Controlled human wood smoke exposure: oxidative stress, inflammation and microvascular function

Lykke Forchhammer, Peter Møller, Ingunn Skogstad Riddervold, Jakob Bønløkke, Andreas Massling, Torben Sigsgaard, Steffen Loft, Lykke Forchhammer, Peter Møller, Ingunn Skogstad Riddervold, Jakob Bønløkke, Andreas Massling, Torben Sigsgaard, Steffen Loft

Abstract

Background: Exposure to wood smoke is associated with respiratory symptoms, whereas knowledge on systemic effects is limited. We investigated effects on systemic inflammation, oxidative stress and microvascular function (MVF) after controlled wood smoke exposure.

Methods: In a randomised, double-blinded, cross-over study 20 non-smoking atopic subjects were exposed at rest to 14, 220, or 354 μg/m3 of particles from a well-burning modern wood stove for 3 h in a climate controlled chamber with 2 week intervals. We investigated the level of oxidatively damaged DNA, inflammatory markers and adhesion molecules before and 0, 6 and 20 h after exposure. Six h after exposure we measured MVF non-invasively by digital peripheral artery tonometry following arm ischemia.

Results: The MVF score was unaltered after inhalation of clean air (1.58 ± 0.07; mean ± SEM), low (1.51 ± 0.07) or high (1.61 ± 0.09) concentrations of wood smoke particles in atopic subjects, whereas unexposed non-atopic subjects had higher score (1.91 ± 0.09). The level of oxidatively damaged DNA, mRNA of ITGAL, CCL2, TNF, IL6, IL8, HMOX1, and OGG1 and surface marker molecules ICAM1, ITGAL and L-selectin in peripheral blood mononuclear cells were not affected by inhalation of wood smoke particles.

Conclusions: Exposure to wood smoke had no effect on markers of oxidative stress, DNA damage, cell adhesion, cytokines or MVF in atopic subjects.

Figures

Figure 1
Figure 1
Mean mobility particle number size distribution obtained during the sessions of different exposure types representing two size modes of particulate matter in the climate chamber. The data are from [23] and the error bars are SEM.
Figure 2
Figure 2
Microvascular function (MVF) score 6 h after termination of each of the different exposures (n = 20). Each symbol corresponds to a person, whereas the bars represent the mean of each exposure. The mean ± SEM were 1.61 ± 0.09, 1.51 ± 0.09, 1.55 ± 0.08 in the subjects exposed to clean air, low and high content of wood smoke particles, respectively.
Figure 3
Figure 3
Level of DNA damage in PBMCs measured 4 times during 24 h after each of the different wood smoke exposure scenarios (n = 20). The figure is divided in three sections. The dark grey section depicts the FPG sensitive sites. The light grey section depicts the EndoIII sensitive sites and the white section depicts the SB.

