Literature Review

Key Aspects in Foramen Magnum Meningiomas: From Old Neuroanatomical

Conceptions to Current Far Lateral Neurosurgical Intervention

Daniel S. Leon-Ariza1,2, Alvaro Campero3, Rubby J. Romero Chaparro2, Diddier G. Prada4,5, Gabriel Vargas Grau2,6,Albert L. Rhoton Jr7,y

Foramen magnum meningiomas represent a challenge for neurosurgeons. Thesetumors require careful surgical manipulation as they are often located inproximity to critical neurovascular structures and the cranial nerves. The farlateral approach is considered the safest neurosurgical approach for excisingforamen magnum lesions. It facilitates the access to the anterior foramenmagnum and reduces the retraction of vital structures. We describe key his-torical, epidemiological, genetic, epigenetic, clinical, and neurosurgical aspectsof foramen magnum meningiomas. We emphasize the far lateral approach forlesions arising in the foramen magnum, as well as the most appropriate patientpositioning for such approach. Caring for these aspects will be rewarded withthe best perioperative neurosurgical outcomes.

Key words- Far lateral approach- Foramen magnum meningiomas- Microsurgical anatomy- Vertebral artery

Abbreviations and AcronymsCN: Cranial nerveFLA: Far lateral approachFM: Foramen magnumFMM: Foramen magnum meningiomasVA: Vertebral artery

From the 1Department of Neurosurgery, Johns HopkinsUniversity, Baltimore, Maryland, USA; 2Faculty of HealthSciences, University of SantandereUDES, Bucaramanga,Colombia; 3Department of Neurosurgery, Hospital Padilla,Tucumán, Argentina; 4Department of Environmental Health,Harvard T.H. Chan School of Public Health, HarvardUniversity, Boston, Massachusetts, USA; 5Unit of BiomedicalResearch in Cancer, National Institute of Cancerology,Institute of Biomedical ResearcheUNAM, Mexico City,Mexico; 6Division of Neurosurgery, Hospital Universitario deBucaramanga Los Comuneros, Bucaramanga, Colombia; and7Department of Neurological Surgery, University of Florida,Gainesville, USA

To whom correspondence should be addressed:Daniel S. Leon-Ariza, M.D.[E-mail: dleonariza@gmail.comyThis publication is dedicated to Dr. Albert Rhoton, Jr. He leftus with his amazing spirit of compassion, thoughtfulness, aswell as his unique way to see the world and the infinitegalaxy that the human brain has yet to be discovered.

Citation: World Neurosurg. (2017) 106:477-483.http://dx.doi.org/10.1016/j.wneu.2017.07.029

Journal homepage: www.WORLDNEUROSURGERY.org

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INTRODUCTION

The foramen magnum (FM) is ananatomical region near the medullaoblongata, at the lower half of the brain-stem; importantly, lower cranial nerves(CNs) and vertebral arteries are positionedwithin this region.1,2 Several techniquesdescribing how to better approach FM le-sions have been published. Such tech-niques include lateral-suboccipital,posterior midline suboccipital, extremelateral, endoscopic endonasal, and

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stereotactic radiosurgery, among others.1-9

When meningiomas are located in the FM,the far lateral approach (FLA) is one of themost delicate neurosurgical interventionsused to remove these tumors.10 We aim topresent a state-of-the-art narrative reviewof neuroanatomical descriptions on FMand introduce a detailed surgical approachand timeline for removing foramen mag-num meningiomas (FMMs) using FLA. Toaccomplish this aim, we report a thor-oughly surgical timeline of a patient whohad FMM in whom the FLA was used. Afull surgical description of this patient isbeyond this article.

KEY HISTORICAL ASPECTS

FMMs are histologically considered ascommon brain tumors within a rare loca-tion.11 Ancient descriptions onmeningiomas were made since AndreasVesalio’s humani corporis fabrica in 1543.12

The first reported autopsy of ameningioma was made by Salzmann in1730 on a patient with behavioral changes,headaches, vertigo, and seizures as themain cause of death.13 Illustrationsfollowed in 1849 by Cruveilhier, whopublished his Traité d’Anatomie PathologiqueGénérale and his initial description of afungus durae matris.14 In 1851, Lebert namedthese tumors tumeurs fibro-plastiques.15

Further surgical reviews made by Sir

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James Paget in 1854 classified thesetumors as “less malignant than cancer.”14

Bennett, in 1858, described the tumor asan epithelial cancer.14 FMMs were firstreported as an incidental postmortemfinding by Hallopeau from an autopsymade in 1872.16,17 Other key historicaldescriptions are detailed inTable 1.24,18,23,21,20,19

