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Integrated Systems and Technologies

Oxygen-Enhanced MRI Accurately Identifies, Quantifies, and Maps Tumor Hypoxia in Preclinical Cancer Models

James P.B. O'Connor, Jessica K.R. Boult, Yann Jamin, Muhammad Babur, Katherine G. Finegan, Kaye J. Williams, Ross A. Little, Alan Jackson, Geoff J.M. Parker, Andrew R. Reynolds, John C. Waterton and Simon P. Robinson
James P.B. O'Connor
1Institute of Cancer Sciences, University of Manchester, Manchester, United Kingdom.
2Centre for Imaging Sciences, University of Manchester, Manchester, United Kingdom.
3Department of Radiology, Christie NHS Foundation Trust, Manchester, United Kingdom.
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  • For correspondence: james.o'connor@manchester.ac.uk
Jessica K.R. Boult
4Division of Radiotherapy and Imaging, The Institute of Cancer Research, London, United Kingdom.
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Yann Jamin
4Division of Radiotherapy and Imaging, The Institute of Cancer Research, London, United Kingdom.
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Muhammad Babur
5Manchester Pharmacy School, University of Manchester, Manchester, United Kingdom.
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Katherine G. Finegan
5Manchester Pharmacy School, University of Manchester, Manchester, United Kingdom.
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Kaye J. Williams
1Institute of Cancer Sciences, University of Manchester, Manchester, United Kingdom.
5Manchester Pharmacy School, University of Manchester, Manchester, United Kingdom.
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Ross A. Little
2Centre for Imaging Sciences, University of Manchester, Manchester, United Kingdom.
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Alan Jackson
2Centre for Imaging Sciences, University of Manchester, Manchester, United Kingdom.
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Geoff J.M. Parker
2Centre for Imaging Sciences, University of Manchester, Manchester, United Kingdom.
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Andrew R. Reynolds
6Tumour Biology Team, Breakthrough Breast Cancer Research Centre, The Institute of Cancer Research, London, United Kingdom.
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John C. Waterton
2Centre for Imaging Sciences, University of Manchester, Manchester, United Kingdom.
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Simon P. Robinson
4Division of Radiotherapy and Imaging, The Institute of Cancer Research, London, United Kingdom.
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DOI: 10.1158/0008-5472.CAN-15-2062 Published February 2016
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Abstract

There is a clinical need for noninvasive biomarkers of tumor hypoxia for prognostic and predictive studies, radiotherapy planning, and therapy monitoring. Oxygen-enhanced MRI (OE-MRI) is an emerging imaging technique for quantifying the spatial distribution and extent of tumor oxygen delivery in vivo. In OE-MRI, the longitudinal relaxation rate of protons (ΔR1) changes in proportion to the concentration of molecular oxygen dissolved in plasma or interstitial tissue fluid. Therefore, well-oxygenated tissues show positive ΔR1. We hypothesized that the fraction of tumor tissue refractory to oxygen challenge (lack of positive ΔR1, termed “Oxy-R fraction”) would be a robust biomarker of hypoxia in models with varying vascular and hypoxic features. Here, we demonstrate that OE-MRI signals are accurate, precise, and sensitive to changes in tumor pO2 in highly vascular 786-0 renal cancer xenografts. Furthermore, we show that Oxy-R fraction can quantify the hypoxic fraction in multiple models with differing hypoxic and vascular phenotypes, when used in combination with measurements of tumor perfusion. Finally, Oxy-R fraction can detect dynamic changes in hypoxia induced by the vasomodulator agent hydralazine. In contrast, more conventional biomarkers of hypoxia (derived from blood oxygenation-level dependent MRI and dynamic contrast–enhanced MRI) did not relate to tumor hypoxia consistently. Our results show that the Oxy-R fraction accurately quantifies tumor hypoxia noninvasively and is immediately translatable to the clinic. Cancer Res; 76(4); 787–95. ©2015 AACR.

Footnotes

  • Note: Supplementary data for this article are available at Cancer Research Online (http://cancerres.aacrjournals.org/).

  • Received July 30, 2015.
  • Revision received November 9, 2015.
  • Accepted November 9, 2015.
  • ©2015 American Association for Cancer Research.
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Cancer Research: 76 (4)
February 2016
Volume 76, Issue 4
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Oxygen-Enhanced MRI Accurately Identifies, Quantifies, and Maps Tumor Hypoxia in Preclinical Cancer Models
James P.B. O'Connor, Jessica K.R. Boult, Yann Jamin, Muhammad Babur, Katherine G. Finegan, Kaye J. Williams, Ross A. Little, Alan Jackson, Geoff J.M. Parker, Andrew R. Reynolds, John C. Waterton and Simon P. Robinson
Cancer Res February 15 2016 (76) (4) 787-795; DOI: 10.1158/0008-5472.CAN-15-2062

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Oxygen-Enhanced MRI Accurately Identifies, Quantifies, and Maps Tumor Hypoxia in Preclinical Cancer Models
James P.B. O'Connor, Jessica K.R. Boult, Yann Jamin, Muhammad Babur, Katherine G. Finegan, Kaye J. Williams, Ross A. Little, Alan Jackson, Geoff J.M. Parker, Andrew R. Reynolds, John C. Waterton and Simon P. Robinson
Cancer Res February 15 2016 (76) (4) 787-795; DOI: 10.1158/0008-5472.CAN-15-2062
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