The use of amino acid PET and conventional MRI for monitoring of brain tumor therapy

Norbert Galldiks, Ian Law, Whitney B Pope, Javier Arbizu, Karl-Josef Langen, Norbert Galldiks, Ian Law, Whitney B Pope, Javier Arbizu, Karl-Josef Langen

Abstract

Routine diagnostics and treatment monitoring of brain tumors is usually based on contrast-enhanced MRI. However, the capacity of conventional MRI to differentiate tumor tissue from posttherapeutic effects following neurosurgical resection, chemoradiation, alkylating chemotherapy, radiosurgery, and/or immunotherapy may be limited. Metabolic imaging using PET can provide relevant additional information on tumor metabolism, which allows for more accurate diagnostics especially in clinically equivocal situations. This review article focuses predominantly on the amino acid PET tracers 11C-methyl-l-methionine (MET), O-(2-[18F]fluoroethyl)-l-tyrosine (FET) and 3,4-dihydroxy-6-[18F]-fluoro-l-phenylalanine (FDOPA) and summarizes investigations regarding monitoring of brain tumor therapy.

Keywords: Bevacizumab; Checkpoint inhibitors; FDOPA; FET; Glioma; Immunotherapy; MET; PET; Pseudoprogression; Pseudoresponse; Temozolomide.

Figures

Fig. 1
Fig. 1
Patient with a newly diagnosed glioblastoma. After resection and chemoradiation with temozolomide, MR and FET PET images show residual tumor in the left frontal lobe (baseline imaging for radiotherapy planning) with complete metabolic response 10 weeks after radiotherapy. The residual contrast-enhancing lesion is metabolically inactive (arrows) indicating a post-treatment effect. This is confirmed 22 months later with complete resolution of this lesion.
Fig. 2
Fig. 2
A 67-year old glioblastoma patient prior to adjuvant chemotherapy (images on the left). After two cycles of temozolomide chemotherapy (images on the right), a clear decrease of both the metabolically active tumor volume and tumor/brain ratios can be observed whereas conventional MRI shows no change of contrast enhancement (“stable disease” according to RANO criteria).
Fig. 3
Fig. 3
A 52-year-old patient with a progressive anaplastic oligoastrocytoma according to the WHO classification 2007 (top row). During follow-up after 8 and 12 months (middle and bottom row) of biweekly bevacizumab therapy, MRI shows a markedly reduction of contrast enhancement and T2 hyperintensity. Correspondingly, FET PET shows a decrease of metabolic activity by means of maximum tumor/brain ratio reduction (TBRmax).

References

    1. Ahluwalia M.S., Wen P.Y. Antiangiogenic therapy for patients with glioblastoma: current challenges in imaging and future directions. Expert. Rev. Anticancer. Ther. 2011;11:653–656.
    1. Albert F.K., Forsting M., Sartor K., Adams H.P., Kunze S. Early postoperative magnetic resonance imaging after resection of malignant glioma: objective evaluation of residual tumor and its influence on regrowth and prognosis. Neurosurgery. 1994;34:45–60.
    1. Albert N.L., Weller M., Suchorska B., Galldiks N., Soffietti R., Kim M.M., la Fougere C., Pope W., Law I., Arbizu J., Chamberlain M.C., Vogelbaum M., Ellingson B.M., Tonn J.C. Response assessment in Neuro-Oncology working group and European Association for Neuro-Oncology recommendations for the clinical use of PET imaging in gliomas. Neuro-Oncology. 2016;18:1199–1208.
    1. Albert N.L., Winkelmann I., Suchorska B., Wenter V., Schmid-Tannwald C., Mille E., Todica A., Brendel M., Tonn J.C., Bartenstein P., la Fougere C. Early static (18)F-FET-PET scans have a higher accuracy for glioma grading than the standard 20–40 min scans. Eur. J. Nucl. Med. Mol. Imaging. 2016;43:1105–1114.
    1. Alkonyi B., Barger G.R., Mittal S., Muzik O., Chugani D.C., Bahl G., Robinette N.L., Kupsky W.J., Chakraborty P.K., Juhasz C. Accurate differentiation of recurrent gliomas from radiation injury by kinetic analysis of alpha-11C-methyl-l-tryptophan PET. J. Nucl. Med. 2012;53:1058–1064.
    1. Awde A.R., Boisgard R., Theze B., Dubois A., Zheng J., Dolle F., Jacobs A.H., Tavitian B., Winkeler A. The translocator protein radioligand 18F-DPA-714 monitors antitumor effect of erufosine in a rat 9L intracranial glioma model. J. Nucl. Med. 2013;54:2125–2131.
    1. Becherer A., Karanikas G., Szabo M., Zettinig G., Asenbaum S., Marosi C., Henk C., Wunderbaldinger P., Czech T., Wadsak W., Kletter K. Brain tumour imaging with PET: a comparison between [18F]fluorodopa and [11C]methionine. Eur. J. Nucl. Med. Mol. Imaging. 2003;30:1561–1567.