Harvey Cushingmade important advancesin the field and in 1992 published anoutstanding monography entitled Meningi-omas.22 By that time, the removal of a tumorlocated in the cervicomedullary junctionwith extension into the posterior fossa wasalso reported by Frazier and Spiller.25 In1929, Elsberg and Strauss reported the firstsurgical resection of a cervicomedullarytumor through a suboccipital craniectomyusing a C1-C3 laminectomy.26 In 1938,Cushing later reported the tumor as a “duralendothelioma,” a tumor arising mainlyfrom the brain and spinal meningealsheets.27 Cushing also did a comprehensiveneurosurgical documentation on the topicbased on 313 patients with meningioma,known by that time as a neurosurgicalmasterpiece.23,27 In 1986, Heros28

introduced the FLA for the management ofvertebral artery (VA) aneurysms at thevertebrobasilar junction, proximal basilartrunk, and arteriovenous malformations ofthe inferolateral cerebellum. In 1988,George et al29 introduced the FLA for

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Table 1. Historical Timeline ofAnatomopathological Descriptions ofMeningiomas

ReferenceInitial TumorDescription

Salzmann, 173013 Exostosis seuexcrescentia craniiosseo-spongiosa

Bright, 183118 Fungoid tumor

Pecchioli, 183819 Fungus of the duramater

Cruveilhier, 194914 Fungus durae matris

Lebert, 185115 Tumeurs fibro-plastiques

Meyer, 185920 Epithelioma

Virchow, 185920 Psammoma

Durante, 188721 Fibrosarcoma

Cushing, 192222 Meningioma

Cushing, et al., 193823 Dural endothelioma

LITERATURE REVIEW

DANIEL S. LEON-ARIZA ET AL. KEY ASPECTS IN FORAMEN MAGNUM MENINGIOMAS

removal of lesions involving the anterior andanterolateral FM. Currently, microvasculardecompression is considered as anothersurgical standard in neurosurgery, due tothe challenge that FLA represents inFMM.22,30-32

KEY EPIDEMIOLOGICAL ASPECTS

Meningiomas are the most common benignand primary brain tumors in adults. Theincidence of these tumors is up to 3.2% ofall intracranial meningiomas.33 Amongthem, FMMs represent about 3.2% ofmeningiomas that are located in the FM.34

On the basis of the anatomicalcompartment, involved FMMs are classifiedas intradural, extradural, or intradural andextradural.35 Intradural FMMs are thensubclassified as anterior, posterior, andlateral.36 Common anatomical locations ofFMMs include anterior, followed byanterolateral and posterolateral.37 FMMsare also classified with regard to VA asabove, below, or bilateral. In thisclassification, the most common locationof FMM is below the VA.36 Meningiomasrepresent about 77% of all benignintramedullary, extramedullary, andintradural extramedullary tumors, withmost of these tumors located intraduraland extramedullar.36 FMMs have also beenfound incidentally at the craniocervical

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junction.34,38 The mean age of presentationof FMM in adults is 55 � 4.2 yearsold.1,4,16,39 Females are usually moreaffected than men.31,40-43 Tumorpresentation could be classified asaggressive and nonaggressive.44 Usually,benign presentations of these tumors havenonaggressive clinical presentations,whereas local invasion leads to a moreaggressive presentation.16

In children, meningiomas in childrenhave an incidence of 0.4%e4.6% of allcentral nervous system malignancies.40

Almost 4% of these tumors are found inmales.45,46 These tumors tend to belocated highly at the cervical spine, overthe craniocervical junction; when thetumors become symptomatic, symptomsresemble those from adults.47 FMMs areconsidered a rare type of primary braintumors in children.40

KEY MOLECULAR ASPECTS

Familial genetic syndromes such asLiFraumeni, Turcot, Gardner, Gorlin, andMEN1 predispose for the presentation ofmeningiomas.48,49 An associationbetween type 2 neurofibromatosis andmutations in chromosome 22q has beenfound. In these cases, gene-tumor pre-sentation is related to aggressive tumoralbehavior and clinical manifestations relyon histopathological findings and highermalignancy rates.49-52

Epigenetics is another key aspect inFMM. Epigenetics relates to changes ingene expression patterns that do notdepend on changes in DNA sequence.53

Epigenetic marks are established duringearly development and modified duringcarcinogenesis.54 These cancer-relatedepigenetic changes are frequently observedin meningiomas that include aberrant pro-moter methylation, disturbed chromatinorganization, and abnormal microRNAexpression.49 Some of these aberrantepigenetic changes have been associatedwith tumor aggressiveness and thepotential of invasiveness; such changeshave been also associated with clinicalstages of the disease.49,55,56 Chromosomalinstability, potentially linked to epigeneticaberrations in heterochromatin regionssuch as centromeric and pericentromericregions where mutations and aneuploidycorrelate, is seen in most solidcancer tumors and should also be

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considered in meningiomas.57 Cases suchas chromosome 1p deletion have beenassociated with recurrence and progressionin meningiomas.58 Additionally, signalingpathway aberrations, such as TFG:ROS1fusionerelated tumor growth in the c-rosoncogene 1 (ROS-1) signaling pathway,have often been found in the pediatricpopulation with simultaneous presentationof meningiomas and type 2neurofibromatosis.59 Gene inactivation ofBAM22, BCR, TIM-1 on chromosomal 22qregion and MEG3, NDRG2 on chromosome14q region have been also associatedwith the presentation of high-grademeningiomas.49,60

