Skip to main content
Top
Published in:

13-11-2024 | Review

Cohort Studies and Multi-omics Approaches to Low-Dose Ionizing Radiation-Induced Cardiovascular Disease: A Comprehensive Review

Authors: Xumin Zong, Lin Zhu, Yan Wang, Jinhan Wang, Yeqing Gu, Qiang Liu

Published in: Cardiovascular Toxicology | Issue 1/2025

Login to get access

Abstract

The effect of low-dose ionizing radiation exposure on the risk of cardiovascular disease (CVD) represents a significant concern in the field of radiation protection. The prevailing approach to mitigating the adverse effects of low-dose or low-dose-rate radiation does not currently incorporate the potential risk of CVD, despite the possibility that such risk may be a substantial contributor to overall health hazards. Current evidence suggests a potential association between radiation exposure and CVD; however, the overall findings remain inconclusive. This is particularly due to the uncertainty surrounding the influence of significant non-radiation risk factors on the associations reported in epidemiological studies. It is difficult to discern the underlying connection in observational epidemiology when there is substantial variation in baseline risk factors. The paucity of epidemiological research in this domain is being partially offset by the advancement of multi-omics approaches. These methods assist in identifying radiosensitive targets, comprehending underlying biological processes, and pinpointing biomarkers. This, in turn, fortifies the evidence gleaned from epidemiological studies. In this review, we delve into the body of epidemiological research pertaining to CVD induced by low-dose ionizing radiation and the application of multi-omics techniques. The integration of these two methodologies holds the promise of identifying specific molecules or biological pathways that can be employed to validate endpoints related to radiation risk assessment.
Literature
1.
3.
go back to reference Stewart, F. A., Akleyev, A. V., Hauer-Jensen, M., Hendry, J. H., Kleiman, N. J., Macvittie, T. J., Aleman, B. M., Edgar, A. B., Mabuchi, K., Muirhead, C. R., Shore, R. E., & Wallace, W. H. (2012). ICRP publication 118: ICRP statement on tissue reactions and early and late effects of radiation in normal tissues and organs–threshold doses for tissue reactions in a radiation protection context. Annals of the ICRP, 41, 1–322. https://doi.org/10.1016/j.icrp.2012.02.001CrossRefPubMed Stewart, F. A., Akleyev, A. V., Hauer-Jensen, M., Hendry, J. H., Kleiman, N. J., Macvittie, T. J., Aleman, B. M., Edgar, A. B., Mabuchi, K., Muirhead, C. R., Shore, R. E., & Wallace, W. H. (2012). ICRP publication 118: ICRP statement on tissue reactions and early and late effects of radiation in normal tissues and organs–threshold doses for tissue reactions in a radiation protection context. Annals of the ICRP, 41, 1–322. https://​doi.​org/​10.​1016/​j.​icrp.​2012.​02.​001CrossRefPubMed
4.
go back to reference Stewart, J. R., & Fajardo, L. F. (1971). Radiation-induced heart disease. Clinical and experimental aspects. Radiologic Clinics of North America, 9, 511–531.CrossRefPubMed Stewart, J. R., & Fajardo, L. F. (1971). Radiation-induced heart disease. Clinical and experimental aspects. Radiologic Clinics of North America, 9, 511–531.CrossRefPubMed
8.
go back to reference Kreuzer, M., Auvinen, A., Cardis, E., Hall, J., Jourdain, J.-R., Laurier, D., Little, M. P., Peters, A., Raj, K., Russell, N. S., Tapio, S., Zhang, W., & Gomolka, M. (2015). Low-dose ionising radiation and cardiovascular diseases–Strategies for molecular epidemiological studies in Europe. Mutation Research/Reviews in Mutation Research, 764, 90–100. https://doi.org/10.1016/j.mrrev.2015.03.002CrossRefPubMed Kreuzer, M., Auvinen, A., Cardis, E., Hall, J., Jourdain, J.-R., Laurier, D., Little, M. P., Peters, A., Raj, K., Russell, N. S., Tapio, S., Zhang, W., & Gomolka, M. (2015). Low-dose ionising radiation and cardiovascular diseases–Strategies for molecular epidemiological studies in Europe. Mutation Research/Reviews in Mutation Research, 764, 90–100. https://​doi.​org/​10.​1016/​j.​mrrev.​2015.​03.​002CrossRefPubMed
9.
go back to reference G. Assembly, UNSCEAR 2012 Report Report to the General Assembly, 2012. G. Assembly, UNSCEAR 2012 Report Report to the General Assembly, 2012.
