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Malignant Supratentorial Astrocytoma Treated with Postoperative Radiation Therapy: Prognostic Value of Pretreatment Quantitative Diffusion-weighted MR Imaging¹

¹ From the Departments of Radiation Oncology (R.M., Y.B., N.O.), Diagnostic Radiology (T.H., M.K., Y.H., Y.B., Y.Y.), and Neurosurgery (H.N., J.i.K.), Kumamoto University Hospital, 1-1-1 Honjo, Kumamoto 860-8556, Japan; and Department of Radiology, Kumamoto Red Cross Hospital, Kumamoto, Japan (T.S.). Received March 12, 2006; revision requested May 9; revision received May 20; accepted June 19; final version accepted September 1. Address correspondence to R.M. (e-mail: murakami{at}kaiju.medic.kumamoto-u.ac.jp).

	ABSTRACT

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Purpose: To retrospectively evaluate whether the minimum apparent diffusion coefficient (ADC) of the tumor seen on pretreatment magnetic resonance (MR) images is of prognostic value in patients with malignant supratentorial astrocytoma.

Materials and Methods: The study was approved by the institutional review board; the requirement for informed patient consent was waived. Between June 1996 and November 2003, 79 patients (44 male, 35 female; age range, 16–76 years) with malignant supratentorial astrocytoma underwent pretreatment MR imaging. Patient age, symptom duration, neurologic function, mental status, Karnofsky performance scale (KPS) score, extent of surgery, histopathologic diagnosis, tumor component enhancement, and minimum ADC were assessed at factor analysis of survival. Radiation Therapy Oncology Group–recursive partitioning analysis (RTOG-RPA) criteria were used to validate the prognostic value of the minimum ADC. Kaplan-Meier survival curves, the log-rank test, and the multivariate Cox proportional hazards model were used to evaluate the prognostic factors.

Results: Twenty-nine patients had anaplastic astrocytoma, and 50 had glioblastoma multiforme. The minimum ADC was significantly lower in patients with glioblastoma multiforme than in those with anaplastic astrocytoma (P < .001). The two-year survival rates associated with low (1.0 x 10^–3 mm²/sec) and high (>1.0 x 10^–3 mm²/sec) minimum ADCs were 14% (six of 42 patients) and 84% (31 of 37 patients), respectively (P < .001). The minimum ADC was the most important prognostic factor (hazard ratio = 10.459; 95% confidence interval: 5.113, 21.396) and could be used to assign patients to different prognostic groups in each RTOG-RPA class.

Conclusion: The minimum ADC at pretreatment MR imaging is a useful clinical prognostic biomarker for survival in patients with malignant supratentorial astrocytoma.

© RSNA, 2007

	INTRODUCTION

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Malignant astrocytoma is the most common primary neoplasm of the central nervous system (1–3). Despite improvements in treatment, most patients die of this disease. The median survival is approximately 3 years for patients with anaplastic astrocytoma (AA) and 1 year for those with glioblastoma multiforme (GBM) (1–7).

Although conventional magnetic resonance (MR) imaging, such as T2-weighted and contrast material–enhanced T1-weighted imaging, provides information about the gross anatomic structure of malignant astrocytomas, it rarely yields functional information (8). Diffusion-weighted MR imaging enables volumetric intravoxel measurement of tissue characteristics that is based on the detection of a change in the random motion of water protons at the cellular or physiologic level. It has been widely used to evaluate acute cerebral ischemia (9). Although the usefulness of diffusion-weighted imaging for preoperative grading and postoperative assessment of glial tumors has been investigated, its value for prognosticating survival has not been fully addressed (10–15). Because the apparent diffusion coefficient (ADC) should be inversely related to tumor cellularity and glioma grade, we postulated that areas with the minimum ADC reflect the sites of highest cellularity within heterogeneous tumors and that these sites may be important for diagnosis and prognosis. Thus, the purpose of our study was to retrospectively evaluate whether the minimum ADC of the tumor seen on pretreatment MR images is of prognostic value in patients with malignant supratentorial astrocytoma.

