrations in the air are predominantly used to estimate the levels of pollen that people are exposed to in a particular area; to research human health impacts of pollen; and to provide inputs to pollen forecasts to inform the public or public health officials. Pollen observations can also be used to study the timing of the start of the flowering season, and where long decadal records exist, to track any changes in the seasonal variations due to climate and non-climatic drivers.

In-Situ

There a number of different methods currently used to measure or estimate pollen release or pollen levels. We will start by looking at how collecting and counting pollen grains is commonly done.

The process of direct pollen measurements can be divided into two steps: collecting the pollen grains from the air and measuring (traditionally by counting) the amount of pollen that has been collected. There are a number of methods that can be used for each step, and these tend to be time consuming, requiring a lot of human interaction and often from highly trained individuals—also the monitoring equipment itself is often expensive. While some initial steps have been made in this field toward using new technologies and automated techniques, this is an area expected to expand.

There are a number of observing networks worldwide. For example, the Europe-wide pollen network collects data from the European Aeroallergen Network (EAN).1

These networks predominantly use Hirst-type volumetric samplers, or sometimes a gravimetric trap (e.g., Werchan et al. [2017] used Durham [1946]). The Hirst-type samplers suck air in at a set rate (10 liters/min), and particles are deposited onto sticky tape. The tape is mounted on a rotating drum, and the speed of rotation means that two-hourly data can be determined. Once collection is complete, the tape is then stained with a dye and examined under an optical microscope. The dye allows the grains to be more clearly identified. From this, the number of pollen grains per cubic meter can be calculated. Traps tend to be located on top of buildings, so that very localized planting has less of an effect on the results. Figure 3 shows a photograph of a Burkard Hirst–type volumetric sampler.

Pollen, Allergens, and Human HealthClick to view larger

Figure 3. A Burkard Hirst–type volumetric sampler, with solar panel. The Hirst-type monitor is the most commonly used aeroallergen sampler.

Image credit: G. Brennan.

Rotorod is another type of trap used predominantly in the United States. In this type of sampler the arms of the trap rotate quickly (~2,400 rpm) and therefore sample at a higher rate of 120 liters/min (Scheifinger et al., 2012).

Once the airborne particles have been collected, the particles need to be identified and counted. Counting pollen grains requires specialist knowledge of the shape and size of pollen grains (pollen morphology). Typically the collected samples are looked at through a 400 × optical microscope, and the species/taxon is identified by the trained pollen counter (a person). The method for counting pollen collected from a Hirst-type trap is outlined here, as it is one of the most common methods currently used. The dyed sticky tape that has collected the pollen can cover a 24-hour period and so could have 12 sections each with two-hourly data. Because of the time required to manually examine by microscope and count every grain on the slide (and repeat every day, at every collection site), methods of sub-selecting part of the slide and scaling up to provide an estimate of the whole day have been devised. The common method, which is still used over 20 years later, is to use the “transverse traverses” method (Emberlin et al., 1994) where slides are counted along 12 equidistant perpendicular transects to provide a statistically representative estimate of daily mean concentrations—this also allows an assessment of the diurnal pattern. As well as counting the pollen grains along these transects, pollen counters will identify the species/taxon of all pollen and record the number of each found. From this technique, the pollen concentration can be calculated (grains/m3) using information about the rate of collection.

While most methods still rely on these manual counts, some automated traps do exist. Little progress has been made in rolling out any sort of automated counting into monitoring networks although some methods have been tested, such as pattern recognition software on digital images of the pollen slides (Boucher et al., 2002; Chen et al., 2006). These methods have differing degrees of success, depending on the number of different types of particles present in the sample. Another method using lasers as particle counters has been used in tests separating pollen from nettle, ragweed, and grass (Kawashima, Clot, Fujita, Takahashi, & Nakamura, 2007).

In Japan, automated pollen collection and counting is successfully used. This is done using automated “pollen bots” to collect and identify pollen in real time (Nursing Link, 2017). The pollen bots are hosted by volunteers, and data from these bots are uploaded and fed into a live online pollen map (Weather News, 2017; Nursing Link, 2017). This may be possible because in Japan there are far fewer species/taxa of allergenic pollen present in the air to identify. This shows that this technology is possible and could allow much wider networks of collection, if the technology could be rolled out in other countries and widened to include other allergenic taxa found elsewhere in the world.

