Hostname: page-component-586b7cd67f-t7fkt Total loading time: 0 Render date: 2024-11-23T01:14:49.291Z Has data issue: false hasContentIssue false
  • English
  • Français

Les effets des rayonnements ionisants sur le systèmecardiovasculaire

Published online by Cambridge University Press:  16 December 2011

F. Milliat ,
M. Benderitter  and
M.-H. Gaugler
F. Milliat
Affiliation:
Institut de radioprotection et de sûreté nucléaire, DRPH, SRBE, Laboratoire de radiopathologie et de thérapies expérimentales (LRTE), Fontenay-aux-Roses, France
M. Benderitter
Affiliation:
Institut de radioprotection et de sûreté nucléaire, DRPH, SRBE, Laboratoire de radiopathologie et de thérapies expérimentales (LRTE), Fontenay-aux-Roses, France
M.-H. Gaugler
Affiliation:
Institut de radioprotection et de sûreté nucléaire, DRPH, SRBE, Laboratoire de radiopathologie et de thérapies expérimentales (LRTE), Fontenay-aux-Roses, France
Get access

Abstract

Le traitement par radiothérapie des cancers des sphères thoracique, médiastinale et ORLest associé à un risque de complications cardiovasculaires. Les patients traités et guérisde leur cancer sont de plus en plus nombreux, vivent de plus en plus longtemps, et leurdevenir à long terme doit être pris en considération. Les complications cardiovasculairesassociées principalement au traitement des cancers du sein, du lymphome de Hodgkin et destumeurs de la tête et du cou se manifestent de manière insidieuse et chronique. Leursurvenue est liée à de nombreux facteurs comme l’âge du patient au moment du traitement,le nombre d’années suivant la radiothérapie, la dose et le volume au cœur et aux grosvaisseaux (artères coronaires et carotides) ou encore l’association avec les autresfacteurs de risque cardiovasculaire traditionnels. Les mécanismes physiopathologiques sontmal connus. Même si des similitudes avec l’athérosclérose liée à l’âge sont établies, lesspécificités et les particularités de l’athérosclérose radio-induite pour des fortes dosesd’irradiation restent à établir. Pour des faibles niveaux d’exposition aux rayonnementsionisants, des études épidémiologiques récentes suggèrent aussi un risque accru dedévelopper des pathologies cardiovasculaires. L’amélioration des connaissances sur lesmécanismes lésionnels à l’origine des pathologies cardiovasculaires radio-induites etl’identification plus précise des populations à risque devraient permettre dans le futurune prise en charge plus efficace de ces patients à risque vasculaire.

Keywords

Ionising radiationradiotherapycardiovascular risk
Type
Research Article
Information
Radioprotection , Volume 46 , Issue 4 , October 2011 , pp. 493 - 510
Copyright
© EDP Sciences, 2011

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Références

Bentzen, S.M.,Dorr, W.,Anscher, M.S.,Denham, J.W.,Hauer-Jensen, M.,Marks, L.B.,Williams, J. (2003) Normal tissue effects: Reporting and analysis, Semin. Radiat. Oncol. 13, 189-202. Google ScholarPubMed
Bolling, T., Willich, N. (2010) Long-term overall and cardiovascular mortality after childhood cancer: The problem of retrospective estimated radiation doses, J. Clin. Oncol. 28, e436; author reply e437-438. Google ScholarPubMed