	MATERIALS AND METHODS

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Prior written informed consent for the routine clinical course of MR examinations and treatments was obtained from all patients. This retrospective study was approved by the institutional review board of our hospital (Kumamoto University Hospital), and the requirement for informed patient consent was waived. In addition, to protect patient privacy, we removed all identifiers from our records at the completion of our analyses.

Patients, Diagnosis, and Treatment
Between 1996 and 2003, we administered postoperative radiation therapy in conjunction with chemotherapy to 133 patients with newly diagnosed malignant supratentorial gliomas. Seventy-nine of these patients (44 male, 35 female; age range, 16–76 years; mean age, 52 years) had malignant supratentorial astrocytoma and fulfilled our inclusion criteria: (a) histopathologic diagnosis of AA (grade 3) or GBM (grade 4) based on World Health Organization criteria, (b) absence of other previous or concurrent malignant diseases, (c) availability of digital pretreatment MR imaging data, including diffusion-weighted images, for review, (d) solid tumor components present and available for ADC analysis, and (e) absence of gross blood products or infratentorial tumor components obstructive to ADC analysis (9,16). We excluded 54 patients owing to the following conditions: histopathologically identified oligodendroglial components (n = 24), unavailability of digital pretreatment diffusion-weighted MR data (n = 25), and MR evidence of intratumoral hemorrhage (n = 5).

Two authors (R.M., Y.H.) reviewed the patients' medical records to obtain information about them and their treatments. The surgical option—resection or biopsy—was chosen by neurosurgeons (J.i.K., H.N.) on the basis of tumor location and the patient's performance status. The tumor was resected to the greatest extent possible in all patients. Histopathologic diagnoses were based on World Health Organization criteria and were reached by consensus between two neuropathologists (J.i.K., H.N., with 25 and 15 years experience, respectively) who were blinded to the MR imaging information. All 79 patients underwent postoperative external-beam radiation therapy. Our protocol for the treatment of malignant astrocytoma consists of 60 Gy of radiation for patients with GBM and 54 Gy for patients with AA, administered by using conventional fractionation—that is, 2 Gy daily for 5 consecutive days—in conjunction with three-dimensional conformal treatment planning. Nitrosourea-based chemotherapy was administered concurrently with radiation therapy.

Patients were followed up for evaluation of tumor control after postoperative radiation therapy. Follow-up evaluation included physical and neurologic examinations and MR imaging. If tumor recurrence or progression was documented, salvage surgery, additional radiation therapy, and/or additional chemotherapy was considered.

MR Examinations and Image Interpretation
All MR examinations were performed with a 1.5-T superconducting imaging unit (Magnetom Vision; Siemens, Erlangen, Germany). Conventional MR images—including T1-weighted (627–670/14–17 [repetition time msec/echo time msec]), T2-weighted (3600/96; echo train length, seven), and contrast-enhanced (gadopentetate dimeglumine, Magnevist; Nihon Schering, Osaka, Japan) T1-weighted (627–670/14–17) images—and diffusion-weighted images were obtained during the same examination. Diffusion-weighted images were acquired in the transverse plane by using a spin-echo echo-planar sequence with diffusion gradient encoding in three orthogonal directions. The additional time required for diffusion-weighted imaging was less than 3 minutes. The parameters used to obtain diffusion-weighted images were 4700/123–139, a 220-mm field of view, a 128 x 128 pixel matrix, 5-mm section thickness, a 1-mm intersection gap, one acquisition, and a b value of 1000 sec/mm². Diffusion-weighted imaging was performed before contrast-enhanced T1-weighted imaging.

ADC values were calculated according to the formula ADC = –[ln(S_b/S₀)]/b, where S_b is the signal intensity of the region of interest obtained through three orthogonally oriented diffusion-weighted images or diffusion trace images, S₀ is the signal intensity of the region of interest acquired through reference T2-weighted images, and b is the gradient b factor with a value of 1000 sec/mm². ADC maps were calculated on a pixel-by-pixel basis by using built-in software on the MR unit.