A different type of pollen observation can be made using phenological observations: the recording of the beginning of the flowering season. Phenological data are easier to collect than pollen counts. As such, phenological datasets exist that either cover larger areas or over much longer historical periods than pollen grain counting (Scheifinger et al., 2012). Phenological data collection has traditionally been done manually by observing bud burst or leaf burst of trees and plants. Now this can be captured by satellite observations. A review of these datasets can be found in Koch (2010).

Satellite Observations: Remote Sensing

A large number of datasets from remote sensing by satellite exist, which can tell us a great deal about when pollen is likely to be released.

Live green plants absorb solar radiation in 400 to 700 nm range (which they use for photosynthesis). They also emit (but do not absorb) radiation in the near-infrared spectrum. This difference in spectral signals in the red and near-infrared regions allows remote sensing methods to identify living green plants. A metric that measures this effect is called the Normalised Difference Vegetation Index (NDVI). NDVI can be used to differentiate vegetation from other land cover areas such as soil, snow, or dead or bare vegetation. Examples of such satellite observations include SPOT VEGETATION (Spot Vegetation, 2019) and MODIS Vegetation Continuous Fields (2017).

Birch flowering has been measured by satellites, which is possible because the timing of leaf-bud burst and flowering of birch trees are well correlated. As such, measurements of NDVI could be used to accurately estimate the timing of flowering (Hogda, Karlsen, Solheim, Tommervik, & Ramfjord, 2002; Karlsen et al., 2008). A caveat for using this type of method is that it does not account for any long-range transport of pollen and so only accounts for local emission of birch pollen, rather than the levels in the air. Karlsen et al. (2008) noted that remote sensing is also a useful tool for revealing regional differences that may not be easily detected by pollen stations alone. Another significant advantage is the larger spatial coverage.

There is much scope to reduce the labor-intensive acts of traditional pollen counting and to combine these satellite observations to exploit these large-area datasets.

Vegetation Inventories

Spatial maps showing the location of vegetation that emits allergenic pollen, often referred to as pollen source maps (or inventories) (Skjøth et al., 2012), can be made. While these types of maps do not provide a forecast of pollen in the air at any one time or give an estimate of the human exposure to the pollen, they do provide the most likely locations of the allergenic taxa.

There have been many studies that use different techniques to map allergenic vegetation or create pollen source maps. Skjøth et al. (2012) outlined two approaches to creating these pollen source maps, which can be categorized as “bottom up” or “top down” approaches. Starting with the location and amount of the pollutant, “bottom up” techniques (e.g., as used in Skjøth et al., 2008) combine land cover maps with regional scale statistics. The latter is a clear limitation because regional scale statistics are often unavailable for certain taxa, particularly weeds. Different areas of the world, and indeed within a country or region, will have varying quality of datasets of this sort. For example, many sources exist that refer to the presence (or absence) of a particular plant type or species in a particular location but do not provide their abundance or percentage cover—and such surveys rarely cover an entire region or country. In contrast to “bottom up” techniques, “top down” inventories start with a measured pollen quantity and work backward using models to calculate the distribution. One can use station-based pollen monitoring observations along with land cover maps (e.g., Skjøth et al., 2012 used data from the European Aeroallergen Network). The spatial distribution of pollen monitoring stations can limit these “top down” methodologies. Geographic coverage of pollen monitors can be sparse; and as they are labor intensive to run (as outlined in the section “Current Approaches to Pollen Monitoring”), those stations that do have data can be limited in temporal coverage.

Current allergenic vegetation mapping includes the example illustrated in Figure 4 of Artemisia (mugwort) (units of percentage cover, quantile color bars) and Betula (birch) (units are number of trees in a 1 km × 1 km grid square) in Great Britain from McInnes et al. (2017). These are at 1 km × 1 km resolution and illustrate current mapping of such allergenic species. Other examples of existing pollen mapping include tree source maps at 50 km × 50 km resolution (Skjøth et al., 2008) and Ambrosia (ragweed) source inventories for different European locations (Skjøth et al., 2010; Thibaudon et al., 2014; Karrer et al., 2015).

Trees over Europe were statistically mapped at 1 km × 1 km resolution and presented in Brus et al. (2011). Footprint areas of Alnus (alder) and Betula (birch) in Worcester (United Kingdom) were created using back-trajectories of pollen observations (Skjøth, Bilinska, Werner, Adams-Groom, & Drzeniecka-Osiadacz, 2015b). Skjøth et al. (2013) created a grass pollen inventory in Aarhus (Denmark) using GIS and remote sensing.

