Abstract
Objective
To develop and test in a clinical setting a double-echo segmented echo planar imaging (DEPI) pulse sequence for proton resonance frequency (PRF)-based temperature monitoring that is faster than conventional PRF thermometry pulse sequences and not affected by thermal changes in tissue conductivity.
Materials and methods
Four tumor patients underwent between one and nine magnetic resonance (MR)-guided regional hyperthermia treatments. During treatment, the DEPI sequence and a FLASH PRF sequence were run in an interleaved manner to compare the results from both sequences in the same patients and same settings. Temperature maps were calculated based on the phase data of both sequences. Temperature measurements of both techniques were compared using Passing and Bablok regression and the Bland–Altman method.
Results
The temperature results from the DEPI and FLASH sequences, on average, do not differ by more than ΔT = 1 °C. DEPI images showed typically more artifacts and approximately a twofold lower signal-to-noise ratio (SNR), but a sufficient temperature precision of 0.5°, which would theoretically allow for a fivefold higher frame rate.
Conclusion
The results indicate that DEPI can replace slower temperature measurement techniques for PRF-based temperature monitoring during thermal treatments. The higher acquisition speed can be exploited for hot spot localization during regional hyperthermia as well as for temperature monitoring during fast thermal therapies.
Similar content being viewed by others
References
Issels RD, Lindner LH, Verweij J, Wust P, Reichardt P, Schem BC, Abdel-Rahman S, Daugaard S, Salat C, Wendtner CM, Vujaskovic Z, Wessalowski R, Jauch KW, Dürr HR, Ploner F, Baur-Melnyk A, Mansmann U, Hiddemann W, Blay JY, Hohenberger P, European Organisation for Research and Treatment of Cancer Soft Tissue and Bone Sarcoma Group (EORTC-STBSG), European Society for Hyperthermic Oncology (ESHO) (2010) Neo-adjuvant chemotherapy alone or with regional hyperthermia for localised high-risk soft-tissue sarcoma: a randomised phase 3 multicentre study. Lancet Oncol 11(6):561–570
van der Zee J, González González D, van Rhoon GC, van Dijk JD, van Putten WL, Hart AA (2000) Comparison of radiotherapy alone with radiotherapy plus hyperthermia in locally advanced pelvic tumours: a prospective, randomised, multicentre trial. Dutch Deep Hyperthermia Group Lancet 355(9210):1119–1125
Falk MH, Issels RD (2001) Hyperthermia in oncology. Int J Hyperthermia 17(1):1–18
Nadobny J, Wlodarczyk W, Westhoff L, Gellermann J, Rau B, Mönich G, Wust P (2003) Development and evaluation of a 3D hyperthermia applicator with water-coated antennas (WACOA). Med Phys 30:2052–2064
Nadobny J, Wlodarczyk W, Westhoff L, Gellermann J, Felix R, Wust P (2005) A clinical water-coated antenna applicator for MR-controlled deep-body hyperthermia: a comparison of calculated and measured 3-D temperature data sets. IEEE T Biomed Eng 52(3):505–519
Sreenivasa G, Gellermann J, Rau B, Nadobny J, Schlag P, Deuflhard P, Felix R, Wust P (2003) Clinical use of the hyperthermia treatment planning system HyperPlan to predict effectiveness and toxicity. Int J Radiat Oncol 55(2):407–419
Fujita S, Tamazawa M, Kuroda K (1998) Effects of blood perfusion rate on the optimization of RF-capacitive hyperthermia. IEEE T Biomed Eng 45(9):1182–1186
Peller M, Kurze V, Loeffler R, Pahernik S, Dellian M, Goetz AE, Issels R, Reiser M (2003) Hyperthermia induces T1 relaxation and blood flow changes in tumors. A MRI thermometry study in vivo. J Magn Reson Imaging 21(5):545–551
Hindman JC (1966) Proton resonance shift of water in the gas and liquid states. J Chem Phys 44:4582–4592
Ishihara Y, Calderon A, Watanabe H, Okamoto K, Suzuki Y, Kuroda K, Suzuki Y (1995) A precise and fast temperature mapping using water proton chemical shift. Magn Reson Med 34:814–823
