The LaryngoscopeLippincott Williams & Wilkins, Inc., Philadelphia© 2003 The American Laryngological,Rhinological and Otological Society, Inc.

Endoscopic Surgery for JuvenileAngiofibroma: When and How

Piero Nicolai, MD; Marco Berlucchi, MD; Davide Tomenzoli, MD; Johnny Cappiello, MD;Matteo Trimarchi, MD; Roberto Maroldi, MD; Giuseppe Battaglia, MD; Antonino R. Antonelli, MD

Objectives/Hypothesis: In recent years, the indi-cations for endoscopic surgery of the sinonasaltract, originally introduced for the treatment ofinflammatory diseases, have been expanded to in-clude selected cases of benign and malignant neo-plastic lesions. The aim of the present study wasto establish the efficacy of endoscopic surgery inthe management of small and intermediate-sizedjuvenile angiofibromas. Study Design: Retrospec-tive study. Methods: We reviewed the clinicalrecords and the preoperative and postoperativeimaging studies of 15 patients with juvenile angio-fibroma who were treated with an endoscopic ap-proach after embolization in the period from Jan-uary 1994 to April 2000. All patients wereprospectively followed by endoscopic and mag-netic resonance imaging evaluations performedat regular intervals (every 4 months during thefirst year and, subsequently, every 6 months). Re-sults: According to a staging system reported in1989, there were two patients with a type I, ninewith a type II, three with a type IIIA, and one witha type IIIB juvenile angiofibroma. Angiographydemonstrated that the vascular supply wasstrictly unilateral in 11 patients and bilateral in 4.Intraoperative blood loss ranged from 80 to 600mL (mean blood loss, 372 mL). During follow-up(range, 24–93 mo; mean follow-up, 50 mo [SD �19.9 mo]), only one patient presented a residuallesion on magnetic resonance imaging, which was16 mm in diameter and was detected 24 monthsafter surgery. Conclusions: The endoscopic ap-proach is a safe and effective technique thatallows removal of small and intermediate-sizedjuvenile angiofibromas (without extensive in-volvement of the infratemporal fossa and cavern-ous sinus) with a low morbidity. Advanced lesionsare more appropriately treated by external ap-

proaches. Key Words: Juvenile nasopharyngealangiofibroma, endoscopic surgery, diode laser, re-currence, imaging.

Laryngoscope, 113:775–782, 2003

INTRODUCTIONJuvenile angiofibroma (JA) is a highly vascularized

benign lesion that typically occurs in adolescent boys com-plaining of nasal obstruction and epistaxis.1 Recent stud-ies seem to suggest that the lesion displays an immuno-histological and electron microscopic profile moreconsistent with a vascular malformation than with a tu-mor2,3; furthermore, the presence of genetic imbalanceshave been demonstrated by comparative genomichybridization.4

Management of JA has always been regarded as aformidable challenge to the otolaryngologist. However,there is general agreement that surgery should be consid-ered the elective therapy. Moreover, the use of radiother-apy and chemotherapy should be better confined to thetreatment of very extensive lesions or recurrent tumorsinvolving critical anatomical areas, where surgical extir-pation can carry a significant morbidity. Several surgicaloptions, including transhyoid, transpalatal, transfacial(through a lateral rhinotomy or a midfacial degloving),and infratemporal approaches, have been advocated. Re-cent reports have focused on more conservative transnasaltreatments, using either purely endoscopic5–20 or com-bined microscopic–endoscopic techniques.21,22

From January 1992 to September 2002, in all, 101benign and malignant lesions of the sinonasal tract ornasopharynx was managed by an endoscopic approach atthe Department of Otolaryngology of the University ofBrescia (Brescia, Italy). The main purpose of the presentreport was to review the results obtained in the group ofpatients who presented with JA, so as to have a betterunderstanding of the possibilities and limitations of theendoscopic approach in this specific disease.

PATIENTS AND METHODSBetween January 1968 and September 2002, 53 patients

with JA were treated at the Department of Otolaryngology, Uni-versity of Brescia; 31 of them had the lesion resected through anexternal approach and 22 underwent a transnasal removal.

