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:

Annual space weather fluctuations and telomere length dynamics in a longitudinal cohort of older men: the Normative Aging Study

Journal of Exposure Science & Environmental Epidemiology (2023)Cite this article

Abstract

Background

Space weather has been associated with increased risk of cardiovascular diseases in space and flight crew. However, limited research has focused on the ground population, particularly among the elderly who are vulnerable to aging-related diseases.

Objective

We evaluated the association between space weather alterations and biological aging using leukocyte telomere length as a biomarker in healthy elderly men.

Methods

We used data from the Normative Aging Study, a longitudinal cohort of healthy elderly men in Massachusetts, USA. Leukocyte telomere length and health information were measured at in-person examinations approximately every three years, contributing to a total of 1,850 visits from 791 participants. Regional space weather information was collected daily, including cosmic ray-induced ionization, neutrons, sunspot number, interplanetary magnetic field, and Kp-index as our exposure of interest. We used mixed-effects models with a random intercept per individual to evaluate the associations between annual averages of space weather indicators and relative telomere length while accounting for participant demographics, environmental parameters, and secular trends.

Results

The mean age at baseline was 72.36 years. A one-year increment in age is associated with a 1.21% reduction in leukocyte telomere length. In the fully adjusted model accounting for individual and environmental factors, an interquartile range (IQR) increase of annual cosmic ray induced ionization (110.0 ion pairs cm−3 sec−1) was associated with a 17.64% (95%CI: −27.73%, −7.55%) decrease in leukocyte telomere length, equivalent to 15-years age increment. Solar and geomagnetic activities were associated with increased leukocyte telomere length, but the association became absent after adjusting for cosmic ray indicators.

Impact

  • Galactic cosmic rays may accelerate the aging process in populations on the Earth, despite the protection by the Earth’s atmosphere and magnetic field. This research enhances our understanding of how changes in space weather can impact health, highlights potential risks from space to Earth’s inhabitants, and helps inform health strategies for vulnerable populations.

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: Daily cosmic rays and solar and geomagnetic activities between 1999 and 2010.
Fig. 2: Distribution of log-transformed relative telomere length (T:S) by quartiles of cosmic rays and solar activities.
Fig. 3: Relationships between relative telomere length with annual moving averages of cosmic rays and solar activities during 1999–2010.

Similar content being viewed by others

Data availability

The data that support the findings of this study are available from the corresponding author upon reasonable request.

References

  1. Zilli Vieira CL, Alvares D, Blomberg A, Schwartz J, Coull B, Huang S, et al. Geomagnetic disturbances driven by solar activity enhance total and cardiovascular mortality risk in 263 U.S. cities. Environ Health. 2019;18:83.

    Article  PubMed  PubMed Central  Google Scholar 

  2. Zilli Vieira CL, Link MS, Garshick E, Peralta AA, Luttmann-Gibson H, Laden F, et al. Solar and geomagnetic activity enhance the effects of air pollutants on atrial fibrillation. Europace. 2022;24:713–20.

    Article  PubMed  Google Scholar 

  3. Vieira CLZ, Janot-Pacheco E, Lage C, Pacini A, Koutrakis P, Cury PR, et al. Long-term association between the intensity of cosmic rays and mortality rates in the city of Sao Paulo. Environ Res Lett. 2018;13:024009.

    Article  Google Scholar 

  4. Scheibler C, Toprani SM, Mordukhovich I, Schaefer M, Staffa S, Nagel ZD, et al. Cancer risks from cosmic radiation exposure in flight: A review. Front Public Health. 2022;10:947068.

    Article  PubMed  PubMed Central  Google Scholar 

  5. Usoskin IG, Desorgher L, Velinov P, Storini M, Flückiger EO, Bütikofer R, et al. Ionization of the earth’s atmosphere by solar and galactic cosmic rays. Acta Geophysica. 2008;57:88–101.

    Article  Google Scholar 

  6. Forbush SE. On the effects in cosmic-ray intensity observed during the recent magnetic storm. Phys Rev. 1937;51:1108–9.

    Article  Google Scholar 

  7. Di Trolio R, Di Lorenzo G, Fumo B, Ascierto PA. Cosmic radiation and cancer: is there a link? Future Oncol. 2015;11:1123–35.

    Article  PubMed  Google Scholar 

  8. Mazzei-Abba A, Folly CL, Kreis C, Ammann RA, Adam C, Brack E, et al. External background ionizing radiation and childhood cancer: Update of a nationwide cohort analysis. J Environ Radioact. 2021;238-239:106734.

    Article  CAS  PubMed  Google Scholar 

  9. Gilchrest BA, Eller MS, Geller AC, Yaar M. The pathogenesis of melanoma induced by ultraviolet radiation. N. Engl J Med. 1999;340:1341–8.

