Skip to main content
SpringerLink
Log in

Characterization of a clinically used charcoal suspension for in vivo EPR oximetry

  • Research Article
  • Published:
Magnetic Resonance Materials in Physics, Biology and Medicine Aims and scope Submit manuscript

Abstract

Objectives

Electron paramagnetic resonance (EPR) oximetry using particulate materials allows repeatable measurements of oxygen in tissues. However, the materials identified so far are not medical devices, thus precluding their immediate use in clinical studies. The aim of this study was to assess the magnetic properties of Carbo-Rep®, a charcoal suspension used as a liquid marker for preoperative tumor localization.

Materials and methods

Calibration curves (EPR linewidth as a function of pO2) were built using 9-GHz EPR spectrometry. The feasibility of performing oxygen measurements was examined in vivo by using a low-frequency (1 GHz) EPR spectrometer and by inducing ischemia in the gastrocnemius muscle of mice or by submitting rats bearing tumors to different oxygen-breathing challenges.

Results

Paramagnetic centers presenting a high oxygen sensitivity were identified in Carbo-Rep®. At 1 GHz, the EPR linewidth varied from 98 to 426 µT in L-band in nitrogen and air, respectively. The sensor allowed repeated measurements of oxygen over 6 months in muscles of mice. Subtle variations of tumor oxygenation were monitored in rats when switching gas breathing from air to carbogen.

Discussion

The magnetic properties of Carbo-Rep® are promising for its future use as oxygen sensor in clinical EPR oximetry.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  1. Springett R, Swartz HM (2007) Measurements of oxygen in vivo: overview and perspectives on methods to measure oxygen within cells and tissues. Antioxid Redox Signal 9:1295–1301

    Article  CAS  PubMed  Google Scholar 

  2. Vikram DS, Zweier JL, Kuppusamy P (2007) Methods for noninvasive imaging of tissue hypoxia. Antioxid Redox Signal 9:1745–1756

    Article  CAS  PubMed  Google Scholar 

  3. Colliez F, Gallez B, Jordan BF (2017) Assessing tumor oxygenation for predicting outcome in radiation oncology: a review of studies correlating tumor hypoxic status and outcome in the preclinical and clinical settings. Front Oncol 7:10

    Article  PubMed  PubMed Central  Google Scholar 

  4. Bussink J, Kaanders JH, van der Kogel AJ (2003) Tumor hypoxia at the micro-regional level: clinical relevance and predictive value of exogenous and endogenous hypoxic cell markers. Radiother Oncol 67:3–15

    Article  PubMed  Google Scholar 

  5. Peeters SG, Zegers CM, Yaromina A, Van Elmpt W, Dubois L, Lambin P (2015) Current preclinical and clinical applications of hypoxia PET imaging using 2-nitroimidazoles. Q J Nucl Med Mol Imaging 59:39–57

    CAS  PubMed  Google Scholar 

  6. Griffiths JR, Robinson SP (1999) The OxyLite: a fibre-optic oxygen sensor. Br J Radiol 72:627–630

    Article  CAS  PubMed  Google Scholar 

  7. Vaupel P, Höckel M, Mayer A (2007) Detection and characterization of tumor hypoxia using pO2 histography. Antioxid Redox Signal 9:1221–1235

    Article  CAS  PubMed  Google Scholar 

  8. Price JM, Robinson SP, Koh DM (2013) Imaging hypoxia in tumours with advanced MRI. Q J Nucl Med Mol Imaging 57:257–270

    CAS  PubMed  Google Scholar 

  9. Howe FA, Robinson SP, McIntyre DJ, Stubbs M, Griffiths JR (2001) Issues in flow and oxygenation dependent contrast (FLOOD) imaging of tumours. NMR Biomed 14:497–506

    Article  CAS  PubMed  Google Scholar 

  10. Baudelet C, Gallez B (2002) How does blood oxygen level-dependent (BOLD) contrast correlate with oxygen partial pressure (pO2) inside tumors? Magn Reson Med 48:980–986

