Auris Nasus Larynx 41 (2014) 359–363
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Auris Nasus Larynx journal homepage: www.elsevier.com/locate/anl
Surgery for juvenile nasopharyngeal angiofibroma with lateral extension to the infratemporal fossa Masato Yamada a, Atsunobu Tsunoda a,*, Takao Tokumaru a, Masaru Aoyagi b, Yoshihisa Kawano b, Tomoyuki Yano c, Seiji Kishimoto d a
Department of Otolaryngology, Tokyo Medical and Dental University, Japan Department of Neurosurgery, Tokyo Medical and Dental University, Japan Department of Plastic and Reconstructive Surgery, Tokyo Medical and Dental University, Japan d Department of Head & Neck Surgery, Tokyo Medical and Dental University, Japan b c
A R T I C L E I N F O
A B S T R A C T
Article history: Received 20 May 2013 Accepted 27 February 2014 Available online 28 March 2014
Objective: The study aimed to assess the usefulness of skull base surgery for large juvenile nasopharyngeal angiofibroma (JNA) with lateral extension to the infratemporal fossa. Materials and methods: Eleven cases were enrolled for this study, and the mean age was 17.7 years old (range: 8–32). Six out of 11 cases underwent surgery as an initial treatment, and the other five underwent secondary surgery after initial surgery or radiotherapy in other institutions. The range of extension of tumor, feeding arteries, surgical approach, and treatment outcome were estimated. Results: All tumors originated from the sphenopalatine foramen. Based on the imaging study, there was extension to the cavernous sinus observed in eight cases, as well as to the middle cranial fossa (8), orbit (4), and anterior cranial fossa (1). These tumors were diagnosed as Andrews’ Stage IVa (3) and IVb (8). However, infiltration into the cavernous sinus was observed in one case only during surgery. Ten tumors were separated carefully from the cavernous sinus or dura and were accurately diagnosed as Stage IIIb. In all cases, the main arterial feeders of the JNAs were branches of the external carotid artery, which were embolized prior to surgery. However, 10 cases were also fed by branches of the internal carotid artery (branches of the ophthalmic artery), in which these arteries could not be embolized. Coronal skin incision (1) and a facial dismasking flap (9) were used, and in one case, wide lateral skin incision with temporary incision of the facial nerve was applied. The orbito-zygomatic approach and its modification was applied to all the cases. Fronto-lateral craniotomy was applied in four cases and lateral craniotomy in seven cases. Total resection was achieved in 10 cases and subtotal resection in one case. No mortality was noted in this series. Temporal trismus was observed in all cases which subsided gradually. Cheek numbness and facial palsy were observed in three and two cases, respectively. Conclusion: Coupled with craniotomy, tumor removal was successfully carried out in 11 patients with JNAs, which showed large lateral extension. Our surgical strategy is a safe and effective approach for the removal of JNAs with infratemporal fossa extension. ß 2014 Elsevier Ireland Ltd. All rights reserved.
Keywords: Juvenile nasopharyngeal angiofibroma Sphenopalatine foramen Infratemporal fossa Craniotomy Orbito-zygomatic approach
1. Introduction Juvenile nasopharyngeal angiofibroma (JNA) is a rare benign tumor that primarily occurs in adolescents and young adults. It represents 0.05–0.5% of all head and neck tumors [1–3]. JNA grows
* Corresponding author at: Department of Otolaryngology and Head and Neck Surgery, Tokyo Medical and Dental University, Bunkyo-ku, Yushima 1-5-45, Tokyo 113-8519, Japan. Tel.: +81 3 5803 5304; fax: +81 3 3813 2134. E-mail address: [email protected] (A. Tsunoda). http://dx.doi.org/10.1016/j.anl.2014.02.009 0385-8146/ß 2014 Elsevier Ireland Ltd. All rights reserved.
aggressively with a huge blood supply. The initial therapy is a surgery, and complete removal of the tumor is required. Currently, endonasal endoscopic resection of JNA has become popular due to its low morbidity. However, surgical resection of a large JNA remains a formidable challenge for the surgeon because of its infiltrative nature and hypervascularity. Removal of JNAs with wide lateral extension is especially difficult by endonasal endoscopic surgery alone. Therefore, safe and total removal of such tumors still requires an extended skull base surgery using a wide surgical field. Moreover, JNAs usually affect adolescent males, so the surgeon must pay attention to cosmetic and developmental problems, such as facial deformities.