Olea (olive) can be much easier to map than the other allergenic tree taxa because it is found in olive groves, which are detectable in high resolution mapping across Europe (Skjøth et al., 2012).

The quality of any mapping of this sort is dependent on the resolution, quality, and taxa specificity of available input datasets and observations. High resolution datasets can provide a big-data challenge, whereas lower resolution inputs (which may be easier to obtain) can miss important spatial detail.

Pollen, Allergens, and Human HealthClick to view larger

Figure 4. Maps showing location of two allergenic taxa plants in Great Britain. Left: Percentage cover of Artemisia (mugwort) in units of percentage cover per 1 km × 1 km grid box. Right: Tree coverage of Betula (birch) in England and Wales. Units are number of trees per 1 km × 1 km grid square. Color ranges of both have been set to five equal-sized quantiles (i.e., each contains 20% of data). Images: Crown copyright, 2016, courtesy of The Met Office. Based on data licensed from National Tree Map, copyright Bluesky International Limited, 2016; digital spatial data licensed from the Centre for Ecology & Hydrology, copyright NERC (CEH) and contains, or is based on, information supplied by the Forestry Commission. Images reproduced from McInnes et al. (2017).

Applications of Pollen Monitoring

Pollen monitoring, phenological observations, satellite observations of pollen sources, and vegetation inventories have many applications worldwide. They can be a source of information for local authorities and health-care practitioners: for example, used as a risk assessment tool to help with the treatment or self-management of patients with health conditions caused by pollen allergies. They can be used to provide advice on risk assessments on invasive species (e.g., Csornai et al., 2011). Detailed information about the location of allergenic species can also be combined with health data to study the health impacts caused by exposure of environmental aeroallergens (e.g., rise in respiratory hospital admissions Newson et al., 2014, Bousquet et al., 2007). And finally, vegetation maps can also be combined with meteorological data to improve pollen forecasting systems (e.g., Zink et al., 2012), or as inputs to pollen emission models (Zink et al., 2013).

Pollen, Allergens, and Human HealthClick to view larger

Figure 5. Vegetation-climate-health interactions, illustrating the complexity of the feedback mechanisms and interactions between vegetation, climate, and health. Pollen and allergies are affected by the climate through many complex interactions. Importantly, none of these interactions are one way: each of these could cause a change in the others.

Image: Crown copyright, 2018, courtesy of The Met Office.

Minimizing the Health Impacts of Pollen

In this section we will look at the health impacts of allergenic pollen and how these may be minimized through existing methods, advances in the field, and new technology. The effect of climate and weather on the many complex interactions between the biosphere (including species, vegetation), hydrosphere (water) atmosphere, and the anthroposphere (human-sphere) are explored.

To understand how weather and climate affects pollen and health, it is helpful to think about the interactions between climate, vegetation, and health.2

Considering components of the climate, there are many complex mechanisms, feedbacks, and climate impacts that could have an effect on vegetation or health. When one considers vegetation and how it interacts with the climate system, one can quickly start to see areas where there will be feedbacks working both ways: for example, the climate affecting the vegetation growth, location, and the vegetation feeding back and impacting on the climate (e.g., through the water cycle, or carbon dioxide levels).

Both vegetation and climate also link to health, and some feedbacks involve all three interactions. The “word cloud” in Figure 5 provides an example of the sorts of interactions that may be important and are presented here to illustrate the complexity of the feedback mechanisms between vegetation, climate, and health. Pollen and allergies are affected by the climate through many complex interactions. Importantly, none of these interactions are one way.

Health Impacts of Allergenic Pollen

A range of health effects are associated with exposure to allergenic pollen, including allergic rhinitis (hay fever, or pollinosis), exacerbation of asthma in susceptible individuals and atopic dermatitis (eczema) (Cecchi, 2012). While allergenic pollen comes from three main groups of plants—certain trees, grasses, and weeds—many people are sensitive to pollen from one or a few taxa only.

