Voxel-based lesion mapping of meningioma: a comprehensive lesion location mapping of 260 lesions

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OBJECTIVE

In the present study the authors aimed to determine preferred locations of meningiomas by avoiding descriptive analysis and instead using voxel-based lesion mapping and 3D image-rendering techniques.

METHODS

Magnetic resonance images obtained in 248 treatment-naïve meningioma patients with 260 lesions were retrospectively and consecutively collected. All images were registered to a 1-mm isotropic, high-resolution, T1-weighted brain atlas provided by the Montreal Neurological Institute (the MNI152), and a lesion frequency map was created, followed by 3D volume rendering to visualize the preferred locations of meningiomas in 3D.

RESULTS

The 3D lesion frequency map clearly showed that skull base structures such as parasellar, sphenoid wing, and petroclival regions were commonly affected by the tumor. The middle one-third of the superior sagittal sinus was most commonly affected in parasagittal tumors. Substantial lesion accumulation was observed around the leptomeninges covering the central sulcus and the sylvian fissure, with very few lesions observed at the frontal, parietal, and occipital convexities.

CONCLUSIONS

Using an objective visualization method, meningiomas were shown to be located around the middle third of the superior sagittal sinus, the perisylvian convexity, and the skull base. These observations, which are in line with previous descriptive analyses, justify further use of voxel-based lesion mapping techniques to help understand the biological nature of this disease.

ABBREVIATIONS FSL-FLIRT = FSL Linear Image Registration Tool; JBTR = Japan Brain Tumor Registry; Mango = Multiimage Analysis GUI; MNI152 = Montreal Neurological Institute brain atlas; NF2 = neurofibromatosis Type 2; NIfTI = Neuroimaging Informatics Technology Initiative; UCSF = University of California, San Francisco.

Article Information

Correspondence Manabu Kinoshita, Department of Neurosurgery, Osaka International Cancer Institute, 3-1-69 Otemae, Chuo-ku, Osaka 541-8567, Japan. email: mail@manabukinoshita.com.

INCLUDE WHEN CITING Published online September 1, 2017; DOI: 10.3171/2017.3.JNS17169.

Disclosures. The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.

© AANS, except where prohibited by US copyright law.

Headings

Figures

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    Workflow for voxel-based lesion mapping. The NIfTI data were registered to a 1-mm isotropic, high-resolution, T1-weighted brain atlas provided by the MNI (the MNI152). The Gd-enhancing lesions were semiautomatically segmented and flipped so that all lesions were concentrated onto the right side of the brain. All lesions were then summed and a heat map for the frequency of lesion occurrence was reconstructed, followed by 3D rendering of the frequency map.

  • View in gallery

    Graph showing tumor volume distribution after image registration. After each individual brain image was de-formed and registered on the MNI152, images were standardized and lesion sizes were calculated. The mean and median volumes were 28.1 ml and 13.6 ml, respectively. Volume distribution did not fit a gaussian distribution (p < 0.0001; D’Agostino and Pearson omnibus normality test).

  • View in gallery

    A 3D rendering of the voxel-based lesion frequency map; 3D lesion frequency map clearly showing that skull base structures such as parasellar, sphenoid wing, and petroclival regions were commonly affected by the tumor. The middle one-third of the superior sagittal sinus was most commonly affected by parasagittal tumors. Noticeable lesion accumulation was observed around the leptomeninges covering the central sulcus and the sylvian fissure, with very few lesions observed at the frontal, parietal, and occipital convexities.

  • View in gallery

    Comparison of meningioma location preferences as documented by Harvey Cushing and in the current study. Both illustrations are in good agreement, showing that parasagittal meningiomas occur around the middle one-third of the superior sagittal sinus and that convexity meningiomas preferentially occur along the sylvian fissure, with very few located at the parietal convexity. The upper left image is from Harvey Cushing and Louise Eisenhardt’s book Meningiomas, Their Classification, Regional Behaviour, Life History, and Surgical End Results (Springfield, IL: Charles C Thomas, 1938; public domain), and the 2 lower left images are from Harvey Cushing’s paper “The meningiomas (dural endotheliomas): their source, and favoured seats of origin” (Brain 45:282–316, 1922; public domain).

