Abstract
Objective
To compare standard (STD-DWI) single-shot echo-planar imaging DWI and simultaneous multislice (SMS) DWI during whole-body positron emission tomography (PET)/MRI regarding acquisition time, image quality, and lesion detection.
Methods
Eighty-three adults (47 females, 57%), median age of 64 years (IQR 52–71), were prospectively enrolled from August 2018 to March 2020. Inclusion criteria were (a) abdominal or pelvic tumors and (b) PET/MRI referral from a clinician. Patients were excluded if whole-body acquisition of STD-DWI and SMS-DWI sequences was not completed. The evaluated sequences were axial STD-DWI at b-values 50–400–800 s/mm2 and the apparent diffusion coefficient (ADC), and axial SMS-DWI at b-values 50–300–800 s/mm2 and ADC, acquired with a 3-T PET/MRI scanner. Three radiologists rated each sequence’s quality on a five-point scale. Lesion detection was quantified using the anatomic MRI sequences and PET as the reference standard. Regression models were constructed to quantify the association between all imaging outcomes/scores and sequence type.
Results
The median whole-body STD-DWI acquisition time was 14.8 min (IQR 14.1–16.0) versus 7.0 min (IQR 6.7–7.2) for whole-body SMS-DWI, p < 0.001. SMS-DWI image quality scores were higher than STD-DWI in the abdomen (OR 5.31, 95% CI 2.76–10.22, p < 0.001), but lower in the cervicothoracic junction (OR 0.21, 95% CI 0.10–0.43, p < 0.001). There was no significant difference in the chest, mediastinum, pelvis, and rectum. STD-DWI detected 276/352 (78%) lesions while SMS-DWI located 296/352 (84%, OR 1.46, 95% CI 1.02–2.07, p = 0.038).
Conclusions
In cancer staging and restaging, SMS-DWI abbreviates acquisition while maintaining or improving the diagnostic yield in most anatomic regions.
Key Points
• Simultaneous multislice diffusion-weighted imaging enables faster whole-body image acquisition.
• Simultaneous multislice diffusion-weighted imaging maintains or improves image quality when compared to single-shot echo-planar diffusion-weighted imaging in most anatomical regions.
• Simultaneous multislice diffusion-weighted imaging leads to superior lesion detection.
Similar content being viewed by others
Abbreviations
- ADC:
-
Apparent diffusion coefficient
- CI:
-
Confidence interval
- DWI:
-
Diffusion-weighted imaging
- IQR:
-
Interquartile range
- OR:
-
Odds ratio
- PET:
-
Positron emission tomography
- SMS:
-
Simultaneous multislice
- STD:
-
Standard
References
Taouli B, Koh D-M (2010) Diffusion-weighted MR imaging of the liver. Radiology 254:47–66
Karatzas I, Shreve SE (1998) Brownian motion. In: Karatzas I, Shreve SE (eds) Brownian motion and stochastic calculus. Springer New York, New York, NY, pp 47–127
Manenti G, Squillaci E, Di Roma M et al (2006) In vivo measurement of the apparent diffusion coefficient in normal and malignant prostatic tissue using thin-slice echo-planar imaging. Radiol Med 111:1124–1133
Hagmann P, Jonasson L, Maeder P et al (2006) Understanding diffusion MR imaging techniques: from scalar diffusion-weighted imaging to diffusion tensor imaging and beyond. Radiographics 26(Suppl 1):S205–S223
Koh D-M, Collins DJ (2007) Diffusion-weighted MRI in the body: applications and challenges in oncology. AJR Am J Roentgenol 188:1622–1635
Taouli B, Vilgrain V, Dumont E et al (2003) Evaluation of liver diffusion isotropy and characterization of focal hepatic lesions with two single-shot echo-planar MR imaging sequences: prospective study in 66 patients. Radiology 226:71–78
