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EJNMMI Research

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01-12-2020 | Magnetic Resonance Imaging | Original research

[¹⁸F]-Fluciclovine PET discrimination of recurrent intracranial metastatic disease from radiation necrosis

Authors: Ephraim E. Parent, Dhruv Patel, Jonathon A. Nye, Zhuo Li, Jeffrey J. Olson, David M. Schuster, Mark M. Goodman

Published in: EJNMMI Research | Issue 1/2020

Abstract

Background

Stereotactic radiosurgery (SRS) is often the primary treatment modality for patients with intracranial metastatic disease. Despite advances in magnetic resonance imaging, including use of perfusion and diffusion sequences and molecular imaging, distinguishing radiation necrosis from progressive tumor remains a diagnostic and clinical challenge. We investigated the sensitivity and specificity of ¹⁸F-fluciclovine PET to accurately distinguish radiation necrosis from recurrent intracranial metastatic disease in patients who had previously undergone SRS.

Methods

Fluciclovine PET imaging was performed in 8 patients with a total of 15 lesions that had previously undergone SRS and had subsequent MRI and clinical features suspicious for recurrent disease. The SUVmax of each lesion and the contralateral normal brain parenchyma were summated and evaluated at four different time points (5 min, 10 min, 30 min, and 55 min). Lesions were characterized as either recurrent disease (11 of 15 lesions) or radiation necrosis (4 of 15 lesions) and confirmed with histopathological correlation (7 lesions) or through serial MRI studies (8 lesions).

Results

Time activity curve analysis found statistically greater radiotracer accumulation for all lesions, including radiation necrosis, when compared to contralateral normal brain. While the mean and median SUV_max for recurrent disease were statistically greater than those of radiation necrosis at all time points, the difference was more significant at the earlier time points (p = 0.004 at 5 min–0.025 at 55 min). Using a SUV_max threshold of ≥ 1.3, fluciclovine PET demonstrated a 100% accuracy in distinguishing recurrent disease from radiation necrosis up to 30 min after injection and an accuracy of 87% (sensitivity = 0.91, specificity = 0.75) at the last time point of 55 min. However, tumor-to-background ratios (TBR_max) were not significantly different between recurrent disease and radiation necrosis at any time point due to variable levels of fluciclovine uptake in the background brain parenchyma.

Conclusions

Fluciclovine PET may play an important role in distinguishing active intracranial metastatic lesions from radiation necrosis in patients previously treated with SRS but needs to be validated in larger studies.

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Barnholtz-Sloan JS, Yu C, Sloan AE, Vengoechea J, Wang M, Dignam JJ, et al. A nomogram for individualized estimation of survival among patients with brain metastasis. Neuro Oncol. 2012;14:910–8. https://doi.org/10.1093/neuonc/nos087.CrossRefPubMedPubMedCentral

Ruzevick J, Kleinberg L, Rigamonti D. Imaging changes following stereotactic radiosurgery for metastatic intracranial tumors: differentiating pseudoprogression from tumor progression and its effect on clinical practice. Neurosurg Rev. 2014;37:193–201. https://doi.org/10.1007/s10143-013-0504-8.CrossRefPubMed

Chuang M-T, Liu Y-S, Tsai Y-S, Chen Y-C, Wang C-K. Differentiating radiation-induced necrosis from recurrent brain tumor using MR perfusion and spectroscopy: a meta-analysis. PLoS ONE. 2016;11:e0141438. https://doi.org/10.1371/journal.pone.0141438.CrossRefPubMedPubMedCentral

Galldiks N, Law I, Pope WB, Arbizu J, Langen K-J. The use of amino acid PET and conventional MRI for monitoring of brain tumor therapy. NeuroImage Clin. 2017;13:386–94.CrossRefPubMed

Zhuang H, Pourdehnad M, Lambright ES, Yamamoto AJ, Lanuti M, Li P, et al. Dual time point ¹⁸F-FDG PET imaging for differentiating malignant from inflammatory processes. J Nucl Med. 2001;42:1412–7.PubMed

