Inflammatory health effects of indoor and outdoor particulate matter

  • Author Footnotes
    ∗ These authors contributed equally to this work.
    Weidong Wu
    Footnotes
    ∗ These authors contributed equally to this work.
    Affiliations
    Department of Occupational and Environmental Health, School of Public Health, Xinxiang Medical University, Xinxiang, China
    Search for articles by this author
  • Author Footnotes
    ∗ These authors contributed equally to this work.
    Yuefei Jin
    Footnotes
    ∗ These authors contributed equally to this work.
    Affiliations
    Department of Epidemiology, College of Public Health, Zhengzhou University, Zhengzhou, China
    Search for articles by this author
  • Author Footnotes
    ∗ These authors contributed equally to this work.
    Chris Carlsten
    Correspondence
    Corresponding author: Chris Carlsten, MD, MPH, Department of Medicine, 2775 Laurel St, Vancouver General Hospital, Vancouver, British Columbia V5Z 1M9, Canada.
    Footnotes
    ∗ These authors contributed equally to this work.
    Affiliations
    Air Pollution Exposure Laboratory, Department of Medicine and School of Population and Public Health, University of British Columbia, Vancouver, British Columbia, Canada
    Search for articles by this author
  • Author Footnotes
    ∗ These authors contributed equally to this work.

      Information for Category 1 CME Credit

      Credit can now be obtained, free for a limited time, by reading the review articles in this issue. Please note the following instructions.
      Method of Physician Participation in Learning Process: The core material for these activities can be read in this issue of the Journal or online at the JACI Web site: www.jacionline.org. The accompanying tests may only be submitted online at www.jacionline.org. Fax or other copies will not be accepted.
      Date of Original Release: March 2018. Credit may be obtained for these courses until February 28, 2019.
      Copyright Statement: Copyright © 2018-2019. All rights reserved.
      Overall Purpose/Goal: To provide excellent reviews on key aspects of allergic disease to those who research, treat, or manage allergic disease.
      Target Audience: Physicians and researchers within the field of allergic disease.
      Accreditation/Provider Statements and Credit Designation: The American Academy of Allergy, Asthma & Immunology (AAAAI) is accredited by the Accreditation Council for Continuing Medical Education (ACCME) to provide continuing medical education for physicians. The AAAAI designates this journal-based CME activity for a maximum of 1.00 AMA PRA Category 1 Credit™. Physicians should claim only the credit commensurate with the extent of their participation in the activity.
      List of Design Committee Members: Weidong Wu, PhD, Yuefei Jin, MD, and Chris Carlsten, MD, MPH (authors); Zuhair K. Ballas, MD (editor)
      Disclosure of Significant Relationships with Relevant Commercial
      Companies/Organizations: The authors declare that they have no relevant conflicts of interest. Z. K. Ballas (editor) disclosed no relevant financial relationships.
      Activity Objectives:
      • 1.
        To recognize that particulate matter (PM) can have significant pulmonary and cardiovascular effects.
      • 2.
        To identify some of the inflammatory changes and potential health consequences that can occur with exposure to PM.
      Recognition of Commercial Support: This CME activity has not received external commercial support.
      List of CME Exam Authors: Evelyn Angulo, MD, Anna Lang, MD, PhD, David Peloza, MD, Cheryl Steiman, MD, and Sameer K. Mathur, MD, PhD.
      Disclosure of Significant Relationships with Relevant Commercial
      Companies/Organizations: The exam authors disclosed no relevant financial relationships.
      Inflammation is a common and essential event in the pathogenesis of diverse diseases. Decades of research has converged on an understanding that all combustion-derived particulate matter (PM) is inflammatory to some extent in the lungs and also systemically, substantially explaining a significant portion of the massive cardiopulmonary disease burden associated with these exposures. In general, this means that efforts to do the following can all be beneficial: reduce particulates at the source, decrease the inflammatory potential of PM output, and, where PM inhalation is unavoidable, administer anti-inflammatory treatment. A range of research, including basic illumination of inflammatory pathways, assessment of disease burden in large cohorts, tailored treatment trials, and epidemiologic, animal, and in vitro studies, is highlighted in this review. However, meaningful translation of this research to decrease the burden of disease and deliver a clear and cohesive message to guide daily clinical practice remains rudimentary. Ongoing efforts to better understand substantial differences in the concentration and type of PM to which the global community is exposed and then distill how that influences inflammation promises to have real-world benefit. This review addresses this complex topic in 3 sections, including ambient PM (typically associated with ground-level transportation), wildfire-induced PM, and PM from indoor biomass burning. Recognizing the overlap between these domains, we also describe differences and suggest future directions to better inform clinical practice and public health.

