management of advanced intracranial intradural juvenile...

O R I G I N A L A R T I C L E

Management of advanced intracranial intradural juvenile nasopharyngealangiofibroma: combined single-stage rhinosurgical and neurosurgical

approachMohsen Naraghi, MD1,2,3, Hooshang Saberi, MD4, Atefeh Sadat Mirmohseni, MD2,3,

Mohammad Sadegh Nikdad, MD2,3 and Mohsen Afarideh, MD, MPH2,3

Background: Although intracranial extension of juvenilenasopharyngeal angiofibroma (JNA) occurs commonly, in-tradural penetration is extremely rare. Management ofsuch tumors is a challenging issue in skull-base surgery, ne-cessitating their removal via combined approaches. In thiswork, we share our experience in management of extensiveintradural JNA.

Methods: In a university hospital–based se�ing of 2 ter-tiary care academic centers, retrospective chart of 6 malepatients (5 between 15 and 19 years old) was reviewed. Pa-tients presented chiefly with nasal obstruction, epistaxis,and proptosis. One of them was an aggressive recurrent tu-mor in a 32-year-old patient. All cases underwent combinedtransnasal, transmaxillary, and craniotomy approaches as-sisted by the use of image-guided endoscopic surgery,with craniotomy preceding the rhinosurgical approach in3 cases.

Results: Adding a transcranial approach to the transnasaland transmaxillary endoscopic approaches provided 2-sided exposure and appreciated access to the huge intradu-ral JNAs. One postoperative cerebrospinal fluid leak and 1postoperative recurrence at the site of infratemporal fossa

were treated successfully. Otherwise, the course was un-eventful in the remaining cases.

Conclusion: Management of intracranial intradural JNArequires a multidisciplinary approach of combined openand endoscopic-assisted rhinosurgery and neurosurgery,because of greater risk for complications during the dis-section. Carotid rupture and brain damage remain 2 catas-trophic complications that should always be kept in mind.A combined rhinosurgical and neurosurgical approach alsohas the advantage of very modest cosmetic complications.C© 2015 ARS-AAOA, LLC.

Key Words:angiofibroma; intracranial approach; intradural approach;transnasal approach; combined approach

How to Cite this Article:NaraghiM, Saberi H,Mirmohseni AS, NikdadMS, AfaridehM. Management of advanced intracranial intradural juve-nile nasopharyngeal angiofibroma: combined single-stagerhinosurgical and neurosurgical approach. Int Forum Al-lergy Rhinol. 2015;5:650–658.

1Department of Otorhinolaryngology–Head and Neck Surgery, TehranUniversity of Medical Sciences, Tehran, Iran; 2Otolaryngology ResearchCenter, Tehran University of Medical Sciences, Tehran, Iran; 3RhinologyResearch Society, Tehran, Iran; 4Department of Neurosurgery, TehranUniversity of Medical Sciences, Tehran, Iran

Correspondence to: Mohsen Naraghi, MD, Dr. Mohsen Naraghi Rhinologyand Facial Plastic Surgery Clinic, No 2417, Vali-Asr Avenue, Tehran,1517843318, Iran; e-mail: [email protected]

Potential conflict of interest: None provided.Presented orally at the 2014 American Academy of Otolaryngology–Headand Neck Surgery (AAO-HNS) Annual Meeting and OTO EXPO onSeptember 21-24, 2014 in Orlando, FL.

Received: 3 November 2014; Revised: 12 January 2015; Accepted:20 January 2015DOI: 10.1002/alr.21507View this article online at wileyonlinelibrary.com.

J uvenile nasopharyngeal angiofibroma (JNA) is a raretumor accounting for less than 0.5% of all head and

neck masses. Classically, JNA presents with the triad ofunilateral nasal obstruction, epistaxis, and nasopharyngealmass.1 Although intracranial extension of JNA often oc-curs, dural penetration is very rare.2 Because of the greaterrisk for complications during surgery, these advanced tu-mors need to be properly addressed in all cases.

Until Andrews stage IIIb (extradural involvement; Ta-ble 1), JNA management does not pose a significant chal-lenge. That is because these not-so-advanced lesions receivetheir primary vascular supply from the external carotid sys-tem (typically the internal maxillary artery). Preoperativeembolization of the extracranial circulation is an extremelyhelpful tool in reducing intraoperative blood loss; today, in

International Forum of Allergy & Rhinology, Vol. 5, No. 7, July 2015 650

Combined management of intradural angiofibroma

TABLE 1. Staging system of juvenile nasopharyngeal angiofibroma according to Andrews et al.6

Type Definition

I Tumor limited to the nasopharynx and nasal cavity. Bone destruction negligible or limited to the sphenopalatine foramen.