References

    1. Kocbach BA, Pagels J, Yttri KE, Barregard L, Sallsten G, Schwarze PE, Boman C. Health effects of residential wood smoke particles: the importance of combustion conditions and physicochemical particle properties. Part Fibre Toxicol. 2009;6:29. doi: 10.1186/1743-8977-6-29.
    1. Moller P, Loft S. Oxidative damage to DNA and lipids as biomarkers of exposure to air pollution. Environ Health Perspect. 2010;118:1126–1136. doi: 10.1289/ehp.0901725.
    1. Brook RD, Rajagopalan S, Pope CA III, Brook JR, Bhatnagar A, Diez-Roux AV, Holguin F, Hong Y, Luepker RV, Mittleman MA, Peters A, Siscovick D, Smith SC Jr, Whitsel L, Kaufman JD. Particulate matter air pollution and cardiovascular disease: an update to the scientific statement from the American Heart Association. Circulation. 2010;121:2331–2378. doi: 10.1161/CIR.0b013e3181dbece1.
    1. Ruckerl R, Schneider A, Breitner S, Cyrys J, Peters A. Health effects of particulate air pollution: a review of epidemiological evidence. Inhal Toxicol. 2011;23:555–592. doi: 10.3109/08958378.2011.593587.
    1. 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. 2008;44:1689–1699. doi: 10.1016/j.freeradbiomed.2008.01.028.
    1. Mills NL, Donaldson K, Hadoke PW, Boon NA, MacNee W, Cassee FR, Sandstrom T, Blomberg A, Newby DE. Adverse cardiovascular effects of air pollution. Nat Clin Pract Cardiovasc Med. 2009;6:36–44. doi: 10.1038/ncpcardio1399.
    1. Moller P, Jacobsen NR, Folkmann JK, Danielsen PH, Mikkelsen L, Hemmingsen JG, Vesterdal LK, Forchhammer L, Wallin H, Loft S. Role of oxidative damage in toxicity of particulates. Free Radic Res. 2010;44:1–46. doi: 10.3109/10715760903300691.
    1. Liu PL, Chen YL, Chen YH, Lin SJ, Kou YR. Wood smoke extract induces oxidative stress-mediated caspase-independent apoptosis in human lung endothelial cells: role of AIF and EndoG. Am J Physiol Lung Cell Mol Physiol. 2005;289:L739–L749. doi: 10.1152/ajplung.00099.2005.
    1. Danielsen PH, Loft S, Kocbach A, Schwarze PE, Moller P. Oxidative damage to DNA and repair induced by Norwegian wood smoke particles in human A549 and THP-1 cell lines. Mutat Res. 2009;674:116–122.
    1. Danielsen PH, Moller P, Jensen KA, Sharma AK, Wallin H, Bossi R, Autrup H, Molhave L, Ravanat JL, Briede JJ, De Kok TM, Loft S. Oxidative stress, DNA damage, and inflammation induced by ambient air and wood smoke particulate matter in human A549 and THP-1 cell lines. Chem Res Toxicol. 2011;24:168–184. doi: 10.1021/tx100407m.
    1. Kocbach A, Namork E, Schwarze PE. Pro-inflammatory potential of wood smoke and traffic-derived particles in a monocytic cell line. Toxicology. 2008;247:123–132. doi: 10.1016/j.tox.2008.02.014.
    1. Barregard L, Sallsten G, Gustafson P, Andersson L, Johansson L, Basu S, Stigendal L. Experimental exposure to wood-smoke particles in healthy humans: effects on markers of inflammation, coagulation, and lipid peroxidation. Inhal Toxicol. 2006;18:845–853. doi: 10.1080/08958370600685798.
    1. Barregard L, Sallsten G, Andersson L, Almstrand AC, Gustafson P, Andersson M, Olin AC. Experimental exposure to wood smoke: effects on airway inflammation and oxidative stress. Occup Environ Med. 2008;65:319–324. doi: 10.1136/oem.2006.032458.
    1. Sallsten G, Gustafson P, Johansson L, Johannesson S, Molnar P, Strandberg B, Tullin C, Barregard L. Experimental wood smoke exposure in humans. Inhal Toxicol. 2006;18:855–864. doi: 10.1080/08958370600822391.