14.
go back to reference Tran, V., Zablotska, L. B., Brenner, A. V., & Little, M. P. (2017). Radiation-associated circulatory disease mortality in a pooled analysis of 77,275 patients from the Massachusetts and Canadian tuberculosis fluoroscopy cohorts. Science and Reports, 7, 1–10. https://doi.org/10.1038/srep44147CrossRef Tran, V., Zablotska, L. B., Brenner, A. V., & Little, M. P. (2017). Radiation-associated circulatory disease mortality in a pooled analysis of 77,275 patients from the Massachusetts and Canadian tuberculosis fluoroscopy cohorts. Science and Reports, 7, 1–10. https://​doi.​org/​10.​1038/​srep44147CrossRef
17.
go back to reference Takahashi, I., Abbott, R. D., Ohshita, T., Takahashi, T., Ozasa, K., Akahoshi, M., Fujiwara, S., Kodama, K., & Matsumoto, M. (2012). A prospective follow-up study of the association of radiation exposure with fatal and non-fatal stroke among atomic bomb survivors in Hiroshima and Nagasaki (1980–2003). British Medical Journal Open, 2, e000654. https://doi.org/10.1136/bmjopen-2011-000654CrossRef Takahashi, I., Abbott, R. D., Ohshita, T., Takahashi, T., Ozasa, K., Akahoshi, M., Fujiwara, S., Kodama, K., & Matsumoto, M. (2012). A prospective follow-up study of the association of radiation exposure with fatal and non-fatal stroke among atomic bomb survivors in Hiroshima and Nagasaki (1980–2003). British Medical Journal Open, 2, e000654. https://​doi.​org/​10.​1136/​bmjopen-2011-000654CrossRef
18.
go back to reference Vrijheid, M., Cardis, E., Ashmore, P., Auvinen, A., Bae, J. M., Engels, H., Gilbert, E., Gulis, G., Habib, R. R., Howe, G., Kurtinaitis, J., Malker, H., Muirhead, C. R., Richardson, D. B., Rodriguez-Artalejo, F., Rogel, A., Schubauer-Berigan, M., Tardy, H., Telle-Lamberton, M., … Veress, K. (2007). Mortality from diseases other than cancer following low doses of ionizing radiation: Results from the 15-Country Study of nuclear industry workers. International Journal of Epidemiology, 36, 1126–1135. https://doi.org/10.1093/ije/dym138CrossRefPubMed Vrijheid, M., Cardis, E., Ashmore, P., Auvinen, A., Bae, J. M., Engels, H., Gilbert, E., Gulis, G., Habib, R. R., Howe, G., Kurtinaitis, J., Malker, H., Muirhead, C. R., Richardson, D. B., Rodriguez-Artalejo, F., Rogel, A., Schubauer-Berigan, M., Tardy, H., Telle-Lamberton, M., … Veress, K. (2007). Mortality from diseases other than cancer following low doses of ionizing radiation: Results from the 15-Country Study of nuclear industry workers. International Journal of Epidemiology, 36, 1126–1135. https://​doi.​org/​10.​1093/​ije/​dym138CrossRefPubMed
20.
22.
go back to reference Gillies, M., Richardson, D. B., Cardis, E., Daniels, R. D., O’Hagan, J. A., Haylock, R., Laurier, D., Leuraud, K., Moissonnier, M., Schubauer-Berigan, M. K., Thierry-Chef, I., & Kesminiene, A. (2017). Mortality from circulatory diseases and other non-cancer outcomes among nuclear workers in France, the United Kingdom and the United States (inworks). Radiation Research, 188, 276–290. https://doi.org/10.1667/RR14608.1CrossRefPubMedPubMedCentral Gillies, M., Richardson, D. B., Cardis, E., Daniels, R. D., O’Hagan, J. A., Haylock, R., Laurier, D., Leuraud, K., Moissonnier, M., Schubauer-Berigan, M. K., Thierry-Chef, I., & Kesminiene, A. (2017). Mortality from circulatory diseases and other non-cancer outcomes among nuclear workers in France, the United Kingdom and the United States (inworks). Radiation Research, 188, 276–290. https://​doi.​org/​10.​1667/​RR14608.​1CrossRefPubMedPubMedCentral
24.