Levels of allergies toward environmental aeroallergens are hard to estimate, and measures vary widely between studies and regions. In Europe, levels among patients range typically from up to 30%–50% (Newson et al., 2014). Here the largest fractions of sensitizations are toward specific pollen, those from grasses and trees of the Betulaceae family. Clinically relevant sensitization rates for grasses have been found to exceed 50% in both the United Kingdom and Denmark (e.g., Burbach et al., 2009). The United Kingdom has one of the highest prevalence of medically diagnosed asthma (10% of the adult population Netuveli et al., 2005). Medically diagnosed allergic rhinitis was measured to be 13.2% (95% confidence interval 11.614.9) in the United Kingdom in 2001 (Bauchau & Durham, 2004). Furthermore, of those people with asthma, Asthma UK (2017a) state that approximately 80% also have a pollen allergy.

Clinically there are different ways to determine whether someone is allergic or sensitized to a particular type of allergen, including pollen. The term “allergic reaction” is used to describe symptoms such as sneezing, redness, and itching on exposure to the allergen. However, a larger portion of the population are sensitized to pollen—which means they have the IgE antibodies capable of causing reactions, but there may be no “reaction” (i.e., no symptoms). Allergies can be determined from skin prick tests where specific criteria are met to determine the allergy.

Both allergic rhinitis and asthma significantly reduce the quality of life of affected individuals and have been shown to have a significant economic impact (Bousquet et al., 2001). Many people’s asthma or hay fever are likely to be well managed, but sometimes these conditions can lead to hospitalization.

The role of pollen in asthma exacerbation is increasingly understood, and a good review can be found in Osborne and Eggen (2014). Many studies have found a significant association between grass pollen exposure and hospital admissions for asthma. A lag of several days between grass pollen exposure and adult hospital admissions for asthma in London has been measured by Osborne et al. (2017) (further detail is given in the section “Pollen Forecasting”).

Possible impacts of pollen on non-allergic diseases—including non-allergic respiratory diseases, cardiovascular diseases, and mental health are reviewed by de Weger et al. (2012). Currently there is not enough evidence to conclude the role pollen may play in these.

There is a need for research to quantify thresholds for impacts on populations. It has been suggested (de Weger et al., 2012) that this could be approached by defining primary thresholds for different regions and validating these with patient symptoms scores. A list of pollen threshold levels in the peer-reviewed literature is presented in de Weger et al. (2012, Table 6.1). The applications (apps) and symptoms trackers mentioned in the following section (see the section “Pollen Forecasting”) provide a way to collect such data.

Self-Management

Although it is difficult to avoid exposure to pollen there are a number of measures that pollen-sufferers can take that may help to minimize exposure and ease the severity of hay fever symptoms.

People can stay informed about when pollen levels are highest in their local area if there is a local or regional pollen forecast, and they can often have alerts sent to them to indicate high pollen levels. Some countries or regions provide a forecast up to five days ahead during the pollen season, and so some advance warning of days likely to be high at different locations can be obtained.

Finally, detailed maps of allergenic pollen producing taxa, in combination with pollen forecasts and pollen calendars, can help sufferers to manage their condition by reducing their exposure and also help them to identify which specific taxa they are sensitive to. This can improve self-management steps as they can be targeted to the right part of the pollen season when pollen levels from those particular taxa are high.

Interaction with Air Quality

The pollutants that have the largest impact on health are nitrogen dioxide (NO2), sulphur dioxide (SO2), particulate matter (PM2.5 and PM10), and ozone (O3). In this section we will look at how these air quality measures interact with the impact of aeroallergens.

Populations in urban areas have been shown to be more affected by pollen allergies (asthma and hay fever) than those who live in rural areas (Ehrenstein et al., 2000; Riedler et al., 2001; D’Amato et al., 2007a). These urban environments have higher levels of vehicle emissions and coincide with increased pollen-induced respiratory allergies. It was discovered in the 1990s that exposure to air pollution prior to pollen exposure could exacerbate symptoms and lower the threshold level of pollen to trigger symptoms in allergy sufferers (Molfino et al., 1991; Emberlin, 1998).

Co-exposure is when people are exposed to both pollen and air pollutants at the same time and is currently an active area of research (Miicke, Wagener, Werchan, & Bergmann, 2014; Ørby et al., 2015). Suring et al. (2016) found that allergens from birch pollen can bind to particulate matter PM10, which allows the pollen allergen to travel into the lower respiratory tract. A range of health risks from indoor pollutants, including pollen, are discussed in Vardoulakis et al. (2015), along with how these could change under a changing climate. Buters et al. (2010) hypothesized that diesel particles in the air could absorb some of the allergen from pollen. It is not clear what the effect of this would be on human health. Currently the exact effect of exposure to both allergenic pollen and pollutants is not fully understood, and so further research is required.