M. Yamada et al. / Auris Nasus Larynx 41 (2014) 359–363
360 Table 1 Case series of this study. Case No
Age
Initial/secondary
Extension Medial
1 2 3 4 5 6 7 8 9 10 11
12 20 17 8 13 27 32 15 17 15 19
Secondary Initial Secondary Initial Secondary Initial Initial Initial Secondary Initial Secondary
Preoperative staging Anterior
Superior
NP
ES
SS
MS
OB
+ + + + + + + + + + +
+ + + + + +
+ + + + + + +
+ + +
+ + +
+
+ + +
+
+
AF +
+ + +
We performed surgery on 11 cases of large JNAs with wide extension to the infratemporal fossa. The purpose of this study was to evaluate the treatment outcome of our surgery for such large JNAs. 2. Materials and methods From 2007 to 2012, we performed surgery on 11 cases of JNAs with wide extension to the infratemporal fossa (Table 1). All cases were male, and their mean age was 17.7 years (range: 8–32). Preoperative imaging, including contrast-enhanced computed tomography (CT) and magnetic resonance imaging (MRI), was performed. In accordance with the study of Vasily et al., tumor extension other than lateral extension, that is, to the infratemporal fossa, was carefully assessed (Fig. 1; Table 1) [4]. The patients’ profiles and their preoperative staging are shown in Table 1. Based on the imaging study, extension to the cavernous sinus was suspected in eight cases, middle cranial fossa in eight, anterior fossa in one, clivus in one, orbit in four, and infratemporal fossa in 11 cases. Therefore, three cases were diagnosed as Andrews’ Stage IVa and eight cases as IVb (Tables 1 and 2). Angiography showed all tumors being supplied by the internal maxillary artery. In addition, six tumors were supplied by the ascending pharyngeal artery, six by the facial artery, and 10 by the branches of the internal carotid artery (mainly from the ophthalmic artery). Embolization of the feeding arteries from the external carotid artery was carried out in all 11 cases at 24–72 h prior to
MF
CS
+
+ + +
+ + + + + +
+ +
+
CV
+
+ + +
Lateral
Inferior
PPF
AB
+ + + + + + + + + + +
+
+
IVb IVb IVb IVa IVa IVb IVb IVa IVb IVb IVb
Table 2 Staging of JNA (Andrews). Stage I II III
IV
Tumor limited to the nasopharynx and nasal cavity Tumor invading the pterygopalatine fossa or sinuses Tumor invading the inflatemporal fossa or orbital region (a) without intracranial involvement and (b) with extradural intracranial involvement Tumor with intradural intracranial involvement (a) without infiltration of cavernous sinus, pituitary fossa or optic chiasma (b) with infiltration of cavernous sinus, pituitary fossa or optic chiasma
surgery. The branches of the internal carotid artery were not embolized. 3. Results All the patients underwent surgery using a wide surgical field (Table 3). In all the 11 cases, coronal incision was applied and a facial dismasking flap was added to nine cases (unilateral 8, bilateral 1). Because of wide extension to the base of the maxillary sinus and alveolar bone, temporary section of the facial nerve and wide lateral skin incision were performed in Case 6. Thus, a wide surgical field was obtained, and the nerve was sutured after tumor removal. The external auditory canal was kept intact in all cases. Regarding osteotomy of the facial skull, the orbito-zygomatic approach was basically applied. In Case 4, Le Fort I osteotomy
Fig. 1. A case of JNA with wide lateral extension developed in a 17-year-old boy (Case 9). (a) axial, (b) coronal. (c) sagittal image. The tumor originated from the sphenopalatine foramen and extended to the infratemporal fossa, as well as the inferior orbital fissure, orbit, foramen rotundum, internal carotid artery, cavernous sinus, and sphenoid sinus. The tumor also protruded into the middle cranial fossa and extended intracranially. Therefore, this case was diagnosed as IVb according to Andrews’ classification.
M. Yamada et al. / Auris Nasus Larynx 41 (2014) 359–363
361
Table 3 Surgical outcome of this series. Case no.
Surgical approach Skin incision
Facial osteotomy
Craniotomy
1 2 3 4 5 6 7 8 9 10 11
Coronal + uniFD Coronal + biFD Coronal Coronal + uniFD Coronal + uniFD Coronal + wide lateral Coronal + uniFD Coronal + uniFD Coronal + uniFD Coronal + uniFD Coronal + uniFD
OZ OZ OZ OZ + Le FortI Z OZ + Partial madibulotomy OZ + Partial madiburectomy OZ OZ + Partial madibulotomy OZ OZ
Lateral Frontolateral Frontolateral Lateral Lateral Lateral Frontolateral Lateral Lateral Frontolateral Lateral
Postoperative staging
Bleeding
Operation time
Tumor resection
Tumor recurrence
IIIb IIIb IIIb IIIb IIIb IIIb IIIb IIIb IVb IIIb IIIb
8547 ml 7437 ml 2490 ml 1234 ml 950 ml 2972 ml 4446 ml 2595 ml 5140 ml 4060 ml 5500 ml
17 h 19 h 16 h 16 h 7h 16 h 17 h 15 h 25 h 18 h 16 h
Complete Complete Subtotal Complete Complete Complete Complete Complete Complete Complete Complete
+
54 min 40 min 22 min 37 min 52 min 27 min 06 min 54 min 24 min 25 min 25 min
+
Fig. 2. Surgical view after total removal of the tumor in Case 9. Because of wide extension, this patient required ipsilateral facial dismaking flap and temporary resection of facial nerve and mandibular ramus (MR). Wide surgical view of the infratemporal fossa was then obtained. Most part of pterygoid process was removed, and the maxillary sinus, sphenoid sinus and nasopharynx were fully exposed. Lateral craniotomy was also performed, and the tumor was removed under this sufficient surgical field. Tumor was tightly attached to dura and cavernous sinus (arrow); however, it was stripped safely. *: nasopharynx; M: body of mandible; MR: mandibular ramus, turned over; T: main part of the tumor in the infratemporal fossa; TL: temporal lobe.