Presented at the 105th Annual Meeting of the Triological Society,Boca Raton, FL, May 14, 2002.

From the Departments of Otorhinolaryngology (P.N., M.B., D.T., J.C.,M.T., A.R.A.) and Radiology (G.B., R.M.), University of Brescia, Brescia, Italy.

Editor’s Note: This Manuscript was accepted for publication Decem-ber 9, 2002.

Send Correspondence to Piero Nicolai, MD, Department of Otorhi-nolaryngology, University of Brescia. Piazza Spedali Civili 1, 25123 Bres-cia, Italy. E-mail: nicolai@master.cci.unibs.it or pieronicolai@virgilio.it

Laryngoscope 113: May 2003 Nicolai et al.: Surgery for Juvenile Angiofibroma

775

TAB

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ient

Cha

ract

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tics.

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ient

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volv

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ize)

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oval

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-up

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ory

men

inge

al,

and

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gp

hary

ngea

lart

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200

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3d

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214

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dib

ular

and

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80m

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s8

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84m

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330

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Laryngoscope 113: May 2003 Nicolai et al.: Surgery for Juvenile Angiofibroma

776

The present report focuses on a cohort of 15 patients (TableI) who were treated by means of an endoscopic approach in theperiod between January 1994 and April 2000 and were followedfor at least 24 months. All were male patients, with ages rangingfrom 13 to 30 years (mean age, 15.8 y). Three of them (cases 3, 9,and 13) had already been treated for their lesions 25, 44, and 42months, respectively, before admission to our department. Pre-operative workup included magnetic resonance imaging (MRI)and angiography in all patients. Magnetic resonance imagingexaminations were performed on axial and coronal planes withcontrast enhancement. The angiographic study, which was per-formed 72 to 24 hours before surgery, encompassed bilateralexamination of the carotid arteries; at the same time, all lesionswere embolized using polyvinyl alcohol particles ranging in sizefrom 150 to 500 �m. Magnetic resonance imaging scans wereretrospectively reviewed by the same radiologist (R.M.) to assessthe volume, extent, and stage of the lesions according to thesystem reported by Andrews et al.1 (Table II). The number offeeding vessels, their compartment of origin (external vs. internalcarotid artery), and the presence of a contralateral supply werealso recorded; correlations among these variables have been eval-uated by means of t test.

The entity of the embolization was expressed by estimatingthe devascularization of the lesion. A value of 100% correspondedto the absence of any blush following embolization. Subtotaldevascularizations were graded by comparing the size of residualblush (in both the anteroposterior and lateral-to-lateral projec-tions) with pretreatment lesion staining.

Every patient had two units of autologous blood bankedduring the 2 weeks before the operation to minimize the intraop-erative or postoperative need for homologous transfusion. Aninformed consent for intraoperative change to an external ap-proach whenever the lesion could not be resected endoscopicallywas obtained from all patients.

All operations were performed by the same surgeon (P.N.).Hypotensive general anesthesia was used in all cases, with thepatient lying supine in a slightly reversed Trendelenburg posi-tion. Both nasal cavities were packed with cottonoid pledgetssoaked in oxymetazoline that were left in place for 10 minutes;further vasoconstriction was achieved by submucosal injection of1% lidocaine with 1:200,000 epinephrine at the level of the root ofthe middle turbinate and of the uncinate process. Even thoughthe surgical technique slightly varied in individual patients ac-cording to the size and extension of the lesion, the dissectionincluded a series of basic surgical steps. Uncinectomy with pres-ervation of the frontal recess area, partial or total resection of themiddle turbinate, and anterior and posterior ethmoidectomy werefirst performed to obtain enough space to adequately work aroundthe lesion with the endoscopic instrumentation. A wide middle

