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British Journal of Radiology (2005) 78, 230-235
© 2005 British Institute of Radiology
doi: 10.1259/bjr/28534346
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Treatment outcomes and prognostic factors in patients with supratentorial low-grade gliomas

S-A Yeh, MD 1 J-T Ho, MD 2 C-C Lui, MD 3 Y-J Huang, MD 1 C-Y Hsiung, MD 1 and E-Y Huang, MD 1

Department of 1 Radiation Oncology, 2 Neurosurgery and 3 Radiology, Chang Gung Memorial Hospital, Kaohsiung, Taiwan

Correspondence: Dr Shyh-An Yeh, 5F., No.181, Wen-Chuan Road, Zuoying District, Kaohsiung City 81361, Taiwan (R.O.C.)


   Abstract
Top
 Abstract
Introduction
 Material and methods
 Results
 Discussion
 Conclusions
 References
 
Low-grade gliomas account for 10–15% of all adult primary intracranial tumours. Currently, there is no consensus on the treatment strategy for low-grade gliomas. This study was designed to evaluate the treatment outcomes, prognostic factors and radiation-related late complications, as well as to assess whether or not post-operative radiotherapy has benefit on local control and overall survival in this population. We retrospectively reviewed 93 consecutive adult patients with supratentorial low-grade gliomas diagnosed at our institution from July 1985 to December 1997. All patients underwent surgical intervention and 60 of them received post-operative radiotherapy. With a median follow-up of 110 months for surviving patients, the 5-year overall and progression-free survival rates were 57% and 47%, respectively. 46 patients experienced local progression of disease during the follow-up period. In multivariate analysis, age at diagnosis, extent of surgery and post-operative Karnofsky performance status showed independent prognostic significance for progression-free and overall survival rates. Post-operative radiotherapy had independent prognostic value for progression-free survival. This analysis has changed our practice and we suggest that aggressive surgical resection and post-operative radiotherapy might be considered for patients with low-grade gliomas. Further efforts should be made to optimize radiotherapy techniques and to integrate new therapeutic modalities.


   Introduction
Top
 Abstract
 Introduction
Material and methods
 Results
 Discussion
 Conclusions
 References
 
Supratentorial low-grade glioma is a heterogeneous group of brain tumours, accounting for roughly 10–15% of all adult primary intracranial tumours [1]. Because of the relatively slow growth rate of low-grade gliomas, a long expected survival is not unreasonable. Surgical resection or observation alone is the mainstay of treatment. Where the tumours involve critical functional regions of the brain, complete removal would be dangerous and is not feasible. Even with grossly total removal, the infiltrative feature of gliomas often leaves behind some microscopic tumours. The microscopic residual tumours might increase the incidence of local relapse and allow adjuvant therapy to play a role in the management of low-grade gliomas.

This analysis was undertaken to investigate the treatment outcomes of patients with supratentorial low-grade gliomas. Treatment options and potential prognostic factors were evaluated to substantiate their relationship to progression-free survival (PFS) and overall survival. Radiation-related complications were surveyed. These results might contribute to treatment recommendations and exploration of avenues of further research.


   Material and methods
Top
 Abstract
 Introduction
 Material and methods
Results
 Discussion
 Conclusions
 References
 
From July 1985 to December 1997, 93 consecutive adult patients with supratentorial low-grade gliomas were treated at our hospital. All patients underwent surgical intervention (grossly total resection in 13 patients, subtotal resection (removal of 20~80% of tumour) in 71, biopsy in 9. Tumours were classified according to the World Health Organization grading system [2]. There were grade II astrocytoma in 46 patients, grade II oligodendroglioma in 32 patients and mixed oligoastrocytoma in 15 patients. Only patients who were operated on for the first time were included. The post-operative performance status was assessed using the Karnofsky performance scale (KPS) [3]. Because residual tumours were often found in patients whose operative records mentioned total removal of tumours, the extent of surgery was determined by review of both the operative records and the serial CT scans (pre-operative and post-operative). Data were analysed retrospectively by reviewing the medical records and radiographic images, by telephone or written correspondence and by review of the death certificate. Surveillance for disease status consisted of physical examination and serial radiographic studies. Only patients with definite tumour regrowth on consecutive CT scans were defined as having progression of disease. There were 57 men and 36 women; age range from 18 years to 80 years (median 41 years). The most common locations of tumours was the frontal lobe (69%), followed by the temporal lobe (37%). The most common presenting symptoms were seizure (46%), followed by increased intracranial pressure (headache, nausea, vomiting; 34%). The characteristics of these patients were given in the Table 1Go.