Chan JH, Tsui EY, Luk SH et al (2001) Diffusion-weighted MR imaging of the liver: distinguishing hepatic abscess from cystic or necrotic tumor. Abdom Imaging 26:161–165
Cova M, Squillaci E, Stacul F et al (2004) Diffusion-weighted MRI in the evaluation of renal lesions: preliminary results. Br J Radiol 77:851–857
Isebaert S, Van den Bergh L, Haustermans K et al (2013) Multiparametric MRI for prostate cancer localization in correlation to whole-mount histopathology. J Magn Reson Imaging 37:1392–1401
Wei C, Tan J, Xu L et al (2015) Differential diagnosis between hepatic metastases and benign focal lesions using DWI with parallel acquisition technique: a meta-analysis. Tumour Biol 36:983–990
Setsompop K, Cohen-Adad J, Gagoski BA et al (2012) Improving diffusion MRI using simultaneous multi-slice echo planar imaging. Neuroimage 63:569–580
Obele CC, Glielmi C, Ream J et al (2015) Simultaneous multislice accelerated free-breathing diffusion-weighted imaging of the liver at 3 T. Abdom Imaging 40:2323–2330
Runge VM, Richter JK, Heverhagen JT (2017) Speed in clinical magnetic resonance. Invest Radiol 52:1–17
Lee EYP, An H, Tse KY, Khong P-L (2020) Molecular imaging of peritoneal carcinomatosis in ovarian carcinoma. AJR Am J Roentgenol 215:305–312
Cianci R, Delli Pizzi A, Patriarca G et al (2020) Magnetic resonance assessment of peritoneal carcinomatosis: Is there a true benefit from diffusion-weighted imaging? Curr Probl Diagn Radiol 49:392–397
Bruegel M, Gaa J, Waldt S et al (2008) Diagnosis of hepatic metastasis: comparison of respiration-triggered diffusion-weighted echo-planar MRI and five t2-weighted turbo spin-echo sequences. AJR Am J Roentgenol 191:1421–1429
Hong SB, Choi SH, Kim KW et al (2019) Diagnostic performance of [18F]FDG-PET/MRI for liver metastasis in patients with primary malignancy: a systematic review and meta-analysis. Eur Radiol 29:3553–3563
Low RN, Sebrechts CP, Barone RM, Muller W (2009) Diffusion-weighted MRI of peritoneal tumors: comparison with conventional MRI and surgical and histopathologic findings--a feasibility study. AJR Am J Roentgenol 193:461–470
Furtado FS, Wu MZ, Esfahani SA et al (2022) Positron emission tomography/magnetic resonance imaging versus the standard of care imaging in the diagnosis of peritoneal carcinomatosis. Ann Surg. https://doi.org/10.1097/SLA.0000000000005418
Chen B-B, Tien Y-W, Chang M-C et al (2018) Multiparametric PET/MR imaging biomarkers are associated with overall survival in patients with pancreatic cancer. Eur J Nucl Med Mol Imaging 45:1205–1217
Mulé S, Reizine E, Blanc-Durand P et al (2020) Whole-body functional MRI and PET/MRI in multiple myeloma. Cancers 12. https://doi.org/10.3390/cancers12113155
Mayerhoefer ME, Archibald SJ, Messiou C et al (2020) MRI and PET/MRI in hematologic malignancies. J Magn Reson Imaging 51:1325–1335
Catalano OA, Daye D, Signore A et al (2017) Staging performance of whole-body DWI, PET/CT and PET/MRI in invasive ductal carcinoma of the breast. Int J Oncol 51:281–288
Becker M, Varoquaux AD, Combescure C et al (2018) Local recurrence of squamous cell carcinoma of the head and neck after radio(chemo)therapy: diagnostic performance of FDG-PET/MRI with diffusion-weighted sequences. Eur Radiol 28:651–663
Seifert R, Kersting D, Rischpler C et al (2022) Clinical use of PET/MR in oncology: an update. Semin Nucl Med 52:356–364