antrostomy was subsequently created to expose the posterior wallof the maxillary sinus, which was removed by angled cuttinginstruments as far laterally as was dictated by the extension ofthe lesion into the pterygomaxillary and infratemporal fossa.After gentle dissection of the mass from the surrounding softtissues, the sphenopalatine or, when required, the internal max-illary artery was isolated and clipped. In patients with sphenoidsinus involvement, the anterior wall of the sinus was entirelyremoved to have a better visualization of the posterior projectionof the lesion. The dissection then proceeded along the subperios-teal plane to free the mass from the nasopharyngeal walls. Whenrequired because of firm adherence, the posterior part of theseptum was resected with the mass. Lesions that were particu-larly large and with deep extension into some critical areas (ie,infratemporal fossa, cavernous sinus) had the nasal-nasopharyngeal portion divided, first, and then removed by usinga diode laser set on pulsed mode (25 W, 0.1 s), vehicled through acontact disposable light guide that was 600 �m in diameter,which was mounted on a malleable handpiece (Dornier Medizin-Laser Gmbh, Germering, Germany). This was performed to speedup the procedure and to gain a bloodless exposure of the deepestextensions of the lesion. Depending on size, the mass was removedtransnasally or transorally. As a final surgical step, patients whoselesion invaded the pterygoid process had the adjacent skull basebone extensively drilled; special attention was paid to disclose anytumor extension along the vidian nerve. After careful review of thesurgical field, both nasal cavities were packed with Lyofoam (SetonHealth Care Group plc, Oldham, UK).

Only one patient (case 4) with a small lesion (2 � 1 � 2 cm)with no lateral extension received a more conservative treatment,which did not include dissection of the pterygomaxillary fossa andspared the middle turbinate. The estimated intraoperative bloodloss was correlated with the presence of afferent vessels from theinternal carotid artery, the number of feeding vessels, and thevolume of the lesion using a t test. All of the patients werefollowed prospectively with periodic evaluations including endos-copy, with storage of the images and MRI scans, scheduled atregular intervals (every 4 months during the first postoperativeyear, every 6 months up to the fifth year, and subsequently oncea year).

RESULTSThe volume of the lesions ranged from 4 to 209 cm3

(mean volume, 61.3 cm3; SD � 60.7 cm3). Nasopharynx,nasal cavity, sphenoid sinus, pterygomaxillary fossa,pterygoid process, and infratemporal fossa were involved,respectively, in 14 (93.3%), 13 (86.6%), 12 (80.0%), 9(60.0%), 8 (60.0%), and 3 (21.4%) patients. One patient(case 8) had a lesion that extended into the inferior andsuperior orbital fissures and into the parasellar region(extradural) (Fig. 1). Two patients had type I lesions, 9had type II lesions, 3 had type IIIA lesions (Fig. 2), and 1patient had a type IIIB lesion.

Angiography demonstrated that all lesions had a vas-cular supply from the distal branches of the internal max-illary artery (sphenopalatine and/or vidian arteries);seven (46.6%) of them received additional vascularizationfrom internal carotid branches (mandibular artery andinferolateral trunk). The lesions were fed by 1 to 5 vessels(mean number of vessels, 2.7) that were distributed asfollows: distal branches of the internal maxillary artery inall cases, ascending pharyngeal artery in nine cases(60.0%), mandibular artery in five cases (33.3%), accessorymeningeal artery in four cases (26.6%), inferolateral trunk

TABLE II.Staging System of Nasopharyngeal Angiofibroma According to

Andrews et al.1

Type I Tumor limited to the nasopharyngeal cavity; bonedestruction negligible or limited to thesphenopalatine foramen

Type II Tumor invading the pterygopalatine fossa or themaxillary, ethmoid, or sphenoid sinus with bonedestruction

Type III Tumor invading the infratemporal fossa or orbitalregion without intracranial involvement (a) or withintracranial extradural (parasellar) involvement (b)

Type IV Intracranial intradural tumor without (a) or with (b)infiltration of the cavernous sinus, pituitary fossa,or optic chiasm

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777

in three cases (20.0%), and facial artery in one case (6.6%).In 11 patients (73.4%) the vascular supply to the lesionwas strictly unilateral. Four patients (26.6%) had con-tralateral feeding vessels arising in all cases from thedistal branches of the internal maxillary artery and in one

case (6.6%) from the mandibular artery. Embolization ob-tained a devascularization rate of 60% to 100% (mean,88.9%).

