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Exclusively Endoscopic Removal of Juvenile Nasopharyngeal Angiofibroma
Trends and Limits
Gilles Roger, MD;
Patrice Tran Ba Huy, MD;
Patrick Froehlich, MD, PhD;
Thierry Van Den Abbeele, MD, PhD;
Jean-Michel Klossek, MD;
Elie Serrano, MD;
Erea-Noel Garabedian, MD;
Philippe Herman, MD, PhD
Arch Otolaryngol Head Neck Surg. 2002;128:928-935.
ABSTRACT
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Objective To determine the feasible conditions for exclusive endoscopic resection
of juvenile nasopharyngeal angiofibroma.
Design Retrospective study of 20 patients, with a mean follow-up of 22 months.
Setting Six academic referral hospitals.
Interventions All patients had a preoperative computed tomographic or magnetic resonance
imaging scan and at least 1 follow-up computed tomographic and/or magnetic
resonance imaging scan 6 or 12 months after surgery. Exclusive endoscopic
removal was performed using conventional functional endoscopic sinus surgery
instrumentation after preoperative embolization.
Results Using Radkowski staging, 4, 7, and 9 patients had stage I, II and IIIA
tumors, respectively. Seven patients were operated on for a recurrence after
open surgery. Extension toward the sphenoid sinus, pterygomaxillary fossa,
or infratemporal fossa could be removed. There was no attempt at endoscopic
removal of deep skull base or temporal fossa invasion. The mean surgery duration
was 135 minutes; mean dimensions of the tumor were 4.5 x 4 x 3
cm; and mean blood loss was 350 mL (median, 300 mL). No recurrences occurred
in this series; there were small asymptomatic remnants in 2 cases.
Conclusions An exclusively endoscopic management of juvenile nasopharyngeal angiofibroma
appears to be effective for small to medium tumors. It should be considered
as a first-choice option for these cases (in view of the minimal bleeding,
shorter duration, and efficacy).
INTRODUCTION
JUVENILE NASOPHARYNGEAL angiofibroma (JNA) is a relatively rare, benign
vascular tumor that arises at the sphenopalatine foramen1
and then extends to the nasal cavities and the nasopharynx to eventually reach,
and even extend beyond, the base of the skull by posterior or lateral invasion.
The latter localization is the principal site of recurrence.2-3
However, the spontaneous involution of a postsurgery remnant is well documented
in the literature.4-5
There are a number of therapeutic options, although the most common
initial treatment is surgical excision preceded by embolization.1-3,6-7
The various surgical approaches that have been used range from transpalatine
to a lateral rhinotomy and to midfacial degloving,8
while for some groups a neurosurgical approach is also required. The use of
endoscopic surgery for the resection of JNA has only recently been reported,9 and there are fewer than 50 cases documented in the
literature.2, 7, 10-20
Most of these patients had relatively limited tumors, Radkowski stage IIA
at most.3 Nevertheless, in an article by Jorissen
et al,18 7 of 13 cases were more advanced than
stage IIA. Apart from this group, significant involvement of the pterygopalatine
or infratemporal fossae has been regarded by most surgeons as a contraindication
to a purely endoscopic approach to sinus surgery. On the other hand, Carrau
et al20 considered that involvement of the
pterygopalatine or infratemporal fossae could be treated by endoscopy alone.
With respect to the use of endoscopic surgery for the excision of maxillofacial
tumors,21-22 it seemed appropriate
to us to reevaluate the limits of endoscopic resection of JNA.
PATIENTS, MATERIALS, AND METHODS
DEMOGRAPHY AND SYMPTOMATOLOGY
The medical notes of patients operated on for JNA (confirmed histologically)
by an exclusively endoscopic approach between 1995 and 2000 were reviewed
in 6 centers. Ten patients were operated on at Lariboisière Hospital
(Paris, France), 5 at Armand-Trousseau Children's Hospital (Paris), 2 at Edouard
Herriot Hospital (Lyon, France), 1 at Robert Debré Children's Hospital
(Paris), 1 at Rangueil Hospital (Toulouse, France), and 1 at Jean Bernard
Hospital (Poitiers, France).
Seven patients had relapses of tumors that had been operated on by a
transfacial approach (mean time, 18 months prior). All were male patients
aged between 11 and 32 years (median age, 15 years). The main presenting symptom
was nasal obstruction, which was present in 17 patients, and in 2 cases the
nasal obstruction was associated with a genuine obstructive sleep apnea syndrome.