Catalano OA, Horn GL, Signore A et al (2017) PET/MR in invasive ductal breast cancer: correlation between imaging markers and histological phenotype. Br J Cancer 116:893–902
Incoronato M, Grimaldi AM, Mirabelli P et al (2019) Circulating miRNAs in untreated breast cancer: an exploratory multimodality morpho-functional study. Cancers (Basel) 11:876
Incoronato M, Grimaldi AM, Cavaliere C et al (2018) Relationship between functional imaging and immunohistochemical markers and prediction of breast cancer subtype: a PET/MRI study. Eur J Nucl Med Mol Imaging 45:1680–1693
Kirchner J, Grueneisen J, Martin O et al (2018) Local and whole-body staging in patients with primary breast cancer: a comparison of one-step to two-step staging utilizing 18F-FDG-PET/MRI. Eur J Nucl Med Mol Imaging 45:2328–2337
Domachevsky L, Bernstine H, Goldberg N et al (2020) Comparison between pelvic PSMA-PET/MR and whole-body PSMA-PET/CT for the initial evaluation of prostate cancer: a proof of concept study. Eur Radiol 30:328–336
Afshar-Oromieh A, Haberkorn U, Schlemmer HP et al (2014) Comparison of PET/CT and PET/MRI hybrid systems using a 68Ga-labelled PSMA ligand for the diagnosis of recurrent prostate cancer: initial experience. Eur J Nucl Med Mol Imaging 41:887–897
Lee MS, Cho JY, Kim SY et al (2017) Diagnostic value of integrated PET/MRI for detection and localization of prostate cancer: comparative study of multiparametric MRI and PET/CT. J Magn Reson Imaging 45:597–609
Galgano SJ, Calderone CE, Xie C et al (2021) Applications of PET/MRI in abdominopelvic oncology. Radiographics 41:1750–1765
Beiderwellen KJ, Poeppel TD, Hartung-Knemeyer V et al (2013) Simultaneous 68Ga-DOTATOC PET/MRI in patients with gastroenteropancreatic neuroendocrine tumors: initial results. Invest Radiol 48:273–279
Furtado FS, Ferrone CR, Lee SI et al (2021) Impact of PET/MRI in the treatment of pancreatic adenocarcinoma: a retrospective cohort study. Mol Imaging Biol 23:456–466
Panda A, Garg I, Truty MJ et al (2021) Borderline resectable and locally advanced pancreatic cancer: FDG PET/MRI and CT tumor metrics for assessment of pathologic response to neoadjuvant therapy and prediction of survival. AJR Am J Roentgenol 217:730–740
Ferrone C, Goyal L, Qadan M et al (2020) Management implications of fluorodeoxyglucose positron emission tomography/magnetic resonance in untreated intrahepatic cholangiocarcinoma. Eur J Nucl Med Mol Imaging 47:1871–1884
Zhang C, O’Shea A, Parente CA et al (2021) Evaluation of the diagnostic performance of positron emission tomography/magnetic resonance for the diagnosis of liver metastases. Invest Radiol. https://doi.org/10.1097/RLI.0000000000000782
Crimì F, Spolverato G, Lacognata C et al (2020) 18F-FDG PET/MRI for rectal cancer TNM restaging after preoperative chemoradiotherapy: Initial experience. Dis Colon Rectum 63:310–318
Furtado FS, Suarez-Weiss KE, Vangel M et al (2021) Clinical impact of PET/MRI in oligometastatic colorectal cancer. Br J Cancer. https://doi.org/10.1038/s41416-021-01494-8
Queiroz MA, Ortega CD, Ferreira FR et al (2021) Diagnostic accuracy of FDG-PET/MRI versus pelvic MRI and thoracic and abdominal CT for detecting synchronous distant metastases in rectal cancer patients. Eur J Nucl Med Mol Imaging 48:186–195
Catalano OA, Lee SI, Parente C et al (2021) Improving staging of rectal cancer in the pelvis: the role of PET/MRI. Eur J Nucl Med Mol Imaging 48:1235–1245