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  		Table 1. Clinical characteristics of 93 patients with low-grade gliomas

 
Radiotherapy
60 patients received post-operative radiotherapy. The median interval between surgical resection and initiation of radiotherapy was 0.9 months (range 0.1–2 months). The prescribed tumour dose ranged from 56 Gy to 70 Gy (median 60 Gy) with daily fractions of 2 Gy, 5 fractions per week. 21 patients received whole brain irradiation (40–46 Gy) followed by focal boost irradiation (total 58–70 Gy). 39 patients received only focal brain irradiation to a total of 56–70 Gy. Radiotherapy was delivered with 10-MV photons through individually shaped, bilateral opposed portals. Focal irradiation fields included the pre-operative tumour volume (contrast-enhanced area or low-attenuation area for non-enhanced tumours) with a 2 cm margin. Evaluation of treatment response was based on the serial changes in neuroradiographic studies. Radiation-related late complications were gauged with SOMA scale [4].

Statistics
The endpoints of this study were overall survival, PFS and radiation-related late complications. Survival was measured from the date of histopathological diagnosis, as was time to tumour progression. Surviving patients were censored at the date of last physician contact. The date of the imaging procedure documenting tumour progression was used to calculate PFS rates. The survival data were analysed using the Kaplan-Meier method [5]. Differences between potentially prognostic subgroups were tested for statistical significance by the log-rank test, with p<0.05 indicating significance [6]. All statistically significant prognostic variables in univariate analysis were considered in the multivariate analysis. Multivariate analysis was performed with the Cox regression model to identify independent prognostic factors [7].


   Results
Top
 Abstract
 Introduction
 Material and methods
 Results
Discussion
 Conclusions
 References
 
The 5-year overall survival and PFS rates were 57% and 47%, respectively. At the time of this retrospective review, 43 patients were alive with a median follow-up of 110 months (range 50–197 months). In terms of overall survival rates, the age at diagnosis, histology, local progression, post-operative radiotherapy, post-operative KPS, extent of surgery and duration of symptoms were identified as significant prognostic factors. Patients undergoing grossly total surgical resection survived longer than those where resection was incomplete (5-year overall survival rate: 92% vs 52%, p=0.0349). In multivariate analysis, the age at diagnosis, post-operative KPS and extent of surgery continued to show independent prognostic significance for overall survival rates.

When PFS rate was considered, univariate analysis showed that age at diagnosis, histology, post-operative radiotherapy, post-operative KPS, extent of surgery and duration of symptoms had prognostic significance. Patients receiving post-operative radiotherapy had a 5-year PFS rate of 56% as compared with 30% for those with surgery alone (p=0.0028, Figure 1Go). Multivariate analysis confirmed that age at diagnosis, post-operative radiotherapy, post-operative KPS and extent of surgery were independent prognostic factors for PFS rates. The details of univariate and multivariate analysis are listed in Tables 2 and 3GoGo.



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  		Figure 1. Progression-free survival according to post-operative radiotherapy (RT) status.

 

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  		Table 2. Prognostic factors for 5-year overall and progression-free survival

 

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  		Table 3. Multivariate analysis data

 
For patients treated with post-operative radiotherapy, the survival rates of patients receiving 62–70 Gy were not significantly different from the corresponding rates of those receiving 56–60 Gy (5-year overall survival rates: 60% vs 70%, p>0.05; 5-year PFS rates: 51% vs 59%, p>0.05). No correlation was found between whole brain irradiation and survival rates. The 5-year overall survival and PFS rates were 70%, 56% for patients without whole brain irradiation and 61%, 57% for those with whole brain irradiation (p>0.05).

Local progression
There was local progression in 46 patients. The interval between surgical intervention and the development of local progression ranged from 4 months to 135 months (median 22 months). For patients who had previously undergone gross total surgical resection, all of the tumour recurrences developed in the immediate vicinity of the primary tumours. Salvage treatment included surgery alone in 11 patients, radiotherapy alone in 8 patients and a combination of surgery and radiotherapy in 12 patients. 15 patients did not receive any salvage treatment. Among the 23 patients receiving salvage surgery, malignant dedifferentiation was noted in 9 patients (39%). The 5-year overall survival rate after disease progression was 39% for patients receiving salvage treatment (surgery and/or radiotherapy), and 0% for patients refusing or unable to receive salvage treatment (p=0.0003). According to subgroups of different salvage treatment modalities, the 5-year overall survival rates after disease progression were 40%, 37.5% and 42% for patients receiving a combination of surgery and radiotherapy, radiotherapy alone and surgery alone, respectively (p>0.05).