go back to reference Kashcheev, V. V., Chekin, S. Y., Maksioutov, M. A., Tumanov, K. A., Menyaylo, A. N., Kochergina, E. V., Kashcheeva, P. V., Gorsky, A. I., Shchukina, N. V., Karpenko, S. V., & Ivanov, V. K. (2016). Radiation-epidemiological study of cerebrovascular diseases in the cohort of russian recovery operation workers of the chernobyl accident. Health Physics, 111, 192–197. https://doi.org/10.1097/HP.0000000000000523CrossRefPubMed Kashcheev, V. V., Chekin, S. Y., Maksioutov, M. A., Tumanov, K. A., Menyaylo, A. N., Kochergina, E. V., Kashcheeva, P. V., Gorsky, A. I., Shchukina, N. V., Karpenko, S. V., & Ivanov, V. K. (2016). Radiation-epidemiological study of cerebrovascular diseases in the cohort of russian recovery operation workers of the chernobyl accident. Health Physics, 111, 192–197. https://​doi.​org/​10.​1097/​HP.​0000000000000523​CrossRefPubMed
25.
go back to reference Kashcheev, V. V., Chekin, S. Y., Karpenko, S. V., Maksioutov, M. A., Menyaylo, A. N., Tumanov, K. A., Kochergina, E. V., Kashcheeva, P. V., Gorsky, A. I., Shchukina, N. V., Lovachev, S. S., Vlasov, O. K., & Ivanov, V. K. (2017). Radiation risk of cardiovascular diseases in the cohort of russian emergency workers of the chernobyl accident. Health Physics, 113, 23–29. https://doi.org/10.1097/HP.0000000000000670CrossRefPubMed Kashcheev, V. V., Chekin, S. Y., Karpenko, S. V., Maksioutov, M. A., Menyaylo, A. N., Tumanov, K. A., Kochergina, E. V., Kashcheeva, P. V., Gorsky, A. I., Shchukina, N. V., Lovachev, S. S., Vlasov, O. K., & Ivanov, V. K. (2017). Radiation risk of cardiovascular diseases in the cohort of russian emergency workers of the chernobyl accident. Health Physics, 113, 23–29. https://​doi.​org/​10.​1097/​HP.​0000000000000670​CrossRefPubMed
26.
go back to reference Azizova, T. V., Muirhead, C. R., Druzhinina, M. B., Grigoryeva, E. S., Vlasenko, E. V., Sumina, M. V., O’Hagan, J. A., Zhang, W., Haylock, R. G. E., & Hunter, N. (2010). Cardiovascular diseases in the cohort of workers first employed at Mayak PA in 1948–1958. Radiation Research, 174, 155–168. https://doi.org/10.1667/RR1789.1CrossRefPubMed Azizova, T. V., Muirhead, C. R., Druzhinina, M. B., Grigoryeva, E. S., Vlasenko, E. V., Sumina, M. V., O’Hagan, J. A., Zhang, W., Haylock, R. G. E., & Hunter, N. (2010). Cardiovascular diseases in the cohort of workers first employed at Mayak PA in 1948–1958. Radiation Research, 174, 155–168. https://​doi.​org/​10.​1667/​RR1789.​1CrossRefPubMed
27.
go back to reference Azizova, T. V., Muirhead, C. R., Druzhinina, M. B., Grigoryeva, E. S., Vlasenko, E. V., Sumina, M. V., O’Hagan, J. A., Zhang, W., Haylock, R. G. E., & Hunter, N. (2010). Cerebrovascular diseases in the cohort of workers first employed at Mayak PA in 1948–1958. Radiation Research, 174, 851–864. https://doi.org/10.1667/RR1928.1CrossRefPubMed Azizova, T. V., Muirhead, C. R., Druzhinina, M. B., Grigoryeva, E. S., Vlasenko, E. V., Sumina, M. V., O’Hagan, J. A., Zhang, W., Haylock, R. G. E., & Hunter, N. (2010). Cerebrovascular diseases in the cohort of workers first employed at Mayak PA in 1948–1958. Radiation Research, 174, 851–864. https://​doi.​org/​10.​1667/​RR1928.​1CrossRefPubMed
28.