    Article  PubMed  Google Scholar 

  11. Baudelet C, Gallez B (2004) Current issues in the utility of blood oxygen level dependent MRI for the assessment of modulations in tumor oxygenation. Curr Med Imaging Rev 1:229–243

    Article  Google Scholar 

  12. O’Connor JP, Boult JK, Jamin Y, Babur M, Finegan KG, Williams KJ, Little RA, Jackson A, Parker GJ, Reynolds AR, Waterton JC, Robinson SP (2016) Oxygen-enhanced MRI accurately identifies, quantifies, and maps tumor hypoxia in preclinical cancer models. Cancer Res 76:787–795

    Article  CAS  PubMed  Google Scholar 

  13. Cao-Pham TT, Tran LB, Colliez F, Joudiou N, El Bachiri S, Grégoire V, Levêque P, Gallez B, Jordan BF (2016) Monitoring tumor response to carbogen breathing by oxygen-sensitive magnetic resonance parameters to predict the outcome of radiation therapy: a preclinical study. Int J Radiat Oncol Biol Phys 96:149–160

    Article  PubMed  Google Scholar 

  14. Kodibagkar VD, Wang X, Mason RP (2008) Physical principles of quantitative nuclear magnetic resonance oximetry. Front Biosci 13:1371–1384

    Article  CAS  PubMed  Google Scholar 

  15. Jordan BF, Cron GO, Gallez B (2009) Rapid monitoring of oxygenation by 19F magnetic resonance imaging: simultaneous comparison with fluorescence quenching. Magn Reson Med 61:634–638

    Article  PubMed  Google Scholar 

  16. Swartz HM, Clarkson RB (1998) The measurement of oxygen in vivo using EPR techniques. Phys Med Biol 43:1957–1975

    Article  CAS  PubMed  Google Scholar 

  17. Gallez B, Baudelet C, Jordan BF (2004) Assessment of tumor oxygenation by electron paramagnetic resonance: principles and applications. NMR Biomed 17:240–262

    Article  CAS  PubMed  Google Scholar 

  18. Krishna MC, Matsumoto S, Yasui H, Saito K, Devasahayam N, Subramanian S, Mitchell JB (2012) Electron paramagnetic resonance imaging of tumor pO2. Radiat Res 177:376–386

    Article  CAS  PubMed  Google Scholar 

  19. Ahmad R, Kuppusamy P (2010) Theory, instrumentation, and applications of electron paramagnetic resonance oximetry. Chem Rev 110:3212–3236

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Epel B, Halpern HJ (2015) In vivo pO2 imaging of tumors: oxymetry with very low-frequency electron paramagnetic resonance. Methods Enzymol 564:501–527

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Liu KJ, Gast P, Moussavi M, Norby SW, Vahidi N, Walczak T, Wu M, Swartz HM (1993) Lithium phthalocyanine: a probe for electron paramagnetic resonance oximetry in viable biological systems. Proc Natl Acad Sci USA 90:5438–5442

    Article  CAS  PubMed  Google Scholar 

  22. Pandian RP, Parinandi NL, Ilangovan G, Zweier JL, Kuppusamy P (2003) Novel particulate spin probe for targeted determination of oxygen in cells and tissues. Free Radic Biol Med 35:1138–1148

    Article  CAS  PubMed  Google Scholar 

  23. Jordan BF, Baudelet C, Gallez B (1998) Carbon-centered radicals as oxygen sensors for in vivo electron paramagnetic resonance: screening for an optimal probe among commercially available charcoals. MAGMA 7:121–129

    Article  CAS  PubMed  Google Scholar 

  24. Lan M, Beghein N, Charlier N, Gallez B (2004) Carbon blacks as EPR sensors for localized measurements of tissue oxygenation. Magn Reson Med 51:1272–1278

    Article  CAS  PubMed  Google Scholar 

  25. Khan N, Mupparaju S, Hou H, Williams BB, Swartz HM (2012) Repeated assessment of orthotopic glioma pO2 by multi-site EPR oximetry: a technique with the potential to guide therapeutic optimization by repeated measurements of oxygen. J Neurosci Methods 204:111–117

