Dynamic oxygen challenge evaluated by NMR T1 and T2* - insights into tumor oxygenation

NMR in Biomedicine

Volumn 28, Issue 8, 2015, Pages 937-947

  Zhao, Dawen ^a   Pacheco Torres, Jesús ^a,b,d   Hallac, Rami R ^a   White, Derek ^a   Peschke, Peter ^c   Cerdán, Sebastian ^b   Mason, Ralph P ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b INSTITUTO DE INVESTIGACIONES BIOMÉDICAS ALBERTO SOLS   (Spain)

^c GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^d MIGUEL HERNÁNDEZ UNIVERSITY   (Spain)

Author keywords

BOLD; Carbogen; Hypoxia; MRI; Oxygen; Prostate; TOLD; Tumor

Indexed keywords

BIOMARKERS; MAGNETIC RESONANCE IMAGING; OXYGEN; OXYGENATION; UROLOGY;

BOLD; CARBOGEN; HYPOXIA; PROSTATE; TOLD;

TUMORS;

BIOLOGICAL MARKER; CARBOGEN; OXYGEN; CARBON DIOXIDE; CONTRAST MEDIUM; TUMOR MARKER;

ADULT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BOLD SIGNAL; BREATHING; CANCER PROGNOSIS; CONTROLLED STUDY; CORRELATION ANALYSIS; DYNAMICS; FEASIBILITY STUDY; GAS; HYPEROXIA; HYPOXIA; IMAGE ANALYSIS; MALE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEAR MAGNETIC RESONANCE SCANNER; OXYGENATION; PRIORITY JOURNAL; PROSTATE ADENOCARCINOMA; RADIATION RESPONSE; RADIOLOGICAL PARAMETERS; RADIOSENSITIVITY; RAT; TOLD SIGNAL; TUMOR CELL LINE; TUMOR VOLUME; ANIMAL; CELL HYPOXIA; INHALATIONAL DRUG ADMINISTRATION; METABOLISM; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; OXIMETRY; PROCEDURES; PROSTATIC NEOPLASMS; REPRODUCIBILITY; SENSITIVITY AND SPECIFICITY;

RATTUS;

ADMINISTRATION, INHALATION; ANIMALS; BIOMARKERS, TUMOR; CARBON DIOXIDE; CELL HYPOXIA; CELL LINE, TUMOR; CONTRAST MEDIA; MAGNETIC RESONANCE SPECTROSCOPY; MALE; OXIMETRY; OXYGEN; PROSTATIC NEOPLASMS; RATS; REPRODUCIBILITY OF RESULTS; SENSITIVITY AND SPECIFICITY;

EID: 84937250755     PISSN: 09523480     EISSN: 10991492     Source Type: Journal    
DOI: 10.1002/nbm.3325     Document Type: Article

References (67)