Amorim BJ, Hong TS, Blaszkowsky LS et al (2019) Clinical impact of PET/MR in treated colorectal cancer patients. Eur J Nucl Med Mol Imaging 46:2260–2269
Esfahani SA, Torrado-Carvajal A, Amorim BJ et al (2022) PET/MRI and PET/CT radiomics in primary cervical cancer: a pilot study on the correlation of pelvic PET, MRI, and CT derived image features. Mol Imaging Biol 24:60–69
Yu Y, Zhang L, Sultana B et al (2022) Diagnostic value of integrated 18F-FDG PET/MRI for staging of endometrial carcinoma: comparison with PET/CT. BMC Cancer 22:947
Atkinson W, Catana C, Abramson JS et al (2016) Hybrid FDG-PET/MR compared to FDG-PET/CT in adult lymphoma patients. Abdom Radiol (NY) 41:1338–1348
Giraudo C, Raderer M, Karanikas G et al (2016) 18F-fluorodeoxyglucose positron emission tomography/magnetic resonance in lymphoma: comparison with 18F-fluorodeoxyglucose positron emission tomography/computed tomography and with the addition of magnetic resonance diffusion-weighted imaging. Invest Radiol 51:163–169
Afaq A, Fraioli F, Sidhu H et al (2017) Comparison of PET/MRI With PET/CT in the evaluation of disease status in lymphoma. Clin Nucl Med 42:e1–e7
Hamilton J, Franson D, Seiberlich N (2017) Recent advances in parallel imaging for MRI. Prog Nucl Magn Reson Spectrosc 101:71–95
Yutzy SR, Seiberlich N, Duerk JL, Griswold MA (2011) Improvements in multislice parallel imaging using radial CAIPIRINHA. Magn Reson Med 65:1630–1637
R Core Team (2021) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. Available from: https://www.R-project.org
EN 60601-2-33:2010/A2:2015 (2015) Medical Electrical Equipment—Part 2-33: particular requirements for the basic safety and essential performance of magnetic resonance equipment for medical diagnosis (IEC 60601-2-33:2010/A2:2015). IEC, Geneva
Dresen RC, De Vuysere S, De Keyzer F et al (2019) Whole-body diffusion-weighted MRI for operability assessment in patients with colorectal cancer and peritoneal metastases. Cancer Imaging 19:1
Larsen SKA, Sivesgaard K, Pedersen EM (2021) Multi-band whole-body diffusion-weighted imaging with inversion recovery fat saturation: effects of respiratory compensation. Eur J Radiol Open 8:100374
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
Taron J, Schraml C, Pfannenberg C et al (2018) 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
Saritas EU, Holdsworth SJ, Bammer R (2014) Susceptibility artifacts. In: Quantitative MRI of the spinal cord. Elsevier, pp 91–105
Fujima N, Carlota Andreu-Arasa V, Barest GD et al (2020) Magnetic resonance spectroscopy of the head and neck. Neuroimaging Clin N Am 30:283–293
Chen J, Hagiwara M, Givi B et al (2020) Assessment of metastatic lymph nodes in head and neck squamous cell carcinomas using simultaneous 18F-FDG-PET and MRI. Sci Rep 10:20764
Queiroz MA, Hüllner M, Kuhn F et al (2014) PET/MRI and PET/CT in follow-up of head and neck cancer patients. Eur J Nucl Med Mol Imaging. https://doi.org/10.1007/s00259-014-2707-9
Queiroz MA, Huellner MW (2015) PET/MR in cancers of the head and neck. Semin Nucl Med 45:248–265
Su T, Chen Y, Zhang Z et al (2020) Optimization of simultaneous multislice, readout-segmented echo planar imaging for accelerated diffusion-weighted imaging of the head and neck: A preliminary study. Acad Radiol 27:e245–e253
