Research ArticleClinical Studies
Open Access

The Predictive Value of Different Glasgow Prognostic Scores and the LabBM Score for Patients With Recurrent Glioblastoma

DIRK RADES, OKSANA ZEMSKOVA, JAN LEPPERT and NATHAN Y. YU
Anticancer Research September 2024, 44 (9) 3973-3981; DOI: https://doi.org/10.21873/anticanres.17226

Abstract

Background/Aim: The prognostic value of scoring instruments was described for newly diagnosed glioblastoma. This study investigated five instruments in patients with recurrent tumors. Patients and Methods: Original Glasgow Prognostic Score (oGPS), modified GPS (mGPS), high-sensitivity mGPS (HS-mGPS), high-sensitivity oGPS (HS-oGPS), LabBM score, and 10 other factors were analyzed for progression-free survival (PFS) and overall survival (OS) in 51 patients. Results: On univariate analyses, oGPS 0-1, mGPS 0-1, and LabBM score 0-1.0 were significantly associated with improved OS and showed trends for improved PFS. On multivariate analysis, a trend was found for associations between LabBM score 0-1.0 and better OS. In addition, maximal cumulative diameter ≤40 mm and systemic therapy were independently associated with better PFS and OS, resection with PFS, and in-field recurrence with OS. Conclusion: Lower oGPS, mGPS, and LabBM scores were significantly associated with improved OS on univariate analyses. These instruments may be helpful when designing personalized treatment regimens for patients with recurrent glioblastoma.

Key Words:

Many patients treated with multimodal therapy for newly diagnosed glioblastoma develop an intracerebral recurrence, a considerable number of them even after a comparably short period of time, i.e., within twelve months (1, 2).

Recurrent glioblastomas are often associated with poor prognoses. Therefore, these patients could benefit from personalized treatment approaches considering the patient’s personal situation, preferences, and estimated overall survival (OS) time. Estimation of OS time can be improved by employment of prognostic factors and scoring instruments. For patients with recurrent glioblastoma, some clinical and treatment-associated factors were previously identified as prognostic factors of OS (3-14). In addition to these predictors, pre-clinical markers and scoring instruments may contribute to optimal treatment personalization for this patient group. Scoring instruments suitable for estimating the OS of patients with recurrent glioblastoma may include different versions of the Glasgow Prognostic Score (GPS), namely the original GPS (oGPS), the modified GPS (mGPS), the high-sensitivity mGPS (HS-mGPS), and the high-sensitivity oGPS (HS-oGPS), which all consider C-reactive protein (CRP) and albumin, and the LabBM score (15-19). The oGPS and mGPS use cut-off values of 10 mg/l for CRP and 35 g/l for albumin, HS-mGPS and HS-oGPS cut-off values of 3 mg/l for CRP and 35 g/l for albumin (15-18). Each GPS version includes three groups, i.e., 0, 1, or 2 points. The LabBM score is based on CRP, albumin, hemoglobin, platelet count, and lactate dehydrogenase (LDH); scores range between 0 and 3.5 points (19).

The five scoring instruments were recently investigated in patients receiving multimodal therapy consisting of resection or biopsy followed by radio-chemotherapy and subsequent maintenance chemotherapy for newly diagnosed glioblastoma (18). In that retrospective study, better OS was significantly associated with lower oGPS on multivariate analysis. In addition, trends were found for associations between better OS and lower mGPS and between better PFS and lower LabBM score (18). Moreover, in a retrospective study from 2018, the oGPS was suggested to be a useful tool to estimate the OS of patients receiving multimodal therapy for newly diagnosed glioblastoma (20). In another retrospective study, mGPS was identified as independent predictor of OS in patients with recurrent high-grade gliomas including glioblastoma and grade III anaplastic glioma (21). Since the data regarding the prognostic role of different versions of the GPS and the LabBM score in patients with newly diagnosed or recurrent glioblastoma are very scarce, additional studies are required. The present study investigated the predictive value of the five scoring instruments mentioned above with respect to OS and progression-free survival (PFS) in patients with recurrent glioblastoma.

