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Clinical evaluation of TOF versus non-TOF on PET artifacts in simultaneous PET/MR: a dual centre experience

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Abstract

Purpose

Our objective was to determine clinically the value of time-of-flight (TOF) information in reducing PET artifacts and improving PET image quality and accuracy in simultaneous TOF PET/MR scanning.

Methods

A total 65 patients who underwent a comparative scan in a simultaneous TOF PET/MR scanner were included. TOF and non-TOF PET images were reconstructed, clinically examined, compared and scored. PET imaging artifacts were categorized as large or small implant-related artifacts, as dental implant-related artifacts, and as implant-unrelated artifacts. Differences in image quality, especially those related to (implant) artifacts, were assessed using a scale ranging from 0 (no artifact) to 4 (severe artifact).

Results

A total of 87 image artifacts were found and evaluated. Four patients had large and eight patients small implant-related artifacts, 27 patients had dental implants/fillings, and 48 patients had implant-unrelated artifacts. The average score was 1.14 ± 0.82 for non-TOF PET images and 0.53 ± 0.66 for TOF images (p < 0.01) indicating that artifacts were less noticeable when TOF information was included.

Conclusion

Our study indicates that PET image artifacts are significantly mitigated with integration of TOF information in simultaneous PET/MR. The impact is predominantly seen in patients with significant artifacts due to metal implants.

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References

  1. Townsend DW. Combined positron emission tomography-computed tomography: the historical perspective. Semin Ultrasound CT MR. 2008;29:232–235.

    Article  PubMed  PubMed Central  Google Scholar 

  2. Delso G, Fürst S, Jakoby B, Ladebeck R, Ganter C, Nekolla SG, et al. Performance measurements of the Siemens mMR integrated whole-body PET/MR scanner. J Nucl Med. 2011;52:1914–1922. doi:10.2967/jnumed.111.092726.

    Article  PubMed  Google Scholar 

  3. Zaidi H, Ojha N, Morich M, Griesmer J, Hu Z, Maniawski P, et al. Design and performance evaluation of a whole-body Ingenuity TF PET-MRI system. Phys Med Biol. 2011;56:3091–3106. doi:10.1088/0031-9155/56/10/013.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Veit-Haibach P, Kuhn F, Wiesinger F, Delso G, von Schulthess G. PET-MR imaging using a tri-modality PET/CT-MR system with a dedicated shuttle in clinical routine. MAGMA. 2013;26:25–35. doi:10.1007/s10334-012-0344-5.

    Article  PubMed  Google Scholar 

  5. Nensa F, Beiderwellen K, Heusch P, Wetter A. Clinical applications of PET/MR: current status and future perspectives. Diagn Interv Radiol. 2014;20:438–447. doi:10.5152/dir.14008.

    Article  PubMed  PubMed Central  Google Scholar 

  6. Moses WW. Time of flight in PET revisited. IEEE Trans Nucl Sci. 2003;50:1325–1330. doi:10.1109/TNS.2003.817319.

    Article  Google Scholar 

  7. Levin C, Glover G, Deller T, McDaniel D, Peterson W, Maramraju SH. Prototype time-of-flight PET ring integrated with a 3T MRI system for simultaneous whole-body PET/MR imaging. JNM Meeting Abstracts. 2013;54:148.

    Google Scholar 

  8. Surti S. Update on time-of-flight PET imaging. J Nucl Med. 2015;56:98–105. doi:10.2967/jnumed.114.145029.

    Article  PubMed  Google Scholar 

  9. Surti S, Karp JS. Advances in time-of-flight PET. Phys Med. 2016;32:12–22. doi:10.1016/j.ejmp.2015.12.007.

    Article  PubMed  PubMed Central  Google Scholar 

  10. Vandenberghe S, Mikhaylova E, D’Hoe E, Mollet P, Karp JS. Recent developments in time-of-flight PET. EJNMMI Phys. 2016;3:3. doi:10.1186/s40658-016-0138-3.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Moses WW. Recent advances and future advances in time-of-flight PET. Nucl Instrum Methods Phys Res A. 2007;580:919–924. doi:10.1016/j.nima.2007.06.038.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Conti M. Focus on time-of-flight PET: the benefits of improved time resolution. Eur J Nucl Med Mol Imaging. 2011;38:1147–1157. doi:10.1007/s00259-010-1711-y.