      Key words

      Abbreviations used:

      ALRI (Acute lower respiratory tract infection), BAL (Bronchoalveolar lavage), COPD (Chronic obstructive pulmonary disease), CVD (Cardiovascular disorder), ED (Emergency department), ICS (Inhaled corticosteroid), PAH (Polycyclic aromatic hydrocarbon), PM (Particulate matter), TLR (Toll-like receptor)
      To read this article in full you will need to make a payment

      References

        • Mannucci P.M.
        • Harari S.
        • Martinelli I.
        • Franchini M.
        Effects on health of air pollution: a narrative review.
        Intern Emerg Med. 2015; 10: 657-662
        • Schins R.P.
        • Lightbody J.H.
        • Borm P.J.
        • Shi T.
        • Donaldson K.
        • Stone V.
        Inflammatory effects of coarse and fine particulate matter in relation to chemical and biological constituents.
        Toxicol Appl Pharmacol. 2004; 195: 1-11
        • Valavanidis A.
        • Fiotakis K.
        • Vlachogianni T.
        Airborne particulate matter and human health: toxicological assessment and importance of size and composition of particles for oxidative damage and carcinogenic mechanisms.
        J Environ Sci Health C Environ Carcinog Ecotoxicol Rev. 2008; 26: 339-362
        • Li Y.
        • Rittenhouse-Olson K.
        • Scheider W.L.
        • Mu L.
        Effect of particulate matter air pollution on C-reactive protein: a review of epidemiologic studies.
        Rev Environ Health. 2012; 27: 133-149
        • Simoni M.
        • Baldacci S.
        • Maio S.
        • Cerrai S.
        • Sarno G.
        • Viegi G.
        Adverse effects of outdoor pollution in the elderly.
        J Thorac Dis. 2015; 7: 34-45
        • Tanaka T.
        • Asai M.
        • Yanagita Y.
        • Nishinakagawa T.
        • Miyamoto N.
        • Kotaki K.
        • et al.
        Longitudinal study of respiratory function and symptoms in a non-smoking group of long-term officially-acknowledged victims of pollution-related illness.
        BMC Public Health. 2013; 13: 766
        • van Berlo D.
        • Hullmann M.
        • Schins R.P.
        Toxicology of ambient particulate matter.
        EXS. 2012; 101: 165-217
        • Zanobetti A.
        • Schwartz J.
        • Dockery D.W.
        Airborne particles are a risk factor for hospital admissions for heart and lung disease.
        Environ Health Perspect. 2000; 108: 1071-1077
        • Dominici F.
        • Peng R.D.
        • Bell M.L.
        • Pham L.
        • McDermott A.
        • Zeger S.L.
        • et al.
        Fine particulate air pollution and hospital admission for cardiovascular and respiratory diseases.
        JAMA. 2006; 295: 1127-1134
        • Gan W.Q.
        • FitzGerald J.M.
        • Carlsten C.
        • Sadatsafavi M.
        • Brauer M.
        Associations of ambient air pollution with chronic obstructive pulmonary disease hospitalization and mortality.
        Am J Respir Crit Care Med. 2013; 187: 721-727
        • Viegi G.
        • Pedreschi M.
        • Baldacci S.
        • Chiaffi L.
        • Pistelli F.
        • Modena P.
        • et al.
        Prevalence rates of respiratory symptoms and diseases in general population samples of North and Central Italy.
        Int J Tuberc Lung Dis. 1999; 3: 1034-1042
        • Schikowski T.
        • Sugiri D.
        • Ranft U.
        • Gehring U.
        • Heinrich J.
        • Wichmann H.E.
        • et al.
        Long-term air pollution exposure and living close to busy roads are associated with COPD in women.
        Respir Res. 2005; 6: 152
        • Balbi B.
        • Pignatti P.
        • Corradi M.
        • Baiardi P.
        • Bianchi L.
        • Brunetti G.
        • et al.
        Bronchoalveolar lavage, sputum and exhaled clinically relevant inflammatory markers: values in healthy adults.
        Eur Respir J. 2007; 30: 769-781
        • Gong J.
        • Zhu T.
        • Kipen H.
        • Wang G.
        • Hu M.
        • Guo Q.
        • et al.
        Comparisons of ultrafine and fine particles in their associations with biomarkers reflecting physiological pathways.
        Environ Sci Technol. 2014; 48: 5264-5273
        • Han Y.
        • Zhu T.
        • Guan T.
        • Zhu Y.
        • Liu J.
        • Ji Y.
        • et al.
        Association between size-segregated particles in ambient air and acute respiratory inflammation.
        Sci Total Environ. 2016; 565: 412-419
        • Wu S.
        • Ni Y.
        • Li H.
        • Pan L.
        • Yang D.
        • Baccarelli A.A.
        • et al.
        Short-term exposure to high ambient air pollution increases airway inflammation and respiratory symptoms in chronic obstructive pulmonary disease patients in Beijing, China.
        Environ Int. 2016; 94: 76-82
        • Chen B.Y.
        • Chan C.C.
        • Lee C.T.
        • Cheng T.J.
        • Huang W.C.
