SUPPLEMENT

Climate Change and Respiratory Health Daniel A. Gerardi, MD, FCCP and Roy A. Kellerman, MD

Objective: To discuss the nature of climate change and both its immediate and long-term effects on human respiratory health. Methods: This review is based on information from a presentation of the American College of Chest Physicians course on Occupational and Environmental Lung Disease held in Toronto, Canada, June 2013. It is supplemented by a PubMed search for climate change, global warming, respiratory tract diseases, and respiratory health. It is also supplemented by a search of Web sites including the Environmental Protection Agency, National Oceanic and Atmospheric Administration, World Meteorological Association, National Snow and Ice Data Center, Carbon Dioxide Information Analysis Center, Inter-Governmental Panel on Climate Change, and the World Health Organization. Results: Health effects of climate change include an increase in the prevalence of certain respiratory diseases, exacerbations of chronic lung disease, premature mortality, allergic responses, and declines in lung function. Conclusions: Climate change, mediated by greenhouse gases, causes adverse health effects to the most vulnerable patient populations—the elderly, children, and those in distressed socioeconomic strata.

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ar beyond increasing global average surface temperature (ie, global warming), climate change reflects an alteration in the earth’s climate system—atmosphere, land surface, oceans, and cryosphere. Climate change is distinguished from weather events in that it reflects an alteration in the “mean” weather, beyond seasonal and regional variation. It is best perceived when global conditions over decades and centuries are analyzed and compared.1 Much of the current knowledge of these effects of climate change has been reviewed in statements by the Inter-Governmental Panel on Climate Change. This international body of volunteer scientists, beginning with its first publication in 1990, has formed thoroughly researched conclusions with ever-increasing certainty, such that it is “extremely likely” that human influences are the source of the “unequivocal” warming of the earth’s climate system.2,3 The current and anticipated manifestations of climate change are reflected in atmospheric temperature increases, warming and acidification of oceans, reductions in the breadth of the cryosphere, and changes in the timing, pattern, and amount of precipitation. Each of these events is intertwined to produce myriad health effects.

WHAT DRIVES CLIMATE CHANGE? The driving force behind climate change is anthropogenic greenhouse gases (GHG), especially carbon dioxide (CO2 ). Other gases include methane, nitrous oxide, tropospheric ozone (O3 ), chlorofluorocarbons, carbon monoxide, and simple water vapor. Anthropogenic greenhouse gases absorb infrared radiation from the earth’s surface, thereby trapping heat in the lower atmosphere (Fig. 1). They come from various sources of combustion, agriculture, and pollution, From the Occupational Lung Disease (Dr Gerardi), Saint Francis Hospital and Medical Center, Hartford, and University of Connecticut School of Medicine, Farmington, Conn; and Department of Internal Medicine (Dr Kellerman), University of Connecticut School of Medicine, Farmington, Conn. The authors declare no conflicts of interest. Address correspondence to: Daniel A. Gerardi, MD, FCCP, Occupational Lung Disease, Saint Francis Hospital and Medical Center, 114 Woodland St, Hartford, CT 06105 ([email protected]). C 2014 by American College of Occupational and Environmental Copyright  Medicine DOI: 10.1097/JOM.0000000000000292

each having its own potential warming effect (usually compared with that of CO2 ) and atmospheric half-life. Water vapor, an intriguing and poorly understood GHG, forms its own positive feedback loop with a warming atmosphere able to absorb increasing amounts of water. This, in turn, absorbs more thermal energy, although clouds paradoxically reflect incoming solar radiation.4 The relative historic contribution of these gases to the radiative force of energy retention is demonstrated in Fig. 2. CO2 , the by-product of industrialization and combustion, is the most important GHG. Global CO2 production has increased on an unprecedented scale, with emissions being 61% higher than in 1990, peaking at 36 billion metric tons in 2013.5 Atmospheric CO2 has been accurately monitored since 1958 at the Mauna Loa Observatory in Hawaii, initially under the direction of C. David Keeling, with a curve that now bears his name (Fig. 3).6 This curve shows it is now over 400 ppm, and this correlates predictably with fossil fuel emissions measured both atmospherically and via ice-core data.4 Atmospheric CO2 is buffered by the world’s great oceans and the terrestrial carbon sink, documented in a complex carbon cycle (Fig. 4). This system is now overloaded such that atmospheric concentrations of long-lived CO2 are inevitable.

