Skip to main content
Springer Nature Link
Log in

Simultaneous multislice diffusion-weighted imaging in whole-body positron emission tomography/magnetic resonance imaging for multiparametric examination in oncological patients

  • Magnetic Resonance
  • Published:
European Radiology Aims and scope Submit manuscript

Abstract

Objectives

The aim of this study was to compare the diagnostic performance of simultaneous multislice diffusion-weighted imaging (DWI-SMS) with that of standard DWI (DWI-STD) in whole-body 3-T PET/MRI examination protocols in oncological patients.

Methods

In a phantom study, we evaluated the apparent diffusion coefficients (ADC) from the two techniques. In ten volunteers, we assessed ADC values in different organs. In 20 oncological patients, we evaluated subjective image quality (Likert scale, 5 indicating excellent) and artefacts in different body regions. We also rated the conspicuity and acquired the ADC values of PET-positive tumorous lesions.

Results

The scan time for the whole-body DWI-SMS examinations was 40% shorter than the scan time for the DWI-STD examinations (84 s vs. 140 s per table position). The phantom and volunteer studies showed lower ADC values from DWI-SMS in the liver and muscle (psoas muscle 1.4 vs. 1.3). In patients, DWI-SMS provided poorer subjective image quality in the thoracoabdominal region (3.0 vs. 3.8, p = 0.02) and overall more artefacts (138 vs. 105). No significant differences regarding conspicuity and ADC values of lesions were found.

Conclusions

DWI-SMS seems to provide reliable conspicuity and ADC values of tumorous lesions similar to those provided by DWI-STD. Therefore, although providing poorer image quality in certain regions, DWI-SMS can clearly reduce PET/MRI scan times in oncological patients.

Key points

• DWI-SMS can reduce PET/MRI scan times in oncological patients.

• DWI-SMS provides reliable ADC values and good lesion conspicuity similar to those provided by DWI-STD.

• DWI-SMS may provide poorer image quality in regions with low signal.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Explore related subjects

Discover the latest articles and news from researchers in related subjects, suggested using machine learning.

Abbreviations

SMS:

Simultaneous multi-slice

STD:

Standard

HASTE:

Half Fourier acquisition single shot turbo spin echo

PSMA:

Prostate-specific membrane antigen

SD:

Standard deviation

CI:

Confidence interval

TR:

Repetition time

References

  1. Padhani AR, Koh D-M, Collins DJ (2011) Whole-body diffusion-weighted MR imaging in cancer: current status and research directions. Radiology 261:700–718

    Article  PubMed  Google Scholar 

  2. Holzapfel K, Reiser-Erkan C, Fingerle AA et al (2011) Comparison of diffusion-weighted MR imaging and multidetector-row CT in the detection of liver metastases in patients operated for pancreatic cancer. Abdom Imaging 36:179–184

    Article  PubMed  Google Scholar 

  3. Moffat BA, Chenevert TL, Lawrence TS et al (2005) Functional diffusion map: a noninvasive MRI biomarker for early stratification of clinical brain tumor response. Proc Natl Acad Sci U S A 102:5524–5529

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  4. Padhani AR, Koh DM (2011) Diffusion MR imaging for monitoring of treatment response. Magn Reson Imaging Clin N Am 19:181–209

    Article  PubMed  Google Scholar 

  5. Moseley ME, Cohen Y, Mintorovitch J et al (1990) Early detection of regional cerebral ischemia in cats: comparison of diffusion- and T2-weighted MRI and spectroscopy. Magn Reson Med 14:330–346

    Article  PubMed  CAS  Google Scholar 

  6. Yoshikawa T, Kawamitsu H, Mitchell DG et al (2006) ADC measurement of abdominal organs and lesions using parallel imaging technique. AJR Am J Roentgenol 187:1521–1530

    Article  PubMed  Google Scholar 

  7. Ichikawa T, Haradome H, Hachiya J, Nitatori T, Araki T (1998) Diffusion-weighted MR imaging with a single-shot echoplanar sequence: detection and characterization of focal hepatic lesions. AJR Am J Roentgenol 170:397–402

    Article  PubMed  CAS  Google Scholar 

  8. Takahara T, Imai Y, Yamashita T, Yasuda S, Nasu S, Van Cauteren M (2004) Diffusion weighted whole body imaging with background body signal suppression (DWIBS): technical improvement using free breathing, STIR and high resolution 3D display. Radiat Med 22:275–282

    PubMed  Google Scholar 

  9. Müller S (1988) Multifrequency selective rf pulses for multislice MR imaging. Magn Reson Med 6:364–371

  10. Souza SP, Szumowski J, Dumoulin CL et al (1988) SIMA: simultaneous multislice acquisition of MR images by Hadamard-encoded excitation. J Comput Assist Tomogr 12:1026–1030

  11. Moeller S, Yacoub E, Olman CA et al (2010) Multiband multislice GE-EPI at 7 tesla, with 16-fold acceleration using partial parallel imaging with application to high spatial and temporal whole-brain fMRI. Magn Reson Med 63:1144–1153