References

  • 1

    Adachi KKawase TYoshida KYazaki TOnozuka S: ABC Surgical Risk Scale for skull base meningioma: a new scoring system for predicting the extent of tumor removal and neurological outcome. Clinical article. J Neurosurg 111:105310612009

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2

    Brastianos PKHorowitz PMSantagata SJones RTMcKenna AGetz G: Genomic sequencing of meningiomas identifies oncogenic SMO and AKT1 mutations. Nat Genet 45:2852892013

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3

    Choy WKim WNagasawa DStramotas SYew AGopen Q: The molecular genetics and tumor pathogenesis of meningiomas and the future directions of meningioma treatments. Neurosurg Focus 30(5):E62011

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4

    Clark VEErson-Omay EZSerin AYin JCotney JOzduman K: Genomic analysis of non-NF2 meningiomas reveals mutations in TRAF7, KLF4, AKT1, and SMO. Science 339:107710802013

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5

    Committee of Brain Tumor Registry of Japan: Report of brain tumor registry of Japan (2001–2004). Neurol Med Chir (Tokyo) 54 (Suppl 1):11022014

    • Search Google Scholar
    • Export Citation
  • 6

    Cushing H: The meningiomas (dural endotheliomas): their source, and favoured seats of origin. Brain 45:2823161922

  • 7

    Cushing HEisenhardt L: Meningiomas, Their Classification, Regional Behaviour, Life History, and Surgical End Results. Springfield, IL: Charles C Thomas1938

    • Export Citation
  • 8

    Hashiba THashimoto NIzumoto SSuzuki TKagawa NMaruno M: Serial volumetric assessment of the natural history and growth pattern of incidentally discovered meningiomas. J Neurosurg 110:6756842009

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9

    Hashimoto NRabo CSOkita YKinoshita MKagawa NFujimoto Y: Slower growth of skull base meningiomas compared with non-skull base meningiomas based on volumetric and biological studies. J Neurosurg 116:5745802012

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10

    Jenkinson MBeckmann CFBehrens TEJWoolrich MWSmith SM: FSL. Neuroimage 62:7827902012

  • 11

    Kane AJSughrue MERutkowski MJShangari GFang SMcDermott MW: Anatomic location is a risk factor for atypical and malignant meningiomas. Cancer 117:127212782011

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12

    Kinoshita MSasayama TNarita YYamashita FKawaguchi AChiba Y: Different spatial distribution between germinal center B and non-germinal center B primary central nervous system lymphoma revealed by magnetic resonance group analysis. Neuro Oncol 16:7287342014

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 13

    Kuratsu JKochi MUshio Y: Incidence and clinical features of asymptomatic meningiomas. J Neurosurg 92:7667702000

  • 14

    Onizuka MSuyama KShibayama AHiura THorie NMiyazaki H: Asymptomatic brain tumor detected at brain check-up. Neurol Med Chir (Tokyo) 41:4314352001

  • 15

    Phan TGDonnan GAWright PMReutens DC: A digital map of middle cerebral artery infarcts associated with middle cerebral artery trunk and branch occlusion. Stroke 36:9869912005

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16

    Reuss DEPiro RMJones DTWSimon MKetter RKool M: Secretory meningiomas are defined by combined KLF4 K409Q and TRAF7 mutations. Acta Neuropathol 125:3513582013

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17

    Scheitzach JSchebesch KMBrawanski AProescholdt MA: Skull base meningiomas: neurological outcome after microsurgical resection. J Neurooncol 116:3813862014

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18

    Shrivastava RKSegal SCamins MBSen CPost KD: Harvey Cushing’s Meningiomas text and the historical origin of resectability criteria for the anterior one third of the superior sagittal sinus. J Neurosurg 99:7877912003

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19

    Takano KKinoshita MTakagaki MSakai MTateishi SAchiha T: Different spatial distributions of brain metastases from lung cancer by histological subtype and mutation status of epidermal growth factor receptor. Neuro Oncol 18:7167242016

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20

    van Alkemade Hde Leau MDieleman EMTKardaun JWPFvan Os RVandertop WP: Impaired survival and long-term neurological problems in benign meningioma. Neuro Oncol 14:6586662012

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 21

    Yaşargil MG: Microsurgical Anatomy of the Basal Cisterns and Vessels of the Brain. Stuttgart: Thieme1984

    • Export Citation
  • 22

    Yoneoka YFujii YTanaka R: Growth of incidental meningiomas. Acta Neurochir (Wien) 142:5075112000

  • 23

    Zentner JMeyer BVieweg UHerberhold CSchramm J: Petroclival meningiomas: is radical resection always the best option? J Neurol Neurosurg Psychiatry 62:3413451997

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

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