    1. Berghoff A.S., Preusser M. In search of a target: PD-1 and PD-L1 profiling across glioma types. Neuro-Oncology. 2016;18(10):1331–1332.
    1. Bergström M., Collins V.P., Ehrin E., Ericson K., Eriksson L., Greitz T., Halldin C., von Holst H., Langstrom B., Lilja A. Discrepancies in brain tumor extent as shown by computed tomography and positron emission tomography using [68Ga]EDTA, [11C]glucose, and [11C]methionine. J. Comput. Assist. Tomogr. 1983;7:1062–1066.
    1. Brandes A.A., Franceschi E., Tosoni A., Blatt V., Pession A., Tallini G., Bertorelle R., Bartolini S., Calbucci F., Andreoli A., Frezza G., Leonardi M., Spagnolli F., Ermani M. MGMT promoter methylation status can predict the incidence and outcome of pseudoprogression after concomitant radiochemotherapy in newly diagnosed glioblastoma patients. J. Clin. Oncol. 2008;26:2192–2197.
    1. Brandsma D., Stalpers L., Taal W., Sminia P., van den Bent M.J. Clinical features, mechanisms, and management of pseudoprogression in malignant gliomas. Lancet Oncol. 2008;9:453–461.
    1. Brandsma D., van den Bent M.J. Pseudoprogression and pseudoresponse in the treatment of gliomas. Curr. Opin. Neurol. 2009;22:633–638.
    1. Calcagni M.L., Galli G., Giordano A., Taralli S., Anile C., Niesen A., Baum R.P. Dynamic O-(2-[18F]fluoroethyl)-l-tyrosine (F-18 FET) PET for glioma grading: assessment of individual probability of malignancy. Clin. Nucl. Med. 2011;36:841–847.
    1. Ceccon G., Lohmann P., Stoffels G., Judov N., Filss C.P., Rapp M., Bauer E., Hamisch C., Ruge M.I., Kocher M., Kuchelmeister K., Sellhaus B., Sabel M., Fink G.R., Shah N.J., Langen K.J., Galldiks N. Dynamic O-(2-18F-fluoroethyl)-l-tyrosine positron emission tomography differentiates brain metastasis recurrence from radiation injury after radiotherapy. Neuro-Oncology. 2016 (Jul 28 Epub ahead of print)
    1. Chen W., Cloughesy T., Kamdar N., Satyamurthy N., Bergsneider M., Liau L., Mischel P., Czernin J., Phelps M.E., Silverman D.H. Imaging proliferation in brain tumors with 18F-FLT PET: comparison with 18F-FDG. J. Nucl. Med. 2005;46:945–952.
    1. Chen W., Delaloye S., Silverman D.H., Geist C., Czernin J., Sayre J., Satyamurthy N., Pope W., Lai A., Phelps M.E., Cloughesy T. Predicting treatment response of malignant gliomas to bevacizumab and irinotecan by imaging proliferation with [18F] fluorothymidine positron emission tomography: a pilot study. J. Clin. Oncol. 2007;25:4714–4721.
    1. Cicone F., Minniti G., Romano A., Papa A., Scaringi C., Tavanti F., Bozzao A., Maurizi Enrici R., Scopinaro F. Accuracy of F-DOPA PET and perfusion-MRI for differentiating radionecrotic from progressive brain metastases after radiosurgery. Eur. J. Nucl. Med. Mol. Imaging. 2015;42:103–111.
    1. Dhermain F.G., Hau P., Lanfermann H., Jacobs A.H., van den Bent M.J. Advanced MRI and PET imaging for assessment of treatment response in patients with gliomas. Lancet Neurol. 2010;9:906–920.
    1. Floeth F.W., Sabel M., Ewelt C., Stummer W., Felsberg J., Reifenberger G., Steiger H.J., Stoffels G., Coenen H.H., Langen K.J. Comparison of (18)F-FET PET and 5-ALA fluorescence in cerebral gliomas. Eur. J. Nucl. Med. Mol. Imaging. 2011;38:731–741.
    1. Galldiks N., Dunkl V., Stoffels G., Hutterer M., Rapp M., Sabel M., Reifenberger G., Kebir S., Dorn F., Blau T., Herrlinger U., Hau P., Ruge M.I., Kocher M., Goldbrunner R., Fink G.R., Drzezga A., Schmidt M., Langen K.J. Diagnosis of pseudoprogression in patients with glioblastoma using O-(2-[(18)F]fluoroethyl)-l-tyrosine PET. Eur. J. Nucl. Med. Mol. Imaging. 2015;42:685–695.