    Article  PubMed  PubMed Central  Google Scholar 

  12. Breuer FA, Blaimer M, Heidemann RM et al (2005) Controlled aliasing in parallel imaging results in higher acceleration (CAIPIRINHA) for multi-slice imaging. Magn Reson Med. 53:684–691

  13. Xu J, Moeller S, Auerbach EJ et al (2013) Evaluation of slice accelerations using multiband echo planar imaging at 3 T. Neuroimage 83:991–1001

    Article  PubMed  Google Scholar 

  14. Auerbach EJ, Xu J, Yacoub E, Moeller S, Ugurbil K (2013) Multiband accelerated spin-echo echo planar imaging with reduced peak RF power using time-shifted RF pulses. Magn Reson Med 69:1261–1267

    Article  PubMed  PubMed Central  Google Scholar 

  15. Setsompop K, Cohen-Adad J, Gagoski BA et al (2012) Improving diffusion MRI using simultaneous multi-slice echo planar imaging. Neuroimage 63:569–580

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  16. Taouli B, Beer AJ, Chenevert T et al (2016) Diffusion-weighted imaging outside the brain: Consensus statement from an ISMRM-sponsored workshop. J Magn Reson Imaging 44:521–540

  17. Kwee TC, Takahara T, Ochiai R et al (2010) Complementary roles of whole-body diffusion-weighted MRI and 18F-FDG PET: the state of the art and potential applications. J Nucl Med 51:1549–1558

    Article  PubMed  Google Scholar 

  18. Mayerhoefer ME, Karanikas G, Kletter K et al (2014) Evaluation of diffusion-weighted MRI for pretherapeutic assessment and staging of lymphoma: results of a prospective study in 140 patients. Clin Cancer Res 20:2984–2993

    Article  PubMed  Google Scholar 

  19. Preda L, Conte G, Bonello L et al (2016) Combining standardized uptake value of FDG-PET and apparent diffusion coefficient of DW-MRI improves risk stratification in head and neck squamous cell carcinoma. Eur Radiol 26:4432–4441

    Article  PubMed  Google Scholar 

  20. Delso G, Furst S, Jakoby B et al (2011) Performance measurements of the Siemens mMR integrated whole-body PET/MR scanner. J Nucl Med 52:1914–1922

    Article  PubMed  Google Scholar 

  21. Brendle CB, Schmidt H, Fleischer S, Braeuning UH, Pfannenberg CA, Schwenzer NF (2013) Simultaneously acquired MR/PET images compared with sequential MR/PET and PET/CT: alignment quality. Radiology 268:190–199

    Article  PubMed  Google Scholar 

  22. Kustner T, Wurslin C, Schwartz M et al (2017) Self-navigated 4D cartesian imaging of periodic motion in the body trunk using partial k-space compressed sensing. Magn Reson Med 78:632–644

    Article  PubMed  Google Scholar 

  23. Fayad H, Schmidt H, Kustner T, Visvikis D (2017) 4-Dimensional MRI and attenuation map generation in PET/MRI with 4-dimensional PET-derived deformation matrices: study of feasibility for lung cancer applications. J Nucl Med 58:833–839

    Article  PubMed  Google Scholar 

  24. Dikaios N, Izquierdo-Garcia D, Graves MJ, Mani V, Fayad ZA, Fryer TD (2012) MRI-based motion correction of thoracic PET: initial comparison of acquisition protocols and correction strategies suitable for simultaneous PET/MRI systems. Eur Radiol 22:439–446

    Article  PubMed  Google Scholar 

  25. Guckel B, Gatidis S, Enck P et al (2015) Patient comfort during positron emission tomography/magnetic resonance and positron emission tomography/computed tomography examinations: subjective assessments with visual analog scales. Invest Radiol 50:726–732

    Article  PubMed  Google Scholar 

  26. Aghighi M, Pisani LJ, Sun Z et al (2016) Speeding up PET/MR for cancer staging of children and young adults. Eur Radiol 26:4239–4248

    Article  PubMed  PubMed Central  Google Scholar 

  27. Giavarina D (2015) Understanding Bland Altman analysis. Biochem Med (Zagreb) 25:141–151

    Article  Google Scholar 

  28. Landis JR, Koch GG (1977) The measurement of observer agreement for categorical data. Biometrics 33:159–174

    Article  PubMed  CAS  Google Scholar 

  29. Fleiss JL (1999) Reliability of Measurement. The Design and Analysis of Clinical Experiments. John Wiley & Sons, Hoboken, pp 1–32

    Book  Google Scholar 

  30. Kenkel D, Wurnig MC, Filli L et al (2016) Whole-body diffusion imaging applying simultaneous multi-slice excitation. Rofo 188:381–388

    Article  PubMed  CAS  Google Scholar 

  31. Taron J, Martirosian P, Erb M et al (2016) Simultaneous multislice diffusion-weighted MRI of the liver: analysis of different breathing schemes in comparison to standard sequences. J Magn Reson Imaging 44:865–879

    Article  PubMed  Google Scholar 

  32. Taron J, Martirosian P, Schwenzer NF et al (2016) Scan time minimization in hepatic diffusion-weighted imaging: evaluation of the simultaneous multislice acceleration technique with different acceleration factors and gradient preparation schemes. MAGMA 29:739–749