    Article  CAS  PubMed  Google Scholar 

  10. Kim Y, He YY. Ultraviolet radiation-induced non-melanoma skin cancer: Regulation of DNA damage repair and inflammation. Genes Dis. 2014;1:188–98.

    Article  PubMed  PubMed Central  Google Scholar 

  11. Fleischer AB Jr., Fleischer SE. Solar radiation and the incidence and mortality of leading invasive cancers in the United States. Dermatoendocrinol. 2016;8:e1162366.

    Article  PubMed  PubMed Central  Google Scholar 

  12. Barnes RP, Fouquerel E, Opresko PL. The impact of oxidative DNA damage and stress on telomere homeostasis. Mech Ageing Dev. 2019;177:37–45.

    Article  CAS  PubMed  Google Scholar 

  13. Hewitt G, Jurk D, Marques FD, Correia-Melo C, Hardy T, Gackowska A, et al. Telomeres are favoured targets of a persistent DNA damage response in ageing and stress-induced senescence. Nat Commun. 2012;3:708.

    Article  PubMed  Google Scholar 

  14. Vaiserman A, Krasnienkov D. Telomere length as a marker of biological age: state-of-the-art, open issues, and future perspectives. Front Genet. 2020;11:630186.

    Article  CAS  PubMed  Google Scholar 

  15. Stone RC, Horvath K, Kark JD, Susser E, Tishkoff SA, Aviv A. Telomere length and the cancer-atherosclerosis trade-off. PLoS Genet. 2016;12:e1006144.

    Article  PubMed  PubMed Central  Google Scholar 

  16. de Lange T. How telomeres solve the end-protection problem. Science. 2009;326:948–52.

    Article  PubMed  PubMed Central  Google Scholar 

  17. Zhang J, Rane G, Dai X, Shanmugam MK, Arfuso F, Samy RP, et al. Ageing and the telomere connection: An intimate relationship with inflammation. Ageing Res Rev. 2016;25:55–69.

    Article  CAS  PubMed  Google Scholar 

  18. von Zglinicki T. Oxidative stress shortens telomeres. Trends Biochemical Sci. 2002;27:339–44.

    Article  Google Scholar 

  19. Morla M, Busquets X, Pons J, Sauleda J, MacNee W, Agusti AG. Telomere shortening in smokers with and without COPD. Eur Respir J. 2006;27:525–8.

    Article  CAS  PubMed  Google Scholar 

  20. Kim S, Parks CG, DeRoo LA, Chen H, Taylor JA, Cawthon RM, et al. Obesity and weight gain in adulthood and telomere length. Cancer Epidemiol Biomark Prev. 2009;18:816–20.

    Article  CAS  Google Scholar 

  21. Haycock PC, Heydon EE, Kaptoge S, Butterworth AS, Thompson A, Willeit P. Leucocyte telomere length and risk of cardiovascular disease: systematic review and meta-analysis. BMJ. 2014;349:g4227.

    Article  PubMed  PubMed Central  Google Scholar 

  22. Miri M, Nazarzadeh M, Alahabadi A, Ehrampoush MH, Rad A, Lotfi MH, et al. Air pollution and telomere length in adults: A systematic review and meta-analysis of observational studies. Environ Pollut. 2019;244:636–47.

    Article  CAS  PubMed  Google Scholar 

  23. McCracken J, Baccarelli A, Hoxha M, Dioni L, Melly S, Coull B, et al. Annual ambient black carbon associated with shorter telomeres in elderly men: Veterans Affairs Normative Aging Study. Environ Health Perspect. 2010;118:1564–70.

    Article  PubMed  PubMed Central  Google Scholar 

  24. Shim G, Ricoul M, Hempel WM, Azzam EI, Sabatier L. Crosstalk between telomere maintenance and radiation effects: A key player in the process of radiation-induced carcinogenesis. Mutat Res Rev Mutat Res. 2014;760:1–17.

    Article  CAS  Google Scholar 

  25. Li P, Hou M, Lou F, Bjorkholm M, Xu D. Telomere dysfunction induced by chemotherapeutic agents and radiation in normal human cells. Int J Biochem Cell Biol. 2012;44:1531–40.

    Article  CAS  PubMed  Google Scholar 

  26. Berardinelli F, Antoccia A, Cherubini R, De Nadal V, Gerardi S, Tanzarella C, et al. Telomere alterations and genomic instability in long-term cultures of normal human fibroblasts irradiated with X rays and protons. Radiat Prot Dosim. 2011;143:274–8.

    Article  CAS  Google Scholar 

  27. Berardinelli F, Antoccia A, Buonsante R, Gerardi S, Cherubini R, et al. The role of telomere length modulation in delayed chromosome instability induced by ionizing radiation in human primary fibroblasts. Environ Mol Mutagen. 2013;54:172–9.