Cheng, S.W.,Wu, L.L.,Ting, A.C.,Lau, H.,Lam, L.K.,Wei, W.I. (1999) Irradiation-induced extracranial carotid stenosis in patients with head and neck malignancies, Am. J. Surg. 178, 323-328. Google ScholarPubMed
Chou, C.H.,Chen, S.U.,Cheng, J.C. (2009) Radiation-induced interleukin-6 expression through mapk/p38/nf-kappab signaling pathway and the resultant antiapoptotic effect on endothelial cells through mcl-1 expression with sil6-ralpha, Int. J. Radiat. Oncol. Biol. Phys. 75, 1553-1561. Google ScholarPubMed
Clarke, M., Collins, R., Darby, S., Davies, C., Elphinstone, P., Evans, E., Godwin, J., Gray, R., Hicks, C., James, S. and others (2005) Effects of radiotherapy and of differences in the extent of surgery for early breast cancer on local recurrence and 15-year survival: An overview of the randomised trials, Lancet 366, 2087-2106. Google ScholarPubMed
Coon, A.B.,Dickler, A.,Kirk, M.C.,Liao, Y.,Shah, A.P.,Strauss, J.B.,Chen, S.,Turian, J.,Griem, K.L. (2010) Tomotherapy and multifield intensity-modulated radiotherapy planning reduce cardiac doses in left-sided breast cancer patients with unfavorable cardiac anatomy, Int. J. Radiat. Oncol. Biol. Phys. 78, 104-110. Google ScholarPubMed
Cottin, Y.,Kollum, M.,Kolodgie, F.D.,Chan, R.C.,Kim, H.S.,Vodovotz, Y.,Virmani, R.,Waksman, R.,Yazdi, H. (2001) Intravascular radiation accelerates atherosclerotic lesion formation of hypercholesteremic rabbits, Cardiovasc. Radiat. Med. 2, 231-240. Google ScholarPubMed
Darby, S.C.,McGale, P.,Taylor, C.W.,Peto, R. (2005) Long-term mortality from heart disease and lung cancer after radiotherapy for early breast cancer: Prospective cohort study of about 300,000 women in us seer cancer registries, Lancet Oncol. 6, 557-565. Google ScholarPubMed
Demirci, S.,Nam, J.,Hubbs, J.L.,Nguyen, T.,Marks, L.B. (2009) Radiation-induced cardiac toxicity after therapy for breast cancer: Interaction between treatment era and follow-up duration, Int. J. Radiat. Oncol. Biol. Phys. 73, 980-987. Google ScholarPubMed
Dorresteijn, L.D.,Kappelle, A.C.,Boogerd, W.,Klokman, W.J.,Balm, A.J.,Keus, R.B., van Leeuwen, F.E.,Bartelink, H. (2002) Increased risk of ischemic stroke after radiotherapy on the neck in patients younger than 60 years, J. Clin. Oncol. 20, 282-288. Google ScholarPubMed
Dorresteijn, L.D.,Kappelle, A.C.,Scholz, N.M.,Munneke, M.,Scholma, J.T.,Balm, A.J.,Bartelink, H.,Boogerd, W. (2005) Increased carotid wall thickening after radiotherapy on the neck, Eur. J. Cancer 41, 1026-1030. Google Scholar
Early Breast Cancer Trialists’ Collaborative Group (EBCTCG) (2000) Favourable and unfavourable effects on long-term survival of radiotherapy for early breast cancer: An overview of the randomised trials. Early breast cancer trialists’ collaborative group, Lancet 355, 1757-1770.
Fajardo, L.F. (2005) The pathology of ionizing radiation as defined by morphologic patterns, Acta Oncol. 44, 13-22. Google ScholarPubMed
Fossa, S.D., Gilbert, E., Dores, G.M., Chen, J., McGlynn, K.A., Schonfeld, S., Storm, H., Hall, P., Holowaty, E., Andersen, A. and others (2007) Noncancer causes of death in survivors of testicular cancer, J. Natl. Cancer. Inst. 99, 533-544.
