Multimodal assessment of early tumor response to chemotherapy: Comparison between diffusion-weighted MRI, 1H-MR spectroscopy of choline and USPIO particles targeted at cell death

NMR in Biomedicine

Volumn 25, Issue 4, 2012, Pages 514-522

  Radermacher, K A ^a   Magat, J ^a   Bouzin, C ^a   Laurent, S ^b   Dresselaers, T ^c   Himmelreich, U ^c   Boutry, S ^b   Mahieu, I ^b   Vander Elst, L ^b   Feron, O ^a   Muller, R N ^b   Jordan, B F ^a   Gallez, B ^a  

^a UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

^b UNIVERSITY OF MONS   (Belgium)

^c KU Leuven   (Belgium)

Author keywords

Choline; Diffusion weighted imaging; EPR; MR spectroscopy; MRI; Targeted contrast agent; Tumor response

Indexed keywords

CHOLINE; DIFFUSION-WEIGHTED IMAGING; MR SPECTROSCOPY; TARGETED CONTRAST AGENTS; TUMOR RESPONSE;

CELL DEATH; CHEMOTHERAPY; DIFFUSION; MAGNETIC RESONANCE; MAGNETIC RESONANCE IMAGING; MAGNETIC RESONANCE SPECTROSCOPY; PARAMAGNETIC RESONANCE;

TUMORS;

CHOLINE; CYCLOPHOSPHAMIDE; ETOPOSIDE; FLUOROURACIL; GADODIAMIDE; PHOSPHATIDYLSERINE; ULTRASMALL SUPERPARAMAGNETIC IRON OXIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER CHEMOTHERAPY; CANCER INHIBITION; CELL DEATH; CLINICAL ASSESSMENT; CLINICAL PROTOCOL; CONTRAST ENHANCEMENT; CONTROLLED STUDY; CORRELATIONAL STUDY; DIFFUSION WEIGHTED IMAGING; DRUG ACCUMULATION; INTERMETHOD COMPARISON; MALE; MOUSE; NEOPLASM; NONHUMAN; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; SURVIVAL RATE; TREATMENT RESPONSE; TUMOR MODEL;

ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; CELL LINE, TUMOR; CHOLINE; DEXTRANS; DIFFUSION MAGNETIC RESONANCE IMAGING; LIVER NEOPLASMS; MAGNETIC RESONANCE SPECTROSCOPY; MAGNETITE NANOPARTICLES; MICE; PROTONS; REPRODUCIBILITY OF RESULTS; SENSITIVITY AND SPECIFICITY; TREATMENT OUTCOME; TUMOR MARKERS, BIOLOGICAL;

MURINAE;

EID: 84858864636     PISSN: 09523480     EISSN: 10991492     Source Type: Journal    
DOI: 10.1002/nbm.1765     Document Type: Article

References (48)

