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Clinical Applications of Arterial Spin Labeling in Brain Tumors

Abdel Razek, Ahmed Abdel Khalek MD*; Talaat, Mona MD; El-Serougy, Lamiaa MD*; Gaballa, Gada MD*; Abdelsalam, Mohamed MD

Journal of Computer Assisted Tomography: July/August 2019 - Volume 43 - Issue 4 - p 525–532
doi: 10.1097/RCT.0000000000000873
Neuroradiology
Free

The aim of this review was to review the basic background, technique, and clinical applications of arterial spin labeling in brain tumors. Arterial spin labeling is used for differentiation of brain tumors from nonneoplastic lesions such as infarction and infection. It has a role in the grading of gliomas and in the differentiation of gliomas from lymphomas and metastasis. It is used for detection of the best biopsy site and prediction of treatment response. Arterial spin labeling is used for the assessment of extra-axial tumors and pediatric tumors. Last, it has a role in the differentiation of tumor recurrence from postradiation changes and in monitoring patients after therapy.

From the *Department of Diagnostic Radiology, Faculty of Medicine, Mansoura University, Mansoura;

Department of Diagnostic Radiology, Faculty of Medicine, Kafr Elsheikh University, Kafr Elsheikh; and

Department of Neurology, Faculty of Medicine, Mansoura University, Mansoura, Egypt.

Received for publication February 20, 2019; accepted February 21, 2019.

Correspondence to: Ahmed Abdel Khalek Abdel Razek, MD, Department of Diagnostic Radiology, Faculty of Medicine, University of Mansoura, Elgomheryia St, Mansoura 13551, DK, Egypt (e-mail: arazek@mans.edu.eg).

The authors declare no conflict of interest.

Online date: June 3, 2019

Brain tumors are encountered difficulties at imaging. Imaging is essential for diagnosis, grading of brain tumors, and evaluating tumor response after therapy.1–3 Conventional magnetic resonance imaging (MRI) replies on morphology, location, mass effect, and multiplicity with some limitation in the differentiation of brain tumors from simulating lesions, characterization of brain tumors, grading of gliomas, and differentiation of recurrent tumor from tissue necrosis.2–5 Perfusion is an emerging MR technique that describes dynamic delivery of blood to body tissues. Two main perfusion MR methods were developed either with or without an exogenous contrast agent administration. The first group of techniques involves dynamic susceptibility contrast MRI and dynamic contrast-enhanced MRI, whereas the second one corresponds to arterial spin labeling (ASL). Dynamic susceptibility contrast perfusion MRI depends on T2* weighting effect as gadolinium reduces T2* signal in the tissue according to its local concentration. Dynamic contrast-enhanced perfusion MRI is the other exogenous contrast-based method. After the bolus of the contrast agent is injected, signal relays the T1 relaxation time and increases because of the T1 shortening effect accompanied with the paramagnetic contrast agent used.6–8 Arterial spin labeling is an emerging noninvasive MRI perfusion technique. It has no exogenous administration of contrast agents; instead, it depends on magnetically labeled blood water protons as an endogenous tracer.9–12

The aim of this work was to highlight the clinical applications of ASL in brain tumors.

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BASIC BACKGROUND

Physical Principle of ASL

Arterial spin labeling is one of the recent MRI methods used for evaluating blood flow and uses electromagnetically labeled arterial blood water as a freely diffusible inner tracer.9–11 Blood contains a large number of water molecules, which mix with tissue water molecules at the capillary exchange site. If the blood water could be distinguished from the tissue water, it would be possible to estimate several hemodynamic parameters like blood flow (perfusion), blood volume, and exchange parameters (eg, permeability of vessel wall).12,13

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Technique of ASL

Data Acquisition

Radiofrequency pulses are applied to the blood water proximal to the tissue to be examined. The magnetization of inflowing blood water protons is inverted in this area. A delay time is allowed (1.5–2 seconds) whereby the radiofrequency (RF)–labeled blood water protons travel to the brain tissue and exchange with tissue water. After a period of time (postlabeling delay), blood labeled with an inverted signal is delivered to the whole brain through the capillaries and smaller arteries.10–12 There are 2 phases during ASL imaging: the preparation phase, in which inflowing blood protons are labeled by inverting their spin polarity, and the acquisition phase, in which perfusion-weighted images are acquired. By alternating acquisition of labeled and control images, which only differ in the magnetized state of arterial blood protons, paired label-control images are obtained.12,13

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Arterial Spin Labeling Methods

