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Research Article

A mouse model of wildfire smoke-induced health effects: sex differences in acute and sustained effects of inhalation exposures

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Received 31 Oct 2023, Accepted 07 May 2024, Published online: 20 May 2024

References

  • Aguilera R, Hansen K, Gershunov A, Ilango SD, Sheridan P, Benmarhnia T. 2020. Respiratory hospitalizations and wildfire smoke: a spatiotemporal analysis of an extreme firestorm in San Diego County, California. Environ Epidemiol. 4(5):e114. doi: 10.1097/EE9.0000000000000114.
  • Antonini JM, Roberts JR, Yang HM, Barger MW, Ramsey D, Castranova V, Ma JY. 2000. Effect of silica inhalation on the pulmonary clearance of a bacterial pathogen in Fischer 344 rats. Lung. 178(6):341–350. doi: 10.1007/s004080000038.
  • Arredouani M, Yang Z, Ning Y, Qin G, Soininen R, Tryggvason K, Kobzik L. 2004. The scavenger receptor MARCO is required for lung defense against pneumococcal pneumonia and inhaled particles. J Exp Med. 200(2):267–272. doi: 10.1084/jem.20040731.
  • Arredouani MS, Yang Z, Imrich A, Ning Y, Qin G, Kobzik L. 2006. The macrophage scavenger receptor SR-AI/II and lung defense against pneumococci and particles. Am J Respir Cell Mol Biol. 35(4):474–478. doi: 10.1165/rcmb.2006-0128OC.
  • Barratt SL, Flower VA, Pauling JD, Millar AB. 2018. VEGF (Vascular Endothelial Growth Factor) and fibrotic lung disease. Int J Mol Sci. 19(5).
  • Bolger AM, Lohse M, Usadel B. 2014. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 30(15):2114–2120. doi: 10.1093/bioinformatics/btu170.
  • Casey JA, Kioumourtzoglou MA, Elser H, Walker D, Taylor S, Adams S, Aguilera R, Benmarhnia T, Catalano R. 2021. Wildfire particulate matter in Shasta County, California and respiratory and circulatory disease-related emergency department visits and mortality, 2013-2018. Environ Epidemiol. 5(1):e124. doi: 10.1097/EE9.0000000000000124.
  • Castranova V, Ma JY, Yang HM, Antonini JM, Butterworth L, Barger MW, Roberts J, Ma JK. 2001. Effect of exposure to diesel exhaust particles on the susceptibility of the lung to infection. Environ Health Perspect. 109(Suppl 4):609–612. doi: 10.1289/ehp.01109s4609.
  • D'Souza A, Hayman SR, Buadi F, Mauermann M, Lacy MQ, Gertz MA, Kyle RA, Kumar S, Greipp PR, Lust JA, et al. 2011. The utility of plasma vascular endothelial growth factor levels in the diagnosis and follow-up of patients with POEMS syndrome. Blood. 118(17):4663–4665. doi: 10.1182/blood-2011-06-362392.
  • Du X, Li C, Wang W, Huang Q, Wang J, Tong Z, Huang K, Chen Y, Yuan H, Lv Z, et al. 2020. IL-33 induced airways inflammation is partially dependent on IL-9. Cell Immunol. 352:104098.
  • Haikerwal A, Akram M, Sim MR, Meyer M, Abramson MJ, Dennekamp M. 2016. Fine particulate matter (PM2.5) exposure during a prolonged wildfire period and emergency department visits for asthma. Respirology. 21(1):88–94. doi: 10.1111/resp.12613.
  • Hamilton RF, Jr., Thakur SA, Holian A. 2008. Silica binding and toxicity in alveolar macrophages [Research Support, N.I.H., Extramural Review]. Free Radical Biol Med. 44(7):1246–1258.
  • Hamilton RF, Jr., Wu Z, Mitra S, Shaw PK, Holian A. 2013. Effect of MWCNT size, carboxylation, and purification on in vitro and in vivo toxicity, inflammation and lung pathology [Research Support, N.I.H., Extramural]. Part Fibre Toxicol. 10(1):57. doi: 10.1186/1743-8977-10-57.
  • Hargrove MM, Kim YH, King C, Wood CE, Gilmour MI, Dye JA, Gavett SH. 2019. Smoldering and flaming biomass wood smoke inhibit respiratory responses in mice. Inhal Toxicol. 31(6):236–247. doi: 10.1080/08958378.2019.1654046.
