Disease free interval regarding the age, type of surgery, and histopathology.
\\n\\n
Released this past November, the list is based on data collected from the Web of Science and highlights some of the world’s most influential scientific minds by naming the researchers whose publications over the previous decade have included a high number of Highly Cited Papers placing them among the top 1% most-cited.
\\n\\nWe wish to congratulate all of the researchers named and especially our authors on this amazing accomplishment! We are happy and proud to share in their success!
Note: Edited in March 2021
\\n"}]',published:!0,mainMedia:null},components:[{type:"htmlEditorComponent",content:'IntechOpen is proud to announce that 191 of our authors have made the Clarivate™ Highly Cited Researchers List for 2020, ranking them among the top 1% most-cited.
\n\nThroughout the years, the list has named a total of 261 IntechOpen authors as Highly Cited. Of those researchers, 69 have been featured on the list multiple times.
\n\n\n\nReleased this past November, the list is based on data collected from the Web of Science and highlights some of the world’s most influential scientific minds by naming the researchers whose publications over the previous decade have included a high number of Highly Cited Papers placing them among the top 1% most-cited.
\n\nWe wish to congratulate all of the researchers named and especially our authors on this amazing accomplishment! We are happy and proud to share in their success!
Note: Edited in March 2021
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Petrov, A. Haddad, G.N. Petrova, H. Griffiths and R.T. Waters",authors:[{id:"109170",title:"Dr.",name:"Nikolai",middleName:"I",surname:"Petrov",fullName:"Nikolai Petrov",slug:"nikolai-petrov"},{id:"116925",title:"Prof.",name:"A",middleName:null,surname:"Haddad",fullName:"A Haddad",slug:"a-haddad"},{id:"116927",title:"Dr.",name:"H",middleName:null,surname:"Griffiths",fullName:"H Griffiths",slug:"h-griffiths"},{id:"116928",title:"Mrs.",name:"Galina",middleName:null,surname:"Petrova",fullName:"Galina Petrova",slug:"galina-petrova"},{id:"116929",title:"Prof.",name:"R.T.",middleName:null,surname:"Waters",fullName:"R.T. Waters",slug:"r.t.-waters"}]}]},relatedBooks:[{type:"book",id:"5136",title:"Recent Progress in Some Aircraft Technologies",subtitle:null,isOpenForSubmission:!1,hash:"6855bfb94011b56313a07020fa05ead6",slug:"recent-progress-in-some-aircraft-technologies",bookSignature:"Ramesh K. 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The classification of diffuse gliomas has undergone significant changes following the introduction of molecular testing, the new WHO 2016 classification introducing a new concept—integrated diagnosis [1]. The current update takes into account both the phenotype and the genotype [2]. This was the preferred alternative, as it is currently impossible to resort only to the molecular parameters in the definition of tumoral entities [3]. The classification relies both on the morphological character (growth pattern) and on the definition of the genetic status by determining the presence of mutations in the IDH1 and IDH2 genes and of the 1p/19q codeletion [4]. According to WHO 2016, diffuse gliomas are lumped together, regardless of their histopathological aspect (astrocytomas or oligodendrogliomas) [5].
The recourse to an integrated diagnosis makes it possible to formulate a more precise diagnosis of the various entities and acknowledges the existence of new entities [6].
The introduction of molecular parameters comes to improve the clinical management of patients, defining entities which feature a similar prognosis. It also paves the way to the identification of new treatment methods aimed at the biological mechanisms common to this type of tumors [5]. The genetic information supplied by the Cancer Genome Atlas Research indicate that the supratentorial gliomas with a diffuse growth pattern can be categorized separately from the other brain tumors (Figure 1) [7]. They are grouped into three categories, according to the genetic profile—the presence or absence of the 1p/19q codeletion and the mutational status of the IDH gene. The first category includes the gliomas with a classical morphology of oligodendrogliomas, having both the IDH gene mutation and the 1p/19q codeletion. The second category is represented by the tumors with an astrocytic histological pattern and IDH mutation, but without the 1p/19q codeletion. In the third category, we find the tumors with an astrocytic phenotype, which display no IDH mutation or 1p/19q codeletion. The latter category usually falls under the classical wild-type glioblastoma diagnosis [8].
Integrated diagnosis of astrocytic and oligodendroglial tumors.
This approach separates between the astrocytomas with a circumscribed growth pattern, no IDH mutation, and with BRAF mutation (pilocytic astrocytoma, pleomorphic xantoastrocytoma, and subependymal giant cell astrocytoma), on the one hand, and the diffuse astrocytic and oligodendroglial tumors, on the other. According to the new classification, the diffuse astrocytic and oligodendroglial tumors are nosologically closer than the diffuse astrocytoma and the pilocytic astrocytoma [9].
The inclusion in these categories on the basis of genetic determinations also has a role in prognosis [10].
When there is a mismatch between the phenotype and the genotype, genetic tests set the final diagnosis in keeping with the rule “molecular beats histopathology [1].”
Glioblastoma with the IDH mutation show a better evolution than the wild-type ones, generally corresponding to a secondary glioblastoma. They also have a better prognosis than the wild-type anaplastic astrocytoma. The wild-type astrocytomas have the worst prognosis of all astrocytomas, their molecular profile being characteristic for glioblastomas (EGFR amplifications, PTEN mutation, and 10q, 9p loss) [11].