Different methods are used for labeling arterial water protons, including pulsed ASL (PASL), continuous ASL, pseudocontinuous ASL (pCASL), and velocity-selective ASL methods. In PASL, a thick slab (10–15 cm) of tissue containing arterial water molecules is inverted proximal to the imaging slice at a single time point using short RF pulses, yet it has lower signal-to-noise ratio.14–16 In continuous ASL, a constant gradient and RF pulse are applied in the direction of flow, yet there is lower inversion efficiency. The most commonly used ASL sequence is pCASL and is thought to have the best performance. Contrary to the previously mentioned ASL labeling methods, velocity-selective ASL saturates arterial water molecules based on velocity rather than spatial location.7Table 1 shows the recommended protocol for ASL in brain tumors by the authors.

TABLE 1

TABLE 1

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Arterial Spin Labeling Postprocessing

The postprocessing of arterial spin-tagging data typically involves initially subtraction of alternating tag and control image pairs, motion correction, and generation of ASL grayscale and colored map. Regions of interest are manually placed within the high signal area and immediate surrounding edema (within a 1-cm distance from the outer margin of the high signal part) on ASL grayscale map. Region of interest sizes in both regions are similar to each other. Necrotic tissue and large vessels were avoided by comparison with other conventional MR images.1,2

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Arterial Spin Labeling analysis

Qualitative (visual assessment): The visual inspection of signal intensity on ASL perfusion maps (both grayscale and color-coded maps) compared with signal of the normal tissue and is given a score (from 0 to 3).

Semiquantitative: Measuring normalized tumor blood flow (TBF); regions of interest are manually drawn (considering similar region of interest size) in an area with the maximum signal with the tumor and normal tissue (contralateral white matter or cerebellum) on ASL TBF map.

Quantitative: Arterial spin labeling perfusion imaging is an absolute quantitative technique and considered as a useful tool in the study of normal brain function. Absolute TBF is calculated by certain equation assumptions.9–12

where CBF is the cerebral blood flow, ΔM(TI2) is the mean difference in the signal intensity between the label and control images, M0, blood is the equilibrium magnetization of blood, α is the tagging efficiency, TI1 is the time duration of the tagging bolus, TI2 is the inversion time of each section, T1, blood is the longitudinal relaxation time of blood, and qp is a correction factor that accounts for the difference between the T1 of blood and the T1 of brain tissue.1–3

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Clinical Applications of ASL in Brain Tumors

Table 2 shows the clinical applications of ASL in brain tumors.

TABLE 2

TABLE 2

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I–Differentiation of Neoplastic From Nonneoplastic Lesions

Cystic Gliomas Versus Brain Abscess

In some cases, it may be difficult to differentiate brain abscesses from necrotic glioblastomas and cystic metastases based on conventional MRI as both entities can appear as rim-enhancing lesions with perifocal edema. The enhancing margins of abscesses typically demonstrate lower TBF than those of cystic glioblastomas (Fig. 1) and metastases at ASL.9–12

FIGURE 1

FIGURE 1

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Low-Grade Gliomas Versus Infarction

Ischemia is identifiable by regions of altered perfusion due to anoxic damage resulting in infarction. Arterial spin labeling can confirm the presence of regional hypoperfusion in acute ischemia, thus ruling out stroke mimics such as low-grade gliomas.13–16

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High-Grade Gliomas Versus Tumefactive Demyelinating Diseases

Tumefactive demyelinating lesions with atypical features can mimic high-grade gliomas on conventional MRI. The ASL is proposed as a diagnostic tool in the differentiation between both entities. There is a reduction of TBF measured by ASL in tumefactive demyelinating disease, whereas high-grade glial tumors show increased TBF, and so, we can differentiate between both entities noninvasively.12–15

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II–Grading of Gliomas

Low-Grade Versus High-Grade Gliomas

Grading of gliomas is important for prognosis and planning of treatment strategies.17–19 The TBF values are an important noninvasive and fast parameter that helps in the grading of gliomas. Arterial spin labeling gives absolute values for tumors which based on tissue perfusion not the contrast enhancement itself with high parameters noted in higher-grade tumors. Parameters from ASL perfusion imaging, particularly normalized maximum TBF, may be useful for distinguishing high-grade from low-grade astrocytoma in patients with equivocal conventional MRI. Several studies have demonstrated that TBF-derived ASL can discriminate low- from high-grade astroglial tumors based on low-grade tumors (Fig. 2) displaying higher CBF than high-grade tumors (Fig. 3). Arterial spin labeling may allow detection of nonenhancing glioblastoma. Nonenhancing high-grade astrocytoma exhibits significantly greater absolute maximum and mean TBF than low-grade gliomas.20 A meta-analysis study reported that there is significant difference in maximum, mean absolute TBF, and maximum mean relative TBF between high- and low-grade gliomas.21 There is a positive correlation between TBF-derived ASL and microvessel density of gliomas, which is a marker of tumor growth and grade.22,23 Arterial spin labeling perfusion shows potential in the differentiation of isocitrate dehydrogenase mutation status and α thalassemia/mental retardation syndrome X-linked gene expression mutation status of gliomas.24