        • Jhou J.C.
        • et al.
        The association of ambient air pollution with airway inflammation in schoolchildren.
        Am J Epidemiol. 2012; 175: 764-774
        • von Klot S.
        • Wolke G.
        • Tuch T.
        • Heinrich J.
        • Dockery D.W.
        • Schwartz J.
        • et al.
        Increased asthma medication use in association with ambient fine and ultrafine particles.
        Eur Respir J. 2002; 20: 691-702
        • Dusseldorp A.
        • Kruize H.
        • Brunekreef B.
        • Hofschreuder P.
        • de Meer G.
        • van Oudvorst A.B.
        Associations of PM10 and airborne iron with respiratory health of adults living near a steel factory.
        Am J Respir Crit Care Med. 1995; 152: 1932-1939
        • Hiltermann T.J.
        • Stolk J.
        • van der Zee S.C.
        • Brunekreef B.
        • de Bruijne C.R.
        • Fischer P.H.
        • et al.
        Asthma severity and susceptibility to air pollution.
        Eur Respir J. 1998; 11: 686-693
        • Roemer W.
        • Hoek G.
        • Brunekreef B.
        Effect of ambient winter air pollution on respiratory health of children with chronic respiratory symptoms.
        Am Rev Respir Dis. 1993; 147: 118-124
        • Gielen M.H.
        • van der Zee S.C.
        • van Wijnen J.H.
        • van Steen C.J.
        • Brunekreef B.
        Acute effects of summer air pollution on respiratory health of asthmatic children.
        Am J Respir Crit Care Med. 1997; 155: 2105-2108
        • Pope 3rd, C.A.
        • Dockery D.W.
        • Spengler J.D.
        • Raizenne M.E.
        Respiratory health and PM10 pollution. A daily time series analysis.
        Am Rev Respir Dis. 1991; 144: 668-674
        • Ierodiakonou D.
        • Zanobetti A.
        • Coull B.A.
        • Melly S.
        • Postma D.S.
        • Boezen H.M.
        • et al.
        Ambient air pollution, lung function, and airway responsiveness in asthmatic children.
        J Allergy Clin Immunol. 2016; 137: 390-399
        • Delfino R.J.
        • Zeiger R.S.
        • Seltzer J.M.
        • Street D.H.
        Symptoms in pediatric asthmatics and air pollution: differences in effects by symptom severity, anti-inflammatory medication use and particulate averaging time.
        Environ Health Perspect. 1998; 106: 751-761
        • Langrish J.P.
        • Bosson J.
        • Unosson J.
        • Muala A.
        • Newby D.E.
        • Mills N.L.
        • et al.
        Cardiovascular effects of particulate air pollution exposure: time course and underlying mechanisms.
        J Intern Med. 2012; 272: 224-239
        • Peters A.
        • Dockery D.W.
        • Muller J.E.
        • Mittleman M.A.
        Increased particulate air pollution and the triggering of myocardial infarction.
        Circulation. 2001; 103: 2810-2815
        • Brook R.D.
        • Rajagopalan S.
        • Pope 3rd, C.A.
        • Brook J.R.
        • Bhatnagar A.
        • Diez-Roux A.V.
        • et al.
        Particulate matter air pollution and cardiovascular disease: an update to the scientific statement from the American Heart Association.
        Circulation. 2010; 121: 2331-2378
        • Delfino R.J.
        • Staimer N.
        • Tjoa T.
        • Arhami M.
        • Polidori A.
        • Gillen D.L.
        • et al.
        Associations of primary and secondary organic aerosols with airway and systemic inflammation in an elderly panel cohort.
        Epidemiology. 2010; 21: 892-902
        • Lee J.T.
        • Son J.Y.
        • Cho Y.S.
        The adverse effects of fine particle air pollution on respiratory function in the elderly.
        Sci Total Environ. 2007; 385: 28-36
        • Zanobetti A.
        • Schwartz J.
        Are diabetics more susceptible to the health effects of airborne particles?.
        Am J Respir Crit Care Med. 2001; 164: 831-833
        • Yang I.A.
        • Fong K.M.
        • Zimmerman P.V.
        • Holgate S.T.
        • Holloway J.W.
        Genetic susceptibility to the respiratory effects of air pollution.
        Postgrad Med J. 2009; 85: 428-436
        • Li N.
        • Xia T.
        • Nel A.E.
        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. 2008; 44: 1689-1699
        • Robinson R.K.
        • Birrell M.A.
        • Adcock J.J.
        • Wortley M.A.
        • Dubuis E.D.
        • Chen S.
        • et al.
        Mechanistic link between diesel exhaust particles and respiratory reflexes.
        J Allergy Clin Immunol. 2017; ([Epub ahead of print])
        • Nemmar A.
        • Al-Salam S.
        • Dhanasekaran S.
        • Sudhadevi M.
        • Ali B.H.