go back to reference Azizova, T. V., Muirhead, C. R., Moseeva, M. B., Grigoryeva, E. S., Sumina, M. V., O’Hagan, J., Zhang, W., Haylock, R. J. G. E., & Hunter, N. (2011). Cerebrovascular diseases in nuclear workers first employed at the Mayak PA in 1948–1972. Radiation and Environmental Biophysics, 50, 539–552. https://doi.org/10.1007/s00411-011-0377-6CrossRefPubMed Azizova, T. V., Muirhead, C. R., Moseeva, M. B., Grigoryeva, E. S., Sumina, M. V., O’Hagan, J., Zhang, W., Haylock, R. J. G. E., & Hunter, N. (2011). Cerebrovascular diseases in nuclear workers first employed at the Mayak PA in 1948–1972. Radiation and Environmental Biophysics, 50, 539–552. https://​doi.​org/​10.​1007/​s00411-011-0377-6CrossRefPubMed
33.
40.
go back to reference Birchall, A., Vostrotin, V., Puncher, M., Efimov, A., Dorrian, M.-D., Sokolova, A., Napier, B., Suslova, K., Miller, S., Zhdanov, A., Strom, D. J., Scherpelz, R., & Schadilov, A. (2017). The mayak worker dosimetry system (MWDS-2013) for internally deposited plutonium: An overview. Radiation Protection Dosimetry, 176, 202. https://doi.org/10.1093/rpd/ncx195CrossRefPubMed Birchall, A., Vostrotin, V., Puncher, M., Efimov, A., Dorrian, M.-D., Sokolova, A., Napier, B., Suslova, K., Miller, S., Zhdanov, A., Strom, D. J., Scherpelz, R., & Schadilov, A. (2017). The mayak worker dosimetry system (MWDS-2013) for internally deposited plutonium: An overview. Radiation Protection Dosimetry, 176, 202. https://​doi.​org/​10.​1093/​rpd/​ncx195CrossRefPubMed
43.
go back to reference Azizova, T. V., Batistatou, E., Grigorieva, E. S., McNamee, R., Wakeford, R., Liu, H., De Vocht, F., & Agius, R. M. (2018). An assessment of radiation-associated risks of mortality from circulatory disease in the cohorts of Mayak and sellafield nuclear workers. Radiation Research, 189, 371–388. https://doi.org/10.1667/RR14468.1CrossRefPubMed Azizova, T. V., Batistatou, E., Grigorieva, E. S., McNamee, R., Wakeford, R., Liu, H., De Vocht, F., & Agius, R. M. (2018). An assessment of radiation-associated risks of mortality from circulatory disease in the cohorts of Mayak and sellafield nuclear workers. Radiation Research, 189, 371–388. https://​doi.​org/​10.​1667/​RR14468.​1CrossRefPubMed
50.
go back to reference Tao, Z., Akiba, S., Zha, Y., Sun, Q., Zou, J., Li, J., Liu, Y., Yuan, Y., Tokonami, S., Morishoma, H., Koga, T., Nakamura, S., Sugahara, T., & Wei, L. (2012). Cancer and non-cancer mortality among Inhabitants in the high background radiation area of Yangjiang, China (1979–1998). Health Physics, 102, 173–181. https://doi.org/10.1097/HP.0b013e31822c7f1eCrossRefPubMed Tao, Z., Akiba, S., Zha, Y., Sun, Q., Zou, J., Li, J., Liu, Y., Yuan, Y., Tokonami, S., Morishoma, H., Koga, T., Nakamura, S., Sugahara, T., & Wei, L. (2012). Cancer and non-cancer mortality among Inhabitants in the high background radiation area of Yangjiang, China (1979–1998). Health Physics, 102, 173–181. https://​doi.​org/​10.​1097/​HP.​0b013e31822c7f1e​CrossRefPubMed
53.
go back to reference Azimzadeh, O., Azizova, T., Merl-Pham, J., Subramanian, V., Bakshi, M. V., Moseeva, M., Zubkova, O., Hauck, S. M., Anastasov, N., Atkinson, M. J., & Tapio, S. (2017). A dose-dependent perturbation in cardiac energy metabolism is linked to radiation-induced ischemic heart disease in Mayak nuclear workers. Oncotarget, 8, 9067–9078. https://doi.org/10.18632/oncotarget.10424CrossRefPubMed Azimzadeh, O., Azizova, T., Merl-Pham, J., Subramanian, V., Bakshi, M. V., Moseeva, M., Zubkova, O., Hauck, S. M., Anastasov, N., Atkinson, M. J., & Tapio, S. (2017). A dose-dependent perturbation in cardiac energy metabolism is linked to radiation-induced ischemic heart disease in Mayak nuclear workers. Oncotarget, 8, 9067–9078. https://​doi.​org/​10.​18632/​oncotarget.​10424CrossRefPubMed
56.