WHAT ARE THE ENVIRONMENTAL CONSEQUENCES OF CLIMATE CHANGE? The environmental consequences of climate change are broad, profound, and deserving of a separate volume of discussion. By necessity, this review is brief. For future information, the American Meteorological Society summary of 2013 contains much valuable information in this regard.7 The earth’s surface temperature, increasing at an average annual rate of 0.06◦ C per decade since 1880, receives much attention.8 Recently, 2010 became the warmest year on record. The fourth warmest year on record, 2013, marks the 37th year that the annual temperature has been above the long-term average.8 Also, the uneven, horizontal distribution of this warming, affecting land area in more northern latitudes, is convincing evidence that these changes are from a forced climate.9 Arctic Sea Ice, declining in age and thickness (2.4% per decade), is a sensitive indicator of climate change because it is surrounded by land and therefore affected by its climate. Another ice mass, the Greenland Ice Sheet had its entire surface melting at one point during the summer season of 2012, which is an unprecedented event.10 In addition, Antarctica, holder of the world’s largest ice sheet with 60% of the earth’s freshwater in frozen state, has shown rapid decline in volume, most recently to its western Thwaites Glacier.11 Oceans are warming as well as land masses. The melting of ice with warmed and expanded oceans results not only in changes to salinity, but with higher sea levels, averaging one-eighth inch per year.12 Over decades this increase has had great significance to coastal areas—damaging infrastructure, affecting sanitation and food supplies, and destroying shelter and farmland in low-lying communities.1 Furthermore, oceans absorb CO2 in a conversion to carbonic acid. The resultant warming and acidification of the sea not only disrupts ocean life by impeding calcification and growth of varied marine life, but induces the loss of important coral reef barriers, leading to important disruptions in food production, storm protection, and groundwater supply.13

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FIGURE 1. Main drivers of climate change.

FIGURE 2. Radiative forcing estimates in 2011 relative to 1750. S50

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JOEM r Volume 56, Number 10S, October 2014

Finally, an increase in extreme weather events such as super typhoons and wildfires is being seen. Hurricane Sandy, with its resultant acute health effects, loss of valuable research materials, and damage to infrastructure, highlights the vulnerability of even the most developed cities.14 The paradox of both increased drought and floods, among other weather variables, indicates that we will continue to see more variable, intense, frequent, and unstable weather patterns.15

WHAT ARE THE IMPORTANT NONRESPIRATORY EFFECTS OF CLIMATE CHANGE TO HUMAN HEALTH? The nonrespiratory effects of climate change are broad and also deserving of their own volume of information. These effects include vector-borne diseases, waterborne diseases, food-borne

FIGURE 3. Keeling curve.

Climate Change and Respiratory Health

illness and malnutrition, neurologic disorders, mental health and stress disorders, storm-related morbidity and mortality, and even malignancy.16 Vector-borne infectious diseases represent a pointed adverse health effect of climate change. These illnesses include Lyme disease, plague, tularemia, West Nile fever, leishmaniasis, malaria, and dengue fever.17 Warmer temperatures and wider weather fluctuations spread disease and affect the timing and intensity of disease outbreaks.18 For example, the tick vector for Lyme disease in North America, Ixodes scapularis, has been shown to be expanding its range into Canada at approximately 46 km/yr, with the most important determinant of such migration to be warming temperatures.19 This has also been seen in Sweden with the described northern migration of Ixodes ricinus related to their milder winters.20 Mosquitoes, which can carry many diseases, are particularly sensitive to climate changes. A warming environment promotes their rate of reproduction, increases their frequency of blood meals, and prolongs their breeding season.21 Already 40% of the world’s population lives in areas with malaria, with children being most likely to succumb.22 Biological models suggest that its transmission season will dramatically increase, placing even larger populations at risk.23 Models for the distribution of another mosquito-borne disease, dengue fever, are similarly both extensive and alarming.24,25 Water-related diseases offer additional infection risks, especially to locations in Africa and the Middle East.15 Diarrheal illnesses, including cholera, are promoted in warm water and algae blooms, or in flood.26 Drought also increases the risk from poor hygiene that results from the combined use (bathing and irrigation) of fresh water.15 Other less direct risks of climate change affect health, usually in the poorest populations. Food supplies are affected by drought and extreme weather conditions. Crops yields are reduced, livestock become weak and fewer, and fishing yields are diminished; yet their cost is elevated by the limited supply.27,28 The resultant food