Chao ST, Suh JH, Raja S, Lee S-Y, Barnett G. The sensitivity and specificity of FDG PET in distinguishing recurrent brain tumor from radionecrosis in patients treated with stereotactic radiosurgery. Int J Cancer. 2001;96:191–7. https://doi.org/10.1002/ijc.1016.CrossRefPubMed

Huang C, McConathy J. Radiolabeled amino acids for oncologic imaging. J Nucl Med. 2013;54:1007–10. https://doi.org/10.2967/jnumed.112.113100.CrossRefPubMed

Chaofeng H, Jonathan M. Fluorine-18 labeled amino acids for oncologic imaging with positron emission tomography. Curr Top Med Chem. 2013;13:871–91. https://doi.org/10.2174/1568026611313080002.CrossRef

McParland BJ, Wall A, Johansson S, Sørensen J. The clinical safety, biodistribution and internal radiation dosimetry of [¹⁸F]fluciclovine in healthy adult volunteers. Eur J Nucl Med Mol Imaging. 2013;40:1256–64. https://doi.org/10.1007/s00259-013-2403-1.CrossRefPubMed

10.

Nye JA, Schuster DM, Yu W, Camp VM, Goodman MM, Votaw JR. Biodistribution and radiation dosimetry of the synthetic nonmetabolized amino acid analogue anti-¹⁸F-FACBC in humans. J Nucl Med. 2007;48:1017–20. https://doi.org/10.2967/jnumed.107.040097.CrossRefPubMed

11.

Terakawa Y, Tsuyuguchi N, Iwai Y, Yamanaka K, Higashiyama S, Takami T, et al. Diagnostic accuracy of 11C-methionine PET for differentiation of recurrent brain tumors from radiation necrosis after radiotherapy. J Nucl Med. 2008;49:694–9. https://doi.org/10.2967/jnumed.107.048082.CrossRefPubMed

12.

Tsuyuguchi N, Sunada I, Iwai Y, Yamanaka K, Tanaka K, Takami T, et al. Methionine positron emission tomography of recurrent metastatic brain tumor and radiation necrosis after stereotactic radiosurgery: is a differential diagnosis possible? J Neurosurg. 2003;98:1056–64. https://doi.org/10.3171/jns.2003.98.5.1056.CrossRefPubMed

13.

Lizarraga KJ, Allen-Auerbach M, Czernin J, DeSalles AAF, Yong WH, Phelps ME, et al. ¹⁸F-FDOPA PET for differentiating recurrent or progressive brain metastatic tumors from late or delayed radiation injury after radiation treatment. J Nucl Med. 2014;55:30–6. https://doi.org/10.2967/jnumed.113.121418.CrossRefPubMed

14.

Parent EE, Schuster DM. Update on ¹⁸F-Fluciclovine PET for prostate cancer imaging. J Nucl Med. 2018;59:733–9. https://doi.org/10.2967/jnumed.117.204032.CrossRefPubMedPubMedCentral

15.

Parent EE, Benayoun M, Ibeanu I, Olson JJ, Hadjipanayis CG, Brat DJ, et al. [¹⁸F]Fluciclovine PET discrimination between high- and low-grade gliomas. EJNMMI Res. 2018;8:67. https://doi.org/10.1186/s13550-018-0415-3.CrossRefPubMedPubMedCentral

16.

Sasajima T, Ono T, Shimada N, Doi Y, Oka S, Kanagawa M, et al. Trans-1-amino-3–18F-fluorocyclobutanecarboxylic acid (anti-18F-FACBC) is a feasible alternative to 11C-methyl-L-methionine and magnetic resonance imaging for monitoring treatment response in gliomas. Nucl Med Biol. 2013;40:808–15. https://doi.org/10.1016/j.nucmedbio.2013.04.007.CrossRefPubMed

17.

Wakabayashi T, Iuchi T, Tsuyuguchi N, Nishikawa R, Arakawa Y, Sasayama T, et al. Diagnostic performance and safety of positron emission tomography using ¹⁸F-Fluciclovine in patients with clinically suspected high- or low-grade gliomas: a multicenter phase IIb trial. Asia Ocean J Nucl Med Biol. 2017;5:10–21. https://doi.org/10.22038/aojnmb.2016.7869.CrossRefPubMedPubMedCentral

18.