go back to reference Azimzadeh, O., Azizova, T., Merl-Pham, J., Blutke, A., Moseeva, M., Zubkova, O., Anastasov, N., Feuchtinger, A., Hauck, S. M., Atkinson, M. J., & Tapio, S. (2020). Chronic occupational exposure to ionizing radiation induces alterations in the structure and metabolism of the heart: A proteomic analysis of human formalin-fixed paraffin-embedded (FFPE) cardiac tissue. International Journal of Molecular Sciences. https://doi.org/10.3390/ijms21186832CrossRefPubMedPubMedCentral Azimzadeh, O., Azizova, T., Merl-Pham, J., Blutke, A., Moseeva, M., Zubkova, O., Anastasov, N., Feuchtinger, A., Hauck, S. M., Atkinson, M. J., & Tapio, S. (2020). Chronic occupational exposure to ionizing radiation induces alterations in the structure and metabolism of the heart: A proteomic analysis of human formalin-fixed paraffin-embedded (FFPE) cardiac tissue. International Journal of Molecular Sciences. https://​doi.​org/​10.​3390/​ijms21186832CrossRefPubMedPubMedCentral
57.
58.
go back to reference Barjaktarovic, Z., Merl-Pham, J., Braga-Tanaka, I., Tanaka, S., Hauck, S. M., Saran, A., Mancuso, M., Atkinson, M. J., Tapio, S., & Azimzadeh, O. (2019). Hyperacetylation of cardiac mitochondrial proteins is associated with metabolic impairment and sirtuin downregulation after chronic total body irradiation of ApoE (−/−) mice. International Journal of Molecular Sciences. https://doi.org/10.3390/ijms20205239CrossRefPubMedPubMedCentral Barjaktarovic, Z., Merl-Pham, J., Braga-Tanaka, I., Tanaka, S., Hauck, S. M., Saran, A., Mancuso, M., Atkinson, M. J., Tapio, S., & Azimzadeh, O. (2019). Hyperacetylation of cardiac mitochondrial proteins is associated with metabolic impairment and sirtuin downregulation after chronic total body irradiation of ApoE (−/−) mice. International Journal of Molecular Sciences. https://​doi.​org/​10.​3390/​ijms20205239CrossRefPubMedPubMedCentral
59.
go back to reference Azimzadeh, O., Merl-Pham, J., Subramanian, V., Oleksenko, K., Krumm, F., Mancuso, M., Pasquali, E., Tanaka, I. B., Tanaka, S., Atkinson, M. J., Tapio, S., & Moertl, S. (2023). Late effects of chronic low dose rate total body irradiation on the heart proteome of ApoE−/− mice resemble premature cardiac ageing. Cancers (Basel), 15, 3417. https://doi.org/10.3390/cancers15133417CrossRefPubMed Azimzadeh, O., Merl-Pham, J., Subramanian, V., Oleksenko, K., Krumm, F., Mancuso, M., Pasquali, E., Tanaka, I. B., Tanaka, S., Atkinson, M. J., Tapio, S., & Moertl, S. (2023). Late effects of chronic low dose rate total body irradiation on the heart proteome of ApoE−/− mice resemble premature cardiac ageing. Cancers (Basel), 15, 3417. https://​doi.​org/​10.​3390/​cancers15133417CrossRefPubMed
60.
go back to reference Azimzadeh, O., Subramanian, V., Ständer, S., Merl-Pham, J., Lowe, D., Barjaktarovic, Z., Moertl, S., Raj, K., Atkinson, M. J., & Tapio, S. (2017). Proteome analysis of irradiated endothelial cells reveals persistent alteration in protein degradation and the RhoGDI and NO signalling pathways. International Journal of Radiation Biology, 93, 920–928. https://doi.org/10.1080/09553002.2017.1339332CrossRefPubMed Azimzadeh, O., Subramanian, V., Ständer, S., Merl-Pham, J., Lowe, D., Barjaktarovic, Z., Moertl, S., Raj, K., Atkinson, M. J., & Tapio, S. (2017). Proteome analysis of irradiated endothelial cells reveals persistent alteration in protein degradation and the RhoGDI and NO signalling pathways. International Journal of Radiation Biology, 93, 920–928. https://​doi.​org/​10.​1080/​09553002.​2017.​1339332CrossRefPubMed
61.
