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Climate Change and Pollen Allergy in India and South Asia

      Keywords

      Key points

      • Anthropogenic emissions continue to increase in one form or other.
      • Health impacts are increasing with de novo symptoms, such as impaired immune tolerance.
      • Massive movement/momentum is needed to reduce emissions of greenhouse gases such as CO2 emissions across the globe.
      The defining concern and challenge for medical science worldwide is the continuously increasing burden of ill-health, low quality of life, and socioeconomic inequality arising because of noncommunicable diseases (NCDs). The limited medical facilities and low economic status are unavoidable factors, especially for the urban poor in developing countries. NCDs principally include cardiovascular diseases, diabetes, cancer, and chronic respiratory diseases. The increasing incidence of respiratory diseases, including allergic rhinitis and asthma, has been attributed to air pollution, climate change, and urbanization affecting both humans and the biosphere.
      • Damialis A.
      • Traidl-Hoffmann C.
      • Treudler R.
      Climate change and pollen allergies.
      Increasing epidemiology-based studies are stressing new cases of respiratory disorders such as rhinitis and asthma, especially among vulnerable groups such as children and older adults, arising because of climate change, the high rate of global warming, and air pollution.
      • Pawankar R.
      • Wang J.Y.
      • Wang I.J.
      • et al.
      Asia pacific association of allergy asthma and clinical immunology white paper 2020 on climate change, air pollution, and biodiversity in asia-pacific and impact on allergic diseases.
      Climate change threatens the last 50 years of gains made in public health.
      • Wheeler N.
      • Watts N.
      Climate change: from science to practice.
      Allergic diseases are a result of the intricate interaction of genetic makeup and environmental factors. The timing of exposure to the allergenic precursors as sensitizing agents is a determining factor in the long-term incidence and prevalence of allergic diseases.
      For respiratory disorders, broadly the risk factors are occupational agents, indoor pollution from cooking fuel and tobacco smoke, and environmental exposure to air pollutants from traffic and fossil fuel burning, all of which are manageable and preventable factors but are underestimated by governmental agencies across the world, despite timely release of monitoring, status, and health impact reports of such diseases by the World Health Organization (WHO) and other international bodies.
      • Schiavoni G.
      • D'Amato G.
      • Afferni C.
      The dangerous liaison between pollens and pollution in respiratory allergy.
      The male reproductive structures of plants, pollen grains, as aeroallergen are well studied across the world and are the primary causative agent of pollen allergy or pollinosis, continuously increasing in these changing climatic conditions. Pollinosis encompasses allergic responses such as rhinitis (hay fever) and asthma and globally are an increasing public health concern.
      • Rasmussen K.
      • Thyrring J.
      • Muscarella R.
      • et al.
      Climate-change-induced range shifts of three allergenic ragweeds (Ambrosia L.) in Europe and their potential impact on human health.
      Apart from inducing asthma and allergic diseases, a high abundance of pollen has also been associated with nonallergic respiratory diseases, such as chronic obstructive pulmonary disease, stroke, myocardial infarction, and even suicide.
      • Hu W.
      • Wang Z.
      • Huang S.
      • et al.
      Biological aerosol particles in polluted regions.
      The pollen count, pollen abundance, dispersal, and allergenicity are the parameters that are affected by the local climate.
      • Ariano R.
      • Canonica G.W.
      • Passalacqua G.
      Possible role of climate changes in variations in pollen seasons and allergic sensitizations during 27 years.
      With changing climatic conditions, these variables fluctuate as the phenology is affected. The total allergenicity is not the same throughout the year (major allergens are few and minor allergens constitute more than 50%). The concentrations of airborne pollen or spores and durations of exposure to these allergens have been found to be important factors influencing the exacerbation of allergic symptoms.
      • Songnuan W.
      • Bunnag C.
      • Soontrapa K.
      • et al.
      Airborne pollen survey in Bangkok, Thailand: A 35-year update.
      Pollen grains or plant-derived paucimicronic components (such as stem particles, trichome parts, plant debris) carry allergens that behave as easily respirable particles that can produce allergic symptoms. These plant-derived particles also interact with air pollution (particulate matter, ozone) to modulate the allergenicity, in turn leading to increased airway sensitization.
      • D'Amato G.
      • Liccardi G.
      • D'Amato M.
      • et al.
      The role of outdoor air pollution and climatic changes on the rising trends in respiratory allergy.
      Pollen grains are produced by flowering plants (angiosperms) and gymnosperms (naked seed plants). Of the 250,000 well-identified and detailed pollen-producing plant species, fewer than 100 are known to induce pollinosis. Among these, pollen grain dispersal mechanisms such as pollination from anemophilous or wind-pollinated plants are the most potent allergen sources, whereas pollens from entomophilous or insect-pollinated plants are known to cause fewer allergic symptoms based on a type I hypersensitivity mechanism.
      • Mothes N.
      • Horak F.
      • Valenta R.
      Transition from a botanical to a molecular classification in tree pollen allergy: implications for diagnosis and therapy.
      Pollen grains or subparticles less than 2.5 to 10 μm readily enter the human body via upper respiratory tract mucosa for eliciting allergic sensitization. The critical threshold pollen concentration expressed as grains per cubic meter of air required to elicit symptoms of seasonal allergic rhinitis varies for different plant taxa: for grasses, the reported value is 50; for Olea, 400; and 1 to ∼50 for Ambrosia pollen.
      • Breton M.C.
      • Garneau M.
      • Fortier I.
      • et al.
      Relationship between climate, pollen concentrations of Ambrosia and medical consultations for allergic rhinitis in Montreal, 1994–2002.
      ,
      • Florido J.F.
      • Delgado P.G.
      • de San Pedro B.
      • et al.
      High levels of Olea Europaea pollen and relation with clinical findings.
      Pollen allergy is also linked with food-allergic disorders, on account of cross reactivity, so any change in pollen abundance and distribution may indirectly affect this condition too.
      • García-Mozo H.
      Poaceae pollen as the leading aeroallergen worldwide: a review.
      • Katelaris C.H.
      • Beggs P.J.
      Climate change: allergens and allergic diseases.
      • Park J.W.
      Revised pollen calendar in Korea.
      Several studies are oriented toward assessing the adverse effects of increasing temperature and increased CO2on phenology regarding productivity, especially for staple and cash crops. Surface pollen records have been widely used for interpretation of fossil pollen history and reconstructions of vegetation and climate in the past.
      • Singh S.
      • Scharf B.W.
      • Khandelwal A.
      • et al.
      Modern pollen-vegetation relationship as an adjunct in the interpretation of fossil pollen records in the Chilka Lagoon, Odisha, India.
      Nonetheless, there are only sparse data on the direct correlations among climate changes, pollen seasons, and allergic sensitizations, because this would require long-term detailed pollen counts and meteorologic monitoring, with simultaneous recording of the clinical data of the resident population of the study site.
      The present article highlights the impact of these 3 major risk factors on pollen production, pollen seasons, and altered allergenic content as reported in various studies, with a focus on India and Southeast Asia.
      NCDs are man-made disorders related to adoption of unhealthy lifestyles (also unhealthy diet, physical inactivity, and increasing tobacco/alcohol consumption, especially at an early age) in line with the increased urbanization, especially in developing regions such as Southeast Asia.
      • Angkurawaranon C.
      • Jiraporncharoen W.
      • Chenthanakij B.
      • et al.
      Urbanization and non-communicable disease in Southeast Asia: a review of current evidence.
      ,
      • Eckert S.
      • Kohler S.
      Urbanization and health in developing countries: a systematic review.
      To create urban areas, the green vegetation cover is eroded, land-use changes, human settlement induces microclimatic changes, and this leads to unmatched levels of air quality caused by anthropogenic emissions such as industrial pollution, vehicular traffic, fossil fuels for energy, and cooking fuels for domestic use.
      • Kumar P.
      • Druckman A.
      • Gallagher J.
      • et al.
      The nexus between air pollution, green infrastructure and human health.
      The major contributors to air pollution worldwide are the transport emissions in cities, associated with health implications such as respiratory and cardiovascular diseases.
      • Heal M.R.
      • Kumar P.
      • Harrison R.M.
      Particles, air quality, policy and health.
      The impact of these climate events has already been documented on agricultural crop productivity, natural species diversity and distribution, and other ecosystem services such as flowering time and pollination.