        Pulmonary exposure to diesel exhaust particles promotes cerebral microvessel thrombosis: protective effect of a cysteine prodrug l-2-oxothiazolidine-4-carboxylic acid.
        Toxicology. 2009; 263: 84-92
        • Nemmar A.
        • Al-Salam S.
        • Zia S.
        • Marzouqi F.
        • Al-Dhaheri A.
        • Subramaniyan D.
        • et al.
        Contrasting actions of diesel exhaust particles on the pulmonary and cardiovascular systems and the effects of thymoquinone.
        Br J Pharmacol. 2011; 164: 1871-1882
        • Mutlu G.M.
        • Green D.
        • Bellmeyer A.
        • Baker C.M.
        • Burgess Z.
        • Rajamannan N.
        • et al.
        Ambient particulate matter accelerates coagulation via an IL-6-dependent pathway.
        J Clin Invest. 2007; 117: 2952-2961
        • Ohtoshi T.
        • Takizawa H.
        • Okazaki H.
        • Kawasaki S.
        • Takeuchi N.
        • Ohta K.
        • et al.
        Diesel exhaust particles stimulate human airway epithelial cells to produce cytokines relevant to airway inflammation in vitro.
        J Allergy Clin Immunol. 1998; 101: 778-785
        • Bayram H.
        • Devalia J.L.
        • Sapsford R.J.
        • Ohtoshi T.
        • Miyabara Y.
        • Sagai M.
        • et al.
        The effect of diesel exhaust particles on cell function and release of inflammatory mediators from human bronchial epithelial cells in vitro.
        Am J Respir Cell Mol Biol. 1998; 18: 441-448
        • Suwa T.
        • Hogg J.C.
        • Quinlan K.B.
        • Ohgami A.
        • Vincent R.
        • van Eeden S.F.
        Particulate air pollution induces progression of atherosclerosis.
        J Am Coll Cardiol. 2002; 39: 935-942
        • Ghio A.J.
        • Sobus J.R.
        • Pleil J.D.
        • Madden M.C.
        Controlled human exposures to diesel exhaust.
        Swiss Med Wkly. 2012; 142: w13597
        • Svartengren M.
        • Strand V.
        • Bylin G.
        • Jarup L.
        • Pershagen G.
        Short-term exposure to air pollution in a road tunnel enhances the asthmatic response to allergen.
        Eur Respir J. 2000; 15: 716-724
        • McCreanor J.
        • Cullinan P.
        • Nieuwenhuijsen M.J.
        • Stewart-Evans J.
        • Malliarou E.
        • Jarup L.
        • et al.
        Respiratory effects of exposure to diesel traffic in persons with asthma.
        N Engl J Med. 2007; 357: 2348-2358
        • Brauner E.V.
        • Moller P.
        • Barregard L.
        • Dragsted L.O.
        • Glasius M.
        • Wahlin P.
        • et al.
        Exposure to ambient concentrations of particulate air pollution does not influence vascular function or inflammatory pathways in young healthy individuals.
        Part Fibre Toxicol. 2008; 5: 13
        • Brauner E.V.
        • Mortensen J.
        • Moller P.
        • Bernard A.
        • Vinzents P.
        • Wahlin P.
        • et al.
        Effects of ambient air particulate exposure on blood-gas barrier permeability and lung function.
        Inhal Toxicol. 2009; 21: 38-47
        • Salvi S.
        • Blomberg A.
        • Rudell B.
        • Kelly F.
        • Sandstrom T.
        • Holgate S.T.
        • et al.
        Acute inflammatory responses in the airways and peripheral blood after short-term exposure to diesel exhaust in healthy human volunteers.
        Am J Respir Crit Care Med. 1999; 159: 702-709
        • Nightingale J.A.
        • Maggs R.
        • Cullinan P.
        • Donnelly L.E.
        • Rogers D.F.
        • Kinnersley R.
        • et al.
        Airway inflammation after controlled exposure to diesel exhaust particulates.
        Am J Respir Crit Care Med. 2000; 162: 161-166
        • Diaz-Sanchez D.
        • Tsien A.
        • Fleming J.
        • Saxon A.
        Combined diesel exhaust particulate and ragweed allergen challenge markedly enhances human in vivo nasal ragweed-specific IgE and skews cytokine production to a T helper cell 2-type pattern.
        J Immunol. 1997; 158: 2406-2413
        • Carlsten C.
        • Blomberg A.
        • Pui M.
        • Sandstrom T.
        • Wong S.W.
        • Alexis N.
        • et al.
        Diesel exhaust augments allergen-induced lower airway inflammation in allergic individuals: a controlled human exposure study.
        Thorax. 2016; 71: 35-44
        • Zhang X.
        • Hirota J.A.
        • Yang C.
        • Carlsten C.
        Effect of GST variants on lung function following diesel exhaust and allergen co-exposure in a controlled human crossover study.
        Free Radic Biol Med. 2016; 96: 385-391
        • Sava F.