Gaugler, M.H. (2005) A unifying system: Does the vascular endothelium have a role to play in multi-organ failure following radiation exposure? BJR Suppl. 27, 100-105. Google Scholar
Gaugler, M.H.,Drouet, F.,Krempf, M. (2011) radiotherapy and atherosclerosis: Current data and issues, Med. Sci. (Paris) 26, 740-746. Google ScholarPubMed
Gaugler, M.H.,Squiban, C., van der Meeren, A.,Bertho, J.M.,Vandamme, M.,Mouthon, M.A. (1997) Late and persistent up-regulation of intercellular adhesion molecule-1 (icam-1) expression by ionizing radiation in human endothelial cells in vitro, Int. J. Radiat. Biol. 72, 201-209. Google ScholarPubMed
Gaugler, M.H.,Vereycken-Holler, V.,Squiban, C.,Aigueperse, J. (2004) Pecam-1 (cd31) is required for interactions of platelets with endothelial cells after irradiation, J. Thromb. Haemost. 2, 2020-2026. Google ScholarPubMed
Gaugler, M.H.,Vereycken-Holler, V.,Squiban, C.,Vandamme, M.,Vozenin-Brotons, M.C.,Benderitter, M. (2005) Pravastatin limits endothelial activation after irradiation and decreases the resulting inflammatory and thrombotic responses, Radiat. Res. 163, 479-487. Google ScholarPubMed
Gerber, T.C.,Carr, J.J.,Arai, A.E.,Dixon, R.L.,Ferrari, V.A.,Gomes, A.S.,Heller, G.V.,McCollough, C.H.,McNitt-Gray, M.F.,Mettler, F.A. et al. (2009) Ionizing radiation in cardiac imaging: A science advisory from the american heart association committee on cardiac imaging of the council on clinical cardiology and committee on cardiovascular imaging and intervention of the council on cardiovascular radiology and intervention, Circulation 119, 1056-1065. Google ScholarPubMed
Guo, W.Y.,Wang, G.J.,Wang, P.,Chen, Q.,Tan, Y.,Cai, L. (2010) Acceleration of diabetic wound healing by low-dose radiation is associated with peripheral mobilization of bone marrow stem cells, Radiat. Res. 174, 467-479. Google ScholarPubMed
Halle, M.,Gabrielsen, A.,Paulsson-Berne, G.,Gahm, C.,Agardh, H.E.,Farnebo, F.,Tornvall, P. (2010) Sustained inflammation due to nuclear factor-kappa b activation in irradiated human arteries, J. Am. Coll. Cardiol. 55, 1227-1236. Google ScholarPubMed
Halle, M.,Hall, P.,Tornvall, P. (2011) Cardiovascular disease associated with radiotherapy: Activation of nuclear factor kappa-b, J. Int. Med. 269, 469-477. Google ScholarPubMed
Harris, E.E.,Correa, C.,Hwang, W.T.,Liao, J.,Litt, H.I.,Ferrari, V.A.,Solin, L.J. (2006) Late cardiac mortality and morbidity in early-stage breast cancer patients after breast-conservation treatment, J. Clin. Oncol. 24, 4100-4106. Google ScholarPubMed
Hauptmann, M.,Mohan, A.K.,Doody, M.M.,Linet, M.S.,Mabuchi, K. (2003) Mortality from diseases of the circulatory system in radiologic technologists in the united states, Am. J. Epidemiol. 157, 239-248. Google ScholarPubMed
Heckmann, M.,Douwes, K.,Peter, R.,Degitz, K. (1998) Vascular activation of adhesion molecule mrna and cell surface expression by ionizing radiation, Exp. Cell. Res. 238, 148-154. Google ScholarPubMed
Heidenreich, P.A.,Kapoor, J.R. (2009) Radiation induced heart disease: Systemic disorders in heart disease, Heart 95, 252-258. Google ScholarPubMed