Jiang W, Yang F, Wang K (2022) Individualized and accurate SAR characterization method based on equivalent circuit model for MRI system. Magn Reson Med 87:2997–3010
Yu J-S, Kim JH, Chung J-J, Kim KW (2009) Added value of diffusion-weighted imaging in the MRI assessment of perilesional tumor recurrence after chemoembolization of hepatocellular carcinomas. J Magn Reson Imaging 30:153–160
Seith F, Schraml C, Reischl G et al (2018) Fast non-enhanced abdominal examination protocols in PET/MRI for patients with neuroendocrine tumors (NET): comparison to multiphase contrast-enhanced PET/CT. Radiol Med 123:860–870
Etchebehere ECS de C, de Oliveira Santos A, Gumz B, et al (2014) 68Ga-DOTATATE PET/CT, 99mTc-HYNIC-octreotide SPECT/CT, and whole-body MR imaging in detection of neuroendocrine tumors: a prospective trial. J Nucl Med 55:1598–1604
Xu S, Pan Y, Zhou J et al (2022) Integrated PET/MRI with 68Ga-DOTATATE and 18F-FDG in pheochromocytomas and paragangliomas: an initial study. Clin Nucl Med 47:299–304
Farchione A, Rufini V, Brizi MG et al (2016) Evaluation of the added value of diffusion-weighted imaging to conventional magnetic resonance imaging in pancreatic neuroendocrine tumors and comparison with 68Ga-DOTANOC positron emission tomography/computed tomography. Pancreas 45:345–354
Çelebi F, Yaghouti K, Cindil E et al (2021) The Role of 18F-FDG PET/MRI in the Assessment of Primary Intrahepatic Neoplasms. Acad Radiol 28:189–198
Jiang L, Tan H, Panje CM et al (2016) Role of 18F-FDG PET/CT imaging in intrahepatic cholangiocarcinoma. Clin Nucl Med 41:1–7
Fritscher-Ravens A, Bohuslavizki KH, Broering DC et al (2001) FDG PET in the diagnosis of hilar cholangiocarcinoma. Nucl Med Commun 22:1277–1285
Spijkers S, Littooij AS, Kwee TC et al (2021) Whole-body MRI versus an FDG-PET/CT-based reference standard for staging of paediatric Hodgkin lymphoma: a prospective multicentre study. Eur Radiol 31:1494–1504
Goerres GW, Schmid DT, Bandhauer F et al (2004) Positron emission tomography in the early follow-up of advanced head and neck cancer. Arch Otolaryngol Head Neck Surg 130:105
Dose-Schwarz J, Tiling R, Avril-Sassen S et al (2010) Assessment of residual tumour by FDG-PET: conventional imaging and clinical examination following primary chemotherapy of large and locally advanced breast cancer. Br J Cancer 102:35–41
Acknowledgements
We would like to thank Robin Striar for coordinating this research study.
Funding
The authors state that this work has not received any funding.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Guarantor
The scientific guarantor of this publication is O.A.C.
Conflict of interest
The authors T.V., T.B., and R. S. declare relationships with Siemens GmbH.
Statistics and biometry
N.D.M. has significant statistical expertise.
Informed consent
Written informed consent was obtained from all subjects (patients) in this study.
Ethical approval
Institutional review board approval was obtained.
Methodology
• prospective
• experimental
• performed at one institution
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
ESM 1
(DOCX 31 kb)
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Furtado, F.S., Mercaldo, N.D., Vahle, T. et al. Simultaneous multislice diffusion-weighted imaging versus standard diffusion-weighted imaging in whole-body PET/MRI. Eur Radiol 33, 2536–2547 (2023). https://doi.org/10.1007/s00330-022-09275-4
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00330-022-09275-4