        • MacNutt M.J.
        • Carlsten C.R.
        Nasal neurogenic inflammation markers increase after diesel exhaust inhalation in individuals with asthma.
        Am J Respir Crit Care Med. 2013; 188: 759-760
        • Kramer M.M.
        • Hirota J.A.
        • Sood A.
        • Teschke K.
        • Carlsten C.
        Airway and serum adipokines after allergen and diesel exposure in a controlled human crossover study of atopic adults.
        Transl Res. 2017; 182: 49-60
        • Hjermann I.
        • Velve Byre K.
        • Holme I.
        • Leren P.
        Effect of diet and smoking intervention on the incidence of coronary heart disease. Report from the Oslo Study Group of a randomised trial in healthy men.
        Lancet. 1981; 2: 1303-1310
        • Avol E.L.
        • Gauderman W.J.
        • Tan S.M.
        • London S.J.
        • Peters J.M.
        Respiratory effects of relocating to areas of differing air pollution levels.
        Am J Respir Crit Care Med. 2001; 164: 2067-2072
        • Bayer-Oglesby L.
        • Grize L.
        • Gassner M.
        • Takken-Sahli K.
        • Sennhauser F.H.
        • Neu U.
        • et al.
        Decline of ambient air pollution levels and improved respiratory health in Swiss children.
        Environ Health Perspect. 2005; 113: 1632-1637
        • Hart J.E.
        • Rimm E.B.
        • Rexrode K.M.
        • Laden F.
        Changes in traffic exposure and the risk of incident myocardial infarction and all-cause mortality.
        Epidemiology. 2013; 24: 734-742
        • Gan W.Q.
        • Tamburic L.
        • Davies H.W.
        • Demers P.A.
        • Koehoorn M.
        • Brauer M.
        Changes in residential proximity to road traffic and the risk of death from coronary heart disease.
        Epidemiology. 2010; 21: 642-649
        • Flannigan M.
        • Cantin A.S.
        • De Groot W.J.
        • Wotton M.
        • Newbery A.
        • Gowman L.M.
        Global wildland fire season severity in the 21st century.
        For Ecol Manage. 2013; 294: 54-61
        • Naeher L.P.
        • Brauer M.
        • Lipsett M.
        • Zelikoff J.T.
        • Simpson C.D.
        • Koenig J.Q.
        • et al.
        Woodsmoke health effects: a review.
        Inhal Toxicol. 2007; 19: 67-106
        • Akagi S.
        • Yokelson R.J.
        • Wiedinmyer C.
        • Alvarado M.
        • Reid J.
        • Karl T.
        • et al.
        Emission factors for open and domestic biomass burning for use in atmospheric models.
        Atmos Chem Phys. 2011; 11: 4039-4072
        • Youssouf H.
        • Liousse C.
        • Roblou L.
        • Assamoi E.M.
        • Salonen R.O.
        • Maesano C.
        • et al.
        Non-accidental health impacts of wildfire smoke.
        Int J Environ Res Public Health. 2014; 11: 11772-11804
        • Adetona O.
        • Reinhardt T.E.
        • Domitrovich J.
        • Broyles G.
        • Adetona A.M.
        • Kleinman M.T.
        • et al.
        Review of the health effects of wildland fire smoke on wildland firefighters and the public.
        Inhal Toxicol. 2016; 28: 95-139
        • Pavese G.
        • Alados-Arboledas L.
        • Cao J.
        • Satheesh S.K.
        Carbonaceous particles in the atmosphere: experimental and modelling issues.
        Adv Meteorol. 2014; 2014: 2
        • Borm P.J.
        • Robbins D.
        • Haubold S.
        • Kuhlbusch T.
        • Fissan H.
        • Donaldson K.
        • et al.
        The potential risks of nanomaterials: a review carried out for ECETOC.
        Particle Fibre Toxicol. 2006; 3: 11
        • Finlay S.E.
        • Moffat A.
        • Gazzard R.
        • Baker D.
        • Murray V.
        Health impacts of wildfires.
        PLoS Curr. 2012; 4
        • Reid C.E.
        • Brauer M.
        • Johnston F.H.
        • Jerrett M.
        • Balmes J.R.
        • Elliott C.T.
        Critical review of health impacts of wildfire smoke exposure.
        Environ Health Perspect. 2016; 124: 1334-1343
        • Rappold A.G.
        • Stone S.L.
        • Cascio W.E.
        • Neas L.M.
        • Kilaru V.J.
        • Carraway M.S.
        • 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
        • Morgan G.
        • Sheppeard V.
        • Khalaj B.
        • Ayyar A.
        • Lincoln D.
        • Jalaludin B.
        • et al.
        Effects of bushfire smoke on daily mortality and hospital admissions in Sydney, Australia.
        Epidemiology. 2010; 21: 47-55
        • Henderson S.B.
        • Brauer M.
        • Macnab Y.C.
