Climate Change, Exposome Change, and Allergy: A Review

Abstract

Climate change is a global phenomenon affecting human health directly and indirectly. A key impact of climate change is the alteration of the exposome—the totality of environmental exposures (meaning all non-genetic) that an individual experiences throughout life. The exposome includes physical, chemical, biological, and psychosocial factors that influence the development and severity of allergic diseases. In this review, we discuss how climate change alters various aspects of the exposome, such as temperature, humidity, air pollution, pollen, radiation, chemical exposure, socioeconomic status, and gut microbiota. We further discuss how climate change can lead to the development or exacerbation of allergic diseases by altering the allergen load, the immune response, and the inflammatory pathways. We discuss the vulnerability of key populations, such as the elderly, children, pregnant women, and those of low socioeconomic status, who are more likely to suffer from the consequences of exposome change. We also propose some strategies for individuals and communities to mitigate the adverse consequences of exposome change arising from climate change. Finally, we summarize some key points for clinical care of allergic patients in the context of climate change and exposome change. We conclude that climate change, exposome change, and allergy are interrelated and require urgent attention from researchers, policymakers, and health professionals to reduce the burden of allergy.

Background

Climate change (CC) involves changes in various aspects of the climate system, such as temperature, precipitation, wind patterns, ocean currents, and atmospheric composition.¹ While CC has natural causes, such as changes in the solar activity or volcanic eruptions, the leading cause is human activities, especially the burning of fossil fuels like coal, oil, and gas. These activities emit greenhouse gases, such as carbon dioxide and methane, into the atmosphere, which act like a blanket and trap heat on the planet. Greenhouse gas concentrations are at their highest levels and emissions continue to rise. Consequently, the Earth is now about 1.1°C warmer than it was in the late 1800s.² The last decade (2011–2020) was the warmest on record, and surface temperature records are moving year after year.³ The impacts of CC are already visible and widespread, such as melting ice caps and glaciers, more frequent and intense extreme weather events, droughts, floods, or wildfires. CC also poses serious challenges for food security, water availability, energy supply, migration patterns and human security, and economic development. Some regions and populations are more vulnerable to climate impacts than others.

Allergies affect millions of people around the world and consists of a maladaptive immune system reaction to foreign substances or allergens, such as pollen, food, or insect venom. Allergens cause various symptoms depending on the type and severity of the allergy including sneezing, itching, swelling, rash, and in severe cases, difficulty breathing.

A multitude of social, chemical, nutritional, and microbial environmental exposures influence allergic and non-allergic respiratory disease programming and natural history. Clinical manifestations result from toxin-induced shifts in a host of molecular, cellular, and physiological states and their interacting systems. Moreover, individuals are not exposed to a single environmental factor at a given time, but to complex mixtures. This complexity has fostered the concept of the exposome, a framework that considers multiple external exposures as well as the internal environment indexed via physiological response biomarkers, accounting for exposure timing.⁴ Exposome is proposed as a complement to the human genome, recognizing that genetic factors alone cannot explain the causes of majority of chronic diseases.⁵ A systematic approach to measuring environmental exposures could fill this knowledge gap and identify potential prevention strategies. While acceptance was slow at first, in recent years exposomics has received a large amount of attention from the scientific community. Exposome includes external factors, such as air pollution, temperature, humidity, chemicals, radiation, or socioeconomic status (SES), and internal factors and biological responses, such as metabolism, hormones, oxidative stress, inflammation, and gut microbiota.⁶

This article aims to provide a comprehensive review of how CC affects exposome change (EC) and how this influences the prevalence and severity of various allergic conditions.

An Overview of Allergy and its types

Allergic reactions can be classified into four types based on the mechanism of the immune response: Type I (anaphylactic), Type II (cytotoxic), Type III (immunocomplex), and Type IV (cell-mediated).⁷ Types I, II, and III are immediate reactions that occur within 24 hours of exposure to the allergen. Type IV is a delayed reaction that usually appears after 24 hours of exposure.⁷ The most common types of allergies are indoor/outdoor allergies (such as hay fever/allergic rhinitis/or nasal allergies), skin allergies (such as eczema, hives, or contact dermatitis), food allergies, or insect allergies (such as bee stings or fire ant bites). Seasonal allergies are caused by airborne particles, such as pollen, that trigger symptoms like sneezing, runny nose, and itchy eyes and vary by calendar months reflecting when different types of pollen are released.⁸ Mold allergies arise from fungi that grow in damp places, such as bathrooms, basements, or outdoors.⁹ Insect allergies are caused by being stung or bitten by insects that inject venom or saliva eliciting swelling, itching, hives, and even anaphylaxis with the most common insects being bees, wasps, fire ants, or mosquitoes.¹⁰

