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Stereotactic radiotherapy of brain metastases: clinical impact of three-dimensional SPACE imaging for 3T-MRI-based treatment planning

Stereotactic radiotherapy of brain metastases: clinical impact of three-dimensional SPACE imaging... Purpose For planning CyberKnife stereotactic radiosurgery (CK SRS) of brain metastases (BM), it is essential to precisely determine the exact number and location of BM in MRI. Recent MR studies suggest the superiority of contrast-enhanced 3D fast spin echo SPACE (sampling perfection with application-optimized contrast by using different flip angle evolutions) images over 3D gradient echo (GE) T1-weighted MPRAGE (magnetization-prepared rapid gradient echo) images for detecting small BM. The aim of this study is to test the usability of the SPACE sequence for MRI-based radiation treatment planning and its impact on changing treatment. Methods For MRI-based radiation treatment planning using 3T MRI in 199 patients with cerebral oligometastases, we compared the detectability of BM in post-gadolinium SPACE images, post-gadolinium MPRAGE images, and post-gadolin- ium late-phase MPRAGE images. Results When SPACE images were used for MRI-based radiation treatment planning, 29.8% and 16.9% more BM, respec- tively, were detected and included in treatment planning than in the post-gadolinium MPRAGE images and the post-gadolin- ium late-phase MPRAGE images (post-gadolinium MPRAGE imaging: n = 681, mean ± SD 3.4 ± 4.2; post-gadolinium total SPACE imaging: n = 884, mean ± SD 4.4 ± 6.0; post-gadolinium late-phase MPRAGE imaging: n = 796, mean ± SD total total 4.0 ± 5.3; P < 0.0001, P post-gadolinium SPACE imaging versus post-gadolinium MPRAGE imaging post-gadolinium SPACE imaging versus post-gadolinium late-phase MPRAGE imaging < 0.0001). Conclusion For 3T MRI-based treatment planning of stereotactic radiosurgery of BM, we recommend the use of post- gadolinium SPACE imaging rather than post-gadolinium MPRAGE imaging. Keywords Brain metastases · CyberKnife · Stereotactic radiosurgery · Variable flip angle · Magnetic resonance imaging Abbreviations GE Gradient echo BM Brain metastasis MPRAGE Magnetization-prepared rapid acquisi- CK CyberKnife tion of gradient echo CR Contrast rate MRI Magnetic resonance imaging Thomas Welzel, MD thomas.welzel@med.uni-heidelberg.de German Cancer Consortium (DKTK), Partner site Heidelberg, German Cancer Research Center (DKFZ), Heidelberg, Department of Radiation Oncology, Heidelberg University Germany Hospital, Im Neuenheimer Feld 400, 69120 Heidelberg, Department of Radiation Oncology, University Medical Germany Center Göttingen, Robert-Koch-Str. 40, 37075 Göttingen, Heidelberg Institute of Radiation Oncology (HIRO), Germany Heidelberg, Germany Department of Radiation Oncology, Klinikum rechts National Center for Tumor diseases (NCT), Heidelberg, der Isar, Technical University Munich, Ismaninger Germany Str. 22, 81675 Munich, Germany K Strahlenther Onkol (2022) 198:926–933 927 SE Spin echo the cortical vessels, the contrast enhancement of very small SPACE Sampling perfection with application- cerebral metastases is much clearer in 3D SPACE than in optimized contrast by using different 3D MPRAGE images. Kato et al. showed in an initial study flip angle evolutions with 16 patients with BM that 3D SPACE visualizes metas- SRS Stereotactic radiosurgery tases significantly better than 3D MPRAGE due to the better WBRT Whole-brain radiotherapy contrast rate (CR) [10]. The clinical significance of this fast (turbo) spin echo technique as black blood imaging for radiotherapy has not Introduction yet been studied. This clinical study aims to investigate whether 3D SPACE can be integrated in preradiotherapy Magnetic resonance imaging (MRI) is a safe and effective staging and radiation treatment planning. The objective of diagnostic examination technique for radiation treatment the study is to clarify how many more metastases are de- planning for cerebral metastases. The decision on the tected using 3D SPACE compared with 3D MPRAGE in ra- optimal radiotherapy for patients with cerebral oligometas- diation treatment planning and what effect the higher num- tases depends to a great extent on the number and lo- ber of metastases has on the later radiation technique (SRS cation of the metastases. While whole-brain radiotherapy versus WBRT). A metastasis count of ≤ 4 BM was specified (WBRT) is performed for diffuse metastasis, for oligometas- as the upper limit for SRS according to the guidelines from tases, stereotactic radiosurgery (SRS) is used to protect 2015 [13]. neurocognitive function [1–4]. In order to detect even the Several authors have reported that the lesion contrast smallest BM, the diagnostic accuracy of the MR examina- of BM increases with delayed imaging time [14, 15]. For tion technique is thus critical. departments that do not have access to black blood imag- In 2000, Hochstenbag et al. reported on the significance ing sequences such as 3D SPACE for radiation treatment of the MRI examination in pretherapeutic staging of BM planning, it should be tested whether a 3D MPRAGE late- [5]. Through the use of MRI alone, the number of newly phase contrast-enhanced image can detect the same number detected BM in SCLC patients increased by 15%. In this of metastases as 3D SPACE. study on a 0.5T MRI, only T1-weighted spin echo (SE) se- quences with a relatively large slice thicknesses of 10 mm Materials and methods were used. However, pulsation artifacts of the vessels in the posterior fossa result in poor image quality in stan- dard SE images. Metastases in the brainstem or cerebel- Patients lum can thus be missed. With the introduction of contrast- enhanced 3D GE T1-weighted MPRAGE (magnetization- All patients had an external diagnostic MRI examination prepared rapid gradient echo) images, Wenz et al. were