    1. Galldiks N., Filss C.P., Goldbrunner R., Langen K.J. Discrepant MR and [(18)F]fluoroethyl-l-tyrosine PET imaging findings in a patient with bevacizumab failure. Case Rep. Oncol. 2012;5:490–494.
    1. Galldiks N., Kracht L.W., Burghaus L., Thomas A., Jacobs A.H., Heiss W.D., Herholz K. Use of 11C-methionine PET to monitor the effects of temozolomide chemotherapy in malignant gliomas. Eur. J. Nucl. Med. Mol. Imaging. 2006;33:516–524.
    1. Galldiks N., Kracht L.W., Burghaus L., Ullrich R.T., Backes H., Brunn A., Heiss W.D., Jacobs A.H. Patient-tailored, imaging-guided, long-term temozolomide chemotherapy in patients with glioblastoma. Mol. Imaging. 2010;9:40–46.
    1. Galldiks N., Langen K., Holy R., Pinkawa M., Stoffels G., Nolte K., Kaiser H., Filss C., Fink G., Coenen H., Eble M., Piroth M. Assessment of treatment response in patients with glioblastoma using [18F]fluoroethyl-l-tyrosine PET in comparison to MRI. J. Nucl. Med. 2012;53:1048–1057.
    1. Galldiks N., Langen K.J. Amino acid PET - an imaging option to identify treatment response, posttherapeutic effects, and tumor recurrence? Front. Neurol. 2016;7:120.
    1. Galldiks N., Langen K.J., Pope W.B. From the clinician's point of view - what is the status quo of positron emission tomography in patients with brain tumors? Neuro-Oncology. 2015;17:1434–1444.
    1. Galldiks N., Rapp M., Stoffels G., Dunkl V., Sabel M., Langen K.J. Earlier diagnosis of progressive disease during bevacizumab treatment using O-(2-18F-fluorethyl)-l-tyrosine positron emission tomography in comparison with magnetic resonance imaging. Mol. Imaging. 2013;12:273–276.
    1. Galldiks N., Rapp M., Stoffels G., Fink G.R., Shah N.J., Coenen H.H., Sabel M., Langen K.J. Response assessment of bevacizumab in patients with recurrent malignant glioma using [18F]fluoroethyl-l-tyrosine PET in comparison to MRI. Eur. J. Nucl. Med. Mol. Imaging. 2013;40:22–33.
    1. Galldiks N., Stoffels G., Filss C., Rapp M., Blau T., Tscherpel C., Ceccon G., Dunkl V., Weinzierl M., Stoffel M., Sabel M., Fink G.R., Shah N.J., Langen K.J. The use of dynamic O-(2-18F-fluoroethyl)-l-tyrosine PET in the diagnosis of patients with progressive and recurrent glioma. Neuro-Oncology. 2015;17:1293–1300.
    1. Galldiks N., Stoffels G., Filss C.P., Piroth M.D., Sabel M., Ruge M.I., Herzog H., Shah N.J., Fink G.R., Coenen H.H., Langen K.J. Role of O-(2-18F-fluoroethyl)-l-tyrosine PET for differentiation of local recurrent brain metastasis from radiation necrosis. J. Nucl. Med. 2012;53:1367–1374.
    1. Galldiks N., Ullrich R., Schroeter M., Fink G.R., Kracht L.W. Imaging biological activity of a glioblastoma treated with an individual patient-tailored, experimental therapy regimen. J. Neuro-Oncol. 2009;93:425–430.
    1. Galldiks N., von Tempelhoff W., Kahraman D., Kracht L.W., Vollmar S., Fink G.R., Schroeter M., Goldbrunner R., Schmidt M., Maarouf M. 11C-methionine positron emission tomographic imaging of biologic activity of a recurrent glioblastoma treated with stereotaxy-guided laser-induced interstitial thermotherapy. Mol. Imaging. 2012;11:265–271.
    1. Gerstner E.R., Zhang Z., Fink J.R., Muzi M., Hanna L., Greco E., Prah M., Schmainda K.M., Mintz A., Kostakoglu L., Eikman E.A., Ellingson B.M., Ratai E.M., Sorensen A.G., Barboriak D.P., Mankoff D.A., Group, A.T ACRIN 6684: assessment of tumor hypoxia in newly diagnosed glioblastoma using 18F-FMISO PET and MRI. Clin. Cancer Res. 2016
    1. Grosu A.L., Astner S.T., Riedel E., Nieder C., Wiedenmann N., Heinemann F., Schwaiger M., Molls M., Wester H.J., Weber W.A. An interindividual comparison of O-(2-[(18)F]fluoroethyl)-l-tyrosine (FET)- and l-[methyl-(11)C]methionine (MET)-PET in patients with brain gliomas and metastases. Int. J. Radiat. Oncol. Biol. Phys. 2011;81:1049–1058.