Heissig, B.,Rafii, S.,Akiyama, H.,Ohki, Y.,Sato, Y.,Rafael, T.,Zhu, Z.,Hicklin, D.J.,Okumura, K.,Ogawa, H. et al. (2005) Low-dose irradiation promotes tissue revascularization through vegf release from mast cells and mmp-9-mediated progenitor cell mobilization, J. Exp. Med. 202, 739-750. Google ScholarPubMed
Hooning, M.J.,Botma, A.,Aleman, B.M.,Baaijens, M.H.,Bartelink, H.,Klijn, J.G.,Taylor, C.W., van Leeuwen, F.E. (2007) Long-term risk of cardiovascular disease in 10-year survivors of breast cancer, J. Natl. Cancer Inst. 99, 365-375. Google ScholarPubMed
Houdart, E.,Mounayer, C.,Chapot, R.,Saint-Maurice, J.P.,Merland, J.J. (2001) Carotid stenting for radiation-induced stenoses: A report of 7 cases, Stroke 32, 118-121. Google ScholarPubMed
Hoving, S., Heeneman, S., Gijbels, M.J., te Poele, J.A.,Russell, N.S.,Daemen, M.J.,Stewart, F.A. (2008) Single-dose and fractionated irradiation promote initiation and progression of atherosclerosis and induce an inflammatory plaque phenotype in apoe(-/-) mice, Int. J. Radiat. Oncol. Biol. Phys. 71, 848-857. Google ScholarPubMed
Jahroudi, N.,Ardekani, A.M.,Greenberger, J.S. (1996) Ionizing irradiation increases transcription of the von willebrand factor gene in endothelial cells, Blood 88, 3801-3814. Google ScholarPubMed
Little, M.P.,Tawn, E.J.,Tzoulaki, I.,Wakeford, R.,Hildebrandt, G.,Paris, F.,Tapio, S.,Elliott, P. (2008) A systematic review of epidemiological associations between low and moderate doses of ionizing radiation and late cardiovascular effects, and their possible mechanisms, Radiat. Res. 169, 99-109. Google ScholarPubMed
Little, M.P.,Tawn, E.J.,Tzoulaki, I.,Wakeford, R.,Hildebrandt, G.,Paris, F.,Tapio, S.,Elliott, P. (2010) Review and meta-analysis of epidemiological associations between low/moderate doses of ionizing radiation and circulatory disease risks, and their possible mechanisms, Radiat. Environ. Biophys. 49, 139-153. Google ScholarPubMed
McDonald, S.,Rubin, P.,Phillips, T.L.,Marks, L.B. (1995) Injury to the lung from cancer therapy: Clinical syndromes, measurable endpoints, and potential scoring systems, Int. J. Radiat. Oncol. Biol. Phys. 31, 1187-1203. Google ScholarPubMed
McGale, P.,Darby, S.C. (2005) Low doses of ionizing radiation and circulatory diseases: A systematic review of the published epidemiological evidence, Radiat. Res. 163, 247-257. Google ScholarPubMed
McGeoghegan, D.,Binks, K.,Gillies, M.,Jones, S.,Whaley, S. (2008) The non-cancer mortality experience of male workers at british nuclear fuels plc, 1946-2005, Int. J. Epidemiol. 37, 506-518. Google ScholarPubMed
Mettler, F.A. Jr.,Thomadsen, B.R.,Bhargavan, M.,Gilley, D.B.,Gray, J.E.,Lipoti, J.A.,McCrohan, J.,Yoshizumi, T.T.,Mahesh, M. (2008) Medical radiation exposure in the u.S. In 2006: Preliminary results, Health. Phys. 95, 502-507. Google ScholarPubMed
Metz-Flamant, C.,Bonaventure, A.,Milliat, F.,Tirmarche, M.,Laurier, D.,Bernier, M.O. (2009) [low doses of ionizing radiation and risk of cardiovascular disease: A review of epidemiological studies], Rev. Epidémiol. Santé Publique 57, 347-359. Google Scholar