and were referred to our CyberKnife (Accuray Inc. Sun- able to detect considerably more metastases in 1.5T MRI nyvale, CA, USA) center for SRS with suspected BM. than with SE sequences alone [6]. This was primarily due The study enrolled 214 consecutive patients with brain to the thinner slices. The superior spatial resolution of the oligometastases (no more than 4 lesions in diagnostic MRI, 3D GE sequences is associated with a greater susceptibility no extracranial metastases) who had an MRI for radiation for artifacts and poorer contrast compared with 2D SE se- planning for SRS between May 2016 and February 2018 at quences [7, 8]. With the introduction of new isotropic 3D the Department of Radiation Oncology and Radiation Ther- fast (turbo) spin echo sequences, it is today possible to de- apy at Heidelberg University Hospital. All patients were tect very small metastatic lesions (< 5 mm) in an acceptable older than 18 years and had no contraindication to an MRI examination time using 3.0T MRI. These sequences feature examination. The MRI data of 15 patients could not be eval- very long echo trains, lower flip angles, and ultrashort echo uated because of the absence of BM in MRI-based radia- spacing. Mugler et al. developed a 3D fast SE sequence tion treatment planning (MPRAGE and SPACE sequences; with variable flip angle refocusing pulses [9]. That which is n = 7 patients after chemotherapy) or had incomplete MRI termed the SPACE sequence solved the previous problems sequences due to poor general condition (n = 8 patients). of poor 3D resolution of gradient echo sequences using The patient characteristics of the remaining 199 patients sampling perfection with application-optimized contrast by are summarized in Table 1. using different flip angle evolutions. Due to the isotropic resolution, the voxels generated are the same size in every Magnetic resonance imaging direction, allowing reconstruction in all three planes. Vari- ous studies have reported on the diagnostic significance of MRI was carried out on a 3T scanner (Magnetom SKYRA , the SPACE sequence [10–12]. By suppressing the signal in Siemens Medical Systems, Erlangen, Germany) using K 928 Strahlenther Onkol (2022) 198:926–933 Table 1 Patient characteristics were diagnosed as cerebral metastases were included in the subsequent radiation treatment planning. For the contrast- All patients, no 199 enhanced MR sequences, the MPRAGE images were first Gender, no. (%) evaluated, then the SPACE images, and finally the post- Female 112 (56.3) gadolinium late-phase MPRAGE images. We measured the Male 87 (43.7) shorter diameter of each lesion in the axial plane of the Age, years MPRAGE and SPACE images. After this reviewing pro- Median (range) 62 (20–90) cess, an expert panel of radiation oncologists considered IQR 17 the scans again. The radiation therapy modality (SRS ver- Immunomodulating therapy, no. (%) sus WBRT) was selected at the discretion of the treating ra- No immunomodulating therapy 143 (71.9) diation oncologists, based on the number of lesions, lesion Immunomodulating therapy 56 (28.1) size, location of the lesions, and the patient’s performance Primary tumor type, no. (%) status. Lung 110 (55.3) The study protocol was approved by the local ethics com- Melanoma 29 (14.6) mittee. The study complies with the Helsinki Declaration, Breast 28 (14.1) the American Medical Association’s professional code of Renal cell carcinoma 13 (6.5) conduct, the principles of Good Clinical Practice guide- Cancer of unknown primary (CUP) 5 (2.5) lines, and the Federal Data Protection Act. Others 14 (7.0) Previous radiotherapy to the brain, no. (%) Statistical methods No SRS/WBRT 154 (77.4) SRS 26 (13.1) The paired-samples t-test was used to compare the mean WBRT 19 (9.5) number of BM on the standard MPRAGE sequence with IQR interquartile range, SRS stereotactic radiosurgery, WBRT whole- brain radiotherapy the mean number of metastases on the late-phase MPRAGE Percentages may not add up to 100 because of rounding and SPACE sequences. Spearman rank-order correlation co- efficients (r ) were computed to test for associations be- a transmit/receive quadrature four-channel head coil. All tween the number of metastatic lesions on the early-phase scans were carried out without immobilization devices for MPRAGE sequence and the number of additional metastatic use in treatment planning. The axial images were conducted lesions on the late-phase MPRAGE and SPACE sequences. without tilting in order to ensure a later fusion with CT All calculations were performed using SPSS version 27 examinations for radiation treatment planning. (IBM, Armonk, NY, USA) with p < 0.05 considered signif- The same imaging protocol was used in all patients and icant. was standardized for timing and sequence order: a three- dimensional high-resolution T1-weighted gradient echo se- quence (repetition time 2000 ms, echo time 2.44 ms, slice thickness 0.9 mm) for MPRAGE was carried out 2 min af- ter intravenous administration of 0.1 mmol/kg body weight Table 2 Brain metastases’ characteristics of gadobutrol (Gadovist, Bayer Schering Pharma, Berlin, Early-phase Late-phase SPACE Germany) with an additional saline flush of 30 ml. The MPRAGE MPRAGE imaging parameters for the SPACE were repetition time Total number 681 796 884 700 ms, echo time 12 ms, and slice thickness 1.0 mm. The Mean (SD) 3.4 (4.2) 4.0 (5.3) 4.4 (6.0) post-gadolinium late-phase MPRAGE images were made Median 2 (0–31) 2 (1–37) 2 (1–37) 10 min after contrast agent administration. (range) The MRI scans were reviewed by a specialized radi- IQR 33 4 ologist (TW) and a specialized radiation oncologist (SR) Grouping of patients by number of brain metastases, no. (%) with > 15 years extensive experience in cerebral MRI. All 03(1.5) 0 0 cerebral lesions were evaluated based on the criteria pub- 1–4 156 (78.4) 155 (77.9) 147 (73.9) lished