1. Tatum JL, Kelloff GJ, Gillies RJ, Arbeit JM, Brown JM, Chao KSC, Chapman JD, Eckelman WC, Fyles AW, Giaccia AJ, Hill RP, Koch CJ, Krishna MC, Krohn KA, Lewis JS, Mason RP, Melillo G, Padhani AR, Powis G, Rajendran JG, Reba R, Robinson SP, Semenza GL, Swartz HM, Vaupel P, Yang D, Croft B, Hoffman J, Liu GY, Stone H, Sullivan D. Hypoxia: importance in tumor biology, noninvasive measurement by imaging, and value of its measurement in the management of cancer therapy. Int. J. Radiat. Biol. 2006; 82: 699-757.
2. Gray L, Conger A, Ebert M, Hornsey S, Scott O. The concentration of oxygen dissolved in tissues at time of irradiation as a factor in radiotherapy. Br. J. Radiol. 1953; 26: 638-648.
3. O2 ratio predicts for outcome in patients with localized prostate cancer: long-term results. Int. J. Radiat. Oncol. Biol. Phys. 2012; 82: E433-E439.
4. Mason RP, Zhao D, Pacheco-Torres J, Cui W, Kodibagkar VD, Gulaka PK, Hao G, Thorpe P, Hahn EW, Peschke P. Multimodality imaging of hypoxia in preclinical settings. Q. J. Nucl. Med. Mol. Imaging 2010; 54: 259-280.
5. Pacheco-Torres J, López-Larrubia P, Ballesteros P, Cerdán S. Imaging tumor hypoxia by magnetic resonance methods. NMR Biomed. 2011; 24: 1-16.
6. Vergis R, Corbishley CM, Norman AR, Bartlett J, Jhavar S, Borre M, Heeboll S, Horwich A, Huddart R, Khoo V, Eeles R, Cooper C, Sydes M, Dearnaley D, Parker C. Intrinsic markers of tumour hypoxia and angiogenesis in localised prostate cancer and outcome of radical treatment: a retrospective analysis of two randomised radiotherapy trials and one surgical cohort study. Lancet Oncol. 2008; 9: 342-351.
7. Alonzi R, Padhani AR, Maxwell RJ, Taylor NJ, Stirling JJ, Wilson JI, d'Arcy JA, Collins DJ, Saunders MI, Hoskin PJ. Carbogen breathing increases prostate cancer oxygenation: a translational MRI study in murine xenografts and humans. Br. J. Cancer 2009; 100: 644-648.
8. 2*) with oxygen electrode measurements: a pilot study in men with prostate cancer. Int. J. Radiat. Biol. 2009; 85: 805-813.
9. Rijpkema M, Kaanders JH, Joosten FB, van der Kogel AJ, Heerschap A. Effects of breathing a hyperoxic hypercapnic gas mixture on blood oxygenation and vascularity of head-and-neck tumors as measured by magnetic resonance imaging. Int. J. Radiat. Oncol. Biol. Phys. 2002; 53: 1185-1191.
10. O'Connor JPB, Naish JH, Parker GJM, Waterton JC, Watson Y, Jayson GC, Buonaccorsi GA, Cheung S, Buckley DL, McGrath D, West CML, Davidson SE, Roberts C, Mills SJ, Mitchell CL, Hope L, Ton C, Jackson A. Preliminary study of oxygen-enhanced longitudinal relaxation in MRI: a potential novel biomarker of oxygenation changes in solid tumors. Int. J. Radiat. Oncol. Biol. Phys. 2009; 75: 1209-1215.
11. Hallac RR, Ding Y, Yuan Q, McColl RW, Lea J, Sims RD, Weatherall PT, Mason RP. Oxygenation in cervical cancer and normal uterine cervix assessed using blood oxygenation level-dependent (BOLD) MRI at 3T. NMR Biomed. 2012; 25: 1321-1330.
12. Jiang L, Weatherall PT, McColl RW, Tripathy D, Mason RP. Blood oxygenation level-dependent (BOLD) contrast magnetic resonance imaging (MRI) for prediction of breast cancer chemotherapy response: a pilot study. J. Magn. Reson. Imaging 2013; 37: 1083-1092.
13. 2* changes during respiratory challenges for the assessment of blood and tissue oxygenation. Magn. Reson. Med. 2013; 70: 136-146.