The solid tumor components with or without contrast enhancement on both conventional MR and diffusion-weighted images were retrospectively identified in consensus between two neuroradiologists (T.H., M.K., with 16 and 15 years experience in brain MR imaging, respectively) who were blinded to the clinical and histopathologic information. We measured ADCs by manually placing five to 10 40–60-mm² regions of interest within solid tumor components on the ADC maps. The regions of interest were carefully placed to avoid volume averaging with cystic and/or necrotic areas that influence ADC values (15). Minimum ADC values were selected for analysis.

Statistical Analyses
To evaluate the relationship between minimum ADC and glioma grade, we compared the minimum ADC values in different histopathologically diagnosed gliomas (AA vs GBM) by using the unpaired Student t test. Survival was measured from the time of pretreatment MR examination to the time of death or last follow-up. The duration of follow-up ranged from 2 to 108 months (median, 20 months). Surviving patients were followed up for more than 2 years. To determine the relationship between minimum ADC and patient survival, the minimum ADC values were compared with the survival times. Furthermore, we compared survival curves on the basis of histopathologic diagnosis of tumor and minimum ADC.

We analyzed the relationship between patient survival and the prognostic factors determined from clinical and MR imaging information. Prognostic factors included patient age (49 vs 50 years), duration of symptoms (3 vs >3 months), neurologic function (able to work vs confined to home or hospitalized), mental status (normal vs abnormal), Karnofsky performance scale (KPS) score (80 vs 90–100), extent of surgery (biopsy vs partial or total resection), histopathologic diagnosis (AA vs GBM), enhancement of tumor components (present vs absent), and minimum ADC (1.0 x 10^–3 mm²/sec vs >1.0 x 10^–3 mm²/sec). We also used the Radiation Therapy Oncology Group–recursive partitioning analysis (RTOG-RPA) criteria to validate the prognostic value of the minimum ADC (5). Survival curves were calculated by using the Kaplan-Meier method; overall differences in the survival curves were analyzed with the log-rank test. The multivariate Cox proportional hazards model was used to adjust for the influence of prognostic factors. The statistical analyses were performed by using computer software (StatView, version 5.0; SAS Institute, Cary, NC). For all analyses, P < .05 was considered to denote a significant difference.

	RESULTS

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Patient, Imaging, and Treatment Characteristics
There were 29 AAs and 50 GBMs. KPS scores were as follows: score of 40 in three, score of 50 in seven, score of 60 in four, score of 70 in 12, score of 80 in 17, score of 90 in 19, and score of 100 in 17 patients. Surgery consisted of biopsy (n = 23) and either partial (n = 31) or total (n = 25) resection. Stratification by RTOG-RPA criteria revealed that 17, five, seven, 20, 25, and five patients belonged to classes I, II, III, IV, V, and VI, respectively (Fig 1). On the conventional MR images, 49 of the 50 GBMs and 12 of the 29 AAs showed enhancing components. The minimum ADC values of all tumors ranged from 0.543 to 2.024 (mean, 1.071 x 10^–3 mm²/sec ± 0.348 [standard deviation]). The mean minimum ADC was significantly lower in patients with GBM (0.897 x 10^–3 mm²/sec ± 0.217) than in those with AA (1.371 x 10^–3 mm²/sec ± 0.327, P < .001).

View larger version (18K): [in this window] [in a new window] [Download PPT slide]   Figure 1: Flow chart of 79 malignant astrocytomas outlined according to RTOG-RPA classification (I–VI). NF = neurologic function, RT = radiation therapy.

