Difference between revisions of "Meningioma"

From Libre Pathology
Jump to navigation Jump to search
(→‎Molecular: update)
(→‎IHC: update)
 
Line 370: Line 370:
*PR +ve (approx. 75%, expression decreases from grade I to III).
*PR +ve (approx. 75%, expression decreases from grade I to III).
*SSTR2A +ve (approx. 95%).
*SSTR2A +ve (approx. 95%).
*S100 variable (up to 35% cases, usually patchy).
*S100 variable (up to 35% cases, usually patchy).<ref>{{cite journal |vauthors=Behling F, Fodi C, Skardelly M, Paulsen F, Tabatabai G, Honegger J, Tatagiba M, Schittenhelm J |title=The prognostic role of the immunohistochemical expression of S100 in meningiomas |journal=J Cancer Res Clin Oncol |volume= |issue= |pages= |date=July 2022 |pmid=35838837 |doi=10.1007/s00432-022-04186-9 |url=}}</ref>
*SOX10 -ve.
*SOX10 -ve.
*GFAP -ve.
*GFAP -ve.
*CD34 usu. -ve (approx 8% cases positive).  
*CD34 usu. -ve (approx 8% cases positive).  
*CD13 +ve.<ref>{{cite journal |vauthors=Marletta S, Luchini C, Sperandio N, Torresani E, Sorio A, Girolami I, Scarpa A, Eccher A, Ghimenton C |title=CD13 is a useful tool in the differential diagnosis of meningiomas with potential biological and prognostic implications |journal=Virchows Arch |volume=480 |issue=6 |pages=1223–1230 |date=June 2022 |pmid=35212813 |pmc=9184408 |doi=10.1007/s00428-022-03304-9 |url=}}</ref>
*Other CKs usually -ve (approx 6% cases positive, mostly secretory meningiomas).
*Other CKs usually -ve (approx 6% cases positive, mostly secretory meningiomas).



Latest revision as of 14:13, 19 September 2022

Meningioma
Diagnosis in short

Meningioma. HPS stain.

LM whorled appearance, calcification - psammomatous, +/-nuclear pseudoinclusions
Subtypes Grade I (meningothelial, fibrous, transistional, psammomatous, angiomatous, microcystic, secretory, lymphoplasmacyte-rich, metaplastic), Grade II (invasive, clear cell, chordoid), Grade III (papillary, rhabdoid)
LM DDx schwannoma, solitary fibrous tumour, hemangiopericytoma, others
IHC EMA +ve, keratins usu. -ve, CD34 -ve/+ve, S-100 -ve (usu.), PR +ve (-ve in more aggressive ones)
Site see CNS tumours

Syndromes neurofibromatosis 2, nevoid basal cell carcinoma syndrome

Clinical history +/-radiation
Prevalence common
Radiology extra-axial, intradural lesion, dural tail sign (on MRI)
Prognosis usually benign, dependent on grade
Clin. DDx dependent on site - see CNS tumours
Treatment surgical removal

Meningioma a very common tumour in neuropathology.

General

Prevalence

  • Most common primary brain tumour.[1]
  • May be caused by prior radiation.[2]
  • Women develop meningioma twice as likely as men.[3]
  • More than 90% are solitary.

Prognosis

  • Most are benign - usu. a good prognosis.
    • Even benign tumors may show extensive local spread - considerable morbidity and mortality.
    • Metastases are rare and then usu. after surgery.
  • May be malignant - bad prognosis.
  • Factors associated with unfavourable prognosis:
    • BAP1 mutations.[4]
    • Presence of TERT promotor mutation.[5]
    • Loss of H3K27me3.[6]

Genetics

Quick overview

Name Histologic criteria Subtypes Image
Classic, WHO I less then 4 mit/10 HPF and no atypia meningeothelial, fibroblastic, transitional, psammomatous, angiomatous, microcytsic, secretory, lymphoplasmacyte-rich, metaplastic
Miningioma (1) transitional type.jpg
Atypical, WHO II brain invasion, 4 or more mit/10 HPF, or 3 of the following: necrosis, increased cellularity, high nuc:cyto ratio, nucleoli, sheeting chordoid, clear cell
Brain invasion meningioma.jpg
Anaplastic, WHO III 20 or more mitoses/10 HPF, morphologiy similiar to carcinoma or sarcoma rhabdoid, papillary
Mitoses anaplastic meningioma.jpg