Feeding by internal carotid branch(es) correlatedwith the number of feeders arising from the external

Fig. 1. Patient 8. (A) The coronal plane demonstrates the lesionspreading between V2 (black arrow) and the internal carotid artery(white arrow) to contact the cavernous sinus. The submucosal ex-tension into the nasopharynx is also detectable. (B) Postoperativemagnetic resonance imaging scan (T1-weighted after paragmag-netic contrast agent injection) after 42 months. No enhancing lesionis detectable. The maxillary nerve and the internal carotid artery arenormal. (C) Endoscopic view (0° rigid fiberscope) of the left-sidenasal cavity 4 years after endoscopic treatment.

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778

carotid artery (3.42 [SD � 0.78] vs. 2.12 [SD � 1.12][P � .01]). No correlation was found among the otherparameters tested.

Intraoperative blood loss varied from 80 to 600 mL(mean blood loss, 372 mL). No patient required autologousblood transfusion. No intraoperative or perioperative com-plications were observed. Nasal packings were removed 2to 4 days after surgery (mean period, 2.3 d). The meanhospitalization time was 6.4 days.

Definitive pathology reports confirmed the diagnosisof JA. At the control evaluations during the follow-upperiod (range, 24–96 mo; mean period, 51.2 mo; SD � 20.3mo), only the patient who had been treated for a type Itumor with a conservative dissection (case 4) presentedwith a 16-mm lesion involving the floor of the sphenoidsinus that was suspect for residual tumor 24 months aftersurgery at the MRI examination (Fig. 3). Subsequent MRI

evaluations scheduled every 4 months showed an increasein size to 21 mm over a period of 20 months.

One patient each developed a sphenoid mucocele anda synechia between the septum and the inferior turbinate.Both patients were otherwise asymptomatic and were suc-cessfully treated under local anesthesia by endoscopicsurgery.

DISCUSSIONDespite its benign nature, JA displays an aggressive

pattern of growth. From the point of origin, which islocated, according to some authors, in the sphenopalatineforamen23,24 or, according to others, in the posterior partof the pterygopalatine fossa at the anterior aperture of thevidian (or pterygoid) canal,25 the lesion first expands intothe nasopharynx and the nasal cavities. Subsequently, itinvades the sphenoid sinus, the pterygomaxillary fossa,the maxillary sinus, the infratemporal fossa, and the orbitby bone erosion. Intracranial extension, a late event re-ported in up to 36% of the patients,26 usually occurs ex-tradurally at the level of the middle cranial fossa; anteriorfossa invasion is an exceedingly rare finding.27 The in-volvement of most of the aforementioned areas is gener-ally asymptomatic and cannot be detected by endoscopicexamination; however, it must be carefully identified be-fore selecting the surgical approach.

Magnetic resonance imaging is the ideal method for amultiplanar evaluation of the lesion and for obtaining de-tailed information on the relationship between the mass andimportant adjacent structures (ie, orbit, dura, internal ca-rotid artery, cavernous sinus). Although MRI is not com-monly indicated for the assessment of invasion of bony struc-tures, in the present series it proved to be accurate indetecting erosion of the pterygoid process (60%) as well asextension into the pterygomaxillary (60%) and infratempo-ral fossa (21.4%). All these findings were confirmed atsurgery.

Fig. 2. Patient 11. (A) Preoperative magnetic resonance imaging(MRI) scan (T1-weighted after paragmagnetic contrast agent injec-tion). The right-side nasal fossa and sphenoid sinus are occupied bythe juvenile angiofibroma. Remodeling of maxillary sinus medial walland contralateral displacement of the nasal septum are demon-strated. Infratemporal extension of the lesion is present, along withincrease diameter of the internal maxillary artery (white arrows). (B)Three years after surgery, the postoperative MRI scan (T1-weightedafter paragmagnetic contrast agent injection) shows nonenhancingtissue (consistent with scar) replacing the infratemporal part of thejuvenile angiofibroma (arrows). The adjacent pterygoid processdoes not present any relevant abnormality.