The introduction of molecular parameters in the definition of entities has led to the recognition of a new entity in the group of diffuse pediatric gliomas: the tumors with a midline location, diffuse growth pattern, and the K27 M mutation in the H3 histone gene. This is the first attempt to distinguish between the pediatric brain tumors and their adult counterparts, the difference in behavior between histopathologically identical tumors being long known [12].
As to the histological grading, the WHO 2016 classification keeps the three-tiered system. The shift from low to high malignancy depends upon morphological parameters that reflect the emergence of new biological processes. The
In the group of low-grade gliomas (II and III), the histopathological stratification features a significant interobserver variability, as also demonstrated by the considerable differences in terms of survival rates manifest within this group. The evaluation of molecular parameters can also be useful in the sense of defining groups that correlate better with the prognosis [16].
As to
Axial T2W (a), FLAIR (b), and T1W + C (c) MRI examination of a patient with right insular DA IDH-mut (personal archive).
The
Mitotic activity is low to absent, the presence of a mitosis in a large biopsy being compatible with the diagnosis. If a mitosis is present in the context of an important nuclear anaplasia within a small biopsy, then the diagnosis of anaplastic astrocytoma cannot be ruled out. The proliferation index determined by way of Ki-67 is under 4%. If there is a gemistocytic component, the proliferation rate is significantly reduced [25].
As we are dealing with low proliferation rate tumor, the changes induced by hypoxia, such as microvascular proliferation and necrosis, are absent.
Secondary structures (Sherer) such as perineuronal satellitosis, subpial infiltration, and perivascular aggregation can also be present.
Other entities that need to be factored in for the differential diagnosis are: the normal brain, the demyelinating disease, anaplastic astrocytoma, oligodendroglioma, and pilocytic astrocytoma. In what concerns the diffuse pattern, the differential diagnosis must be done with lymphomas and small-cell carcinomas [26].
Gemistocytic astrocytoma is a variant of the grade II diffuse astrocytoma, characterized by the presence of more than 20% angular neoplastic astrocytes, with abundant eosinophilic cytoplasm. The nucleus is pushed toward the periphery, showing nucleoli and a dense chromatin. Electronic microscopy reveals the presence of numerous mitochondria and glial filaments, as also confirmed by the positive GFAP. A characteristic feature is the presence of the perivascular cuffing lymphocyte [27].
The classical morphopathological aspect is astrocytic, but an “oligodendroglioma-like” component can be accepted in the absence of 1p/19q codeletion.
Immunohistochemically, the battery of antibodies that can be used includes: GFAP, vimentin, IDH R132H, p53, ATRX, Olig2, and Ki67. GFAP and vimentin are positive, but of variable expression. The existence of an antibody that makes it possible to indirectly identify the R132H mutation, present in approximately 90% of tumors, is one way of identifying the tumor cells featuring this mutation. Another important antibody is ATRX, and the presence of the mutation leads to the loss of nuclear expression in the tumor cells. P53 can be used, as an intense nuclear expression is consistent with the presence of the TP53 mutation. Olig2 is nearly always present. As already indicated, Ki-67 can be used in assessing the proliferation index [28, 29, 30, 31].
ATRX encodes a chromatin-binding protein. The mutations of this gene are associated with epigenetic changes [40]. It also activates the alternative telomere lengthening mechanism, necessary in the pathogenesis of diffuse gliomas [41]. Furthermore, ATRX deficiency can create a context of generalized genetic instability which, when P53 is intact, can induce apoptosis. The occurrence of a P53 mutation alongside the ATRX one can allow tumor cells to survive [42]. This instability is reflected in the occurrence of low-level amplifications for other oncogenes, such as MYC and CCND2 [43]. The TP53 mutation is also present in nearly all IDH-mutant gemistocytic astrocytomas, in both gemistocytes and non-gemistocytes, indicating that gemistocytes are oncogenically non-reactive cells [44]. Quite interestingly, the presence of the ATRX mutation is mutually exclusive with the mutation of the gene that encodes the catalytic component of TERT telomerase. The mutations of the TERT gene are characteristic for oligodendrogliomas and wild-type glioblastomas [45].
The methylation of the MGMT gene promoter is present in more than 50% of IDH-mutant astrocytomas, but the presence of this methylation is not correlated with the status of G-CIMP [46]. By definition, 1p/19q codeletion is absent (Figure 3).
Integrated histological and molecular diagnosis of diffuse astrocytoma IDH-mutant grade II.
The genetic profile of diffuse astrocytomas is different in children and in adults; so, we can talk of adult-type and pediatric-type diffuse astrocytomas. The genetic profile of pediatric tumors involves amplifications and rearrangements of the MYB gene, alterations of FGFR1, and mutations of BRAF (V600) and KRAS [47].
There are two entities that increase the susceptibility to diffuse astrocytomas. Low-grade astrocytomas are usually diagnosed in patients with Ollier-type multiple enchondromatosis [48]. Also, those having the Li-Fraumeni syndrome are more likely to develop diffuse gliomas, but these are high-grade anaplastic astrocytomas and high-grade glioblastomas [49].