Kondo A, Ishii H, Aoki S, Suzuki M, Nagasawa H, Kubota K, et al. Phase IIa clinical study of [¹⁸F]fluciclovine: efficacy and safety of a new PET tracer for brain tumors. Ann Nucl Med. 2016;30:608–18. https://doi.org/10.1007/s12149-016-1102-y.CrossRefPubMed

19.

McConathy J, Voll RJ, Yu W, Crowe RJ, Goodman MM. Improved synthesis of anti-[¹⁸F]FACBC: improved preparation of labeling precursor and automated radiosynthesis. Appl Radiat Isot. 2003;58:657–66. https://doi.org/10.1016/s0969-8043(03)00029-0.CrossRefPubMed

20.

Miyatake S, Nonoguchi N, Furuse M, Yoritsune E, Miyata T, Kawabata S, et al. Pathophysiology, diagnosis, and treatment of radiation necrosis in the brain. Neurol Med Chir (Tokyo). 2015;55(Suppl 1):50–9.CrossRef

21.

Weller M, van den Bent M, Tonn JC, Stupp R, Preusser M, Cohen-Jonathan-Moyal E, et al. European Association for Neuro-Oncology (EANO) guideline on the diagnosis and treatment of adult astrocytic and oligodendroglial gliomas. Lancet Oncol. 2017;18:e315–29. https://doi.org/10.1016/S1470-2045(17)30194-8.CrossRefPubMed

22.

Kocher M, Soffietti R, Abacioglu U, Villa S, Fauchon F, Baumert BG, et al. Adjuvant whole-brain radiotherapy versus observation after radiosurgery or surgical resection of one to three cerebral metastases: results of the EORTC 22952–26001 study. J Clin Oncol. 2011;29:134–41. https://doi.org/10.1200/JCO.2010.30.1655.CrossRefPubMed

23.

Hygino da Cruz LC, Jr., Rodriguez I, Domingues RC, Gasparetto EL, Sorensen AG, . Pseudoprogression and pseudoresponse: imaging challenges in the assessment of posttreatment glioma. AJNR Am J Neuroradiol. 2011;32:1978–85. https://doi.org/10.3174/ajnr.A2397.CrossRefPubMedPubMedCentral

24.

Minniti G, Clarke E, Lanzetta G, Osti MF, Trasimeni G, Bozzao A, et al. Stereotactic radiosurgery for brain metastases: analysis of outcome and risk of brain radionecrosis. Radiat Oncol. 2011;6:48. https://doi.org/10.1186/1748-717X-6-48.CrossRefPubMedPubMedCentral

25.

Barajas RF Jr, Chang JS, Segal MR, Parsa AT, McDermott MW, Berger MS, et al. Differentiation of recurrent glioblastoma multiforme from radiation necrosis after external beam radiation therapy with dynamic susceptibility-weighted contrast-enhanced perfusion MR imaging. Radiology. 2009;253:486–96. https://doi.org/10.1148/radiol.2532090007.CrossRefPubMedPubMedCentral

26.

Bette S, Huber T, Gempt J, Boeckh-Behrens T, Wiestler B, Kehl V, et al. Local fractional anisotropy is reduced in areas with tumor recurrence in glioblastoma. Radiology. 2017;283:499–507. https://doi.org/10.1148/radiol.2016152832.CrossRefPubMed

27.

Li H, Deng L, Bai HX, Sun J, Cao Y, Tao Y, et al. Diagnostic accuracy of amino acid and FDG-PET in differentiating brain metastasis recurrence from radionecrosis after radiotherapy: a systematic review and meta-analysis. AJNR Am J Neuroradiol. 2018;39:280–8. https://doi.org/10.3174/ajnr.A5472.CrossRefPubMedPubMedCentral

28.