Fig. 3. (Case 4). Recurrent juvenile angiofibroma (JA) at 24 monthsafter endonasal surgery. Follow-up magnetic resonance imagingscan (T1-weighted after paragmagnetic contrast agent injection)demonstrates a submucosal enhancing lesion close to the inferiorborder of the basisphenoid (arrows). The different signal betweenthe residual JA and the adjacent adenoid tissue is evident.

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The pattern of vascularization of the lesion, anotherimportant feature to be considered when planning treat-ment, is assessed by angiography, which is extremelyhelpful, particularly in advanced lesions, in ruling out adirect involvement of the internal carotid artery. Never-theless, the presence of additional (nonembolized) feedersfrom the internal carotid artery did not correlate with theamount of blood loss and did not prevent the endoscopicapproach. The epidemiological profile, endoscopic appear-ance, and imaging findings of the lesion usually allow fora correct diagnosis without performing a biopsy, whichcan expose the patient to the risk of severe hemorrhage.28

Once data on the extent and vascularization of thelesion are available, the surgeon can select the techniquethat allows the best exposure with minimal morbidity. Inthis regard, we think that in the treatment of JA involvingthe nasopharynx, the nasal cavities, the sphenoid sinus, thepterygomaxillary fossa, the ethmoid, and the maxillary si-nus, endoscopic surgery can favorably compete with othertechniques, such as the midfacial degloving and lateral rhi-notomy approach. In fact, since 1994, we have treatedthrough a purely endoscopic approach all the patients withtype I or II lesions (according to the classification of Andrewset al.1) who came to our observation. The first importantadvantage of the endoscopic approach is the possibility ofobtaining a magnified, multi-angled view of the mass and ofits adjacent anatomical structures, which must necessarilybe coupled with a good control of intraoperative bleeding. Inthis respect, preoperative embolization, which in our experi-ence proved to be a safe procedure with only minimal mor-bidity, is a key element. Other tools we found effective inminimizing bleeding included the use of a delicate, atrau-matic dissection technique with the help of bipolar coagula-tion and a diode laser, which is especially helpful for theresection of a part of the lesion or for the incision of the nasalor nasopharyngeal mucosa in a nearly bloodless fashion. Thesecond major advantage of the endoscopic procedure is thatit does not require any skin or mucosal incision, elevation ofsoft tissues from the anterior wall of the maxilla, removal ofbone, facial osteotomies, or plating of the maxillary frame-work. It is well known from experiments in animals,29 aswell as from observations in humans,30,31 that when per-formed in adolescent patients, most of these surgical maneu-vers can interfere with the pattern of midface growth.

Compared with the microscope, one of the major lim-itations of the use of endoscopes for endonasal surgery isthe availability of only one hand for surgical maneuvers.In our experience, in situations such as those which in-volve dissection of the lesion from the basisphenoid orwhen cutting the mucosa with a laser, we found it partic-ularly helpful to have an experienced assistant available.This person may keep the tissue to be dissected undertraction and can also help with suction, using the so-calledtwo-handed technique.32 Resorting to a microscope or toan endoscope holder are additional alternatives that maybe used to overcome such limitations of the standard en-doscopic technique in advanced indications.

Although we have successfully treated three patientswhose lesions extended into the infratemporal fossa andan additional patient with a digitation of the mass thathad grown along the lateral aspect of the cavernous sinus,

we maintain that only patients with extremely limitedtype IIIa or IIIb lesions should be selected for an endona-sal approach. In fact, neither of the two patients withlarge type IIIb lesions that we observed from 1992 to 2000were considered amenable to treatment with endoscopicsurgery (Fig. 4); both cases were managed through a mid-facial degloving approach using microsurgical techniques.Our series of cases did not include any lesions with intra-dural extent (type IV), which are, indeed, extremelyrare.33 However, it is our opinion that they can be moreappropriately treated by an infratemporal approach, anextended transfacial approach, or a craniofacial resection.