under midfacial degloving was performed simultaneously because the tumor extended widely to the contralateral nasopharynx. In Cases 6 and 9, temporary transection of the mandibular ramus was added (Fig. 2). In these three cases, the separated bones were returned and fixed with titanium plates. In Case 7, resection of the coronoid process of the mandible was added. However, a temporoparietal fascia-pericranial flap was used for packing dead space, so the coronoid process was not reconstructed in this case. The average surgical time was 17 h 6 min. The average blood loss was 4125 ml, and mean transfusions of 14.7 units of packed red blood cells, and 6.1 units of fresh frozen plasma were given to the patients. Intraoperatively, only one case showed tumor infiltration into the cavernous sinus. The rest of the tumors were separated carefully from the cavernous sinus or dura. The tumors seemed to be tightly adherent to the dura mater; therefore, they were accurately diagnosed as Stage IIIb. The mean follow-up period was 29.6 months (range: 6–72). Complete removal of JNA was achieved in 10 cases. In Case 3, excessive bleeding from branches of the internal carotid artery in the medial part of the pterygoid process was difficult to control. Such a bleeding was temporarily stopped by the application of absorbable cotton soaked with fibrin glue. Then, the tumor was removed carefully from the carotid artery using bipolar
electro-coagulator. As a result, subtotal removal of the tumor was carried out. In one secondary case (Case 1), recurrence of the tumor was found in the parapharyngeal space. Multiple recurrences were noted in two cases (Cases 1 and 3), and the residual tumor was too small to find during surgery. These two cases underwent successive radiotherapy. No mortality was noted after the surgery. Concerning morbidity, mild trismus developed in all cases; however, this symptom gradually ceased and no severe trouble in mastication was observed (Table 4). Other complications included hyposmia, temporary failing vision, and CSF leak, but these symptoms were transient. Facial palsy was observed in two cases. In one case, temporal section of the frontal branch of the facial nerve
Table 4 Complications after the surgery. Complications
No of patients (%)
Temporary trismus Cheek numbness Facial palsy Temporary failing vision Hyposmia CSF leak
11 3 2 2 1 1
(100) (27) (18) (18) (9) (9)
362
M. Yamada et al. / Auris Nasus Larynx 41 (2014) 359–363
Fig. 3. Postoperative MR image and face 2 years after the surgery in Case 9. No tumor recurrence is observed in this image. Nevertheless, a scar after the circumperipalpebral skin incision is noted, and H-B grade III palsy is persistent. The patient and his family are content with his postoperative looks.
was needed for safe removal of the tumor (Case 9). Even after the nerve was sutured, forehead movement was weak and HouseBrackmann (H-B) grade III palsy was noted. In another case (Case 6) who required temporal section of the facial nerve, total facial palsy (H-B grade VI) developed immediately after the surgery. The palsy gradually improved to H-B grade III after a year. In three cases (Cases 7, 8 and 10), the tumors were mainly around the foramen rotundum and involved the maxillary nerve. The maxillary nerve was sacrificed, and cheek numbness persisted. 4. Discussion The effectiveness of radiation therapy has been reported for unresectable or postoperative residual tumors. However, the wellknown long-term complications of radiation therapy, such as secondary malignancies, endocrine hypofunction, and cataracts, must be taken into account [5]. At present, the initial therapy for JNAs is surgery [6,7]. Several surgical approaches have been reported for the removal of JNAs, but an appropriate surgical approach should be decided on the basis of tumor size and location, as well as bleeding control and developmental problems. Transnasal and transantral removals are less invasive approaches, and the endonasal endoscopic removal has been applied to stage IIIb JNA [8]. In cases of JNAs without pericavernous sinus involvement and/or enhancement of the ICA, the transfacial approach alone was sufficient for the removal of these tumors without craniotomy [9]. Other reports have even suggested that JNAs with infratemporal fossa extension could be removed by transantral endoscopic management with additional removal of the posterior wall of the maxillary sinus [10]. Using a multi-angle infratemporal fossa approach, such as a combination of endonasal, Caldwell-Luc, and transtemporal/Gillies approaches, JNAs with lateral extension can be accessible [11]. However, these approaches cannot provide a wide surgical view of the lateral part of the infratemporal fossa, middle fossa, and cavernous sinus. The endoscopic endonasal approach is limited to JNAs without lateral extension; therefore, removal of laterally extending JNAs is still difficult at present [12]. The present 11 cases of JNA with infratemporal fossa extension also showed extensions to the cavernous sinus and/or middle cranial fossa in the preoperative imaging study. For the purpose of safe removal of these huge JNAs, we applied a suitable surgical approach which can manage both intracranial lesions and
involvement of the infratemporal fossa simultaneously. Endonasal or transantral approach alone seemed difficult for this purpose even with the use of endoscope. Lateral rhinotomy coupled with the maxillary swing approach may broaden the surgical field to the infratemporal fossa, as well as the nasopharyx and paranasal sinus at the same time [13,14]. However, in the management of the far lateral part of the infratemporal fossa and/or intracranial extension, this approach also seemed insufficient for safe removal of the tumor. In addition, this approach requires Weber’s skin incision. Development of scar on the face is unavoidable and seems unsuitable for adolescent patients. Through the anatomical and cadaveric assessments, we were convinced that a sufficient surgical field with minimum morbidity could be obtained by a lateral approach, such as a coronal skin incision with or without facial dismasking, coupled with the orbito-zygomatic approach (Figs. 2 and 3) [15]. Even with the addition of the facial dismasking flap, incisions on the face are limited to circumpalpebral incision with almost negligible development of facial scars; therefore, our technique poses a greater advantage compared to the frontal approach, such as lateral rhinotomy or maxillary swing approach (Fig. 3) [16]. In addition to this, stripping of tumor from the cavenous sinus and/or root of pterygoid process is potentially difficult in the removal of such a huge invasive angiofibroma. These tumors suffer blood loss mainly from the internal carotid artery in these surgical sites; however, embolization of the internal carotid artery and its branches has a high risk of severe sequelae. The JNA tends to show severe bleeding without embolization of the feeding artery, so hemostasis is very difficult. However, the lateral approach provided sufficient surgical field even in these sites (Figs. 2 and 4). As a result, 10 out of 11 cases underwent total resection and one case of subtotal resection by this approach with minimum damages to the facial skin. Therefore, we basically applied the lateral approach instead of the frontal approach. Although this approach offers wide and safe surgical view, a certain case with massive tumor invasion, such as involvement of the brain, may entail difficult surgical removal. Therefore, a thorough estimation of the imaging study is critical before the surgical removal of extended JNA. Concerning the complications, we temporarily cut the facial nerve for safe total removal of the tumor in two cases because of lower extension. We cut the two branches distal to the bifurcation of the facial nerve trunk and sutured them after tumor removal. As
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applied. This technique seems promising; however, data are not shown and are reported elsewhere. 5. Conclusion To accomplish the total removal of large laterally extended JNA with a good surgical field, we recommend coronal skin incision with or without a facial dismasking flap for skin incision and the orbito-zygomatic approach for osteotomy. From our experience, the lateral approach for large JNAs provides a safe and adequate surgical view with minimum morbidity. This type of surgical technique seems invasive, but there is no mortality and all the patients returned to normal life. Therefore, we recommend our strategy for such huge JNAs with infratemporal fossa extension. References
Fig. 4. Comparison of each approach for the removal of JNA with extension to the infratemporal fossa. Endoscopic endonasal approach (red dot) and frontal approach (green dot) offer a limited surgical field in the medial and posterior borders of the tumor; whereas, the lateral approach offers wide and sufficient surgical field.