Burden of Disease due to Allergy

Allergy causes significant morbidity, mortality, and economic burden. Allergic diseases vary depending on the type of allergy, the geographic region, the age group, and the method of diagnosis, with multiple allergies often coexisting in the same individual, increasing the complexity and severity of the condition. Allergies are often comorbid with asthma, chronic rhinitis and atopic dermatitis (AD).¹¹ Allergies are the greatest contributor to the disability-adjusted life years (DALYs) of skin diseases.¹² The regional burden of disease due to allergies varies depending on the type and severity of allergic diseases, as well as the availability and accessibility of health care services. The World Bank regions with the highest age-standardized DALYs for both sexes due to AD in 2019 are shown in Figure 1. In the United States, about 26% of adults and 20% of children have diagnosed allergic conditions with similar rates in Europe.¹³ The costs of allergic diseases is in the billions and includes medical care as well as lost productivity and reduced quality of life.¹⁴ Allergic diseases can also impair the physical, psychological, and social well-being of affected individuals and their families.¹⁵ Reduced sleep quality and daytime functioning due to nasal congestion, coughing, or itching; increased anxiety and depression due to fear of exposure to allergens or anaphylaxis; and increased school absenteeism and lower academic performance due to asthma or allergic rhinitis are just some examples.¹⁶

Figure 1 –

Disability-adjusted life years for atopic dermatitis for both sexes, age-standardized across World Bank regions. Source: IHME; permalink: http://ihmeuw.org/63eq.

Climate Change, Exposome Change, and Allergy

Impacts on temperature, humidity, air pollution, pollen, and allergy

Human activities have caused the global average annual temperature to rise by nearly 2 degrees Fahrenheit (1.1 degrees Celsius) since pre-Industrial times.¹⁷ These impacts are uneven with many regions warming faster than others. It is noteworthy that CC is not evenly distributed globally and may actually cause colder extended winter seasons in some parts of the world. This adds complexity to CC research as low and high ambient temperatures have been both associated with increased cardiorespiratory hospitalization in previous studies.^{18, 19}

With CC, atmospheric pressure and circulation patterns change, leading to more frequent extreme weather events. Melting ice sheets, rising sea levels, more frequent and intense heat waves, droughts, wildfires, storms, and floods are becoming more commonplace. These events can have serious consequences for human and natural systems.

CC is not only affecting global temperature, but also the amount of water vapor in the air. This has significant impacts on both the frequency and intensity of extreme weather events, such as heavy rainfall and heatwaves. According to Williams et al. (2018), specific humidity has increased over both land and ocean as the air has warmed. However, relative humidity has decreased over land as it has warmed faster than the ocean.²⁰ This means that the air over land is relatively drier over time even though the capacity to hold water vapor has increased. This creates a humidity paradox that affects the Earth’s water cycle and the energy balance explaining why some geographic areas have higher rainfall while others experience drought. Higher specific humidity can lead to heavier rainfall events and more flooding, as more water vapor is available to condense and precipitate. Higher specific humidity combined with higher temperatures can cause heat stress, a condition that reduces the ability of the body to cool down by sweating and can be fatal in some cases.²¹

While air pollution is a major cause of CC, the effects are bidirectional with CC also increasing air pollution levels across the world. This is because CC alters weather patterns that affect the dispersion of pollutants in the atmosphere. Moreover, CC can increase the frequency and intensity of wildfires, dust storms and other events that produce large amounts of smoke and particulate matter.²² Short and long-term exposure to air pollution has been associated with higher mortality and morbidity consistently across the world.^23–27 Higher temperatures increase the formation of ground-level ozone, which can cause respiratory problems and damage crops.²⁸ Previous researchers have investigated what is known as the “climate penalty” for air pollution, defined as the additional increases in air pollution relative to trends assuming constant weather conditions.²⁹ This climate penalty in the United States has led to increases in ozone associated with an additional 290 (95% CI: 80, 510) premature mortalities annually.²⁹ For fine particulate matter ≤ 2.5 μm (PM_2.5) it was linked to 770 (95% CI: 190, 1350) excess annual deaths.²⁹ Numerous studies have also documented substantial impacts of wildfire smoke, which is expected to increase due to CC,³⁰ on a spectrum of health outcomes, such as exacerbations of asthma and chronic obstructive pulmonary disease, and respiratory infections.^{25, 31, 32}