      Anthropogenic activity leading to climate change: much to be understood

      The Mother Land Earth provides the basics for living through the availability of food, freshwater, and multiple other ecosystem services, as well as rich biodiversity. Humans use more than 70% of the global, ice-free land surface.

      Intergovernmental Panel on Climate Change, IPCC 2019. Summary for policymakers. In: Shukla PR, Skea J, Buendia EC et al editors. Climate change and land: an IPCC special report on climate change, desertification, land degradation, sustainable land management, food security, and greenhouse gas fluxes in terrestrial ecosystems,(in press).

      Massive deforestation leads to urbanization and industrialization, population explosion and resulting enhanced transportation and associated increasing vehicular pollution have only eroded the environment but not renewed it at the same rate. Primarily burning of fossil fuels such as coal and oil that have formed over millions of years through photosynthesis-based trapping of carbon is reverting to atmospheric carbon in a shorter time period, adding to the already increased level induced by anthropogenic activity. Second is the massive deforestation leading to unexpected higher levels of carbon in the atmosphere (acting as a sink). Primary emissions from industries and vehicles, secondary emissions and photochemical oxidation, and the concentrations of various air pollutants such as reactive trace gases and aerosols such as ozone, nitrogen, sulfur oxides, and soot have greatly increased, especially in heavily populated and agricultural environments around the globe.
      • Reinmuth-Selzle K.
      • Kampf C.J.
      • Lucas K.
      • et al.
      Air pollution and climate change effects on allergies in the anthropocene: abundance, interaction, and modification of allergens and adjuvants.
      The ever-increasing population continuously supported by improved agriculture and forestry productivity in the Anthropocene era has continuously and abruptly led to environmental variation such as change in biodiversity and vegetation, air quality, precipitation duration, and temperature recordings on local, regional, and global scales as climate change events.
      • Reinmuth-Selzle K.
      • Kampf C.J.
      • Lucas K.
      • et al.
      Air pollution and climate change effects on allergies in the anthropocene: abundance, interaction, and modification of allergens and adjuvants.
      The Intergovernmental Panel on Climate Change Reports
      • Hegerl G.C.
      • Zwiers F.W.
      • Braconnot P.
      • et al.
      Understanding and attributing climate change.
      ,
      Intergovernmental Panel on Climate Change, IPCC
      document evidence of increased CO2 concentrations and other greenhouse gases leading to a higher frequency of extreme climate events and being involved in the exchange of energy, water, and aerosols between the land surface and atmosphere and defining climatic conditions. As a consequence of anthropogenic emissions, the planet Earth is facing an increased greenhouse effect leading to global warming, unanticipated climatic events such as extreme heat waves, temperature extremes, shrinking glaciers, forest fires, droughts, and floods, all of which put human health at risk. Paleoclimatic studies have clearly recorded that, within the late Quaternary period, the Holocene (»11,600 years to the present) has witnessed a highly variable climate.
      • Kar R.
      • Quamar M.
      Pollen-based Quaternary palaeoclimatic studies in India: an overview of recent advance.

      Prevalence and economic impact of noncommunicable diseases caused by climate change

      According to various timely estimates released by WHO, NCDs had killed 38 million and 41 million people by the years 2012 and 2016, respectively, an undesired but real scenario that is still increasing.

      Noncommunicable diseases country profiles 2018. Geneva: World Health Organization; 2018. Licence: CC BY-NC-SA 3.0 IGO.

      NCD deaths have occurred at the highest rate in the WHO Southeast Asia region, from 6.7 million to 8.5 million from 2000 to 2012, and in the western Pacific region, from 8.6 to 10.9 million. During 2011 to 2025, cumulative economic losses caused by NCDs under a business-as-usual scenario in low-income and middle-income countries have been estimated at nearly US$7 trillion as against the estimated annual US$11.2 billion cost of implementing impactful interventions to reduce the NCD burden.

      Global status report on noncommunicable diseases 2014. Geneva: World Health Organization; 2014.Licence: CC BY-NC-SA 3.0 IGO.

      Five years from now, (2025) globally NCDs will be accountable for 70% of all deaths, of which 85% will be in developing countries, especially low-income and middle-income countries.

      Noncommunicable diseases country profiles 2018. Geneva: World Health Organization; 2018. Licence: CC BY-NC-SA 3.0 IGO.

      Global status report on noncommunicable diseases 2014. Geneva: World Health Organization; 2014.Licence: CC BY-NC-SA 3.0 IGO.

      Noncommunicable diseases progress monitor 2015. Geneva: World Health Organization; 2014. Licence: CC BY-NC-SA 3.0 IGO.

      Prevalence of respiratory disorders

      A large body of epidemiologic studies have been revealing a general increase in both the incidence and the prevalence of respiratory diseases, including allergic rhinitis (hay fever) and asthma.
      • Damialis A.
      • Traidl-Hoffmann C.
      • Treudler R.
      Climate change and pollen allergies.
      During the last 60 years, there has been an increase in the epidemic prevalence of allergic disorders, which is expected to reach up to 4 billion in the 2050s.
      • Lötvall J.
      • Pawankar R.
      • Wallace D.V.
      • et al.
      American academy of allergy, asthma & immunology (AAAAI), the American college of allergy, asthma & immunology (ACAAI), the European academy of allergy and clinical immunology (EAACI), and the word allergy organisation (WAO). We call for iCAALL: international collaboration in asthma, allergy and immunology.
      Asthma, allergic rhinitis, atopic dermatitis, and inhalant sensitization have been appropriately referred to as the first wave of the epidemic of the twenty-first century, which will become a pandemic comparable with infectious diseases.
      • Holgate S.T.
      The epidemic of allergy and asthma.
      • Vlahov D.
      • Galea S.
      Urbanization, urbanicity, and health.
      • Prescott S.
      • Allen K.J.
      Food allergy: riding the second wave of the allergy epidemic.
      • Asam C.
      • Hofer H.
      • Wolf M.
      • et al.
      Tree pollen allergens—an update from a molecular perspective.

      How climate change and air pollution affect human health

      The undesired impacts on human health caused by the combination of climate change and air pollution have become the defining issues for policy makers.
      • Paramesh H.
      Air pollution and allergic airway diseases: social determinants and sustainability in the control and prevention.
      Air pollution, climate change, and reduced biodiversity caused by urban lifestyles are presenting threats to human health with unfavorable effects on a variety of chronic disorders such as respiratory and cardiovascular diseases.
      • Pawankar R.
      Climate change, air pollution, and biodiversity in Asia Pacific: impact on allergic diseases.
      The constant exposure to pollutants and the reduced biodiversity in urban settings have led to limited plant, animal, and microbial interaction, which in turn is causing immune dysfunction and impaired immune tolerance in humans compared with rural populations exposed to the same levels of pollution but residing in habitats rich in flora and fauna. Air pollution is strongly associated with climate change.
      • D’Amato G.
      • Vitale C.
      • Rosario N.
      • et al.
      Climate change, allergy and asthma, and the role of tropical forests.
      A recent position statement on climate change and health impacts from the European Respiratory Society (ERS) was developed after a workshop co-organized by the Health and Environment Network (HENVINET) Project and the American Thoracic Society. The position statement highlights climate-related health impacts, including deaths and acute morbidity caused by heat waves, increased frequency of acute cardiorespiratory events caused by higher concentrations of ground-level ozone, changes in the frequency of respiratory diseases caused by transboundary particle pollution, and altered spatial and temporal distribution of allergens (pollens, molds, and mites) and some infectious disease vectors.
      • Ayres J.G.
      • Forsberg B.
      • Annesi-Maesano I.
      • et al.
      Climate change and respiratory disease: European respiratory society position statement.
      • D’Amato G.
      • Pawankar R.
      • Vitale C.
      • et al.
      Climate change and air pollution: effects on respiratory allergy.
      • Krishna M.T.
      • Mahesh P.A.
      • Vedanthan P.
      • et al.
      An appraisal of allergic disorders in India and an urgent call for action.
      According to the WHO, every year 3 million people die prematurely because of outdoor air pollution, which is heaviest in major cities of Asia, Africa, and Latin America.
      • Pawankar R.
      Climate change, air pollution, and biodiversity in Asia Pacific: impact on allergic diseases.
      Fossil fuel and transportation are the main sources of air pollution (eg, sulfur oxide and nitrous oxides) released into the atmosphere, leading to health problems, poor air quality, and acid rain. Air pollutants show these effects by causing direct cellular injury or by inducing intracellular signaling pathways and transcription factors that are known to be sensitive to oxidative stress. Outdoor air pollution exacerbates asthma in people who already have the condition.
      • Pawankar R.
      • Wang J.Y.
      • Wang I.J.
      • et al.
      Asia pacific association of allergy asthma and clinical immunology white paper 2020 on climate change, air pollution, and biodiversity in asia-pacific and impact on allergic diseases.