  • Helming L, Winter J, Gordon S. 2009. The scavenger receptor CD36 plays a role in cytokine-induced macrophage fusion [Research Support, Non-U.S. J Cell Sci. 122(Pt 4):453–459. doi: 10.1242/jcs.037200.
  • Henderson SB, Johnston FH. 2012. Measures of forest fire smoke exposure and their associations with respiratory health outcomes. Curr Opin Allergy Clin Immunol. 12(3):221–227. doi: 10.1097/ACI.0b013e328353351f.
  • Henry S, Ospina MB, Dennett L, Hicks A. 2021. Assessing the risk of respiratory-related healthcare visits associated with wildfire smoke exposure in children 0-18 years old: a systematic review. Int J Environ Res Public Health. 18(16): 8799.
  • Holm SM, Miller MD, Balmes JR. 2021. Health effects of wildfire smoke in children and public health tools: a narrative review. J Expo Sci Environ Epidemiol. 31(1):1–20. doi: 10.1038/s41370-020-00267-4.
  • Hutchinson JA, Vargo J, Milet M, French NHF, Billmire M, Johnson J, Hoshiko S. 2018. The San Diego 2007 wildfires and Medi-Cal emergency department presentations, inpatient hospitalizations, and outpatient visits: an observational study of smoke exposure periods and a bidirectional case-crossover analysis. PLoS Med. 15(7):e1002601. doi: 10.1371/journal.pmed.1002601.
  • Karkout R, Gaudreault V, Labrie L, Aldossary H, Azalde Garcia N, Shan J, Fixman ED. 2023. Female-specific enhancement of eosinophil recruitment and activation in a type 2 innate inflammation model in the lung. Clin Exp Immunol. 216(1):13-24.
  • Keeley JE, Syphard AD. 2016. Climate change and future fire regimes: examples from California. Geosciences. 6(3):37. doi: 10.3390/geosciences6030037.
  • Lacher SE, Johnson C, Jessop F, Holian A, Migliaccio CT. 2010. Murine pulmonary inflammation model: a comparative study of anesthesia and instillation methods. Inhal Toxicol. 22(1):77–83. doi: 10.3109/08958370902929969.
  • Landguth EL, Holden ZA, Graham J, Stark B, Mokhtari EB, Kaleczyc E, Anderson S, Urbanski S, Jolly M, Semmens EO, et al. 2020. The delayed effect of wildfire season particulate matter on subsequent influenza season in a mountain west region of the USA. Environ Int. 139:105668.
  • Lee CG, Link H, Baluk P, Homer RJ, Chapoval S, Bhandari V, Kang MJ, Cohn L, Kim YK, McDonald DM, et al. 2004. Vascular endothelial growth factor (VEGF) induces remodeling and enhances TH2-mediated sensitization and inflammation in the lung. Nat Med. 10(10):1095–1103. doi: 10.1038/nm1105.
  • Lee CG, Ma B, Takyar S, Ahangari F, Delacruz C, He CH, Elias JA. 2011. Studies of vascular endothelial growth factor in asthma and chronic obstructive pulmonary disease. Proc Am Thorac Soc. 8(6):512–515. doi: 10.1513/pats.201102-018MW.
  • Leibel S, Nguyen M, Brick W, Parker J, Ilango S, Aguilera R, Gershunov A, Benmarhnia T. 2020. Increase in pediatric respiratory visits associated with Santa Ana wind-driven wildfire smoke and PM2.5 levels in San Diego County. Ann Am Thorac Soc. 17(3):313–320.
  • Lescoat A, Ballerie A, Lelong M, Augagneur Y, Morzadec C, Jouneau S, Jégo P, Fardel O, Vernhet L, Lecureur V. 2020. Crystalline silica impairs efferocytosis abilities of human and mouse macrophages: implication for silica-associated systemic sclerosis. Front Immunol. 11:219. doi: 10.3389/fimmu.2020.00219.
  • Levings DC, Lacher SE, Palacios-Moreno J, Slattery M. 2021. Transcriptional reprogramming by oxidative stress occurs within a predefined chromatin accessibility landscape. Free Radic Biol Med. 171:319–331. doi: 10.1016/j.freeradbiomed.2021.05.016.
  • Love MI, Huber W, Anders S. 2014. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15(12):550. doi: 10.1186/s13059-014-0550-8.