a result, facial palsy had developed inevitably in these cases. Facial dismasking flap offers wide surgical field of the upper 2/3 part of the face; however, the lower 1/3 cannot be exposed by this method [18]. For removal of the lower part of the tumor with less morbidity, an endoscopic-assisted procedure may be promising, and we currently plan to apply such technique [10,11]. Based on enhanced MRI, our preoperative diagnoses of the present cases were Stage IVa and IVb. As mentioned, these tumors were separated safely from the cavernous sinus or dura under the microscope with a sufficient surgical field, except one case (Case 9). As a result, preoperative staging of most of the cases was overestimated, and a similar experience has been reported elsewhere [17]. In other words, the surgery was performed safely under the wide surgical field even with the necessary manipulation around the cavernous sinus in eight out of 11 cases. Nevertheless, such an overestimation in preoperative staging may occur, and we still advocate our surgical strategy. Concerning tumor recurrence, most can be attributed to the residual tumor. The average rate of residual tumors in major JNAs surgery was 32%. The average rate of residual tumors in JNAs with intracranial extension was 40–50% one year after the surgery [19,20]. Young-onset, invasion to the sphenoid sinus, cavernous sinus, and clivus, and blood supply from the internal carotid artery are also high risk factors for residual tumors or recurrence [17,21,22]. In such cases with residual tumors or recurrence, additional surgery might be risky, so the postoperative radiotherapy plays an important role to treat residual lesions [5]. In our study, however, total removal of the tumor was carried out in 10 out of 11 cases, even including the five residual cases. Huge blood loss was recorded in most of our cases and could be inevitable in the removal of large tumors. Hence prevention of blood loss may be managed by more effective preoperative embolization. Currently, direct embolization to the tumor is being
[1] Gruber B, Kron TK, Goldman ME. Nasopharyngeal angiofibroma in two young children. Otolaryngol Head Neck Surg 1985;93:803–6. [2] Krause CJ, Baker CR. Extended transantral approach to pterygomaxillary tumors. Ann Otolaryngol 1982;91:391–8. [3] Tsunoda A, Ishikawa N, Kohda H, Komatsuzaki A. Juvenile angiofibroma limited to the sphenoid sinus. J Otolaryngol 1998;27:37–9. [4] Vasily AC, Denis AG, Dmitry NK, Vitaly VR, Sergey BY, Sergey RA. Advanced craniofacial juvenile nasopharyngeal angiofibroma. Description of surgical series, case report, and review of literature. Acta Neurochir 2011;153:499–508. [5] Suvi R, Jaana H, Jyrki V, Mika N, Matti P, Sanna MK, et al. The changing surgical management of juvenile nasopharyngeal angiofibroma. Eur Arch Otorhinolaryngol 2011;268:599–607. [6] Kuppersmith RB, Teh BS, Donovan DT. The use of intensity modurated radiotherapy for the treatment of extensive and recurrent juvenile angiofibroma. Int J Pediatr Otorhinolaryngol 2000;52:261–8. [7] Deguchi K, Fukuiwa T, Saito K, Kurono K. Application of cyberknife for the treatment of juvenile nasopharyngeal angiofibroma: a case report. Auris Nasus Larynx 2002;29:395–400. [8] Nishiike S, Shikina T, Maeda H, Hio S, Inohara H. Juvenile nasopharyngeal angiofibroma – evaluation of the invasion of the pterygoid canal. Nippon Jibiinnkouka Gakkai Kaiho (Tokyo) 2012;115:965–70. [9] Asser AE, Elsharawy MK, Ali T, Ahmed Z, Mohamed K. Juvenile nasopharyngeal angiofibroma with intracranial extension: analysis of 23 Egyptian patients. Int J Pediatr Otorhinolaryngol 2010;74:755–9. [10] Mohamed AK, Sameh MR. Endoscopic assisted antral window approach for type nasopharyngeal angiofibroma with inflatemporal fossa extension. Int J Pediatr Otorhinolaryngol 2008;72:1855–60. [11] Eloy JA, Murray KP, Friedel ME, Tessema B, Liu JK. Graduated endoscopic multiangle approach for access to the infratemporal fossa: a cadaveric study with clinical correlates. Otolaryngol Head Neck Surg 2012;147:369–78. [12] Piero N, Andrea BV, Davide F, Sylvie N, Arkadi Y, Marco B, et al. Endoscopic surgery for juvenile angiofibroma: a critical review of indications after 46 cases. Am J Rhinol Allergy 2010;24:e67–72. [13] Sumi T, Tsunoda A, Shirakura S, Kishimoto S. Partial maxillary swing approach for removal of the tumors in the retromaxillary area. Auris Nasus Larynx 2009;36:567–70. [14] Wei WI, Lam KH, Sham JS. New approach to the nasopharynx: the maxillary swing approach. Head Neck 1991;13:200–7. [15] Okada R, Tsunoda A, Momiyama N, Kishine