      Prevalence of asthma

      A global study found that from 9 million to 23 million and from 5 million to 10 million annual asthma emergency room visits globally in 2015 could be attributable to O3 and particulate matter (PM) with a diameter of 2.5 μm or less (PM2.5), respectively, representing 8% to 20% and 4% to 9% of the annual number of global visits, respectively The top 3 countries for both asthma incidence and prevalence in Asia are India, China, and Indonesia, driven largely by population size; nearly half (48%) of estimated O3-attributable and more than half (56%) of PM2.5-attributable asthma emergency room visits were estimated in Southeast Asia (including India), and western Pacific regions.
      • Anenberg S.C.
      • Henze D.K.
      • Tinney V.
      • et al.
      Estimates of the global burden of ambient PM2.5, ozone, and NO2 on asthma incidence and emergency room visits.
      Of all countries globally, India and China had the most estimated asthma emergency room visits attributable to total air pollution concentrations, respectively contributing 23% and 10% of global asthma emergency room visits estimated to be associated with O3, 30% and 12% for PM2.5%, and 15% and 17% for nitrogen dioxide (NO2). The national pediatric asthma incidence that may be attributable to anthropogenic PM2.5 was estimated to be 57% in India, 51% in China, and more than 70% in Bangladesh. PM2.5 has been causatively linked to the most premature deaths. Acute respiratory tract infections, asthma, chronic obstructive pulmonary disease, exacerbations of preexisting obstructive airway disease, and lung cancer are proven adverse respiratory effects of air pollution.
      • Pawankar R.
      • Wang J.Y.
      • Wang I.J.
      • et al.
      Asia pacific association of allergy asthma and clinical immunology white paper 2020 on climate change, air pollution, and biodiversity in asia-pacific and impact on allergic diseases.
      The drastic changes in climate and air quality have a quantifiable impact on the morbidity of respiratory diseases.
      • D’Amato G.
      • Pawankar R.
      • Vitale C.
      • et al.
      Climate change and air pollution: effects on respiratory allergy.
      An easily understandable tabular association of environmental changes with impacts on health systems is presented in Table 1.
      • D’Amato G.
      • Vitale C.
      • Rosario N.
      • et al.
      Climate change, allergy and asthma, and the role of tropical forests.
      Climate change as been found to affect human health via 3 pathways. Primarily, the direct unpredictable impacts are caused by the associated extreme weather events of heat and drought, heavy rainfall, flooding, and cyclones. The consequences of the primary events are witnessed through their impacts on natural ecosystems, agricultural productivity, species migration, and through changing the burden and pattern of distribution of vector-borne, water-borne, and food-borne diseases. In addition, climate change may affect health indirectly, via social institutions, resulting in health-related unemployment, undernutrition, mental ill-health, violence, and conflict.
      • Wheeler N.
      • Watts N.
      Climate change: from science to practice.
      Table 1Climate change and impact on the biosphere
      Adapted from D’Amato G, Vitale C, Rosario N et al. Climate change, allergy and asthma, and the role of tropical forests. World Allergy Organ J 2017;10(1):11; with permission.
      Climate EventsAgriculture, ForestryHuman Health Impact
      Heavy precipitation events: frequency increases over most areasDamage to crops; soil erosion, inability to cultivate land, waterlogging of soils; adverse effects on quality of surface and groundwater; contamination of water supplyDeaths, injuries, infectious diseases, allergies, and dermatitis from floods and landslides
      Area affected by droughtLand degradation, lower yields/crop damage and failure; livestock deaths; land degradation; more widespread water stressIncreased risk of food and water shortage; increased risk of water-borne and food-borne diseases; cardiovascular disorders
      Number of intense tropical cyclonesDamage to crops; windthrow of trees; power outages cause disruption of public water supplyIncreased risk of water-borne and food-borne diseases; asthma
      Incidence of extreme highsea levelSalinization of irrigation and well water; decreased freshwater availability caused by saltwater intrusionIncrease in stress-related disease; other allergic conditions

      Climate change affecting biosphere

      A large number of evidence-based studies
      • Reinmuth-Selzle K.
      • Kampf C.J.
      • Lucas K.
      • et al.
      Air pollution and climate change effects on allergies in the anthropocene: abundance, interaction, and modification of allergens and adjuvants.
      ,
      • D’Amato G.
      • Vitale C.
      • Rosario N.
      • et al.
      Climate change, allergy and asthma, and the role of tropical forests.
      ,
      • Rogers C.A.
      • Wayne P.M.
      • Macklin E.A.
      • et al.
      Interaction of the onset of spring and elevated atmospheric CO2 on ragweed (Ambrosia artemisiifolia L.) pollen production.
      ,
      • Kaushik G.
      • Khalid M.A.
      Climate change impact on forestry in India.
      have explored and detailed the indirect unending impacts of climatic events on various components of the biosphere, such as:
      • Altered agricultural productivity
      • Changing patterns of natural species diversity and distribution
      • Migration of pests and vectors affecting pollination
      • Easy entry of new invasive plant species to new areas
      • Phenology (ie, ecosystem factors such as flowering time and onset, duration, and intensity of pollination, fruiting pattern)
      • Altered allergenicity of pollen and fungal spores
      The primary indirect effect is from the spatial increase in temperature caused by greenhouse gas concentrations varying with geography. Water vapor is the primary greenhouse gas at the equator, creating a warm, humid climate, so the influence of CO2 is less pronounced, whereas, at the poles and in deserts, the effect is impactful. Likewise, the winters at northern latitudes are colder and drier and will get warm faster because of CO2. The variation arising from anthropogenic greenhouse gases is driving extreme climatic events, with a strong influence on plant biology worldwide.
      • Ziska L.H.
      • Beggs P.J.
      Anthropogenic climate change and allergen exposure: the role of plant biology.
      The second direct factor affecting all aspects of plants’ life cycles is the increasing atmospheric CO2 concentration, which affects plant growth. Atmospheric CO2is the raw material for terrestrial green plant photosynthesis, and thus it represents the first molecular link in the food chain of the entire Earth. The impact of this factor is species and tissue development dependent. Under optimal conditions of temperature and light intensity, the rate of photosynthesis markedly increases.
      National Research Council, NRC
      Managing water resources in the west under conditions of climate uncertainty: a proceedings.

