Comprehensive Physiology Wiley Online Library

Respiratory Health Effects of Exposure to Ambient Particulate Matter and Bioaerosols

Full Article on Wiley Online Library



Abstract

Researchers have been studying the respiratory health effects of ambient air pollution for more than 70 years. While air pollution as a whole can include gaseous, solid, and liquid constituents, this article focuses only on the solid and liquid fractions, termed particulate matter (PM). Although PM may contain anthropogenic, geogenic, and/or biogenic fractions, in this article, particles that originate from microbial, fungal, animal, or plant sources are distinguished from PM as bioaerosols. Many advances have been made toward understanding which particle and exposure characteristics most influence deposition and clearance processes in the respiratory tract. These characteristics include particle size, shape, charge, and composition as well as the exposure concentration and dose rate. Exposure to particles has been directly associated with the exacerbation and, under certain circumstances, onset of respiratory disease. The circumstances of exposure leading to disease are dependent on stressors such as human activity level and changing particle composition in the environment. Historically, researchers assumed that bioaerosols were too large to be inhaled into the deep lung, and thus, not applicable for study in conjunction with PM2.5 (the 2.5‐μm and below size fraction that can reach the deep lung); however, this concept is beginning to be challenged. While there is extensive research on the health effects of PM and bioaerosols independent of each other, only limited work has been performed on their coexposure. Studying these two particle types as dual stressors to the respiratory system may aid in more thoroughly understanding the etiology of respiratory injury and disease. © 2020 American Physiological Society. Compr Physiol 10:1‐20, 2020.

Comprehensive Physiology offers downloadable PowerPoint presentations of figures for non-profit, educational use, provided the content is not modified and full credit is given to the author and publication.

Download a PowerPoint presentation of all images


Figure 1. Figure 1. Simplified schematic of the combined effects of climate, bioaerosols, and particulate matter acting as multiple stressors in the onset of respiratory disease.
Figure 2. Figure 2. Comparison of particle size fractions including particulate matter (PM), bioaerosols and reference particles. Adapted, with permission, from Kaiser J, 2005 66.
Figure 3. Figure 3. Probability of particle deposition in different regions of the respiratory tract. This graph is modeled after an adult exposed to spherical particles with a density of 1000 kg/m3, respiring during light exercise (25 L/min). Adapted, with permission, from Madl AK, et al., 2010 82.
Figure 4. Figure 4. Impaction, sedimentation, interception, diffusion, and electrostatic deposition are the main mechanisms of particle deposition. Impaction and sedimentation are dependent on the inertia of the particle size and shape, whereas diffusion is dependent on the properties of the aerosol and the trumpet effect of the alveolar space. Interception is dependent on an edge of a particle touching the tract surface and thus changing the final particle trajectory. Electrostatic deposition is dependent on particle charge. Adapted, with permission, from Madl AK, et al., 2010 82.
Figure 5. Figure 5. Clearance of particles from the tracheobronchial tree. Mechanisms include (i) sneezing, coughing, and transport of mucin to the nasopharyngeal region where it is swallowed; (ii) direct mucociliary transport of particles up the tracheobronchial tree and subsequent passage to the gastrointestinal tract; (iii) macrophage uptake and transport up the bronchiolar airways or across the alveolar epithelium and clearance through the pulmonary circulation or interstitial lymphatics; and (iv) physicochemical processes, including dissolution, leaching, and physical breakdown of particles. Courtesy of Dr. Patrick J. Haley, Nycomed R&D, Inc., Collegeville, PA, from an original drawing.
Figure 6. Figure 6. Mechanisms of reactive oxygen species (ROS) generation due to the intrinsic properties and cellular interactions of particulate matter (PM). PM containing transition metals, free radicals, or pieces of organic bioaerosols can generate ROS intrinsically. PM also interacts with cellular surface proteins and internal cellular components prior to and after phagocytosis. Adapted, with permission, from Madl AK, et al., 2014 83.
Figure 7. Figure 7. Mortality hazard ratio for PM‐related diseases. Abbreviations: LRI, lower respiratory infection; IHD, ischemic heart disease; COPD, chronic obstructive pulmonary disease. Adapted, with permission, from Burnett R, et al., 2018 18.


Figure 1. Simplified schematic of the combined effects of climate, bioaerosols, and particulate matter acting as multiple stressors in the onset of respiratory disease.


Figure 2. Comparison of particle size fractions including particulate matter (PM), bioaerosols and reference particles. Adapted, with permission, from Kaiser J, 2005 66.


Figure 3. Probability of particle deposition in different regions of the respiratory tract. This graph is modeled after an adult exposed to spherical particles with a density of 1000 kg/m3, respiring during light exercise (25 L/min). Adapted, with permission, from Madl AK, et al., 2010 82.


Figure 4. Impaction, sedimentation, interception, diffusion, and electrostatic deposition are the main mechanisms of particle deposition. Impaction and sedimentation are dependent on the inertia of the particle size and shape, whereas diffusion is dependent on the properties of the aerosol and the trumpet effect of the alveolar space. Interception is dependent on an edge of a particle touching the tract surface and thus changing the final particle trajectory. Electrostatic deposition is dependent on particle charge. Adapted, with permission, from Madl AK, et al., 2010 82.


Figure 5. Clearance of particles from the tracheobronchial tree. Mechanisms include (i) sneezing, coughing, and transport of mucin to the nasopharyngeal region where it is swallowed; (ii) direct mucociliary transport of particles up the tracheobronchial tree and subsequent passage to the gastrointestinal tract; (iii) macrophage uptake and transport up the bronchiolar airways or across the alveolar epithelium and clearance through the pulmonary circulation or interstitial lymphatics; and (iv) physicochemical processes, including dissolution, leaching, and physical breakdown of particles. Courtesy of Dr. Patrick J. Haley, Nycomed R&D, Inc., Collegeville, PA, from an original drawing.


Figure 6. Mechanisms of reactive oxygen species (ROS) generation due to the intrinsic properties and cellular interactions of particulate matter (PM). PM containing transition metals, free radicals, or pieces of organic bioaerosols can generate ROS intrinsically. PM also interacts with cellular surface proteins and internal cellular components prior to and after phagocytosis. Adapted, with permission, from Madl AK, et al., 2014 83.