N, Kitamura K, Kishimoto S, et al. Thiel’s method of embalming and its usefulness in surgical assessments. Nippon Jibiinnkouka Gakkai Kaiho (Tokyo) 2012;115:791–4. [16] Yamada M, Tsunoda A, Hagino K, Aoyagi M, Yano T, Kishimoto S, et al. Surgical management of large juvenile nasopharyngeal angiofibroma invading the inflatemporal fossa with intracranial extradural parasellar involvement in an 8-year-old boy. Auris Nasus Larynx 2012;39:341–4. [17] Giovanni D, Davide TP, Richard JH, Cristina A. Juvenile nasopharyngeal angiofibroma: evaluation and surgical management of advanced disease. Otolaryngol Head Neck Surg 2008;138:581–6. [18] Koda H, Tsunoda A, Iida H, Akita K, Kishimoto S. Facial dismasking flap for removal of tumors in the craniofacial region. Laryngoscope 2007;117:1533–8. [19] Philippe H, Guillaume L, Rene C, Didier S, Patrice TBH. Long-term follow-up of juvenile nasopharyngeal angiofibromas: analysis of recurrences. Laryngoscope 1999;109:140–7. [20] Glad H, Vainer B, Buchwald C, Peterson BL, Theilgaard SA, Bonvin P, et al. Juvenile nasopharyngeal angiofibromas in Denmark 1981–2003: diagnosis, incidence, and treatment. Acta Otolaryngol 2007;127:292–9. [21] Tyagi I, Syal R, Goyal A. Recurrent and residural juvenile angiofibromas. J Laryngol Otol 2007;121:460–7. [22] Karin P, Miriam RC, Bjorn P, Caterina F. Juvenile nasopharyngeal angiofibroma: long-term results in preoperative embolized and non-embolized patients. Acta Otolaryngol 2002;122:96–100.
Contents lists available at ScienceDirect
Auris Nasus Larynx journal homepage: www.elsevier.com/locate/anl
Surgery for juvenile nasopharyngeal angiofibroma with lateral extension to the infratemporal fossa Masato Yamada a, Atsunobu Tsunoda a,*, Takao Tokumaru a, Masaru Aoyagi b, Yoshihisa Kawano b, Tomoyuki Yano c, Seiji Kishimoto d a
Department of Otolaryngology, Tokyo Medical and Dental University, Japan Department of Neurosurgery, Tokyo Medical and Dental University, Japan Department of Plastic and Reconstructive Surgery, Tokyo Medical and Dental University, Japan d Department of Head & Neck Surgery, Tokyo Medical and Dental University, Japan b c
A R T I C L E I N F O
A B S T R A C T
Article history: Received 20 May 2013 Accepted 27 February 2014 Available online 28 March 2014
Objective: The study aimed to assess the usefulness of skull base surgery for large juvenile nasopharyngeal angiofibroma (JNA) with lateral extension to the infratemporal fossa. Materials and methods: Eleven cases were enrolled for this study, and the mean age was 17.7 years old (range: 8–32). Six out of 11 cases underwent surgery as an initial treatment, and the other five underwent secondary surgery after initial surgery or radiotherapy in other institutions. The range of extension of tumor, feeding arteries, surgical approach, and treatment outcome were estimated. Results: All tumors originated from the sphenopalatine foramen. Based on the imaging study, there was extension to the cavernous sinus observed in eight cases, as well as to the middle cranial fossa (8), orbit (4), and anterior cranial fossa (1). These tumors were diagnosed as Andrews’ Stage IVa (3) and IVb (8). However, infiltration into the cavernous sinus was observed in one case only during surgery. Ten tumors were separated carefully from the cavernous sinus or dura and were accurately diagnosed as Stage IIIb. In all cases, the main arterial feeders of the JNAs were branches of the external carotid artery, which were embolized prior to surgery. However, 10 cases were also fed by branches of the internal carotid artery (branches of the ophthalmic artery), in which these arteries could not be embolized. Coronal skin incision (1) and a facial dismasking flap (9) were used, and in one case, wide lateral skin incision with temporary incision of the facial nerve was applied. The orbito-zygomatic approach and its modification was applied to all the cases. Fronto-lateral craniotomy was applied in four cases and lateral craniotomy in seven cases. Total resection was achieved in 10 cases and subtotal resection in one case. No mortality was noted in this series. Temporal trismus was observed in all cases which subsided gradually. Cheek numbness and facial palsy were observed in three and two cases, respectively. Conclusion: Coupled with craniotomy, tumor removal was successfully carried out in 11 patients with JNAs, which showed large lateral extension. Our surgical strategy is a safe and effective approach for the removal of JNAs with infratemporal fossa extension. ß 2014 Elsevier Ireland Ltd. All rights reserved.