Gross/Radiology

  • Extra-axial, intradural.
    • Can be extradural - very rare.[10]
  • Dural tail sign (DTS) on MRI.[11][12]
    • Enhancement of dura adjacent to the mass lesion - commonly seen (~70% of cases).[13]
    • May be subclassified radiologically - predictive of grading.[14]
  • +/-Hyperostosis.
    • Associated with invasion into the skull in ~20% of cases.[15]

Microscopic

Features (memory device WCN):

  • Whorled appearance - key feature.
  • Calcification, psammomatous (target-like appearance; (tight) onion skin).
  • +/-Nuclear pseudoinclusions - focal nuclear clearing with a sharp interface to unremarkable chromatin.

Notes:

  • May involute into benign sclerotic tissue.[16]
  • Thick-walled blood vessels -> think schwannoma.

DDx:

Images

www:

Morphologic subtypes

  • Many subtypes exist.[17]
  • The histologic subtypes generally don't have much prognostic significance.
    • Some subtypes are high grade by definition; also see histologic grading.

Grade I

Meningothelial meningioma
  • Most common.

Microscopic:

  • Syncytial, nuclear clearing (pseudoinclusions).
  • Whorls, Onion bulb formations.
  • Few psammoma bodies.

Molecular:

  • AKT E17K mutations.[18]
Fibrous meningioma
  • AKA fibroblastic meningioma.
  • Not collagen... but looks like it.
    • It is really laminin or fibronectin.
  • Spindle cells in parallel bundles.
  • Few to none whorl formations.
Transitional meningioma
  • AKA mixed.
  • Common.
  • Lobular and fasicular growth patterns coexist.
  • Usu. a mixture of meningeothelial and fibromatous meningioma
Psammomatous meningioma

Microscopic:

  • Psammoma bodies dominate over tumor cells.
    • Irregular calcifications (confluent psammoma bodies).
  • Usually found in spinal cord.
Angiomatous meningioma
  • AKA vascular.
  • May bleed like stink.
  • May show extensive edema.
  • Hyalinized vessels dominate over tumor cells.
  • Degenerative nuclear atypia.

DDx:

  • Vascular malformatons
  • Hemangioblastoma
Microcystic meningioma

Microscopic:

  • Cystic appearance.
  • Increased cytologic pleomorphism of the elongated cells.

DDx:

  • Clear cell meningioma
  • Hemangioblastoma
Secretory meningioma
  • Associated with brain edema; may have a worse outcome.

Microscopic:[19]

  • Eosinophilic intracytoplasmic inclusions that are CEA +ve and PAS +ve.

Molecular:

  • Combined KLF4 K409Q and TRAF7 mutations.[20]

DDx:

Images:

Lymphoplasmacyte-rich meningioma

Microscopic:

  • Lymphocytes.
  • Plasma cells.

Images:

Metaplastic meningioma
  • No clinical significance.
  • Probably do not represent true metaplasia in all cases.
  • Clincal information is rquired to distinguish between bone invasion and meningiomas with bone formation.

Microscopic:

  • Cartilage or bone formation.
  • Myxoid or xanthomatous changes.

Grade II

Brain invasive meningioma
  • Invades the brain (irregular, tongue-like).
  • Absence of leptomeningeal layer.
  • Brain invasion can be present in grade I tumors, these are then classified as "atypical", ie. as grade II tumors.
  • The prognostic significance of brain invasion is still unclear, some studies do not show a course similiar to grade II meningiomas.[22][23][24]

Images:

Clear cell meningioma

Epidemiology:

  • Usu. spinal cord.[25]

Microscopic:

  • Clear cells - contain glycogen (PAS +ve).

Molecular:

  • SMARCE1 mutations.[26]

Images:

Chordoid meningioma
  • Chordoma-like.

Microscopic:


Image:

Grade III

Papillary meningioma

Microscopic:

  • discohesive meningothelial tumour cells around a fibrovascular core.
  • perivascular pseudorosettes.
Rhabdoid meningioma

Microscopic:

  • Rhabdoid appearance (abundant cytoplasm).
    • Cross-striations.

www:

Other morphological variants

These are currently not listed in the WHO as separate entities.

