Hybrid PET/MRI in non-small cell lung cancer (NSCLC) and lung nodules—a literature review

Abstract

Background

The use of hybrid PET/MRI for clinical staging is growing in several cancer forms and, consequently, PET/MRI has also gained interest in the assessment of non-small cell lung cancer (NSCLC) and lung lesions. However, lung evaluation with PET/MRI is associated with challenges related to technical issues and diagnostic image quality. We, therefore, investigated the published literature on PET/MRI for clinical staging in NSCLC or lung nodule detection specifically addressing diagnostic accuracy and technical issues.

Methods

The data originates from a systematic search performed in PubMed/MEDLINE, Embase, and Cochrane Library on hybrid PET/MRI in patients with cancer for a scoping review published earlier (https://doi.org/10.1007/s00259-019-04402-8). Studies in English and German evaluating the diagnostic performance of hybrid PET/MRI for NSCLC or lung nodule detection in cancer patients were selected. Data reported in peer-reviewed journals without restrictions to year of publication were included.

Results

A total of 3138 publications were identified from which 116 published 2012–2018 were included. Of these, nine studies addressed PET/MRI in NSCLC (4) or lung nodule detection (5). Overall, PET/MRI did not provide advantages in preoperative T- and N-staging in NSCLC compared to PET/CT. The data on M-staging were too few for conclusions to be drawn. The lung nodule detection rate of PET/MRI was comparable to that of PET/CT for FDG-avid nodules larger than 10 mm, but the sensitivity of PET/MRI for detection of non-FDG-avid nodules smaller than 5 mm was low.

Conclusion

PET/MRI did not provide advantages in T- and N-staging of NSCLC compared to PET/CT. PET/MRI had a comparable sensitivity for detection of FDG-avid lung nodules and nodules over 10 mm, but PET/CT yielded a higher detection rate in non FDG-avid lung nodules under 5 mm. With PET/MRI, the overall detection rate for lung nodules in various cancer types remains inferior to that of PET/CT due to the lower diagnostic performance of MRI than CT in the lungs.

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References

  1. 1.

    Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A, et al. GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2018;2018. https://doi.org/10.3322/caac.21492.

  2. 2.

    Gavra M, Syed R, Fraioli F, Afaq A, Bomanji J. PET/MRI in the upper abdomen. Semin Nucl Med. 2015. https://doi.org/10.1053/j.semnuclmed.2015.03.00.

  3. 3.

    Catalano OA, Coutinho AM, Sahani DV, Vangel MG, Gee MS, Hahn PF, et al. Colorectal cancer staging: comparison of whole-body PET/CT and PET/MR. Abdom Radiol. 2017. https://doi.org/10.1053/j.semnuclmed.2015.03.002.

  4. 4.

    Lee DH, Lee JM. Whole-body PET/MRI for colorectal cancer staging: is it the way forward? J Magn Reson Imaging. 2017. https://doi.org/10.1002/jmri.25337.

  5. 5.

    de Barbosa F G, Queiroz MA, Nunes RF, Marin JFG, Buchpiguel CA, Cerri GG. Clinical perspectives of PSMA PET/MRI for prostate cancer. Clinics. 2018. https://doi.org/10.6061/clinics/2018/e586s

  6. 6.

    Milovanovic IS, Stjepanovic M, Mitrovic D. Distribution patterns of the metastases of the lung carcinoma in relation to histological type of the primary tumor: an autopsy study. Ann Thorac Med. 2017. https://doi.org/10.4103/atm.ATM_276_16.

  7. 7.

    Popper HH. Progression and metastasis of lung cancer. Cancer Metastasis Rev. 2016. https://doi.org/10.1007/s10555-016-96180.

  8. 8.

    Gould MK, Maclean CC, Kuschner WG, Rydzak CE, Owens DK. Accuracy of positron emission tomography for diagnosis of pulmonary nodules and mass lesions: a meta-analysis. J Am Med Assoc. 2001. https://doi.org/10.1001/jama.285.7.914.

  9. 9.

    Nomori H, Watanabe K, Ohtsuka T, Naruke T, Suemasu K, Uno K. Evaluation of F-18 fluorodeoxyglucose (FDG) PET scanning for pulmonary nodules less than 3 cm in diameter, with special reference to the CT images. Lung Cancer. 2004. https://doi.org/10.1016/j.lungcan.2004.01.009.

  10. 10.

    Wild JM, Marshall H, Bock M, Schad LR, Jakob PM, Puderbach M, et al. MRI of the lung (1/3): methods. Insights Imaging. 2012. https://doi.org/10.1007/s13244-012-0176-x.

  11. 11.

    Biederer J, Beer M, Hirsch W, Wild J, Fabel M, Puderbach M, et al. MRI of the lung (2/3). Why... when ... how? Insights Imaging. 2012; https://doi.org/10.1007/s13244-011-0146-8

  12. 12.