Keywords: Juvenile nasopharyngeal angiofibroma Sphenopalatine foramen Infratemporal fossa Craniotomy Orbito-zygomatic approach
1. Introduction Juvenile nasopharyngeal angiofibroma (JNA) is a rare benign tumor that primarily occurs in adolescents and young adults. It represents 0.05–0.5% of all head and neck tumors [1–3]. JNA grows
* Corresponding author at: Department of Otolaryngology and Head and Neck Surgery, Tokyo Medical and Dental University, Bunkyo-ku, Yushima 1-5-45, Tokyo 113-8519, Japan. Tel.: +81 3 5803 5304; fax: +81 3 3813 2134. E-mail address: [email protected] (A. Tsunoda). http://dx.doi.org/10.1016/j.anl.2014.02.009 0385-8146/ß 2014 Elsevier Ireland Ltd. All rights reserved.
aggressively with a huge blood supply. The initial therapy is a surgery, and complete removal of the tumor is required. Currently, endonasal endoscopic resection of JNA has become popular due to its low morbidity. However, surgical resection of a large JNA remains a formidable challenge for the surgeon because of its infiltrative nature and hypervascularity. Removal of JNAs with wide lateral extension is especially difficult by endonasal endoscopic surgery alone. Therefore, safe and total removal of such tumors still requires an extended skull base surgery using a wide surgical field. Moreover, JNAs usually affect adolescent males, so the surgeon must pay attention to cosmetic and developmental problems, such as facial deformities.
M. Yamada et al. / Auris Nasus Larynx 41 (2014) 359–363
360 Table 1 Case series of this study. Case No
Age
Initial/secondary
Extension Medial
1 2 3 4 5 6 7 8 9 10 11
12 20 17 8 13 27 32 15 17 15 19
Secondary Initial Secondary Initial Secondary Initial Initial Initial Secondary Initial Secondary
Preoperative staging Anterior
Superior
NP
ES
SS
MS
OB
+ + + + + + + + + + +
+ + + + + +
+ + + + + + +
+ + +
+ + +
+
+ + +
+
+
AF +
+ + +
We performed surgery on 11 cases of large JNAs with wide extension to the infratemporal fossa. The purpose of this study was to evaluate the treatment outcome of our surgery for such large JNAs. 2. Materials and methods From 2007 to 2012, we performed surgery on 11 cases of JNAs with wide extension to the infratemporal fossa (Table 1). All cases were male, and their mean age was 17.7 years (range: 8–32). Preoperative imaging, including contrast-enhanced computed tomography (CT) and magnetic resonance imaging (MRI), was performed. In accordance with the study of Vasily et al., tumor extension other than lateral extension, that is, to the infratemporal fossa, was carefully assessed (Fig. 1; Table 1) [4]. The patients’ profiles and their preoperative staging are shown in Table 1. Based on the imaging study, extension to the cavernous sinus was suspected in eight cases, middle cranial fossa in eight, anterior fossa in one, clivus in one, orbit in four, and infratemporal fossa in 11 cases. Therefore, three cases were diagnosed as Andrews’ Stage IVa and eight cases as IVb (Tables 1 and 2). Angiography showed all tumors being supplied by the internal maxillary artery. In addition, six tumors were supplied by the ascending pharyngeal artery, six by the facial artery, and 10 by the branches of the internal carotid artery (mainly from the ophthalmic artery). Embolization of the feeding arteries from the external carotid artery was carried out in all 11 cases at 24–72 h prior to
MF
CS
+
+ + +
+ + + + + +
+ +
+
CV
+
+ + +
Lateral
Inferior
PPF
AB
+ + + + + + + + + + +
+
+
IVb IVb IVb IVa IVa IVb IVb IVa IVb IVb IVb
Table 2 Staging of JNA (Andrews). Stage I II III
IV
Tumor limited to the nasopharynx and nasal cavity Tumor invading the pterygopalatine fossa or sinuses Tumor invading the inflatemporal fossa or orbital region (a) without intracranial involvement and (b) with extradural intracranial involvement Tumor with intradural intracranial involvement (a) without infiltration of cavernous sinus, pituitary fossa or optic chiasma (b) with infiltration of cavernous sinus, pituitary fossa or optic chiasma
surgery. The branches of the internal carotid artery were not embolized. 3. Results All the patients underwent surgery using a wide surgical field (Table 3). In all the 11 cases, coronal incision was applied and a facial dismasking flap was added to nine cases (unilateral 8, bilateral 1). Because of wide extension to the base of the maxillary sinus and alveolar bone, temporary section of the facial nerve and wide lateral skin incision were performed in Case 6. Thus, a wide surgical field was obtained, and the nerve was sutured after tumor removal. The external auditory canal was kept intact in all cases. Regarding osteotomy of the facial skull, the orbito-zygomatic approach was basically applied. In Case 4, Le Fort I osteotomy
Fig. 1. A case of JNA with wide lateral extension developed in a 17-year-old boy (Case 9). (a) axial, (b) coronal. (c) sagittal image. The tumor originated from the sphenopalatine foramen and extended to the infratemporal fossa, as well as the inferior orbital fissure, orbit, foramen rotundum, internal carotid artery, cavernous sinus, and sphenoid sinus. The tumor also protruded into the middle cranial fossa and extended intracranially. Therefore, this case was diagnosed as IVb according to Andrews’ classification.
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Table 3 Surgical outcome of this series. Case no.