      Phenology and climate change

      The mechanism of flowering is primarily dependent on photoperiodism: the effect of day length (periodicity), temperature, Co2, and water content. A critical duration of light in long-day plants and dark in short-day plants is required by different species. The plant pigment phytochrome in its 2 forms phytochrome red (Pr660) and phytochrome far red (Pfr730) perceives the light stimulus, leading to hormonal changes and induction of flowering. Addressing the effect of these environmental factors on flowering events such as time of day of anthesis and flowering time (duration from germination till flowering) is essential to understand the adaptation of plants/crops to changing climatic conditions. Flowering is the decisive phase determining reproductive success and seed set in the later life cycle of plants emerging after the vegetative growth phase.
      • Jagadish S.V.K.
      • Bahuguna R.N.
      • Djanaguiraman M.
      • et al.
      Implications of high temperature and elevated CO2 on flowering time in plants.
      Phenology is the study of effects of climatic factors on the life cycle events of animals and plants. The various reproductive events in the life cycles of flowering plants are termed phenoevents, such as the onset of flowering and fruiting and seed dispersal, and they follow a seasonal pattern. Phenoevents serve as sensor-indicators for climate change, of migration of species to higher elevations and altitudes.
      • Katelaris C.H.
      • Beggs P.J.
      Climate change: allergens and allergic diseases.
      ,
      • Shivanna K.R.
      • Tandon R.
      Reproductive ecology of flowering plants: a manual.
      A noteworthy example is the accurate long-term records on the phenology of flowering time of cherry blossom (Prunus jamasakura) in Japan for the past 1200 years, coinciding with the cherry blossom festival from time immemorial. The flowers blossom an average of 7 days earlier compared with records before 1970.
      • Primack R.B.
      • Higuchi H.
      • Miller-Rushing A.J.
      The impact of climate change on cherry trees and other species in Japan.
      For a nearly 50-year dataset from a Europe-wide network (1951–1996), the International Phenological Gardens reported an increase in annual growing season by approximately 11 days.
      • Menzel A.
      Trends in phenological phases in Europe between 1951 and 1996.
      A detailed compilation of the effects of 2 environmental factors, increased CO2 and temperature, alone or in combination, on the flowering times of a wide range of flowering species and specific ecosystems has been analyzed and reported.
      • Jagadish S.V.K.
      • Bahuguna R.N.
      • Djanaguiraman M.
      • et al.
      Implications of high temperature and elevated CO2 on flowering time in plants.
      As per the records of flowering time, pollen data, and herbaria, for perennials, flowering time had advanced, with an annual advancement of 9 days and a delay of up to 16 days being recorded.
      • Crimmins T.
      • Crimmins M.
      • Bertelsen C.D.
      Onset of summer flowering in a ‘Sky Island’ is driven by monsoon moisture.
      ,
      • Hulme P.E.
      Contrasting impacts of climate-driven flowering phenology on changes in alien and native plant species distributions.
      On average, flowering time advanced by 4 to 6 days per 1°C according to historical data for more than 400 plant species and deciduous trees at decadal time scale for the past few centuries. For annual grasses, flowering time has been delayed up to 6 days under increased CO2 levels, whereas, in combination with warming effects, advancement of 2 to 4 days has been reported. For C4 weeds, an advanced flowering of 10 to 15 days has been reported under high CO2 concentrations, whereas, for desert shrubs under high-temperature regimes, flowering has been advanced by 20 to 41 days.

      Impact on phenology in India

      An overall delay in flowering has been recorded for legumes. In India, the data for different varieties of peach, apple, and kiwi growing in hilly regions show a considerable delay in flowering in 2008 owing to low winter temperatures, whereas in 2006 and 2009 it was early because of warmer winters.
      • Rana J.C.
      • Sharma S.K.
      Plant genetic resources management under emerging climate change.
      In the Uttaranchal state, located in the upper hilly region (Himalayas) of north India, the most notable evidence is the flowering of Rhododendron spp, which have been flowering15 days earlier with small flowers in relation to 15 to 20 years ago because of changing rainfall patterns.
      • Kaushik G.
      • Khalid M.A.
      Climate change impact on forestry in India.

      C3/C4 anatomy: adaptation to high temperature and increased CO2

      The shift in C3 and C4 plant types seems to be related to change in moisture and atmospheric CO2, with lower moisture and CO2 levels favoring the C4 plant types. The oscillating climate has resulted in mean temperatures in the tropics increasing by at least 1°C to 2°C as a result of increase in atmospheric CO2, methane, and other greenhouse gases.
      Intergovernmental Panel on Climate Change, IPCC
      General circulation models predict an intensification of the Indian summer monsoon as a consequence of the increased temperature,
      • Kaushik G.
      • Khalid M.A.
      Climate change impact on forestry in India.
      which is consistent with the paleoclimate record. These climatic changes can be expected to favor the expansion of C3 vegetation more than C4 vegetation for several reasons. Higher CO2 levels would enhance photosynthesis rates in C3 plants to a greater extent than in C4 plants. Higher temperatures would reduce the incidence of frost and promote the survival of C3 forest plants. Higher precipitation and soil moisture would favor the growth of C3 plants. Thus, the montane evergreen forest can be expected to expand into the grasslands, whereas C3 grasses and herbs could potentially replace C4 grasses in the grasslands.
      • Kaushik G.
      • Khalid M.A.
      Climate change impact on forestry in India.
      However, a counterargument is that C4 plants will have better adaptability for long-term survival in drier conditions because of being able to cope better with water stress and higher temperatures. An increase in C4 plants may result in ecosystems with more allergenic plant species.
      • Blando J.
      • Bielory L.
      • Nguyen V.
      • et al.
      Anthropogenic climate change and allergic diseases.

      Impact of climate on pollen allergy

      Aerobiology deals with the study of the impact of the bioparticulate matter present in the Earth’s atmosphere on human health. The bioparticulates described to cause allergic symptoms are pollen grains, fungal spores, insect debris, house dust mites, animal dander, chemicals, foods, and so forth.
      • Singh A.B.
      • Mathur C.
      An aerobiological perspective in allergy and asthma.
      Among all these agents, pollen grains and fungal spores are the predominant allergens in the air worldwide. Climate change is related to aeroallergens, in particular pollen, because various climate change events affect the phenological response of plant life cycles, leading to increased and faster growth, earlier start of pollen seasons, greater pollen production, and enhanced allergenic response in susceptible individuals.
      The word pollen is derived from a Latin word meaning fine flour or dust.
      • Jarzen D.M.
      • Nichols D.J.
      Pollen.
      The pollen is the minute vital part of flowering plants and has special morphology and function. Pollens are single cells representing the microgametophytes of seed plants destined to produce male gametes (sperm cells).
      • Stephen A.
      Pollen – a microscopic wonder of plant kingdom.
      Pollen allergens are classified into size classes and generally belong to the coarse fraction of air particulate matter (particle diameters >10 μm), but fungal spores and pollen fragments are also found in fine particulate matter (<2.5 μm; PM2.5), which can penetrate deep into the human respiratory tract and alveolar regions of the lung.
      • Reinmuth-Selzle K.
      • Kampf C.J.
      • Lucas K.
      • et al.
      Air pollution and climate change effects on allergies in the anthropocene: abundance, interaction, and modification of allergens and adjuvants.
      Pollen allergens are classified into size classes as detailed in Table 2.
      • Kremp O.W.
      Morphologic encyclopedia of palynology.
      Most of the living angiosperms have pollen grains in the range of 25 to 100 μm. Pollen of the families Boraginaceae, Piperaceae, Crypteroniaceae, and Cunoniaceae have low size ranges. Monocots have been reported to produce grains in the size range of 15 to 80 μm. Pollen of anemophilous plants are small, whereas those of entomophilous plants are large.
      • Agashe S.N.
      Pollen morphology. In: pollen and spores: applications with special emphasis on aerobiology and allergy.
      • Koenig J.Q.
      • Morgan M.S.
      • Horike M.
      • et al.
      The effect of sulfur dioxide on nasal and lung function in adolescents with extrinsic asthma.
      • Molfino N.A.
      • Wright S.C.
      • Katz I.
      • et al.
      Effect of low concentrations of ozone on inhaled allergen responses in asthmatic subjects.
      • Rusznak C.
      • Devalia J.L.
      • Davies R.J.
      The airway response to asthmatics to inhaled allergen after exposure to pollutants.
      • Puttonen E.
      • Pilstrom L.
      Purification of birch pollen extract by gel filtration. Chemical and immunological characterization of the fractions.
      • Richman P.G.
      • Gissel D.S.
      A procedure for total protein determination with special application to allergenic extract standardization.
      • Park J.W.
      • Ko S.H.
      • Kim C.W.
      • et al.
      Identification and characterization of the major allergen of the Humulus japonicus pollen.
      • Rawat A.
      • Singh A.
      • Singh A.B.
      • et al.
      Clinical and immunologic evaluation of Cedrus deodara pollen: a new allergen from India.
      • O'Conner C.J.
      • Ashford K.P.
      • Speeding D.J.
      Germination and metabolism of Pinus radiata pollen in the presence of sulfur dioxide.
      • Omura M.
      • Matsuta N.
      • Mariguchi T.
      • et al.
      Variation in physiological and genetic characteristics and pollen grain number in Japanese pear depending on the growing conditions.
      • Majd A.
      • Ghanati F.
      The effect of air pollution on the allergenicity of Pinus elderica (Pinaceae) pollen.
      • Ruffin J.
      • Liu M.Y.G.
      • Sessoms R.
      • et al.
      Effects of certain atmospheric pollutants (SO, NO and CO) on the soluble amino acids, molecular weight and antigenicity of some airborne pollen grains.
      • Bist A.
      • Pandit T.
      • Bhatnagar A.K.
      Variability in protein content of pollen of Castor bean (Ricinus communis) before and after exposure to the air pollutants SO and NO.
      • Kalkar S.A.
      • Jaiswal R.
      Effects of industrial pollution on pollen morphology of Cassia species.
      • Talukdar P.
      • Dutta A.
      Biomonitoring with special reference to leaf and pollen morphology in Cassia sophera L. to detect roadside air pollution.
      • Hinge V.
      • Tidke J.
      • Das B.
      • et al.
      Air pollution exacerbates effect of allergenic pollen proteins of Cassia siamea: a preliminary report.
      Table 2Size-based categorization of pollen grains
      From Morphologic Encyclopedia of Palynology by Gerhard Kremp © 1965 The Arizona Board of Regents. Reprinted by permission of the University of Arizona Press.
      Size (μm)Category
      <10Very small pollens (Myosotis)
      10–25Small pollens (Salix)
      25–50Medium pollens (Quercus)
      50–100Large pollens (Zea)
      100–200Very large pollens (Cucurbita)
      >200Giant pollens (Mirabilis)