In the last decade, a great switch was produced in the therapeutical management of DA. Since it was demonstrated that these tumors have an annual linear grow of 4 mm/year on diameter [50], they are nowadays considered “infiltrating chronic disease that invades the central nervous system, that will ineluctably become malignant” [51]. It is now well established that surgery has a great impact on both the natural history and the malignant transformation. As a consequence, radical surgery becomes the goal in the treatment of diffuse gliomas in order to prevent malignant transformation and to prolong overall survival [52]. Additionally, radical surgery significantly improves seizure control compared with subtotal resection [53].
General principles of surgery, as they were underlined by Hugh Duffau, are generally accepted by the neurosurgical community: early radical surgery, awake surgery in high eloquent areas, cortical mapping, “resection according to cortico-subcortical functional and not oncological boundaries,” and “multistage resection in critical regions” [51]. The most difficult part of the operation is at the boundaries of the tumor, where even with adjuvant intraoperative MRI, the distinction between normal brain and infiltrative brain is very difficult. Surgical experience contributes to better surgical results, but even in very experienced hands, there are cases in which a residual tumor could be identified on postoperative MRI (Figure 4).
Preoperative FLAIR MR sequence (a) and immediate postoperative axial CT (b) and 3 months postoperative FLAIR examination revealing a complete removal of an insular grade II DA. (c) One year follow-up axial FLAIR MR examination reveal complete removal of tumor with no local signs of recurrence.
Neuronavigation and intraoperative ultrasound are more and more used in order to improve the surgical resection, since they are able to reveal large residual tumors. Enhanced intraoperative ultrasound is at the beginning of experience, more studies being necessary to establish its usefulness in diffuse astrocytomas resection (Figure 5) [54].
Preoperative coronal FLAIR (a), axial T2W (b) and intraoperative ultrasound examination (c) before resection of a diffuse astrocytoma subtotally removed as it is demonstrated by intraoperative ultrasound (f) and immediate postoperative CT scan (d and e).
Factors to take into consideration for immediate postoperative therapy are those considered risk factors for worse outcome namely age > 40 years, preoperative tumor diameter > 4 cm, incomplete resection, astrocytic histology, and absence of 1p/19q codeletion [55]. In this perspective, cases with DA IDH-mut completely resected, in young patients (<40 year), are candidates for close clinical imagistic observation and no adjuvant therapy is recommended in the immediate postoperative period. However, it is expected that these tumors will recur, so additional surgical and adjuvant therapy will be added at the time of progression. For tumors with subtotal removal, in patients older than 40 years of age, immediate postoperative treatment is recommended. Concerning adjuvant radiotherapy, the recommendation is in favor of lower doses (45–50.4 Gy) which are equivalent in terms of results with the high doses (59.4–64.8 Gy) but with reduced toxicity. Relative to chemotherapeutic regimen, actual data suggest that the PCV (procarbazine, CCNU, and vincristine) formula is superior to temozolomide regimen in terms of overall survival for the treatment of DA IDH-mut, mostly in cases with codeletion of 1p/19q genes [19].
The
Surgical treatment with the goal of early radical surgery is nowadays the first step in the standard of care of low-grade gliomas. Complete tumor removal based on functional borders more than on imagistic ones with the help of neuronavigation, awake surgery, and intraoperative neurophysiological monitoring (IEM) proved to offer a longer progression-free survival (PFS) and overall survival (OS) compared with subtotal removal, with reduced neurological deficits [57, 58].
Knowing that the wild-type astrocytomas have a worse prognosis, a low-dose radiotherapy regimen in the immediate postoperative period is recommended instead of close clinical imagistic observation. There are arguments in favor of radiotherapy in terms of prolonged PFS but not necessarily the OS [59]. Due to the fact that the patients receiving associated radiotherapy and chemotherapy have an improved long-term survival [60], a combined radio-chemotherapy regimen seems to be recommendable. Further studies will have to determine whether temozolomide, which was historically preferred by neuro-oncologists due to its lower toxicity and oral administration, is superior or not to PCV [61].
Axial and coronal CT scan examination of a case with an hypodense left frontal lobe lesion with intratumoral calcifications and discrete enhancement (a and b).
Axial T2W (a), axial (b) and coronal (c) FLAIR sequences of a left frontal oligodendroglioma.
T1W + C sequence (a), DTI (b) and perfusion MR (c) sequences in a patient with a LGG with a nodule of contrast enhancement corresponding to a region of increased rCBV; the patient presented 4 years previously for epileptic fits; MRI examination performed at that time was suggestive for a LGG, but the patient refused any treatment except the antiepileptic one; readmitted for signs of increased intracranial pressure and clear imagistic findings for progression and malignant transformation.
Molecular sand histopathological diagnosis of oligodendrogliomas.
Surgical principles are the same with those of DA IDH-mut, gross total resection (>90% volume reduction on 24–48 h postoperative MRI) being correlated with a longer PFS and OS, compared with subtotal resection [57].
The use of neuronavigation with co-registered preoperative T2W and FLAIR sequences and CT scan data in the presence of intratumoral calcification improved the grade of resection (Figure 10). As for other LGG, intraoperative electrostimulation mapping (IEM) on awake patient greatly improved not only functional outcome of the patient but also made possible to extend safely the grade of resection, with a great impact on the prolonged survival rate [72].