62.
go back to reference Schofield, P. N., & Garcia-Bernardo, J. (2007). Radiation, oxidative stress and senescence: The vascular endothelial cell as a common Target. In C. Mothersill, I. Mosse, & C. Seymour (Eds.), Multiple stressors: A challenge for the future (pp. 325–334). Springer.CrossRef Schofield, P. N., & Garcia-Bernardo, J. (2007). Radiation, oxidative stress and senescence: The vascular endothelial cell as a common Target. In C. Mothersill, I. Mosse, & C. Seymour (Eds.), Multiple stressors: A challenge for the future (pp. 325–334). Springer.CrossRef
80.
go back to reference Barjaktarovic, Z., Anastasov, N., Azimzadeh, O., Sriharshan, A., Sarioglu, H., Ueffing, M., Tammio, H., Hakanen, A., Leszczynski, D., Atkinson, M. J., & Tapio, S. (2013). Integrative proteomic and microRNA analysis of primary human coronary artery endothelial cells exposed to low-dose gamma radiation. Radiation and Environmental Biophysics, 52, 87–98. https://doi.org/10.1007/s00411-012-0439-4CrossRefPubMed Barjaktarovic, Z., Anastasov, N., Azimzadeh, O., Sriharshan, A., Sarioglu, H., Ueffing, M., Tammio, H., Hakanen, A., Leszczynski, D., Atkinson, M. J., & Tapio, S. (2013). Integrative proteomic and microRNA analysis of primary human coronary artery endothelial cells exposed to low-dose gamma radiation. Radiation and Environmental Biophysics, 52, 87–98. https://​doi.​org/​10.​1007/​s00411-012-0439-4CrossRefPubMed
85.
go back to reference Kerns, S. L., Fachal, L., Dorling, L., Barnett, G. C., Baran, A., Peterson, D. R., Hollenberg, M., Hao, K., Di Narzo, A., Ahsen, M. E., Pandey, G., Bentzen, S. M., Janelsins, M., Elliott, R. M., Pharoah, P. D. P., Burnet, N. G., Dearnaley, D. P., Gulliford, S. L., Hall, E., … West, C. M. L. (2020). Radiogenomics consortium genome-wide association study meta-analysis of late toxicity after prostate cancer radiotherapy. Journal of the National Cancer Institute, 112, 179–190. https://doi.org/10.1093/jnci/djz075CrossRefPubMed Kerns, S. L., Fachal, L., Dorling, L., Barnett, G. C., Baran, A., Peterson, D. R., Hollenberg, M., Hao, K., Di Narzo, A., Ahsen, M. E., Pandey, G., Bentzen, S. M., Janelsins, M., Elliott, R. M., Pharoah, P. D. P., Burnet, N. G., Dearnaley, D. P., Gulliford, S. L., Hall, E., … West, C. M. L. (2020). Radiogenomics consortium genome-wide association study meta-analysis of late toxicity after prostate cancer radiotherapy. Journal of the National Cancer Institute, 112, 179–190. https://​doi.​org/​10.​1093/​jnci/​djz075CrossRefPubMed
94.
go back to reference Subramanian, V., Seemann, I., Merl-Pham, J., Hauck, S. M., Stewart, F. A., Atkinson, M. J., Tapio, S., & Azimzadeh, O. (2017). Role of TGF beta and PPAR alpha signaling pathways in radiation response of locally exposed heart: integrated global transcriptomics and proteomics analysis. Journal of Proteome Research, 16, 307–318. https://doi.org/10.1021/acs.jproteome.6b00795CrossRefPubMed Subramanian, V., Seemann, I., Merl-Pham, J., Hauck, S. M., Stewart, F. A., Atkinson, M. J., Tapio, S., & Azimzadeh, O. (2017). Role of TGF beta and PPAR alpha signaling pathways in radiation response of locally exposed heart: integrated global transcriptomics and proteomics analysis. Journal of Proteome Research, 16, 307–318. https://​doi.​org/​10.​1021/​acs.​jproteome.​6b00795CrossRefPubMed
95.