Fifteen patients also had epistaxis of variable severity. In addition, 2 patients
had serous otitis media, and 1 had hypoesthesia of the infraorbital nerve.
RADIOLOGICAL INVESTIGATION
All 20 patients had a preoperative computed tomographic and/or magnetic
resonance imaging scan, as well as preoperative arteriography with embolization
(except for 1 patient). In addition, all underwent a follow-up computed tomographic
and/or magnetic resonance imaging scan at least 6 months after surgery for
5 patients and greater than 12 months for the 15 others (range, 12-60 months;
median, 18 months). The techniques used for evaluating the extent of invasion
by the tumors have been reported previously.7
Eighteen different topographic sites were systematically analyzed, and the
results are given in Table 1.
Arteriography with embolization was performed systematically with the exception
of 1 patient who had a relapse limited to the sphenoid sinus. No complications
occurred with the 19 arteriographies. The embolization technique has been
previously reported.23-24 The
branches of the external carotid artery were systematically embolized. In
2 cases, the branches of the contralateral external carotid also needed to
be embolized. Embolization of the tumoral vasculature arising from the internal
carotid artery was performed in 6 cases, preceded by a test occlusion. Embolization
by direct injection was also necessary in 2 cases. The devascularization was
judged to be complete in all but 2 cases (a residual blush of 10% to 20% was
related to inaccessible vessels arising from the internal carotid artery).
The surgical resection was performed between 1 and 6 days after embolization
(median delay of 2 days).
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Extensions of Tumors and Outcome*
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STAGING
All patients were staged using the Radkowski classification,3 derived from the Sessions classification (compare
with Table 1), 25
which, within stage III, allows differentiation from an erosion of the base
of the skull, corresponding to stage IIIA.
SURGICAL TECHNIQUES
A protocol of autologous blood donation was systematically used to collect
1 to 3 U of packed red cells (depending on the hemoglobin level at the time
of diagnosis) during the 3 weeks prior to surgery. Surgery was preceded by
arteriography with embolization. Surgery was performed under general anesthesia.
The nasal fossa was packed with cotton swabs soaked in a vasoconstrictor and
left in place for 15 to 20 minutes. The surgery was performed using a 30°
telescope in all cases, as well as a 0° telescope in 1 case. Standard
surgical endonasal instrumentation was used, often accompanied by an Obwegeser
raspatory. Usually, the first point of intervention was the septum where the
tumor was frequently attached and where the vasculature arising from the posterior
ethmoidal artery (a branch of the ophthalmic artery) had not been embolized.
A bipolar coagulation of the septal mucosa all around the zone of insertion
of the tumor was performed before attempting to release the septal attachment.
When the vomer was deeply involved, the surgery started with sectioning of
the septum just in front of the tumor. The tumor was then progressively detached
by pushing it downward and posteriorly, which exposed the choanal arch, enabling
a sphenoidotomy around the tumor. Excision of tumor in the sphenoid sinus
could then usually be completed by progressive traction and detachment. Thereafter,
the region of the sphenopalatine foramen was exposed. This usually required
resection of the posterior half of the middle turbinate, a middle meatotomy
and possibly a posterior ethmoidectomy, which allowed exposure right down
to the orbital surface. Afterward, the posterior wall of the maxillary sinus
was removed using a sphenoid punch. This procedure was usually not difficult
in view of the curvature and thinning of the bone caused by the tumor. Thus,
it is possible to remove virtually all of the posterior wall.
Endoscopy allowed clear identification between tumor and fat and therefore
dissection of the internal maxillary artery was often possible. The latter
then underwent diathermy, and the tumor was located medially. Even large tumors
could then be pushed toward the cavum. The resection then continued at the
level of the inferior orbital fissure toward the roof of the infratemporal
fossa. After having checked for extension to the foramen ovale and rotundum,
the resection was completed at the pterygoids. Extension to the base of the
pterygoids, in the interpterygoid fossa or to the body of the sphenoid, may
necessitate reaming of the pterygoid plates.
En bloc resection of the tumor was possible in 2 cases, even for 1 tumor
with the greatest diameter of 7 cm. The tumor was pushed down into the pharynx,
and the extraction was then orally performed.
A careful inspection of the operative field should be performed to detect
any possible remnants. Additional coagulation was carried out as necessary.
Packing of the nasal fossa was not performed in 16 cases, while packs were
left in place for 2 days in 4 patients. Almost half of the patients in this
series had extensive involvement of the infratemporal fossa.