The effect on both the allergenicity (such as increased allergenicity of pollen under raised levels of air pollution [see Ghiani et al., 2012; Cuinica et al., 2013] are further discussed in the section “Changing Allergenicity”), and the total volume of pollen grains released under increased air pollution must be established.

Finally, the health impacts of all these factors on populations in high co-exposure areas need to be better understood to inform public health policy.

Thunderstorm Asthma

Thunderstorms have been linked to asthma epidemics, especially during the grass pollen seasons. It is thought that allergenic pollen plays a role in this health impact of “thunderstorm asthma.” Thunderstorm asthma is an observed phenomenon where a rapid increase in the number of asthma attacks (evidenced by increased hospitalizations for this symptom) occurs after a local thunderstorm. These events are strongly associated with high levels of allergenic pollen in the air (Taylor & Jonsson, 2004; D’Amato et al., 2007b; Elliot et al., 2013). However, it should be noted that the precise mechanisms explaining this phenomenon are not known. Notable examples of such thunderstorm asthma outbreaks have been observed in several cities—in Europe (United Kingdom and Italy), United States, Canada, and Australia. A table summarizing known examples of thunderstorm asthma events can be found in D’Amato et al. (2016, Table 1). Patients without asthma symptoms but affected by allergic rhinitis can experience an asthma attack. A large outbreak of thunderstorm asthma overwhelmed medical services in Melbourne (Australia) in November 2016. Experts suggested this was related to high levels of rye pollen (a grass) in the air at the time of the thunderstorm (Guardian Australia, 2017; Asthma UK, 2017b). It was reported that many of those who suffered an asthma attack at this time had not previously experienced asthma symptoms but that as many as 95% were hay fever sufferers. D’Amato et al. (2016) suggested that all people affected by pollen allergy should be alerted to the danger of being outdoors during a thunderstorm in the pollen season.

D’Amato et al. (2016) concluded that there is increasing evidence that thunderstorms trigger epidemics of asthma during the pollen season by washing down pollen grains and concentrating them in a band of air at ground level. This occurs specifically during a thunderstorm and not during frontal rain; this is because strong downdrafts and dry, cold outflows occur during a thunderstorm. The meteorological conditions present at the beginning of a thunderstorm may expose susceptible people to a rapid increase in pollen concentration, and smaller pieces of these grains may be in the air that can enter into the lower airways and trigger asthmatic reactions (Taylor & Jonsson, 2004).

It is hypothesized that during a thunderstorm, pollen grains absorb water and can be split open or burst (rupture) to present either smaller pieces that could be more easily transported by the wind and enter the airways and lungs more easily due to their smaller size (D’Amato et al., 2007b). Often the larger-sized grass pollen size gets trapped in the nasal passage and does not reach the lungs. When the pollen grain is broken up it can enter the lungs, and this might be what triggers the more severe reaction. At present this theory is yet to be proven with experimental evidence.

The effect of climate change on the frequency or severity of thunderstorms under a future climate is highly uncertain and may differ across regions globally.

Pollen Forecasting

Forecasting of pollen is still relatively underdeveloped. Globally there are various regional or country-wide pollen forecasts, either providing such a forecast in general categories or species-specific forecast. There are a huge number of regional or country-wide pollen forecasts available, and Table 7.3 in Karatzas, Riga, and Smith (2012) presented a thorough list of pollen information systems and services. They review here the information available from 67 different pollen information services; they instruct on how to access these services, tell you whether they are free of charge, and provide the relevant links.

Future pollen forecasting systems will require detailed maps of the location of pollen producing plants, detailed emission models characterizing the plant phenology combined with dispersion models, and pollen monitoring for model validation. An area that appears to have potential is related to new ways to identify individual species of aeroallergens—currently a time- consuming and highly skilled task and not always possible when it comes to certain grass species. The PollerGEN (2017) project has begun extracting DNA from pollen observations and using this genetic material to identify grass species in the United Kingdom. Combinations of “shotgun metagenomics,” “DNA barcoding,” “metabarcoding,” and “quantitative PCR approaches” are being used (introductions to these DNA sequencing methods can be found in Creer et al., 2016).

Whether it is these DNA methods, or other methods, a future area of development is likely to be in automated detection and identification technology. A challenge in the future will be the assimilation of any of these direct observations of aeroallergens, along with phenological observations and remote sensing of vegetation (satellites) into numerical aeroallergen forecast systems.