View larger version (9K): [in this window] [in a new window] [Download PPT slide]   Figure 2: Graph illustrates relationship between minimum ADC and survival time, as measured from the date of pretreatment MR imaging, in all patients, including 25 alive subjects. The patients who died within 1 year had tumors with a minimum ADC lower than 1.0 x 10–3 mm2/sec. = patients with AA who survived, = patients with AA who died, = patients with GBM who survived, = patients with GBM who died.

View larger version (11K): [in this window] [in a new window] [Download PPT slide]   Figure 3: Survival curves based on histopathologic diagnosis (AA vs GBM) and minimum ADC (1.0 x 10–3 mm2/sec vs >1.0 x 10–3 mm2/sec). = patients with AA and high minimum ADC (>1.0 x 10–3 mm2/sec), = patients with AA and low minimum ADC (1.0 x 10–3 mm2/sec), = patients with GBM and high minimum ADC, = patients with GBM and low minimum ADC.

View larger version (154K): [in this window] [in a new window] [Download PPT slide]   Figure 4: Transverse MR images obtained in 53-year-old man with GBM (RTOG-RPA class V). A, T2-weighted (3700/96), and, B, contrast-enhanced T1-weighted (627/17) images show an enhancing tumor with a cystic component and peritumor edema. C, On DW image (5378/139), the enhancing area has moderately high signal intensity. D, On ADC map, the enhancing area (arrow) has a minimum ADC of 1.2103 x 10–3 mm2/sec. This patient survived for 44 months after the initial MR examination.

View larger version (165K): [in this window] [in a new window] [Download PPT slide]   Figure 5: Transverse MR images obtained in 52-year-old man with GBM (RTOG-RPA class IV). A, T2-weighted (3600/96), and, B, contrast-enhanced T1-weighted (627/17) images show an enhancing tumor with a cystic component. C, On DW image (5378/139), the enhancing area has high signal intensity. D, On ADC map, the enhancing area (arrow) has a minimum ADC of 0.6635 x 10–3 mm2/sec. This patient died 16 months after the initial MR examination.

	DISCUSSION

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Conventional MR imaging, such as T2-weighted and contrast-enhanced T1-weighted examinations, has an important role in the assessment of the gross anatomic structure of tumors. High-grade gliomas are usually enhanced, and the enhancing areas are considered the regions of gross tumor extension. However, the absence of enhancement does not necessarily imply a histopathologic diagnosis of low-grade tumor: One-third of nonenhancing diffuse gliomas in adults are high-grade tumors (8). Furthermore, because some low-grade gliomas show abnormal enhancement, the contrast-enhanced region does not necessarily represent the portion that is most relevant in terms of tumor grade and extension.

Diffusion-weighted imaging reveals the microscopic structure of a tumor at the cellular or physiologic level—for example, cell density and necrotic cell clusters—and therefore yields indirect information about the aggressiveness of the tumor. Diffusion-weighted imaging and the quantitative parameter of this examination, the ADC, can be used to characterize highly cellular versus acellular regions. Tissues with high cellularity have a low ADC because the mobility of water protons is impeded. Cystic regions, on the other hand, have a high ADC owing to the rapid diffusion of water protons (17,18). In tumors, the ADC is usually highest in cystic or necrotic areas and then in solid tumor components (13). Low-grade gliomas tend to have a higher ADC compared with high-grade gliomas. This higher ADC may reflect an increase in the water content of the interstitial spaces (10–12,15). The ADC value should be inversely related to tumor cellularity and glioma grade. Yamasaki et al (10) suggested inverse relationships between mean ADC and astrocytic tumors of World Health Organization grades 2–4. Our study also revealed that minimum ADC values are substantially higher in patients with AA (World Health Organization grade 3) than in those with GBM (World Health Organization grade 4).