    Article  PubMed  Google Scholar 

  33. Padhani AR, Liu G, Mu-Koh D et al (2009) Diffusion-weighted magnetic resonance imaging as a cancer biomarker: consensus and recommendations. Neoplasia 11:102–125

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  34. Kenkel D, von Spiczak J, Wurnig MC et al (2016) Whole-body diffusion tensor imaging: a feasibility study. J Comput Assist Tomogr 40:183–188

    Article  PubMed  Google Scholar 

  35. Rosenkrantz AB, Geppert C, Kiritsy M, Feiweier T, Mossa DJ, Chandarana H (2015) Diffusion-weighted imaging of the liver: comparison of image quality between monopolar and bipolar acquisition schemes at 3T. Abdom Imaging 40:289–298

    Article  PubMed  Google Scholar 

  36. Filli L, Wurnig M, Nanz D, Luechinger R, Kenkel D, Boss A (2014) Whole-body diffusion kurtosis imaging: initial experience on non-Gaussian diffusion in various organs. Invest Radiol 49:773–778

    Article  PubMed  Google Scholar 

  37. Le Bihan D, Poupon C, Amadon A, Lethimonnier F (2006) Artifacts and pitfalls in diffusion MRI. J Magn Reson Imaging 24:478–488

    Article  PubMed  Google Scholar 

  38. Seith F, Gatidis S, Schmidt H et al (2016) Comparison of positron emission tomography quantification using magnetic resonance- and computed tomography-based attenuation correction in physiological tissues and lesions: a whole-body positron emission tomography/magnetic resonance study in 66 patients. Invest Radiol 51:66–71

    Article  PubMed  Google Scholar 

  39. Feinberg DA, Moeller S, Smith SM et al (2010) Multiplexed echo planar imaging for sub-second whole brain fMRI and fast diffusion imaging. PLoS One 5:e15710

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  40. Weller A, Papoutsaki MV, Waterton JC et al (2017) Diffusion-weighted (DW) MRI in lung cancers: ADC test-retest repeatability. Eur Radiol. https://doi.org/10.1007/s00330-017-4828-6

Download references

Acknowledgements

The authors thank the University of Minnesota Center for Magnetic Resonance Research for providing continuous support regarding the SMS sequence. The authors gratefully acknowledge the support of Dr. Christian Wuerslin, Stanford, Radiological Sciences Laboratory, in kindly sharing the MATLAB postprocessing software. The authors thank Holger Schmidt, PhD, Siemens Healthineers GmbH, for kindly supporting the revision of the manuscript.

Author information

Authors and Affiliations

  1. Diagnostic and Interventional Radiology, University Department of Radiology, University Hospital of Tuebingen, Hoppe-Seyler-Str. 3, 72076, Tuebingen, Germany

    Jana Taron, Christina Schraml, Christina Pfannenberg, Konstantin Nikolaou & Ferdinand Seith

  2. Section on Experimental Radiology, Diagnostic and Interventional Radiology, University Department of Radiology, University Hospital of Tuebingen, Hoppe-Seyler-Str. 3, 72076, Tuebingen, Germany

    Nina Schwenzer & Petros Martirosian

  3. Nuclear Medicine and Clinical Molecular Imaging, Department of Radiology, Eberhard Karls University, Otfried-Mueller-Str. 14, 72076, Tuebingen, Germany

    Matthias Reimold

Authors
  1. Jana Taron
    View author publications

    You can also search for this author inPubMed Google Scholar

  2. Christina Schraml
    View author publications

    You can also search for this author inPubMed Google Scholar

  3. Christina Pfannenberg
    View author publications

    You can also search for this author inPubMed Google Scholar

  4. Matthias Reimold
    View author publications

    You can also search for this author inPubMed Google Scholar

  5. Nina Schwenzer
    View author publications

    You can also search for this author inPubMed Google Scholar

  6. Konstantin Nikolaou
    View author publications

    You can also search for this author inPubMed Google Scholar

  7. Petros Martirosian
    View author publications

    You can also search for this author inPubMed Google Scholar

  8. Ferdinand Seith
    View author publications

    You can also search for this author inPubMed Google Scholar

Corresponding author

Correspondence to Petros Martirosian.

Ethics declarations

Guarantor

The scientific guarantor of this publication is Petros Martirosian.

Conflict of interest

The authors of this manuscript declare no relationships with any companies whose products or services may be related to the subject matter of the article.

Funding

The authors state that this work did not receive any funding.

Statistics and biometry

No complex statistical methods were necessary for this paper.

Ethical approval

Institutional Review Board approval was obtained.

Informed consent

Written informed consent was obtained from all patients.

Methodology

• prospective

• experimental

• performed at one institution

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Taron, J., Schraml, C., Pfannenberg, C. et al. Simultaneous multislice diffusion-weighted imaging in whole-body positron emission tomography/magnetic resonance imaging for multiparametric examination in oncological patients. Eur Radiol 28, 3372–3383 (2018). https://doi.org/10.1007/s00330-017-5216-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00330-017-5216-y

Keywords