Also emerging are personal aeroallergen monitors—small devices that can be worn or carried by people and that measure aeroallergens or air quality at that location. In addition to this aeroallergen measurement, information about the time and location of the observation can be transmitted via smartphone. These could in the future, alongside social sensing information, and symptom trackers, be combined into an aeroallergen impact forecast. These types of information bypass the detection of the pollen level in the air and instead monitor the health impact due to pollen. This is what many of the forecasts are designed to inform, so skipping the exposure and instead modeling the impact may prove possible in the future. One final example of modern technology is Propeller Health (2017), which is providing digital management of asthma and COPD (chronic obstructive pulmonary disease) through sensors, mobile apps, and reminder services. It is expected that similar technology will follow the trend of wearable personal activity monitors and fitness trackers and will become more widely adopted for people to track, manage, and share their health impacts data.

Climate Change

Climate change can prolong or shorten pollen seasons, increase or decrease their intensity, and aid the spread of allergenic species. In addition, an increase of heavy rainfall events (including thunderstorms) and increased urban air pollution can provoke or aggravate respiratory health conditions.

Any statements about the overall effect of climate change on pollen concentrations are still highly uncertain. This is largely due to the complex nature and number of feedbacks that affect all the elements of pollen production, release timing, transport, and deposition that have been discussed thus far. The impact of climate change on pollen allergies is highly uncertain. Osborne and Eggen (2014) stated with low confidence that amounts and/or allergenicity of pollen may increase because of higher temperatures, higher CO2 (carbon dioxide) concentrations, different patterns of rainfall and humidity, longer growing seasons, and increased air pollution.

There is some evidence that climate change may lead to an earlier appearance in the season of respiratory symptoms due to exposure to pollen and that these symptoms may last longer (Fitter & Fitter, 2002; Vardoulakis & Heaviside, 2012). Across the Northern Hemisphere, early onset of spring has been measured, with some taxa releasing pollen earlier (Emberlin et al., 1997; Frei, 1998; Emberlin et al., 2002; Beggs, 2004) and measured cases of longer pollen seasons (Ziska et al., 2011). In addition, failure to frost can lead to prolonged pollen seasons (Gezon et al., 2016). Longer growing seasons, due to the earlier onset of spring, could mean that plants may be able to pollinate longer (Osborne & Eggen, 2014). In addition, climate change may enable allergenic species to spread into new locations (Smith et al., 2013; Hamaoui-Laguel et al., 2015; Pashley et al., 2015). Further warming of global temperatures and increases in atmospheric CO2 concentration may lead to greater pollen release through increased plant productivity, unless the plants are limited by other factors such as water stress. Ragweed has been shown to increase in height by 9%, while 61% more pollen is produced when it is grown under doubled CO2 (Wayne et al., 2002).

Vardoulakis et al. (2015) discussed how a range of health risks from indoor pollutants, including pollen, may change under a changing climate. More detail on air quality and the effect it has on aeroallergens is presented in the section “Interaction with Air Quality.”

Furthermore, the effect of climate change on the frequency or severity of thunderstorms and thus the health impact of thunderstorm asthma (see the section “Thunderstorm Asthma”) under a future climate is very uncertain. Climate change may also affect the allergenicity of pollen for some taxa, which is discussed in the following section.

Changing Allergenicity

Pollen grains contain molecules that contain different specific allergens. These allergenic molecules have been identified and named, for example, the major allergen from birch pollen is called “Bet v 1.” A full explanation and lists of these allergenic molecules can be found in (Matricardi et al., 2016).

The allergenicity (also known as the allergen content, or the potency) of the pollen grain has been shown to vary throughout the season and across regions. Climate change may also affect the allergenicity of pollen for some taxa (Cecchi et al., 2010).

Buters et al. (2015) found that allergen content in grass pollen varied significantly, both by location (in Europe) and by time in the pollen season. Similarly, in a study of birch pollen, it has been said that health impacts may be difficult to correlate with pollen counts but that it may correlate better with allergen exposure (Buters et al., 2010).

The pollen count (number of grains per m3 of air) can be used as a proxy for human exposure, but it cannot be used as an actual measure of the amount of allergens in the air. Increased allergenicity of pollen that had been exposed to NO2 pollution has been found (Cuinica et al., 2013). Similarly, high levels of air pollution have been found to increase the allergenicity of pollen in plants growing in these areas (Ghiani et al., 2012).

