Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Effects of particulate matter gamma radiation on oxidative stress biomarkers in COPD patients

Journal of Exposure Science & Environmental Epidemiology volume 31, pages 727–735 (2021)Cite this article

Abstract

Inhalation of particulate matter (PM) radioactivity is an important pathway of ionizing radiation exposure. We investigated the associations between short-term exposures to PM gamma radioactivity with oxidative stress in COPD patients. Urinary concentrations of 8-hydroxy-2’-deoxyguanosine (8-OHdG) and malondialdehyde (MDA) of 81 COPD patients from Eastern Massachusetts were measured 1–4 times during 2012–2014. Daily ambient and indoor PM gamma activities (gamma-3 through gamma-9) were calculated based on EPA RadNet data and indoor–outdoor infiltration ratios. Linear mixed-effects models were used to examine the associations between biomarkers with PM gamma activities for moving averages from urine collection day to 7 days before. Our results indicate that ambient and indoor PM gamma activities were positively associated with 8-OHdG, with stronger effects for exposure windows closer to urine collection day. For per interquartile range increase in indoor PM gamma activities averaged over urine collection day and 1 day before, 8-OHdG increased from 3.41% (95% CI: −0.88, 7.88) to 8.87% (95% CI: 2.98, 15.1), adjusted for indoor black carbon. For MDA, the timing of greatest effects across the exposure week varied but was nearly all positive. These findings provide insight into the toxigenic properties associated with PM radioactivity and suggest that these exposures promote systemic oxidative stress.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Senior RM, Anthonisen NR 1998. Chronic obstructive pulmonary disease (COPD). Am J Respir Crit Care Med.1998;157:S139–47.

  2. GBD 2015 DALYs and HALE Collaborators. Global, regional, and national incidence, prevalence, and years lived with disability for 310 diseases and injuries, 1990-2015: a systematic analysis for the Global Burden of Disease Study 2015. Lancet. 2016;388:1545–602.

    Article  Google Scholar 

  3. Hurst JR, Elborn JS, De Soyza A. COPD-bronchiectasis overlap syndrome. Eur Respir J. 2015;45:310–3.

    Article  Google Scholar 

  4. Kochanek KD, Murphy SL, Xu J, Arias E Mortality in the united states, 2016. NCHS Data Brief 293. Centers for Disease Control and Prevention, National Center for Health Statistics, 2017.

  5. Therond P. Oxidative stress and damages to biomolecules (lipids, proteins, DNA). Ann Pharm Fr. 2006;64:383–9.

    Article  CAS  Google Scholar 

  6. Van Eeden SF, Sin DD. Oxidative stress in chronic obstructive pulmonary disease: a lung and systemic process. Can Respir J. 2013;20:27–29.

    Article  Google Scholar 

  7. Cheng WE, Shih CM, Hang LW, Wu KY, Yang HL, Hsu WH, et al. Urinary biomarker of oxidative stress correlating with outcome in critically septic patients. Intensive Care Med. 2007;33:1468–72.

    Article  Google Scholar 

  8. Kelly FJ. Oxidative stress: its role in air pollution and adverse health effects. Occup Environ Med. 2003;60:612–6.

    Article  Google Scholar 

  9. Tramuto F, Cusimano R, Cerame G, Vultaggio M, Calamusa G, Maida CM, et al. Urban air pollution and emergency room admissions for respiratory symptoms: a case-crossover study in Palermo, Italy. Environ Health. 2001;10:31.

    Article  Google Scholar 

  10. Barregard L, Sallsten G, Andersson L, Almstrand AC, Gustafson P, Andersson M, et al. Experimental exposure to wood smoke: effects on airway inflammation and oxidative stress. Occup Environ Med. 2008;65:319–24.

    Article  CAS  Google Scholar 

  11. Ceylan E, Kocyigit A, Gencer M, Aksoy N, Selek S. Increased DNA damage in patients with chronic obstructive pulmonary disease who had once smoked or been exposed to biomass. Respir Med. 2006;100:1270–6.

    Article  Google Scholar 

  12. Neophytou AM, Hart JE, Chang Y, Zhang JJ, Smith TJ, Garshick E, et al. Short-term traffic related exposures and biomarkers of nitro-PAH exposure and oxidative DNA damage. Toxics. 2014;2:377–90.

    Article  Google Scholar 

  13. Romieu I, Barraza-Villarreal A, Escamilla-Nunez C, Almstrand AC, Diaz-Sanchez D, Sly PD, et al. Exhaled breath malondialdehyde as a marker of effect of exposure to air pollution in children with asthma. J Allergy Clin Immunol. 2008;121:903-9.e6.

  14. Zhang J, Zhu T, Kipen H, Wang G, Huang W, Rich D, et al. Cardiorespiratory biomarker responses in healthy young adults to drastic air quality changes surrounding the 2008 Beijing Olympics. Res Rep Health Eff Inst. 2013;174:5–174.

    Google Scholar 

  15. Heinrich J, Schikowski T. COPD patients as vulnerable subpopulation for exposure to ambient air pollution. Curr Environ Health Rep. 2018;5:70–6.