Figure 7. Mortality hazard ratio for PM‐related diseases. Abbreviations: LRI, lower respiratory infection; IHD, ischemic heart disease; COPD, chronic obstructive pulmonary disease. Adapted, with permission, from Burnett R, et al., 2018 18.
References
 1.An Z, Jin Y, Li J, Li W, Wu W. Impact of particulate air pollution on cardiovascular health. Curr Allergy Asthma Rep 18: 15, 2018.
 2.Anderson JO, Thundiyil JG, Stolbach A. Clearing the air: A review of the effects of particulate matter air pollution on human health. J Med Toxicol 8: 166‐175, 2012.
 3.Araujo JA, Barajas B, Kleinman M, Wang X, Bennett BJ, Gong KW, Navab M, Harkema J, Sioutas C, Lusis AJ, Nel AE. Ambient particulate pollutants in the ultrafine range promote early atherosclerosis and systemic oxidative stress. Circ Res 102: 589‐596, 2008.
 4.Arbes SJ Jr, Gergen PJ, Elliott L, Zeldin DC. Prevalences of positive skin test responses to 10 common allergens in the US population: Results from the third National Health and Nutrition Examination Survey. J Allergy Clin Immunol 116: 377‐383, 2005.
 5.Aust AE, Cook PM, Dodson RF. Morphological and chemical mechanisms of elongated mineral particle toxicities. J Toxicol Environ Health B Crit Rev 14: 40‐75, 2011.
 6.Badirdast P, Rezazadeh Azari M, Salehpour S, Ghadjari A, Khodakarim S, Panahi D, Fadaei M, Rahimi A. The effect of wood aerosols and bioaerosols on the respiratory systems of wood manufacturing industry workers in Golestan Province. Tanaffos 16: 53‐59, 2017.
 7.Bahadur R, Russell LM, Prather K. Composition and morphology of individual combustion, biomass burning, and secondary organic particle types obtained using urban and coastal ATOFMS and STXM‐NEXAFS measurements. Aerosol Sci Tech 44: 551‐562, 2010.
 8.Baran S, Swietlik K, Teul I. Lung function: Occupational exposure to wood dust. Eur J Med Res 14 (Suppl 4): 14‐17, 2009.
 9.Bauer RN, Diaz‐Sanchez D, Jaspers I. Effects of air pollutants on innate immunity: The role of Toll‐like receptors and nucleotide‐binding oligomerization domain‐like receptors. J Allergy Clin Immunol 129: 14‐26, 2012.
 10.Bayram H. Impact of air pollution on COPD; underlying mechanisms. Tanaffos 16: S10‐S10, 2017.
 11.Bedard K, Krause KH. The NOX family of ROS‐generating NADPH oxidases: Physiology and pathophysiology. Physiol Rev 87: 245‐313, 2007.
 12.Blaisdell CJ, Weiss SR, Kimes DS, Levine ER, Myers M, Timmins S, Bollinger ME. Using seasonal variations in asthma hospitalizations in children to predict hospitalization frequency. J Asthma 39: 567‐575, 2002.
 13.Boueiz A, Hassoun PM. Regulation of endothelial barrier function by reactive oxygen and nitrogen species. Microvasc Res 77: 26‐34, 2009.
 14.Brook JR, Dann TF, Burnett RT. The relationship among TSP, PM10, PM2.5 and inorganic constituents of atmospheric particulate matter at multiple Canadian locations. J Air Waste Manage Assoc 47: 2‐19, 1997.
 15.Brook Robert D, Rajagopalan S, Pope CA, Brook Jeffrey R, Bhatnagar A, Diez‐Roux Ana V, Holguin F, Hong Y, Luepker Russell V, Mittleman Murray A, Peters A, Siscovick D, Smith Sidney C, Whitsel L, Kaufman JD. Particulate matter air pollution and cardiovascular disease. Circulation 121: 2331‐2378, 2010.
 16.Buckley A, Warren J, Hodgson A, Marczylo T, Ignatyev K, Guo C, Smith R. Slow lung clearance and limited translocation of four sizes of inhaled iridium nanoparticles. Part Fibre Toxicol 14: 5, 2017.
 17.Bunger J, Schappler‐Scheele B, Hilgers R, Hallier E. A 5‐year follow‐up study on respiratory disorders and lung function in workers exposed to organic dust from composting plants. Int Arch Occup Environ Health 80: 306‐312, 2007.
 18.Burnett R, Chen H, Szyszkowicz M, Fann N, Hubbell B, Pope CA, Apte JS, Brauer M, Cohen A, Weichenthal S, Coggins J, Di Q, Brunekreef B, Frostad J, Lim SS, Kan H, Walker KD, Thurston GD, Hayes RB, Lim CC, Turner MC, Jerrett M, Krewski D, Gapstur SM, Diver WR, Ostro B, Goldberg D, Crouse DL, Martin RV, Peters P, Pinault L, Tjepkema M, van Donkelaar A, Villeneuve PJ, Miller AB, Yin P, Zhou M, Wang L, NAH J, Marra M, Atkinson RW, Tsang H, Quoc Thach T, Cannon JB, Allen RT, Hart JE, Laden F, Cesaroni G, Forastiere F, Weinmayr G, Jaensch A, Nagel G, Concin H, Spadaro JV. Global estimates of mortality associated with long‐term exposure to outdoor fine particulate matter. Proc Natl Acad Sci 115: 9592‐9597, 2018.
 19.Burnett RT, Pope CA III, Ezzati M, Olives C, Lim SS, Mehta S, Shin HH, Singh G, Hubbell B, Brauer M, Anderson HR, Smith KR, Balmes JR, Bruce NG, Kan H, Laden F, Pruss‐Ustun A, Turner MC, Gapstur SM, Diver WR, Cohen A. An integrated risk function for estimating the global burden of disease attributable to ambient fine particulate matter exposure. Environ Health Perspect 122: 397‐403, 2014.
 20.Carnes MU, Hoppin JA, Metwali N, Wyss AB, Hankinson JL, O'Connell EL, Richards M, Long S, Freeman LEB, Sandler DP, Henneberger PK, Barker‐Cummings C, Umbach DM, Thorne PS, London SJ. House dust endotoxin levels are associated with adult asthma in a U.S. Farming Population. Ann Am Thorac Soc 14: 324‐331, 2017.
 21.Castañeda AR, Pinkerton KE. Investigating the effects of particulate matter on house dust mite and ovalbumin allergic airway inflammation in mice. Curr Protoc Toxicol 68: 18.18.11‐18.18.18, 2016.
 22.Castaneda AR, Vogel CFA, Bein KJ, Hughes HK, Smiley‐Jewell S, Pinkerton KE. Ambient particulate matter enhances the pulmonary allergic immune response to house dust mite in a BALB/c mouse model by augmenting Th2‐ and Th17‐immune responses. Physiol Rep 6: e13827, 2018.
 23.Chang M‐W, Lee C‐R, Hung H‐F, Teng K‐S, Huang H, Chuang C‐Y. Bioaerosols from a food waste composting plant affect human airway epithelial cell remodeling genes. Int J Environ Res Public Health 11: 337‐354, 2013.