by Kato et al. [10]. First, the normal structures with 5–10 27 (13.6) 29 (14.6) 36 (18.1) contrast enhancement such as cortical vessels were differ- > 10 13 (6.5) 15 (7.5) 16 (8.0) entiated from suspicious lesions. Of the suspicious cerebral IQR interquartile range, SD standard deviation, MPRAGE magneti- contrast-enhancing lesions, the lesions not suspicious for zation-prepared rapid acquisition of gradient echo, SPACE sampling metastasis (such as venous anomalies) were differentiated perfection with application-optimized contrast by using different flip from the lesions suspicious for metastasis. All lesions that angle evolutions K Strahlenther Onkol (2022) 198:926–933 929 Results five developmental venous anomalies (DVA). The mean numbers of BM on the 3D SPACE and 3D MPRAGE A summary of the BM characteristics is shown in Table 2. late-phase sequences were significantly higher than those Overall, we detected 29.8% more BM on the 3D SPACE found on the standard 3D MPRAGE sequences (p < 0.0001, sequences and 16.9% more BM on the 3D MPRAGE paired-samples t-test for both comparisons). Of note, le- late-phase sequences than on the established standard 3D sions of less than 2 mm in diameter on the 3D SPACE MPRAGE sequences. Incidental findings were detected in sequence were not seen in either the established standard 3% of the 199 patients and included one meningioma and 3D MPRAGE or the 3D MPRAGE late-phase sequence. Fig. 1 a MPRAGE post gadolinium: cystic metastasis in the right temporal lobe poorly differentiable from surrounding structures. b MPRAGE late post gadolinium: increasing contrast enhancement of the right temporal metastasis. c SPACE post gadolinium: metastasis clearly more differ- entiable from the cortical veins. d CyberKnife (Accuray Inc. Sunnyvale, CA, USA) treatment plan K 930 Strahlenther Onkol (2022) 198:926–933 Fig. 2 a MPRAGE post gadolin- ium: periventricular metastasis (arrow) poorly differentiable from periventricular vessels. b SPACE post gadolinium: sig- nificantly improved visualiza- tion of periventricular metastasis (arrow) due to signal suppres- sion of periventricular vessels Fig. 3 Correlation between the number of metastatic lesions Spearman's correlation r = 0.38 in the early-phase MPRAGE s 95% CI 0.05-0.64 sequence and the number of additional metastatic lesions 16 p = 0.015 in the late-phase MPRAGE sequence (a)and the SPACE sequence (b) 0 2 4 6 8 101214161820222426283032 Number of metastatic lesions early phase MPRAGE Spearman's correlation r = 0.49 95% CI 0.24-0.68 p < 0.001 0 2 4 6 8 101214161820222426283032 Number of metastatic lesions early phase MPRAGE Number of additional metastatic lesions Number of additional metastatic lesions SPACE late phase MPRAGE Strahlenther Onkol (2022) 198:926–933 931 Table 3 Numbers (and percentages) of patients, metastases, and SRS treatments by grouping the patients with 0–4 metastases in the early-phase MPRAGE sequence according to the presence or absence of additional metastases on the SPACE and late-phase MPRAGE sequences Patients Metastases Decision for SRS SRS performed based on SPACE imag- ing Detection of metastatic Early- Late- SPACE Number of Patients Metastases Patients Metastases lesions relative to early- phase phase additional de- (%) (%) (%) (%) phase MPRAGE imaging MPRAGE MPRAGE tected metas- tases Additional metastases on 16 35 35 54 SPACE: +19 12 (75.0) 33 (61.1) 11 27 SPACE imaging Late-phase (91.7) (81.8) MPRAGE: +0 Additional metastases 18 35 71 86 SPACE: +51 10 (55.6) 28 (32.6) 9 23 on SPACE ± late-phase Late-phase (90.0) (82.1) MPRAGE imaging MPRAGE: +36 No additional metastases 125 230 230 230 SPACE: +0 125 230 121 221 on SPACE + late-phase Late-phase (100) (100) (96.8) (96.1) MPRAGE imaging MPRAGE: +0 MPRAGE magnetization-prepared rapid acquisition of gradient echo, SPACE sampling perfection with application-optimized contrast by using different flip angle evolutions Metastatic lesions near the cortical vessels (Fig. 1c) and 10 patients, so these patients were given a recommendation periventricular metastases (Fig. 2b) were particularly well for SRS from the tumor board. SRS was carried out in a to- detected by the 3D SPACE sequence. tal of 9 patients. One patient with only one brain metastasis At the patient level, the 3D SPACE sequence showed could not be treated with SRS because he could not tolerate 57.8% more metastatic lesions than the standard 3D prolonged immobilization during treatment. He was given MPRAGE sequence in 60 of the 199 patients (554 ver- WBRT with boost for this metastasis (details are shown sus 351 metastases in 30.2% of the patients), and the 3D in Table 3). Summarizing the two oligometastatic groups, MPRAGE late-phase sequence detected 39.1% more le- a total of 20 oligometastatic patients were given SRS for sions than the standard 3D MPRAGE sequence in 41 of the additional metastases detected solely on the basis of the 199 patients (409 versus 294 metastases in 20.6% of SPACE. the patients). The higher the number of BM detected in the standard 3D MPRAGE sequence, the higher the number of additional metastases in the 3D MPRAGE late-phase Discussion sequence (for details see Fig. 3). Several studies have shown that black blood (BB) MRI Modification of radiotherapy based on SPACE (SPACE, VISTA) detects significantly more brain lesions findings <5mm [10, 16, 17]. This study showed for the first time that BB imaging (SPACE) can be effectively integrated In this study, 80% of the patients (n = 159) had cerebral into stereotactic radiation treatment planning with the Cy- oligometastases with between 0 and 4 BM. In a total of 125 berKnife. Among the multifactorial causes for the supe- oligometastatic patients in whom the standard early-phase rior detectability of BM using SPACE are the better sig- MPRAGE showed 0–4 metastases, no additional metastases nal-to-noise ratio and the higher spatial