    Article  PubMed  Google Scholar 

  26. Ilangovan G, Liebgott T, Kutala VK, Petryakov S, Zweier JL, Kuppusamy P (2004) EPR oximetry in the beating heart: myocardial oxygen consumption rate as an index of postischemic recovery. Magn Reson Med 51:835–842

    Article  PubMed  Google Scholar 

  27. Jordan BF, Kimpalou JZ, Beghein N, Dessy C, Feron O, Gallez B (2004) Contribution of oxygenation to BOLD contrast in exercising muscle. Magn Reson Med 52:391–396

    Article  PubMed  Google Scholar 

  28. James PE, Miyake M, Swartz HM (1999) Simultaneous measurement of NO and pO2 from tissue by in vivo EPR. Nitric Oxide 3:292–301

    Article  CAS  PubMed  Google Scholar 

  29. He G, Shankar RA, Chzhan M, Samouilov A, Kuppusamy P, Zweier JL (1999) Noninvasive measurement of anatomic structure and intraluminal oxygenation in the gastrointestinal tract of living mice with spatial and spectral EPR imaging. Proc Natl Acad Sci USA 96:4586–4591

    Article  CAS  PubMed  Google Scholar 

  30. James PE, Bacic G, Grinberg OY, Goda F, Dunn JF, Jackson SK, Swartz HM (1996) Endotoxin-induced changes in intrarenal pO2, measured by in vivo electron paramagnetic resonance oximetry and magnetic resonance imaging. Free Radic Biol Med 21:25–34

    Article  CAS  PubMed  Google Scholar 

  31. Krzic M, Sentjurc M, Kristl J (2001) Improved skin oxygenation after benzyl nicotinate application in different carriers as measured by EPR oximetry in vivo. J Control Release 70:203–211

    Article  CAS  PubMed  Google Scholar 

  32. Van Eyck AS, Jordan BF, Gallez B, Heilier JF, Van Langendonckt A, Donnez J (2009) Electron paramagnetic resonance as a tool to evaluate human ovarian tissue reoxygenation after xenografting. Fertil Steril 92:374–381

    Article  CAS  PubMed  Google Scholar 

  33. Vériter S, Gianello P, Igarashi Y, Beaurin G, Ghyselinck A, Aouassar N, Jordan B, Gallez B, Dufrane D (2014) Improvement of subcutaneous bioartificial pancreas vascularization and function by coencapsulation of pig islets and mesenchymal stem cells in primates. Cell Transplant 23:1349–1364

    Article  PubMed  Google Scholar 

  34. Desmet CM, Lafosse A, Vériter S, Porporato PE, Sonveaux P, Dufrane D, Levêque P, Gallez B (2015) Application of electron paramagnetic resonance (EPR) oximetry to monitor oxygen in wounds in diabetic models. PLoS One 10:e0144914

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Gallez B, Jordan BF, Baudelet C, Misson PD (1999) Pharmacological modifications of the partial pressure of oxygen in murine tumors: evaluation using in vivo EPR oximetry. Magn Reson Med 42:627–630

    Article  CAS  PubMed  Google Scholar 

  36. Jordan BF, Grégoire V, Demeure RJ, Sonveaux P, Feron O, O’Hara J, Vanhulle VP, Delzenne N, Gallez B (2002) Insulin increases the sensitivity of tumors to irradiation: involvement of an increase in tumor oxygenation mediated by a nitric oxide-dependent decrease of the tumor cells oxygen consumption. Cancer Res 62:3555–3561

    CAS  PubMed  Google Scholar 

  37. Crokart N, Radermacher K, Jordan BF, Baudelet C, Cron GO, Grégoire V, Beghein N, Bouzin C, Feron O, Gallez B (2005) Tumor radiosensitization by antiinflammatory drugs: evidence for a new mechanism involving the oxygen effect. Cancer Res 65:7911–7916

    Article  CAS  PubMed  Google Scholar 

  38. Ansiaux R, Baudelet C, Jordan BF, Beghein N, Sonveaux P, De Wever J, Martinive P, Grégoire V, Feron O, Gallez B (2005) Thalidomide radiosensitizes tumors through early changes in the tumor microenvironment. Clin Cancer Res 11:743–750