Tomura N, Kokubun M, Saginoya T, Mizuno Y, Kikuchi Y. Differentiation between treatment-induced necrosis and recurrent tumors in patients with metastatic brain tumors: comparison among ¹¹C-methionine-PET, FDG-PET, MR permeability imaging, and MRI-ADC-preliminary results. AJNR Am J Neuroradiol. 2017;38:1520–7. https://doi.org/10.3174/ajnr.A5252.CrossRefPubMedPubMedCentral

29.

Yomo S, Oguchi K. Prospective study of ¹¹C-methionine PET for distinguishing between recurrent brain metastases and radiation necrosis: limitations of diagnostic accuracy and long-term results of salvage treatment. BMC Cancer. 2017;17:713. https://doi.org/10.1186/s12885-017-3702-x.CrossRefPubMedPubMedCentral

30.

Lohmann P, Stoffels G, Ceccon G, Rapp M, Sabel M, Filss CP, et al. Radiation injury vs. recurrent brain metastasis: combining textural feature radiomics analysis and standard parameters may increase ¹⁸F-FET PET accuracy without dynamic scans. Eur Radiol. 2017;27:2916–27. https://doi.org/10.1007/s00330-016-4638-2.CrossRefPubMed

31.

Ceccon G, Lohmann P, Stoffels G, Judov N, Filss CP, Rapp M, et al. Dynamic O-(2–18F-fluoroethyl)-L-tyrosine positron emission tomography differentiates brain metastasis recurrence from radiation injury after radiotherapy. Neuro Oncol. 2017;19:281–8. https://doi.org/10.1093/neuonc/now149.CrossRefPubMed

32.

Ulaner GA, Goldman DA, Corben A, Lyashchenko SK, Gonen M, Lewis JS, et al. Prospective clinical trial of ¹⁸F-fluciclovine PET/CT for determining the response to neoadjuvant therapy in invasive ductal and invasive lobular breast cancers. J Nucl Med. 2017;58:1037–42. https://doi.org/10.2967/jnumed.116.183335.CrossRefPubMedPubMedCentral

33.

Schuster DM, Nye JA, Nieh PT, Votaw JR, Halkar RK, Issa MM, et al. Initial experience with the radiotracer anti-1-amino-3-[18F]Fluorocyclobutane-1-carboxylic acid (anti-[18F]FACBC) with PET in renal carcinoma. Mol Imaging Biol. 2009;11:434–8. https://doi.org/10.1007/s11307-009-0220-5.CrossRefPubMed

34.

Oka S, Okudaira H, Ono M, Schuster DM, Goodman MM, Kawai K, et al. Differences in transport mechanisms of trans-1-amino-3-[¹⁸F]fluorocyclobutanecarboxylic acid in inflammation, prostate cancer, and glioma cells: comparison with L-[methyl-¹¹C]methionine and 2-deoxy-2-[¹⁸F]fluoro-D-glucose. Mol Imaging Biol. 2014;16:322–9. https://doi.org/10.1007/s11307-013-0693-0.CrossRefPubMed

35.

Chernov MF, Ono Y, Abe K, Usukura M, Hayashi M, Izawa M, et al. Differentiation of tumor progression and radiation-induced effects after intracranial radiosurgery. Acta Neurochir Suppl. 2013;116:193–210. https://doi.org/10.1007/978-3-7091-1376-9_29.CrossRefPubMed

Title: [18F]-Fluciclovine PET discrimination of recurrent intracranial metastatic disease from radiation necrosis
Authors: Ephraim E. Parent
Dhruv Patel
Jonathon A. Nye
Zhuo Li
Jeffrey J. Olson
David M. Schuster
Mark M. Goodman
Publication date: 01-12-2020
Publisher: Springer Berlin Heidelberg
Keywords: Magnetic Resonance Imaging
Magnetic Resonance Imaging
Metastasis
Positron Emission Tomography
Published in: EJNMMI Research / Issue 1/2020
Electronic ISSN: 2191-219X
DOI: https://doi.org/10.1186/s13550-020-00739-6

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

[¹⁸F]-Fluciclovine PET discrimination of recurrent intracranial metastatic disease from radiation necrosis

Abstract

Background

Methods

Results

Conclusions

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Abstract

Background

Methods

Results

Conclusions

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