Preoperative T2W and T1W + C (a and b), respectively; 12 months postoperative T2W and T1W + C (c and d) sequences of a case with left frontal oligodendroglioma completely removed without any neurological deficit; (e) intraoperative aspect after completion of radical removal of a right temporal low-grade glioma with the preservation of Labbe vein (personal archive).
Despite the fact that there are no randomized trials comparing grade of resection with and without intraoperative MRI, it is intuitive that having real-time data on the progression of removal is at least useful for completion of tumor excision. An alternative is the intraoperative ultrasound which can detect significant remnants in real time without interruption of surgery (Figure 11). The introduction of new equipment with 4D and contrast enhancement dramatically improves the quality of images, but their role in detecting fine details in low-grade gliomas is to be established in near future.
Staged resection of a high-grade gliomas with the aid of intraoperative contrasted ultrasound: after the dural opening (a), partial resection (b) and after complete resection (c) of the tumor.
Immediate postoperative radiotherapy of completely removed oligodendroglioma IDH-mut 1p/19q codel is still under debate. Based on the results of EORTC 22845 trial which revealed that there is no significant difference in terms of OS between patients receiving immediatepostoperative radiotherapy and those receiving radiotherapy as a salvage therapy, the actual recommendation is to delay radiotherapy until signs of progression are evident. In cases of incompletely removed tumors or in the presence of any imagistic or clinical signs of progression, combined radiotherapy and PCV chemotherapy is superior to radiotherapy alone (Figure 12) [73].
Serial follow-up MRI examination of a patient with oligodendroglioma completely removed in September 2009, presenting with imagistic signs of progression 1 year later, but without any additional clinical manifestation; 15 months later the patient was readmitted for signs of increased intracranial pressure and clear findings of malignant transformation; re-operated in emergency, patient followed the standard radio-chemotherapy regimen.
Some authors argued that even in cases with foci of anaplasia imbedded in low-grade glioma, the total resection is sufficient for a long-term PFS, and no adjuvant treatment is needed; but this is not the standard of care as the authors already mentioned at the conclusions [74].
Upper row: left frontal lesion hyperintense in T2W (a) and FLAIR (b) sequences with no contrast and T1W sequence (c) MRI in a 24 years old men diagnosed with grade III astrocytoma; lower row: left frontal lesion having similar characteristics in T2W (d) and FLAIR (e) sequences but with a discrete enhancement in T1W (f) sequences revealed in the young men’s father MRI examinations, operated 5 years before with an anaplastic astrocytoma (personal archive) suggesting a hereditary determinism in this particular case.
The immunohistochemical analysis (Clone H09) of the IDH1 R132H mutation performed on a patient with anaplastic astrocytoma. Infiltrating tumor cells positives at cytoplasmic level are observed in a background of negative normal astrocytes (left). In vivo single-voxel localized PRESS spectra were performed for the same patient. Black line represents the sum of spectra obtained during MRS. Pink line represent the spectra of 2-hydroxyglutarate identified at TE 35 ms (right).
Being malignant tumors, early radical surgery represents the first step of the multimodal treatment of anaplastic astrocytomas. Due to the diffuse infiltration of the brain, radical excision is rarely achieved, meaning that if 1% of the initial volume remains in place, a local recurrence is almost certain. Additionally, the location of tumor in high eloquent areas prevents a radical excision in order not to produce severe neurological deficits. The main goals of surgery in high-grade gliomas (HGG) are to reduce the mass effect, to obtain relevant pathological tissue, to reduce the tumor burden, and to prolong survival with improved quality of life. There are many factors influencing OS in high-grade gliomas such as preoperative Karnofsky score, age, general and neurological status at the preoperative and postoperative period, pathology and genetics of the tumor, grade of resection, response and tolerance to the adjuvant therapy. Among all these factors only those related to surgery could be influenced, namely the grade of resection and the neurological status after the operation [78]. There is a very delicate balance between the radical surgery and preservation of neurological function. The more aggressive the surgery, the higher the risk for neurological deficiencies stands (Figure 15). After the publication of the trial conducted by Stupp and in 2005 [79], in which the role of surgery was minimized, a large amount of studies were published underlying the importance of gross total resection (GTR) compared not only with biopsy but also with near total resection (NTR) and subtotal resection (STS) as a factor that independently influences OS in HGG. For example, in anaplastic astrocytomas, there is a difference of 12 months in median of survival in favor of GTR compared with STR [80].
Integrated histological and molecular diagnosis of anaplastic astrocytoma IDH-mutant.
A retrospective study performed by us on 266 cases of HGG reveals the fact that gross total removal (GTR) greatly influences survival compared with STR. At the three periods of monitoring (12, 18, and 24 months), the difference regarding survival mean between GTR vs. STR ranged from 2.8 months (at 12 months monitoring) to 4.4 months (at 18 months monitoring) up to 5.1 months (at 24 months monitoring) including all types of malignant gliomas. We also found that the type of surgery and the age are prognostic factors that significantly influenced in all three periods of monitoring, while the histopathology was a prognostic factor for survival only at the 24 months monitoring (Table 1) [81].