II Tumor invading the pterygopalatine fossa or the maxillary, ethmoid, or sphenoid sinus with bone destruction.

IIIa Tumor invading the infratemporal fossa or orbit region without intracranial involvement.

IIIb Tumor invading the infratemporal fossa or orbit with intracranial extradural (parasellar) involvement.

IVa Intracranial intradural tumor without infiltration of the cavernous sinus, pituitary fossa, or optic chiasm.

IVb Intracranial intradural tumor with infiltration of the cavernous sinus, pituitary fossa, or optic chiasm.

these settings, exclusive endoscopic endonasal treatment iswidely considered the treatment of choice.1,3,4

Contrastingly, Andrews stage IVa and IVb JNAs receiveadditional vascular supply from the cavernous branchesof the internal carotid artery (ICA), which most oftencomplicates the routine preoperative embolization of thefeeding arteries to the tumor; this increases the risk ofstroke. The gold standard of treatment in these advanced-staged patients is to perform as complete a resection asis possible to avoid the much-maligned neoadjuvant oradjuvant radiation or chemotherapy. Total tumor resec-tion is alternatively achieved using a combined neurosur-gical and rhinosurgical approach. The rhinosurgical ap-proach consists of endoscopic-assisted midface degloving,endoscopic-assisted transpalatal techniques, and endonasalendoscopic techniques. The neurosurgical approaches con-sist of temporoparietal, subtemporal, frontotemporal, orbifrontal craniotomy. In these settings, combined surgi-

cal approaches may be initiated by either rhinosurgery orneurosurgery.

The present study is the largest reported case-series ofintradural JNA in the literature. Additionally, we wouldlike to share our clinical experience in the safe and effectivemanagement of intradural JNA by emphasizing the impor-tance of a multidisciplinary approach aimed at meticuloustotal tumor resection.

Patients and methodsRetrospective chart review of 6 cases with intracranial in-tradural JNA presenting from September 2008 to March2012 was performed. All cases were males; 5 of themwere between 15 and 19 years old (cases 1 to 5). Pa-tients were followed for a mean of 37 months (range, 18to 60 months); presenting symptoms mainly included nasalobstruction, epistaxis, and proptosis (Table 2). Cavernous

TABLE 2. Characteristics of the cases

Case# Age

(years)

Presentation Stagea Cavernous

sinus

involvement

Preoperative

embolization

(hours)

Side Primary vs

revision

Follow-up

(months)

1 18 Recurrent epistaxis, nasalobstruction, proptosis, leftsuperior orbital fissuresyndrome

IVb + 24 Left Revision 18

2 15 Intermittent epistaxis, nasalobstruction, cheek swelling

IVa – Left Primary 26

3 16 Recurrent epistaxis, nasalobstruction

IVb + 48 Left Primary 38

4 16 Severe epistaxis, nasalobstruction, proptosis

IVb + 24 Right Primary 42

5 19 Recurrent epistaxis, nasalobstruction, proptosis,temple swelling


6 32 Headache, recurrent epistaxis,nasal obstruction,proptosis, left-sidedblindness


aStaging according to Andrews staging system.6

651 International Forum of Allergy & Rhinology, Vol. 5, No. 7, July 2015

Naraghi et al.

FIGURE 1. Coronal and axial CTs demonstrate extensive involvement oforbital apex and nasal cavity with significant encasement of intradural ju-venile nasopharyngeal angiofibroma to optic chiasm and cavernous sinus(case 6). CT = computed tomography.

sinus involvement was observed in all but one of the cases(case 2). One of the cases (a 32-year-old patient, case 6)had been experiencing multiple aggressive recurrences ofthe tumor for 15 years, mainly involving the pterygomaxil-lary, middle cranial, and infratemporal fossae. He had left-sided blindness because of extensive intradural JNA withtumor encasement of both cavernous sinus and optic chi-asm (Fig. 1); this was observed later. Institutional review

board (IRB) exemptions were obtained for conducting thisretrospective review in accordance with the Human Sub-jects Research policy. In addition, written informed con-sent for displaying the photograph of case 5 was obtainedfrom the patient and family. All patients were scheduledfor a complete preoperative diagnostic workup to localizethe tumor area and adjacent compartments, including spi-ral computed tomography (CT) scan, gadolinium-enhancedmagnetic resonance imaging (MRI), and multidetector CT(MDCT) with 3-dimensional (3D) reconstruction (Fig. 2).Image-guided systems (IGS) surgery from the inputs of cra-nial navigation planning software was applied throughoutthe combined procedures (Fig. 3). Selective and superselec-tive embolization of feeding arteries was performed with350-μm to 500-μm polyvinyl alcohol particles 24 to 48hours preoperatively. Preoperative diagnostic CT and MRIimaging studies showed a large mass of intradural JNA inall patients (Fig. 4A and B).