Including the present series, approximately 100 casesof JA treated by endonasal approach have been reported inthe literature5–22; thus, this procedure cannot be consideredas a “standard” technique. Therefore, patients who undergosuch a treatment require careful follow-up evaluation for theearly detection of possible residual lesions. Only a few re-ports11,25,34–36 have focused on the issue of residual lesionsand have tried to address important questions such as thekey points in obtaining a radical extirpation, the best radio-logic technique available for early detection of residual le-sions, the natural evolution of these lesions, when retreat-ment is required, and what the best options are.

The first important prerequisite for surgical radicalsurgery is the possibility of working under magnificationso that the interfaces between the lesion and the adjacentsoft tissues or bony structures can be more precisely iden-tified. The latter point is of utmost importance, and weconcur with other authors33,36 that whenever the lesionextends into the cancellous bone of the basisphenoid, acareful, meticulous drilling of the involved bone must beperformed to minimize the chances of leaving behindpathological tissue.

Digital angiography has been considered to be anaccurate technique for the early detection of residual le-

Fig. 4. A type IIIb juvenile angiofibroma not treated by endonasalsurgery. The sphenoid sinus is entirely occupied by the tumor thatextends into the bony structure (left sphenoid greater wing) of theskull base. Blurring of the interface between the lesion and overlyingbrain tissue suggests, at least, a close relationship with the duramater. The left-side superior orbital fissure (white arrow) and theentire infratemporal fossa (black arrows) are occupied. Contralateralextension into the right-side pterygoid process is also present.

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sions.37 However, cross-sectional imaging provides a sim-ilar accuracy without the need for invasive procedures. Anadditional advantage of MRI over computed tomography(CT) is the absence of radiation exposure, a relevant as-pect in a population of young patients. In our experience,periodic MRI examinations have proven to be accurate inidentifying one residual tumor and one sphenoid mucocelein patients who were otherwise asymptomatic and pre-sented a normal endoscopic appearance.

The natural history of JA is not fully understood; it iscommonly thought that the lesion displays a constantgrowth during the puberal period, whereas with increasingage it tends to spontaneously involute. However, there is notenough evidence in the literature to substantiate this theoryfor either the primary or the residual lesions. Therefore, anypatient who is found to have a residual lesion at radiologicalcontrol must be carefully evaluated in relation to a series offactors: age, site and size of the lesion, availability for follow-up, and patient compliance. Scheduled endoscopic and radio-logical examinations have the advantage of preventing latediagnosis of residual lesions, which are identified by MRI orCT at an early stage. Small remnants can reasonably befollowed by imaging techniques at regular intervals (4–6mo) to monitor the pattern of growth. Whenever the massclearly and regularly increases in size, surgical resection isgenerally the preferred form of treatment; in small (1–3 cm)residual lesions, radiosurgery can be considered an alterna-tive option today.

The incidence of residual disease in the literaturevaries from 13%16 to 50%.38 This large variability ismainly related to the distribution of patients in the differ-ent published series in terms of stage and the criteria(clinical or radiological) used to establish the presence of aresidual lesion. According to Herman et al.,11 the rates ofremnant identification by CT were 7% and 39.5% in thepatients without and with skull base involvement, respec-tively. In our series, which included patients who werefollowed prospectively by MRI for at least 24 months aftersurgery, the observation of only one residual lesion (6.6%)favorably compares with the results reported in the liter-ature for small and intermediate-size juvenile angiofibro-mas treated by traditional external approaches.

CONCLUSIONThe results of the present study involving a single

institution reveal that, when carefully and properlyplanned according to data provided by imaging, an endo-scopic approach is a promising alternative to externaltechniques in the management of small to intermediate-sized juvenile angiofibromas. During preoperative coun-seling, the need to switch intraoperatively to an externalprocedure should always be discussed with the patient;consequently, informed consent should be obtained. Aschedule for endoscopic and MRI follow-up evaluationsmust be planned, to identify possible residual lesionsearly. Refinement in surgical instrumentation, the use ofCT- or MRI-guided surgical navigation, and the availabil-ity of intraoperative imaging techniques will certainlyallow gradual expansion of the indications for endoscopicsurgery in the management of JA.

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