RESULTS
Using the Radkowski classification, 9 patients had stage IIIA tumors;
7 patients, stage II (5, stage IIA; 1, stage IIB; and 1, stage IIC); and 4
patients, stage I (2, stage IA; 2, stage IB). In 2 patients, a remnant was
detected at the time of the follow-up imaging at 6 months. In 1 case, the
remnant was situated at the apex of the orbit (which was deliberately left
in place at the time of surgery); this patient had stage IIIA tumor. In the
other, the remnant was situated in the interpterygoid fossa; this patient
had stage IIC tumor. These 2 patients had follow-up imaging at 18 and 20 months
after surgery, which demonstrated that the remnants had not progressed.
The mean follow-up was 22 months, with a median of 15 months. The last
follow-up scan (7 magnetic resonance imaging and 13 computed tomographic scans)
was performed on average 16 months after surgery (median, 18 months). The
average dimension of the resected tumors was 4.5 x 4 x 3 cm. The
use of an exclusively endoscopic approach enabled a relatively quick surgical
resection (mean duration of surgery was 135 minutes), that is, a shorter duration
than would have been expected for the same tumors operated on by an open approach.
Two patients in this series were operated on using computer-assisted navigation.
Blood loss was systematically monitored (measurement of the volume of
blood aspirated). The mean volume of blood loss was 350 mL (range, 50-750
mL; median, 300 mL). In 4 cases, all of which were stage IIIA, there was greater
than 500 mL of blood loss, which represents a significant difference with
respect to stages I and II for which there were no cases of hemorrhage at
this level (P<.02,  2 test). Two
of these 4 cases resulted from significant bleeding from the internal maxillary
artery, while the other 2 resulted from bleeding from the body of the sphenoid.
No patient required heterologous transfusion, and 1 patient who had congenital
factor VII deficiency was operated on with replacement of this coagulation
factor and without significant hemorrhage.
No other perioperative complications were noted. Furthermore, there
was no postoperative hemorrhage. Erosion of the nares due to the traction
of the instruments and possibly to passage of the motor (Figure 1) usually heals without leaving any trace. In 2 cases, there
was anesthesia of the infraorbital nerve related to extensive adhesion of
the tumor to the nerve in the inferior orbital fissure. In the present study,
no additional treatment was necessary.
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Figure 1. Erosion of the nostril at the
end of surgery (with absorbable nasal packing).
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COMMENT
This series of 20 purely endoscopic resections of JNA demonstrates that
a surgical endoscopic approach can be used for tumors of variable size. The
treatment of JNA is associated with several of the following problems: the
perioperative risk of hemorrhage; the difficulty of the resection; the morbidity
associated with involvement of certain sites; and the risk of recurrence.
RECURRENCES
With respect to the risk of recurrence, staging is extremely important.
The Radkowski classification allows prognostication based on the stage. Specifically,
involvement of the base of the skull and in particular the roof of the infratemporal
fossa, the cavernous sinus, and the body of the sphenoid are associated with
an increased rate of relapse.7 Surgical endoscopy
encounters the same difficulties as open surgery, in particular, at these
sites.18-19 Nevertheless, in all
of the published series in which an exclusively endoscopic approach has been
used10-20
and in our patients, no relapses were found in cases with stage I, IIA, and
IIB tumors. The standard relapse rate for tumors staged I through IIB varies
between 0% and 15%,2-3,6
which indicates that endoscopy is at least as effective as open surgery. In
our series, of the 9 patients with Radkowski stage IIIA tumor, there was only
1 case in which a complete eradication was not possible (which was also the
case for 1 patient with stage IIC tumor). Furthermore, these 2 remnants have
not required any additional treatment (with a clinical follow-up of 36 and
30 months, respectively) and the success rate for stages IIC and IIIA would
appear to be better than after open surgery: no true relapses occurred in
the 10 cases in our series compared with the usual rate of 25% for stage IIC
and 40% to 50% for stage III tumors.7, 18
However, the relatively small number of patients with these large tumors that
have been treated by an exclusively endoscopic approach means that it is not
possible to be certain about this apparent reduction in the relapse rate.
In addition, the radiological follow-up of our patients does not allow one
to completely eliminate the possibility of a late relapse, even though this
is a rare occurrence. This would require imaging for all patients for at least
2 years after surgery. The remnants following surgical excision of JNA may
remain stable and may even spontaneously regress,4-5,7
and if they are asymptomatic, clinical and radiological surveillance is all
that is required. If symptoms reoccur (epistaxis or nasal obstruction) or
the lesions progress, appropriate treatment must be instigated, with further
surgery or radiotherapy being the principal therapeutic modalities.