FIGURE 2

FIGURE 2

FIGURE 3

FIGURE 3

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Grade II Versus Grade III Gliomas

Only 1 study discussed the role of ASL in differentiating grade II from grade III gliomas. This study reported that normalized TBF-derived ASL shows excellent performance in grading of gliomas with area under receiver operating characteristic curves of 0.813 (grade II vs. III), 0.964 (grade II vs. IV), and 0.872 (grade III vs. IV). Combined normalized TBF-derived ASL and normalized bolus arrival time improved accuracy to 72% compared with the normalized TBF. Combined normalized TBF-derived ASL and conventional MRI have the best performance, with an accuracy of 81.40%.25

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III–Characterization of Brain Tumors

Gliomas Versus Metastasis

Discriminating glioblastomas from solitary brain metastasis using conventional MR is still considered an important unsolved problem. However, it is clinically important to differentiate between them because these 2 entities differ from each other in clinical course and management. Metastasis reveals variable blood flow (Fig. 4), those usually lower than that of a high-grade primary tumor. The peritumoral regions of glioblastomas reveal an increase in the TBF due to tumor infiltration and associated neoangiogenesis. In contrast, in metastatic tumors, the peritumoral region represents edematous brain parenchyma. Studies showed that glioblastomas exhibited higher TBF values based on ASL perfusion MRI using both qualitative and quantitative approaches. Both intratumoral and peritumoral perfusion on ASL can aid in the differentiation of glioblastomas from brain metastasis. The TBF gradient in the peritumoral edema region appears to be a more promising ASL perfusion metrics in differentiating high-grade glioma from solitary metastasis.26,27

FIGURE 4

FIGURE 4

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Gliomas Versus Lymphoma

Because the management of primary central nervous system lymphoma (PCNSL) and glioblastoma is different, an early and accurate diagnosis is the key to improving prognosis. Primary central nervous system lymphomas are generally treated with chemotherapy and whole-brain radiotherapy; on the other hand, patients with glioblastomas are commonly treated with gross surgical resection followed by chemoradiotherapy. Conventional MRI may show overlapping imaging features. A study using the PASL technique reported that quantitatively measured intratumoral blood flow is significantly lower in PCNSL than in glioblastoma. Other studies showed that the normalized TBF peritumoral value of PCNSL is significantly lower than that of glioblastoma. It demonstrated better diagnostic performance [area under the curve (AUC) = 0.90] than normalized TBF intratumoral. This is attributed to that neovascularization in glioblastomas, which is known to be pronounced in contrary to PCNSL.28–30 Another study added that the TBF of PCNSL (26.41 ± 4.03 mL/100 g/min) was significantly lower than that of glioblastoma (51.08 ± 3.9 mL/100 g/min; P = 0.001).31

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Hemangioblastomas Versus Metastasis

Hemangioblastomas and metastasis are the most common cerebellar masses in adults. Hemangioblastomas are benign tumors of vascular origin. Discriminating between both is important because their therapeutic approaches and prognosis are quite different. In addition, hemangioblastomas are associated with good survival rate than brain metastasis. The use of ASL perfusion imaging in the evaluation of the vascularity of brain tumors has been explored in a few studies. It was reported that absolute TBF is significantly higher in hemangioblastomas (TBF = 437 ± 274 mL/100 g/min) than in metastasis (TBF = 125 ± 134 mL/100 g/min).32,33

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IV–Pretreatment Evaluation

Infiltration and Extent of Brain Tumors

Tumor infiltration assessment is crucial for presurgical planning and safety margin consideration. Arterial spin labeling provides a roadmap for evaluating tumor infiltration along different vascular channels that determine radiotherapy and drug delivery effectiveness.11–15

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Targeting Site of Biopsy

Tissue biopsy is considered the most accurate for the diagnosis and grading of brain tumors; yet, the highest grade portion of the tumor might not be sampled, thus undergrading the tumor. Tumor angiogenesis is a key factor in histologic tumor grading, and TBF serves as an in vivo marker of the tumor angiogenic characteristic that can be evaluated with ASL.15,34