  • Oncocytic.[27]
  • Whorling-sclerosing.[28]
  • Rosette-forming.[29]

Histologic grading

Grading:[17]

  • Grade 1:
    • Low mitotic rate (< 4 mitoses/10 HPF - for whatever HPF means, see HPFitis).
    • Excludes clear cell, chordoid, papillary, and rhabdoid subtypes.
  • Grade 2 (either #1, #2 or #3):
    1. Brain-invasive meningioma.
      • Invasion of meningioma into brain.
        • Meninogioma with entraped GFAP +ve tissue.
    2. Atypical meningioma (by histomorphology) - either A or B.
      • A. Intermediate mitotic rate (>= 4 mitoses/10 HPF - for whatever HPF means, see HPFitis.)
      • B. Three of the following five features:
        1. Sheeting architecture.
        2. High NC ratio clusters; clusters of "lymphocyte-like" cells.
        3. Hypercellularity.
        4. Macronucleoli.
        5. Necrosis not caused by treatment, e.g. radiation or embolization.
    3. Clear cell or chordoid subtype.
  • Grade 3 (either of the following):
    • High mitotic rate (>=20 mitoses/10 HPF - for whatever HPF means, see HPFitis.)
    • "Frank anaplasia"; marked nuclear atypia.
    • Papillary or rhabdoid subtype.

Notes:

  • Grade II soft criteria memory device HMNs: hypercellular, macronucleoli, NC ratio increased, necrosis, sheeting.

IHC

  • EMA +ve (approx. 90%).[30]
  • PR +ve (approx. 75%, expression decreases from grade I to III).
  • SSTR2A +ve (approx. 95%).
  • S100 variable (up to 35% cases, usually patchy).[31]
  • SOX10 -ve.
  • GFAP -ve.
  • CD34 usu. -ve (approx 8% cases positive).
  • CD13 +ve.[32]
  • Other CKs usually -ve (approx 6% cases positive, mostly secretory meningiomas).

Molecular

Non-syndromal meningiomas may show AKT1/TRAF7, SMO, KLF4/TRAF7, and PIK3CA mutations (1/3 of cases).[33]

  • AKT/TRAF7 mutations are usually basal and associated with meningothelial histology.
  • KLF4/TRAF7 mutations are highly specific for secretory histology.
  • TRAF7 mutations are the first step and occur thorughout the WD40 domain. [34]

Intraventricular meningiomas have NF2 mutations. [35]

Several inherited diseases are associated with meningiomas:

Methylation profiling distinguishes two major groups with six distinct clinically relevant methylation classes.[41]


DDx of meningioma & IHC[42]

A standard work-up

  • Ki-67 >5-10% - predicts re-occurrence.[45]
  • PR (progesterone receptor) +ve in > 80% of meningiomas.[46]
    • Loss of PR staining predicts recurrence.
    • Strong association with tumour grade:[47]
      • Low WHO grade tumours usu. +ve.
      • High WHO grade tumours usu. -ve.