Zasloff (2017) reported that pollen grains carry a diverse population of live bacteria, which they call the pollen microbiome. They speculate that bacteria-forming biofilms on pollen may alter the allergenicity of the pollen. In fact, the latter has been shown to correlate to the microbiome (Obersteiner et al., 2016). When pollen enters a person’s airways, their immune system is presented with both the antigen (pollen) and the bacterial cells which are an adjuvant (a substance that enhances the body’s immune response to an antigen) (Zasloff, 2017).

All of these findings show that this is an area where much more research is required to understand how allergenicity of pollen may change in the future. There are many highly complex effects here—of a changing climate and changing pollution levels—and any possible variation in microbiomes on the overall allergenicity of pollen grains.

Adaptation and Mitigation

To reduce the exposure to or impact from pollen grains in the air, a number of adaptation and mitigation options may be adopted. Many of these would need to be done either through policy changes, or at a local or regional level, although some can be done by individuals to minimize their exposure to pollen that they are sensitive to. Here we outline a number of adaptation and mitigation measures that are possible.

One such method is through regulation of the planting of allergenic taxa to reduce the number of allergenic species that are planted. For example, restriction of Platanus (plane) trees in urban areas where there are large populations. In the United States an allergenicity scale to select suitable taxa for urban planting has been proposed (Seitz & Francisco Escobedo, 2009). Cecchi et al. (2010), D’Amato (2011) recommend planting non-allergenic trees such as Palmaceae (palm) and Ulmaceae (elm), avoiding Cupressaceae (cyprus), Betulaceae (birch), and Oleaceae (olive). After World War II, Cryptomeria japonica (Sugi, or Japanese cedars) were planted extensively in Japan, Asia, and North America. These are highly allergenic trees and have had a significant health effect on the populations (Okuda, 2003; Yamada et al., 2014). Jianan et al. (2007) offered a review of allergenic planting in urban areas, with a focus on species planted in China.

The current practice of the planting of only male trees in urban areas (which is done to reduce street litter from seeds and fruit produced by the female trees) increases the total pollen load. Reduction of pollen exposure through female tree planting could potentially mitigate these effects. The services (and disservices) that a particular tree taxon and canopy design may provide must be examined by local decision makers (Salmond et al., 2016).

Other vegetation management schemes such as grass-cutting regimes where grass is cut before it flowers (and thus before it releases pollen) could be used where there are highly populous areas with high coverage of grass in the vicinity. It should, however, be noted that there will be negative impacts on biodiversity if plants are routinely managed to restrict flowering.

Reducing levels of air pollution would also reduce health impacts from pollen.

Once we know more about the population-wide health impacts of different allergenic species, further localized advice could be provided for vegetation management practices: including, as discussed above, choice of tree species, sex of tree for planting, and grass cutting regimes to limit exposure to the most allergenic pollen. These practices can be targeted toward those most allergenic species, or areas with highest risk to the population.

Future reductions in asthma hospitalizations may be achieved by better understanding of environmental risks, which could lead to improved alert systems and supporting patients to self-manage their conditions (Osborne et al., 2017). As detailed in the section “Self-Management,” there are a number of self-management steps for individuals to try who are sensitive to aeroallergens in order to reduce their exposure. Raising awareness of these techniques among those who suffer from asthma or hay fever could improve the uptake of these methods.

Conclusion

The health impacts of human exposure to allergenic pollen are undoubtedly serious. Allergenic pollen is associated with a range of health effects (including pollen-related asthma and hay fever) and can have a major effect on the well-being of many people worldwide. There are a number of challenges that remain in this research field. More cross-disciplinary and international work with large multi-institution collaborations will be vital to extend current knowledge and face the outstanding questions in this complex field.

In the 2010s there is greater awareness among the scientific and public health communities as to the importance of fungal spores as a source of aeroallergens. Fungal spores are produced by fungi (which include micro-organisms such as yeasts and molds and also larger organisms such as mushrooms) in order to reproduce.3 A useful overview of allergenic spores can be found at Worcester University (2017b).

It is understood that fungal spores—and in particular those of Alternaria—produce respiratory symptoms in those with allergies (Knutsen et al., 2012; Behbod et al., 2015), and in severe cases can cause hospitalization (Bush & Prochnau, 2004; Dales et al., 2000). Sensitization to allergenic fungal spores has been linked to cases of life-threatening asthma, and Black et al. (2000) have correlated outdoor spore concentrations with asthma symptoms.