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Prediction of Treatment Response

Early prediction of treatment response and identification of tumor progression are important because these improve treatment strategy by determining whether to continue the current therapy or change treatment for nonresponsive disease. Studies showed that ASL is capable of predicting tumor response as early as 6 weeks after treatment, with improved accuracy over tumor volume measurements. Perfusion of high-grade tumors can be measured with ASL before and after treatment to assess response and progression.11–17

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V–Posttreatment Evaluation

Residual/Recurrent Tumor Versus Posttreatment Changes

Arterial spin labeling is used for the evaluation of recurrent tumor after therapy in different regions of the body.35–37 Distinguishing tumor recurrence from treatment necrosis is very important and challenging for proper diagnosis and treatment planning. Assessment of treatment response by routine MRI alone is not adequate due to decreased specificity. In ASL, tumor recurrence (Fig. 5) is associated with neoangiogenesis that appears as regions of hyperperfusion with higher blood flow and volume. Treatment necrosis, on the contrary, is associated with regions of reduced perfusion (Fig. 6) due to treatment-induced vascular endothelial damage and coagulative necrosis.38–40

FIGURE 5

FIGURE 5

FIGURE 6

FIGURE 6

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Pseudoprogression of Tumor

Pseudoprogression is defined as an increase in enhancement and/or edema on MRI without tumor progression during radiotherapy and antiangiogenic drugs. These transient changes are stabilized or resolved without change in management. Pseudoprogression occurs in 15% to 50% of patients with gliomas undergoing standard therapy.41,42 One study reported that ASL grade is an independent predictor differentiating pseudoprogression from early tumor progression with an odds ratio of 4.73.41 Another study added that the perfusion fraction within the contrast-enhancing lesion at ASL is significantly higher (P = 0.03) in the nonprogression group compared with the progression group.42 Another study added that for the prediction of pseudoprogression of tumor, the CBF value of 0.995 has 100% sensitivity and 73.7% specificity, and a value 1.02 has 92.3% sensitivity and 92.9% specificity (AUC = 0.967; P = 0.001).43

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Monitoring Treatment Response

During follow-up of tumor, perfusion MRI could also be a surrogate marker for treatment response, particularly with the development of antiangiogenic drugs. Arterial spin labeling can be used for monitoring treatment response of gliomas after therapy.42 On qualitative analysis, ASL perfusion map is more accurate than dynamic susceptibility contrast perfusion in differentiation pseudoprogression from early tumor progression (odds ratio, 4.73; P = 0.0017).41 Arterial spin labeling shows significant differences between progression and pseudoprogression of glioma. The regional tumor blood flow value of 1.02 has 92.3% sensitivity and 92.9% specificity (AUC = 0.967; P = 0.001).43

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VII–Extra-Axial Neoplasms

Meningioma

Meningiomas are the most common extra-axial brain tumors that often show “light bulb bright” of high blood flow with ASL (Fig. 7), which would be valuable for differentiating meningioma from other extra-axial lesions such as nerve sheath tumors, which do not show robust blood flow. In addition, ASL improves reader sensitivity for detecting multiple meningiomas.44–49

FIGURE 7

FIGURE 7

The World Health Organization classifies meningiomas into 3 histological grades. Differentiation of aggressive meningiomas (World Health Organization grade II/III meningiomas) from nonaggressive grade I meningiomas is important before deciding the suitable treatment plan to improve the patient's prognosis. Arterial spin labeling shows 3 perfusion patterns of meningiomas. Both pattern 1 and pattern 2 were characterized by the presence of hyperperfusion in the tumor tissue, which appears as bright areas in TBF maps. Pattern 1 shows a homogenous hyperperfusion compared with pattern 2, whereas pattern 3 shows absence of hyperperfused tumor tissues. Another study revealed that the peritumoral TBF value, rather than the tumoral TBF value, from pCASL imaging may serve as a key factor in discriminating different grades of meningiomas. Some studies suggest increased TBF is associated with higher tumor grade in meningioma.44–51 Territorial ASL also complements unenhanced time-of-flight MR angiography and increases accuracy in the identification of the feeding arteries of meningiomas. The information about feeding arteries is very crucial for neurosurgeons in planning surgery as well as in evaluating prognosis.47,49,51

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Schwannoma

Arterial spin labeling perfusion helps in the differential diagnosis between cerebellopontine angle schwannoma and meningioma without the use of contrast medium. Arterial spin labeling can be used to adequately evaluate tumor perfusion even if the tumors are located in the skull base. The median TBF of meningiomas (168.0 mL/100 g/min) is significantly higher (P = 0.001) than schwannomas (35.68 mL/100 g/min).52

