Skip to main content
Erschienen in: Journal of Bone and Mineral Metabolism 5/2014

01.09.2014 | Original Article

Low level irradiation in mice can lead to enhanced trabecular bone morphology

verfasst von: Lamya Karim, Stefan Judex

Erschienen in: Journal of Bone and Mineral Metabolism | Ausgabe 5/2014

Einloggen, um Zugang zu erhalten

Abstract

Charged particle radiation such as iron ions and their secondary fragmentation products are of particular concern to the skeleton due to their high charge and energy deposition. However, little is known about the long-term effects of these particles on trabecular and cortical bone morphology when applied at relatively low levels. We hypothesized that even a 4.4 cGy dose of a complex secondary iron ion radiation field will compromise skeletal quantity and architecture in adult mice. One year after radiation exposure and compared to age-matched controls, 4.4 cGy irradiated mice had 51 % more trabecular bone, 56 % greater trabecular bone volume fraction, 16 % greater trabecular number, and 17 % less trabecular separation in the distal metaphysis of the femur. Similar to the metaphysis, trabecular bone of the distal femoral epiphysis in 4.4 cGy mice had 33 % more trabecular bone, 31 % greater trabecular bone volume fraction, and a 33 % smaller structural model index. Cortical bone morphology, whole bone mechanical properties, and lower leg muscle mass were unaffected. When compared to two additional groups, irradiated at either 8.9 or 17.8 cGy, a (negative) dose response relationship was observed for trabecular bone in the metaphysis but not in the epiphysis. In contrast to our original hypothesis, these data indicated that a secondary field of low-level, high-linear energy transfer iron radiation may cause long-term augmentation, rather than deterioration, of trabecular bone in the femoral metaphysis and epiphysis of mice.
Literatur
1.
Zurück zum Zitat Hellweg CE, Baumstark-Khan C (2007) Getting ready for the manned mission to Mars: the astronauts’ risk from space radiation. Naturwissenschaften 94:517–526PubMedCrossRef Hellweg CE, Baumstark-Khan C (2007) Getting ready for the manned mission to Mars: the astronauts’ risk from space radiation. Naturwissenschaften 94:517–526PubMedCrossRef
2.
Zurück zum Zitat Willey JS, Lloyd SA, Nelson GA, Bateman TA (2011) Space radiation and bone loss. Gravit Space Biol Bull 25:14–21PubMedCentralPubMed Willey JS, Lloyd SA, Nelson GA, Bateman TA (2011) Space radiation and bone loss. Gravit Space Biol Bull 25:14–21PubMedCentralPubMed
3.
Zurück zum Zitat Orwoll ES, Adler RA, Amin S, Binkley N, Lewiecki EM, Petak SM, Shapses SA, Sinaki M, Watts NB, Sibonga JD (2013) Skeletal health in long-duration astronauts: nature, assessment, and management recommendations from the NASA bone summit. J Bone Miner Res 28:1243–1255PubMedCrossRef Orwoll ES, Adler RA, Amin S, Binkley N, Lewiecki EM, Petak SM, Shapses SA, Sinaki M, Watts NB, Sibonga JD (2013) Skeletal health in long-duration astronauts: nature, assessment, and management recommendations from the NASA bone summit. J Bone Miner Res 28:1243–1255PubMedCrossRef
4.