FIGURE 4. Carbon cycle for the 1990s.  C 2014 American College of Occupational and Environmental Medicine

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insecurity increases the vulnerability to illness of an at-risk population. Anxiety and depression can also ensue because of illness, economic loss, overcrowding, or displacement.15

WHAT IS THE IMPACT OF CLIMATE CHANGE ON RESPIRATORY HEALTH? Climate change is having a specifically impactful change on respiratory health through a complex interaction of weather, allergens, and pollutants. This influences respiratory health through the occurrence of respiratory illness, exacerbations of chronic respiratory diseases, premature mortality, allergic responses, declines in lung function, and lung cancer.29 Sudden increases in temperature and humidity are linked to increased emergency department (ED) visits for patients suffering from chronic respiratory disease. Thermosensitive bronchopulmonary cfibers, which are activated from increased temperatures and stimulate reflex bronchoconstriction, are a possible mechanism. The University of Kentucky demonstrated a 112% increase in airway resistance after hyperventilation of warmed humid air verses an increase of 38% after hyperventilation of simple room air. This increase in airway resistance represented bronchoconstriction, whose persistence can progress to chronic obstructive pulmonary disease (COPD) exacerbation, resulting in increased ED visits and hospitalizations.30 Whatever the mechanism, cardiovascular and respiratory morbidity and mortality from dehydration, organ damage, fatigue, and riskprone behavior ensues. Recall the deaths and hospitalizations in Chicago in 1995 and in Western Europe in 2003. Strikingly, persons in cooler climates, perhaps less prepared to tolerate temperature extremes, exhibit more heat-related deaths.1 In these areas, the most vulnerable populations include the elderly, those with chronic heart and lung disease, children, pregnant women, and those in health care facilities.31,32 With the observed trends of climate change and global warming, heat waves and their resultant morbidity and mortality will become increasingly frequent and of greater duration and intensity.33 Much more than warming of air temperature, increases in GHG create air quality conditions that further trigger exacerbations of chronic lung disease. Ozone, in particular, produced when oxides react with other volatile organic compounds in the presence of ultraviolet radiation and heat, has been shown to facilitate inflammatory changes in the respiratory epithelium.34 Ground-level ozone concentration is increased by exhaust emissions from automobiles and fossil fuel-burning power plants, and is thereby found at higher concentrations in most urban areas. Although there has been some reduction in air pollution achieved by developed countries, further attempts to reduce ozone formation may prove difficult in the setting of global warming because of the competing effect of increased temperature on the reaction leading to its formation.1 A number of epidemiologic studies have shown that asthmatic patients are the most affected by increases in ground-level ozone.35 For example, a study completed in San Francisco measured the response of 81 asthmatic patients to exposure ambient levels of O3 (0.2 ppm) with intermittent exercise in three phases. Inflammatory effects of the exposure were measured directly or indirectly in several ways, including pulmonary function testing, bronchoscopy, bronchoalveolar lavage, and bronchial biopsy. Although the study did not demonstrate a significant increase in lower respiratory symptoms or lung function response secondary to O3 exposure, it did show an enhanced O3 -induced inflammatory response, with elevations in the percentage of neutrophils and total protein concentrations in bronchoalveolar lavage in asthmatic versus nonasthmatic patients.36 The Center for Environmental Medicine, Asthma, and Lung Biology at the University of North Carolina also evaluated the mechanism of this increased inflammatory response in asthmatic patients. Their study confirmed that near-ambient levels of ozone caused pulmonary inflammation in healthy adults, evidenced by significant increases in S52