CC, rising carbon dioxide (CO₂) concentrations, and increased temperature have significant impacts on pollen production and distribution.^{33, 34} Higher temperatures cause plants to produce more pollen and release it earlier in its particular season.³⁵ This extends the duration and intensity of pollen exposure for people who suffer from allergies and asthma.³⁶ Additionally, higher temperatures increase the amount of ozone and other pollutants in the air, which worsen the effects of pollen on respiratory health.³⁷ CC also affect the geographic range and the diversity of pollen sources, potentially exposing people to new allergens that they are not accustomed to.³⁸

The impact of CC on the external exposome and its impact on allergy is complex and affects geographic location and vulnerable populations differently.³⁹ Altered outdoor and indoor exposome, such as temperature, humidity, air pollution etc. affect allergies (e.g., respiratory or skin allergies) in many ways. As explained above, higher temperatures along with rising CO₂ extend the pollen season and increase the amount of pollen produced by plants, especially ragweed, which is one of the main triggers of fall allergies.³⁸ These exposures impact allergic individuals disproportionately and trigger more frequent reactions.⁴⁰ Higher temperature and humidity further create favorable conditions for the growth of mold and dust mites, which are common indoor allergens.⁴¹ This may increase the exposure and sensitivity of allergic individuals to these allergens, and trigger allergic reactions.^{9, 42} Another potential effect of CC is triggering or exacerbation of temperature based urticaria, a type of allergic reaction that occurs when the skin is exposed to cold or hot temperatures in sensitive individuals. Cold or hot urticaria causes itching, swelling, redness and hives on the skin, and, while rare, in severe cases, anaphylaxis.⁴³ Higher temperatures can increase the production of pro-inflammatory cytokines and reactive oxygen species (ROS), which damage cells and tissues.⁴⁴

Higher temperatures as discussed above may further increase the levels of some air pollutants, such as ozone and particulate matter, which irritate the respiratory system, breaking down defensive barriers and making individuals more sensitive to allergens and allergic symptoms.⁴⁵ Air pollution is an important risk factor for atopic dermatitis.⁴⁶ Possible mechanisms for this association include increased water loss, physicochemical injury, effects on skin microflora, and damage to the skin barrier through oxidative stress. Importantly, immune dysregulation can be triggered by oxidative stress, causing increased sensitization to allergens.⁴⁶ Short-term exposure to air pollution has been associated with psoriasis flare.⁴⁷ Long-term exposure to air pollution has also been associated with increased prevalence of psoriasis and eczema in the United States, with a magnitude comparable to the risk associated with smoking.⁴⁸ Increased air pollution and pollen under CC and complex interactions with other allergens could trigger inflammatory responses and oxidative stress leading to aggravated allergies and higher burden of allergic disease worldwide.⁴⁹

Prior research has shown that air pollution can impair vitamin D production directly by blocking ultraviolet B photons (e.g., under smoke or dust pollution) or indirectly by decreasing outdoor activity and less exposure to ambient ultraviolet radiation.⁵⁰ Atopic dermatitis, asthma, and respiratory infection have been associated with vitamin D deficiency across several studies.⁵¹

Impacts on electromagnetic field radiation

Electromagnetic field (EMFs) radiation arises from electrical devices and power lines, and can affect living organisms. Under changing climate, the demand for electricity and the use of electrical devices, especially for cooling and heating purposes will be increased and may increase population level EMF exposure. CC may also alter natural background EMF levels via changes in atmospheric and geomagnetic conditions, such as solar storms and lightning activity. The EMF exposure can cause changes in cell function, gene expression, hormone levels, and disturbance of the immune system.⁵² Most interestingly, EMF radiation may also trigger a condition called electromagnetic hypersensitivity or electrohypersensitivity (EHS), which is a perceived sensitivity to EMFs emitted by various sources such as power lines, cell phones, computers, and microwaves.⁵³ Symptoms of EHS include nausea, vomiting, diarrhea, headache, fever, dizziness, disorientation, weakness, fatigue, hair loss, and bloody vomit and stools from internal bleeding.⁵⁴ Anyhow, whether EHS is caused by EMFs or that it is a true allergic reaction is still an area of investigation.