Surgical proceduresFor earlier cases (cases 3, 4, and 6), the rhinosurgical ap-proach was carried out before neurosurgery. Under thisprotocol, we continued with a second-stage rhinosurgeryto remove the final remnants of the tumor and to performrhinosurgical repair of the surgical defect. However, forrecent cases (cases 1, 2, and 5) we decided to use the neuro-surgical method in the first place to marginalize the tumordown away from the middle cranial fossa, followed by therhinosurgical procedure to resect the huge extracranial por-tion and intermediate zone of JNA (Fig. 5). We found withexperience that primary implementation of the neurosur-gical approach results in a simpler and faster operation.By this procedure, intermediate and extracranial parts ofthe tumor are being pushed downward by a neurosurgeon.

FIGURE 2. Multidetector CT with 3D reconstructions shows extensive feeding of the intradural tumor from the cavernous branches of internal carotid artery(carotid arterial tree and intracranial views, case 5). 3D = 3-dimensional; CT = computed tomography.



FIGURE 3. Coronal, sagittal, and axial views obtained by navigation planning software shows the area of tumor invasion and its extensive internal carotidartery relations (case 3). Virtual 3D topography of the involved temporal lobe, infratemporal fossa, and orbit is constructed to plan the optimal combinedrhinosurgical and neurosurgical approach. 3D = 3-dimensional.

Consequently, inferior encasements of tumor are easier torecognize for a rhinologist.

Neurosurgical approachTemporoparietal, subtemporal, frontotemporal, orbifrontal craniotomy proceeded from the nearest siteto the precise location of tumor invasion based on thepreoperative imaging for each case. Primarily, macroscopicextradural dissection was performed to expose the foramenovale (V3) and foramen rotundum (V2). With incision ofthe dura and the subsequent intraoperative drainage ofcerebrospinal fluid, the edge of the temporal lobe wasswiftly retracted using a brain spatula to unveil the tumorperiphery with extensive intradural invasion. Thoroughcare was taken to resect the intracranial portion of thetumor as much as possible with special regard to the vitaladjacent areas (to avoid the possible risk of catastrophiccomplications of massive hemorrhages and/or neurologicdeficits). Subsequently, we found a massive involvementof the floor of middle cranial fossa by the tumor, withpenetration of the dura. After the removal of the bulk ofthe tumor via the skull-base orifice, the remaining partswere gently pushed toward the inferior of the skull baseand were retained for rhinosurgical approaches. The duralcavity was filled with serum to help the brain retreat backto its original position and then repaired. In addition, the

dural opening gap into the skull base and dural cavitywere repaired by grafts from fascia lata. To reinforce thedural closure, the temporalis muscle flap (in cases 1, 2,and 4), pericranial flap (in case 5), or a combination ofboth (in cases 3 and 6; Fig. 6) were laid inferior to thefascia lata. In cases 1, 2, and 4, the temporalis muscle wasreflected across the floor of the middle fossa and fixedby its attached pericranial cuff to the clival periosteum.We used the dural tucking technique to prevent the riskof epidural hematoma expansion in the space definedbetween the layer of previously detached convexity duraand calvarium border.

Rhinosurgical approachA combination of endoscopic-assisted midface degloving,endoscopic-assisted transpalatal, and exclusive endonasalendoscopic approaches were used according to the extentof fossa involvement, previous history of tumor recurrence,and tumor residue. All these methods are associated withbetter cosmetic outcomes and will not leave unsightly scars.Rhinosurgical reinforcement of dural incision using septalflaps that were located just beneath the previous neurosur-gical repair provided further solidity to the skull-base defectclosure.


Naraghi et al.

FIGURE 4. Preoperative imaging studies. (A) coronal, sagittal, and axial gadolinium-enhanced MRIs show significant tumor penetration of temporal lobe (case3). (B) Coronal and axial CTs reveal involvement of orbital cavity and tumor encasement into adjacent cavernous sinus (case 5). CT = computed tomography;MRI = magnetic resonance imaging.