  • Martin RJ, Wexler RB, Day BJ, Harbeck RJ, Pinkerton KE, Chu HW. 2006. Interaction between cigarette smoke and mycoplasma infection: a murine model. Copd. 3(1):3–8.
  • McDonald JD, Harrod KS, Seagrave J, Seilkop SK, Mauderly JL. 2004. Effects of low sulfur fuel and a catalyzed particle trap on the composition and toxicity of diesel emissions. Environ Health Perspect. 112(13):1307–1312. doi: 10.1289/ehp.7059.
  • Migliaccio CT, Kobos E, King QO, Porter V, Jessop F, Ward T. 2013. Adverse effects of wood smoke PM(2.5) exposure on macrophage functions [Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov’t]. Inhalation Toxicol. 25(2):67–76. doi: 10.3109/08958378.2012.756086.
  • Mishra V, Retherford RD. 1997. Cooking smoke increases the risk of acute respiratory infection in children. Natl Fam Health Surv Bull. (8):1–4.
  • Morris K, Morgenlander M, Coulehan JL, Gahagen S, Arena VC. 1990. Wood-burning stoves and lower respiratory tract infection in American Indian children. Am J Dis Child. 144(1):105–108.
  • O'Dell K, Hornbrook RS, Permar W, Levin EJT, Garofalo LA, Apel EC, Blake NJ, Jarnot A, Pothier MA, Farmer DK, et al. 2020. Hazardous air pollutants in fresh and aged western us wildfire smoke and implications for long-term exposure. Environ Sci Technol. 54(19):11838–11847.
  • Orr A, A L Migliaccio C, Buford M, Ballou S, Migliaccio CT. 2020. Sustained effects on lung function in community members following exposure to hazardous PM2.5 levels from wildfire smoke. Toxics. 8(3):53. doi: 10.3390/toxics8030053.
  • Patro R, Duggal G, Love MI, Irizarry RA, Kingsford C. 2017. Salmon provides fast and bias-aware quantification of transcript expression. Nat Methods. 14(4):417–419. doi: 10.1038/nmeth.4197.
  • Rebuli ME, Speen AM, Martin EM, Addo KA, Pawlak EA, Glista-Baker E, Robinette C, Zhou H, Noah TL, Jaspers I. 2019. 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. doi: 10.1164/rccm.201807-1287OC.
  • Reid CE, Jerrett M, Tager IB, Petersen ML, Mann JK, Balmes JR. 2016. Differential respiratory health effects from the 2008 northern California wildfires: a spatiotemporal approach. Environ Res. 150:227–235. doi: 10.1016/j.envres.2016.06.012.
  • Reid CE, Maestas MM. 2019. Wildfire smoke exposure under climate change: impact on respiratory health of affected communities. Curr Opin Pulm Med. 25(2):179–187. doi: 10.1097/MCP.0000000000000552.
  • Ross MH, Murray J. 2004. Occupational respiratory disease in mining. Occup Med (Lond). 54(5):304–310.
  • Rossiello MR, Szema A. 2019. Health effects of climate change-induced wildfires and heatwaves. Cureus. 11(5):e4771. doi: 10.7759/cureus.4771.
  • Saikumar Jayalatha AK, Hesse L, Ketelaar ME, Koppelman GH, Nawijn MC. 2021. The central role of IL-33/IL-1RL1 pathway in asthma: from pathogenesis to intervention. Pharmacol Ther. 225:107847. doi: 10.1016/j.pharmthera.2021.107847.
  • Schoennagel T, Balch JK, Brenkert-Smith H, Dennison PE, Harvey BJ, Krawchuk MA, Mietkiewicz N, Morgan P, Moritz MA, Rasker R, et al. 2017. Adapt to more wildfire in western North American forests as climate changes. Proc Natl Acad Sci USA. 114(18):4582–4590. doi: 10.1073/pnas.1617464114.
  • Sjöberg LC, Nilsson AZ, Lei Y, Gregory JA, Adner M, Nilsson GP. 2017. Interleukin 33 exacerbates antigen driven airway hyperresponsiveness, inflammation and remodeling in a mouse model of asthma. Sci Rep. 7(1):4219. doi: 10.1038/s41598-017-03674-0.
  • Smith KR, Samet JM, Romieu I, Bruce N. 2000. Indoor air pollution in developing countries and acute lower respiratory infections in children. Thorax. 55(6):518–532. doi: 10.1136/thorax.55.6.518.