When determining the tumor diagnosis and the patient prognosis, one needs to take into account the most aggressive part of the tumor, from not only a pathologic perspective but also an imaging perspective. Oh et al (14) evaluated the mean ADCs of GBMs seen on MR images obtained after surgery but before the start of radiation therapy and found that the patients with low ADCs had substantially shorter survivals. We found the minimum ADC of the tumor seen at pretreatment MR imaging to be a useful prognosticator of the survival of patients with malignant astrocytoma. The observation that a low ADC is associated with a poor prognosis is consistent with previous study results suggesting that the higher the World Health Organization grade of astrocytic tumor, the lower the ADC (10). However, Lam et al (13), who evaluated the ADCs of the enhanced, nonenhanced, and cystic components of gliomas, concluded that there were no substantial differences in mean ADC between the components of low-grade gliomas and the components of high-grade gliomas. We suggest that the areas exhibiting the minimum ADC are the sites of highest glioma grade within heterogeneous tumors and are thus the important sites for diagnosis and prognosis.

When combined with conventional MR imaging, diffusion-weighted imaging can yield additional useful information about morphologic and physiologic changes. Diffusion-weighted imaging enables assessment of the entire tumor, whereas tissue sampling is invasive and may not yield information about the entire tumor. The choice of a suboptimal biopsy site may result in inaccurate glioma grading because these tumors are histologically heterogeneous (1,2). Because diffusion-weighted imaging facilitates identification of the areas of highest cellularity within a tumor, it is helpful in selecting the biopsy targets with the highest informational yield. Furthermore, diffusion-weighted imaging may help in selecting appropriate treatment strategies: AAs with components that have a low minimum ADC may be associated with a poor prognosis and may require the same aggressive treatment that GBMs require.

In terms of limitations, diffusion-weighted imaging does not eliminate the perfusion effects caused by tumor vascularity or preserved myelin tracts. In addition, ADC changes due to the presence of cystic, necrotic, and/or hemorrhagic areas and the influence of artifacts caused by inhomogeneous structures such as the skull base bone and sinus air must be considered (9,16). To avoid the influence of susceptibility artifacts or ADC changes, we excluded lesions with infratentorial components or gross hemorrhage from our study. Although the results of our retrospective study show that the minimum ADC is one of the most important prognostic factors, other variables related to the patient, tumor, and treatment must be considered because malignant astrocytomas are heterogeneous. In our study patients, the KPS score was also an independent factor.

In conclusion, the minimum ADC of the tumor seen on pretreatment MR images is a useful clinical prognostic biomarker for survival in patients with malignant supratentorial astrocytoma. Patients who have tumors with a low minimum ADC (1.0 x 10^–3 mm²/sec) may have a poor prognosis. Thus, pretreatment diffusion-weighted MR imaging may be helpful in the treatment of patients with malignant astrocytoma.

	ADVANCE IN KNOWLEDGE

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• The apparent diffusion coefficient (ADC) of the tumor seen on pretreatment MR images is of prognostic value in terms of survival for patients with malignant astrocytoma; patients who have tumors with a low minimum ADC tend to have a poor prognosis.
  

	FOOTNOTES

 

Abbreviations: AA = anaplastic astrocytoma • ADC = apparent diffusion coefficient • GBM = glioblastoma multiforme • KPS = Karnofsky performance scale • RTOG-RPA = Radiation Therapy Oncology Group–recursive partitioning analysis

Authors stated no financial relationship to disclose.

Author contributions: Guarantor of integrity of entire study, R.M.; study concepts/study design or data acquisition or data analysis/interpretation, all authors; manuscript drafting or manuscript revision for important intellectual content, all authors; manuscript final version approval, all authors; literature research, R.M., T.S., H.N., T.H.; clinical studies, R.M., H.N., T.H., M.K., Y.H., Y.B.; statistical analysis, R.M., Y.B.; and manuscript editing, T.S., T.H., N.O., J.i.K., Y.Y.

	References

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This Article Abstract Figures Only Full Text (PDF) All Versions of this Article: 2432060450v1 243/2/493    most recent Submit a response Alert me when this article is cited Alert me when eLetters are posted Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Murakami, R. Articles by Yamashita, Y. Search for Related Content PubMed PubMed Citation Articles by Murakami, R. Articles by Yamashita, Y.