International Journal of Radiation Oncology * Biology * Physics
Volume 60, Issue 3 , Pages 909-919 , 1 November 2004

In vivo determination of tumor oxygenation during growth and in response to carbogen breathing using 15C5-loaded alginate capsules as fluorine-19 magnetic resonance imaging oxygen sensors

This work was presented in part at the ISMRM–ESMRMB 2001 Joint Annual Meeting, in Glasgow, Scotland.

  • Ulrike Nöth, Ph.D.

      Affiliations

    • Cancer Research UK Biomedical Magnetic Resonance Research Group, Department of Basic Medical Sciences, St. George's Hospital Medical School, London, United Kingdom
    • Corresponding Author InformationReprint requests to: Ulrike Nöth, Ph.D., Wellcome Department of Imaging Neuroscience, Institute of Neurology, UCL, 12 Queen Square, London WC1N 3BG, United Kingdom. Tel: (+44) 20-7833-7488; Fax: (+44) 20-7813-1420
  • ,
  • Loreta M. Rodrigues, M.Sc.

      Affiliations

    • Cancer Research UK Biomedical Magnetic Resonance Research Group, Department of Basic Medical Sciences, St. George's Hospital Medical School, London, United Kingdom
  • ,
  • Simon P. Robinson, Ph.D.

      Affiliations

    • Cancer Research UK Biomedical Magnetic Resonance Research Group, Department of Basic Medical Sciences, St. George's Hospital Medical School, London, United Kingdom
  • ,
  • Anette Jork, Ph.D.

      Affiliations

    • Department of Biotechnology, University of Würzburg, Würzburg, Germany
  • ,
  • Ulrich Zimmermann, Ph.D.

      Affiliations

    • Department of Biotechnology, University of Würzburg, Würzburg, Germany
  • ,
  • Barry Newell, M.B.B.S., M.R.C.P.

      Affiliations

    • Farnborough Hospital, Farnborough Common, Orpington, Kent, United Kingdom
  • ,
  • John R. Griffiths, M.B.B.S., D.Phil.

      Affiliations

    • Cancer Research UK Biomedical Magnetic Resonance Research Group, Department of Basic Medical Sciences, St. George's Hospital Medical School, London, United Kingdom

Received 29 May 2003 ,Revised 28 June 2004 ,Accepted 7 July 2004.