Disease free interval | Log rank (Mantel-Cox) factor: age (<65 years/≥65 years) | Log rank (Mantel-Cox) factor: type of surgery (gross total removal/subtotal removal) | Log rank (Mantel-Cox) factor: histopathological diagnosis | Log rank (Mantel-Cox) factor: gender |
---|---|---|---|---|
12 months | 0.000 | 0.000 | 0.090 | 0.296 |
18 months | 0.000 | 0.000 | 0.122 | 0.836 |
24 months | 0.000 | 0.000 | 0.031 | 0.756 |
Disease free interval regarding the age, type of surgery, and histopathology.
A more detailed discussion regarding the role of surgery will be presented later in the chapter, along with the types of glioblastomas.
Preoperative T2W and T1W+ C (a and b) sequences of a case with left frontal anaplastic astrocytoma completely removed; follow-up MRI performed at 4 months postoperatively and after concomitant radio- and chemotherapy with temozolomide showed no signs of local recurrence (c and d).
The diagnosis of
As for the other types of gliomas, the grade of surgical resection is an independent factor for PFS and OS. As a consequence, GTR is recommendable wherever is possible without neurological damage (Figure 17).
Axial (a) and coronal (b) contrasted CT scan demonstrating the presence of a voluminous expansive lesion with large cystic components and peripheral calcification with a reduced perilesional edema, aspect highly suggestive for an anaplastic oligodendroglioma; after GTR the axial T2W (c) and coronal FLAIR (d) sequences at 2 years follow-up do not indicate a local progression.
Due to the good response of anaplastic oligodendrogliomas to chemotherapy, the subtotal resection with preservation of neurological function is also an acceptable surgical strategy [88].
Adjuvant treatment is recommended in anaplastic oligodendrogliomas on a regular basis. Recent studies failed to demonstrate a benefit of temozolomide over the classical PCV regimen, which remains the main tool for first-line chemotherapy in anaplastic oligodendrogliomas. Radiotherapy is reserved for cases of clear imagistic evidence of tumor progress. Fractions of 1.8–2 Gy for a total dose of 54–60 Gy are the actual recommended radiotherapy regimen based on clinical evidence [89].
Axial T2W (a), axial FLAIR (b) and coronal T1W + C (c) sequences of an extremely rare intraventricular anaplastic oligodendroglioma completely removed, as it is demonstrated by the 6 months follow-up MRI (d–f).
Once the suspicion brain tumor is raised, an
Coronal (a) and axial (b) preoperative contrasted CT scan examination of a case with left temporal inhomogeneous expansive lesion with a “ring enhancement” highly suggestive for a glioblastoma; (c) and (d) immediate postoperative contrasted CT scan examination demonstrating gross total removal of the tumor.
Nevertheless,
T2W (a), FLAIR (b) and T1W + C MRI (c) sequences of a left frontal expansive lesion, aspects that are highly suggestive for a glioblastoma.
Advanced MRI techniques are also useful for differentiating between local recurrence and radionecrosis (pseudoprogression). Recently, it was showed that rCBV as a single examination modality is superior to volume transfer constant (Ktrans) or apparent diffusion coefficient (ADC) for the prediction of local recurrence. The combination of rCBV and Ktrans improves the accuracy of the recurrence diagnosis [94].
There are a number of cellular morphologies common to glioblastomas: fibrillary astrocytes, gemistocytes, smalls cells (highly infiltrative, bipolar, and mitotically active), epithelioid, rhabdoid, granular, or lipidized cells. The areas that contain astrocytes whose phenotype is more easily identified can be more or less clearly separated from the areas of high pleomorphism. The cells are poorly differentiated, with pleomorphism, significant atypia, and brisk mitotic activity. The presence of a cellular population having a different phenotype indicates the emergence of a new tumoral clone through new genetic events [96].
The dominance of a specific cell type in the tumor generates a pattern that is useful in the diagnosis of small cells, with a neuroectodermal component, with an oligodendroglial component, with granular cells, with gemistocytes, and with lipidized cells. This is an indicative for the diagnosis but insufficient for a distinct variant.
Three histological variants are known: giant cell glioblastoma, gliosarcoma, and epithelioid glioblastoma.
From a molecular point of view, they showed a high incidence of PTEN and TP53 mutations; but, no EGFR amplifications and no homozygous deletion of CDK2A were shown. As a variant of the wild-type glioblastoma, it features no IDH mutations. The prognosis is slightly better than in the case of usual glioblastomas [107].
Necrosis and microvascular proliferations are required for a diagnosis.
The microvascular proliferations are in direct relation with the necrosis, hypoxia being a significant factor that stimulates the formation of vessels by way of HIF1A and VEGFA [114]. Another characteristic is the thrombosis of small vessels. Although, in glioblastomas, vascularization is very well represented, the vascular structures are immature and largely incapable of compensating for the hypoxia caused by the exuberant proliferation [115].