KEY CLINICAL ASPECTS

Clinical presentation of meningiomas islocation dependent. When the primarylesion is supratentorial, patients tend todevelop orthostatic headache, secondary toirritation of the leptomeningeal sheets.61

Should papilledema be found, the courseof visual impairment is due to the masseffect these tumors produce over theoptic chiasm.62 When a diagnosis ofprimary extradural meningioma is made,compressive signs and symptoms arepresent in more advanced stages of thedisease depending on location and extentof the tumor.63 Another location-relatedsymptoms include facial nerve palsy,dizziness, diplopia, and hearing distur-bances.64 In cases where recurrence isfound, the Simpson grading system usedfor meningioma recurrence must beapplied.65-67

Symptoms of FMM include gait ataxia,suboccipital headache, and cervical pain.These symptoms are exacerbated by Val-salva maneuvers and cough.16,46 Some-times FMM may mimic nervous systemdisorders such as amyotrophic lateralsclerosis, multiple sclerosis, and evencompressive-like presentations such asnormal pressure hydrocephalus, cervicalspondylopathy, carpal tunnel syndrome,and intramedullary tumors.68

FM syndrome due to transoperativechanges on lumbar cerebrospinal fluiddrainage in Chiari malformation type I hasinduced quadriparesis and late-onset car-diopulmonary arrest.1,69-72 Muscle atrophydue to spinal cranial nerve (CN XI) deficitfollowing FMM compressive effects hasbeen found simultaneously with injury over

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lower cranial nerves.72 Sternocleidomastoidmuscle and trapezius muscle atrophy withhypoglossal cranial nerve (CN XII) palsy,hoarseness, dysphagia, and tonguedeviation could also appear in casesinvolving lower cranial nervecompression.72,73 Dysarthria, gait ataxia,and hemihyperesthesia have also beendescribed in FMM.34 In rare occasions,lower limb anomalies along with suddenfalls without loss of conscience have alsobeen reported.31 FMM may also debut asa subarachnoid hemorrhage.74

Figure 1. Patient head positioning and dural exposure. (A) Patient head positioning and hockey-stickincision demarcation. (B) Scalene muscle retraction. (CeF) Occiput and dural exposure with furtheropening and exposure.

KEY NEUROSURGICAL ASPECTS

Several approaches have been used toremove FMM; however, limitationsapply. For instance, the midlineapproach in suboccipital craniotomylimits the lateral dissection for visuali-zation of the extracranial VA. The sub-occipital approach allows visualizing themedulla when a C1 laminectomy needsto be done, as well as when making aposterolateral exposure; however, thisapproach is limited when an aggressiveand extensive exposure is made. Thelateral extension of the midline approachis limited due to a major anatomicalexposure of key neurovascularstructures.36,75

In neurosurgery, patient positioningplays an important role in outcomes.Germane to this work, the head of thepatient should be carefully placed in aneutral position. In light of this, priorneck flexion positioning of the individualmust be avoided because it worsens theneuroaxis compression.65 Using thementioned positioning, the FLA hasshown fewer complications comparedwith approaches such as midline,suboccipital, and posterolateral, whichmay increase perioperative morbiditydue to its aggressive and extensiveexposure.76,77

Cerebrospinal fluid fistulae and pseudo-meningocele could appear when a majorsurgical exposure of the hypoglossal canal ismade.78 Intraoperative monitoring of motorand somatosensory evoked potentials isrecommended when manipulation of CNVII and CN XI is considered.79 Skinincision should be carefully addressedconsidering the approach to the C2spinous process and throughout thecraniocervical junction.80-83

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FLA SURGICAL TECHNIQUE

After adequate patient positioning andtrichotomy, antiseptic measures should becarried out with povidone, benzoin, andthe like to guarantee safeness when mak-ing the approach.84 A hockey stickeshaped incision is made in the skin withprior zone demarcation; use of bipolarcoagulation is recommended to avoidbleeding of scalp vessels. One limb ofthe incision was made in the midline,beginning below the spinous process ofC3 with extension above the inion(Figure 1A).82 The horizontal incision

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extends from the inion toward themastoid process, and then the approachextends below the mastoid process andupward the horizontal incision withipsilateral scalene exposure (Figure 1B).The transverse sinus and sigmoid sinusis paralleled, providing the possibility oflaterally folding a mucocutaneous flap.This approach allows exposing theocciput and arch of C1 out to thetransverse process angulation (Figure 1Cand D).83,85

After this step is completed, soft tissueis located and periosteal dissectors, as well