    CAS  PubMed  Google Scholar 

  39. Hou H, Khan N, Grinberg OY, Yu H, Grinberg SA, Lu S, Demidenko E, Steffen RP, Swartz HM (2007) The effects of Efaproxyn (efaproxiral) on subcutaneous RIF-1 tumor oxygenation and enhancement of radiotherapy-mediated inhibition of tumor growth in mice. Radiat Res 168:218–225

    Article  CAS  PubMed  Google Scholar 

  40. Crokart N, Jordan BF, Baudelet C, Cron GO, Hotton J, Radermacher K, Grégoire V, Beghein N, Martinive P, Bouzin C, Feron O, Gallez B (2007) Glucocorticoids modulate tumor radiation response through a decrease in tumor oxygen consumption. Clin Cancer Res 13:630–635

    Article  CAS  PubMed  Google Scholar 

  41. Diepart C, Karroum O, Magat J, Feron O, Verrax J, Calderon PB, Grégoire V, Leveque P, Stockis J, Dauguet N, Jordan BF, Gallez B (2012) Arsenic trioxide treatment decreases the oxygen consumption rate of tumor cells and radiosensitizes solid tumors. Cancer Res 72:482–490

    Article  CAS  PubMed  Google Scholar 

  42. O’Hara JA, Goda F, Liu KJ, Bacic G, Hoopes PJ, Swartz HM (1995) The pO2 in a murine tumor after irradiation: an in vivo electron paramagnetic resonance oximetry study. Radiat Res 144:222–229

    Article  PubMed  Google Scholar 

  43. Crokart N, Jordan BF, Baudelet C, Ansiaux R, Sonveaux P, Grégoire V, Beghein N, DeWever J, Bouzin C, Feron O, Gallez B (2005) Early reoxygenation in tumors after irradiation: determining factors and consequences for radiotherapy regimens using daily multiple fractions. Int J Radiat Oncol Biol Phys 63:901–910

    Article  CAS  PubMed  Google Scholar 

  44. Cron GO, Beghein N, Crokart N, Chavée E, Bernard S, Vynckier S, Scalliet P, Gallez B (2005) Changes in the tumor microenvironment during low-dose-rate permanent seed implantation iodine-125 brachytherapy. Int J Radiat Oncol Biol Phys 63:1245–1251

    Article  CAS  PubMed  Google Scholar 

  45. Fujii H, Sakata K, Katsumata Y, Sato R, Kinouchi M, Someya M, Masunaga S, Hareyama M, Swartz HM, Hirata H (2008) Tissue oxygenation in a murine SCC VII tumor after X-ray irradiation as determined by EPR spectroscopy. Radiother Oncol 86:354–360

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Salikhov I, Walczak T, Lesniewski P, Khan N, Iwasaki A, Comi R, Buckey J, Swartz HM (2005) EPR spectrometer for clinical applications. Magn Reson Med 54:1317–1320

    Article  CAS  PubMed  Google Scholar 

  47. Swartz HM, Williams BB, Zaki BI, Hartford AC, Jarvis LA, Chen EY, Comi RJ, Ernstoff MS, Hou H, Khan N, Swarts SG, Flood AB, Kuppusamy P (2014) Clinical EPR: unique opportunities and some challenges. Acad Radiol 21:197–206

    Article  PubMed  PubMed Central  Google Scholar 

  48. Swartz HM, Williams BB, Hou H, Khan N, Jarvis LA, Chen EY, Schaner PE, Ali A, Gallez B, Kuppusamy P, Flood AB (2016) Direct and repeated clinical measurements of pO2 for enhancing cancer therapy and other applications. Adv Exp Med Biol 923:95–104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Gallez B, Mäder K (2000) Accurate and sensitive measurements of pO2 in vivo using low frequency EPR spectroscopy: how to confer biocompatibility to the oxygen sensors. Free Radic Biol Med 29:1078–1084