 24.Charrier JG, Anastasio C. On dithiothreitol (DTT) as a measure of oxidative potential for ambient particles: Evidence for the importance of soluble transition metals. Atmos Chem Phys 12: 11317‐11350, 2012.
 25.Cherrie JW, Brosseau LM, Hay A, Donaldson K. Low‐toxicity dusts: Current exposure guidelines are not sufficiently protective. Ann Occup Hyg 57: 685‐691, 2013.
 26.Churg A, Brauer M. Human lung parenchyma retains PM2.5. Am J Respir Crit Care Med 155: 2109‐2111, 1997.
 27.Churg A, Brauer M, del Carmen A‐CM, Fortoul TI, Wright JL. Chronic exposure to high levels of particulate air pollution and small airway remodeling. Environ Health Perspect 111: 714‐718, 2003.
 28.Churg A, Brauer M, Vedal S, Stevens B. Ambient mineral particles in the small airways of the normal human lung. J Environ Med 1: 39‐45, 1999.
 29.Churg A, Wright JL. Bronchiolitis caused by occupational and ambient atmospheric particles. Semin Respir Crit Care Med 24: 577‐584, 2003.
 30.Churg AM, Green FHY. Occupational lung disease. In: Churg AM, Myers JL, Tazelaar HD, Wright JL, editors. Thurlbeck's Pathology of the Lung. New York: Thieme Medical Publishers, Inc., 2005, p. 769‐862.
 31.Clark NA, Demers PA, Karr CJ, Koehoorn M, Lencar C, Tamburic L, Brauer M. Effect of early life exposure to air pollution on development of childhood asthma. Environ Health Perspect 118: 284‐290, 2010.
 32.Coates SJ, Fox LP. Disseminated coccidioidomycosis as a harbinger of climate change. JAAD Case Rep 4: 424‐425, 2018.
 33.Dai J, Xie C, Vincent R, Churg A. Air pollution particles produce airway wall remodeling in rat tracheal explants. Am J Respir Cell Mol Biol 29: 352‐358, 2003.
 34.Davies LC, Rice CM, McVicar DW, Weiss JM. Diversity and environmental adaptation of phagocytic cell metabolism. J Leukoc Biol 105 (1): 37, 48, 2018.
 35.Deering‐Rice CE, Nguyen N, Lu Z, Cox JE, Shapiro D, Romero EG, Mitchell VK, Burrell KL, Veranth JM, Reilly CA. Activation of TRPV3 by wood smoke particles and roles in pneumotoxicity. Chem Res Toxicol 31: 291‐301, 2018.
 36.Despres VR, Huffman JA, Burrows SM, Hoose C, Safatov AS, Buryak G, Fröhlich‐Nowoisky J, Elbert W, Andreae MO, Pöschl U, Jaenicke R. Primary biological aerosol particles in the atmosphere: A review. Tellus/B 64: Art.Nr.:‐15598/15591, 2012.
 37.DeVries R, Kriebel D, Sama S. Low level air pollution and exacerbation of existing COPD: A case crossover analysis. Environ Health 15: 98, 2016.
 38.Dockery DW. Epidemiologic evidence of cardiovascular effects of particulate air pollution. Environ Health Perspect 109 (Suppl 4): 483‐486, 2001.
 39.Dockery DW, Pope CA III, Xu X, Spengler JD, Ware JH, Fay ME, Ferris BG Jr, Speizer FE. An association between air pollution and mortality in six U.S. cities. N Engl J Med 329: 1753‐1759, 1993.
 40.Dominici F, Peng RD, Bell ML, Pham L, McDermott A, Zeger SL, Samet JM. Fine particulate air pollution and hospital admission for cardiovascular and respiratory diseases. JAMA 295: 1127‐1134, 2006.
 41.Dostert C, Petrilli V, Van Bruggen R, Steele C, Mossman BT, Tschopp J. Innate immune activation through Nalp3 inflammasome sensing of asbestos and silica. Science (New York, NY) 320: 674‐677, 2008.
 42.Dougherty RH, Fahy JV. Acute exacerbations of asthma: Epidemiology, biology and the exacerbation‐prone phenotype. Clin Exp Allergy 39: 193‐202, 2009.
 43.Douglas P, Robertson S, Gay R, Hansell AL, Gant TW. A systematic review of the public health risks of bioaerosols from intensive farming. Int J Hyg Environ Health 221: 134‐173, 2018.
 44.Douwes J, Thorne P, Pearce N, Heederik D. Bioaerosol health effects and exposure assessment: Progress and prospects. Ann Occup Hyg 47: 187‐200, 2003.
 45.Fubini B, Hubbard A. Reactive oxygen species (ROS) and reactive nitrogen species (RNS) generation by silica in inflammation and fibrosis. Free Radic Biol Med 34: 1507‐1516, 2003.
 46.Furuyama A, Kanno S, Kobayashi T, Hirano S. Extrapulmonary translocation of intratracheally instilled fine and ultrafine particles via direct and alveolar macrophage‐associated routes. Arch Toxicol 83: 429‐437, 2009.
 47.Gergen PJ, Turkeltaub PC. The association of individual allergen reactivity with respiratory disease in a national sample: Data from the second National Health and Nutrition Examination Survey, 1976–1980 (NHANES II). J Allergy Clin Immunol 90: 579‐588, 1992.
 48.Gordian ME, Haneuse S, Wakefield J. An investigation of the association between traffic exposure and the diagnosis of asthma in children. J Expo Sci Environ Epidemiol 16: 49, 2005.
 49.Gosens I, Post JA, de la Fonteyne LJJ, Jansen EHJM, Geus JW, Cassee FR, de Jong WH. Impact of agglomeration state of nano‐ and submicron sized gold particles on pulmonary inflammation. Part Fibre Toxicol 7: 37‐37, 2010.
 50.Gross P, Tuma J, DeTreville RTP. Lungs of workers exposed to fibreglass. Arch Environ Health 23: 67, 1971.
 51.Guarnieri M, Balmes JR. Outdoor air pollution and asthma. Lancet 383: 1581‐1592, 2014.
 52.Gulumian M, Borm PJ, Vallyathan V, Castranova V, Donaldson K, Nelson G, Murray J. Mechanistically identified suitable biomarkers of exposure, effect, and susceptibility for silicosis and coal‐worker's pneumoconiosis: A comprehensive review. J Toxicol Environ Health B Crit Rev 9: 357‐395, 2006.
 53.Hajat S, Anderson HR, Atkinson RW, Haines A. Effects of air pollution on general practitioner consultations for upper respiratory diseases in London. Occup Environ Med 59: 294‐299, 2002.