Surgical approach Skin incision
Facial osteotomy
Craniotomy
1 2 3 4 5 6 7 8 9 10 11
Coronal + uniFD Coronal + biFD Coronal Coronal + uniFD Coronal + uniFD Coronal + wide lateral Coronal + uniFD Coronal + uniFD Coronal + uniFD Coronal + uniFD Coronal + uniFD
OZ OZ OZ OZ + Le FortI Z OZ + Partial madibulotomy OZ + Partial madiburectomy OZ OZ + Partial madibulotomy OZ OZ
Lateral Frontolateral Frontolateral Lateral Lateral Lateral Frontolateral Lateral Lateral Frontolateral Lateral
Postoperative staging
Bleeding
Operation time
Tumor resection
Tumor recurrence
IIIb IIIb IIIb IIIb IIIb IIIb IIIb IIIb IVb IIIb IIIb
8547 ml 7437 ml 2490 ml 1234 ml 950 ml 2972 ml 4446 ml 2595 ml 5140 ml 4060 ml 5500 ml
17 h 19 h 16 h 16 h 7h 16 h 17 h 15 h 25 h 18 h 16 h
Complete Complete Subtotal Complete Complete Complete Complete Complete Complete Complete Complete
+
54 min 40 min 22 min 37 min 52 min 27 min 06 min 54 min 24 min 25 min 25 min
+
Fig. 2. Surgical view after total removal of the tumor in Case 9. Because of wide extension, this patient required ipsilateral facial dismaking flap and temporary resection of facial nerve and mandibular ramus (MR). Wide surgical view of the infratemporal fossa was then obtained. Most part of pterygoid process was removed, and the maxillary sinus, sphenoid sinus and nasopharynx were fully exposed. Lateral craniotomy was also performed, and the tumor was removed under this sufficient surgical field. Tumor was tightly attached to dura and cavernous sinus (arrow); however, it was stripped safely. *: nasopharynx; M: body of mandible; MR: mandibular ramus, turned over; T: main part of the tumor in the infratemporal fossa; TL: temporal lobe.
under midfacial degloving was performed simultaneously because the tumor extended widely to the contralateral nasopharynx. In Cases 6 and 9, temporary transection of the mandibular ramus was added (Fig. 2). In these three cases, the separated bones were returned and fixed with titanium plates. In Case 7, resection of the coronoid process of the mandible was added. However, a temporoparietal fascia-pericranial flap was used for packing dead space, so the coronoid process was not reconstructed in this case. The average surgical time was 17 h 6 min. The average blood loss was 4125 ml, and mean transfusions of 14.7 units of packed red blood cells, and 6.1 units of fresh frozen plasma were given to the patients. Intraoperatively, only one case showed tumor infiltration into the cavernous sinus. The rest of the tumors were separated carefully from the cavernous sinus or dura. The tumors seemed to be tightly adherent to the dura mater; therefore, they were accurately diagnosed as Stage IIIb. The mean follow-up period was 29.6 months (range: 6–72). Complete removal of JNA was achieved in 10 cases. In Case 3, excessive bleeding from branches of the internal carotid artery in the medial part of the pterygoid process was difficult to control. Such a bleeding was temporarily stopped by the application of absorbable cotton soaked with fibrin glue. Then, the tumor was removed carefully from the carotid artery using bipolar
electro-coagulator. As a result, subtotal removal of the tumor was carried out. In one secondary case (Case 1), recurrence of the tumor was found in the parapharyngeal space. Multiple recurrences were noted in two cases (Cases 1 and 3), and the residual tumor was too small to find during surgery. These two cases underwent successive radiotherapy. No mortality was noted after the surgery. Concerning morbidity, mild trismus developed in all cases; however, this symptom gradually ceased and no severe trouble in mastication was observed (Table 4). Other complications included hyposmia, temporary failing vision, and CSF leak, but these symptoms were transient. Facial palsy was observed in two cases. In one case, temporal section of the frontal branch of the facial nerve
Table 4 Complications after the surgery. Complications
No of patients (%)
Temporary trismus Cheek numbness Facial palsy Temporary failing vision Hyposmia CSF leak
11 3 2 2 1 1
(100) (27) (18) (18) (9) (9)
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Fig. 3. Postoperative MR image and face 2 years after the surgery in Case 9. No tumor recurrence is observed in this image. Nevertheless, a scar after the circumperipalpebral skin incision is noted, and H-B grade III palsy is persistent. The patient and his family are content with his postoperative looks.