Milliat, F.,Francois, A.,Isoir, M. et al. (2006) Influence of endothelial cells on vascular smooth muscle cells phenotype after irradiation: Implication in radiation-induced vascular damages, Am. J. Pathol. 169, 1484-1495. Google ScholarPubMed
Milliat, F.,Francois, A.,Tamarat, R.,Benderitter, M. (2008a) role of endothelium in radiation-induced normal tissue damages, Ann. Cardiol. Angeiol. (Paris) 57, 139-148. Google ScholarPubMed
Milliat, F.,Sabourin, J.C.,Tarlet, G.,Holler, V.,Deutsch, E.,Buard, V.,Tamarat, R.,Atfi, A.,Benderitter, M.,Francois, A. (2008b) Essential role of plasminogen activator inhibitor type-1 in radiation enteropathy, Am. J. Pathol. 172, 691-701. Google ScholarPubMed
Miltenyi, Z.,Keresztes, K.,Garai, I.,Edes, I.,Galajda, Z.,Toth, L.,Illes, A. (2004) Radiation-induced coronary artery disease in hodgkin’s disease, Cardiovasc. Radiat. Med. 5, 38-43. Google ScholarPubMed
Mitchel, R.E.,Hasu, M.,Bugden, M.,Wyatt, H.,Little, M.P.,Gola, A.,Hildebrandt, G.,Priest, N.D.,Whitman, S.C. (2011) Low-dose radiation exposure and atherosclerosis in apoe(-/-) mice, Radiat. Res. 175, 665-675. Google ScholarPubMed
Modrall, J.G.,Sadjadi, J. (2003) Early and late presentations of radiation arteritis, Semin. Vasc. Surg. 16, 209-214. Google ScholarPubMed
Mouthon, M.A., Vereycken-Holler, V., Van der Meeren, A.,Gaugler, M.H. (2003) Irradiation increases the interactions of platelets with the endothelium in vivo: Analysis by intravital microscopy, Radiat. Res. 160, 593-599. Google ScholarPubMed
Paszat, L.F.,Mackillop, W.J.,Groome, P.A.,Boyd, C.,Schulze, K.,Holowaty, E. (1998) Mortality from myocardial infarction after adjuvant radiotherapy for breast cancer in the surveillance, epidemiology, and end-results cancer registries, J. Clin. Oncol. 16, 2625-2631. Google ScholarPubMed
Peiro, C.,Redondo, J.,Rodriguez-Martinez, M.A.,Angulo, J.,Marin, J.,Sanchez-Ferrer, C.F. (1995) Influence of endothelium on cultured vascular smooth muscle cell proliferation, Hypertension 25, 748-751. Google ScholarPubMed
Quarmby, S.,Hunter, R.D.,Kumar, S. (2000) Irradiation induced expression of cd31, icam-1 and vcam-1 in human microvascular endothelial cells, Anticancer Res. 20, 3375-3381. Google ScholarPubMed
Quarmby, S.,Kumar, P.,Wang, J.,Macro, J.A.,Hutchinson, J.J.,Hunter, R.D.,Kumar, S. (1999) Irradiation induces upregulation of cd31 in human endothelial cells, Arterioscler Thromb. Vasc. Biol. 19, 588-597. Google ScholarPubMed
Richter, K.K.,Fink, L.M.,Hughes, B.M.,Sung, C.C.,Hauer-Jensen, M. (1997) Is the loss of endothelial thrombomodulin involved in the mechanism of chronicity in late radiation enteropathy? Radiother. Oncol. 44, 65-71. Google ScholarPubMed
Rodel, F.,Keilholz, L.,Herrmann, M.,Sauer, R.,Hildebrandt, G. (2007) Radiobiological mechanisms in inflammatory diseases of low-dose radiation therapy, Int. J. Radiat. Biol. 83, 357-366. Google ScholarPubMed
Rodel, F.,Hofmann, D.,Auer, J.,Keilholz, L.,Rollinghoff, M.,Sauer, R.,Beuscher, H.U. (2008) The anti-inflammatory effect of low-dose radiation therapy involves a diminished ccl20 chemokine expression and granulocyte/endothelial cell adhesion, Strahlenther Onkol. 184, 41-47. Google ScholarPubMed