Complications
In this article, 23 patients suffered from somnolence during the follow-up period (grade I: 3, grade II: 20) and the 5-year complication-free rate was 74% for all patients. Patients receiving post-operative radiotherapy had a 5-year complication-free rate (for somnolence) of 72% compared with 77.5% for those who did not have radiotherapy (p>0.05). 16 patients had memory impairment (grade I: 5, grade II: 11) and the 5-year complication-free rate was 83% for all patients. Patients treated with post-operative radiotherapy had a higher incidence of memory impairment than those with surgery alone (5-year complication-free rate: 75% vs 96%, p=0.0268). Among patients receiving post-operative radiotherapy, a radiation dose of 62–70 Gy was not associated with higher incidence of somnolence and memory impairment compared with a radiation dose of 56–60 Gy (5-year complication-free rate, for somnolence: 71% vs 73%, p>0.05; for memory impairment: 78% vs 73%, p>0.05). Among those not initially presenting with seizure, seven patients developed seizures (grade II: 7) and the 5-year complication-free rate was 92% for all patients. CT scans of these patients were carefully reviewed to exclude the possible association with tumour progression or recurrence. Patients with post-operative radiotherapy had a 5-year complication-free rate (for seizure) of 95% compared with 86% for patients after surgery alone (p>0.05). Among patients receiving post-operative radiotherapy, whole brain irradiation was associated with a higher incidence of somnolence and memory impairment, but the differences did not reach statistical significance (5-year complication-free rate, for somnolence: 64% vs 76%, p>0.05; for memory impairment: 70% vs 78%, p>0.05). Two patients had radiation-related low-density white matter changes with irregular enhancement revealed by CT scans. No significant neurological deficits could be attributed to the white matter changes.


   Discussion
Top
 Abstract
 Introduction
 Material and methods
 Results
 Discussion
Conclusions
 References
 
In this article, the 5-year overall survival and PFS rates were 57% and 47%, respectively. Our treatment results were in agreement with the reported experience [8–12]. The goal of surgery is to provide a histological diagnosis, relieve symptoms, reduce the tumour burden as much as possible, and guide further treatment. Owing to the infiltrative growth pattern of gliomas, it is difficult to achieve complete removal without producing or exacerbating neurological deficits. Conflicting results regarding the prognostic significance of the extent of surgery have been reported in the literature. There were articles demonstrating that the extent of surgery was an important prognostic factor for survival and local control [8, 13–19]. On the other hand, some investigators reported that the extent of surgery was not correlated with the survival rates of patients with low-grade gliomas [11, 12, 20]. According to our results, the extent of surgery was correlated to PFS and overall survival rates. Therefore, we suggest that a radical surgery should be attempted unless the surgical resection will create significant neurological sequelae.

The influence of histological subtypes on survival was controversial. There were reports that oligodendroglioma was associated with better treatment outcomes [16, 19, 21, 22]. On the other hand, some physicians indicated that if tumours fit the histological criteria of low-grade gliomas, further subdivision might not greatly increase the prognostic value of the histological diagnosis [20, 23]. Our univariate analysis showed that oligodendroglioma was associated with significantly higher overall survival and PFS rates compared with astrocytoma. However, multivariate analysis failed to show an independent prognostic significance of histological subtypes.

The optimal treatment strategy of low-grade gliomas is uncertain. Controversy regarding the indication of post-operative radiotherapy continues to exist. Some investigators suggested that when a complete removal was achieved, no further adjuvant therapy was warranted [24]. On the other hand, Shaw [25] suggested that post-operative radiotherapy should be routinely delivered to all adult patients with histologically verified supratentorial low-grade non-pilocytic gliomas. Several retrospective series demonstrated that post-operative radiotherapy had survival benefit for those who underwent subtotal removal of tumours [15, 21, 24, 26, 27]. Another major uncertainty is the optimal timing of post-operative radiotherapy. Radiotherapy deferred until tumour progression was found to be associated with a longer survival or a trend toward improved survival on univariate analysis, but was not significant in multivariate analysis [16, 23]. Some investigators suggested that radiotherapy could be deferred until tumour progression in young patients despite the extent of surgery [8]. Furthermore, several reports demonstrated that early post-operative radiotherapy had no survival benefit [8, 28–30]. However, there were reports claiming that immediate post-operative radiotherapy could improve overall survival or local control for most patients with low-grade gliomas [11, 15, 25, 27, 31–33]. In our study, patients receiving post-operative radiotherapy had higher overall survival and PFS rates than those with surgery alone regardless of the extent of surgery. Multivariate analysis also showed the independent prognostic significance of post-operative radiotherapy for PFS, but not for overall survival. Our results were in accord with the reported experience [33].

For patients receiving post-operative radiotherapy, the optimal radiation dose has yet to be determined. Some publications indicated the existence of a dose–response relationship for low-grade gliomas [26, 32]. On the other hand, several articles including a large prospective randomized study demonstrated that no clear dose–response relationship could be observed [9, 11, 20, 21]. We also could not demonstrate a dose–response effect of radiotherapy in this study.