See also

References

  1. Rogers, L.; Barani, I.; Chamberlain, M.; Kaley, TJ.; McDermott, M.; Raizer, J.; Schiff, D.; Weber, DC. et al. (Oct 2014). "Meningiomas: knowledge base, treatment outcomes, and uncertainties. A RANO review.". J Neurosurg: 1-20. doi:10.3171/2014.7.JNS131644. PMID 25343186.
  2. Baldi, I.; Engelhardt, J.; Bonnet, C.; Bauchet, L.; Berteaud, E.; Grüber, A.; Loiseau, H. (Sep 2014). "Epidemiology of meningiomas.". Neurochirurgie. doi:10.1016/j.neuchi.2014.05.006. PMID 25249493.
  3. Wiemels, J.; Wrensch, M.; Claus, EB. (Sep 2010). "Epidemiology and etiology of meningioma.". J Neurooncol 99 (3): 307-14. doi:10.1007/s11060-010-0386-3. PMID 20821343.
  4. Shankar, GM.; Abedalthagafi, M.; Vaubel, RA.; Merrill, PH.; Nayyar, N.; Gill, CM.; Brewster, R.; Bi, WL. et al. (04 2017). "Germline and somatic BAP1 mutations in high-grade rhabdoid meningiomas.". Neuro Oncol 19 (4): 535-545. doi:10.1093/neuonc/now235. PMID 28170043.
  5. Sahm, F.; Schrimpf, D.; Olar, A.; Koelsche, C.; Reuss, D.; Bissel, J.; Kratz, A.; Capper, D. et al. (May 2016). "TERT Promoter Mutations and Risk of Recurrence in Meningioma.". J Natl Cancer Inst 108 (5). doi:10.1093/jnci/djv377. PMID 26668184.
  6. Katz, LM.; Hielscher, T.; Liechty, B.; Silverman, J.; Zagzag, D.; Sen, R.; Wu, P.; Golfinos, JG. et al. (Apr 2018). "Loss of histone H3K27me3 identifies a subset of meningiomas with increased risk of recurrence.". Acta Neuropathol. doi:10.1007/s00401-018-1844-9. PMID 29627952.
  7. URL: http://moon.ouhsc.edu/kfung/jty1/neurotest/Q13-Ans.htm. Accessed on: 26 October 2010.
  8. Kimonis, VE.; Mehta, SG.; Digiovanna, JJ.; Bale, SJ.; Pastakia, B.. "Radiological features in 82 patients with nevoid basal cell carcinoma (NBCC or Gorlin) syndrome.". Genet Med 6 (6): 495-502. doi:10.109701.GIM.0000145045.17711.1C. PMID 15545745.
  9. Lee, CW.; Tan, TC. (Feb 2014). "Meningioma associated with Gorlin's syndrome.". J Clin Neurosci 21 (2): 349-50. doi:10.1016/j.jocn.2013.02.033. PMID 24100109.
  10. URL: http://path.upmc.edu/cases/case702.html. Accessed on: 2 February 2012.
  11. Ikeda, D.; Chiocca, EA. (Oct 2012). "Editorial: dural tail sign.". J Neurosurg 117 (4): 643-4. doi:10.3171/2012.2.JNS12266. PMID 22839655.
  12. Wen, M.; Jung, S.; Moon, KS.; Pei, J.; Lee, KH.; Jin, SG.; Li, SY.; Ryu, HH. (Dec 2014). "Immunohistochemical profile of the dural tail in intracranial meningiomas.". Acta Neurochir (Wien) 156 (12): 2263-73. doi:10.1007/s00701-014-2216-4. PMID 25238986.
  13. Aoki, S.; Sasaki, Y.; Machida, T.; Tanioka, H.. "Contrast-enhanced MR images in patients with meningioma: importance of enhancement of the dura adjacent to the tumor.". AJNR Am J Neuroradiol 11 (5): 935-8. PMID 2120998.
  14. Qi, ST.; Liu, Y.; Pan, J.; Chotai, S.; Fang, LX. (Oct 2012). "A radiopathological classification of dural tail sign of meningiomas.". J Neurosurg 117 (4): 645-53. doi:10.3171/2012.6.JNS111987. PMID 22839654.
  15. Goyal, N.; Kakkar, A.; Sarkar, C.; Agrawal, D.. "Does bony hyperostosis in intracranial meningioma signify tumor invasion? A radio-pathologic study.". Neurol India 60 (1): 50-4. doi:10.4103/0028-3886.93589. PMID 22406780.
  16. URL: http://radiographics.rsna.org/content/23/3/785.long. Accessed on: 3 November 2010.
  17. 17.0 17.1 Perry, Arie; Brat, Daniel J. (2010). Practical Surgical Neuropathology: A Diagnostic Approach: A Volume in the Pattern Recognition series (1st ed.). Churchill Livingstone. pp. 194. ISBN 978-0443069826.
  18. Sahm, F.; Bissel, J.; Koelsche, C.; Schweizer, L.; Capper, D.; Reuss, D.; Böhmer, K.; Lass, U. et al. (Nov 2013). "AKT1E17K mutations cluster with meningothelial and transitional meningiomas and can be detected by SFRP1 immunohistochemistry.". Acta Neuropathol 126 (5): 757-62. doi:10.1007/s00401-013-1187-5. PMID 24096618.