resolution in the were found in the late-phase MPRAGE and SPACE scans. submillimeter range. The sequence is clearly superior to The SPACE scan alone detected 19 additional metastases in MPRAGE in detecting smaller short-axis diameters and 16 oligometastatic patients, so SRS treatment was indicated thus also smaller metastases. However, false-positive find- for 12 patients. In 11 patients, these additional metastases ings due to insufficient suppression of cortical vessels or could be irradiated using SRS. For one patient, the radi- small contrast enhancement of an immunological inflam- ation treatment planning MRI showed additional calvarial matory response due to antibody treatment can be misinter- metastases, so WBRT was carried out. preted to be a metastasis. In 18 oligometastatic patients, more metastases were In the late-phase MPRAGE imaging, cerebral metastases found simultaneously in the late-phase MPRAGE (n = 36) show contrast blush as an expression of neovascularization and in the SPACE (n = 51) scans than in the standard early- compared with early-phase MPRAGE imaging (Fig. 1b). In phase MPRAGE scan. In this patient group, the SPACE scan addition, washout of the contrast agent was seen in the cere- showed more metastases than the late-phase MPRAGE in bral vessels in late-phase MPRAGE imaging (Fig. 1b). This K 932 Strahlenther Onkol (2022) 198:926–933 facilitates better differentiation of the intracerebral vessels Conclusion from metastases in late-phase MPRAGE imaging as well. The 3D SPACE image showed more intracerebral metas- Using 3D SPACE is a practical alternative to the routinely tases and, above all, smaller metastases in MRI-based used T1-weighted 3D MPRAGE, especially for radio- radiation treatment planning compared with conventional surgery treatment planning for BM. Our data show that 3D MPRAGE. These metastases would not have been 3D SPACE allows detection of significantly more cerebral included in radiation treatment if only contrast-enhanced metastases that can be included in radiation treatment plan- 3D MPRAGE had been used. This would have led later ning. For radiotherapists, the increasing use of SRS even to a poorer clinical outcome of the patients, as a total for patients with up to 10 BM increases the importance of of 197 metastases were not detected in conventional 3D precise pretherapeutic detection of all cerebral lesions in MPRAGE. Another advantage is the administration of one the MRI examination for radiation treatment planning [19, dose of MR contrast with a good signal-to-noise ratio of 3D 21]. The further clinical significance of using 3D SPACE SPACE even in the submillimeter range. The administration for radiation treatment planning on patient outcome and of three times as much gadolinium, as described by Don- quality of life after radiosurgery is currently being tested ahue et al. when using 1-mm thick MPRAGE sequences, in an ongoing two-armed prospective randomized phase II is not necessary with 3D SPACE [18]. The good spatial study at our center (Clinical Trial Code: NCT03303365). resolution allowed false-positive lesions such as cortical Funding No funding to declare. veins to be recognized and excluded from the radiation treatment planning [10]. Author Contribution TW initiated the project, was involved in the study design, analyzed the data and wrote the manuscript. RE, BN, Image acquisition for radiation treatment planning places DB, SR, JD contributed patient data and participated in reviewing of special demands on MRI. For radiation treatment planning the manuscript. All authors read and approved the final manuscript. for CyberKnife radiosurgery on the cranium in particular, slice thicknesses less than 1 mm are required with three-di- Funding Open Access funding enabled and organized by Projekt DEAL. mensional resolution and a good signal-to-noise ratio. This would not be possible with conventional 2D T1 spin echo Conflict of interest T. Welzel, R.A. El Shafie, B. v. Nettelbladt, sequences. In addition to good spatial resolution, low ge- D. Bernhardt, S. Rieken, and J. Debus declare that they have no competing interests. ometric distortion in the MR image is also important. The sharp delineation of the contrast enhancement of a metasta- Open Access This article is licensed under a Creative Commons At- sis in 3D SPACE allows precise determination of the target tribution 4.0 International License, which permits use, sharing, adapta- tion, distribution and reproduction in any medium or format, as long as volume with a steep dose gradient, while simultaneously you give appropriate credit to the original author(s) and the source, pro- protecting the surrounding brain tissue. For the radiothera- vide a link to the Creative Commons licence, and indicate if changes pist, detection and target volume contouring of small BM were made. The images or other third party material in this article are are considerably easier in 3D SPACE, as there is no inter- included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included ference from cortical veins. in the article’s Creative Commons licence and your intended use is not Our patients were treated between 2016 and 2018, at permitted by statutory regulation or exceeds the permitted use, you will a time when SRS of brain metastases was limited to up need to obtain permission directly from the copyright holder. To view to four brain metastases. Now it is not uncommon to treat a copy of this licence, visit http://creativecommons.org/licenses/by/4. 0/. up to 10 metastases or more [19]. Therefore, the change in treatment concept based on SPACE imaging needs to be considered in the current management of BM, as many References centers would still offer SRS for more brain lesions. We 1. 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Stereotactic radiotherapy of brain metastases: clinical impact of three-dimensional SPACE imaging for 3T-MRI-based treatment planning