HEMORRHAGIC RISK
The resection of JNA is classically considered to be high-risk surgery
with respect to hemorrhage and may require blood transfusion, which is not
without morbidity. In addition, the perioperative bleeding can significantly
hinder the excision. Consequently, most authors agree that preoperative embolization
should be performed.23-24,26
Embolization was used in all the patients in the present study, apart from
1 patient who had a relapse with a small intrasphenoidal tumor following previous
open surgery. The hemorrhagic risk is of course increased with congenital
defects of hemostasis (eg, hemophilia27 or
factor VII deficiency, as in 1 patient in our series).
The greater availability of procedures for autologous blood donation
has allowed the use of heterologous transfusion to be avoided. However, collecting
autologous units can delay surgery by several weeks and may be difficult to
achieve if there is significant epistaxis. One patient in our series could
only donate blood following the use of erythropoietin.
The risk of perioperative bleeding is greater at certain sites of dissection,
for example, adjacent to the internal maxillary artery, the body of the sphenoid
sinus, the roots of the pterygoids, the interpterygoid fossa as well as in
the region of the cavernous sinus. Involvement of the cavernous sinus itself
or extension toward the internal carotid artery through the foramen lacerum
are associated with a risk of uncontrollable bleeding and probably represent
the limits of endoscopy.7, 18 To
control bleeding in the region of the body of the sphenoid, it may be necessary
to ream the pterygoid process of the sphenoid bone or even the sphenoid itself.
It is essential that the surgical team is adequately trained and has
sufficient experience. One of the frequently mentioned problems with endoscopic
surgery is the use of 1 hand to hold the endoscope. With the aid of videoendoscopy,
it is possible for a trained assistant to position an aspiration tube at the
correct site and thereby greatly facilitate the surgical procedure. The passage
of 3 instruments via the nares does not usually lead to any problems even
if slight damage occurs for a few days (Figure
1).
ANATOMICAL AND ENDOSCOPIC FEATURES
Invasion of certain structures leads to great difficulty with respect
to access regardless of the type of approach used due to the narrowness of
the access to the operative field, namely, the pterygoid recess of a sphenoid
sinus with marked pneumatization or a very deep site in the operative field
such as the clivus or the foramen lacerum. Similarly, the roots of the pterygoid
and the interpterygoid fossa are also difficult to reach both by a transfacial
or a lateral approach.
The use of a 30° telescope allowed this problem to be partly overcome
owing to the additional angulation that could be achieved (Figure 2). The anterior limits of the field of exposure were constituted
by the piriform aperture and the nasal septum. However, the latter can be
easily pushed laterally, and the 30° angulation allows wide exposure of
the retromaxillary region. Significant lateral extension into the infratemporal
fossa, especially toward the area of the cheek, is probably not accessible
by endoscopy alone. Even using more angulated equipment (45° or 70°),
it is unlikely that the instruments would be able to satisfactorily reach
such lateral invasion. In the roof of the infratemporal fossa, the possible
interdigitating penetration by the tumor would make resection very difficult
regardless of the surgical technique used. Although endoscopy undoubtedly
provides better visualization in this part of the operative field, penetration
of the temporal fossa itself requires an approach in which the surgeon has
both hands free. The angle of vision provided by endoscopy is greater than
that with open surgery because it enables very close inspection of the tumor
in all directions. One zone, however, remains very difficult to expose initially,
namely, the posterior part of the tumor. Consequently, we propose that it
is best to start with mobilization of the anterior and lateral parts of the
tumor to access its posterior connections as laterally as possible.
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Figure 2. Patient with stage IIIA tumor.
Endoscopic access to the pterygopalatine fossa with a 30°-angled telescope
(black lines). Maximum amplitude of axis position with a 0° telescope
(white lines).
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The progressive detachment and traction of the tumor allow progression
to the posterior regions, namely, the body of the sphenoid, the roots of the
pterygoids, and the interpterygoid fossa. Even in these sites, the view with
endoscopy is better than that with open surgery. Furthermore, careful reappraisal
is easier with endoscopy in view of the better visual field and the ability
to aspirate selectively.
Combining endoscopy with open surgery is another interesting possibility.7, 20 This would have the advantages of
both techniques (the quality of the field of exposure and the availability
of both hands) but would have the disadvantage of the morbidity associated
with open surgery (possible scarring, duration of the surgery, and risk of
increased hemorrhage). The choice between an exclusively endoscopic approach
and surgery facilitated by endoscopy depends on the localization of the tumor
as well as the experience of the surgeon. Figure 3,
Figure 4,
Figure 5, and Figure 6 illustrate the resection of JNA by a endoscopic approach.