    Morsing A, Hildebrandt MG, Vilstrup MH, Wallenius SE, Gerke O, Petersen H, et al. Hybrid PET/MRI in major cancers: a scoping review. Eur. J. Nucl. Med. Mol. Imaging. Springer Berlin Heidelberg; 2019. p. 2138–51. https://doi.org/10.1007/s00259-019-04402-8

  13. 13.

    Schaarschmidt BM, Grueneisen J, Metzenmacher M, Gomez B, Gauler T, Roesel C, et al. Thoracic staging with18F-FDG PET/MR in non-small cell lung cancer – does it change therapeutic decisions in comparison to18F-FDG PET/CT? Eur Radiol. 2017. https://doi.org/10.1007/s00330-016-4397-0.

  14. 14.

    Lee SM, Goo JM, Park CM, Yoon SH, Paeng JC, Cheon GJ, et al. Preoperative staging of non-small cell lung cancer: prospective comparison of PET/MR and PET/CT. Eur Radiol. 2016. https://doi.org/10.1007/s00330-016-4255-0.

  15. 15.

    Fraioli F, Screaton NJ, Janes SM, Win T, Menezes L, Kayani I, et al. Non-small-cell lung cancer resectability: diagnostic value of PET/MR. Eur J Nucl Med Mol Imaging. 2015. https://doi.org/10.1007/s00259-014-2873-9.

  16. 16.

    Heusch P, Buchbender C, Kohler J, Nensa F, Gauler T, Gomez B, et al. Thoracic staging in lung cancer: prospective comparison of 18F-FDG PET/MR imaging and 18F-FDG PET/CT. J Nucl Med. 2014. https://doi.org/10.2967/jnumed.113.129825.

  17. 17.

    Sawicki LM, Grueneisen J, Buchbender C, Schaarschmidt BM, Gomez B, Ruhlmann V, et al. Comparative performance of 18F-FDG PET/MRI and 18F-FDG PET/CT in detection and characterization of pulmonary lesions in 121 oncologic patients. J Nucl Med. 2016. https://doi.org/10.2967/jnumed.115.167486.

  18. 18.

    Sawicki LM, Grueneisen J, Buchbender C, Schaarschmidt BM, Gomez B, Ruhlmann V, et al. Evaluation of the outcome of lung nodules missed on 18F-FDG PET/MRI compared with 18F-FDG PET/CT in patients with known malignancies. J Nucl Med. 2016. https://doi.org/10.2967/jnumed.115.162966.

  19. 19.

    Raad RA, Friedman KP, Heacock L, Ponzo F, Melsaether A, Chandarana H. Outcome of small lung nodules missed on hybrid PET/MRI in patients with primary malignancy. J Magn Reson Imaging. 2016. https://doi.org/10.1002/jmri.25005.

  20. 20.

    Rauscher I, Eiber M, Furst S, Souvatzoglou M, Nekolla SG, Ziegler SI, et al. PET/MR imaging in the detection and characterization of pulmonary lesions: technical and diagnostic evaluation in comparison to PET/CT. J Nucl Med. 2014. https://doi.org/10.2967/jnumed.113.129247.

  21. 21.

    Chandarana H, Heacock L, Rakheja R, DeMello LR, Bonavita J, Block TK, et al. Pulmonary nodules in patients with primary malignancy: comparison of hybrid PET/MR and PET/CT imaging. Radiology. 2013. https://doi.org/10.1148/radiol.13130620.

  22. 22.

    Kirchner J, Sawicki LM, Nensa F, Schaarschmidt BM, Reis H, Ingenwerth M, et al. Prospective comparison of 18F-FDG PET/MRI and 18F-FDG PET/CT for thoracic staging of non-small cell lung cancer. Eur J Nucl Med Mol Imaging. 2019. https://doi.org/10.1007/s00259-018-4109-x.

  23. 23.

    Martin O, Schaarschmidt BM, Kirchner J, Suntharalingam S, Grueneisen J, Demircioglu A, et al. PET/MRI versus PET/CT in whole-body staging: results from a unicenter observational study in 1003 subsequent examinations. J Nucl Med. 2019. https://doi.org/10.2967/jnumed.119.233940.

  24. 24.

    Mayerhoefer ME, Prosch H, Beer L, Tamandl D, Beyer T, Hoeller C, et al. PET/MRI versus PET/CT in oncology: a prospective single-center study of 330 examinations focusing on implications for patient management and cost considerations. Eur J Nucl Med Mol Imaging. 2020;47:51–60. https://doi.org/10.1007/s00259-019-04452-y.

    CAS  Article  PubMed  Google Scholar 

  25. 25.

    Brea TP, Raviña AR, Villamor JMC, Gómez AG, de Alegría AM, Valdèc)s L. Use of magnetic resonance imaging for N-staging in patients with non-small cell lung cancer. A systematic review. Arch Bronconeumol (English Ed. 2019;55:9–16. https://doi.org/10.1016/j.arbr.2018.03.013.