Ross, R. (1999) Atherosclerosis – an inflammatory disease, N. Engl. J. Med. 340, 115-126. Google ScholarPubMed
Rubin, D.B., Drab, E.A., Ts’ao, C.H., Gardner, D.,Ward, W.F. (1985) Prostacyclin synthesis in irradiated endothelial cells cultured from bovine aorta, J. Appl. Physiol. 58, 592-597. Google ScholarPubMed
Russell, N.S., Hoving, S., Heeneman, S., Hage, J.J., Woerdeman, L.A., de Bree, R., Lohuis, P.J., Smeele, L., Cleutjens, J., Valenkamp, A. and others (2009) Novel insights into pathological changes in muscular arteries of radiotherapy patients, Radiother. Oncol. 92, 477-483. Google ScholarPubMed
Seegenschmiedt, M.H.,Micke, O.,Willich, N. (2004) Radiation therapy for nonmalignant diseases in germany. Current concepts and future perspectives, Strahlenther Onkol. 180, 718-730. Google ScholarPubMed
Senkus-Konefka, E.,Jassem, J. (2007) Cardiovascular effects of breast cancer radiotherapy, Cancer Treat. Rev. 33, 578-593. Google ScholarPubMed
Seppenwoolde, Y., De Jaeger, K.,Boersma, L.J.,Belderbos, J.S.,Lebesque, J.V. (2004) Regional differences in lung radiosensitivity after radiotherapy for non-small-cell lung cancer, Int. J. Radiat. Oncol. Biol. Phys. 60, 748-758. Google ScholarPubMed
Shapiro, C.L.,Hardenbergh, P.H.,Gelman, R.,Blanks, D.,Hauptman, P.,Recht, A.,Hayes, D.F.,Harris, J.,Henderson, I.C. (1998) Cardiac effects of adjuvant doxorubicin and radiation therapy in breast cancer patients, J. Clin. Oncol. 16, 3493-3501. Google ScholarPubMed
Shimizu, Y., Kodama, K., Nishi, N., Kasagi, F., Suyama, A., Soda, M., Grant, E.J., Sugiyama, H., Sakata, R., Moriwaki, H. et al. (2010) Radiation exposure and circulatory disease risk: Hiroshima and Nagasaki atomic bomb survivor data, 1950-2003, BMJ 340, b5349. Google Scholar
Silverberg, G.D.,Britt, R.H.,Goffinet, D.R. (1978) Radiation-induced carotid artery disease, Cancer 41, 130-137. Google ScholarPubMed
Smith, G.L.,Smith, B.D.,Buchholz, T.A.,Giordano, S.H.,Garden, A.S.,Woodward, W.A.,Krumholz, H.M.,Weber, R.S.,Ang, K.K.,Rosenthal, D.I. (2008) Cerebrovascular disease risk in older head and neck cancer patients after radiotherapy, J. Clin. Oncol. 26, 5119-5125. Google ScholarPubMed
Stewart, F.A., Heeneman, S., Te Poele, J.,Kruse, J.,Russell, N.S.,Gijbels, M.,Daemen, M. (2006) Ionizing radiation accelerates the development of atherosclerotic lesions in apoe-/- mice and predisposes to an inflammatory plaque phenotype prone to hemorrhage, Am. J. Pathol. 168, 649-658. Google Scholar
Sugihara, T.,Hattori, Y.,Yamamoto, Y.,Qi, F.,Ichikawa, R.,Sato, A.,Liu, M.Y.,Abe, K.,Kanno, M. (1999) Preferential impairment of nitric oxide-mediated endothelium-dependent relaxation in human cervical arteries after irradiation, Circulation 100, 635-641. Google ScholarPubMed
Swerdlow, A.J., Higgins, C.D., Smith, P., Cunningham, D., Hancock, B.W., Horwich, A., Hoskin, P.J., Lister, A., Radford, J.A., Rohatiner, A.Z. and others (2007) Myocardial infarction mortality risk after treatment for hodgkin disease: A collaborative british cohort study, J. Natl. Cancer Inst. 99, 206-214. Google ScholarPubMed