    Article  CAS  PubMed  Google Scholar 

  50. Swartz HM, Liu KJ, Goda F, Walczak T (1994) India ink: a potential clinically applicable EPR oximetry probe. Magn Reson Med 31:229–232

    Article  CAS  PubMed  Google Scholar 

  51. Charlier N, Beghein N, Gallez B (2004) Development and evaluation of biocompatible inks for the local measurement of oxygen using in vivo EPR. NMR Biomed 17:303–310

    Article  CAS  PubMed  Google Scholar 

  52. Gallez B, Debuyst R, Liu KJ, Demeure R, Dejehet F, Swartz HM (1996) Development of biocompatible implants of fusinite for in vivo EPR oximetry. MAGMA 4:71–75

    Article  CAS  PubMed  Google Scholar 

  53. He J, Beghein N, Ceroke P, Clarkson RB, Swartz HM, Gallez B (2001) Development of biocompatible oxygen-permeable films holding paramagnetic carbon particles: evaluation of their performance and stability in EPR oximetry. Magn Reson Med 46:610–614

    Article  CAS  PubMed  Google Scholar 

  54. Dinguizli M, Jeumont S, Beghein N, He J, Walczak T, Lesniewski PN, Hou H, Grinberg OY, Sucheta A, Swartz HM, Gallez B (2006) Development and evaluation of biocompatible films of polytetrafluoroethylene polymers holding lithium phthalocyanine crystals for their use in EPR oximetry. Biosens Bioelectron 21:1015–1022

    Article  CAS  PubMed  Google Scholar 

  55. Dinguizli M, Beghein N, Gallez B (2008) Retrievable micro-inserts containing oxygen sensors for monitoring tissue oxygenation using EPR oximetry. Physiol Meas 29:1247–1254

    Article  CAS  PubMed  Google Scholar 

  56. Eteshola E, Pandian RP, Lee SC, Kuppusamy P (2009) Polymer coating of paramagnetic particulates for in vivo oxygen-sensing applications. Biomed Microdevices 11:379–387

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Pandian RP, Meenakshisundaram G, Bratasz A, Eteshola E, Lee SC, Kuppusamy P (2010) An implantable teflon chip holding lithium naphthalocyanine microcrystals for secure, safe, and repeated measurements of pO2 in tissues. Biomed Microdevices 12:381–387

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Hou H, Khan N, Gohain S, Kuppusamy ML, Kuppusamy P (2018) Pre-clinical evaluation of OxyChip for long-term EPR oximetry. Biomed Microdevices 20:29

    Article  CAS  PubMed  Google Scholar 

  59. Baudelet C, Gallez B (2004) Effect of anesthesia on the signal intensity in tumors using BOLD-MRI: comparison with flow measurements by Laser Doppler flowmetry and oxygen measurements by luminescence-based probes. Magn Reson Imaging 22:905–912

    Article  CAS  PubMed  Google Scholar 

  60. Walsh JC, Lebedev A, Aten E, Madsen K, Marciano L, Kolb HC (2001) The clinical importance of assessing tumor hypoxia: relationship of tumor hypoxia to prognosis and therapeutic opportunities. Antioxid Redox Signal 21:1516–1554

    Article  CAS  Google Scholar 

  61. Vaupel P, Kelleher DK, Höckel M (2001) Oxygen status of malignant tumors: pathogenesis of hypoxia and significance for tumor therapy. Semin Oncol 28:29–35

    Article  CAS  PubMed  Google Scholar 

  62. Horsman MR, Wouters BG, Joiner MC, Overgaard J (2009) The oxygen effect and fractionated radiotherapy. In: Joiner M, van der Kogel A (eds) Basic clinical radiobiology, 4th edn. H. Arnold, London, pp 207–216

    Chapter  Google Scholar 

  63. Wouters BG, Korintzinsky M (2009) The tumor micro-environment and cellular hypoxia responses. In: Joiner M, van der Kogel A (eds) Basic clinical radiobiology, 4th edn. H. Arnold, London, pp 217–232