  • Spracklen DV, Mickley LJ, Logan JA, Hudman RC, Yevich R, Flannigan MD, Westerling AL. 2009. Impacts of climate change from 2000 to 2050 on wildfire activity and carbonaceous aerosol concentrations in the western United States. J Geophys Res. 114:D20. doi: 10.1029/2008JD010966.
  • Stone KC, Mercer RR, Gehr P, Stockstill B, Crapo JD. 1992. Allometric relationships of cell numbers and size in the mammalian lung. Am J Respir Cell Mol Biol. 6(2):235–243. doi: 10.1165/ajrcmb/6.2.235.
  • Tajbakhsh A, Gheibihayat SM, Mortazavi D, Medhati P, Rostami B, Savardashtaki A, Momtazi-Borojeni AA. 2021. The effect of cigarette smoke exposure on efferocytosis in chronic obstructive pulmonary disease; molecular mechanisms and treatment opportunities. COPD. 18(6):723–736. doi: 10.1080/15412555.2021.1978419.
  • Torres-Duque C, Maldonado D, Pérez-Padilla R, Ezzati M, Viegi G, Forum of International Respiratory Studies (FIRS) Task Force on Health Effects of Biomass Exposure. 2008. Biomass fuels and respiratory diseases: a review of the evidence. Proc Am Thorac Soc. 5(5):577–590. doi: 10.1513/pats.200707-100RP.
  • USGCRP. 2017. Climate science special report: fourth national climate assessment, vol. 1. Washington, DC: USGCRP.
  • Wang X, Cunha C, Grau MS, Robertson SJ, Lacerda JF, Campos A, Jr., Lagrou K, Maertens J, Best SM, Carvalho A, et al. 2022. MAVS expression in alveolar macrophages is essential for host resistance against Aspergillus fumigatus. J Immunol. 209(2):346–353. doi: 10.4049/jimmunol.2100759.
  • Ward TJ, Lincoln E. 2006. Concentrations of PM(2.5)-associated OC, EC, and PCDD/Fs measured during the 2003 wildfire season in Missoula, Montana. Environ Monit Assess. 115(1-3):39–50. doi: 10.1007/s10661-006-5252-6.
  • Wells SM, Buford MC, Braseth SN, Hutchison JD, Holian A. 2008. Acute inhalation exposure to vaporized methamphetamine causes lung injury in mice. Inhal Toxicol. 20(9):829–838. doi: 10.1080/08958370801895121.
  • Wells SM, Buford MC, Migliaccio CT, Holian A. 2009. Elevated asymmetric dimethylarginine alters lung function and induces collagen deposition in mice. Am J Respir Cell Mol Biol. 40(2):179–188. doi: 10.1165/rcmb.2008-0148OC.
  • WMO. 2020. WMO statement on the state of the global climate in 2019. Geneva: WMO.
  • Xia J, Zhao J, Shang J, Li M, Zeng Z, Zhao J, Wang J, Xu Y, Xie J. 2015. Increased IL-33 expression in chronic obstructive pulmonary disease. Am J Physiol Lung Cellular Molecul Physiol. 308(7):L619–627.
  • Zajkowska M, Lubowicka E, Fiedorowicz W, Szmitkowski M, Jamiolkowski J, Lawicki S. 2019. Human plasma levels of VEGF-A, VEGF-C, VEGF-D, their soluble receptor - VEGFR-2 and applicability of these parameters as tumor markers in the diagnostics of breast cancer. Pathol Oncol Res. 25(4):1477–1486.
  • Zelikoff JT, Chen LC, Cohen MD, Schlesinger RB. 2002. The toxicology of inhaled woodsmoke. J Toxicol Environ Health B Crit Rev. 5(3):269–282.
  • Zhang Q, Fang W, Ma L, Wang ZD, Yang YM, Lu YQ. 2018. VEGF levels in plasma in relation to metabolic control, inflammation, and microvascular complications in type-2 diabetes: A cohort study. Medicine (Baltimore). 97(15):e0415. doi: 10.1097/MD.0000000000010415.
  • Zhao H, Moarbes V, Gaudreault V, Shan J, Aldossary H, Cyr L, Fixman ED. 2019. Sex differences in IL-33-induced STAT6-dependent type 2 airway inflammation. Front Immunol. 10:859. doi: 10.3389/fimmu.2019.00859.

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