Zurück zum Zitat Judex S, Zhang W, Donahue LR, Ozcivici E (2013) Genetic loci that control the loss and regain of trabecular bone during unloading and reambulation. J Bone Miner Res 28:1537–1549PubMedCrossRef Judex S, Zhang W, Donahue LR, Ozcivici E (2013) Genetic loci that control the loss and regain of trabecular bone during unloading and reambulation. J Bone Miner Res 28:1537–1549PubMedCrossRef
5.
6.
Zurück zum Zitat Kim MHY, De Angelis G, Cucinotta FA (2011) Probabilistic assessment of radiation risk for astronauts in space missions. Acta Astronaut 68:747–759CrossRef Kim MHY, De Angelis G, Cucinotta FA (2011) Probabilistic assessment of radiation risk for astronauts in space missions. Acta Astronaut 68:747–759CrossRef
7.
Zurück zum Zitat Adriani O, Barbarino GC, Bazilevskaya GA, Bellotti R, Boezio M et al (2011) PAMELA measurements of cosmic-ray proton and helium spectra. Science 332:69–72PubMedCrossRef Adriani O, Barbarino GC, Bazilevskaya GA, Bellotti R, Boezio M et al (2011) PAMELA measurements of cosmic-ray proton and helium spectra. Science 332:69–72PubMedCrossRef
8.
Zurück zum Zitat Williams HJ, Davies AM (2006) The effect of X-rays on bone: a pictorial review. Eur Radiol 16:619–633PubMedCrossRef Williams HJ, Davies AM (2006) The effect of X-rays on bone: a pictorial review. Eur Radiol 16:619–633PubMedCrossRef
9.
Zurück zum Zitat Green DE, Adler BJ, Chan ME, Rubin CT (2012) Devastation of adult stem cell pools by irradiation precedes collapse of trabecular bone quality and quantity. J Bone Miner Res 27:749–759PubMedCrossRef Green DE, Adler BJ, Chan ME, Rubin CT (2012) Devastation of adult stem cell pools by irradiation precedes collapse of trabecular bone quality and quantity. J Bone Miner Res 27:749–759PubMedCrossRef
10.
Zurück zum Zitat Alwood JS, Kumar A, Tran LH, Wang A, Limoli CL, Globus RK (2012) Low-dose, ionizing radiation and age-related changes in skeletal microarchitecture. J Aging Res 2012:481983PubMedCentralPubMedCrossRef Alwood JS, Kumar A, Tran LH, Wang A, Limoli CL, Globus RK (2012) Low-dose, ionizing radiation and age-related changes in skeletal microarchitecture. J Aging Res 2012:481983PubMedCentralPubMedCrossRef
11.
Zurück zum Zitat Lloyd SA, Bandstra ER, Travis ND, Nelson GA, Bourland JD, Pecaut MJ, Gridley DS, Willey JS, Bateman TA (2008) Spaceflight-relevant types of ionizing radiation and cortical bone: potential LET effect? Adv Space Res 42:1889–1897PubMedCentralPubMedCrossRef Lloyd SA, Bandstra ER, Travis ND, Nelson GA, Bourland JD, Pecaut MJ, Gridley DS, Willey JS, Bateman TA (2008) Spaceflight-relevant types of ionizing radiation and cortical bone: potential LET effect? Adv Space Res 42:1889–1897PubMedCentralPubMedCrossRef
12.
Zurück zum Zitat Kamada T, Tsujii H, Tsuji H, Yanagi T, Mizoe JE, Miyamoto T, Kato H, Yamada S, Morita S, Yoshikawa K, Kandatsu S, Tateishi A, Working Group for the Bone and Soft Tissue Sarcomas (2002) Efficacy and safety of carbon ion radiotherapy in bone and soft tissue sarcomas. J Clin Oncol 20:4466–4471 Kamada T, Tsujii H, Tsuji H, Yanagi T, Mizoe JE, Miyamoto T, Kato H, Yamada S, Morita S, Yoshikawa K, Kandatsu S, Tateishi A, Working Group for the Bone and Soft Tissue Sarcomas (2002) Efficacy and safety of carbon ion radiotherapy in bone and soft tissue sarcomas. J Clin Oncol 20:4466–4471
13.