De Poorter J, De Wagter C, De Deene Y, Thomsen C, Ståhlberg F, Achten E (1995) Noninvasive MRI thermometry with the proton resonance frequency (PRF) method: in vivo results in human muscle. Magn Reson Med 33(1):74–81
Gellermann J, Wlodarczyk W, Feussner A, Fähling H, Nadobny J, Hildebrandt B, Felix R, Wust P (2005) Methods and potentials of magnetic resonance imaging for monitoring radiofrequency hyperthermia in a hybrid system. Int J Hyperther 21(6):497–513
McDannold N (2005) Quantitative MRI-based temperature mapping based on the proton resonant frequency shift: review of validation studies. Int J Hyperther 21(6):533–546
Bottomley PA, Andrew ER (1978) RF magnetic field penetration, phase shift and power dissipation in biological tissue: implications for NMR imaging. Phys Med Biol 23:630–643
Peters RD, Henkelman RM (2000) Proton-resonance frequency shift MR thermometry is affected by changes in the electrical conductivity of tissue. Magn Reson Med 43(1):62–71
Weidensteiner C, Quesson B, Caire-Gana B, Kerioui N, Rullier A, Trillaud H, Moonen CT (2003) Real-time MR temperature mapping of rabbit liver in vivo during thermal ablation. Magn Reson Med 50(2):322–330
Kickhefel A, Roland J, Weiss C, Schick F (2010) Accuracy of real-time MR temperature mapping in the brain: a comparison of fast sequences. Phys Med 26(4):192–201
Cernicanu A, Lepetit-Coiffe M, Roland J, Becker CD, Terraz S (2008) Validation of fast MR thermometry at 1.5 T with gradient-echo echo planar imaging sequences: phantom and clinical feasibility studies. NMR Biomed 21(8):849–858
Stafford RJ, Price RE, Diederich CJ, Kangasniemi M, Olsson LE, Hazle JD (2004) Interleaved echo-planar imaging for fast multiplanar magnetic resonance temperature imaging of ultrasound thermal ablation therapy. J Magn Reson Imaging 20(4):706–714
Wust P, Gellermann J, Seebass M, Fähling H, Turner P, Wlodarczyk W, Nadobny J, Rau B, Hildebrandt B, Oppelt A, Schlag PM, Felix R (2004) Part-body hyperthermia with a radiofrequency multiantenna applicator under online control in a 1.5 T MR-tomograph. Rofo 176:363–374
Bernstein MA, King KF, Zhou XJ (2004) Handbook of MRI pulse sequences. Academic Press, Waltham
Haase A, Frahm J, Matthaei D, Hänicke W, Merboldt KD (1986) FLASH imaging. Rapid NMR imaging using low flip-angle pulses. J Magn Reson 67:258–266
Bowman RR (1976) A probe for measuring temperature in radio-frequency-heated material. IEEE T Microw Theory 24(1):43–45
Passing H, Bablok W (1983) A new biomedical procedure for testing the equality of measurements from two different analytical methods. J Clin Chem Clin Biol 21:709–720
Padoan A (2010) Passing and Bablok regression. http://www.mathworks.de/matlabcentral/fileexchange/24894-passing-and-bablok-regression. MATLAB central file exchange. Retrieved 4 April 2014
Bland JM, Altman DG (1986) Statistical methods for assessing agreement between two methods of clinical measurements. Lancet 1(8476):307–310
Gellermann J, Wlodarczyk W, Ganter H, Nadobny J, Fähling H, Seebass M, Felix R, Wust P (2005) A practical approach to thermography in a hyperthermia/magnetic resonance hybrid system: validation in a heterogeneous phantom. Int J Radiat Oncol 61(1):267–277
Numan WC, Hofstetter LW, Kotek G, Bakker JF, Fiveland EW, Houston GC, Kudielka G, Yeo DT, Paulides MM (2014) Exploration of MR-guided head and neck hyperthermia by phantom testing of a modified prototype applicator for use with proton resonance frequency shift thermometry. Int J Hyperther 30(3):184–191
Wlodarczyk W, Boroschewski R, Hentschel M, Wust P, Mönich G, Felix R (1998) Three-dimensional monitoring of small temperature changes for therapeutic hyperthermia using MR. J Magn Reson Imaging 8:165–174
Gudbjartsson H, Patz S (1995) The Rician distribution of noisy MRI data. Magn Reson Med 34(6):910–914
Carter DL, MacFall JR, Clegg ST, Wan X, Prescott DM, Charles HC, Samulski TV (1998) Magnetic resonance thermometry during hyperthermia for human high-grade sarcoma. Int J Radiat Oncol 40(4):815–822