    Article  CAS  PubMed  Google Scholar 

  28. Moller P, Wils RS, Jensen DM, Andersen MHG, Roursgaard M. Telomere dynamics and cellular senescence: an emerging field in environmental and occupational toxicology. Crit Rev Toxicol. 2018;48:761–88.

    Article  PubMed  Google Scholar 

  29. Garrett-Bakelman FE, Darshi M, Green SJ, Gur RC, Lin L, Macias BR, et al. The NASA Twins Study: A multidimensional analysis of a year-long human spaceflight. Science. 2019;364:eaau8650.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Luxton JJ, McKenna MJ, Lewis A, Taylor LE, George KA, Dixit SM, et al. Telomere length dynamics and DNA damage responses associated with long-duration spaceflight. Cell Rep. 2020;33:108457.

    Article  CAS  PubMed  Google Scholar 

  31. Luxton JJ, McKenna MJ, Taylor LE, George KA, Zwart SR, Crucian BE, et al. Temporal telomere and DNA damage responses in the space radiation environment. Cell Rep. 2020;33:108435.

    Article  CAS  PubMed  Google Scholar 

  32. Das B, Saini D, Seshadri M. Telomere length in human adults and high level natural background radiation. PLoS One. 2009;4:e8440.

    Article  PubMed  PubMed Central  Google Scholar 

  33. Chougaonkar MP, Eappen KP, Ramachandran TV, Shetty PG, Mayya YS, Sadasivan S, et al. Profiles of doses to the population living in the high background radiation areas in Kerala, India. J Environ Radioactivity. 2004;71:275–97.

    Article  CAS  Google Scholar 

  34. Cucinotta FA, Kim MH, Willingham V, George KA. Physical and biological organ dosimetry analysis for international space station astronauts. Radiat Res. 2008;170:127–38.

    Article  CAS  PubMed  Google Scholar 

  35. Scherthan H, Sotnik N, Peper M, Schrock G, Azizova T, Abend M. Telomere Length in Aged Mayak PA Nuclear Workers Chronically Exposed to Internal Alpha and External Gamma Radiation. Radiat Res. 2016;185:658–67.

    Article  CAS  PubMed  Google Scholar 

  36. Andreassi MG, Piccaluga E, Gargani L, Sabatino L, Borghini A, Faita F, et al. Subclinical carotid atherosclerosis and early vascular aging from long-term low-dose ionizing radiation exposure: a genetic, telomere, and vascular ultrasound study in cardiac catheterization laboratory staff. JACC Cardiovasc Interv 2015;8:616–27.

    Article  PubMed  Google Scholar 

  37. Usoskin IG, Kovaltsov GA. Cosmic ray induced ionization in the atmosphere: Full modeling and practical applications. J Geophys Res. 2006;111:D21206.

    Google Scholar 

  38. Zilli Vieira CL, Koutrakis P. The impact of solar activity on ambient ultrafine particle concentrations: An analysis based on 19-year measurements in Boston, USA. Environ Res. 2021;201:111532.

    Article  CAS  PubMed  Google Scholar 

  39. University of Delaware Bartol Research Institute neutron monitor program. 2021. https://neutronm.bartol.udel.edu/ Accessed 30 June 2022.

  40. Cawthon RM. Telomere measurement by quantitative PCR. Nucleic Acids Res. 2002;30:e47.

    Article  PubMed  PubMed Central  Google Scholar 

  41. Hou L, Savage SA, Blaser MJ, Perez-Perez G, Hoxha M, Dioni L, et al. Telomere length in peripheral leukocyte DNA and gastric cancer risk. Cancer Epidemiol Biomark Prev. 2009;18:3103–9.

    Article  CAS  Google Scholar 

  42. Hou L, Joyce BT, Gao T, Liu L, Zheng Y, Penedo FJ, et al. Blood Telomere Length Attrition and Cancer Development in the Normative Aging Study Cohort. EBioMedicine. 2015;2:591–6.

    Article  PubMed  PubMed Central  Google Scholar 

  43. Vitti ET, Parsons JL. The Radiobiological Effects of Proton Beam Therapy: Impact on DNA Damage and Repair. Cancers (Basel). 2019;11:946.

    Article  CAS  PubMed  Google Scholar 

  44. Alan Mitteer R, Wang Y, Shah J, Gordon S, Fager M, Butter PP, et al. Proton beam radiation induces DNA damage and cell apoptosis in glioma stem cells through reactive oxygen species. Sci Rep. 2015;5:13961.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Sridharan DM, Asaithamby A, Blattnig SR, Costes SV, Doetsch PW, Dynan WS, et al. Evaluating biomarkers to model cancer risk post cosmic ray exposure. Life Sci Space Res (Amst). 2016;9:19–47.