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as monopolar cautery, are used to exposethe anatomical landmarks. Simulta-neously, ipsilateral occiput is cleared fromthe soft tissue to the FM. Next, FM isexposed until the mastoid process curvesmedially and anteriorly.86,87 C1 lamina isexposed laterally until palpation of C1process below the oblique muscles withinthe suboccipital triangle.88,89 The sub-occipital triangle is composed by therectus capitis posterior major, superioroblique, and inferior oblique muscles; itsfloor is formed by the posterior atlanto-occipital membrane, where the terminalextradural VA and first and second cervicalneural roots are located. The course of theVA is then identified, outlined, and safelymobilized. The intravascular and peri-vascular plexus should be controlled withcautery. The posterior portion of thetransverse foramen is then removed by adrill. It allows releasing of the VA poste-riorly and mobilization from the occipitalcondyle, and protection of the VA with avessel loop should be carefullyaddressed.8,88-92

Unilateral suboccipital craniotomy andC1 hemilaminectomy are done by a

Figure 2. Far lateral approach microsurgical anatomy ehemilaminectomy; (B) Dural dissection away from bosheet mobilization for vertebral artery protection; (D)between posterolateral and transcondylar approach. *approach; B.s, brainstem; Cn: condyle; PICA, posterotonsil; V.a, vertebral artery; XI, accessory nerve.

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J-shaped plate of the hemioccipital bonefor formation of the bone flap(Figure 1E).83 The medial vertical limb ofthe bone flap then extends upward fromthe FM to the transverse sinus(Figure 1F). The lateral vertical limbextends from the asterion and thenfurther extends as an inferomedial curvedline, reaching the FM as laterally aspossible. The horizontal limb connectsthe upper portions of the vertical limbsand parallels the transverse sinus. A C1hemilaminectomy lengthens the duralincision, which is made using a side-cutting bur with a footplate (Figure 2A).83

Once C1 hemilaminectomy is done,retrosigmoid mastoidectomy is achievedby exposure of the transverse andsigmoid sinuses from the torcularHerophili to the beginning of the jugularbulb for the superolateral extent of thedural incision. For tumor extraction inthe FM, a wider exposure of the durashould be obtained. In this stage, duraldissection is made away from the bone,drill bone is thinned, and removal of theKerrison punch is completed(Figure 2B).85

xposure of the foramen magnum (FM). (A) C1ne; (C) Occipital condyle drilling with prior duralComplete FM exposure and comparisonPosterolateral approach; **Transcondylarinferior cerebellar artery; S.s, sigmoid sinus; T,

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In a timely fashion, occipital condyledrilling allows the anterior visualizationthat the FLA provides. A minimal amountof condyle can be removed before occipito-cervical fusion is considered. Retractionand mobilization of the dural sheet sur-rounding the VA guarantees preservation ofadjacent structures (Figure 2C). Protectionof the VA should be carefully done beforedrilling.42 The far lateral exposure alsoprovides access for the followingneurosurgical approaches: First, thetranscondylar approach directed throughthe occipital condyle allows access to thelower clivus and premedullary area;second, the supracondylar approach ismade through the area above the occipitalcondyle to the hypoglossal canal andjugular tubercle; and, third, thetranscondylar exposure through the lateralarea to the occipital condyle is done. Itincludes drilling of the jugular process inthe area lateral to the occipital condyle toaccess the posterior portion of the jugularforamen and to the mastoid on the lateralside of the jugular foramen (Figure 2D).93

A dural incision is made as a J-shapedincision, using a scalpel and continuedwith Metzenbaum scissors, surroundingthe dura from the transverse-sigmoidjunction curving medially and inferiorlyfor posterior crossing of the FM to theintradural entry point of the VA.93,94 Cer-vical dura should be opened linearly andparalinearly downwards to at least the C2lamina, and the dura should be reflectedanteriorly as deeply as possible.Lastly, microsurgical removal is achieved

by using Cavitron ultrasonic surgical aspi-ration, microbipolar coagulation, andmicrosurgical instruments.29 After thetumor is removed and hemostasis isaccomplished, closure of the dura is done.When it is not possible, dural substitutescan be used for hemostasis. The occipitalbone fragment is replaced and then fixed.The muscles are reattached, and theaponeurosis, subcutaneous tissue, andskin closure are attained.

CONCLUSIONS

FMMs have been a challenge to neuro-surgeons for centuries. A perfect knowl-edge of the surgical anatomy is the mostimportant requisite to safely perform theexposure. Since Andreas Vesalio’s humananatomical dissections to current times,

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several techniques have been used fortreating FM lesions; however, the FLA hasbecome the safest intervention to solve it.This approach shows less mortality andmorbidity rate than other neurosurgicalapproaches. This microsurgical approachprotects vital neurovascular structures,allowing a careful approach to the VA andlower cranial nerves. Having said this, itbecomes mandatory in neurosurgical ed-ucation to distribute tasks in the surgicalscenario for the improvement of patientsafety, applying state-of-the-art materialsand techniques. Future generations ofneurosurgeons will benefit by having amore comprehensive view of not only theanatomy of FM based on historical roots ofhuman brain studies but also the advancesmade to apply safer neuroanatomical ap-proaches such as the far lateral one.

REFERENCES

1. Boulton MR, Cusimano MD. Foramen magnummeningiomas: concepts, classifications, and nu-ances. Neurosurg Focus. 2003;14:51-59.