airway neutrophils and inflammatory cytokines. In addition, they demonstrated that O3 exposure caused an influx of dendritic cells and monocytes that express higher levels of CD14, CD80, CD86, and HLA-DR compared with samples collected at baseline. This result suggests that O3 exposure not only results in the recruitment of granulocytes to the airway, but also results in an influx of immunemodulatory cells with modified cell surface phenotypes with a bias toward antigen presentation.37 The sum effect is to increase bronchial responsiveness and exacerbate disease in susceptible populations, directly leading to increased ED visits, hospitalizations, and health care costs. Of even greater concern is the effect of increased ozone pollution on mortality. In a complex analysis of models of climate change and emissions, Orru and colleagues38 not only demonstrated a 5% increase in hospitalization or mortality in Europe over the last 20 years attributable to ozone exposure, but projected striking future adverse outcomes. In addition, in a study of 96 US metropolitan areas over 18 years (using an American Cancer Society cohort), Jerrett and colleagues39 revealed that for every 10-ppb increase in exposure to ozone there was a corresponding increase in respiratory deaths of about 2.9%, this increasing to 4.0% using a two-pollutant (PM 2.5) model. Air pollution from particulate matter (PM) is also of concern for exacerbation of asthma and COPD as well as increased cardiopulmonary morbidity. Particulate matters are dangerous because they are of respirable size and their size to weight ratio allows them to carry adsorbed toxic compounds deep into the lung. Although desertification and droughts are accountable for much of PM, massive PM releases into the atmosphere can occur as a result of forest fires. A change in climate creates settings conducive to fires, generating a wide array of pollutants, in addition to PM, organic compounds (acrolein), gases, and carcinogens (benzene and formaldehyde).40 Although the fires themselves are of relatively short duration, their plumes can extend over a great distance and last for a long time, affecting a potentially vast population. Increases in mortality, hospitalizations, ED visits, exacerbations of asthma and COPD, and respiratory symptoms associated with declines in lung function in healthy persons have been shown in a number of studies.41–43 Much of this assessment is from US data, as in review of the Peat Bog Wildfire in rural North Carolina in 2008. In this analysis, Rappold showed increases in the relative risk of exacerbation of asthma (1.65 [95% confidence interval, 1.25 to 2.1]), COPD (1.73 [1.06 to 2.83]), and pneumonia and acute bronchitis (1.59 [1.07 to 2.34]) in this toxic setting. ED visits associated with cardiopulmonary symptoms

TABLE 1. Mitigation and Adaptation Mitigation strategies Reduced energy demand Reduction of fossil fuel emissions Improved energy efficiency Improved energy transportation Reduction of wood and biomass burning Increased public transportation Reduction in meat consumption Reforestation Carbon capture Adaptation strategies Added warning systems for extreme weather events Increased crop diversity Improving disease surveillance and vaccinations Protecting and harvesting clean water

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(1.23 [1.06 to 1.43]) and heart failure (1.37 [1.01 to 1.85]) were also significantly increased.44 The interaction of ozone, temperature, and air pollution produces a “perfect storm” of increased inflammation and aggravation of symptoms and physiologic dysfunction to patients suffering from chronic lung disease. This effect is likely often underestimated, as results differ for each pollutant studied and its study area. Increased ventilation and lung volumes in heat, increased time spent out of doors, and increased airway permeability from pollutants, increase the exposure and absorption of allergens and pollutants, amplifying their toxic effect.29 This synergy increases excess overall mortality and respiratory-related admissions.29,45 Ozone increases inflammation of bronchial epithelium as well as airway hyperresponsiveness through its direct impact on inflammatory cell recruitment and its ability to potentiate the effects of other pollutants.1 A warming world alters the growing season and geography of various pollen-producing plants, lengthening their season and increasing the potential for sensitization to aeroallergens. Increases in air-borne allergens increase asthma exacerbations and hospital visits and the burden of allergic rhinitis.46 The common allergen ragweed is known to grow 10% taller and produce 40% to 60% more pollen in experimental models that double of the concentration of ambient CO2 .47 In urban areas, where there is increased average temperature and CO2 exposure, ragweed is found to grow faster, flower more quickly, and demonstrate greater above-ground biomass and pollen when compared with rural areas.48 Asthma incidence and prevalence has increased over recent decades alongside increasing atmospheric CO2 concentrations and average temperature. Exposure to allergens in early childhood is thought to sensitize individuals to atopic conditions such as asthma, allergic rhinitis, and eczema. Bjorksten and Suoniemi49 were able to demonstrate a link between exposures to pollen in the first 6 months of life, with increased chances of pollen allergy for up to 20 years postexposure, and that elimination of early childhood exposure potentially eliminated allergies by approximately 20% in the age group 0 to 19 years. Understanding the complexity of asthma causation and incidence, Beggs and colleagues have suggested that these allergic health effects may be an early indication of anthropogenic climate change, affecting not only asthma morbidity but also its prevalence.50