 54.Han SG, Lee JS, Ahn K, Kim YS, Kim JK, Lee JH, Shin JH, Jeon KS, Cho WS, Song NW, Gulumian M, Shin BS, Yu IJ. Size‐dependent clearance of gold nanoparticles from lungs of Sprague‐Dawley rats after short‐term inhalation exposure. Arch Toxicol 89: 1083‐1094, 2015.
 55.Hargrove MM, McGee JK, Gibbs‐Flournoy EA, Wood CE, Kim YH, Gilmour MI, Gavett SH. Source‐apportioned coarse particulate matter exacerbates allergic airway responses in mice. Inhal Toxicol 30: 405‐415, 2018.
 56.Hasegawa G, Hirano M, Ishihara Y. Differential gene expression associated with inflammation and blood pressure regulation induced by concentrated ambient particle exposure. Inhal Toxicol 23: 897‐905, 2011.
 57.He Y, Gu Z, Lu W, Zhang L, Okuda T, Fujioka K, Luo H, Yu CW. Atmospheric humidity and particle charging state on agglomeration of aerosol particles. Atmos Environ 197: 141‐149, 2019.
 58.Heederik D, Brouwer R, Biersteker K, Boleij JS. Relationship of airborne endotoxin and bacteria levels in pig farms with the lung function and respiratory symptoms of farmers. Int Arch Occup Environ Health 62: 595‐601, 1991.
 59.Henao‐Mejia J, Elinav E, Thaiss CA, Flavell RA. Inflammasomes and metabolic disease. Annu Rev Physiol 76: 57‐78, 2014.
 60.Hopkins LE, Laing EA, Peake JL, Uyeminami D, Mack SM, Li X, Smiley‐Jewell S, Pinkerton KE. Repeated iron‐soot exposure and nose‐to‐brain transport of inhaled ultrafine particles. Toxicol Pathol 46: 75‐84, 2018.
 61.Hou L, Zhu ZZ, Zhang X, Nordio F, Bonzini M, Schwartz J, Hoxha M, Dioni L, Marinelli B, Pegoraro V, Apostoli P, Bertazzi PA, Baccarelli A. Airborne particulate matter and mitochondrial damage: A cross‐sectional study. Environ Health 9: 48, 2010.
 62.Ibald‐Mulli A, Timonen K, Peters A, Heinrich J, Wolke G, Lanki T, Buzorius G, Kreyling W, de Hartog J, Hoek G, ten Brink H, Pekkanen J. Effects of particulate air pollution on blood pressure and heart rate in subjects with cardiovascular disease: A multicenter approach. Environ Health Perspect 112: 369‐377, 2004.
 63.Int Panis L, Provost EB, Cox B, Louwies T, Laeremans M, Standaert A, Dons E, Holmstock L, Nawrot T, De Boever P. Short‐term air pollution exposure decreases lung function: A repeated measures study in healthy adults. Environ Health 16: 60, 2017.
 64.Jou MJ. Pathophysiological and pharmacological implications of mitochondria‐targeted reactive oxygen species generation in astrocytes. Adv Drug Deliv Rev 60: 1512‐1526, 2008.
 65.Kaan PM, Hegele RG. Interaction between respiratory syncytial virus and particulate matter in guinea pig alveolar macrophages. Am J Respir Cell Mol Biol 28: 697‐704, 2003.
 66.Kaiser J. Mounting Evidence Indicts Fine‐Particle Pollution. Science (New York, NY) 307: 1858, 2005.
 67.Kelly FJ, Fussell JC. Air pollution and airway disease. Clin Exp Allergy 41: 1059‐1071, 2011.
 68.Kim CS, Hu S‐C. Total respiratory tract deposition of fine micrometer‐sized particles in healthy adults: Empirical equations for sex and breathing pattern. J Appl Physiol 101: 401‐412, 2006.
 69.Kim J, Chankeshwara SV, Thielbeer F, Jeong J, Donaldson K, Bradley M, Cho WS. Surface charge determines the lung inflammogenicity: A study with polystyrene nanoparticles. Nanotoxicology 10: 94‐101, 2016.
 70.Knaapen AM, Borm PJ, Albrecht C, Schins RP. Inhaled particles and lung cancer. Part A: Mechanisms. Int J Cancer 109: 799‐809, 2004.
 71.Koster ES, Raaijmakers JA, Vijverberg SJ, van der Ent CK, Maitland‐van der Zee AH. Asthma symptoms in pediatric patients: Differences throughout the seasons. J Asthma 48: 694‐700, 2011.
 72.Kovacic P, Somanathan R. Biomechanisms of nanoparticles (toxicants, antioxidants and therapeutics): Electron transfer and reactive oxygen species. J Nanosci Nanotechnol 10: 7919‐7930, 2010.
 73.Kresge N, Simoni RD, Hill RL. Otto Fritz Meyerhof and the elucidation of the glycolytic pathway. J Biol Chem 280: e3, 2005.
 74.Kreyling WG, Semmler M, Erbe F, Mayer P, Takenaka S, Schulz H, Oberdorster G, Ziesenis A. Translocation of ultrafine insoluble iridium particles from lung epithelium to extrapulmonary organs is size dependent but very low. J Toxicol Environ Health A 65: 1513‐1530, 2002.
 75.Lambert AL, Dong W, Selgrade MK, Gilmour MI. Enhanced allergic sensitization by residual oil fly ash particles is mediated by soluble metal constituents. Toxicol Appl Pharmacol 165: 84‐93, 2000.
 76.Lambert AL, Mangum JB, DeLorme MP, Everitt JI. Ultrafine carbon black particles enhance respiratory syncytial virus‐induced airway reactivity, pulmonary inflammation, and chemokine expression. Toxicol Sci 72: 339‐346, 2003.
 77.Lee MK, Xu CJ, Carnes MU, Nichols CE, Ward JM, Kwon SO, Kim SY, Kim WJ, London SJ. Genome‐wide DNA methylation and long‐term ambient air pollution exposure in Korean adults. Clin Epigenetics 11: 37, 2019.
 78.Li JJ, Muralikrishnan S, Ng CT, Yung LY, Bay BH. Nanoparticle‐induced pulmonary toxicity. Exp Biol Med (Maywood) 235: 1025‐1033, 2010.
 79.Li J, Sun S, Tang R, et al. Major air pollutants and risk of COPD exacerbations: a systematic review and meta-analysis. Int J Chron Obstruct Pulmon Dis 11: 3079‐3091, 2016.
 80.Li N, Xia T, Nel AE. The role of oxidative stress in ambient particulate matter‐induced lung diseases and its implications in the toxicity of engineered nanoparticles. Free Radic Biol Med 44: 1689‐1699, 2008.
 81.Lin M, Stieb DM, Chen Y. Coarse particulate matter and hospitalization for respiratory infections in children younger than 15 years in Toronto: A case‐crossover analysis. Pediatrics 116: e235‐e240, 2005.
 82.Lundborg M, Dahlén S‐E, Johard U, Gerde P, Jarstrand C, Camner P, Låstbom L. Aggregates of ultrafine particles impair phagocytosis of microorganisms by human alveolar macrophages. Environ Res 100: 197‐204, 2006.