2. Komotar RJ, Zacharia BE, McGovern RA,Sisti MB, Bruce JN, D’Ambrosio AL. Approachesto anterior and anterolateral foramen magnumlesions: a critical review. J Craniovertebr JunctionSpine. 2010;1:86-99.

3. Cheshier SH, Hanft SJ, Adler JR, Chang SD.CyberKnife radiosurgery for lesions of the fora-men magnum. Technol Cancer Res Treat. 2007;6:329-336.

4. Goel A, Desai K, Muzumdar D. Surgery on ante-rior foramen magnum meningiomas using aconventional posterior suboccipital approach: areport on an experience with 17 cases. Neurosur-gery. 2001;49:102-107.

5. Kassam A, Snyderman CH, Mintz A, Gardner P,Carrau RL. Expanded endonasal approach: therostrocaudal axis. Part I. Crista galli to the sellaturcica. Neurosurg Focus. 2005;19:E3.

6. Kassam A, Snyderman CH, Mintz A, Gardner P,Carrau RL. Expanded endonasal approach: therostrocaudal axis. Part II. Posterior clinoids to theforamen magnum. Neurosurg Focus. 2005;19:E4.

7. Muthukumar N, Kondziolka D, Lunsford LD,Flickinger JC. Stereotactic radiosurgery for ante-rior foramen magnum meningiomas. Surg Neurol.1999;51:268-273.

8. Nicolato A, Foroni R, Pellegrino M, Ferraresi P,Alessandrini F, Gerosa M, et al. Gamma Kniferadiosurgery in meningiomas of the posteriorfossa. Experience with 62 treated lesions. MinimInvasive Neurosurg. 2001;44:211-217.

9. Salas E, Sekhar LN, Ziyal IM, Caputy AJ,Wright DC. Variations of the extreme-lateral cra-niocervical approach: anatomical study and

WORLD NEUROSURGERY 106: 477-483,

clinical analysis of 69 patients. J Neurosurg. 1999;90(suppl 2):206-219.

10. Singh H, Patir R, Vaishya S, Gupta A, Miglani R.Application of far-lateral approach to sub-axialspine—application, technical difficulties and re-sults. World Neurosurg. 2017;100:167-172.

11. Jurinovic P, Bulicic AR, Marcic M, Mise NI,Titlic M, Suljic E. Foramen magnum meningioma:a case report and review of literature. Acta InformMed. 2016;24:74-77.

12. Gomes M, Moscovici M, Engelhardt E. AndreasVesalius as a renaissance innovative neuroanato-mist: his 5th centenary of birth. Arq Neuropsiquiatr.2015;73:155-158.

13. Salzmann J. [Exostosis or excrescences of the skullbone-porous.]. Acta Physio-Med. 1730;2:225-228[Latin].

14. Cruveilhier J. Treaty of general anatomical pathology[Traité d’Anatomie pathologique générale]. Paris: J. B.Ballière; 1849.

15. Lebert H. [Excess cancer and the cancer-confounded tumors in the brain and its sheets.].Virchows Arch. 1851;3:462-569 [German].

16. Bassiouni H, Ntoukas V, Asgari S,Sandalcioglu EI, Stolke D, Seifert V. Foramenmagnum meningiomas: clinical outcome aftermicrosurgical resection via a posterolateral sub-occipital retrocondylar approach. Neurosurgery.2006;59:1177-1185.

17. Hallopeau H. [Note about two cases of tumors ofthe mesencephalon.]. Gaz Med Paris. 1874;3:2[French].

18. Bright R. Reports of medical cases, symptoms andmorbid anatomy. In: Bright R, ed. Diseases of theBrain and Nervous System. London, England: Long-man; 1831. Vol. 2, part I, 342-347.

19. Pecchioli Z. [History of a fungus of duramateroperated and extirpated from professor ZanobiPecchioli.]. Nuovo Giorn dei Letterati-Scienze. 1838;36:39-44 [Italian].

20. Meyer L. The epithelial granulations of thearachnoides. Virchows Arch. 1859;17:209-227[German].

21. Durante F. Contribution to endocranial surgery.Lancet. 1887;2:654-655.

22. Cushing H. The meningiomas (dural endotheli-omas): their source and favoured seats of origin.Brain. 1922;45:282-316.

23. Cushing H, Eisenhardt L. Meningiomas: Their Clas-sification, Regional Behaviour, Life History, and SurgicalEnd Results. Springfield, IL: Charles C Thomas;1938.

24. al-Rodhan NR, Laws ER. Meningioma: a histori-cal study of the tumor and its surgical manage-ment. Neurosurgery. 1990;26:832-846 [discussion:847].

25. Frazier C, Spiller W. An analysis of fourteenconsecutive cases of spinal cord tumor. Arch NeurolPsychiatr (Chicago). 1922;8:455-501.

OCTOBER 2017 ww

26. Elsberg CA, Strauss I. Tumors of the spinal cordwhich project into the posterior cranial fossa.Report of a case in which a growth was removedfrom the ventral and lateral aspects of the medullaoblongata and upper cervical cord. Arch NeurolPsychiatry. 1929;21:261-273.