    Article  PubMed  Google Scholar 

  13. Tomitani T. Image reconstruction and noise evaluation in photon time-of-flight assisted positron emission tomography. IEEE Trans Nucl Sci. 1981;28:4581–4589. doi:10.1109/TNS.1981.4335769.

    Article  Google Scholar 

  14. El Fakhri G, Surti S, Trott CM, Scheuermann J, Karp JS. Improvement in lesion detection with whole-body oncologic time-of-flight PET. J Nucl Med. 2011;52:347–353. doi:10.2967/jnumed.110.080382.

    Article  PubMed  PubMed Central  Google Scholar 

  15. Karp JS, Surti S, Daube-Witherspoon ME, Muehllehner G. Benefit of time-of-flight in PET: experimental and clinical results. J Nucl Med. 2008;49:462–470. doi:10.2967/jnumed.107.044834.

    Article  PubMed  PubMed Central  Google Scholar 

  16. Surti S, Karp JS. Experimental evaluation of a simple lesion detection task with time-of-flight PET. Phys Med Biol. 2009;54:373–384. doi:10.1088/0031-9155/54/2/013.

    Article  CAS  PubMed  Google Scholar 

  17. Lois C, Jakoby BW, Long MJ, Hubner KF, Barker DW, Casey ME, et al. An assessment of the impact of incorporating time-of-flight information into clinical PET/CT imaging. J Nucl Med. 2010;51:237–245. doi:10.2967/jnumed.109.068098.

    Article  PubMed  PubMed Central  Google Scholar 

  18. Daube-Witherspoon ME, Surti S, Perkins AE, Karp JS. Determination of accuracy and precision of lesion uptake measurements in human subjects with time-of-flight PET. J Nucl Med. 2014;55:602–607. doi:10.2967/jnumed.113.127035.

    Article  PubMed  PubMed Central  Google Scholar 

  19. Delso G, Khalighi M, Ter Voert E, Barbosa F, Sekine T, Hullner M, et al. Effect of time-of-flight information on PET/MR reconstruction artifacts: comparison of free-breathing versus breath-hold MR-based attenuation correction. Radiology. 2017:282;229–235. doi:10.1148/radiol.2016152509.

    Article  PubMed  Google Scholar 

  20. Hofmann M, Pichler B, Scholkopf B, Beyer T. Towards quantitative PET/MRI: a review of MR-based attenuation correction techniques. Eur J Nucl Med Mol Imaging. 2009;36 Suppl 1:S93–S104. doi:10.1007/s00259-008-1007-7.

    Article  PubMed  Google Scholar 

  21. Visvikis D, Monnier F, Bert J, Hatt M, Fayad H. PET/MR attenuation correction: where have we come from and where are we going? Eur J Nucl Med Mol Imaging. 2014;41:1172–1175. doi:10.1007/s00259-014-2748-0.

    Article  PubMed  Google Scholar 

  22. Wagenknecht G, Kaiser H-J, Mottaghy F, Herzog H. MRI for attenuation correction in PET: methods and challenges. Magn Reson Mater Phys. 2013;26:99–113. doi:10.1007/s10334-012-0353-4.

    Article  Google Scholar 

  23. Wollenweber SD, Ambwani S, Delso G, Lonn AHR, Mullick R, Wiesinger F, et al. Evaluation of an atlas-based PET head attenuation correction using PET/CT & MR patient data. IEEE Trans Nucl Sci. 2013;60:3383–3390. doi:10.1109/TNS.2013.2273417.

    Article  Google Scholar 

  24. Martinez-Moller A, Souvatzoglou M, Delso G, Bundschuh RA, Chefd’hotel C, Ziegler SI, et al. Tissue classification as a potential approach for attenuation correction in whole-body PET/MRI: evaluation with PET/CT data. J Nucl Med. 2009;50:520–526. doi:10.2967/jnumed.108.054726.