 83.Madl AK, Carosino C, Pinkerton KE. 8.22 – Particle toxicities. In: McQueen CA, editor. Comprehensive Toxicology (2nd ed). Oxford: Elsevier, 2010, p. 421‐451.
 84.Madl AK, Plummer LE, Carosino C, Pinkerton KE. Nanoparticles, lung injury, and the role of oxidant stress. Annu Rev Physiol 76: 447‐465, 2014.
 85.Matthews NC, Pfeffer PE, Mann EH, Kelly FJ, Corrigan CJ, Hawrylowicz CM, Lee TH. Urban particulate matter‐activated human dendritic cells induce the expansion of potent inflammatory Th1, Th2, and Th17 effector cells. Am J Respir Cell Mol Biol 54: 250‐262, 2016.
 86.McConnell R, Berhane K, Gilliland F, London SJ, Islam T, Gauderman WJ, Avol E, Margolis HG, Peters JM. Asthma in exercising children exposed to ozone: A cohort study. Lancet 359: 386‐391, 2002.
 87.McConnell R, Berhane K, Gilliland F, London SJ, Vora H, Avol E, Gauderman WJ, Margolis HG, Lurmann F, Thomas DC, Peters JM. Air pollution and bronchitic symptoms in Southern California children with asthma. Environ Health Perspect 107: 757‐760, 1999.
 88.McConnell R, Islam T, Shankardass K, Jerrett M, Lurmann F, Gilliland F, Gauderman J, Avol E, Künzli N, Yao L, Peters J, Berhane K. Childhood incident asthma and traffic‐related air pollution at home and school. Environ Health Perspect 118: 1021‐1026, 2010.
 89.Millner PD. Bioaerosols associated with animal production operations. Bioresour Technol 100: 5379‐5385, 2009.
 90.Mombaerts P. Axonal wiring in the mouse olfactory system. Annu Rev Cell Dev Biol 22: 713‐737, 2006.
 91.Morgan A, Holmes A. Concentrations and dimensions of coated and uncoated asbestos fibres in the human lung. Br J Ind Med 37: 25, 1980.
 92.Mossman BT, Lippmann M, Hesterberg TW, Kelsey KT, Barchowsky A, Bonner JC. Pulmonary endpoints (lung carcinomas and asbestosis) following inhalation exposure to asbestos. J Toxicol Environ Health B Crit Rev 14: 76‐121, 2011.
 93.Mutlu EA, Comba IY, Cho T, Engen PA, Yazici C, Soberanes S, Hamanaka RB, Nigdelioglu R, Meliton AY, Ghio AJ, Budinger GRS, Mutlu GM. Inhalational exposure to particulate matter air pollution alters the composition of the gut microbiome. Environ Pollut 240: 817‐830, 2018.
 94.Mutlu EA, Engen PA, Soberanes S, Urich D, Forsyth CB, Nigdelioglu R, Chiarella SE, Radigan KA, Gonzalez A, Jakate S, Keshavarzian A, Budinger GR, Mutlu GM. Particulate matter air pollution causes oxidant‐mediated increase in gut permeability in mice. Part Fibre Toxicol 8: 19, 2011.
 95.Nayak AP, Green BJ, Lemons AR, Marshall NB, Goldsmith WT, Kashon ML, Anderson SE, Germolec DR, Beezhold DH. Subchronic exposures to fungal bioaerosols promotes allergic pulmonary inflammation in naïve mice. Clin Exp Allergy 46: 861‐870, 2016.
 96.Nikula KJ, Avila KJ, Griffith WC, Mauderly JL. Lung tissue responses and sites of particle retention differ between rats and cynomolgus monkeys exposed chronically to diesel exhaust and coal dust. Fundam Appl Toxicol 37: 37‐53, 1997.
 97.Noah TL, Zhou H, Zhang H, Horvath K, Robinette C, Kesic M, Meyer M, Diaz‐Sanchez D, Jaspers I. Diesel exhaust exposure and nasal response to attenuated influenza in normal and allergic volunteers. Am J Respir Crit Care Med 185: 179‐185, 2012.
 98.Nygard K, Werner‐Johansen O, Ronsen S, Caugant DA, Simonsen O, Kanestrom A, Ask E, Ringstad J, Odegard R, Jensen T, Krogh T, Hoiby EA, Ragnhildstveit E, Aaberge IS, Aavitsland P. An outbreak of legionnaires disease caused by long‐distance spread from an industrial air scrubber in Sarpsborg, Norway. Clin Infect Dis 46: 61‐69, 2008.
 99.Oberdörster G. Lung dosimetry: Pulmonary clearance of inhaled particles. Aerosol Sci Tech 18: 279‐289, 1993.
 100.Ong WY, Shalini SM, Costantino L. Nose‐to‐brain drug delivery by nanoparticles in the treatment of neurological disorders. Curr Med Chem 21: 4247‐4256, 2014.
 101.Orellano P, Quaranta N, Reynoso J, Balbi B, Vasquez J. Effect of outdoor air pollution on asthma exacerbations in children and adults: Systematic review and multilevel meta‐analysis. PLoS One 12: e0174050, 2017.
 102.Oya E, Zegeye FD, Bolling AK, Ovstebo R, Afanou AKJ, Ovrevik J, Refsnes M, Holme JA. Hyphae fragments from A. fumigatus sensitize lung cells to silica particles (Min‐U‐Sil): Increased release of IL‐1beta. Toxicol In Vitro 55: 1‐10, 2019.
 103.Passchier W, Knottnerus A, Albering H, Walda I. Public health impact of large airports. Rev Environ Health 15: 83‐96, 2000.
 104.Pearson C, Littlewood E, Douglas P, Robertson S, Gant TW, Hansell AL. Exposures and health outcomes in relation to bioaerosol emissions from composting facilities: A systematic review of occupational and community studies. J Toxicol Environ Health B Crit Rev 18: 43‐69, 2015.
 105.Pinkerton KE, Green FH, Saiki C, Vallyathan V, Plopper CG, Gopal V, Hung D, Bahne EB, Lin SS, Menache MG, Schenker MB. Distribution of particulate matter and tissue remodeling in the human lung. Environ Health Perspect 108: 1063‐1069, 2000.
 106.Pinkerton KE, Plopper CG, Mercer RR, Roggli VL, Patra AL, Brody AR, Crapo JD. Airway branching patterns influence asbestos fiber location and the extent of tissue injury in the pulmonary parenchyma. Lab Invest 55: 688‐695, 1986.
 107.Plummer LE, Pinkerton KE, Reynolds S, Meschke S, Mitloehner F, Bennett D, Smiley‐Jewell S, Schenker MB. Aerosols in the agricultural setting. J Agromed 14: 413‐416, 2009.
 108.Pope CA III. Epidemiology of fine particulate air pollution and human health: Biologic mechanisms and who's at risk? Environ Health Perspect 108 (Suppl 4): 713‐723, 2000.
 109.Rebuli ME, Speen AM, Martin EM, Addo KA, Pawlak EA, Glista‐Baker E, Robinette C, Zhou H, Noah TL, Jaspers I. Wood smoke exposure alters human inflammatory responses to viral infection in a sex‐specific manner: A randomized, placebo‐controlled study. Am J Respir Crit Care Med 199 (8): 996, 1007, 2018.