      Climate and pollen morphology

      The wall of pollen is primarily divided into an inner intine and an outer sculptured exine. The inner layer is rich in cellulose and the outer wall is composed of sporopollenin, a tough, resistant biopolymer enabling the pollen to withstand extremely high temperatures of up to 3000°C, strong acids, and harmful radiation.
      • Stephen A.
      Pollen – a microscopic wonder of plant kingdom.
      ,
      • Agashe S.N.
      Pollen morphology. In: pollen and spores: applications with special emphasis on aerobiology and allergy.
      Chemically, intine is composed of cellulose and lignin. Chemically, the sporopollenin resembles lignin and is a polymerization product of hydrocarbons, carotenoid, and carotenoid esters. The pollen wall imparts protection to sperm while the pollen grain is traveling in the air from the anther to the stigma; it protects the vital genetic material from drying out. When pollen lands on a pistil of the same flower or another flower, the pollen germinates and a pollen tube emerges, which grows downward in the pistil to reach the ovule (female gametophyte), fertilize it, and begin a new generation. The entire process involves a variety of stored compounds, with glycoproteins predominating in the mature pollen grain.
      • Dahl A.
      • van den Bosch M.
      • Ogren T.
      Allergic pollen emissions from vegetation-threats and prevention.
      Pollen apertures are named for the various wall modifications, which may involve thinning, ridges, and pores. They serve as an exit for the pollen’s contents and allow shrinking and swelling of the grain caused by changes in osmotic potential of the surrounding medium. Morphologically, it is an aperture or a thinning of exine (except in operculate apertures) where the intine is thickened, except in the poplar plant (Populus), which lacks them.
      Pollen grains primarily cause asthma, allergic rhinitis, and allergic conjunctivitis in atopic patients.
      • Oh J.W.
      Pollen and climate. In pollen allergy in a changing world . A guide to scientific understanding and clinical practice.
      The distribution and prevalence of pollen allergy are subject to both geographic and chronologic variations.
      • Park H.J.
      • Lee J.H.
      • Park K.H.
      • et al.
      A six-year study on the changes in airborne pollen counts and skin positivity rates in Korea: 2008–2013.
      Pollen allergy is a topic for studying the interrelationship between air pollution and allergic respiratory diseases such as rhinitis and asthma.
      • D'Amato G.
      • Liccardi G.
      • D'Amato M.
      • et al.
      The role of outdoor air pollution and climatic changes on the rising trends in respiratory allergy.
      ,
      • Sedghy F.
      • Varasteh A.R.
      • Sankian M.
      • et al.
      Interaction between air pollutants and pollen grains: the role on the rising trend in allergy.
      Pollen grains are more sensitive at the early stages of development (anther wall development, microsporogenesis, and microgametogenesis) than at later stages (pollen maturation and anther dehiscence) or during the progamic phase (pollen hydration, germination, growth and guidance of the pollen tube). During maturation, pollen grains undergo various degrees of cellular dehydration before and/or after an anther dehiscence. The water content of pollen grains decreases to 40% to 58% and pollen becomes physiologically dormant until landing on a receptive stigma.
      • iron N.
      • Nepi M.
      • Pacini E.
      Water status and associated processes mark critical stages in pollen development and functioning.
      The ready-to-disperse pollen thus has a reduced metabolic activity to ensure long-term viability in the external environment. Bicellular pollen is generally more dehydrated and less metabolically active than tricellular pollen. Temperature variations have a strong effect on pollen desiccation. Stacks of rough endoplasmic reticulum are largely dissociated in heat-stressed pollen, consequently affecting protein processing and secretion.
      • Ciampolini F.
      • Shivanna K.R.
      • Cresti M.
      High humidity and heat stress causes dissociation of endoplasmic reticulum in tobacco plants.
      Heat stress induces adverse effects on dehiscence of anthers and discharge of pollen in rice.
      • Singh A.B.
      • Babu C.R.
      Studies on pollen allergy in Delhi: diurnal periodicity of common allergenic pollen.
      • Jagadish S.V.K.
      • Muthurajan R.
      • Oane R.
      • et al.
      Physiological and proteomic approaches to address heat tolerance during anthesis in rice (Oryza sativa L.).
      • Cunningham D.D.
      Microscopic examination of air.
      • Shivpuri D.N.
      • Singh A.B.
      • Babu C.R.
      New allergenic pollens of Delhi state, India and their clinical significance.
      Anonymous
      All India coordinated project on aeroallergens and human health. Report.
      • Singh K.
      • Shivpuri D.N.
      Studies in yet unknown allergenic pollens of Delhi state, metropolitan: botanical aspects.
      • Malik P.
      • Singh A.B.
      • Babu C.R.
      • et al.
      Atmospheric concentration of pollen grains at human height.
      • Mittre V.
      • Khandelwal A.
      Airborne pollen grains and fungal spores at Lucknow during 1969-1970.
      • Chanda S.
      • Sarkar P.K.
      Pollen grains as a causative agent of respiratory allergy with reference to aeropalynology of greater calcutta.
      • Singh A.B.
      • Kumar P.
      Aerial pollen diversity in India and their clinical significance in allergic diseases.
      • Singh N.
      • Devi K.K.
      Aerobiology and allergic human diseases in Manipur. II. Airborne pollen grains of Imphal, Imphal District.