Zurück zum Zitat Hamilton SA, Pecaut MJ, Gridley DS, Travis ND, Bandstra ER, Willey JS, Nelson GA, Bateman TA (2006) A murine model for bone loss from therapeutic and space-relevant sources of radiation. J Appl Physiol 101:789–793PubMedCrossRef Hamilton SA, Pecaut MJ, Gridley DS, Travis ND, Bandstra ER, Willey JS, Nelson GA, Bateman TA (2006) A murine model for bone loss from therapeutic and space-relevant sources of radiation. J Appl Physiol 101:789–793PubMedCrossRef
14.
Zurück zum Zitat Sawajiri M, Mizoe J (2003) Changes in bone volume after irradiation with carbon ions. Radiat Environ Biophys 42:101–106PubMedCrossRef Sawajiri M, Mizoe J (2003) Changes in bone volume after irradiation with carbon ions. Radiat Environ Biophys 42:101–106PubMedCrossRef
15.
Zurück zum Zitat Sawajiri M, Mizoe J, Tanimoto K (2003) Changes in osteoclasts after irradiation with carbon ion particles. Radiat Environ Biophys 42:219–223PubMedCrossRef Sawajiri M, Mizoe J, Tanimoto K (2003) Changes in osteoclasts after irradiation with carbon ion particles. Radiat Environ Biophys 42:219–223PubMedCrossRef
16.
Zurück zum Zitat Kondo H, Searby ND, Mojarrab R, Phillips J, Alwood J, Yumoto K, Almeida EA, Limoli CL, Globus RK (2009) Total-body irradiation of postpubertal mice with (137)Cs acutely compromises the microarchitecture of cancellous bone and increases osteoclasts. Radiat Res 171:283–289PubMedCrossRef Kondo H, Searby ND, Mojarrab R, Phillips J, Alwood J, Yumoto K, Almeida EA, Limoli CL, Globus RK (2009) Total-body irradiation of postpubertal mice with (137)Cs acutely compromises the microarchitecture of cancellous bone and increases osteoclasts. Radiat Res 171:283–289PubMedCrossRef
17.
Zurück zum Zitat Willey JS, Livingston EW, Robbins ME, Bourland JD, Tirado-Lee L, Smith-Sielicki H, Bateman TA (2010) Risedronate prevents early radiation-induced osteoporosis in mice at multiple skeletal locations. Bone 46:101–111PubMedCentralPubMedCrossRef Willey JS, Livingston EW, Robbins ME, Bourland JD, Tirado-Lee L, Smith-Sielicki H, Bateman TA (2010) Risedronate prevents early radiation-induced osteoporosis in mice at multiple skeletal locations. Bone 46:101–111PubMedCentralPubMedCrossRef
18.
Zurück zum Zitat Fukuda S, Iida H, Yan X (2002) Preventive effects of running exercise on bones in heavy ion particle irradiated rats. J Radiat Res 43:S233–S238PubMedCrossRef Fukuda S, Iida H, Yan X (2002) Preventive effects of running exercise on bones in heavy ion particle irradiated rats. J Radiat Res 43:S233–S238PubMedCrossRef
19.
Zurück zum Zitat Bandstra ER, Thompson RW, Nelson GA, Willey JS, Judex S, Cairns MA, Benton ER, Vazquez ME, Carson JA, Bateman TA (2009) Musculoskeletal changes in mice from 20–50 cGy of simulated galactic cosmic rays. Radiat Res 172:21–29PubMedCrossRef Bandstra ER, Thompson RW, Nelson GA, Willey JS, Judex S, Cairns MA, Benton ER, Vazquez ME, Carson JA, Bateman TA (2009) Musculoskeletal changes in mice from 20–50 cGy of simulated galactic cosmic rays. Radiat Res 172:21–29PubMedCrossRef
20.
Zurück zum Zitat Zeitlin C, Heilbronn L, Miller J (1998) Detailed characterization of the 1087 MeV/nucleon iron-56 beam used for radiobiology at the alternating gradient synchrotron. Radiat Res 149:560–569PubMedCrossRef Zeitlin C, Heilbronn L, Miller J (1998) Detailed characterization of the 1087 MeV/nucleon iron-56 beam used for radiobiology at the alternating gradient synchrotron. Radiat Res 149:560–569PubMedCrossRef
21.