    Article  PubMed  Google Scholar 

  46. Nassour J, Schmidt TT, Karlseder J. Telomeres and cancer: resolving the paradox. Annu Rev Cancer Biol. 2021;5:59–77.

    Article  PubMed  PubMed Central  Google Scholar 

  47. Telomeres Mendelian Randomization C, Haycock PC, Burgess S, Nounu A, Zheng J, Okoli GN, et al. Association between telomere length and risk of cancer and non-neoplastic diseases: a mendelian randomization study. JAMA Oncol. 2017;3:636–51.

    Article  Google Scholar 

  48. Zhang C, Doherty JA, Burgess S, Hung RJ, Lindstrom S, Kraft P, et al. Genetic determinants of telomere length and risk of common cancers: a Mendelian randomization study. Hum Mol Genet. 2015;24:5356–66.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Mirabello L, Yu K, Kraft P, De Vivo I, Hunter DJ, Prescott J, et al. The association of telomere length and genetic variation in telomere biology genes. Hum Mutat. 2010;31:1050–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Jeggo PA, Pearl LH, Carr AM. DNA repair, genome stability and cancer: a historical perspective. Nat Rev Cancer. 2016;16:35–42.

    Article  CAS  PubMed  Google Scholar 

  51. Nagel ZD, Chaim IA, Samson LD. Inter-individual variation in DNA repair capacity: a need for multi-pathway functional assays to promote translational DNA repair research. DNA Repair (Amst). 2014;19:199–213.

    Article  CAS  PubMed  Google Scholar 

  52. Nagel ZD, Engelward BP, Brenner DJ, Begley TJ, Sobol RW, Bielas JH, et al. Towards precision prevention: Technologies for identifying healthy individuals with high risk of disease. Mutat Res. 2017;800-802:14–28.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We offer our special thanks to the NAS participants. The authors would like to thank the study participants for their dedicated participation.

Funding

Funding

The VA Normative Aging Study is supported by the Cooperative Studies Program/Epidemiology Research and Information Center of the U.S. Department of Veterans Affairs and is a component of the Massachusetts Veterans Epidemiology Research and Information Center (MAVERIC), Boston, Massachusetts. This material is the result of work supported with resources and the use of facilities at the Veterans Affairs Boston Healthcare System. The views expressed in this article are those of the authors and do not necessarily reflect the position or policy of the Department of Veterans Affairs or the United States government. This work was supported by National Institutes of Health (grants R01ES015172, R21ES021895, R21ES028472, R01ES021733, R21-ES029637 (JS, AAB); and U01ES029520 (ZDN, TZ)) and EPA grant RD-835872 (PK). Its contents are solely the responsibility of the grantee and do not necessarily represent the official views of the U.S. EPA. Further, U.S. EPA 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, 02115, USA

    Ting Zhai, Carolina L. Zilli Vieira, Zachary D. Nagel, Joel Schwartz & Petros Koutrakis

  2. VA Normative Aging Study, Veterans Affairs Boston Healthcare System and the Department of Medicine, Boston University Chobanian and Avadisian School of Medicine, Boston, MA, 02115, USA

    Pantel Vokonas

  3. Department of Environmental Health Sciences, Columbia University Mailman School of Public Health, New York, NY, 10032, USA

    Andrea A. Baccarelli

Authors
  1. Ting Zhai
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Carolina L. Zilli Vieira
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Pantel Vokonas
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Andrea A. Baccarelli
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Zachary D. Nagel
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Joel Schwartz
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Petros Koutrakis
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Conceptualization: PK, CLZV, JS. Methodology: TZ, CLZV. Investigation: AAB. Formal analysis: TZ. Visualization: TZ. Funding acquisition: JS, AAB, ZDN, PV, PK. Project administration: PV. Supervision: PK, CLZV, ZDN. Writing – original draft: TZ, CLZV. Writing – review & editing: all authors

Corresponding author

Correspondence to Carolina L. Zilli Vieira.

Ethics declarations

Competing interests

The authors declare no competing interests.

Ethical approval

The VA normative aging study was approved by the institutional review boards of the Harvard T.H. School of Public Health and the Veterans Administration Boston Healthcare System, and all participants provided written informed consent.

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

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhai, T., Zilli Vieira, C.L., Vokonas, P. et al. Annual space weather fluctuations and telomere length dynamics in a longitudinal cohort of older men: the Normative Aging Study. J Expo Sci Environ Epidemiol (2023). https://doi.org/10.1038/s41370-023-00616-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1038/s41370-023-00616-z

Keywords

Search

Advanced search

Quick links