 110.Reinmuth‐Selzle K, Kampf CJ, Lucas K, Lang‐Yona N, Frohlich‐Nowoisky J, Shiraiwa M, Lakey PSJ, Lai S, Liu F, Kunert AT, Ziegler K, Shen F, Sgarbanti R, Weber B, Bellinghausen I, Saloga J, Weller MG, Duschl A, Schuppan D, Poschl U. Air pollution and climate change effects on allergies in the anthropocene: Abundance, interaction, and modification of allergens and adjuvants. Environ Sci Technol 51: 4119‐4141, 2017.
 111.Reisetter AC, Stebounova LV, Baltrusaitis J, Powers L, Gupta A, Grassian VH, Monick MM. Induction of inflammasome‐dependent pyroptosis by carbon black nanoparticles. J Biol Chem 286: 21844‐21852, 2011.
 112.Renwick LC, Donaldson K, Clouter A. Impairment of alveolar macrophage phagocytosis by ultrafine particles. Toxicol Appl Pharmacol 172: 119‐127, 2001.
 113.Rice MB, Ljungman PL, Wilker EH, Gold DR, Schwartz JD, Koutrakis P, Washko GR, O'Connor GT, Mittleman MA. Short‐term exposure to air pollution and lung function in the Framingham Heart Study. Am J Respir Crit Care Med 188: 1351‐1357, 2013.
 114.Robertson S, Douglas P, Jarvis D, Marczylo E. Bioaerosol exposure from composting facilities and health outcomes in workers and in the community: A systematic review update. Int J Hyg Environ Health 222: 364‐386, 2019.
 115.Robinson RK, Birrell MA, Adcock JJ, Wortley MA, Dubuis ED, Chen S, McGilvery CM, Hu S, Shaffer MSP, Bonvini SJ, Maher SA, Mudway IS, Porter AE, Carlsten C, Tetley TD, Belvisi MG. Mechanistic link between diesel exhaust particles and respiratory reflexes. J Allergy Clin Immunol 141: 1074.e9‐1084.e9, 2018.
 116.Rylance J, Chimpini C, Semple S, Russell DG, Jackson MJ, Heyderman RS, Gordon SB. Chronic household air pollution exposure is associated with impaired alveolar macrophage function in malawian non‐smokers. PLoS One 10: e0138762, 2015.
 117.Rylance J, Fullerton DG, Scriven J, Aljurayyan AN, Mzinza D, Barrett S, Wright AKA, Wootton DG, Glennie SJ, Baple K, Knott A, Mortimer K, Russell DG, Heyderman RS, Gordon SB. Household air pollution causes dose‐dependent inflammation and altered phagocytosis in human macrophages. Am J Respir Cell Mol Biol 52: 584‐593, 2015.
 118.Samake A, Uzu G, Martins JMF, Calas A, Vince E, Parat S, Jaffrezo JL. The unexpected role of bioaerosols in the Oxidative Potential of PM. Sci Rep 7: 10978, 2017.
 119.Samaridou E, Alonso MJ. Nose‐to‐brain peptide delivery – The potential of nanotechnology. Bioorg Med Chem 26: 2888‐2905, 2018.
 120.Samet JM, Dominici F, Curriero FC, Coursac I, Zeger SL. Fine particulate air pollution and mortality in 20 U.S. cities, 1987‐1994. N Engl J Med 343: 1742‐1749, 2000.
 121.Sana A, Somda SMA, Meda N, Bouland C. Chronic obstructive pulmonary disease associated with biomass fuel use in women: A systematic review and meta‐analysis. BMJ Open Respir Res 5: e000246, 2018.
 122.Saunders V, Breysse P, Clark J, Sproles A, Davila M, Wills‐Karp M. Particulate matter‐induced airway hyperresponsiveness is lymphocyte dependent. Environ Health Perspect 118: 640‐646, 2010.
 123.Schenker MB, Pinkerton KE, Mitchell D, Vallyathan V, Elvine‐Kreis B, Green FHY. Pneumoconiosis from agricultural dust exposure among young California farmworkers. Environ Health Perspect. 117(6): 988‐994, 2009.
 124.Selvaraj K, Gowthamarajan K, Karri V. Nose to brain transport pathways an overview: Potential of nanostructured lipid carriers in nose to brain targeting. Artif Cells Nanomed Biotechnol 46: 2088‐2095, 2018.
 125.Shahan TA, Sorenson WG, Paulauskis JD, Morey R, Lewis DM. Concentration‐ and time‐dependent upregulation and release of the cytokines MIP‐2, KC, TNF, and MIP‐1 α in rat alveolar macrophages by fungal spores implicated in airway inflammation. Am J Respir Cell Mol Biol 18: 435‐440, 1998.
 126.Shamsollahi HR, Ghoochani M, Jaafari J, Moosavi A, Sillanpää M, Alimohammadi M. Environmental exposure to endotoxin and its health outcomes: A systematic review. Ecotoxicol Environ Saf 174: 236‐244, 2019.
 127.Shvedova AA, Kapralov AA, Feng WH, Kisin ER, Murray AR, Mercer RR, St Croix CM, Lang MA, Watkins SC, Konduru NV, Allen BL, Conroy J, Kotchey GP, Mohamed BM, Meade AD, Volkov Y, Star A, Fadeel B, Kagan VE. Impaired clearance and enhanced pulmonary inflammatory/fibrotic response to carbon nanotubes in myeloperoxidase‐deficient mice. PLoS One 7: e30923, 2012.
 128.Siddharthan T, Grigsby MR, Goodman D, Chowdhury M, Rubinstein A, Irazola V, Gutierrez L, Miranda JJ, Bernabe‐Ortiz A, Alam D, Kirenga B, Jones R, van Gemert F, Wise RA, Checkley W. Association between household air pollution exposure and chronic obstructive pulmonary disease outcomes in 13 low‐ and middle‐income country settings. Am J Respir Crit Care Med 197: 611‐620, 2018.
 129.Sint T, Donohue JF, Ghio AJ. Ambient air pollution particles and the acute exacerbation of chronic obstructive pulmonary disease. Inhal Toxicol 20: 25‐29, 2008.
 130.Smith KR, Kim S, Recendez JJ, Teague SV, Menache MG, Grubbs DE, Sioutas C, Pinkerton KE. Airborne particles of the california central valley alter the lungs of healthy adult rats. Environ Health Perspect 111: 902‐908; discussion A408‐909, 2003.
 131.Sokol K, Sur S, Ameredes BT. Inhaled environmental allergens and toxicants as determinants of the asthma phenotype. Adv Exp Med Biol 795: 43‐73, 2014.
 132.Spieksma FTM, Nikkels BH, Dijkman JH. Seasonal appearance of grass pollen allergen in natural, pauci‐micronic aerosol of various size fractions. Relationship with airborne grass pollen concentration. Clin Exp Allergy 25: 234‐239, 1995.
 133.Sundar IK, Yin Q, Baier BS, Yan L, Mazur W, Li D, Susiarjo M, Rahman I. DNA methylation profiling in peripheral lung tissues of smokers and patients with COPD. Clin Epigenetics 9: 38, 2017.