Necrosis, of the coagulative type, is typical for glioblastoma. It affects both the cells and the vascular structures and is indicative of the extremely high proliferation rate associated with this type of tumor. It is considered to be an aggressive factor in astrocytic tumors, its size being associated with a lower survival rate. In the necrotic areas, we can see “shadows” of the dilated vessels surrounded by tumor cells in various stages of decay [116]. We can also see vessels that still contain oxygenated blood surrounded by viable cells. Undoubtedly, the high proliferation rate of glioblastomas plays an important part in the onset of necrosis, as there is a mismatch between the need for oxygen and the number of functioning vessels. As in the vicinity of the necrotic areas, we notice venal occlusions and vascular thrombosis, and it has been hypothesized that this is the mechanism that could trigger or spread the necrosis. Lesions of the endothelium trigger the release of procoagulants, which generate microscopic or macroscopic vascular thrombosis. Vascular thrombosis is usually accompanied by the so-called pseudopalisading [25]. This is caused by the migration of cells from the central necrotic area to the more oxygenated exterior ones, in a “moving away wave” toward the vessels unaffected by thrombosis and capable of maintaining a level of oxygenation sufficient for their survival. In an attempt to somewhat restore the level of oxygenation, these cells also secrete proangiogenic factors (VEGFs), causing the vascular alterations mentioned above [117].
A perivascular positioning of lymphocytes can occur in the areas with gemistocytes. In glioblastomas, the number of lymphocytes can vary, and they are mainly LT CD8. Quite interestingly, the presence of an extensive LT CD8 infiltration has been identified with the long-term survivors. LT CD4 and LB are also present, but in small numbers. Microglia and histiocytes can also be seen [118].
Immunohistochemically, GFAP has a positive expression, its variability reflecting the heterogeneous nature of the tumor. Sarcomatous and primitive cellular components are negative, while the gemistocytic component is strongly positive. It is also positive in the lipidized variant. S100 and Olig2 are positive in glioblastomas and are quite useful in the diagnosis of poorly differentiated tumors [119]. Nestin is of particular importance in the differential diagnosis in regard to other high-grade gliomas, as it is positive in glioblastomas [120]. P53 is positive in the glioblastomas with a missense mutation of TP53 [121]. Together with WT1 (which can be positive in low-grade gliomas), it makes the distinction between tumor cells and the reactive post-treatment cells [122]. EGFR indicates the relative amplification of the gene, being expressed in 45–95% of cases. EGFRvIII is present in one third of all cases [123]. The expression of Ki-67 varies. A positive IDH R132H is incompatible with the diagnosis of IDH wild-type glioblastomas.
In what concerns the
The PTEN gene suffers changes almost exclusively in the primary glioblastomas, either by the way of a missense mutation in the area homologous to tensin/auxilin, or following truncation at various sites caused by the loss of the chomosomal region [128].
The
The CDKN2A locus generates several CDKN2 and p14ARF proteins that act as tumor suppressors. The loss of p14ARF expression is encountered in glioblastomas, being correlated with the methylation of the promoter of the deletion of the CDKN2 gene.
TERT can show mutations at the level of the promoter, especially in wild-type glioblastomas, being mutually exclusive with TP53. The occurrence of the mutation (in one of the two hot spots) is followed by the accumulation of the GABP transcription factor at the level of the promoter, leading to the aberrant expression of the gene [130].
The IDH gene is not mutated by definition in wild-type glioblastomas, and the evaluation of the mutational status of this gene can make the distinction between primary and secondary glioblastomas [131].
MicroRNA and long non-coding RNA have also been studied in glioblastomas. miR10b controls the cycle of stem and tumoral cells in GBM and is associated with a poor prognosis. The role of the interaction between microRNA and the oncogenetic pathways known as drivers in GBM, such as for instance PI3K, has also been demonstrated [133].
The currently defined histological entities have different genetic expression profiles, which are correlated with the grade and are a better predictor of patient outcome [37].
The methylation profile of the MGMT gene promoter is predictive for the response to the treatment with alkylants such as temozolomide or methylants. It is variable, being higher in the IDH-mutant tumors, having a G-CIMP profile [134].
The ATRX gene is also mutated, the same mutation being present in the grade II and III precursor astrocytic lesions. Alongside the ATRX and IDH mutation, TP53 is more frequently mutated in secondary glioblastomas [31]. EGFR amplifications are rare, as opposed to the GBM wild-type, indicating that the genetic onset and progression pathways are different.
The genetic expression of GBM IDH-mutant is relatively homogeneous, most of them falling under the proneural profile [126]. Epigenetically, the occurrence of the IDH mutation induces an extensive hypermethylation of the DNA, all IDH-mutant tumors belonging to a hypermethylated phenotype [138]. The prognosis for GBM IDH-mutant is better than that for GBM wild-type, the survival rate being 2.4 times higher (Table 2) [139].
Astrocytoma | Oligodendroglioma | GBM-wt | |
---|---|---|---|
IDH | + | + | - |
ATRX | + | - | - |
TERT | - | + | + |
p53 | + | - | + |
1p/19q | - | + | - |
Synthesis of the mutational status in the main categories of diffuse gliomas.
Sir Rickman Godlee was the first surgeon who reported a resection of a glioma in 1884. More than one century later, the results of the treatment in malignant gliomas remained unsatisfactory. Improvements of surgical techniques and technology developed in this period, including microsurgery, neuronavigation, intraoperative MRI, intraoperative neuromonitoring, and 5-ALA merely improved the grade of resection while increasing the postoperative quality of life of the patient; however, they were unable to change the inexorable course of malignant gliomas to recurrence and death. Perhaps the most important adjuvant of surgery was the introduction of radiotherapy in the middle of the last century, adding a median survival of at least 7 months, as it was highlighted by Ley and coworkers in 1962. In their reported series of glioma, the largest at that time, the median of survival through surgery alone was 7 months, whereas in the group receiving additional radiotherapy the median survival rate was at 15 months [140]. The addition of chemotherapy further improved the survival, but despite the large advancements in research within the last decade, the median survival rate barely increased by no more than 2 months, inexorably close to the data reported 20 years ago [141].