WHAT CAN BE DONE TO COMBAT THE HEALTH EFFECTS OF CLIMATE CHANGE? Mitigation and adaptation are components of a two-pronged approach toward combating this great issue of our time. Mitigation aims at reducing GHGs through reduced energy demand and increased conservation. Energy conservation through efficiency, mass transit, and carbon capture is the cornerstone of this approach, keeping in mind that the magnitude of any intervention is related to the energy source that is being substituted15 (Table 1). Alternative fuels, including solar, wind, geothermal, nuclear, and hydro, are required to be expanded and modernized to confront the energy demands of an enlarging world population.16 Adaptation to the health effects of climate change requires coordination of care and is especially important in lower-income countries.1 Greater attention is needed in disease surveillance and providing vaccinations to prevent the spread of illness. This is as critical as protecting clean water supplies, marine fisheries, and agricultural productivity. Overcoming the impetus to affect change in underdeveloped populations requires the dissemination of knowledge of climate events to promote a regional desire and ability to enact positive change.51 Finally, health care practitioners must assume a greater role in communicating the health effects of forced climate to the general public and individuals with the power to change policy.27 Thus, a collaborative effort of physicians, nurses, scientists, industry, and

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government (national and international) is needed to protect health, increase awareness of climate change, discover alternative energy resources, and fund research.52

ACKNOWLEDGMENTS We gratefully acknowledge assistance from Joseph Pallis, MLS, and Paula Bernardino.