The optimal irradiated volume is another important issue that might influence the treatment outcomes. Prior analysis of failure patterns of patients with low-grade gliomas showed that most failures occurred within the irradiated fields [21, 34]. Whole brain irradiation has been reported to have no survival benefit over partial brain irradiation [32]. Furthermore, whole brain irradiation has been considered to be associated with greater morbidity [25]. Our study failed to demonstrate any survival benefit for whole brain irradiation over partial brain irradiation. We also found that there was a trend for patients with whole brain irradiation to have higher incidence of late complications; although this trend did not reach statistical significance. Because prolonged survival could be expected in patients with low-grade gliomas, the irradiated volume should be limited to the pre-operative tumour site (contrast-enhanced area or low-attenuation area for non-enhanced tumours) and multiple conformally shaped treatment fields should be used with the aim of reducing the late complications. Whole brain irradiation is no longer recommended. In general, MRI is more precise and sensitive in brain tumour detection and could offer a greater accuracy in tumour delineation and treatment field determination. MRI or multimodality image fusion (CT and MRI) might be used in the treatment planning process. The advent of intensity-modulated radiotherapy might allow a further reduction in the irradiated volume and radiation dose to normal brain.

Our study revealed that the administration of post-operative radiotherapy was an independent prognostic factor for predicting tumour progression. Patients who had post-operative radiotherapy had a higher incidence of mild memory impairment than those after surgery alone. The radiation-related late complications were limited to grade II of the SOMA scale. These results might further constitute the rationale for the use of adjuvant post-operative radiotherapy. We do not recommend deferring radiotherapy until tumour progression or recurrence. Where tumour progression or recurrence occurs, brain tissue damage due to the tumour itself is unavoidable. Salvage surgery might also remove or damage some normal brain tissue and further compromise the neurological function and quality of life. On the other hand, if the patient undergoes radiotherapy after the first surgical intervention, the incidence of tumour progression or recurrence is significantly decreased at the cost of only a slightly higher incidence of radiation-related neurotoxicities. Based on the above results, we recommend that application of post-operative radiotherapy might be considered for all patients with low-grade gliomas regardless of the extent of surgery and the histological subtypes. The role of radiotherapy should not be only limited to serve as a salvage therapy for local progression or recurrence. For patients who will receive post-operative radiotherapy, we suggest partial brain irradiation to a dose not more than 60 Gy.

The importance of age as a determinant of survival has been demonstrated in the literature; the younger the patients, the better the prognosis [8, 12, 14–20, 23, 29, 30]. In this article, patients younger than 40 years had significantly higher overall survival and PFS rates than those older than 40 years. Multivariate analysis further confirmed the independent prognostic significance of age on overall survival and PFS rates. A long duration of symptoms prior to surgery had been shown to be associated with longer survival in patients with low-grade gliomas [15]. In this study, the median duration of symptoms before histological diagnosis was 1 month and it had significant impact on overall survival and PFS; the longer the duration, the better the prognosis. The possible explanation was that a protracted duration of symptoms was associated with less aggressive tumour behaviour. However, there was no independent prognostic significance in multivariate analysis.

For patients suffering from tumour progression, the optimal management is unclear. In our study, patients undergoing salvage treatment had a significantly better prognosis than those without salvage treatment. In this study, there was a trend for salvage surgery to provide better long-term survival after disease progression. However, the independent prognostic significance of salvage surgery needs to be proved by further studies.

Malignant dedifferentiation has been noted in patients undergoing salvage surgery for progressive or recurrent diseases. In the literature, the reported dedifferentiation rate of low-grade gliomas ranged from 45% to 86% [10, 18, 20, 29]. The gemistocytic variant is known to be particularly prone to malignant progression [35]. It is conceivable that radiotherapy might initiate or accelerate malignant transformation [36]. Among the 23 patients who had salvage surgery in our study, malignant transformation was noted in nine patients. Four of these patients received post-operative radiotherapy. Eight patients had astrocytoma and one had oligodendroglioma. The dedifferentiation rate was 39%. Due to small case numbers, no factors were found to be associated with the occurrence of malignant dedifferentiation.


   Conclusions
Top
 Abstract
 Introduction
 Material and methods
 Results
 Discussion
 Conclusions
References
 
Based on our results, we recommend that aggressive surgical resection followed by post-operative radiotherapy should be considered for patients with supratentorial low-grade gliomas. The potential survival benefit and dose–response relationship of post-operative radiotherapy for low-grade gliomas need further prospective randomized studies. The treatment strategy for low-grade gliomas is evolving and a multidisciplinary approach is advocated.

Received for publication July 2, 2004. Revision received October 11, 2004. Accepted for publication November 23, 2004.


   References
Top
 Abstract
 Introduction
 Material and methods
 Results
 Discussion
 Conclusions
 References
 

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