Regarding the role of surgery, there is an increasing body of literature underlining the importance of GTR comparing with STR or biopsy. A meta-analysis covering 41,117 unique patients in 37 retrospective studies revealed a significant improvement of OS in GTR cases compared with STR [142]. Another prospective study comparing grade of resection with the aid of immunofluorescence (5-ALA) versus white light also demonstrated a significant median of survival in favor of those with GTR (16.7 months vs. 11.7 months) [143]. Currently, there is sufficient data favoring GTR to encourage surgeons to increase the grade of resection, while also striving not to cause additional neurological deficits (Figure 21).
MRI examination of a patient with left paraventricular glioblastoma: (a) T2W sequence reveals an inhomogeneous lesion adjacent to occipital horn of left lateral ventricle surrounded by a hyperintense region of edema; (b) T1W + C sequence expose classical aspect of “ring enhancement”; (c) DWI study demonstrating a restricted diffusion corresponding to the region of tumor; MRI perfusion reveals a heterogeneous rCBV (d) and increased cerebral blood flow (CBF) corresponding to the enhanced lesion (e) ; (f) Tractography shows a disruption of fibers compared to the contralateral side.
New tools were introduced in the last two decades in order to facilitate GTR, simultaneously with the permanent improvement of the operative microscope. Contemporary neuronavigation equipment offers a more precise localization with real-time correction adapted to the brain shift. Functional and anatomical data are merged in order to facilitate surgical intervention, while also avoiding damage to eloquent areas and tracts. Intraoperative tools, such as intraoperative MRI, are now available in many centers, allowing surgeons to achieve a more complete tumor removal and, as a direct consequence, prolong survival [144]. Intraoperative ultrasonography, having been introduced in practice two decades prior, is at present more accurate in defining intracerebral lesions, especially in cases of HGG, facilitating a real-time control of resection (Figure 22) [145].
Preoperative (a and b) and postoperative (c and d) contrasted CT scan images demonstrating the GTR of a left gliosarcoma.
Contrasted intraoperative ultrasound guidance apparently adds more detailed information concerning the grade of resection [146].
We may conclude that surgery, and radical surgery especially, remains the first and most important step of the multimodal treatment in prolonging the survival of patients with malignant gliomas.
Whole brain radiation therapy stood as the most important adjuvant to surgery up until the randomized trial conducted by Walker el al. in 1980. In this trial, the authors compared the efficacy of radiotherapy alone to the addition of nitrosourea chemotherapy. They demonstrated a benefit of 2–3 months in the group treated with combined radio-chemotherapy and this combination has been the standard of care for almost 25 years [147]. In time, whole brain radiotherapy was replaced by a more focal radiotherapy, in order to prevent secondary effects of radionecrosis. The current standard of radiotherapy is a fractionated conformational dose of 2Gy fractions/day, 5 days/week for a period of 6 weeks. The radiotherapy regimen must be initiated in three to no more than 6 weeks after the surgery [148].
Concerning chemotherapy, the actual standard consists of concomitant radiotherapy and temozolomide (TMZ) administration, followed by six cycles of TMZ at every 28 days. This was established in 2005 based on the results of the trial conducted by Stupp et al. (Figure 23) [79].
Ultrasonography-guided resection (a) of a diffuse astrocytoma with foci of glioblastoma (arrow) demonstrated on T1W + C image (b).
The response of the patients to the TMZ regimen is highly variable, with one of the factors influencing the positive response being the methylation of the MGMT promoter, which is present in less than 50% of glioblastoma cases. It was showed that only 65–70% of new cases of glioblastoma respond to TMZ; although in spite of these evidences, TMZ is still the main agent in multimodal treatment of glioblastoma (Figure 24) [149].
Preoperative axial (a), coronal (b) and sagittal (c) T1W + C sequences of a patient with glioblastoma completely removed and treated with the standard radio-chemotherapy regimen; postoperative enhanced T1W images (d–f) reveal the removal of the tumor with the persistence of a small contrasted nodule, which is stable at 5 years after surgery.
A large number of researches were made in order to decrypt the intimate mechanism of apparition and development of glioblastomas, as well as the response of tumor cells to different chemical, physical, or biological agents. Among these agents, only few met the clinical criteria to be introduced in practice. Gliadel (carmustine-impregnated biodegradable wafers) on local application proved to add a median of survival of 2.3 months compared to the standard treatment, yet was accompanied by an increased incidence of local complications (infection and CSF fistula) [150]. We also add our research effort on glioblastoma stem cell cultures in order to improve the response to TMZ by addition of new drugs like arsenic trioxide or metformin as sensitizers [151, 152]. New ways to deliver TMZ have been proposed [153]. Antiangiogenic agents (Bevacizumab) was also tested on glioblastoma stem cells with controversial response (in some cultures, they increased angiogenesis) (Figure 25).
Preoperative T1W + C sequence (a) of a glioblastoma, almost completely removed as it was revealed by immediate postoperative CT scan (b); the patient was not responsive to the standard adjuvant treatment as it is demonstrated by the postoperative enhanced MRI at 4 months (c).