14. Linnik IV, Scott MLJ, Holliday KF, Woodhouse N, Waterton JC, O'Connor JPB, Barjat H, Liess C, Ulloa J, Young H, Dive C, Hodgkinson CL, Ward T, Roberts D, Mills SJ, Thompson G, Buonaccorsi GA, Cheung S, Jackson A, Naish JH, Parker GJM. Noninvasive tumor hypoxia measurement using magnetic resonance imaging in murine U87 glioma xenografts and in patients with glioblastoma. Magn. Reson. Med. 2014; 71: 1854-1862.
15. Robinson SP, Collingridge DR, Howe FA, Rodrigues LM, Chaplin DJ, Griffiths JR. Tumor response to hypercapnia and hyperoxia monitored by FLOOD magnetic resonance imaging. NMR Biomed. 1999; 12: 98-106.
16. Al-Hallaq HA, River JN, Zamora M, Oikawa H, Karczmar GS. Correlation of magnetic resonance and oxygen microelectrode measurements of carbogen-induced changes in tumor oxygenation. Int. J. Radiat. Oncol. Biol. Phys. 1998; 41: 151-159.
17. 2) inside tumors? Magn. Reson. Med. 2002; 48: 980-986.
18. Dunn JF, O'Hara JA, Zaim-Wadghiri Y, Lei H, Meyerand ME, Grinberg OY, Hou H, Hoopes PJ, Demidenko E, Swartz HM. Changes in oxygenation of intracranial tumors with carbogen: a BOLD MRI and EPR oximetry study. J. Magn. Reson. Imaging 2002; 16: 511-521.
19. Elas M, Williams BB, Parasca A, Mailer C, Pelizzari CA, Lewis MA, River JN, Karczmar GS, Barth ED, Halpern HJ. Quantitative tumor oxymetric images from 4D electron paramagnetic resonance imaging (EPRI): methodology and comparison with blood oxygen level-dependent (BOLD) MRI. Magn. Reson. Med. 2003; 49: 682-691.
20. 19F MRI to investigate tumor oxygenation. Magn. Reson. Med. 2009; 62: 357-364.
21. Fan XB, River JN, Zamora M, Al-Hallaq HA, Karczmar GS. Effect of carbogen on tumor oxygenation: combined fluorine-19 and proton MRI measurements. Int. J. Radiat. Oncol. Biol. Phys. 2002; 54: 1202-1209.
22. Robinson SP, Rijken PF, Howe FA, McSheehy PM, van der Sanden BP, Heerschap A, Stubbs M, Van Der Kogel AJ, Griffiths JR. Tumor vascular architecture and function evaluated by non-invasive susceptibility MRI methods and immunohistochemistry. J. Magn. Reson. Imaging 2003; 17: 445-454.
23. 2* as a noninvasive imaging biomarker of improved tumor oxygenation. Int. J. Radiat. Oncol. Biol. Phys. 2013; 87: 160-167.
24. Howe FA, Robinson SP, McIntyre DJO, Stubbs M, Griffiths JR. Issues in flow and oxygenation dependent contrast (FLOOD) imaging of tumours. NMR Biomed. 2001; 14: 497-506.
25. Baudelet C, Gallez B. Current issues in the utility of blood oxygen level dependent MRI for the assessment of modulations in tumor oxygenation. Curr. Med. Imaging Rev. 2005; 1: 229-243.
26. Robinson SP, Rijken P, Howe FA, McSheehy PMJ, van der Sanden BPJ, Heerschap A, Stubbs M, van der Kogel AJ, Griffiths JR. Tumor vascular architecture and function evaluated by non-invasive susceptibility MRI methods and immunohistochemistry. J. Magn. Reson. Imaging 2003; 17: 445-454.
27. Berkowitz BA, McDonald C, Ito Y, Tofts PS, Latif Z, Gross J. Measuring the human retinal oxygenation response to a hyperoxic challenge using MRI: eliminating blinking artifacts and demonstrating proof of concept. Magn. Reson. Med. 2001; 46: 412-416.
28. Akber SF. Correlation between oxygen tension and spin-lattice relaxation rate in tumors. Eur. J. Radiol. 1989; 9: 56-59.
29. Matsumoto K, Bernardo M, Subramanian S, Choyke P, Mitchell JB, Krishna MC, Lizak MJ. MR assessment of changes of tumor in response to hyperbaric oxygen treatment. Magn. Reson. Med. 2006; 56: 240-246.
30. Winter JD, Akens MK, Cheng H-LM. Quantitative MRI assessment of VX2 tumour oxygenation changes in response to hyperoxia and hypercapnia. Phys. Med. Biol. 2011; 56: 1225.