References 

  1. Semenza GL . HIF-1 and tumour progression: Pathophysiology and therapeutics . Trends Mol Med . 2002;8(Suppl):S62–S67
  2. Gray LH , Conger AD , Ebert M , et al.  The concentration of oxygen dissolved in tissues at the time of irradiation as a factor in radiotherapy . Br J Radiol . 1953;26:636–648
  3. Teicher BA , Lazo JS , Sartorelli AC . Classification of antineoplastic agents by their selective toxicities toward oxygenated and hypoxic tumour cells . Cancer Res . 1981;41:73–81
  4. Britzel DM , Sibley GS , Prosnitz LR , et al.  Tumour hypoxia adversely affects the prognosis of carcinoma of the head and neck . Int J Radiat Oncol Biol Phys . 1997;38:285–289
  5. Fyles AW , Milosevic M , Wong R , et al.  Oxygen predicts radiation response and survival in patients with cervix cancer . Radiother Oncol . 1998;48:149–156
  6. Nordsmark M , Overgaard J . A confirmatory study on oxygenationstatus and loco-regional control in advanced head and neck squamous cell carcinoma treated by radiation therapy . Radiother Oncol . 2000;57:39–43
  7. Vaupel P , Briest S , Hckel M . Hypoxia in breast cancer: Pathogenesis, characterization and biological/therapeutic implications . Wien Med Wochenschr . 2002;152:334–342
  8. Brown MJ . Exploiting the hypoxic cancer cell: Mechanisms and therapeutic strategies . Mol Med Today . 2000;6:157–162
  9. Saunders MP , Patterson AV , Chinje EC , et al.  NADPH:cytochrome c (P450) reductase activates tirapazamine (SR4233) to restore hypoxic and oxic cytotoxicity in an aerobic resistant derivative of the A549 lung cancer cell line . Br J Cancer . 2000;82:651–656
  10. Brizel DM , Scully SP , Harrelson JM , et al.  Tumour oxygenation predicts for the likelihood of distant metastasis in human soft tissue sarcoma . Cancer Res . 1996;56:941–943
  11. Pitson G , Fyles A , Milosevic M , et al.  Tumour size and oxygenation are independent predictors of nodal disease in patients with cervix cancer . Int J Radiat Oncol Biol Phys . 2001;51:699–703
  12. Seddon BM, Honess DJ, Vojnovic B, et al.Measurement of tumour oxygenation: In vivo comparison of a luminescence fiber-optic sensor and a polarographic electrode in the p22 tumour. Radiat Res 2001;155:37–846.
  13. Braun RD , Lanzen JL , Snyder SA , et al.  Comparison of tumour and normal tissue tension measurements using OxyLite or microelectrodes in rodents . Am J Physiol Heart Circ Physiol . 2001;280:H2533–H2544
  14. Bussink J , Kaanders JH , Strik AM , et al.  Effects of nicotinamide and carbogen on oxygenation in human tumour xenografts measured with luminescence based fiber-optic probes . Radiother Oncol . 2000;57:21–30
  15. Parhami P , Fung PM . Fluorine-19 relaxation study of perfluoro chemicals as oxygen carriers . J Phys Chem . 1983;87:1928–1931
  16. Dardzinski BJ , Sotak CH . Rapid tissue oxygen tension mapping using 19F inversion-recovery echo-planar imaging of perfluoro-15-crown-5-ether . Magn Reson Med . 1994;32:88–97
  17. van der Sanden BPJ , Heerschap A , Simonetti AW , et al.  Characterisation and validation of non-invasive oxygen tension measurements in human glioma xenografts by 19F-MR relaxometry . Int J Radiat Oncol Biol Phys . 1999;44:649–658
  18. Duong DQ , Iadecola C , Kim S-G . Effect of hyperoxia, hypercapnia, and hypoxia on cerebral interstitial oxygen tension and cerebral blood flow . Magn Reson Med . 2001;45:61–70
  19. McIntyre DJO , McCoy CL , Griffiths JR . Tumour oxygenation measurements by 19F magnetic resonance imaging of perfluorocarbons . Curr Sci . 1999;76:753–762
  20. Fan X , River JN , Zamora M , et al.  Effect of carbogen on tumour oxygenation: Combined fluorine-19 and proton MRI measurements . Int J Radiat Oncol Biol Phys . 2002;54:1202–1209
  21. Le D , Mason RP , Hunjan S , et al.  Regional tumour oxygen dynamics: 19F PBSR EPI of hexafluorobenzene . Magn Reson Imag . 1997;15:971–981
  22. Hunjan S , Zhao D , Constantinescu A , et al.  Tumour oximetry: Demonstration of an enhanced dynamic mapping procedure using fluorine-19 echo planar magnetic resonance imaging in the Dunning prostate R3327-AT1 rat tumour . Int J Radiat Oncol Biol Phys . 2001;49:1097–1108
  23. Milosevic MF , Fyles AW , Wong R , et al.  Interstitial fluid pressure in cervical carcinoma . Cancer . 1998;82:2418–2426
  24. Zekorn T , Horcher A , Siebers U , et al.  Barium-cross-linked alginate beads: A simple one-step method for successful immuno-isolated transplantation of islets of Langerhans . Acta Diabetol . 1992;29:99–9106
  25. Nöth U , Gröhn P , Jork A , et al.  In vivo determination of the partial oxygen pressure in perfluorocarbon-loaded alginate capsules implanted into the peritoneal cavity and different tissues by 19F-MRI . Magn Reson Med . 1999;42:1039–1047