REFERENCES 1. McMichael AJ, Lindgren E. Climate change: present and future risks to health, and necessary responses. J Intern Med. 2011;270:401–413. 2. Houghton JT, Jenkins GJ, Ephraums GJ. Report prepared for Intergovernmental Panel on Climate Change (IPCC) by Working Group I. Cambridge University Press; 1990. 3. IPCC, 2013: Summary for Policymakers. In:Stocker TF, Qin D, Plattner G-K, et al., eds. Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge, UK, and New York, NY: Cambridge University Press. 4. National Research Council. Advancing the Science of Climate Change. Washington, DC: The National Academies Press; 2010. 5. Le Quere C, Peters GP, Robert RJ, et al. Global carbon budget 2013. Earth Sys Sci Data. 2014;6:235–263. 6. Kennedy C. Carbon Dioxide: Earth’s Hottest Topic is Just Warming Up. NOAA Climate.gov. October 21, 2009. Available at http://www.climate.gov/news-features/understanding-climate/carbon-dioxideearths-hottest-topic-just-warming. Accessed July 22, 2014. 7. Blunden J, Arndt DS, eds. 2014: State of the Climate in 2013. Bull Amer Meteor Soc. 2014;95:S1–S257. 8. NOAA Climate.gov. 2013 State of the Climate: Earth’s Surface Temperature. July 12, 2014. Available at http://www.climate.gov/news-features/ understanding-climate/2013-state-climate-earth-surface-temperature. Accessed July 22, 2014. 9. Hansen J, Sato M, Ruedy R, Lo K, Lea DW, Medina-Elizade M. Global temperature change. Proc Nat Acad Sci USA. 2006;103:14288–14293. 10. NOAA Climate.gov. 2013 State of the Climate: Arctic Sea Ice. July 12, 2014. Available at http://www.climate.gov/news-features/understanding-climate/ 2013-state-climate-arctic-sea-ice. Accesses July 22, 2014. 11. Joaghin I, Smith B, Medley B. Marine ice sheet collapse under way for the Thwaites glacier basin, west Antarctica. Science. 2014;344:735–738. 12. NOAA Climate.gov. 2013 State of the Climate: Sea Level. July 12, 2014. Available at http://www.climate.gov/news-features/understanding-climate/ 2013-state-climate-sea-level. Accessed July 22, 2014. 13. NOAA. 2013 NOAA Coral Health and Monitoring Program. Available at http://www.coral.noaa.gov/research/climate-change/coral-bleaching.html. Accessed July 22, 2014. 14. Rom WN, Evans L, Uppal A. The sentinel event of climate change: hurricane sandy and its consequences for pulmonary and critical care medicine. Am J Respir Crti Care Med. 2013;187:iii–iv. 15. Haines A, Patz JA. Health effects of climate change. JAMA. 2004;291:99–103. 16. Portier CJ, Thigpen Tart K, Carter SR, et al. A Human Health Perspective on Climate Change: A Report Outlining the Research Needs on the Human Health Effects of Climate Change. Research Triangle Park, NC: Environmental Health Perspectives; 2010. doi:10.1289/ehp.1002272. Available at www.niehs.nih.gov/climatereport. 17. Mills J, Gage K, Khan A. Potential influence of climate change on vectorborne and zoonotic diseases: a review and proposed research plan. Environ Health Perspect. 2010;118:1507–1514. 18. McMichael AJ, Campbell-Lendrum DH, Corval´an CF, et al., eds. Climate Change and Human Health: Risks and Responses. Geneva: World Health Organization; 2003:250. 19. Leighton P, Kroft J, Pelcat Y, Lindsay LR, Ogden NH. Predicting the sped of tick invasion: an empirical model of range expansion for the Lyme disease vector Ixodes scapularis in Canada. J Appl Ecol. 2012;49:457–464. 20. Lindgren E, Talleklint L, Polfedt T. Impact of climate change of the northern latitude limit and population density of the disease-transmitting European tick Ixodes ricinus. Environ Health Perspect. 2000;108:119–123. 21. Epstein PR, Diaz HF, Elias S, et al. Biological and physical signs of climate change: focus on mosquito-borne diseases. Bull Am Meteorol Soc. 1998;78:409–417. 22. Greenwood B, Mutabingwa T. Malaria in 2002. Nature. 2002;415:670–672.

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23. Martens P, Kovats RS, Nijhof S, et al. Climate change and future populations at risk of malaria. Glob Environ Change. 1999;9:s89–s107. 24. Astrom C, Rocklov J, Hales S, B´eguin A, Louis V, Sauerborn R. Potential distribution of dengue fever under scenarios of climate change and economic development. Ecohealth. 2012;9:448–454. 25. Hales S, de Wet N, Woodward A. Potential effect of population and climate changes on global distribution of dengue fever: an empirical model. Lancet. 2002;360:830–833. 26. Rodo X, Pascual M, Fuchs G, Faruque AS. ENSO and cholera: a nonstationary link related to climate change? Proc Natl Acad Sci USA. 2002;99:12901– 12906. 27. McMichael T, Montgomery H, Costello A. Health risks, present and future, from global climate change. BMJ. 2012;344:e1359. 28. Teazono E. UN says food prices to remain high. Financial Times. 2011. 29. De Sario M, Katsouyanni K, Michelozzi P. Climate change, extreme weather events, air pollution and respiratory health. Eur Respir J. 2013;42: 826–843. 30. Hayes D Jr, Collins P, Khosravi M, Lin R-L, Lee L-Y. Bronchoconstriction triggered by breathing hot humid air in patients with asthma: role of cholinergic reflex. Am J Respir Crit Care Med. 2012;185:1190– 1196. 31. Staffogia M, Forasteire F, Aqostini D. Vulnerability to heat-related mortality: a multicity, population-based, case-crossover analysis. Epidemiology. 2006;17:315–323. 32. Balbus JM, Malina C. Identifying vulnerable subpopulations for climate change health effects in the United States. J Occup Environ Med. 2009;51: 33–37. 33. O’Neill MS, Ebi KL. Temperature extremes and health: impacts of climate variability and change in the United States. J Ocup Envir Med. 2009;51: 13–25. 34. Scannel C, Chen L, Aris R. Greater ozone-induced inflammatory responses in subjects with asthma. Am J Respir Crit Care Med. 1996;154:24–29. 35. Whittemore AS, Korn EL. Asthma and air pollution in the Los Angeles area. Am J Public Health. 1980;70:687–696. 36. Balmes J, Aris RM, Chen LL, et al. Effects of ozone on normal and potentially sensitive human subjects. Part I: airway inflammation and responsiveness to ozone in normal and asthmatic subjects. Res Resp Health Eff Inst. 1997;78: 1–37. 37. Alexis NE, Lay JC, Hazucha M, et al. Low-level ozone exposure induces airways inflammation and modifies cell surface phenotypes in healthy humans. Inhal Toxicol. 2010;22:593–600.