Patients and Methods

The data of 51 patients who experienced a recurrence of their glioblastoma after multimodal therapy including resection or biopsy followed by concurrent radio-chemotherapy with temozolomide (TMZ) and maintenance chemotherapy were retrospectively analyzed with respect to PFS and OS. The original study protocol submitted in 2022 and subsequent amendments (last amendment submitted in 2024) were approved by the Ethics Committee of the University of Lübeck under the file number 2022-509.

For treatment of the recurrence of glioblastoma, 26 patients underwent a resection of their recurrent lesions. Eleven of these patients received a gross tumor resection and 15 patients a subtotal resection, respectively. Re-irradiation (Re-RT) was performed in twelve patients. In ten of these patients, Re-RT regimens included two fractions per day of 1.1-1.5 Gy (plus/minus a simultaneous integrated boost) and total doses of 21.0-39.6 Gy. One patient was treated once daily with 2.5 Gy up to 40.0 Gy, and in one patient Re-RT was stopped after three fractions of 1.6 Gy given once daily. Thirty-five patients received systemic therapy for recurrent glioblastoma, most frequently with TMZ alone (15 patients) or procarbazine/lomustine (13 patients). In the other seven patients, regimens of systemic therapy included TMZ plus lomustine (n=2), TMZ plus procarbazine/lomustine (n=2), TMZ plus procarbazine/lomustine and bevacizumab (n=1), procarbazine/lomustine plus vincristine (n=1), and bevacizumab alone (n=1). In two patients, systemic therapy was recommended, but it remained unclear whether it was administered. Four patients received additional treatment with tumor treating fields.

In these patients, oGPS, mGPS, HS-mGPS, HS-oGPS, and the LabBM score plus ten patient or treatment related factors were evaluated for associations with PFS or OS (Table I). In the oGPS, 0 points are assigned if CRP is ≤10 mg/l and albumin is ≥35 g/l, 1 point if CRP is >10 mg/l or albumin is <35 g/l, and 2 points if CRP is >10 mg/l and albumin is <35 g/l (15). In the mGPS, 0 and 2 points are assigned as in the oGPS, and 1 point is assigned if CRP is >10 mg/l and albumin is ≥35 g/l (16). The HS-mGPS and the HS-oGPS use a cut-off value of 3 mg/l for CRP, otherwise assignment is the same as for mGPS and oGPS (17, 18). In all four GPS versions, scores range between 0 and 2 points, where higher scores mean worse outcomes. In this study, 0 points, 1 point and 2 points were compared. In the LabBM score, one point each is assigned in case of elevated CRP and LDH levels, and 0.5 points in case of decreased hemoglobin, platelet count, and albumin levels (19). Thus, scores range between 0 and 3.5 points. Again, worse outcomes are represented by higher scores. In this study, 0-1.0 points were compared to 1.5-3.5 points.

View this table:
Table I.

Distribution of potential prognostic factors.

The ten additional factors were age at the time of recurrence (≤60 vs. ≥61 years, median=60 years), sex (female vs. male), Karnofsky performance score (KPS) at the time of recurrence (≤80 vs. 90-100, median KPS=80), interval between primary radiotherapy and time of recurrent glioblastoma (≤5 vs. ≥6 months, median=5 months), number of recurrent lesions (1 vs. ≥2), maximal cumulative diameter of recurrent lesion(s) (≤40 vs. >40 mm), site(s) of recurrent lesion(s) (old=in field vs. new or both), resection of recurrent lesions(s) (no vs. yes), re-RT of recurrent lesions(s) (no vs. yes), and systemic therapy for recurrent lesions(s) (no vs. yes).