    Chapter  Google Scholar 

  64. Khan N, Williams BB, Hou H, Li H, Swartz HM (2007) Repetitive tissue pO2 measurements by electron paramagnetic resonance oximetry: current status and future potential for experimental and clinical studies. Antioxid Redox Signal 9:1169–1182

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Swartz HM, Hou H, Khan N, Jarvis LA, Chen EY, Williams BB, Kuppusamy P (2014) Advances in probes and methods for clinical EPR oximetry. Adv Exp Med Biol 812:73–79

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Flood AB, Wood VA, Swartz HM (2017) Using India ink as a sensor for oximetry: evidence of its safety as a medical device. Adv Exp Med Biol 977:297–312

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Vahidi N, Clarkson RB, Liu KJ, Norby SW, Wu M, Swartz HM (1994) In vivo and in vitro EPR oximetry with fusinite: a new coal-derived, particulate EPR probe. Magn Reson Med 31:139–146

    Article  CAS  PubMed  Google Scholar 

  68. James PE, Grinberg OY, Goda F, Panz T, O’Hara JA, Swartz HM (1997) Gloxy: an oxygen-sensitive coal for accurate measurement of low oxygen tensions in biological systems. Magn Reson Med 38:48–58

    Article  CAS  PubMed  Google Scholar 

  69. Swartz HM, Khan N, Buckey J, Comi R, Gould L, Grinberg O, Hartford A, Hopf H, Hou H, Hug E, Iwasaki A, Lesniewski P, Salikhov I, Walczak T (2004) Clinical applications of EPR: overview and perspectives. NMR Biomed 17:335–351

    Article  CAS  PubMed  Google Scholar 

  70. Desmet CM, Préat V, Gallez B (2018) Nanomedicines and gene therapy for the delivery of growth factors to improve perfusion and oxygenation in wound healing. Adv Drug Deliv Rev 129:262–284

    Article  CAS  PubMed  Google Scholar 

  71. Matsuo M, Matsumoto S, Mitchell JB, Krishna MC, Camphausen K (2014) Magnetic resonance imaging of the tumor microenvironment in radiotherapy: perfusion, hypoxia, and metabolism. Semin Radiat Oncol 24:210–217

    Article  PubMed  PubMed Central  Google Scholar 

  72. Epel B, Maggio M, Pelizzari C, Halpern HJ (2017) Electron paramagnetic resonance pO2 image tumor oxygen-guided radiation therapy optimization. Adv Exp Med Biol 977:287–296

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors wish to thank Dr. Fabienne Danhier for performing the particle-size measurements.

Funding

The work was supported by the National Cancer Institute (NCI, USA) PO1CA190193, the Actions de Recherches Concertées ARC 14/19-058, and the Fonds Joseph Maisin. This research used the EPR facilities of the technological platform Nuclear and Electron Spin Technologies of the Louvain Drug Research Institute.

Author information

Author notes

  1. C. M. Desmet and L. B. A. Tran contributed equally to the study.

Authors and Affiliations

  1. Biomedical Magnetic Resonance Research Group, Louvain Drug Research Institute, Université catholique de Louvain, Avenue Mounier 73-B1.73.08, 1200, Brussels, Belgium

    Céline Marie Desmet, Ly Binh An Tran, Pierre Danhier & Bernard Gallez

Authors
  1. Céline Marie Desmet
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ly Binh An Tran
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Pierre Danhier
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Bernard Gallez
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

CMD, LBAT, PD: data acquisition, analysis, and interpretation; manuscript drafting; critical revision. BG: study conception and design; data analysis and interpretation; manuscript drafting; critical revision.

Corresponding author

Correspondence to Bernard Gallez.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Statement of human rights

This article does not contain any studies with human participants performed by any of the authors

Statement on the welfare of animals

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted (authorization 2014/UCL/MD/026).

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Desmet, C.M., Tran, L.B.A., Danhier, P. et al. Characterization of a clinically used charcoal suspension for in vivo EPR oximetry. Magn Reson Mater Phy 32, 205–212 (2019). https://doi.org/10.1007/s10334-018-0704-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10334-018-0704-x

Keywords

Search

Navigation