go back to reference Watanabe, K., Fujii, H., Takahashi, T., Kodama, M., Aizawa, Y., Ohta, Y., Ono, T., Hasegawa, G., Naito, M., Nakajima, T., Kamijo, Y., Gonzalez, F. J., & Aoyama, T. (2000). Constitutive regulation of cardiac fatty acid metabolism through peroxisome proliferator-activated receptor alpha associated with age-dependent cardiac toxicity. Journal of Biological Chemistry, 275, 22293–22299. https://doi.org/10.1074/jbc.M000248200CrossRefPubMed Watanabe, K., Fujii, H., Takahashi, T., Kodama, M., Aizawa, Y., Ohta, Y., Ono, T., Hasegawa, G., Naito, M., Nakajima, T., Kamijo, Y., Gonzalez, F. J., & Aoyama, T. (2000). Constitutive regulation of cardiac fatty acid metabolism through peroxisome proliferator-activated receptor alpha associated with age-dependent cardiac toxicity. Journal of Biological Chemistry, 275, 22293–22299. https://​doi.​org/​10.​1074/​jbc.​M000248200CrossRefPubMed
97.
go back to reference Dewald, O., Sharma, S., Adrogue, J., Salazar, R., Duerr, G. D., Crapo, J. D., Entman, M. L., & Taegtmeyer, H. (2005). Downregulation of peroxisome proliferator-activated receptor-alpha gene expression in a mouse model of ischemic cardiomyopathy is dependent on reactive oxygen species and prevents lipotoxicity. Circulation, 112, 407–415. https://doi.org/10.1161/CIRCULATIONAHA.105.536318CrossRefPubMed Dewald, O., Sharma, S., Adrogue, J., Salazar, R., Duerr, G. D., Crapo, J. D., Entman, M. L., & Taegtmeyer, H. (2005). Downregulation of peroxisome proliferator-activated receptor-alpha gene expression in a mouse model of ischemic cardiomyopathy is dependent on reactive oxygen species and prevents lipotoxicity. Circulation, 112, 407–415. https://​doi.​org/​10.​1161/​CIRCULATIONAHA.​105.​536318CrossRefPubMed
98.
go back to reference Little, M. P., Azizova, T. V., Bazyka, D., Bouffler, S. D., Cardis, E. S. C., Chekin, S., Chumak, V. V., Cucinotta, F. A., de Vathaire, F., Hall, P., Harrison, J. D., Hildebrandt, G., Ivanov, V., Kashcheev, V. V., Klymenko, S. V., Kreuzer, M., Laurent, O., Ozasa, K., Schneider, T., … Lipshultz, S. E. (2012). Systematic review and meta-analysis of circulatory disease from exposure to low-level ionizing radiation and estimates of potential population mortality risks. Environmental Health Perspectives, 120, 1503–1511. https://doi.org/10.1289/ehp.1204982CrossRefPubMedPubMedCentral Little, M. P., Azizova, T. V., Bazyka, D., Bouffler, S. D., Cardis, E. S. C., Chekin, S., Chumak, V. V., Cucinotta, F. A., de Vathaire, F., Hall, P., Harrison, J. D., Hildebrandt, G., Ivanov, V., Kashcheev, V. V., Klymenko, S. V., Kreuzer, M., Laurent, O., Ozasa, K., Schneider, T., … Lipshultz, S. E. (2012). Systematic review and meta-analysis of circulatory disease from exposure to low-level ionizing radiation and estimates of potential population mortality risks. Environmental Health Perspectives, 120, 1503–1511. https://​doi.​org/​10.​1289/​ehp.​1204982CrossRefPubMedPubMedCentral
99.
100.
101.
go back to reference T. J. McMillan. (2010). Circulatory disease risk report of the independent advisory group on ionising radiation T. J. McMillan. (2010). Circulatory disease risk report of the independent advisory group on ionising radiation
104.
go back to reference Subedi, P., Moertl, S., & Azimzadeh, O. (2022). Omics in radiation biology: Surprised but not disappointed. Radiation, 2, 124.CrossRef Subedi, P., Moertl, S., & Azimzadeh, O. (2022). Omics in radiation biology: Surprised but not disappointed. Radiation, 2, 124.CrossRef
105.