 134.Sykes A, Johnston SL. Etiology of asthma exacerbations. J Allergy Clin Immunol 122: 685‐688, 2008.
 135.Taylor PE, Flagan RC, Valenta R, Glovsky MM. Release of allergens as respirable aerosols: A link between grass pollen and asthma. J Allergy Clin Immunol 109: 51‐56, 2002.
 136.Thomas RJ, Davies C, Nunez A, Hibbs S, Eastaugh L, Harding S, Jordan J, Barnes K, Oyston P, Eley S. Particle‐size dependent effects in the Balb/c murine model of inhalational melioidosis. Front Cell Infect Microbiol 2: 101‐101, 2012.
 137.Timbrell V. Measurement of Fibers in Human Lung Tissue. International Agency for Research on Cancer: Lyon, France, 1980.
 138.Timm M, Madsen AM, Hansen JV, Moesby L, Hansen EW. Assessment of the total inflammatory potential of bioaerosols by using a granulocyte assay. Appl Environ Microbiol 75: 7655‐7662, 2009.
 139.Tong DQ, Wang JXL, Gill TE, Lei H, Wang B. Intensified dust storm activity and Valley fever infection in the southwestern United States. Geophys Res Lett 44: 4304‐4312, 2017.
 140.Touri L, Marchetti H, Sari‐Minodier I, Molinari N, Chanez P. The airport atmospheric environment: Respiratory health at work. Eur Respir Rev 22: 124, 2013.
 141.Uh S‐T, Koo SM, Kim Y, Kim K, Park S, Jang AS, Kim D, Kim YH, Park C‐S. The activation of NLRP3‐inflammsome by stimulation of diesel exhaust particles in lung tissues from emphysema model and RAW 264.7 cell line. Korean J Intern Med 32: 865‐874, 2017.
 142.US EPA. Air Quality Criteria for Particulate Matter. EPA 600/P‐99/002aF‐bF. Washington, D.C.: US Environmental Protection Agency (US EPA), 2004.
 143.US EPA. Provisional Assessment of Recent Studies on Particulate Matter. EPA/600/R‐06/063. Washington, D.C.: US Environmental Protection Agency (US EPA), 2006.
 144.US EPA. Air Quality Index: A Guide to Air Quality and Your Health EPA‐456/F‐14‐002. Washington, D.C.: US Environmental Protection Agency (US EPA), 2014.
 145.van Kampen V, Hoffmeyer F, Deckert A, Kendzia B, Casjens S, Neumann HD, Buxtrup M, Willer E, Felten C, Schoneich R, Bruning T, Raulf M, Bunger J. Effects of bioaerosol exposure on respiratory health in compost workers: A 13‐year follow‐up study. Occup Environ Med 73: 829‐837, 2016.
 146.Vandini S, Corvaglia L, Alessandroni R, Aquilano G, Marsico C, Spinelli M, Lanari M, Faldella G. Respiratory syncytial virus infection in infants and correlation with meteorological factors and air pollutants. Ital J Pediatr 39: 1‐1, 2013.
 147.Velali E, Papachristou E, Pantazaki A, Besis A, Samara C, Labrianidis C, Lialiaris T. In vitro cellular toxicity induced by extractable organic fractions of particles exhausted from urban combustion sources – Role of PAHs. Environ Pollut 243: 1166‐1176, 2018.
 148.Veranth JM, Kaser EG, Veranth MM, Koch M, Yost GS. Cytokine responses of human lung cells (BEAS‐2B) treated with micron‐sized and nanoparticles of metal oxides compared to soil dusts. Part Fibre Toxicol 4: 2, 2007.
 149.Veranth JM, Reilly CA, Veranth MM, Moss TA, Langelier CR, Lanza DL, Yost GS. Inflammatory cytokines and cell death in BEAS‐2B lung cells treated with soil dust, lipopolysaccharide, and surface‐modified particles. Toxicol Sci 82: 88‐96, 2004.
 150.Vidrio E, Jung H, Anastasio C. Generation of hydroxyl radicals from dissolved transition metals in surrogate lung fluid solutions. Atmos Environ 42: 4369‐4379, 2008.
 151.Wang H, Song L, Ju W, Wang X, Dong L, Zhang Y, Ya P, Yang C, Li F. The acute airway inflammation induced by PM2.5 exposure and the treatment of essential oils in Balb/c mice. Sci Rep 7: 44256, 2017.
 152.Weaver EA, Kolivras KN. Investigating the relationship between climate and valley fever (coccidioidomycosis). Ecohealth, 2018.
 153.Wilson AF, Novey HS, Berke RA, Surprenant EL. Deposition of inhaled pollen and pollen extract in human airways. N Engl J Med 288: 1056‐1058, 1973.
 154.Xia T, Kovochich M, Brant J, Hotze M, Sempf J, Oberley T, Sioutas C, Yeh JI, Wiesner MR, Nel AE. Comparison of the abilities of ambient and manufactured nanoparticles to induce cellular toxicity according to an oxidative stress paradigm. Nano Lett 6: 1794‐1807, 2006.
 155.Xiao GG, Wang M, Li N, Loo JA, Nel AE. Use of proteomics to demonstrate a hierarchical oxidative stress response to diesel exhaust particle chemicals in a macrophage cell line. J Biol Chem 278: 50781‐50790, 2003.
 156.Yazdi AS, Guarda G, Riteau N, Drexler SK, Tardivel A, Couillin I, Tschopp J. Nanoparticles activate the NLR pyrin domain containing 3 (Nlrp3) inflammasome and cause pulmonary inflammation through release of IL‐1alpha and IL‐1beta. Proc Natl Acad Sci U S A 107: 19449‐19454, 2010.
 157.Zamfir M, Gerstner DG, Walser SM, Bünger J, Eikmann T, Heinze S, Kolk A, Nowak D, Raulf M, Sagunski H, Sedlmaier N, Suchenwirth R, Wiesmüller GA, Wollin K‐M, Tesseraux I, Herr CEW. A systematic review of experimental animal studies on microbial bioaerosols: Dose‐response data for the derivation of exposure limits. Int J Hyg Environ Health 222: 249‐259, 2019.
 158.Zhang J, Fulgar CC, Mar T, Young DE, Zhang Q, Bein KJ, Cui L, Castaneda A, Vogel CFA, Sun X, Li W, Smiley‐Jewell S, Zhang Z, Pinkerton KE. TH17‐induced neutrophils enhance the pulmonary allergic response following BALB/c exposure to house dust mite allergen and fine particulate matter from California and China. Toxicol Sci 164: 627‐643, 2018.
 159.Zwozdziak A, Sówka I, Willak‐Janc E, Zwozdziak J, Kwiecińska K, Balińska‐Miśkiewicz W. Influence of PM(1) and PM(2.5) on lung function parameters in healthy schoolchildren‐a panel study. Environ Sci Pollut Res Int 23: 23892‐23901, 2016.