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38. Orru H, Andersson C, Ebi J, Langer J, Astr¨om C, Forsberg B. Impact of climate change on ozone-related mortality and morbidity in Europe. Eur Respir J. 2013;41:285–294. 39. Jerrett M, Burnett RT, Pope A III, et al. Long-term ozone exposure and mortality. N Engl J Med. 2009;360:1085–1095. 40. Bernstein A, Rice M. Lungs in a warming world climate change and respiratory health. Chest. 2013;143:1455–1459. 41. Finlay SE, Moffat A, Gazzard R, Baker D, Murray V. Health impacts of wildfires. PLoS Curr. 2012;4:e4f959951cce2c. doi:10.1371/4f959951cce2c. 42. Henderson SB, Brauer M, Macnab YC, Kennedy SM. Three measures of forest fire smoke exposure and their associations with respiratory and cardiovascular health outcomes in a population-based cohort. Environ Health Perspect. 2011;119:1266-1271. 43. Delfino RJ, Brummel S, Wu J, et al. The relationship of respiratory and cardiovascular hospital admissions to the southern California wildfires of 2003. Occup Environ Med. 2009;66:189-197. 44. Rappold AG, Stone SL, Cascio WE, et al. Peat Bog wildfire smoke exposure in rural North Carolina is associated with cardiopulmonary emergency department visits assessed through syndromic surveillance. Environ Health Perspect. 2011;119:1415–1420. 45. Katsouyanni K, Pantazopoulou A, Touloumi G, et al. Evidence for interaction between air pollution and high temperature in the causation of excess mortality. Arch Environ Health. 1993;48:235–242. 46. Barnes CS, Alexis NE, Bernstein JA, et al. Climate change and our environment: the effect on respiratory and allergic disease. J Allergy Clin Immunol Pract. 2012;1:137–141. 47. Wayne P, Foster S, Connolly J, Bazzaz F, Epstein P. Production of allergenic pollen by ragweed is increased in CO2 -enriched atmospheres. Ann Allergy Asthma Immunol. 2002;88:279–282. 48. Ziska LH, Gebhard DE, Frenz DA, Faulkner S, Singer BD, Straka JG. Cities as harbingers of climate change: common ragweed, urbanization, and public health. J Clin Immunol. 2003;111:290–295. 49. Bjorksten F, Suoniemi I. Time and intensity of first pollen contacts and risks of subsequent pollen allergies. Acta Med Scand. 1981;209:299–303. 50. Beggs PJ, Bambrick HJ. Is the global rise of asthma an early impact of anthropogenic climate change? Environ Health Perspect. 2005;113:915–919. 51. Mills DM. Climate change. Extreme weather events, and US health impacts: what can we say? J Occup Environ Med. 2009;51:26–32. 52. Pinkerton KE, Rom W, Akpinar-Elci M, et al. An official American Thoracic Society workshop report: climate change and human health. Proc Am Thorac Soc. 2012;9:3–8.

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Climate change and respiratory health.

To discuss the nature of climate change and both its immediate and long-term effects on human respiratory health...
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