    1. Haining Z., Kawai N., Miyake K., Okada M., Okubo S., Zhang X., Fei Z., Tamiya T. Relation of LAT1/4F2hc expression with pathological grade, proliferation and angiogenesis in human gliomas. BMC Clin. Pathol. 2012;12:4.
    1. Heinzel A., Müller D., Langen K.J., Blaum M., Verburg F.A., Mottaghy F.M., Galldiks N. The use of O-(2-18F-fluoroethyl)-l-tyrosine PET for treatment management of bevacizumab and irinotecan in patients with recurrent high-grade glioma: a cost-effectiveness analysis. J. Nucl. Med. 2013;54:1217–1222.
    1. Herholz K., Kracht L.W., Heiss W.D. Monitoring the effect of chemotherapy in a mixed glioma by C-11-methionine PET. J. Neuroimaging. 2003;13:269–271.
    1. Herholz K., Langen K.J., Schiepers C., Mountz J.M. Brain tumors. Semin. Nucl. Med. 2012;42:356–370.
    1. Hodi F.S., Hwu W.J., Kefford R., Weber J.S., Daud A., Hamid O., Patnaik A., Ribas A., Robert C., Gangadhar T.C., Joshua A.M., Hersey P., Dronca R., Joseph R., Hille D., Xue D., Li X.N., Kang S.P., Ebbinghaus S., Perrone A., Wolchok J.D. Evaluation of immune-related response criteria and RECIST v1.1 in patients with advanced melanoma treated with pembrolizumab. J. Clin. Oncol. 2016;34:1510–1517.
    1. Huang C., McConathy J. Radiolabeled amino acids for oncologic imaging. J. Nucl. Med. 2013;54:1007–1010.
    1. Hutterer M., Nowosielski M., Putzer D., Waitz D., Tinkhauser G., Kostron H., Muigg A., Virgolini I.J., Staffen W., Trinka E., Gotwald T., Jacobs A.H., Stockhammer G. O-(2-18F-fluoroethyl)-l-tyrosine PET predicts failure of antiangiogenic treatment in patients with recurrent high-grade glioma. J. Nucl. Med. 2011;52:856–864.
    1. Jacobs A.H., Thomas A., Kracht L.W., Li H., Dittmar C., Garlip G., Galldiks N., Klein J.C., Sobesky J., Hilker R., Vollmar S., Herholz K., Wienhard K., Heiss W.D. 18F-fluoro-l-thymidine and 11C-methylmethionine as markers of increased transport and proliferation in brain tumors. J. Nucl. Med. 2005;46:1948–1958.
    1. Jansen N.L., Suchorska B., Schwarz S.B., Eigenbrod S., Lutz J., Graute V., Bartenstein P., Belka C., Kreth F.W., la Fougere C. [18F]fluoroethyltyrosine-positron emission tomography-based therapy monitoring after stereotactic iodine-125 brachytherapy in patients with recurrent high-grade glioma. Mol. Imaging. 2013;12:137–147.
    1. Jansen N.L., Suchorska B., Wenter V., Eigenbrod S., Schmid-Tannwald C., Zwergal A., Niyazi M., Drexler M., Bartenstein P., Schnell O., Tonn J.C., Thon N., Kreth F.W., la Fougere C. Dynamic 18F-FET PET in newly diagnosed astrocytic low-grade glioma identifies high-risk patients. J. Nucl. Med. 2014;55:198–203.
    1. Jansen N.L., Suchorska B., Wenter V., Schmid-Tannwald C., Todica A., Eigenbrod S., Niyazi M., Tonn J.C., Bartenstein P., Kreth F.W., la Fougere C. Prognostic significance of dynamic 18F-FET PET in newly diagnosed astrocytic high-grade glioma. J. Nucl. Med. 2015;56:9–15.
    1. Kamson D.O., Juhasz C., Buth A., Kupsky W.J., Barger G.R., Chakraborty P.K., Muzik O., Mittal S. Tryptophan PET in pretreatment delineation of newly-diagnosed gliomas: MRI and histopathologic correlates. J. Neuro-Oncol. 2013;112:121–132.
    1. Kamson D.O., Mittal S., Robinette N.L., Muzik O., Kupsky W.J., Barger G.R., Juhasz C. Increased tryptophan uptake on PET has strong independent prognostic value in patients with a previously treated high-grade glioma. Neuro-Oncology. 2014;16:1373–1383.
    1. Kebir S., Fimmers R., Galldiks N., Schafer N., Mack F., Schaub C., Stuplich M., Niessen M., Tzaridis T., Simon M., Stoffels G., Langen K.J., Scheffler B., Glas M., Herrlinger U. Late pseudoprogression in glioblastoma: diagnostic value of dynamic O-(2-[18F]fluoroethyl)-l-tyrosine PET. Clin. Cancer Res. 2016;22:2190–2196.