PFS and OS were referenced from the diagnosis of recurrent glioblastoma. Univariate analyses were performed using the Kaplan-Meier method and the log-rank test. After Bonferroni adjustment for 15 tests, p-values <0.0033 were significant representing an alpha level of <5%. Moreover, p-values <0.05 indicated a trend. Factors indicating significance or a trend were additionally incorporated in a Cox proportional hazards model (multivariate analysis), where p-values <0.05 represented an independent association with PFS or OS and p-values <0.10 represented a trend. If more than one of the investigated scoring instruments (oGPS, mGPS, HS-mGPS, HS-oGPS, LabBM score) was significant or showed a trend on univariate analysis, separate multivariate analyses were performed, each considering one scoring instrument, since the investigated instrument were considered confounding variables.

Results

On univariate analyses (Table II), favorable PFS was significantly associated with maximal cumulative diameter of recurrent lesion(s) ≤40 mm (p<0.001). After Bonferroni adjustment, trends were found for oGPS of 0-1 points (p=0.046, Figure 1), mGPS of 0-1 points (p=0.047, Figure 2), LabBM score of 0-1.0 points (p=0.018, Figure 3), KPS of 90-100 at the time of recurrence (p=0.005), resection of recurrent lesion(s) (p=0.023), and systemic therapy for recurrent lesions(s) (p=0.004). On multivariate analyses of PFS (Table III), maximal cumulative diameter of recurrent lesion(s) (p=0.003), resection (p=0.021), and systemic therapy (p<0.001) were significant.

View this table:
Table II.

Progression-free survival rates at 3, 6, and 12 months following the diagnosis of recurrent glioblastoma (univariate analyses).

Figure 1.
Figure 1.

Comparison of the prognostic groups (0 vs. 1 vs. 2 points) of the original Glasgow Prognostic Score (oGPS) with respect to progression-free survival.

Figure 2.
Figure 2.

Comparison of the prognostic groups (0 vs. 1 vs. 2 points) of the modified Glasgow Prognostic Score (mGPS) with respect to progression-free survival.

Figure 3.
Figure 3.

Comparison of the two prognostic groups (0-1.0 vs. 1.5-3.5 points) of the LabBM score with respect to progression-free survival.

View this table:
Table III.

Results of the multivariate analyses of progression-free survival.

On univariate analyses (Table IV), favorable OS was significantly associated with oGPS of 0-1 points (p<0.001, Figure 4), mGPS of 0-1 points (p<0.001, Figure 5), LabBM score of 0-1.0 points (p<0.001, Figure 6), and maximal cumulative diameter of recurrent lesion(s) ≤40 mm (p<0.001). After Bonferroni adjustment, trends were found for KPS of 90-100 at the time of recurrence (p=0.032), in-field recurrence only (p=0.005), and systemic therapy for recurrent lesions(s) (p=0.007). On multivariate analyses of OS (Table V), maximal cumulative diameter of recurrent lesion(s) (p<0.001), site(s) of recurrent lesion(s) (p<0.001), and systemic therapy (p=0.001) achieved significance. In addition, a trend was found for the LabBM score (p=0.075).

View this table:
Table IV.

Overall survival rates at 3, 6, and 12 months following the diagnosis of recurrent glioblastoma (univariate analyses).

Figure 4.
Figure 4.

Comparison of the prognostic groups (0 vs. 1 vs. 2 points) of the original Glasgow Prognostic Score (oGPS) with respect to overall survival.

Figure 5.
Figure 5.

Comparison of the prognostic groups (0 vs. 1 vs. 2 points) of the modified Glasgow Prognostic Score (mGPS) with respect to overall survival.

Figure 6.
Figure 6.

Comparison of the two prognostic groups (0-1.0 vs. 1.5-3.5 points) of the LabBM score with respect to overall survival.

View this table:
Table V.

Multivariate analysis of overall survival.