    Article  PubMed  Google Scholar 

  25. Wollenweber SD, Ambwani S, Lonn AHR, Shanbhag DD, Thiruvenkadam S, Kaushik S, et al. Comparison of 4-class and continuous fat/water methods for whole-body, MR-based PET attenuation correction. IEEE Trans Nucl Sci. 2013;60:3391–3398. doi:10.1109/TNS.2013.2278759.

    Article  Google Scholar 

  26. Paulus DH, Quick HH, Geppert C, Fenchel M, Zhan Y, Hermosillo G, et al. Whole-body PET/MR imaging: quantitative evaluation of a novel model-based MR attenuation correction method including bone. J Nucl Med. 2015;56:1061–1066. doi:10.2967/jnumed.115.156000.

    Article  PubMed  PubMed Central  Google Scholar 

  27. Delso G, Wiesinger F, Sacolick LI, Kaushik SS, Shanbhag DD, Hullner M, et al. Clinical evaluation of zero-echo-time MR imaging for the segmentation of the skull. J Nucl Med. 2015;56:417–422. doi:10.2967/jnumed.114.149997.

    Article  PubMed  Google Scholar 

  28. Cabello J, Lukas M, Forster S, Pyka T, Nekolla SG, Ziegler SI. MR-based attenuation correction using ultrashort-echo-time pulse sequences in dementia patients. J Nucl Med. 2015;56:423–429. doi:10.2967/jnumed.114.146308.

    Article  PubMed  Google Scholar 

  29. Sekine T, Ter Voert EE, Warnock G, Buck A, Huellner MW, Veit-Haibach P, et al. Clinical evaluation of zero-echo-time attenuation correction for brain 18F-FDG PET/MRI: comparison with atlas attenuation correction. J Nucl Med. 2016;57:1927–1932. doi:10.2967/jnumed.116.175398.

    Article  PubMed  Google Scholar 

  30. Nuyts J, Dupont P, Stroobants S, Benninck R, Mortelmans L, Suetens P. Simultaneous maximum a posteriori reconstruction of attenuation and activity distributions from emission sinograms. IEEE Trans Med Imaging. 1999;18:393–403. doi:10.1109/42.774167.

    Article  CAS  PubMed  Google Scholar 

  31. Rezaei A, Defrise M, Bal G, Michel C, Conti M, Watson C, et al. Simultaneous reconstruction of activity and attenuation in time-of-flight PET. IEEE Trans Med Imaging. 2012;31:2224–2233. doi:10.1109/tmi.2012.2212719.

    Article  PubMed  Google Scholar 

  32. Defrise M, Rezaei A, Nuyts J. Time-of-flight PET data determine the attenuation sinogram up to a constant. Phys Med Biol. 2012;57:885–899. doi:10.1088/0031-9155/57/4/885.

    Article  PubMed  Google Scholar 

  33. Brendle C, Schmidt H, Oergel A, Bezrukov I, Mueller M, Schraml C, et al. Segmentation-based attenuation correction in positron emission tomography/magnetic resonance: erroneous tissue identification and its impact on positron emission tomography interpretation. Invest Radiol. 2015;50:339–346. doi:10.1097/rli.0000000000000131.

    Article  PubMed  Google Scholar 

  34. Andersen FL, Ladefoged CN, Beyer T, Keller SH, Hansen AE, Hojgaard L, et al. Combined PET/MR imaging in neurology: MR-based attenuation correction implies a strong spatial bias when ignoring bone. Neuroimage. 2014;84:206–216. doi:10.1016/j.neuroimage.2013.08.042.

    Article  PubMed  Google Scholar 

  35. Davison H, ter Voert EE, de Galiza BF, Veit-Haibach P, Delso G. Incorporation of time-of-flight information reduces metal artifacts in simultaneous positron emission tomography/magnetic resonance imaging: a simulation study. Invest Radiol. 2015;50:423–429. doi:10.1097/RLI.0000000000000146.

    Article  PubMed  Google Scholar 

  36. Conti M. Why is TOF PET reconstruction a more robust method in the presence of inconsistent data? Phys Med Biol. 2011;56:155–168. doi:10.1088/0031-9155/56/1/010.