  19. URL: http://moon.ouhsc.edu/kfung/jty1/Com04/Com405-1-Diss.htm. Accessed on: 12 October 2011.
  20. Reuss, DE.; Piro, RM.; Jones, DT.; Simon, M.; Ketter, R.; Kool, M.; Becker, A.; Sahm, F. et al. (Mar 2013). "Secretory meningiomas are defined by combined KLF4 K409Q and TRAF7 mutations.". Acta Neuropathol 125 (3): 351-8. doi:10.1007/s00401-013-1093-x. PMID 23404370.
  21. URL: http://moon.ouhsc.edu/kfung/jty1/Com04/Com405-1-Diss.htm. Accessed on: 3 January 2012.
  22. Baumgarten, P.; Gessler, F.; Schittenhelm, J.; Skardelly, M.; Tews, DS.; Senft, C.; Dunst, M.; Imoehl, L. et al. (Sep 2016). "Brain invasion in otherwise benign meningiomas does not predict tumor recurrence.". Acta Neuropathol 132 (3): 479-81. doi:10.1007/s00401-016-1598-1. PMID 27464983.
  23. Brokinkel, B.; Hess, K.; Mawrin, C. (Apr 2017). "Brain invasion in Meningiomas - Clinical considerations and impact of neuropathological evaluation: A systematic Review.". Neuro Oncol. doi:10.1093/neuonc/nox071. PMID 28419308.
  24. Pizem, J.; Velnar, T.; Prestor, B.; Mlakar, J.; Popovic, M.. "Brain invasion assessability in meningiomas is related to meningioma size and grade, and can be improved by extensive sampling of the surgically removed meningioma specimen.". Clin Neuropathol 33 (5): 354-63. doi:10.5414/NP300750. PMID 25034703.
  25. Perry, Arie; Brat, Daniel J. (2010). Practical Surgical Neuropathology: A Diagnostic Approach: A Volume in the Pattern Recognition series (1st ed.). Churchill Livingstone. pp. 200. ISBN 978-0443069826.
  26. Smith, MJ.; Wallace, AJ.; Bennett, C.; Hasselblatt, M.; Elert-Dobkowska, E.; Evans, LT.; Hickey, WF.; van Hoff, J. et al. (Dec 2014). "Germline SMARCE1 mutations predispose to both spinal and cranial clear cell meningiomas.". J Pathol 234 (4): 436-40. doi:10.1002/path.4427. PMID 25143307.
  27. Zunarelli, E.; Tallarico, E.; Valentini, A.; Maiorana, A. (2010). "Oncocytic meningioma: study of eight new cases and analysis of 13 reported cases.". Pathology 42 (6): 587-9. doi:10.3109/00313025.2010.508740. PMID 20854082.
  28. Haberler, C.; Jarius, C.; Lang, S.; Rössler, K.; Gruber, A.; Hainfellner, JA.; Budka, H. (Feb 2002). "Fibrous meningeal tumours with extensive non-calcifying collagenous whorls and glial fibrillary acidic protein expression: the whorling-sclerosing variant of meningioma.". Neuropathol Appl Neurobiol 28 (1): 42-7. PMID 11849562.
  29. Liverman, C.; Mafra, M.; Chuang, SS.; Shivane, A.; Chakrabarty, A.; Highley, R.; Hilton, DA.; Byrne, NP. et al. (Aug 2015). "A clinicopathologic study of 11 rosette-forming meningiomas: a rare and potentially confusing pattern.". Acta Neuropathol 130 (2): 311-3. doi:10.1007/s00401-015-1456-6. PMID 26106026.
  30. Perry, Arie; Brat, Daniel J. (2010). Practical Surgical Neuropathology: A Diagnostic Approach: A Volume in the Pattern Recognition series (1st ed.). Churchill Livingstone. pp. 13. ISBN 978-0443069826.
  31. "The prognostic role of the immunohistochemical expression of S100 in meningiomas". J Cancer Res Clin Oncol. July 2022. doi:10.1007/s00432-022-04186-9. PMID 35838837.
  32. "CD13 is a useful tool in the differential diagnosis of meningiomas with potential biological and prognostic implications". Virchows Arch 480 (6): 1223–1230. June 2022. doi:10.1007/s00428-022-03304-9. PMC 9184408. PMID 35212813. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9184408/.
  33. Clark, VE.; Erson-Omay, EZ.; Serin, A.; Yin, J.; Cotney, J.; Ozduman, K.; Avşar, T.; Li, J. et al. (Mar 2013). "Genomic analysis of non-NF2 meningiomas reveals mutations in TRAF7, KLF4, AKT1, and SMO.". Science 339 (6123): 1077-80. doi:10.1126/science.1233009. PMID 23348505.