31. 2* modulation by oxygen and carbogen. Magn. Reson. Med. 2009; 61: 75-83.
32. 1 as imaging biomarkers of tumor oxygenation. J. Magn. Reson. Imaging 2013; 38: 429-434.
33. 2 and relevance to tumor radiation response. Magn. Reson. Med. 2014; 71: 1863-1873.
34. Zhao D, Constantinescu A, Chang C-H, Hahn EW, Mason RP. Correlation of tumor oxygen dynamics with radiation response of the Dunning prostate R3327-HI tumor. Radiat. Res. 2003; 159: 621-631.
35. Bourke VA, Zhao D, Gilio J, Chang C-H, Jiang L, Hahn EW, Mason RP. Correlation of radiation response with tumor oxygenation in the Dunning prostate R3327-AT1 tumor. Int. J. Radiat. Oncol. Biol. Phys. 2007; 67: 1179-1186.
36. Zhao D, Ran S, Constantinescu A, Hahn EW, Mason RP. Tumor oxygen dynamics: correlation of in vivo MRI with histological findings. Neoplasia 2003; 5: 308-318.
37. Zhao D, Constantinescu C, Hahn EW, Mason RP. Differential oxygen dynamics in two diverse Dunning prostate R3327 rat tumor sublines (MAT-Lu and HI) with respect to growth and respiratory challenge. Int. J. Radiat. Oncol. Biol. Phys. 2002; 53: 744-756.
38. Peschke P, Hahn EW, Wenz F, Lohr F, Braunschweig F, Wolber G, Zuna I, Wannenmacher M. Differential sensitivity of three sublines of the rat Dunning prostate tumor system R3327 to radiation and/or local tumor hyperthermia. Radiat. Res. 1998; 150: 423-430.
39. Isaacs JT, Isaac WB, Feitz WFJ, Scheres J. Establishment and characterization of 7 Dunning prostate cancer cell lines and their use in developing methods for predicting metastatic ability of prostate cancer. Prostate 1986; 9: 261-281.
40. Hahn EW, Peschke P, Mason RP, Babcock EE, Antich PP. Isolated tumor growth in a surgically formed skin pedicle in the rat: a new tumor model for NMR studies. Magn. Reson. Imaging 1993; 11: 1007-1017.
41. Zechmann CM, Woenne EC, Brix G, Radzwill N, Ilg M, Bachert P, Peschke P, Kirsch S, Kauczor HU, Delorme S, Semmler W, Kiessling F. Impact of stroma on the growth, microcirculation, and metabolism of experimental prostate tumors. Neoplasia 2007; 9: 57-67.
42. Zhao D, Constantinescu A, Hahn EW, Mason RP. Tumor oxygen dynamics with respect to growth and respiratory challenge: investigation of the Dunning prostate R3327-HI tumor. Radiat. Res. 2001; 156: 510-520.
43. 31P-MR spectroscopy and in-vivo radiosensitivity. In Tumor Oxygenation, Vaupel PW, Kelleher DK, Günderoth M (eds). Gustav Fischer: Stuttgart, 1995, pp. 95-105.
44. Liu H, Gu Y, Kim JG, Mason RP. Near infrared spectroscopy and imaging of tumor vascular oxygenation. Methods Enzymol. 2004; 386: 349-378.
45. 2* the case of insulin and NS-398, two inhibitors of oxygen consumption. Magn. Reson. Med. 2006; 56: 637-643.
46. Arias N, Pacheco-Torres J, López-Larrubia P. Predicting response to hyperbaric oxygen radiotherapy treatment in high grade gliomas using magnetic resonance imaging techniques. In Proceedings of the ISMRM 20th Annual Meeting, Melbourne, International Society of Magnetic Resonance in Medicine: Berkley, CA; 2012, p. 852.
47. 2* is a prognostic indicator of acute radiotherapeutic response in rodent tumors. J. Magn. Reson. Imaging 2004; 19: 482-488.
48. Jiang L, Zhao D, Constantinescu A, Mason RP. Comparison of BOLD contrast and Gd-DTPA dynamic contrast enhanced imaging in rat prostate tumor. Magn. Reson. Med. 2004; 51: 953-960.
49. McPhail LD, Robinson SP. Intrinsic susceptibility MR imaging of chemically induced rat mammary tumors: relationship to histologic assessment of hypoxia and fibrosis. Radiology 2010; 254: 110-118.