    Article  CAS  Google Scholar 

  16. Grady ST, Koutrakis P, Hart JE, Coull BA, Schwartz J, Laden F, et al. Indoor black carbon exposure and oxidative stress biomarkers in COPD patients. Environ Int. 2018;115:188–95.

    Article  CAS  Google Scholar 

  17. Bruce N, Perez-Padilla R, Albalak R. Indoor air pollution in developing countries: a major environmental and public health challenge. Bull World Health Organ. 2000;78:1078–92.

    CAS  PubMed  PubMed Central  Google Scholar 

  18. Huang S, Garshick E, Vieira CLZ, Grady ST, Schwartz JD, Coull BA, et al. Short-term exposures to particulate matter gamma radiation activities and biomarkers of systemic inflammation and endothelial activation in COPD patients. Environ Res. 2019;180:108841.

  19. Marsh JW, Bailey MR. A review of lung-to-blood absorption rates for radon progeny. Radiat Prot Dosim. 2013;2013:499–514.

    Article  Google Scholar 

  20. Li W, Nyhan MM, Wiker EH, CLZ Vieira, Lin HH, Schwartz JD, et al. Recent exposure to particle radioactivity and biomarkers of oxidative stress and inflammation: the Framingham Heart study. Environ Int. 2018;121:1210–6.

    Article  CAS  Google Scholar 

  21. Nyhan MM, Coull BA, Blomberg AJ, Vieira CLZ, Garshick E, Aba A, et al. Associations between ambient particle radioactivity and blood pressure: the NAS (Normative Aging Study). J Am Heart Assoc. 2018;7:pii: e008245.

  22. Nyhan MM, Rice M, Blomberg A, Coull BA, Garshick E, Vokonas P, et al. Associations between ambient particle radioactivity and lung function. Environ Int. 2019;130:104795.

    Article  CAS  Google Scholar 

  23. Garshick E. Effects of short- and long-term exposures to ambient air pollution on COPD. Eur Respir J. 2014;44:558–61.

    Article  CAS  Google Scholar 

  24. Vieira CLZ, Koutrakis P, Huang S, Grady S, Hart JE, Coull BA, et al. Short-term effects of particle gamma radiation activities on pulmonary function in COPD patients. Environ Res. 2019;175:221–7.

    Article  CAS  Google Scholar 

  25. Garshick E, Grady ST, Hart JE, Coull BA, Schwartz J, Laden F, et al. Indoor Black Carbon and Biomarkers of Systemic Inflammation and endothelial activation in COPD Patients. Environ Res. 2018;165:358–64.

    Article  CAS  Google Scholar 

  26. Cui X, Gong J, Han H, He L, Teng Y, Tetley T, et al. Relationship between free and total malondialdehyde, a well-established marker of oxidative stress, in various types of human biospecimens. J Thorac Dis. 2018;10:3088–97.

    Article  Google Scholar 

  27. Commodore AA, Zhang JJ, Chang Y, Hartinger SM, Lanata CF, Mausezahl D, et al. Concentrations of urinary 8-hydroxy-2′-deoxyguanosine and 8-isoprostane in women exposed to woodsmoke in a cookstove intervention study in San Marcos, Peru. Environ Int. 2013;60:112–22.

    Article  CAS  Google Scholar 

  28. Gong J, Zhu T, Kipen H, Wang G, Hu M, Ohman-Strickland P, et al. Malondialdehyde in exhaled breath condensate and urine as a biomarker of air pollution induced oxidative stress. J Expo Sci Environ Epidemiol. 2013;23:322–7.

    Article  CAS  Google Scholar 

  29. Environmental Protection Agency (EPA). Expansion and upgrade of the RadNet Air monitoring network. U.S. EPA. 2005.

  30. Environmental Protection Agency (EPA). Radiological Laboratory Sample Analysis Guide for Incidents of National Significance-Radionuclides in Air. U.S. EPA. 2009.

  31. Ramadhan RA, Abdullah KMS. Background reduction by Cu/Pb shielding and efficiency study of NaI (TI) detector. Nucl Eng Technol. 2018;50:462–9.

    Article  CAS  Google Scholar 

  32. Tang CH, Garshick E, Grady S, Coull B, Schwartz J, Koutrakis P. Development of a modeling approach to estimate indoor to-outdoor sulfur ratios and predict indoor PM2.5 and black carbon concentrations for Eastern Massachusetts households. J Expo Sci Env Epidemiol. 2018;28:125–30.

    Article  CAS  Google Scholar 

  33. Huang SD, Lawrence J, Kang CM, Li J, Martins M, Vokonas P, et al. Road proximity influences indoor exposures to ambient fine particle mass and components. Environ Pollut. 2018;243:978–87.

    Article  CAS  Google Scholar 

  34. Kang CM, Koutrakis P, Suh HH. Hourly measurements of fine particulate sulfate and carbon aerosols at the Harvard-U.S. Environmental protection agency supersite in Boston. J Air Waste Manag Assoc. 2010;60:1327–34.