    Article  PubMed  Google Scholar 

  37. Bai C, Kinahan PE, Brasse D, Comtat C, Townsend DW, Meltzer CC, et al. An analytic study of the effects of attenuation on tumor detection in whole-body PET oncology imaging. J Nucl Med. 2003;44:1855–1861.

    PubMed  Google Scholar 

  38. Turkington TG, Wilson JM. Attenuation artifacts and time-of-flight PET. IEEE Nuclear Science Symposium Conference Record (NSS/MIC), New York, NY: IEEE; 2009. p. 2997–2999.

  39. Boellaard R, Hofman MB, Hoekstra OS, Lammertsma AA. Accurate PET/MR quantification using time of flight MLAA image reconstruction. Mol Imaging Biol. 2014;16:469–477. doi:10.1007/s11307-013-0716-x.

    Article  CAS  PubMed  Google Scholar 

  40. Antoch G, Freudenberg LS, Beyer T, Bockisch A, Debatin JF. To enhance or not to enhance? 18F-FDG and CT contrast agents in dual-modality 18F-FDG PET/CT. J Nucl Med. 2004;45:56S–65S.

    CAS  PubMed  Google Scholar 

  41. Zeimpekis KG, Barbosa F, Hullner M, ter Voert E, Davison H, Veit-Haibach P, et al. Clinical evaluation of PET image quality as a function of acquisition time in a new TOF-PET/MRI compared to TOF-PET/CT – initial results. Mol Imaging Biol. 2015;17:735–44. doi:10.1007/s11307-015-0845-5.

    Article  CAS  PubMed  Google Scholar 

  42. Salomon A, Goedicke A, Schweizer B, Aach T, Schulz V. Simultaneous reconstruction of activity and attenuation for PET/MR. IEEE Trans Med Imaging. 2011;30:804–813. doi:10.1109/tmi.2010.2095464.

    Article  PubMed  Google Scholar 

  43. Mehranian A, Zaidi H. Clinical assessment of emission- and segmentation-based MR-guided attenuation correction in whole-body time-of-flight PET/MR imaging. J Nucl Med. 2015;56:877–883. doi:10.2967/jnumed.115.154807.

    Article  PubMed  Google Scholar 

  44. Mehranian A, Zaidi H. Emission-based estimation of lung attenuation coefficients for attenuation correction in time-of-flight PET/MR. Phys Med Biol. 2015;60:4813–4833. doi:10.1088/0031-9155/60/12/4813.

    Article  PubMed  Google Scholar 

  45. Mehranian A, Zaidi H. MR constrained simultaneous reconstruction of activity and attenuation maps in brain TOF-PET/MR imaging. EJNMMI Phys. 2014;1 Suppl 1:A55. doi:10.1186/2197-7364-1-s1-a55.

    Article  PubMed  PubMed Central  Google Scholar 

  46. Mollet P, Keereman V, Bini J, Izquierdo-Garcia D, Fayad ZA, Vandenberghe S. Improvement of attenuation correction in time-of-flight PET/MR imaging with a positron-emitting source. J Nucl Med. 2014;55:329–336. doi:10.2967/jnumed.113.125989.

    Article  PubMed  PubMed Central  Google Scholar 

  47. Mollet P, Keereman V, Clementel E, Vandenberghe S. Simultaneous MR-compatible emission and transmission imaging for PET using time-of-flight information. IEEE Trans Med Imaging. 2012;31:1734–1742. doi:10.1109/tmi.2012.2198831.

    Article  PubMed  Google Scholar 

  48. Rothfuss H, Panin V, Moor A, Young J, Hong I, Michel C, et al. LSO background radiation as a transmission source using time of flight. Phys Med Biol. 2014;59:5483–5500. doi:10.1088/0031-9155/59/18/5483.

    Article  PubMed  Google Scholar 

  49. Ladefoged C, Andersen F, Keller S, Löfgren J, Hansen A, Holm S, et al. PET/MR imaging of the pelvis in the presence of endoprostheses: reducing image artifacts and increasing accuracy through inpainting. Eur J Nucl Med Mol Imaging. 2013;40:594–601. doi:10.1007/s00259-012-2316-4.