      Pollinosis and pollen allergens

      Allergen release from pollen is a prerequisite for sensitization and elicitation of the allergic symptoms in humans. A 2-route process has been suggested: first, outside the individual organism when pollen grains are spreading through the atmosphere, and, second, on reaching and in contact with the mucosal surface of the upper respiratory tract. Aeroallergenic particles such as pollen and plant/pollen-derived submicronic (<10 μm) and paucimicronic (<1 μm) particles can reach the lower airways, eliciting allergic symptoms in susceptible people. These particles are mainly composed of starch granules and polysaccharide particles, which may be absent in mature pollen.
      • Prado N.
      • De Linares C.
      • Sanz M.L.
      • et al.
      Pollensomes as natural vehicles for pollen allergens.
      The most important outdoor sources of allergens are pollen grains from anemophilous plants, including trees, grasses, and weeds. To increase the chance of fertilization, wind-pollinated plants have evolved characteristic features such as small, dehydrated pollen with good aerodynamic properties that allow dissemination over hundreds of kilometers.
      The presence of allergens in pollen and their levels of expression may vary depending on plant species, changing climate, maturation stage, and environmental factors (pollution). Because of changes in climatic conditions, observations on diurnal and seasonal prevalence become very important because information gained in this way has direct applications to treating patients with hay fever.
      • Sharma D.
      • Dutta B.K.
      • Singh A.B.
      Seasonal variation in atmospheric pollen concentration in humid tropical climate of South Assam, India.
      Climate change affects aeroallergens and, in particular, plant allergens, as reported by several experimental and epidemiologic studies. As described earlier in the article, climate change interacts with the increased concentration of atmospheric CO2 to boost plant growth, which in turn leads to increased pollen production, affecting anther dehiscence and pollen dispersal and transport, accelerating the start and duration of the pollen season, along with the emergence of new pollen species in new locations that are not endemic to the specific area.
      • Pawankar R.
      • Wang J.Y.
      • Wang I.J.
      • et al.
      Asia pacific association of allergy asthma and clinical immunology white paper 2020 on climate change, air pollution, and biodiversity in asia-pacific and impact on allergic diseases.
      The onset, duration, and intensity of pollination, the fruiting patterns and sporulation of fungi, along with the allergen content and allergenicity of pollen grains, fungal spores, and other bioparticulates become altered under changing climatic conditions.
      • Reinmuth-Selzle K.
      • Kampf C.J.
      • Lucas K.
      • et al.
      Air pollution and climate change effects on allergies in the anthropocene: abundance, interaction, and modification of allergens and adjuvants.
      ,
      • D’Amato G.
      • Vitale C.
      • Rosario N.
      • et al.
      Climate change, allergy and asthma, and the role of tropical forests.
      ,
      • D’amato G.
      • Vitale C.
      • De Martino A.
      • et al.
      Effects on asthma and respiratory allergy of Climate change and air pollution.
      Global warming–led increased CO2 in the atmosphere is reported to alter the start, duration, and intensity of the pollen season along with the rate of asthma exacerbations arising from respiratory infections and cold air inhalation.
      • D’amato G.
      • Vitale C.
      • De Martino A.
      • et al.
      Effects on asthma and respiratory allergy of Climate change and air pollution.

      Allergenic plants, climate change, and pollutants affecting allergenicity

      In order to monitor the occurrence and abundances of pollen grains in the ambient air for early warning of allergic diseases as well as other health risks, a limited number of studies have been conducted in Southeast Asia.
      • Hu W.
      • Wang Z.
      • Huang S.
      • et al.
      Biological aerosol particles in polluted regions.
      A planned routine study is investigating the diurnal, seasonal, and annual fluctuations in the concentrations of atmospheric pollen, especially from allergenic plants, in relation to the meterological factors that will always be the governing factor in the correct diagnosis and therapeutic treatment of patients with pollen-induced respiratory allergic disorders.
      • Singh A.B.
      • Babu C.R.
      Studies on pollen allergy in Delhi: diurnal periodicity of common allergenic pollen.
      With a continuously changing climate, such information is essential for timely prevention and better patient outcomes in this era of customized precision treatment. Classic relevant studies of this topic are reviewed and highlighted later.
      Reports from the Australian Institute of Health and Welfare (AIHW) show that, in 2014 to 2015, nearly 1 in 5 Australians had pollen allergy, which amounts to 4.5 million citizens, mainly comprising the working population.
      • Rong J.
      • Michalska S.
      • Subramani S.
      • et al.
      Deep learning for pollen allergy surveillance from twitter in Australia.
      Grasses are the major aeroallergens in Australia, with varying clinical implications. The indigenous vegetation includes plant species of Eucalyptus, Acacia, and Sorthum grass along with introduced self-thriving northern hemisphere species such as ragweed, birch, and exotic invasive species expanding their range under the changing climate conditions.
      • Jalbert I.
      • Golebiowski B.
      Environmental aeroallergens and allergic rhino-conjunctivitis.
      For the available sporadic studies, pollen monitoring has been restricted to sites within the coastal state capital cities, where most of the Australian population resides.
      • Beggs P.J.
      • Katelaris C.H.
      • Medek D.
      • et al.
      Differences in grass pollen allergen exposure across Australia.
      ,
      • Singh A.B.
      • Pandit T.
      • Dahiya P.
      Changes in airborne pollen concentrations in Delhi, India.
      No national level prospective planned studies encompassing aerobiological monitoring, impact of climate change, along with increased hospital visits have been performed. Grasses have been showing increased atmospheric pollen concentrations resulting in the strong, consistent appearance of allergic asthma symptoms leading to heightened primary care or emergency department visits during peak pollen seasons. Because the seasonality is affected in an unpredictable manner by anthropogenic climate change, urbanization and global warming future strategies for prevention and treatment are difficult to plan. Ironically, little research has been focused on studying the impact of climate change on timing and duration of the grass pollen season in Australasia.
      • Davies J.M.
      • Beggs P.J.
      • Medek D.E.
      • et al.
      Trans-disciplinary research in synthesis of grass pollen aerobiology and its importance for respiratory health in Australasia.
      The available pollen indices published on the Internet are not based on current local pollen data and have been found to be misleading, risking public health.
      • Davies J.M.
      • Beggs P.J.
      • Medek D.E.
      • et al.
      Trans-disciplinary research in synthesis of grass pollen aerobiology and its importance for respiratory health in Australasia.
      It is disappointing that research on pollen aerobiology in a developed country such as Australia is lagging.
      The necessity and importance of aerobiological surveys was clear after a Melbourne thunderstorm asthma event in November 2016 that resulted in 10 deaths and 9000 patients requiring hospital emergency department visits for asthma attacks.
      • D’Amato G.
      • Tedeschini E.
      • Frenguelli G.
      • et al.
      Allergens as trigger factors for allergic respiratory diseases and severe asthma during thunderstorms in pollen season.
      Because of the lack of planned studies, a national pollen monitoring service within a partnership known as the AusPollen project has been advocated to fill the knowledge gap and attempt to map allergenic pollen and fungi distributions and correlate thee with respiratory allergy incidents and likely hospital visits.
      • Katelaris C.H.
      • Beggs P.J.
      Climate change: allergens and allergic diseases.
      However, few modern pollen monitoring programs use automated counting instruments capable of integrating with transdisciplinary research areas such as geospatial science climate change science, molecular allergology, and mathematical modeling of pollen transport and dispersal.
      • Ziska L.H.
      • Beggs P.J.
      Anthropogenic climate change and allergen exposure: the role of plant biology.
      ,
      • Davies J.M.
      • Beggs P.J.
      • Medek D.E.
      • et al.
      Trans-disciplinary research in synthesis of grass pollen aerobiology and its importance for respiratory health in Australasia.
      A study assessed atmospheric pollen concentrations and the clinical grass pollen season and grass pollen peaks over a long time period (1995–2013) for various cities in Australia, such as Brisbane, Canberra, Darwin, Hobart, Melbourne, and Sydney. Climate, weather, and meteorological variables have been identified as influencing factors for the pollen season and larger-scale climate fluctuations events such as the El Niño. The delayed and lessened 1997 to 1998 grass pollen season in Brisbane corresponded with a 12-month to 14-month El Niño effect that started early in 1997, which was associated with below-average rainfall in eastern subtropical Queensland, and this is an added dimension of climate change impact.
      • Beggs P.J.
      • Katelaris C.H.
      • Medek D.
      • et al.
      Differences in grass pollen allergen exposure across Australia.