Zurück zum Zitat Wilson JW, Townsend LW, Nealy JE, Chun SY, Hong BS, Buck WW, Lamkin SL, Ganapol BD, Khan F, Cucinotta FA (1989) Bryntrn: a baryon transport model, Washington, DC Wilson JW, Townsend LW, Nealy JE, Chun SY, Hong BS, Buck WW, Lamkin SL, Ganapol BD, Khan F, Cucinotta FA (1989) Bryntrn: a baryon transport model, Washington, DC
22.
Zurück zum Zitat Turner CH, Burr DB (1993) Basic biomechanical measurements of bone: a tutorial. Bone 14:595–608PubMedCrossRef Turner CH, Burr DB (1993) Basic biomechanical measurements of bone: a tutorial. Bone 14:595–608PubMedCrossRef
23.
24.
Zurück zum Zitat Bandstra ER, Pecaut MJ, Anderson ER, Willey JS, De Carlo F, Stock SR, Gridley DS, Nelson GA, Levine HG, Bateman TA (2008) Long-term dose response of trabecular bone in mice to proton radiation. Radiat Res 169:607–614PubMedCrossRef Bandstra ER, Pecaut MJ, Anderson ER, Willey JS, De Carlo F, Stock SR, Gridley DS, Nelson GA, Levine HG, Bateman TA (2008) Long-term dose response of trabecular bone in mice to proton radiation. Radiat Res 169:607–614PubMedCrossRef
25.
Zurück zum Zitat Willey JS, Grilly LG, Howard SH, Pecaut MJ, Obenaus A, Gridley DS, Nelson GA, Bateman TA (2008) Bone architectural and structural properties after 56Fe26+ radiation-induced changes in body mass. Radiat Res 170:201–207PubMedCrossRef Willey JS, Grilly LG, Howard SH, Pecaut MJ, Obenaus A, Gridley DS, Nelson GA, Bateman TA (2008) Bone architectural and structural properties after 56Fe26+ radiation-induced changes in body mass. Radiat Res 170:201–207PubMedCrossRef
26.
Zurück zum Zitat Frassica DA (2003) General principles of external beam radiation therapy for skeletal metastases. Clin Orthop Relat Res 415:S158–S164 Frassica DA (2003) General principles of external beam radiation therapy for skeletal metastases. Clin Orthop Relat Res 415:S158–S164
27.
Zurück zum Zitat Garmatis CJ, Chu FC (1978) The effectiveness of radiation therapy in the treatment of bone metastases from breast cancer. Radiology 126:235–237PubMedCrossRef Garmatis CJ, Chu FC (1978) The effectiveness of radiation therapy in the treatment of bone metastases from breast cancer. Radiology 126:235–237PubMedCrossRef
28.
Zurück zum Zitat FitzGerald TJ, McKenna M, Rothstein L, Daugherty C, Kase K, Greenberger JS (1986) Radiosensitivity of human bone marrow granulocyte-macrophage progenitor cells and stromal colony-forming cells: effect of dose rate. Radiat Res 107:205–215PubMedCrossRef FitzGerald TJ, McKenna M, Rothstein L, Daugherty C, Kase K, Greenberger JS (1986) Radiosensitivity of human bone marrow granulocyte-macrophage progenitor cells and stromal colony-forming cells: effect of dose rate. Radiat Res 107:205–215PubMedCrossRef
29.
Zurück zum Zitat Kolesnikova AI, Konoplyannikov AG, Hendry JH (1995) Differential sensitivity of two predominant stromal progenitor cell subpopulations in bone marrow to single and fractionated radiation doses. Radiat Res 144:342–345PubMedCrossRef Kolesnikova AI, Konoplyannikov AG, Hendry JH (1995) Differential sensitivity of two predominant stromal progenitor cell subpopulations in bone marrow to single and fractionated radiation doses. Radiat Res 144:342–345PubMedCrossRef
30.