27. Pendleton C, Olivi A, Brem H, Quiñones-Hinojosa A. Harvey Cushing’s early treatment ofmeningiomas: the untold story. World Neurosurg.2013;80:217-221.

28. Heros RC. Lateral suboccipital approach forvertebral and vertebrobasilar artery lesions.J Neurosurg. 1986;64:559-562.

29. Moscovici S, Umansky F, Spektor S. “Lazy” far-lateral approach to the anterior foramen magnumand lower clivus. Neurosurg Focus. 2015;38:E14.

30. Li D, Wu Z, Ren C, Hao SY, Wang L, Xiao XR,et al. Foramen magnum meningiomas: surgicalresults and risks predicting poor outcomes basedon a modified classification. J Neurosurg. 2017;126:661-676.

31. Meyer FB, Ebersold MJ, Reese DF. Benign tumorsof the foramen magnum. J Neurosurg. 1984;61:136-142.

32. Stein BM, Leeds NE, Taveras JM, Pool JL. Me-ningiomas of the foramen magnum. J Neurosurg.1963;20:740-751.

33. Yamahata H, Yamaguchi S, Takayasu M,Takasaki K, Osuka K, Aoyama M, et al. Exploita-tion of simple classification and space created bythe tumor for the treatment of foramen magnummeningiomas. World Neurosurg. 2016;87:1-7.

34. Arnautovic KI, Al-Mefty O, Husain M. Ventralforamen magnum meningiomas. J Neurosurg.2000;92(Spine 1):71-80.

35. Bernard F, Lemee JM, Delion M, Fournier HD.Lower third clivus and foramen magnum intra-dural tumor removal: the plea for a simpleposterolateral approach. Neurochirurgie. 2016;62:86-93.

36. Bruneau M, George B. Foramen magnum me-ningiomas: detailed surgical approaches andtechnical aspects at Lariboisière Hospital and re-view of the literature. Neurosurg Rev. 2008;31:19-33.

37. Kandenwein JA, Richter H-P, Antoniadis G. Fo-ramen magnum meningiomas-experience withthe posterior suboccipital approach. Br J Neurosurg.2009;23:33-39.

38. Gilsbach JM. Extreme lateral approach to intra-dural lesions of the cervical spine and foramenmagnum. Neurosurgery. 1991;28:779.

39. George B, Lot G, Boissonnet H. Meningioma ofthe foramen magnum: a series of 40 cases. SurgNeurol. 1997;47:371-379.

40. Ben Nsir A, Boubaker A, Jemel H. Cervico-oc-cipital meningioma in a 5-year-old child: a casereport. Turk Neurosurg. 2014;24:131-134.

41. Borba LAB, De Oliveira JG, Giudicissi-Filho M,Colli BO. Surgical management of foramen mag-num meningiomas. Neurosurg Rev. 2009;32:49-59.

w.WORLDNEUROSURGERY.org 481

LITERATURE REVIEW

DANIEL S. LEON-ARIZA ET AL. KEY ASPECTS IN FORAMEN MAGNUM MENINGIOMAS

42. Seçkin H, Ates Ö, Bauer AM, Baskaya MK.Microsurgical anatomy of the posterior spinal ar-tery via a far-lateral transcondylar approach.J Neurosurg Spine. 2009;10:228-233.

43. Wu Z, Hao S, Zhang J, Zhang L, Jia G, Tang J,et al. Foramen magnum meningiomas: experi-ences in 114 patients at a single institute over 15years. Surg Neurol. 2009;72:376-382.

44. McCarthy C, Hofer M, Vlychou M, Khundkar R,Critchley P, Cudlip S, et al. Metastatic meningi-oma presenting as a malignant soft tissue tumour.Clin Sarcoma Res. 2016;6:23.

45. Gao X, Zhang R, Mao Y, Wang Y. Childhood andjuvenile meningiomas. Child’s Nerv Syst. 2009;25:1571-1580.

46. Kotecha RS, Junckerstorff RC, Lee S, Cole CH,Gottardo NG. Pediatric meningioma: current ap-proaches and future direction. J Neurooncol. 2011;104:1-10.

47. Athanasiou A, Magras I, Sarlis P, Spyridopoulos E,Polyzoidis K. Anterolateral meningioma of theforamen magnum and high cervical spine pre-senting intradural and extradural growth in achild: case report and literature review. Child’s NervSyst. 2015;31:2345-2351.

48. Leon-Ariza DS, Leon-Ariza JS, Leon-Sarmiento FE. “Unclassical” combination of smelldysfunction, altered abdominal nociception andhuman hypertension associated “classical” adre-nal-augmentation. J Med Cases. 2015;6:527-533.

49. Mawrin C, Perry A. Pathological classification andmolecular genetics of meningiomas. J Neurooncol.2010;99:379-391.

50. Durand A, Labrousse F, Jouvet A, Bauchet L,Kalamaridès M, Menei P, et al. WHO grade II andIII meningiomas: a study of prognostic factors.J Neurooncol. 2009;95:367-375.