      Thunderstorm-associated asthma epidemics in pollen seasons

      The Intergovernmental Panel on Climate Change Reports
      • Hegerl G.C.
      • Zwiers F.W.
      • Braconnot P.
      • et al.
      Understanding and attributing climate change.
      ,
      Intergovernmental Panel on Climate Change, IPCC
      document evidence of increased concentrations of CO2 and other greenhouse gases leading to a higher frequency of extreme climate events. Thunderstorms present a unique sum of environmental factors that lead to increase aeroallergen burden.
      • Weber R.W.
      Meteorologic variables in aerobiology.
      Some of the first observation-based evidence regarding thunderstorms and asthma outbreaks was reported from East Birmingham Hospital (Birmingham, United Kingdom) on July 6 and 7, 1983, leading to increased hospital visits.
      • Packe G.E.
      • Ayres J.
      Asthma outbreak during a thunderstorm.
      In the United Kingdom, a large number of thunderstorms (those with a large number of lightning discharges, such as electromagnetic impulses or sferics), probably after days of high grass pollen counts, have been associated with heightened emergency department visits, especially among child and adult asthmatics.
      • Weber R.W.
      Meteorologic variables in aerobiology.
      The 2016 asthma epidemic in Melbourne, Victoria, represented an unusual association of environmental factors, such as prevailing weather wind conditions and torrential rain combined with a high pollen count (the dominant aeroallergen was grass pollen with density >100/m3), resulting a city-wide spread of huge pollen and pollen-derived particles of respirable size. Melbourne was unprepared for the rapid response needed to combat the growing medical emergencies, and this day tested the capacity of Melbourne’s health system.
      • D’Amato G.
      • Tedeschini E.
      • Frenguelli G.
      • et al.
      Allergens as trigger factors for allergic respiratory diseases and severe asthma during thunderstorms in pollen season.
      The focus of the European and Mediterranean Plant Protection Organization is the alien, invasive, and noxious plant species Ambrosia artemisiifolia L. (common ragweed), which has highly allergenic pollen.
      • Damialis A.
      • Traidl-Hoffmann C.
      • Treudler R.
      Climate change and pollen allergies.
      Ragweed, a native of North America, has been invading large areas of South America and Europe for the last few decades and has been identified as a major contributor to severe respiratory allergic diseases. The plant has been rightly described as successful dominant species in abandoned lands even under severe ecophysiologic conditions of extreme and unpredictable environments.
      • Bazzaz F.A.
      Ecophysiology of Ambrosia artemisiifolia: a successional dominant.
      The species has naturalized across Europe at a rapid rate, and accounts for high sensitization rates. The most important allergen is named Amb a 1. In another German health study, immunoglobulin E sensitization rates to A artemisiifolia were 8.2% among German adults, with the prevalence increasing even at very low concentrations (5–10 pollen grains per cubic meter of air), which were sufficient to trigger allergic reactions in sensitive patients. Sikoparija and colleagues
      • Sikoparija B.
      • Skjøth C.A.
      • Celenk S.
      • et al.
      Spatial and temporal variations in airborne Ambrosia pollen in Europe.
      reported increased prevalence and incidence of asthma with this new allergen at a high frequency compared with other pollen types. The effect of doubling CO2 levels led to a 61% increase in the amount of pollen, whereas another study reported an increase in major allergen concentration, Amb a 1, with increasing CO2 with no change in total protein level.
      • Katelaris C.H.
      • Beggs P.J.
      Climate change: allergens and allergic diseases.
      ,
      • Beggs P.J.
      Impacts of climate change on aeroallergens: past and future.
      Furthermore, ragweed pollen collected along high-traffic roads showed a higher allergenicity than pollen sampled in vegetated areas, probably caused by traffic-related pollution. The overall impact will be altered pollen season timing and load, and hence change in exposure.
      • D’Amato G.
      • Vitale C.
      • Rosario N.
      • et al.
      Climate change, allergy and asthma, and the role of tropical forests.
      About a third of the airborne pollen increase is caused by on-going seed dispersal, irrespective of climate change. The remaining two-thirds are related to climate and land-use changes that will extend ragweed habitat suitability in northern and eastern Europe and increase pollen production in established ragweed areas owing to increasing CO2.
      • Damialis A.
      • Traidl-Hoffmann C.
      • Treudler R.
      Climate change and pollen allergies.
      ,
      • Katelaris C.H.
      • Beggs P.J.
      Climate change: allergens and allergic diseases.
      There is a long-term record of 27 years (1981–2007) of pollen counts, meteorological factors, and clinical data for western Liguaria (northwest Italy), thanks to a detailed cause-effect study highlighting the effect of climate variables on the allergic sensitization rate. The duration of pollen seasons was recorded to lengthen for Parietaria (85 days), olive (18 days), and cypress (18 days), with an advancement in their start dates (Table 3). Except for the grasses, the pollen load increased for the other 2 stated species. The noteworthy analysis was the constant increase in pollen sensitization through the year with the increasing pollen load, whereas sensitization to house dust mite remained stable.
      • Ariano R.
      • Canonica G.W.
      • Passalacqua G.
      Possible role of climate changes in variations in pollen seasons and allergic sensitizations during 27 years.
      Table 3Start and end dates and durations of the pollen seasons of 5 allergenic plants under consideration (5-year averages)
      Adapted from Ariano R, Canonica GW, Passalacqua G. Possible role of climate changes in variations in pollen seasons and allergic sensitizations during 27 years. Ann Allergy Asthma Immunol 2010;104(3):215–22; with permission.
      Pollen1981–19851986–19901991–19951996–20002001–2007
      SEDSEDSEDSEDSED
      Birch711659142148765714181451331044414579
      Cypress3091461783059615432661112303121161300138196
      Parietaria107291219552792171443172703329627524342304
      Olive15120256124267781182261091201826510518074
      Grass144230971022571051152291061362169911821487
      Abbreviations: D, duration; E, end; S, start.

      South Asia

      Only scant information is available from Southeast Asian countries, including India. The airspora in Southeast Asia, a tropical region, mainly comprises trees and shrubs flourishing year-round, with an abundance of ferns. There is no distinct definable major flowering season for plants compared with temperate countries.
      • Ong E.K.
      • Singh M.B.
      • Knox R.B.
      Seasonal distribution of pollen in the atmosphere of Melbourne: an airborne pollen calendar.
      • Calderón-Ezquerro M.C.
      • Guerrero-Guerra C.
      • Martínez-López B.
      • et al.
      First airborne pollen calendar for Mexico City and its relationship with bioclimatic factors.
      • Werchan M.
      • Werchan B.
      • Bergmann K.C.
      German pollen calendar 4.0–update based on 2011–2016 pollen data.
      • Mandal J.
      • Chakraborty P.
      • Roy I.
      Prevalence of allergenic pollen grains in the aerosol of the city of Calcutta, India – a two year perspective study.
      • Mari Bhat M.
      • Rajasab A.H.
      Flowering calendar of potentially allergenic pollen producing plants of Gulbarga.
      • Singh A.B.
      • Dahiya P.
      Aerobiological researches on pollen and fungi in India during the last fifty years.
      • Mondal A.K.
      • Mondal S.
      • Mandal S.
      Pollen production in some plant taxa with a supposed role in allergy in Eastern India.
      • Singh A.B.
      • Kumar P.
      Common environmental allergens causing respiratory allergy in India.

      Singh BP, Singh AB, Gangal SV. Pollen Calendars of different states of India. Delhi (India):CSIR Centre for Biochemicals, Delhi,India; 199.

      • Singh A.B.
      • Khandelwal A.
      An atlas of allergenically significant plants of India.
      In an investigational study based on the medical data records of patients visiting University Hospital in Gyeonggi Province Seoul, Korea, from 1999 to 2008, a possible correlation of skin test positivity results and hospitalization of patients with tree pollen allergy affected temporally by meteorologic variations is reported. Controlling for the air pollutant levels during the study period of months April to July, a contributory association of increasing minimum temperature in March (preflowering period) with higher pollen counts leading to increase tree pollen sensitization and hence more hospital visits has been suggested. In Korea, pollen levels of trees are higher than those of grass/weeds, with yearly tree pollen accounting for 95% in the spring season, which extends from March to May, as did the study period.

      KimS, Park H, JangJ. Impact of meteorological variation on hospital visits of patients with tree pollen allergy. BMC Public Health 2011;11:890.