Discussion

A considerable number of patients who received multimodal therapy for glioblastoma experience an intracerebral recurrence of their disease. Many of these patients cannot receive a second extensive resection or re-RT with appropriate total doses. Their prognoses are often limited, and personalized treatment approaches considering the patient’s remaining lifespan are desirable. For patients with short estimated survival times, treatment regimens should be as short as reasonably responsible and little stressful. For patients with longer expected survival times, long-term disease control and late treatment-related toxicity are gaining in importance.

Several studies were already performed to identify patient or treatment related predictors of OS in patients with recurrent glioblastoma (3-14). In a retrospective study from 2017, favorable OS was associated with age ≤65 years at the diagnosis of recurrent glioblastoma, O6-methylguanine-DNA methyl-transferase (MGMT) promoter methylation, and re-resection plus salvage treatment including radiotherapy, systemic therapy, or both (3). In a retrospective study of patients undergoing resection of recurrent glioblastoma, improved OS was significantly associated with pre-operative KPS ≥80 prior to resection and gross re-resection (4). In another retrospective study of patients receiving resection of their recurrence, KPS >70, younger age, and gross re-resection were independent predictors of more favorable OS (5). In a third retrospective study that investigated resection of recurrent glioblastoma, younger age, and MGMT promoter methylation showed significant associations with improved OS (6). Moreover, in a prospective study of patients treated with re-resection, younger age, absence of symptoms caused by intracranial pressure, and a longer period between resection and re-resection were identified as independent predictors of more favorable OS (7). In a re-analysis of patients previously included in prospective trials, better OS was significantly associated with higher performance score, maximal size <42 mm of the largest recurrent lesion, only one recurrent lesion, and main site of recurrent lesions(s) in the frontal lobe (8). In a recent retrospective study of patients treated with repeat surgery, improved OS was significantly associated with several factors, e.g., younger age, smaller tumor volume, and higher KPS (9). In a study that used data from a national neuro-oncological registry, more favorable OS following re-resection of recurrent glioblastoma was associated with KPS ≥70, longer period between resection and re-resection, and MGMT promoter methylation (10). In another retrospective study, better OS was significantly associated with KPS 90-100, age ≤60 years, gross re-resection, and adjuvant treatment (11). In a previous retrospective study from our group that analyzed data of patients re-irradiated for recurrent glioblastoma, site (frontal lobe) and cumulative radiation dose were independent predictors of OS (12). In a retrospective study of patients receiving systemic therapy with bevacizumab for recurrence of glioblastoma, more favorable OS was associated with KPS ≥80 and additional administration of irinotecan (13). Moreover, in a retrospective study from 2023 that investigated re-irradiation plus bevacizumab after treatment with bevacizumab, a smaller volume of radiotherapy was identified as independent predictor of improved OS (14).

In addition to these patient or treatment related factors, pre-clinical markers or scoring instruments based on such markers may play a prognostic role for patients with recurrent glioblastoma. Scoring instruments that may be of prognostic value include oGPS, mGPS, HS-mGPS, HS-oGPS, and the LabBM score (15-19). In a recent study that investigated these five instruments in patients with newly diagnosed glioblastoma, lower oGPS was found to be independently associated with improved OS (18). Moreover, trends were observed for positive associations between lower mGPS and OS and lower LabBM score and PFS (18). In addition to our previous study (18), lower oGPS was associated with better OS in the retrospective study of Topkan et al. that investigated patients treated with multimodal therapy for newly diagnosed glioblastoma (20). Moreover, lower mGPS was independently associated with more favorable OS in the retrospective study of Alan et al. that did not focus on glioblastoma alone but included also patients with grade III anaplastic glioma (21). In our present study, improved OS was significantly associated with lower oGPS, lower mGPS, and lower LabBM scores on univariate analyses. Moreover, lower LabBM scores showed a trend for an association with better OS in the corresponding multivariate analyses. The results regarding oGPS and mGPS are in line with previous studies in patients with newly diagnosed or recurrent glioblastoma (18, 20, 21). The LabBM score showed no significant association with OS in our previous study of patients with newly diagnosed glioblastoma (18). However, comparisons regarding the prognostic role of the LabBM score between our present study and previous studies may be limited, since the role of the LabBM score was not yet evaluated in patients with recurrent glioblastoma. The prognostic value of HS-mGPS, HS-oGPS was also not investigated in patients with recurrent glioblastoma before. In our previous study, both scoring instruments had no significant prognostic role regarding OS in patients with newly diagnosed glioblastoma (18). These findings agree with the results for patients with recurrent glioblastoma in the present study.