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Abstract

Purpose For planning CyberKnife stereotactic radiosurgery (CK SRS) of brain metastases (BM), it is essential to precisely determine the exact number and location of BM in MRI. Recent MR studies suggest the superiority of contrast-enhanced 3D fast spin echo SPACE (sampling perfection with application-optimized contrast by using different flip angle evolutions) images over 3D gradient echo (GE) T1-weighted MPRAGE (magnetization-prepared rapid gradient echo) images for detecting small BM. The aim of this study is to test the usability of the SPACE sequence for MRI-based radiation treatment planning and its impact on changing treatment. Methods For MRI-based radiation treatment planning using 3T MRI in 199 patients with cerebral oligometastases, we compared the detectability of BM in post-gadolinium SPACE images, post-gadolinium MPRAGE images, and post-gadolin- ium late-phase MPRAGE images. Results When SPACE images were used for MRI-based radiation treatment planning, 29.8% and 16.9% more BM, respec- tively, were detected and included in treatment planning than in the post-gadolinium MPRAGE images and the post-gadolin- ium late-phase MPRAGE images (post-gadolinium MPRAGE imaging: n = 681, mean ± SD 3.4 ± 4.2; post-gadolinium total SPACE imaging: n = 884, mean ± SD 4.4 ± 6.0; post-gadolinium late-phase MPRAGE imaging: n = 796, mean ± SD total total 4.0 ± 5.3; P < 0.0001, P post-gadolinium SPACE imaging versus post-gadolinium MPRAGE imaging post-gadolinium SPACE imaging versus post-gadolinium late-phase MPRAGE imaging < 0.0001). Conclusion For 3T MRI-based treatment planning of stereotactic radiosurgery of BM, we recommend the use of post- gadolinium SPACE imaging rather than post-gadolinium MPRAGE imaging. Keywords Brain metastases · CyberKnife · Stereotactic radiosurgery · Variable flip angle · Magnetic resonance imaging Abbreviations GE Gradient echo BM Brain metastasis MPRAGE Magnetization-prepared rapid acquisi- CK CyberKnife tion of gradient echo CR Contrast rate MRI Magnetic resonance imaging Thomas Welzel, MD thomas.welzel@med.uni-heidelberg.de German Cancer Consortium (DKTK), Partner site Heidelberg, German Cancer Research Center (DKFZ), Heidelberg, Department of Radiation Oncology, Heidelberg University Germany Hospital, Im Neuenheimer Feld 400, 69120 Heidelberg, Department of Radiation Oncology, University Medical Germany Center Göttingen, Robert-Koch-Str. 40, 37075 Göttingen, Heidelberg Institute of Radiation Oncology (HIRO), Germany Heidelberg, Germany Department of Radiation Oncology, Klinikum rechts National Center for Tumor diseases (NCT), Heidelberg, der Isar, Technical University Munich, Ismaninger Germany Str. 22, 81675 Munich, Germany K Strahlenther Onkol (2022) 198:926–933 927 SE Spin echo the cortical vessels, the contrast enhancement of very small SPACE Sampling perfection with application- cerebral metastases is much clearer in 3D SPACE than in optimized contrast by using different 3D MPRAGE images. Kato et al. showed in an initial study flip angle evolutions with 16 patients with BM that 3D SPACE visualizes metas- SRS Stereotactic radiosurgery tases significantly better than 3D MPRAGE due to the better WBRT Whole-brain radiotherapy contrast rate (CR) [10]. The clinical significance of this fast (turbo) spin echo technique as black blood imaging for radiotherapy has not Introduction yet been studied. This clinical study aims to investigate whether 3D SPACE can be integrated in preradiotherapy Magnetic resonance imaging (MRI) is a safe and effective staging and radiation treatment planning. The objective of diagnostic examination technique for radiation treatment the study is to clarify how many more metastases are de- planning for cerebral metastases. The decision on the tected using 3D SPACE compared with 3D MPRAGE in ra- optimal radiotherapy for patients with cerebral oligometas- diation treatment planning and what effect the higher num- tases depends to a great extent on the number and lo- ber of metastases has on the later radiation technique (SRS cation of the metastases. While whole-brain radiotherapy versus WBRT). A metastasis count of ≤ 4 BM was specified (WBRT) is performed for diffuse metastasis, for oligometas- as the upper limit for SRS according to the guidelines from tases, stereotactic radiosurgery (SRS) is used to protect 2015 [13]. neurocognitive function [1–4]. In order to detect even the Several authors have reported that the lesion contrast smallest BM, the diagnostic accuracy of the MR examina- of BM increases with delayed imaging time [14, 15]. For tion technique is thus critical. departments that do not have access to black blood imag- In 2000, Hochstenbag et al. reported on the significance ing sequences such as 3D SPACE for radiation treatment of the MRI examination in pretherapeutic staging of BM planning, it should be tested whether a 3D MPRAGE late- [5]. Through the use of MRI alone, the number of newly phase contrast-enhanced image can detect the same number detected BM in SCLC patients increased by 15%. In this of metastases as 3D SPACE. study on a 0.5T MRI, only T1-weighted spin echo (SE) se- quences with a relatively large slice thicknesses of 10 mm Materials and methods were used. However, pulsation artifacts of the vessels in the posterior fossa result in poor image quality in stan- dard SE images. Metastases in the brainstem or cerebel- Patients lum can thus be missed. With the introduction of contrast- enhanced 3D GE T1-weighted MPRAGE (magnetization- All patients had an external diagnostic MRI examination prepared rapid gradient echo) images, Wenz et al. were and were referred to our CyberKnife (Accuray Inc. Sun- able to detect considerably more metastases in 1.5T MRI nyvale, CA, USA) center for SRS with suspected BM. than with