Gellermann J, Wlodarczyk W, Hildebrandt B, Ganter H, Nicolau A, Rau B, Tilly W, Fähling H, Nadobny J, Felix R, Wust P (2005) Noninvasive magnetic resonance thermography of recurrent rectal carcinoma in a 1.5 Tesla hybrid system. Cancer Res 65(13):5872–5880
Gellermann J, Hildebrandt B, Issels R, Ganter H, Wlodarczyk W, Budach V, Felix R, Tunn PU, Reichardt P, Wust P (2006) Noninvasive magnetic resonance thermography of soft tissue sarcomas during regional hyperthermia: correlation with response and direct thermometry. Cancer 107(6):1373–1382
Sapareto SA, Dewey WC (1984) Thermal dose determination in cancer therapy. Int J Radiat Oncol 10:787–800
Stauffer P, Craciunescu O, Maccarini P, Wyatt C, Arunachalam K, Arabe O, Stakhursky V, Li Z, Soher B, Macfall J, Rangarao S, Cheng K, Das S, Martins C, Charles C, Dewhirst M, Wong T, Jones E, Vujaskovic Z (2009) Clinical utility of magnetic resonance thermal imaging (MRTI) for realtime guidance of deep hyperthermia. Proc SPIE 7181. doi:10.1117/12.812188
Craciunescu OI, Stauffer PR, Soher BJ, Wyatt CR, Arabe O, Maccarini P, Das SK, Cheng KS, Wong TZ, Jones EL, Dewhirst MW, Vujaskovic Z, MacFall JR (2009) Accuracy of real time noninvasive temperature measurements using magnetic resonance thermal imaging in patients treated for high grade extremity soft tissue sarcomas. Med Phys 36(11):4848–4858
Ellis S, Rieke V, Kohi M, Westphalen AC (2013) Clinical applications for magnetic resonance guided high intensity focused ultrasound (MRgHIFU): present and future. J Med Imag Radiat Oncol 57:391–399
Terraz S, Cernicanu A, Lepetit-Coiffé M, Viallon M, Salomir R, Mentha G, Becker CD (2010) Radiofrequency ablation of small liver malignancies under magnetic resonance guidance: progress in targeting and preliminary observations with temperature monitoring. Eur Radiol 20:886–897
Carpentier A, McNichols RJ, Stafford J, Guichard JP, Reizine D, Delaloge S, Vicaut E, Payen D, Gowda A, George B (2011) Laser thermal therapy: real-time MRI-guided and computer-controlled procedures for metastatic brain tumors. Laser Surg Med 43:943–950
Quesson B, Laurent C, Maclair G, de Senneville BD, Mougenot C, Ries M, Carteret T, Rullier A, Moonen CT (2011) Real-time volumetric MRI thermometry of focused ultrasound ablation in vivo: a feasibility study in pig liver and kidney. NMR Biomed 24(2):145–153
Celicanin Z, Auboiroux V, Bieri O, Petrusca L, Santini F, Viallon M, Scheffler K, Salomir R (2014) Real-time method for motion-compensated MR thermometry and MRgHIFU treatment in abdominal organs. Magn Reson Med 72(4):1087–1095
Auboiroux V, Viallon M, Roland J, Hyacinthe JN, Petrusca L, Morel DR, Goget T, Terraz S, Gross P, Becker CD, Salomir R (2012) ARFI-prepared MRgHIFU in liver: simultaneous mapping of ARFI-displacement and temperature elevation, using a fast GRE-EPI sequence. Magn Reson Med 68(3):932–946
Krafft AJ, Rauschenberg J, Maier F, Jenne JW, Bock M (2013) Crushed rephased orthogonal slice selection (CROSS) for simultaneous acquisition of two orthogonal proton resonance frequency temperature maps. J Magn Reson Imaging 38(6):1510–1520
Acknowledgments
This work was supported by the BMBF, Eurostars Project E!6620 PROFUS. The authors would like to thank Denis Kokorin and Maxim Zaitsev for their help in MR sequence programming.
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical standard
The patient studies were approved by the local ethics committee of the University Hospital Tübingen (UKT) and have, therefore, been performed in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki and its later amendments. All persons gave their informed consent prior to their inclusion in the study.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Dadakova, T., Gellermann, J., Voigt, O. et al. Fast PRF-based MR thermometry using double-echo EPI: in vivo comparison in a clinical hyperthermia setting. Magn Reson Mater Phy 28, 305–314 (2015). https://doi.org/10.1007/s10334-014-0467-y
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10334-014-0467-y