In addition to OS, we investigated the prognostic value of the five scoring instruments mentioned above for PFS, which was not done in previous studies of recurrent glioblastoma. On univariate analyses, lower oGPS and lower mGPS showed a trend for associations with improved PFS. These results were different from those of our previous study performed in patients with newly diagnosed glioblastoma, where no significant associations were found between oGPS or mGPS and PFS (18). This difference suggests that prognostic factors identified for primary glioblastomas cannot be generalized to recurrent tumors.

However, when interpreting the results of our present study, one must be aware that the study has several limitations. These limitations include the retrospective study design associated with the risk of hidden selection biases, the small sample size, and the fact that only 37 patients could be analyzed for the impact of the LabBM score. Moreover, the MGMT promoter methylation of the recurrent lesion(s) was not available for most of our patients and absolutely precise definition of the maximal diameter of the recurrent lesion(s) appeared sometimes difficult due to alteration of brain tissue caused by previous resection or irradiation.

Given these limitations, patients with oGPS of 0-1 points, mGPS of 0-1 points, or LabBM score of 0-1.0 points, who have more favorable OS prognoses, may be candidates for more intensive, ideally multimodal treatment of their recurrent glioblastoma, since longer-term local disease control is important. Moreover, the risk of late treatment-related toxicities needs to be considered. In contrast, patients with oGPS of 2 points, mGPS of 2 points, or LabBM score of 1.5-3.5 points, who have less favorable OS prognoses, should be considered for little burdensome therapies with short overall treatment times. Since patients with oGPS or mGPS of 2 points have very poor prognoses with an OS probability of less than 3 months, these patients may even be considered for best supportive care (BSC) alone. When assigning a patient to BSC alone, one must consider that the subgroups of patients with oGPS or mGPS of 2 points were very small (n=4), resulting in a limited validity.

In conclusion, lower oGPS, mGPS, and LabBM scores were significantly associated with improved OS on univariate analyses. Moreover, lower LabBM scores showed a trend on multivariate analysis. These scoring instruments may help estimating the remaining lifespan of patients diagnosed with recurrent glioblastoma. Patients with poor OS prognoses should receive little burdensome therapies with short overall treatment times. For patients with more favorable prognoses, long term disease control and late toxicities become more important and need to be considered when designing a personalized treatment. When using the significant scoring instruments, the limitations of this study should be considered. Our results need to be confirmed in prospective clinical trials.

Acknowledgements

O.Z. received a scholarship from the University of Lübeck within the framework of the Emergency Aid Program for the Support of Refugee Academics from Ukraine.

Footnotes

  • Authors’ Contributions

    The study was designed by all Authors. Collection of the data was performed by O.Z. and D.R., analyses of the data by D.R. and N.Y.Y. The article drafted by D.R. was reviewed and finally approved by all Authors.

  • Conflicts of Interest

    The Authors report no conflicts of interest related to this study.

  • Received June 20, 2024.
  • Revision received July 8, 2024.
  • Accepted July 9, 2024.

This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY-NC-ND) 4.0 international license (https://creativecommons.org/licenses/by-nc-nd/4.0).

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The Predictive Value of Different Glasgow Prognostic Scores and the LabBM Score for Patients With Recurrent Glioblastoma
DIRK RADES, OKSANA ZEMSKOVA, JAN LEPPERT, NATHAN Y. YU
Anticancer Research Sep 2024, 44 (9) 3973-3981; DOI: 10.21873/anticanres.17226
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