The clinical trials testing Bevacizumab in newly diagnosed glioblastoma failed to demonstrate a benefit on survival [154, 155]. Immunotherapy is a highly experimental approach of present days, as are other therapies. A special interest was raised in the use of an electric field delivered by noninvasive transducers placed on a headpiece, the so-called Novocure treatment. The addition of this new modality to the standard radio-chemotherapy regimen improved the PFS and OS in glioblastoma-treated patients [156].
We can conclude that despite the huge efforts and investments made in research and therapies, the results still disappoint. This suggests the fact that we are possibly on the correct course, but against the tide. The future multimodality treatment may consist of patient-tailored treatments owing to the multiple individual and tumor-related factors that influence the response to therapy.
In vitro 3D model of glioblastoma stem cells culture demonstrating an increase angiogenesis in contact with TMZ and resistance to the addition of Bevacizumab compared with the control (ctrl) (personal archive).
This type of tumor is not amenable for surgical treatment. The single debate is related to the role of biopsy. The actual accepted strategy is that biopsy (open or stereotactic) is indicated only in atypical tumors. The term of atypical is somehow unclear, but generally it is accepted that the unilateral extension of tumor and the presence of cystic components or focal hemorrhages offer a rationale for surgery.
In centers with experience in stereotactic biopsy, this could be the method of choice. Otherwise, open surgery is performed, guided by the most superficial part of lesion or throughout the so-called “safe entry zone.” In selected cases, surgical interventions can offer the opportunity of cytoreductive surgery, thus creating proper conditions for radiotherapy (Figure 27) [161].
T2W (a), FLAIR (b) and DWI (c) sequences of an infiltrative tumor into the brainstem and left cerebellar peduncles.
Radiotherapy is the single recommendable therapy for this kind of lesions (Figure 28). A total dose between 54 and 60 Gy, administered in fractions of 1.8–2 Gy, is the actual recommendation of oncologists. No chemotherapy regimen was able to demonstrate a benefit in terms of survival. Corticosteroids are also administered during radiotherapy. After a period of symptom amelioration, the tumor will inevitably progress [162].
(a) T2W sequence of a diffuse infiltrative brainstem astrocytoma, partially resected; the 18 months follow-up MRI (b) demonstrates a stable lesion after radiotherapy.
Despite having a particular clinical evolution, pediatric tumors have been lumped together with the adult ones, according to the histopathological similarities [163]. We now know that their onset and progression genetic mechanisms are different. A well-defined entity that occurs predominantly in children is the one described above. As opposed to adult tumors, the pediatric ones show changes in the genes regulating chromatin structure and the genetic expression profile. Apart from the diffuse midline glioma, H3 K27 M-mutant, another mutation present in the same gene, but in the G34 rather than the K27 position, defines another entity usually encountered in youths. The location differs, as it is no longer situated in the midline area, but in the brain hemispheres. High-grade astrocytic pediatric tumors with a telencephalic location show the TP53, CDK2A, ATRX, and SETD2 mutations [164]. The genetic syndromes that favor the onset of brain tumors during childhood are type 1 neurofibromatosis and Li-Fraumeni syndrome.
The 2016 brain tumor classification represents an important step forward in the introduction of molecular diagnosis in the daily current practice. This is also an important step toward a personalized patient-tailored multimodal management of brain tumors. Neurosurgeons, as part of a multidisciplinary team, need to be familiarized with all the aspects regarding specific brain tumors in order to offer the best chance to their patients and to prolong survival with a good quality of life.
We thank our colleagues Dr. Reka David for spectroscopy and DTI analysis, Dr. Alexandru Florian and Lecturer Bogdan Aldea for English language improvement and to Dr. Anne-Marie Constantin for manuscript editing.
The authors declare that there is no conflict of interest.
1p/19q-codel | 1p/19q-codeleted |
ATRX | alpha thalassemia/mental retardation syndrome X-linked |
CK | cytokeratin |
DA | diffuse astrocytoma |
DTI | diffusion tensor images |
EGFR | epidermal growth factor receptor |
EMA | epithelial membrane antigen |
FGFR1 | fibroblast growth factor receptor 1 |
GBM | glioblastoma |
GFAP | glial fibrillary acidic protein |
HIF1A | hypoxia-inducible factor 1-alpha |
IDH | isocitrate dehydrogenase |
IDH-mut | IDH-mutant |
LT | lymphocyte B |
LT | lymphocyte T |
MDM2 | mouse double minute 2 homolog |
MDM4 | mouse double minute 4 |
MGMT | O6-methylguanine DNA methyltransferase |
MRI | magnetic resonance imaging |
MRS | magnetic resonance spectroscopy |
ms | milliseconds |
NCAM1 | neural cell adhesion molecule |
NF1 | neurofibromatosis 1 |
NOS | not other specified |
PI3K | phosphatidylinositol-3 kinase |
PRESS spectra | point-resolved spectroscopy |
PTEN | phosphatase and tensin homolog |
Rb | retinoblastoma |
TE | echo time |
TERT | telomerase reverse transcriptase |
TP53 | tumor protein |
VEGFA | vascular endothelial growth factor A |
wt | wild type |
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