SE sequences alone [6]. This was primarily due The study enrolled 214 consecutive patients with brain to the thinner slices. The superior spatial resolution of the oligometastases (no more than 4 lesions in diagnostic MRI, 3D GE sequences is associated with a greater susceptibility no extracranial metastases) who had an MRI for radiation for artifacts and poorer contrast compared with 2D SE se- planning for SRS between May 2016 and February 2018 at quences [7, 8]. With the introduction of new isotropic 3D the Department of Radiation Oncology and Radiation Ther- fast (turbo) spin echo sequences, it is today possible to de- apy at Heidelberg University Hospital. All patients were tect very small metastatic lesions (< 5 mm) in an acceptable older than 18 years and had no contraindication to an MRI examination time using 3.0T MRI. These sequences feature examination. The MRI data of 15 patients could not be eval- very long echo trains, lower flip angles, and ultrashort echo uated because of the absence of BM in MRI-based radia- spacing. Mugler et al. developed a 3D fast SE sequence tion treatment planning (MPRAGE and SPACE sequences; with variable flip angle refocusing pulses [9]. That which is n = 7 patients after chemotherapy) or had incomplete MRI termed the SPACE sequence solved the previous problems sequences due to poor general condition (n = 8 patients). of poor 3D resolution of gradient echo sequences using The patient characteristics of the remaining 199 patients sampling perfection with application-optimized contrast by are summarized in Table 1. using different flip angle evolutions. Due to the isotropic resolution, the voxels generated are the same size in every Magnetic resonance imaging direction, allowing reconstruction in all three planes. Vari- ous studies have reported on the diagnostic significance of MRI was carried out on a 3T scanner (Magnetom SKYRA , the SPACE sequence [10–12]. By suppressing the signal in Siemens Medical Systems, Erlangen, Germany) using K 928 Strahlenther Onkol (2022) 198:926–933 Table 1 Patient characteristics were diagnosed as cerebral metastases were included in the subsequent radiation treatment planning. For the contrast- All patients, no 199 enhanced MR sequences, the MPRAGE images were first Gender, no. (%) evaluated, then the SPACE images, and finally the post- Female 112 (56.3) gadolinium late-phase MPRAGE images. We measured the Male 87 (43.7) shorter diameter of each lesion in the axial plane of the Age, years MPRAGE and SPACE images. After this reviewing pro- Median (range) 62 (20–90) cess, an expert panel of radiation oncologists considered IQR 17 the scans again. The radiation therapy modality (SRS ver- Immunomodulating therapy, no. (%) sus WBRT) was selected at the discretion of the treating ra- No immunomodulating therapy 143 (71.9) diation oncologists, based on the number of lesions, lesion Immunomodulating therapy 56 (28.1) size, location of the lesions, and the patient’s performance Primary tumor type, no. (%) status. Lung 110 (55.3) The study protocol was approved by the local ethics com- Melanoma 29 (14.6) mittee. The study complies with the Helsinki Declaration, Breast 28 (14.1) the American Medical Association’s professional code of Renal cell carcinoma 13 (6.5) conduct, the principles of Good Clinical Practice guide- Cancer of unknown primary (CUP) 5 (2.5) lines, and the Federal Data Protection Act. Others 14 (7.0) Previous radiotherapy to the brain, no. (%) Statistical methods No SRS/WBRT 154 (77.4) SRS 26 (13.1) The paired-samples t-test was used to compare the mean WBRT 19 (9.5) number of BM on the standard MPRAGE sequence with IQR interquartile range, SRS stereotactic radiosurgery, WBRT whole- brain radiotherapy the mean number of metastases on the late-phase MPRAGE Percentages may not add up to 100 because of rounding and SPACE sequences. Spearman rank-order correlation co- efficients (r ) were computed to test for associations be- a transmit/receive quadrature four-channel head coil. All tween the number of metastatic lesions on the early-phase scans were carried out without immobilization devices for MPRAGE sequence and the number of additional metastatic use in treatment planning. The axial images were conducted lesions on the late-phase MPRAGE and SPACE sequences. without tilting in order to ensure a later fusion with CT All calculations were performed using SPSS version 27 examinations for radiation treatment planning. (IBM, Armonk, NY, USA) with p < 0.05 considered signif- The same imaging protocol was used in all patients and icant. was standardized for timing and sequence order: a three- dimensional high-resolution T1-weighted gradient echo se- quence (repetition time 2000 ms, echo time 2.44 ms, slice thickness 0.9 mm) for MPRAGE was carried out 2 min af- ter intravenous administration of 0.1 mmol/kg body weight Table 2 Brain metastases’ characteristics of gadobutrol (Gadovist, Bayer Schering Pharma, Berlin, Early-phase Late-phase SPACE Germany) with an additional saline flush of 30 ml. The MPRAGE MPRAGE imaging parameters for the SPACE were repetition time Total number 681 796 884 700 ms, echo time 12 ms, and slice thickness 1.0 mm. The Mean (SD) 3.4 (4.2) 4.0 (5.3) 4.4 (6.0) post-gadolinium late-phase MPRAGE images were made Median 2 (0–31) 2 (1–37) 2 (1–37) 10 min after contrast agent administration. (range) The MRI scans were reviewed by a specialized radi- IQR 33 4 ologist (TW) and a specialized radiation oncologist (SR) Grouping of patients by number of brain metastases, no. (%) with > 15 years extensive experience in cerebral MRI. All 03(1.5) 0 0 cerebral lesions were evaluated based on the criteria pub- 1–4 156 (78.4) 155 (77.9) 147 (73.9) lished by Kato et al. [10]. First, the normal structures with 5–10 27 (13.6) 29 (14.6) 36 (18.1) contrast enhancement such as cortical vessels were differ- > 10 13 (6.5) 15 (7.5) 