        • Kennedy S.M.
        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
        • Delfino R.J.
        • Brummel S.
        • Wu J.
        • Stern H.
        • Ostro B.
        • Lipsett M.
        • et al.
        The relationship of respiratory and cardiovascular hospital admissions to the southern California wildfires of 2003.
        Occup Environ Med. 2009; 66: 189-197
        • Yao J.
        • Eyamie J.
        • Henderson S.B.
        Evaluation of a spatially resolved forest fire smoke model for population-based epidemiologic exposure assessment.
        J Expo Sci Environ Epidemiol. 2016; 26: 233-240
        • Padkao T.
        • Amput P.
        • Kluayhomthong S.
        • Jones C.U.
        Impacts of wildfire smog on lung volume and pulmonary function in healthy people. Phayao Research Conference.
        University of Phayao, Phayao, Thailand, 17-18 January 2013
        • Alman B.L.
        • Pfister G.
        • Hao H.
        • Stowell J.
        • Hu X.
        • Liu Y.
        • et al.
        The association of wildfire smoke with respiratory and cardiovascular emergency department visits in Colorado in 2012: a case crossover study.
        Environ Health. 2016; 15: 64
        • Liu J.C.
        • Pereira G.
        • Uhl S.A.
        • Bravo M.A.
        • Bell M.L.
        A systematic review of the physical health impacts from non-occupational exposure to wildfire smoke.
        Environ Res. 2015; 136: 120-132
        • Gaughan D.M.
        • Cox-Ganser J.M.
        • Enright P.L.
        • Castellan R.M.
        • Wagner G.R.
        • Hobbs G.R.
        • et al.
        Acute upper and lower respiratory effects in wildland firefighters.
        J Occup Environ Med. 2008; 50: 1019-1028
        • Swiston J.R.
        • Davidson W.
        • Attridge S.
        • Li G.T.
        • Brauer M.
        • van Eeden S.F.
        Wood smoke exposure induces a pulmonary and systemic inflammatory response in firefighters.
        Eur Respir J. 2008; 32: 129-138
        • Hejl A.M.
        • Adetona O.
        • Diaz-Sanchez D.
        • Carter J.D.
        • Commodore A.A.
        • Rathbun S.L.
        • et al.
        Inflammatory effects of woodsmoke exposure among wildland firefighters working at prescribed burns at the Savannah River Site, SC.
        J Occup Environ Hyg. 2013; 10: 173-180
        • Wegesser T.C.
        • Pinkerton K.E.
        • Last J.A.
        California wildfires of 2008: coarse and fine particulate matter toxicity.
        Environ Health Perspect. 2009; 117: 893-897
        • Wegesser T.C.
        • Franzi L.M.
        • Mitloehner F.M.
        • Eiguren-Fernandez A.
        • Last J.A.
        Lung antioxidant and cytokine responses to coarse and fine particulate matter from the great California wildfires of 2008.
        Inhal Toxicol. 2010; 22: 561-570
        • Myatt T.A.
        • Vincent M.S.
        • Kobzik L.
        • Naeher L.P.
        • MacIntosh D.L.
        • Suh H.
        Markers of inflammation in alveolar cells exposed to fine particulate matter from prescribed fires and urban air.
        J Occup Environ Med. 2011; 53: 1110-1114
        • Nakayama Wong L.S.
        • Aung H.H.
        • Lame M.W.
        • Wegesser T.C.
        • Wilson D.W.
        Fine particulate matter from urban ambient and wildfire sources from California's San Joaquin Valley initiate differential inflammatory, oxidative stress, and xenobiotic responses in human bronchial epithelial cells.
        Toxicol In Vitro. 2011; 25: 1895-1905
        • Franzi L.M.
        • Bratt J.M.
        • Williams K.M.
        • Last J.A.
        Why is particulate matter produced by wildfires toxic to lung macrophages?.
        Toxicol Appl Pharmacol. 2011; 257: 182-188
        • Tan W.C.
        • Qiu D.
        • Liam B.L.
        • Ng T.P.
        • Lee S.H.
        • van Eeden S.F.
        • et al.
        The human bone marrow response to acute air pollution caused by forest fires.
        Am J Respir Crit Care Med. 2000; 161: 1213-1217
        • van Eeden S.F.
        • Tan W.C.
        • Suwa T.
        • Mukae H.
        • Terashima T.
        • Fujii T.
        • et al.
        Cytokines involved in the systemic inflammatory response induced by exposure to particulate matter air pollutants (PM(10)).
        Am J Respir Crit Care Med. 2001; 164: 826-830
        • Ghio A.J.
        • Soukup J.M.
        • Case M.
        • Dailey L.A.
        • Richards J.
        • Berntsen J.
        • et al.
        Exposure to wood smoke particles produces inflammation in healthy volunteers.
        Occup Environ Med. 2012; 69: 170-175
        • Diffey B.L.
        An overview analysis of the time people spend outdoors.