    1. Kebir S., Rauschenbach L., Galldiks N., Schlaak M., Hattingen E., Landsberg J., Bundschuh R.A., Langen K.J., Scheffler B., Herrlinger U., Glas M. Dynamic O-(2-[18F]fluoroethyl)-l-tyrosine PET imaging for the detection of checkpoint inhibitor-related pseudoprogression in melanoma brain metastases. Neuro-Oncology. 2016;18(10):1462–1464.
    1. Kläsner B., Buchmann N., Gempt J., Ringel F., Lapa C., Krause B.J. Early [18F]FET-PET in gliomas after surgical resection: comparison with MRI and histopathology. PLoS One. 2015;10
    1. Kondo A., Ishii H., Aoki S., Suzuki M., Nagasawa H., Kubota K., Minamimoto R., Arakawa A., Tominaga M., Arai H. Phase IIa clinical study of [18F]fluciclovine: efficacy and safety of a new PET tracer for brain tumors. Ann. Nucl. Med. 2016;30:608–618.
    1. Kratochwil C., Combs S.E., Leotta K., Afshar-Oromieh A., Rieken S., Debus J., Haberkorn U., Giesel F.L. Intra-individual comparison of (18)F-FET and (18)F-DOPA in PET imaging of recurrent brain tumors. Neuro-Oncology. 2014;16:434–440.
    1. Kruser T.J., Mehta M.P., Robins H.I. Pseudoprogression after glioma therapy: a comprehensive review. Expert. Rev. Neurother. 2013;13:389–403.
    1. Kumar A.J., Leeds N.E., Fuller G.N., Van Tassel P., Maor M.H., Sawaya R.E., Levin V.A. Malignant gliomas: MR imaging spectrum of radiation therapy- and chemotherapy-induced necrosis of the brain after treatment. Radiology. 2000;217:377–384.
    1. Lacroix M., Abi-Said D., Fourney D.R., Gokaslan Z.L., Shi W., DeMonte F., Lang F.F., McCutcheon I.E., Hassenbusch S.J., Holland E., Hess K., Michael C., Miller D., Sawaya R. A multivariate analysis of 416 patients with glioblastoma multiforme: prognosis, extent of resection, and survival. J. Neurosurg. 2001;95:190–198.
    1. Langen K.J., Hamacher K., Weckesser M., Floeth F., Stoffels G., Bauer D., Coenen H.H., Pauleit D. O-(2-[18F]fluoroethyl)-l-tyrosine: uptake mechanisms and clinical applications. Nucl. Med. Biol. 2006;33:287–294.
    1. Langen K.J., Jarosch M., Mühlensiepen H., Hamacher K., Broer S., Jansen P., Zilles K., Coenen H.H. Comparison of fluorotyrosines and methionine uptake in F98 rat gliomas. Nucl. Med. Biol. 2003;30:501–508.
    1. Langen K.J., Watts C. Neuro-oncology: amino acid PET for brain tumours - ready for the clinic? Nat. Rev. Neurol. 2016;12:375–376.
    1. Lee S.T., Scott A.M. Hypoxia positron emission tomography imaging with 18f-fluoromisonidazole. Semin. Nucl. Med. 2007;37:451–461.
    1. Lescher S., Schniewindt S., Jurcoane A., Senft C., Hattingen E. Time window for postoperative reactive enhancement after resection of brain tumors: less than 72 hours. Neurosurg. Focus. 2014;37
    1. Lizarraga K.J., Allen-Auerbach M., Czernin J., DeSalles A.A., Yong W.H., Phelps M.E., Chen W. (18)F-FDOPA PET for differentiating recurrent or progressive brain metastatic tumors from late or delayed radiation injury after radiation treatment. J. Nucl. Med. 2014;55:30–36.
    1. Macdonald D.R., Cascino T.L., Schold S.C., Jr., Cairncross J.G. Response criteria for phase II studies of supratentorial malignant glioma. J. Clin. Oncol. 1990;8:1277–1280.
    1. Minniti G., Clarke E., Lanzetta G., Osti M.F., Trasimeni G., Bozzao A., Romano A., Enrici R.M. Stereotactic radiosurgery for brain metastases: analysis of outcome and risk of brain radionecrosis. Radiat. Oncol. 2011:48. (May 15)
    1. Morana G., Piccardo A., Garre M.L., Nozza P., Consales A., Rossi A. Multimodal magnetic resonance imaging and 18F-l-dihydroxyphenylalanine positron emission tomography in early characterization of pseudoresponse and nonenhancing tumor progression in a pediatric patient with malignant transformation of ganglioglioma treated with bevacizumab. J. Clin. Oncol. 2013;31:e1–e5.
    1. Moulin-Romsée G., D'Hondt E., de Groot T., Goffin J., Sciot R., Mortelmans L., Menten J., Bormans G., Van Laere K. Non-invasive grading of brain tumours using dynamic amino acid PET imaging: does it work for 11C-methionine? Eur. J. Nucl. Med. Mol. Imaging. 2007;34:2082–2087.