  34. "Single-cell DNA sequencing reveals order of mutational acquisition in TRAF7/AKT1 and TRAF7/KLF4 mutant meningiomas". Acta Neuropathol 144 (4): 799–802. October 2022. doi:10.1007/s00401-022-02485-6. PMID 35984495.
  35. "Intraventricular meningiomas frequently harbor NF2 mutations but lack common genetic alterations in TRAF7, AKT1, SMO, KLF4, PIK3CA, and TERT". Acta Neuropathol Commun 7 (1): 140. August 2019. doi:10.1186/s40478-019-0793-4. PMC 6716845. PMID 31470906. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6716845/.
  36. Fontaine, B.; Rouleau, GA.; Seizinger, BR.; Menon, AG.; Jewell, AF.; Martuza, RL.; Gusella, JF. (1991). "Molecular genetics of neurofibromatosis 2 and related tumors (acoustic neuroma and meningioma).". Ann N Y Acad Sci 615: 338-43. PMID 2039155.
  37. Smith, MJ.; O'Sullivan, J.; Bhaskar, SS.; Hadfield, KD.; Poke, G.; Caird, J.; Sharif, S.; Eccles, D. et al. (Mar 2013). "Loss-of-function mutations in SMARCE1 cause an inherited disorder of multiple spinal meningiomas.". Nat Genet 45 (3): 295-8. doi:10.1038/ng.2552. PMID 23377182.
  38. van den Munckhof, P.; Christiaans, I.; Kenter, SB.; Baas, F.; Hulsebos, TJ. (Feb 2012). "Germline SMARCB1 mutation predisposes to multiple meningiomas and schwannomas with preferential location of cranial meningiomas at the falx cerebri.". Neurogenetics 13 (1): 1-7. doi:10.1007/s10048-011-0300-y. PMID 22038540.
  39. Aavikko, M.; Li, SP.; Saarinen, S.; Alhopuro, P.; Kaasinen, E.; Morgunova, E.; Li, Y.; Vesanen, K. et al. (Sep 2012). "Loss of SUFU function in familial multiple meningioma.". Am J Hum Genet 91 (3): 520-6. doi:10.1016/j.ajhg.2012.07.015. PMID 22958902.
  40. Sievers, P.; Chiang, J.; Schrimpf, D.; Stichel, D.; Paramasivam, N.; Sill, M.; Gayden, T.; Casalini, B. et al. (Nov 2019). "YAP1-fusions in pediatric NF2-wildtype meningioma.". Acta Neuropathol. doi:10.1007/s00401-019-02095-9. PMID 31734728.
  41. Sahm, F.; Schrimpf, D.; Stichel, D.; Jones, DT.; Hielscher, T.; Schefzyk, S.; Okonechnikov, K.; Koelsche, C. et al. (Mar 2017). "DNA methylation-based classification and grading system for meningioma: a multicentre, retrospective analysis.". Lancet Oncol. doi:10.1016/S1470-2045(17)30155-9. PMID 28314689.
  42. Hahn HP, Bundock EA, Hornick JL (February 2006). "Immunohistochemical staining for claudin-1 can help distinguish meningiomas from histologic mimics". Am. J. Clin. Pathol. 125 (2): 203–8. doi:10.1309/G659-FVVB-MG7U-4RPQ. PMID 16393681. http://ajcp.ascpjournals.org/content/125/2/203.full.pdf.
  43. Agaimy, A.; Buslei, R.; Coras, R.; Rubin, BP.; Mentzel, T. (Jul 2014). "Comparative study of soft tissue perineurioma and meningioma using a five-marker immunohistochemical panel.". Histopathology 65 (1): 60-70. doi:10.1111/his.12366. PMID 24393170.
  44. Grunberg, SM. (1991). "The role of progesterone receptors in meningioma.". Cancer Treat Res 58: 127-37. PMID 1683782.
  45. Croul, SE. 8 November 2010.
  46. Takei, H.; Buckleair, LW.; Powell, SZ. (Feb 2008). "Immunohistochemical expression of apoptosis regulating proteins and sex hormone receptors in meningiomas.". Neuropathology 28 (1): 62-8. doi:10.1111/j.1440-1789.2007.00852.x. PMID 18021195.
  47. Tao, Y.; Liang, G.; Li, Z.; Wang, Y.; Wu, A.; Wang, H.; Lu, Y.; Liu, Z. et al. (May 2012). "Clinical features and immunohistochemical expression levels of androgen, estrogen, progesterone and Ki-67 receptors in relationship with gross-total resected meningiomas relapse.". Br J Neurosurg. doi:10.3109/02688697.2012.685780. PMID 22616825.