    Article  CAS  Google Scholar 

  35. Ruiz PA, Toro C, Cáceres J, López G, Oyola P, Koutrakis P. Effect of gas and kerosene space heaters on indoor air quality: a Study in Homes of Santiago, Chile. J Air Waste Manag. 2000;60:98–108.

    Article  Google Scholar 

  36. Schwartz J. The distributed lag between air pollution and daily deaths. Epidemiology 2000;11:320–6.

    Article  CAS  Google Scholar 

  37. Sarnat J, Long CM, Koutrakis P. Using sulfur as a tracer of outdoor fine particulate matter. Environ Sci Technol. 2002;36:5305–14.

    Article  CAS  Google Scholar 

  38. Porstendörfer J. Physical parameters and dose factors of the radon and thoron decay products. Radiat Prot Dosim. 2001;94:365–973.

    Article  Google Scholar 

  39. Porstendörfer J, Gründel M. Radon decay products in outdoor air. Radioactiv Environ. 2005;7:56–65.

    Article  Google Scholar 

  40. Kloog I, Nordio F, Coull BA, Schwartz J. Predicting spatiotemporal mean air temperature using MODIS satellite surface temperature measurements across the NorthEastern USA. Remote Sens Environ. 2014;150:132–9.

    Article  Google Scholar 

  41. Reinhold K, Wei P, Dambacher M, Yan M, Zhou XL. Experimental effects and individual differences in linear mixed models: estimating the relationship between spatial, object, and attraction effects in visual attention. Front Psychol 2011;1:238.

    Google Scholar 

  42. Azzam EI, Jay-Gerin JP, Pain D. Ionizing radiation-induced metabolic oxidative stress and prolonged cell injury. Cancer Lett. 2012;327:48–60.

    Article  CAS  Google Scholar 

  43. Szumiel I. Ionizing radiation-induced oxidative stress, epigenetic changes and genomic instability: the pivotal role of mitochondria. Int J Radiat Biol. 2015;91:1–12.

    Article  CAS  Google Scholar 

  44. Stacey WM Introductory nuclear physics, 2nd, completely revised and enlarged edition. Wiley-VCH, Verlag GmbH & Co. KgaA, Weinheim, 2007.

Download references

Acknowledgements

This study was funded by the National Institute of Environmental Health Sciences (NIEHS) (grant numbers: P30-ES000002, P01-ES009825, and R01-ES019853), and was conducted with resources and the use of facilities at the VA Boston Healthcare System. This publication was also made possible by United States Environmental Protection Agency (USEPA) (grant number: RD-835872-01) through the Harvard University USEPA sponsored Air, Climate & Environment (ACE) Centre. The contents do not reflect the position of the Department of Veterans Affairs or the United States Government. As well, the contents of the study are solely the responsibility of the grantee and do not necessarily represent the official views of the USEPA. Further, USEPA does not endorse the purchase of any commercial products or services mentioned in the publication.

Author information

Authors and Affiliations

  1. Department of Environmental Health, Harvard T.H. Chan School of Public Health, Boston, MA, USA

    Shaodan Huang, Petros Koutrakis, Carolina L. Z. Vieira, Joel D. Schwartz, Brent A. Coull, Jaime E. Hart & Francine Laden

  2. Research and Development Service, VA Boston Healthcare System, Boston, MA, USA

    Stephanie T. Grady

  3. Channing Division of Network Medicine, Department of Medicine, Brigham and Women’s Hospital and Harvard Medical School, Boston, MA, USA

    Stephanie T. Grady, Joel D. Schwartz, Jaime E. Hart, Francine Laden & Eric Garshick

  4. Department of Epidemiology, Harvard T.H. Chan School of Public Health, Boston, MA, USA

    Joel D. Schwartz & Francine Laden

  5. Department of Biostatistics, Harvard T.H. Chan School of Public Health, Boston, MA, USA

    Brent A. Coull

  6. Nicholas School of the Environment, Duke University, Durham, NC, USA

    Junfeng (Jim) Zhang

  7. Pulmonary, Allergy, Sleep, and Critical Care Medicine Section, Medical Service, VA Boston Healthcare System, Boston, MA, USA

    Eric Garshick

Authors
  1. Shaodan Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Petros Koutrakis
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Stephanie T. Grady
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Carolina L. Z. Vieira
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Joel D. Schwartz
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Brent A. Coull
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Jaime E. Hart
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Francine Laden
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Junfeng (Jim) Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Eric Garshick
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Eric Garshick.

Ethics declarations

Conflict of interest

The authors declare no conflict of interests, including relevant financial interests, activities, relationships, and affiliations.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Huang, S., Koutrakis, P., Grady, S.T. et al. Effects of particulate matter gamma radiation on oxidative stress biomarkers in COPD patients. J Expo Sci Environ Epidemiol 31, 727–735 (2021). https://doi.org/10.1038/s41370-020-0204-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41370-020-0204-8

Keywords

Search

Advanced search

Quick links