      Among several cities in Korea for which pollen counts are monitored, Japanese cedar (JC) pollen was detected only in Jeju as the most frequent sensitizer among outdoor aeroallergens. The sensitization rates for JC pollen are much higher (33.8%) in Jeju than in Seoul (1.1%) and Suwon (0.7%). A first-of-its-kind study on pollinosis to JC pollen in Jeju City, South Korea, a temperate geographic zone, has been reported. The JC has been the dominant tree species as a windbreak for the tangerine orchard industry. A study on school children from Jeju in northern region (NR) and Seogwipo in southern region (SR) locations on aeroallergen sensitization showed the highest sensitization to Dermatophagoides pteronyssinus (35.8%), followed by Dermatophagoides farinae (26.2%), and JC pollen (17.6%). The JC pollen season was estimated from 2011 to 2013.
      In the SR, the JC pollen season lasted for 47 days in 2011, 72 days in 2012, and 95 days in 2013, whereas in the NR it lasted for 43 days in 2011, 65 days in 2012, and 65 days in 2013. The JC pollen season started earlier and lasted longer in the SR than in the NR (see Table 3). For pollen counts measured on the peak days, the level of JC pollen in the atmosphere in the SR was estimated to be 2 to 8 times higher than that in the NR. Overall, the JC pollen season in Jeju can be considered to be from late January to mid-April. A case of JC pollinosis was defined as one with pollinosis symptoms present during the JC efflorescence season in a patient sensitized to JC pollen. The rate of sensitization to JC among schoolchildren in Jeju has undoubtedly increased over time, and, as postulated earlier, a higher rate of sensitization in the older participants might be related to their longer cumulative environmental exposure to pollen. Interestingly, an age-related increment in sensitization was observed in the Seogwipo residents but not in the Jeju residents. This finding could be related to the difference in climate between the 2 geographic regions. The sensitization rate for JC pollen has been increasing year by year. In 1998, the sensitization rate for JC pollen was 9.7%, which increased to 18.2% in 2008,17.6% in 2010, and 24.4% in 2013 among schoolchildren in Jeju (unpublished data from the Environmental Health Center). Why is the rate of sensitization to JC pollen increasing? During the JC pollen season, there was a difference in the mean temperature between the geographic regions. The mean temperature during the main efflorescence season for JC pollen was higher by 2.0°C in February and by 1.9°C in March in Seogwipo than in Jeju. It is hypothesized that there may be 2 ways that global climate change could influence human health: an indirect effect by increasing the average temperature, and a direct effect caused by CO2-induced stimulation of photosynthesis and plant growth.
      • Katelaris C.H.
      • Beggs P.J.
      Climate change: allergens and allergic diseases.
      ,
      • Park J.W.
      Revised pollen calendar in Korea.
      Warmer weather evokes earlier flowering, more effective pollen scattering in the air, and a prolonged efflorescence season.
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      • Kumar P.
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      The nexus between air pollution, green infrastructure and human health.
      The current study supports the hypothesis that any global warming, especially in the flowering season, might increase the rate of sensitization to JC pollen in future, which results in a greater prevalence of pollinosis. The prevalence of symptomatic JC pollinosis is estimated to be half that of JC pollen sensitization, regardless of the region. This study is the first to address the relationship between pollen counts, sensitization rate, and the prevalence of JC pollinosis in Jeju, Korea.

      Lee J, Lee KH, Lee HS, et al. Japanese Cedar (Cryptomeria japonica) Pollinosis in Jeju, Korea: Is It Increasing? Allergy Asthma Immunol Res 2015;7:295-300.

      A 6-year study (2008–2013) from Seoul, Korea, evaluated the changes in pollen count and retrospectively examined the Skin Prick Test (SPT) results of 4442 patients of an asthma clinic. Meteorologic observations suggest no significant annual increase in pollen count for trees, grasses, and weeds. Clinically, the skin positivity rates in relation to pollen from grasses, weeds, and trees increased significantly during the study. The SPT rates increased significantly in response to pollen from walnut, popular, elm, and alder. Further, there was a significant correlation between the annual rate of change in pollen count and the rate of change in skin positivity rate for oak and Japanese hop. Therefore, there must be a climate-related increased increase in pollen count for the last 2 of these plants, whereas, for the 4 trees, despite no increase in pollen count, SPT increased positively, indicating there might be some enhancement in pollen allergenicity or more efficient pollen dispersal and duration of suspension in the air.
      • D'Amato G.
      • Liccardi G.
      • D'Amato M.
      • et al.
      The role of outdoor air pollution and climatic changes on the rising trends in respiratory allergy.
      ,
      • Park H.J.
      • Lee J.H.
      • Park K.H.
      • et al.
      A six-year study on the changes in airborne pollen counts and skin positivity rates in Korea: 2008–2013.
      In Japan after World War II, from early 1950 to early 1960, an undesired consequence arising from the mass afforestation program was the planting of 4.6 billion straight and tall JC trees (Cryptomeria japonica; ie, sugi), covering nearly 18% of the total land area of Japan. These trees were considered an ideal construction material but, after heavy tariff reduction in 1964, imported wood put the native foresters out of business. As a result, most of the sugi trees are standing abandoned, growing taller each year and producing more pollen year after year. The yellow green dust or JC pollen is scattered across the whole of Japan with the exception of Hokkaido and the Okinawan islands. Cedar pollen released from male flowers of sugi trees is dispersed in large quantities, over long distances (up to 100 km in some cases), remains airborne for more than 12 hours (prolonged season), and has been positively linked to uninterrupted increasing prevalence and severity of sugi pollinosis. The total JC pollen count is continuously increasing because there was a significant difference from 1995 to 2013 compared with the initial period of monitoring, 1965 to 1994 (P<.05). Sugi pollinosis was first reported in 1963. Seasonal Allergic Rhinitis (SAR) caused by JC pollen has been rightly declared to be the national affliction of Japan. The prevalence rate of SAR in Tokyo schoolchildren has been found to be extremely high by the International Study of Asthma and Allergies in Childhood (ISAAC). The pollen season is January to February. The temperature in these months influences the start of sugi pollen production and the pollen season. To worsen the conditions further, pollen release from the Japanese cypress (Chamaecyparis obtusa) follows, causing SAR, in the months of April and May, immediately after the release of JC pollen. JC and cypress pollens are considered to contain several components that cross react with each other, leading to additional severity in 70% of patients with sugi pollinosis. Therefore allergic symptoms can last for as long as 4 months, from February to May. Hot summers usually affect sugi trees, promoting flower bud development and increasing pollen production; meanwhile, cool summers have the opposite effects. Ironically, warm summers (higher mean temperature) have been affected by the side effects of global warming and climate change affecting plant morphology, flowering phenology, and pollen production. Climate change in Japan has been more severe, with temperatures increasing by an average of 1.158 C during the past 100 years. As such, the length of the sugi pollinosis season has increased since 1995, leading to increased prevalence, as stated earlier, and this is in line with the various reported epidemiologic studies highlighting global climate change–led temperature increase correlating with the increasing number of pollen-induced respiratory allergies. Pollution in the form of Asian dust (AD) and urban particulate matter (PM2.5) are risk factors for sugi pollinosis. AD is a seasonal phenomenon affecting much of eastern Asia, including Japan, and occasionally spreads around the globe, affecting the United States as well.
      • Park J.W.
      Revised pollen calendar in Korea.
      The number of spring dust storms has increased in the last 13 years. The frequency of the storms combined with increased air pollutant concentrations have been reported for adverse health effects such as increased allergic symptoms in Japan and Taipei. Animal studies have shown that the combination of AD plus JC pollen results in inducing type I hypersensitivity and sensitization in nonatopic or unsensitized atopic people.

      Yamada T, Saito H, Fujieda S. Present state of Japanese cedar pollinosis: the national affliction. J Allergy Clin Immunol 2014;133:632-9.

      Clinics care points

      • The incidence of allergic diseases is partially increasing due to climate change with increasing pollen productivity and duration of exposure.

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