51. Ohgaki H, Kleihues P. Genetic alterations andsignaling pathways in the evolution of gliomas.Cancer Sci. 2009;100:2235-2241.

52. Perry A, Stafford SL, Scheithauer BW, Suman VJ,Lohse CM. Meningioma grading: an analysis ofhistologic parameters. Am J Surg Pathol. 1997;21:1455-1465.

53. Ning B, Li W, Zhao W, Wang R. Targetingepigenetic regulations in cancer. Acta Biochim Bio-phys Sin (Shanghai). 2015;48:97-109.

54. Kishida Y, Natsume A, Kondo Y, Takeuchi I,An B, Okamoto Y, et al. Epigenetic subclassifi-cation of meningiomas based on genome-wideDNA methylation analyses. Carcinogenesis. 2012;33:436-441.

55. Murnyák B, Bognár L, Klekner Á, Hortobágyi T.Epigenetics of meningiomas. Biomed Res Int. 2015;2015:532451.

56. Tsai HC, Baylin SB. Cancer epigenetics: linkingbasic biology to clinical medicine. Cell Research.2011;21:502-517.

482 www.SCIENCEDIRECT.com

57. Herrera LA, Prada D, Andonegui MA, Dueñas-González A. The epigenetic origin of aneuploidy.Curr Genomics. 2008;9:43-50.

58. Esteller M. Cancer epigenetics for the 21st century:what’s next? Genes Cancer. 2011;2:604-606.

59. Rossing M, Yde CW, Sehested A, Østrup O,Scheie D, Dangouloff-Ros V, et al. Genomic di-agnostics leading to the identification of a TFG-ROS1 fusion in a child with possible atypicalmeningioma. Cancer Genet. 2017;212-213:32-37.

60. Riemenschneider MJ, Perry A, Reifenberger G.Histological classification and molecular geneticsof meningiomas. Lancet Neurol. 2006;5:1045-1054.

61. Linsler S, Kraemer D, Driess C, Oertel K,Kammers K, Rahnenfuhrer J, et al. Molecularbiological determinations of meningioma pro-gression and recurrence. PLoS One. 2014;9:e94987.

62. Smith RM, Robertson CE, Garza I. Orthostaticheadache from supratentorial meningioma. Ceph-alalgia. 2015;35:1214.

63. Bettaswamy G, Ambesh P, Das KK, Sahu R,Srivastava A, Mehrotra A, et al. Extradural spinalmeningioma: revisiting a rare entity. J CraniovertebrJunction Spine. 2016;7:65-68.

64. Sahinoglu-Keskek N, Soker G, Keskek SO,Sahinoglu S, Unal F, Unal F, et al. A frontal lobemeningioma in a child leading to visual loss. CaseRep Ophthalmol Med. 2015;2015:420964.

65. Liu Y, Wang H, Shao H, Wang C. Primary extra-dural meningiomas in head: a report of 19 casesand review of literature. Int J Clin Exp Pathol. 2015;8:5624-5632.

66. Maroon JC, Kennerdell JS, Vidovich DV, Abla A,Sternau L. Recurrent spheno-orbital meningioma.J Neurosurg. 1994;80:202-208.

67. Violaris K, Katsarides V, Sakellariou P. Therecurrence rate in meningiomas: analysis of tumorlocation, histological grading, and extent ofresection. Open J Modern Neurosurg. 2010;2:6-10.

68. Xue H, Sveinsson O, Tomson T, Mathiesen T.Intracranial meningiomas and seizures: a reviewof the literature. Acta Neurochir (Wien). 2015;157:1541-1548.

69. Alegre S, García-Rubira JC, Patrignani G. Cardiacarrest in a 31-year-old man because of the Arnold-Chiari malformation. Int J Cardiol. 1994;46:286-288.

70. Ali MM, Russell N, Awada A, McLean D. A cranio-cervical malformation presenting as acute respi-ratory failure. J Emerg Med. 1996;14:569-572.

71. Dagnew E, Van Loveren HR, Tew JM. Acute fo-ramen magnum syndrome caused by an acquiredChiari malformation after lumbar drainage of ce-rebrospinal fluid: report of three cases. Neurosur-gery. 2002;51:823-829.

72. Rhoton AL. Meningiomas of the cerebellopontineangle and foramen magnum. Neurosurg Clin N Am.1994;5:349-377.

WORLD NEUROSURGERY, http://

73. Bakar B. Jugular foramen meningiomas: review ofthe major surgical series. Neurol Med Chir (Tokyo).2010;50:89-96 [discussion: 97].

74. Yasuoka S, Okazaki H, Daube JR, MacCarty CS.Foramen magnum tumors. Analysis of 57 cases ofbenign extramedullary tumors. J Neurosurg. 1978;49:828-838.