        Br J Dermatol. 2011; 164: 848-854
        • Farmer S.A.
        • Nelin T.D.
        • Falvo M.J.
        • Wold L.E.
        Ambient and household air pollution: complex triggers of disease.
        Am J Physiol Heart Circ Physiol. 2014; 307: H467-H476
        • Mortimer K.
        • Gordon S.B.
        • Jindal S.K.
        • Accinelli R.A.
        • Balmes J.
        • Martin 2nd, W.J.
        Household air pollution is a major avoidable risk factor for cardiorespiratory disease.
        Chest. 2012; 142: 1308-1315
        • Salin J.T.
        • Salkinoja-Salonen M.
        • Salin P.J.
        • Nelo K.
        • Holma T.
        • Ohtonen P.
        • et al.
        Building-related symptoms are linked to the in vitro toxicity of indoor dust and airborne microbial propagules in schools: a cross-sectional study.
        Environ Res. 2017; 154: 234-239
        • de Koning H.W.
        • Smith K.R.
        • Last J.M.
        Biomass fuel combustion and health.
        Bull World Health Organ. 1985; 63: 11-26
        • Subramanian M.
        Global health: deadly dinners.
        Nature. 2014; 509: 548-551
        • Manuel J.
        The quest for fire: hazards of a daily struggle.
        Environ Health Perspect. 2003; 111: A28-A33
      1. United States Environmental Protection Agency. NAAQS table. Available at: https://www.epa.gov/criteria-air-pollutants/naaqs-table. Accessed January 26, 2018.

        • Johnston F.
        • Hanigan I.
        • Henderson S.
        • Morgan G.
        • Bowman D.
        Extreme air pollution events from bushfires and dust storms and their association with mortality in Sydney, Australia 1994-2007.
        Environ Res. 2011; 111: 811-816
        • Zhuang X.-G.
        • Wang Y.-X.
        • Zhu Z.-C.
        • Querol X.
        • Alastuey A.
        • Rodríguez S.
        • et al.
        Origin of PM10 Pollution Episodes in an Industrialized Mega-City in Central China.
        Aerosol Air Qual Res. 2014; 14: 338-346
      2. World Health Organization burden of disease from household air pollution for 2012. World Health Organization. Available at: http://www.who.int/phe/health_topics/outdoorair/databases/AAP_BoD_results_March2014.pdf. Accessed January 26, 2018.

        • Liu S.
        • Zhou Y.
        • Wang X.
        • Wang D.
        • Lu J.
        • Zheng J.
        • et al.
        Biomass fuels are the probable risk factor for chronic obstructive pulmonary disease in rural South China.
        Thorax. 2007; 62: 889-897
        • Fullerton D.G.
        • Bruce N.
        • Gordon S.B.
        Indoor air pollution from biomass fuel smoke is a major health concern in the developing world.
        Trans R Soc Trop Med Hyg. 2008; 102: 843-851
        • Karr C.J.
        • Demers P.A.
        • Koehoorn M.W.
        • Lencar C.C.
        • Tamburic L.
        • Brauer M.
        Influence of ambient air pollutant sources on clinical encounters for infant bronchiolitis.
        Am J Respir Crit Care Med. 2009; 180: 995-1001
        • Mishra V.
        Effect of indoor air pollution from biomass combustion on prevalence of asthma in the elderly.
        Environ Health Perspect. 2003; 111: 71-78
        • Rylance J.
        • Kankwatira A.
        • Nelson D.E.
        • Toh E.
        • Day R.B.
        • Lin H.
        • et al.
        Household air pollution and the lung microbiome of healthy adults in Malawi: a cross-sectional study.
        BMC Microbiol. 2016; 16: 182
        • Li C.
        • Zhihong H.
        • Wenlong L.
        • Xiaoyan L.
        • Qing C.
        • Wenzhi L.
        • et al.
        The nucleotide-binding oligomerization domain-like receptor family pyrin domain-containing 3 inflammasome regulates bronchial epithelial cell injury and proapoptosis after exposure to biomass fuel smoke.
        Am J Respir Cell Mol Biol. 2016; 55: 815-824
        • Krimmer D.
        • Ichimaru Y.
        • Burgess J.
        • Black J.
        • Oliver B.
        Exposure to biomass smoke extract enhances fibronectin release from fibroblasts.
        PLoS One. 2013; 8: e83938
        • Sussan T.E.
        • Ingole V.
        • Kim J.H.
        • McCormick S.
        • Negherbon J.
        • Fallica J.
        • et al.
        Source of biomass cooking fuel determines pulmonary response to household air pollution.
        Am J Respir Cell Mol Biol. 2014; 50: 538-548
        • Olloquequi J.
        • Silva O.R.
        Biomass smoke as a risk factor for chronic obstructive pulmonary disease: effects on innate immunity.
        Innate Immun. 2016; 22: 373-381
        • Dutta A.