    Article  PubMed  Google Scholar 

  50. Schramm G, Maus J, Hofheinz F, Petr J, Lougovski A, Beuthien-Baumann B, et al. Evaluation and automatic correction of metal-implant-induced artifacts in MR-based attenuation correction in whole-body PET/MR imaging. Phys Med Biol. 2014;59:2713–2726. doi:10.1088/0031-9155/59/11/2713.

    Article  CAS  PubMed  Google Scholar 

  51. Carl M, Koch K, Du J. MR imaging near metal with undersampled 3D radial UTE-MAVRIC sequences. Magn Reson Med. 2013;69:27–36. doi:10.1002/mrm.24219.

    Article  PubMed  Google Scholar 

  52. den Harder JC, van Yperen GH, Blume UA, Bos C. Off-resonance suppression for multispectral MR imaging near metallic implants. Magn Reson Med. 2015;73:233–243. doi:10.1002/mrm.25126.

    Article  Google Scholar 

  53. Alessio AM, Stearns CW, Shan T, Ross SG, Kohlmyer S, Ganin A, et al. Application and evaluation of a measured spatially variant system model for PET image reconstruction. IEEE Trans Med Imaging. 2010;29:938–949. doi:10.1109/TMI.2010.2040188.

    Article  PubMed  PubMed Central  Google Scholar 

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Authors and Affiliations

  1. Department of Nuclear Medicine, University Hospital Zurich, Rämistrasse 100, CH-8091, Zurich, Switzerland

    Edwin E. G. W. ter Voert, Patrick Veit-Haibach & Martin Huellner

  2. University of Zurich, Zurich, Switzerland

    Edwin E. G. W. ter Voert, Patrick Veit-Haibach & Martin Huellner

  3. Department of Diagnostic and Interventional Radiology, University Hospital Zurich, Zurich, Switzerland

    Patrick Veit-Haibach

  4. GE Global Research, Niskayuna, NY, USA

    Sangtae Ahn

  5. GE Global Research, München, Germany

    Florian Wiesinger

  6. GE Healthcare, Waukesha, WI, USA

    M. Mehdi Khalighi & Gaspar Delso

  7. Department of Radiology, Molecular Imaging Program at Stanford, Stanford University, Stanford, CA, USA

    Craig S. Levin

  8. Department of Radiology, Division of Nuclear Medicine and Molecular Imaging, Stanford University, Stanford, CA, USA

    Andrei H. Iagaru

  9. Department of Radiology, Neuroradiology, Stanford University, Stanford, CA, USA

    Greg Zaharchuk

  10. Department of Neuroradiology, University Hospital Zurich, Zurich, Switzerland

    Martin Huellner

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  1. Edwin E. G. W. ter Voert
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Corresponding author

Correspondence to Edwin E. G. W. ter Voert.

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Funding

This study received funding from GE. Part of the study was carried out in the context of a GE-sponsored clinical trial to obtain CE marking and FDA approval of the TOF-PET/MR prototype.

Conflicts of Interest

The authors declare relationships with the following companies: P.V.-H. received IIS grants from Bayer Healthcare, Siemens Healthcare and Roche Pharmaceuticals, and speaker’s fees from GE Healthcare; G.Z. received research support and speaker’s fees from GE Healthcare; A.H.I. received research support and speaker’s fees from GE Healthcare; C.S.L. received research sponsorship from Siemens Healthcare, Philips Healthcare, and GE Healthcare; S.A. and F.W. are employees of GE Global Research; M.M.K. and G.D. are employees of GE Healthcare.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the principles of the 1964 Declaration of Helsinki and its later amendments or comparable ethical standards.

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ter Voert, E.E.G.W., Veit-Haibach, P., Ahn, S. et al. Clinical evaluation of TOF versus non-TOF on PET artifacts in simultaneous PET/MR: a dual centre experience. Eur J Nucl Med Mol Imaging 44, 1223–1233 (2017). https://doi.org/10.1007/s00259-017-3619-2

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