TABLE 3. Intraoperative information

Surgical resection approach

Case# Neurosurgical Rhinosurgical Extent of tumor resection Postoperative complications

1 Subtemporal Endoscopic-assisted midface degloving Total Uneventful

2 Temporoparietal Exclusive endonasal endoscopic Total Uneventful

3 Frontotemporal Endoscopic-assisted midface degloving Total Uneventful

4 Subtemporal Endoscopic-assisted midface degloving Total Cerebrospinal fluid leak

5 Bifrontal Endoscopic-assisted midface degloving Total Uneventful

6 Frontotemporal Endoscopic-assisted transpalatal Total Recurrence

ResultsAdding the transcranial approach to the transnasal andtransmaxillary endoscopic approach provided 2-sided ex-posure and excellent access to huge intracranial JNAs withintradural extension in our cases (Fig. 7). Details of each

procedure have been tabulated in Table 3. A postsurgi-cal cerebrospinal fluid leak (in case 4) was repaired us-ing the fascia lata transcranially. The left superior orbitalfissure syndrome presentation in case 1 required meticu-lous management of subtemporal craniotomy followed byendoscopic-assisted midface degloving surgery to resect the



FIGURE 5. Huge extracranial bulk of the tumor mass removed using therhinosurgical approach (case 5).

FIGURE 6. Pericranial flaps were used before closing the craniotomy andwere placed above dural closure repair complex to reinforce the primaryrepair by grafts from fascia lata (case 6).

tumor. Four out of our 6 cases displayed proptosis as a pre-senting syndrome; however, introducing the combined rhi-nosurgical and neurosurgical approach was associated witha dramatic proptosis improvement in these cases (Fig. 8).The postoperative recurrence rate for our combined proce-dure was confined to case 6 with previous history of mul-tiple local recurrences of the tumor. Prior to our visit oneach separate occasion, he had been operated by the trans-maxillary approach without satisfying outcomes. His newrecurrence site was restricted to the infratemporal fossa,for which he subsequently underwent a rhinosurgical ap-proach of endoscopic-assisted midface degloving surgery.Otherwise, the course was uneventful in the rest of thecases. Total resection of the tumor was later confirmed bypostoperative MRI (Fig. 9).

DiscussionComplete surgical removal of the tumor remains the initialtherapeutic option for advanced intracranial JNA.2 Var-ious open surgical approaches have been encouraged inthe past, including transfacial, transoral, and craniofacialprocedures for these tumors.5–7 Recent advances in endo-scopic endonasal JNA surgery, however, coupled with thesuccess of preoperative arterial embolization, have seen thistechnique being regarded as the treatment of choice in the

FIGURE 7. Intraoperative images of neurosurgical approach. Combinedneurosurgical and rhinosurgical 2-sided exposure in case 3 (frontotemporalcraniotomy) and case 5 (bifrontal craniotomy) determines the extent of tu-mor and its feeding vessels to achieve minimal bleeding. (A) temporal lobe,(B) retreated dura over the lesser wing of sphenoid bone, (C) middle cranialfossa, (D) resected floor of the middle cranial fossa.

FIGURE 8. Proptosis in intradural juvenile nasopharyngeal angiofibroma.(Top) Preoperative left eye proptosis is clearly visible with front, upward,and downward positioning of the head. (Bottom) Three years postoperation;patient shows almost no signs of proptosis (case 5).


Naraghi et al.

FIGURE 9. Comparison between preoperative and postoperative gadolinium-enhanced MRIs. In preoperative axial cuts, compression of tumor posterior tothe orbital cavity causing proptosis of the left eye is visible and 36 months later postoperative axial cuts confirm that proptosis is corrected after the combinedneurosurgical and rhinosurgical approach (case 5).

management of advanced JNA.1,3 Previously, we showedendoscopic resection of JNA by a combination of transnasaland transoral routes to be reliable in reduction of intraop-erative bleeding, morbidity, and hospitalization period inpre-advanced JNA.8 Nevertheless, as outlined in the firstsection of this article, there are considerable anatomic andpractical barriers that preclude the use of endoscopic ap-proach alone for meticulous management of highlyadvanced JNA with intradural transcendence.9,10 In fact,most surgeons regard significant involvement of the in-fratemporal fossae (as is the case with intradural JNA)as a contraindication to a purely endoscopic approach.1

These represented some major problems to prompt us indeploying an endoscopic-assisted approach (in conjunctionwith transnasal, transmaxillary, and craniotomy surgicalroutes) instead of exclusive endoscopic resection for themanagement of end-stage JNA.