1. De Saint-Hubert M, Prinsen K, Mortelmans L, Verbruggen A, and Mottaghy FM. Molecular imaging of cell death. Methods, 2009; 48: 178-187.
2. Therasse P, Arbuck SG, Eisenhauer EA, Wanders J, Kaplan RS, Rubinstein L, Verweij J, Van Glabbeke M, van Oosterom AT, Christian MC, and Gwyther SG. New guidelines to evaluate the response to treatment in solid tumors. European Organization for Research and Treatment of Cancer, National Cancer Institute of the United States, National Cancer Institute of Canada. J. Natl. Cancer Inst. 2000; 92: 205-216.
3. Chaiken L, Rege S, Hoh C, Choi Y, Jabour B, Juillard G, Hawkins R, and Parker R. Positron emission tomography with fluorodeoxyglucose to evaluate tumor response and control after radiation therapy. Int. J. Radiat. Oncol. Bio. Phys. 1993; 27: 455-464.
4. Berlangieri SU, Brizel DM, Scher RL, Schifter T, Hawk TC, Hamblen S, Coleman RE, and Hoffman JM. Pilot study of positron emission tomography in patients with advanced head and neck cancer receiving radiotherapy and chemotherapy. Head Neck, 1994; 16: 340-346.
5. Fadok VA, Voelker DR, Campbell PA, Cohen JJ, Bratton DL, and Henson PM. Exposure of phosphatidylserine on the surface of apoptotic lymphocytes triggers specific recognition and removal by macrophages. J. Immunol. 1992; 148: 2207-2216.
6. Blankenberg F, Mari C, and Strauss HW. Imaging cell death in vivo. Q. J. Nucl. Med. 2003; 47: 337-348.
7. Haas RL, de Jong D, Valdés Olmos RA, Hoefnagel CA, van den Heuvel I, Zerp SF, Bartelink H, and Verheij M. In vivo imaging of radiation-induced apoptosis in follicular lymphoma patients. Int. J. Radiat. Oncol. Biol. Phys. 2004; 59: 782-787.
8. Kartachova M, Haas RL, Olmos RA, Hoebers FJ, van Zandwijk N, and Verheij M. In vivo imaging of apoptosis by 99mTc-Annexin V scintigraphy: visual analysis in relation to treatment response. Radiother. Oncol. 2004; 72: 333-339.
9. Vermeersch H, Loose D, Lahorte C, Mervillie K, Dierckx R, Steinmetz N, Vanderheyden JL, Cuvelier C, Slegers G, and Van de Wiele C. 99mTc-HYNIC Annexin-V imaging of primary head and neck carcinoma. Nucl. Med. Commun. 2004; 25: 259-263.
10. Belhocine T, Steinmetz N, Green A, and Rigo P. In vivo imaging of chemotherapy-induced apoptosis in human cancers. Ann. N. Y. Acad. Sci. 2003; 1010: 525-529.
11. Laumonier C, Segers J, Laurent S, Michel A, Coppée F, Belayew A, Elst LV, and Muller RN. A new peptidic vector for molecular imaging of apoptosis, identified by phage display technology. J. Biomol. Screen. 2006; 11: 537-545.
12. Thapa N, Kim S, So IS, Lee BH, Kwon IC, Choi K, and Kim IS. Discovery of a phosphatidylserine-recognizing peptide and its utility in molecular imaging of tumour apoptosis. J. Cell. Mol. Med. 2007; 12: 1649-1660.
13. Hong HY, Choi JS, Kim YJ, Lee HY, Kwak W, Yoo J, Lee JT, Kwon TH, Kim IS, Han HS, and Lee BH. Detection of apoptosis in a rat model of focal cerebral ischemia using a homing peptide selected from in vivo phage display. J. Control Release, 2008; 131: 167-172.
14. Zhao M, Beauregard DA, Loizou L, Davletov B, and Brindle KM. Non-invasive detection of apoptosis using magnetic resonance imaging and a targeted contrast agent. Nat. Med. 2001; 7: 1241-1244.
15. Bose S, Tuunainen I, Parry M, Medina OP, Mancini G, and Kinnunen PK. Binding of cationic liposomes to apoptotic cells. Anal. Biochem. 2004; 331: 385-394.
16. Hanshaw RG, Lakshmi C, Lambert TN, Johnson JR, and Smith BD. Fluorescent detection of apoptotic cells by using zinc coordination complexes with a selective affinity for membrane surfaces enriched with phosphatidylserine. Chembiochem. 2005; 6: 2214-2220.