    1. Nduom E.K., Wei J., Yaghi N.K., Huang N., Kong L.Y., Gabrusiewicz K., Ling X., Zhou S., Ivan C., Chen J.Q., Burks J.K., Fuller G.N., Calin G.A., Conrad C.A., Creasy C., Ritthipichai K., Radvanyi L., Heimberger A.B. PD-L1 expression and prognostic impact in glioblastoma. Neuro-Oncology. 2016;18:195–205.
    1. Okada H., Weller M., Huang R., Finocchiaro G., Gilbert M.R., Wick W., Ellingson B.M., Hashimoto N., Pollack I.F., Brandes A.A., Franceschi E., Herold-Mende C., Nayak L., Panigrahy A., Pope W.B., Prins R., Sampson J.H., Wen P.Y., Reardon D.A. Immunotherapy response assessment in neuro-oncology: a report of the RANO working group. Lancet Oncol. 2015;16:e534–e542.
    1. Okubo S., Zhen H.N., Kawai N., Nishiyama Y., Haba R., Tamiya T. Correlation of l-methyl-11C-methionine (MET) uptake with l-type amino acid transporter 1 in human gliomas. J. Neuro-Oncol. 2010;99:217–225.
    1. Papin-Michault C., Bonnetaud C., Dufour M., Almairac F., Coutts M., Patouraux S., Virolle T., Darcourt J., Burel-Vandenbos F. Study of LAT1 expression in brain metastases: towards a better understanding of the results of positron emission tomography using amino acid tracers. PLoS One. 2016;11
    1. Piroth M.D., Holy R., Pinkawa M., Stoffels G., Kaiser H.J., Galldiks N., Herzog H., Coenen H.H., Eble M.J., Langen K.J. Prognostic impact of postoperative, pre-irradiation (18)F-fluoroethyl-l-tyrosine uptake in glioblastoma patients treated with radiochemotherapy. Radiother. Oncol. 2011;99:218–224.
    1. Piroth M.D., Liebenstund S., Galldiks N., Stoffels G., Shah N.J., Eble M.J., Coenen H.H., Langen K.J. Monitoring of radiochemotherapy in patients with glioblastoma using O-(2-(18)fluoroethyl)-l-tyrosine positron emission tomography: is dynamic imaging helpful? Mol. Imaging. 2013;12:388–395.
    1. Piroth M.D., Pinkawa M., Holy R., Klotz J., Nussen S., Stoffels G., Coenen H.H., Kaiser H.J., Langen K.J., Eble M.J. Prognostic value of early [18F]fluoroethyltyrosine positron emission tomography after radiochemotherapy in glioblastoma multiforme. Int. J. Radiat. Oncol. Biol. Phys. 2011;80:176–184.
    1. Pirotte B.J., Levivier M., Goldman S., Massager N., Wikler D., Dewitte O., Bruneau M., Rorive S., David P., Brotchi J. Positron emission tomography-guided volumetric resection of supratentorial high-grade gliomas: a survival analysis in 66 consecutive patients. Neurosurgery. 2009;64:471–481.
    1. Pöpperl G., Goldbrunner R., Gildehaus F.J., Kreth F.W., Tanner P., Holtmannspotter M., Tonn J.C., Tatsch K. O-(2-[18F]fluoroethyl)-l-tyrosine PET for monitoring the effects of convection-enhanced delivery of paclitaxel in patients with recurrent glioblastoma. Eur. J. Nucl. Med. Mol. Imaging. 2005;32:1018–1025.
    1. Pöpperl G., Götz C., Rachinger W., Schnell O., Gildehaus F.J., Tonn J.C., Tatsch K. Serial O-(2-[(18)F]fluoroethyl)-l:-tyrosine PET for monitoring the effects of intracavitary radioimmunotherapy in patients with malignant glioma. Eur. J. Nucl. Med. Mol. Imaging. 2006;33:792–800.
    1. Pöpperl G., Kreth F.W., Mehrkens J.H., Herms J., Seelos K., Koch W., Gildehaus F.J., Kretzschmar H.A., Tonn J.C., Tatsch K. FET PET for the evaluation of untreated gliomas: correlation of FET uptake and uptake kinetics with tumour grading. Eur. J. Nucl. Med. Mol. Imaging. 2007;34:1933–1942.
    1. Poulsen S.H., Urup T., Grunnet K., Christensen I.J., Larsen V.A., Jensen M.L., Af Rosenschold P.M., Poulsen H.S., Law I. The prognostic value of FET PET at radiotherapy planning in newly diagnosed glioblastoma. Eur. J. Nucl. Med. Mol. Imaging. 2016 (Epub ahead of print 23 Aug)
    1. Preusser M., Lim M., Hafler D.A., Reardon D.A., Sampson J.H. Prospects of immune checkpoint modulators in the treatment of glioblastoma. Nat. Rev. Neurol. 2015;11:504–514.