Impacts on chemical exposure

CC may indirectly increase exposure to chemicals that could harm our bodies and ecosystems. For example, floods may cause chemicals stored in landfills, tanks, or debris to leak or spread to new areas.⁵⁵ The melting of permafrost in Alaska may release chemicals that were previously frozen and volatile chemicals such as mercury will carry to different geographic areas based on temperature.⁵⁶ CC is able to impact internal hormones by altering the natural or human-made chemicals that interact with the endocrine system, called endocrine-disrupting chemicals (EDCs).⁵⁷ EDCs have been found in many products, such as plastics, pesticides, cosmetics, and pharmaceuticals, and can contaminate water, air, and soil.⁵⁸ Some examples of EDCs are atrazine, bisphenol A (BPA), and phthalates.⁵⁹ The EDCs mimic, block, or interfere with the body’s hormones and cause various health problems.⁶⁰ As an example, CC can increase the population exposure to the herbicide atrazine where higher temperatures increase the volatility and evaporation of atrazine from soil and water surfaces, leading to greater atmospheric deposition. Increased rainfall and flooding also can increase the runoff of atrazine from agricultural fields into surface water and groundwater.⁶¹ These scenarios can result in higher levels of atrazine in humans. Atrazine can affect the immune system by altering the production of cytokines, chemokines, and immunoglobulins, and modulating the function of macrophages, T cells, and B cells, affecting a range of allergies.⁶²

As another example, CC can make people more exposed to BPA. Higher temperatures can make BPA leach out of plastic products into food or water, and more rain and flooding can make BPA wash away from landfills into surface water. These situations again can lead to higher levels of BPA in humans. BPA may trigger systemic para-inflammation in epithelial tissues, such as the skin, gut, and lung.⁶³ Para-inflammation is a low-grade chronic inflammatory state that is normally protective against stress or injury, but can become maladaptive if prolonged or excessive.⁶⁴ Para-inflammation can impair the epithelial barrier function and increase the permeability to allergens and pathogens.⁶⁵ It can also activate innate immune cells and induce the production of pro-inflammatory cytokines, such as IL-6 and TNF-α, which can promote allergic inflammation.⁶⁶

Plastics are ubiquitous and exacerbated degradation of discarded plastics yields nanoplastic particles that are incorporated into microorganisms under different temperature levels in a dose-dependent manner.⁶⁷ Emission of micro/nanoplastics along with different chemicals during wildfires and burning of plastic material is an underappreciated impact of climate change as they can induce an immune response leading to cellular toxicity, and genotoxicity. ⁶⁸ CC induced increased temperature may result in increased release of chemicals from plastics, increasing the risk of exposure.⁶⁹ Some of these chemicals, such as phthalates, interfere with the endocrine system and may cause allergic reactions.⁷⁰ Phthalates are used to make plastics soft and flexible, but they leach out of the plastic and attach to dust particles that can be inhaled or ingested.⁷¹ Children exposed to high levels of phthalates in household dust have been shown to be more likely to have asthma, eczema, and rhinitis than children exposed to low levels in previous studies.⁷² Some studies suggest that phthalates may potentiate the immune response to other allergens.⁷³ Besides phthalates, other chemicals from plastics may also have adverse effects on the respiratory system, allergic airway inflammation, and the skin.⁷⁴ Overall, EDCs may interact with temperature and other environmental factors and can cause synergistic or antagonistic effects on immune systems.⁷⁵

Impacts on socioeconomic status

CC is intertwined with socioeconomic status (SES) in that poorer, minoritized populations are more impacted and its effects are a serious threat to socioeconomic stability, impacting the business community, and creating environmental injustice. Unfortunately, CC affects different regions and groups unevenly contributing to economic inequality between and within countries.⁷⁶ Across the globe, wealthy countries in colder regions may benefit long term from warmer temperatures, while poor countries in hotter regions may have suffered from reduced agricultural productivity, water scarcity, and health risks.⁷⁷ However, given the interconnectedness of the global economy adverse impacts will be experienced by all countries. The effects of redlining in the United States, segregation and lack of resources in poorer communities will likely disproportionately limit access to potentially lifesaving resources, such as air conditioning during heat waves. The poorest and most marginalized people are often the most vulnerable to climate impacts, yet they have the least responsibility for causing them and fewer resources to address CC.⁷⁸

SES as a measure of one’s access to economic and social resources, such as income, education, and health care, can greatly influence the risk of developing allergies.⁷⁹ Low SES does not directly cause any disease, but is a correlate of factors that predict poorer health, such as access to healthcare, heat/air conditioning, local pollution levels and access to healthy foods. Because low SES is associated with greater exposure to environmental pollutants, poor housing conditions, lack of preventive health care, and limited access to healthy foods as well as with climate change effects, the impacts of allergic diseases are disproportionately borne by low SES communities.⁸⁰