17. Quinti L, Weissleder R, and Tung CH. A fluorescent nanosensor for apoptotic cells. Nano. Lett. 2006; 6: 488-490.
18. Bullok KE, Gammon ST, Violini S, Prantner AM, Villalobos VM, Sharma V, and Piwnica-Worms D. Permeation peptide conjugates for in vivo molecular imaging applications. Mol. Imaging, 2006; 5: 1-15.
19. Zhou D, Chu W, Rothfuss J, Zeng C, Xu J, Jones L, Welch MJ, and Mach RH. Synthesis, radiolabeling, and in vivo evaluation of an 18F-labeled isatin analog for imaging caspase-3 activation in apoptosis. Bioorg. Med. Chem. Lett. 2006; 16: 5041-5046.
20. Cohen A, Ziv I, Aloya T, Levin G, Kidron D, Grimberg H, Reshef A, and Shirvan A. Monitoring of chemotherapy-induced cell death in melanoma tumors by N, N'-Didansyl-L-cystine. Technol. Cancer. Res. Treat. 2007; 6: 221-234.
21. Reshef A, Shirvan A, Waterhouse RN, Grimberg H, Levin G, Cohen A, Ulysse LG, Friedman G, Antoni G, and Ziv I. Molecular imaging of neurovascular cell death in experimental cerebral stroke by PET. J. Nucl. Med. 2008; 49: 1520-1528.
22. Radermacher KA, Beghein N, Boutry S, Laurent S, Vander Elst L, Muller RN, Jordan BF, and Gallez B. In vivo detection of inflammation using pegylated iron oxide particles targeted at E-selectin: a multimodal approach using MR imaging and EPR spectroscopy. Invest. Radiol. 2009; 44: 398-404.
23. Radermacher KA, Boutry S, Laurent S, Vander Elst L, Mahieu I, Bouzin C, Magat J, Gregoire V, Feron O, Muller RN, Jordan BF, and Gallez B. Iron Oxide Particles Covered with Hexapeptides Targeted at Phosphatidylserine as MR Biomarkers of Tumor Cell Death. Contrast Media Mol. Imaging, 2010; 5: 258-267.
24. Brindle KM. Detection of apoptosis in tumors using magnetic resonance imaging and spectroscopy. Adv. Enzyme Regul. 2002; 42: 101-112.
25. Moseley ME, Cohen Y, Mintorovitch J, Chileuitt L, Shimizu H, Kucharczyk J, Wendland MF, and Weinstein PR. Early detection of regional cerebral ischemia in cats: comparison of diffusion- and T2-weighted MRI and spectroscopy. Magn. Reson. Med. 1990; 14: 330-346.
26. Lidar Z, Mardor Y, Jonas T, Pfeffer R, Faibel M, Nass D, Hadani M, and Ram Z. Convection-enhanced delivery of paclitaxel for the treatment of recurrent malignant glioma: a phase I/II clinical study. J. Neurosurg. 2004; 100: 472-479.
27. Charles-Edwards EM and de Souza NM. Diffusion-weighted magnetic resonance imaging and its application to cancer. Cancer Imaging, 2006; 13: 135-143.
28. Deng J, Miller FH, Rhee TK, Sato KT, Mulcahy MF, Kulik LM, Salem R, Omary RA, and Larson AC. Diffusion-weighted MR imaging for determination of hepatocellular carcinoma response to yttrium-90 radioembolization. J. Vasc. Interv. Radiol. 2006; 17: 1195-1200.
29. Jordan BF, Runquist M, Raghunand N, Baker A, Williams R, Kirkpatrick L, Powis G, and Gillies RJ. Dynamic contrast-enhanced and diffusion MRI show rapid and dramatic changes in tumor microenvironment in response to inhibition of HIF-1alpha using PX-478. Neoplasia, 2005; 7: 475-485.
30. Szwergold BS. NMR spectroscopy of cells. Annu. Rev. Physiol. 1992; 54: 775-798.
31. Fulham MJ, Bizzi A, Dietz MJ, Shih HH, Raman R, Sobering GS, Frank JA, Dwyer AJ, Alger JR, and Di Chiro G. Mapping of brain tumor metabolites with proton MR spectroscopic imaging: clinical relevance. Radiology, 1992; 185: 675-686.