    1. Reithmeier T., Lopez W.O., Spehl T.S., Nguyen T., Mader I., Nikkhah G., Pinsker M.O. Bevacizumab as salvage therapy for progressive brain stem gliomas. Clin. Neurol. Neurosurg. 2013;115:165–169.
    1. Roelcke U., Wyss M.T., Nowosielski M., Ruda R., Roth P., Hofer S., Galldiks N., Crippa F., Weller M., Soffietti R. Amino acid positron emission tomography to monitor chemotherapy response and predict seizure control and progression-free survival in WHO grade II gliomas. Neuro-Oncology. 2016;18:744–751.
    1. Schwarzenberg J., Czernin J., Cloughesy T.F., Ellingson B.M., Pope W.B., Grogan T., Elashoff D., Geist C., Silverman D.H., Phelps M.E., Chen W. Treatment response evaluation using 18F-FDOPA PET in patients with recurrent malignant glioma on bevacizumab therapy. Clin. Cancer Res. 2014;20:3550–3559.
    1. Shah A.H., Snelling B., Bregy A., Patel P.R., Tememe D., Bhatia R., Sklar E., Komotar R.J. Discriminating radiation necrosis from tumor progression in gliomas: a systematic review what is the best imaging modality? J. Neuro-Oncol. 2013;112:141–152.
    1. Singhal T., Narayanan T.K., Jain V., Mukherjee J., Mantil J. 11C-l-methionine positron emission tomography in the clinical management of cerebral gliomas. Mol. Imaging Biol. 2008;10:1–18.
    1. Spence A.M., Muzi M., Swanson K.R., O'Sullivan F., Rockhill J.K., Rajendran J.G., Adamsen T.C., Link J.M., Swanson P.E., Yagle K.J., Rostomily R.C., Silbergeld D.L., Krohn K.A. Regional hypoxia in glioblastoma multiforme quantified with [18F]fluoromisonidazole positron emission tomography before radiotherapy: correlation with time to progression and survival. Clin. Cancer Res. 2008;14:2623–2630.
    1. Stummer W., Pichlmeier U., Meinel T., Wiestler O.D., Zanella F., Reulen H.J. Fluorescence-guided surgery with 5-aminolevulinic acid for resection of malignant glioma: a randomised controlled multicentre phase III trial. Lancet Oncol. 2006;7:392–401.
    1. Stuplich M., Hadizadeh D.R., Kuchelmeister K., Scorzin J., Filss C., Langen K.J., Schafer N., Mack F., Schuller H., Simon M., Glas M., Pietsch T., Urbach H., Herrlinger U. Late and prolonged pseudoprogression in glioblastoma after treatment with lomustine and temozolomide. J. Clin. Oncol. 2012;30:e180–e183.
    1. Su Z., Herholz K., Gerhard A., Roncaroli F., Du Plessis D., Jackson A., Turkheimer F., Hinz R. [(11)C]-(R)PK11195 tracer kinetics in the brain of glioma patients and a comparison of two referencing approaches. Eur. J. Nucl. Med. Mol. Imaging. 2013;40:1406–1419.
    1. Su Z., Roncaroli F., Durrenberger P.F., Coope D.J., Karabatsou K., Hinz R., Thompson G., Turkheimer F.E., Janczar K., Du Plessis D., Brodbelt A., Jackson A., Gerhard A., Herholz K. The 18-kDa mitochondrial translocator protein in human gliomas: a 11C-(R)PK11195 PET imaging and neuropathology study. J. Nucl. Med. 2015;56:512–517.
    1. Suchorska B., Jansen N.L., Linn J., Kretzschmar H., Janssen H., Eigenbrod S., Simon M., Popperl G., Kreth F.W., la Fougere C., Weller M., Tonn J.C., German Glioma N. Biological tumor volume in 18FET-PET before radiochemotherapy correlates with survival in GBM. Neurology. 2015;84:710–719.
    1. Suchorska B., Tonn J.C., Jansen N.L. PET imaging for brain tumor diagnostics. Curr. Opin. Neurol. 2014;27:683–688.
    1. Swissmedic Swiss agency for therapeutic products. J. Swissmedic. 2014;13:651.
    1. Terakawa Y., Tsuyuguchi N., Iwai Y., Yamanaka K., Higashiyama S., Takami T., Ohata K. Diagnostic accuracy of 11C-methionine PET for differentiation of recurrent brain tumors from radiation necrosis after radiotherapy. J. Nucl. Med. 2008;49:694–699.
    1. Tsuyuguchi N., Sunada I., Iwai Y., Yamanaka K., Tanaka K., Takami T., Otsuka Y., Sakamoto S., Ohata K., Goto T., Hara M. Methionine positron emission tomography of recurrent metastatic brain tumor and radiation necrosis after stereotactic radiosurgery: is a differential diagnosis possible? J. Neurosurg. 2003;98:1056–1064.