75. Bertalanffy H, Seeger W. The dorsolateral, sub-occipital, transcondylar approach to the lowerclivus and anterior portion of the craniocervicaljunction. Neurosurgery. 1991;29:815-821.

76. Sanai N, McDermott MW. A modified far-lateralapproach for large or giant meningiomas of theposterior fossa. J Neurosurg. 2010;112:907-912.

77. Wu B, Chen LY, Huang GF, Liu WD. Disposal ofoccipital condyle in far lateral approach forventrolateral foramen magnum meningiomas.World Neurosurg. 2016;93:29-37.

78. Menezes AH. Surgical approaches: postoperativecare and complications “posterolateral-far lateraltranscondylar approach to the ventral foramenmagnum and upper cervical spinal canal.”. Child’sNerv Syst. 2008;24:1203-1207.

79. Calzada G, Isaacson B, Yoshor D, Oghalai JS.Surgical approaches to the hypoglossal canal. SkullBase. 2007;17:187-196.

80. Aoyama Y-I, Ohta S, Sakaki S, Fujita T. [Foramenmagunum meningioma presented as subarach-noid haemorrhage]. No Shinkei Geka. 2015;43:445-450 [Japanese].

81. Kryzanski JT, Robertson JH, Heilman CB.A minimal access far-lateral approach to foramenmagnum lesions. J Neurol Surgery, Part B Skull Base.2014;75:236-242.

82. Lanzino G, Paolini S, Spetzler RF. Far-lateralapproach to the craniocervical junction. Neurosur-gery. 2005;57(suppl 4):367-371.

83. Liu JK, Couldwell WT. Far-lateral transcondylarapproach: surgical technique and its applicationin neurenteric cysts of the cervicomedullary junc-tion. Report of two cases. Neurosurg Focus. 2005;19:E9.

84. Samii M, Klekamp J, Carvalho G. Surgical resultsfor meningiomas of the craniocervical junction.Neurosurgery. 1996;39:1086-1094.

85. Chaddad-Neto F, Campos-Filho JM, Dória-Netto HL, Faria MH, Ribas GC, Oliveira E. Thepterional craniotomy: tips and tricks. Arq Neuro-psiquiatr. 2012;70:727-732.

86. Puzzilli F, Mastronardi L, Agrillo U, Nardi P.Glossopharyngeal nerve schwannoma: report of acase operated on by the far-lateral transcondylarapproach. Skull Base Surg. 1999;9:57-63.

87. Campero A, Ajler P, Emmerich J. [Posterolateralapproach]. In: Campero A, ed. Abordajes Quirúrgicosal Cerebro y la Base de Cráneo. Buenos Aires,Argentina: Ediciones Journal; 2013:111-121[Spanish].

88. Campero A, Ajler P, Martins C, Rhoton AL.[Posterolateral approach (extreme lateral or far

dx.doi.org/10.1016/j.wneu.2017.07.029

LITERATURE REVIEW

DANIEL S. LEON-ARIZA ET AL. KEY ASPECTS IN FORAMEN MAGNUM MENINGIOMAS

lateral)]. In: García Navarro V, CastilloVelázquez GA, eds. Estrategias y Abordajes en Neu-rocirugía Craneal. Distrito Federal: Amolca; 2015:321-328 [Spanish].

89. Spektor S, Anderson GJ, McMenomey SO,Horgan MA, Kellogg JX, Delashaw JB. Quantita-tive description of the far-lateral transcondylartranstubercular approach to the foramen magnumand clivus. J Neurosurg. 2000;92:824-831.

90. Campero A, Rubino P, Rhoton AL. Anatomy ofthe vertebral artery. In: George B, Bruneau M,Spetzler RF, eds. Pathology and Surgery Around theVertebral Artery. Paris: Springer; 2011:29-40.

WORLD NEUROSURGERY 106: 477-483,

91. Jiang T, Wang Z, Yu C. [Microsurgical anatomy offar-lateral transcondylar approach.]. Zhonghua YiXue Za Zhi. 1998;78:448-451 [Chinese].

92. Peris-Celda M, Campero A, Rubino P, Rhoton AL.Microsurgical anatomy of the internal carotid andvertebral arteries. In: Spetzler RF, Kalani MYS,Nakaji P, eds. Neurovascular Surgery. New York, NY:Thieme; 2015:12-36.

93. Rhoton AL Jr. The far-lateral approach and itstranscondylar, supracondylar, and paracondylarextensions: Neurosurgery. 2000;47:S195-S209.

94. Zhang HZ, Lan Q. [Anatomic study on the designof far-lateral transcondylar transtubercular

OCTOBER 2017 ww

keyhole approach assisted by neuro-navigation.].Zhonghua Yi Xue Za Zhi. 2006;86:736-739 [Chinese].

Conflict of interest statement: The authors of this manuscriptreport no conflicts of interests concerning this manuscriptand have nothing to disclose.

Received 20 May 2017; accepted 6 July 2017

Citation: World Neurosurg. (2017) 106:477-483.http://dx.doi.org/10.1016/j.wneu.2017.07.029

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