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Figure 3. Patient with stage IIC tumor.
Preoperative computed tomographic scan: axial (A and B) and coronal (C and
D) views. E, Magnetic resonance imaging scan, coronal view. Note the erosion
of the pterygoid plates and sphenoid bone (A and D, arrows).
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Figure 4. Same patient as in Figure 3. Postoperative
magnetic resonance imaging scan at 9 months (A and B) and 18 months (C and
D). Small asymptomatic remnant (A-D, arrows), nonevolving with time.
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Figure 5. Patient with stage IIIA tumor.
Magnetic resonance image scan: axial (A and B) and coronal (C and D) views.
Note adhesion to the infraorbital fissure (C and D, arrows). E, Sagittal view.
F, En bloc resection.
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Figure 6. Same patient as in Figure 5. Postoperative
computed tomographic scan (with iodine injection) at 12 months: axial (A-C)
and coronal (D-F) views. Note the mucosal inflammation without tumor recurrence.
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OTHER ADVANTAGES OF ENDOSCOPY
An exclusively endoscopic surgical approach was associated with a shorter
duration of hospitalization (most of our patients were able to be discharged
within 48 hours after surgery). In addition, this avoids all of the complications
specifically related to different approaches with open surgery (epiphora,
dysesthesia, trismus, pain, and possible effects on facial growth). These
advantages, combined with the reduction in the duration of surgery (related
to the absence of a surgical incision) and especially the expected reduction
in perioperative bleeding, do not of themselves constitute adequate reasons
for considering a purely endoscopic approach as being the first choice for
the resection of JNA. Nevertheless, the published results10-20
have demonstrated an identical efficacy to that of open surgery, at least
for stages I and II and probably for some stage III cases, without intracranial
involvement.
PERSPECTIVES
The development of computer-assisted endoscopic surgery (2 cases in
the present series) should allow improved landmarking of the tumor and consequently
make endoscopy easier to perform.28 The use
of a potassium-titanyl-phosphate laser15 may
possibly help achieve good hemostatic control during the operation. Further
development of the endoscopic approach will also lead to a greater number
of surgeons becoming familiar with this procedure for treating JNA and thereby
allow a progressive extension of the indications for an exclusively endoscopic
management of small, medium, and even large tumors.
CONCLUSIONS
The resection of JNA by a purely endoscopic approach is a reliable technique,
and the results, in terms of excision, are certainly as good as with open
surgery. Even Radkowski stage IIC and IIIA tumors can be removed using this
technique, although the patient must be informed that it may be necessary
to resort to an open procedure. For lower-stage tumors, the efficacy of endoscopy
has been established. Detailed analysis of high-quality imaging as well as
embolization are essential preoperative requirements. Similarly, it is essential
that the entire surgical team is highly experienced with endoscopic techniques.
The presence of 2 experienced surgeons allows the use of 3 hands in the operative
field, thus considerably facilitating operative gestures. Endoscopic surgery
allows quicker resection with less hemorrhage and is very effective. The areas
where excision is difficult are the same and may lead to the risk of residual
tumor remnants, which can be simply observed. The recurrence of symptoms or
progression of lesions may require further treatment.
AUTHOR INFORMATION
Accepted for publication January 18, 2002.
This study was presented at the 16th annual meeting of the American
Society of Pediatric Otolaryngology, Scottsdale, Ariz, May 11, 2001.
Corresponding author and reprints: Gilles Roger, MD, Pediatric Ear,
Nose, and Throat Department, Armand-Trousseau Children's Hospital, 26 Avenue
Arnold Netter, 75571 Paris CEDEX 12, France (e-mail: gilles.roger{at}trs.ap-hop-paris.fr).
From the Ear, Nose, and Throat and Head and Neck Surgery Departments,
Armand-Trousseau Children's Hospital, Assistance Publique-Hôpitaux de
Paris, Paris (Drs Roger and Garabedian); Lariboisière Hospital, Assistance
Publique-Hôpitaux de Paris, Paris (Drs Tran Ba Huy and Herman); Edouard
Herriot Hospital, Hospices Civils de Lyon, Lyon (Dr Froehlich); Robert Debré
Children's Hospital, Assistance Publique-Hôpitaux de Paris, Paris (Dr
Van Den Abbeele); Jean Bernard Hospital, Poitiers, France (Dr Klossek); and
Rangueil Hospital, Toulouse (Dr Serrano), France.
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