Impacts on gut microbiota

CC can further affect gut microbiota, which is increasingly found to be associated with immune function.⁸¹ Rising temperatures may alter the composition and diversity of microbial communities in the gut, leading to changes in metabolic functions and immune responses.⁸² Additionally, CC could increase the exposure to environmental toxins that are released by pathogens.⁸³ Excessive antibiotic use can disrupt the balance of gut microbiota altering risk of disease associated with the gut microbiome.⁸³ Rising temperatures increase the spread of infectious diseases by expanding the range of disease vectors, such as mosquitoes and ticks, which increase the demand for antibiotics.⁸⁴ CC can also affect the behavior and distribution of animals that carry zoonotic diseases, such as rabies and anthrax, which again may require antibiotic or anti-viral treatment.⁸⁵ CC may increase the contamination of water and soil by antibiotic residues from human and animal waste that may pose a risk for environmental and human health. Antibiotic residues can disrupt the balance of microbes in the environment and in the body, which may affect the immune system’s ability to respond to allergens and infections.⁸⁶

Impacts on vulnerable populations

CC and EC will influence sub-groups of populations differently across the world with the elderly, children, pregnant women, and low income communities facing higher risks for adverse health effects.⁸⁷ This is due to a combination of factors, such as their location, occupation, SES, education level, race and ethnicity, and age. These groups may have higher rates of existing medical conditions, such as asthma, diabetes, hypertension, and chronic obstructive pulmonary disease, that can be exacerbated by CC and EC impacts. A study in Sweden by Schyllert et al. (2020) reported an interaction between income and sex in which women with low income had an increased risk for allergic asthma.⁸⁸ It is important to note that such results may not be generalizable to other populations and further studies are needed.

Strategies to mitigate the adverse consequences of exposome change due to climate change

Unfortunately, CC will not be alleviated in the short term, and to cope with these impacts, individuals and populations need to take action to protect themselves from exposome change by reducing their exposure to environmental triggers, enhancing their resilience through lifestyle modifications, and seeking timely medical attention when needed. Individuals with resources should adapt their lifestyle by adopting behaviors to reduce the impact of CC (e.g. air conditioning, use of apps that predict weather and air pollution, etc.) in conjunctions with more sustainable practices, such as using renewable energy sources, public transport, and reduced fossil fuel use (e.g. flying less). Most importantly, policy makers must consider the needs of vulnerable populations to create programs to help them mitigate the risks of heat waves and other weather disasters that are specific to their communities as the impacts of CC are highly variable geographically. This need is urgent. Populations also may need to reduce their waste and emissions, promote green spaces and urban planning, and enhance disaster preparedness. Such activities will increase resilience and support local communities and vulnerable sub-groups of the population.

Summary

As explained above, climate change is part of the exposome and has both direct and indirect effects on environmental exposures and human health. Through a number of interconnected pathways, CC can have significant effects on onset of allergies and may pose a challenge for allergic individuals by exacerbation of their existing allergies, and for health care providers. Exposome change can have serious impacts on vulnerable populations, such as the elderly, children, or pregnant women, who may have weaker immune systems, higher sensitivity, or lower access to resources. Individuals and populations need to take action to protect themselves from exposome change, such as by reducing their exposure, enhancing their resilience, or advocating for policies that mitigate environmental hazards.

Synopsis:

Climate change is a major threat to human respiratory health and associated allergic disorders given broad impact on the exposome. Climate change can affect exposure to allergens, such as pollen, dust mites, molds, as well as other factors such as temperature, air pollution, and nutritional factors, which synergistically impact the immune response to these allergens. Exposome change can differentially exacerbate allergic reactions across sub-groups of populations, especially those who are more vulnerable to environmental stressors. Understanding links between climate change and health impacts can help inform how to protect individuals and vulnerable populations from adverse health effects.

Key Points.

• Climate change impacts a host of environmental influences on respiratory health and related allergic disorders

• Vulnerable populations (elderly, children, or pregnant women), especially of low socioeconomic status, will be disproportionately impacted by climate-related environmental shifts

• Our understanding of the broad impact of climate change on disease risk will be advanced through emerging technologies and data science advancements using an exposome framework.

Clinics Care Points.

• A comprehensive assessment of the patient’s exposome history, including personal, occupational, and environmental factors, can help identify potential triggers and risk factors for allergic diseases

• A personalized approach to allergy management, taking into account the patient’s exposome profile, genetic predisposition, comorbidities, and preferences, can improve outcomes and quality of life