Distinct topographic-anatomical patterns in primary and secondary brain tumors and their therapeutic potential

Abstract

Purpose: Understanding the topographic-anatomical patterns of brain tumors has the potential to improve our pathophysiological understanding and may allow for anatomical tailoring of surgery and radiotherapy. This study analyzed topographic-anatomical patterns underlying neuroepithelial tumors, primary CNS lymphoma and metastases.

Methods: Any histologically confirmed supra- or infratentorial parenchymal neoplasia of one institution over a 4-year period was included. Using high-resolution magnetic resonance imaging data, a detailed analysis of the topographic-anatomical tumor features was performed. Differences between neuroepithelial tumors, primary central nervous system lymphoma (PCNSL) and metastases were assessed using pairwise comparisons adjusted for multiple testing, upon significance of the omnibus test.

Results: Based on image analysis of 648 patients-419 (65%) neuroepithelial tumors, 28 (5%) PCNSL and 201 (31%) metastases-entity-specific topographic-anatomical patterns were identified. Neuroepithelial tumors showed a radial ventriculo-cortical orientation, inconsistent with the current belief of a growth along white matter tracts, whereas the pattern in PCNSL corresponded to a growth along such. Metastases preferentially affected the cortex and subcortical white matter of large arteries' terminal supply areas. This study provides a comprehensive anatomical description of the topography of NT, PCNSL and metastases intended to serve as a topographic reference for clinicians and neuroscientists.

Conclusions: The identified distinct anatomical patterns provide evidence for a specific interaction between tumor and anatomical structures, following a pathoclitic concept. Understanding differences in their anatomical behavior has the potential to improve our pathophysiological understanding and to tailor therapy of brain tumors.

Keywords: Anatomically tailored supratotal resection; Anatomy; Pathoclisis; Topography; Ventriculo-cortical radial unit.

Fig. 1

Surface topographic anatomy of supratentorial brain tumors: A lateral and medial view on the telencephalon and its gyral segments. B Gyral distribution pattern of neuroepithelial tumors. C Gyral distribution pattern of primary CNS (central nervous system) lymphomas. D Gyral distribution pattern of metastases. ANG angular gyrus, CIN cingulate gyrus, CNS central nervous system, CU cuneus, F1 superior frontal gyrus, F2 middle frontal gyrus, F3 inferior frontal gyrus, FP frontal pole, FUS fusiform gyrus, L lingual gyrus, LI long insular gyri, O1 superior occipital gyrus, O2 middle occipital gyrus, O3 inferior occipital gyrus, OP occipital pole, ORB orbital gyri, PC paracentral lobule, PHG parahippocampal gyrus, PostC postcentral gyrus, PreC precentral gyrus, PreCU precuneus, RE gyrus rectus, RO rostral gyrus, SCA subcallosal area, SI short insular gyri, SMG supramarginal gyrus, SPL superior parietal lobule, SubC subcentral gyrus, T1 superior temporal gyrus, T2 middle temporal gyrus, T3 inferior temporal gyrus, TP temporal pole

Fig. 2

Deep topographic anatomy of supratentorial brain tumors. A Telencephalic cortex, white matter and deep gray matter: Coronal section through the telencephalon showing the cortex, white matter sectors (subcortical, subgyral, gyral, lobar), corpus callosum, ventricular wall, central white matter (extreme capsule, external capsule, internal capsule) and central gray matter (caudate nucleus, claustrum, putamen, globus pallidus, thalamus). The classification of the white matter into white matter sectors follows a structural dichotomous division. The prevalence of involvement of subcortical telencephalic structures in neuroepithelial tumors, primary CNS (central nervous system) lymphomas and metastases is shown. B Central telencephalic white and gray matter: Superior view on the telencephalic deep gray matter (caudate nucleus, claustrum, putamen, globus pallidus, thalamus, amygdala, hippocampus) and white matter (extreme capsule, external capsule, internal capsule) in a cross-section. The prevalence of involvement in neuroepithelial tumors, primary CNS (central nervous system) lymphomas and metastases is shown. C Supratentorial ventricular walls: Segments of the lateral ventricle (frontal horn, body, atrium, occipital horn, temporal horn) and 3rd ventricle from a left oblique view. The prevalence of contact of neuroepithelial tumors, primary CNS (central nervous system) lymphomas and metastases to the wall of the ventricular segments is shown. 3rd third ventricle, A atrium, Am amygdala, B body of the lateral ventricle, CC corpus callosum, Cl claustrum, CN caudate nucleus, CNS central nervous system, Co Cortex, EC external capsule, EeC extreme capsule, FH frontal horn of the lateral ventricle, Gyr gyral white matter sector, Hipp hippocampus, IC internal capsule, OH occipital horn of the lateral ventricle, P putamen, GP globus pallidus, SubC subcortical white matter sector, SubG subgyral white matter sector, TH temporal horn of the lateral ventricle, Th thalamus, VW ventricular wall