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Pituitary Adenoma

Two studies discuss the role of ASL in pituitary adenomas. One study reported that pituitary adenomas depend on angiogenesis for growth. Differences in vascular density of pituitary adenomas may help in predicting tumor aggressiveness and vascular complications such as bleeding associated with a trans-sphenoidal operation. Arterial spin labeling can reflect the vascular density of nonfunctioning pituitary macroadenomas, which helps in preoperative prediction of intra- and postoperative tumor hemorrhage.53 Another study added that TBF measured by ASL shows reduced size and growth hormone secretions of growth hormone–producing pituitary adenoma after therapy with antiangiogenic effect of octreotide.54 Another study added that the median TBF of meningiomas (172.95 mL/100 g/min) of the suprasellar region is significantly higher (P = 0.001) than that of pituitary adenoma (34.57 mL/100 g/min).52

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VIII–Pediatric Brain Tumors

Characterization

Pilocytic astrocytomas are characterized by low TBF due to the microvascular architecture or integrity or vessel density. Optic pathway glioma is of slightly lower perfusion than other pilocytic astrocytomas. Medulloblastomas show higher perfusion compared with pilocytic astrocytoma. Medulloblastoma shows higher blood flow than ependymoma. Medulloblastomas with increased TBF indicated more aggressive behavior and early death from time of diagnosis.1,2 The TBF of hemangioblastomas is extremely high in children, which is helpful in differentiating hemangioblastoma from pilocytic astrocytoma.55

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Grading

There is high perfusion of pediatric high-grade tumors at ASL that correlates well with increased microvascular density. High-grade tumors show both high vascular density and high TBF. Therefore, measurement of TBF is clinically useful for predicting the tumor grade.56,57 Another study added that there was a wider rTBF range among high-grade tumors (2.14 ± 1.78) compared with low-grade tumors (0.60 ± 0.29) (P = 0.001).55 The rTBF of low-grade gliomas (0.81 ± 0.56) is significantly lower than that of high-grade gliomas (2.08 ± 0.98).57

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Posttreatment

One study that discussed brain perfusion abnormalities in children treated for posterior fossa brain tumors revealed that global CBF decreased in pediatric patients with treated medulloblastoma but not pilocytic astrocytoma, suggesting that the perfusion changes are a consequence of adjuvant therapy or underlying tumor biology rather than surgical treatment.58 Another study that discussed the response of diffuse infiltrating pontine gliomas to radiotherapy reported that cerebral blood volume increases after radiotherapy, and higher values are correlated with better progressive-free survival. High cerebral blood volume values after radiotherapy should not be mistaken for progression and could be an indicator of response to therapy. The median rTBF value increased from 1.094 to 1.992 (P = 0.001). The rTBF increases after radiotherapy, and higher values are correlated with better patient progression-free survival59

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Merits and Limitations

Merits of ASL

The merits of ASL are noninvasiveness, nonionizing radiation, no contrast medium injection, repeated safely, and able to give quantitative values. These merits make ASL much more suitable for perfusion studies in healthy individuals, repetitive follow-ups, patients with renal insufficiency, and pediatric populations.9–12 In addition, multiparametric MRI of ASL with other noninvasive MR sequences such as diffusion tensor imaging60–62 and proton MR spectroscopy63,64 at higher three-tesla65,66 machine increased the diagnostic performance of ASL in the assessment of brain tumors.67

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Limitations of ASL

The limitations of ASL include low signal-to-noise ratio of TBF maps and the potential for systematic measurement errors due to prolonged transit delay between the tagging region and the imaging slice, dependence of measured relaxation on the exchange of water between intra- and extravascular compartments, and clearance of unextracted water by outflow in the venous system. In addition, ASL may be associated with some artifacts such as susceptibility artifact, motion artifact, gadolinium-based contrast agent effect, and paradoxical hyperperfusion.55,67 There is variation of thresholds for various parameters based on different techniques used and vendor machine. Small differences in sequence parameters have an effect on the reproducibility of ASL that limits the clinical and research applications of ASL. Further studies to standardize ASL parameters of different vendors are recommended.68

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Conclusion

We concluded that ASL is essential for the differentiation of brain tumors from simulating lesions, characterization of brain tumors, grading of brain tumors, pretreatment assessment, and posttreatment evaluation and discrimination of tumor recurrence from posttreatment changes.

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Keywords:

perfusion; magnetic resonance imaging; glioma; recurrence

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