Teaching Material

Savannah M. Mack, Amy K. Madl, Kent E. Pinkerton. Respiratory Health Effects of Exposure to Ambient Particulate Matter and Bioaerosols. Compr Physiol 10: 2020,1-20.

Didactic Synopsis

Major Teaching Points:

*Particulate matter (PM) includes all solid and liquid pollutants. Examples are environmental, anthropogenic and combustion-based particles.

*Bioaerosols are particles originating from microbial, fungal, animal, and plant sources.

*When combined with other stressors (such as bioaerosols), chronic exposure to PM could lead to new onset lung disease.

*Respirable bioaerosol fragments can be found in PM2.5 and PM10.

*Bioaerosol dispersion is dependent on the environment (i.e., the location, weather, and climate).

*Co-exposure of PM and bioaerosols is associated with increased inflammation, lung injury, and disease exacerbation.

*New research on co-exposure to PM and bioaerosols in human populations, cellular and animal models is needed.

Didactic Legends

The following legends to the figures that appear throughout the article are written to be useful for teaching.

Figure 1: Teaching point: the environment has an effect on air pollution and how it subsequently affects respiratory health.

Figure 2: This figure compares the sizes of common bioaerosols and regularly measured and regulated PM fractions.

Figure 3: This figure illustrates where particles land in the respiratory tract based on their diameter.

Figure 4: This figure illustrates the five main mechanisms of particle deposition in the respiratory tract.

Figure 5: Teaching point: ROS can be produced by PM intrinsically, or by PM-cellular interactions.

Figure 6: This figure illustrates the main mechanisms of particle clearance from the respiratory tract.

Figure 7: This figure illustrates the increased hazard of disease mortality with increasing concentrations of PM2.5.

body>  


Related Articles:

Lung Mechanics in Disease
Particle Transport and Deposition: Basic Physics of Particle Kinetics
Teaching Material

Contact Editor

Submit a note to the editor about this article by filling in the form below.

* Required Field

How to Cite

Savannah M. Mack, Amy K. Madl, Kent E. Pinkerton. Respiratory Health Effects of Exposure to Ambient Particulate Matter and Bioaerosols. Compr Physiol 2019, 10: 1-20. doi: 10.1002/cphy.c180040