50. McSheehy PMJ, Weidensteiner C, Cannet C, Ferretti S, Laurent D, Ruetz S, Stumm M, Allegrini PR. Quantified tumor T1 is a generic early-response imaging biomarker for chemotherapy reflecting cell viability. Clin. Cancer Res. 2010; 16: 212-225.
51. Howe FA, Robinson SP, Rodrigues LM, Griffiths JR. Flow and oxygenation dependent (FLOOD) contrast MR imaging to monitor the response of rat tumors to carbogen breathing. Magn. Reson. Imaging 1999; 17: 1307-1318.
52. Zhang Z, Hallac RR, Peschke P, Mason RP. A noninvasive tumor oxygenation imaging strategy using magnetic resonance imaging of endogenous blood and tissue water. Magn. Reson. Med. 2014; 71: 561-569.
53. 1 relaxation time at 0.2 Tesla for monitoring regional hyperthermia: feasibility study in muscle and adipose tissue. Magn. Reson. Med. 2002; 47: 1194-1201.
54. Zaharchuk G, Busse RF, Rosenthal G, Manley GT, Glenn OA, Dillon WP. Noninvasive oxygen partial pressure measurement of human body fluids in vivo using magnetic resonance imaging. Acad. Radiol. 2006; 13: 1016-1024.
55. 2) relaxation time constants at 11.7 Tesla. Magn. Reson. Mat. Phys. Biol. Med. 2012; 25: 245-249.
56. Zhao D, Jiang L, Mason RP. Measuring changes in tumor oxygenation. Methods Enzymol. 2004; 386: 378-418.
57. 19F MRI in a mouse model. Magn. Reson. Med. 2013; 69: 248-254.
58. 19F nuclear magnetic resonance methodologies for the assessment of tumour hypoxia. Phil. Trans. Biol. Sci. 2004; 359: 987-996.
59. Kodibagkar VD, Wang X, Pacheco-Torres J, Gulaka P, Mason RP. Proton imaging of siloxanes to map tissue oxygenation levels (PISTOL): a tool for quantitative tissue oximetry. NMR Biomed. 2008; 21: 899-907.
60. Mason RP, Antich PP, Babcock EE, Constantinescu A, Peschke P, Hahn EW. Non-invasive determination of tumor oxygen tension and local variation with growth. Int. J. Radiat. Oncol. Biol. Phys. 1994; 29: 95-103.
61. Krohn KA, Link JM, Mason RP. Molecular imaging of hypoxia. J. Nucl. Med. 2008; 49: 129S-148S.
62. Tran L-B-A, Bol A, Labar D, Jordan B, Magat J, Mignion L, Gregoire V, Gallez B. Hypoxia imaging with the nitroimidazole 18F-FAZA PET tracer: a comparison with OxyLite, EPR oximetry and 19F-MRI relaxometry. Radiother. Oncol. 2012; 105: 29-35.
63. Oehler C, O'Donoghue JA, Russell J, Zanzonico P, Lorenzen S, Ling CC, Carlin S. F-18-fluromisonidazole PET imaging as a biomarker for the response to 5, 6-dimethylxanthenone-4-acetic acid in colorectal xenograft tumors. J. Nucl. Med. 2011; 52: 437-444.
64. Gu Y, Xia M, Liu H, Kodibagkar V, Constantinescu A, Mason RP. Correlation of NIR spectroscopy with BOLD MR imaging of assessing breast tumor vascular oxygen status. In Biomedical Topical Meeting. OSA Technical Digest (Optical Society of America, 2004), paper FB6. doi:10.1364/BIO.2004.FB6
65. 19F magnetic resonance imaging in rats. Phys. Med. Biol. 2006; 51: 45-60.
66. Burton NC, Patel M, Morscher S, Driessen WHP, Claussen J, Beziere N, Jetzfellner T, Taruttis A, Razansky D, Bednar B, Ntziachristos V. Multispectral opto-acoustic tomography (MSOT) of the brain and glioblastoma characterization. Neuroimage 2013; 65: 522-528.
67. Jordan BF, Magat J, Colliez F, Ozel E, Fruytier A-C, Marchand V, Mignion L, Bouzin C, Cani PD, Vandeputte C, Feron O, Delzenne N, Himmelreich U, Denolin V, Duprez T, Gallez B. Mapping of oxygen by imaging lipids relaxation enhancement: a potential sensitive endogenous MRI contrast to map variations in tissue oxygenation. Magn. Reson. Med. 2013; 70: 732-744.