    1. Danielsen PH, Bräuner EV, Barregard L, Sallsten G, Wallin M, Olinski R, Rozalski R, Moller P, Loft S. Oxidatively damaged DNA and its repair after experimental exposure to wood smoke in healthy humans. Mutat Res. 2008;642:37–42. doi: 10.1016/j.mrfmmm.2008.04.001.
    1. Sehlstedt M, Dove R, Boman C, Pagels J, Swietlicki E, Londahl J, Westerholm R, Bosson J, Barath S, Behndig AF, Pourazar J, Sandstrom T, Mudway IS, Blomberg A. Antioxidant airway responses following experimental exposure to wood smoke in man. Part Fibre Toxicol. 2010;7:21. doi: 10.1186/1743-8977-7-21.
    1. Hersoug LG, Husemoen LL, Thomsen SF, Sigsgaard T, Thuesen BH, Linneberg A. Association of indoor air pollution with rhinitis symptoms, atopy and nitric oxide levels in exhaled air. Int Arch Allergy Immunol. 2010;153:403–412. doi: 10.1159/000316352.
    1. Yu O, Sheppard L, Lumley T, Koenig JQ, Shapiro GG. Effects of ambient air pollution on symptoms of asthma in Seattle-area children enrolled in the CAMP study. Environ Health Perspect. 2000;108:1209–1214. doi: 10.1289/ehp.001081209.
    1. Moller P, Mikkelsen L, Vesterdal LK, Folkmann JK, Forchhammer L, Roursgaard M, Danielsen PH, Loft S. Hazard identification of particulate matter on vasomotor dysfunction and progression of atherosclerosis. Crit Rev Toxicol. 2011;41:339–368. doi: 10.3109/10408444.2010.533152.
    1. Bräuner EV, Forchhammer L, Moller P, Barregard L, Gunnarsen L, Afshari A, Wahlin P, Glasius M, Dragsted LO, Basu S, Raaschou-Nielsen O, Loft S. Indoor particles affect vascular function in the aged: an air filtration-based intervention study. Am J Respir Crit Care Med. 2008;177:419–425.
    1. Allen RW, Carlsten C, Karlen B, Leckie S, Eeden S, Vedal S, Wong I, Brauer M. An air filter intervention study of endothelial function among healthy adults in a woodsmoke-impacted community. Am J Respir Crit Care Med. 2011;183:1222–1230. doi: 10.1164/rccm.201010-1572OC.
    1. Bräuner EV, Moller P, Barregard L, Dragsted LO, Glasius M, Wahlin P, Vinzents P, Raaschou-Nielsen O, Loft S. 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. doi: 10.1186/1743-8977-5-13.
    1. Riddervold IS, Bonlokke JH, Molhave L, Massling A, Jensen B, Gronborg TK, Bossi R, Forchhammer L, Kjaergaard SK, Sigsgaard T. Wood smoke in a controlled exposure experiment with human volunteers. Inhal Toxicol. 2011;23:277–288. doi: 10.3109/08958378.2011.567401.
    1. Forchhammer L, Bräuner EV, Folkmann JK, Danielsen PH, Nielsen C, Jensen A, Loft S, Friis G, Moller P. Variation in assessment of oxidatively damaged DNA in mononuclear blood cells by the comet assay with visual scoring. Mutagenesis. 2008;23:223–231. doi: 10.1093/mutage/gen006.
    1. Londahl J, Pagels J, Boman C, Swietlicki E, Massling A, Rissler J, Blomberg A, Bohgard M, Sandstrom T. Deposition of biomass combustion aerosol particles in the human respiratory tract. Inhal Toxicol. 2008;20:923–933. doi: 10.1080/08958370802087124.
    1. Yildiz P, Oflaz H, Cine N, Genchallac H, Erginel-Unaltuna N, Yildiz A, Yilmaz V. Endothelial dysfunction in patients with asthma: the role of polymorphisms of ACE and endothelial NOS genes. J Asthma. 2004;41:159–166. doi: 10.1081/JAS-120026073.
    1. Rubinshtein R, Kuvin JT, Soffler M, Lennon RJ, Lavi S, Nelson RE, Pumper GM, Lerman LO, Lerman A. Assessment of endothelial function by non-invasive peripheral arterial tonometry predicts late cardiovascular adverse events. Eur Heart J. 2010;31:1142–1148. doi: 10.1093/eurheartj/ehq010.