It has been proposed that spores are an underestimated source of respiratory allergy (Crameri et al., 2014). As such, the prevalence of fungal spores sensitization among the general population is still unknown (Crameri, Weichel, Flückiger, Glaser, & Rhyner, 2006). However Pashley et al. (2012) suggested fungal respiratory allergy may affect up to 30% of atopic individuals (those having a predisposition toward developing certain allergic hypersensitivity reactions), and the prevalence of fungal spores allergy in those patients with severe asthma ranges from 35% to 70% (Denning et al., 2006). Furthermore, it has been suggested that fungal spores may play a role in thunderstorm asthma, after sensitization to Alternaria species was found in those affected by thunderstorm asthma (D’Amato et al., 2016).

Weather, climate, and environmental conditions also have an impact on the levels and varieties of spores present in the air.4 The spatial distribution and timing of release of fungal spores can be expected to change under changing climate (Comrie, 2007). However, as with pollen, the effect of climate change on fungal spores is highly uncertain, and longer observational datasets are needed to be able to provide, with any certainty, trends in airborne fungal spore concentrations (Sindt et al., 2016).

Unlike pollen, observations of allergenic fungal spores have poor geographic and temporal coverage, with few sites globally monitoring daily levels, and so there are not the large networks that have been developed for pollen monitoring. This is partly due to limitations of the traditional identification methodologies (Pashley et al., 2012) that require highly skilled experts to count them and because species identification is not always possible. However, some of the techniques to capture pollen grains will also capture other airborne particles of similar sizes, and so spores can be collected using some of these same methods.

Many areas of aeroallergen research and monitoring are more developed for pollen than for fungal spores and so much further progress is expected here in the coming years. This includes further research into monitoring and observing fungal spores, research into health impacts, and the interactions between fungal spores and other environmental factors such as specific weather and climate conditions and air quality.

Given the multiple and interconnected effects of weather and climate on aeroallergens and the significant health impacts globally, the total effect of any future climate change on pollen production, allergenicity, and spread must be better understood. Similarly, further understanding of the risks of co-exposure to both aeroallergens and air pollutants is needed to better inform public health policy. The health impacts to populations in these high co­exposure areas need to be identified and considered. Further understanding of taxon-specific aeroallergen-related health impacts could help focus mitigation efforts: for example, planting choice and vegetation management.

Furthermore, improved aeroallergen forecast models could be developed to provide detailed taxon-specific, localized information to the public. One challenge will be combining the many different sources of aeroallergen data likely to become available in the future into numerical forecast systems. Examples of these potential inputs are: automated observations of aeroallergens, real-time phenological observations and remote sensing of vegetation, social sensing, DNA analysis of specific aeroallergens, and data from symptom trackers or personal monitors. All of these have the potential to improve the forecasts and information available to the public. Finally, localized alert warnings for those with hay fever during pollen season and local thunderstorms could be introduced and tested for its effectiveness in terms of the health impacts.

Acknowledgments

This work was undertaken as part of the PollerGEN project funded by NERC, grant ID: NE/N002431/1. The author thanks Rosa Barciela for reviewing the draft article; Yoko Tsushima for translating from Japanese; Bernd Eggen for some useful links; Georgina Brennan for the photograph of the pollen monitor at Bangor; and the anonymous peer reviewer and editor who provided valuable feedback to improve this article.

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Notes:

(2.) Although this article focuses on human health, in terms of these interactions generally, health could also include animal health through disease spread and ecosystem health.

(3.) Crameri et al. (2014) and de Weger et al. (2012) reported that the most important allergenic fungal spores come from the genera Alternaria, Aspergillus, and Cladosporium (Crameri et al., 2006), with Candida, Penicillium, and Clavularia being less important as allergens (Mari et al., 2003). Didymella and Epiccocum are also reported to be allergenic (Worcester University, 2017b).

(4.) Alternaria and Cladosporium are released during warm, dry weather, while Didymella, Tilletiopsis, Sporobolomyces and some basidiospores require warm humid conditions and respond to the dew during the night (Worcester University, 2017b). Spores can be produced and released after heavy the rain or during light showers or drizzly rain. There is a lower spore risk in very windy, unusually cold and dry weather, while the lowest risk is on dry, cold frosty days during winter (Worcester University, 2017b).