go back to reference Pernot, E., Hall, J., Baatout, S., Benotmane, M. A., Blanchardon, E., Bouffler, S., El Saghire, H., Gomolka, M., Guertler, A., Harms-Ringdahl, M., Jeggo, P., Kreuzer, M., Laurier, D., Lindholm, C., Mkacher, R., Quintens, R., Rothkamm, K., Sabatier, L., Tapio, S., … Cardis, E. (2012). Ionizing radiation biomarkers for potential use in epidemiological studies. Mutation Research, 751, 258–286. https://doi.org/10.1016/j.mrrev.2012.05.003CrossRefPubMed Pernot, E., Hall, J., Baatout, S., Benotmane, M. A., Blanchardon, E., Bouffler, S., El Saghire, H., Gomolka, M., Guertler, A., Harms-Ringdahl, M., Jeggo, P., Kreuzer, M., Laurier, D., Lindholm, C., Mkacher, R., Quintens, R., Rothkamm, K., Sabatier, L., Tapio, S., … Cardis, E. (2012). Ionizing radiation biomarkers for potential use in epidemiological studies. Mutation Research, 751, 258–286. https://​doi.​org/​10.​1016/​j.​mrrev.​2012.​05.​003CrossRefPubMed
106.
go back to reference Azimzadeh, O., Moertl, S., Ramadan, R., Baselet, B., Laiakis, E. C., Sebastian, S., Beaton, D., Hartikainen, J. M., Kaiser, J. C., Beheshti, A., Salomaa, S., Chauhan, V., & Hamada, N. (2022). Application of radiation omics in the development of adverse outcome pathway networks: An example of radiation-induced cardiovascular disease. International Journal of Radiation Biology, 98, 1722–1751. https://doi.org/10.1080/09553002.2022.2110325CrossRefPubMed Azimzadeh, O., Moertl, S., Ramadan, R., Baselet, B., Laiakis, E. C., Sebastian, S., Beaton, D., Hartikainen, J. M., Kaiser, J. C., Beheshti, A., Salomaa, S., Chauhan, V., & Hamada, N. (2022). Application of radiation omics in the development of adverse outcome pathway networks: An example of radiation-induced cardiovascular disease. International Journal of Radiation Biology, 98, 1722–1751. https://​doi.​org/​10.​1080/​09553002.​2022.​2110325CrossRefPubMed
107.
110.
go back to reference Preston, R. J., Boice, J. D. J., Brill, A. B., Chakraborty, R., Conolly, R., Hoffman, F. O., Hornung, R. W., Kocher, D. C., Land, C. E., Shore, R. E., & Woloschak, G. E. (2013). Uncertainties in estimating health risks associated with exposure to ionising radiation. Journal of Radiological Protection, 33, 573–588. https://doi.org/10.1088/0952-4746/33/3/573CrossRefPubMed Preston, R. J., Boice, J. D. J., Brill, A. B., Chakraborty, R., Conolly, R., Hoffman, F. O., Hornung, R. W., Kocher, D. C., Land, C. E., Shore, R. E., & Woloschak, G. E. (2013). Uncertainties in estimating health risks associated with exposure to ionising radiation. Journal of Radiological Protection, 33, 573–588. https://​doi.​org/​10.​1088/​0952-4746/​33/​3/​573CrossRefPubMed
Metadata
Title
Cohort Studies and Multi-omics Approaches to Low-Dose Ionizing Radiation-Induced Cardiovascular Disease: A Comprehensive Review
Authors
Xumin Zong
Lin Zhu
Yan Wang
Jinhan Wang
Yeqing Gu
Qiang Liu
Publication date
13-11-2024
Publisher
Springer US
Published in
Cardiovascular Toxicology / Issue 1/2025
Print ISSN: 1530-7905
Electronic ISSN: 1559-0259
DOI
https://doi.org/10.1007/s12012-024-09943-5

Keynote series | Spotlight on menopause

Menopause can have a significant impact on the body, with effects ranging beyond the endocrine and reproductive systems. Learn about the systemic effects of menopause, so you can help patients in your clinics through the transition.   

Prof. Martha Hickey
Dr. Claudia Barth
Dr. Samar El Khoudary
Developed by: Springer Medicine
Watch now
Video

A quick guide to ECGs

Improve your ECG interpretation skills with this comprehensive, rapid, interactive course. Expert advice provides detailed feedback as you work through 50 ECGs covering the most common cardiac presentations to ensure your practice stays up to date. 

PD Dr. Carsten W. Israel
Developed by: Springer Medizin
Start the cases