Taylor, C.W.,Nisbet, A.,McGale, P.,Darby, S.C. (2007) Cardiac exposures in breast cancer radiotherapy: 1950s-1990s, Int. J. Radiat. Oncol. Biol. Phys. 69, 1484-1495. Google ScholarPubMed
Taylor, C.W.,Povall, J.M.,McGale, P.,Nisbet, A.,Dodwell, D.,Smith, J.T.,Darby, S.C. (2008) Cardiac dose from tangential breast cancer radiotherapy in the year 2006, Int. J. Radiat. Oncol. Biol. Phys. 72, 501-507. Google ScholarPubMed
Tribble, D.L.,Barcellos-Hoff, M.H.,Chu, B.M.,Gong, E.L. (1999) Ionizing radiation accelerates aortic lesion formation in fat-fed mice via sod-inhibitable processes, Arterioscler Thromb. Vasc. Biol. 19, 1387-1392. Google ScholarPubMed
Tsoutsou, P.G.,Koukourakis, M.I. (2006) Radiation pneumonitis and fibrosis: Mechanisms underlying its pathogenesis and implications for future research, Int. J. Radiat. Oncol. Biol. Phys. 66, 1281-1293. Google ScholarPubMed
Tukenova, M., Guibout, C., Oberlin, O., Doyon, F., Mousannif, A., Haddy, N., Guerin, S., Pacquement, H., Aouba, A., Hawkins, M. and others (2010) Role of cancer treatment in long-term overall and cardiovascular mortality after childhood cancer, J. Clin. Oncol. 28, 1308-1315. Google ScholarPubMed
van Luijk, P.,Faber, H.,Meertens, H.,Schippers, J.M.,Langendijk, J.A.,Brandenburg, S.,Kampinga, H.H.,Coppes, R.P. (2007) The impact of heart irradiation on dose-volume effects in the rat lung, Int. J. Radiat. Oncol. Biol. Phys. 69, 552-559. Google ScholarPubMed
Veinot, J.P.,Edwards, W.D. (1996) Pathology of radiation-induced heart disease: A surgical and autopsy study of 27 cases, Hum. Pathol. 27, 766-773. Google ScholarPubMed
Vereycken-Holler, V.,Aigueperse, J.,Gaugler, M.H. (2002) Radiation effects on circulating and endothelial cell interactions studied by quantitative real-time videomicroscopy, Int. J. Radiat. Biol. 78, 923-930. Google ScholarPubMed
Verheij, M.,Dewit, L.G., van Mourik, J.A. (1995) The effect of ionizing radiation on endothelial tissue factor activity and its cellular localization, Thromb. Haemost. 73, 894-895. Google ScholarPubMed
Verheij, M.,Dewit, L., van Mourik, J.A. (1997) Radiation-induced von willebrand factor release, Blood 90, 2109-2110. Google ScholarPubMed
Yamada, M.,Wong, F.L.,Fujiwara, S.,Akahoshi, M.,Suzuki, G. (2004) Noncancer disease incidence in atomic bomb survivors, 1958-1998, Radiat. Res. 161, 622-632. Google ScholarPubMed
Zhang, C.,Tan, Y.,Guo, W.,Li, C.,Ji, S.,Li, X.,Cai, L. (2009) Attenuation of diabetes-induced renal dysfunction by multiple exposures to low-dose radiation is associated with the suppression of systemic and renal inflammation, Am. J. Physiol. Endocrinol. Metab. 297, E1366-1377. Google ScholarPubMed
Zhang, C.,Jin, S.,Guo, W.,Li, C.,Li, X.,Rane, M.J.,Wang, G.,Cai, L. (2011) Attenuation of diabetes-induced cardiac inflammation and pathological remodeling by low-dose radiation, Radiat. Res. 175, 307-321. Google ScholarPubMed
Zhou, Q.,Zhao, Y.,Li, P.,Bai, X.,Ruan, C. (1992) Thrombomodulin as a marker of radiation-induced endothelial cell injury, Radiat. Res. 131, 285-289. Google ScholarPubMed