32. Usenius JP, Vainio P, Hernesniemi J, and Kauppinen RA. Choline-containing compounds in human astrocytomas studied by 1H NMR spectroscopy in vivo and in vitro. J. Neurochem. 1994; 63: 1538-1543.
33. Negendank WG, Brown TR, Evelhoch JL, Griffiths JR, Liotta LA, Margulis AR, Morrisett JD, Ross BD, and Shtern F. Proceedings of a National Cancer Institute workshop: MR spectroscopy and tumor cell biology. Radiology, 1992; 185: 875-883.
34. Leach MO, Verrill M, Glaholm J, Smith TA, Collins DJ, Payne GS, Sharp JC, Ronen SM, McCready VR, Powles TJ, and Smith IE. Measurements of human breast cancer using magnetic resonance spectroscopy: a review of clinical measurements and a report of localized 31P measurements of response to treatment. NMR Biomed. 1998; 11: 314-340.
35. Jordan BF, Black K, Robey IF, Runquist M, Powis G, and Gillies RJ. Metabolite changes in HT-29 xenograft tumors following HIF-1alpha inhibition with PX-478 as studied by MR spectroscopy in vivo and ex vivo. NMR Biomed. 2005; 18: 430-439.
36. Payne GS and Leach MO. Applications of magnetic resonance spectroscopy in radiotherapy treatment planning. Br. J. Radiol. 2006; 79: 16-26.
37. Shah N, Sattar A, Benanti M, Hollander S, and Cheuck L. Magnetic resonance spectroscopy as an imaging tool for cancer: a review of the literature. J. Am. Osteopath. Assoc. 2006; 106: 23-27.
38. Taper H, Woolley GW, Teller MN, Lardis MP. A new transplantable mouse liver tumor of spontaneous origin. Cancer Res. 1966; 26: 143-148.
39. Port M, Corot C, Raynal I, and Rousseaux O. Novel compositions magnetic particles covered with gem-bisphosphonate derivatives. US Patent 2004/0253181 A1.
40. Iannone A, Federico M, Tomasi A, Magin RL, Casasco A, Calligaro A, and Vannini V. Detection and quantification in rat tissues of the superparamagnetic magnetite resonance contrast agent dextran magnetite as demonstrated by electron spin resonance spectroscopy. Invest. Radiol. 1992; 27: 450-455.
41. Fujii H, Yoshikawa K, and Berliner LJ. In vivo fate of superparamagnetic iron oxides during sepsis. Magn. Reson. Imag. 2002; 20: 271-276.
42. Hamstra DA, Rehemtulla A, and Ross BD. Diffusion magnetic resonance imaging: a biomarker for treatment response in oncology. J. Clin. Oncol. 2007; 25: 4104-4109.
43. Padhani AR, Liu G, Mu-Koh D, Chenevert TL, Thoeny HC, Takahara T, Dzik-Jurasz A, Ross BD, Van Cauteren M, Collins D, Hammoud DA, Rustin GJS, Taouli B, and Choyke PL. Neoplasia, 2009; 11: 102-125.
44. Bizzi A, Movsas B, Tedeschi G, Phillips CL, Okunieff P, Alger JR, and Di Chiro G. Response of non-Hodgkin lymphoma to radiation therapy: early and long-term assessment with H-1 MR spectroscopic imaging. Radiology, 1995; 194: 271-276.
45. Schwarz AJ, Maisey NR, Collins DJ, Cunningham D, Huddart R, and Leach MO. Early in vivo detection of metabolic response: a pilot study of 1H MR spectroscopy in extracranial lymphoma and germ cell tumours. Br. J. Radiol. 2002; 75: 959-966.
46. Seierstad T, Røe K, Olsen DR. Noninvasive monitoring of radiation-induced treatment response using proton magnetic resonance spectroscopy and diffusion-weighted magnetic resonance imaging in a colorectal tumor model. Radiother. Oncol. 2007; 85: 187-194.
47. Strauss HW, Blankenberg F, Vanderheyden JL, and Tait J. Translational imaging: imaging of apoptosis. Handb. Exp. Pharmacol. 2008; 185: 259-275.
48. Beloueche-Babari M, Chung YL, Al-Saffar NM, Falck-Miniotis M, Leach MO. Metabolic assessment of the action of targeted cancer therapeutics using magnetic resonance spectroscopy. Br. J. Cancer. 2010; 102: 1-7.