        • Roychoudhury S.
        • Chowdhury S.
        • Ray M.R.
        Changes in sputum cytology, airway inflammation and oxidative stress due to chronic inhalation of biomass smoke during cooking in premenopausal rural Indian women.
        Int J Hyg Environ Health. 2013; 216: 301-308
        • Guarnieri M.J.
        • Diaz J.V.
        • Basu C.
        • Diaz A.
        • Pope D.
        • Smith K.R.
        • et al.
        Effects of woodsmoke exposure on airway inflammation in rural Guatemalan women.
        PLoS One. 2014; 9: e88455
        • Sehlstedt M.
        • Dove R.
        • Boman C.
        • Pagels J.
        • Swietlicki E.
        • Londahl J.
        • et al.
        Antioxidant airway responses following experimental exposure to wood smoke in man.
        Particle Fibre Toxicol. 2010; 7: 21
        • Burroughs Pena M.S.
        • Velazquez E.J.
        • Rivera J.D.
        • Alenezi F.
        • Wong C.
        • Grigsby M.
        • et al.
        Biomass fuel smoke exposure was associated with adverse cardiac remodeling and left ventricular dysfunction in Peru.
        Indoor Air. 2017; 27: 737-745
        • Caravedo M.A.
        • Herrera P.M.
        • Mongilardi N.
        • de Ferrari A.
        • Davila-Roman V.G.
        • Gilman R.H.
        • et al.
        Chronic exposure to biomass fuel smoke and markers of endothelial inflammation.
        Indoor Air. 2016; 26: 768-775
        • Dutta A.
        • Ray M.R.
        • Banerjee A.
        Systemic inflammatory changes and increased oxidative stress in rural Indian women cooking with biomass fuels.
        Toxicol Appl Pharmacol. 2012; 261: 255-262
        • Lee A.
        • Kinney P.
        • Chillrud S.
        • Jack D.
        A systematic review of innate immunomodulatory effects of household air pollution secondary to the burning of biomass fuels.
        Ann Global Health. 2015; 81: 368-374
        • Rylance J.
        • Fullerton D.G.
        • Scriven J.
        • Aljurayyan A.N.
        • Mzinza D.
        • Barrett S.
        • et al.
        Household air pollution causes dose-dependent inflammation and altered phagocytosis in human macrophages.
        Am J Respir Cell Mol Biol. 2015; 52: 584-593
        • Saha H.
        • Mukherjee B.
        • Bindhani B.
        • Ray M.R.
        Changes in RANKL and osteoprotegerin expression after chronic exposure to indoor air pollution as a result of cooking with biomass fuel.
        J Appl Toxicol. 2016; 36: 969-976
        • Muala A.
        • Rankin G.
        • Sehlstedt M.
        • Unosson J.
        • Bosson J.A.
        • Behndig A.
        • et al.
        Acute exposure to wood smoke from incomplete combustion—indications of cytotoxicity.
        Particle Fibre Toxicol. 2015; 12: 33
        • Dutta A.
        • Bhattacharya P.
        • Lahiri T.
        • Ray M.R.
        Immune cells and cardiovascular health in premenopausal women of rural India chronically exposed to biomass smoke during daily household cooking.
        Sci Total Environ. 2012; 438: 293-298
        • Cundale K.
        • Thomas R.
        • Malava J.K.
        • Havens D.
        • Mortimer K.
        • Conteh L.
        A health intervention or a kitchen appliance? Household costs and benefits of a cleaner burning biomass-fuelled cookstove in Malawi.
        Soc Sci Med. 2017; 183: 1-10
        • Mortimer K.
        • Ndamala C.B.
        • Naunje A.W.
        • Malava J.
        • Katundu C.
        • Weston W.
        • et al.
        A cleaner burning biomass-fuelled cookstove intervention to prevent pneumonia in children under 5 years old in rural Malawi (the Cooking and Pneumonia Study): a cluster randomised controlled trial.
        Lancet. 2017; 389: 167-175
        • Romieu I.
        • Riojas-Rodriguez H.
        • Marron-Mares A.T.
        • Schilmann A.
        • Perez-Padilla R.
        • Masera O.
        Improved biomass stove intervention in rural Mexico: impact on the respiratory health of women.
        Am J Respir Crit Care Med. 2009; 180: 649-656
        • McDonald E.
        • Cook D.
        • Newman T.
        • Griffith L.
        • Cox G.
        • Guyatt G.
        Effect of air filtration systems on asthma: a systematic review of randomized trials.
        Chest. 2002; 122: 1535-1542
        • Reisman R.E.
        • Mauriello P.M.
        • Davis G.B.
        • Georgitis J.W.
        • DeMasi J.M.
        A double-blind study of the effectiveness of a high-efficiency particulate air (HEPA) filter in the treatment of patients with perennial allergic rhinitis and asthma.
        J Allergy Clin Immunol. 1990; 85: 1050-1057