    1. Pope CA III, Hansen JC, Kuprov R, Sanders MD, Anderson MN, Eatough DJ. Vascular function and short-term exposure to fine particulate air pollution. J Air Waste Manag Assoc. 2011;61:858–863. doi: 10.3155/1047-3289.61.8.858.
    1. Bonetti PO, Lardi E, Geissmann C, Kuhn MU, Bruesch H, Reinhart WH. Effect of brief secondhand smoke exposure on endothelial function and circulating markers of inflammation. Atherosclerosis. 2011;215:218–222. doi: 10.1016/j.atherosclerosis.2010.12.011.
    1. Mills NL, Tornqvist H, Robinson SD, Gonzalez M, Darnley K, MacNee W, Boon NA, Donaldson K, Blomberg A, Sandstrom T, Newby DE. Diesel exhaust inhalation causes vascular dysfunction and impaired endogenous fibrinolysis. Circulation. 2005;112:3930–3936. doi: 10.1161/CIRCULATIONAHA.105.588962.
    1. Barath S, Mills NL, Lundback M, Tornqvist H, Lucking AJ, Langrish JP, Soderberg S, Boman C, Westerholm R, Londahl J, Donaldson K, Mudway IS, Sandstrom T, Newby DE, Blomberg A. Impaired vascular function after exposure to diesel exhaust generated at urban transient running conditions. Part Fibre Toxicol. 2010;7:19. doi: 10.1186/1743-8977-7-19.
    1. Langrish JP, Lundback M, Barath S, Soderberg S, Mills NL, Newby DE, Sandstrom T, Blomberg A. Exposure to nitrogen dioxide is not associated with vascular dysfunction in man. Inhal Toxicol. 2010;22:192–198. doi: 10.3109/08958370903144105.
    1. Mills NL, Finlayson AE, Gonzalez MC, Tornqvist H, Barath S, Vink E, Goudie C, Langrish JP, Soderberg S, Boon NA, Fox KA, Donaldson K, Sandstrom T, Blomberg A, Newby DE. Diesel exhaust inhalation does not affect heart rhythm or heart rate variability. Heart. 2011;97:544–550. doi: 10.1136/hrt.2010.199042.
    1. Londahl J, Massling A, Bräuner EV, Swietlicki E, Ketzel M, Pagels J, Loft S. Experimentally determined human respiratory tract deposition of airborne particles at a busy street. Environ Sci Technol. 2009;43:4659–4664. doi: 10.1021/es803029b.
    1. Libby P. Atherosclerosis: disease biology affecting the coronary vasculature. Am J Cardiol. 2006;98:3Q–9Q.
    1. Forchhammer L, Loft S, Roursgaard M, Cao Y, Riddervold IS, Sigsgaard T, Moller P. Expression of adhesion molecules, monocyte interactions and oxidative stress in human endothelial cells exposed to wood smoke and diesel exhaust particulate matter. Toxicol Lett. 2012;209:121–128. doi: 10.1016/j.toxlet.2011.12.003.
    1. Frampton MW, Stewart JC, Oberdorster G, Morrow PE, Chalupa D, Pietropaoli AP, Frasier LM, Speers DM, Cox C, Huang LS, Utell MJ. Inhalation of ultrafine particles alters blood leukocyte expression of adhesion molecules in humans. Environ Health Perspect. 2006;114:51–58. doi: 10.1289/ehp.7962.
    1. Banerjee A, Mondal NK, Das D, Ray MR. Neutrophilic Inflammatory Response and Oxidative Stress in Premenopausal Women Chronically Exposed to Indoor Air Pollution from Biomass Burning. Inflammation. 2011. doi: 10.1007/s10753-011-9360-2.
    1. Ghio AJ, Soukup JM, Case M, Dailey LA, Richards J, Berntsen J, Devlin RB, Stone S, Rappold A. Exposure to wood smoke particles produces inflammation in healthy volunteers. Occup Environ Med. 2011. doi:oem.2011.065276 [pii];10.1136/oem.2011.065276.
    1. Sehlstedt M, Behndig AF, Boman C, Blomberg A, Sandstrom T, Pourazar J. Airway inflammatory response to diesel exhaust generated at urban cycle running conditions. Inhal Toxicol. 2010;22:1144–1150. doi: 10.3109/08958378.2010.529181.