  26. 26.

    Catalano OA, Rosen BR, Sahani DV, Hahn PF, Guimaraes AR, Vangel MG, et al. Clinical impact of PET / MR imaging in patients with cancer initial experience in 134 patients. Radiology. 2013;269:857–69. https://doi.org/10.1148/radiol.13131306/-/DC1.

    Article  PubMed  Google Scholar 

  27. 27.

    Benjamin MS, Drucker EA, McLoud TC, Shepard JO. Small pulmonary nodules: detection at chest CT and outcome. Radiology. 2003. https://doi.org/10.1148/radiol.2262010556.

  28. 28.

    Delso G, Voert E Ter, Barbosa FDG, Veit-Haibach P. Pitfalls and limitations in simultaneous PET/MRI. Semin. Nucl. Med. 2015. https://doi.org/10.1053/j.semnuclmed.2015.04.002.

  29. 29.

    Biederer J, Hintze C, Fabel M. MRI of pulmonary nodules: technique and diagnostic value. Cancer Imaging. 2008. https://doi.org/10.1102/1470-73302008.0018.

  30. 30.

    Heye T, Ley S, Heussel CP, Dienemann H, Kauczor HU, Hosch W, et al. Detection and size of pulmonary lesions: how accurate is MRI? A prospective comparison of CT and MRI. Acta Radiol. 2012. https://doi.org/10.1258/ar.2011.110445.

  31. 31.

    Boada FE, Koesters T, Block KT, Chandarana H. Improved detection of small pulmonary nodules through simultaneous MR/PET imaging. Magn Reson Imaging Clin N Am. 2017. https://doi.org/10.1016/j.mric.2016.12.009.

  32. 32.

    Schleyer PJ, O’Doherty MJ, Barrington SF, Marsden PK. Retrospective data-driven respiratory gating for PET/CT. Phys Med Biol. 2009. https://doi.org/10.1088/0031-9155/54/7/005.

  33. 33.

    Dewes P, Frellesen C, Al-Butmeh F, Albrecht MH, Scholtz JE, Metzger SC, et al. Comparative evaluation of non-contrast CAIPIRINHA-VIBE 3T-MRI and multidetector CT for detection of pulmonary nodules: in vivo evaluation of diagnostic accuracy and image quality. Eur J Radiol Elsevier Ireland Ltd. 2016;85:193–8. https://doi.org/10.1016/j.ejrad.2015.11.020.

    Article  Google Scholar 

  34. 34.

    Ohno Y, Koyama H, Yoshikawa T, Kishida Y, Seki S, Takenaka D, et al. Standard-, reduced-, and no-dose thin-section radiologic examinations: comparison of capability for nodule detection and nodule type assessment in patients suspected of having pulmonary nodules. Radiology. 2017. https://doi.org/10.1148/radiol.2017161037.

  35. 35.

    Cha MJ, Park HJ, Paek MY, Stemmer A, Lee ES, Park S Bin, et al. Free-breathing ultrashort echo time lung magnetic resonance imaging using stack-of-spirals acquisition: a feasibility study in oncology patients. Magn Reson Imaging. 2018; https://doi.org/10.1016/j.mri.2018.05.002

  36. 36.

    Burris NS, Johnson KM, Larson PEZ, Hope MD, Nagle SK, Behr SC, et al. Detection of small pulmonary nodules with ultrashort echo time sequences in oncology patients by using a PET/MR system. Radiology. 2016. https://doi.org/10.1148/radiol.2015150489.

  37. 37.

    Bae K, Jeon KN, Hwang MJ, Lee JS, Ha JY, Ryu KH, et al. Comparison of lung imaging using three-dimensional ultrashort echo time and zero echo time sequences: preliminary study. Eur Radiol European Radiology. 2019;29:2253–62. https://doi.org/10.1007/s00330-018-5889-x.

    Article  PubMed  Google Scholar 

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Acknowledgments

Research librarian L. Østengaard, PhD, University Library of Southern Denmark and Head of Department, and Associate Professor J.S. Madsen, Biochemistry and Immunology, Institute of Regional Health Research, University of Southern Denmark are acknowledged for help with the literature search.

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Correspondence to Sara E. Dahlsgaard-Wallenius.

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Dahlsgaard-Wallenius, S.E., Hildebrandt, M.G., Johansen, A. et al. Hybrid PET/MRI in non-small cell lung cancer (NSCLC) and lung nodules—a literature review. Eur J Nucl Med Mol Imaging 48, 584–591 (2021). https://doi.org/10.1007/s00259-020-04955-z

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Keywords

  • PET/MRI
  • PET/CT
  • 18F-FDG
  • NSCLC
  • Lung lesions