  26. Zimmermann U , Nöth U , Gröhn P , et al.  Non-invasive evaluation of the location, the functional integrity and the oxygen supply of implants: 19F nuclear magnetic resonance imaging of perfluorocarbon-loaded Ba2+-alginate beads . Art Cells Blood Subs Immob Biotech . 2000;28:129–146
  27. Zimmermann U , Thürmer F , Jork A , et al.  A novel class of amitogenic alginate microcapsules for long-term immunoisolated transplantation . Ann NY Acad Sci . 2001;944:199–215
  28. Gröhn P , Klöck G , Schmitt J , et al.  Large scale production of Ba2+-alginate-coated islets of Langerhans for immunoisolation . Exp Clin Endocrinol . 1994;102:380–387
  29. Deichmann R , Haase A . Quantification of T1 values by snapshot-flash NMR imaging . J Magn Reson . 1992;96:608–612
  30. Riess JG , Le Blanc M . Solubility and transport phenomena in perfluorochemicals relevant to blood substitution and other biomedical applications . Pure Appl Chem . 1982;54:2383–2406
  31. Baldwin NJ , Ng TC . Oxygenation and metabolic status of KHT tumours as measured simultaneously by 19F magnetic resonance imaging and 31P magnetic resonance spectroscopy . Magn Reson Imag . 1996;14:541–551
  32. Mason RP , Antich PP , Babcock EE , et al.  Non-invasive determination of tumor oxygen tension and local variation with growth . Int J Radiat Oncol Biol Phys . 1994;29:95–9103
  33. Gallez B , Jordan BF , Baudelet C , et al.  Pharmalogical modifications of the partial pressure of oxygen in murine tumours: Evaluation using in vivo EPR oxymetry . Magn Reson Med . 1999;42:627–630
  34. Jordan BF , Misson P-D , Demeure R , et al.  Changes in tumour oxygenation/perfusion induced by the NO donor isosorbide dinitrate, in comparison with carbogen: Monitoring by EPR and MRI . Int J Radiat Oncol Biol Phys . 2000;48:565–570
  35. O'Hara JA , Blumenthal RD , Grinberg OJ , et al.  Response to radioimmunotherapy correlates with tumour pO2 measured by EPR oximetry in human tumour xenografts . Radiat Res . 2001;155:466–473
  36. James PE , O'Hara JA , Grinberg OY , et al.  Intratumoral pO2 measured using a new oxygen sensitive paramagnetic material, gloxy . Adv Exp Med Biol . 1997;428:97–9106
  37. Robinson SP , Collingridge DR , Howe FA , et al.  Tumour response to hypercapnia and hyperoxia monitored by FLOOD magnetic resonance imaging . Nucl Magn Reson Biomed . 1999;12:98–9106
  38. Zhao D , Constantinescu A , Jiang L , et al.  Prognostic radiology: Quantitative assessment of tumour oxygen dynamics by MRI . Am J Clin Oncol (CCT) . 2001;24:462–466
  39. Kaanders JH , Wijffels KI , Marres HA , et al.  Pimonidazole binding and tumour vascularity predict for treatment outcome in head and neck cancer . Cancer Res . 2002;62:7066–7074
  40. Bernier J , Denekamp J , Rojas A , et al.  ARCON: Accelerated radiotherapy with carbogen and nicotinamide in non small cell lung cancer: A phase I/II study by the EORTC . Radiother Oncol . 1999;52:149–156
  41. Honess DJ , Bleehen NM . Effects of the radiosensitizing agent nicotinamide on relative tissue perfusion and kidney function in C3H mice . Radiother Oncol . 1993;27:140–148
  42. Kelleher DK , Vaupel PW . Possible mechanisms involved in tumour radiosensitization following nicotinamide administration . Radiother Oncol . 1994;32:47–53
  43. Hees PS , Sotak CH . Assessment of changes in murine tumour oxygenation in response to nicotinamide using 19F NMR relaxometry of a perfluorocarbon emulsion . Magn Reson Med . 1993;29:303–310
  44. Robinson SP , Howe FA , Stubbs M , et al.  Effects of nicotinamide and carbogen on tumour oxygenation, blood flow, energetics and blood glucose levels . Br J Cancer . 2000;82:2007–2014
  45. Jirtle R . Chemical modification of tumour blood flow . Int J Hyperthermia . 1998;4:355–371
  46. Leinfelder U , Brunnenmeier F , Cramer H , et al.  A highly sensitive assay for validation of purification regimes of alginates . Biomaterials . 2003;24:4161–4172
  47. Schneider S , Feilen P , Cramer H , et al.  Beneficial effects of human serum albumine on stability and functionality of alginate microcapsules fabricated in different ways . J Microencapsul . 2003;20:627–636

 This work was supported by the Deutsche Forschungsgemeinschaft (NO395/1-1, to Dr. Noth; ZI99/15-1, to Dr. Zimmerman), the Bundesministerium fuer Bildung und Forschung (0311588, to Dr. Zimmermann) and Cancer Research UK [CRC] Grant C12/A1209. Doctor Robinson is the recipient of a Royal Society University Research Fellowship.

PII: S0360-3016(04)02008-5

doi: 10.1016/j.ijrobp.2004.07.671

International Journal of Radiation Oncology * Biology * Physics
Volume 60, Issue 3 , Pages 909-919 , 1 November 2004