was needed for safe removal of the tumor (Case 9). Even after the nerve was sutured, forehead movement was weak and HouseBrackmann (H-B) grade III palsy was noted. In another case (Case 6) who required temporal section of the facial nerve, total facial palsy (H-B grade VI) developed immediately after the surgery. The palsy gradually improved to H-B grade III after a year. In three cases (Cases 7, 8 and 10), the tumors were mainly around the foramen rotundum and involved the maxillary nerve. The maxillary nerve was sacrificed, and cheek numbness persisted. 4. Discussion The effectiveness of radiation therapy has been reported for unresectable or postoperative residual tumors. However, the wellknown long-term complications of radiation therapy, such as secondary malignancies, endocrine hypofunction, and cataracts, must be taken into account [5]. At present, the initial therapy for JNAs is surgery [6,7]. Several surgical approaches have been reported for the removal of JNAs, but an appropriate surgical approach should be decided on the basis of tumor size and location, as well as bleeding control and developmental problems. Transnasal and transantral removals are less invasive approaches, and the endonasal endoscopic removal has been applied to stage IIIb JNA [8]. In cases of JNAs without pericavernous sinus involvement and/or enhancement of the ICA, the transfacial approach alone was sufficient for the removal of these tumors without craniotomy [9]. Other reports have even suggested that JNAs with infratemporal fossa extension could be removed by transantral endoscopic management with additional removal of the posterior wall of the maxillary sinus [10]. Using a multi-angle infratemporal fossa approach, such as a combination of endonasal, Caldwell-Luc, and transtemporal/Gillies approaches, JNAs with lateral extension can be accessible [11]. However, these approaches cannot provide a wide surgical view of the lateral part of the infratemporal fossa, middle fossa, and cavernous sinus. The endoscopic endonasal approach is limited to JNAs without lateral extension; therefore, removal of laterally extending JNAs is still difficult at present [12]. The present 11 cases of JNA with infratemporal fossa extension also showed extensions to the cavernous sinus and/or middle cranial fossa in the preoperative imaging study. For the purpose of safe removal of these huge JNAs, we applied a suitable surgical approach which can manage both intracranial lesions and
involvement of the infratemporal fossa simultaneously. Endonasal or transantral approach alone seemed difficult for this purpose even with the use of endoscope. Lateral rhinotomy coupled with the maxillary swing approach may broaden the surgical field to the infratemporal fossa, as well as the nasopharyx and paranasal sinus at the same time [13,14]. However, in the management of the far lateral part of the infratemporal fossa and/or intracranial extension, this approach also seemed insufficient for safe removal of the tumor. In addition, this approach requires Weber’s skin incision. Development of scar on the face is unavoidable and seems unsuitable for adolescent patients. Through the anatomical and cadaveric assessments, we were convinced that a sufficient surgical field with minimum morbidity could be obtained by a lateral approach, such as a coronal skin incision with or without facial dismasking, coupled with the orbito-zygomatic approach (Figs. 2 and 3) [15]. Even with the addition of the facial dismasking flap, incisions on the face are limited to circumpalpebral incision with almost negligible development of facial scars; therefore, our technique poses a greater advantage compared to the frontal approach, such as lateral rhinotomy or maxillary swing approach (Fig. 3) [16]. In addition to this, stripping of tumor from the cavenous sinus and/or root of pterygoid process is potentially difficult in the removal of such a huge invasive angiofibroma. These tumors suffer blood loss mainly from the internal carotid artery in these surgical sites; however, embolization of the internal carotid artery and its branches has a high risk of severe sequelae. The JNA tends to show severe bleeding without embolization of the feeding artery, so hemostasis is very difficult. However, the lateral approach provided sufficient surgical field even in these sites (Figs. 2 and 4). As a result, 10 out of 11 cases underwent total resection and one case of subtotal resection by this approach with minimum damages to the facial skin. Therefore, we basically applied the lateral approach instead of the frontal approach. Although this approach offers wide and safe surgical view, a certain case with massive tumor invasion, such as involvement of the brain, may entail difficult surgical removal. Therefore, a thorough estimation of the imaging study is critical before the surgical removal of extended JNA. Concerning the complications, we temporarily cut the facial nerve for safe total removal of the tumor in two cases because of lower extension. We cut the two branches distal to the bifurcation of the facial nerve trunk and sutured them after tumor removal. As
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applied. This technique seems promising; however, data are not shown and are reported elsewhere. 5. Conclusion To accomplish the total removal of large laterally extended JNA with a good surgical field, we recommend coronal skin incision with or without a facial dismasking flap for skin incision and the orbito-zygomatic approach for osteotomy. From our experience, the lateral approach for large JNAs provides a safe and adequate surgical view with minimum morbidity. This type of surgical technique seems invasive, but there is no mortality and all the patients returned to normal life. Therefore, we recommend our strategy for such huge JNAs with infratemporal fossa extension. References
Fig. 4. Comparison of each approach for the removal of JNA with extension to the infratemporal fossa. Endoscopic endonasal approach (red dot) and frontal approach (green dot) offer a limited surgical field in the medial and posterior borders of the tumor; whereas, the lateral approach offers wide and sufficient surgical field.
a result, facial palsy had developed inevitably in these cases. Facial dismasking flap offers wide surgical field of the upper 2/3 part of the face; however, the lower 1/3 cannot be exposed by this method [18]. For removal of the lower part of the tumor with less morbidity, an endoscopic-assisted procedure may be promising, and we currently plan to apply such technique [10,11]. Based on enhanced MRI, our preoperative diagnoses of the present cases were Stage IVa and IVb. As mentioned, these tumors were separated safely from the cavernous sinus or dura under the microscope with a sufficient surgical field, except one case (Case 9). As a result, preoperative staging of most of the cases was overestimated, and a similar experience has been reported elsewhere [17]. In other words, the surgery was performed safely under the wide surgical field even with the necessary manipulation around the cavernous sinus in eight out of 11 cases. Nevertheless, such an overestimation in preoperative staging may occur, and we still advocate our surgical strategy. Concerning tumor recurrence, most can be attributed to the residual tumor. The average rate of residual tumors in major JNAs surgery was 32%. The average rate of residual tumors in JNAs with intracranial extension was 40–50% one year after the surgery [19,20]. Young-onset, invasion to the sphenoid sinus, cavernous sinus, and clivus, and blood supply from the internal carotid artery are also high risk factors for residual tumors or recurrence [17,21,22]. In such cases with residual tumors or recurrence, additional surgery might be risky, so the postoperative radiotherapy plays an important role to treat residual lesions [5]. In our study, however, total removal of the tumor was carried out in 10 out of 11 cases, even including the five residual cases. Huge blood loss was recorded in most of our cases and could be inevitable in the removal of large tumors. Hence prevention of blood loss may be managed by more effective preoperative embolization. Currently, direct embolization to the tumor is being
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![[Juvenile nasopharyngeal angiofibroma with orbital extension].](/assets/img/hold.png)