16 (8.0) entiated from suspicious lesions. Of the suspicious cerebral IQR interquartile range, SD standard deviation, MPRAGE magneti- contrast-enhancing lesions, the lesions not suspicious for zation-prepared rapid acquisition of gradient echo, SPACE sampling metastasis (such as venous anomalies) were differentiated perfection with application-optimized contrast by using different flip from the lesions suspicious for metastasis. All lesions that angle evolutions K Strahlenther Onkol (2022) 198:926–933 929 Results five developmental venous anomalies (DVA). The mean numbers of BM on the 3D SPACE and 3D MPRAGE A summary of the BM characteristics is shown in Table 2. late-phase sequences were significantly higher than those Overall, we detected 29.8% more BM on the 3D SPACE found on the standard 3D MPRAGE sequences (p < 0.0001, sequences and 16.9% more BM on the 3D MPRAGE paired-samples t-test for both comparisons). Of note, le- late-phase sequences than on the established standard 3D sions of less than 2 mm in diameter on the 3D SPACE MPRAGE sequences. Incidental findings were detected in sequence were not seen in either the established standard 3% of the 199 patients and included one meningioma and 3D MPRAGE or the 3D MPRAGE late-phase sequence. Fig. 1 a MPRAGE post gadolinium: cystic metastasis in the right temporal lobe poorly differentiable from surrounding structures. b MPRAGE late post gadolinium: increasing contrast enhancement of the right temporal metastasis. c SPACE post gadolinium: metastasis clearly more differ- entiable from the cortical veins. d CyberKnife (Accuray Inc. Sunnyvale, CA, USA) treatment plan K 930 Strahlenther Onkol (2022) 198:926–933 Fig. 2 a MPRAGE post gadolin- ium: periventricular metastasis (arrow) poorly differentiable from periventricular vessels. b SPACE post gadolinium: sig- nificantly improved visualiza- tion of periventricular metastasis (arrow) due to signal suppres- sion of periventricular vessels Fig. 3 Correlation between the number of metastatic lesions Spearman's correlation r = 0.38 in the early-phase MPRAGE s 95% CI 0.05-0.64 sequence and the number of additional metastatic lesions 16 p = 0.015 in the late-phase MPRAGE sequence (a)and the SPACE sequence (b) 0 2 4 6 8 101214161820222426283032 Number of metastatic lesions early phase MPRAGE Spearman's correlation r = 0.49 95% CI 0.24-0.68 p < 0.001 0 2 4 6 8 101214161820222426283032 Number of metastatic lesions early phase MPRAGE Number of additional metastatic lesions Number of additional metastatic lesions SPACE late phase MPRAGE Strahlenther Onkol (2022) 198:926–933 931 Table 3 Numbers (and percentages) of patients, metastases, and SRS treatments by grouping the patients with 0–4 metastases in the early-phase MPRAGE sequence according to the presence or absence of additional metastases on the SPACE and late-phase MPRAGE sequences Patients Metastases Decision for SRS SRS performed based on SPACE imag- ing Detection of metastatic Early- Late- SPACE Number of Patients Metastases Patients Metastases lesions relative to early- phase phase additional de- (%) (%) (%) (%) phase MPRAGE imaging MPRAGE MPRAGE tected metas- tases Additional metastases on 16 35 35 54 SPACE: +19 12 (75.0) 33 (61.1) 11 27 SPACE imaging Late-phase (91.7) (81.8) MPRAGE: +0 Additional metastases 18 35 71 86 SPACE: +51 10 (55.6) 28 (32.6) 9 23 on SPACE ± late-phase Late-phase (90.0) (82.1) MPRAGE imaging MPRAGE: +36 No additional metastases 125 230 230 230 SPACE: +0 125 230 121 221 on SPACE + late-phase Late-phase (100) (100) (96.8) (96.1) MPRAGE imaging MPRAGE: +0 MPRAGE magnetization-prepared rapid acquisition of gradient echo, SPACE sampling perfection with application-optimized contrast by using different flip angle evolutions Metastatic lesions near the cortical vessels (Fig. 1c) and 10 patients, so these patients were given a recommendation periventricular metastases (Fig. 2b) were particularly well for SRS from the tumor board. SRS was carried out in a to- detected by the 3D SPACE sequence. tal of 9 patients. One patient with only one brain metastasis At the patient level, the 3D SPACE sequence showed could not be treated with SRS because he could not tolerate 57.8% more metastatic lesions than the standard 3D prolonged immobilization during treatment. He was given MPRAGE sequence in 60 of the 199 patients (554 ver- WBRT with boost for this metastasis (details are shown sus 351 metastases in 30.2% of the patients), and the 3D in Table 3). Summarizing the two oligometastatic groups, MPRAGE late-phase sequence detected 39.1% more le- a total of 20 oligometastatic patients were given SRS for sions than the standard 3D MPRAGE sequence in 41 of the additional metastases detected solely on the basis of the 199 patients (409 versus 294 metastases in 20.6% of SPACE. the patients). The higher the number of BM detected in the standard 3D MPRAGE sequence, the higher the number of additional metastases in the 3D MPRAGE late-phase Discussion sequence (for details see Fig. 3). Several studies have shown that black blood (BB) MRI Modification of radiotherapy based on SPACE (SPACE, VISTA) detects significantly more brain lesions findings <5mm [10, 16, 17]. This study showed for the first time that BB imaging (SPACE) can be effectively integrated In this study, 80% of the patients (n = 159) had cerebral into stereotactic radiation treatment planning with the Cy- oligometastases with between 0 and 4 BM. In a total of 125 berKnife. Among the multifactorial causes for the supe- oligometastatic patients in whom the standard early-phase rior detectability of BM using SPACE are the better sig- MPRAGE showed 0–4 metastases, no additional metastases nal-to-noise ratio and the higher spatial resolution in the were found in the late-phase MPRAGE and SPACE scans. submillimeter range. The sequence is clearly superior to The SPACE scan alone detected 19 additional