Considering that JNA bone destruction typically re-sults from a compressive growth pattern instead of aninfiltrative one,11 intracranial JNA usually eludes duralinvolvement.12–14 In fact, intradural penetration of ad-vanced JNA is extremely rare, and is reported mainlyin Brazil and the United States.11,15–19 In this work, wedelineate a method with the combination of transnasal,transmaxillary, and craniotomy approaches to manage 6cases of intracranial intradural JNA. We had one atypi-cal 32-year-old patient with prior aggressive recurrencesof the tumor that may call the diagnosis into question.He had a long history of recurrences of extensive in-tradural JNA for more than 15 years and the postsur-gical pathologic examination confirmed the diagnosis ofJNA. Recent reports of JNA even after the third decade oflife3 suggests that the upsurge of sex hormones may not

be the main reason behind JNA occurrence in adolescentmales.20

Reported approaches for the management of intracra-nial intradural JNA in these studies are summarized inTable 4. In the most recent case-series of intradural JNA,15

the authors proposed a combination of a subtemporaland transfacial approach for the near-total resection ofadvanced intradural tumor. They concluded that thisapproach is safe and efficacious in circumvention of long-term morbidities associated with radiotherapy in youngmales who are expected to have a regression in tumor sizein adulthood due to arrested tumor growth and involutionwithin the vascular bed.21 Contrary to their suggestions,some observed later recurrence of JNA might be because ofan incomplete resection during the aggressive growth phasein adolescence.22,23 Although postoperative recurrencesof tumor are primarily seen with high-stage tumors,2 thelower rate of recurrence also accounts for the primarymeasure of success in the treatment. Unfortunately, post-operative recurrence rate of the approach by Kumar et al.15

leaves a lot to be desired. From their 4 Andrews stage IVbpatients, 3 were submitted later on with local/widespreadrecurrences of the tumor; 1 with multiple local recurrences.To control these recurrences, they required frequentpostoperative endoscopic and transnasal debridements ortranscervical and endoscopic resections of the tumor.15 Us-ing the combined approach, the entire tumor was removedsuccessfully in all our patients and, unlike previous invasiveapproaches that were used to manage these aggressivetumors (eg, cranio-orbitozygomatic approach15,18), hasthe advantage of minimal, if any, cosmetic dissatisfaction.The only recurrence of JNA among our cases was seenin the infratemporal fossa, which was later managed



TABLE 4. Previously reported approaches for the management of intracranial intradural juvenile nasopharyngealangiofibroma

Study# Year Author(s) Cases

(n)

Approach of management Age (years)

(mean)

Postoperative

follow-up

(months)

(mean)

Postoperative

recurrencea

1 1979 Jafeket al.16

1 Frontotemporal craniotomy,nasal septum transection andtransmaxillary resection oftumor followed by removal ofthe sphenoid sinus extension

15.5 36 0

2 1984 Cummingset al.19

4 External beam megavoltageradiation therapy

20 >60 n/a

3 1992 Lyons andDonald17

1 Total resection by combinedtranspalatal, Caldwell Lucprocedure and a lateralinfratemporal/middle fossaapproach

13 0 1

4 1995 Butuganet al.11

3 Degloving surgery, incompleteorbito-fronto-temporo-zygomatic resection,second-time completedegloving extracranialresection followed by radiationand hormone therapy

15 42 2

5 2011 Ramoset al.18

1 Craniotomy withtranszygomatic approachthrough the left frontotemporalfossa

16 24 1

6 2015 Kumaret al.15

4 Near-total resection withcombinedsubtemporal-transfacialsurgical approach

15.75 38 3

Currentstudy

2015 Naraghiet al.

6 Total resection by combinedrhinosurgical andneurosurgical approach

19.3 37 1

aValues are number of cases.n/a = not applicable (the authors did not measure these values).

using the endoscopic-assisted midface degloving approachwithout further recurrence in the 5-year postoperativefollow-up period. It should be kept in mind that ourpatients comprised a heterogeneous group with respect totumor location and involved structures, and therefore theresults may be only cautiously generalized to Andrews IVaand IVb JNA.

ConclusionIntracranial intradural extension of JNA requires anexquisitely meticulous approach in terms of completetumor-resecting surgery, because of the greater risk forcomplications during intradural dissection compared toearlier stages of the disease. Carotid rupture and brain dam-age are 2 catastrophic complications that should always bekept in mind in these circumstances. In cases with extensive

intradural involvement of the middle cranial fossa, cran-iotomy with a combination of transnasal and transmax-illary approaches could help decrease the complications.Total tumor resection is possible with minimum neurolog-ical deficits, but dura reconstruction is necessary. A com-bined neurosurgical and rhinosurgical approach is benefi-cial to achieve a lower postsurgical recurrence rate as wellas acceptable cosmetic outcome for the cases of intraduralJNAs.

AcknowledgmentsWe thank the operating room (OR) staff of Amir-Alamand Imam-Khomeini Hospitals for their assistance of thesurgical approaches. We also pay tribute to our patients aswell as their families for their continuous support and theirunconditional dedication to the current work.


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