Zurück zum Zitat Matsumura S, Hiranuma H, Deguchi A, Maeda T, Jikko A, Fuchihata H (1998) Changes in phenotypic expression of osteoblasts after X irradiation. Radiat Res 149:463–471PubMedCrossRef Matsumura S, Hiranuma H, Deguchi A, Maeda T, Jikko A, Fuchihata H (1998) Changes in phenotypic expression of osteoblasts after X irradiation. Radiat Res 149:463–471PubMedCrossRef
31.
Zurück zum Zitat Dudziak ME, Saadeh PB, Mehrara BJ, Steinbrech DS, Greenwald JA, Gittes GK, Longaker MT (2000) The effects of ionizing radiation on osteoblast-like cells in vitro. Plast Reconstr Surg 106:1049–1061PubMedCrossRef Dudziak ME, Saadeh PB, Mehrara BJ, Steinbrech DS, Greenwald JA, Gittes GK, Longaker MT (2000) The effects of ionizing radiation on osteoblast-like cells in vitro. Plast Reconstr Surg 106:1049–1061PubMedCrossRef
32.
Zurück zum Zitat Ikeda S, Hachisu R, Yamaguchi A, Gao YH, Okano T (2000) Radiation retards muscle differentiation but does not affect osteoblastic differentiation induced by bone morphogenetic protein-2 in C2C12 myoblasts. Int J Radiat Biol 76:403–411PubMedCrossRef Ikeda S, Hachisu R, Yamaguchi A, Gao YH, Okano T (2000) Radiation retards muscle differentiation but does not affect osteoblastic differentiation induced by bone morphogenetic protein-2 in C2C12 myoblasts. Int J Radiat Biol 76:403–411PubMedCrossRef
33.
Zurück zum Zitat Calabrese EJ, Baldwin LA (2000) Radiation hormesis: its historical foundations as a biological hypothesis. Hum Exp Toxicol 19:41–75PubMedCrossRef Calabrese EJ, Baldwin LA (2000) Radiation hormesis: its historical foundations as a biological hypothesis. Hum Exp Toxicol 19:41–75PubMedCrossRef
34.
Zurück zum Zitat Zhang L, Tian Y, Wu Y, Zhang H, Wang Z, Huo H, Zhang Y, Zhang M, Ning P, Jiang J (2010) Low-dose radiation-induced hormetic effect on hematopoietic reconstitution. Int J Radiat Biol 86:329–333PubMedCrossRef Zhang L, Tian Y, Wu Y, Zhang H, Wang Z, Huo H, Zhang Y, Zhang M, Ning P, Jiang J (2010) Low-dose radiation-induced hormetic effect on hematopoietic reconstitution. Int J Radiat Biol 86:329–333PubMedCrossRef
35.
Zurück zum Zitat Song XS, Zhou XZ, Zhang G, Dong QR, Qin L (2010) Low-dose X-ray irradiation promotes fracture healing through up-regulation of vascular endothelial growth factor. Med Hypotheses 75:522–524PubMedCrossRef Song XS, Zhou XZ, Zhang G, Dong QR, Qin L (2010) Low-dose X-ray irradiation promotes fracture healing through up-regulation of vascular endothelial growth factor. Med Hypotheses 75:522–524PubMedCrossRef
36.
Zurück zum Zitat Feinendegen LE (2005) Evidence for beneficial low level radiation effects and radiation hormesis. Br J Radiol 78:3–7PubMedCrossRef Feinendegen LE (2005) Evidence for beneficial low level radiation effects and radiation hormesis. Br J Radiol 78:3–7PubMedCrossRef
Metadaten
Titel
Low level irradiation in mice can lead to enhanced trabecular bone morphology
verfasst von
Lamya Karim
Stefan Judex
Publikationsdatum
01.09.2014
Verlag
Springer Japan
Erschienen in
Journal of Bone and Mineral Metabolism / Ausgabe 5/2014
Print ISSN: 0914-8779
Elektronische ISSN: 1435-5604
DOI
https://doi.org/10.1007/s00774-013-0518-x

Weitere Artikel der Ausgabe 5/2014

Journal of Bone and Mineral Metabolism 5/2014 Zur Ausgabe

Leitlinien kompakt für die Innere Medizin

Mit medbee Pocketcards sicher entscheiden.

Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag

Update Innere Medizin

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.