    1. Sällsten G, Gustafson P, Johansson L, Johannesson S, Molnar P, Strandberg B, Tullin C, Barregard L. Experimental wood smoke exposure in humans. Inhal Toxicol. 2006;18:855–864. doi: 10.1080/08958370600822391.
    1. Danielsen PH, Loft S, Jacobsen NR, Jensen KA, Autrup H, Ravanat JL, Wallin H, Moller P. Oxidative stress, inflammation, and DNA damage in rats after intratracheal instillation or oral exposure to ambient air and wood smoke particulate matter. Toxicol Sci. 2010;118:574–585. doi: 10.1093/toxsci/kfq290.
    1. Avogbe P, Ayi-Fanou L, Autrup H, Loftm S, Fayomi B, Sanni A, Vinzents P, Møller P. Ultrafine particulate matter and high-level benzene urban air pollution in relation to oxidative DNA damage. Carcinogenesis. 2005;26:613–620.
    1. Vinzents P, Møller P, Sørensen M, Knudsen LE, Hertel O, Schibye B, Loft S. Personal exposure to ultrafine particles and oxidative DNA damage. Environ Health Perspect. 2005;113:1485–1490. doi: 10.1289/ehp.7562.
    1. Bräuner EV, Forchhammer L, Moller P, Simonsen J, Glasius M, Wahlin P, Raaschou-Nielsen O, Loft S. Exposure to ultrafine particles from ambient air and oxidative stress-induced DNA damage. Environ Health Perspect. 2007;115:1177–1182. doi: 10.1289/ehp.9984.
    1. Moller P. Assessment of reference values for DNA damage detected by the comet assay in human blood cell DNA. Mutat Res. 2006;612:84–104. doi: 10.1016/j.mrrev.2005.10.001.
    1. Danielsen PH, Risom L, Wallin H, Autrup H, Vogel U, Loft S, Moller P. DNA damage in rats after a single oral exposure to diesel exhaust particles. Mutat Res. 2008;637:49–55. doi: 10.1016/j.mrfmmm.2007.06.011.
    1. Mills NL, Miller MR, Lucking AJ, Beveridge J, Flint L, Boere AJ, Fokkens PH, Boon NA, Sandstrom T, Blomberg A, Duffin R, Donaldson K, Hadoke PW, Cassee FR, Newby DE. Combustion-derived nanoparticulate induces the adverse vascular effects of diesel exhaust inhalation. Eur Heart J. 2011;32:2660–2671. doi: 10.1093/eurheartj/ehr195.
    1. Patvardhan EA, Heffernan KS, Ruan JM, Soffler MI, Karas RH, Kuvin JT. Assessment of vascular endothelial function with peripheral arterial tonometry: information at your fingertips? Cardiol Rev. 2010;18:20–28. doi: 10.1097/CRD.0b013e3181c46a15.
    1. Moller P, Friis G, Christensen PH, Risom L, Plesner G, Kjaersgaard J, Vinzents P, Loft S, Jensen A, Tved M. Intra-laboratory comet assay sample scoring exercise for determination of formamidopyrimidine DNA glycosylase sites in human mononuclear blood cell DNA. Free Radic Res. 2004;38:1207–1214. doi: 10.1080/10715760400016824.
    1. Forchhammer L, Johansson C, Loft S, Moller L, Godschalk RW, Langie SA, Jones GD, Kwok RW, Collins AR, Azqueta A, Phillips DH, Sozeri O, Stepnik M, Palus J, Vogel U, Wallin H, Routledge MN, Handforth C, Allione A, Matullo G, Teixeira JP, Costa S, Riso P, Porrini M, Moller P. Variation in the measurement of DNA damage by comet assay measured by the ECVAG inter-laboratory validation trial. Mutagenesis. 2010;25:113–123. doi: 10.1093/mutage/gep048.
    1. Johansson C, Moller P, Forchhammer L, Loft S, Godschalk RW, Langie SA, Lumeij S, Jones GD, Kwok RW, Azqueta A, Phillips DH, Sozeri O, Routledge MN, Charlton AJ, Riso P, Porrini M, Allione A, Matullo G, Palus J, Stepnik M, Collins AR, Moller L. An ECVAG trial on assessment of oxidative damage to DNA measured by the comet assay. Mutagenesis. 2010;25:125–132. doi: 10.1093/mutage/gep055.

Source: PubMed

3
S'abonner