Fig. 3

Surface topographic anatomy of cerebellar brain tumors: A superior, B inferior and C anterior view on the cerebellum with its vermian and corresponding hemispheric lobules. The cerebellar distribution of neuroepithelial tumors, primary CNS (central nervous system) lymphomas and metastases is shown. AQL anterior quadrangular lobule, Bi biventer/biventral lobule, Ce central lobule, Ce al ala lobuli centralis/wing of the central lobule, CNS central nervous system, Cu culmen, De declive, Floc flocculus, Fo folium, ISL/Gr inferior semilunar and gracile lobules—not separable on magnetic resonance imaging, Li lingual—not reliably separable on MRI, No nodule, PQL posterior quadrangular/simplex lobule, Py pyramid, SSL superior semilunar lobule, To tonsil, Tu tuber, Uv uvula, Vin vinculum—not reliably separable on MRI

Fig. 4

Brainstem and deep topographic anatomy of infratentorial brain tumors: A—brainstem: A1 cross-section through the mesencephalon with its base, tegmentum, tectum and central aqueduct. A2 Cross-section through the pons with its base and tegmentum. The frequency of involvement in neuroepithelial tumors, primary CNS (central nervous system) lymphomas and metastases is shown. A3 Cross-section through the medulla oblongata with its base and tegmentum. The prevalence of involvement in neuroepithelial tumors, primary CNS (central nervous system) lymphomas and metastases is shown. B—Deep topographic anatomy of infratentorial brain tumors: B1 Posterior view on the 4th ventricle (apex, lateral recesses, obex, fastigium), cerebellar peduncles (superior, middle, inferior) and subcortical cerebellar structures (white matter sector: subcortical, sublobular, sublobar, lobar; cerebellar nuclei). The prevalence of involvement in neuroepithelial tumours (B2), primary CNS (central nervous system) lymphomas (B3) and metastases (B4) is shown. Ap apex of the 4th ventricle, C central aqueduct, CN cerebellar nuclei, CNS central nervous system, Co cortex, Fa fastigium of the 4th ventricle, IP inferior cerebellar peduncle, Lo lobar white matter sector, LR lateral recess of the 4th ventricle, Lu lobular white matter sector, MP middle cerebellar peduncle, Ob obex of the 4th ventricle, SP superior cerebellar peduncle, SubL sublobular white matter sector, SubC subcortical white matter sector

Fig. 5

Illustrative magnetic resonance imaging based topographic anatomical tumor behavior: A—glioblastoma: example of a patient with glioblastoma of the left superior frontal gyrus. Despite the extended character of the tumor, a segmental topographic-anatomical behavior with displacement of the adjacent gyri and a tail-like relationship to the wall of the frontal horn is observed. B—Glioblastoma: another case of a patient with glioblastoma of the left occipital pole and superior occipital gyrus. Despite the extended character of the tumor, the spatial character along the ventriculo-cortical radial unit is preserved. C—WHO grade II astrocytoma: example of a patient with grade II astrocytoma of the left medial frontal gyrus. The segmental topographic-anatomical behavior of the tumor with tail-like relationship to the wall of the left frontal horn becomes evident here as well. D—Primary CNS lymphoma: this example of a patient with primary CNS lymphoma illustrates the topographic-anatomical pattern of these tumors along the projection and commissural white matter fibers. The tumor can be followed from the internal capsule, through the cerebral peduncles via the pons to the ventral medulla oblongata and the cerebellar peduncles. In addition, an infiltration along the corpus callosum can be seen. E—Primary CNS lymphoma: another example of a patient with primary CNS lymphoma, which demonstrates the tumor distribution along the short association fibers. F—Multiple metastases: a patient with multiple intracranial metastases due to an adenocarcinoma of the lung. This example illustrates both the cortico-subcortical character and the topographic-anatomical preference for watershed areas of metastases. CNS central nervous system