metastases in MPRAGE in detecting smaller short-axis diameters and 16 oligometastatic patients, so SRS treatment was indicated thus also smaller metastases. However, false-positive find- for 12 patients. In 11 patients, these additional metastases ings due to insufficient suppression of cortical vessels or could be irradiated using SRS. For one patient, the radi- small contrast enhancement of an immunological inflam- ation treatment planning MRI showed additional calvarial matory response due to antibody treatment can be misinter- metastases, so WBRT was carried out. preted to be a metastasis. In 18 oligometastatic patients, more metastases were In the late-phase MPRAGE imaging, cerebral metastases found simultaneously in the late-phase MPRAGE (n = 36) show contrast blush as an expression of neovascularization and in the SPACE (n = 51) scans than in the standard early- compared with early-phase MPRAGE imaging (Fig. 1b). In phase MPRAGE scan. In this patient group, the SPACE scan addition, washout of the contrast agent was seen in the cere- showed more metastases than the late-phase MPRAGE in bral vessels in late-phase MPRAGE imaging (Fig. 1b). This K 932 Strahlenther Onkol (2022) 198:926–933 facilitates better differentiation of the intracerebral vessels Conclusion from metastases in late-phase MPRAGE imaging as well. The 3D SPACE image showed more intracerebral metas- Using 3D SPACE is a practical alternative to the routinely tases and, above all, smaller metastases in MRI-based used T1-weighted 3D MPRAGE, especially for radio- radiation treatment planning compared with conventional surgery treatment planning for BM. Our data show that 3D MPRAGE. These metastases would not have been 3D SPACE allows detection of significantly more cerebral included in radiation treatment if only contrast-enhanced metastases that can be included in radiation treatment plan- 3D MPRAGE had been used. This would have led later ning. For radiotherapists, the increasing use of SRS even to a poorer clinical outcome of the patients, as a total for patients with up to 10 BM increases the importance of of 197 metastases were not detected in conventional 3D precise pretherapeutic detection of all cerebral lesions in MPRAGE. Another advantage is the administration of one the MRI examination for radiation treatment planning [19, dose of MR contrast with a good signal-to-noise ratio of 3D 21]. The further clinical significance of using 3D SPACE SPACE even in the submillimeter range. The administration for radiation treatment planning on patient outcome and of three times as much gadolinium, as described by Don- quality of life after radiosurgery is currently being tested ahue et al. when using 1-mm thick MPRAGE sequences, in an ongoing two-armed prospective randomized phase II is not necessary with 3D SPACE [18]. The good spatial study at our center (Clinical Trial Code: NCT03303365). resolution allowed false-positive lesions such as cortical Funding No funding to declare. veins to be recognized and excluded from the radiation treatment planning [10]. Author Contribution TW initiated the project, was involved in the study design, analyzed the data and wrote the manuscript. RE, BN, Image acquisition for radiation treatment planning places DB, SR, JD contributed patient data and participated in reviewing of special demands on MRI. For radiation treatment planning the manuscript. All authors read and approved the final manuscript. for CyberKnife radiosurgery on the cranium in particular, slice thicknesses less than 1 mm are required with three-di- Funding Open Access funding enabled and organized by Projekt DEAL. mensional resolution and a good signal-to-noise ratio. This would not be possible with conventional 2D T1 spin echo Conflict of interest T. Welzel, R.A. El Shafie, B. v. Nettelbladt, sequences. In addition to good spatial resolution, low ge- D. Bernhardt, S. Rieken, and J. Debus declare that they have no competing interests. ometric distortion in the MR image is also important. The sharp delineation of the contrast enhancement of a metasta- Open Access This article is licensed under a Creative Commons At- sis in 3D SPACE allows precise determination of the target tribution 4.0 International License, which permits use, sharing, adapta- tion, distribution and reproduction in any medium or format, as long as volume with a steep dose gradient, while simultaneously you give appropriate credit to the original author(s) and the source, pro- protecting the surrounding brain tissue. For the radiothera- vide a link to the Creative Commons licence, and indicate if changes pist, detection and target volume contouring of small BM were made. The images or other third party material in this article are are considerably easier in 3D SPACE, as there is no inter- included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included ference from cortical veins. in the article’s Creative Commons licence and your intended use is not Our patients were treated between 2016 and 2018, at permitted by statutory regulation or exceeds the permitted use, you will a time when SRS of brain metastases was limited to up need to obtain permission directly from the copyright holder. To view to four brain metastases. Now it is not uncommon to treat a copy of this licence, visit http://creativecommons.org/licenses/by/4. 0/. up to 10 metastases or more [19]. Therefore, the change in treatment concept based on SPACE imaging needs to be considered in the current management of BM, as many References centers would still offer SRS for more brain lesions. We 1. 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Journal

Strahlentherapie und Onkologie – Springer Journals

Published: Oct 1, 2022

Keywords: Brain metastases; CyberKnife; Stereotactic radiosurgery; Variable flip angle; Magnetic resonance imaging

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