    1. Venneti S., Dunphy M.P., Zhang H., Pitter K.L., Zanzonico P., Campos C., Carlin S.D., La Rocca G., Lyashchenko S., Ploessl K., Rohle D., Omuro A.M., Cross J.R., Brennan C.W., Weber W.A., Holland E.C., Mellinghoff I.K., Kung H.F., Lewis J.S., Thompson C.B. Glutamine-based PET imaging facilitates enhanced metabolic evaluation of gliomas in vivo. Sci. Transl. Med. 2015;7 (274ra217)
    1. Voges J., Herholz K., Holzer T., Würker M., Bauer B., Pietrzyk U., Treuer H., Schroder R., Sturm V., Heiss W.D. 11C-methionine and 18F-2-fluorodeoxyglucose positron emission tomography: a tool for diagnosis of cerebral glioma and monitoring after brachytherapy with 125I seeds. Stereotact. Funct. Neurosurg. 1997;69:129–135.
    1. Wardak M., Schiepers C., Cloughesy T.F., Dahlbom M., Phelps M.E., Huang S.C. 18F-FLT and 18F-FDOPA PET kinetics in recurrent brain tumors. Eur. J. Nucl. Med. Mol. Imaging. 2014;41:1199–1209.
    1. Weber W.A., Wester H.J., Grosu A.L., Herz M., Dzewas B., Feldmann H.J., Molls M., Stocklin G., Schwaiger M. O-(2-[18F]fluoroethyl)-l-tyrosine and l-[methyl-11C]methionine uptake in brain tumours: initial results of a comparative study. Eur. J. Nucl. Med. 2000;27:542–549.
    1. Wen P.Y., Macdonald D.R., Reardon D.A., Cloughesy T.F., Sorensen A.G., Galanis E., Degroot J., Wick W., Gilbert M.R., Lassman A.B., Tsien C., Mikkelsen T., Wong E.T., Chamberlain M.C., Stupp R., Lamborn K.R., Vogelbaum M.A., van den Bent M.J., Chang S.M. Updated response assessment criteria for high-grade gliomas: response assessment in neuro-oncology working group. J. Clin. Oncol. 2010;28:1963–1972.
    1. Wester H.J., Herz M., Weber W., Heiss P., Senekowitsch-Schmidtke R., Schwaiger M., Stocklin G. Synthesis and radiopharmacology of O-(2-[18F]fluoroethyl)-l-tyrosine for tumor imaging. J. Nucl. Med. 1999;40:205–212.
    1. Winkeler A., Boisgard R., Awde A.R., Dubois A., Theze B., Zheng J., Ciobanu L., Dolle F., Viel T., Jacobs A.H., Tavitian B. The translocator protein ligand [18F]DPA-714 images glioma and activated microglia in vivo. Eur. J. Nucl. Med. Mol. Imaging. 2012;39:811–823.
    1. Wiriyasermkul P., Nagamori S., Tominaga H., Oriuchi N., Kaira K., Nakao H., Kitashoji T., Ohgaki R., Tanaka H., Endou H., Endo K., Sakurai H., Kanai Y. Transport of 3-fluoro-l-alpha-methyl-tyrosine by tumor-upregulated l-type amino acid transporter 1: a cause of the tumor uptake in PET. J. Nucl. Med. 2012;53:1253–1261.
    1. Wolchok J.D., Hoos A., O'Day S., Weber J.S., Hamid O., Lebbe C., Maio M., Binder M., Bohnsack O., Nichol G., Humphrey R., Hodi F.S. Guidelines for the evaluation of immune therapy activity in solid tumors: immune-related response criteria. Clin. Cancer Res. 2009;15:7412–7420.
    1. Würker M., Herholz K., Voges J., Pietrzyk U., Treuer H., Bauer B., Sturm V., Heiss W.D. Glucose consumption and methionine uptake in low-grade gliomas after iodine-125 brachytherapy. Eur. J. Nucl. Med. 1996;23:583–586.
    1. Wyss M., Hofer S., Bruehlmeier M., Hefti M., Uhlmann C., Bartschi E., Buettner U.W., Roelcke U. Early metabolic responses in temozolomide treated low-grade glioma patients. J. Neuro-Oncol. 2009;95:87–93.
    1. Youland R.S., Kitange G.J., Peterson T.E., Pafundi D.H., Ramiscal J.A., Pokorny J.L., Giannini C., Laack N.N., Parney I.F., Lowe V.J., Brinkmann D.H., Sarkaria J.N. The role of LAT1 in (18)F-DOPA uptake in malignant gliomas. J. Neuro-Oncol. 2013;111:11–18.

Source: PubMed

3
Subscribe